Genome-wide analysis of germ cell proliferation in C. elegans identifies VRK-1 as a key regulator of CEP-1/p53

Developmental Biology

Volumn 344, Issue 2, 2010, Pages 1011-1025

  Waters, Katherine ^a   Yang, Alison Z ^a   Reinke, Valerie ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

C. elegans; Germ cells; Kinase; P53; Proliferation; VRK 1

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; PROTEIN KINASE; PROTEIN P53; PROTEIN VRK 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; DNA MICROARRAY; FUNCTIONAL GENOMICS; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GERM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS;

EID: 77955272277     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.06.022     Document Type: Article

References (39)

1. Aggarwal B.D., Calvi B.R. Chromatin regulates origin activity in Drosophila follicle cells. Nature 2004, 430:372-376.
2. Aladjem M.I., Spike B.T., Rodewald L.W., Hope T.J., Klemm M., Jaenisch R., Wahl G.M. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr. Biol. 1998, 8:145-155.
3. Berry L.W., Westlund B., Schedl T. Germ-line tumor formation caused by activation of glp-1, a Caenorhabditis elegans member of the Notch family of receptors. Development 1997, 124:925-936.
4. Boehme K.A., Blattner C. Regulation of p53-insights into a complex process. Crit. Rev. Biochem. Mol. Biol. 2009, 44:367-392.
5. Bosl G.J., Motzer R.J. Testicular germ-cell cancer. N Engl J. Med. 1997, 337:242-253.
6. Brauchle M., Baumer K., Gonczy P. Differential activation of the DNA replication checkpoint contributes to asynchrony of cell division in C. elegans embryos. Curr. Biol. 2003, 13:819-827.
7. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
8. Byrd D.T., Kimble J. Scratching the niche that controls Caenorhabditis elegans germline stem cells. Semin. Cell Dev. Biol. 2009, 20:1107-1113.
9. Chi W., Reinke V. Promotion of oogenesis and embryogenesis in the C. elegans gonad by EFL-1/DPL-1 (E2F) does not require LIN-35 (pRB). Development 2006, 133:3147-3157.
10. Crittenden S.L., Eckmann C.R., Wang L., Bernstein D.S., Wickens M., Kimble J. Regulation of the mitosis/meiosis decision in the Caenorhabditis elegans germline. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358:1359-1362.
11. Crittenden S.L., Leonhard K.A., Byrd D.T., Kimble J. Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line. Mol. Biol. Cell 2006, 17:3051-3061.
12. Cullen C.F., Brittle A.L., Ito T., Ohkura H. The conserved kinase NHK-1 is essential for mitotic progression and unifying acentrosomal meiotic spindles in Drosophila melanogaster. J. Cell Biol. 2005, 171:593-602.
13. Derry W.B., Putzke A.P., Rothman J.H. Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 2001, 294:591-595.
14. Derry W.B., Bierings R., van Iersel M., Satkunendran T., Reinke V., Rothman J.H. Regulation of developmental rate and germ cell proliferation in Caenorhabditis elegans by the p53 gene network. Cell Death Differ. 2007, 14:662-670.
15. Giono L.E., Manfredi J.J. The p53 tumor suppressor participates in multiple cell cycle checkpoints. J. Cell. Physiol. 2006, 209:13-20.
16. Golden A., Sadler P.L., Wallenfang M.R., Schumacher J.M., Hamill D.R., Bates G., Bowerman B., Seydoux G., Shakes D.C. Metaphase to anaphase (mat) transition-defective mutants in Caenorhabditis elegans. J. Cell Biol. 2000, 151:1469-1482.
17. Gorjanacz M., Klerkx E.P., Galy V., Santarella R., Lopez-Iglesias C., Askjaer P., Mattaj I.W. Caenorhabditis elegans BAF-1 and its kinase VRK-1 participate directly in post-mitotic nuclear envelope assembly. EMBO J. 2007, 26:132-143.
18. Gumienny T.L., Lambie E., Hartwieg E., Horvitz H.R., Hengartner M.O. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 1999, 126:1011-1022.
19. Hagstrom K.A., Holmes V.F., Cozzarelli N.R., Meyer B.J. C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev. 2002, 16:729-742.
20. Ivanovska I., Khandan T., Ito T., Orr-Weaver T.L. A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes. Genes Dev. 2005, 19:2571-2582.
21. Jaramillo-Lambert A., Ellefson M., Villeneuve A.M., Engebrecht J. Differential timing of S phases, X chromosomal replication, and meiotic prophase in the C. elegans germ line. Dev. Biol. 2007, 308:206-221.
22. Killian D.J., Hubbard E.J. C. elegans pro-1 activity is required for soma/germline interactions that influence proliferation and differentiation in the germ line. Development 2004, 131:1267-1278.
23. Klerkx E.P., Alarcon P., Waters K., Reinke V., Sternberg P.W., Askjaer P. Protein kinase VRK-1 regulates cell invasion and EGL-17/FGF signaling in Caenorhabditis elegans. Dev. Biol. 2009, 335:12-21.
24. Kudron M.M., Reinke V. C. elegans nucleostemin is required for larval growth and germline stem cell division. PLoS Genet. 2008, 4:e1000181.
25. Lopez-Borges S., Lazo P.A. The human vaccinia-related kinase 1 (VRK1) phosphorylates threonine-18 within the mdm-2 binding site of the p53 tumour suppressor protein. Oncogene 2000, 19:3656-3664.
26. Maciejowski J., Ugel N., Mishra B., Isopi M., Hubbard E.J.A. Quantitative analysis of germline mitosis in adult C. elegans. Dev. Biol. 2006, 292:142-151.
27. Maeda I., Kohara Y., Yamamoto M., Sugimoto A. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 2001, 11:171-176.
28. Petcherski A.G., Kimble J. LAG-3 is a putative transcriptional activator in the C. elegans Notch pathway. Nature 2000, 405:364-368.
29. Pintard L., Willis J.H., Willems A., Johnson J.L., Srayko M., Kurz T., Glaser S., Mains P.E., Tyers M., Bowerman B., et al. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 2003, 425:311-316.
30. Praitis V., Casey E., Collar D., Austin J. Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 2001, 157:1217-1226.
31. Reinke V., Gil I.S., Ward S., Kazmer K. Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 2004, 131:311-323.
32. Schumacher B., Hanazawa M., Lee M.H., Nayak S., Volkmann K., Hofmann E.R., Hengartner M., Schedl T., Gartner A. Translational repression of C. elegans p53 by GLD-1 regulates DNA damage-induced apoptosis. Cell 2005, 120:357-368.
33. Seydoux G., Dunn M.A. Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. Development 1997, 124:2191-2201.
34. Srinivasan D.G., Fisk R.M., Xu H., van den Heuvel S. A complex of LIN-5 and GPR proteins regulates G protein signaling and spindle function in C elegans. Genes Dev. 2003, 17:1225-1239.
35. Strome S., Wood W.B. Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 1982, 79:1558-1562.
36. Subramaniam K., Seydoux G. nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development 1999, 126:4861-4871.
37. Voutev R., Killian D.J., Ahn J.H., Hubbard E.J. Alterations in ribosome biogenesis cause specific defects in C. elegans hermaphrodite gonadogenesis. Dev. Biol. 2006, 298:45-58.
38. Xu L., Wei Y., Reboul J., Vaglio P., Shin T.H., Vidal M., Elledge S.J., Harper J.W. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 2003, 425:316-321.
39. Zhang B., Gallegos M., Puoti A., Durkin E., Fields S., Kimble J., Wickens M.P. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 1997, 390:477-484.