Nucleus reprogramming/remodeling through selective enucleation (SE) of immature oocytes and zygotes: a nucleolus point of view
Jazyk angličtina Země Japonsko Médium print-electronic
Typ dokumentu časopisecké články
PubMed
35431279
PubMed Central
PMC9184824
DOI
10.1262/jrd.2022-004
Knihovny.cz E-zdroje
- Klíčová slova
- Nucleus, Remodeling, Reprogramming, Selective enucleation,
- MeSH
- buněčné jádro metabolismus MeSH
- chromatin metabolismus MeSH
- oocyty MeSH
- ovce genetika MeSH
- savci genetika MeSH
- techniky jaderného přenosu * veterinární MeSH
- zvířata MeSH
- zygota * metabolismus MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- chromatin MeSH
It is now approximately 25 years since the sheep Dolly, the first cloned mammal where the somatic cell nucleus from an adult donor was used for transfer, was born. So far, somatic cell nucleus transfer, where G1-phase nuclei are transferred into cytoplasts obtained by enucleation of mature metaphase II (MII) oocytes followed by the activation of the reconstructed cells, is the most efficient approach to reprogram/remodel the differentiated nucleus. In general, in an enucleated oocyte (cytoplast), the nuclear envelope (NE, membrane) of an injected somatic cell nucleus breaks down and chromosomes condense. This condensation phase is followed, after subsequent activation, by chromatin decondensation and formation of a pseudo-pronucleus (i) whose morphology should resemble the natural postfertilization pronuclei (PNs). Thus, the volume of the transferred nuclei increases considerably by incorporating the content released from the germinal vesicles (GVs). In parallel, the transferred nucleus genes must be reset and function similarly as the relevant genes in normal embryo reprogramming. This, among others, covers the relevant epigenetic modifications and the appropriate organization of chromatin in pseudo-pronuclei. While reprogramming in SCNT is often discussed, the remodeling of transferred nuclei is much less studied, particularly in the context of the developmental potential of SCNT embryos. It is now evident that correct reprogramming mirrors appropriate remodeling. At the same time, it is widely accepted that the process of rebuilding the nucleus following SCNT is instrumental to the overall success of this procedure. Thus, in our contribution, we will mostly focus on the remodeling of transferred nuclei. In particular, we discuss the oocyte organelles that are essential for the development of SCNT embryos.
Faculty of Natural Sciences Constantine the Philosopher University in Nitra Slovak Republic
Faculty of Veterinary Medicine University of Teramo Teramo Italy
Institute of Animal Science Prague Czech Republic
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Matoba S, Zhang Y. Somatic cell nuclear transfer reprogramming: Mechanisms and applications. Cell Stem Cell 2018; 23: 471–485. PubMed PMC
Ogura A, Matoba S, Inoue K. 25th ANNIVERSARY OF CLONING BY SOMATIC-CELL NUCLEAR TRANSFER: Epigenetic abnormalities associated with somatic cell nuclear transfer. Reproduction 2021; 162: F45–F58. PubMed
Atamna H, Cheung I, Ames BN. A method for detecting abasic sites in living cells: age-dependent changes in base excision repair. Proc Natl Acad Sci USA 2000; 97: 686–691. PubMed PMC
Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993; 362: 709–715. PubMed
Dechat T, Adam SA, Taimen P, Shimi T, Goldman RD. Nuclear lamins. Cold Spring Harb Perspect Biol 2010; 2: a000547. PubMed PMC
Gonzalo S. DNA damage and lamins. Adv Exp Med Biol 2014; 773: 377–399. PubMed PMC
Gurdon JB, Melton DA. Nuclear reprogramming in cells. Science 2008; 322: 1811–1815. PubMed
Halley-Stott RP, Pasque V, Gurdon JB. Nuclear reprogramming. Development 2013; 140: 2468–2471. PubMed
Halley-Stott RP, Pasque V, Astrand C, Miyamoto K, Simeoni I, Jullien J, Gurdon JB. Mammalian nuclear transplantation to Germinal Vesicle stage Xenopus oocytes - a method for quantitative transcriptional reprogramming. Methods 2010; 51: 56–65. PubMed PMC
Tada M, Takahama Y, Abe K, Nakatsuji N, Tada T. Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Curr Biol 2001; 11: 1553–1558. PubMed
Brown KE, Fisher AG. Reprogramming lineage identity through cell-cell fusion. Curr Opin Genet Dev 2021; 70: 15–23. PubMed
Collas P, Taranger CK. Epigenetic reprogramming of nuclei using cell extracts. Stem Cell Rev 2006; 2: 309–317. PubMed
Hu J, Zhao Q, Feng Y, Li N, Gu Y, Sun R, Duan L, Wu Y, Shan Z, Lei L. Embryonic germ cell extracts erase imprinted genes and improve the efficiency of induced pluripotent stem cells. Sci Rep 2018; 8: 10955. PubMed PMC
Liu G, David BT, Trawczynski M, Fessler RG. Advances in pluripotent stem cells: History, mechanisms, technologies, and applications. Stem Cell Rev Rep 2020; 16: 3–32. PubMed PMC
Shi Y, Inoue H, Wu JC, Yamanaka S. Induced pluripotent stem cell technology: a decade of progress. Nat Rev Drug Discov 2017; 16: 115–130. PubMed PMC
Egli D, Rosains J, Birkhoff G, Eggan K. Developmental reprogramming after chromosome transfer into mitotic mouse zygotes. Nature 2007; 447: 679–685. PubMed
Kang E, Wu G, Ma H, Li Y, Tippner-Hedges R, Tachibana M, Sparman M, Wolf DP, Schöler HR, Mitalipov S. Nuclear reprogramming by interphase cytoplasm of two-cell mouse embryos. Nature 2014; 509: 101–104. PubMed PMC
Hyttel P. Electron microscopy of mammalian oocyte development, maturation and fertilization. In: Tosti E, Boni R (eds.), Oocyte Maturation and Fertilization: A Long History for a Short Event. Bussum: Bentham Science Publishers Ltd; 2011: 1–37.
Boisvert FM, van Koningsbruggen S, Navascués J, Lamond AI. The multifunctional nucleolus. Nat Rev Mol Cell Biol 2007; 8: 574–585. PubMed
Fulka H, Langerova A. The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte to embryo transition. Development 2014; 141: 1694–1704. PubMed
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: 267–281. PubMed
Inoue A, Aoki F. Role of the nucleoplasmin 2 C-terminal domain in the formation of nucleolus-like bodies in mouse oocytes. FASEB J 2010; 24: 485–494. PubMed
Ogushi S, Yamagata K, Obuse C, Furuta K, Wakayama T, Matzuk MM, Saitou M. Reconstitution of the oocyte nucleolus in mice through a single nucleolar protein, NPM2. J Cell Sci 2017; 130: 2416–2429. PubMed PMC
Fulka H, Aoki F. Nucleolus precursor bodies and ribosome biogenesis in early Mammalian Embryos: Old theories and new discoveries. Biol Reprod 2016; 94: 143. PubMed
Schatten G, Maul GG, Schatten H, Chaly N, Simerly C, Balczon R, Brown DL. Nuclear lamins and peripheral nuclear antigens during fertilization and embryogenesis in mice and sea urchins. Proc Natl Acad Sci USA 1985; 82: 4727–4731. PubMed PMC
Koncicka M, Cervenka J, Jahn D, Sucha R, Vodicka P, Gad A, Alsheimer M, Susor A. Expression of lamin C2 in mammalian oocytes. PLoS One 2020; 15: e0229781. PubMed PMC
Link J, Jahn D, Schmitt J, Göb E, Baar J, Ortega S, Benavente R, Alsheimer M. The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse. PLoS Genet 2013; 9: e1003261. PubMed PMC
Susor A, Jansova D, Anger M, Kubelka M. Translation in the mammalian oocyte in space and time. Cell Tissue Res 2016; 363: 69–84. PubMed
Ogushi S, Fulka J, Jr, Miyano T. Germinal vesicle materials are requisite for male pronucleus formation but not for change in the activities of CDK1 and MAP kinase during maturation and fertilization of pig oocytes. Dev Biol 2005; 286: 287–298. PubMed
Fulka H, Novakova Z, Mosko T, Fulka J, Jr. The inability of fully grown germinal vesicle stage oocyte cytoplasm to transcriptionally silence transferred transcribing nuclei. Histochem Cell Biol 2009; 132: 457–468. PubMed
Zatsepina O, Baly C, Chebrout M, Debey P. The step-wise assembly of a functional nucleolus in preimplantation mouse embryos involves the cajal (coiled) body. Dev Biol 2003; 253: 66–83. PubMed
Ogushi S, Palmieri C, Fulka H, Saitou M, Miyano T, Fulka J, Jr. The maternal nucleolus is essential for early embryonic development in mammals. Science 2008; 319: 613–616. PubMed
Aguirre-Lavin T, Adenot P, Bonnet-Garnier A, Lehmann G, Fleurot R, Boulesteix C, Debey P, Beaujean N. 3D-FISH analysis of embryonic nuclei in mouse highlights several abrupt changes of nuclear organization during preimplantation development. BMC Dev Biol 2012; 12: 30. PubMed PMC
Bouniol-Baly C, Nguyen E, Besombes D, Debey P. Dynamic organization of DNA replication in one-cell mouse embryos: relationship to transcriptional activation. Exp Cell Res 1997; 236: 201–211. PubMed
Aoki E, Schultz RM. DNA replication in the 1-cell mouse embryo: stimulatory effect of histone acetylation. Zygote 1999; 7: 165–172. PubMed
Yamauchi Y, Ward MA, Ward WS. Asynchronous DNA replication and origin licensing in the mouse one-cell embryo. J Cell Biochem 2009; 107: 214–223. PubMed PMC
Houliston E, Guilly MN, Courvalin JC, Maro B. Expression of nuclear lamins during mouse preimplantation development. Development 1988; 102: 271–278. PubMed
Moreira PN, Robl JM, Collas P. Architectural defects in pronuclei of mouse nuclear transplant embryos. J Cell Sci 2003; 116: 3713–3720. PubMed
Liu W, Yin J, Kou X, Jiang Y, Gao H, Zhao Y, Huang B, He W, Wang H, Han Z, Gao S. Asymmetric reprogramming capacity of parental pronuclei in mouse zygotes. Cell Reports 2014; 6: 1008–1016. PubMed
Bui HT, Wakayama S, Mizutani E, Park KK, Kim JH, Van Thuan N, Wakayama T. Essential role of paternal chromatin in the regulation of transcriptional activity during mouse preimplantation development. Reproduction 2011; 141: 67–77. PubMed
Hajkova P, Jeffries SJ, Lee C, Miller N, Jackson SP, Surani MA. Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 2010; 329: 78–82. PubMed PMC
Lavrentyeva E, Shishova K, Kagarlitsky G, Zatsepina O. Localisation of RNAs and proteins in nucleolar precursor bodies of early mouse embryos. Reprod Fertil Dev 2017; 29: 509–520. PubMed
Abe K, Yamamoto R, Franke V, Cao M, Suzuki Y, Suzuki MG, Vlahovicek K, Svoboda P, Schultz RM, Aoki F. The first murine zygotic transcription is promiscuous and uncoupled from splicing and 3′ processing. EMBO J 2015; 34: 1523–1537. PubMed PMC
Funaya S, Aoki F. Regulation of zygotic gene activation by chromatin structure and epigenetic factors. J Reprod Dev 2017; 63: 359–363. PubMed PMC
Kresoja-Rakic J, Santoro R. Nucleolus and rRNA gene chromatin in early embryo development. Trends Genet 2019; 35: 868–879. PubMed PMC
Burton A, Torres-Padilla ME. Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis. Nat Rev Mol Cell Biol 2014; 15: 723–734. PubMed
Modliński JA. Haploid mouse embryos obtained by microsurgical removal of one pronucleus. J Embryol Exp Morphol 1975; 33: 897–905. PubMed
Clark TG, Rosenbaum JL. An actin filament matrix in hand-isolated nuclei of X. laevis oocytes. Cell 1979; 18: 1101–1108. PubMed
Handwerger KE, Cordero JA, Gall JG. Cajal bodies, nucleoli, and speckles in the Xenopus oocyte nucleus have a low-density, sponge-like structure. Mol Biol Cell 2005; 16: 202–211. PubMed PMC
Borsuk E. Preimplantation development of gynogenetic diploid mouse embryos. J Embryol Exp Morphol 1982; 69: 215–222. PubMed
Mohammed AA, Karasiewicz J, Modliński JA. Developmental potential of selectively enucleated immature mouse oocytes upon nuclear transfer. Mol Reprod Dev 2008; 75: 1269–1280. PubMed
Greda P, Karasiewicz J, Modlinski JA. Mouse zygotes as recipients in embryo cloning. Reproduction 2006; 132: 741–748. PubMed
Gręda P, Modliński JA, Piliszek A. Developmental potential of selectively enucleated mouse zygotes reconstituted with embryonic cell, embryonic stem cell and somatic cell nuclei. Anim Sci Pap Rep 2015; 33: 323–336.
Fulka H, Ogura A, Loi P, Fulka J, Jr. Dissecting the role of the germinal vesicle nuclear envelope and soluble content in the process of somatic cell remodelling and reprogramming. J Reprod Dev 2019; 65: 433–441. PubMed PMC
McGrath J, Solter D. Nuclear transplantation in the mouse embryo by microsurgery and cell fusion. Science 1983; 220: 1300–1302. PubMed
McGrath J, Solter D. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 1984; 37: 179–183. PubMed
Fulka J, Jr, Horská M, Moor RM, Fulka J, Kanka J. Oocyte-specific modulation of female pronuclear development in mice. Dev Biol 1996; 178: 1–12. PubMed
Fulka J, Jr, Moor RM, Loi P, Fulka J. Enucleolation of porcine oocytes. Theriogenology 2003; 59: 1879–1885. PubMed
Fulka H, Mrazek M, Fulka J, Jr. Nucleolar dysfunction may be associated with infertility in humans. Fertil Steril 2004; 82: 486–487. PubMed
Kyogoku H, Ogushi S, Miyano T. Nucleoli from two-cell embryos support the development of enucleolated germinal vesicle oocytes in the pig. Biol Reprod 2012; 87: 113. PubMed
Fulka J, Jr, Langerova A, Loi P, Martinkova S, Fulka H. Transplantation of nucleoli into human zygotes: not as simple as expected? J Assist Reprod Genet 2011; 28: 385–389. PubMed PMC
Nguyen Ba AN, Pogoutse A, Provart N, Moses AM. NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 2009; 10: 202. PubMed PMC
Scott MS, Boisvert FM, McDowall MD, Lamond AI, Barton GJ. Characterization and prediction of protein nucleolar localization sequences. Nucleic Acids Res 2010; 38: 7388–7399. PubMed PMC
Fulka J, Jr, Benc M, Loi P, Langerova A, Fulka H. Function of atypical mammalian oocyte/zygote nucleoli and its implications for reproductive biology and medicine. Int J Dev Biol 2019; 63: 105–112. PubMed
Kyogoku H, Wakayama T, Kitajima TS, Miyano T. Single nucleolus precursor body formation in the pronucleus of mouse zygotes and SCNT embryos. PLoS One 2018; 13: e0202663. PubMed PMC
Ogushi S, Saitou M. The nucleolus in the mouse oocyte is required for the early step of both female and male pronucleus organization. J Reprod Dev 2010; 56: 495–501. PubMed
Kyogoku H, Fulka J, Jr, Wakayama T, Miyano T. De novo formation of nucleoli in developing mouse embryos originating from enucleolated zygotes. Development 2014; 141: 2255–2259. PubMed
Mao YS, Zhang B, Spector DL. Biogenesis and function of nuclear bodies. Trends Genet 2011; 27: 295–306. PubMed PMC
Gurdon JB. From nuclear transfer to nuclear reprogramming: the reversal of cell differentiation. Annu Rev Cell Dev Biol 2006; 22: 1–22. PubMed
Bui HT, Wakayama S, Kishigami S, Kim JH, Van Thuan N, Wakayama T. The cytoplasm of mouse germinal vesicle stage oocytes can enhance somatic cell nuclear reprogramming. Development 2008; 135: 3935–3945. PubMed
Maeda Y, Yanagimachi H, Tateno H, Usui N, Yanagimachi R. Decondensation of the mouse sperm nucleus within the interphase nucleus. Zygote 1998; 6: 39–45. PubMed
Egli D, Eggan K. Recipient cell nuclear factors are required for reprogramming by nuclear transfer. Development 2010; 137: 1953–1963. PubMed PMC
Konno S, Wakayama S, Ito D, Kazama K, Hirose N, Ooga M, Wakayama T. Removal of remodeling/reprogramming factors from oocytes and the impact on the full-term development of cloned embryos. Development 2020; 147: dev190777. PubMed
Fulka H, Fulka J, Jr. Nucleolar transplantation in oocytes and zygotes: challenges for further research. Mol Hum Reprod 2010; 16: 63–67. PubMed
Fulka H, Langerova A. Nucleoli in embryos: a central structural platform for embryonic chromatin remodeling? Chromosome Res 2019; 27: 129–140. PubMed
Campbell KHS, Loi P, Otaegui PJ, Wilmut I. Cell cycle co-ordination in embryo cloning by nuclear transfer. Rev Reprod 1996; 1: 40–46. PubMed
Probst AV, Okamoto I, Casanova M, El Marjou F, Le Baccon P, Almouzni G. A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell 2010; 19: 625–638. PubMed
Jachowicz JW, Santenard A, Bender A, Muller J, Torres-Padilla ME. Heterochromatin establishment at pericentromeres depends on nuclear position. Genes Dev 2013; 27: 2427–2432. PubMed PMC
Mukherjee RN, Sallé J, Dmitrieff S, Nelson KM, Oakey J, Minc N, Levy DL. The perinuclear ER scales nuclear size independently of cell size in early embryos. Dev Cell 2020; 54: 395–409.e7. PubMed PMC
Chen H, Good MC. Nuclear sizER in early development. Dev Cell 2020; 54: 297–298. PubMed
Ungricht R, Kutay U. Mechanisms and functions of nuclear envelope remodelling. Nat Rev Mol Cell Biol 2017; 18: 229–245. PubMed
Dang-Nguyen TQ, Torres-Padilla ME. How cells build totipotency and pluripotency: nuclear, chromatin and transcriptional architecture. Curr Opin Cell Biol 2015; 34: 9–15. PubMed
Borsos M, Perricone SM, Schauer T, Pontabry J, de Luca KL, de Vries SS, Ruiz-Morales ER, Torres-Padilla ME, Kind J. Genome-lamina interactions are established de novo in the early mouse embryo. Nature 2019; 569: 729–733. PubMed PMC
Martin C, Beaujean N, Brochard V, Audouard C, Zink D, Debey P. Genome restructuring in mouse embryos during reprogramming and early development. Dev Biol 2006; 292: 317–332. PubMed
Martin C, Brochard V, Migné C, Zink D, Debey P, Beaujean N. Architectural reorganization of the nuclei upon transfer into oocytes accompanies genome reprogramming. Mol Reprod Dev 2006; 73: 1102–1111. PubMed
Fulka H, Rychtarova J, Loi P. The nucleolus-like and precursor bodies of mammalian oocytes and embryos and their possible role in post-fertilization centromere remodelling. Biochem Soc Trans 2020; 48: 581–593. PubMed
Cavazza T, Takeda Y, Politi AZ, Aushev M, Aldag P, Baker C, Choudhary M, Bucevičius J, Lukinavičius G, Elder K, Blayney M, Lucas-Hahn A, Niemann H, Herbert M, Schuh M. Parental genome unification is highly error-prone in mammalian embryos. Cell 2021; 184: 2860–2877.e22. PubMed PMC
Inoue T, Taguchi S, Uemura M, Tsujimoto Y, Miyazaki K, Yamashita Y. Migration speed of nucleolus precursor bodies in human male pronuclei: a novel parameter for predicting live birth. J Assist Reprod Genet 2021; 38: 1725–1736. PubMed PMC
Tesarik J, Greco E. The probability of abnormal preimplantation development can be predicted by a single static observation on pronuclear stage morphology. Hum Reprod 1999; 14: 1318–1323. PubMed
Benc M, Martinkova S, Rychtarova J, Fulka J, Jr, Bartkova A, Fulka H, Laurincik J. Assessing the effect of interspecies oocyte nucleolar material dosage on embryonic development. Theriogenology 2020; 155: 17–24. PubMed
Morovic M, Strejcek F, Nakagawa S, Deshmukh RS, Murin M, Benc M, Fulka H, Kyogoku H, Pendovski L, Fulka J, Jr, Laurincik J. Mouse oocytes nucleoli rescue embryonic development of porcine enucleolated oocytes. Zygote 2017; 25: 675–685. PubMed
Chen M, Zhu Q, Li C, Kou X, Zhao Y, Li Y, Xu R, Yang L, Yang L, Gu L, Wang H, Liu X, Jiang C, Gao S. Chromatin architecture reorganization in murine somatic cell nuclear transfer embryos. Nat Commun 2020; 11: 1813. PubMed PMC
Zhao K, Wang M, Gao S, Chen J. Chromatin architecture reorganization during somatic cell reprogramming. Curr Opin Genet Dev 2021; 70: 104–114. PubMed
Yang M, Yu H, Yu X, Liang S, Hu Y, Luo Y, Izsvák Z, Sun C, Wang J. Chemical-induced chromatin remodeling reprograms mouse ESCs to totipotent-like stem cells. Cell Stem Cell 2022; 29: 400–418.e13. PubMed