Effect of exercise intensity on cerebrospinal fluid interleukin-6 concentration during recovery from exhaustive exercise in rats

Acta Physiologica Hungarica

Volumn 101, Issue 1, 2014, Pages 21-31

  Kilic M ^a   Ulusoy, O ^a   Cirrik, S ^a   Hindistan, I ^a   Ozkaya Y ^a  

^a AKDENIZ UNIVERSITY   (Turkey)

Author keywords

cerebrospinal fluid; cytokines; exhaustion; glycogen supercompensation; interleukin 6; strenuous training; swimming

Indexed keywords

CITRATE SYNTHASE; INTERLEUKIN 6;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CEREBROSPINAL FLUID; CONTROLLED STUDY; DECAPITATION; ENZYME ACTIVITY; EXERCISE INTENSITY; EXHAUSTION; MALE; NONHUMAN; RAT; SOLEUS MUSCLE; SWIMMING; WEIGHT GAIN; WEIGHT REDUCTION;

CEREBROSPINAL FLUID; CYTOKINES; EXHAUSTION; GLYCOGEN SUPERCOMPENSATION; INTERLEUKIN-6; STRENUOUS TRAINING; SWIMMING;

ANIMALS; BODY WEIGHT; CITRATE (SI)-SYNTHASE; INTERLEUKIN-6; MALE; MUSCLE FATIGUE; MUSCLE, SKELETAL; PHYSICAL EXERTION; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; SEDENTARY LIFESTYLE; SWIMMING; TIME FACTORS;

EID: 84896374432     PISSN: 0231424X     EISSN: 15882683     Source Type: Journal    
DOI: 10.1556/APhysiol.100.2013.019     Document Type: Article

References (54)

1. Banks WA, Kastin AJ, Broadwell RD: Passage of cytokines across the blood-brain barrier. Neuroimmunomodulat. 2, 241-248 (1995)
2. Bastard JP, Jardel C, Bruckert E, Blondy P, Capeau J, Laville M, Vidal H, Hainque B: Elevated levels of interleukin-6 are reduced in serum and subcutaneous adipose tissue of obese women after weight loss. J. Clin. Endocrinol. Metab. 85, 3338-3342 (2000)
3. Benveniste EN: Cytokine actions in the central nervous system. Cytokine Growth Factor Rev. 9, 259-275 (1998)
4. 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. (Lond). 499 ( Pt 3), 833-841 (1997)
5. 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: Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes 55, 2688-2697 (2006)
6. Dalsgaard M, Ott P, Dela F, Juul A, Pedersen B, Warberg J, Fahrenkrug J, Secher N: The CSF and arterial to internal jugular venous hormonal differences during exercise in humans. Exp. Physiol. 89, 271-277 (2004)
7. Dawson CA, Horvath SM: Swimming in small laboratory animals. Med. Sci. Sports 78, 251-278 (1970)
8. Divertie GD, Jensen MD, Cryer PE, Miles JM: Lipolytic responsiveness to epinephrine in nondiabetic and diabetic humans. Am. J. Physiol. Endocrinol. Metab. 272, E1130-E1135 (1997)
9. Febbraio MA, Pedersen BK: Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J. 16, 1335-1347 (2002)
10. Fischer CP, Hiscock NJ, Penkowa M, Basu S, Vessby B, Kallner A, Sjoberg LB, Pedersen BK: Supplementation with vitamins C and E inhibits the release of interleukin-6 from contracting human skeletal muscle. J. Physiol. 558, 633-645 (2004)
11. Fischer CP: Interleukin-6 in acute exercise and training: what is the biological relevance Exerc. Immunol. Rev. 12, 6-33 (2006)
12. Fischer CP, Berntsen A, Perstrup LB, Eskildsen P, Pedersen BK: Plasma levels of IL-6 and CRP are associated with physical inactivity independent of obesity. Scand. J. Med. Sci. Sport. 17, 580-587 (2007)
13. Fisman EZ, Tenenbaum A: The ubiquitous interleukin-6: a time for reappraisal. Cardiovasc. Diabetol. 9, 62 (2010)
14. 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 55, 2554-2561 (2006)
15. Garthwaite SM, Cheng H, Bryan JE, Craig BW, Holloszy JO: Ageing, exercise and food restriction: effects on body composition. Mech. Ageing Dev. 36, 187-196 (1986)
16. Goforth HW, Jr Laurent D, Prusaczyk WK, Schneider KE, Petersen KF, Shulman GI: Effects of depletion exercise and light training on muscle glycogen supercompensation in men. Am. J. Physiol. Endocrinol. Metab. 285, E1304-E1311 (2003)
17. Gonzalez-Hernandez JA, Bornstein SR, Ehrhart-Bornstein M, Spath-Schwalbe E, Jirikowski G, Scherbaum WA: Interleukin-6 messenger ribonucleic acid expression in human adrenal gland in vivo: new clue to a paracrine or autocrine regulation of adrenal function. J. Clin. Endocrinol. Metab. 79, 1492-1497 (1994)
18. Hanisch A, Dieterich KD, Dietzmann K, Ludecke K, Buchfelder M, Fahlbusch R, Lehnert H: Expression of members of the interleukin-6 family of cytokines and their receptors in human pituitary and pituitary adenomas. J. Clin. Endocrinol. Metab. 85, 4411 (2000)
19. Holst, HH, Hansen PA, Nolte LA, Chen MM, Holloszy JO: Glycogen supercompensation masks the effect of a training induced increase in GLUT-4 on muscle glucose transport. J. Appl. Physiol. 85, 133-138 (1998)
20. Jensen MD, Caruso M, Heiling V, Miles JM: Insulin regulation of lipolysis in nondiabetic and IDDM subjects. Diabetes 38, 1595-1601 (1989)
21. Juttler V, Tarabin M: Interleukin-6 (IL-6): a possible neuromodulator induced by neuronal activity. Neuroscientist 8, 268-275 (2002)
22. Keller C, Steensberg A, Pilegaard H, Osada T, Saltin B, Pedersen BK, Neufer PD: Transcriptional activation of the IL-6 gene in human contracting skeletal muscle: influence of muscle glycogen content. FASEB J. 15, 2748-2750 (2001)
23. Keller P, Keller C, Carey AL, Jauffred S, Fischer CP, Steensberg A, Pedersen BK: Interleukin-6 production by contracting human skeletal muscle: autocrine regulation by IL-6. Biochem. Biophys. Res. Commun. 310, 550-554 (2003)
24. Margeli A, Skenderi K, Tsironi M, Hantzi E, Matalas AL, Vrettou C, Kanavakis E, Chrousos G, Papassotiriou I: Dramatic elevations of interleukin-6 and acute phase reactants in athletes participating in the ultradistance foot race "spartathlon": severe systemic inflammation and lipid and lipoprotein changes in protracted exercise. J. Clin. Endocrinol. Metab. 90, 3914-3918 (2005)
25. Matsui T, Soya S, Okamoto M, Ichitani Y, Kawanaka K, Soya H: Brain glycogen decreases during prolonged exercise. J. Physiol. 1, 589 (Pt 13), 3383-3393 (2011)
26. Naitoh Y, Fukata J, Tominaga T, Nakai Y, Tamai S, Mori K, Imura H: Interleukin-6 stimulates the secretion of adrenocorticotropic hormone in conscious, freely-moving rats. Biochem. Biophys. Res. Commun. 155, 1459-1463 (1988)
27. Moore AW, Timmerman S, Brownlee KK, Rubin DA, Hackney AC: Strenuous, fatiguing exercise: relationship of cortisol to circulating thyroid hormones. Int. J. Endocriol. Metab. 3, 18-24 (2005)
28. Nieman DC, Nehlsen-Canarella SL, Fagoaga OR, Henson DA, Utter A, Davis JM, Williams F, Butterworth DE: Influence of mode and carbohydrate on the cytokine response to heavy exertion. Med. Sci. Sports Exerc. 30, 671-678 (1998)
29. Nybo L, Moller K, Pedersen BK, Nielsen B, Secher NH: Association between fatigue and failure to preserve cerebral energy turnover during prolonged exercise. Acta Physiol. Scand. 179, 67-74 (2003)
30. Nybo L, Nielsen B, Pedersen BK, Moller K, Secher NH: Interleukin-6 release from the human brain during prolonged exercise. J. Physiol. 542, 991-995 (2002)
31. Ogonovszky H, Berkes I, Kumagai S, Kaneko T, Tahara S, Goto S, Radák Z: The effects of moderate-, strenuous-and over-training on oxidative stress markers, DNA repair, and memory, in rat brain. Neurochem. Int. 46, 635-640 (2005)
32. Oscai LB, Spirakis CN, Wolff CA, Beck RJ: Effects of exercise and of food restriction on adipose tissue cellularity. J. Lipid Res. 13, 588-592 (1972)
33. Ostrowski K, Hermann C, Bangash A, Schjerling P, Nielsen JN, Pedersen BK: A trauma like elevation of plasma cytokines in humans in response to treadmill running. J. Physiol. 513 (Pt 3), 889-894 (1998)
34. Ostrowski K, Rohde T, Zacho M, Asp S, Pedersen BK: Evidence that interleukin-6 is produced in human skeletal muscle during prolonged running. J. Physiol. 508 ( Pt 3), 949-953 (1998)
35. Ozdemir O, Ozdem S, Ozkaya YG: Melatonin administration does not alter muscle glycogen concentration during recovery from exhaustive exercise in rats. Eur. J. Sport. Sci. 13, 174-182 (2013)
36. Papanicolaou DA, Petrides JS, Tsigos C, Bina S, Kalogeras KT, Wilder R, Gold PW, Deuster PA, Chrousos GP: Exercise stimulates interleukin-6 secretion: inhibition by glucocorticoids and correlation with catecholamines. Am. J. Physiol. Endocrinol. Metab. 271, E601-E605 (1996)
37. Pedersen BK, Febbraio MA: Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol. Rev. 88, 1379-1406 (2008)
38. Pedersen BK, Fischer CP: Beneficial health effects of exercise-the role of IL-6 as a myokine. Trends Pharmacol. Sci. 28, 152-156 (2007)
39. Pedersen BK: The anti-inflammatory effect of exercise: its role in diabetes and cardiovascular disease control. Essays Biochem. 42, 105-117 (2006)
40. Penkowa M, Keller C, Keller P, Jauffred S, Pedersen BK: Immunohistochemical detection of interleukin-6 in human skeletal muscle fibers following exercise. FASEB J. 17, 2166-2168 (2003)
41. Perlstein RS, Whitnall MH, Abrams JS, Mougey EH, Neta R: Synergistic roles of interleukin-6, interleukin-1, and tumor necrosis factor in the adrenocorticotropin response to bacterial lipopolysaccharide in vivo. Endocrinology 132, 946-952 (1993)
42. Rasmussen P, Vedel JC, Olesen J, Adser H, Pedersen MV, Hart E, Secher NH, Pilegaard H: In humans IL-6 is released from the brain during and after exercise and paralleled by enhanced IL-6 mRNA expression in the hippocampus of mice. Acta Physiol. (Oxf). 201, 475-482 (2011)
43. Ropelle ER, Fernandes MF, Flores MB, Ueno M, Rocco S: Central exercise action increases the AMPK and mTOR response to leptin. PLoS ONE. 3, e3856.doi: 10.1371/journal.pone.000385610.1371/journal.pone.0003856 (2008)
44. Sadagurski M, Norquay L, Farhang J, D'Aquino K, Copps K: Human IL6 enhances leptin action in mice. Diabetologia 53, 525-535 (2010)
45. Spangelo BL, Judd AM, MacLeod RM, Goodman DW, Isakson PC: Endotoxin-induced release of interleukin-6 from rat medial basal hypothalami. Endocrinol. 127, 1779-1785 (1990)
46. Srere PA: Citrate synthase, Methods Enzymol. 13, 3-5 (1969)
47. Steensberg A, Febbraio MA, Osada T, Schjerling P, van Hall G, Saltin B, Pedersen BK: Interleukin-6 production in contracting human skeletal muscle is influenced by pre-exercise muscle glycogen content. J. Physiol. 537, 633-639 (2001)
48. Steensberg A, Van Hall G, Osada T, Sacchetti M, Saltin B, Klarlund PB: Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J. Physiol. 529 Pt 1, 237-242 (2000)
49. Stenlof K, Wernstedt I, Fjallman 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. 88, 4379-4383 (2003)
50. Tabata I, Nishimura K, Kouzaki M, Hirai Y, Ogita F, Miyachi M, Yamamoto K: Effects of moderate-intensity endurance training and high-intensity intermittent training on anaerobic capacity and VO2 max. Med. Sci. Sports. Exerc. 28, 1327-1330 (1996)
51. Terada S, Yokozeki T, Kawanaka K, Ogawa K, Higuchi M, Ezaki O, Tabata I: Effects of high-intensity swimming training on GLUT-4 and glucose transport activity in rat skeletal muscle. J. Appl. Physiol. 90, 2019-2024 (2001)
52. Tsigos C, Papanicolaou DA, Defensor R, Mitsiadis CS, Kyrou I, Chrousos GP: Dose effects of recombinant human interleukin-6 on pituitary hormone secretion and energy expenditure. Neuroendocrinology 66, 54-62 (1997)
53. Van Hall G, Steensberg A, Sacchetti M, Fischer C, Keller C, Schjerling P, Hiscock N, Moller K, Saltin B, Febbraio MA, Pedersen BK: Interleukin-6 stimulates lipolysis and fat oxidation in humans. J. Clin. Endocrinol. Metab. 88, 3005-3010 (2003)
54. Wallenius V, Wallenius K, Ahren B, Rudling M, Carlsten H, Dickson SL, Ohlsson C, Jansson JO: Interleukin-6-deficient mice develop mature-onset obesity. Nat. Med. 8, 5-79 (2002)