CDC-25.1 controls the rate of germline mitotic cell cycle by counteracting WEE-1.3 and by positively regulating CDK-1 in Caenorhabditis elegans

Cell Cycle

Volumn 11, Issue 7, 2012, Pages 1354-1363

  Yoon, Sunghee ^a   Kawasaki, Ichiro ^a   Shim, Yhong Hee ^a  

^a Konkuk University   (South Korea)

Author keywords

C. Elegans; cdc 25.1; cdk 1; Cell cycle rate; cyb 3; Germline mitotic proliferation; wee 1.3

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 25 1; CYCLIN DEPENDENT KINASE 4; RNA; RNA CYB 3; RNA WEE 1 3; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE REGULATION; CELL PROLIFERATION; DOWNSTREAM PROCESSING; ENZYME ACTIVITY; EPISTASIS; GERM LINE; MITOSIS; NONHUMAN;

CAENORHABDITIS ELEGANS;

EID: 84860351540     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.19755     Document Type: Article

References (69)

1. Beach D, Durkacz B, Nurse P. Functionally homologous cell cycle control genes in budding and fission yeast. Nature 1982; 300:706-9; PMID:6757758; http://dx.doi.org/10.1038/300706a0.
2. Hartwell LH. Saccharomyces cerevisiae cell cycle. Bacteriol Rev 1974; 38:164-98; PMID:4599449.
3. 2 for control of mitosis in fission yeast. Nature 1981; 292:558-60; PMID:7254352; http://dx.doi.org/10.1038/292558a0.
4. Malumbres M, Barbacid M. Mammalian cyclin-dependent kinases. Trends Biochem Sci 2005; 30:630-41; PMID:16236519; http://dx.doi.org/10.1016/j.tibs. 2005.09.005.
5. +, a gene encoding a protein kinase homolog. Cell 1987; 49:559-67; PMID:3032459; http://dx.doi.org/10.1016/0092-8674(87)90458-2.
6. Kim J, Kawasaki I, Shim YH. Cdc25.2, a C. elegans ortholog of Cdc25, is required to promote oocyte maturation. J Cell Sci 2010; 123:993-1000; PMID:20200231; http://dx.doi.org/10.1242/jcs.060442.
7. Mueller PR, Coleman TR, Kumagai A, Dunphy WG. Myt1: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science 1995; 270:86-90; PMID:7569953; http://dx.doi.org/10.1126/ science.270.5233.86.
8. Cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science 1992; 257:1955-7; PMID:1384126; http://dx.doi.org/10.1126/science.1384126.
9. Liu F, Stanton JJ, Wu Z, Piwnica-Worms H. The human Myt1 kinase preferentially phosphorylates Cdc2 on threonine 14 and localizes to the endoplasmic reticulum and Golgi complex. Mol Cell Biol 1997; 17:571-83; PMID:9001210.
10. Wroble BN, Finkielstein CV, Sible JC. Wee1 kinase alters cyclin E/Cdk2 and promotes apoptosis during the early embryonic development of Xenopus laevis. BMC Dev Biol 2007; 7:119; PMID:17961226; http://dx.doi.org/10.1186/1471-213X-7- 119.
11. Chen S, Gardner DG. Suppression of WEE1 and stimulation of Cdc25A correlates with endothelin-dependent proliferation of rat aortic smooth muscle cells. J Biol Chem 2004; 279:13755-63; PMID:14742443; http://dx.doi.org/10.1074/ jbc.M310064200.
12. Gu Y, Rosenblatt J, Morgan DO. Cell cycle regulation of Cdk2 activity by phosphorylation of Thr160 and Tyr15. EMBO J 1992; 11:3995-4005; PMID:1396589.
13. Watanabe N, Broome M, Hunter T. Regulation of the human WEE1Hu Cdk tyrosine 15-kinase during the cell cycle. EMBO J 1995; 14:1878-91; PMID:7743995.
14. Sebastian B, Kakizuka A, Hunter T. Cdc25M2 activation of cyclin-dependent kinases by dephosphorylation of threonine-14 and tyrosine-15. Proc Natl Acad Sci USA 1993; 90:3521-4; PMID:8475101; http://dx.doi.org/10.1073/pnas.90.8.3521.
15. + functions as an inducer in the mitotic control of fission yeast. Cell 1986; 45:145-53; PMID:3955656; http://dx.doi.org/10.1016/0092-8674(86)90546-5.
16. Russell P, Moreno S, Reed SI. Conservation of mitotic controls in fission and budding yeasts. Cell 1989; 57:295-303; PMID:2649252; http://dx.doi.org/10. 1016/0092-8674(89)90967-7.
17. Ashcroft NR, Kosinski ME, Wickramasinghe D, Donovan PJ, Golden A. The four Cdc25 genes from the nematode Caenorhabditis elegans. Gene 1998; 214:59-66; PMID:9651482; http://dx.doi.org/10.1016/S0378-1119(98)00228-5.
18. Edgar BA, O'Farrell PH. Genetic control of cell division patterns in the Drosophila embryo. Cell 1989; 57:177-87; PMID:2702688; http://dx.doi.org/10. 1016/0092-8674(89)90183-9.
19. Alphey L, Jimenez J, White-Cooper H, Dawson I, Nurse P, Glover DM. twine, a Cdc25 homolog that functions in the male and female germline of Drosophila. Cell 1992; 69:977-88; PMID:1606618; http://dx.doi.org/10.1016/0092-8674(92) 90616-K.
20. Draetta G, Eckstein J. Cdc25 protein phosphatases in cell proliferation. Biochim Biophys Acta 1997; 1332:53-63; PMID:9141461.
21. Ashcroft NR, Srayko M, Kosinski ME, Mains PE, Golden A. RNA-Mediated interference of a Cdc25 homolog in Caenorhabditis elegans results in defects in the embryonic cortical membrane, meiosis and mitosis. Dev Biol 1999; 206:15-32; PMID:9918692; http://dx.doi.org/10.1006/dbio.1998.9135.
22. Ashcroft N, Golden A. Cdc25.1 regulates germline proliferation in Caenorhabditis elegans. Genesis 2002; 33:1-7; PMID:12001064; http://dx.doi.org/10.1002/gene.10083.
23. Kim J, Lee AR, Kawasaki I, Strome S, Shim YH. A mutation of Cdc25.1 causes defects in germ cells but not in somatic tissues in C. elegans. Mol Cells 2009; 28:43-8; PMID:19533027; http://dx.doi.org/10.1007/s10059-009-0098-8.
24. Sulston JE, Schierenberg E, White JG, Thomson JN. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 1983; 100:64-119; PMID:6684600; http://dx.doi.org/10.1016/0012-1606(83)90201-4.
25. Hirsh D, Oppenheim D, Klass M. Development of the reproductive system of Caenorhabditis elegans. Dev Biol 1976; 49:200-19; PMID:943344; http://dx.doi.org/10.1016/0012-1606(76)90267-0.
26. Hubbard EJ, Greenstein D. The Caenorhabditis elegans gonad: a test tube for cell and developmental biology. Dev Dyn 2000; 218:2-22; PMID:10822256; http://dx.doi.org/10.1002/(SICI)1097-0177(200005)218:1〈2::AID-DVDY2〉3. 0.CO;2-W.
27. Kawasaki I, Shim YH, Kirchner J, Kaminker J, Wood WB, Strome S. PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 1998; 94:635-45; PMID:9741628; http://dx.doi.org/10.1016/S0092- 8674(00)81605-0.
28. Fantes P. Epistatic gene interactions in the control of division in fission yeast. Nature 1979; 279:428-30; PMID:16068179; http://dx.doi.org/10. 1038/279428a0.
29. Maeda I, Kohara Y, Yamamoto M, Sugimoto A. Largescale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol 2001; 11:171-6; PMID:11231151; http://dx.doi.org/10.1016/S0960-9822(01)00052-5.
30. Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S, Timmons L, et al. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 2001; 107:465-76; PMID:11719187; http://dx.doi.org/10.1016/S0092-8674(01)00576-1.
31. Burrows AE, Sceurman BK, Kosinski ME, Richie CT, Sadler PL, Schumacher JM, et al. The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 2006; 133:697-709; PMID:16421191; http://dx.doi.org/10.1242/dev.02241.
32. Koff A, Cross F, Fisher A, Schumacher J, Leguellec K, Philippe M, et al. Human cyclin E, a new cyclin that interacts with two members of the Cdc2 gene family. Cell 1991; 66:1217-28; PMID:1833068; http://dx.doi.org/10.1016/0092- 8674(91)90044-Y.
33. 1/S phase transition. Nat Cell Biol 2005; 7:831-6; PMID:16007079; http://dx.doi.org/10.1038/ncb1284.
34. Barrière C, Santamaría D, Cerqueira A, Galán J, Martín A, Ortega S, et al. Mice thrive without Cdk4 and Cdk2. Mol Oncol 2007; 1:72-83; PMID:19383288; http://dx.doi.org/10.1016/j.molonc.2007.03.001.
35. Santamaría D, Barrière C, Cerqueira A, Hunt S, Tardy C, Newton K, et al. Cdk1 is sufficient to drive the mammalian cell cycle. Nature 2007; 448:811-5; PMID:17700700; http://dx.doi.org/10.1038/nature06046.
36. 2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997; 106:348-60; PMID:9362543; http://dx.doi.org/10.1007/s004120050256.
37. Morgan DE, Crittenden SL, Kimble J. The C. elegans adult male germline: stem cells and sexual dimorphism. Dev Biol 2010; 346:204-14; PMID:20659446; http://dx.doi.org/10.1016/j.ydbio.2010.07.022.
38. Ito K, McGhee JD. Parental DNA strands segregate randomly during embryonic development of Caenorhabditis elegans. Cell 1987; 49:329-36; PMID:3568128; http://dx.doi.org/10.1016/0092-8674(87)90285-6.
39. Kimble J, Hirsh D. The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol 1979; 70:396-417; PMID:478167; http://dx.doi.org/10.1016/0012-1606(79)90035-6.
40. Bao Z, Zhao Z, Boyle TJ, Murray JI, Waterston RH. Control of cell cycle timing during C. elegans embryogenesis. Dev Biol 2008; 318:65-72; PMID:18430415; http://dx.doi.org/10.1016/j.ydbio.2008.02.054.
41. + protein kinase regulates entry into mitosis. Nature 1989; 342:39-45; PMID:2682257; http://dx.doi.org/10.1038/342039a0.
42. Morla AO, Draetta G, Beach D, Wang JY. Reversible tyrosine phosphorylation of Cdc2: dephosphorylation accompanies activation during entry into mitosis. Cell 1989; 58:193-203; PMID:2473839; http://dx.doi.org/10.1016/ 0092-8674(89)90415-7.
43. Den Haese GJ, Walworth N, Carr AM, Gould KL. The Wee1 protein kinase regulates T14 phosphorylation of fission yeast Cdc2. Mol Biol Cell 1995; 6:371-85; PMID:7626804.
44. 2/M transitions of the cell cycle: identification of major phosphorylation sites. EMBO J 1991; 10:305-16; PMID:1846803.
45. Cdc2 protein kinase in vertebrates. EMBO J 1991; 10:3321-9; PMID:1655417.
46. Cdc2. Cell 1991; 67:197-211; PMID:1913817; http://dx.doi.org/10.1016/0092-8674(91)90583-K.
47. Cdc2/cyclin B complex in vitro by human Cdc25 protein. Nature 1991; 351:242-5; PMID:1828290; http://dx.doi.org/10.1038/351242a0.
48. Cdc2. Mol Biol Cell 1992; 3:73-84; PMID:1312880.
49. Boxem M, Srinivasan DG, van den Heuvel S. The Caenorhabditis elegans gene ncc-1 encodes a Cdc2-related kinase required for M phase in meiotic and mitotic cell divisions, but not for S phase. Development 1999; 126:2227-39; PMID:10207147.
50. Updike DL, Strome S. A genomewide RNAi screen for genes that affect the stability, distribution and function of P granules in Caenorhabditis elegans. Genetics 2009; 183:1397-419; PMID:19805813; http://dx.doi.org/10.1534/genetics. 109.110171.
51. van der Voet M, Lorson MA, Srinivasan DG, Bennett KL, van den Heuvel S. C. elegans mitotic cyclins have distinct as well as overlapping functions in chromosome segregation. Cell Cycle 2009; 8:4091-102; PMID:19829076; http://dx.doi.org/10.4161/cc.8.24.10171.
52. Malumbres M, Sotillo R, Santamaría D, Galán J, Cerezo A, Ortega S, et al. Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Cell 2004; 118:493-504; PMID:15315761; http://dx.doi.org/10.1016/j.cell.2004.08.002.
53. Berthet C, Aleem E, Coppola V, Tessarollo L, Kaldis P. Cdk2 knockout mice are viable. Curr Biol 2003; 13:1775-85; PMID:14561402; http://dx.doi.org/10. 1016/j.cub.2003.09.024.
54. Ortega S, Prieto I, Odajima J, Martín A, Dubus P, Sotillo R, et al. Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat Genet 2003; 35:25-31; PMID:12923533; http://dx.doi.org/10. 1038/ng1232.
55. Kosti I, Roy R. Organ-specific cell division abnormalities caused by mutation in a general cell cycle regulator in C. elegans. Development 2002; 129:2155-65; PMID:11959825.
56. 1/S transition. EMBO J 1994; 13:4302-10; PMID:7523110.
57. Jinno S, Suto K, Nagata A, Igarashi M, Kanaoka Y, Nojima H, et al. Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J 1994; 13:1549-56; PMID:8156993.
58. Blomberg I, Hoffmann I. Ectopic expression of Cdc25A accelerates the G(1)/S transition and leads to premature activation of cyclin E- and cyclin A-dependent kinases. Mol Cell Biol 1999; 19:6183-94; PMID:10454565.
59. Millar JB, Blevitt J, Gerace L, Sadhu K, Featherstone C, Russell P. p55Cdc25 is a nuclear protein required for the initiation of mitosis in human cells. Proc Natl Acad Sci USA 1991; 88:10500-4; PMID:1961714; http://dx.doi.org/10.1073/pnas.88.23.10500.
60. Seki T, Yamashita K, Nishitani H, Takagi T, Russell P, Nishimoto T. Chromosome condensation caused by loss of RCC1 function requires the Cdc25C protein that is located in the cytoplasm. Mol Biol Cell 1992; 3:1373-88; PMID:1337289.
61. Gabrielli BG, De Souza CP, Tonks ID, Clark JM, Hayward NK, Ellem KA. Cytoplasmic accumulation of Cdc25B phosphatase in mitosis triggers centrosomal microtubule nucleation in HeLa cells. J Cell Sci 1996; 109:1081-93; PMID:8743955.
62. 2/M phase transition in human cells. J Cell Sci 1998; 111:2445-53; PMID:9683638.
63. Garner-Hamrick PA, Fisher C. Antisense phosphorothioate oligonucleotides specifically downregulate Cdc25B causing S-phase delay and persistent antiproliferative effects. Int J Cancer 1998; 76:720-8; PMID:9610732; http://dx.doi.org/10.1002/(SICI)1097-0215(19980529)76:5〈720:: AIDIJC18〉3.0.CO;2-7.
64. Mailand N, Podtelejnikov AV, Groth A, Mann M, Bartek J, Lukas J. Regulation of G(2)/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J 2002; 21:5911-20; PMID:12411508; http://dx.doi.org/10.1093/emboj/cdf567.
65. Turowski P, Franckhauser C, Morris MC, Vaglio P, Fernandez A, Lamb NJ. Functional Cdc25C dualspecificity phosphatase is required for S-phase entry in human cells. Mol Biol Cell 2003; 14:2984-98; PMID:12857880; http://dx.doi.org/ 10.1091/mbc.E02-08-0515.
66. Lindqvist A, Källström H, Lundgren A, Barsoum E, Rosenthal CK. Cdc25B cooperates with Cdc25A to induce mitosis but has a unique role in activating cyclin B1-Cdk1 at the centrosome. J Cell Biol 2005; 171:35-45; PMID:16216921; http://dx.doi.org/10.1083/jcb.200503066.
67. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974; 77:71-94; PMID:4366476.
68. Lee SJ, Gartner A, Hyun M, Ahn B, Koo HS. The Caenorhabditis elegans Werner syndrome protein functions upstream of ATR and ATM in response to DNA replication inhibition and double-strand DNA breaks. PLoS Genet 2010; 6:1000801; PMID:20062519; http://dx.doi.org/10.1371/journal.pgen.1000801.
69. Crittenden SL, Leonhard KA, Byrd DT, Kimble J. Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line. Mol Biol Cell 2006; 17:3051-61; PMID:16672375; http://dx.doi.org/10.1091/mbc.E06-03-0170.