Obesity and Cancer Metastasis: Molecular and Translational Perspectives
Abstract
:Simple Summary
Abstract
1. Introduction
2. The Metastatic Cascade
3. Mechanisms Linking Adipose Tissue to the Metastatic Cascade
3.1. Adipocytes and Adipokines
3.2. Immune Cells and Inflammatory Factors
3.3. Angiogenesis
3.4. Metabolic Repogramming
3.5. Extracellular Matrix
3.6. Extracellular Vesicles
4. Targeting Metastasis through Adipose Tissue-Tumor Interactions
5. Targeting Metastasis via the Treatment of Obesity
6. Conclusions
Funding
Conflicts of Interest
References
- Steele, C.B.; Thomas, C.C.; Henley, S.J.; Massetti, G.M.; Galuska, D.A.; Agurs-Collins, T.; Puckett, M.; Richardson, L.C. Vital Signs: Trends in Incidence of Cancers Associated with Overweight and Obesity—United States, 2005–2014. MMWR Morb. Mortal. Wkly. Rep. 2017, 66, 1052–1058. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chan, D.S.M.; Vieira, A.R.; Aune, D.; Bandera, E.V.; Greenwood, D.C.; McTiernan, A.; Rosenblatt, D.N.; Thune, I.; Vieira, R.; Norat, T. Body mass index and survival in women with breast cancer—Systematic literature review and meta-analysis of 82 follow-up studies. Ann. Oncol. 2014, 25, 1901–1914. [Google Scholar] [CrossRef] [PubMed]
- Lengyel, E.; Makowski, L.; DiGiovanni, J.; Kolonin, M.G. Cancer as a Matter of Fat: The Crosstalk between Adipose Tissue and Tumors. Trends Cancer 2018, 4, 374–384. [Google Scholar] [CrossRef] [PubMed]
- Renehan, A.G.; Zwahlen, M.; Egger, M. Adiposity and cancer risk: New mechanistic insights from epidemiology. Nat. Rev. Cancer 2015, 15, 484–498. [Google Scholar] [CrossRef]
- Allott, E.H.; Masko, E.M.; Freedland, S.J. Obesity and prostate cancer: Weighing the evidence. Eur. Urol. 2013, 63, 800–809. [Google Scholar] [CrossRef] [Green Version]
- Huffman, D.M.; Johnson, M.S.; Watts, A.; Elgavish, A.; Eltoum, I.A.; Nagy, T.R. Cancer progression in the transgenic adenocarcinoma of mouse prostate mouse is related to energy balance, body mass, and body composition, but not food intake. Cancer Res. 2007, 67, 417–424. [Google Scholar] [CrossRef] [Green Version]
- Ewertz, M.; Jensen, M.B.; Gunnarsdóttir, K.Á.; Højris, I.; Jakobsen, E.H.; Nielsen, D.; Stenbygaard, L.E.; Tange, U.B.; Cold, S. Effect of obesity on prognosis after early-stage breast cancer. J. Clin. Oncol. 2011, 29, 25–31. [Google Scholar] [CrossRef]
- Kyrgiou, M.; Kalliala, I.; Markozannes, G.; Gunter, M.J.; Paraskevaidis, E.; Gabra, H.; Martin-Hirsch, P.; Tsilidis, K.K. Adiposity and cancer at major anatomical sites: Umbrella review of the literature. BMJ 2017, 356, 477. [Google Scholar] [CrossRef] [Green Version]
- O’Sullivan, J.; Lysaght, J.; Donohoe, C.L.; Reynolds, J.V. Obesity and gastrointestinal cancer: The interrelationship of adipose and tumour microenvironments. Nat. Rev. Gastroenterol. Hepatol. 2018, 15, 699–714. [Google Scholar] [CrossRef]
- Fang, X.; Wei, J.; He, X.; Lian, J.; Han, D.; An, P.; Zhou, T.; Liu, S.; Wang, F.; Min, J. Quantitative association between body mass index and the risk of cancer: A global Meta-analysis of prospective cohort studies. Int. J. Cancer 2018, 143, 1595–1603. [Google Scholar] [CrossRef] [Green Version]
- Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Welch, D.R.; Hurst, D.R. Defining the Hallmarks of Metastasis. Cancer Res. 2019, 79, 3011–3027. [Google Scholar] [CrossRef] [PubMed]
- Bakhoum, S.F.; Ngo, B.; Laughney, A.M.; Cavallo, J.A.; Murphy, C.J.; Ly, P.; Shah, P.; Sriram, R.K.; Watkins, T.B.K.; Taunk, N.K.; et al. Chromosomal instability drives metastasis through a cytosolic DNA response. Nature 2018, 553, 467–472. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ye, X.; Weinberg, R.A. Epithelial-Mesenchymal Plasticity: A Central Regulator of Cancer Progression. Trends Cell Biol. 2015, 25, 675–686. [Google Scholar] [CrossRef] [Green Version]
- Rankin, E.B.; Giaccia, A.J. Hypoxic control of metastasis. Science 2016, 352, 175–180. [Google Scholar] [CrossRef] [Green Version]
- Lamouille, S.; Xu, J.; Derynck, R. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 2014, 15, 178–196. [Google Scholar] [CrossRef] [Green Version]
- Zheng, X.; Carstens, J.L.; Kim, J.; Scheible, M.; Kaye, J.; Sugimoto, H.; Wu, C.-C.; LeBleu, V.S.; Kalluri, R. Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature 2015, 527, 525–530. [Google Scholar] [CrossRef] [Green Version]
- Fischer, K.R.; Durrans, A.; Lee, S.; Sheng, J.; Li, F.; Wong, S.T.C.; Choi, H.; El Rayes, T.; Ryu, S.; Troeger, J.; et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature 2015, 527, 472–476. [Google Scholar] [CrossRef]
- Lytle, N.K.; Barber, A.G.; Reya, T. Stem cell fate in cancer growth, progression and therapy resistance. Nat. Rev. Cancer 2018, 18, 669–680. [Google Scholar] [CrossRef]
- Fares, J.; Fares, M.Y.; Khachfe, H.H.; Salhab, H.A.; Fares, Y. Molecular principles of metastasis: A hallmark of cancer revisited. Signal Transduct. Target. Ther. 2020, 5, 1–17. [Google Scholar] [CrossRef]
- Pastushenko, I.; Brisebarre, A.; Sifrim, A.; Fioramonti, M.; Revenco, T.; Boumahdi, S.; Van Keymeulen, A.; Brown, D.; Moers, V.; Lemaire, S.; et al. Identification of the tumour transition states occurring during EMT. Nature 2018, 556, 463–468. [Google Scholar] [CrossRef] [PubMed]
- Jolly, M.K.; Ware, K.E.; Gilja, S.; Somarelli, J.A.; Levine, H. EMT and MET: Necessary or permissive for metastasis? Mol. Oncol. 2017, 11, 755–769. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fox, R.G.; Lytle, N.K.; Jaquish, D.V.; Park, F.D.; Ito, T.; Bajaj, J.; Koechlein, C.S.; Zimdahl, B.; Yano, M.; Kopp, J.L.; et al. Image-based detection and targeting of therapy resistance in pancreatic adenocarcinoma. Nature 2016, 534, 407–411. [Google Scholar] [CrossRef] [Green Version]
- Balic, M.; Lin, H.; Young, L.; Hawes, D.; Giuliano, A.; McNamara, G.; Datar, R.H.; Cote, R.J. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin. Cancer Res. 2006, 12, 5615–5621. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grillet, F.; Bayet, E.; Villeronce, O.; Zappia, L.; Lagerqvist, E.L.; Lunke, S.; Charafe-Jauffret, E.; Pham, K.; Molck, C.; Rolland, N.; et al. Circulating tumour cells from patients with colorectal cancer have cancer stem cell hallmarks in ex vivo culture. Gut 2017, 66, 1802–1810. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aktas, B.; Tewes, M.; Fehm, T.; Hauch, S.; Kimmig, R.; Kasimir-Bauer, S. Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res. 2009, 11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baccelli, I.; Schneeweiss, A.; Riethdorf, S.; Stenzinger, A.; Schillert, A.; Vogel, V.; Klein, C.; Saini, M.; Bäuerle, T.; Wallwiener, M.; et al. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat. Biotechnol. 2013, 31, 539–544. [Google Scholar] [CrossRef]
- Hermann, P.C.; Huber, S.L.; Herrler, T.; Aicher, A.; Ellwart, J.W.; Guba, M.; Bruns, C.J.; Heeschen, C. Distinct Populations of Cancer Stem Cells Determine Tumor Growth and Metastatic Activity in Human Pancreatic Cancer. Cell Stem Cell 2007, 1, 313–323. [Google Scholar] [CrossRef] [Green Version]
- Phi, L.T.H.; Sari, I.N.; Yang, Y.G.; Lee, S.H.; Jun, N.; Kim, K.S.; Lee, Y.K.; Kwon, H.Y. Cancer stem cells (CSCs) in drug resistance and their therapeutic implications in cancer treatment. Stem Cells Int. 2018, 2018. [Google Scholar] [CrossRef] [Green Version]
- Peinado, H.; Zhang, H.; Matei, I.R.; Costa-Silva, B.; Hoshino, A.; Rodrigues, G.; Psaila, B.; Kaplan, R.N.; Bromberg, J.F.; Kang, Y.; et al. Pre-metastatic niches: Organ-specific homes for metastases. Nat. Rev. Cancer 2017, 17, 302–317. [Google Scholar] [CrossRef]
- Luzzi, K.J.; MacDonald, I.C.; Schmidt, E.E.; Kerkvliet, N.; Morris, V.L.; Chambers, A.F.; Groom, A.C. Multistep nature of metastatic inefficiency: Dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am. J. Pathol. 1998, 153, 865–873. [Google Scholar] [CrossRef]
- Bockhorn, M.; Jain, R.K.; Munn, L.L. Active versus passive mechanisms in metastasis: Do cancer cells crawl into vessels, or are they pushed? Lancet Oncol. 2007, 8, 444–448. [Google Scholar] [CrossRef] [Green Version]
- Hillen, F.; Griffioen, A.W. Tumour vascularization: Sprouting angiogenesis and beyond. Cancer Metastasis Rev. 2007, 26, 489–502. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Park, S.Y.; Nam, J.S. The force awakens: Metastatic dormant cancer cells. Exp. Mol. Med. 2020, 52, 569–581. [Google Scholar] [CrossRef] [Green Version]
- Giancotti, F.G. XMechanisms governing metastatic dormancy and reactivation. Cell 2013, 155, 750. [Google Scholar] [CrossRef] [Green Version]
- Albrengues, J.; Shields, M.A.; Ng, D.; Park, C.G.; Ambrico, A.; Poindexter, M.E.; Upadhyay, P.; Uyeminami, D.L.; Pommier, A.; Küttner, V.; et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science 2018, 361. [Google Scholar] [CrossRef] [Green Version]
- Choi, J.; Cha, Y.J.; Koo, J.S. Adipocyte biology in breast cancer: From silent bystander to active facilitator. Prog. Lipid Res. 2018, 69, 11–20. [Google Scholar] [CrossRef]
- Gerber, S.A.; Rybalko, V.Y.; Bigelow, C.E.; Lugade, A.A.; Foster, T.H.; Frelinger, J.G.; Lord, E.M. Preferential attachment of peritoneal tumor metastases to omental immune aggregates and possible role of a unique vascular microenvironment in metastatic survival and growth. Am. J. Pathol. 2006, 169, 1739–1752. [Google Scholar] [CrossRef] [Green Version]
- Nieman, K.M.; Kenny, H.A.; Penicka, C.V.; Ladanyi, A.; Buell-Gutbrod, R.; Zillhardt, M.R.; Romero, I.L.; Carey, M.S.; Mills, G.B.; Hotamisligil, G.S.; et al. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat. Med. 2011, 17, 1498–1503. [Google Scholar] [CrossRef] [Green Version]
- Cao, H.; Sekiya, M.; Ertunc, M.E.; Burak, M.F.; Mayers, J.R.; White, A.; Inouye, K.; Rickey, L.M.; Ercal, B.C.; Furuhashi, M.; et al. Adipocyte lipid chaperone aP2 Is a secreted adipokine regulating hepatic glucose production. Cell Metab. 2013, 17, 768–778. [Google Scholar] [CrossRef] [Green Version]
- Hao, J.; Zhang, Y.; Yan, X.; Yan, F.; Sun, Y.; Zeng, J.; Waigel, S.; Yin, Y.; Fraig, M.M.; Egilmez, N.K.; et al. Circulating Adipose Fatty Acid Binding Protein Is a New Link Underlying Obesity-Associated Breast/Mammary Tumor Development. Cell Metab. 2018, 28, 689–705.e5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yan, F.; Shen, N.; Pang, J.X.; Zhang, Y.W.; Rao, E.Y.; Bode, A.M.; Al-Kali, A.; Zhang, D.E.; Litzow, M.R.; Li, B.; et al. Fatty acid-binding protein FABP4 mechanistically links obesity with aggressive AML by enhancing aberrant DNA methylation in AML cells. Leukemia 2017, 31, 1434–1442. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, Q.; Li, B.; Li, Z.; Li, J.; Sun, S.; Sun, S. Cancer-associated adipocytes: Key players in breast cancer progression. J. Hematol. Oncol. 2019, 12, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Guerrero, J.; Tobar, N.; Cáceres, M.; Espinoza, L.; Escobar, P.; Dotor, J.; Smith, P.C.; Martínez, J. Soluble factors derived from tumor mammary cell lines induce a stromal mammary adipose reversion in human and mice adipose cells. Possible role of TGF-β1 and TNF-α. Breast Cancer Res. Treat. 2010, 119, 497–508. [Google Scholar] [CrossRef]
- Andarawewa, K.L.; Motrescu, E.R.; Chenard, M.P.; Gansmuller, A.; Stoll, I.; Tomasetto, C.; Rio, M.C. Stromelysin-3 is a potent negative regulator of adipogenesis participating to cancer cell-adipocyte interaction/crosstalk at the tumor invasive front. Cancer Res. 2005, 65, 10862–10871. [Google Scholar] [CrossRef] [Green Version]
- Meunier, P.; Aaron, J.; Edouard, C.; Vignon, G. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin. Orthop. Relat. Res. 1971, 80, 147–154. [Google Scholar] [CrossRef]
- Scheller, E.L.; Rosen, C.J. What’s the matter with MAT? Marrow adipose tissue, metabolism, and skeletal health. Ann. N. Y. Acad. Sci. 2014, 1311, 14–30. [Google Scholar] [CrossRef] [Green Version]
- Morris, E.V.; Edwards, C.M. The role of bone marrow adipocytes in bone metastasis. J. Bone Oncol. 2016, 5, 121–123. [Google Scholar] [CrossRef] [Green Version]
- Olechnowicz, S.W.Z.; Edwards, C.M. Contributions of the host microenvironment to cancer-induced bone disease. Cancer Res. 2014, 74, 1625–1631. [Google Scholar] [CrossRef] [Green Version]
- Woolthuis, C.M.; Stranahan, A.W.; Park, C.Y.; Minhajuddin, M.; Gasparetto, M.; Stevens, B.; Pei, S.; Jordan, C.T. Leukemic Stem Cells Evade Chemotherapy by Metabolic Adaptation to an Adipose Tissue Niche. Cell Stem Cell 2016, 19, 23–37. [Google Scholar] [CrossRef] [Green Version]
- Herroon, M.K.; Rajagurubandara, E.; Hardaway, A.L.; Powell, K.; Turchick, A.; Feldmann, D.; Podgorski, I. Bone marrow adipocytes promote tumor growth in bone via FABP4-dependent mechanisms. Oncotarget 2013, 4, 2108–2123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Diedrich, J.D.; Rajagurubandara, E.; Herroon, M.K.; Mahapatra, G.; Hüttemann, M.; Podgorski, I. Bone marrow adipocytes promote the warburg phenotype in metastatic prostate tumors via HIF-1α activation. Oncotarget 2016, 7, 64854–64877. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cawthorn, W.P.; Scheller, E.L.; Learman, B.S.; Parlee, S.D.; Simon, B.R.; Mori, H.; Ning, X.; Bree, A.J.; Schell, B.; Broome, D.T.; et al. Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metab. 2014, 20, 368–375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katira, A.; Tan, P.H. Evolving role of adiponectin in cancer-controversies and update. Cancer Biol. Med. 2016, 13, 101–119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Batista, M.L.; Olivan, M.; Alcantara, P.S.M.; Sandoval, R.; Peres, S.B.; Neves, R.X.; Silverio, R.; Maximiano, L.F.; Otoch, J.P.; Seelaender, M. Adipose tissue-derived factors as potential biomarkers in cachectic cancer patients. Cytokine 2013, 61, 532–539. [Google Scholar] [CrossRef] [Green Version]
- Tan, P.H.; Tyrrell, H.E.J.; Gao, L.; Xu, D.; Quan, J.; Gill, D.; Rai, L.; Ding, Y.; Plant, G.; Chen, Y.; et al. Adiponectin receptor signaling on dendritic cells blunts antitumor immunity. Cancer Res. 2014, 74, 5711–5722. [Google Scholar] [CrossRef] [Green Version]
- Trayhurn, P. Hypoxia and adipose tissue function and dysfunction in obesity. Physiol. Rev. 2013, 93, 1–21. [Google Scholar] [CrossRef] [Green Version]
- Chen, B.; Lam, K.S.L.; Wang, Y.; Wu, D.; Lam, M.C.; Shen, J.; Wong, L.; Hoo, R.L.C.; Zhang, J.; Xu, A. Hypoxia dysregulates the production of adiponectin and plasminogen activator inhibitor-1 independent of reactive oxygen species in adipocytes. Biochem. Biophys. Res. Commun. 2006, 341, 549–556. [Google Scholar] [CrossRef]
- Wang, B.; Wood, I.S.; Trayhurn, P. Hypoxia induces leptin gene expression and secretion in human preadipocytes: Differential effects of hypoxia on adipokine expression by preadipocytes. J. Endocrinol. 2008, 198, 127–134. [Google Scholar] [CrossRef] [Green Version]
- Chen, D.C.; Chung, Y.F.; Yeh, Y.T.; Chaung, H.C.; Kuo, F.C.; Fu, O.Y.; Chen, H.Y.; Hou, M.F.; Yuan, S.S.F. Serum adiponectin and leptin levels in Taiwanese breast cancer patients. Cancer Lett. 2006, 237, 109–114. [Google Scholar] [CrossRef]
- Sultana, R.; Kataki, A.C.; Borthakur, B.B.; Basumatary, T.K.; Bose, S. Imbalance in leptin-adiponectin levels and leptin receptor expression as chief contributors to triple negative breast cancer progression in Northeast India. Gene 2017, 621, 51–58. [Google Scholar] [CrossRef]
- Barone, I.; Giordano, C.; Bonofiglio, D.; Andò, S.; Catalano, S. The weight of obesity in breast cancer progression and metastasis: Clinical and molecular perspectives. Semin. Cancer Biol. 2020, 60, 274–284. [Google Scholar] [CrossRef] [PubMed]
- Alshaker, H.; Krell, J.; Frampton, A.E.; Waxman, J.; Blyuss, O.; Zaikin, A.; Winkler, M.; Stebbing, J.; Yagüe, E.; Pchejetski, D. Leptin induces upregulation of sphingosine kinase 1 in oestrogen receptor-negative breast cancer via Src family kinase-mediated, janus kinase 2-independent pathway. Breast Cancer Res. 2014, 16, 426. [Google Scholar] [CrossRef] [PubMed]
- Sabol, R.A.; Bowles, A.C.; Côté, A.; Wise, R.; O’Donnell, B.; Matossian, M.D.; Hossain, F.M.; Burks, H.E.; Del Valle, L.; Miele, L.; et al. Leptin produced by obesity-altered adipose stem cells promotes metastasis but not tumorigenesis of triple-negative breast cancer in orthotopic xenograft and patient-derived xenograft models. Breast Cancer Res. 2019, 21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chang, C.C.; Wu, M.J.; Yang, J.Y.; Camarillo, I.G.; Chang, C.J. Leptin-STAT3-G9a signaling promotes obesity-mediated breast cancer progression. Cancer Res. 2015, 75, 2375–2386. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brandon, J.A.; Kraemer, M.; Vandra, J.; Halder, S.; Ubele, M.; Morris, A.J.; Smyth, S.S. Adipose-derived autotaxin regulates inflammation and steatosis associated with diet-induced obesity. PLoS ONE 2019, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benesch, M.G.K.; Tang, X.; Brindley, D.N. Autotaxin and breast cancer: Towards overcoming treatment barriers and sequelae. Cancers 2020, 12, 374. [Google Scholar] [CrossRef] [Green Version]
- Gupta, P.B.; Onder, T.T.; Jiang, G.; Tao, K.; Kuperwasser, C.; Weinberg, R.A.; Lander, E.S. Identification of Selective Inhibitors of Cancer Stem Cells by High-Throughput Screening. Cell 2009, 138, 645–659. [Google Scholar] [CrossRef] [Green Version]
- Shim, S.J.; Shin, E.; Lee, C.-S.; Koo, J.S. The expressions of autotaxin-lysophosphatidate signaling-related proteins in metastatic breast cancer. Int. J. Clin. Exp. Pathol. 2019, 12, 2920–2930. [Google Scholar]
- Dusaulcy, R.; Rancoule, C.; Grès, S.; Wanecq, E.; Colom, A.; Guigné, C.; Van Meeteren, L.A.; Moolenaar, W.H.; Valet, P.; Saulnier-Blache, J.S. Adipose-specific disruption of autotaxin enhances nutritional fattening and reduces plasma lysophosphatidic acid. J. Lipid Res. 2011, 52, 1247–1255. [Google Scholar] [CrossRef] [Green Version]
- Rancoule, C.; Dusaulcy, R.; Tréguer, K.; Grès, S.; Guigné, C.; Quilliot, D.; Valet, P.; Saulnier-Blache, J.S. Depot-specific regulation of autotaxin with obesity in human adipose tissue. J. Physiol. Biochem. 2012, 68, 635–644. [Google Scholar] [CrossRef] [PubMed]
- Benesch, M.G.K.; Macintyre, I.T.K.; McMullen, T.P.W.; Brindley, D.N. Coming of age for autotaxin and lysophosphatidate signaling: Clinical applications for preventing, detecting and targeting tumor-promoting inflammation. Cancers 2018, 10, 73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reeves, V.L.; Trybula, J.S.; Wills, R.C.; Goodpaster, B.H.; Dubé, J.J.; Kienesberger, P.C.; Kershaw, E.E. Serum Autotaxin/ENPP2 correlates with insulin resistance in older humans with obesity. Obesity 2015, 23, 2371–2376. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Azare, J.; Doane, A.; Leslie, K.; Chang, Q.; Berishaj, M.; Nnoli, J.; Mark, K.; Al-Ahmadie, H.; Gerald, W.; Hassimi, M.; et al. Stat3 mediates expression of autotaxin in breast cancer. PLoS ONE 2011, 6. [Google Scholar] [CrossRef] [Green Version]
- Du, J.; Sun, C.; Hu, Z.; Yang, Y.; Zhu, Y.; Zheng, D.; Gu, L.; Lu, X. Lysophosphatidic Acid Induces MDA-MB-231 Breast Cancer Cells Migration through Activation of PI3K/PAK1/ERK Signaling. PLoS ONE 2010, 5, e15940. [Google Scholar] [CrossRef]
- Wu, T.; Van der Kooi, C.; Shah, P.; Charnigo, R.; Huang, C.; Smyth, S.S.; Morris, A.J. Integrin-mediated cell surface recruitment of autotaxin promotes persistent directional cell migration. FASEB J. 2014, 28, 861–870. [Google Scholar] [CrossRef] [Green Version]
- Cha, Y.J.; Koo, J.S. Adipokines as therapeutic targets in breast cancer treatment. Expert Opin. Ther. Targets 2018, 22, 941–953. [Google Scholar] [CrossRef]
- Benesch, M.G.K.; Tang, X.; Maeda, T.; Ohhata, A.; Zhao, Y.Y.; Kok, B.P.C.; Dewald, J.; Hitt, M.; Curtis, J.M.; McMullen, T.P.W.; et al. Inhibition of autotaxin delays breast tumor growth and lung metastasis in mice. FASEB J. 2014, 28, 2655–2666. [Google Scholar] [CrossRef]
- Boucharaba, A.; Serre, C.-M.; Grès, S.; Saulnier-Blache, J.S.; Bordet, J.-C.; Guglielmi, J.; Clézardin, P.; Peyruchaud, O. Platelet-derived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer. J. Clin. Invest. 2004, 114, 1714–1725. [Google Scholar] [CrossRef] [Green Version]
- Zhang, H.; Xu, X.; Gajewiak, J.; Tsukahara, R.; Fujiwara, Y.; Liu, J.; Fells, J.I.; Perygin, D.; Parrill, A.L.; Tigyi, G.; et al. Dual activity lysophosphatidic acid receptor pan-antagonist/autotaxin inhibitor reduces breast cancer cell migration in vitro and causes tumor regression in vivo. Cancer Res. 2009, 69, 5441–5449. [Google Scholar] [CrossRef] [Green Version]
- Magkrioti, C.; Galaris, A.; Kanellopoulou, P.; Stylianaki, E.A.; Kaffe, E.; Aidinis, V. Autotaxin and chronic inflammatory diseases. J. Autoimmun. 2019, 104, 102327. [Google Scholar] [CrossRef] [PubMed]
- Maher, T.M.; Kreuter, M.; Lederer, D.J.; Brown, K.K.; Wuyts, W.; Verbruggen, N.; Stutvoet, S.; Fieuw, A.; Ford, P.; Abi-Saab, W.; et al. Rationale, design and objectives of two phase III, randomised, placebo-controlled studies of GLPG1690, a novel autotaxin inhibitor, in idiopathic pulmonary fibrosis (ISABELA 1 and 2). BMJ Open Respir. Res. 2019, 6. [Google Scholar] [CrossRef]
- Maher, T.M.; van der Aar, E.M.; Van de Steen, O.; Allamassey, L.; Desrivot, J.; Dupont, S.; Fagard, L.; Ford, P.; Fieuw, A.; Wuyts, W. Safety, tolerability, pharmacokinetics, and pharmacodynamics of GLPG1690, a novel autotaxin inhibitor, to treat idiopathic pulmonary fibrosis (FLORA): A phase 2a randomised placebo-controlled trial. Lancet Respir. Med. 2018, 6, 627–635. [Google Scholar] [CrossRef]
- Tang, X.; Wuest, M.; Benesch, M.G.K.; Dufour, J.; Zhao, Y.Y.; Curtis, J.M.; Monjardet, A.; Heckmann, B.; Murray, D.; Wuest, F.; et al. Inhibition of autotaxin with GLPG1690 increases the efficacy of radiotherapy and chemotherapy in a mouse model of breast cancer. Mol. Cancer Ther. 2020, 19, 63–74. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dirat, B.; Bochet, L.; Dabek, M.; Daviaud, D.; Dauvillier, S.; Majed, B.; Wang, Y.Y.; Meulle, A.; Salles, B.; Le Gonidec, S.; et al. Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 2011, 71, 2455–2465. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kern, L.; Mittenbühler, M.J.; Vesting, A.J.; Ostermann, A.L.; Wunderlich, C.M.; Wunderlich, F.T. Obesity-induced TNFα and IL-6 signaling: The missing link between obesity and inflammation-driven liver and colorectal cancers. Cancers 2019, 11, 24. [Google Scholar] [CrossRef] [Green Version]
- Arendt, L.M.; McCready, J.; Keller, P.J.; Baker, D.D.; Naber, S.P.; Seewaldt, V.; Kuperwasser, C. Obesity promotes breast cancer by CCL2-mediated macrophage recruitment and angiogenesis. Cancer Res. 2013, 73, 6080–6093. [Google Scholar] [CrossRef] [Green Version]
- Tsuyada, A.; Chow, A.; Wu, J.; Somlo, G.; Chu, P.; Loera, S.; Luu, T.; Li, A.X.; Wu, X.; Ye, W.; et al. CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells. Cancer Res. 2012, 72, 2768–2779. [Google Scholar] [CrossRef] [Green Version]
- D’Esposito, V.D.; Liguoro, D.; Ambrosio, M.R.; Collina, F.; Cantile, M.; Spinelli, R.; Raciti, G.A.; Miele, C.; Valentino, R.; Campiglia, P.; et al. Adipose microenvironment promotes triple negative breast cancer cell invasiveness and dissemination by producing CCL5. Oncotarget 2016, 7, 24495–24509. [Google Scholar] [CrossRef] [Green Version]
- Velasco-Velázquez, M.; Jiao, X.; De La Fuente, M.; Pestell, T.G.; Ertel, A.; Lisanti, M.P.; Pestell, R.G. CCR5 antagonist blocks metastasis of basal breast cancer cells. Cancer Res. 2012, 72, 3839–3850. [Google Scholar] [CrossRef] [Green Version]
- Rybinska, I.; Agresti, R.; Trapani, A.; Tagliabue, E.; Triulzi, T. Adipocytes in Breast Cancer, the Thick and the Thin. Cells 2020, 9, 560. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bastard, J.-P.; Jardel, C.; Bruckert, E.; Blondy, P.; Capeau, J.; Laville, M.; Vidal, H.; Hainque, B. Elevated Levels of Interleukin 6 Are Reduced in Serum and Subcutaneous Adipose Tissue of Obese Women after Weight Loss*. J. Clin. Endocrinol. Metab. 2000, 85, 3338–3342. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.S.; Jung, M.; Choi, S.K.; Woo, J.; Piao, Y.J.; Hwang, E.H.; Kim, H.; Kim, S.J.; Moon, W.K. IL-6-mediated cross-talk between human preadipocytes and ductal carcinoma in situ in breast cancer progression. J. Exp. Clin. Cancer Res. 2018, 37, 200. [Google Scholar] [CrossRef] [PubMed]
- Sansone, P.; Storci, G.; Tavolari, S.; Guarnieri, T.; Giovannini, C.; Taffurelli, M.; Ceccarelli, C.; Santini, D.; Paterini, P.; Marcu, K.B.; et al. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J. Clin. Invest. 2007, 117, 3988–4002. [Google Scholar] [CrossRef]
- Marotta, L.L.C.; Almendro, V.; Marusyk, A.; Shipitsin, M.; Schemme, J.; Walker, S.R.; Bloushtain-Qimron, N.; Kim, J.J.; Choudhury, S.A.; Maruyama, R.; et al. The JAK2/STAT3 signaling pathway is required for growth of CD44 +CD24- stem cell-like breast cancer cells in human tumors. J. Clin. Invest. 2011, 121, 2723–2735. [Google Scholar] [CrossRef]
- Bergmann, J.; Müller, M.; Baumann, N.; Reichert, M.; Heneweer, C.; Bolik, J.; Lücke, K.; Gruber, S.; Carambia, A.; Boretius, S.; et al. IL-6 trans-signaling is essential for the development of hepatocellular carcinoma in mice. Hepatology 2017, 65, 89–103. [Google Scholar] [CrossRef]
- Wang, C.-Q.; Sun, H.-T.; Gao, X.-M.; Ren, N.; Sheng, Y.-Y.; Wang, Z.; Zheng, Y.; Wei, J.-W.; Zhang, K.-L.; Yu, X.-X.; et al. Interleukin-6 enhances cancer stemness and promotes metastasis of hepatocellular carcinoma via up-regulating osteopontin expression. Am. J. Cancer Res. 2016, 6, 1873–1889. [Google Scholar]
- Lukens, J.R.; Dixit, V.D.; Kanneganti, T.D. Inflammasome activation in obesity-related inflammatory diseases and autoimmunity. Discov. Med. 2011, 12, 65–74. [Google Scholar]
- Coleman, R.E.; Marshall, H.; Cameron, D.; Dodwell, D.; Burkinshaw, R.; Keane, M.; Gil, M.; Houston, S.J.; Grieve, R.J.; Barrett-Lee, P.J.; et al. Breast-cancer adjuvant therapy with zoledronic acid. N. Engl. J. Med. 2011, 365, 1396–1405. [Google Scholar] [CrossRef] [Green Version]
- Tulotta, C.; Ottewell, P. The role of IL-1B in breast cancer bone metastasis. Endocr. Relat. Cancer 2018, 25, R421–R434. [Google Scholar] [CrossRef] [Green Version]
- Nutter, F.; Holen, I.; Brown, H.K.; Cross, S.S.; Evans, C.A.; Walker, M.; Coleman, R.E.; Westbrook, J.A.; Selby, P.J.; Brown, J.E.; et al. Different molecular profiles are associated with breast cancer cell homing compared with colonisation of bone: Evidence using a novel bone-seeking cell line. Endocr. Relat. Cancer 2014, 21, 327–341. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hagemann, T.; Wilson, J.; Kulbe, H.; Li, N.F.; Leinster, D.A.; Charles, K.; Klemm, F.; Pukrop, T.; Binder, C.; Balkwill, F.R. Macrophages Induce Invasiveness of Epithelial Cancer Cells Via NF-κB and JNK. J. Immunol. 2005, 175, 1197–1205. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chua, H.L.; Bhat-Nakshatri, P.; Clare, S.E.; Morimiya, A.; Badve, S.; Nakshatri, H. NF-κB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: Potential involvement of ZEB-1 and ZEB-2. Oncogene 2007, 26, 711–724. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sturm, J.W.; Magdeburg, R.; Berger, K.; Petruch, B.; Samel, S.; Bönninghoff, R.; Keese, M.; Hafner, M.; Post, S. Influence of TNFA on the formation of liver metastases in a syngenic mouse model. Int. J. Cancer 2003, 107, 11–21. [Google Scholar] [CrossRef]
- Ham, B.; Fernandez, M.C.; D’Costa, Z.; Brodt, P. The diverse roles of the TNF axis in cancer progression and metastasis. Trends Cancer Res. 2016, 11, 1–27. [Google Scholar]
- Faria, S.S.; Corrêa, L.H.; Heyn, G.S.; de Sant’Ana, L.P.; Almeida, R.D.N.; Magalhães, K.G. Obesity and breast cancer: The role of crown-like structures in breast adipose tissue in tumor progression, prognosis, and therapy. J. Breast Cancer 2020, 23, 233–245. [Google Scholar] [CrossRef]
- Berstein, L.M.; Iyevleva, A.G.; Mukhina, M.S.; Vasilyev, D.A.; Poroshina, T.E. Features of omental adipose tissue in endometrial cancer patients with ‘standard’ or ‘metabolically healthy’ obesity: Associations with tumor process characteristics. Springerplus 2016, 5, 1900. [Google Scholar] [CrossRef] [Green Version]
- Gucalp, A.; Iyengar, N.M.; Zhou, X.K.; Giri, D.D.; Falcone, D.J.; Wang, H.; Williams, S.; Krasne, M.D.; Yaghnam, I.; Kunzel, B.; et al. Periprostatic adipose inflammation is associated with high-grade prostate cancer. Prostate Cancer Prostatic Dis. 2017, 20, 418–423. [Google Scholar] [CrossRef]
- Itoh, M.; Kato, H.; Suganami, T.; Konuma, K.; Marumoto, Y.; Terai, S.; Sakugawa, H.; Kanai, S.; Hamaguchi, M.; Fukaishi, T.; et al. Hepatic crown-like structure: A unique histological feature in non-alcoholic steatohepatitis in mice and humans. PLoS ONE 2013, 8. [Google Scholar] [CrossRef] [Green Version]
- Mullooly, M.; Yang, H.P.; Falk, R.T.; Nyante, S.J.; Cora, R.; Pfeiffer, R.M.; Radisky, D.C.; Visscher, D.W.; Hartmann, L.C.; Carter, J.M.; et al. Relationship between crown-like structures and sex-steroid hormones in breast adipose tissue and serum among postmenopausal breast cancer patients. Breast Cancer Res. 2017, 19. [Google Scholar] [CrossRef] [Green Version]
- Cortellini, A.; Bersanelli, M.; Buti, S.; Cannita, K.; Santini, D.; Perrone, F.; Giusti, R.; Tiseo, M.; Michiara, M.; Di Marino, P.; et al. A multicenter study of body mass index in cancer patients treated with anti-PD-1/PD-L1 immune checkpoint inhibitors: When overweight becomes favorable. J. Immunother. Cancer 2019, 7, 57. [Google Scholar] [CrossRef] [PubMed]
- Plaks, V.; Kong, N.; Werb, Z. The Cancer Stem Cell Niche: How Essential Is the Niche in Regulating Stemness of Tumor Cells? Cell Stem Cell 2015, 16, 225–238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, S.; Yang, X.; Wang, L.; Zhang, C. Interplay between inflammatory tumor microenvironment and cancer stem cells (Review). Oncol. Lett. 2018, 16, 679–686. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.H.; Hong, H.S.; Liu, Z.X.; Kim, R.H.; Kang, M.K.; Park, N.-H.; Shin, K.-H. TNFα enhances cancer stem cell-like phenotype via Notch-Hes1 activation in oral squamous cell carcinoma cells. Biochem. Biophys. Res. Commun. 2012, 424, 58–64. [Google Scholar] [CrossRef] [Green Version]
- Ostyn, P.; El Machhour, R.; Begard, S.; Kotecki, N.; Vandomme, J.; Flamenco, P.; Segard, P.; Masselot, B.; Formstecher, P.; Touil, Y.; et al. Transient TNF regulates the self-renewing capacity of stem-like label-retaining cells in sphere and skin equivalent models of melanoma. Cell Commun. Signal. 2014, 12. [Google Scholar] [CrossRef] [PubMed]
- Zhao, X.; Ma, L.; Dai, L.; Zuo, D.; Li, X.; Zhu, H.; Xu, F. TNF-α promotes the malignant transformation of intestinal stem cells through the NF-κB and Wnt/β-catenin signaling pathways. Oncol. Rep. 2020, 44, 577–588. [Google Scholar] [CrossRef]
- Storci, G.; Sansone, P.; Mari, S.; D’Uva, G.; Tavolari, S.; Guarnieri, T.; Taffurelli, M.; Ceccarelli, C.; Santini, D.; Chieco, P.; et al. TNFalpha up-regulates SLUG via the NF-kappaB/HIF1alpha axis, which imparts breast cancer cells with a stem cell-like phenotype. J. Cell. Physiol. 2010, 225, 682–691. [Google Scholar] [CrossRef] [Green Version]
- Liu, W.; Lu, X.; Shi, P.; Yang, G.; Zhou, Z.; Li, W.; Mao, X.; Jiang, D.; Chen, C. TNF-α increases breast cancer stem-like cells through up-regulating TAZ expression via the non-canonical NF-κB pathway. Sci. Rep. 2020, 10, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Teslow, E.A.; Mitrea, C.; Bao, B.; Mohammad, R.M.; Polin, L.A.; Dyson, G.; Purrington, K.S.; Bollig-Fischer, A. Obesity-induced MBD2_v2 expression promotes tumor-initiating triple-negative breast cancer stem cells. Mol. Oncol. 2019, 13, 894–908. [Google Scholar] [CrossRef]
- Fukumura, D.; Ushiyama, A.; Duda, D.G.; Xu, L.; Tam, J.; Krishna, V.; Chatterjee, K.; Garkavtsev, I.; Jain, R.K. Paracrine regulation of angiogenesis and adipocyte differentiation during in vivo adipogenesis. Circ. Res. 2003, 93. [Google Scholar] [CrossRef] [Green Version]
- Fukumura, D.; Incio, J.; Shankaraiah, R.C.; Jain, R.K. Obesity and Cancer: An Angiogenic and Inflammatory Link. Microcirculation 2016, 23, 191–206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, W.; Guo, S.; Gonzalez-Perez, R.R. Leptin pro-angiogenic signature in breast cancer is linked to IL-1 signalling. Br. J. Cancer 2011, 104, 128–137. [Google Scholar] [CrossRef] [PubMed]
- Kolb, R.; Kluz, P.; Tan, Z.W.; Borcherding, N.; Bormann, N.; Vishwakarma, A.; Balcziak, L.; Zhu, P.; Davies, B.S.; Gourronc, F.; et al. Obesity-associated inflammation promotes angiogenesis and breast cancer via angiopoietin-like 4. Oncogene 2019, 38, 2351–2363. [Google Scholar] [CrossRef] [PubMed]
- Lohmann, A.E.; Chia, S. Patients with metastatic breast cancer using bevacizumab as a treatment: Is there still a role for it? Curr. Treat. Options Oncol. 2012, 13, 249–262. [Google Scholar] [CrossRef]
- Jain, R.K.; Duda, D.G.; Willett, C.G.; Sahani, D.V.; Zhu, A.X.; Loeffler, J.S.; Batchelor, T.T.; Sorensen, A.G. Biomarkers of response and resistance to antiangiogenic therapy. Nat. Rev. Clin. Oncol. 2009, 6, 327–338. [Google Scholar] [CrossRef]
- Incio, J.; Ligibel, J.A.; McManus, D.T.; Suboj, P.; Jung, K.; Kawaguchi, K.; Pinter, M.; Babykutty, S.; Chin, S.M.; Vardam, T.D.; et al. Obesity promotes resistance to anti-VEGF therapy in breast cancer by up-regulating IL-6 and potentially FGF-2. Sci. Transl. Med. 2018, 10, 945. [Google Scholar] [CrossRef] [Green Version]
- Fernández-Cortés, M.; Delgado-Bellido, D.; Oliver, F.J. Vasculogenic Mimicry: Become an Endothelial Cell “But Not So Much”. Front. Oncol. 2019, 9, 803. [Google Scholar] [CrossRef] [Green Version]
- Coelho, P.; Almeida, J.; Prudêncio, C.; Fernandes, R.; Soares, R. Effect of Adipocyte Secretome in Melanoma Progression and Vasculogenic Mimicry. J. Cell. Biochem. 2016, 117, 1697–1706. [Google Scholar] [CrossRef] [Green Version]
- Marín, D.; Sabater, B. The cancer Warburg effect may be a testable example of the minimum entropy production rate principle. Phys. Biol. 2017, 14, 024001. [Google Scholar] [CrossRef]
- Fu, Y.; Liu, S.; Yin, S.; Niu, W.; Xiong, W.; Tan, M.; Li, G.; Zhou, M. The reverse Warburg effect is likely to be an Achilles’ heel of cancer that can be exploited for cancer therapy. Oncotarget 2017, 8, 57813–57825. [Google Scholar] [CrossRef] [Green Version]
- Pavlides, S.; Whitaker-Menezes, D.; Castello-Cros, R.; Flomenberg, N.; Witkiewicz, A.K.; Frank, P.G.; Casimiro, M.C.; Wang, C.; Fortina, P.; Addya, S.; et al. The reverse Warburg effect: Aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle 2009, 8, 3984–4001. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Armignacco, R.; Cantini, G.; Poli, G.; Guasti, D.; Nesi, G.; Romagnoli, P.; Mannell, M.; Luconi, M. The adipose stem cell as a novel metabolic actor in adrenocortical carcinoma progression: Evidence from an in vitro tumor microenvironment crosstalk model. Cancers 2019, 11, 11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martinez-Outschoorn, U.E.; Lin, Z.; Whitaker-Menezes, D.; Howell, A.; Sotgia, F.; Lisanti, M.P. Ketone body utilization drives tumor growth and metastasis. Cell Cycle 2012, 11, 3964–3971. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Y.Y.; Attané, C.; Milhas, D.; Dirat, B.; Dauvillier, S.; Guerard, A.; Gilhodes, J.; Lazar, I.; Alet, N.; Laurent, V.; et al. Mammary adipocytes stimulate breast cancer invasion through metabolic remodeling of tumor cells. JCI Insight 2017, 2. [Google Scholar] [CrossRef] [Green Version]
- Zaidi, N.; Lupien, L.; Kuemmerle, N.B.; Kinlaw, W.B.; Swinnen, J.V.; Smans, K. Lipogenesis and lipolysis: The pathways exploited by the cancer cells to acquire fatty acids. Prog. Lipid Res. 2013, 52, 585–589. [Google Scholar] [CrossRef] [Green Version]
- Zhang, M.; Di Martino, J.S.; Bowman, R.L.; Campbell, N.R.; Baksh, S.C.; Simon-Vermot, T.; Kim, I.S.; Haldeman, P.; Mondal, C.; Yong-Gonzales, V.; et al. Adipocyte-derived lipids mediate melanoma progression via FATP proteins. Cancer Discov. 2018, 8, 1006–1025. [Google Scholar] [CrossRef] [Green Version]
- Shafat, M.S.; Oellerich, T.; Mohr, S.; Robinson, S.D.; Edwards, D.R.; Marlein, C.R.; Piddock, R.E.; Fenech, M.; Zaitseva, L.; Abdul-Aziz, A.; et al. Leukemic blasts program bone marrow adipocytes to generate a protumoral microenvironment. Blood 2017, 129, 1320–1332. [Google Scholar] [CrossRef]
- Martinez-Outschoorn, U.E.; Peiris-Pagés, M.; Pestell, R.G.; Sotgia, F.; Lisanti, M.P. Cancer metabolism: A therapeutic perspective. Nat. Rev. Clin. Oncol. 2017, 14, 11–31. [Google Scholar] [CrossRef]
- Cluntun, A.A.; Lukey, M.J.; Cerione, R.A.; Locasale, J.W. Glutamine Metabolism in Cancer: Understanding the Heterogeneity. Trends Cancer 2017, 3, 169–180. [Google Scholar] [CrossRef] [Green Version]
- Yang, L.; Achreja, A.; Yeung, T.L.; Mangala, L.S.; Jiang, D.; Han, C.; Baddour, J.; Marini, J.C.; Ni, J.; Nakahara, R.; et al. Targeting Stromal Glutamine Synthetase in Tumors Disrupts Tumor Microenvironment-Regulated Cancer Cell Growth. Cell Metab. 2016, 24, 685–700. [Google Scholar] [CrossRef] [Green Version]
- Petrus, P.; Lecoutre, S.; Dollet, L.; Wiel, C.; Sulen, A.; Gao, H.; Tavira, B.; Laurencikiene, J.; Rooyackers, O.; Checa, A.; et al. Glutamine Links Obesity to Inflammation in Human White Adipose Tissue. Cell Metab. 2020, 31, 375–390. [Google Scholar] [CrossRef] [PubMed]
- Recouvreux, M.V.; Moldenhauer, M.R.; Galenkamp, K.M.O.; Jung, M.; James, B.; Zhang, Y.; Lowy, A.; Bagchi, A.; Commisso, C. Glutamine depletion regulates Slug to promote EMT and metastasis in pancreatic cancer. J. Exp. Med. 2020, 217. [Google Scholar] [CrossRef] [PubMed]
- Pavlova, N.N.; Hui, S.; Ghergurovich, J.M.; Fan, J.; Intlekofer, A.M.; White, R.M.; Rabinowitz, J.D.; Thompson, C.B.; Zhang, J. As Extracellular Glutamine Levels Decline, Asparagine Becomes an Essential Amino Acid. Cell Metab. 2018, 27, 428–438.e5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, M.; Brooks, M.; Wicha, M.S. Asparagine and Glutamine: Co-conspirators Fueling Metastasis. Cell Metab. 2018, 27, 947–949. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Knott, S.R.V.; Wagenblast, E.; Khan, S.; Kim, S.Y.; Soto, M.; Wagner, M.; Turgeon, M.O.; Fish, L.; Erard, N.; Gable, A.L.; et al. Asparagine bioavailability governs metastasis in a model of breast cancer. Nature 2018, 554, 378–381. [Google Scholar] [CrossRef] [PubMed]
- Rizi, B.S.; Caneba, C.; Nowicka, A.; Nabiyar, A.W.; Liu, X.; Chen, K.; Klopp, A.; Nagrath, D. Nitric oxide mediates metabolic coupling of omentum-derived adipose stroma to ovarian and endometrial cancer cells. Cancer Res. 2015, 75, 456–471. [Google Scholar] [CrossRef] [Green Version]
- Al-Koussa, H.; El Mais, N.; Maalouf, H.; Abi-Habib, R.; El-Sibai, M. Arginine deprivation: A potential therapeutic for cancer cell metastasis? A review. Cancer Cell Int. 2020, 20, 150. [Google Scholar] [CrossRef]
- You, J.; Chen, W.; Chen, J.; Zheng, Q.; Dong, J.; Zhu, Y. The oncogenic role of ARG1 in progression and metastasis of hepatocellular carcinoma. BioMed Res. Int. 2018, 2018. [Google Scholar] [CrossRef]
- Zaytouni, T.; Tsai, P.Y.; Hitchcock, D.S.; Dubois, C.D.; Freinkman, E.; Lin, L.; Morales-Oyarvide, V.; Lenehan, P.J.; Wolpin, B.M.; Mino-Kenudson, M.; et al. Critical role for arginase 2 in obesity-Associated pancreatic cancer. Nat. Commun. 2017, 8, 1–12. [Google Scholar] [CrossRef]
- Spinelli, J.B.; Yoon, H.; Ringel, A.E.; Jeanfavre, S.; Clish, C.B.; Haigis, M.C. Metabolic recycling of ammonia via glutamate dehydrogenase supports breast cancer biomass. Science 2017, 358, 941–946. [Google Scholar] [CrossRef] [Green Version]
- Thomas, D.D.; Corkey, B.E.; Istfan, N.W.; Apovian, C.M. Hyperinsulinemia: An early indicator of metabolic dysfunction. J. Endocr. Soc. 2019, 3, 1727–1747. [Google Scholar] [CrossRef] [PubMed]
- Ireland, L.; Santos, A.; Campbell, F.; Figueiredo, C.; Hammond, D.; Ellies, L.G.; Weyer-Czernilofsky, U.; Bogenrieder, T.; Schmid, M.; Mielgo, A. Blockade of insulin-like growth factors increases efficacy of paclitaxel in metastatic breast cancer. Oncogene 2018, 37, 2022–2036. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Malaguarnera, R.; Belfiore, A. The emerging role of insulin and insulin-like growth factor signaling in cancer stem cells. Front. Endocrinol. 2014, 5, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baserga, R. The decline and fall of the IGF-I receptor. J. Cell. Physiol. 2013, 228, 675–679. [Google Scholar] [CrossRef]
- Tong, Y.; Wu, J.; Huang, O.; He, J.; Zhu, L.; Chen, W.; Li, Y.; Chen, X.; Shen, K. IGF-1 Interacted With Obesity in Prognosis Prediction in HER2-Positive Breast Cancer Patients. Front. Oncol. 2020, 10. [Google Scholar] [CrossRef]
- Wu, Y.; Brodt, P.; Sun, H.; Mejia, W.; Novosyadlyy, R.; Nunez, N.; Chen, X.; Mendoza, A.; Hong, S.H.; Khanna, C.; et al. Insulin-like growth factor-I regulates the liver microenvironment in obese mice and promotes liver metastasis. Cancer Res. 2010, 70, 57–67. [Google Scholar] [CrossRef] [Green Version]
- Rayes, R.F.; Milette, S.; Fernandez, M.C.; Ham, B.; Wang, N.; Bourdeau, F.; Perrino, S.; Yakar, S.; Brodt, P. Loss of neutrophil polarization in colon carcinoma liver metastases of mice with an inducible, liver-specific IGF-I deficiency. Oncotarget 2018, 9, 15691–15704. [Google Scholar] [CrossRef] [Green Version]
- Ruiz-Ojeda, F.J.; Méndez-Gutiérrez, A.; Aguilera, C.M.; Plaza-Díaz, J. Extracellular matrix remodeling of adipose tissue in obesity and metabolic diseases. Int. J. Mol. Sci. 2019, 20, 4888. [Google Scholar] [CrossRef] [Green Version]
- Buechler, C.; Krautbauer, S.; Eisinger, K. Adipose tissue fibrosis. World J. Diabetes 2015, 6, 548. [Google Scholar] [CrossRef]
- Hasegawa, Y.; Ikeda, K.; Chen, Y.; Alba, D.L.; Stifler, D.; Shinoda, K.; Hosono, T.; Maretich, P.; Yang, Y.; Ishigaki, Y.; et al. Repression of Adipose Tissue Fibrosis through a PRDM16-GTF2IRD1 Complex Improves Systemic Glucose Homeostasis. Cell Metab. 2018, 27, 180–194.e6. [Google Scholar] [CrossRef] [Green Version]
- Oikonomou, E.K.; Antoniades, C. The role of adipose tissue in cardiovascular health and disease. Nat. Rev. Cardiol. 2019, 16, 83–99. [Google Scholar] [CrossRef] [PubMed]
- Moorman, A.M.; Vink, R.; Heijmans, H.J.; Van Der Palen, J.; Kouwenhoven, E.A. The prognostic value of tumour-stroma ratio in triple-negative breast cancer. Eur. J. Surg. Oncol. 2012, 38, 307–313. [Google Scholar] [CrossRef] [PubMed]
- Zippi, M.; De Toma, G.; Minervini, G.; Cassieri, C.; Pica, R.; Colarusso, D.; Stock, S.; Crispino, P. Desmoplasia influenced recurrence of disease and mortality in stage III colorectal cancer within five years after surgery and adjuvant therapy. Saudi J. Gastroenterol. 2017, 23, 39. [Google Scholar] [CrossRef] [PubMed]
- Incio, J.; Liu, H.; Suboj, P.; Chin, S.M.; Chen, I.X.; Pinter, M.; Ng, M.R.; Nia, H.T.; Grahovac, J.; Kao, S.; et al. Obesity-induced inflammation and desmoplasia promote pancreatic cancer progression and resistance to chemotherapy. Cancer Discov. 2016, 6, 852–869. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Verset, L.; Tommelein, J.; Lopez, X.M.; Decaestecker, C.; Boterberg, T.; De Vlieghere, E.; Salmon, I.; Mareel, M.; Bracke, M.; De Wever, O.; et al. Impact of neoadjuvant therapy on cancer-associated fibroblasts in rectal cancer. Radiother. Oncol. 2015, 116, 449–454. [Google Scholar] [CrossRef] [PubMed]
- Arkan, M.C. Cancer: Fat and the fate of pancreatic tumours. Nature 2016, 536, 157–158. [Google Scholar] [CrossRef] [PubMed]
- Bochet, L.; Lehuédé, C.; Dauvillier, S.; Wang, Y.Y.; Dirat, B.; Laurent, V.; Dray, C.; Guiet, R.; Maridonneau-Parini, I.; Le Gonidec, S.; et al. Adipocyte-derived fibroblasts promote tumor progression and contribute to the desmoplastic reaction in breast cancer. Cancer Res. 2013, 73, 5657–5668. [Google Scholar] [CrossRef] [Green Version]
- Park, J.; Scherer, P.E. Adipocyte-derived endotrophin promotes malignant tumor progression. J. Clin. Invest. 2012, 122, 4243–4256. [Google Scholar] [CrossRef] [Green Version]
- Iyengar, P.; Espina, V.; Williams, T.W.; Lin, Y.; Berry, D.; Jelicks, L.A.; Lee, H.; Temple, K.; Graves, R.; Pollard, J.; et al. Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor/stroma microenvironment. J. Clin. Invest. 2005, 115, 1163–1176. [Google Scholar] [CrossRef] [Green Version]
- Wei, X.; Li, S.; He, J.; Du, H.; Liu, Y.; Yu, W.; Hu, H.; Han, L.; Wang, C.; Li, H.; et al. Tumor-secreted PAI-1 promotes breast cancer metastasis via the induction of adipocyte-derived collagen remodeling. Cell Commun. Signal. 2019, 17, 58. [Google Scholar] [CrossRef] [Green Version]
- Jotzu, C.; Alt, E.; Welte, G.; Li, J.; Hennessy, B.T.; Devarajan, E.; Krishnappa, S.; Pinilla, S.; Droll, L.; Song, Y.H. Adipose tissue derived stem cells differentiate into carcinoma-associated fibroblast-like cells under the influence of tumor derived factors. Cell. Oncol. 2011, 34, 55–67. [Google Scholar] [CrossRef] [PubMed]
- Kang, H.; Watkins, G.; Parr, C.; Douglas-Jones, A.; Mansel, R.E.; Jiang, W.G. Stromal cell derived factor-1: Its influence on invasiveness and migration of breast cancer cells in vitro, and its association with prognosis and survival in human breast cancer. Breast Cancer Res. 2005, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cozzo, A.J.; Fuller, A.M.; Makowski, L. Contribution of adipose tissue to development of cancer. Compr. Physiol. 2018, 8, 237–282. [Google Scholar] [CrossRef]
- Wynn, T.A.; Barron, L. Macrophages: Master regulators of inflammation and fibrosis. Semin. Liver Dis. 2010, 30, 245–257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Corrêa, L.H.; Corrêa, R.; Farinasso, C.M.; de Sant’Ana, D.L.P.; Magalhães, K.G. Adipocytes and macrophages interplay in the orchestration of tumor microenvironment: New implications in cancer progression. Front. Immunol. 2017, 8, 1. [Google Scholar] [CrossRef] [PubMed]
- Jaoude, J.; Koh, Y. Matrix metalloproteinases in exercise and obesity. Vasc. Health Risk Manag. 2016, 12, 287–295. [Google Scholar] [PubMed] [Green Version]
- Motrescu, E.R.; Blaise, S.; Etique, N.; Messaddeq, N.; Chenard, M.P.; Stoll, I.; Tomasetto, C.; Rio, M.C. Matrix metalloproteinase-11/stromelysin-3 exhibits collagenolytic function against collagen VI under normal and malignant conditions. Oncogene 2008, 27, 6347–6355. [Google Scholar] [CrossRef] [Green Version]
- De Lope, L.R.; Alcíbar, O.L.; López, A.A.; Hergueta-Redondo, M.; Peinado, H. Tumour–adipose tissue crosstalk: Fuelling tumour metastasis by extracellular vesicles. Philos. Trans. R. Soc. B Biol. Sci. 2018, 373, 20160485. [Google Scholar] [CrossRef]
- Colombo, M.; Raposo, G.; Théry, C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 2014, 30, 255–289. [Google Scholar] [CrossRef]
- Lazar, I.; Clement, E.; Dauvillier, S.; Milhas, D.; Ducoux-Petit, M.; LeGonidec, S.; Moro, C.; Soldan, V.; Dalle, S.; Balor, S.; et al. Adipocyte Exosomes Promote Melanoma Aggressiveness through Fatty Acid Oxidation: A Novel Mechanism Linking Obesity and Cancer. Cancer Res. 2016, 76, 4051–4057. [Google Scholar] [CrossRef] [Green Version]
- Milane, L.; Singh, A.; Mattheolabakis, G.; Suresh, M.; Amiji, M.M. Exosome mediated communication within the tumor microenvironment. J. Control. Release 2015, 219, 278–294. [Google Scholar] [CrossRef] [PubMed]
- Sun, S.; Wu, Q.; Li, J.; Li, Z.; Sun, S.; Zhu, S.; Wang, L.; Wu, J.; Yuan, J.; Zhang, Y.; et al. Exosomes from the tumour-adipocyte interplay stimulate beige/brown differentiation and reprogram metabolism in stromal adipocytes to promote tumour progression. J. Exp. Clin. Cancer Res. 2019, 38, 223. [Google Scholar] [CrossRef] [Green Version]
- Sagar, G.; Sah, R.P.; Javeed, N.; Dutta, S.K.; Smyrk, T.C.; Lau, J.S.; Giorgadze, N.; Tchkonia, T.; Kirkland, J.L.; Chari, S.T.; et al. Pathogenesis of pancreatic cancer exosome-induced lipolysis in adipose tissue. Gut 2016, 65, 1165–1174. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.; Wu, Y.; Guo, J.; Fei, X.; Yu, L.; Ma, S. Adipocyte-derived exosomes promote lung cancer metastasis by increasing MMP9 activity via transferring MMP3 to lung cancer cells. Oncotarget 2017, 8, 81880–81891. [Google Scholar] [CrossRef]
- Wang, S.; Su, X.; Xu, M.; Xiao, X.; Li, X.; Li, H.; Keating, A.; Zhao, R.C. Exosomes secreted by mesenchymal stromal/stem cell-derived adipocytes promote breast cancer cell growth via activation of Hippo signaling pathway. Stem Cell Res. Ther. 2019, 10, 117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benito-Martin, A.; Paik, P.; Mushannen, M.; Bhardwaj, P.; Oshchepkova, S.; Spector, J.; Brown, K.A. SAT-126 Breast Adipose Tissue Extracellular Vesicles from Obese Women Increase Breast Cancer Aggressiveness—A Novel Mechanism for the Obesity-Breast Cancer Link. J. Endocr. Soc. 2020, 4. [Google Scholar] [CrossRef]
- Clement, E.; Lazar, I.; Attané, C.; Carrié, L.; Dauvillier, S.; Ducoux-Petit, M.; Menneteau, T.; Moutahir, M.; Le Gonidec, S.; Dalle, S.; et al. Adipocyte vesicles: ‘all-in-one’ packages that stimulate tumor mitochondrial metabolism and dynamics. bioRxiv 2019, 649327. [Google Scholar] [CrossRef]
- Balaban, S.; Shearer, R.F.; Lee, L.S.; van Geldermalsen, M.; Schreuder, M.; Shtein, H.C.; Cairns, R.; Thomas, K.C.; Fazakerley, D.J.; Grewal, T.; et al. Adipocyte lipolysis links obesity to breast cancer growth: Adipocyte-derived fatty acids drive breast cancer cell proliferation and migration. Cancer Metab. 2017, 5, 1. [Google Scholar] [CrossRef] [Green Version]
- Kuo, C.Y.; Ann, D.K. When fats commit crimes: Fatty acid metabolism, cancer stemness and therapeutic resistance. Cancer Commun. 2018, 38, 47. [Google Scholar] [CrossRef] [Green Version]
- Skowron, F.; Bérard, F.; Balme, B.; Maucort-Boulch, D. Role of obesity on the thickness of primary cutaneous melanoma. J. Eur. Acad. Dermatol. Venereol. 2015, 29, 262–269. [Google Scholar] [CrossRef]
- Clement, E.; Lazar, I.; Muller, C.; Nieto, L. Obesity and melanoma: Could fat be fueling malignancy? Pigment Cell Melanoma Res. 2017, 30, 294–306. [Google Scholar] [CrossRef] [Green Version]
- Lopatina, T.; Bruno, S.; Tetta, C.; Kalinina, N.; Porta, M.; Camussi, G. Platelet-derived growth factor regulates the secretion of extracellular vesicles by adipose mesenchymal stem cells and enhances their angiogenic potential. Cell Commun. Signal. 2014, 12, 26. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ren, S.; Chen, J.; Duscher, D.; Liu, Y.; Guo, G.; Kang, Y.; Xiong, H.; Zhan, P.; Wang, Y.; Wang, C.; et al. Microvesicles from human adipose stem cells promote wound healing by optimizing cellular functions via AKT and ERK signaling pathways. Stem Cell Res. Ther. 2019, 10, 47. [Google Scholar] [CrossRef] [PubMed]
- An, Y.; Zhao, J.; Nie, F.; Qin, Z.; Xue, H.; Wang, G.; Li, D. Exosomes from Adipose-Derived Stem Cells (ADSCs) Overexpressing miR-21 Promote Vascularization of Endothelial Cells. Sci. Rep. 2019, 9, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Z.; Xu, Y.; Wan, Y.; Gao, J.; Chu, Y.; Li, J. Exosomes from adipose-derived mesenchymal stem cells prevent cardiomyocyte apoptosis induced by oxidative stress. Cell Death Discov. 2019, 5, 1–7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blazquez, R.; Sanchez-Margallo, F.M.; de la Rosa, O.; Dalemans, W.; Álvarez, V.; Tarazona, R.; Casado, J.G. Immunomodulatory potential of human adipose mesenchymal stem cells derived exosomes on in vitro stimulated T cells. Front. Immunol. 2014, 5, 556. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hong, P.; Yang, H.; Wu, Y.; Li, K.; Tang, Z. The functions and clinical application potential of exosomes derived from adipose mesenchymal stem cells: A comprehensive review. Stem Cell Res. Ther. 2019, 10, 1–12. [Google Scholar] [CrossRef]
- Gernapudi, R.; Yao, Y.; Zhang, Y.; Wolfson, B.; Roy, S.; Duru, N.; Eades, G.; Yang, P.; Zhou, Q. Targeting exosomes from preadipocytes inhibits preadipocyte to cancer stem cell signaling in early-stage breast cancer. Breast Cancer Res. Treat. 2015, 150, 685–695. [Google Scholar] [CrossRef] [Green Version]
- Lin, R.; Wang, S.; Zhao, R.C. Exosomes from human adipose-derived mesenchymal stem cells promote migration through Wnt signaling pathway in a breast cancer cell model. Mol. Cell. Biochem. 2013, 383, 13–20. [Google Scholar] [CrossRef]
- Zhan, T.; Rindtorff, N.; Boutros, M. Wnt signaling in cancer. Oncogene 2017, 36, 1461–1473. [Google Scholar] [CrossRef]
- Wang, Y.; Chu, Y.; Li, K.; Zhang, G.; Guo, Z.; Wu, X.; Qiu, C.; Li, Y.; Wan, X.; Sui, J.; et al. Exosomes Secreted by Adipose-Derived Mesenchymal Stem Cells Foster Metastasis and Osteosarcoma Proliferation by Increasing COLGALT2 Expression. Front. Cell Dev. Biol. 2020, 8, 353. [Google Scholar] [CrossRef] [PubMed]
- Otvos, L.; Haspinger, E.; La Russa, F.; Maspero, F.; Graziano, P.; Kovalszky, I.; Lovas, S.; Nama, K.; Hoffmann, R.; Knappe, D.; et al. Design and development of a peptide-based adiponectin receptor agonist for cancer treatment. BMC Biotechnol. 2011, 11, 90. [Google Scholar] [CrossRef] [Green Version]
- Gelsomino, L.; Naimo, G.D.; Catalano, S.; Mauro, L.; Andò, S. The emerging role of adiponectin in female malignancies. Int. J. Mol. Sci. 2019, 20, 2127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Silva, F.M.; De Almeida, J.C.; Feoli, A.M. Effect of diet on adiponectin levels in blood. Nutr. Rev. 2011, 69, 599–612. [Google Scholar] [CrossRef] [PubMed]
- Kriketos, A.D.; Gan, S.K.; Poynten, A.M.; Furler, S.M.; Chisholm, D.J.; Campbell, L.V. Exercise Increases Adiponectin Levels and Insulin Sensitivity in Humans. Diabetes Care 2004, 27, 629–630. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giordano, C.; Chemi, F.; Panza, S.; Barone, I.; Bonofiglio, D.; Lanzino, M.; Cordella, A.; Campana, A.; Hashim, A.; Rizza, P.; et al. Leptin as a mediator of tumor-stromal interactions promotes breast cancer stem cell activity. Oncotarget 2016, 7, 1262–1275. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otvos, L.; Kovalszky, I.; Riolfi, M.; Ferla, R.; Olah, J.; Sztodola, A.; Nama, K.; Molino, A.; Piubello, Q.; Wade, J.D.; et al. Efficacy of a leptin receptor antagonist peptide in a mouse model of triple-negative breast cancer. Eur. J. Cancer 2011, 47, 1578–1584. [Google Scholar] [CrossRef] [PubMed]
- Ferla, R.; Bonomi, M.; Otvos, L.; Surmacz, E. Glioblastoma-derived Leptin Induces Tube Formation and Growth of Endothelial Cells: Comparison with VEGF Effects. BMC Cancer 2011, 11, 303. [Google Scholar] [CrossRef] [Green Version]
- Otvos, L.; Surmacz, E. Targeting the leptin receptor: A potential new mode of treatment for breast cancer. Expert Rev. Anticancer Ther. 2011, 11, 1147–1150. [Google Scholar] [CrossRef]
- Johnson, D.E.; O’Keefe, R.A.; Grandis, J.R. Targeting the IL-6/JAK/STAT3 signalling axis in cancer. Nat. Rev. Clin. Oncol. 2018, 15, 234–248. [Google Scholar] [CrossRef]
- Guo, C.; Chen, Y.; Gao, W.; Chang, A.; Ye, Y.; Shen, W.; Luo, Y.; Yang, S.; Sun, P.; Xiang, R.; et al. Liposomal nanoparticles carrying anti-IL6R antibody to the tumour microenvironment inhibit metastasis in two molecular subtypes of breast cancer mouse models. Theranostics 2017, 7, 775–788. [Google Scholar] [CrossRef] [PubMed]
- Holen, I.; Lefley, D.V.; Francis, S.E.; Rennicks, S.; Bradbury, S.; Coleman, R.E.; Ottewell, P. IL-1 drives breast cancer growth and bone metastasis in vivo. Oncotarget 2016, 7, 75571–75584. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lust, J.A.; Lacy, M.Q.; Zeldenrust, S.R.; Dispenzieri, A.; Gertz, M.A.; Witzig, T.E.; Kumar, S.; Hayman, S.R.; Russell, S.J.; Buadi, F.K.; et al. Induction of a chronic disease state in patients with smoldering or indolent multiple myeloma by targeting interleukin 1β-induced interleukin 6 production and the myeloma proliferative component. Mayo Clin. Proc. 2009, 84, 114–122. [Google Scholar] [CrossRef] [PubMed]
- Ridker, P.M.; MacFadyen, J.G.; Thuren, T.; Everett, B.; Libby, P.; Glynn, R.J.; Ridker, P.; Lorenzatti, A.; Krum, H.; Varigos, J.; et al. Effect of interleukin-1β inhibition with canakinumab on incident lung cancer in patients with atherosclerosis: Exploratory results from a randomised, double-blind, placebo-controlled trial. Lancet 2017, 390, 1833–1842. [Google Scholar] [CrossRef]
- Baker, K.J.; Houston, A.; Brint, E. IL-1 family members in cancer; two sides to every story. Front. Immunol. 2019, 10, 1197. [Google Scholar] [CrossRef] [Green Version]
- Castaño, Z.; Juan, B.P.S.; Spiegel, A.; Pant, A.; DeCristo, M.J.; Laszewski, T.; Ubellacker, J.M.; Janssen, S.R.; Dongre, A.; Reinhardt, F.; et al. IL-1β inflammatory response driven by primary breast cancer prevents metastasis-initiating cell colonization. Nat. Cell Biol. 2018, 20, 1084–1097. [Google Scholar] [CrossRef]
- Lashinger, L.M.; Rossi, E.L.; Hursting, S.D. Obesity and resistance to cancer chemotherapy: Interacting roles of inflammation and metabolic dysregulation. Clin. Pharmacol. Ther. 2014, 96, 458–463. [Google Scholar] [CrossRef]
- Wang, Z.; Aguilar, E.G.; Luna, J.I.; Dunai, C.; Khuat, L.T.; Le, C.T.; Mirsoian, A.; Minnar, C.M.; Stoffel, K.M.; Sturgill, I.R.; et al. Paradoxical effects of obesity on T cell function during tumor progression and PD-1 checkpoint blockade. Nat. Med. 2019, 25, 141–151. [Google Scholar] [CrossRef]
- McQuade, J.L.; Daniel, C.R.; Hess, K.R.; Mak, C.; Wang, D.Y.; Rai, R.R.; Park, J.J.; Haydu, L.E.; Spencer, C.; Wongchenko, M.; et al. Association of body-mass index and outcomes in patients with metastatic melanoma treated with targeted therapy, immunotherapy, or chemotherapy: A retrospective, multicohort analysis. Lancet Oncol. 2018, 19, 310–322. [Google Scholar] [CrossRef] [Green Version]
- Vonderheide, R.H.; Domchek, S.M.; Clark, A.S. Immunotherapy for breast cancer: What are we missing? Clin. Cancer Res. 2017, 23, 2640–2646. [Google Scholar] [CrossRef] [Green Version]
- Dirix, L.Y.; Takacs, I.; Jerusalem, G.; Nikolinakos, P.; Arkenau, H.T.; Forero-Torres, A.; Boccia, R.; Lippman, M.E.; Somer, R.; Smakal, M.; et al. Avelumab, an anti-PD-L1 antibody, in patients with locally advanced or metastatic breast cancer: A phase 1b JAVELIN solid tumor study. Breast Cancer Res. Treat. 2018, 167, 671–686. [Google Scholar] [CrossRef] [Green Version]
- Naik, A.; Monjazeb, A.M.; Decock, J. The obesity paradox in cancer, tumor immunology, and immunotherapy: Potential therapeutic implications in triple negative breast cancer. Front. Immunol. 2019, 10, 1940. [Google Scholar] [CrossRef] [PubMed]
- Mirsoian, A.; Bouchlaka, M.N.; Sckisel, G.D.; Chen, M.; Pai, C.C.S.; Maverakis, E.; Spencer, R.G.; Fishbein, K.W.; Siddiqui, S.; Monjazeb, A.M.; et al. Adiposity induces lethal cytokine storm after systemic administration of stimulatory immunotherapy regimens in aged mice. J. Exp. Med. 2014, 211, 2373–2383. [Google Scholar] [CrossRef] [PubMed]
- Furuhashi, M.; Hotamisligil, G.S. Fatty acid-binding proteins: Role in metabolic diseases and potential as drug targets. Nat. Rev. Drug Discov. 2008, 7, 489–503. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carbonetti, G.; Wilpshaar, T.; Kroonen, J.; Studholme, K.; Converso, C.; d’Oelsnitz, S.; Kaczocha, M. FABP5 coordinates lipid signaling that promotes prostate cancer metastasis. Sci. Rep. 2019, 9. [Google Scholar] [CrossRef] [Green Version]
- O’Sullivan, S.E.; Kaczocha, M. FABP5 as a novel molecular target in prostate cancer. Drug Discov. Today 2020. [Google Scholar] [CrossRef]
- Field, C.S.; Baixauli, F.; Kyle, R.L.; Pearce, E.J.; Blazar, B.R.; Pearce, E.L. Mitochondrial Integrity Regulated by Lipid Metabolism Is a Cell-Intrinsic Checkpoint for Treg Suppressive Function. Cell Metab. 2020, 31, 422–437. [Google Scholar] [CrossRef] [Green Version]
- Verma, A.; Mathur, R.; Farooque, A.; Kaul, V.; Gupta, S.; Dwarakanath, B.S. T-regulatory cells in tumor progression and therapy. Cancer Manag. Res. 2019, 11, 10731–10747. [Google Scholar] [CrossRef] [Green Version]
- Wang, J.; Li, Y. CD36 tango in cancer: Signaling pathways and functions. Theranostics 2019, 9, 4893–4908. [Google Scholar] [CrossRef]
- Pascual, G.; Avgustinova, A.; Mejetta, S.; Martín, M.; Castellanos, A.; Attolini, C.S.O.; Berenguer, A.; Prats, N.; Toll, A.; Hueto, J.A.; et al. Targeting metastasis-initiating cells through the fatty acid receptor CD36. Nature 2017, 541, 41–45. [Google Scholar] [CrossRef]
- DeFilippis, R.A.; Chang, H.; Dumont, N.; Rabban, J.T.; Chen, Y.Y.; Fontenay, G.V.; Berman, H.K.; Gauthier, M.L.; Zhao, J.; Hu, D.; et al. CD36 repression activates a multicellular stromal program shared by high mammographic density and tumor tissues. Cancer Discov. 2012, 2, 826–839. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Enciu, A.M.; Radu, E.; Popescu, I.D.; Hinescu, M.E.; Ceafalan, L.C. Targeting CD36 as Biomarker for Metastasis Prognostic: How Far from Translation into Clinical Practice? BioMed Res. Int. 2018, 2018. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ehsanipour, E.A.; Sheng, X.; Behan, J.W.; Wang, X.; Butturini, A.; Avramis, V.I.; Mittelman, S.D. Adipocytes cause leukemia cell resistance to l-asparaginase via release of glutamine. Cancer Res. 2013, 73, 2998–3006. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nikonorova, I.A.; Al-Baghdadi, R.J.T.; Mirek, E.T.; Wang, Y.; Goudie, M.P.; Wetstein, B.B.; Dixon, J.L.; Hine, C.; Mitchell, J.R.; Adams, C.M.; et al. Obesity challenges the hepatoprotective function of the integrated stress response to asparaginase exposure in mice. J. Biol. Chem. 2017, 292, 6786–6798. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, J.; Deng, Y.; Khoo, B.L. Fasting to enhance Cancer treatment in models: The next steps. J. Biomed. Sci. 2020, 27, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Quail, D.F.; Olson, O.C.; Bhardwaj, P.; Walsh, L.A.; Akkari, L.; Quick, M.L.; Chen, I.C.; Wendel, N.; Ben-Chetrit, N.; Walker, J.; et al. Obesity alters the lung myeloid cell landscape to enhance breast cancer metastasis through IL5 and GM-CSF. Nat. Cell Biol. 2017, 19, 974–987. [Google Scholar] [CrossRef]
- Nagase, H.; Ueki, S.; Fujieda, S. The roles of IL-5 and anti-IL-5 treatment in eosinophilic diseases: Asthma, eosinophilic granulomatosis with polyangiitis, and eosinophilic chronic rhinosinusitis. Allergol. Int. 2020, 69, 178–186. [Google Scholar] [CrossRef]
- Sirin, O.; Kolonin, M.G. Treatment of obesity as a potential complementary approach to cancer therapy. Drug Discov. Today 2013, 18, 567–573. [Google Scholar] [CrossRef]
- Lv, M.; Zhu, X.; Wang, H.; Wang, F.; Guan, W. Roles of Caloric Restriction, Ketogenic Diet and Intermittent Fasting during Initiation, Progression and Metastasis of Cancer in Animal Models: A Systematic Review and Meta-Analysis. PLoS ONE 2014, 9, e115147. [Google Scholar] [CrossRef]
- O’Flanagan, C.H.; Smith, L.A.; McDonell, S.B.; Hursting, S.D. When less may be more: Calorie restriction and response to cancer therapy. BMC Med. 2017, 15. [Google Scholar] [CrossRef]
- De Groot, S.; Pijl, H.; Van Der Hoeven, J.J.M.; Kroep, J.R. Effects of short-term fasting on cancer treatment. J. Exp. Clin. Cancer Res. 2019, 38, 1–14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bonsang-Kitzis, H.; Chaltier, L.; Belin, L.; Savignoni, A.; Rouzier, R.; Sablin, M.-P.; Lerebours, F.; Bidard, F.-C.; Cottu, P.; Sastre-Garau, X.; et al. Beyond Axillary Lymph Node Metastasis, BMI and Menopausal Status Are Prognostic Determinants for Triple-Negative Breast Cancer Treated by Neoadjuvant Chemotherapy. PLoS ONE 2015, 10, e0144359. [Google Scholar] [CrossRef] [PubMed]
- Litton, J.K.; Gonzalez-Angulo, A.M.; Warneke, C.L.; Buzdar, A.U.; Kau, S.W.; Bondy, M.; Mahabir, S.; Hortobagyi, G.N.; Brewster, A.M. Relationship between obesity and pathologic response to neoadjuvant chemotherapy among women with operable breast cancer. J. Clin. Oncol. 2008, 26, 4072–4077. [Google Scholar] [CrossRef]
- De Azambuja, E.; McCaskill-Stevens, W.; Francis, P.; Quinaux, E.; Crown, J.P.A.; Vicente, M.; Giuliani, R.; Nordenskjöld, B.; Gutiérez, J.; Andersson, M.; et al. The effect of body mass index on overall and disease-free survival in node-positive breast cancer patients treated with docetaxel and doxorubicin-containing adjuvant chemotherapy: The experience of the BIG 02-98 trial. Breast Cancer Res. Treat. 2010, 119, 145–153. [Google Scholar] [CrossRef] [Green Version]
- Kusuoka, O.; Fujiwara-Tani, R.; Nakashima, C.; Fujii, K.; Ohmori, H.; Mori, T.; Kishi, S.; Miyagawa, Y.; Goto, K.; Kawahara, I.; et al. Intermittent calorie restriction enhances epithelial-mesenchymal transition through the alteration of energy metabolism in a mouse tumor model. Int. J. Oncol. 2018, 52, 413–423. [Google Scholar] [CrossRef] [PubMed]
- Schmid, D.; Leitzmann, M.F. Association between physical activity and mortality among breast cancer and colorectal cancer survivors: A systematic review and meta-analysis. Ann. Oncol. 2014, 25, 1293–1311. [Google Scholar] [CrossRef]
- De ten Ryen, S.D.; Deldicque, L. The regulation of the metastatic cascade by physical activity: A narrative review. Cancers 2020, 12, 153. [Google Scholar] [CrossRef] [Green Version]
- Buss, L.A.; Dachs, G.U. Effects of Exercise on the Tumour Microenvironment. In Advances in Experimental Medicine and Biology; Springer: Berlin/Heidelberg, Germany, 2020; Volume 1225, pp. 31–51. [Google Scholar]
- Faustino-Rocha, A.I.; Silva, A.; Gabriel, J.; da Costa, R.M.G.; Moutinho, M.; Oliveira, P.A.; Gama, A.; Ferreira, R.; Ginja, M. Long-term exercise training as a modulator of mammary cancer vascularization. Biomed. Pharmacother. 2016, 81, 273–280. [Google Scholar] [CrossRef] [Green Version]
- Jones, L.W.; Fels, D.R.; West, M.; Allen, J.D.; Broadwater, G.; Barry, W.T.; Wilke, L.G.; Masko, E.; Douglas, P.S.; Dash, R.C.; et al. Modulation of circulating angiogenic factors and tumor biology by aerobic training in breast cancer patients receiving neoadjuvant chemotherapy. Cancer Prev. Res. 2013, 6, 925–937. [Google Scholar] [CrossRef] [Green Version]
- Dieli-Conwright, C.M.; Courneya, K.S.; Demark-Wahnefried, W.; Sami, N.; Lee, K.; Buchanan, T.A.; Spicer, D.V.; Tripathy, D.; Bernstein, L.; Mortimer, J.E. Effects of aerobic and resistance exercise on metabolic syndrome, sarcopenic obesity, and circulating biomarkers in overweight or obese survivors of breast cancer: A randomized controlled trial. J. Clin. Oncol. 2018, 36, 875–883. [Google Scholar] [CrossRef]
- Sjöström, L.; Gummesson, A.; Sjöström, C.D.; Narbro, K.; Peltonen, M.; Wedel, H.; Bengtsson, C.; Bouchard, C.; Carlsson, B.; Dahlgren, S.; et al. Effects of bariatric surgery on cancer incidence in obese patients in Sweden (Swedish Obese Subjects Study): A prospective, controlled intervention trial. Lancet Oncol. 2009, 10, 653–662. [Google Scholar] [CrossRef]
- Schauer, D.P.; Feigelson, H.S.; Koebnick, C.; Caan, B.; Weinmann, S.; Leonard, A.C.; Powers, J.D.; Yenumula, P.R.; Arterburn, D.E. Bariatric Surgery and the Risk of Cancer in a Large Multisite Cohort. Ann. Surg. 2019, 269, 95–101. [Google Scholar] [CrossRef] [PubMed]
- Castagneto-Gissey, L.; Casella-Mariolo, J.; Casella, G.; Mingrone, G. Obesity Surgery and Cancer: What Are the Unanswered Questions? Front. Endocrinol. 2020, 11, 213. [Google Scholar] [CrossRef] [PubMed]
- Bruno, D.S.; Berger, N.A. Impact of bariatric surgery on cancer risk reduction. Ann. Transl. Med. 2020, 8, S13. [Google Scholar] [CrossRef]
- Sainsbury, A.; Goodlad, R.A.; Perry, S.L.; Pollard, S.G.; Robins, G.G.; Hull, M.A. Increased colorectal epithelial cell proliferation and crypt fission associated with obesity and Roux-en-Y gastric bypass. Cancer Epidemiol. Biomark. Prev. 2008, 17, 1401–1410. [Google Scholar] [CrossRef] [Green Version]
- Philip, E.J.; Torghabeh, M.H.; Strain, G.W. Bariatric surgery in cancer survivorship: Does a history of cancer affect weight loss outcomes? Surg. Obes. Relat. Dis. 2015, 11, 1105–1108. [Google Scholar] [CrossRef] [Green Version]
- MacKintosh, M.L.; Derbyshire, A.E.; McVey, R.J.; Bolton, J.; Nickkho-Amiry, M.; Higgins, C.L.; Kamieniorz, M.; Pemberton, P.W.; Kirmani, B.H.; Ahmed, B.; et al. The impact of obesity and bariatric surgery on circulating and tissue biomarkers of endometrial cancer risk. Int. J. Cancer 2019, 144, 641–650. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Annett, S.; Moore, G.; Robson, T. Obesity and Cancer Metastasis: Molecular and Translational Perspectives. Cancers 2020, 12, 3798. https://doi.org/10.3390/cancers12123798
Annett S, Moore G, Robson T. Obesity and Cancer Metastasis: Molecular and Translational Perspectives. Cancers. 2020; 12(12):3798. https://doi.org/10.3390/cancers12123798
Chicago/Turabian StyleAnnett, Stephanie, Gillian Moore, and Tracy Robson. 2020. "Obesity and Cancer Metastasis: Molecular and Translational Perspectives" Cancers 12, no. 12: 3798. https://doi.org/10.3390/cancers12123798