CRL2LRR-1 E3-Ligase Regulates Proliferation and Progression through Meiosis in the Caenorhabditis elegans Germline

PLoS Genetics

Volumn 9, Issue 3, 2013, Pages

  Burger, Julien ^a   Merlet, Jorge ^a   Tavernier, Nicolas ^a   Richaudeau, Bénédicte ^a   Arnold, Andreas ^b   Ciosk, Rafal ^b   Bowerman, Bruce ^c   Pintard, Lionel ^a  

^a INSTITUT JACQUES MONOD   (France)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^c UNIVERSITY OF OREGON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATL 1 PROTEIN; CELL PROTEIN; CUL 2 PROTEIN; CUL2 RING E3 UBIQUITIN LIGASE; HTP 3 PROTEIN; LRR 1 PROTEIN; REGULATOR PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ATL 1 PROTEIN, C ELEGANS; ATL-1 PROTEIN, C ELEGANS; CAENORHABDITIS ELEGANS PROTEIN; CELL CYCLE PROTEIN; CULLIN; CULLIN 2 PROTEIN, C ELEGANS; CULLIN-2 PROTEIN, C ELEGANS; HTP 3 PROTEIN, C ELEGANS; HTP-3 PROTEIN, C ELEGANS; PHOSPHOTRANSFERASE;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL PROLIFERATION; CHROMOSOME; CONTROLLED STUDY; CUL 2 GENE; DNA REPLICATION; GENE MUTATION; GERM LINE; MEIOSIS; NONHUMAN; PROPHASE; REGULATORY MECHANISM; ANIMAL; CELL CYCLE; CYTOLOGY; GENETICS; GERM CELL; METABOLISM; MITOSIS; SYNAPTONEMAL COMPLEX;

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CELL PROLIFERATION; CULLIN PROTEINS; DNA REPLICATION; GERM CELLS; MEIOSIS; MITOSIS; PHOSPHOTRANSFERASES; SYNAPTONEMAL COMPLEX;

MLCS; MLOWN;

EID: 84875982100     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003375     Document Type: Article

References (64)

1. Hershko A, Ciechanover A, (1998) The ubiquitin system. Annu Rev Biochem 67: 425-479.
2. Shabek N, Ciechanover A, (2010) Degradation of ubiquitin: the fate of the cellular reaper. Cell Cycle 9: 523-530.
3. Hershko A, Heller H, Elias S, Ciechanover A, (1983) Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J Biol Chem 258: 8206-8214.
4. Welcker M, Clurman BE, (2008) FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 8: 83-93.
5. Frescas D, Pagano M, (2008) Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat Rev Cancer 8: 438-449.
6. Lee J, Zhou P, (2012) Pathogenic Role of the CRL4 Ubiquitin Ligase in Human Disease. Front Oncol 2: 21.
7. Ye Y, Rape M, (2009) Building ubiquitin chains: E2 enzymes at work. Nat Rev Mol Cell Biol 10: 755-764.
8. Chau V, Tobias JW, Bachmair A, Marriott D, Ecker DJ, et al. (1989) A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243: 1576-1583.
9. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM, (2000) Recognition of the polyubiquitin proteolytic signal. EMBO J 19: 94-102.
10. Glotzer M, Murray AW, Kirschner MW, (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349: 132-138.
11. Jin L, Williamson A, Banerjee S, Philipp I, Rape M, (2008) Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 133: 653-665.
12. Mocciaro A, Rape M, (2012) Emerging regulatory mechanisms in ubiquitin-dependent cell cycle control. J Cell Sci 125: 255-263.
13. Deshaies RJ, Joazeiro CA, (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78: 399-434.
14. Sarikas A, Hartmann T, Pan ZQ, (2011) The cullin protein family. Genome Biol 12: 220.
15. Petroski MD, Deshaies RJ, (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6: 9-20.
16. Merlet J, Burger J, Gomes JE, Pintard L, (2009) Regulation of cullin-RING E3 ubiquitin-ligases by neddylation and dimerization. Cell Mol Life Sci.
17. Okumura F, Matsuzaki M, Nakatsukasa K, Kamura T, (2012) The Role of Elongin BC-Containing Ubiquitin Ligases. Front Oncol 2: 10.
18. Feng H, Zhong W, Punkosdy G, Gu S, Zhou L, et al. (1999) CUL-2 is required for the G1-to-S-phase transition and mitotic chromosome condensation in Caenorhabditis elegans. Nat Cell Biol 1: 486-492.
19. Merlet J, Burger J, Tavernier N, Richaudeau B, Gomes JE, et al. (2010) The CRL2LRR-1 ubiquitin ligase regulates cell cycle progression during C. elegans development. Development 137: 3857-3866.
20. Starostina NG, Simpliciano JM, McGuirk MA, Kipreos ET, (2010) CRL2(LRR-1) targets a CDK inhibitor for cell cycle control in C. elegans and actin-based motility regulation in human cells. Dev Cell 19: 753-764.
21. Sonneville R, Gonczy P, (2004) Zyg-11 and cul-2 regulate progression through meiosis II and polarity establishment in C. elegans. Development 131: 3527-3543.
22. Liu J, Vasudevan S, Kipreos ET, (2004) CUL-2 and ZYG-11 promote meiotic anaphase II and the proper placement of the anterior-posterior axis in C. elegans. Development 131: 3513-3525.
23. DeRenzo C, Reese KJ, Seydoux G, (2003) Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation. Nature 424: 685-689.
24. Encalada SE, Martin PR, Phillips JB, Lyczak R, Hamill DR, et al. (2000) DNA replication defects delay cell division and disrupt cell polarity in early Caenorhabditis elegans embryos. Dev Biol 228: 225-238.
25. Starostina NG, Lim JM, Schvarzstein M, Wells L, Spence AM, et al. (2007) A CUL-2 ubiquitin ligase containing three FEM proteins degrades TRA-1 to regulate C. elegans sex determination. Dev Cell 13: 127-139.
26. Byrd DT, Kimble J, (2009) Scratching the niche that controls Caenorhabditis elegans germline stem cells. Semin Cell Dev Biol 20: 1107-1113.
27. Hansen D, Schedl T, (2006) The regulatory network controlling the proliferation-meiotic entry decision in the Caenorhabditis elegans germ line. Curr Top Dev Biol 76: 185-215.
28. Kimble J, Crittenden SL, (2007) Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu Rev Cell Dev Biol 23: 405-433.
29. Zetka MC, Kawasaki I, Strome S, Muller F, (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev 13: 2258-2270.
30. MacQueen AJ, Villeneuve AM, (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15: 1674-1687.
31. Vasudevan S, Starostina NG, Kipreos ET, (2007) The Caenorhabditis elegans cell-cycle regulator ZYG-11 defines a conserved family of CUL-2 complex components. EMBO Rep 8: 279-286.
32. Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, et al. (2002) A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417: 660-663.
33. Kershner AM, Kimble J, (2010) Genome-wide analysis of mRNA targets for Caenorhabditis elegans FBF, a conserved stem cell regulator. Proc Natl Acad Sci U S A 107: 3936-3941.
34. Qiao L, Lissemore JL, Shu P, Smardon A, Gelber MB, et al. (1995) Enhancers of glp-1, a gene required for cell-signaling in Caenorhabditis elegans, define a set of genes required for germline development. Genetics 141: 551-569.
35. Penkner AM, Fridkin A, Gloggnitzer J, Baudrimont A, Machacek T, et al. (2009) Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139: 920-933.
36. Holway AH, Hung C, Michael WM, (2005) Systematic, RNA-interference-mediated identification of mus-101 modifier genes in Caenorhabditis elegans. Genetics 169: 1451-1460.
37. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, et al. (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123: 1037-1050.
38. Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, et al. (2008) HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 14: 263-274.
39. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM, (2002) Synapsis-dependent and-independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16: 2428-2442.
40. Aravind L, Koonin EV, (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 23: 284-286.
41. Severson AF, Ling L, van Zuylen V, Meyer BJ, (2009) The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev 23: 1763-1778.
42. Couteau F, Zetka M, (2011) DNA damage during meiosis induces chromatin remodeling and synaptonemal complex disassembly. Dev Cell 20: 353-363.
43. Hayashi M, Chin GM, Villeneuve AM, (2007) C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet 3: e191 doi:10.1371/journal.pgen.0030191.
44. Austin J, Kimble J, (1987) glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51: 589-599.
45. Kadyk LC, Kimble J, (1998) Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125: 1803-1813.
46. Hansen D, Hubbard EJ, Schedl T, (2004) Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev Biol 268: 342-357.
47. Fox PM, Vought VE, Hanazawa M, Lee MH, Maine EM, et al. (2011) Cyclin E and CDK-2 regulate proliferative cell fate and cell cycle progression in the C. elegans germline. Development 138: 2223-2234.
48. Kurz T, Pintard L, Willis JH, Hamill DR, Gonczy P, et al. (2002) Cytoskeletal regulation by the Nedd8 ubiquitin-like protein modification pathway. Science 295: 1294-1298.
49. Kulkarni M, Smith HE, (2008) E1 ubiquitin-activating enzyme UBA-1 plays multiple roles throughout C. elegans development. PLoS Genet 4: e1000131 doi:10.1371/journal.pgen.1000131.
50. Macdonald LD, Knox A, Hansen D, (2008) Proteasomal regulation of the proliferation vs. meiotic entry decision in the Caenorhabditis elegans germ line. Genetics 180: 905-920.
51. Merritt C, Seydoux G, (2010) The Puf RNA-binding proteins FBF-1 and FBF-2 inhibit the expression of synaptonemal complex proteins in germline stem cells. Development 137: 1787-1798.
52. Jeong J, Verheyden JM, Kimble J, (2011) Cyclin E and Cdk2 control GLD-1, the mitosis/meiosis decision, and germline stem cells in Caenorhabditis elegans. PLoS Genet 7: e1001348 doi:10.1371/journal.pgen.1001348.
53. Biedermann B, Wright J, Senften M, Kalchhauser I, Sarathy G, et al. (2009) Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis. Dev Cell 17: 355-364.
54. Kalchhauser I, Farley BM, Pauli S, Ryder SP, Ciosk R, (2011) FBF represses the Cip/Kip cell-cycle inhibitor CKI-2 to promote self-renewal of germline stem cells in C. elegans. EMBO J 30: 3823-3829.
55. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
56. Garcia-Muse T, Boulton SJ, (2005) Distinct modes of ATR activation after replication stress and DNA double-strand breaks in Caenorhabditis elegans. EMBO J 24: 4345-4355.
57. Eckmann CR, Crittenden SL, Suh N, Kimble J, (2004) GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168: 147-160.
58. Lamont LB, Crittenden SL, Bernstein D, Wickens M, Kimble J, (2004) FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev Cell 7: 697-707.
59. Fay D, Bender A, (2008) SNPs: introduction and two-point mapping. Worm Book pp. 1-10.
60. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, et al. (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408: 325-330.
61. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
62. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J, (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2: RESEARCH0002 doi:10.1186/gb-2000-2-1-research0002.
63. Sasagawa Y, Otani M, Higashitani N, Higashitani A, Sato K, et al. (2009) Caenorhabditis elegans p97 controls germline-specific sex determination by controlling the TRA-1 level in a CUL-2-dependent manner. J Cell Sci 122: 3663-3672.
64. Luke-Glaser S, Roy M, Larsen B, Le Bihan T, Metalnikov P, et al. (2007) CIF-1, a shared subunit of the COP9/signalosome and eukaryotic initiation factor 3 complexes, regulates MEL-26 levels in the Caenorhabditis elegans embryo. Mol Cell Biol 27: 4526-4540.