The Drosophila mei-S332 Gene Promotes Sister-Chromatid Cohesion in Meiosis Following Kinetochore Differentiation

INVESTIGATIONS

The Drosophila mei-S332 Gene Promotes Sister-Chromatid Cohesion in Meiosis Following Kinetochore Differentiation

A. W. Kerrebrock, W. Y. Miyazaki, D. Birnby and T. L. Orr-Weaver
Whitehead Institute, Cambridge, Massachusetts 02142

The Drosophila mei-S332 gene acts to maintain sister-chromatid cohesion before anaphase II of meiosis in both males and females. By isolating and analyzing seven new alleles and a deficiency uncovering the mei-S332 gene we have demonstrated that the onset of the requirement for mei-S332 is not until late anaphase I. All of our alleles result primarily in equational (meiosis II) nondisjunction with low amounts of reductional (meiosis I) nondisjunction. Cytological analysis revealed that sister chromatids frequently separate in late anaphase I in these mutants. Since the sister chromatids remain associated until late in the first division, chromosomes segregate normally during meiosis I, and the genetic consequences of premature sister-chromatid dissociation are seen as nondisjunction in meiosis II. The late onset of mei-S332 action demonstrated by the mutations was not a consequence of residual gene function because two strong, and possibly null, alleles give predominantly equational nondisjunction both as homozygotes and in trans to a deficiency. mei-S332 is not required until after metaphase I, when the kinetochore differentiates from a single hemispherical kinetochore jointly organized by the sister chromatids into two distinct sister kinetochores. Therefore, we propose that the mei-S322 product acts to hold the doubled kinetochore together until anaphase II. All of the alleles are fully viable when in trans to a deficiency, thus mei-S332 is not essential for mitosis. Four of the alleles show an unexpected sex specificity.

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				A. L. Marston, W.-H. Tham, H. Shah, and A. Amon A Genome-Wide Screen Identifies Genes Required for Centromeric Cohesion Science, February 27, 2004; 303(5662): 1367 - 1370. [Abstract] [Full Text] [PDF]

				E. M. Balicky, M. W. Endres, C. Lai, and S. E. Bickel Meiotic Cohesion Requires Accumulation of ORD on Chromosomes before Condensation Mol. Biol. Cell, November 1, 2002; 13(11): 3890 - 3900. [Abstract] [Full Text] [PDF]

				I. Sumara, E. Vorlaufer, C. Gieffers, B. H. Peters, and J.-M. Peters Characterization of Vertebrate Cohesin Complexes and Their Regulation in Prophase J. Cell Biol., November 13, 2000; 151(4): 749 - 762. [Abstract] [Full Text] [PDF]

				R. V. Skibbens Holding Your Own: Establishing Sister Chromatid Cohesion Genome Res., November 1, 2000; 10(11): 1664 - 1671. [Full Text]

				L. V. Paliulis and R. B. Nicklas The Reduction of Chromosome Number in Meiosis Is Determined by Properties Built into the Chromosomes J. Cell Biol., September 18, 2000; 150(6): 1223 - 1232. [Abstract] [Full Text] [PDF]

				X. Zeng and W. S. Saunders The Saccharomyces cerevisiae Centromere Protein Slk19p Is Required for Two Successive Divisions During Meiosis Genetics, June 1, 2000; 155(2): 577 - 587. [Abstract] [Full Text]

				M. D. Krawchuk, L. C. DeVeaux, and W. P. Wahls Meiotic Chromosome Dynamics Dependent Upon the rec8+, rec10+ and rec11+ Genes of the Fission Yeast Schizosaccharomyces pombe Genetics, September 1, 1999; 153(1): 57 - 68. [Abstract] [Full Text]

				J. Basu, H. Bousbaa, E. Logarinho, Z. Li, B. C. Williams, C. Lopes, C. E. Sunkel, and M. L. Goldberg Mutations in the Essential Spindle Checkpoint Gene bub1 Cause Chromosome Missegregation and Fail to Block Apoptosis in Drosophila J. Cell Biol., July 12, 1999; 146(1): 13 - 28. [Abstract] [Full Text] [PDF]

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				S. Parisi, M. J. McKay, M. Molnar, M. A. Thompson, P. J. van der Spek, E. van Drunen-Schoenmaker, R. Kanaar, E. Lehmann, J. H. J. Hoeijmakers, and J. Kohli Rec8p, a Meiotic Recombination and Sister Chromatid Cohesion Phosphoprotein of the Rad21p Family Conserved from Fission Yeast to Humans Mol. Cell. Biol., May 1, 1999; 19(5): 3515 - 3528. [Abstract] [Full Text] [PDF]

				D Bopp, C Schutt, J Puro, H Huang, and R Nothiger Recombination and disjunction in female germ cells of Drosophila depend on the germline activity of the gene sex-lethal Development, January 12, 1999; 126(24): 5785 - 5794. [Abstract] [PDF]

				C. Rieder and R Cole Chromatid cohesion during mitosis: lessons from meiosis J. Cell Sci., January 8, 1999; 112(16): 2607 - 2613. [Abstract] [PDF]

				T. T.-L. Tang, S. E. Bickel, L. M. Young, and T. L. Orr-Weaver Maintenance of sister-chromatid cohesion at the centromere by the Drosophila MEI-S332 protein Genes & Dev., December 15, 1998; 12(24): 3843 - 3856. [Abstract] [Full Text]

				S. E. Bickel, D. P. Moore, C. Lai, and T. L. Orr-Weaver Genetic Interactions Between mei-S332 and ord in the Control of Sister-Chromatid Cohesion Genetics, December 1, 1998; 150(4): 1467 - 1476. [Abstract] [Full Text]

				D. P. Moore, A. W. Page, T. T.-L. Tang, A. W. Kerrebrock, and T. L. Orr-Weaver The Cohesion Protein MEI-S332 Localizes to Condensed Meiotic and Mitotic Centromeres until Sister Chromatids Separate J. Cell Biol., March 9, 1998; 140(5): 1003 - 1012. [Abstract] [Full Text] [PDF]

				G. S. Roeder Meiotic chromosomes: it takes two to tango Genes & Dev., October 15, 1997; 11(20): 2600 - 2621. [Full Text] [PDF]

				T Torok, P D Harvie, M Buratovich, and P J Bryant The product of proliferation disrupter is concentrated at centromeres and required for mitotic chromosome condensation and cell proliferation in Drosophila. Genes & Dev., January 15, 1997; 11(2): 213 - 225. [Abstract] [PDF]

				A. Page and T. Orr-Weaver The Drosophila genes grauzone and cortex are necessary for proper female meiosis J. Cell Sci., January 7, 1996; 109(7): 1707 - 1715. [Abstract] [PDF]