Lewis X-containing glycans are specific and potent competitive inhibitors of the binding of ZP3 to complementary sites on capacitated, acrosome-intact mouse sperm

Biology of Reproduction

Volumn 71, Issue 3, 2004, Pages 770-777

  Kerr, Candace L ^a   Hanna, William F ^a   Shaper, Joel H ^b   Wright, William W ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Fertilization; Gamete biology; Sperm

Indexed keywords

FLUOROCHROME; GLYCAN DERIVATIVE; GLYCOPROTEIN; LEWIS X ANTIGEN; NEOGLYCOPROTEIN; PROTEIN ZP3; UNCLASSIFIED DRUG;

ACROSOME; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DOSE RESPONSE; FERTILIZATION; FLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SPERMATOZOON CAPACITATION; ZONA PELLUCIDA;

ACROSOME; ANIMALS; BINDING, COMPETITIVE; CARBOHYDRATE SEQUENCE; CELL MEMBRANE; EGG PROTEINS; FEMALE; FUCOSE; GALACTOSE; GLYCOPROTEINS; LACTOSE; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED ICR; MOLECULAR SEQUENCE DATA; N-ACETYLNEURAMINIC ACID; POLYSACCHARIDES; RECEPTORS, CELL SURFACE; SERUM ALBUMIN, BOVINE; SPERM CAPACITATION; TRISACCHARIDES;

ALEXA; ANIMALIA; MAMMALIA;

EID: 4243068580     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.103.023812     Document Type: Article

References (30)

1. Wassarman PM. Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell 1999; 96:175-183.
2. Yanagimachi R. Mammalian fertilization. In: Neill JD (ed.), The Physiology of Reproduction, vol. 1, 2nd ed. New York: Raven Press; 1994: 189-317.
3. Kim KS, Cha MC, Gerton GL. Mouse sperm protein sp56 is a component of the acrosomal matrix. Biol Reprod 2001; 64:36-43.
4. Cohen N, Wassarman PM. Association of egg zona pellucida glycoprotein mZP3 with sperm protein sp56 during fertilization in mice. Int J Dev Biol 2001; 45:569-576.
5. 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.
6. Kerr CL, Hanna WF, Shaper JH, Wright WW. Characterization of zona pellucida glycoprotein 3 (ZP3) and ZP2 binding sites on acrosome-intact mouse sperm. Biol Reprod 2002; 66:1585-1595.
7. Evans JP, Florman HM. The state of the union: the cell biology of fertilization. Nat Cell Biol 2002; 4(suppl):S57-S63.
8. Florman HM, Wassarman PM. O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell 1985; 41:313-324.
9. 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 U S A 1998; 95:6193-6197.
10. Johnston DS, Wright WW, Shaper JH, Hokke CH, Van den Eijnden DH, Joziasse DH. Murine sperm-zona binding, a fucosyl residue is required for a high affinity sperm-binding ligand. A second site on sperm binds a nonfucosylated, beta-galactosyl-capped oligosaccharide. J Biol Chem 1998; 273:1888-1895.
11. 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 U S A 1988; 85:6778-6782.
12. Nixon B, Lu Q, Wassler MJ, Foote CI, Ensslin MA, Shur BD. Galactosyltransferase function during mammalian fertilization. Cells Tissues Organs 2001; 168:46-57.
13. Cornwall GA, Tulsiani DR, Orgebin-Crist MC. Inhibition of the mouse sperm surface α-D-mannosidase inhibits sperm-egg binding in vitro. Biol Reprod 1991; 44:913-921.
14. Litscher ES, Juntunen K, Seppo A, Penttila L, Niemela R, Renkonen O, Wassarman PM. Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro. Biochemistry 1995; 34:4662-4669.
15. a antigen. J Biol Chem 2000; 275:7731-7742.
16. 2+ release. J Biochem (Tokyo) 1997; 122:498-505.
17. Hanna WF, Kerr CL, Shaper JH, Wright WW. Lewis X-containing neoglycoproteins mimic the intrinsic ability of zona pellucida glycoprotein ZP3 to induce the acrosome reaction in capacitated mouse sperm. Biol Reprod 2004; 71:778-789.
18. Bertozzi CR, Fukuda S, Rosen SD. Sulfated disaccharide inhibitors of L-selectin: deriving structural leads from a physiological selectin ligand. Biochemistry 1995; 34:14271-14278.
19. Koenig A, Jain R, Vig R, Norgard-Sumnicht KE, Matta KL, Varki A. Selectin inhibition: synthesis and evaluation of novel sialylated, sulfated and fucosylated oligosaccharides, including the major capping group of GlyCAM-1. Glycobiology 1997; 7:79-93.
20. Leteux C, Chai W, Loveless RW, Yuen CT, Uhlin-Hansen L, Combamous Y, Jankovic M, Maric SC, Misulovin Z, Nussenzweig MC, Ten F. The cysteine-rich domain of the macrophage mannose receptor is a multispecific lectin that recognizes chondroitin sulfates A and B and sulfated oligosaccharides of blood group Lewis(a) and Lewis(x) types in addition to the sulfated N-glycans of lutropin. J Exp Med 2000; 191:1117-1126.
21. Lee RT, Lee YC. Affinity enhancement by multivalent lectin-carbohydrate interaction. Glycoconj J 2000; 17:543-551.
22. Miller KE, Mukhopadhyay C, Cagas P, Bush CA. Solution structure of the Lewis x oligosaccharide determined by NMR spectroscopy and molecular dynamics simulations. Biochemistry 1992; 31:6703-6709.
23. Azurmendi HF, Martin-Pastor M, Bush CA. Conformational studies of Lewis X and Lewis A trisaccharides using NMR residual dipolar couplings. Biopolymers 2002; 63:89-98.
24. Ichikawa Y, Lin Y-C, Dumas DP, Shen G-J, Garcia-Junceda E, Williams MA, Bayer R, Ketcham C, Walker LE, Paulson JC, Wong CH. Chemical-enzymatic synthesis and conformational analysis of sialyl lewis x and derivatives. J Am Chem Soc 1992; 114:9283-9298.
25. Tyrrell D, James P, Rao N, Foxall C, Abbas S, Dasgupta F, Nashed M, Hasegawa A, Kiso M, Asa D, et al. Structural requirements for the carbohydrate ligand of E-selectin. Proc Natl Acad Sci U S A 1991; 88:10372-10376.
26. Alon R, Feigelson S. From rolling to arrest on blood vessels: leukocyte tap dancing on endothelial integrin ligands and chemokines at sub-second contacts. Semin Immunol 2002; 14:93-104.
27. Galustian C, Childs RA, Stoll M, Ishida H, Kiso M, Feizi T Synergistic interactions of the two classes of ligand, sialyl-Lewis(a/x) fucooligosaccharides and short sulpho-motifs, with the P- and L-selectins: implications for therapeutic inhibitor designs. Immunology 2002; 105: 350-359.
28. Somers WS, Tang J, Shaw GD, Camphausen RT. Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLe(X) and PSGL-1. Cell 2000; 103:467-479.
29. Fukuda M, Hiraoka N, Yeh JC. C-type lectins and sialyl Lewis X oligosaccharides. Versatile roles in cell-cell interaction. J Cell Biol 1999; 147:467-470.
30. Leyton L, Saling P. Evidence that aggregation of mouse sperm receptors by ZP3 triggers the acrosome reaction. J Cell Biol 1989; 108: 2163-2168.