Chromatin configuration and epigenetic landscape at the sex chromosome bivalent during equine spermatogenesis.
Abstract: Pairing of the sex chromosomes during mammalian meiosis is characterized by the formation of a unique heterochromatin structure at the XY body. The mechanisms underlying the formation of this nuclear domain are reportedly highly conserved from marsupials to mammals. In this study, we demonstrate that in contrast to all eutherian species studied to date, partial synapsis of the heterologous sex chromosomes during pachytene stage in the horse is not associated with the formation of a typical macrochromatin domain at the XY body. While phosphorylated histone H2AX (γH2AX) and macroH2A1.2 are present as a diffuse signal over the entire macrochromatin domain in mouse pachytene spermatocytes, γH2AX, macroH2A1.2, and the cohesin subunit SMC3 are preferentially enriched at meiotic sex chromosome cores in equine spermatocytes. Moreover, although several histone modifications associated with this nuclear domain in the mouse such as H3K4me2 and ubH2A are conspicuously absent in the equine XY body, prominent RNA polymerase II foci persist at the sex chromosomes. Thus, the localization of key marker proteins and histone modifications associated with the XY body in the horse differs significantly from all other mammalian systems described. These results demonstrate that the epigenetic landscape and heterochromatinization of the equine XY body might be regulated by alternative mechanisms and that some features of XY body formation may be evolutionary divergent in the domestic horse. We propose equine spermatogenesis as a unique model system for the study of the regulatory networks leading to the epigenetic control of gene expression during XY body formation.
Publication Date: 2011-01-28 PubMed ID: 21274552PubMed Central: PMC3100478DOI: 10.1007/s00412-010-0306-5Google Scholar: Lookup
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Summary
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The research article delves into the unique structural formation of the XY sex chromosome body during equine (horse) spermatogenesis—the process of sperm cell formation. The unique chromatin structure, histone modifications, and protein localizations observed differ from previously studied mammalian systems, suggesting alternative regulatory mechanisms and evolutionarily divergent characteristics.
Understanding chromatin structures and epigenetic landscapes
- The article focuses on how sex chromosomes are paired during meiosis, a process of cell division that produces gametes or sexual reproduction cells. The emergence of a rare heterochromatin structure on the XY body—a massive nuclear domain—is a focus of this study.
- Typically, the mechanisms steering the formation of this nuclear domain appear to be largely conserved from marsupials to mammals. Conventional belief holds that these processes are generally standardized.
Unique characteristics of equine spermatogenesis
- In a dramatic departure from prior studies of eutherian species, this research shows how the partial synapsis (joining together) of differing sex chromosomes during the pachytene stage in horse spermatogenesis doesn’t lead to the usual macrochromatin domain on the XY body. In other words, horse sex chromosome pairing differs from the norm.
- In horse pachytene spermatocytes, three factors—phosphorylated histone H2AX (γH2AX), macroH2A1.2, and the cohesin subunit SMC3—show a preference for enriching at meiotic sex chromosome cores, rather than diffusing over the macrochromatin domain (as they do in mouse cells).
Significant differences from other mammals
- The research notes the absence in equine XY bodies of certain histone modifications normally associated with this nuclear domain in mice, such as H3K4me2 (a specific modification to chromosomes’ nuclear proteins) and ubH2A.
- However, it also noted that RNA polymerase II foci, responsible for transcribing DNA into mRNA, continue to persist at the sex chromosomes.
- The localization, or arrangement, of crucial marker proteins and histone modifications associated with the equine XY body differ significantly from all other mammals. This implies that horses have somewhat unique systems for managing the formation and function of their sex chromosomes.
Implications of the Study
- This research suggests that certain features of XY body formation may be evolutionary divergent in the domestic horse. It also suggests that the epigenetic landscape and heterochromatinization of the equine XY body might be regulated by alternative mechanisms from those observed in other mammals.
- The uniqueness of equine spermatogenesis, as demonstrated, presents an opportunity for researchers to gain insight into how different species have evolved distinct regulatory networks to control gene expression during XY body formation. Thus, this study proposes the equine spermatogenesis process as an excellent model system for further investigation.
Cite This Article
APA
Baumann C, Daly CM, McDonnell SM, Viveiros MM, De La Fuente R.
(2011).
Chromatin configuration and epigenetic landscape at the sex chromosome bivalent during equine spermatogenesis.
Chromosoma, 120(3), 227-244.
https://doi.org/10.1007/s00412-010-0306-5 Publication
Researcher Affiliations
- Female Germ Cell Biology Group, Department of Clinical Studies, University of Pennsylvania, New Bolton Center, Kennett Square, PA 19348, USA.
MeSH Terms
- Animals
- Chromatin / chemistry
- Chromosomal Proteins, Non-Histone / metabolism
- Chromosome Pairing
- Epigenomics
- Heterochromatin / genetics
- Histones / genetics
- Horses / genetics
- Mice
- Miosis / genetics
- Pachytene Stage / genetics
- Sex Chromosomes / genetics
- Spermatogenesis / genetics
Grant Funding
- R01 HD042740 / NICHD NIH HHS
- R01 HD042740-06 / NICHD NIH HHS
- R56 HD093383 / NICHD NIH HHS
- 2R01HDO42740 / PHS HHS
References
This article includes 60 references
- Akhmedov AT, Gross B, Jessberger R. Mammalian SMC3 C-terminal and coiled-coil protein domains specifically bind palindromic DNA, do not block DNA ends, and prevent DNA bending.. J Biol Chem 1999 Dec 31;274(53):38216-24.
- Anderson SF, Schlegel BP, Nakajima T, Wolpin ES, Parvin JD. BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A.. Nat Genet 1998 Jul;19(3):254-6.
- Baarends WM, Hoogerbrugge JW, Roest HP, Ooms M, Vreeburg J, Hoeijmakers JH, Grootegoed JA. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis.. Dev Biol 1999 Mar 15;207(2):322-33.
- Baarends WM, Wassenaar E, van der Laan R, Hoogerbrugge J, Sleddens-Linkels E, Hoeijmakers JH, de Boer P, Grootegoed JA. Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis.. Mol Cell Biol 2005 Feb;25(3):1041-53.
- Bannister LA, Schimenti JC. Homologous recombinational repair proteins in mouse meiosis.. Cytogenet Genome Res 2004;107(3-4):191-200.
- Burgoyne PS, Mahadevaiah SK, Turner JM. The management of DNA double-strand breaks in mitotic G2, and in mammalian meiosis viewed from a mitotic G2 perspective.. Bioessays 2007 Oct;29(10):974-86.
- Burgoyne PS, Mahadevaiah SK, Turner JM. The consequences of asynapsis for mammalian meiosis.. Nat Rev Genet 2009 Mar;10(3):207-16.
- Chandley AC, Jones RC, Dott HM, Allen WR, Short RV. Meiosis in interspecific equine hybrids. I. The male mule (Equus asinus X E. caballus) and hinny (E. caballus X E. asinus).. Cytogenet Cell Genet 1974;13(4):330-41.
- De La Fuente R, Viveiros MM, Burns KH, Adashi EY, Matzuk MM, Eppig JJ. Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function.. Dev Biol 2004 Nov 15;275(2):447-58.
- De La Fuente R, Baumann C, Fan T, Schmidtmann A, Dobrinski I, Muegge K. Lsh is required for meiotic chromosome synapsis and retrotransposon silencing in female germ cells.. Nat Cell Biol 2006 Dec;8(12):1448-54.
- de la Fuente R, Parra MT, Viera A, Calvente A, Gómez R, Suja JA, Rufas JS, Page J. Meiotic pairing and segregation of achiasmate sex chromosomes in eutherian mammals: the role of SYCP3 protein.. PLoS Genet 2007 Nov;3(11):e198.
- Eijpe M, Heyting C, Gross B, Jessberger R. Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes.. J Cell Sci 2000 Feb;113 ( Pt 4):673-82.
- Escalier D, Garchon HJ. XMR is associated with the asynapsed segments of sex chromosomes in the XY body of mouse primary spermatocytes.. Chromosoma 2000 Jul;109(4):259-65.
- Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, Manova K, Burgoyne P, Nussenzweig A. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis.. Dev Cell 2003 Apr;4(4):497-508.
- Franco MJ, Sciurano RB, Solari AJ. Protein immunolocalization supports the presence of identical mechanisms of XY body formation in eutherians and marsupials.. Chromosome Res 2007;15(6):815-24.
- Froenicke L, Anderson LK, Wienberg J, Ashley T. Male mouse recombination maps for each autosome identified by chromosome painting.. Am J Hum Genet 2002 Dec;71(6):1353-68.
- Handel MA. The XY body: a specialized meiotic chromatin domain.. Exp Cell Res 2004 May 15;296(1):57-63.
- Handel MA, Hunt PA. Sex-chromosome pairing and activity during mammalian meiosis.. Bioessays 1992 Dec;14(12):817-22.
- Hawley RS. The human Y chromosome: rumors of its death have been greatly exaggerated.. Cell 2003 Jun 27;113(7):825-8.
- Hoyer-Fender S. Molecular aspects of XY body formation.. Cytogenet Genome Res 2003;103(3-4):245-55.
- Hoyer-Fender S, Singh PB, Motzkus D. The murine heterochromatin protein M31 is associated with the chromocenter in round spermatids and Is a component of mature spermatozoa.. Exp Cell Res 2000 Jan 10;254(1):72-9.
- Hoyer-Fender S, Czirr E, Radde R, Turner JM, Mahadevaiah SK, Pehrson JR, Burgoyne PS. Localisation of histone macroH2A1.2 to the XY-body is not a response to the presence of asynapsed chromosome axes.. J Cell Sci 2004 Jan 15;117(Pt 2):189-98.
- Jessberger R. The many functions of SMC proteins in chromosome dynamics.. Nat Rev Mol Cell Biol 2002 Oct;3(10):767-78.
- Khalil AM, Driscoll DJ. Histone H3 lysine 4 dimethylation is enriched on the inactive sex chromosomes in male meiosis but absent on the inactive X in female somatic cells.. Cytogenet Genome Res 2006;112(1-2):11-5.
- Khalil AM, Driscoll DJ. Trimethylation of histone H3 lysine 4 is an epigenetic mark at regions escaping mammalian X inactivation.. Epigenetics 2007 Apr-Jun;2(2):114-8.
- Khalil AM, Boyar FZ, Driscoll DJ. Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis.. Proc Natl Acad Sci U S A 2004 Nov 23;101(47):16583-7.
- Losada A, Hirano T. Dynamic molecular linkers of the genome: the first decade of SMC proteins.. Genes Dev 2005 Jun 1;19(11):1269-87.
- Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-Rodríguez J, Jasin M, Keeney S, Bonner WM, Burgoyne PS. Recombinational DNA double-strand breaks in mice precede synapsis.. Nat Genet 2001 Mar;27(3):271-6.
- Manders EEM, Verbeek FJ, Aten JA. Measurement of colocalisation of objects in dual-colour confocal images. J Microsc 1993;169:375–382.
- Monesi V. Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse.. Chromosoma 1965;17(1):11-21.
- Namekawa SH, Lee JT. XY and ZW: is meiotic sex chromosome inactivation the rule in evolution?. PLoS Genet 2009 May;5(5):e1000493.
- Namekawa SH, VandeBerg JL, McCarrey JR, Lee JT. Sex chromosome silencing in the marsupial male germ line.. Proc Natl Acad Sci U S A 2007 Jun 5;104(23):9730-5.
- Page J, Berríos S, Rufas JS, Parra MT, Suja JA, Heyting C, Fernández-Donoso R. The pairing of X and Y chromosomes during meiotic prophase in the marsupial species Thylamys elegans is maintained by a dense plate developed from their axial elements.. J Cell Sci 2003 Feb 1;116(Pt 3):551-60.
- Page J, de la Fuente R, Gómez R, Calvente A, Viera A, Parra MT, Santos JL, Berríos S, Fernández-Donoso R, Suja JA, Rufas JS. Sex chromosomes, synapsis, and cohesins: a complex affair.. Chromosoma 2006 Jun;115(3):250-9.
- Pelttari J, Hoja MR, Yuan L, Liu JG, Brundell E, Moens P, Santucci-Darmanin S, Jessberger R, Barbero JL, Heyting C, Höög C. A meiotic chromosomal core consisting of cohesin complex proteins recruits DNA recombination proteins and promotes synapsis in the absence of an axial element in mammalian meiotic cells.. Mol Cell Biol 2001 Aug;21(16):5667-77.
- Perry J, Palmer S, Gabriel A, Ashworth A. A short pseudoautosomal region in laboratory mice.. Genome Res 2001 Nov;11(11):1826-32.
- 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.
- Power MM, Gustavsson I, Switoński M, Plöen L. Synaptonemal complex analysis of an autosomal trisomy in the horse.. Cytogenet Cell Genet 1992;61(3):202-7.
- Prieto I, Tease C, Pezzi N, Buesa JM, Ortega S, Kremer L, Martínez A, Martínez-A C, Hultén MA, Barbero JL. Cohesin component dynamics during meiotic prophase I in mammalian oocytes.. Chromosome Res 2004;12(3):197-213.
- Revenkova E, Jessberger R. Shaping meiotic prophase chromosomes: cohesins and synaptonemal complex proteins.. Chromosoma 2006 Jun;115(3):235-40.
- Richler C, Ast G, Goitein R, Wahrman J, Sperling R, Sperling J. Splicing components are excluded from the transcriptionally inactive XY body in male meiotic nuclei.. Mol Biol Cell 1994 Dec;5(12):1341-52.
- Scherthan H. A bouquet makes ends meet.. Nat Rev Mol Cell Biol 2001 Aug;2(8):621-7.
- Schoenmakers S, Wassenaar E, Hoogerbrugge JW, Laven JS, Grootegoed JA, Baarends WM. Female meiotic sex chromosome inactivation in chicken.. PLoS Genet 2009 May;5(5):e1000466.
- Sciurano R, Rahn M, Rey-Valzacchi G, Solari AJ. The asynaptic chromatin in spermatocytes of translocation carriers contains the histone variant gamma-H2AX and associates with the XY body.. Hum Reprod 2007 Jan;22(1):142-50.
- Scott IS, Long SE. An examination of chromosomes in the stallion (Equus caballus) during meiosis.. Cytogenet Cell Genet 1980;26(1):7-13.
- Solari AJ. The behaviour of chromosomal axes during diplotene in mouse spermatocytes.. Chromosoma 1970;31(2):217-30.
- Solari AJ. The spatial relationship of the X and Y chromosomes during meiotic prophase in mouse spermatocytes.. Chromosoma 1970;29(2):217-36.
- Tres LL. Extensive pairing of the XY bivalent in mouse spermatocytes as visualized by whole-mount electron microscopy.. J Cell Sci 1977 Jun;25:1-15.
- Turner JM. Meiotic sex chromosome inactivation.. Development 2007 May;134(10):1823-31.
- Turner JM, Aprelikova O, Xu X, Wang R, Kim S, Chandramouli GV, Barrett JC, Burgoyne PS, Deng CX. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation.. Curr Biol 2004 Dec 14;14(23):2135-42.
- Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng CX, Burgoyne PS. Silencing of unsynapsed meiotic chromosomes in the mouse.. Nat Genet 2005 Jan;37(1):41-7.
- Turner JM, Mahadevaiah SK, Ellis PJ, Mitchell MJ, Burgoyne PS. Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids.. Dev Cell 2006 Apr;10(4):521-9.
- van der Heijden GW, Derijck AA, Pósfai E, Giele M, Pelczar P, Ramos L, Wansink DG, van der Vlag J, Peters AH, de Boer P. Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation.. Nat Genet 2007 Feb;39(2):251-8.
- 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.
- White GE, Erickson HP. Sequence divergence of coiled coils--structural rods, myosin filament packing, and the extraordinary conservation of cohesins.. J Struct Biol 2006 May;154(2):111-21.
- Wichman HA, Payne CT, Ryder OA, Hamilton MJ, Maltbie M, Baker RJ. Genomic distribution of heterochromatic sequences in equids: implications to rapid chromosomal evolution.. J Hered 1991 Sep-Oct;82(5):369-77.
- Xu X, Aprelikova O, Moens P, Deng CX, Furth PA. Impaired meiotic DNA-damage repair and lack of crossing-over during spermatogenesis in BRCA1 full-length isoform deficient mice.. Development 2003 May;130(9):2001-12.
- Zickler D. From early homologue recognition to synaptonemal complex formation.. Chromosoma 2006 Jun;115(3):158-74.
- Zinchuk V, Zinchuk O. Quantitative colocalization analysis of confocal fluorescence microscopy images. Curr Protoc Cell Biol 2008;39:4.19.1–4.19.16.
- Zinchuk V, Zinchuk O, Okada T. Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena.. Acta Histochem Cytochem 2007 Aug 30;40(4):101-11.
Citations
This article has been cited 11 times.- Cruz A, Sullivan DB, Doty KF, Hess RA, Canisso IF, Reddi PP. Acrosomal marker SP-10 (gene name Acrv1) for staging of the cycle of seminiferous epithelium in the stallion. Theriogenology 2020 Oct 15;156:214-221.
- Spangenberg V, Arakelyan M, Cioffi MB, Liehr T, Al-Rikabi A, Martynova E, Danielyan F, Stepanyan I, Galoyan E, Kolomiets O. Cytogenetic mechanisms of unisexuality in rock lizards. Sci Rep 2020 May 26;10(1):8697.
- Matveevsky SN, Pavlova SV, Atsaeva MM, Searle JB, Kolomiets OL. Dual mechanism of chromatin remodeling in the common shrew sex trivalent (XY (1)Y (2)). Comp Cytogenet 2017;11(4):727-745.
- Casey AE, Daish TJ, Barbero JL, Grützner F. Differential cohesin loading marks paired and unpaired regions of platypus sex chromosomes at prophase I. Sci Rep 2017 Jun 26;7(1):4217.
- El Zowalaty AE, Baumann C, Li R, Chen W, De La Fuente R, Ye X. Seipin deficiency increases chromocenter fragmentation and disrupts acrosome formation leading to male infertility. Cell Death Dis 2015 Jul 16;6(7):e1817.
- Biswas U, Wetzker C, Lange J, Christodoulou EG, Seifert M, Beyer A, Jessberger R. Meiotic cohesin SMC1β provides prophase I centromeric cohesion and is required for multiple synapsis-associated functions. PLoS Genet 2013;9(12):e1003985.
- Rich T, Henderson LB, Becker DL, Cornell H, Patterson-Kane JC. Indicators of replicative damage in equine tendon fibroblast monolayers. BMC Vet Res 2013 Sep 11;9:180.
- Fayrer-Hosken R, Stanley A, Hill N, Heusner G, Christian M, De La Fuente R, Baumann C, Jones L. Effect of feeding fescue seed containing ergot alkaloid toxins on stallion spermatogenesis and sperm cells. Reprod Domest Anim 2012 Dec;47(6):1017-26.
- Ichijima Y, Sin HS, Namekawa SH. Sex chromosome inactivation in germ cells: emerging roles of DNA damage response pathways. Cell Mol Life Sci 2012 Aug;69(15):2559-72.
- Sciurano RB, Rahn MI, Rossi L, Luaces JP, Merani MS, Solari AJ. Synapsis, recombination, and chromatin remodeling in the XY body of armadillos. Chromosome Res 2012 Feb;20(2):293-302.
- Golbabapour S, Abdulla MA, Hajrezaei M. A concise review on epigenetic regulation: insight into molecular mechanisms. Int J Mol Sci 2011;12(12):8661-94.
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