Analyze Diet
Genome research2018; 28(6); 789-799; doi: 10.1101/gr.231159.117

Birth, evolution, and transmission of satellite-free mammalian centromeric domains.

Abstract: Mammalian centromeres are associated with highly repetitive DNA (satellite DNA), which has so far hindered molecular analysis of this chromatin domain. Centromeres are epigenetically specified, and binding of the CENPA protein is their main determinant. In previous work, we described the first example of a natural satellite-free centromere on Chromosome 11. Here, we investigated the satellite-free centromeres of by using ChIP-seq with anti-CENPA antibodies. We identified an extraordinarily high number of centromeres lacking satellite DNA (16 of 31). All of them lay in LINE- and AT-rich regions. A subset of these centromeres is associated with DNA amplification. The location of CENPA binding domains can vary in different individuals, giving rise to epialleles. The analysis of epiallele transmission in hybrids (three mules and one hinny) showed that centromeric domains are inherited as Mendelian traits, but their position can slide in one generation. Conversely, centromere location is stable during mitotic propagation of cultured cells. Our results demonstrate that the presence of more than half of centromeres void of satellite DNA is compatible with genome stability and species survival. The presence of amplified DNA at some centromeres suggests that these arrays may represent an intermediate stage toward satellite DNA formation during evolution. The fact that CENPA binding domains can move within relatively restricted regions (a few hundred kilobases) suggests that the centromeric function is physically limited by epigenetic boundaries.
Publication Date: 2018-04-30 PubMed ID: 29712753PubMed Central: PMC5991519DOI: 10.1101/gr.231159.117Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

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.

The study explores the nature of mammalian centromeres, specifically the example of satellite-free centromeres in Chromosome 11. The researchers utilized ChIP-seq with anti-CENPA antibodies to examine these centromeres and found a surprising number of centromeres lacking satellite DNA. The analysis also suggests that the position of these centromeres can slightly differ between individuals and generations, but remains generally stable during cell division. The study advances our understanding of genome stability and the potential evolutionary path of these centromere types.

Exploration of Satellite-free Centromeres

  • The researchers use ChIP-seq, a method to analyze protein interactions with DNA, to investigate the centromeres of Chromosome 11. They utilize anti-CENPA antibodies, as CENPA protein is a crucial component in the formation of centromeres.
  • In the process, they found a remarkably high number of centromeres that have no satellite DNA, which is a kind of repetitive DNA commonly present in typical centromeres. Out of 31, 16 centromeres were found to be void of satellite DNA, laying specifically in regions rich in LINE and AT elements.

Variations and Inheritance of Centromeres

  • The study also discovered variations in the location of CENPA binding domains across different individuals, indicating the existence of epigenetic variations or ‘epialleles’. These variations aren’t changes in the genome itself, but modifications in the expression of the genes that can be passed on to the next generations.
  • By analyzing the transmission of these variations in hybrids (mules and a hinny), the researchers found that while these centromeric domains are inherited following Mendelian genetics rules, their physical position on the chromosome can change over a single generation. However, the location of the centromeres maintains stability during cell division.

Implications for Evolution and Genome Stability

  • The research concludes that over half of the centromeres being void of satellite DNA does not interfere with genetic stability or species survival. This challenges previous notions about the necessity of satellite DNA for proper centromere function and genome stability.
  • Moreover, the presence of amplified DNA sequences at some centromeres may serve as an intermediate stage in the evolution of satellite DNA. This offers a new perspective on the evolutionary path of centromeres.
  • The observation that CENPA binding domains can shift their position within specific regions hints that the centromeric function might be under the control of certain epigenetic boundaries. Hence, even though the genetic content of these centromeric regions can vary between individuals and generations, their function remains restricted within specific physical constraints.

Cite This Article

APA
(2018). Birth, evolution, and transmission of satellite-free mammalian centromeric domains. Genome Res, 28(6), 789-799. https://doi.org/10.1101/gr.231159.117

Publication

ISSN: 1549-5469
NlmUniqueID: 9518021
Country: United States
Language: English
Volume: 28
Issue: 6
Pages: 789-799

Researcher Affiliations

MeSH Terms

  • Animals
  • Autoantigens / genetics
  • Centromere / genetics
  • Centromere Protein A / genetics
  • Chromatin / genetics
  • DNA, Satellite / genetics
  • Evolution, Molecular
  • Genomic Instability / genetics
  • Horses
  • Mammals

References

This article includes 78 references
  1. Adams AP, Antczak DF. Ectopic transplantation of equine invasive trophoblast.. Biol Reprod 2001 Mar;64(3):753-63.
    pubmed: 11207188doi: 10.1095/biolreprod64.3.753google scholar: lookup
  2. Amor DJ, Choo KH. Neocentromeres: role in human disease, evolution, and centromere study.. Am J Hum Genet 2002 Oct;71(4):695-714.
    pmc: PMC378529pubmed: 12196915doi: 10.1086/342730google scholar: lookup
  3. Cacheux L, Ponger L, Gerbault-Seureau M, Richard FA, Escudé C. Diversity and distribution of alpha satellite DNA in the genome of an Old World monkey: Cercopithecus solatus.. BMC Genomics 2016 Nov 14;17(1):916.
    pmc: PMC5109768pubmed: 27842493doi: 10.1186/s12864-016-3246-5google scholar: lookup
  4. Capozzi O, Purgato S, Verdun di Cantogno L, Grosso E, Ciccone R, Zuffardi O, Della Valle G, Rocchi M. Evolutionary and clinical neocentromeres: two faces of the same coin?. Chromosoma 2008 Aug;117(4):339-44.
    pubmed: 18274768doi: 10.1007/s00412-008-0150-zgoogle scholar: lookup
  5. Capozzi O, Purgato S, D'Addabbo P, Archidiacono N, Battaglia P, Baroncini A, Capucci A, Stanyon R, Della Valle G, Rocchi M. Evolutionary descent of a human chromosome 6 neocentromere: a jump back to 17 million years ago.. Genome Res 2009 May;19(5):778-84.
    pmc: PMC2675966pubmed: 19411601doi: 10.1101/gr.085688.108google scholar: lookup
  6. 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, Guérin G, Archidiacono N, Rocchi M, Giulotto E. Evolutionary movement of centromeres in horse, donkey, and zebra.. Genomics 2006 Jun;87(6):777-82.
    pubmed: 16413164doi: 10.1016/j.ygeno.2005.11.012google scholar: lookup
  7. Cardone MF, Alonso A, Pazienza M, Ventura M, Montemurro G, Carbone L, de Jong PJ, Stanyon R, D'Addabbo P, Archidiacono N, She X, Eichler EE, Warburton PE, Rocchi M. Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs.. Genome Biol 2006;7(10):R91.
    pmc: PMC1794570pubmed: 17040560doi: 10.1186/gb-2006-7-10-r91google scholar: lookup
  8. Cerutti F, Gamba R, Mazzagatti A, Piras FM, Cappelletti E, Belloni E, Nergadze SG, Raimondi E, Giulotto E. The major horse satellite DNA family is associated with centromere competence.. Mol Cytogenet 2016;9:35.
    pmc: PMC4847189pubmed: 27123044doi: 10.1186/s13039-016-0242-zgoogle scholar: lookup
  9. Chueh AC, Wong LH, Wong N, Choo KH. Variable and hierarchical size distribution of L1-retroelement-enriched CENP-A clusters within a functional human neocentromere.. Hum Mol Genet 2005 Jan 1;14(1):85-93.
    pubmed: 15537667doi: 10.1093/hmg/ddi008google scholar: lookup
  10. Chueh AC, Northrop EL, Brettingham-Moore KH, Choo KH, Wong LH. LINE retrotransposon RNA is an essential structural and functional epigenetic component of a core neocentromeric chromatin.. PLoS Genet 2009 Jan;5(1):e1000354.
  11. Clarke L, Carbon J. The structure and function of yeast centromeres.. Annu Rev Genet 1985;19:29-55.
  12. Cleveland DW, Mao Y, Sullivan KF. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling.. Cell 2003 Feb 21;112(4):407-21.
    pubmed: 12600307doi: 10.1016/s0092-8674(03)00115-6google scholar: lookup
  13. Earnshaw WC, Migeon BR. Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome.. Chromosoma 1985;92(4):290-6.
    pubmed: 2994966doi: 10.1007/bf00329812google scholar: lookup
  14. Eichler EE. Repetitive conundrums of centromere structure and function.. Hum Mol Genet 1999 Feb;8(2):151-5.
    pubmed: 9931322doi: 10.1093/hmg/8.2.151google scholar: lookup
  15. Fachinetti D, Han JS, McMahon MA, Ly P, Abdullah A, Wong AJ, Cleveland DW. DNA Sequence-Specific Binding of CENP-B Enhances the Fidelity of Human Centromere Function.. Dev Cell 2015 May 4;33(3):314-27.
  16. Ferreri GC, Liscinsky DM, Mack JA, Eldridge MD, O'Neill RJ. Retention of latent centromeres in the Mammalian genome.. J Hered 2005 May-Jun;96(3):217-24.
    pubmed: 15653556doi: 10.1093/jhered/esi029google scholar: lookup
  17. Fukagawa T, Earnshaw WC. The centromere: chromatin foundation for the kinetochore machinery.. Dev Cell 2014 Sep 8;30(5):496-508.
  18. Geigl EM, Bar-David S, Beja-Pereira A, Cothran EG, Giulotto E, Hrabar H, Oyunsuren T, Pruvost M. Genetics and paleogenetics of equids. In Wild equids (ed. Ransom JI, Kaczensky P), pp. 87–104. Johns Hopkins University Press, Baltimore, MD.
  19. Giulotto E, Saito I, Stark GR. Structure of DNA formed in the first step of CAD gene amplification.. EMBO J 1986 Sep;5(9):2115-21.
  20. Giulotto E, Raimondi E, Sullivan KF. The Unique DNA Sequences Underlying Equine Centromeres.. Prog Mol Subcell Biol 2017;56:337-354.
    pubmed: 28840244doi: 10.1007/978-3-319-58592-5_14google scholar: lookup
  21. Gong Z, Wu Y, Koblízková A, Torres GA, Wang K, Iovene M, Neumann P, Zhang W, Novák P, Buell CR, Macas J, Jiang J. Repeatless and repeat-based centromeres in potato: implications for centromere evolution.. Plant Cell 2012 Sep;24(9):3559-74.
    pmc: PMC3480287pubmed: 22968715doi: 10.1105/tpc.112.100511google scholar: lookup
  22. Han Y, Zhang Z, Liu C, Liu J, Huang S, Jiang J, Jin W. Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation.. Proc Natl Acad Sci U S A 2009 Sep 1;106(35):14937-41.
    pmc: PMC2736423pubmed: 19706458doi: 10.1073/pnas.0904833106google scholar: lookup
  23. Hayden KE, Strome ED, Merrett SL, Lee HR, Rudd MK, Willard HF. Sequences associated with centromere competency in the human genome.. Mol Cell Biol 2013 Feb;33(4):763-72.
    pmc: PMC3571344pubmed: 23230266doi: 10.1128/mcb.01198-12google scholar: lookup
  24. Henikoff S, Furuyama T. Epigenetic inheritance of centromeres.. Cold Spring Harb Symp Quant Biol 2010;75:51-60.
    pubmed: 21047902doi: 10.1101/sqb.2010.75.001google scholar: lookup
  25. Henikoff S, Ahmad K, Malik HS. The centromere paradox: stable inheritance with rapidly evolving DNA.. Science 2001 Aug 10;293(5532):1098-102.
    pubmed: 11498581doi: 10.1126/science.1062939google scholar: lookup
  26. Hori T, Kagawa N, Toyoda A, Fujiyama A, Misu S, Monma N, Makino F, Ikeo K, Fukagawa T. Constitutive centromere-associated network controls centromere drift in vertebrate cells.. J Cell Biol 2017 Jan 2;216(1):101-113.
    pmc: PMC5223601pubmed: 27940888doi: 10.1083/jcb.201605001google scholar: lookup
  27. Huang J, Zhao Y, Bai D, Shiraigol W, Li B, Yang L, Wu J, Bao W, Ren X, Jin B, Zhao Q, Li A, Bao S, Bao W, Xing Z, An A, Gao Y, Wei R, Bao Y, Bao T, Han H, Bai H, Bao Y, Zhang Y, Daidiikhuu D, Zhao W, Liu S, Ding J, Ye W, Ding F, Sun Z, Shi Y, Zhang Y, Meng H, Dugarjaviin M. Donkey genome and insight into the imprinting of fast karyotype evolution.. Sci Rep 2015 Sep 16;5:14106.
    pmc: PMC4571621pubmed: 26373886doi: 10.1038/srep14106google scholar: lookup
  28. Iwata-Otsubo A, Dawicki-McKenna JM, Akera T, Falk SJ, Chmátal L, Yang K, Sullivan BA, Schultz RM, Lampson MA, Black BE. Expanded Satellite Repeats Amplify a Discrete CENP-A Nucleosome Assembly Site on Chromosomes that Drive in Female Meiosis.. Curr Biol 2017 Aug 7;27(15):2365-2373.e8.
    pmc: PMC5567862pubmed: 28756949doi: 10.1016/j.cub.2017.06.069google scholar: lookup
  29. Kalitsis P, Choo KH. The evolutionary life cycle of the resilient centromere.. Chromosoma 2012 Aug;121(4):327-40.
    pubmed: 22527114doi: 10.1007/s00412-012-0369-6google scholar: lookup
  30. Karpen GH, Allshire RC. The case for epigenetic effects on centromere identity and function.. Trends Genet 1997 Dec;13(12):489-96.
    pubmed: 9433139doi: 10.1016/s0168-9525(97)01298-5google scholar: lookup
  31. Kobayashi T, Yamada F, Hashimoto T, Abe S, Matsuda Y, Kuroiwa A. Centromere repositioning in the X chromosome of XO/XO mammals, Ryukyu spiny rat.. Chromosome Res 2008;16(4):587-93.
    pubmed: 18432393doi: 10.1007/s10577-008-1199-5google scholar: lookup
  32. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2.. Nat Methods 2012 Mar 4;9(4):357-9.
    pmc: PMC3322381pubmed: 22388286doi: 10.1038/nmeth.1923google scholar: lookup
  33. Leeb T, Vogl C, Zhu B, de Jong PJ, Binns MM, Chowdhary BP, Scharfe M, Jarek M, Nordsiek G, Schrader F, Blöcker H. A human-horse comparative map based on equine BAC end sequences.. Genomics 2006 Jun;87(6):772-6.
    pubmed: 16603334doi: 10.1016/j.ygeno.2006.03.002google scholar: lookup
  34. Locke DP, Hillier LW, Warren WC, Worley KC, Nazareth LV, Muzny DM, Yang SP, Wang Z, Chinwalla AT, Minx P, Mitreva M, Cook L, Delehaunty KD, Fronick C, Schmidt H, Fulton LA, Fulton RS, Nelson JO, Magrini V, Pohl C, Graves TA, Markovic C, Cree A, Dinh HH, Hume J, Kovar CL, Fowler GR, Lunter G, Meader S, Heger A, Ponting CP, Marques-Bonet T, Alkan C, Chen L, Cheng Z, Kidd JM, Eichler EE, White S, Searle S, Vilella AJ, Chen Y, Flicek P, Ma J, Raney B, Suh B, Burhans R, Herrero J, Haussler D, Faria R, Fernando O, Darré F, Farré D, Gazave E, Oliva M, Navarro A, Roberto R, Capozzi O, Archidiacono N, Della Valle G, Purgato S, Rocchi M, Konkel MK, Walker JA, Ullmer B, Batzer MA, Smit AF, Hubley R, Casola C, Schrider DR, Hahn MW, Quesada V, Puente XS, Ordoñez GR, López-Otín C, Vinar T, Brejova B, Ratan A, Harris RS, Miller W, Kosiol C, Lawson HA, Taliwal V, Martins AL, Siepel A, Roychoudhury A, Ma X, Degenhardt J, Bustamante CD, Gutenkunst RN, Mailund T, Dutheil JY, Hobolth A, Schierup MH, Ryder OA, Yoshinaga Y, de Jong PJ, Weinstock GM, Rogers J, Mardis ER, Gibbs RA, Wilson RK. Comparative and demographic analysis of orang-utan genomes.. Nature 2011 Jan 27;469(7331):529-33.
    pmc: PMC3060778pubmed: 21270892doi: 10.1038/nature09687google scholar: lookup
  35. Malik HS, Bayes JJ. Genetic conflicts during meiosis and the evolutionary origins of centromere complexity.. Biochem Soc Trans 2006 Aug;34(Pt 4):569-73.
    pubmed: 16856863doi: 10.1042/bst0340569google scholar: lookup
  36. Maloney KA, Sullivan LL, Matheny JE, Strome ED, Merrett SL, Ferris A, Sullivan BA. Functional epialleles at an endogenous human centromere.. Proc Natl Acad Sci U S A 2012 Aug 21;109(34):13704-9.
    pmc: PMC3427087pubmed: 22847449doi: 10.1073/pnas.1203126109google scholar: lookup
  37. Marshall OJ, Chueh AC, Wong LH, Choo KH. Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution.. Am J Hum Genet 2008 Feb;82(2):261-82.
    pmc: PMC2427194pubmed: 18252209doi: 10.1016/j.ajhg.2007.11.009google scholar: lookup
  38. Martins NM, Bergmann JH, Shono N, Kimura H, Larionov V, Masumoto H, Earnshaw WC. Epigenetic engineering shows that a human centromere resists silencing mediated by H3K27me3/K9me3.. Mol Biol Cell 2016 Jan 1;27(1):177-96.
    pmc: PMC4694756pubmed: 26564795doi: 10.1091/mbc.e15-08-0605google scholar: lookup
  39. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. Demethylation of the zygotic paternal genome.. Nature 2000 Feb 3;403(6769):501-2.
    pubmed: 10676950doi: 10.1038/35000656google scholar: lookup
  40. McKinley KL, Cheeseman IM. The molecular basis for centromere identity and function.. Nat Rev Mol Cell Biol 2016 Jan;17(1):16-29.
    pmc: PMC8603311pubmed: 26601620doi: 10.1038/nrm.2015.5google scholar: lookup
  41. 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. Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution.. Genome Biol 2013 Jan 30;14(1):R10.
    pmc: PMC4053949pubmed: 23363705doi: 10.1186/gb-2013-14-1-r10google scholar: lookup
  42. Mendiburo MJ, Padeken J, Fülöp S, Schepers A, Heun P. Drosophila CENH3 is sufficient for centromere formation.. Science 2011 Nov 4;334(6056):686-90.
    pubmed: 22053052doi: 10.1126/science.1206880google scholar: lookup
  43. Mondello C, Smirnova A, Giulotto E. Gene amplification, radiation sensitivity and DNA double-strand breaks.. Mutat Res 2010 Apr-Jun;704(1-3):29-37.
    pubmed: 20093194doi: 10.1016/j.mrrev.2010.01.008google scholar: lookup
  44. Montefalcone G, Tempesta S, Rocchi M, Archidiacono N. Centromere repositioning.. Genome Res 1999 Dec;9(12):1184-8.
    pmc: PMC311001pubmed: 10613840doi: 10.1101/gr.9.12.1184google scholar: lookup
  45. Musilova P, Kubickova S, Vahala J, Rubes J. Subchromosomal karyotype evolution in Equidae.. Chromosome Res 2013 Apr;21(2):175-87.
    pubmed: 23532666doi: 10.1007/s10577-013-9346-zgoogle scholar: lookup
  46. Nergadze SG, Belloni E, Piras FM, Khoriauli L, Mazzagatti A, Vella F, Bensi M, Vitelli V, Giulotto E, Raimondi E. Discovery and comparative analysis of a novel satellite, EC137, in horses and other equids.. Cytogenet Genome Res 2014;144(2):114-23.
    pubmed: 25342230doi: 10.1159/000368138google scholar: lookup
  47. Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PL, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas AS, Vogt J, Szklarczyk D, Kelstrup CD, Vinther J, Dolocan A, Stenderup J, Velazquez AM, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Røed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KA, Ryder O, Andersson L, Mundy J, Krogh A, Gilbert MT, Kjær K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.. Nature 2013 Jul 4;499(7456):74-8.
    pubmed: 23803765doi: 10.1038/nature12323google scholar: lookup
  48. Palmer DK, O'Day K, Margolis RL. The centromere specific histone CENP-A is selectively retained in discrete foci in mammalian sperm nuclei.. Chromosoma 1990 Dec;100(1):32-6.
    pubmed: 2101350doi: 10.1007/bf00337600google scholar: lookup
  49. Palmer DK, O'Day K, Trong HL, Charbonneau H, Margolis RL. Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone.. Proc Natl Acad Sci U S A 1991 May 1;88(9):3734-8.
    pmc: PMC51527pubmed: 2023923doi: 10.1073/pnas.88.9.3734google scholar: lookup
  50. Panchenko T, Black BE. The epigenetic basis for centromere identity.. Prog Mol Subcell Biol 2009;48:1-32.
    pubmed: 19521810doi: 10.1007/978-3-642-00182-6_1google scholar: lookup
  51. Phanstiel DH, Boyle AP, Araya CL, Snyder MP. Sushi.R: flexible, quantitative and integrative genomic visualizations for publication-quality multi-panel figures.. Bioinformatics 2014 Oct;30(19):2808-10.
  52. Piras FM, Nergadze SG, Poletto V, Cerutti F, Ryder OA, Leeb T, Raimondi E, Giulotto E. Phylogeny of horse chromosome 5q in the genus Equus and centromere repositioning.. Cytogenet Genome Res 2009;126(1-2):165-72.
    pubmed: 20016166doi: 10.1159/000245916google scholar: lookup
  53. Piras FM, Nergadze SG, Magnani E, Bertoni L, Attolini C, Khoriauli L, Raimondi E, Giulotto E. Uncoupling of satellite DNA and centromeric function in the genus Equus.. PLoS Genet 2010 Feb 12;6(2):e1000845.
  54. Plohl M, Meštrović N, Mravinac B. Centromere identity from the DNA point of view.. Chromosoma 2014 Aug;123(4):313-25.
    pmc: PMC4107277pubmed: 24763964doi: 10.1007/s00412-014-0462-0google scholar: lookup
  55. Probst AV, Almouzni G. Heterochromatin establishment in the context of genome-wide epigenetic reprogramming.. Trends Genet 2011 May;27(5):177-85.
    pubmed: 21497937doi: 10.1016/j.tig.2011.02.002google scholar: lookup
  56. Purgato S, Belloni E, Piras FM, Zoli M, Badiale C, Cerutti F, Mazzagatti A, Perini G, Della Valle G, Nergadze SG, Sullivan KF, Raimondi E, Rocchi M, Giulotto E. Centromere sliding on a mammalian chromosome.. Chromosoma 2015 Jun;124(2):277-87.
    pmc: PMC4446527pubmed: 25413176doi: 10.1007/s00412-014-0493-6google scholar: lookup
  57. Raimondi E, Piras FM, Nergadze SG, Di Meo GP, Ruiz-Herrera A, Ponsà M, Ianuzzi L, Giulotto E. Polymorphic organization of constitutive heterochromatin in Equus asinus (2n = 62) chromosome 1.. Hereditas 2011 Jun;148(3):110-3.
  58. Ramírez F, Dündar F, Diehl S, Grüning BA, Manke T. deepTools: a flexible platform for exploring deep-sequencing data.. Nucleic Acids Res 2014 Jul;42(Web Server issue):W187-91.
    pmc: PMC4086134pubmed: 24799436doi: 10.1093/nar/gku365google scholar: lookup
  59. Raudsepp T, Lear TL, Chowdhary BP. Comparative mapping in equids: the asine X chromosome is rearranged compared to horse and Hartmann's mountain zebra.. Cytogenet Genome Res 2002;96(1-4):206-9.
    pubmed: 12438800doi: 10.1159/000063050google scholar: lookup
  60. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. Integrative genomics viewer.. Nat Biotechnol 2011 Jan;29(1):24-6.
    pmc: PMC3346182pubmed: 21221095doi: 10.1038/nbt.1754google scholar: lookup
  61. Ross JE, Woodlief KS, Sullivan BA. Inheritance of the CENP-A chromatin domain is spatially and temporally constrained at human centromeres.. Epigenetics Chromatin 2016;9:20.
    pmc: PMC4888493pubmed: 27252782doi: 10.1186/s13072-016-0071-7google scholar: lookup
  62. Saito I, Groves R, Giulotto E, Rolfe M, Stark GR. Evolution and stability of chromosomal DNA coamplified with the CAD gene.. Mol Cell Biol 1989 Jun;9(6):2445-52.
  63. Santos F, Peters AH, Otte AP, Reik W, Dean W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos.. Dev Biol 2005 Apr 1;280(1):225-36.
    pubmed: 15766761doi: 10.1016/j.ydbio.2005.01.025google scholar: lookup
  64. Schueler MG, Sullivan BA. Structural and functional dynamics of human centromeric chromatin.. Annu Rev Genomics Hum Genet 2006;7:301-13.
  65. Shang WH, Hori T, Toyoda A, Kato J, Popendorf K, Sakakibara Y, Fujiyama A, Fukagawa T. Chickens possess centromeres with both extended tandem repeats and short non-tandem-repetitive sequences.. Genome Res 2010 Sep;20(9):1219-28.
    pmc: PMC2928500pubmed: 20534883doi: 10.1101/gr.106245.110google scholar: lookup
  66. Steiner CC, Mitelberg A, Tursi R, Ryder OA. Molecular phylogeny of extant equids and effects of ancestral polymorphism in resolving species-level phylogenies.. Mol Phylogenet Evol 2012 Nov;65(2):573-81.
    pubmed: 22846684doi: 10.1016/j.ympev.2012.07.010google scholar: lookup
  67. Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M. 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 1995 Mar 1;9(5):573-86.
    pubmed: 7698647doi: 10.1101/gad.9.5.573google scholar: lookup
  68. Sullivan BA, Karpen GH. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin.. Nat Struct Mol Biol 2004 Nov;11(11):1076-83.
    pmc: PMC1283111pubmed: 15475964doi: 10.1038/nsmb845google scholar: lookup
  69. Tolomeo D, Capozzi O, Stanyon RR, Archidiacono N, D'Addabbo P, Catacchio CR, Purgato S, Perini G, Schempp W, Huddleston J, Malig M, Eichler EE, Rocchi M. Epigenetic origin of evolutionary novel centromeres.. Sci Rep 2017 Feb 3;7:41980.
    pmc: PMC5290474pubmed: 28155877doi: 10.1038/srep41980google scholar: lookup
  70. van de Werken HJG, Haan JC, Feodorova Y, Bijos D, Weuts A, Theunis K, Holwerda SJB, Meuleman W, Pagie L, Thanisch K, Kumar P, Leonhardt H, Marynen P, van Steensel B, Voet T, de Laat W, Solovei I, Joffe B. Small chromosomal regions position themselves autonomously according to their chromatin class.. Genome Res 2017 Jun;27(6):922-933.
    pmc: PMC5453326pubmed: 28341771doi: 10.1101/gr.213751.116google scholar: lookup
  71. Ventura M, Weigl S, Carbone L, Cardone MF, Misceo D, Teti M, D'Addabbo P, Wandall A, Björck E, de Jong PJ, She X, Eichler EE, Archidiacono N, Rocchi M. Recurrent sites for new centromere seeding.. Genome Res 2004 Sep;14(9):1696-703.
    pmc: PMC515314pubmed: 15342555doi: 10.1101/gr.2608804google scholar: lookup
  72. Ventura M, Antonacci F, Cardone MF, Stanyon R, D'Addabbo P, Cellamare A, Sprague LJ, Eichler EE, Archidiacono N, Rocchi M. Evolutionary formation of new centromeres in macaque.. Science 2007 Apr 13;316(5822):243-6.
    pubmed: 17431171doi: 10.1126/science.1140615google scholar: lookup
  73. Vidale P, Magnani E, Nergadze SG, Santagostino M, Cristofari G, Smirnova A, Mondello C, Giulotto E. The catalytic and the RNA subunits of human telomerase are required to immortalize equid primary fibroblasts.. Chromosoma 2012 Oct;121(5):475-88.
    pmc: PMC3443485pubmed: 22797876doi: 10.1007/s00412-012-0379-4google scholar: lookup
  74. Voullaire LE, Slater HR, Petrovic V, Choo KH. A functional marker centromere with no detectable alpha-satellite, satellite III, or CENP-B protein: activation of a latent centromere?. Am J Hum Genet 1993 Jun;52(6):1153-63.
    pmc: PMC1682274pubmed: 7684888
  75. Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR, Blöcker 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, Guérin 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, Røed KH, Ryder OA, Searle S, Skow L, Swinburne JE, Syvänen AC, Tozaki T, Valberg SJ, Vaudin M, White JR, Zody MC, Lander ES, Lindblad-Toh K. Genome sequence, comparative analysis, and population genetics of the domestic horse.. Science 2009 Nov 6;326(5954):865-7.
    pmc: PMC3785132pubmed: 19892987doi: 10.1126/science.1178158google scholar: lookup
  76. Yang F, Fu B, O'Brien PC, Nie W, Ryder OA, Ferguson-Smith MA. Refined genome-wide comparative map of the domestic horse, donkey and human based on cross-species chromosome painting: insight into the occasional fertility of mules.. Chromosome Res 2004;12(1):65-76.
  77. Zeitlin SG, Baker NM, Chapados BR, Soutoglou E, Wang JY, Berns MW, Cleveland DW. Double-strand DNA breaks recruit the centromeric histone CENP-A.. Proc Natl Acad Sci U S A 2009 Sep 15;106(37):15762-7.
    pmc: PMC2747192pubmed: 19717431doi: 10.1073/pnas.0908233106google scholar: lookup
  78. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. Model-based analysis of ChIP-Seq (MACS).. Genome Biol 2008;9(9):R137.
    pmc: PMC2592715pubmed: 18798982doi: 10.1186/gb-2008-9-9-r137google scholar: lookup

Citations

This article has been cited 28 times.
  1. Gržan T, Dombi M, Despot-Slade E, Veseljak D, Volarić M, Meštrović N, Plohl M, Mravinac B. The Low-Copy-Number Satellite DNAs of the Model Beetle Tribolium castaneum.. Genes (Basel) 2023 Apr 28;14(5).
    doi: 10.3390/genes14050999pubmed: 37239359google scholar: lookup
  2. Piras FM, Cappelletti E, Abdelgadir WA, Salamon G, Vignati S, Santagostino M, Sola L, Nergadze SG, Giulotto E. A Satellite-Free Centromere in Equus przewalskii Chromosome 10.. Int J Mol Sci 2023 Feb 18;24(4).
    doi: 10.3390/ijms24044134pubmed: 36835543google scholar: lookup
  3. Cappelletti E, Piras FM, Sola L, Santagostino M, Abdelgadir WA, Raimondi E, Lescai F, Nergadze SG, Giulotto E. Robertsonian Fusion and Centromere Repositioning Contributed to the Formation of Satellite-free Centromeres During the Evolution of Zebras.. Mol Biol Evol 2022 Aug 3;39(8).
    doi: 10.1093/molbev/msac162pubmed: 35881460google scholar: lookup
  4. Singchat W, Ahmad SF, Jaisamut K, Panthum T, Ariyaraphong N, Kraichak E, Muangmai N, Duengkae P, Payungporn S, Malaivijitnond S, Srikulnath K. Population Scale Analysis of Centromeric Satellite DNA Reveals Highly Dynamic Evolutionary Patterns and Genomic Organization in Long-Tailed and Rhesus Macaques.. Cells 2022 Jun 17;11(12).
    doi: 10.3390/cells11121953pubmed: 35741082google scholar: lookup
  5. 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 Apr 10;23(8).
    doi: 10.3390/ijms23084183pubmed: 35457002google scholar: lookup
  6. Talbert PB, Henikoff S. The genetics and epigenetics of satellite centromeres.. Genome Res 2022 Apr;32(4):608-615.
    doi: 10.1101/gr.275351.121pubmed: 35361623google scholar: lookup
  7. Kumon T, Lampson MA. Evolution of eukaryotic centromeres by drive and suppression of selfish genetic elements.. Semin Cell Dev Biol 2022 Aug;128:51-60.
    doi: 10.1016/j.semcdb.2022.03.026pubmed: 35346579google scholar: lookup
  8. Niu Y, Teng X, Zhou H, Shi Y, Li Y, Tang Y, Zhang P, Luo H, Kang Q, Xu T, He S. Characterizing mobile element insertions in 5675 genomes.. Nucleic Acids Res 2022 Mar 21;50(5):2493-2508.
    doi: 10.1093/nar/gkac128pubmed: 35212372google scholar: lookup
  9. Barbosa AC, Xu Z, Karari K, Williams W, Hauf S, Brown WRA. Mutation and selection explain why many eukaryotic centromeric DNA sequences are often A + T rich.. Nucleic Acids Res 2022 Jan 11;50(1):579-596.
    doi: 10.1093/nar/gkab1219pubmed: 34928384google scholar: lookup
  10. Peng S, Petersen JL, Bellone RR, Kalbfleisch T, Kingsley NB, Barber AM, Cappelletti E, Giulotto E, Finno CJ. Decoding the Equine Genome: Lessons from ENCODE.. Genes (Basel) 2021 Oct 27;12(11).
    doi: 10.3390/genes12111707pubmed: 34828313google scholar: lookup
  11. Mellone BG, Fachinetti D. Diverse mechanisms of centromere specification.. Curr Biol 2021 Nov 22;31(22):R1491-R1504.
    doi: 10.1016/j.cub.2021.09.083pubmed: 34813757google scholar: lookup
  12. Giannuzzi G, Logsdon GA, Chatron N, Miller DE, Reversat J, Munson KM, Hoekzema K, Bonnet-Dupeyron MN, Rollat-Farnier PA, Baker CA, Sanlaville D, Eichler EE, Schluth-Bolard C, Reymond A. Alpha Satellite Insertion Close to an Ancestral Centromeric Region.. Mol Biol Evol 2021 Dec 9;38(12):5576-5587.
    doi: 10.1093/molbev/msab244pubmed: 34464971google scholar: lookup
  13. Schotanus K, Yadav V, Heitman J. Epigenetic dynamics of centromeres and neocentromeres in Cryptococcus deuterogattii.. PLoS Genet 2021 Aug;17(8):e1009743.
    doi: 10.1371/journal.pgen.1009743pubmed: 34464380google scholar: lookup
  14. Kuhn GCS, Heringer P, Dias GB. Structure, Organization, and Evolution of Satellite DNAs: Insights from the Drosophila repleta and D. virilis Species Groups.. Prog Mol Subcell Biol 2021;60:27-56.
    doi: 10.1007/978-3-030-74889-0_2pubmed: 34386871google scholar: lookup
  15. Murillo-Pineda M, Valente LP, Dumont M, Mata JF, Fachinetti D, Jansen LET. Induction of spontaneous human neocentromere formation and long-term maturation.. J Cell Biol 2021 Mar 1;220(3).
    doi: 10.1083/jcb.202007210pubmed: 33443568google scholar: lookup
  16. Balzano E, Giunta S. Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function.. Genes (Basel) 2020 Aug 10;11(8).
    doi: 10.3390/genes11080912pubmed: 32784998google scholar: lookup
  17. Ali-Ahmad A, Sekulić N. CENP-A nucleosome-a chromatin-embedded pedestal for the centromere: lessons learned from structural biology.. Essays Biochem 2020 Sep 4;64(2):205-221.
    doi: 10.1042/EBC20190074pubmed: 32720682google scholar: lookup
  18. Santagostino M, Piras FM, Cappelletti E, Del Giudice S, Semino O, Nergadze SG, Giulotto E. Insertion of Telomeric Repeats in the Human and Horse Genomes: An Evolutionary Perspective.. Int J Mol Sci 2020 Apr 18;21(8).
    doi: 10.3390/ijms21082838pubmed: 32325780google scholar: lookup
  19. Schotanus K, Heitman J. Centromere deletion in Cryptococcus deuterogattii leads to neocentromere formation and chromosome fusions.. Elife 2020 Apr 20;9.
    doi: 10.7554/eLife.56026pubmed: 32310085google scholar: lookup
  20. Gambogi CW, Dawicki-McKenna JM, Logsdon GA, Black BE. The unique kind of human artificial chromosome: Bypassing the requirement for repetitive centromere DNA.. Exp Cell Res 2020 Jun 15;391(2):111978.
    doi: 10.1016/j.yexcr.2020.111978pubmed: 32246994google scholar: lookup
  21. Tolomeo D, Capozzi O, Chiatante G, Sineo L, Ishida T, Archidiacono N, Rocchi M, Stanyon R. Eight million years of maintained heterozygosity in chromosome homologs of cercopithecine monkeys.. Chromosoma 2020 Mar;129(1):57-67.
    doi: 10.1007/s00412-020-00731-ypubmed: 31925526google scholar: lookup
  22. Ling YH, Lin Z, Yuen KWY. Genetic and epigenetic effects on centromere establishment.. Chromosoma 2020 Mar;129(1):1-24.
    doi: 10.1007/s00412-019-00727-3pubmed: 31781852google scholar: lookup
  23. Cappelletti E, Piras FM, Badiale C, Bambi M, Santagostino M, Vara C, Masterson TA, Sullivan KF, Nergadze SG, Ruiz-Herrera A, Giulotto E. CENP-A binding domains and recombination patterns in horse spermatocytes.. Sci Rep 2019 Nov 1;9(1):15800.
    doi: 10.1038/s41598-019-52153-1pubmed: 31676881google scholar: lookup
  24. Raudsepp T, Finno CJ, Bellone RR, Petersen JL. Ten years of the horse reference genome: insights into equine biology, domestication and population dynamics in the post-genome era.. Anim Genet 2019 Dec;50(6):569-597.
    doi: 10.1111/age.12857pubmed: 31568563google scholar: lookup
  25. Roberti A, Bensi M, Mazzagatti A, Piras FM, Nergadze SG, Giulotto E, Raimondi E. Satellite DNA at the Centromere is Dispensable for Segregation Fidelity.. Genes (Basel) 2019 Jun 20;10(6).
    doi: 10.3390/genes10060469pubmed: 31226862google scholar: lookup
  26. Chang CH, Chavan A, Palladino J, Wei X, Martins NMC, Santinello B, Chen CC, Erceg J, Beliveau BJ, Wu CT, Larracuente AM, Mellone BG. Islands of retroelements are major components of Drosophila centromeres.. PLoS Biol 2019 May;17(5):e3000241.
    doi: 10.1371/journal.pbio.3000241pubmed: 31086362google scholar: lookup
  27. Hartley G, O'Neill RJ. Centromere Repeats: Hidden Gems of the Genome.. Genes (Basel) 2019 Mar 16;10(3).
    doi: 10.3390/genes10030223pubmed: 30884847google scholar: lookup
  28. Matveevsky S, Ivanitskaya E, Spangenberg V, Bakloushinskaya I, Kolomiets O. Reorganization of the Y Chromosomes Enhances Divergence in Israeli Mole Rats Nannospalax ehrenbergi (Spalacidae, Rodentia): Comparative Analysis of Meiotic and Mitotic Chromosomes.. Genes (Basel) 2018 May 24;9(6).
    doi: 10.3390/genes9060272pubmed: 29794981google scholar: lookup