Vascular endothelial growth factor recovers suppressed cytochrome c oxidase activity by restoring copper availability in hypertrophic cardiomyocytes

Experimental Biology and Medicine

Volumn 239, Issue 12, 2014, Pages 1671-1677

  Sun, Miao ^a   Zuo, Xiao ^a   Li, Rui ^a   Wang, Tao ^a   Kang, Y James ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

Cardiomyocyte; Cytochrome c oxidase; Homocysteine; Hypertrophy; Vascular endothelial growth factor

Indexed keywords

COPPER; COX 4 PROTEIN; COX11 PROTEIN; COX17 PROTEIN; CYTOCHROME C OXIDASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HOMOCYSTEINE; PHENYLEPHRINE; REACTIVE OXYGEN METABOLITE; SCO2 PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; HEART MUSCLE CELL; MUSCLE HYPERTROPHY; NONHUMAN; QUANTITATIVE ASSAY; RAT; WESTERN BLOTTING; ANIMAL; CHEMISTRY; CYTOSOL; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; COPPER; CYTOSOL; ELECTRON TRANSPORT COMPLEX IV; MYOCYTES, CARDIAC; RATS, SPRAGUE-DAWLEY; SPECTROPHOTOMETRY, ATOMIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84918530027     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370214541910     Document Type: Article

References (29)

1. Jiang Y,Reynolds C,Xiao C,Feng W,Zhou Z,Rodriguez W,Tyagi SC,Eaton JW,Saari JT,Kang YJ.Dietary copper supplementation reverses hypertrophic cardiomyopathy induced by chronic pressure overload in mice.J Exp Med. 2007;204:657-66
2. Zhou Y,Jiang Y,Kang YJ.Copper reverses cardiomyocyte hypertrophy through vascular endothelial growth factor-mediated reduction in the cell size.J Mol Cell Cardiol. 2008;45:106-17
3. Zhou Y,Bourcy K,Kang YJ.Copper-induced regression of cardiomyocyte hypertrophy is associated with enhanced vascular endothelial growth factor receptor-1 signalling pathway.Cardiovasc Res. 2009;84:54-63
4. Zuo X,Xie H,Dong D,Jiang N,Zhu H,Kang YJ.Cytochrome c oxidase is essential for copper-induced regression of cardiomyocyte hypertrophy.Cardiovasc Toxicol. 2010;10:208-15
5. Iwata S.Structure and function of bacterial cytochrome c oxidase.J Biol Chem. 1998;123:369-75
6. Abramson J,Svensson-Ek M,Byrne B,Iwata S.Structure of cytochrome c oxidase: a comparison of the bacterial and mitochondrial enzymes.Biochim Biophys Acta. 2001;1544:1-9
7. Yoshikawa S,Shinzawa-Itoh K,Tsukihara T.X-ray structure and the reaction mechanism of bovine heart cytochrome c oxidase.J Inorg Biochem. 2000;82:1-7
8. Saraste M.Structural features of cytochrome oxidase.Q Rev Biophys. 1990;23:331-66
9. Tsukihara T,Aoyama H,Yamashita E,Tomizaki T,Yamaguchi H,Shinzawa-Itoh K,Nakashima R,Yaono R,Yoshikawa S.The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å.Science. 1996;272:1136-44
10. Das J,Miller ST,Stern DL.Comparison of diverse protein sequences of the nuclear-encoded subunits of cytochrome c oxidase suggests conservation of structure underlies evolving functional sites.Mol Biol Evol. 2004;21:1572-82
11. Geier BM,Schägger H,Ortwein C,Link TA,Hagen WR,Brandt U,Von Jagow G.Kinetic properties and ligand binding of the eleven-subunit cytochrome-c oxidase from Saccharomyces cerevisiae isolated with a novel large-scale purification method.Eur J Biochem. 1995;227:296-302
12. Tsukihara T,Aoyama H,Yamashita E,Tomizaki T,Yamaguchi H,Shinzawa-Itoh K,Nakashima R,Yaono R,Yoshikawa S.Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 A.Science. 1995;269:1069-74
13. Dallman PR.Cytochrome oxidase repair during treatment of copper deficiency: relation to mitochondrial turnover.J Clin Invest. 1967;46:1819-1819
14. Prohaska JR.Changes in tissue growth, concentrations of copper, iron, cytochrome oxidase and superoxide dismutase subsequent to dietary or genetic copper deficiency in mice.J Nutr. 1983;113:2048-58
15. Prohaska JR.Changes in Cu, Zn-superoxide dismutase, cytochrome c oxidase, glutathione peroxidase and glutathione transferase activities in copper-deficient mice and rats.J Nutr. 1991;121:355-355
16. Johnson WT,Brown-Borg HM.Cardiac cytochrome-c oxidase deficiency occurs during late postnatal development in progeny of copper-deficient rats.Exp Biol Med. 2006;231:172-80
17. Glerum DM,Shtanko A,Tzagoloff A.Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase.J Biol Chem. 1996;271:14504-09
18. Takahashi Y,Kako K,Kashiwabara S-i,Takehara A,Inada Y,Arai H,Nakada K,Kodama H,Hayashi J,Baba T,Munekata E.Mammalian copper chaperone Cox17p has an essential role in activation of cytochrome C oxidase and embryonic development.Mol Cell Biol. 2002;22:7614-21
19. Leary SC,Kaufman BA,Pellecchia G,Guercin G-H,Mattman A,Jaksch M,Shoubridge EA.Human SCO1 and SCO2 have independent, cooperative functions in copper delivery to cytochrome c oxidase.Hum Mol Genet. 2004;13:1839-48
20. Leary SC,Cobine PA,Kaufman BA,Guercin G-H,Mattman A,Palaty J,Lockitch G,Winge DR,Rustin P,Horvath R,Shoubridge EA.The human cytochrome c oxidase assembly factors SCO1 and SCO2 have regulatory roles in the maintenance of cellular copper homeostasis.Cell Metab. 2007;5:9-20
21. Lu Y-M,Han F,Shioda N,Moriguchi S,Shirasaki Y,Qin Z-H,Fukunaga K.Phenylephrine-induced cardiomyocyte injury is triggered by superoxide generation through uncoupled endothelial nitric-oxide synthase and ameliorated by 3-[2-[4-(3-chloro-2-methylphenyl)-1-piperazinyl] ethyl]-5, 6-dimethoxyindazole (DY-9836), a novel calmodulin antagonist.Mol Pharmacol. 2009;75:101-12
22. Celano L,Gil M,Carballal S,Durán R,Denicola A,Banerjee R,Alvarez B.Inactivation of cystathionine β-synthase with peroxynitrite.Arch Biochem Biophys. 2009;491:96-105
23. Zuo X,Dong D,Sun M,Xie H,Kang YJ.Homocysteine restricts copper availability leading to suppression of cytochrome C oxidase activity in phenylephrine-treated cardiomyocytes.PLoS One. 2013;8:e67549-e67549
24. Linnebank M,Lutz H,Jarre E,Vielhaber S,Noelker C,Struys E,Jakobs C,Klockgether T,Evert BO,Kunz WS,Wüllner U.Binding of copper is a mechanism of homocysteine toxicity leading to COX deficiency and apoptosis in primary neurons, PC12 and SHSY-5Y cells.Neurobiol Dis. 2006;23:725-30
25. Dong D,Wang B,Yin W,Ding X,Yu J,Kang YJ.Disturbance of copper homeostasis is a mechanism for homocysteine-induced vascular endothelial cell injury.PLoS One. 2013;8:e76209-e76209
26. Hoffmann P,Richards D,Heinroth-Hoffmann I,Mathias P,Wey H,Toraason M.Arachidonic acid disrupts calcium dynamics in neonatal rat cardiac myocytes.Cardiovasc Res. 1995;30:889-98
27. Siddiqui RA,Shaikh SR,Kovacs R,Stillwell W,Zaloga G.Inhibition of phenylephrine-induced cardiac hypertrophy by docosahexaenoic acid.J Cell Biochem. 2004;92:1141-59
28. Garcia AJ,Apitz-Castro R.Plasma total homocysteine quantification: an improvement of the classical high-performance liquid chromatographic method with fluorescence detection of the thiol-SBD derivatives.J Chromatogr B. 2002;779:359-63
29. Dong D,Xu X,Yin W,Kang YJ.Changes in copper concentrations affect the protein levels but not the mRNA levels of copper chaperones in human umbilical vein endothelial cells.Metallomics. 2014;6:554-9