Effects of Cyclin-Dependent Kinase-5 Activity on Apoptosis and Tau Phosphorylation in Immortalized Mouse Brain Cortical Cells

Journal of Neuroscience Research

Volumn 76, Issue 1, 2004, Pages 110-120

  Shelton, Shirley B ^a   Krishnamurthy, Pavan ^a   Johnson, Gail V W ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Alzheimer's disease; Apoptosis; Caspase 3; CDK5; CN1.4; PARP; Tau

Indexed keywords

CASPASE 3; CYCLIN DEPENDENT KINASE 5; DOXYCYCLINE; EPITOPE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHF 1 PROTEIN; PROTEIN P25; TAU 1 PROTEIN; TAU PROTEIN; THAPSIGARGIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CELL IMMORTALIZATION; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME DEGRADATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; MODEL; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBODIES, MONOCLONAL; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CASPASES; CELL LINE; CEREBRAL CORTEX; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASES; DOXYCYCLINE; ENZYME ACTIVATION; ENZYME ACTIVATORS; EPITOPES; HUMANS; MICE; NERVE TISSUE PROTEINS; NEURONS; PHOSPHORYLATION; PLASMIDS; TAU PROTEINS; THAPSIGARGIN; TRANSFECTION;

EID: 1842532304     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20051     Document Type: Article

References (73)

1. Agarwal-Mawal A, Paudel HK. 2001. Neuronal Cdc2-like protein kinase (Cdk5/p25) is associated with protein phosphatase 1 and phosphorylates inhibitor-2. J Biol Chem 276:23712-23718.
2. Ahlijanian MK, Barrezueta NX, Williams RD, Jakowski A, Kowsz KP, McCarthy S, Coskran T, Carlo A, Seymour PA, Burkhardt JE, Nelson RB, McNeish JD. 2000. Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc Natl Acad Sci USA 97:2910-2915.
3. Ahuja HS, Zhu Y, Zakeri Z. 1997. Association of cyclin-dependent kinase 5 and its activator p35 with apoptotic cell death. Dev. Genet 21:258-267.
4. Angelo M, Plattner F, Irvine EE, Giese KP. 2003. Improved reversal learning and altered fear conditioning in transgenic mice with regionally restricted p25 expression. Eur J Neurosci 18:423-431.
5. Bettany JT, Wolowacz RG. 1998. Tetracycline derivatives Induce apoptosis selectively in cultured monocytes and macrophages but not in mesenchymal cells. Adv Dent Res 12:136-143.
6. Bian F, Nath R, Sobocinski G, Booher RN, Lipinski WJ, Callahan MJ, Pack A, Wang KK, Walker LC. 2002. Axonopathy, tau abnormalities, and dyskinesia, but no neurofibrillary tangles in p25-transgenic mice. J Comp Neurol 446:257-266.
7. Bibb JA, Nishi A, O'Callaghan JP, Ule J, Lan M, Snyder GL, Horiuchi A, Saito T, Hisanaga S, Czernik AJ, Naim AC, Greengard P. 2001. Phosphorylation of protein phosphatase inhibitor-1 by Cdk5. J Biol Chem 276:14490-14497.
8. Bibb JA, Snyder GL, Nishi A, Yan Z, Meijer L, Fienberg AA, Tsai LH, Kwon YT, Girault JA, Czernik AJ, Huganir RL, Hemmings HC, Jr., Nairn AC, Greengard P. 1999. Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature 402:669-671.
9. Bongarzone ER, Foster L, Byravan S, Casaccia-Bonnefil P, Schonmann V, Campagnoni AT. 1998. Two neuronal cell lines expressing the myelin basic protein gene display differences in their in vitro survival and in their response to glia. J Neurosci Res 54:309-319.
10. Carmel G, Mager EM, Binder LI, Kuret J. 1996. The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J Biol Chem 271:32789-32795.
11. Davis PK, Dudek SM, Johnson GV. 1997. Select alterations in protein kinases and phosphatases during apoptosis of differentiated PC12 cells. J Neurochem 68:2338-2347.
12. Delacourte A, Buec L. 1997. Normal and pathological Tau proteins as factors for microtubule assembly. Int Rev Cytol 171:167-224.
13. Dhavan R, Tsai LH. 2001. A decade of CDK5. Nat Rev Mol Cell Biol 2:749-759.
14. Fife RS, Sledge GW Jr, Roth BJ, Proctor C. 1998. Effects of doxycycline on human prostate cancer cells in vitro. Cancer Lett 127:37-41.
15. Fu AK, Fu WY, Cheung J, Tsim KW, Ip FC, Wang JH, Ip NY. 2001. Cdk5 is involved in neuregulin-induced AChR expression at the neuro-muscular junction. Nat Neurosci 4:374-381.
16. Gong CX, Grundke-Iqbal I, Damuni Z, Iqbal K. 1994. Dephosphorylation of microtubule-associated protein tau by protein phosphatase-1 and -2C and its implication in Alzheimer disease. FEBS Lett 341:94-98.
17. Gong X, Tang X, Wiedntann 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 38:33-46.
18. Gustke N, Steiner B, Mandelkow EM, Biernat J, Meyer HE, Goedert M, Mandelkow E. 1992. The Alzheimer-like phosphorylation of tau protein reduces microtubule binding and involves Ser-Pro and Thr-Pro motifs. FEBS Lett 307:199-205.
19. Hallows JL, Chen K, DePinho RA, Vincent I. 2003. Decreased cyclin-dependent kinase 5 (cdk5) activity is accompanied by redistribution of cdk5 and cytoskeletal protein, and increased cytoskeletal protein phosphorylation in p35 null mice. J Neurosci 23:10633-10644.
20. Hamdane M, Sambo AV, Delobel P, Begard S, Violleau A, Delacourte A, Bertrand P, Benavides J, Buee L. 2003. Mitotic-like Tau phosphorylation by p25/Cdk5 kinase complex. J Biol Chem. 278:34026-34034.
21. Harriman JF, Liu XL, Aleo MD, Machaca K, Schnellmann RG. 2002. Endoplasmic reticulum Ca(2+) signaling and calpains mediate renal cell death. Cell Death Differ 9:734-741.
22. Hasegawa M, Crowther RA, Jakes R, Goedert M. 1997. Alzheimer-like changes in microtubule-associated protein Tau induced by sulfated glycosaminoglycans. Inhibition of microtubule binding, stimulation of phosphorylation, and filament assembly depend on the degree of sulfation. J Biol Chem 272:33118-33124.
23. Hashiguchi M, Saito T, Hisanaga S, Hashiguchi T. 2002. Truncation of CDK5 activator p35 induces intensive phosphorylation of Ser202/ Thr205 of human tau. J Biol Chem 277:44525-44530.
24. Hellmich MR, Pant HC, Wada E, Battey JF. 1992. Neuronal cdc2-like kinase: a cdc2-related protein kinase with predominantly neuronal expression. Proc Natl Acad Sci USA 89:10867-10871.
25. Henchcliffe C, Burke RE. 1997. Increased expression of cyclin-dependent kinase 5 in induced apoptotic neuron death in rat substantia nigra. Neurosci Lett 230:41-44.
26. Huang KX, Paudel HK. 2000. Ser67-phosphorylated inhibitor 1 is a potent protein phosphatase 1 inhibitor. Proc Natl Acad Sci USA 97:5824-5829.
27. Illenberger S, Zheng-Fischhofer Q, Preuss U, Starner K, Baumann K, Trinczek B, Biernat J, Godemann R, Mandelkow EM, Mandelkow E. 1998, The endogenous and cell cycle-dependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease. Mol Biol Cell 9:1495-1512.
28. Ishiguro K, Takamatsu M, Tomizawa K, Omori A, Takahashi M, Arioka M, Uchida T, Imahori K. 1992. Tau protein kinase I converts normal tau protein into A68-like component of paired helical filaments. J Biol Chem 267:10897-10901.
29. Iwasaki H, Inoue H, Mitsuke Y, Badran A, Ikegaya S, Ueda T. 2002. Doxycycline induces apoptosis by way of caspase-3 activation with inhibition of matrix metalloproteinase in human T-lymphoblastic leukemia CCRF-CEM cells. J Lab Clin Med 140:382-386.
30. Johnson GV, Seubert P, Cox TM, Motter R, Brown JP, Galasko D. 1997. The tau protein in human cerebrospinal fluid in Alzheimer's disease consists of proteolytically derived fragments. J Neurochem 68:430-433.
31. Kerokoski P, Suuronen T, Salminen A, Soininen H, Pirttila T. 2001. The levels of cdk5 and p35 proteins and tau phosphorylation are reduced during neuronal apoptosis. Biochem Biophys Res Commun 280:998-1002.
32. Kerokoski P, Suuronen T, Salminen A, Soininen H, Pirttila T. 2002. Cleavage of the cyclin-dependent kinase 5 activator p35 to p25 does not induce tau hyperphosphorylation. Biochem Biophys Res Commun 298:693-698.
33. Krishnamurthy PK, Mays JL, Bijur GN, Johnson GV. 2000. Transient oxidative stress in SH-SY5Y human neuroblastoma cells results in caspase dependent and independent cell death and tau proteolysis. J Neurosci Res 61:515-523.
34. Kusakawa G, Saito T, Onuki R, Ishiguro K, Kishimoto T, Hisanaga S. 2000. Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J Biol Chem 275:17166-17172.
35. Lee KY, Helbing CC, Choi KS, Johnston RN, Wang JH. 1997. Neuronal Cdc2-like kinase (Nclk) binds and phosphorylates the retinoblastoma protein. J Biol Chem 272:5622-5626.
36. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH. 2000. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405:360-364.
37. Lee MS, Tsai LH. 2003. Cdk5: one of the links between senile plaques and neurofibrillary tangles? J Alzheimers Dis 5:127-137.
38. Lew J, Huang QQ, Qi Z, Winkfein RJ, Aebersold R, Hunt T, Wang JH. 1994, A brain-specific activator of cyclin-dependent kinase 5. Nature 371:423-426.
39. Lew J, Winkfein RJ, Paudel HK, Wang JH. 1992. Brain proline-directed protein kinase is a neurofilament kinase which displays high sequence homology to p34cdc2. J Biol Chem 267:25922-25926.
40. Li BS, Ma W, Jaffe H, Zheng Y, Takahashi S, Zhang L, Kulkami AB, Pant HC. 2003. Cdk5 is involved in neuregulin-dependent activation of P1-3 kinase and Akt activity mediating neuronal survival. J Biol Chem 278:35702-35709.
41. 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 21:324-333.
42. Lindwall G, Cole RD. 1984. Phosphorylation affects the ability of tau protein to promote microtubule assembly. J Biol Chem 259:5301-5305.
43. Liu F, lqbal K, Grundke-Iqbal I, Gong CX. 2002. Involvement of aberrant glycosylation in phosphorylation of tau by cdk5 and GSK-3beta. FEBS Lett 530:209-214.
44. Lu T, Xu Y, Mericle MT, Mellgren RL. 2002. Participation of the conventional calpains in apoptosis. Biochim Biophys Acta 1590:16-26.
45. Lund ET, McKenna R, Evans DB, Sharma SK, Mathews WR. 2001. Characterization of the in vitro phosphorylation of human tau by tau protein kinase II (cdk5/p20) using mass spectrometry. J Neurochem 76:1221-1232.
46. Meikrantz W, Schlegel R. 1996. Suppression of apoptosis by dominant negative mutants of cyclin-dependent protein kinases. J Biol Chem 271:10205-10209.
47. Meyerson M, Enders GH, Wu CL, Su LK, Gorka C, Nelson C, Harlow E, Tsai LH. 1992. A family of human cdc2-related protein kinases. EMBO J 11:2909-2917.
48. Nath R, Davis M, Probert AW, Kupina NC, Ren X, Schielke GP, Wang KK. 2000. Processing of cdk5 activator p35 to its truncated form (p25) by calpain in acutely injured neuronal cells. Biochem Biophys Res Commun 274:16-21.
49. Neystat M, Rzhetskaya M, Oo TF, Kholodilov N, Yarygina O, Wilson A, El-Khodor BF, Burke RE. 2001. Expression of cyclin-dependent kinase 5 and its activator p35 in models of induced apoptotic death in neurons of the substantia nigra in vivo. J Neurochem 77:1611-1625.
50. Nguyen MD, Mushynski WE, Julien JP. 2002. Cycling at the interface between neurodevelopment and neurodegeneration. Cell Death Differ 9:1294-1306.
51. Noble W, Olm V, Takata K, Casey E, Mary O, Meyerson J, Gaynor K, LaFrancois J, Wang L, Kondo T, Davies P, Bums M, Veeranna, Nixon R, Dickson D, Matsuoka Y, Ahlijanian M, Lau LF, Duff K. 2003. Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38:555-565.
52. Nuydens R, Dispersyn G, de Jong M, van den Kieboom G, Borgers M, Geerts H. 1997. Aberrant tau phosphorylation and neurite retraction during NGF deprivation in PC12 cells. Biochem Biophys Res Commun 240:687-691.
53. Otvos L Jr, Feiner L, Lang E, Szendrei GI, Goedert M, Lee VM. 1994. Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. J Neurosci Res 39:669-673.
54. 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 402:615-622.
55. Patzke H, Maddineni U, Ayala R, Morabito M, Volker J, Dikkes P, Ahlijanian MK, Tsai LH. 2003. Partial rescue of the p35-/-brain phenotype by low expression of a neuronal-specific enolase p25 transgene. J Neurosci 23:2769-2778.
56. Patzke H, Tsai LH. 2002. Calpain-mediated cleavage of the cyclin-dependent kinase-5 activator p39 to p29. J Biol Chem 277:8054-8060.
57. Paudel HK, Lew J, Ali Z, Wang JH. 1993. Brain proline-directed protein kinase phosphorylates tau on sites that are abnormally phosphorylated in tau associated with Alzheimer's paired helical filaments. J Biol Chem 268:23512-23518.
58. Seubert P, Mawal-Dewan M, Barbour R, Jakes R, Goedert M, Johnson GV, Litersky JM, Schenk D, Lieberburg I, Trojanowski JQ, et al. 1995. Detection of phosphorylated Ser262 in fetal tau, adult tau, and paired helical filament tau. J Biol Chem 270:18917-18922.
59. Sohn J, Khaoustov VI, Xie Q, Chung CC, Krishnan B, Yoffe B. 2003. The effect of ursodeoxycholic acid on the survivin in thapsigargin-induced apoptosis. Cancer Lett 191:83-92.
60. Strathdee CA, McLeod MR, Hall JR. 1999. Efficient control of tetracycline-responsive gene expression from an autoregulated hidirectional expression vector. Gene 229:21-29.
61. Szendrei GI, Lee VM, Otvos L Jr. 1993. Recognition of the minimal epitope of monoclonal antibody Tau-1 depends upon the presence of a phosphate group but not its location. J Neurosci Res 34:243-249.
62. Takahashi S, Saito T, Hisanaga SI, Pant HC, Kulkami AB. 2003. Tau phosphorylation by cyclin-dependent kinase5/p39 during brain development reduces its affinity for microtubules. J Biol Chem 278:10506-10515.
63. Takashima A, Murayama M, Yasutake K, Takahashi H, Yokoyama M, Ishiguro K. 2001. Involvement of cyclin dependent kinase5 activator p25 on tau phosphorylation in mouse brain. Neurosci Lett 306:37-40.
64. Tang D, Yeung J, Lee KY, Matsushita M, Matsui H, Tomizasca K, Hatase O, Wang JH. 1995. An isoform of the neuronal cyclin-dependent kinase 5 (Cdk5) activator. J Biol Chem 270:26897-26903.
65. Thastrup O, Cullen PJ, Drobak BK, Hanley MR, Dawson AP. 1990. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci USA 87:2466-2470.
66. Tsai LH, Delalle I, Caviness VS Jr, Chae T, Harlow E. 1994. p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371:419-423.
67. Tsai LH, Takahashi T, Caviness VS Jr, Harlow E. 1993. Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 119:1029-1040.
68. Uchida T, Ishiguro K, Ohnuma J, Takamatsu M, Yonekura S, Imahori K. 1994. Precursor of cdk5 activator, the 23 kDa subunit of tau protein kinase II: its sequence and developmental change in brain. FEBS Lett 355:35-40.
69. Van den Haute C, Spittaels K, Van Dorpe J, Lasrado R, Vandezande K, Laenen I, Geerts H, Van Leuven F. 2001. Coexpression of human cdk5 and its activator p35 with human protein tau in neurons in brain of triple transgenic mice. Neurobiol Dis 8:32-44.
70. Weishaupt JH, Neusch C, Bahr M. 2003. Cyclin-dependent kinase 5 (CDK5) and neuronal cell death. Cell Tissue Res 312:1-8.
71. Zhang J, Krishnamurthy PK, Johnson GV. 2002a. Cdk5 phosphorylates p53 and regulates its activity. J Neurochem 81:307-313.
72. Zhang J, Luan CH, Chou KC, Johnson GV. 2002b. Identification of the N-terminal functional domains of Cdk5 by molecular truncation and computer modeling. Proteins 48:447-453.
73. Zhivotovsky B, Cedervall B, Jiang S, Nicotera P, Orrenius S. 1994. Involvement of Ca2+ in the formation of high molecular weight DNA fragments in thymocyte apoptosis. Biochem Biophys Res Commun 202:120-127.