Application of interspecific Somatic Cell Nuclear Transfer (iSCNT) in sturgeons and an unexpectedly produced gynogenetic sterlet with homozygous quadruple haploid
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29662093
PubMed Central
PMC5902484
DOI
10.1038/s41598-018-24376-1
PII: 10.1038/s41598-018-24376-1
Knihovny.cz E-zdroje
- MeSH
- druhová specificita MeSH
- genotyp MeSH
- haploidie MeSH
- homozygot MeSH
- klonování organismů metody MeSH
- mikrosatelitní repetice MeSH
- ohrožené druhy MeSH
- ryby embryologie genetika růst a vývoj MeSH
- techniky jaderného přenosu * MeSH
- tetraploidie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Rusko MeSH
Somatic cell nuclear transfer (SCNT) is a very promising cloning technique for reconstruction of endangered animals. The aim of the present research is to implement the interspecific SCNT (iSCNT) technique to sturgeon; one fish family bearing some of the most critically endangered species. We transplanted single cells enzymatically isolated from a dissociated fin-fragment of the Russian sturgeon (Acipenser gueldenstaedtii) into non-enucleated eggs of the sterlet (Acipenser ruthenus), two species bearing different ploidy (4n and 2n, respectively). Up to 6.7% of the transplanted eggs underwent early development, and one feeding larva (0.5%) was successfully produced. Interestingly, although this transplant displayed tetraploidism (4n) as the donor species, the microsatellite and species-specific analysis showed recipient-exclusive homozygosis without any donor markers. Namely, with regards to this viable larva, host genome duplication occurred twice to form tetraploidism during its early development, probably due to iSCNT manipulation. The importance of this first attempt is to apply iSCNT in sturgeon species, establishing the crucial first steps by adjusting the cloning-methodology in sturgeon's biology. Future improvements in sturgeon's cloning are necessary for providing with great hope in sturgeon's reproduction.
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Wildt DE. Genetic resource banks for conserving wildlife species: Justification, examples and becoming organized on a global basis. Anim. Reprod. Sci. 1992;28:247–257.
Wells DN, Misica PM, Tervit HR, Vivanco WH. Adult somatic cell nuclear transfer is used to preserve the last surviving cow of the Enderby Island cattle breed. Reprod. Fertil. Dev. 1998;10:369–378. PubMed
Lanza RP, et al. Cloning of an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning. 2000;2:79–90. PubMed
Solti L, Crichton EG, Loskutoff NM, Cseh S. Economical and ecological importance of indigenous livestock and the application of assisted reproduction to their preservation. Theriogenology. 2000;53:149–162. PubMed
Loi P, et al. Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat. Biotechnol. 2001;19:962–964. PubMed
Labbé, C., Robles, V. & Herraez, M. P. Cryopreservation of gametes for aquaculture and alternative cell sources for genome preservation. In book: Advances in Aquaculture Hatchery Technology (eds Allan, G. & Burnell, G) 76–116 (Elsevier, 2013).
Srirattana K, et al. Full-term development of gaur-bovine interspecies somatic cell nuclear transfer embryos: Effect of trichostatin A treatment. Cell. Reprogram. 2012;14:248–257. PubMed
Gómez MC, Pope CE, Dresser BL. Nuclear transfer in cats and its application. Theriogenology. 2006;66:72–81. PubMed
Wani NA, Vettical BS, Hong SB. First cloned Bactrian camel (Camelus bactrianus) calf produced by interspecies somatic cell nuclear transfer: A step towards preserving the critically endangered wild Bactrian camels. PLoS ONE. 2017;12(5):e0177800. PubMed PMC
Birstein VJ, Bemis WE, Waldman JR. The threatened status of acipenseriform species: a summary. Environ. Biol. Fish. 1997;48:427–435.
International Union for Conservation of Nature (2017). The IUCN Red List of Threatened Species, Version 2017–2, www.iucnredlist.org (accessed on 14 September 2017).
Birstein VJ, Vasiľev VP. Tetraploid-octoploid relationships and karyological evolution in the order Acipenseriformes (Pisces): karyotypes, nucleoli, and nucleolus-organizer regions in four acipenserid species. Genetica. 1987;73:3–12.
Fontana F, et al. Karyotypic characterization of the great sturgeon, Huso huso, by multiple staining techniques and fluorescent in situ hybridization. Mar. Biol. 1998;132:495–501.
Tagliavini J, et al. Molecular cytogenetic analysis of the karyotype of the European Atlantic sturgeon. Acipenser sturio. Heredity. 1999;83:520–525. PubMed
Fontana F, Lanfredi M, Rossi R, Bronzi P, Arlati G. Karyotypic characterization of Acipenser gueldenstaedti with C-, AgNO3 and fluorescence banding techniques. Ital. J. Zool. 1996;63:113–118.
Vasiľev VP, Vasiľeva ED, Shedko SV, Novomodny GV. Ploidy levels in the kaluga Huso dauricus and sakhalin sturgeon Acipenser mikadoi (Acipenseridae, Pisces) Dokl. Biol. Sci. 2009;426:228–231. PubMed
Fontana F, et al. Evidence of hexaploid karyotype in shortnose sturgeon. Genome. 2008;51:113–119. PubMed
Zhu ZY, Sun YH. Embryonic and genetic manipulation in fish. Cell Res. 2000;10:17–27. PubMed
Lee KY, Huang H, Ju B, Yang Z, Lin S. Cloned zebrafish by nuclear transfer from long-term-cultured cells. Nat. Biotechnol. 2002;20:795–799. PubMed
Ju B, et al. Development and gene expression of nuclear transplants generated by transplantation of cultured cells nuclei into non-enucleated eggs in the medaka Oryzias latipes. Dev. Growth Differ. 2003;45:167–174. PubMed
Kaftanovskaya E, Motosugi N, Kinoshita M, Ozato K, Wakamatsu Y. Ploidy mosaicism in well-developed nuclear transplants produced by transfer of adult somatic cell nuclei to non-enucleated eggs of medaka (Oryzias latipes) Dev. Growth Differ. 2007;49:691–698. PubMed
Wakamatsu Y. Novel method for the nuclear transfer of adult somatic cells in medaka fish (Oryzias latipes): use of diploidized eggs as recipients. Dev. Growth Differ. 2008;50:427–436. PubMed
Siripattarapravat K, Pinmee B, Venta PJ, Chang CC, Cibelli JB. Somatic cell nuclear transfer in zebrafish. Nat. Methods. 2009;6:733–735. PubMed
Luo DJ, Hu W, Chen SP, Zhu ZY. Critical developmental stages for the efficiency of somatic cell nuclear transfer in zebrafish. Int. J. Biol. Sci. 2011;7:476–486. PubMed PMC
Liu TM, et al. Factors affecting the efficiency of somatic cell nuclear transplantation in the fish embryo. J. Exp. Zool. 2002;293:719–725. PubMed
Akimenko MA, Mari-Beffa M, Becerra J, Geraudie J. Old questions, new tools, and some answers to the mystery of fin regeneration. Dev. Dynam. 2003;226:190–201. PubMed
Chenais N, Depincé A, Le Bail PY, Labbé C. Fin cell cryopreservation and fish reconstruction by nuclear transfer stand as promising technologies for preservation of finfish genetic resources. Aquac. Int. 2014;22:63–76.
Le Bail PY, et al. Optimization of somatic cell injection in the perspective of nuclear transfer in goldfish. BMC Dev. Biol. 2010;10:64. PubMed PMC
Meissner A, Jaenisch R. Mammalian nuclear transfer. Dev. Dynam. 2006;235:2460–2469. PubMed
Hochleithner, M. & Gessner, J. The Sturgeons and Paddlefishes (Acipenseriformes) of the World - Biology and Aquaculture. 1–248 (AquaTech Publications, 2012).
Siripattarapravat K, Busta A, Steibel JP, Cibelli J. Characterization and in vitro control of MPF activity in zebrafish eggs. Zebrafish. 2009;6:97–105. PubMed
Bubenshchikova E, et al. Generation of fertile and diploid fish, medaka (Oryzias latipes), from nuclear transplantation of blastula and four-somite-stage embryonic cells into nonenucleated unfertilized eggs. Cloning Stem Cells. 2005;7:255–264. PubMed
Gasaryan KG, Hung NM, Neyfahk AA, Ivanenkov VV. Nuclear transplantation in teleost Misgurnus fossilis L. Nature. 1979;280:585–587. PubMed
Tung TC, et al. Nuclear transplantation in fishes. Sci. Sin. 1963;14:1244–1245.
Gibbs PDL, Peek A, Thorgaard G. An in vivo screen for the luciferase transgene in zebrafish. Mol. Mar. Biol. Biotechnol. 1994;3:307–316. PubMed
Lee KW, Webb SE, Miller AL. A wave of free cytosolic calcium traverses zebrafish eggs on activation. BMC Dev. Biol. 1999;214:168–180. PubMed
Depincé A, Marandel L, Goardon L, Le Bail PY, Labbé C. Trout coelomic fluid suitability as Goldfish oocyte extender can be determined by a simple turbidity test. Theriogenology. 2011;75:1755–1761. PubMed
Siripattarapravat K, et al. The influence of donor nucleus source on the outcome of zebrafish somatic cell nuclear transfer. Int. J. Dev. Biol. 2010;54:1679–1683. PubMed
Ikegami R, Rivera-Bennetts AK, Brooker DL, Yager TD. Effect of inhibitors of DNA replication on early zebrafish embryos: evidence for coordinate activation of multiple intrinsic cell-cycle checkpoints at the mid-blastula transition. Zygote. 1997;5:153–175. PubMed
Kane DA, Kimmel CB. The zebrafish midblastula transition. Development. 1993;119:447–456. PubMed
Blelloch R, et al. Reprogramming efficiency following somatic cell nuclear transfer is influenced by the differentiation and methylation state of the donor nucleus. Stem Cells. 2006;24:2007–2013. PubMed PMC
Niemann H, Tian XC, King WA, Lee RSF. Epigenetic reprogramming in embryonic and foetal development upon somatic cell nuclear transfer cloning. Reproduction. 2008;135:151–163. PubMed
Bubenshchikova E, et al. Diploidized eggs reprogram adult somatic cell nuclei to pluripotency in nuclear transfer in medaka fish (Oryzias latipes) Dev. Growth Differ. 2007;49:699–709. PubMed
Newport J, Kirschner M. A Major Developmental Transition in Early Xenopus Embryos: I. Characterization and Timing of Cellular Changes at the Midblastula Stage. Cell. 1982;3:675–686. PubMed
Havelka M, Kašpar V, Hulak M, Flajšhans M. Sturgeon genetics and cytogenetics: a review related to ploidy levels and interspecific hybridization. Folia Zool. 2011;60:93–103.
Havelka M, Fujimoto T, Hagihara S, Adachi S, Arai K. Nuclear DNA markers for identification of Beluga and Sterlet sturgeons and their interspecific Bester hybrid. Sci Rep. 2017;7:1694. PubMed PMC
Cherr GN, Clark WH., Jr. Fine structure of the envelope and micropyles in the eggs of the white sturgeon, Acipenser transmontanus Richardson. Dev. Growth Differ. 1982;24:341–352. PubMed
Piferrer F, et al. Polyploid fish and shellfish: production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture. 2009;239:125–156.
Yabe T, Ge X, Pelegri F. The zebrafish maternal-effect gene cellular atoll encodes the centriolar component sas-6 and defects in its paternal function promote whole genome duplication. Dev. Biol. 2007;312:44–60. PubMed PMC
Sohrabnezhad M, Kalbassi MR, Nazari RM, Bahmani M. Short-term storage of Persian sturgeon (Acipenser persicus) ova in artificial media and coelomic fluid. J. Appl. Ichthyol. 2006;22:395–399.
May B, Krueger CC, Kincaid HL. Genetic variation at microsatellite loci in sturgeon: primer sequence homology in Acipenser and Scaphirhynchus. Can. J. Fish Aquat. Sci. 1997;54:1542–1547.
King TL, Lubinski BA, Spidle AP. Microsatellite DNA variation in Atlantic sturgeon Acipenser oxyrinchus oxyrinchus: and cross-species amplification in the Acipenseridae. Conserv. Genet. 2001;2:103–119.
McQuown E, Gall GAE, May B. Characterization and inheritance of six microsatellite loci in lake sturgeon. Trans. Am. Fish Soc. 2002;131:299–307.
Havelka M, Hulak M, Bailie DA, Prodöhl PA, Flajšhans M. Extensive Genome Duplication in Sturgeons: New Evidence from Microsatellite Data. J. Appl. Ichthyol. 2013;29:704–708.
Kearse M, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. PubMed PMC