Abstract
Germ cells have drawn much attention as gamete precursors because of their exceptional potential for fundamental biological studies, as well as for being a potential alternative to gene resource banking for breeding and restocking purposes via surrogacy. Research has developed markers for germ cell identification, shedding light on their origin and specification mechanism. Then, pioneering studies focused on germ cell transplantation into the surrogate host with donor-derived gamete production have followed suit. The advent of transgenic technologies allowed the development of lines expressing green fluorescent protein (GFP) in their germ cells exclusively or the use of artificially synthesised mRNA conjugated with GFP to label and trace germ cells in vivo and facilitate studies on transplantation. The power of germ cell manipulation techniques was significantly enhanced by the development of a wide range of cryopreservation methods; with these approaches, valuable genetic material can be cryopreserved even during the blastula stage, as well as harvested from an adult specimen. In turn, the germ cells in the cryogenic storage can be recovered by transplantation in the surrogate host, producing donor-derived gametes after maturation. The aim of this chapter is to provide basic knowledge about a relatively novel biotechnological approach in fish reproduction and summarise performed studies on germ cell cryopreservation.
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References
Anil S, Rawson D, Zhang T (2018) Development of molecular markers for zebrafish (Danio rerio) ovarian follicle growth assessment following in-vitro culture in cryopreservation studies. Cryobiology 83:75–83. https://doi.org/10.1016/j.cryobiol.2018.05.004
Bar I, Smith A, Bubner E, Yoshizaki G, Takeuchi Y, Yazawa R, Chen BN, Cummins S, Elizur A (2016) Assessment of yellowtail kingfish (Seriola lalandi) as a surrogate host for the production of southern bluefin tuna (Thunnus maccoyii) seed via spermatogonial germ cell transplantation. Reprod Fertil Dev 28:2051. https://doi.org/10.1071/RD15136
Blaser H, Eisenbeiss S, Neumann M, Reichman-Fried M, Thisse B, Thisse C, Raz E (2005) Transition from non-motile behaviour to directed migration during early PGC development in zebrafish. J Cell Sci 118:4027–4038. https://doi.org/10.1242/jcs.02522
Braat A, Speksnijder JE, Zivkovic D (1999) Germ line development in fishes. Int J Dev Biol 43:745–760
Cabrita E, Sarasquete C, Martínez-Páramo S, Robles V, Beirão J, Pérez-Cerezales S, Herráez MP (2010) Cryopreservation of fish sperm: applications and perspectives. J Appl Ichthyol 26:623–635. https://doi.org/10.1111/j.1439-0426.2010.01556.x
Carmichael C, Westerfield M, Varga ZM (2009) Cryopreservation and in vitro fertilization at the zebrafish international resource center. Methods Mol Biol (Clifton, NJ) 546:45–65. https://doi.org/10.1007/978-1-60327-977-2_4
de Mello F, Garcia JS, Godoy LC, Depincé A, Labbé C, Streit DP Jr (2017) The effect of cryoprotectant agents on DNA methylation patterns and progeny development in the spermatozoa of Colossoma macropomum. Gen Comp Endocrinol 245:94–101. https://doi.org/10.1016/j.ygcen.2016.06.003
de Siqueira-Silva DH, dos Santos Silva AP, Ninhaus-Silveira A, Veríssimo-Silveira R (2015) The effects of temperature and busulfan (Myleran) on the yellowtail tetra Astyanax altiparanae (Pisces, Characiformes) spermatogenesis. Theriogenology 84:1033–1042. https://doi.org/10.1016/j.theriogenology.2015.06.004
Doitsidou M, Reichman-Fried M, Stebler J, Köprunner M, Dörries J, Meyer D, Esguerra CV, Leung T, Raz E (2002) Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111:647–659. https://doi.org/10.1016/S0092-8674(02)01135-2
Dosch R (2015) Next generation mothers: maternal control of germline development in zebrafish. Crit Rev Biochem Mol Biol 50:54–68. https://doi.org/10.3109/10409238.2014.985816
Franěk R, Marinović Z, Lujić J, Urbányi B, Fučíková M, Kašpar V, Pšenička M, Horváth Á (2019a) Cryopreservation and transplantation of common carp spermatogonia. PLoS One 14:e0205481. https://doi.org/10.1371/journal.pone.0205481
Franěk R, Tichopád T, Fučíková M, Steinbach C, Pšenička M (2019b) Production and use of triploid zebrafish for surrogate reproduction. Theriogenology 140:33–43. https://doi.org/10.1016/j.theriogenology.2019.08.016
Franěk R, Tichopád T, Steinbach C, Xie X, Lujić J, Marinović Z, Horváth Á, Kašpar V, Pšenička M, Lujić J, Horváth Á, Pšenička M (2019c) Preservation of female genetic resources of common carp through oogonial stem cell manipulation. Cryobiology 87:78–85. https://doi.org/10.1016/j.cryobiol.2019.01.016
Fujimoto T, Saito T, Sakao S, Arai K, Yamaha E (2010) Developmental potential of embryonic cells in a nucleocytoplasmic hybrid formed using a goldfish haploid nucleus and loach egg cytoplasm. Int J Dev Biol 54:827–835. https://doi.org/10.1387/ijdb.092896tf
Godoy LC, Streit DP, Zampolla T, Bos-Mikich A, Zhang T (2013) A study on the vitrification of stage III zebrafish (Danio rerio) ovarian follicles. Cryobiology 67:347–354. https://doi.org/10.1016/j.cryobiol.2013.10.002
Goto R, Saito T (2019) A state-of-the-art review of surrogate propagation in fish. Theriogenology 133:216–227. https://doi.org/10.1016/j.theriogenology.2019.03.032
Goto R, Saito T, Takeda T, Fujimoto T, Takagi M, Arai K, Yamaha E (2012) Germ cells are not the primary factor for sexual fate determination in goldfish. Dev Biol 370:98–109. https://doi.org/10.1016/j.ydbio.2012.07.010
Guan M, Rawson DM, Zhang T (2008) Cryopreservation of zebrafish (Danio rerio) oocytes using improved controlled slow cooling protocols. Cryobiology 56:204–208. https://doi.org/10.1016/j.cryobiol.2008.03.001
Guan M, Rawson DM, Zhang T (2010) Cryopreservation of zebrafish (Danio rerio) oocytes by vitrification. Cryo-Letters 31:230–238
Güralp H, Pocherniaieva K, Blecha M, Policar T, Pšenička M, Saito T (2016) Early embryonic development in pikeperch (Sander lucioperca) related to micromanipulation. Czech J Anim Sci 61:273–280. https://doi.org/10.17221/35/2015-CJAS
Güralp H, Pocherniaieva K, Blecha M, Policar T, Pšenička M, Saito T (2017) Migration of primordial germ cells during late embryogenesis of pikeperch Sander lucioperca relative to blastomere transplantation. Czech J Anim Sci 62:121–129. https://doi.org/10.17221/40/2016-CJAS
Hagedorn MM, Daly JP, Carter VL, Cole KS, Jaafar Z, Lager CVA, Parenti LR (2018) Cryopreservation of fish spermatogonial cells: the future of natural history collections. Sci Rep 8:1–11. https://doi.org/10.1038/s41598-018-24269-3
Hamasaki M, Takeuchi Y, Yazawa R, Yoshikawa S, Kadomura K, Yamada T, Miyaki K, Kikuchi K, Yoshizaki G (2017) Production of Tiger puffer Takifugu rubripes offspring from triploid grass puffer Takifugu niphobles parents. Mar Biotechnol 19:579–591. https://doi.org/10.1007/s10126-017-9777-1
Higaki S, Mochizuki K, Baba H, Akashi Y, Yamaha E, Katagiri S, Takahashi Y (2009) Feasibility of cryopreservation of zebrafish (Danio rerio) primordial germ cells by whole embryo freezing. Jpn J Vet Res 57:119–128
Higaki S, Todo T, Teshima R, Tooyama I, Fujioka Y, Sakai N, Takada T (2018) Cryopreservation of male and female gonial cells by vitrification in the critically endangered cyprinid honmoroko Gnathopogon caerulescens. Fish Physiol Biochem 44:503–513. https://doi.org/10.1007/s10695-017-0449-x
Inoue D, Fujimoto T, Kawakami Y, Yasui GS, Yamaha E, Arai K (2012) Vitrification of primordial germ cells using whole embryos for gene-banking in loach, Misgurnus anguillicaudatus. J Appl Ichthyol 28:919–924. https://doi.org/10.1111/jai.12058
IUCN (2016) The IUCN red list of threatened species. http://www.iucnredlist.org. Accessed 31 Jan 2017
Kawakami Y, Goto-Kazeto R, Saito T, Fujimoto T, Higaki S, Takahashi Y, Arai K, Yamaha E (2010) Generation of germ-line chimera zebrafish using primordial germ cells isolated from cultured blastomeres and cryopreserved embryoids. Int J Dev Biol 54:1491–1499. https://doi.org/10.1387/ijdb.093059yk
Kawakami Y, Ishihara M, Saito T, Fujimoto T, Adachi S, Arai K, Yamaha E (2012a) Cryopreservation of green fluorescent protein (GFP)-labeled primordial germ cells with GFP fused to the 3′ untranslated region of the nanos gene by vitrification of Japanese eel (Anguilla japonica) somite stage embryos1. J Anim Sci 90:4256–4265. https://doi.org/10.2527/jas.2011-4884
Kawakami Y, Saito T, Fujimoto T, Goto-Kazeto R, Takahashi E, Adachi S, Arai K, Yamaha E (2012b) Technical note: viability and motility of vitrified/thawed primordial germ cell isolated from common carp (Cyprinus carpio) somite embryos. J Anim Sci 90:495–500. https://doi.org/10.2527/jas.2011-4329
Khosla K, Wang Y, Hagedorn M, Qin Z, Bischof J (2017) Gold nanorod induced warming of embryos from the cryogenic state enhances viability. ACS Nano 11:7869–7878. https://doi.org/10.1021/acsnano.7b02216
Knaut H, Pelegri F, Bohmann K, Schwarz H, Nüsslein-Volhard C (2000) Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J Cell Biol 149:875–888. https://doi.org/10.1083/jcb.149.4.875
Kobayashi T, Yoshizaki G, Takeuchi Y, Takeuchi T (2004) Isolation of highly pure and viable primordial germ cells from rainbow trout by GFP-dependent flow cytometry. Mol Reprod Dev 67:91–100. https://doi.org/10.1002/mrd.20003
Kobayashi T, Takeuchi Y, Takeuchi T, Yoshizaki G (2007) Generation of viable fish from cryopreserved primordial germ cells. Mol Reprod Dev 74:207–213. https://doi.org/10.1002/mrd
Komen H, Thorgaard GH (2007) Androgenesis, gynogenesis and the production of clones in fishes: a review. Aquaculture 269:150–173. https://doi.org/10.1016/j.aquaculture.2007.05.009
Kunwar PS, Lehmann R (2006) Germ-cell attraction. Dev Biol 421:226–227
Lacerda S, Batlouni S, Silva S, Homem C, França L (2006) Germ cells transplantation in fish: the Nile-tilapia model. Anim Reprod 3:146–159
Lacerda SMSN, Batlouni SR, Costa GMJ, Segatelli TM, Quirino BR, Queiroz BM, Kalapothakis E, França LR (2010) A new and fast technique to generate offspring after germ cells transplantation in adult fish: the nile tilapia (Oreochromis niloticus) model. PLoS One 5:1–9. https://doi.org/10.1371/journal.pone.0010740
Lee S, Yoshizaki G (2016) Successful cryopreservation of spermatogonia in critically endangered Manchurian trout (Brachymystax lenok). Cryobiology 72:165–168. https://doi.org/10.1016/j.cryobiol.2016.01.004
Lee S, Iwasaki Y, Shikina S, Yoshizaki G (2013) Generation of functional eggs and sperm from cryopreserved whole testes. PNAS 110:1640–1645. https://doi.org/10.1073/pnas.1218468110
Lee S, Iwasaki Y, Yoshizaki G (2016a) Long-term (5 years) cryopreserved spermatogonia have high capacity to generate functional gametes via interspecies transplantation in salmonids. Cryobiology 73:5–9. https://doi.org/10.1016/j.cryobiol.2016.08.001
Lee S, Katayama N, Yoshizaki G (2016b) Generation of juvenile rainbow trout derived from cryopreserved whole ovaries by intraperitoneal transplantation of ovarian germ cells. Biochem Biophys Res Commun 478:1478–1483. https://doi.org/10.1016/j.bbrc.2016.08.156
Li Q, Fujii W, Naito K, Yoshizaki G (2017) Application of dead end-knockout zebrafish as recipients of germ cell transplantation. Mol Reprod Dev 84(10):1100–1111. https://doi.org/10.1002/mrd.22870
Lin S, Long W, Chen J, Hopkins N (1992) Production of germ-line chimeras in zebrafish by cell transplants from genetically pigmented to albino embryos. Proc Natl Acad Sci 89:4519–4523. https://doi.org/10.1073/pnas.89.10.4519
Linhartová Z, Rodina M, Guralp H, Gazo I, Saito T, Pšenička M (2014) Isolation and cryopreservation of early stages of germ cells of tench (Tinca tinca). CJAS 59:381–390
Lubzens E, Young G, Bobe J, Cerdà J (2010) Oogenesis in teleosts: how fish eggs are formed. Gen Comp Endocrinol 165:367–389. https://doi.org/10.1016/j.ygcen.2009.05.022
Lujić J, Marinović Z, Sušnik Bajec S, Djurdjevič I, Kása E, Urbányi B, Horváth Á (2017) First successful vitrification of salmonid ovarian tissue. Cryobiology 76:154–157. https://doi.org/10.1016/j.cryobiol.2017.04.005
Majhi SK, Hattori RS, Rahman SM, Strüssmann CA (2014) Surrogate production of eggs and sperm by intrapapillary transplantation of germ cells in cytoablated adult fish. PLoS One 9(4):e95294. https://doi.org/10.1371/journal.pone.0095294
Marinović Z, Lujić J, Kása E, Bernáth G, Urbányi B, Horváth Á (2016) Cryosurvival of isolated testicular cells and testicular tissue of tench Tinca tinca and goldfish Carassius auratus following slow-rate freezing. Gen Comp Endocrinol. https://doi.org/10.1016/j.ygcen.2016.07.005
Marinović Z, Lujić J, Kása E, Csenki Z, Urbányi B, Horváth Á (2018) Cryopreservation of zebrafish spermatogonia by whole testes needle immersed ultra-rapid cooling. J Vis Exp 2–7. https://doi.org/10.3791/56118
Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Phys 247(3 Pt 1):C125–C142. https://doi.org/10.1152/ajpcell.1984.247.3.C125
McLaren A (2003) Primordial germ cells in the mouse. Dev Biol 262:1–15. https://doi.org/10.1016/S0012-1606(03)00214-8
Nóbrega RH, Greebe CD, van de Kant H, Bogerd J, de França LR, Schulz RW (2010) Spermatogonial stem cell niche and spermatogonial stem cell transplantation in zebrafish. PLoS One 5:1–16. https://doi.org/10.1371/journal.pone.0012808
Octavera A, Yoshizaki G (2019) Production of donor-derived offspring by allogeneic transplantation of spermatogonia in Chinese rosy bitterling. Biol Reprod 100:1108–1117. https://doi.org/10.1093/biolre/ioy236
Okutsu T, Suzuki K, Takeuchi Y, Takeuchi T, Yoshizaki G (2006) Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proc Natl Acad Sci U S A 103:2725–2729. https://doi.org/10.1073/pnas.0509218103
Pradhan A, Olsson P-E (2014) Juvenile ovary to testis transition in zebrafish involves inhibition of Ptges1. Biol Reprod 91:1–15. https://doi.org/10.1095/biolreprod.114.119016
Pšenička M, Saito T, Linhartová Z, Gazo I (2015) Isolation and transplantation of sturgeon early-stage germ cells. Theriogenology 83:1085–1092. https://doi.org/10.1016/j.theriogenology.2014.12.010
Pšenička M, Saito T, Rodina M, Dzyuba B (2016) Cryopreservation of early stage Siberian sturgeon Acipenser baerii germ cells, comparison of whole tissue and dissociated cells. Cryobiology 72:199–122. https://doi.org/10.1016/j.cryobiol.2016.02.005
Raz E (2003) Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet 4:690–700. https://doi.org/10.1038/nrg1154
Raz E, Reichman-Fried M (2006) Attraction rules: germ cell migration in zebrafish. Curr Opin Genet Dev 16:355–359. https://doi.org/10.1016/j.gde.2006.06.007
Riemer S, Bontems F, Krishnakumar P, Gömann J, Dosch R (2015) A functional Bucky ball-GFP transgene visualizes germ plasm in living zebrafish. Gene Expr Patterns 18:44–52. https://doi.org/10.1016/j.gep.2015.05.003
Riesco MF, Robles V (2013) Cryopreservation causes genetic and epigenetic changes in zebrafish genital ridges. PLoS One 8:e67614. https://doi.org/10.1371/journal.pone.0067614
Riesco MF, Martínez-Pastor F, Chereguini O, Robles V (2012) Evaluation of zebrafish (Danio rerio) PGCs viability and DNA damage using different cryopreservation protocols. Theriogenology 77:122–130.e2. https://doi.org/10.1016/j.theriogenology.2011.07.024
Riesco MF, Valcarce DG, Alfonso J, Herráez MP, Robles V (2014) In vitro generation of zebrafish PGC-like cells. Biol Reprod 91(5):114. https://doi.org/10.1095/biolreprod.114.121491
Robles V, Cabrita E, Paz Herráez M (2009) Germplasm cryobanking in zebrafish and other aquarium model species. Zebrafish 6:281–293. https://doi.org/10.1089/zeb.2009.0592
Robles V, Riesco MF, Psenicka M, Saito T, Valcarce DG, Cabrita E, Herráez P (2017) Biology of teleost primordial germ cells (PGCs) and spermatogonia: biotechnological applications. Aquaculture 472:4–20. https://doi.org/10.1016/j.aquaculture.2016.03.004
Saito T, Fujimoto T, Maegawa S, Inoue K, Tanaka M, Arai K, Yamaha E (2006) Visualization of primordial germ cells in vivo using GFP-nos1 3′UTR mRNA. Int J Dev Biol 50:691–700. https://doi.org/10.1387/ijdb.062143ts
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 Reprod 78:159–166. https://doi.org/10.1095/biolreprod.107.060038
Saito T, Goto-Kazeto R, Fujimoto T, Kawakami Y, Arai K, Yamaha E (2010) Inter-species transplantation and migration of primordial germ cells in cyprinid fish. Int J Dev Biol 54:1479–1484. https://doi.org/10.1387/ijdb.103111ts
Saito T, Goto-Kazeto R, Kawakami Y, Nomura K, Tanaka H, Adachi S, Arai K, Yamaha E (2011) The mechanism for primordial germ-cell migration is conserved between Japanese eel and zebrafish. PLoS One 6(9):e24460. https://doi.org/10.1371/journal.pone.0024460
Saito T, Pšeničkka M, Goto R, Adachi S, Inoue K, Arai K, Yamaha E (2014) The origin and migration of primordial germ cells in sturgeons. PLoS One 9(2):e86861. https://doi.org/10.1371/journal.pone.0086861
Schulz RW, Renato L, França D, Lareyre J, Legac F, Chiarini-garcia H, Henrique R, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411. https://doi.org/10.1016/j.ygcen.2009.02.013
Seki S, Kusano K, Lee S, Iwasaki Y, Yagisawa M, Ishida M, Hiratsuka T, Sasado T, Naruse K, Yoshizaki G (2017) Production of the medaka derived from vitrified whole testes by germ cell transplantation. Sci Rep 7:43185. https://doi.org/10.1038/srep43185
Shikina S, Nagasawa K, Hayashi M, Furuya M, Yoshizaki G (2013) Short-term in vitro culturing improves transplantability of type A spermatogonia in rainbow trout (Oncorhynchus mykiss). Mol Reprod Dev 773:n/a. https://doi.org/10.1002/mrd.22208
Starz-Gaiano M, Lehmann R (2001) Moving towards the next generation. Mech Dev 105:5–18. https://doi.org/10.1016/S0925-4773(01)00392-6
Strüssmann CA, Nakamura M (2002) Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes. Fish Physiol Biochem 26:13–29. https://doi.org/10.1023/A:1023343023556
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. https://doi.org/10.1095/biolreprod.102.005660
Takeuchi Y, Yoshizaki G, Takeuchi T (2003) Generation of live fry from intraperitoneally transplanted primordial germ cells in rainbow trout. Biol Reprod 69:1142–1149. https://doi.org/10.1095/biolreprod.103.017624
Takeuchi Y, Higuchi K, Yatabe T, Miwa M, Yoshizaki G (2009) Development of spermatogonial cell transplantation in Nibe croaker, Nibea mitsukurii (Perciformes, Sciaenidae). Biol Reprod 81:1055–1063. https://doi.org/10.1095/biolreprod.109.077701
Tsai S, Rawson DM, Zhang T (2010) Development of in vitro culture method for early stage zebrafish (Danio rerio) ovarian follicles for use in cryopreservation studies. Theriogenology 74:290–303. https://doi.org/10.1016/j.theriogenology.2010.02.013
Weidinger G, Wolke U, Köprunner M, Klinger M, Raz E (1999) Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells. Development 126:5295–5307
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. https://doi.org/10.1095/biolreprod.110.088427
Xu HY, Li MY, Gui JF, Hong YH (2010) Fish germ cells. Sci China Life Sci 53:435–446. https://doi.org/10.1007/s11427-010-0058-8
Yamaha E, Kazama-Wakabayashi M, Otani S, Fujimoto T, Arai K (2001) Germ-line chimera by lower-part blastoderm transplantation between diploid goldfish and triploid crucian carp. Genetica 111:227–236. https://doi.org/10.1023/A:1013780423986
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
Yazawa R, Takeuchi Y, Higuchi K, Yoshizaki G (2010) Chub mackerel gonads support colonization, survival, and proliferation of intraperitoneally transplanted xenogenic germ cells. Biol Reprod 82:896–904
Yazawa R, Takeuchi Y, Morita T, Ishida M, Yoshizaki G (2013) The Pacific bluefin tuna (Thunnus orientalis) dead end gene is suitable as a specific molecular marker of type A spermatogonia. Mol Reprod Dev 80:871–880. https://doi.org/10.1002/mrd.22224
Ye H, Li C-J, Yue H-M, Du H, Yang X-G, Yoshino T, Hayashida T, Takeuchi Y, Wei Q-W (2017) Establishment of intraperitoneal germ cell transplantation for critically endangered Chinese sturgeon Acipenser sinensis. Theriogenology 94:37–47. https://doi.org/10.1016/j.theriogenology.2017.02.009
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 (Cambridge, England) 124:3157–3165
Yoshikawa H, Takeuchi Y, Ino Y, Wang J, Iwata G, Kabeya N, Yazawa R, Yoshizaki G (2017) Efficient production of donor-derived gametes from triploid recipients following intra-peritoneal germ cell transplantation into a marine teleost, Nibe croaker (Nibea mitsukurii). Aquaculture 478:35–47. https://doi.org/10.1016/j.aquaculture.2016.05.011
Yoshikawa H, Xu D, Ino Y, Yoshino T, Hayashida T, Wang J, Yazawa R, Yoshizaki G, Takeuchi Y (2018) Hybrid sterility in fish caused by mitotic arrest of primordial germ cells. Genetics 209:507–521. https://doi.org/10.1534/genetics.118.300777
Yoshizaki G, Lee S (2018) Production of live fish derived from frozen germ cells via germ cell transplantation. Stem Cell Res 29:103–110. https://doi.org/10.1016/j.scr.2018.03.015
Yoshizaki G, Ichikawa M, Hayashi M, Iwasaki Y, Miwa M, Shikina S, Okutsu T (2010) Sexual plasticity of ovarian germ cells in rainbow trout. Development 137:1227–1230. https://doi.org/10.1242/dev.044982
Yoshizaki G, Takashiba K, Shimamori S, Fujinuma K, Shikina S, Okutsu T, Kume S, Hayashi M (2016) Production of germ cell-deficient salmonids by dead end gene knockdown, and their use as recipients for germ cell transplantation. Mol Reprod Dev 83:298–311. https://doi.org/10.1002/mrd.22625
Yoshizaki G, Yazawa R (2019) Application of surrogate broodstock technology in aquaculture. Fish Sci 85:429–437. https://doi.org/10.1007/s12562-019-01299-y
Zhu ZY, Sun YH (2000) Embryonic and genetic manipulation in fish. Cell Res 10:17–27. https://doi.org/10.1038/sj.cr.7290032
Zimmermann J, Hajibabaei M, Blackburn DC, Hanken J, Cantin E, Posfai J, Evans TC (2008) DNA damage in preserved specimens and tissue samples: a molecular assessment. Front Zool 5:18. https://doi.org/10.1186/1742-9994-5-18
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The study was financially supported by the Ministry of Education, Youth and Sports of the Czech Republic, projects CENAKVA (LM2018099), Biodiversity (CZ.02.1.01/0.0/0.0/16_025/0007370), and NAZV QK1910428.
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Franěk, R., Pšenička, M. (2020). Cryopreservation of Germ Stem Cells in Fish. In: Betsy, J., Kumar, S. (eds) Cryopreservation of Fish Gametes. Springer, Singapore. https://doi.org/10.1007/978-981-15-4025-7_12
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