CDK5 Contributes to Neuronal Apoptosis via Promoting MEF2D Phosphorylation in Rat Model of Intracerebral Hemorrhage

Journal of Molecular Neuroscience

Volumn 56, Issue 1, 2015, Pages 48-59

  Ke, Kaifu ^a   Shen, Jiabing ^a   Song, Yan ^a   Cao, Maohong ^a   Lu, Hongjian ^b   Liu, Chun ^a   Shen, Jianhong ^a   Li, Aihong ^a   Huang, Jie ^a   Ni, Haidan ^a   Chen, Xiaomei ^c   Liu, Yonghua ^a,d  

^a NANTONG UNIVERSITY   (China)

^b The Second People's Hospital of Nantong   (China)

^c Chinese Academy of Sciences   (China)

^d NANTONG MEDICAL COLLEGE   (China)

Author keywords

Apoptosis; CDK5; Hemorrhage; MEF2D; Neurons

Indexed keywords

CDK5 PROTEIN, RAT; CYCLIN DEPENDENT KINASE 5; MEF2D PROTEIN, RAT; MYOCYTE ENHANCER FACTOR 2;

ANIMAL; APOPTOSIS; ASTROCYTE; BRAIN HEMORRHAGE; GENETICS; MALE; METABOLISM; NERVE CELL; PHOSPHORYLATION; PROTEIN PROCESSING; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; ASTROCYTES; CEREBRAL HEMORRHAGE; CYCLIN-DEPENDENT KINASE 5; MALE; MEF2 TRANSCRIPTION FACTORS; NEURONS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84939938661     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-014-0466-5     Document Type: Article

References (39)

1. Barros-Minones L, Martin-de-Saavedra D, Perez-Alvarez S, Orejana L, Suquia V, Goni-Allo B, Hervias I, Lopez MG, Jordan J, Aguirre N, Puerta E (2013) Inhibition of calpain-regulated p35/cdk5 plays a central role in sildenafil-induced protection against chemical hypoxia produced by malonate. Biochim Biophys Acta 1832(6):705–717
2. Bhattacharjee RN, Banks GC, Trotter KW, Lee HL, Archer TK (2001) Histone H1 phosphorylation by Cdk2 selectively modulates mouse mammary tumor virus transcription through chromatin remodeling. Mol Cell Biol 21(16):5417–5425
3. Crandall KM, Rost NS, Sheth KN (2011) Prognosis in intracerebral hemorrhage. Rev Neurol Dis 8(1–2):23–29
4. Dhavan R, Tsai LH (2001) A decade of CDK5. Nat Rev Mol Cell Biol 2(10):749–759
5. Falcone GJ, Biffi A, Devan WJ, Brouwers HB, Anderson CD, Valant V, Ayres AM, Schwab K, Rost NS, Goldstein JN, Viswanathan A, Greenberg SM, Selim M, Meschia JF, Brown DL, Worrall BB, Silliman SL, Tirschwell DL, Rosand J (2013) Burden of blood pressure-related alleles is associated with larger hematoma volume and worse outcome in intracerebral hemorrhage. Stroke 44(2):321–326
6. Giannoulias D, Patel FA, Holloway AC, Lye SJ, Tai HH, Challis JR (2002) Differential changes in 15-hydroxyprostaglandin dehydrogenase and prostaglandin H synthase (types I and II) in human pregnant myometrium. J Clin Endocrinol Metab 87(3):1345–1352
7. Gomes JA, Manno E (2013) New developments in the treatment of intracerebral hemorrhage. Neurol Clin 31(3):721–735
8. Gong X, Tang X, Wiedmann M, Wang X, Peng J, Zheng D, Blair LA, Marshall J, Mao Z (2003) Cdk5-mediated inhibition of the protective effects of transcription factor MEF2 in neurotoxicity-induced apoptosis. Neuron 38(1):33–46
9. Hua Y, Schallert T, Keep RF, Wu J, Hoff JT, Xi G (2002) Behavioral tests after intracerebral hemorrhage in the rat. Stroke 33(10):2478–2484
10. Hwang BY, Appelboom G, Ayer A, Kellner CP, Kotchetkov IS, Gigante PR, Haque R, Kellner M, Connolly ES (2011) Advances in neuroprotective strategies: potential therapies for intracerebral hemorrhage. Cerebrovasc Dis 31(3):211–222
11. Karabiyikoglu M, Hua Y, Keep RF, Ennis SR, Xi G (2004) Intracerebral hirudin injection attenuates ischemic damage and neurologic deficits without altering local cerebral blood flow. J Cereb Blood Flow Metab 24(2):159–166
12. Ke K, Li L, Rui Y, Zheng H, Tan X, Xu W, Cao J, Xu J, Cui G, Xu G, Cao M (2013) Increased expression of small heat shock protein alphaB-crystallin after intracerebral hemorrhage in adult rats. J Mol Neurosci 51(1):159–169
13. Kesavapany S, Amin N, Zheng YL, Nijhara R, Jaffe H, Sihag R, Gutkind JS, Takahashi S, Kulkarni A, Grant P, Pant HC (2004) p35/cyclin-dependent kinase 5 phosphorylation of ras guanine nucleotide releasing factor 2 (RasGRF2) mediates Rac-dependent extracellular signal-regulated kinase 1/2 activity, altering RasGRF2 and microtubule-associated protein 1b distribution in neurons. J Neurosci 24(18):4421–4431
14. Li M, Linseman DA, Allen MP, Meintzer MK, Wang X, Laessig T, Wierman ME, Heidenreich KA (2001) Myocyte enhancer factor 2A and 2D undergo phosphorylation and caspase-mediated degradation during apoptosis of rat cerebellar granule neurons. J Neurosci 21(17):6544–6552
15. Li BS, Zhang L, Takahashi S, Ma W, Jaffe H, Kulkarni AB, Pant HC (2002) Cyclin-dependent kinase 5 prevents neuronal apoptosis by negative regulation of c-Jun N-terminal kinase 3. EMBO J 21(3):324–333
16. Li BS, Ma W, Jaffe H, Zheng Y, Takahashi S, Zhang L, Kulkarni AB, Pant HC (2003) Cyclin-dependent kinase-5 is involved in neuregulin-dependent activation of phosphatidylinositol 3-kinase and Akt activity mediating neuronal survival. J Biol Chem 278(37):35702–35709
17. Lopes JP, Agostinho P (2011) Cdk5: multitasking between physiological and pathological conditions. Prog Neurobiol 94(1):49–63
18. Ma Y, Bao J, Zhao X, Shen H, Lv J, Ma S, Zhang X, Li Z, Wang S, Wang Q, Ji J (2013) Activated cyclin-dependent kinase 5 promotes microglial phagocytosis of fibrillar beta-amyloid by up-regulating lipoprotein lipase expression. Mol Cell Proteomics 12(10):2833–2844
19. Mao Z, Bonni A, Xia F, Nadal-Vicens M, Greenberg ME (1999) Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 286(5440):785–790
20. Nguyen MD, Boudreau M, Kriz J, Couillard-Despres S, Kaplan DR, Julien JP (2003) Cell cycle regulators in the neuronal death pathway of amyotrophic lateral sclerosis caused by mutant superoxide dismutase 1. J Neurosci 23(6):2131–2140
21. Nikolic M, Dudek H, Kwon YT, Ramos YF, Tsai LH (1996) The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev 10(7):816–825
22. O’Hare MJ, Kushwaha N, Zhang Y, Aleyasin H, Callaghan SM, Slack RS, Albert PR, Vincent I, Park DS (2005) Differential roles of nuclear and cytoplasmic cyclin-dependent kinase 5 in apoptotic and excitotoxic neuronal death. J Neurosci 25(39):8954–8966
23. Okamoto S, Li Z, Ju C, Scholzke MN, Mathews E, Cui J, Salvesen GS, Bossy-Wetzel E, Lipton SA (2002) Dominant-interfering forms of MEF2 generated by caspase cleavage contribute to NMDA-induced neuronal apoptosis. Proc Natl Acad Sci U S A 99(6):3974–3979
24. Otyepka M, Bartova I, Kriz Z, Koca J (2006) Different mechanisms of CDK5 and CDK2 activation as revealed by CDK5/p25 and CDK2/cyclin a dynamics. J Biol Chem 281(11):7271–7281
25. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402(6762):615–622
26. Rashidian J, Rousseaux MW, Venderova K, Qu D, Callaghan SM, Phillips M, Bland RJ, During MJ, Mao Z, Slack RS, Park DS (2009) Essential role of cytoplasmic cdk5 and Prx2 in multiple ischemic injury models, in vivo. J Neurosci 29(40):12497–12505
27. Reimann-Philipp U, Ovase R, Weigel PH, Grammas P (2001) Mechanisms of cell death in primary cortical neurons and PC12 cells. J Neurosci Res 64(6):654–660
28. Saito T, Onuki R, Fujita Y, Kusakawa G, Ishiguro K, Bibb JA, Kishimoto T, Hisanaga S (2003) Developmental regulation of the proteolysis of the p35 cyclin-dependent kinase 5 activator by phosphorylation. J Neurosci 23(4):1189–1197
29. Sharma P, Veeranna SM, Amin ND, Sihag RK, Grant P, Ahn N, Kulkarni AB, Pant HC (2002) Phosphorylation of MEK1 by cdk5/p35 down-regulates the mitogen-activated protein kinase pathway. J Biol Chem 277(1):528–534
30. Slevin M, Krupinski J (2009) Cyclin-dependent kinase-5 targeting for ischaemic stroke. Curr Opin Pharmacol 9(2):119–124
31. Sundaram JR, Poore CP, Sulaimee NH, Pareek T, Asad AB, Rajkumar R, Cheong WF, Wenk MR, Dawe GS, Chuang KH, Pant HC, Kesavapany S (2013) Specific inhibition of p25/Cdk5 activity by the Cdk5 inhibitory peptide reduces neurodegeneration in vivo. J Neurosci 33(1):334–343
32. Tang X, Wang X, Gong X, Tong M, Park D, Xia Z, Mao Z (2005) Cyclin-dependent kinase 5 mediates neurotoxin-induced degradation of the transcription factor myocyte enhancer factor 2. J Neurosci 25(19):4823–4834
33. Wu J, Yang S, Xi G, Song S, Fu G, Keep RF, Hua Y (2008) Microglial activation and brain injury after intracerebral hemorrhage. Acta Neurochir Suppl 105:59–65
34. Xue M, Del Bigio MR (2000) Intracerebral injection of autologous whole blood in rats: time course of inflammation and cell death. Neurosci Lett 283(3):230–232
35. Xue M, Fan Y, Liu S, Zygun DA, Demchuk A, Yong VW (2009) Contributions of multiple proteases to neurotoxicity in a mouse model of intracerebral haemorrhage. Brain 132(Pt 1):26–36
36. Yang S, Song S, Hua Y, Nakamura T, Keep RF, Xi G (2008) Effects of thrombin on neurogenesis after intracerebral hemorrhage. Stroke 39(7):2079–2084
37. Zhang J, Krishnamurthy PK, Johnson GV (2002) Cdk5 phosphorylates p53 and regulates its activity. J Neurochem 81(2):307–313
38. Zhou Y, Wang Y, Wang J, Anne Stetler R, Yang QW (2014) Inflammation in intracerebral hemorrhage: from mechanisms to clinical translation. Prog Neurobiol 115:25–44
39. Zhu J, Li W, Mao Z (2011) Cdk5: mediator of neuronal development, death and the response to DNA damage. Mech Ageing Dev 132(8–9):389–394