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The diagnostic significance of the induced acrosome reaction

Published online by Cambridge University Press:  02 March 2009

Christopher J De Jonge
Christopher J De Jonge*
Affiliation:
University of Nebraska Medical Center, Omaha, Nebraska, USA
*
Christopher J De Jonge, Department of Obstetrics and Gynecology, University of Nebraska Medical Center, Omaha, NE 68198-3255, USA.
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Extract

In trying to discern potential causes of male infertility, little investigation has been done to determine if there is predictive value in assessing acrosome reaction inducibility of human spermatozoa for clinical interpretation and application. The purpose of this review is to outline what is currently known in terms of the diagnostic significance of the induced acrosome reaction and to discuss what might be anticipated for the future. In constructing this review, every effort has been made to provide a comprehensive literature review for the reader and a number of review articles have been cited to serve as sources for additional related material. Regarding the aforementioned, it is essential to qualify that, with the exception of the Section entitled: ‘General characteristics of capacitation and the acrosome reaction’, only characteristics, properties and areas relevant to human spermatozoa will be addressed. Thus, in total, this review will: (1) provide a general description of capacitation and the acrosome reaction; (2) briefly characterize the acrosome and its properties; (3) address the signalling mechanism(s) by which the acrosome reaction occurs; (4) outline various methods for detecting the acrosome reaction; (5) define in vitro culture conditions that facilitate the acrosome reaction; (6) define agents, i.e., biological and chemical, that induce the reaction; (7) discuss the association of the acrosome reaction with fertilization; (8) discuss the clinical implications of the induced acrosome reaction; (9) discuss the relevance of sperm function assays in general; and lastly, (10) discuss future application of acrosome reaction assessment for the clinical diagnosis of male infertility.

Type
Articles
Information
Reproductive Medicine Review , Volume 3 , Issue 3 , October 1994 , pp. 159 - 178
Copyright
Copyright © Cambridge University Press 1994

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References

1Chang, MC. Fertilizing capacity of spermatozoa deposited in fallopian tubes. Nature 1951; 168: 997–98.CrossRefGoogle ScholarPubMed
2Austin, CR. The ‘capacitation’ of the mammalian sperm. Nature 1952; 170: 326.CrossRefGoogle ScholarPubMed
3Austin, CR. Sperm maturation in the male and female genital tracts. In: Metz, CB, Monroy, A eds. Biology of fertilization. Volume 2. New York: Academic Press, 1985: 121–55.CrossRefGoogle Scholar
4Bedford, JM. Sperm capacitation and fertilization in mammals. Biol Reprod 1970; 2 (suppl): 128–58.CrossRefGoogle ScholarPubMed
5Bedford, JM, Cooper, GW. Membrane fusion events in fertilization of vertebrate eggs. In: Poste, G, Nicolson, GL eds. Membrane surface reviews (membrane fusion), Volume 5. Amsterdam: North-Holland, 1978: 65–125.Google Scholar
6Bedford, JM, Hoskins, DD. The mammalian spermatozoa: morphology, biochemistry and physiology. In: Lamming, GE ed. Physiology of reproduction, Volume 2. Edinburgh: Churchill Livingston, 1990: 379–658.Google Scholar
7Chang, MC. Meaning of sperm capacitation. J Androl 1984; 5: 45–50.CrossRefGoogle ScholarPubMed
8Clegg, ED. Mechanisms of mammalian sperm capacitation. In: Hartman, JF ed. Mechanism and control of animal fertilization. New York: Academic Press, 1983: 177–212.Google Scholar
9Davis, BK, Byrne, R, Bedigan, K. Studies on the mechanism of capacitation: albumin mediated changes in plasma membrane lipids during in vitro incubation of rat cells. Proc Natl Acad Sci USA 1980; 77: 387–97.CrossRefGoogle Scholar
10Drobnis, E. Capacitation and acrosome reaction. In: Scialli, AR, Zinaman, MJ eds. Reproductive toxicology and infertility. New York: McGraw-Hill, 1993; 77–132.Google Scholar
11Florman, HM, Babcock, DF. Progress toward understanding the molecular basis of capacitation. In: Wassarman, PM ed. Elements of mammalian fertilization. Volume 1. Boca Raton, Florida: CRC Press, 1991: 105–32.Google Scholar
12Fraser, LR. Requirements for successful mammalian sperm capacitatoin and fertilization. Arch Path Lab Med 1992; 116: 345–50.Google ScholarPubMed
13Hinrichsen-Kohane, AC, Hinrichsen, MJ, Schill, WB. Molecular events leading to fertilization. Andrologia 1984; 16: 321–41.CrossRefGoogle ScholarPubMed
14Langlais, J, Roberts, KD. A molecular membrane model of sperm capacitation and the acrosome reaction of mammalian spermatozoa. Gamete Res 1985; 12: 183–224.CrossRefGoogle Scholar
15O'Rand, MG. Changes in sperm surface properties correlated with capacitation. In: Fawcett, DW, Bedford, JM eds. The spermatozoa. Baltimore: Urban and Schwarzenberg, 1979: 195–204.Google Scholar
16O'Rand, MG. Modification of the sperm membrane during capacitation. Ann N Y Acad Sci 1982; 383: 392–404.CrossRefGoogle ScholarPubMed
17Rogers, BJ. Mammalian sperm capacitation and fertilization in vitro: a critique of methodology. Gamete Res 1978; 1: 165–223.CrossRefGoogle Scholar
18Rogers, BJ, Bentwood, BJ. Capacitation, acrosome reaction and fetilization. In: Zaneveld, LJD, Chatterton, RT eds. Biochemistry of mammalian fertilization. New York: Wiley, 1982: 203–30.Google Scholar
19Sidhu, KS, Guraya, SS. Cellular and molecular biology of capacitation and acrosome reaction in mammalian spermatozoa. Int Rev Cytol 1989; 188: 231–80.CrossRefGoogle Scholar
20Storey, BT. Sperm capacitation and the acrosome reaction. Ann N Y Acad Sci 1991; 637: 457–73.CrossRefGoogle ScholarPubMed
21Yanagimachi, R. Mammalian fertilization. In: Knobil, E, Neill, J eds. The physiology of reproduction, Volume 1. New York: Raven Press, 1994: 189–317.Google Scholar
22Zaneveld, LJD, De Jonge, CJ, Anderson, RA, Mack, SR. Human sperm capacitation and the acrosome reaction. Human Reprod 1991; 6: 1265–74.CrossRefGoogle ScholarPubMed
23Go, KJ, Wolf, DP. Albumin mediated changes in sperm sterol content during capacitation. Biol Reprod 1985; 32: 145–53.CrossRefGoogle ScholarPubMed
24JrAnderson, RA, Feathergill, KA, De Jonge, CJ, Mack, SR, Zaneveld, LJD. Facilitative effect of pulsed addition of dibutyryl cAMP on the acrosome reaction of noncapacitated spermatozoa. J Androl 1992; 13: 398–408.CrossRefGoogle ScholarPubMed
25Anderson, RA, Feathergill, KA, Drisdel, RC, Rawlins, RG, Mack, SR, Zaneveld, LJD. Atrial natriuretic peptide (ANP) as a stimulus of the human acrosome reaction and a component of ovarian follicular fluid: correlation of follicular ANP content with in vitro fertilization outcome. J Androl 1994; 15: 61–70.CrossRefGoogle Scholar
26Zaneveld, LJD, Anderson, RA, Mack, SR, De Jonge, CJ. Mechanism and control of the human sperm acrosome reaction. Human Reprod 1994; 8: 2006–2008.CrossRefGoogle Scholar
27Dinbar, BS, O'Rand, MG eds. A comparative overview of mammalian fertilization. New York: Plenum Press, 1991.CrossRefGoogle Scholar
28Kopf, GS, Gerton, GL. The mammalian sperm acrosome and the acrosome reaction. In: Wassarman, PM ed. Elements of mammalian fertilization. Volume 1. Boca Raton, Florida: CRC Press, 1991: 153–203.Google Scholar
29Meizel, S. The mammalian sperm acrosome reaction. A biochemical approach. In: Johnson, MH ed. Development in mammals. New York: North-Holland, 1978: 1–64.Google Scholar
30Meizel, S. Molecules that initiate or help stimulate the acrosome reaction by their interaction with the mammalian sperm surface. Am J Anat 1985; 174: 285–302.CrossRefGoogle ScholarPubMed
31Zaneveld, LJD, De Jonge, CJ. Mammalian sperm acrosomal enzymes and the acrosome reaction. In: Dunbar, BS, O'Rand, MG eds. A comparative overview of mammalian fertilization. New York: Plenum Press, 1991: 63–79.CrossRefGoogle Scholar
32De Jonge, CJ, Barratt, CLR, Radwanska, E, Cooke, ID. The acrosome reaction inducing effect of human follicular and oviductal fluid. J Androl 1993; 14: 359–05.CrossRefGoogle ScholarPubMed
33Tesarik, J. 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 1985; 74: 383–88.CrossRefGoogle ScholarPubMed
34Meizel, S, Pillai, MC, Diaz-Perez, E, Thomas, P. Initiation of the human sperm acrosome reaction by components of human follicular fluid and cumulus secretions including steroids. In: Bavister, BD, Cummins, J, Roldan, ERS eds. Fertilization in Mammals. Norwell, MA: Serono Symposia, 1991: 205–22.Google Scholar
35Suarez, SS, Wolf, DP, Meizel, S. Induction of the acrosome reaction in human spermatozoa by a fraction of human follicular fluid. Gamete Res 1986; 14: 107–21.CrossRefGoogle Scholar
36De Jonge, CJ, Han, H-L, Mack, SR, Zaneveld, LJD. Effect of phorbol diesters, synthetic diacylglycerols, and a protein kinase inhibitor on the human sperm acrosome reaction. J Androl 1991; 12: 62–70.CrossRefGoogle Scholar
37De Jonge, CJ, Han, H-L, Lawrie, H, Mack, SR, Zaneveld, LJD (1991). Modulation of the human sperm acrosome reaction by effectors of the adenylate cyclase/cyclic AMP second messenger pathway. J Exp Zool 1991; 258: 113–25.CrossRefGoogle ScholarPubMed
38De Jonge, CJ, Mack, SR, Radwanska, E, Zaneveld, LJD. Regulation of the human sperm acrosome reaction by two second messenger pathways. In: Baccetti, B ed. Comparative spermatology 20 years after, Volume 75. New York: Serono Symposia Publications, Raven Press, 1991: 143–47.Google Scholar
39Bhattacharyya, AK, Zaneveld, LJD. The sperm head. In: Zaneveld, LJD, Chatterton, RT eds. Biochemistry of mammalian fertilization. New York: Wiley, 1982: 119–51.Google Scholar
40Eddy, EM, O'Brien, DA. The spermatozoon. In: Knobil, E, Neill, J eds. The physiology of reproduction, Volume 1. New York: Raven Press, 1994: 29–77.Google Scholar
41Tesarik, J, Drahorad, J, Testart, J, Mendoza, C. Acrosin activation follows its surface exposure and precedes membrane fusion in human sperm acrosome reaction. Development 1990; 110: 391–400.CrossRefGoogle ScholarPubMed
42Tesarik, J, Drahorad, J, Peknicova, J. Subcellular immunochemical localization of acrosin in human spermatozoa during the acrosome reaction and the zona pellucida penetration. Fertil Steril 1988; 50: 133–41.CrossRefGoogle ScholarPubMed
43De Jonge, CJ, Mack, SR, Zaneveld, LJD. Inhibition of the human sperm acrosome reaction by proteinase inhibitors. Gamete Res 1989; 23: 287–97.CrossRefGoogle ScholarPubMed
44Tesarik, J. Appropriate timing of the acrosome reaction is a major requirement for the fertilizing spermatozoon. Human Reprod 1989; 4: 957–67.CrossRefGoogle Scholar
45Oehninger, S, Coddington, CC, Scott, R et al. Hemizona assay: assessment of sperm dysfunction and prediction o. in vitro fertilization outcome. Fertil Steril 1989; 51: 665–70.CrossRefGoogle Scholar
46Goodpasture, JC, Zavos, PM, Cohen, MR, Zaneveld, LJD. Relationship of human sperm acrosin and proacrosin to semen parameters. Comparisons between symptomatic men of infertile couples and asymptomatic men, and between different split ejaculate fractions. J Androl 1982; 3: 151–56.CrossRefGoogle Scholar
47Kennedy, WP, Kaminski, JM, Van der Ven, HH et al. A simple, clinical assay to evaluate the acrosin activity of human spermatozoa. J Androl 1989; 10: 221–31.CrossRefGoogle ScholarPubMed
48Koukoulis, GN, Vantman, D, Dennison, L, Banks, SM, Sherins, RJ. Low acrosin activity in a group of men with idiopathic infertility does not correlate with sperm density, percent motility, curvilinear velocity, or linearity. Fertil Steril 1989; 52: 120–27.CrossRefGoogle ScholarPubMed
49Mohsenian, M, Syner, FN, Moghissi, KS. A study of sperm acrosin in patients with unexplained infertility. Fertil Steril 1982; 37: 223–29.CrossRefGoogle ScholarPubMed
50De Jonge, CJ, Tarchala, SM, Rawlins, RG, Binor, Z, Radwanska, E. Acrosin activity in human spermatozoa in relation to semen quality and in vitro fertilization. Human Reprod 1993; 8: 253–57.CrossRefGoogle ScholarPubMed
51Tummon, IS, Yuzpe, AA, Daniel, SAJ, Deutsch, A. Total acrosin activity correlates with fertility potential after fertilization in vitro. Fertil Steril 1991; 56: 933–38.CrossRefGoogle ScholarPubMed
52Birnbaumer, L. Transduction of receptor signal into modulation of effector activity by G proteins: the first 20 years or so. FASEB J 1990; 4: 3068–78.CrossRefGoogle ScholarPubMed
53Birnbaumer, L, Abramowitz, J, Brown, AM. Receptor-effector coupling by G proteins. Biochim Biophys Acta 1990; 1031: 163–224.CrossRefGoogle ScholarPubMed
54Berridge, MJ. The molecular basis of communication in the cell. Sci Am 1985; 253: 142–52.CrossRefGoogle ScholarPubMed
55Garty, NB, Galiani, D, Aharonheim, A et al. G-proteins in mammalian gametes: an immunocytochemical study. J Cell Sci 1988; 99: 21–31.CrossRefGoogle Scholar
56Thomas, P, Meizel, S. Phosphatidylinositol 4,5-biphosphate hydrolysis in human sperm stimulated with follicular fluid or progesterone is dependent upon Ca2+ influx. Biochem J 1989; 264: 539–46.CrossRefGoogle ScholarPubMed
57Roldan, ERS, Harrison, RAP. Polyphosphoinositide breakdown and subsequent exocytosis in the Ca2+/ionophore-induced acrosome reaction of mammalian spermatozoa. Biochem J 1989; 259: 397–406.CrossRefGoogle ScholarPubMed
58Bielfeld, P, Zaneveld, LJD, De Jonge, CJ. The zona pellucida-induced acrosome reaction of human spermatozoa is mediated by protein kinases. Fertil Steril 1994; 61: 536–41.CrossRefGoogle ScholarPubMed
59Tesarik, J, Mendoza, C, Moos, J, Carreras, A. Selective expression of a progesterone receptor on the human sperm surface. Fertil Steril 1992; 58: 784–92.CrossRefGoogle ScholarPubMed
60Doherty, C, Tarchala, SM, De Jonge, CJ. Characterization of signal transduction pathway interactions in eliciting the human sperm acrosome reaction. J Androl 1993 (suppl): P-26.Google Scholar
61Thomas, P, Meizel, S. An influx of extracellular calcium is required for initiation of the human sperm acrosome reaction induced by human follicular fluid. Gamete Res 1988; 20: 397–411.CrossRefGoogle ScholarPubMed
62Blackmore, PF, Beebe, SJ, Danforth, DR, Alexander, N. Progesterone and 17a-hydroxyprogesterone novel stimulators of calcium influx in human sperm. J Biol Chem 1990; 265: 1376–80.CrossRefGoogle Scholar
63Baldi, E, Gasano, R, Flasetti, C, Krausz, C, Maggi, M, Forti, G. Intracellular calcium accumulation and responsiveness to progesterone in capacitating human spermatozoa. J Androl 1991; 12: 323–30.CrossRefGoogle ScholarPubMed
64Osman, RA, Andria, ML, Jones, DA, Meizel, S. Steroid induced exocytosis: the human sperm acrosome reaction. Biochem Biophys Res Commun 1989; 160: 828–33.CrossRefGoogle ScholarPubMed
65Parinaud, J, Labal, B, Vieitez, G. High progesterone concentrations induce acrosome reaction with a low cytotoxic effect. Fertil Steril 1992; 58: 599–602.CrossRefGoogle ScholarPubMed
66Wistrom, CA, Meizel, S. Evidence suggesting involvement of a unique human sperm steroid receptor/CI channel complex in the progesterone-initiated acrosome reaction. Develop Biol 1993; 159: 679–90.Google Scholar
67Rubin, RP, Weiss, GB, Putney, JW eds. Calcium in biological systems. New York: Plenum Press, 1985.CrossRefGoogle Scholar
68Gomperts, BD. Calcium shares the limelight in stimulus-secretion coupling. Trends Biochem Sci 1986; 11: 290–92.CrossRefGoogle Scholar
69Putney, JW, Bird, GStJ. The signal for capacitative calcium entry. Cell 1993; 75: 199–201.CrossRefGoogle ScholarPubMed
70Aitken, RJ, Ross, A, Hargreave, T, Richardson, D, Best, F. Analysis of human sperm function following exposure to the ionophore A23187. J Androl 1984; 5: 321–29.CrossRefGoogle Scholar
71Byrd, W, Wolf, DP. Acrosomal status in fresh and capacitated human ejaculated sperm. Biol Reprod 1986; 34: 859–69.CrossRefGoogle ScholarPubMed
72Byrd, W, Tsu, J, Wolf, DP. Kinetics of spontaneous and induced acrosomal loss in human sperm incubated under capacitating and noncapacitating conditions. Gamete Res 1989; 22: 109–22.CrossRefGoogle ScholarPubMed
73De Jonge, CJ, Mack, SR, Zaneveld, LJD. Synchronous assay for human sperm capacitation, and the acrosome reaction. J Androl 1989; 10: 232–39.CrossRefGoogle ScholarPubMed
74Stock, CE, Fraser, LR. Divalent cations, capacitation and the acrosome reaction reactions in human spermatozoa. J Reprod Fert 1989; 87: 463–78.CrossRefGoogle ScholarPubMed
75Meizel, S, Turner, KO. Initiation of the human sperm acrosome reaction by thapsigargin. J Exp Zool 1993; 267: 350–55.CrossRefGoogle ScholarPubMed
76Bielfeld, P, Anderson, RA, Mack, SR, De Jonge, CJ, Zaneveld, LJD. Are capacitation or calcium ion influx required for the human sperm acrosome reaction? Fertil Steril 1994 (in press).CrossRefGoogle Scholar
77Levitski, A. Cross-talk between PKC and cyclic AMP pathways. Nature 1987; 330: 319–20.CrossRefGoogle Scholar
78Houslay, MD. ‘Crosstalk’: a pivitol role for protein kinase C in modulating relationships between signal transduction pathway. Eur J Biochem 1991; 195: 9–27.CrossRefGoogle Scholar
79Sofikitis, N, Miyagawa, I, Toda, T, Terakawa, N. Effects of an inhibitor of adenylate cyclase on acrosome reaction induced by protein kinase C activators. Arch Androl 1993; 30: 87–92.CrossRefGoogle ScholarPubMed
80Cross, NL, Meizel, S. Methods for evaluating the acrosomal status of mammalian sperm. Biol Reprod 1989; 41: 635–41.CrossRefGoogle ScholarPubMed
81Talbot, P, Chacon, RS. A triple stain technique for evaluating normal acrosome reactions of human sperm. J Exp Zool 1981; 215: 201–208.CrossRefGoogle ScholarPubMed
82Mack, SR, De Jonge, CJ, Bielfeld, P, Zaneveld, LJD. Acrosome reaction of human spermatozoa: comparative evaluation by triple stain and electron microscopy. Mol Androl 1990; 2: 265–79.Google Scholar
83Cross, NL, Morales, P, Overstreet, JW, Hanson, FW. Two simple methods for detecting acrosome-reacted human sperm. Gamete Res 1986; 15: 235–44.CrossRefGoogle Scholar
84Holden, CA, Trounson, AO. Staining of the inner acrosomal membrane of human spermatozoa with concanavalin A lectin as an indicator of potential egg penetration ability. Fertil Steril 1991; 56: 967–74.CrossRefGoogle ScholarPubMed
85 Mendoza C, Carreras A, Moos J, Tesarik, J. Distinction between true acrosome reaction and degenerative acrosome reaction loss by a one-step staining method using Pisum sativum agglutinin. J Reprod Fertil 1992; 95: 755–63.Google Scholar
86Tesarik, J, Mendoza, C, Carreras, A. Fast acrosome reaction measure: a highly sensitive method for evaluating stimulus-induced acrosome reaction. Fertil Steril 1993; 59: 424–30.CrossRefGoogle Scholar
87Wolf, DP, Boldt, J, Byrd, W, Bechtol, KB. Acrosomal status evaluation in human ejaculate sperm with monoclonal antibodies. Biol Reprod 1985; 32: 1157–62.CrossRefGoogle ScholarPubMed
88Moore, HDM, Smith, CA, Hartman, TD, Bye, AP. Visualization and characterization of the acrosome reaction of human spermatozoa by immunolocalization with monoclonal antibody. Gamete Res 1987; 17: 245–59.CrossRefGoogle ScholarPubMed
89Sanchez, R, Topfer-Petersen, E, Aitken, RJ, Schill, WB. A new method for evaluation of the acrosome reaction in viable human spermatozoa. Andrologia 1991; 23: 197–203.CrossRefGoogle ScholarPubMed
90Lee, MA, Trucco, GS, Bechtol, KB et al. Capacitation and acrosome reactions in human spermatozoa monitored by a chlortetracycline fluorescence assay. Fertil Steril 1987; 48: 649–58.CrossRefGoogle ScholarPubMed
91Mortimer, D. Sperm preparation techniques and iatrogenic failures of in-vitro fertilization. Human Reprod 1991; 6: 173–76.CrossRefGoogle ScholarPubMed
92Aitken, RJ, Clarkson, JS. Significance of reactive oxygen species and antioxidants in defining the efficiency of sperm preparation techniques. J Androl 1988; 9: 367–76.CrossRefGoogle Scholar
93Aitken, RJ, Clarkson, JS, Fishel, S. Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod 1989; 40: 183–97.CrossRefGoogle Scholar
94Iwasaki, A, Gagnon, C. Formation of reactive oxygen species in spermatozoa of infertile patients. Fertil Steril 1992; 57: 409–16.CrossRefGoogle ScholarPubMed
95Kovalski, NN, de Lamirande, E, Gagnon, C. Reactive oxygen species generated by human neutrophils inhibit sperm motility: prospective effect of seminal plasma and scavengers. Fertil Steril 1992; 58: 809–16.CrossRefGoogle Scholar
96Aitken, RJ, Buckingham, D, Harkiss, D. Use of a xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J Reprod Fertil 1993; 97: 441–50.CrossRefGoogle ScholarPubMed
97Aitken, RJ, Irvine, DS, Wu, FC. Prospective analysis of sperm-oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am J Obstet Gynecol 1991; 164: 542–51.CrossRefGoogle ScholarPubMed
98Mortimer, D. Practical laboratory andrology. Oxford: Oxford University Press, 1994: 267–86.CrossRefGoogle Scholar
99Yanagimachi, R, Chang, MC. Fertilization of hamster eggs in vitro. Nature 1963; 200: 281–82.CrossRefGoogle ScholarPubMed
100Barros, C, Austin, CR. In vitro fertilization and sperm acrosome reaction in the hamster. J Exp Zool 1967; 166: 317–24.CrossRefGoogle ScholarPubMed
101Yanagimachi, R. In vitro capacitation of golden hamster spermatozoa by homologous and heterologous blood sera. Biol Reprod 1970; 3: 147–53.CrossRefGoogle ScholarPubMed
102Aitken, RJ, Wang, Y-F, Liu, J, Best, F, Richardson, DW. The influence of medium composition, osmolarity and albumin content on the acrosome reaction and fertilizing capacity of human spermatozoa: development of an improved zona-free hamster egg penetration test. Int J Androl 1983; 6: 180–93.CrossRefGoogle ScholarPubMed
103Ravnik, SE, Albers, JJ, Muller, CH. A novel view of albumin-supported sperm capacitation: role of Lipid Transfer Protein-I. Fertil Steril 1993; 59: 629–38.CrossRefGoogle ScholarPubMed
104Ravnik, SE, Zarutskie, PW, Muller, CH. Lipid transfer activity in human follicular fluid: relation to human sperm capacitation. J Androl 1990; 11: 216–26.CrossRefGoogle ScholarPubMed
105Ravnik, SE, Zarutskie, PW, Muller, CH. Purification and characterization of a human follicular fluid lipid transfer protein that stimulates human sperm capacitation. Biol Reprod 1992; 47: 1126–33.CrossRefGoogle ScholarPubMed
106Calvo, L, Vantman, D, Banks, SM et al. Follicular fluid-induced acrosome reaction distinguishes a subgroup of men with unexplained infertility not identified by semen analysis. Fertil Steril 1989; 52: 1048–54.CrossRefGoogle Scholar
107Bielfeld, P, Jeyendran, RS, Zaneveld, LJD. Human spermatozoa do not undergo the acrosome reaction during storage in the cervix. Int J Fertil 1991; 36: 302–306.Google Scholar
108Babcock, DF, First, NL, Lardy, HA. Action of ionophore A23187 at the cellular level. J Biol Chem 1976; 251: 3881–86.CrossRefGoogle ScholarPubMed
109Aitken, RJ, Buckingham, DW, Fang, HG. Analysis of the responses of human spermatozoa to A23187 employing a novel technique for assessing the acrosome reaction. J Androl 1993; 14: 132–41.CrossRefGoogle ScholarPubMed
110Tournaye, H, Janssens, R, Camus, M, Staessen, C, Devroey, P, Van Steirteghem, A. Pentoxifylline is not useful in enhancing sperm function in cases with previous in vitro fertilization failure. Fertil Steril 1993; 59: 210–15.CrossRefGoogle Scholar
111Lewis, SEH, Moohan, JM, Thompson, W. Effects of pentoxifylline on human sperm motility in normospermic individuals using computer-assisted analysis. Fertil Steril 1993; 59: 418–23.CrossRefGoogle ScholarPubMed
112Pang, SC, Williams, DB, Huang, T, Wang, C. Effects of pentoxifylline on sperm motility and hyperactivated motility in vitro: a preliminary report. Fertil Steril 1993; 59: 465–67.CrossRefGoogle ScholarPubMed
113Tesarik, J, Mendoza, C, Carreras, A. Effects of phosphodiesterase inhibitors caffeine and pentoxyfylline on spontaneous and stimulus-induced acrosome reactions in human sperm. Fertil Steril 1992; 58: 1185–90.CrossRefGoogle ScholarPubMed
114Tesarik, J, Mendoza, C. Sperm treatment with pentoxifylline improves the fertilizing ability in patients with acrosome reaction insufficiency. Fertil Steril 1993; 60: 141–48.CrossRefGoogle ScholarPubMed
115Tasdemir, M, Tasdemir, I, Kodama, H, Tanaka, T. Pentoxifylline-enhanced acrosome reaction correlates with fertilization in vitro. Human Reprod 1993; 8: 2102–107.CrossRefGoogle ScholarPubMed
116Mbizvo, MT, Burkman, LJ, Alexander, NJ. Human follicular fluid stimulates hyperactivated motility in human sperm. Fertil Steril 1990; 54: 708–12.CrossRefGoogle ScholarPubMed
117Cross, NL, Morales, P, Overstreet, JW, Hanson, FW. Induction of acrosome reactions by the human zona pellucida. Boil Reprod 1988; 38: 235–44.CrossRefGoogle ScholarPubMed
118Coddington, C, Fulgham, DL, Alexander, NJ, Johnson, DJ, Herr, JC, Hodgen, GD. Sperm bound to zona pellucida in hemizona assay demonstrate acrosome reaction when stained with T-6 antibody. Fertil Steril 1990; 54: 504–508.CrossRefGoogle ScholarPubMed
119Hoshi, K, Sugano, T, Endo, C, Yoshimatsu, N, Yanagida, K, Sato, A. Induction of the acrosome reaction in human spermatozoa by human zona pellucida and effect of cervical mucus on zona-induced acrosome reaction. Fertil Steril 1993; 60: 149–53.CrossRefGoogle ScholarPubMed
120Burkman, LJ, Coddington, CC, Franken, DR, Kruger, TF, Rosenwaks, Z, Hodgen, GD. The hemizona assay (HZA): development of a diagnostic test for the binding of human spermatozoa to the human hemizona pellucida to predict fertilization potential. Fertil Steril 1988; 49: 688–97.CrossRefGoogle Scholar
121Barratt, CLR, McCann, CT, Hornby, DP, Andrews, PD. Recombinant zona pellucida 3 expressed in Chinese hamster ovary cells is a potent inducer of the human acrosome reaction. Human Reprod 1993; 8: 407.Google Scholar
122De Jonge, CJ, Rawlins, RG, Zaneveld, LJD. Induction of the human sperm acrosome reaction by human oocytes. Fertil Steril 1988; 50: 949–53.CrossRefGoogle ScholarPubMed
123Plachot, M, Mandelbaum, J, Junca, AM. Acrosome reaction of human sperm used for in vitro fertilization. Fertil Steril 1984; 42: 418–23.CrossRefGoogle ScholarPubMed
124Fenichel, P, Donzeau, M, Farahifar, D, Basteris, B, Ayraud, N, Hsi, B-L. Dynamics of human sperm acrosome reaction: relation with in vitro fertilization. Fertil Steril 1991; 55: 994–99.CrossRefGoogle ScholarPubMed
125Henkel, R, Muller, C, Miska, W, Gips, H, Schul, WB. Determination of the acrosome reaction in human spermatozoa is predictive of fertilization in vitro. Human Reprod 1993; 8: 2128–32.CrossRefGoogle ScholarPubMed
126Takahashi, K, Wetzels, AMM, Goverde, HJM, Bastiaans, BA, Janssen, HJG, Rolland, R. The kinetics of the acrosome reaction of human spermatozoa and its correlation with in vitro fertilization. Fertil Steril 1992; 57: 889–94.CrossRefGoogle ScholarPubMed
127Topfer-Petersen, E, Heissler, E, Schill, WB. The kinetic of acrosome reaction: an additional sperm parameter. Andrologia 1985; 17: 224–27.CrossRefGoogle ScholarPubMed
128Pampiglione, JS, Tan, S-L, Campbell, S. The use of the stimulated acrosome reaction test as a test of fertilizing ability in human spermatozoa. Fertil Steril 1993; 59: 1280–84.CrossRefGoogle ScholarPubMed
129Cummins, JM, Pember, SM, Jequier, AM, Yovich, JL, Hartmann, PE. A test of the human sperm acrosome reaction following ionophore challenge. Relationship to fertility and other seminal parameters. J Androl 1991; 12: 98–103.CrossRefGoogle ScholarPubMed
130Shimizu, Y, Nord, EP, Bronson, RA. Progesterone-evoked increases in sperm [Ca2+]i correlate with the egg penetrating ability of sperm from fertile but not infertile men. Fertil Steril 1993; 60: 526–32.CrossRefGoogle Scholar
131Tesarik, J, Mendoza, C. Defective function of a nongenomic progesterone receptor as a sole sperm anomaly in infertile patients. Fertil Steril 1992; 58: 793–97.CrossRefGoogle ScholarPubMed
132Falsetti, C, Baldi, E, Krausz, C, Casano, R, Failli, P, Forti, G. Decreased responsiveness to progesterone of spermatozoa in oligozoospermic patients. J Androl 1993; 14: 17–22.CrossRefGoogle ScholarPubMed
133Oehninger, S, Blackmore, P, Morshedi, M, Suedlo, C, Acosta, AA, Alexander, NJ. Defective calcium influx and acrosome reaction (spontaneous and progesterone-induced) in spermatozoa of infertile men with severe teratozoospermia. Fertil Steril 1994; 61: 349–54.CrossRefGoogle ScholarPubMed
134Amann, RP. Can the fertility potential of a seminal sample be predicted accurately? J Androl 1989; 10: 89–98.CrossRefGoogle Scholar
135Amann, RP, Hammerstedt, RH. In vitro evaluation of sperm quality: an opinion. J Androl 1993; 14: 397–406.CrossRefGoogle ScholarPubMed
136Duncan, WW, Glew, MJ, Wang, X-J, Flaherty, SP, Matthews, CD. Prediction of in vitro fertilization rates from semen variables. Fertil Steril 1993; 59: 1233–38.CrossRefGoogle ScholarPubMed
137Jeyendran, RS, Zaneveld, LJD. Controversies in the development and validation of new sperm assays. Fertil Steril 1993; 59: 726–28.CrossRefGoogle ScholarPubMed
138Pampiglione, JS. Semen analysis and the acrosome reaction as a measure of fertilizing ability. Contemp Rev Obstet Gynecol 1991; 2: 1059–65.Google Scholar
139World Health Organization. Adenosine triphosphate in semen and other sperm characteristics: their relevance for fertility prediction in men with normal sperm concentration. Fertil Steril 1992; 57: 877–81.CrossRefGoogle Scholar
140Zaneveld, LJD, Jeyendran, RS. Sperm function tests. Infertil Reprod Med Clinics North Am 1992; 3: 353–71.Google Scholar
141World Health Organization. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction, third edition. Cambridge: Cambridge University Press, 1992.Google Scholar