Binding of sperm proacrosin/β-acrosin to zona pellucida glycoproteins is sulfate and stereodependent. Synthesis of a novel fertilization inhibitor

Developmental Biology

Volumn 306, Issue 2, 2007, Pages 646-657

  Gaboriau, David ^a   Howes, Elizabeth A ^a   Clark, Jonathan ^b   Jones, Roy ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b Babraham Hall   (United Kingdom)

Author keywords

Fertilization; Moonlighting proteins; Proacrosin; Sulfation code; Suramin mimetics; Zona pellucida

Indexed keywords

BETA ACROSIN; GLYCOPROTEIN; PROACROSIN; QUERCETRIN; QUERCETRIN 3BETA DEXTRO GLUCOSIDE SULFATE; SURAMIN; UNCLASSIFIED DRUG;

ACROSOME; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FERTILIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; SPERMATOZOON; STEREOSPECIFICITY; SULFATION; ZONA PELLUCIDA;

ANIMALIA; MAMMALIA;

EID: 34249894223     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.04.001     Document Type: Article

References (61)

1. Bi M., Wassler M.J., and Hardy D.M. Sperm adhesion to the extracellular matrix of the egg. In: Hardy D.M. (Ed). Fertilization (2002), Academic Press, San Diego, CA 153-180
2. Bleil J.D., and Wassarmann P.M. Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20 (1980) 873-882
3. Bou Khalil M., Chakrabandhu K., Xu H., Weerachatyanukul W., Buhr M., Berger T., Carmona E., Vuong N., Kumarathasan P., Wong P.T., Carrier D., and Tanphaichitr N. Sperm capacitation induces an increase in lipid rafts having zona pellucida binding ability and containing sulfogalactosylglycerolipid. Dev. Biol. 290 (2005) 220-235
4. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
5. Brown C.R., and Jones R. Binding of zone pellucida glycoproteins to a boar sperm polypeptide of Mr 53,000 and identification of zona moieties involved. Development 99 (1987) 333-339
6. Bulow H.E., and Hobert O. Differential sulfations and epimerization define heparin sulfate specificity in nervous system development. Neuron 41 (2004) 723-736
7. Burkin H.R., and Miller D.J. Zona pellucida protein binding ability of porcine sperm during epididymal maturation and the acrosome reaction. Dev. Biol. 222 (2000) 99-109
8. Cadéne M., Duranton J., North A., Si-Takar M., Chignard M., and Bieth J.G. Inhibition of neutrophil serine proteinases by suramin. J. Biol. Chem. 272 (1997) 9950-9955
9. Caputo M., Riccio S., Paglierucci P., Tretola L., Diglio C., Carotenuto R., De Marco N., and Campanella C. Sulphated glycoconjugates are powerful inhibitors of spermatozoa binding to the vitelline envelope in amphibian eggs. Biol. Cell 97 (2005) 435-444
10. Crosby J.A., Jones R., Barros C., and Carvallo P. Characterization of the functional domains of boar acrosin involved in nonenzymatic binding to homologous zona pellucida glycoproteins. Mol. Reprod. Dev. 49 (1998) 426-434
11. Dean J. Reassessing the molecular biology of sperm-egg recognition with mouse genetics. BioEssays 26 (2004) 29-38
12. De Angelis P.L., and Glabe C.G. Polysaccharide structural features that are critical for the binding of sulfated fucans to bindin, the adhesive protein from sea urchin sperm. J. Biol. Chem. 262 (1987) 13946-13952
13. Duhme S.T., and Lennarz W.J. The involvement of O-linked oligosaccharide chains of the sea urchin egg receptor for sperm in fertilization. Glycobiology 5 (1995) 11-17
14. Foster J.A., Friday B.B., Maulit M.T., Blobel C., Winfrey V.P., Olsen G.E., Kim K.S., and Gerton G.L. AM67, a secretory component of the guinea-pig sperm acrosomal matrix, is related to mouse sperm sp56 and the complement component 4-binding proteins. J. Biol. Chem. 272 (1997) 12714-12722
15. Gama C.I., Tully S.E., Sotogaku N., Clark P.M., Rawat M., Vaidehi N., Goddard III W.A., Nishi A., and Hsieh-Wilson L.C. Sulfation patterns of glycosaminoglycans encode molecular recognition and activity. Nat. Chem. Biol. 2 (2006) 467-473
16. Hardy D.M., and Garbers D.L. A sperm membrane protein that binds in a species-specific manner to the egg extracellular matrix is homologous to von Willebrand factor. J. Biol. Chem. 270 (1995) 26025-26028
17. Harkema W., Harrison R.A., Miller N.G., Topper E.K., and Woelders M. Enhanced binding of zona pellucida proteins to the acrosomal region of the intact boar spermatozoa in response to fertility conditions: a flow cytometric study. Biol. Reprod. 58 (1998) 421-430
18. Hermans J.M., Haines D.S., James P.S., and Jones R. Kinetics of inhibition of sperm β-acrosin by suramin. FEBS Lett. 544 (2003) 119-122
19. Holt C.E., and Dickson B.J. Sugar codes for axons?. Neuron 46 (2005) 169-172
20. Howes L., and Jones R. Interactions between zona pellucida glycoproteins and sperm proacrosin/acrosin during fertilization. J. Reprod. Immunol. 53 (2002) 181-192
21. Howes E., Pascall J.C., Engel W., and Jones R. Interactions between mouse ZP2 glycoprotein and proacrosin; a mechanism for secondary binding of sperm to the zona pellucida during fertilization. J. Cell Sci. 114 (2001) 4127-4136
22. Jansen S., Quigley M., Reik W., and Jones R. Analysis of polysulphate-binding domains in boar proacrosin, a putative zona adhesion molecule from mammalian spermatozoa. Int. J. Dev. Biol. 39 (1995) 501-510
23. Jansen S., Jones R., Jenneckens I., Marschall B., Kriegesmann B., Coadwell J., and Brenig B. Site-directed mutagenesis of boar proacrosin reveals residues involved in binding of zona pellucida glycoproteins. Mol. Reprod. Dev. 51 (1998) 184-192
24. Jeffery C.J. Moonlighting proteins. Trends Biochem. Sci. 24 (1999) 8-11
25. Jentsch K.D., Hunsman G., Hartmann H., and Nickel P. Inhibition of human immuno-deficiency versus type 1 reverse transcriptase by suramin-related compounds. J. Gen. Virol. 68 (1987) 2183-2192
26. Jin L., Abrahams J.P., Skinner R., Petitou M., Pike R.N., and Carrell R.W. The anticoagulant activation of antithrombin by heparin. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 14683-14688
27. Jones R. Interaction of zona pellucida glycoproteins, sulphated carbohydrates and synthetic polymers with proacrosin the putative egg-binding molecule from mammalian spermatozoa. Development 111 (1991) 1155-1163
28. Jones R., Parry R., Lo Leggio L., and Nickel P. Inhibition of sperm-zona binding by suramin, a potential 'lead' compound for design of new anti-fertility agents. Mol. Hum. Reprod. 2 (1996) 597-605
29. Jovine L., Darie C.C., Litscher E.S., and Wassarman P.M. Zona pellucida domain proteins. Annu. Rev. Biochem. 74 (2005) 83-114
30. Kim K.-S., Cha M.C., and Gerton G.L. Mouse sperm protein sp56 is a component of the acrosomal matrix. Biol. Reprod. 64 (2001) 36-43
31. Klemm U., Muller-Esterl W., and Engel W. Acrosin, the peculiar sperm-specific serine protease. Hum. Genet. 87 (1991) 635-641
32. Lo Leggio L., Williams R.M., and Jones R. Some effects of zona pellucida glycoproteins and sulphated polymers on the autoactivation of boar sperm proacrosin and activity of β-acrosin. J. Reprod. Fertil. 100 (1994) 177-185
33. Maehashi E., Sato C., Ohta K., Harada Y., Matsuda T., Hirohashi T., Lennarz W.J., and Kitajima K. Identification of the sea urchin 350-kDa sperm binding protein as a new sialic acid-binding lectin that belongs to the heat shock protein 110 family: implication of its binding to gangliosides in sperm lipid rafts in fertilization. J. Biol. Chem. 278 (2003) 42050-42057
34. Moore B. Bifunctional and moonlighting enzymes: lighting the way to regulatory control. Trends Plant Sci. 9 (2004) 221-228
35. Moreno R.D., Sepulveda M.S., de Ioannes A., and Barros C. The polysulphate binding domain of human proacrosin/acrosin is involved in both the enzyme activation and spermatozoa-zona pellucida interaction. Zygote 6 (1998) 75-83
36. Mori E., Kashiwabara S., Baba T., Inagaki Y., and Mori T. Amino acid sequences of porcine Sp38 and proacrosin required for binding to the zona pellucida. Dev. Biol. 168 (1995) 575-583
37. Mourǎo P.A.S. A carbohydrate-based mechanism of species recognition in sea urchin fertilization. Braz. J. Med. Biol. Res. 40 (2007) 5-17
38. Nakano M., Hatanaka Y., Kobayashi M., Noguchi S., Ishikawa S., and Tobita T. Further fractionation of the glycoprotein families of porcine zona pellucida by ion-exchange HPLC and some characterization of the separated fractions. J. Biochem. 107 (1990) 144-150
39. Omata S., and Katagiri C. Involvement of carbohydrate moieties of the toad egg vitelline coat in binding with fertilizing sperm. Dev. Growth Diff. 38 (1996) 663-672
40. Peterson R.N., Russell L.D., Bundman D., Conway M., and Freund M. The interaction of living boar sperm and sperm plasma membrane vesicles with the porcine zona pellucida. Dev. Biol. 84 (1981) 144-156
41. Rankin T., and Dean J. The zona pellucida: using molecular genetics to study the mammalian egg coat. Rev. Reprod. 5 (2000) 114-121
42. Rankin T., Coleman J.S., Hoodboy T., Turner S.G., Castle P.E., Lee E., Gore-Langton R., and Dean J. Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologues. Dev. Cell 5 (2003) 33-34
43. Richardson R.T., and O'Rand M.G. Site-directed mutagenesis of rabbit proacrosin. Identification of residues involved in zona pellucida binding. J. Biol. Chem. 271 (1996) 24069-24074
44. Shimizu S., Tsuji M., and Dean J. In vitro biosynthesis of three sulphated glycoproteins in murine zonae pellucidae by oocytes grown in organ culture. J. Biol. Chem. 258 (1983) 5858-5863
45. Shur B.D., Rodeheffer C., Ensslin M.A., Lyng T., and Raymond A. Identification of novel gamete receptors that mediate sperm adhesion to the egg coat. Mol. Cell. Endrocinol. 250 (2006) 137-148
46. Stears R.L., and Lennarz W.J. Mapping sperm binding domains on the sea urchin egg receptor for sperm. Dev. Biol. 187 (1997) 200-208
47. Suzuki-Toyota F., Maekawa M., Cheng A., and Bleil J.D. Immuno-colloidal gold labeled surface replica, and its application to detect sp56, the egg recognition and binding protein, on the mouse spermatozoon. J. Electron Microsc. 44 (1995) 135-139
48. Tranter R., Read J.A., Jones R., and Brady R.L. Effector sites in the three-dimensional structure of mammalian sperm β-acrosin. Structure 8 (2000) 1179-1188
49. Urch U.A., and Patel H. The interaction of boar sperm proacrosin with its natural substrate, the zona pellucida and with polysulphated polysaccharides. Development 111 (1991) 1165-1172
50. Ushiyama A., Araki T., Chilea K., and Hoshi M. Specific binding of acrosome- reaction-inducing substance to the head of starfish spermatozoa. Zygote 1 (1993) 121-127
51. Vacquier V.D., and Moy G.W. Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs. Proc. Natl. Acad. Sci. U. S. A. 74 (1977) 2456-2460
52. van Gestel R.A., Brewis I.A., Ashton P.R., Helms J.B., Brouwers J.F., and Gadella B.M. Capacitation-dependent concentration of lipid rafts in the apical ridge area of porcine sperm cells. Mol. Hum. Reprod. 11 (2005) 583-590
53. Vo L.H., Yen T.-Y., Macher B.A., and Hedrick J.L. Identification of the ZPC oligosaccharide ligand involved in sperm binding and the glycan structures of Xenopus laevis vitelline envelope glycoproteins. Biol. Reprod. 69 (2003) 1822-1830
54. Whisstock J.C., Pike P.N., Jin L., Skinner R., Pei X.Y., Carrell R.W., and Lesk A.M. Conformational changes in serpins: II. The mechanism of activation of antithrombin by heparindagger. J. Mol. Biol. 301 (2000) 1287-1305
55. Williams R.M., and Jones R. Specificity of binding of zona pellucida glycoproteins to sperm proacrosin and related proteins. J. Exp. Zool. 266 (1993) 65-73
56. Yanagimachi R., and Phillips D.M. The status of acrosomal caps of hamster spermatozoa immediately before fertilization in vivo. Gamete Res. 9 (1983) 1-19
57. Yonezawa N., Hatanaka Y., Takeyama H., and Nakano M. Binding of pig sperm receptor in the zona pellucida to the boar sperm acrosome. J. Reprod. Fertil. 103 (1995) 1-8
58. Yonezawa M., Mitsui S., Kudo K., and Nakano M. Identification of an N-glycosylated region of pig zona pellucida glycoprotein ZPB that is involved in sperm binding. Eur. J. Biochem. 248 (1997) 86-92
59. Yoshizawa M., Nagai T., Yonezawa N., and Nakano M. Native zona pellucida structure is required for completion of sperm acrosome reaction in porcine fertilization. Theriogenology 41 (1994) 1307-1313
60. Yurewicz E.C., Pack B.A., Armant D.R., and Sacco A.G. Porcine zona pellucida ZP3 alpha glycoprotein mediates binding of the biotin-labelled M(r) 55,000 family (ZP3) to boar sperm membrane vesicles. Mol. Reprod. Dev. 36 (1993) 382-389
61. Yurewicz E.C., Sacco A.G., Gupta S.K., Xu N., and Gage D.A. Hetero-oligomerization-dependent binding of pig oocyte zona pellucida glycoproteins ZPB and ZPC to boar sperm membrane vesicles. J. Biol. Chem. 273 (1998) 7488-7494