Fertilization‐Induced changes in the vitelline envelope of echinoderm and amphibian eggs: Self‐assembly of an extracellular matrix

Abstract

The surface of the unfertilized sea urchin egg is covered by the vitelline layer (VL), a fibrous extracellular matrix that contains receptors for sperm. At fertilization, cortical granule exocytosis releases enzymes and structural proteins that cause the VL to elevate and become remodelled into the mechanically and chemically tough fertilization envelope. This envelope prevents further penetration of sperm and protects the embryo during early development. A thicker, more complex vitelline envelope surrounds the Xenopus laevis egg. This fibrous coat is also restructured at fertilization to produce an impenetrable barrier to sperm. The biochemical steps that occur during self-assembly of these fertilization envelopes are reviewed, and the ultrastructural changes that occur, as seen in platinum replicas of quick-frozen, deep-etched, and rotary-shadowed eggs, are illustrated.

The Primary Egg Envelope of the Anuran Lepidobatrachus laevis: Physicochemical and Macromolecular Alterations During Development

“…Surprisingly, the Lepidobatrachus VE and the FE were very similar in structure. The tangled fibers of the VE were not modified to form concentric layers as noted in Xenopus (19), and an electron dense F layer was not evident in the Lepidobatrachus FE.…”

Extracellular matrix modifications at fertilization: regulation of dityrosine crosslinking by transamidation

“…When these modifications are absent or go awry, however, the associated changes can gravely affect tissue integrity such that overall health is at risk. The absence of transamidation negatively impacts the survival of some animal zygotes (Battaglia and Shapiro, 1988; Chandler and Kazilek, 1986; Chang et al, 2002;Ha and Iuchi, 1998;Larabell and Chandler, 1991;Mozingo and Chandler, 1991;Oppen-Berntsen et al, 1990;Veron et al, 1977;Yamagami et al, 1992). Similarly, inhibition of an extracellular transglutaminase blocks normal peroxidase-dependent isodityrosine crosslinking of Chlamydomonas reinhardtii cell walls, which is lethal to the single cell alga (Waffenschmidt et al, 1999;Waffenschmidt et al, 1993).…”

“…ε(γ-glutamyl)lysine crosslinks are the major contributor to teleost chorion hardening (Chang et al, 2002;Ha and Iuchi, 1998;OppenBerntsen et al, 1990;Yamagami et al, 1992), and are associated with morphological changes on the surface of the sea urchin fertilization envelope (Battaglia and Shapiro, 1988;Chandler and Kazilek, 1986;Larabell and Chandler, 1991;Mozingo and Chandler, 1991;Veron et al, 1977). The fertilization envelope establishes a physical block to polyspermy that protects the zygote from environmental and microbial agents Wong and Wessel, 2006a).…”

“…Together, Udx1 and ovoperoxidase crosslink the proteins found throughout the fertilization envelope, thereby establishing the permeability of this zygotic extracellular matrix Veron et al, 1977;Wong and Wessel, 2008). Inter-protein crosslinking occurs in two discrete subdomains of the fertilization envelope: first at the microvillar casts, the segments of the vitelline layer that cover the egg microvilli, followed by the intercast region, the area between the microvillar casts (Chandler and Kazilek, 1986;Larabell and Chandler, 1991;Mozingo and Chandler, 1991). Transamidation of proteins localized at microvillar casts is associated with the morphological change from a rounded ('igloo') to a pointed ('tent') shape (e.g.…”

“…Within the first 2 minutes of fertilization (Larabell and Chandler, 1991), (3) a surfaceassociated population of eTG activates Udx1 while (4) the remaining transglutaminases are released with the vitelline layer. As cortical granule structural proteins are woven into the vitelline layer, active transglutaminases retained at the microvillar casts mediate the I-to-T transmogrification, crosslinking microvillar cast proteins such as SFE9 (Wessel, 1995) prior to any crosslinking of the intercast regions (Chandler and Heuser, 1980;Larabell and Chandler, 1991). Transglutaminases in the intercast region or in solution modify (or are modified by) active ovoperoxidase tethered within the fertilization envelope; the parallel profiles of transamidation and dityrosine crosslinking within the first 2 minutes of fertilization (Fig.…”