Prolyl isomerase pin1 acts downstream of mir200c to promote cancer stem-like cell traits in breast cancer

Cancer Research

Volumn 74, Issue 13, 2014, Pages 3603-3616

  Luo, Man Li ^a   Gong, Chang ^d   Chen, Chun Hau ^a   Lee, Daniel Y ^a   Hu, Hai ^a   Huang, Pengyu ^a   Yao, Yandan ^a   Guo, Wenjun ^c   Reinhardt, Ferenc ^c   Wulf, Gerburg ^a   Lieberman, Judy ^b   Zhou, Xiao Zhen ^a   Song, Erwei ^d   Lu, Kun Ping ^a,e  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d SUN YAT SEN UNIVERSITY   (China)

^e FUJIAN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA 200C; PEPTIDYLPROLYL ISOMERASE PIN1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER STEM CELL; CARCINOGENICITY; CELL ISOLATION; CELL LINEAGE; CELL POPULATION; CELL RENEWAL; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE DELETION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL EXPANSION; TUMOR INVASION;

ANIMALS; BREAST NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PEPTIDYLPROLYL ISOMERASE; PHENANTHROLINES; RNA INTERFERENCE; TRANSDUCTION, GENETIC; TUMOR CELLS, CULTURED;

EID: 84904045311     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2785     Document Type: Article

References (50)

1. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010;140:62-73.
2. Stingl J, Caldas C. Molecular heterogeneity of breast carcinomas and the cancer stem cell hypothesis. Nat Rev Cancer 2007;7:791-9.
3. Liu S, Wicha MS. Targeting breast cancer stem cells. J Clin Oncol 2010;28:4006-12.
4. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 2009;138:592-603.
5. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, et al. let-7 regulates selfrenewal and tumorigenicity of breast cancer cells. Cell 2007;131: 1109-23.
6. Adam L, Zhong M, Choi W, Qi W, Nicoloso M, Arora A, et al. miR-200 expression regulates epithelial-to-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin Cancer Res 2009;15:5060-72.
7. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008;10:593-601.
8. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the Ecadherin repressors ZEB1 and ZEB2. Genes Dev 2008;22:894-907.
9. Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature 2001; 411:355-65.
10. Lu KP, Zhou XZ. The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat Rev Mol Cell Biol 2007; 8:904-16.
11. Bao L, Kimzey A, Sauter G, Sowadski JM, Lu KP, Wang DG. Prevalent overexpression of prolyl isomerase Pin1 in human cancers. Am J Pathol 2004;164:1727-37.
12. Wulf GM, Ryo A, Wulf GG, Lee SW, Niu T, Petkova V, et al. Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1. EMBO J 2001;20:3459-72.
13. Han CH, Lu J, Wei Q, Bondy ML, Brewster AM, Yu TK, et al. The functional promoter polymorphism (-842G>C) in the PIN1 gene is associated with decreased risk of breast cancer in non-Hispanic white women 55 years and younger. Breast Cancer Res Treat 2010;122: 243-9.
14. Xu HR, Xu ZF, Sun YL, Han JJ, Li ZJ. The -842G/C polymorphisms of PIN1 contributes to cancer risk: a meta-analysis of 10 case-control studies. PLoS ONE 2013;8:e71516.
15. Finn G, Luo ML, Zhou XZ, Lu KP. Pin1: a promising novel diagnostic and therapeutic target that acts on numerous cancer-driving pathways. In: Atta-ur-Rahman, editor. Sharjah, United Arab Emirates: Curr Cancer Drug Targets, 2013. Sharjah, United Arab Emirates. p. 146-71.
16. Ryo A, Liou YC, Wulf G, Nakamura M, Lee SW, Lu KP. PIN1 is an E2F target gene essential for Neu/Ras-induced transformation of mammary epithelial cells. Mol Cell Biol 2002;22:5281-95.
17. Suizu F, Ryo A, Wulf G, Lim J, Lu KP. Pin1 regulates centrosome duplication, and its overexpression induces centrosome amplification, chromosome instability, and oncogenesis. Mol Cell Biol 2006;26: 1463-79.
18. Lee TH, Tun-Kyi A, Shi R, Lim J, Soohoo C, Finn G, et al. Essential role of Pin1 in the regulation of TRF1 stability and telomere maintenance. Nat Cell Biol 2009;11:97-105.
19. Liou YC, Ryo A, Huang HK, Lu PJ, Bronson R, Fujimori F, et al. Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1- null phenotypes. Proc Natl Acad Sci U S A 2002;99:1335-40.
20. Wulf G, Garg P, Liou YC, Iglehart D, Lu KP. Modeling breast cancer in vivo and ex vivo reveals an essential role of Pin1 in tumorigenesis. EMBO J 2004;23:3397-407.
21. Moretto-Zita M, Jin H, Shen Z, Zhao T, Briggs SP, Xu Y. Phosphorylation stabilizes Nanog by promoting its interaction with Pin1. Proc Natl Acad Sci U S A 2010;107:13312-7.
22. Nishi M, Akutsu H, Masui S, Kondo A, Nagashima Y, Kimura H, et al. A distinct role for Pin1 in the induction and maintenance of pluripotency. J Biol Chem 2011;286:11593-603.
23. Lee DY, Shatseva T, Jeyapalan Z, Du WW, Deng Z, Yang BB. A 30- untranslated region (30UTR) induces organ adhesion by regulating miR-199a functions. PLoS ONE 2009;4:e4527.
24. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin- Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature 2006;439:84-8.
25. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, et al. Purification and unique properties of mammary epithelial stem cells. Nature 2006;439:993-7.
26. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003;100:3983-8.
27. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1:555-67.
28. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15.
29. Bonnefoix T, Bonnefoix P, Callanan M, Verdiel P, Sotto JJ. Graphical representation of a generalized linear model-based statistical test estimating the fit of the single-hit Poisson model to limiting dilution assays. J Immunol 2001;167:5725-30.
30. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, et al
31. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are micro- RNA targets. Cell 2005;120:15-20.
32. Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL, et al. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev 2001;15:50-65.
33. Uchida T, Takamiya M, Takahashi M, Miyashita H, Ikeda H, Terada T, et al. Pin1 and Par14 peptidyl prolyl isomerase inhibitors block cell proliferation. Chem Biol 2003;10:15-24.
34. Nakamura K, Greenwood A, Binder L, Bigio EH, Denial S, Nicholson L, et al. Proline isomer-specific antibodies reveal the early pathogenic tau conformation in Alzheimer's disease. Cell 2012;149:232-44.
35. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008;40:499-507.
36. Merlos-Suarez A, Barriga FM, Jung P, Iglesias M, Cespedes MV, Rossell D, et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 2011; 8:511-24.
37. Visvader JE. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 2009;23:2563-77.
38. Zhang Y, Daum S, Wildemann D, Zhou XZ, Verdecia MA, Bowman ME, et al. Structural basis for high-affinity peptide inhibition of human Pin1. ACS Chem Biol 2007;2:320-8.
39. Ayala G, Wang D, Wulf G, Frolov A, Li R, Sowadski J, et al. The prolyl isomerase Pin1 is a novel prognostic marker in human prostate cancer. Cancer Res 2003;63:6244-51.
40. Lu J, Hu Z, Wei S, Wang LE, Liu Z, El-Naggar AK, et al. A novel functional variant (-842G>C) in the PIN1 promoter contributes to decreased risk of squamous cell carcinoma of the head and neck by diminishing the promoter activity. Carcinogenesis 2009;30:1717-21.
41. Lu J, Yang L, Zhao H, Liu B, Li Y, Wu H, et al. The polymorphism and haplotypes of PIN1 gene are associated with the risk of lung cancer in Southern and Eastern Chinese populations. Hum Mutat 2011;32: 1299-308.
42. Ryo A, Uemura H, Ishiguro H, Saitoh T, Yamaguchi A, Perrem K, et al. Stable suppression of tumorigenicity by Pin1-targeted RNA interference in prostate cancer. Clin Cancer Res 2005;11:7523-31.
43. Dong L, Marakovits J, Hou X, Guo C, Greasley S, Dagostino E, et al. Structure-based design of novel human Pin1 inhibitors (II). Bioorg Med Chem Lett 2010;20:2210-4.
44. Guo C, Hou X, Dong L, Dagostino E, Greasley S, Ferre R, et al. Structure-based design of novel human Pin1 inhibitors (I). Bioorg Med Chem Lett 2009;19:5613-6.
45. Liu T, Liu Y, Kao HY, Pei D. Membrane permeable cyclic peptidyl inhibitors against human Peptidylprolyl Isomerase Pin1. J Med Chem 2010;53:2494-501.
46. Potter A, Oldfield V, Nunns C, Fromont C, Ray S, Northfield CJ, et al. Discovery of cell-active phenyl-imidazole Pin1 inhibitors by structureguided fragment evolution. Bioorg Med Chem Lett 2010;20:6483-8.
47. Potter AJ, Ray S, Gueritz L, Nunns CL, Bryant CJ, Scrace SF, et al. Structure-guided design of alpha-amino acid-derived Pin1 inhibitors. Bioorg Med Chem Lett 2010;20:586-90.
48. Wildemann D, Erdmann F, Alvarez BH, Stoller G, Zhou XZ, Fanghanel J, et al. Nanomolar inhibitors of the peptidyl prolyl cis/trans isomerase Pin1 from combinatorial peptide libraries. J Med Chem 2006;49: 2147-50.
49. Zhang Y, Fussel S, Reimer U, Schutkowski M, Fischer G. Substratebased design of reversible Pin1 inhibitors. Biochemistry (Mosc) 2002;41:11868-77.
50. Moore JD, Potter A. Pin1 inhibitors: Pitfalls, progress and cellular pharmacology. Bioorg Med Chem Lett 2013;23:4283-91.