Pin1 regulates centrosome duplication, and its overexpression induces centrosome amplification, chromosome instability, and oncogenesis

Molecular and Cellular Biology

Volumn 26, Issue 4, 2006, Pages 1463-1479

  Suizu, Futoshi ^a   Ryo, Akihide ^a   Wulf, Gerburg ^a   Lim, Jormay ^a   Lu, Kun Ping ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Laboratory of Cancer Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOMERASE; PEPTIDYLPROLYL ISOMERASE PIN1; UNCLASSIFIED DRUG;

ANEUPLOIDY; ANIMAL CELL; ARTICLE; BREAST CANCER; BREAST HYPERPLASIA; CARCINOGENESIS; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL TRANSFORMATION; CENTROSOME; CHO CELL; CHROMOSOMAL INSTABILITY; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA SYNTHESIS; FIBROBLAST; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; INTERPHASE; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; REGULATORY MECHANISM; TRANSGENIC MOUSE;

AMINO ACID MOTIFS; ANEUPLOIDY; ANIMALS; BREAST NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; CENTROSOME; CHO CELLS; CHROMOSOMAL INSTABILITY; CRICETINAE; FEMALE; GENE EXPRESSION; HUMANS; INTERPHASE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOSIS; NIH 3T3 CELLS; PEPTIDYLPROLYL ISOMERASE; PHOSPHORYLATION;

ANIMALIA; MUS MUSCULUS;

EID: 32044460171     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.4.1463-1479.2006     Document Type: Article

References (90)

1. Andersen, J. S., C. J. Wilkinson, T. Mayor, P. Mortensen, E. A. Nigg, and M. Mann. 2003. Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426:570-574.
2. Atchison, F. W., B. Capel, and A. R. Means. 2003. Pin1 regulates the timing of mammalian primordial germ cell proliferation. Development 130:3579-3586.
3. Ayala, G., D. Wang, G. Wulf, A. Frolov, R. Le, T. Wheeler, J. M. Sowadski, K. P. Lu, and L. Bao. 2003. Pin1 is a novel prognostic marker in prostate cancer. Cancer Res. 63:6244-6251.
4. Balczon, R., L. Bao, W. E. Zimmer, K. Brown, R. P. Zinkowski, and B. R. Brinkley. 1995. Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells. J. Cell Biol. 130:105-115.
5. Bao, L., G. Sauter, J. Sowadski, K. P. Lu, and D. Wang. 2004. Prevalent overexpression of prolyl isomerase Pin1 in human cancers. Am. J. Pathol. 164:1727-1737.
6. Borel, F., O. D. Lohez, F. B. Lacroix, and R. L. Margolis. 2002. Multiple centrosomes arise from tetraploidy checkpoint failure and mitotic centrosome clusters in p53 and RB pocket protein-compromised cells. Proc. Natl. Acad. Sci. USA 99:9819-9824.
7. Bornens, M. 2002. Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14:25-34.
8. Bornens, M., M. Paintrand, J. Berges, M. C. Marty, and E. Karsenti. 1987. Structural and chemical characterization of isolated centrosomes. Cell Motil. Cytoskeleton 8:238-249.
9. Cato, A. C., J. Weinmann, S. Mink, H. Ponta, D. Henderson, and A. Sonnenberg. 1989. The regulation of expression of mouse mammary tumor virus DNA by steroid hormones and growth factors. J. Steroid Biochem. 34:139-143.
10. Chen, Z., V. B. Indjeian, M. McManus, L. Wang, and B. D. Dynlacht. 2002. CP110, a cell cycle-dependent CDK substrate, regulates centrosome duplication in human cells. Dev. Cell 3:339-350.
11. Choi, Y. W., D. Henrard, I. Lee, and S. R. Ross. 1987. The mouse mammary tumor virus long terminal repeat directs expression in epithelial and lymphoid cells of different tissues in transgenic mice. J. Virol. 61:3013-3019.
12. D'Assoro, A. B., S. L. Barrett, C. Folk, V. C. Negron, K. Boeneman, R. Busby, C. Whitehead, F. Stivala, W. L. Lingle, and J. L. Salisbury. 2002. Amplified centrosomes in breast cancer: a potential indicator of tumor aggressiveness. Breast Cancer Res. Treat. 75:25-34.
13. 1/S cell cycle checkpoint. Oncogene 23:4068-4075.
14. D'Assoro, A. B., W. L. Lingle, and J. L. Salisbury. 2002. Centrosome amplification and the development of cancer. Oncogene 21:6146-6153.
15. Deshpande, A., P. Sicinski, and P. W. Hinds. 2005. Cyclins and cdks in development and cancer: a perspective. Oncogene 24:2909-2915.
16. Dougherty, M. K., J. Müller, D. A. Ritt, X. Z. Zhou, M. Zhou, T. D. Copeland, T. P. Conrads, T. Veenstra, K. P. Lu, and D. K. Morrison. 2005. Regulation of Raf-1 by direct feedback phosphorylation. Mol. Cell 17:215-224.
17. Doxsey, S. 2002. Duplicating dangerously: linking centrosome duplication and aneuploidy. Mol. Cell 10:439-440.
18. Doxsey, S., D. McCollum, and W. Theurkauf. 2005. Centrosomes in cellular regulation. Annu. Rev. Cell Dev. Biol. 21:411-434.
19. Doxsey, S., W. Zimmerman, and K. Mikule. 2005. Centrosome control of the cell cycle. Trends Cell Biol. 15:303-311.
20. Duensing, S., A. Duensing, C. P. Crum, and K. Munger. 2001. Human papillomavirus type 16 E7 oncoprotein-induced abnormal centrosome synthesis is an early event in the evolving malignant phenotype. Cancer Res. 61:2356-2360.
21. Duensing, S., L. Y. Lee, A. Duensing, J. Basile, S. Piboonniyom, S. Gonzalez, C. P. Crum, and K. Munger. 2000. The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle. Proc. Natl. Acad. Sci. USA 97:10002-10007.
22. El-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
23. Fisk, H. A., and M. Winey. 2001. The mouse Mps1p-like kinase regulates centrosome duplication. Cell 106:95-104.
24. 0 arrest. Biochem. Biophys. Res. Commun. 265:658-663.
25. Fukasawa, K., T. Choi, R. Kuriyama, S. Rulong, and G. F. Vande Woude. 1996. Abnormal centrosome amplification in the absence of p53. Science 271:1744-1747.
26. Ghadimi, B. M., D. L. Sackett, M. J. Difilippantonio, E. Schrock, T. Neumann, A. Jauho, G. Auer, and T. Ried. 2000. Centrosome amplification and instability occurs exclusively in aneuploid, but not in diploid colorectal cancer cell lines, and correlates with numerical chromosomal aberrations. Genes Chromosomes Cancer 27:183-190.
27. Goepfert, T. M., Y. E. Adigun, L. Zhong, J. Gay, D. Medina, and W. R. Brinkley. 2002. Centrosome amplification and overexpression of aurora A are early events in rat mammary carcinogenesis. Cancer Res. 62:4115-4122.
28. 1 cyclin-dependent kinases. Cell 75:805-816.
29. Reference deleted.
30. Hennighausen, L. 2000. Mouse models for breast cancer. Breast Cancer Res. 2:2-7.
31. Hennighausen, L., R. J. Wall, U. Tillmann, M. Li, and P. A. Furth. 1995. Conditional gene expression in secretory tissues and skin of transgenic mice using the MMTV-LTR and the tetracycline responsive system. J. Cell Biochem. 59:463-472.
32. Hinchcliffe, E. H., C. Li, E. A. Thompson, J. L. Maller, and G. Sluder. 1999. Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283:851-854.
33. Hinchcliffe, E. H., and G. Sluder. 2001. "It takes two to tango": understanding how centrosome duplication is regulated throughout the cell cycle. Genes Dev. 15:1167-1181.
34. Katayama, H., K. Sasai, H. Kawai, Z. M. Yuan, J. Bondaruk, F. Suzuki, S. Fujii, R. B. Arlinghaus, B. A. Czerniak, and S. Sen. 2004. Phosphorylation by aurora kinase A induces Mdm2-mediated destabilization and inhibition of p53. Nat. Genet. 36:55-62.
35. Kuriyama, R., S. Dasgupta, and G. G. Borisy. 1986. Independence of centriole formation and initiation of DNA synthesis in Chinese hamster ovary cells. Cell Motil. Cytoskeleton 6:355-362.
36. Lacey, K. R., P. K. Jackson, and T. Stearns. 1999. Cyclin-dependent kinase control of centrosome duplication. Proc. Natl. Acad. Sci. USA 96:2817-2822.
37. Lamb, J., S. Ramaswamy, H. L. Ford, B. Contreras, R. V. Martinez, F. S. Kittrell, C. A. Zahnow, N. Patterson, T. R. Golub, and M. E. Ewen. 2003. A mechanism of cyclin D1 action encoded in the patterns of gene expression in human cancer. Cell 114:323-334.
38. Lingle, W. L., S. L. Barrett, V. C. Negron, A. B. D'Assoro, K. Boeneman, W. Liu, C. M. Whitehead, C. Reynolds, and J. L. Salisbury. 2002. Centrosome amplification drives chromosomal instability in breast tumor development. Proc. Natl. Acad. Sci. USA 99:1978-1983.
39. Lingle, W. L., W. H. Lutz, J. N. Ingle, N. J. Maihle, and J. L. Salisbury. 1998. Centrosome hypertrophy in human breast tumors: implications for genomic stability and cell polarity. Proc. Natl. Acad. Sci. USA 95:2950-2955.
40. Lingle, W. L., and J. L. Salisbury. 1999. Altered centrosome structure is associated with abnormal mitoses in human breast tumors. Am. J. Pathol. 155:1941-1951.
41. Liou, Y. C., R. Ryo, H. K. Huang, P. J. Lu, R. Bronson, F. Fujimori, U. Uchidafl, T. Hunter, and K. P. Lu. 2002. Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1-null phenotypes. Proc. Natl. Acad. Sci. USA 99:1335-1340.
42. Lu, K. P. 2004. Pinning down cell signaling, cancer and Alzheimer's disease. Trends Biochem. Sci. 29:200-209.
43. Lu, K. P. 2003. Prolyl isomerase Pin1 as a molecular target for cancer diagnostics and therapeutics. Cancer Cell 4:175-180.
44. Lu, K. P., S. D. Hanes, and T. Hunter. 1996. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380:544-547.
45. Lu, K. P., Y. C. Liou, and X. Z. Zhou. 2002. Pinning down the proline-directed phosphorylation signaling. Trends Cell Biol. 12:164-172.
46. Lu, P. J., X. Z. Zhou, Y. C. Liou, J. P. Noel, and K. P. Lu. 2002. Critical role of WW domain phosphorylation in regulating its phosphoserine-binding activity and the Pin1 function. J. Biol. Chem. 277:2381-2384.
47. Lu, P. J., X. Z. Zhou, M. Shen, and K. P. Lu. 1999. A function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 283:1325-1328.
48. Mantovani, F., S. Piazza, M. Gostissa, S. Strano, P. Zacchi, R. Mantovani, G. Blandino, and G. Del Sal. 2004. Pin1 links the activities of c-Abl and p300 in regulating p73 function. Mol. Cell 14:625-636.
49. Matsumoto, Y., K. Hayashi, and E. Nishida. 1999. Cyclin-dependent kinase 2 (Cdk2) is required for centrosome duplication in mammalian cells. Curr. Biol. 9:429-432.
50. McDonald, K. 1984. Osmium ferricyanide fixation improves microfilament preservation and membrane visualization in a variety of animal cell types. J. Ultrastruct Res. 86:107-118.
51. -/- cells. EMBO J. 21:483-492.
52. Meraldi, P., J. Lukas, A. M. Fry, J. Bartek, and E. A. Nigg. 1999. Centrosome duplication in mammalian somatic cells requires E2F and Cdk2-cyclin A. Nat. Cell Biol. 1:88-93.
53. Meraldi, P., and E. A. Nigg. 2002. The centrosome cycle. FEBS Lett. 521:9-13.
54. Muller, W. J., E. Sinn, P. K. Pattengale, R. Wallace, and P. Leder. 1988. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54:105-115.
55. Nelsen, C. J., R. Kuriyama, B. Hirsch, V. C. Negron, W. L. Lingle, M. M. Goggin, M. W. Stanley, and J. H. Albrecht. 2005. Short term cyclin D1 overexpression induces centrosome amplification, mitotic spindle abnormalities, and aneuploidy. J. Biol. Chem. 280:768-776.
56. Nigg, E. A. 2002. Centrosome aberrations: cause or consequence of cancer progression? Nat. Rev. Cancer 2:815-825.
57. Okuda, M., H. F. Horn, P. Tarapore, Y. Tokuyama, A. G. Smulian, P. K. Chan, E. S. Knudsen, I. A. Hofmann, J. D. Snyder, K. E. Bove, and K. Fukasawa. 2000. Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication. Cell 103:127-140.
58. Pihan, G., and S. J. Doxsey. 2003. Mutations and aneuploidy: co-conspirators in cancer? Cancer Cell 4:89-94.
59. Pihan, G. A., and S. J. Doxsey. 1999. The mitotic machinery as a source of genetic instability in cancer. Semin. Cancer Biol. 9:289-302.
60. Pihan, G. A., A. Purohit, J. Wallace, H. Knecht, B. Woda, P. Quesenberry, and S. J. Doxsey. 1998. Centrosome defects and genetic instability in malignant tumors. Cancer Res. 58:3974-3985.
61. Pihan, G. A., A. Purohit, J. Wallace, R. Malhotra, L. Liotta, and S. J. Doxsey. 2001. Centrosome defects can account for cellular and genetic changes that characterize prostate cancer progression. Cancer Res. 61:2212-2219.
62. Pihan, G. A., J. Wallace, Y. Zhou, and S. J. Doxsey. 2003. Centrosome abnormalities and chromosome instability occur together in pre-invasive carcinomas. Cancer Res. 63:1398-1404.
63. Ranganathan, R., K. P. Lu, T. Hunter, and J. P. Noel. 1997. Structural and functional analysis of the mitotic peptidyl-prolyl isomerase Pin1 suggests that substrate recognition is phosphorylation dependent. Cell 89:875-886.
64. Rippmann, J. F., S. Hobbie, C. Daiber, B. Guilliard, M. Bauer, J. Birk, H. Nar, P. Garin-Chesa, W. J. Rettig, and A. Schnapp. 2000. Phosphorylation- dependent proline isomerization catalyzed by Pin1 is essential for tumor cell survival and entry into mitosis. Cell Growth Differ. 11:409-416.
65. Ryo, A., Y. C. Liou, K. P. Lu, and G. Wulf. 2003. Prolyl isomerase Pin1: a catalyst for oncogenesis and a potential therapeutic target in cancer. J. Cell Sci. 116:773-783.
66. Ryo, A., Y. C. Liou, G. Wulf, N. Nakamura, S. W. Lee, and K. P. Lu. 2002. PIN1 is an E2F target gene essential for the Neu/Ras-induced transformation of mammary epithelial cells. Mol. Cell. Biol. 22:5281-5295.
67. Ryo, A., N. Nakamura, G. Wulf, Y. C. Liou, and K. P. Lu. 2001. Pin1 regulates turnover and subcellular localization of beta-catenin by inhibiting its interaction with APC. Nature Cell Biol. 3:793-801.
68. Ryo, A., F. Suizu, Y. Yoshida, K. Perrem, Y. C. Liou, G. Wulf, R. Rottapel, S. Yamaoka, and K. P. Lu. 2003. Regulation of NF-κB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol. Cell 12:1413-1426.
69. Saavedra, H. I., B. Maiti, C. Timmers, R. Altura, Y. Tokuyama, K. Fukasawa, and G. Leone. 2003. Inactivation of E2F3 results in centrosome amplification. Cancer Cell 3:333-346.
70. Salisbury, J. L., A. B. D'Assoro, and W. L. Lingle. 2004. Centrosome amplification and the origin of chromosomal instability in breast cancer. J. Mammary Gland Biol. Neoplasia 9:275-283.
71. Sato, N., K. Mizumoto, M. Nakamura, N. Maehara, Y. A. Minamishima, S. Nishio, E. Nagai, and M. Tanaka. 2001. Correlation between centrosome abnormalities and chromosomal instability in human pancreatic cancer cells. Cancer Genet. Cytogenet. 126:13-19.
72. Sicinski, P., J. L. Donaher, S. B. Parker, T. Li, A. Fazeli, H. Gardner, S. Z. Haslam, R. T. Bronson, S. J. Elledge, and R. A. Weinberg. 1995. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82:621-630.
73. Sinn, E., W. Muller, P. Pattengale, I. Tepler, R. Wallace, and P. Leder. 1987. Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo. Cell 49:465-475.
74. Stukenberg, P. T., and M. W. Kirschner. 2001. Pin1 acts catalytically to promote a conformational change in Cdc25. Mol. Cell 7:1071-1083.
75. Tarapore, P., H. F. Horn, Y. Tokuyama, and K. Fukasawa. 2001. Direct regulation of the centrosome duplication cycle by the p53-p21Waf1/Cip1 pathway. Oncogene 20:3173-3184.
76. Tutt, A., A. Gabriel, D. Bertwistle, F. Connor, H. Paterson, J. Peacock, G. Ross, and A. Ashworth. 1999. Absence of Brca2 causes genome instability by chromosome breakage and loss associated with centrosome amplification. Curr. Biol. 9:1107-1110.
77. Wang, T. C., R. D. Cardiff, L. Zukerberg, E. Lees, A. Arnold, and E. V. Schmidt. 1994. Mammary hyperplasia and carcinoma in MMTV-cyclin D1 transgenic mice. Nature 369:669-671.
78. Winkler, K. E., K. I. Swenson, S. Kornbluth, and A. R. Means. 2000. Requirement of the prolyl isomerase Pin1 for the replication checkpoint. Science 287:1644-1647.
79. Wulf, G., G. Finn, F. Suizu, and K. P. Lu. 2005. Phosphorylation-specific prolyl isomerization: is there an underlying theme? Nature Cell Biol. 7:435-441.
80. Wulf, G., P. Garg, Y. C. Liou, D. Iglehart, and K. P. Lu. 2004. Modeling breast cancer in vivo and ex vivo reveals an essential role of Pin1 in tumorigenesis. EMBO J. 23:3397-3407.
81. Wulf, G. M., Y. C. Liou, A. Ryo, S. W. Lee, and K. P. Lu. 2002. Role of Pin1 in the regulation of p53 stability and p21 transactivation, and cell cycle checkpoints in response to DNA damage. J. Biol. Chem. 277:47976-47979.
82. Wulf, G. M., A. Ryo, G. G. Wulf, S. W. Lee, T. Niu, and K. P. Lu. 2001. Pin1 is overexpressed in breast cancer and potentiates the transcriptional activity of phosphorylated c-Jun towards the cyclin D1 gene. EMBO J. 20:3459-3472.
83. 2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Mol. Cell 3:389-395.
84. Yaffe, M. B., M. Schutkowski, M. Shen, X. Z. Zhou, P. T. Stukenberg, J. Rahfeld, J. Xu, J. Kuang, M. W. Kirschner, G. Fischer, L. C. Cantley, and K. P. Lu. 1997. Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 278:1957-1960.
85. Yeh, E., M. Cunningham, H. Arnold, D. Chasse, T. Monteith, G. Ivaldi, W. C. Hahn, P. T. Stukenberg, S. Shenolikar, T. Uchida, C. M. Counter, J. R. Nevins, A. R. Means, and R. Sears. 2004. A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat. Cell Biol. 6:308-318.
86. Yu, Q., Y. Geng, and P. Sicinski. 2001. Specific protection against breast cancers by cyclin D1 ablation. Nature 411:1017-1021.
87. Zacchi, P., M. Gostissa, T. Uchida, C. Salvagno, A. Avolio, S. Voliniak, Z. Ronai, G. Blandino, C. Schneider, and G. Del Sal. 2002. The prolyl isomerase Pin1 reveals a mechanism to control p53 functions after genotoxic insults. Nature 419:853-857.
88. Zheng, H., H. You, X. Z. Zhou, S. A. Murray, T. Uchida, G. Wulf, L. Gu, X. Tang, K. P. Lu, and Z. X. J. Xiao. 2002. The prolyl isomerase Pin1 is a regulator of p53 in genotoxic response. Nature 419:849-853.
89. Zhou, H., J. Kuang, L. Zhong, W. L. Kuo, J. W. Gray, A. Sahin, B. R. Brinkley, and S. Sen. 1998. Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation. Nat. Genet. 20:189-193.
90. Zhou, X. Z., O. Kops, A. Werner, P. J. Lu, M. Shen, G. Stoller, G. Küllertz, M. Stark, G. Fischer, and K. P. Lu. 2000. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol. Cell 6:873-883.