Fisheries Science

, Volume 77, Issue 1, pp 69–77 | Cite as

Colonization, proliferation, and survival of intraperitoneally transplanted yellowtail Seriola quinqueradiata spermatogonia in nibe croaker Nibea mitsukurii recipient

  • Kentaro Higuchi
  • Yutaka Takeuchi
  • Misako Miwa
  • Yoji Yamamoto
  • Kazunobu Tsunemoto
  • Goro Yoshizaki
Original Article Biology
First Online:
Received:
Accepted:

Abstract

Recently, we developed an intraspecies spermatogonial transplantation technique in a pelagic egg spawning marine teleost, nibe croaker Nibea mitsukurii. Nibe croaker is an ideal candidate recipient for spermatogonial transplantation since it has a short generation time and small body size. In the present study, yellowtail Seriola quinqueradiata spermatogonia were transplanted into nibe croaker larvae, and the behavior of transplanted spermatogonia in recipient gonads was observed. Three weeks post-transplantation, yellowtail spermatogonia were incorporated into the gonads of 72 out of 88 recipients. An antiproliferating cell nuclear antigen was detected in incorporated yellowtail spermatogonia, suggesting that the xenogenic germ cells were proliferating in recipient gonads. Yellowtail vasa-positive spermatogonia survived for 11 months after transplantation in the gonads of recipient fish. Thus, we showed that the microenvironment in nibe croaker gonads can support the colonization, proliferation, and survival of germ cells derived from a different taxonomic family.

Keywords

Xenogenic transplantation Spermatogonia Marine teleost Vasa 
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Notes

Acknowledgments

The authors are grateful to the members of the Tateyama Station (J. Ito, M. Masuko, N. Ishikawa, R. Yazawa, T. Yatabe, N. Kabeya, N. Hayashi, and M. Hayakawa) of Tokyo University of Marine Science and Technology for their assistance in the maintenance of fishes.

References

  1. 1.
    Sawada Y, Okada T, Miyashita S, Murata O, Kumai H (2005) Completion of the Pacific bluefin tuna, Thunnus orientalis, life cycle under aquaculture conditions. Aquacult Res 36:413–421CrossRefGoogle Scholar
  2. 2.
    Seoka M, Kato K, Kubo T, Mukai Y, Sakamoto W, Kumai H, Murata O (2007) Gonadal maturation of Pacific bluefin tuna Thunnus orientalis in captivity. Aquac Sci 55:289–292Google Scholar
  3. 3.
    de Rooji DG, Grootegoed JA (1998) Spermatogonial stem cells. Curr Opin Cell Biol 10:694–701CrossRefGoogle Scholar
  4. 4.
    Okutsu T, Yano A, Nagasawa K, Shikina S, Kobayashi T, Takeuchi Y, Yoshizaki G (2006) Manipulation of fish germ cell: visualization, cryopreservation and transplantation. J Reprod Dev 52:685–693CrossRefPubMedGoogle Scholar
  5. 5.
    Okutsu T, Shikina S, Kanno M, Takeuchi Y, Yoshizaki G (2007) Production of trout offspring from triploid salmon parents. Science 317:1517CrossRefPubMedGoogle Scholar
  6. 6.
    Kobayashi T, Takeuchi Y, Takeuchi T, Yoshizaki G (2007) Generation of viable fish from cryopreserved primordial germ cells. Mol Reprod Dev 74:207–213CrossRefPubMedGoogle Scholar
  7. 7.
    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 D. doi: 10.1016/j.cbd.2010.05.003
  8. 8.
    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 81:1055–1063CrossRefPubMedGoogle Scholar
  9. 9.
    Nelson JS (2006) Fishes of the world, 4th edn. Wiley, New York, pp 372–373Google Scholar
  10. 10.
    Abascal FJ, Medina A (2005) Ultrastructure of oogenesis in the bluefin tuna, Thunnus thynnus. J Morphol 264:149–160CrossRefPubMedGoogle Scholar
  11. 11.
    Matsuyama M, Kagawa H, Arimoto M, Maruyama K, Hirotsuji H, Kashiwagi M, Liu R (1996) Change of ovarian maturity in the yellowtail Seriola quinqueradiata induced by human chorionic gonadotropin (in Japanese with English abstract). Suisanzoshoku 44:189–195Google Scholar
  12. 12.
    Battaglene SC, Talbot RB (1994) Hormone induction and larval rearing of mulloway, Argyrosomus hololepidotus (Pisces: Sciaenidae). Aquaculture 126:73–81CrossRefGoogle Scholar
  13. 13.
    Okumura S, Okamoto K, Oomori R, Nakazono A (2002) Spawning behavior and artificial fertilization in captive reared red spotted grouper, Epinephelus akaara. Aquaculture 206:165–173CrossRefGoogle Scholar
  14. 14.
    Kaji T, Tanaka M, Tagawa M (1999) Laboratory study of density-dependent survival after handling in yolk-sac larvae of tunas and a grouper. Fish Sci 65:482–483Google Scholar
  15. 15.
    Honda H, Kawasaki T (1983) A comparative life historical study on the two sciaenoid species, white croaker and nibe croaker, inhabiting Sendai Bay. Tohoku J Agric Res 33:164–177Google Scholar
  16. 16.
    Yoshizaki G, Miwa M, Takeuchi T, Patino R (2001) Gonadotropin-dependent oocyte maturational competence requires activation of the protein kinase A pathway and synthesis of RNA and protein in ovarian follicles of nibe, Nibea mitsukurii (Teleostei, Sciaenidae). Fish Physiol Biochem 25:201–208CrossRefGoogle Scholar
  17. 17.
    Noce T, Okamoto-Ito S, Tsunekawa N (2001) Vasa homolog genes in mammalian germ cell development. Cell Struct Funct 26:131–136CrossRefPubMedGoogle Scholar
  18. 18.
    Nagasawa K, Takeuchi Y, Miwa M, Higuchi K, Morita T, Mitsuboshi T, Miyaki K, Kadomura K, Yoshizaki G (2009) cDNA cloning and expression analysis of a vasa-like gene in Pacific bluefin tuna Thunnus orientalis. Fish Sci 75:71–79CrossRefGoogle Scholar
  19. 19.
    Landberg G, Roos G (1991) Antibodies to proliferating cell nuclear antigen as S-phase probes in flow cytometric cell cycle analysis. Cancer Res 51:4570–4574PubMedGoogle Scholar
  20. 20.
    Takeuchi Y, Yoshizaki G, Takeuchi T (1999) Green fluorescent protein as a cell-labeling tool and a reporter of gene expression in transgenic rainbow trout. Mar Biotechnol 5:448–457CrossRefGoogle Scholar
  21. 21.
    Yano A, Suzuki K, Yoshizaki G (2008) Flow-cytometric isolation of testicular germ cells from rainbow trout (Oncorhynchus mykiss) carrying the green fluorescent protein gene driven by trout vasa regulatory regions. Biol Reprod 78:151–158CrossRefPubMedGoogle Scholar
  22. 22.
    Schulz RW, Franca LR, Lareyre JJ, LeGac F, Chiarini-Garcia H, Nobrega RH, Miura T (2009) Spermatogenesis in fish. Gen Comp Endrinol 165:390–411CrossRefGoogle Scholar
  23. 23.
    Takeuchi Y, Yoshizaki G, Takeuchi T (2004) Surrogate broodstock produces salmonids. Nature 430:629–630CrossRefPubMedGoogle Scholar
  24. 24.
    Yoshizaki G, Tago Y, Takeuchi Y, Sawatari E, Kobayashi T, Takeuchi T (2005) Green fluorescent protein labeling of primordial germ cells using a nontransgenic method and its application for germ cell transplantation in Salmonidae. Biol Reprod 73:88–93CrossRefPubMedGoogle Scholar
  25. 25.
    Yazawa R, Takeuchi Y, Higuchi K, Yatabe T, Kabeya N, Yoshizaki G (2010) Chub mackerel gonads support colonization, survival, and proliferation of intraperitoneally transplanted xenogenic germ cells. Biol Reprod 82:896–904CrossRefPubMedGoogle Scholar
  26. 26.
    Raz E, Reichman-Fried M (2006) Attraction rules: germ cell migration in zebrafish. Curr Opin Genet Dev 16:355–359CrossRefPubMedGoogle Scholar
  27. 27.
    Sang X, Curran MS, Wood AW (2008) Paracrine insulin-like growth factor signaling influences primordial germ cell migration: in vivo evidence from the zebrafish model. Endocrinology 149:5035–5042CrossRefPubMedGoogle Scholar
  28. 28.
    Kanatsu-Shinohara M, Ogonuki N, Iwano T, Lee J, Kazuki Y, Inoue K, Miki H, Takahashi M, Toyokuni S, Shinkai Y, Oshimura M, Ishino F, Ogura A, Shinohara T (2005) Genetic and epigenetic properties of mouse male germline stem cells during long-term culture. Development 132:4155–4163CrossRefPubMedGoogle Scholar
  29. 29.
    Shikina S, Ihara S, Yoshizaki G (2008) Culture conditions for maintaining the survival and mitotic activity of rainbow trout transplantable type A spermatogonia. Mol Reprod Dev 75:529–537CrossRefPubMedGoogle Scholar
  30. 30.
    Shikina S, Yoshizaki G (2010) Improved in vitro culture conditions to enhance the survival, mitotic activity, and transplantability of rainbow trout type A spermatogonia. Biol Reprod. doi: 10.1095/biolreprod.109.082123
  31. 31.
    Russell LD, Brinster RL (1996) Ultrastructural observations of spermatogenesis following transplantation of rat testis cells into mouse seminiferous tubules. J Androl 17:615–627PubMedGoogle Scholar
  32. 32.
    Franca LR, Ogawa T, Avarbock MR, Brinster RL, Russell LD (1998) Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 59:1371–1377CrossRefPubMedGoogle Scholar
  33. 33.
    Dobrinski I, Avarbock MR, Brinster RL (1999) Transplantation of germ cells from rabbits and dogs into mouse testes. Biol Reprod 61:1331–1339CrossRefPubMedGoogle Scholar
  34. 34.
    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 USA 103:2725–2729CrossRefPubMedGoogle Scholar
  35. 35.
    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 78:159–166CrossRefPubMedGoogle Scholar
  36. 36.
    Reagan RE (1985) Life histories and environmental requirements of coastal fishes and invertebrates (Gulf of Mexico), red drum. Mississippi State University, StarkvilleGoogle Scholar
  37. 37.
    Pirozzi I, Booth MA (2009) The effect of temperature and body weight on the routine metabolic rate and postprandial metabolic response in mulloway, Argyrosomus japonicus. Comp Biochem Physiol A 154:110–118CrossRefGoogle Scholar

Copyright information

© The Japanese Society of Fisheries Science 2010

Authors and Affiliations

  • Kentaro Higuchi
    • 1
    • 3
  • Yutaka Takeuchi
    • 2
  • Misako Miwa
    • 1
  • Yoji Yamamoto
    • 1
  • Kazunobu Tsunemoto
    • 1
  • Goro Yoshizaki
    • 1
  1. 1.Department of Marine BioscienceTokyo University of Marine Science and TechnologyTokyoJapan
  2. 2.Research Center for Advanced Science and TechnologyTokyo University of Marine Science and TechnologyTateyamaJapan
  3. 3.Amami Station, National Center for Stock EnhancementFisheries Research Agency, HyouSetouchiJapan

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