Hyperthermia, dehydration, and osmotic stress: Unconventional sources of exercise-induced reactive oxygen species

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 310, Issue 2, 2016, Pages R105-R114

  King, Michelle A ^a   Clanton, Thomas L ^a   Laitano, Orlando ^a,b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSIDADE FEDERAL DO VALE DO SÃO FRANCISCO   (Brazil)

Author keywords

Heat stress; Lipoxygenase; Oxidative stress; Skeletal muscle; Taurine

Indexed keywords

CATALASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HEAT SHOCK PROTEIN 72; HEME OXYGENASE 1; ISOPROSTANE DERIVATIVE; OXIDIZING AGENT; PROSTAGLANDIN SYNTHASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; WATER; ANTIOXIDANT;

ANTIOXIDANT ACTIVITY; DEHYDRATION; EXERCISE; HEMOCONCENTRATION; HUMAN; HYPERTHERMIA; LIPID PEROXIDATION; MUSCLE CELL; OSMOREGULATION; OSMOTIC STRESS; PRIORITY JOURNAL; REVIEW; SARCOLEMMA; SHEAR STRESS; ADAPTATION; ANIMAL; BLOOD VOLUME; ELECTROLYTE BALANCE; FEVER; METABOLISM; MUSCLE CONTRACTION; OSMOTIC PRESSURE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; SKELETAL MUSCLE; THERMOREGULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIOXIDANTS; BLOOD VOLUME; BODY TEMPERATURE REGULATION; DEHYDRATION; EXERCISE; FEVER; HUMANS; MUSCLE CONTRACTION; MUSCLE, SKELETAL; OSMOREGULATION; OSMOTIC PRESSURE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; WATER-ELECTROLYTE BALANCE;

EID: 84952664192     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00395.2015     Document Type: Review

References (94)

1. Ahmadizad S, El-Sayed MS, MacLaren DP. Effects of water intake on the responses of haemorheological variables to resistance exercise. Clin Hemorheol Microcirc 35: 317–327, 2006.
2. Ahmadizad S, Moradi A, Nikookheslat S, Ebrahimi H, Rahbaran A, Connes P. Effects of age on hemorheological responses to acute endurance exercise. Clin Hemorheol Microcirc 49: 165–174, 2011.
3. Ajmani RS, Fleg JL, Demehin AA, Wright JG, O’Connor F, Heim JM, Tarien E, Rifkind JM. Oxidative stress and hemorheological changes induced by acute treadmill exercise. Clin Hemorheol Microcirc 28: 29–40, 2003.
4. Anderson EJ, Neufer PD. Type II skeletal myofibers possess unique properties that potentiate mitochondrial H2O2 generation. Am J Physiol Cell Physiol 290: C844–C851, 2006.
5. Bennekou P, de Franceschi L, Pedersen O, Lian L, Asakura T, Evans G, Brugnara C, Christophersen P. Treatment with NS3623, a novel Cl-conductance blocker, ameliorates erythrocyte dehydration in transgenic SAD mice: a possible new therapeutic approach for sickle cell disease. Blood 97: 1451–1457, 2001.
6. Blomstrand E, Saltin B. Effect of muscle glycogen on glucose, lactate and amino acid metabolism during exercise and recovery in human subjects. J Physiol 514: 293–302, 1999.
7. Boehning F, Mejia T, Schmitz-Rode T, Steinseifer U. Hemolysis in a laminar flow-through Couette shearing device: an experimental study. Artif Organs 38: 761–765, 2014.
8. Brooks GA, Hittelman KJ, Faulkner JA, Beyer RE. Temperature, skeletal muscle mitochondrial functions, and oxygen debt. Am J Physiol 220: 1053–1059, 1971.
9. Brun JF, Khaled S, Raynaud E, Bouix D, Micallef JP, Orsetti A. The triphasic effects of exercise on blood rheology: which relevance to physiology and pathophysiology? Clin Hemorheol Microcirc 19: 89–104, 1998.
10. Brun JF, Micallef JP, Orsetti A. Hemorheologic effects of light prolonged exercise. Clin Hemorheol 14: 807–818, 1994.
11. Brun JF, Micallef JP, Supparo I, Orsetti A. Effects of a standardized breakfast compared to fasting on the hemorheologic responses to submaximal exercise. Clin Hemorheol 15: 213–220, 1995.
12. Calderwood SK, Bornstein B, Farnum EK, Stevenson MA. Heat shock stimulates the release of arachidonic acid and the synthesis of prostaglandins and leukotriene B4 in mammalian cells. J Cell Physiol 141: 325–333, 1989.
13. Cho KJ, Seo JM, Kim JH. Bioactive lipoxygenase metabolites stimulation of NADPH oxidases and reactive oxygen species. Mol Cells 32: 1–5, 2011.
14. Connes P, Simmonds MJ, Brun JF, Baskurt OK. Exercise hemorheology: classical data, recent findings and unresolved issues. Clin Hemorheol Microcirc 53: 187–199, 2013.
15. Cotgreave IA, Goldschmidt L, Tonkonogi M, Svensson M. Differentiation-specific alterations to glutathione synthesis in and hormonally stimulated release from human skeletal muscle cells. FASEB J 16: 435–437, 2002.
16. Davies KJ, Quintanilha AT, Brooks GA, Packer L. Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107: 1198–1205, 1982.
17. Di Meo S, Venditti P. Mitochondria in exercise-induced oxidative stress. Biol Signals Recept 10: 125–140, 2001.
18. Dillard CJ, Litov RE, Savin WM, Dumelin EE, Tappel AL. Effects of exercise, vitamin E, and ozone on pulmonary function and lipid peroxidation. J Appl Physiol 45: 927–932, 1978.
19. Durand MJ, Dharmashankar K, Bian JT, Das E, Vidovich M, Gutterman DD, Phillips SA. Acute exertion elicits a H2O2-dependent vasodilator mechanism in the microvasculature of exercise-trained but not sedentary adults. Hypertension 65: 140–145, 2015.
20. El-Sayed MS. Effects of exercise and training on blood rheology. Sports Med 26: 281–292, 1998.
21. El-Sayed MS, Ali N, El-Sayed Ali Z. Haemorheology in exercise and training. Sports Med 35: 649–670, 2005.
22. Ernst E, Daburger L, Saradeth T. The kinetics of blood rheology during and after prolonged standardized exercise. Clin Hemorheol 11: 429–439, 1991.
23. Gailly P. TRP channels in normal and dystrophic skeletal muscle. Curr Opin Pharmacol 12: 326–334, 2012.
24. Gervais P, Martínez de Marañón I, Evrard C, Ferret E, Moundanga S. Cell volume changes during rapid temperature shifts. J Biotechnol 102: 269–279, 2003.
25. Gil SM, Yazaki E, Evans DF. Aetiology of running-related gastrointestinal dysfunction. How far is the finishing line? Sports Med 26: 365–378, 1998.
26. Golub AS, Pittman RN. Bang-bang model for regulation of local blood flow. Microcirculation 20: 455–483, 2013.
27. Gong MC, Arbogast S, Guo Z, Mathenia J, Su W, Reid MB. Calciumindependent phospholipase A2 modulates cytosolic oxidant activity and contractile function in murine skeletal muscle cells. J Appl Physiol (1985) 100: 399–405, 2006.
28. Gonzalez-Alonso J, Crandall CG, Johnson JM. The cardiovascular challenge of exercising in the heat. J Physiol 586: 45–53, 2008.
29. Hall DM, Buettner GR, Matthes RD, Gisolfi CV. Hyperthermia stimulatesnitricoxideformation:electronparamagneticresonancedetectionof NO-heme in blood. J Appl Physiol (1985) 77: 548–553, 1994.
30. Hall DM, Buettner GR, Oberley LW, Xu L, Matthes RD, Gisolfi CV. Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am J Physiol Heart Circ Physiol 280: H509–H521, 2001.
31. Hass MA, Massaro D. Regulation of the synthesis of superoxide dismutases in rat lungs during oxidant and hyperthermic stresses. J Biol Chem 263: 776–781, 1988.
32. Herman TS, Gerner EW, Magun BE, Stickney D, Sweets CC, White DM. Rate of heating as a determinant of hyperthermic cytotoxicity. Cancer Res 41: 3519–3523, 1981.
33. Herrero A, Barja G. ADP-regulation of mitochondrial free radical production is different with complex I- or complex II-linked substrates: implications for the exercise paradox and brain hypermetabolism. J Bioenerg Biomembr 29: 241–249, 1997.
34. Hillman AR, Turner MC, Peart DJ, Bray JW, Taylor L, McNaughton LR, Siegler JC. A comparison of hyperhydration versus ad libitum fluid intake strategies on measures of oxidative stress, thermoregulation, and performance. Res Sports Med 21: 305–317, 2013.
35. Hillman AR, Vince RV, Taylor L, McNaughton L, Mitchell N, Siegler J. Exercise-induced dehydration with and without environmental heat stress results in increased oxidative stress. Appl Physiol Nutr Metab 36: 698–706, 2011.
36. Hilton JK, Rath P, Helsell CV, Beckstein O, Van Horn WD. Understanding thermosensitive transient receptor potential channels as versatile polymodal cellular sensors. Biochemistry 54: 2401–2413, 2015.
37. Hoffmann EK, Lambert IH, Pedersen SF. Physiology of cell volume regulation in vertebrates. Physiol Rev 89: 193–277, 2009.
38. Jackson MJ, Edwards RH, Symons MC. Electron spin resonance studies of intact mammalian skeletal muscle. Biochim Biophys Acta 847: 185–190, 1985.
39. Jones AM, Wilkerson DP, Berger NJ, Fulford J. Influence of endurance training on muscle [PCr] kinetics during high-intensity exercise. Am J Physiol Regul Integr Comp Physiol 293: R392–R401, 2007.
40. Kadenbach B, Ramzan R, Wen L, Vogt S. New extension of the Mitchell Theory for oxidative phosphorylation in mitochondria of living organisms. Biochim Biophys Acta 1800: 205–212, 2010.
41. Kikusato M, Toyomizu M. Crucial role of membrane potential in heat stress-induced overproduction of reactive oxygen species in avian skeletal muscle mitochondria. PLoS One 8: e64412, 2013.
42. Laitano O, Kalsi KK, Pearson J, Lotlikar M, Reischak-Oliveira A, Gonzalez-Alonso J. Effects of graded exercise-induced dehydration and rehydration on circulatory markers of oxidative stress across the resting and exercising human leg. Eur J Appl Physiol 112: 1937–1944, 2012.
43. Laitano O, Kalsi KK, Pook M, Oliveira AR, Gonzalez-Alonso J. Separate and combined effects of heat stress and exercise on circulatory markers of oxidative stress in euhydrated humans. Eur J Appl Physiol 110: 953–960, 2010.
44. Lehoux S. Redox signalling in vascular responses to shear and stretch. Cardiovasc Res 71: 269–279, 2006.
45. Letcher RL, Pickering TG, Chien S, Laragh JH. Effects of exercise on plasma viscosity in athletes and sedentary normal subjects. Clin Cardiol 4: 172–179, 1981.
46. Leverett LB, Hellums JD, Alfrey CP, Lynch EC. Redbloodcelldamage by shear stress. Biophys J 12: 257–273, 1972.
47. Loven DP, Leeper DB, Oberley LW. Superoxide dismutase levels in Chinese hamster ovary cells and ovarian carcinoma cells after hyperthermia or exposure to cycloheximide. Cancer Res 45: 3029–3033, 1985.
48. Martin DG, Ferguson EW, Wigutoff S, Gawne T, Schoomaker EB. Blood viscosity responses to maximal exercise in endurance-trained and sedentary female subjects. J Appl Physiol (1985) 59: 348–353, 1985.
49. Martins AS, Shkryl VM, Nowycky MC, Shirokova N. Reactive oxygen species contribute to Ca2 signals produced by osmotic stress in mouse skeletal muscle fibres. J Physiol 586: 197–210, 2008.
50. Maughan RJ, Shirreffs SM, Leiper JB. Errors in the estimation of hydration status from changes in body mass. J Sports Sci 25: 797–804, 2007.
51. McAnulty SR, McAnulty L, Pascoe DD, Gropper SS, Keith RE, Morrow JD, Gladden LB. Hyperthermia increases exercise-induced oxidative stress. Int J Sports Med 26: 188–192, 2005.
52. Mestre-Alfaro A, Ferrer MD, Banquells M, Riera J, Drobnic F, Sureda A, Tur JA, Pons A. Body temperature modulates the antioxidant and acute immune responses to exercise. Free Radic Res 46: 799–808, 2012.
53. Montilla SIR, Johnson TP, Pearce SC, Gardan-Salmon D, Gabler NK, Ross JW, Rhoads RP, Baumgard LH, Lonergan SM, Selsby JT. Heat stress causes oxidative stress but not inflammatory signaling in porcine skeletal muscle. Temperature 1: 42–50, 2014.
54. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 417: 1–13, 2009.
55. Nethery D, Stofan D, Callahan L, DiMarco A, Supinski G. Formation of reactive oxygen species by the contracting diaphragm is PLA(2) dependent. J Appl Physiol (1985) 87: 792–800, 1999.
56. Ohira Y, Ito A, Ikawa S. Hemoconcentration during isotonic handgrip exercise. J Appl Physiol 42: 744–745, 1977.
57. Ohtsuka Y, Yabunaka N, Fujisawa H, Watanabe I, Agishi Y. Effect of thermal stress on glutathione metabolism in human erythrocytes. Eur J Appl Physiol Occup Physiol 68: 87–91, 1994.
58. Oliver SR, Phillips NA, Novosad VL, Bakos MP, Talbert EE, Clanton TL. Hyperthermia induces injury to the intestinal mucosa in the mouse: evidence for an oxidative stress mechanism. Am J Physiol Regul Integr Comp Physiol 302: R845–R853, 2012.
59. Oliver SR, Wright VP, Parinandi N, Clanton TL. Thermal tolerance of contractile function in oxidative skeletal muscle: no protection by antioxidants and reduced tolerance with eicosanoid enzyme inhibition. Am J Physiol Regul Integr Comp Physiol 295: R1695–R1705, 2008.
60. Omar RA, Yano S, Kikkawa Y. Antioxidant enzymes and survival of normal and simian virus 40-transformed mouse embryo cells after hyperthermia. Cancer Res 47: 3473–3476, 1987.
61. Ortenblad N, Young JF, Oksbjerg N, Nielsen JH, Lambert IH. Reactive oxygen species are important mediators of taurine release from skeletalmusclecells. Am J Physiol Cell Physiol 284:C1362–C1373,2003.
62. Paik IY, Jeong MH, Jin HE, Kim YI, Suh AR, Cho SY, Roh HT, Jin CH, Suh SH. Fluid replacement following dehydration reduces oxidative stress during recovery. Biochem Biophys Res Commun 383: 103–107, 2009.
63. Parkin JM, Carey MF, Zhao S, Febbraio MA. Effect of ambient temperature on human skeletal muscle metabolism during fatiguing submaximal exercise. J Appl Physiol (1985) 86: 902–908, 1999.
64. Pilch W, Szygula Z, Tyka AK, Palka T, Tyka A, Cison T, Pilch P, Teleglow A. Disturbances in pro-oxidant-antioxidant balance after passive body overheating and after exercise in elevated ambient temperatures in athletes and untrained men. PLoS One 9: e85320, 2014.
65. Powers SK, Talbert EE, Adhihetty PJ. Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle. J Physiol 589: 2129–2138, 2011.
66. Quarrie R, Lee DS, Reyes L, Erdahl W, Pfeiffer DR, Zweier JL, Crestanello JA. Mitochondrial uncoupling does not decrease reactive oxygen species production after ischemia-reperfusion. Am J Physiol Heart Circ Physiol 307: H996–H1004, 2014.
67. Quindry J, Miller L, McGinnis G, Kliszczewiscz B, Slivka D, Dumke C, Cuddy J, Ruby B. Environmental temperature and exercise-induced blood oxidative stress. Int J Sport Nutr Exerc Metab 23: 128–136, 2013.
68. Ramamoorthy S, Leibach FH, Mahesh VB, Han H, Yang-Feng T, Blakely RD, Ganapathy V. Functional characterization and chromosomal localization of a cloned taurine transporter from human placenta. Biochem J 300: 893–900, 1994.
69. Ramanadham S, Ali T, Ashley JW, Bone RN, Hancock WD, Lei X. Calcium-independent phospholipases A2 (iPLA2s) and their roles in biological processes and diseases. J Lipid Res 2015.
70. Reid MB, Haack KE, Franchek KM, Valberg PA, Kobzik L, West MS. Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro. J Appl Physiol (1985) 73: 1797–1804, 1992.
71. Reid MB, Shoji T, Moody MR, Entman ML. Reactive oxygen in skeletal muscle. II. Extracellular release of free radicals. J Appl Physiol (1985) 73: 1805–1809, 1992.
72. Rifkind JM, Ajmani RS, Heim J. Impaired hemorheology in the aged associated with oxidative stress. Adv Exp Med Biol 428: 7–13, 1997.
73. Ristow M, Zarse K, Oberbach A, Kloting N, Birringer M, Kiehntopf M, Stumvoll M, Kahn CR, Bluher M. Antioxidants prevent health-promoting effectsofphysicalexerciseinhumans. ProcNatlAcadSciUSA 106:8665–8670, 2009.
74. Ryan AJ, Gisolfi CV, Moseley PL. Synthesis of 70K stress protein by human leukocytes: effect of exercise in the heat. J Appl Physiol (1985) 70: 466–471, 1991.
75. Salo DC, Donovan CM, Davies KJ. HSP70 and other possible heat shock or oxidative stress proteins are induced in skeletal muscle, heart, and liver during exercise. Free Radic Biol Med 11: 239–246, 1991.
76. Sawka MN, Noakes TD. Does dehydration impair exercise performance? Med Sci Sports Exerc 39: 1209–1217, 2007.
77. Senay LC Jr, Pivarnik JM. Fluid shifts during exercise. Exerc Sport Sci Rev 13: 335–387, 1985.
78. Stutzin A, Torres R, Oporto M, Pacheco P, Eguiguren AL, Cid LP, Sepulveda FV. Separate taurine and chloride efflux pathways activated during regulatory volume decrease. Am J Physiol Cell Physiol 277: C392–C402, 1999.
79. Sureda A, Ferrer MD, Tauler P, Romaguera D, Drobnic F, Pujol P, Tur JA, Pons A. Effects of exercise intensity on lymphocyte H2O2 production and antioxidant defences in soccer players. Brit J Sport Med 43: 186–190, 2009.
80. Sureda A, Mestre-Alfaro A, Banquells M, Riera J, Drobnic F, Camps J, Joven J, Tur JA, Pons A. Exercise in a hot environment influences plasma anti-inflammatory and antioxidant status in well-trained athletes. J Therm Biol 47: 91–98, 2015.
81. Usher-Smith JA, Huang CL, Fraser JA. Control of cell volume in skeletal muscle. Biol Rev Camb Philos Soc 84: 143–159, 2009.
82. van der Poel C, Stephenson DG. Effects of elevated physiological temperatures on sarcoplasmic reticulum function in mechanically skinned muscle fibers of the rat. Am J Physiol Cell Physiol 293: C133–C141, 2007.
83. Vandewalle H, Lacombe C, Lelievre JC, Poirot C. Bloodviscosityaftera1-h submaximal exercise with and without drinking. Int J Sports Med 9: 104–107, 1988.
84. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci USA 101: 396–401, 2004.
85. Welc SS, Phillips NA, Oca-Cossio J, Wallet SM, Chen DL, Clanton TL. Hyperthermia increases interleukin-6 in mouse skeletal muscle. Am J Physiol Cell Physiol 303: C455–C466, 2012.
86. Wendt D, van Loon LJ, Lichtenbelt WD. Thermoregulation during exercise in the heat: strategies for maintaining health and performance. Sports Med 37: 669–682, 2007.
87. Woo CH, You HJ, Cho SH, Eom YW, Chun JS, Yoo YJ, Kim JH. LeukotrieneB(4)stimulatesRac-ERKcascadetogeneratereactiveoxygen species that mediates chemotaxis. J Biol Chem 277: 8572–8578, 2002.
88. Wood SC, Doyle MP, Appenzeller O. Effects of endurance training and long distancerunningonbloodviscosity. MedSciSportsExerc 23:1265–1269,1991.
89. Wright VP, Reiser PJ, Clanton TL. Redox modulation of global phosphatase activity and protein phosphorylation in intact skeletal muscle. J Physiol 587: 5767–5781, 2009.
90. Yasuda T, Fukumura K, Iida H, Nakajima T. Effectoflow-loadresistance exercise with and without blood flow restriction to volitional fatigue on muscle swelling. Eur J Appl Physiol 115: 919–926, 2015.
91. Zanou N, Mondin L, Fuster C, Seghers F, Dufour I, de Clippele M, Schakman O, Tajeddine N, Iwata Y, Wakabayashi S, Voets T, Allard B, Gailly P. Osmosensation in TRPV2 dominant negative expressing skeletal muscle fibres. J Physiol 593: 3849–3863, 2015.
92. Zuo L, Christofi FL, Wright VP, Bao S, Clanton TL. Lipoxygenase-dependent superoxide release in skeletal muscle. J Appl Physiol (1985) 97: 661–668, 2004.
93. Zuo L, Christofi FL, Wright VP, Liu CY, Merola AJ, Berliner LJ, Clanton TL. Intra- and extracellular measurement of reactive oxygen species produced during heat stress in diaphragm muscle. Am J Physiol Cell Physiol 279: C1058–C1066, 2000.
94. Zuo L, Pasniciuc S, Wright VP, Merola AJ, Clanton TL. Sources for superoxide release: lessons from blockade of electron transport, NADPH oxidase, and anion channels in diaphragm. Antioxid Redox Signal 5: 667–675, 2003.