Mechanism of fertilization: A modern view

Experimental Animals

Volumn 63, Issue 4, 2014, Pages 357-365

  Okabe, Masaru ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Acrosome reaction; Fertilization; Gene manipulated animals; Live imaging; Sperm egg fusion

Indexed keywords

CD9 ANTIGEN; FERTILIN; LYSOSOME ENZYME; MICRORNA; MYOGENIC FACTOR; MYOGENIC FACTOR 4; UNCLASSIFIED DRUG;

ACROSOME REACTION; CELL FUSION; EGG; FERTILIZATION; GENE DISRUPTION; HUMAN; IMAGING; NONHUMAN; PHENOTYPE; REVIEW; SPERM; SPERMATOZOON MIGRATION; TRANSGENIC ANIMAL; ZONA PELLUCIDA; ANIMAL; FEMALE; FERTILITY; FERTILIZATION IN VITRO; MALE; PHYSIOLOGY;

ANIMALIA;

ACROSOME REACTION; ANIMALS; ANIMALS, GENETICALLY MODIFIED; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; MALE; SPERM-OVUM INTERACTIONS;

EID: 84908347068     PISSN: 13411357     EISSN: None     Source Type: Journal    
DOI: 10.1538/expanim.14-0026     Document Type: Review

References (60)

1. Almeida, E.A., Huovila, A.P., Sutherland, A.E., Stephens, L.E., Calarco, P.G., Shaw, L.M., Mercurio, A.M., Sonnen-berg, A., Primakoff, P., Myles, D.G., and White, J.M. 1995. Mouse egg integrin alpha 6 beta 1 functions as a sperm receptor. Cell 81: 1095–1104.
2. Baba, D., Kashiwabara, S., Honda, A., Yamagata, K., Wu, Q., Ikawa, M., Okabe, M., and Baba, T. 2002. Mouse sperm lacking cell surface hyaluronidase PH-20 can pass through the layer of cumulus cells and fertilize the egg. J. Biol. Chem. 277: 30310–30314.
3. Baba, T., Azuma, S., Kashiwabara, S., and 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.
4. Baibakov, B., Gauthier, L., Talbot, P., Rankin, T.L., and Dean, J. 2007. Sperm binding to the zona pellucida is not sufficient to induce acrosome exocytosis. Development 134: 933–943.
5. Bianchi, E., Doe, B., Goulding, D., and Wright, G.J. 2014. Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508: 483–487.
6. Bleil, J.D. and Wassarman, P.M. 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.
7. Blobel, C.P., Wolfsberg, T.G., Turck, C.W., Myles, D.G., Pri-makoff, P., and White, J.M. 1992. A potential fusion peptide and an integrin ligand domain in a protein active in sperm-egg fusion. Nature 356: 248–252.
8. Chen, M.S., Tung, K.S., Coonrod, S.A., Takahashi, Y., Big-ler, D., Chang, A., Yamashita, Y., Kincade, P.W., Herr, J.C., and White, J.M. 1999. Role of the integrin-associated protein CD9 in binding between sperm ADAM 2 and the egg integ-rin alpha6beta1: implications for murine fertilization. Proc. Natl. Acad. Sci. USA 96: 11830–11835.
9. Cho, C., Bunch, D.O., Faure, J.E., Goulding, E.H., Eddy, E.M., Primakoff, P., and Myles, D.G. 1998. Fertilization defects in sperm from mice lacking fertilin beta. Science 281: 1857–1859.
10. Da Ros, V.G., Maldera, J.A., Willis, W.D., Cohen, D.J., Goulding, E.H., Gelman, D.M., Rubinstein, M., Eddy, E.M., and Cuasnicu, P.S. 2008. Impaired sperm fertilizing ability in mice lacking Cysteine-RIch Secretory Protein 1 (CRISP1). Dev. Biol. 320: 12–18.
11. Ensslin, M.A. and Shur, B.D. 2003. Identification of mouse sperm SED1, a bimotif EGF repeat and discoidin-domain protein involved in sperm-egg binding. Cell 114: 405–417.
12. Florman, H.M. and Ducibella, T. 2006. Fertilization in mammals. Knbil and Neill’s Physiology of Reproduction 1 (3rd ed): 55–112.
13. Fujihara, Y., Okabe, M., and Ikawa, M. 2014. GPI-anchored protein complex, LY6K/TEX101, is required for sperm migration into the oviduct and male fertility in mice. Biol Re-prod. 90: 60.
14. Fujihara, Y., Tokuhiro, K., Muro, Y., Kondoh, G., Araki, Y., Ikawa, M., and Okabe, M. 2013. Expression of TEX101, regulated by aCe, is essential for the production of fertile mouse spermatozoa. Proc. Natl. Acad. Sci. USA 110: 8111–8116.
15. Gahlay, G., Gauthier, L., Baibakov, B., Epifano, O., and Dean, J. 2010. Gamete recognition in mice depends on the cleavage status of an egg’s zona pellucida protein. Science 329: 216–219.
16. Gong, X., Dubois, D.H., Miller, D.J., and Shur, B.D. 1995. Activation of a G protein complex by aggregation of be-ta-1,4-galactosyltransferase on the surface of sperm. Science 269: 1718–1721.
17. Hagaman, J.R., Moyer, J.S., Bachman, E.S., Sibony, M., Magyar, P.L., Welch, J.E., Smithies, O., Krege, J.H., and O’Brien, D.A. 1998. Angiotensin-converting enzyme and male fertility. Proc. Natl. Acad. Sci. USA 95: 2552–2557.
18. Hanayama, R., Tanaka, M., Miyasaka, K., Aozasa, K., Koike, M., Uchiyama, Y., and Nagata, S. 2004. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-defcient mice. Science 304: 1147–1150.
19. Hartmann, J.F., Gwatkin, R.B., and Hutchison, C.F. 1972. Early contact interactions between mammalian gametes in vitro: evidence that the vitellus influences adherence between sperm and zona pellucida. Proc. Natl. Acad. Sci. USA 69: 2767–2769.
20. Hasuwa, H., Muro, Y., Ikawa, M., Kato, N., Tsujimoto, Y., and Okabe, M. 2010. Transgenic mouse sperm that have green acrosome and red mitochondria allow visualization of sperm and their acrosome reaction in vivo. Exp. Anim. 59: 105–107.
21. He, Z.Y., Brakebusch, C., Fässler, R., Kreidberg, J.A., Pri-makoff, P., and Myles, D.G. 2003. None of the integrins known to be present on the mouse egg or to be aDaM receptors are essential for sperm-egg binding and fusion. Dev. Biol. 254: 226–237.
22. Hinsch, K.D., Hinsch, E., Meinecke, B., Töpfer-Petersen, E., Pfsterer, S., and Schill, W.B. 1994. Identification of mouse ZP3 protein in mammalian oocytes with antisera against synthetic ZP3 peptides. Biol. Reprod. 51: 193–204.
23. Ikawa, M., Inoue, N., Benham, A.M., and Okabe, M. 2010. Fertilization: a sperm’s journey to and interaction with the oocyte. J. Clin. Invest. 120: 984–994.
24. Ikawa, M., Wada, I., Kominami, K., Watanabe, D., Toshi-mori, K., Nishimune, Y., and Okabe, M. 1997. The putative chaperone calmegin is required for sperm fertility. Nature 387: 607–611.
25. Ikawa, M., Yamaguchi, R., Inoue, N., and Okabe, M. 2008. Haploid-specific chaperone calspelin (Calr3) is required for sperm fertility. Biol. Reprod. 578. 78, 190.
26. Inoue, N., Ikawa, M., Isotani, A., and Okabe, M. 2005. The immunoglobulin super family protein Izumo is required for sperm to fuse with eggs. Nature 434: 234–238.
27. Inoue, N., Ikawa, M., Nakanishi, T., Matsumoto, M., Nomu-ra, M., Seya, T., and Okabe, M. 2003. Disruption of mouse CD46 causes an accelerated spontaneous acrosome reaction in sperm. Mol. Cell. Biol. 23: 2614–2622.
28. Inoue, N., Kasahara, T., Ikawa, M., and Okabe, M. 2010. Identification and disruption of sperm-specific angioten-sin converting enzyme-3 (aCe3) in mouse. PLoS ONE 5: e10301.
29. Inoue, N., Nishikawa, T., Ikawa, M., and Okabe, M. 2012. Tetraspanin-interacting protein IGSF8 is dispensable for mouse fertility. Fertil. Steril. 98: 465–470.
30. Inoue, N., Satouh, Y., Ikawa, M., Okabe, M., and Yanagi-machi, R. 2011. Acrosome-reacted mouse spermatozoa recovered from the perivitelline space can fertilize other eggs. Proc. Natl. Acad. Sci. USA 108: 20008–20011.
31. Jin, M., Fujiwara, E., Kakiuchi, Y., Okabe, M., Satouh, Y., Baba, S.A., Chiba, K., and Hirohashi, N. 2011. Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc. Natl. Acad. Sci. USA 108: 4892–4896.
32. Kaji, K., Oda, S., Shikano, T., Ohnuki, T., Uematsu, Y., Sak-agami, J., Tada, N., Miyazaki, S., and Kudo, A. 2000. The gamete fusion process is defective in eggs of Cd9-defcient mice. Nat. Genet. 24: 279–282.
33. Kim, E., Yamashita, M., Nakanishi, T., Park, K.E., Kimura, M., Kashiwabara, S., and Baba, T. 2006. Mouse sperm lacking ADAM1b/ADAM2 fertilin can fuse with the egg plasma membrane and effect fertilization. J. Biol. Chem. 281: 5634–5639.
34. Krutskikh, A., Poliandri, A., Cabrera-Sharp, V., Dacheux, J.L., Poutanen, M., and Huhtaniemi, I. 2012 Epididymal protein Rnase10 is required for post-testicular sperm maturation and male fertility. FASEB J. 26:4198–4209.
35. Le Naour, F., Rubinstein, E., Jasmin, C., Prenant, M., and Boucheix, C. 2000. Severely reduced female fertility in CD9-defcient mice. Science 287: 319–321.
36. Lu, Q. and Shur, B.D. 1997. Sperm from beta 1,4-galactos-yltransferase-null mice are refractory to ZP3-induced acro-some reactions and penetrate the zona pellucida poorly. Development 124: 4121–4131.
37. Marcello, M.R., Jia, W., Leary, J.A., Moore, K.L., and Evans, J.P. 2011. Lack of tyrosylprotein sulfotransferase-2 activity results in altered sperm-egg interactions and loss of aDaM3 and aDaM6 in epididymal sperm. J. Biol. Chem. 286: 13060–13070.
38. Miller, B.J., Georges-Labouesse, E., Primakoff, P., and Myl-es, D.G. 2000. Normal fertilization occurs with eggs lacking the integrin alpha6beta1 and is CD9-dependent. J. Cell Biol. 149: 1289–1296.
39. Miyado, K., Yamada, G., Yamada, S., Hasuwa, H., Naka-mura, Y., Ryu, F., Suzuki, K., Kosai, K., Inoue, K., Ogura, A., Okabe, M., and Mekada, E. 2000. Requirement of CD9 on the egg plasma membrane for fertilization. Science 287: 321–324.
40. Muro, Y., Buffone, M.G., Okabe, M., and Gerton, G.L. 2012. Function of the acrosomal matrix: zona pellucida 3 receptor (ZP3R/sp56) is not essential for mouse fertilization. Biol. Reprod. 86: 1–6.
41. Nakanishi, T., Ikawa, M., Yamada, S., Parvinen, M., Baba, T., Nishimune, Y., and Okabe, M. 1999. Real-time observation of acrosomal dispersal from mouse sperm using GFP as a marker protein. FEBS Lett. 449: 277–283.
42. Nishimura, H., Kim, E., Nakanishi, T., and Baba, T. 2004. Possible function of the ADAM1a/ADAM2 Fertilin complex in the appearance of aDaM3 on the sperm surface. J. Biol. Chem. 279: 34957–34962.
43. Okabe, M. 2013. The cell biology of mammalian fertilization. Development 140: 4471–4479.
44. Olson, E.N., Arnold, H.H., Rigby, P.W., and Wold, B.J. 1996. Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell 85: 1–4.
45. Osokine, I., Hsu, R., Loeb, G.B., and McManus, M.T. 2008. Unintentional miRNa ablation is a risk factor in gene knockout studies: a short report. PLoS Genet. 4: e34.
46. Primakoff, P. and Myles, D.G. 2002. Penetration, adhesion, and fusion in mammalian sperm-egg interaction. Science 296: 2183–2185.
47. Rossi, D., Cozzio, A., Flechsig, E., klein, M.A., Rülicke, T., Aguzzi, A., and Weissmann, C. 2001. Onset of ataxia and Purkinje cell loss in PrP null mice inversely correlated with Dpl level in brain. EMBO J. 20: 694–702.
48. Satouh, Y., Inoue, N., Ikawa, M., and Okabe, M. 2012. Visualization of the moment of mouse sperm-egg fusion and dynamic localization of IZUMO1. J. Cell Sci. 125: 4985–4990.
49. Shamsadin, R., Adham, I.M., Nayernia, K., Heinlein, U.A., Oberwinkler, H., and Engel, W. 1999. Male mice deficient for germ-cell cyritestin are infertile. Biol. Reprod. 61: 1445–1451.
50. Shen, C., Kuang, Y., Liu, J., Feng, J., Chen, X., Wu, W., Chi, J., Tang, L., Wang, Y., Fei, J., and Wang, Z. 2013. Prss37 is required for male fertility in the mouse. Biol. Reprod. 88: 123.
51. Sutton, K.A., Jungnickel, M.K., and Florman, H.M. 2008. A polycystin-1 controls postcopulatory reproductive selection in mice. Proc. Natl. Acad. Sci. USA 105: 8661–8666.
52. Tardif, S., Wilson, M.D., Wagner, R., Hunt, P., Gertsenstein, M., Nagy, A., Lobe, C., Koop, B.F., and Hardy, D.M. 2010. Zonadhesin is essential for species specifcity of sperm adhesion to the egg zona pellucida. J. Biol. Chem. 285: 24863–24870.
53. Tokuhiro, K., Ikawa, M., Benham, A.M., and Okabe, M. 2012. Protein disulfide isomerase homolog PDILT is required for quality control of sperm membrane protein aDaM3 and male fertility [corrected]. Proc. Natl. Acad. Sci. USA 109: 3850–3855.
54. Valdivia, M., Sillerico, T., De Ioannes, A. and Barros, C. 1999. Proteolytic activity of rabbit perivitelline spermato-zoa. Zygote 7: 143–149.
55. Wassarman, P.M., and Litscher, E.S. 2008. Mammalian fertilization: the egg’s multifunctional zona pellucida. Int. J. Dev. Biol. 52: 665–676.
56. Yamaguchi, R., Fujihara, Y., Ikawa, M., and Okabe, M. 2012. Mice expressing aberrant sperm-specific protein PMIS2 produce normal-looking but fertilization-incompetent spermatozoa. Mol. Biol. Cell 23: 2671–2679.
57. Yamaguchi, R., Muro, Y., Isotani, A., Tokuhiro, K., Takumi, K., Adham, I., Ikawa, M., and Okabe, M. 2009. Disruption of aDaM3 impairs the migration of sperm into oviduct in mouse. Biol. Reprod. 81: 142–146.
58. Yamaguchi, R., Yamagata, K., Ikawa, M., Moss, S.B., and Okabe, M. 2006. Aberrant distribution of ADAM3 in sperm from both angiotensin-converting enzyme (ace)- and calmegin (Clgn)-defcient mice. Biol. Reprod. 75: 760–766.
59. Yanagimachi, R. 1994 Mammalian Fertilization (Raven Press, LTD., New York) second Ed pp 189–317.
60. Yanagimachi, R. and Chang, M.C. 1963. Fertilization of hamster eggs in vitro. Nature 200: 281–282.