Characterization of potential spermatogonia biomarker genes in the European eel (Anguilla anguilla)
Jazyk angličtina Země Nizozemsko Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
Project EELGONIA; RTI2018-096413-B-I00
Ministerio de Ciencia e Innovación y Universidades
PAID-01-20
Universitat Politècnica de València
THINKINAZUL/2021/012
European Union NextGenerationEU
RYC2021-031558-I
European Union NextGenerationEU
THINKINAZUL/2021/012
Generalitat Valenciana
GRISOLIAP/2020/063
Generalitat Valenciana
TKP2020-NKA-16
Ministry of Innovation and Technology Hungary
Nº 642893 (IMPRESS)
European Union's Horizon 2020 Marie Skłodowska-Curie
Project CENAKVA (LM2018099)
Ministry of Education, Youth and Sports of the Czech Republic
CZ.02.1.01/0.0/0.0/16_025/0007370
Biodiversity
22-31141J
Czech Science Foundation
RYC2021-031558-I
Ministerio de Ciencia e Innovación
PubMed
38639895
PubMed Central
PMC11576858
DOI
10.1007/s10695-024-01338-1
PII: 10.1007/s10695-024-01338-1
Knihovny.cz E-zdroje
- Klíčová slova
- Dnd1, Nanos2, Vasa, Fish, Gene expression, Testis,
- MeSH
- Anguilla * genetika MeSH
- biologické markery * metabolismus MeSH
- proteiny vázající RNA genetika metabolismus MeSH
- rybí proteiny genetika MeSH
- spermatogonie * metabolismus MeSH
- testis * metabolismus MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- biologické markery * MeSH
- proteiny vázající RNA MeSH
- rybí proteiny MeSH
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.
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Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105. 10.1093/bioinformatics/bti263 PubMed DOI
Aoki Y, Nakamura S, Ishikawa Y, Tanaka M (2009) Expression and syntenic analyses of four PubMed DOI
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. 10.3390/ani9040174 PubMed DOI PMC
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. 10.1038/s41598-017-17204-5 PubMed DOI PMC
Beer RL, Draper BW (2013) PubMed DOI
Begum S, Gnanasree SM, Anusha N, Senthilkumaran B (2022) Germ cell markers in fishes – a review. Aquaculture and Fisheries 7:540–552. 10.1016/j.aaf.2022.03.015 DOI
Bellaiche J, Lareyre JJ, Cauty C, Yano A, Allemand I, Le Gac F (2014) Spermatogonial stem cell quest: PubMed DOI
Blázquez M, González A, Mylonas CC, Piferrer F (2011) Cloning and sequence analysis of PubMed DOI
Booncherd K, Sreebun S, Pasomboon P, Boonanuntanasarn S (2024) Effects of CRISPR/Cas9-mediated PubMed
Bosseboeuf A, Gautier A, Auvray P, Mazan S, Sourdaine P (2014) Characterization of spermatogonial markers in the mature testis of the dogfish ( PubMed DOI
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 ( DOI
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, PubMed DOI
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. 10.1073/pnas.160274797 PubMed DOI PMC
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. 10.1007/978-1-4939-4017-2_8 PubMed DOI
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 ( PubMed DOI
Duangkaew R, Jangprai A, Ichida K, Yoshizaki G, Boonanuntanasarn S (2019) Characterization and expression of PubMed DOI
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. 10.1016/0016-6480(88)90090-1 PubMed DOI
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. 10.3390/app12062820 DOI
Han K, Chen S, Cai M, Jiang Y, Zhang Z, Wang Y (2018) PubMed DOI
Hay B, Jan LY, Jan YN (1988) A protein component of PubMed DOI
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. 10.1371/journal.pone.0032231 PubMed DOI PMC
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, PubMed DOI
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. 10.1080/01926230590896145 PubMed DOI
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. 10.1016/j.ygcen.2017.07.031 PubMed DOI
Jolly C, Rousseau K, Prézeau L, Vol C, Tomkiewicz J, Dufour S, Pasqualini C (2016) Functional characterisation of eel dopamine D PubMed
Kobayashi T, Kajiura-Kobayashi H, Nagahama Y (1998) A novel stage-specific antigen is expressed only in early stages of spermatogonia in Japanese eel, PubMed DOI
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 ( PubMed DOI
Lacerda SMdSN, Costa GMJ, de França LR (2014) Biology and identity of fish spermatogonial stem cell. Gen Comp Endocrinol 207:56–65. 10.1016/j.ygcen.2014.06.018 PubMed DOI
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 PubMed DOI
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 ( PubMed DOI
Maugars G, Dufour S (2015) Demonstration of the coexistence of duplicated PubMed PMC
Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945. 10.1002/bies.20293 PubMed
Mochizuki K, Nishimiya-Fujisawa C, Fujisawa T (2001) Universal occurrence of the PubMed DOI
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. 10.1016/j.cbpa.2015.05.028 PubMed DOI
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. 10.3389/fendo.2022.1013868 PubMed DOI PMC
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. 10.1095/biolreprod.109.082081 PubMed DOI
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 DOI
Nagasawa K, Fernandes JMO, Yoshizaki G, Miwa M, Babiak I (2013) Identification and migration of primordial germ cells in Atlantic salmon, PubMed DOI PMC
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. 10.1126/science.1185473 PubMed DOI
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. 10.1186/s40851-017-0079-2 PubMed PMC
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. 10.1101/gr.6316407 PubMed DOI PMC
Okamura A, Yamada Y, Yokouchi K, Horie N, Mikawa N, Utoh T, Tanaka S, Tsukamoto K (2007) A silvering index for the Japanese eel DOI
Ozaki Y, Saito K, Shinya M, Kawasaki T, Sakai N (2011) Evaluation of PubMed DOI
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. 10.1007/s10695-011-9496-x PubMed DOI PMC
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. 10.1111/j.1439-0531.2008.01206.x PubMed DOI
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 ( PubMed DOI
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. 10.1016/j.aquaculture.2016.03.004 DOI
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. 10.1002/dvdy.22198 PubMed DOI
Schmidt J (1923) Breeding places and migration of the eel. Nature 111:51–54. 10.1038/111051a0 DOI
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 10.1016/j.ygcen.2009.02.013 PubMed
Schüpbach T, Wieschaus E (1986) Germline autonomy of maternal effect mutations altering the embryonic body pattern of PubMed DOI
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. 10.1038/msb.2011.75 PubMed DOI PMC
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. 10.1098/rstb.2008.0163 PubMed DOI PMC
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. 10.1126/science.1085222 PubMed DOI
Tsuda M, Kiso M, Saga Y (2006) Implication of nanos2-3’UTR in the expression and function of PubMed DOI
van Ginneken VJ, Maes GE (2005) The European eel ( DOI
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 PubMed DOI
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. 10.1093/humrep/deq053 PubMed DOI
Wang M, Ding H, Wu S, Wang M, Wei C, Wang B, Bao Z, Hu J (2022) PubMed PMC
Wargelius A, Leininger S, Skaftnesmo KO, Kleppe L, Andersson E, Taranger GL, Schulz R, Edvardsen RB (2016) PubMed PMC
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)00537-2 PubMed DOI
Xu H, Gui J, Hong Y (2005) Differential expression of vasa RNA and protein during spermatogenesis and oogenesis in the gibel carp ( PubMed DOI
Xu H, Lim M, Dwarakanath M, Hong Y (2014) PubMed DOI PMC
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 PubMed DOI
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 PubMed DOI
Yazawa R, Takeuchi Y, Morita T, Ishida M, Yoshizaki G (2013) The Pacific bluefin tuna ( PubMed DOI
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 PubMed DOI
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. 10.1002/mrd.22625 PubMed DOI
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. 10.1016/j.gene.2014.05.017 PubMed DOI