#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Lateral and End-On Kinetochore Attachments Are Coordinated to Achieve Bi-orientation in Oocytes


In acentrosomal oocytes, spindle assembly depends on the chromosomes. The nature of the chromosome-microtubule interactions in oocytes that organize spindle bipolarity and orientation of the homologs has been unclear. We have found that several types of functional chromosome-microtubule interactions exist in oocytes, and that each type participates in unique aspects of chromosome orientation and spindle assembly. We present here a model for chromosome-based spindle assembly and chromosome movements in oocytes that highlights the multiple and unappreciated roles played by the kinetochores and has implications for how homologous chromosomes bi-orient during meiosis.


Vyšlo v časopise: Lateral and End-On Kinetochore Attachments Are Coordinated to Achieve Bi-orientation in Oocytes. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005605
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005605

Souhrn

In acentrosomal oocytes, spindle assembly depends on the chromosomes. The nature of the chromosome-microtubule interactions in oocytes that organize spindle bipolarity and orientation of the homologs has been unclear. We have found that several types of functional chromosome-microtubule interactions exist in oocytes, and that each type participates in unique aspects of chromosome orientation and spindle assembly. We present here a model for chromosome-based spindle assembly and chromosome movements in oocytes that highlights the multiple and unappreciated roles played by the kinetochores and has implications for how homologous chromosomes bi-orient during meiosis.


Zdroje

1. Szollosi D, Calarco P, Donahue RP. Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J Cell Sci. 1972;11(2):521–41. 5076360

2. Theurkauf WE, Hawley RS. Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J Cell Biol. 1992;116(5):1167–80. 1740471

3. Albertson DG, Thomson JN. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1993;1(1):15–26. 8143084

4. Deng M, Gao J, Suraneni P, Li R. Kinetochore-independent chromosome poleward movement during anaphase of meiosis II in mouse eggs. PLoS One. 2009;4(4):e5249. doi: 10.1371/journal.pone.0005249 19365562

5. Dumont J, Oegema K, Desai A. A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat Cell Biol. 2010;12(9):894–901. doi: 10.1038/ncb2093 20729837

6. Brunet S, Maria AS, Guillaud P, Dujardin D, Kubiak JZ, Maro B. Kinetochore fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M phase. J Cell Biol. 1999;146(1):1–12. 10402455

7. Kitajima TS, Ohsugi M, Ellenberg J. Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell. 2011;146(4):568–81. doi: 10.1016/j.cell.2011.07.031 21854982

8. Wignall SM, Villeneuve AM. Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat Cell Biol. 2009;11(7):839–44. doi: 10.1038/ncb1891 19525937

9. Jang JK, Rahman T, McKim KS. The kinesinlike protein Subito contributes to central spindle assembly and organization of the meiotic spindle in Drosophila oocytes. Mol Biol Cell. 2005;16(10):4684–94. 16055508

10. Radford SJ, Jang JK, McKim KS. The Chromosomal Passenger Complex is required for Meiotic Acentrosomal Spindle Assembly and Chromosome Bi-orientation. Genetics. 2012;192:417–29. doi: 10.1534/genetics.112.143495 22865736

11. Sun SC, Zhang DX, Lee SE, Xu YN, Kim NH. Ndc80 regulates meiotic spindle organization, chromosome alignment, and cell cycle progression in mouse oocytes. Microsc Microanal. 2011;17(3):431–9. doi: 10.1017/S1431927611000274 21600073

12. Sun SC, Lee SE, Xu YN, Kim NH. Perturbation of Spc25 expression affects meiotic spindle organization, chromosome alignment and spindle assembly checkpoint in mouse oocytes. Cell Cycle. 2010;9(22):4552–9. 21084868

13. King RC. Ovarian Development in Drosophila melanogaster. New York: Academic Press Inc.; 1970.

14. Dernburg AF, Sedat JW, Hawley RS. Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell. 1996;86(1):135–46. 8689681

15. Obeso D, Pezza RJ, Dawson D. Couples, pairs, and clusters: mechanisms and implications of centromere associations in meiosis. Chromosoma. 2014;123(1–2):43–55. doi: 10.1007/s00412-013-0439-4 24126501

16. Takeo S, Hawley RS. Rumors of its disassembly have been greatly exaggerated: the secret life of the synaptonemal complex at the centromeres. PLoS Genet. 2012;8(6):e1002807. doi: 10.1371/journal.pgen.1002807 22761598

17. Hughes SE, Gilliland WD, Cotitta JL, Takeo S, Collins KA, Hawley RS. Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genet. 2009;5(1):e1000348. doi: 10.1371/journal.pgen.1000348 19165317

18. Gilliland WD, Hughes SF, Vietti DR, Hawley RS. Congression of achiasmate chromosomes to the metaphase plate in Drosophila melanogaster oocytes. Dev Biol. 2009;325(1):122–8. doi: 10.1016/j.ydbio.2008.10.003 18977343

19. Cai S, O'Connell CB, Khodjakov A, Walczak CE. Chromosome congression in the absence of kinetochore fibres. Nat Cell Biol. 2009;11(7):832–8. 19525938. doi: 10.1038/ncb1890

20. Kapoor TM, Lampson MA, Hergert P, Cameron L, Cimini D, Salmon ED, et al. Chromosomes can congress to the metaphase plate before biorientation. Science. 2006;311(5759):388–91. 16424343

21. Bakhoum SF, Compton DA. Kinetochores and disease: keeping microtubule dynamics in check! Curr Opin Cell Biol. 2012;24(1):64–70. doi: 10.1016/j.ceb.2011.11.012 22196931

22. Watanabe Y. Geometry and force behind kinetochore orientation: lessons from meiosis. Nat Rev Mol Cell Biol. 2012;13(6):370–82. doi: 10.1038/nrm3349 22588367

23. Dumont J, Desai A. Acentrosomal spindle assembly and chromosome segregation during oocyte meiosis. Trends Cell Biol. 2012;22(5):241–9. doi: 10.1016/j.tcb.2012.02.007 22480579

24. Varma D, Salmon ED. The KMN protein network—chief conductors of the kinetochore orchestra. J Cell Sci. 2012;125(Pt 24):5927–36. doi: 10.1242/jcs.093724 23418356

25. DeLuca JG, Musacchio A. Structural organization of the kinetochore-microtubule interface. Curr Opin Cell Biol. 2012;24(1):48–56. doi: 10.1016/j.ceb.2011.11.003 22154944

26. Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell. 2006;127(5):983–97. 17129783

27. Schittenhelm RB, Heeger S, Althoff F, Walter A, Heidmann S, Mechtler K, et al. Spatial organization of a ubiquitous eukaryotic kinetochore protein network in Drosophila chromosomes. Chromosoma. 2007;116(4):385–402. 17333235

28. Schittenhelm RB, Chaleckis R, Lehner CF. Intrakinetochore localization and essential functional domains of Drosophila Spc105. Embo J. 2009;28(16):2374–86. doi: 10.1038/emboj.2009.188 19590494

29. Venkei Z, Przewloka MR, Glover DM. Drosophila Mis12 complex acts as a single functional unit essential for anaphase chromosome movement and a robust spindle assembly checkpoint. Genetics. 2011;187(1):131–40. doi: 10.1534/genetics.110.119628 20980244

30. Williams B, Leung G, Maiato H, Wong A, Li Z, Williams EV, et al. Mitch a rapidly evolving component of the Ndc80 kinetochore complex required for correct chromosome segregation in Drosophila. J Cell Sci. 2007;120(Pt 20):3522–33. 17895365

31. DeLuca JG, Dong Y, Hergert P, Strauss J, Hickey JM, Salmon ED, et al. Hec1 and nuf2 are core components of the kinetochore outer plate essential for organizing microtubule attachment sites. Mol Biol Cell. 2005;16(2):519–31. 15548592

32. Feijão T, Afonso O, Maia AF, Sunkel CE. Stability of kinetochore-microtubule attachment and the role of different KMN network components in Drosophila. Cytoskeleton (Hoboken). 2013;70(10):661–75.

33. Przewloka MR, Zhang W, Costa P, Archambault V, D'Avino PP, Lilley KS, et al. Molecular analysis of core kinetochore composition and assembly in Drosophila melanogaster. PLoS One. 2007;2(5):e478. 17534428

34. Basto R, Scaerou F, Mische S, Wojcik E, Lefebvre C, Gomes R, et al. In vivo dynamics of the rough deal checkpoint protein during Drosophila mitosis. Curr Biol. 2004;14(1):56–61. 14711415

35. Gassmann R, Essex A, Hu JS, Maddox PS, Motegi F, Sugimoto A, et al. A new mechanism controlling kinetochore-microtubule interactions revealed by comparison of two dynein-targeting components: SPDL-1 and the Rod/Zwilch/Zw10 complex. Genes Dev. 2008;22(17):2385–99. doi: 10.1101/gad.1687508 18765790

36. Caldas GV, DeLuca JG. KNL1: bringing order to the kinetochore. Chromosoma. 2014;123(3):169–81. doi: 10.1007/s00412-013-0446-5 24310619

37. McCollum D. Monopolin. Curr Biol. 2012;22(22):R937–8. doi: 10.1016/j.cub.2012.09.024 23174290

38. Kim J, Ishiguro K, Nambu A, Akiyoshi B, Yokobayashi S, Kagami A, et al. Meikin is a conserved regulator of meiosis-I-specific kinetochore function. Nature. 2015;517(7535):466–71. doi: 10.1038/nature14097 25533956

39. Bickel SE, Wyman DW, Miyazaki WY, Moore DP, Orr-Weaver TL. Identification of ORD, a Drosophila protein essential for sister chromatid cohesion. EMBO Journal. 1996;15:1451–9. 8635478

40. Kitajima TS, Kawashima SA, Watanabe Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature. 2004;427(6974):510–7. 14730319

41. Yucel JK, Marszalek JD, McIntosh JR, Goldstein LS, Cleveland DW, Philp AV. CENP-meta, an essential kinetochore kinesin required for the maintenance of metaphase chromosome alignment in Drosophila. J Cell Biol. 2000;150(1):1–11. 10893249

42. Chou TB, Perrimon N. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics. 1996;144(4):1673–9. 8978054

43. Gudimchuk N, Vitre B, Kim Y, Kiyatkin A, Cleveland DW, Ataullakhanov FI, et al. Kinetochore kinesin CENP-E is a processive bi-directional tracker of dynamic microtubule tips. Nat Cell Biol. 2013;15(9):1079–88. doi: 10.1038/ncb2831 23955301

44. Maffini S, Maia AR, Manning AL, Maliga Z, Pereira AL, Junqueira M, et al. Motor-independent targeting of CLASPs to kinetochores by CENP-E promotes microtubule turnover and poleward flux. Curr Biol. 2009;19(18):1566–72. doi: 10.1016/j.cub.2009.07.059 19733075

45. Dumont J, Desai A. Acentrosomal spindle assembly and chromosome segregation during oocyte meiosis. Trends Cell Biol. 2012;22(5):241–9. doi: 10.1016/j.tcb.2012.02.007 22480579

46. Jang JK, Rahman T, McKim KS. The kinesin-like protein Subito contributes to central spindle assembly and organization of the meiotic spindle in Drosophila oocytes. Mol Biol Cell. 2005;16(10):4684–94. 16055508

47. Giunta KL, Jang JK, Manheim EA, Subramanian G, McKim KS. subito encodes a kinesin-like protein required for meiotic spindle pole formation in Drosophila melanogaster. Genetics. 2002;160(4):1489–501. 11973304

48. Hartl TA, Smith HF, Bosco G. Chromosome alignment and transvection are antagonized by condensin II. Science. 2008;322(5906):1384–7. doi: 10.1126/science.1164216 19039137

49. Muscat CC, Torre-Santiago KM, Tran MV, Powers JA, Wignall SM. Kinetochore-independent chromosome segregation driven by lateral microtubule bundles. Elife. 2015;4.

50. Sharp DJ, Mennella V, Buster DW. KLP10A and KLP59C: the dynamic duo of microtubule depolymerization. Cell Cycle. 2005;4(11):1482–5. 16205125

51. Rogers GC, Rogers SL, Schwimmer TA, Ems-McClung SC, Walczak CE, Vale RD, et al. Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase. Nature. 2004;427(6972):364–70. 14681690

52. Gui L, Homer H. Spindle assembly checkpoint signalling is uncoupled from chromosomal position in mouse oocytes. Development. 2012;139(11):1941–6. doi: 10.1242/dev.078352 22513372

53. Maia AF, Lopes CS, Sunkel CE. BubR1 and CENP-E have antagonistic effects upon the stability of microtubule-kinetochore attachments in Drosophila S2 cell mitosis. Cell Cycle. 2007;6(11):1367–78. 17525528

54. Godek KM, Kabeche L, Compton DA. Regulation of kinetochore-microtubule attachments through homeostatic control during mitosis. Nat Rev Mol Cell Biol. 2015;16(1):57–64.

55. Nasmyth K. A meiotic mystery: How sister kinetochores avoid being pulled in opposite directions during the first division. Bioessays. 2015;37(6):657–65. doi: 10.1002/bies.201500006 25874377

56. Li X, Dawe RK. Fused sister kinetochores initiate the reductional division in meiosis I. Nat Cell Biol. 2009;11(9):1103–8. doi: 10.1038/ncb1923 19684578.

57. Sakuno T, Tada K, Watanabe Y. Kinetochore geometry defined by cohesion within the centromere. Nature. 2009;458(7240):852–8. doi: 10.1038/nature07876 19370027

58. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, Belcram K, et al. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci. 2005;118(Pt 20):4621–32. 16176934

59. Tzur YB, Egydio de Carvalho C, Nadarajan S, Van Bostelen I, Gu Y, Chu DS, et al. LAB-1 targets PP1 and restricts Aurora B kinase upon entrance into meiosis to promote sister chromatid cohesion. PLoS Biol. 2012;10(8):e1001378. doi: 10.1371/journal.pbio.1001378 22927794

60. Emanuele MJ, Lan W, Jwa M, Miller SA, Chan CS, Stukenberg PT. Aurora B kinase and protein phosphatase 1 have opposing roles in modulating kinetochore assembly. J Cell Biol. 2008;181(2):241–54. doi: 10.1083/jcb.200710019 18426974

61. Kim S, Yu H. Multiple assembly mechanisms anchor the KMN spindle checkpoint platform at human mitotic kinetochores. J Cell Biol. 2015;208(2):181–96. doi: 10.1083/jcb.201407074 25601404

62. Rago F, Gascoigne KE, Cheeseman IM. Distinct organization and regulation of the outer kinetochore KMN network downstream of CENP-C and CENP-T. Curr Biol. 2015;25(5):671–7. doi: 10.1016/j.cub.2015.01.059 25660545

63. Funabiki H, Wynne DJ. Making an effective switch at the kinetochore by phosphorylation and dephosphorylation. Chromosoma. 2013;122(3):135–58. doi: 10.1007/s00412-013-0401-5 23512483

64. Sarangapani KK, Asbury CL. Catch and release: how do kinetochores hook the right microtubules during mitosis? Trends Genet. 2014;30(4):150–9. doi: 10.1016/j.tig.2014.02.004 24631209

65. Yoshida S, Kaido M, Kitajima TS. Inherent Instability of Correct Kinetochore-Microtubule Attachments during Meiosis I in Oocytes. Dev Cell. 2015.

66. Kolano A, Brunet S, Silk AD, Cleveland DW, Verlhac MH. Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. Proc Natl Acad Sci U S A. 2012;109(27):E1858–67. doi: 10.1073/pnas.1204686109 22552228

67. St Pierre SE, Ponting L, Stefancsik R, McQuilton P. FlyBase 102—advanced approaches to interrogating FlyBase. Nucleic Acids Res. 2014;42(Database issue):D780–8. doi: 10.1093/nar/gkt1092 24234449

68. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, Yang-Zhou D, et al. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods. 2011;8(5):405–7. doi: 10.1038/nmeth.1592 21460824

69. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993;118:401–15. 8223268

70. Sugimura I, Lilly MA. Bruno inhibits the expression of mitotic cyclins during the prophase I meiotic arrest of Drosophila oocytes. Dev Cell. 2006;10(1):127–35. 16399084

71. Rorth P. Gal4 in the Drosophila female germline. Mech Dev. 1998;78(1–2):113–8. 9858703

72. Gloor GB, Preston CR, Johnson-Schlitz DM, Nassif NA, Phillis RW, Benz WK, et al. Type I repressors of P element mobility. Genetics. 1993;135(1):81–95. 8224830

73. Casso D, Ramirez-Weber F, Kornberg TB. GFP-tagged balancer chromosomes for Drosophila melanogaster. Mech Dev. 2000;91(1–2):451–4. 10704882

74. Schaar BT, Chan GK, Maddox P, Salmon ED, Yen TJ. CENP-E function at kinetochores is essential for chromosome alignment. J Cell Biol. 1997;139(6):1373–82. 9396744

75. Radford SJ, Harrison AM, McKim KS. Microtubule-depolymerizing Kinesin KLP10A Restricts the Length of the Acentrosomal Meiotic Spindle in Drosophila Females. Genetics. 2012;192:431–40. doi: 10.1534/genetics.112.143503 22865737

76. 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. 16140985

77. Wu C, Singaram V, McKim KS. mei-38 is required for chromosome segregation during meiosis in Drosophila females. Genetics. 2008;180(1):61–72. doi: 10.1534/genetics.108.091140 18757915

78. Blower MD, Karpen GH. The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat Cell Biol. 2001;3(8):730–9. 11483958

79. Matthies HJ, Clarkson M, Saint RB, Namba R, Hawley RS. Analysis of meiosis in fixed and live oocytes by light microscopy. In: Sullivan W, Ashburner M, Hawley RS, editors. Drosophila Protocols. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2000. p. 67–85.

80. McKim KS, Jang JK, Theurkauf WE, Hawley RS. Mechanical basis of meiotic metaphase arrest. Nature. 1993;362(6418):364–6. 8455723

81. Bickel SE, Orr-Weaver TL, Balicky EM. The sister-chromatid cohesion protein ORD is required for chiasma maintenance in Drosophila oocytes. Curr Biol. 2002;12(11):925–9. 12062057

82. Matthies HJ, McDonald HB, Goldstein LS, Theurkauf WE. Anastral meiotic spindle morphogenesis: role of the non-claret disjunctional kinesin-like protein. J Cell Biol. 1996;134(2):455–64. 8707829

83. Cullen CF, Ohkura H. Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nature Cell Biol. 2001;3:637–42. 11433295

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 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#