Reduction of cytosolic p27Kip1 inhibits cancer cell motility, survival, and tumorigenicity

Cancer Research

Volumn 66, Issue 4, 2006, Pages 2162-2172

  Wu, Frederick Y ^a   Wang, Shizhen Emily ^a   Sanders, Melinda E ^a   Shin, Incheol ^a,b   Rojo, Federico ^c   Baselga, Jose ^c   Arteaga, Carlos L ^a,d  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b Hanyang University   (South Korea)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; PROTEIN KINASE B; PROTEIN P27; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CARCINOMA; CANCER INVASION; CARCINOGENICITY; CELL CYCLE; CELL MOTILITY; CELL STRAIN MCF 7; CELL SURVIVAL; CONTROLLED STUDY; CYTOSOL; ENZYME METABOLISM; ENZYME STABILITY; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; TUMOR XENOGRAFT;

AMINO ACID SEQUENCE; ANIMALS; BREAST NEOPLASMS; CELL ADHESION; CELL MOVEMENT; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYTOSOL; DOWN-REGULATION; GLIOMA; HUMANS; MICE; MICE, NUDE; MOLECULAR SEQUENCE DATA; NEOPLASM TRANSPLANTATION; PROTO-ONCOGENE PROTEINS C-AKT; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS;

EID: 33644509197     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-3304     Document Type: Article

References (55)

1. 1-phase progression. Genes Dev 1999;13:1501-12.
2. 1 cell-cycle control and cancer. Nature 2004;432:298-306.
3. Philipp-Staheli J, Payne SR, Kemp CJ. p27(Kip1): regulation and function of a haploinsufficient tumor suppressor and its misregulation in cancer. Exp Cell Res 2001;264:148-68.
4. Fero ML, Randel E, Gurley KE, Roberts JM, Kemp CJ. The murine gene p27Kip1 is haplo-insufficient for tumour suppression. Nature 1998;396:177-80.
5. Alkarain A, Jordan R, Slingerland J. p27 deregulation in breast cancer: prognostic significance and implications for therapy. J Mammary Gland Biol Neoplasia 2004;9:67-80.
6. Viglietto G, Motti ML, Fusco A. Understanding p27(kip1) deregulation in cancer: down-regulation or mislocalization. Cell Cycle 2002;1:394-400.
7. Bloom J, Pagano M. Deregulated degradation of the cdk inhibitor p27 and malignant transformation. Semin Cancer Biol 2003;13:41-7.
8. Boehm M, Yoshimoto T, Crook MF, et al. A growth factor-dependent nuclear kinase phosphorylates p27(Kip1) and regulates cell cycle progression. EMBO J 2002;21:3390-401.
9. 1 arrest. Nat Med 2002;8:1153-60.
10. Viglietto G, Motti ML, Bruni P, et al. Cytoplasmic relocalization and inhibition of the cyclin-dependent kinase inhibitor p27(Kip1) by PKB/Akt-mediated phosphorylation in breast cancer. Nat Med 2002;8:1136-44.
11. Shin I, Yakes FM, Rojo F, et al. PKB/Akt mediates cell-cycle progression by phosphorylation of p27(Kip1) at threonine 157 and modulation of its cellular localization. Nat Med 2002;8:1145-52.
12. Cheng M, Olivier P, Diehl JA, et al. The p21(Cip1) and p27(Kip1) CDK "inhibitors" are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J 1999;18:1571-83.
13. Muraoka RS, Lenferink AE, Simpson J, et al. Cyclin-dependent kinase inhibitor p27(Kip1) is required for mouse mammary gland morphogenesis and function. J Cell Biol 2001;153:917-32.
14. Nagahara H, Vocero-Akbani AM, Snyder EL, et al. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat Med 1998;4:1449-52.
15. McAllister SS, Becker-Hapak M, Pintucci G, Pagano M, Dowdy SF. Novel p27(kip1) C-terminal scatter domain mediates Rac-dependent cell migration independent of cell cycle arrest functions. Mol Cell Biol 2003;23:216-28.
16. Besson A, Gurian-West M, Schmidt A, Hall A, Roberts JM. p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev 2004;18:862-76.
17. Muraoka RS, Lenferink AE, Law B, et al. ErbB2/Neu-induced, cyclin D1-dependent transformation is accelerated in p27-haploinsufficient mammary epithelial cells but impaired in p27-null cells. Mol Cell Biol 2002;22:2204-19.
18. Grignani F, Kinsella T, Mencarelli A, et al. High-efficiency gene transfer and selection of human hematopoietic progenitor cells with a hybrid EBV/retroviral vector expressing the green fluorescence protein. Cancer Res 1998;58:14-9.
19. Oliff A, McKinney MD, Agranovsky O. Contribution of the gag and pol sequences to the leukemogenicity of Friend murine leukemia virus. J Virol 1985;54:864-8.
20. Brummelkamp TR, Bernards R, Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002;296:550-3.
21. Wang SE, Wu FY, Shin I, Qu S, Arteaga CL. Transforming growth factor {β} (TGF-{β})-Smad target gene protein tyrosine phosphatase receptor type κ is required for TGF-{β} function. Mol Cell Biol 2005;25:4703-15.
22. Ueda Y, Wang S, Dumont N, Yi JY, Koh Y, Arteaga CL. Overexpression of HER2 (erbB2) in human breast epithelial cells unmasks transforming growth factor β-induced cell motility. J Biol Chem 2004;279:24505-13.
23. Bakin AV, Rinehart C, Tomlinson AK, Arteaga CL. p38 mitogen-activated protein kinase is required for TGFβ-mediated fibroblastic transdifferentiation and cell migration. J Cell Sci 2002;115:3193-206.
24. Dumont N, Bakin AV, Arteaga CL. Autocrine transforming growth factor-β signaling mediates Smad-independent motility in human cancer cells. J Biol Chem 2003;278:3275-85.
25. Shin I, Bakin AV, Rodeck U, Brunet A, Arteaga CL. Transforming growth factor β enhances epithelial cell survival via Akt-dependent regulation of FKHRL1. Mol Biol Cell 2001;12:3328-39.
26. Connor MK, Kotchetkov R, Cariou S, et al. CRM1/Ran-mediated nuclear export of p27(Kip1) involves a nuclear export signal and links p27 export and proteolysis. Mol Biol Cell 2003;14:201-13.
27. Ishida N, Kitagawa M, Hatakeyama S, Nakayama K. Phosphorylation at serine 10, a major phosphorylation site of p27(Kip1), increases its protein stability. J Biol Chem 2000;275:25146-54.
28. 1 and prevents nuclear reentry. J Biol Chem 2005;280:6055-63.
29. Pore N, Liu S, Haas-Kogan DA, O'Rourke DM, Maity A. PTEN mutation and epidermal growth factor receptor activation regulate vascular endothelial growth factor (VEGF) mRNA expression in human glioblastoma cells by transactivating the proximal VEGF promoter. Cancer Res 2003;63:236-41.
30. Sekimoto T, Fukumoto M, Yoneda Y. 14-3-3 suppresses the nuclear localization of threonine 157-phosphorylated p27(Kip1). EMBO J 2004;23:1934-42.
31. Fujita N, Sato S, Katayama K, Tsuruo T. Akt-dependent phosphorylation of p27Kip1 promotes binding to 14-3-3 and cytoplasmic localization. J Biol Chem 2002;277:28706-13.
32. Motti ML, De Marco C, Califano D, Fusco A, Viglietto G. Akt-dependent T198 phosphorylation of cyclin-dependent kinase inhibitor p27kip1 in breast cancer. Cell Cycle 2004;3:1074-80.
33. Gao H, Ouyang X, Banach-Petrosky W, et al. A critical role for p27kip1 gene dosage in a mouse model of prostate carcinogenesis. Proc Natl Acad Sci U S A 2004;101:17204-9.
34. Cheng M, Sexl V, Sherr CJ, Roussel MF. Assembly of cyclin D-dependent kinase and titration of p27Kip1 regulated by mitogen-activated protein kinase kinase (MEK1). Proc Natl Acad Sci U S A 1998;95:1091-6.
35. Davison EA, Lee CS, Naylor MJ, et al. The cyclin-dependent kinase inhibitor p27 (Kip1) regulates both DNA synthesis and apoptosis in mammary epithelium but is not required for its functional development during pregnancy. Mol Endocrinol 2003;17:2436-47.
36. Orend G, Hunter T, Ruoslahti E. Cytoplasmic displacement of cyclin E-cdk2 inhibitors p21Cip1 and p27Kip1 in anchorage-independent cells. Oncogene 1998;16:2575-83.
37. Singh SP, Lipman J, Goldman H, et al. Loss or altered subcellular localization of p27 in Barrett's associated adenocarcinoma. Cancer Res 1998;58:1730-5.
38. Ciaparrone M, Yamamoto H, Yao Y, et al. Localization and expression of p27KIP1 in multistage colorectal carcinogenesis. Cancer Res 1998;58:114-22.
39. Soucek T, Yeung RS, Hengstschlager M. Inactivation of the cyclin-dependent kinase inhibitor p27 upon loss of the tuberous sclerosis complex gene-2. Proc Natl Acad Sci U S A 1998;95:15653-8.
40. Baldassarre G, Belletti B, Bruni P, et al. Overexpressed cyclin D3 contributes to retaining the growth inhibitor p27 in the cytoplasm of thyroid tumor cells. J Clin Invest 1999;104:865-74.
41. Hiromura K, Pippin JW, Fero ML, Roberts JM, Shankland SJ. Modulation of apoptosis by the cyclin-dependent kinase inhibitor p27(Kip1). J Clin Invest 1999;103:597-604.
42. Eymin B, Haugg M, Droin N, Sordet O, Dimanche-Boitrel MT, Solary E. p27Kip1 induces drug resistance by preventing apoptosis upstream of cytochrome c release and procaspase-3 activation in leukemic cells. Oncogene 1999;18:1411-8.
43. Masuda A, Osada H, Yatabe Y, et al. Protective function of p27(KIP1) against apoptosis in small cell lung cancer cells in unfavorable microenvironments. Am J Pathol 2001;158:87-96.
44. Ophascharoensuk V, Fero ML, Hughes J, Roberts JM, Shankland SJ. The cyclin-dependent kinase inhibitor p27Kip1 safeguards against inflammatory injury. Nat Med 1998;4:575-80.
45. Lee SH, McCormick F. Downregulation of Skp2 and p27/Kip1 synergistically induces apoptosis in T98G glioblastoma cells. J Mol Med 2005;83:296-307.
46. Kouvaraki M, Gorgoulis VG, Rassidakis GZ, et al. High expression levels of p27 correlate with lymph node status in a subset of advanced invasive breast carcinomas: relation to E-cadherin alterations, proliferative activity, and ploidy of the tumors. Cancer 2002;94:2454-65.
47. Barbareschi M, van Tinteren H, Mauri FA, et al. p27(kip1) expression in breast carcinomas: an immunohistochemical study on 512 patients with long-term follow-up. Int J Cancer 2000;89:236-41.
48. Katayose Y, Kim M, Rakkar AN, Li Z, Cowan KH, Seth P. Promoting apoptosis: a novel activity associated with the cyclin- dependent kinase inhibitor p27. Cancer Res 1997;57:5441-5.
49. Craig C, Wersto R, Kim M, et al. A recombinant adenovirus expressing p27Kip1 induces cell cycle arrest and loss of cyclin-Cdk activity in human breast cancer cells. Oncogene 1997;14:2283-9.
50. Zhang Q, Tian L, Mansouri A, Korapati AL, Johnson TJ, Claret FX. Inducible expression of a degradation-resistant form of p27Kip1 causes growth arrest and apoptosis in breast cancer cells. FEBS Lett 2005;579:3932-40.
51. Turturro F, Arnold MD, Frist AY, Seth P. Effects of adenovirus-mediated expression of p27Kip1, p21Waf1 and p16INK4A in cell lines derived from t(2;5) anaplastic large cell lymphoma and Hodgkin's disease. Leuk Lymphoma 2002;43:1323-8.
52. Katner AL, Gootam P, Hoang QB, Gnarra JR, Rayford W. A recombinant adenovirus expressing p7(Kip1) induces cell cycle arrest and apoptosis in human 786-0 renal carcinoma cells. J Urol 2002;168:766-73.
53. Katner AL, Hoang QB, Gootam P, et al. Induction of cell cycle arrest and apoptosis in human prostate carcinoma cells by a recombinant adenovirus expressing p27(Kip1). Prostate 2002;53:77-87.
54. Naruse I, Hoshino H, Dobashi K, Minato K, Saito R, Mori M. Over-expression of p27kip1 induces growth arrest and apoptosis mediated by changes of pRb expression in lung cancer cell lines. Int J Cancer 2000;88:377-83.
55. Tetsu O, McCormick F. Proliferation of cancer cells despite CDK2 inhibition. Cancer Cell 2003;3:233-45.