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. 2002 Feb;160(2):805–813. doi: 10.1093/genetics/160.2.805

Multiple subunits of the Caenorhabditis elegans anaphase-promoting complex are required for chromosome segregation during meiosis I.

Edward S Davis 1, Lucia Wille 1, Barry A Chestnut 1, Penny L Sadler 1, Diane C Shakes 1, Andy Golden 1
PMCID: PMC1461975  PMID: 11861581

Abstract

Two genes, originally identified in genetic screens for Caenorhabditis elegans mutants that arrest in metaphase of meiosis I, prove to encode subunits of the anaphase-promoting complex or cyclosome (APC/C). RNA interference studies reveal that these and other APC/C subunits are essential for the segregation of chromosomal homologs during meiosis I. Further, chromosome segregation during meiosis I requires APC/C functions in addition to the release of sister chromatid cohesion.

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Selected References

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  1. Albertson D. G., Thomson J. N. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1993 May;1(1):15–26. doi: 10.1007/BF00710603. [DOI] [PubMed] [Google Scholar]
  2. Blatch G. L., Lässle M. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays. 1999 Nov;21(11):932–939. doi: 10.1002/(SICI)1521-1878(199911)21:11<932::AID-BIES5>3.0.CO;2-N. [DOI] [PubMed] [Google Scholar]
  3. Blose S. H., Meltzer D. I., Feramisco J. R. 10-nm filaments are induced to collapse in living cells microinjected with monoclonal and polyclonal antibodies against tubulin. J Cell Biol. 1984 Mar;98(3):847–858. doi: 10.1083/jcb.98.3.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Doi A., Doi K. Cloning and nucleotide sequence of the CDC23 gene of Saccharomyces cerevisiae. Gene. 1990 Jul 2;91(1):123–126. doi: 10.1016/0378-1119(90)90172-n. [DOI] [PubMed] [Google Scholar]
  5. Fire A., Xu S., Montgomery M. K., Kostas S. A., Driver S. E., Mello C. C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998 Feb 19;391(6669):806–811. doi: 10.1038/35888. [DOI] [PubMed] [Google Scholar]
  6. Fraser A. G., Kamath R. S., Zipperlen P., Martinez-Campos M., Sohrmann M., Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature. 2000 Nov 16;408(6810):325–330. doi: 10.1038/35042517. [DOI] [PubMed] [Google Scholar]
  7. Funabiki H., Murray A. W. The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell. 2000 Aug 18;102(4):411–424. doi: 10.1016/s0092-8674(00)00047-7. [DOI] [PubMed] [Google Scholar]
  8. Furuta T., Tuck S., Kirchner J., Koch B., Auty R., Kitagawa R., Rose A. M., Greenstein D. EMB-30: an APC4 homologue required for metaphase-to-anaphase transitions during meiosis and mitosis in Caenorhabditis elegans. Mol Biol Cell. 2000 Apr;11(4):1401–1419. doi: 10.1091/mbc.11.4.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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 Dec 25;151(7):1469–1482. doi: 10.1083/jcb.151.7.1469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Guo S., Kemphues K. J. A non-muscle myosin required for embryonic polarity in Caenorhabditis elegans. Nature. 1996 Aug 1;382(6590):455–458. doi: 10.1038/382455a0. [DOI] [PubMed] [Google Scholar]
  11. Gönczy P., Echeverri C., Oegema K., Coulson A., Jones S. J., Copley R. R., Duperon J., Oegema J., Brehm M., Cassin E. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature. 2000 Nov 16;408(6810):331–336. doi: 10.1038/35042526. [DOI] [PubMed] [Google Scholar]
  12. Kent W. J., Zahler A. M. The intronerator: exploring introns and alternative splicing in Caenorhabditis elegans. Nucleic Acids Res. 2000 Jan 1;28(1):91–93. doi: 10.1093/nar/28.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Krawchuk M. D., DeVeaux L. C., Wahls W. P. Meiotic chromosome dynamics dependent upon the rec8(+), rec10(+) and rec11(+) genes of the fission yeast Schizosaccharomyces pombe. Genetics. 1999 Sep;153(1):57–68. doi: 10.1093/genetics/153.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lamb J. R., Michaud W. A., Sikorski R. S., Hieter P. A. Cdc16p, Cdc23p and Cdc27p form a complex essential for mitosis. EMBO J. 1994 Sep 15;13(18):4321–4328. doi: 10.1002/j.1460-2075.1994.tb06752.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Leverson J. D., Joazeiro C. A., Page A. M., Huang H. k., Hieter P., Hunter T. The APC11 RING-H2 finger mediates E2-dependent ubiquitination. Mol Biol Cell. 2000 Jul;11(7):2315–2325. doi: 10.1091/mbc.11.7.2315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Maeda I., Kohara Y., Yamamoto M., Sugimoto A. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol. 2001 Feb 6;11(3):171–176. doi: 10.1016/s0960-9822(01)00052-5. [DOI] [PubMed] [Google Scholar]
  17. Michaelis C., Ciosk R., Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell. 1997 Oct 3;91(1):35–45. doi: 10.1016/s0092-8674(01)80007-6. [DOI] [PubMed] [Google Scholar]
  18. Molnar M., Bähler J., Sipiczki M., Kohli J. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics. 1995 Sep;141(1):61–73. doi: 10.1093/genetics/141.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nasmyth K. Separating sister chromatids. Trends Biochem Sci. 1999 Mar;24(3):98–104. doi: 10.1016/s0968-0004(99)01358-4. [DOI] [PubMed] [Google Scholar]
  20. Ohta T., Michel J. J., Schottelius A. J., Xiong Y. ROC1, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. Mol Cell. 1999 Apr;3(4):535–541. doi: 10.1016/s1097-2765(00)80482-7. [DOI] [PubMed] [Google Scholar]
  21. Parry D. H., O'Farrell P. H. The schedule of destruction of three mitotic cyclins can dictate the timing of events during exit from mitosis. Curr Biol. 2001 May 1;11(9):671–683. doi: 10.1016/s0960-9822(01)00204-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pasierbek P., Jantsch M., Melcher M., Schleiffer A., Schweizer D., Loidl J. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev. 2001 Jun 1;15(11):1349–1360. doi: 10.1101/gad.192701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Peter M., Castro A., Lorca T., Le Peuch C., Magnaghi-Jaulin L., Dorée M., Labbé J. C. The APC is dispensable for first meiotic anaphase in Xenopus oocytes. Nat Cell Biol. 2001 Jan;3(1):83–87. doi: 10.1038/35050607. [DOI] [PubMed] [Google Scholar]
  24. Peters J. M., King R. W., Hög C., Kirschner M. W. Identification of BIME as a subunit of the anaphase-promoting complex. Science. 1996 Nov 15;274(5290):1199–1201. doi: 10.1126/science.274.5290.1199. [DOI] [PubMed] [Google Scholar]
  25. Seydoux G., Savage C., Greenwald I. Isolation and characterization of mutations causing abnormal eversion of the vulva in Caenorhabditis elegans. Dev Biol. 1993 Jun;157(2):423–436. doi: 10.1006/dbio.1993.1146. [DOI] [PubMed] [Google Scholar]
  26. Sikorski R. S., Michaud W. A., Hieter P. p62cdc23 of Saccharomyces cerevisiae: a nuclear tetratricopeptide repeat protein with two mutable domains. Mol Cell Biol. 1993 Feb;13(2):1212–1221. doi: 10.1128/mcb.13.2.1212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Starborg M., Brundell E., Gell K., Hög C. A novel murine gene encoding a 216-kDa protein is related to a mitotic checkpoint regulator previously identified in Aspergillus nidulans. J Biol Chem. 1994 Sep 30;269(39):24133–24137. [PubMed] [Google Scholar]
  28. Tabara H., Grishok A., Mello C. C. RNAi in C. elegans: soaking in the genome sequence. Science. 1998 Oct 16;282(5388):430–431. doi: 10.1126/science.282.5388.430. [DOI] [PubMed] [Google Scholar]
  29. Taieb F. E., Gross S. D., Lewellyn A. L., Maller J. L. Activation of the anaphase-promoting complex and degradation of cyclin B is not required for progression from Meiosis I to II in Xenopus oocytes. Curr Biol. 2001 Apr 3;11(7):508–513. doi: 10.1016/s0960-9822(01)00145-2. [DOI] [PubMed] [Google Scholar]
  30. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Timmons L., Court D. L., Fire A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene. 2001 Jan 24;263(1-2):103–112. doi: 10.1016/s0378-1119(00)00579-5. [DOI] [PubMed] [Google Scholar]
  32. Uhlmann F., Lottspeich F., Nasmyth K. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature. 1999 Jul 1;400(6739):37–42. doi: 10.1038/21831. [DOI] [PubMed] [Google Scholar]
  33. Yamashita Y. M., Nakaseko Y., Kumada K., Nakagawa T., Yanagida M. Fission yeast APC/cyclosome subunits, Cut20/Apc4 and Cut23/Apc8, in regulating metaphase-anaphase progression and cellular stress responses. Genes Cells. 1999 Aug;4(8):445–463. doi: 10.1046/j.1365-2443.1999.00274.x. [DOI] [PubMed] [Google Scholar]
  34. Yamashita Y. M., Nakaseko Y., Samejima I., Kumada K., Yamada H., Michaelson D., Yanagida M. 20S cyclosome complex formation and proteolytic activity inhibited by the cAMP/PKA pathway. Nature. 1996 Nov 21;384(6606):276–279. doi: 10.1038/384276a0. [DOI] [PubMed] [Google Scholar]
  35. Yu H., Peters J. M., King R. W., Page A. M., Hieter P., Kirschner M. W. Identification of a cullin homology region in a subunit of the anaphase-promoting complex. Science. 1998 Feb 20;279(5354):1219–1222. doi: 10.1126/science.279.5354.1219. [DOI] [PubMed] [Google Scholar]
  36. Zachariae W., Nasmyth K. Whose end is destruction: cell division and the anaphase-promoting complex. Genes Dev. 1999 Aug 15;13(16):2039–2058. doi: 10.1101/gad.13.16.2039. [DOI] [PubMed] [Google Scholar]
  37. Zachariae W., Shevchenko A., Andrews P. D., Ciosk R., Galova M., Stark M. J., Mann M., Nasmyth K. Mass spectrometric analysis of the anaphase-promoting complex from yeast: identification of a subunit related to cullins. Science. 1998 Feb 20;279(5354):1216–1219. doi: 10.1126/science.279.5354.1216. [DOI] [PubMed] [Google Scholar]
  38. Zachariae W., Shin T. H., Galova M., Obermaier B., Nasmyth K. Identification of subunits of the anaphase-promoting complex of Saccharomyces cerevisiae. Science. 1996 Nov 15;274(5290):1201–1204. doi: 10.1126/science.274.5290.1201. [DOI] [PubMed] [Google Scholar]
  39. Zhao N., Lai F., Fernald A. A., Eisenbart J. D., Espinosa R., Wang P. W., Le Beau M. M. Human CDC23: cDNA cloning, mapping to 5q31, genomic structure, and evaluation as a candidate tumor suppressor gene in myeloid leukemias. Genomics. 1998 Oct 15;53(2):184–190. doi: 10.1006/geno.1998.5473. [DOI] [PubMed] [Google Scholar]
  40. Zipperlen P., Fraser A. G., Kamath R. S., Martinez-Campos M., Ahringer J. Roles for 147 embryonic lethal genes on C.elegans chromosome I identified by RNA interference and video microscopy. EMBO J. 2001 Aug 1;20(15):3984–3992. doi: 10.1093/emboj/20.15.3984. [DOI] [PMC free article] [PubMed] [Google Scholar]

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