Mutant p53 exerts oncogenic effects through microRNAs and their target gene networks

FEBS Letters

Volumn 588, Issue 16, 2014, Pages 2610-2615

  Li, Xiao Ling ^a   Jones, Matthew F ^a   Subramanian, Murugan ^a   Lal, Ashish ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cancer; Gain of function; Invasion; Let 7; Metastasis; microRNA; miR 128 2; miR 130b; miR 155; miR 205; miR 223; miR 27a; miRNA; Mutant p53

Indexed keywords

MICRORNA; MICRORNA 128 2; MICRORNA 130B; MICRORNA 155; MICRORNA 205; MICRORNA 223; MICRORNA 27A; MICRORNA LET 7I; PROTEIN P53; UNCLASSIFIED DRUG;

BIOGENESIS; CANCER INHIBITION; DOWN REGULATION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; GENETIC ASSOCIATION; HUMAN; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION;

CANCER; GAIN-OF-FUNCTION; INVASION; LET-7; METASTASIS; MICRORNA; MIR-128-2; MIR-130B; MIR-155; MIR-205; MIR-223; MIR-27A; MIRNA; MUTANT P53;

ANIMALS; GENE REGULATORY NETWORKS; HUMANS; MICRORNAS; MUTATION; NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84905098153     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.03.054     Document Type: Review

References (85)

1. B.P. Lewis, C.B. Burge, and D.P. Bartel Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets Cell 120 2005 15 20
2. R.C. Friedman, K.K. Farh, C.B. Burge, and D.P. Bartel Most mammalian mRNAs are conserved targets of microRNAs Genome Res. 19 2009 92 105
3. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
4. V.N. Kim MicroRNA biogenesis: coordinated cropping and dicing Nat. Rev. Mol. Cell Biol. 6 2005 376 385
5. Y. Lee, M. Kim, J. Han, K.H. Yeom, S. Lee, S.H. Baek, and V.N. Kim MicroRNA genes are transcribed by RNA polymerase II EMBO J. 23 2004 4051 4060
6. R.I. Gregory, and R. Shiekhattar MicroRNA biogenesis and cancer Cancer Res. 65 2005 3509 3512
7. G.A. Calin, and C.M. Croce MicroRNA signatures in human cancers Nat. Rev. Cancer 6 2006 857 866
8. A.L. Kasinski, and F.J. Slack Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy Nat. Rev. Cancer 11 2011 849 864
9. P.P. Medina, and F.J. Slack MicroRNAs and cancer: an overview Cell Cycle 7 2008 2485 2492
10. S. Roush, and F.J. Slack The let-7 family of microRNAs Trends Cell Biol. 18 2008 505 516
11. S.M. Johnson, H. Grosshans, J. Shingara, M. Byrom, R. Jarvis, A. Cheng, E. Labourier, K.L. Reinert, D. Brown, and F.J. Slack RAS is regulated by the let-7 microRNA family Cell 120 2005 635 647
12. C.D. Johnson, A. Esquela-Kerscher, G. Stefani, M. Byrom, K. Kelnar, D. Ovcharenko, M. Wilson, X. Wang, J. Shelton, J. Shingara, L. Chin, D. Brown, and F.J. Slack The let-7 microRNA represses cell proliferation pathways in human cells Cancer Res. 67 2007 7713 7722
13. T.C. Chang, L.R. Zeitels, H.W. Hwang, R.R. Chivukula, E.A. Wentzel, M. Dews, J. Jung, P. Gao, C.V. Dang, M.A. Beer, A. Thomas-Tikhonenko, and J.T. Mendell Lin-28B transactivation is necessary for Myc-mediated let-7 repression and proliferation Proc. Natl. Acad. Sci. USA 106 2009 3384 3389
14. T.C. Chang, D. Yu, Y.S. Lee, E.A. Wentzel, D.E. Arking, K.M. West, C.V. Dang, A. Thomas-Tikhonenko, and J.T. Mendell Widespread microRNA repression by Myc contributes to tumorigenesis Nat. Genetics 40 2008 43 50
15. T.V. Bui, and J.T. Mendell Myc: Maestro of MicroRNAs Genes Cancer 1 2010 568 575
16. G.A. Calin, C.D. Dumitru, M. Shimizu, R. Bichi, S. Zupo, E. Noch, H. Aldler, S. Rattan, M. Keating, K. Rai, L. Rassenti, T. Kipps, M. Negrini, F. Bullrich, and C.M. Croce Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia Proc. Natl. Acad. Sci. USA 99 2002 15524 15529
17. A. Cimmino, G.A. Calin, M. Fabbri, M.V. Iorio, M. Ferracin, M. Shimizu, S.E. Wojcik, R.I. Aqeilan, S. Zupo, M. Dono, L. Rassenti, H. Alder, S. Volinia, C.G. Liu, T.J. Kipps, M. Negrini, and C.M. Croce MiR-15 and miR-16 induce apoptosis by targeting BCL2 Proc. Natl. Acad. Sci. USA 102 2005 13944 13949
18. T.C. Chang, E.A. Wentzel, O.A. Kent, K. Ramachandran, M. Mullendore, K.H. Lee, G. Feldmann, M. Yamakuchi, M. Ferlito, C.J. Lowenstein, D.E. Arking, M.A. Beer, A. Maitra, and J.T. Mendell Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis Mol. Cell 26 2007 745 752
19. N. Raver-Shapira, E. Marciano, E. Meiri, Y. Spector, N. Rosenfeld, N. Moskovits, Z. Bentwich, and M. Oren Transcriptional activation of miR-34a contributes to p53-mediated apoptosis Mol. Cell 26 2007 731 743
20. H. Hermeking MiR-34a and p53 Cell Cycle 8 2009 1308
21. L. He, X. He, L.P. Lim, E. de Stanchina, Z. Xuan, Y. Liang, W. Xue, L. Zender, J. Magnus, D. Ridzon, A.L. Jackson, P.S. Linsley, C. Chen, S.W. Lowe, M.A. Cleary, and G.J. Hannon A microRNA component of the p53 tumour suppressor network Nature 447 2007 1130 1134
22. H. Hermeking P53 enters the microRNA world Cancer Cell 12 2007 414 418
23. V. Tarasov, P. Jung, B. Verdoodt, D. Lodygin, A. Epanchintsev, A. Menssen, G. Meister, and H. Hermeking Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest Cell Cycle 6 2007 1586 1593
24. A. Lal, M.P. Thomas, G. Altschuler, F. Navarro, E. O'Day, X.L. Li, C. Concepcion, Y.C. Han, J. Thiery, D.K. Rajani, A. Deutsch, O. Hofmann, A. Ventura, W. Hide, and J. Lieberman Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling PLoS Genet. 7 2011 e1002363
25. P.P. Medina, M. Nolde, and F.J. Slack OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma Nature 467 2010 86 90
26. A. Esquela-Kerscher, and F.J. Slack Oncomirs - microRNAs with a role in cancer Nat. Rev. Cancer 6 2006 259 269
27. K.A. O'Donnell, E.A. Wentzel, K.I. Zeller, C.V. Dang, and J.T. Mendell C-Myc-regulated microRNAs modulate E2F1 expression Nature 435 2005 839 843
28. Y. Hayashita, H. Osada, Y. Tatematsu, H. Yamada, K. Yanagisawa, S. Tomida, Y. Yatabe, K. Kawahara, Y. Sekido, and T. Takahashi A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation Cancer Res. 65 2005 9628 9632
29. L. He, J.M. Thomson, M.T. Hemann, E. Hernando-Monge, D. Mu, S. Goodson, S. Powers, C. Cordon-Cardo, S.W. Lowe, G.J. Hannon, and S.M. Hammond A microRNA polycistron as a potential human oncogene Nature 435 2005 828 833
30. G. Lanza, M. Ferracin, R. Gafa, A. Veronese, R. Spizzo, F. Pichiorri, C.G. Liu, G.A. Calin, C.M. Croce, and M. Negrini MRNA/microRNA gene expression profile in microsatellite unstable colorectal cancer Mol. Cancer 6 2007 54
31. K.H. Vousden, and X. Lu Live or let die: the cell's response to p53 Nat. Rev. Cancer 2 2002 594 604
32. W.S. el-Deiry, S.E. Kern, J.A. Pietenpol, K.W. Kinzler, and B. Vogelstein Definition of a consensus binding site for p53 Nat. Genetics 1 1992 45 49
33. C. Prives, and P.A. Hall The p53 pathway J. Pathol. 187 1999 112 126
34. R. Beckerman, and C. Prives Transcriptional regulation by p53 Cold Spring Harb. Perspect. Biol. 2 2010 a000935
35. K.H. Vousden, and C. Prives Blinded by the light: the growing complexity of p53 Cell 137 2009 413 431
36. E. Gottlieb, and K.H. Vousden P53 regulation of metabolic pathways Cold Spring Harb. Perspect. Biol. 2 2010 a001040
37. B. Vogelstein, D. Lane, and A.J. Levine Surfing the p53 network Nature 408 2000 307 310
38. A. Petitjean, E. Mathe, S. Kato, C. Ishioka, S.V. Tavtigian, P. Hainaut, and M. Olivier Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database Hum. Mutat. 28 2007 622 629
39. P.A. Muller, and K.H. Vousden P53 mutations in cancer Nat. Cell Biol. 15 2013 2 8
40. P.A. Muller, K.H. Vousden, and J.C. Norman P53 and its mutants in tumor cell migration and invasion J. Cell Biol. 192 2011 209 218
41. P.A. Muller, A.G. Trinidad, P. Timpson, J.P. Morton, S. Zanivan, P.V. van den Berghe, C. Nixon, S.A. Karim, P.T. Caswell, J.E. Noll, C.R. Coffill, D.P. Lane, O.J. Sansom, P.M. Neilsen, J.C. Norman, and K.H. Vousden Mutant p53 enhances MET trafficking and signalling to drive cell scattering and invasion Oncogene 32 2013 1252 1265
42. P.A. Muller, P.T. Caswell, B. Doyle, M.P. Iwanicki, E.H. Tan, S. Karim, N. Lukashchuk, D.A. Gillespie, R.L. Ludwig, P. Gosselin, A. Cromer, J.S. Brugge, O.J. Sansom, J.C. Norman, and K.H. Vousden Mutant p53 drives invasion by promoting integrin recycling Cell 139 2009 1327 1341
43. M. Oren, and V. Rotter Mutant p53 gain-of-function in cancer Cold Spring Harbor Perspect. Biol. 2 2010 a001107
44. T. Cooks, I.S. Pateras, O. Tarcic, H. Solomon, A.J. Schetter, S. Wilder, G. Lozano, E. Pikarsky, T. Forshew, N. Rosenfeld, N. Harpaz, S. Itzkowitz, C.C. Harris, V. Rotter, V.G. Gorgoulis, and M. Oren Mutant p53 prolongs NF-kappaB activation and promotes chronic inflammation and inflammation-associated colorectal cancer Cancer Cell 23 2013 634 646
45. P.A. Muller, A.G. Trinidad, P.T. Caswell, J.C. Norman, and K.H. Vousden Mutant p53 Regulates Dicer through p63-dependent and -independent Mechanisms to Promote an Invasive Phenotype J. Biol. Chem. 289 2014 122 132
46. C. Cadwell, and G.P. Zambetti The effects of wild-type p53 tumor suppressor activity and mutant p53 gain-of-function on cell growth Gene 277 2001 15 30
47. A.B. DeLeo, G. Jay, E. Appella, G.C. Dubois, L.W. Law, and L.J. Old Detection of a transformation-related antigen in chemically induced sarcomas and other transformed cells of the mouse Proc. Natl. Acad. Sci. USA 76 1979 2420 2424
48. M. Kress, E. May, R. Cassingena, and P. May Simian virus 40-transformed cells express new species of proteins precipitable by anti-simian virus 40 tumor serum J. Virol. 31 1979 472 483
49. D.P. Lane, and L.V. Crawford T antigen is bound to a host protein in SV40-transformed cells Nature 278 1979 261 263
50. D. Eliyahu, D. Michalovitz, and M. Oren Overproduction of p53 antigen makes established cells highly tumorigenic Nature 316 1985 158 160
51. D. Eliyahu, A. Raz, P. Gruss, D. Givol, and M. Oren Participation of p53 cellular tumour antigen in transformation of normal embryonic cells Nature 312 1984 646 649
52. J.R. Jenkins, K. Rudge, and G.A. Currie Cellular immortalization by a cDNA clone encoding the transformation-associated phosphoprotein p53 Nature 312 1984 651 654
53. P. Hinds, C. Finlay, and A.J. Levine Mutation is required to activate the p53 gene for cooperation with the ras oncogene and transformation J. Virol. 63 1989 739 746
54. A.J. Levine, and M. Oren The first 30 years of p53: growing ever more complex Nat. Rev. Cancer 9 2009 749 758
55. G.A. Lang, T. Iwakuma, Y.A. Suh, G. Liu, V.A. Rao, J.M. Parant, Y.A. Valentin-Vega, T. Terzian, L.C. Caldwell, L.C. Strong, A.K. El-Naggar, and G. Lozano Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome Cell 119 2004 861 872
56. K.P. Olive, D.A. Tuveson, Z.C. Ruhe, B. Yin, N.A. Willis, R.T. Bronson, D. Crowley, and T. Jacks Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome Cell 119 2004 847 860
57. L.A. Donehower, and G. Lozano 20 years studying p53 functions in genetically engineered mice Nat. Rev. Cancer 9 2009 831 841
58. G. Blandino, A.J. Levine, and M. Oren Mutant p53 gain of function: differential effects of different p53 mutants on resistance of cultured cells to chemotherapy Oncogene 18 1999 477 485
59. A. Lanyi, D. Deb, R.C. Seymour, J.H. Ludes-Meyers, M.A. Subler, and S. Deb 'Gain of function' phenotype of tumor-derived mutant p53 requires the oligomerization/nonsequence-specific nucleic acid-binding domain Oncogene 16 1998 3169 3176
60. D. Dittmer, S. Pati, G. Zambetti, S. Chu, A.K. Teresky, M. Moore, C. Finlay, and A.J. Levine Gain of function mutations in p53 Nat. Genet. 4 1993 42 46
61. S.P. Deb, R.M. Munoz, D.R. Brown, M.A. Subler, and S. Deb Wild-type human p53 activates the human epidermal growth factor receptor promoter Oncogene 9 1994 1341 1349
62. S. Deb, C.T. Jackson, M.A. Subler, and D.W. Martin Modulation of cellular and viral promoters by mutant human p53 proteins found in tumor cells J. Virol. 66 1992 6164 6170
63. K.V. Chin, K. Ueda, I. Pastan, and M.M. Gottesman Modulation of activity of the promoter of the human MDR1 gene by Ras and p53 Science 255 1992 459 462
64. W.A. Freed-Pastor, and C. Prives Mutant p53: one name, many proteins Genes Dev. 26 2012 1268 1286
65. M. Lokshin, Y. Li, C. Gaiddon, and C. Prives P53 and p73 display common and distinct requirements for sequence specific binding to DNA Nucleic Acids Res. 35 2007 340 352
66. Y. Li, and C. Prives Are interactions with p63 and p73 involved in mutant p53 gain of oncogenic function? Oncogene 26 2007 2220 2225
67. C. Gaiddon, M. Lokshin, J. Ahn, T. Zhang, and C. Prives 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 2001 1874 1887
68. C.J. Di Como, C. Gaiddon, and C. Prives P73 function is inhibited by tumor-derived p53 mutants in mammalian cells Mol. Cell. Biol. 19 1999 1438 1449
69. S. Di Agostino, S. Strano, V. Emiliozzi, V. Zerbini, M. Mottolese, A. Sacchi, G. Blandino, and G. Piaggio 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 2006 191 202
70. G. Fontemaggi, S. Dell'Orso, D. Trisciuoglio, T. Shay, E. Melucci, F. Fazi, I. Terrenato, M. Mottolese, P. Muti, E. Domany, D. Del Bufalo, S. Strano, and G. Blandino The execution of the transcriptional axis mutant p53, E2F1 and ID4 promotes tumor neo-angiogenesis Nat. Struct. Mol. Biol. 16 2009 1086 1093
71. P. Stambolsky, Y. Tabach, G. Fontemaggi, L. Weisz, R. Maor-Aloni, Z. Siegfried, I. Shiff, I. Kogan, M. Shay, E. Kalo, G. Blandino, I. Simon, M. Oren, and V. Rotter Modulation of the vitamin D3 response by cancer-associated mutant p53 Cancer Cell 17 2010 273 285
72. E. Kim, and W. Deppert Transcriptional activities of mutant p53: when mutations are more than a loss J. Cell. Biochem. 93 2004 878 886
73. S. Strano, S. Dell'Orso, S. Di Agostino, G. Fontemaggi, A. Sacchi, and G. Blandino Mutant p53: an oncogenic transcription factor Oncogene 26 2007 2212 2219
74. S. Donzelli, G. Fontemaggi, F. Fazi, S. Di Agostino, F. Padula, F. Biagioni, P. Muti, S. Strano, and G. Blandino MicroRNA-128-2 targets the transcriptional repressor E2F5 enhancing mutant p53 gain of function Cell Death Differ. 19 2012 1038 1048
75. P.M. Neilsen, J.E. Noll, S. Mattiske, C.P. Bracken, P.A. Gregory, R.B. Schulz, S.P. Lim, R. Kumar, R.J. Suetani, G.J. Goodall, and D.F. Callen Mutant p53 drives invasion in breast tumors through up-regulation of miR-155 Oncogene 32 2013 2992 3000
76. S. Masciarelli, G. Fontemaggi, S. Di Agostino, S. Donzelli, E. Carcarino, S. Strano, and G. Blandino Gain-of-function mutant p53 downregulates miR-223 contributing to chemoresistance of cultured tumor cells Oncogene. 33 2014 1601 1608
77. P. Dong, M. Karaayvaz, N. Jia, M. Kaneuchi, J. Hamada, H. Watari, S. Sudo, J. Ju, and N. Sakuragi Mutant p53 gain-of-function induces epithelial-mesenchymal transition through modulation of the miR-130b-ZEB1 axis Oncogene 32 2013 3286 3295
78. W. Wang, B. Cheng, L. Miao, Y. Mei, and M. Wu Mutant p53-R273H gains new function in sustained activation of EGFR signaling via suppressing miR-27a expression Cell Death Dis. 4 2013 e574
79. M. Subramanian, P. Francis, S. Bilke, X.L. Li, T. Hara, X. Lu, M.F. Jones, R.L. Walker, Y. Zhu, M. Pineda, C. Lee, L. Varanasi, Y. Yang, L.A. Martinez, J. Luo, S. Ambs, S. Sharma, L.M. Wakefield, P.S. Meltzer, and A. Lal A mutant p53/let-7i-axis-regulated gene network drives cell migration, invasion and metastasis Oncogene. 2014 10.1038/onc.2014.46
80. P. Tucci, M. Agostini, F. Grespi, E.K. Markert, A. Terrinoni, K.H. Vousden, P.A. Muller, V. Dotsch, S. Kehrloesser, B.S. Sayan, G. Giaccone, S.W. Lowe, N. Takahashi, P. Vandenabeele, R.A. Knight, A.J. Levine, and G. Melino Loss of p63 and its microRNA-205 target results in enhanced cell migration and metastasis in prostate cancer Proc. Natl. Acad. Sci. USA 109 2012 15312 15317
81. H.I. Suzuki, K. Yamagata, K. Sugimoto, T. Iwamoto, S. Kato, and K. Miyazono Modulation of microRNA processing by p53 Nature 460 2009 529 533
82. M. Huarte, M. Guttman, D. Feldser, M. Garber, M.J. Koziol, D. Kenzelmann-Broz, A.M. Khalil, O. Zuk, I. Amit, M. Rabani, L.D. Attardi, A. Regev, E.S. Lander, T. Jacks, and J.L. Rinn A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response Cell 142 2010 409 419
83. J.L. Rinn, and H.Y. Chang Genome regulation by long noncoding RNAs Annu. Rev. Biochem. 81 2012 145 166
84. M. Subramanian, M.F. Jones, and A. Lal Long Non-coding RNAs embedded in the Rb and p53 pathways Cancers 5 2013 1655 1675
85. V. Tripathi, Z. Shen, A. Chakraborty, S. Giri, S.M. Freier, X. Wu, Y. Zhang, M. Gorospe, S.G. Prasanth, A. Lal, and K.V. Prasanth Long non-coding RNA MALAT1 controls cell cycle progression by regulating the expression of oncogenic transcription factor B-MYB PLoS Genetics 9 2013 e1003368