Acrosome reaction in the cumulus oophorus revisited: involvement of a novel sperm-released factor NYD-SP8

Abstract

Fertilization is a process involving multiple steps that lead to the final fusion of one sperm and the oocyte to form the zygote. One of the steps, acrosome reaction (AR), is an exocytosis process, during which the outer acrosome membrane fuses with the inner sperm membrane, leading to the release of acrosome enzymes that facilitate sperm penetration of the egg investments. Though AR has been investigated for decades, the initial steps of AR in vivo, however, remain largely unknown. A well elucidated model holds the view that AR occurs on the surface of the zona pellucida (ZP), which is triggered by binding of sperm with one of the ZP glycosylated protein, ZP3. However, this model fails to explain the large number of ‘falsely’ acrosome-reacted sperms found within the cumulus layer in many species examined. With the emerging evidence of cross-talk between sperm and cumulus cells, the potential significance of AR in the cumulus oophorus, the outer layer of the egg, has been gradually revealed. Here we review the acrosome status within the cumulus layer, the cross-talk between sperm and cumulus cells with the involvement of a novel sperm-released factor, NYD-SP8, and re-evaluate the importance and physiological significance of the AR in the cumulus in fertilization.

Keywords

sperm / acrosome reaction / cumulus / NYP-SP8 / progesterone

References

[1] Anderson, R.A. Jr, Feathergill, K.A., Rawlins, R.G., Mack, S.R., and Zaneveld, L.J. (1995). Atrial natriuretic peptide: a chemoattractant of human spermatozoa by a guanylate cyclase-dependent pathway. Mol Reprod Dev 40, 371-378 .7772348
[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 .12065596
[3] Bedford, J.M. (1968). Ultrastructural changes in the sperm head during fertilization in the rabbit. Am J Anat 123, 329-358 .5750218
[4] Bedford, J.M. (1972). An electron microscopic study of sperm penetration into the rabbit egg after natural mating. Am J Anat 133, 213-254 .5009247
[5] Bleil, J.D., and Wassarman, P.M. (1980). Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20, 873-882 .7418009
[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 .6402397
[7] Breitbart, H., Rotman, T., Rubinstein, S., and Etkovitz, N. (2010). Role and regulation of PI3K in sperm capacitation and the acrosome reaction. Mol Cell Endocrinol 314, 234-238 .19560510
[8] Brucker, C., and Lipford, G.B. (1995). The human sperm acrosome reaction: physiology and regulatory mechanisms. An update. Hum Reprod Update 1, 51-62 .9080206
[9] Carrell, D.T., Middleton, R.G., Peterson, C.M., Jones, K.P., and Urry, R.L. (1993). Role of the cumulus in the selection of morphologically normal sperm and induction of the acrosome reaction during human in vitro fertilization. Arch Androl 31, 133-137 .8215693
[10] Cross, N.L., Morales, P., Overstreet, J.W., and Hanson, F.W. (1988). Induction of acrosome reactions by the human zona pellucida. Biol Reprod 38, 235-244 .3365471
[11] Crozet, N. (1984b). Ultrastructural aspects of in vivo fertilization in the cow. Gamete Res 10, 241-251 .
[12] Crozet, N., and Dumont, M. (1984a). The site of the acrosome reaction during in vivo penetration of the sheep oocyte. Gamete Res 10, 97-105 .
[13] Cummins, J.M., and Yanagimachi, R. (1982). Sperm-egg ratios and the site of the acrosome reaction during in vivo fertilization in the hamster. Gamete Res 5, 239-256 .
[14] Fukami, K., Nakao, K., Inoue, T., Kataoka, Y., Kurokawa, M., Fissore, R.A., Nakamura, K., Katsuki, M., Mikoshiba, K., Yoshida, N., (2001). Requirement of phospholipase Cdelta4 for the zona pellucida-induced acrosome reaction. Science 292, 920-923 .11340203
[15] Gil, P.I., Guidobaldi, H.A., Teves, M.E., U?ates, D.R., Sanchez, R., and Giojalas, L.C. (2008). Chemotactic response of frozen-thawed bovine spermatozoa towards follicular fluid. Anim Reprod Sci 108, 236-246 .17889460
[16] Guidobaldi, H.A., Teves, M.E., U?ates, D.R., Anastasía, A., and Giojalas, L.C. (2008). Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex. PLoS One 3, e3040.18725941
[17] Gupta, S.K., Bansal, P., Ganguly, A., Bhandari, B., and Chakrabarti, K. (2009). Human zona pellucida glycoproteins: functional relevance during fertilization. J Reprod Immunol 83, 50-55 .19850354
[18] Gwatkin, R.B.L., Carter, H.W., and Patterson, H. (1976). Association of mammalian sperm with the cumulus cells and the zona pellucida studied by scanning electron microscopy. In: Scanning Electron Microscopy, Proceedings of Workshopon SEM in Reproductive Biology, Part 2 . Johari, O. ed. Chicago: IIT Res Inst. 379-384 .
[19] Hardy, D.M., Oda, M.N., Friend, D.S., and Huang, T.T. Jr. (1991). A mechanism for differential release of acrosomal enzymes during the acrosome reaction. Biochem J 275, 759-766 .1903927
[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 .20224175
[21] Hong, S.J., Chiu, P.C., Lee, K.F., Tse, J.Y., Ho, P.C., and Yeung, W.S. (2009). Cumulus cells and their extracellular matrix affect the quality of the spermatozoa penetrating the cumulus mass. Fertil Steril 92, 971-978 .18930198
[22] 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 .20364096
[23] Jeon, B.G., Moon, J.S., Kim, K.C., Lee, H.J., Choe, S.Y., and Rho, G.J. (2001). Follicular fluid enhances sperm attraction and its motility in human. J Assist Reprod Genet 18, 407-412 .11599459
[24] Jezová, M., Scsuková, S., Nagyová, E., Vranová, J., Procházka, R., and Kolena, J. (2001). Effect of intraovarian factors on porcine follicular cells: cumulus expansion, granulosa and cumulus cell progesterone production. Anim Reprod Sci 65, 115-126 .11182513
[25] Kim, E., Baba, D., Kimura, M., Yamashita, M., Kashiwabara, S., and Baba, T. (2005). Identification of a hyaluronidase, Hyal5, involved in penetration of mouse sperm through cumulus mass. Proc Natl Acad Sci U S A 102, 18028-18033 .16330764
[26] Kim, K.S., Foster, J.A., and Gerton, G.L. (2001). Differential release of guinea pig sperm acrosomal components during exocytosis. Biol Reprod 64, 148-156 .11133669
[27] Kim, K.S., and Gerton, G.L. (2003). Differential release of soluble and matrix components: evidence for intermediate states of secretion during spontaneous acrosomal exocytosis in mouse sperm. Dev Biol 264, 141-152 .14623237
[28] Kimura, M., Kim, E., Kang, W., Yamashita, M., Saigo, M., Yamazaki, T., Nakanishi, T., Kashiwabara, S., and Baba, T. (2009). Functional roles of mouse sperm hyaluronidases, HYAL5 and SPAM1, in fertilization. Biol Reprod 81, 939-947 .19605784
[29] Lee, M.A., Check, J.H., and Kopf, G.S. (1992). A guanine nucleotide-binding regulatory protein in human sperm mediates acrosomal exocytosis induced by the human zona pellucida. Mol Reprod Dev 31, 78-86 .1562331
[30] Lin, Y., Mahan, K., Lathrop, W.F., Myles, D.G., and 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 .8195297
[31] Miller, D.J., Macek, M.B., and Shur, B.D. (1992). Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357, 589-593 .1608469
[32] 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 .10338148
[33] Nakanishi, T., Ikawa, M., Yamada, S., Toshimori, K., and Okabe, M. (2001). Alkalinization of acrosome measured by GFP as a pH indicator and its relation to sperm capacitation. Dev Biol 237, 222-231 .11518518
[34] O’Donnell, J.B. Jr, Hill, J.L., and Gross, D.J. (2004). Epidermal growth factor activates cytosolic [Ca²⁺] elevations and subsequent membrane permeabilization in mouse cumulus-oocyte complexes. Reproduction 127, 207-220 .15056787
[35] Oren-Benaroya, R., Orvieto, R., Gakamsky, A., Pinchasov, M., and Eisenbach, M. (2008). The sperm chemoattractant secreted from human cumulus cells is progesterone. Hum Reprod 23, 2339-2345 .18621752
[36] Osman, R.A., Andria, M.L., Jones, A.D., and Meizel, S. (1989). Steroid induced exocytosis: the human sperm acrosome reaction. Biochem Biophys Res Commun 160, 828-833 .2719699
[37] Pereda, J., and Coppo, M. (1985). An electron microscopic study of sperm penetration into the human egg investments. Anat Embryol (Berl) 173, 247-252 .4083525
[38] Rijsdijk, M., and Franken, D.R. (2007). Use of the capillary-cumulus oophorus model for evaluating the selection of spermatozoa. Fertil Steril 88, 1595-1602 .17448468
[39] Sliwa, L. (1993). Heparin as a chemoattractant for mouse spermatozoa. Arch Androl 31, 149-152 .8274040
[40] Sliwa, L. (1994). Chemotactic effect of hormones in mouse spermatozoa. Arch Androl 32, 83-88 .8166580
[41] Sliwa, L. (1995). Chemotaction of mouse spermatozoa induced by certain hormones. Arch Androl 35, 105-110 .8579470
[42] Sun, F., Bahat, A., Gakamsky, A., Girsh, E., Katz, N., Giojalas, L.C., Tur-Kaspa, I., and Eisenbach, M. (2005). Human sperm chemotaxis: both the oocyte and its surrounding cumulus cells secrete sperm chemoattractants. Hum Reprod 20, 761-767 .15591080
[43] Sutovsky, P.Sperm capacitation, the acrosome reaction and fertilization. (2010). In: Reproductive Endocrinology and Infertility: Integrating Modern Clinical and Laboratory Practice . Carrell, D.T. and Peterson, C.M., eds. New York: Springer Science Business Media. 389-421 .
[44] Talbot, P. (1985). Sperm penetration through oocyte investments in mammals. Am J Anat 174, 331-346 .4072945
[45] Tanii, I., Aradate, T., Matsuda, K., Komiya, A., and Fuse, H. (2011). PACAP-mediated sperm-cumulus cell interaction promotes fertilization. Reproduction 141, 163-171 . 21071464.
[46] Tesarík, J. (1985). Comparison of acrosome reaction-inducing activities of human cumulus oophorus, follicular fluid and ionophore A23187 in human sperm populations of proven fertilizing ability in vitro. J Reprod Fertil 74, 383-388 .3930710
[47] Thomas, P., and Meizel, S. (1989). Phosphatidylinositol 4,5-bisphosphate hydrolysis in human sperm stimulated with follicular fluid or progesterone is dependent upon Ca²⁺ influx. Biochem J 264, 539-546 .2557843
[48] Tulsiani, D.R.P., Abou-Haila, A., Loeser, C.R., and Pereira, B.M. (1998). The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization. Exp Cell Res 240, 151-164 .9596988
[49] van Duin, M., Polman, J.E.M., De Breet, I.T.M., van Ginneken, K., Bunschoten, H., Grootenhuis, A., Brindle, J., and Aitken, R.J. (1994). Recombinant human zona pellucida protein ZP3 produced by chinese hamster ovary cells induces the human sperm acrosome reaction and promotes sperm-egg fusion. Biol Reprod 51, 607-617 .7819440
[50] Villanueva-Díaz, C., Arias-Martínez, J., Bermejo-Martínez, L., and Vadillo-Ortega, F. (1995). Progesterone induces human sperm chemotaxis. Fertil Steril 64, 1183-1188 .7589674
[51] Wang, Y., Storeng, R., Dale, P.O., Abyholm, T., and Tanbo, T. (2001). Effects of follicular fluid and steroid hormones on chemotaxis and motility of human spermatozoa in vitro. Gynecol Endocrinol 15, 286-292 .11560102
[52] Witte, T.S., and Sch?fer-Somi, S. (2007). Involvement of cholesterol, calcium and progesterone in the induction of capacitation and acrosome reaction of mammalian spermatozoa. Anim Reprod Sci 102, 181-193 .17870257
[53] Yanagimachi, R. (1988). Mammalian fertilization. In: The Physiology of Reproduction , 1st edi. E.Knobil and J.D.Neil, eds. New York: Raven Press. 135-185 .
[54] Yanagimachi, R. (1994). Mammalian fertilization. In: The Physiology of Reproduction , 2nd edi. E.Knobil and J.D.Neil, eds. New York: Raven Press. 189-317 .
[55] Yin, L., Chung, C.M., Huo, R., Liu, H., Zhou, C., Xu, W., Zhu, H., Zhang, J., Shi, Q., Wong, H.Y., (2009). A sperm GPI-anchored protein elicits sperm-cumulus cross-talk leading to the acrosome reaction. Cell Mol Life Sci 66, 900-908 .19153666