Assembly, activation, and substrate specificity of cyclin D1/Cdk2 complexes

Biochemistry

Volumn 52, Issue 20, 2013, Pages 3489-3501

  Jahn, Stephan C ^a,b   Law, Mary E ^a,b   Corsino, Patrick E ^a,b   Rowe, Thomas C ^a,b   Davis, Bradley J ^a,b   Law, Brian K ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE COMPLEXES; CELLULAR ACTIVITIES; CHEMOTHERAPEUTIC AGENTS; CHROMOSOMAL INSTABILITY; MUTANT PROTEINS; PROTEIN-ASSOCIATED SPLICING FACTORS; SCAFFOLDING PROTEINS; SUBSTRATE SPECIFICITY;

DISEASES; ENZYMES; OLIGOMERS; PHOSPHORYLATION; PROTEINS; SUBSTRATES;

SCAFFOLDS (BIOLOGY);

CYCLIN D1; CYCLIN DEPENDENT KINASE 2; CYCLIN E; HYBRID PROTEIN; MUTANT PROTEIN; NUCLEOPHOSMIN; POLYPYRIMIDINE TRACT BINDING PROTEIN; PROTEIN P21; RETINOBLASTOMA PROTEIN; UVOMORULIN;

ARTICLE; CENTROSOME; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

BINDING SITES; CELLS, CULTURED; CYCLIN D1; CYCLIN-DEPENDENT KINASE 2; HCT116 CELLS; HUMANS; MULTIPROTEIN COMPLEXES; SUBSTRATE SPECIFICITY;

EID: 84878254981     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400047u     Document Type: Article

References (72)

1. Hannon, G. J. and Beach, D. (1994) p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest Nature 371, 257-261
2. Guan, K. L., Jenkins, C. W., Li, Y., Nichols, M. A., Wu, X., O'Keefe, C. L., Matera, A. G., and Xiong, Y. (1994) Growth suppression by p18, a p16INK4/MTS1- and p14INK4B/MTS2-related CDK6 inhibitor, correlates with wild-type pRb function Genes Dev. 8, 2939-2952
3. Serrano, M., Hannon, G. J., and Beach, D. (1993) A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4 Nature 366, 704-707
4. Okuda, T., Hirai, H., Valentine, V. A., Shurtleff, S. A., Kidd, V. J., Lahti, J. M., Sherr, C. J., and Downing, J. R. (1995) Molecular cloning, expression pattern, and chromosomal localization of human CDKN2D/INK4d, an inhibitor of cyclin D-dependent kinases Genomics 29, 623-630
5. Ewen, M. E., Sluss, H. K., Sherr, C. J., Matsushime, H., Kato, J., and Livingston, D. M. (1993) Functional interactions of the retinoblastoma protein with mammalian D-type cyclins Cell 73, 487-497
6. Higashi, H., Suzuki-Takahashi, I., Saitoh, S., Segawa, K., Taya, Y., Okuyama, A., Nishimura, S., and Kitagawa, M. (1996) Cyclin-dependent kinase-2 (Cdk2) forms an inactive complex with cyclin D1 since Cdk2 associated with cyclin D1 is not phosphorylated by Cdk7-cyclin-H Eur. J. Biochem. 237, 460-467
7. Morisaki, H., Ando, A., Nagata, Y., Pereira-Smith, O., Smith, J. R., Ikeda, K., and Nakanishi, M. (1999) Complex mechanisms underlying impaired activation of Cdk4 and Cdk2 in replicative senescence: roles of p16, p21, and cyclin D1 Exp. Cell Res. 253, 503-510
8. Chytil, A., Waltner-Law, M., West, R., Friedman, D., Aakre, M., Barker, D., and Law, B. (2004) Construction of a cyclin D1-Cdk2 fusion protein to model the biological functions of cyclin D1-Cdk2 complexes J. Biol. Chem. 279, 47688-47698
9. Bienvenu, F., Jirawatnotai, S., Elias, J. E., Meyer, C. A., Mizeracka, K., Marson, A., Frampton, G. M., Cole, M. F., Odom, D. T., Odajima, J., Geng, Y., Zagozdzon, A., Jecrois, M., Young, R. A., Liu, X. S., Cepko, C. L., Gygi, S. P., and Sicinski, P. (2010) Transcriptional role of cyclin D1 in development revealed by a genetic-proteomic screen Nature 463, 374-378
10. Jirawatnotai, S., Hu, Y., Michowski, W., Elias, J. E., Becks, L., Bienvenu, F., Zagozdzon, A., Goswami, T., Wang, Y. E., Clark, A. B., Kunkel, T. A., van Harn, T., Xia, B., Correll, M., Quackenbush, J., Livingston, D. M., Gygi, S. P., and Sicinski, P. (2011) A function for cyclin D1 in DNA repair uncovered by protein interactome analyses in human cancers Nature 474, 230-234
11. Bowe, D. B., Kenney, N. J., Adereth, Y., and Maroulakou, I. G. (2002) Suppression of Neu-induced mammary tumor growth in cyclin D1 deficient mice is compensated for by cyclin E Oncogene 21, 291-298
12. Reddy, H. K., Mettus, R. V., Rane, S. G., Grana, X., Litvin, J., and Reddy, E. P. (2005) Cyclin-dependent kinase 4 expression is essential for neu-induced breast tumorigenesis Cancer Res. 65, 10174-10178
13. Ray, D., Terao, Y., Christov, K., Kaldis, P., and Kiyokawa, H. (2011) Cdk2-null mice are resistant to ErbB-2-induced mammary tumorigenesis Neoplasia 13, 439-444
14. Sweeney, K. J., Swarbrick, A., Sutherland, R. L., and Musgrove, E. A. (1998) Lack of relationship between CDK activity and G1 cyclin expression in breast cancer cells Oncogene 16, 2865-2878
15. Junk, D. J., Cipriano, R., Stampfer, M., and Jackson, M. W. (2013) Constitutive CCND1/CDK2 Activity Substitutes for p53 Loss, or MYC or Oncogenic RAS Expression in the Transformation of Human Mammary Epithelial Cells PLoS One 8, e53776
16. Law, M., Forrester, E., Chytil, A., Corsino, P., Green, G., Davis, B., Rowe, T., and Law, B. (2006) Rapamycin disrupts cyclin/cyclin-dependent kinase/p21/proliferating cell nuclear antigen complexes and cyclin D1 reverses rapamycin action by stabilizing these complexes Cancer Res. 66, 1070-1080
17. Corsino, P., Davis, B., Law, M., Chytil, A., Forrester, E., Norgaard, P., Teoh, N., and Law, B. (2007) Tumors initiated by constitutive Cdk2 activation exhibit transforming growth factor beta resistance and acquire paracrine mitogenic stimulation during progression Cancer Res. 67, 3135-3144
18. Jahn, S. C., Corsino, P. E., Davis, B. J., Law, M. E., Norgaard, P., and Law, B. K. (2013) Constitutive Cdk2 activity promotes aneuploidy while altering the spindle assembly and tetraploidy checkpoints J. Cell Sci. 126, 1207-1217
19. Corsino, P. E., Davis, B. J., Norgaard, P. H., Parker, N. N., Law, M., Dunn, W., and Law, B. K. (2008) Mammary tumors initiated by constitutive Cdk2 activation contain an invasive basal-like component Neoplasia 10, 1240-1252
20. Canavese, M., Santo, L., and Raje, N. (2012) Cyclin dependent kinases in cancer: Potential for therapeutic intervention Cancer Biol Ther 13, 451-457
21. Azimzadeh, J. and Marshall, W. F. (2010) Building the centriole Curr. Biol. 20, R816-825
22. Okuda, M., Horn, H. F., Tarapore, P., Tokuyama, Y., Smulian, A. G., Chan, P. K., Knudsen, E. S., Hofmann, I. A., Snyder, J. D., Bove, K. E., and Fukasawa, K. (2000) Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication Cell 103, 127-140
23. Garcia-Higuera, I., Manchado, E., Dubus, P., Canamero, M., Mendez, J., Moreno, S., and Malumbres, M. (2008) Genomic stability and tumour suppression by the APC/C cofactor Cdh1 Nat. Cell Biol. 10, 802-811
24. Lindon, C. (2008) Control of mitotic exit and cytokinesis by the APC/C Biochem. Soc. Trans. 36, 405-410
25. Shav-Tal, Y. and Zipori, D. (2002) PSF and p54(nrb)/NonO - multi-functional nuclear proteins FEBS Lett. 531, 109-114
26. Patton, J. G., Porro, E. B., Galceran, J., Tempst, P., and Nadal-Ginard, B. (1993) Cloning and characterization of PSF, a novel pre-mRNA splicing factor Genes Dev. 7, 393-406
27. Rosonina, E., Ip, J. Y., Calarco, J. A., Bakowski, M. A., Emili, A., McCracken, S., Tucker, P., Ingles, C. J., and Blencowe, B. J. (2005) Role for PSF in mediating transcriptional activator-dependent stimulation of pre-mRNA processing in vivo Mol. Cell. Biol. 25, 6734-6746
28. Gozani, O., Patton, J. G., and Reed, R. (1994) A novel set of spliceosome-associated proteins and the essential splicing factor PSF bind stably to pre-mRNA prior to catalytic step II of the splicing reaction EMBO J. 13, 3356-3367
29. Liang, S. and Lutz, C. S. (2006) p54nrb is a component of the snRNP-free U1A (SF-A) complex that promotes pre-mRNA cleavage during polyadenylation RNA 12, 111-121
30. Emili, A., Shales, M., McCracken, S., Xie, W., Tucker, P. W., Kobayashi, R., Blencowe, B. J., and Ingles, C. J. (2002) Splicing and transcription- associated proteins PSF and p54nrb/nonO bind to the RNA polymerase II CTD RNA 8, 1102-1111
31. Kaneko, S., Rozenblatt-Rosen, O., Meyerson, M., and Manley, J. L. (2007) The multifunctional protein p54nrb/PSF recruits the exonuclease XRN2 to facilitate pre-mRNA 3′ processing and transcription termination Genes Dev. 21, 1779-1789
32. Bladen, C. L., Udayakumar, D., Takeda, Y., and Dynan, W. S. (2005) Identification of the polypyrimidine tract binding protein-associated splicing factor.p54(nrb) complex as a candidate DNA double-strand break rejoining factor J. Biol. Chem. 280, 5205-5210
33. Ha, K., Takeda, Y., and Dynan, W. S. (2011) Sequences in PSF/SFPQ mediate radioresistance and recruitment of PSF/SFPQ-containing complexes to DNA damage sites in human cells DNA Repair (Amst) 10, 252-259
34. Lukong, K. E., Huot, M. E., and Richard, S. (2009) BRK phosphorylates PSF promoting its cytoplasmic localization and cell cycle arrest Cell. Signal. 21, 1415-1422
35. Shav-Tal, Y., Cohen, M., Lapter, S., Dye, B., Patton, J. G., Vandekerckhove, J., and Zipori, D. (2001) Nuclear relocalization of the pre-mRNA splicing factor PSF during apoptosis involves hyperphosphorylation, masking of antigenic epitopes, and changes in protein interactions Mol. Biol. Cell 12, 2328-2340
36. Heyd, F. and Lynch, K. W. (2010) Phosphorylation-dependent regulation of PSF by GSK3 controls CD45 alternative splicing Mol. Cell 40, 126-137
37. Law, B. K., Chytil, A., Dumont, N., Hamilton, E. G., Waltner-Law, M. E., Aakre, M. E., Covington, C., and Moses, H. L. (2002) Rapamycin potentiates transforming growth factor beta-induced growth arrest in nontransformed, oncogene-transformed, and human cancer cells Mol. Cell. Biol. 22, 8184-8198
38. Cozar-Castellano, I., Harb, G., Selk, K., Takane, K., Vasavada, R., Sicari, B., Law, B., Zhang, P., Scott, D. K., Fiaschi-Taesch, N., and Stewart, A. F. (2008) Lessons from the first comprehensive molecular characterization of cell cycle control in rodent insulinoma cell lines Diabetes 57, 3056-3068
39. Nakanishi, M., Robetorye, R. S., Pereira-Smith, O. M., and Smith, J. R. (1995) The C-terminal region of p21SDI1/WAF1/CIP1 is involved in proliferating cell nuclear antigen binding but does not appear to be required for growth inhibition J. Biol. Chem. 270, 17060-17063
40. Pfleger, C. M., Lee, E., and Kirschner, M. W. (2001) Substrate recognition by the Cdc20 and Cdh1 components of the anaphase-promoting complex Genes Dev. 15, 2396-2407
41. Wang, W., Budhu, A., Forgues, M., and Wang, X. W. (2005) Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication Nat. Cell Biol. 7, 823-830
42. Waldman, T., Kinzler, K. W., and Vogelstein, B. (1995) p21 is necessary for the p53-mediated G1 arrest in human cancer cells Cancer Res. 55, 5187-5190
43. Zhang, H., Hannon, G. J., and Beach, D. (1994) p21-containing cyclin kinases exist in both active and inactive states Genes Dev. 8, 1750-1758
44. Koundrioukoff, S., Jonsson, Z. O., Hasan, S., de Jong, R. N., van der Vliet, P. C., Hottiger, M. O., and Hubscher, U. (2000) A direct interaction between proliferating cell nuclear antigen (PCNA) and Cdk2 targets PCNA-interacting proteins for phosphorylation J. Biol. Chem. 275, 22882-22887
45. Gulbis, J. M., Kelman, Z., Hurwitz, J., O'Donnell, M., and Kuriyan, J. (1996) Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA Cell 87, 297-306
46. Li, R., Hannon, G. J., Beach, D., and Stillman, B. (1996) Subcellular distribution of p21 and PCNA in normal and repair-deficient cells following DNA damage Curr. Biol. 6, 189-199
47. Chapados, B. R., Hosfield, D. J., Han, S., Qiu, J., Yelent, B., Shen, B., and Tainer, J. A. (2004) Structural basis for FEN-1 substrate specificity and PCNA-mediated activation in DNA replication and repair Cell 116, 39-50
48. Levin, D. S., McKenna, A. E., Motycka, T. A., Matsumoto, Y., and Tomkinson, A. E. (2000) Interaction between PCNA and DNA ligase I is critical for joining of Okazaki fragments and long-patch base-excision repair Curr. Biol. 10, 919-922
49. Koundrioukoff, S., Jonsson, Z. O., Hasan, S., de Jong, R. N., van der Vliet, P. C., Hottiger, M. O., and Hubscher, U. (2000) A direct interaction between proliferating cell nuclear antigen (PCNA) and Cdk2 targets PCNA-interacting proteins for phosphorylation J. Biol. Chem. 275, 22882-22887
50. Tarapore, P., Shinmura, K., Suzuki, H., Tokuyama, Y., Kim, S. H., Mayeda, A., and Fukasawa, K. (2006) Thr199 phosphorylation targets nucleophosmin to nuclear speckles and represses pre-mRNA processing FEBS Lett. 580, 399-409
51. Cuomo, M. E., Knebel, A., Morrice, N., Paterson, H., Cohen, P., and Mittnacht, S. (2008) p53-Driven apoptosis limits centrosome amplification and genomic instability downstream of NPM1 phosphorylation Nat. Cell Biol. 10, 723-730
52. Buckley, M. F., Sweeney, K. J., Hamilton, J. A., Sini, R. L., Manning, D. L., Nicholson, R. I., deFazio, A., Watts, C. K., Musgrove, E. A., and Sutherland, R. L. (1993) Expression and amplification of cyclin genes in human breast cancer Oncogene 8, 2127-2133
53. Loden, M., Stighall, M., Nielsen, N. H., Roos, G., Emdin, S. O., Ostlund, H., and Landberg, G. (2002) The cyclin D1 high and cyclin E high subgroups of breast cancer: separate pathways in tumorogenesis based on pattern of genetic aberrations and inactivation of the pRb node Oncogene 21, 4680-4690
54. Lindahl, T., Landberg, G., Ahlgren, J., Nordgren, H., Norberg, T., Klaar, S., Holmberg, L., and Bergh, J. (2004) Overexpression of cyclin E protein is associated with specific mutation types in the p53 gene and poor survival in human breast cancer Carcinogenesis 25, 375-380
55. Coletta, R. D., Christensen, K., Reichenberger, K. J., Lamb, J., Micomonaco, D., Huang, L., Wolf, D. M., Muller-Tidow, C., Golub, T. R., Kawakami, K., and Ford, H. L. (2004) The Six1 homeoprotein stimulates tumorigenesis by reactivation of cyclin A1 Proc. Natl. Acad. Sci. U. S. A. 101, 6478-6483
56. Keck, J. M., Summers, M. K., Tedesco, D., Ekholm-Reed, S., Chuang, L. C., Jackson, P. K., and Reed, S. I. (2007) Cyclin E overexpression impairs progression through mitosis by inhibiting APC(Cdh1) J. Cell Biol. 178, 371-385
57. Mayya, V., Lundgren, D. H., Hwang, S. I., Rezaul, K., Wu, L., Eng, J. K., Rodionov, V., and Han, D. K. (2009) Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions Sci. Signal. 2, ra46
58. Wang, Z., Zhang, Y., Gu, J. J., Davitt, C., Reeves, R., and Magnuson, N. S. (2010) Pim-2 phosphorylation of p21(Cip1/WAF1) enhances its stability and inhibits cell proliferation in HCT116 cells Int. J. Biochem. Cell Biol. 42, 1030-1038
59. Hodeify, R., Tarcsafalvi, A., Megyesi, J., Safirstein, R. L., and Price, P. M. (2011) Cdk2-dependent phosphorylation of p21 regulates the role of Cdk2 in cisplatin cytotoxicity Am. J. Physiol. Renal Physiol. 300, F1171-1179
60. Harms, C., Albrecht, K., Harms, U., Seidel, K., Hauck, L., Baldinger, T., Hubner, D., Kronenberg, G., An, J., Ruscher, K., Meisel, A., Dirnagl, U., von Harsdorf, R., Endres, M., and Hortnagl, H. (2007) Phosphatidylinositol 3-Akt-kinase-dependent phosphorylation of p21(Waf1/Cip1) as a novel mechanism of neuroprotection by glucocorticoids J. Neurosci. 27, 4562-4571
61. Hukkelhoven, E., Liu, Y., Yeh, N., Ciznadija, D., Blain, S. W., and Koff, A. (2012) Tyrosine phosphorylation of the p21 cyclin-dependent kinase inhibitor facilitates the development of proneural glioma J. Biol. Chem. 287, 38523-38530
62. Kim, G. Y., Mercer, S. E., Ewton, D. Z., Yan, Z., Jin, K., and Friedman, E. (2002) The stress-activated protein kinases p38 alpha and JNK1 stabilize p21(Cip1) by phosphorylation J. Biol. Chem. 277, 29792-29802
63. Dash, B. C. and El-Deiry, W. S. (2005) Phosphorylation of p21 in G2/M promotes cyclin B-Cdc2 kinase activity Mol. Cell. Biol. 25, 3364-3387
64. Mohanty, A. R., Kan, Q., Srivastava, S., Uranbileg, B., Arakawa-Takeuchi, S., Fujita, N., and Okayama, H. (2012) Successive phosphorylation of p27(KIP1) protein at serine-10 and C terminus crucially controls its potency to inactivate Cdk2 J. Biol. Chem. 287, 21757-21764
65. Ou, L., Ferreira, A. M., Otieno, S., Xiao, L., Bashford, D., and Kriwacki, R. W. (2011) Incomplete folding upon binding mediates Cdk4/cyclin D complex activation by tyrosine phosphorylation of inhibitor p27 protein J. Biol. Chem. 286, 30142-30151
66. Wang, D., He, F., Zhang, L., Zhang, F., Wang, Q., Qian, X., Pan, X., Meng, J., Peng, C., Shen, A., and Chen, J. (2011) The role of p27(Kip1) phosphorylation at serine 10 in the migration of malignant glioma cells in vitro Neoplasma 58, 65-73
67. Short, J. D., Dere, R., Houston, K. D., Cai, S. L., Kim, J., Bergeron, J. M., Shen, J., Liang, J., Bedford, M. T., Mills, G. B., and Walker, C. L. (2010) AMPK-mediated phosphorylation of murine p27 at T197 promotes binding of 14-3-3 proteins and increases p27 stability Mol. Carcinog. 49, 429-439
68. Hong, F., Larrea, M. D., Doughty, C., Kwiatkowski, D. J., Squillace, R., and Slingerland, J. M. (2008) mTOR-raptor binds and activates SGK1 to regulate p27 phosphorylation Mol. Cell 30, 701-711
69. Chu, I., Sun, J., Arnaout, A., Kahn, H., Hanna, W., Narod, S., Sun, P., Tan, C. K., Hengst, L., and Slingerland, J. (2007) p27 phosphorylation by Src regulates inhibition of cyclin E-Cdk2 Cell 128, 281-294
70. Viglietto, G., Motti, M. L., Bruni, P., Melillo, R. M., D'Alessio, A., Califano, D., Vinci, F., Chiappetta, G., Tsichlis, P., Bellacosa, A., Fusco, A., and Santoro, M. (2002) Cytoplasmic relocalization and inhibition of the cyclin-dependent kinase inhibitor p27(Kip1) by PKB/Akt-mediated phosphorylation in breast cancer Nat. Med. 8, 1136-1144
71. Shin, I., Yakes, F. M., Rojo, F., Shin, N. Y., Bakin, A. V., Baselga, J., and Arteaga, C. L. (2002) PKB/Akt mediates cell-cycle progression by phosphorylation of p27(Kip1) at threonine 157 and modulation of its cellular localization Nat. Med. 8, 1145-1152
72. Ciarallo, S., Subramaniam, V., Hung, W., Lee, J. H., Kotchetkov, R., Sandhu, C., Milic, A., and Slingerland, J. M. (2002) Altered p27(Kip1) phosphorylation, localization, and function in human epithelial cells resistant to transforming growth factor beta-mediated G(1) arrest Mol. Cell. Biol. 22, 2993-3002