Regulation of ES cell differentiation by functional and conformational modulation of p53

EMBO Journal

Volumn 16, Issue 20, 1997, Pages 6217-6229

  Sabapathy, Kanaga ^a   Klemm, Martina ^b   Jaenisch, Rudolf ^b   F wagner, Erwin ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Apoptosis; Cell differentiation; Conformation; Embryonic stem cells; p53

Indexed keywords

MUTANT PROTEIN; PROTEIN ANTIBODY; PROTEIN P53;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EMBRYO; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; STEM CELL; TEMPERATURE; ULTRAVIOLET IRRADIATION;

ANIMALS; APOPTOSIS; BLASTOCYST; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MODELS, BIOLOGICAL; PROTEIN CONFORMATION; RADIATION TOLERANCE; STEM CELLS; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

ANIMALIA;

EID: 0030663519     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.20.6217     Document Type: Article

References (86)

1. Attardi, L.D., Lowe, S.W., Brugarolas, J. and Jacks, T. (1996) Transcriptional activation by p53, but not induction of the p21 gene. is essential for oncogene mediated apoptosis. EMBO J., 15, 3693-3701.
2. Banerjee, D., Lenz, H.J., Schnieders, B.D., Manno, J. Ju, J.F. Spears, C.P., Hochhauser, D., Danenberg, K., Danenberg, P. and Bertino, J.R. (1995) Transfection of wild-type but not mutant p53 induces early monocytic differentiation in HL60 cells and increases their sensitivity to stress. Cell Growth Differ., 6, 1405-1413.
3. Belloc, F. Dumain, P. Boisseau, M.R., Jalloustre, C., Reiffers, J., Bernard, P. and Lacombe, F. (1994) A flow cytometric method using Hoechst 33342 and propidium iodide for simultaneous cell cycle analysis and apoptosis determination in unfixed cells. Cytometry, 17, 59-65.
4. Brenner, L., Munoz-Antonia, T., Vellucci, V.F., Zhou, Z. and Reiss, M. (1993) Wild-type p53 tumor suppressor gene restores differentiation of human squamous carcinoma cells but not the response to transforming growth factor β. Cell Growth Differ., 4, 993-1004.
5. Chen, X., Ko, L.J., Jayaraman, L. and Prives, C. (1996) p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev., 10, 2438-2451.
6. de Oca Luna, R.M., Wagner, D.S. and Lozano, G. (1995) Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature. 378, 203-206.
7. Donehower, L.A., Harvey, M., Slagle, B.L., McArthur, M.J., Montgomery, C.A., Jr. Butel, J.S. and Bradley, A. (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours, Nature. 356, 215-221.
8. Dulic, V., Kaufmann, W.K., Wilson, S.J., Tlsty, T.D., Lees, E., Harper, J.W., Elledge, S.J. and Reed, S.I. (1994) p53 dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest, Cell. 76, 1013-1023.
9. Ehinger, M., Nilsson, H., Persson, A.M., Olsen, I. and Gullberg, U. (1995) Involvement of the tumor suppressor gene p53 in tumor necrosis factor-induced differentiation of the leukemic cell line K562. Cell Growth Differ., 6, 9-17.
10. El-Deiry, W.S., Kern, S.E., Pietenpol, J.A., Kinzler, J.A. and Vogelstein, B. (1992) Definition of a consensus binding site for p53. Nature Genet., 1, 45-49.
11. Evans, M.J. and Kaufman, M. (1981) Establishment in culture of pluripotent cells from mouse embryos. Nature. 292, 154-156.
12. Evans, M.J., Lovell-Badge, R.H., Stern, P.L. and Stinnakre, M.G. (1979) Cell lineage of the mouse embryo and embryonal carcinoma cells: Forssman antigen distribution and patterns of protein synthesis. In Le Douarin, N. (ed.), Cell Lineages. Stem Cells und Cell Determination. INSERM Symposium No. 10. Elscvier/North-Holland Biomedical Press. Amsterdam. The Netherlands, pp. 115-129.
13. Feinstein, K., Gale, R.P., Reed, J. and Canaani, E. (1992) Expression of the normal p53 gene induces differentiation of K562 cells. Oncogene. 7. 1853-1857.
14. Frebourg, T. Barbier, N., Kassel, J., Ng, Y.S., Romero, P. and Friend, S.H. (1992) A functional screen for germ line p53 mutations based on transcriptional activation. Cancer Res., 52, 6976-6978.
15. Friedlander, P., Haupt, Y., Prives, C. and Oren, M. (1996) A mutant p53 that discriminates between p53-responsive genes cannot induce apoptosis. Mol. Cell. Biol., 16, 4961-4971.
16. Funk, W.D., Pak, D.T., Karas, R.H., Wright, W.E. and Shay, J.W. (1992) A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol. 12, 2866-2871.
17. Cannon, J.V., Greaves, R. and Lane, D. (1990) Activating mutations in p53 produce a common conformational effect. A monoclonal antibody specific for the mutant form. EMBO J., 9, 1595-1602.
18. Generoso, W.M., Rutledge, J.C. and Aronson, J. (1990) Developmental anomalies: Mutational consequence of mouse zygote exposure. In Allen, J.A., Bridges, B.A., Lyon, M.F., Moses, M.J. and Russell, L.B. (eds). Biology of Mammalian Germ Cell Mutagenesis. Cold Spring Harbor Laboratory Press. Cold Spring Harbor. NY. Vol. 34, pp. 311-320.
19. Ginsberg, D., Mechtor, F., Yaniv, M. and Oren, M. (1991) Wild-type p53 can down-modulate the activity of various promoters. Proc. Natl Acad. Sci. USA. 88, 9979-9983.
20. Gottlieb, E., Haffner, R., von Ruden, T., Wagner, E.F. and Oren, M. (1994) Down-regulation of wild-type p53 activity interferes with apoptosis of IL-3-dependent hematopoietic cells following IL-3 withdrawal. EMBO J., 13, 1368-1374.
21. Gottlieb, E., Haffner, R., King, A., Asher, G., Gruss, P., Lonai, P. and Oren, M. (1997) Transgenic mouse model for studying the transcriptional activity of the p53 protein: age and tissue dependent changes in radiation-induced activation during embryogenesis. EMBO J., 16, 1381-1390.
22. Gottlieb, M.T. and Oren, M. (1996) p53 in growth control and neoplasia. Biochim. Biophys. Acta. 1287, 77-102.
23. 6-methylguanine-DNA methyltransferase gene. Cancer Res., 56, 2029-2032.
24. Harvey, M., Sands, A.T., Weiss, R.S., Hegi, M.E., Wiseman, R.W., Pantazis, P., Giovanella, B.C., Tainsky, M.A., Bradley, A. and Donehower, L.A. (1993) In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene. 8, 2457-2467.
25. Haupt, Y., Rowan, S., Shaulian, E., Vousden, K. and Oren, M. (1995) Induction of apoptosis in HeLa cells by transactivation-deficient p53. Genes Dev., 9, 2170-2183.
26. Haupt, Y., Maya, R., Kazaz, A. and Oren, M. (1997) Mdm2 promotes the rapid degradation of p53. Nature. 387, 296-299.
27. Hunter, T. (1993) Braking the cell-cycle. Cell. 75, 839-841.
28. Hupp, T.R., Meek, D.W., Midgley, C.A. and Lane, D.P. (1992) Regulation of the specific DNA binding function of p53. Cell. 71, 875-886.
29. Hupp, T.R., Sparks, A. and Lane, D. (1995) Small peptides activate the latent sequence-specific DNA binding function of p53. Cell. 83, 237-245.
30. Jacks, T., Remington, L., Williams, B.O., Schmitt, E.M., Halachmi, S., Bronson, R.T. and Weinberg, R.A. (1994) Tumor spectrum analysis in p53-mutant mice. Curr. Biol., 4, 1-7.
31. Jones, S.N., Roe, A.E., Donehower, L.A. and Bradley, A. (1995) Rescue of embryonic lethality on Mdm2-dcficient mice by absence of p53. Nature. 378, 206-208.
32. Kastan, M.B., Onyekwere, O., Sidransky, D., Vogelstein, B. and Craig, R.W. (1991a) Participation of p53 protein in the cellular response to DNA damage. Cancer Res., 51, 6304-6311.
33. Kastan, M.B., Radin, A.I., Kuerbitz, S.J., Onyekwere, O., Wolkow, C.A., Civin, C.I., Stone, T., Woo, K.D., Ravindranath, Y. and Craig, R.W. (1991b) Levels of p53 increase with maturation in human hematopoietic cells. Cancer Res., 51, 4279-4286.
34. Kemler, R. (1980) Analysis of mouse embryonic cell differentiation. In Saner, H.W. (ed.), Progress in Developmental Biology. Gustav Fischer Verlag, Stuttgart, Germany, band 26, pp. 175-181.
35. Kemp, C.J., Wheldon, T. and Balmain, A. (1994) p53-deficient mice are extremely susceptible to radiation-induced tumorigenesis. Nature Genet., 8, 66-69.
36. Knippschild, U., Oren, M. and Deppert, W. (1996) Abrogation of wild-type p53 mediated growth-inhibition by nuclear exclusion. Oncogene. 12, 1755-1765.
37. Knudson, A.G. (1992) Stem cell regulation, tissue ontogeny, and oncogenic events. Semin. Cancer Biol., 3, 99-106.
38. Ko, L.J. and Prives, C. (1996) p53: puzzle und paradigm. Genes Dev., 10, 1054-1072.
39. Kubbutat, M.H.G., Jones, S.N. and Vousden, K.H. (1997) Regulation of p53 stability by Mdm2. Nature. 387, 299-303.
40. Lechner, M.S., Mack, D.H., Finiele, A.B., Crook, T., Vousden, K.H. and Lechner, M.S. (1992) Human papillomavirus E6 protein bind p53 in vivo and abrogate p53-mediated repression of transcription. EMBO J., 11, 3045-3052.
41. Louis, J.M., McFarland, V.W., May, P. and Mora, P.T. (1988) The phosphoprotein p53 is down-regulated post transcriptionally during embryogenesis in vertebrates. Biochim. Biophys. Acta. 950, 395-402.
42. Lu, X. and Lane, D. (1993) Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell. 75, 765-778.
43. Lu, X., Park, S.H., Thompson, T.C. and Lane, D.P. (1992) ras-induced hsperplasia occurs with mutation of p53. but activated ras and myc together can induce carcinoma without p53 mutation. Cell. 70, 153-161.
44. Ludwig, R.L., Bates, S. and Vousden, K.H. (1996) Differential activation of target cellular promoters by p53 mutants with impaired apoptotic function. Mol. Cell. Biol., 16, 4952-4960.
45. Lutzker, S.G. and Levine, A.J. (1996) A functionally inactive p53 protein in teratocarcinoma cells is activated by either DNA damage or cellular differentiation. Nature Med., 2, 804-810.
46. MacCallum, D.E., Hupp, T.R., Midgley, C.A., Stuart, D., Campbell, S.J., Harper, A., Walsh, F.S., Wright, E.G., Balmain, A., Lane, D.P. and Hall, P.A. (1996) The p53 response to ionising radiation in adult and developing murine tissues. Oncogene. 13, 2575-2587.
47. Mack, D.H., Vartikar, J., Pipas, J.M. and Laimins, L.A. (1993) Specific repression of TATA-mediated but not initiator-mediated transcription by wild-type p53. Nature. 363, 281-283.
48. MacQueen, H.A. (1979) Lethality of radioisotopes in early mouse embryos. J. Embryol. Exp. Morphol. 52, 203-208.
49. Maltzman, W. and Czyzyk, L. (1984) UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol. Cell. Biol., 4, 1689-1694.
50. Martinez, J., Georgoff, I., Martinez, J. and Levine, A.J. (1991) Cellular localization and cell cycle regulation by a temperature-sensitive p53 protein. Genes Dev., 5, 151-159.
51. Michalovitz, D., Halevy, O. and Oren, M. (1990) Conditional inhibition of transformation and of cell proliferation by a temperature-sensitive mutant of p53. Cell. 62, 671-680.
52. Milner, J. (1984) Different forms of p53 detected by monoclonal antibodies in non-dividing and dividing lymphocytes, Nature. 310, 143-145.
53. Milner, J. (1995) Flexibility: the key to p53 function? Trends Biochem. Sci., 20, 49-51.
54. Milner, J. and Medcalf, E.A. (1991) Cotranslation of activated mutant p53 with wild-type drives the wild-type p53 protein into the mutant conformation. Cell. 65, 765-774.
55. Milner, J. and Watson, J.V. (1990) Addition of fresh medium induces cell cycle and conformation changes in p53. a tumor suppressor protein. Oncogene. 5, 1683-1690.
56. 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.
57. Nevins, J.R. (1992) E2F: a link between Rb tumor suppressor protein and viral oncoproteins. Science. 258, 424-429.
58. Oren, M., Maltzman, W. and Levine, A.J. (1981) Post-translational regulation of the 54K cellular tumor antigen in normal and transformed cells. Mol. Cell. Biol. 1, 101-110.
59. Oren, M., Reid, N.C. and Levine, A.J. (1952) Regulation of the cellular p53 tumor antigen in teratocarcinoma cells and their differentiated progeny. Mol. Cell. Biol., 2, 443-449.
60. Parker, S.B., Eichele, G., Zhang, P. Rawls, A., Sands, A.T., Bradley, A., Olsen, E.N., Harper, J.W. and Elledge, S.J. (1995) p53-independent expression of p21 Cip in muscle and other terminally differentiating cells. Science. 267, 1024-1027.
61. Perry, M.E. and Levine, A.J. (1993) Tumor suppressor p53 and the cell cycle. Curr. Opin. Genes Dev., 3, 50-54.
62. Pierce, G.B. and Speers, W.C. (1988) Tumors as caricatures of the process of tissue renewal: prospects for therapy by directing differentiation. Cancer Res., 48, 1996-2004.
63. Pratt, M.A.C., Kralova, J. and McBurney, M.W. (1990) A dominant negative mutation of the alpha retinoic acid receptor gene in a retinoic acid-nonresponsive embryonal carcinoma cell. Mol. Cell. Biol., 10, 6445-6453.
64. Purdie, C.A., Harrison, D.J., Peter, A., Dobbie, L., White, S., Howie, S.E.M., Salter, D.M., Bird, C.C., Wylie, A.H., Hooper, M.L. and Clarke, A.R. (1994) Tumor incidence. spectrum and ploidy in mice with a large deletion in the p53 gene. Oncogene. 9, 603-609.
65. Rivas, C.I., Wisniewski, D., Strife, A., Perez, A., Lambek, C., Bruno, S., Darzynkiewicz, Z., and Clarkson, B. (1992) Constitutive expression of p53 protein in enriched normal human marrow blast cell populations. Blood. 79, 1982-1986.
66. Robertson, E., Bradley, A., Kuehn, M. and Evans, M. (1986) Germ line transmission of genes introduced into cultured pluripotent cells by retroviral vector. Nature. 323, 445-448.
67. Rogel, A., Popliker, M., Webb, C.G. and Oren, M. (1985) p53 cellular tumor antigen: Analysis of mRNA levels in normal adult tissues, embryos, and tumors. Mol. Cell. Biol., 5, 2851-2855.
68. Ronen, D., Schwartz, D., Teitz, Y., Goldfinger, N. and Rotter, V. (1996) Induction of HL-60 cells to undergo apoptosis is determined by high levels of wild-type p53 protein whereas differentiation of the cells is mediated by lower p53 levels. Cell Growth Differ., 7, 21-30.
69. Rutledge, J.C., Shourbaji, A.G., Hughes, L.A., Polifka, J.E., Cruz, Y.P., Bishop, J.B. and Generoso, W.M. (1994) Limb and lower-body duplications induced by retinoic acid in mice. Proc. Natl Acad. Sci. USA. 91, 5436-5440.
70. Sabbatini, R. Lin, J., Levine, A.J. and White, E. (1995) Essential role for p53-mediated transcription in E1A-induced apoptosis. Genes Dev., 9, 2184-2192.
71. Sah, V.P., Attardi, L.D., Mulligan, G.J., Williams, B.O., Bronson, R.T. and Jacks, T. (1995) A subset of p53-deficient embryos exhibit exencephaly. Nature Genet., 10, 175-180.
72. Savatier, P., Huang, S., Szekely, L., Wilman, K.G. and Samarut, J. (1994) Contrasting patterns of retinoblastoma protein expression in mouse embryonic stem cells and embryonic fibroblasts. Oncogene. 9, 809-818.
73. Savatier, P., Lapillonne, H., van Grunsven, L.A., Rudkin, B.B. and Samarut, J. (1995) Withdrawal of differentiation inhibitory activity/leukemia inhibitory factor up-regulates D-type cyclins and cyclin-dependent kinase inhibitors in mouse embryonic stem cells. Oncogene. 12, 309-322.
74. Schreiber, M., Baumann, B., Cotten, M., Angel, P. and Wagner, E.F. (1995) Fos is an essential component of the mammalian UV response. EMBO J., 14, 5338-5349.
75. Shaulsky, G., Goldfinger, N., Peled, A. and Rotter, V. (1991) Involvement of wild-type p53 in pre-B-cell differentiation in vitro. Proc. Natl Acad. Sci. USA. 88, 8982-8986.
76. Sibilia, M. and Wagner E.F. (1995) Strain-dependent epithelial defects in mice lacking the EGF receptor, Science. 269, 234-237.
77. Soddu, S., Blandino, G., Citro, G., Scardigli, R., Piaggio, G., Ferber, A., Calabretta, B. and Sacchi, A. (1994) Wild-type p53 gene expression induces granulocytic differentiation of HL-60 cells. Blood. 83, 2230-2237.
78. Soddu, S., Blandino, G., Scardigli, R., Coen, S., Marchetti, A., Rizzi, M.G., Bossi, G., Cimino, L., Cresccnzi, M. and Sacchi, A. (1996) Interference with p53 protein inhibits hematopoietic and muscle differentiation. J. Cell Biol., 134, 193-204.
79. Symonds, H., Krall, L., Remington, L., Saenz-Robles, M., Lowe, S., Jacks, T. and Dykc, T.V. (1994) p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell. 78, 703-711.
80. Ueda, H., Ullrich, S.J., Gangemi, D., Kappel, C.A., Ngo, L., Feitelson, M.A. and Jay, G. (1995) Functional inactivation but not structural mutation of p53 causes liver cancer. Nature Genet., 9, 41-47.
81. Vogelstein, B. and Kinzler, K. (1992) p53 function and dysfunction. Cell. 70, 523-526.
82. 3 in HL60 cells. Cancer Res., 56, 264-267.
83. Wang, Z.Q., Grigoriadis, A.E., Moble-Steinlein, U. and Wagner, E.F. (1991) A novel target cell for c-fos-induced oncogenesis: development of chondrogenic tumours in embryonic stem cell chimeras. EMBO J., 10, 2437-2450.
84. Weinberg, W.C., Azzoli, C.A., Chapman, K., Levine, A.J. and Yuspa, S.H. (1995) p53-mediated transcriptional activity increases in differentiating epidermal keratinocytes in association with decreased p53 protein. Oncogene. 10, 2271-2279.
85. Wilman, K.G. (1993) The retinoblastoma gene: role in cell cycle control and cell differentiation. FASEB J., 7, 841-845.
86. Wolkowicz, R. and Rotter, V. (1997) The DNA binding regulatory domain of p53: See the C. In Soussi, T. (ed.), Pathologie-Biologie, in press.