Nucleolus-like body of mouse oocytes contains lamin A and B and TRF2 but not actin and topo II
Tóm tắt
During the final stages of oocyte development, all chromosomes join in a limited nuclear volume for the final formation of a single complex chromatin structure – the karyosphere. In the majority of mammalian species, the chromosomes surround a round protein/fibrillar body known as the central body, or nucleolus-like body (NLB). Nothing seems to unite the inner portion of the karyosphere with the nucleolus except position at its remnants. Nevertheless, in this study we will use term NLB as the conventional one for karyosphere with the central body. At the morphological level, NLBs consist of tightly-packed fibres of 6–10 nm. The biochemical structure of this dense, compact NLB fibre centre remains uncertain. The aim of this study was to determine which proteins represent the NLB components at final stages of karyosphere formation in mouse oogenesis. To determine this, three antibodies (ABs) have been examined against different actin epitopes. Examination of both ABs against the actin N-end provided similar results: spots inside the nucleus. Double staining with AB against SC35 and actin revealed the colocalization of these proteins in IGCs (interchromatin granule clusters/nuclear speckles/SC35 domains). In contrast, examination of polyclonal AB against peptide at the C-end reveals a different result: actin is localized exclusively in connection with the chromatin. Surprisingly, no forms of actin or topoisomerase II are present as components of the NLB. It was discovered that: (1) lamin B is an NLB component from the beginning of NLB formation, and a major portion of it resides in the NLB at the end of oocyte development; (2) lamin A undergoes rapid movement into the NLB, and a majority of it remains in the NLB; (3) the telomere-binding protein TRF2 resides in the IGCs/nuclear speckles until the end of oocyte development, when significant part of it transfers to the NLB. NLBs do not contain actin or topo II. Lamin B is involved from the beginning of NLB formation. Both Lamin A and TRF2 exhibit rapid movement to the NLB at the end of oogenesis. This dynamic distribution of proteins may reflect the NLB’s role in future chromatin organization post-fertilisation.
Tài liệu tham khảo
De La Fuente R. Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol. 2006;292:1–12.
Blackman MW. The spermatogenesis of the Myriapods. I. Notes on the spermatocytes and spermatids of Scolopendra. Kansas Univ Quart. 1901;10:61–76.
Bogolyubova IO, Bogolyubov DS. Oocyte nuclear structure during mammalian oogenesis. In: Perrotte A, editor. Recent Adv Germ Cells Research. New York: Nova Science Publishers, Inc.; 2013. p. 105–33.
Parfenov V, Potchukalina G, Dudina L, Kostyuchek D, Gruzova M. Human antral follicles: oocyte nucleus and the karyosphere formation (electron microscopic and autoradiographic data). Gamete Res. 1989;22:219–31.
Gruzova MN, Parfenov VN. Karyosphere in oogenesis and intranuclear morphogenesis. Int Rev Cytol. 1993;144:1–52.
Gruzova MN, Parfenov VN. Ultrastructure of late oocyte nuclei in Rana temporaria. J Cell Sci. 1977;28:1–13.
Mattson BA, Albertini DF. Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol Reprod Dev. 1990;25:374–83.
Zybina EV, Zybina TG. Changes in the arrangement of chromosomes and nucleoli related to functional peculiarities of developing mammalian oocytes during meiotic prophase. Tsitologiia. 1992;34:3–23.
Pochukalina GN, Parfenov VN. Nucleolus transformation in mouse antral follicles: Distribution of coilin and components of RNA-polymerase I complex. Cell Tissue Biol. 2008;2:522–30.
Zybina EV, Grishchenko TA, Semenov VM. Ultrastructure of the fibrillar center in oocyte nucleoli at the diplonema stage in the golden hamster. Tsitologiia. 1984;26:1246–9.
Tan JH, Wang HL, Sun XS, Liu Y, Sui HS, Zhang J. Chromatin configurations in the germinal vesicle of mammalian oocytes. Mol Hum Reprod. 2009;15:1–9.
Luciano AM, Franciosi F, Dieci C, Tessaro I, Terzaghi L, Modina SC, et al. Large-scale chromatin structure and function changes during oogenesis : the interplay between oocyte and companion cumulus cells. Anim Reprod. 2014;11:141–9.
Antoine N, Lepoint A, Baeckeland E, Goessens G. Ultrastructural cytochemistry of the nucleolus in rat oocytes at the end of the folliculogenesis. Histochemistry. 1988;89:221–6.
Fulka H, Langerova A. The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte to embryo transition. Development. 2014;141:1694–704.
Shishova KV, Lavrentyeva EA, Dobrucki JW, Zatsepina OV. Nucleolus-like bodies of fully-grown mouse oocytes contain key nucleolar proteins but are impoverished for rRNA. Dev Biol. 2015;397(2):267–81.
Burns KH, Viveiros MM, Ren Y, Wang P, DeMayo FJ, Frail DE, et al. Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science. 2003;300(5619):633–6.
Swiatek P. Formation of the karyosome in developing oocytes of weevils (Coleoptera, Curculionidae). Tissue Cell. 1999;31:587–93.
Rübsam R, Büning J. F-actin is a component of the karyosome in neuropteran oocyte nuclei. Arthropod Struct Dev. 2001;30:125–33.
Bogolyubov DS, Batalova FM, Kiselyov AM, Stepanova IS. Nuclear structures in Tribolium castaneum oocytes. Cell Biol Int. 2013;37:1061–79.
Parfenov VN, Davis DS, Pochukalina GN, Sample CE, Bugaeva EA, Murti KG. Nuclear actin filaments and their topological changes in frog oocytes. Exp Cell Res. 1995;217:385–94.
Kiseleva E, Drummond SP, Goldberg MW, Rutherford SA, Allen TD, Wilson KL. Actin- and protein-4.1-containing filaments link nuclear pore complexes to subnuclear organelles in Xenopus oocyte nuclei. J Cell Sci. 2004;117:2481–90.
Maslova A, Krasikova A. Nuclear actin depolymerization in transcriptionally active avian and amphibian oocytes leads to collapse of intranuclear structures. Nucleus. 2012;3:300–11.
Pochukalina GN, Bogolyubov DS, Parfenov VN. Interchromatin Granule Clusters of Mouse Preovulatory Oocytes: Organization Molecular Composition, and Possible Functions Cell and Tissue Biology. Cell Tissue Biol. 2010;4:167–76.
Bogolyubov D, Stepanova I, Parfenov V. Universal nuclear domains of somatic and germ cells: some lessons from oocyte interchromatin granule cluster and Cajal body structure and molecular composition. Bioessays. 2009;31:400–9.
Spector DL, Lamond AI. Nuclear Speckles. Cold Spring Harb Perspect Biol. 2011;3:a000646.
Misteli T, Spector DL. The cellular organization of gene expression. Curr Opin Cell Biol. 1998;10:323–31.
Dundr M, Misteli T. Functional architecture in the cell nucleus. Biochem J. 2001;356:297–310.
Earnshaw WC, Halligan B, Cooke CA, Heck MM, Liu LF. Topoisomerase II is a structural component of mitotic chromosome scaffolds. J Cell Biol. 1985;100:1706–15.
Gasser SM. Laroche T, Falquet J, Boy de la Tour E, Laemmli UK. Metaphase chromosome structure. Involvement of topoisomerase II. J Mol Biol. 1986;188:613–29.
Schoeffler AJ, Berger JM. DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q Rev Biophys. 2008;41:41–101.
Maeshima K, Laemmli UK. A two-step scaffolding model for mitotic chromosome assembly. Dev Cell. 2003;4:467–80.
Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, et al. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 2008;22:832–53.
Adam SA, Goldman RD. Insights into the Differences between the A- and B-Type Nuclear Lamins. Adv Biol Regul. 2012;52:108–13.
Shimi T, Pfleghaar K, Kojima S, Pack CG, Solovei I, Goldman AE, et al. The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev. 2008;22:3409–21.
Goldberg MW, Huttenlauch I, Hutchison CJ, Stick R. Filaments made from A- and B-type lamins differ in structure and organization. J Cell Sci. 2008;121:215–25.
Nickerson J. Experimental observations of a nuclear matrix. J Cell Sci. 2001;114:463–74.
Berezney R, Mortillaro MJ, Ma H, Wei X, Samarabandu J. The nuclear matrix: a structural milieu for genomic function. Int Rev Cytol. 1995;162A:1–65.
Malyavantham KS, Bhattacharya S, Barbeitos M, Mukherjee L, Xu J, Fackelmayer FO, et al. Identifying functional neighborhoods within the cell nucleus: proximity analysis of early S-phase replicating chromatin domains to sites of transcription, RNA polymerase II, HP1gamma, matrin 3 and SAF-A. J Cell Biochem. 2008;105:391–403.
Podgornaya OI, Voronin AP, Enukashvily NI, Matveev IV, Lobov IB. Structure-specific DNA-binding proteins as the foundation for three-dimensional chromatin organization. Int Rev Cytol. 2003;224:227–96.
Bugaeva EA, Podgornaya OI. Telomere-binding protein from the nuclear envelope of oocytes of the frog Rana temporaria. Biochemistry (Mosc). 1997;62:1311–22.
Lima-de-Faria A. Molecular evolution and organization of chromosomes. New York: Elsevier Science Press; 1983.
Dernburg AF, Sedat JW, Cande WZ, Bass HW. Cytology of Telomeres. In: Telomeres, vol. 29. New York: Cold Spring Harbor Laboratory Press; 1995. p. 295–338.
Podgornaya OI, Bugaeva EA, Voronin AP, Gilson E, Mitchell AR. Nuclear envelope associated protein that binds telomeric DNAs. Mol Reprod Dev. 2000;57:16–25.
Voronin AP, Lobov IB, Gilson E, Podgornaya OI. A telomere-binding protein (TRF2/MTBP) from mouse nuclear matrix with motives of an intermediate filament-type rod domain. J Anti Aging Med. 2003;6:205–18.
Chong L, van Steensel B, Broccoli D, Erdjument-Bromage H, Hanish J, Tempst P, et al. A human telomeric protein. Science. 1995;270:1663–7.
Broccoli D, Chong L, Oelmann S, Fernald AA, Marziliano N, van Steensel B, et al. Comparison of the human and mouse genes encoding the telomeric protein, TRF1: chromosomal localization, expression and conserved protein domains. Hum Mol Genet. 1997;6:69–76.
Bilaud T, Koering CE, Binet-Brasselet E, Ancelin K, Pollice A, Gasser SM, et al. The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res. 1996;24:1294–303.
Bilaud T, Brun C, Ancelin K, Koering CE, Laroche T, Gilson E. Telomeric localization of TRF2, a novel human telobox protein. Nat Genet. 1997;17:236–9.
Palm W, de Lange T. How shelterin protects mammalian telomeres. Annu Rev Genet. 2008;42:301–34.
Van Steensel B, Smogorzewska A, de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell. 1998;92:401–13.
Muñoz P, Blanco R, Blasco MA. Role of the TRF2 telomeric protein in cancer and ageing. Cell Cycle. 2006;5:718–21.
Glass JR, Gerace L. Lamins A and C bind and assemble at the surface of mitotic chromosomes. J Cell Biol. 1990;111:1047–57.
Lessard JL. Two monoclonal antibodies to actin: one muscle selective and one generally reactive. Cell Motil Cytoskeleton. 1988;10:349–62.
Cmarko D, Verschure PJ, Martin TE, Dahmus ME, Krause S, Fu X-D, et al. Ultrastructural Analysis of Transcription and Splicing in the Cell Nucleus after Bromo-UTP Microinjection. Mol Biol Cell. 1999;10:211–23.
Belgrader P, Siegel AJ, Berezney R. A comprehensive study on the isolation and characterisation of the HeLa S3 nuclear matrix. J Cell Sci. 1991;98:281–91.
Lobov IB, Tsutsui K, Mitchell AR, Podgornaya OI. Specific interaction of mouse major satellite with MAR-binding protein SAF-A. Eur J Cell Biol. 2000;79:839–49.
Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–5.
Pochukalina GN, Parfenov VN. Nucleolus in multilayer follicles oocytes of mouse (fibrillarin and RNA polymerase I topography, their association with coilin). Tsitologiia. 2006;8:674–83.
Ilicheva NV, Podgornaya OI, Voronin AP. Telomere repeat factor 2 (TRF2) is responsible for the telomere attachment to the nuclear membrane. Adv Prot Chem Struct Biol. 2015;101:67–96.
Enukashvily N, Donev R, Sheer D, Podgornaya O. Satellite DNA binding and cellular localisation of RNA helicase P68. J Cell Sci. 2005;118:611–22.
Zatsepina OV, Zharskaya OO, Prusov AN. Isolation of the constitutive heterochromatin from mouse liver nuclei. Methods Mol Biol. 2008;463:169–80.
Berchtold D, Fesser S, Bachmann G, Kaiser A, Eilert JC, Frohns F, et al. Nuclei of chicken neurons in tissues and three-dimensional cell cultures are organized into distinct radial zones. Chromosome Res. 2011;19:165–82.
Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell. 2013;152:584–98.
Dolnik AV, Kuznetsova IS, Voronin AP, Podgornaya OI. Telomere-binding TRF2/MTBP localization during mouse spermatogenesis and cell cycle of the mouse cells L929. J Anti Aging Med. 2003;6:107–21.
Dolnik AV, Pochukalina GN, Parfenov VN, Karpushev AV, Podgornaya OI, Voronin AP. Dynamics of satellite binding protein CENP-B and telomere binding protein TRF2/MTBP in the nuclei of mouse spermatogenic line. Cell Biol Int. 2007;31:316–29.
Kuznetsova IS, Voronin AP, Podgornaya OI. Telomere and TRF2/MTBP localization in respect to satellite DNA during the cell cycle of mouse cell line L929. Rejuvenation Res. 2006;9:391–401.
Bouniol-Baly C, Hamraoui L, Guibert J, Beaujean N, Szöllösi MS, Debey P. Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biol Reprod. 1999;3:580–7.
Bonnet-Garnier A, Feuerstein P, Chebrout M, Fleurot R, Jan HU, Debey P, et al. Genome organization and epigenetic marks in mouse germinal vesicle oocytes. Int J Dev Biol. 2012;56:877–87.
Belin BJ, Cimini BA, Blackburn EH, Mullins RD. Visualization of actin filaments and monomers in somatic cell nuclei. Mol Biol Cell. 2013;24:982–94.
Weston L, Coutts AS, La Thangue NB. Actin nucleators in the nucleus: an emerging theme. J Cell Sci. 2012;125:3519–27.
Vagnarelli P. Chromatin reorganization through mitosis. Adv Protein Chem Struct Biol. 2013;90:179–224.
Constantinescu D, Gray HL, Sammak PJ, Schatten GP, Csoka AB. Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells. 2006;24:177–85.
Kiselev A, Stepanova I, Adonin L, Batalova F, Parfenov V, Bogolyubov D, et al. Characterization of Tibolium castaneum oocyte nuclear structures using microinjection of a fusion nuclear porotein mRNA. Mol Repod & Dev. 2015;82:628–9.
Bartholomew B. Monomeric actin required for INO80 remodeling. Nat Stuct Mol Biol. 2013;20:405–7.
Safer D, Golla R, Nachmias VT. Isolation of a 5-kilodalton actin-sequestering peptide from human blood platelets. Proc Natl Acad Sci U S A. 1990;87:2536–40.
Shlüter K, Jockusch BM, Rothkegel M. Profilins as regulators of actin dynamics. Biochim Biophys Acta. 1997;1359:97–109.
Pochukalina GN, Parfenov VN. Localization of actin and mRNA export factors in the nucleus of murine preovulatory oocytes. Cell Tissue Biol. 2012;6:423–34.
Kapoor P, Chen M, Winkler DD, Luger K, Shen X. Evidence for monomeric actin function in INO80 chromatin remodeling. Nat Struct Mol Biol. 2013;20:426–32.
Bogolyubova I, Stein G, Bogolyubov D. FRET analysis of interactions between actin and exon-exon-junction complex proteins in early mouse embryos. Cell Tissue Biol. 2013;7:37–42.
Bogolyubova IO, Parfenov VN. Immunofluorescence detection of nuclear actin in early mouse embryos. Cell Tissue Biol. 2012;6:458–64.
Mazumdar M, Sundareshan S, Misteli T. Human chromokinesin KIF4A functions in chromosome condensation and segregation. J Cell Biol. 2004;166:613–20.
Samejima K, Samejima I, Vagnarelli P, Ogawa H, Vargiu G, Kelly DA, et al. Mitotic chromosomes are compacted laterally by KIF4 and condensin and axially by topoisomerase IIα. J Cell Biol. 2012;199:755–70.
Tavormina PA, Côme MG, Hudson JR, Mo YY, Beck WT, Gorbsky GJ. Rapid exchange of mammalian topoisomerase II alpha at kinetochores and chromosome arms in mitosis. J Cell Biol. 2002;158:23–9.
Taniguchi K, Wakabayashi T, Yoshida T, Mizuno M, Yoshikawa K, Kikuchi A, et al. Immunohistochemical staining of DNA topoisomerase IIalpha in human gliomas. J Neurosurg. 1999;91:477–82.
Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature. 2008;453:948–51.
Comings DE. Arrangement of chromatin in the nucleus. Hum Genet. 1980;53:131–43.
De Vos WH, Houben F, Hoebe RA, Hennekam R, van Engelen B, Manders EM, et al. Increased plasticity of the nuclear envelope and hypermobility of telomeres due to the loss of A-type lamins. Biochim Biophys Acta. 1800;2010:448–58.
Wood AM, Rendtlew Danielsen JM, Lucas CA, Rice EL, Scalzo D, et al. TRF2 and lamin A/C interact to facilitate the functional organization of chromosome ends. Nat Commun. 2014;5:5467.
Andrés V, González JM. Role of A-type lamins in signaling, transcription, and chromatin organization. J Cell Biol. 2009;187:945–57.
Decker ML, Chavez E, Vulto I, Lansdorp PM. Telomere length in Hutchinson-Gilford progeria syndrome. Mech Ageing Dev. 2009;130:377–83.
Gonzalez-Suarez I, Redwood AB, Perkins SM, Vermolen B, Lichtensztejin D, Grotsky DA, et al. Novel roles for A-type lamins in telomere biology and the DNA damage response pathway. EMBO J. 2009;28:2414–27.
Kyogoku H, Fulka Jr J, Wakayama T, Miyano T. De novo formation of nucleoli in developing mouse embryos originating from enucleolated zygotes. Development. 2014;141:2255–9.
