1932

Abstract

Kinetochores are molecular machines that power chromosome segregation during the mitotic and meiotic cell divisions of all eukaryotes. Aristotle explains how we think we have knowledge of a thing only when we have grasped its cause. In our case, to gain understanding of the kinetochore, the four causes correspond to questions that we must ask: () What are the constituent parts, () how does it assemble, () what is the structure and arrangement, and () what is the function? Here we outline the current blueprint for the assembly of a kinetochore, how functions are mapped onto this architecture, and how this is shaped by the underlying pericentromeric chromatin. The view of the kinetochore that we present is possible because an almost complete parts list of the kinetochore is now available alongside recent advances using in vitro reconstitution, structural biology, and genomics. In many organisms, each kinetochore binds to multiple microtubules, and we propose a model for how this ensemble-level architecture is organized, drawing on key insights from the simple one microtubule–one kinetochore setup in budding yeast and innovations that enable meiotic chromosome segregation.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-072820-034559
2022-11-30
2024-04-17
Loading full text...

Full text loading...

/deliver/fulltext/genet/56/1/annurev-genet-072820-034559.html?itemId=/content/journals/10.1146/annurev-genet-072820-034559&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abad MA, Medina B, Santamaria A, Zou J, Plasberg-Hill C et al. 2014. Structural basis for microtubule recognition by the human kinetochore Ska complex. Nat. Commun. 5:2964
    [Google Scholar]
  2. 2.
    Abad MA, Zou J, Medina-Pritchard B, Nigg EA, Rappsilber J et al. 2016. Ska3 ensures timely mitotic progression by interacting directly with microtubules and Ska1 microtubule binding domain. Sci. Rep 6:134042
    [Google Scholar]
  3. 3.
    Akiyoshi B, Nelson CR, Biggins S. 2013. The Aurora B kinase promotes inner and outer kinetochore interactions in budding yeast. Genetics 194:3785–89
    [Google Scholar]
  4. 4.
    Allan LA, Camacho Reis M, Ciossani G, Huis in ‘t Veld PJ, Wohlgemuth S et al. 2020. Cyclin B1 scaffolds MAD1 at the kinetochore corona to activate the mitotic checkpoint. EMBO J 39:12e103180
    [Google Scholar]
  5. 5.
    Allshire RC, Karpen GH. 2008. Epigenetic regulation of centromeric chromatin: old dogs, new tricks?. Nat. Rev. Genet. 9:12923–37
    [Google Scholar]
  6. 6.
    Allu PK, Dawicki-McKenna JM, Van Eeuwen T, Slavin M, Braitbard M et al. 2019. Structure of the human core centromeric nucleosome complex. Curr. Biol. 29:162625–39.e5
    [Google Scholar]
  7. 7.
    Alushin GM, Musinipally V, Matson D, Tooley J, Stukenberg PT, Nogales E. 2012. Multimodal microtubule binding by the Ndc80 kinetochore complex. Nat. Struct. Mol. Biol. 19:111161–67
    [Google Scholar]
  8. 8.
    Alushin GM, Ramey VH, Pasqualato S, Ball DA, Grigorieff N et al. 2010. The Ndc80 kinetochore complex forms oligomeric arrays along microtubules. Nature 467:7317805–10
    [Google Scholar]
  9. 9.
    Anedchenko EA, Samel-Pommerencke A, Tran Nguyen TM, Shahnejat-Bushehri S, Pöpsel J et al. 2019. The kinetochore module Okp1CENP-Q/Ame1CENP-U is a reader for N-terminal modifications on the centromeric histone Cse4CENP-A. EMBO J 38:1e98991
    [Google Scholar]
  10. 10.
    Aravamudhan P, Goldfarb AA, Joglekar AP. 2015. The kinetochore encodes a mechanical switch to disrupt spindle assembly checkpoint signalling. Nat. Cell Biol. 17:7868–79
    [Google Scholar]
  11. 11.
    Asakawa H, Hayashi A, Haraguchi T, Hiraoka Y. 2005. Dissociation of the Nuf2-Ndc80 complex releases centromeres from the spindle-pole body during meiotic prophase in fission yeast. Mol. Biol. Cell 16:52325–38
    [Google Scholar]
  12. 12.
    Asbury CL, Tien JF, Davis TN. 2011. Kinetochores’ gripping feat: conformational wave or biased diffusion?. Trends Cell Biol 21:138–46
    [Google Scholar]
  13. 13.
    Auckland P, Clarke NI, Royle SJ, McAinsh AD. 2017. Congressing kinetochores progressively load Ska complexes to prevent force-dependent detachment. J. Cell Biol. 216:61623–39
    [Google Scholar]
  14. 14.
    Auckland P, Roscioli E, Coker HLE, McAinsh AD. 2020. CENP-F stabilizes kinetochore-microtubule attachments and limits dynein stripping of corona cargoes. J. Cell Biol. 219:5e201905018
    [Google Scholar]
  15. 15.
    Bancroft J, Auckland P, Samora CP, McAinsh AD. 2015. Chromosome congression is promoted by CENP-Q- and CENP-E-dependent pathways. J. Cell Sci. 128:1171–84
    [Google Scholar]
  16. 16.
    Barton RE, Massari LF, Robertson D, Marston AL. 2022. Eco1-dependent cohesin acetylation anchors chromatin loops and cohesion to define functional meiotic chromosome domains. eLife 11:e74447
    [Google Scholar]
  17. 17.
    Bernard P, Schmidt CK, Vaur S, Dheur S, Drogat J et al. 2008. Cell-cycle regulation of cohesin stability along fission yeast chromosomes. EMBO J 27:1111–21
    [Google Scholar]
  18. 18.
    Berto A, Yu J, Morchoisne-Bolhy S, Bertipaglia C, Vallee R et al. 2018. Disentangling the molecular determinants for Cenp-F localization to nuclear pores and kinetochores. EMBO Rep 19:5 19:e44742
    [Google Scholar]
  19. 19.
    Biggins S. 2013. The composition, functions, and regulation of the budding yeast kinetochore. Genetics 194:4817–46
    [Google Scholar]
  20. 20.
    Blower MD, Sullivan BA, Karpen GH. 2002. Conserved organization of centromeric chromatin in flies and humans. Dev. Cell 2:3319–30
    [Google Scholar]
  21. 21.
    Bock LJ, Pagliuca C, Kobayashi N, Grove RA, Oku Y et al. 2012. Cnn1 inhibits the interactions between the KMN complexes of the yeast kinetochore. Nat. Cell Biol. 14:6614–24
    [Google Scholar]
  22. 22.
    Bodor DL, Mata JF, Sergeev M, David AF, Salimian KJ et al. 2014. The quantitative architecture of centromeric chromatin. eLife 3:3e02137
    [Google Scholar]
  23. 23.
    Boeckmann L, Takahashi Y, Au W-C, Mishra PK, Choy JS et al. 2013. Phosphorylation of centromeric histone H3 variant regulates chromosome segregation in Saccharomyces cerevisiae. Mol. Biol. Cell 24:122034–44
    [Google Scholar]
  24. 24.
    Bonner AM, Hughes SE, Hawley RS. 2020. Regulation of Polo kinase by matrimony is required for cohesin maintenance during Drosophila melanogaster female meiosis. Curr. Biol. 30:4715–22.e3
    [Google Scholar]
  25. 25.
    Bonner MK, Haase J, Swinderman J, Halas H, Miller Jenkins LM, Kelly AE 2019. Enrichment of Aurora B kinase at the inner kinetochore controls outer kinetochore assembly. J. Cell Biol. 218:103237–57
    [Google Scholar]
  26. 26.
    Borek WE, Vincenten N, Duro E, Makrantoni V, Spanos C et al. 2021. The proteomic landscape of centromeric chromatin reveals an essential role for the Ctf19CCAN complex in meiotic kinetochore assembly. Curr. Biol. 31:2283–96.e7
    [Google Scholar]
  27. 27.
    Brar GA, Amon A. 2008. Emerging roles for centromeres in meiosis I chromosome segregation. Nat. Rev. Genet. 9:12899–910
    [Google Scholar]
  28. 28.
    Broad AJ, DeLuca KF, DeLuca JG. 2020. Aurora B kinase is recruited to multiple discrete kinetochore and centromere regions in human cells. J. Cell Biol. 219:3e201905144
    [Google Scholar]
  29. 29.
    Campbell CS, Desai A. 2013. Tension sensing by Aurora B kinase is independent of survivin-based centromere localization. Nature 497:7447118–21
    [Google Scholar]
  30. 30.
    Carroll CW, Milks KJ, Straight AF. 2010. Dual recognition of CENP-A nucleosomes is required for centromere assembly. J. Cell Biol. 189:71143–55
    [Google Scholar]
  31. 31.
    Carroll CW, Silva MCC, Godek KM, Jansen LET, Straight AF. 2009. Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat. Cell Biol. 11:7896–902
    [Google Scholar]
  32. 32.
    Chan YW, Jeyaprakash AA, Nigg EA, Santamaria A. 2012. Aurora B controls kinetochore–microtubule attachments by inhibiting Ska complex–KMN network interaction. J. Cell Biol. 196:5563–71
    [Google Scholar]
  33. 33.
    Cheerambathur DK, Gassmann R, Cook B, Oegema K, Desai A. 2013. Crosstalk between microtubule attachment complexes ensures accurate chromosome segregation. Science 342:61631239–42
    [Google Scholar]
  34. 34.
    Cheerambathur DK, Prevo B, Hattersley N, Lewellyn L, Corbett KD et al. 2017. Dephosphorylation of the Ndc80 tail stabilizes kinetochore-microtubule attachments via the Ska complex. Dev. Cell 41:4424–37.e4
    [Google Scholar]
  35. 35.
    Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A. 2006. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127:5983–97
    [Google Scholar]
  36. 36.
    Chen J, Liao A, Powers EN, Liao H, Kohlstaedt LA et al. 2020. Aurora B-dependent Ndc80 degradation regulates kinetochore composition in meiosis. Genes Dev 34:3–4209–25
    [Google Scholar]
  37. 37.
    Chen J, Tresenrider A, Chia M, McSwiggen DT, Spedale G et al. 2017. Kinetochore inactivation by expression of a repressive mRNA. eLife 6:e27417
    [Google Scholar]
  38. 38.
    Chittori S, Hong J, Saunders H, Feng H, Ghirlando R et al. 2018. Structural mechanisms of centromeric nucleosome recognition by the kinetochore protein CENP-N. Science 359:6373339–43
    [Google Scholar]
  39. 39.
    Cho US, Harrison SC. 2011. Ndc10 is a platform for inner kinetochore assembly in budding yeast. Nat. Struct. Mol. Biol. 19:148–56
    [Google Scholar]
  40. 40.
    Ciferri C, De Luca J, Monzani S, Ferrari KJ, Ristic D et al. 2005. Architecture of the human Ndc80-Hec1 complex, a critical constituent of the outer kinetochore. J. Biol. Chem. 280:3229088–95
    [Google Scholar]
  41. 41.
    Ciferri C, Pasqualato S, Screpanti E, Varetti G, Santaguida S et al. 2008. Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell 133:3427–39
    [Google Scholar]
  42. 42.
    Ciossani G, Overlack K, Petrovic A, Huis in ’t Veld PJ, Koerner C et al. 2018. The kinetochore proteins CENP-E and CENP-F directly and specifically interact with distinct BUB mitotic checkpoint Ser/Thr kinases. J. Biol. Chem. 293:2610084–101
    [Google Scholar]
  43. 43.
    Çivril F, Wehenkel A, Giorgi FM, Santaguida S, Di Fonzo A et al. 2010. Structural analysis of the RZZ complex reveals common ancestry with multisubunit vesicle tethering machinery. Structure 18:5616–26
    [Google Scholar]
  44. 44.
    Cleveland DW, Mao Y, Sullivan KF. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112:4407–21
    [Google Scholar]
  45. 45.
    Cohen RL, Espelin CW, De Wulf P, Sorger PK, Harrison SC, Simons KT. 2008. Structural and functional dissection of Mif2p, a conserved DNA-binding kinetochore protein. Mol. Biol. Cell 19:104480–91
    [Google Scholar]
  46. 46.
    Cole HA, Howard BH, Clark DJ. 2011. The centromeric nucleosome of budding yeast is perfectly positioned and covers the entire centromere. PNAS 108:3112687–92
    [Google Scholar]
  47. 47.
    Corbett KD, Harrison SC. 2016. Molecular architecture of the yeast monopolin complex. Cell Rep 17:3583–89
    [Google Scholar]
  48. 48.
    Corbett KD, Yip CK, Ee L-S, Walz T, Amon A, Harrison SC. 2010. The monopolin complex crosslinks kinetochore components to regulate chromosome-microtubule attachments. Cell 142:4556–67
    [Google Scholar]
  49. 49.
    Costantino L, Hsieh T-HS, Lamothe R, Darzacq X, Koshland D. 2020. Cohesin residency determines chromatin loop patterns. eLife 9:e59889
    [Google Scholar]
  50. 50.
    Cross RA, McAinsh A. 2014. Prime movers: the mechanochemistry of mitotic kinesins. Nat. Rev. Mol. Cell Biol. 15:4257–71
    [Google Scholar]
  51. 51.
    Currie CE, Mora-Santos M, Smith CA, McAinsh AD, Millar JBA. 2018. Bub1 is not essential for the checkpoint response to unattached kinetochores in diploid human cells. Curr. Biol. 28:17R929–30
    [Google Scholar]
  52. 52.
    De Wulf P, McAinsh AD, Sorger PK. 2003. Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev 17:232902–21
    [Google Scholar]
  53. 53.
    Debose-Scarlett EM, Sullivan BA. 2021. Genomic and epigenetic foundations of neocentromere formation. Annu. Rev. Genet. 55:331–48
    [Google Scholar]
  54. 54.
    Dechassa ML, Wyns K, Luger K. 2014. Scm3 deposits a (Cse4–H4)2 tetramer onto DNA through a Cse4–H4 dimer intermediate. Nucleic Acids Res 42:95532–42
    [Google Scholar]
  55. 55.
    del Castillo U, Norkett R, Gelfand VI. 2019. Unconventional roles of cytoskeletal mitotic machinery in neurodevelopment. Trends Cell Biol 29:11901–11
    [Google Scholar]
  56. 56.
    Dimitrova YN, Jenni S, Valverde R, Khin Y, Harrison SC 2016. Structure of the MIND complex defines a regulatory focus for yeast kinetochore assembly. Cell 167:41014–27.e12
    [Google Scholar]
  57. 57.
    Dong Y, Vanden Beldt KJ, Meng X, Khodjakov A, McEwen BF 2007. The outer plate in vertebrate kinetochores is a flexible network with multiple microtubule interactions. Nat. Cell Biol. 9:5516–22
    [Google Scholar]
  58. 58.
    Doodhi H, Tanaka TU. 2022. Swap and stop—Kinetochores play error correction with microtubules: mechanisms of kinetochore–microtubule error correction. Bioessays 44:e2100246
    [Google Scholar]
  59. 59.
    Drechsler H, McAinsh AD. 2012. Exotic mitotic mechanisms. Open Biol 2:12120140
    [Google Scholar]
  60. 60.
    Dudziak A, Engelhard L, Bourque C, Klink BU, Rombaut P et al. 2021. Phospho-regulated Bim1/EB1 interactions trigger Dam1c ring assembly at the budding yeast outer kinetochore. EMBO J 40:18e108004
    [Google Scholar]
  61. 61.
    Dumont M, Gamba R, Gestraud P, Klaasen S, Worrall JT et al. 2020. Human chromosome-specific aneuploidy is influenced by DNA-dependent centromeric features. EMBO J 39:2e102924
    [Google Scholar]
  62. 62.
    Dunsch AK, Linnane E, Barr FA, Gruneberg U. 2011. The astrin–kinastrin/SKAP complex localizes to microtubule plus ends and facilitates chromosome alignment. J. Cell Biol. 192:6959–68
    [Google Scholar]
  63. 63.
    Duro E, Marston AL. 2015. From equator to pole: splitting chromosomes in mitosis and meiosis. Genes Dev 29:2109–22
    [Google Scholar]
  64. 64.
    Eckert CA, Gravdahl DJ, Megee PC. 2007. The enhancement of pericentric cohesin association by conserved kinetochore components promotes high-fidelity chromosome segregation and is sensitive to microtubule-based tension. Genes Dev 21:3278–91
    [Google Scholar]
  65. 65.
    Falk SJ, Guo LY, Sekulic N, Smoak EM, Mani T et al. 2015. CENP-C reshapes and stabilizes CENP-A nucleosomes at the centromere. Science 348:6235699–703
    [Google Scholar]
  66. 66.
    Fernius J, Marston AL. 2009. Establishment of cohesion at the pericentromere by the Ctf19 kinetochore subcomplex and the replication fork-associated factor, Csm3. PLOS Genet 5:9e1000629
    [Google Scholar]
  67. 67.
    Fernius J, Nerusheva OO, Galander S, de Lima Alves F, Rappsilber J, Marston AL. 2013. Cohesin-dependent association of Scc2/4 with the centromere initiates pericentromeric cohesion establishment. Curr. Biol. 23:7599–606
    [Google Scholar]
  68. 68.
    Fischböck-Halwachs J, Singh S, Potocnjak M, Hagemann G, Solis-Mezarino V et al. 2019. The COMA complex interacts with Cse4 and positions Sli15/Ipl1 at the budding yeast inner kinetochore. eLife 8:e42879
    [Google Scholar]
  69. 69.
    Foltz DR, Jansen LET, Bailey AO, Yates JR, Bassett EA et al. 2009. Centromere-specific assembly of CENP-A nucleosomes is mediated by HJURP. Cell 137:3472–84
    [Google Scholar]
  70. 70.
    Foltz DR, Jansen LET, Black BE, Bailey AO, Yates JR, Cleveland DW. 2006. The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 8:5458–69
    [Google Scholar]
  71. 71.
    Friese A, Faesen AC, Huis in 't Veld PJ, Fischböck J, Prumbaum D et al. 2016. Molecular requirements for the inter-subunit interaction and kinetochore recruitment of SKAP and Astrin. Nat. Commun. 7:11407
    [Google Scholar]
  72. 72.
    Furuyama S, Biggins S. 2007. Centromere identity is specified by a single centromeric nucleosome in budding yeast. PNAS 104:3714706–11
    [Google Scholar]
  73. 73.
    Galander S, Barton RE, Borek WE, Spanos C, Kelly DA et al. 2019. Reductional meiosis I chromosome segregation is established by coordination of key meiotic kinases. Dev. Cell 49:4526–41.e5
    [Google Scholar]
  74. 74.
    Galander S, Marston AL. 2020. Meiosis I kinase regulators: conserved orchestrators of reductional chromosome segregation. Bioessays 42:102000018
    [Google Scholar]
  75. 75.
    García-Rodríguez LJ, Kasciukovic T, Denninger V, Tanaka TU. 2019. Aurora B-INCENP localization at centromeres/inner kinetochores is required for chromosome bi-orientation in budding yeast. Curr. Biol. 29:91536–44.e4
    [Google Scholar]
  76. 76.
    Gartenberg M. 2009. Heterochromatin and the cohesion of sister chromatids. Chromosom. Res. 17:2229–38
    [Google Scholar]
  77. 77.
    Gascoigne KE, Takeuchi K, Suzuki A, Hori T, Fukagawa T, Cheeseman IM. 2011. Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 145:3410–22
    [Google Scholar]
  78. 78.
    Gassmann R, Holland AJ, Varma D, Wan X, Çivril F et al. 2010. Removal of Spindly from microtubule-attached kinetochores controls spindle checkpoint silencing in human cells. Genes Dev 24:9957–71
    [Google Scholar]
  79. 79.
    Ghongane P, Kapanidou M, Asghar A, Elowe S, Bolanos-Garcia VM. 2014. The dynamic protein Knl1—a kinetochore rendezvous. J. Cell Sci. 127:Part 163415–23
    [Google Scholar]
  80. 80.
    Glynn EF, Megee PC, Yu H-G, Mistrot C, Unal E et al. 2004. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLOS Biol 2:9e259
    [Google Scholar]
  81. 81.
    Goldstein LS. 1981. Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. Cell 25:3591–602
    [Google Scholar]
  82. 82.
    Gonen S, Akiyoshi B, Iadanza MG, Shi D, Duggan N et al. 2012. The structure of purified kinetochores reveals multiple microtubule-attachment sites. Nat. Struct. Mol. Biol. 19:9925–29
    [Google Scholar]
  83. 83.
    Gregan J, Riedel CG, Pidoux AL, Katou Y, Rumpf C et al. 2007. The kinetochore proteins Pcs1 and Mde4 and heterochromatin are required to prevent merotelic orientation. Curr. Biol. 17:141190–1200
    [Google Scholar]
  84. 84.
    Gruhn JR, Zielinska AP, Shukla V, Blanshard R, Capalbo A et al. 2019. Chromosome errors in human eggs shape natural fertility over reproductive life span. Science 365:64601466–69
    [Google Scholar]
  85. 85.
    Gryaznova Y, Keating L, Touati SA, Cladière D, El Yakoubi W et al. 2021. Kinetochore individualization in meiosis I is required for centromeric cohesin removal in meiosis II. EMBO J 40:7e106797
    [Google Scholar]
  86. 86.
    Guan R, Lian T, Zhou B-R, He E, Wu C et al. 2021. Structural and dynamic mechanisms of CBF3-guided centromeric nucleosome formation. Nat. Commun. 12:11763
    [Google Scholar]
  87. 87.
    Gudimchuk NB, McIntosh JR. 2021. Regulation of microtubule dynamics, mechanics and function through the growing tip. Nat. Rev. Mol. Cell Biol. 22:12777–95
    [Google Scholar]
  88. 88.
    Gudimchuk NB, Vitre B, Kim Y, Kiyatkin A, Cleveland DW et al. 2013. Kinetochore kinesin CENP-E is a processive bi-directional tracker of dynamic microtubule tips. Nat. Cell Biol. 15:91079–88
    [Google Scholar]
  89. 89.
    Guo LY, Allu PK, Zandarashvili L, McKinley KL, Sekulic N et al. 2017. Centromeres are maintained by fastening CENP-A to DNA and directing an arginine anchor-dependent nucleosome transition. Nat. Commun. 8:15775
    [Google Scholar]
  90. 90.
    Hara M, Ariyoshi M, Okumura E-I, Hori T, Fukagawa T. 2018. Multiple phosphorylations control recruitment of the KMN network onto kinetochores. Nat. Cell Biol. 20:121378–88
    [Google Scholar]
  91. 91.
    Hara M, Fukagawa T. 2020. Dynamics of kinetochore structure and its regulations during mitotic progression. Cell. Mol. Life Sci. 77:2981–95
    [Google Scholar]
  92. 92.
    Helgeson LA, Zelter A, Riffle M, MacCoss MJ, Asbury CL, Davis TN. 2018. Human Ska complex and Ndc80 complex interact to form a load-bearing assembly that strengthens kinetochore–microtubule attachments. PNAS 115:112740–45
    [Google Scholar]
  93. 93.
    Hill TL. 1985. Theoretical problems related to the attachment of microtubules to kinetochores. PNAS 82:134404–8
    [Google Scholar]
  94. 94.
    Hindriksen S, Lens SMA, Hadders MA. 2017. The ins and outs of Aurora B inner centromere localization. Front. Cell Dev. Biol. 5:112
    [Google Scholar]
  95. 95.
    Hinshaw SM, Dates AN, Harrison SC. 2019. The structure of the yeast Ctf3 complex. eLife 8:e48215
    [Google Scholar]
  96. 96.
    Hinshaw SM, Harrison SC. 2019. The structure of the Ctf19c/CCAN from budding yeast. eLife 8:e44239
    [Google Scholar]
  97. 97.
    Hinshaw SM, Harrison SC. 2020. The structural basis for kinetochore stabilization by Cnn1/CENP-T. Curr. Biol. 30:173425–31.e3
    [Google Scholar]
  98. 98.
    Hinshaw SM, Makrantoni V, Harrison SC, Marston AL. 2017. The kinetochore receptor for the cohesin loading complex. Cell 171:172–84.e13
    [Google Scholar]
  99. 99.
    Hinshaw SM, Makrantoni V, Kerr A, Marston AL, Harrison SC. 2015. Structural evidence for Scc4-dependent localization of cohesin loading. eLife 4:e06057
    [Google Scholar]
  100. 100.
    Hori T, Amano M, Suzuki A, Backer CB, Welburn JP et al. 2008. CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135:61039–52
    [Google Scholar]
  101. 101.
    Hornung P, Maier M, Alushin GM, Lander GC, Nogales E, Westermann S. 2011. Molecular architecture and connectivity of the budding yeast Mtw1 kinetochore complex. J. Mol. Biol. 405:2548–59
    [Google Scholar]
  102. 102.
    Hornung P, Troc P, Malvezzi F, Maier M, Demianova Z et al. 2014. A cooperative mechanism drives budding yeast kinetochore assembly downstream of CENP-A. J. Cell Biol. 206:4509–24
    [Google Scholar]
  103. 103.
    Howell BJ, McEwen BF, Canman JC, Hoffman DB, Farrar EM et al. 2001. Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J. Cell Biol. 155:71159–72
    [Google Scholar]
  104. 104.
    Huis in ’t Veld PJ, Jeganathan S, Petrovic A, Singh P, John J et al. 2016. Molecular basis of outer kinetochore assembly on CENP-T. eLife 5:e21007
    [Google Scholar]
  105. 105.
    Huis in ’t Veld PJ, Volkov VA, Stender ID, Musacchio A, Dogterom M. 2019. Molecular determinants of the Ska-Ndc80 interaction and their influence on microtubule tracking and force-coupling. eLife 8:e49539
    [Google Scholar]
  106. 106.
    Ishii M, Akiyoshi B. 2022. Plasticity in centromere organization and kinetochore composition: lessons from diversity. Curr. Opin. Cell Biol. 74:47–54
    [Google Scholar]
  107. 107.
    Izuta H, Ikeno M, Suzuki N, Tomonaga T, Nozaki N et al. 2006. Comprehensive analysis of the ICEN (Interphase Centromere Complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 11:6673–84
    [Google Scholar]
  108. 108.
    Janczyk P, Skorupka KA, Tooley JG, Matson DR, Kestner CA et al. 2017. Mechanism of Ska recruitment by Ndc80 complexes to kinetochores. Dev. Cell 41:4438–49.e4
    [Google Scholar]
  109. 109.
    Jenni S, Harrison SC 2018. Structure of the DASH/Dam1 complex shows its role at the yeast kinetochore-microtubule interface. Science 360:6388552–58
    [Google Scholar]
  110. 110.
    Jeyaprakash AA, Santamaria A, Jayachandran U, Chan YW, Benda C et al. 2012. Structural and functional organization of the Ska complex, a key component of the kinetochore-microtubule interface. Mol. Cell 46:3274–86
    [Google Scholar]
  111. 111.
    Joglekar AP, Bloom K, Salmon ED. 2009. In vivo protein architecture of the eukaryotic kinetochore with nanometer scale accuracy. Curr. Biol. 19:8694–99
    [Google Scholar]
  112. 112.
    Joglekar AP, Kukreja AA. 2017. How kinetochore architecture shapes the mechanisms of its function. Curr. Biol. 27:16R816–24
    [Google Scholar]
  113. 113.
    Johnston K, Joglekar A, Hori T, Suzuki A, Fukagawa T, Salmon ED. 2010. Vertebrate kinetochore protein architecture: protein copy number. J. Cell Biol. 189:6937–43
    [Google Scholar]
  114. 114.
    Jokelainen PT. 1967. The ultrastructure and spatial organization of the metaphase kinetochore in mitotic rat cells. J. Ultrastruct. Res. 19:119–44
    [Google Scholar]
  115. 115.
    Kanfer G, Peterka M, Arzhanik VK, Drobyshev AL, Ataullakhanov FI et al. 2017. CENP-F couples cargo to growing and shortening microtubule ends. Mol. Biol. Cell 28:182400–9
    [Google Scholar]
  116. 116.
    Kang YH, Park CH, Kim T-S, Soung N-K, Bang JK et al. 2011. Mammalian polo-like kinase 1-dependent regulation of the PBIP1-CENP-Q complex at kinetochores. J. Biol. Chem. 286:2219744–57
    [Google Scholar]
  117. 117.
    Katis VL, Matos J, Mori S, Shirahige K, Zachariae W, Nasmyth K. 2004. Spo13 facilitates monopolin recruitment to kinetochores and regulates maintenance of centromeric cohesion during yeast meiosis. Curr. Biol. 14:242183–96
    [Google Scholar]
  118. 118.
    Kato H, Jiang J, Zhou BR, Rozendaal M, Feng H et al. 2013. A conserved mechanism for centromeric nucleosome recognition by centromere protein CENP-C. Science 340:61361110–13
    [Google Scholar]
  119. 119.
    Kern DM, Monda JK, Su KC, Wilson-Kubalek EM, Cheeseman IM. 2017. Astrin-SKAP complex reconstitution reveals its kinetochore interaction with microtubule-bound Ndc80. eLife 6:e26866
    [Google Scholar]
  120. 120.
    Kiewisz R, Fabig G, Conway W, Baum D, Needleman DJ, Müller-Reichert T. 2022. Three-dimensional structure of kinetochore-fibers in human mitotic spindles. eLife 11:e75459
    [Google Scholar]
  121. 121.
    Killinger K, Böhm M, Steinbach P, Hagemann G, Blüggel M et al. 2020. Auto-inhibition of Mif2/CENP-C ensures centromere-dependent kinetochore assembly in budding yeast. EMBO J 39:e102938
    [Google Scholar]
  122. 122.
    Kim J, Ishiguro K-I, Nambu A, Akiyoshi B, Yokobayashi S et al. 2015. Meikin is a conserved regulator of meiosis-I-specific kinetochore function. Nature 517:7535466–71
    [Google Scholar]
  123. 123.
    Kim JO, Zelter A, Umbreit NT, Bollozos A, Riffle M et al. 2017. The Ndc80 complex bridges two Dam1 complex rings. eLife 6:e21069
    [Google Scholar]
  124. 124.
    Kim S, Yu H. 2015. Multiple assembly mechanisms anchor the KMN spindle checkpoint platform at human mitotic kinetochores. J. Cell Biol. 208:2181–96
    [Google Scholar]
  125. 125.
    Kitamura E, Tanaka K, Kitamura Y, Tanaka TU. 2007. Kinetochore–microtubule interaction during S phase in Saccharomyces cerevisiae. Genes Dev 21:243319–30
    [Google Scholar]
  126. 126.
    Klare K, Weir JR, Basilico F, Zimniak T, Massimiliano L et al. 2015. CENP-C is a blueprint for constitutive centromere-associated network assembly within human kinetochores. J. Cell Biol. 210:111–22
    [Google Scholar]
  127. 127.
    Koch B, Kueng S, Ruckenbauer C, Wendt KS, Peters JM. 2008. The Suv39h–HP1 histone methylation pathway is dispensable for enrichment and protection of cohesin at centromeres in mammalian cells. Chromosoma 117:2199–210
    [Google Scholar]
  128. 128.
    Kops GJPL, Gassmann R. 2020. Crowning the kinetochore: the fibrous corona in chromosome segregation. Trends Cell Biol 30:8653–67
    [Google Scholar]
  129. 129.
    Kops GJPL, Kim Y, Weaver BAA, Mao Y, McLeod I et al. 2005. ZW10 links mitotic checkpoint signaling to the structural kinetochore. J. Cell Biol. 169:149–60
    [Google Scholar]
  130. 130.
    Krenn V, Wehenkel A, Li X, Santaguida S, Musacchio A. 2012. Structural analysis reveals features of the spindle checkpoint kinase Bub1–kinetochore subunit Knl1 interaction. J. Cell Biol. 196:4451–67
    [Google Scholar]
  131. 131.
    Kuhl LM, Vader G. 2019. Kinetochores, cohesin, and DNA breaks: controlling meiotic recombination within pericentromeres. Yeast 36:3121–27
    [Google Scholar]
  132. 132.
    Kukreja AA, Kavuri S, Joglekar AP. 2020. Microtubule attachment and centromeric tension shape the protein architecture of the human kinetochore. Curr. Biol. 30:244869–81.e5
    [Google Scholar]
  133. 133.
    Lampert F, Hornung P, Westermann S. 2010. The Dam1 complex confers microtubule plus end-tracking activity to the Ndc80 kinetochore complex. J. Cell Biol. 189:4641–49
    [Google Scholar]
  134. 134.
    Lampert F, Mieck C, Alushin GM, Nogales E, Westermann S. 2013. Molecular requirements for the formation of a kinetochore–microtubule interface by Dam1 and Ndc80 complexes. J. Cell Biol. 200:121–30
    [Google Scholar]
  135. 135.
    Lampson MA, Cheeseman IM. 2011. Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends Cell Biol 21:3133–40
    [Google Scholar]
  136. 136.
    Lampson MA, Grishchuk EL. 2017. Mechanisms to avoid and correct erroneous kinetochore-microtubule attachments. Biology 6:11
    [Google Scholar]
  137. 137.
    Lang J, Barber A, Biggins S. 2018. An assay for de novo kinetochore assembly reveals a key role for the CENP-T pathway in budding yeast. eLife 7:e37819
    [Google Scholar]
  138. 138.
    Lara-Gonzalez P, Pines J, Desai A. 2021. Spindle assembly checkpoint activation and silencing at kinetochores. Semin. Cell Dev. Biol. 117:86–98
    [Google Scholar]
  139. 139.
    Lazar-Stefanita L, Scolari VF, Mercy G, Muller HH, Guérin TM et al. 2017. Cohesins and condensins orchestrate the 4D dynamics of yeast chromosomes during the cell cycle. EMBO J 36:182684–97
    [Google Scholar]
  140. 140.
    Leber V, Nans A, Singleton MR. 2018. Structural basis for assembly of the CBF3 kinetochore complex. EMBO J 37:2269–81
    [Google Scholar]
  141. 141.
    Leclerc S, Kitagawa K. 2021. The role of human centromeric RNA in chromosome stability. Front. Mol. Biosci. 8:170
    [Google Scholar]
  142. 142.
    Lee BH, Kiburz BM, Amon A. 2004. Spo13 maintains centromeric cohesion and kinetochore coorientation during meiosis I. Curr. Biol. 14:242168–82
    [Google Scholar]
  143. 143.
    Li X, Dawe RK. 2009. Fused sister kinetochores initiate the reductional division in meiosis I. Nat. Cell Biol 11:91103–8
    [Google Scholar]
  144. 144.
    Li Y, Bachant J, Alcasabas AA, Wang Y, Qin J, Elledge SJ. 2002. The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev 16:2183–97
    [Google Scholar]
  145. 145.
    Li Y, Haarhuis JHI, Sedeño Cacciatore Á, Oldenkamp R, van Ruiten MS et al. 2020. The structural basis for cohesin–CTCF-anchored loops. Nature 578:7795472–76
    [Google Scholar]
  146. 146.
    London N, Biggins S. 2014. Mad1 kinetochore recruitment by Mps1-mediated phosphorylation of Bub1 signals the spindle checkpoint. Genes Dev 28:2140–52
    [Google Scholar]
  147. 147.
    Long AF, Kuhn J, Dumont S. 2019. The mammalian kinetochore-microtubule interface: robust mechanics and computation with many microtubules. Curr. Opin. Cell Biol. 60:60–67
    [Google Scholar]
  148. 148.
    Ma W, Zhou J, Chen J, Carr AM, Watanabe Y. 2021. Meikin synergizes with shugoshin to protect cohesin Rec8 during meiosis I. Genes Dev 35:9–10692–97
    [Google Scholar]
  149. 149.
    Maciejowski J, Drechsler H, Grundner-Culemann K, Ballister ER, Rodriguez-Rodriguez JA et al. 2017. Mps1 regulates kinetochore-microtubule attachment stability via the Ska complex to ensure error-free chromosome segregation. Dev. Cell 41:2143–56.e6
    [Google Scholar]
  150. 150.
    Magidson V, He J, Ault JG, O'Connell CB, Yang N et al. 2016. Unattached kinetochores rather than intrakinetochore tension arrest mitosis in taxol-treated cells. J. Cell Biol. 212:3307–19
    [Google Scholar]
  151. 151.
    Maier NK, Ma J, Lampson MA, Cheeseman IM. 2021. Separase cleaves the kinetochore protein Meikin at the meiosis I/II transition. Dev. Cell 56:152192–206.e8
    [Google Scholar]
  152. 152.
    Malvezzi F, Litos G, Schleiffer A, Heuck A, Mechtler K et al. 2013. A structural basis for kinetochore recruitment of the Ndc80 complex via two distinct centromere receptors. EMBO J 32:3409–23
    [Google Scholar]
  153. 153.
    Manning AL, Bakhoum SF, Maffini S, Correia-Melo C, Maiato H, Compton DA. 2010. CLASP1, astrin and Kif2b form a molecular switch that regulates kinetochore-microtubule dynamics to promote mitotic progression and fidelity. EMBO J 29:203531–43
    [Google Scholar]
  154. 154.
    Marco E, Dorn JF, Hsu PH, Jaqaman K, Sorger PK, Danuser G. 2013. S. cerevisiae chromosomes biorient via gradual resolution of syntely between S phase and anaphase. Cell 154:51127–39
    [Google Scholar]
  155. 155.
    Marston AL. 2014. Chromosome segregation in budding yeast: sister chromatid cohesion and related mechanisms. Genetics 196:131–63
    [Google Scholar]
  156. 156.
    Marston AL. 2015. Shugoshins: tension-sensitive pericentromeric adaptors safeguarding chromosome segregation. Mol. Cell Biol 35:4634–48
    [Google Scholar]
  157. 157.
    Maskell DP, Hu XW, Singleton MR. 2010. Molecular architecture and assembly of the yeast kinetochore MIND complex. J. Cell Biol. 190:5823–34
    [Google Scholar]
  158. 158.
    Matos J, Lipp JJ, Bogdanova A, Guillot S, Okaz E et al. 2008. Dbf4-dependent Cdc7 kinase links DNA replication to the segregation of homologous chromosomes in meiosis I. Cell 135:4662–78
    [Google Scholar]
  159. 159.
    McAinsh AD, Tytell JD, Sorger PK. 2003. Structure, function, and regulation of budding yeast kinetochores. Annu. Rev. Cell Dev. Biol. 19:519–39
    [Google Scholar]
  160. 160.
    McClelland SE, Borusu S, Amaro AC, Winter JR, Belwal M et al. 2007. The CENP-A NAC/CAD kinetochore complex controls chromosome congression and spindle bipolarity. EMBO J 26:245033–47
    [Google Scholar]
  161. 161.
    McKinley KL, Sekulic N, Guo LY, Tsinman T, Black BE, Cheeseman IM. 2015. The CENP-L-N complex forms a critical node in an integrated meshwork of interactions at the centromere-kinetochore interface. Mol. Cell 60:6886–98
    [Google Scholar]
  162. 162.
    Measday V, Hailey DW, Pot I, Givan SA, Hyland KM et al. 2002. Ctf3p, the Mis6 budding yeast homolog, interacts with Mcm22p and Mcm16p at the yeast outer kinetochore. Genes Dev. 16:1101–13
    [Google Scholar]
  163. 163.
    Medina-Pritchard B, Lazou V, Zou J, Byron O, Abad MA et al. 2020. Structural basis for centromere maintenance by Drosophila CENP-A chaperone CAL1. EMBO J 39:7e103234
    [Google Scholar]
  164. 164.
    Mellone BG, Fachinetti D. 2021. Diverse mechanisms of centromere specification. Curr. Biol. 31:22R1491–504
    [Google Scholar]
  165. 165.
    Meraldi P, McAinsh AD, Rheinbay E, Sorger PK. 2006. Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7:3R23
    [Google Scholar]
  166. 166.
    Meyer RE, Chuong HH, Hild M, Hansen CL, Kinter M, Dawson DS. 2015. Ipl1/Aurora-B is necessary for kinetochore restructuring in meiosis I in Saccharomyces cerevisiae. Mol. Biol. Cell 26:172986–3000
    [Google Scholar]
  167. 167.
    Milks KJ, Moree B, Straight AF. 2009. Dissection of CENP-C-directed centromere and kinetochore assembly. Mol. Biol. Cell 20:194246–55
    [Google Scholar]
  168. 168.
    Miller MP, Ünal E, Brar GA, Amon A. 2012. Meiosis I chromosome segregation is established through regulation of microtubule-kinetochore interactions. eLife 2012:1e00117
    [Google Scholar]
  169. 169.
    Miranda JJL, De Wulf P, Sorger PK, Harrison SC. 2005. The yeast DASH complex forms closed rings on microtubules. Nat. Struct. Mol. Biol. 12:2138–43
    [Google Scholar]
  170. 170.
    Miyazaki S, Kim J, Yamagishi Y, Ishiguro T, Okada Y et al. 2017. Meikin-associated polo-like kinase specifies Bub1 distribution in meiosis I. Genes Cells 22:6552–67
    [Google Scholar]
  171. 171.
    Mizuguchi G, Xiao H, Wisniewski J, Smith MM, Wu C. 2007. Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129:61153–64
    [Google Scholar]
  172. 172.
    Monda JK, Whitney IP, Tarasovetc EV, Wilson-Kubalek E, Milligan RA et al. 2017. Microtubule tip tracking by the spindle and kinetochore protein Ska1 requires diverse tubulin-interacting surfaces. Curr. Biol. 27:233666–75.e6
    [Google Scholar]
  173. 173.
    Mosalaganti S, Keller J, Altenfeld A, Winzker M, Rombaut P et al. 2017. Structure of the RZZ complex and molecular basis of its interaction with Spindly. J. Cell Biol. 216:4961–81
    [Google Scholar]
  174. 174.
    Nambu M, Kishikawa A, Yamada T, Ichikawa K, Kira Y et al. 2022. Direct evaluation of cohesin-mediated sister kinetochore associations at meiosis I in fission yeast. J. Cell Sci. 135:1jcs259102
    [Google Scholar]
  175. 175.
    Nguyen AL, Fadel MD, Cheeseman IM. 2021. Differential requirements for the CENP-O complex reveal parallel PLK1 kinetochore recruitment pathways. Mol. Biol. Cell 32:8712–21
    [Google Scholar]
  176. 176.
    Nishimura K, Komiya M, Hori T, Itoh T, Fukagawa T. 2019. 3D genomic architecture reveals that neocentromeres associate with heterochromatin regions. J. Cell Biol. 218:1134–49
    [Google Scholar]
  177. 177.
    Nishino T, Rago F, Hori T, Tomii K, Cheeseman IM, Fukagawa T. 2013. CENP-T provides a structural platform for outer kinetochore assembly. EMBO J 32:3424–36
    [Google Scholar]
  178. 178.
    Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M et al. 2002. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat. Cell Biol 4:189–93
    [Google Scholar]
  179. 179.
    Obeso D, Pezza RJ, Dawson D 2014. Couples, pairs, and clusters: mechanisms and implications of centromere associations in meiosis. Chromosoma 123:1–243–55
    [Google Scholar]
  180. 180.
    Ogushi S, Rattani A, Godwin J, Metson J, Schermelleh L, Nasmyth K. 2021. Loss of sister kinetochore co-orientation and peri-centromeric cohesin protection after meiosis I depends on cleavage of centromeric REC8. Dev. Cell 56:223100–14.e4
    [Google Scholar]
  181. 181.
    Okada M, Cheeseman IM, Hori T, Okawa K, McLeod IX et al. 2006. The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat. Cell Biol. 8:5446–57
    [Google Scholar]
  182. 182.
    Ortiz J, Stemmann O, Rank S, Lechner J. 1999. A putative protein complex consisting of Ctf19, Mcm21, and Okp1 represents a missing link in the budding yeast kinetochore. Genes Dev 13:91140–55
    [Google Scholar]
  183. 183.
    O'Toole E, Morphew M, McIntosh JR. 2020. Electron tomography reveals aspects of spindle structure important for mechanical stability at metaphase. Mol. Biol. Cell 31:3184–95
    [Google Scholar]
  184. 184.
    Paldi F, Alver B, Robertson D, Schalbetter SA, Kerr A et al. 2020. Convergent genes shape budding yeast pericentromeres. Nature 582:7810119–23
    [Google Scholar]
  185. 185.
    Paliulis LV, Nicklas RB. 2000. The reduction of chromosome number in meiosis is determined by properties built into the chromosomes. J. Cell Biol. 150:61223–31
    [Google Scholar]
  186. 186.
    Patel J, Tan SL, Hartshorne GM, McAinsh AD. 2015. Unique geometry of sister kinetochores in human oocytes during meiosis I may explain maternal age-associated increases in chromosomal abnormalities. Biol. Open 5:2178–84
    [Google Scholar]
  187. 187.
    Pekgöz Altunkaya G, Malvezzi F, Demianova Z, Zimniak T, Litos G et al. 2016. CCAN assembly configures composite binding interfaces to promote cross-linking of Ndc80 complexes at the kinetochore. Curr. Biol. 26:172370–78
    [Google Scholar]
  188. 188.
    Pentakota S, Zhou K, Smith C, Maffini S, Petrovic A et al. 2017. Decoding the centromeric nucleosome through CENP-N. eLife 6:e33442
    [Google Scholar]
  189. 189.
    Pereira C, Reis RM, Gama JB, Celestino R, Cheerambathur DK et al. 2018. Self-assembly of the RZZ complex into filaments drives kinetochore expansion in the absence of microtubule attachment. Curr. Biol. 28:213408–21.e8
    [Google Scholar]
  190. 190.
    Pesenti ME, Prumbaum D, Auckland P, Smith CM, Faesen AC et al. 2018. Reconstitution of a 26-subunit human kinetochore reveals cooperative microtubule binding by CENP-OPQUR and NDC80. Mol. Cell 71:6923–39.e10
    [Google Scholar]
  191. 191.
    Pesenti ME, Raisch T, Conti D, Hoffmann I, Vogt D et al. 2022. Structure of the human inner kinetochore CCAN complex and its significance for human centromere organization. Mol. Cell 82:2113–31.e8
    [Google Scholar]
  192. 192.
    Pesenti ME, Weir JR, Musacchio A. 2016. Progress in the structural and functional characterization of kinetochores. Curr. Opin. Struct. Biol. 37:152–63
    [Google Scholar]
  193. 193.
    Petronczki M, Matos J, Mori S, Gregan J, Bogdanova A et al. 2006. Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 126:61049–64
    [Google Scholar]
  194. 194.
    Petrovic A, Keller J, Liu Y, Overlack K, John J et al. 2016. Structure of the MIS12 complex and molecular basis of its interaction with CENP-C at human kinetochores. Cell 167:41028–40.e15
    [Google Scholar]
  195. 195.
    Petrovic A, Mosalaganti S, Keller J, Mattiuzzo M, Overlack K et al. 2014. Modular assembly of RWD domains on the Mis12 complex underlies outer kinetochore organization. Mol. Cell 53:4591–605
    [Google Scholar]
  196. 196.
    Petrovic A, Pasqualato S, Dube P, Krenn V, Santaguida S et al. 2010. The MIS12 complex is a protein interaction hub for outer kinetochore assembly. J. Cell Biol. 190:5835–52
    [Google Scholar]
  197. 197.
    Plowman R, Singh N, Tromer EC, Payan A, Duro E et al. 2019. The molecular basis of monopolin recruitment to the kinetochore. Chromosoma 128:3331–54
    [Google Scholar]
  198. 198.
    Pot I, Measday V, Snydsman B, Cagney G, Fields S et al. 2003. Chl4p and Iml3p are two new members of the budding yeast outer kinetochore. Mol. Biol. Cell 14:2460–76
    [Google Scholar]
  199. 199.
    Przewloka MR, Venkei Z, Bolanos-Garcia VM, Debski J, Dadlez M, Glover DM. 2011. CENP-C is a structural platform for kinetochore assembly. Curr. Biol. 21:5399–405
    [Google Scholar]
  200. 200.
    Raaijmakers JA, van Heesbeen RGHP, Blomen VA, Janssen LME, van Diemen F et al. 2018. BUB1 is essential for the viability of human cells in which the spindle assembly checkpoint is compromised. Cell Rep 22:61424–38
    [Google Scholar]
  201. 201.
    Rabitsch KP, Petronczki M, Javerzat J-P, Genier S, Chwalla B et al. 2003. Kinetochore recruitment of two nucleolar proteins is required for homolog segregation in meiosis I. Dev. Cell 4:4535–48
    [Google Scholar]
  202. 202.
    Rago F, Gascoigne KE, Cheeseman IM. 2015. Distinct organization and regulation of the outer kinetochore KMN network downstream of CENP-C and CENP-T. Curr. Biol. 25:5671–77
    [Google Scholar]
  203. 203.
    Raisch T, Ciossani G, d'Amico E, Cmentowski V, Carmignani S et al. 2022. Structure of the RZZ complex and molecular basis of Spindly-driven corona assembly at human kinetochores. EMBO J. 41:e110411
    [Google Scholar]
  204. 204.
    Ramey VH, Wang H-W, Nakajima Y, Wong A, Liu J et al. 2011. The Dam1 ring binds to the E-hook of tubulin and diffuses along the microtubule. Mol. Biol. Cell 22:4457–66
    [Google Scholar]
  205. 205.
    Renda F, Khodjakov A 2021. Role of spatial patterns and kinetochore architecture in spindle morphogenesis. Semin. Cell Dev. Biol. 117:75–85
    [Google Scholar]
  206. 206.
    Ribeiro SA, Gatlin JC, Dong Y, Joglekar A, Cameron L et al. 2009. Condensin regulates the stiffness of vertebrate centromeres. Mol. Biol. Cell 20:92371–80
    [Google Scholar]
  207. 207.
    Ribeiro SA, Vagnarelli P, Dong Y, Hori T, McEwen BF et al. 2010. A super-resolution map of the vertebrate kinetochore. PNAS 107:2310484–89
    [Google Scholar]
  208. 208.
    Rieder CL. 1982. The formation, structure, and composition of the mammalian kinetochore and kinetochore fiber. Int. Rev. Cytol. 79:1–58
    [Google Scholar]
  209. 209.
    Rodriguez-Rodriguez JA, Lewis C, McKinley KL, Sikirzhytski V, Corona J et al. 2018. Distinct roles of RZZ and Bub1-KNL1 in mitotic checkpoint signaling and kinetochore expansion. Curr. Biol. 28:213422–29.e5
    [Google Scholar]
  210. 210.
    Rosas-Salvans M, Sutanto R, Suresh P, Dumont S. 2022. The Astrin-SKAP complex reduces friction at the kinetochore-microtubule interface. Curr. Biol. 32:2621–31
    [Google Scholar]
  211. 211.
    Roscioli E, Germanova TE, Smith CA, Embacher PA, Erent M et al. 2020. Ensemble-level organization of human kinetochores and evidence for distinct tension and attachment sensors. Cell Rep 31:4107535
    [Google Scholar]
  212. 212.
    Sacristan C, Ahmad MUD, Keller J, Fermie J, Groenewold V et al. 2018. Dynamic kinetochore size regulation promotes microtubule capture and chromosome biorientation in mitosis. Nat. Cell Biol. 20:7800–10
    [Google Scholar]
  213. 212a.
    Sacristan C, Samejima K, Ruiz LA, Lambers MLA, Buckle Aet al 2022. Condensin reorganizes centromeric chromatin during mitotic entry into a bipartite structure stabilized by cohesin. bioRxiv 2022.08.01.502248. https://doi.org/10.1101/2022.08.01.502248
    [Crossref] [Google Scholar]
  214. 213.
    Sakuno T, Tada K, Watanabe Y. 2009. Kinetochore geometry defined by cohesion within the centromere. Nature 458:7240852–58
    [Google Scholar]
  215. 214.
    Sarangapani KK, Duro E, Deng Y, De Lima Alves F, Ye Q et al. 2014. Sister kinetochores are mechanically fused during meiosis I in yeast. Science 346:6206248–51
    [Google Scholar]
  216. 215.
    Sarangapani KK, Koch LB, Nelson CR, Asbury CL, Biggins S. 2021. Kinetochore-bound Mps1 regulates kinetochore–microtubule attachments via Ndc80 phosphorylation. J. Cell Biol. 220:12e202106130
    [Google Scholar]
  217. 216.
    Sarkar S, Shenoy RT, Dalgaard JZ, Newnham L, Hoffmann E et al. 2013. Monopolin subunit Csm1 associates with MIND complex to establish monopolar attachment of sister kinetochores at meiosis I. PLOS Genet 9:7e1003610
    [Google Scholar]
  218. 217.
    Saurin AT. 2018. Kinase and phosphatase cross-talk at the kinetochore. Front. . Cell Dev. Biol. 6:62
    [Google Scholar]
  219. 218.
    Scarborough EA, Davis TN, Asbury CL. 2019. Tight bending of the Ndc80 complex provides intrinsic regulation of its binding to microtubules. eLife 8:e44489
    [Google Scholar]
  220. 219.
    Schalbetter SA, Goloborodko A, Fudenberg G, Belton J-M, Miles C et al. 2017. SMC complexes differentially compact mitotic chromosomes according to genomic context. Nat. Cell Biol. 19:91071–80
    [Google Scholar]
  221. 220.
    Scherthan H. 2001. A bouquet makes ends meet. Nat. Rev. Mol. Cell Biol. 2:621–27
    [Google Scholar]
  222. 221.
    Schleiffer A, Maier M, Litos G, Lampert F, Hornung P et al. 2012. CENP-T proteins are conserved centromere receptors of the Ndc80 complex. Nat. Cell Biol. 14:6604–13
    [Google Scholar]
  223. 222.
    Schmidt JC, Arthanari H, Boeszoermenyi A, Dashkevich NM, Wilson-Kubalek EM et al. 2012. The kinetochore-bound Ska1 complex tracks depolymerizing microtubules and binds to curved protofilaments. Dev. Cell 23:5968–80
    [Google Scholar]
  224. 223.
    Schmidt JC, Kiyomitsu T, Hori T, Backer CB, Fukagawa T, Cheeseman IM. 2010. Aurora B kinase controls the targeting of the Astrin-SKAP complex to bioriented kinetochores. J. Cell Biol. 191:2269–80
    [Google Scholar]
  225. 224.
    Screpanti E, De Antoni A, Alushin GM, Petrovic A, Melis T et al. 2011. Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr. Biol. 21:5391–98
    [Google Scholar]
  226. 225.
    Silió V, McAinsh AD, Millar JB. 2015. KNL1-Bubs and RZZ provide two separable pathways for checkpoint activation at human kinetochores. Dev. Cell 35:5600–13
    [Google Scholar]
  227. 226.
    Singh P, Pesenti ME, Maffini S, Carmignani S, Hedtfeld M et al. 2021. BUB1 and CENP-U, primed by CDK1, are the main PLK1 kinetochore receptors in mitosis. Mol. Cell 81:167–87.e9
    [Google Scholar]
  228. 227.
    Smith CA, McAinsh AD, Burroughs NJ. 2016. Human kinetochores are swivel joints that mediate microtubule attachments. eLife 5:e16159
    [Google Scholar]
  229. 228.
    Stephens AD, Haase J, Vicci L, Taylor RM, Bloom K. 2011. Cohesin, condensin, and the intramolecular centromere loop together generate the mitotic chromatin spring. J. Cell Biol. 193:71167–80
    [Google Scholar]
  230. 229.
    Sullivan BA, Karpen GH. 2004. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat. Struct. Mol. Biol. 11:111076–83
    [Google Scholar]
  231. 230.
    Suresh P, Long AF, Dumont S. 2020. Microneedle manipulation of the mammalian spindle reveals specialized, short-lived reinforcement near chromosomes. eLife 9:e53807
    [Google Scholar]
  232. 231.
    Suzuki A, Badger BL, Salmon ED. 2015. A quantitative description of Ndc80 complex linkage to human kinetochores. Nat. Commun. 6:8161
    [Google Scholar]
  233. 232.
    Suzuki A, Badger BL, Wan X, DeLuca JG, Salmon ED. 2014. The architecture of CCAN proteins creates a structural integrity to resist spindle forces and achieve proper intrakinetochore stretch. Dev. Cell 30:6717–30
    [Google Scholar]
  234. 233.
    Tanaka K, Chang HL, Kagami A, Watanabe Y. 2009. CENP-C functions as a scaffold for effectors with essential kinetochore functions in mitosis and meiosis. Dev. Cell 17:3334–43
    [Google Scholar]
  235. 234.
    Tang NH, Toda T. 2013. Ndc80 Loop as a protein-protein interaction motif. Cell Div 8:12
    [Google Scholar]
  236. 235.
    Thakur J, Packiaraj J, Henikoff S. 2021. Sequence, chromatin and evolution of satellite DNA. Int. J. Mol. Sci. 22:94309
    [Google Scholar]
  237. 236.
    Tien JF, Umbreit NT, Gestaut DR, Franck AD, Cooper J et al. 2010. Cooperation of the Dam1 and Ndc80 kinetochore complexes enhances microtubule coupling and is regulated by aurora B. J. Cell Biol. 189:4713–23
    [Google Scholar]
  238. 237.
    Tóth A, Rabitsch KP, Gálová M, Schleiffer A, Buonomo SB, Nasmyth K. 2000. Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis I. Cell 103:71155–68
    [Google Scholar]
  239. 238.
    Tromer EC, van Hooff JJE, Kops GJPL, Snel B. 2019. Mosaic origin of the eukaryotic kinetochore. PNAS 116:2612873–82
    [Google Scholar]
  240. 239.
    Tromer EC, Wemyss TA, Ludzia P, Waller RF, Akiyoshi B. 2021. Repurposing of synaptonemal complex proteins for kinetochores in Kinetoplastida. Open Biol 11:5210049
    [Google Scholar]
  241. 240.
    Valverde R, Ingram J, Harrison SC. 2016. Conserved tetramer junction in the kinetochore Ndc80 complex. Cell Rep 17:81915–22
    [Google Scholar]
  242. 241.
    Vargiu G, Makarov AA, Allan J, Fukagawa T, Booth DG, Earnshaw WC. 2017. Stepwise unfolding supports a subunit model for vertebrate kinetochores. PNAS 114:123133–38
    [Google Scholar]
  243. 242.
    Varma D, Wan X, Cheerambathur D, Gassmann R, Suzuki A et al. 2013. Spindle assembly checkpoint proteins are positioned close to core microtubule attachment sites at kinetochores. J. Cell Biol. 202:5735–46
    [Google Scholar]
  244. 243.
    Verzijlbergen KF, Nerusheva OO, Kelly D, Kerr A, Clift D et al. 2014. Shugoshin biases chromosomes for biorientation through condensin recruitment to the pericentromere. eLife 3:e01374
    [Google Scholar]
  245. 244.
    Volkov VA, Grissom PM, Arzhanik VK, Zaytsev AV, Renganathan K et al. 2015. Centromere protein F includes two sites that couple efficiently to depolymerizing microtubules. J. Cell Biol. 209:6813–28
    [Google Scholar]
  246. 245.
    Volkov VA, Huis in ’t Veld PJ, Dogterom M, Musacchio A. 2018. Multivalency of NDC80 in the outer kinetochore is essential to track shortening microtubules and generate forces. eLife 7:e36764
    [Google Scholar]
  247. 246.
    Walstein K, Petrovic A, Pan D, Hagemeier B, Vogt D et al. 2021. Assembly principles and stoichiometry of a complete human kinetochore module. Sci. Adv. 7:27eabg1037
    [Google Scholar]
  248. 247.
    Wan X, O'Quinn RP, Pierce HL, Joglekar AP, Gall WE et al. 2009. Protein architecture of the human kinetochore microtubule attachment site. Cell 137:4672–84
    [Google Scholar]
  249. 248.
    Watanabe R, Hara M, Okumura EI, Hervé S, Fachinetti D et al. 2019. CDK1-mediated CENP-C phosphorylation modulates CENP-A binding and mitotic kinetochore localization. J. Cell Biol. 218:124042–62
    [Google Scholar]
  250. 249.
    Watanabe Y, Nurse P. 1999. Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:6743461–64
    [Google Scholar]
  251. 250.
    Weber SA, Gerton JL, Polancic JE, DeRisi JL, Koshland D et al. 2004. The kinetochore is an enhancer of pericentric cohesin binding. PLOS Biol 2:9e260
    [Google Scholar]
  252. 251.
    Wei RR, Al-Bassam J, Harrison SC. 2007. The Ndc80/HEC1 complex is a contact point for kinetochore-microtubule attachment. Nat. Struct. Mol. Biol. 14:154–59
    [Google Scholar]
  253. 252.
    Wei RR, Schnell JR, Larsen NA, Sorger PK, Chou JJ, Harrison SC. 2006. Structure of a central component of the yeast kinetochore: the Spc24p/Spc25p globular domain. Structure 14:61003–9
    [Google Scholar]
  254. 253.
    Wei RR, Sorger PK, Harrison SC. 2005. Molecular organization of the Ndc80 complex, an essential kinetochore component. PNAS 102:155363–67
    [Google Scholar]
  255. 254.
    Weir JR, Faesen AC, Klare K, Petrovic A, Basilico F et al. 2016. Insights from biochemical reconstitution into the architecture of human kinetochores. Nature 537:7619249–53
    [Google Scholar]
  256. 255.
    Westermann S, Avila-Sakar A, Wang HW, Niederstrasser H, Wong J et al. 2005. Formation of a dynamic kinetochore-microtubule interface through assembly of the Dam1 ring complex. Mol. Cell 17:2277–90
    [Google Scholar]
  257. 256.
    Westhorpe FG, Straight AF. 2014. The centromere: epigenetic control of chromosome segregation during mitosis. Cold Spring Harb. Perspect. Biol. 7:1a015818
    [Google Scholar]
  258. 257.
    Wimbish RT, DeLuca JG. 2020. Hec1/Ndc80 tail domain function at the kinetochore-microtubule interface. Front. Cell Dev. Biol. 8:43
    [Google Scholar]
  259. 258.
    Winey M, Mamay CL, O'Toole ET, Mastronarde DN, Giddings THJ et al. 1995. Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle. J. Cell Biol. 129:61601–15
    [Google Scholar]
  260. 259.
    Xiao H, Wang F, Wisniewski J, Shaytan AK, Ghirlando R et al. 2017. Molecular basis of CENP-C association with the CENP-A nucleosome at yeast centromeres. Genes Dev 31:191958–72
    [Google Scholar]
  261. 260.
    Yamagishi Y, Sakuno T, Shimura M, Watanabe Y. 2008. Heterochromatin links to centromeric protection by recruiting shugoshin. Nature 455:7210251–55
    [Google Scholar]
  262. 261.
    Yan K, Yang J, Zhang Z, McLaughlin SH, Chang L et al. 2019. Structure of the inner kinetochore CCAN complex assembled onto a centromeric nucleosome. Nature 574:278–82
    [Google Scholar]
  263. 262.
    Yan K, Zhang Z, Yang J, McLaughlin SH, Barford D. 2018. Architecture of the CBF3-centromere complex of the budding yeast kinetochore. Nat. Struct. Mol. Biol. 25:121103–10
    [Google Scholar]
  264. 263.
    Yatskevich S, Muir KW, Bellini D, Zhang Z, Yang J et al. 2022. Structure of the human inner kinetochore bound to a centromeric CENP-A nucleosome. Science 376:844–52
    [Google Scholar]
  265. 264.
    Ye AA, Cane S, Maresca TJ. 2016. Chromosome biorientation produces hundreds of piconewtons at a metazoan kinetochore. Nat. Commun. 7:13221
    [Google Scholar]
  266. 265.
    Ye Q, Ur SN, Su TY, Corbett KD. 2016. Structure of the Saccharomyces cerevisiae Hrr25:Mam1 monopolin subcomplex reveals a novel kinase regulator. EMBO J 35:192139–51
    [Google Scholar]
  267. 266.
    Yeh E, Haase J, Paliulis LV, Joglekar A, Bond L et al. 2008. Pericentric chromatin is organized into an intramolecular loop in mitosis. Curr. Biol. 18:281–90
    [Google Scholar]
  268. 267.
    Zaytsev AV, Mick JE, Maslennikov E, Nikashin B, De Luca JG, Grishchuk EL. 2015. Multisite phosphorylation of the NDC80 complex gradually tunes its microtubule-binding affinity. Mol. Biol. Cell 26:101829–44
    [Google Scholar]
  269. 268.
    Zhang Q, Sivakumar S, Chen Y, Gao H, Yang L et al. 2017. Ska3 phosphorylated by Cdk1 binds Ndc80 and recruits Ska to kinetochores to promote mitotic progression. Curr. Biol. 27:101477–84.e4
    [Google Scholar]
  270. 269.
    Zhang W, Lukoynova N, Miah S, Lucas J, Vaughan CK 2018. Insights into centromere DNA bending revealed by the cryo-EM structure of the core centromere binding factor 3 with Ndc10. Cell Rep 24:3744–54
    [Google Scholar]
  271. 270.
    Zhang Z, Bellini D, Barford D. 2020. Crystal structure of the Cenp-HIKHead-TW sub-module of the inner kinetochore CCAN complex. Nucleic Acids Res 48:1911172–84
    [Google Scholar]
  272. 271.
    Zhao W, Jensen GJ. 2022. In situ architecture of human kinetochore-microtubule interface visualized by cryo-electron tomography. bioRxiv 2022.02.17.480955. https://doi.org/10.1101/2022.02.17.480955
    [Crossref]
  273. 272.
    Zhou K, Gebala M, Woods D, Sundararajan K, Edwards G et al. 2022. CENP-N promotes the compaction of centromeric chromatin. Nat. Struct. Mol. Biol. 29:403–13
    [Google Scholar]
  274. 273.
    Zhou X, Zheng F, Wang C, Wu M, Zhang XX et al. 2017. Phosphorylation of CENP-C by Aurora B facilitates kinetochore attachment error correction in mitosis. PNAS 114:50E10667–76
    [Google Scholar]
  275. 274.
    Zhou Z, Feng H, Zhou BR, Ghirlando R, Hu K et al. 2011. Structural basis for recognition of centromere histone variant CenH3 by the chaperone Scm3. Nature 472:7342234–38
    [Google Scholar]
  276. 275.
    Zielinska AP, Bellou E, Sharma N, Frombach AS, Seres KB et al. 2019. Meiotic kinetochores fragment into multiple lobes upon cohesin loss in aging eggs. Curr. Biol. 29:223749–65.e7
    [Google Scholar]
  277. 276.
    Zielinska AP, Holubcová Z, Blayney M, Elder K, Schuh M. 2015. Sister kinetochore splitting and precocious disintegration of bivalents could explain the maternal age effect. eLife 4:e11389
    [Google Scholar]
  278. 277.
    Zinkowski RP, Meyne J, Brinkley BR. 1991. The centromere-kinetochore complex: a repeat subunit model. J. Cell Biol. 113:51091–110
    [Google Scholar]
/content/journals/10.1146/annurev-genet-072820-034559
Loading
/content/journals/10.1146/annurev-genet-072820-034559
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error