Prolonged swimming promotes cellular oxidative stress and p66Shc phosphorylation, but does not induce oxidative stress in mitochondria in the rat heart

Free Radical Research

Volumn 49, Issue 1, 2015, Pages 7-16

  Ziolkowski, Wieslaw ^a   Flis, D J ^b   Halon, M ^b   Vadhana, D M S ^c   Olek, R A ^a   Carloni, M ^c   Antosiewicz, J ^b   Kaczor, J J ^a   Gabbianelli, R ^c  

^a GDANSK UNIVERSITY OF PHYSICAL EDUCATION AND SPORT   (Poland)

^b MEDICAL UNIVERSITY OF GDANSK   (Poland)

^c UNIVERSITY OF CAMERINO   (Italy)

Author keywords

Cell signaling; Exercise; Mitochondria; Oxidative stress

Indexed keywords

ADAPTOR PROTEIN; ALKADIENE; CARBONYL DERIVATIVE; CATALASE; FERRITIN; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; P66SHC PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; XANTHINE OXIDASE; APOFERRITIN; BAX PROTEIN, RAT; PROTEIN SHC; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; EXTRACELLULAR SPACE; HEART MITOCHONDRION; IRON STORAGE; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SWIMMING; ANIMAL; HEART MUSCLE; METABOLISM; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; WISTAR RAT;

RATTUS;

ANIMALS; APOFERRITINS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; MALE; MITOCHONDRIA, HEART; MYOCARDIUM; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; SWIMMING;

EID: 84915748067     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2014.968147     Document Type: Article

References (67)

1. Pons S, Martin V, Portal L, Zini R, Morin D, Berdeaux A, Ghaleh B. Regular treadmill exercise restores cardioprotective signaling pathways in obese mice independently from improvement in associated co-morbidities. J Mol Cell Cardiol 2013;54:82-89.
2. Ciminelli M, Ascah A, Bourduas K, Burelle Y. Short term training attenuates opening of the mitochondrial permeability transition pore without affecting myocardial function following ischemia-reperfusion. Mol Cell Biochem 2006;291:39-47.
3. Powers SK, Sollanek KJ, Wiggs MP, Demirel HA, Smuder AJ. Exercise-induced improvements in myocardial antioxidant capacity: the antioxidant players and cardioprotection. Free Radic Res 2014;48:43-51.
4. Fisher-Wellman KH, Mattox TA, Thayne K, Katunga LA, La Favor JD, Neufer PD, et al. Novel role for thioredoxin reductase-2 in mitochondrial redox adaptations to obesogenic diet and exercise in heart and skeletal muscle. J Physiol 2013.
5. Lee Y, Min K, Talbert EE, Kavazis AN, Smuder AJ, Willis WT, Powers SK. Exercise protects cardiac mitochondria against ischemia-reperfusion injury. Med Sci Sports Exerc 2012;44:397-405.
6. Siu PM, Pei XM, Teng BT, Benzie IF, Ying M, Wong SH. Habitual exercise increases resistance of lymphocytes to oxidant-induced DNA damage by upregulating expression of antioxidant and DNA repairing enzymes. Exp Physiol 2011;96:889-906.
7. Ziolkowski W, Vadhana DM, Kaczor JJ, Olek RA, Flis DJ, Halon M, et al. Exercise-induced heart mitochondrial cholesterol depletion influences the inhibition of mitochondrial swelling. Exp Physiol 2013;98:1457-1468.
8. Ziolkowski W, Szkatula M, Nurczyk A, Wakabayashi T, Kaczor JJ, Olek RA, et al. Methyl-beta-cyclodextrin induces mitochondrial cholesterol depletion and alters the mitochondrial structure and bioenergetics. FEBS Lett 2010;584:4606-4610.
9. Garofalo T, Giammarioli AM, Misasi R, Tinari A, Manganelli V, Gambardella L, et al. Lipid microdomains contribute to apoptosis-associated modifications of mitochondria in T cells. Cell Death Differ 2005;12:1378-1389.
10. Garofalo T, Tinari A, Matarrese P, Giammarioli AM, Manganelli V, Ciarlo L, et al. Do mitochondria act as "cargo boats" in the journey of GD3 to the nucleus during apoptosis? FEBS Lett 2007;581):3899-3903.
11. Martinez-Abundis E, Garcia N, Correa F, Franco M, Zazueta C. Changes in specific lipids regulate BAX-induced mitochondrial permeability transition. FEBS J 2007;274:6500-6510.
12. Raimondo F, Morosi L, Chinello C, Perego R, Bianchi C, Albo G, et al. Protein profiling of microdomains purified from renal cell carcinoma and normal kidney tissue samples. Mol Biosyst 2012;8:1007-1016.
13. Sorice M, Mattei V, Matarrese P, Garofalo T, Tinari A, Gambardella L, et al. Dynamics of mitochondrial raft-like microdomains in cell life and death. Commun Integr Biol 2012;5:217-219.
14. Area-Gomez E, Del Carmen Lara Castillo M, Tambini MD, Guardia-Laguarta C, de Groof AJ, Madra M, et al. Upregulated function of mitochondria-associated ER membranes in Alzheimer disease. EMBO J 2012;31:4106-4123.
15. Fujimoto M, Hayashi T, Su TP. The role of cholesterol in the association of endoplasmic reticulum membranes with mitochondria. Biochem Biophys Res Commun 2012;417:635-639.
16. Voelker DR. Bridging gaps in phospholipid transport. Trends Biochem Sci 2005;30:396-404.
17. Rizzuto R, Pinton P, Brini M, Chiesa A, Filippin L, Pozzan T. Mitochondria as biosensors of calcium microdomains. Cell Calcium 1999;26:193-199.
18. Budiono BP, See Hoe LE, Peart JN, Sabapathy S, Ashton KJ, Haseler LJ, Headrick JP. Voluntary running in mice beneficially modulates myocardial ischemic tolerance, signaling kinases, and gene expression patterns. Am J Physiol Regul Integr Comp Physiol 2012;302:R1091-100.
19. Borkowska A, Sielicka-Dudzin A, Herman-Antosiewicz A, Wozniak M, Fedeli D, Falcioni G, Antosiewicz J. Diallyl trisulfide-induced prostate cancer cell death is associated with Akt/PKB dephosphorylation mediated by P-p66shc. Eur J Nutr 2012;51:817-825.
20. Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 2002;295:2450-2452.
21. Wieckowski MR, Giorgi C, Lebiedzinska M, Duszynski J, Pinton P. Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat Protoc 2009;4:1582-1590.
22. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, et al. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 2005;122:221-233.
23. Camici GG, Cosentino F, Tanner FC, Luscher TF. The role of p66Shc deletion in age-associated arterial dysfunction and disease states. J Appl Physiol 2008;105:1628-1631.
24. Pelicci G, Lanfrancone L, Grignani F, McGlade J, Cavallo F, Forni G, et al. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 1992;70:93-104.
25. Maj MC, Tkachyova I, Patel P, Addis JB, Mackay N, Levandovskiy V, et al. Oxidative stress alters the regulatory control of p66Shc and Akt in PINK1 deficient cells. Biochem Biophys Res Commun 2010;399:331-335.
26. Francia P, Cosentino F, Schiavoni M, Huang Y, Perna E, Camici GG, et al. p66(Shc) protein, oxidative stress, and cardiovascular complications of diabetes: the missing link. J Mol Med (Berl) 2009;87:885-891.
27. Miura T, Tanno M, Sato T. Mitochondrial kinase signalling pathways in myocardial protection from ischaemia/reperfusion-induced necrosis. Cardiovasc Res 2010;88:7-15.
28. Iemitsu M, Maeda S, Jesmin S, Otsuki T, Kasuya Y, Miyauchi T. Activation pattern of MAPK signaling in the hearts of trained and untrained rats following a single bout of exercise. J Appl Physiol 2006;101:151-163.
29. Ruppert C, Deiss K, Herrmann S, Vidal M, Oezkur M, Gorski A, et al. Interference with ERK(Thr188) phosphorylation impairs pathological but not physiological cardiac hypertrophy. Proc Natl Acad Sci U S A 2013;110:7440-7445.
30. Borkowska A, Sielicka-Dudzin A, Herman-Antosiewicz A, Halon M, Wozniak M, Antosiewicz J. P66Shc mediated ferritin degradation - a novel mechanism of ROS formation. Free Radic Biol Med 2011;51:658-663.
31. Brown JE, Zeiger SL, Hettinger JC, Brooks JD, Holt B, Morrow JD, et al. Essential role of the redox-sensitive kinase p66shc in determining energetic and oxidative status and cell fate in neuronal preconditioning. J Neurosci 2010;30:5242-5252.
32. Keatisuwan W, Kinjo M, Koyama T. Changes in phospholipid constituents in mitochondrial membranes after long lasting exercise in rat heart. Life Sci 1991;48:2173-2181.
33. Singh NP, McCoy MT, Tice RR, Schneider EL. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 1988;175:184-191.
34. Vadhana MS, Nasuti C, Gabbianelli R. Purine bases oxidation and repair following permethrin insecticide treatment in rat heart cells. Cardiovasc Toxicol 2010;10:199-207.
35. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-275.
36. Marcil M, Bourduas K, Ascah A, Burelle Y. Exercise training induces respiratory substrate-specific decrease in Ca2+-induced permeability transition pore opening in heart mitochondria. Am J Physiol Heart Circ Physiol 2006;290:H1549-H1557.
37. Barja G. Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J Bioenerg Biomembr 1999;31:347-366.
38. Pamplona R, Portero-Otin M, Requena J, Gredilla R, Barja G. Oxidative, glycoxidative and lipoxidative damage to rat heart mitochondrial proteins is lower after 4 months of caloric restriction than in age-matched controls. Mech Ageing Dev 2002;123:1437-1446.
39. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 1990;186:464-478.
40. Misik V, Ondrias K, Balgavy P. Effect of lipid peroxidation on molecular arrangement of phospholipids in liposomes prepared from egg yolk phosphatidylcholine or total rat brain lipids. A 31P NMR study. Gen Physiol Biophys 1992;11:317-325.
41. Flohe L, Otting F. Superoxide dismutase assays. Methods Enzymol 1984;105:93-104.
42. Mahoney DJ, Kaczor JJ, Bourgeois J, Yasuda N, Tarnopolsky MA. Oxidative stress and antioxidant enzyme upregulation in SOD1-G93A mouse skeletal muscle. Muscle Nerve 2006;33:809-816.
43. Aebi H. Catalase in vitro. Methods Enzymol 1984;105:121-126.
44. Pinton P, Rimessi A, Marchi S, Orsini F, Migliaccio E, Giorgio M, et al. Protein kinase C beta and prolyl isomerase 1 regulate mitochondrial effects of the life-span determinant p66Shc. Science 2007;315:659-663.
45. Orsini F, Migliaccio E, Moroni M, Contursi C, Raker VA, Piccini D, et al. The life span determinant p66Shc localizes to mitochondria where it associates with mitochondrial heat shock protein 70 and regulates trans-membrane potential. J Biol Chem 2004;279:25689-25695.
46. Nemoto S, Combs CA, French S, Ahn BH, Fergusson MM, Balaban RS, Finkel T. The mammalian longevity-associated gene product p66shc regulates mitochondrial metabolism. J Biol Chem 2006;281:10555-10560.
47. Mota MP, Peixoto FM, Soares JF, Figueiredo PA, Leitao JC, Gaivao I, Duarte JA. Influence of aerobic fitness on age-related lymphocyte DNA damage in humans: relationship with mitochondria respiratory chain and hydrogen peroxide production. Age (Dordr) 2010;32:337-346.
48. Wierzba TH, Olek RA, Fedeli D, Falcioni G. Lymphocyte DNA damage in rats challenged with a single bout of strenuous exercise. J Physiol Pharmacol 2006;57:115-131.
49. Pozzi R, Rosa JC, Eguchi R, Oller do Nascimento CM, Oyama LM, Aguiar O Jr, et al. Genetic damage in multiple organs of acutely exercised rats. Cell Biochem Funct 2010;28:632-636.
50. Clarkson PM, Thompson HS. Antioxidants: what role do they play in physical activity and health? Am J Clin Nutr 2000;72:637S-646S.
51. Chance B, Sies H, Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 1979;59:527-605.
52. Papa S, Guerrieri F, Capitanio N. A possible role of slips in cytochrome C oxidase in the antioxygen defense system of the cell. Biosci Rep 1997;17:23-31.
53. Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, et al. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 1999;402:309-313.
54. Yamamori T, Mizobata A, Saito Y, Urano Y, Inanami O, Irani K, Noguchi N. Phosphorylation of p66shc mediates 6-hydroxydopamine cytotoxicity. Free Radic Res 2011;45:342-350.
55. Orsini F, Moroni M, Contursi C, Yano M, Pelicci P, Giorgio M, Migliaccio E. Regulatory effects of the mitochondrial energetic status on mitochondrial p66Shc. Biol Chem 2006;387:1405-1410.
56. Graiani G, Lagrasta C, Migliaccio E, Spillmann F, Meloni M, Madeddu P, et al. Genetic deletion of the p66Shc adaptor protein protects from angiotensin II-induced myocardial damage. Hypertension 2005;46:433-440.
57. Bianchi G, Di Giulio C, Rapino C, Rapino M, Antonucci A, Cataldi A. p53 and p66 proteins compete for hypoxia-inducible factor 1 alpha stabilization in young and old rat hearts exposed to intermittent hypoxia. Gerontology 2006;52:17-23.
58. Rota M, LeCapitaine N, Hosoda T, Boni A, De Angelis A, Padin-Iruegas ME, et al. Diabetes promotes cardiac stem cell aging and heart failure, which are prevented by deletion of the p66shc gene. Circ Res 2006;99:42-52.
59. Malhotra A, Vashistha H, Yadav VS, Dube MG, Kalra SP, Abdellatif M, Meggs LG. Inhibition of p66ShcA redox activity in cardiac muscle cells attenuates hyperglycemia-induced oxidative stress and apoptosis. Am J Physiol Heart Circ Physiol 2009;296:H380-H388.
60. Ascensao A, Lumini-Oliveira J, Machado NG, Ferreira RM, Goncalves IO, Moreira AC, et al. Acute exercise protects against calcium-induced cardiac mitochondrial permeability transition pore opening in doxorubicin-treated rats. Clin Sci (Lond) 2011;120:37-49.
61. Brancaccio P, Lippi G, Maffulli N. Biochemical markers of muscular damage. Clin Chem Lab Med 2010;48:757-767.
62. De Domenico I, Vaughn MB, Li L, Bagley D, Musci G, Ward DM, Kaplan J. Ferroportin-mediated mobilization of ferritin iron precedes ferritin degradation by the proteasome. EMBO J 2006;25:5396-5404.
63. Konijn AM, Glickstein H, Vaisman B, Meyron-Holtz EG, Slotki IN, Cabantchik ZI. The cellular labile iron pool and intracellular ferritin in K562 cells. Blood 1999;94:2128-2134.
64. Epsztejn S, Glickstein H, Picard V, Slotki IN, Breuer W, Beaumont C, Cabantchik ZI. H-ferritin subunit overexpression in erythroid cells reduces the oxidative stress response and induces multidrug resistance properties. Blood 1999;94:3593-3603.
65. Kruszewski M. Labile iron pool: the main determinant of cellular response to oxidative stress. Mutat Res 2003;531:81-92.
66. Harrison PM, Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1996;1275:161-203.
67. Coven DL, Hu X, Cong L, Bergeron R, Shulman GI, Hardie DG, Young LH. Physiological role of AMP-activated protein kinase in the heart: graded activation during exercise. Am J Physiol Endocrinol Metab 2003;285:E629-E636.