Mouse HORMAD1 is a meiosis I checkpoint protein that modulates DNA double- strand break repair during female meiosis

Biology of Reproduction

Volumn 89, Issue 2, 2013, Pages

  Shin, Yong Hyun ^a   McGuire, Megan M ^a   Rajkovic, Aleksandar ^a,b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Double strand break repair; HORMAD1; Meiosis I; Oocyte; Ovary

Indexed keywords

HORMA DOMAIN CONTAINING PROTEIN 1; PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; NOHMA PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FEMALE; IRRADIATION; MEIOSIS; MOUSE; NONHUMAN; OOCYTE; OVARY; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; PACHYTENE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SYNAPTONEMAL COMPLEX; WILD TYPE; ANIMAL; CELL CYCLE CHECKPOINT; GENETICS; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; FEMALE; MEIOSIS; MICE; MICE, KNOCKOUT; OOCYTES;

EID: 84886926024     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.106773     Document Type: Article

References (47)

1. Pepling ME, Spradling AC. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 2001; 234: 339-351.
2. Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, Brignull E, Handel MA, Schimenti JC. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1998; 1:697-705.
3. Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y, Morita T. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell 1998; 1:707-718.
4. Barlow C, Liyanage M, Moens PB, Tarsounas M, Nagashima K, Brown K, Rottinghaus S, Jackson SP, Tagle D, Ried T, Wynshaw-Boris A. Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development 1998; 125:4007-4017.
5. de Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, Yuan L, Liu JG, van Zeeland AA, Heyting C, Pastink A. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 2005; 19:1376-1389.
6. Yang F, De La Fuente R, Leu NA, Baumann C, McLaughlin KJ, Wang PJ. Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J Cell Biol 2006; 173: 497-507.
7. Wang H, Hoog C. Structural damage to meiotic chromosomes impairs DNA recombination and checkpoint control in mammalian oocytes. J Cell Biol 2006; 173:485-495.
8. Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 2004; 305:1157-1159.
9. Shin YH, Choi Y, Erdin SU, Yatsenko SA, Kloc M, Yang F, Wang PJ, Meistrich ML, Rajkovic A. Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet 2010; 6:e1001190.
10. Pangas SA, Choi Y, Ballow DJ, Zhao Y, Westphal H, Matzuk MM, Rajkovic A. Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. Proc Natl Acad Sci U S A 2006; 103: 8090-8095.
11. Choi Y, Yuan D, Rajkovic A. Germ cell-specific transcriptional regulator Sohlh2 is essential for early mouse folliculogenesis and oocyte-specific gene expression. Biol Reprod 2008; 79:1176-1182.
12. Lange J, Pan J, Cole F, Thelen MP, Jasin M, Keeney S. ATM controls meiotic double-strand-break formation. Nature 2011; 479:237-240.
13. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 2000; 6:989-998.
14. Di Giacomo M, Barchi M, Baudat F, Edelmann W, Keeney S, Jasin M. 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.
15. Barchi M, Roig I, Di Giacomo M, de Rooij DG, Keeney S, Jasin M. ATM promotes the obligate XY crossover and both crossover control and chromosome axis integrity on autosomes. PLoS Genet 2008; 4:e1000076.
16. Romanienko PJ, Camerini-Otero RD. The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 2000; 6:975-987.
17. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, Eckmann CR, Cooke HJ, Jasin M, Keeney S, McKay MJ, Toth A. 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.
18. Fukuda T, Daniel K, Wojtasz L, Toth A, Hoog C. A novel mammalian HORMA domain-containing protein, HORMAD1, preferentially associates with unsynapsed meiotic chromosomes. Exp Cell Res 2010; 316: 158-171.
19. Daniel K, Lange J, Hached K, Fu J, Anastassiadis K, Roig I, Cooke HJ, Stewart AF, Wassmann K, Jasin M, Keeney S, Toth A. Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol 2011; 13:599-610.
20. Fukuda T, Pratto F, Schimenti JC, Turner JM, Camerini-Otero RD, Hoog C. Phosphorylation of chromosome core components may serve as axis marks for the status of chromosomal events during mammalian meiosis. PLoS Genet 2012; 8:e1002485.
21. Kogo H, Tsutsumi M, Ohye T, Inagaki H, Abe T, Kurahashi H.HORMAD1-dependent checkpoint/surveillance mechanism eliminates asynaptic oocytes. Genes Cells 2012; 17:439-454.
22. Aravind L, Koonin EV. The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 1998; 23:284-286.
23. Hollingsworth NM, Goetsch L, Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 1990; 61:73-84.
24. Smith AV, Roeder GS. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 1997; 136:957-967.
25. Couteau F, Nabeshima K, Villeneuve A, Zetka M. A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol 2004; 14: 585-592.
26. Zetka MC, Kawasaki I, Strome S, Muller F. Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev 1999; 13:2258-2270.
27. Sanchez-Moran E, Santos JL, Jones GH, Franklin FC. ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 2007; 21:2220-2233.
28. Kironmai KM, Muniyappa K, Friedman DB, Hollingsworth NM, Byers B. DNA-binding activities of Hop1 protein, a synaptonemal complex component from Saccharomyces cerevisiae. Mol Cell Biol 1998; 18: 1424-1435.
29. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev 1996; 10:2411-2422.
30. Hama H, Kurokawa H, Kawano H, Ando R, Shimogori T, Noda H, Fukami K, Sakaue-Sawano A, Miyawaki A. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat Neurosci 2011; 14:1481-1488.
31. O'Brien MJ, Pendola JK, Eppig JJ. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod 2003; 68: 1682-1686.
32. Tilly JL. Ovarian follicle count-not as simple as 1, 2, 3. Reprod Biol Endocrinol 2003; 1:11.
33. Moens PB, Kolas NK, Tarsounas M, Marcon E, Cohen PE, Spyropoulos B. 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 2002; 115:1611-1622.
34. Buard J, Barthes P, Grey C, de Massy B. Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J 2009; 28:2616-2624.
35. Prieler S, Penkner A, Borde V, Klein F. The control of Spo11's interaction with meiotic recombination hotspots. Genes Dev 2005; 19:255-269.
36. Sedelnikova OA, Rogakou EP, Panyutin IG, Bonner WM. Quantitative detection of 125IdU-induced DNA double-strand breaks with gamma- H2AX antibody. Radiat Res 2002; 158:486-492.
37. Stewart RD. Two-lesion kinetic model of double-strand break rejoining and cell killing. Radiat Res 2001; 156:365-378.
38. Howard-Till RA, Lukaszewicz A, Loidl J. The recombinases Rad51 and Dmc1 play distinct roles in DNA break repair and recombination partner choice in the meiosis of Tetrahymena. PLoS Genet 2011; 7:e1001359.
39. Goodarzi AA, Block WD, Lees-Miller SP. The role of ATM and ATR in DNA damage-induced cell cycle control. Prog Cell Cycle Res 2003; 5: 393-411.
40. Moens PB, Tarsounas M, Morita T, Habu T, Rottinghaus ST, Freire R, Jackson SP, Barlow C, Wynshaw-Boris A. The association of ATR protein with mouse meiotic chromosome cores. Chromosoma 1999; 108:95-102.
41. Latypov V, Rothenberg M, Lorenz A, Octobre G, Csutak O, Lehmann E, Loidl J, Kohli J. Roles of Hop1 and Mek1 in meiotic chromosome pairing and recombination partner choice in Schizosaccharomyces pombe. Mol Cell Biol 2010; 30:1570-1581.
42. Carballo JA, Johnson AL, Sedgwick SG, Cha RS. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 2008; 132:758-770.
43. Edelmann W, Cohen PE, Kneitz B, Winand N, Lia M, Heyer J, Kolodner R, Pollard JW, Kucherlapati R. Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat Genet 1999; 21:123-127.
44. Anderson LK, Reeves A, Webb LM, Ashley T. Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 1999; 151:1569-1579.
45. Li XC, Bolcun-Filas E, Schimenti JC. Genetic evidence that synaptonemal complex axial elements govern recombination pathway choice in mice. Genetics 2011; 189:71-82.
46. Wojtasz L, Cloutier JM, Baumann M, Daniel K, Varga J, Fu J, Anastassiadis K, Stewart AF, Remenyi A, Turner JM, Toth A. Meiotic DNA double-strand breaks and chromosome asynapsis in mice are monitored by distinct HORMAD2-independent and -dependent mechanisms. Genes Dev 2012; 26:958-973.
47. Kogo H, Tsutsumi M, Inagaki H, Ohye T, Kiyonari H, Kurahashi H. HORMAD2 is essential for synapsis surveillance during meiotic prophase via the recruitment of ATR activity. Genes Cells 2012; 17:897-912.