DNA damage in oocytes induces a switch of the quality control factor TAp63α from dimer to tetramer

Cell

Volumn 144, Issue 4, 2011, Pages 566-576

  Deutsch, Gregor B ^a   Zielonka, Elisabeth M ^b,c   Coutandin, Daniel ^a   Weber, Tobias A ^a   Schäfer, Birgit ^a   Hannewald, Jens ^d   Luh, Laura M ^a   Durst, Florian G ^a   Ibrahim, Mohamed ^a   Hoffmann, Jan ^a   Niesen, Frank H ^e   Sentürk, Aycan ^a   Kunkel, Hana ^g   Brutschy, Bernd ^a   Schleiff, Enrico ^a   Knapp, Stefan ^e,f   Acker Palmer, Amparo ^a   Grez, Manuel ^g   McKeon, Frank ^b,c,h   Dötsch, Volker ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c GENOME INSTITUTE OF SINGAPORE   (Singapore)

^d MERCK KGAA   (Germany)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

^h HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; DNA; PROTEIN P63; PROTEIN TAP63ALPHA; TETRAMER; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; FEMALE; HUMAN; IN VIVO STUDY; MOUSE; NONHUMAN; OLIGOMERIZATION; OOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION;

EID: 79951687016     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2011.01.013     Document Type: Article

References (44)

1. Brandt, T., Petrovich, M., Joerger, A.C., and Veprintsev, D.B. (2009). Conservation of DNA-binding specificity and oligomerisation properties within the p53 family. BMC Genomics 10, 628.
2. Brooks, C.L., and Gu, W. (2006). p53 ubiquitination: Mdm2 and beyond. Mol. Cell 21, 307-315. (Pubitemid 43163526)
3. Burge, S., Teufel, D.P., Townsley, F.M., Freund, S.M., Bycroft, M., and Fersht, A.R. (2009). Molecular basis of the interactions between the p73 N terminus and p300: effects on transactivation and modulation by phosphorylation. Proc. Natl. Acad. Sci. USA 106, 3142-3147.
4. Celli, J., Duijf, P., Hamel, B.C., Bamshad, M., Kramer, B., Smits, A.P., Newbury-Ecob, R., Hennekam, R.C., Van Buggenhout, G., van Haeringen, A., et al. (1999). Heterozygous germline mutations in the p53 homolog p63 are the cause of EEC syndrome. Cell 99, 143-153. (Pubitemid 29491781)
5. Chan, W.M., Siu, W.Y., Lau, A., and Poon, R.Y. (2004). How many mutant p53 molecules are needed to inactivate a tetramer? Mol. Cell. Biol. 24, 3536-3551.
6. Chene, P. (2001). The role of tetramerization in p53 function. Oncogene 20, 2611-2617.
7. Cole, J.L. (2004). Analysis of heterogeneous interactions. Methods Enzymol. 384, 212-232.
8. Coutandin, D., Löhr, F., Niesen, F., Ikeya, T., Weber, T., Schäfer, B., Bullock, A., Yang, A., Güntert, P., Knapp, S., et al. (2009). Conformational stability and activity of p73 require a second helix in the tetramerization domain. Cell Death Differ. 16, 1582-1589.
9. Coutandin, D., Der Ou, H., Lohr, F., and Dotsch, V. (2010). Tracing the protectors path from the germ line to the genome. Proc. Natl. Acad. Sci. USA 107, 15318-15325.
10. Davison, T.S., Nie, X., Ma, W., Lin, Y., Kay, C., Benchimol, S., and Arrowsmith, C.H. (2001). Structure and functionality of a designed p53 dimer. J. Mol. Biol. 307, 605-617.
11. De Laurenzi, V., Catani, M., Terrinoni, A., Corazzari, M., Melino, G., Costanzo, A., Levrero, M., and Knight, R.A. (1999). Additional complexity in p73: induction by mitogens in lymphoid cells and identification of two new splicing variants epsilon and zeta. Cell Death Differ. 6, 389-390. (Pubitemid 29245951)
12. Derry, W.B., Putzke, A.P., and Rothman, J.H. (2001). Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294, 591-595. (Pubitemid 32999555)
13. Guo, X., Keyes, W.M., Papazoglu, C., Zuber, J., Li, W., Lowe, S.W., Vogel, H., and Mills, A.A. (2009). TAp63 induces senescence and suppresses tumorigenesis in vivo. Nat. Cell Biol. 11, 1451-1457.
14. Hoffmann, J., Schmidt, T.L., Heckel, A., and Brutschy, B. (2009). Probing the limits of liquid droplet laser desorption mass spectrometry in the analysis of oligonucleotides and nucleic acids. Rapid Commun. Mass Spectrom. 23, 2176-2180.
15. Horikoshi, N., Usheva, A., Chen, J., Levine, A.J., Weinmann, R., and Shenk, T. (1995). Two domains of p53 interact with the TATA-binding protein, and the adenovirus 13S E1A protein disrupts the association, relieving p53-mediated transcriptional repression. Mol. Cell. Biol. 15, 227-234.
16. Jeffrey, P.D., Gorina, S., and Pavletich, N.P. (1995). Crystal structure of the tetramerization domain of the p53 tumor suppressor at 1.7 angstroms. Science 267, 1498-1502.
17. Joerger, A.C., Rajagopalan, S., Natan, E., Veprintsev, D.B., Robinson, C.V., and Fersht, A.R. (2009). Structural evolution of p53, p63, and p73: implication for heterotetramer formation. Proc. Natl. Acad. Sci. USA 106, 17705-17710.
18. Kaghad, M., Bonnet, H., Yang, A., Creancier, L., Biscan, J.C., Valent, A., Minty, A., Chalon, P., Lelias, J.M., Dumont, X., et al. (1997). Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers. Cell 90, 809-819. (Pubitemid 27357971)
19. Kussie, P.H., Gorina, S., Marechal, V., Elenbaas, B., Moreau, J., Levine, A.J., and Pavletich, N.P. (1996). Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 274, 948-953. (Pubitemid 26398409)
20. Lambert, J.M., Gorzov, P., Veprintsev, D.B., Soderqvist, M., Segerback, D., Bergman, J., Fersht, A.R., Hainaut, P., Wiman, K.G., and Bykov, V.J. (2009). PRIMA-1 reactivates mutant p53 by covalent binding to the core domain. Cancer Cell 15, 376-388.
21. Lebowitz, J., Lewis, M.S., and Schuck, P. (2002). Modern analytical ultracentrifugation in protein science: a tutorial review. Protein Sci. 11, 2067-2079. (Pubitemid 34919611)
22. Lee, W., Harvey, T.S., Yin, Y., Yau, P., Litchfield, D., and Arrowsmith, C.H. (1994). Solution structure of the tetrameric minimum transforming domain of p53. Nat. Struct. Biol. 1, 877-890.
23. Lu, H., and Levine, A.J. (1995). Human TAFII31 protein is a transcriptional coactivator of the p53 protein. Proc. Natl. Acad. Sci. USA 92, 5154-5158.
24. McGrath, J.A., Duijf, P.H., Doetsch, V., Irvine, A.D., de Waal, R., Vanmolkot, K.R., Wessagowit, V., Kelly, A., Atherton, D.J., Griffiths, W.A., et al. (2001). Hay-Wells syndrome is caused by heterozygous missense mutations in the SAM domain of p63. Hum. Mol. Genet. 10, 221-229.
25. Mills, A.A., Zheng, B., Wang, X.J., Vogel, H., Roop, D.R., and Bradley, A. (1999). p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398, 708-713. (Pubitemid 29197649)
26. Morgner, N., Kleinschroth, T., Barth, H.D., Ludwig, B., and Brutschy, B. (2007). A novel approach to analyze membrane proteins by laser mass spectrometry: from protein subunits to the integral complex. J. Am. Soc. Mass Spectrom. 18, 1429-1438.
27. Ortt, K., and Sinha, S. (2006). Derivation of the consensus DNA-binding sequence for p63 reveals unique requirements that are distinct from p53. FEBS Lett. 580, 4544-4550. (Pubitemid 44118257)
28. Ou, H.D., Löhr, F., Vogel, V., Mäntele, W., and Dötsch, V. (2007). Structural evolution of C-terminal domains in the p53 family. EMBO J. 26, 3463-3473. (Pubitemid 47123529)
29. Pearson, B.J., and Sanchez Alvarado, A. (2010). A planarian p53 homolog regulates proliferation and self-renewal in adult stem cell lineages. Development 137, 213-221.
30. Rossi, M., Aqeilan, R.I., Neale, M., Candi, E., Salomoni, P., Knight, R.A., Croce, C.M., and Melino, G. (2006). The E3 ubiquitin ligase Itch controls the protein stability of p63. Proc. Natl. Acad. Sci. USA 103, 12753-12758.
31. Schleiff, E., Jelic, M., and Soll, J. (2003). A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proc. Natl. Acad. Sci. USA 100, 4604-4609.
32. Schmale, H., and Bamberger, C. (1997). A novel protein with strong homology to the tumor suppressor p53. Oncogene 15, 1363-1367. (Pubitemid 27429753)
33. Senoo, M., Pinto, F., Crum, C.P., and McKeon, F. (2007). p63 Is essential for the proliferative potential of stem cells in stratified epithelia. Cell 129, 523-536. (Pubitemid 46660965)
34. Senoo, M., Seki, N., Ohira, M., Sugano, S., Watanabe, M., Inuzuka, S., Okamoto, T., Tachibana, M., Tanaka, T., Shinkai, Y., et al. (1998). A second p53-related protein, p73L, with high homology to p73. Biochem. Biophys. Res. Commun. 248, 603-607.
35. Serber, Z., Lai, H.C., Yang, A., Ou, H.D., Sigal, M.S., Kelly, A.E., Darimont, B.D., Duijf, P.H., Van Bokhoven, H., McKeon, F., et al. (2002). A C-terminal inhibitory domain controls the activity of p63 by an intramolecular mechanism. Mol. Cell. Biol. 22, 8601-8611.
36. Straub, W.E., Weber, T.A., Schäfer, B., Candi, E., Durst, F., Ou, H.D., Rajalingam, K., Melino, G., and Dötsch, V. (2010). The C-terminus of p63 contains multiple regulatory elements with different functions. Cell Death Dis. 1, e5. 10.1038/cddis.2009.1.
37. Suh, E.K., Yang, A., Kettenbach, A., Bamberger, C., Michaelis, A.H., Zhu, Z., Elvin, J.A., Bronson, R.T., Crum, C.P., and McKeon, F. (2006). p63 protects the female germ line during meiotic arrest. Nature 444, 624-628. (Pubitemid 44864440)
38. Thut, C.J., Chen, J.L., Klemm, R., and Tjian, R. (1995). p53 transcriptional activation mediated by coactivators TAFII40 and TAFII60. Science 267, 100-104.
39. Trink, B., Okami, K., Wu, L., Sriuranpong, V., Jen, J., and Sidransky, D. (1998). A new human p53 homologue. Nat. Med. 4, 747-748.
40. Wade, M., Wang, Y.V., and Wahl, G.M. (2010). The p53 orchestra: Mdm2 and Mdmx set the tone. Trends Cell Biol. 20, 299-309.
41. Yang, A., Kaghad, M., Wang, Y., Gillett, E., Fleming, M.D., Dotsch, V., Andrews, N.C., Caput, D., and McKeon, F. (1998). p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol. Cell 2, 305-316. (Pubitemid 128379271)
42. Yang, A., Schweitzer, R., Sun, D., Kaghad, M., Walker, N., Bronson, R.T., Tabin, C., Sharpe, A., Caput, D., Crum, C., et al. (1999). p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398, 714-718. (Pubitemid 29197650)
43. Yang, A., Walker, N., Bronson, R., Kaghad, M., Oosterwegel, M., Bonnin, J., Vagner, C., Bonnet, H., Dikkes, P., Sharpe, A., et al. (2000). p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature 404, 99-103. (Pubitemid 30143141)
44. Ying, H., Chang, D.L., Zheng, H., McKeon, F., and Xiao, Z.X. (2005). DNA-binding and transactivation activities are essential for TAp63 protein degradation. Mol. Cell. Biol. 25, 6154-6164.