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Abstract
Consisting of Kit ligand and receptor Kit, the Kit system is involved in regulating many ovarian functions such as follicle activation, granulosa cell proliferation, and oocyte growth and maturation. In mammals, Kit ligand is derived from the granulosa cells and Kit receptor is expressed in the oocyte and theca cells. In the zebrafish, the Kit system contains two ligands (Kitlga and Kitlgb) and two receptors (Kita and Kitb). Interestingly, Kitlga and Kitb are localized in the somatic follicle cells, but Kitlgb and Kita are expressed in the oocyte. Using recombinant zebrafish Kitlga and Kitlgb, we demonstrated that Kitlga preferentially activated Kita whereas Kitlgb specifically activated Kitb by Western analysis for receptor phosphorylation. In support of this, Kitlgb triggered a stronger and longer MAPK phosphorylation in follicle cells than Kitlga, whereas Kitlga but not Kitlgb activated MAPK in the denuded oocytes, in agreement with the distribution of Kita and Kitb in the follicle and their specificity for Kitlga and Kitlgb. Further analysis of the interaction between Kit ligands and receptors by homology modeling showed that Kitlga-Kita and Kitlgb-Kitb both have more stable electrostatic interaction than Kitlgb-Kita or Kitlga-Kitb. A functional study of Kit involvement in final oocyte maturation showed that Kitlga and Kitlgb both suppressed the spontaneous maturation significantly; in contrast, Kitlgb but not Kitlga significantly promoted 17α, 20β-dihydroxy-4-pregnen-3-one (DHP) -induced oocyte maturation. Our results provided strong evidence for a Kit-mediated bi-directional communication system in the zebrafish ovarian follicle, which could be part of the complex interplay between the oocyte and the follicle cells in the development of follicles.
Highlights
Kit ligand, referred to as stem cell factor (SCF), mast cell growth factor (MGF) or steel factor (SF), is the product of the Steel (Sl) locus in mice [1,2,3] and its receptor, Kit, is encoded by the White Spotting (W) locus [2,3,4,5,6,7]
Spatial distribution of Kit system within the follicle Zebrafish ovarian follicle consists of two compartments: a developing oocyte in the center and a surrounding thin follicle layer of somatic cells containing the granulosa and theca cells
Consistent with our previous reports [37], lhcgr was exclusively expressed in the somatic follicle cells whereas the expression of gdf9 was restricted in the oocyte
Summary
Referred to as stem cell factor (SCF), mast cell growth factor (MGF) or steel factor (SF), is the product of the Steel (Sl) locus in mice [1,2,3] and its receptor, Kit, is encoded by the White Spotting (W) locus [2,3,4,5,6,7]. It has been documented in mammals that Kit ligand is involved in promoting growth and survival of oocytes [10,11,12,13] but maintaining the arrest of meiosis [14,15] by direct activation of Kit on the oocytes. These effects represent part of the mechanisms by which the follicle cells support the development of oocytes, which has long been considered an example of granulosa cell-tooocyte communication in the ovarian follicle. It has been postulated that Kit ligand may exert its mitogenic effect on the granulosa cells indirectly by inducing an oocyte-derived factor that in turn acts on the granulosa cells [17]
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