Extreme heterogeneity in the molecular events leading to the establishment of chiasmata during meiosis I in human oocytes

American Journal of Human Genetics

Volumn 76, Issue 1, 2005, Pages 112-127

  Lenzi, Michelle L ^a   Smith, Jenetta ^a   Snowden, Timothy ^b   Kim, Mimi ^a   Fishel, Richard ^b   Poulos, Bradford K ^a   Cohen, Paula E ^a,c  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b Kimmel Cancer Center   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2A; HISTONE H2AX; PROTEIN MLH1; PROTEIN MLH3; RAD51 PROTEIN; RECA PROTEIN; RPA PROTEIN; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANEUPLOIDY; ARTICLE; CHROMOSOME CHIASM; CONTROLLED STUDY; CROSSING OVER; EMBRYO DEVELOPMENT; HUMAN; HUMAN CELL; MEIOSIS; NONDISJUNCTION; OOCYTE; PACHYTENE; PRIORITY JOURNAL; PROPHASE; PROTEIN PHOSPHORYLATION; SPONTANEOUS ABORTION; STATISTICAL ANALYSIS;

MAMMALIA; PACHYNEMA;

EID: 11144325648     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1086/427268     Document Type: Article

References (61)

1. Abdullah MF, Hoffmann ER, Cotton VE, Borts RH (2004) A role for the MutL homologue MLH2 in controlling heteroduplex formation and in regulating between two different crossover pathways in budding yeast. Cytogenet Genome Res 107:180-190
2. Allers T, Lichten M (2001) Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol Cell 8:225-231
3. Ashley T, Plug AW, Xu J, Solari AJ, Reddy G, Golub EI, Ward DC (1995) Dynamic changes in Rad51 distribution onchromatin during meiosis in male and female vertebrates. Chromosoma 104:19-28
4. Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, Yao X, Christie DM, Monell C, Arnheim N, Bradley A, Ashley T, Liskay RM (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13:336-342
5. Bannister LA, Schimenti JC (2004) Homologous recombinational repair proteins in mouse meiosis. Cytogenet Genome Res 107:191-200
6. Barlow AL, Benson FE, West SC, Hulten MA (1997) Distribution of the Rad51 recombinase in human and mouse spermatocytes. EMBO J 16:5207-5215
7. Barlow AL, Hulten MA (1998) Crossing over analysis at pachytene in man. Eur J Hum Genet 6:350-358
8. Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79:1081-1092
9. Bocker T, Barusevicius A, Snowden T, Rasio D, Guerrette S, Robbins D, Schmidt C, Burczak J, Croce CM, Copeland T, Kovatich AJ, Fishel R (1999) hMSH5: a human MutS homologue that forms a novel heterodimer with MSH4 and is expressed during spermatogenesis. Cancer Res 59:816-822
10. Borts RH, Chambers SR, Abdullah MF (2000) The many faces of mismatch repair in meiosis. Mutat Res 451:129-150
11. Broman KW, Murray JC, Sheffield VC, White RL, Weber JL (1998) Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am J Hum Genet 63:861-869
12. Broman KW, Weber JL (2000) Characterization of human crossover interference. Am J Hum Genet 66:1911-1926
13. Brown AS, Feingold E, Broman KW, Sherman SL (2000) Genome-wide variation in recombination in female meiosis: a risk factor for non-disjunction of chromosome 21. Hum Mol Genet 9:515-523
14. Cohen PE, Pollard JW (2001) Regulation of meiotic recombination and prophase I progression in mammals. Bioessays 23:996-1009
15. de Vries SS, Baart EB, Dekker M, Siezen A, de Rooij DG, de Boer P, te Riele H (1999) Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev 13:523-531
16. Eaker S, Cobb J, Pyle A, Handel MA (2002) Meiotic prophase abnormalities and metaphase cell death in MLH1-deficient mouse spermatocytes: insights into regulation of spermatogenic progress. Dev Biol 249:85-95
17. Edelmann W, Cohen PE, Kane M, Lau K, Morrow B, Bennett S, Umar A, Kunkel T, Cattoretti G, Chaganti R, Pollard JW, Kolodner RD, Kucherlapati R (1996) Meiotic pachytene arrest in MLH1-deficient mice. Cell 85:1125-1134
18. Edelmann W, Cohen PE, Kneitz B, Winand N, Lia M, Heyer J, Kolodner R, Pollard JW, Kucherlapati R (1999) Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat Genet 21:123-127
19. Hamer G, Roepers-Gajadien HL, van Duyn-Goedhart A, Gademan IS, Kal HB, van Buul PP, de Rooij DG (2003) DNA double-strand breaks and gamma-H2AX signaling in the testis. Biol Reprod 68:628-634
20. Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2:280-291
21. Hassold T, Judis L, Chan ER, Schwartz S, Seftel A, Lynn A (2004) Cytological studies of meiotic recombination in human males. Cytogenet Genome Res 107:249-255
22. Hassold T, Sherman S (2000) Down syndrome: genetic recombination and the origin of the extra chromosome 21. Clin Genet 57:95-100
23. Hassold T, Sherman S, Hunt PA (2000) Counting cross-overs: characterizing meiotic recombination in mammals. Hum Mol Genet 9:2409-2419
24. Higgins JD, Armstrong SJ, Franklin FC, Jones GH (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18:2557-2570
25. Hoffmann ER, Borts RH (2004) Meiotic recombination intermediates and mismatch repair proteins. Cytogenet Genome Res 107:232-248
26. Hoffmann ER, Shcherbakova PV, Kunkel TA, Borts RH (2003) MLH1 mutations differentially affect meiotic functions in Saccharomyces cerevisiae. Genetics 163:515-526
27. Hollingsworth NM, Ponte L, Halsey C (1995) MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev 9:1728-1739
28. Hunter N, Borts RH (1997) Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev 11:1573-1582
29. Judis L, Chan ER, Schwanz S, Seftel A, Hassold T (2004) Meiosis I arrest and azoospermia in an infertile male explained by failure of formation of a component of the synaptonemal complex. Fertil Steril 81:205-209
30. Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375-384
31. Kelly KO, Dernburg AF, Stanfield GM, Villeneuve AM (2000) Caenorhabditis elegans msb-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156:617-630
32. Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, Hou H Jr, Kolodner RD, Kucherlapati R, Pollard JW, Edelmann W (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14:1085-1097
33. Kolas NK, Cohen PE (2004) Novel and diverse functions of the DNA mismatch repair family in mammalian meiosis and recombination. Cytogenet Genome Res 107:216-231
34. Lipkin SM, Moens PB, Wang V, Lenzi ML, Shanmugarajah D, Gilgeous A, Thomas J, Cheng J, Touchman JW, Green ED, Schwartzberg P, Collins FS, Cohen PE (2002) Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat Genet 31:385-390
35. Lynn A, Ashley T, Hassold T (2004) Variation in human meiotic recombination. Annu Rev Genomics Hum Genet 5:317-349
36. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-Rodriguez J, Jasin M, Keeney S, Bonner WM, Burgoyne PS (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27:271-276
37. Marcon E, Moens P (2003) MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 165:2283-2287
38. Moens PB, Kolas NK, Tarsounas M, Marcon E, Cohen PE, Spyropoulos B (2002) The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci 115:1611-1622
39. Novak JE, Ross-Macdonald PB, Roeder GS (2001) The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158:1013-1025
40. Pepling ME, Spradling AC (2001) Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 234:339-351
41. Peters AH, Plug AW, van Vugt MJ, de Boer P (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5:66-68
42. Plug AW, Peters AH, Keegan KS, Hoekstra MF, de Boer P, Ashley T (1998) Changes in protein composition of meiotic nodules during mammalian meiosis. J Cell Sci 111:413-423
43. Plug AW, Xu J, Reddy G, Golub EI, Ashley T (1996) Presynaptic association of Rad51 protein with selected sites in meiotic chromatin. Proc Natl Acad Sci USA 93:5920-5924
44. Roig I, Liebe B, Egozcue J, Cabero L, Garcia M, Scherthan H (2004) Female-specific features of recombinational double-stranded DNA repair in relation to synapsis and telomere dynamics in human oocytes. Chromosoma 113:22-33
45. Romanienko PJ, Camerini-Otero RD (1999) Cloning, characterization, and localization of mouse and human SPO11. Genomics 61:156-169
46. Ross-Macdonald P, Roeder GS (1994) Mutation of a meiosis-specific MutS homolog decreases crossing over but not mis-match correction. Cell 79:1069-1080
47. Santucci-Darmanin S, Walpita D, Lespinasse F, Desnuelle C, Ashley T, Paquis-Flucklinger V (2000) MSH4 acts in conjunction with MLH1 during mammalian meiosis. FASEB J 14:1539-1547
48. Savage AR, Petersen MB, Pettay D, Taft L, Allran K, Freeman SB, Karadima G, Avramopoulos D, Torfs C, Mikkelsen M, Hassold TJ, Sherman SL (1998) Elucidating the mechanisms of paternal non-disjunction of chromosome 21 in humans. Hum Mol Genet 7:1221-1227
49. Sherman SL, Petersen MB, Freeman SB, Hersey J, Pettay D, Taft L, Frantzen M, Mikkelsen M, Hassold TJ (1994) Non-disjunction of chromosome 21 in maternal meiosis I: evidence for a maternal age-dependent mechanism involving reduced recombination. Hum Mol Genet 3:1529-1535
50. Sherman SL, Takaesu N, Freeman SB, Grantham M, Phillips C, Blackston RD, Jacobs PA, Cockwell AE, Freeman V, Uchida I, Mikkelsen M, Kurnit DM, Buraczynska M, Keats BJB, Hassold TJ (1991) Trisomy 21: association between reduced recombination and nondisjunction. Am J Hum Genet 49:608-620
51. Snowden T, Acharya S, Butz C, Berardini M, Fishel R (2004) MSH4-MSH5 recognizes Holliday junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15:437-451
52. Tease C, Hartshorne GM, Hulten MA (2002) Patterns of meiotic recombination in human fetal oocytes. Am J Hum Genet 70:1469-1479
53. Tilly JL (2001) Commuting the death sentence: how oocytes strive to survive. Nat Rev Mol Cell Biol 2:838-848
54. van Veen JE, Hawley RS (2003) Meiosis: when even two is a crowd. Curr Biol 13:R831-R833
55. Wang TF, Kleckner N, Hunter N (1999) Functional specificity of MutL homologs in yeast: evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc Natl Acad Sci USA 96:13914-13919
56. Warren AC, Chakravarti A, Wong C, Slaugenhaupt SA, Halloran SL, Watkins PC, Metaxotou C, Antonarakis SE (1987) Evidence for reduced recombination on the nondisjoined chromosomes 21 in Down syndrome. Science 237:652-654
57. Winand NJ, Panzer JA, Kolodner RD (1998) Cloning and characterization of the human and Caenorhabditis elegans homologs of the Saccharomyces cerevisiae MSH5 gene. Genomics 53:69-80
58. Woods LM, Hodges CA, Baart E, Baker SM, Liskay RM, Hunt PA (1999) Chromosomal influence on meiotic spindle assembly: abnormal meiosis I in female Mlh1 mutant mice. J Cell Biol 145:1395-1406
59. Yuan L, Liu JG, Hoja MR, Wilbertz J, Nordqvist K, Hoog C (2002) Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3. Science 296:1115-1118
60. Yuan L, Liu JG, Zhao J, Brundell E, Daneholt B, Hoog C (2000) The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol Cell 5:73-83
61. Zalevsky J, MacQueen AJ, Duffy JB, Kemphues KJ, Villeneuve AM (1999) Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153:1271-1283