The transcription factor E2f1 modulates apoptosis of neurons

Journal of Neurochemistry

Volumn 75, Issue 1, 2000, Pages 91-100

  Hou, Sheng T ^b   Callaghan, Debbie ^a   Fournier, Marie Christine ^c   Hill, Irene ^c   Kang, Liping ^c   Massie, Bernard ^b   Morley, Paul ^c   Murray, Christine ^c   Rasquinha, Ingrid ^c   Slack, Ruth ^a   MacManus, John P ^c  

^a UNIVERSITY OF OTTAWA   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c Montreal Road Labs ^*

Author keywords

Apoptosis; Caspase; Cortical neurons; DNA fragmentation; E2F1; Replication deficient adenovirus

Indexed keywords

CASPASE 3; DNA FRAGMENT; STAUROSPORINE; TRANSCRIPTION FACTOR E2F;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL COUNT; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; CARRIER PROTEINS; CASPASE 3; CASPASES; CELL CYCLE PROTEINS; CELLS, CULTURED; CEREBRAL CORTEX; DNA FRAGMENTATION; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; E2F1 TRANSCRIPTION FACTOR; GENE EXPRESSION; IN SITU NICK-END LABELING; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STAUROSPORINE; TRANSCRIPTION FACTOR DP1; TRANSCRIPTION FACTORS; TRANSFECTION;

ADENOVIRIDAE; ANIMALIA; TRIXIS;

EID: 0034086552     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.0750091.x     Document Type: Article

References (67)

1. Acsadi G., Jani A., Massie B., Simoneau M., Holland P., Blaschuk K., and Karpati G. (1994) A differential efficiency of adenovirus-mediated in vivo gene transfer into skeletal muscle cells of different maturity. Hum. Mol. Genet. 3, 579-584.
2. Agah R., Kirshenbaum L. A., Abdellatif M., Truong L. D., Chakraborty S., Michael L. H., and Schneider M. D. (1997) Adenoviral delivery of E2F1 directs cell cycle reentry and p53-independent apoptosis in postmitotic adult myocardium in viva. J. Clin. Invest. 100, 2722-2728.
3. Almasan A., Yin Y., Kelly R. E., Lee E. Y. H. P., Bradley A., Li W., Bertino J., and Wahl G. M. (1995) Deficiency of retinoblastoma protein leads to inappropriate S-phase entry, activation of E2F-responsive genes, and apoptosis. Proc. Natl. Acad. Sci. USA 92, 5436-5440.
4. Bertrand R., Solary E., O'Connor P., Kohn K. W., and Pommier Y. (1994) Induction of a common pathway of apoptosis by staurosporine. Exp. Cell Res. 211, 314-321.
5. Brehm A., Miska E. A., McCance D. J., Reid J. L., Bannister A. J., and Kouzarides T. (1998) Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391, 597-601.
6. Cao L., Faha B., Dembski M., Tsai L. H., Harlow E., and Dyson N. (1992) Independent binding of the retinoblastoma protein and p107 to the transcription factor E2F. Nature 355, 176-179.
7. Corbeil H. B., Whyte P., and Branton P. E. (1995) Characterization of transcription factor E2F complexes during muscle and neuronal differentiation. Oncogene 11, 909-920.
8. Dagnino L., Fry C. J., Hartley S. M., Farnham P., Gallic B. L., and Phillips R. A. (1997) Expression patterns of the E2F family of transcription factors during mouse nervous system development. Mech. Dev. 66, 13-25.
9. DeGregori J. G., Leone G., Miron A., Kakoi L., and Nevins J. R. (1997) Distinct role for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. USA 94, 7245-7250.
10. Dirks P. B., Rutka J. T., Hubbard S. L., Mondai S., and Hamel P. A. (1998) The E2F-family proteins induce distinct cell cycle regulatory factors in p16-arrested, U343 astrocytoma cells. Oncogene 17, 867-876.
11. D'Mello S. R. (1998) Molecular regulation of neuronal apoptosis. Curr. Topics Dev. Biol. 39, 187-211.
12. Durham H. D., Lochmuller H., Jani A., Acsadi G., Massie B., and Karpati G. (1996) Toxicity of replication-defective adenoviral recombinants in dissociated cultures of nervous tissue. Exp. Neurol. 140, 14-20.
13. Dyson N. (1998) The regulation of E2F by pRB-family proteins. Genes Dev. 12, 2245-2262.
14. Easton R. M., Johnson E. M., and Creedon D. J. (1998) Analysis of events leading to neuronal death after infection with E1-deficient adenoviral vectors. Mol. Cell. Neurosci. 11, 334-347.
15. Field S. J., Tsai F. Y., Kuo F., Zubiaga A. M., Kaelin W. G., Livingston D. M., Orkin S. H., and Greenberg M. E. (1996) E2F1 functions in mice to promote apoptosis and suppress proliferation. Cell 85, 549-561.
16. Friedlander R. M. and Yuan J. (1998) ICE, neuronal apoptosis and neurodegeneration. Cell Death Differ. 5, 823-831.
17. Gavrieli Y., Sherman Y., and Ben-Sasson S. A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
18. Giovanni A., Wirtz-Brugger F., Keramaris E., Slack R., and Park D. S. (1999) Involvement of cell cycle elements, CDKs and E2F, in β-amyloid-induced neuronal death. J. Biol. Chem. 274, 19011-19016.
19. Gorman A. M., Orrenius S., and Ceccatelli S. (1998) Apoptosis in neuronal cells: role of caspases. Neuroreport 9, R49-R55.
20. Holmberg C., Helin K., Sehested M., and Karlstrom O. (1998) E2F-1-induced p53-independent apoptosis in transgenic mice. Oncogene 17, 143-155.
21. Hou S. T., Tu Y. H., Buchan A. M., Huang A. M., Preston E., Rasquinha I., Robertson G. S., and MacManus J. P. (1997) Increases in DNA lesions and the DNA damage indicator Gadd45 following transient cerebral ischemia. Biochem. Cell. Biol. 75, 383-392.
22. Hsieh J. K., Fredersdorf S., Kouzarides T., Martin K., and Lu X. (1997) E2F1-induced apoptosis requires DNA binding but not transactivation and is inhibited by the retinoblastoma protein through direct interaction. Genes Dev. 11, 1840-1852.
23. Huang Y., Ishiko T., Nakada S., Utsugisawa T., Kato T., and Yuan Z. M. (1997) Role for E2F in DNA damage-induced entry of cells into S phase. Cancer Res. 57, 3640-3643.
24. Hunt K. K., Deng J., Liu T. J., Wilson-Heiner, Swisher S. G., Clayman G., and Hung M. C. (1997) Adenovirus-mediated overexpression of the transcription factor E2F1 induces apoptosis in human breast and ovarian carcinoma cell lines and does not require p53. Cancer Res. 57, 4722-4726.
25. Jacks T., Fazeli A., Schmitt E. M., Bronson R. T., Goodell M. A., and Weinberg R. A. (1992) Effects of an Rb mutation in the mouse. Nature 359, 295-300.
26. Johnson D. G., Schwarz J. K., Cress W. D., and Nevins J. R. (1993) Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 36, 349-352.
27. Johnson M. D., Kinoshita Y., Xiang H., Ghatan S., and Morrison R. S. (1999) Contribution of p53-dependent caspase activation to neuronal cell death declines with neuronal maturation. J. Neurosci. 19, 2996-3006.
28. Kirshenbaum L. A., Abdellatif S., Chakraborty S., and Schneider M. D. (1996) Human E2F-1 reactivates cell cycle progression in ventricular myocytes and represses cardiac gene transcription. Dev. Biol. 179, 402-411.
29. Kowalik T. F., DeGregori J., Schwarz J. K., and Nevins J. R. (1995) E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 69, 2491-2500.
30. Kowalik T. F., DeGregori J., Leono G., Jakoi L., and Nevins J. (1998) E2F1-specific induction of apoptosis and p53 accumulation, which is blocked by Mdm2. Cell Growth Differ. 9, 113-118.
31. Kruman I., Bruce-Keller A. J., Bredesen D., Waeg G., and Mattson P. (1997) Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J. Neurosci. 17, 5089-5100.
32. Kruman I., Guo Q., and Mattson P. (1998) Calcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC12 cells. J. Neurosci. Res. 51, 293-308.
33. Lee E. Y. H. P., Chang C. Y., Hu N., Wang Y. C. J., Lai C. C., Herrup K., Lee W. H., and Bradley A. (1992) Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359, 388-394.
34. Lee J. M., Zipfel G. J., and Choi D. W. (1999) The changing landscape of ischemic brain injury mechanisms. Nature 399 (Suppl.), A7-A13.
35. Luo R. X., Postigo A. A., and Dean D. C. (1998) Rb interacts with histone deacetylase to repress transcription. Cell 92, 463-473.
36. MacLeod K. F., Hu Y., and Jacks T. (1996) Loss of Rb activates both p53-depedent and independent cell death pathways in the developing mouse nervous system. EMBO J. 15, 6178-6188.
37. MacManus J. P. and Linnik M. D. (1997) Gene expression induced by cerebral ischemia: an apoptotic perspective. J. Cereb. Blood Flow Metab. 17, 815-832.
38. MacManus J. P., Rasquinha I., Black M. A., Laferriere N. B., Monette R., Walker T., and Morley P. (1997) Glutamate-treated rat cortical neuronal cultures die in a way different from the classical apoptosis induced by staurosporine. Exp. Cell Res. 233, 310-320.
39. MacManus J. P., Koch C. J., Jian M., Walker T., and Zurakowski B. (1999) Decreased brain infarct following focal ischemia in mice lacking the transcription factor E2F1. Neuroreport 10, 2711-2714.
40. Magnaghi-Jaulin L., Groisman R., Naguibneva I., Robin P., Lorain S., LeVillain J. P., Troalen F., Trouche D., and Harel-Bellan A. (1998) Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391, 601-604.
41. Massie B., Mosser D. D., Koutroumanis M., Vitte-Mony I., Lamoureux L., Couture F., Paquet L., Guilbault C., Dionne J., Chahla D., Jolicoeur P., and Langelier Y. (1998) New adenovirus vectors for protein production and gene transfer. Cytotechnology 28, 53-64.
42. Morgenbesser S. D., Williams B. O., Jacks T., and DePinho R. A. (1994) p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature 371, 72-74.
43. Namura S., Zhu J., Fink K., Endres M., Srinivasan A., Tomaselli K. J., Yuan J., and Moskowitz M. A. (1998) Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J. Neurosci. 18, 3659-3668.
44. Nevins J. R. (1998) Towards an understanding of the functional complexity of the E2F and retinoblastoma families. Cell Growth Differ. 9, 585-593.
45. Nip J., Strom D. K., Fee B. E., Zambetti G., Cleveland J. L., and Hiebert S. W. (1997) E2F-1 cooperates with topoisomerase II inhibition and DNA damage to selectively augment p53-independent apoptosis. Mol Cell Biol. 17, 1049-1056.
46. Phillips A. C., Bates S., Ryan K. M., Helin K., and Vousden K. H. (1997) Induction of DNA synthesis and apoptosis are separable functions of E2F-1. Genes Dev. 11, 1853-1863.
47. Pierce A. M., Gimenez-Conti I. B., Schineider-Broussard R., Martinez L. A., Conti C. J., and Johnson D. G. (1998) Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc. Natl. Acad. Sci. USA 95, 8858-8863.
48. 2+ and reactive oxygen species in staurosporine-induced neuronal apoptosis. J. Neurochem. 68, 1679-1685.
49. Qin X. Q., Livingston D. M., Kaelin W. G., and Adams P. (1994) Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 91, 10918-10922.
50. Rudin C. M. and Thompson C. R. (1997) Apoptosis and disease: regulation and clinical relevance of programmed cell death. Annu. Rev. Med. 48, 267-281.
51. Shan B. and Lee W. H. (1994) Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 14, 8166-8173.
52. Shan B., Durfee T., and Lee W. H. (1996) Disruption of RB/E2F-1 interaction by single point mutations in E2F-1 enhances S-phase entry and apoptosis. Proc. Natl. Acad. Sci. USA 93, 679-684.
53. 50-values and cell survival. Ear. J. Clin. Chem. Clin. Biochem. 33, 813-823.
54. Slack R. S., Belliveau D. J., Rosenberg M., Atwal J., Lochmuller H., Aloyz R., Haghighi A., Lach B., Seth P., Cooper E., and Miller F. D. (1996) Adenovirus-mediated gene transfer of the tumor suppressor, p53, induces apoptosis in postmitotic neurons. J. Cell Biol. 135, 1085-1095.
55. Stanimirovic D. B., Ball R., and Durkin J. P. (1997) Stimulation of glutamate uptake and Na,K-ATPase activity in rat astrocytes exposed to ischemic-like insults. Glia 19, 123-134.
56. Taya Y. (1997) RB kinases and RB-binding proteins: new points of view. Trends Biochem. Sci. 22, 14-17.
57. Templeton D. J., Park S. H., Lanier L., and Weinberg R. A. (1991) Nonfunctional mutants of the retinoblastoma protein are characterized by defects in phosphorylation, viral oncoprotein association, and nuclear tethering. Proc. Natl. Acad. Sci. USA 88, 3033-3037.
58. Thompson C. B. (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456-1462.
59. Tsai K. Y., Hu Y., MacLeod K. F., Crowley D., Yamasaki L., and Jacks T. (1998) Mutation of E2F1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol. Cell 2, 293-304.
60. Tu Y., Hou S. T., Huang Z., Robertson G. S., and MacManus J. P. (1998) Increased Mdm2 expression in rat after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 18, 658-669.
61. Vigo E., Muller H., Prosperini E., Hateboer G., Cartwright P., Moroni M. C., and Helin K. (1999) CDC25A phosphatase is a target of E2F and is required for efficient E2F-induced S phase. Mol. Cell Biol. 19, 6379-6395.
62. Walker P. R. and Sikorska M. (1997) New aspects of the mechanism of DNA fragmentation in apoptosis. Biochem. Cell. Biol. 75, 287-299.
63. Wiesner D. A. and Dawson G. (1996) Staurosporine induces programmed cell death in embryonic neurons and activation of the ceramide pathway. J. Neurochem. 66, 1418-1425.
64. Wu X. and Levine A. J. (1994) p53 and E2F1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 91, 3602-3606.
65. Xiang H., Hochman D. W., Saya H., Fujiwara T., Schwartzkroin P. A., and Morrison R. S. (1996) Evidence for p53-mediated modulation of neuronal viability. J. Neurosci. 16, 6753-6765.
66. Yamasaki L., Jacks T., Bronson R., Goillot E., Harlow E., and Dyson N. J. (1996) Tumor induction and tissue atrophy in mice lacking E2F1. Cell 85, 537-548.
67. Young W. S. III (1992) in situ hybridization with oligodeoxyribonucleotide probes, in In Situ Hybridization, a Practical Approach (Wilkinson D. G., ed), pp. 33-44. IRL Press, Oxford.