The Effects of Adipocytes on the Regulation of Breast Cancer in the Tumor Microenvironment: An Update
Abstract
:1. Introduction
2. Adipocytes Regulate Breast Cancer via Their Metabolic Substrates
3. Adipocytes Regulate Breast Cancer via Their Released Hormones
4. Adipocytes Regulate Breast Cancer via Released Cytokines
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- DeSantis, C.E.; Ma, J.; Sauer, A.G.; Newman, L.A.; Jemal, A. Breast cancer statistics, 2017, racial disparity in mortality by state. CA A Cancer J. Clin. 2017, 67, 439–448. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA A Cancer J Clin. 2018, 68, 394–424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fan, L.; Strasser-Weippl, K.; Li, J.-J.; St Louis, J.; Finkelstein, D.M.; Yu, K.-D.; Chen, W.-Q.; Shao, Z.-M.; Goss, P.E. Breast cancer in China. Lancet Oncol. 2014, 15, e279–e289. [Google Scholar] [CrossRef]
- Kops, N.L.; Bessel, M.; Caleffi, M.; Ribeiro, R.A.; Wendland, E.M. Body Weight and Breast Cancer: Nested Case–Control Study in Southern Brazil. Clin. Breast Cancer 2018, 18, e797–e803. [Google Scholar] [CrossRef] [PubMed]
- De Silva, S.; Tennekoon, K.H.; Karunanayake, E.H. Overview of the genetic basis toward early detection of breast cancer. Breast Cancer Targets Ther. 2019, 11, 71. [Google Scholar] [CrossRef]
- Chu, D.-T.; Nguyet, N.T.M.; Dinh, T.C.; Lien, N.V.T.; Nguyen, K.-H.; Ngoc, V.T.N.; Tao, Y.; Le, D.-H.; Nga, V.B.; Jurgoński, A. An update on physical health and economic consequences of overweight and obesity. Diabetes Metab. Syndr. Clin. Res. Rev. 2018, 12, 1095–1100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schottenfeld, D.; Beebe-Dimmer, J.L.; Buffler, P.A.; Omenn, G.S. Current perspective on the global and United States cancer burden attributable to lifestyle and environmental risk factors. Annu. Rev. Public Health 2013, 34, 97–117. [Google Scholar] [CrossRef]
- Picon-Ruiz, M.; Morata-Tarifa, C.; Valle-Goffin, J.J.; Friedman, E.R.; Slingerland, J.M. Obesity and adverse breast cancer risk and outcome: Mechanistic insights and strategies for intervention. CA A Cancer J. Clin. 2017, 67, 378–397. [Google Scholar] [CrossRef]
- Engin, A. Obesity-associated Breast Cancer: Analysis of risk factors. In Obesity and Lipotoxicity; Engin, A.B., Engin, A., Eds.; Springer International Publishing: Cham, Germany, 2017; pp. 571–606. [Google Scholar]
- Kolb, R.; Phan, L.; Borcherding, N.; Liu, Y.; Yuan, F.; Janowski, A.M.; Xie, Q.; Markan, K.R.; Li, W.; Potthoff, M.J.; et al. Obesity-associated NLRC4 inflammasome activation drives breast cancer progression. Nat. Commun. 2016, 7, 13007. [Google Scholar] [CrossRef]
- Chan, D.S.M.; Vieira, A.R.; Aune, D.; Bandera, E.V.; Greenwood, D.C.; McTiernan, A.; Navarro Rosenblatt, D.; 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]
- Bhaskaran, K.; Douglas, I.; Forbes, H.; dos-Santos-Silva, I.; Leon, D.A.; Smeeth, L. Body-mass index and risk of 22 specific cancers: A population-based cohort study of 5·24 million UK adults. Lancet 2014, 384, 755–765. [Google Scholar] [CrossRef]
- Singh, P.; Kapil, U.; Shukla, N.K.; Deo, S.V.S.; Dwivedi, S.N. Association of overweight and obesity with breast cancer in India. Indian J. Community Med. Off. Publ. Indian Assoc. Prev. Soc. Med. 2011, 36, 259. [Google Scholar]
- Rabiepoor, S.; Khalkhali, H.R.; Sadeghi, E. What kind of sexual dysfunction is most common among overweight and obese women in reproductive age? Int. J. Impot. Res. 2017, 29, 61. [Google Scholar] [CrossRef] [PubMed]
- Veronelli, A.; Mauri, C.; Zecchini, B.; Peca, M.G.; Turri, O.; Valitutti, M.T.; Dall’Asta, C.; Pontiroli, A.E. Sexual Dysfunction Is Frequent in Premenopausal Women with Diabetes, Obesity, and Hypothyroidism, and Correlates with Markers of Increased Cardiovascular Risk. A Preliminary Report. J. Sex. Med. 2009, 6, 1561–1568. [Google Scholar] [CrossRef] [PubMed]
- Freeman, E.W.; Gracia, C.R.; Sammel, M.D.; Lin, H.; Lim, L.C.-L.; Strauss Iii, J.F. Association of anti-mullerian hormone levels with obesity in late reproductive-age women. Fertil. Steril. 2007, 87, 101–106. [Google Scholar] [CrossRef] [PubMed]
- Kerr, J.; Anderson, C.; Lippman, S.M. Physical activity, sedentary behaviour, diet, and cancer: An update and emerging new evidence. Lancet Oncol. 2017, 18, e457–e471. [Google Scholar] [CrossRef]
- Renehan, A.G.; Roberts, D.L.; Dive, C. Obesity and cancer: Pathophysiological and biological mechanisms. Arch. Physiol. Biochem. 2008, 114, 71–83. [Google Scholar] [CrossRef] [PubMed]
- National Cancer Institute. SEER Stat Fact Sheets: Female Breast Cancer; National Cancer Institute: Bethesda, MD, USA. Available online: https://seer.cancer.gov/statfacts/html/breast.html (accessed on 1 June 2019).
- Winkels, R.M.; Beijer, S.; van Lieshout, R.; van Barneveld, D.; Hofstede, J.; Kuiper, J.; Vreugdenhil, A.; van Warmerdam, L.J.C.; Schep, G.; Blaisse, R.; et al. Changes in body weight during various types of chemotherapy in breast cancer patients. e-SPEN J. 2014, 9, e39–e44. [Google Scholar] [CrossRef] [Green Version]
- Pedersen, B.; Delmar, C.; Lörincz, T.; Falkmer, U.; Grønkjær, M. Investigating Changes in Weight and Body Composition Among Women in Adjuvant Treatment for Breast Cancer: A Scoping Review. Cancer Nurs. 2019, 42, 91–105. [Google Scholar] [CrossRef]
- Caan, B.J.; Kwan, M.L.; Shu, X.O.; Pierce, J.P.; Patterson, R.E.; Nechuta, S.J.; Poole, E.M.; Kroenke, C.H.; Weltzien, E.K.; Flatt, S.W.; et al. Weight Change and Survival after Breast Cancer in the After Breast Cancer Pooling Project. Cancer Epidemiol. Biomark. Prev. 2012, 21, 1260–1271. [Google Scholar] [CrossRef] [Green Version]
- Reddy, S.M.; Sadim, M.; Li, J.; Yi, N.; Agarwal, S.; Mantzoros, C.S.; Kaklamani, V.G. Clinical and genetic predictors of weight gain in patients diagnosed with breast cancer. Br. J. Cancer 2013, 109, 872. [Google Scholar] [CrossRef] [PubMed]
- Chu, D.-T.; Tao, Y.; Taskén, K. OPA1 in Lipid Metabolism: Function of OPA1 in Lipolysis and Thermogenesis of Adipocytes. Horm. Metab. Res. 2017, 49, 276–285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chu, D.-T.; Tao, Y. Human thermogenic adipocytes: A reflection on types of adipocyte, developmental origin, and potential application. J. Physiol. Biochem. 2017, 73, 1–4. [Google Scholar] [CrossRef] [PubMed]
- Chu, D.-T.; Tao, Y.; Son, L.H.; Le, D.-H. Cell source, differentiation, functional stimulation, and potential application of human thermogenic adipocytes in vitro. J. Physiol. Biochem. 2016, 73, 315–321. [Google Scholar] [CrossRef] [PubMed]
- Chu, D.-T.; Gawronska-Kozak, B. Brown and brite adipocytes: Same function, but different origin and response. Biochimie 2017, 138, 102–105. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ackerman, S.E.; Blackburn, O.A.; Marchildon, F.; Cohen, P. Insights into the Link Between Obesity and Cancer. Curr. Obes. Rep. 2017, 6, 195–203. [Google Scholar] [PubMed]
- Zhang, Z.; Scherer, P.E. The dysfunctional adipocyte—a cancer cell’s best friend. Nat. Rev. Endocrinol. 2018, 14, 132. [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]
- Cozzo, A.J.; Fuller, A.M.; Makowski, L. Contribution of Adipose Tissue to Development of Cancer. Compr. Physiol. 2017, 8, 237–282. [Google Scholar] [CrossRef]
- Lehr, S.; Hartwig, S.; Sell, H. Adipokines: A treasure trove for the discovery of biomarkers for metabolic disorders. PROTEOMICS–Clin. Appl. 2012, 6, 91–101. [Google Scholar] [CrossRef]
- Goodwin, P.J.; Stambolic, V. Impact of the obesity epidemic on cancer. Annu. Rev. Med. 2015, 66, 281–296. [Google Scholar] [CrossRef] [PubMed]
- Sheng, X.; Parmentier, J.-H.; Tucci, J.; Pei, H.; Cortez-Toledo, O.; Dieli-Conwright, C.M.; Oberley, M.J.; Neely, M.; Orgel, E.; Louie, S.G. Adipocytes sequester and metabolize the chemotherapeutic daunorubicin. Mol. Cancer Res. 2017, 15, 1704–1713. [Google Scholar] [CrossRef] [PubMed]
- Sun, K.; Tordjman, J.; Clément, K.; Scherer, P.E. Fibrosis and adipose tissue dysfunction. Cell Metab. 2013, 18, 470–477. [Google Scholar] [CrossRef] [PubMed]
- Chu, D.T.; Nguyet, N.T.M.; Nga, V.T.; Thai Lien, N.V.; Vo, D.D.; Lien, N.; Nhu Ngoc, V.T.; Son, L.H.; Le, D.-H.; Nga, V.B.; et al. An update on obesity: Mental consequences and psychological interventions. Diabetes Metab. Syndr. Clin. Res. Rev. 2019, 13, 155–160. [Google Scholar] [CrossRef] [PubMed]
- Baek, A.E.; Nelson, E.R. The Contribution of Cholesterol and Its Metabolites to the Pathophysiology of Breast Cancer. Horm. Cancer 2016, 7, 219–228. [Google Scholar] [CrossRef] [Green Version]
- Garcia-Estevez, L.; Moreno-Bueno, G. Updating the role of obesity and cholesterol in breast cancer. Breast Cancer Res. 2019, 21, 35. [Google Scholar] [CrossRef] [PubMed]
- Gilbert, C.A.; Slingerland, J.M. Cytokines, obesity, and cancer: New insights on mechanisms linking obesity to cancer risk and progression. Annu. Rev. Med. 2013, 64, 45–57. [Google Scholar] [CrossRef]
- Gunter, M.J.; Hoover, D.R.; Yu, H.; Wassertheil-Smoller, S.; Rohan, T.E.; Manson, J.E.; Li, J.; Ho, G.Y.F.; Xue, X.; Anderson, G.L.; et al. Insulin, insulin-like growth factor-I, and risk of breast cancer in postmenopausal women. J. Natl. Cancer Inst. 2009, 101, 48–60. [Google Scholar] [CrossRef]
- He, S.; Nelson, E.R. 27-Hydroxycholesterol, an endogenous selective estrogen receptor modulator. Maturitas 2017, 104, 29–35. [Google Scholar] [CrossRef]
- Kimbung, S.; Chang, C.-Y.; Bendahl, P.-O.; Dubois, L.; Thompson, J.W.; McDonnell, D.P.; Borgquist, S. Impact of 27-hydroxylase (CYP27A1) and 27-hydroxycholesterol in breast cancer. Endocr. Relat. Cancer 2017, 24, 339–349. [Google Scholar] [CrossRef]
- Liu, J.; Ma, D.W.L. The role of n-3 polyunsaturated fatty acids in the prevention and treatment of breast cancer. Nutrients 2014, 6, 5184–5223. [Google Scholar] [CrossRef] [PubMed]
- Lu, C.-W.; Lo, Y.-H.; Chen, C.-H.; Lin, C.-Y.; Tsai, C.-H.; Chen, P.-J.; Yang, Y.-F.; Wang, C.-H.; Tan, C.-H.; Hou, M.-F.; et al. VLDL and LDL, but not HDL, promote breast cancer cell proliferation, metastasis and angiogenesis. Cancer Lett. 2017, 388, 130–138. [Google Scholar] [CrossRef] [PubMed]
- Monk, J.M.; Turk, H.F.; Liddle, D.M.; De Boer, A.A.; Power, K.A.; Ma, D.W.L.; Robinson, L.E. n-3 polyunsaturated fatty acids and mechanisms to mitigate inflammatory paracrine signaling in obesity-associated breast cancer. Nutrients 2014, 6, 4760–4793. [Google Scholar] [CrossRef] [PubMed]
- Parrales, A.; Ranjan, A.; Iwakuma, T. Unsaturated fatty acids regulate stemness of ovarian cancer cells through NF-κB. Stem Cell Investig. 2017, 4, 49. [Google Scholar] [CrossRef] [PubMed]
- Rose, D.P.; Connolly, J.M. Effects of fatty acids and inhibitors of eicosanoid synthesis on the growth of a human breast cancer cell line in culture. Cancer Res. 1990, 50, 7139–7144. [Google Scholar] [PubMed]
- Thomou, T.; Mori, M.A.; Dreyfuss, J.M.; Konishi, M.; Sakaguchi, M.; Wolfrum, C.; Rao, T.N.; Winnay, J.N.; Garcia-Martin, R.; Grinspoon, S.K. Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature 2017, 542, 450. [Google Scholar] [CrossRef] [PubMed]
- Stoll, B.A. N-3 fatty acids and lipid peroxidation in breast cancer inhibition. Br. J. Nutr. 2002, 87, 193–198. [Google Scholar] [CrossRef]
- Rajarajan, D.; Selvarajan, S.; Charan Raja, M.R.; Kar Mahapatra, S.; Kasiappan, R. Genome-wide analysis reveals miR-3184-5p and miR-181c-3p as a critical regulator for adipocytes-associated breast cancer. J. Cell. Physiol. 2019. [Google Scholar] [CrossRef]
- Liu, T.-W.; Heden, T.D.; Matthew Morris, E.; Fritsche, K.L.; Vieira-Potter, V.J.; Thyfault, J.P. High-Fat Diet Alters Serum Fatty Acid Profiles in Obesity Prone Rats: Implications for In Vitro Studies. Lipids 2015, 50, 997–1008. [Google Scholar] [CrossRef]
- Raatz, S.K.; Bibus, D.; Thomas, W.; Kris-Etherton, P. Total Fat Intake Modifies Plasma Fatty Acid Composition in Humans. J. Nutr. 2001, 131, 231–234. [Google Scholar] [CrossRef]
- Vigushin, D.M.; Dong, Y.; Inman, L.; Peyvandi, N.; Alao, J.P.; Sun, C.; Ali, S.; Niesor, E.J.; Bentzen, C.L.; Coombes, R.C. The nuclear oxysterol receptor LXRα is expressed in the normal human breast and in breast cancer. Med Oncol. 2004, 21, 123–131. [Google Scholar] [CrossRef]
- Morris, P.G.; Hudis, C.A.; Giri, D.; Morrow, M.; Falcone, D.J.; Zhou, X.K.; Du, B.; Brogi, E.; Crawford, C.B.; Kopelovich, L.; et al. Inflammation and increased aromatase expression occur in the breast tissue of obese women with breast cancer. Cancer Prev. Res. 2011, 4, 1021–1029. [Google Scholar] [CrossRef] [PubMed]
- Iyengar, N.M.; Ghossein, R.A.; Morris, L.G.; Zhou, X.K.; Kochhar, A.; Morris, P.G.; Pfister, D.G.; Patel, S.G.; Boyle, J.O.; Hudis, C.A.; et al. White adipose tissue inflammation and cancer-specific survival in patients with squamous cell carcinoma of the oral tongue. Cancer 2016, 122, 3794–3802. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Subbaramaiah, K.; Howe, L.R.; Bhardwaj, P.; Du, B.; Gravaghi, C.; Yantiss, R.K.; Zhou, X.K.; Blaho, V.A.; Hla, T.; Yang, P.; et al. Obesity is associated with inflammation and elevated aromatase expression in the mouse mammary gland. Cancer Prev. Res. 2011, 4, 329–346. [Google Scholar] [CrossRef] [PubMed]
- Soto-Guzman, A.; Navarro-Tito, N.; Castro-Sanchez, L.; Martinez-Orozco, R.; Salazar, E.P. Oleic acid promotes MMP-9 secretion and invasion in breast cancer cells. Clin. Exp. Metastasis 2010, 27, 505–515. [Google Scholar] [CrossRef] [PubMed]
- Hardy, S.; Langelier, Y.; Prentki, M. Oleate Activates Phosphatidylinositol 3-Kinase and Promotes Proliferation and Reduces Apoptosis of MDA-MB-231 Breast Cancer Cells, Whereas Palmitate Has Opposite Effects 1. Cancer Res. 2000, 60, 6353. [Google Scholar] [PubMed]
- Cleofas, M.-M.; Alejandra, O.-M.; Christian, G.-R.; Pedro, C.-R.; Eduardo Perez, S. Oleic acid induces migration through a FFAR1/4, EGFR and AKT-dependent pathway in breast cancer cells. Endocr. Connect. 2019, 8, 252–265. [Google Scholar] [CrossRef] [Green Version]
- Touvier, M.; Fassier, P.; His, M.; Norat, T.; Chan, D.S.M.; Blacher, J.; Hercberg, S.; Galan, P.; Druesne-Pecollo, N.; Latino-Martel, P. Cholesterol and breast cancer risk: A systematic review and meta-analysis of prospective studies. Br. J. Nutr. 2015, 114, 347–357. [Google Scholar] [CrossRef]
- His, M.; Dartois, L.; Fagherazzi, G.; Boutten, A.; Dupré, T.; Mesrine, S.; Boutron-Ruault, M.-C.; Clavel-Chapelon, F.; Dossus, L. Associations between serum lipids and breast cancer incidence and survival in the E3N prospective cohort study. Cancer Causes Control 2017, 28, 77–88. [Google Scholar] [CrossRef]
- Carter, P.R.; Uppal, H.; Chandran, S.; Bainey, K.R.; Potluri, R. Patients with a diagnosis of hyperlipidaemia have a reduced risk of developing breast cancer and lower mortality rates: A large retrospective longitudinal cohort study from the UK ACALM registry. Eur. Heart J. 2017, 38 (Suppl. 1), 644–645. [Google Scholar]
- Zhong, S.; Zhang, X.; Chen, L.; Ma, T.; Tang, J.; Zhao, J. Statin use and mortality in cancer patients: Systematic review and meta-analysis of observational studies. Cancer Treat. Rev. 2015, 41, 554–567. [Google Scholar] [CrossRef] [PubMed]
- Borgquist, S.; Tamimi, R.M.; Chen, W.Y.; Garber, J.E.; Eliassen, A.H.; Ahern, T.P. Statin use and breast cancer risk in the nurses’ health study. Cancer Epidemiol. Prev. Biomark. 2016, 25, 201–206. [Google Scholar] [CrossRef] [PubMed]
- Borgquist, S.; Bjarnadottir, O.; Kimbung, S.; Ahern, T.P. Statins: A role in breast cancer therapy? J. Intern. Med. 2018, 284, 346–357. [Google Scholar] [CrossRef] [PubMed]
- DuSell, C.D.; Nelson, E.R.; Abdo, J.; McDonnell, D.P.; Gesty-Palmer, D.; Wang, X.; Khosla, S.; Mödder, U.I.; Umetani, M.; Javitt, N.B. The Endogenous Selective Estrogen Receptor Modulator 27-Hydroxycholesterol Is a Negative Regulator of Bone Homeostasis. Endocrinology 2010, 151, 3675–3685. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fu, X.; Menke, J.G.; Chen, Y.; Zhou, G.; MacNaul, K.L.; Wright, S.D.; Sparrow, C.P.; Lund, E.G. 27-hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J. Biol. Chem. 2001, 276, 38378–38387. [Google Scholar] [CrossRef] [PubMed]
- Lu, D.-L.; Le Cornet, C.; Sookthai, D.; Johnson, T.S.; Kaaks, R.; Fortner, R.T. Circulating 27-hydroxycholesterol and breast cancer risk: Results from the EPIC-Heidelberg cohort. JNCI J. Natl. Cancer Inst. 2018, 111, 365–371. [Google Scholar] [CrossRef] [PubMed]
- Lazar, I.; Clement, E.; Dauvillier, S.; Milhas, D.; Ducoux-Petit, M.; LeGonidec, S.; Moro, C.; Soldan, V.; Dalle, S.; Balor, S. 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] [PubMed]
- Kasiappan, R.; Rajarajan, D. Role of MicroRNA Regulation in Obesity-Associated Breast Cancer: Nutritional Perspectives. Adv. Nutr. 2017, 8, 868–888. [Google Scholar] [CrossRef] [PubMed]
- Adams, B.D.; Arem, H.; Hubal, M.J.; Cartmel, B.; Li, F.; Harrigan, M.; Sanft, T.; Cheng, C.J.; Pusztai, L.; Irwin, M.L. Exercise and weight loss interventions and miRNA expression in women with breast cancer. Breast Cancer Res. Treat. 2018, 170, 55–67. [Google Scholar] [CrossRef]
- Wu, Q.; Li, J.; Li, Z.; Sun, S.; Zhu, S.; Wang, L.; Wu, J.; Yuan, J.; Zhang, Y.; Sun, S.; 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]
- Huang, H. Matrix Metalloproteinase-9 (MMP-9) as a Cancer Biomarker and MMP-9 Biosensors: Recent Advances. Sensors 2018, 18, 3249. [Google Scholar] [CrossRef] [PubMed]
- Gautam, J.; Banskota, S.; Lee, H.; Lee, Y.-J.; Jeon, Y.H.; Kim, J.-A.; Jeong, B.-S. Down-regulation of cathepsin S and matrix metalloproteinase-9 via Src, a non-receptor tyrosine kinase, suppresses triple-negative breast cancer growth and metastasis. Exp. Mol. Med. 2018, 50, 118. [Google Scholar] [CrossRef] [PubMed]
- Lafleur, M.A.; Drew, A.F.; De Sousa, E.L.; Blick, T.; Bills, M.; Walker, E.C.; Williams, E.D.; Waltham, M.; Thompson, E.W. Upregulation of matrix metalloproteinases (MMPs) in breast cancer xenografts: A major induction of stromal MMP-13. Int. J. Cancer 2005, 114, 544–554. [Google Scholar] [CrossRef]
- Roscilli, G.; Cappelletti, M.; De Vitis, C.; Ciliberto, G.; Di Napoli, A.; Ruco, L.; Mancini, R.; Aurisicchio, L. Circulating MMP11 and specific antibody immune response in breast and prostate cancer patients. J. Transl. Med. 2014, 12, 54. [Google Scholar] [CrossRef] [PubMed]
- Bhardwaj, P.; Au, C.C.; Benito-Martin, A.; Ladumor, H.; Oshchepkova, S.; Moges, R.; Brown, K.A. Estrogens and breast cancer: Mechanisms involved in obesity-related development, growth and progression. J. Steroid Biochem. Mol. Biol. 2019, 189, 161–170. [Google Scholar] [CrossRef] [PubMed]
- Yue, W.; Wang, J.-P.; Li, Y.; Fan, P.; Liu, G.; Zhang, N.; Conaway, M.; Wang, H.; Korach, K.S.; Bocchinfuso, W.; et al. Effects of estrogen on breast cancer development: Role of estrogen receptor independent mechanisms. Int. J. Cancer 2010, 127, 1748–1757. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Russo, J.; Russo, I.H. The role of estrogen in the initiation of breast cancer. The J. Steroid Biochem. Mol. Biol. 2006, 102, 89–96. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lukanova, A.; Lundin, E.; Zeleniuch-Jacquotte, A.; Muti, P.C.; Mure, A.J.; Rinaldi, S.; Dossus, L.; Micheli, A.; Arslan, A.; Lenner, P.; et al. Body mass index, circulating levels of sex-steroid hormones, IGF-I and IGF-binding protein-3: A cross-sectional study in healthy women. Eur. J. Endocrinol. 2004, 150, 161–171. [Google Scholar] [CrossRef]
- McTiernan, A.; Wu, L.; Chen, C.; Chlebowski, R.; Mossavar-Rahmani, Y.; Modugno, F.; Perri, M.G.; Stanczyk, F.Z.; Van Horn, L.; Wang, C.Y.; et al. Relation of BMI and Physical Activity to Sex Hormones in Postmenopausal Women. Obesity 2006, 14, 1662–1677. [Google Scholar] [CrossRef]
- Boyapati, S.M.; Shu, X.O.; Gao, Y.-T.; Dai, Q.; Yu, H.; Cheng, J.R.; Jin, F.; Zheng, W. Correlation of Blood Sex Steroid Hormones with Body Size, Body Fat Distribution, and Other Known Risk Factors for Breast Cancer in Post-Menopausal Chinese Women. Cancer Causes Control 2004, 15, 305–311. [Google Scholar] [CrossRef]
- Purohit, A.; Reed, M.J. Regulation of estrogen synthesis in postmenopausal women. Steroids 2002, 67, 979–983. [Google Scholar] [CrossRef]
- Sebastian, S.; Bulun, S.E. A Highly Complex Organization of the Regulatory Region of the Human CYP19 (Aromatase) Gene Revealed by the Human Genome Project. J. Clin. Endocrinol. Metab. 2001, 86, 4600–4602. [Google Scholar] [CrossRef] [PubMed]
- Van Landeghem, A.A.J.; Poortman, J.; Nabuurs, M.; Thijssen, J.H.H. Endogenous Concentration and Subcellular Distribution of Androgens in Normal and Malignant Human Breast Tissue. Cancer Res. 1985, 45, 2907. [Google Scholar] [PubMed]
- Purohit, A.; Newman, S.P.; Reed, M.J. The role of cytokines in regulating estrogen synthesis: Implications for the etiology of breast cancer. Breast Cancer Res. BCR 2002, 4, 65–69. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Nichols, J.E.; Valdez, R.; Mendelson, C.R.; Simpson, E.R. Tumor necrosis factor-alpha stimulates aromatase gene expression in human adipose stromal cells through use of an activating protein-1 binding site upstream of promoter 1.4. Mol. Endocrinol. 1996, 10, 1350–1357. [Google Scholar] [CrossRef] [PubMed]
- Richards, J.A.; Brueggemeier, R.W. Prostaglandin E2 Regulates Aromatase Activity and Expression in Human Adipose Stromal Cells via Two Distinct Receptor Subtypes. J. Clin. Endocrinol. Metab. 2003, 88, 2810–2816. [Google Scholar] [CrossRef] [PubMed]
- Omoto, Y.; Kobayashi, S.; Inoue, S.; Ogawa, S.; Toyama, T.; Yamashita, H.; Muramatsu, M.; Gustafsson, J.Å.; Iwase, H. Evaluation of oestrogen receptor β wild-type and variant protein expression, and relationship with clinicopathological factors in breast cancers. Eur. J. Cancer 2002, 38, 380–386. [Google Scholar] [CrossRef]
- Rose, D.P.; Komninou, D.; Stephenson, G.D. Obesity, adipocytokines, and insulin resistance in breast cancer. Obes. Rev. 2004, 5, 153–165. [Google Scholar] [CrossRef]
- Kawai, M.; Minami, Y.; Kuriyama, S.; Kakizaki, M.; Kakugawa, Y.; Nishino, Y.; Ishida, T.; Fukao, A.; Tsuji, I.; Ohuchi, N. Adiposity, adult weight change and breast cancer risk in postmenopausal Japanese women: The Miyagi Cohort Study. Br. J. Cancer 2010, 103, 1443–1447. [Google Scholar] [CrossRef]
- Hall, J.M.; Couse, J.F.; Korach, K.S. The Multifaceted Mechanisms of Estradiol and Estrogen Receptor Signaling. J. Biol. Chem. 2001, 276, 36869–36872. [Google Scholar] [CrossRef] [Green Version]
- McKenna, N.J.; Lanz, R.B.; O’Malley, B.W. Nuclear Receptor Coregulators: Cellular and Molecular Biology. Endocr. Rev. 1999, 20, 321–344. [Google Scholar] [CrossRef] [PubMed]
- Wong, C.-W.; McNally, C.; Nickbarg, E.; Komm, B.S.; Cheskis, B.J. Estrogen receptor-interacting protein that modulates its nongenomic activity-crosstalk with Src/Erk phosphorylation cascade. Proc. Natl. Acad. Sci. USA 2002, 99, 14783–14788. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schiff, R.; Massarweh, S.A.; Shou, J.; Bharwani, L.; Mohsin, S.K.; Osborne, C.K. Cross-Talk between Estrogen Receptor and Growth Factor Pathways as a Molecular Target for Overcoming Endocrine Resistance. Clin. Cancer Res. 2004, 10, 331s. [Google Scholar] [CrossRef] [PubMed]
- Migliaccio, A.; Di Domenico, M.; Castoria, G.; de Falco, A.; Bontempo, P.; Nola, E.; Auricchio, F. Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J. 1996, 15, 1292–1300. [Google Scholar] [CrossRef] [PubMed]
- Acconcia, F.; Totta, P.; Ogawa, S.; Cardillo, I.; Inoue, S.; Leone, S.; Trentalance, A.; Muramatsu, M.; Marino, M. Survival versus apoptotic 17β-estradiol effect: Role of ERα and ERβ activated non-genomic signaling. J. Cell. Physiol. 2005, 203, 193–201. [Google Scholar] [CrossRef] [PubMed]
- Marino, M.; Acconcia, F.; Bresciani, F.; Weisz, A.; Trentalance, A. Distinct nongenomic signal transduction pathways controlled by 17beta-estradiol regulate DNA synthesis and cyclin D(1) gene transcription in HepG2 cells. Mol. Biol. Cell 2002, 13, 3720–3729. [Google Scholar] [CrossRef] [PubMed]
- Doisneau-Sixou, S.F.; Sergio, C.M.; Carroll, J.S.; Hui, R.; Musgrove, E.A.; Sutherland, R.L. Estrogen and antiestrogen regulation of cell cycle progression in breast cancer cells. Endocr. Relat. Cancer 2003, 10, 179–186. [Google Scholar] [CrossRef] [PubMed]
- Giretti, M.S.; Fu, X.-D.; De Rosa, G.; Sarotto, I.; Baldacci, C.; Garibaldi, S.; Mannella, P.; Biglia, N.; Sismondi, P.; Genazzani, A.R.; et al. Extra-nuclear signalling of estrogen receptor to breast cancer cytoskeletal remodelling, migration and invasion. PLoS ONE 2008, 3, e2238. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Q.-F.; Wu, T.-T.; Yang, J.-Y.; Dong, C.-R.; Wang, N.; Liu, X.-H.; Liu, Z.-M. 17β-Estradiol promotes the invasion and migration of nuclear estrogen receptor-negative breast cancer cells through cross-talk between GPER1 and CXCR1. J. Steroid Biochem Mol. Biol. 2013, 138, 314–324. [Google Scholar] [CrossRef]
- Kadowaki, T.; Yamauchi, T. Adiponectin and Adiponectin Receptors. Endocr. Rev. 2005, 26, 439–451. [Google Scholar] [CrossRef] [Green Version]
- Mantzoros, C.; Markopoulos, C.; Chavelas, C.; Alexe, D.M.; Dalamaga, M.; Dessypris, N.; Trichopoulos, D.; Petridou, E.; Papadiamantis, Y.; Spanos, E.; et al. Adiponectin and Breast Cancer Risk. J. Clin. Endocrinol. Metab. 2004, 89, 1102–1107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Körner, A.; Pazaitou-Panayiotou, K.; Kelesidis, T.; Kelesidis, I.; Williams, C.J.; Kaprara, A.; Bullen, J.W.; Neuwirth, A.K.; Tseleni, S.; Mitsiades, N.S.; et al. Total and high-molecular-weight adiponectin in breast cancer: In vitro and in vivo studies. J. Clin. Endocrinol. Metab. 2007, 2, 1041–1048. [Google Scholar] [CrossRef] [PubMed]
- Ye, J.; Jia, J.; Dong, S.; Zhang, C.; Yu, S.; Li, L.; Mao, C.; Wang, D.; Chen, J.; Yuan, G. Circulating adiponectin levels and the risk of breast cancer: A meta-analysis. Eur. J. Cancer Prev. 2014, 23, 158–165. [Google Scholar] [CrossRef] [PubMed]
- Berg, A.H.; Combs, T.P.; Du, X.; Brownlee, M.; Scherer, P.E. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat. Med. 2001, 7, 947. [Google Scholar] [CrossRef] [PubMed]
- Kadowaki, T.; Kubota, N.; Hara, K.; Ueki, K.; Tobe, K. Adiponectin and its receptors in insulin resistance, diabetes, and metabolic syndrome, and obesity. J. Clin. Investig. 2006, 116, 1784–1792. [Google Scholar] [CrossRef] [PubMed]
- Dalamaga, M.; Diakopoulos, K.N.; Mantzoros, C.S. The role of adiponectin in cancer: A review of current evidence. Endocr. Rev. 2012, 33, 547–594. [Google Scholar] [CrossRef]
- Kim, A.Y.; Lee, Y.S.; Kim, K.H.; Lee, J.H.; Lee, H.K.; Jang, S.-H.; Kim, S.-E.; Lee, G.Y.; Lee, J.-W.; Jung, S.-A.; et al. Adiponectin Represses Colon Cancer Cell Proliferation via AdipoR1-and-R2-Mediated AMPK Activation. Mol. Endocrinol. 2010, 24, 1441–1452. [Google Scholar] [CrossRef]
- Bråkenhielm, E.; Veitonmäki, N.; Cao, R.; Kihara, S.; Matsuzawa, Y.; Zhivotovsky, B.; Funahashi, T.; Cao, Y. Adiponectin-induced antiangiogenesis and antitumor activity involve caspase-mediated endothelial cell apoptosis. Proc. Natl. Acad. Sci. USA 2004, 101, 2476. [Google Scholar] [CrossRef]
- Abrahamsson, A.; Morad, V.; Dabrosin, C. Estradiol Affects Extracellular Leptin: Adiponectin Ratio in Human Breast Tissue in Vivo. J. Clin. Endocrinol. Metab. 2014, 99, 3460–3467. [Google Scholar] [CrossRef]
- Mauro, L.; Pellegrino, M.; Giordano, F.; Ricchio, E.; Rizza, P.; De Amicis, F.; Catalano, S.; Bonofiglio, D.; Panno, M.L.; Andò, S. Estrogen receptor-α drives adiponectin effects on cyclin D1 expression in breast cancer cells. FASEB J. 2015, 29, 2150–2160. [Google Scholar] [CrossRef]
- Vaisse, C.; Halaas, J.L.; Horvath, C.M.; Darnell, J.E.; Stoffel, M.; Friedman, J.M. Leptin activation of Stat3 in the hypothalamus of wild–type and ob/ob mice but not db/db mice. Nature Genet. 1996, 14, 95–97. [Google Scholar] [CrossRef] [PubMed]
- Guo, S.; Liu, M.; Wang, G.; Torroella-Kouri, M.; Gonzalez-Perez, R.R. Oncogenic role and therapeutic target of leptin signaling in breast cancer and cancer stem cells. Biochim. Biophys. Acta 2012, 1825, 207–222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Delort, L.; Rossary, A.; Farges, M.-C.; Vasson, M.-P.; Caldefie-Chézet, F. Leptin, adipocytes and breast cancer: Focus on inflammation and anti-tumor immunity. Life Sci. 2015, 140, 37–48. [Google Scholar] [CrossRef] [PubMed]
- Ishikawa, M.; Kitayama, J.; Nagawa, H. Enhanced Expression of Leptin and Leptin Receptor (OB-R) in Human Breast Cancer. Clin. Cancer Res. 2004, 10, 4325. [Google Scholar] [CrossRef] [PubMed]
- Catalano, S.; Mauro, L.; Marsico, S.; Giordano, C.; Rizza, P.; Rago, V.; Montanaro, D.; Maggiolini, M.; Panno, M.L.; Andó, S. Leptin induces, via ERK1/ERK2 signal, functional activation of estrogen receptor α in MCF-7 cells. J. Biol. Chem. 2004, 279, 19908–19915. [Google Scholar] [CrossRef] [PubMed]
- Geisler, J.; Haynes, B.; Ekse, D.; Dowsett, M.; Lønning, P.E. Total body aromatization in postmenopausal breast cancer patients is strongly correlated to plasma leptin levels. J. Steroid Biochem. Mol. Biol. 2007, 104, 27–34. [Google Scholar] [CrossRef] [PubMed]
- Fan, Y.; Gan, Y.; Shen, Y.; Cai, X.; Song, Y.; Zhao, F.; Yao, M.; Gu, J.; Tu, H. Leptin signaling enhances cell invasion and promotes the metastasis of human pancreatic cancer via increasing MMP-13 production. Oncotarget 2015, 6, 16120–16134. [Google Scholar] [CrossRef] [Green Version]
- Coughlin, S.S.; Giovannucci, E.L. Diabetes and Cancer. Diabetes 2012, 294–305. [Google Scholar] [CrossRef]
- Ferguson, R.D.; Novosyadlyy, R.; Fierz, Y.; Alikhani, N.; Sun, H.; Yakar, S.; LeRoith, D. Hyperinsulinemia enhances c-Myc-mediated mammary tumor development and advances metastatic progression to the lung in a mouse model of type 2 diabetes. Breast Cancer Res. 2012, 14, R8. [Google Scholar] [CrossRef]
- Ulanet, D.B.; Ludwig, D.L.; Kahn, C.R.; Hanahan, D. Insulin receptor functionally enhances multistage tumor progression and conveys intrinsic resistance to IGF-1R targeted therapy. Proc. Natl. Acad. Sci. USA 2010, 107, 10791–10798. [Google Scholar] [CrossRef] [Green Version]
- Goodwin, P.J.; Ennis, M.; Pritchard, K.I.; Trudeau, M.E.; Koo, J.; Madarnas, Y.; Hartwick, W.; Hoffman, B.; Hood, N. Fasting Insulin and Outcome in Early-Stage Breast Cancer: Results of a Prospective Cohort Study. J. Clin. Oncol. 2002, 20, 42–51. [Google Scholar] [CrossRef] [PubMed]
- Rose, D.P.; Gracheck, P.J.; Vona-Davis, L. The Interactions of Obesity, Inflammation and Insulin Resistance in Breast Cancer. Cancers 2015, 7, 2147–2168. [Google Scholar] [CrossRef] [PubMed]
- Lopez, T.; Hanahan, D. Elevated levels of IGF-1 receptor convey invasive and metastatic capability in a mouse model of pancreatic islet tumorigenesis. Cancer Cell 2002, 1, 339–353. [Google Scholar] [CrossRef] [Green Version]
- Christopoulos, P.F.; Msaouel, P.; Koutsilieris, M. The role of the insulin-like growth factor-1 system in breast cancer. Mol. Cancer 2015, 14, 43. [Google Scholar] [CrossRef] [PubMed]
- Peiró, G.; Adrover, E.; Sánchez-Tejada, L.; Lerma, E.; Planelles, M.; Sánchez-Payá, J.; Aranda, F.I.; Giner, D.; Gutiérrez-Aviñó, F.J. Increased insulin-like growth factor-1 receptor mRNA expression predicts poor survival in immunophenotypes of early breast carcinoma. Mod. Pathol. 2010, 24, 201. [Google Scholar] [CrossRef] [PubMed]
- Assiri, A.M.A.; Kamel, H.F.M.; Hassanien, M.F.R. Resistin, visfatin, adiponectin, and leptin: Risk of breast cancer in pre-and postmenopausal saudi females and their possible diagnostic and predictive implications as novel biomarkers. Dis. Markers 2015, 2015, 253519. [Google Scholar] [CrossRef]
- Wang, C.H.; Wang, P.J.; Hsieh, Y.C.; Lo, S.; Lee, Y.C.; Chen, Y.C.; Tsai, C.H.; Chiu, W.C.; Chu-Sung Hu, S.; Lu, C.W.; et al. Resistin facilitates breast cancer progression via TLR4-mediated induction of mesenchymal phenotypes and stemness properties. Oncogene 2017, 37, 589. [Google Scholar] [CrossRef]
- Carter, J.C.; Church, F.C. Obesity and breast cancer: The roles of peroxisome proliferator-activated receptor-γ and plasminogen activator inhibitor-1. PPAR Res. 2009, 2009, 345320. [Google Scholar] [CrossRef]
- 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]
- Bougaret, L.; Delort, L.; Billard, H.; Le Huede, C.; Boby, C.; De la Foye, A.; Rossary, A.; Mojallal, A.; Damour, O.; Auxenfans, C.; et al. Adipocyte/breast cancer cell crosstalk in obesity interferes with the anti-proliferative efficacy of tamoxifen. PloS ONE 2018, 13, e0191571. [Google Scholar] [CrossRef]
- Carter, J.C.; Church, F.C. Mature breast adipocytes promote breast cancer cell motility. Exp. Mol. Pathol. 2012, 92, 312–317. [Google Scholar] [CrossRef] [PubMed]
- Dalamaga, M.; Sotiropoulos, G.; Karmaniolas, K.; Pelekanos, N.; Papadavid, E.; Lekka, A. Serum resistin: A biomarker of breast cancer in postmenopausal women? Association with clinicopathological characteristics, tumor markers, inflammatory and metabolic parameters. Clin. Biochem. 2013, 46, 584–590. [Google Scholar] [CrossRef] [PubMed]
- Georgiou, G.P.; Provatopoulou, X.; Kalogera, E.; Siasos, G.; Menenakos, E.; Zografos, G.C.; Gounaris, A. Serum resistin is inversely related to breast cancer risk in premenopausal women. Breast 2016, 29, 163–169. [Google Scholar] [CrossRef] [PubMed]
- Coppack, S.W. Pro-inflammatory cytokines and adipose tissue. Proc. Nutr. Soc. 2007, 60, 349–356. [Google Scholar] [CrossRef]
- Picon-Ruiz, M.; Pan, C.; Drews-Elger, K.; Jang, K.; Besser, A.H.; Zhao, D.; Morata-Tarifa, C.; Kim, M.; Ince, T.A.; Azzam, D.J.; et al. Interactions between Adipocytes and Breast Cancer Cells Stimulate Cytokine Production and Drive Src/Sox2/miR-302b–Mediated Malignant Progression. Cancer Res. 2016, 76, 491. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Yang, X. Association between serum cytokines and progression of breast cancer in Chinese population. Medicine 2017, 96, e8840. [Google Scholar] [CrossRef] [PubMed]
- Waugh, D.J.J.; Wilson, C. The interleukin-8 pathway in cancer. Clin. Cancer Res. 2008, 14, 6735–6741. [Google Scholar] [CrossRef] [PubMed]
- Soria, G.; Ben-Baruch, A. The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett. 2008, 267, 271–285. [Google Scholar] [CrossRef]
- Nicolini, A.; Carpi, A.; Rossi, G. Cytokines in breast cancer. Cytokine Growth Factor Rev. 2006, 17, 325–337. [Google Scholar] [CrossRef]
- Fasoulakis, Z.; Kolios, G.; Papamanolis, V.; Kontomanolis, E.N. Interleukins Associated with Breast Cancer. Cureus 2018, 10, e3549. [Google Scholar] [CrossRef] [Green Version]
- Ma, Y.; Ren, Y.; Dai, Z.-J.; Wu, C.-J.; Ji, Y.-H.; Xu, J. IL-6, IL-8 and TNF-α levels correlate with disease stage in breast cancer patients. Adv. Clin. Exp. Med. 2017, 26, 421–426. [Google Scholar] [CrossRef] [PubMed]
- Sheen-Chen, S.-M.; Chen, W.-J.; Eng, H.-L.; Chou, F.-F. Serum concentration of tumor necrosis factor in patients with breast cancer. Breast Cancer Res. Treat. 1997, 43, 211–215. [Google Scholar] [CrossRef] [PubMed]
- Cai, X.; Cao, C.; Li, J.; Chen, F.; Zhang, S.; Liu, B.; Zhang, W.; Zhang, X.; Ye, L. Inflammatory factor TNF-α promotes the growth of breast cancer via the positive feedback loop of TNFR1/NF-κB (and/or p38)/p-STAT3/HBXIP/TNFR1. Oncotarget 2017, 8, 58338–58352. [Google Scholar] [CrossRef] [PubMed]
- Aggarwal, B.B. Signalling pathways of the TNF superfamily: A double-edged sword. Nat. Rev. Immunol. 2003, 3, 745. [Google Scholar] [CrossRef] [PubMed]
- Rivas, M.A.; Carnevale, R.P.; Proietti, C.J.; Rosemblit, C.; Beguelin, W.; Salatino, M.; Charreau, E.H.; Frahm, I.; Sapia, S.; Brouckaert, P. TNFα acting on TNFR1 promotes breast cancer growth via p42/P44 MAPK, JNK, Akt and NF-κB-dependent pathways. Exp. Cell Res. 2008, 314, 509–529. [Google Scholar] [CrossRef] [PubMed]
- Rubio, M.F.; Werbajh, S.; Cafferata, E.G.A.; Quaglino, A.; Coló, G.P.; Nojek, I.M.; Kordon, E.C.; Nahmod, V.E.; Costas, M.A. TNF-α enhances estrogen-induced cell proliferation of estrogen-dependent breast tumor cells through a complex containing nuclear factor-kappa B. Oncogene 2005, 25, 1367. [Google Scholar] [CrossRef]
- Kim, S.; Choi, J.H.; Kim, J.B.; Nam, S.J.; Yang, J.-H.; Kim, J.-H.; Lee, J.E. Berberine suppresses TNF-alpha-induced MMP-9 and cell invasion through inhibition of AP-1 activity in MDA-MB-231 human breast cancer cells. Molecules 2008, 13, 2975–2985. [Google Scholar] [CrossRef]
- Varela, L.M.; Stangle-Castor, N.C.; Shoemaker, S.F.; Shea-Eaton, W.K.; Ip, M.M. TNFα induces NFκB/p50 in association with the growth and morphogenesis of normal and transformed rat mammary epithelial cells. J. Cell. Physiol. 2001, 188, 120–131. [Google Scholar] [CrossRef]
- Kamel, M.; Shouman, S.; El-Merzebany, M.; Kilic, G.; Veenstra, T.; Saeed, M.; Wagih, M.; Diaz-Arrastia, C.; Patel, D.; Salama, S. Effect of tumour necrosis factor-alpha on estrogen metabolic pathways in breast cancer cells. J. Cancer 2012, 3, 310. [Google Scholar] [CrossRef]
- Valdivia-Silva, J.E.; Franco-Barraza, J.; Silva, A.L.E.; Pont, G.D.; Soldevila, G.; Meza, I.; García-Zepeda, E.A. Effect of pro-inflammatory cytokine stimulation on human breast cancer: Implications of chemokine receptor expression in cancer metastasis. Cancer Lett. 2009, 283, 176–185. [Google Scholar] [CrossRef]
- Warren, M.A.; Shoemaker, S.F.; Shealy, D.J.; Bshara, W.; Ip, M.M. Tumor necrosis factor deficiency inhibits mammary tumorigenesis and a tumor necrosis factor neutralizing antibody decreases mammary tumor growth in neu/erbB2 transgenic mice. Mol. Cancer Ther. 2009, 8, 2655. [Google Scholar] [CrossRef] [PubMed]
- Macci, A.; Madeddu, C. Obesity, Inflammation, and Postmenopausal Breast Cancer: Therapeutic Implications. Sci. World J. 2011, 11, 17. [Google Scholar] [CrossRef] [PubMed]
- Grisouard, J.; Dembinski, K.; Mayer, D.; Keller, U.; Müller, B.; Christ-Crain, M. Targeting AMP-activated protein kinase in adipocytes to modulate obesity-related adipokine production associated with insulin resistance and breast cancer cell proliferation. Diabetol. Metab. Syndr. 2011, 3, 16. [Google Scholar] [CrossRef] [PubMed]
- Kim, K.-Y.; Kim, J.K.; Jeon, J.H.; Yoon, S.R.; Choi, I.; Yang, Y. c-Jun N-terminal kinase is involved in the suppression of adiponectin expression by TNF-α in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 2005, 327, 460–467. [Google Scholar] [CrossRef] [PubMed]
- Dinarello, C.A. The IL-1 family and inflammatory diseases. Clin. Exp. Rheumatol 2002, 20, S1–S13. [Google Scholar] [PubMed]
- Howe, L.R. Inflammation and breast cancer. Cyclooxygenase/prostaglandin signaling and breast cancer. Breast Cancer Res. BCR 2007, 9, 210. [Google Scholar] [CrossRef]
- Wang, F.-M.; Liu, H.-Q.; Liu, S.-R.; Tang, S.-P.; Yang, L.; Feng, G.-S. SHP-2 promoting migration and metastasis of MCF-7 with loss of E-cadherin, dephosphorylation of FAK and secretion of MMP-9 induced by IL-1 βin vivo andin vitro. Breast Cancer Res. Treat. 2005, 89, 5–14. [Google Scholar] [CrossRef]
- Liao, D.; Johnson, R.S. Hypoxia: A key regulator of angiogenesis in cancer. Cancer Metastasis Rev. 2007, 26, 281–290. [Google Scholar] [CrossRef]
- Grivennikov, S.; Karin, E.; Terzic, J.; Mucida, D.; Yu, G.-Y.; Vallabhapurapu, S.; Scheller, J.; Rose-John, S.; Cheroutre, H.; Eckmann, L.; et al. IL-6 and Stat3 Are Required for Survival of Intestinal Epithelial Cells and Development of Colitis-Associated Cancer. Cancer Cell 2009, 15, 241. [Google Scholar] [CrossRef] [Green Version]
- Ranger, J.J.; Levy, D.E.; Shahalizadeh, S.; Hallett, M.; Muller, W.J. Identification of a Stat3-dependent transcription regulatory network involved in metastatic progression. Cancer Res. 2009, 69, 6823–6830. [Google Scholar] [CrossRef]
- Zhang, G.J.; Adachi, I. Serum interleukin-6 levels correlate to tumor progression and prognosis in metastatic breast carcinoma. Anticancer Res. 1999, 19, 1427–1432. [Google Scholar]
- Sullivan, N.J.; Sasser, A.K.; Axel, A.E.; Vesuna, F.; Raman, V.; Ramirez, N.; Oberyszyn, T.M.; Hall, B.M. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 2009, 28, 2940–2947. [Google Scholar] [CrossRef]
- Penson, R.T.; Kronish, K.; Duan, Z.; Feller, A.J.; Stark, P.; Cook, S.E.; Duska, L.R.; Fuller, A.F.; Goodman, A.K.; Nikrui, N.; et al. Cytokines IL-1beta, IL-2, IL-6, IL-8, MCP-1, GM-CSF and TNFalpha in patients with epithelial ovarian cancer and their relationship to treatment with paclitaxel. Int. J. Gynecol. Cancer 2000, 10, 33–41. [Google Scholar] [CrossRef]
- Ali, S.; Lazennec, G. Chemokines: Novel targets for breast cancer metastasis. Cancer Metastasis Rev. 2007, 26, 401–420. [Google Scholar] [CrossRef]
- Luboshits, G.; Shina, S.; Kaplan, O.; Engelberg, S.; Nass, D.; Lifshitz-Mercer, B.; Chaitchik, S.; Keydar, I.; Ben-Baruch, A. Elevated Expression of the CC Chemokine Regulated on Activation, Normal T Cell Expressed and Secreted (RANTES) in Advanced Breast Carcinoma. Cancer Res. 1999, 59, 4681. [Google Scholar]
- Chen, J.; Yao, Y.; Gong, C.; Yu, F.; Su, S.; Chen, J.; Liu, B.; Deng, H.; Wang, F.; Lin, L.; et al. CCL18 from tumor-associated macrophages promotes breast cancer metastasis via PITPNM3. Cancer Cell 2011, 19, 541–555. [Google Scholar] [CrossRef]
- Biswas, S.K.; Mantovani, A. Macrophage plasticity and interaction with lymphocyte subsets: Cancer as a paradigm. Nat. Immunol. 2010, 11, 889. [Google Scholar] [CrossRef]
- DeNardo, D.G.; Barreto, J.B.; Andreu, P.; Vasquez, L.; Tawfik, D.; Kolhatkar, N.; Coussens, L.M. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009, 16, 91–102. [Google Scholar] [CrossRef]
- Chavey, C.; Bibeau, F.; Gourgou-Bourgade, S.; Burlinchon, S.; Boissière, F.; Laune, D.; Roques, S.; Lazennec, G. Oestrogen receptor negative breast cancers exhibit high cytokine content. Breast Cancer Res. BCR 2007, 9, R15. [Google Scholar] [CrossRef]
- Lebrecht, A.; Grimm, C.; Lantzsch, T.; Ludwig, E.; Hefler, L.; Ulbrich, E.; Koelbl, H. Monocyte chemoattractant protein-1 serum levels in patients with breast cancer. Tumor Biol. 2004, 25, 14–17. [Google Scholar] [CrossRef]
- Goede, V.; Brogelli, L.; Ziche, M.; Augustin, H.G. Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int. J. Cancer 1999, 82, 765–770. [Google Scholar] [CrossRef]
- Jin, W.J.; Kim, B.; Kim, D.; Park Choo, H.-Y.; Kim, H.-H.; Ha, H.; Lee, Z.H. NF-κB signaling regulates cell-autonomous regulation of CXCL10 in breast cancer 4T1 cells. Exp. Mol. Med. 2017, 49, e295. [Google Scholar] [CrossRef]
- Ejaeidi, A.A.; Craft, B.S.; Puneky, L.V.; Lewis, R.E.; Cruse, J.M. Hormone receptor-independent CXCL10 production is associated with the regulation of cellular factors linked to breast cancer progression and metastasis. Exp. Mol. Pathol. 2015, 99, 163–172. [Google Scholar] [CrossRef]
- Kitamura, T.; Pollard, J.W. Therapeutic potential of chemokine signal inhibition for metastatic breast cancer. Pharmacol. Res. 2015, 100, 266–270. [Google Scholar] [CrossRef] [Green Version]
- Mittal, S.; Brown, N.J.; Holen, I. The breast tumor microenvironment: Role in cancer development, progression and response to therapy. Expert Rev. Mol. Diagn. 2018, 18, 227–243. [Google Scholar] [CrossRef]
- Vielma, S.A.; Klein, R.L.; Levingston, C.A.; Young, M.R.I. Adipocytes as immune regulatory cells. Int. Immunopharmacol. 2013, 16, 224–231. [Google Scholar] [CrossRef] [Green Version]
- Korkaya, H.; Liu, S.; Wicha, M.S. Breast cancer stem cells, cytokine networks, and the tumor microenvironment. J. Clin. Investig. 2011, 121, 3804–3809. [Google Scholar] [CrossRef]
- Mao, Y.; Keller, E.T.; Garfield, D.H.; Shen, K.; Wang, J. Stromal cells in tumor microenvironment and breast cancer. Cancer Metastasis Rev. 2013, 32, 303–315. [Google Scholar] [CrossRef]
- Shiga, K.; Hara, M.; Nagasaki, T.; Sato, T.; Takahashi, H.; Takeyama, H. Cancer-associated fibroblasts: Their characteristics and their roles in tumor growth. Cancers 2015, 7, 2443–2458. [Google Scholar] [CrossRef]
- Orimo, A.; Gupta, P.B.; Sgroi, D.C.; Arenzana-Seisdedos, F.; Delaunay, T.; Naeem, R.; Carey, V.J.; Richardson, A.L.; Weinberg, R.A. Stromal Fibroblasts Present in Invasive Human Breast Carcinomas Promote Tumor Growth and Angiogenesis through Elevated SDF-1/CXCL12 Secretion. Cell 2005, 121, 335–348. [Google Scholar] [CrossRef]
- Chu, Q.D.; Panu, L.; Holm, N.T.; Li, B.D.L.; Johnson, L.W.; Zhang, S. High Chemokine Receptor CXCR4 Level in Triple Negative Breast Cancer Specimens Predicts Poor Clinical Outcome. J. Surg. Res. 2010, 159, 689–695. [Google Scholar] [CrossRef]
- Burger, J.A.; Kipps, T.J. CXCR4: A key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006, 107, 1761. [Google Scholar] [CrossRef]
- Okumura, T.; Ohuchida, K.; Kibe, S.; Iwamoto, C.; Ando, Y.; Takesue, S.; Nakayama, H.; Abe, T.; Endo, S.; Koikawa, K.; et al. Adipose tissue-derived stromal cells are sources of cancer-associated fibroblasts and enhance tumor progression by dense collagen matrix. Int. J. Cancer 2019, 144, 1401–1413. [Google Scholar] [CrossRef]
- Lopes-Coelho, F.; Gouveia-Fernandes, S.; Serpa, J. Metabolic cooperation between cancer and non-cancerous stromal cells is pivotal in cancer progression. Tumor Biol. 2018, 40, 1010428318756203. [Google Scholar] [CrossRef]
- Bussard, K.M.; Mutkus, L.; Stumpf, K.; Gomez-Manzano, C.; Marini, F.C. Tumor-associated stromal cells as key contributors to the tumor microenvironment. Breast Cancer Res. BCR 2016, 18, 84. [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]
- Singh, R.; Parveen, M.; Basgen, J.M.; Fazel, S.; Meshesha, M.F.; Thames, E.C.; Moore, B.; Martinez, L.; Howard, C.B.; Vergnes, L. Increased expression of beige/brown adipose markers from host and breast cancer cells influence xenograft formation in mice. Mol. Cancer Res. 2016, 14, 78–92. [Google Scholar] [CrossRef]
- Cao, Q.; Hersl, J.; La, H.; Smith, M.; Jenkins, J.; Goloubeva, O.; Dilsizian, V.; Tkaczuk, K.; Chen, W.; Jones, L. A pilot study of FDG PET/CT detects a link between brown adipose tissue and breast cancer. BMC Cancer 2014, 14, 126. [Google Scholar] [CrossRef]
- Ahirwar, D.K.; Nasser, M.W.; Ouseph, M.M.; Elbaz, M.; Cuitiño, M.C.; Kladney, R.D.; Varikuti, S.; Kaul, K.; Satoskar, A.R.; Ramaswamy, B.; et al. Fibroblast-derived CXCL12 promotes breast cancer metastasis by facilitating tumor cell intravasation. Oncogene 2018, 37, 4428–4442. [Google Scholar] [CrossRef]
- Lee, Y.; Jung, W.H.; Koo, J.S. Adipocytes can induce epithelial-mesenchymal transition in breast cancer cells. Breast Cancer Res. Treat. 2015, 153, 323–335. [Google Scholar] [CrossRef]
- 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. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat. Med. 2011, 17, 1498. [Google Scholar] [CrossRef]
Metabolic Substrates | Released by White/Brite/Brown Adipocytes | Effect on BC Development | Effect on BC Cell Proliferation | Effect on BC Cell Invasion | References | |
---|---|---|---|---|---|---|
Free fatty acids | Saturated; (n-6) fatty acids | White | Increase | Increase | Increase | [46,47,53,57,58,59] |
(n-3) fatty acids | White | Decrease | Decrease | Decrease | [43,45,49] | |
Lipids, Triglycerides | White | Increase | Increase | Increase | [61] | |
Cholesterol | Total | White | Increase | Increase | Increase | [60,62,63] |
HDL | White | Decrease | Decrease | Decrease | [44] | |
LDL | White | Increase | Increase | [44] | ||
VLDL | White | Increase | Increase | Increase | [44] | |
27-OHC | White | Decrease | Decrease | [41,53] | ||
Exosome | mir- 3184-5p | White | - | Increase | Increase | [50] |
mir- 184c-3p | White | - | Decrease | Decrease | [50] | |
Proteases (MMP-9, MMP-11) | White | Increase | Increase | Increase | [74,75,76] |
Hormone | Released by White/Brite/Brown Adipocytes | Effect on BC Development | Effect on BC Cell Proliferation | Effect on BC Cell Invasion | Reference |
---|---|---|---|---|---|
Estrogen | White | Increase | Increase | Increase | [97,98,99,100,101] |
Adiponectin | White | Decrease | Decrease | Decrease | [108,109,110,111,112,128] |
Leptin | White | Increase | Increase | Increase | [111,112,113,114,118,119,128,132] |
Insulin | White | Increase | Increase | Increase | [40,120,121,125,126] |
Visfatin | White | Increase | Increase | Increase | [128] |
PAI-1 | White | Increase | Increase | Increase | [130,133] |
Resistin | White | Increase | Increase | Increase | [128,129,134] |
White | Decrease | Decrease | Decrease | [135] |
Hormone | Released by White/Bright/Brown Adipocytes | Effect on BC Development | Effect on BC Cell Proliferation | Effect on BC Cell Invasion | Reference | |
---|---|---|---|---|---|---|
TNFα | Visceral, subcutaneous white | Increase | Increase | Increase | [132,143,144,145,147,148,149,150] | |
Interleukins | IL-1b | White | Increase | Increase | Increase | [142,157,158,159] |
IL-6 | White | Increase | Increase | Increase | [132,138,141,142,143,161] | |
IL-8 | Visceral, subcutaneous white | Increase | Increase | Increase | [138,139,141,142,143] | |
IL10 | White | [138] | ||||
Chemokines | CCL2 | White | Increase | Increase | Increase | [140,142] |
CCL5 | White | Increase | Increase | Increase | [140,142] | |
CXCL18 | White | [169,170] | ||||
CXCL12 | White | Increase | Increase | Increase | [191,192] | |
CXCL10/IP-10 | White | Increase | Increase | Increase | [174,175] |
© 2019 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
Chu, D.-T.; Nguyen Thi Phuong, T.; Tien, N.L.B.; Tran, D.-K.; Nguyen, T.-T.; Thanh, V.V.; Luu Quang, T.; Minh, L.B.; Pham, V.H.; Ngoc, V.T.N.; et al. The Effects of Adipocytes on the Regulation of Breast Cancer in the Tumor Microenvironment: An Update. Cells 2019, 8, 857. https://doi.org/10.3390/cells8080857
Chu D-T, Nguyen Thi Phuong T, Tien NLB, Tran D-K, Nguyen T-T, Thanh VV, Luu Quang T, Minh LB, Pham VH, Ngoc VTN, et al. The Effects of Adipocytes on the Regulation of Breast Cancer in the Tumor Microenvironment: An Update. Cells. 2019; 8(8):857. https://doi.org/10.3390/cells8080857
Chicago/Turabian StyleChu, Dinh-Toi, Thuy Nguyen Thi Phuong, Nguyen Le Bao Tien, Dang-Khoa Tran, Tran-Thuy Nguyen, Vo Van Thanh, Thuy Luu Quang, Le Bui Minh, Van Huy Pham, Vo Truong Nhu Ngoc, and et al. 2019. "The Effects of Adipocytes on the Regulation of Breast Cancer in the Tumor Microenvironment: An Update" Cells 8, no. 8: 857. https://doi.org/10.3390/cells8080857