Checkpoint mechanisms: The puppet masters of meiotic prophase

Trends in Cell Biology

Volumn 21, Issue 7, 2011, Pages 393-400

  MacQueen, Amy J ^a   Hochwagen, Andreas ^b  

^a WESLEYAN UNIVERSITY   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; HISTONE H2AX; PROTEIN KINASE; PROTEIN P53; PROTEIN RAD1; PROTEIN RAD9;

CELL CYCLE; CELL CYCLE ARREST; CHROMOSOME PAIRING; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; FERTILITY; GAMETE; HUMAN; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROPHASE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL CYCLE PROTEINS; CHROMOSOME PAIRING; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; HUMANS; MEIOTIC PROPHASE I;

EID: 79959610377     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2011.03.004     Document Type: Review

References (89)

1. Hartwell L.H., Weinert T.A. Checkpoints: controls that ensure the order of cell cycle events. Science 1989, 246:629-634.
2. Elledge S.J. Cell cycle checkpoints: preventing an identity crisis. Science 1996, 274:1664-1672.
3. Cha R.S., Kleckner N. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 2002, 297:602-606.
4. Musacchio A., Salmon E.D. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell. Biol. 2007, 8:379-393.
5. Petronczki M., et al. Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 2003, 112:423-440.
6. Keeney S., Neale M.J. Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem. Soc. Trans. 2006, 34:523-525.
7. Heyer W.D., et al. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 2010, 44:113-139.
8. Zickler D. From early homologue recognition to synaptonemal complex formation. Chromosoma 2006, 115:158-174.
9. Hochwagen A., Amon A. Checking your breaks: surveillance mechanisms of meiotic recombination. Curr. Biol. 2006, 16:R217-228.
10. Longhese M.P., et al. DNA double-strand breaks in meiosis: checking their formation, processing and repair. DNA Repair (Amst.) 2009, 8:1127-1138.
11. Lovejoy C.A., Cortez D. Common mechanisms of PIKK regulation. DNA Repair (Amst.) 2009, 8:1004-1008.
12. Harrison J.C., Haber J.E. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 2006, 40:209-235.
13. Burgoyne P.S., et al. The management of DNA double-strand breaks in mitotic G2, and in mammalian meiosis viewed from a mitotic G2 perspective. Bioessays 2007, 29:974-986.
14. Carballo J.A., Cha R.S. Meiotic roles of Mec1, a budding yeast homolog of mammalian ATR/ATM. Chromosome Res. 2007, 15:539-550.
15. Cartagena-Lirola H., et al. Role of the Saccharomyces cerevisiae Rad53 checkpoint kinase in signaling double-strand breaks during the meiotic cell cycle. Mol. Cell. Biol. 2008, 28:4480-4493.
16. MacQueen A.J., Roeder G.S. Fpr3 and Zip3 ensure that initiation of meiotic recombination precedes chromosome synapsis in budding yeast. Curr. Biol. 2009, 19:1519-1526.
17. Thorne L.W., Byers B. Stage-specific effects of X-irradiation on yeast meiosis. Genetics 1993, 134:29-42.
18. Malkova A., et al. HO endonuclease-induced recombination in yeast meiosis resembles Spo11-induced events. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:14500-14505.
19. Roeder G.S., Bailis J.M. The pachytene checkpoint. Trends Genet. 2000, 16:395-403.
20. Wu H.Y., et al. Mek1 kinase governs outcomes of meiotic recombination and the checkpoint response. Curr. Biol. 2010, 20:1707-1716.
21. Gartner A., et al. A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol. Cell 2000, 5:435-443.
22. MacQueen A.J., Villeneuve A.M. Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev. 2001, 15:1674-1687.
23. Jaramillo-Lambert A. Meiotic errors activate checkpoints that improve gamete quality without triggering apoptosis in male germ cells. Curr. Biol. 2010, 20:2078-2089.
24. Perez-Hidalgo L., et al. The fission yeast meiotic checkpoint kinase Mek1 regulates nuclear localization of Cdc25 by phosphorylation. Cell Cycle 2008, 7:3720-3730.
25. Sourirajan A., Lichten M. Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev. 2008, 22:2627-2632.
26. Lancaster O.M., et al. The meiotic recombination checkpoint suppresses NHK-1 kinase to prevent reorganisation of the oocyte nucleus in Drosophila. PLoS Genet. 2010, 6:e1001179.
27. Couteau F., et al. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 1999, 11:1623-1634.
28. Shimada M., et al. The meiotic recombination checkpoint is regulated by checkpoint rad+ genes in fission yeast. Embo J. 2002, 21:2807-2818.
29. Di Giacomo M., et al. Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:737-742.
30. Barchi M., et al. ATM promotes the obligate XY crossover and both crossover control and chromosome axis integrity on autosomes. PLoS Genet. 2008, 4:e1000076.
31. Barlow C., et al. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 1996, 86:159-171.
32. Garcia V., et al. AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 2003, 15:119-132.
33. Cartagena-Lirola H., et al. Budding yeast Sae2 is an in vivo target of the Mec1 and Tel1 checkpoint kinases during meiosis. Cell Cycle 2006, 5:1549-1559.
34. Terasawa M., et al. Sae2p phosphorylation is crucial for cooperation with Mre11p for resection of DNA double-strand break ends during meiotic recombination in Saccharomyces cerevisiae. Genes Genet. Syst. 2008, 83:209-217.
35. Garcia-Muse T., Boulton S.J. Distinct modes of ATR activation after replication stress and DNA double-strand breaks in Caenorhabditis elegans. EMBO J. 2005, 24:4345-4355.
36. Lu W.J., et al. Meiotic recombination provokes functional activation of the p53 regulatory network. Science 2010, 328:1278-1281.
37. Peretz G., et al. The Drosophila hus1 gene is required for homologous recombination repair during meiosis. Mech. Dev. 2009, 126:677-686.
38. Falk J.E., et al. A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev. Cell 2010, 19:599-611.
39. Sumiyoshi E., et al. Protein phosphatase 4 is required for centrosome maturation in mitosis and sperm meiosis in C. elegans. J. Cell Sci. 2002, 115:1403-1410.
40. Bartrand A.J., et al. Evidence of meiotic crossover control in Saccharomyces cerevisiae through Mec1-mediated phosphorylation of replication protein A. Genetics 2006, 172:27-39.
41. Carpenter A.T., Baker B.S. On the control of the distribution of meiotic exchange in Drosophila melanogaster. Genetics 1982, 101:81-89.
42. Grushcow J.M., et al. Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice. Genetics 1999, 153:607-620.
43. Thompson D.A., Stahl F.W. Genetic control of recombination partner preference in yeast meiosis. Isolation and characterization of mutants elevated for meiotic unequal sister-chromatid recombination. Genetics 1999, 153:621-641.
44. Wan L., et al. Mek1 kinase activity functions downstream of RED1 in the regulation of meiotic double strand break repair in budding yeast. Mol. Biol. Cell 2004, 15:11-23.
45. Niu H., et al. Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis. Mol. Cell. Biol. 2007, 27:5456-5467.
46. Niu H., et al. Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol. Biol. Cell 2005, 16:5804-5818.
47. Carballo J.A., et al. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 2008, 132:758-770.
48. Niu H., et al. Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol. Cell 2009, 36:393-404.
49. Govin J., et al. Systematic screen reveals new functional dynamics of histones H3 and H4 during gametogenesis. Genes Dev. 2010, 24:1772-1786.
50. Xu L., et al. Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 1997, 11:106-118.
51. Shin Y.H., et al. Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet. 2010, 6:e1001190.
52. Martinez-Perez E., Villeneuve A.M. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 2005, 19:2727-2743.
53. Couteau F., Zetka M. HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev. 2005, 19:2744-2756.
54. Goodyer W., et al. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev. Cell 2008, 14:263-274.
55. Sato A., et al. Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 2009, 139:907-919.
56. Wojtasz L., et al. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet. 2009, 5:e1000702.
57. Borner G.V., et al. Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3327-3332.
58. Martinez-Perez E., et al. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 2008, 22:2886-2901.
59. Kemp B., et al. A role for centromere pairing in meiotic chromosome segregation. Genes Dev. 2004, 18:1946-1951.
60. Scherthan H. A bouquet makes ends meet. Nat. Rev. Mol. Cell Biol. 2001, 2:621-627.
61. Fernandez-Capetillo O., et al. H2AX regulates meiotic telomere clustering. J. Cell Biol. 2003, 163:15-20.
62. Pandita T.K., et al. Atm inactivation results in aberrant telomere clustering during meiotic prophase. Mol. Cell Biol. 1999, 19:5096-5105.
63. Liebe B., et al. Mutations that affect meiosis in male mice influence the dynamics of the mid-preleptotene and bouquet stages. Exp. Cell Res. 2006, 312:3768-3781.
64. Culligan K.M., Britt A.B. Both ATM and ATR promote the efficient and accurate processing of programmed meiotic double-strand breaks. Plant J. 2008, 55:629-638.
65. Loidl J., Mochizuki K. Tetrahymena meiotic nuclear reorganization is induced by a checkpoint kinase-dependent response to DNA damage. Mol. Biol. Cell 2009, 20:2428-2437.
66. Dernburg A.F., et al. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 1998, 94:387-398.
67. McKim K.S., et al. Meiotic synapsis in the absence of recombination. Science 1998, 279:876-878.
68. Higashitani A., et al. Caenorhabditis elegans Chk2-like gene is essential for meiosis but dispensable for DNA repair. FEBS Lett. 2000, 485:35-39.
69. Penkner A.M., et al. Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 2009, 139:920-933.
70. Bhalla N., Dernburg A.F. A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science 2005, 310:1683-1686.
71. Joyce E.F., McKim K.S. Drosophila PCH2 is required for a pachytene checkpoint that monitors double-strand-break-independent events leading to meiotic crossover formation. Genetics 2009, 181:39-51.
72. Jaramillo-Lambert A., Engebrecht J. A single unpaired and transcriptionally silenced X chromosome locally precludes checkpoint signaling in the Caenorhabditis elegans germ line. Genetics 2009, 184:613-628.
73. MacQueen A.J., et al. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 2005, 123:1037-1050.
74. San-Segundo P.A., Roeder G.S. Pch2 links chromatin silencing to meiotic checkpoint control. Cell 1999, 97:313-324.
75. Wu H.Y., Burgess S.M. Two distinct surveillance mechanisms monitor meiotic chromosome metabolism in budding yeast. Curr. Biol. 2006, 16:2473-2479.
76. Greiss S., et al. C. elegans SIR-2.1 translocation is linked to a proapoptotic pathway parallel to cep-1/p53 during DNA damage-induced apoptosis. Genes Dev. 2008, 22:2831-2842.
77. Barchi M., et al. Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. Mol. Cell Biol. 2005, 25:7203-7215.
78. Kouznetsova A., et al. BRCA1-mediated chromatin silencing is limited to oocytes with a small number of asynapsed chromosomes. J. Cell Sci. 2009, 122:2446-2452.
79. Mahadevaiah S.K., et al. Extensive meiotic asynapsis in mice antagonises meiotic silencing of unsynapsed chromatin and consequently disrupts meiotic sex chromosome inactivation. J. Cell Biol. 2008, 182:263-276.
80. Li X.C., Schimenti J.C. Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet. 2007, 3:e130.
81. Roig I., et al. Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLoS Genet. 2010, 6:e1001062.
82. Turner J.M. Meiotic sex chromosome inactivation. Development 2007, 134:1823-1831.
83. Fernandez-Capetillo O., et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 2003, 4:497-508.
84. Bellani M.A., et al. SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-/- spermatocytes. J. Cell Sci. 2005, 118:3233-3245.
85. Turner J.M., et al. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr. Biol. 2004, 14:2135-2142.
86. Mahadevaiah S.K., et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 2001, 27:271-276.
87. Galanty Y., et al. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 2009, 462:935-939.
88. Vigodner M. Sumoylation precedes accumulation of phosphorylated H2AX on sex chromosomes during their meiotic inactivation. Chromosome Res. 2009, 17:37-45.
89. de Carvalho C.E., Colaiacovo M.P. SUMO-mediated regulation of synaptonemal complex formation during meiosis. Genes Dev. 2006, 20:1986-1992.