Phosphorylation of p27^Kip1 Regulates Assembly and Activation of Cyclin D1-Cdk4

REFERENCES

• Bagui, T. K., R. J. Jackson, D. Agrawal, and W. J. Pledger. 2000. Analysis of cyclin D3-cdk4 complexes in fibroblasts expressing and lacking p27kip1 and p21cip1. Mol. Cell. Biol. 20:8748–8757.
   PubMedGoogle Scholar
• Bagui, T. K., S. Mohapatra, E. Haura, and W. J. Pledger. 2003. p27Kip1 and p21Cip1 are not required for the formation of active D cyclin-cdk4 complexes. Mol. Cell. Biol. 23:7285–7290.
   PubMedGoogle Scholar
• Bates, S., D. Parry, L. Bonetta, K. Vousden, C. Dickson, and G. Peters. 1994. Absence of cyclin D/cdk complexes in cells lacking functional retinoblastoma protein. Oncogene 9:1633–1640.
   PubMed Web of Science ®Google Scholar
• Besson, A., M. Gurian-West, X. Chen, K. S. Kelly-Spratt, C. J. Kemp, and J. M. Roberts. 2006. A pathway in quiescent cells that controls p27Kip1 stability, subcellular localization, and tumor suppression. Genes Dev. 20:47–64.
   PubMed Web of Science ®Google Scholar
• Besson, A., M. Gurian-West, A. Schmidt, A. Hall, and J. M. Roberts. 2004. p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 18:862–876.
   PubMed Web of Science ®Google Scholar
• Blagosklonny, M. V., and A. B. Pardee. 2002. The restriction point of the cell cycle. Cell Cycle 1:103–110.
   PubMed Web of Science ®Google Scholar
• Boehm, M., T. Yoshimoto, M. F. Crook, S. Nallamshetty, A. True, G. J. Nabel, and E. G. Nabel. 2002. A growth factor-dependent nuclear kinase phosphorylates p27Kip1 and regulates cell cycle progression. EMBO J. 21:3390–3401.
   PubMed Web of Science ®Google Scholar
• Cariou, S., J. C. Donovan, W. M. Flanagan, A. Milic, N. Bhattacharya, and J. M. Slingerland. 2000. Down-regulation of p21WAF1/CIP1 or p27Kip1 abrogates antiestrogen-mediated cell cycle arrest in human breast cancer cells. Proc. Natl. Acad. Sci. USA 97:9042–9046.
   PubMedGoogle Scholar
• Cheng, M., P. Olivier, J. A. Diehl, M. Fero, M. F. Roussel, J. M. Roberts, and C. J. Sherr. 1999. The p21Cip1 and p27Kip1 CDK ‘inhibitors’ are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J. 18:1571–1583.
   PubMed Web of Science ®Google Scholar
• Chu, I., J. Sun, A. Arnaout, H. Kahn, W. Hanna, S. Narod, P. Sun, C. K. Tan, L. Hengst, and J. Slingerland. 2007. p27 phosphorylation by Src regulates inhibition of cyclin E-Cdk2. Cell 128:281–294.
   PubMed Web of Science ®Google Scholar
• Chu, I. M., L. Hengst, and J. M. Slingerland. 2008. The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy. Nat. Rev. Cancer 8:253–267.
   PubMed Web of Science ®Google Scholar
• Ciarallo, S., V. Subramaniam, W. Hung, J. H. Lee, R. Kotchetkov, C. Sandhu, A. Milic, and J. M. Slingerland. 2002. Altered p27Kip1 phosphorylation, localization, and function in human epithelial cells resistant to transforming growth factor β-mediated G1 arrest. Mol. Cell. Biol. 22:2993–3002.
   PubMedGoogle Scholar
• Cornil, I., D. Theodorescu, S. Man, M. Herlyn, J. Jambrosic, and B. Kerbel. 1991. Fibroblast cell interactions with human melanoma cells affect tumor cell growth as a function of tumor progression. Proc. Natl. Acad. Sci. USA 88:6028–6032.
   PubMedGoogle Scholar
• Deng, X., S. E. Mercer, S. Shah, D. Z. Ewton, and E. Friedman. 2004. The cyclin-dependent kinase inhibitor p27Kip1 is stabilized in G0 by Mirk/dyrk1B kinase. J. Biol. Chem. 279:22498–22504.
   PubMedGoogle Scholar
• Denicourt, C., C. C. Saenz, B. Datnow, X. S. Cui, and S. F. Dowdy. 2007. Relocalized p27KiP1 tumor suppressor functions as a cytoplasmic metastatic oncogene in melanoma. Cancer Res. 67:9238–9243.
   PubMed Web of Science ®Google Scholar
• Diehl, J. A., F. Zindy, and C. J. Sherr. 1997. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev. 11:957–972.
   PubMed Web of Science ®Google Scholar
• Dufner, A., and G. Thomas. 1999. Ribosomal S6 kinase signaling and the control of translation. Exp. Cell Res. 253:100–109.
   PubMed Web of Science ®Google Scholar
• Florenes, V. A., N. Bhattacharya, M. R. Bani, Y. Ben-David, R. S. Kerbel, and J. M. Slingerland. 1996. TGF-beta mediated G1 arrest in a human melanoma cell line lacking p15INK4B: evidence for cooperation between p21Cip1/WAF1 and p27Kip1. Oncogene 13:2447–2457.
   PubMedGoogle Scholar
• Fujita, N., S. Sato, K. Katayama, and T. Tsuruo. 2002. Akt-dependent phosphorylation of p27Kip1 promotes binding to 14-3-3 and cytoplasmic localization. J. Biol. Chem. 277:28706–28713.
   PubMedGoogle Scholar
• Fujita, N., S. Sato, and T. Tsuruo. 2003. Phosphorylation of p27Kip1 at threonine 198 by p90 ribosomal protein S6 kinases promotes its binding to 14-3-3 and cytoplasmic localization. J. Biol. Chem. 278:49254–49260.
   PubMed Web of Science ®Google Scholar
• Grimmler, M., Y. Wang, T. Mund, Z. Cilensek, E. M. Keidel, M. B. Waddell, H. Jakel, M. Kullmann, R. W. Kriwacki, and L. Hengst. 2007. Cdk-inhibitory activity and stability of p27Kip1 are directly regulated by oncogenic tyrosine kinases. Cell 128:269–280.
   PubMed Web of Science ®Google Scholar
• Hara, T., T. Kamura, K. Nakayama, K. Oshikawa, S. Hatakeyama, and K.-I. Nakayama. 2001. Degradation of p27Kip1 at the G0-G1 transition mediated by a Skp2-independent ubiquitination pathway. J. Biol. Chem. 276:48937–48943.
   PubMed Web of Science ®Google Scholar
• Herlyn, M. 1990. Human melanoma: development and progression. Cancer Metastasis Rev. 9:101–112.
   PubMed Web of Science ®Google Scholar
• Hong, F., M. D. Larrea, C. Doughty, D. J. Kwiatkowski, R. Squillace, and J. M. Slingerland. 2008. mTOR-raptor binds and activates SGK1 to regulate p27 phosphorylation. Mol. Cell 30:701–711.
   PubMed Web of Science ®Google Scholar
• Ishida, N., M. Kitagawa, S. Hatakeyama, and K. Nakayama. 2000. Phosphorylation at serine 10, a major phosphorylation site of p27Kip1, increases its protein stability. J. Biol. Chem. 275:25146–25154.
   PubMed Web of Science ®Google Scholar
• James, M., A. Ray, D. Leznova, and S. W. Blain. 2008. Differential modification of p27Kip1 controls its cyclin D-cdk4 inhibitory activity. Mol. Cell. Biol. 28:498–510.
   PubMed Web of Science ®Google Scholar
• Kamura, T., T. Hara, M. Matsumoto, N. Ishida, F. Okumura, S. Hatakeyama, M. Yoshida, K. Nakayama, and K. I. Nakayama. 2004. Cytoplasmic ubiquitin ligase KPC regulates proteolysis of p27Kip1 at G1 phase. Nat. Cell Biol. 6:1229–1235.
   PubMed Web of Science ®Google Scholar
• Kardinal, C., M. Dangers, A. Kardinal, A. Koch, D. T. Brandt, T. Tamura, and K. Welte. 2006. Tyrosine phosphorylation modulates binding preference to cyclin-dependent kinases and subcellular localization of p27Kip1 in the acute promyelocytic leukemia cell line NB4. Blood 107:1133–1140.
   PubMedGoogle Scholar
• Koff, A., M. Ohtsuki, K. Polyak, J. M. Roberts, and J. Massague. 1993. Negative regulation of G1 in mammalian cells: inhibition of cyclin E-dependent kinase by TGF-beta. Science 260:536–539.
   PubMed Web of Science ®Google Scholar
• Kossatz, U., J. Vervoorts, I. Nickeleit, H. A. Sundberg, J. S. C. Arthur, M. P. Manns, and N. P. Malek. 2006. C-terminal phosphorylation controls the stability and function of p27kip1. EMBO J. 25:5159–5170.
   PubMedGoogle Scholar
• Kotake, Y., K. Nakayama, N. Ishida, and K. I. Nakayama. 2005. Role of serine 10 phosphorylation in p27 stabilization revealed by analysis of p27 knock-in mice harboring a serine 10 mutation. J. Biol. Chem. 280:1095–1102.
   PubMed Web of Science ®Google Scholar
• LaBaer, J., M. D. Garrett, L. F. Stevenson, J. M. Slingerland, C. Sandhu, H. S. Chou, A. Fattaey, and E. Harlow. 1997. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 11:847–862.
   PubMed Web of Science ®Google Scholar
• Laiho, M., J. A. DeCaprio, J. W. Ludlow, D. M. Livingston, and J. Massague. 1990. Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation. Cell 62:175–185.
   PubMed Web of Science ®Google Scholar
• Lee, S., and D. M. Helfman. 2004. Cytoplasmic p21Cip1 is involved in Ras-induced inhibition of the ROCK/LIMK/cofilin pathway. J. Biol. Chem. 279:1885–1891.
   PubMed Web of Science ®Google Scholar
• Li, Y., D. Dowbenko, and L. A. Lasky. 2002. AKT/PKB phosphorylation of p21Cip/WAF1 enhances protein stability of p21Cip/WAF1 and promotes cell survival. J. Biol. Chem. 277:11352–11361.
   PubMed Web of Science ®Google Scholar
• Liang, J., S. H. Shao, Z. Xu, B. Hennessy, Z. Ding, M. Larrea, S. Kondo, D. J. Dumont, J. U. Gutterman, C. L. Walker, J. M. Slingerland, and G. B. Mills. 2007. The energy sensing LKB1-AMPK pathway regulates p27kip1 phosphorylation mediating the decision to enter autophagy or apoptosis. Nat. Cell Biol. 9:218–224.
   PubMed Web of Science ®Google Scholar
• Liang, J., and J. M. Slingerland. 2003. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2:339–345.
   PubMed Web of Science ®Google Scholar
• Liang, J., J. Zubovitz, T. Petrocelli, R. Kotchetkov, M. K. Connor, K. Han, J. H. Lee, S. Ciarallo, C. Catzavelos, R. Beniston, E. Franssen, and J. M. Slingerland. 2002. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat. Med. 8:1153–1160.
   PubMed Web of Science ®Google Scholar
• Malumbres, M., and M. Barbacid. 2005. Mammalian cyclin-dependent kinases. Trends Biochem. Sci. 30:630–641.
   PubMed Web of Science ®Google Scholar
• Matsushime, H., D. E. Quelle, S. A. Shurtleff, M. Shibuya, C. J. Sherr, and J. Y. Kato. 1994. D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell. Biol. 14:2066–2076.
   PubMed Web of Science ®Google Scholar
• McAllister, S. S., M. Becker-Hapak, G. Pintucci, M. Pagano, and S. F. Dowdy. 2003. Novel p27kip1 C-terminal scatter domain mediates Rac-dependent cell migration independent of cell cycle arrest functions. Mol. Cell. Biol. 23:216–228.
   PubMed Web of Science ®Google Scholar
• Motti, M. L., C. De Marco, D. Califano, A. Fusco, and G. Viglietto. 2004. Akt-dependent T198 phosphorylation of cyclin-dependent kinase inhibitor p27kip1 in breast cancer. Cell Cycle 3:1074–1080.
   PubMedGoogle Scholar
• Muise-Helmericks, R. C., H. L. Grimes, A. Bellacosa, S. E. Malstrom, P. N. Tsichlis, and N. Rosen. 1998. Cyclin D expression is controlled post-transcriptionally via a phosphatidylinositol 3-kinase/Akt-dependent pathway. J. Biol. Chem. 273:29864–29872.
   PubMed Web of Science ®Google Scholar
• Nacusi, L. P., and R. J. Sheaff. 2006. Akt1 sequentially phosphorylates p27kip1 within a conserved but non-canonical region. Cell Div. 1:11.
   PubMedGoogle Scholar
• Nagahara, H., A. M. Vocero-Akbani, E. L. Synder, A. Ho, D. G. Latham, N. A. Lissy, M. Becker-Hapak, S. A. Ezhevsky, and S. F. Dowdy. 1998. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat. Med. 4:1449–1452.
   PubMed Web of Science ®Google Scholar
• Parry, D., S. Bates, D. J. Mann, and G. Peters. 1995. Lack of cyclin D-Cdk complexes in Rb-negative cells correlates with high levels of p16INK4/MTS1 tumour suppressor gene product. EMBO J. 14:503–511.
   PubMed Web of Science ®Google Scholar
• Polyak, K., J. Y. Kato, M. J. Solomon, C. J. Sherr, J. Massague, J. M. Roberts, and A. Koff. 1994. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev. 8:9–22.
   PubMed Web of Science ®Google Scholar
• Polyak, K., M. H. Lee, H. Erdjument-Bromage, A. Koff, J. Roberts, P. Tempst, and J. Massagué. 1994. Cloning of p27KIP1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78:59–66.
   PubMed Web of Science ®Google Scholar
• Rodier, G., A. Montagnoli, L. Di Marcotullio, P. Coulombe, G. F. Draetta, M. Pagano, and S. Meloche. 2001. p27 cytoplasmic localization is regulated by phosphorylation on Ser10 and is not a prerequisite for its proteolysis. EMBO J. 20:6672–6682.
   PubMed Web of Science ®Google Scholar
• Rössig, L., A. S. Jadidi, C. Urbich, C. Badorff, A. M. Zeiher, and S. Dimmeler. 2001. Akt-dependent phosphorylation of p21Cip1 regulates PCNA binding and proliferation of endothelial cells. Mol. Cell. Biol. 21:5644–5657.
   PubMed Web of Science ®Google Scholar
• Sandhu, C., J. Garbe, N. Bhattacharya, J. Daksis, C. H. Pan, P. Yaswen, J. Koh, J. M. Slingerland, and M. R. Stampfer. 1997. Transforming growth factor β stabilizes p15INK4B protein, increases p15INK4B-cdk4 complexes, and inhibits cyclin D1-cdk4 association in human mammary epithelial cells. Mol. Cell. Biol. 17:2458–2467.
   PubMedGoogle Scholar
• Sheaff, R. J., M. Groudine, M. Gordon, J. M. Roberts, and B. E. Clurman. 1997. Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev. 11:1464–1478.
   PubMed Web of Science ®Google Scholar
• Sherr, C. J. 2000. The Pezcoller Lecture: cancer cell cycles revisited. Cancer Res. 60:3689–3695.
   PubMed Web of Science ®Google Scholar
• Sherr, C. J., and J. M. Roberts. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1501–1512.
   PubMed Web of Science ®Google Scholar
• Shin, I., F. M. Yakes, F. Rojo, N. Y. Shin, A. V. Bakin, J. Baselga, and C. L. Arteaga. 2002. PKB/Akt mediates cell-cycle progression by phosphorylation of p27Kip1 at threonine 157 and modulation of its cellular localization. Nat. Med. 8:1145–1152.
   PubMed Web of Science ®Google Scholar
• Slingerland, J., and M. Pagano. 2000. Regulation of the cdk inhibitor p27 and its deregulation in cancer. J. Cell. Physiol. 183:10–17.
   PubMed Web of Science ®Google Scholar
• Slingerland, J. M., L. Hengst, C. H. Pan, D. Alexander, M. R. Stampfer, and S. I. Reed. 1994. A novel inhibitor of cyclin-Cdk activity detected in transforming growth factor β-arrested epithelial cells. Mol. Cell. Biol. 14:3683–3694.
   PubMed Web of Science ®Google Scholar
• Stampfer, M. 1985. Isolation and growth of human mammary epithelial cells. J. Tissue Cult. Methods 9:107–115.
   Google Scholar
• Viglietto, G., M. L. Motti, P. Bruni, R. M. Melillo, A. D'Alessio, D. Califano, F. Vinci, G. Chiappetta, P. Tsichlis, A. Bellacosa, A. Fusco, and M. Santoro. 2002. Cytoplasmic relocalization and inhibition of the cyclin-dependent kinase inhibitor p27Kip1 by PKB/Akt-mediated phosphorylation in breast cancer. Nat. Med. 8:1136–1144.
   PubMed Web of Science ®Google Scholar
• Vlach, J., S. Hennecke, and B. Amati. 1997. Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. EMBO J. 16:5334–5344.
   PubMed Web of Science ®Google Scholar
• Wu, F. Y., S. E. Wang, M. E. Sanders, I. Shin, F. Rojo, J. Baselga, and C. L. Arteaga. 2006. Reduction of cytosolic p27Kip1 inhibits cancer cell motility, survival, and tumorigenicity. Cancer Res. 66:2162–2172.
   PubMed Web of Science ®Google Scholar
• Yakes, F. M., W. Chinratanalab, C. A. Ritter, W. King, S. Seelig, and C. L. Arteaga. 2002. Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt Is required for antibody-mediated effects on p27, cyclin D1, and antitumor action. Cancer Res. 62:4132–4141.
   PubMed Web of Science ®Google Scholar
• Zhang, H., G. Hannon, and D. Beach. 1994. p21-containing cyclin kinases exist in both active and inactive states. Genes Dev. 8:1750–1758.
   PubMed Web of Science ®Google Scholar
• Zhou, B. P., Y. Liao, W. Xia, B. Spohn, M. H. Lee, and M. C. Hung. 2001. Cytoplasmic localization of p21Cip1/WAF1 by Akt-induced phosphorylation in HER-2/neu-overexpressing cells. Nat. Cell Biol. 3:245–252.
   PubMed Web of Science ®Google Scholar