Cyclin-dependent kinase 2 signaling regulates myocardial ischemia/reperfusion injury

Journal of Molecular and Cellular Cardiology

Volumn 45, Issue 5, 2008, Pages 610-616

  Liem, David A ^a   Zhao, Peng ^a   Angelis, Ekaterini ^a   Chan, Shing S ^a   Zhang, Jun ^a   Wang, Guangwu ^a   Berthet, Cyril ^b   Kaldis, Philipp ^b   Ping, Peipei ^a   MacLellan, W Robb ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Apoptosis; Cardioprotection; Cyclin dependent kinase 2; Myocardial ischemia; Retinoblastoma gene

Indexed keywords

CASPASE 3; CYCLIN DEPENDENT KINASE 2; PROTEIN BAX; RETINOBLASTOMA PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; ENZYME ACTIVITY; ENZYME INHIBITION; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; MALE; MITOCHONDRIAL PERMEABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REPERFUSION INJURY; UPREGULATION;

ANIMALS; APOPTOSIS; CASPASE 3; CELL NUCLEUS; CYCLIN-DEPENDENT KINASE 2; MALE; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; MITOCHONDRIAL MEMBRANES; MYOCARDIAL ISCHEMIA; RATS; REPERFUSION INJURY; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION;

MUS;

EID: 55649119998     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2008.07.003     Document Type: Article

References (56)

1. Reiss K., Cheng W., Giorando A., DeLuca A., Li B., Kajstura J., et al. Myocardial infarction is coupled with activation of cyclin and cyclin-dependent kinases in myocytes. Exp Cell Res 225 (1996) 44-54
2. Adachi S., Ito H., Tamamori-Adachi M., Ono Y., Nozato T., Abe S., et al. Cyclin A/cdk2 activation is involved in hypoxia-induced apoptosis in cardiomyocytes. Circ Res 88 4 (2001) 408-414
3. Maejima Y., Adachi S., Ito H., Nobori K., Tamamori-Adachi M., and Isobe M. Nitric oxide inhibits ischemia/reperfusion-induced myocardial apoptosis by modulating cyclin A-associated kinase activity. Cardiovasc Res 59 2 (2003) 308-320
4. Price P.M., Yu F., Kaldis P., Aleem E., Nowak G., Safirstein R.L., et al. Dependence of cisplatin-induced cell death in vitro and in vivo on cyclin-dependent kinase 2. J Am Soc Nephrol 17 9 (2006) 2434-2442
5. Anderson J.A., Lewellyn A.L., and Maller J.L. Ionizing radiation induces apoptosis and elevates cyclin A1-Cdk2 activity before but not after the midblastula transition in Xenopus. Mol Biol Cell 8 7 (1997) 1195-1206
6. Harvey K.J., Lukovic D., and Ucker D.S. Caspase-dependent Cdk activity is a requisite effector of apoptotic death events. J Cell Biol 148 1 (2000) 59-72
7. Zhou B.B., Li H., Yuan J., and Kirschner M.W. Caspase-dependent activation of cyclin-dependent kinases during Fas-induced apoptosis in Jurkat cells. Proc Natl Acad Sci USA 95 12 (1998) 6785-6790
8. Hauck L., Hansmann G., Dietz R., and von Harsdorf R. Inhibition of hypoxia-induced apoptosis by modulation of retinoblastoma protein-dependent signaling in cardiomyocytes. Circ Res 91 9 (2002) 782-789
9. Katchanov J., Harms C., Gertz K., Hauck L., Waeber C., Hirt L., et al. Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal cell death. J Neurosci 21 14 (2001) 5045-5053
10. Hakem A., Sasaki T., Kozieradzki I., and Penninger J.M. The cyclin-dependent kinase Cdk2 regulates thymocyte apoptosis. J Exp Med 189 6 (1999) 957-968
11. Akli S., Zhan S., Abdellatif M., and Schneider M.D. E1A can provoke G1 exit that is refractory to p21 and independent of activating cdk2. Circ Res 85 4 (1999) 319-328
12. Liao H.S., Kang P.M., Nagashima H., Yamasaki N., Usheva A., Ding B., et al. Cardiac-specific overexpression of cyclin-dependent kinase 2 increases smaller mononuclear cardiomyocytes. Circ Res 88 4 (2001) 443-450
13. Chau B.N., Borges H.L., Chen T.T., Masselli A., Hunton I.C., and Wang J.Y. Signal-dependent protection from apoptosis in mice expressing caspase-resistant Rb. Nat Cell Biol 4 10 (2002) 757-765
14. Wang J., Guo K., Wills K.N., and Walsh K. Rb functions to inhibit apoptosis during myocyte differentiation. Cancer Res 57 3 (1997) 351-354
15. Ip S.M., Huang T.G., Yeung W.S., and Ngan H.Y. pRb-expressing adenovirus Ad5-Rb attenuates the p53-induced apoptosis in cervical cancer cell lines. Eur J Cancer 37 18 (2001) 2475-2483
16. Jacks T., Fazeli A., Schmitt E.M., Bronson R.T., Goodell M.A., and Weinberg R.A. Effects of an Rb mutation in the mouse. Nature 359 (1992) 295-300
17. Almasan A., Yin Y., Kelly R.E., Lee E.Y.H.P., Bradley A., Li W., et al. Deficiency of retinoblastoma protein leads to inappropriate s-phase entry, activation of E2F-responsive genes, and apoptosis. Proc Natl Acad Sci USA 92 (1995) 5436-5440
18. Clarke A.R., Maandag E.R., van Roon M., van der Lugt N.M., van der Valk M., Hooper M.L., et al. Requirement for a functional Rb-1 gene in murine development. Nature 359 6393 (1992) 328-330
19. Macleod K.F., Hu Y., and Jacks T. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J 15 22 (1996) 6178-6188
20. Wu L., de Bruin A., Saavedra H.I., Starovic M., Trimboli A., Yang Y., et al. Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421 6926 (2003) 942-947
21. MacPherson D., Sage J., Crowley D., Trumpp A., Bronson R.T., and Jacks T. Conditional mutation of Rb causes cell cycle defects without apoptosis in the central nervous system. Mol Cell Biol 23 3 (2003) 1044-1053
22. Janicke R.U., Walker P.A., Lin X.Y., and Porter A.G. Specific cleavage of the retinoblastoma protein by an ICE-like protease in apoptosis. EMBO J 15 24 (1996) 6969-6978
23. Fattman C.L., An B., and Dou Q.P. Characterization of interior cleavage of retinoblastoma protein in apoptosis. J Cell Biochem 67 3 (1997) 399-408
24. Pediconi N., Ianari A., Costanzo A., Belloni L., Gallo R., Cimino L., et al. Differential regulation of E2F1 apoptotic target genes in response to DNA damage. Nat Cell Biol 5 6 (2003) 552-558
25. Furukawa Y., Nishimura N., Furukawa Y., Satoh M., Endo H., Iwase S., et al. Apaf-1 is a mediator of E2F-1-induced apoptosis. J Biol Chem 277 42 (2002) 39760-39768
26. Moroni M.C., Hickman E.S., Denchi E.L., Caprara G., Colli E., Cecconi F., et al. Apaf-1 is a transcriptional target for E2F and p53. Nat Cell Biol 3 6 (2001) 552-558
27. Luciakova K., Barath P., Li R., Zaid A., and Nelson B.D. Activity of the human cytochrome c1 promoter is modulated by E2F. Biochem J 351 Pt 1 (2000) 251-256
28. Nahle Z., Polakoff J., Davuluri R.V., McCurrach M.E., Jacobson M.D., Narita M., et al. Direct coupling of the cell cycle and cell death machinery by E2F. Nat Cell Biol 4 11 (2002) 859-864
29. Berthet C., Aleem E., Coppola V., Tessarollo L., and Kaldis P. Cdk2 knockout mice are viable. Curr Biol 13 20 (2003) 1775-1785
30. MacLellan W.R., Garcia A., Oh H., Frenkel P., Jordan M.C., Roos K.P., et al. Overlapping roles of pocket proteins in the myocardium are unmasked by germ line deletion of p130 plus heart-specific deletion of Rb. Mol Cell Biol 25 6 (2005) 2486-2497
31. Agah R., Frenkel P.A., French B.A., Michael L.H., Overbeek P.A., and Schneider M.D. Gene recombination in postmitotic cells. Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J Clin Invest 100 1 (1997) 169-179
32. Wang G., Liem D.A., Vondriska T.M., Honda H.M., Korge P., Pantaleon D.M., et al. Nitric oxide donors protect murine myocardium against infarction via modulation of mitochondrial permeability transition. Am J Physiol Heart Circ Physiol 288 3 (2005) H1290-H1295
33. MacLellan W.R., Lee T.C., Schwartz R.J., and Schneider M.D. Transforming growth factor-b response elements of the skeletal a-actin gene. J Biol Chem 269 (1994) 16754-16760
34. Nijmeijer R., Willemsen M., Meijer C.J., Visser C.A., Verheijen R.H., Gottlieb R.A., et al. Type II secretory phospholipase A2 binds to ischemic flip-flopped cardiomyocytes and subsequently induces cell death. Am J Physiol Heart Circ Physiol 285 5 (2003) H2218-H2224
35. Graham F.L., and Prevec L. Methods in molecular biology vol. 7 (1991), The Humana Press Inc, Clifton, NJ
36. Webster K.A., Discher D.J., Kaiser S., Hernandez O., Sato B., and Bishopric N.H. Hypoxia-activated apoptosis of cardiac myocytes requires reoxygenation or a pH shift and is independent of p53. J Clin Invest 104 3 (1999) 239-252
37. Golsteyn R.M. Cdk1 and Cdk2 complexes (cyclin dependent kinases) in apoptosis: a role beyond the cell cycle. Cancer Lett 217 2 (2005) 129-138
38. Jin Y.H., Yim H., Park J.H., and Lee S.K. Cdk2 activity is associated with depolarization of mitochondrial membrane potential during apoptosis. Biochem Biophys Res Commun 305 4 (2003) 974-980
39. Osuga H., Osuga S., Wang F., Fetni R., Hogan M.J., Slack R.S., et al. Cyclin-dependent kinases as a therapeutic target for stroke. Proc Natl Acad Sci U S A 97 18 (2000) 10254-10259
40. Ortega S., Prieto I., Odajima J., Martin A., Dubus P., Sotillo R., et al. Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat Genet 35 1 (2003) 25-31
41. Geng Y., Yu Q., Sicinska E., Das M., Schneider J.E., Bhattacharya S., et al. Cyclin E ablation in the mouse. Cell 114 4 (2003) 431-443
42. Parisi T., Beck A.R., Rougier N., McNeil T., Lucian L., Werb Z., et al. Cyclins E1 and E2 are required for endoreplication in placental trophoblast giant cells. EMBO J 22 18 (2003) 4794-4803
43. Berthet C., Rodriguez-Galan M.C., Hodge D.L., Gooya J., Pascal V., Young H.A., et al. Hematopoiesis and thymic apoptosis are not affected by the loss of Cdk2. Mol Cell Biol 27 14 (2007) 5079-5089
44. Hirai H., Kawanishi N., and Iwasawa Y. Recent advances in the development of selective small molecule inhibitors for cyclin-dependent kinases. Curr Top Med Chem 5 2 (2005) 167-179
45. Marino S., Vooijs M., van Der G.H., Jonkers J., and Berns A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev 14 8 (2000) 994-1004
46. de Bruin A., Wu L., Saavedra H.I., Wilson P., Yang Y., Rosol T.J., et al. Rb function in extraembryonic lineages suppresses apoptosis in the CNS of Rb-deficient mice. Proc Natl Acad Sci USA 100 11 (2003) 6546-6551
47. Rashidian J., Iyirhiaro G., Aleyasin H., Rios M., Vincent I., Callaghan S., et al. Multiple cyclin-dependent kinases signals are critical mediators of ischemia/hypoxic neuronal death in vitro and in vivo. Proc Natl Acad Sci USA 102 39 (2005) 14080-14085
48. Bouchard C., Thieke K., Maier A., Saffrich R., Hanley-Hyde J., Ansorge W., et al. Direct induction of cyclin D2 by Myc contributes to cell cycle progression and sequestration of p27. EMBO J 18 19 (1999) 5321-5333
49. Perez-Roger I., Kim S.H., Griffiths B., Sewing A., and Land H. Cyclins D1 and D2 mediate myc-induced proliferation via sequestration of p27(Kip1) and p21(Cip1). EMBO J 18 19 (1999) 5310-5320
50. MacManus J.P., Koch C.J., Jian M., Walker T., and Zurakowski B. Decreased brain infarct following focal ischemia in mice lacking the transcription factor E2F1. Neuroreport 10 13 (1999) 2711-2714
51. Yurkova N., Shaw J., Blackie K., Weidman D., Jayas R., Flynn B., et al. The cell cycle factor E2F-1 activates Bnip3 and the intrinsic death pathway in ventricular myocytes. Circ Res 102 4 (2008) 472-479
52. Hamacher-Brady A., Brady N.R., Logue S.E., Sayen M.R., Jinno M., Kirshenbaum L.A., et al. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ 14 1 (2007) 146-157
53. Keramaris E., Ruzhynsky V.A., Callaghan S.M., Wong E., Davis R.J., Flavell R., et al. Required roles of Bax and JNKs in central and peripheral nervous system death of retinoblastoma-deficient mice. J Biol Chem 283 1 (2008) 405-415
54. Hochhauser E., Kivity S., Offen D., Maulik N., Otani H., Barhum Y., et al. Bax ablation protects against myocardial ischemia-reperfusion injury in transgenic mice. Am J Physiol Heart Circ Physiol 284 6 (2003) H2351-H2359
55. Miller D.L., and Van Winkle D.M. Ischemic preconditioning limits infarct size following regional ischemia-reperfusion in in situ mouse hearts. Cardiovasc Res 42 3 (1999) 680-684
56. MacLellan W.R., and Schneider M.D. Death by design. Programmed cell death in cardiovascular biology and disease. Circ Res 81 2 (1997) 137-144