Phylogenetic analysis of CDK and cyclin proteins in premetazoan lineages

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Cao, Lihuan ^a   Chen, Fang ^a   Yang, Xianmei ^a   Xu, Weijin ^a   Xie, Jun ^a   Yu, Long ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

CDK; Cell cycle; Cyclin; Evolution; Metazoan emergence

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLINE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; ENZYMOLOGY; EUKARYOTE; FUNGUS; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY;

AMINO ACID SEQUENCE; ANIMALS; CYCLIN-DEPENDENT KINASES; CYCLINS; EUKARYOTA; EVOLUTION, MOLECULAR; FUNGI; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY;

EID: 84892470353     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-14-10     Document Type: Article

References (96)

1. Cyclins and cyclin-dependent kinases: a biochemical view. Pines J, Biochem J 1995 308 Pt 3 697 711 8948422
2. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Nigg EA, Bioessays 1995 17 6 471 480 10.1002/bies.950170603 7575488
3. Cyclins and their associated cyclin-dependent kinases in the human cell cycle. Pines J, Biochem Soc Trans 1993 21 4 921 925 8132094 (Pubitemid 24011757)
4. Roles of ubiquitin-mediated proteolysis in cell cycle control. Hershko A, Curr Opin Cell Biol 1997 9 6 788 799 10.1016/S0955-0674(97)80079-8 9425343 (Pubitemid 27517267)
5. Cyclin-dependent kinases: engines, clocks, and microprocessors. Morgan DO, Annu Rev Cell Dev Biol 1997 13 261 291 10.1146/annurev.cellbio.13.1.261 9442875 (Pubitemid 28034527)
6. Physiological relevance of cell cycle kinases. Malumbres M, Physiol Rev 2011 91 3 973 1007 10.1152/physrev.00025.2010 21742793
7. Early animal evolution: emerging views from comparative biology and geology. Knoll AH, Carroll SB, Science 1999 284 5423 2129 2137 10.1126/science.284.5423.2129 10381872 (Pubitemid 29297467)
8. The molecular origins of multicellular transitions. Rokas A, Curr Opin Genet Dev 2008 18 6 472 478 10.1016/j.gde.2008.09.004 18926910
9. The origins of multicellularity and the early history of the genetic toolkit for animal development. Rokas A, Annu Rev Genet 2008 42 235 251 10.1146/annurev.genet.42.110807.091513 18983257
10. The origins of multicellularity: a multi-taxon genome initiative. Ruiz-Trillo I, Burger G, Holland PW, King N, Lang BF, Roger AJ, Gray MW, Trends Genet 2007 23 3 113 118 10.1016/j.tig.2007.01.005 17275133
11. Ancient origin of the integrin-mediated adhesion and signaling machinery. Sebe-Pedros A, Roger AJ, Lang FB, King N, Ruiz-Trillo I, Proc Natl Acad Sci U S A 2010 107 22 10142 10147 10.1073/pnas.1002257107 20479219
12. Early evolution of metazoan transcription factors. Degnan BM, Vervoort M, Larroux C, Richards GS, Curr Opin Genet Dev 2009 19 6 591 599 10.1016/j.gde.2009.09.008 19880309
13. Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Sebe-Pedros A, de Mendoza A, Lang BF, Degnan BM, Ruiz-Trillo I, Mol Biol Evol 2011 28 3 1241 1254 10.1093/molbev/msq309 21087945
14. Ancient origin of the Hox gene cluster. Ferrier DE, Holland PW, Nat Rev Genet 2001 2 1 33 38 11253066 (Pubitemid 33674767)
15. The genesis and evolution of homeobox gene clusters. Garcia-Fernandez J, Nat Rev Genet 2005 6 12 881 892 10.1038/nrg1723 16341069 (Pubitemid 41778696)
16. Premetazoan ancestry of the Myc-Max network. Young SL, Diolaiti D, Conacci-Sorrell M, Ruiz-Trillo I, Eisenman RN, King N, Mol Biol Evol 2011 28 10 2961 2971 10.1093/molbev/msr132 21571926
17. Unexpected complexity of the Wnt gene family in a sea anemone. Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, Technau U, von Haeseler A, Hobmayer B, Martindale MQ, et al. Nature 2005 433 7022 156 160 10.1038/nature03158 15650739
18. The evolutionary history of the catenin gene family during metazoan evolution. Zhao ZM, Reynolds AB, Gaucher EA, BMC Evol Biol 2011 11 198 10.1186/1471-2148-11-198 21740572
19. A receptor tyrosine kinase from choanoflagellates: molecular insights into early animal evolution. King N, Carroll SB, Proc Natl Acad Sci U S A 2001 98 26 15032 15037 10.1073/pnas.261477698 11752452 (Pubitemid 34013964)
20. Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages. Pincus D, Letunic I, Bork P, Lim WA, Proc Natl Acad Sci U S A 2008 105 28 9680 9684 10.1073/pnas.0803161105 18599463 (Pubitemid 352031360)
21. Unicellular Ca2+ signaling 'toolkit' at the origin of metazoa. Cai X, Mol Biol Evol 2008 25 7 1357 1361 10.1093/molbev/msn077 18385221 (Pubitemid 351882007)
22. The premetazoan ancestry of cadherins. Abedin M, King N, Science 2008 319 5865 946 948 10.1126/science.1151084 18276888 (Pubitemid 351263763)
23. New insights into the evolution of metazoan cadherins. Hulpiau P, van Roy F, Mol Biol Evol 2011 28 1 647 657 10.1093/molbev/msq233 20817718
24. Origin and evolution of laminin gene family diversity. Fahey B, Degnan BM, Mol Biol Evol 2012 29 7 1823 1836 10.1093/molbev/mss060 22319142
25. Early evolution of animal cell signaling and adhesion genes. Nichols SA, Dirks W, Pearse JS, King N, Proc Natl Acad Sci U S A 2006 103 33 12451 12456 10.1073/pnas.0604065103 16891419 (Pubitemid 44267280)
26. Diverse evolutionary paths to cell adhesion. Abedin M, King N, Trends Cell Biol 2010 20 12 734 742 10.1016/j.tcb.2010.08.002 20817460
27. The evolution of metazoan extracellular matrix. Hynes RO, J Cell Biol 2012 196 6 671 679 10.1083/jcb.201109041 22431747
28. The Amphimedon queenslandica genome and the evolution of animal complexity. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, et al. Nature 2010 466 7307 720 726 10.1038/nature09201 20686567
29. The origins and evolution of the p53 family of genes. Belyi VA, Ak P, Markert E, Wang H, Hu W, Puzio-Kuter A, Levine AJ, Cold Spring Harb Perspect Biol 2010 2 6 001198 20516129
30. The ancient function of RB-E2F pathway: insights from its evolutionary history. Cao L, Peng B, Yao L, Zhang X, Sun K, Yang X, Yu L, Biol Direct 2010 5 55 10.1186/1745-6150-5-55 20849664
31. Cell cycle control across the eukaryotic kingdom. Harashima H, Dissmeyer N, Schnittger A, Trends Cell Biol 2013 23 7 345 356 10.1016/j.tcb.2013.03.002 23566594
32. Model scenarios for evolution of the eukaryotic cell cycle. Novak B, Csikasz-Nagy A, Gyorffy B, Nasmyth K, Tyson JJ, Philos Trans R Soc Lond B Biol Sci 1998 353 1378 2063 2076 10.1098/rstb.1998.0352 10098216 (Pubitemid 29032760)
33. Evolution of networks and sequences in eukaryotic cell cycle control. Cross FR, Buchler NE, Skotheim JM, Philos Trans R Soc Lond B Biol Sci 2011 366 1584 3532 3544 10.1098/rstb.2011.0078 22084380
34. Evolution of eukaryotic cell cycle regulation: stepwise addition of regulatory kinases and late advent of the CDKs. Krylov DM, Nasmyth K, Koonin EV, Curr Biol 2003 13 2 173 177 10.1016/S0960-9822(03)00008-3 12546794 (Pubitemid 36154348)
35. Mammalian cyclin-dependent kinases. Malumbres M, Barbacid M, Trends Biochem Sci 2005 30 11 630 641 10.1016/j.tibs.2005.09.005 16236519 (Pubitemid 41540083)
36. Cyclin-dependent kinases: a family portrait. Malumbres M, Harlow E, Hunt T, Hunter T, Lahti JM, Manning G, Morgan DO, Tsai LH, Wolgemuth DJ, Nat Cell Biol 2009 11 11 1275 1276 10.1038/ncb1109-1275 19884882
37. Functional evolution of cyclin-dependent kinases. Doonan JH, Kitsios G, Mol Biotechnol 2009 42 1 14 29 10.1007/s12033-008-9126-8 19145493
38. Evolution of cyclin-dependent kinases (CDKs) and CDK-activating kinases (CAKs): differential conservation of CAKs in yeast and metazoa. Liu J, Kipreos ET, Mol Biol Evol 2000 17 7 1061 1074 10.1093/oxfordjournals.molbev.a026387 10889219 (Pubitemid 30419219)
39. Comparative genomics of cyclin-dependent kinases suggest co-evolution of the RNAP II C-terminal domain and CTD-directed CDKs. Guo Z, Stiller JW, BMC Genomics 2004 5 69 10.1186/1471-2164-5-69 15380029 (Pubitemid 39546650)
40. Molecular evolution of cyclin proteins in animals and fungi. Gunbin KV, Suslov V, Turnaev II, Afonnikov DA, Kolchanov NA, BMC Evol Biol 2011 11 224 10.1186/1471-2148-11-224 21798004
41. Phylogenetic analysis reveals the evolution and diversification of cyclins in eukaryotes. Ma Z, Wu Y, Jin J, Yan J, Kuang S, Zhou M, Zhang Y, Guo AY, Mol Phylogenet Evol 2013 66 3 1002 1010 10.1016/j.ympev.2012.12.007 23261709
42. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, et al. Nature 2008 451 7180 783 788 10.1038/nature06617 18273011 (Pubitemid 351253174)
43. The Trichoplax genome and the nature of placozoans. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, et al. Nature 2008 454 7207 955 960 10.1038/nature07191 18719581
44. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, et al. Science 2007 317 5834 86 94 10.1126/science.1139158 17615350 (Pubitemid 47056460)
45. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ, Nucleic Acids Res 1997 25 17 3389 3402 10.1093/nar/25.17.3389 9254694 (Pubitemid 27359211)
46. HMMER web server: interactive sequence similarity searching. Finn RD, Clements J, Eddy SR, Nucleic Acids Res 2011 39 Web Server issue 29 W37 21593126
47. The Pfam protein families database. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, et al. Nucleic Acids Res 2008 36 Database issue 281 D288 18039703
48. SMART 5: domains in the context of genomes and networks. Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, Bork P, Nucleic Acids Res 2006 34 Database issue 257 D260 16381859
49. MSAProbs: multiple sequence alignment based on pair hidden Markov models and partition function posterior probabilities. Liu Y, Schmidt B, Maskell D, Bioinformatics 2010 26 16 1958 1964 10.1093/bioinformatics/btq338 20576627
50. PROMALS: towards accurate multiple sequence alignments of distantly related proteins. Pei J, Grishin NV, Bioinformatics 2007 23 7 802 808 10.1093/bioinformatics/btm017 17267437 (Pubitemid 47049913)
51. ProtTest 3: fast selection of best-fit models of protein evolution. Darriba D, Taboada GL, Doallo R, Posada D, Bioinformatics 2011 27 8 1164 1165 10.1093/bioinformatics/btr088 21335321
52. Pfeiffer W, Stamatakis A, Hybrid MPI/Pthreads Parallelization of the RAxML Phylogenetics Code Atlanta: Ninth IEEE International Workshop on High Performance Computational Biology (HiCOMB 2010) 2010
53. Miller MA, Pfeiffer W, Schwartz T, Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees New Orleans, LA: Proceedings of the Gateway Computing Environments Workshop (GCE) 2010 1 8
54. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Lartillot N, Lepage T, Blanquart S, Bioinformatics 2009 25 17 2286 2288 10.1093/bioinformatics/btp368 19535536
55. Dendroscope: an interactive viewer for large phylogenetic trees. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R, BMC Bioinforma 2007 8 460 10.1186/1471-2105-8-460 (Pubitemid 351168201)
56. Application of phylogenetic networks in evolutionary studies. Huson DH, Bryant D, Mol Biol Evol 2006 23 2 254 267 16221896 (Pubitemid 43100040)
57. Computational methods for gene orthology inference. Kristensen DM, Wolf YI, Mushegian AR, Koonin EV, Brief Bioinform 2011 12 5 379 391 10.1093/bib/bbr030 21690100
58. A genomic perspective on protein families. Tatusov RL, Science 1997 278 631 637 10.1126/science.278.5338.631 9381173 (Pubitemid 27464953)
59. Predicting function: from genes to genomes and back. Bork P, Dandekar T, Diaz-Lazcoz Y, Eisenhaber F, Huynen M, Yuan Y, J Mol Biol 1998 283 707 725 10.1006/jmbi.1998.2144 9790834 (Pubitemid 28495340)
60. Ancient complexity, opisthokont plasticity, and discovery of the 11th subfamily of Arf GAP proteins. Schlacht A, Mowbrey K, Elias M, Kahn RA, Dacks JB, Traffic 2013 14 6 636 649 10.1111/tra.12063 23433073
61. The genome of the social amoeba Dictyostelium discoideum. Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, et al. Nature 2005 435 7038 43 57 10.1038/nature03481 15875012 (Pubitemid 40655903)
62. Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single-copy protein domains. Torruella G, Derelle R, Paps J, Lang BF, Roger AJ, Shalchian-Tabrizi K, Ruiz-Trillo I, Mol Biol Evol 2012 29 2 531 544 10.1093/molbev/msr185 21771718
63. Cell cycle, CDKs and cancer: a changing paradigm. Malumbres M, Barbacid M, Nat Rev Cancer 2009 9 3 153 166 10.1038/nrc2602 19238148
64. Cellular control of gene expression by T-type cyclin/CDK9 complexes. Garriga J, Grana X, Gene 2004 337 15 23 15276198 (Pubitemid 38970101)
65. Cdk10, a Cdc2-related kinase, associates with the Ets2 transcription factor and modulates its transactivation activity. Kasten M, Giordano A, Oncogene 2001 20 15 1832 1838 10.1038/sj.onc.1204295 11313931 (Pubitemid 32458693)
66. Nuclear localization of Cdk5 is a key determinant in the postmitotic state of neurons. Zhang J, Cicero SA, Wang L, Romito-Digiacomo RR, Yang Y, Herrup K, Proc Natl Acad Sci U S A 2008 105 25 8772 8777 10.1073/pnas.0711355105 18550843 (Pubitemid 351987755)
67. Multiple levels of cyclin specificity in cell-cycle control. Bloom J, Cross FR, Nat Rev Mol Cell Biol 2007 8 2 149 160 10.1038/nrm2105 17245415 (Pubitemid 46432532)
68. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Soni R, Carmichael JP, Shah ZH, Murray JA, Plant Cell 1995 7 1 85 103 7696881
69. Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, DePamphilis CW, Ma H, Plant Physiol 2004 135 2 1084 1099 10.1104/pp.104.040436 15208425 (Pubitemid 38819051)
70. Morgan DO, The Cell Cycle: Principles of Control London, UK: New Science Press 2007
71. A- and B-type cyclins differentially modulate substrate specificity of cyclin-cdk complexes. Peeper DS, Parker LL, Ewen ME, Toebes M, Hall FL, Xu M, Zantema A, van der Eb AJ, Piwnica-Worms H, EMBO J 1993 12 5 1947 1954 8491188 (Pubitemid 23157711)
72. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Loog M, Morgan DO, Nature 2005 434 7029 104 108 10.1038/nature03329 15744308 (Pubitemid 40349393)
73. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Kato J, Matsushime H, Hiebert SW, Ewen ME, Sherr CJ, Genes Dev 1993 7 3 331 342 8449399 (Pubitemid 23139228)
74. Ultrasensitivity in the Regulation of Cdc25C by Cdk1. Trunnell NB, Poon AC, Kim SY, Ferrell JE Jr, Mol Cell 2011 41 3 263 274 10.1016/j.molcel.2011.01. 012 21292159
75. M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFbeta-TrCP. Watanabe N, Arai H, Nishihara Y, Taniguchi M, Hunter T, Osada H, Proc Natl Acad Sci U S A 2004 101 13 4419 4424 10.1073/pnas.0307700101 15070733 (Pubitemid 38437427)
76. Crystal structure of human CDK4 in complex with a D-type cyclin. Day PJ, Cleasby A, Tickle IJ, O'Reilly M, Coyle JE, Holding FP, McMenamin RL, Yon J, Chopra R, Lengauer C, et al. Proc Natl Acad Sci U S A 2009 106 11 4166 4170 10.1073/pnas.0809645106 19237565
77. The structure of CDK4/cyclin D3 has implications for models of CDK activation. Takaki T, Echalier A, Brown NR, Hunt T, Endicott JA, Noble ME, Proc Natl Acad Sci U S A 2009 106 11 4171 4176 10.1073/pnas.0809674106 19237555
78. Cln3 activates G1-specific transcription via phosphorylation of the SBF bound repressor Whi5. de Bruin RA, McDonald WH, Kalashnikova TI, Yates J, Wittenberg C, Cell 2004 117 887 898 10.1016/j.cell.2004.05.025 15210110 (Pubitemid 38798855)
79. An architectural perspective of cell-cycle control at the G1/S phase cell-cycle transition. Stein GS, van Wijnen AJ, Stein JL, Lian JB, Montecino M, et al. J Cell Physiol 2006 209 706 710 10.1002/jcp.20843 17001681 (Pubitemid 44665691)
80. Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase. Becker KA, Ghule PN, Therrien JA, Lian JB, Stein JL, van Wijnen AJ, Stein GS, J Cell Physiol 2006 209 3 883 893 10.1002/jcp.20776 16972248 (Pubitemid 44665710)
81. Establishment of histone gene regulation and cell cycle checkpoint control in human embryonic stem cells. Becker KA, Stein JL, Lian JB, van Wijnen AJ, Stein GS, J Cell Physiol 2007 210 2 517 526 10.1002/jcp.20903 17096384 (Pubitemid 44956897)
82. A restriction point for control of normal animal cell proliferation. Pardee AB, Proc Natl Acad Sci U S A 1974 71 4 1286 1290 10.1073/pnas.71.4.1286 4524638
83. G1 events and regulation of cell proliferation. Pardee AB, Science 1989 246 4930 603 608 10.1126/science.2683075 2683075
84. A single fission yeast mitotic cyclin B-p34cdc2 kinase promotes both S-phase and mitosis in the absence of G1 cyclins. Fisher DL, Nurse P, EMBO J 1996 15 4 850 860 8631306
85. Living with or without cyclins and cyclin-dependent kinases. Sherr CJ, Roberts JM, Genes Dev 2004 18 22 2699 2711 10.1101/gad.1256504 15545627 (Pubitemid 39507762)
86. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Sicinski P, Donaher JL, Parker SB, Li T, Fazeli A, Gardner H, Haslam SZ, Bronson RT, Elledge SJ, Weinberg RA, Cell 1995 82 4 621 630 10.1016/0092-8674(95)90034-9 7664341
87. Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Fantl V, Stamp G, Andrews A, Rosewell I, Dickson C, Genes Dev 1995 9 19 2364 2372 10.1101/gad.9.19.2364 7557388
88. Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Sicinski P, Donaher JL, Geng Y, Parker SB, Gardner H, Park MY, Robker RL, Richards JS, McGinnis LK, Biggers JD, et al. Nature 1996 384 6608 470 474 10.1038/384470a0 8945475 (Pubitemid 26414665)
89. Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Huard JM, Forster CC, Carter ML, Sicinski P, Ross ME, Development 1999 126 9 1927 1935 10101126 (Pubitemid 29240326)
90. Requirement for cyclin D3 in lymphocyte development and T cell leukemias. Sicinska E, Aifantis I, Le Cam L, Swat W, Borowski C, Yu Q, Ferrando AA, Levin SD, Geng Y, von Boehmer H, et al. Cancer Cell 2003 4 6 451 461 10.1016/S1535-6108(03)00301-5 14706337 (Pubitemid 38050042)
91. Development of mice expressing a single D-type cyclin. Ciemerych MA, Kenney AM, Sicinska E, Kalaszczynska I, Bronson RT, Rowitch DH, Gardner H, Sicinski P, Genes Dev 2002 16 24 3277 3289 10.1101/gad.1023602 12502747 (Pubitemid 36025979)
92. Mouse development and cell proliferation in the absence of D-cyclins. Kozar K, Ciemerych MA, Rebel VI, Shigematsu H, Zagozdzon A, Sicinska E, Geng Y, Yu Q, Bhattacharya S, Bronson RT, et al. Cell 2004 118 4 477 491 10.1016/j.cell.2004.07.025 15315760 (Pubitemid 39485667)
93. Targeted disruption of CDK4 delays cell cycle entry with enhanced p27(Kip1) activity. Tsutsui T, Hesabi B, Moons DS, Pandolfi PP, Hansel KS, Koff A, Kiyokawa H, Mol Cell Biol 1999 19 10 7011 7019 10490638 (Pubitemid 29441883)
94. Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in beta-islet cell hyperplasia. Rane SG, Dubus P, Mettus RV, Galbreath EJ, Boden G, Reddy EP, Barbacid M, Nat Genet 1999 22 1 44 52 10.1038/8751 10319860 (Pubitemid 29214803)
95. Pituitary hypoplasia and lactotroph dysfunction in mice deficient for cyclin-dependent kinase-4. Moons DS, Jirawatnotai S, Parlow AF, Gibori G, Kineman RD, Kiyokawa H, Endocrinology 2002 143 8 3001 3008 10.1210/endo.143.8. 8956 12130566 (Pubitemid 34809873)
96. Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Malumbres M, Sotillo R, Santamaria D, Galan J, Cerezo A, Ortega S, Dubus P, Barbacid M, Cell 2004 118 4 493 504 10.1016/j.cell.2004.08.002 15315761 (Pubitemid 39485668)