ECB-ART-41123
Development
2009 Jun 01;13611:1835-47. doi: 10.1242/dev.030775.
Show Gene links
Show Anatomy links
Extracellular matrix modifications at fertilization: regulation of dityrosine crosslinking by transamidation.
Wong JL
,
Wessel GM
.
???displayArticle.abstract???
Fertilization is accompanied by the construction of an extracellular matrix that protects the new zygote. In sea urchins, this structure is built from glycoproteins residing at the egg surface and in secretory vesicles at the egg cortex. Four enzymatic activities are required for the transformation of these proteins into the mechanically and chemically resilient fertilization envelope: proteolysis, transamidation, NADPH-dependent oxidation and peroxidation. Here, we identify the Strongylocentrotus purpuratus enzymes responsible for the formation of epsilon(gamma-glutamyl)lysine crosslinks (transamidation). We find that these two transglutaminases are activated by local acidification and act on specific substrates within the fertilization envelope (including ovoperoxidase, rendezvin and SFE9). Surprisingly, these enzymes also regulate dityrosine crosslinking both by direct conjugation of ovoperoxidase and by modulating hydrogen peroxide production. Together, these results emphasize how transglutaminases can coordinate the activities of other enzymes during extracellular matrix transmogrifications.
???displayArticle.pubmedLink??? 19403662
???displayArticle.pmcLink??? PMC2680108
???displayArticle.link??? Development
???displayArticle.grants??? [+]
T32 GM007601 NIGMS NIH HHS
Genes referenced: LOC100887844 LOC590297 op sfe9
???displayArticle.antibodies??? LOC590790 Ab3 tgm1 Ab1 tgml Ab1
References [+] :
Adány,
Factor XIII subunit A as an intracellular transglutaminase.
2003, Pubmed
Adány, Factor XIII subunit A as an intracellular transglutaminase. 2003, Pubmed
Aeschlimann, Protein crosslinking in assembly and remodelling of extracellular matrices: the role of transglutaminases. 2000, Pubmed
Antonyak, Two isoforms of tissue transglutaminase mediate opposing cellular fates. 2006, Pubmed
Arenas-Mena, Spatial expression of Hox cluster genes in the ontogeny of a sea urchin. 2000, Pubmed , Echinobase
Bakker, Two decades of screening for congenital hypothyroidism in The Netherlands: TPO gene mutations in total iodide organification defects (an update). 2000, Pubmed
Battaglia, Hierarchies of protein cross-linking in the extracellular matrix: involvement of an egg surface transglutaminase in early stages of fertilization envelope assembly. 1988, Pubmed , Echinobase
Bryan, On the reconstitution of the crystalline components of the sea urchin fertilization membrane. 1970, Pubmed , Echinobase
Candi, The cornified envelope: a model of cell death in the skin. 2005, Pubmed
Cariello, Effects of inhibiting transglutaminase during egg fertilization and development. 1994, Pubmed , Echinobase
Carroll, Isolation and biological activity of the proteases released by sea urchin eggs following fertilization. 1975, Pubmed , Echinobase
Carroll, Structure, assembly and function of the surface envelope (fertilization envelope) from eggs of the sea urchin, Strongylocentrotus purpuratus. 1986, Pubmed , Echinobase
Carroll, A novel procedure for obtaining denuded sea urchin eggs and observations on the role of the vitelline layer in sperm reception and egg activation. 1977, Pubmed , Echinobase
Chandler, Extracellular coats on the surface of Strongylocentrotus purpuratus eggs: stereo electron microscopy of quick-frozen and deep-etched specimens. 1986, Pubmed , Echinobase
Chandler, The vitelline layer of the sea urchin egg and its modification during fertilization. A freeze-fracture study using quick-freezing and deep-etching. 1980, Pubmed , Echinobase
Chandler, Membrane fusion during secretion: cortical granule exocytosis in sex urchin eggs as studied by quick-freezing and freeze-fracture. 1979, Pubmed , Echinobase
Chang, Cross-linking of ZP2 and ZP3 by transglutaminase is required for the formation of the outer layer of fertilization envelope of carp egg. 2002, Pubmed
Chen, More than one type of transglutaminase in invertebrates? A second type of transglutaminase is involved in shrimp coagulation. 2005, Pubmed
Coburn, A hydrogen peroxide block to polyspermy in the sea urchin Arbacia punctulata. 1981, Pubmed , Echinobase
Cooper, Cross linking of polyglutamine domains catalyzed by tissue transglutaminase is greatly favored with pathological-length repeats: does transglutaminase activity play a role in (CAG)(n)/Q(n)-expansion diseases? 2002, Pubmed
Davies, Protein damage and degradation by oxygen radicals. IV. Degradation of denatured protein. 1987, Pubmed
Davies, Protein damage and degradation by oxygen radicals. II. Modification of amino acids. 1987, Pubmed
Deits, Purification and properties of ovoperoxidase, the enzyme responsible for hardening the fertilization membrane of the sea urchin egg. 1984, Pubmed , Echinobase
Deits, Conformational control of ovoperoxidase catalysis in the sea urchin fertilization membrane. 1986, Pubmed , Echinobase
Deits, pH-induced hysteretic transitions of ovoperoxidase. 1985, Pubmed , Echinobase
Detering, Isolation and characterization of plasma membrane-associated cortical granules from sea urchin eggs. 1977, Pubmed , Echinobase
Epel, Methods for revoval of the vitelline membrane of sea urchin eggs. I. Use of dithiothreitol (Cleland Reagent). 1970, Pubmed , Echinobase
Esposito, Mammalian transglutaminases. Identification of substrates as a key to physiological function and physiopathological relevance. 2005, Pubmed
Foerder, Hydrogen peroxide production, chemiluminescence, and the respiratory burst of fertilization: interrelated events in early sea urchin development. 1978, Pubmed , Echinobase
Foerder, Release of ovoperoxidase from sea urchin eggs hardens the fertilization membrane with tyrosine crosslinks. 1977, Pubmed , Echinobase
Fridovich, Oxygen toxicity: a radical explanation. 1998, Pubmed
Griffin, Transglutaminases: nature's biological glues. 2002, Pubmed
Ha, Enzyme responsible for egg envelope (chorion) hardening in fish: purification and partial characterization of two transglutaminases associated with their substrate, unfertilized egg chorion, of the rainbow trout, Oncorhynchus mykiss. 1998, Pubmed
Haley, Regulated proteolysis by cortical granule serine protease 1 at fertilization. 2004, Pubmed , Echinobase
Haley, The cortical granule serine protease CGSP1 of the sea urchin, Strongylocentrotus purpuratus, is autocatalytic and contains a low-density lipoprotein receptor-like domain. 1999, Pubmed , Echinobase
Hall, Hardening of the sea urchin fertilization envelope by peroxidase-catalyzed phenolic coupling of tyrosines. 1978, Pubmed , Echinobase
Heinecke, Mass spectrometric quantification of amino acid oxidation products in proteins: insights into pathways that promote LDL oxidation in the human artery wall. 1999, Pubmed
Iijima, Comprehensive sequence analysis of horseshoe crab cuticular proteins and their involvement in transglutaminase-dependent cross-linking. 2005, Pubmed
Inoue, Fine structure of the fertilization membranes of sea urchin embryos. 1971, Pubmed , Echinobase
Jacob, Human phagocytes employ the myeloperoxidase-hydrogen peroxide system to synthesize dityrosine, trityrosine, pulcherosine, and isodityrosine by a tyrosyl radical-dependent pathway. 1996, Pubmed
Karlsson, Proteomic analysis of the Drosophila larval hemolymph clot. 2004, Pubmed
Kay, Ovoperoxidase assembly into the sea urchin fertilization envelope and dityrosine crosslinking. 1987, Pubmed , Echinobase
Kinsey, Purification and properties of the egg plasma membrane. 1986, Pubmed , Echinobase
LaFleur, Sea urchin ovoperoxidase: oocyte-specific member of a heme-dependent peroxidase superfamily that functions in the block to polyspermy. 1998, Pubmed , Echinobase
Lambeth, Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. 2007, Pubmed
Larabell, Fertilization-induced changes in the vitelline envelope of echinoderm and amphibian eggs: self-assembly of an extracellular matrix. 1991, Pubmed , Echinobase
Levine, Oxidative modification of proteins during aging. 2001, Pubmed
Lindsay, Proteolysis of Xenopus laevis egg envelope ZPA triggers envelope hardening. 2004, Pubmed
Lorand, Transglutaminases: crosslinking enzymes with pleiotropic functions. 2003, Pubmed
Matese, Regulated exocytosis and sequential construction of the extracellular matrix surrounding the sea urchin zygote. 1997, Pubmed , Echinobase
Mhaouty-Kodja, Ghalpha/tissue transglutaminase 2: an emerging G protein in signal transduction. 2004, Pubmed
Mian, The importance of the GTP-binding protein tissue transglutaminase in the regulation of cell cycle progression. 1995, Pubmed
Moreno, Inactivating mutations in the gene for thyroid oxidase 2 (THOX2) and congenital hypothyroidism. 2002, Pubmed
Morgan, Fertilization and nicotinic acid adenine dinucleotide phosphate induce pH changes in acidic Ca(2+) stores in sea urchin eggs. 2007, Pubmed , Echinobase
Mozingo, Ultrastructure of the proteoliaisin-ovoperoxidase complex and its spatial organization within the Strongylocentrotus purpuratus fertilization envelope. 1994, Pubmed , Echinobase
Mozingo, Evidence for the existence of two assembly domains within the sea urchin fertilization envelope. 1991, Pubmed , Echinobase
Nagahara, Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. 1998, Pubmed
Negoescu, F(ab) secondary antibodies: a general method for double immunolabeling with primary antisera from the same species. Efficiency control by chemiluminescence. 1994, Pubmed
Nemes, Structure-function relationships of transglutaminases--a contemporary view. 2005, Pubmed
Oppen-Berntsen, The major structural proteins of cod (Gadus morhua) eggshells and protein crosslinking during teleost egg hardening. 1990, Pubmed
Paul, Fertilization acid of sea urchin eggs is not a consequence of cortical granule exocytosis. 1976, Pubmed , Echinobase
Piacentini, "Tissue" transglutaminase in animal development. 2000, Pubmed
Santiago, Intermolecular cross-linking of vitelline envelope polypeptides predominates in the hardened sea urchin fertilization envelope. 1987, Pubmed , Echinobase
Showman, Removal of the fertilization membrane of sea urchin embryos employing aminotriazole. 1979, Pubmed , Echinobase
Smith, Low pH inhibits compensatory endocytosis at a step between depolarization and calcium influx. 2002, Pubmed , Echinobase
Sodergren, The genome of the sea urchin Strongylocentrotus purpuratus. 2006, Pubmed , Echinobase
Somers, Localization and developmental fate of ovoperoxidase and proteoliaisin, two proteins involved in fertilization envelope assembly. 1989, Pubmed , Echinobase
Song, Oogenesis: single cell development and differentiation. 2006, Pubmed , Echinobase
Turner, The relationship between a novel NAD(P)H oxidase activity of ovoperoxidase and the CN- -resistant respiratory burst that follows fertilization of sea urchin eggs. 1985, Pubmed , Echinobase
Verderio, Tissue transglutaminase in normal and abnormal wound healing: review article. 2004, Pubmed
Veron, Sequential biochemical and morphological events during assembly of the fertilization membrane of the sea urchin. 1977, Pubmed , Echinobase
Waffenschmidt, Isodityrosine cross-linking mediates insolubilization of cell walls in Chlamydomonas. 1993, Pubmed
Waffenschmidt, A transglutaminase immunologically related to tissue transglutaminase catalyzes cross-linking of cell wall proteins in Chlamydomonas reinhardtii. 1999, Pubmed
Wang, Inhibitory actions of diphenyleneiodonium on endothelium-dependent vasodilatations in vitro and in vivo. 1993, Pubmed
Weidman, Assembly of the sea urchin fertilization membrane: isolation of proteoliaisin, a calcium-dependent ovoperoxidase binding protein. 1985, Pubmed , Echinobase
Wessel, A protein of the sea urchin cortical granules is targeted to the fertilization envelope and contains an LDL-receptor-like motif. 1995, Pubmed , Echinobase
Wessel, A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. 1984, Pubmed
Wessel, A molecular analysis of hyalin--a substrate for cell adhesion in the hyaline layer of the sea urchin embryo. 1998, Pubmed , Echinobase
Wessel, Two embryonic, tissue-specific molecules identified by a double-label immunofluorescence technique for monoclonal antibodies. 1986, Pubmed , Echinobase
Winterbourn, Myeloperoxidase. 2000, Pubmed
Wong, The oxidative burst at fertilization is dependent upon activation of the dual oxidase Udx1. 2004, Pubmed , Echinobase
Wong, Rendezvin: An essential gene encoding independent, differentially secreted egg proteins that organize the fertilization envelope proteome after self-association. 2006, Pubmed , Echinobase
Wong, Defending the zygote: search for the ancestral animal block to polyspermy. 2006, Pubmed
Wong, Free-radical crosslinking of specific proteins alters the function of the egg extracellular matrix at fertilization. 2008, Pubmed , Echinobase
Wong, Membrane hemifusion is a stable intermediate of exocytosis. 2007, Pubmed , Echinobase
Wong, Major components of a sea urchin block to polyspermy are structurally and functionally conserved. 2004, Pubmed , Echinobase
Yamagami, Molecular and cellular basis of formation, hardening, and breakdown of the egg envelope in fish. 1992, Pubmed