The prolyl isomerase Pin1 in breast development and cancer

Breast Cancer Research

Volumn 5, Issue 2, 2003, Pages 76-82

  Wulf, Gerburg ^a   Ryo, Akihide ^a   Liou, Yih Cherng ^a   Lu, Kun Ping ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Breast cancer; Breast development; Cyclin D1; Phosphorylation signaling; Pin1

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIN D1; CYCLOPHILIN; FLAVOPIRIDOL; GEFITINIB; PROTEIN INHIBITOR; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; RAS PROTEIN; TIPIFARNIB; TRASTUZUMAB; UNCLASSIFIED DRUG;

BREAST CANCER; BREAST CARCINOGENESIS; BREAST DEVELOPMENT; BREAST EPITHELIUM; CELL ACTIVITY; CELL DIVISION; CELL PROLIFERATION; CELL TRANSFORMATION; COLON ADENOCARCINOMA; DRUG TARGETING; EPITHELIUM CELL; GENE FUNCTION; GENE OVEREXPRESSION; HUMAN; INHIBITION KINETICS; ISOMERISM; KNOCKOUT MOUSE; LUNG ADENOCARCINOMA; LYMPHOMA; MELANOMA; MOUSE; NONHUMAN; PREGNANCY; PROSTATE ADENOCARCINOMA; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REVIEW; SARCOMA; UPREGULATION;

ANIMALS; BREAST; BREAST NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAMMARY GLANDS, ANIMAL; MICE; PEPTIDYLPROLYL ISOMERASE;

EID: 0037230513     PISSN: 14655411     EISSN: None     Source Type: Journal    
DOI: 10.1186/bcr572     Document Type: Review

References (96)

1. Hanahan D, Weinberg RA: The hallmarks of cancer. Cell 2000, 100:57-70.
2. Blume-Jensen P, Hunter T: Oncogenic kinase signalling. Nature 2001, 411:355-365.
3. Lu KP, Liou YC, Zhou XZ: Pinning down the proline-directed phosphorylation signaling. Trends Cell Biol 2002, 12:164-172.
4. Andrechek ER, Muller WJ: Tyrosine kinase signalling in breast cancer: tyrosine kinase-mediated signal transduction in transgenic mouse models of human breast cancer. Breast Cancer Res 2000, 2:211-216.
5. Lee RJ, Albanese C, Fu M, D'Amico M, Lin B, Watanabe G, Haines GK, 3rd, Siegel PM, Hung MC, Yarden Y, Horowitz JM, Muller WJ, Pestell RG: Cyclin D1 is required for transformation by activated Neu and is induced through an E2F-dependent signaling pathway. Mol Cell Biol 2000, 20:672-683.
6. Harari D, Yarden Y: Molecular mechanisms underlying ErbB2/HER2 action in breast cancer. Oncogene 2000, 19:6102-6114.
7. Albanese C, Johnson J, Watanabe G, Eklund N, Vu D, Arnold A, Pestell RG: Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J Biol Chem 1995, 270:23589-23597.
8. Lin SY, Xia W, Wang JC, Kwong KY, Spohn B, Wen Y, Pestell RG, Hung MC: Beta-catenin, a novel prognostic marker for breast cancer: its roles in cyclin D1 expression and cancer progression. Proc Natl Acad Sci USA 2000, 97:4262-4266.
9. Diehl JA, Zindy F, Sherr CJ: Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev 1997 11:957-972.
10. Diehl JA, Cheng M, Roussel MF, Sherr CJ: Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998, 12:3499-3511.
11. Alt JR, Cleveland JL, Hannink M, Diehl JA: Phosphorylation-dependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes Dev 2000, 14: 3102-3114.
12. Gillett C , Fantl V, Smith R, Fisher C, Bartek J, Dickson C, Barnes D, Peters G: Amplification and overexpression of cyclin D1 in breast cancer detected by immunohistochemical staining. Cancer Res 1994, 54:1812-1817.
13. Bartkova J, Lukas J, Muller H, Lutzhoft D, Strauss M, Bartek J: Cyclin D1 protein expression and function in human breast cancer. Int J Cancer 1994, 57:353-361.
14. Hinds PW, Dowdy SF, Eaton EN, Arnold A, Weinberg RA: Function of a human cyclin gene as an oncogene. Proc Natl Acad Sci USA 1994, 91:709-713.
15. Wang TC, Cardiff RD, Zukerberg L, Lees E, Arnold A, Schmidt EV: Mammary hyperplasia and carcinoma in MMTV-cyclin D1 transgenic mice. Nature 1994, 369:669-671.
16. Yu Q, Geng Y, Sicinski P: Specific protection against breast cancers by cyclin D1 ablation. Nature 2001, 411:1017-1021.
17. Lu KP, Hanes SD, Hunter T: A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 1996, 380:544-547.
18. Yaffe MB, Schutkowski M, Shen M, Zhou XZ, Stukenberg PT, Rahfeld J, Xu J, Kuang J, Kirschner MW, Fischer G, Cantley LC, Lu KP: Sequence-specific and phosphorylation-dependent proline isomerization: A potential mitotic regulatory mechanism. Science 1997, 278:1957-1960.
19. Ranganathan R, Lu KP, Hunter T, Noel JP: Structural and functional analysis of the mitotic peptidyl-prolyl isomerase Pin1 suggests that substrate recognition is phosphorylation dependent. Cell 1997, 89:875-886.
20. Fischer G: Peptidyl-prolyl cis/trans isomerases. Angew Chem Int Ed Engl 1994, 33:1415-1436.
21. Hunter T: Prolyl isomerase and nuclear function. Cell 1998, 92: 141-143.
22. Dolinski K, Muir S, Cardenas M, Heitman J: All cyclophilins and FKBPs, individually and collectively, are dispensable for viability in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1997, 94:13093-13098.
23. Shen M, Stukenberg PT, Kirschner MW, Lu KP: The essential mitotic peptidyl-prolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins. Genes Dev 1998, 12:706-720.
24. Crenshaw DG, Yang J, Means AR, Kornbluth S: The mitotic peptidyl-prolyl isomerase, Pin1, interacts with Cdc25 and Plx1. EMBO J 1998, 17:1315-1327.
25. Lu PJ, Zhou XZ, Shen M, Lu KP: A function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 1999, 283:1325-1328.
26. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP: The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 1999, 399:784-788.
27. Zhou XZ, Lu PJ, Wulf G, Lu KP: Phosphorylation-dependent prolyl isomerization: A novel signaling regulatory mechanism. Cell Mol Life Sci 1999, 56:788-806.
28. Zhou XZ, Kops O, Werner A, Lu PJ, Shen M, Stoller G, Küllertz G, Stark M, Fischer G, Lu KP: Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell 2000, 6:873-883.
29. Stukenberg PT, Kirschner MW: Pin1 acts catalytically to promote a conformational change in Cdc25. Mol Cell 2001, 7: 1071-1083.
30. Patra D, Wang SX, Kumagai A, Dunphy WG: The xenopus Suc1/Cks protein promotes the phosphorylation of G(2)/M regulators. J Biol Chem 1999, 274:36839-36842.
31. Fujimori F, Takahashi K, Uchida C, Uchida T: Mice lacking Pin1 develop normally, but are defective in entering cell cycle from G(0) arrest. Biochem Biophys Res Commun 1999, 265:658-663.
32. Winkler KE, Swenson KI, Kornbluth S, Means AR: Requirement of the prolyl isomerase Pin1 for the replication checkpoint. Science 2000, 287:1644-1647.
33. Gerez L, Mohrmann K, va Raak M, Jongeneelen M, Zhou XZ, Lu KP, van der Sluijs P: Accumulation of rab4GTP in the cytoplasm and association with the peptidyl-prolyl isomerase Pin1 during mitosis. Mol Biol Cell 2000, 11:2201-2211.
34. Wulf GM, Ryo A, Wulf GG, Lee SW, Niu T, Lu KP: Pin1 is overexpressed in breast cancer and potentiates the transcriptional activity of phosphorylated c-Jun towards the cyclin D1 gene. EMBO J 2001, 20:3459-3472.
35. Ryo A, Nakamura N, Wulf G, Liou YC, Lu KP: Pin1 regulates turnover and subcellular localization of beta-catenin by inhibiting its interaction with APC. Nature Cell Biol 2001, 3: 793-801.
36. Ryo A, Liou YC, Wulf G, Nakamura N, Lee SW, Lu KP: Pin1 is an E2F target gene essential for the Neu/Ras-induced transformation of mammary epithelial cells. Mol Cell Biol 2002, 22: 5281-5295.
37. Liou YC, Ryo R, Huang HK, Lu PJ, Bronson R, Fujimori F, Uchida U, Hunter T, Lu KP: Loss of Pin1 function in the mouse resembles the cyclin D1-null phenotypes. Proc Natl Acad Sci USA 2002, 99:1335-1340.
38. Albert A, Lavoie S, Vincent M: A hyperphosphorylated form of RNA polymerase II is the major interphase antigen of the phosphoprotein antibody MPM-2 and interacts with the peptidyl-prolyl isomerase Pin1. J Cell Sci 1999, 112:2493-2500.
39. Morris DP, Phatnani HP, Greenleaf AL: Phospho-carboxyl-terminal domain binding and the role of a prolyl isomerase in pre-mRNA 3′-end formation. J Biol Chem 1999, 274:31583-31587.
40. Arevalo-Rodriguez M, Cardenas ME, Wu X, Hanes SD, Heitman J: Cyclophilin A and Ess1 interact with and regulate silencing by the Sin3- Rpd3 histone deacetylase. EMBO J 2000, 19:3739-3749.
41. Wu X, Wilcox CB, Devasahayam G, Hackett RL, Arevalo-Rodriguez M, Cardenas ME, Heitman J, Hanes SD: The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO J 2000, 19:3727-3738.
42. Hsu T, McRackan D, Vincent TS, Gert De Couet H: Drosophila Pin1 prolyl isomerase Dodo is a MAP kinase signal responder during oogenesis. Nat Cell Biol 2001, 3:538-543.
43. Liu W, Youn HD, Zhou XZ, Lu KP, Liu JO: Binding and regulation of the transcription factor NFAT by the peptidyl prolyl cistrans isomerase Pin1. FEBS Lett 2001, 496:105-108.
44. Kops O, Zhou XZ, Lu KP: Pin1 enhances the dephosphorylation of the C-terminal domain of the RNA polymerase II by Fcp1. FEBS Lett 2002, 513:305-311.
45. Wulf GM, Liou YC, Ryo A, W. LS, Lu KP: Role of Pin1 in the regulation of p53 stability and p21 transactivation, and cell cycle checkpoints in response to DNA damage. J Biol Chem 2002, 277:47976-47979.
46. Zheng H, You H, Zhou XZ, Murray SA, Uchida T, Wulf G, Gu L, Tang X, Lu KP, Xiao ZXJ: The prolyl isomerase Pin1 is a regulator of p53 in genotoxic response. Nature 2002, 419:849-853.
47. Zacchi P, Gostissa M, Uchida T, Salvagno C, Avolio A, Voliniak 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.
48. Sudol M, Hunter T: New wrinkles for an old domain. Cell 2000, 103:1001-1004.
49. Shaw PE: Peptidyl-prolyl isomerases: a new twist to transcription. EMBO Rep 2002, 3:521-526.
50. Lu KP, Liou YC, Vincent I: Proline-directed phosphorylation and isomerization in mitosis and in Alzheimer's disease (a hypothesis). BioEssays 2002, in press.
51. Daniel CW, Silberstein GB: Developmental biology of the mammary gland. In: The Mammary Gland Neville MC, Daniel CW (eds). New York: Plenum Pub Corp.; 1987:3-36.
52. Sakakura T: Mammary embryogenesis. In: The Mammary Gland. Neville MC, Daniel CW (eds). New York: Plenum Pub Corp.; 1987:37-66.
53. Russo J, Russo IH: Development of the human mammary gland. In: The Mammary Gland. Neville MC, Daniel CW (eds). New York: Plenum Pub Corp.; 1987:67-93.
54. Sicinski P, Donaher JL, Parker SB, Li T, Fazeli A, Gardner H, Haslam SZ, Bronson RT, Elledge SJ, Weinberg RA: Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 1995, 82:621-630.
55. Fantl V, Stamp G, Andrews A, Rosewell I, Dickson C: Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes Dev 1995, 9:2364-2372.
56. van Diest PJ, Michalides RJ, Jannink L, van der Valk P, Peterse HL, de Jong JS, Meijer CJ, Baak JP: Cyclin D1 expression in invasive breast cancer. Correlations and prognostic value. Am J Pathol 1997, 150:705-711.
57. Bieche I, Olivi M, Nogues C, Vidaud M, Lidereau R: Prognostic value of CCND1 gene status in sporadic breast tumours, as determined by real-time quantitative PCR assays. Br J Cancer 2002, 86:580-586.
58. Naidu R, Wahab NA, Yadav MM, Kutty MK: Expression and amplification of cyclin D1 in primary breast carcinomas: relationship with histopathological types and clinico-pathological parameters. Oncol Rep 2002, 9:409-416.
59. Fantl V, Smith R, Brookes S, Dickson C, Peters G: Chromosome 11q13 abnormalities in human breast cancer [see comments]. Cancer Surv 1993, 18:77-94.
60. MacLachlan TK, Somasundaram K, Sgagias M, Shifman Y, Muschel RJ, Cowan KH, El-Deiry WS: BRCA1 effects on the cell cycle and the DNA damage response are linked to altered gene expression. J Biol Chem 2000, 275:2777-2785.
61. Lu PJ, Zhou XZ, Liou YC, Noel JP, Lu KP: Critical role of WW domain phosphorylation in regulating its phosphoserine-binding activity and the Pin1 function. J Biol Chem 2002, 277: 2381-2384.
62. Zhang SY, Liu SC, Al-Saleem LF, Holloran D, Babb J, Guo X, Klein-Szanto AJ: E2F-1: a proliferative marker of breast neoplasia. Cancer Epidemiol Biomarkers Prev 2000, 9:395-401.
63. Nevins JR: The Rb/E2F pathway and cancer. Hum Mol Genet 2001, 10:699-703.
64. Weinberg RA: The retinoblastoma protein and cell cycle control. Cell 1995, 81:323-330.
65. Macleod K: pRb and E2f-1 in mouse development and tumorigenesis. Curr Opin Genet Dev 1999, 9:31-39.
66. Trimarchi JM, Lees JA: Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 2002, 3:11-20.
67. Hunter T, Karin M: The regulation of transcription by phosphorylation. Cell 1992, 70:375-387.
68. Whitmarsh AJ, Davis RJ: Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 1996, 74:589-607.
69. Karin M, Liu Z, Zandi E: AP-1 function and regulation. Curr Opin Cell Biol 1997, 9:240-246.
70. Binetruy B, Smeal T, Karin M: Ha-Ras augments c-Jun activity and stimulates phosphorylation of its activation domain. Nature 1991, 351:122-127.
71. Smeal T, Binetruy B, Mercola DA, Birrer M, Karin M: Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73. Nature 1991, 354: 494-496.
72. Derijard B, Hibi M, Wu IH, Barrett T, Su B, Deng T, Karin M, Davis RJ: JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 1994, 76:1025-1037.
73. Albanese C, D'Amico M, Reutens AT, Fu M, Watanabe G, Lee RJ, Kitsis RN, Henglein B, Avantaggiati M, Somasundaram K, Thimmapaya B, Pestell RG: Activation of the cyclin D1 gene by the E1A-associated protein p300 through AP-1 inhibits cellular apoptosis. J Biol Chem 1999, 274:34186-34195.
74. Bakiri L, Lallemand D, Bossy-Wetzel E, Yaniv M: Cell cycle-dependent variations in c-Jun and JunB phosphorylation: a role in the control of cyclin D1 expression. EMBO J 2000, 19: 2056-2068.
75. Robles AI, Rodriguez-Puebla ML, Glick AB, Trempus C, Hansen L, Sicinski P, Tennant RW, Weinberg RA, Yuspa SH, Conti CJ: Reduced skin tumor development in cyclin D1-deficient mice highlights the oncogenic ras pathway in vivo. Genes Dev 1998, 12:2469-2474.
76. Roose J, Huls G, van Beest M, Moerer P, van der Horn K, Goldschmeding R, Logtenberg T, Clevers H: Synergy between tumor suppressor APC and the bete-catenin-Tcf4 target Tcf1. Science 1999, 285:1923-1926.
77. Jonsson M, Borg A, Nilbert M, Andersson T: Involvement of adenomatous polyposis coli (APC)/beta-catenin signalling in human breast cancer. Eur J Cancer 2000, 36:242-248.
78. Schlosshauer PW, Brown SA, Eisinger K, Yan Q, Guglielminetti ER, Parsons R, Ellenson LH, Kitajewski J: APC truncation and increased bete-catenin levels in a human breast cancer cell line. Carcinogenesis 2000, 21:1453-1456.
79. Petersen OW, Ronnov-Jessen L, Howlett AR, Bissell MJ: Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci USA 1992, 89:9064-9068.
80. Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS: ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 2001, 3:785-792.
81. Druker BJ: Perspectives on the development of a molecularly targeted agent. Cancer Cell 2002, 1:31-36.
82. Chabner BA: Cytotoxic agents in the era of molecular targets and genomics. Oncologist 2002, 7 (suppl 2):34-41.
83. Ghosh S, Liu XP, Zheng Y, Uckun FM: Rational design of potent and selective EGFR tyrosine kinase inhibitors as anticancer agents. Curr Cancer Drug Targets 2001, 1:129-140.
84. Moulder SL, Yakes FM, Muthuswamy SK, Bianco R, Simpson JF, Arteaga CL: Epidermal growth factor receptor (HER1) tyrosine kinase inhibitor ZD1839 (Iressa) inhibits HER2/neu (erbB2)-overexpressing breast cancer cells in vitro and in vivo. Cancer Res 2001, 61:8887-8895.
85. Arteaga CL, Moulder SL, Yakes FM: HER (erbB) tyrosine kinase inhibitors in the treatment of breast cancer. Semin Oncol 2002, 29:4-10.
86. Nahta R, Iglehart JD, Kempkes B, Schmidt EV: Rate-limiting effects of Cyclin D1 in transformation by ErbB2 predicts synergy between herceptin and flavopiridol. Cancer Res 2002, 62:2267-2271.
87. Moasser MM, Basso A, Averbuch SD, Rosen N: The tyrosine kinase inhibitor ZD1839 ("Iressa") inhibits HER2-driven signaling and suppresses the growth of HER2-overexpressing tumor cells. Cancer Res 2001, 61:7184-7188.
88. Albanell J, Codony-Servat J, Rojo F, Del Campo JM, Sauleda S, Anido J, Raspall G, Giralt J, Rosello J, Nicholson RI, Mendelsohn J, Baselga J: Activated extracellular signal-regulated kinases: association with epidermal growth factor receptor/transforming growth factor alpha expression in head and neck squamous carcinoma and inhibition by anti-epidermal growth factor receptor treatments. Cancer Res 2001, 61:6500-6510.
89. Karp JE, Kaufmann SH, Adjei AA, Lancet JE, Wright JJ, End DW: Current status of clinical trials of farnesyltransferase inhibitors. Curr Opin Oncol 2001, 13:470-476.
90. Rippmann JF, Hobbie S, Daiber C, Guilliard B, Bauer M, Birk J, Nar H, Garin-Chesa P, Rettig WJ, Schnapp A: Phosphorylation-dependent proline isomerization catalyzed by Pin1 is essential for tumor cell survival and entry into mitosis. Cell Growth Differ 2000, 11:409-416.
91. Hennig L, Christner C, Kipping M, Schelbert B, Rucknagel KP, Grabley S, Kullertz G, Fischer G: Selective inactivation of parvulin-like peptidyl-prolyl cis/trans isomerases by juglone. Biochemistry 1998, 37:5953-5960.
92. Chao SH, Greenleaf AL, Price DH: Juglone, an inhibitor of the peptidyl-prolyl isomerase Pin1, also directly blocks transcription. Nucleic Acids Res 2001, 29:767-773.
93. He J, Lau AG, Yaffe MB, Hall RA: Phosphorylation and cell cycle-dependent regulation of the Na+/H+ exchanger regulatory factor (NHERF-1) by cdc2 kinase. J Biol Chem 2001, 276: 41559-41565.
94. Muto N, Inouye K, Inada A, Nakanishi T, Tan L: Inhibition of cytochrome P-450-linked monooxygenase systems by naphthoquinones. Biochem Biophys Res Commun 1987, 146:487-494.
95. Duhaiman AS: Characterization of zeta-crystallin inhibition by juglone. Biochem Biophys Res Commun 1996, 218:648-652.
96. Munday R, Munday CM: Induction of quinone reductase and glutathione transferase in rat tissues by juglone and plumbagin. Planta Med 2000, 66:399-402.