Prophase I Mouse Oocytes Are Deficient in the Ability to Respond to Fertilization by Decreasing Membrane Receptivity to Sperm and Establishing a Membrane Block to Polyspermy

• Published in: Biology of reproduction Vol. 89; no. 2; p. 44
• Main Authors: KRYZAK, Cassie A, MORAINE, Maia M, KYLE, Diane D, LEE, Hyo J, CUBENAS-POTTS, Caelin, ROBINSON, Douglas N, EVANS, Janice P
• Format: Journal Article
• Language: English
• Published: Madison, WI Society for the Study of Reproduction 01.08.2013
• Subjects: Animals; Biological and medical sciences; Cell Membrane - physiology; Female; Fertilization - physiology; Fundamental and applied biological sciences. Psychology; Male; Meiotic Prophase I - physiology; Metaphase - physiology; Mice; Oocytes - physiology; Sperm-Ovum Interactions - physiology; Vertebrates: reproduction; Zona Pellucida - physiology; block to polyspermy; Spermatozoa; Polyspermy; Rodentia; Germinal cell; activation competence; Vertebrata; Reproduction; Mammalia; Mouse; Animal; CD9; cytoplasmic maturation; Fertilization membrane; Oocyte; polyspermy
• ISSN: 0006-3363; 1529-7268
• DOI: 10.1095/biolreprod.113.110221

Changes occurring as the prophase I oocyte matures to metaphase II are critical for the acquisition of competence for normal egg activation and early embryogenesis. A prophase I oocyte cannot respond to a fertilizing sperm as a metaphase II egg does, including the ability to prevent polyspermic fertilization. Studies here demonstrate that the competence for the membrane block to polyspermy is deficient in prophase I mouse oocytes. In vitro fertilization experiments using identical insemination conditions result in monospermy in 87% of zona pellucida (ZP)-free metaphase II eggs, while 92% of ZP-free prophase I oocytes have four or more fused sperm. The membrane block is associated with a postfertilization reduction in the capacity to support sperm binding, but this reduction in sperm-binding capacity is both less robust and slower to develop in fertilized prophase I oocytes. Fertilization of oocytes is dependent on the tetraspanin CD9, but little to no release of CD9 from the oocyte membrane is detected, suggesting that release of CD9-containing vesicles is not essential for fertilization. The deficiency in membrane block establishment in prophase I oocytes correlates with abnormalities in two postfertilization cytoskeletal changes: sperm-induced cortical remodeling that results in fertilization cone formation and a postfertilization increase in effective cortical tension. These data indicate that cortical maturation is a component of cytoplasmic maturation during the oocyte-to-egg transition and that the egg cortex has to be appropriately primed and tuned to be responsive to a fertilizing sperm.