Crosstalk between c-Jun and TAp73α/β contributes to the apoptosis-survival balance

Nucleic Acids Research

Volumn 39, Issue 14, 2011, Pages 6069-6085

  Koeppel, Max ^a   Van Heeringen, Simon J ^a   Kramer, Daniela ^b   Smeenk, Leonie ^a   Janssen Megens, Eva ^a   Hartmann, Marianne ^b   Stunnenberg, Hendrik G ^a   Lohrum, Marion ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

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

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MESSENGER RNA; PROTEIN AP1; PROTEIN C JUN; PROTEIN TAP73ALPHA; PROTEIN TAP73BETA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BINDING SITE; CELL SURVIVAL; CONSENSUS SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE TARGETING; GENOMICS; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; RNA SEQUENCE; RNA TRANSCRIPTION; UPREGULATION;

APOPTOSIS; BINDING SITES; CELL LINE; CELL SURVIVAL; DNA-BINDING PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HUMANS; INTERLEUKIN-1 RECEPTOR ACCESSORY PROTEIN; NUCLEAR PROTEINS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-JUN; REGULATORY ELEMENTS, TRANSCRIPTIONAL; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 80051730985     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr028     Document Type: Article

References (75)

1. Deyoung, M.P. and Ellisen, L.W. (2007) p63 and p73 in human cancer: defining the network. Oncogene, 26, 5169-5183. (Pubitemid 47237632)
2. Moll, U. and Slade, N. (2004) p63 and p73: roles in development and tumor formation. Mol. Cancer Res., 2, 371-386. (Pubitemid 39031071)
3. Zaika, A.I., Slade, N., Erster, S.H., Sansome, C., Joseph, T.W., Pearl, M., Chalas, E. and Moll, U.M. (2002) DeltaNp73, a dominant-negative inhibitor of wild-type p53 and TAp73, is up-regulated in human tumors. J. Exp. Med., 196, 765-780.
4. Concin, N., Becker, K., Slade, N., Erster, S., Mueller-Holzner, E., Ulmer, H., Daxenbichler, G., Zeimet, A., Zeillinger, R., Marth, C. et al. (2004) Transdominant DeltaTAp73 isoforms are frequently up-regulated in ovarian cancer. Evidence for their role as epigenetic p53 inhibitors in vivo. Cancer Res., 64, 2449-2460. (Pubitemid 38523899)
5. Melino, G., De Laurenzi, V. and Vousden, K.H. (2002) p73: Friend or foe in tumorigenesis. Nat. Rev. Cancer, 2, 605-615. (Pubitemid 37328927)
6. Flores, E.R., Tsai, K.Y., Crowley, D., Sengupta, S., Yang, A., McKeon, F. and Jacks, T. (2002) p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature, 416, 560-564. (Pubitemid 34288861)
7. Flores, E.R., Sengupta, S., Miller, J.B., Newman, J.J., Bronson, R., Crowley, D., Yang, A., McKeon, F. and Jacks, T. (2005) Tumor predisposition in mice mutant for p63 and p73: evidence for broader tumor suppressor functions for the p53 family. Cancer Cell, 7, 363-373. (Pubitemid 40544653)
8. 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)
9. Tomasini, R., Tsuchihara, K., Wilhelm, M., Fujitani, M., Rufini, A., Cheung, C., Khan, F., Itie-Youten, A., Wakeham, A., Tsao, M. et al. (2008) TAp73 knockout shows genomic instability with infertility and tumor suppressor functions. Genes Dev., 22, 2677-2691.
10. Agami, R., Blandino, G., Oren, M. and Shaul, Y. (1999) Interaction of c-Abl and p73alpha and their collaboration to induce apoptosis. Nature, 399, 809-813.
11. Yuan, Z.M., Shioya, H., Ishiko, T., Sun, X., Gu, J., Huang, Y.Y., Lu, H., Kharbanda, S., Weichselbaum, R. and Kufe, D. (1999) p73 is regulated by tyrosine kinase c-Abl in the apoptotic response to DNA damage. Nature, 399, 814-817. (Pubitemid 29293181)
12. Gong, J.G., Costanzo, A., Yang, H.Q., Melino, G., Kaelin, W.G., Levrero, M. and Wang, J.Y. (1999) The tyrosine kinase c-Abl regulates p73 in apoptotic response to cisplatin-induced DNA damage. Nature, 399, 806-809. (Pubitemid 29293179)
13. Pediconi, N., Ianari, A., Costanzo, A., Belloni, L., Gallo, R., Cimino, L., Porcellini, A., Screpanti, I., Balsano, C., Alesse, E. et al. (2003) Differential regulation of E2F1 apoptotic target genes in response to DNA damage. Nat. Cell. Biol., 5, 552-558. (Pubitemid 36781090)
14. Irwin, M.S., Kondo, K., Marin, M.C., Cheng, L.S., Hahn, W.C. and Kaelin, W.G. (2003) Chemosensitivity linked to p73 function. Cancer Cell, 3, 403-410. (Pubitemid 38340308)
15. De Laurenzi, V., Costanzo, A., Barcaroli, D., Terrinoni, A., Falco, M., Annicchiarico-Petruzzelli, M., Levrero, M. and Melino, G. (1998) Two new p73 splice variants, gamma and delta, with different transcriptional activity. J. Exp. Med., 188, 1763-1768. (Pubitemid 28516121)
16. Melino, G., Bernassola, F., Ranalli, M., Yee, K., Zong, W.X., Corazzari, M., Knight, R.A., Green, D.R., Thompson, C. and Vousden, K.H. (2004) p73 Induces apoptosis via PUMA transactivation and Bax mitochondrial translocation. J. Biol. Chem., 279, 8076-8083. (Pubitemid 38294697)
17. Flinterman, M., Guelen, L., Ezzati-Nik, S., Killick, R., Melino, G., Tominaga, K., Mymryk, J.S., Gaken, J. and Tavassoli, M. (2005) E1A activates transcription of p73 and Noxa to induce apoptosis. J. Biol. Chem., 280, 5945-5959. (Pubitemid 40280079)
18. Blint, E., Phillips, A.C., Kozlov, S., Stewart, C.L. and Vousden, K.H. (2002) Induction of p57(KIP2) expression by p73beta. Proc. Natl Acad. Sci. USA, 99, 3529-3534.
19. Toh, W.H., Logette, E., Corcos, L. and Sabapathy, K. (2008) TAp73beta and DNp73beta activate the expression of the pro-survival caspase-2S. Nucleic Acids Res., 36, 4498-4509.
20. Nyman, U., Sobczak-Pluta, A., Vlachos, P., Perlmann, T., Zhivotovsky, B. and Joseph, B. (2005) Full-length p73alpha represses drug-induced apoptosis in small cell lung carcinoma cells. J. Biol. Chem., 280, 34159-34169. (Pubitemid 41443140)
21. Vikhanskaya, F., Toh, W., Dulloo, I., Wu, Q., Boominathan, L., Ng, H., Vousden, K. and Sabapathy, K. (2007) p73 supports cellular growth through c-Jun-dependent AP-1 transactivation. Nat. Cell. Biol., 9, 698-706. (Pubitemid 47214733)
22. Toh, W.H., Siddique, M.M., Boominathan, L., Lin, K.W. and Sabapathy, K. (2004) c-Jun regulates the stability and activity of the p53 homologue, p73. J. Biol. Chem., 279, 44713-44722. (Pubitemid 39430881)
23. Shaulian, E. and Karin, M. (2002) AP-1 as a regulator of cell life and death. Nat. Cell. Biol., 4, E131-E136. (Pubitemid 34521026)
24. Wisdom, R., Johnson, R.S. and Moore, C. (1999) c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J., 18, 188-197. (Pubitemid 29005035)
25. Johnson, R.S., van Lingen, B., Papaioannou, V.E. and Spiegelman, B.M. (1993) A null mutation at the c-jun locus causes embryonic lethality and retarded cell growth in culture. Genes Dev., 7, 1309-1317. (Pubitemid 23210880)
26. Schreiber, M., Kolbus, A., Piu, F., Szabowski, A., Mö hle-Steinlein, U., Tian, J., Karin, M., Angel, P. and Wagner, E.F. (1999) Control of cell cycle progression by c-Jun is p53 dependent. Genes Dev., 13, 607-619. (Pubitemid 29131884)
27. Shaulian, E., Schreiber, M., Piu, F., Beeche, M., Wagner, E.F. and Karin, M. (2000) The mammalian UV response: c-Jun induction is required for exit from p53-imposed growth arrest. Cell, 103, 897-907.
28. Smeenk, L., Van Heeringen, S., Koeppel, M., Van Driel, M., Bartels, S., Akkers, R., Denissov, S., Stunnenberg, H. and Lohrum, M. (2008) Characterization of genome-wide p53-binding sites upon stress response. Nucleic Acids Res., 36, 3639-3654. (Pubitemid 351917528)
29. Denissov, S., van Driel, M., Voit, R., Hekkelman, M., Hulsen, T., Hernandez, N., Grummt, I., Wehrens, R. and Stunnenberg, H. (2007) Identification of novel functional TBP-binding sites and general factor repertoires. EMBO J., 26, 944-954.
30. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nussbaum, C., Myers, R.M., Brown, M., Li, W. et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Bio., 9, R137.
31. Wang, L., Feng, Z., Wang, X., Wang, X. and Zhang, X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics, 26, 136-138.
32. Ouyang, Z., Zhou, Q. and Wong, W.H. (2009) ChIP-Seq of transcription factors predicts absolute and differential gene expression in embryonic stem cells. Proc. Natl Acad. Sci. USA, 22, 21521-21526.
33. Thijs, G., Lescot, M., Marchal, K., Rombauts, S., De Moor, B., Rouze, P. and Moreau, Y. (2001) A higher-order background model improves the detection of promoter regulatory elements by Gibbs sampling. Bioinformatics, 17, 1113-1122. (Pubitemid 33735337)
34. Pavesi, G., Mereghetti, P., Mauri, G. and Pesole, G. (2004) Weeder Web: discovery of transcription factor binding sites in a set of sequences from co-regulated genes. Nucleic Acids Res., 32, W199-203. (Pubitemid 38997329)
35. Liu, X., Brutlag, D. and Liu, J. (2002) An algorithm for finding protein-DNA binding sites with applications to chromatin-immunoprecipitation microarray experiments. Nat. Biotechnol., 5, 835-839. (Pubitemid 34836763)
36. Vlieghe, D., Sandelin, A., De Bleser, P.J., Vleminckx, K., Wasserman, W.W., van Roy, F. and Lenhard, B. (2006) A new generation of JASPAR, the open-access repository for transcription factor binding site profiles. Nucleic Acids Res., 34, D95-D97.
37. Mahony, S. and Benos, P.V. (2007) STAMP: a web tool for exploring DNA-binding motif similarities. Nucleic Acids Res., 35, W253-W258.
38. Edgar, R., Domrachev, M. and Lash, A.E. (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res., 30, 207-210. (Pubitemid 34679544)
39. Dennis, G. Jr, Sherman, B.T., Hosack, D.A., Yang, J., Gao, W., Lane, H.C. and Lempicki, R.A. (2003) DAVID: Database for annotation, visualization, and integrated discovery. Genome Bio., 4, P3.
40. Huang da, W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
41. Kanehisa, M., Goto, S., Hattori, M., Aoki-Kinoshita, K.F., Itoh, M., Kawashima, S., Katayama, T., Araki, M. and Hirakawa, M. (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res., 34, D354-D357.
42. Nakabeppu, Y., Ryder, K. and Nathans, D. (1988) DNA binding activities of three murine Jun proteins: stimulation by Fos. Cell, 55, 907-915.
43. Barenco, M., Brewer, D., Papouli, E., Tomescu, D., Callard, R., Stark, J. and Hubank, M. (2009) Dissection of a complex transcriptional response using genome-wide transcriptional modelling. Mol. Syst. Bio., 5, 327.
44. Klanrit, P., Flinterman, M.B., Odell, E.W., Melino, G., Killick, R., Norris, J.S. and Tavassoli, M. (2008) Specific isoforms of p73 control the induction of cell death induced by the viral proteins, E1A or apoptin. Cell Cycle, 7, 205-215. (Pubitemid 351366521)
45. 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)
46. Lim, J.T., Mansukhani, M. and Weinstein, I.B. (2005) Cyclin-dependent kinase 6 associates with the androgen receptor and enhances its transcriptional activity in prostate cancer cells. Proc. Natl Acad. Sci. USA, 102, 5156-5161.
47. Sugiura, T., Yamaguchi, A. and Miyamoto, K. (2008) A cancer-associated RING finger protein, RNF43, is a ubiquitin ligase that interacts with a nuclear protein, HAP95. Exp. Cell Res., 314, 1519-1528.
48. Lee, C.W. and La Thangue, N.B. (1999) Promoter specificity and stability control of the p53-related protein p73. Oncogene, 18, 4171-4181. (Pubitemid 29377848)
49. Ueda, Y., Hijikata, M., Takagi, S., Chiba, T. and Shimotohno, K. (1999) New p73 variants with altered C-terminal structures have varied transcriptional activities. Oncogene, 18, 4993-4998. (Pubitemid 29425306)
50. Fontemaggi, G., Kela, I., Amariglio, N., Rechavi, G., Krishnamurthy, J., Strano, S., Sacchi, A., Givol, D. and Blandino, G. (2002) Identification of direct p73 target genes combining DNA microarray and chromatin immunoprecipitation analyses. J. Biol. Chem., 277, 43359-43368. (Pubitemid 35285724)
51. Oshima, Y., Sasaki, Y., Negishi, H., Idogawa, M., Toyota, M., Yamashita, T., Wada, T., Nagoya, S., Kawaguchi, S., Yamashita, T. et al. (2007) Antitumor effect of adenovirus-mediated p53 family gene transfer on osteosarcoma cell lines. Cancer Biol. Ther., 6, 1058-1066. (Pubitemid 351574957)
52. Gonzalez, S., Perez-Perez, M.M., Hernando, E., Serrano, M. and Cordon-Cardo, C. (2005) p73beta-Mediated apoptosis requires p57kip2 induction and IEX-1 inhibition. Cancer Res., 65, 2186-2192. (Pubitemid 40490126)
53. Scian, M., Carchman, E., Mohanraj, L., Stagliano, K., Anderson, M., Deb, D., Crane, B., Kiyono, T., Windle, B., Deb, S. et al. (2008) Wild-type p53 and p73 negatively regulate expression of proliferation related genes. Oncogene, 27, 2583-2593. (Pubitemid 351550876)
54. Danovi, S.A., Rossi, M., Gudmundsdottir, K., Yuan, M., Melino, G. and Basu, S. (2008) Yes-associated protein (YAP) is a critical mediator of c-Jun-dependent apoptosis. Cell Death Differ., 15, 217-219. (Pubitemid 350286191)
55. Strano, S., Monti, O., Pediconi, N., Baccarini, A., Fontemaggi, G., Lapi, E., Mantovani, F., Damalas, A., Citro, G. and Sacchi, A. (2005) The transcriptional coactivator yes-associated protein drives p73 gene-target specificity in response to DNA damage. Mol. Cell, 18, 447-459. (Pubitemid 40704759)
56. Crooks, G.E., Hon, G., Chandonia, J.M. and Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190. (Pubitemid 38811555)
57. Yagyu, R., Furukawa, Y., Lin, Y.M., Shimokawa, T., Yamamura, T. and Nakamura, Y. (2004) A novel oncoprotein RNF43 functions in an autocrine manner in colorectal cancer. Int. J. Oncol., 25, 1343-1348.
58. Arévalo, J.C., Waite, J., Rajagopal, R., Beyna, M., Chen, Z.Y., Lee, F.S. and Chao, M.V. (2006) Cell survival through Trk neurotrophin receptors is differentially regulated by ubiquitination. Neuron, 50, 549-559.
59. Lee, H.S., Park, M.H., Yang, S.J., Park, K.C., Kim, N.S., Kim, Y.S., Kim, D.I., Yoo, H.S., Choi, E.J. and Yeom, Y.I. (2007) Novel candidate targets of Wnt/beta-catenin signaling in hepatoma cells. Life Sci., 80, 690-698. (Pubitemid 46074058)
60. Mendrzyk, F., Radlwimmer, B., Joos, S., Kokocinski, F., Benner, A., Stange, D.E., Neben, K., Fiegler, H., Carter, N.P., Reifenberger, G. et al. (2005) Genomic and protein expression profiling identifies CDK6 as novel independent prognostic marker in medulloblastoma. J. Clin. Oncol., 23, 8853-8862. (Pubitemid 46211532)
61. Cullinan, E.B., Kwee, L., Nunes, P., Shuster, D.J., Ju, G., McIntyre, K.W., Chizzonite, R.A. and Labow, M.A. (1998) IL-1 receptor accessory protein is an essential component of the IL-1 receptor. J. Immunol., 161, 5614-5620. (Pubitemid 28519127)
62. Towne, J.E., Garka, K.E., Renshaw, B.R., Virca, G.D. and Sims, J.E. (2004) Interleukin (IL)-1F6, IL-1F8, and IL-1F9 signal through IL-1Rrp2 and IL-1RAcP to activate the pathway leading to NF-kappaB and MAPKs. J. Biol. Chem., 279, 13677-13688. (Pubitemid 38468896)
63. Bajou, K., Noel, A., Gerard, R.D., Masson, V., Brunner, N., Holst-Hansen, C., Skobe, M., Fusenig, N.E., Carmeliet, P., Collen, D. et al. (1998) Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nature Med., 4, 923-928. (Pubitemid 28364031)
64. Gutierrez, L.S., Schulman, A., Brito-Robinson, T., Noria, F., Ploplis, V.A. and Castellino, F.J. (2000) Tumor development is retarded in mice lacking the gene for urokinase-type plasminogen activator or its inhibitor, plasminogen activator inhibitor-1. Cancer Res., 60, 5839-5847.
65. Kortlever, R.M. and Bernards, R. (2006) Senescence, wound healing and cancer: the PAI-1 connection. Cell Cycle, 5, 2697-2703. (Pubitemid 44901726)
66. Nekarda, H., Siewert, J.R., Schmitt, M. and Ulm, K. (1994) Tumour-associated proteolytic factors uPA and PAI-1 and survival in totally resected gastric cancer. Lancet, 343, 117. (Pubitemid 24019365)
67. Adams, S., Pankow, S., Werner, S. and Munz, B. (2007) Regulation of NF-kappaB activity and keratinocyte differentiation by the RIP4 protein: implications for cutaneous wound repair. J. Invest. Dermatol., 127, 538-544.
68. Meylan, E., Martinon, F., Thome, M., Gschwendt, M. and Tschopp, J. (2002) RIP4 (DIK/PKK), a novel member of the RIP kinase family, activates NF-kappa B and is processed during apoptosis. EMBO Rep., 3, 1201-1208. (Pubitemid 36105011)
69. Diolaiti, D., Bernardoni, R., Trazzi, S., Papa, A., Porro, A., Bono, F., Herbert, J.M., Perini, G. and Della Valle, G. (2007) Functional cooperation between TrkA and p75(NTR) accelerates neuronal differentiation by increased transcription of GAP-43 and p21(CIP/WAF) genes via ERK1/2 and AP-1 activities. Exp. Cell. Res., 313, 2980-2992. (Pubitemid 47125888)
70. Choi, D., Kim, J., Ryu, H., Kim, H., Han, J., Lee, J. and Min, C. (2007) Syndecan-1, a key regulator of cell viability in endometrial cancer. Int. J. Cancer, 121, 741-750. (Pubitemid 47106202)
71. Maeda, T., Desouky, J. and Friedl, A. (2006) Syndecan-1 expression by stromal fibroblasts promotes breast carcinoma growth in vivo and stimulates tumor angiogenesis. Oncogene, 25, 1408-1412. (Pubitemid 43336469)
72. Dimaras, H. and Gallie, B.L. (2008) The p75 NTR neurotrophin receptor is a tumor suppressor in human and murine retinoblastoma development. Int. J. Cancer, 122, 2023-2029. (Pubitemid 351441191)
73. Johnston, A.L., Lun, X., Rahn, J.J., Liacini, A., Wang, L., Hamilton, M.G., Parney, I.F., Hempstead, B.L., Robbins, S.M., Forsyth, P.A. et al. (2007) The p75 neurotrophin receptor is a central regulator of glioma invasion. PLoS Biol., 5, e212.
74. Khwaja, F., Tabassum, A., Allen, J. and Djakiew, D. (2006) The p75(NTR) tumor suppressor induces cell cycle arrest facilitating caspase mediated apoptosis in prostate tumor cells. Biochem. Biophys. Res. Commun., 341, 1184-1192. (Pubitemid 43221790)
75. Okumura, T., Tsunoda, S., Mori, Y., Ito, T., Kikuchi, K., Wang, T.C., Yasumoto, S. and Shimada, Y. (2006) The biological role of the low-affinity p75 neurotrophin receptor in esophageal squamous cell carcinoma. Clin. Cancer Res., 12, 5096-5103. (Pubitemid 44453336)