Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosomes of mammalian sperm

doi:10.1083/jcb.130.4.857

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Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosomes of mammalian sperm

LD Walensky and SH Snyder
Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.

Calcium flux is required for the mammalian sperm acrosome reaction, an exocytotic event triggered by egg binding, which results in a dramatic rise in sperm intracellular calcium. Calcium-dependent membrane fusion results in the release of enzymes that facilitate sperm penetration through the zona pellucida during fertilization. We have characterized inositol 1,4,5-trisphosphate (IP3)-gated calcium channels and upstream components of the phosphoinositide signaling system in mammalian sperm. Peptide antibodies colocalized G alpha q/11 and the beta 1 isoform of phospholipase C (PLC beta 1) to the anterior acrosomal region of mouse sperm. Western blotting using a polyclonal antibody directed against purified brain IP3 receptor (IP3R) identified a specific 260 kD band in 1% Triton X-100 extracts of rat, hamster, mouse and dog sperm. In each species, IP3R immunostaining localized to the acrosome cap. Scatchard analysis of [3H]IP3 binding to rat sperm sonicates revealed a curvilinear plot with high affinity (Kd = 26 nM, Bmax = 30 pmol/mg) and low affinity (Kd = 1.6 microM, Bmax = 550 pmol/mg) binding sites, reflecting among the highest receptor densities in mammalian tissue. Immunoelectron microscopy confirmed the acrosomal localization in rat sperm. The IP3R fractionated with acrosomes by discontinuous sucrose gradient centrifugation and was enriched in the medium of acrosome- reacted sperm. ATP-dependent 45Ca2+ loading of digitonin permeabilized rat sperm was decreased by 45% in the presence of 10 microM IP3. The IP3-mediated release of calcium was blocked by heparin. Thapsigargin, a sequiterpene lactone inhibitor of the microsomal Ca(2+)-ATPase, stimulated the acrosome reaction of mouse sperm to the same extent as the Ca2+ ionophore, A23187. The failure of caffeine and ryanodine to affect calcium accumulation suggested that thapsigargin acted through an IP3-sensitive store. The presence of G alpha q/11, PLC beta 1 and a functional IP3R in the anterior acrosomal region of mammalian sperm, as well as thapsigargin's induction of the acrosome reaction, implicate IP3-gated calcium release in the mammalian acrosome reaction.
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Wilson, K. L., Fitch, K. R., Bafus, B. T., Wakimoto, B. T. (2006). Sperm plasma membrane breakdown during Drosophila fertilization requires Sneaky, an acrosomal membrane protein. Development 133: 4871-4879 [Abstract] [Full Text]
Jeske, N. A., Patwardhan, A. M., Gamper, N., Price, T. J., Akopian, A. N., Hargreaves, K. M. (2006). Cannabinoid WIN 55,212-2 Regulates TRPV1 Phosphorylation in Sensory Neurons. J. Biol. Chem. 281: 32879-32890 [Abstract] [Full Text]
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Jimenez-Gonzalez, C., Michelangeli, F., Harper, C.V., Barratt, C.L.R., Publicover, S.J. (2006). Calcium signalling in human spermatozoa: a specialized 'toolkit' of channels, transporters and stores. Hum Reprod Update 12: 253-267 [Abstract] [Full Text]
Bray, C., Son, J.-H., Meizel, S. (2005). Acetylcholine causes an increase of intracellular calcium in human sperm. Mol Hum Reprod 11: 881-889 [Abstract] [Full Text]
Harper, C. V., Publicover, S. J. (2005). Reassessing the role of progesterone in fertilization--compartmentalized calcium signalling in human spermatozoa?. Hum Reprod 20: 2675-2680 [Abstract] [Full Text]
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Chiarella, P., Puglisi, R., Sorrentino, V., Boitani, C., Stefanini, M. (2004). Ryanodine receptors are expressed and functionally active in mouse spermatogenic cells and their inhibition interferes with spermatogonial differentiation. J. Cell Sci. 117: 4127-4134 [Abstract] [Full Text]
Gonzalez-Martinez, M. T. (2003). Induction of a Sodium-dependent Depolarization by External Calcium Removal in Human Sperm. J. Biol. Chem. 278: 36304-36310 [Abstract] [Full Text]
Wennemuth, G., Babcock, D. F., Hille, B. (2003). Calcium Clearance Mechanisms of Mouse Sperm. JGP 122: 115-128 [Abstract] [Full Text]
Ho, H.-C., Suarez, S. S. (2003). Characterization of the Intracellular Calcium Store at the Base of the Sperm Flagellum That Regulates Hyperactivated Motility. Biol. Reprod. 68: 1590-1596 [Abstract] [Full Text]
Fukami, K., Yoshida, M., Inoue, T., Kurokawa, M., Fissore, R. A., Yoshida, N., Mikoshiba, K., Takenawa, T. (2003). Phospholipase C{delta}4 is required for Ca2+ mobilization essential for acrosome reaction in sperm. JCB 161: 79-88 [Abstract] [Full Text]
Dorval, V., Dufour, M., Leclerc, P. (2003). Role of protein tyrosine phosphorylation in the thapsigargin-induced intracellular Ca2+ store depletion during human sperm acrosome reaction. Mol Hum Reprod 9: 125-131 [Abstract] [Full Text]
Yoshida, M., Ishikawa, M., Izumi, H., De Santis, R., Morisawa, M. (2003). Store-operated calcium channel regulates the chemotactic behavior of ascidian sperm. Proc. Natl. Acad. Sci. USA 100: 149-154 [Abstract] [Full Text]
Harayama, H., Okada, K., Miyake, M. (2003). Involvement of Cytoplasmic Free Calcium in Boar Sperm: Head-to-Head Agglutination Induced by a Cell-Permeable Cyclic Adenosine Monophosphate Analog. J Androl 24: 91-99 [Abstract] [Full Text]
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Ho, H.-C., Suarez, S. S. (2001). An Inositol 1,4,5-Trisphosphate Receptor-Gated Intracellular Ca2+ Store Is Involved in Regulating Sperm Hyperactivated Motility. Biol. Reprod. 65: 1606-1615 [Abstract] [Full Text]
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Rossato, M., Virgilio, F.D., Rizzuto, R., Galeazzi, C., Foresta, C. (2001). Intracellular calcium store depletion and acrosome reaction in human spermatozoa: role of calcium and plasma membrane potential. Mol Hum Reprod 7: 119-128 [Abstract] [Full Text]
Garbi, M., Rubinstein, S., Lax, Y., Breitbart, H. (2000). Activation of Protein Kinase C{alpha} in the Lysophosphatidic Acid-Induced Bovine Sperm Acrosome Reaction and Phospholipase D1 Regulation. Biol. Reprod. 63: 1271-1277 [Abstract] [Full Text]
Minelli, A., Allegrucci, C., Piomboni, P., Mannucci, R., Lluis, C., Franco, R. (2000). Immunolocalization of A1 Adenosine Receptors in Mammalian Spermatozoa. J. Histochem. Cytochem. 48: 1163-1172 [Abstract] [Full Text]
Morales, P., Pizarro, E., Kong, M., Kerr, B., Ceric, F., Vigil, P. (2000). Gonadotropin-Releasing Hormone-Stimulated Sperm Binding to the Human Zona Is Mediated by a Calcium Influx. Biol. Reprod. 63: 635-642 [Abstract] [Full Text]
Kobori, H., Miyazaki, S., Kuwabara, Y. (2000). Characterization of Intracellular Ca2+ Increase in Response to Progesterone and Cyclic Nucleotides in Mouse Spermatozoa. Biol. Reprod. 63: 113-120 [Abstract] [Full Text]
Leclerc, P., Goupil, S. (2000). Distribution and Localization of Calmodulin-Binding Proteins in Bull Spermatozoa. Biol. Reprod. 62: 1875-1881 [Abstract] [Full Text]
Patrat, C., Serres, C., Jouannet, P. (2000). Induction of a Sodium Ion Influx by Progesterone in Human Spermatozoa1. Biol. Reprod. 62: 1380-1386 [Abstract] [Full Text]
O'Toole, C. M.B., Arnoult, C., Darszon, A., Steinhardt, R. A., Florman, H. M. (2000). Ca2+ Entry through Store-operated Channels in Mouse Sperm Is Initiated by Egg ZP3 and Drives the Acrosome Reaction. Mol. Biol. Cell 11: 1571-1584 [Abstract] [Full Text]
Harrison, D.A., Carr, D.W., Meizel, S. (2000). Involvement of Protein Kinase A and A Kinase Anchoring Protein in the Progesterone-Initiated Human Sperm Acrosome Reaction. Biol. Reprod. 62: 811-820 [Abstract] [Full Text]
Goodwin, L. O., Karabinus, D. S., Pergolizzi, R. G., Benoff, S. (2000). L-type voltage-dependent calcium channel {alpha}-1C subunit mRNA is present in ejaculated human spermatozoa. Mol Hum Reprod 6: 127-136 [Abstract] [Full Text]
Dragileva, E., Rubinstein, S., Breitbart, H. (1999). Intracellular Ca2+-Mg2+-ATPase Regulates Calcium Influx and Acrosomal Exocytosis in Bull and Ram Spermatozoa. Biol. Reprod. 61: 1226-1234 [Abstract] [Full Text]
Arnoult, C., Kazam, I. G., Visconti, P. E., Kopf, G. S., Villaz, M., Florman, H. M. (1999). Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. Proc. Natl. Acad. Sci. USA 96: 6757-6762 [Abstract] [Full Text]
Blackmore, P. F., Eisoldt, S. (1999). The neoglycoprotein mannose�bovine serum albumin, but not progesterone, activates T-type calcium channels in human spermatozoa. Mol Hum Reprod 5: 498-506 [Abstract] [Full Text]
Sabatini, D. M., Barrow, R. K., Blackshaw, S., Burnett, P. E., Lai, M. M., Field, M. E., Bahr, B. A., Kirsch, J., Betz, H., Snyder, S. H. (1999). Interaction of RAFT1 with Gephyrin Required for Rapamycin-Sensitive Signaling. Science 284: 1161-1164 [Abstract] [Full Text]
Publicover, S.J., Barratt, C.L.R. (1999). Voltage-operated Ca2+ channels and the acrosome reaction: which channels are present and what do they do?. Hum Reprod 14: 873-879 [Abstract] [Full Text]
Darszon, A., Labarca, P., Nishigaki, T., Espinosa, F. (1999). Ion Channels in Sperm Physiology. Physiol. Rev. 79: 481-510 [Abstract] [Full Text]
Merlet, F., Weinstein, L. S., Goldsmith, P. K., Rarick, T., Hall, J. L., Bisson, J.-P., de Mazancourt, P. (1999). Identification and localization of G protein subunits in human spermatozoa. Mol Hum Reprod 5: 38-45 [Abstract] [Full Text]
Florman, H. M., Arnoult, C., Kazam, I. G., Li, C., O'Toole, C. M.B. (1998). A Perspective on the Control of Mammalian Fertilization by Egg-Activated Ion Channels in Sperm: A Tale of Two Channels. Biol. Reprod. 59: 12-16 [Full Text]
Walensky, L. D., Ruat, M., Bakin, R. E., Blackshaw, S., Ronnett, G. V., Snyder, S. H. (1998). Two Novel Odorant Receptor Families Expressed in Spermatids Undergo 5'-Splicing. J. Biol. Chem. 273: 9378-9387 [Abstract] [Full Text]
Schaefer, M., Hofmann, T., Schultz, G., Gudermann, T. (1998). A new prostaglandin E receptor mediates calcium influx and acrosome reaction in human spermatozoa. Proc. Natl. Acad. Sci. USA 95: 3008-3013 [Abstract] [Full Text]
Schreiber, M., Wei, A., Yuan, A., Gaut, J., Saito, M., Salkoff, L. (1998). Slo3, a Novel pH-sensitive K+ Channel from Mammalian Spermatocytes. J. Biol. Chem. 273: 3509-3516 [Abstract] [Full Text]
Revelli, A., Massobrio, M., Tesarik, J. (1998). Nongenomic Actions of Steroid Hormones in Reproductive Tissues. Endocr. Rev. 19: 3-17 [Abstract] [Full Text]
Yang, Z.-h., Gallicano, G. I., Yu, Q.-C., Fuchs, E. (1997). An Unexpected Localization of Basonuclin in the Centrosome, Mitochondria, and Acrosome of Developing Spermatids. JCB 137: 657-669 [Abstract] [Full Text]
Arnoult, C., Cardullo, R.�A., Lemos, J.�R., Florman, H.�M. (1996). Activation of mouse sperm T-type Ca2+ channels by adhesion to the egg zona�pellucida. Proc. Natl. Acad. Sci. USA 93: 13004-13009 [Abstract] [Full Text]
Spungin, B, Breitbart, H (1996). Calcium mobilization and influx during sperm exocytosis. J. Cell Sci. 109: 1947-1955 [Abstract]