Novel targets and interaction partners of mutant p53 Gain-Of-Function

Biochemical Society Transactions

Volumn 44, Issue 2, 2016, Pages 460-466

  Aschauer, Lydia ^a   Muller, Patricia A J ^a  

^a MRC TOXICOLOGY UNIT   (United Kingdom)

Author keywords

Gain Of Function; Hallmarks of cancer; Mutant p53

Indexed keywords

PROTEIN P53; PROTEIN BINDING;

ANGIOGENESIS; APOPTOSIS; CARCINOGENESIS; CELL DEATH; CELL PROLIFERATION; CHROMATIN; CLINICAL RESEARCH; ENERGY TRANSFER; GAIN OF FUNCTION MUTATION; GENE REPLICATION; GENOMIC INSTABILITY; HUMAN; IMMUNE RESPONSE; INFLAMMATION; MALIGNANT NEOPLASM; METASTASIS; NONHUMAN; NUCLEAR REPROGRAMMING; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; TUMOR INVASION; TUMOR SUPPRESSOR GENE; CHROMATIN ASSEMBLY AND DISASSEMBLY; ENERGY METABOLISM; METABOLISM; MUTATION; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; VASCULARIZATION;

APOPTOSIS; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; ENERGY METABOLISM; GENOMIC INSTABILITY; HUMANS; MUTATION; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN BINDING; TUMOR SUPPRESSOR PROTEIN P53;

EID: 85009843942     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20150261     Document Type: Review

References (75)

1. Muller, P.A. and Vousden, K.H. (2013) p53 mutations in cancer. Nat. Cell Biol. 15, 2-8
2. Hanahan, D. and Weinberg, R.A. (2000) The hallmarks of cancer. Cell 100, 57-70
3. Hanahan, D. and Weinberg, R.A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
4. Solomon, H., Madar, S. and Rotter, V. (2011) Mutant p53 gain of function is interwoven into the hallmarks of cancer. J. Pathol. 225, 475-478
5. Lang, G.A., Iwakuma, T., Suh, Y.A., Liu, G., Rao, V.A., Parant, J.M., Valentin-Vega, Y.A., Terzian, T., Caldwell, L.C., Strong, L.C. et al. (2004) Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 119, 861-872
6. Olive, K.P., Tuveson, D.A., Ruhe, Z.C., Yin, B., Willis, N.A., Bronson, R.T., Crowley, D. and Jacks, T. (2004) Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 119, 847-860
7. Muller, P.A., Caswell, P.T., Doyle, B., Iwanicki, M.P., Tan, E.H., Karim, S., Lukashchuk, N., Gillespie, D.A., Ludwig, R.L., Gosselin, P. et al. (2009) Mutant p53 drives invasion by promoting integrin recycling. Cell 139, 1327-1341
8. Muller, P.A., Trinidad, A.G., Caswell, P.T., Norman, J.C. and Vousden, K.H. (2013) Mutant p53 regulates Dicer through p63 dependent and independent mechanisms to promote an invasive phenotype. J. Biol. Chem. 289, 122-132
9. Muller, P.A., Trinidad, A.G., Timpson, P., Morton, J.P., Zanivan, S., van den Berghe, P.V., Nixon, C., Karim, S.A., Caswell, P.T., Noll, J.E. et al. (2012) Mutant p53 enhances MET trafficking and signalling to drive cell scattering and invasion. Oncogene 32, 1252-1265
10. Tan, E.H., Morton, J.P., Timpson, P., Tucci, P., Melino, G., Flores, E.R., Sansom, O.J., Vousden, K.H. and Muller, P.A. (2013) Functions of TAp63 and p53 in restraining the development of metastatic cancer. Oncogene 33, 3325-3333
11. Gaiddon, C., Lokshin, M., Ahn, J., Zhang, T. and Prives, C. (2001) A subset of tumor-derived mutant forms of p53 down-regulate p63 and p73 through a direct interaction with the p53 core domain. Mol. Cell Biol. 21, 1874-1887
12. Xu, J., Reumers, J., Couceiro, J.R., De Smet, F., Gallardo, R., Rudyak, S., Cornelis, A., Rozenski, J., Zwolinska, A., Marine, J.C. et al. (2011) Gain of function of mutant p53 by coaggregation with multiple tumor suppressors. Nat. Chem. Biol. 7, 285-295
13. Adorno, M., Cordenonsi, M., Montagner, M., Dupont, S., Wong, C., Hann, B., Solari, A., Bobisse, S., Rondina, M.B., Guzzardo, V. et al. (2009) A mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis. Cell 137, 87-98
14. Ji, L., Xu, J., Liu, J., Amjad, A., Zhang, K., Liu, Q., Zhou, L., Xiao, J. and Li, X. (2015) Mutant p53 promotes tumor cell malignancy by both positive and negative regulation of the transforming growth factor beta (TGF-beta) pathway. J. Biol. Chem. 290, 11729-11740
15. Wei, S., Wang, H., Lu, C., Malmut, S., Zhang, J., Ren, S., Yu, G., Wang, W., Tang, D.D. and Yan, C. (2014) The activating transcription factor 3 protein suppresses the oncogenic function of mutant p53 proteins. J. Biol. Chem. 289, 8947-8959
16. Stindt, M.H., Muller, P.A., Ludwig, R.L., Kehrloesser, S., Dotsch, V. and Vousden, K.H. (2015) Functional interplay between MDM2, p63/p73 and mutant p53. Oncogene 34, 4300-4310
17. Subramanian, M., Francis, P., Bilke, S., Li, X.L., Hara, T., Lu, X., Jones, M.F., Walker, R.L., Zhu, Y., Pineda, M. et al. (2015) A mutant p53/let-7i-axis-regulated gene network drives cell migration, invasion and metastasis. Oncogene 34, 1094-1104
18. Di Agostino, S., Strano, S., Emiliozzi, V., Zerbini, V., Mottolese, M., Sacchi, A., Blandino, G. and Piaggio, G. (2006) Gain of function of mutant p53: the mutant p53/NF-Y protein complex reveals an aberrant transcriptional mechanism of cell cycle regulation. Cancer Cell 10, 191-202
19. Weissmueller, S., Manchado, E., Saborowski, M., Morris, J.P.T., Wagenblast, E., Davis, C.A., Moon, S.H., Pfister, N.T., Tschaharganeh, D.F., Kitzing, T. et al. (2014) Mutant p53 drives pancreatic cancer metastasis through cell-autonomous PDGF receptor beta signaling. Cell 157, 382-394
20. Huang, X., Zhang, Y., Tang, Y., Butler, N., Kim, J., Guessous, F., Schiff, D., Mandell, J. and Abounader, R. (2013) A novel PTEN/mutant p53/c-Myc/Bcl-XL axis mediates context-dependent oncogenic effects of PTEN with implications for cancer prognosis and therapy. Neoplasia 15, 952-965
21. Alam, S.K., Yadav, V.K., Bajaj, S., Datta, A., Dutta, S.K., Bhattacharyya, M., Bhattacharya, S., Debnath, S., Roy, S., Boardman, L.A. et al. (2015) DNA damage-induced ephrin-B2 reverse signaling promotes chemoresistance and drives EMT in colorectal carcinoma harboring mutant p53. Cell Death Differ. 23, epub ahead of print
22. Freed-Pastor, W.A., Mizuno, H., Zhao, X., Langerod, A., Moon, S.H., Rodriguez-Barrueco, R., Barsotti, A., Chicas, A., Li, W., Polotskaia, A. et al. (2012) Mutant p53 disrupts mammary tissue architecture via the mevalonate pathway. Cell 148, 244-258
23. Zhao, Y., Zhang, C., Yue, X., Li, X., Liu, J., Yu, H., Belyi, V.A., Yang, Q., Feng, Z. and Hu, W. (2015) Pontin, a new mutant p53-binding protein, promotes gain-of-function of mutant p53. Cell Death Differ. 22, 1824-1836
24. Xiong, S., Tu, H., Kollareddy, M., Pant, V., Li, Q., Zhang, Y., Jackson, J.G., Suh, Y.A., Elizondo-Fraire, A.C., Yang, P. et al. (2014) Pla2g16 phospholipase mediates gain-of-function activities of mutant p53. Proc. Natl. Acad. Sci. U.S.A. 111, 11145-11150
25. Kollareddy, M., Dimitrova, E., Vallabhaneni, K.C., Chan, A., Le, T., Chauhan, K.M., Carrero, Z.I., Ramakrishnan, G., Watabe, K., Haupt, Y. et al. (2015) Regulation of nucleotide metabolism by mutant p53 contributes to its gain-of-function activities. Nat. Commun. 6, 7389
26. Arjonen, A., Kaukonen, R., Mattila, E., Rouhi, P., Hognas, G., Sihto, H., Miller, B.W., Morton, J.P., Bucher, E., Taimen, P. et al. (2014) Mutant p53-associated myosin-X upregulation promotes breast cancer invasion and metastasis. J. Clin. Invest. 124, 1069-1082
27. Ali, A., Shah, A.S. and Ahmad, A. (2014) Gain-of-function of mutant p53: mutant p53 enhances cancer progression by inhibiting KLF17 expression in invasive breast carcinoma cells. Cancer Lett. 354, 87-96
28. Wang, H., Bao, W., Jiang, F., Che, Q., Chen, Z., Wang, F., Tong, H., Dai, C., He, X., Liao, Y. et al. (2015) Mutant p53 (p53-R248Q) functions as an oncogene in promoting endometrial cancer by up-regulating REGgamma. Cancer Lett. 360, 269-279
29. Frazier, M.W., He, X., Wang, J., Gu, Z., Cleveland, J.L. and Zambetti, G.P. (1998) Activation of c-myc gene expression by tumor-derived p53 mutants requires a discrete C-terminal domain. Mol. Cell Biol. 18, 3735-3743
30. Deb, S., Jackson, C.T., Subler, M.A. and Martin, D.W. (1992) Modulation of cellular and viral promoters by mutant human p53 proteins found in tumor cells. J. Virol. 66, 6164-6170
31. Ludes-Meyers, J.H., Subler, M.A., Shivakumar, C.V., Munoz, R.M., Jiang, P., Bigger, J.E., Brown, D.R., Deb, S.P. and Deb, S. (1996) Transcriptional activation of the human epidermal growth factor receptor promoter by human p53. Mol. Cell Biol. 16, 6009-6019
32. Wang, W., Cheng, B., Miao, L., Mei, Y. and Wu, M. (2013) Mutant p53-R273H gains new function in sustained activation of EGFR signaling via suppressing miR-27a expression. Cell Death Dis. 4, e574
33. Vaughan, C.A., Singh, S., Windle, B., Yeudall, W.A., Frum, R., Grossman, S.R., Deb, S.P. and Deb, S. (2012) Gain-of-function activity of mutant p53 in lung cancer through up-regulation of receptor protein tyrosine kinase Axl. Genes Cancer 3, 491-502
34. Di Como, C.J., Gaiddon, C. and Prives, C. (1999) p73 function is inhibited by tumor-derived p53 mutants in mammalian cells. Mol. Cell. Biol. 19, 1438-1449
35. Irwin, M.S., Kondo, K., Marin, M.C., Cheng, L.S., Hahn, W.C. and Kaelin, Jr, W.G. (2003) Chemosensitivity linked to p73 function. Cancer Cell 3, 403-410
36. Alexandrova, E.M., Yallowitz, A.R., Li, D., Xu, S., Schulz, R., Proia, D.A., Lozano, G., Dobbelstein, M. and Moll, U.M. (2015) Improving survival by exploiting tumour dependence on stabilized mutant p53 for treatment. Nature 523, 352-356
37. Ali, A., Wang, Z., Fu, J., Ji, L., Liu, J., Li, L., Wang, H., Chen, J., Caulin, C., Myers, J.N. et al. (2013) Differential regulation of the REGgamma-proteasome pathway by p53/TGF-beta signalling and mutant p53 in cancer cells. Nat. Commun. 4, 2667
38. Oren, M. and Rotter, V. (2010) Mutant p53 gain-of-function in cancer. Cold Spring Harb. Perspect. Biol. 2, a001107
39. Tan, B.S., Tiong, K.H., Choo, H.L., Fei-Lei Chung, F., Hii, L.W., Tan, S.H., Yap, I.K., Pani, S., Khor, N.T., Wong, S.F. et al. (2015) Mutant p53-R273H mediates cancer cell survival and anoikis resistance through AKT-dependent suppression of BCL2-modifying factor (BMF). Cell Death Dis. 6, e1826
40. Scian, M.J., Stagliano, K.E., Anderson, M.A., Hassan, S., Bowman, M., Miles, M.F., Deb, S.P. and Deb, S. (2005) Tumor-derived p53 mutants induce NF-kappaB2 gene expression. Mol. Cell Biol. 25, 10097-1110
41. Wang, X., Chen, J.X., Liu, J.P., You, C., Liu, Y.H. and Mao, Q. (2014) Gain of function of mutant TP53 in glioblastoma: prognosis and response to temozolomide. Ann. Surg. Oncol. 21, 1337-44
42. Kolukula, V.K., Sahu, G., Wellstein, A., Rodriguez, O.C., Preet, A., Iacobazzi, V., D'Orazi, G., Albanese, C., Palmieri, F. and Avantaggiati, M.L. (2014) SLC25A1, or CIC, is a novel transcriptional target of mutant p53 and a negative tumor prognostic marker. Oncotarget 5, 1212-1225
43. Krishnan, S.R., Nair, B.C., Sareddy, G.R., Roy, S.S., Natarajan, M., Suzuki, T., Peng, Y., Raj, G. and Vadlamudi, R.K. (2015) Novel role of PELP1 in regulating chemotherapy response in mutant p53-expressing triple negative breast cancer cells. Breast Cancer Res Treat. 150, 487-499
44. Kalo, E., Kogan-Sakin, I., Solomon, H., Bar-Nathan, E., Shay, M., Shetzer, Y., Dekel, E., Goldfinger, N., Buganim, Y., Stambolsky, P. et al. (2012) Mutant p53R273H attenuates the expression of phase 2 detoxifying enzymes and promotes the survival of cells with high levels of reactive oxygen species. J. Cell Sci. 125 Pt 22, 5578-5586
45. Li, D., Yallowitz, A., Ozog, L. and Marchenko, N. (2014) A gain-of-function mutant p53-HSF1 feed forward circuit governs adaptation of cancer cells to proteotoxic stress. Cell Death Dis. 5, e1194
46. Donzelli, S., Fontemaggi, G., Fazi, F., Di Agostino, S., Padula, F., Biagioni, F., Muti, P., Strano, S. and Blandino, G. (2012) MicroRNA-128-2 targets the transcriptional repressor E2F5 enhancing mutant p53 gain of function. Cell Death Differ. 19, 1038-1048
47. Masciarelli, S., Fontemaggi, G., Di Agostino, S., Donzelli, S., Carcarino, E., Strano, S. and Blandino, G. (2014) Gain-of-function mutant p53 downregulates miR-223 contributing to chemoresistance of cultured tumor cells. Oncogene 33, 1601-1608
48. Khromova, N.V., Kopnin, P.B., Stepanova, E.V., Agapova, L.S. and Kopnin, B.P. (2009) p53 hot-spot mutants increase tumor vascularization via ROS-mediated activation of the HIF1/VEGF-A pathway. Cancer Lett. 276, 143-151
49. Joshi, H., Bhanot, G., Borresen-Dale, A.L. and Kristensen, V. (2012) Potential tumorigenic programs associated with TP53 mutation status reveal role of VEGF pathway. Br. J. Cancer 107, 1722-1728
50. Montero, E., Abreu, C. and Tonino, P. (2008) Relationship between VEGF and p53 expression and tumor cell proliferation in human gastrointestinal carcinomas. J. Cancer Res. Clin. Oncol. 134, 193-201
51. Fontemaggi, G., Dell'Orso, S., Trisciuoglio, D., Shay, T., Melucci, E., Fazi, F., Terrenato, I., Mottolese, M., Muti, P., Domany, E. et al. (2009) The execution of the transcriptional axis mutant p53, E2F1 and ID4 promotes tumor neo-angiogenesis. Nat. Struct. Mol. Biol. 16, 1086-1093
52. Gudkov, A.V., Gurova, K.V. and Komarova, E.A. (2011) Inflammation and p53: a tale of two stresses. Genes Cancer 2, 503-516
53. Weisz, L., Damalas, A., Liontos, M., Karakaidos, P., Fontemaggi, G., Maor-Aloni, R., Kalis, M., Levrero, M., Strano, S., Gorgoulis, V.G. et al. (2007) Mutant p53 enhances nuclear factor kappaB activation by tumor necrosis factor alpha in cancer cells. Cancer Res. 67, 2396-2401
54. Cooks, T., Pateras, I.S., Tarcic, O., Solomon, H., Schetter, A.J., Wilder, S., Lozano, G., Pikarsky, E., Forshew, T., Rosenfeld, N. et al. (2013) Mutant p53 prolongs NF-kappaB activation and promotes chronic inflammation and inflammation-associated colorectal cancer. Cancer Cell 23, 634-646
55. Di Minin, G., Bellazzo, A., Dal Ferro, M., Chiaruttini, G., Nuzzo, S., Bicciato, S., Piazza, S., Rami, D., Bulla, R., Sommaggio, R. et al. (2014) Mutant p53 reprograms TNF signaling in cancer cells through interaction with the tumor suppressor DAB2IP. Mol. Cell 56, 617-629
56. Ubertini, V., Norelli, G., D'Arcangelo, D., Gurtner, A., Cesareo, E., Baldari, S., Gentileschi, M.P., Piaggio, G., Nistico, P., Soddu, S. et al. (2015) Mutant p53 gains new function in promoting inflammatory signals by repression of the secreted interleukin-1 receptor antagonist. Oncogene 34, 2493-2504
57. Schreiber, R.D., Old, L.J. and Smyth, M.J. (2011) Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331, 1565-1570
58. Samassekou, O., Bastien, N., Lichtensztejn, D., Yan, J., Mai, S. and Drouin, R. (2014) Different TP53 mutations are associated with specific chromosomal rearrangements, telomere length changes, and remodeling of the nuclear architecture of telomeres. Genes Chromosomes Cancer 53, 934-950
59. Hanel, W. and Moll, U.M. (2012) Links between mutant p53 and genomic instability. J. Cell Biochem. 113, 433-439
60. Valenti, F., Ganci, F., Fontemaggi, G., Sacconi, A., Strano, S., Blandino, G. and Di Agostino, S. (2015) Gain of function mutant p53 proteins cooperate with E2F4 to transcriptionally downregulate RAD17 and BRCA1 gene expression. Oncotarget 6, 5547-5566
61. Hingorani, S.R., Wang, L., Multani, A.S., Combs, C., Deramaudt, T.B., Hruban, R.H., Rustgi, A.K., Chang, S. and Tuveson, D.A. (2005) Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 7, 469-483
62. Scian, M.J., Stagliano, K.E., Deb, D., Ellis, M.A., Carchman, E.H., Das, A., Valerie, K., Deb, S.P. and Deb, S. (2004) Tumor-derived p53 mutants induce oncogenesis by transactivating growth-promoting genes. Oncogene 23, 4430-4443
63. Zhou, G., Wang, J., Zhao, M., Xie, T.X., Tanaka, N., Sano, D., Patel, A.A., Ward, A.M., Sandulache, V.C., Jasser, S.A. et al. (2014) Gain-of-function mutant p53 promotes cell growth and cancer cell metabolism via inhibition of AMPK activation. Mol. Cell 54, 960-974
64. Zhang, C., Liu, J., Liang, Y., Wu, R., Zhao, Y., Hong, X., Lin, M., Yu, H., Liu, L., Levine, A.J. et al. (2013) Tumour-associated mutant p53 drives the Warburg effect. Nat. Commun. 4, 2935
65. Li, X., Wu, J.B., Chung, L.W. and Huang, W.C. (2015) Anti-cancer efficacy of SREBP inhibitor, alone or in combination with docetaxel, in prostate cancer harboring p53 mutations. Oncotarget 6, 41018-41032
66. Zhu, J., Sammons, M.A., Donahue, G., Dou, Z., Vedadi, M., Getlik, M., Barsyte-Lovejoy, D., Al-awar, R., Katona, B.W., Shilatifard, A. et al. (2015) Gain-of-function p53 mutants co-opt chromatin pathways to drive cancer growth. Nature 525, 206-211
67. Polotskaia, A., Xiao, G., Reynoso, K., Martin, C., Qiu, W.G., Hendrickson, R.C. and Bargonetti, J. (2015) Proteome-wide analysis of mutant p53 targets in breast cancer identifies new levels of gain-of-function that influence PARP, PCNA, and MCM4. Proc. Natl. Acad. Sci. U.S.A. 112, E1220-E1229
68. Pfister, N.T., Fomin, V., Regunath, K., Zhou, J.Y., Zhou, W., Silwal-Pandit, L., Freed-Pastor, W.A., Laptenko, O., Neo, S.P., Bargonetti, J. et al. (2015) Mutant p53 cooperates with the SWI/SNF chromatin remodeling complex to regulate VEGFR2 in breast cancer cells. Genes Dev. 29, 1298-1315
69. Muller, P.A. and Vousden, K.H. (2014) Mutant p53 in cancer: new functions and therapeutic opportunities. Cancer Cell 25, 304-317
70. Blanden, A.R., Yu, X., Loh, S.N., Levine, A.J. and Carpizo, D.R. (2015) Reactivating mutant p53 using small molecules as zinc metallochaperones: awakening a sleeping giant in cancer. Drug Discov. Today 20, 1391-1397
71. Lehmann, S., Bykov, V.J., Ali, D., Andren, O., Cherif, H., Tidefelt, U., Uggla, B., Yachnin, J., Juliusson, G., Moshfegh, A. et al. (2012) Targeting p53 in vivo: a first-in-human study with p53-targeting compound APR-246 in refractory hematologic malignancies and prostate cancer. J. Clin. Oncol. 30, 3633-3639
72. He, X., Liao, J., Liu, F., Yan, J., Yan, J., Shang, H., Dou, Q., Chang, Y., Lin, J. and Song, Y. (2015) Functional repair of p53 mutation in colorectal cancer cells using trans-splicing. Oncotarget 6, 2034-2045
73. He, X., Liu, F., Yan, J., Zhang, Y., Yan, J., Shang, H., Dou, Q., Zhao, Q. and Song, Y. (2015) Trans-splicing repair of mutant p53 suppresses the growth of hepatocellular carcinoma cells in vitro and in vivo. Sci. Rep. 5, 8705
74. Wang, Y., Suh, Y.A., Fuller, M.Y., Jackson, J.G., Xiong, S., Terzian, T., Quintas-Cardama, A., Bankson, J.A., El-Naggar, A.K. and Lozano, G. (2011) Restoring expression of wild-type p53 suppresses tumor growth but does not cause tumor regression in mice with a p53 missense mutation. J Clin Invest. 121, 893-904
75. Freed-Pastor, W.A. and Prives, C. (2012) Mutant p53: one name, many proteins. Genes Dev. 26, 1268-1286