Adenosine-dependent induction of glutathione peroxidase 1 in human primary endothelial cells and protection against oxidative stress

Circulation Research

Volumn 96, Issue 8, 2005, Pages 831-837

  Zhang, Yufeng ^a   Handy, Diane E ^a   Loscalzo, Joseph ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenosine; Antioxidant; Cellular glutathione peroxidase; Endothelial cells; RNA stability

Indexed keywords

ADENOSINE; ADENOSINE DEAMINASE INHIBITOR; ALCOHOL; BISINDOLYLMALEIMIDE; GLUTATHIONE PEROXIDASE; HYDROGEN; LIPID PEROXIDE; MESSENGER RNA; PROTEIN KINASE C INHIBITOR; SMALL INTERFERING RNA;

ARTICLE; CELL DAMAGE; CELL PROTECTION; CONTROLLED STUDY; ENDOTHELIUM CELL; EUKARYOTIC CELL; HUMAN; HUMAN CELL; ISCHEMIA; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; RNA STABILITY;

ADENINE; ADENOSINE; APOPTOSIS; CELLS, CULTURED; ENDOTHELIAL CELLS; ENZYME INDUCTION; GLUTATHIONE PEROXIDASE; HUMANS; HYDROGEN PEROXIDE; OXIDATIVE STRESS; PROTEIN KINASE C; RECEPTORS, PURINERGIC P1; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 18044377400     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000164401.21929.CF     Document Type: Article

References (55)

1. Liu GS, Thornton J, Van Winkle DM, Stanley AW, Olsson RA, Downey JM. Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart. Circulation. 1991;84:350-356.
2. Ely SW, Mentzer RM Jr, Lasley RD, Lee BK, Berne RM. Functional and metabolic evidence of enhanced myocardial tolerance to ischemia and reperfusion with adenosine. J Thorac Cardiovasc Surg. 1985;90:549-556.
3. Olafsson B, Forman MB, Puett DW, Pou A, Cates CU, Friesinger GC, Virmani R. Reduction of reperfusion injury in the canine preparation by intracoronary adenosine: importance of the endothelium and the no-reflow phenomenon. Circulation. 1987;76:1135-11345.
4. Mahaffey KW, Puma JA, Barbagelata NA, DiCarli MF, Leesar MA, Browne KF, Eisenberg PR, Bolli R, Casas AC, Molina-Viamonte V, Orlandi C, Blevins R, Gibbons RJ, Califf RM, Granger CB. Adenosine as an adjunct to thrombolytic therapy for acute myocardial infarction: results of a multicenter, randomized, placebo-controlled trial: the Acute Myocardial Infarction STudy of ADenosine (AMISTAD) trial. J Am Coll Cardiol. 1999;34:1711-1120.
5. Lefer DJ, Granger DN. Oxidative stress and cardiac disease. Am J Med. 2000;109:315-323.
6. Kuroda S, Siesjo BK. Reperfusion damage following focal ischemia: pathophysiology and therapeutic windows. Clin Neurosci. 1997;4:199-212.
7. Xu Z, Cohen MV, Downey JM, Vanden Hoek TL, Yao Z. Attenuation of oxidant stress during reoxygenation by AMP 579 in cardiomyocytes. Am J Physiol Heart Circ Physiol. 2001;281:H2585-H2589.
8. Lee HT, Emala CW. Adenosine attenuates oxidant injury in human proximal tubular cells via A(1) and A(2a) adenosine receptors. Am J Physiol Renal Physiol. 2002;282:F844-F852.
9. Lee HT, Emala CW. Systemic adenosine given after ischemia protects renal function via A(2a) adenosine receptor activation. Am J Kidney Dis. 2001;38:610-618.
10. Lee HT, Emala CW. Protein kinase C and G(i/o) proteins are involved in adenosine- and ischemic preconditioning-mediated renal protection. J Am Soc Nephrol. 2001;12:233-240.
11. Almeida CG, de Mendonca A, Cunha RA, Ribeiro JA. Adenosine promotes neuronal recovery from reactive oxygen species induced lesion in rat hippocampal slices. Neurosci Lett. 2003;339:127-130.
12. + channels in cerebral ischemic preconditioning. Proc Natl Acad Sci USA. 1995;92:4666-4670.
13. Driscoll DM, Copeland PR. Mechanism and regulation of selenoprotein synthesis. Annu Rev Nutr. 2003;23:17-40.
14. de Haan JB, Bladier C, Griffiths P, Keiner M, O'Shea RD, Cheung NS, Bronson RT, Silvestro MJ, Wild S, Zheng SS, Beart PM, Hertzog PJ, Kola I. Mice with a homozygous null mutation for the most abundant glutathione peroxidase, Gpx1, show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide. J Biol Chem. 1998;273:22528-22536.
15. Ter Horst GJ, Knollema S, Stuiver B, Hom H, Yoshimura S, Ruiters MH, Korf J. Differential glutathione peroxidase mRNA up-regulations in rat forebrain areas after transient hypoxia-ischemia. Ann N Y Acad Sci. 1994;738:329-333.
16. Das DK. Ischaemic preconditioning and myocardial adaptation to ischaemia. Cardiovasc Res. 1993;27:2077-2079.
17. Forgione MA, Cap A, Liao R, Moldovan NI, Eberhardt RT, Lim CC, Jones J, Goldschmidt-Clermont PJ, Loscalzo J. Heterozygous cellular glutathione peroxidase deficiency in the mouse: abnormalities in vascular and cardiac function and structure. Circulation. 2002;106:1154-1158.
18. Forgione MA, Weiss N, Heydrick S, Cap A, Klings ES, Bierl C, Eberhardt RT, Farber HW, Loscalzo J. Cellular glutathione peroxidase deficiency and endothelial dysfunction. Am J Physiol Heart Circ Physiol. 2002;282:H1255-H1261.
19. Weisbrot-Lefkowitz M, Reuhl K, Perry B, Chan PH, Inouye M, Mirochnitchenko O. Overexpression of human glutathione peroxidase protects transgenic mice against focal cerebral ischemia/reperfusion damage. Brain Res Mol Brain Res. 1998;53:333-338.
20. Yoshida T, Watanabe M, Engelman DT, Engelman RM, Schley JA, Maulik N, Ho YS, Oberley TD, Das DK. Transgenic mice overexpressing glutathione peroxidase are resistant to myocardial ischemia reperfusion injury. J Mol Cell Cardiol. 1996;28:1759-1767.
21. Mullane K, Bullough D. Harnessing an endogenous cardioprotective mechanism: cellular sources and sites of action of adenosine. J Mol Cell Cardiol. 1995;27:1041-1054.
22. Sommerschild HT, Kirkeboen KA. Adenosine and cardioprotection during ischaemia and reperfusion: an overview. Acta Anaesthesiol Scand. 2000;44:1038-1055.
23. Fryer RM, Auchampach JA, Gross GJ. Therapeutic receptor targets of ischemic preconditioning. Cardiovasc Res. 2002;55:520-525.
24. Jornot L, Junod AF. Hyperoxia, unlike phorbol ester, induces glutathione peroxidase through a protein kinase C-independent mechanism. Biochem J. 1997;326:117-123.
25. Baker RD, Baker SS, LaRosa K, Whitney C, Newburger PE. Selenium regulation of glutathione peroxidase in human hepatoma cell line Hep3B. Arch Biochem Biophys. 1993;304:53-57.
26. Islam KN, Kayanoki Y, Kaneto H, Suzuki K, Asahi M, Fujii J, Taniguchi N. TGF-beta1 triggers oxidative modifications and enhances apoptosis in HIT cells through accumulation of reactive oxygen species by suppression of catalase and glutathione peroxidase. Free Radic Biol Med. 1997;22:1007-1017.
27. Zavacki AM, Mansell JB, Chung M, Klimovitsky B, Harney JW, Berry MJ. Coupled tRNA(Sec)-dependent assembly of the selenocysteine decoding apparatus. Mol Cell. 2003;11:773-781.
28. Moriarty PM, Reddy CC, Maquat LE. Selenium deficiency reduces the abundance of mRNA for Se-dependent glutathione peroxidase 1 by a UGA-dependent mechanism likely to be nonsense codon-mediated decay of cytoplasmic mRNA. Mol Cell Biol. 1998;18:2932-2939.
29. Bermano G, Nicol F, Dyer JA, Sunde RA, Beckett GJ, Arthur JR, Hesketh JE. Selenoprotein gene expression during selenium-repletion of selenium-deficient rats. Biol Trace Elem Res. 1996;51:211-223.
30. Hers I, Tavare JM, Denton RM. The protein kinase C inhibitors bisindolyl-maleimide I (GF 109203x) and IX (Ro 31-8220) are potent inhibitors of glycogen synthase kinase-3 activity. FEBS Lett. 1999;460:433-436.
31. Chen CY, Shyu AB. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci. 1995;20:465-470.
32. Thiele BJ, Doller A, Kahne T, Pregla R, Hetzer R, Regitz-Zagrosek V. RNA-binding proteins heterogeneous nuclear ribonucleoprotein A1, E1, and K are involved in post-transcriptional control of collagen I and III synthesis. Circ Res. 2004;95:1058-1066.
33. Singh K, Laughlin J, Kosinski PA, Covey LR. Nucleolin is a second component of the CD154 mRNA stability complex that regulates mRNA turnover in activated T cells. J Immunol. 2004;173:976-985.
34. Wu R, Shen Q, Newburger PE. Recognition and binding of the human selenocysteine insertion sequence by nucleolin. J Cell Biochem. 2000;77:507-516.
35. Zhou G, Seibenhener ML, Woolen MW. Nucleolin is a protein kinase C-zeta substrate. Connection between cell surface signaling and nucleus in PC12 cells. J Biol Chem. 1997;272:31130-31137.
36. Asahi M, Fujii J, Suzuki K, Seo HG, Kuzuya T, Hori M, Tada M, Fujii S, Taniguchi N. Inactivation of glutathione peroxidase by nitric oxide. Implication for cytotoxicity. J Biol Chem. 1995;270:21035-21039.
37. Asahi M, Fujii J, Takao T, Kuzuya T, Hori M, Shimonishi Y, Taniguchi N. The oxidation of selenocysteine is involved in the inactivation of glutathione peroxidase by nitric oxide donor. J Biol Chem. 1997;272:19152-19157.
38. 2+ signaling in endothelial cells. Am J Physiol. 1995;268:H278-H287.
39. Gouaze V, Mirault ME, Carpentier S, Salvayre R, Levade T, Andrieu-Abadie N. Glutathione peroxidase-1 overexpression prevents ceramide production and partially inhibits apoptosis in doxorubicin-treated human breast carcinoma cells. Mol Pharmacol. 2001;60:488-496.
40. Merad-Saidoune M, Boitier E, Nicole A, Marsac C, Martinou JC, Sola B, Sinet PM, Ceballos-Picot I. Overproduction of Cu/Zn-superoxide dismutase or Bcl-2 prevents the brain mitochondrial respiratory dysfunction induced by glutathione depletion. Exp Neurol. 1999;158:428-436.
41. Rosenblat M, Aviram M. Macrophage glutathione content and glutathione peroxidase activity are inversely related to cell-mediated oxidation of LDL: in vitro and in vivo studies. Free Radic Biol Med. 1998;24:305-317.
42. Dringen R, Hamprecht B. Involvement of glutathione peroxidase and catalase in the disposal of exogenous hydrogen peroxide by cultured astroglial cells. Brain Res. 1997;759:67-75.
43. Fu Y, Sies H, Lei XG. Opposite roles of selenium-dependent glutathione peroxidase-1 in superoxide generator diquat- and peroxynitrite-induced apoptosis and signaling. J Biol Chem. 2001;276:43004-43009.
44. Tsukamoto M, Tampo Y, Sawada M, Yonaha M. Paraquat-induced oxidative stress and dysfunction of the glutathione redox cycle in pulmonary microvascular endothelial cells. Toxicol Appl Pharmacol. 2002;178:82-92.
45. Shingu M, Yoshioka K, Nobunaga M, Yoshida K. Human vascular smooth muscle cells and endothelial cells lack catalase activity and are susceptible to hydrogen peroxide. Inflammation. 1985;9:309-320.
46. Lin SJ, Shyue SK, Liu PL, Chen YH, Ku HH, Chen JW, Tam KB, Chen YL. Adenovirus-mediated overexpression of catalase attenuates oxLDL-induced apoptosis in human aortic endothelial cells via AP-1 and C-Jun N-terminal kinase/extracellular signal-regulated kinase mitogen-activated protein kinase pathways. J Mol Cell Cardiol. 2004;36:129-139.
47. Mirault ME, Tremblay A, Beaudoin N, Tremblay M. Overexpression of seleno-glutathione peroxidase by gene transfer enhances the resistance of T47D human breast cells to clastogenic oxidants. J Biol Chem. 1991;266:20752-20760.
48. Weiss N, Zhang YY, Heydrick S, Bierl C, Loscalzo J. Overexpression of cellular glutathione peroxidase rescues homocyst(e)ine-induced endothelial dysfunction. Proc Natl Acad Sci USA. 2001;98:12503-12508.
49. Crack PJ, Taylor JM, Flentjar NJ, de Haan J, Hertzog P, Iannello RC, Kola I. Increased infarct size and exacerbated apoptosis in the glutathione peroxidase-1 (Gpx-1) knockout mouse brain in response to ischemia/reperfusion injury. J Neurochem. 2001;78;1389-1399.
50. Tabrizchi R, Bedi S. Pharmacology of adenosine receptors in the vasculature. Pharmacol Ther. 2001;91:133-147.
51. Maggirwar SB, Dhanraj DN, Somani SM, Ramkumar V. Adenosine acts as an endogenous activator of the cellular antioxidant defense system. Biochem Biophys Res Commun. 1994;201:508-515.
52. Baxter GF, Zaman MJ, Kerac M, Yellon DM. Protection against global ischemia in the rabbit isolated heart 24 hours after transient adenosine A1 receptor activation. Cardiovasc Drugs Ther. 1997;11:83-85.
53. Takano H, Bolli R, Black RG Jr, Kodani E, Tang XL, Yang Z, Bhattacharya S, Auchampach JA. A(1) or A(3) adenosine receptors induce late preconditioning against infarction in conscious rabbits by different mechanisms. Circ Res. 2001;88:520-528.
54. Ping P, Zhang J, Cao X, Li RC, Kong D, Tang XL, Qiu Y, Manchikalapudi S, Auchampach JA, Black RG, Bolli R. PKC-dependent activation of p44/p42 MAPKs during myocardial ischemia-reperfusion in conscious rabbits. Am J Physiol. 1999;276:H1468-H1481.
55. Vondriska TM, Zhang J, Song C, Tang XL, Cao X, Baines CP, Pass JM, Wang S, Bolli R, Ping P. Protein kinase C epsilon-Src modules direct signal transduction in nitric oxide-induced cardioprotection: complex formation as a means for cardioprotective signaling. Circ Res. 2001;88:1306-1313.