The C. elegans anaphase promoting complex and MBK-2/DYRK kinase act redundantly with CUL-3/MEL-26 ubiquitin ligase to degrade MEI-1 microtubule-severing activity after meiosis

Developmental Biology

Volumn 302, Issue 2, 2007, Pages 438-447

  Lu, Chenggang ^a   Mains, Paul E ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Anaphase Promoting Complex (APC); C. elegans; DYRK kinase; Meiosis; Protein degradation; Ubiquitin E3 ligase

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CAENORHABDITIS ELEGANS PROTEIN; DYRK PROTEIN; MBK 2 PROTEIN; MEI 1 PROTEIN; MEL 26 PROTEIN; MUTANT PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CAENORHABDITIS ELEGANS; GASTRULATION; HATCHING; LETHALITY; MEIOSIS; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION;

CAENORHABDITIS ELEGANS;

EID: 33846799159     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.09.053     Document Type: Article

References (36)

1. Albertson D.G. Formation of the first cleavage spindle in nematode embryos. Dev. Biol. 101 (1984) 61-72
2. Albertson D.G., and Thomson J.N. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1 (1993) 15-26
3. Bowerman B., and Kurz T. Degrade to create: developmental requirements for ubiquitin-mediated proteolysis during early C. elegans embryogenesis. Development 133 (2006) 773-784
4. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
5. Clark-Maguire S., and Mains P.E. Localization of the mei-1 gene product of Caenorhabditis elegans, a meiotic-specific spindle component. J. Cell Biol. 126 (1994) 199-209
6. DeRenzo C., and Seydoux G. A clean start: degradation of maternal proteins at the oocyte-to-embryo transition. Trends Cell Biol. 14 (2004) 420-426
7. Deshaies R.J. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15 (1999) 435-467
8. Dow M.R., and Mains P.E. Genetic and molecular characterization of the Caenorhabditis elegans gene, mel-26, a postmeiotic negative regulator of mei-1, a meiotic-specific spindle component. Genetics 150 (1998) 119-128
9. Furukawa M., He Y.J., Borchers C., and Xiong Y. Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases. Nat. Cell Biol. 5 (2003) 1001-1007
10. Gengyo-Ando K., and Mitani S. Characterization of mutations induced by ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 269 (2000) 64-69
11. Glickman M.H., and Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82 (2002) 373-428
12. Golden A., Sadler P.L., Wallenfang M.R., Schumacher J.M., Hamill D.R., Bates G., Bowerman B., Seydoux G., and Shakes D.C. Metaphase to anaphase (mat) transition-defective mutants in Caenorhabditis elegans. J. Cell Biol. 151 (2000) 1469-1482
13. Harper J.W. A phosphorylation-driven ubiquitination switch for cell-cycle control. Trends Cell Biol. 12 (2002) 104-107
14. Harper J.W., Burton J.L., and Solomon M.J. The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 16 (2002) 2179-2206
15. Hartman J.J., Mahr J., McNally K., Okawa K., Iwamatsu A., Thomas S., Cheesman S., Heuser J., Vale R.D., and McNally F.J. Katanin, a microtubule-severing protein, is a novel AAA ATPase that targets to the centrosome using a WD40-containing subunit. Cell 93 (1998) 277-287
16. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., and Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421 (2003) 231-237
17. Kemphues K.J., Wolf N., Wood W.B., and Hirsh D. Two loci required for cytoplasmic organization in early embryos of Caenorhabditis elegans. Dev. Biol. 113 (1986) 449-460
18. Kipreos E.T. Ubiquitin-mediated pathways in C. elegans. In: Community T.C.e.R. (Ed). WormBook (2005). http://www.wormbook.org www.wormbook.org
19. Kurz T., Pintard L., Willis J.H., Hamill D.R., Gonczy P., Peter M., and Bowerman B. Cytoskeletal regulation by the Nedd8 ubiquitin-like protein modification pathway. Science 295 (2002) 1294-1298
20. Li S., Armstrong C.M., Bertin N., Ge H., Milstein S., Boxem M., Vidalain P.O., Han J.D., Chesneau A., Hao T., Goldberg D.S., Li N., Martinez M., Rual J.F., Lamesch P., Xu L., Tewari M., Wong S.L., Zhang L.V., Berriz G.F., Jacotot L., Vaglio P., Reboul J., Hirozane-Kishikawa T., Li Q., Gabel H.W., Elewa A., Baumgartner B., Rose D.J., Yu H., Bosak S., Sequerra R., Fraser A., Mango S.E., Saxton W.M., Strome S., Van Den Heuvel S., Piano F., Vandenhaute J., Sardet C., Gerstein M., Doucette-Stamm L., Gunsalus K.C., Harper J.W., Cusick M.E., Roth F.P., Hill D.E., and Vidal M. A map of the interactome network of the metazoan C. elegans. Science 303 (2004) 540-543
21. Lu C., Srayko M., and Mains P.E. The Caenorhabditis elegans Microtubule-severing Complex MEI-1/MEI-2 katanin interacts differently with two superficially redundant beta-tubulin isotypes. Mol. Biol Cell. 15 (2004) 142-150
22. Mains P.E., Kemphues K.J., Sprunger S.A., Sulston I.A., and Wood W.B. Mutations affecting the meiotic and mitotic divisions of the early Caenorhabditis elegans embryo. Genetics 126 (1990) 593-605
23. Mains P.E., Sulston I.A., and Wood W.B. Dominant maternal-effect mutations causing embryonic lethality in Caenorhabditis elegans. Genetics 125 (1990) 351-369
24. McCarter J., Bartlett B., Dang T., and Schedl T. On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 205 (1999) 111-128
25. Ming Pang K., Ishidate T., Nakamura K., Shirayama M., Trzepacz C., Schubert C.M., Priess J.R., and Mello C.C. The minibrain kinase homolog, mbk-2, is required for spindle positioning and asymmetric cell division in early C. elegans embryos. Dev. Biol. 265 (2004) 127-139
26. Pellettieri J., Reinke V., Kim S.K., and Seydoux G. Coordinate activation of maternal protein degradation during the Egg-to-Embryo Transition in C. elegans. Dev. Cell 5 (2003) 451-462
27. Pintard L., Willis J.H., Willems A., Johnson J.L., Srayko M., Kurz T., Glaser S., Mains P.E., Tyers M., Bowerman B., and Peter M. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425 (2003) 311-316
28. Quintin S., Mains P.E., Zinke A., and Hyman A.A. The mbk-2 kinase is required for inactivation of MEI-1/katanin in the one-cell Caenorhabditis elegans embryo. EMBO Rep. 4 (2003) 1175-1181
29. Raich W.B., Moorman C., Lacefield C.O., Lehrer J., Bartsch D., Plasterk R.H., Kandel E.R., and Hobert O. Characterization of Caenorhabditis elegans homologs of the down syndrome candidate gene DYRK1A. Genetics 163 (2003) 571-580
30. Shakes D.C., Sadler P.L., Schumacher J.M., Abdolrasulnia M., and Golden A. Developmental defects observed in hypomorphic anaphase-promoting complex mutants are linked to cell cycle abnormalities. Development 130 (2003) 1605-1620
31. Shirayama M., Soto M.C., Ishidate T., Kim S., Nakamura K., Bei Y., van den Heuvel S., and Mello C.C. The conserved kinases CDK-1, GSK-3, KIN-19, and MBK-2 promote OMA-1 destruction to regulate the oocyte-to-embryo transition in C. elegans. Curr. Biol. 16 (2006) 47-55
32. Srayko M., Buster D.W., Bazirgan O.A., McNally F.J., and Mains P.E. MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes Dev. 14 (2000) 1072-1084
33. Stitzel M.L., Pellettieri J., and Seydoux G. The C. elegans DYRK kinase MBK-2 marks oocyte proteins for degradation in response to meiotic maturation. Curr. Biol. 16 (2006) 56-62
34. Vodermaier H.C. APC/C and SCF: controlling each other and the cell cycle. Curr. Biol. 14 (2004) R787-R796
35. Xu L., Wei Y., Reboul J., Vaglio P., Shin T.H., Vidal M., Elledge S.J., and Harper J.W. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425 (2003) 316-321
36. Yang H., McNally K., and McNally F.J. MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C. elegans. Dev. Biol. 260 (2003) 245-259