Abstract
Transforming viral proteins such as E1A which force quiescent cells into S phase have two essential cellular target proteins, Rb and CBP/p300. Rb regulates the G1/S transition by controlling the transcription factor E2F. CBP/p300 is a transcriptional co-activator with intrinsic histone acetyl-transferase activity. This activity is regulated in a cell cycle dependent manner and shows a peak at the G1/S transition, suggesting a function for CBP/p300 in this crucial step of the cell cycle. Here, we have artificially modulated CBP/p300 levels in individual cells through microinjection of specific antibodies and expression vectors. We show that CBP/p300 is required for cell proliferation and has an essential function during the G1/S transition. Using the same microinjection system and GFP-reporter vectors, we demonstrate that CBP/p300 is essential for the activity of E2F, a transcription factor that controls the G1/S transition. In addition, our results suggest that CBP HAT activity is required both for the G1/S transition and for E2F activity. Thus CBP/p300 seems to be a versatile protein involved in opposing cellular processes, which raises the question of how its multiple activities are regulated.
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References
Ait-Si-Ali S, Ramirez S, Barre FX, Dkhissi F, Magnaghi-Jaulin L, Girault JA, Robin P, Knibiehler M, Pritchard LL, Ducommun B, Trouche D and Harel-Bellan A . 1998a Nature 396: 184–186
Ait-Si-Ali S, Ramirez S, Robin P, Trouche D and Harel-Bellan A . 1998b Nucl Acid Res 26: 3869–3870
Arany Z, Newsome D, Oldread E, Livingston DM and Eckner R . 1995 Nature 374: 81–84
Bannister AJ and Kouzarides T . 1996 Nature 384: 641–643
Bennett JD, Farlie PG and Watson RJ . 1996 Oncogene 13: 1073–1082
Bernards R . 1997 Biochem Biophys Acta 1333: 33–40
Brehm A, Miska EA, McCance DJ, Reid JL, Bannister AJ and Kouzarides T . 1998 Nature 391: 597–601
Chakravarti D, Ogryzko V, Kao HY, Nash A, Chen H, Nakatani Y and Evans RM . 1999 Cell 96: 393–403
Chellappan SP, Hiebert S, Mudryj M, Horowitz JM and Nevins JR . 1991 Cell 65: 1053–1061
Chen H, Lin RJ, Schiltz RL, Chakravarti D, Nash A, Nagy L, Privalsky ML, Nakatani Y and Evans RM . 1997 Cell 90: 569–580
Chiarugi V, Cinelli M and Magnelli L . 1998 Oncol Res 10: 55–57
DeGregori J, Kowalik T and Nevins JR . 1995 Mol Cell Biol 15: 4215–4224
Dyson N, Buchkovich K, Whyte P and Harlow E . 1989 Princess Takamatsu Symp 20: 191–198
Eckner R . 1996 Biol Chem 377: 685–688
Eckner R, Yao TP, Oldread E and Livingston DM . 1996 Genes Dev 10: 2478–2490
Fry CJ, Pearson A, Malinowski E, Bartley SM, Greenblatt J and Farnham PJ . 1999 J Biol Chem 274: 15883–15891
Giles RH, Peters DJM and Breuning MH . 1998 Trends Genet 14: 178–183
Goldman PS, Tran VK and Goodman RH . 1997 Recent Prog Horm Res 52: 103–119; discussion 119–120
Groisman R, Masutani H, Leibovitch MP, Robin P, Soudant I, Trouche D and Harel-Bellan A . 1996 J Biol Chem 271: 5258–5264
Gu W and Roeder RG . 1997 Cell 90: 595–606
Gu W, Shi XL and Roeder RG . 1997 Nature 387: 819–823
Hamamori Y, Sartorelli V, Ogryzko V, Puri PL, Wu HY, Wang JY, Nakatani Y and Kedes L . 1999 Cell 96: 405–413
Hasegawa K, Meyers MB and Kitsis RN . 1997 J Biol Chem 272: 20049–20054
Hateboer G, Wobst A, Petersen BO, Le Cam L, Vigo E, Sardet C and Helin K . 1998 Mol Cell Biol 18: 6679–6697
Janknecht R and Hunter T . 1996 Curr Biol 6: 951–954
Kamei Y, Xu L, Heinzel T, Torchia J, Kurokawa R, Gloss B, Lin S-K, Heyman RA, Rose DW, Glass CK and Rosenfeld MG . 1996 Cell 85: 403–414
Karuppayil SM, Moran E and Das GM . 1998 J Biol Chem 273: 17303–17306
Kee BI, Arias J and Montminy MR . 1996 J Biol Chem 271: 2373–2375
Kitabayashi I, Yokoyama A, Shimizu K and Ohki M . 1998 EMBO J 17: 2994–3004
Korzus E, Torchia J, Rose DW, Xu L, Kurokawa R, McInerney EM, Mullen TM, Glass CK and Rosenfeld MG . 1998 Science 279: 703–707
Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, Brennan RG, Roberts SG, Green MR and Goodman RH . 1994 Nature 370: 223–226
Lam EW and Watson RJ . 1993 EMBO J 12: 2705–2713
Lee BH and Mathews MB . 1997 Proc Natl Acad Sci USA 94: 4481–4486
Lee CW, Sorensen TS, Shikama N and Lathangue NB . 1998 Oncogene 16: 2695–2710
Li Q, Imhof A, Collingwood TN, Urnov FD and Wolffe AP . 1999 EMBO J 18: 5634–5652
Lill NL, Grossman SR, Ginsberg D, DeCaprio J and Livingston DM . 1997 Nature 387: 823–827
Lundblad JR, Kwok RP, Laurance ME, Harter ML and Goodman RH . 1995 Nature 374: 85–88
Luo RX, Postigo AA and Dean DC . 1998 Cell 92: 463–473
Magnaghi-Jaulin L, Ait-Si-Ali S and Harel-Bellan A . 1999 Semin Cell Dev Biol 10: 197–203
Magnaghi-Jaulin L, Groisman R, Naguibneva I, Robin P, Lorain S, Le Villain JP, Troalen F, Trouche D and Harel-Bellan A . 1998 Nature 391: 601–605
Mink S, Haenig B and Klempnauer KH . 1997 Mol Cell Biol 17: 6609–6617
Missero C, Calautti E, Eckner R, Chin J, Tsai LH, Livingston DM and Dotto GP . 1995 Proc Natl Acad Sci USA 92: 5451–5455
Muraoka M, Konishi M, Kikuchi-Yanoshita R, Tanaka K, Shitara N, Chong JM, Iwama T and Miyaki M . 1996 Oncogene 12: 1565–1569
Nakajima T, Uchida C, Anderson SF, Parvin JD and Montminy M . 1997 Genes Dev 11: 738–747
Nevins JR . 1998 Cell Growth Differ 9: 585–593
Nevins JR, Leone G, Degregori J and Jakoi L . 1997 J Cell Physiol 173: 233–236
Ogryzko VV, Schiltz RL, Russanova V, Howard BH and Nakatani Y . 1996 Cell 87: 953–959
Puri PL, Avantaggiati ML, Balsano C, Sang N, Graessmann A, Giordano A and Levrero M . 1997a EMBO J 16: 369–383
Puri PL, Sartorelli V, Yang XJ, Hamamori Y, Ogryzko VV, Howard BH, Kedes L, Wang JY, Graessmann A, Nakatani Y and Levrero M . 1997b Mol Cell 1: 35–45
Ramirez S, Ali SAS, Robin P, Trouche D and Harel-Bellan A . 1997 J Biol Chem 272: 31016–31021
Sartorelli V, Huang J, Hamamori Y and Kedes L . 1997 Mol Cell Biol 17: 1010–1026
Satake N, Ishida Y, Otoh Y, Hinohara S, Kobayashi H, Sakashita A, Maseki N and Kaneko Y . 1997 Genes Chromosomes Cancer 20: 60–63
Sato S, Roberts K, Gambino G, Cook A, Kouzarides T and Goding CR . 1997 Oncogene 14: 3083–3092
Scolnick DM, Chehab NH, Stavridi ES, Lien MC, Caruso L, Moran E, Berger SL and Halazonetis TD . 1997 Cancer Res 57: 3693–3696
Shi Y and Mello C . 1998 Gene Dev 12: 943–955
Shikama N, Lyon J and La Thangue N . 1997 Trends Cell Biol 7: 230–236
Smits PH, de Wit L, van der Eb AJ and Zantema A . 1996 Oncogene 12: 1529–1535
Swope DL, Mueller CL and Chrivia JC . 1996 J Biol Chem 271: 28138–28145
Taki T, Sako M, Tsuchida M and Hayashi Y . 1997 Blood 89: 3945–3950
Tanaka Y, Naruse I, Maekawa T, Masuya H, Shiroishi T and Ishii S . 1997 Proc Natl Acad Sci USA 94: 10215–10220
Torchia J, Rose DW, Inostroza J, Kamei Y, Westin S, Glass CK and Rosenfeld MG . 1997 Nature 387: 677–684
Trouche D, Cook A and Kouzarides T . 1996 Nucl Acids Res 24: 4139–4145
Weinberg RA . 1992 Cancer Surv 12: 43–57
Wolffe AP and Pruss D . 1996 Cell 84: 817–819
Yang XJ, Ogryzko VV, Nishikawa J, Howard BH and Nakatani Y . 1996 Nature 382: 319–324
Yao TP, Oh SP, Fuchs M, Zhou ND, Chng LE, Newsome D, Bronson RT, Li E, Livingston DM and Eckner R . 1998 Cell 93: 361–372
Zhang HS, Postigo AA and Dean DC . 1999 Cell 97: 53–61
Acknowledgements
The authors thank Tony Kouzarides for the gift of plasmids and Linda L Pritchard for critical reading of the manuscript. This work was supported by grants from the Comité de l'Essonne and the Comité du Val de Marne de la Ligue Contre le Cancer, from the Ligue Nationale Contre le Cancer, from the Association pour la Recherche sur le Cancer, and from the European Commission (Grant QLRT-1999-00866). S Ait-Si-Ali was supported by a fellowship from the Ligue Nationale Contre le Cancer. A Polesskaya was awarded a fellowship from the FEBS organization. R Ferreira was supported by a fellowship from the Comité du Val-d'Oise de la Ligue Contre le Cancer.
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Ait-Si-Ali, S., Polesskaya, A., Filleur, S. et al. CBP/p300 histone acetyl-transferase activity is important for the G1/S transition. Oncogene 19, 2430–2437 (2000). https://doi.org/10.1038/sj.onc.1203562
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DOI: https://doi.org/10.1038/sj.onc.1203562
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