Regulation of energy intake after physical exercise by interleukin-6;Interleuquina-6 en la regulación de la ingesta energética post-ejercicio físico

Revista Chilena de Nutricion

Volumn 40, Issue 2, 2013, Pages 174-180

  Santos M , José Luis ^a   Almada F , Carmen ^a   Smalley M , Susan V ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Energy expenditure; Energy intake; Interleukin 6; Physical activity

Indexed keywords

EID: 84884176601     PISSN: 07177518     EISSN: None     Source Type: Journal    
DOI: 10.4067/S0717-75182013000200013     Document Type: Review

References (83)

1. Frayn K. Metabolic Regulation: A Human Perspective. Blackwell Science, Oxford 2010.
2. Martins C, Morgan L, Truby H. A review of the effects of exercise on appetite regulation: obesity perspective. Internat J Obesity 2008; 32:1337-47.
3. Blundell JE. Perspective on the central control appetite. Obesity Res 2006; 14 (Supplement): 160S-3S.
4. Cook CM, Schoeller DA. Physical activity and weight control: conflicting findings. Clin Nutr Metab Care 2011; 14: 419-24.
5. King N. A, Burley V. J, Blundell J.E. Exercise-induced suppression of appetite: effects on food intake and implications for energy balance. Eur J Clin Nutr. 1994; 48: 715-24.
6. Petersen AMW, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol 2005a; 98: 1154-62.
7. Jonsdottir IH, Schjerling P, Ostrowski K, Asp S, Richter EA, Pedersen BK. Muscle contractions induce interleukin-6 mRNA production in rat skeletal muscles. J Physiol 2000; 528 Pt 1: 157-63.
8. Almada C, Cataldo LR, Smalley SV, Diaz E, Serrano A, Hodgson MI, Santos JL. Plasma levels of interleukin-6 and interleukin-18 after an acute physical exercise: relation with post-exercise energy intake in twins. J Physiol Biochem. 2012 Jul 19. [Epub ahead of print].
9. Thompson DA, Wolfe LA, Eikelboom R. Acute effects of exercise intensity on appetite in young men. Med Sci Sports Exerc. 1988; 20: 222-7.
10. Ostrowski K, Rohde T, Zacho M, Asp S, Pedersen BK. Evidence that inter-leukin-6 is produced in human skeletal muscle during prolonged running. J Physiol. 1998; 508 (Pt 3): 949-53.
11. Ostrowski, K., Rohde, T., Asp, S., Schjerling, P., Pedersen B. K. Chemokines are elevated in plasma after strenuous exercise. Eur J Cell Physiol. 2001; 84: 244-5.
12. Pedersen, B. K., Bruunsgaard, H., Klokker, M., Kappel, M., MacLean, D. A., Nielsen, H. B., Rohde, T., Ullum, H., Zacho, M. Exercise-induced immunomodulation-possible roles of neuroendocrine factors and metabolic factors. Int J Sports Med. 1997; 18:S2-S7.
13. Steensberg A, Fischer CP, Keller C, Moller K, Pedersen BK. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab. 2003; 285: E433-E7.
14. Keller C, Steensberg A, Hansen AK, Fischer CP, Plomgaard P, Pedersen BK. Effect of exercise, training, and glycogen availability on IL-6 receptor expression in human skeletal muscle. J Appl Physiol. 2005; 99: 2075-9.
15. Hoene M, Weigert C. The role of interleukin-6 in insulin resistance, body fat distribution and energy balance. Obes Rev. 2008; 9: 20-9.
16. Kishimoto T. The biology of interleukin-6. Blood 1989; 74: 1-10.
17. Pedersen BK, Steensberg A, Schjerling P. Muscle-derived interleukin-6: possible biological effects. J Physiol. 2001; 536: 329-37.
18. Bruunsgaard H, Galbo H, Halkjaer-Kristensen J, Johansen TL, MacLean DA, Pedersen BK. Exercise-induced increase in serum interleukin-6 in humans is related to muscle damage. J Physiol. 1997; (Lond) 499 (Pt 3): 833-41.
19. Friedland JS, Suputtamongkol Y, Remick DG, Chaowagul W, Strieter RM, Kunkel SL, White NJ, Griffin GE. Prolonged elevation of interleukin-8 and interleukin-6 concentrations in plasma and of leukocyte interleukin-8 mRNA levels during septicemic and localized Pseudomonas pseudomallei infection. Infect Immun. 1992; 60: 2402-8.
20. Hirano T, Yasukawa K, Harada H, Taga T, Watanabe Y, Matsuda T, Kashiwamura S, Nakajima K, Koyama K, Iwamatsu A, et al. Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 1986; 324(6092):73-6.
21. Kishimoto T, Akira S, Narazaki M, Taga T. Interleukin-6 family of cytokines and gp130. Blood 1995; 86: 1243-54.
22. Rose-John S. Interleukin-6 biology is coordinated by membrane bound and soluble receptors. Acta Biochim Pol. 2003; 50: 603-11.
23. Robson-Ansley PJ, de Milander L, Collins M, Noakes TD. Acute interleukin-6 administration impairs athletic performance in healthy, trained male runners. Can J Appl Physiol. 2004.; 29: 411-8.
24. Gaillard J, Pugniere M, Tresca J, Mani J, Klein B, Brochier J. Interleukin-6 receptor signaling. II. Bio-availability of in terleukin-6 in serum. Eur Cytokine Netw 1999; 10: 337-4.
25. Jostock T, Mullberg J, Ozbek S, Atreya R, Blinn G, Voltz N, Fischer M, Neurath MF, Rose-John S. Soluble gp130 is the natural inhibitor of soluble interleukin-6 receptor transsignaling responses. Eur J Biochem. 2001; 268: 160-7.
26. Broberger C. Brain regulation of food intake and appetite: molecules and networks. J Intern Med. 2005; 258: 301-27.
27. Jakicic JM, Otto AM. Physical activity considerations for the treatment and prevention of obesity. Am J Clin Nutr. 2005; 82: S226-9.
28. Long SJ, Hart K, Morgan M. The ability of habitual exercise to influence appetite and food intake in response to high-and low-energy pre-loads in man. Br J Nutr. 2002; 87: 517-23.
29. Donnelly JE, Smith B, Jacobsen DJ, Kirk E, Dubose K, Hyder M, Bailey B, Washburn R The role of exercise for weight loss and maintenance. Best Pract Res Clin Gastroenterol. 2004; 18: 1009-29.
30. Melzer K, Kayser B, Saris WHM, Pichard C. Effects of physical activity on food intake. Clin Nutr. 2005; 8: 2-11.
31. Wynne K, Stanley S, McGowan B, Bloom S. Appetite control. J Endocrinol 2005; 184: 291-318.
32. Puyau MR, Adolph FA, Zakeri NF Butte. Prediction of activity energy expenditure using accelerometers in children. Med Sci Sport Exerc. 2004; 36: 1625-31.
33. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 2000; 404: 661-71.
34. Martins C, Morgan LM, Bloom S, Robertson MD. Effects of exercise on gut peptides, energy intake and appetite. J Endocrinol. 2007; 193: 251-8.
35. Pedersen BK, Fisher CP. Physiological role of muscle-derived interleukin-6 in response to exercise. Clin Nutr Metab Care. 2007;10: 265-71.
36. Blundell JE. The biology of appetite. Clin Applied Nutr 1991; 21-31.
37. Sullivan SN, Champion MD, Christofides ND, Adrian TE & Bloom SR. Gastrointestinal regulatory peptide responses in long-distance runners. Physician Sportsmed 1984; 12 77-82.
38. Blundell JE, King NA. Physical activity and regulation of food intake: current evidence. Med Sci Sports Exerc. 1999; 31 (11suppl): 573-83.
39. Atkinson TJ. Central and peripheral neuroendocrine peptides and signalling in appetite regulation: considerations for obesity pharmacotherapy. Obesity Rev. 2008; 9: 108-120.
40. Cintra DE, Ropelle ER, Pauli JR. Regulación central de la ingestión alimentaria y el gasto energético: acciones moleculares de la insulina, la leptina y el ejercicio físico. Rev Neurol. 2007; 45: 672-82.
41. Young SN. How to increase serotonin in the human brain without drugs. Psychiatry Neurosci 2007; 32: 394-9.
42. Melancon MO, Lorrain D, Dionne IJ. Exercise increases tryptophan availability to the brain in older men age 57-70 years. Med Sci Sports Exerc. 2012: 44(5):881-7.
43. Jacobs BL, Fornal CA. Activity of serotonergic neurons in behaving animals. Neuropsychopharmacol 1999; 21: 9S-15S.
44. Leibowitz SF, Alexander JT. Hypothalamic serotonin in control of eating behavior, meal size, and body weight. Biol Psych. 1998; 44: 851-64.
45. Yadav VK, Oury F, Suda N, Liu ZW, Gao XB, Confavreux C, Klemenhagen KC, Tanaka KF, Gingrich JA, Guo XE, Tecott LH, Mann JJ, Hen R, Horvath TL, Karsenty G. A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell. 2009; 138(5):976-89.
46. Perboni S, Inui A. Anorexia in cancer: role of feeding-regulatory peptides. Phil Trans R Soc B. 2006; 361: 1281-89.
47. Coll AP, Farooqi S, O'Rahilli S. The hormonal control of food intake. Cell 2007; 129: 251-62.
48. Wallenius K, Wallenius V, Sunter D, Dickson SL, Jansson JO. Intracerebroventricular interleukin-6 treatment decreases body fat in rats. Biochem Biophys Res Commun. 2002a; 293: 560-5.
49. Wallenius V, Wallenius K, Ahrén B, Rudling M, Carlsten H, Dickson SL, Ohlsson C, Jansson JO. Interleukin-6-deficient mice develop mature-onset obesity. Nat Med. 2002b; 8:75-9.
50. Chida D, Osaka T, Hashimoto O, Iwakura Y. Combined interleukin-6 and interleukin-1 deficiency causes obesity in young mice. Diabetes 2006; 55: 971-7.
51. Stenlöf K, Wernstedt I, Fjällman T, Wallenius V, Wallenius K, Jansson JO. Interleukin-6 levels in the central nervous system are negatively correlated with fat mass in overweight/obese subjects. J Clin Endocrinol Metab. 2003; 88: 4379-83.
52. Gadient RA, Otten AU. Interleukin-6 and Interleukin-6 Receptor mRNA Expression in Rat Central Nervous System. Ann New York Acad Sci. 1995; 762: 403-6.
53. Rothwell NJ, Busbridge NJ, Lefeuvre RA, Hardwick AJ, Gauldie J, Hopkins SJ. Interleukin-6 is centrally acting endogenous pyrogen in the rat. Can J Physiol Pharmacol. 1991; 69:1465-9.
54. Dishman RK. Brain monoamines, exercise, and behavioral stress: animal models. Med Sci Sports Exerc. 1997; 29: 63-74.
55. Trayhurn P, Drevon CA, Eckel J. Secreted proteins from adipose tissue and skeletal muscle-adipokines, myokines and adipose/muscle cross-talk. Arch Physiol Biochem. 2011; 117(2): 47-56.
56. Bi S, Scott KA, Hyun J, Ladenheim EE, Moran TH. Running wheel activity prevents hyperphagia and obesity in Otsuka long-evans Tokushima fatty rats: role of hypothalamic signaling. Endocrinology 2005; 146: 1646-85.
57. Nybo L, Nielsen B, Pedersen BK, Møller K, Secher NH. Interleukin-6 release from the human brain during prolongued exercise. J Physiol. 2002; 542: 991-5.
58. Febbraio MAl Pedersen BK. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J 2002; 16: 1335-47.
59. Santos JL, Martínez JA, Pérez F, Albala C. Genetic epidemiology of obesity:family studies. Rev Med Chil. 2005; 133(3):349-61.
60. Lage R, Dieguez C, Vidal-Puig A, López M. AMPK: a metabolic gauge regulation whole-body energy homeostasis. Cell 2008; 14: 539-49.
61. Holmes BF, Kurth-Kraczek EJ, Winder WW. Chronic activation of 5 AMP-activated protein kinase increases GLUT-4, hexokinase, angd glycogen in muscle. J Appl Physiol. 1999; 87: 1990-5.
62. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Müller C, Carling D, Kahn BB. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature. 2002; 415: 339-43.
63. Minokoshi Y, Alquier T, Furukawa N, Kim YB, Lee A, Xue B, Mu J, Foufelle F, Ferré P, Birnbaum MJ, Stuck BJ, Kahn BB. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature. 2004; 428: 569-74.
64. López M, Lelliott CJ, Tovar S, Kimber W, Gallego R, Virtue S, Blount M, Vázquez MJ, Finer N, Powles TJ, O'Rahilly S, Saha AK, Diéguez C, Vidal-Puig AJ. Tamoxifen-induced anorexia is associated with fatty acid synthase inhibition in the ventromedial nucleus of the hypothalamus and accumulation of malonyl-CoA. Diabetes 2006; 55:1327-36.
65. Hu Z, Cha SH, van Haasteren G, Wang J, Lane MD. Effect of centrally administered C75, a fatty acid synthase inhibitor, on ghrelin secretion and its downstream effects. Proc Natl Acad Sci USA 2005;102: 3972-7.
66. Laviano A, Meguid MM, Inui A, Rossi-Fanelli F. Role of leucine in regulating food intake. Science 2006; 313: 1236-7.
67. Cota D, Proulx K, Smith KA, Kozma SC, Thomas G, Woods SC, Seeley RJ. Hypothalamic mTOR signaling regulates food intake. Science 2006; 12: 927-30.
68. Flores MB, Fernandes MF, Ropelle ER, Faria MC, Ueno M, Velloso LA, Saad MJ, Carvalheira JB. Exercise improves insulin and leptin sensitivity in hypothalamus of Wistar rats. Diabetes 2006; 55: 2554-61.
69. Ropelle ER, Fernandes MF, Flores MB, Ueno M, Rocco S, Marin R, Intra DE, Velloso LA, Franchini KG, Saad MJ, Carvalheira JB. Central Exercise Action Increases the AMPK and mTOR Response to Leptin. PLoS ONE 2008; 3(12): e3856.
70. Ropelle ER, Flores MB, Cintra DE, Rocha GZ, Pauli JR, Morari J, de Souza CT, Moraes JC, Prada PO, Guadagnini D, Marin RM, Oliveira AG, Augusto TM, Carvalho HF, Velloso LA, Saad MJ, Carvalheira JB. IL-6 and il-10 anti-inflammatory activity links exercise to hypothalamic insulin and leptin sensitivity through IKKb and ER stress inhibition. Plos Biol. 2010; 8(8): e100046.
71. Martínez de Morentin PB, López M. "Mens sana in corpore sano": exercise and hypothalamic ER stress. PLoS Biol. 2010; 8(8).
72. Steensberg A, Febbraio MA, Osada T, Schjerling P, van Hall G, Saltin B, Pedersen BK. Il-6 production in contracting human skeletal muscle is influenced by preexercise muscle glycogen content. J Physiol. 2001; 537: 633-9.
73. Febbraio MA, Hiscock N, Sacchetti M, Fischer CP, Pedersen BK. Interleukin-6 is a novel factor mediating glucose homeostasis during skeletal muscle contraction. Diabetes 2004;. 53: 1643-8.
74. Ostrowski, K., Rohde, T, Zacho, M, Asp, S, Pedersen, B. K. Evidence that IL-6 is produced in skeletal muscle during intense long-term muscle activity. J Physiol London. 1998; 508: 949-53.
75. Nehlsen-Canarella, S. L., Fagoaga, O.R., Nieman, D.C. Carbohydrate and the cytokine response to 2.5 hours of running. J Cell Physiol. 1997; 82:1662-7.
76. Keller P, Penkowa M, Keller C, Steensberg A, Fischer CP, Giralt M, Hidalgo J, Pedersen BK. Interleukin-6 receptor expression in contracting human skeletal muscle: regulating role of IL-6. FASEB J. 2005; 19:1181-3.
77. Carey AL, Steinberg GR, Macaulay SL, Thomas WG, Holmes AG, Ramm G, Prelovsek O, Hohnen-Behrens C, Watt MJ, James DE, Kemp BE, Pedersen BK, Febbraio MA. IL-6 increases insulin stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMPK. Diabetes. 2006; 55: 2688-97.
78. Ellingsgaard H, Hauselmann I, Schuler B, Habib AM, Baggio LL, Meier DT, Eppler E, Bouzakri K, Wueest S, Muller YD, Hansen AM, Reinecke M, Konrad D, Gassmann M, Reimann F, Halban PA, Gromada J, Drucker DJ, Gribble FM, Ehses JA, Donath MY. Interleukin-6 enhances insulin secretion by increasing glucagon-like peptide-1 secretion from L cells and alpha cells. Nat Med. 2011; 17: 1481-9.
79. Handschin C, Choi CS, Chin S, Kim S, Kawamori D, Kurpad AJ, Neubauer N, Hu J, Mootha VK, Kim YB, Kulkarni RN, Shulman GI, Spiegelman BM. Abnormal glucose homeostasis in skeletal muscle-specific PGC-1alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk. J Clin Invest. 2007; 117(11):3463-74.
80. Calegari VC, Zoppi CC, Rezende LF, Silveira LR, Carneiro EM, Boschero AC. Endurance training activates AMP-activated protein kinase, increases expression of uncoupling protein 2 and reduces insulin secretion from rat pancreatic islets. J Endocrinol. 2011; 208(3):257-64.
81. Moreno-Aliaga MJ, Pérez-Echarri N, Marcos-Gómez B, Larequi E, Gil-Bea FJ, Viollet B, Gimenez I, Martínez JA, Prieto J, Bustos M. Cardiotrophin-1 is a key regulator of glucose and Lipid Metabolism. Cell Metab. 2011; 14: 242-53.
82. Iñiguez M, Berasain C, Martinez-Ansó E, Bustos M, Fortes P, Pennica D, Avila MA, Prieto J. Cardiotrophin-1 defends the liver against ischemia-reperfusion injury and mediates the protective effect of ischemic preconditioning. J Exp Med. 2006, 203 (13): 2809-15.
83. Marquéz JM, Belza I, Holtmann B, Pennica D et al. Cardiotrophin-1 Is an Essential Factor in the Natural Defense of the Liver Against Apoptosis. Hepatology 2007;45: 639-48.