The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization

Experimental Cell Research

Volumn 240, Issue 2, 1998, Pages 151-164

  Tulsiani, Daulat R P ^a   Abou Haila, Aida ^a   Loeser, Christoph R ^a   Pereira, Ben M J ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acrosome reaction; Mammalian fertilization; Sperm acrosome; Sperm egg interaction; Zona pellucida

Indexed keywords

ACROSOME; ACROSOME REACTION; CELL INTERACTION; ENZYME ACTIVITY; EXOCYTOSIS; FERTILIZATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SPERMATOZOON MATURATION;

MAMMALIA;

EID: 0031826659     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1998.3943     Document Type: Review

References (125)

1. Yanagimachi R. Mammalian fertilization. The Physiology of Reproduction. 1994;Raven Press, New York.
2. Tulsiani D. R. P., Yoshida-Komiya H., Araki Y. Mammalian fertilization: A carbohydrate mediated event. Biol. Reprod. 57:1997;487-494.
3. Wassarman P. M. Cell surface carbohydrate and mammalian fertilization. Fukuda M. Cell Surface Carbohydrate and Development. 1992;CRC Press, Boston.
4. Eddy, E. M. O'Brien, D. A. 1994, The spermatozoon, In, The Physiology of Reproduction, E. KnobilJ. D. Neill, Raven Press, New York.
5. Skudlarek M. D., Tulsiani D. R. P., Nagdas S. K., Orgebin-Crist M.-C. β-D-Galactosidase of rat spermatozoa: subcellular distribution, substrate specificity and molecular changes during epididymal maturation. Biol. Reprod. 49:1993;204-213.
6. Tulsiani D. R. P., Skudlarek M. D., Orgebin-Crist M.-C. Human sperm plasma membranes possess α-D-mannosidase activity but no galactosyl transferase activity. Biol. Reprod. 42:1990;843-858.
7. Tulsiani D. R. P., Skudlarek M. D., Holland M. K., Orgebin-Crist M.-C. Glycosylation of rat sperm plasma membrane during epididymal maturation. Biol. Reprod. 48:1993;417-428.
8. Saling P. M., Storey B. T. Mouse gamete interactions during fertilization in vitro: Chlortetracycline as fluorescent probe for the mouse sperm acrosome reaction. J. Cell Biol. 83:1979;544-555.
9. Storey B. T., Lee M. A., Muller C., Ward C. R., Wirtshafter D. G. Binding of mouse spermatozoa to the Zona pellucida of mouse egg in cumulus: Evidence that the acrosome remain substantially intact. Biol. Reprod. 31:1984;1119-1128.
10. Phillips D. M., Shalgi R. Sperm penetration into rat ova fertilized in vivo. J. Exp. Zool. 221:1982;373-378.
11. Wassarman P. M. Zona pellucida glycoproteins. Annu. Rev. Biochem. 57:1988;415-442.
12. Wassarman P. M. Mammalian fertilization: egg and sperm (glyco) protein that support gamete adhesion. Am. J. Reprod. Immunol. 33:1995;253-258.
13. Snell W. J., White J. M. The molecules of mammalian fertilization. Cell. 85:1996;629-637.
14. Shur B. D. Glycosyltransferases as cell adhesion molecules. Curr. Opin. Cell Biol. 5:1992;854-863.
15. Myles D. G. Molecular mechanism of sperm-egg membrane binding and fusion in mammals. Dev. Biol. 158:1993;35-45.
16. Chapman N. R., Barratt C. L. R. The role of carbohydrate in sperm-ZP3 adhesion. Mol. Hum. Reprod. 2:1996;767-774.
17. Benoff S. Carbohydrates and fertilization: An overview. Mol. Hum. Reprod. 3:1997;599-637.
18. Ward C. R., Kopf G. S. Molecular events mediating sperm activation. Dev. Biol. 158:1993;9-34.
19. de Kretser D. M., Kerr J. B. The cytology of the testis. Knobil E., Neill J. D. The Physiology of Reproduction. 1994;Raven Press, New York.
20. Kierszenbaum A. L. Mammalian spermatogenesisin vivoandin vitro: A partnership of spermatogenic and somatic cell lineages. Endocr. Rev. 15:1994;116-134.
21. Parvinen M., Vihko K. K., Toppari J. Cell interactions during the seminiferous epithelial cycle. Int. Rev. Cytol. 104:1986;115-151.
22. Clermont Y., Oko R., Hermo L. Cell biology of mammalian spermiogenesis. Desjardins C., Ewing L. L. Cell and Molecular Biology of the Testis. 1993;Oxford Univ. Press, Oxford, New York.
23. Huang T. T. F. Jr., Yanagimachi R. Inner acrosomal membrane of mammalian spermatozoa: Its properties and possible functions in fertilization. Am. J. Anat. 174:1985;249-268.
24. Fenderson B. A., O'Brien D. A., Millette C. F., Eddy E. M. Stage-specific expression of three cell surface carbohydrate antigens during murine spermatogenesis detected with monoclonal antibodies. Dev. Biol. 103:1984;117-128.
25. Gerton G. L., Millette C. F. Stage-specific synthesis and fucosylation of plasma membrane proteins by mouse pachytene spermatocytes and round spermatids in culture. Biol. Reprod. 35:1986;1025-1035.
26. Scully N. F., Shaper J. H., Shur B. D. Spatial and temporal expression of cell surface galactosyltransferase during mouse spermatogenesis and epididymal maturation. Dev. Biol. 124:1987;111-124.
27. Millette C. F., Bellve A. R. Selective partitioning of plasma membrane antigens during mouse spermatogenesis. Dev. Biol. 79:1980;309-324.
28. Millette C. F., Cardullo R. A., Armant D. R., Gerton G. L. Fucosylation events during mammalian spermatogenesis. Ann. N. Y. Acad. Sci. 513:1987;58-73.
29. Blobel C. P., Myles D. G., Primakoff P., White J. M. Proteolytic processing of a protein involved in sperm-egg fusion correlates with acquisition of fertilization competence. J. Cell Biol. 111:1990;69-78.
30. Tulsiani D. R. P., Nagdas S. K., Skudlarek M. D., Orgebin-Crist M.-C. Rat sperm plasma membrane mannosidase: Localization and evidence for proteolytic processing during epididymal maturation. Dev. Biol. 167:1995;584-595.
31. Neurath H. Proteolytic processing and physiological regulation. Trends Biochem. Sci. 14:1989;268-271.
32. Myles D. G. Sperm cell surface proteins of testicular origin: expression and localization in the testis and beyond. Desjardins C., Ewing L. L. Cell and Molecular Biology of the Testis. 1993;Oxford Univ. Press, Oxford.
33. Jones R. Membrane remodelling during sperm maturation in the epididymis. Milligan S. R. Oxford Reviews of Reproductive Biology. 1989;Oxford Univ. Press, Oxford.
34. Hall J. C., Killian G. J. Changes in rat sperm membrane glycosidase activities and carbohydrate and protein contents associated with epididymal transit. Biol. Reprod. 25:1987;385-392.
35. Tulsiani D. R. P., Skudlarek M. D., Araki Y., Orgebin-Crist M.-C. Purification and characterization of two forms of β-D-galactosidase from rat epididymal luminal fluid: Evidence for their role in the modification of sperm plasma membrane glycoprotein(s). Biochem. J. 305:1995;41-50.
36. r= ~24,000 molecule from rat spermatozoa that is glycosylated during epididymal maturation. Biol. Reprod. 34:1986;925-936.
37. Jones R., Ma A., Hou S. T., Shalgi R., Hall L. Testicular biosynthesis and epididymal endoproteolytic processing of rat sperm surface antigen 2B1. J. Cell Sci. 109:1996;2561-2570.
38. Phelps B. M., Koppel D. E., Primakoff P., Myles D. G. Evidence that proteolysis of the surface is an initial step in the mechanism of formation of sperm cell surface domains. J. Cell Biol. 111:1991;1839-1847.
39. Saling, P. M. 1989, Mammalian sperm interaction with extracellular matrices of the egg, In, Oxford Reviews of Reproductive Biology, S. R. Milligan, Oxford Univ. Press, Oxford.
40. Hamilton D. W., Gould R. P. Preliminary observation on enzymatic galactosylation of glycoproteins on the rat caput epididymal spermatozoa. Int. J. Androl. (Suppl.). 5:1982;73-80.
41. Lakoski K. A., Williams C., Saling P. M. Epididymal maturation and the acrosomal reaction in mouse sperm: Immunological probes reveal post-testicular modifications. Gamete Res. 23:1988;21-37.
42. Petruszak J. A. M., Nehme C. L., Bartles J. R. Endoproteolytic cleavage in the extracellular domain of the integral plasma membrane protein CE9 preceeds its redistribution from the posterior to the anterior tail of the rat spermatozoa during epididymal maturation. J. Cell Sci. 114:1991;917-927.
43. Hancock L. W., Raab L. S., Aronson N. N. Jr. Synthesis and processing of rat sperm associated α-fucosidase. Biol. Reprod. 48:1993;1228-1238.
44. Nagdas S. K., Skudlarek M. D., Orgebin-Crist M.-C., Tulsiani D. R. P. Biochemical alterations in proacrosin-acrosin system during epididymal maturation of the rat spermatozoa. J. Androl. 13:1992;36-43.
45. Anakwe O. O., Gerton G. L. Acrosome biogenesis begins during meiosis: Evidence from the synthesis and distribution of an acrosomal glycoprotein, acrogranin, during guinea pig spermatogenesis. Biol. Reprod. 42:1990;317-328.
46. de Duve C. The lysosome. Sci. Am. 208:1963;64-72.
47. Garbers D. L., Wakabayashi T., Reed P. W. Enzyme profile of the cytoplasmic droplet from bovine epididymal spermatozoa. Biol. Reprod. 3:1970;327-337.
48. Kornfeld R., Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:1985;631-664.
49. Bischoff J., Kornfeld R. Evidence for an α-mannosidase in endoplasmic reticulum of rat liver. J. Biol. Chem. 258:1983;7907-7910.
50. Tabas I., Kornfeld S. Purification and characterization of a rat liver Golgi α-mannosidase capable of processing asparagine-linked oligosaccharides. J. Biol. Chem. 254:1979;11655-11663.
51. 5intermediate. J. Biol. Chem. 257:1982;3660-3668.
52. Harpaz N., Schachter H. Control of glycoprotein synthesis: processing of asparagine-linked oligosaccharide by one or more rat liver Golgi α-D-mannosidases dependent on the prior action of UDP-N-acetylglucosamine: α-D-Mannoside β-N-acetylglucosaminyl transferase I. J. Biol. Chem. 255:1980;4894-4902.
53. Tulsiani D. R. P., Touster O. Swainsonine causes the production of hybrid glycoproteins by human skin fibroblasts and rat liver Golgi preparations. J. Biol. Chem. 258:1983;7578-7585.
54. Kornfeld S., Mellman I. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5:1989;483-525.
55. Hille-Rehfeld A. Mannose-6-phosphate receptors in sorting and transport of lysosomal enzymes. Biochim. Biophys. Acta. 1241:1995;177-194.
56. Kornfeld S. Structure and function of the mannose 6-phosphate/insulin-like growth factor II receptors. Annu. Rev. Biochem. 61:1992;307-330.
57. Brown W. J., Goodhouse J., Farquhar M. G. M6P receptors for lysosomal enzymes recycle between Golgi complex and endosomes. J. Cell. Biol. 103:1986;1235-1347.
58. O'Brien D. A., Gabel C. A., Rockett D. L., Eddy E. M. Receptor-mediated endocytosis and differential synthesis of mannose-6-phosphate receptors in isolated spermatogenic and Sertoli cells. Endocrinology. 125:1989;2973-2984.
59. Conzelman E., Sandhoff K. Glycolipid and glycoprotein degradation. Adv. Enzymol. Relat. Areas Mol. Biol. 60:1987;89-216.
60. Ichikawa Y., Look G. C., Wong C. H. Enzyme-catalyzed oligosaccharide synthesis. Anal. Biochem. 202:1992;215-238.
61. Talbot P., Dicarlantonio G. Cytochemical localization of dipeptidyl peptidase II (DPP-II) in mature guinea pig sperm. J. Histochem. Cytochem. 33:1985;1169-1172.
62. Yotsumoto H., Sato S., Shibuya M. Localization of angiotensin converting enzyme (dipeptidyl carboxypeptidase) in swine sperm by immunofluorescence. Life Sci. 35:1984;1257-1261.
63. Schollmeier J. E. Identification of calpain II in porcine sperm. Biol. Reprod. 34:1986;721-731.
64. Kashiwabara S. T., Arai Y., Kodaira K., Baba T. Acrosin biosynthesis in meiotic and post meiotic spermatogenic cells. Biochem. Biophys. Res. Commun. 173:1990;240-245.
65. Baba T., Azuma S., Kashiwabara S. I., Toyoda Y. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J. Biol. Chem. 269:1994;31845-31849.
66. Zaneveld L. J. D., de Jonge C. J. Mammalian sperm acrosomal enzymes and the acrosome reaction. Dunbar B., O'Rand M. A Comparative Overview of Mammalian Fertilization. 1991;Plenum, New York.
67. de Lamirande E., Leclerc P., Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol. Hum. Reprod. 3:1997;175-194.
68. Fraser L. R. Cellular biology of capacitation and the acrosome reaction. Hum. Reprod. 10:1995;22-30.
69. Langlais J., Roberts K. D. A molecular membrane model of sperm capacitation and the acrosomal reaction of mammalian spermatozoa. Gamete Res. 12:1985;183-224.
70. Hoshi M., Matsui T., Nishiyama I., Amano T., Okita Y. Physiological inducers of the acrosome reaction. Cell Differ. Dev. 25:1988;19-24.
71. Roldan E. R., Murase T., Shi Q. X. Exocytosis in spermatozoa in response to progesterone and zona pellucida. Science. 266:1994;1578-1581.
72. Murase T., Roldan E. R. Progesterone and the Zona pellucida activate different transducing pathways in the sequence of events leading to diacylglycerol generation during mouse sperm acrosomal exocytosis. Biochem. J. 320:1996;1017-1023.
73. Brucker C., Lipford G. B. The human sperm acrosome reaction: physiology and regulatory mechanisms. An update. Hum. Reprod. Update. 1:1995;51-62.
74. Lenz R. W., Ball G. D., Lohse J. K., First N. L., Ax R. L. Chondroitin sulfate facilitates an acrosome reaction in bovine spermatozoa as evidenced by light microscopy, electron microscopy andin vitrofertilization. Biol. Reprod. 28:1983;683-690.
75. Zaneveld L. J. D., De Jonge C. J., Anderson R. A., Mack S. R. Human sperm capacitation and the acrosome reaction. Hum. Reprod. 6:1991;1265-1274.
76. Tarin J. J., Trounson A. O. Zona-free sperm penetration assay and inducers of the acrosome reaction: A model for sperm microinjection under the zona pellucida. Mol. Reprod. Dev. 35:1993;95-104.
77. Breitbart H., Spungin B. The biochemistry of the acrosome reaction. Mol. Hum. Reprod. 3:1997;195-202.
78. Kopf G. S., Gerton G. L. The mammalian sperm acrosome and the acrosomal reaction. Wassarman P. M. Elements of Mammalian Fertilization. 1991;CRC Press, Boca Raton.
79. Florman H. M., Bechtol K. B., Wassarman P. M. Enzymatic dissection of the functions of the mouse egg's receptor for sperm. Dev. Biol. 106:1984;243-255.
80. Leyton L., Saling P. Evidence that aggregation of mouse sperm receptors by ZP3 triggers the acrosome reaction. J. Cell. Biol. 108:1989;2163-2168.
81. Gong X., Dubois D. H., Miller D. J., Shur B. D. Activation of a G protein complex by aggregation of beta-1,4-galactosyltransferase on the surface of sperm. Science. 269:1995;1718-1721.
82. Boettger-Tong H. L., Arons D. J., Biegler B. E., George B., Poirier G. R. Binding of a murine proteinase inhibitor to the acrosome region of the human sperm head. Mol. Reprod. Dev. 36:1993;346-353.
83. 2+permeability: Population and single cell kinetics. Gamete Res. 24:1989;303-326.
84. Hyne R. V., Garbers D. L. Calcium-dependent increase in adenosine 3′5′-monophosphate and induction of the acrosomal reaction in guinea pig spermatozoa. Proc. Natl. Acad. Sci. USA. 76:1979;5699-5703.
85. Garde J., Roldan E. R. rab-3-peptide stimulates exocytosis of the ram sperm acrosome via interaction with cyclic AMP and phospholipase A2 metabolites. FEBS Lett. 391:1996;263-268.
86. Walensky L. D., Snyder S. H. Inositol 1,4,5-triphosphate receptors selectively localized to the acrosomes of mammalian sperm. J. Cell Biol. 130:1995;857-869.
87. 2+influx. Biochem. J. 264:1989;539-546.
88. Domino S. E., Garbers D. L. The fucose sulfate glycoconjugate that induces an acrosome reaction in spermatozoa stimulates inositol 1,4,5-triphosphate accumulation. J. Biol. Chem. 263:1988;690-695.
89. Ward C. R., Storey B. T., Kopf G. S. Selective activation of Gi1 and Gi2 in mouse sperm by the zona pellucida, the egg's extracellular matrix. J. Biol. Chem. 269:1994;13254-13258.
90. Ward C. R., Kopf G. S., Storey B. T. Solubilization and partial purification from mouse sperm membranes of the specific binding activity for 3-quinuclidinyl benzilate, a potent inhibitor of the zona pellucida-induced acrosome reaction. Mol. Reprod. Dev. 39:1994;423-432.
91. Ning X., Ward C. R., Kopf G. S. Activation of a Gi protein in digitonin/cholate-solubilized membrane preparations of mouse sperm by the zona pellucida, an egg-specific extracellular matrix. Mol. Reprod. Dev. 40:1995;355-363.
92. Karnik N. S., Newman S., Kopf G. S., Gerton G. L. Developmental expression of G protein alpha subunits in mouse spermatogenic cells: evidence that G alpha i is associated with the developing acrosome. Dev. Biol. 152:1992;393-402.
93. Ward C. R., Storey B. T., Kopf G. S. Activation of a Gi protein in mouse sperm membranes by solubilized proteins of the zona pellucida, the egg's extracellular matrix. J. Biol. Chem. 267:1992;14061-14067.
94. 2+and pH that mediates mammalian sperm acrosomal exocytosis. Dev. Biol. 135:1989;133-146.
95. Leyton L., Saling P. 95 kD sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding. Cell. 57:1989;1123-1130.
96. 2+channels by protein tyrosine phosphorylation. EMBO J. 16:1997;1593-1599.
97. Tomes C. N., McMaster C. R., Saling P. M. Activation of mouse sperm phosphatidylinositol-4,5 bisphosphate-phospholipase C by zona pellucida is modulated by tyrosine phosphorylation. Mol. Reprod. Dev. 43:1996;196-204.
98. 2+/ionophore-induced acrosome reaction of ram spermatozoa. J. Biol. Chem. 268:1993;13962-13970.
99. Leclerc P., Kopf G. S. Mouse sperm adenylyl cyclase: General properties and regulation by the zona pellucida. Biol. Reprod. 52:1995;1227-1233.
100. De Jonge C. J., Han H. L., Mack S. R, Zaneveld L. J. D. Modulation of the human sperm acrosome reaction by effectors of the adenylate/cyclic AMP second messanger pathway. J. Exp. Zool. 258:1991;113-125.
101. Spungin B., Margalit I., Breitbart H. Sperm exocytosis reconstructed in a cell-free system: Evidence for the involvement of phospholipase C and actin filaments in membrane fusion. J. Cell Sci. 108:1995;2525-2535.
102. Florman H. M., Corron M. E., Kim T. D. H., Babcock D. F. Activation of voltage dependent calcium channels of mammalian sperm is required for zona-induced acrosomal exocytosis. Dev. Biol. 152:1992;304-314.
103. 2+are initiated by the zona pellucida during acrosomal exocytosis. Dev. Biol. 165:1994;152-164.
104. 2+ATPase. J. Reprod. Fertil. 96:1992;363-377.
105. Breitbart H., Darshan R., Rubinstein S. Evidence for the presence of ATP-dependent calcium pump and ATPase activities in bull sperm head membranes. Biochem. Biophys. Res. Commun. 122:1984;479-484.
106. Polakoski K. L., Zaneveld L. J. D. Proacrosin. Lorand L. Methods in Enzymology: Proteolytic Enzymes. 1976;Academic Press, New York.
107. McRorie R. A., Turner R. B., Bradford M. M., Williams W. L. Acrolysin, the aminoproteinase catalyzing the initial conversion of proacrosin to acrosin in mammalian fertilization. Biochem. Biophys. Res. Commun. 71:1976;492-498.
108. Srivastava P. N., Ninjoor V. Isolation of rabbit testicular cathepsin D and its role in the activation of proacrosin. Biochem. Biophys. Res. Commun. 109:1982;63-69.
109. McDonald J. K., Kodhodayan S. Cathepsin L - a latent proteinase in guinea pig sperm. Biochem. Biophys. Res. Commun. 151:1988;827-835.
110. Scott R. P., Ninjoor V., Srivastava P. N. Isolation and characterization of cathepsin B from rabbit testis. J. Reprod. Fertil. 79:1987;67-74.
111. McDonald J. K., Culbertson J. T., Owers N. O. Identification and localization of a novel cathepsin S-like proteinase in guinea pig spermatozoa. Arch. Biochem. Biophys. 305:1993;1-8.
112. Gottlieb W., Meizel S. Biochemical studies of metalloendoproteinase activity in the spermatozoa of three mammalian species. J. Androl. 8:1987;14-24.
113. 2+dependent ATPase activity stimulated by decapacitation factor and calmodulin, in mouse sperm. Mol. Reprod. Dev. 44:1996;111-120.
114. 2+-dependent ATPase activity in guinea pig sperm head before and during the acrosome reaction. Gamete Res. 13:1986;271-280.
115. 2+ATPase in hamster sperm head membranes. Biochem. Biophys. Res. Commun. 104:1982;1060-1065.
116. +-ATPase activity are required for the hamster sperm acrosome reaction. J. Cell Biol. 91:1981;77-82.
117. Foresta C., Rossato M., Chiozzi P., Divirgilio F. Mechanism of human sperm activation by extracellular ATP. Am. J. Physiol. 270:1996;c1709-1714.
118. Bradley M. P., Forrester I. T. A sodium-calcium exchange mechanism in plasma membrane vesicles isolated from ram sperm flagella. FEBS Lett. 121:1980;15-18.
119. +requiring mechanisms modulate capacitation and acrosomal exocytosis in mouse spermatozoa. J. Reprod. Fertil. 97:1993;539-549.
120. -channel complex in the progesterone-initiated acrosome reaction. Dev. Biol. 159:1993;679-690.
121. +modifications can modulate mouse sperm capacitation and acrosomal exocytosis. J. Reprod. Fertil. Abstr. Ser. 14:1994;9.
122. 2+Channel found in sea urchin and mouse spermatozoa. FEBS Lett. 338:1994;23-26.
123. 2+channels by adhesion to the egg zona pellucida. Proc. Natl. Acad. Sci. USA. 93:1996;13004-13009.
124. 2+channels and alpha 1E expression in spermatogenic cells and their possible relevance to the sperm acrosome reaction. FEBS Lett. 388:1996;150-154.
125. 2+-selective channels in planar lipid bilayers. Am. J. Physiol. 268:1995;c1284-1294.