A Pin1/Mutant p53 Axis Promotes Aggressiveness in Breast Cancer

Cancer Cell

Volumn 20, Issue 1, 2011, Pages 79-91

  Girardini, Javier E ^a,b   Napoli, Marco ^a,b   Piazza, Silvano ^a   Rustighi, Alessandra ^a,b   Marotta, Carolina ^a,b   Radaelli, Enrico ^c,d   Capaci, Valeria ^a,b   Jordan, Lee ^e   Quinlan, Phil ^e   Thompson, Alastair ^e,f   Mano, Miguel ^g   Rosato, Antonio ^h   Crook, Tim ^e   Scanziani, Eugenio ^c,d   Means, Anthony R ⁱ   Lozano, Guillermina ^f   Schneider, Claudio ^a,j   Del Sal, Giannino ^a,b  

^a Laboratorio Nazionale CIB LNCIB   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d Mouse and Animal Pathology Lab   (Italy)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^g INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^h UNIVERSITY OF PADOVA   (Italy)

ⁱ DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^j UNIVERSITY OF UDINE   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; PEPTIDYLPROLYL ISOMERASE PIN1; PROTEIN P53; PROTEIN P63; RAS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER AGGRESSIVENESS; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER MODEL; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; GENE EXPRESSION; GENE INTERACTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; MISSENSE MUTATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGNOSIS; TRANSCRIPTION REGULATION;

EID: 79960039752     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2011.06.004     Document Type: Article

References (45)

1. Adorno M., Cordenonsi M., Montagner M., Dupont S., Wong C., Hann B., Solari A., Bobisse S., Rondina M.B., Guzzardo V., et al. A Mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis. Cell 2009, 137:87-98.
2. Anania M.C., Sensi M., Radaelli E., Miranda C., Vizioli M.G., Pagliardini S., Favini E., Cleris L., Supino R., Formelli F., et al. TIMP3 regulates migration, invasion and in vivo tumorigenicity of thyroid tumor cells. Oncogene 2011, in press. Published online February 21, 2011. 10.1038/onc.2011.18.
3. Atchison F.W., Capel B., Means A.R. Pin1 regulates the timing of mammalian primordial germ cell proliferation. Development 2003, 130:3579-3586.
4. Bao L., Kimzey A., Sauter G., Sowadski J.M., Lu K.P., Wang D.G. Prevalent overexpression of prolyl isomerase Pin1 in human cancers. Am. J. Pathol. 2004, 164:1727-1737.
5. Bouras T., Lisanti M.P., Pestell R.G. Caveolin-1 in breast cancer. Cancer Biol. Ther. 2004, 3:931-941.
6. Brosh R., Rotter V. When mutants gain new powers: news from the mutant p53 field. Nat. Rev. Cancer 2009, 9:701-713.
7. Caulin C., Nguyen T., Lang G.A., Goepfert T.M., Brinkley B.R., Cai W.W., Lozano G., Roop D.R. An inducible mouse model for skin cancer reveals distinct roles for gain- and loss-of-function p53 mutations. J. Clin. Invest. 2007, 117:1893-1901.
8. Desmedt C., Piette F., Loi S., Wang Y., Lallemand F., Haibe-Kains B., Viale G., Delorenzi M., Zhang Y., d'Assignies M.S., et al. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin. Cancer Res. 2007, 13:3207-3214. TRANSBIG Consortium.
9. Di Agostino S., Strano S., Emiliozzi V., Zerbini V., Mottolese M., Sacchi A., Blandino G., Piaggio G. Gain of function of mutant p53: the mutant p53/NF-Y protein complex reveals an aberrant transcriptional mechanism of cell cycle regulation. Cancer Cell 2006, 10:191-202.
10. Guida E., Bisso A., Fenollar-Ferrer C., Napoli M., Anselmi C., Girardini J.E., Carloni P., Del Sal G. Peptide aptamers targeting mutant p53 induce apoptosis in tumor cells. Cancer Res. 2008, 68:6550-6558.
11. Hidalgo-Curtis C., Chase A., Drachenberg M., Roberts M.W., Finkelstein J.Z., Mould S., Oscier D., Cross N.C., Grand F.H. The t(1;9)(p34;q34) and t(8;12)(p11;q15) fuse pre-mRNA processing proteins SFPQ (PSF) and CPSF6 to ABL and FGFR1. Genes Chromosomes Cancer 2008, 47:379-385.
12. Hingorani S.R., Wang L., Multani A.S., Combs C., Deramaudt T.B., Hruban R.H., Rustgi A.K., Chang S., Tuveson D.A. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005, 7:469-483.
13. Kanehira M., Harada Y., Takata R., Shuin T., Miki T., Fujioka T., Nakamura Y., Katagiri T. Involvement of upregulation of DEPDC1 (DEP domain containing 1) in bladder carcinogenesis. Oncogene 2007, 26:6448-6455.
14. 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. Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 2004, 119:861-872.
15. Langerød A., Zhao H., Borgan O., Nesland J.M., Bukholm I.R.K., Ikdahl T., Kåresen R., Børresen-Dale A.L., Jeffrey S.S. TP53 mutation status and gene expression profiles are powerful prognostic markers of breast cancer. Breast Cancer Res. 2007, 9:R30.
16. Larriba M.J., Casado-Vela J., Pendás-Franco N., Peña R., García de Herreros A., Berciano M.T., Lafarga M., Casal J.I., Muñoz A. Novel snail1 target proteins in human colon cancer identified by proteomic analysis. PLoS ONE 2010, 5:e10221.
17. Lu K.P., Zhou X.Z. The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat. Rev. Mol. Cell Biol. 2007, 8:904-916.
18. Luo J., Emanuele M.J., Li D., Creighton C.J., Schlabach M.R., Westbrook T.F., Wong K.K., Elledge S.J. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 2009, 137:835-848.
19. Malkin D., Li F.P., Strong L.C., Fraumeni J.F., Nelson C.E., Kim D.H., Kassel J., Gryka M.A., Bischoff F.Z., Tainsky M.A., et al. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science 1990, 250:1233-1238.
20. Mantovani F., Piazza S., Gostissa M., Strano S., Zacchi P., Mantovani R., Blandino G., Del Sal G. Pin1 links the activities of c-Abl and p300 in regulating p73 function. Mol. Cell 2004, 14:625-636.
21. Mantovani F., Tocco F., Girardini J.E., Smith P., Gasco M., Lu X., Crook T., Del Sal G. The prolyl isomerase Pin1 orchestrates p53 acetylation and dissociation from the apoptosis inhibitor iASPP. Nat. Struct. Mol. Biol. 2007, 14:912-920.
22. Miller L.D., Smeds J., George J., Vega V.B., Vergara L., Ploner A., Pawitan Y., Hall P., Klaar S., Liu E.T., Bergh J. An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc. Natl. Acad. Sci. USA 2005, 102:13550-13555.
23. 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. Mutant p53 drives invasion by promoting integrin recycling. Cell 2009, 139:1327-1341.
24. Olive K.P., Tuveson D.A., Ruhe Z.C., Yin B., Willis N.A., Bronson R.T., Crowley D., Jacks T. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004, 119:847-860.
25. Olivier M., Langerød A., Carrieri P., Bergh J., Klaar S., Eyfjord J., Theillet C., Rodriguez C., Lidereau R., Bièche I., et al. The clinical value of somatic TP53 gene mutations in 1,794 patients with breast cancer. Clin. Cancer Res. 2006, 12:1157-1167.
26. Oren M., Rotter V. Mutant p53 gain-of-function in cancer. Cold Spring Harb. Perspect. Biol. 2010, 2:a001107.
27. Pawitan Y., Bjöhle J., Amler L., Borg A.L., Egyhazi S., Hall P., Han X., Holmberg L., Huang F., Klaar S., et al. Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Res. 2005, 7:R953-R964.
28. Rustighi A., Tiberi L., Soldano A., Napoli M., Nuciforo P., Rosato A., Kaplan F., Capobianco A., Pece S., Di Fiore P.P., Del Sal G. The prolyl-isomerase Pin1 is a Notch1 target that enhances Notch1 activation in cancer. Nat. Cell Biol. 2009, 11:133-142.
29. Ryo A., Liou Y.C., Wulf G., Nakamura M., Lee S.W., Lu K.P. PIN1 is an E2F target gene essential for Neu/Ras-induced transformation of mammary epithelial cells. Mol. Cell. Biol. 2002, 22:5281-5295.
30. Selivanova G., Wiman K.G. Reactivation of mutant p53: molecular mechanisms and therapeutic potential. Oncogene 2007, 26:2243-2254.
31. Song H., Hollstein M., Xu Y. p53 gain-of-function cancer mutants induce genetic instability by inactivating ATM. Nat. Cell Biol. 2007, 9:573-580.
32. Song B., Wang C., Liu J., Wang X., Lv L., Wei L., Xie L., Zheng Y., Song X. MicroRNA-21 regulates breast cancer invasion partly by targeting tissue inhibitor of metalloproteinase 3 expression. J. Exp. Clin. Cancer Res. 2010, 29:29.
33. Sotiriou C., Wirapati P., Loi S., Harris A., Fox S., Smeds J., Nordgren H., Farmer P., Praz V., Haibe-Kains B., et al. Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J. Natl. Cancer Inst. 2006, 98:262-272.
34. Soussi T., Béroud C. Assessing TP53 status in human tumours to evaluate clinical outcome. Nat. Rev. Cancer 2001, 1:233-240.
35. Soussi T., Wiman K.G. Shaping genetic alterations in human cancer: the p53 mutation paradigm. Cancer Cell 2007, 12:303-312.
36. Sparano J.A., Goldstein L.J., Childs B.H., Shak S., Badve S., Baehner F.L., Davidson N.E., Sledge G.W., Gray R. Genotypic characterization of phenotypically defined triple-negative breast cancer. J. Clin. Oncol. 2009, 27:500.
37. Su X., Chakravarti D., Cho M.S., Liu L., Gi Y.J., Lin Y.L., Leung M.L., El-Naggar A.K., Creighton C.J., Suraokar M.B., et al. TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 2010, 467:986-990.
38. Terzian T., Suh Y.A., Iwakuma T., Post S.M., Neumann M., Lang G.A., Van Pelt C.S., Lozano G. The inherent instability of mutant p53 is alleviated by Mdm2 or p16INK4a loss. Genes Dev. 2008, 22:1337-1344.
39. UKCCCR guidelines for the welfare of animals in experimental neoplasia. Cancer Metastasis Rev. 1989, 8:82-88. UKCCCR.
40. van't Veer L.J., Dai H., van de Vijver M.J., He Y.D., Hart A.A., Mao M., Peterse H.L., van der Kooy K., Marton M.J., Witteveen A.T., et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536.
41. Wolf I., O'Kelly J., Rubinek T., Tong M., Nguyen A., Lin B.T., Tai H.H., Karlan B.Y., Koeffler H.P. 15-hydroxyprostaglandin dehydrogenase is a tumor suppressor of human breast cancer. Cancer Res. 2006, 66:7818-7823.
42. Wulf G., Garg P., Liou Y.C., Iglehart D., Lu K.P. Modeling breast cancer in vivo and ex vivo reveals an essential role of Pin1 in tumorigenesis. EMBO J. 2004, 23:3397-3407.
43. Yeh E.S., Means A.R. PIN1, the cell cycle and cancer. Nat. Rev. Cancer 2007, 7:381-388.
44. Zacchi P., Gostissa M., Uchida T., Salvagno C., Avolio F., Volinia S., Ronai Z., Blandino G., Schneider C., Del Sal G. The prolyl isomerase Pin1 reveals a mechanism to control p53 functions after genotoxic insults. Nature 2002, 419:853-857.
45. Zheng H., You H., Zhou X.Z., Murray S.A., Uchida T., Wulf G., Gu L., Tang X., Lu K.P., Xiao Z.X. The prolyl isomerase Pin1 is a regulator of p53 in genotoxic response. Nature 2002, 419:849-853.