The CENP-L-N Complex Forms a Critical Node in an Integrated Meshwork of Interactions at the Centromere-Kinetochore Interface

Molecular Cell

Volumn 60, Issue 6, 2015, Pages 886-898

  McKinley, Kara L ^a,b   Sekulic, Nikolina ^c   Guo, Lucie Y ^c   Tsinman, Tonia ^a   Black, Ben E ^c   Cheeseman, Iain M ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CenH3; CENP A; Centromere; Kinetochore; Mitosis

Indexed keywords

CENTROMERE PROTEIN A; CENTROMERE PROTEIN C; CENTROMERE PROTEIN H; CENTROMERE PROTEIN I; CENTROMERE PROTEIN K; CENTROMERE PROTEIN L; CENTROMERE PROTEIN M; CENTROMERE PROTEIN N; CENTROMERE PROTEIN O; CENTROMERE PROTEIN P; CENTROMERE PROTEIN Q; CENTROMERE PROTEIN R; CENTROMERE PROTEIN S; CENTROMERE PROTEIN T; CENTROMERE PROTEIN U; CENTROMERE PROTEIN W; CENTROMERE PROTEIN X; CONSTITUTIVE CENTROMERE ASSOCIATED NETWORK PROTEIN; PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CENPL PROTEIN, HUMAN; CENPN PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN;

ARTICLE; CELL CYCLE; CENTROMERE; CHROMATIN; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CRISPR CAS SYSTEM; HUMAN; HUMAN CELL; INTERPHASE; NUCLEOSOME; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; CHEMISTRY; GENETICS; HELA CELL LINE; METABOLISM; MOLECULAR MODEL;

CELL CYCLE; CELL CYCLE PROTEINS; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; CRISPR-CAS SYSTEMS; HELA CELLS; HUMANS; KINETOCHORES; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES;

EID: 84953638894     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.10.027     Document Type: Article

References (62)

1. Amano M., Suzuki A., Hori T., Backer C., Okawa K., Cheeseman I.M., Fukagawa T. The CENP-S complex is essential for the stable assembly of outer kinetochore structure. J. Cell Biol. 2009, 186:173-182.
2. Athwal R.K., Walkiewicz M.P., Baek S., Fu S., Bui M., Camps J., Ried T., Sung M.H., Dalal Y. CENP-A nucleosomes localize to transcription factor hotspots and subtelomeric sites in human cancer cells. Epigenetics Chromatin 2015, 8:2.
3. Barnhart M.C., Kuich P.H., Stellfox M.E., Ward J.A., Bassett E.A., Black B.E., Foltz D.R. HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J. Cell Biol. 2011, 194:229-243.
4. Basilico F., Maffini S., Weir J.R., Prumbaum D., Rojas A.M., Zimniak T., De Antoni A., Jeganathan S., Voss B., van Gerwen S., et al. The pseudo GTPase CENP-M drives human kinetochore assembly. eLife 2014, 3:e02978.
5. Black B.E., Cleveland D.W. Epigenetic centromere propagation and the nature of CENP-a nucleosomes. Cell 2011, 144:471-479.
6. Blower M.D., Sullivan B.A., Karpen G.H. Conserved organization of centromeric chromatin in flies and humans. Dev. Cell 2002, 2:319-330.
7. Bodor D.L., Mata J.F., Sergeev M., David A.F., Salimian K.J., Panchenko T., Cleveland D.W., Black B.E., Shah J.V., Jansen L.E. The quantitative architecture of centromeric chromatin. eLife 2014, 3:e02137.
8. Carroll C.W., Silva M.C., Godek K.M., Jansen L.E., Straight A.F. Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat. Cell Biol. 2009, 11:896-902.
9. Carroll C.W., Milks K.J., Straight A.F. Dual recognition of CENP-A nucleosomes is required for centromere assembly. J. Cell Biol. 2010, 189:1143-1155.
10. Cheeseman I.M., Desai A. A combined approach for the localization and tandem affinity purification of protein complexes from metazoans. Sci. STKE 2005, 2005:pl1.
11. Cheeseman I.M., Desai A. Molecular architecture of the kinetochore-microtubule interface. Nat. Rev. Mol. Cell Biol. 2008, 9:33-46.
12. Cheeseman I.M., Chappie J.S., Wilson-Kubalek E.M., Desai A. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 2006, 127:983-997.
13. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A., Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
14. Dambacher S., Deng W., Hahn M., Sadic D., Fröhlich J., Nuber A., Hoischen C., Diekmann S., Leonhardt H., Schotta G. CENP-C facilitates the recruitment of M18BP1 to centromeric chromatin. Nucleus 2012, 3:101-110.
15. Earnshaw W.C., Rothfield N. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 1985, 91:313-321.
16. Eskat A., Deng W., Hofmeister A., Rudolphi S., Emmerth S., Hellwig D., Ulbricht T., Döring V., Bancroft J.M., McAinsh A.D., et al. Step-wise assembly, maturation and dynamic behavior of the human CENP-P/O/R/Q/U kinetochore sub-complex. PLoS ONE 2012, 7:e44717.
17. Fachinetti D., Folco H.D., Nechemia-Arbely Y., Valente L.P., Nguyen K., Wong A.J., Zhu Q., Holland A.J., Desai A., Jansen L.E., Cleveland D.W. A two-step mechanism for epigenetic specification of centromere identity and function. Nat. Cell Biol. 2013, 15:1056-1066.
18. Falk S.J., Guo L.Y., Sekulic N., Smoak E.M., Mani T., Logsdon G.A., Gupta K., Jansen L.E., Van Duyne G.D., Vinogradov S.A., et al. Chromosomes. CENP-C reshapes and stabilizes CENP-A nucleosomes at the centromere. Science 2015, 348:699-703.
19. Fang J., Liu Y., Wei Y., Deng W., Yu Z., Huang L., Teng Y., Yao T., You Q., Ruan H., et al. Structural transitions of centromeric chromatin regulate the cell cycle-dependent recruitment of CENP-N. Genes Dev. 2015, 29:1058-1073.
20. Fitzgerald D.J., Berger P., Schaffitzel C., Yamada K., Richmond T.J., Berger I. Protein complex expression by using multigene baculoviral vectors. Nat. Methods 2006, 3:1021-1032.
21. Folco H.D., Campbell C.S., May K.M., Espinoza C.A., Oegema K., Hardwick K.G., Grewal S.I., Desai A. The CENP-A N-tail confers epigenetic stability to centromeres via the CENP-T branch of the CCAN in fission yeast. Curr. Biol. 2015, 25:348-356.
22. Foltz D.R., Jansen L.E., Black B.E., Bailey A.O., Yates J.R., Cleveland D.W. The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 2006, 8:458-469.
23. Fukagawa T., Earnshaw W.C. The centromere: chromatin foundation for the kinetochore machinery. Dev. Cell 2014, 30:496-508.
24. Gascoigne K.E., Takeuchi K., Suzuki A., Hori T., Fukagawa T., Cheeseman I.M. Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 2011, 145:410-422.
25. Guse A., Carroll C.W., Moree B., Fuller C.J., Straight A.F. In vitro centromere and kinetochore assembly on defined chromatin templates. Nature 2011, 477:354-358.
26. Heun P., Erhardt S., Blower M.D., Weiss S., Skora A.D., Karpen G.H. Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev. Cell 2006, 10:303-315.
27. Hinshaw S.M., Harrison S.C. An Iml3-Chl4 heterodimer links the core centromere to factors required for accurate chromosome segregation. Cell Rep. 2013, 5:29-36.
28. Holland A.J., Fachinetti D., Han J.S., Cleveland D.W. Inducible, reversible system for the rapid and complete degradation of proteins in mammalian cells. Proc. Natl. Acad. Sci. USA 2012, 109:E3350-E3357.
29. Hori T., Amano M., Suzuki A., Backer C.B., Welburn J.P., Dong Y., McEwen B.F., Shang W.H., Suzuki E., Okawa K., et al. CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 2008, 135:1039-1052.
30. Hori T., Okada M., Maenaka K., Fukagawa T. CENP-O class proteins form a stable complex and are required for proper kinetochore function. Mol. Biol. Cell 2008, 19:843-854.
31. Hori T., Shang W.H., Takeuchi K., Fukagawa T. The CCAN recruits CENP-A to the centromere and forms the structural core for kinetochore assembly. J. Cell Biol. 2013, 200:45-60.
32. Izuta H., Ikeno M., Suzuki N., Tomonaga T., Nozaki N., Obuse C., Kisu Y., Goshima N., Nomura F., Nomura N., Yoda K. Comprehensive analysis of the ICEN (Interphase Centromere Complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 2006, 11:673-684.
33. Kato H., Jiang J., Zhou B.R., Rozendaal M., Feng H., Ghirlando R., Xiao T.S., Straight A.F., Bai Y. A conserved mechanism for centromeric nucleosome recognition by centromere protein CENP-C. Science 2013, 340:1110-1113.
34. Klare K., Weir J.R., Basilico F., Zimniak T., Massimiliano L., Ludwigs N., Herzog F., Musacchio A. CENP-C is a blueprint for constitutive centromere-associated network assembly within human kinetochores. J. Cell Biol. 2015, 210:11-22.
35. Kwon M.S., Hori T., Okada M., Fukagawa T. CENP-C is involved in chromosome segregation, mitotic checkpoint function, and kinetochore assembly. Mol. Biol. Cell 2007, 18:2155-2168.
36. Liu S.T., Rattner J.B., Jablonski S.A., Yen T.J. Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J. Cell Biol. 2006, 175:41-53.
37. Logsdon G.A., Barrey E.J., Bassett E.A., DeNizio J.E., Guo L.Y., Panchenko T., Dawicki-McKenna J.M., Heun P., Black B.E. Both tails and the centromere targeting domain of CENP-A are required for centromere establishment. J. Cell Biol. 2015, 208:521-531.
38. McClelland S.E., Borusu S., Amaro A.C., Winter J.R., Belwal M., McAinsh A.D., Meraldi P. The CENP-A NAC/CAD kinetochore complex controls chromosome congression and spindle bipolarity. EMBO J. 2007, 26:5033-5047.
39. McKinley K.L., Cheeseman I.M. Polo-like kinase 1 licenses CENP-A deposition at centromeres. Cell 2014, 158:397-411.
40. McKinley K.L., Cheeseman I.M. The molecular basis for centromere identity and function. Nat. Rev. Mol. Cell Biol. 2016, Published online November 25, 2015. 10.1038/nrm.2015.5.
41. Moree B., Meyer C.B., Fuller C.J., Straight A.F. CENP-C recruits M18BP1 to centromeres to promote CENP-A chromatin assembly. J. Cell Biol. 2011, 194:855-871.
42. Nagpal H., Hori T., Furukawa A., Sugase K., Osakabe A., Kurumizaka H., Fukagawa T. Dynamic changes in CCAN organization through CENP-C during cell-cycle progression. Mol. Biol. Cell 2015, 26:3768-3776.
43. Nishimura K., Fukagawa T., Takisawa H., Kakimoto T., Kanemaki M. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods 2009, 6:917-922.
44. Nishino T., Takeuchi K., Gascoigne K.E., Suzuki A., Hori T., Oyama T., Morikawa K., Cheeseman I.M., Fukagawa T. CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell 2012, 148:487-501.
45. Nishino T., Rago F., Hori T., Tomii K., Cheeseman I.M., Fukagawa T. CENP-T provides a structural platform for outer kinetochore assembly. EMBO J. 2013, 32:424-436.
46. Okada M., Cheeseman I.M., Hori T., Okawa K., McLeod I.X., Yates J.R., Desai A., Fukagawa T. The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat. Cell Biol. 2006, 8:446-457.
47. Przewloka M.R., Venkei Z., Bolanos-Garcia V.M., Debski J., Dadlez M., Glover D.M. CENP-C is a structural platform for kinetochore assembly. Curr. Biol. 2011, 21:399-405.
48. Ribeiro S.A., Vagnarelli P., Dong Y., Hori T., McEwen B.F., Fukagawa T., Flors C., Earnshaw W.C. A super-resolution map of the vertebrate kinetochore. Proc. Natl. Acad. Sci. USA 2010, 107:10484-10489.
49. Saitoh H., Tomkiel J., Cooke C.A., Ratrie H., Maurer M., Rothfield N.F., Earnshaw W.C. CENP-C, an autoantigen in scleroderma, is a component of the human inner kinetochore plate. Cell 1992, 70:115-125.
50. Screpanti E., De Antoni A., Alushin G.M., Petrovic A., Melis T., Nogales E., Musacchio A. Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr. Biol. 2011, 21:391-398.
51. Shalem O., Sanjana N.E., Hartenian E., Shi X., Scott D.A., Mikkelsen T.S., Heckl D., Ebert B.L., Root D.E., Doench J.G., Zhang F. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 2014, 343:84-87.
52. Shang W.H., Hori T., Martins N.M., Toyoda A., Misu S., Monma N., Hiratani I., Maeshima K., Ikeo K., Fujiyama A., et al. Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev. Cell 2013, 24:635-648.
53. Sullivan B.A., Karpen G.H. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat. Struct. Mol. Biol. 2004, 11:1076-1083.
54. Sullivan K.F., Hechenberger M., Masri K. Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J. Cell Biol. 1994, 127:581-592.
55. Suzuki A., Badger B.L., Wan X., DeLuca J.G., Salmon E.D. The architecture of CCAN proteins creates a structural integrity to resist spindle forces and achieve proper Intrakinetochore stretch. Dev. Cell 2014, 30:717-730.
56. Tachiwana H., Müller S., Blümer J., Klare K., Musacchio A., Almouzni G. HJURP involvement in de novo CenH3(CENP-A) and CENP-C recruitment. Cell Rep. 2015, 11:22-32.
57. Tanaka K., Chang H.L., Kagami A., Watanabe Y. CENP-C functions as a scaffold for effectors with essential kinetochore functions in mitosis and meiosis. Dev. Cell 2009, 17:334-343.
58. Van Hooser A.A., Ouspenski I.I., Gregson H.C., Starr D.A., Yen T.J., Goldberg M.L., Yokomori K., Earnshaw W.C., Sullivan K.F., Brinkley B.R. Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J. Cell Sci. 2001, 114:3529-3542.
59. Wang G., McCain M.L., Yang L., He A., Pasqualini F.S., Agarwal A., Yuan H., Jiang D., Zhang D., Zangi L., et al. Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat. Med. 2014, 20:616-623.
60. Wang T., Wei J.J., Sabatini D.M., Lander E.S. Genetic screens in human cells using the CRISPR-Cas9 system. Science 2014, 343:80-84.
61. Wang T., Birsoy K., Hughes N.W., Krupczak K.M., Post Y., Wei J.J., Lander E.S., Sabatini D.M. Identification and characterization of essential genes in the human genome. Science 2015, Published online October 15, 2015. 10.1126/science.aac7041.
62. Westhorpe F.G., Fuller C.J., Straight A.F. A cell-free CENP-A assembly system defines the chromatin requirements for centromere maintenance. J. Cell Biol. 2015, 209:789-801.