Rabbit zona pellucida composition: A molecular, proteomic and phylogenetic approach

Journal of Proteomics

Volumn 75, Issue 18, 2012, Pages 5920-5935

  Stetson, I ^a,b   Izquierdo Rico, M J ^a   Moros, C ^a   Chevret, P ^c   Lorenzo, P L ^d   Ballesta, J ^a   Rebollar, P G ^f   Gutierrez Gallego R ^e   Aviles M ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b UNIVERSIDAD NACIONAL DE MISIONES   (Argentina)

^c UNIVERSITÉ LYON 1   (France)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^e UNIVERSITAT POMPEU FABRA   (Spain)

^f UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

Author keywords

Fertilization; Oocyte; Rabbit; Sperm egg interaction; Zona pellucida

Indexed keywords

COMPLEMENTARY DNA; GLYCOPROTEIN; MESSENGER RNA;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; FEMALE; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; RABBIT; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; ZONA PELLUCIDA;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EGG PROTEINS; FEMALE; GLYCOPROTEINS; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEOMICS; PSEUDOGENES; RABBITS; RECEPTORS, CELL SURFACE; SEQUENCE ALIGNMENT; TANDEM MASS SPECTROMETRY; ZONA PELLUCIDA;

EQUIDAE; MAMMALIA; ORYCTOLAGUS CUNICULUS; RATTUS; SUIDAE;

EID: 84866546249     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.07.027     Document Type: Article

References (67)

1. Yanagimachi R. Mammalian fertilization. Physiology of reproduction 1994, 189-317. Raven Press, New York. E. Knobil, J.D. Neill (Eds.).
2. Dean J. The enigma of sperm-egg recognition in mice. Soc Reprod Fertil Suppl 2007, 63:359-365.
3. Wassarman P.M., Litscher E.S. The multifunctional zona pellucida and mammalian fertilization. J Reprod Immunol 2009, 83:45-49.
4. Goudet G., Mugnier S., Callebaut I., Monget P. Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol Reprod 2008, 78:796-806.
5. Bausek N., Waclawek M., Wolfgang J.S., Wohlrab F. The major chicken egg envelope protein ZP1 is different from ZPB and is synthesized in the liver. J Biol Chem 2000, 275:28866-28872.
6. Spargo S.C., Hope R.M. Evolution and nomenclature of zona pellucida gene family. Biol Reprod 2003, 68:358-362.
7. Bleil J.D., Wassarman P.M. Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev Biol 1980, 76:185-202.
8. Hedrick J.L., Wardrip N.J. On the macromolecular of the zona pellucida from porcine oocytes. Dev Biol 1987, 121:478-488.
9. Noguchi S., Yonezawa N., Katsumata T., Hashizume K., Kuwayama M., Hamano S., et al. Characterization of the zona pellucida glycoproteins from bovine ovarian and fertilized eggs. Biochim Biophys Acta 1994, 1201:7-14.
10. Hughes D.C., Barratt C.L. Identification of the true human orthologue of the mouse Zp1 gene: evidence for greater complexity in the mammalian zona pellucida. Biochim Biophys Acta 1999, 1447:303-306.
11. Lefièvre L., Conner S.J., Salpekar A., Olufowobi O., Ashton P., Pavlovic B., et al. Four zona pellucida glycoproteins are expressed in the human. Hum Reprod 2004, 19:580-586.
12. Hoodbhoy T., Joshi S., Boja E.S., Williams S.A., Stanley P., Dean J. Human sperm do not bind to rat zonae pellucidae despite the presence of four homologous glycoproteins. J Biol Chem 2005, 280:12721-12731.
13. Izquierdo-Rico M.J., Jiménez-Movilla M., Llop E., Pérez-Oliva A.B., Ballesta J., Gutierrez-Gallego R., et al. Hamster zona pellucida is formed by four glycoproteins. J Proteome Res 2009, 8:926-941.
14. Jiménez-Movilla M., Martínez-Alonso E., Castells M.T., Izquierdo-Rico M.J., Saavedra M.D., Gutiérrez-Gallego R., et al. Cytochemical and biochemical evidences for a complex tridimensional structure of the hamster zona pellucida. Histol Histopathol 2009, 24:599-609.
15. Dunbar B.S., Timmons T.M., Skinner S.M., Prasad S.V. Molecular analysis of a carbohydrate antigen involved in the structure and function of zona pellucida glycoproteins. Biol Reprod 2001, 65:951-960.
16. Easton R.L., Patankar M.S., Lattanzio F.A., Leaven T.H., Morris H.R., Clark G.F., et al. Structural analysis of murine zona pellucida glycans. Evidence for the expression of core 2-type O-glycans and the Sd(a) antigen. J Biol Chem 2000, 275:7731-7742.
17. von Witzendorff D., Ekhlasi-Hundrieser M., Dostalova Z., Resch M., Rath D., Michelmann H.W., et al. Analysis of N-linked glycans of porcine zona pellucida glycoprotein ZPA by MALDI-TOF MS: a contribution to understanding zona pellucida structure. Glycobiology 2005, 15:475-488.
18. von Witzendorff D., Maass K., Pich A., Ebeling S., Kölle S., Kochel C., et al. Characterization of the acidic N-linked glycans of the zona pellucida of prepuberal pigs by a mass spectrometric approach. Carbohydr Res 2009, 344:1541-1549.
19. Lee V.H., Schwoebel E., Prasad S., Cheung P., Timmons T.M., Cook R., et al. Identification and structural characterization of the 75-kDa rabbit zona pellucida protein. J Biol Chem 1993, 268:12412-12417.
20. Schwoebel E.D., Vandevoort C.A., Lee V.H., Lo Y.K., Dunbar B.S. Molecular analysis of the antigenicity and immunogenicity of recombinant zona pellucida antigens in a primate model. Biol Reprod 1992, 47:857-865.
21. Harris J.D., Hibler D.W., Fontenot G.K., Hsu K.T., Yurewicz E.C., Sacco A.G. 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, 4:361-393.
22. Prasad S.V., Mujtaba S., Lee V.H., Dunbar B.S. Immunogenicity enhancement of recombinant rabbit 55-kilodalton zona pellucida protein expressed using the baculovirus expression system. Biol Reprod 1995, 52:1167-1178.
23. Lee V.H. Expression of rabbit zona pellucida-1 messenger ribonucleic acid during early follicular development. Biol Reprod 2000, 63:401-408.
24. Schwoebel E., Prasad S., Timmons T.M., Cook R., Kimura H., Niu E.M., et al. Isolation and characterization of a full-length cDNA encoding the 55-kDa rabbit zona pellucida protein. J Biol Chem 1991, 266:7214-7219.
25. Arias-Álvarez M., García-García R.M., Torres-Rovira L., González-Bulnes A., Rebollar P.G., Lorenzo P.L. Influence of leptin on in vitro maturation and steroidogenic secretion of cumulus-oocyte complexes through JAK2/STAT3 and MEK 1/2 pathways in the rabbit model. Reproduction 2010, 139:523-532.
26. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic Local Alignment Search Tool. J Mol Biol 1990, 215:403-410.
27. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 1997, 10:1-6.
28. Hansen J.E., Lund O., Tolstrup N., Gooley A.A., Williams K.L., Brunak S. NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconj J 1998, 15:115-130.
29. Gupta R., Brunak S. Prediction of glycosilation across the human proteome and the correlation to protein function. Pac Symp Biocomput 2002, 310-322.
30. Gouy M., Guindon S., Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010, 27:221-224.
31. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
32. Posada D., Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
33. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795.
34. Ducker P., Brunak S., Blom N. Prediction of proprotein convertase cleavage sites. Protein Eng Des Sel 2004, 17:107-112.
35. Boja E.S., Hoodbhoy T., Fales H.M., Dean J. Structural characterization of native mouse zona pellucida proteins using mass spectrometry. J Biol Chem 2003, 278:34189-34202.
36. Boja E.S., Hoodbhoy T., Garfield M., Fales H.M. Structural conservation of mouse and rat zona pellucida glycoproteins. Probing the native rat zona pellucida proteome by mass spectrometry. Biochemistry 2005, 44:16445-16460.
37. Epifano O., Liang L.F., Familiari M., Moos M.C., Dean J. Coordinate expression of the three zona pellucida genes during mouse oogenesis. Development 1995, 121:1947-1956.
38. Zhao M., Boja E.S., Hoodbhoy T., Nawrocki J., Kaufman J.B., Kresge N., et al. Mass spectrometry analysis of recombinant human ZP3 expressed in glycosylation-deficient CHO cells. Biochemistry 2004, 43:12090-12104.
39. Chakravarty S., Kadunganattil S., Bansal P., Sharma R.K., Gupta S.K. Relevance of glycosylation of human zona pellucida glycoproteins for their binding to capacitated human spermatozoa and subsequent induction of acrosomal exocytosis. Mol Reprod Dev 2008, 75:75-88.
40. Visconti P.E., Florman H.M. Mechanisms of sperm-egg interactions: between sugars and broken bonds. Sci Signal 2010, 3:35.
41. Clark G.F. Molecular models for mouse sperm-oocyte binding. Glycobiology 2011, 21:3-5.
42. Gahlay G., Gauthier L., Baibakov B., Epifano O., Dean J. Gamete recognition in mice depends on the cleavage status of an egg's zona pellucida protein. Science 2010, 329:216-219.
43. Lee V.H., Dunbar B.S. Developmental expression of the rabbit 55-kDa zona pellucida protein and messenger RNA in ovarian follicles. Dev Biol 1993, 155:371-382.
44. Dunbar B.S., Avery S., Lee V., Prasad S., Schwahn D., Schwoebel E., et al. The mammalian zona pellucida: its biochemistry, immunochemistry, molecular biology, and developmental expression. Reprod Fertil Dev 1994, 6:331-347.
45. Hinsch K.D., Hinsch E., Meinecke B., Töpfer-Petersen E., Pfisterer S., Schill W.B. Identification of mouse ZP3 protein in mammalian oocytes with antisera against synthetic ZP3 peptides. Biol Reprod 1994, 51:193-204.
46. Grootenhuis A.J., Philipsen H.L., de Breet-Grijsbach J.T., van Duin M. Immunocytochemical localization of ZP3 in primordial follicles of rabbit, marmoset, rhesus monkey and human ovaries using antibodies against human ZP3. J Reprod Fertil Suppl 1996, 50:43-54.
47. Martínez M.L., Fontenot G.K., Harris J.D. The expression and localization of zona pellucida glycoproteins and mRNA in cynomolgus monkeys (Macaca fascicularis). J Reprod Fertil Suppl 1996, 50:35-41.
48. Gook D.A., Edgar D.H., Borg J., Martic M. Detection of zona pellucida proteins during human folliculogenesis. Hum Reprod 2008, 23:394-402.
49. Bleil J.D., Wassarman P.M. Synthesis of zona pellucida proteins by denuded and follicle-enclosed mouse oocytes during culture in vitro. Proc Natl Acad Sci U S A 1980, 77:1029-1033.
50. Fléchon J.E., Pavlok A., Kopecný V. Dynamics of zona pellucida formation by the mouse oocyte. An autoradiographic study. Biol Cell 1984, 51:403-406.
51. Sinowatz F., Kölle S., Töpfer-Petersen E. Biosynthesis and expression of zona pellucida glycoproteins in mammals. Cells Tissues Organs 2001, 168:24-35.
52. El Mestrah M., Castle P.E., Borrosa G., Kan F.W. Subcellular distribution of ZP1, ZP2, and ZP3 glycoproteins during folliculogenesis and demonstration of their topographical disposition within the zona matrix of mouse ovarian oocytes. Biol Reprod 2002, 66:866-876.
53. Scobie G.A., Kerr L.E., MacDuff P., Aitken R.J. Cloning, sequencing and site of origin of the rat sperm receptor protein, ZP3. Zygote 1999, 7:27-35.
54. Izquierdo-Rico M.J., Gimeno L., Jiménez-Cervantes C., Ballesta J., Avilés M. Biosynthesis of hamster zona pellucida is restricted to the oocyte. Theriogenology 2011, 75:463-472.
55. Conner S.J., Hughes D.C. Analysis of fish ZP1/ZPB homologous genes-evidence for both genome duplication and species-specific amplification models of evolution. Reproduction 2003, 126:347-352.
56. Gupta S.K., Bhandari B. Acrosome reaction: relevance of zona pellucida glycoproteins. Asian J Androl 2011, 13:97-105.
57. Wassarman P.M. Zona pellucida glycoproteins. Annu Rev Biochem 1988, 57:415-442.
58. Rankin T., Talbot P., Lee E., Dean J. Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development 1999, 126:3847-3855.
59. Ganguly A., Bukovsky A., Sharma R.K., Bansal P., Bhandari B., Gupta S.K. In humans, zona pellucida glycoprotein-1 binds to spermatozoa and induces acrosomal exocytosis. Hum Reprod 2010, 25:1643-1656.
60. Ganguly A., Bansal P., Gupta T., Gupta S.K. 'ZP domain' of human zona pellucida glycoprotein-1 binds to human spermatozoa and induces acrosomal exocytosis. Reprod Biol Endocrinol 2010, 8:110. [11].
61. Topper E.K., Kruijt L., Calvete J., Mann K., Töpfer-Petersen E., Woelders H. Identification of bovine zona pellucida glycoproteins. Mol Reprod Dev 1997, 46:344-350.
62. Govind C.K., Hasegawa A., Koyama K., Gupta S.K. Delineation of a conserved B cell epitope on bonnet monkey (Macaca radiata) and human zona pellucida glycoprotein-B by monoclonal antibodies demonstrating inhibition of sperm-egg binding. Biol Reprod 2000, 62:67-75.
63. Chakravarty S., Suraj K., Gupta S.K. Baculovirus-expressed recombinant human zona pellucida glycoprotein-B induces acrosomal exocytosis in capacitated spermatozoa in addition to zona pellucida glycoprotein-C. Mol Hum Reprod 2005, 11:365-372.
64. Prasad S.V., Wilkins B., Skinner S.M., Dunbar B.S. Evaluating zona pellucida structure and function using antibodies to rabbit 55kDa ZP protein expressed in baculovirus expression system. Mol Reprod Dev 1996, 43:519-529.
65. Chiu P.C., Wong B.S., Chung M.K., Lam K.K., Pang R.T., Lee K.F., et al. Effects of native human zona pellucida glycoproteins 3 and 4 on acrosome reaction and zona pellucida binding of human spermatozoa. Biol Reprod 2008, 79:869-877.
66. Yurewicz E.C., Sacco A.G., Gupta S.K., Xu N., Gage D.A. Hetero-oligomerization-dependent binding of pig oocyte zona pellucida glycoproteins ZPB and ZPC to boar sperm membrane vesicles. J Biol Chem 1998, 273:7488-7494.
67. Kanai S., Yonezawa N., Ishii Y., Tanakura M., Nakano M. Recombinant bovine zona pellucida glycoproteins ZP3 and ZP4 coexpressed in Sf9 cells form a sperm-binding active hetero-complex. FEBS J 2007, 274:5390-5405.