Fish Physiology and Biochemistry

, Volume 43, Issue 2, pp 527–537 | Cite as

Evidences for involvement of growth hormone and insulin-like growth factor in ovarian development of starry flounder (Platichthys stellatus)

  • Yongjiang Xu
  • Bin Wang
  • Xuezhou Liu
  • Bao Shi
  • Kun Zang
Article

Abstract

Although gonadotrophins are major regulators of ovarian function in teleosts and other vertebrates, accumulating evidence indicates that the growth hormone (GH)-insulin-like growth factor (IGF) axis also plays an important role in fish reproduction. As a first step to understand the physiological role of the GH-IGF system in the ovarian development of starry flounder (Platichthys stellatus), the expression profiles of GH and IGF messenger RNAs (mRNAs) and plasma GH, IGF-I, estradiol-17β (E2), and testosterone (T) levels during the ovarian development were investigated. The developmental stages of ovaries were divided into five stages (II, III, IV, V, and VI) by histological analysis. The hepatosomatic index (HSI) and gonadosomatic index (GSI) values increased and peaked at stage IV and stage V, respectively, and then declined at stage VI. Pituitary GH mRNA levels decreased sharply at stage III and raised to top level at stage VI. The hepatic IGF-I mRNA levels ascended to maximum value at stage V and then declined significantly at stage VI. However, the hepatic IGF-II mRNA levels remained stable and increased significantly at stage VI. In contrast, the ovarian IGF-I mRNA levels increased gradually and peaked at stage VI. The ovarian IGF-II mRNA levels were initially stable and increased significantly at stage V until the top level at stage VI. Consistent with the pituitary GH mRNA levels, plasma GH levels reduced sharply at stage III and remained depressed until stage V and then raised remarkably at stage VI. Plasma IGF-I level peaked at stage V and then declined to initial level. Plasma E2 level peaked at stage IV and then dramatically descended to the basal level. Plasma T level peaked at stage V and then declined significantly back to the basal level. Based on statistical analysis, significant positive correlations between hepatic IGF-I mRNA and GSI, ovarian IGF-II mRNA and hepatic IGF-II mRNA, ovarian IGF-I mRNA and ovarian IGF-II mRNA, and plasma IGF-I and plasma T were observed, respectively. These results suggest that the GH-IGF system may be involved in the ovarian development of starry flounder; GH and IGFs appear to play distinct roles in the regulation of the ovarian development in paracrine/autocrine manners. These findings extend our knowledge of the roles of the GH-IGF axis on reproduction regulation in fish.

Keywords

Ovarian development Growth hormone Insulin-like growth factor Starry flounder 

Notes

Acknowledgments

This work was supported by grants from the National High Technology Research and Development Program of China (2012AA10A413) and the China Agriculture Research System (CARS-50).

Compliance with ethical standards

All of the animal experiments were approved by the Animal Care and Use Committee of Chinese Academy of Fishery Sciences.

References

  1. Baroiller JF, D’Cotta H, Shved N, Berishvili G, Toguyeni A, Fostier A, Eppler E, Reinecke M (2014) Oestrogen and insulin-like growth factors during the reproduction and growth of the tilapia Oreochromis niloticus and their interactions. Gen Comp Endocrinol 205:142–150CrossRefPubMedGoogle Scholar
  2. Beckman BR (2011) Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes. Gen Comp Endocrinol 170:233–252CrossRefPubMedGoogle Scholar
  3. Berishvili G, Baroiller JF, Eppler E, Reinecke M (2010) Insulin-like growth factor-3 (IGF-3) in male and female gonads of the tilapia: development and regulation of gene expression by growth hormone (GH) and 17alpha-ethinylestradiol (EE2). Gen Comp Endocrinol 167:128–134CrossRefPubMedGoogle Scholar
  4. Berishvili G, D’Cotta H, Baroiller JF, Segner H, Reinecke M (2006) Differential expression of IGF-I mRNA and peptide in the male and female gonad during early development of a bony fish, the tilapia Oreochromis niloticus. Gen Comp Endocrinol 146:204–210CrossRefPubMedGoogle Scholar
  5. Bevers MM, Izadyar F (2002) Role of growth hormone and growth hormone receptor in oocyte maturation. Mol Cell Endocrinol 197:173–178CrossRefPubMedGoogle Scholar
  6. Biga PR, Schelling GT, Hardy RW, Cain KD, Overturf K, Ott TL (2004) The effects of recombinant bovine somatotropin (rbST) on tissue IGF-I, IGF-I receptor, and GH mRNA levels in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 135:324–333CrossRefPubMedGoogle Scholar
  7. Bobe J, Maugars G, Nguyen T, Rime H, Jalabert B (2003) Rainbow trout follicular maturational competence acquisition is associated with an increased expression of follicle stimulating hormone receptor and insulin-like growth factor 2 messenger RNAs. Mol Reprod Dev 66:46–53CrossRefPubMedGoogle Scholar
  8. Bobe J, Nguyen T, Jalabert B (2004) Targeted gene expression profiling in the rainbow trout (Oncorhynchus mykiss) ovary during maturational competence acquisition and oocyte maturation. Biol Reprod 71:73–82CrossRefPubMedGoogle Scholar
  9. Canosa LF, Chang JP, Peter RE (2007) Neuroendocrine control of growth hormone in fish. Gen Comp Endocrinol 151:1–26CrossRefPubMedGoogle Scholar
  10. Chang JP, Habibi HR, Yu Y, Moussavi M, Grey CL, Pemberton JG (2012) Calcium and other signalling pathways in neuroendocrine regulation of somatotroph functions. Cell Calcium 51:240–252CrossRefPubMedGoogle Scholar
  11. Dahle R, Taranger GL, Karlsen O, Kjesbu OS, Norberg B (2003) Gonadal development and associated changes in liver size and sexual steroids during the reproductive cycle of captive male and female Atlantic cod (Gadus morhua L.). Comp Biochem Physiol A Mol Integr Physiol 136:641–653CrossRefPubMedGoogle Scholar
  12. Davis LK, Hiramatsu N, Hiramatsu K, Reading BJ, Matsubara T, Hara A, Sullivan CV, Pierce AL, Hirano T, Grau EG (2007) Induction of three vitellogenins by 17beta-estradiol with concurrent inhibition of the growth hormone-insulin-like growth factor 1 axis in a euryhaline teleost, the tilapia (Oreochromis mossambicus). Biol Reprod 77:614–625CrossRefPubMedGoogle Scholar
  13. Duan C, Duguay SJ, Plisetskaya EM (1993) Insulin-like growth factor I (IGF-I) mRNA expression in coho salmon, Oncorhynchus kisutch: tissue distribution and effects of growth hormone/prolactin family proteins. Fish Physiol Biochem 11:371–379CrossRefPubMedGoogle Scholar
  14. Duguay SJ, Swanson P, Dickhoff WW (1994) Differential expression and hormonal regulation of alternatively spliced IGF-I mRNA transcripts in salmon. J Mol Endocrinol 12:25–37CrossRefPubMedGoogle Scholar
  15. Gahete MD, Duran-Prado M, Luque RM, Martinez-Fuentes AJ, Quintero A, Gutierrez-Pascual E, Cordoba-Chacon J, Malagon MM, Gracia-Navarro F, Castano JP (2009) Understanding the multifactorial control of growth hormone release by somatotropes: lessons from comparative endocrinology. Ann N Y Acad Sci 1163:137–153CrossRefPubMedGoogle Scholar
  16. Garcia-Lopez A, Couto E, Canario AV, Sarasquete C, Martinez-Rodriguez G (2007) Ovarian development and plasma sex steroid levels in cultured female Senegalese sole Solea senegalensis. Comp Biochem Physiol A Mol Integr Physiol 146:342–354CrossRefPubMedGoogle Scholar
  17. Gioacchini G, Cardinali M, Maradonna F, Funkenstein B, Mosconi G, Carnevali O (2005) Hormonal control of the IGF system in the sea bream ovary. Ann N Y Acad Sci 1040:320–322CrossRefPubMedGoogle Scholar
  18. Gomez JM, Mourot B, Fostier A, Le Gac F (1999) Growth hormone receptors in ovary and liver during gametogenesis in female rainbow trout (Oncorhynchus mykiss). J Reprod Fertil 115:275–285CrossRefPubMedGoogle Scholar
  19. Harmin S, Crim L, Wiegand M (1995) Plasma sex steroid profiles and the seasonal reproductive cycle in male and female winter flounder, Pleuronectes americanus. Mar Biol 121:601–610CrossRefGoogle Scholar
  20. Hull KL, Harvey S (2014) Growth hormone and reproduction: a review of endocrine and autocrine/paracrine interactions. Int J Endocrinol 2014:234014CrossRefPubMedPubMedCentralGoogle Scholar
  21. Johnson LL, Casillas E, Myers MS, Rhodes LD, Olson OP (1991) Patterns of oocyte development and related changes in plasma 17-β estradiol, vitellogenin, and plasma chemistry in English sole Parophrys vetulus Girard. J Exp Mar Biol Ecol 152:161–185CrossRefGoogle Scholar
  22. 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 68:1562–1568CrossRefPubMedGoogle Scholar
  23. Kagawa H, Kobayashi M, Hasegawa Y, Aida K (1994) Insulin and insulin-like growth factors I and II induce final maturation of oocytes of red seabream, Pagrus major, in vitro. Gen Comp Endocrinol 95:293–300CrossRefPubMedGoogle Scholar
  24. Kagawa H, Moriyama S, Kawauchi H (1995) Immunocytochemical localization of IGF-I in the ovary of the red seabream, Pagrus major. Gen Comp Endocrinol 99:307–315CrossRefPubMedGoogle Scholar
  25. Kajimura S, Kawaguchi N, Kaneko T, Kawazoe I, Hirano T, Visitacion N, Grau EG, Aida K (2004) Identification of the growth hormone receptor in an advanced teleost, the tilapia (Oreochromis mossambicus) with special reference to its distinct expression pattern in the ovary. J Endocrinol 181:65–76CrossRefPubMedGoogle Scholar
  26. Larsson DG, Mayer I, Hyllner SJ, Forlin L (2002) Seasonal variations of vitelline envelope proteins, vitellogenin, and sex steroids in male and female eelpout (Zoarces viviparus). Gen Comp Endocrinol 125:184–196CrossRefPubMedGoogle Scholar
  27. Lee W-K, Yang S-W (2002) Relationship between ovarian development and serum levels of gonadal steroid hormones, and induction of oocyte maturation and ovulation in the cultured female Korean spotted sea bass Lateolabrax maculatus (Jeom-nong-eo). Aquaculture 207:169–183CrossRefGoogle Scholar
  28. Li J, Chu L, Sun X, Liu Y, Cheng CH (2015) IGFs mediate the action of LH on oocyte maturation in zebrafish. Mol Endocrinol 29:373–383CrossRefPubMedPubMedCentralGoogle Scholar
  29. Li J, Liu Z, Wang D, Cheng CH (2011) Insulin-like growth factor 3 is involved in oocyte maturation in zebrafish. Biol Reprod 84:476–486CrossRefPubMedGoogle Scholar
  30. Lokman PM, George KA, Divers SL, Algie M, Young G (2007) 11-Ketotestosterone and IGF-I increase the size of previtellogenic oocytes from shortfinned eel, Anguilla australis, in vitro. Reproduction 133:955–967CrossRefPubMedGoogle Scholar
  31. Lubzens E, Young G, Bobe J, Cerda J (2010) Oogenesis in teleosts: how eggs are formed. Gen Comp Endocrinol 165:367–389CrossRefPubMedGoogle Scholar
  32. Maddock D, Burton M (1998) Gross and histological observations of ovarian development and related condition changes in American plaice. J Fish Biol 53:928–944CrossRefGoogle Scholar
  33. Maestro MA, Planas JV, Moriyama S, Gutierrez J, Planas J, Swanson P (1997) Ovarian receptors for insulin and insulin-like growth factor I (IGF-I) and effects of IGF-I on steroid production by isolated follicular layers of the preovulatory coho salmon ovarian follicle. Gen Comp Endocrinol 106:189–201CrossRefPubMedGoogle Scholar
  34. Micale V, Maricchiolo G, Genovese L (1999) The reproductive biology of the amberjack, Seriola dumerilii (Risso 1810). I. Oocyte development in captivity. Aquac Res 30:349–355CrossRefGoogle Scholar
  35. Moriyama S, Ayson FG, Kawauchi H (2000) Growth regulation by insulin-like growth factor-I in fish. Biosci Biotechnol Biochem 64:1553–1562CrossRefPubMedGoogle Scholar
  36. Onuma TA, Makino K, Ban M, Ando H, Fukuwaka MA, Azumaya T, Swanson P, Urano A (2009) Elevation of the plasma level of insulin-like growth factor-I with reproductive maturation prior to initiation of spawning migration of chum salmon. Ann N Y Acad Sci 1163:497–500CrossRefPubMedGoogle Scholar
  37. Perrot V, Moiseeva EB, Gozes Y, Chan SJ, Funkenstein B (2000) Insulin-like growth factor receptors and their ligands in gonads of a hermaphroditic species, the gilthead seabream (Sparus aurata): expression and cellular localization. Biol Reprod 63:229–241CrossRefPubMedGoogle Scholar
  38. Picha ME, Shi B, Thomas P (2012) Dual role of IGF-II in oocyte maturation in southern flounder Paralichthys lethostigma: up-regulation of mPRalpha and resumption of meiosis. Gen Comp Endocrinol 177:220–230CrossRefPubMedGoogle Scholar
  39. Reindl KM, Sheridan MA (2012) Peripheral regulation of the growth hormone-insulin-like growth factor system in fish and other vertebrates. Comp Biochem Physiol A Mol Integr Physiol 163:231–245CrossRefPubMedGoogle Scholar
  40. Reinecke M (2010) Insulin-like growth factors and fish reproduction. Biol Reprod 82:656–661CrossRefPubMedGoogle Scholar
  41. Schmid AC, Naf E, Kloas W, Reinecke M (1999) Insulin-like growth factor-I and -II in the ovary of a bony fish, Oreochromis mossambicus, the tilapia: in situ hybridisation, immunohistochemical localisation, Northern blot and cDNA sequences. Mol Cell Endocrinol 156:141–149CrossRefPubMedGoogle Scholar
  42. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108CrossRefPubMedGoogle Scholar
  43. Scott P, Witthames P, Turner R, Canario AV (1998) Plasma concentrations of ovarian steroids in relation to oocyte final maturation and ovulation in female plaice sampled at sea. J Fish Biol 52:128–145CrossRefGoogle Scholar
  44. Shi B, Liu X, Xu Y, Wang S (2015) Molecular characterization of three gonadotropin subunits and their expression patterns during ovarian maturation in Cynoglossus semilaevis. Int J Mol Sci 16:2767–2793CrossRefPubMedPubMedCentralGoogle Scholar
  45. Silva JR, Figueiredo JR, van den Hurk R (2009) Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 71:1193–1208CrossRefPubMedGoogle Scholar
  46. Singh H, Thomas P (1993) Mechanism of stimulatory action of growth hormone on ovarian steroidogenesis in spotted seatrout, Cynoscion nebulosus. Gen Comp Endocrinol 89:341–353CrossRefPubMedGoogle Scholar
  47. Sol SY, Olson O, Lomax D, Johnson LL (1998) Gonadal development and associated changes in plasma reproductive steroids in English sole, Pleuronectes vetulus, from Puget sound, Washington. Fishery Bulletin-National Oceanic and Atmospheric Administration 96:859–870Google Scholar
  48. Sundararaj BI, Goswami SV, Lamba VJ (1982) Role of testosterone, estradiol-17β, and cortisol during vitellogenin synthesis in the catfish, Heteropneustes fossilis (Bloch). Gen Comp Endocrinol 48:390–397CrossRefPubMedGoogle Scholar
  49. Van der Kraak G, Rosenblum PM, Peter RE (1990) Growth hormone-dependent potentiation of gonadotropin-stimulated steroid production by ovarian follicles of the goldfish. Gen Comp Endocrinol 79:233–239CrossRefPubMedGoogle Scholar
  50. Wang B, Jia J, Yang G, Qin J, Zhang C, Zhang Q, Sun C, Li W (2015) In vitro effects of somatostatin on the growth hormone-insulin-like growth factor axis in orange-spotted grouper (Epinephelus coioides). Gen Comp Endocrinol. doi: 10.1016/j.ygcen.2015.1010.1014 Google Scholar
  51. Wang B, Qin C, Zhang C, Jia J, Sun C, Li W (2014) Differential involvement of signaling pathways in the regulation of growth hormone release by somatostatin and growth hormone-releasing hormone in orange-spotted grouper (Epinephelus coioides). Mol Cell Endocrinol 382:851–859CrossRefPubMedGoogle Scholar
  52. Wang D-S, Jiao B, Hu C, Huang X, Liu Z, Cheng CH (2008) Discovery of a gonad-specific IGF subtype in teleost. Biochem Biophys Res Commun 367:336–341CrossRefPubMedGoogle Scholar
  53. Weber GM, Moore AB, Sullivan CV (2007) In vitro actions of insulin-like growth factor-I on ovarian follicle maturation in white perch (Morone americana). Gen Comp Endocrinol 151:180–187CrossRefPubMedGoogle Scholar
  54. Weber GM, Sullivan CV (2000) Effects of insulin-like growth factor-I on in vitro final oocyte maturation and ovarian steroidogenesis in striped bass, Morone saxatilis. Biol Reprod 63:1049–1057CrossRefPubMedGoogle Scholar
  55. Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285CrossRefPubMedGoogle Scholar
  56. Wuertz S, Gessner J, Kirschbaum F, Kloas W (2007) Expression of IGF-I and IGF-I receptor in male and female sterlet, Acipenser ruthenus—evidence for an important role in gonad maturation. Comp Biochem Physiol A Mol Integr Physiol 147:223–230CrossRefPubMedGoogle Scholar
  57. Xu Y, Zang K, Liu X, Shi B, Li C, Shi X (2015) Insulin-like growth factors I and II in starry flounder (Platichthys stellatus): molecular cloning and differential expression during embryonic development. Fish Physiol Biochem 41:139–152CrossRefPubMedGoogle Scholar
  58. Xu YJ, Liu XZ, Liao MJ, Wang HP, Wang QY (2012) Molecular cloning and differential expression of three GnRH genes during ovarian maturation of spotted halibut, Verasper variegatus. J Exp Zool A Ecol Genet Physiol 317:434–446CrossRefPubMedGoogle Scholar
  59. Zang K, Liu X, Xu Y, Zhang K, Shi B, Shi X, Li C (2014) Molecular cloning and in vitro expression of growth hormone gene from Platichthys stellatus. J Fish China 38:1230–1242Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research InstituteChinese Academy of Fishery SciencesQingdaoChina
  2. 2.Laboratory for Marine Fisheries and AquacultureQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.College of Fisheries and Life ScienceShanghai Ocean UniversityShanghaiChina

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