Induced sterility in fish and its potential and challenges for aquaculture and germ cell transplantation technology: a review
Abstract
Interest in reproductively sterile fish in aquaculture has prompted research into their production. Several methods are available for inducing sterility and optimizing its application in the global fishery industry. Sterilization can potentially be accomplished through irradiation, surgery, or chemical and hormonal treatment. Alternative approaches include triploidization, hybridization, and generation of new lines via advanced biotechnological techniques. Triploids of many commercially important species have been studied extensively and have been produced on a large scale for many years. Novel approaches, including disruption of gonadotropin releasing hormone signalling and genetic ablation of germ cells, have been developed that are effective in producing infertile fish but have the disadvantage of not being 100% reliable or are impractical for large-scale aquaculture. We review currently used technologies and recent advances in induction of sterility in fish, especially those intended for use in germ cell transplantation. Knowledge of the implications of these approaches remains incomplete, imposing considerable limitations.
Acknowledgements
The study was financially supported by the Ministry of Education, Youth and Sports of the Czech Republic – projects CENAKVA (No. CZ.1.05/2.1.00/01.0024) and CENAKVA II (No. LO1205 under the NPU I program), and by the Grant Agency of the University of South Bohemia in Ceske Budejovice (No. 125/2016/Z) and by the Czech Science Foundation (No. P502/13/26952S).
References
Allen S.K.J. & Wattendorf R.J. 1987. Triploid grass carp: status and management implications. Fisheries 12: 20–24.10.1577/1548-8446(1987)012<0020:TGCSAM>2.0.CO;2Search in Google Scholar
Arai K. 2001. Genetic improvement of aquaculture finfish species by chromosome manipulation techniques in Japan. Aquaculture 197: 205–228.10.1016/B978-0-444-50913-0.50013-8Search in Google Scholar
Bart A.N. & Dunham R.A., 1990. Factors affecting survival of channel catfish after surgical removal of testes. Progressive Fish Culturist 52: 241–246.10.1577/1548-8640(1990)052<0241:FASOCC>2.3.CO;2Search in Google Scholar
Bartley D.M., Rana K. & Immink A.J. 2001. The use of interspecific hybrids in aquaculture and fisheries. Rev. Fish Biol. Fish. 10: 325–337.10.1023/A:1016691725361Search in Google Scholar
Beaumont A.R. & Fairbrother J.E. 1991. Ploidy manipulation in molluscan shellfish: a review. J. Shellfish Res. 10: 1–18.Search in Google Scholar
Benfey T.J. 1999. The physiology and behavior of triploid fishes. Rev. Fish. Sci. 7: 39–67.10.1080/10641269991319162Search in Google Scholar
Benfey T.J., 2001. Use of sterile triploid Atlantic salmon (Salmo salar L.) for aquaculture in New Brunswick, Canada. ICES J. Mar. Sci. 58: 525–529.10.1006/jmsc.2000.1019Search in Google Scholar
Benfey T.J., Bosa P.G., Richardson N.L. & Donaldson E.M. 1988. Effectiveness of a commercial-scale pressure shocking device for producing triploid salmonids. Aquacult. Eng. 7: 147–154.10.1016/0144-8609(88)90017-9Search in Google Scholar
Benfey T.J. & Sutterlin, A.M. 1984a. Growth and gonadal development in triploid landlocked Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 41: 1387–1392.10.1139/f84-171Search in Google Scholar
Benfey T.J. & Sutterlin, A.M. 1984b. Triploidy induced by heat shock and hydrostatic pressure in landlocked Atlantic salmon (Salmo salar L.) Aquaculture 4: 359–367.10.1016/0044-8486(84)90328-4Search in Google Scholar
Billard R. 1982. Attempts to inhibit testicular growth in rainbow trout with anti-androgens (cyproterone, cyproterone acetate, oxymetholone) and busulfan given during the period of spermatogenesis. Gen. Comp. Endocrinol. 1: 33–38.10.1016/0016-6480(82)90035-1Search in Google Scholar
Bonham K. & Donaldson L.R. 1972. Sex ratios and retardation of gonadal development in chronically gamma irradiated Chinook salmon smolts. Transact. Amer. Fish. Soc. 3: 428–423.10.1577/1548-8659(1972)101<428:SRAROG>2.0.CO;2Search in Google Scholar
Bontems F., Stein A., Marlow F., Lyautey J., Gupta T., Mullins M.C. & Dosch R. 2009. Bucky ball organizes germ plasm assembly in zebrafish. Curr. Biol. 19: 414–422.10.1016/j.cub.2009.01.038Search in Google Scholar
Boonanuntanasarn S., Yoshizaki G. & Takeuchi T., 2003. Specific gene silencing using small interfering RNAs in fish embryos. Biochem. Biophys. Res. Commun. 310: 1089–1095.10.1016/j.bbrc.2003.09.127Search in Google Scholar
Boonanuntanasarn S., Yoshizaki G., Takeuchi Y., Morita T. & Takeuchi T. 2002. Gene: knock-down in rainbow trout embryos using antisense morpholino phosphorodiamidate oligonucleotides. Mar. Biotechnol. 4: 256–266.10.1007/s10126-002-0017-xSearch in Google Scholar
Brinster R.L. 2002. Germline stem cell transplantation and transgenesis. Science 296: 2174–2175.10.1126/science.1071607Search in Google Scholar
Brinster R.L. & Avarbock M.R. 1994. Germline transmission of donor haplotype following spermatogonial transplantation. Proc. Natl. Acad. Sci. USA 91: 11303–11307.10.1073/pnas.91.24.11303Search in Google Scholar
Bucci L.R. & Meistrich M.L. 1987. Effects of busulfan on murine spermatogenesis: cytotoxicity, sterility, sperm abnormalities, and dominant lethal mutations. Mutat. Res. 176: 259–268.10.1016/0027-5107(87)90057-1Search in Google Scholar
Byamungua N., Darras VM. & Kühn ER. 2001. Growth of heat-shock induced triploids of blue tilapia, Oreochromis aureus, reared in tanks and in ponds in Eastern Congo 1: feeding regimes and compensatory growth response of triploid females. Aquaculture 1—2: 109–122.10.1016/S0044-8486(00)00605-0Search in Google Scholar
Cal R.M., Vidal S., Gómez C., Álvarez-Blázquez B., Martínez P. & Piferrer F. 2006. Growth and gonadal development in diploid and triploid turbot (Scophthalmus maximus). Aquaculture 251: 99–108.10.1016/j.aquaculture.2005.05.010Search in Google Scholar
Chen S.L., Sha Z.X. Ye H.Q., Liu Y., Tian Y.S., Hong Y. & Tang Q.S. 2007. Pluripotency and chimera competence of an embryonic stem cell line from the sea perch (Lateolabrax japonicus). Mar. Biotechnol. 1: 82–91.10.1007/s10126-006-6050-1Search in Google Scholar
Cherfas N.B., Gomelsky B., Ben-Dom N., Peretz Y. & Hulata G. 1994. Assessment of triploid common carp (Cyprinus carpio L.) for culture. Aquaculture 1: 11–18.10.1016/0044-8486(94)90187-2Search in Google Scholar
Chevassus B. 1983. Hybridization in fish. Aquaculture 33: 245–262.10.1016/0044-8486(83)90405-2Search in Google Scholar
Chourrout D., Chevassus B., Krieg F., Happe A., Burger G. & Renard P. 1986. Production of second generation triploid and tetraploid rainbow trout by mating tetraploid males and diploid females. Potential of tetraploid fish. Theor. Appl. Genet. 72: 193–206.10.1007/BF00266992Search in Google Scholar
Ciruna B., Weidinger G., Knaut H., Thisse B., Thisse C., Raz E. & Schier A.F. 2002. Production of maternal-zygotic mutant zebrafish by germ-line replacement. Proc. Natl. Acad. Sci. USA 99: 14919–14924.10.1073/pnas.222459999Search in Google Scholar
Daya A., Vatine G.D., Becker-Cohen M., Tal-Goldberg T., Friedmann A., Gothilf Y., Du S.J. & Mitrani-Rosenbaum S. 2014. Gne depletion during zebrafish development impairs skeletal muscle structure and function. Hum. Mol. Gen. 13: 3349–3361.10.1093/hmg/ddu045Search in Google Scholar
de Siqueira-Silva, D.H., dos Santos Silva, A.P., Ninhaus-Silveira, A., Verissimo-Silveira R. 2015. The effects of temperature and busulfan (Myleran) on yellowtail tetra Astyanax altiparanae (Pisces, Characiformes) spermatogenesis. Theriogenology 6: 1033–1042.10.1016/j.theriogenology.2015.06.004Search in Google Scholar
Devlin R.H. & Nagahama Y. 2002. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208: 191–364.10.1016/S0044-8486(02)00057-1Search in Google Scholar
Dodd A., Chambers S.P. & Love D.R. 2004. Short interfering RNA-mediated gene targeting in the zebrafish. FEBS Letters. 561: 89–93.10.1016/S0014-5793(04)00129-2Search in Google Scholar
Draper B.W., McCallum C.M. & Moens C.B. 2007. Nanos1 is required to maintain oocyte production in adult zebrafish. Dev. Biol. 305: 589–598.10.1016/j.ydbio.2007.03.007Search in Google Scholar PubMed PubMed Central
Draper W.B., Morcos P.A. & Kimmel C.B. 2001. Inhibition of zebrafish fgf8 pre-mRNA splicing with morpholino oligos: a quantifiable method for gene knockdown. Genesis 30: 154–156.10.1002/gene.1053Search in Google Scholar PubMed
Dumstrei K., Mennecke R. & Raz E. 2004. Signaling pathways controlling primordial germ cell migration in zebrafish. J. Cell. Sci. 117: 4787–4795.10.1242/jcs.01362Search in Google Scholar
Ekker S.C. & Larson J.D. 2001. Morphant technology in Mmodel developmental systems. Genesis 30: 89–93.10.1002/gene.1038Search in Google Scholar
Felip A., Piferrer F., Carrillo M. & Zanuy S. 2001a. Comparative growth performance between diploid and triploid sea bass (Dicentrarchus labrax L.) over the first four spawning seasons. J. Fish. Biol. 58: 76–88.10.1111/j.1095-8649.2001.tb00500.xSearch in Google Scholar
Felip A., Zanuy S., Carrillo M., Martínez G., Ramos J. & Piferrer F. 1997. Optimal conditions for the induction of triploidy in the sea bass (Dicentrarchus labrax L.). Aquaculture 152: 287–298.10.1016/S0044-8486(96)01509-8Search in Google Scholar
Felip A., Zanuy S., Carrillo M. & Piferrer F. 2001b. Induction of triploidy and gynogenesis in teleost fish with emphasis on marine species. Genetica 111: 175–195.10.1023/A:1013724322169Search in Google Scholar
França L.R., Ogawa T., Avarbock M.R., Brinster R.L. & Russell L.D. 1998. Germ cell genotype controls cell cycle during spermatogenesis. Biol. Rep. 59: 1371–1377.10.1095/biolreprod59.6.1371Search in Google Scholar
Francescon A., Barbaro A., Bertotto D., Libertini A., Cepollaro F., Richard J., Belvedere P. & Colombo L. 2004. Assessment of homozygosity and fertility in meiotic gynogens of the European sea bass (Dicentrarchus labrax L.). Aquaculture 243: 93–102.10.1016/j.aquaculture.2004.10.023Search in Google Scholar
Fraser T.W.K., Fjelldal P.G., Hansen T. & Maye I. 2012. Welfare considerations of triploid fish. Rev. Fish. Sci. 4: 192–211.10.1080/10641262.2012.704598Search in Google Scholar
Galderisi U., Cascino A. & Giordano A. 1999. Antisense oligonucleotides as therapeutic agents. J. Cell Physiol. 181: 251–257.10.1002/(SICI)1097-4652(199911)181:2<251::AID-JCP7>3.0.CO;2-DSearch in Google Scholar
Gillet C., Vauchez C. & Haffray P. 2001. Triploidy induced by pressure shock in Arctic charr (Salvelinus alpinus): growth, survival and maturation until the third year. Aquatic Living Resources 14: 327–334.10.1016/S0990-7440(01)01129-9Search in Google Scholar
Gruber J., Manninga H., Tuschl T., Osborn M. & Weber K. 2005. Specific RNAi mediated gene knockdown in zebrafish cell lines. RNA Biol. 2: 101–105.10.4161/rna.2.3.2060Search in Google Scholar
Haffray P., Bruant J.S., Facqueur J.M. & Fostier A. 2005. Gonad development, growth and quality traits in triploids of the protandrous hermaphrodite gilthead seabream Sparus aurata. Aquaculture 247: 107–117.10.1016/j.aquaculture.2005.02.037Search in Google Scholar
Hallerman E.M. & Kapuscinski A.R. 1993. Genetic conservation of salmonid fishes, pp. 93–112. In: Cloud J.G. & Thorgaard G.H. (eds), Potential Impacts of Transgenic and Genetically Manipulated Fish on Natural Populations. Plenum Press, New York.10.1007/978-1-4615-2866-1_7Search in Google Scholar
Hallerman E.M. & Kapuscinsky A.R. 1995. Incorporating risk assessment and risk management into public policies on genetically modified finfish and shellfish. Aquaculture 137: 9–17.10.1016/0044-8486(95)01089-0Search in Google Scholar
Hamaguchi S. & Sakaizum M. 1992. Sexually differentiated mechanisms of sterility in interspecific hybrids between Oryzias latipes and O. curvinotus. J. Exp. Zool. 3: 323–329.10.1002/jez.1402630312Search in Google Scholar
Hamasaki M., Takeuchi Y., Miyaki K. & Yoshizaki G. 2013. Gonadal development and fertility of triploid grass puffer Takifugu niphobles induced by cold shock treatment. Mar. Biotechnol. 15: 133–144.10.1007/s10126-012-9470-3Search in Google Scholar
Holmefjord I. & Refstie T. 1997. Induction of triploidy in Atlantic halibut by temperature shocks. Aquacult. Int. 5: 169–173.Search in Google Scholar
Houwing S., Kamminga L.M., Berezikov E., Cronembold D., Girard A., Van den Elst H., Filippov D.V., Blaser H., Raz E., Moens C.B, Plasterk R.H, Hannon G.J., Draper B.W. & Ketting R.F. 2007. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell 129: 69–82.10.1016/j.cell.2007.03.026Search in Google Scholar
Hruscha A., Krawitz P., Rechenberg A., Heinrich V., Hecht J., Haass C. & Schmid B. 2013. Efficient CRISPR/Cas9 genome editing with low off-target effects in zebrafish. Development 24: 4982–4987.10.1242/dev.099085Search in Google Scholar
Hsiao C.D. & Tsa H.J. 2003. Transgenic zebrafish with fluorescent germ cell: a useful tool to visualize germ cell proliferation and juvenile hermaphroditism in vivo. Dev. Biol. 262: 313–323.10.1016/S0012-1606(03)00402-0Search in Google Scholar
Hsu C.C., Hou M.F., Hong J.R., Wu J.L. & Her G.M. 2010. Inducible male infertility by targeted cell ablation in zebrafish testis. Mar. Biotechnol. 12: 466–478.10.1007/s10126-009-9248-4Search in Google Scholar PubMed
Hu S.Y., Lin P.Y., Liao C.H., Gong H.Y., Lin G.H., Kawakami K. & Wu J.L. 2009. Nitroreductase mediated gonadal dysgenesis for infertility control of genetically modified zebrafish. Mar. Biotechnol. 12: 569–578.10.1007/s10126-009-9244-8Search in Google Scholar
Hu W., Li S., Tang B., Wang Y., Lin H., Liu X., Zou J. & Zhu Z. 2007. Antisense for gonadotropin-releasing hormone reduces gonadotropin synthesis and gonadal development in transgenic common carp (Cyprinus carpio). Aquaculture 271: 498–506.10.1016/j.aquaculture.2007.04.075Search in Google Scholar
Ihssen P.E., McKay L.R, McMillan I. & Phillips R.B. 1990. Ploidy manipulation and gynogenesis in fishes: cytogenetic and fisheries applications. Transact. Amer. Fish. Soc. 119: 698–717.10.1577/1548-8659(1990)119<0698:PMAGIF>2.3.CO;2Search in Google Scholar
Ito L.S., Cornejo A.M., Yamashita M. & Strüssmann C.A. 2008a. Thermal threshold and histological process of heat-induced sterility in adult pejerrey (Odontesthes bonariensis): a comparative analysis of laboratory and wild specimens. Physiol. Biochem. Zool. 81: 775–784.10.1086/591035Search in Google Scholar
Ito L.S., Takahashi C., Yamashita M. & Strüssmann C.A. 2008b. Warm water induces apoptosis, gonadal degeneration, and germ cell loss in subadult pejerrey Odontesthes bonariensis (Pisces, Atheriniformes). Physiol. Biochem. Zool. 81: 762–774.10.1086/590219Search in Google Scholar
Johnstone R. 1993. Maturity control in Atlantic salmon, pp. 99–105. In: Muir J.F. & Roberts R.J. (eds), Recent Advances in Aquaculture. Blackwell Scientific Publications, London.Search in Google Scholar
Knaut H., Pelegri F., Bohmann K., Schwarz H. & Nusslein-Volhard C. 2000. Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregation asymmetrically before germline specification. J. Cell. Biol. 149: 875–888.10.1083/jcb.149.4.875Search in Google Scholar
Kobayashi S. & Mogami M. 1958. Effects of X-irradiation upon rainbow trout (Salmo irideus). III. Ovary growth in the stages of fry and fingerlings. Bull. Fac. Fish. Hokkaido Univ. 9: 89–94.Search in Google Scholar
Kobayashi T., Kajiura-Kobayashi H. & Nagahama Y., 2002. Two isoforms of vasa homologs in a teleost fish: their differential expression during germ cell differentiation. Mech. Dev. 111: 167–171.10.1016/S0925-4773(01)00613-XSearch in Google Scholar
Koprunner M., Thisse C., Thisse B. & Raz E. 2001. A zebrafish nanos-related gene is essential for the development of primordial germ cells. Gen. Dev. 15: 2877–2885.10.1101/gad.212401Search in Google Scholar
Kucharczyk D., Targońska K., Szczerbowski A., Łuczyński M., Rożek W., Kujawa R. & Mamcarz A. 2008. Genetic inactivation of dace, Leuciscus leuciscus (L.), gametes using UV irradiation. Arch. Polish Fish. 4: 437–446.10.2478/s10086-008-0030-4Search in Google Scholar
Lacerda S.M.S.N., Batlouni S.R., Costa G.M., Segatelli T.M., Quirino B.R., Queiroz B.M., Kalapothakis E. & França L.R. 2010. A new and fast technique to generate offspring after germ cells transplantation in adult fish: the Nile tilapia (Oreochromis niloticus) model. PLoS One 5: e10740.10.1371/journal.pone.0010740Search in Google Scholar
Lacerda S.M.S.N., Batlouni S.R., Luiz H., Assis F., Resende M., Campos-Silva S.M., Campos-Silva R., Segatelli T.M. & França L.R. 2008. Germ cell transplantation in tilapia (Oreochromis niloticus). Cybium 2: 115–118.Search in Google Scholar
Lacerda S.M.S.N., Batlouni S.R., Silva S.B.G., Homem C.S.P. & França L.R. 2006. Germ cells transplantation in fish: the Nile-tilapia model. Animal Rep. 2: 146–159.Search in Google Scholar
Li M., Shen Q., Wong F.M., Xu H., Hong N., Zeng L., Liu L., Wei Q. & Hong Y. 2011. Germ cell sex prior to meiosis in the rainbow trout. Protein Cell 1: 48–54.10.1007/s13238-011-1003-8Search in Google Scholar PubMed PubMed Central
Li M.Y., Hong N., Xu H., Yi M., Li C., Gui J.F. & Hong Y. 2009. Medaka vasa are required for migration but not survival of primordial germ cells. Mech. Dev. 126: 366–381.10.1016/j.mod.2009.02.004Search in Google Scholar PubMed
Lin H.J., Lee S.H., Wu J.L., Duann Y.F. & Chen J.Y., 2013. Development of Cre-loxP technology in zebrafish to study the regulation of fish reproduction. Fish Physiol. Biochem. 39: 1525–1539.10.1007/s10695-013-9806-6Search in Google Scholar PubMed
Linhart O., Rodina M., Flajšhans M., Mavrodiev N., Nebesarova J., Gela D. & Kocour M. 2006. Studies on sperm of diploid and triploid tench (Tinca tinca L.). Aquacult. Int. 14: 9–25.10.1007/s10499-005-9010-5Search in Google Scholar
Liu L., Hong N., Xu H., Li M., Yan Y., Purwanti Y., Yi M., Li Z., Wang L. & Hong Y. 2009. Medaka dead end encodes a cytoplasmic protein and identifies embryonic and adult germ cells. Gene Expr. Patterns 9: 541–548.10.1016/j.gep.2009.06.008Search in Google Scholar PubMed
Maclean N., Hwang G., Molina A., Ashton T., Müller M., Rahman M.A. & Iyengar A. 2003. Reversibly-sterile fish via transgenesis. ISB News Report 12: 3–5.Search in Google Scholar
Majhi S.K., Hattori R.S., Rahman S.M. & Strussmann C.A. 2014. Surrogate production of eggs and sperm by intrapapillary transplantation of germ cells in cytoablated adult fish. PLoS One 4: e95294.10.1371/journal.pone.0095294Search in Google Scholar PubMed PubMed Central
Majhi S.K., Hattori R.S., Rahman S.M., Suzuki T. & Struss-mann C.A. 2009a. Experimentally induced depletion of germ cells in sub-adult Patagonian pejerrey (Odontesthes hatcheri) Theriogenology 71: 1162–1172.10.1016/j.theriogenology.2008.12.008Search in Google Scholar PubMed
Majhi S.K., Hattori R.S., Yokota M., Watanabe S. & Strussmann C.A. 2009b. Germ cell transplantation using sexually competent fish: an approach for rapid propagation of endangered and valuable germlines. PLoS One 7: e6132.10.1371/journal.pone.0006132Search in Google Scholar PubMed PubMed Central
Morcos P.A. 2007. Achieving targeted and quantifiable alteration of mRNA splicing with morpholino oligos. Biochem. Biophys. Res. Commun. 358: 521–527.10.1016/j.bbrc.2007.04.172Search in Google Scholar PubMed
Nam Y.K. & Kim D.S. 2004. Ploidy status of progeny from the crosses between tetraploid males and diploid females in mud loach (Misgurnus mizolepis). Aquaculture 236: 575–582.10.1016/j.aquaculture.2003.12.026Search in Google Scholar
Nobrega R.H., Greebe C.D., van de Kant H., Bogerd J., de Franca L.R. & Schulz R.W. 2010. Spermatogonial stem cell niche and spermatogonial stem cell transplantation in zebrafish. PLoS One 9: e12808.10.1371/journal.pone.0012808Search in Google Scholar
Oates A.C., Bruce A.E.E. & Ho R.K. 2000. Too much interference: injection of double stranded RNA has nonspecific effects in the zebrafish embryo. Dev. Biol. 224: 20–28.10.1006/dbio.2000.9761Search in Google Scholar
Okutsu T., Shikina S., Kanno M., Takeuchi Y. & Yoshizaki G. 2007. Production of trout offspring from triploid salmon parents. Science 317: 1517.10.1126/science.1145626Search in Google Scholar
Pacchiarini T., Olague E., Sarasquete C. & Cabrita E. 2014. Busulfan administration produces sublethal effects on somatic tissues and inhibits gametogenesis in Senegalese sole juveniles. Hist. Histopathol. 29: 619–628.Search in Google Scholar
Pacchiarini T., Cross I., Leite R.B., Gavaia P., Ortiz-Delgado J.B, Pousao-Ferreira P., Rebordinos L., Sarasquete C. & Cabrita E. 2013. Solea senegalensis vasa transcripts: molecular characterization, tissue distribution and developmental expression profiles. Reprod. Fertil. Dev. 25: 646–660.10.1071/RD11240Search in Google Scholar
Peruzzi, S. Chatain, B., Saillant E., Haffray P., Menu B. & Falguiere J.C. 2004. Production of meiotic gynogenetic and triploid sea bass, Dicentrarchus labrax L.: performances, maturation and carcass quality. Aquaculture 230: 41–64.10.1016/S0044-8486(03)00417-4Search in Google Scholar
Peruzzi S. & Chatain B. 2000. Pressure and cold shock induction of meiotic gynogenesis and triploidy in the European sea bass, Dicentrarchus labrax L.: relative efficiency of methods and parental variability. Aquaculture 189: 23–37.10.1016/S0044-8486(00)00355-0Search in Google Scholar
Peruzzi S., Rudolfsen G., Primicerio R., Frantzen M. & Kauric G. 2009. Milt characteristics of diploid and triploid Atlantic cod (Gadus morhua L.). Aquacult. Res. 40: 1160–1169.10.1111/j.1365-2109.2009.02212.xSearch in Google Scholar
Piferrer F., Beaumont A., Falguiere J.C., Flajšhans M., Haffray P. & Colombo L. 2009. Polyploid fish and shellfish: production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture 293: 125–156.10.1016/j.aquaculture.2009.04.036Search in Google Scholar
Piferrer F., Benfey T.J. & Donaldson E.M. 1994. Gonadal morphology of normal and sex reversed triploid and gynogenetic diploid Coho salmon (Oncorhynchus kisutch). J. Fish. Biol. 45: 541–553.10.1111/j.1095-8649.1994.tb00923.xSearch in Google Scholar
Piferrer F., Cal R.M., Alvarez-Blazquez B., Sanchez L. & Martinez P. 2000. Induction of triploidy in the turbot (Scophthalmus maximus). I. Ploidy determination and the effects of cold shocks. Aquaculture 188: 79–90.10.1016/S0044-8486(00)00306-9Search in Google Scholar
Piferrer F., Cal R. M., Gomez C., Bouza C. & Martinez P., 2003. Induction of triploidy in the turbot (Scophthalmus maximus) II. Effects of cold shock timing and induction of triploidy in a large volume of eggs. Aquaculture 220: 821–831.10.1016/S0044-8486(02)00535-5Search in Google Scholar
Presslauer C., Nagasawa K., Fernandes J.M. & Babiak I. 2012. Expression of vasa and nanos3 during primordial germ cell formation and migration in Atlantic cod (Gadus morhua L.). Theriogenology 78: 1262–1277.10.1016/j.theriogenology.2012.05.022Search in Google Scholar
Qiu C., Cheng B., Zhang Y., Huang R., Liao L., Li Y., Luo D., Hu W. & Wang Y. 2014. Efficient knockout of transplanted green fluorescent protein gene in medaka using TALENs. Mar. Biotechnol. 6: 674–683.10.1007/s10126-014-9584-xSearch in Google Scholar
Rahman M.A., Uehara T. & Lawrence J.M. 2005. Growth and heterosis of hybrids of two closely related species of Pacific sea urchins (Genus Echinometra) in Okinawa. Aquaculture 245: 121–133.10.1016/j.aquaculture.2004.11.049Search in Google Scholar
Ramasamy S., Wang H., Quach H.N. & Sampath K. 2006. Zebrafish Staufen1 and Staufen2 are required for the survival and migration of primordial germ cells. Dev. Biol. 292: 393–406.10.1016/j.ydbio.2006.01.014Search in Google Scholar
Raz E. & Reichman-Fried M. 2006. Attraction rules: germ cell migration in zebrafish. Curr. Opin. Gen. Dev. 4: 355–359.10.1016/j.gde.2006.06.007Search in Google Scholar
Rougeot C., Minet L., Prignon C., Vanderplasschen A., Detry B., Pastoret P.P. & Melard C. 2003. Induce triploidy by heat shock in Eurasian perch, Perca fluviatilis. Aquatic Living Resources 2: 90–94.10.1016/S0990-7440(03)00030-5Search in Google Scholar
Saffman E.E. & Lasko P. 1999. Germline development in vertebrates and invertebrates. Cell. Mol. Life Sci. 55: 1141–1163.10.1007/s000180050363Search in Google Scholar
Solar I.I., Donaldson E.M. & Hunter G.A. 1994. Induction of triploidy in rainbow trout (Salmo gairdneri Richardson) by heat shock, and investigation of early growth. Aquaculture 42: 57–67.10.1016/0044-8486(84)90313-2Search in Google Scholar
Saito T., Goto-Kazeto R., Arai K. & Yamaha E. 2008. Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation. Biol. Rep. 78: 159–166.10.1095/biolreprod.107.060038Search in Google Scholar PubMed
Sawatari E., Shikina S., Takeuchi T. & Yoshizaki G. 2007. A novel transforming growth factor-² superfamily member expressed in gonadal somatic cells enhances primordial germ cell and spermatogonial proliferation in rainbow trout (Oncorhynchus mykiss). Dev. Biol. 301: 266–275.10.1016/j.ydbio.2006.10.001Search in Google Scholar
Schafhauser-Smith D. & Benfey T.J. 2003. In vitro steroid production by triploid ovarian follicles. Gen. Comp. Endocrinol. 133: 279–286.10.1016/S0016-6480(03)00187-4Search in Google Scholar
Scheerer P.D. & Thorgaard G.H. 1983. Increased survival in salmonid hybrids by induced triploidy. Can. J. Fish. Aquatic Sci. 11: 2040–2044.10.1139/f83-235Search in Google Scholar
Schlueter P.J., Sang X., Duan C. & Wood A.W. 2007. Insulin-like growth factor receptor 1b is required for zebrafish primordial germ cell migration and survival. Dev. Biol. 305: 377–387.10.1016/j.ydbio.2007.02.015Search in Google Scholar PubMed PubMed Central
Schmid B. & Haass C. 2013. Genomic editing opens new avenues for zebrafish as a model for neurodegeneration. Neurochemistry 127: 461–470.10.1111/jnc.12460Search in Google Scholar PubMed
Seruggia D. & Montoliu L. 2014. The new CRISPR-Cas system: RNA-guided genome engineering to efficiently produce any desired genetic alteration in animals. Transgenic Res. 23: 707–716.10.1007/s11248-014-9823-ySearch in Google Scholar PubMed
Shepherd L.T., Beattie C.E. & Raible D.W. 2001. Functional analysis of zebra fish GNDF. Dev. Biol. 231: 420–435.10.1006/dbio.2000.0145Search in Google Scholar PubMed
Shimada A. & Takeda H. 2008. Production of a maternal-zygotic medaka mutant using hybrid sterility. Dev. Growth Differ. 50: 421–426.10.1111/j.1440-169X.2008.01051.xSearch in Google Scholar PubMed
Shinomiya A.I., Hamaguchi S. & Shibata N. 2001. Sexual differentiation of germ cell deficient gonads in the medaka, Oryzias latipes. J. Exp. Zool. 290: 402–410.10.1002/jez.1081Search in Google Scholar PubMed
Škugor A., Tveiten H., Krasnov A. & Andersen O. 2014. Knockdown of the germ cell factor Dead end induces multiple transcriptional changes in Atlantic cod (Gadus morhua) hatchlings. Anim. Reprod. Sci. 144: 129–137.10.1016/j.anireprosci.2013.12.010Search in Google Scholar PubMed
Slanchev K., Stebler J., de la Cueva-Mendez G. & Raz E. 2005. Development without germ cells: the role of the germ line in zebrafish sex differentiation. Proc. Natl. Acad. Sci. USA 102: 4074–4079.10.1073/pnas.0407475102Search in Google Scholar
Smith T.I.J. 1988. Aquaculture of striped bass and its hybrids in North America. Aquacult. Mag. 14: 40–49.Search in Google Scholar
Strüssmann C.A., Saito T. & Takashima F. 1998. Heat-induced germ cell deficiency in the teleosts Odontesthes bonariensis and Patagonina hatcheri. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 119: 637–644.10.1016/S1095-6433(97)00477-7Search in Google Scholar
Sui G., Soohoo C., Affar E.B., Gray F., Shi Y., Forrester W. & Shi Y. 2002. A DNA vector-based RNAi technology to suppress gene expression in mammalian cells. Proc. Natl. Acad. Sci. USA 99: 5515–5520.10.1073/pnas.082117599Search in Google Scholar
Summerton J. 1999. Morpholino antisense oligomers: the case for an RNAse-H independent structural type. Biochim. Biophys. Acta 1: 141–158.10.1016/S0167-4781(99)00150-5Search in Google Scholar
Summerton J.E. 2007. Morpholino, siRNA, and S-DNA compared: impact of structure and mechanism of action on offtarget effects and sequence specificity. Curr. Top. Med. Chem. 7: 651–660.10.2174/156802607780487740Search in Google Scholar
Takeuchi Y., Yoshizaki G., Kobayashi T. & Takeuchi T. 2002. Mass isolation of primordial germ cells from transgenic rainbow trout carrying the green fluorescent protein gene driven by the vasa gene promoter. Biol. Reprod. 67: 1087–1092.10.1095/biolreprod67.4.1087Search in Google Scholar
Tashiro F. 1972. Effects of irradiation 60Co γ ray on the maturation of rainbow trout. Bull. Jap. Soc. Sci. Fish. Niss. 38: 793–797.10.2331/suisan.38.793Search in Google Scholar
Taylor J.F., Sambraus F., Mota-Velasco J., Guy D.R., Hamilton A., Hunter D., Corrigan D. & Migaud H. 2013. Ploidy and family effects on Atlantic salmon (Salmo salar) growth, deformity and harvest quality during a full commercial production cycle. Aquaculture 410–411: 41–50.10.1016/j.aquaculture.2013.06.004Search in Google Scholar
Thorgaard G.H. 1983. Chromosome set manipulation and sex control in fish, pp. 405–434. In: Hoar W.H., Randall D.J. & Donaldson E.M. (eds), Fish Physiology. Academic Press, Belgium.10.1016/S1546-5098(08)60308-8Search in Google Scholar
Thorpe J.L., Doitsidou M., Ho S.Y., Raz E. & Farber S.A. 2004. Germ cell migration in zebrafish is dependent on HMGCoA reductase activity and prenylation. Dev. Cell. 6: 295–302.10.1016/S1534-5807(04)00032-2Search in Google Scholar
Tsunekawa N., Naito M., Sakai Y., Nishida T. & Noce T. 2000. Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127: 2741–2750.10.1242/dev.127.12.2741Search in Google Scholar
Um-E-Kalsoom S.M., Shahzadi T. & Barlas A. 2009. Growth performance and feed conversion ratio (FCR) in hybrid fish (Catla catla × Labeo rohita) fed on wheat bran, rice broken and blood meal. Pak. Vet. J. 29: 55–58.Search in Google Scholar
Underwood J.L., Hestand R.S., Thompson B.Z. 1986. Gonad regeneration in grass carp following bilateral gonadectomy. Progressive Fish Culturist 48: 54–56.10.1577/1548-8640(1986)48<54:GRIGCF>2.0.CO;2Search in Google Scholar
Uzbekova S., Chyb J., Ferrière F., Bailhache T., Prunet P., Alestrom P. & Breton B. 2000. Transgenic rainbow trout expressed sGnRH-antisense RNA under the control of sGnRH promoter of Atlantic salmon. J. Mol. Endocrinol. 3: 337–50.10.1677/jme.0.0250337Search in Google Scholar
Verdegem M.C.J., Hilbrands A.D. & Boon J.H. 1997. Influence of salinity and dietary composition on blood parameter values of hybrid red tilapia, Oreochromis niloticus × Oreochromis mossambicus. Aquacult. Res. 28: 453–459.10.1111/j.1365-2109.1997.tb01063.xSearch in Google Scholar
Wargelius A., Ellingsen S. & Fjose A. 1999. Double-stranded RNA induces specific developmental defects in zebrafish embryos. Biochem. Biophys. Res. Commun. 263: 156–161.10.1006/bbrc.1999.1343Search in Google Scholar
Weidinger G., Stebler J., Slanchev K., Dumstrei K., Wise C., Lovell-Badge R., Thisse C., Thisse B. & Raz E. 2003. Dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr. Biol. 13: 1429–1434.10.1016/S0960-9822(03)00537-2Search in Google Scholar
Weidinger G., Wolke U., Köprunner M., Thisse C., Thisse B. & Raz E. 2002. Regulation of zebrafish primordial germ cell migration by attraction towards an intermediate target. Development 129: 25–36.10.1242/dev.129.1.25Search in Google Scholar
Withler R.E., Beacham T.D., Solar I.I. & Donaldson E.M. 1995. Freshwater growth, smolting, and marine survival and growth of diploid and triploid coho salmon. (Oncorhynchus kisutch). Aquaculture 1-2: 91–107.10.1016/0044-8486(95)01036-XSearch in Google Scholar
Wohlfarth G.W. 1994. The unexploited potential of tilapia hybrids in aquaculture. Aquat. Fish. Manag. 25: 781–788.10.1111/j.1365-2109.1994.tb00743.xSearch in Google Scholar
Wong T.T. & Collodi P. 2013. Inducible sterilization of zebrafish by disruption of primordial germ cell migration. PLoS One 6: e68455.10.1371/journal.pone.0068455Search in Google Scholar
Wong T.T., Saito T., Crodian J. & Collodi P. 2011. Zebrafish germline chimeras produced by transplantation of ovarian germ cells into sterile host larvae. Biol. Reprod. 84: 1190–1197.10.1095/biolreprod.110.088427Search in Google Scholar PubMed PubMed Central
Wu X., Wang Z., Jiang J., Gao J., Wang J., Zhou X. & Zhang Q. 2014. Cloning, expression promoter analysis of vasa gene in Japanese flounder (Paralichthys olivaceus). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 167: 2014. 41–50.10.1016/j.cbpb.2013.06.004Search in Google Scholar PubMed
Xu H., Li M., Gui J. & Hong Y. 2010. Fish germ cells. Sci. China Life. Sci. 53: 435–446.10.1007/s11427-010-0058-8Search in Google Scholar PubMed
Xu H., Li Z., Li M., Wang L. & Hong Y. 2009. Boule is present in fish and bisexually expressed in adult and embryonic germ cells of medaka. PLoS One 6: e6097.10.1371/journal.pone.0006097Search in Google Scholar PubMed PubMed Central
Xu J., You F., Wu X., Zhang P., Lin Y., Jiang H. & Zheng C. 2008. Induction of triploidy in large yellow croacker Pseudosciaena crocea (Richardson, 1846): effects of pressure shocks and growth performance in the first rearing year. Aquacult. Res. 39: 1369–1376.10.1111/j.1365-2109.2008.02005.xSearch in Google Scholar
Yamaha E. Murakami M., Hada K., Otani S., Fujimoto T., Tanaka M., Sakao S., Kimura S., Sato S. & Arai K. 2003. Recovery of fertility in male hybrids of a cross between goldfish and common carp by transplantation of PGC (primordial germ cell)-containing graft. Genetica 119: 121–131.10.1023/A:1026061828744Search in Google Scholar
Yamaha E., Saito T., Goto-Kazeto R. & Arai K. 2007. Developmental biotechnology for aquaculture, with special reference to surrogate production in teleost fishes. J. Sea Res. 58: 8–22.10.1016/j.seares.2007.02.003Search in Google Scholar
Yoon C., Kawakami K. & Hopkins N. 1997. Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124: 3157–3166.10.1242/dev.124.16.3157Search in Google Scholar PubMed
Yoshizaki G., Fujinuma K., Iwasaki Y., Okutsu T., Shikina S., Yazawa R. & Takeuchi Y. 2010. Spermatogonial transplantation in fish: a novel method for the preservation of genetic resources. Comp. Biochem. Physiol. Part D Genomics Proteomics 6: 55–61.10.1016/j.cbd.2010.05.003Search in Google Scholar PubMed
Yoshizaki G., Okutsu T., Morita T., Terasawa M., Yazawa R. & Takeuchi Y. 2012. Biological characteristics of fish germ cells and their application to developmental biotechnology. Reprod. Domest. Anim. 47: 187–192.10.1111/j.1439-0531.2012.02074.xSearch in Google Scholar PubMed
Zajicek P., Goodwin A.E. & Weier T. 2011. Triploid grass carp: triploid induction, sterility, reversion, and certification. North Amer. J. Fish. Manag. 4: 614–618.10.1080/02755947.2011.608616Search in Google Scholar
Zhao Z., Cao Y., Li M. & Meng A. 2001. Double-stranded RNA injection produces nonspecific defects in zebrafish. Dev. Biol. 229: 215–223.10.1006/dbio.2000.9982Search in Google Scholar PubMed
- Abbreviations
- dnd
dead end
- dsRNA
double-stranded RNA
- GFP
green fluorescent protein
- GnRH
gonadotropin releasing hormone
- GSI
gonadosomatic index
- MOs
modified oligonucleotides
- PGCs
primordial germ cells
- qPCR
quantitative PCR
- siRNA
small interfering RNA
- Sdf1a
stromal-derived factor-1alpha.
©2016 Institute of Molecular Biology, Slovak Academy of Sciences
Articles in the same Issue
- Cellular and Molecular Biology
- Mitochondrial clock: moderating evolution of early eukaryotes in light of the Proterozoic oceans
- Cellular and Molecular Biology
- Induced sterility in fish and its potential and challenges for aquaculture and germ cell transplantation technology: a review
- Botany
- Human impact on sandy beach vegetation along the southeastern Adriatic coast
- Botany
- Temporal dynamics in the genetic structure of a natural population of Picea abies
- Botany
- Ecotypic adaptations in Bermuda grass (Cynodon dactylon) for altitudinal stress tolerance
- Botany
- Zinc sulfide nanoparticle mediated alterations in growth and anti-oxidant status of Brassica juncea
- Zoology
- Climatic conditions driving a part of changes in the biochemical composition in land snails: Insights from the endangered Codringtonia(Gastropoda: Pulmonata)
- Zoology
- New and little known ptyctimous mites (Acari: Oribatida) with a key to known species of Oribotritia from the Australasian Region
- Zoology
- Using radio telemetry to track ground beetles: Movement of Carabus ullrichii
- Zoology
- Trophic relations between adult water beetles from the Dytiscidae family and non-biting midges (Diptera: Chironomidae)
- Zoology
- Role of the invasive Chinese sleeper Perccottus glenii (Actinopterygii: Odontobutidae) in the distribution of fish parasites in Europe: New data and a review
- Zoology
- Translocations of tropical and subtropical marine fish species into the Mediterranean. A case study based on Siganus virgatus (Teleostei: Siganidae)
- Zoology
- Distribution, habitats and abundance of the herb field mouse (Apodemus uralensis) in Lithuania
Articles in the same Issue
- Cellular and Molecular Biology
- Mitochondrial clock: moderating evolution of early eukaryotes in light of the Proterozoic oceans
- Cellular and Molecular Biology
- Induced sterility in fish and its potential and challenges for aquaculture and germ cell transplantation technology: a review
- Botany
- Human impact on sandy beach vegetation along the southeastern Adriatic coast
- Botany
- Temporal dynamics in the genetic structure of a natural population of Picea abies
- Botany
- Ecotypic adaptations in Bermuda grass (Cynodon dactylon) for altitudinal stress tolerance
- Botany
- Zinc sulfide nanoparticle mediated alterations in growth and anti-oxidant status of Brassica juncea
- Zoology
- Climatic conditions driving a part of changes in the biochemical composition in land snails: Insights from the endangered Codringtonia(Gastropoda: Pulmonata)
- Zoology
- New and little known ptyctimous mites (Acari: Oribatida) with a key to known species of Oribotritia from the Australasian Region
- Zoology
- Using radio telemetry to track ground beetles: Movement of Carabus ullrichii
- Zoology
- Trophic relations between adult water beetles from the Dytiscidae family and non-biting midges (Diptera: Chironomidae)
- Zoology
- Role of the invasive Chinese sleeper Perccottus glenii (Actinopterygii: Odontobutidae) in the distribution of fish parasites in Europe: New data and a review
- Zoology
- Translocations of tropical and subtropical marine fish species into the Mediterranean. A case study based on Siganus virgatus (Teleostei: Siganidae)
- Zoology
- Distribution, habitats and abundance of the herb field mouse (Apodemus uralensis) in Lithuania