Cell cycle molecules and vertebrate neuron death: E2F at the hub

Cell Death and Differentiation

Volumn 11, Issue 1, 2004, Pages 49-60

  Greene, L A ^a   Biswass, S C ^a   Liu, D X ^a  

^a Columbia Univ Coll of Phys/Surg ^*  (United States)

Author keywords

Cell cycle; Cyclin dependent kinases; Cyclins; E2F; Neuron death; Pocket proteins

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; BH3 PROTEIN; CASPASE; CYCLIN B; CYCLIN D1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN E; FLAVOPIRIDOL; PROTEIN BCL 2; PROTEIN C JUN; PROTEIN P16; PROTEIN P27; PROTEIN P53; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR FKHR;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CAENORHABDITIS ELEGANS; CANCER; CELL CULTURE; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; CLINICAL TRIAL; CORRELATION ANALYSIS; DEGENERATIVE DISEASE; DRUG DESIGN; ENZYME ACTIVITY; EXPERIMENTAL DESIGN; GENE ACTIVATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HUMAN; NERVE CELL NECROSIS; NERVOUS SYSTEM INJURY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE;

ANIMALS; APOPTOSIS; CELL CYCLE; CELL CYCLE PROTEINS; CELL DEATH; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; NEURONS; NUCLEAR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ANIMALIA; CAENORHABDITIS ELEGANS; VERTEBRATA;

EID: 1642433100     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401341     Document Type: Review

References (128)

1. Oppenheim RW (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci. 14: 453-501
2. Hamburger V (1992) History of the discovery of neuronal death in embryos. J. Neurobiol. 23: 1116-1123
3. Putcha GV and Johnson EM (2004) 'Men are but Worms:' neuronal cell dealth in C. elegans and vertebrates. Cell Death Differ. 11: 38-48
4. Bennet MR, Gibson WG and Lemon G (2002) Neuronal cell death, nerve growth factor and neurotrophic models: 50 years on. Auton. Neurosci. 95: 1-23
5. Lee R, Kermani P, Teng KK and Hempstead BL (2001) Regulation of cell survival by secreted proneurotrophins. Science 294: 1945-1948
6. Martin LJ (2001) Neuronal cell death in nervous system development, disease, and injury (review). Int. J. Mol. Med. 7: 455-478
7. Ham J, Eilers A, Whitfield J, Neame SJ and Shah B (2000) c-Jun and the transcriptional control of neuronal apoptosis. Biochem. Pharmacol. 60: 1015-1021
8. Martin DP, Schmidt RE, DiStefano PS, Lowry OH, Carter JG and Johnson Jr EM (1988) Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106: 829-844
9. Oppenheim RW, Prevette D, Tytell M and Homma S (1990) Naturally occurring and induced neuronal death in the chick embryo in vivo requires protein and RNA synthesis: evidence for the role of cell death genes. Dev. Biol. 138: 104-113
10. Tong L, Toliver-Kinsky T, Taglialatela G, Werrbach-Perez K, Wood T and Perez-Polo JR (1998) Signal transduction in neuronal death. J. Neurochem. 71: 447-459
11. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R and Johnson Jr EM (1994) Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J. Cell Biol. 127: 1717-1727
12. Miller FD, Pozniak CD and Walsh GS (2000) Neuronal life and death: an essential role for the p53 family. Cell Death Differ. 7: 880-888
13. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J and Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868
14. Vermeulen K, Berneman ZN and Van Bockstaele DR (2003) Cell cycle and apoptosis. Cell Prolif. 36: 165-175
15. Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M, Waters CM, Penn LZ and Hancock DC (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell 69: 119-128
16. Feddersen RM, Ehlenfeldt R, Yunis WS, Clark HB and Orr HT (1992) Disrupted cerebellar cortical development and progressive degeneration of Purkinje cells in SV40 T antigen transgenic mice. Neuron 9: 955-966
17. Ferrari G and Greene LA (1994) Proliferative inhibition by dominant-negative Ras rescues naive and neuronally differentiated PC12 cells from apoptotic death. EMBO J. 13: 5922-5928
18. Freeman RS, Estus S and Johnson Jr EM (1994) Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of cyclin D1 during programmed cell death. Neuron 12: 343-355
19. Heintz N (1993) Cell death and the cell cycle: a relationship between transformation and neurodegeneration? Trends Biochem. Sci. 18: 157-159
20. Herrup K and Busser JC (1995) The induction of multiple cell cycle events precedes target-related neuronal death. Development 121: 2385-2395
21. Rubin LL, Gatchalian CL, Rimon G and Brooks SF (1994) The molecular mechanisms of neuronal apoptosis. Curr. Opin. Neurobiol. 4: 696-702
22. Feddersen RM, Clark HB, Yunis WS and Orr HT (1995) In vivo viability of postmitotic Purkinje neurons requires pRb family member function. Mol. Cell. Neurosci. 6: 153-167
23. Farinelli SE and Greene LA (1996) Cell cycle blockers mimosine, ciclopirox, and deferoxamine prevent the death of PC12 cells and postmitotic sympathetic neurons after removal of trophic support. J. Neurosci. 16: 1150-1162
24. Pines J (1995) Cyclins and cyclin-dependent kinases: a biochemical view. Biochem. J. 308 (Part 3): 697-711
25. Vermeulen K, Van Bockstaele DR and Berneman ZN (2003) The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif. 36: 131-149
26. Sakai K, Suzuki K, Tanaka S and Koike T (1999) Up-regulation of cyclin D1 occurs in apoptosis of immature but not mature cerebellar granule neurons in culture. J. Neurosci. Res. 58: 396-406
27. Padmanabhan J, Park DS, Greene LA and Shelanski ML (1999) Role of cell cycle regulatory proteins in cerebellar granule neuron apoptosis. J. Neurosci. 19: 8747-8756
28. Martin-Romero FJ, Santiago-Josefat B, Correa-Bordes J, Gutierrez-Merino C and Fernandez-Salguero P (2000) Potassium-induced apoptosis in rat cerebellar granule cells involves cell-cycle blockade at the G1/S transition. J. Mol. Neurosci. 15: 155-165
29. Boutillier AL, Kienlen-Campard P and Loeffler JP (1999) Depolarization regulates cyclin D1 degradation and neuronal apoptosis: a hypothesis about the role of the ulbiquitin/proteasome signalling pathway. Eur. J. Neurosci. 11: 441-448
30. Giardina SF, Cheung NS, Reid MT and Beart PM (1998) Kainate-induced apoptosis in cultured murine cerebellar granule cells elevates expression of the cell cycle gene cyclin D1. J. Neurochem. 71: 1325-1328
31. Copani A, Condorelli F, Caruso A, Vancheri C, Sala A, Giuffrida Stella AM, Canonico PL, Nicoletti F and Sortino MA (1999) Mitotic signaling by beta-amyloid causes neuronal death. FASEB J. 13: 2225-2234
32. Gill JS and Windebank AJ (1998) Cisplatin-induced apoptosis in rat dorsal root ganglion neurons is associated with attempted entry into the cell cycle. J. Clin. Invest. 101: 2842-2850
33. Kranenburg O, van der Eb AJ and Zantema A (11996) Cyclin D1 is an essential mediator of apoptotic neuronal cell death. EMBO J. 15: 46-54
34. Di Giovanni S, Knoblach SM, Brandoli C, Aden SA, Hoffman EP and Faden AI (2003) Gene profiling in spinal cord injury shows role of cell cycle in neuronal death. Ann. Neurol. 53: 454-468
35. Fischer SJ, McDonald ES, Gross L and Windebank AJ (2001) Alterations in cell cycle regulation underlie cisplatin induced apoptosis of dorsal root ganglion neurons in vivo. Neurobiol. Dis. 8: 1027-1035
36. Guegan C, Levy V, David JP, Ajchenbaum-Cymbalista F and Sola B (1997) c-Jun and cyclin D1 proteins as mediators of neuronal death after a focal ischaemic insult. Neuroreport 8: 1003-1007
37. Osuga H, Osuga S, Wang F, Fetni R, Hogan MJ, Slack RS, Hakim AM, Ikeda JE and Park DS (2000) Cyclin-dependent kinases as a therapeutic target for stroke. Proc. Natl. Acad. Sci. USA 97: 10254-10259
38. Timsit S, Rivera S, Ouaghi P, Guischard F, Tremblay E, Ben-Ari Y and Khrestchatisky M (1999) Increased cyclin D1 in vulnerable neurons in the hippocampus after ischaemia and epilepsy: a modulator of in vivo programmed cell death? Eur. J. Neurosci. 11: 263-278
39. Kuroiwa S, Katai N, Shibuki H, Kurokawa T, Umihira J, Nikaido T, Kametani K and Yoshimura N (1998) Expression of cell cycle-related genes in dying cells in retinal ischemic injury. Invest. Ophthalmol. Vis. Sci. 39: 610-617
40. Sakurai M, Hayashi T, Abe K, Itoyama Y, Tabayashi K and Rosenblum WI (2000) Cyclin D1 and Cdk4 protein induction in motor neurons after transient spinal cord ischemia in rabbits. Stroke 31: 200-207
41. Park DS, Obeidat A, Giovanni A and Greene LA (2000) Cell cycle regulators in neuronal death evoked by excitotoxic stress: implications for neurodegeneration and its treatment. Neurobiol. Aging 21: 771-781
42. Ino H and Chiba T (2001) Cyclin-dependent kinase 4 and cyclin D1 are required for excitotoxin-induced neuronal cell death in vivo. J. Neurosci. 21: 6086-6094
43. Nguyen MD, Boudreau M, Kriz J, Couillard-Despres S, Kaplan DR and Julien JP (2003) Cell cycle regulators in the neuronal death pathway of amyotrophic lateral sclerosis caused by mutant superoxide dismutase 1. J. Neurosci. 23: 2131-2140
44. Busser J, Geldmacher DS and Herrup K (1998) Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J. Neurosci. 18: 2801-2807
45. Ranganathan S and Bowser R (2003) Alterations in G(1) to S phase cell-cycle regulators during amyotrophic lateral sclerosis. Am. J. Pathol. 162: 823-835
46. Verdaguer E, Garcia-Jorda E, Canudas AM, Dominguez E, Jimenez A, Pubill D, Escubedo E, Pallas JC and Camins A (2002) Kainic acid-induced apoptosis in cerebellar granule neurons: an attempt at cell cycle re-entry. Neuroreport 13: 413-416
47. Nagy Z, Esiri MM, Cato AM and Smith AD (1997) Cell cycle markers in the hippocampus in Alzheimer's disease. Acta Neuropathol (Berl). 94: 6-15
48. Geng Y, Eaton EN, Picon M, Roberts JM, Lundberg AS, Gifford A, Sardet C and Weinberg RA (1996) Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene 12: 1173-1180
49. Shirvan A, Ziv I, Machlin T, Zilkha-Falb R, Melamed E and Barzilai A (1997) Two waves of cyclin B and proliferating cell nuclear antigen expression during dopamine-triggered neuronal apoptosis. J. Neurochem. 69: 539-549
50. Shirvan A, Ziv I, Barzilai A, Djaldeti R, Zilkh-Falb R, Michlin T and Melamed E (1997) Induction of mitosis-related genes during dopamine-triggered apoptosis in sympathetic neurons. J. Neural Transm. Suppl. 50: 67-78
51. Frade JM (2000) Unscheduled re-entry into the cell cycle induced by NGF precedes cell death in nascent retinal neurones. J. Cell Sci. 113 (Part 7): 1139-1148
52. Husseman JW, Nochlin D and Vincent I (2000) Mitotic activation: a convergent mechanism for a cohort of neurodegenerative diseases. Neurobiol. Aging 21: 815-828
53. Vincent I, Jicha G, Rosado M and Dickson DW (1997) Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimers disease brain. J. Neurosci. 17: 3588-3598
54. Vincent I, Bu B, Hudson K, Husseman J, Nochlin D and Jin L (2001) Constitutive Cdc25B tyrosine phosphatase activity in adult brain neurons with M phase-type alterations in Alzheimers disease. Neuroscience 105: 639-650
55. Yang Y, Mufson EJ and Herrup K (2003) Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J. Neurosci. 23: 2557-2563
56. Smith MZ, Nagy Z and Esiri MM (1999) Cell cycle-related protein expression in vascular dementia and Alzheimer's disease. Neurosci. Lett. 271: 45-48
57. Nagy Z, Esiri MM and Smith AD (1998) The cell division cycle and the pathophysiology of Alzheimer's disease. Neuroscience 87: 731-739
58. Arendt T, Holzer M, Stobe A, Gartner U, Luth HJ, Bruckner MK and Ueberham U (2000) Activated mitogenic signaling induces a process of dedifferentiation in Alzheimer's disease that eventually results in cell death. Ann. N. Y. Acad. Sci. 920: 249-255
59. Vincent I, Zheng JH, Dickson DW, Kress Y and Davies P (1998) Mitotic phosphoepitopes precede paired helical filaments in Alzheimer's disease. Neurobiol. Aging. 19: 287-296
60. Yang Y, Geldmacher DS and Herrup K (2001) DNA replication precedes neuronal cell death in Alzheimer's disease. J. Neurosci. 21: 2661-2668
61. Wu Q, Combs C, Cannady SB, Geldmacher DS and Herrup K (2000) Beta-amyloid activated microglia induce cell cycling and cell death in cultured cortical neurons. Neurobiol. Aging. 21: 797-806
62. Smith DS and Tsai LH (2002) Cdk5 behind the wheel: a role in trafficking and transport? Trends Cell Biol. 12: 28-36
63. Greene LA and Tischler AS (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocyloma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA 73: 2424-2428
64. Angelastro JM, Klimaschewski L, Tang S, Vitolo OV, Weissman TA, Donlin LT, Shelanski ML and Greene LA (2000) Identification of diverse nerve growth factor-regulated genes by serial analysis of gene expression (SAGE) profiling. Proc. Natl. Acad. Sci. USA 97: 10424-10429
65. Giovanni A, Wirtz-Brugger F, Keramaris E, Slack R and Park DS (1999) Involvement of cell cycle elements, cyclin-dependent kinases, pRb, and E2F × DP, in B-amyloid-induced neuronal death. J. Biol. Chem. 274: 19011-19016
66. McShea A, Harris PL, Webster KR, Wahl AF and Smith MA (1997) Abnormal expression of the cell cycle regulators P16 and CDK4 in Alzheimer's disease. Am. J. Pathol. 150: 1933-1939
67. Park DS, Morris EJ, Padmanabhan J, Shelanski ML, Geller HM and Greene LA (1998) Cyclin-dependent kinases participate in death of neurons evoked by DNA-damaging agents. J. Cell Biol. 143: 457-467
68. Trinh E, Boutillier AL and Loeffler JP (2001) Regulation of the retinoblastoma-dependent Mdm2 and E2F-1 signaling pathways during neuronal apoptosis. Mol. Cell. Neurosci. 17: 342-353
69. Tan AR and Swain SM (2002) Review of flavopiridol, a cyclin-dependent kinase inhibitor, as breast cancer therapy. Semin. Oncol. 29: 77-85
70. Park DS, Farinelli SE and Greene LA (1996) Inhibitors of cyclin-dependent kinases promote survival of post-mitotic neuronally differentiated PC12 cells and sympathetic neurons. J. Biol. Chem. 271: 8161-8169
71. Courtney MJ and Coffey ET (1999) The mechanism of Ara-C-induced apoptosis of differentiating cerebellar granule neurons. Eur. J. Neurosci. 11: 1073-1084
72. Park DS, Morris EJ, Greene LA and Geller HM (1997) G1/S cell cycle blockers and inhibitors of cyclin-dependent kinases suppress camptothecin-induced neuronal apoptosis. J. Neurosci. 17: 1256-1270
73. Rideout HJ, Wang Q, Park DS and Stefanis L (2003) Cyclin-dependent kinase activity is required for apoptotic death but not inclusion formation in cortical neurons after proteasomal inhibition. J. Neurosci. 23: 1237-1245
74. Dai Y and Grant S (2003) Cyclin-dependent kinase inhibitors. Curr. Opin. Pharmacol. 3: 362-370
75. Fischer PM and Gianella-Borradori A (2003) CDK inhibitors in clinical development for the treatment of cancer. Expert Opin. Investig. Drugs. 12: 955-970
76. Harper JW (1997) Cyclin dependent kinase inhibitors. Cancer Surv. 29: 91-107
77. Chellappan SP, Giordano A and Fisher PB (1998) Role of cyclin-dependent kinases and their inhibitors in cellular differentiation and development. Curr. Top. Microbiol. Immunol. 227: 57-103
78. Park DS, Levine B, Ferrari G and Greene LA (1997) Cyclin dependent kinase inhibitors and dominant negative cyclin dependent kinase 4 and 6 promote survival of NGF-deprived sympathetic neurons. J. Neurosci. 17: 8975-8983
79. Katchanov J, Harms C, Gertz K, Hauck L, Waeber C, Hirt L, Priller J, von Harsdorf R, Bruck W, Hortnagl H, Dimagl U, Bhide PG and Endres M (2001) Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal cell death. J. Neurosci, 21: 5045-5053
80. Taylor WR, Schonthal AH, Galante J and Stark GR (2001) p130/E2F4 binds to and represses the cdc2 promoter in response to p53. J. Biol. Chem. 276: 1998-2006
81. Athanasiou MC, Yunis W, Coleman N, Ehlenfeldt R, Clark HB, Orr HT and Feddersen RM (1998) The transcription factor E2F-1 in SV40 T antigen-induced cerebellar Purkinje cell degeneration. Mol. Cell. Neurosci. 12: 16-28
82. El-Khodor BF, Oo TF, Kholodilov N and Burke RE (2003) Ectopic expression of cell cycle markers in models of induced programmed cell death in dopamine neurons of the rat substantia nigra pars compacta. Exp. Neurol. 179: 17-27
83. Konishi Y, Lehtinen M, Donovan N and Bonni A (2002) Cdc2 phosphorylation of BAD links the cell cycle to the cell death machinery. Mol. Cell 9: 1005-1016
84. Konishi Y and Bonni A (2003) The E2F-Cdc2 cell-cycle pathway specifically mediates activity deprivation-induced apoptosis of postmitotic neurons. J. Neurosci. 23: 1649-1658
85. Dranovsky A, Vincent I, Gregori L, Schwarzman A, Colflesh D, Enghild J, Strittmatter W, Davies P and Goldgaber D (2001) Cdc2 phosphorylation of nucleolin demarcates mitotic stages and Alzheimer's disease pathology. Neurobiol. Aging 22: 517-528
86. Rehen SK, Cid M, Fragel-Madeira L and Linden R (2002) Differential effects of cyclin-dependent kinase blockers upon cell death in the developing retina. Brain Res. 947: 78-83
87. Bossenmeyer-Pourie C, Chihab R, Schroeder H and Daval JL (1999) Transient hypoxia may lead to neuronal proliferation in the developing mammalian brain: from apoptosis to cell cycle completion. Neuroscience 91: 221-231
88. Maas Jr JW, Horstmann S, Borasio GD, Anneser JM, Shooter EM and Kahle PJ (1998) Apoptosis of central and peripheral neurons can be prevented with cyclin-dependent kinase/mitogen-activated protein kinase inhibitors. J. Neurochem. 70: 1401-1410
89. Bain J, McLauchlan H, Elliott M and Cohen P (2003) The specificities of protein kinase inhibitors: an update. Biochem. J. 371: 199-204
90. Zindy F, Cunningham JJ, Sherr CJ, Jogal S, Smeyne RJ and Roussel MF (1999) Postnatal neuronal proliferation in mice lacking Ink4d and Kip1 inhibitors of cyclin-dependent kinases. Proc. Natl. Acad. Sci. USA 96: 13462-13467
91. Stevaux O and Dyson NJ (2002) A revised picture of the E2F transcriptional network and RB function. Curr. Opin. Cell. Biol. 14: 684-691
92. Park DS, Morris EJ, Bremner R, Keramaris E, Padmanabhan J, Rosenbaum M, Shelanski ML, Geller HM and Greene LA (2000) Involvement of retinoblastoma family members and E2F/DP complexes in the death of neurons evoked by DNA damage. J. Neurosci. 20: 3104-3114
93. Jordan-Sciutto KL, Malaiyandi LM and Bowser R (2002) Altered distribution of cell cycle transcriptional regulators during Alzheimer disease. J. Neuropathol. Exp. Neurol. 61: 358-367
94. Liu DX and Greene LA (2001) Regulation of neuronal survival and death by E2F-dependent gene repression and derepression. Neuron 32: 425-438
95. Ferguson KL and Slack RS (2001) The Rb pathway in neurogenesis. Neuroreport 12: A55-A62
96. Ferguson KL, Vanderluit JL, Hebert JM, McIntosh WC, Tibbo E, MacLaurin JG, Park DS, Wallace VA, Vooijs M, McConnell SK and Slack RS (2002) Telencephalon-specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J. 21: 3337-3346
97. MacPherson D, Sage J, Crowley D, Trumpp A, Bronson RT and Jacks T (2003) Conditional mutation of Rb causes cell cycle defects without apoptosis in the central nervous system. Mol. Cell. Biol. 23: 1044-1053
98. Baldi A, Esposito V, De Luca A, Fu Y, Meoli I, Giordano GG, Caputi M, Baldi F and Giordano A (1997) Differential expression of Rb2/p130 and p107 in normal human tissues and in primary lung cancer. Clin. Cancer Res. 3: 1691-1697
99. Jiang Z, Zacksenhaus E, Gallie BL and Phillips RA (1997) The retinoblastoma gene family is differentially expressed during embryogenesis. Oncogene 14: 1789-1797
100. LeCouter JE, Kablar B, Hardy WR, Ying C, Megeney LA, May LL and Rudnicki MA (1998) Strain-dependent myeloid hyperplasia, growth deficiency, and accelerated cell cycle in mice lacking the Rb-related p107 gene. Mol. Cell. Biol. 18: 7455-7465
101. Marino S, Hoogervoorst D, Brandner S and Berns A (2003) Rb and p107 are required for normal cerebellar development and granule cell survival but not for Purkinje cell persistence. Development 130: 3359-3368
102. Kusek JC, Greene RM and Pisano MM (2001) Expression of the E2F and retinoblastoma families of proteins during neural differentiation. Brain Res. Bull. 54: 187-198
103. LeCouter JE, Kablar B, Whyte PF, Ying C and Rudnicki MA (1998) Strain-dependent embryonic lethality in mice lacking the retinoblastoma-related p130 gene. Development 125: 4669-4679
104. Hou ST, Cowan E, Walker T, Ohan N, Dove M, Rasqinha I and MacManus JP (2001) The transcription factor E2F1 promotes dopamine-evoked neuronal apoptosis by a mechanism independent of transcriptional activation. J. Neurochem. 78: 287-297
105. Boutillier AL, Trinh E and Loeffler JP (2003) Selective E2F-dependent gene transcription is controlled by histone deacetylase activity during neuronal apoptosis. J. Neurochem. 84: 814-828
106. Azuma-Hara M, Taniura H, Uetsuki T, Niinobe M and Yoshikawa K (1999) Regulation and deregulation of E2F1 in postmitotic neurons differentiated from embryonal carcinoma P19 cells. Exp. Cell Res. 251: 442-451
107. Hou ST, Cowan E, Dostanic S, Rasquinha I, Comas T, Morley P and MacManus JP (2001) Increased expression of the transcription factor E2F1 during dopamine-evoked, caspase-3-mediated apoptosis in rat cortical neurons. Neurosci. Lett. 306: 153-156
108. Kobayashi M, Taniura H and Yoshikawa K (2002) Ectopic expression of necdin induces differentiation of mouse neuroblastoma cells. J. Biol. Chem. 277: 42128-42135
109. O'Hare MJ, Hou ST, Morris EJ, Cregan SP, Xu Q, Slack RS and Park DS (2000) Induction and modulation of cerebellar granule neuron death by E2F-1. J. Biol. Chem. 275: 25358-25364
110. Motonaga K, Itoh M, Hirayama A, Hirano S, Becker LE, Goto Y and Takashima S (2001) Up-regulation of E2F-1 in Down's syndrome brain exhibiting neuropathological features of Alzheimer-type dementia. Brain Res. 905: 250-253
111. Gendron TF, Mealing GA, Paris J, Lou A, Edwards A, Hou ST, MacManus JP, Hakim AM and Morley P (2001) Attenuation of neurotoxicity in cortical cultures and hippocampal slices from E2F1 knockout mice. J. Neurochem. 78: 316-324
112. Giovanni A, Keramaris E, Morris EJ, Hou ST, O'Hare M, Dyson N, Robertson GS, Slack RS and Park DS (2000) E2F1 mediates death of B-amyloid-treated cortical neurons in a manner independent of p53 and dependent on Bax and caspase 3. J. Biol. Chem. 275: 11553-11560
113. Hou ST, Callaghan D, Fournier MC, Hill I, Kang L, Massie B, Morley P, Murray C, Rasquinha I, Slack R and MacManus JP (2000) The transcription factor E2F1 modulates apoptosis of neurons. J. Neurochem. 75: 91-100
114. Ghahremani MH, Keramaris E, Shree T, Xia Z, Davis RJ, Flavell R, Slack RS and Park DS (2002) Interaction of the c-Jun/JNK pathway and cyclin-dependent kinases in death of embryonic cortical neurons evoked by DNA damage. J. Biol. Chem. 277: 35586-35596
115. Oh IH and Reddy EP (1999) The myb gene family in cell growth, differentiation and apoptosis. Oncogene 18: 3017-3033
116. Catchpole S, Tavner F, Le Cam L, Sardet C and Watson RJ (2002) A B-myb promoter corepressor site facilitates in vivo occupation of the adjacent E2F site by p107 × E2F and p130 × E2F complexes. J. Biol. Chem. 277: 39015-39024
117. Whitfield J, Neame SJ, Paquet L, Bernard O and Ham J (2001) Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29: 629-643
118. Putcha GV, Moulder KL, Golden JP, Bouillet P, Adams JA, Strasser A and Johnson EM (2001) Induction of BIM, a proapoptotic BH3-only BCL-2 family member, is critical for neuronal apoptosis. Neuron 29: 615-628
119. Biswas SC and Greene LA (2002) Nerve growth factor (NGF) down-regulates the Bcl-2 homology 3 (BH3) domain-only protein Bim and suppresses its proapoptotic activity by phosphorylation. J. Biol. Chem. 277: 49511-49516
120. Persengiev SP, Kondova II and Kilpatrick DL (1999) E2F4 actively promotes the initiation and maintenance of nerve growth factor-induced cell differentiation. Mol. Cell. Biol. 19: 6048-6056
121. Gilley J, Coffer PJ and Ham J (2003) FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J. Cell Biol. 162: 613-622
122. Herrup K and Arendt T (2002) Re-expression of cell cycle proteins induces neuronal cell death during Alzheimer's disease. J. Alzheimers Dis. 4: 243-247
123. Copani A, Sortino MA, Nicoletti F and Giuffrida SA (2002) Alzheimer's disease research enters a 'new cycle': how significant? Neurochem. Res. 27:173-176
124. Liu DX and Greene LA (2001) Neuronal apoptosis at the G1/S cell cycle checkpoint. Cell Tissue Res. 305: 217-228
125. McShea A, Wahl AF and Smith MA (1999) Re-entry into the cell cycle: a mechanism for neurodegeneration in Alzheimer disease. Med. Hypotheses 52: 525-527
126. O'Hare M, Wang F and Park DS (2002) Cyclin-dependent kinases as potential targets to improve stroke outcome. Pharmacol Ther. 93: 135-143
127. Raina AK, Zhu X, Rottkamp CA, Monteiro M, Takeda A and Smith MA (2000) Cyclin' toward dementia: cell cycle abnormalities and abortive oncogenesis in Alzheimer disease. J. Neurosci. Res. 61: 128-133
128. Huwe A, Mazitschek R and Giannis A (2003) Small molecules as inhibitors of cyclin-dependent kinases. Angew. Chem. Int. Ed. Eng. 42: 2122-2138