Characterization of potential spermatogonia biomarker genes in the European eel (Anguilla anguilla).
Dnd1
Nanos2
Vasa
Fish
Gene expression
Testis
Journal
Fish physiology and biochemistry
ISSN: 1573-5168
Titre abrégé: Fish Physiol Biochem
Pays: Netherlands
ID NLM: 100955049
Informations de publication
Date de publication:
19 Apr 2024
19 Apr 2024
Historique:
received:
20
09
2023
accepted:
22
03
2024
medline:
19
4
2024
pubmed:
19
4
2024
entrez:
19
4
2024
Statut:
aheadofprint
Résumé
Identification of specific molecular markers for spermatogonial stem cells in teleost is crucial for enhancing the efficacy of reproductive biotechnologies in aquaculture, such as transplantation and surrogate production in fishes. Since it is not yet possible to distinguish spermatogonial stem cells of European eel (Anguilla anguilla) using specific molecular markers, we isolated spermatogonial cells from immature European eels to find these potential markers. We attempted this by studying three candidate genes: vasa, nanos2, and dnd1. Two vasa (vasa1 and vasa2) genes, nanos2, and dnd1 were identified, characterized, and studied in the muscle, testis, and isolated spermatogonia. Our results showed that vasa1 and vasa2 had the highest levels of expression when measured by qPCR. In situ hybridization and immunochemistry assays showed that the four genes were localized explicitly in type A spermatogonia. However, vasa1 and vasa2 exhibited stronger signals in the immature testicular tissue than the other two potential markers. According to this, vasa1 and vasa2 were found to be the most effective markers for spermatogonial cells in the European eel.
Identifiants
pubmed: 38639895
doi: 10.1007/s10695-024-01338-1
pii: 10.1007/s10695-024-01338-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Ministerio de Ciencia e Innovación y Universidades
ID : Project EELGONIA; RTI2018-096413-B-I00
Organisme : Ministerio de Ciencia e Innovación y Universidades
ID : Project EELGONIA; RTI2018-096413-B-I00
Organisme : Ministerio de Ciencia e Innovación y Universidades
ID : Project EELGONIA; RTI2018-096413-B-I00
Organisme : Ministerio de Ciencia e Innovación y Universidades
ID : Project EELGONIA; RTI2018-096413-B-I00
Organisme : Ministerio de Ciencia e Innovación y Universidades
ID : Project EELGONIA; RTI2018-096413-B-I00
Organisme : Universitat Politècnica de València
ID : PAID-01-20
Organisme : Universitat Politècnica de València
ID : PAID-01-20
Organisme : European Union NextGenerationEU
ID : THINKINAZUL/2021/012
Organisme : European Union NextGenerationEU
ID : THINKINAZUL/2021/012
Organisme : European Union NextGenerationEU
ID : RYC2021-031558-I
Organisme : European Union NextGenerationEU
ID : THINKINAZUL/2021/012
Organisme : European Union NextGenerationEU
ID : THINKINAZUL/2021/012
Organisme : European Union NextGenerationEU
ID : THINKINAZUL/2021/012
Organisme : Generalitat Valenciana
ID : THINKINAZUL/2021/012
Organisme : Generalitat Valenciana
ID : GRISOLIAP/2020/063
Organisme : Generalitat Valenciana
ID : THINKINAZUL/2021/012
Organisme : Generalitat Valenciana
ID : GRISOLIAP/2020/063
Organisme : Generalitat Valenciana
ID : THINKINAZUL/2021/012
Organisme : Ministry of Innovation and Technology Hungary
ID : TKP2020-NKA-16
Organisme : Ministry of Innovation and Technology Hungary
ID : TKP2020-NKA-16
Organisme : Ministry of Innovation and Technology Hungary
ID : TKP2020-NKA-16
Organisme : European Union's Horizon 2020 Marie Skłodowska-Curie
ID : Nº 642893 (IMPRESS)
Organisme : European Union's Horizon 2020 Marie Skłodowska-Curie
ID : Nº 642893 (IMPRESS)
Organisme : European Union's Horizon 2020 Marie Skłodowska-Curie
ID : Nº 642893 (IMPRESS)
Organisme : European Union's Horizon 2020 Marie Skłodowska-Curie
ID : Nº 642893 (IMPRESS)
Organisme : European Union's Horizon 2020 Marie Skłodowska-Curie
ID : Nº 642893 (IMPRESS)
Organisme : European Union's Horizon 2020 Marie Skłodowska-Curie
ID : Nº 642893 (IMPRESS)
Organisme : Ministry of Education, Youth and Sports of the Czech Republic
ID : Project CENAKVA (LM2018099)
Organisme : Biodiversity
ID : CZ.02.1.01/0.0/0.0/16_025/0007370
Organisme : Czech Science Foundation
ID : 22-31141J
Organisme : Ministerio de Ciencia e Innovación
ID : RYC2021-031558-I
Organisme : Ministerio de Ciencia e Innovación
ID : RYC2021-031558-I
Informations de copyright
© 2024. The Author(s).
Références
Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105. https://doi.org/10.1093/bioinformatics/bti263
doi: 10.1093/bioinformatics/bti263
pubmed: 15647292
Aoki Y, Nakamura S, Ishikawa Y, Tanaka M (2009) Expression and syntenic analyses of four nanos genes in medaka. Zool Sci 6:112–118. https://doi.org/10.2108/zsj.26.112
doi: 10.2108/zsj.26.112
Asturiano JF (2020) Improvements on the reproductive control of the European eel. In: Yoshida M, Asturiano JF (eds) Reproduction in aquatic animals: from basic biology to aquaculture technology. Springer Singapore, Singapore, p 293–320
Baloch AR, Franěk R, Tichopád T, Fučíková M, Rodina M, Pšenička M (2019) Dnd1 knockout in sturgeons by CRISPR/Cas9 generates germ cell free host for surrogate production. Animals 9:74. https://doi.org/10.3390/ani9040174
doi: 10.3390/ani9040174
Bankhead P, Loughrey MB, Fernández JA, Dombrowski Y, McArt DG, Dunne PD, McQuaid S, Gray RT, Murray LJ, Coleman HG, James JA, Salto-Tellez M, Hamilton PW (2017) QuPath: Open source software for digital pathology image analysis. Sci Rep 7:1–7. https://doi.org/10.1038/s41598-017-17204-5
doi: 10.1038/s41598-017-17204-5
Beer RL, Draper BW (2013) Nanos3 maintains germline stem cells and expression of the conserved germline stem cell gene nanos2 in the zebrafish ovary. Dev Biol 374:308–318. https://doi.org/10.1016/j.ydbio.2012.12.003
doi: 10.1016/j.ydbio.2012.12.003
pubmed: 23228893
Begum S, Gnanasree SM, Anusha N, Senthilkumaran B (2022) Germ cell markers in fishes – a review. Aquaculture and Fisheries 7:540–552. https://doi.org/10.1016/j.aaf.2022.03.015
doi: 10.1016/j.aaf.2022.03.015
Bellaiche J, Lareyre JJ, Cauty C, Yano A, Allemand I, Le Gac F (2014) Spermatogonial stem cell quest: nanos2, marker of a subpopulation of undifferentiated A spermatogonia in trout testis. Biol Reprod 79:1–14. https://doi.org/10.1095/biolreprod.113.116392
doi: 10.1095/biolreprod.113.116392
Blázquez M, González A, Mylonas CC, Piferrer F (2011) Cloning and sequence analysis of vasa homolog in the European sesa bass (Dicentrarchus labrax): tissue distribution and mRNA expression levels during early development and sex differentiation. Gen Com Endocrinol 170:322–333. https://doi.org/10.1016/j.ygcen.2010.10.007
doi: 10.1016/j.ygcen.2010.10.007
Booncherd K, Sreebun S, Pasomboon P, Boonanuntanasarn S (2024) Effects of CRISPR/Cas9-mediated dnd1 knockout impairs gonadal development in striped catfish. Animal 18. https://doi.org/10.1016/j.animal.2023.101039
Bosseboeuf A, Gautier A, Auvray P, Mazan S, Sourdaine P (2014) Characterization of spermatogonial markers in the mature testis of the dogfish (Scyliorhinus canicula L.). Reproduction 147:125–139. https://doi.org/10.1530/REP-13-0316
doi: 10.1530/REP-13-0316
pubmed: 24123129
Burgerhout E, Lokman PM, van den Thillart GEEJM, Dirks RP (2019) The time-keeping hormone melatonin: a possible key cue for puberty in freshwater eels (Anguilla spp.). Rev Fish Biol Fisheries 29:1–21. https://doi.org/10.1007/s11160-018-9540-3
doi: 10.1007/s11160-018-9540-3
Cao M, Yang Y, Xu H, Duan J, Cheng N, Wang J, Hu W, Zhao H (2012) Germ cell specific expression of Vasa in rare minnow, Gobiocypris rarus. Comp Biochem Physiol A 162:163–170. https://doi.org/10.1016/j.cbpa.2012.02.007
doi: 10.1016/j.cbpa.2012.02.007
Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP (2000) The human vasa gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci USA 97(9585):9590. https://doi.org/10.1073/pnas.160274797
doi: 10.1073/pnas.160274797
Dekker W (2002) Monitoring of glass eel recruitment. Netherlands: Institute of Fisheries Research, report C007/02-WD
Draper BW (2017) Identification of germ-line stem cells in zebrafish. Methods Mol Biol 1463:103–113. https://doi.org/10.1007/978-1-4939-4017-2_8
doi: 10.1007/978-1-4939-4017-2_8
pubmed: 27734351
Duan J, Feng G, Chang P, Zhang X, Zhou Q, Zhong X, Qi C, Xie S, Zhao H (2015) Germ cell-specific expression of dead end (dnd) in rare minnow (Gobiocypris rarus). Fish Physiol Biochem 41:561–571. https://doi.org/10.1007/s10695-015-0029-x
doi: 10.1007/s10695-015-0029-x
pubmed: 25663436
Duangkaew R, Jangprai A, Ichida K, Yoshizaki G, Boonanuntanasarn S (2019) Characterization and expression of vasa homolog in the gonads and primordial germ cells of the striped catfish (Pangasianodon hypophthalmus). Theriogenology 131:61–71. https://doi.org/10.1016/j.theriogenology.2019.01.022
doi: 10.1016/j.theriogenology.2019.01.022
pubmed: 30947076
Dufour S, Lopez E, Le Menn F, Le Belle N, Baloche S, Fontaine YA (1988) Stimulation of gonadotropin release and of ovarian development, by the administration of a gonadoliberin agonist and of dopamine antagonists, in female silver eel pretreated with estradiol. Gen Comp Endocrinol 70:20–30. https://doi.org/10.1016/0016-6480(88)90090-1
doi: 10.1016/0016-6480(88)90090-1
pubmed: 3286369
Gentile L, Casalini A, Emmanuele P, Brusa R, Zaccaroni A, Mordenti O (2022) Gonadal development in European eel populations of North Adriatic lagoons at different silvering stages. Appl Sci 12:2820. https://doi.org/10.3390/app12062820
doi: 10.3390/app12062820
Han K, Chen S, Cai M, Jiang Y, Zhang Z, Wang Y (2018) Nanos3 not nanos1 and nanos2 is a germ cell marker gene in large yellow croaker during embryogenesis. Comp Biochem Physiol A 218:13–22. https://doi.org/10.1016/j.cbpb.2018.01.002
doi: 10.1016/j.cbpb.2018.01.002
Hay B, Jan LY, Jan YN (1988) A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55:577–587. https://doi.org/10.1016/0092-8674(88)90216-4
doi: 10.1016/0092-8674(88)90216-4
pubmed: 3052853
Henkel CV, Burgerhout E, de Wijze DL, Dirks RP, Minegishi Y, Jansen HJ, Spaink HP, Dufour S, Weltzien F-A, Tsukamoto K, van den Thillart GEEJM (2012a) Primitive duplicate Hox clusters in the European eel’s genome. PLoS ONE 7:e32231. https://doi.org/10.1371/journal.pone.0032231
doi: 10.1371/journal.pone.0032231
pubmed: 22384188
Henkel CV, Dirks RP, de Wijze DL, Minegishi Y, Aoyama J, Jansen HJ, Turner B, Dufour S, Tsukamoto K, Spaink HP, van den Thillart GE (2012b) First draft genome sequence of the Japanese eel, Anguilla japonica. Gene 511:195–201. https://doi.org/10.1371/journal.pone.0032231
doi: 10.1371/journal.pone.0032231
pubmed: 23026207
Howroyd P, Hoyle-Thacker R, Lyght O, Williams D, Kleymenova E (2005) Morphology of the fetal rat testis preserved in different fixatives. Toxicology Pathology 33:300–304. https://doi.org/10.1080/01926230590896145
doi: 10.1080/01926230590896145
Jeng SR, Wu GC, Yueh WS, Kuo SF, Dufour S, Chang CF (2018) Gonadal development and expression of sex-specific genes during sex differentiation in the Japanese eel. Gen Comp Endocrinol 257:74–85. https://doi.org/10.1016/j.ygcen.2017.07.031
doi: 10.1016/j.ygcen.2017.07.031
pubmed: 28826812
Jolly C, Rousseau K, Prézeau L, Vol C, Tomkiewicz J, Dufour S, Pasqualini C (2016) Functional characterisation of eel dopamine D
Kobayashi T, Kajiura-Kobayashi H, Nagahama Y (1998) A novel stage-specific antigen is expressed only in early stages of spermatogonia in Japanese eel, Anguilla japonica testis. Mol Reprod Dev 51:355–361. https://doi.org/10.1002/(SICI)1098-2795(199812)51:4%3c355::AID-MRD1%3e3.0.CO;2-G
doi: 10.1002/(SICI)1098-2795(199812)51:4<355::AID-MRD1>3.0.CO;2-G
pubmed: 9820193
Lacerda SMSN, Costa GMJ, da Silva MdA, Campos-Junior PHA, Segatelli TM, Peixoto MTD, Resende RR, de França LR (2013) Phenotypic characterization and in vitro propagation and transplantation of the Nile tilapia (Oreochromis niloticus) spermatogonial stem cells. Gen Comp Endocrinol 192:95–106. https://doi.org/10.1016/j.ygcen.2013.06.013
doi: 10.1016/j.ygcen.2013.06.013
Lacerda SMdSN, Costa GMJ, de França LR (2014) Biology and identity of fish spermatogonial stem cell. Gen Comp Endocrinol 207:56–65. https://doi.org/10.1016/j.ygcen.2014.06.018
doi: 10.1016/j.ygcen.2014.06.018
pubmed: 24967950
Lacerda SMdSN, Aponte PM, Costa GMJ, Campos-Junior PHA, Segatelli TM, da Silva MdA, de França LR (2018) An overview of spermatogonial stem cell physiology, niche and transplantation in fish. Anim Reprod 9:798–808
Lasko PF, Ashburner M (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335:611–617. https://doi.org/10.1038/335611a0
doi: 10.1038/335611a0
pubmed: 3140040
Lin F, Zhao C, Xu S, Ma D, Xiao Z, Xiao Y, Xu C, Liu Q, Li J (2013) Germline-specificand sexually dimorphic expression of a dead end gene homologue in turbot (Scophthalmus maximus). Theriogenology 80:665–672. https://doi.org/10.1016/j.theriogenology.2013.06.016
doi: 10.1016/j.theriogenology.2013.06.016
pubmed: 23906483
Maugars G, Dufour S (2015) Demonstration of the coexistence of duplicated lh receptors in teleosts, and their origin in ancestral actinopterygians. PLoS ONE 10. https://doi.org/10.1371/journal.pone.0135184
Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945. https://doi.org/10.1002/bies.20293
Mochizuki K, Nishimiya-Fujisawa C, Fujisawa T (2001) Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra. Dev Genes Evol 211:299–308. https://doi.org/10.1007/s004270100156
doi: 10.1007/s004270100156
pubmed: 11466525
Morini M, Peñaranda DS, Vílchez MC, Gallego V, Nourizadeh-Lillabadi R, Asturiano JF, Weltzien FA, Pérez L (2015) Transcript levels of the soluble sperm factor protein phospholipase C zeta 1 (PLCζ1) increase through induced spermatogenesis in European eel. Comp Biochem Physiol A 187:168–176. https://doi.org/10.1016/j.cbpa.2015.05.028
doi: 10.1016/j.cbpa.2015.05.028
Morini M, Bergqvist CA, Asturiano JF, Larhammar D, Dufour S (2022) Dynamic evolution of transient receptor potential vanilloid (TRPV) ion channel family with numerous gene duplications and losses. Front Endocrinol 13:1013868. https://doi.org/10.3389/fendo.2022.1013868
doi: 10.3389/fendo.2022.1013868
Nagasawa K, Shikina S, Takeuchi Y, Yoshizaki G (2010) Lymphocyte antigen 75 (Ly75/CD205) is a surface marker on mitotic germ cells in rainbow trout. Biol Reprod 83:597–606. https://doi.org/10.1095/biolreprod.109.082081
doi: 10.1095/biolreprod.109.082081
pubmed: 20554922
Nagasawa K, Miwa M, Yazawa R, Morita T, Takeuchi Y, Yoshizaki G (2012) Characterization of lymphocyte antigen 75 (Ly75/CD205) as a potential cell-surface marker on spermatogonia in Pacific bluefin tuna Thunnus orientalis. Fisheries Sci 78:791–800. https://doi.org/10.1007/s12562-012-0501-9
doi: 10.1007/s12562-012-0501-9
Nagasawa K, Fernandes JMO, Yoshizaki G, Miwa M, Babiak I (2013) Identification and migration of primordial germ cells in Atlantic salmon, Salmo salar: characterization of vasa, dead end, and lymphocyte antigen 75 genes. Mol Reprod Dev 80:118–131. https://doi.org/10.1002/mrd.22142
doi: 10.1002/mrd.22142
pubmed: 23239145
Nakamura S, Kobayashi K, Nishimura T, Higashijima S-i, Tanaka M (2010) Identification of germline stem cells in the ovary of the teleost medaka. Science 328:1561–1563. https://doi.org/10.1126/science.1185473
doi: 10.1126/science.1185473
pubmed: 20488987
Nakamura Y, Yasuike M, Mekuchi M, Iwasaki Y, Ojima N, Fujiwara A, Chow S, Saitoh K (2017) Rhodopsin gene copies in Japanese eel originated in a teleost-specific genome duplication. Zool Lett 3. https://doi.org/10.1186/s40851-017-0079-2
Nakatani Y, Takeda H, Kohara Y, Morishita S (2007) Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res 17:1254–1265. https://doi.org/10.1101/gr.6316407
doi: 10.1101/gr.6316407
pubmed: 17652425
Okamura A, Yamada Y, Yokouchi K, Horie N, Mikawa N, Utoh T, Tanaka S, Tsukamoto K (2007) A silvering index for the Japanese eel Anguilla japonica. Environ Biol Fish 80:77–89. https://doi.org/10.1007/s10641-006-9121-5
doi: 10.1007/s10641-006-9121-5
Ozaki Y, Saito K, Shinya M, Kawasaki T, Sakai N (2011) Evaluation of Sycp3, Plzf and Cyclin B3 expression and suitability as spermatogonia and spermatocyte markers in zebrafish. Gene Expr Patterns 11:309–315. https://doi.org/10.1016/j.gep.2011.03.002
doi: 10.1016/j.gep.2011.03.002
pubmed: 21402175
Palstra AP, Guerrero MA, de Laak G, Breteler JPGK, van den Thillart GEEJM (2011) Temporal progression in migratory status and sexual maturation in European silver eels during downstream migration. Fish Physiol Biochem 37:285–296. https://doi.org/10.1007/s10695-011-9496-x
doi: 10.1007/s10695-011-9496-x
pubmed: 21556699
Peñaranda DS, Pérez L, Gallego V, Barrera R, Jover M, Asturiano JF (2010) European eel sperm diluent for short-term storage. Reprod Domest Anim 45:407–415. https://doi.org/10.1111/j.1439-0531.2008.01206.x
doi: 10.1111/j.1439-0531.2008.01206.x
pubmed: 18954399
Peñaranda DS, Gallego V, Rozenfeld C, Herranz-Jusdado JG, Pérez L, Gómez A, Giménez I, Asturiano JF (2018) Using specific recombinant gonadotropins to induce spermatogenesis and spermiation in the European eel (Anguilla anguilla). Theriogenology 107:6–20. https://doi.org/10.1016/j.theriogenology.2017.11.002
doi: 10.1016/j.theriogenology.2017.11.002
pubmed: 29120707
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
doi: 10.1016/j.aquaculture.2016.03.004
Sánchez-Sánchez AV, Camp E, García-España A, Leal-Tassias A, Mullor JL (2010) Medaka Oct4 is expressed during early embryo development, and in primordial germ cells and adult gonads. Dev Dyn 239:672–679. https://doi.org/10.1002/dvdy.22198
doi: 10.1002/dvdy.22198
pubmed: 20034054
Schmidt J (1923) Breeding places and migration of the eel. Nature 111:51–54. https://doi.org/10.1038/111051a0
doi: 10.1038/111051a0
Schulz RW, de França LR, Lareyre J-J, Le Gac F, Chiarini-García H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. 165:390 411 https://doi.org/10.1016/j.ygcen.2009.02.013
Schüpbach T, Wieschaus E (1986) Germline autonomy of maternal effect mutations altering the embryonic body pattern of Drosophila. Dev Biol 113:443–448. https://doi.org/10.1016/0012-1606(86)90179-x
doi: 10.1016/0012-1606(86)90179-x
pubmed: 3081391
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, Mc William H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. https://doi.org/10.1038/msb.2011.75
doi: 10.1038/msb.2011.75
pubmed: 21988835
Stamatakis A, Ott M (2008) Efficient computation of the phylogenetic likelihood function on multi-gene alignments and multi-core architectures. Philos Trans R Soc B 363:3977–3984. https://doi.org/10.1098/rstb.2008.0163
doi: 10.1098/rstb.2008.0163
Tsuda M, Sasaoka Y, Kiso M, Abe K, Haraguchi S, Kobayashi S, Saga Y (2003) Conserved role of NANOS proteins in germ cell development. Science 301:1239–1241. https://doi.org/10.1126/science.1085222
doi: 10.1126/science.1085222
pubmed: 12947200
Tsuda M, Kiso M, Saga Y (2006) Implication of nanos2-3’UTR in the expression and function of nanos2. Mech Dev 123:440–449. https://doi.org/10.1016/j.mod.2006.04.002
doi: 10.1016/j.mod.2006.04.002
pubmed: 16806845
van Ginneken VJ, Maes GE (2005) The European eel (Anguilla anguilla, Linnaeus), its lifecycle, evolution and reproduction: a literature review. Rev Fish Biol Fisher 15:367–398. https://doi.org/10.1007/s11160-006-0005-8
doi: 10.1007/s11160-006-0005-8
Vasconcelos ACN, Streit DP, Octavera A, Miwa M, Kabeya N, Garcia RRF, Rotili DA, Yoshizaki G (2019) Isolation and characterization of a germ cell marker in teleost fish Colossoma macropomum. Gene 683:54–60. https://doi.org/10.1016/j.gene.2018.10.027
doi: 10.1016/j.gene.2018.10.027
pubmed: 30316926
von Kopylow K, Kirchhoff C, Jezek D, Schulze W, Feig C, Primig M, Steinkraus V, Spiess A-N (2010) Screening for biomarkers of spermatogonia within the human testis: a whole genome approach. Hum Reprod 25:1104–1112. https://doi.org/10.1093/humrep/deq053
doi: 10.1093/humrep/deq053
Wang M, Ding H, Wu S, Wang M, Wei C, Wang B, Bao Z, Hu J (2022) Vasa is a potential germ cell marker in leopard coral grouper (Plectropomus leopardus). Genes 13. https://doi.org/10.3390/genes13061077
Wargelius A, Leininger S, Skaftnesmo KO, Kleppe L, Andersson E, Taranger GL, Schulz R, Edvardsen RB (2016) Dnd knockout ablates germ cells and demonstrates germ cell independent sex differentiation in Atlantic salmon. Sci Rep 6. https://doi.org/10.1038/srep21284
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. https://doi.org/10.1016/s0960-9822(03)00537-2
doi: 10.1016/s0960-9822(03)00537-2
pubmed: 12932328
Xu H, Gui J, Hong Y (2005) Differential expression of vasa RNA and protein during spermatogenesis and oogenesis in the gibel carp (Carassius auratus gibelio), a bisexually and gynogenetically reproducing vertebrate. Dev Dyn 233:872–882. https://doi.org/10.1002/dvdy.20410
doi: 10.1002/dvdy.20410
pubmed: 15880437
Xu H, Lim M, Dwarakanath M, Hong Y (2014) Vasa identifies germ cells and critical stages of oogenesis in the Asian seabass. Int J Biol Sci 10:225–235. https://doi.org/10.7150/ijbs.6797
doi: 10.7150/ijbs.6797
pubmed: 24550690
Yang X, Yue H, Ye H, Li C, Wei Q (2015) Identification of a germ cell marker gene, the dead end homologue, in Chinese sturgeon Acipenser sinensis. Gene 558:118–125. https://doi.org/10.1016/j.gene.2014.12.059
doi: 10.1016/j.gene.2014.12.059
pubmed: 25550043
Yano A, Von Schalburg K, Cooper G, Koop BF, Yoshizaki G (2009) Identification of a molecular marker for type A spermatogonia by microarray analysis using gonadal cells from pvasa-GFP transgenic rainbow trout (Oncorhynchus mykiss). Mol Reprod Dev 76:246–254. https://doi.org/10.1002/mrd.20947
doi: 10.1002/mrd.20947
pubmed: 18646050
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
doi: 10.1002/mrd.22224
pubmed: 23913406
Ye D, Lv D, Song P, Peng M, Chen Y, Guo M, Yang Q, Hu Y (2007) Cloning and characterization of a rice field eel vasa-like gene cDNA and its expression in gonads during natural sex transformation. Biochem Genet 45:211–224. https://doi.org/10.1007/s10528-006-9066-6
doi: 10.1007/s10528-006-9066-6
pubmed: 17318374
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
doi: 10.1002/mrd.22625
pubmed: 26860442
Yuan Y, Li M, Hong Y (2014) Light and electron microscopic analyses of Vasa expression in adult germ cells of the fish medaka. Gene 545:15–22. https://doi.org/10.1016/j.gene.2014.05.017
doi: 10.1016/j.gene.2014.05.017
pubmed: 24814190
Zhu T, Gui L, Zhu Y, Li M (2018) Dnd is required for primordial germ cell specification in Oryzias celebensis. Gene 679:36–43. https://doi.org/10.1016/j.gene.2018.08.068
doi: 10.1016/j.gene.2018.08.068
pubmed: 30171940