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Regulation of energy balance by inflammation: Common theme in physiology and pathology

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Abstract

Inflammation regulates energy metabolism in both physiological and pathological conditions. Pro-inflammatory cytokines involves in energy regulation in several conditions, such as obesity, aging (calorie restriction), sports (exercise), and cancer (cachexia). Here, we introduce a view of integrative physiology to understand pro-inflammatory cytokines in the control of energy expenditure. In obesity, chronic inflammation is derived from energy surplus that induces adipose tissue expansion and adipose tissue hypoxia. In addition to the detrimental effect on insulin sensitivity, pro-inflammatory cytokines also stimulate energy expenditure and facilitate adipose tissue remodeling. In caloric restriction (CR), inflammatory status is decreased by low energy intake that results in less energy supply to immnue cells to favor energy saving under caloric restriction. During physical exercise, inflammatory status is elevated due to muscle production of pro-inflammatory cytokines, which promote fatty acid mobilization from adipose tissue to meet the muscle energy demand. In cancer cachexia, chronic inflammation is elevated by the immune response in the fight against cancer. The energy expenditure from chronic inflammation contributes to weight loss. Immune tolerant cancer cells gains more nutrients during the inflammation. In these conditions, inflammation coordinates energy distribution and energy demand between tissues. If the body lacks response to the pro-inflammatory cytokines (Inflammation Resistance), the energy metabolism will be impaired leading to an increased risk for obesity. In contrast, super-induction of the inflammation activity leads to weight loss and malnutrition in cancer cachexia. In summary, inflammation is a critical component in the maintenance of energy balance in the body. Literature is reviewed in above fields to support this view.

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References

  1. Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444(7121):860–7.

    Article  CAS  PubMed  Google Scholar 

  2. Qatanani M, Lazar MA. Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev. 2007;21(12):1443–55.

    Article  CAS  PubMed  Google Scholar 

  3. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol. 2010;72:219–46.

    Article  CAS  PubMed  Google Scholar 

  4. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011;11(2):98–107.

    Article  CAS  PubMed  Google Scholar 

  5. Saltiel AR. Insulin resistance in the defense against obesity. Cell Metab. 2012;15(6):798–804.

    Article  CAS  PubMed  Google Scholar 

  6. De Souza CT, Araujo EP, Bordin S, Ashimine R, Zollner RL, Boschero AC, et al. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology. 2005;146(10):4192–9.

    Article  PubMed  Google Scholar 

  7. Zhang X, Zhang G, Zhang H, Karin M, Bai H, Cai D. Hypothalamic IKK[beta]/NF-[kappa]B and ER stress link overnutrition to energy imbalance and obesity. Cell. 2008;135(1):61–73.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Kleinridders A, Schenten D, Konner AC, Belgardt BF, Mauer J, Okamura T, et al. MyD88 signaling in the CNS is required for development of fatty acid-induced leptin resistance and diet-induced obesity. Cell Metab. 2009;10(4):249–59.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Holland WL, Bikman BT, Wang LP, Yuguang G, Sargent KM, Bulchand S, et al. Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J Clin Invest. 2011;121(5):1858–70.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Ozcan U, Cao Q, Yilmaz E, Lee A-H, Iwakoshi NN, Ozdelen E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 2004;306(5695):457–61.

    Article  PubMed  Google Scholar 

  11. Lee Yun S, Kim J-W, Osborne O, Oh Da Y, Sasik R, Schenk S, et al. Increased adipocyte O2 consumption triggers HIF-1α, causing inflammation and insulin resistance in obesity. Cell. 2014;157(6):1339–52.

    Article  PubMed  Google Scholar 

  12. Qiu Y, Nguyen Khoa D, Odegaard Justin I, Cui X, Tian X, Locksley Richard M, et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell. 2014;157(6):1292–308.

    Article  CAS  PubMed  Google Scholar 

  13. Rao Rajesh R, Long Jonathan Z, White James P, Svensson Katrin J, Lou J, Lokurkar I, et al. Meteorin-like is a hormone that regulates immune-adipose interactions to increase beige fat thermogenesis. Cell. 2014;157(6):1279–91.

    Article  CAS  PubMed  Google Scholar 

  14. Ye J, McGuinness OP. Inflammation during obesity is not all bad: evidence from animal and human studies. Am J Physiol Endocrinol Metab. 2013;304(5):E466–77.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Samuel VT, Shulman GI. Mechanisms for insulin resistance: common threads and missing links. Cell. 2012;148(5):852–71.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Johnson AM, Olefsky JM. The origins and drivers of insulin resistance. Cell. 2013;152(4):673–84.

    Article  CAS  PubMed  Google Scholar 

  17. Ye J. Mechanisms of insulin resistance in obesity. Front Med. 2013;7(1):14–24.

    Article  PubMed Central  PubMed  Google Scholar 

  18. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest. 2006;116(7):1793–801.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Ye J. Emerging role of adipose tissue hypoxia in obesity and insulin resistance. Int J Obes. 2009;33(1):54–66.

    Article  CAS  Google Scholar 

  20. Trayhurn P. Hypoxia and adipose tissue function and dysfunction in obesity. Physiol Rev. 2013;93(1):1–21.

    Article  CAS  PubMed  Google Scholar 

  21. Brose N, Rosenmund C. Move over protein kinase C, you’ve got company: alternative cellular effectors of diacylglycerol and phorbol esters. J Cell Sci. 2002;115(Pt 23):4399–411.

    Article  CAS  PubMed  Google Scholar 

  22. Lee JY, Ye J, Gao Z, Youn HS, Lee WH, Zhao L, et al. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J Biol Chem. 2003;278(39):37041–51.

    Article  CAS  PubMed  Google Scholar 

  23. Weigert C, Brodbeck K, Staiger H, Kausch C, Machicao F, Haring HU, et al. Palmitate, but not unsaturated fatty acids, induces the expression of interleukin-6 in human myotubes through proteasome-dependent activation of nuclear factor kappa B. J Biol Chem. 2004;279(23):23942–52.

    Article  CAS  PubMed  Google Scholar 

  24. Gao Z, Zhang X, Zuberi A, Hwang D, Quon MJ, Lefevre M, et al. Inhibition of insulin sensitivity by free fatty acids requires activation of multiple serine kinases in 3 T3-L1 adipocytes. Mol Endocrinol. 2004;18(8):2024–34.

  25. Costanzi S, Neumann S, Gershengorn MC. Seven transmembrane-spanning receptors for free fatty acids as therapeutic targets for diabetes mellitus: pharmacological, phylogenetic, and drug discovery aspects. J Biol Chem. 2008;283(24):16269–73.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Nakamura T, Furuhashi M, Li P, Cao H, Tuncman G, Sonenberg N, et al. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell. 2010;140(3):338–48.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Ye J, Gao Z, Yin J, He H. 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:E1118–28.

    Article  CAS  PubMed  Google Scholar 

  28. Hosogai N, Fukuhara A, Oshima K, Miyata Y, Tanaka S, Segawa K, et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes. 2007;56(4):901–11.

    Article  CAS  PubMed  Google Scholar 

  29. Halberg N, Khan T, Trujillo ME, Wernstedt-Asterholm I, Attie AD, Sherwani S, et al. HIF 1 alpha induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol. 2009;29(16):4467–83.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Khan T, Muise ES, Iyengar P, Wang ZV, Chandalia M, Abate N, et al. Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol Cell Biol. 2009;29(6):1575–91.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Ye J. Regulation of PPARg function by TNF-a. Biochem Biophys Res Commun. 2008;374:405–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Ye J. Adipose tissue vascularization: its role in chronic inflammation. Curr Diabet Rep. 2011;11(3):203–10.

    Article  CAS  Google Scholar 

  33. Sun K, Kusminski CM, Scherer PE. Adipose tissue remodeling and obesity. J Clin Invest. 2011;121(6):2094–101.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Pang C, Gao Z, Yin J, Zhang J, Jia W, Ye J. Macrophage infiltration into adipose tissue may promote angiogenesis for adipose tissue remodeling in obesity. Am J Physiol Endocrinol Metab. 2008;295:E313–22.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Yin J, Lee JH, Zhang J, Gao Z, Polotsky VY, Ye J. Regulation of hepatocyte growth factor expression by NF-kB and PPARggamma in adipose tissue. Am J Physiol Endocrinol Metab. 2014.

  36. Xu F, Burk D, Gao Z, Yin J, Zhang X, Weng J, et al. Angiogenic deficiency and adipose tissue dysfunction are associated with macrophage malfunction in SIRT1−/− Mice. Endocrinology. 2012;153(4):1706–16.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Nishimura S, Manabe I, Nagasaki M, Hosoya Y, Yamashita H, Fujita H, et al. Adipogenesis in obesity requires close interplay between differentiating adipocytes, stromal cells, and blood vessels. Diabetes. 2007;56(6):1517–26.

    Article  CAS  PubMed  Google Scholar 

  38. Cho C-H, Jun Koh Y, Han J, Sung H-K, Jong Lee H, Morisada T, et al. Angiogenic role of LYVE-1-positive macrophages in adipose tissue. Circ Res. 2007;100(4):e47–57.

    Article  CAS  PubMed  Google Scholar 

  39. He Q, Gao Z, Yin J, Zhang J, Yun Z, Ye J. Regulation of HIF-1a activity in adipose tissue by obesity-associated factors: adipogenesis, insulin and hypoxia. Am J Physiol Endocrinol Metab. 2011;300:E877–85.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Cao Y. Adipose tissue angiogenesis as a therapeutic target for obesity and metabolic diseases. Nat Rev Drug Discov. 2010;9(2):107–15.

    Article  CAS  PubMed  Google Scholar 

  41. Myers MG, Olson DP. Central nervous system control of metabolism. Nature. 2012;491(7424):357–63.

    Article  CAS  PubMed  Google Scholar 

  42. Cohen SL, Halaas JL, Friedman JM, Chait BT, Bennett L, Chang D, et al. Human leptin characterization. Nature. 1996;382(6592):589.

    Article  CAS  PubMed  Google Scholar 

  43. Grosfeld A, Andre J, Hauguel-De Mouzon S, Berra E, Pouyssegur J, Guerre-Millo M. Hypoxia-inducible factor 1 transactivates the human leptin gene promoter. J Biol Chem. 2002;277(45):42953–7.

    Article  CAS  PubMed  Google Scholar 

  44. Grunfeld C, Zhao C, Fuller J, Pollack A, Moser A, Friedman J, et al. Endotoxin and cytokines induce expression of leptin, the ob gene product, in hamsters. J Clin Invest. 1996;97(9):2152–7.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Sarraf P, Frederich RC, Turner EM, Ma G, Jaskowiak NT, Rivet 3rd DJ, et al. Multiple cytokines and acute inflammation raise mouse leptin levels: potential role in inflammatory anorexia. J Exp Med. 1997;185(1):171–5.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Zumbach MS, Boehme MWJ, Wahl P, Stremmel W, Ziegler R, Nawroth PP. Tumor necrosis factor increases serum leptin levels in humans. J Clin Endocrinol Metab. 1997;82(12):4080–2.

    Article  CAS  PubMed  Google Scholar 

  47. Gan L, Guo K, Cremona ML, McGraw TE, Leibel RL, Zhang Y. TNF-alpha up-regulates protein level and cell surface expression of the leptin receptor by stimulating its export via a PKC-dependent mechanism. Endocrinology. 2012;153(12):5821–33.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature. 1998;394(6696):897–901.

    Article  CAS  PubMed  Google Scholar 

  49. Loffreda S, Yang SQ, Lin HZ, Karp CL, Brengman ML, Wang DJ, et al. Leptin regulates proinflammatory immune responses. FASEB J. 1998;12(1):57–65.

    CAS  PubMed  Google Scholar 

  50. Mattioli B, Straface E, Quaranta MG, Giordani L, Viora M. Leptin promotes differentiation and survival of human dendritic cells and licenses them for Th1 priming. J Immunol. 2005;174(11):6820–8.

    Article  CAS  PubMed  Google Scholar 

  51. Gainsford T, Willson TA, Metcalf D, Handman E, McFarlane C, Ng A, et al. Leptin can induce proliferation, differentiation, and functional activation of hemopoietic cells. Proc Natl Acad Sci. 1996;93(25):14564–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Martin-Romero C, Sanchez-Margalet V. Human leptin activates PI3K and MAPK pathways in human peripheral blood mononuclear cells: possible role of Sam68. Cell Immunol. 2001;212(2):83–91.

    Article  CAS  PubMed  Google Scholar 

  53. Najib S, Sanchez-Margalet V. Human leptin promotes survival of human circulating blood monocytes prone to apoptosis by activation of p42/44 MAPK pathway. Cell Immunol. 2002;220(2):143–9.

    Article  CAS  PubMed  Google Scholar 

  54. Morton GJ, Schwartz MW. Leptin and the central nervous system control of glucose metabolism. Physiol Rev. 2011;91(2):389–411.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  55. Kahles F, Meyer C, Mollmann J, Diebold S, Findeisen HM, Lebherz C, et al. GLP-1 secretion is increased by inflammatory stimuli in an IL-6-dependent manner, leading to hyperinsulinemia and blood glucose lowering. Diabetes. 2014;63(10):3221–9.

    Article  CAS  PubMed  Google Scholar 

  56. Barrera JG, Sandoval DA, D’Alessio DA, Seeley RJ. GLP-1 and energy balance: an integrated model of short-term and long-term control. Nat Rev Endocrinol. 2011;7(9):507–16.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Beiroa D, Imbernon M, Gallego R, Senra A, Herranz D, Villarroya F, et al. GLP-1 agonism stimulates brown adipose tissue thermogenesis and browning through hypothalamic AMPK. Diabetes. 2014;63(10):3346–58.

    Article  CAS  PubMed  Google Scholar 

  58. Jimenez A, Mari A, Casamitjana R, Lacy A, Ferrannini E, Vidal J. GLP-1 and glucose tolerance after sleeve gastrectomy in morbidly obese subjects with type 2 diabetes. Diabetes. 2014;63(10):3372–7.

    Article  CAS  PubMed  Google Scholar 

  59. Wilson-Perez HE, Chambers AP, Ryan KK, Li B, Sandoval DA, Stoffers D, et al. Vertical sleeve gastrectomy is effective in two genetic mouse models of glucagon-like Peptide 1 receptor deficiency. Diabetes. 2013;62(7):2380–5.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  60. Ye J, Hao Z, Mumphrey MB, Townsend RL, Patterson LM, Stylopoulos N, et al. GLP-1 receptor signaling is not required for reduced body weight after RYGB in rodents. Am J Physiol Regul Integr Comp Physiol. 2014;306(5):R352–362.

    Article  CAS  PubMed  Google Scholar 

  61. Anforth HR, Bluthe RM, Bristow A, Hopkins S, Lenczowski MJ, Luheshi G, et al. Biological activity and brain actions of recombinant rat interleukin-1alpha and interleukin-1beta. Eur Cytokine Netw. 1998;9(3):279–88.

    CAS  PubMed  Google Scholar 

  62. Garcia MC, Wernstedt I, Berndtsson A, Enge M, Bell M, Hultgren O, et al. Mature-onset obesity in interleukin-1 receptor I knockout mice. Diabetes. 2006;55(5):1205–13.

    Article  CAS  PubMed  Google Scholar 

  63. Wallenius V, Wallenius K, Ahren B, Rudling M, Carlsten H, Dickson SL, et al. Interleukin-6-deficient mice develop mature-onset obesity. Nat Med. 2002;8(1):75–9.

    Article  CAS  PubMed  Google Scholar 

  64. Xu H, Hirosumi J, Uysal KT, Guler AD, Hotamisligil GS. Exclusive action of transmembrane TNF alpha in adipose tissue leads to reduced adipose mass and local but not systemic insulin resistance. Endocrinology. 2002;143(4):1502–11.

    CAS  PubMed  Google Scholar 

  65. Pamir N, McMillen TS, Kaiyala KJ, Schwartz MW, LeBoeuf RC. Receptors for tumor necrosis factor-{alpha} play a protective role against obesity and alter adipose tissue macrophage status. Endocrinology. 2009;150(9):4124–34.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. Lee YH, Petkova AP, Granneman JG. Identification of an adipogenic niche for adipose tissue remodeling and restoration. Cell Metab. 2013;18(3):355–67.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  67. Petruzzelli M, Schweiger M, Schreiber R, Campos-Olivas R, Tsoli M, Allen J, et al. A switch from white to brown fat increases energy expenditure in cancer-associated cachexia. Cell Metab. 2014;20(3):433–47.

    Article  CAS  PubMed  Google Scholar 

  68. Kong X, Banks A, Liu T, Kazak L, Rao RR, Cohen P, et al. IRF4 is a key thermogenic transcriptional partner of PGC-1alpha. Cell. 2014;158(1):69–83.

    Article  CAS  PubMed  Google Scholar 

  69. Chida D, Osaka T, Hashimoto O, Iwakura Y. Combined interleukin-6 and interleukin-1 deficiency causes obesity in young mice. Diabetes. 2006;55(4):971–7.

    Article  CAS  PubMed  Google Scholar 

  70. Tang T, Zhang J, Yin J, Staszkiewicz J, Gawronska-Kozak B, Mynatt R, et al. Uncoupling of inflammation and insulin resistance by NF-kB in transgenic mice through induction of energy expenditure. J Biol Chem. 2010;285:4637–44.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Jiao P, Feng B, Ma J, Nie Y, Paul E, Li Y, et al. Constitutive activation of IKKβ in adipose tissue prevents diet-induced obesity in mice. Endocrinology. 2012;153(1):154–65.

    Article  CAS  PubMed  Google Scholar 

  72. Barra NG, Reid S, MacKenzie R, Werstuck G, Trigatti BL, Richards C, et al. Interleukin-15 contributes to the regulation of murine adipose tissue and human adipocytes. Obesity (Silver Spring). 2010;18(8):1601–7.

    Article  CAS  Google Scholar 

  73. Vegiopoulos A, Muller-Decker K, Strzoda D, Schmitt I, Chichelnitskiy E, Ostertag A, et al. Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science. 2010;328(5982):1158–61.

    Article  CAS  PubMed  Google Scholar 

  74. Goldfine AB, Fonseca V, Jablonski KA, Chen YD, Tipton L, Staten MA, et al. Targeting inflammation using salsalate in type 2 diabetes study T. salicylate (salsalate) in patients with type 2 diabetes: a randomized trial. Ann Intern Med. 2013;159(1):1–12.

    Article  PubMed Central  PubMed  Google Scholar 

  75. Saraceno R, Schipani C, Mazzotta A, Esposito M, Di Renzo L, De Lorenzo A, et al. Effect of anti-tumor necrosis factor-alpha therapies on body mass index in patients with psoriasis. Pharmacol Res. 2008;57(4):290–5.

    Article  CAS  PubMed  Google Scholar 

  76. Younis S, Rosner I, Rimar D, Boulman N, Rozenbaum M, Odeh M, et al. Weight change during pharmacological blockade of interleukin-6 or tumor necrosis factor-alpha in patients with inflammatory rheumatic disorders: a 16-week comparative study. Cytokine. 2013;61(2):353–5.

    Article  CAS  PubMed  Google Scholar 

  77. Fontana L. Neuroendocrine factors in the regulation of inflammation: excessive adiposity and calorie restriction. Exp Gerontol. 2009;44(1–2):41–5.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. Morgan TE, Wong AM, Finch CE. Anti-inflammatory mechanisms of dietary restriction in slowing aging processes. Interdiscip Top Gerontol. 2007;35:83–97.

    CAS  PubMed  Google Scholar 

  79. Muzumdar R, Allison DB, Huffman DM, Ma X, Atzmon G, Einstein FH, et al. Visceral adipose tissue modulates mammalian longevity. Aging Cell. 2008;7(3):438–40.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  80. Barzilai N, Banerjee S, Hawkins M, Chen W, Rossetti L. Caloric restriction reverses hepatic insulin resistance in aging rats by decreasing visceral fat. J Clin Invest. 1998;101(7):1353–61.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  81. Gabriely I, Ma XH, Yang XM, Atzmon G, Rajala MW, Berg AH, et al. Removal of visceral fat prevents insulin resistance and glucose intolerance of aging: an adipokine-mediated process? Diabetes. 2002;51(10):2951–8.

    Article  CAS  PubMed  Google Scholar 

  82. Smith JV, Heilbronn LK, Ravussin E. Energy restriction and aging. Curr Opin Clin Nutr Metab Care. 2004;7(6):615–22.

    Article  PubMed  Google Scholar 

  83. Redman LM, Martin CK, Williamson DA, Ravussin E. Effect of caloric restriction in non-obese humans on physiological, psychological and behavioral outcomes. Physiol Behav. 2008;94(5):643–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  84. Pedersen BK, Steensberg A, Fischer C, Keller C, Keller P, Plomgaard P, et al. Searching for the exercise factor: is IL-6 a candidate? J Muscle Res Cell Motil. 2003;24(2–3):113–9.

    Article  CAS  PubMed  Google Scholar 

  85. Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol. 2012;8(8):457–65.

    Article  CAS  PubMed  Google Scholar 

  86. Febbraio MA, Pedersen BK. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J. 2002;16(11):1335–47.

    Article  CAS  PubMed  Google Scholar 

  87. Steensberg A. The role of IL-6 in exercise-induced immune changes and metabolism. Exerc Immunol Rev. 2003;9:40–7.

    PubMed  Google Scholar 

  88. Wolsk E, Mygind H, Grondahl TS, Pedersen BK, van Hall G. IL-6 selectively stimulates fat metabolism in human skeletal muscle. Am J Physiol Endocrinol Metab. 2010;299(5):E832–840.

    Article  CAS  PubMed  Google Scholar 

  89. Mathur N, Pedersen BK. Exercise as a mean to control low-grade systemic inflammation. Mediat Inflamm. 2008;2008:109502.

    Google Scholar 

  90. Fearon Kenneth CH, Glass David J, Guttridge DC. Cancer cachexia: mediators, signaling, and metabolic pathways. Cell Metab. 2012;16(2):153–66.

    Article  CAS  PubMed  Google Scholar 

  91. Martignoni ME, Kunze P, Hildebrandt W, Kunzli B, Berberat P, Giese T, et al. Role of mononuclear cells and inflammatory cytokines in pancreatic cancer-related cachexia. Clin Cancer Res. 2005;11(16):5802–8.

    Article  CAS  PubMed  Google Scholar 

  92. Hoesel B, Schmid JA. The complexity of NF-kappaB signaling in inflammation and cancer. Mol Cancer. 2013;12:86.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  93. Grossberg AJ, Scarlett JM, Marks DL. Hypothalamic mechanisms in cachexia. Physiol Behav. 2010;100(5):478–89.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  94. Ward Patrick S, Thompson CB. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell. 2012;21(3):297–308.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  95. Bayliss TJ, Smith JT, Schuster M, Dragnev KH, Rigas JR. A humanized anti-IL-6 antibody (ALD518) in non-small cell lung cancer. Expert Opin Biol Ther. 2011;11(12):1663–8.

    Article  CAS  PubMed  Google Scholar 

  96. Jatoi A, Ritter HL, Dueck A, Nguyen PL, Nikcevich DA, Luyun RF, et al. A placebo-controlled, double-blind trial of infliximab for cancer-associated weight loss in elderly and/or poor performance non-small cell lung cancer patients (N01C9). Lung Cancer. 2010;68(2):234–9.

    Article  PubMed  Google Scholar 

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The authors have no conflict of interest in the publication of this study.

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This study is supported by NIH funds (DK085495 and DK068036) to Ye J.

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  1. Collaborative Innovation Center of Molecular Diagnosis and Laboratory Medicine in Henan Province, School of Laboratory Medicine, Xinxiang Medical University, Xinxiang, 453003, People’s Republic of China

    Hui Wang

  2. Antioxidant and Gene Regulation Laboratory, Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, LA, USA

    Jianping Ye

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Wang, H., Ye, J. Regulation of energy balance by inflammation: Common theme in physiology and pathology. Rev Endocr Metab Disord 16, 47–54 (2015). https://doi.org/10.1007/s11154-014-9306-8

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