Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis

PLoS Genetics

Volumn 6, Issue 11, 2010, Pages

  Shin, Yong Hyun ^a,b   Choi, Youngsok ^c   Erdin, Serpil Uckac ^a   Yatsenko, Svetlana A ^a   Kloc, Malgorzata ^d   Yang, Fang ^e   Wang, P Jeremy ^e   Meistrich, Marvin L ^f   Rajkovic, Aleksandar ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c CHA University   (South Korea)

^d HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; BRCA1 PROTEIN; CARRIER PROTEIN; CELL PROTEIN; GAMMA HISTONE H2AX; HISTONE H2AX; PROTEIN DMC1; PROTEIN HORMAD1; RAD51 PROTEIN; REPLICATION FACTOR A; UNCLASSIFIED DRUG; ATM PROTEIN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; MESSENGER RNA; NOHMA PROTEIN, MOUSE; NUCLEAR PROTEIN; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOCYTE; CHROMOSOME INACTIVATION; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; ELECTRON MICROSCOPY; FEMALE; GAMETOGENESIS; KNOCKOUT MOUSE; MALE; MEIOSIS; MEIOTIC RECOMBINATION; MITOSIS INHIBITION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY FOLLICLE DEVELOPMENT; PACHYTENE; PROTEIN LOCALIZATION; SEX CHROMOSOME; SILENCER ELEMENT; SYNAPTONEMAL COMPLEX; ANEUPLOIDY; ANIMAL; ANTIBODY SPECIFICITY; CYTOLOGY; EMBRYO DEVELOPMENT; FETUS; GENETIC RECOMBINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; OOCYTE; OVARY; PHOSPHORYLATION; PROTEIN TRANSPORT; SPERMATOGENESIS; SPERMATOZOON; ULTRASTRUCTURE;

MAMMALIA; MUS; SYNAPSIS;

ANEUPLOIDY; ANIMALS; CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; DNA-BINDING PROTEINS; EMBRYONIC DEVELOPMENT; FEMALE; FETUS; MALE; MEIOSIS; MICE; MUTATION; NUCLEAR PROTEINS; OOCYTES; ORGAN SPECIFICITY; OVARY; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC; RNA, MESSENGER; SEX CHROMOSOMES; SPERMATOGENESIS; SPERMATOZOA; SYNAPTONEMAL COMPLEX; TUMOR SUPPRESSOR PROTEINS;

EID: 78649715690     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001190     Document Type: Article

References (69)

1. Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525-558.
2. Bailis JM, Roeder GS (1998) Synaptonemal complex morphogenesis and sisterchromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev 12: 3551-3563.
3. Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, et al. (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98: 91-103.
4. Loidl J, Klein F, Scherthan H (1994) Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J Cell Biol 125: 1191-1200.
5. Aravind L, Koonin EV (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 23: 284-286.
6. Michel LS, Liberal V, Chatterjee A, Kirchwegger R, Pasche B, et al. (2001) MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409: 355-359.
7. Dobles M, Liberal V, Scott ML, Benezra R, Sorger PK (2000) Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101: 635-645.
8. Hollingsworth NM, Goetsch L, Byers B (1990) The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61: 73-84.
9. Smith AV, Roeder GS (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136: 957-967.
10. Zetka MC, Kawasaki I, Strome S, Muller F (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev 13: 2258-2270.
11. Armstrong SJ, Caryl AP, Jones GH, Franklin FC (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115: 3645-3655.
12. Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, et al. (2003) Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 5: 463-474.
13. Couteau F, Nabeshima K, Villeneuve A, Zetka M (2004) A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol 14: 585-592.
14. Ross KJ, Fransz P, Armstrong SJ, Vizir I, Mulligan B, et al. (1997) Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNAtransformed lines. Chromosome Res 5: 551-559.
15. Caryl AP, Armstrong SJ, Jones GH, Franklin FC (2000) A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109: 62-71.
16. Pangas SA, Yan W, Matzuk MM, Rajkovic A (2004) Restricted germ cell expression of a gene encoding a novel mammalian HORMA domain-containing protein. Gene Expr Patterns 5: 257-263.
17. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, et al. (2009) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAAATPase. PLoS Genet 5: e1000702. doi:10.1371/journal.pgen.1000702.
18. Fukuda T, Daniel K, Wojtasz L, Toth A, Hoog C (2010) A novel mammalian HORMA domain-containing protein, HORMAD1, preferentially associates with unsynapsed meiotic chromosomes. Exp Cell Res 316: 158-171.
19. Kironmai KM, Muniyappa K, Friedman DB, Hollingsworth NM, Byers B (1998) DNA-binding activities of Hop1 protein, a synaptonemal complex component from Saccharomyces cerevisiae. Mol Cell Biol 18: 1424-1435.
20. Mao-Draayer Y, Galbraith AM, Pittman DL, Cool M, Malone RE (1996) Analysis of meiotic recombination pathways in the yeast Saccharomyces cerevisiae. Genetics 144: 71-86.
21. Carballo JA, Johnson AL, Sedgwick SG, Cha RS (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132: 758-770.
22. Bailis JM, Smith AV, Roeder GS (2000) Bypass of a meiotic checkpoint by overproduction of meiotic chromosomal proteins. Mol Cell Biol 20: 4838-4848.
23. Meuwissen RL, Offenberg HH, Dietrich AJ, Riesewijk A, van Iersel M, et al. (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 11: 5091-5100.
24. Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB (1994) Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci 107(Pt 10): 2749-2760.
25. Lammers JH, Offenberg HH, van Aalderen M, Vink AC, Dietrich AJ, et al. (1994) The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol 14: 1137-1146.
26. Offenberg HH, Schalk JA, Meuwissen RL, van Aalderen M, Kester HA, et al. (1998) SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res 26: 2572-2579.
27. Yuan L, Liu JG, Zhao J, Brundell E, Daneholt B, et al. (2000) The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol Cell 5: 73-83.
28. del Mazo J, Kremer L, Avila J (1987) Centromeric proteins recognized by CREST sera and meiotic chromosome segregation. Chromosoma 96: 55-59.
29. Yuan L, Liu JG, Hoja MR, Wilbertz J, Nordqvist K, et al. (2002) Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3. Science 296: 1115-1118.
30. Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, et al. (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1: 697-705.
31. de Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, et al. (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19: 1376-1389.
32. Gasior SL, Wong AK, Kora Y, Shinohara A, Bishop DK (1998) Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev 12: 2208-2221.
33. Edelmann W, Cohen PE, Kane M, Lau K, Morrow B, et al. (1996) Meiotic pachytene arrest in MLH1-deficient mice. Cell 85: 1125-1134.
34. Kolas NK, Marcon E, Crackower MA, Hoog C, Penninger JM, et al. (2005) Mutant meiotic chromosome core components in mice can cause apparent sexual dimorphic endpoints at prophase or X-Y defective male-specific sterility. Chromosoma 114: 92-102.
35. Woltering D, Baumgartner B, Bagchi S, Larkin B, Loidl J, et al. (2000) Meiotic segregation, synapsis, and recombination checkpoint functions require physical interaction between the chromosomal proteins Red1p and Hop1p. Mol Cell Biol 20: 6646-6658.
36. Ward IM, Chen J (2001) Histone H2AX is phosphorylated in an ATRdependent manner in response to replicational stress. J Biol Chem 276: 47759-47762.
37. Prieler S, Penkner A, Borde V, Klein F (2005) The control of Spo11's interaction with meiotic recombination hotspots. Genes Dev 19: 255-269.
38. Nakamura TM, Du LL, Redon C, Russell P (2004) Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast. Mol Cell Biol 24: 6215-6230.
39. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, et al. (2003) H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 4: 497-508.
40. Turner JM, Aprelikova O, Xu X, Wang R, Kim S, et al. (2004) BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol 14: 2135-2142.
41. Kozlov SV, Graham ME, Peng C, Chen P, Robinson PJ, et al. (2006) Involvement of novel autophosphorylation sites in ATM activation. EMBO J 25: 3504-3514.
42. Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y, et al. (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell 1: 707-718.
43. Edelmann W, Cohen PE, Kneitz B, Winand N, Lia M, et al. (1999) Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat Genet 21: 123-127.
44. Barlow C, Liyanage M, Moens PB, Tarsounas M, Nagashima K, et al. (1998) Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development 125: 4007-4017.
45. Pangas SA, Choi Y, Ballow DJ, Zhao Y, Westphal H, et al. (2006) Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. Proc Natl Acad Sci U S A 103: 8090-8095.
46. Deb K, Reese J, Paria BC (2006) Methodologies to study implantation in mice. Methods Mol Med 121: 9-34.
47. Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, et al. (2004) Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 6: 555-562.
48. Yang F, De La Fuente R, Leu NA, Baumann C, McLaughlin KJ, et al. (2006) Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J Cell Biol 173: 497-507.
49. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, et al. (1996) Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev 10: 2411-2422.
50. Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6: 975-987.
51. de los Santos T, Hollingsworth NM (1999) Red1p, a MEK1-dependent phosphoprotein that physically interacts with Hop1p during meiosis in yeast. J Biol Chem 274: 1783-1790.
52. Wang H, Hoog C (2006) Structural damage to meiotic chromosomes impairs DNA recombination and checkpoint control in mammalian oocytes. J Cell Biol 173: 485-495.
53. Di Giacomo M, Barchi M, Baudat F, Edelmann W, Keeney S, et al. (2005) Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc Natl Acad Sci U S A 102: 737-742.
54. Hollingsworth NM, Ponte L (1997) Genetic interactions between HOP1, RED1 and MEK1 suggest that MEK1 regulates assembly of axial element components during meiosis in the yeast Saccharomyces cerevisiae. Genetics 147: 33-42.
55. Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2: 280-291.
56. Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA (2005) SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 37: 1351-1355.
57. Handel MA, Schimenti JC (2010) Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat Rev Genet 11: 124-136.
58. Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R (2001) Novel meiosisspecific isoform of mammalian SMC1. Mol Cell Biol 21: 6984-6998.
59. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, et al. (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349: 704-706.
60. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG (2005) Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33: e36.
61. Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM (2004) NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305: 1157-1159.
62. Baltus AE, Menke DB, Hu YC, Goodheart ML, Carpenter AE, et al. (2006) In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat Genet 38: 1430-1434.
63. Choi Y, Ballow DJ, Xin Y, Rajkovic A (2008) Lim homeobox gene, lhx8, is essential for mouse oocyte differentiation and survival. Biol Reprod 79: 442-449.
64. Li M, Shin YH, Hou L, Huang X, Wei Z, et al. (2008) The adaptor protein of the anaphase promoting complex Cdh1 is essential in maintaining replicative lifespan and in learning and memory. Nat Cell Biol.
65. Rajkovic A, Yan MSC, Klysik M, Matzuk M (2001) Discovery of germ cellspecific transcripts by expressed sequence tag database analysis. Fertil Steril 76: 550-554.
66. Wang PJ, McCarrey JR, Yang F, Page DC (2001) An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27: 422-426.
67. Mouillet JF, Chu T, Nelson DM, Mishima T, Sadovsky Y (2010) MiR-205 silences MED1 in hypoxic primary human trophoblasts. FASEB J.
68. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
69. Seli E, Lalioti MD, Flaherty SM, Sakkas D, Terzi N, et al. (2005) An embryonic poly(A)-binding protein (ePAB) is expressed in mouse oocytes and early preimplantation embryos. Proc Natl Acad Sci U S A 102: 367-372.