Role of CDK5/cyclin complexes in ischemia-induced death and survival of renal tubular cells

Cell Cycle

Volumn 13, Issue 10, 2014, Pages 1617-1626

  Guevara, Tatiana ^a,b   Sancho, Mónica ^a   Peŕez Payá, Enrique ^a,b   Orzaéz, Mar ^a  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^b INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

Apoptosis; CDK5; Ischemia reperfusion; Kidney injury; Renal preservation

Indexed keywords

CASPASE 3; CASPASE 7; CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLINE; DSB TAT NBI 1; HISTONE H2AX; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; ROSCOVITINE; SMALL INTERFERING RNA; TAT NBI 1; TUBULIN; UNCLASSIFIED DRUG; CYCLIN A; NERVE PROTEIN; NEURONAL CDK5 ACTIVATOR (P25-P35);

ANIMAL CELL; ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; IN VITRO STUDY; KIDNEY ISCHEMIA; KIDNEY PRESERVATION; KIDNEY TUBULE CELL; LLC PK1 CELL LINE; NONHUMAN; PROTEIN EXPRESSION; RENAL PROTECTION; REPERFUSION; SWINE; ANIMAL; CELL HYPOXIA; CELL LINE; CYTOLOGY; GENETICS; KIDNEY TUBULE; METABOLISM; PIG;

ANIMALS; CELL DEATH; CELL HYPOXIA; CELL LINE; CELL SURVIVAL; CYCLIN A; CYCLIN-DEPENDENT KINASE 5; KIDNEY TUBULES; NERVE TISSUE PROTEINS; SWINE;

EID: 84900548645     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.28628     Document Type: Article

References (38)

1. Bagshaw SM, Mortis G, Godinez-Luna T, Doig CJ, Laupland KB. Renal recovery after severe acute renal failure. Int J Artif Organs 2006; 29:1023-30; PMID:17160959
2. Legrand M, Mik EG, Johannes T, Payen D, Ince C. Renal hypoxia and dysoxia after reperfusion of the ischemic kidney. Mol Med 2008; 14:502-16; PMID:18488066; http://dx.doi.org/10.2119/2008-00006.Legrand
3. Kosieradzki M, Rowiński W. Ischemia/reperfusion injury in kidney transplantation: mechanisms and prevention. Transplant Proc 2008; 40:3279-88; PMID:19100373; http://dx.doi.org/10.1016/j.transproceed.2008.10.004
4. Rashidian J, Iyirhiaro G, Aleyasin H, Rios M, Vincent I, Callaghan S, Bland RJ, Slack RS, During MJ, Park DS. Multiple cyclin-dependent kinases signals are critical mediators of ischemia/hypoxic neuronal death in vitro and in vivo. Proc Natl Acad Sci U S A 2005; 102:14080-5; PMID:16166266; http://dx.doi.org/10.1073/pnas.0500099102
5. Iyirhiaro GO, Brust TB, Rashidian J, Galehdar Z, Osman A, Phillips M, Slack RS, Macvicar BA, Park DS. Delayed combinatorial treatment with flavopiridol and minocycline provides longer term protection for neuronal soma but not dendrites following global ischemia. J Neurochem 2008; 105:703-13; PMID:18205749; http://dx.doi.org/10.1111/j.1471-4159.2007.05166.x
6. Hardcastle IR, Golding BT, Griffin RJ. Designing inhibitors of cyclin-dependent kinases. Annu Rev Pharmacol Toxicol 2002; 42:325-48; PMID:11807175; http://dx.doi.org/10.1146/annurev.pharmtox.42.090601.125940
7. Canela N, Orzáez M, Fucho R, Mateo F, Gutierrez R, Pineda-Lucena A, Bachs O, Pérez-Payá E. Identification of an hexapeptide that binds to a surface pocket in cyclin A and inhibits the catalytic activity of the complex cyclin-dependent kinase 2-cyclin A. J Biol Chem 2006; 281:35942-53; PMID:17001081; http://dx.doi.org/10.1074/jbc.M603511200
8. Orzáez M, Guevara T, Sancho M, Pérez-Payá E. Intrinsic caspase-8 activation mediates sensitization of erlotinib-resistant tumor cells to erlotinib/cell-cycle inhibitors combination treatment. Cell Death Dis 2012; 3:e415; PMID:23096116; http://dx.doi.org/10.1038/cddis.2012.155
9. Hotter G, Palacios L, Sola A. Low O2 and high CO2 in LLC-PK1 cells culture mimics renal ischemia-induced apoptosis. Lab Invest 2004; 84:213-20; PMID:14688798; http://dx.doi.org/10.1038/labinvest.3700026
10. Lalioti V, Muruais G, Dinarina A, van Damme J, Vandekerckhove J, Sandoval IV. The atypical kinase Cdk5 is activated by insulin, regulates the association between GLUT4 and E-Syt1, and modulates glucose transport in 3T3-L1 adipocytes. Proc Natl Acad Sci U S A 2009; 106:4249-53; PMID:19255425; http://dx.doi.org/ 10.1073/pnas.0900218106
11. Hisanaga S, Endo R. Regulation and role of cyclin-dependent kinase activity in neuronal survival and death. J Neurochem 2010; 115:1309-21; PMID:21044075; http://dx.doi.org/10.1111/j.1471-4159.2010.07050.x
12. Dhariwala FA, Rajadhyaksha MS. An unusual member of the Cdk family: Cdk5. Cell Mol Neurobiol 2008; 28:351-69; PMID:18183483; http://dx.doi.org/10.1007/ s10571-007-9242-1
13. Brinkkoetter PT, Pippin JW, Shankland SJ. Cyclin I-Cdk5 governs survival in post-mitotic cells. Cell Cycle 2010; 9:1729-31; PMID:20404535; http://dx.doi.org/10.4161/cc.9.9.11471
14. Brinkkoetter PT, Olivier P, Wu JS, Henderson S, Krofft RD, Pippin JW, Hockenbery D, Roberts JM, Shankland SJ. Cyclin I activates Cdk5 and regulates expression of Bcl-2 and Bcl-XL in post-mitotic mouse cells. J Clin Invest 2009; 119:3089-101; PMID:19729834; http://dx.doi.org/10.1172/JCI37978
15. Taniguchi Y, Pippin JW, Hagmann H, Krofft RD, Chang AM, Zhang J, Terada Y, Brinkkoetter P, Shankland SJ. Both cyclin I and p35 are required for maximal survival benefit of cyclin-dependent kinase 5 in kidney podocytes. Am J Physiol Renal Physiol 2012; 302:F1161-71; PMID:22262481; http://dx.doi.org/10.1152/ ajprenal.00614.2011
16. Griffin SV, Olivier JP, Pippin JW, Roberts JM, Shankland SJ. Cyclin I protects podocytes from apoptosis. J Biol Chem 2006; 281:28048-57; PMID:16847066; http://dx.doi.org/10.1074/jbc.M513336200
17. MacCallum DE, Melville J, Frame S, Watt K, Anderson S, Gianella-Borradori A, Lane DP, Green SR. Seliciclib (CYC202, R-Roscovitine) induces cell death in multiple myeloma cells by inhibition of RNA polymerase II-dependent transcription and downregulation of Mcl-1. Cancer Res 2005; 65:5399-407; PMID:15958589; http://dx.doi.org/10.1158/0008-5472.CAN-05-0233
18. Hilton GD, Stoica BA, Byrnes KR, Faden AI. Roscovitine reduces neuronal loss, glial activation, and neurologic deficits after brain trauma. J Cereb Blood Flow Metab 2008; 28:1845-59; PMID:18612315; http://dx.doi.org/10.1038/ jcbfm.2008.75
19. Menn B, Bach S, Blevins TL, Campbell M, Meijer L, Timsit S. Delayed treatment with systemic (S)-roscovitine provides neuroprotection and inhibits in vivo CDK5 activity increase in animal stroke models. PLoS One 2010; 5:e12117; PMID:20711428; http://dx.doi.org/10.1371/journal.pone.0012117
20. Brinkkoetter PT, Wu JS, Ohse T, Krofft RD, Schermer B, Benzing T, Pippin JW, Shankland SJ. p35, the non-cyclin activator of Cdk5, protects podocytes against apoptosis in vitro and in vivo. Kidney Int 2010; 77:690-9; PMID:20130526; http://dx.doi.org/10.1038/ki.2009.548
21. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, Inagaki N, Inagaki M, Delcros JG, Moulinoux JP. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 1997; 243:527-36; PMID:9030781; http://dx.doi.org/10.1111/j. 1432-1033.1997.t01-2-00527.x
22. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273:5858-68; PMID:9488723; http://dx.doi.org/10.1074/jbc.273.10.5858
23. Capasso H, Palermo C, Wan S, Rao H, John UP, O'Connell MJ, Walworth NC. Phosphorylation activates Chk1 and is required for checkpoint-mediated cell cycle arrest. J Cell Sci 2002; 115:4555-64; PMID:12415000; http://dx.doi.org/10. 1242/jcs.00133
24. Wang CX, Song JH, Song DK, Yong VW, Shuaib A, Hao C. Cyclin-dependent kinase-5 prevents neuronal apoptosis through ERK-mediated upregulation of Bcl-2. Cell Death Differ 2006; 13:1203-12; PMID:16273078; http://dx.doi.org/10.1038/ sj.cdd.4401804
25. Piedrahita D, Hernández I, López-Tobón A, Fedorov D, Obara B, Manjunath BS, Boudreau RL, Davidson B, Laferla F, Gallego-Gómez JC, et al. Silencing of CDK5 reduces neurofibrillary tangles in transgenic alzheimer's mice. J Neurosci 2010; 30:13966-76; PMID:20962218; http://dx.doi.org/10.1523/JNEUROSCI.3637-10.2010
26. Kaminosono S, Saito T, Oyama F, Ohshima T, Asada A, Nagai Y, Nukina N, Hisanaga S. Suppression of mutant Huntingtin aggregate formation by Cdk5/p35 through the effect on microtubule stability. J Neurosci 2008; 28:8747-55; PMID:18753376; http://dx.doi.org/10.1523/JNEUROSCI.0973-08.2008
27. Strock CJ, Park JI, Nakakura EK, Bova GS, Isaacs JT, Ball DW, Nelkin BD. Cyclin-dependent kinase 5 activity controls cell motility and metastatic potential of prostate cancer cells. Cancer Res 2006; 66:7509-15; PMID:16885348; http://dx.doi.org/10.1158/0008-5472.CAN-05-3048
28. Paoletti P, Vila I, Rifé M, Lizcano JM, Alberch J, Ginés S. Dopaminergic and glutamatergic signaling crosstalk in Huntington's disease neurodegeneration: the role of p25/cyclin-dependent kinase 5. J Neurosci 2008; 28:10090-101; PMID:18829967; http://dx.doi.org/10.1523/JNEUROSCI.3237-08.2008
29. Aydemir A, Abbasoglu O, Topaloglu S, Ertoy D, Ayhan A, Kilinç K, Karabulut E, Sayek I. Protective effect of roscovitine on renal ischemia reperfusion injury. Transplant Proc 2002; 34:2027-8; PMID:12270300; http://dx.doi.org/10.1016/S0041-1345(02)02838-5
30. Timsit S, Menn B. Cerebral ischemia, cell cycle elements and Cdk5. Biotechnol J 2007; 2:958-66; PMID:17619233; http://dx.doi.org/10.1002/biot. 200700072
31. Topaloglu S, Abbasoglu O, Ayhan A, Sokmensuer C, Kilinc K. Antiapoptotic and protective effects of roscovitine on ischemia reperfusion injury of the rat liver. Liver Int 2003; 23:300-7; PMID:12895271; http://dx.doi.org/10.1034/j. 1600-0676.2003.00842.x
32. Lew J. CDK5: A new lead to survival. Cell Cycle 2013; 12:1981-2; PMID:23759582; http://dx.doi.org/10.4161/cc.25304
33. Contreras-Vallejos E, Utreras E, Gonzalez-Billault C. Going out of the brain: non-nervous system physiological and pathological functions of Cdk5. Cell Signal 2012; 24:44-52; PMID:21924349; http://dx.doi.org/10.1016/j.cellsig.2011. 08.022
34. de Matos AC, Camara NO, de Oliveira AF, Franco MF, Moura LA, Nishida S, Pereira AB, Pacheco-Silva A. Functional and morphologic evaluation of kidney proximal tubuli and correlation with renal allograft prognosis. Transplant international: official journal of the European Society for Organ Transplantation 2010; 23:493-9
35. Chibazakura T. Cyclin proteolysis and CDK inhibitors: two redundant pathways to maintain genome stability in mammalian cells. Cell Cycle 2004; 3:1243-5; PMID:15477761; http://dx.doi.org/10.4161/cc.3.10.1199
36. King RW, Deshaies RJ, Peters JM, Kirschner MW. How proteolysis drives the cell cycle. Science 1996; 274:1652-9; PMID:8939846; http://dx.doi.org/10.1126/ science.274.5293.1652
37. Landberg G, Nilsson K, Jirström K, Rydén L, Kitching R, Burger AM, Seth A. Cyclin I is expressed in human breast cancer and closely associated with VEGF and KDR expression. Breast Cancer Res Treat 2005; 89:313-6; PMID:15754132; http://dx.doi.org/10.1007/s10549-004-2230-y
38. Nakamura T, Sanokawa R, Sasaki YF, Ayusawa D, Oishi M, Mori N. Cyclin I: a new cyclin encoded by a gene isolated from human brain. Exp Cell Res 1995; 221:534-42; PMID:7493655; http://dx.doi.org/10.1006/excr.1995.1406