Mammalian oocyte activation by the synergistic action of discrete sperm head components: induction of calcium transients and involvement of proteolysis.
Sperm-borne oocyte-activating factor (SOAF) elicits activation sufficient for full development and originates from sperm head submembrane matrices. SOAF comprises discrete, heat-sensitive and -stable components (referred to here respectively as SOAF-I and -II) which are each necessary but not sufficient to activate oocytes. The heat-sensitive SOAF component, SOAF-I(m), becomes solubilized from the perinuclear matrix under reducing conditions (the SOAF transition) to generate SOAF-I(s). Although calcium transients likely play an important role in oocyte activation at fertilization, the question is open as to whether demembranated heads or SOAF-I(s) and/or SOAF-II can induce calcium transients. We now report that injection of demembranated sperm heads into mouse oocytes efficiently induced Ca(2+) oscillations. When injected independently, SOAF-I(s) and demembranated heads heated to 48 degrees C failed to generate Ca(2+) oscillations. However, co-injection of SOAF-I(s) and 48 degrees C-heated heads induced oscillations, mirroring their synergistic ability to activate oocytes. This suggests that SOAF-mediated activation proceeds via pathways resembling those at fertilization and provides the first direct evidence that multiple sperm components are required to induce Ca(2+) oscillations. We probed the SOAF-I(s) liberation at the center of this activation and show that in vitro it was sensitive to a profile of serine protease inhibitors. These findings support a model in which mammalian oocyte activation, including the induction of calcium transients, involves proteolytic processing of SOAF from sperm head submembrane compartments.
Perry
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AC
Laboratory of Vertebrate Developmental Neurogenetics, Rockefeller University, 1230 York Avenue, New York, New York, 10021-6399, USA. perrya@rockvax.rockefeller.edu
Wakayama
T
T
Cooke
I M
IM
Yanagimachi
R
R
D000818:Animals; D020013:Calcium Signaling; D005260:Female; D008297:Male; D008540:Meiosis; D008677:Metaphase; D051379:Mice; D008954:Models, Biological; D009865:Oocytes / Q000502:physiology*; D010507:Periodicity; D011506:Proteins / Q000378:metabolism; D012697:Serine Endopeptidases / Q000378:metabolism; D015842:Serine Proteinase Inhibitors / Q000378:metabolism; D013077:Sperm Head / Q000502:physiology*; D013084:Sperm-Ovum Interactions / Q000502:physiology*
D011506:Proteins; D015842:Serine Proteinase Inhibitors; D012697:Serine Endopeptidases