Osteoblast differentiation and skeletal development are regulated by Mdm2-p53 signaling

Journal of Cell Biology

Volumn 172, Issue 6, 2006, Pages 909-921

  Lengner, Christopher J ^a,d   Steinman, Heather A ^a   Gagnon, James ^a,e   Smith, Thomas W ^a   Henderson, Janet E ^b   Kream, Barbara E ^c   Stein, Gary S ^a   Lian, Jane B ^a   Jones, Stephen N ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^e BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; PROTEIN MDM2; PROTEIN P53; TRANSCRIPTION FACTOR RUNX2;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CAUSE OF DEATH; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; GENE DELETION; MOUSE; MOUSE STRAIN; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKELETON MALFORMATION; TRANSGENIC MOUSE;

ANIMALIA; MUS MUSCULUS;

EID: 33644879150     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200508130     Document Type: Article

References (41)

1. Alt, J.R., T.C. Greiner, J.L. Cleveland, and C.M. Eischen. 2003. Mdm2 haplo-insufficiency profoundly inhibits Myc-induced lymphomagenesis. EMBO J. 22:1442-1450.
2. Armstrong, J.F., M.H. Kaufman, D.J. Harrison, and A.R. Clarke. 1995. High-frequency developmental abnormalities in p53-deficient mice. Curr. Biol. 5:931-936.
3. Banerjee, C., L.R. McCabe, J.-Y. Choi, S.W. Hiebert, J.L. Stein, G.S. Stein, and J.B. Lian. 1997. Runt homology domain proteins in osteoblast differentiation: AML3/CBFA1 is a major component of a bone-specific complex. J. Cell. Biochem. 66:1-8.
4. Chen, J., J. Lin, and A.J. Levine. 1995. Regulation of transcription functions of the p53 tumor suppressor by the mdm-2 oncogene. Mol. Med. 1:142-152.
5. Deng, C., P. Zhang, J.W. Harper, S.J. Elledge, and P. Leder. 1995. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell. 82:675-684.
6. Donehower, L.A., M. Harvey, B.L. Slagle, M.J. McArthur, C.A. Montgomery Jr., J.S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature. 356:215-221.
7. Doumont, G., A. Martoriati, C. Beekman, S. Bogaerts, P.J. Mee, F. Bureau, E. Colombo, M. Alcalay, E. Bellefroid, F. Marchesi, et al. 2005. G1 checkpoint failure and increased tumor susceptibility in mice lacking the novel p53 target Ptprv. EMBO J. 24:3093-3103.
8. Ducy, P., R. Zhang, V. Geoffroy, A.L. Ridall, and G. Karsenty. 1997. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell. 89:747-754.
9. Freedman, D.A., and A.J. Levine. 1998. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell. Biol. 18:7288-7293.
10. Geyer, R.K., Z.K. Yu, and C.G. Maki. 2000. The MDM2 RING-finger domain is required to promote p53 nuclear export. Nat. Cell Biol. 2:569-573.
11. Gottlieb, E., R. Haffner, A. King, G. Asher, P. Gruss, P. Lonai, and M. Oren. 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.
12. Harada, S., and G.A. Rodan. 2003. Control of osteoblast function and regulation of bone mass. Nature. 423:349-355.
13. Harvey, M., M.J. McArthur, C.A. Montgomery Jr., A. Bradley, and L.A. Donehower. 1993a. Genetic background alters the spectrum of tumors that develop in p53-deficient mice. FASEB J. 7:938-943.
14. Harvey, M., M.J. McArthur, C.A. Montgomery Jr., J.S. Butel, A. Bradley, and L.A. Donehower. 1993b. Spontaneous and carcinogen-induced tumorigenesis in p53-deficient mice. Nat. Genet. 5:225-229.
15. Haupt, Y., R. Maya, A. Kazaz, and M. Oren. 1997. Mdm2 promotes the rapid degradation of p53. Nature. 387:296-299.
16. Honda, R., H. Tanaka, and H. Yasuda. 1997. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420:25-27.
17. Hopyan, S., N. Gokgoz, R.S. Bell, I.L. Andrulis, B.A. Alman, and J.S. Wunder. 1999. Expression of osteocalcin and its transcriptional regulators corebinding factor alpha 1 and MSX2 in osteoid-forming tumours. J. Orthop. Res. 17:633-638.
18. Iwakuma, T., and G. Lozano. 2003. MDM2, an introduction. Mol. Cancer Res. 1:993-1000.
19. Jones, S.N., A.E. Roe, L.A. Donehower, and A. Bradley. 1995. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature. 378:206-208.
20. Jones, S.N., A.T. Sands, A.R. Hancock, H. Vogel, L.A. Donehower, S.P. Linke, G.M. Wahl, and A. Bradley. 1996. The tumorigenic potential and cell growth characteristics of p53-deficient cells are equivalent in the presence or absence of Mdm2. Proc. Natl. Acad. Sci. USA. 93:14106-14111.
21. Juven, T., Y. Barak, A. Zauberman, D.L. George, and M. Oren. 1993. Wild type p53 can mediate sequence-specific transactivation of an internal promoter within the mdm2 gene. Oncogene. 8:3411-3416.
22. Komori, T., H. Yagi, S. Nomura, A. Yamaguchi, K. Sasaki, K. Deguchi, Y. Shimizu, R.T. Bronson, Y.H. Gao, M. Inada, et al. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 89:755-764.
23. Kubbutat, M.H., S.N. Jones, and K.H. Vousden. 1997. Regulation of p53 stability by Mdm2. Nature. 387:299-303.
24. Li, M., C.L. Brooks, F. Wu-Baer, D. Chen, R. Baer, and W. Gu. 2003. Mono-versus polyubiquitination: differential control of p53 fate by Mdm2. Science. 302:1972-1975.
25. Liu, F., H.W. Woitge, A. Braut, M.S. Kronenberg, A.C. Lichtler, M. Mina, and B.E. Kream. 2004. Expression and activity of osteoblast-targeted Cre recombinase transgenes in murine skeletal tissues. Int. J. Dev. Biol. 48:645-653.
26. Marino, S., M. Vooijs, H. van Der Gulden, J. Jonkers, and A. Berns. 2000. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 14:994-1004.
27. Mendrysa, S.M., M.K. McElwee, J. Michalowski, K.A. O'Leary, K.M. Young, and M.E. Perry. 2003. mdm2 Is critical for inhibition of p53 during lymphopoiesis and the response to ionizing irradiation. Mol. Cell. Biol. 23:462-472.
28. Momand, J., G.P. Zambetti, D.C. Olson, D. George, and A.J. Levine. 1992. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell. 69:1237-1245.
29. Montes de Oca Luna, R., D.S. Wagner, and G. Lozano. 1995. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature. 378:203-206.
30. Otto, F., A.P. Thornell, T. Crompton, A. Denzel, K.C. Gilmour, I.R. Rosewell, G.W. Stamp, R.S. Beddington, S. Mundlos, B.R. Olsen, et al. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 89:765-771.
31. Owen, T.A., J. Holthuis, E. Markose, A.J. van Wijnen, S.A. Wolfe, S.R. Grimes, J.B. Lian, and G.S. Stein. 1990. Modifications of protein-DNA interactions in the proximal promoter of a cell-growth-regulated histone gene during onset and progression of osteoblast differentiation. Proc. Natl. Acad. Sci. USA. 87:5129-5133.
32. Sah, V.P., L.D. Attardi, G.J. Mulligan, B.O. Williams, R.T. Bronson, and T. Jacks. 1995. A subset of p53-deficient embryos exhibit exencephaly. Nat. Genet. 10:175-180.
33. Soriano, P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21:70-71.
34. Soussi, T., and C. Beroud. 2001. Assessing TP53 status in human tumours to evaluate clinical outcome. Nat. Rev. Cancer. 1:233-240.
35. Stein, G.S., J.B. Lian, A.J. van Wijnen, J.L. Stein, M. Montecino, A. Javed, S.K. Zaidi, D.W. Young, J.-Y. Choi, and S.M. Pockinwise. 2004. Runx2 control of organization and activity of the regulatory machinery for skeletal gene expression. Oncogene. 23:4315-4329.
36. Steinman, H.A., and S.N. Jones. 2002. Generation of an Mdm2 conditional allele in mice. Genesis. 32:142-144.
37. Thomas, D.M., S.A. Johnson, N.A. Sims, M.K. Trivett, J.L. Slavin, B.P. Rubin, P. Waring, G.A. McArthur, C.R. Walkley, A.J. Holloway, et al. 2004. Terminal osteoblast differentiation, mediated by runx2 and p27KIP1, is disrupted in osteosarcoma. J. Cell Biol. 167:925-934.
38. Tyner, S.D., S. Venkatachalam, J. Choi, S. Jones, N. Ghebranious, H. Igelmann, X. Lu, G. Soron, B. Cooper, C. Brayton, et al. 2002. p53 mutant mice that display early ageing-associated phenotypes. Nature. 415:45-53.
39. Vousden, K.H. 2000. p53: death star. Cell. 103:691-694.
40. Xirodimas, D.P., M.K. Saville, J.C. Bourdon, R.T. Hay, and D.P. Lane. 2004. Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell. 118:83-97.
41. Wu, X., J.H. Bayle, D. Olson, and A.J. Levine. 1993. The p53-mdm-2 autoregulatory feedback loop. Genes Dev. 7:1126-1132.