Glycobiology is the study of complex carbohydrates in biological systems and represents a developing field of science that has made huge advances in the last half century. In fact, it combines all branches of biomedical research, revealing the vast and diverse forms of carbohydrate structures that exist in nature. Advances in structure determination have enabled scientists to study the function of complex carbohydrates in more depth and to determine the role that they play in a wide range of biological processes. Glycobiology research in marine systems has primarily focused on reproduction, in particular for what concern the chemical communication between the gametes. The current status of marine glycobiology is primarily descriptive, devoted to characterizing marine glycoconjugates with potential biomedical and biotechnological applications. In this review, we describe the current status of the glycobiology in the reproductive processes from gametogenesis to fertilization and embryo development of marine animals.
References
[1]
Caldwell, G.S.; Pagett, H.E. Marine glycobiology: Current status and future perspectives. Mar. Biotechnol. 2010, 12, 241–252, doi:10.1007/s10126-010-9263-5.
[2]
Shriver, Z.; Raguram, S.; Sasisekharan, R. Glycomics: A pathway to a class of new and improved therapeutics. Nat. Rev. Drug Discov. 2004, 3, 863–873.
[3]
Shur, B.D. Glycobiology: The beginning of a sweet tale. Curr. Biol. 1994, 4, 996–999, doi:10.1016/S0960-9822(00)00224-4.
[4]
O’Donnell, N. Intracellular glycosylation and development. Biochim. Biophys. Acta 2002, 1573, 336–345, doi:10.1016/S0304-4165(02)00401-4.
[5]
Morris, H.R.; Dell, A.; Easton, R.L.; Panico, M.; Koistinen, H.; Koistinen, R.; Oehninger, S.; Patankar, M.S.; Seppala, M.; Clark, G.F. Gender-specific glycosylation of human glycodelin affects its contraceptive activity. J. Biol. Chem. 1996, 271, 32159–32167.
[6]
Dell, A.; Morris, H.R.; Easton, R.L.; Patankar, M.; Clark, G.F. The glycobiology of gametes and fertilization. Biochim. Biophys. Acta 1999, 1473, 196–205, doi:10.1016/S0304-4165(99)00179-8.
[7]
Sarasquete, C.; Cardenas, S.; de Gonzalez, C.M.; Pascual, E. Oogenesis in the bluefin tuna, Thunnus thynnus L.: A histological and histochemical study. Histol. Histopathol. 2002, 17, 775–788.
[8]
Ortiz-Delgado, J.B.; Porcelloni, S.; Fossi, C.; Sarasquete, C. Histochemical characterisation of oocytes of the swordfish Xiphias gladius. Sci. Mar. 2008, 72, 549–564.
[9]
Patino, R.; Sullivan, C.V. Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish. Physiol. Biochem. 2002, 26, 57–70, doi:10.1023/A:1023311613987.
[10]
Inoue, S.; Iwasaki, M. Isolation of a novel glycoprotein from the eggs of rainbowtrout: Occurrence of disialosyl groups on all carbohydrate chains. Biochem. Biophys. Res. Commun. 1978, 83, 1018–1023, doi:10.1016/0006-291X(78)91497-3.
[11]
Kitajima, K.; Sorimachi, H.; Inoue, S.; Inoue, Y. Comparative structures of the apopolysialoglycoproteins from unfertilized and fertilized eggs of salmonid fishes. Biochemistry 1988, 27, 7141–7145, doi:10.1021/bi00418a071.
[12]
Song, Y.; Kitajima, K.; Inoue, Y. New tandem-repeating peptide structures in polysialoglycoproteins from the unfertilized eggs of kokanee salmon. Arch. Biochem. Biophys. 1990, 283, 167–172, doi:10.1016/0003-9861(90)90627-B.
[13]
Seko, A.; Kitajima, K.; Iwasaki, M.; Inoue, S.; Inoue, Y. Structural studies of fertilization-associated carbohydrate-rich glycoproteins (hyosophorin) isolated from the fertilized and unfertilized eggs of flounder, Paralichthys olivaceus. Presence of a novel penta-antennary N-linked glycan chain in the tandem repeating glycopeptide unit of hyosophorin. J. Biol. Chem. 1989, 264, 15922–15929.
[14]
Iwasaki, M.; Inoue, S. Structures of the carbohydrate units of polysialoglycoproteins isolated from the eggs of four species of salmonid fishes. Glycoconj. J. 1985, 2, 209–228, doi:10.1007/BF01049269.
[15]
Kitajima, K.; Inoue, Y.; Inoue, S. Polysialoglycoproteins of Salmonidae fish eggs. Complete structure of 200-kDa polysialoglycoprotein from the unfertilized eggs of rainbow trout (Salmo gairdneri). J. Biol. Chem. 1986, 261, 5262–5269.
[16]
Nadano, D.; Iwasaki, M.; Endo, S.; Kitajima, K.; Inoue, S.; Inoue, Y. A naturally occurring deaminated neuraminic acid, 3-deoxy-D-glycero-D-galacto-nonulosonic acid (KDN). ts unique occurrence at the nonreducing ends of oligosialyl chains in polysialoglycoprotein of rainbow trout eggs. J. Biol. Chem. 1986, 261, 11550–11557.
[17]
Asahina, S.; Sato, C.; Matsuno, M.; Matsuda, T.; Colley, K.; Kitajima, K. Involvement of the alpha2,8-polysialyltransferases II/STX and IV/PST in the biosynthesis of polysialic acid chains on the O-linked glycoproteins in rainbow trout ovary. J. Biochem. 2006, 140, 687–701, doi:10.1093/jb/mvj200.
[18]
Inoue, S.; Kanamori, A.; Kitajima, K.; Inoue, Y. KDN-glycoprotein: A novel deaminated neuraminic acid-rich glycoprotein isolated from vitelline envelope of rainbow trout eggs. Biochem. Biophys. Res. Commun. 1988, 153, 172–176, doi:10.1016/S0006-291X(88)81204-X.
[19]
Accogli, G.; Zizza, S.; Garcia-Lopez, A.; Sarasquete, C.; Desantis, S. Lectin-binding pattern of the Senegalese sole Solea senegalensis oogenesis. Microsc. Res. Tech. 2012, 75, 1124–1135, doi:10.1002/jemt.22040.
[20]
Mandich, A.; Massari, A.; Bottero, S.; Marino, G. Histological and histochemical study of female germ cell development in the dusky grouper Epinephelus marginatus (Lowe, 1834). Eur. J. Histochem. 2002, 46, 87–100.
Schuel, H. Secretory Functions of Egg Cortical Granules. In Biology of Fertilization; Metz, C.B., Monroy, A., Eds.; Academic Press: San Diego, CA, USA, 1985; Volume 3, pp. 1–44.
[23]
Zamboni, L. Ultrastructure of mammalian oocytes and ova. Biol. Reprod. 1970, 2, 44–63, doi:10.1095/biolreprod2.Supplement_2.44.
[24]
Wolf, D.P. On the contents of the cortical granules from Xenopus laevis eggs. Dev. Biol. 1974, 38, 14–29, doi:10.1016/0012-1606(74)90255-3.
[25]
Gilkey, J.C. Mechanisms of fertilization in fishes. Am. Zool. 1981, 21, 359–375.
[26]
Deits, T.; Farrance, M.; Kay, E.S.; Medill, L.; Turner, E.E.; Weidman, P.J.; Shapiro, B.M. Purification and properties of ovoperoxidase, the enzyme responsible for hardening the fertilization membrane of the sea urchin egg. J. Biol. Chem. 1984, 259, 13525–13533.
[27]
Wessel, G.M.; Brooks, J.M.; Green, E.; Haley, S.; Voronina, E.; Wong, J.; Zaydfudim, V.; Conner, S. The biology of cortical granules. Int. Rev. Cytol. 2001, 209, 117–206, doi:10.1016/S0074-7696(01)09012-X.
[28]
Anderson, S.L.; Chang, E.S.; Clark, W.H.J. Timing of postvitellogenic ovarian changes in the ridgeback prawn Sicyonia ingentis (Penaeidae) determined by ovarian biopsy. Aquaculture 1984, 42, 257–271, doi:10.1016/0044-8486(84)90106-6.
[29]
Lynn, J.W.; Clark, W.H.J. Physiological and biochemical investigations of the egg jelly release in Penaeus aztecus. Biol. Bull. 1987, 173, 451–460, doi:10.2307/1541692.
[30]
Pongtippatee-Taweepreda, P.; Chavadej, J.; Plodpai, P.; Pratoomchart, B.; Sobhon, P.; Weerachatyanukul, W.; Withyachumnarnkul, B. Egg activation in the black tiger shrimp Penaeus monodon. Aquaculture 2004, 234, 183–198, doi:10.1016/j.aquaculture.2003.10.036.
[31]
Rankin, S.M.; Davis, R.W. Ultrastructure of oocytes of the shrimp, Penaeus vannamei: Cortical specialization formation. Tissue Cell 1990, 22, 879–893, doi:10.1016/0040-8166(90)90050-J.
[32]
Kruevaisayawan, H.; Vanichviriyakit, R.; Withyachumnarnkul, B.; Chavadej, J.; Sobhon, P. Oogenesis and formation of cortical rods in the black tiger shrimp, Penaeus monodon. Aquaculture 2010, 301, 91–98, doi:10.1016/j.aquaculture.2010.01.018.
Khayat, M.; Babin, P.J.; Funkenstein, B.; Sammar, M.; Nagasawa, H.; Tietz, A.; Lubzens, E. Molecular characterization and high expression during oocyte development of a shrimp ovarian cortical rod protein homologous to insect intestinal peritrophins. Biol. Reprod. 2001, 64, 1090–1099, doi:10.1095/biolreprod64.4.1090.
[36]
Avarre, J.C.; Khayat, M.; Michelis, R.; Nagasawa, H.; Tietz, A.; Lubzens, E. Inhibition of de novo synthesis of a jelly layer precursor protein by crustacean hyperglycemic hormone family peptides and posttranscriptional regulation by sinus gland extracts in Penaeus semisulcatus ovaries. Gen. Comp. Endocrinol. 2001, 124, 257–268, doi:10.1006/gcen.2001.7710.
[37]
Kim, Y.K.; Kawazoe, I.; Tsutsui, N.; Jasmani, S.; Wilder, M.N.; Aida, K. Isolation and cDNA cloning of ovarian cortical rod protein in kuruma prawn Marsupenaeus japonicus (Crustacea: Decapoda: Penaeidae). Zool. Sci. 2004, 21, 1109–1119, doi:10.2108/zsj.21.1109.
[38]
Kim, Y.K.; Tsutsui, N.; Kawazoe, I.; Okumura, T.; Kaneko, T.; Aida, K. Localization and developmental expression of mRNA for cortical rod protein in kuruma prawn Marsupenaeus japonicus. Zool. Sci. 2005, 22, 675–680, doi:10.2108/zsj.22.675.
[39]
Kruevaisayawan, H.; Vanichviriyakit, R.; Weerachatyanukul, W.; Withyachumnarnkul, W.; Sobhon, P. Biochemical characterization and physiological role of cortical rods in black tiger shrimp, Penaeus monodon. Aquaculture 2007, 270, 289–298.
[40]
Matozzo, V.; Gagne, F.; Marin, M.G.; Ricciardi, F.; Blaise, C. Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: A review. Environ. Int. 2008, 34, 531–545, doi:10.1016/j.envint.2007.09.008.
[41]
Fabra, M.; Raldua, D.; Bozzo, M.G.; Deen, P.M.; Lubzens, E.; Cerda, J. Yolk proteolysis and aquaporin-1o play essential roles to regulate fish oocyte hydration during meiosis resumption. Dev. Biol. 2006, 295, 250–262, doi:10.1016/j.ydbio.2006.03.034.
[42]
Matsubara, T.; Ohkubo, N.; Andoh, T.; Sullivan, C.V.; Hara, A. Two forms of vitellogenin, yielding two distinct lipovitellins, play different roles during oocyte maturation and early development of barfin flounder, Verasper moseri, a marine teleost that spawns pelagic eggs. Dev. Biol. 1999, 213, 18–32, doi:10.1006/dbio.1999.9365.
[43]
Arukwe, A.; Goksoyr, A. Eggshell and egg yolk proteins in fish: Hepatic proteins for the next generation: Oogenetic, population, and evolutionary implications of endocrine disruption. Comp. Hepatol. 2003, 2, 4, doi:10.1186/1476-5926-2-4.
[44]
Abdu, U.; Davis, C.; Khalaila, I.; Sagi, A. The vitellogenin cDNA of Cherax quadricarinatus encodes a lipoprotein with calcium binding ability, and its expression is induced following the removal of the androgenic gland in a sexually plastic system. Gen. Comp. Endocrinol. 2002, 127, 263–272, doi:10.1016/S0016-6480(02)00053-9.
[45]
Khalaila, I.; Peter-Katalinic, J.; Tsang, C.; Radcliffe, C.M.; Aflalo, E.D.; Harvey, D.J.; Dwek, R.A.; Rudd, P.M.; Sagi, A. Structural characterization of the N-glycan moiety and site of glycosylation in vitellogenin from the decapod crustacean Cherax quadricarinatus. Glycobiology 2004, 14, 767–774, doi:10.1093/glycob/cwh105.
[46]
Jaenicke, R. Protein stability and protein folding. Ciba Found. Symp. 1991, 161, 206–221.
[47]
Raikhel, A.S.; Dhadialla, T.S. Accumulation of yolk proteins in insect oocytes. Annu. Rev. Entomol. 1992, 37, 217–251, doi:10.1146/annurev.en.37.010192.001245.
[48]
Warrier, S.; Subramoniam, T. Receptor mediated yolk protein uptake in the crab Scylla serrata: Crustacean vitellogenin receptor recognizes related mammalian serum lipoproteins. Mol. Reprod. Dev. 2002, 61, 536–548, doi:10.1002/mrd.10106.
[49]
Shyu, A.B.; Raff, R.A.; Blumenthal, T. Expression of the vitellogenin gene in female and male sea urchin. Proc. Natl. Acad. Sci. USA 1986, 83, 3865–3869, doi:10.1073/pnas.83.11.3865.
[50]
Ozaki, H.; Moriya, O.; Harrington, F.E. A glycoprotein in the accessory cell of the echinoid ovary and its role in vitellogenesis. Dev. Genes Evol. 1986, 195, 74–79.
[51]
Unuma, T.; Suzuki, T.; Kurokawa, T.; Yamamoto, T.; Akiyama, T. A protein identical to the yolk protein is stored in the testis in male red sea urchin, Pseudocentrotus depressus. Biol. Bull. 1998, 194, 92–97, doi:10.2307/1542517.
[52]
Harrington, F.E.; Ozaki, H. The major yolk glycoprotein precursor in echinoids is secreted by coelomocytes into the coelomic plasma. Cell Differ. 1986, 19, 51–57, doi:10.1016/0045-6039(86)90025-4.
[53]
Degroote, S.; Wolthoorn, J.; van Meer, G. The cell biology of glycosphingolipids. Semin. Cell Dev. Biol. 2004, 15, 375–387.
[54]
Fishman, P.H. Recent advances in identifying the functions of gangliosides. Chem. Phys. Lipids 1986, 42, 137–151, doi:10.1016/0009-3084(86)90049-6.
[55]
Hakomori, S. Glycosphingolipids in cellular interaction, differentiation, and oncogenesis. Annu. Rev. Biochem. 1981, 50, 733–764, doi:10.1146/annurev.bi.50.070181.003505.
[56]
Hakomori, S. Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions. J. Biol. Chem. 1990, 265, 18713–18716.
[57]
Hakomori, S. Structure and function of sphingoglycolipids in transmembrane signalling and cell-cell interactions. Biochem. Soc. Trans. 1993, 21, 583–595.
[58]
Hakomori, S.I. Cell adhesion/recognition and signal transduction through glycosphingolipid microdomain. Glycoconj. J. 2000, 17, 143–151, doi:10.1023/A:1026524820177.
[59]
Kojima, H.; Tohsato, Y.; Kabayama, K.; Itonori, S.; Ito, M. Biochemical studies on sphingolipids of Artemia franciscana: Complex neutral glycosphingolipids. Glycoconj. J. 2012, doi:10.1007/s10719-012-9436-8.
[60]
Yamamoto, T.; Teshima, T.; Saitoh, U.; Hoshi, M.; Shiba, T. Synthesis of ganglioside M5 from sea urchin egg. Tetrahedron Lett. 1994, 35, 2701–2704, doi:10.1016/S0040-4039(00)77010-9.
[61]
Kubo, H.; Irie, A.; Inagaki, F.; Hoshi, M. Gangliosides from the eggs of the sea urchin, Anthocidaris crassispina. J. Biochem. 1990, 108, 185–192.
[62]
Nezuo, M.; Shogomori, H.; Hoshi, M.; Yamamoto, T.; Teshima, T.; Shiba, T.; Chiba, K. Developmental changes in localization of the main ganglioside during sea urchin embryogenesis. Glycobiology 2000, 10, 1243–1247, doi:10.1093/glycob/10.11.1243.
[63]
Shogomori, H.; Chiba, K.; Kubo, H.; Hoshi, M. Non-plasmalemmal localisation of the major ganglioside in sea urchin eggs. Zygote 1993, 1, 215–223.
[64]
Shogomori, H.; Chiba, K.; Hoshi, M. Association of the major ganglioside in sea urchin eggs with yolk lipoproteins. Glycobiology 1997, 7, 391–398, doi:10.1093/glycob/7.3.391.
[65]
Kubo, H.; Hoshi, M. Immunocytochemical study of the distribution of a ganglioside in sea urchin eggs. J. Biochem. 1990, 108, 193–199.
[66]
Kubo, H.; Jiang, G.J.; Irie, A.; Morita, M.; Matsubara, T.; Hoshi, M. A novel ceramide trihexoside from the eggs of the sea urchin, Hemicentrotus pulcherrimus. J. Biochem. 1992, 111, 726–731.
[67]
Kubo, H.; Jiang, G.J.; Irie, A.; Suzuki, M.; Inagaki, F.; Hoshi, M. A novel difucosylated neutral glycosphingolipid from the eggs of the sea urchin, Hemicentrotus pulcherrimus: I. Purification and structural determination of the glycolipid. J. Biochem. 1992, 112, 281–285.
[68]
Kubo, H.; Irie, A.; Inagaki, F.; Hoshi, M. Melibiosylceramide as the sole ceramide dihexoside from the eggs of the sea urchin, Anthocidaris crassispina. J. Biochem. 1988, 104, 755–760.
[69]
Inagaki, F.; Tate, S.; Kubo, H.; Hoshi, M. A novel difucosylated neutral glycosphingolipid from the eggs of the sea urchin, Hemicentrotus pulcherrimus: II. Structural determination by two-dimensional NMR. J. Biochem. 1992, 112, 286–289.
Glabe, C.G.; Grabel, L.B.; Vacquier, V.D.; Rosen, S.D. Carbohydrate specificity of sea urchin sperm bindin: A cell surface lectin mediating sperm-egg adhesion. J. Cell Biol. 1982, 94, 123–128, doi:10.1083/jcb.94.1.123.
[72]
Focarelli, R.; Rosa, D.; Rosati, F. Differentiation of the vitelline coat and the polarized site of sperm entrance in the egg of Unio elongatulus (Mollusca, Bivalvia). J. Exp. Zool. 1990, 254, 88–96, doi:10.1002/jez.1402540113.
[73]
Wikramanayake, A.H.; Clark, W.H. Two extracellular matrices from oocytes of the marine shrimp Sicyonia ingentis that independently mediate only primary or secondary sperm binding. Dev. Growth Differ. 1994, 36, 89–101.
[74]
Honegger, T.G.; Koyanagi, R. The ascidian egg envelope in fertilization: Structural and molecular features. Int. J. Dev. Biol. 2008, 52, 527–533, doi:10.1387/ijdb.072547th.
[75]
Murata, K.; Sugiyama, H.; Yasumasu, S.; Iuchi, I.; Yasumasu, I.; Yamagami, K. Cloning of cDNA and estrogen-induced hepatic gene expression for choriogenin H, a precursor protein of the fish egg envelope (chorion). Proc. Natl. Acad. Sci. USA 1997, 94, 2050–2055.
Mold, D.E.; Kim, I.F.; Tsai, C.M.; Lee, D.; Chang, C.Y.; Huang, R.C. Cluster of genes encoding the major egg envelope protein of zebrafish. Mol. Reprod. Dev. 2001, 58, 4–14, doi:10.1002/1098-2795(200101)58:1<4::AID-MRD2>3.0.CO;2-P.
[78]
Kanamori, A. Systematic identification of genes expressed during early oogenesis in medaka. Mol. Reprod. Dev. 2000, 55, 31–36, doi:10.1002/(SICI)1098-2795(200001)55:1<31::AID-MRD5>3.0.CO;2-7.
[79]
Hyllner, S.J.; Westerlund, L.; Olsson, P.E.; Schopen, A. Cloning of rainbow trout egg envelope proteins: Members of a unique group of structural proteins. Biol. Reprod. 2001, 64, 805–811, doi:10.1095/biolreprod64.3.805.
[80]
Lee, C.; Jeon, S.H.; Na, J.G.; Park, K. Sequence analysis of choriogenin H gene of medaka (Oryzias latipes) and mRNA expression. Environ. Toxicol. Chem. 2002, 21, 1709–1714.
[81]
Miller, D.J.; Ax, R.L. Carbohydrates and fertilization in animals. Mol. Reprod. Dev. 1990, 26, 184–198, doi:10.1002/mrd.1080260213.
[82]
Kanamori, A.; Inoue, S.; Iwasaki, M.; Kitajima, K.; Kawai, G.; Yokoyama, S.; Inoue, Y. Deaminated neuraminic acid-rich glycoprotein of rainbow trout egg vitelline envelope. Occurrence of a novel alpha-2,8-linked oligo(deaminated neuraminic acid) structure in O-linked glycan chains. J. Biol. Chem. 1990, 265, 21811–21819.
[83]
Tezuka, T.; Taguchi, T.; Kanamori, A.; Muto, Y.; Kitajima, K.; Inoue, Y.; Inoue, S. Identification and structural determination of the KDN-containing N-linked glycan chains consisting of bi- and triantennary complex-type units of KDN-glycoprotein previously isolated from rainbow trout vitelline envelopes. Biochemistry 1994, 33, 6495–6502, doi:10.1021/bi00187a016.
[84]
Inoue, S.; Inoue, Y. Fish Glycoprotein. In Glycoprotein II; Montreuil, J., Vliegenthart, J.F.G., Schachter, H., Eds.; Elsevier Science BV: Amsterdam, The Netherlands, 1997; Volume 29, pp. 143–161.
[85]
Pillai, M.C.; Clark, W.H., Jr. Development of cortical vesicles in Sicyonia ingentis ova: Their heterogeneity and role in elaboration of the hatching envelope. Mol. Reprod. Dev. 1990, 26, 78–89, doi:10.1002/mrd.1080260112.
[86]
Dupré, E.; Gòmez, D.; Araya, A.; Gallardo, C. Role of egg surface glycoconjugate in the fertilization of the rock shrimp Rhynchocinetes typus (Milne-Edwards, 1837). Lat. Am. J. Aquat. Res. 2012, 40, 22–29, doi:10.3856/vol40-issue1-fulltext-3.
[87]
Litscher, E.; Honegger, T.G. Glycoprotein constituents of the vitelline coat of Phallusia mammillata (Ascidiacea) with fertilization inhibiting activity. Dev. Biol. 1991, 148, 536–551, doi:10.1016/0012-1606(91)90272-5.
[88]
Baginski, T.; Hirohashi, N.; Hoshi, M. Sulfated O-linked glycans of the vitelline coat as ligands in gamete interaction in the ascidian, Halocynthia roretzi. Dev. Growth Differ. 1999, 41, 357–364.
[89]
De Santis, R.; Pinto, M.R. Gamete Interaction in Ascidians: Sperm Binding and Penetration through the Vitelline Coat. In Mechanism of Fertilization: Plants to Humans; Dale, B., Ed.; Springer-Verlag: Berlin, Germany, 1990; pp. 297–304.
[90]
Rosati, F.; Cotelli, F.; de Santis, R.; Monroy, A.; Pinto, M.R. Synthesis of fucosyl-containing glycoproteins of the vitelline coat in oocytes of Ciona intestinalis (Ascidia). Proc. Natl. Acad. Sci. USA 1982, 79, 1908–1911.
[91]
SeGall, G.K.; Lennarz, W.J. Chemical characterization of the component of the jelly coat from sea urchin eggs responsible for induction of the acrosome reaction. Dev. Biol. 1979, 71, 33–48, doi:10.1016/0012-1606(79)90080-0.
[92]
Shimizu, T.; Kinoh, H.; Yamaguchi, M.; Suzuki, N. Purification and characterization of the egg jelly macromolecules, sialoglycoprotein and fucose sulfate glycoconjugate, of the sea urchin Hemicentrotus Pulcherrimus. Dev. Growth Differ. 1990, 32, 473–487.
[93]
Kitazume, S.; Kitajima, K.; Inoue, S.; Troy, F.A., II.; Cho, J.W.; Lennarz, W.J.; Inoue, Y. Identification of polysialic acid-containing glycoprotein in the jelly coat of sea urchin eggs. Occurrence of a novel type of polysialic acid structure. J. Biol. Chem. 1994, 269, 22712–22718.
[94]
Hirohashi, N.; Kamei, N.; Kubo, H.; Sawada, H.; Matsumoto, M.; Hoshi, M. Egg and sperm recognition systems during fertilization. Dev. Growth Differ. 2008, 50, S221–S238, doi:10.1111/j.1440-169X.2008.01017.x.
[95]
Mulloy, B.; Ribeiro, A.C.; Alves, A.P.; Vieira, R.P.; Mourao, P.A. Sulfated fucans from echinoderms have a regular tetrasaccharide repeating unit defined by specific patterns of sulfation at the 0–2 and 0–4 positions. J. Biol. Chem. 1994, 269, 22113–22123.
[96]
Alves, A.P.; Mulloy, B.; Diniz, J.A.; Mourao, P.A. Sulfated polysaccharides from the egg jelly layer are species-specific inducers of acrosomal reaction in sperms of sea urchins. J. Biol. Chem. 1997, 272, 6965–6971, doi:10.1074/jbc.272.11.6965.
[97]
Vacquier, V.D.; Moy, G.W. The fucose sulfate polymer of egg jelly binds to sperm REJ and is the inducer of the sea urchin sperm acrosome reaction. Dev. Biol. 1997, 192, 125–135, doi:10.1006/dbio.1997.8729.
[98]
Alves, A.P.; Mulloy, B.; Moy, G.W.; Vacquier, V.D.; Mourao, P.A. Females of the sea urchin Strongylocentrotus purpuratus differ in the structures of their egg jelly sulfated fucans. Glycobiology 1998, 8, 939–946, doi:10.1093/glycob/8.9.939.
[99]
Vilela-Silva, A.C.; Castro, M.O.; Valente, A.P.; Biermann, C.H.; Mourao, P.A. Sulfated fucans from the egg jellies of the closely related sea urchins Strongylocentrotus droebachiensis and Strongylocentrotus pallidus ensure species-specific fertilization. J. Biol. Chem. 2002, 277, 379–387.
[100]
Endo, T.; Hoshi, M.; Endo, S.; Arata, Y.; Kobata, A. Structures of the sugar chains of a major glycoprotein present in the egg jelly coat of a starfish, Asterias amurensis. Arch. Biochem. Biophys. 1987, 252, 105–112, doi:10.1016/0003-9861(87)90013-0.
[101]
Hoshi, M.; Nishigaki, T.; Ushiyama, A.; Okinaga, T.; Chiba, K.; Matsumoto, M. Egg-jelly signal molecules for triggering the acrosome reaction in starfish spermatozoa. Int. J. Dev. Biol. 1994, 38, 167–174.
[102]
Uno, Y.; Hoshi, M. Separation of the sperm agglutinin and the acrosome reaction-inducing substance in egg jelly of starfish. Science 1978, 200, 58–59.
[103]
Naruse, M.; Suetomo, H.; Matsubara, T.; Sato, T.; Yanagawa, H.; Hoshi, M.; Matsumoto, M. Acrosome reaction-related steroidal saponin, Co-ARIS, from the starfish induces structural changes in microdomains. Dev. Biol. 2010, 347, 147–153, doi:10.1016/j.ydbio.2010.08.019.
[104]
Koyota, S.; Wimalasiri, K.M.; Hoshi, M. Structure of the main saccharide chain in the acrosome reaction-inducing substance of the starfish, Asterias amurensis. J. Biol. Chem. 1997, 272, 10372–10376, doi:10.1074/jbc.272.16.10372.
[105]
Gunaratne, H.M.; Yamagaki, T.; Matsumoto, M.; Hoshi, M. Biochemical characterization of inner sugar chains of acrosome reaction-inducing substance in jelly coat of starfish eggs. Glycobiology 2003, 13, 567–580, doi:10.1093/glycob/cwg070.
[106]
Hoshi, M.; Moriyama, H.; Matsumoto, M. Structure of acrosome reaction-inducing substance in the jelly coat of starfish eggs: A mini review. Biochem. Biophys. Res. Commun. 2012, 425, 595–598, doi:10.1016/j.bbrc.2012.08.033.
[107]
Suphamungmee, W.; Chansela, P.; Weerachatyanukul, W.; Poomtong, T.; Vanichviriyakit, R.; Sobhon, P. Ultrastructure, composition, and possible roles of the egg coats in Haliotis asinin. J. Shellfish Res. 2010, 29, 687–697, doi:10.2983/035.029.0320.
[108]
Shigekawa, K.; Clark, W.H., Jr. Spermiogenesis in the marine shrimp, Sicyonia ingentis. Dev. Growth Differ. 1986, 28, 95–112.
[109]
Nagao, J.; Munehara, H. Annual cycle of testicular maturation in the helmet crab Telmessus cheiragonus. Fish. Sci. 2003, 69, 1200–1208, doi:10.1111/j.0919-9268.2003.00746.x.
[110]
Okumura, T.; Hara, M. Androgenic gland cell structure and spermatogenesis during the molt cycle and correlation to morphotypic differentiation in the giant freshwater prawn, Macrobrachium rosenbergii. Zool. Sci. 2004, 21, 621–628, doi:10.2108/zsj.21.621.
[111]
Garcia, T.M.; Silva, J.R.F. Testis and vas deferens morphology of the red-clawed mangrove tree crab (Goniopsis cruentata) (Latreille, 1803). Braz. Arch. Biol. Technol. 2006, 49, 339–345.
[112]
Jones, R.; Brown, C.R.; Lancaster, R.T. Carbohydrate-binding properties of boar sperm proacrosin and assessment of its role in sperm-egg recognition and adhesion during fertilization. Dev. Genes Evol. 1988, 102, 781–779.
[113]
Anakwe, O.O.; Gerton, G.L. Acrosome biogenesis begins during meiosis: Evidence from the synthesis and distribution of an acrosomal glycoprotein, acrogranin, during guinea pig spermatogenesis. Biol. Reprod. 1990, 42, 317–328, doi:10.1095/biolreprod42.2.317.
[114]
Martinez-Menarguez, J.A.; Ballesta, J.; Aviles, M.; Castells, M.T.; Madrid, J.F. Cytochemical characterization of glycoproteins in the developing acrosome of rats. An ultrastructural study using lectin histochemistry, enzymes and chemical deglycosylation. Histochemistry 1992, 97, 439–449, doi:10.1007/BF00270391.
[115]
Pratt, S.A.; Scully, N.F.; Shur, B.D. Cell surface beta 1,4 galactosyltransferase on primary spermatocytes facilitates their initial adhesion to Sertoli cells in vitro. Biol. Reprod. 1993, 49, 470–482, doi:10.1095/biolreprod49.3.470.
[116]
Raychoudhury, S.S.; Millette, C.F. Multiple fucosyltransferases and their carbohydrate ligands are involved in spermatogenic cell-Sertoli cell adhesion in vitro in rats. Biol. Reprod. 1997, 56, 1268–1273.
[117]
Schulz, R.W.; Miura, T. Spermatogenesis and its endocrine regulation. Fish. Physiol. Biochem. 2002, 26, 43–56, doi:10.1023/A:1023303427191.
[118]
Nobrega, R.H.; Batlouni, S.R.; Franca, L.R. An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish. Fish. Physiol. Biochem. 2009, 35, 197–206, doi:10.1007/s10695-008-9252-z.
[119]
Parenti, L.R.; Grier, H.J. Evolution and phylogeny of gonad morphology in bony fishes. Integr. Comp. Biol. 2004, 44, 333–348, doi:10.1093/icb/44.5.333.
[120]
Desantis, S.; Zizza, S.; Garcia-Lopez, A.; Sciscioli, V.; Mananos, E.; de Metrio, V.G.; Sarasquete, C. Lectin-binding pattern of Senegalese sole Solea senegalensis (Kaup) testis. Histol. Histopathol. 2010, 25, 205–216.
[121]
Liguoro, A.; Prisco, M.; Mennella, C.; Ricchiari, L.; Angelini, F.; Andreuccetti, P. Distribution of terminal sugar residues in the testis of the spotted ray Torpedo marmorata. Mol. Reprod. Dev. 2004, 68, 524–530, doi:10.1002/mrd.20112.
[122]
Tokalov, S.V.; Gutzeit, H.O. Lectin-binding pattern as tool to identify and enrich specific primary testis cells of the tilapia (Oreochromis niloticus) and medaka (Oryzias latipes). J. Exp. Zool. Part A 2007, 308, 127–138.
[123]
Varki, A.; Cummings, R.; Esko, J.; Freeze, H.; Hart, G.; Marth, J. Nuclear and Cytoplasmic Glycosylation. In Essentials of Glycobiology; Varki, A., Cummings, R., Esko, J., Freeze, H., Hart, G., Marth, J., Eds.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 1999; pp. 171–183.
[124]
Martinez-Menarguez, J.A.; Aviles, M.; Madrid, J.F.; Castells, M.T.; Ballesta, J. Glycosylation in Golgi apparatus of early spermatids of rat. A high resolution lectin cytochemical study. Eur. J. Cell Biol. 1993, 61, 21–33.
[125]
Unuma, T.; Yamamoto, T.; Akiyama, T.; Shiraishi, M.; Ohta, H. Quantitative changes in yolk protein and other components in the ovary and testis of the sea urchin Pseudocentrotus depressus. J. Exp. Biol. 2003, 206, 365–372, doi:10.1242/jeb.00102.
[126]
Verhey, C.A.; Moyer, F.H. Fine structural changes during sea urchin oogenesis. J. Exp. Zool. 1967, 162, 195–225, doi:10.1002/jez.1401640206.
[127]
Marsh, A.G.; Watts, S.A. Energy metabolism and gonad development. Dev. Aquac. Fish. Sci. 2001, 32, 27–42, doi:10.1016/S0167-9309(01)80004-1.
[128]
Miyata, S.; Sato, C.; Kitamura, S.; Toriyama, M.; Kitajima, K. A major flagellum sialoglycoprotein in sea urchin sperm contains a novel polysialic acid, an alpha2,9-linked poly-N-acetylneuraminic acid chain, capped by an 8-O-sulfated sialic acid residue. Glycobiology 2004, 14, 827–840, doi:10.1093/glycob/cwh100.
[129]
Miyata, S.; Sato, C.; Kumita, H.; Toriyama, M.; Vacquier, V.D.; Kitajima, K. Flagellasialin: A novel sulfated alpha2,9-linked polysialic acid glycoprotein of sea urchin sperm flagella. Glycobiology 2006, 16, 1229–1241, doi:10.1093/glycob/cwl036.
[130]
Kambara, Y.; Shiba, K.; Yoshida, M.; Sato, C.; Kitajima, K.; Shingyoji, C. Mechanism regulating Ca2+-dependent mechanosensory behaviour in sea urchin spermatozoa. Cell Struct. Funct. 2011, 36, 69–82, doi:10.1247/csf.10020.
[131]
Ijuin, T.; Kitajima, K.; Song, Y.; Kitazume, S.; Inoue, S.; Haslam, S.M.; Morris, H.R.; Dell, A.; Inoue, Y. Isolation and identification of novel sulfated and nonsulfated oligosialyl glycosphingolipids from sea urchin sperm. Glycoconj. J. 1996, 13, 401–413, doi:10.1007/BF00731473.
[132]
Miyata, S.; Yamakawa, N.; Toriyama, M.; Sato, C.; Kitajima, K. Co-expression of two distinct polysialic acids, alpha2,8- and alpha2,9-linked polymers of N-acetylneuraminic acid, in distinct glycoproteins and glycolipids in sea urchin sperm. Glycobiology 2011, 21, 1596–1605, doi:10.1093/glycob/cwr081.
[133]
Desantis, S.; Labate, M.; Maiorano, P.; Tursi, A. An ultrastructural and histochemical study of the germinal cells contained in hemispermatophores of males of the Aristaeomorpha foliacea (Risso, 1827). Hydrobiologia 2006, 557, 41–49, doi:10.1007/s10750-005-1306-y.
[134]
Subramonian, T. Spermatophore formation in two intertidal crabs Albunea symnista and Emerita asiatica (Decapoda: Anomura). Biol. Bull. 1984, 166, 78–95, doi:10.2307/1541432.
[135]
Radha, T.; Subramonian, T. Origin and nature of spermatophoric mass of spiny lobster Panulirus homarus. Mar. Biol. 1985, 86, 13–19, doi:10.1007/BF00392575.
[136]
Yufeng, W.; Nanshan, D.; Wei, L. A histochemical study on the male reproductive system of Macrobrachium rosenbergii. J. Northwest Atl. Fish. Sci. 1997, 4, 13–16.
[137]
Sasikala, S.L.; Subramoniam, T. On the occurrence of acid mucopolysaccharides in the spermatophores of two marine prawns, Penaeus indiens (Milne-Edwards) and Metapenaeus monoceros (Fabricius) (Crustacea: Macrura). J. Exp. Mar. Biol. Ecol. 1987, 113, 145–153, doi:10.1016/0022-0981(87)90161-4.
[138]
Subramonian, T. Chemical Composition of Spermatophores in Decapod Crustaceans. In Crustacean Sexual Biology; Bauer, R.T., Martin, J.A., Eds.; Columbia University Press: New York, NY, USA, 1991; pp. 308–321.
[139]
Desantis, S.; Labate, M.; Cirillo, F.; Labate, G.M. Testicular activity and sperm glycoproteins in giant red shrimp (Aristaeomorpha foliacea). J. Northwest Atl. Fish. Sci. 2003, 31, 205–212.
[140]
Yanagimachi, R. Fertility of mammalian spermatozoa: Its development and relativity. Zygote 1994, 2, 371–372.
[141]
Snell, W.J.; White, J.M. The molecules of mammalian fertilization. Cell 1996, 85, 629–637, doi:10.1016/S0092-8674(00)81230-1.
Tosti, E. Sperm activation in species with external fertilisation. Zygote 1994, 2, 359–361.
[144]
Wassarman, P.M.; Litscher, E.S. Towards the molecular basis of sperm and egg interaction during mammalian fertilization. Cells Tissues Organs 2001, 168, 36–45, doi:10.1159/000016804.
[145]
Monroy, A.; Rosati, F. A comparative analysis of sperm-egg interaction. Gamete Res. 1983, 7, 85–102, doi:10.1002/mrd.1120070108.
[146]
Wassarman, P.M. The biology and chemistry of fertilization. Science 1987, 235, 553–560.
[147]
Moy, G.W.; Mendoza, L.M.; Schulz, J.R.; Swanson, W.J.; Glabe, C.G.; Vacquier, V.D. The sea urchin sperm receptor for egg jelly is a modular protein with extensive homology to the human polycystic kidney disease protein, PKD1. J. Cell Biol. 1996, 133, 809–817, doi:10.1083/jcb.133.4.809.
[148]
Mengerink, K.J.; Vacquier, V.D. Glycobiology of sperm-egg interactions in deuterostomes. Glycobiology 2001, 11, 37R–43R, doi:10.1093/glycob/11.4.37R.
[149]
Vacquier, V.D.; Swanson, W.J.; Hellberg, M.E. What have we learned about sea urchin sperm bindin? Dev. Growth Differ. 1995, 37, 1–10.
[150]
Ohlendieck, K.; Partin, J.S.; Stears, R.L.; Lennarz, W.J. Developmental expression of the sea urchin egg receptor for sperm. Dev. Biol. 1994, 165, 53–62, doi:10.1006/dbio.1994.1233.
[151]
Dhume, S.T.; Lennarz, W.J. The involvement of O-linked oligosaccharide chains of the sea urchin egg receptor for sperm in fertilization. Glycobiology 1995, 5, 11–17, doi:10.1093/glycob/5.1.11.
[152]
Hirohashi, N.; Lennarz, W.J. Role of a vitelline layer-associated 350 kDa glycoprotein in controlling species-specific gamete interaction in the sea urchin. Dev. Growth Differ. 2001, 43, 247–255, doi:10.1046/j.1440-169x.2001.00571.x.
[153]
Hoshi, M.; Matsui, T.; Nishiyama, I.; Amano, T.; Okita, Y. Physiological inducers of the acrosome reaction. Cell Differ. Dev. 1988, 25 Suppl., 19–24, doi:10.1016/0922-3371(88)90095-0.
[154]
Longo, F.J.; Ushiyama, A.; Chiba, K.; Hoshi, M. Ultrastructural localization of acrosome reaction-inducing substance (ARIS) on sperm of the starfish Asterias amurensis. Mol. Reprod. Dev. 1995, 41, 91–99, doi:10.1002/mrd.1080410114.
[155]
Ushiyama, A.; Araki, T.; Chiba, K.; Hoshi, M. Specific binding of acrosome-reaction-inducing substance to the head of starfish spermatozoa. Zygote 1993, 1, 121–127.
[156]
Hoshi, M.; Amano, T.; Okita, Y.; Okinaga, T.; Matsui, T. Egg signals for triggering the acrosome reaction in starfish spermatozoa. J. Reprod. Fertil. 1990, 42, 23–31.
[157]
Nishiyama, I.; Matsui, T.; Fujimoto, Y.; Ikekawa, N.; Hoshi, M. Correlation between the molecular structure and the biological activity of Co-ARIS, a cofactor for acrosome reaction-inducing substance. Dev. Growth Differ. 1987, 29, 171–176.
[158]
Nishigaki, T.; Chiba, K.; Miki, W.; Hoshi, M. Structure and function of asterosaps, sperm-activating peptides from the jelly coat of starfish eggs. Zygote 1996, 4, 237–245.
[159]
Nishigaki, T.; Chiba, K.; Hoshi, M. A 130-kDa membrane protein of sperm flagella is the receptor for asterosaps, sperm-activating peptides of starfish Asterias amurensis. Dev. Biol. 2000, 219, 154–162, doi:10.1006/dbio.1999.9598.
[160]
Matsumoto, M.; Hirata, J.; Hirohashi, N.; Hoshi, M. Sperm-egg binding mediated by sperm alpha-D-fucosidase in the ascidian, Halocynthia roretzi. Zool. Sci. 2002, 19, 43–48, doi:10.2108/zsj.19.43.
[161]
Matsumoto, M.; Kawase, O.; Islam, M.S.; Naruse, M.; Watanabe, S.N.; Ishikawa, R.; Hoshi, M. Regulation of the starfish sperm acrosome reaction by cGMP, pH, cAMP and Ca2+. Int. J. Dev. Biol. 2008, 52, 523–526, doi:10.1387/ijdb.072511mm.
[162]
Swanson, W.J.; Vacquier, V.D. The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule. Proc. Natl. Acad. Sci. USA 1997, 94, 6724–6729, doi:10.1073/pnas.94.13.6724.
[163]
Vacquier, V.D.; Carner, K.R.; Stout, C.D. Species-specific sequences of abalone lysin, the sperm protein that creates a hole in the egg envelope. Proc. Natl. Acad. Sci. USA 1990, 87, 5792–5796, doi:10.1073/pnas.87.15.5792.
[164]
Kresge, N.; Vacquier, V.D.; Stout, C.D. Abalone lysin: The dissolving and evolving sperm protein. Bioessays 2001, 23, 95–103.
[165]
Swanson, W.J.; Aquadro, C.F.; Vacquier, V.D. Polymorphism in abalone fertilization proteins is consistent with the neutral evolution of the egg’s receptor for lysin (VERL) and positive darwinian selection of sperm lysin. Mol. Biol. Evol. 2001, 18, 376–383, doi:10.1093/oxfordjournals.molbev.a003813.
[166]
Hoshi, M.; de Santis, R.; Pinto, M.R.; Cotelli, F.; Rosati, F. Sperm glycosidases as mediators of sperm-egg binding in the ascidians. Zool. Sci. 1985, 2, 65–69.
[167]
Hoshi, M. Sperm glycosidase as a plausible mediator of sperm binding to the vitelline envelope in Ascidians. Adv. Exp. Med. Biol. 1986, 207, 251–260.
[168]
Godknecht, A.; Honegger, T.G. Isolation, characterization, and localization of a sperm-bound N-acetylglucosaminidase that is indispensable for fertilization in the ascidian, Phallusia mammilla. Dev. Biol. 1991, 143, 398–407, doi:10.1016/0012-1606(91)90090-P.
[169]
Godknecht, A.J.; Honegger, T.G. Specific inhibition of sperm β-N-acetylglucosaminidase by the synthetic inhibitor N-acetylglucosaminono-1,5-lactone O-(phenylcarbamoyl)oxime inhibits fertilization in the ascidian, Phallusia mammillata. Dev. Growth Differ. 1995, 37, 183–189.
[170]
Xie, M.; Honegger, T.G. Ultrastructural investigations on sperm penetration and gamete fusion in the ascidians Boltenia villosa and Phallusia mammillata. Mar. Biol. , 1993 116, 117–127.
[171]
Hoshi, M.; de Santis, R.; Pinto, M.R.; Cotelli, F.; Rosati, F. Is Sperm L-fucosidase Responsible for Sperm-Egg Binding in Ciona Intestinalis. In The Sperm Cell; André, J., Ed.; Martinus Nijhoff: Leiden, NL, USA, 1983; pp. 107–110.
[172]
Fukumoto, M. Fertilization in ascidians apical processes and gamete fusion in Ciona intestinalis spermatozoa. J. Cell Sci. 1988, 89, l89–l96.
[173]
Fukumoto, M. Morphological aspects of ascidian fertilization: Acrosome reaction, apical processes and gamete fusion in Ciona intestinalis. Invertebr. Reprod. Dev. 1990, 17, 147–154, doi:10.1080/07924259.1990.9672103.
[174]
Fukumoto, M.; Numakunai, T. Morphological aspects of fertilization in Halocynthia roretzi (Ascidiacea, Tunicata). J. Struct. Biol. 1995, 114, 157–166, doi:10.1006/jsbi.1995.1015.
[175]
Sawada, H.; Sakai, N.; Abe, Y.; Tanaka, E.; Takahashi, Y.; Fujino, J.; Kodama, E.; Takizawa, S.; Yokosawa, H. Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc. Natl. Acad. Sci. USA 2002, 99, 1223–1228.
[176]
Sawada, H.; Yokosawa, H.; Ishii, S. Purification and characterization of two types of trypsin-like enzymes from sperm of the ascidian (Prochordata) Halocynthia roretzi. Evidence for the presence of spermosin, a novel acrosin-like enzyme. J. Biol. Chem. 1984, 259, 2900–2904.
[177]
Lambert, C.C.; Someno, T.; Sawada, H. Sperm surface proteases in ascidian fertilization. J. Exp. Zool. 2002, 292, 88–95, doi:10.1002/jez.1145.
[178]
Dupre, E.M.; Barros, C. In vitro fertilization of the rock shrimp, Rhynchocinetes typus (Decapoda, Caridea): A review. Biol. Res. 2011, 44, 125–133, doi:10.4067/S0716-97602011000200003.
[179]
Barros, C.; Dupré, E.; Viveros, L. Sperm-egg interactions in the shrimp Rhynchocinetes typus. Gamete Res. 1986, 14, 171–180, doi:10.1002/mrd.1120140208.
[180]
Rios, M.; Barros, C. Trypsin-like enzymes during fertilization in the shrimp Rhynchocinetes typus. Mol. Reprod. Dev. 1997, 46, 581–586, doi:10.1002/(SICI)1098-2795(199704)46:4<581::AID-MRD15>3.0.CO;2-Z.
[181]
Bustamante, E.; Palomino, J.; Amoroso, A.; Moreno, R.D.; Barros, C. Purification and biochemical characterization of a trypsin-like enzyme present in the sperm of the rock shrimp, Rhynchocinetes typus. Invertebr. Reprod. Dev. 2001, 39, 175–181, doi:10.1080/07924259.2001.9652482.
Foltz, K.R.; Shilling, F.M. Receptor-mediated signal transduction and egg activation. Zygote 1993, 1, 276–279.
[184]
Hirohashi, N.; Lennarz, W.J. Sperm-egg binding in the sea urchin: A high level of intracellular ATP stabilizes sperm attachment to the egg receptor. Dev. Biol. 1998, 201, 270–279, doi:10.1006/dbio.1998.8984.
[185]
Kamei, N.; Glabe, C.G. The species-specific egg receptor for sea urchin sperm adhesion is EBR1, a novel ADAMTS protein. Genes Dev. 2003, 17, 2502–2507, doi:10.1101/gad.1133003.
[186]
Kamei, N.; Swanson, W.J.; Glabe, C.G. A rapidly diverging EGF protein regulates species-specific signal transduction in early sea urchin development. Dev. Biol. 2000, 225, 267–276, doi:10.1006/dbio.2000.9837.
[187]
Hagstrom, B.E. Further studies on cross fertilization in sea urchins. Exp. Cell Res. 1956, 11, 507–510, doi:10.1016/0014-4827(56)90132-X.
[188]
Adelson, D.L.; Alliegro, M.C.; McClay, D.R. On the ultrastructure of hyalin, a cell adhesion protein of the sea urchin embryo extracellular matrix. J. Cell Biol. 1992, 116, 1283–1289, doi:10.1083/jcb.116.5.1283.
[189]
Shapiro, B.M.; Somers, C.; Weidman, P.J. Extracellular Remodeling during Fertilization. In Cell Biology of Fertilization; Schatten, H., Schatten, G., Eds.; Academic Press: San Diego, CA, USA, 1989; pp. 251–276.
[190]
Somers, C.E.; Shapiro, B.M. Functional domains of proteoliaisin, the adhesive protein that orchestrates fertilization envelope assembly. J. Biol. Chem. 1991, 266, 16870–16875.
[191]
Nomura, K.; Suzuki, N. Sea urchin ovoperoxidase: Solubilization and isolation from the fertilization envelope, some structural and functional properties, and degradation by hatching enzyme. Arch. Biochem. Biophys. 1995, 319, 525–534, doi:10.1006/abbi.1995.1327.
[192]
Inoue, S.; Inoue, Y. Fertilization (activation)-induced 200- to 9-kDa depolymerization of polysialoglycoprotein, a distinct component of cortical alveoli of rainbow trout eggs. J. Biol. Chem. 1986, 261, 5256–5261.
[193]
Inoue, S.; Kitajima, K.; Inoue, Y.; Kudo, S. Localization of polysialoglycoprotein as a major glycoprotein component in cortical alveoli of the unfertilized eggs of Salmo gairdneri. Dev. Biol. 1987, 123, 442–454, doi:10.1016/0012-1606(87)90402-7.
[194]
Laale, H.W. The perivitelline space and egg envelopes of bony fishes: A review. Copeia 1980, 1980, 210–226, doi:10.2307/1443999.
[195]
Rudy, P.P., Jr.; Potts, W.T. Sodium balance in the eggs of the Atlantic salmon, Salmo salar. J. Exp. Biol. 1969, 50, 239–246.
[196]
Eddy, F.B. Osmotic properties of the perivitelline fluid and some properties of the chorion of Atlantic salmon eggs (Salmo salar). J. Zool. 1974, 174, 237–243, doi:10.1111/j.1469-7998.1974.tb03154.x.
[197]
Peterson, R.H.; Martin-Robichaud, D.J. Rates of ionic diffusion across the egg chorion of Atlantic salmon (Salmo salar). Physiol. Zool. 1993, 66, 289–306.
[198]
Li, X.; Jenssen, E.; Fyhn, H.J. Effects of salinity on egg swelling in Atlantic salmon (Salmo salar). Aquaculture 1989, 76, 317–334, doi:10.1016/0044-8486(89)90084-7.
[199]
Kudo, S. Fertilization, cortical reaction, polyspermy-preventing and anti-microbial mechanisms in fish eggs. Bull. Inst. Zool. Acad. Sci. Monogr. 1991, 16, 313–340.
[200]
Kobayashi, W.; Yamamoto, T.S. Factors inducing closure of the micropylar canal in the chum salmon egg. J. Fish. Biol. 1993, 42, 385–394, doi:10.1111/j.1095-8649.1993.tb00341.x.
[201]
Kudo, S.; Teshima, C. Assembly in vitro of vitelline envelope components induced by a cortical alveolus sialoglycoprotein of eggs of the fish Tribolodon hakonensis. Zygote 1998, 6, 193–201, doi:10.1017/S0967199498000124.
[202]
Oppen-Berntsen, D.O.; Helvik, J.V.; Walther, B.T. The major structural proteins of cod (Gadus morhua) eggshells and protein crosslinking during teleost egg hardening. Dev. Biol. 1990, 137, 258–265, doi:10.1016/0012-1606(90)90252-E.
[203]
Koyanagi, R.; Honegger, T.G. Molecular cloning and sequence analysis of an ascidian egg beta-N-acetylhexosaminidase with a potential role in fertilization. Dev. Growth Differ. 2003, 45, 209–218, doi:10.1046/j.1524-4725.2003.689.x.
[204]
Lambert, C.C. Fertilization-induced modification of chorion N-acetylglucosamine groups blocks polyspermy in ascidian eggs. Dev. Biol. 1986, 116, 168–173, doi:10.1016/0012-1606(86)90053-9.
[205]
Lambert, C.C. Ascidian eggs release glycosidase activity which aids in the block against polyspermy. Development 1989, 105, 415–420.
[206]
Schneider, E.G.; Nguyen, H.T.; Lennarz, W.J. The effect of tunicamycin, an inhibitor of protein glycosylation, on embryonic development in the sea urchin. J. Biol. Chem. 1978, 253, 2348–2355.
[207]
Heifetz, A.; Lennarz, W.J. Biosynthesis of N-glycosidically linked glycoproteins during gastrulation of sea urchin embryos. J. Biol. Chem. 1979, 254, 6119–6127.
Carson, D.D.; Lennarz, W.J. Inhibition of polyisoprenoid and glycoprotein biosynthesis causes abnormal embryonic development. Proc. Natl. Acad. Sci. USA 1979, 76, 5709–5713.
[210]
Carson, D.D.; Lennarz, W.J. Relationship of dolichol synthesis to glycoprotein synthesis during embryonic development. J. Biol. Chem. 1981, 256, 4679–4686.
[211]
Carson, D.D.; Farach, M.C.; Earles, D.S.; Decker, G.L.; Lennarz, W.J. A monoclonal antibody inhibits calcium accumulation and skeleton formation in cultured embryonic cells of the sea urchin. Cell 1985, 41, 639–648, doi:10.1016/S0092-8674(85)80036-2.
[212]
Farach, M.C.; Valdizan, M.; Park, H.R.; Decker, G.L.; Lennarz, W.J. Developmental expression of a cell-surface protein involved in calcium uptake and skeleton formation in sea urchin embryos. Dev. Biol. 1987, 122, 320–331, doi:10.1016/0012-1606(87)90297-1.
[213]
Farach-Carson, M.C.; Carson, D.D.; Collier, J.L.; Lennarz, W.J.; Park, H.R.; Wright, G.C. A calcium-binding, asparagine-linked oligosaccharide is involved in skeleton formation in the sea urchin embryo. J. Cell Biol. 1989, 109, 1289–1299, doi:10.1083/jcb.109.3.1289.
[214]
Decker, G.L.; Valdizan, M.C.; Wessel, G.M.; Lennarz, W.J. Developmental distribution of a cell surface glycoprotein in the sea urchin Strongylocentrotus purpuratus. Dev. Biol. 1988, 129, 339–349, doi:10.1016/0012-1606(88)90381-8.
[215]
Anstrom, J.A.; Chin, J.E.; Leaf, D.S.; Parks, A.L.; Raff, R.A. Localization and expression of msp130, a primary mesenchyme lineage-specific cell surface protein in the sea urchin embryo. Development 1987, 101, 255–265.
[216]
McClay, D.R.; Matranga, V.; Wessel, G. Expression and Appearance of Germ-Layer Specific Antigens on the Surface of Embryonic Sea Urchin Cells. In The Cellular and Molecular Biology of Invertebrate Development; Sawyer, R.H., Showman, R.M., Eds.; University of South Carolina Press: Columbia, SC, USA, 1985; pp. 171–186.
[217]
Kabakoff, B.; Lennarz, W.J. Inhibition of glycoprotein processing blocks assembly of spicules during development of the sea urchin embryo. J. Cell Biol. 1990, 111, 391–400, doi:10.1083/jcb.111.2.391.
[218]
Hoshi, M.; Nagai, Y. Biochemistry of mucolipids of sea urchin gametes and embryos. 3. Mucolipids during early development. Jpn. J. Exp. Med. 1970, 40, 361–365.
[219]
Cheresh, D.A.; Klier, F.G. Disialoganglioside GD2 distributes preferentially into substrate-associated microprocesses on human melanoma cells during their attachment to fibronectin. J. Cell Biol. 1986, 102, 1887–1897, doi:10.1083/jcb.102.5.1887.
[220]
Spiegel, S.; Yamada, K.M.; Hom, B.E.; Moss, J.; Fishman, P.H. Fluorescent gangliosides as probes for the retention and organization of fibronectin by ganglioside-deficient mouse cells. J. Cell Biol. 1985, 100, 721–726, doi:10.1083/jcb.100.3.721.
[221]
Wessel, G.M.; Marchase, R.B.; McClay, D.R. Ontogeny of the basal lamina in the sea urchin embryo. Dev. Biol. 1984, 103, 235–245, doi:10.1016/0012-1606(84)90025-3.
[222]
Jackson, R.L.; Busch, S.J.; Cardin, A.D. Glycosaminoglycans: Molecular properties, protein interactions, and role in physiological processes. Physiol. Rev. 1991, 71, 481–539.
[223]
Vilela-Silva, A.C.; Werneck, C.C.; Valente, A.P.; Vacquier, V.D.; Mourao, P.A. Embryos of the sea urchin Strongylocentrotus purpuratus synthesize a dermatan sulfate enriched in 4-O- and 6-O-disulfated galactosamine units. Glycobiology 2001, 11, 433–440, doi:10.1093/glycob/11.6.433.
[224]
Oguri, K.; Yamagata, T. Appearance of a proteoglycan in developing sea urchin embryos. Biochim. Biophys. Acta 1978, 541, 385–393, doi:10.1016/0304-4165(78)90197-6.
[225]
Kinoshita, S.; Yoshii, K. The role of proteoglycan synthesis in the development of sea urchins. II. The effect of administration of exogenous proteoglycan. Exp. Cell Res. 1979, 124, 361–369, doi:10.1016/0014-4827(79)90211-8.
[226]
Akasaka, K.; Amemiya, S.; Terayama, H. Scanning electron microscopical study of the inside of sea urchin embryos (Pseudocentotus depressus). Effects of Aryl beta-xyloside, tunicamycin and deprivation of sulfate tions. Exp. Cell Res. 1980, 129, 1–13, doi:10.1016/0014-4827(80)90325-0.
[227]
Solursh, M.; Mitchell, S.L.; Katow, H. Inhibition of cell migration in sea urchin embryos by beta-D-xyloside. Dev. Biol. 1986, 118, 325–332, doi:10.1016/0012-1606(86)90001-1.