The CDK Subunit CKS2 Counteracts CKS1 to Control Cyclin A/CDK2 Activity in Maintaining Replicative Fidelity and Neurodevelopment

Developmental Cell

Volumn 23, Issue 2, 2012, Pages 356-370

  Frontini, Mattia ^a   Kukalev, Alexander ^a,b   Leo, Elisabetta ^c   Ng, Yiu Ming ^b,d   Cervantes, Marcella ^a   Cheng, Chi Wai ^d   Holic, Roman ^a,e   Dormann, Dirk ^a   Tse, Eric ^d   Pommier, Yves ^c   Yu, Veronica ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b GUY S HOSPITAL   (United Kingdom)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

^e INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; PROTEIN P27;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CYCLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; ENZYME ACTIVITY; IN VIVO STUDY; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; STEM CELL;

ANIMALS; CDC2-CDC28 KINASES; CDC28 PROTEIN KINASE, S CEREVISIAE; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; CELLS, CULTURED; CYCLIN A; CYCLIN-DEPENDENT KINASE 2; DNA DAMAGE; ENZYME ACTIVATION; MICE; MICE, KNOCKOUT; NEURONS;

EID: 84865077612     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.06.018     Document Type: Article

References (55)

1. Anglana M., Apiou F., Bensimon A., Debatisse M. Dynamics of DNA replication in mammalian somatic cells: nucleotide pool modulates origin choice and interorigin spacing. Cell 2003, 114:385-394.
2. Arai Y., Pulvers J.N., Haffner C., Schilling B., Nüsslein I., Calegari F., Huttner W.B. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2011, 2:154.
3. Bensimon A., Aebersold R., Shiloh Y. Beyond ATM: the protein kinase landscape of the DNA damage response. FEBS Lett. 2011, 585:1625-1639.
4. Berthet C., Aleem E., Coppola V., Tessarollo L., Kaldis P. Cdk2 knockout mice are viable. Curr. Biol. 2003, 13:1775-1785.
5. Bourne Y., Watson M.H., Hickey M.J., Holmes W., Rocque W., Reed S.I., Tainer J.A. Crystal structure and mutational analysis of the human CDK2 kinase complex with cell cycle-regulatory protein CksHs1. Cell 1996, 84:863-874.
6. Caillava C., Vandenbosch R., Jablonska B., Deboux C., Spigoni G., Gallo V., Malgrange B., Baron-Van Evercooren A. Cdk2 loss accelerates precursor differentiation and remyelination in the adult central nervous system. J. Cell Biol. 2011, 193:397-407.
7. Calegari F., Huttner W.B. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J. Cell Sci. 2003, 116:4947-4955.
8. Conti C., Caburet S., Schurra C., Bensimon A. Molecular combing. Curr. Protoc. Cytom. 2001, Chapter 8, Unit 8, 10.
9. Conti C., Saccà B., Herrick J., Lalou C., Pommier Y., Bensimon A. Replication fork velocities at adjacent replication origins are coordinately modified during DNA replication in human cells. Mol. Biol. Cell 2007, 18:3059-3067.
10. Cotta-Ramusino C., McDonald E.R., Hurov K., Sowa M.E., Harper J.W., Elledge S.J. A DNA damage response screen identifies RHINO, a 9-1-1 and TopBP1 interacting protein required for ATR signaling. Science 2011, 332:1313-1317.
11. Courbet S., Gay S., Arnoult N., Wronka G., Anglana M., Brison O., Debatisse M. Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 2008, 455:557-560.
12. De Cola A., Bongiorno-Borbone L., Bianchi E., Barcaroli D., Carletti E., Knight R.A., Di Ilio C., Melino G., Sette C., De Laurenzi V. FLASH is essential during early embryogenesis and cooperates with p73 to regulate histone gene transcription. Oncogene 2012, 31:573-582.
13. Dickins R.A., Hemann M.T., Zilfou J.T., Simpson D.R., Ibarra I., Hannon G.J., Lowe S.W. Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat. Genet. 2005, 37:1289-1295.
14. Egan E.A., Solomon M.J. Cyclin-stimulated binding of Cks proteins to cyclin-dependent kinases. Mol. Cell. Biol. 1998, 18:3659-3667.
15. Ge X.Q., Blow J.J. Chk1 inhibits replication factory activation but allows dormant origin firing in existing factories. J. Cell Biol. 2010, 191:1285-1297.
16. Hao B., Zheng N., Schulman B.A., Wu G., Miller J.J., Pagano M., Pavletich N.P. Structural basis of the Cks1-dependent recognition of p27(Kip1) by the SCF(Skp2) ubiquitin ligase. Mol. Cell 2005, 20:9-19.
17. Holic R., Kukalev A., Lane S., Andress E.J., Lau I., Yu C.W., Edelmann M.J., Kessler B.M., Yu V.P. Cks1 activates transcription by binding to the ubiquitylated proteasome. Mol. Cell. Biol. 2010, 30:3894-3901.
18. Jablonska B., Aguirre A., Vandenbosch R., Belachew S., Berthet C., Kaldis P., Gallo V. Cdk2 is critical for proliferation and self-renewal of neural progenitor cells in the adult subventricular zone. J. Cell Biol. 2007, 179:1231-1245.
19. Karnani N., Dutta A. The effect of the intra-S-phase checkpoint on origins of replication in human cells. Genes Dev. 2011, 25:621-633.
20. Kawabata T., Luebben S.W., Yamaguchi S., Ilves I., Matise I., Buske T., Botchan M.R., Shima N. Stalled fork rescue via dormant replication origins in unchallenged S phase promotes proper chromosome segregation and tumor suppression. Mol. Cell 2011, 41:543-553.
21. Kõivomägi M., Valk E., Venta R., Iofik A., Lepiku M., Balog E.R., Rubin S.M., Morgan D.O., Loog M. Cascades of multisite phosphorylation control Sic1 destruction at the onset of S phase. Nature 2011, 480:128-131.
22. Lange C., Huttner W.B., Calegari F. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 2009, 5:320-331.
23. Liberal V., Martinsson-Ahlzén H.S., Liberal J., Spruck C.H., Widschwendter M., McGowan C.H., Reed S.I. Cyclin-dependent kinase subunit (Cks) 1 or Cks2 overexpression overrides the DNA damage response barrier triggered by activated oncoproteins. Proc. Natl. Acad. Sci. USA 2012, 109:2754-2759.
24. Martinsson-Ahlzén H.S., Liberal V., Grünenfelder B., Chaves S.R., Spruck C.H., Reed S.I. Cyclin-dependent kinase-associated proteins Cks1 and Cks2 are essential during early embryogenesis and for cell cycle progression in somatic cells. Mol. Cell. Biol. 2008, 28:5698-5709.
25. Merrick K.A., Larochelle S., Zhang C., Allen J.J., Shokat K.M., Fisher R.P. Distinct activation pathways confer cyclin-binding specificity on Cdk1 and Cdk2 in human cells. Mol. Cell 2008, 32:662-672.
26. Merrick K.A., Wohlbold L., Zhang C., Allen J.J., Horiuchi D., Huskey N.E., Goga A., Shokat K.M., Fisher R.P. Switching Cdk2 on or off with small molecules to reveal requirements in human cell proliferation. Mol. Cell 2011, 42:624-636.
27. Montagnoli A., Fiore F., Eytan E., Carrano A.C., Draetta G.F., Hershko A., Pagano M. Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. Genes Dev. 1999, 13:1181-1189.
28. Morris M.C., Kaiser P., Rudyak S., Baskerville C., Watson M.H., Reed S.I. Cks1-dependent proteasome recruitment and activation of CDC20 transcription in budding yeast. Nature 2003, 423:1009-1013.
29. Nakayama K., Nagahama H., Minamishima Y.A., Miyake S., Ishida N., Hatakeyama S., Kitagawa M., Iemura S., Natsume T., Nakayama K.I. Skp2-mediated degradation of p27 regulates progression into mitosis. Dev. Cell 2004, 6:661-672.
30. Nguyen L., Besson A., Heng J.I., Schuurmans C., Teboul L., Parras C., Philpott A., Roberts J.M., Guillemot F. p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 2006, 20:1511-1524.
31. Nguyen L., Besson A., Roberts J.M., Guillemot F. Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle 2006, 5:2314-2318.
32. Nord A.S., Chang P.J., Conklin B.R., Cox A.V., Harper C.A., Hicks G.G., Huang C.C., Johns S.J., Kawamoto M., Liu S., et al. The International Gene Trap Consortium Website: a portal to all publicly available gene trap cell lines in mouse. Nucleic Acids Res. 2006, 34(Database issue):D642-D648.
33. Ortega S., Prieto I., Odajima J., Martín A., Dubus P., Sotillo R., Barbero J.L., Malumbres M., Barbacid M. Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat. Genet. 2003, 35:25-31.
34. Pagano M., Pepperkok R., Lukas J., Baldin V., Ansorge W., Bartek J., Draetta G. Regulation of the cell cycle by the cdk2 protein kinase in cultured human fibroblasts. J. Cell Biol. 1993, 121:101-111.
35. Pagliuca F.W., Collins M.O., Lichawska A., Zegerman P., Choudhary J.S., Pines J. Quantitative proteomics reveals the basis for the biochemical specificity of the cell-cycle machinery. Mol. Cell 2011, 43:406-417.
36. Patra D., Wang S.X., Kumagai A., Dunphy W.G. The xenopus Suc1/Cks protein promotes the phosphorylation of G(2)/M regulators. J. Biol. Chem. 1999, 274:36839-36842.
37. Pilaz L.J., Patti D., Marcy G., Ollier E., Pfister S., Douglas R.J., Betizeau M., Gautier E., Cortay V., Doerflinger N., et al. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc. Natl. Acad. Sci. USA 2009, 106:21924-21929.
38. Poli J., Tsaponina O., Crabbé L., Keszthelyi A., Pantesco V., Chabes A., Lengronne A., Pasero P. dNTP pools determine fork progression and origin usage under replication stress. EMBO J. 2012, 31:883-894.
39. Polo S.E., Jackson S.P. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 2011, 25:409-433.
40. Reynard G.J., Reynolds W., Verma R., Deshaies R.J. Cks1 is required for G(1) cyclin-cyclin-dependent kinase activity in budding yeast. Mol. Cell. Biol. 2000, 20:5858-5864.
41. Santamaría D., Barrière C., Cerqueira A., Hunt S., Tardy C., Newton K., Cáceres J.F., Dubus P., Malumbres M., Barbacid M. Cdk1 is sufficient to drive the mammalian cell cycle. Nature 2007, 448:811-815.
42. Seiler J.A., Conti C., Syed A., Aladjem M.I., Pommier Y. The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses. Mol. Cell. Biol. 2007, 27:5806-5818.
43. Sicinski P., Zacharek S., Kim C. Duality of p27Kip1 function in tumorigenesis. Genes Dev. 2007, 21:1703-1706.
44. Sitry D., Seeliger M.A., Ko T.K., Ganoth D., Breward S.E., Itzhaki L.S., Pagano M., Hershko A. Three different binding sites of Cks1 are required for p27-ubiquitin ligation. J. Biol. Chem. 2002, 277:42233-42240.
45. Spruck C., Strohmaier H., Watson M., Smith A.P., Ryan A., Krek T.W., Reed S.I. A CDK-independent function of mammalian Cks1: targeting of SCF(Skp2) to the CDK inhibitor p27Kip1. Mol. Cell 2001, 7:639-650.
46. Spruck C.H., de Miguel M.P., Smith A.P., Ryan A., Stein P., Schultz R.M., Lincoln A.J., Donovan P.J., Reed S.I. Requirement of Cks2 for the first metaphase/anaphase transition of mammalian meiosis. Science 2003, 300:647-650.
47. Tane S., Chibazakura T. Cyclin A overexpression induces chromosomal double-strand breaks in mammalian cells. Cell Cycle 2009, 8:3900-3903.
48. Todaro G.J., Green H. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 1963, 17:299-313.
49. van Zon W., Ogink J., ter Riet B., Medema R.H., te Riele H., Wolthuis R.M. The APC/C recruits cyclin B1-Cdk1-Cks in prometaphase before D box recognition to control mitotic exit. J. Cell Biol. 2010, 190:587-602.
50. Westbrook L., Manuvakhova M., Kern F.G., Estes N.R., Ramanathan H.N., Thottassery J.V. Cks1 regulates cdk1 expression: a novel role during mitotic entry in breast cancer cells. Cancer Res. 2007, 67:11393-11401.
51. Wheeler L.W., Lents N.H., Baldassare J.J. Cyclin A-CDK activity during G1 phase impairs MCM chromatin loading and inhibits DNA synthesis in mammalian cells. Cell Cycle 2008, 7:2179-2188.
52. Wilsker D., Petermann E., Helleday T., Bunz F. Essential function of Chk1 can be uncoupled from DNA damage checkpoint and replication control. Proc. Natl. Acad. Sci. USA 2008, 105:20752-20757.
53. Wolthuis R., Clay-Farrace L., van Zon W., Yekezare M., Koop L., Ogink J., Medema R., Pines J. Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A. Mol. Cell 2008, 30:290-302.
54. Yao Z.P., Zhou M., Kelly S.E., Seeliger M.A., Robinson C.V., Itzhaki L.S. Activation of ubiquitin ligase SCF(Skp2) by Cks1: insights from hydrogen exchange mass spectrometry. J. Mol. Biol. 2006, 363:673-686.
55. Yu V.P., Baskerville C., Grünenfelder B., Reed S.I. A kinase-independent function of Cks1 and Cdk1 in regulation of transcription. Mol. Cell 2005, 17:145-151.