Evidences for involvement of growth hormone and insulin-like growth factor in ovarian development of starry flounder (Platichthys stellatus)
- 253 Downloads
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.
KeywordsOvarian development Growth hormone Insulin-like growth factor Starry flounder
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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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