Gamete interaction: Is it species-specific?

Molecular Reproduction and Development

Volumn 73, Issue 11, 2006, Pages 1422-1429

  Vieira, Ana ^a   Miller, David J ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acrosome; Binding; Egg; Fertilization; Receptor; Sperm

Indexed keywords

ARTICLE; CELL INTERACTION; FERTILIZATION; GAMETE; GAMETE INTERACTION; INTRASPECIFIC VARIATION; MOLECULAR BIOLOGY; MOLECULAR RECOGNITION; NONHUMAN; POSTZYGOTIC BARRIER; PREZYGOTIC BARRIER; PRIORITY JOURNAL; REPRODUCTIVE ISOLATION; SPAWNING; SPECIES DIFFERENCE; SPECIES DIVERSITY; ZYGOTE;

ANIMALS; MAMMALS; POLYSACCHARIDES; SEA URCHINS; SPECIES SPECIFICITY; SPERM-OVUM INTERACTIONS; STARFISH;

ANIMALIA;

EID: 33748859212     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20542     Document Type: Article

References (96)

1. Alves AP, Mulloy B, Diniz JA, Mourao PA. 1997. Sulfated polysaccharides from the eggjelly layer are species-specific inducers of acrosomal reaction in sperms of sea urchins. J Biol Chem 272:6965-6971.
2. Alves AP, Mulloy B, Moy GW, Vacquier VD, Mourao PA. 1998. Females of the sea urchin Strongylocentrotus purpuratus differ in the structures of their egg jelly sulfated fucans. Glycobiology 8:939-946.
3. Bedford JM. 1977. Sperm/egg interaction: The specificity of human spermatozoa. Anat Rec 188:477-487.
4. Bedford JM. 1981. Why mammalian gametes don't mix. Nature 291:286-288.
5. Biermann CH, Marks JA, Vilela-Silva AC, Castro MO, Mourao PA. 2004. Carbohydrate-based species recognition in sea urchin fertilization: Another avenue for speciation? Evol Dev 6:353-361.
6. Bleil JD, Wassarman PM. 1980. Mammalian sperm-egg interaction: Identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20:873-882.
7. Bleil JD, Wassarman PM. 1986. Autoradiographic visualization of the mouse egg's sperm receptor bound to sperm. J Cell Biol 102:1363-1371.
8. Brackett BG, Bousquet D, Boice ML, Donawick WJ, Evans JF, Dressel MA. 1982. Normal development following in vitro fertilization in the cow. Biol Reprod 27:147-158.
9. 2+ fluctuations in sperm physiology. Int Rev Cytol 243:79-172.
10. Dean J. 2004. Reassessing the molecular biology of sperm-egg recognition with mouse genetics. Bioessays 26:29-38.
11. Fleming AD, Yanagimachi R, Yanagimachi H. 1981. Spermatozoa of the Atlantic bottlenosed dolphin, Tursiops truncatus. J Reprod Fertil 63:509-514.
12. Florman HM, Wassarman PM. 1985. O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell 41:313-324.
13. Florman HM, Bechtol KB, Wassarman PM. 1984. Enzymatic dissection of the functions of the mouse egg's receptor function for sperm. Dev Biol 106:243-255.
14. Gao B, Klein LE, Britten RJ, Davidson EH. 1986. Sequence of mRNA coding for bindin, a species-specific sea urchin sperm protein required for fertilization. Proc Natl Acad Sci USA 83:8634-8638.
15. Glabe CG, Vacquier VD. 1977. Species specific agglutination of eggs by bindin isolated from sea urchin sperm. Nature 267:836-838.
16. Glabe CG, Vacquier VD. 1978. Egg surface glycoprotein receptor for sea urchin sperm bindin. Proc Natl Acad Sci USA 75:881-885.
17. Glabe CG, Grabel LB, Vacquier VD, Rosen SD. 1982. Carbohydrate specificity of sea urchin sperm bindin: A cell surface lectin mediating sperm-egg adhesion. J Cell Biol 94:123-128.
18. Gunaratne HM, Yamagaki T, Matsumoto M, Hoshi M. 2003. Biochemical characterization of inner sugar chains of acrosome reaction-inducing substance in jelly coat of starfish eggs. Glycobiology 13:567-580.
19. Gwatkin RB, Williams DT. 1977. Receptor activity of the hamster and mouse solubilized zona pellucida before and after the zona reaction. J Reprod Fertil 49:55-59.
20. Hanada A, Chang MC. 1972. Penetration of zone-free eggs by spermatozoa of different species. Biol Reprod 6:300-309.
21. Hanada A, Chang MC. 1976a. In-vitro fertilization of hamster eggs in different media and the stimulating effect of heterologous and homologous spermatozoa. J Reprod Fertil 46:105-114.
22. Hanada A, Chang MC. 1976b. Penetration of hamster and rabbit zona-free eggs by rat and mouse spermatozoa with special reference to sperm capacitation. J Reprod Fertil 46:239-241.
23. Hanada A, Chang MC. 1978. Penetration of the zona-free or intact eggs by foreign spermatozoa and the fertilization of deer mouse eggs in vitro. J Exp Zool 203:277-285.
24. Hill KL, L'Hernault SW. 2001. Analyses of reproductive interactions that occur after heterospecific matings within the genus Caenorhabditis. Dev Biol 232:105-114.
25. Hirohashi N, Vacquier VD. 2002a. Egg sialoglycans increase intracellular pH and potentiate the acrosome reaction of sea urchin sperm. J Biol Chem 277:8041-8047.
26. 2+ channels involved in triggering the sea urchin sperm acrosome reaction. J Biol Chem 277:1182-1189.
27. Hirohashi N, Vilela-Silva AC, Mourao PA, Vacquier VD. 2002. Structural requirements for species-specific induction of the sperm acrosome reaction by sea urchin egg sulfated fucan. Biochem Biophys Res Commun 298:403-407.
28. Hoodbhoy T, Joshi S, Boja ES, Williams SA, Stanley P, Dean J. 2005. Human sperm do not bind to rat zonae pellucidae despite the presence of four homologous glycoproteins. J Biol Chem 280:12721-12731.
29. Hoshi T, Zagotta WN, Aldrich RW. 1990. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science 250:533-538.
30. Hoshi M, Okinaga T, Kontani K, Araki T, Chiba K. 1991. Acrosome reaction-inducing glycoconjugate in the jelly coat of starfish eggs. In: Baccetti B, editor. Comparative Spermatology 20 Years After. New York: Raven Press, pp 175-180.
31. Hoshi M, Nishigaki T, Ushiyama A, Okinaga T, Chiba K, Matsumoto M. 1994. Egg-jelly signal molecules for triggering the acrosome reaction in starfish spermatozoa. Int J Dev Biol 38:167-174.
32. Hoshi M, Kawamura M, Maruyama Y, Yoshida E, Nishigaki T, Ikeda M, Ogiso M, Moriyama Y, Matsumoto M. 1999. How does the jelly coat of starfish eggs trigger the acrosome reaction in homologous sperm. In: Gagnon C, editor. The Male Gamete: From Basic Science to Clinical Applications. Vienna, IL: Cache River Press, pp 119-125.
33. Imai H, Niwa K, Iritani A. 1977. Penetration in vitro of zona-free hamster eggs by ejaculated boar spermatozoa. J Reprod Fertil 51:495-497.
34. Johnston DS, Wright WW, Shaper JH, Hokke CH, Van den Eijnden DH, Joziasse DH. 1998. Murine sperm-zona binding, a fucosyl residue is required for a high affinity sperm-binding ligand. J Biol Chem 273:1888-1895.
35. Kamei N, Glabe CG. 2003. The species-specific egg receptor for sea urchin sperm adhesion is EBR1, a novel ADAMTS protein. Genes Dev 17:2502-2507.
36. Kim CI, Niwa K, Imai H, Iritani A. 1980. Penetration of zona-free hamster eggs in vitro by goat spermatozoa preincubated in the reproductive tract isolated from a maturing gilt. J Exp Zool 213:181-183.
37. Koyota S, Wimalasiri KM, Hoshi M. 1997. Structure of the main saccharide chain in the acrosome reaction-inducing substance of the starfish, Asterias amurensis. J Biol Chem 272:10372-10376.
38. Kresge N, Vacquier VD, Stout CD. 2001a. Abalone lysin: The dissolving and evolving sperm protein. Bioessays 23:95-103.
39. Kresge N, Vacquier VD, Stout CD. 2001b. The crystal structure of a fusagenic sperm protein reveals extreme surface properties. Biochemistry 40:5407-5413.
40. Lee YH, Ota T, Vacquier VD. 1995. Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Mol Biol Evol 12:231-238.
41. Litscher ES, Juntunen K, Seppo A, Penttila L, Niemela R, Renkonen O, Wassarman PM. 1995. Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro. Biochemistry 34:4662-4669.
42. Lopez A, Miraglia SJ, Glabe CG. 1993. Structure/function analysis of the sea urchin sperm adhesive protein bindin. Dev Biol 156:24-33.
43. Lyon JD, Vacquier VD. 1999. Interspecies chimeric sperm lysins identify regions mediating species-specific recognition of the abalone egg vitelline envelope. Dev Biol 214:151-159.
44. Mah SA, Swanson WJ, Vacquier VD. 2005. Positive selection in the carbohydrate recognition domains of sea urchin sperm receptor for egg jelly (suREJ) proteins. Mol Biol Evol 22:533-541.
45. Matsumoto M, Ikeda M, Hoshi M. 2000. Species-specificity of the acrosome reaction in starfish. Zygote 8:S62.
46. Metz EC, Palumbi SR. 1996. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol Biol Evol 13:397-406.
47. Metz EC, Gomez-Gutierrez G, Vacquier VD. 1998. Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia. Mol Biol Evol 15:185-195.
48. Miller DJ, Macek MB, Shur BD. 1992. Complementarity between sperm surface b-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357:589-593.
49. Mortillo S, Wassarman PM. 1991. Differential binding of gold-labeled zona pellucida glycoproteins mZP2 and mZP3 to mouse sperm membrane compartments. Development 113:141-149.
50. Moy GW, Mendoza LM, Schulz JR, Swanson WJ, Glabe CG, Vacquier VD. 1996. The sea urchin sperm receptor for egg jelly is a modular protein with extensive homology to the human polycystic kidney disease protein, PKD1. J Cell Biol 133:809-817.
51. Mulloy B, Ribeiro AC, Alves AP, Vieira RP, Mourao PA. 1994. Sulfated fucans from echinoderms have a regular tetrasaccharide repeating unit denned by specific patterns of sulfation at the 0-2 and 0-4 positions. J Biol Chem 269:22113-22123.
52. 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.
53. Neill AT, Vacquier VD. 2004. Ligands and receptors mediating signal transduction in sea urchin spermatozoa. Reproduction 127:141-149.
54. Neill AT, Moy GW, Vacquier VD. 2004. Polycystin-2 associates with the polycystin-1 homolog, suREJ3, and localizes to the acrosomal region of sea urchin spermatozoa. Mol Reprod Dev 67:472-477.
55. Nishigaki T, Chiba K, Miki W, Hoshi M. 1996. Structure and function of asterosaps, sperm-activating peptides from the jelly coat of starfish eggs. Zygote 4:237-245.
56. Nishiyama I, Matsui T, Hoshi M. 1987a. Purification of Co-ARIS, a cofactor for acrosome reaction-inducing substance, from the eggjelly of starfish. Dev Growth Differ 29:161-169.
57. Ohlendieck K, Dhume ST, Partin JS, Lennarz WJ. 1993. The sea urchin egg receptor for sperm: Isolation and characterization of the intact, biologically active receptor. J Cell Biol 122:887-895.
58. Patil S, Totey S. 2003. Developmental failure of hybrid embryos generated by in vitro fertilization of water buffalo (Bubalus bubalis) oocyte with bovine spermatozoa. Mol Reprod Dev 64:360-368.
59. Peterson RN, Russel LD, Bundman D, Freund M. 1980. Sperm-egg interactions: Evidence for boar sperm plasma membrane receptors for porcine zona pellucida. Science 207:73-74.
60. Rankin TL, Tong ZB, Castle PE, Lee E, Gore-Langton R, Nelson LM, Dean J. 1998. Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding. Development 125:2415-2424.
61. Rankin TL, Coleman JS, Epifano O, Hoodbhoy T, Turner SG, Castle PE, Lee E, Gore-Langton R, Dean J. 2003. Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologs. Dev Cell 5:33-43.
62. Schmell ED, Gulyas BJ. 1980. Mammalian sperm-egg recognition and binding in vitro. I. Specificity of sperm interactions with live and fixed eggs in homologous and heterologous insemination of hamster, mouse, and guinea pig oocytes. Biol Reprod 23:1075-1085.
63. SeGall GK, Lennarz WJ. 1979. Chemical characterization of the component of the jelly coat from sea urchin eggs responsible for induction of the acrosome reaction. Dev Biol 71:33-48.
64. SeGall GK, Lennarz WJ. 1981. Jelly coat and induction of the acrosome reaction in echinoid sperm. Dev Biol 86:87-93.
65. Sinowatz F, Wessa E, Neumuller C, Palma G. 2003. On the species specificity of sperm binding and sperm penetration of the zona pellucida. Reprod Dornest Anim 38:141-146.
66. Snell WJ, White JM. 1996. The molecules of mammalian fertilization. Cell 85:629-637.
67. Suzuki N. 1990. Structure and function of sea urchin egg jelly molecules. Zoological Science 7:355-370.
68. Suzuki N, Yoshino K. 1992. The relationship between amino acid sequences of sperm-activating peptides and the taxonomy of echinoids. Comp Biochem Physiol B 102:679-690.
69. Swanson WJ, Vacquier VD. 1997. The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule. Proc Natl Acad Sci USA 94:6724-6729.
70. Swanson WJ, Vacquier VD. 1998. Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. Science 281:710-712.
71. Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nat Rev Genet 3:137-144.
72. Tilney LG, Hatano S, Ishikawa H, Mooseker MS. 1973. The polymerization of actin: Its role in the generation of the acrosomal process of certain echinoderm sperm. J Cell Biol 59:109-126.
73. Ulrich AS, Otter M, Glabe CG, Hoekstra D. 1998. Membrane fusion is induced by a distinct peptide sequence of the sea urchin fertilization protein bindin. J Biol Chem 273:16748-16755.
74. Ulrich AS, Tichelaar W, Forster G, Zschornig O, Weinkauf S, Meyer HW. 1999. Ultrastructural characterization of peptide-induced membrane fusion and peptide self-assembly in the lipid bilayer. Biophys J 77:829-841.
75. Ushiyama A, Araki T, Chiba K, Hoshi M. 1993. Specific binding of acrosome-reaction-inducing substance to the head of starfish spermatozoa. Zygote 1:121-127.
76. Uto N, Yoshimatsu N, Lopata A, Yanagimachi R. 1988. Zona-induced acrosome reaction of hamster spermatozoa. J Exp Zool 248:113-120.
77. Vacquier VD. 1998. Evolution of gamete recognition proteins. Science 281:1995-1998.
78. Vacquier VD, Moy GW. 1977. Isolation of bindin: The protein responsible for adhesion of sperm to sea urchin eggs. Proc Natl Acad Sci USA 74:2456-2460.
79. Vacquier VD, Moy GW. 1997. The fucose sulfate polymer of egg jelly binds to sperm REJ and is the inducer of the sea urchin sperm acrosome reaction. Dev Biol 192:125-135.
80. Vacquier VD, Swanson WJ, Hellberg ME. 1995. What have we learned about sea urchin sperm bindin? Development Growth and Differentiation 37:1-10.
81. Vilela-Silva AC, Alves AP, Valente AP, Vacquier VD, Mourao PA. 1999. Structure of the sulfated alpha-L-fucan from the eggjelly coat of the sea urchin Strongylocentrotus franciscanus: Patterns of preferential 2-O- and 4-O-sulfation determine sperm cell recognition. Glycobiology 9:927-933.
82. Vilela-Silva AC, Castro MO, Valente AP, Biermann CH, Mourao PA. 2002. Sulfated fucans from the egg jellies of the closely related sea urchins Strongylocentrotus droebachiensis and Strongylocentrotus pallidus ensure species-specific fertilization. J Biol Chem 277:379-387.
83. Ward CR, Kopf GS. 1993. Molecular events mediating sperm activation. Dev Biol 158:9-34.
84. Wassarman PM. 1987. Early events in mammalian fertilization. Annu Rev Cell Biol 3:109-142.
85. Wassarman PM. 1988. Fertilization in mammals. Sci Am 259:78-84.
86. Wassarman PM. 1990. Profile of a mammalian sperm receptor. Development 108:1-17.
87. Wassarman PM. 1999. Mammalian fertilization: Molecular aspects of gamete adhesion, exocytosis, and fusion. Cell 96:175-183.
88. Wassarman PM. 2002. Sperm receptors and fertilization in mammals. Mt Sinai J Med 69:148-155.
89. Wassarman PM. 2005. Contribution of mouse egg zona pellucida glycoproteins to gamete recognition during fertilization. J Cell Physiol 204:388-391.
90. Wassarman PM, Jovine L, Qi H, Williams Z, Darie C, Litscher ES. 2005. Recent aspects of mammalian fertilization research. Mol Cell Endocrinol 234:95-103.
91. Yanagimachi R. 1994. Mammalian fertilization. In: Knobil E, Neill JD, editors. Physiology of Reproduction, 2nd edn. New York: Raven Press, pp A189-A317.
92. Yanagimachi R, Noda YD. 1972. Acrosome loss in fertilizing mammalian spermatozoa: A rebuttal of criticism. J Ultrastruct Res 39:217-221.
93. Yanagimachi R, Phillips DM. 1984. The status of acrosomal caps of hamster spermatozoa immediately before fertilization in vivo. Gamete Res 9:1-19.
94. Yanagimachi R, Winkelhake J, Nicolson GL. 1976. Immunological block to mammalian fertilization: Survival and organ distribution of immunoglobulin which inhibits fertilization in vivo. Proc Natl Acad Sci USA 73:2405-2408.
95. Yang Z, Swanson WJ, Vacquier VD. 2000. Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites. Mol Biol Evol 17:1446-1455.
96. Zigler KS, McCartney MA, Levitan DR, Lessios HA. 2005. Sea urchin bindin divergence predicts gamete compatibility. Evolution Int J Org Evolution 59:2399-2404.