Membrane molecule bouncer regulates sperm binding activity in immature oocytes in the viviparous teleost species Poecilia reticulata (guppy)

• Published in: Development, growth & differentiation growth & differentiation, 2024-04, Vol.66 (3), p.194-204
• Main Authors: Yoshida, Junki, Tajika, Yuki, Uchida, Kazuko, Kuwahara, Makoto, Sano, Kaori, Suzuki, Takayuki, Hondo, Eiichi, Iida, Atsuo
• Format: Article
• Language: English
• Subjects: Animals; Danio rerio; Ectopic expression; Female; Fertilization; internal fertilization; Male; Oocytes; Oocytes - metabolism; Oryzias; Ovulation; Poecilia - physiology; Poecilia reticulata; Semen; spaca4l; Sperm; Spermatozoa; sperm–egg binding; U-Plasminogen activator; viviparous teleost; Zebrafish
• ISSN: 0012-1592; 1440-169X
• DOI: 10.1111/dgd.12914

Generally, in vertebrates, the first step toward fertilization is the ovulation of mature oocytes, followed by their binding to sperm cells outside of the ovary. Exceptionally, the oocytes of poeciliid fish are fertilized by sperm cells within the follicle, and the developmental embryo is subsequently released into the ovarian lumen before delivery. In the present study, we aimed to identify the factor(s) responsible for intrafollicular fertilization in a viviparous teleost species, Poecilia reticulata (guppy). Sperm tracking analysis in this regard indicated that in this species, sperm cells reached immature oocytes including the germinal vesicle, and the insemination assay indicated that the immature oocytes robustly adhered to the sperm cells; similar binding was not observed in Danio rerio (zebrafish) and Oryzias latipes (medaka). We also identified the Ly6/uPAR protein bouncer as the factor responsible for the observed sperm binding activity of the immature oocytes in this species. The recombinant bouncer peptide acted as an inhibitory decoy for the sperm–oocyte binding in guppy. On the other hand, ectopic expression of guppy bouncer in zebrafish oocytes resulted in interspecific sperm–oocyte binding. These results argue that bouncer is responsible for sperm–immature oocyte binding. Our findings highlight the unique reproductive strategies of guppy fish and enhance our understanding of the diverse reproductive mechanisms in vertebrates. Previtellogenic oocytes in the follicle possess sperm binding activity in guppy. The immature oocyte–sperm binding is not observed in medaka and zebrafish. Bouncer, a GPI anchor protein, plays a critical role in the sperm–oocyte binding of guppy.