ABSTRACT
Gynogenetic silver crucian carp, Carassius auratus gibelio, is an intriguing model system. In the present work, a systemic study has been initiated by introducing suppression subtractive hybridization technique into this model system to identify the differentially expressed genes in oocytes between gynogenetic silver crucian carp and its closely related gonochoristic color crucian carp. Five differential cDNA fragments were identified from the preliminary screening, and two of them are ZP3 homologues. Moreover, the full length ZP3 cDNAs were cloned from their oocyte cDNA libraries. The length of ZP3 cDNAs were 1378 bp for gyno-carp and 1367 bp for gono-carp, and they can be translated into proteins with 435 amino acids. Obvious differences are not only in the composition of amino acids, but also in the number of potential O-linked oligosaccharide sites. In addition, gyno-carp ZP3 amino acid sequence has an unexpected higher identity value with common carp (83.5%) than that with the closely related gono-carp (74.7%). The unique homology may be originated from the ancient hybridization. Northern blot analysis confirmed that expression of the ZP3 gene occurred exclusively in the oocytes. Because O-linked oligosaccharides on ZP3 have been demonstrated to play very important roles in fertilization, it is suggested that the extra O-linked glycosylation sites may be related to the unique sperm-egg recognition mechanism in gynogenesis.
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References
Wassarman PM . The biology and chemistry of fertilization. Science 1987; 235:553–560.
Foltz KF, Lennarz WJ . The molecular basis of sea urchin gamete interactions at the egg plasma membrane. Dev Biol 1993; 158:46–61.
Wassarman PM . Profile of a mammalian sperm receptor. Development 1990; 108:1–17.
Whitaker M . Lighting the fuse at fertilization. Development 1993; 117:112.
Barros C, Crosby JA, Moreno RD . Early steps of sperm-egg interactions during mammalian fertilization. Cell Biol Int Rev 1996; 20:33–9.
Snell WJ, White JM . The molecules of mammalian fertilization. Cell 1996; 85:629–37.
Vacquier VD . Evolution of gamete recognition proteins. Science 1998; 281:1995–8.
Wassarman PM . Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell 1999; 96:175–83.
Gui JF . A unique study system: gynogenetic fish Carassius auratus gibelio. Science Foundation in China 1996; 4:44–6.
Gui JF . Retrospect and prospects of studies on the mechanism of natural gynogenesis in silver crucian carp ( Carassius auratus gibelio). Bulletin of Natural National Science Foundation of China 1997; 11:11–6. (in Chinese)
Ge W, Jiang YG . A preliminary study on the mode in the egg of the naturally gynogenetic crucian carp for inhibiting heterologous sperm from transforming into male pronucleus. Acta Hydrobiologica Sinica 1985; 9:203–8. (in Chinese)
Ding J, Jiang YG, Shan SX, Wei LH . Roles of plasma membrane proteins of heterologous sperm in mediating primary control of gynogenetic silver crucian carp eggs. Chinese Science Bulletin 1993; 38: (in Chinese)
Fan LC, Gui JF, Ding J, Zhu LF, Liang SC, Yang ZA . Cytological mechanism on the integration of heterologous genoe or chromosomes in the unique gynogenetic Carassius auratus gibelio. Dev Reprod Biol 1997; 6:33–44.
Yamashita M, Onozato H, Nakanishi T, Nagahama Y . Breakdown of the sperm nuclear envelop is a prerequisite for male pronucleus formation: Direct evidence from the gynogenetic crucian carp Carassius auratus langsdorfii. Dev Biol 1990; 137:155–60.
Xie J, Zhu Y, Zhang F, Gui JF . Differential gene expression of protein kinases in oocytes between natural gynogenetic silver crucian carp and gonochoristic crucian carp. Chinese Science Bulletin 1999; 44: 1297–1301.
Yang ZA, Li QH, Wang YF, Gui JF . Comparative investigation on spindle behavior and MPF activity changes during oocyte maturation between gynogenetic and amphimictic crucian carp. Cell research 1999; 9:145–54.
Wang L, Brown DD . A gene expression screen. Proc Natl Acad Sci USA 1991; 88:11505–9.
Liang P, Pardee AB . Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 1992; 257:967–71.
Diatchenko L, Lau YC, Campbell AP, Chenchik A, Mooadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov E, Siebert PD . Suppression subtractive hybridization: A method for generating differentially regulated or tissue- specific cDNA probes. Proc Natl Acad Sci USA 1996; 93:6025–30.
Chu ZL, Mckinsey TA . Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kB control. Proc Natl Acad Sci USA 1997; 94:10057–62.
Davis CA, Benzer S . Generation of cDNA expression libraries enriched for in-frame sequences. Proc Natl Acad Sci USA 1997; 94:2128–32.
Wong BR, Rho J, Arron J, Robinson E, Orlinick J, Chao M, Kalachikov S, Cayani E, Barlett III FS, Frankel WN, Lee SY, Choi Y . TRANCE is a novel ligand of the tumor necrosis factor receptor family that activates c-Jun N-terminal kinase in T cells. J Biol Chem 1997; 272:25190–4.
Shimono A, Behringer RR . Isolation of novel cDNAs by subtractions between the anterior mesendoderm of single mouse gastrula atage embryos. Dev Biol 1999; 209:369–80.
Evans JD, Wheeler DE . Differential gene expression between developing queens and workers in the honey bee, Apis mellifera. Proc Natl Acad Sci USA 1999; 96:5575–80.
Gui JF . Fish developmental genetics and Artificial propagation. In: Fish Genetics and Breeding Engineering (edited by Wu C and Gui JF), Shanghai Scientific and Technical Publishers, Shanghai, 1999; pp41–62. (in Chinese).
Fan LC, Xie J, Wang Y, Gui JF . Construction of oocyte cDNA libraries of gynogenetic silver crucian carp and gonochoristic color crucian carp and cloning of their cyclin A1 cDNAs. Acta Hydrobiologica Sinica 2000; 24:573–81. (in Chinese).
Nielsen H, Engelbrecht J, Brunak S, Heijne GV . Identifition of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 1997; 10:1–6.
Kim KS, Febbraio M, Han TH . Analysis of gene expression by blotting techniques. In Gene Probes 2: A Practical Approach (eds. Hames BD, Higgins SJ.), New York, Oxford University Press, 1995; pp156–165.
Yurewicz E, Sacco A, Subramanian M . Structural characterization of the Mr=55,000 antigen (ZP3) of porcine oocyte zona pellucida. J Biol Chem 1987; 262:564–71.
Harris J, Hibler D, Fontenot G, Hsu K, Yurewicz E, Sacco A . Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: the ZPA, ZPB and ZPC gene families. DNA Seq 1994; 4:361–93.
Yang J, Hedrick J . cDNA cloning and sequence analysis of the Xenopus laevis egg envelope glycoprotein gp43. Dev Growth Differ 1997; 39:457–67.
Kozak M . Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 1986; 44:283–92.
Chang YS, Wang SC, Tsao CC, Huang FL . Molecular cloning, structural analysis, and expression of carp ZP3 gene. Mol Reprod Dev 1996; 44:295–304.
von Heijne G . A new method for predicting signal sequence cleavage site. Nucleic Acids Res 1986; 14:4683–90.
Hirokawa T, Boon-Chieng S, Mitaku S . SOSUI: Classification and Secondary Structure Prediction System for Membrane Proteins. Bioinformatics (formerly CABIOS) 1998; 14(4):378–9.
Hansen JE, Lund O, Rapacki K, Brunak S . O-glycbase version 2.0 – A revised database of O-glycosylated proteins. Nucleic Acids Res 1997; 25: 278–282.
Wang H, Gong Z . Characterization of two zebrafish cDNA clones encoding egg envelope proteins ZP2 and ZP3. Biochim Biophys Acta 1999; 1446:156–60.
Murata K, Sasaki T, Yasumasu S, Iuchi I, Enami J, Yasumasu I, Yamagimi K . Cloning of cDNAs for the precursor protein of a low-molecular-weight subunit of the inner layer of the egg envelope (chorion) of the fish Oryzias latipes. Dev Biol 1995; 167:9–17.
Waclawek M, Foisner R, Nimpf J, Schneider WJ . The chicken homologue of zona pellucida protein-3 is synthesized by granulosa cells. Biol Repro 1998; 59:1230–9.
Takeuchi Y, Nishimura K, Aoki N, Adachi T, Sato C, Kitajima K, Matsuda T . A 42-kDa glycoprotein from chicken egg-envelope, an avian homolog of the ZPC family glycoproteins in mammalian Zona pellucida. Its first identification, cDNA cloning and granulosa cell-specific expression. Eur J Biochem 1999; 260:736–42.
Ringuette MJ, Chamberlin ME, Baur AW, Sobieski DA, Dean J . Molecular analysis of cDNA coding for ZP3, a sperm binding protein of the mouse zona pellucida. Dev Biol 1988; 127:287–95.
Van-Duin M, Polman J, Verkoelen C, Bunschoten H, Meyerink J, Olijve W, Aitken R . Cloning and characterization of the human sperm receptor ligand ZP3: evidence for a second polymorphic allele with a different frequency in the Caucasian and Japanese populations. Genomics 1992; 14:1064–70.
Avise JC, Trexvis JC, Travis J, Nelson WS . Poecilia mexicana is the recent female parent of the unisexual fish Poecilia formosa. Evolution 1991; 45:1530–3.
Schartl M, Nanda I, Schlupp I, Wilde B, Epplen JT, Schmid M, Parzefall J . Incorporation of subgenomic amounts of host species DNA in the gynogenetic Amazon Molly. Nature 1995; 373:68–71.
Schlupp I, Nanda I, Dobler M, Lamatsch DK, Epplen JT, Parzefall J, Schmid M, Schartl M . Dispensable and indispensable genes in an ameiotic fish, the Amazon molly Poecilia formosa. Cytogenet Cell Genet 1998; 80:193–8.
Zhu L, Gui JF . Comparative studies on gene expression of isozymes in the 4 types of various ploidy crucian carp during embryogenesis. Acta Biologiae Experimentalis Sinica 1998; 31(4):369–76. (in Chinese)
Wassarman PM, Litscher ES . Sperm-egg recognition mechanisms in mammals. Curr Top Dev Biol 1995; 30:1–19.
Bleil JD, Wassarman PM . Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev Biol 1980; 76:180–202.
Kinloch RA, Sakai Y, Wassarman PM . Mapping the mouse ZP3 combing sites for sperm by exon swapping and site-directed mutagenesis. Proc Natl Acad Sci USA 1995; 92:263–7.
Litscher ES, Wassarman PM . Characterization of a mouse ZP3-derived glycopeptides, gp55, that exhibits sperm receptor and acrosome reaction-inducing activity in vitro. Biochemistry 1996; 35:3980–5.
Chen J, Litscher ES, Wassarman PM . Inactivation of the mouse sperm receptor, mZP3, by site-directed mutagenesis of individual serine residues located at the combining-site for sperm. Proc Natl Acad Sci USA 1998; 95:6193–7.
Kozak M . Comparation of initiation of protein synthesis in prokaryotes, eukaryotes, and organelles. Microbiol Res 1983; 47:1–45.
Philpott CC, Ringuette MJ, Dean J . Oocyte-specific expression and developmental regulation of ZP3, the sperm receptor of the mouse zona pellucida. Dev Biol 1987; 121:568–75.
Bleil JD, Wassarman PM . Galactose at the nonreducing terminus of O-linked oligosaccharides of mouse egg zona pellucida glycoprotein ZP3 is essential for the glycoprotein's sperm receptor activity. Proc Natl Acad Sci USA 1988; 85:6778–82.
Schmizu S, Tsuji M, Dean J . In vitro biosynthesis of three sulfated glycoproteins of murine zonae pellucidae by oocytes grown in follicle culture. J Biol Chem 1983; 258:5858–63.
Acknowledgements
These studies were supported by the National Natural Science Foundation of China (Grants No. 39700070 and 30070379), the Chinese Academy of Sciences (Grant No. KJ951-B1-607-03), and the Major State Basic Research Program (No. G1999053908) of China.
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FAN, L., YANG, S. & GUI, J. Differential screening and characterization analysis of the egg envelope glycoprotein ZP3 cDNAs between gynogenetic and gonochoristic crucian carp. Cell Res 11, 17–27 (2001). https://doi.org/10.1038/sj.cr.7290062
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DOI: https://doi.org/10.1038/sj.cr.7290062
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