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Aquaculture International

, Volume 26, Issue 4, pp 1083–1094 | Cite as

PGF and gonadal steroid plasma levels of successful and unsuccessful spawning Piaractus mesopotamicus (Teleostei, Characiformes) females

  • Rafael Yutaka Kuradomi
  • Sergio Ricardo BatlouniEmail author
Article
  • 183 Downloads

Abstract

Gonadal steroid and prostaglandin F2α (PGF) plasma levels were evaluated in successfully (SP) and unsuccessfully ovulated (UN) female Piaractus mesopotamicus. Forty-one females were injected with crude carp pituitary extract (0.6 and 5.4 mg kg−1 with a 24-h interval between the doses) and sampled to determine the plasma concentration of 17β-estradiol (E2), 17α-hydroxyprogesterone (17α-OHP), 17α,20β-dihydroxy-4-pregnen-3-one (DHP), PGF, and testosterone (T) after each injection (first—A1 and second—A2), and at the time of ovulation for SP and UN. Two clusters were obtained using multivariate analysis: 1—composed of all A1, all A2, and some UN; and 2—composed of all SP and some UN. Median values of E2 plasma levels were similar between clusters; however, plasma levels of T, 17α-OHP, DHP, and PGF of cluster 2 (predominantly formed by SP) were higher than those of cluster 1. Since cluster 2 contained all SP and females of this cluster presented higher levels of PGF, T, 17α-OHP, and DHP, here we evidently shown in an unprecedented manner that concomitant increased levels of these substances were associated with successful ovulation in this species, but such an increase was not determinant for successful ovulation due to the presence of some UN females in the same cluster 2. These findings highlight the unexplored potential of PGF to be used as an accessory tool for inducing successful ovulation for fish farming purposes.

Keywords

Pacu Crude carp pituitary extract Successful spawning Gonadal steroid plasma levels Prostaglandin F Multivariate analysis 

Notes

Acknowledgements

The authors are grateful to Dr. Elisabeth Criscuolo Urbinati (Departamento de Morfologia e Fisiologia Animal/Faculdade de Ciências Agrárias e Veterinárias de Jaboticabal - FCAV) for helping with the initial hypothesis.

Funding information

The main source of funding was the National Council for Scientific and Technological Development (CNPq, Portuguese: Conselho Nacional de Desenvolvimento Científico e Tecnológico) by Process 458274/2014-3 and 447169/2014-9 and “Programa de Apoio aos Biotérios da Unesp” – PROPE-UNESP-2014. Additionally, the cost of the fish and their maintenance was covered by the Centro de Aquicultura da UNESP – CAUNESP. R.Y.K. was supported by Coordination for the Improvement of Higher Education Personnel (CAPES, Portuguese: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) under the National Postdoctoral Program (PNPD-CAPES).

References

  1. Asturiano JF, Sorbera LA, Ramos J, Kime DE, Carrillo M, Zanuy S (2002) Group-synchronous ovarian development, ovulation and spermiation in the European sea bass (Dicentrarchus labrax L.) could be regulated by shifts in gonadal steroidogenesis. Sci Mar 66:273–282CrossRefGoogle Scholar
  2. Berndston AK, Goetz FW, Duman P (1989) In vitro ovulation, prostaglandin synthesis, and proteolysis in isolated ovarian components of yellow perch (Perca flavescens): effects of 17,20β-diidroxi-4-pregnen-3-one and phorbol ester. Gen Comp Endocrinol 75:454–465CrossRefGoogle Scholar
  3. Bradley JA, Goetz FW (1994) The inhibitory effects of indometachin nordihydroguaiaretic acid, and pyrrolidinedithiocarbamate on ovulation and protaglandin synthesis in yellow perch (Perca flavescens) follicle incubates. Prostaglandins 48:11–20CrossRefPubMedGoogle Scholar
  4. Cetta F, Goetz FW (1982) Ovarian and plasma prostaglandin E and F levels in brook trout (Salvelinus fontinalis) during pituitary-induced ovulation. Biol Reprod 27:1216–1221CrossRefPubMedGoogle Scholar
  5. Chourasia TK, Joy KP (2012) Role of catecholestrogens on ovarian prostaglandin secretion in vitro in the catfish Heteropneustes fossilis and possible mechanism of regulation. Gen Comp Endocrinol 177:128–142CrossRefPubMedGoogle Scholar
  6. Criscuolo-Urbinati E, Kuradomi RY, Urbinati EC, Batlouni SR (2012) The administration of exogenous prostaglandin may improve ovulation in pacu (Piaractus mesopotamicus). Theriogenology 78:2087–2094CrossRefPubMedGoogle Scholar
  7. Fostier A, Weil C, Terqui M, Breton B, Jalabert B (1978) Plasma estradiol-17β and gonadotropin during ovulation in rainbow trout (Salmo gairdneri R.). Ann Biol Anim Biochim Biophys 18:929–936CrossRefGoogle Scholar
  8. Fujimori C, Ogiwara K, Hagiwara A, Rajapakse S, Kimura A, Takahashi T (2011) Expression of cyclooxygenase-2 and prostaglandin receptor EP4b mRNA in the ovary of the medaka fish, Oryzias latipes: possible involvement in ovulation. Mol Cell Endocrinol 332:67–77CrossRefPubMedGoogle Scholar
  9. Fujimori C, Ogiwara K, Hagiwara A, Takahashi T (2012) New evidence for the involvement of prostaglandin receptor EP4b in ovulation of the medaka, Oryzias latipes. Mol Cell Endocrinol 362:76–84CrossRefPubMedGoogle Scholar
  10. Goetz FW (1983) Hormonal control of oocyte final maturation and ovulation in fishes. In: Hoar WS, Randall DJ, Donaldson ΕΜ (eds) Fish physiology. Academic, New YorkGoogle Scholar
  11. Goetz FW, Theofan G (1979) In vitro stimulation of germinal vesicle breakdown and ovulation of yellow perch (Perca flavescens) oocytes. Effects of 17α-hydroxy-20β-dihydroprogesterone and prostaglandins. Gen Comp Endocrinol 37:273–285CrossRefPubMedGoogle Scholar
  12. Gohin M, Bodinier P, Fostier A, Chesnel F, Bobe J (2011) Aromatase is expressed and active in the rainbow trout oocyte during final oocyte maturation. Mol Reprod Dev 78:510–518CrossRefPubMedGoogle Scholar
  13. Hainfellner P, De Souza TG, Muños ME, Freitas GA, Batlouni SR (2012) Spawning failure in Brycon amazonicus may be associated with ovulation and not with final oocyte maturation. Arq Bras Med Vet Zootec 64:515–517CrossRefGoogle Scholar
  14. Hoogenboom MO, Metcalfe NB, Groothuis TGG, De Vries B, Costantini D (2012) Relationship between oxidative stress and circulating testosterone and cortisol in pre-spawning female brown trout. Comp Biochem Physiol A Mol Integr Physiol 163:379–387CrossRefPubMedGoogle Scholar
  15. Jalabert B, Fostier A (1984) The modulatory effectin vitro of oestradiol-17β, testosterone or cortisol on the output of 17α-hydroxy-20β dihydroprogesterone by rainbow trout (Salmo gairdneri) ovarian follicles stimulated by the maturational gonadotropin s-GtH. Reprod Nutr Dev 24:127–136CrossRefGoogle Scholar
  16. Jalabert B, Szöllösi D (1975) In vitro ovulation of trout oocytes: effect of prostaglandin on smooth muscle-like cells of the theca. Prostaglandins 9:765–779CrossRefPubMedGoogle Scholar
  17. Joy KP, Chaube R (2015) Vasotocin—a new player in the control of oocyte maturation and ovulation in fish. Gen Comp Endocrinol 221:54–63CrossRefPubMedGoogle Scholar
  18. Joy KP, Singh V (2013) Functional interactions between vasotocin and prostaglandins during final oocyte maturation and ovulation in the catfish Heteropneustes fossilis. Gen Comp Endocrinol 186:126–135CrossRefPubMedGoogle Scholar
  19. Kagawa H, Tanaka H, Unuma T, Ohta H, Geen K, Ozukawa K (2003) Role of prostaglandin in the control of ovulation in the Japanese eel Anguilla japonica. Fish Sci 69:234–241CrossRefGoogle Scholar
  20. Knight OM, Van Der Kraak G (2015) The role of eicosanoids in 17α, 20β-dihydroxy-4-pregnen-3-one-induced ovulation and spawning in Danio rerio. Gen Comp Endocrinol 213:50–58CrossRefPubMedGoogle Scholar
  21. Levavi-Sivan B, Vaiman R, Sachs O, Tzchori I (2004) Spawning induction and hormonal levels during final oocyte maturation in the silver perch (Bidyanus bidyanus). Aquaculture 229:419–431CrossRefGoogle Scholar
  22. Levavi-Zermonsky B, Yaron Z (1986) Changes in gonadotropin and ovarian steroids associated with oocytes maturation during spawning induction in the carp. Gen Comp Endocrinol 62:89–98CrossRefPubMedGoogle Scholar
  23. Lister AL, Van Der Kraak G (2008) An investigation into the role of prostaglandins in zebrafish oocyte maturation and ovulation. Gen Comp Endocrinol 159:46–57CrossRefPubMedGoogle Scholar
  24. Lubzens E, Young G, Bobe J, Cerda J (2010) Oogenesis in teleosts: how eggs are formed. Gen Comp Endocrinol 165:367–389CrossRefPubMedGoogle Scholar
  25. Malison JA, Procarione LS, Barry TP, Kapuscinski AR, Kayes TB (1994) Endocrine and gonadal changes during annual reproductive cycle of the freshwater teleost, Stizostedion vitreum. Fish Physiol Biochem 13:473–484CrossRefPubMedGoogle Scholar
  26. Mercure F, Van Der Kraak G (1995) Inhibition of gonadotropin stimulated ovarian steroid production by polyunsaturated fatty acids in teleost fish. Lipids 30:547–554CrossRefPubMedGoogle Scholar
  27. Mikolajczyk T, Sokosmallerska-Mikolajczyk M, Chyb J, Szczerbik P, Socha M, Foks M, Duc M, Epler P (2007) LH secretion and 17β-oestradiol concentration in the blood plasma and hypothalamus of goldfish (Carassius auratus gibelio B.) and common carp (Cyprinus carpio L.) treated with fadrozole (aromatase inhibitor) and GnRH analogues. Czech J Anim Sci 52:354–362CrossRefGoogle Scholar
  28. Moro GV, Rezende FP, Alves AL, Hashimoto DT, Varela ES, Torati LS (2013) Espécies de peixe para piscicultura. In: Rodrigues APO, Lima AF, Alves AL, Rosa DK, Torati LS, Santos VVR (eds) Piscicultura de água doce: Multiplicando conhecimentos, 1st edn. Embrapa, BrasíliaGoogle Scholar
  29. Mylonas CC, Fostier A, Zanuy S (2010) Broodstock management and hormonal manipulations of fish reproduction. Gen Comp Endocrinol 165:516–534CrossRefPubMedGoogle Scholar
  30. Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Develop Growth Differ 50:S195–S219CrossRefGoogle Scholar
  31. Ogata H, Nomura T, Hata M (1979) Prostaglandin F2 alfa changes induced by ovulatory stimuli in the pond loach, Misgurnus anguilicaudatus. Nippon Suisan Gakkai Shi 45:929–931CrossRefGoogle Scholar
  32. Ogiwara K, Takahashi T (2016) A dual role for melatonin in medaka ovulation: ensuring prostaglandin synthesis and actin cytoskeleton rearrangement in follicular cells. Biol Reprod 94:1–15CrossRefGoogle Scholar
  33. Pang Y, Thomas P (2010) Role of G protein-coupled estrogen receptor 1, GPER, in inhibition of oocyte maturation by endogenous estrogens in zebrafish. Dev Biol 342:194–206CrossRefPubMedPubMedCentralGoogle Scholar
  34. Pang Y, Dong J, Thomas P (2008) Estrogen signaling characteristics of Atlantic croaker G protein-coupled receptor 30 (GPR30) and evidence it is involved in maintenance of oocyte meiotic arrest. Endocrinology 149:3410–3426CrossRefPubMedPubMedCentralGoogle Scholar
  35. Pinter J, Thomas P (1999) Induction of ovulation of mature oocytes by the maturation-inducing steroid 17,20beta,21-trihydroxy-4-pregnen-3-one in the spotted seatrout. Gen Comp Endocrinol 115:200–209CrossRefPubMedGoogle Scholar
  36. Pottinger TG, Pickering AD, Hurley MA (1992) Consistency in the stress response of individuals of two strains of rainbow trout, Oncorhynchus mykiss. Aquaculture 103:275–289CrossRefGoogle Scholar
  37. Romagosa E, Paiva P, Godinho HM (1990) Pattern of oocyte diameter frequency distribution in females of the pacu, Piaractus mesopotamicus (Holmberg, 1887) (= Colossoma mitrei Berg, 1895), induced to spawn. Aquaculture 86:105–110CrossRefGoogle Scholar
  38. Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol 165:549–556CrossRefPubMedGoogle Scholar
  39. Senthilkumaran B, Yoshikuni M, Nagahama Y (2004) A shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. Mol Cell Endocrinol 215:11–18CrossRefPubMedGoogle Scholar
  40. Slater CH, Schreck CB, Swanson P (1994) Plasma profiles of the sex steroids and gonadotropins in maturing female spring Chinook salmon (Oncorhynchus tshawytscha). Comp Biochem Physiol A Mol Integr Physiol 109:167–175CrossRefGoogle Scholar
  41. Takahashi T, Fujimori C, Hagiwara A, Ogiwara K (2013) Recent advances in the understanding of teleost medaka ovulation: the roles of proteases and prostaglandins. Zool Sci 30:239–247CrossRefPubMedGoogle Scholar
  42. Theofan G, Goetz FW (1981) The in vitro effects of transcriptional and translational protein synthesis inhibitors on final maturation and ovulation of yellow perch (Perca flavescens) oocytes. Comp Biochem Physiol A Mol Integr Physiol 69:557–561CrossRefGoogle Scholar
  43. Van Der Kraak G, Chang J (1990) Arachidonic acid stimulates steroidogenesis in goldfish preovulatory ovarian follicles. Gen Comp Endocrinol 77:221–228CrossRefPubMedGoogle Scholar
  44. Wade M, Van Der Kraak G (1993) Arachidonic acid and prostaglandin E2 stimulate testosterone production by goldfish testis in vitro. Gen Comp Endocrinol 90:109–118CrossRefPubMedGoogle Scholar
  45. Yaron Z, Bogomolnaya A, Drori S, Biton I, Aizen J, Kulikovsky Z, Levavi-Sivan B (2009) Spawning induction in the carp. Past experience and future prospects—a review. Isr J Aquacult 61:5–26Google Scholar
  46. Zohar Y, Mylonas CC (2001) Endocrine manipulations of spawning in cultured fish: from hormones to genes. Aquaculture 197:99–136CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centro de Aquicultura da UNESP – CAUNESPUniversidade Estadual Paulista – UNESPJaboticabalBrazil
  2. 2.Programa de Pós-Graduação em AquiculturaUniversidade Nilton LinsManausBrazil

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