Meiosis-Specific Cohesin Component, Stag3 Is Essential for Maintaining Centromere Chromatid Cohesion, and Required for DNA Repair and Synapsis between Homologous Chromosomes

PLoS Genetics

Volumn 10, Issue 7, 2014, Pages

  Hopkins, Jessica ^a   Hwang, Grace ^a   Jacob, Justin ^a   Sapp, Nicklas ^a   Bedigian, Rick ^b   Oka, Kazuhiro ^c   Overbeek, Paul ^c   Murray, Steve ^b   Jordan, Philip W ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JACKSON LABORATORY   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; COHESIN; PROTEIN RAD21L; PROTEIN REC8; PROTEIN SMC1 BETA; PROTEIN STAG3; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; RAD21L PROTEIN, MOUSE; REC8 PROTEIN, MOUSE; SMC1L2 PROTEIN, MOUSE; STAG3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ISOLATION; CENTROMERE; CHROMATID; CHROMOSOME PAIRING; CONTROLLED STUDY; DNA REPAIR; FEMALE; GERM CELL; HETEROCHROMATIN; HISTOLOGY; MALE; MEIOSIS; MOUSE; MUTANT; MUTATION; NONHUMAN; OVARY; PROPHASE; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; SISTER CHROMATID; TESTIS; ANIMAL; GENETICS; METABOLISM;

ANIMALS; CELL CYCLE PROTEINS; CENTROMERE; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME PAIRING; DNA REPAIR; MEIOSIS; MICE; MULTIPROTEIN COMPLEXES; MUTATION; NUCLEAR PROTEINS; PHOSPHOPROTEINS;

EID: 84905457928     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004413     Document Type: Article

References (70)

1. Jordan P, (2006) Initiation of homologous chromosome pairing during meiosis. Biochem Soc Trans 34: 545-549.
2. Nasmyth K, (2011) Cohesin: a catenase with separate entry and exit gates? Nat Cell Biol 13: 1170-1177.
3. Ishiguro K-I, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y, (2011) A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep 12: 267-275.
4. Gómez R, Valdeolmillos A, Parra M, Viera A, Carreiro C, et al. (2007) Mammalian SGO2 appears at the inner centromere domain and redistributes depending on tension across centromeres during meiosis II and mitosis. EMBO Rep 8: 173-180.
5. Prieto I, Suja JA, Pezzi N, Kremer L, Martinez-A C, et al. (2001) Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat Cell Biol 3: 761-766.
6. Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R, (2001) Novel Meiosis-Specific Isoform of Mammalian SMC1. Mol Cell Biol 21: 6984-6998.
7. Gutiérrez-Caballero C, Herrán Y, Sánchez-Martín M, Suja JÁ, Barbero JL, et al. (2011) Identification and molecular characterization of the mammalian α-kleisin RAD21L. Cell Cycle 10: 1477-1487.
8. Lee J, Hirano T, (2011) RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol 192: 263-276.
9. Garcia-Cruz R, Brieno MA, Roig I, Grossmann M, Velilla E, et al. (2010) Dynamics of cohesin proteins REC8, STAG3, SMC1β and SMC3 are consistent with a role in sister chromatid cohesion during meiosis in human oocytes. Hum Reprod 25: 2316-2327.
10. Parra MT, Viera A, Gomez R, Page J, Benavente R, et al. (2004) Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J Cell Sci 117: 1221-1234.
11. Xu H, B.M., Verschoor S, Inselman A, Handel MA, McKay MJ, (2004) A new role for the mitotic RAD21/SCC1 cohesin in meiotic chromosome cohesion and segregation in the mouse. EMBO Rep 5: 378-384.
12. Llano E, Herrán Y, García-Tuñón I, Gutiérrez-Caballero C, de Álava E, et al. (2012) Meiotic cohesin complexes are essential for the formation of the axial element in mice. J Cell Biol 197: 877-885.
13. Boateng Kingsley A, Bellani Marina A, Gregoretti Ivan V, Pratto F, Camerini-Otero RD, (2013) Homologous Pairing Preceding SPO11-Mediated Double-Strand Breaks in Mice. Dev Cell 24: 196-205.
14. Scherthan H, Weich S, Schwegler H, Heyting C, Härle M, et al. (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134: 1109-1125.
15. Shibuya H, Ishiguro K-i, Watanabe Y, (2014) The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis. Nat Cell Biol 16: 145-156.
16. Herran Y, Gutierrez-Caballero C, Sanchez-Martin M, Hernandez T, Viera A, et al. (2011) The cohesin subunit RAD21L functions in meiotic synapsis and exhibits sexual dimorphism in fertility. EMBO J 30: 3091-3105.
17. Adelfalk C, Janschek J, Revenkova E, Blei C, Liebe B, et al. (2009) Cohesin SMC1β protects telomeres in meiocytes. JCB 187: 185-199.
18. Verver DE, van Pelt AM, Repping S, Hamer G, (2013) Role for rodent Smc6 in pericentromeric heterochromatin domains during spermatogonial differentiation and meiosis. Cell Death Dis 4: e749.
19. Gómez R, Jordan PW, Viera A, Alsheimer M, Fukuda T, et al. (2013) Dynamic localization of SMC5/6 complex proteins during mammalian meiosis and mitosis implies functions in distinct chromosome processes. J Cell Sci 125: 5061-5072.
20. Guenatri M, Bailly D, Maison C, Almouzni G, (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166: 493-505.
21. Lange UC, Siebert S, Wossidlo M, Weiss T, Ziegler-Birling C, et al. (2013) Dissecting the role of H3K64me3 in mouse pericentromeric heterochromatin. Nat Commun 4: 2233.
22. Bellani MA, Romanienko PJ, Cairatti DA, Camerini-Otero RD, (2005) SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-/- spermatocytes. J Cell Sci 118: 3233-3245.
23. Royo H, Prosser H, Ruzankina Y, Mahadevaiah SK, Cloutier JM, et al. (2013) ATR acts stage specifically to regulate multiple aspects of mammalian meiotic silencing. Genes Dev 27: 1484-1494.
24. Refolio E, Cavero S, Marcon E, Freire R, San-Segundo PA, (2011) The Ddc2/ATRIP checkpoint protein monitors meiotic recombination intermediates. J Cell Sci 124: 2488-2500.
25. Moens PB, Heyting C, Dietrich AJ, van Raamsdonk W, Chen Q, (1987) Synaptonemal complex antigen location and conservation. J Cell Biol 105: 93-103.
26. Offenberg HH, Schalk JAC, Meuwissen RLJ, 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. 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 AAA-ATPase. PLoS Genet 5: e1000702.
28. Hamer G, Gell K, Kouznetsova A, Novak I, Benavente R, et al. (2006) Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J Cell Sci 119: 4025-4032.
29. Turner JMA, (2007) Meiotic sex chromosome inactivation. Development 134: 1823-1831.
30. Handel MA, (2004) The XY body: a specialized meiotic chromatin domain. Expt Cell Res 296: 57-63.
31. Jordan PW, Karppinen J, Handel MA, (2012) Polo-like kinase is required for synaptonemal complex disassembly and phosphorylation in mouse spermatocytes. J Cell Sci 125: 5061-5072.
32. Ishiguro K-i, Kim J, Shibuya H, Hernández-Hernández A, Suzuki A, et al. (2014) Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes. Genes Dev 28: 594-607.
33. Gao Y-F, Li T, Chang Y, Wang Y-B, Zhang W-N, et al. (2011) Cdk1-phosphorylated CUEDC2 promotes spindle checkpoint inactivation and chromosomal instability. Nat Cell Biol 13: 924-933.
34. Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, et al. (2004) Cohesin SMC1β is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 6: 555-562.
35. Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA, (2005) SMC1β-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 37: 1351-1355.
36. Bannister LA, Reinholdt LG, Munroe RJ, Schimenti JC, (2004) Positional cloning and characterization of mouse mei8, a disrupted allele of the meiotic cohesin Rec8. Genesis 40: 184-194.
37. Xu H, Beasley MD, Warren WD, van der Horst GT, McKay MJ, (2005) Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 8: 949-961.
38. Liebe B, Alsheimer M, Höög C, Benavente R, Scherthan H, (2004) Telomere Attachment, Meiotic Chromosome Condensation, Pairing, and Bouquet Stage Duration Are Modified in Spermatocytes Lacking Axial Elements. Mol Biol Cell 15: 827-837.
39. Qiao H, Chen JK, Reynolds A, Höög C, Paddy M, et al. (2012) Interplay between Synaptonemal Complex, Homologous Recombination, and Centromeres during Mammalian Meiosis. PLoS Genet 8: e1002790.
40. Bisig CG, Guiraldelli MF, Kouznetsova A, Scherthan H, Höög C, et al. (2012) Synaptonemal Complex Components Persist at Centromeres and Are Required for Homologous Centromere Pairing in Mouse Spermatocytes. PLoS Genet 8: e1002701.
41. Wiltshire T, Park C, Caldwell KA, Handel MA, (1995) Induced Premature G2/M-Phase Transition in Pachytene Spermatocytes Includes Events Unique to Meiosis. Dev Biol 169: 557-567.
42. Zou L, Elledge SJ, (2003) Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes. Science 300: 1542-1548.
43. Plug AW, Peters AH, Keegan KS, Hoekstra MF, de Boer P, et al. (1998) Changes in protein composition of meiotic nodules during mammalian meiosis. J Cell Sci 111: 413-423.
44. Kogo H, Tsutsumi M, Inagaki H, Ohye T, Kiyonari H, et al. (2012) HORMAD2 is essential for synapsis surveillance during meiotic prophase via the recruitment of ATR activity. Genes to Cells 17: 897-912.
45. Wojtasz L, Cloutier JM, Baumann M, Daniel K, Varga J, et al. (2012) Meiotic DNA double-strand breaks and chromosome asynapsis in mice are monitored by distinct HORMAD2-independent and-dependent mechanisms. Genes Dev 26: 958-973.
46. Daniel K, Lange J, Hached K, Fu J, Anastassiadis K, et al. (2011) Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol 13: 599-610.
47. Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y, (2003) Distinct cohesin complexes organize meiotic chromosome domains. Science 300: 1152-1155.
48. Thomas SE, Soltani-Bejnood M, Roth P, Dorn R, Logsdon JJM, et al. (2005) Identification of Two Proteins Required for Conjunction and Regular Segregation of Achiasmate Homologs in Drosophila Male Meiosis. Cell 123: 555.
49. Molnar M, Doll E, Yamamoto A, Hiraoka Y, Kohli J, (2003) Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing. J Cell Sci 116: 1719-1731.
50. Ponticelli AS, Smith GR, (1989) Meiotic recombination-deficient mutants of Schizosaccharomyces pombe. Genetics 123: 45-54.
51. Biswas U, Wetzker C, Lange J, Christodoulou E, Seifert M, et al. (2013) Meiotic Cohesin SMC1β Provides Prophase I Centromeric Cohesion and Is Required for Multiple Synapsis-Associated Functions. PLoS Genet 9p. e1003985.
52. Sumara I, Vorlaufer E, Gieffers C, Peters BH, Peters J-M, (2000) Characterization of Vertebrate Cohesin Complexes and Their Regulation in Prophase. JCB 151: 749-762.
53. Peters J-M, Tedeschi A, Schmitz J, (2008) The cohesin complex and its roles in chromosome biology. Genes Dev 22: 3089-3114.
54. Laugsch M, Seebach J, Schnittler H, Jessberger R, (2013) Imbalance of SMC1 and SMC3 Cohesins Causes Specific and Distinct Effects. PLoS ONE 8: e65149.
55. Murdoch B, Owen N, Stevense M, Smith H, Nagaoka S, et al. (2013) Altered Cohesin Gene Dosage Affects Mammalian Meiotic Chromosome Structure and Behavior. PLoS Genet 9: e1003241.
56. Hiraoka Y, Dernburg AF, (2009) The SUN Rises on Meiotic Chromosome Dynamics. Dev Cell 17: 598-605.
57. Hahn M, Dambacher S, Dulev S, Kuznetsova AY, Eck S, et al. (2013) Suv4-20h2 mediates chromatin compaction and is important for cohesin recruitment to heterochromatin. Genes Dev 27: 859-872.
58. Whelan G, Kreidl E, Wutz G, Egner A, Peters J-M, et al. (2012) Cohesin acetyltransferase Esco2 is a cell viability factor and is required for cohesion in pericentric heterochromatin. EMBO J 31: 71-82.
59. Barbero JL, (2013) Genetic basis of cohesinopathies. App Clin Genet 6: 15-23.
60. Deardorff Matthew A, Wilde Jonathan J, Albrecht M, Dickinson E, Tennstedt S, et al. (2012) RAD21 Mutations Cause a Human Cohesinopathy. Am J of Human Genet 90: 1014-1027.
61. Deardorff MA, Kaur M, Yaeger D, Rampuria A, Korolev S, et al. (2007) Mutations in Cohesin Complex Members SMC3 and SMC1A Cause a Mild Variant of Cornelia de Lange Syndrome with Predominant Mental Retardation. Am J of Human Genet 80: 485-494.
62. Musio A, Selicorni A, Focarelli ML, Gervasini C, Milani D, et al. (2006) X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat Genet 38: 528-530.
63. Remeseiro S, Cuadrado A, Gomez-Lopez G, Pisano DG, Losada A, (2012) A unique role of cohesin-SA1 in gene regulation and development. EMBO J 31: 2090-2102.
64. Kalejs M, Ivanov A, Plakhins G, Cragg M, Emzinsh D, et al. (2006) Upregulation of meiosis-specific genes in lymphoma cell lines following genotoxic insult and induction of mitotic catastrophe. BMC Cancer 6: 6.
65. Notaridou M, Quaye L, Dafou D, Jones C, Song H, et al. (2011) Common alleles in candidate susceptibility genes associated with risk and development of epithelial ovarian cancer. Int J Cancer 128: 2063-2074.
66. Caburet S. Arboleda V, Llano E, Overbeek P, Barbero JL, et al. (2014) Mutant Cohesin in Premature Ovarian Failure. NEJM 370: 943-949.
67. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, et al. (2011) A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474: 337-342.
68. Bellve AR (1993) Purification, culture, and fractionation of spermatogenic cells. Methods in Enzymology: Academic Press. 84-113 p.
69. La Salle, S., F Sun and M.A Handel. 2009. Isolation and Short-Term Culture of Mouse Spermatocytes for Analysis of Meiosis. Meiosis. Vol. 558. J.M Walker, editor. Humana Press. 279-297 p.
70. Novak I, Wang H, Revenkova E, Jessberger R, Scherthan H, Höög C, (2008) Cohesin Smc1β determines meiotic chromatin axis loop organization. JCB 180: 83-90.