Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1996 Mar 15;15(6):1451–1459.

Identification of ORD, a Drosophila protein essential for sister chromatid cohesion.

S E Bickel 1, D W Wyman 1, W Y Miyazaki 1, D P Moore 1, T L Orr-Weaver 1
PMCID: PMC450050  PMID: 8635478

Abstract

Attachment between the sister chromatids is required for proper chromosome segregation in meiosis and mitosis, but its molecular basis is not understood. Mutations in the Drosophila ord gene result in premature sister chromatid separation in meiosis, indicating that the product of this gene is necessary for sister chromatid cohesion. We isolated the ord gene and found that it encodes a novel 55 kDa protein. Some of the ord mutations exhibit unusual complementation properties, termed negative complementation, in which particular alleles poison the activity of another allele. Negative complementation predicts that protein-protein interactions are critical for ORD function. The position and nature of these unusual ord mutations demonstrate that the C-terminal half of ORD is essential for sister chromatid cohesion and suggest that it mediates protein binding.

Full text

PDF
1454

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Bankier A. T., Weston K. M., Barrell B. G. Random cloning and sequencing by the M13/dideoxynucleotide chain termination method. Methods Enzymol. 1987;155:51–93. doi: 10.1016/0076-6879(87)55009-1. [DOI] [PubMed] [Google Scholar]
  3. Cavener D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 1987 Feb 25;15(4):1353–1361. doi: 10.1093/nar/15.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chevaillier P. Pest sequences in nuclear proteins. Int J Biochem. 1993 Apr;25(4):479–482. doi: 10.1016/0020-711x(93)90653-v. [DOI] [PubMed] [Google Scholar]
  5. Davis B. K. Genetic analysis of a meiotic mutant resulting in precocious sister-centromere separation in Drosophila melanogaster. Mol Gen Genet. 1971;113(3):251–272. doi: 10.1007/BF00339546. [DOI] [PubMed] [Google Scholar]
  6. Dobson M. J., Pearlman R. E., Karaiskakis A., Spyropoulos B., Moens P. B. Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci. 1994 Oct;107(Pt 10):2749–2760. doi: 10.1242/jcs.107.10.2749. [DOI] [PubMed] [Google Scholar]
  7. Dreesen T. D., Johnson D. H., Henikoff S. The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes. Mol Cell Biol. 1988 Dec;8(12):5206–5215. doi: 10.1128/mcb.8.12.5206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Foster G. G. Negative complementation at the notch locus of Drosophila melanogaster. Genetics. 1975 Sep;81(1):99–120. doi: 10.1093/genetics/81.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Glotzer M., Murray A. W., Kirschner M. W. Cyclin is degraded by the ubiquitin pathway. Nature. 1991 Jan 10;349(6305):132–138. doi: 10.1038/349132a0. [DOI] [PubMed] [Google Scholar]
  10. Goldstein L. S. Mechanisms of chromosome orientation revealed by two meiotic mutants in Drosophila melanogaster. Chromosoma. 1980;78(1):79–111. doi: 10.1007/BF00291909. [DOI] [PubMed] [Google Scholar]
  11. Herskowitz I. Functional inactivation of genes by dominant negative mutations. Nature. 1987 Sep 17;329(6136):219–222. doi: 10.1038/329219a0. [DOI] [PubMed] [Google Scholar]
  12. Holloway S. L., Glotzer M., King R. W., Murray A. W. Anaphase is initiated by proteolysis rather than by the inactivation of maturation-promoting factor. Cell. 1993 Jul 2;73(7):1393–1402. doi: 10.1016/0092-8674(93)90364-v. [DOI] [PubMed] [Google Scholar]
  13. Irniger S., Piatti S., Michaelis C., Nasmyth K. Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell. 1995 Apr 21;81(2):269–278. doi: 10.1016/0092-8674(95)90337-2. [DOI] [PubMed] [Google Scholar]
  14. Kelley M. R., Kidd S., Deutsch W. A., Young M. W. Mutations altering the structure of epidermal growth factor-like coding sequences at the Drosophila Notch locus. Cell. 1987 Nov 20;51(4):539–548. doi: 10.1016/0092-8674(87)90123-1. [DOI] [PubMed] [Google Scholar]
  15. Kerrebrock A. W., Miyazaki W. Y., Birnby D., Orr-Weaver T. L. The Drosophila mei-S332 gene promotes sister-chromatid cohesion in meiosis following kinetochore differentiation. Genetics. 1992 Apr;130(4):827–841. doi: 10.1093/genetics/130.4.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kerrebrock A. W., Moore D. P., Wu J. S., Orr-Weaver T. L. Mei-S332, a Drosophila protein required for sister-chromatid cohesion, can localize to meiotic centromere regions. Cell. 1995 Oct 20;83(2):247–256. doi: 10.1016/0092-8674(95)90166-3. [DOI] [PubMed] [Google Scholar]
  17. King R. W., Peters J. M., Tugendreich S., Rolfe M., Hieter P., Kirschner M. W. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell. 1995 Apr 21;81(2):279–288. doi: 10.1016/0092-8674(95)90338-0. [DOI] [PubMed] [Google Scholar]
  18. Kramer J. M., Johnson J. J., Edgar R. S., Basch C., Roberts S. The sqt-1 gene of C. elegans encodes a collagen critical for organismal morphogenesis. Cell. 1988 Nov 18;55(4):555–565. doi: 10.1016/0092-8674(88)90214-0. [DOI] [PubMed] [Google Scholar]
  19. Kusch M., Edgar R. S. Genetic studies of unusual loci that affect body shape of the nematode Caenorhabditis elegans and may code for cuticle structural proteins. Genetics. 1986 Jul;113(3):621–639. doi: 10.1093/genetics/113.3.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Levis R., Hazelrigg T., Rubin G. M. Effects of genomic position on the expression of transduced copies of the white gene of Drosophila. Science. 1985 Aug 9;229(4713):558–561. doi: 10.1126/science.2992080. [DOI] [PubMed] [Google Scholar]
  21. Lin H. P., Church K. Meiosis in Drosophila melanogaster, III. The effect of orientation disruptor (ord) on gonial mitotic and the meiotic divisions in males. Genetics. 1982 Dec;102(4):751–770. doi: 10.1093/genetics/102.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lin Y., Larson K. L., Dorer R., Smith G. R. Meiotically induced rec7 and rec8 genes of Schizosaccharomyces pombe. Genetics. 1992 Sep;132(1):75–85. doi: 10.1093/genetics/132.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
  24. Maguire M. P., Paredes A. M., Riess R. W. The desynaptic mutant of maize as a combined defect of synaptonemal complex and chiasma maintenance. Genome. 1991 Dec;34(6):879–887. doi: 10.1139/g91-135. [DOI] [PubMed] [Google Scholar]
  25. Maguire M. P., Riess R. W., Paredes A. M. Evidence from a maize desynaptic mutant points to a probable role of synaptonemal complex central region components in provision for subsequent chiasma maintenance. Genome. 1993 Oct;36(5):797–807. doi: 10.1139/g93-105. [DOI] [PubMed] [Google Scholar]
  26. Mason J. M. Orientation disruptor (ord): a recombination-defective and disjunction-defective meiotic mutant in Drosophila melanogaster. Genetics. 1976 Nov;84(3):545–572. doi: 10.1093/genetics/84.3.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miyazaki W. Y., Orr-Weaver T. L. Sister-chromatid cohesion in mitosis and meiosis. Annu Rev Genet. 1994;28:167–187. doi: 10.1146/annurev.ge.28.120194.001123. [DOI] [PubMed] [Google Scholar]
  28. Miyazaki W. Y., Orr-Weaver T. L. Sister-chromatid misbehavior in Drosophila ord mutants. Genetics. 1992 Dec;132(4):1047–1061. doi: 10.1093/genetics/132.4.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Mullins M. C., Rio D. C., Rubin G. M. cis-acting DNA sequence requirements for P-element transposition. Genes Dev. 1989 May;3(5):729–738. doi: 10.1101/gad.3.5.729. [DOI] [PubMed] [Google Scholar]
  31. Muskavitch M. A., Hoffmann F. M. Homologs of vertebrate growth factors in Drosophila melanogaster and other invertebrates. Curr Top Dev Biol. 1990;24:289–328. doi: 10.1016/s0070-2153(08)60091-5. [DOI] [PubMed] [Google Scholar]
  32. Orr-Weaver T. L. Meiosis in Drosophila: seeing is believing. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10443–10449. doi: 10.1073/pnas.92.23.10443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Portin P. Allelic negative complementation at the Abruptex locus of Drosophila melanogaster. Genetics. 1975 Sep;81(1):121–133. doi: 10.1093/genetics/81.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Raz E., Schejter E. D., Shilo B. Z. Interallelic complementation among DER/flb alleles: implications for the mechanism of signal transduction by receptor-tyrosine kinases. Genetics. 1991 Sep;129(1):191–201. doi: 10.1093/genetics/129.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rechsteiner M. Regulation of enzyme levels by proteolysis: the role of pest regions. Adv Enzyme Regul. 1988;27:135–151. doi: 10.1016/0065-2571(88)90014-3. [DOI] [PubMed] [Google Scholar]
  36. Rockmill B., Roeder G. S. Meiosis in asynaptic yeast. Genetics. 1990 Nov;126(3):563–574. doi: 10.1093/genetics/126.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rockmill B., Roeder G. S. RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6057–6061. doi: 10.1073/pnas.85.16.6057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rogers S., Wells R., Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 1986 Oct 17;234(4774):364–368. doi: 10.1126/science.2876518. [DOI] [PubMed] [Google Scholar]
  39. Smith T. F., Waterman M. S. Identification of common molecular subsequences. J Mol Biol. 1981 Mar 25;147(1):195–197. doi: 10.1016/0022-2836(81)90087-5. [DOI] [PubMed] [Google Scholar]
  40. Tamkun J. W., Deuring R., Scott M. P., Kissinger M., Pattatucci A. M., Kaufman T. C., Kennison J. A. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell. 1992 Feb 7;68(3):561–572. doi: 10.1016/0092-8674(92)90191-e. [DOI] [PubMed] [Google Scholar]
  41. Thisse B., el Messal M., Perrin-Schmitt F. The twist gene: isolation of a Drosophila zygotic gene necessary for the establishment of dorsoventral pattern. Nucleic Acids Res. 1987 Apr 24;15(8):3439–3453. doi: 10.1093/nar/15.8.3439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Thompson E. A., Roeder G. S. Expression and DNA sequence of RED1, a gene required for meiosis I chromosome segregation in yeast. Mol Gen Genet. 1989 Aug;218(2):293–301. doi: 10.1007/BF00331281. [DOI] [PubMed] [Google Scholar]
  43. Tugendreich S., Tomkiel J., Earnshaw W., Hieter P. CDC27Hs colocalizes with CDC16Hs to the centrosome and mitotic spindle and is essential for the metaphase to anaphase transition. Cell. 1995 Apr 21;81(2):261–268. doi: 10.1016/0092-8674(95)90336-4. [DOI] [PubMed] [Google Scholar]
  44. Ullrich A., Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell. 1990 Apr 20;61(2):203–212. doi: 10.1016/0092-8674(90)90801-k. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES