Previtellogenic Oocyte Growth in Salmon: Relationships among Body Growth, Plasma Insulin-Like Growth Factor-1, Estradiol-17beta, Follicle-Stimulating Hormone and Expression of Ovarian Genes for Insulin-Like Growth Factors, Steroidogenic-Acute Regulatory Protein and Receptors for Gonadotropins, Growth Hormone, and Somatolactin1

Abstract

Body growth during critical periods is known to be an important factor in determining the age of maturity and fecundity in fish. However, the endocrine mechanisms controlling oogenesis in fish and the effects of growth on this process are poorly understood. In this study interactions between the growth and reproductive systems were examined by monitoring changes in various components of the FSH-ovary axis, plasma insulin-like growth factor 1 (Igf1), and ovarian gene expression in relation to body and previtellogenic oocyte growth in coho salmon. Samples were collected from females during two hypothesized critical periods when growth influences maturation in this species. Body growth during the fall-spring months was strongly related to the degree of oocyte development, with larger fish possessing more advanced oocytes than smaller, slower growing fish. The accumulation of cortical alveoli in the oocytes was associated with increases in plasma and pituitary FSH, plasma estradiol-17beta, and ovarian steroidogenic acute regulatory protein (star) gene expression, whereas ovarian transcripts for growth hormone receptor and somatolactin receptor decreased. As oocytes accumulated lipid droplets, a general increase occurred in plasma Igf1 and components of the FSH-ovary axis, including plasma FSH, estradiol-17beta, and ovarian mRNAs for gonadotropin receptors, star, igf1, and igf2. A consistent positive relationship between plasma Igf1, estradiol-17beta, and pituitary FSH during growth in the spring suggests that these factors are important links in the mechanism by which body growth influences the rate of oocyte development.

Gh is produced by the testis of Japanese eel and stimulates proliferation of spermatogonia

“…In addition to these roles, Gh has been implicated, directly and indirectly, in the regulation of reproductive processes in several vertebrate taxa. In salmonid fishes, several studies have shown that growth rate at critical periods determines whether animals will undergo gonadal maturation and initiation of spermatogenesis or secondary ovarian follicle growth, an effect that may be mediated through plasma levels of Igf (Campbell et al 2003(Campbell et al , 2006. Gh and Igf1 have also been shown to act on the gonad to stimulate steroid production (Lubzens et al 2010, Schulz et al 2010 and Igf1 is involved in the regulation of final oocyte maturation (Lubzens et al 2010).…”

Gonads directly regulate growth in teleosts

“…In general, reproduction is closely related to body growth (5)(6)(7)(8), and gonads are recognized as important organs for growth. However, few examples showing a clear relationship between the gonad and body growth have been published.…”

Changes in the plasma levels of insulin-like growth factor-I from the onset of spawning migration through upstream migration in chum salmon

“…They estimated growth history from annuli of scales in hatchery-arrived chum salmon, and showed that the recent growth rate is the most important factor for oceanic fish to determine whether mature or not mature in the subsequent spawning period. Since the plasma levels of IGF-I correlated well with the growth rates and body sizes in immature and early maturing salmonids (Beckman et al, 1998;Shimizu et al, 2000;Campbell et al, 2003;Campbell et al, 2006), the plasma IGF-I levels may be an important somatotropic signal that interrelated with the onset of spawning migration.…”

“…A possible explanation for this discrepancy is that gonads themselves influence circulating IGF-I levels, because the gonads are suggested to be one of the sources of IGF-I (Le Gac et al, 1996;Campbell et al, 2006), and actually express GH receptors (Fukada et al, 2005). The role of developing gonads in IGF-I secretion remains to be clarified.…”

“…The previous studies in salmonid reproduction established that the plasma levels of insulin-like growth factor I (IGF-I), a liver polypeptide that acts as a mediator of growth-promoting action of growth hormone (GH) in teleost fishes (Duan and Hirano, 1992), are increased with body growth during winter and spring, and the seasonal increase in circulating IGF-I was linked to initiation of gametogenesis in male chinook salmon (Campbell et al, 2003) and female coho salmon (Campbell et al, 2006). We thus hypothesized that IGF-I might be involved in reproductive maturation of oceanic chum salmon.…”