Instruction of Immunometabolism by Adipose Tissue: Implications for Cancer Progression
Abstract
:Simple Summary
Abstract
1. Introduction
2. Adipose Tissue in Cancer
2.1. Obesity and Cancer Risk
2.2. The Role of Visceral Adipose Tissue in Cancer
3. Adaptive Immune Cell Metabolism and Adipose Tissue
3.1. CD4 T Helper Cells
3.2. Regulatory T (Treg) Cells
3.3. CD8 T Cells
3.4. B Cells
4. Innate Immune Cell Metabolism and Adipose Tissue
4.1. Macrophages
4.2. Eosinophils
4.3. Neutrophils
4.4. Innate Lymphoid Cells (ILCs)
4.5. NK and iNKT Cells
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Rosen, E.D.; Spiegelman, B.M. Adipocytes as regulators of energy balance and glucose homeostasis. Nature 2006, 444, 847–853. [Google Scholar] [CrossRef] [Green Version]
- Haslam, D.W.; James, W.P. Obesity. Lancet 2005, 366, 1197–1209. [Google Scholar] [CrossRef]
- DiSpirito, J.R.; Mathis, D. Immunological contributions to adipose tissue homeostasis. Semin. Immunol. 2015, 27, 315–321. [Google Scholar] [CrossRef] [Green Version]
- Booth, A.; Magnuson, A.; Fouts, J.; Foster, M. Adipose tissue, obesity and adipokines: Role in cancer promotion. Horm. Mol. Biol. Clin. Investig. 2015, 21, 57–74. [Google Scholar] [CrossRef] [PubMed]
- Friedman, J. 20 years of leptin: Leptin at 20: An overview. J. Endocrinol. 2014, 223, T1–T8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Margetic, S.; Gazzola, C.; Pegg, G.G.; Hill, R.A. Leptin: A review of its peripheral actions and interactions. Int. J. Obes. 2002, 26, 1407–1433. [Google Scholar] [CrossRef] [Green Version]
- Lord, G.M.; Matarese, G.; Howard, J.K.; Baker, R.J.; Bloom, S.R.; Lechler, R.I. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 1998, 394, 897–901. [Google Scholar] [CrossRef]
- Duncan, B.B.; Schmidt, M.I.; Pankow, J.S.; Bang, H.; Couper, D.; Ballantyne, C.M.; Hoogeveen, R.C.; Heiss, G. Adiponectin and the Development of Type 2 Diabetes. Atheroscler. Risk Communities Study 2004, 53, 2473–2478. [Google Scholar] [CrossRef] [Green Version]
- Hotta, K.; Funahashi, T.; Bodkin, N.L.; Ortmeyer, H.K.; Arita, Y.; Hansen, B.C.; Matsuzawa, Y. Circulating Concentrations of the Adipocyte Protein Adiponectin Are Decreased in Parallel With Reduced Insulin Sensitivity During the Progression to Type 2 Diabetes in Rhesus Monkeys. Diabetes 2001, 50, 1126–1133. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scherer, P.E.; Williams, S.; Fogliano, M.; Baldini, G.; Lodish, H.F. A Novel Serum Protein Similar to C1q, Produced Exclusively in Adipocytes (*). J. Biol. Chem. 1995, 270, 26746–26749. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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] [Green Version]
- Global BMI Mortality Collaboration; Di Angelantonio, E.; Bhupathiraju, S.; Wormser, D.; Gao, P.; Kaptoge, S.; Berrington de Gonzalez, A.; Cairns, B.J.; Huxley, R.; Jackson, C.; et al. Body-mass index and all-cause mortality: Individual-participant-data meta-analysis of 239 prospective studies in four continents. Lancet 2016, 388, 776–786. [Google Scholar] [CrossRef] [Green Version]
- Ligibel, J.A.; Alfano, C.M.; Courneya, K.S.; Demark-Wahnefried, W.; Burger, R.A.; Chlebowski, R.T.; Fabian, C.J.; Gucalp, A.; Hershman, D.L.; Hudson, M.M.; et al. American Society of Clinical Oncology position statement on obesity and cancer. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2014, 32, 3568–3574. [Google Scholar] [CrossRef] [PubMed]
- Renehan, A.G.; Tyson, M.; Egger, M.; Heller, R.F.; Zwahlen, M. Body-mass index and incidence of cancer: A systematic review and meta-analysis of prospective observational studies. Lancet 2008, 371, 569–578. [Google Scholar] [CrossRef]
- Choi, E.K.; Park, H.B.; Lee, K.H.; Park, J.H.; Eisenhut, M.; van der Vliet, H.J.; Kim, G.; Shin, J.I. Body mass index and 20 specific cancers: Re-analyses of dose-response meta-analyses of observational studies. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2018, 29, 749–757. [Google Scholar] [CrossRef] [Green Version]
- Friedman, J.M. Obesity: Causes and control of excess body fat. Nature 2009, 459, 340–342. [Google Scholar] [CrossRef]
- Meza-Perez, S.; Randall, T.D. Immunological Functions of the Omentum. Trends Immunol. 2017, 38, 526–536. [Google Scholar] [CrossRef]
- Worzfeld, T.; Pogge von Strandmann, E.; Huber, M.; Adhikary, T.; Wagner, U.; Reinartz, S.; Muller, R. The Unique Molecular and Cellular Microenvironment of Ovarian Cancer. Front. Oncol. 2017, 7, 24. [Google Scholar] [CrossRef] [Green Version]
- Litbarg, N.O.; Gudehithlu, K.P.; Sethupathi, P.; Arruda, J.A.; Dunea, G.; Singh, A.K. Activated omentum becomes rich in factors that promote healing and tissue regeneration. Cell Tissue Res. 2007, 328, 487–497. [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.; 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]
- Ladanyi, A.; Mukherjee, A.; Kenny, H.A.; Johnson, A.; Mitra, A.K.; Sundaresan, S.; Nieman, K.M.; Pascual, G.; Benitah, S.A.; Montag, A.; et al. Adipocyte-induced CD36 expression drives ovarian cancer progression and metastasis. Oncogene 2018, 37, 2285–2301. [Google Scholar] [CrossRef]
- Maguire, O.A.; Ackerman, S.E.; Szwed, S.K.; Maganti, A.V.; Marchildon, F.; Huang, X.; Kramer, D.J.; Rosas-Villegas, A.; Gelfer, R.G.; Turner, L.E.; et al. Creatine-mediated crosstalk between adipocytes and cancer cells regulates obesity-driven breast cancer. Cell Metab. 2021, 33, 499–512.e496. [Google Scholar] [CrossRef]
- Hotamisligil, G.; Shargill, N.; Spiegelman, B. Adipose expression of tumor necrosis factor-alpha: Direct role in obesity-linked insulin resistance. Science 1993, 259, 87–91. [Google Scholar] [CrossRef] [PubMed]
- Tay, R.E.; Richardson, E.K.; Toh, H.C. Revisiting the role of CD4+ T cells in cancer immunotherapy—new insights into old paradigms. Cancer Gene Ther. 2021, 28, 5–17. [Google Scholar] [CrossRef] [PubMed]
- Kratz, M.; Coats, B.R.; Hisert, K.B.; Hagman, D.; Mutskov, V.; Peris, E.; Schoenfelt, K.Q.; Kuzma, J.N.; Larson, I.; Billing, P.S.; et al. Metabolic Dysfunction Drives a Mechanistically Distinct Proinflammatory Phenotype in Adipose Tissue Macrophages. Cell Metab. 2014, 20, 614–625. [Google Scholar] [CrossRef] [Green Version]
- McLaughlin, T.; Ackerman, S.E.; Shen, L.; Engleman, E. Role of innate and adaptive immunity in obesity-associated metabolic disease. J. Clin. Investig. 2017, 127, 5–13. [Google Scholar] [CrossRef] [Green Version]
- Kintscher, U.; Hartge, M.; Hess, K.; Foryst-Ludwig, A.; Clemenz, M.; Wabitsch, M.; Fischer-Posovszky, P.; Barth, T.F.; Dragun, D.; Skurk, T.; et al. T-lymphocyte infiltration in visceral adipose tissue: A primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 1304–1310. [Google Scholar] [CrossRef] [Green Version]
- Khan, I.M.; Dai Perrard, X.Y.; Perrard, J.L.; Mansoori, A.; Smith, C.W.; Wu, H.; Ballantyne, C.M. Attenuated adipose tissue and skeletal muscle inflammation in obese mice with combined CD4+ and CD8+ T cell deficiency. Atherosclerosis 2014, 233, 419–428. [Google Scholar] [CrossRef] [Green Version]
- Lumeng, C.N.; Saltiel, A.R. Inflammatory links between obesity and metabolic disease. J. Clin. Investig. 2011, 121, 2111–2117. [Google Scholar] [CrossRef] [Green Version]
- Gordon, S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3, 23–35. [Google Scholar] [CrossRef] [PubMed]
- Winer, S.; Chan, Y.; Paltser, G.; Truong, D.; Tsui, H.; Bahrami, J.; Dorfman, R.; Wang, Y.; Zielenski, J.; Mastronardi, F.; et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat. Med. 2009, 15, 921–929. [Google Scholar] [CrossRef]
- McLaughlin, T.; Liu, L.F.; Lamendola, C.; Shen, L.; Morton, J.; Rivas, H.; Winer, D.; Tolentino, L.; Choi, O.; Zhang, H.; et al. T-cell profile in adipose tissue is associated with insulin resistance and systemic inflammation in humans. Arterioscler. Thromb. Vasc. Biol. 2014, 34, 2637–2643. [Google Scholar] [CrossRef] [Green Version]
- Weaver, C.T.; Hatton, R.D.; Mangan, P.R.; Harrington, L.E. IL-17 Family Cytokines and the Expanding Diversity of Effector T Cell Lineages. Annu. Rev. Immunol. 2007, 25, 821–852. [Google Scholar] [CrossRef] [Green Version]
- Sumarac-Dumanovic, M.; Stevanovic, D.; Ljubic, A.; Jorga, J.; Simic, M.; Stamenkovic-Pejkovic, D.; Starcevic, V.; Trajkovic, V.; Micic, D. Increased activity of interleukin-23/interleukin-17 proinflammatory axis in obese women. Int. J. Obes. 2009, 33, 151–156. [Google Scholar] [CrossRef] [Green Version]
- Fabbrini, E.; Cella, M.; McCartney, S.A.; Fuchs, A.; Abumrad, N.A.; Pietka, T.A.; Chen, Z.; Finck, B.N.; Han, D.H.; Magkos, F.; et al. Association Between Specific Adipose Tissue CD4+ T-Cell Populations and Insulin Resistance in Obese Individuals. Gastroenterology 2013, 145, 366–374.e363. [Google Scholar] [CrossRef] [Green Version]
- Zúñiga, L.A.; Shen, W.-J.; Joyce-Shaikh, B.; Pyatnova, E.A.; Richards, A.G.; Thom, C.; Andrade, S.M.; Cua, D.J.; Kraemer, F.B.; Butcher, E.C. IL-17 Regulates Adipogenesis, Glucose Homeostasis, and Obesity. J. Immunol. 2010, 185, 6947–6959. [Google Scholar] [CrossRef] [Green Version]
- Kohlgruber, A.C.; Gal-Oz, S.T.; LaMarche, N.M.; Shimazaki, M.; Duquette, D.; Koay, H.F.; Nguyen, H.N.; Mina, A.I.; Paras, T.; Tavakkoli, A.; et al. gammadelta T cells producing interleukin-17A regulate adipose regulatory T cell homeostasis and thermogenesis. Nat. Immunol. 2018, 19, 464–474. [Google Scholar] [CrossRef] [PubMed]
- Harley, I.T.W.; Stankiewicz, T.E.; Giles, D.A.; Softic, S.; Flick, L.M.; Cappelletti, M.; Sheridan, R.; Xanthakos, S.A.; Steinbrecher, K.A.; Sartor, R.B.; et al. IL-17 signaling accelerates the progression of nonalcoholic fatty liver disease in mice. Hepatology 2014, 59, 1830–1839. [Google Scholar] [CrossRef] [PubMed]
- Mehta, P.; Nuotio-Antar, A.M.; Smith, C.W. γδ T cells promote inflammation and insulin resistance during high fat diet-induced obesity in mice. J. Leukoc. Biol. 2015, 97, 121–134. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gentles, A.J.; Newman, A.M.; Liu, C.L.; Bratman, S.V.; Feng, W.; Kim, D.; Nair, V.S.; Xu, Y.; Khuong, A.; Hoang, C.D.; et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat. Med. 2015, 21, 938–945. [Google Scholar] [CrossRef] [PubMed]
- Zou, W.; Restifo, N.P. T(H)17 cells in tumour immunity and immunotherapy. Nat. Rev. Immunol. 2010, 10, 248–256. [Google Scholar] [CrossRef] [PubMed]
- Kryczek, I.; Banerjee, M.; Cheng, P.; Vatan, L.; Szeliga, W.; Wei, S.; Huang, E.; Finlayson, E.; Simeone, D.; Welling, T.H.; et al. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 2009, 114, 1141–1149. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Coffelt, S.B.; Kersten, K.; Doornebal, C.W.; Weiden, J.; Vrijland, K.; Hau, C.-S.; Verstegen, N.J.M.; Ciampricotti, M.; Hawinkels, L.J.A.C.; Jonkers, J.; et al. IL-17-producing γδ T cells and neutrophils conspire to promote breast cancer metastasis. Nature 2015, 522, 345–348. [Google Scholar] [CrossRef]
- Curiel, T.J. Tregs and rethinking cancer immunotherapy. J. Clin. Investig. 2007, 117, 1167–1174. [Google Scholar] [CrossRef]
- Feuerer, M.; Herrero, L.; Cipolletta, D.; Naaz, A.; Wong, J.; Nayer, A.; Lee, J.; Goldfine, A.B.; Benoist, C.; Shoelson, S.; et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 2009, 15, 930–939. [Google Scholar] [CrossRef]
- Cipolletta, D.; Feuerer, M.; Li, A.; Kamei, N.; Lee, J.; Shoelson, S.E.; Benoist, C.; Mathis, D. PPAR-gamma is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 2012, 486, 549–553. [Google Scholar] [CrossRef]
- Ahmadian, M.; Suh, J.M.; Hah, N.; Liddle, C.; Atkins, A.R.; Downes, M.; Evans, R.M. PPARgamma signaling and metabolism: The good, the bad and the future. Nat. Med. 2013, 19, 557–566. [Google Scholar] [CrossRef] [Green Version]
- Woo, E.Y.; Chu, C.S.; Goletz, T.J.; Schlienger, K.; Yeh, H.; Coukos, G.; Rubin, S.C.; Kaiser, L.R.; June, C.H. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res. 2001, 61, 4766–4772. [Google Scholar]
- Liyanage, U.K.; Moore, T.T.; Joo, H.G.; Tanaka, Y.; Herrmann, V.; Doherty, G.; Drebin, J.A.; Strasberg, S.M.; Eberlein, T.J.; Goedegebuure, P.S.; et al. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J. Immunol. 2002, 169, 2756–2761. [Google Scholar] [CrossRef]
- Shen, Z.; Zhou, S.; Wang, Y.; Li, R.L.; Zhong, C.; Liang, C.; Sun, Y. Higher intratumoral infiltrated Foxp3+ Treg numbers and Foxp3+/CD8+ ratio are associated with adverse prognosis in resectable gastric cancer. J. Cancer Res. Clin. Oncol. 2010, 136, 1585–1595. [Google Scholar] [CrossRef]
- Gao, Q.; Qiu, S.J.; Fan, J.; Zhou, J.; Wang, X.Y.; Xiao, Y.S.; Xu, Y.; Li, Y.W.; Tang, Z.Y. Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2007, 25, 2586–2593. [Google Scholar] [CrossRef] [Green Version]
- Curiel, T.J.; Coukos, G.; Zou, L.; Alvarez, X.; Cheng, P.; Mottram, P.; Evdemon-Hogan, M.; Conejo-Garcia, J.R.; Zhang, L.; Burow, M.; et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 2004, 10, 942–949. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Franco, F.; Tsui, Y.-C.; Xie, X.; Trefny, M.P.; Zappasodi, R.; Mohmood, S.R.; Fernández-García, J.; Tsai, C.-H.; Schulze, I.; et al. CD36-mediated metabolic adaptation supports regulatory T cell survival and function in tumors. Nat. Immunol. 2020, 21, 298–308. [Google Scholar] [CrossRef]
- Zhang, L.; Conejo-Garcia, J.R.; Katsaros, D.; Gimotty, P.A.; Massobrio, M.; Regnani, G.; Makrigiannakis, A.; Gray, H.; Schlienger, K.; Liebman, M.N.; et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 2003, 348, 203–213. [Google Scholar] [CrossRef] [Green Version]
- Galon, J.; Costes, A.; Sanchez-Cabo, F.; Kirilovsky, A.; Mlecnik, B.; Lagorce-Pages, C.; Tosolini, M.; Camus, M.; Berger, A.; Wind, P.; et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006, 313, 1960–1964. [Google Scholar] [CrossRef] [Green Version]
- McGranahan, N.; Furness, A.J.; Rosenthal, R.; Ramskov, S.; Lyngaa, R.; Saini, S.K.; Jamal-Hanjani, M.; Wilson, G.A.; Birkbak, N.J.; Hiley, C.T.; et al. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science 2016, 351, 1463–1469. [Google Scholar] [CrossRef] [Green Version]
- Huang, A.C.; Postow, M.A.; Orlowski, R.J.; Mick, R.; Bengsch, B.; Manne, S.; Xu, W.; Harmon, S.; Giles, J.R.; Wenz, B.; et al. T-cell invigoration to tumour burden ratio associated with anti-PD-1 response. Nature 2017, 545, 60–65. [Google Scholar] [CrossRef] [Green Version]
- Rausch, M.E.; Weisberg, S.; Vardhana, P.; Tortoriello, D.V. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int. J. Obes. 2008, 32, 451–463. [Google Scholar] [CrossRef] [Green Version]
- Strissel, K.J.; DeFuria, J.; Shaul, M.E.; Bennett, G.; Greenberg, A.S.; Obin, M.S. T-Cell Recruitment and Th1 Polarization in Adipose Tissue During Diet-Induced Obesity in C57BL/6 Mice. Obesity 2010, 18, 1918–1925. [Google Scholar] [CrossRef]
- McGillicuddy, F.C.; Chiquoine, E.H.; Hinkle, C.C.; Kim, R.J.; Shah, R.; Roche, H.M.; Smyth, E.M.; Reilly, M.P. Interferon γ Attenuates Insulin Signaling, Lipid Storage, and Differentiation in Human Adipocytes via Activation of the JAK/STAT Pathway. J. Biol. Chem. 2009, 284, 31936–31944. [Google Scholar] [CrossRef] [Green Version]
- Nishimura, S.; Manabe, I.; Nagasaki, M.; Eto, K.; Yamashita, H.; Ohsugi, M.; Otsu, M.; Hara, K.; Ueki, K.; Sugiura, S.; et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 2009, 15, 914–920. [Google Scholar] [CrossRef]
- Yang, H.; Youm, Y.H.; Vandanmagsar, B.; Ravussin, A.; Gimble, J.M.; Greenway, F.; Stephens, J.M.; Mynatt, R.L.; Dixit, V.D. Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: Implications for systemic inflammation and insulin resistance. J. Immunol. 2010, 185, 1836–1845. [Google Scholar] [CrossRef] [Green Version]
- Klebanoff, C.A.; Gattinoni, L.; Palmer, D.C.; Muranski, P.; Ji, Y.; Hinrichs, C.S.; Borman, Z.A.; Kerkar, S.P.; Scott, C.D.; Finkelstein, S.E.; et al. Determinants of Successful CD8+ T-Cell Adoptive Immunotherapy for Large Established Tumors in Mice. Clin. Cancer Res. 2011, 17, 5343–5352. [Google Scholar] [CrossRef] [Green Version]
- Krishna, S.; Lowery, F.J.; Copeland, A.R.; Bahadiroglu, E.; Mukherjee, R.; Jia, L.; Anibal, J.T.; Sachs, A.; Adebola, S.O.; Gurusamy, D.; et al. Stem-like CD8 T cells mediate response of adoptive cell immunotherapy against human cancer. Science 2020, 370, 1328–1334. [Google Scholar] [CrossRef] [PubMed]
- Van der Windt, G.J.; Everts, B.; Chang, C.H.; Curtis, J.D.; Freitas, T.C.; Amiel, E.; Pearce, E.J.; Pearce, E.L. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity 2012, 36, 68–78. [Google Scholar] [CrossRef] [Green Version]
- Pearce, E.L.; Poffenberger, M.C.; Chang, C.-H.; Jones, R.G. Fueling Immunity: Insights into Metabolism and Lymphocyte Function. Science 2013, 342, 1242454. [Google Scholar] [CrossRef] [Green Version]
- Leone, R.D.; Powell, J.D. Metabolism of immune cells in cancer. Nat. Rev. Cancer 2020, 20, 516–531. [Google Scholar] [CrossRef]
- Pan, Y.; Tian, T.; Park, C.O.; Lofftus, S.Y.; Mei, S.; Liu, X.; Luo, C.; O’Malley, J.T.; Gehad, A.; Teague, J.E.; et al. Survival of tissue-resident memory T cells requires exogenous lipid uptake and metabolism. Nature 2017, 543, 252–256. [Google Scholar] [CrossRef] [Green Version]
- Han, S.-J.; Glatman Zaretsky, A.; Andrade-Oliveira, V.; Collins, N.; Dzutsev, A.; Shaik, J.; Morais da Fonseca, D.; Harrison, O.J.; Tamoutounour, S.; Byrd, A.L.; et al. White Adipose Tissue Is a Reservoir for Memory T Cells and Promotes Protective Memory Responses to Infection. Immunity 2017, 47, 1154–1168.e1156. [Google Scholar] [CrossRef] [Green Version]
- Bengsch, B.; Johnson, A.L.; Kurachi, M.; Odorizzi, P.M.; Pauken, K.E.; Attanasio, J.; Stelekati, E.; McLane, L.M.; Paley, M.A.; Delgoffe, G.M.; et al. Bioenergetic Insufficiencies Due to Metabolic Alterations Regulated by the Inhibitory Receptor PD-1 Are an Early Driver of CD8+ T Cell Exhaustion. Immunity 2016, 45, 358–373. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wherry, E.J.; Ha, S.J.; Kaech, S.M.; Haining, W.N.; Sarkar, S.; Kalia, V.; Subramaniam, S.; Blattman, J.N.; Barber, D.L.; Ahmed, R. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 2007, 27, 670–684. [Google Scholar] [CrossRef] [Green Version]
- Wherry, E.J. T cell exhaustion. Nat. Immunol. 2011, 12, 492. [Google Scholar] [CrossRef]
- Delgoffe, G.M.; Powell, J.D. Feeding an army: The metabolism of T cells in activation, anergy, and exhaustion. Mol. Immunol. 2015, 68, 492–496. [Google Scholar] [CrossRef] [Green Version]
- Barber, D.L.; Wherry, E.J.; Masopust, D.; Zhu, B.; Allison, J.P.; Sharpe, A.H.; Freeman, G.J.; Ahmed, R. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006, 439, 682–687. [Google Scholar] [CrossRef]
- Chang, C.-H.; Qiu, J.; O’Sullivan, D.; Buck, M.D.; Noguchi, T.; Curtis, J.D.; Chen, Q.; Gindin, M.; Gubin, M.M.; van der Windt Gerritje, J.W.; et al. Metabolic Competition in the Tumor Microenvironment Is a Driver of Cancer Progression. Cell 2015, 162, 1229–1241. [Google Scholar] [CrossRef] [Green Version]
- Scharping, N.E.; Rivadeneira, D.B.; Menk, A.V.; Vignali, P.D.A.; Ford, B.R.; Rittenhouse, N.L.; Peralta, R.; Wang, Y.; Wang, Y.; DePeaux, K.; et al. Mitochondrial stress induced by continuous stimulation under hypoxia rapidly drives T cell exhaustion. Nat. Immunol. 2021, 22, 205–215. [Google Scholar] [CrossRef]
- Ma, X.; Xiao, L.; Liu, L.; Ye, L.; Su, P.; Bi, E.; Wang, Q.; Yang, M.; Qian, J.; Yi, Q. CD36-mediated ferroptosis dampens intratumoral CD8+ T cell effector function and impairs their antitumor ability. Cell Metab. 2021. [Google Scholar] [CrossRef]
- Xu, S.; Chaudhary, O.; Rodríguez-Morales, P.; Sun, X.; Chen, D.; Zappasodi, R.; Xu, Z.; Pinto, A.F.M.; Williams, A.; Schulze, I.; et al. Uptake of oxidized lipids by the scavenger receptor CD36 promotes lipid peroxidation and dysfunction in CD8+ T cells in tumors. Immunity 2021. [Google Scholar] [CrossRef]
- Ma, X.; Bi, E.; Lu, Y.; Su, P.; Huang, C.; Liu, L.; Wang, Q.; Yang, M.; Kalady, M.F.; Qian, J.; et al. Cholesterol Induces CD8(+) T Cell Exhaustion in the Tumor Microenvironment. Cell Metab. 2019, 30, 143–156.e145. [Google Scholar] [CrossRef]
- Zhang, Y.; Kurupati, R.; Liu, L.; Zhou, X.Y.; Zhang, G.; Hudaihed, A.; Filisio, F.; Giles-Davis, W.; Xu, X.; Karakousis, G.C.; et al. Enhancing CD8+ T Cell Fatty Acid Catabolism within a Metabolically Challenging Tumor Microenvironment Increases the Efficacy of Melanoma Immunotherapy. Cancer Cell 2017, 32, 377–391.e379. [Google Scholar] [CrossRef] [Green Version]
- Winer, D.A.; Winer, S.; Chng, M.H.; Shen, L.; Engleman, E.G. B Lymphocytes in obesity-related adipose tissue inflammation and insulin resistance. Cell. Mol. Life Sci. 2014, 71, 1033–1043. [Google Scholar] [CrossRef] [Green Version]
- Winer, D.A.; Winer, S.; Shen, L.; Wadia, P.P.; Yantha, J.; Paltser, G.; Tsui, H.; Wu, P.; Davidson, M.G.; Alonso, M.N.; et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 2011, 17, 610–617. [Google Scholar] [CrossRef] [PubMed]
- DeFuria, J.; Belkina, A.C.; Jagannathan-Bogdan, M.; Snyder-Cappione, J.; Carr, J.D.; Nersesova, Y.R.; Markham, D.; Strissel, K.J.; Watkins, A.A.; Zhu, M.; et al. B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proc. Natl. Acad. Sci. USA 2013, 110, 5133–5138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nishimura, S.; Manabe, I.; Takaki, S.; Nagasaki, M.; Otsu, M.; Yamashita, H.; Sugita, J.; Yoshimura, K.; Eto, K.; Komuro, I.; et al. Adipose Natural Regulatory B Cells Negatively Control Adipose Tissue Inflammation. Cell Metab. 2013, 18, 759–766. [Google Scholar] [CrossRef] [Green Version]
- Wynn, T.A.; Chawla, A.; Pollard, J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496, 445–455. [Google Scholar] [CrossRef] [PubMed]
- Lumeng, C.N.; Bodzin, J.L.; Saltiel, A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Investig. 2007, 117, 175–184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weisberg, S.P.; McCann, D.; Desai, M.; Rosenbaum, M.; Leibel, R.L.; Ferrante, A.W., Jr. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Investig. 2003, 112, 1796–1808. [Google Scholar] [CrossRef]
- Wu, D.; Molofsky, A.B.; Liang, H.E.; Ricardo-Gonzalez, R.R.; Jouihan, H.A.; Bando, J.K.; Chawla, A.; Locksley, R.M. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011, 332, 243–247. [Google Scholar] [CrossRef] [Green Version]
- Kang, K.; Reilly, S.M.; Karabacak, V.; Gangl, M.R.; Fitzgerald, K.; Hatano, B.; Lee, C.-H. Adipocyte-Derived Th2 Cytokines and Myeloid PPARδ Regulate Macrophage Polarization and Insulin Sensitivity. Cell Metab. 2008, 7, 485–495. [Google Scholar] [CrossRef] [Green Version]
- Vats, D.; Mukundan, L.; Odegaard, J.I.; Zhang, L.; Smith, K.L.; Morel, C.R.; Wagner, R.A.; Greaves, D.R.; Murray, P.J.; Chawla, A. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 2006, 4, 13–24. [Google Scholar] [CrossRef] [Green Version]
- Odegaard, J.I.; Ricardo-Gonzalez, R.R.; Goforth, M.H.; Morel, C.R.; Subramanian, V.; Mukundan, L.; Eagle, A.R.; Vats, D.; Brombacher, F.; Ferrante, A.W.; et al. Macrophage-specific PPARγ controls alternative activation and improves insulin resistance. Nature 2007, 447, 1116–1120. [Google Scholar] [CrossRef] [Green Version]
- Rodríguez-Prados, J.-C.; Través, P.G.; Cuenca, J.; Rico, D.; Aragonés, J.; Martín-Sanz, P.; Cascante, M.; Boscá, L. Substrate Fate in Activated Macrophages: A Comparison between Innate, Classic, and Alternative Activation. J. Immunol. 2010, 185, 605–614. [Google Scholar] [CrossRef] [Green Version]
- Jha Abhishek, K.; Huang Stanley, C.-C.; Sergushichev, A.; Lampropoulou, V.; Ivanova, Y.; Loginicheva, E.; Chmielewski, K.; Stewart Kelly, M.; Ashall, J.; Everts, B.; et al. Network Integration of Parallel Metabolic and Transcriptional Data Reveals Metabolic Modules that Regulate Macrophage Polarization. Immunity 2015, 42, 419–430. [Google Scholar] [CrossRef] [Green Version]
- Huang, S.C.-C.; Everts, B.; Ivanova, Y.; O'Sullivan, D.; Nascimento, M.; Smith, A.M.; Beatty, W.; Love-Gregory, L.; Lam, W.Y.; O'Neill, C.M.; et al. Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages. Nat. Immunol. 2014, 15, 846–855. [Google Scholar] [CrossRef] [Green Version]
- Xu, X.; Grijalva, A.; Skowronski, A.; van Eijk, M.; Serlie, M.J.; Ferrante, A.W., Jr. Obesity activates a program of lysosomal-dependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metab. 2013, 18, 816–830. [Google Scholar] [CrossRef] [Green Version]
- Qian, B.-Z.; Pollard, J.W. Macrophage Diversity Enhances Tumor Progression and Metastasis. Cell 2010, 141, 39–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ruffell, B.; Coussens Lisa, M. Macrophages and Therapeutic Resistance in Cancer. Cancer Cell 2015, 27, 462–472. [Google Scholar] [CrossRef] [Green Version]
- Lin, E.Y.; Li, J.F.; Gnatovskiy, L.; Deng, Y.; Zhu, L.; Grzesik, D.A.; Qian, H.; Xue, X.N.; Pollard, J.W. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 2006, 66, 11238–11246. [Google Scholar] [CrossRef] [Green Version]
- Yuan, X.; Zhang, J.; Li, D.; Mao, Y.; Mo, F.; Du, W.; Ma, X. Prognostic significance of tumor-associated macrophages in ovarian cancer: A meta-analysis. Gynecol. Oncol. 2017, 147, 181–187. [Google Scholar] [CrossRef] [PubMed]
- Tiwari, P.; Blank, A.; Cui, C.; Schoenfelt, K.Q.; Zhou, G.; Xu, Y.; Khramtsova, G.; Olopade, F.; Shah, A.M.; Khan, S.A.; et al. Metabolically activated adipose tissue macrophages link obesity to triple-negative breast cancer. J. Exp. Med. 2019, 216, 1345–1358. [Google Scholar] [CrossRef] [PubMed]
- Klion, A.D.; Ackerman, S.J.; Bochner, B.S. Contributions of Eosinophils to Human Health and Disease. Annu. Rev. Pathol. Mech. Dis. 2020, 15, 179–209. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grisaru-Tal, S.; Itan, M.; Klion, A.D.; Munitz, A. A new dawn for eosinophils in the tumour microenvironment. Nat. Rev. Cancer 2020, 20, 594–607. [Google Scholar] [CrossRef] [PubMed]
- Davis, B.P.; Rothenberg, M.E. Eosinophils and Cancer. Cancer Immunol. Res. 2014, 2, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Carretero, R.; Sektioglu, I.M.; Garbi, N.; Salgado, O.C.; Beckhove, P.; Hammerling, G.J. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nat. Immunol. 2015, 16, 609–617. [Google Scholar] [CrossRef]
- Tepper, R.I.; Coffman, R.L.; Leder, P. An eosinophil-dependent mechanism for the antitumor effect of interleukin-4. Science 1992, 257, 548–551. [Google Scholar] [CrossRef]
- Lucarini, V.; Ziccheddu, G.; Macchia, I.; La Sorsa, V.; Peschiaroli, F.; Buccione, C.; Sistigu, A.; Sanchez, M.; Andreone, S.; D’Urso, M.T.; et al. IL-33 restricts tumor growth and inhibits pulmonary metastasis in melanoma-bearing mice through eosinophils. Oncoimmunology 2017, 6, e1317420. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kratochvill, F.; Neale, G.; Haverkamp, J.M.; Van de Velde, L.-A.; Smith, A.M.; Kawauchi, D.; McEvoy, J.; Roussel, M.F.; Dyer, M.A.; Qualls, J.E.; et al. TNF Counterbalances the Emergence of M2 Tumor Macrophages. Cell Rep. 2015, 12, 1902–1914. [Google Scholar] [CrossRef] [Green Version]
- Astigiano, S.; Morandi, B.; Costa, R.; Mastracci, L.; D’Agostino, A.; Ratto, G.B.; Melioli, G.; Frumento, G. Eosinophil Granulocytes Account for Indoleamine 2,3-Dioxygenase-Mediated Immune Escape in Human Non Small Cell Lung Cancer. Neoplasia 2005, 7, 390–396. [Google Scholar] [CrossRef] [Green Version]
- Injarabian, L.; Devin, A.; Ransac, S.; Marteyn, B.S. Neutrophil Metabolic Shift during their Lifecycle: Impact on their Survival and Activation. Int. J. Mol. Sci. 2019, 21, 287. [Google Scholar] [CrossRef] [Green Version]
- Kolaczkowska, E.; Kubes, P. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 2013, 13, 159–175. [Google Scholar] [CrossRef]
- Ferrante, A.W., Jr. The immune cells in adipose tissue. Diabetes Obes. Metab. 2013, 15, 34–38. [Google Scholar] [CrossRef] [Green Version]
- Shah, T.J.; Leik, C.E.; Walsh, S.W. Neutrophil infiltration and systemic vascular inflammation in obese women. Reprod. Sci. 2010, 17, 116–124. [Google Scholar] [CrossRef] [Green Version]
- Manfredi, A.A.; Ramirez, G.A.; Rovere-Querini, P.; Maugeri, N. The Neutrophil’s Choice: Phagocytose vs Make Neutrophil Extracellular Traps. Front. Immunol. 2018, 9, 288. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jeon, J.H.; Hong, C.W.; Kim, E.Y.; Lee, J.M. Current Understanding on the Metabolism of Neutrophils. Immune Netw. 2020, 20, e46. [Google Scholar] [CrossRef]
- Papayannopoulos, V. Neutrophil extracellular traps in immunity and disease. Nat. Rev. Immunol. 2018, 18, 134–147. [Google Scholar] [CrossRef] [PubMed]
- Lee, W.; Ko, S.Y.; Mohamed, M.S.; Kenny, H.A.; Lengyel, E.; Naora, H. Neutrophils facilitate ovarian cancer premetastatic niche formation in the omentum. J. Exp. Med. 2018, 216, 176–194. [Google Scholar] [CrossRef] [PubMed]
- Veglia, F.; Tyurin, V.A.; Blasi, M.; De Leo, A.; Kossenkov, A.V.; Donthireddy, L.; To, T.K.J.; Schug, Z.; Basu, S.; Wang, F.; et al. Fatty acid transport protein 2 reprograms neutrophils in cancer. Nature 2019, 569, 73–78. [Google Scholar] [CrossRef]
- Boland, J.L.; Zhou, Q.; Martin, M.; Callahan, M.K.; Konner, J.; O’Cearbhaill, R.E.; Friedman, C.F.; Tew, W.; Makker, V.; Grisham, R.N.; et al. Early disease progression and treatment discontinuation in patients with advanced ovarian cancer receiving immune checkpoint blockade. Gynecol. Oncol. 2018, 152, 251–258. [Google Scholar] [CrossRef] [Green Version]
- Granot, Z. Neutrophils as a Therapeutic Target in Cancer. Front. Immunol. 2019, 10, 1710. [Google Scholar] [CrossRef] [Green Version]
- Vivier, E.; Artis, D.; Colonna, M.; Diefenbach, A.; Di Santo, J.P.; Eberl, G.; Koyasu, S.; Locksley, R.M.; McKenzie, A.N.J.; Mebius, R.E.; et al. Innate Lymphoid Cells: 10 Years On. Cell 2018, 174, 1054–1066. [Google Scholar] [CrossRef] [Green Version]
- Boulenouar, S.; Michelet, X.; Duquette, D.; Alvarez, D.; Hogan, A.E.; Dold, C.; O’Connor, D.; Stutte, S.; Tavakkoli, A.; Winters, D.; et al. Adipose Type One Innate Lymphoid Cells Regulate Macrophage Homeostasis through Targeted Cytotoxicity. Immunity 2017, 46, 273–286. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- O’Sullivan, T.E.; Rapp, M.; Fan, X.; Weizman, O.-E.; Bhardwaj, P.; Adams, N.M.; Walzer, T.; Dannenberg, A.J.; Sun, J.C. Adipose-resident group 1 innate lymphoid cells promote obesity-associated insulin resistance. Immunity 2016, 45, 428–441. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Molofsky, A.B.; Van Gool, F.; Liang, H.E.; Van Dyken, S.J.; Nussbaum, J.C.; Lee, J.; Bluestone, J.A.; Locksley, R.M. Interleukin-33 and Interferon-gamma Counter-Regulate Group 2 Innate Lymphoid Cell Activation during Immune Perturbation. Immunity 2015, 43, 161–174. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brestoff, J.R.; Kim, B.S.; Saenz, S.A.; Stine, R.R.; Monticelli, L.A.; Sonnenberg, G.F.; Thome, J.J.; Farber, D.L.; Lutfy, K.; Seale, P.; et al. Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature 2015, 519, 242–246. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Ota, N.; Manzanillo, P.; Kates, L.; Zavala-Solorio, J.; Eidenschenk, C.; Zhang, J.; Lesch, J.; Lee, W.P.; Ross, J.; et al. Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes. Nature 2014, 514, 237–241. [Google Scholar] [CrossRef]
- Hasnain, S.Z.; Borg, D.J.; Harcourt, B.E.; Tong, H.; Sheng, Y.H.; Ng, C.P.; Das, I.; Wang, R.; Chen, A.C.H.; Loudovaris, T.; et al. Glycemic control in diabetes is restored by therapeutic manipulation of cytokines that regulate beta cell stress. Nat. Med. 2014, 20, 1417–1426. [Google Scholar] [CrossRef]
- Kirchberger, S.; Royston, D.J.; Boulard, O.; Thornton, E.; Franchini, F.; Szabady, R.L.; Harrison, O.; Powrie, F. Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 2013, 210, 917–931. [Google Scholar] [CrossRef]
- Kim, J.; Kim, W.; Moon, U.J.; Kim, H.J.; Choi, H.J.; Sin, J.I.; Park, N.H.; Cho, H.R.; Kwon, B. Intratumorally Establishing Type 2 Innate Lymphoid Cells Blocks Tumor Growth. J. Immunol. 2016, 196, 2410–2423. [Google Scholar] [CrossRef] [Green Version]
- Wensveen, F.M.; Jelenčić, V.; Valentić, S.; Šestan, M.; Wensveen, T.T.; Theurich, S.; Glasner, A.; Mendrila, D.; Štimac, D.; Wunderlich, F.T.; et al. NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat. Immunol. 2015, 16, 376–385. [Google Scholar] [CrossRef]
- Morvan, M.G.; Lanier, L.L. NK cells and cancer: You can teach innate cells new tricks. Nat. Rev. Cancer 2016, 16, 7. [Google Scholar] [CrossRef]
- Vivier, E.; Ugolini, S.; Blaise, D.; Chabannon, C.; Brossay, L. Targeting natural killer cells and natural killer T cells in cancer. Nat. Rev. Immunol. 2012, 12, 239–252. [Google Scholar] [CrossRef]
- Imai, K.; Matsuyama, S.; Miyake, S.; Suga, K.; Nakachi, K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: An 11-year follow-up study of a general population. Lancet 2000, 356, 1795–1799. [Google Scholar] [CrossRef]
- Guerra, N.; Tan, Y.X.; Joncker, N.T.; Choy, A.; Gallardo, F.; Xiong, N.; Knoblaugh, S.; Cado, D.; Greenberg, N.R.; Raulet, D.H. NKG2D-Deficient Mice Are Defective in Tumor Surveillance in Models of Spontaneous Malignancy. Immunity 2008, 28, 571–580. [Google Scholar] [CrossRef] [Green Version]
- Assmann, N.; O’Brien, K.L.; Donnelly, R.P.; Dyck, L.; Zaiatz-Bittencourt, V.; Loftus, R.M.; Heinrich, P.; Oefner, P.J.; Lynch, L.; Gardiner, C.M. Srebp-controlled glucose metabolism is essential for NK cell functional responses. Nat. Immunol. 2017, 18, 1197. [Google Scholar] [CrossRef]
- Donnelly, R.P.; Loftus, R.M.; Keating, S.E.; Liou, K.T.; Biron, C.A.; Gardiner, C.M.; Finlay, D.K. mTORC1-Dependent Metabolic Reprogramming Is a Prerequisite for NK Cell Effector Function. J. Immunol. 2014, 193, 4477–4484. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Michelet, X.; Dyck, L.; Hogan, A.; Loftus, R.M.; Duquette, D.; Wei, K.; Beyaz, S.; Tavakkoli, A.; Foley, C.; Donnelly, R.; et al. Metabolic reprogramming of natural killer cells in obesity limits antitumor responses. Nat. Immunol. 2018, 19, 1330–1340. [Google Scholar] [CrossRef] [PubMed]
- Lynch, L.; Nowak, M.; Varghese, B.; Clark, J.; Hogan, A.E.; Toxavidis, V.; Balk, S.P.; O’Shea, D.; O’Farrelly, C.; Exley, M.A. Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production. Immunity 2012, 37, 574–587. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lynch, L.; O’Shea, D.; Winter, D.C.; Geoghegan, J.; Doherty, D.G.; O’Farrelly, C. Invariant NKT cells and CD1d(+) cells amass in human omentum and are depleted in patients with cancer and obesity. Eur. J. Immunol. 2009, 39, 1893–1901. [Google Scholar] [CrossRef]
- Huh, J.Y.; Park, Y.J.; Kim, J.B. Adipocyte CD1d determines adipose inflammation and insulin resistance in obesity. Adipocyte 2018, 7, 129–136. [Google Scholar] [CrossRef] [Green Version]
- Huh, J.Y.; Park, J.; Kim, J.I.; Park, Y.J.; Lee, Y.K.; Kim, J.B. Deletion of CD1d in Adipocytes Aggravates Adipose Tissue Inflammation and Insulin Resistance in Obesity. Diabetes 2017, 66, 835–847. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cui, J.; Shin, T.; Kawano, T.; Sato, H.; Kondo, E.; Toura, I.; Kaneko, Y.; Koseki, H.; Kanno, M.; Taniguchi, M. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 1997, 278, 1623–1626. [Google Scholar] [CrossRef] [PubMed]
- Smyth, M.J.; Thia, K.Y.; Street, S.E.; Cretney, E.; Trapani, J.A.; Taniguchi, M.; Kawano, T.; Pelikan, S.B.; Crowe, N.Y.; Godfrey, D.I. Differential tumor surveillance by natural killer (NK) and NKT cells. J. Exp. Med. 2000, 191, 661–668. [Google Scholar] [CrossRef] [Green Version]
- Terabe, M.; Matsui, S.; Noben-Trauth, N.; Chen, H.; Watson, C.; Donaldson, D.D.; Carbone, D.P.; Paul, W.E.; Berzofsky, J.A. NKT cell–mediated repression of tumor immunosurveillance by IL-13 and the IL-4R–STAT6 pathway. Nat. Immunol. 2000, 1, 515–520. [Google Scholar] [CrossRef] [PubMed]
- Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Raja, R.; Wu, C.; Limbeck, F.; Butler, K.; Acharya, A.P.; Curtis, M. Instruction of Immunometabolism by Adipose Tissue: Implications for Cancer Progression. Cancers 2021, 13, 3327. https://doi.org/10.3390/cancers13133327
Raja R, Wu C, Limbeck F, Butler K, Acharya AP, Curtis M. Instruction of Immunometabolism by Adipose Tissue: Implications for Cancer Progression. Cancers. 2021; 13(13):3327. https://doi.org/10.3390/cancers13133327
Chicago/Turabian StyleRaja, Remya, Christopher Wu, Francesca Limbeck, Kristina Butler, Abhinav P. Acharya, and Marion Curtis. 2021. "Instruction of Immunometabolism by Adipose Tissue: Implications for Cancer Progression" Cancers 13, no. 13: 3327. https://doi.org/10.3390/cancers13133327