Regulation of p63 protein stability via ubiquitin-proteasome pathway

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Li, Chenghua ^a   Xiao, Zhi Xiong ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ATM PROTEIN; CYCLIN DEPENDENT KINASE 2; FBW7 PROTEIN; HOMEODOMAIN INTERACTING PROTEIN KINASE 2; I KAPPA B KINASE BETA; ISOPROTEIN; ITCH PROTEIN; PIRH2 PROTEIN; PROTEASOME; PROTEIN KINASE; PROTEIN P53; PROTEIN P63; RECEPTOR FOR ACTIVATED C KINASE 1; S6 KINASE; STRATIFIN; STXBP4 PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; WWP1 PROTEIN; PHOSPHOPROTEIN; TP63 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; TRP63 PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

HUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; MOUSE;

ANIMALS; HUMANS; MICE; PHOSPHOPROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN;

EID: 84900013760     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/175721     Document Type: Review

References (69)

1. Osada M., Ohba M., Kawahara C., Ishioka C., Kanamaru R., Katoh I., Ikawa Y., Nimura Y., Nakagawara A., Obinata M., Ikawa S., Cloning and functional analysis of human p51, which structurally and functionally resembles p53. Nature Medicine 1998 4 7 839 843 2-s2.0-0031852337 10.1038/nm0798-839
2. Trink B., Okami K., Wu L., Sriuranpong V., Jen J., Sidransky D., A new human p53 homologue. Nature Medicine 1998 4 7 747 748 2-s2.0-0031874340 10.1038/nm0798-747
3. Hibi K., Trink B., Patturajan M., Westra W. H., Caballero O. L., Hill D. E., Ratovitski E. A., Jen J., Sidransky D., AIS is an oncogene amplified in squamous cell carcinoma. Proceedings of the National Academy of Sciences of the United States of America 2000 97 10 5462 5467 2-s2.0-0034625043 10.1073/pnas.97.10.5462
4. Senoo M., Pinto F., Crum C. P., McKeon F., p63 is essential for the proliferative potential of stem cells in stratified epithelia. Cell 2007 129 3 523 536 2-s2.0-34247511981 10.1016/j.cell.2007.02.045
5. Guo X., Keyes W. M., Papazoglu C., Zuber J., Li W., Lowe S. W., Vogel H., Mills A. A., TAp63 induces senescence and suppresses tumorigenesis in vivo. Nature cell biology 2009 11 12 1451 1457 2-s2.0-73349088166
6. Su X., Chakravarti D., Cho M. S., Liu L., Gi Y. J., Lin Y.-L., Leung M. L., El-Naggar A., Creighton C. J., Suraokar M. B., Wistuba I., Flores E. R., TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 2010 467 7318 986 990 2-s2.0-77958558613 10.1038/nature09459
7. Keyes W. M., Pecoraro M., Aranda V., Vernersson-Lindahl E., Li W., Vogel H., Guo X., Garcia E. L., Michurina T. V., Enikolopov G., Muthuswamy S. K., Mills A. A., Δnp63 α is an oncogene that targets chromatin remodeler Lsh to drive skin stem cell proliferation and tumorigenesis. Cell Stem Cell 2011 8 2 164 176 2-s2.0-79551607574 10.1016/j.stem.2010.12.009
8. Carroll D. K., Carroll J. S., Leong C.-O., Cheng F., Brown M., Mills A. A., Brugge J. S., Ellisen L. W., p63 regulates an adhesion programme and cell survival in epithelial cells. Nature Cell Biology 2006 8 6 551 561 2-s2.0-33744796255 10.1038/ncb1420
9. Maisse C., Guerrieri P., Melino G., p73 and p63 protein stability: the way to regulate function? Biochemical Pharmacology 2003 66 8 1555 1561 2-s2.0-0642375803 10.1016/S0006-2952(03)00511-2
10. Finlan L. E., Hupp T. R., p63: the phantom of the tumor suppressor. Cell Cycle 2007 6 9 1062 1071 2-s2.0-34248151361
11. Yang A., Kaghad M., Wang Y., Gillett E., Fleming M. D., Dötsch V., Andrews N. C., Caput D., McKeon F., p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Molecular Cell 1998 2 3 305 316 2-s2.0-0032161624
12. Murray-Zmijewski F., Lane D. P., Bourdon J.-C., p53/p63/p73 isoforms: an orchestra of isoforms to harmonise cell differentiation and response to stress. Cell Death and Differentiation 2006 13 6 962 972 2-s2.0-33646798450 10.1038/sj.cdd.4401914
13. Mangiulli M., Valletti A., Caratozzolo M. F., Tullo A., Sbisà E., Pesole G., D'Erchia A. M., Identification and functional characterization of two new transcriptional variants of the human p63 gene. Nucleic Acids Research 2009 37 18 6092 6104 2-s2.0-70350674206 10.1093/nar/gkp674
14. van Bokhoven H., Hamel B. C. J., Bamshad M., Sangiorgi E., Gurrieri F., Duijf P. H. G., Vanmolkot K. R. J., Van Beusekom E., Van Beersum S. E. C., Celli J., Merkx G. F. M., Tenconi R., Fryns J. P., Verloes A., Newbury-Ecob R. A., Raas-Rotschild A., Majewski F., Beemer F. A., Janecke A., Chitayat D., Crisponi G., Kayserili H., Yates J. R. W., Neri G., Brunner H. G., p63 gene mutations in EEC syndrome, limb-mammary syndrome, and isolated split hand-split foot malformation suggest a genotype-phenotype correlation. American Journal of Human Genetics 2001 69 3 481 492 2-s2.0-0034892604 10.1086/323123
15. Mills A. A., Zheng B., Wang X.-J., Vogel H., Roop D. R., Bradley A., p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 1999 398 6729 708 713 2-s2.0-0033594491 10.1038/19531
16. Di Costanzo A., Festa L., Duverger O., Vivo M., Guerrini L., La Mantia G., Morasso M. I., Calabrò V., Homeodomain protein Dlx3 induces phosphorylation-dependent p63 degradation. Cell Cycle 2009 8 8 1185 1195 2-s2.0-65949100595
17. King K. E., Ponnamperuma R. M., Gerdes M. J., Tokino T., Yamashita T., Baker C. C., Weinberg W. C., Unique domain functions of p63 isotypes that differentially regulate distinct aspects of epidermal homeostasis. Carcinogenesis 2006 27 1 53 63 2-s2.0-29744445504 10.1093/carcin/bgi200
18. Paris M., Rouleau M., Pucéat M., Aberdam D., Regulation of skin aging and heart development by TAp63. Cell Death and Differentiation 2012 19 2 186 193 2-s2.0-84855677635 10.1038/cdd.2011.181
19. Wu G., Nomoto S., Hoque M. O., Dracheva T., Osada M., Lee C.-C. R., Dong S. M., Guo Z., Benoit N., Cohen Y., Rechthand P., Califano J., Moon C.-S., Ratovitski E., Jen J., Sidransky D., Trink B., ΔNp63 α and TAp63 α regulate transcription of genes with distinct biological functions in cancer and development. Cancer Research 2003 63 10 2351 2357 2-s2.0-0037507296
20. Gressner O., Schilling T., Lorenz K., Schleithoff E. S., Koch A., Schulze-Bergkamen H., Lena A. M., Candi E., Terrinoni A., Catani M. V., Oren M., Melino G., Krammer P. H., Stremmel W., Müller M., TAp63 α induces apoptosis by activating signaling via death receptors and mitochondria. The EMBO Journal 2005 24 13 2458 2471 2-s2.0-22744459472 10.1038/sj.emboj.7600708
21. Deutsch G. B., Zielonka E. M., Coutandin D., Weber T. A., Schäfer B., Hannewald J., Luh L. M., Durst F. G., Ibrahim M., Hoffmann J., Niesen F. H., Sentürk A., Kunkel H., Brutschy B., Schleiff E., Knapp S., Acker-Palmer A., Grez M., McKeon F., Dötsch V., DNA damage in oocytes induces a switch of the quality control factor TAp63 α from dimer to tetramer. Cell 2011 144 4 566 576 2-s2.0-79951687016 10.1016/j.cell.2011.01.013
22. Gonfloni S., Di Tella L., Caldarola S., Cannata S. M., Klinger F. G., Di Bartolomeo C., Mattei M., Candi E., De Felici M., Melino G., Cesareni G., Inhibition of the c-Abl-TAp63 pathway protects mouse oocytes from chemotherapy-induced death. Nature Medicine 2009 15 10 1179 1185 2-s2.0-70350506325 10.1038/nm.2033
23. Deutsch G. B., Zielonka E. M., Coutandin D., Dötsch V., Quality control in oocytes: domain-domain interactions regulate the activity of p63. Cell Cycle 2011 10 12 1884 1885 2-s2.0-79959263193 10.4161/cc.10.12.15590
24. Su X., Paris M., Gi Y. J., Tsai K. Y., Cho M. S., Lin Y.-L., Biernaskie J. A., Sinha S., Prives C., Pevny L. H., Miller F. D., Flores E. R., TAp63 prevents premature aging by promoting adult stem cell maintenance. Cell Stem Cell 2009 5 1 64 75 2-s2.0-67649159970 10.1016/j.stem.2009.04.003
25. Su X., Gi Y. J., Chakravarti D., TAp63 is a master transcriptional regulator of lipid and glucose metabolism. Cell Metabolism 2012 16 511 525
26. Rossi M., Aqeilan R. I., Neale M., Candi E., Salomoni P., Knight R. A., Croce C. M., Melino G., The E3 ubiquitin ligase Itch controls the protein stability of p63. Proceedings of the National Academy of Sciences of the United States of America 2006 103 34 12753 12758 2-s2.0-33748065322 10.1073/pnas.0603449103
27. Romano R.-A., Smalley K., Magraw C., Serna V. A., Kurita T., Raghavan S., Sinha S., ΔNp63 knockout mice reveal its indispensable role as a master regulator of epithelial development and differentiation. Development 2012 139 4 772 782 2-s2.0-84856188471 10.1242/dev.071191
28. Westfall M. D., Mays D. J., Sniezek J. C., Pietenpol J. A., The ΔNp63 α phosphoprotein binds the p21 and 14-3-3 σ promoters in vivo and has transcriptional repressor activity that is reduced by Hay-Wells syndrome-derived mutations. Molecular and Cellular Biology 2003 23 7 2264 2276 2-s2.0-0037377761 10.1128/MCB.23.7.2264-2276.2003
29. Ratovitski E. A., Patturajan M., Hibi K., Trink B., Yamaguchi K., Sidransky D., p53 associates with and targets ΔNp63 into a protein degradation pathway. Proceedings of the National Academy of Sciences of the United States of America 2001 98 4 1817 1822 2-s2.0-0035852688 10.1073/pnas.98.4.1817
30. Bergholz J., Zhang Y., Wu J., ΔNp63 α regulates Erk signaling via MKP3 to inhibit cancer metastasis. Oncogene 2012 33 2 212 224 10.1038/onc.2012.564
31. Ihrie R. A., Marques M. R., Nguyen B. T., Horner J. S., Papazoglu C., Bronson R. T., Mills A. A., Attardi L. D., Perp is a p63-regulated gene essential for epithelial integrity. Cell 2005 120 6 843 856 2-s2.0-17644381260 10.1016/j.cell.2005.01.008
32. Wu G., Osada M., Guo Z., Fomenkov A., Begum S., Zhao M., Upadhyay S., Xing M., Wu F., Moon C., Westra W. H., Koch W. M., Mantovani R., Califano J. A., Ratovitski E., Sidransky D., Trink B., ΔNp63 α up-regulates the Hsp70 gene in human cancer. Cancer Research 2005 65 3 758 766 2-s2.0-13444250890
33. Ying H., Chang D. L. F., Zheng H., McKeon F., Xiao Z.-X. J., DNA-binding and transactivation activities are essential for TAp63 protein degradation. Molecular and Cellular Biology 2005 25 14 6154 6164 2-s2.0-21744440252 10.1128/MCB.25.14.6154-6164.2005
34. Okada Y., Osada M., Kurata S.-I., Sato S., Aisaki K.-I., Kageyama Y., Kihara K., Ikawa Y., Katoh I., p53 gene family p51(p63)-encoded, secondary transactivator p51b(TAp63 α) occurs without forming an immunoprecipitable complex with MDM2, but responds to genotoxic stress by accumulation. Experimental Cell Research 2002 276 2 194 200 2-s2.0-0036352550 10.1006/excr.2002.5535
35. Galli F., Rossi M., D'Alessandra Y., De Simone M., Lopardo T., Haupt Y., Alsheich-Bartok O., Anzi S., Shaulian E., Calabrò V., La Mantia G., Guerrini L., MDM2 and Fbw7 cooperate to induce p63 protein degradation following DNA damage and cell differentiation. Journal of Cell Science 2010 123 14 2423 2433 2-s2.0-77954894921 10.1242/jcs.061010
36. Bakkers J., Camacho-Carvajal M., Nowak M., Kramer C., Danger B., Hammerschmidt M., Destabilization of ΔNp63 α by Nedd4-mediated ubiquitination and Ubc9-mediated sumoylation, and its implications on dorsoventral patterning of the zebrafish embryo. Cell Cycle 2005 4 6 790 800 2-s2.0-25144501596
37. Rossi M., De Simone M., Pollice A., Santoro R., La Mantia G., Guerrini L., Calabrò V., Itch/AIP4 associates with and promotes p63 protein degradation. Cell Cycle 2006 5 16 1816 1822 2-s2.0-33748585368
38. Jeon Y. J., Jo M. G., Yoo H. M., Chemosensitivity is controlled by p63 modification with ubiquitin-like protein ISG15. The Journal of Clinical Investigation 2012 122 2622 2636
39. Ghioni P., D'Alessandra Y., Mansueto G., Jaffray E., Hay R. T., La Mantia G., Guerrini L., The protein stability and transcriptional activity of p63 α are regulated by SUMO-1 conjugation. Cell Cycle 2005 4 1 183 190 2-s2.0-17644407601
40. Leonard M. K., Hill N. T., Grant E. D., Kadakia M. P., DeltaNp63alpha represses nuclear translocation of PTEN by inhibition of NEDD4-1 in keratinocytes. Archives of Dermatological Research 2013 305 733 739
41. Rossi M., De Laurenzi V., Munarriz E., Green D. R., Liu Y.-C., Vousden K. H., Cesareni G., Melino G., The ubiquitin-protein ligase Itch regulates p73 stability. The EMBO Journal 2005 24 4 836 848 2-s2.0-15444367709 10.1038/sj.emboj.7600444
42. Li Y., Zhou Z., Chen C., WW domain-containing E3 ubiquitin protein ligase 1 targets p63 transcription factor for ubiquitin-mediated proteasomal degradation and regulates apoptosis. Cell Death and Differentiation 2008 15 12 1941 1951 2-s2.0-56349108922 10.1038/cdd.2008.134
43. Li X., Chen J., Yi Y., Li C., Zhang Y., DNA damage down-regulates ΔNp63 α and induces apoptosis independent of wild type p53. Biochemical and Biophysical Research Communications 2012 423 2 338 343 10.1016/j.bbrc.2012.05.126
44. Dobbelstein M., Wienzek S., König C., Roth J., Inactivation of the p53-homologue p73 by the mdm2-oncoprotein. Oncogene 1999 18 12 2101 2106 2-s2.0-0033602462
45. Wang X., Arooz T., Siu W. Y., Chiu C. H. S., Lau A., Yamashita K., Poon R. Y. C., MDM2 and MDMX can interact differently with ARF and members of the p53 family. FEBS Letters 2001 490 3 202 208 2-s2.0-0035895602 10.1016/S0014- 5793(01)02124-X
46. Calabrò V., Mansueto G., Parisi T., Vivo M., Calogero R. A., Mantia G. L., The human MDM2 oncoprotein increases the transcriptional activity and the protein level of the p53 homolog p63. Journal of Biological Chemistry 2002 277 4 2674 2681 2-s2.0-0037169519 10.1074/jbc.M107173200
47. Jung Y. S., Qian Y., Yan W., Chen X., Pirh2 E3 ubiquitin ligase modulates keratinocyte differentiation through p63. Journal of Investigative Dermatology 2013 133 1178 1187
48. Yan W., Chen X., Zhang Y., Zhang J., Jung Y. S., Arsenic suppresses cell survival via Pirh2-mediated proteasomal degradation of DeltaNp63 protein. The Journal of Biological Chemistry 2013 288 2907 2913
49. Huang Y., Sen T., Nagpal J., Upadhyay S., Trink B., Ratovitski E., Sidransky D., ATM kinase is a master switch for the ΔNp63 α phosphorylation/degradation in human head and neck squamous cell carcinoma cells upon DNA damage. Cell Cycle 2008 7 18 2846 2855 2-s2.0-51849085683
50. Craig A. L., Holcakova J., Finlan L. E., Nekulova M., Hrstka R., Gueven N., DiRenzo J., Smith G., Hupp T. R., Vojtesek B., ΔNp63 transcriptionally regulates ATM to control p53 Serine-15 phosphorylation. Molecular Cancer 2010 9, article 195 2-s2.0-77954680626 10.1186/1476-4598-9-195
51. MacPartlin M., Zeng S. X., Lu H., Phosphorylation and stabilization of TAp63 γ by I B kinase- β Journal of Biological Chemistry 2008 283 23 15754 15761 2-s2.0-47049128060 10.1074/jbc.M801394200
52. Chatterjee A., Chang X., Sen T., Ravi R., Bedi A., Sidransky D., Regulation of p53 family member isoform ΔNp63 α by the nuclear factor- B targeting kinase I B kinase β Cancer Research 2010 70 4 1419 1429 2-s2.0-76749100683 10.1158/0008-5472.CAN-09-2613
53. D'Orazi G., Cecchinelli B., Bruno T., Manni I., Higashimoto Y., Saito S., Gostissa M., Coen S., Marchetti A., Del Sal G., Piaggio G., Fanciulli M., Appella E., Soddu S., Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nature Cell Biology 2002 4 1 11 20 2-s2.0-18244379872 10.1038/ncb714
54. Hofmann T. G., Möller A., Sirma H., Zentgraf H., Taya Y., Dröge W., Will H., Lienhard Schmitz M., Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nature Cell Biology 2002 4 1 1 10 2-s2.0-0036141392 10.1038/ncb715
55. Lazzari C., Prodosmo A., Siepi F., Rinaldo C., Galli F., Gentileschi M., Bartolazzi A., Costanzo A., Sacchi A., Guerrini L., Soddu S., HIPK2 phosphorylates Δnp63 α and promotes its degradation in response to DNA damage. Oncogene 2011 30 48 4802 4813 2-s2.0-82455209036 10.1038/onc.2011.182
56. Simonatto M., Marullo F., Chiacchiera F., DNA damage-activated ABL-MyoD signaling contributes to DNA repair in skeletal myoblasts. Cell Death & Disease 2013 20 12 1664 1674 10.1038/cdd.2013.118
57. Reuven N., Adler J., Meltser V., Shaul Y., The Hippo pathway kinase Lats2 prevents DNA damage-induced apoptosis through inhibition of the tyrosine kinase c-Abl. Cell Death & Disease 2013 20 1330 1340
58. Yuan M., Luong P., Hudson C., Gudmundsdottir K., Basu S., C-Abl phosphorylation of Δnp63 α is critical for cell viability. Cell Death and Disease 2010 1 1, article e16 2-s2.0-77954784171 10.1038/cddis.2009.15
59. Komatsu S., Takenobu H., Ozaki T., Ando K., Koida N., Suenaga Y., Ichikawa T., Hishiki T., Chiba T., Iwama A., Yoshida H., Ohnuma N., Nakagawara A., Kamijo T., Plk1 regulates liver tumor cell death by phosphorylation of TAp63. Oncogene 2009 28 41 3631 3641 2-s2.0-70350057293 10.1038/onc.2009.216
60. Hildesheim J., Belova G. I., Tyner S. D., Zhou X., Vardanian L., Fornace A. J. Jr., Gadd45a regulates matrix metalloproteinases by suppressing ΔNp63 α and β -catenin via p38 MAP kinase and APC complex activation. Oncogene 2004 23 10 1829 1837 2-s2.0-1842429927 10.1038/sj.onc. 1207301
61. Fomenkov A., Zangen R., Huang Y.-P., Osada M., Guo Z., Fomenkov T., Trink B., Sidransky D., Ratovitski E. A., RACK1 and stratifin target ΔNp63 α for a proteasome degradation in head and neck squamous cell carcinoma cells upon DNA damage. Cell Cycle 2004 3 10 1285 1295 2-s2.0-13944255793
62. Serrels B., Sandilands E., Serrels A., Baillie G., Houslay M. D., Brunton V. G., Canel M., MacHesky L. M., Anderson K. I., Frame M. C., A complex between FAK, RACK1, and PDE4D5 controls spreading initiation and cancer cell polarity. Current Biology 2010 20 12 1086 1092 2-s2.0-77954543000 10.1016/j.cub.2010.04. 042
63. Dohn M., Zhang S., Chen X., p63 α and ΔNp63 α can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes. Oncogene 2001 20 25 3193 3205 2-s2.0-0034743628 10.1038/sj.onc.1204427
64. Li Y., Peart M. J., Prives C., Stxbp4 regulates ΔNp63 stability by suppression of RACK1-dependent degradation. Molecular and Cellular Biology 2009 29 14 3953 3963 2-s2.0-67650088240 10.1128/MCB.00449-09
65. Wang N., Guo L., Rueda B. R., Tilly J. L., Cables1 protects p63 from proteasomal degradation to ensure deletion of cells after genotoxic stress. EMBO Reports 2010 11 8 633 639 2-s2.0-77955055804 10.1038/embor.2010.82
66. Bernassola F., Oberst A., Melino G., Pandolfi P. P., The promyelocytic leukaemia protein tumour suppressor functions as a transcriptional regulator of p63. Oncogene 2005 24 46 6982 6986 2-s2.0-27144507300 10.1038/sj.onc.1208843
67. Li C., Chang D. L., Yang Z., Pin1 modulates p63alpha protein stability in regulation of cell survival, proliferation and tumor formation. Cell Death & Disease 2013 4 e943
68. Nylander K., Vojtesek B., Nenutil R., Lindgren B., Roos G., Zhanxiang W., Sjöström B., Dahlqvist Å., Coates P. J., Differential expression of p63 isoforms in normal tissues and neoplastic cells. Journal of Pathology 2002 198 4 417 427 2-s2.0-0036900291 10.1002/path.1231
69. Michaelis M., Rothweiler F., Barth S., Cinat J., Van Rikxoort M., Löschmann N., Voges Y., Breitling R., Von Deimling A., Rödel F., Weber K., Fehse B., MacK E., Stiewe T., Doerr H. W., Speidel D., Cinatl J., Adaptation of cancer cells from different entities to the MDM2 inhibitor nutlin-3 results in the emergence of p53-mutated multi-drug-resistant cancer cells. Cell Death and Disease 2011 2 12, article e243 2-s2.0-84856098041 10.1038/cddis.2011.129