#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Centromeric SMC1 promotes centromer clustering and stabilizes meiotic homolog pairing


Autoři: Talia Hatkevich aff001;  Vincent Boudreau aff002;  Thomas Rubin aff003;  Paul S. Maddox aff002;  Jean-René Huynh aff003;  Jeff Sekelsky aff001
Působiště autorů: Curriculum in Genetics and Molecular Biology, University of North Carolina, Chapel Hill, North Carolina, United States of America aff001;  Department of Biology, University of North Carolina, Chapel Hill, North Carolina, United States of America aff002;  CIRB, Collège de France, PSL Research University, CNRS UMR7241, Inserm U1050, Paris, France aff003;  Integrative Program in Biological and Genome Sciences, University of North Carolina, Chapel Hill, North Carolina, United States of America aff004
Vyšlo v časopise: Centromeric SMC1 promotes centromer clustering and stabilizes meiotic homolog pairing. PLoS Genet 15(10): e32767. doi:10.1371/journal.pgen.1008412
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1008412

Souhrn

During meiosis, each chromosome must selectively pair and synapse with its own unique homolog to enable crossover formation and subsequent segregation. How homolog pairing is maintained in early meiosis to ensure synapsis occurs exclusively between homologs is unknown. We aimed to further understand this process by examining the meiotic defects of a unique Drosophila mutant, Mcm5A7. We found that Mcm5A7 mutants are proficient in homolog pairing at meiotic onset yet fail to maintain pairing as meiotic synapsis ensues, causing seemingly normal synapsis between non-homologous loci. This pairing defect corresponds with a reduction of SMC1-dependent centromere clustering at meiotic onset. Overexpressing SMC1 in this mutant significantly restores centromere clustering, homolog pairing, and crossover formation. These data indicate that the initial meiotic pairing of homologs is not sufficient to yield synapsis exclusively between homologs and provide a model in which meiotic homolog pairing must be stabilized by centromeric SMC1 to ensure proper synapsis.

Klíčová slova:

Drosophila melanogaster – Meiosis – Chromosome pairs – Ovaries – Centromeres – Homologous chromosomes – Synapsis – Corolla


Zdroje

1. Lake CM, Teeter K, Page SL, Nielsen R, Hawley RS. A genetic analysis of the Drosophila mcm5 gene defines a domain specifically required for meiotic recombination. Genetics. 2007;176(4):2151–63. doi: 10.1534/genetics.107.073551 17565942.

2. Zickler D, Kleckner N. Recombination, piring, and synapsis of homologs during meiosis. Cold Spring Harbor perspectives in biology. 2015;7(6). Epub 2015/05/20. doi: 10.1101/cshperspect.a016626 25986558; PubMed Central PMCID: PMC4448610.

3. Page SL, Hawley RS. The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol. 2004;20:525–58. Epub 2004/10/12. doi: 10.1146/annurev.cellbio.19.111301.155141 15473851.

4. Alleva B, Smolikove S. Moving and stopping: Regulation of chromosome movement to promote meiotic chromosome pairing and synapsis. Nucleus. 2017;8(6):613–24. Epub 2017/09/12. doi: 10.1080/19491034.2017.1358329 28892406; PubMed Central PMCID: PMC5788555.

5. Klutstein M, Cooper JP. The Chromosomal Courtship Dance-homolog pairing in early meiosis. Curr Opin Cell Biol. 2014;26:123–31. Epub 2014/02/18. doi: 10.1016/j.ceb.2013.12.004 24529254; PubMed Central PMCID: PMC6329632.

6. Morgan TH. Sex limited inheritance in Drosophila. Science. 1910;32(812):120–2. doi: 10.1126/science.32.812.120 17759620.

7. Christophorou N, Rubin T, Bonnet I, Piolot T, Arnaud M, Huynh JR. Microtubule-driven nuclear rotations promote meiotic chromosome dynamics. Nat Cell Biol. 2015;17(11):1388–400. doi: 10.1038/ncb3249 26458247.

8. Joyce EF, Apostolopoulos N, Beliveau BJ, Wu CT. Germline progenitors escape the widespread phenomenon of homolog pairing during Drosophila development. PLoS Genet. 2013;9(12):e1004013. doi: 10.1371/journal.pgen.1004013 24385920; PubMed Central PMCID: PMC3868550.

9. Christophorou N, Rubin T, Huynh JR. Synaptonemal complex components promote centromere pairing in pre-meiotic germ cells. PLoS Genet. 2013;9(12):e1004012. Epub 2013/12/25. doi: 10.1371/journal.pgen.1004012 24367278; PubMed Central PMCID: PMC3868581.

10. Khetani RS, Bickel SE. Regulation of meiotic cohesion and chromosome core morphogenesis during pachytene in Drosophila oocytes. J Cell Sci. 2007;120(Pt 17):3123–37. doi: 10.1242/jcs.009977 17698920.

11. Takeo S, Lake CM, Morais-de-Sa E, Sunkel CE, Hawley RS. Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr Biol. 2011;21(21):1845–51. doi: 10.1016/j.cub.2011.09.044 22036182.

12. Tanneti NS, Landy K, Joyce EF, McKim KS. A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr Biol. 2011;21(21):1852–7. doi: 10.1016/j.cub.2011.10.005 22036181.

13. Lake CM, Hawley RS. The molecular control of meiotic chromosomal behavior: events in early meiotic prophase in Drosophila oocytes. Annu Rev Physiol. 2012;74:425–51. Epub 2012/02/18. doi: 10.1146/annurev-physiol-020911-153342 22335798.

14. Collins KA, Unruh JR, Slaughter BD, Yu Z, Lake CM, Nielsen RJ, et al. Corolla Is a novel protein that contributes to the architecture of the synaptonemal complex of Drosophila. Genetics. 2014. doi: 10.1534/genetics.114.165290 24913682.

15. Jeffress JK, Page SL, Royer SK, Belden ED, Blumenstiel JP, Anderson LK, et al. The formation of the central element of the synaptonemal complex may occur by multiple mechanisms: the roles of the N- and C-terminal domains of the Drosophila C(3)G protein in mediating synapsis and recombination. Genetics. 2007;177(4):2445–56. doi: 10.1534/genetics.107.078717 17947423; PubMed Central PMCID: PMC2219479.

16. Dernburg AF, Sedat JW, Hawley RS. Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell. 1996;86(1):135–46. doi: 10.1016/s0092-8674(00)80084-7 8689681.

17. Lohe AR, Hilliker AJ, Roberts PA. Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics. 1993;134(4):1149–74. 8375654; PubMed Central PMCID: PMC1205583.

18. Gyuricza MR, Manheimer KB, Apte V, Krishnan B, Joyce EF, McKee BD, et al. Dynamic and stable cohesins regulate synaptonemal complex assembly and chromosome segregation. Curr Biol. 2016. doi: 10.1016/j.cub.2016.05.006 27291057.

19. Perkins AT, Das TM, Panzera LC, Bickel SE. Oxidative stress in oocytes during midprophase induces premature loss of cohesion and chromosome segregation errors. Proc Natl Acad Sci USA. 2016;113(44):E6823–E30. Epub 2016/11/03. doi: 10.1073/pnas.1612047113 27791141; PubMed Central PMCID: PMC5098651.

20. Krishnan B, Thomas SE, Yan R, Yamada H, Zhulin IB, McKee BD. Sisters unbound is required for meiotic centromeric cohesion in Drosophila melanogaster. Genetics. 2014;198(3):947–65. Epub 2014/09/07. doi: 10.1534/genetics.114.166009 25194162; PubMed Central PMCID: PMC4224182.

21. Webber HA, Howard L, Bickel SE. The cohesion protein ORD is required for homologue bias during meiotic recombination. J Cell Biol. 2004;164(6):819–29. doi: 10.1083/jcb.200310077 15007062; PubMed Central PMCID: PMC2172286.

22. Yan R, McKee BD. The cohesion protein SOLO associates with SMC1 and is required for synapsis, recombination, homolog bias and cohesion and pairing of centromeres in Drosophila meiosis. PLoS Genet. 2013;9(7):e1003637. Epub 2013/07/23. doi: 10.1371/journal.pgen.1003637 23874232; PubMed Central PMCID: PMC3715423.

23. Joyce EF, Paul A, Chen KE, Tanneti N, McKim KS. Multiple barriers to nonhomologous DNA end joining during meiosis in Drosophila. Genetics. 2012;191(3):739–46. Epub 2012/05/01. doi: 10.1534/genetics.112.140996 22542963; PubMed Central PMCID: PMC3389970.

24. Laugsch M, Seebach J, Schnittler H, Jessberger R. Imbalance of SMC1 and SMC3 cohesins causes specific and distinct effects. PLoS One. 2013;8(6):e65149. Epub 2013/06/19. doi: 10.1371/journal.pone.0065149 23776448; PubMed Central PMCID: PMC3680458.

25. Lin W, Wang M, Jin H, Yu HG. Cohesin plays a dual role in gene regulation and sister-chromatid cohesion during meiosis in Saccharomyces cerevisiae. Genetics. 2011;187(4):1041–51. Epub 2011/01/29. doi: 10.1534/genetics.110.122358 21270391; PubMed Central PMCID: PMC3070514.

26. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 2002;16(18):2428–42. Epub 2002/09/17. doi: 10.1101/gad.1011602 12231631; PubMed Central PMCID: PMC187442.

27. Albini SM, Jones GH. Synaptonemal complex spreading in Allium cepa and A. fistulosum I. The initiation and sequence of pairing. Chromosoma. 1987;95(5):324–38. doi: 10.1007/BF00293179 6389162.

28. Da Ines O, White CI. Centromere associations in meiotic chromosome pairing. Annu Rev Genet. 2015;49:95–114. doi: 10.1146/annurev-genet-112414-055107 26421510.

29. 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(7):585–92. Epub 2004/04/06. doi: 10.1016/j.cub.2004.03.033 15062099.

30. Couteau F, Zetka M. HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev. 2005;19(22):2744–56. Epub 2005/11/18. doi: 10.1101/gad.1348205 16291647; PubMed Central PMCID: PMC1283966.

31. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell. 2005;123(6):1037–50. Epub 2005/12/20. doi: 10.1016/j.cell.2005.09.034 16360034; PubMed Central PMCID: PMC4435800.

32. Martinez-Perez E, Villeneuve AM. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 2005;19(22):2727–43. Epub 2005/11/18. doi: 10.1101/gad.1338505 16291646; PubMed Central PMCID: PMC1283965.

33. Pattabiraman D, Roelens B, Woglar A, Villeneuve AM. Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis. PLoS Genet. 2017;13(3):e1006670. doi: 10.1371/journal.pgen.1006670 28339470; PubMed Central PMCID: PMC5384771.

34. Penkner A, Tang L, Novatchkova M, Ladurner M, Fridkin A, Gruenbaum Y, et al. The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Developmental cell. 2007;12(6):873–85. Epub 2007/06/05. doi: 10.1016/j.devcel.2007.05.004 17543861.

35. Sato A, Isaac B, Phillips CM, Rillo R, Carlton PM, Wynne DJ, et al. Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell. 2009;139(5):907–19. Epub 2009/11/17. doi: 10.1016/j.cell.2009.10.039 19913287; PubMed Central PMCID: PMC2825574.

36. Zickler D, Kleckner N. Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 1999;33:603–754. Epub 2000/02/26. doi: 10.1146/annurev.genet.33.1.603 10690419.

37. Rog O, Kohler S, Dernburg AF. The synaptonemal complex has liquid crystalline properties and spatially regulates meiotic recombination factors. eLife. 2017;6. doi: 10.7554/eLife.21455 28045371.

38. Unhavaithaya Y, Orr-Weaver TL. Centromere proteins CENP-C and CAL1 functionally interact in meiosis for centromere clustering, pairing, and chromosome segregation. Proc Natl Acad Sci USA. 2013;110(49):19878–83. Epub 2013/11/20. doi: 10.1073/pnas.1320074110 24248385; PubMed Central PMCID: PMC3856785.

39. Bell SD, Botchan MR. The minichromosome maintenance replicative helicase. Cold Spring Harbor perspectives in biology. 2013;5(11):a012807. Epub 2013/07/25. doi: 10.1101/cshperspect.a012807 23881943; PubMed Central PMCID: PMC3809582.

40. Forsburg SL. Eukaryotic MCM proteins: beyond replication initiation. Microbiol Mol Biol Rev. 2004;68(1):109–31. Epub 2004/03/10. doi: 10.1128/MMBR.68.1.109-131.2004 15007098; PubMed Central PMCID: PMC362110.

41. Sherwood R, Takahashi TS, Jallepalli PV. Sister acts: coordinating DNA replication and cohesion establishment. Genes Dev. 2010;24(24):2723–31. Epub 2010/12/17. doi: 10.1101/gad.1976710 21159813; PubMed Central PMCID: PMC3003188.

42. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, Huppert K, et al. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet. 2004;36(3):288–92. Epub 2004/02/26. doi: 10.1038/ng1312 14981519.

43. Grell RF. Time of recombination in the Drosophila melanogaster oocyte: evidence from a temperature-sensitive recombination-deficient mutant. Proc Natl Acad Sci USA. 1978;75(7):3351–4. doi: 10.1073/pnas.75.7.3351 98767.

44. Matsubayashi H, Yamamoto MT. REC, a new member of the MCM-related protein family, is required for meiotic recombination in Drosophila. Genes Genet Syst. 2003;78(5):363–71. 14676427.

45. Heeger S, Leismann O, Schittenhelm R, Schraidt O, Heidmann S, Lehner CF. Genetic interactions of separase regulatory subunits reveal the diverged Drosophila Cenp-C homolog. Genes Dev. 2005;19(17):2041–53. Epub 2005/09/06. doi: 10.1101/gad.347805 16140985; PubMed Central PMCID: PMC1199574.

46. Unhavaithaya Y, Park EA, Royzman I, Orr-Weaver TL. Drosophila embryonic cell-cycle mutants. G3 (Bethesda). 2013;3(10):1875–80. Epub 2013/08/28. doi: 10.1534/g3.113.007880 23979936; PubMed Central PMCID: PMC3789813.

47. Liu H, Jang JK, Kato N, McKim KS. mei-P22 encodes a chromosome-associated protein required for the initiation of meiotic recombination in Drosophila melanogaster. Genetics. 2002;162(1):245–58. 12242237.

48. Zeng Y, Li H, Schweppe NM, Hawley RS, Gilliland WD. Statistical analysis of nondisjunction assays in Drosophila. Genetics. 2010;186(2):505–13. doi: 10.1534/genetics.110.118778 20660647; PubMed Central PMCID: PMC2954469.

49. Anderson LK, Royer SM, Page SL, McKim KS, Lai A, Lilly MA, et al. Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of Drosophila synaptonemal complex. Proc Natl Acad Sci USA. 2005;102(12):4482–7. doi: 10.1073/pnas.0500172102 15767569; PubMed Central PMCID: PMC555515.

50. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–82. Epub 2012/06/30. doi: 10.1038/nmeth.2019 22743772; PubMed Central PMCID: PMC3855844.

51. Hartmann M, Umbanhowar J, Sekelsky J. Centromere-proximal meiotic crossovers in Drosophila melanogaster are suppressed by both highly-repetitive heterochromatin and proximity to the centromere. Genetics. 2019. Epub 2019/07/28. doi: 10.1534/genetics.119.302509 31345993.

52. Stevens WL. The analysis of interference. J Genet. 1936;32:51–64.

53. Thurmond J, Goodman JL, Strelets VB, Attrill H, Gramates LS, Marygold SJ, et al. FlyBase 2.0: The next Generation. Nucleic Acids Res. 2018;47:D759–65.

54. Hatkevich T, Kohl KP, McMahan S, Hartmann MA, Williams AM, Sekelsky J. Bloom syndrome helicase promotes meiotic crossover patterning and homolog disjunction. Curr Biol. 2017;27(1):96–102. Epub 2016/12/19. doi: 10.1016/j.cub.2016.10.055 27989672; PubMed Central PMCID: PMC5225052.

55. Miller DE, Smith CB, Yeganeh Kazemi N, Cockrell AJ, Arvanitakis AV, Blumenstiel JP, et al. Whole-genome analysis of individual meiotic events in Drosophila melanogaster reveals that noncrossover gene conversions are insensitive to interference and the centromere effect. Genetics. 2016;203(1):159–71. doi: 10.1534/genetics.115.186486 26944917; PubMed Central PMCID: PMC4858771.

56. Gong WJ, McKim KS, Hawley RS. All paired up with no place to go: pairing, synapsis, and DSB formation in a balancer heterozygote. PLoS Genet. 2005;1(5):e67. doi: 10.1371/journal.pgen.0010067 16299588; PubMed Central PMCID: PMC1285065.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2019 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#