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The Unique DNA Sequences Underlying Equine Centromeres

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Centromeres and Kinetochores

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

Abstract

Centromeres are highly distinctive genetic loci whose function is specified largely by epigenetic mechanisms. Understanding the role of DNA sequences in centromere function has been a daunting task due to the highly repetitive nature of centromeres in animal chromosomes. The discovery of a centromere devoid of satellite DNA in the domestic horse consolidated observations on the epigenetic nature of centromere identity, showing that entirely natural chromosomes could function without satellite DNA cues. Horses belong to the genus Equus which exhibits a very high degree of evolutionary plasticity in centromere position and DNA sequence composition. Examination of horses has revealed that the position of the satellite-free centromere is variable among individuals. Analysis of centromere location and composition in other Equus species, including domestic donkey and zebras, confirms that the satellite-less configuration of centromeres is common in this group which has undergone particularly rapid karyotype evolution. These features have established the equids as a new mammalian system in which to investigate the molecular organization, dynamics and evolutionary behaviour of centromeres.

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References

  • Alkan C, Cardone MF, Catacchio CR et al (2011) Genome-wide characterization of centromeric satellites from multiple mammalian genomes. Genome Res 21:137–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amor DJ, Choo KHA (2002) Neocentromeres: role in human disease, evolution, and centromere study. Am J Hum Genet 71:695–714

    Article  PubMed  PubMed Central  Google Scholar 

  • Amor DJ, Bentley K, Ryan J et al (2004) Human centromere repositioning “in progress”. Proc Natl Acad Sci USA 101:6542–6547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anglana M, Bertoni L, Giulotto E (1996a) Cloning of a polymorphic sequence from the nontranscribed spacer of horse rDNA. Mamm Genome 7:539–541

    Article  CAS  PubMed  Google Scholar 

  • Anglana M, Vigoni MT, Giulotto E (1996b) Four horse genomic fragments containing minisatellites detect highly polymorphic DNA fingerprints. Anim Genet 27:286

    Article  CAS  PubMed  Google Scholar 

  • Barry AE, Bateman M, Howman EV et al (2000) The 10q25 neocentromere and its inactive progenitor have identical primary nucleotide sequence: further evidence for epigenetic modification. Genome Res 10:832–838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergmann JH, Rodríguez MG, Martins NMC et al (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore: H3K4me2 and kinetochore maintenance. EMBO J 30:328–340

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broad TE, Ede AJ, Forrest JW et al (1995a) Families of tandemly repeated DNA elements from horse: cloning, nucleotide sequence, and organization. Genome 38:1285–1289

    Article  CAS  PubMed  Google Scholar 

  • Broad TE, Forrest JW, Lewis PE et al (1995b) Cloning of a DNA repeat element from horse: DNA sequence and chromosomal localization. Genome 38:1132–1138

    Article  CAS  PubMed  Google Scholar 

  • Carbone L, Nergadze SG, Magnani E et al (2006) Evolutionary movement of centromeres in horse, donkey, and zebra. Genomics 87:777–782

    Article  CAS  PubMed  Google Scholar 

  • Carone DM, Longo MS, Ferreri GC et al (2009) A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres. Chromosoma 118(1):113–125

    Article  CAS  PubMed  Google Scholar 

  • Cerutti F, Gamba R, Mazzagatti A et al (2016) The major horse satellite DNA family is associated with centromere competence. Mol Cytogenet 9:35

    Article  PubMed  PubMed Central  Google Scholar 

  • Chueh AC, Northrop EL, Brettingham-Moore KH et al (2009) LINE retrotransposon RNA is an essential structural and functional epigenetic component of a core neocentromeric chromatin. PLoS Genet 5(1):e1000354

    Article  PubMed  PubMed Central  Google Scholar 

  • Earnshaw WC, Ratrie H, Stetten G (1989) Visualization of centromere proteins CENP-B and CENP-C on a stable dicentric chromosome in cytological spreads. Chromosoma 98:1–12

    Article  CAS  PubMed  Google Scholar 

  • Ekwall K (2007) Epigenetic control of centromere behavior. Annu Rev Genet 41:63–81

    Article  CAS  PubMed  Google Scholar 

  • Fachinetti D, Han JS, McMahon MA et al (2015) dna sequence-specific binding of CENP-B enhances the fidelity of human centromere function. Dev Cell 33:314–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong Z, Wu Y, Koblízková A, Torres GA et al (2012) Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24(9):3559–3574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayden KE, Strome ED, Merrett SL et al (2013) Sequences associated with centromere competency in the human genome. Mol Cell Biol 33:763–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102

    Article  CAS  PubMed  Google Scholar 

  • Karpen GH, Allshire RC (1997) The case for epigenetic effects on centromere identity and function. Trends Genet TIG 13:489–496

    Article  CAS  PubMed  Google Scholar 

  • Locke DP, Hillier LW, Warren WC et al (2011) Comparative and demographic analysis of orang-utan genomes. Nature 469:529–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maloney KA, Sullivan LL, Matheny JE et al (2012) Functional epialleles at an endogenous human centromere. Proc Natl Acad Sci USA 109:13704–13709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marshall OJ, Chueh AC, Wong LH, Choo KHA (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82:261–282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montefalcone G, Tempesta S, Rocchi M, Archidiacono N (1999) Centromere repositioning. Genome Res 9:1184–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Musilova P, Kubickova S, Zrnova E et al (2007) Karyotypic relationships among Equus grevyi, Equus burchelli and domestic horse defined using horse chromosome arm-specific probes. Chromosome Res 15:807–813

    Article  CAS  PubMed  Google Scholar 

  • Musilova P, Kubickova S, Vahala J, Rubes J (2013) Subchromosomal karyotype evolution in Equidae. Chromosome Res 21:175–187

    Article  CAS  PubMed  Google Scholar 

  • Nergadze SG, Lupotto M, Pellanda P et al (2010) Mitochondrial DNA insertions in the nuclear horse genome. Anim Genet 41(Suppl 2):176–185

    Article  CAS  PubMed  Google Scholar 

  • Nergadze SG, Belloni E, Piras FM et al (2014) Discovery and comparative analysis of a novel satellite, EC137, in horses and other equids. Cytogenet Genome Res 144:114–123

    Article  PubMed  Google Scholar 

  • Oakenfull EA, Clegg JB (1998) Phylogenetic relationships within the genus Equus and the evolution of alpha and theta globin genes. J Mol Evol 47:772–783

    Article  CAS  PubMed  Google Scholar 

  • Orlando L, Ginolhac A, Zhang G et al (2013) Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499(7456):74–78

    Article  CAS  PubMed  Google Scholar 

  • Panchenko T, Black BE (2009) The epigenetic basis for centromere identity. Springer, Berlin, pp 1–32

    Google Scholar 

  • Piras FM, Nergadze SG, Poletto V et al (2009) Phylogeny of horse chromosome 5q in the genus Equus and centromere repositioning. Cytogenet Genome Res 126:165–172

    Article  CAS  PubMed  Google Scholar 

  • Piras FM, Nergadze SG, Magnani E et al (2010) Uncoupling of satellite DNA and centromeric function in the genus Equus. PLoS Genet 6:e1000845

    Article  PubMed  PubMed Central  Google Scholar 

  • Purgato S, Belloni E, Piras FM et al (2015) Centromere sliding on a mammalian chromosome. Chromosoma 124:277–287

    Article  CAS  PubMed  Google Scholar 

  • Quénet D, Dalal Y (2014) A long non-coding RNA is required for targeting centromeric protein A to the human centromere. Elife 3:e03254

    Article  PubMed  PubMed Central  Google Scholar 

  • Raimondi E, Piras FM, Nergadze SG et al (2011) Polymorphic organization of constitutive heterochromatin in Equus asinus (2n = 62) chromosome 1. Hereditas 148:110–113

    Article  PubMed  Google Scholar 

  • Rocchi M, Archidiacono N, Schempp W et al (2012) Centromere repositioning in mammals. Heredity 108:59–67

    Article  CAS  PubMed  Google Scholar 

  • Ryder OA, Epel NC, Benirschke K (1978) Chromosome banding studies of the Equidae. Cytogenet Cell Genet 20:332–350

    Article  CAS  PubMed  Google Scholar 

  • Saffery R, Irvine DV, Griffiths B et al (2000) Human centromeres and neocentromeres show identical distribution patterns of >20 functionally important kinetochore-associated proteins. Hum Mol Genet 9:175–185

    Article  CAS  PubMed  Google Scholar 

  • Sakagami M, Hirota K, Awata T, Yasue H (1994) Molecular cloning of an equine satellite-type DNA sequence and its chromosomal localization. Cytogenet Cell Genet 66:27–30

    Article  CAS  PubMed  Google Scholar 

  • Santagostino M, Khoriauli L, Gamba R et al (2015) Genome-wide evolutionary and functional analysis of the equine repetitive element 1: an insertion in the myostatin promoter affects gene expression. BMC Genet 16:126

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanyal K, Baum M, Carbon J (2004) Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc Natl Acad Sci USA 101(31):11374–11379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scocchi M, Bontempo D, Boscolo S et al (1999) Novel cathelicidins in horse leukocytes(1). FEBS Lett 457:459–464

    Article  CAS  PubMed  Google Scholar 

  • Shang W-H, Hori T, Martins NMC et al (2013) Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell 24:635–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • She X, Horvath JE, Jiang Z et al (2004) The structure and evolution of centromeric transition regions within the human genome. Nature 430:857–864

    Article  CAS  PubMed  Google Scholar 

  • Shepelev VA, Alexandrov AA, Yurov YB, Alexandrov IA (2009) 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 5(9):e1000641

    Article  PubMed  PubMed Central  Google Scholar 

  • Springer MS, Murphy WJ, Eizirik E, O’Brien SJ (2003) Placental mammal diversification and the Cretaceous-Tertiary boundary. PNAS 100:1056–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanyon R, Rocchi M, Capozzi O et al (2008) Primate chromosome evolution: ancestral karyotypes, marker order and neocentromeres. Chromosome Res 16:17–39

    Article  CAS  PubMed  Google Scholar 

  • Steiner CC, Mitelberg A, Tursi R, Ryder OA (2012) Molecular phylogeny of extant equids and effects of ancestral polymorphism in resolving species-level phylogenies. Mol Phylogenet Evol 65:573–581

    Article  PubMed  Google Scholar 

  • Trifonov VA, Stanyon R, Nesterenko AI et al (2008) Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla. Chromosome Res 16:89–107

    Article  CAS  PubMed  Google Scholar 

  • Tyler-Smith C, Gimelli G, Giglio S et al (1999) Transmission of a fully functional human neocentromere through three generations. Am J Hum Genet 64:1440–1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ventura M, Antonacci F, Cardone MF et al (2007) Evolutionary formation of new centromeres in macaque. Science 316:243–246

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wade CM, Giulotto E, Sigurdsson S et al (2009) Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 326:865–867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warburton PE, Dolled M, Mahmood R et al (2000) Molecular cytogenetic analysis of eight inversion duplications of human chromosome 13q that each contain a neocentromere. Am J Hum Genet 66:1794–1806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wijers ER, Zijlstra C, Lenstra JA (1993) Rapid evolution of horse satellite DNA. Genomics 18:113–117

    Article  CAS  PubMed  Google Scholar 

  • Willard HF (1991) Evolution of alpha satellite. Curr Opin Genet Dev 1:509–514

    Article  CAS  PubMed  Google Scholar 

  • Yang F, Fu B, O’Brien PCM et al (2003) Karyotypic relationships of horses and zebras: results of cross-species chromosome painting. Cytogenet Genome Res 102:235–243

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The laboratories were supported by grants from Consiglio Nazionale delle Ricerche (CNR-Progetto Bandiera Epigenomica), from Ministero dell’Istruzione dell’Università e della Ricerca (MIUR-PRIN) and from Science Foundation Ireland (12/A/1370).

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Correspondence to Elena Giulotto .

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Giulotto, E., Raimondi, E., Sullivan, K.F. (2017). The Unique DNA Sequences Underlying Equine Centromeres. In: Black, B. (eds) Centromeres and Kinetochores. Progress in Molecular and Subcellular Biology, vol 56. Springer, Cham. https://doi.org/10.1007/978-3-319-58592-5_14

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