Sea urchin ovoperoxidase: oocyte-specific member of a heme-dependent peroxidase superfamily that functions in the block to polyspermy
Open accessAbstract
Ovoperoxidase is one of several oocyte-specific proteins that are stored within sea urchin cortical granules, released during the cortical reaction, and incorporated into the newly formed fertilization envelope. Ovoperoxidase plays a particularly important role in this process, crosslinking the envelope into a hardened matrix that is insensitive to biochemical and mechanical challenges and thus providing a permanent block to polyspermy. Here we present the primary structures of two ovoperoxidases as predicted from cDNAs cloned from the sea urchins Strongylocentrotus purpuratus (AF035380) and Lytechinus variegatus (AF035381). We also present a proposed scheme for the post-translational processing of ovoperoxidase based upon comparisons between the cDNA and protein structures and taking into account previously published reports. The sea urchin ovoperoxidase sequences conform to a profile shared by members of a heme-dependent animal peroxidase family, including the mammalian myelo-, lacto-, eosinophil, and thyroid peroxidases. Using in situ RNA hybridizations, we showed that the mRNA of S. purpuratus ovoperoxidase (4 kb) is present exclusively in oocytes, and is turned over rapidly following germinal vesicle breakdown. Taking into account our immunoblot and N-terminal sequencing data along with reports from similar peroxidases, we propose that ovoperoxidases are synthesized in a pre-pro form and proteolytically processed to result in the 70 and 50 kDa forms that are found in the fertilization envelope. The sequence and structural data presented here will facilitate our continuing studies of the biogenesis of cortical granules and the fertilization envelope. Additionally, since ovoperoxidase activities have been reported in a wide range of animals, these cDNAs will be useful in uncovering similar peroxidases used in the fertilization reactions of other metazoan eggs.
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Ovoperoxidase has superoxide dismutase activity.
“Urchins also posses a heme peroxidase important during fertilization, ovoperoxidase, which has superoxide dismutase activity (Heinecke and Shapiro, 1990;LaFleur et al., 1998) and is similar to human myeloperoxidase (Nomura et al., 1999).”
From The chemical defensome: Environmental sensing and response genes in the Strongylocentrotus purpuratus genome (2006) · cites this paper as LaFleur et al., 1998
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Cites
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
LAEMMLI, U. K. (1970) · Nature · doi:10.1038/227680a0 · Cited by 249,961 · see citing works
Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
DNA sequencing with chain-terminating inhibitors
Sanger, F., Nicklen, S., & Coulson, A. R. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.12.5463 · Cited by 68,572 · see citing works
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.22.4673 · Cited by 64,617 · see citing works
Towbin, H., Staehelin, T., & Gordon, J. (1979) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.76.9.4350 · Cited by 51,421 · see citing works
A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity
Feinberg, A. P., & Vogelstein, B. (1983) · Analytical Biochemistry · doi:10.1016/0003-2697(83)90418-9 · Cited by 24,512 · see citing works
A comprehensive set of sequence analysis programs for the VAX
Devereux, J., Haeberli, P. E., & Smithies, O. (1984) · Nucleic Acids Research · doi:10.1093/nar/12.1part1.387 · Cited by 14,222 · see citing works
Antibodies, a laboratory manual
(1989) · Biomedicine & Pharmacotherapy · doi:10.1016/0753-3322(89)90130-3 · Cited by 12,318 · see citing works
Tree View: An application to display phylogenetic trees on personal computers
Page, R. (1996) · Computer applications in the biosciences · doi:10.1093/bioinformatics/12.4.357 · Cited by 10,223 · see citing works
Smith, D. B., & Johnson, K. S. (1988) · Gene · doi:10.1016/0378-1119(88)90005-4 · Cited by 5,974 · see citing works
Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites
Nielsen, H., Engelbrecht, J., Brunak, S., & von HEIJNE, G. (1997) · Protein Engineering Design and Selection · doi:10.1093/protein/10.1.1 · Cited by 5,324 · see citing works
Kozak, M. (1986) · Cell · doi:10.1016/0092-8674(86)90762-2 · Cited by 4,741 · see citing works
Foerder, C. A., & Shapiro, B. M. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.10.4214 · Cited by 316 · see citing works
Peroxidasin: a novel enzyme‐matrix protein of Drosophila development.
Nelson, R. E., Fessler, L. I., Takagi, Y., Blumberg, B., Keene, D. R., Olson, P. F., Parker, C. G., & Fessler, J. H. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06649.x · Cited by 297 · see citing works
Kimura, S., Kotani, T., McBride, O. W., Umeki, K., Hirai, K., Nakayama, T., & Ohtaki, S. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.16.5555 · Cited by 282 · see citing works
A tetrazolium method for non-specific alkaline phosphatase
McGadey, J. (1970) · Histochemistry and Cell Biology · doi:10.1007/bf00305851 · Cited by 272 · see citing works
Kinetics of Oxidation of Tyrosine and Dityrosine by Myeloperoxidase Compounds I and II
Marquez‐Curtis, L. A., & Dunford, H. B. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.51.30434 · Cited by 237 · see citing works
Covalent structure of the glycoprotein horseradish peroxidase (EC 1.11.1.7)
Welinder, K. G. (1976) · FEBS Letters · doi:10.1016/0014-5793(76)80804-6 · Cited by 226 · see citing works
Isolation and characterization of the human catalase gene
Quan, F., Korneluk, R. G., Tropak, M. B., & Gravel, R. A. (1986) · Nucleic Acids Research · doi:10.1093/nar/14.13.5321 · Cited by 211 · see citing works
Chandler, D. E., & Heuser, J. E. (1979) · The Journal of Cell Biology · doi:10.1083/jcb.83.1.91 · Cited by 196 · see citing works
TEN, R. M., Pease, L. R., McKEAN, D. J., Bell, M. P., & Gleich, G. J. (1989) · The Journal of Experimental Medicine · doi:10.1084/jem.169.5.1757 · Cited by 186 · see citing works
Ontogeny of the basal lamina in the sea urchin embryo
Wessel, G. M., Marchase, R. B., & McClay, D. R. (1984) · Developmental Biology · doi:10.1016/0012-1606(84)90025-3 · Cited by 180 · see citing works
Hall, H. G. (1978) · Cell · doi:10.1016/0092-8674(78)90003-x · Cited by 180 · see citing works
Peroxinectin, a Novel Cell Adhesion Protein from Crayfish Blood
Johansson, M. W., Lind, M., Holmblad, T., Thörnqvist, P., & Söderhäll, K. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.2731 · Cited by 176 · see citing works
Johnson, K. R., Nauseef, W. M., Carè, A., Wheelock, M. J., Shane, S., Hudson, S., Koeffler, H. P., Selsted, M. E., Miller, C. W., & Rovera, G. (1987) · Nucleic Acids Research · doi:10.1093/nar/15.5.2013 · Cited by 162 · see citing works
Structure of the Green Heme in Myeloperoxidase
Fenna, R. E., Zeng, J., & Davey, C. A. (1995) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1995.1086 · Cited by 159 · see citing works
Kimura, S., & Ikeda‐Saito, M. (1988) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340030206 · Cited by 151 · see citing works
Removal of the fertilization membrane of sea urchin embryos employing aminotriazole
Showman, R. M., & Foerder, C. A. (1979) · Experimental Cell Research · doi:10.1016/0014-4827(79)90385-9 · Cited by 148 · see citing works
Mechanism of Simultaneous Iodination and Coupling Catalyzed by Thyroid Peroxidase
Taurog, A., Dorris, M. L., & Doerge, D. R. (1996) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1996.0222 · Cited by 137 · see citing works
Oppen-Berntsen, D. O., Helvik, J. V., & Walther, B. T. (1990) · Developmental Biology · doi:10.1016/0012-1606(90)90252-e · Cited by 131 · see citing works
Ransick, A., Ernst, S. G., Britten, R. J., & Davidson, E. H. (1993) · Mechanisms of Development · doi:10.1016/0925-4773(93)90001-e · Cited by 128 · see citing works
Sea Urchin Eggs Release Protease Activity at Fertilization
Vacquier, V. D., Epel, D. D., & DOUGLAS, L. A. (1972) · Nature · doi:10.1038/237034a0 · Cited by 121 · see citing works
Structure of the horseradish peroxidase isozyme C genes
Fujiyama, K., Takemura, H., SHIBAYAMA, S., Kobayashi, K., Jong‐Kyu, C. H. O. I., Shinmyō, A., Takano, M., Yamada, Y., & Okada, H. (1988) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1988.tb14052.x · Cited by 116 · see citing works
Primary structure of bovine lactoperoxidase, a fourth member of a mammalian heme peroxidase family
Marie‐Madeleine, C. A. L. S., Mailliart, P., Brignon, G., Anglade, P., & Dumas, B. R. (1991) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1991.tb16073.x · Cited by 116 · see citing works
Deits, T. L., Farrance, M. L., Kay, E., Medill, L., Turner, E. E., Weidman, P. J., & Shapiro, B. M. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)90725-8 · Cited by 115 · see citing works
Morishita, K., Tsuchiya, M., Asano, S., Kaziro, Y., & Nagata, S. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)48159-8 · Cited by 102 · see citing works
Chandler, D. E., & Heuser, J. E. (1980) · The Journal of Cell Biology · doi:10.1083/jcb.84.3.618 · Cited by 99 · see citing works
Mullenbach, G. T., Tabrizi, A., Irvine, B. D., Bell, G. I., & Hallewell, R. A. (1987) · Nucleic Acids Research · doi:10.1093/nar/15.13.5484 · Cited by 90 · see citing works
Accumulation of histone repeat transcripts in the sea urchin egg pronucleus
Venezky, D. L., Angerer, L. M., & Angerer, R. C. (1981) · Cell · doi:10.1016/0092-8674(81)90328-7 · Cited by 85 · see citing works
Seto, P., Hirayu, H., Magnusson, R. P., Gestautas, J., Portmann, L., DeGroot, L. J., & Rapoport, B. (1987) · Journal of Clinical Investigation · doi:10.1172/jci113181 · Cited by 83 · see citing works
Schmell, E. D., & Gulyas, B. J. (1980) · Gamete Research · doi:10.1002/mrd.1120030310 · Cited by 78 · see citing works
Klebanoff, S. J., Foerder, C. A., Eddy, E. M., & Shapiro, B. M. (1979) · The Journal of Experimental Medicine · doi:10.1084/jem.149.4.938 · Cited by 78 · see citing works
Primary structure of yeast cytochrome c peroxidase
Takio, K., Titani, K., Ericsson, L. H., & Yonetani, T. (1980) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(80)90219-2 · Cited by 77 · see citing works
Greve, L. C., & Hedrick, J. L. (1978) · Gamete Research · doi:10.1002/mrd.1120010104 · Cited by 64 · see citing works
Aromatic substrate molecules bind at the distal heme pocket of myeloperoxidase.
Hori, H., Fenna, R. E., Kimura, S., & Ikeda‐Saito, M. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37206-x · Cited by 63 · see citing works
Akin, D. T., & Kinkade, J. M. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83922-4 · Cited by 61 · see citing works
Ovoperoxidase activity in ionophore treated mouse eggs. I. Electron microscopic localization
Gulyas, B. J., & Schmell, E. D. (1980) · Gamete Research · doi:10.1002/mrd.1120030309 · Cited by 61 · see citing works
Human myeloperoxidase gene: molecular cloning and expression in leukemic cells
Chang, K., Trujillo, J., Cook, R. G., & Stass, S. (1986) · Blood · doi:10.1182/blood.v68.6.1411.1411 · Cited by 60 · see citing works
Molecular cloning of the structural gene for porcine thyroid peroxidase.
Magnusson, R. P., Gestautas, J., Taurog, A., & Rapoport, B. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47875-1 · Cited by 60 · see citing works
Weidman, P. J., Kay, E., & Shapiro, B. M. (1985) · The Journal of Cell Biology · doi:10.1083/jcb.100.3.938 · Cited by 57 · see citing works
Cortical granule biogenesis is active throughout oogenesis in sea urchins
Laidlaw, M., & Wessel, G. M. (1994) · Development · doi:10.1242/dev.120.5.1325 · Cited by 56 · see citing works
Chapter 17 Embryo Dissociation, Cell Isolation, and Cell Reassociation
McClay, D. R. (1986) · Methods in cell biology · doi:10.1016/s0091-679x(08)60355-6 · Cited by 55 · see citing works
Heinecke, J. W., & Shapiro, B. M. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)42390-3 · Cited by 54 · see citing works
Lønning, S., Kjørsvik, E., & Davenport, J. (1984) · Journal of Fish Biology · doi:10.1111/j.1095-8649.1984.tb04821.x · Cited by 53 · see citing works
Chandler, D. E. (1984) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(84)80015-5 · Cited by 47 · see citing works
Somers, C. E., Battaglia, D. E., & Shapiro, B. M. (1989) · Developmental Biology · doi:10.1016/s0012-1606(89)80054-5 · Cited by 45 · see citing works
Isolation and characterization of a cDNA coding for human myeloperoxidase
Yamada, M., Hur, S.-J., Hashinaka, K., Tsuneoka, K., Saeki, T., Nishio, C., Sakiyama, F., & Tsunasawa, S. (1987) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(87)90304-3 · Cited by 43 · see citing works
Peroxidatic activity of catalase in the cortical granules of sea urchin eggs
Katsura, S., & Tominaga, A. (1974) · Developmental Biology · doi:10.1016/0012-1606(74)90131-6 · Cited by 38 · see citing works
Alliegro, M. C., & Schuel, H. (1988) · Developmental Biology · doi:10.1016/0012-1606(88)90069-3 · Cited by 38 · see citing works
Nucleotide sequence of cDNA for murine myeloperoxidase
Venturelli, D., Shirsat, N. V., Gemperlein, I., Bittenbender, S., Hudson, S., & Rovera, G. (1989) · Nucleic Acids Research · doi:10.1093/nar/17.14.5852 · Cited by 33 · see citing works
Harvey, E. N. (1910) · Journal of Experimental Zoology · doi:10.1002/jez.1400080402 · Cited by 32 · see citing works
pH-induced hysteretic transitions of ovoperoxidase.
Deits, T. L., & Shapiro, B. M. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)39535-2 · Cited by 31 · see citing works
Nomura, K., & Suzuki, N. (1995) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1995.1327 · Cited by 27 · see citing works
Nucleotide sequence of the cDNA encoding mouse thyroid peroxidase
Kotani, T., Umeki, K., Ikuo, Y., Masanori, T., Takechi, S., Nakayama, T., & Ohtaki, S. (1993) · Gene · doi:10.1016/0378-1119(93)90141-o · Cited by 26 · see citing works
Anstrom, J. A., Chin, J. E., Leaf, D. S., Parks, A. L., & Raff, R. A. (1988) · Developmental Biology · doi:10.1016/0012-1606(88)90053-x · Cited by 26 · see citing works
Palumbo, A., & Jackson, I. J. (1995) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(94)00221-2 · Cited by 25 · see citing works
Informational Content of the Echinoderm Egg
Brandhorst, B. P. (1985) · Springer eBooks · doi:10.1007/978-1-4615-6814-8_12 · Cited by 24 · see citing works
Chapter 8 Purification and Properties of the Egg Plasma Membrane
Kinsey, W. H. (1986) · Methods in cell biology · doi:10.1016/s0091-679x(08)60346-5 · Cited by 23 · see citing works
Chorionic peroxidase activity in the eggs of the fish Tribolodon hakonensis
Kudo, S., Sato, A., & Inoue, M. (1988) · Journal of Experimental Zoology · doi:10.1002/jez.1402450110 · Cited by 22 · see citing works
Conformational control of ovoperoxidase catalysis in the sea urchin fertilization membrane.
Deits, T. L., & Shapiro, B. M. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)67217-5 · Cited by 21 · see citing works
Chapter 7 Egg and Embryonic Extracellular Coats: Isolation and Purification
Weidman, P. J., & Kay, E. (1986) · Methods in cell biology · doi:10.1016/s0091-679x(08)60345-3 · Cited by 21 · see citing works
Characterization of soybean trypsin inhibitor sensitive protease from unfertilized sea urchin eggs
Alliegro, M. C., & Schuel, H. (1985) · Biochemistry · doi:10.1021/bi00336a018 · Cited by 19 · see citing works
Molecular characterization of a putative peroxidase gene of Drosophila melanogaster
Ng, S. W., Wiedemann, M. S. F., Kontermann, R. E., & Petersen, G. (1992) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/0167-4781(92)90127-l · Cited by 18 · see citing works
Insights into the Molecular Mechanisms Involved in Sea Urchin Fertilization Envelope Assembly
Somers, C. E., & Shapiro, B. M. (1989) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.1989.00001.x · Cited by 16 · see citing works
THE CATALASE OF ECHINODERM EGGS BEFORE AND AFTER FERTILIZATION
Lyon, E. P. (1909) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1909.25.4.199 · Cited by 15 · see citing works
Holt, C. A., & Childs, G. J. (1984) · Nucleic Acids Research · doi:10.1093/nar/12.16.6455 · Cited by 13 · see citing works
Cortical granule matrix disassembly during exocytosis in sea urchin eggs
Merkle, C. J., & Chandler, D. E. (1991) · Developmental Biology · doi:10.1016/0012-1606(91)90262-2 · Cited by 9 · see citing works
Mozingo, N. M., Somers, C. E., & Chandler, D. E. (1994) · Journal of Cell Science · doi:10.1242/jcs.107.10.2769 · Cited by 8 · see citing works
Flagged first, then by citations
1 of the 79 references couldn’t be matched to a known paper.
Research works printed but not linked: 4
- Browder, L.W. (Ed.), Developmental Biology. A Comprehensive Synth- esis, Vol. 1, Oogenesis. Plenum Press, New York, pp. 525-576.
- Kinsey, W.H., (1986). Purification and properties of the egg plasma mem- brane. In Schroeder, T.H. (Ed.), Echinoderm Gametes and Embryos, Vol. 27, Methods in Cell Biology. Academic Press, San Diego, pp. 139-152.
- McClay, D.R., (1986). Embryo dissociation, cell isolation, and cell reas- sociation. In: Schroeder, T.H. (Ed.), Echinoderm Gametes and Embryos, Vol. 27, Methods in Cell Biology. Academic Press, San Diego, pp. 1986.
- Weidman, P.J. and Kay, E.S., (1986). Egg and embryonic extracellular coats: isolation and purification. In: Schroeder, T.E. (Ed.), Methods in Cell Biology, Vol. 27, Echinoderm Gametes and Embryos. Academic Press, San Diego, pp. 111-138.
Cited by
Sorted by citations
Goldstone, J. V., Hamdoun, A., Cole, B. J., Howard-Ashby, M., Nebert, D. W., Scally, M., Dean, M., Epel, D., Hahn, M. E., & Stegeman, J. J. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.08.066 · Cited by 280 · see citing works
“Urchins also posses a heme peroxidase important during fertilization, ovoperoxidase, which has superoxide dismutase activity (Heinecke and Shapiro, 1990; LaFleur et al., 1998) and is similar to human myeloperoxidase (Nomura et al., 1999).”
BackgroundGoud, A. P., Goud, P. T., Diamond, M. P., Gonik, B., & Abu‐Soud, H. M. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.11.014 · Cited by 245 · see citing works
“Ovoperoxidase plays a particularly important role in this process, crosslinking the envelope into a hardened matrix that is insensitive to biochemical and mechanical challenges, thereby providing a permanent block to polyspermy [74].”
BackgroundTransitioning from egg to embryo: Triggers and mechanisms of egg activation
Horner, V. L., & Wolfner, M. F. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21454 · Cited by 197 · see citing works
The biology and dynamics of mammalian cortical granules
Liu, M. (2011) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-9-149 · Cited by 181 · see citing works
Defending the Zygote: Search for the Ancestral Animal Block to Polyspermy
Wong, J. L., & Wessel, G. M. (2005) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(05)72001-9 · Cited by 148 · see citing works
“CG‐derived ovoperoxidase is definitely required for the hardening of the sea urchin fertilization envelope, specifically at the intercast regions found between the microvillar caps identifiable within the vitelline layer scaVold (Deits et al., 1984; Foerder and Shapiro, 1977; Hall, 1978; LaFleur et al., 1998; Mozingo…”
BackgroundThe biology of cortical granules.
Wessel, G., Brooks, J., Green, E., Haley, S. A., Voronina, E., Wong, J., Zaydfudim, V., & Conner, S. D. (2001) · International Review of Cytology · doi:10.1016/s0074-7696(01)09012-x · Cited by 141 · see citing works
Autocatalytic radical reactions in physiological prosthetic heme modification
Colas, C., & Ortiz de Montellano, P. R. (2003) · Chemical Reviews · doi:10.1021/cr0204303 · Cited by 139 · see citing works
Sun, Q. (2003) · Microscopy Research and Technique · doi:10.1002/jemt.10347 · Cited by 129 · see citing works
The Oxidative Burst at Fertilization Is Dependent upon Activation of the Dual Oxidase Udx1
Wong, J. L., Créton, R., & Wessel, G. M. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.10.014 · Cited by 128 · see citing works
“All urchin, this protein is expressed exclusively during oo- samples were isolated in isotonic, calcium-free buffer (0.5 M NaCl, genesis (LaFleur et al., 1998) and requires H2O2 synthesis 0.01 M KCl, 1.5 mM NaHCO3, 60 mM NaOH, 20 mM EGTA [pH 8.0]) in the presence of Complete Mini EDTA-free Protease…”
MethodInfluentialThe Regulation of Oocyte Maturation
Voronina, E., & Wessel, G. M. (2003) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(03)58003-6 · Cited by 127 · see citing works
Segal, A. W. (2007) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2007.10.003 · Cited by 122 · see citing works
Péterfi, Z., Donkó, Á., Orient, A., Sum, A., Prókai, Á., Molnár, B., Veréb, Z., Rajnavölgyi, É., Kovács, K., Müller, V., et al. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2009.080693 · Cited by 114 · see citing works
“ECM stabilization by dityrosine bridges is well-documented during sea urchin fertilization, where secreted ovoperoxidase is responsible for the formation of cross-links.(6) Dityrosine formation is also involved in the stabilization of C.”
BackgroundOgasawara, M. (2000) · Development Genes and Evolution · doi:10.1007/s004270050309 · Cited by 107 · see citing works
“On the other hand, BbTPO shows less identity than non-thyroid-type peroxidase: its identity with human salivary peroxidase is 38.3% (Kiser et al. 1996), with human eosinophil peroxidase 38.8% (Ten et al. 1989), with human myeloperoxidase 40.7% (Hashinaka et al. 1988), and with sea urchin ovoperoxidase 32.9% ( LaFleur…”
BackgroundInfluentialMolecular Evolution of the Myeloperoxidase Family
Daiyasu, H., & Toh, H. (2000) · Journal of Molecular Evolution · doi:10.1007/s002390010106 · Cited by 97 · see citing works
“Subfamily 6 includes two ovoperoxidases, derived from urchin oocytes, involved in the block to polyspermy ( LaFleur et al. 1998 ) and in protecting the embryo from oxidants driven from superoxide anion (Heinecke and Shapiro 1990).”
BackgroundResultInfluentialHennebert, E., Leroy, B., Wattiez, R., & Ladurner, P. (2015) · Journal of Proteomics · doi:10.1016/j.jprot.2015.07.002 · Cited by 81 · see citing works
“Ovoperoxidase is related to other hemedependant peroxidases which favor tyrosine as a substrate [39].”
BackgroundHow to make an egg: transcriptional regulation in oocytes
Song, J. L., & Wessel, G. M. (2005) · Differentiation · doi:10.1111/j.1432-0436.2005.07301005.x · Cited by 80 · see citing works
“These structural proteins modify the extracellular environment of the oocyte to prevent polyspermy and are constructed promptly after fertilization (LaFleur et al., 1998; Wessel et al., 2000a).”
BackgroundLeMosy, E. K., & Hashimoto, C. (2000) · Developmental Biology · doi:10.1006/dbio.1999.9562 · Cited by 71 · see citing works
Yamano, K., Qiu, G., & Unuma, T. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.025379 · Cited by 70 · see citing works
“In the mouse and the sea urchin, proteins released from cortical granules block polyspermy by modulating the sperm receptor, the egg surface, or the fertilization membrane [20, 21], although the presence of TSP 3, 4/COMP in cortical granules has not been reported in these animals.”
BackgroundProteomic identification of quality factors for oocytes in the Pacific oyster Crassostrea gigas
Corporeau, C., Vanderplancke, G., Boulais, M., Suquet, M., Quéré, C., Boudry, P., Huvet, A., & Madec, S. (2012) · Journal of Proteomics · doi:10.1016/j.jprot.2012.07.040 · Cited by 68 · see citing works
“Some protease activities during oogenesis [47] might thus ensure specific Vg breakdown related to the status of oocytes and with consequences for fertilisation and the developmental success [33].”
BackgroundActinobacterial Peroxidases: an Unexplored Resource for Biocatalysis
Roes‐Hill, M. L., Khan, N., & Burton, S. G. (2011) · Applied Biochemistry and Biotechnology · doi:10.1007/s12010-011-9167-5 · Cited by 67 · see citing works
Oogenesis: Single cell development and differentiation
Song, J. L., Wong, J. L., & Wessel, G. M. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.07.041 · Cited by 64 · see citing works
“…X, EM) egg (blot, X, EM) embryo (blot, X) (Wessel et al., 2000) Oocyte (blot, X) egg (enz, blot, X, WM) FE (enz, blot, X, WM) (Deits et al., 1984) (LaFleur et al., 1998) Cortical granule serine protease (CGSP1) CG enzyme SPU_19872 SPU_04123 Ovary (RT′) Egg (enz, blot, X, WM) (Haley and…”
BackgroundCyclin B synthesis is required for sea urchin oocyte maturation
Voronina, E., Marzluff, W. F., & Wessel, G. M. (2003) · Developmental Biology · doi:10.1016/s0012-1606(02)00134-3 · Cited by 47 · see citing works
Mammalian peroxidasin (PXDN): From physiology to pathology
Cheng, G., & Shi, R. (2022) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2022.02.026 · Cited by 44 · see citing works
Lebesgue, N., da Costa, G., Mesquita-Ribeiro, R., Ribeiro-Silva, C., Martins, G. G., Matranga, V., Scholten, A., CORDEIRO, C. A., Heck, A. J. R., & Santos, R. (2016) · Journal of Proteomics · doi:10.1016/j.jprot.2016.02.026 · Cited by 44 · see citing works
“Like Ovoperoxidase , Dual oxidase 1 and 2 are heme-dependant peroxidases, which favor tyrosine as a substrate [51].”
Haley, S. A., & Wessel, G. M. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9299 · Cited by 42 · see citing works
“One form of ovoperoxidase is cleaved after an arginine residue before incorporation into the FE (LaFleur et al., 1998), though the effect of this proteolysis on peroxidase activity is not known.”
BackgroundCell surface changes in the egg at fertilization
Wessel, G. M., & Wong, J. L. (2009) · Molecular Reproduction and Development · doi:10.1002/mrd.21090 · Cited by 35 · see citing works
“A serine protease, CGSP1 (see Table 1), and ovoperoxidase are stored as inactive enzymes in the CG (Deits and Shapiro, 1985; Somers et al., 1989; LaFleur et al., 1998; Haley and Wessel, 1999), thereby blocking precocious activity on other content proteins.”
Wong, J. L., & Wessel, G. M. (2007) · Development · doi:10.1242/dev.015503 · Cited by 32 · see citing works
Reactive oxygen species and Udx1 during early sea urchin development
Wong, J. L., & Wessel, G. M. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.07.004 · Cited by 30 · see citing works
Regulated Proteolysis by Cortical Granule Serine Protease 1 at Fertilization
Haley, S. A., & Wessel, G. M. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-11-0843 · Cited by 30 · see citing works
“, 2000), SFE9 (Wessel, 1995), and MGB (Conner, unpublished data), each at 1:125 dilution; ovoperoxidase (LaFleur et al., 1998) at 1:50 dilution; and glucanase at 1:500 dilution.”
InfluentialMajor components of a sea urchin block to polyspermy are structurally and functionally conserved
Wong, J. L., & Wessel, G. M. (2004) · Evolution & Development · doi:10.1111/j.1525-142x.2004.04019.x · Cited by 30 · see citing works
“1994; Tatemoto and Terada 1999), (b) detectable peroxidase (Hall 1978; Gulyas and Schmell 1980a,b; Deits et al. 1984; Kudo 1988; Nomura and Suzuki 1995; Li et al. 1996; LaFleur et al. 1998; Nomura et al. 1999) and proteinase activity (Carroll and Epel 1975b; Gulyas and Schmell 1980a; Moller and Wassarman 1989; Haley a…”
BackgroundInfluentialThe Relationship of NADPH Oxidases and Heme Peroxidases: Fallin' in and Out
Sirokmány, G., & Geiszt, M. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00394 · Cited by 29 · see citing works
The function of the NADPH oxidase of phagocytes, and its relationship to other NOXs
Béhé, P., & Segal, A. W. (2007) · Biochemical Society Transactions · doi:10.1042/bst0351100 · Cited by 28 · see citing works
Diversity in the fertilization envelopes of echinoderms
Oulhen, N., Reich, A. M., Wong, J. L., Ramos, I., & Wessel, G. M. (2013) · Evolution & Development · doi:10.1111/ede.12012 · Cited by 27 · see citing works
“In the sea urchin S. purpuratus, the ovoperoxidase mRNA is present exclusively in oocytes and is turned over rapidly following germinal vesicle breakdown (LaFleur et al. 1998).”
BackgroundInfluentialMutations Affecting the Calcium-Binding Site of Myeloperoxidase and Lactoperoxidase
Shin, K., Hayasawa, H., & Lönnerdal, B. L. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.4448 · Cited by 27 · see citing works
Wessel, G. M., Conner, S. D., Laidlaw, M., Harrison, J. C., & LaFleur, G. (2000) · Biology of Reproduction · doi:10.1095/biolreprod63.6.1706 · Cited by 27 · see citing works
“This pattern is identical to the 4-kb ovoperoxidase transcript, encoding a known cortical granule content protein [29].”
BackgroundResultRegulatory contribution of heterotrimeric G-proteins to oocyte maturation in the sea urchin
Voronina, E., & Wessel, G. M. (2004) · Mechanisms of Development · doi:10.1016/j.mod.2004.01.005 · Cited by 22 · see citing works
“Northern blot analysis for Ga subunit mRNA expression during development was performed as described (LaFleur et al., 1998) using 10 mg of total RNA from S. purpuratus ovaries, eggs, and embryos at several developmental stages.”
Renovation of the egg extracellular matrix at fertilization
Wong, J. L., & Wessel, G. M. (2008) · The International Journal of Developmental Biology · doi:10.1387/ijdb.072557jw · Cited by 21 · see citing works
“This myeloperoxidaselike family of enzymes is specifically transcribed in oocytes, and packaged into cortical granules (LaFleur et al., 1998; Nomura and Suzuki, 1995).”
BackgroundNomura, K., Hoshino, K., & Suzuki, N. (1999) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1219 · Cited by 19 · see citing works
CO2-induced fertilization impairment in Strongylocentrotus droebachiensis collected in the Arctic
Bögner, D., Bickmeyer, U., & Köhler, A. (2014) · Helgoland Marine Research · doi:10.1007/s10152-014-0394-3 · Cited by 16 · see citing works
“Impairment in the FE formation may be involved in polyspermy events as documented in the literature (Vacquier et al. 1973; LaFleur et al. 1998; Haley and Wessel 2004b; Levitan et al. 2007; Runnström and Manelli 1964; Longo 1978; Longo and Schuel 1973; Hiramoto 1962).”
Wong, J. L., & Wessel, G. M. (2009) · Development · doi:10.1242/dev.030775 · Cited by 16 · see citing works
“CGSP1 also regulates the activity of another cortical granule enzyme, ovoperoxidase (Haley and Wessel, 2004), which is responsible for establishing dityrosine crosslinks between adjacent proteins (Foerder and Shapiro, 1977; Kay and Shapiro, 1987; LaFleur et al., 1998; Wong and Wessel, 2008).”
BackgroundImmune Defense of Marine Invertebrates: The Role of Reactive Oxygen and Nitrogen Species
Philipp, E. E. R., Lipinski, S., Rast, J. P., & Rosenstiel, P. C. (2011) · doi:10.1002/9781444345988.ch17 · Cited by 13 · see citing works
Mashanov, V. S., Machado, D. J., Reid, R. W., Brouwer, C., Kofsky, J., & Janies, D. A. (2022) · BMC Genomics · doi:10.1186/s12864-022-08750-y · Cited by 12 · see citing works
2 Genes and Their Products in Sea Urchin Development
Ciudice, G. (1999) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)60314-2 · Cited by 8 · see citing works
Fertilization in Invertebrates
Schatten, H., & Chakrabarti, A. (2000) · Springer eBooks · doi:10.1007/978-3-642-58301-8_2 · Cited by 7 · see citing works
Analysis of Sea Urchin Embryo Gene Expression by Immunocytochemistry
Venuti, J. M., Pepicelli, C. V., & Flowers, V. L. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)74015-7 · Cited by 6 · see citing works
Detection of hydrogen peroxide by lactoperoxidase-mediated dityrosine formation
Donkó, Á., Orient, A., Szabó, P. T., Németh, G., Vántus, T., Kéri, G., Őrfi, L., Hunyady, L., Buday, L., & Geiszt, M. (2009) · Free Radical Research · doi:10.1080/10715760902859069 · Cited by 5 · see citing works
“The ability to form dityrosine seems to be a general feature of peroxidases; enzymes of lower species and mammalian peroxidases were previously described to catalyse this reaction [4,6,8,9].”
BackgroundThe many faces of egg activation at fertilization
Leguia, M., & Wessel, G. (2007) · Signal Transduction · doi:10.1002/sita.200600122 · Cited by 5 · see citing works
“matrix and the cortical granules to one another, further stabilizing thematrix [7, 37].”
BackgroundMashanov, V. S., Machado, D. J., Reid, R. W., Brouwer, C., Kofsky, J., & Janies, D. A. (2022) · Research Square · doi:10.21203/rs.3.rs-1148623/v1 · Cited by 5 · see citing works
Pieplow, C. A., Silvia, M., Gourlay, A. N., Rhyne, A. L., Oulhen, N., & Wessel, G. M. (2025) · Developmental Biology · doi:10.1016/j.ydbio.2025.09.013 · Cited by 3 · see citing works
Bögner, D., Bickmeyer, U., & Köhler, A. (2013) · doi:10.5194/bgd-10-8027-2013 · Cited by 3 · see citing works
Zazueta‐Novoa, V., Martínez‐Cadena, G., Wessel, G. M., Zazueta‐Sandoval, R., Castellano, L. E., & Garcı́a-Soto, J. (2011) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2011.01261.x · Cited by 2 · see citing works
Huang, X., Huan, P., & Liu, B. (2016) · PROTEOMICS · doi:10.1002/pmic.201600251 · Cited by 2 · see citing works
“Third, it has been shown that a sea urchin peroxidase hardens the oocyte envelope after sperm cell entry [43,44], thereby blocking polyspermy, which can cause chaos during cleavage and embryo death [45, 46].”
Background
- Authors
- LaFleur, G. J., Horiuchi, Y., & Wessel, G. M.
- Affiliations
- Brown University (US)
- Corresponding author
- LaFleur, Gary J
- ORCID
- Wessel, Gary M
- Venue
- Mechanisms of Development
- Publisher
- Elsevier BV
- Published
- 1998-01
- Volume
- 70
- Issue
- 1-2
- Pages
- 77-89
- ISSN
- 0925-4773 (ISSN-L)
- OpenAlex
- W2095422854
- Cited by
- 53
- References
- 79
- Citations by year
- 2025: 1 · 2022: 3 · 2019: 1 · 2016: 2 · 2015: 1 · 2014: 1 · 2013: 2 · 2012: 1
- FWCI
- 1.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Mechanisms of Development (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- sea urchins, Strongylocentrotus purpuratus, Lytechinus variegatus, cortical reaction, fertilization envelope, polyspermy block, cortical granules, post-translational processing, germinal vesicle breakdown, mRNA turnover, fertilisation (biology)
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Cloning, Molecular, Female, Fertilization, Heme, Male, Molecular Sequence Data, Oocytes, Peroxidases, Protein Processing, Post-Translational, Sea Urchins, Substrate Specificity, Tyrosine, Sequence Homology, Amino Acid, DNA Primers, DNA, Complementary
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