Advertisement

Chromosoma

pp 1–24 | Cite as

Genetic and epigenetic effects on centromere establishment

  • Yick Hin Ling
  • Zhongyang Lin
  • Karen Wing Yee YuenEmail author
Review

Abstract

Endogenous chromosomes contain centromeres to direct equal chromosomal segregation in mitosis and meiosis. The location and function of existing centromeres is usually maintained through cell cycles and generations. Recent studies have investigated how the centromere-specific histone H3 variant CENP-A is assembled and replenished after DNA replication to epigenetically propagate the centromere identity. However, existing centromeres occasionally become inactivated, with or without change in underlying DNA sequences, or lost after chromosomal rearrangements, resulting in acentric chromosomes. New centromeres, known as neocentromeres, may form on ectopic, non-centromeric chromosomal regions to rescue acentric chromosomes from being lost, or form dicentric chromosomes if the original centromere is still active. In addition, de novo centromeres can form after chromatinization of purified DNA that is exogenously introduced into cells. Here, we review the phenomena of naturally occurring and experimentally induced new centromeres and summarize the genetic (DNA sequence) and epigenetic features of these new centromeres. We compare the characteristics of new and native centromeres to understand whether there are different requirements for centromere establishment and propagation. Based on our understanding of the mechanisms of new centromere formation, we discuss the perspectives of developing more stably segregating human artificial chromosomes to facilitate gene delivery in therapeutics and research.

Keywords

Centromeres Neocentromeres Epigenetics Acentric chromosomes Dicentric chromosomes Artificial chromosomes 

Notes

References

  1. Aldrup-MacDonald ME, Kuo ME, Sullivan LL, Chew K, Sullivan BA (2016) Genomic variation within alpha satellite DNA influences centromere location on human chromosomes with metastable epialleles. Genome Research 26:1301–1311PubMedPubMedCentralCrossRefGoogle Scholar
  2. Allshire RC, Ekwall K (2015a) Epigenetic regulation of chromatin states in Schizosaccharomyces pombe. Cold Spring Harb Perspect Biol 7:a018770PubMedPubMedCentralCrossRefGoogle Scholar
  3. Alonso A, Fritz B, Hasson D, Abrusan G, Cheung F, Yoda K, Radlwimmer B, Ladurner AG, Warburton PE (2007) Co-localization of CENP-C and CENP-H to discontinuous domains of CENP-A chromatin at human neocentromeres. Genome Biol 8:R148PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alonso A, Hasson D, Cheung F, Warburton PE (2010) A paucity of heterochromatin at functional human neocentromeres. Epigenetics Chromatin 3:6PubMedPubMedCentralCrossRefGoogle Scholar
  5. Alonso A, Mahmood R, Li S, Cheung F, Yoda K, Warburton PE (2003) Genomic microarray analysis reveals distinct locations for the CENP-A binding domains in three human chromosome 13q32 neocentromeres. Human Mol Genet 12:2711–2721CrossRefGoogle Scholar
  6. Ambartsumyan G, Gill RK, Perez SD, Conway D, Vincent J, Dalal Y, Clark AT (2010) Centromere protein A dynamics in human pluripotent stem cell self-renewal, differentiation and DNA damage. Hum Mol Genet 19:3970–3982PubMedPubMedCentralCrossRefGoogle Scholar
  7. Amor DJ, Bentley K, Ryan J, Perry J, Wong L, Slater H, Choo KH (2004) Human centromere repositioning “in progress”. Proc Natl Acad Sci U S A 101:6542–6547PubMedPubMedCentralCrossRefGoogle Scholar
  8. Amor DJ, Choo KH (2002) Neocentromeres: role in human disease, evolution, and centromere study. Am J Hum Genet 71:695–714PubMedPubMedCentralCrossRefGoogle Scholar
  9. Athwal RK, Walkiewicz MP, Baek S, Fu S, Bui M, Camps J, Ried T, Sung MH, Dalal Y (2015) CENP-A nucleosomes localize to transcription factor hotspots and subtelomeric sites in human cancer cells. Epigenetics Chromatin 8:2PubMedPubMedCentralCrossRefGoogle Scholar
  10. Baker RE, Rogers K (2005) Genetic and genomic analysis of the AT-rich centromere DNA element II of Saccharomyces cerevisiae. Genetics 171:1463–1475PubMedPubMedCentralCrossRefGoogle Scholar
  11. Baldini A, Ried T, Shridhar V, Ogura K, D’Aiuto L, Rocchi M, Ward DC (1993) An alphoid DNA sequence conserved in all human and great ape chromosomes: evidence for ancient centromeric sequences at human chromosomal regions 2q21 and 9q13. Hum Genet 90:577–583PubMedCrossRefGoogle Scholar
  12. Barrey EJ, Heun P (2017) Artificial chromosomes and strategies to initiate epigenetic centromere establishment. Prog Mol Subcell Biol 56:193–212PubMedCrossRefGoogle Scholar
  13. Basu J, Compitello G, Stromberg G, Willard HF, Van Bokkelen G (2005) Efficient assembly of de novo human artificial chromosomes from large genomic loci. BMC Biotechnol 5:21PubMedPubMedCentralCrossRefGoogle Scholar
  14. Basu J, Stromberg G, Compitello G, Willard HF, Van Bokkelen G (2005) Rapid creation of BAC-based human artificial chromosome vectors by transposition with synthetic alpha-satellite arrays. Nucleic Acids Res 33:587–596PubMedPubMedCentralCrossRefGoogle Scholar
  15. Beh TT, MacKinnon RN, Kalitsis P (2016) Active centromere and chromosome identification in fixed cell lines. Mol Cytogenet 9:28PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bergmann JH, Jakubsche JN, Martins NM, Kagansky A, Nakano M, Kimura H, Kelly DA, Turner BM, Masumoto H, Larionov V, Earnshaw WC (2012) Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function. J Cell Sci 125:411–421PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bergmann JH, Rodriguez MG, Martins NM, Kimura H, Kelly DA, Masumoto H, Larionov V, Jansen LE, Earnshaw WC (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 30:328–340PubMedCrossRefGoogle Scholar
  18. Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294:2539–2542PubMedCrossRefGoogle Scholar
  19. Birchler JA, Presting GG (2012) Retrotransposon insertion targeting: a mechanism for homogenization of centromere sequences on nonhomologous chromosomes. Genes Dev 26:638–640CrossRefGoogle Scholar
  20. Birchler JA (2015) Engineered minichromosomes in plants. Chromosome Res 23:77–85PubMedCrossRefGoogle Scholar
  21. Black BE, Cleveland DW (2011) Epigenetic centromere propagation and the nature of CENP-a nucleosomes. Cell 144:471–479PubMedPubMedCentralCrossRefGoogle Scholar
  22. Black BE, Jansen LE, Foltz DR, Cleveland DW (2010) Centromere identity, function, and epigenetic propagation across cell divisions. Cold Spring Harb Symp Quant Biol 75:403–418PubMedCrossRefGoogle Scholar
  23. Blom E, Heyning FH, Kroes WG (2010) A case of angioimmunoblastic T-cell non-Hodgkin lymphoma with a neocentric inv dup(1). Cancer Genet Cytogenet 202:38–42PubMedCrossRefGoogle Scholar
  24. Blower MD (2016) Centromeric transcription regulates Aurora-B localization and activation. Cell Rep 15:1624–1633PubMedPubMedCentralCrossRefGoogle Scholar
  25. Bobkov GOM, Gilbert N, Heun P (2018) Centromere transcription allows CENP-A to transit from chromatin association to stable incorporation. J Cell Biol 217:1957–1972PubMedPubMedCentralCrossRefGoogle Scholar
  26. Bouzinba-Segard H, Guais A, Francastel C (2006) Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc Natl Acad Sci U S A 103:8709–8714PubMedPubMedCentralCrossRefGoogle Scholar
  27. Brown KE, Barnett MA, Burgtorf C, Shaw P, Buckle VJ, Brown WR (1994) Dissecting the centromere of the human Y chromosome with cloned telomeric DNA. Human Molecular Genetics 3:1227–1237PubMedCrossRefGoogle Scholar
  28. Brown DM, Chan YA, Desai PJ, Grzesik P, Oldfield LM, Vashee S, Way JC, Silver PA, Glass JI (2017) Efficient size-independent chromosome delivery from yeast to cultured cell lines. Nucleic Acids Res 45(7):e50PubMedGoogle Scholar
  29. Buckler ES, Phelps-Durr TL, Buckler CS, Dawe RK, Doebley JF, Holtsford TP (1999) Meiotic drive of chromosomal knobs reshaped the maize genome. Genetics 153:415–426PubMedPubMedCentralGoogle Scholar
  30. Bulazel KV, Ferreri GC, Eldridge MD, O’Neill RJ (2007) Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol 8:R170PubMedPubMedCentralCrossRefGoogle Scholar
  31. Camahort R, Li B, Florens L, Swanson SK, Washburn MP, Gerton JL (2007) Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Molecular Cell 26:853–865PubMedCrossRefGoogle Scholar
  32. Canzonetta C, Vernarecci S, Iuliani M, Marracino C, Belloni C, Ballario P, Filetici P (2015) SAGA DUB-Ubp8 deubiquitylates centromeric histone variant Cse4. G3 (Bethesda) 6:287–298CrossRefGoogle Scholar
  33. Capozzi O, Purgato S, Verdun di Cantogno L, Grosso E, Ciccone R, Zuffardi O, Della Valle G, Rocchi M (2008) Evolutionary and clinical neocentromeres: two faces of the same coin? Chromosoma 117:339–344PubMedCrossRefGoogle Scholar
  34. Carbone L, Nergadze SG, Magnani E, Misceo D, Francesca Cardone M, Roberto R, Bertoni L, Attolini C, Francesca Piras M, de Jong P, Raudsepp T, Chowdhary BP, Guerin G, Archidiacono N, Rocchi M, Giulotto E (2006) Evolutionary movement of centromeres in horse, donkey, and zebra. Genomics 87:777–782PubMedCrossRefGoogle Scholar
  35. Cardinale S, Bergmann JH, Kelly D, Nakano M, Valdivia MM, Kimura H, Masumoto H, Larionov V, Earnshaw WC (2009) Hierarchical inactivation of a synthetic human kinetochore by a chromatin modifier. Mol Biol Cell 20:4194–4204PubMedPubMedCentralCrossRefGoogle Scholar
  36. Catania S, Pidoux AL, Allshire RC (2015) Sequence features and transcriptional stalling within centromere DNA promote establishment of CENP-A chromatin. PLoS Genet 11:e1004986PubMedPubMedCentralCrossRefGoogle Scholar
  37. Chan DYL, Moralli D, Khoja S, Monaco ZL (2017) Noncoding centromeric RNA expression impairs chromosome stability in human and murine stem cells. Dis Markers 2017:7506976PubMedPubMedCentralCrossRefGoogle Scholar
  38. Chen CC, Dechassa ML, Bettini E, Ledoux MB, Belisario C, Heun P, Luger K, Mellone BG (2014) CAL1 is the Drosophila CENP-A assembly factor. J Cell Biol 204:313–329PubMedPubMedCentralCrossRefGoogle Scholar
  39. Chikashige Y, Kinoshita N, Nakaseko Y, Matsumoto T, Murakami S, Niwa O, Yanagida M (1989) Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of NotI restriction sites. Cell 57:739–751PubMedCrossRefGoogle Scholar
  40. Chmatal L, Gabriel SI, Mitsainas GP, Martinez-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 24:2295–2300PubMedPubMedCentralCrossRefGoogle Scholar
  41. Choi ES, Stralfors A, Catania S, Castillo AG, Svensson JP, Pidoux AL, Ekwall K, Allshire RC (2012) Factors that promote H3 chromatin integrity during transcription prevent promiscuous deposition of CENP-A(Cnp1) in fission yeast. PLoS Genetics 8:e1002985PubMedPubMedCentralCrossRefGoogle Scholar
  42. 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: CB 14:1968–1972PubMedCrossRefGoogle Scholar
  43. Contreras-Galindo R, Kaplan MH, He S, Contreras-Galindo AC, Gonzalez-Hernandez MJ, Kappes F, Dube D, Chan SM, Robinson D, Meng F, Dai M, Gitlin SD, Chinnaiyan AM, Omenn GS, Markovitz DM (2013) HIV infection reveals widespread expansion of novel centromeric human endogenous retroviruses. Genome Research 23:1505–1513PubMedPubMedCentralCrossRefGoogle Scholar
  44. Copenhaver GP, Ketel C, Wang HSW, McClellan M, Bouchonville K, Selmecki A, Lahav T, Gerami-Nejad M, Berman J (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genetics 5:e1000400CrossRefGoogle Scholar
  45. Cottarel G, Shero JH, Hieter P, Hegemann JH (1989) A 125-base-pair CEN6 DNA fragment is sufficient for complete meiotic and mitotic centromere functions in Saccharomyces cerevisiae. Mol Cell Biol 9:3342–3349PubMedPubMedCentralCrossRefGoogle Scholar
  46. Dawe RK, Lowry EG, Gent JI, Stitzer MC, Swentowsky KW, Higgins DM, Ross-Ibarra J, Wallace JG, Kanizay LB, Alabady M, Qiu W, Tseng KF, Wang N, Gao Z, Birchler JA, Harkess AE, Hodges AL, Hiatt EN (2018) A kinesin-14 motor activates neocentromeres to promote meiotic drive in maize. Cell 173:839–850 e818CrossRefGoogle Scholar
  47. De Lorenzi L, Iannuzzi A, Rossi E, Bonacina S, Parma P (2017) Centromere repositioning in cattle (Bos taurus) chromosome 17. Cytogenetic and Genome Res 151(4):191–197CrossRefGoogle Scholar
  48. de Wolf B, Kops G (2017) Kinetochore malfunction in human pathologies. Adv Exp Med Biol 1002:69–91PubMedCrossRefGoogle Scholar
  49. Deyter GM, Biggins S (2014) The FACT complex interacts with the E3 ubiquitin ligase Psh1 to prevent ectopic localization of CENP-A. Genes & Development 28:1815–1826CrossRefGoogle Scholar
  50. Drinnenberg IA, de Young D, Henikoff S, Malik HS (2014) Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. Elife 3Google Scholar
  51. Du Y, Topp CN, Dawe RK (2010) DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA. PLoS Genet 6:e1000835PubMedPubMedCentralCrossRefGoogle Scholar
  52. 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 137:485–497PubMedCrossRefGoogle Scholar
  53. Fachinetti D, Han JS, McMahon MA, Ly P, Abdullah A, Wong AJ, Cleveland DW (2015) DNA sequence-specific binding of CENP-B enhances the fidelity of human centromere function. Dev Cell 33:314–327PubMedPubMedCentralCrossRefGoogle Scholar
  54. Farr C, Fantes J, Goodfellow P, Cooke H (1991) Functional reintroduction of human telomeres into mammalian cells. Proceedings of the National Academy of Sciences of the United States of America 88:7006–7010PubMedPubMedCentralCrossRefGoogle Scholar
  55. Farr CJ, Stevanovic M, Thomson EJ, Goodfellow PN, Cooke HJ (1992) Telomere-associated chromosome fragmentation: applications in genome manipulation and analysis. Nature Genetics 2:275–282PubMedCrossRefGoogle Scholar
  56. Ferreri GC, Liscinsky DM, Mack JA, Eldridge MD, O’Neill RJ (2005) Retention of latent centromeres in the mammalian genome. J Hered 96:217–224PubMedCrossRefGoogle Scholar
  57. Ferreri GC, Marzelli M, Rens W, O’Neill RJ (2004) A centromere-specific retroviral element associated with breaks of synteny in macropodine marsupials. Cytogenetic and Genome Research 107:115–118PubMedCrossRefGoogle Scholar
  58. Ferri F, Bouzinba-Segard H, Velasco G, Hube F, Francastel C (2009) Non-coding murine centromeric transcripts associate with and potentiate Aurora B kinase. Nucleic Acids Res 37:5071–5080PubMedPubMedCentralCrossRefGoogle Scholar
  59. Folco HD, Pidoux AL, Urano T, Allshire RC (2008) Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319:94–97PubMedPubMedCentralCrossRefGoogle Scholar
  60. Foltz DR, Jansen LE, Bailey AO, Yates JR 3rd, Bassett EA, Wood S, Black BE, Cleveland DW (2009) Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137:472–484PubMedPubMedCentralCrossRefGoogle Scholar
  61. Fukagawa T, Nogami M, Yoshikawa M, Ikeno M, Okazaki T, Takami Y, Nakayama T, Oshimura M (2004) Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 6:784–791PubMedCrossRefGoogle Scholar
  62. Gaeta RT, Masonbrink RE, Krishnaswamy L, Zhao C, Birchler JA (2012) Synthetic chromosome platforms in plants. Annu Rev Plant Biol 63:307–330PubMedCrossRefGoogle Scholar
  63. Gambogi CW, Black BE (2019) The nucleosomes that mark centromere location on chromosomes old and new. Essays Biochem 63:15–27PubMedCrossRefGoogle Scholar
  64. Garsed DW, Marshall OJ, Corbin VD, Hsu A, Di Stefano L, Schroder J, Li J, Feng ZP, Kim BW, Kowarsky M, Lansdell B, Brookwell R, Myklebost O, Meza-Zepeda L, Holloway AJ, Pedeutour F, Choo KH, Damore MA, Deans AJ, Papenfuss AT, Thomas DM (2014) The architecture and evolution of cancer neochromosomes. Cancer Cell 26:653–667PubMedCrossRefGoogle Scholar
  65. 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 145:410–422PubMedPubMedCentralCrossRefGoogle Scholar
  66. Gassmann R, Rechtsteiner A, Yuen KW, Muroyama A, Egelhofer T, Gaydos L, Barron F, Maddox P, Essex A, Monen J, Ercan S, Lieb JD, Oegema K, Strome S, Desai A (2012) An inverse relationship to germline transcription defines centromeric chromatin in C. elegans. Nature 484:534–537PubMedPubMedCentralCrossRefGoogle Scholar
  67. Giordano-Santini R, Milstein S, Svrzikapa N, Tu D, Johnsen R, Baillie D, Vidal M, Dupuy D (2010) An antibiotic selection marker for nematode transgenesis. Nature Methods 7:721–723PubMedCrossRefGoogle Scholar
  68. Gonzalez M, He H, Dong Q, Sun S, Li F (2014) Ectopic centromere nucleation by CENP—a in fission yeast. Genetics 198:1433–1446PubMedPubMedCentralCrossRefGoogle Scholar
  69. Goodspeed A, Heiser LM, Gray JW, Costello JC (2016) Tumor-derived cell lines as molecular models of cancer pharmacogenomics. Mol Cancer Res 14:3–13PubMedCrossRefGoogle Scholar
  70. Grimes BR, Rhoades AA, Willard HF (2002) Alpha-satellite DNA and vector composition influence rates of human artificial chromosome formation. Mol Ther 5:798–805PubMedCrossRefGoogle Scholar
  71. Guo X, Su H, Shi Q, Fu S, Wang J, Zhang X, Hu Z, Han F (2016) De novo centromere formation and centromeric sequence expansion in wheat and its wide hybrids. PLoS Genetics 12:e1005997PubMedCrossRefGoogle Scholar
  72. Hahnenberger KM, Baum MP, Polizzi CM, Carbon J, Clarke L (1989) Construction of functional artificial minichromosomes in the fission yeast Schizosaccharomyces pombe. Proc Natl Acad Sci U S A 86:577–581PubMedPubMedCentralCrossRefGoogle Scholar
  73. Han Y, Zhang Z, Liu C, Liu J, Huang S, Jiang J, Jin W (2009) Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation. Proc Natl Acad Sci U S A 106:14937–14941PubMedPubMedCentralCrossRefGoogle Scholar
  74. Harrington JJ, Van Bokkelen G, Mays RW, Gustashaw K, Willard HF (1997) Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat Genet 15:345–355PubMedCrossRefGoogle Scholar
  75. Hasson D, Alonso A, Cheung F, Tepperberg JH, Papenhausen PR, Engelen JJ, Warburton PE (2011) Formation of novel CENP-A domains on tandem repetitive DNA and across chromosome breakpoints on human chromosome 8q21 neocentromeres. Chromosoma 120(6):621–632PubMedCrossRefGoogle Scholar
  76. Hayden KE, Strome ED, Merrett SL, Lee HR, Rudd MK, Willard HF (2013) Sequences associated with centromere competency in the human genome. Molecular and Cellular Biology 33:763–772PubMedPubMedCentralCrossRefGoogle Scholar
  77. Hedouin S, Grillo G, Ivkovic I, Velasco G, Francastel C (2017) CENP-A chromatin disassembly in stressed and senescent murine cells. Sci Rep 7:42520PubMedPubMedCentralCrossRefGoogle Scholar
  78. Helfricht A, Wiegant W, Thijssen P, Vertegaal A, Luijsterburg M, Van Attikum H (2013) Remodeling and spacing factor 1 (RSF1) deposits centromere proteins at DNA double-strand breaks to promote non-homologous end-joining. Cell Cycle 12:3070–3082PubMedPubMedCentralCrossRefGoogle Scholar
  79. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102PubMedCrossRefGoogle Scholar
  80. 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 10:303–315PubMedPubMedCentralCrossRefGoogle Scholar
  81. Hewawasam G, Shivaraju M, Mattingly M, Venkatesh S, Martin-Brown S, Florens L, Workman JL, Gerton JL (2010) Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Molecular Cell 40:444–454PubMedPubMedCentralCrossRefGoogle Scholar
  82. Hiatt EN, Kentner EK, Dawe RK (2002) Independently regulated neocentromere activity of two classes of tandem repeat arrays. Plant Cell 14:407–420PubMedPubMedCentralCrossRefGoogle Scholar
  83. Hill A, Bloom K (1987) Genetic manipulation of centromere function. Mol Cell Biol 7:2397–2405PubMedPubMedCentralCrossRefGoogle Scholar
  84. Hiratsuka M, Ueda K, Uno N, Uno K, Fukuhara S, Kurosaki H, Takehara S, Osaki M, Kazuki Y, Kurosawa Y, Nakamura T, Katoh M, Oshimura M (2015) Retargeting of microcell fusion towards recipient cell-oriented transfer of human artificial chromosome. BMC Biotechnol 15:58PubMedPubMedCentralCrossRefGoogle Scholar
  85. Ho KH, Tsuchiya D, Oliger AC, Lacefield S (2014) Localization and function of budding yeast CENP-A depends upon kinetochore protein interactions and is independent of canonical centromere sequence. Cell Rep 9:2027–2033PubMedPubMedCentralCrossRefGoogle Scholar
  86. Hori T, Shang WH, Takeuchi K, Fukagawa T (2013) The CCAN recruits CENP-A to the centromere and forms the structural core for kinetochore assembly. The Journal of Cell Biology 200:45–60PubMedPubMedCentralCrossRefGoogle Scholar
  87. Houben A, Dawe RK, Jiang J, Schubert I (2008) Engineered plant minichromosomes: a bottom-up success? The Plant Cell 20:8–10PubMedPubMedCentralCrossRefGoogle Scholar
  88. Ideue T, Cho Y, Nishimura K, Tani T (2014) Involvement of satellite I noncoding RNA in regulation of chromosome segregation. Genes Cells 19:528–538PubMedCrossRefGoogle Scholar
  89. Ishii K, Ogiyama Y, Chikashige Y, Soejima S, Masuda F, Kakuma T, Hiraoka Y, Takahashi K (2008) Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science 321:1088–1091PubMedCrossRefGoogle Scholar
  90. Iwata-Otsubo A, Dawicki-McKenna JM, Akera T, Falk SJ, Chmatal L, Yang K, Sullivan BA, Schultz RM, Lampson MA, Black BE (2017) Expanded satellite repeats amplify a discrete CENP-A nucleosome assembly site on chromosomes that drive in female meiosis. Curr Biol 27:2365–2373 e2368CrossRefGoogle Scholar
  91. Jaco I, Canela A, Vera E, Blasco MA (2008) Centromere mitotic recombination in mammalian cells. Journal of Cell Biology 181:885–892PubMedCrossRefGoogle Scholar
  92. Jain M, Olsen HE, Turner DJ, Stoddart D, Bulazel KV, Paten B, Haussler D, Willard HF, Akeson M, Miga KH (2018) Linear assembly of a human centromere on the Y chromosome. Nat Biotechnol 36:321–323PubMedPubMedCentralCrossRefGoogle Scholar
  93. Jansen LE, Black BE, Foltz DR, Cleveland DW (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176:795–805PubMedPubMedCentralCrossRefGoogle Scholar
  94. Jiang J, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575PubMedCrossRefGoogle Scholar
  95. Johnson WL, Yewdell WT, Bell JC, McNulty SM, Duda Z, O’Neill RJ, Sullivan BA, Straight AF (2017) RNA-dependent stabilization of SUV39H1 at constitutive heterochromatin. eLife 6Google Scholar
  96. Jolly C, Metz A, Govin J, Vigneron M, Turner BM, Khochbin S, Vourc’h C (2004) Stress-induced transcription of satellite III repeats. J Cell Biol 164:25–33PubMedPubMedCentralCrossRefGoogle Scholar
  97. Kagansky A, Folco HD, Almeida R, Pidoux AL, Boukaba A, Simmer F, Urano T, Hamilton GL, Allshire RC (2009) Synthetic heterochromatin bypasses RNAi and centromeric repeats to establish functional centromeres. Science 324:1716–1719PubMedPubMedCentralCrossRefGoogle Scholar
  98. Kalitsis P, Choo KH (2012) The evolutionary life cycle of the resilient centromere. Chromosoma 121:327–340PubMedCrossRefGoogle Scholar
  99. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19:489–501PubMedPubMedCentralCrossRefGoogle Scholar
  100. Kanizay LB, Albert PS, Birchler JA, Dawe RK (2013) Intragenomic conflict between the two major knob repeats of maize. Genetics 194:81–89PubMedPubMedCentralCrossRefGoogle Scholar
  101. Kapoor M, Montes de Oca Luna R, Liu G, Lozano G, Cummings C, Mancini M, Ouspenski I, Brinkley BR, May GS (1998) The cenpB gene is not essential in mice. Chromosoma 107:570–576PubMedCrossRefGoogle Scholar
  102. Kapusi E, Ma L, Teo CH, Hensel G, Himmelbach A, Schubert I, Mette MF, Kumlehn J, Houben A (2012) Telomere-mediated truncation of barley chromosomes. Chromosoma 121:181–190PubMedCrossRefGoogle Scholar
  103. Kasinathan S, Henikoff S (2018) Non-B-form DNA is enriched at centromeres. Molecular Biology and Evolution 35:949–962PubMedPubMedCentralCrossRefGoogle Scholar
  104. Katoh M, Ayabe F, Norikane S, Okada T, Masumoto H, Horike S, Shirayoshi Y, Oshimura M (2004) Construction of a novel human artificial chromosome vector for gene delivery. Biochem Biophys Res Commun 321:280–290PubMedCrossRefGoogle Scholar
  105. Kattermann G (1939) Ein neuer Karyotyp bei Roggen. Zeitschrift für Zellforschung und Mikroskopische Anatomie Abt B Chromosoma 1:284–299Google Scholar
  106. Kazuki Y, Oshimura M (2011) Human artificial chromosomes for gene delivery and the development of animal models. Mol Ther 19:1591–1601PubMedPubMedCentralCrossRefGoogle Scholar
  107. Ketel C, Wang HS, McClellan M, Bouchonville K, Selmecki A, Lahav T, Gerami-Nejad M, Berman J (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5:e1000400PubMedPubMedCentralCrossRefGoogle Scholar
  108. Kim JH, Kononenko A, Erliandri I, Kim TA, Nakano M, Iida Y, Barrett JC, Oshimura M, Masumoto H, Earnshaw WC, Larionov V, Kouprina N (2011) Human artificial chromosome (HAC) vector with a conditional centromere for correction of genetic deficiencies in human cells. Proc Natl Acad Sci U S A 108:20048–20053PubMedPubMedCentralCrossRefGoogle Scholar
  109. Klein E, Rocchi M, Ovens-Raeder A, Kosyakova N, Weise A, Ziegler M, Meins M, Morlot S, Fischer W, Volleth M, Polityko A, Ogilvie CM, Kraus C, Liehr T (2012) Five novel locations of neocentromeres in human: 18q22.1, Xq27.1 approximately 27.2, Acro p13, Acro p12, and heterochromatin of unknown origin. Cytogenet Genome Res 136:163–166PubMedCrossRefGoogle Scholar
  110. Kobayashi T, Yamada F, Hashimoto T, Abe S, Matsuda Y, Kuroiwa A (2008) Centromere repositioning in the X chromosome of XO/XO mammals, Ryukyu spiny rat. Chromosome Res 16:587–593PubMedCrossRefGoogle Scholar
  111. Koo DH, Han F, Birchler JA, Jiang J (2011) Distinct DNA methylation patterns associated with active and inactive centromeres of the maize B chromosome. Genome Res 21:908–914PubMedPubMedCentralCrossRefGoogle Scholar
  112. 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 53:631–644PubMedCrossRefGoogle Scholar
  113. Lam AL, Boivin CD, Bonney CF, Rudd MK, Sullivan BA (2006) Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc Natl Acad Sci U S A 103:4186–4191PubMedPubMedCentralCrossRefGoogle Scholar
  114. Lampson MA, Black BE (2017) Cellular and molecular mechanisms of centromere drive. Cold Spring Harb Symp Quant Biol 82:249–257PubMedCrossRefGoogle Scholar
  115. Lawrence KS, Chau T, Engebrecht J (2015) DNA damage response and spindle assembly checkpoint function throughout the cell cycle to ensure genomic integrity. PLoS Genet 11:e1005150PubMedPubMedCentralCrossRefGoogle Scholar
  116. Lee BC, Lin Z, Yuen KW (2016) RbAp46/48(LIN-53) Is required for holocentromere assembly in Caenorhabditis elegans. Cell Rep 14:1819–1828PubMedCrossRefGoogle Scholar
  117. Lefrancois P, Auerbach RK, Yellman CM, Roeder GS, Snyder M (2013) Centromere-like regions in the budding yeast genome. PLoS Genet 9:e1003209PubMedPubMedCentralCrossRefGoogle Scholar
  118. Ling YH, Yuen KWY (2019a) Centromeric non-coding RNA as a hidden epigenetic factor of the point centromere. Curr Genet 65(5):1165–1171PubMedCrossRefGoogle Scholar
  119. Ling YH, Yuen KWY (2019b) Point centromere activity requires an optimal level of centromeric noncoding RNA. Proc Natl Acad Sci U S A 116:6270–6279PubMedPubMedCentralCrossRefGoogle Scholar
  120. Liskovykh M, Lee NC, Larionov V, Kouprina N (2016) Moving toward a higher efficiency of microcell-mediated chromosome transfer. Mol Ther Methods Clin Dev 3:16043PubMedPubMedCentralCrossRefGoogle Scholar
  121. Lo AW, Craig JM, Saffery R, Kalitsis P, Irvine DV, Earle E, Magliano DJ, Choo KH (2001) A 330 kb CENP-A binding domain and altered replication timing at a human neocentromere. EMBO J 20:2087–2096PubMedPubMedCentralCrossRefGoogle Scholar
  122. Lo AW, Magliano DJ, Sibson MC, Kalitsis P, Craig JM, Choo KH (2001) A novel chromatin immunoprecipitation and array (CIA) analysis identifies a 460-kb CENP-A-binding neocentromere DNA. Genome Res 11:448–457PubMedPubMedCentralCrossRefGoogle Scholar
  123. Logsdon GA, Barrey EJ, Bassett EA, DeNizio JE, Guo LY, Panchenko T, Dawicki-McKenna JM, Heun P, Black BE (2015) Both tails and the centromere targeting domain of CENP-A are required for centromere establishment. The Journal of Cell Biology 208:521–531PubMedPubMedCentralCrossRefGoogle Scholar
  124. Logsdon GA, Gambogi CW, Liskovykh MA, Barrey EJ, Larionov V, Miga KH, Heun P, Black BE (2019) Human artificial chromosomes that bypass centromeric DNA. Cell 178:624–639 e619CrossRefGoogle Scholar
  125. Lorincz MC, Dickerson DR, Schmitt M, Groudine M (2004) Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells. Nat Struct Mol Biol 11:1068–1075PubMedCrossRefGoogle Scholar
  126. Lu J, Gilbert DM (2007) Proliferation-dependent and cell cycle regulated transcription of mouse pericentric heterochromatin. J Cell Biol 179:411–421PubMedPubMedCentralCrossRefGoogle Scholar
  127. Lyttle TW (1991) Segregation distorters. Annu Rev Genet 25:511–557PubMedCrossRefGoogle Scholar
  128. Macchia G, Nord KH, Zoli M, Purgato S, D’Addabbo P, Whelan CW, Carbone L, Perini G, Mertens F, Rocchi M, Storlazzi CT (2015) Ring chromosomes, breakpoint clusters, and neocentromeres in sarcomas. Genes Chromosomes Cancer 54:156–167PubMedCrossRefGoogle Scholar
  129. Macnab S, Whitehouse A (2009) Progress and prospects: human artificial chromosomes. Gene Ther 16:1180–1188PubMedCrossRefGoogle Scholar
  130. Maggert KA, Karpen GH (2001) The activation of a neocentromere in Drosophila requires proximity to an endogenous centromere. Genetics 158:1615–1628PubMedPubMedCentralGoogle Scholar
  131. Mahajan S, Wei KH, Nalley MJ, Gibilisco L, Bachtrog D (2018) De novo assembly of a young Drosophila Y chromosome using single-molecule sequencing and chromatin conformation capture. PLoS Biology 16:e2006348PubMedPubMedCentralCrossRefGoogle Scholar
  132. Maison C, Bailly D, Peters AH, Quivy JP, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G (2002) Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nature Genetics 30:329–334PubMedCrossRefGoogle Scholar
  133. Maison C, Bailly D, Roche D, Montes de Oca R, Probst AV, Vassias I, Dingli F, Lombard B, Loew D, Quivy JP, Almouzni G (2011) SUMOylation promotes de novo targeting of HP1alpha to pericentric heterochromatin. Nat Genet 43:220–227PubMedCrossRefGoogle Scholar
  134. Malik HS, Henikoff S (2009) Major evolutionary transitions in centromere complexity. Cell 138:1067–1082PubMedCrossRefGoogle Scholar
  135. Maloney KA, Sullivan LL, Matheny JE, Strome ED, Merrett SL, Ferris A, Sullivan BA (2012) Functional epialleles at an endogenous human centromere. Proceedings of the National Academy of Sciences of the United States of America 109:13704–13709PubMedPubMedCentralCrossRefGoogle Scholar
  136. Manzanero S, Puertas MJ (2003) Rye terminal neocentromeres: characterisation of the underlying DNA and chromatin structure. Chromosoma 111:408–415PubMedCrossRefGoogle Scholar
  137. Marshall OJ, Chueh AC, Wong LH, Choo KH (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82:261–282PubMedPubMedCentralCrossRefGoogle Scholar
  138. McClintock B (1939) The behavior in successive nuclear divisions of a chromosome broken at meiosis. Proc Natl Acad Sci U S A 25:405–416PubMedPubMedCentralCrossRefGoogle Scholar
  139. McClintock B (1941) The stability of broken ends of chromosomes in Zea mays. Genetics 26:234–282PubMedPubMedCentralGoogle Scholar
  140. McKinley KL, Cheeseman IM (2016) The molecular basis for centromere identity and function. Nat Rev Mol Cell Biol 17:16–29PubMedCrossRefGoogle Scholar
  141. McNulty SM, Sullivan LL, Sullivan BA (2017) Human centromeres produce chromosome-specific and array-specific alpha satellite transcripts that are complexed with CENP-A and CENP-C. Developmental Cell 42:226–+PubMedPubMedCentralCrossRefGoogle Scholar
  142. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10:3959–3970PubMedPubMedCentralCrossRefGoogle Scholar
  143. Mellone BG, Grive KJ, Shteyn V, Bowers SR, Oderberg I, Karpen GH (2011) Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genetics 7:e1002068PubMedPubMedCentralCrossRefGoogle Scholar
  144. Melters DP, Bradnam KR, Young HA, Telis N, May MR, Ruby JG, Sebra R, Peluso P, Eid J, Rank D, Garcia JF, Derisi JL, Smith T, Tobias C, Ross-Ibarra J, Korf I, Chan SW (2013) Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol 14:R10PubMedPubMedCentralCrossRefGoogle Scholar
  145. Meluh PB, Koshland D (1997) Budding yeast centromere composition and assembly as revealed by in vivo cross-linking. Genes Dev 11:3401–3412PubMedPubMedCentralCrossRefGoogle Scholar
  146. Mendiburo MJ, Padeken J, Fulop S, Schepers A, Heun P (2011) Drosophila CENH3 is sufficient for centromere formation. Science 334:686–690PubMedCrossRefGoogle Scholar
  147. Meraldi P, McAinsh AD, Rheinbay E, Sorger PK (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7:R23PubMedPubMedCentralCrossRefGoogle Scholar
  148. Mette MF, Houben A (2015) Engineering of plant chromosomes. Chromosome Res 23:69–76PubMedCrossRefGoogle Scholar
  149. Molina O, Vargiu G, Abad MA, Zhiteneva A, Jeyaprakash AA, Masumoto H, Kouprina N, Larionov V, Earnshaw WC (2016) Epigenetic engineering reveals a balance between histone modifications and transcription in kinetochore maintenance. Nat Commun 7:13334PubMedPubMedCentralCrossRefGoogle Scholar
  150. Montefalcone G, Tempesta S, Rocchi M, Archidiacono N (1999) Centromere repositioning. Genome Res 9:1184–1188PubMedPubMedCentralCrossRefGoogle Scholar
  151. Moreno-Moreno O, Torras-Llort M, Azorin F (2006) Proteolysis restricts localization of CID, the centromere-specific histone H3 variant of Drosophila, to centromeres. Nucleic Acids Research 34:6247–6255PubMedPubMedCentralCrossRefGoogle Scholar
  152. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ (2005) Characterization of Dicer-deficient murine embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 102:12135–12140PubMedPubMedCentralCrossRefGoogle Scholar
  153. Murray AW, Schultes NP, Szostak JW (1986) Chromosome length controls mitotic chromosome segregation in yeast. Cell 45:529–536PubMedCrossRefGoogle Scholar
  154. Murray AW, Szostak JW (1983) Construction of artificial chromosomes in yeast. Nature 305:189–193PubMedCrossRefGoogle Scholar
  155. Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J (2004) Sequencing of a rice centromere uncovers active genes. Nature Genetics 36:138–145PubMedCrossRefGoogle Scholar
  156. Nagaki K, Neumann P, Zhang D, Ouyang S, Buell CR, Cheng Z, Jiang J (2005) Structure, divergence, and distribution of the CRR centromeric retrotransposon family in rice. Mol Biol Evol 22: 845–855PubMedCrossRefGoogle Scholar
  157. Nakano M, Cardinale S, Noskov VN, Gassmann R, Vagnarelli P, Kandels-Lewis S, Larionov V, Earnshaw WC, Masumoto H (2008) Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev Cell 14:507–522PubMedPubMedCentralCrossRefGoogle Scholar
  158. Nakano M, Okamoto Y, Ohzeki J, Masumoto H (2003) Epigenetic assembly of centromeric chromatin at ectopic alpha-satellite sites on human chromosomes. J Cell Sci 116:4021–4034PubMedCrossRefGoogle Scholar
  159. Nakaseko Y, Adachi Y, Funahashi S, Niwa O, Yanagida M (1986) Chromosome walking shows a highly homologous repetitive sequence present in all the centromere regions of fission yeast. EMBO J 5:1011–1021PubMedPubMedCentralCrossRefGoogle Scholar
  160. Nakashima H, Nakano M, Ohnishi R, Hiraoka Y, Kaneda Y, Sugino A, Masumoto H (2005) Assembly of additional heterochromatin distinct from centromere-kinetochore chromatin is required for de novo formation of human artificial chromosome. Journal of Cell Science 118:5885–5898PubMedCrossRefPubMedCentralGoogle Scholar
  161. Nechemia-Arbely Y, Miga KH, Shoshani O, Aslanian A, McMahon MA, Lee AY, Fachinetti D, Yates JR 3rd, Ren B, Cleveland DW (2019) DNA replication acts as an error correction mechanism to maintain centromere identity by restricting CENP-A to centromeres. Nature Cell Biology 21:743–754PubMedCrossRefPubMedCentralGoogle Scholar
  162. Nelson AD, Lamb JC, Kobrossly PS, Shippen DE (2011) Parameters affecting telomere-mediated chromosomal truncation in Arabidopsis. The Plant Cell 23:2263–2272PubMedPubMedCentralCrossRefGoogle Scholar
  163. Nergadze SG, Piras FM, Gamba R, Corbo M, Cerutti F, McCarter JGW, Cappelletti E, Gozzo F, Harman RM, Antczak DF, Miller D, Scharfe M, Pavesi G, Raimondi E, Sullivan KF, Giulotto E (2018) Birth, evolution, and transmission of satellite-free mammalian centromeric domains. Genome Res 28:789–799PubMedPubMedCentralCrossRefGoogle Scholar
  164. Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M, Grewal SI, Watanabe Y (2002) Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol 4:89–93PubMedCrossRefGoogle Scholar
  165. Nye J, Sturgill D, Athwal R, Dalal Y (2018) HJURP antagonizes CENP-A mislocalization driven by the H3.3 chaperones HIRA and DAXX. PLoS One 13:e0205948PubMedPubMedCentralCrossRefGoogle Scholar
  166. Ohkuni K, Kitagawa K (2012) Role of transcription at centromeres in budding yeast. Transcription 3:193–197PubMedPubMedCentralCrossRefGoogle Scholar
  167. Ohkuni K, Takahashi Y, Fulp A, Lawrimore J, Au WC, Pasupala N, Levy-Myers R, Warren J, Strunnikov A, Baker RE, Kerscher O, Bloom K, Basrai MA (2016) SUMO-targeted ubiquitin ligase (STUbL) Slx5 regulates proteolysis of centromeric histone H3 variant Cse4 and prevents its mislocalization to euchromatin. Mol Biol CellGoogle Scholar
  168. Ohzeki J, Bergmann JH, Kouprina N, Noskov VN, Nakano M, Kimura H, Earnshaw WC, Larionov V, Masumoto H (2012) Breaking the HAC barrier: histone H3K9 acetyl/methyl balance regulates CENP-A assembly. EMBO J 31:2391–2402PubMedPubMedCentralCrossRefGoogle Scholar
  169. Ohzeki J, Larionov V, Earnshaw WC, Masumoto H (2015) Genetic and epigenetic regulation of centromeres: a look at HAC formation. Chromosome Research: an International Journal on the Molecular, Supramolecular and Evolutionary Aspects of Chromosome Biology 23:87–103CrossRefGoogle Scholar
  170. Ohzeki J, Nakano M, Okada T, Masumoto H (2002) CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J Cell Biol 159:765–775PubMedPubMedCentralCrossRefGoogle Scholar
  171. Okada T, Ohzeki J, Nakano M, Yoda K, Brinkley WR, Larionov V, Masumoto H (2007) CENP-B controls centromere formation depending on the chromatin context. Cell 131:1287–1300PubMedCrossRefGoogle Scholar
  172. Okamoto Y, Nakano M, Ohzeki J, Larionov V, Masumoto H (2007) A minimal CENP-A core is required for nucleation and maintenance of a functional human centromere. EMBO J 26:1279–1291PubMedPubMedCentralCrossRefGoogle Scholar
  173. 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 13:799–808PubMedCrossRefGoogle Scholar
  174. Papenfuss AT, Thomas DM (2015) The life history of neochromosomes revealed. Mol Cell Oncol 2:e1000698PubMedPubMedCentralCrossRefGoogle Scholar
  175. Partridge JF, Borgstrom B, Allshire RC (2000) Distinct protein interaction domains and protein spreading in a complex centromere. Genes Dev 14:783–791PubMedPubMedCentralGoogle Scholar
  176. Peacock WJ, Dennis ES, Rhoades MM, Pryor AJ (1981) Highly repeated DNA sequence limited to knob heterochromatin in maize. Proc Natl Acad Sci U S A 78:4490–4494PubMedPubMedCentralCrossRefGoogle Scholar
  177. Piras FM, Nergadze SG, Poletto V, Cerutti F, Ryder OA, Leeb T, Raimondi E, Giulotto E (2009) Phylogeny of horse chromosome 5q in the genus Equus and centromere repositioning. Cytogenet Genome Res 126:165–172PubMedCrossRefGoogle Scholar
  178. Ranjitkar P, Press MO, Yi X, Baker R, MacCoss MJ, Biggins S (2010) An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol Cell 40:455–464PubMedPubMedCentralCrossRefGoogle Scholar
  179. Ren X, Katoh M, Hoshiya H, Kurimasa A, Inoue T, Ayabe F, Shibata K, Toguchida J, Oshimura M (2005) A novel human artificial chromosome vector provides effective cell lineage-specific transgene expression in human mesenchymal stem cells. Stem Cells 23:1608–1616PubMedCrossRefGoogle Scholar
  180. Rhoades MM (1942) Preferential segregation in maize. Genetics 27:395–407PubMedPubMedCentralGoogle Scholar
  181. Rocchi M, Archidiacono N (2006) Genome plasticity in evolution. In: Lupski JR, Stankiewicz P (eds) Genomic disorders: the genomic basis of disease. Humana, Totowa, pp 153–165CrossRefGoogle Scholar
  182. Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R (2012) Centromere repositioning in mammals. Heredity (Edinb) 108:59–67CrossRefGoogle Scholar
  183. Roure V, Medina-Pritchard B, Anselm E, Jeyaprakash AA, Heun P (2019) Epigenetic inheritance of centromere identity in a heterologous system. biorxivGoogle Scholar
  184. Rudert F, Bronner S, Garnier JM, Dolle P (1995) Transcripts from opposite strands of gamma satellite DNA are differentially expressed during mouse development. Mamm Genome 6:76–83PubMedCrossRefGoogle Scholar
  185. Saffery R, Sumer H, Hassan S, Wong LH, Craig JM, Todokoro K, Anderson M, Stafford A, Choo KH (2003) Transcription within a functional human centromere. Mol Cell 12:509–516PubMedCrossRefGoogle Scholar
  186. Saksouk N, Simboeck E, Dejardin J (2015) Constitutive heterochromatin formation and transcription in mammals. Epigenetics Chromatin 8:3PubMedPubMedCentralCrossRefGoogle Scholar
  187. Sandler L, Novitski E (1957) Meiotic drive as an evolutionary force. The American Naturalist 91:105–110CrossRefGoogle Scholar
  188. Schaefer H, Heibl C, Renner SS (2009) Gourds afloat: a dated phylogeny reveals an Asian origin of the gourd family (Cucurbitaceae) and numerous oversea dispersal events. Proc Biol Sci 276:843–851PubMedCrossRefGoogle Scholar
  189. Schneider KL, Xie Z, Wolfgruber TK, Presting GG (2016) Inbreeding drives maize centromere evolution. Proceedings of the National Academy of Sciences of the United States of America 113:E987–E996PubMedPubMedCentralCrossRefGoogle Scholar
  190. Schubert I (2018) What is behind “centromere repositioning”? Chromosoma 127:229–234PubMedCrossRefGoogle Scholar
  191. Semple JI, Garcia-Verdugo R, Lehner B (2010) Rapid selection of transgenic C. elegans using antibiotic resistance. Nature Methods 7:725–727PubMedCrossRefGoogle Scholar
  192. Shang WH, H, Ori T, Martins NM, Toyoda A, Misu S, Monma N, Hiratani I, Maeshima K, Ikeo K, Fujiyama A, Kimura H, Earnshaw WC, Fukagawa T (2013) Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell 24:635–648PubMedPubMedCentralCrossRefGoogle Scholar
  193. Shang WH, Hori T, Martins NM, Toyoda A, Misu S, Monma N, Hiratani I, Maeshima K, Ikeo K, Fujiyama A, Kimura H, Earnshaw WC, Fukagawa T (2013) Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell 24:635–648PubMedPubMedCentralCrossRefGoogle Scholar
  194. Sharma S (2011) Non-B DNA secondary structures and their resolution by RecQ helicases. Journal of Nucleic Acids 2011:Article ID 724215 15 pagesCrossRefGoogle Scholar
  195. Sharma AB, Dimitrov S, Hamiche A, Van Dyck E (2019) Centromeric and ectopic assembly of CENP-A chromatin in health and cancer: old marks and new tracks. Nucleic Acids Research 47:1051–1069PubMedCrossRefGoogle Scholar
  196. Sharma A, Wolfgruber TK, Presting GG (2013) Tandem repeats derived from centromeric retrotransposons. BMC Genomics 14:142PubMedPubMedCentralCrossRefGoogle Scholar
  197. Shelby RD, Monier K, Sullivan KF (2000) Chromatin assembly at kinetochores is uncoupled from DNA replication. The Journal of Cell Biology 151:1113–1118PubMedCrossRefGoogle Scholar
  198. Shrestha RL, Ahn GS, Staples MI, Sathyan KM, Karpova TS, Foltz DR, Basrai MA (2017) Mislocalization of centromeric histone H3 variant CENP-A contributes to chromosomal instability (CIN) in human cells. Oncotarget 8:46781–46800PubMedPubMedCentralCrossRefGoogle Scholar
  199. Shukla M, Tong P, White SA, Singh PP, Reid AM, Catania S, Pidoux AL, Allshire RC (2018) Centromere DNA destabilizes H3 nucleosomes to promote CENP-A deposition during the cell cycle. Current Biology: CB 28:3924–3936 e3924CrossRefGoogle Scholar
  200. Sirvent N, Forus A, Lescaut W, Burel F, Benzaken S, Chazal M, Bourgeon A, Vermeesch JR, Myklebost O, Turc-Carel C, Ayraud N, Coindre JM, Pedeutour F (2000) Characterization of centromere alterations in liposarcomas. Genes Chromosomes Cancer 29:117–129PubMedCrossRefGoogle Scholar
  201. Steiner FA, Henikoff S (2014) Holocentromeres are dispersed point centromeres localized at transcription factor hotspots. Elife 3:e02025PubMedPubMedCentralCrossRefGoogle Scholar
  202. Stimpson KM, Sullivan BA (2011) Histone H3K4 methylation keeps centromeres open for business. EMBO J 30:233–234PubMedPubMedCentralCrossRefGoogle Scholar
  203. Stinchcomb DT, Shaw JE, Carr SH, Hirsh D (1985) Extrachromosomal DNA transformation of Caenorhabditis elegans. Mol Cell Biol 5:3484–3496PubMedPubMedCentralCrossRefGoogle Scholar
  204. Stirzaker C, Song JZ, Davidson B, Clark SJ (2004) Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Cancer Res 64:3871–3877PubMedCrossRefGoogle Scholar
  205. Sullivan LL, Maloney KA, Towers AJ, Gregory SG, Sullivan BA (2016) Human centromere repositioning within euchromatin after partial chromosome deletion. Chromosome Research: an International Journal on the Molecular, Supramolecular and Evolutionary Aspects of Chromosome Biology 24:451–466CrossRefGoogle Scholar
  206. Suzuki T, Kazuki Y, Oshimura M, Hara T (2016) Highly efficient transfer of chromosomes to a broad range of target cells using Chinese hamster ovary cells expressing murine leukemia virus-derived envelope proteins. PLoS One 11:e0157187PubMedPubMedCentralCrossRefGoogle Scholar
  207. Teo CH, Ma L, Kapusi E, Hensel G, Kumlehn J, Schubert I, Houben A, Mette MF (2011) Induction of telomere-mediated chromosomal truncation and stability of truncated chromosomes in Arabidopsis thaliana. Plant J 68:28–39PubMedCrossRefGoogle Scholar
  208. Thakur J, Sanyal K (2013) Efficient neocentromere formation is suppressed by gene conversion to maintain centromere function at native physical chromosomal loci in Candida albicans. Genome Res 23:638–652PubMedPubMedCentralCrossRefGoogle Scholar
  209. Tomonaga T, Matsushita K, Yamaguchi S, Oohashi T, Shimada H, Ochiai T, Yoda K, Nomura F (2003) Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res 63:3511–3516PubMedGoogle Scholar
  210. Tong P, Pidoux AL, Toda NRT, Ard R, Berger H, Shukla M, Torres-Garcia J, Muller CA, Nieduszynski CA, Allshire RC (2019) Interspecies conservation of organisation and function between nonhomologous regional centromeres. Nat Commun 10:2343PubMedPubMedCentralCrossRefGoogle Scholar
  211. Tsukahara S, Kawabe A, Kobayashi A, Ito T, Aizu T, Shin-i T, Toyoda A, Fujiyama A, Tarutani Y, Kakutani T (2012) Centromere-targeted de novo integrations of an LTR retrotransposon of Arabidopsis lyrata. Genes Dev 26:705–713CrossRefGoogle Scholar
  212. Valgardsdottir R, Chiodi I, Giordano M, Rossi A, Bazzini S, Ghigna C, Riva S, Biamonti G (2008) Transcription of Satellite III non-coding RNAs is a general stress response in human cells. Nucleic Acids Res 36:423–434PubMedCrossRefGoogle Scholar
  213. Van Hooser AA, Ouspenski II, Gregson HC, Starr DA, Yen TJ, Goldberg ML, Yokomori K, Earnshaw WC, Sullivan KF, Brinkley BR (2001) Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J Cell Sci 114:3529–3542PubMedGoogle Scholar
  214. Ventura M, Antonacci F, Cardone MF, Stanyon R, D’Addabbo P, Cellamare A, Sprague LJ, Eichler EE, Archidiacono N, Rocchi M (2007) Evolutionary formation of new centromeres in macaque. Science 316:243–246PubMedCrossRefGoogle Scholar
  215. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672–676PubMedPubMedCentralCrossRefGoogle Scholar
  216. Villasante A, Abad JP, Mendez-Lago M (2007) Centromeres were derived from telomeres during the evolution of the eukaryotic chromosome. Proceedings of the National Academy of Sciences of the United States of America 104:10542–10547PubMedPubMedCentralCrossRefGoogle Scholar
  217. Villasante A, Mendez-Lago M, Abad JP, Montejo de Garcini E (2007) The birth of the centromere. Cell Cycle 6:2872–2876PubMedCrossRefGoogle Scholar
  218. 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 52:1153–1163PubMedPubMedCentralGoogle Scholar
  219. Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR, Blocker H, Distl O, Edgar RC, Garber M, Leeb T, Mauceli E, MacLeod JN, Penedo MC, Raison JM, Sharpe T, Vogel J, Andersson L, Antczak DF, Biagi T, Binns MM, Chowdhary BP, Coleman SJ, Della Valle G, Fryc S, Guerin G, Hasegawa T, Hill EW, Jurka J, Kiialainen A, Lindgren G, Liu J, Magnani E, Mickelson JR, Murray J, Nergadze SG, Onofrio R, Pedroni S, Piras MF, Raudsepp T, Rocchi M, Roed KH, Ryder OA, Searle S, Skow L, Swinburne JE, Syvanen AC, Tozaki T, Valberg SJ, Vaudin M, White JR, Zody MC, Broad Institute Genome Sequencing P, Broad Institute Whole Genome Assembly T, Lander ES, Lindblad-Toh K (2009) Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 326:865–867PubMedPubMedCentralCrossRefGoogle Scholar
  220. Wang K, Wu Y, Zhang W, Dawe RK, Jiang J (2014) Maize centromeres expand and adopt a uniform size in the genetic background of oat. Genome Research 24:107–116PubMedPubMedCentralCrossRefGoogle Scholar
  221. Warburton PE, Dolled M, Mahmood R, Alonso A, Li S, Naritomi K, Tohma T, Nagai T, Hasegawa T, Ohashi H, Govaerts LC, Eussen BH, Van Hemel JO, Lozzio C, Schwartz S, Dowhanick-Morrissette JJ, Spinner NB, Rivera H, Crolla JA, Yu C, Warburton D (2000) Molecular cytogenetic analysis of eight inversion duplications of human chromosome 13q that each contain a neocentromere. Am J Hum Genet 66:1794–1806PubMedPubMedCentralCrossRefGoogle Scholar
  222. Waye JS, Willard HF (1987) Nucleotide sequence heterogeneity of alpha satellite repetitive DNA: a survey of alphoid sequences from different human chromosomes. Nucleic Acids Res 15:7549–7569PubMedPubMedCentralCrossRefGoogle Scholar
  223. Willard HF, Waye JS (1987) Chromosome-specific subsets of human alpha satellite DNA: analysis of sequence divergence within and between chromosomal subsets and evidence for an ancestral pentameric repeat. J Mol Evol 25:207–214PubMedCrossRefGoogle Scholar
  224. Williams BC, Murphy TD, Goldberg ML, Karpen GH (1998) Neocentromere activity of structurally acentric mini-chromosomes in Drosophila. Nat Genet 18:30–37PubMedCrossRefGoogle Scholar
  225. Wolfgruber TK, Sharma A, Schneider KL, Albert PS, Koo DH, Shi J, Gao Z, Han F, Lee H, Xu R, Allison J, Birchler JA, Jiang J, Dawe RK, Presting GG (2009) Maize centromere structure and evolution: sequence analysis of centromeres 2 and 5 reveals dynamic Loci shaped primarily by retrotransposons. PLoS Genet 5: e1000743PubMedPubMedCentralCrossRefGoogle Scholar
  226. Wong LH, Choo KH (2001) Centromere on the move. Genome Res 11:513–516PubMedCrossRefGoogle Scholar
  227. Wong NC, Wong LH, Quach JM, Canham P, Craig JM, Song JZ, Clark SJ, Choo KH (2006) Permissive transcriptional activity at the centromere through pockets of DNA hypomethylation. PLoS Genet 2:e17PubMedPubMedCentralCrossRefGoogle Scholar
  228. Wu JC, Manuelidis L (1980) Sequence definition and organization of a human repeated DNA. J Mol Biol 142:363–386PubMedCrossRefGoogle Scholar
  229. Xu C, Cheng Z, Yu W (2012) Construction of rice mini-chromosomes by telomere-mediated chromosomal truncation. Plant J 70:1070–1079PubMedCrossRefGoogle Scholar
  230. Yan X, Li C, Yang J, Wang L, Jiang C, Wei W (2017) Induction of telomere-mediated chromosomal truncation and behavior of truncated chromosomes in Brassica napus. Plant J 91:700–713PubMedCrossRefGoogle Scholar
  231. Yang L, Koo DH, Li D, Zhang T, Jiang J, Luan F, Renner SS, Henaff E, Sanseverino W, Garcia-Mas J, Casacuberta J, Senalik DA, Simon PW, Chen J, Weng Y (2014) Next-generation sequencing, FISH mapping and synteny-based modeling reveal mechanisms of decreasing dysploidy in Cucumis. Plant J 77:16–30PubMedCrossRefGoogle Scholar
  232. Yang JW, Pendon C, Yang J, Haywood N, Chand A, Brown WR (2000) Human mini-chromosomes with minimal centromeres. Human Molecular Genetics 9:1891–1902PubMedCrossRefGoogle Scholar
  233. Yu W, Han F, Gao Z, Vega JM, Birchler JA (2007) Construction and behavior of engineered minichromosomes in maize. Proceedings of the National Academy of Sciences of the United States of America 104:8924–8929PubMedPubMedCentralCrossRefGoogle Scholar
  234. Yu HG, Hiatt EN, Chan A, Sweeney M, Dawe RK (1997) Neocentromere-mediated chromosome movement in maize. J Cell Biol 139:831–840PubMedPubMedCentralCrossRefGoogle Scholar
  235. Yu W, Lamb JC, Han F, Birchler JA (2006) Telomere-mediated chromosomal truncation in maize. Proceedings of the National Academy of Sciences of the United States of America 103:17331–17336PubMedPubMedCentralCrossRefGoogle Scholar
  236. Yu Z, Zhou X, Wang W, Deng W, Fang J, Hu H, Wang Z, Li S, Cui L, Shen J, Zhai L, Peng S, Wong J, Dong S, Yuan Z, Ou G, Zhang X, Xu P, Lou J, Yang N, Chen P, Xu RM, Li G (2015) Dynamic phosphorylation of CENP-A at Ser68 orchestrates its cell-cycle-dependent deposition at centromeres. Dev Cell 32:68–81PubMedCrossRefGoogle Scholar
  237. Yuan J, Shi Q, Guo X, Liu Y, Su H, Guo X, Lv Z, Han F (2017) Site-specific transfer of chromosomal segments and genes in wheat engineered chromosomes. J Genet Genomics 44:531–539PubMedCrossRefGoogle Scholar
  238. Yuen KW, Nabeshima K, Oegema K, Desai A (2011) Rapid de novo centromere formation occurs independently of heterochromatin protein 1 in C. elegans embryos. Curr Biol 21:1800–1807PubMedPubMedCentralCrossRefGoogle Scholar
  239. Zahn J, Kaplan MH, Fischer S, Dai M, Meng F, Saha AK, Cervantes P, Chan SM, Dube D, Omenn GS, Markovitz DM, Contreras-Galindo R (2015) Expansion of a novel endogenous retrovirus throughout the pericentromeres of modern humans. Genome Biology 16:74PubMedPubMedCentralCrossRefGoogle Scholar
  240. Zeitlin SG, Baker NM, Chapados BR, Soutoglou E, Wang JY, Berns MW, Cleveland DW (2009) Double-strand DNA breaks recruit the centromeric histone CENP-A. Proc Natl Acad Sci U S A 106:15762–15767PubMedPubMedCentralCrossRefGoogle Scholar
  241. Zeng K, de las Heras JI, Ross A, Yang J, Cooke H, Shen MH (2004) Localisation of centromeric proteins to a fraction of mouse minor satellite DNA on a mini-chromosome in human, mouse and chicken cells. Chromosoma 113:84–91PubMedCrossRefGoogle Scholar
  242. Zhang W, Mao JH, Zhu W, Jain AK, Liu K, Brown JB, Karpen GH (2016) Centromere and kinetochore gene misexpression predicts cancer patient survival and response to radiotherapy and chemotherapy. Nat Commun 7:12619PubMedPubMedCentralCrossRefGoogle Scholar
  243. Zhang K, Mosch K, Fischle W, Grewal SI (2008) Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat Struct Mol Biol 15:381–388PubMedCrossRefGoogle Scholar
  244. Zhu J, Cheng KCL, Yuen KWY (2018) Histone H3K9 and H4 acetylations and transcription facilitate the initial CENP-A(HCP-3) deposition and de novo centromere establishment in Caenorhabditis elegans artificial chromosomes. Epigenetics Chromatin 11:16PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Biological SciencesThe University of Hong KongPokfulam RoadHong Kong

Personalised recommendations