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. 1988 Dec 1;107(6):2447–2454. doi: 10.1083/jcb.107.6.2447

Hierarchies of protein cross-linking in the extracellular matrix: involvement of an egg surface transglutaminase in early stages of fertilization envelope assembly

PMCID: PMC2115685  PMID: 2904448

Abstract

The involvement of transglutaminase activity in fertilization envelope (FE) formation was investigated using eggs from the sea urchin, Strongylocentrotus purpuratus. Eggs fertilized in the presence of the transglutaminase inhibitors, putrescine and cadaverine, had disorganized and expanded FEs with inhibition of the characteristic I-T transition. The permeability of the FE was increased by these agents, as revealed by the loss of proteins from the perivitelline space and the appearance of ovoperoxidase activity in supernates from putrescine- treated eggs. [3H]putrescine was incorporated into the FE during fertilization in a reaction catalyzed by an egg surface transglutaminase that could also use dimethylcasein as a substrate in vitelline layer-denuded eggs. Egg secretory products alone had no transglutaminase activity. The cell surface transglutaminase activity was transient and maximal within 4 min of activation. The enzyme was Ca2+ dependent and was inhibited by Zn2+. We conclude that sea urchin egg surface transglutaminase catalyzes an early step in a hierarchy of cross-linking events during FE assembly, one that occurs before ovoperoxidase-mediated dityrosine formation (Foerder, C. A., and B. M. Shapiro. 1977. Proc. Natl. Acad. Sci. USA. 74:4214-4218). Thus it provides a graphic example of the physiological function of a cell surface transglutaminase.

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Selected References

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  1. Alliegro M. C., Schuel H. Immunocytochemical localization of the 35-kDa sea urchin egg trypsin-like protease and its effects upon the egg surface. Dev Biol. 1988 Jan;125(1):168–180. doi: 10.1016/0012-1606(88)90069-3. [DOI] [PubMed] [Google Scholar]
  2. Cariello L., Wilson J., Lorand L. Activation of transglutaminase during embryonic development. Biochemistry. 1984 Dec 18;23(26):6843–6850. doi: 10.1021/bi00321a087. [DOI] [PubMed] [Google Scholar]
  3. Carroll E. J., Jr, Epel D. Elevation and hardening of the fertilization membrane in sea urchin eggs. Role of the soluble fertilization product. Exp Cell Res. 1975 Feb;90(2):429–432. doi: 10.1016/0014-4827(75)90332-8. [DOI] [PubMed] [Google Scholar]
  4. Carroll E. J., Jr, Epel D. Isolation and biological activity of the proteases released by sea urchin eggs following fertilization. Dev Biol. 1975 May;44(1):22–32. doi: 10.1016/0012-1606(75)90373-5. [DOI] [PubMed] [Google Scholar]
  5. Chandler D. E., Heuser J. The vitelline layer of the sea urchin egg and its modification during fertilization. A freeze-fracture study using quick-freezing and deep-etching. J Cell Biol. 1980 Mar;84(3):618–632. doi: 10.1083/jcb.84.3.618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chandler D. E., Kazilek C. J. Extracellular coats on the surface of Strongylocentrotus purpuratus eggs: stereo electron microscopy of quick-frozen and deep-etched specimens. Cell Tissue Res. 1986;246(1):153–161. doi: 10.1007/BF00219012. [DOI] [PubMed] [Google Scholar]
  7. Cocuzzi E. T., Chung S. I. Cellular transglutaminase. Lung matrix-associated transglutaminase: characterization and activation with sulfhydryls. J Biol Chem. 1986 Jun 25;261(18):8122–8127. [PubMed] [Google Scholar]
  8. Foerder C. A., Shapiro B. M. Release of ovoperoxidase from sea urchin eggs hardens the fertilization membrane with tyrosine crosslinks. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4214–4218. doi: 10.1073/pnas.74.10.4214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fuller G. M., Doolittle R. F. Studies of invertebrate fibrinogen. II. Transformation of lobster fibrinogen into fibrin. Biochemistry. 1971 Apr 13;10(8):1311–1315. doi: 10.1021/bi00784a006. [DOI] [PubMed] [Google Scholar]
  10. Juprelle-Soret M., Wattiaux-De Coninck S., Wattiaux R. Subcellular localization of transglutaminase. Effect of collagen. Biochem J. 1988 Mar 1;250(2):421–427. doi: 10.1042/bj2500421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kay E. S., Shapiro B. M. Ovoperoxidase assembly into the sea urchin fertilization envelope and dityrosine crosslinking. Dev Biol. 1987 Jun;121(2):325–334. doi: 10.1016/0012-1606(87)90168-0. [DOI] [PubMed] [Google Scholar]
  12. LORAND L., DOOLITTLE R. F., KONISHI K., RIGGS S. K. A NEW CLASS OF BLOOD COAGULATION INHIBITORS. Arch Biochem Biophys. 1963 Aug;102:171–179. doi: 10.1016/0003-9861(63)90168-1. [DOI] [PubMed] [Google Scholar]
  13. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  14. Lallier R. A. Formation of fertilization membrane in sea urchin eggs. Exp Cell Res. 1970 Dec;63(2):460–462. doi: 10.1016/0014-4827(70)90239-9. [DOI] [PubMed] [Google Scholar]
  15. Lallier R. Effects of various inhibitors of protein cross-linking on the formation of fertilization membrane in sea urchin egg. Experientia. 1971;27(11):1323–1324. doi: 10.1007/BF02136716. [DOI] [PubMed] [Google Scholar]
  16. Lorand L., Conrad S. M. Transglutaminases. Mol Cell Biochem. 1984;58(1-2):9–35. doi: 10.1007/BF00240602. [DOI] [PubMed] [Google Scholar]
  17. Lorand L. Fibrinoligase: the fibrin-stabilizing factor system of blood plasma. Ann N Y Acad Sci. 1972 Dec 8;202:6–30. doi: 10.1111/j.1749-6632.1972.tb16319.x. [DOI] [PubMed] [Google Scholar]
  18. Lorand L., Parameswaran K. N., Stenberg P., Tong Y. S., Velasco P. T., Jönsson N. A., Mikiver L., Moses P. Specificity of guinea pig liver transglutaminase for amine substrates. Biochemistry. 1979 May 1;18(9):1756–1765. doi: 10.1021/bi00576a019. [DOI] [PubMed] [Google Scholar]
  19. Schroeder T. E. Surface area change at fertilization: resorption of the mosaic membrane. Dev Biol. 1979 Jun;70(2):306–326. doi: 10.1016/0012-1606(79)90030-7. [DOI] [PubMed] [Google Scholar]
  20. Slife C. W., Dorsett M. D., Bouquett G. T., Register A., Taylor E., Conroy S. Subcellular localization of a membrane-associated transglutaminase activity in rat liver. Arch Biochem Biophys. 1985 Sep;241(2):329–336. doi: 10.1016/0003-9861(85)90554-5. [DOI] [PubMed] [Google Scholar]
  21. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985 Oct;150(1):76–85. doi: 10.1016/0003-2697(85)90442-7. [DOI] [PubMed] [Google Scholar]
  22. Tyrrell D. J., Sale W. S., Slife C. W. Localization of a liver transglutaminase and a large molecular weight transglutaminase substrate to a distinct plasma membrane domain. J Biol Chem. 1986 Nov 5;261(31):14833–14836. [PubMed] [Google Scholar]
  23. Veron M., Foerder C., Eddy E. M., Shapiro Sequential biochemical and morphological events during assembly of the fertilization membrane of the sea urchin. Cell. 1977 Feb;10(2):321–328. doi: 10.1016/0092-8674(77)90226-4. [DOI] [PubMed] [Google Scholar]
  24. Weidman P. J., Kay E. S., Shapiro B. M. Assembly of the sea urchin fertilization membrane: isolation of proteoliaisin, a calcium-dependent ovoperoxidase binding protein. J Cell Biol. 1985 Mar;100(3):938–946. doi: 10.1083/jcb.100.3.938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Weidman P. J., Shapiro B. M. Regulation of extracellular matrix assembly: in vitro reconstitution of a partial fertilization envelope from isolated components. J Cell Biol. 1987 Jul;105(1):561–567. doi: 10.1083/jcb.105.1.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Williams-Ashman H. G., Notides A. C., Pabalan S. S., Lorand L. Transamidase reactions involved in the enzymic coagulation of semen: isolation of -glutamyl- -lysine dipeptide from clotted secretion protein of guinea pig seminal vesicle. Proc Natl Acad Sci U S A. 1972 Aug;69(8):2322–2325. doi: 10.1073/pnas.69.8.2322. [DOI] [PMC free article] [PubMed] [Google Scholar]

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