Emerging roles for centromeres in meiosis I chromosome segregation

Nature Reviews Genetics

Volumn 9, Issue 12, 2008, Pages 899-910

  Brar, Gloria A ^a   Amon, Angelika ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN;

CENTROMERE; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; EUKARYOTIC CELL; MEIOTIC PROPHASE I; MICROTUBULE; MITOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

ANIMALS; CENTROMERE; CHROMOSOME SEGREGATION; HUMANS; KINETOCHORES; MEIOSIS;

EUKARYOTA;

EID: 56549105643     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg2454     Document Type: Review

References (117)

1. Nasmyth, K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35, 673-745 (2001).
2. Lee, B. & Amon, A. Meiosis: how to create a specialized cell cycle. Curr. Opin. Cell Biol. 13, 770-777 (2001).
3. Marston, A. L. & Amon, A. Meiosis: cell-cycle controls shuffle and deal. Nature Rev. Mol. Cell Biol. 5, 983-997 (2004).
4. Sharp, L. Introduction to Cytology 3rd edn (McGraw-Hill, New York, 1934).
5. Fitzgerald-Hayes, M., Clarke, L. & Carbon, J. Nucleotide sequence comparisons and functional analysis of yeast centromere DNAs. Cell 29, 235-244 (1982). The authors conclude that a 25-bp sequence from budding yeast is sufficient for plasmid segregation. This sequence is conserved between chromosomes. This study is the first identification of a discrete centromere sequence.
6. Fitzgerald-Hayes, M., Buhler, J. M., Cooper, T. G. & Carbon, J. Isolation and subcloning analysis of functional centromere DNA (CEN11) from Saccharomyces cerevisiae chromosome XI. Mol. Cell Biol. 2, 82-87 (1982).
7. Malik, H. S. & Henikoff, S. Conflict begets complexity: the evolution of centromeres. Curr. Opin. Genet. Dev. 12, 711-718 (2002).
8. Zinkowski, R. P., Meyne, J. & Brinkley, B. R. The centromere-kinetochore complex: a repeat subunit model. J. Cell Biol. 113, 1091-1110 (1991).
9. Marschall, L. G. & Clarke, L. A novel cis-acting centromeric DNA element affects S. pombe centromeric chromatin structure at a distance. J. Cell Biol. 128, 445-454 (1995).
10. Yeh, E. et al. Pericentric chromatin is organized into an intramolecular loop in mitosis. Curr. Biol. 18, 81-90 (2008). This paper uses an elegant microscopic strategy to reveal the looped structure of budding yeast centromeres, showing cohesins to be a major determinant of this structure.
11. Blat, Y. & Kleckner, N. Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98, 249-259 (1999).
12. Weber, S. A. et al. The kinetochore is an enhancer of pericentric cohesin binding. PLoS Biol. 2, E260 (2004).
13. Ekwall, K. Epigenetic control of centromere behavior. Annu. Rev. Genet. 41, 63-81 (2007).
14. De Wulf, P., McAinsh, A. D. & Sorger, P. K. Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev. 17, 2902-2921 (2003).
15. Chan, G. K., Liu, S. T. & Yen, T. J. Kinetochore structure and function. Trends Cell Biol. 15, 589-598 (2005).
16. Cheeseman, I. M. & Desai, A. Molecular architecture of the kinetochore-microtubule interface. Nature Rev. Mol. Cell Biol. 9, 33-46 (2008).
17. Musacchio, A. & Salmon, E. D. The spindle-assembly checkpoint in space and time. Nature Rev. Mol. Cell Biol. 8, 379-393 (2007).
18. Westermann, S., Drubin, D. G. & Barnes, G. Structures and functions of yeast kinetochore complexes. Annu. Rev. Biochem. 76, 563-591 (2007).
19. Volpe, T. A. et al. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833-1837 (2002).
20. Hall, I. M. et al. Establishment and maintenance of a heterochromatin domain. Science 297, 2232-2237 (2002).
21. Nakayama, J., Rice, J. C., Strahl, B. D., Allis, C. D. & Grewal, S. I. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292, 110-113 (2001).
22. Cleard, F., Delattre, M. & Spierer, P. SU(VAR)3-7, a Drosophila heterochromatin-associated protein and companion of HP1 in the genomic silencing of position-effect variegation. EMBO J. 16, 5280-5288 (1997).
23. Eskeland, R. et al. The N-terminus of Drosophila SU(VAR)3-9 mediates dimerization and regulates its methyltransferase activity. Biochemistry 43, 3740-3749 (2004).
24. Kiburz, B. M. et al. The core centromere and Sgo1 establish a 50-kb cohesin-protected domain around centromeres during meiosis I. Genes Dev. 19, 3017-3030 (2005). The authors use genome-wide location analysis to show the precise location of protected cohesins in meiosis I, which coincides with Sgo1 localization and covers 50 kb around each centromere. The authors also determine core centromeric sequences to be necessary and sufficient for assembly of this protected domain.
25. Megee, P. C. & Koshland, D. A functional assay for centromere-associated sister chromatid cohesion. Science 285, 254-257 (1999).
26. Megee, P. C., Mistrot, C., Guacci, V. & Koshland, D. The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences. Mol. Cell 4, 445-450 (1999).
27. Zickler, D. & Kleckner, N. Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33, 603-754 (1999).
28. McKee, B. D. Homologous pairing and chromosome dynamics in meiosis and mitosis. Biochim. Biophys. Acta 1677, 165-180 (2004).
29. Keeney, S. & Neale, M. J. Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem. Soc. Trans. 34, 523-525 (2006).
30. Whitby, M. C. Making crossovers during meiosis. Biochem. Soc. Trans. 33, 1451-1455 (2005).
31. Zickler, D. & Kleckner, N. The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32, 619-697 (1998).
32. Hawley, R. S. & Theurkauf, W. E. Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet. 9, 310-317 (1993).
33. Grell, R. F. Distributive pairing: the size-dependent mechanism for regular segregation of the fourth chromosomes in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 52, 226-232 (1964).
34. Guacci, V. & Kaback, D. B. Distributive disjunction of authentic chromosomes in Saccharomyces cerevisiae. Genetics 127, 475-488 (1991).
35. Maxfield Boumil, R., Kemp, B., Angelichio, M., Nilsson-Tillgren, T. & Dawson, D. S. Meiotic segregation of a homeologous chromosome pair. Mol. Genet. Genomics 268, 750-760 (2003).
36. Peoples-Holst, T. L. & Burgess, S. M. Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast. Genes Dev. 19, 863-874 (2005).
37. Tsubouchi, T. & Roeder, G. S. A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308, 870-873 (2005).
38. Kemp, B., Boumil, R. M., Stewart, M. N. & Dawson, D. S. A role for centromere pairing in meiotic chromosome segregation. Genes Dev. 18, 1946-1951 (2004). This study uses budding yeast strains that have been engineered to carry homeologous copies of chromosome 5 as a model to investigate distributive segregation. The authors find that centromere association of the homeologues precedes and is required for their proper segregation in meiosis I.
39. Koehler, K. E., Hawley, R. S., Sherman, S. & Hassold, T. Recombination and nondisjunction in humans and flies. Hum. Mol. Genet. 5, 1495-1504 (1996).
40. Hawley, R. S. et al. There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology. Dev. Genet. 13, 440-467 (1992).
41. Fung, J. C., Marshall, W. F., Dernburg, A., Agard, D. A. & Sedat, J. W. Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J. Cell Biol. 141, 5-20 (1998).
42. Hiraoka, Y. et al. The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J. Cell Biol. 120, 591-600 (1993).
43. Karpen, G. H., Le, M. H. & Le, H. Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273, 118-122 (1996).
44. Dalal, Y., Furuyama, T., Vermaak, D. & Henikoff, S. Structure, dynamics, and evolution of centromeric nucleosomes. Proc. Natl Acad. Sci. USA 104, 15974-15981 (2007).
45. Kusch, T. & Workman, J. L. Histone variants and complexes involved in their exchange. Subcell. Biochem. 41, 91-109 (2007).
46. Maddox, P. S., Oegema, K., Desai, A. & Cheeseman, I. M. 'Holo'er than thou: chromosome segregation and kinetochore function in C. elegans. Chromosome Res. 12, 641-653 (2004).
47. MacQueen, A. J. et al. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123, 1037-1050 (2005).
48. Villeneuve, A. M. A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136, 887-902 (1994).
49. McKim, K. S., Peters, K. & Rose, A. M. Two types of sites required for meiotic chromosome pairing in Caenorhabditis elegans. Genetics 134, 749-768 (1993).
50. Phillips, C. M. et al. HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123, 1051-1063 (2005).
51. Phillips, C. M. & Dernburg, A. F. A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev. Cell 11, 817-829 (2006).
52. Riley, R., Chapman, V. Genetic control of the cytologically diploid behaviour of hexaploid wheat. Nature 182, 713-715 (1958). The authors perform crosses of various wheat lines, identifying a general homeologous-pairing restriction activity that correlates with monosomy for a particular chromosome, later identified as chromosome 5.
53. Wall, A. M., Riley, R., Gale, M. D. The position of a locus on chromosome 5B of Triticum aestivum affecting homeologous meiotic pairing. Genet. Res. 18, 329-339 (1971).
54. Gill, K. S. & Gill, B. S. A DNA fragment mapped within the submicroscopic deletion of Ph1, a chromosome pairing regulator gene in polyploid wheat. Genetics 129, 257-259 (1991).
55. Griffiths, S. et al. Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439, 749-752 (2006).
56. Prieto, P., Moore, G. & Reader, S. Control of conformation changes associated with homologue recognition during meiosis. Theor. Appl. Genet. 111, 505-510 (2005).
57. Sidhu, G. K., Rustgi, S., Shafqat, M. N., von Wettstein, D. & Gill, K. S. Fine structure mapping of a gene-rich region of wheat carrying Ph1, a suppressor of crossing over between homoeologous chromosomes. Proc. Natl Acad. Sci. USA 105, 5815-5820 (2008).
58. Aragon-Alcaide, L. et al. Association of homologous chromosomes during floral development. Curr. Biol. 7, 905-908 (1997).
59. Aragon-Alcaide, L., Reader, S., Miller, T. & Moore, G. Centromeric behaviour in wheat with high and low homoeologous chromosomal pairing. Chromosoma 106, 327-333 (1997).
60. Martinez-Perez, E., Shaw, P., Aragon-Alcaide, L. & Moore, G. Chromosomes form into seven groups in hexaploid and tetraploid wheat as a prelude to meiosis. Plant J. 36, 21-29 (2003).
61. Martinez-Perez, E., Shaw, P. & Moore, G. The Ph1 locus is needed to ensure specific somatic and meiotic centromere association. Nature 411, 204-207 (2001).
62. Nasmyth, K. & Haering, C. H. The structure and function of SMC and kleisin complexes. Annu. Rev. Biochem. 74, 595-648 (2005).
63. Uhlmann, F. Chromosome cohesion and separation: from men and molecules. Curr. Biol. 13, R104-R114 (2003).
64. Yu, H. Regulation of APC-Cdc20 by the spindle checkpoint. Curr. Opin. Cell Biol. 14, 706-714 (2002).
65. Chen, R. H. Dual inhibition of Cdc20 by the spindle checkpoint. J. Biomed. Sci. 14, 475-479 (2007).
66. Shonn, M. A., McCarroll, R. & Murray, A. W. Requirement of the spindle checkpoint for proper chromosome segregation in budding yeast meiosis. Science 289, 300-303 (2000).
67. Craig, J. M. & Choo, K. H. Kiss and break up - a safe passage to anaphase in mitosis and meiosis. Chromosoma 114, 252-262 (2005).
68. Kitajima, T. S., Kawashima, S. A. & Watanabe, Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427, 510-517 (2004). The authors identify Sgo1 in fission yeast as the protein responsible for protecting centromeric cohesion during meiosis I. The authors further determine Sgo1 to have homologues in many organisms, including the Drosophila protein MEIS-332, long known to be important for centromeric cohesion.
69. Riedel, C. G. et al. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441, 53-61 (2006).
70. Tang, Z. et al. PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation. Dev. Cell 10, 575-85 (2006).
71. Lee, B. H. & Amon, A. Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation. Science 300, 482-486 (2003).
72. Brar, G. A. et al. Rec8 phosphorylation and recombination promote the step-wise loss of cohesins in meiosis. Nature 441, 532-536 (2006).
73. Eckert, C. A., Gravdahl, D. J. & Megee, P. C. The enhancement of pericentromeric cohesin association by conserved kinetochore components promotes high-fidelity chromosome segregation and is sensitive to microtubule-based tension. Genes Dev. 21, 278-291 (2007).
74. Kitajima, T. S., Yokobayashi, S., Yamamoto, M. & Watanabe, Y. Distinct cohesin complexes organize meiotic chromosome domains. Science 300, 1152-1155 (2003).
75. Koch, B., Kueng, S., Ruckenbauer, C., Wendt, K. S. & Peters, J. M. The Suv39h-HP1 histone methylation pathway is dispensable for enrichment and protection of cohesin at centromeres in mammalian cells. Chromosoma 117, 199-210 (2008).
76. Lopez, J. M., Karpen, G. H. & Orr-Weaver, T. L. Sister-chromatid cohesion via MEI-S332 and kinetochore assembly are separable functions of the Drosophila centromere. Curr. Biol. 10, 997-1000 (2000).
77. Lee, J. et al. Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nature Cell Biol. 10, 42-52 (2008).
78. Hamant, O. et al. A REC8-dependent plant Shugoshin is required for maintenance of centromeric cohesion during meiosis and has no mitotic functions. Curr. Biol. 15, 948-954 (2005).
79. Winey, M., Morgan, G. P., Straight, P. D., Giddings, T. H. Jr & Mastronarde, D. N. Three-dimensional ultrastructure of Saccharomyces cerevisiae meiotic spindles. Mol. Biol. Cell 16, 1178-1188 (2005).
80. Suja, J. A., de la Torre, J., Gimenez-Abian, J. F., Garcia de la Vega, C. & Rufas, J. S. Meiotic chromosome structure. Kinetochores and chromatid cores in standard and B chromosomes of Arcyptera fusca (Orthoptera) revealed by silver staining. Genome 34, 19-27 (1991).
81. Goldstein, L. S. Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. Cell 25, 591-602 (1981).
82. Rabitsch, K. P. et al. Kinetochore recruitment of two nucleolar proteins is required for homolog segregation in meiosis I. Dev. Cell 4, 535-548 (2003).
83. Toth, A. et al. Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis I. Cell 103, 1155-1168 (2000). The authors use a clever genetic strategy combined with genome-wide transcription analyses, to identify Mam1, a protein central to co-orientation of sister kinetochores in budding yeast.
84. Huang, J. et al. Inhibition of homologous recombination by a cohesin-associated clamp complex recruited to the rDNA recombination enhancer. Genes Dev. 20, 2887-2901 (2006).
85. Lo, H. C., Wan, L., Rosebrock, A., Futcher, B. & Hollingsworth, N. M. Cdc7-Dbf4 regulates NDT80 transcription as well as reductional segregation during budding yeast meiosis. Mol. Biol. Cell 3 Sep 2008 (doi:10.1091/mbc.E08-07-0755).
86. Clyne, R. K. et al. Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nature Cell Biol. 5, 480-485 (2003).
87. Monje-Casas, F., Prabhu, V. R., Lee, B. H., Boselli, M. & Amon, A. Kinetochore orientation during meiosis is controlled by Aurora B and the monopolin complex. Cell 128, 477-490 (2007).
88. Lee, B. H., Kiburz, B. M. & Amon, A. Spo13 maintains centromeric cohesion and kinetochore coorientation during meiosis I. Curr. Biol. 14, 2168-2182 (2004).
89. Katis, V. L. et al. Spo13 facilitates monopolin recruitment to kinetochores and regulates maintenance of centromeric cohesion during yeast meiosis. Curr. Biol. 14, 2183-2196 (2004).
90. Petronczki, M. et al. Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 126, 1049-1064 (2006).
91. Watanabe, Y. A one-sided view of kinetochore attachment in meiosis. Cell 126, 1030-1032 (2006).
92. Yokobayashi, S. & Watanabe, Y. The kinetochore protein Moa1 enables cohesion-mediated monopolar attachment at meiosis I. Cell 123, 803-817 (2005). The authors identify the fission yeast sister-kinetochore co-orientation factor, Moa1, which acts partially through collaboration with cohesins. The authors further establish the importance of centromeric cohesins in proper kinetochore orientation: they force premature cleavage of centromeric Rec8 with a protease tethered to the core centromere region, which results in cells that erroneously bi-orient sister kinetechores in meiosis I.
93. Chelysheva, L. et al. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J. Cell Sci. 118, 4621-4632 (2005).
94. Hassold, T. & Hunt, P. To err (meiotically) is human: the genesis of human aneuploidy. Nature Rev. Genet. 2, 280-291 (2001).
95. Hunt, P. A. & Hassold, T. J. Sex matters in meiosis. Science 296, 2181-2183 (2002).
96. Hunt, P. A. & Hassold, T. J. Human female meiosis: what makes a good egg go bad? Trends Genet. 24, 86-93 (2008).
97. Sherman, S. L., Lamb, N. E. & Feingold, E. Relationship of recombination patterns and maternal age among non-disjoined chromosomes 21. Biochem. Soc. Trans. 34, 578-580 (2006).
98. Cherry, J. M. et al. Genetic and physical maps of Saccharomyces cerevisiae. Nature 387, 67-73 (1997).
99. Chen, S. Y. et al. Global analysis of the meiotic crossover landscape. Dev. Cell 15, 401-415 (2008).
100. Rockmill, B., Voelkel-Meiman, K. & Roeder, G. S. Centromere-proximal crossovers are associated with precocious separation of sister chromatids during meiosis in Saccharomyces cerevisiae. Genetics 174, 1745-1754 (2006).
101. Vialard, F. et al. Evidence of a high proportion of premature unbalanced separation of sister chromatids in the first polar bodies of women of advanced age. Hum. Reprod. 21, 1172-1178 (2006).
102. Pellestor, F., Andreo, B., Arnal, F., Humeau, C. & De-maille, J. Maternal aging and chromosomal abnormalities: new data drawn from in vitro unfertilized human oocytes. Hum. Genet. 112, 195-203 (2003).
103. Pellestor, F., Andreo, B., Arnal, F., Humeau, C. & De-maille, J. Mechanisms of non-disjunction in human female meiosis: the co-existence of two modes of malsegregation evidenced by the karyotyping of 1,397 in-vitro unfertilized oocytes. Hum. Reprod. 17, 2134-2145 (2002).
104. Wolstenholme, J. & Angell, R. R. Maternal age and trisomy - a unifying mechanism of formation. Chromosoma 109, 435-438 (2000).
105. Hodges, C. A., Revenkova, E., Jessberger, R., Hassold, T. J. & Hunt, P. A. SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nature Genet. 37, 1351-1355 (2005). This paper finds that cohesin-deficient mice show meiotic segregation errors that phenocopy age-related errors that are observed in humans. The results provide an intriguing hint to the cause of 'the age effect', in which meiotic missegregation dramatically increases with maternal age.
106. Carlile, T. M. & Amon, A. Meiosis I is established through division-specific translational control of a cyclin. Cell 133, 280-291 (2008).
107. Shannon, K. B. & Salmon, E. D. Chromosome dynamics: new light on Aurora B kinase function. Curr. Biol. 12, R458-460 (2002).
108. Wang, H. W. et al. Architecture of the Dam1 kinetochore ring complex and implications for microtubule-driven assembly and force-coupling mechanisms. Nature Struct. Mol. Biol. 14, 721-726 (2007).
109. Cheeseman, I. M. et al. Phospho-regulation of kinetochore- microtubule attachments by the Aurora kinase Ipl1p. Cell 111, 163-172 (2002).
110. Kang, J. et al. Functional cooperation of Dam1, Ipl1, and the inner centromere protein (INCENP)-related protein Sli15 during chromosome segregation. J. Cell Biol. 155, 763-774 (2001).
111. Li, Y. et al. The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev. 16, 183-197 (2002).
112. Vogt, E., Kirsch-Volders, M., Parry, J. & Eichenlaub-Ritter, U. Spindle formation, chromosome segregation and the spindle checkpoint in mammalian oocytes and susceptibility to meiotic error. Mutat. Res. 651, 14-29 (2008).
113. Lew, D. J. & Burke, D. J. The spindle assembly and spindle position checkpoints. Annu. Rev. Genet. 37, 251-282 (2003).
114. Ke, Y. W., Dou, Z., Zhang, J. & Yao, X. B. Function and regulation of Aurora/Ipl1p kinase family in cell division. Cell Res. 13, 69-81 (2003).
115. Courtwright, A. M. & He, X. Dam1 is the right one: phosphoregulation of kinetochore biorientation. Dev. Cell 3, 610-611 (2002).
116. Terada, Y. Role of chromosomal passenger complex in chromosome segregation and cytokinesis. Cell Struct. Funct. 26, 653-657 (2001).
117. Lengronne, A. et al. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430, 573-578 (2004).