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Genome biology2025; 26(1); 23; doi: 10.1186/s13059-025-03490-0

CENP-A/CENP-B uncoupling in the evolutionary reshuffling of centromeres in equids.

Abstract: While CENP-A is the epigenetic determinant of the centromeric function, the role of CENP-B, a centromeric protein binding a specific DNA sequence, the CENP-B-box, remains elusive. In the few mammalian species analyzed so far, the CENP-B box is contained in the major satellite repeat that is present at all centromeres, with the exception of the Y chromosome. We previously demonstrated that, in the genus Equus, numerous centromeres lack any satellite repeat. Results: In four Equus species, CENP-B is expressed but does not bind the majority of satellite-based centromeres, or the satellite-free ones, while it is localized at several ancestral, now-inactive, centromeres. Centromeres lacking CENP-B are functional and recruit normal amounts of CENP-A and CENP-C. The absence of CENP-B is related to the lack of CENP-B boxes rather than to peculiar features of the protein itself. CENP-B boxes are present in a previously undescribed repeat which is not the major satellite bound by CENP-A. Comparative sequence analysis suggests that this satellite was centromeric in the equid ancestor, lost centromeric function during evolution, and gave rise to a shorter CENP-A bound repeat not containing the CENP-B box but enriched in dyad symmetries. Conclusions: We propose that the uncoupling between CENP-B and CENP-A may have played a role in the extensive evolutionary reshuffling of equid centromeres. This study provides new insights into the complexity of centromere organization in a largely biodiverse world where the majority of mammalian species still have to be studied.
Publication Date: 2025-02-06 PubMed ID: 39915813PubMed Central: PMC11804003DOI: 10.1186/s13059-025-03490-0Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

CENP-A and CENP-B are proteins involved in the function and structure of centromeres, the chromosome regions critical for cell division. This study investigates how these proteins interact with centromeric DNA in different horse species, revealing that CENP-B does not always associate with centromeres, suggesting a unique evolutionary pathway for centromere organization in equids.

Background and Research Motivation

  • Centromeres are essential chromosomal regions acting as anchors during cell division, ensuring proper chromosome segregation.
  • CENP-A is a protein recognized as the key epigenetic marker defining centromere identity and function.
  • CENP-B is another centromeric protein that binds specifically to a DNA sequence known as the CENP-B box, often found in satellite DNA repeats at centromeres.
  • Previous studies in mammals show that the CENP-B box is present in major satellite repeats at almost all centromeres, except on the Y chromosome.
  • The genus Equus, which includes horses and related species, is unique because many of their centromeres lack traditional satellite DNA repeats.
  • The study aims to explore the relationship between CENP-A and CENP-B proteins and their DNA-binding sites in equids to understand centromere evolution and organization.

Key Findings

  • CENP-B protein is expressed in four different Equus species (horse family members).
  • Despite its presence, CENP-B does not bind to most centromeres that contain satellite DNA nor to those lacking satellite DNA.
  • CENP-B localizes instead to several ancestral centromeres which are currently inactive (no longer serving a centromeric function).
  • Centromeres without CENP-B are still fully functional, recruiting normal levels of CENP-A and CENP-C proteins, both important for centromere activity.
  • The lack of CENP-B binding corresponds to an absence of the CENP-B box DNA sequence, not to any unusual features in the CENP-B protein itself.
  • A previously undescribed DNA repeat containing CENP-B boxes was discovered, but this repeat is not the major satellite sequence that binds CENP-A.
  • Comparative sequence analyses suggest this satellite DNA was centromeric in the equid ancestor but lost its centromere function over time, evolving into a shorter repeat sequence lacking the CENP-B box but rich in dyad symmetries (a particular DNA structure).

Conclusions and Implications

  • The decoupling or “uncoupling” of CENP-B and CENP-A binding activities may have been an important factor in the extensive evolutionary rearrangement of centromeres observed in equids.
  • This uncoupling challenges the previously assumed strict link between satellite DNA, CENP-B presence, and centromere function in mammals.
  • Centromeres can remain functional without CENP-B, indicating variability in centromere organization and suggesting alternative mechanisms ensuring centromere stability and inheritance.
  • The findings highlight the complexity and diversity of centromere structures in natural populations and underscore the importance of studying more species beyond traditional mammalian models.
  • This research contributes to the broader understanding of chromosome evolution and epigenetic regulation in diverse taxa, helping explain how centromeres can adapt and evolve across species.

Cite This Article

APA
(2025). CENP-A/CENP-B uncoupling in the evolutionary reshuffling of centromeres in equids. Genome Biol, 26(1), 23. https://doi.org/10.1186/s13059-025-03490-0

Publication

ISSN: 1474-760X
NlmUniqueID: 100960660
Country: England
Language: English
Volume: 26
Issue: 1
Pages: 23
PII: 23

Researcher Affiliations

MeSH Terms

  • Centromere / genetics
  • Centromere / metabolism
  • Animals
  • Centromere Protein A
  • Centromere Protein B / genetics
  • Centromere Protein B / metabolism
  • Evolution, Molecular
  • Equidae / genetics
  • DNA, Satellite / genetics
  • Autoantigens / genetics
  • Autoantigens / metabolism
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism
  • Horses / genetics

Grant Funding

  • 2019-67015-29340 / National Institute of Food and Agriculture

Conflict of Interest Statement

Declarations. Ethics approval and consent to participate: Not applicable. Consent for publication: Not applicable. Competing interests: The authors declare that they have no competing interests.

References

This article includes 108 references
  1. Kalitsis P, Choo KH. The evolutionary life cycle of the resilient centromere. Chromosoma 2012;121(4):327–40.
    doi: 10.1007/s00412-012-0369-6pubmed: 22527114google scholar: lookup
  2. Choo KH. Centromerization. Trends Cell Biol 2000;10(5):182–8.
    doi: 10.1016/S0962-8924(00)01739-6pubmed: 10754560google scholar: lookup
  3. Henikoff S, Ahmad K, Malik HS. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 2001;293(5532):1098–102.
    doi: 10.1126/science.1062939pubmed: 11498581google scholar: lookup
  4. Cleveland DW, Mao Y, Sullivan KF. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 2003;112(4):407–21.
    doi: 10.1016/S0092-8674(03)00115-6pubmed: 12600307google scholar: lookup
  5. Plohl M, Luchetti A, Mestrović N, Mantovani B. Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene 2008;409(1–2):72–82.
    doi: 10.1016/j.gene.2007.11.013pubmed: 18182173google scholar: lookup
  6. Fry K, Salser W. Nucleotide sequences of HS-alpha satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 1977;12(4):1069–84.
    doi: 10.1016/0092-8674(77)90170-2pubmed: 597857google scholar: lookup
  7. Garrido-Ramos MA. Satellite DNA: An Evolving Topic. Genes (Basel) 2017;8(9):230.
    pmc: PMC5615363pubmed: 28926993
  8. Shepelev VA, Alexandrov AA, Yurov YB, Alexandrov IA. The evolutionary origin of man can be traced in the layers of defunct ancestral alpha satellites flanking the active centromeres of human chromosomes. PLoS Genet 2009;5(9): e1000641.
  9. Kursel LE, Malik HS. The cellular mechanisms and consequences of centromere drive. Curr Opin Cell Biol 2018;52:58–65.
    doi: 10.1016/j.ceb.2018.01.011pmc: PMC5988936pubmed: 29454259google scholar: lookup
  10. Allshire RC, Karpen GH. Epigenetic regulation of centromeric chromatin: old dogs, new tricks?. Nat Rev Genet 2008;9(12):923–37.
    doi: 10.1038/nrg2466pmc: PMC2586333pubmed: 19002142google scholar: lookup
  11. Sullivan KF, 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(3):581–92.
    doi: 10.1083/jcb.127.3.581pmc: PMC2120219pubmed: 7962047google scholar: lookup
  12. Masumoto H, Masukata H, Muro Y, Nozaki N, Okazaki T. A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite. J Cell Biol 1989;109(5):1963–73.
    doi: 10.1083/jcb.109.5.1963pmc: PMC2115871pubmed: 2808515google scholar: lookup
  13. Kipling D, Warburton PE. Centromeres, CENP-B and Tigger too. Trends Genet 1997;13(4):141–5.
    doi: 10.1016/S0168-9525(97)01098-6pubmed: 9097724google scholar: lookup
  14. Gamba R, Fachinetti D. From evolution to function: two sides of the same CENP-B coin?. Exp Cell Res 2020;390(2): 111959.
    doi: 10.1016/j.yexcr.2020.111959pubmed: 32173469google scholar: lookup
  15. Tanaka Y, Nureki O, Kurumizaka H, Fukai S, Kawaguchi S, Ikuta M. Crystal structure of the CENP-B protein-DNA complex: the DNA-binding domains of CENP-B induce kinks in the CENP-B box DNA. EMBO J 2001;20(23):6612–8.
    doi: 10.1093/emboj/20.23.6612pmc: PMC125324pubmed: 11726497google scholar: lookup
  16. Tawaramoto MS, Park SY, Tanaka Y, Nureki O, Kurumizaka H, Yokoyama S. Crystal structure of the human centromere protein B (CENP-B) dimerization domain at 1.65-A resolution.. J Biol Chem 2003;278(51):51454–61.
    doi: 10.1074/jbc.M310388200pubmed: 14522975google scholar: lookup
  17. Logsdon GA, Gambogi CW, Liskovykh MA, Barrey EJ, Larionov V, Miga KH. Human artificial chromosomes that bypass centromeric DNA.. Cell 2019;178(3):624-39.e19.
    doi: 10.1016/j.cell.2019.06.006pmc: PMC6657561pubmed: 31348889google scholar: lookup
  18. Kapoor M, Montes Oca Luna R de, Liu G, Lozano G, Cummings C, Mancini M. The cenpB gene is not essential in mice.. Chromosoma 1998;107(8):570–6.
    pubmed: 9933410
  19. Hudson DF, Fowler KJ, Earle E, Saffery R, Kalitsis P, Trowell H. Centromere protein B null mice are mitotically and meiotically normal but have lower body and testis weights.. J Cell Biol 1998;141(2):309–19.
    doi: 10.1083/jcb.141.2.309pmc: PMC2148459pubmed: 9548711google scholar: lookup
  20. Fowler KJ, Hudson DF, Salamonsen LA, Edmondson SR, Earle E, Sibson MC. Uterine dysfunction and genetic modifiers in centromere protein B-deficient mice.. Genome Res 2000;10(1):30–41.
    pmc: PMC310504pubmed: 10645947
  21. Dai X, Otake K, You C, Cai Q, Wang Z, Masumoto H. Identification of novel α-n-methylation of CENP-B that regulates its binding to the centromeric DNA.. J Proteome Res 2013;12(9):4167–75.
    doi: 10.1021/pr400498ypmc: PMC3787123pubmed: 23978223google scholar: lookup
  22. Fachinetti D, Han JS, McMahon MA, Ly P, Abdullah A, Wong AJ. DNA sequence-specific binding of CENP-B enhances the fidelity of human centromere function.. Dev Cell 2015;33(3):314–27.
  23. Dumont M, Gamba R, Gestraud P, Klaasen S, Worrall JT, De Vries SG. Human chromosome-specific aneuploidy is influenced by DNA-dependent centromeric features.. Embo j 2020;39(2): e102924.
    doi: 10.15252/embj.2019102924pmc: PMC6960447pubmed: 31750958google scholar: lookup
  24. Abdel-Hafiz HA, Schafer JM, Chen X, Xiao T, Gauntner TD, Li Z. Y chromosome loss in cancer drives growth by evasion of adaptive immunity.. Nature 2023;619(7970):624–31.
    doi: 10.1038/s41586-023-06234-xpmc: PMC10975863pubmed: 37344596google scholar: lookup
  25. McNulty SM, Sullivan LL, Sullivan BA. Human centromeres produce chromosome-specific and array-specific alpha satellite transcripts that are complexed with CENP-A and CENP-C.. Dev Cell 2017;42(3):226-40.e6.
  26. Morozov VM, Giovinazzi S, Ishov AM. CENP-B protects centromere chromatin integrity by facilitating histone deposition via the H3.3-specific chaperone Daxx.. Epigenetics Chromatin 2017;10(1):63.
    doi: 10.1186/s13072-017-0164-ypmc: PMC5741900pubmed: 29273057google scholar: lookup
  27. Kumon T, Ma J, Akins RB, Stefanik D, Nordgren CE, Kim J. Parallel pathways for recruiting effector proteins determine centromere drive and suppression.. Cell 2021;184(19):4904-18.e11.
    doi: 10.1016/j.cell.2021.07.037pmc: PMC8448984pubmed: 34433012google scholar: lookup
  28. Cam HP, Noma K, Ebina H, Levin HL, Grewal SI. Host genome surveillance for retrotransposons by transposon-derived proteins.. Nature 2008;451(7177):431–6.
    doi: 10.1038/nature06499pubmed: 18094683google scholar: lookup
  29. Zaratiegui M, Vaughn MW, Irvine DV, Goto D, Watt S, Bähler J. CENP-B preserves genome integrity at replication forks paused by retrotransposon LTR.. Nature 2011;469(7328):112–5.
    doi: 10.1038/nature09608pmc: PMC3057531pubmed: 21151105google scholar: lookup
  30. Kasinathan S, Henikoff S. Non-B-form DNA is enriched at centromeres.. Mol Biol Evol 2018;35(4):949–62.
    doi: 10.1093/molbev/msy010pmc: PMC5889037pubmed: 29365169google scholar: lookup
  31. Nagpal H, Ali-Ahmad A, Hirano Y, Cai W, Halic M, Fukagawa T. CENP-A and CENP-B collaborate to create an open centromeric chromatin state.. Nat Commun 2023;14(1):8227.
    doi: 10.1038/s41467-023-43739-5pmc: PMC10716449pubmed: 38086807google scholar: lookup
  32. Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.. Nature 2013;499(7456):74–8.
    doi: 10.1038/nature12323pubmed: 23803765google scholar: lookup
  33. Trifonov VA, Musilova P, Kulemsina AI. Chromosome evolution in Perissodactyla.. Cytogenet Genome Res 2012;137(2–4):208–17.
    doi: 10.1159/000339900pubmed: 22813844google scholar: lookup
  34. Trifonov VA, Stanyon R, Nesterenko AI, Fu B, Perelman PL, O’Brien PC. Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla.. Chromosome Res 2008;16(1):89–107.
    doi: 10.1007/s10577-007-1201-7pubmed: 18293107google scholar: lookup
  35. Jónsson H, Schubert M, Seguin-Orlando A, Ginolhac A, Petersen L, Fumagalli M. Speciation with gene flow in equids despite extensive chromosomal plasticity.. Proc Natl Acad Sci U S A 2014;111(52):18655–60.
    doi: 10.1073/pnas.1412627111pmc: PMC4284605pubmed: 25453089google scholar: lookup
  36. Carbone L, Nergadze SG, Magnani E, Misceo D, Francesca Cardone M, Roberto R. Evolutionary movement of centromeres in horse, donkey, and zebra.. Genomics 2006;87(6):777–82.
    doi: 10.1016/j.ygeno.2005.11.012pubmed: 16413164google scholar: lookup
  37. Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F. Genome sequence, comparative analysis, and population genetics of the domestic horse.. Science 2009;326(5954):865–7.
    doi: 10.1126/science.1178158pmc: PMC3785132pubmed: 19892987google scholar: lookup
  38. Piras FM, Nergadze SG, Poletto V, Cerutti F, Ryder OA, Leeb T. Phylogeny of horse chromosome 5q in the genus Equus and centromere repositioning.. Cytogenet Genome Res 2009;126(1–2):165–72.
    doi: 10.1159/000245916pubmed: 20016166google scholar: lookup
  39. Piras FM, Nergadze SG, Magnani E, Bertoni L, Attolini C, Khoriauli L. Uncoupling of satellite DNA and centromeric function in the genus Equus.. PLoS Genet 2010;6(2): e1000845.
  40. Musilova P, Kubickova S, Vahala J, Rubes J. Subchromosomal karyotype evolution in Equidae.. Chromosome Res 2013;21(2):175–87.
    doi: 10.1007/s10577-013-9346-zpubmed: 23532666google scholar: lookup
  41. Purgato S, Belloni E, Piras FM, Zoli M, Badiale C, Cerutti F. Centromere sliding on a mammalian chromosome.. Chromosoma 2015;124(2):277–87.
    doi: 10.1007/s00412-014-0493-6pmc: PMC4446527pubmed: 25413176google scholar: lookup
  42. Giulotto E, Raimondi E, Sullivan KF. The unique DNA sequences underlying equine centromeres.. Prog Mol Subcell Biol 2017;56:337–54.
    doi: 10.1007/978-3-319-58592-5_14pubmed: 28840244google scholar: lookup
  43. Nergadze SG, Piras FM, Gamba R, Corbo M, Cerutti F, McCarter JGW. Birth, evolution, and transmission of satellite-free mammalian centromeric domains.. Genome Res 2018;28(6):789–99.
    doi: 10.1101/gr.231159.117pmc: PMC5991519pubmed: 29712753google scholar: lookup
  44. Peng S, Petersen JL, Bellone RR, Kalbfleisch T, Kingsley NB, Barber AM. Decoding the equine genome: lessons from ENCODE.. Genes (Basel) 2021;12(11):1707.
    pmc: PMC8625040pubmed: 34828313
  45. Piras FM, Cappelletti E, Santagostino M, Nergadze SG, Giulotto E, Raimondi E. Molecular dynamics and evolution of centromeres in the genus Equus.. Int J Mol Sci 2022;23(8):4183.
    pmc: PMC9024551pubmed: 35457002
  46. Cappelletti E, Piras FM, Sola L, Santagostino M, Abdelgadir WA, Raimondi E. Robertsonian fusion and centromere repositioning contributed to the formation of satellite-free centromeres during the evolution of zebras. Mol Biol Evol 2022;39(8):msac162.
    pmc: PMC9356731pubmed: 35881460
  47. Piras FM, Cappelletti E, Abdelgadir WA, Salamon G, Vignati S, Santagostino M. A satellite-free centromere in Equus przewalskii Chromosome 10. Int J Mol Sci 2023;24(4):4134.
    pmc: PMC9961726pubmed: 36835543
  48. Cappelletti E, Piras FM, Sola L, Santagostino M, Petersen JL, Bellone RR. The localization of centromere protein A is conserved among tissues. Commun Biol 2023;6(1):963.
    doi: 10.1038/s42003-023-05335-7pmc: PMC10514049pubmed: 37735603google scholar: lookup
  49. Cerutti F, Gamba R, Mazzagatti A, Piras FM, Cappelletti E, Belloni E. The major horse satellite DNA family is associated with centromere competence. Mol Cytogenet 2016;9:35.
    doi: 10.1186/s13039-016-0242-zpmc: PMC4847189pubmed: 27123044google scholar: lookup
  50. Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R. Centromere repositioning in mammals. Heredity (Edinb) 2012;108(1):59–67.
    doi: 10.1038/hdy.2011.101pmc: PMC3238114pubmed: 22045381google scholar: lookup
  51. Kalbfleisch TS, Rice ES, DePriest MS, Walenz BP, Hestand MS, Vermeesch JR. Improved reference genome for the domestic horse increases assembly contiguity and composition. Commun Biol 2018;1:197.
    doi: 10.1038/s42003-018-0199-zpmc: PMC6240028pubmed: 30456315google scholar: lookup
  52. DNA Zoo Website [cited 2023 31 August]. Available from: https://www.dnazoo.org/.
  53. Nergadze SG, Belloni E, Piras FM, Khoriauli L, Mazzagatti A, Vella F. Discovery and comparative analysis of a novel satellite, EC137, in horses and other equids. Cytogenet Genome Res 2014;144(2):114–23.
    doi: 10.1159/000368138pubmed: 25342230google scholar: lookup
  54. Santagostino M, Khoriauli L, Gamba R, Bonuglia M, Klipstein O, Piras FM. Genome-wide evolutionary and functional analysis of the Equine Repetitive Element 1: an insertion in the myostatin promoter affects gene expression. BMC Genet 2015;16:126.
    doi: 10.1186/s12863-015-0281-1pmc: PMC4623272pubmed: 26503543google scholar: lookup
  55. Novák P, Ávila Robledillo L, Koblížková A, Vrbová I, Neumann P, Macas J. TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Res 2017;45(12): e111.
    doi: 10.1093/nar/gkx257pmc: PMC5499541pubmed: 28402514google scholar: lookup
  56. Patchigolla VSP, Mellone BG. Enrichment of non-B-form DNA at D. melanogaster centromeres. Genome Biol Evol 2022;14(5):evac054.
    pmc: PMC9070824pubmed: 35441684
  57. Vidale P, Magnani E, Nergadze SG, Santagostino M, Cristofari G, Smirnova A. The catalytic and the RNA subunits of human telomerase are required to immortalize equid primary fibroblasts. Chromosoma 2012;121(5):475–88.
    doi: 10.1007/s00412-012-0379-4pmc: PMC3443485pubmed: 22797876google scholar: lookup
  58. Vidale P, Piras FM, Nergadze SG, Bertoni L, Verini-Supplizi A, Adelson D. Chromosomal assignment of six genes (EIF4G3, HSP90, RBBP6, IL8, TERT, and TERC) in four species of the genus Equus. Anim Biotechnol 2011;22(3):119–23.
    doi: 10.1080/10495398.2011.575300pubmed: 21774619google scholar: lookup
  59. Zongaro S, de Stanchina E, Colombo T, D’Incalci M, Giulotto E, Mondello C. Stepwise neoplastic transformation of a telomerase immortalized fibroblast cell line. Cancer Res 2005;65(24):11411–8.
    doi: 10.1158/0008-5472.CAN-05-1140pubmed: 16357149google scholar: lookup
  60. Bailey JA, Gu Z, Clark RA, Reinert K, Samonte RV, Schwartz S. Recent segmental duplications in the human genome. Science 2002;297(5583):1003–7.
    doi: 10.1126/science.1072047pubmed: 12169732google scholar: lookup
  61. Ventura M, Weigl S, Carbone L, Cardone MF, Misceo D, Teti M. Recurrent sites for new centromere seeding. Genome Res 2004;14(9):1696–703.
    doi: 10.1101/gr.2608804pmc: PMC515314pubmed: 15342555google scholar: lookup
  62. Talbert PB, Henikoff S. What makes a centromere?. Exp Cell Res 2020;389(2): 111895.
    doi: 10.1016/j.yexcr.2020.111895pubmed: 32035948google scholar: lookup
  63. Suntronpong A, Kugou K, Masumoto H, Srikulnath K, Ohshima K, Hirai H. CENP-B box, a nucleotide motif involved in centromere formation, occurs in a New World monkey. Biol Lett 2016;12(3):20150817.
    doi: 10.1098/rsbl.2015.0817pmc: PMC4843215pubmed: 27029836google scholar: lookup
  64. Kugou K, Hirai H, Masumoto H, Koga A. Formation of functional CENP-B boxes at diverse locations in repeat units of centromeric DNA in New World monkeys. Sci Rep 2016;6:27833.
    doi: 10.1038/srep27833pmc: PMC4904201pubmed: 27292628google scholar: lookup
  65. Yoda K, Nakamura T, Masumoto H, Suzuki N, Kitagawa K, Nakano M. Centromere protein B of African green monkey cells: gene structure, cellular expression, and centromeric localization. Mol Cell Biol 1996;16(9):5169–77.
    doi: 10.1128/MCB.16.9.5169pmc: PMC231517pubmed: 8756674google scholar: lookup
  66. Goldberg IG, Sawhney H, Pluta AF, Warburton PE, Earnshaw WC. Surprising deficiency of CENP-B binding sites in African green monkey alpha-satellite DNA: implications for CENP-B function at centromeres. Mol Cell Biol 1996;16(9):5156–68.
    doi: 10.1128/MCB.16.9.5156pmc: PMC231516pubmed: 8756673google scholar: lookup
  67. Roberti A, Bensi M, Mazzagatti A, Piras FM, Nergadze SG, Giulotto E. Satellite DNA at the centromere is dispensable for segregation fidelity. Genes (Basel) 2019;10(6):469.
    pmc: PMC6627300pubmed: 31226862
  68. She X, Horvath JE, Jiang Z, Liu G, Furey TS, Christ L. The structure and evolution of centromeric transition regions within the human genome. Nature 2004;430(7002):857–64.
    doi: 10.1038/nature02806pubmed: 15318213google scholar: lookup
  69. Cacheux L, Ponger L, Gerbault-Seureau M, Loll F, Gey D, Richard FA. The targeted sequencing of alpha satellite DNA in Cercopithecus pogonias provides new insight into the diversity and dynamics of centromeric repeats in Old World monkeys. Genome Biol Evol 2018;10(7):1837–51.
    doi: 10.1093/gbe/evy109pmc: PMC6061836pubmed: 29860303google scholar: lookup
  70. Repenning CA, Weasma TR, Scott GR. The early Pleistocene (latest Blancan-earliest Irvingtonian) Froman Ferry fauna and history of the Glenns Ferry Formation, southwestern Idaho. Report 1995. Report No.: 2105.
  71. Bernor RL, Cirilli O, Jukar AM, Potts R, Buskianidze M, Rook L. Evolution of early Equus in Italy, Georgia, the Indian Subcontinent, East Africa, and the origins of African zebras. Front Ecol Evol 2019;7(166).
    doi: 10.3389/fevo.2019.00166google scholar: lookup
  72. Marshall OJ, Chueh AC, Wong LH, Choo KH. Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 2008;82(2):261–82.
    doi: 10.1016/j.ajhg.2007.11.009pmc: PMC2427194pubmed: 18252209google scholar: lookup
  73. Tanaka Y, Kurumizaka H, Yokoyama S. CpG methylation of the CENP-B box reduces human CENP-B binding. FEBS J 2005;272(1):282–9.
  74. Altemose N, Logsdon GA, Bzikadze AV, Sidhwani P, Langley SA, Caldas GV. Complete genomic and epigenetic maps of human centromeres. Science 2022;376(6588):eabl4178.
    doi: 10.1126/science.abl4178pmc: PMC9233505pubmed: 35357911google scholar: lookup
  75. Heslop-Harrison JS, Schwarzacher T. Nucleosomes and centromeric DNA packaging. Proc Natl Acad Sci U S A 2013;110(50):19974–5.
    doi: 10.1073/pnas.1319945110pmc: PMC3864337pubmed: 24282300google scholar: lookup
  76. Hasson D, Panchenko T, Salimian KJ, Salman MU, Sekulic N, Alonso A. The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat Struct Mol Biol 2013;20(6):687–95.
    doi: 10.1038/nsmb.2562pmc: PMC3760417pubmed: 23644596google scholar: lookup
  77. Talbert PB, Henikoff S. The genetics and epigenetics of satellite centromeres. Genome Res 2022;32(4):608–15.
    doi: 10.1101/gr.275351.121pmc: PMC8997354pubmed: 35361623google scholar: lookup
  78. Mohibi S, Srivastava S, Wang-France J, Mirza S, Zhao X, Band H. Alteration/deficiency in activation 3 (ADA3) protein, a cell cycle regulator, associates with the centromere through CENP-B and regulates chromosome segregation. J Biol Chem 2015;290(47):28299–310.
    doi: 10.1074/jbc.M115.685511pmc: PMC4653685pubmed: 26429915google scholar: lookup
  79. Trazzi S, Perini G, Bernardoni R, Zoli M, Reese JC, Musacchio A. The C-terminal domain of CENP-C displays multiple and critical functions for mammalian centromere formation. PLoS ONE 2009;4(6): e5832.
  80. Cappelletti E, Piras FM, Badiale C, Bambi M, Santagostino M, Vara C. CENP-A binding domains and recombination patterns in horse spermatocytes. Sci Rep 2019;9(1):15800.
    doi: 10.1038/s41598-019-52153-1pmc: PMC6825197pubmed: 31676881google scholar: lookup
  81. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009;10(3):R25.
    doi: 10.1186/gb-2009-10-3-r25pmc: PMC2690996pubmed: 19261174google scholar: lookup
  82. Feng J, Liu T, Qin B, Zhang Y, Liu XS. Identifying ChIP-seq enrichment using MACS. Nat Protoc 2012;7(9):1728–40.
    doi: 10.1038/nprot.2012.101pmc: PMC3868217pubmed: 22936215google scholar: lookup
  83. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999;27(2):573–80.
    doi: 10.1093/nar/27.2.573pmc: PMC148217pubmed: 9862982google scholar: lookup
  84. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 1988;16(22):10881–90.
    doi: 10.1093/nar/16.22.10881pmc: PMC338945pubmed: 2849754google scholar: lookup
  85. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9(4):357–9.
    doi: 10.1038/nmeth.1923pmc: PMC3322381pubmed: 22388286google scholar: lookup
  86. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009;25(16):2078–9.
  87. Neumann P, Navrátilová A, Schroeder-Reiter E, Koblížková A, Steinbauerová V, Chocholová E. Stretching the rules: monocentric chromosomes with multiple centromere domains. PLoS Genet 2012;8(6): e1002777.
  88. Cer RZ, Donohue DE, Mudunuri US, Temiz NA, Loss MA, Starner NJ. Non-B DB v2.0: a database of predicted non-B DNA-forming motifs and its associated tools. Nucleic Acids Res 2013;41(Database issue):D94-D100.
    pmc: PMC3531222pubmed: 23125372
  89. DNA Zoo Website [Available from: https://www.dnazoo.org/.
  90. Social Science Statistics Website [Available from: https://www.socscistatistics.com/.
  91. VassarStats: Website for Statistical Computation [Available from: http://vassarstats.net/.
  92. Ramírez F, Ryan DP, Grüning B, Bhardwaj V, Kilpert F, Richter AS. deepTools2: a next generation web server for deep-sequencing data analysis.. Nucleic Acids Res 2016;44(W1):W160–5.
    doi: 10.1093/nar/gkw257pmc: PMC4987876pubmed: 27079975google scholar: lookup
  93. Lopez-Delisle L, Rabbani L, Wolff J, Bhardwaj V, Backofen R, Grüning B. pyGenomeTracks: reproducible plots for multivariate genomic datasets.. Bioinformatics 2021;37(3):422–3.
  94. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif.. Bioinformatics 2011;27(7):1017–8.
  95. Suzuki K, Bose P, Leong-Quong RY, Fujita DJ, Riabowol K. REAP: A two minute cell fractionation method.. BMC Res Notes 2010;3:294.
    doi: 10.1186/1756-0500-3-294pmc: PMC2993727pubmed: 21067583google scholar: lookup
  96. Nergadze SG, Farnung BO, Wischnewski H, Khoriauli L, Vitelli V, Chawla R. CpG-island promoters drive transcription of human telomeres.. RNA 2009;15(12):2186–94.
    doi: 10.1261/rna.1748309pmc: PMC2779677pubmed: 19850908google scholar: lookup
  97. Solovei I, Cremer M. 3D-FISH on cultured cells combined with immunostaining.. Methods Mol Biol 2010;659:117–26.
    doi: 10.1007/978-1-60761-789-1_8pubmed: 20809307google scholar: lookup
  98. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T. Fiji: an open-source platform for biological-image analysis.. Nat Methods 2012;9(7):676–82.
    doi: 10.1038/nmeth.2019pmc: PMC3855844pubmed: 22743772google scholar: lookup
  99. Giulotto E. ChIP-seq with anti-CENP-B antibody on chromatin extracted from primary fibroblasts of horse, donkey, Grevy’s zebra and Burchell’s zebra.. National Center for Biotechnology Information .
  100. University of Pavia. Sequencing of horse centromeres. HSF fibroblasts ChIP.. Sequence Read Archive .
  101. University of Pavia. Sequencing of horse centromeres. HSF fibroblasts Input.. Sequence Read Archive .
  102. University of Pavia. Horse and donkey centromeres. DonkeyB-rep1-IP.. Sequence Read Archive .
  103. University of Pavia. Horse and donkey centromeres. DonkeyB-rep1.2-Input. Sequence Read Archive .
  104. University of Pavia. Centromeres of Burchell’s and Grevy’s zebras. EGR CENP-A ChIP. Sequence Read Archive .
  105. University of Pavia. Centromeres of Burchell’s and Grevy’s zebras. EGR Input. Sequence Read Archive .
  106. University of Pavia. Centromeres of Burchell’s and Grevy’s zebras. EBU CENP-A ChIP. Sequence Read Archive .
  107. University of Pavia. Centromeres of Burchell’s and Grevy’s zebras. EBU Input. Sequence Read Archive .
  108. Cappelletti E, Piras FM, Biundo M, Raimondi E, Nergadze S, Giulotto E. CENP-A/CENP-B uncoupling in the evolutionary reshuffling of centromeres in equids. Figshare (2025).

Citations

This article has been cited 5 times.
  1. Giunta S, Fukagawa T, O'Neill RJ, Akiyoshi B. 40 years of CENP-A: the foundation of a new era of centromere biology.. Chromosoma 2025 Dec 22;134(1):13.
    doi: 10.1007/s00412-025-00842-4pubmed: 41460345google scholar: lookup
  2. Giunta S, Fukagawa T, O'Neill RJ, Akiyoshi B. 40 years of CENP-A: the foundation of a new era of centromere biology.. Chromosome Res 2025 Dec 22;33(1):32.
    doi: 10.1007/s10577-025-09790-2pubmed: 41428263google scholar: lookup
  3. Enriquez A, Nechemia-Arbely Y. The dynamic centromere.. Chromosome Res 2025 Oct 16;33(1):22.
    doi: 10.1007/s10577-025-09779-xpubmed: 41099875google scholar: lookup
  4. Talbert PB, Henikoff S. Centromeres drive and take a break.. Chromosome Res 2025 Aug 4;33(1):17.
    doi: 10.1007/s10577-025-09777-zpubmed: 40759764google scholar: lookup
  5. Cappelletti E, Piras FM, Biundo M, Bellone RR, Finno CJ, Kalbfleisch TS, Petersen JL, Nergadze SG, Giulotto E. CENP-A and centromere evolution in equids.. Chromosome Res 2025 Jun 30;33(1):13.
    doi: 10.1007/s10577-025-09773-3pubmed: 40586953google scholar: lookup