Santella L et al. (2020), Cellular and molecular aspects of oocyte matura...

ECB-ART-49861

Zoological Lett 2020 Jan 01;6:5. doi: 10.1186/s40851-020-00157-5.

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Cellular and molecular aspects of oocyte maturation and fertilization: a perspective from the actin cytoskeleton.

Santella L , Limatola N , Chun JT .

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ABSTRACT: Much of the scientific knowledge on oocyte maturation, fertilization, and embryonic development has come from the experiments using gametes of marine organisms that reproduce by external fertilization. In particular, echinoderm eggs have enabled the study of structural and biochemical changes related to meiotic maturation and fertilization owing to the abundant availability of large and transparent oocytes and eggs. Thus, in vitro studies of oocyte maturation and sperm-induced egg activation in starfish are carried out under experimental conditions that resemble those occurring in nature. During the maturation process, immature oocytes of starfish are released from the prophase of the first meiotic division, and acquire the competence to be fertilized through a highly programmed sequence of morphological and physiological changes at the oocyte surface. In addition, the changes in the cortical and nuclear regions are essential for normal and monospermic fertilization. This review summarizes the current state of research on the cortical actin cytoskeleton in mediating structural and physiological changes during oocyte maturation and sperm and egg activation in starfish and sea urchin. The common denominator in these studies with echinoderms is that exquisite rearrangements of the egg cortical actin filaments play pivotal roles in gamete interactions, Ca2+ signaling, exocytosis of cortical granules, and control of monospermic fertilization. In this review, we also compare findings from studies using invertebrate eggs with what is known about the contributions made by the actin cytoskeleton in mammalian eggs. Since the cortical actin cytoskeleton affects microvillar morphology, movement, and positioning of organelles and vesicles, and the topography of the egg surface, these changes have impacts on the fertilization process, as has been suggested by recent morphological studies on starfish oocytes and eggs using scanning electron microscopy. Drawing the parallelism between vitelline layer of echinoderm eggs and the zona pellucida of mammalian eggs, we also discuss the importance of the egg surface in mediating monospermic fertilization.

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	Fig. 1. Light microscopy images of the ovary, and of living oocytes from the starfish Patiria pectinifera before and after 1-methyladenine (1-MA) treatment. a A ripe ovary dissected from P. pectinifera, containing numerous fully grown immature oocytes. b Immature oocytes isolated from the ovary are surrounded by a layer of follicle cells (FC); the large nucleus termed germinal vesicle (GV) is visible in the cytoplasm. c Maturing oocytes treated with 1-MA for 50 min; at this point in maturation, the FC are clustered to one side of the oocytes. This is the optimal time at which eggs can be successfully fertilized (i.e., monospermic fertilization). d Fertilized eggs 3 min after insemination are surrounded by the fertilization envelope (FE) as a result of the cortical granules exocytosis. e In the absence of fertilization, the first polar body (PB) forms 65 to 75 min after 1-MA application. f Extrusion of the second polar body 105 to 115 min after fertilization of eggs matured for 50 min with 1-MA (arrow)
	Fig. 2. Scanning electron micrographs of the surface of immature, mature and overripe eggs of P. pectinifera before and after fertilization. a An immature oocyte showing the projections of the follicle cells (FC, arrows) penetrating the vitelline layer (VL). b Polyspermic fertilization of an immature oocyte. Note the formation of the fertilization cones made by a large number of long microvilli protruding from the porous VL (arrows) and capturing the multiple sperm for their incorporation. c An oocyte treated with 1-MA for 50 min showing the VL without the openings characteristically present in the surface of immature oocytes in A. d The surface of a control egg fertilized at its optimal period of maturation (50 min 1-MA treatment) shows that, at variance with the multiple sperm penetration in immature oocytes shown in B, only the fertilizing sperm is captured by cytoplasmic protrusions emanating from the fertilization envelope (FE) (arrow). Note the different structure of the fertilization cone which is formed at this stage of maturation. e The structural modification of the VL of the overripe eggs makes this envelope more similar to that of immature oocytes and its openings. f Multiple sperm penetration (arrows) through the FE in an overripe egg upon insemination
	Fig. 3. Scanning and transmission electron micrographs of immature oocytes and mature eggs before and after fertilization. a A fractured immature oocyte showing microvilli (M) beneath the vitelline layer (VL) and organelles in the cytoplasm. b Microvilli project from the oocyte’s surface into the VL. Cortical granules (CG). c A mature egg treated with 1-MA for 50 min. At this optimal period of fertilizability, microvilli (M) beneath the VL are shorter. d The ultrastructure of a mature egg stimulated with 1-MA for 50 min shows shortened microvilli (M) and cortical granules (CG) positioned beneath the egg surface. e Fertilization envelope (FE) elevation in a mature egg 3 min after insemination showing the spherical bodies (arrow) in the perivitelline space following CG exocytosis. Hyaline layer (HL). f The electron-dense spherical bodies of the CG in the egg surface before fertilization in D are now seen in the perivitelline space (PS) upon insemination. Same magnification in all figures
	Fig. 4. Acrosome reaction in P. pectinifera spermatozoa and the sperm-induced Ca2+ responses in the egg. a Scanning electron microscopy micrographs of spermatozoa fixed in natural seawater without eggs. No sign of acrosome reaction is present. bP. pectinifera spermatozoa on the egg surface after acrosome reaction has taken place (see the long filamentous process, AP). c Ca2+ signals in a mature egg of Astropecten aranciacus following the interaction of the tip of the AP with the egg surface. A simultaneous increase of Ca2+ over the entire periphery of the egg (cortical flash, CF) is observed when the fertilizing sperm head (marked in red dot) is still in the outer jelly coat (JC) (t = 0:17). This Ca2+ increase is followed by a Ca2+ wave that starts from the sperm-egg interaction and propagates to the opposite side of the egg, while the head of the sperm is still far away from the egg surface (t = 0:20). Only after the Ca2+ wave has spread globally to the opposite side do sperm become incorporated into the egg by passing through the FE
	Fig. 5. F-actin staining in living A. aranciacus oocytes at different maturation stages and calcium responses upon insemination. a Confocal image of the F-actin in an immature oocyte (GV-stage). A network of actin filaments is visible in the cytoplasm of oocytes not treated with 1-MA. b Reorganization of F-actin following 1-MA stimulation: The cytoplasmic F-actin network seen in a is no longer visible. At this stage of maturation (70 min of hormonal treatment) the actin fibers are perpendicular to the egg surface. c Alteration of the cortical actin in an overripe egg (1-MA treatment for 6 h) as evidenced by the irregular layer of the cortical F-actin as compared to that in b. Note the absence of the actin fibres perpendicularly oriented at the egg surface. a’ Ca2+ response of an immature polyspermic oocyte upon insemination. Two Ca2+ waves (arrowheads) that converge to the centre of the oocyte precede the release of Ca2+ in the oocyte cortex (CF, arrow). b’ Egg treated with 1-MA for 70 min experience a normal Ca2+ response with a CF (arrow) which precedes the single Ca2+ wave. c′ Two Ca2+ waves (arrowheads) as a result of polyspermic fertilization in overripe eggs inseminated 6 h after hormonal treatment
	Fig. 6. Confocal images of the cortical actin cytoskeleton in starfish oocytes fertilized at different meiotic stages. Immature oocytes, mature eggs and overripe eggs of A. aranciacus were microinjected with Alexa Fluor 568 phalloidin. a F-actin staining of the fertilization cones in a polyspermic immature oocyte. Note the large number of actin bundles composing the fertilization cones that will incorporate the sperm in the absence of a FE elevation shown in the overlay image in a’. b A mature monospermic egg fertilized in its optimal stage of maturation (70 min 1-MA treatment) that shows a fertilization cone. Note the initiation of the centripetal translocation of individual actin fibres at the subplasmalemmal zone and the elevation of the FE in the overlay image in b′ as a result of the CG exocytosis. c Reorganization of the F-actin in an overripe egg fertilized after 6 h hormonal treatment. Note that the centripetal translocation seen in fertilized mature eggs is absent in overripe eggs upon insemination. c′) Image overlay showing the fertilization envelope (FE) elevation and incorporation of sperm in the egg (arrowhead). Multiple spermatozoa enter even in the presence of normal elevation of FE

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Albertini, The developmental origins of mammalian oocyte polarity. 2004, Pubmed