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. 1979 Apr 1;149(4):938–953. doi: 10.1084/jem.149.4.938

Metabolic similarities between fertilization and phagocytosis. Conservation of a peroxidatic mechanism

PMCID: PMC2184842  PMID: 372484

Abstract

At the time of fertilization, sea urchin eggs release a peroxidase which, together with H2O2 generated by a respiratory burst, is responsible for hardening of the fertilization membrane. We demonstrate here that the ovoperoxidase of unfertilized eggs is located in cortical granules and, after fertilization, is concentrated in the fertilization membrane. Fertilization of sea urchin eggs or their parthenogenetic activation with the ionophor A23187 also results in (a) the conversion of iodide to a trichloroacetic acid-precipitable form (iodination), (b) the deiodination of eggs exogenously labeled with myeloperoxidase and H2O2, (c) the degradation of thyroxine as measured by the recovery of the released radioiodine at the origin and in the inorganic iodide spot on paper chromatography, and (d) the conversion of estradiol to an alcohol-precipitable form (estrogen binding). The iodination reaction and the binding of estradio occurs predominantly in the fertilization membrane where the ovoperoxidase is concentrated. From the estimation of the kinetics of incorporation of iodine, we determine that the peroxidative system is active for 30 min after fertilization, long after hardening of the fertilization membrane is complete. Most of the bound iodine is lost during the hatching process. Iodination of albumin is catalyzed by the material released from the egg during fertilization, when combined with H2O2 and iodide. Iodination, thyroxine degradation, and estradiol binding are inhibited by azide, cyanide, aminotriazole, methimazole, ascorbic acid and ergothioneine, all of which can inhibit peroxidase-catalyzed reactions. These responses of the sea urchin egg to fertilization are strikingly similar to the changes induced in polymorphonuclear leukocytes by phagocytosis and, in both instances, a peroxidative mechanism may be involved.

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Selected References

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  1. Allen R. C., Stjernholm R. L., Steele R. H. Evidence for the generation of an electronic excitation state(s) in human polymorphonuclear leukocytes and its participation in bactericidal activity. Biochem Biophys Res Commun. 1972 May 26;47(4):679–684. doi: 10.1016/0006-291x(72)90545-1. [DOI] [PubMed] [Google Scholar]
  2. Baehner R. L., Johnston R. B., Jr Monocyte function in children with neutropenia and chronic infections. Blood. 1972 Jul;40(1):31–41. [PubMed] [Google Scholar]
  3. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  4. Bujak J. S., Root R. K. The role of peroxidase in the bactericidal activity of human blood eosinophils. Blood. 1974 May;43(5):727–736. [PubMed] [Google Scholar]
  5. Eddy E. M., Shapiro B. M. Changes in the topography of the sea urchin egg after fertilization. J Cell Biol. 1976 Oct;71(1):35–48. doi: 10.1083/jcb.71.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Epel D. Methods for removal of the vitelline membrane of sea urchin eggs. II. Controlled exposure to trypsin to eliminate post-fertilization clumping of embryos. Exp Cell Res. 1970 Jul;61(1):69–70. doi: 10.1016/0014-4827(70)90258-2. [DOI] [PubMed] [Google Scholar]
  7. Foerder C. A., Klebanoff S. J., Shapiro B. M. Hydrogen peroxide production, chemiluminescence, and the respiratory burst of fertilization: interrelated events in early sea urchin development. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3183–3187. doi: 10.1073/pnas.75.7.3183. [DOI] [PMC free article] [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. Hall H. G. Hardening of the sea urchin fertilization envelope by peroxidase-catalyzed phenolic coupling of tyrosines. Cell. 1978 Oct;15(2):343–355. doi: 10.1016/0092-8674(78)90003-x. [DOI] [PubMed] [Google Scholar]
  10. Isono N., Yasumasu I. Pathways of carbohydrate breakdown in sea urchin eggs. Exp Cell Res. 1968 Jun;50(3):616–626. doi: 10.1016/0014-4827(68)90423-0. [DOI] [PubMed] [Google Scholar]
  11. Jensen M. S., Bainton D. F. Temporal changes in pH within the phagocytic vacuole of the polymorphonuclear neutrophilic leukocyte. J Cell Biol. 1973 Feb;56(2):379–388. doi: 10.1083/jcb.56.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Katsura S., Tominaga A. Peroxidatic activity of catalase in the cortical granules of sea urchin eggs. Dev Biol. 1974 Oct;40(2):292–297. doi: 10.1016/0012-1606(74)90131-6. [DOI] [PubMed] [Google Scholar]
  13. Klebanoff S. J. Antimicrobial mechanisms in neutrophilic polymorphonuclear leukocytes. Semin Hematol. 1975 Apr;12(2):117–142. [PubMed] [Google Scholar]
  14. Klebanoff S. J., Clark R. A. Iodination by human polymorphonuclear leukocytes: a re-evaluation. J Lab Clin Med. 1977 Mar;89(3):675–686. [PubMed] [Google Scholar]
  15. Klebanoff S. J. Estrogen binding by leukocytes during phagocytosis,. J Exp Med. 1977 Apr 1;145(4):983–998. doi: 10.1084/jem.145.4.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Klebanoff S. J., Green W. L. Degradation of thyroid hormones by phagocytosing human leukocytes. J Clin Invest. 1973 Jan;52(1):60–72. doi: 10.1172/JCI107174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Klebanoff S. J. Iodination of bacteria: a bactericidal mechanism. J Exp Med. 1967 Dec 1;126(6):1063–1078. doi: 10.1084/jem.126.6.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Morrison M., Schonbaum G. R. Peroxidase-catalyzed halogenation. Annu Rev Biochem. 1976;45:861–888. doi: 10.1146/annurev.bi.45.070176.004241. [DOI] [PubMed] [Google Scholar]
  19. Rous P. THE RELATIVE REACTION WITHIN LIVING MAMMALIAN-TISSUES : II. ON THE MOBILIZATION OF ACID MATERIAL WITHIN CELLS, AND THE REACTION AS INFLUENCED BY THE CELL STATE. J Exp Med. 1925 Feb 28;41(3):399–411. doi: 10.1084/jem.41.3.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. SBARRA A. J., KARNOVSKY M. L. The biochemical basis of phagocytosis. I. Metabolic changes during the ingestion of particles by polymorphonuclear leukocytes. J Biol Chem. 1959 Jun;234(6):1355–1362. [PubMed] [Google Scholar]
  21. Shapiro B. M. Limited proteolysis of some egg surface components is an early event following fertilization of the sea urchin, Strongylocentrotus purpuratus. Dev Biol. 1975 Sep;46(1):88–102. doi: 10.1016/0012-1606(75)90089-5. [DOI] [PubMed] [Google Scholar]
  22. Smith D. C., Klebanoff S. J. A uterine fluid-mediated sperm-inhibitory system. Biol Reprod. 1970 Oct;3(2):229–235. doi: 10.1093/biolreprod/3.2.229. [DOI] [PubMed] [Google Scholar]
  23. Taurog A. Thyroid peroxidase and thyroxine biosynthesis. Recent Prog Horm Res. 1970;26:189–247. doi: 10.1016/b978-0-12-571126-5.50009-1. [DOI] [PubMed] [Google Scholar]
  24. 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]

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