PH-20 but not acrosin is involved in sperm penetration of the macaque zona pellucida

Molecular Reproduction and Development

Volumn 53, Issue 3, 1999, Pages 350-362

  Yudin, Ashley I ^a   Vandevoort, Catherine A ^b   Li, Ming Wen ^a   Overstreet, James W ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acrosin; CD 46; PH 20; Sperm; Zona pellucida

Indexed keywords

ACROSIN; CALCIMYCIN; CELL SURFACE PROTEIN; IMMUNOGLOBULIN G; MEMBRANE PROTEIN; SOYBEAN TRYPSIN INHIBITOR;

ACROSOME; ACROSOME REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; ENZYME LOCALIZATION; MACACA; NONHUMAN; PRIORITY JOURNAL; SPERMATOZOON; SPERMATOZOON PENETRATION; ZONA PELLUCIDA;

ACROSIN; ACROSOME; ANIMALS; ANTIGENS, CD; ANTIGENS, CD46; BLOTTING, WESTERN; CELL ADHESION MOLECULES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; HYALURONOGLUCOSAMINIDASE; MACACA FASCICULARIS; MALE; MEMBRANE GLYCOPROTEINS; SPERM-OVUM INTERACTIONS; SPERMATOZOA; ZONA PELLUCIDA;

ANIMALIA; GLYCINE MAX; MACACA; SUS SCROFA;

EID: 0344299181     PISSN: 1040452X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2795(199907)53:3<350::AID-MRD11>3.0.CO;2-9     Document Type: Article

References (70)

1. Adham IM, Nayermia K, Engel W. 1997. Spermatozoa lacking acrosin protein show delayed fertilization. Mol Reprod Dev 46:370-376.
2. Anderson DF, Abbott AF, Jack RM. 1993. The role of complement component C3b and its receptors in sperm-oocyte interaction. Proc Natl Acad Sci USA 90:10051-10055.
3. Austin CR. 1960. Capacitation and the release of hyaluronidase from the spermatozoa. J Reprod Fertil 3:310-311.
4. Baba T, Azuma S, Kashiwabara S, Toyoda Y. 1994. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J Biol Chem 269:31845-31849.
5. Barros C, Capote C, Perez C, Crosby JA, Becker M, DeIoannes A. 1992. Immunodetection of acrosin during the acrosome reaction of hamster, guinea pig, and human spermatozoa. Biol Res 25:31-40.
6. Bedford JM. 1991. The coevolution of mammalian gametes. In: Dunbar BS, O'Rand MG, editors. A comparative overview of mammalian fertilization. New York: Plenum Press, p 3-35.
7. Bedford JM. 1998. Mammalian fertilization misread? Penetration of the eutherian zona pellucida is unlikely to be a hytic event. Biol Reprod 59:1275-1287.
8. Bedford JM, Hoskins DD. 1990. The mammalian spermatozoa: morphology, biochemistry, and physiology. In: Lamming GE, editor. Marshall's physiology of reproduction vol 2. Edinburgh: Churchill Livingston. p 379-468.
9. Bleil JD, Greve JM, Wassarman PM. 1988. Identification of a secondary sperm receptor in the mouse egg zona pellucida: a role in maintenance of binding of acrosome-reacted sperm to eggs. Dev Biol 128:376-385.
10. Bleil JD, Washerman PM. 1980. Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20:873-882.
11. Bleil JD, Wassarman PM. 1983. Sperm-egg interactions in the mouse: Sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev Biol 95:317-324.
12. Bleil JD, Wassarman, PM. 1986. Autoradiographic visualization of the mouse egg's sperm receptor bound to sperm. J Cell Biol 102:1363-1371.
13. Cherr GN, Lambert H, Meizel S, Katz DF. 1986. In vitro studies of the golden hamster sperm acrosome reaction: Completion on the zona pellucida and induction by homologous soluble zonae pellucida. Dev Biol 114:119-131.
14. Cherr GN, Meyers SA, Yudin AI, VandeVoort CA, Myles DG, Primakoff P, Overstreet JW. 1996. The PH-20 protein in cynomolgus macaque spermatozoa: Identification of two different forms exhibiting hyaluronidase activity. Dev Biol 175:142-153.
15. Cherr GN, Yudin AI, Li M-W, Overstreet JW. 1999. Hyaluronic acid and the cumulus extracellular matrix induce increases in intracellular calcium in macaque sperm via the plasma membrane protein PH-20. Zygote (in press).
16. Crosby JA, Jones R., Barros C, Carvallo P. 1998. Characterization of the functional domains of boar acrosin involved in non enzymatic binding to homologous zona pellucida glycoproteins. Mol Reprod Dev 49:426-434.
17. Cummins JM, Yanagimachi R. 1986. Development of ability to penetrate the cumulus oophorus by hamster spermatozoa capacitated in vitro, in relation to the timing of the acrosome reaction. Gamete Res 15:187-212.
18. Drobnis EZ, Yudin AI, Cherr GN, Katz DF. 1988. Hamster sperm penetration of the zona pellucida: Kinematic analysis and mechanical implications. Dev Biol 130:311-323.
19. Fénichel P, Dohr G, Grivaux C, Cervoni F, Donzeau M, Hsi BL. 1990. Localization and characterization of the acrosomal antigen recognized by GB24 on human spermatozoa. Mol Reprod Dev 27:173-178.
20. Gacesa P, Civill ND, Harrison, RA. 1994. PH-20 and sperm hyaluronidase: a conceptual conundrum in mammalian fertilization. Biochem J 303:335-336.
21. Gmachl M and Kreil G. 1993. Bee venom hyaluronidase is homologous to a membrane protein of mammalian sperm. Proc Natl Acad Sci USA 90:3569-3573.
22. Green DPL. 1988. Sperm thrusts and problem of penetration. Biol Rev 63:79-105.
23. Hedrick JL, Urch UA, Hardy DM. 1989. The structure-function properties of the sperm enzyme acrosin. In: Whitaker JR, Sonnett PE, editors. Biocatalysis in agricultural biotechnology. Washington, DC: American Chemical Society, p 212-229.
24. Huang TT Jr, Yanagimachi R. 1985. Inner acrosomal membrane of mammalian spermatozoa: its properties and possible functions in fertilization. Am J Anat 174:249-268.
25. Hunnicutt GR, Primakoff P, Myles DG. 1996. Sperm surface protein PH-20 is bifunctional: one activity is a hyaluronidase and a second, distinct activity is required in secondary sperm-zona binding. Biol Reprod 55:80-86.
26. Jones R. 1991. Interaction of zona pellucida glycoproteins, sulfated carbohydrates, and synthetic polymers with proacrosin, the putative egg-binding protein from mammalian spermatozoa. Development 111:1155-1163.
27. Jones R, Ma A, Hou S, Shalgi R, Hall L. 1996. Testicular biosynthesis and epididymal andoproteolytic processing of rat sperm surface antigen ZB1. J Cell Sci 109:2561-2570.
28. Jones R, Williams RM. 1990. Identification of zona-and fucoidin-binding proteins in guinea-pig spermatozoa and mechanisms of recognition. Development 109:41-50.
29. Jones R, Brown CR, Lancaster RT. 1988. Carbohydrate-binding properties of boar sperm proacrosin and assessment of its role in sperm-egg recognition and adhesion during fertilization. Development 102:781-792.
30. Kan FWK. 1990. High resolution localization of hyaluronic acid in the golden hamster oocyte-cumulus complex by use of a hyaluronidase-gold complex. Anat Rec 228:370-382.
31. Kuzan FB, Fleming AD, Seidel, GE Jr. 1984. Successful fertilization in vitro of fresh intact oocytes by perivitelline (acrosome-reacted) spermatozoa of the rabbit. Fertil Steril 41:766-770.
32. Llanos M, Vigil P, Salgado AM, Morales P. 1993. Inhibition of the acrosome reaction by trypsin inhibitors and prevention of penetration of spermatozoa through the human zona pellucida. J Reprod Fertil 97:173-178.
33. Li MW, Yudin AI, VandeVoort CA, Sabeur K, Primakoff P, Overstreet JW. 1997a. Inhibition of monkey sperm hyaluronidase activity and heterologous cumulus penetration by flavonoids. Biol Reprod 56: 1383-1389.
34. Li M, Cherr GN, Yudin AI, Overstreet JW. 1997b. Biochemical characterization of the PH-20 protein on the plasma membrane and inner acrosomal membrane of cynomolgus macaque spermatozoa. Mol Reprod Dev 48:356-366.
35. Lin Y, Kimmel LH, Myles DG, Primakoff P. 1993. Molecular cloning of the human and monkey sperm surface protein PH-20. Proc Natl Acad Sci USA 90:10071-10075.
36. Lin Y, Mahan K, Lathrop WF, Myles DG, Primakoff P. 1994. A hyaluronidase activity of the sperm plasma membrane protein PH-20 enables sperm to penetrate the cumulus cell layer surrounding the egg. J Cell Biol 125:1157-1163.
37. Liu DY, Baker HWG. 1993. Inhibition of acrosin activity with a trypsin inhibitor blocks human sperm penetration of the zona pellucida. Biol Reprod 48:340-348.
38. Lopez LC, Shur BD. 1987. Redistribution of mouse sperm surface galactosyltransferase after the acrosome reaction. J Cell Biol 105: 1663-1670.
39. Martinez ML, Fontenot GK, Harris JD. 1996. The expression and localization of zona pellucida glycoproteins and mRNA in cynomolgus monkeys (Macaca fascicularis). J Reprod Fertil (Suppl) 50: 35-41.
40. Meyers SA, Yudin AL, Cherr GN, VandeVoort CA, Myles DG, Primakoff P, Overstreet JW. 1997. Hyaluronidase activity of macaque sperm assessed by an in vitro cumulus penetration assay. Mol Reprod Dev 46:392-400.
41. Morales P, Cross NL, Overstreet JW, Hanson FW. 1989. Acrosome intact and acrosome-reacted sperm can initiate binding to the zona pellucida. Dev Biol 133:385-392.
42. Mortillo S, Wassarman P. 1991. Differential binding of gold-labeled zona pellucida glycoproteins mZP2 and mZP3 to mouse sperm membrane compartments Development 113:141-149.
43. Myles DG, Hyatt H, Primakoff P. 1987. Binding of both acrosome intact and acrosome reacted guinea pig sperm bind to the zona pellucida during in vitro fertilization. Dev Biol 121:559-567.
44. Myles DG, Primakoff P. 1984. Localized surface antigens of guinea pig sperm migrate to new regions prior to fertilization. J Cell Biol 99:1634-1641.
45. Myles DG, Primakoff P. 1997. Why did the sperm cross the cumulus? To get to the oocyte; functions of the sperm surface proteins PH-20 and fertilin in arriving at, and fusing with, the egg. Biol Reprod 56:320-327.
46. Overstreet JW, Lin Y, Yudin AI, Meyers SA, Primakoff P, Myles DG, Katz DF, VandeVoort CA. 1995. Location of the PH-20 protein on acrosome intact and acrosome reacted spermatozoa of cynomolgus macaques. Biol Reprod 52:105-114.
47. Phelps BM, Myles DG. 1987. The guinea pig sperm plasma membrane protein, PH-20 reaches the surface via two transport pathways and becomes localized to a domain after an initial uniform distribution. Dev Biol 123:63-72.
48. Pillai MC, Meizel S. 1991. Trypsin inhibitors prevent the progesterone-initiated increase in intracellular calcium required for the human sperm acrosome reaction. J Exp Zool 258:384-393.
49. Primakoff P, Lathrop W, Woolman L, Cowan A, Myles DG. 1988. Fully effective contraception in male and female guinea pig immunized with the sperm protein PH-20. Nature 335:543-546.
50. Primakoff P, Myles DG. 1983. A map of the guinea pig sperm surface constructed with monoclonal antibodies. Dev Biol 98:417-428.
51. Sabeur K, Cherr GN, Yudin AI, Primakoff P, Li M-W, Overstreet JW. 1997. The PH-20 protein in human spermatozoa. J Androl 18:151-158.
52. Sabeur K, Cherr GN, Yudin AI, Overstreet JW. 1998. Hyaluronic acid enhances induction of the acrosome reaction of human sperm through interaction with the PH-20 protein. Zygote 6:103-111.
53. Saling PM. 1981. Involvement of trypsin-like activity in binding of mouse spermatozoa to zona pellucida. Proc Natl Acad Sci USA 78:6231-6235.
54. Saling PM, Sowinski J, Storey BT. 1979. An ultrastructural study of epididymal mouse spermatozoa binding to zona pellucida in vitro: Sequential relationship to the acrosome reaction. J Exp Zool 209:229-238.
55. Sarason RL, VandeVoort CA, Mader DR, Overstreet JW. 1991. The use of nonmetal electrodes in electroejaculation of restrained but unanesthetized macaques. J Med Primatol 20:122-125.
56. Suarez SS, Katz DF, Meizel S. 1984. Changes in motility that accompany the acrosome reaction in hyperactivated hamster spermatozoa. Gamete Res. 10:253-266.
57. Talbot P, DiCarlantonio G. 1984. Architecture of the hamster oocyte-cumulus complex. Gamete Res 103:261-272.
58. Tesarik J, Drahorad J, Peknicova J. 1988. Subcellular immunochemical localization of acrosin in human spermatozoa during acrosome reaction and zona pellucida penetration. Fertil Steril 50:133-141.
59. Tesarik J, Drahorad J, Testart J, Mendoza C. 1990. Acrosin activation follows its surface exposure and precedes membrane fusion in human sperm acrosome reaction. Development 110:391-400.
60. Urch UA. 1991. Biochemisty and function of acrosin. In: Wassarman PM, editor. Elements of mammalian fertilization. Boca Raton: CRC Press, p 233-248.
61. Urch UA, Patel H. 1991. The interaction of boar sperm proacrosin with its natural substrate, zona pellucida, and with polysulfated polysaccharides. Development 111:1165-1172.
62. Urch UA, Wardrip NJ, Hedrick JL. 1985. Limited and specific proteolysis of the zona pellucida by acrosin. J Exp Zool 233:479-483.
63. VandeVoort CA, Tollner TL, Overstreet JW. 1992. Sperm-zona pellucida interaction in cynomolgus and rhesus macaques. J Androl 13:428-432.
64. VandeVoort CA, Yudin AI, Overstreet JW. 1997. Interaction of acrosome-reacted macaque sperm with the macaque zona pellucida. Biol Reprod 56:1307-1316.
65. Wassarman PM. 1992. Mouse gamete adhesion molecules. Biol Reprod 46:186-191.
66. Wassarman PM, Mortillo S. 1991. Structure of the mouse egg extracellular coat, the zona pellucida. Int Rev Cytol 130:85-110.
67. Yanagimachi R. 1981. Mechanisms of fertilization in mammals. In: Mastroianni I, Biggers JD, editors. Fertilization and embryonic development in vitro. New York: Plenum Press, p 81-92.
68. Yanagimachi R. 1988. Mammalian fertilization. In: Knobil Z et al, editors. The physiology of reproduction, vol 1. New York: Raven Press, p 135-185.
69. Yanagimachi R. 1994. Mammalian fertilization. In: Knobil Z, Neill ID, editors. The physiology of reproduction, vol 2. New York: Raven Press. p 189-317.
70. Yudin AI, Cherr GN, Vandevoort CA, Overstreet, JW. 1998. Rearrangement of the PH-20 protein on the surface of macaque spermatozoa following exposure to anti-PH-20 antibodies or binding to zona pellucida. Mol Reprod Dev 50:207-220.