Vitamin E isoform-specific inhibition of the exercise-induced heat shock protein 72 expression in humans

Journal of Applied Physiology

Volumn 100, Issue 5, 2006, Pages 1679-1687

  Fischer, Christian P ^a,b   Hiscock, Natalie J ^c   Basu, Samar ^d   Vessby, Bengt ^d   Kallner, Anders ^e   Sjöberg, Lars Börje ^f   Febbraio, Mark A ^c   Pedersen, Bente K ^a,b  

^a Rigshospitalet   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c RMIT UNIVERSITY   (Australia)

^d UPPSALA UNIVERSITY   (Sweden)

^e KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^f Research and Quality Department   (Sweden)

Author keywords

tocopherol; tocopherol; Ascorbic acid; Serum; Skeletal muscle

Indexed keywords

8 ISOPROSTAGLANDIN F2 ALPHA; ADRENALIN; ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; GAMMA TOCOPHEROL; GLUCOSE; HEAT SHOCK PROTEIN 72; HYDROCORTISONE; MESSENGER RNA; NORADRENALIN; PLACEBO;

ADULT; ARTICLE; BLOOD SAMPLING; CIRCULATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG ACTIVITY; DRUG BLOOD LEVEL; DRUG INHIBITION; EXERCISE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; LIPID PEROXIDATION; MALE; MUSCLE BIOPSY; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CONTENT; PROTEIN EXPRESSION; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE; VITAMIN BLOOD LEVEL; VITAMIN SUPPLEMENTATION;

ADULT; ALPHA-TOCOPHEROL; ASCORBIC ACID; BLOOD GLUCOSE; DINOPROST; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPINEPHRINE; EXERCISE; GAMMA-TOCOPHEROL; GENE EXPRESSION REGULATION; HSP72 HEAT-SHOCK PROTEINS; HUMANS; HYDROCORTISONE; LIPID PEROXIDATION; MALE; MUSCLE, SKELETAL; NOREPINEPHRINE; PROTEIN ISOFORMS; RNA, MESSENGER; VITAMIN E;

EID: 33646419773     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00421.2005     Document Type: Article

References (66)

1. Adrie C, Richter C, Bachelet M, Banzet N, Francois D, Dinh-Xuan AT, Dhainaut JF, Polla BS, and Richard MJ. Contrasting effects of NO and peroxynitrites on HSP70 expression and apoptosis in human monocytes. Am J Physiol Cell Physiol 279: C452-C460, 2000.
2. Alessio HM, Goldfarb AH, and Cutler RG. MDA content increases in fast- and slow-twitch skeletal muscle with intensity of exercise in a rat. Am J Physiol Cell Physiol 255: C874-C877, 1988.
3. Andersen P, Adams RP, Sjogaard G, Thorboe A, and Saltin B. Dynamic knee extension as model for study of isolated exercising muscle in humans. J Appl Physiol 59: 1647-1653, 1985.
4. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, and Calderwood SK. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 6: 435-442, 2000.
5. Balon TW and Nadler JL. Nitric oxide release is present from incubated skeletal muscle preparations. J Appl Physiol 77: 2519-2521, 1994.
6. Basu S. Radioimmunoassay of 8-iso-prostaglandin F2alpha: an index for oxidative injury via free radical catalysed lipid peroxidation. Prostaglandins Leukot Essent Fatty Acids 58: 319-325, 1998.
7. Bergstedt K, Hu BR, and Wieloch T. Initiation of protein synthesis and heat-shock protein-72 expression in the rat brain following severe insulin-induced hypoglycemia. Acta Neuropathol (Berl) 86: 145-153, 1993.
8. Bergstrom J. Muscle electrolytes in man. Scand J Clin Lab Invest 68: 1-101, 1962.
9. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
10. Bruce CR, Carey AL, Hawley JA, and Febbraio MA. Intramuscular heat shock protein 72 and heme oxygenase-1 mRNA are reduced in patients with Type 2 diabetes: evidence that insulin resistance is associated with a disturbed antioxidant defense mechanism. Diabetes 52: 2338-2345, 2003.
11. Buettner GR. The pecking order of free radicals and antioxidants: lipid peroxidation, alpha-tocopherol, and ascorbate. Arch Biochem Biophys 300: 535-543, 1993.
12. Childs A, Jacobs C, Kaminski T, Halliwell B, and Leeuwenburgh C. Supplementation with vitamin C and N-acetyl-cysteine increases oxidative stress in humans after an acute muscle injury induced by eccentric exercise. Free Radic Biol Med 31: 745-753, 2001.
13. x and complements α-tocopherol: physiological implications. Proc Natl Acad Sci USA 94: 3217-3222, 1997.
14. Commoner B, Townsend J, and Pake GE. Free radicals in biological materials. Nature 174: 689-691, 1954.
15. Cooney RV, Franke AA, Harwood PJ, Hatch-Pigott V, Custer LJ, and Mordan LJ. Gamma-tocopherol detoxification of nitrogen dioxide: superiority to alpha-tocopherol. Proc Natl Acad Sci USA 90: 1771-1775, 1993.
16. Davies KJ, Quintanilha AT, Brooks GA, and Packer L. Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107: 1198-1205, 1982.
17. Deutsch MJ and Weeks CE. Microfluorometric assay for vitamin C. J Ass Offic Chem 48: 1248-1256, 1965.
18. Dill DB and Costill DL. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol 37: 247-248, 1974.
19. Febbraio MA and Koukoulas I. HSP72 gene expression progressively increases in human skeletal muscle during prolonged, exhaustive exercise. J Appl Physiol 89: 1055-1060, 2000.
20. Febbraio MA, Ott P, Nielsen HB, Steensberg A, Keller C, Krustrup P, Secher NH, and Pedersen BK. Exercise induces hepatosplanchnic release of heat shock protein 72 in humans. J Physiol 544: 957-962, 2002.
21. Febbraio MA, Steensberg A, Walsh R, Koukoulas I, Van Hall G, and Pedersen BK. Reduced muscle glycogen availability elevates HSP72 in contracting human skeletal muscle. J Physiol 538: 911-917, 2002.
22. Feder ME and Hofmann GE. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61: 243-282, 1999.
23. Gastpar R, Gehrmann M, Bausero MA, Asea A, Gross C, Schroeder JA, and Multhoff G. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res 65: 5238-5247, 2005.
24. Gysin R, Azzi A, and Visarius T. γ-Tocopherol inhibits human cancer cell cycle progression and cell proliferation by down-regulation of cyclins. FASEB J 16: 1952-1954, 2002.
25. Hammerer-Lercher A, Mair J, Bonatti J, Watzka SB, Puschendorf B, and Dirnhofer S. Hypoxia induces heat shock protein expression in human coronary artery bypass grafts. Cardiovasc Res 50: 115-124, 2001.
26. Handelman GJ, Machlin LJ, Fitch K, Weiter JJ, and Dratz EA. Oral alpha-tocopherol supplements decrease plasma gamma-tocopherol levels in humans. J Nutr 115: 807-813, 1985.
27. Helzlsouer KJ, Huang HY, Alberg AJ, Hoffman S, Burke A, Norkus EP, Morris JS, and Comstock GW. Association between alpha-tocopherol, gamma-tocopherol, selenium, and subsequent prostate cancer. J Natl Cancer Inst 92: 2018-2023, 2000.
28. Hensley K, Benaksas EJ, Bolli R, Comp P, Grammas P, Hamdheydari L, Mou S, Pye QN, Stoddard MF, and Wallis G. New perspectives on vitamin E: γ-tocopherol and carboxyethylhydroxychroman metabolites in biology and medicine. Free Radic Biol Med 36: 1-15, 2004.
29. Huang HY, Appel LJ, Croft KD, Miller ER III, Mori TA, and Puddey IB. Effects of vitamin C and vitamin E on in vivo lipid peroxidation: results of a randomized controlled trial. Am J Clin Nutr 76: 549-555, 2002.
30. Jackson MJ, Edwards RH, and Symons MC. Electron spin resonance studies of intact mammalian skeletal muscle. Biochim Biophys Acta 847: 185-190, 1985.
31. Jiang Q and Ames BN. γ-Tocopherol, but not α-tocopherol, decreases proinflammatory eicosanoids and inflammation damage in rats. FASEB J 17: 816-822, 2003.
32. Jiang Q, Christen S, Shigenaga MK, and Ames BN. Gamma-tocopherol, the major form of vitamin E in the US diet, deserves more attention. Am J Clin Nutr 74: 714-722, 2001.
33. Jiang Q, Elson-Schwab I, Courtemanche C, and Ames BN. γ-Tocopherol and its major metabolite, in contrast to α-tocopherol, inhibit cyclooxygenase activity in macrophages and epithelial cells. Proc Natl Acad Sci USA 97: 11494-11499, 2000.
34. Kanter MM, Nolte LA, and Holloszy JO. Effects of an antioxidant vitamin mixture on lipid peroxidation at rest and postexercise. J Appl Physiol 74: 965-969, 1993.
35. Khassaf M, McArdle A, Esanu C, Vasilaki A, McArdle F, Griffiths RD, Brodie DA, and Jackson MJ. Effect of vitamin C supplements on antioxidant defence and stress proteins in human lymphocytes and skeletal muscle. J Physiol 549: 645-652, 2003.
36. Kregel KC. Molecular Biology of Thermoregulation: Invited Review: Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92: 2177-2186, 2002.
37. Kurucz I, Morva A, Vaag A, Eriksson KF, Huang X, Groop L, and Koranyi L. Decreased expression of heat shock protein 72 in skeletal muscle of patients with type 2 diabetes correlates with insulin resistance. Diabetes 51: 1102-1109, 2002.
38. Laemmli UK. Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227: 680-685, 1970.
39. Lepore DA, Hurley JV, Stewart AG, Morrison WA, and Anderson RL. Prior heat stress improves survival of ischemic-reperfused skeletal muscle in vivo. Muscle Nerve 23: 1847-1855, 2000.
40. Liu M, Wallin R, Wallmon A, and Saldeen T. Mixed tocopherols have a stronger inhibitory effect on lipid peroxidation than alpha-tocopherol alone. J Cardiovasc Pharmacol 39: 714-721, 2002.
41. Liu Y, Mayr S, Opitz-Gress A, Zeller C, Lormes W, Baur S, Lehmann M, and Steinacker JM. Human skeletal muscle HSP70 response to training in highly trained rowers. J Appl Physiol 86: 101-104, 1999.
42. T method. Methods 25: 402-408, 2001.
43. Locke M, Noble EG, and Atkinson BG. Exercising mammals synthesize stress proteins. Am J Physiol Cell Physiol 258: C723-C729, 1990.
44. Marber MS, Mestril R, Chi SH, Sayen MR, Yellon DM, and Dillmann WH. Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J Clin Invest 95: 1446-1456, 1995.
45. Marini M, Frabetti F, Musiani D, and Franceschi C. Oxygen radicals induce stress proteins and tolerance to oxidative stress in human lymphocytes. Int J Radiat Biol 70: 337-350, 1996.
46. Messner T, Erkstam UB, Gustafsson IB, Nilsson SB, and Vessby B. Diet and dietary markers in Kiruna and Uppsala, Sweden - a comparison. Int J Circumpolar Health 56: 21-29, 1997.
47. Meydani M, Fielding RA, Cannon JG, Blumberg J, and Evans WJ. Muscle uptake of vitamin E and its association with muscle fiber type. J Nutr Biochem 8: 74-78, 1997.
48. Mizzen LA and Welch WJ. Characterization of the thermotolerant cell. I. Effects on protein synthesis activity and the regulation of heat-shock protein 70 expression. J Cell Biol 106: 1105-1116, 1988.
49. Morrow JD, Awad JA, Boss HJ, Blair IA, and Roberts LJ. Noncyclooxygenase-derived prostanoids (F2-isoprostanes) are formed in situ on phospholipids. Proc Natl Acad Sci USA 89: 10721-10725, 1992.
50. Morrow JD, Minton TA, Badr KF, and Roberts LJ. Evidence that the F-2-isoprostane, 8-epi-prostaglandin F2-alpha, is formed in-vivo. Biochim Biophys Acta 1210: 244-248, 1994.
51. Nieman DC, Peters EM, Henson DA, Nevines EI, and Thompson MM. Influence of vitamin C supplementation on cytokine changes following an ultramarathon. J Interferon Cytokine Res 20: 1029-1035, 2000.
52. Niess AM, Fehrenbach E, Schlotz E, Sommer M, Angres C, Tschositsch K, Battenfeld N, Golly IC, Biesalski HK, Northoff H, and Dickhuth HH. Effects of RRR-alpha-tocopherol on leukocyte expression of HSP72 in response to exhaustive treadmill exercise. Int J Sports Med 23: 445-452, 2002.
53. Ohrvall M, Tengblad S, and Vessby B. Lower tocopherol serum levels in subjects with abdominal adiposity. J Intern Med 234: 53-60, 1993.
54. Paroo Z and Noble EG. Isoproterenol potentiates exercise-induction of Hsp70 in cardiac and skeletal muscle. Cell Stress Chaperones 4: 199-204, 1999.
55. Peters EM, Anderson R, and Theron AJ. Attenuation of increase in circulating cortisol and enhancement of the acute phase protein response in vitamin C-supplemented ultramarathoners. Int J Sports Med 22: 120-126, 2001.
56. Petersen EW, Ostrowski K, Ibfelt T, Richelle M, Offord E, Halkjaer-Kristensen J, and Pedersen BK. Effect of vitamin supplementation on cytokine response and on muscle damage after strenuous exercise. Am J Physiol Cell Physiol 280: C1570-C1575, 2001.
57. Poulsen HE, Loft S, and Vistisen K. Extreme exercise and oxidative DNA modification. J Sports Sci 14: 343-346, 1996.
58. Puntschart A, Vogt M, Widmer HR, Hoppeler H, and Billeter R. Hsp70 expression in human skeletal muscle after exercise. Acta Physiol Scand 157: 411-417, 1996.
59. Smolka MB, Zoppi CC, Alves AA, Silveira LR, Marangoni S, Pereira-Da-Silva L, Novello JC, and Macedo DV. HSP72 as a complementary protection against oxidative stress induced by exercise in the soleus muscle of rats. Am J Physiol Regul Integr Comp Physiol 279: R1539-R1545, 2000.
60. Steensberg A, Toft AD, Schjerling P, Halkjaer-Kristensen J, and Pedersen BK. Plasma interleukin-6 during strenuous exercise: role of epinephrine. Am J Physiol Cell Physiol 281: C1001-C1004, 2001.
61. Thompson HS, Scordilis SP, Clarkson PM, and Lohrer WA. A single bout of eccentric exercise increases HSP27 and HSC/HSP70 in human skeletal muscle. Acta Physiol Scand 171: 187-193, 2001.
62. Vuilleumier JP and Keck E. Fluorometric assay of vitamin C in biological materials using a centrifugal analyser with fluorescence attachment. J Micronutr Anal 5: 25-34, 1989.
63. Wallen ES, Buettner GR, and Moseley PL. Oxidants differentially regulate the heat shock response. Int J Hyperthermia 13: 517-524, 1997.
64. Walsh RC, Koukoulas I, Garnham AP, Moseley PL, Hargreaves M, and Febbraio MA. Exercise increases serum Hsp72 in humans. Cell Stress Chaperones 6: 386-393, 2001.
65. 2+-ionophore-regulated proteins. J Biol Chem 258: 7102-7111, 1983.
66. Wolf G. γ-Tocopherol: an efficient protector of lipids against nitric oxide-initiated peroxidative damage. Nutr Rev 55: 376-378, 1997.