Interactions between adipose tissue and the immune system in health and malnutrition

Seminars in Immunology

Volumn 27, Issue 5, 2015, Pages 322-333

  Wensveen, Felix M ^a,b   Valentić, Sonja ^a   Šestan, Marko ^a   Turk Wensveen, Tamara ^c   Polić, Bojan ^a  

^a UNIVERSITY OF RIJEKA   (Croatia)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c KBC RIJEKA   (Croatia)

Author keywords

Adipocytes; Immune system; Inflammation; Malnutrition; Obesity; Starvation

Indexed keywords

ADIPOCYTOKINE;

ADIPOCYTE; ADIPOSE TISSUE; CELL ACTIVATION; DIET INDUCED OBESITY; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNITY; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INTRAABDOMINAL FAT; MALNUTRITION; NUTRIENT; OBESITY; REVIEW; STARVATION; TISSUE METABOLISM; ANIMAL; CYTOLOGY; DIET; ENERGY METABOLISM; FOOD; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; SIGNAL TRANSDUCTION;

ADIPOKINES; ADIPOSE TISSUE; ANIMALS; DIET; ENERGY METABOLISM; FOOD; HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; IMMUNITY; IMMUNOMODULATION; MALNUTRITION; OBESITY; SIGNAL TRANSDUCTION; STARVATION;

EID: 84952877023     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2015.10.006     Document Type: Review

References (208)

1. Murray J.M., Kaufmann G.R., Hodgkin P.D., Lewin S.R., Kelleher A.D., Davenport M.P., et al. Naive T cells are maintained by thymic output in early ages but by proliferation without phenotypic change after age twenty. Immunol. Cell Biol. 2003, 81:487-495.
2. Gubser P.M., Bantug G.R., Razik L., Fischer M., Dimeloe S., Hoenger G., et al. Rapid effector function of memory CD8(+) T cells requires an immediate-early glycolytic switch. Nature. Immunol. 2013, 14:1064-+.
3. van der Windt G.J., Everts B., Chang C.H., Curtis J.D., Freitas T.C., Amiel E., et al. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity 2012, 36:68-78.
4. Wing E.J., Magee D.M., Barczynski L.K. Acute starvation in mice reduces the number of T cells and suppresses the development of T-cell-mediated immunity. Immunology 1988, 63:677-682.
5. Ronti T., Lupattelli G., Mannarino E. The endocrine function of adipose tissue: an update. Clin. Endocrinol. (Oxf.) 2006, 64:355-365.
6. Ouchi N., Parker J.L., Lugus J.J., Walsh K. Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 2011, 11:85-97.
7. Leibel R.L. Molecular physiology of weight regulation in mice and humans. Int. J. Obes. (Lond) 2008, 32(Suppl. 7):S98-S108.
8. 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.
9. Popkin B.M. Global changes in diet and activity patterns as drivers of the nutrition transition. Nestle Nutr. Workshop Ser. Pediatr. Program. 2009, 63:1-10. (discussion 10-14, 259-268).
10. Stevens G.A., Singh G.M., Lu Y., Danaei G., Lin J.K., Finucane M.M., et al. National, regional, and global trends in adult overweight and obesity prevalences. Popul. Health Metr. 2012, 10:22.
11. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444:860-867.
12. Kern P.A., Saghizadeh M., Ong J.M., Bosch R.J., Deem R., Simsolo R.B. The expression of tumor necrosis factor in human adipose tissue. Regulation by obesity, weight loss, and relationship to lipoprotein lipase. J. Clin. Invest. 1995, 95:2111-2119.
13. Visser M., Bouter L.M., McQuillan G.M., Wener M.H., Harris T.B. Elevated C-reactive protein levels in overweight and obese adults. JAMA 1999, 282:2131-2135.
14. Vozarova B., Weyer C., Hanson K., Tataranni P.A., Bogardus C., Pratley R.E. Circulating interleukin-6 in relation to adiposity, insulin action, and insulin secretion. Obes. Res. 2001, 9:414-417.
15. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112:1796-1808.
16. Xu H., Barnes G.T., Yang Q., Tan G., Yang D., Chou C.J., et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 2003, 112:1821-1830.
17. Johnson A.R., Milner J.J., Makowski L. The inflammation highway: metabolism accelerates inflammatory traffic in obesity. Immunol. Rev. 2012, 249:218-238.
18. Sanchez-Gurmaches J., Guertin D.A. Adipocyte lineages: tracing back the origins of fat. Biochim. Biophys. Acta 2014, 1842:340-351.
19. Banerji M.A., Faridi N., Atluri R., Chaiken R.L., Lebovitz H.E. Body composition, visceral fat, leptin, and insulin resistance in Asian Indian men. J. Clin. Endocrinol. Metab. 1999, 84:137-144.
20. Hung C.M., Calejman C.M., Sanchez-Gurmaches J., Li H., Clish C.B., Hettmer S., et al. Rictor/mTORC2 loss in the Myf5 lineage reprograms brown fat metabolism and protects mice against obesity and metabolic disease. Cell Rep. 2014, 8:256-271.
21. Sluik D., Boeing H., Montonen J., Pischon T., Kaaks R., Teucher B., et al. Associations between general and abdominal adiposity and mortality in individuals with diabetes mellitus. Am. J. Epidemiol. 2011, 174:22-34.
22. Guilherme A., Virbasius J.V., Puri V., Czech M.P. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell Biol. 2008, 9:367-377.
23. Betz M.J., Enerback S. Human Brown adipose tissue: what we have learned so far. Diabetes 2015, 64:2352-2360.
24. Nedergaard J., Bengtsson T., Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E444-E452.
25. Sethi J.K., Vidal-Puig A.J. Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. J. Lipid Res. 2007, 48:1253-1262.
26. Sanchez-Gurmaches J., Guertin D.A. Adipocytes arise from multiple lineages that are heterogeneously and dynamically distributed. Nat. Commun. 2014, 5:4099.
27. Garvey W.T., Garber A.J., Mechanick J.I., Bray G.A., Dagogo-Jack S., Einhorn D., et al. American association of clinical endocrinologists and american college of endocrinology position statement on the 2014 advanced framework for a new diagnosis of obesity as a chronic disease. Endocrinol. Pract. 2014, 20:977-989.
28. West D.B., Boozer C.N., Moody D.L., Atkinson R.L. Dietary obesity in nine inbred mouse strains. Am. J. Physiol. 1992, 262:R1025-R1032.
29. Wang Q.A., Tao C., Gupta R.K., Scherer P.E. Tracking adipogenesis during white adipose tissue development, expansion and regeneration. Nat. Med. 2013, 19:1338-1344.
30. Jeffery E., Church C.D., Holtrup B., Colman L., Rodeheffer M.S. Rapid depot-specific activation of adipocyte precursor cells at the onset of obesity. Nat. Cell Biol. 2015, 17(4):376-385. 10.1038/ncb3122.
31. Frayn K.N., Shadid S., Hamlani R., Humphreys S.M., Clark M.L., Fielding B.A., et al. Regulation of fatty acid movement in human adipose tissue in the postabsorptive-to-postprandial transition. Am. J. Physiol. 1994, 266:E308-E317.
32. Horowitz J.F., Coppack S.W., Paramore D., Cryer P.E., Zhao G., Klein S. Effect of short-term fasting on lipid kinetics in lean and obese women. Am. J. Physiol. 1999, 276:E278-E284.
33. Combs T.P., Berg A.H., Obici S., Scherer P.E., Rossetti L. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J. Clin. Invest. 2001, 108:1875-1881.
34. Yamauchi T., Kamon J., Waki H., Terauchi Y., Kubota N., Hara K., et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 2001, 7:941-946.
35. Maeda N., Shimomura I., Kishida K., Nishizawa H., Matsuda M., Nagaretani H., et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 2002, 8:731-737.
36. Sada K.E., Yamasaki Y., Maruyama M., Sugiyama H., Yamamura M., Maeshima Y., et al. Altered levels of adipocytokines in association with insulin resistance in patients with systemic lupus erythematosus. J. Rheumatol. 2006, 33:1545-1552.
37. Balistreri C.R., Caruso C., Candore G. The role of adipose tissue and adipokines in obesity-related inflammatory diseases. Mediators Inflamm. 2010, 2010:802078.
38. Leibel R.L. The role of leptin in the control of body weight. Nutr. Rev. 2002, 60:S15-S19. (discussion S68-84, 85-17).
39. Despres J.P., Lemieux I. Abdominal obesity and metabolic syndrome. Nature 2006, 444:881-887.
40. Altintas M.M., Azad A., Nayer B., Contreras G., Zaias J., Faul C., et al. Mast cells, macrophages, and crown-like structures distinguish subcutaneous from visceral fat in mice. J. Lipid Res. 2011, 52:480-488.
41. Wensveen F.M., Jelencic V., Valentic S., Sestan M., Wensveen T.T., Theurich S., et al. NK cells link obesity-induced adipose stress to inflammation and insulin resistance. Nat. Immunol. 2015, 16:376-385.
42. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372:425-432.
43. Bluher M., Mantzoros C.S. From leptin to other adipokines in health and disease: facts and expectations at the beginning of the 21st century. Metab.: clin. Exp. 2015, 64:131-145.
44. Rayner D.V., Trayhurn P. Regulation of leptin production: sympathetic nervous system interactions. J. Mol. Med. 2001, 79:8-20.
45. Trayhurn P., Jones P.M., McGuckin M.M., Goodbody A.E. Effects of overfeeding on energy balance and brown fat thermogenesis in obese (ob/ob) mice. Nature 1982, 295:323-325.
46. Matarese G., Moschos S., Mantzoros C.S. Leptin in immunology. J. Immunol. 2005, 174:3137-3142.
47. Harris R.B. Leptin-much more than a satiety signal. Annu. Rev. Nutr. 2000, 20:45-75.
48. Gorska E., Popko K., Stelmaszczyk-Emmel A., Ciepiela O., Kucharska A., Wasik M. Leptin receptors. Eur. J. Med. Res. 2010, 15(Suppl. 2):50-54.
49. Bates S.H., Stearns W.H., Dundon T.A., Schubert M., Tso A.W., Wang Y., et al. STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature 2003, 421:856-859.
50. Fruhbeck G. Intracellular signalling pathways activated by leptin. Biochem. J. 2006, 393:7-20.
51. Fernandez-Riejos P., Najib S., Santos-Alvarez J., Martin-Romero C., Perez-Perez A., Gonzalez-Yanes C., et al. Role of leptin in the activation of immune cells. Mediators Inflamm. 2010, 2010:568343.
52. Wisse B.E. The inflammatory syndrome: the role of adipose tissue cytokines in metabolic disorders linked to obesity. J. Am. Soc. Nephrol.: JASN 2004, 15:2792-2800.
53. Steppan C.M., Bailey S.T., Bhat S., Brown E.J., Banerjee R.R., Wright C.M., et al. The hormone resistin links obesity to diabetes. Nature 2001, 409:307-312.
54. Kusminski C.M., McTernan P.G., Kumar S. Role of resistin in obesity, insulin resistance and Type II diabetes. Clin. Sci. 2005, 109:243-256.
55. Bokarewa M., Nagaev I., Dahlberg L., Smith U., Tarkowski A. Resistin, an adipokine with potent proinflammatory properties. J. Immunol. 2005, 174:5789-5795.
56. Benomar Y., Gertler A., De Lacy P., Crepin D., Ould Hamouda H., Riffault L., et al. Central resistin overexposure induces insulin resistance through Toll-like receptor 4. Diabetes 2013, 62:102-114.
57. Kim I., Moon S.O., Koh K.N., Kim H., Uhm C.S., Kwak H.J., et al. Molecular cloning, expression, and characterization of angiopoietin-related protein. angiopoietin-related protein induces endothelial cell sprouting. J. Biol. Chem. 1999, 274:26523-26528.
58. Tabata M., Kadomatsu T., Fukuhara S., Miyata K., Ito Y., Endo M., et al. Angiopoietin-like protein 2 promotes chronic adipose tissue inflammation and obesity-related systemic insulin resistance. Cell Metab. 2009, 10:178-188.
59. Doi Y., Ninomiya T., Hirakawa Y., Takahashi O., Mukai N., Hata J., et al. Angiopoietin-like protein 2 and risk of type 2 diabetes in a general Japanese population: the Hisayama study. Diabetes care 2013, 36:98-100.
60. Fukuhara A., Matsuda M., Nishizawa M., Segawa K., Tanaka M., Kishimoto K., et al. Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science 2005, 307:426-430.
61. Adeghate E. Visfatin: structure, function and relation to diabetes mellitus and other dysfunctions. Curr. Med. Chem. 2008, 15:1851-1862.
62. Samal B., Sun Y., Stearns G., Xie C., Suggs S., McNiece I. Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor. Mol. Cell Biol. 1994, 14:1431-1437.
63. Moschen A.R., Kaser A., Enrich B., Mosheimer B., Theurl M., Niederegger H., et al. Visfatin, an adipocytokine with proinflammatory and immunomodulating properties. J. Immunol. 2007, 178:1748-1758.
64. Maeda K., Okubo K., Shimomura I., Funahashi T., Matsuzawa Y., Matsubara K. cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (adipose most abundant gene transcript 1). Biochem. Biophys. Res. Commun. 2012, 425:556-559. 1996.
65. Schaeffer W.I., Chuang A.H., Heintz N., Bresnick E. Sensitivity of cultured rat hepatocytes to aflatoxin B1 and benzo(a)pyrene. In Vitro 1979, 15:437-440.
66. Yamauchi T., Kamon J., Ito Y., Tsuchida A., Yokomizo T., Kita S., et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 2003, 423:762-769.
67. Barnes M.A., Carson M.J., Nair M.G. Non-traditional cytokines: how catecholamines and adipokines influence macrophages in immunity, metabolism and the central nervous system. Cytokine 2015, 72:210-219.
68. Kubota N., Yano W., Kubota T., Yamauchi T., Itoh S., Kumagai H., et al. Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab. 2007, 6:55-68.
69. Saxena A., Chumanevich A., Fletcher E., Larsen B., Lattwein K., Kaur K., et al. Adiponectin deficiency: role in chronic inflammation induced colon cancer. Biochim. Biophys. Acta 2012, 1822:527-536.
70. Tilg H., Moschen A.R. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat. Rev. Immunol. 2006, 6:772-783.
71. Wilk S., Scheibenbogen C., Bauer S., Jenke A., Rother M., Guerreiro M., et al. Adiponectin is a negative regulator of antigen-activated T cells. Eur. J. Immunol. 2011, 41:2323-2332.
72. White R.T., Damm D., Hancock N., Rosen B.S., Lowell B.B., Usher P., et al. Human adipsin is identical to complement factor D and is expressed at high levels in adipose tissue. J. Biol. Chem. 1992, 267:9210-9213.
73. Lo J.C., Ljubicic S., Leibiger B., Kern M., Leibiger I.B., Moede T., et al. Adipsin is an adipokine that improves beta cell function in diabetes. Cell 2014, 158:41-53.
74. Lumeng C.N., Bodzin J.L., Saltiel A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 2007, 117:175-184.
75. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8:958-969.
76. Feuerer M., Herrero L., Cipolletta D., Naaz A., Wong J., Nayer A., 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.
77. Vasanthakumar A., Moro K., Xin A., Liao Y., Gloury R., Kawamoto S., et al. The transcriptional regulators IRF4, BATF and IL-33 orchestrate development and maintenance of adipose tissue-resident regulatory T cells. Nat. Immunol. 2015, 16:276-285.
78. Pichery M., Mirey E., Mercier P., Lefrancais E., Dujardin A., Ortega N., et al. Endogenous IL-33 is highly expressed in mouse epithelial barrier tissues, lymphoid organs, brain, embryos, and inflamed tissues: in situ analysis using a novel Il-33-LacZ gene trap reporter strain. J. Immunol. 2012, 188:3488-3495.
79. Lynch L., Nowak M., Varghese B., Clark J., Hogan A.E., Toxavidis V., et al. Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production. Immunity 2012, 37:574-587.
80. Schipper H.S., Rakhshandehroo M., van de Graaf S.F., Venken K., Koppen A., Stienstra R., et al. Natural killer T cells in adipose tissue prevent insulin resistance. J. Clin. Invest. 2012, 122:3343-3354.
81. Ohmura K., Ishimori N., Ohmura Y., Tokuhara S., Nozawa A., Horii S., et al. Natural killer T cells are involved in adipose tissues inflammation and glucose intolerance in diet-induced obese mice. Arterioscler. Thromb. Vasc. Biol. 2010, 30:193-199.
82. Wu L., Parekh V.V., Gabriel C.L., Bracy D.P., Marks-Shulman P.A., Tamboli R.A., et al. Activation of invariant natural killer T cells by lipid excess promotes tissue inflammation, insulin resistance, and hepatic steatosis in obese mice. Proc. Natl. Acad. Sci. U S A 2012, 109:E1143-E1152.
83. Molofsky A.B., Nussbaum J.C., Liang H.E., Van Dyken S.J., Cheng L.E., Mohapatra A., et al. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J. Exp. Med. 2013, 210:535-549.
84. Wu D., Molofsky A.B., Liang H.E., Ricardo-Gonzalez R.R., Jouihan H.A., Bando J.K., et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011, 332:243-247.
85. Mauer J., Chaurasia B., Goldau J., Vogt M.C., Ruud J., Nguyen K.D., et al. Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesity-associated resistance to insulin. Nat. Immunol. 2014, 15:423-430.
86. Brestoff J.R., Kim B.S., Saenz S.A., Stine R.R., Monticelli L.A., Sonnenberg G.F., et al. Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature 2015, 519:242-246.
87. WHO Fact Sheet on Healthy Diet 2015, WHO.
88. Esposito K., Nappo F., Marfella R., Giugliano G., Giugliano F., Ciotola M., et al. Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation 2002, 106:2067-2072.
89. Ferreira A.V., Menezes-Garcia Z., Viana J.B., Mario E.G., Botion L.M. Distinct metabolic pathways trigger adipocyte fat accumulation induced by high-carbohydrate and high-fat diets. Nutrition 2014, 30:1138-1143.
90. El Khoury D., Anderson G.H. Recent advances in dietary proteins and lipid metabolism. Curr. Opin. Lipid 2013, 24:207-213.
91. Jahan-Mihan A., Luhovyy B.L., El Khoury D., Anderson G.H. Dietary proteins as determinants of metabolic and physiologic functions of the gastrointestinal tract. Nutrients 2011, 3:574-603.
92. Bortolotti M., Kreis R., Debard C., Cariou B., Faeh D., Chetiveaux M., et al. High protein intake reduces intrahepatocellular lipid deposition in humans. Am. J. Clin. Nutr. 2009, 90:1002-1010.
93. Raymond F., Wang L., Moser M., Metairon S., Mansourian R., Zwahlen M.C., et al. Consequences of exchanging carbohydrates for proteins in the cholesterol metabolism of mice fed a high-fat diet. PLoS ONE 2012, 7:e49058.
94. Hosomi R., Fukunaga K., Arai H., Kanda S., Nishiyama T., Yoshida M. Fish protein hydrolysates affect cholesterol metabolism in rats fed non-cholesterol and high-cholesterol diets. J. Med. Food 2012, 15:299-306.
95. Zhang X., Beynen A.C. Lowering effect of dietary milk-whey protein v. casein on plasma and liver cholesterol concentrations in rats. Br. J. Nutr. 1993, 70:139-146.
96. Shukla A., Brandsch C., Bettzieche A., Hirche F., Stangl G.I., Eder K. Isoflavone-poor soy protein alters the lipid metabolism of rats by SREBP-mediated down-regulation of hepatic genes. J. Nutr. Biochem. 2007, 18:313-321.
97. Chen Q., Reimer R.A. Dairy protein and leucine alter GLP-1 release and mRNA of genes involved in intestinal lipid metabolism in vitro. Nutrition 2009, 25:340-349.
98. Oliva M.E., Selenscig D., D'Alessandro M.E., Chicco A., Lombardo Y.B. Soya protein ameliorates the metabolic abnormalities of dysfunctional adipose tissue of dyslipidaemic rats fed a sucrose-rich diet. Br. J. Nutr. 2011, 105:1188-1198.
99. Sarr O., Gondret F., Jamin A., Le Huerou-Luron I., Louveau I. A high-protein neonatal formula induces a temporary reduction of adiposity and changes later adipocyte physiology. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R387-R397.
100. Leidy H.J., Mattes R.D., Campbell W.W. Effects of acute and chronic protein intake on metabolism, appetite, and ghrelin during weight loss. Obesity (Silver Spring) 2007, 15:1215-1225.
101. Tovar A.R., Torres N. The role of dietary protein on lipotoxicity. Biochim. Biophys. Acta 2010, 1801:367-371.
102. Mortensen L.S., Hartvigsen M.L., Brader L.J., Astrup A., Schrezenmeir J., Holst J.J., et al. Differential effects of protein quality on postprandial lipemia in response to a fat-rich meal in type 2 diabetes: comparison of whey, casein, gluten, and cod protein. Am. J. Clin. Nutr. 2009, 90:41-48.
103. Ceriello A., Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler. Thromb. Vasc. Biol. 2004, 24:816-823.
104. Ott M., Gogvadze V., Orrenius S., Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis 2007, 12:913-922.
105. Yin F., Sancheti H., Cadenas E. Mitochondrial thiols in the regulation of cell death pathways. Antioxid. Redox Signal. 2012, 17:1714-1727.
106. Shoelson S.E., Herrero L., Naaz A. Obesity, inflammation, and insulin resistance. Gastroenterology 2007, 132:2169-2180.
107. 2+]i) inhibition of lipolysis in human adipocytes. FASEB J. 2001, 15:2527-2529.
108. Munoz A., Costa M. Nutritionally mediated oxidative stress and inflammation. Oxid. Med. Cell Longev. 2013, 2013:610950.
109. Kromhout D., Yasuda S., Geleijnse J.M., Shimokawa H. Fish oil and omega-3 fatty acids in cardiovascular disease: do they really work?. Eur. Heart J. 2012, 33:436-443.
110. Rommel C., Camps M., Ji H. PI3K delta and PI3K gamma: partners in crime in inflammation in rheumatoid arthritis and beyond?. Nat. Rev. Immunol. 2007, 7:191-201.
111. Bellido C., Lopez-Miranda J., Blanco-Colio L.M., Perez-Martinez P., Muriana F.J., Martin-Ventura J.L., et al. Butter and walnuts, but not olive oil, elicit postprandial activation of nuclear transcription factor kappaB in peripheral blood mononuclear cells from healthy men. Am. J. Clin. Nutr. 2004, 80:1487-1491.
112. Wensveen F.M., Valentic S., Sestan M., Wensveen T.T., Polic B. The "Big Bang" in obese fat: events initiating obesity-induced adipose tissue inflammation. Eur. J. Immunol. 2015, 45(9):2446-2456. 10.1002/eji.201545502.
113. Talukdar S., Oh da Y., Bandyopadhyay G., Li D., Xu J., McNelis J., et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat. Med. 2012, 18:1407-1412.
114. Kanda H., Tateya S., Tamori Y., Kotani K., Hiasa K., Kitazawa R., et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J. Clin. Invest. 2006, 116:1494-1505.
115. Amano S.U., Cohen J.L., Vangala P., Tencerova M., Nicoloro S.M., Yawe J.C., et al. Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation. Cell Metab. 2014, 19:162-171.
116. Goldszmid R.S., Caspar P., Rivollier A., White S., Dzutsev A., Hieny S., et al. NK cell-derived interferon-gamma orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity 2012, 36:1047-1059.
117. Pal D., Dasgupta S., Kundu R., Maitra S., Das G., Mukhopadhyay S., et al. Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat. Med. 2012, 18:1279-1285.
118. Pussinen P.J., Havulinna A.S., Lehto M., Sundvall J., Salomaa V. Endotoxemia is associated with an increased risk of incident diabetes. Diabetes Care 2011, 34:392-397.
119. Khan T., Muise E.S., Iyengar P., Wang Z.V., Chandalia M., Abate N., et al. Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol. Cell Biol. 2009, 29:1575-1591.
120. Ye J., Gao Z., Yin J., He Q. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E1118-E1128.
121. O'Rourke R.W., White A.E., Metcalf M.D., Winters B.R., Diggs B.S., Zhu X., et al. Systemic inflammation and insulin sensitivity in obese IFN-gamma knockout mice. Metab. Clin. Exp. 2012, 61:1152-1161.
122. Nishimura S., Manabe I., Nagasaki M., Eto K., Yamashita H., Ohsugi M., et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 2009, 15:914-920.
123. Winer S., Chan Y., Paltser G., Truong D., Tsui H., Bahrami J., et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat. Med. 2009, 15:921-929.
124. Winer D.A., Winer S., Shen L., Wadia P.P., Yantha J., Paltser G., et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 2011, 17:610-617.
125. Li P., Oh da Y., Bandyopadhyay G., Lagakos W.S., Talukdar S., Osborn O., et al. LTB4 promotes insulin resistance in obese mice by acting on macrophages, hepatocytes and myocytes. Nat. Med. 2015, 21:239-247.
126. Vandanmagsar B., Youm Y.H., Ravussin A., Galgani J.E., Stadler K., Mynatt R.L., et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 2011, 17:179-188.
127. TUFaAO The State of Food Insecurity in the World: Strengthening the Enabling Environment For Food Security and Nutrition 2014, TUFaAO, 〈http://www.fao.org/3/a-i4030e.pdf2014〉.
128. Caulfield L.E., de Onis M., Blossner M., Black R.E. Undernutrition as an underlying cause of child deaths associated with diarrhea, pneumonia, malaria, and measles. Am. J. Clin. Nutr. 2004, 80:193-198.
129. Hickman D., Jones M.K., Zhu S., Kirkpatrick E., Ostrov D.A., Wang X., et al. The effect of malnutrition on norovirus infection. MBio 2014, 5(2). e01032-13. 10.1128/mBio.01032-13.
130. Neumann C.G., Gewa C., Bwibo N.O. Child nutrition in developing countries. Pediatr. Ann. 2004, 33:658-674.
131. Black R.E., Victora C.G., Walker S.P., Bhutta Z.A., Christian P., de Onis M., et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 2013, 382:427-451.
132. Wang T., Hung C.C., Randall D.J. The comparative physiology of food deprivation: from feast to famine. Annu. Rev. Physiol. 2006, 68:223-251.
133. Cahill G.F. Fuel metabolism in starvation. Annu. Rev. Nutr. 2006, 26:1-22.
134. Hardie D.G. AMP-activated protein kinase: maintaining energy homeostasis at the cellular and whole-body levels. Annu. Rev. Nutr. 2014, 34:31-55.
135. Fryer L.G., Foufelle F., Barnes K., Baldwin S.A., Woods A., Carling D. Characterization of the role of the AMP-activated protein kinase in the stimulation of glucose transport in skeletal muscle cells. Biochem. J. 2002, 363:167-174.
136. Habets D.D., Coumans W.A., El Hasnaoui M., Zarrinpashneh E., Bertrand L., Viollet B., et al. Crucial role for LKB1 to AMPKalpha2 axis in the regulation of CD36-mediated long-chain fatty acid uptake into cardiomyocytes. Biochim. Biophys. Acta 2009, 1791:212-219.
137. Kurth-Kraczek E.J., Hirshman M.F., Goodyear L.J., Winder W.W. 5' AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 1999, 48:1667-1671.
138. Marsin A.S., Bertrand L., Rider M.H., Deprez J., Beauloye C., Vincent M.F., et al. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 2000, 10:1247-1255.
139. Marsin A.S., Bouzin C., Bertrand L., Hue L. The stimulation of glycolysis by hypoxia in activated monocytes is mediated by AMP-activated protein kinase and inducible 6-phosphofructo-2-kinase. J. Biol. Chem. 2002, 277:30778-30783.
140. Merrill G.F., Kurth E.J., Hardie D.G., Winder W.W. AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am. J. Physiol. 1997, 273:E1107-E1112.
141. Egan D.F., Shackelford D.B., Mihaylova M.M., Gelino S., Kohnz R.A., Mair W., et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011, 331:456-461.
142. Russell R.C., Tian Y., Yuan H., Park H.W., Chang Y.Y., Kim J., et al. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat. Cell Biol. 2013, 15:741-750.
143. Bultot L., Guigas B., Von Wilamowitz-Moellendorff A., Maisin L., Vertommen D., Hussain N., et al. AMP-activated protein kinase phosphorylates and inactivates liver glycogen synthase. Biochem. J. 2012, 443:193-203.
144. Gillespie J.G., Hardie D.G. Phosphorylation and inactivation of HMG-CoA reductase at the AMP-activated protein kinase site in response to fructose treatment of isolated rat hepatocytes. FEBS Lett. 1992, 306:59-62.
145. Jorgensen S.B., Nielsen J.N., Birk J.B., Olsen G.S., Viollet B., Andreelli F., et al. The alpha2-5'AMP-activated protein kinase is a site 2 glycogen synthase kinase in skeletal muscle and is responsive to glucose loading. Diabetes 2004, 53:3074-3081.
146. Koo S.H., Flechner L., Qi L., Zhang X., Screaton R.A., Jeffries S., et al. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 2005, 437:1109-1111.
147. Mihaylova M.M., Shaw R.J. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell Biol. 2011, 13:1016-1023.
148. Claret M., Smith M.A., Batterham R.L., Selman C., Choudhury A.I., Fryer L.G., et al. AMPK is essential for energy homeostasis regulation and glucose sensing by POMC and AgRP neurons. J. Clin. Invest. 2007, 117:2325-2336.
149. McCrimmon R.J., Shaw M., Fan X., Cheng H., Ding Y., Vella M.C., et al. Key role for AMP-activated protein kinase in the ventromedial hypothalamus in regulating counterregulatory hormone responses to acute hypoglycemia. Diabetes 2008, 57:444-450.
150. Willesen M.G., Kristensen P., Romer J. Co-localization of growth hormone secretagogue receptor and NPY mRNA in the arcuate nucleus of the rat. Neuroendocrinology 1999, 70:306-316.
151. Yamauchi T., Kamon J., Minokoshi Y., Ito Y., Waki H., Uchida S., et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 2002, 8:1288-1295.
152. Cutrera A.P., Zenuto R.R., Luna F., Antenucci C.D. Mounting a specific immune response increases energy expenditure of the subterranean rodent Ctenomys talarum (tuco-tuco): implications for intraspecific and interspecific variation in immunological traits. J. Exp. Biol. 2010, 213:715-724.
153. Ganeshan K., Chawla A. Metabolic regulation of immune responses. Annu. Rev. Immunol. 2014, 32:609-634.
154. Segal A.W. How neutrophils kill microbes. Annu. Rev. Immunol. 2005, 23:197-223.
155. Boxer L.A., Baehner R.L., Davis J. The effect of 2-deoxyglucose on guinea pig polymorphonuclear leukocyte phagocytosis. J. Cell. Physiol. 1977, 91:89-102.
156. Sbarra A.J., Karnovsky M.L. The biochemical basis of phagocytosis. I. Metabolic changes during the ingestion of particles by polymorphonuclear leukocytes. J. Biol. Chem. 1959, 234:1355-1362.
157. Weisdorf D.J., Craddock P.R., Jacob H.S. Granulocytes utilize different energy sources for movement and phagocytosis. Inflammation 1982, 6:245-256.
158. Wynn T.A., Chawla A., Pollard J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496:445-455.
159. Vats D., Mukundan L., Odegaard J.I., Zhang L., Smith K.L., Morel C.R., et al. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 2006, 4:13-24.
160. Newsholme P., Curi R., Gordon S., Newsholme E.A. Metabolism of glucose, glutamine, long-chain fatty acids and ketone bodies by murine macrophages. Biochem. J. 1986, 239:121-125.
161. Newsholme P., Newsholme E.A. Rates of utilization of glucose, glutamine and oleate and formation of end-products by mouse peritoneal macrophages in culture. Biochem. J. 1989, 261:211-218.
162. Cramer T., Yamanishi Y., Clausen B.E., Forster I., Pawlinski R., Mackman N., et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 2003, 112:645-657.
163. Frauwirth K.A., Riley J.L., Harris M.H., Parry R.V., Rathmell J.C., Plas D.R., et al. The CD28 signaling pathway regulates glucose metabolism. Immunity 2002, 16:769-777.
164. Delgoffe G.M., Kole T.P., Zheng Y., Zarek P.E., Matthews K.L., Xiao B., et al. The mTOR kinase differentially regulates effector and regulatory T cell lineage commitment. Immunity 2009, 30:832-844.
165. Michalek R.D., Gerriets V.A., Jacobs S.R., Macintyre A.N., MacIver N.J., Mason E.F., et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J. Immunol. 2011, 186:3299-3303.
166. Pearce E.L., Walsh M.C., Cejas P.J., Harms G.M., Shen H., Wang L.S., et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 2009, 460:103-107.
167. Gerriets V.A., MacIver N.J. Role of T cells in malnutrition and obesity. Front. Immunol. 2014, 5:379.
168. Howard J.K., Lord G.M., Matarese G., Vendetti S., Ghatei M.A., Ritter M.A., et al. Leptin protects mice from starvation-induced lymphoid atrophy and increases thymic cellularity in ob/ob mice. J. Clin. Invest. 1999, 104:1051-1059.
169. Procaccini C., De Rosa V., Galgani M., Carbone F., Cassano S., Greco D., et al. Leptin-induced mTOR activation defines a specific molecular and transcriptional signature controlling CD4+ effector T cell responses. J. Immunol. 2012, 189:2941-2953.
170. Saucillo D.C., Gerriets V.A., Sheng J., Rathmell J.C., Maciver N.J. Leptin metabolically licenses T cells for activation to link nutrition and immunity. J. Immunol. 2014, 192:136-144.
171. Tanaka M., Suganami T., Kim-Saijo M., Toda C., Tsuiji M., Ochi K., et al. Role of central leptin signaling in the starvation-induced alteration of B-cell development. J. Neurosci. 2011, 31:8373-8380.
172. Pena-Cruz V., Reiss C.S., McIntosh K. Sendai virus infection of mice with protein malnutrition. J. Virol. 1989, 63:3541-3544.
173. Taylor A.K., Cao W., Vora K.P., De La Cruz J., Shieh W.J., Zaki S.R., et al. Protein energy malnutrition decreases immunity and increases susceptibility to influenza infection in mice. J. Infect. Dis. 2013, 207:501-510.
174. Najera O., Gonzalez C., Toledo G., Lopez L., Ortiz R. Flow cytometry study of lymphocyte subsets in malnourished and well-nourished children with bacterial infections. Clin. Diagn. Lab. Immunol. 2004, 11:577-580.
175. Xia C.Q., Chernatynskaya A.V., Looney B., Wan S., Clare-Salzler M.J. Anti-CD3 antibody treatment induces hypoglycemia and super tolerance to glucose challenge in mice through enhancing glucose consumption by activated lymphocytes. J. Immunol. Res. 2014, 2014:326708.
176. Jacobs S.R., Herman C.E., Maciver N.J., Wofford J.A., Wieman H.L., Hammen J.J., et al. Glucose uptake is limiting in T cell activation and requires CD28-mediated Akt-dependent and independent pathways. J. Immunol. 2008, 180:4476-4486.
177. Cham C.M., Gajewski T.F. Glucose availability regulates IFN-gamma production and p70S6 kinase activation in CD8+ effector T cells. J. Immunol. 2005, 174:4670-4677.
178. Gonzalez-Torres C., Gonzalez-Martinez H., Miliar A., Najera O., Graniel J., Firo V., et al. Effect of malnutrition on the expression of cytokines involved in Th1 cell differentiation. Nutrients 2013, 5:579-593.
179. Mengheri E., Nobili F., Crocchioni G., Lewis J.A. Protein starvation impairs the ability of activated lymphocytes to produce interferon-gamma. J. Interferon Res. 1992, 12:17-21.
180. Gonzalez-Martinez H., Rodriguez L., Najera O., Cruz D., Miliar A., Dominguez A., et al. Expression of cytokine mRNA in lymphocytes of malnourished children. J. Clin. Immunol. 2008, 28:593-599.
181. Murphy E.D., Roths J.B. A Y chromosome associated factor in strain BXSB producing accelerated autoimmunity and lymphoproliferation. Arthritis Rheum. 1979, 22:1188-1194.
182. Piccio L., Stark J.L., Cross A.H. Chronic calorie restriction attenuates experimental autoimmune encephalomyelitis. J. Leukoc. Biol. 2008, 84:940-948.
183. Sanna V., Di Giacomo A., La Cava A., Lechler R.I., Fontana S., Zappacosta S., et al. Leptin surge precedes onset of autoimmune encephalomyelitis and correlates with development of pathogenic T cell responses. J. Clin. Invest. 2003, 111:241-250.
184. Clinthorne J.F., Beli E., Duriancik D.M., Gardner E.M. NK cell maturation and function in C57BL/6 mice are altered by caloric restriction. J. Immunol. 2013, 190:712-722.
185. Ritz B.W., Aktan I., Nogusa S., Gardner E.M. Energy restriction impairs natural killer cell function and increases the severity of influenza infection in young adult male C57BL/6 mice. J. Nutr. 2008, 138:2269-2275.
186. Banks A.S., Davis S.M., Bates S.H., Myers M.G. Activation of downstream signals by the long form of the leptin receptor. J. Biol. Chem. 2000, 275:14563-14572.
187. La Cava A., Matarese G. The weight of leptin in immunity. Nat. Rev. Immunol. 2004, 4:371-379.
188. Rodriguez L., Graniel J., Ortiz R. Effect of leptin on activation and cytokine synthesis in peripheral blood lymphocytes of malnourished infected children. Clin. Exp. Immunol. 2007, 148:478-485.
189. Mancuso P., Gottschalk A., Phare S.M., Peters-Golden M., Lukacs N.W., Huffnagle G.B. Leptin-deficient mice exhibit impaired host defense in Gram-negative pneumonia. J. Immunol. 2002, 168:4018-4024.
190. Dixit V.D., Mielenz M., Taub D.D., Parvizi N. Leptin induces growth hormone secretion from peripheral blood mononuclear cells via a protein kinase C- and nitric oxide-dependent mechanism. Endocrinology 2003, 144:5595-5603.
191. Caldefie-Chezet F., Poulin A., Tridon A., Sion B., Vasson M.P. Leptin: a potential regulator of polymorphonuclear neutrophil bactericidal action?. J. Leukoc. Biol. 2001, 69:414-418.
192. Caldefie-Chezet F., Poulin A., Vasson M.P. Leptin regulates functional capacities of polymorphonuclear neutrophils. Free Radical Res. 2003, 37:809-814.
193. Siegmund B., Lear-Kaul K.C., Faggioni R., Fantuzzi G. Leptin deficiency, not obesity, protects mice from Con A-induced hepatitis. Eur. J. Immunol. 2002, 32:552-560.
194. Tian Z., Sun R., Wei H., Gao B. Impaired natural killer (NK) cell activity in leptin receptor deficient mice: leptin as a critical regulator in NK cell development and activation. Biochem. Biophys. Res. Commun. 2002, 298:297-302.
195. Zhao Y., Sun R., You L., Gao C., Tian Z. Expression of leptin receptors and response to leptin stimulation of human natural killer cell lines. Biochem. Biophys. Res. Commun. 2003, 300:247-252.
196. McGorrian C., Yusuf S., Islam S., Jung H., Rangarajan S., Avezum A., et al. Estimating modifiable coronary heart disease risk in multiple regions of the world: the INTERHEART modifiable risk score. Eur. Heart J. 2011, 32:581-589.
197. Wolf M.J., Adili A., Piotrowitz K., Abdullah Z., Boege Y., Stemmer K., et al. Metabolic activation of intrahepatic CD8+ T cells and NKT cells causes nonalcoholic steatohepatitis and liver cancer via cross-talk with hepatocytes. Cancer Cell 2014, 26:549-564.
198. Suganami T., Nishida J., Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler. Thromb. Vasc. Biol. 2005, 25:2062-2068.
199. Lopez-Garcia E., Schulze M.B., Fung T.T., Meigs J.B., Rifai N., Manson J.E., et al. Major dietary patterns are related to plasma concentrations of markers of inflammation and endothelial dysfunction. Am. J. Clin. Nutr. 2004, 80:1029-1035.
200. Kabir M., Skurnik G., Naour N., Pechtner V., Meugnier E., Rome S., et al. Treatment for 2 mo with n 3 polyunsaturated fatty acids reduces adiposity and some atherogenic factors but does not improve insulin sensitivity in women with type 2 diabetes: a randomized controlled study. Am. J. Clin. Nutr. 2007, 86:1670-1679.
201. Kallio P., Kolehmainen M., Laaksonen D.E., Kekalainen J., Salopuro T., Sivenius K., et al. Dietary carbohydrate modification induces alterations in gene expression in abdominal subcutaneous adipose tissue in persons with the metabolic syndrome: the FUNGENUT study. Am. J. Clin. Nutr. 2007, 85:1417-1427.
202. Uusitupa M., Hermansen K., Savolainen M.J., Schwab U., Kolehmainen M., Brader L., et al. Effects of an isocaloric healthy Nordic diet on insulin sensitivity, lipid profile and inflammation markers in metabolic syndrome-a randomized study (SYSDIET). J. Int. Med. 2013, 274:52-66.
203. Kolehmainen M., Ulven S.M., Paananen J., de Mello V., Schwab U., Carlberg C., et al. Healthy Nordic diet downregulates the expression of genes involved in inflammation in subcutaneous adipose tissue in individuals with features of the metabolic syndrome. Am. J. Clin. Nutr. 2015, 101:228-239.
204. Baggio L.L., Drucker D.J. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007, 132:2131-2157.
205. Gogebakan O., Osterhoff M.A., Schuler R., Pivovarova O., Kruse M., Seltmann A.C., et al. GIP increases adipose tissue expression and blood levels of MCP-1 in humans and links high energy diets to inflammation: a randomised trial. Diabetologia 2015, 58:1759-1768.
206. Milner J.J., Beck M.A. The impact of obesity on the immune response to infection. Proc. Nutr. Soc. 2012, 71:298-306.
207. Donath M.Y., Shoelson S.E. Type 2 diabetes as an inflammatory disease. Nat. Rev. Immunol. 2011, 11:98-107.
208. Phung D.T., Wang Z., Rutherford S., Huang C., Chu C. Body mass index and risk of pneumonia: a systematic review and meta-analysis. Obes. Rev. 2013, 14:839-857.