Skip to main content

Quantitative Microscopy Reveals Centromeric Chromatin Stability, Size, and Cell Cycle Mechanisms to Maintain Centromere Homeostasis

  • Chapter
  • First Online:
Centromeres and Kinetochores

Part of the book series: Progress in Molecular and Subcellular Biology ((PMSB,volume 56))

Abstract

Centromeres are chromatin domains specified by nucleosomes containing the histone H3 variant, CENP-A. This unique centromeric structure is at the heart of a strong self-templating epigenetic mechanism that renders centromeres heritable. We review how specific quantitative microscopy approaches have contributed to the determination of the copy number, architecture, size, and dynamics of centromeric chromatin and its associated centromere complex and kinetochore. These efforts revealed that the key to long-term centromere maintenance is the slow turnover of CENP-A nucleosomes, a critical size of the chromatin domain and its cell cycle-coupled replication. These features come together to maintain homeostasis of a chromatin locus that directs its own epigenetic inheritance and facilitates the assembly of the mitotic kinetochore.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akiyoshi B, Gull K (2013) Evolutionary cell biology of chromosome segregation: insights from trypanosomes. Open Biol 3:130023

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Amor DJ, Bentley K, Ryan J, Perry J, Wong L, Slater H, Choo KHA (2004) Human centromere repositioning “in progress”. Proc Natl Acad Sci U S A 101:6542–6547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aravamudhan P, Felzer-Kim I, Joglekar AP (2013) The budding yeast point centromere associates with two Cse4 molecules during mitosis. Curr Biol 23:770–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Athwal RK, Walkiewicz MP, Baek S, Fu S, Bui M, Camps J, Ried T, Sung M-H, Dalal Y (2015) CENP-A nucleosomes localize to transcription factor hotspots and subtelomeric sites in human cancer cells. Epigenetics Chromatin 8:2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnhart MC, Kuich PHJL, Stellfox ME, Ward JA, Bassett EA, Black BE, Foltz DR (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J Cell Biol 194:229–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassett EA, Wood S, Salimian KJ, Ajith S, Foltz DR, Black BE (2010) Epigenetic centromere specification directs aurora B accumulation but is insufficient to efficiently correct mitotic errors. J Cell Biol 190:177–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergmann JH, Rodríguez MG, Martins NMC, Kimura H, Kelly DA, Masumoto H, Larionov V, Jansen LET, Earnshaw WC (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 30:328–340

    Article  CAS  PubMed  Google Scholar 

  • Bernad R, Sánchez P, Rivera T, Rodríguez-Corsino M, Boyarchuk E, Vassias I, Ray-Gallet D, Arnaoutov A, Dasso M, Almouzni G et al (2011) Xenopus HJURP and condensin II are required for CENP-A assembly. J Cell Biol 192:569–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Black BE, Cleveland DW (2011) Epigenetic centromere propagation and the nature of CENP-A nucleosomes. Cell 144:471–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Black BE, Foltz DR, Chakravarthy S, Luger K, Woods VL, Cleveland DW (2004) Structural determinants for generating centromeric chromatin. Nature 430:578–582

    Article  CAS  PubMed  Google Scholar 

  • Black BE, Jansen LET, Maddox PS, Foltz DR, Desai AB, Shah JV, Cleveland DW (2007a) Centromere identity maintained by nucleosomes assembled with histone H3 containing the CENP-A targeting domain. Mol Cell 25:309–322

    Article  CAS  PubMed  Google Scholar 

  • Black BE, Brock MA, Bédard S, Woods VL, Cleveland DW (2007b) An epigenetic mark generated by the incorporation of CENP-A into centromeric nucleosomes. Proc Natl Acad Sci U S A 104:5008–5013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blower MD, Karpen GH (2001) The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat Cell Biol 3:730–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blower MD, Sullivan BA, Karpen GH (2002) Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2:319–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bodor DL, Rodríguez MG, Moreno N, Jansen LET (2012) Analysis of protein turnover by quantitative SNAP-based pulse-chase imaging. Curr Protoc Cell Biol 8 (Chapter 8, Unit 8.8)

    Google Scholar 

  • Bodor DL, Valente LP, Mata JF, Black BE, Jansen LET (2013) Assembly in G1 phase and long-term stability are unique intrinsic features of CENP-A nucleosomes. Mol Biol Cell 24:923–932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bodor DL, Mata JF, Sergeev M, David AF, Salimian KJ, Panchenko T, Cleveland DW, Black BE, Shah JV, Jansen LET (2014) The quantitative architecture of centromeric chromatin. Elife 3:1–26

    Article  CAS  Google Scholar 

  • Brown WRA, Xu Z (2009) The “kinetochore maintenance loop”—the mark of regulation? BioEssays 31:228–236

    Article  PubMed  Google Scholar 

  • Buchwitz BJ, Ahmad K, Moore LL, Roth MB, Henikoff S (1999) Cell division: a histone-H3-like protein in C. elegans. Nature 401:547–548

    Article  CAS  PubMed  Google Scholar 

  • Carroll CW, Silva MCCC, Godek KM, Jansen LETT, Straight AF (2009) Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat Cell Biol 11:896–902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll CW, Milks KJ, Straight AF (2010) Dual recognition of CENP-A nucleosomes is required for centromere assembly. J Cell Biol 189:1143–1155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9:33–46

    Article  CAS  PubMed  Google Scholar 

  • Cheeseman IM, Niessen S, Anderson S, Hyndman F, Yates JR, Oegema K, Desai A (2004) A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev 18:2255–2268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A (2006) The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127:983–997

    Article  CAS  PubMed  Google Scholar 

  • Chmátal L, Gabriel SIII, Mitsainas GP, Martínez-Vargas J, Ventura J, Searle JB, Schultz RM, Lampson MA (2014) Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Curr Biol 24:2295–2300

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Coffman VC, Wu P, Parthun MR, Wu J-Q (2011) CENP-A exceeds microtubule attachment sites in centromere clusters of both budding and fission yeast. J Cell Biol 195:563–572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins KA, Furuyama S, Biggins S (2004) Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A Histone H3 variant. Current Biology 14, no. 21 (2004): 1968–1972

    Google Scholar 

  • Csink AK, Henikoff S (1998) Something from nothing: the evolution and utility of satellite repeats. Trends Genet 14:200–204

    Article  CAS  PubMed  Google Scholar 

  • Dambacher S, Deng W, Hahn M, Sadic D, Fröhlich J, Nuber A, Hoischen C, Diekmann S, Leonhardt H, Schotta G (2012) CENP-C facilitates the recruitment of M18BP1 to centromeric chromatin. Nucleus 3:101–110

    Article  PubMed  PubMed Central  Google Scholar 

  • Deaton AM, Gómez-Rodríguez M, Mieczkowski J, Tolstorukov MY, Kundu S, Sadreyev RI, Jansen LE, Kingston RE (2016) Enhancer regions show high histone H3.3 turnover that changes during differentiation. Elife 5:e15316

    Google Scholar 

  • DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, Salmon ED (2006) Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127:969–982

    Article  CAS  PubMed  Google Scholar 

  • Dodd IB, Micheelsen MA, Sneppen K, Thon G (2007) Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 129:813–822

    Article  CAS  PubMed  Google Scholar 

  • Drinnenberg IA, DeYoung D, Henikoff S, Malik HS (2014) Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. Elife 3:e03676

    Article  PubMed Central  CAS  Google Scholar 

  • Dunleavy EM, Roche D, Tagami H, Lacoste N, Ray-Gallet D, Nakamura Y, Daigo Y, Nakatani Y, Almouzni-Pettinotti G (2009) HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137:485–497

    Article  CAS  PubMed  Google Scholar 

  • Dunleavy EM, Almouzni G, Karpen GH (2011) H3.3 is deposited at centromeres in S phase as a placeholder for newly assembled CENP-A in G(1) phase. Nucleus 2:146–157

    Article  PubMed  PubMed Central  Google Scholar 

  • Dunleavy EM, Beier NL, Gorgescu W, Tang J, Costes SV, Karpen GH (2012) The cell cycle timing of centromeric chromatin assembly in drosophila meiosis is distinct from mitosis yet requires CAL1 and CENP-C. PLoS Biol 10:e1001460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Earnshaw WC, Migeon BR (1985) Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma 92:290–296

    Article  CAS  PubMed  Google Scholar 

  • Earnshaw WC, Rothfield N (1985) Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91:313–321

    Article  CAS  PubMed  Google Scholar 

  • Fachinetti D, Diego Folco H, Nechemia-Arbely Y, Valente LP, Nguyen K, Wong AJ, Zhu Q, Holland AJ, Desai A, Jansen LET et al (2013) A two-step mechanism for epigenetic specification of centromere identity and function. Nat Cell Biol 15:1056–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falk SJ, Guo LY, Sekulic N, Smoak EM, Mani T, Logsdon GA, Gupta K, Jansen LET, Van Duyne GD, Vinogradov SA et al (2015) CENP-C reshapes and stabilizes CENP-A nucleosomes at the centromere. Science (80)348:699–703

    Google Scholar 

  • Falk SJ, Lee J, Sekulic N, Sennett MA, Lee T-H, Black BE (2016) CENP-C directs a structural transition of CENP-A nucleosomes mainly through sliding of DNA gyres. Nat Struct Mol Biol 23:204–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foltz DR, Jansen LET, Black BE, Bailey AO, Yates JR, Cleveland DW (2006) The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8:458–469

    Article  CAS  PubMed  Google Scholar 

  • Foltz DR, Jansen LET, Bailey AO, Yates JR, Bassett EA, Wood S, Cleveland DW (2009) Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137:472–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita Y, Hayashi T, Kiyomitsu T, Toyoda Y, Kokubu A, Obuse C, Yanagida M (2007) Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev Cell 12:17–30

    Article  CAS  PubMed  Google Scholar 

  • Furuyama S, Biggins S (2007) Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc Natl Acad Sci U S A 104:14706–14711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 145:410–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gassmann R, Rechtsteiner A, Yuen KW, Muroyama A, Egelhofer T, Gaydos L, Barron F, Maddox P, Essex A, Monen J et al (2012) An inverse relationship to germline transcription defines centromeric chromatin in C. elegans. Nature 484:534–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez-Rodríguez M, Jansen LET (2013) Basic properties of epigenetic systems: lessons from the centromere. Curr Opin Genet Dev 23:219–227

    Article  PubMed  CAS  Google Scholar 

  • Guse A, Carroll CW, Moree B, Fuller CJ, Straight AF (2011) In vitro centromere and kinetochore assembly on defined chromatin templates. Nature 477:354–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haase J, Mishra PK, Stephens A, Haggerty R, Quammen C, Taylor RM, Yeh E, Basrai MA, Bloom K (2013) A 3D map of the yeast kinetochore reveals the presence of core and accessory centromere-specific histone. Curr Biol 23:1939–1944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasson D, Panchenko T, Salimian KJ, Salman MU, Sekulic N, Alonso A, Warburton PE, Black BE (2013) The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat Struct Mol Biol 6:687–695

    Google Scholar 

  • Hemmerich P, Weidtkamp-Peters S, Hoischen C, Schmiedeberg L, Erliandri I, Diekmann S (2008) Dynamics of inner kinetochore assembly and maintenance in living cells. J Cell Biol 180:1101–1114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henikoff S, Ahmad K, Platero JS, van Steensel B (2000) Heterochromatic deposition of centromeric histone H3-like proteins. Proc Natl Acad Sci 97:716–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heun P, Erhardt S, Blower MD, Weiss S, Skora AD, Karpen GH (2006) Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell 10:303–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann S, Dumont M, Barra V, Ly P, Nechemia-Arbely Y, McMahon MA, Hervé S, Cleveland DW, Fachinetti D, Bade D et al (2016) CENP-A is dispensable for mitotic centromere function after initial centromere/kinetochore assembly. Cell Rep 17:2394–2404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hori T, Shang W-HH, Takeuchi K, Fukagawa T (2013) The CCAN recruits CENP-A to the centromere and forms the structural core for kinetochore assembly. J Cell Biol 200:45–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howman EV, Fowler KJ, Newson AJ, Redward S, MacDonald AC, Kalitsis P, Choo KHA (2000) Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc Natl Acad Sci 97:1148–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hudson DF, Fowler KJ, Earle E, Saffery R, Kalitsis P, Trowell H, Hill J, Wreford NG, de Kretser DM, Cancilla MR et al (1998) centromere protein B null mice are mitotically and meiotically normal but have lower body and testis weights. J Cell Biol 141:309–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Izuta H, Ikeno M, Suzuki N, Tomonaga T, Nozaki N, Obuse C, Kisu Y, Goshima N, Nomura F, Nomura N et al (2006) Comprehensive analysis of the ICEN (Interphase Centromere Complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 11:673–684

    Article  CAS  PubMed  Google Scholar 

  • Jansen LET, Black BE, Foltz DR, Cleveland DW (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176:795–805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joglekar AP, Bouck DC, Molk JN, Bloom KS, Salmon ED (2006) Molecular architecture of a kinetochore-microtubule attachment site. Nat Cell Biol 8:581–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joglekar AP, Bouck D, Finley K, Liu X, Wan Y, Berman J, He X, Salmon ED, Bloom KS (2008) Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J Cell Biol 181:587–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston K, Joglekar A, Hori T, Suzuki A, Fukagawa T, Salmon EDD (2010) Vertebrate kinetochore protein architecture: protein copy number. J Cell Biol 189:937–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanesaki Y, Imamura S, Matsuzaki M, Tanaka K (2015) Identification of centromere regions in chromosomes of a unicellular red alga, Cyanidioschyzon merolae. FEBS Lett 589:1219–1224

    Article  CAS  PubMed  Google Scholar 

  • Kato H, Jiang J, Zhou B-R, Rozendaal M, Feng H, Ghirlando R, Xiao TS, Straight AF, Bai Y (2013) A conserved mechanism for centromeric nucleosome recognition by centromere protein CENP-C. Science (80)340:1110–1113

    Google Scholar 

  • Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, Johnsson K (2003) A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat Biotechnol 21:86–89

    Article  CAS  PubMed  Google Scholar 

  • Lacoste N, Woolfe A, Tachiwana H, Garea AV, Barth T, Cantaloube S, Kurumizaka H, Imhof A, Almouzni G (2014) Mislocalization of the centromeric histone variant CenH3/CENP-A in human cells depends on the chaperone DAXX. Mol Cell 53:631–644

    Article  CAS  PubMed  Google Scholar 

  • Lagana AA, Dorn JF, De Rop VV, Ladouceur A-M, Maddox AS, Maddox PS (2010) A small GTPase molecular switch regulates epigenetic centromere maintenance by stabilizing newly incorporated CENP-A. Nat Cell Biol 12:1186–1193

    Article  CAS  PubMed  Google Scholar 

  • Lando D, Endesfelder U, Berger H, Subramanian L, Dunne PD, McColl J, Klenerman D, Carr AM, Sauer M, Allshire RC et al (2012) Quantitative single-molecule microscopy reveals that CENP-ACnp1 deposition occurs during G2 in fission yeast. Open Biol 2:120078

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lawrimore J, Bloom KS, Salmon ED (2011) Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. J Cell Biol 195:573–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leake MC, Chandler JH, Wadhams GH, Bai F, Berry RM, Armitage JP (2006) Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443:355–358

    Article  CAS  PubMed  Google Scholar 

  • Lermontova I, Schubert V, Fuchs J, Klatte S, Macas J, Schubert I (2006) Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18:2443–2451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lidsky PV, Sprenger F, Lehner CF (2013) Distinct modes of centromere protein dynamics during cell cycle progression in Drosophila S2R+ cells. J Cell Sci 126:4782–4793

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Mao Y (2016) Diaphanous formin mDia2 regulates CENP-A levels at centromeres. J Cell Biol 213:415–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S-T, Rattner JB, Jablonski SA, Yen TJ (2006) Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J Cell Biol 175:41–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Mol Biol 10:882–891

    Article  CAS  Google Scholar 

  • Maruyama S, Kuroiwa H, Miyagishima S, Tanaka K, Kuroiwa T (2007) Centromere dynamics in the primitive red alga Cyanidioschyzon merolae. Plant J 49:1122–1129

    Article  CAS  PubMed  Google Scholar 

  • McEwen BF, Chan GKT, Zubrowski B, Savoian MS, Sauer MT, Yen TJ (2001) CENP-E is essential for reliable bioriented spindle attachment, but chromosome alignment can be achieved via redundant mechanisms in mammalian cells. Mol Biol Cell 12:2776–2789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKinley KL, Cheeseman IM (2014) Polo-like Kinase 1 licenses CENP-A deposition at centromeres. Cell 158:397–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mellone BG, Grive KJ, Shteyn V, Bowers SR, Oderberg I, Karpen GH (2011) Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genet 7:e1002068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendiburo MJ, Padeken J, Fülöp S, Schepers A, Heun P (2011) Drosophila CENH3 is sufficient for centromere formation. Science (80)334:686–690

    Google Scholar 

  • Milks KJ, Moree B, Straight AF (2009) Dissection of CENP-C-directed centromere and kinetochore assembly. Mol Biol Cell 20:4246–4255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monen J, Maddox PS, Hyndman F, Oegema K, Desai A (2005) Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 7:1248–1255

    Article  PubMed  CAS  Google Scholar 

  • Moree B, Meyer CB, Fuller CJ, Straight AF (2011) CENP-C recruits M18BP1 to centromeres to promote CENP-A chromatin assembly. J Cell Biol 194:855–871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller S, Montes de Oca R, Lacoste N, Dingli F, Loew D, Almouzni G, Montes de Oca R, Lacoste N, Dingli F, Loew D et al (2014) Phosphorylation and DNA binding of HJURP determine its centromeric recruitment and function in CenH3(CENP-A) loading. Cell Report 8:190–203

    Article  CAS  Google Scholar 

  • Nardi IKK, Zasadzińska E, Stellfox MEE, Knippler CMM, Foltz DRR (2016) Licensing of centromeric chromatin assembly through the Mis18α-Mis18β heterotetramer. Mol Cell 61:774–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niikura Y, Kitagawa R, Kitagawa K (2016) CENP-A ubiquitylation is inherited through dimerization between cell divisions. Cell Report 15:61–76

    Article  CAS  Google Scholar 

  • Okada M, Cheeseman IM, Hori T, Okawa K, McLeod IX, Yates JR 3rd, Desai A, Fukagawa T (2006) The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat Cell Biol 8:446–457

    Article  CAS  PubMed  Google Scholar 

  • Olszak AM, van Essen D, Pereira AJ, Diehl S, Manke T, Maiato H, Saccani S, Heun P (2011) Heterochromatin boundaries are hotspots for de novo kinetochore formation. Nat Cell Biol 13:799–808

    Article  CAS  PubMed  Google Scholar 

  • Palmer DK, O’Day K, Wener MH, Andrews BS, Margolis RL (1987) A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J Cell Biol 104:805–815

    Article  CAS  PubMed  Google Scholar 

  • Palmer DK, O’Day K, Margolis RL (1990) The centromere specific histone CENP-A is selectively retained in discrete foci in mammalian sperm nuclei. Chromosoma 100:32–36

    Article  CAS  PubMed  Google Scholar 

  • Pearson CG, Maddox PS, Salmon ED, Bloom K (2001) Budding yeast chromosome structure and dynamics during mitosis. J Cell Biol 152:1255–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearson CG, Yeh E, Gardner M, Odde D, Salmon ED, Bloom K (2004) Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase. Curr Biol 14:1962–1967

    Article  CAS  PubMed  Google Scholar 

  • Perpelescu M, Nozaki N, Obuse C, Yang H, Yoda K (2009) Active establishment of centromeric CENP-A chromatin by RSF complex. J Cell Biol 185:397–407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pluta AF, Saitoh N, Goldberg I, Earnshaw WC (1992) Identification of a subdomain of CENP-B that is necessary and sufficient for localization to the human centromere. J Cell Biol 116:1081–1093

    Article  CAS  PubMed  Google Scholar 

  • Prendergast L, van Vuuren C, Kaczmarczyk A, Doering V, Hellwig D, Quinn N, Hoischen C, Diekmann S, Sullivan KF (2011) Premitotic assembly of human CENPs-T and -W switches centromeric chromatin to a mitotic state. PLoS Biol 9:e1001082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raychaudhuri N, Dubruille R, Orsi GA, Bagheri HC, Loppin B, Lehner CF (2012) Transgenerational propagation and quantitative maintenance of paternal centromeres depends on Cid/Cenp-A presence in drosophila sperm. PLoS Biol 10:e1001434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ray-Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N, Puri A, Schultz DC, Pchelintsev NA, Adams PD, Jansen LE et al (2011) Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol Cell 44:928–941

    Article  CAS  PubMed  Google Scholar 

  • Régnier V, Vagnarelli P, Fukagawa T, Zerjal T, Burns E, Trouche D, Earnshaw W, Brown W (2005) CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol Cell Biol 25:3967–3981

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ribeiro SA, Vagnarelli P, Dong Y, Hori T, McEwen BF, Fukagawa T, Flors C, Earnshaw WC (2010) A super-resolution map of the vertebrate kinetochore. J Cell Sci USA 107:10484–10489

    Article  CAS  Google Scholar 

  • Ross JE, Woodlief KS, Sullivan BA (2016) Inheritance of the CENP-A chromatin domain is spatially and temporally constrained at human centromeres. Epigenetics Chromatin 9:20

    Article  PubMed  PubMed Central  Google Scholar 

  • Sagolla MJ, Uzawa S, Cande WZ (2003) Individual microtubule dynamics contribute to the function of mitotic and cytoplasmic arrays in fission yeast. J Cell Sci 116

    Google Scholar 

  • Schittenhelm RB, Althoff F, Heidmann S, Lehner CF (2010) Detrimental incorporation of excess Cenp-A/Cid and Cenp-C into Drosophila centromeres is prevented by limiting amounts of the bridging factor Cal1. J Cell Sci 123:3768–3779

    Article  CAS  PubMed  Google Scholar 

  • Schuh M, Lehner CF, Heidmann S (2007) Incorporation of drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17:237–243

    Article  CAS  PubMed  Google Scholar 

  • Shelby RD, Vafa O, Sullivan KF (1997) Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites. J Cell Biol 136:501–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shelby RD, Monier K, Sullivan KF (2000) Chromatin assembly at kinetochores is uncoupled from dna replication. J Cell Biol 151:1113–1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shivaraju M, Unruh JRR, Slaughter BDD, Mattingly M, Berman J, Gerton JL, Alber F, Dokudovskaya S, Veenhoff LM, Zhang W et al (2012) Cell-cycle-coupled structural oscillation of centromeric nucleosomes in yeast. Cell 150:304–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shono N, Ohzeki J-I, Otake K, Martins NMC, Nagase T, Kimura H, Larionov V, Earnshaw WC, Masumoto H (2015) CENP-C and CENP-I are key connecting factors for kinetochore and CENP-A assembly. J Cell Sci jcs-180786

    Google Scholar 

  • Silva MCC, Bodor DL, Stellfox ME, Martins NMC, Hochegger H, Foltz DR, Jansen LET (2012) Cdk activity couples epigenetic centromere inheritance to cell cycle progression. Dev Cell 22:52–63

    Article  CAS  PubMed  Google Scholar 

  • Smoak EM, Stein P, Schultz RM, Lampson MA, Black BE (2016) Long-term retention of Cenp-A nucleosomes in mammalian oocytes underpins transgenerational inheritance of centromere identity. Curr Biol 26:1110–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stankovic A, Guo LY, Mata JF, Bodor DL, Cao X-Y, Bailey AO, Shabanowitz Jeffrey, Hunt DF, Garcia BA, Black BE, Jansen LET (2017) A dual inhibitory mechanism sufficient to maintain cell cycle restricted CENP-A assembly. Mol Cell 65:231–246

    Article  CAS  PubMed  Google Scholar 

  • Steiner FA, Henikoff S (2014) Holocentromeres are dispersed point centromeres localized at transcription factor hotspots. Elife 3:e02025

    Article  PubMed  PubMed Central  Google Scholar 

  • Stellfox ME, Nardi IK, Knippler CM, Foltz DR (2016) Differential binding partners of the Mis18α/β YIPPEE domains regulate Mis18 complex recruitment to centromeres. Cell Rep 1–9

    Google Scholar 

  • Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M (1995) A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev 9:573–586

    Article  CAS  PubMed  Google Scholar 

  • Sullivan KF, Hechenberger M, Masri K (1994) Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol 127:581–592

    Article  CAS  PubMed  Google Scholar 

  • Talbert PB, Henikoff S (2013) Phylogeny as the basis for naming histones. Trends Genet 29:499–500

    Article  CAS  PubMed  Google Scholar 

  • Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S (2002) Centromeric localization and adaptive evolution of an arabidopsis histone H3 variant. Plant Cell Online 14:1053–1066

    Article  CAS  Google Scholar 

  • Talbert PB, Ahmad K, Almouzni G, Ausió J, Berger F, Bhalla PL, Bonner WM, Cande WZ, Chadwick BP, Chan SWL et al (2012) A unified phylogeny-based nomenclature for histone variants. Epigenetics Chromatin 5:7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyler-Smith C, Gimelli G, Giglio S, Floridia G, Pandya A, Terzoli G, Warburton PE, Earnshaw WC, Zuffardi O (1999) Transmission of a fully functional human neocentromere through three generations. Am J Hum Genet 64:1440–1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voullaire LE, Slater HR, Petrovic V, Choo KH (1993) A functional marker centromere with no detectable alpha-satellite, satellite III, or CENP-B protein: activation of a latent centromere? Am J Hum Genet 52:1153–1163

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Liu X, Dou Z, Chen L, Jiang H, Fu C, Fu G, Liu D, Zhang J, Zhu T (2014) Mitotic regulator mis18 interacts with and specifies the centromeric assembly of molecular chaperone holliday junction recognition protein (HJURP). J Biol Chem 289:8326–8336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westhorpe FG, Fuller CJ, Straight AF (2015) A cell-free CENP-A assembly system defines the chromatin requirements for centromere maintenance. J Cell Biol jcb-201503132

    Google Scholar 

  • Wisniewski J, Hajj B, Chen J, Mizuguchi G, Xiao H, Wei D, Dahan M, Wu C (2014) Imaging the fate of histone Cse4 reveals de novo replacement in S phase and subsequent stable residence at centromeres. Elife 3:e02203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zinkowski RP, Meyne J, Brinkley BR (1991) The centromere-kinetochore complex: a repeat subunit model. J Cell Biol 113:1091–1110

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lars E. T. Jansen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Stankovic, A., Jansen, L.E.T. (2017). Quantitative Microscopy Reveals Centromeric Chromatin Stability, Size, and Cell Cycle Mechanisms to Maintain Centromere Homeostasis. In: Black, B. (eds) Centromeres and Kinetochores. Progress in Molecular and Subcellular Biology, vol 56. Springer, Cham. https://doi.org/10.1007/978-3-319-58592-5_6

Download citation

Publish with us

Policies and ethics