A Role for Centromere Pairing in Meiotic Chromosome Segregation

Overview

Journal Genes Dev

Specialty Molecular Biology

Date 2004 Aug 4

PMID 15289462

Citations 48

Authors

Benedict Kemp

Rebecca Maxfield Boumil

Mara N Stewart

Dean S Dawson

Affiliations

Soon will be listed here.

Abstract

In meiosis I, exchanges provide a connection between homologous chromosome pairs that facilitates their proper attachment to the meiotic spindle. In many eukaryotes, homologous chromosomes that fail to become linked by exchanges exhibit elevated levels of meiotic errors, but they do not segregate randomly, demonstrating that mechanisms beyond exchange can promote proper meiosis I segregation. The experiments described here demonstrate the existence of a meiotic centromere pairing mechanism in budding yeast. This centromere pairing mediates the meiosis I bipolar spindle attachment of nonexchange chromosome pairs and likely plays the same role for all homologous chromosome pairs.

Citing Articles

FBXO47 regulates centromere pairing as key component of centromeric SCF E3 ligase in mouse spermatocytes.

Ma A, Yang Y, Cao L, Chen L, Zhang J Commun Biol. 2024; 7(1):1099.

PMID: 39244596 PMC: 11380685. DOI: 10.1038/s42003-024-06782-6.

Molecular evolution of the mammalian kinetochore complex.

Arora U, Dumont B bioRxiv. 2024; .

PMID: 38979348 PMC: 11230421. DOI: 10.1101/2024.06.27.600994.

Centromere pairing enables correct segregation of meiotic chromosomes.

Evatt J, Sadli A, Rapacz B, Chuong H, Meyer R, Ridenour J Curr Biol. 2024; 34(10):2085-2093.e6.

PMID: 38670094 PMC: 11111343. DOI: 10.1016/j.cub.2024.04.008.

Meiosis in budding yeast.

Borner G, Hochwagen A, MacQueen A Genetics. 2023; 225(2).

PMID: 37616582 PMC: 10550323. DOI: 10.1093/genetics/iyad125.

The courtship choreography of homologous chromosomes: timing and mechanisms of DSB-independent pairing.

Sole M, Pascual A, Anton E, Blanco J, Sarrate Z Front Cell Dev Biol. 2023; 11:1191156.

PMID: 37377734 PMC: 10291267. DOI: 10.3389/fcell.2023.1191156.

References

Dernburg A, Sedat J, Hawley R . Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell. 1996; 86(1):135-46. DOI: 10.1016/s0092-8674(00)80084-7. View

Karpen G, Le M, Le H . Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science. 1996; 273(5271):118-22. DOI: 10.1126/science.273.5271.118. View

Straight A, Belmont A, Robinett C, Murray A . GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol. 1996; 6(12):1599-608. DOI: 10.1016/s0960-9822(02)70783-5. View

Michaelis C, Ciosk R, Nasmyth K . Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell. 1997; 91(1):35-45. DOI: 10.1016/s0092-8674(01)80007-6. View

ROSS L, Dawson D . Chiasmata, crossovers, and meiotic chromosome segregation. Adv Genet. 1997; 35:253-84. DOI: 10.1016/s0065-2660(08)60452-6. View

Hayashi A, Ogawa H, Kohno K, Gasser S, Hiraoka Y . Meiotic behaviours of chromosomes and microtubules in budding yeast: relocalization of centromeres and telomeres during meiotic prophase. Genes Cells. 1998; 3(9):587-601. DOI: 10.1046/j.1365-2443.1998.00215.x. View

Guerra C, Kaback D . The role of centromere alignment in meiosis I segregation of homologous chromosomes in Saccharomyces cerevisiae. Genetics. 1999; 153(4):1547-60. PMC: 1460858. DOI: 10.1093/genetics/153.4.1547. View

Goshima G, Yanagida M . Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell. 2000; 100(6):619-33. DOI: 10.1016/s0092-8674(00)80699-6. View

He X, Asthana S, Sorger P . Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell. 2000; 101(7):763-75. DOI: 10.1016/s0092-8674(00)80888-0. View

10.

Shonn M, McCarroll R, Murray A . Requirement of the spindle checkpoint for proper chromosome segregation in budding yeast meiosis. Science. 2000; 289(5477):300-3. DOI: 10.1126/science.289.5477.300. View

11.

Kamieniecki R, Shanks R, Dawson D . Slk19p is necessary to prevent separation of sister chromatids in meiosis I. Curr Biol. 2000; 10(19):1182-90. DOI: 10.1016/s0960-9822(00)00723-5. View

12.

. Sister chromatid separation: falling apart at the seams. Curr Biol. 2000; 10(22):R816-9. DOI: 10.1016/s0960-9822(00)00799-5. View

13.

Hassold T, Hunt P . To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet. 2001; 2(4):280-91. DOI: 10.1038/35066065. View

14.

Aragon-Alcaide L, Strunnikov A . Functional dissection of in vivo interchromosome association in Saccharomyces cerevisiae. Nat Cell Biol. 2000; 2(11):812-8. PMC: 2673479. DOI: 10.1038/35041055. View

15.

Maxfield Boumil R, Kemp B, Angelichio M, Nilsson-Tillgren T, Dawson D . Meiotic segregation of a homeologous chromosome pair. Mol Genet Genomics. 2003; 268(6):750-60. DOI: 10.1007/s00438-002-0796-9. View

16.

NICKLAS R, Koch C . Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J Cell Biol. 1969; 43(1):40-50. PMC: 2107850. DOI: 10.1083/jcb.43.1.40. View

17.

Mann C, Davis R . Meiotic disjunction of circular minichromosomes in yeast does not require DNA homology. Proc Natl Acad Sci U S A. 1986; 83(16):6017-9. PMC: 386428. DOI: 10.1073/pnas.83.16.6017. View

18.

Dawson D, Murray A, Szostak J . An alternative pathway for meiotic chromosome segregation in yeast. Science. 1986; 234(4777):713-7. DOI: 10.1126/science.3535068. View

19.

Guacci V, Kaback D . Distributive disjunction of authentic chromosomes in Saccharomyces cerevisiae. Genetics. 1991; 127(3):475-88. PMC: 1204375. DOI: 10.1093/genetics/127.3.475. View

20.

Loidl J, Nairz K, Klein F . Meiotic chromosome synapsis in a haploid yeast. Chromosoma. 1991; 100(4):221-8. DOI: 10.1007/BF00344155. View