In humans, zona pellucida glycoprotein-1 binds to spermatozoa and induces acrosomal exocytosis

Human Reproduction

Volumn 25, Issue 7, 2010, Pages 1643-1656

  Ganguly, Anasua ^a   Bukovsky, Antonin ^b   Sharma, Raj K ^c   Bansal, Pankaj ^a   Bhandari, Beena ^a   Gupta, Satish K ^a  

^a NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

^b UNIVERSITY OF TENNESSEE GRADUATE SCHOOL OF MEDICINE   (United States)

^c ARMY HOSPITAL   (India)

Author keywords

acrosome reaction; fertilization; monoclonal antibodies; sperm binding; zona pellucida

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; FETUIN; FLUORESCEIN ISOTHIOCYANATE; G PROTEIN COUPLED RECEPTOR; GLYCOPROTEIN; LECTIN; MONOCLONAL ANTIBODY; PROTEIN KINASE C; UNCLASSIFIED DRUG; ZONA PELLUCIDA GLYCOPROTEIN 1; ZONA PELLUCIDA GLYCOPROTEIN 2; ZONA PELLUCIDA GLYCOPROTEIN 3; ZONA PELLUCIDA GLYCOPROTEIN 4;

ACROSOME; ARTICLE; BACULOVIRUS; ENDOMETRIUM; ESCHERICHIA COLI; EXOCYTOSIS; FERTILIZATION; GLYCOSYLATION; HUMAN; HUMAN CELL; KIDNEY; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; OOCYTE; OVARY FOLLICLE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPERMATOZOON; UTERINE TUBE; ZONA PELLUCIDA;

ESCHERICHIA COLI;

EID: 77955907224     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deq105     Document Type: Article

References (57)

1. Baldi E, Luconi M, Bonaccorsi L, Krausz C, Forti G. Human sperm activation during capacitation and acrosome reaction: role of calcium, protein phosphorylation and lipid remodelling pathways. Front Biosci 1996;1:189-205.
2. Baldi E, Luconi M, Bonaccorsi L, Forti G. Signal transduction pathways in human spermatozoa. J Reprod Immunol 2002;53:121-131.
3. Bansal P, Chakrabarti K, Gupta SK. Functional activity of human ZP3-primary sperm receptor resides towards its C-terminus. Biol Reprod 2009;81:7-15.
4. Bausek N, Waclawek M, Schneider WJ, 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.
5. Beebe SJ, Leyton L, Burks D, Ishikawa M, Fuerst T, Dean J, Saling P. Recombinant mouse ZP3 inhibits sperm binding and induces the acrosome reaction. Dev Biol 1992;151:48-54.
6. Bhandari B, Bansal P, Talwar P, Gupta SK. Delineation of downstream signalling components during acrosome reaction mediated by heat solubilized human zona pellucida. Reprod Biol Endocrinol 2010;8:7.
7. Biggers JD, Whitten WK, Whittingham DG. The culture of mouse embryos in vitro. In: Daniel JC Jr (ed). Methods in Mammalian Embryology. San Francisco, USA: WH Freeman and Co, 1971. 86-116.
8. Björndahl L, Söderlund I, Kvist U. Evaluation of the one-step eosin-nigrosin staining technique for human sperm vitality assessment. Hum Reprod 2003;18:813-816.
9. 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 1980a;76:185-202.
10. Bleil JD, Wassarman PM. Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 1980b;20:873-882.
11. Bleil JD, Greve JM, Wassarman PM. Identification of a secondary sperm receptor in the mouse egg zona pellucida: role in maintenance of binding of acrosome-reacted sperm to eggs. Dev Biol 1988;128:376-385.
12. 2 channel in the acrosome reaction initiated by recombinant ZP3. Biol Reprod 2002;66:91-97.
13. Breitbart H. Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Mol Cell Endocrinol 2002;187:139-144.
14. Bukovsky A, Keenan JA, Caudle MR, Wimalasena J, Upadhyaya NB, Van Meter SE. Immunohistochemical studies of the adult human ovary: possible contribution of immune and epithelial factors to folliculogenesis. Am J Reprod Immunol 1995;33:323-340.
15. Bukovsky A, Gupta SK, Bansal P, Chakravarty S, Chaudhary M, Svetlikova M, White RS, Copas P, Upadhyaya NB, Van Meter SE et al. Production of monoclonal antibodies against recombinant human zona pellucida glycoproteins: utility in immunolocalization of respective zona proteins in ovarian follicles. J Reprod Immunol 2008;78:102-114.
16. Caballero-Campo P, Chirinos M, Fan XJ, González-González ME, Galicia-Chavarŕa M, Larrea F, Gerton GL. Biological effects of recombinant human zona pellucida proteins on sperm function. Biol Reprod 2006;74:760-768.
17. Castle PE. Could multiple low-affinity bonds mediate primary sperm-zona pellucida binding? Reproduction 2002;124:29-32.
18. Chakravarty S, Kadunganattil S, Gupta SK. 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.
19. Chakravarty S, Kadunganattil S, Bansal P, Sharma RK, Gupta SK. 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.
20. Chiu PC, Wong BS, Lee CL, Pang RT, Lee KF, Sumitro SB, Gupta SK, Yeung WS. Native human zona pellucida glycoproteins: purification and binding properties. Hum Reprod 2008a;23:1385-1393.
21. Chiu PC, Wong BS, Chung MK, Lam KKW, Pang RT, Lee KF, Sumitro SB, Gupta SK, Yeung WS. Effects of native human zona pellucida glycoprotein-3 and-4 on acrosome reaction and zona pellucida binding of human spermatozoa. Biol Reprod 2008;79:869-877.
22. Clark GF, Dell A. Molecular models for murine sperm-egg binding. J Biol Chem 2006;281:13853-13856.
23. Conner SJ, Lefievre L, Hughes DC, Barratt CL. Cracking the egg: increased complexity in the human zona pellucida. Hum Reprod 2005; 5:1148-1152.
24. Cornwall GA, Tulsiani DR, Orgebin-Crist MC. Inhibition of the mouse sperm surface alpha-D-mannosidase inhibits sperm-egg binding in vitro. Biol Reprod 1991;44:913-921.
25. De Jonge C, Han HL, Lawrie H, Mack SR, Zaneveld LJD. Modulation of the human sperm acrosome reaction by effector of adenylate cyclase/cyclic AMP second messenger pathway. J Exp Zool 1991a;258:113-125.
26. De Jonge C, Han HL, Mack SR, Zaneveld JD. Effect of phorboldiesters synthetic diacylglycerols and a protein kinase C inhibitor on the human sperm acrosome reaction. J Androl 1991b;12:62-70.
27. Doherty CM, Tarchala SM, Radwanska E, De Jonge CJ. Characterization of two second messenger pathways and their interactions in eliciting the human sperm acrosome reaction. J Androl 1995;16:36-46.
28. El-Mestrah M, Castle PE, Borossa G, Kan FW. 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.
29. Familiari G, Relucenti M, Heyn R, Micara G, Correr S. Three-dimensional structure of the zona pellucida at ovulation. Microsc Res Tech 2006; 69:415-426.
30. Furlong LI, Harris JD, Vazquez-Levin MH. Binding of recombinant human proacrosin/acrosin to zona pellucida (ZP) glycoproteins. Studies with recombinant human ZPA, ZPB, and ZPC. Fertil Steril 2005; 83:1780-1790.
31. Gahlay GK, Gupta SK. Glycosylation of zona pellucida glycoprotein-3 is required for inducing acrosomal exocytosis in the bonnet monkey. Cell Mol Biol (Noisy-le-grand) 2003;49:389-397.
32. Gahlay GK, Srivastava N, Govind CK, Gupta SK. Primate recombinant zona pellucida proteins expressed in Escherichia coli bind to spermatozoa. J Reprod Immunol 2002;53:67-77.
33. Ganguly A, Sharma RK, Gupta SK. Bonnet Monkey (Macaca radiata) ovaries, like human oocytes, express four zona pellucida glycoproteins. Mol Reprod Dev 2008;75:156-166.
34. 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.
35. Govind CK, Hasegawa A, Koyama K, Gupta SK. Delineation of conserved B cell epitope on bonnet monkey (Macaca radiata) and human zona pellucida glycoprotein-B by monoclonal antibodies demonstrated inhibition of sperm-egg binding. Biol Reprod 2000;62:67-75.
36. Govind CK, Gahlay GK, Choudhury S, Gupta SK. Purified and refolded recombinant bonnet monkey (Macaca radiata) zona pellucida glycoprotein-B expressed in Escherichia coli binds to spermatozoa. Biol Reprod 2001;64:1147-1152.
37. Greve JM, Wassarman PM. Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. J Mol Biol 1985;181:253-264.
38. Grootenhuis AJ, Philipsen HL, de Breet-Grijsbach JT, 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 1996;50:43-54.
39. Hoodbhoy T, Avilés M, Baibakov B, Epifano O, Jiménez- Movilla M, Gauthier L, Dean J. ZP2 and ZP3 traffic independently within oocytes prior to assembly into the extra cellular zona pellucida. Mol Cell Biol 2006;26:7991-7998.
40. Hughes DC, Barratt CL. 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.
41. Jimenez-Movilla M, Aviles M, Gomez-Torres MJ, Fernandez-Colom PJ, Castells MT, de Juan J, Romeu A, Ballesta J. Carbohydrate analysis of the zona pellucida and cortical granules of human oocytes by means of ultrastructural cytochemistry. Hum Reprod 2004;19:1842-1855.
42. Kaul R, Afzalpurkar A, Gupta SK. Expression of bonnet monkey (Macaca radiata) zona pellucida-3 (ZP3) in a prokaryotic system and its immunogenicity. Mol Reprod Dev 1997;47:140-147.
43. Lefievre L, Conner SJ, Salpekar A, Olufowobi O, Ashton P, Pavlovic B, Lenton W, Afnan M, Brewis IA, Monk M et al. Four zona pellucida glycoproteins are expressed in the human. Hum Reprod 2004; 19:1580-1586.
44. McLeskey SB, Dowds C, Carballada R, White RR, Saling PM. Molecules involved in mammalian sperm-egg interaction. Int Rev Cytol 1998;177:57-113.
45. Melendrez CS, Meizel S. Studies of porcine and human sperm suggesting a role for a sperm glycine receptor/chloride channel in the zona pellucida initiated acrosome reaction. Biol Reprod 1995;53:676-683.
46. Mori K, Daitoh T, Irahara M, Kamada M, Aono T. Significance of D-mannose as a sperm receptor site on the zona pellucida in human fertilization. Am J Obstet Gynecol 1989;161:207-211.
47. Okumura H, Kohno Y, Iwata Y, Mori H, Aoki N, Sato C, Kitajima K, Nadano D, Matsuda T. A newly identified zona pellucida glycoprotein, ZPD, and dimeric ZP1 of chicken egg envelope are involved in sperm activation on sperm-egg interaction. Biochem J 2004;384:191-199.
48. Prasad SV, Wilkins B, Skinner SM, Dunbar BS. Evaluating zona pellucida structure and function using antibodies to rabbit 55 kDa ZP protein expressed in baculovirus expression system. Mol Reprod Dev 1996; 43:519-529.
49. 2+-independent induction of acrosome reaction by protein kinase C in human sperm. Endocrinology 1992;131:2235-2243.
50. Sasanami T, Murata T, Ohtsuki M, Matsushima K, Hiyama G, Kansaku N, Mori M. Induction of sperm acrosome reaction by perivitelline membrane glycoprotein ZP1 in Japanese quail (Coturnix japonica). Reproduction 2007;133:41-49.
51. i protein and extracellular calcium, and priming effect of progesterone and follicular fluid. Mol Hum Reprod 2002;8:722-727.
52. Swanson WJ, Vacquier VD. The rapid evolution of reproductive proteins. Nat Rev Genet 2002;3:137-144.
53. Vo LH, Hedrick JL. Independent and hetero-oligomeric-dependent sperm binding to egg envelope glycoprotein ZPC in Xenopus laevis. Biol Reprod 2000;62:766-774.
54. Wassarman PM, Litscher ES. Mammalian fertilization: the egg's multifunctional zona pellucida. Int J Dev Biol 2008;52:665-676.
55. World Health Organization 1922. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction. 3rd edn. Cambridge: Cambridge University Press.
56. World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction. 3rd edn. Cambridge: Cambridge University Press, 1992. Youssef HM, Doncel GF, Bassiouni BA, Acosta AA. Mannose binding sites on human spermatozoa and sperm morphology. Fertil Steril 1996; 66:640-645.
57. Yurewicz EC, Sacco AG, Gupta SK, Xu N, Gage DA. 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.