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Immunoreactive changes in pituitary FSH and LH cells during seasonal reproductive and spawning cycles of female chub mackerel Scomber japonicus

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Abstract

The physiological functions of pituitary gonadotropins (GtHs) are well established in higher vertebrates, whereas those in teleosts are still poorly understood. To describe the role of GtHs during gonadal development of female chub mackerel Scomber japonicus, changes in follicle-stimulating hormone (FSH) and luteinizing hormone (LH) cells were investigated immunohistochemically during the seasonal reproductive and spawning cycles. FSH and LH cells were identified in the different cell types of the proximal pars distalis (PPD); FSH cells were located in the central PPD, whereas LH cells were localized along the border of the pars intermedia. To examine changes in FSH and LH cells, the percentage of FSH or LH cell-occupying area in the PPD was evaluated and represented as FSHβ-immunoreactive (ir) or LHβ-ir levels, respectively. FSHβ-ir levels increased significantly from immature to the completion of vitellogenesis, whereas LHβ-ir levels were maintained at high levels from early vitellogenesis to post-spawning. During the spawning cycle, which consisted of four stages from just after spawning to the next oocyte maturation, both FSHβ-ir and LHβ-ir levels showed no significant changes among different stages; however, LHβ-ir levels remained relatively high, and FSHβ-ir levels were constantly low. These results suggest that both FSH and LH may be involved in vitellogenesis and LH may act at final oocyte maturation in female chub mackerel, although the role of FSH during the spawning cycle is still unclear.

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References

  1. Somoza GM, Miranda LA, Strobl-Mazzulla P, Guilgur LG (2002) Gonadotropin-releasing hormone (GnRH): from fish to mammalian brains. Cell Mol Neurobiol 22:589–609

    Article  PubMed  CAS  Google Scholar 

  2. Sherwood NM, Adams BA (2005) Gonadotropin-releasing hormone in fish: evolution, expression and regulation of the GnRH gene. In: Melamed P, Sherwood N (eds) Hormones and their receptors in fish reproduction. World Scientific, Singapore, pp 1–39

    Chapter  Google Scholar 

  3. Rosenfeld H, Meiri I, Elizur A (2007) Gonadotropic regulation of oocyte development. In: Babin PJ, Cerdà J, Lubzens E (eds) The fish oocyte: from basic studies to biotechnological applications. Springer, Dordrecht, pp 175–202

    Google Scholar 

  4. Pierce JG, Parsons TF (1981) Glycoprotein hormones: structure and function. Annu Rev Biochem 50:465–495

    Article  PubMed  CAS  Google Scholar 

  5. Planas JV, Swanson P (2007) Physiological function of gonadotropins in fish. In: Rocha MJ, Arukwe A, Kapoor BJ (eds) Fish reproduction. Science, Enfield, pp 37–66

    Google Scholar 

  6. Suzuki K, Kawauchi H, Nagahama Y (1988) Isolation and characterization of two distinct gonadotropins from chum salmon pituitary glands. Gen Comp Endocrinol 71:292–301

    Article  PubMed  CAS  Google Scholar 

  7. Tyler CR, Sumpter JP, Kawauchi H, Swanson P (1991) Involvement of gonadotropin in the uptake of vitellogenin into vitellogenic oocytes of the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 84:291–299

    Article  PubMed  CAS  Google Scholar 

  8. Swanson P, Dickey JT, Cambell B (2003) Biochemistry and physiology of fish gonadotropins. Fish Physiol Biochem 28:53–59

    Article  CAS  Google Scholar 

  9. Aizen J, Kasuto H, Levavi-Sivan B (2007) Development of specific enzyme-linked immunosorbent assay for determining LH and FSH levels in tilapia, using recombinant gonadotropins. Gen Comp Endocrinol 153:323–332

    Article  PubMed  CAS  Google Scholar 

  10. Levavi-Sivan B, Bogerd J, Mañanós E, Gómez A, Lareyre JJ (2010) Perspectives on fish gonadotropins and their receptors. Gen Comp Endocrinol 165:412–437

    Article  PubMed  CAS  Google Scholar 

  11. Van Der Kraak G, Suzuki K, Peter RE, Itoh H, Kawauchi H (1992) Properties of common carp gonadotropin I and gonadotropin II. Gen Comp Endocrinol 85:217–229

    Article  PubMed  Google Scholar 

  12. Okada T, Kawazoe I, Kimura S, Sasamoto Y, Aida K, Kawauchi H (1994) Purification and characterization of gonadotropin I and II from pituitary glands of tuna (Thunnus obesus). Int J Pept Protein Res 43:69–80

    Article  PubMed  CAS  Google Scholar 

  13. Kagawa H, Tanaka H, Okuzawa K, Kobayashi M (1998) GTH II but not GTH I induces final maturation and the development of maturational competence of oocytes of red seabream in vitro. Gen Comp Endocrinol 112:80–88

    Article  PubMed  CAS  Google Scholar 

  14. Kagawa H, Gen K, Okuzawa K, Tanaka H (2003) Effects of luteinizing hormone and follicle stimulating hormone and insulin-like growth factor-I on aromatase activity and P450 aromatase gene expression in the ovarian follicles of red seabream, Pagrus major. Biol Reprod 68:1562–1568

    Article  PubMed  CAS  Google Scholar 

  15. Molés G, Gómez A, Rocha A, Carrillo M, Zanuy S (2008) Purification and characterization of follicle-glands of sea bass (Dicentrarchus labrax). Gen Comp Endocrinol 158:68–76

    Article  PubMed  Google Scholar 

  16. Shimizu A, Yamashita M (2002) Purification of mummichog (Fundulus heteroclitus) gonadotropins and their subunits, using an immunochemical assay with antisera raised against synthetic peptides. Gen Comp Endocrinol 125:79–91

    Article  PubMed  CAS  Google Scholar 

  17. Shimizu A, Sakai T, Nashida K, Honda H (2003) Universal antisera for immunocytochemical identification of two different gonadotrophs in acanthopterygian fishes. Fish Physiol Biochem 29:275–287

    Article  CAS  Google Scholar 

  18. Shimizu A, Tanaka H, Kagawa H (2003) Immunocytochemical applications of specific antisera raised against synthetic fragment peptides of mummichog GtH subunits: examining seasonal variations of gonadotrophs (FSH cells and LH cells) in the mummichog and applications to other acanthopterygian fishes. Gen Comp Endocrinol 132:35–45

    Article  PubMed  CAS  Google Scholar 

  19. Pham KR, Amano M, Kurita Y, Shimizu A, Fujinami Y, Amiya N, Yamamori K (2008) Changes in the immunostaining intensities of follicle-stimulating hormone and luteinizing hormone during ovarian maturation in the female Japanese flounder. Fish Physiol Biochem 34:357–365

    Article  PubMed  CAS  Google Scholar 

  20. Matsuyama M, Shiraishi T, Sundaray JK, Rahman MA, Ohta K, Yamaguchi A (2005) Steroidogenesis in ovarian follicles of chub mackerel, Scomber japonicus. Zool Sci 22:101–110

    Article  PubMed  CAS  Google Scholar 

  21. Mendiola D, Yamashita Y, Matsuyama M, Alvarez P, Tanaka M (2008) Scomber japonicus, H. is a better candidate species for juvenile production activities than Scomber scombrus, L. Aquac Res 39:1122–1127

    Article  Google Scholar 

  22. Shiraishi T, Ohta K, Yamaguchi A, Yoda M, Chuda H, Matsuyama M (2005) Reproductive parameters of the chub mackerel Scomber japonicus estimated from human chorionic gonadotropin-induced final oocyte maturation and ovulation in captivity. Fish Sci 71:531–542

    Article  CAS  Google Scholar 

  23. Shiraishi T, Ketkar SD, Kitano H, Nyuji M, Yamaguchi A, Matsuyama M (2008) Time course of final oocyte maturation and ovulation in chub mackerel Scomber japonicus induced by hCG and GnRHa. Fish Sci 74:764–769

    Article  CAS  Google Scholar 

  24. Scott AP, Whitthames PR, Vermeirssen ELM, Carolsfeld J (1999) Prolonged-release gonadotropin-releasing hormone analogue implants enhance oocyte final maturation and ovulation, and increase plasma concentration of sulphated C21 steroids in North Sea plaice. J Fish Biol 55:316–328

    CAS  Google Scholar 

  25. Shiraishi T, Ketkar SD, Katoh Y, Nyuji M, Yamaguchi A, Matsuyama M (2009) Spawning frequency of the Tsushima Current subpopulation of chub mackerel Scomber japonicus off Kyushu, Japan. Fish Sci 75:649–655

    Article  CAS  Google Scholar 

  26. Kagawa H, Kawazoe I, Tanaka H, Okuzawa K (1998) Immunocytochemical identification of two distinct gonadotropic cells (GTH I and GTH II) in the pituitary of bluefin tuna, Thunnus thynnus. Gen Comp Endocrinol 110:11–18

    Article  PubMed  CAS  Google Scholar 

  27. Nozaki M, Naito N, Swanson P, Miyata K, Nakai Y, Oota Y, Suzuki K, Kawauchi H (1990) Salmonid pituitary gonadotropins I. Distinct cellular distributions of two gonadotropins, GTH I and GTH II. Gen Comp Endocrinol 77:348–357

    Article  PubMed  CAS  Google Scholar 

  28. Calman B, Lin Y-WP, Wallace RA (2001) Preparation and use of specific antibodies to the β-I and β-II subunits of gonadotropic hormone from Fundulus heteroclitus pituitary. Gen Comp Endocrinol 123:203–209

    Article  PubMed  CAS  Google Scholar 

  29. Miranda LA, Strüssmann CA, Somoza GM (2001) Immunocytochemical identification of GtH1 and GtH2 cells during the temperature-sensitive period for sex determination in pejerrey, Odontesthes bonariensis. Gen Comp Endocrinol 124:45–52

    Article  PubMed  CAS  Google Scholar 

  30. García Hernández MP, García Ayala A, Elbal MT, Agulleiro B (1996) The adenohypophysis of Mediterranean yellowtail, Seriola dumerilii (Risso, 1810): an immunocytochemical study. Tissue Cell 28:577–585

    Article  PubMed  Google Scholar 

  31. García Ayala A, Villaplana M, García Hernández MP, Chaves Pozo E, Agulleiro B (2003) FSH-, LH-, and TSH-expressing cells during development of Sparus aurata L. (Teleostei). An immunocytochemical study. Gen Comp Endocrinol 134:72–79

    Article  PubMed  Google Scholar 

  32. Kasper RS, Shved N, Takahashi A, Reinecke M, Eppler E (2006) A systematic immunohistochemical survey of the distribution patterns of GH, prolactin, somatolactin, β-TSH, β-FSH, β-LH, ACTH, and α-MSH in the adenohypophysis of Oreochromis niloticus, the Nile tilapia. Cell Tissue Res 325:303–313

    Article  PubMed  CAS  Google Scholar 

  33. Gen K, Okuzawa K, Senthilkumaran B, Tanaka H, Moriyama S, Kagawa H (2000) Unique expression of gonadotropin-I and II subunit genes in male and female red seabream (Pagrus major) during sexual maturation. Biol Reprod 63:308–319

    Article  PubMed  CAS  Google Scholar 

  34. Gen K, Yamaguchi S, Okuzawa K, Kumakura N, Tanaka H, Kagawa H (2003) Physiological roles of FSH and LH in red seabream, Pagrus major. Fish Physiol Biochem 28:77–80

    Article  CAS  Google Scholar 

  35. Gomez JM, Weil C, Ollitrault M, Le Bail P-Y, Breton B, Le Gac F (1999) Growth hormone (GH) and gonadotropin subunit gene expression and pituitary and plasma changes during spermatogenesis and oogenesis in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 113:413–428

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the students of the Laboratory of Marine Biology, Kyushu University, for their kind help with this study. M.N. is supported by a JSPS Research Fellowship for Young Scientist. This research work was supported by a grant for scientific research (20380113 to M.M.) from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT), and through a subproject on studies on the prediction and application of fish species alternation (SUPRFISH) financed by the Agriculture, Forestry, and Fisheries Research Council (AFFRC) of Japan, as part of the Population Outbreak of Marine Life (POMAL) Project.

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  1. Vu Van In

    Present address: National Broodstock Center for Mariculture in Northern Vietnam, Haiphong, Vietnam

Authors and Affiliations

  1. Laboratory of Marine Biology, Faculty of Agriculture, Kyushu University, Fukuoka, 812-8581, Japan

    Mitsuo Nyuji, Tetsuro Shiraishi, Sethu Selvaraj, Vu Van In, Hajime Kitano, Akihiko Yamaguchi & Michiya Matsuyama

  2. Oita Prefectural Agriculture, Forestry and Fisheries Research Center, Saiki, 879-2602, Japan

    Kumiko Okamoto & Shizumasa Onoue

  3. National Research Institute of Fisheries Science, Fisheries Research Agency, Yokohama, 236-8648, Japan

    Akio Shimizu

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  1. Mitsuo Nyuji
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Correspondence to Michiya Matsuyama.

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Nyuji, M., Shiraishi, T., Selvaraj, S. et al. Immunoreactive changes in pituitary FSH and LH cells during seasonal reproductive and spawning cycles of female chub mackerel Scomber japonicus . Fish Sci 77, 731–739 (2011). https://doi.org/10.1007/s12562-011-0380-5

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  • DOI: https://doi.org/10.1007/s12562-011-0380-5

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