Different extent of cardiac malfunction and resistance to oxidative stress in heterozygous and homozygous manganese-dependent superoxide dismutase-mutant mice

Cardiovascular Research

Volumn 82, Issue 3, 2009, Pages 448-457

  Loch, Tomasz ^a,b   Vakhrusheva, Olesya ^c   Piotrowska, Izabela ^a,c,f   Ziolkowski, Wieslaw ^d,e   Ebelt, Henning ^a   Braun, Thomas ^c   Bober, Eva ^c  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b MEDICAL UNIVERSITY OF SILESIA   (Poland)

^c MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

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

^e MEDICAL UNIVERSITY OF GDANSK   (Poland)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Apoptosis; Fibrosis; Heart failure; Oxygen radicals; Ventricular function

Indexed keywords

ATRIAL NATRIURETIC FACTOR; CATALASE; COMPLEMENTARY DNA; COPPER ZINC SUPEROXIDE DISMUTASE; DOXORUBICIN; DOXYCYCLINE; GLUTATHIONE PEROXIDASE; MANGANESE SUPEROXIDE DISMUTASE; TETRACYCLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; HEART FUNCTION; HEART HYPERTROPHY; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE FIBROSIS; HEART MUSCLE NECROSIS; HETEROZYGOSITY; HOMOZYGOSITY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBIOTICS, ANTINEOPLASTIC; ANTIOXIDANTS; APOPTOSIS; ATRIAL NATRIURETIC FACTOR; CARDIOMEGALY; DOXORUBICIN; DOXYCYCLINE; FIBROSIS; HEART FUNCTION TESTS; HETEROZYGOTE; HOMOZYGOTE; MICE; MICE, TRANSGENIC; MUTATION; MYOCARDIUM; NECROSIS; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE;

EID: 66249089511     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvp092     Document Type: Article

References (38)

1. Li Y, Huang TT, Carlson EJ, Melov S, Ursell PC, Olson JL et al. Dilated car-diomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 1995;11:376-381.
2. Lebovitz RM, Zhang H, Vogel H, Cartwright J Jr, Dionne L, Lu N et al. Neu-rodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci USA 1996;93: 9782-9787.
3. Huang TT, Carlson EJ, Kozy HM, Mantha S, Goodman SI, Ursell PC et al. Genetic modification of prenatal lethality and dilated cardiomyopathy in Mn superoxide dismutase mutant mice. Free Radic Biol Med 2001;31: 1101-1110.
4. Lynn S, Huang EJ, Elchuri S, Naeemuddin M, Nishinaka Y, Yodoi J et al. Selective neuronal vulnerability and inadequate stress response in superoxide dismutase mutant mice. Free Radic Biol Med 2005;38:817-828.
5. Huang TT, Naeemuddin M, Elchuri S, Yamaguchi M, Kozy HM, Carlson EJ et al. Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase. Hum Mol Genet 2006;15:1187-1194.
6. Van Remmen H, Salvador C, Yang H, Huang TT, Epstein CJ, Richardson A. Characterization of the antioxidant status of the heterozygous manganese superoxide dismutase knockout mouse. Arch Biochem Biophys 1999;363:91-97.
7. Van Remmen H, Ikeno Y, Hamilton M, Pahlavani M, Wolf N, Thorpe SR et al. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol Genomics 2003; 16:29-37.
8. Hoshino Y, Shioji K, Nakamura H, Masutani H, Yodoi J. From oxygen sensing to heart failure: role of thioredoxin. Antioxid Redox Signal 2007;9:689-699.
9. Dhalla NS, Saini HK, Tappia PS, Sethi R, Mengi SA, Gupta SK. Potential role and mechanisms of subcellular remodeling in cardiac dysfunction due to ischemic heart disease. J Cardiovasc Med (Hagerstown) 2007;8:238-250.
10. Takimoto E, Kass DA. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 2007;49:241-248.
11. Molavi B, Mehta JL Oxidative stress in cardiovascular disease: molecular basis of its deleterious effects, its detection, and therapeutic considerations. Curr Opin Cardiol 2004;19:488-493.
12. Li M, Chiu JF, Mossman BT, Fukagawa NK. Down-regulation of manganese-superoxide dismutase through phosphorylation of FO×O3a by Akt in explanted vascular smooth muscle cells from old rats. J Biol Chem 2006;281:40429-40439.
13. van der Loo B, Labugger R, Skepper JN, Bachschmid M, Kilo J, Powell JM et al. Enhanced peroxynitrite formation is associated with vascular aging. J Exp Med 2000;192:1731 -1744.
14. van der Loo B, Bachschmid M, Labugger R, Schildknecht S, Kilo J, Hahn R et al. Expression and activity patterns of nitric oxide synthases and anti-oxidant enzymes reveal a substantial heterogeneity between cardiac and vascular aging in the rat. Biogerontology 2005;6:325-334.
15. Nojiri H, Shimizu T, Funakoshi M, Yamaguchi O, Zhou H, Kawakami S et al. Oxidative stress causes heart failure with impaired mitochondrial respiration. J Biol Chem 2006;281:33789-33801.
16. Valenti L, Conte D, Piperno A, Dongiovanni P, Fracanzani AL, Fraquelli M et al. The mitochondrial superoxide dismutase A16V polymorphism in the cardiomyopathy associated with hereditary haemochromatosis. J Med Genet 2004;41:946-950.
17. Gottlieb MG, Schwanke CH, Santos AF, Jobim PF, Mussel DP, da Cruz IB. Association among oxidized LDL levels, MnSOD, apolipoprotein E polymorphisms, and cardiovascular risk factors in a south Brazilian region population. Genet Mol Res 2005;4:691-703.
18. Bober E, Lyons GE, Braun T, Cossu G, Buckingham M, Arnold HH. The muscle regulatory gene, Myf-6, has a biphasic pattern of expression during early mouse development. J Cell Biol 1991;113:1255-1265.
19. McCord JM, Fridovich I. The reduction of cytochrome c by milk xanthine oxidase. J Biol Chem 1968;243:5753-5760.
20. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 1995;92:9363-9367.
21. Neuhaus P, Oustanina S, Loch T, Kruger M, Bober E, Dono R et al. Reduced mobility of fibroblast growth factor (FGF)-deficient myoblasts might contribute to dystrophic changes in the musculature of FGF2/FGF6/mdx triple-mutant mice. Mol Cell Biol 2003;23:6037-6048.
22. Strassburger M, Bloch W, Sulyok S, Schuller J, Keist AF, Schmidt A et al. Heterozygous deficiency of manganese superoxide dismutase results in severe lipid peroxidation and spontaneous apoptosis in murine myocardium in vivo. Free Radic Biol Med 2005;38:1458-1470.
23. Van Remmen H, Williams MD, Guo Z, Estlack L, Yang H, Carlson EJ et al. Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am J Physiol Heart Circ Physiol 2001; 281:H1422-H1432.
24. Franch HA, Dixon RA, Blaine EH, Siegl PK. Ventricular atrial natriuretic factor in the cardiomyopathic hamster model of congestive heart failure. Circ Res 1988;62:31-36.
25. Michel JB, Arnal JF, Corvol P. Atrial natriuretic factor as a marker in congestive heart failure. Horm Res 1990;34:166-168.
26. Abassi Z, Karram T, Ellaham S, Winaver J, Hoffman A. Implications of the natriuretic peptide system in the pathogenesis of heart failure: diagnostic and therapeutic importance. Pharmacol Ther 2004;102:223-241.
27. Wang X, Gerdes AM. Chronic pressure overload cardiac hypertrophy and failure in guinea pigs. III. Intercalated disc remodeling. J Mol Cell Cardiol 1999;31:333-343.
28. Robert-Offerman SR, Leers MP, van Suylen RJ, Nap M, Daemen MJ, Theunissen PH. Evaluation of the membrane attack complex of complement for the detection of a recent myocardial infarction in man. J Pathol 2000;191:48-53.
29. Vikstrom KL, Bohlmeyer T, Factor SM, Leinwand LA. Hypertrophy, pathology, and molecular markers of cardiac pathogenesis. Circ Res 1998;82: 773-778.
30. Pimentel DR, Amin JK, Xiao L, Miller T, Viereck J, Oliver-Krasinski J et al. Reactive oxygen species mediate amplitude-dependent hypertrophic and apoptotic responses to mechanical stretch in cardiac myocytes. Circ Res 2001;89:453-460.
31. Nakagami H, Takemoto M, Liao JK. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced cardiac hypertrophy. J Mol Cell Cardiol 2003;35:851-859.
32. Dixit R, Boelsterli UA. Healthy animals and animal models of human disease(s) in safety assessment of human pharmaceuticals, including therapeutic antibodies. Drug Discov Today 2007;12:336-342.
33. Sam F, Kerstetter DL, Pimental DR, Mulukutla S, Tabaee A, Bristow MR et al. Increased reactive oxygen species production and functional alterations in antioxidant enzymes in human failing myocardium. J Card Fail 2005;11:473-480.
34. Hiroi S, Harada H, Nishi H, Satoh M, Nagai R, Kimura A. Polymorphisms in the SOD2 and HLA-DRB1 genes are associated with nonfamilial idiopathic dilated cardiomyopathy in Japanese. Biochem Biophys Res Commun 1999;261:332-339.
35. Sutton A, Imbert A, Igoudjil A, Descatoire V, Cazanave S, Pessayre D et al. The manganese superoxide dismutase Ala16Val dimorphism modulates both mitochondrial import and mRNA stability. Pharmacogenet Genomics 2005;15:311-319.
36. Thomas SR, Chen K, Keaney JF Jr. Oxidative stress and endothelial nitric oxide bioactivity. Antioxid Redox Signal 2003;5:181-194.
37. Bitar MS, Wahid S, Mustafa S, Al-Saleh E, Dhaunsi GS, Al-Mulla F. Nitric oxide dynamics and endothelial dysfunction in type II model of genetic diabetes. Eur J Pharmacol 2005;511:53-64.
38. Ungvari Z, Parrado-Fernandez C, Csiszar A, de Cabo R. Mechanisms underlying caloric restriction and lifespan regulation: implications for vascular aging. Circ Res 2008;102:519-528.