HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

J. Biol. Chem., Vol. 279, Issue 44, 46315-46325, October 29, 2004

This Article Full Text Full Text (PDF) Supplemental Data All Versions of this Article: 279/44/46315    most recent M401194200v1 Submit a Letter to Editor Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Harper, C. V. Articles by Publicover, S. J. Search for Related Content PubMed PubMed Citation Articles by Harper, C. V. Articles by Publicover, S. J. Social Bookmarking                      What's this?

Stimulation of Human Spermatozoa with Progesterone Gradients to Simulate Approach to the Oocyte

INDUCTION OF [Ca²⁺]_i OSCILLATIONS AND CYCLICAL TRANSITIONS IN FLAGELLAR BEATING^*

Claire V. Harper¶, Christopher L. R. Barratt||, and Stephen J. Publicover**

From the School of Biosciences and the Reproductive Biology and Genetics Research Group, Medical School, University of Birmingham, Birmingham B15 2TT, United Kingdom and the ^||Assisted Conception Unit, Birmingham Women's Hospital, Birmingham B15 2TG, United Kingdom

Progesterone is present at micromolar concentrations in the cumulus matrix, which surrounds mammalian oocytes. Exposure of human spermatozoa to a concentration gradient of progesterone (0–3 µM) to simulate approach to the oocyte induced a slowly developing increase in [Ca²⁺]_i upon which, in many cells, slow oscillations were superimposed. [Ca²⁺]_i oscillations often started at very low progesterone (<10 nM), and their frequency did not change during the subsequent rise in concentration. Oscillations also occurred, but in a much smaller proportion of cells, in response to stepped application of progesterone (3 µM). When progesterone was removed, [Ca²⁺]_i oscillations often persisted or quickly resumed. Superfusion with low-Ca²⁺ bathing medium (no added Ca²⁺) did not prevent [Ca²⁺]_i oscillations, but they could be abolished by addition of EGTA or La³⁺. Inhibitors of sarcoplasmic/endoplasmic reticulum Ca²⁺-ATPases or inositol trisphosphate signaling had no effect on [Ca²⁺]_i oscillations, but pharmacological manipulation of ryanodine receptors affected both their frequency and amplitude. Staining of live spermatozoa with BODIPY FL-X ryanodine showed localization of ryanodine binding primarily to the caudal part of the head and mid-piece. [Ca²⁺]_i oscillations did not induce acrosome reaction, but in cells generating oscillations, the flagellar beat mode alternated in synchrony with the oscillation cycle. Flagellar bending and lateral movement of the sperm head during [Ca²⁺]_i peaks were markedly increased compared with during [Ca²⁺]_i troughs. This alternating pattern of activity is likely to facilitate zona penetration. These observations show that progesterone initiates unusual and complex store-mediated [Ca²⁺]_i signaling in human spermatozoa and identify a previously unrecognized effect of progesterone in regulating sperm "behavior" during fertilization.

Received for publication, February 3, 2004 , and in revised form, August 20, 2004.

^* This work was supported in part by the Wellcome Trust. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains Supplemental Figs. 1–5 and a video.

^¶ Recipient of a Biotechnology and Biological Sciences Research Council studentship. Present address: School of Biological Sciences, University of Liverpool, Liverpool L69 7ZB, UK.

^** To whom correspondence should be addressed: School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK. Tel.: 121-414-5455; Fax: 121-414-5925; E-mail: s.j.publicover{at}bham.ac.uk.

CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    What's this?

This article has been cited by other articles:

				A. Kawashima, B. A.H. Osman, M. Takashima, A. Kikuchi, S. Kohchi, E. Satoh, M. Tamba, M. Matsuda, and N. Okamura CABS1 Is a Novel Calcium-Binding Protein Specifically Expressed in Elongate Spermatids of Mice Biol Reprod, June 1, 2009; 80(6): 1293 - 1304. [Abstract] [Full Text] [PDF]

				G. M. Gibbs, K. Roelants, and M. K. O'Bryan The CAP Superfamily: Cysteine-Rich Secretory Proteins, Antigen 5, and Pathogenesis-Related 1 Proteins--Roles in Reproduction, Cancer, and Immune Defense Endocr. Rev., December 1, 2008; 29(7): 865 - 897. [Abstract] [Full Text] [PDF]

				G. Machado-Oliveira, L. Lefievre, C. Ford, M. B. Herrero, C. Barratt, T. J. Connolly, K. Nash, A. Morales-Garcia, J. Kirkman-Brown, and S. Publicover Mobilisation of Ca2+ stores and flagellar regulation in human sperm by S-nitrosylation: a role for NO synthesised in the female reproductive tract Development, November 15, 2008; 135(22): 3677 - 3686. [Abstract] [Full Text] [PDF]

				S. S. Suarez Control of hyperactivation in sperm Hum. Reprod. Update, November 1, 2008; 14(6): 647 - 657. [Abstract] [Full Text] [PDF]

				J. Cosson, A.-L. Groison, M. Suquet, C. Fauvel, C. Dreanno, and R. Billard Marine fish spermatozoa: racing ephemeral swimmers Reproduction, September 1, 2008; 136(3): 277 - 294. [Abstract] [Full Text] [PDF]

				C. V. Harper, J. A. Cummerson, M. R. H. White, S. J. Publicover, and P. M. Johnson Dynamic resolution of acrosomal exocytosis in human sperm J. Cell Sci., July 1, 2008; 121(13): 2130 - 2135. [Abstract] [Full Text] [PDF]

				D. Jamsai, D. M Bianco, S. J Smith, D. J Merriner, J. D Ly-Huynh, A. Herlihy, B. Niranjan, G. M Gibbs, and M. K O'Bryan Characterization of gametogenetin 1 (GGN1) and its potential role in male fertility through the interaction with the ion channel regulator, cysteine-rich secretory protein 2 (CRISP2) in the sperm tail Reproduction, June 1, 2008; 135(6): 751 - 759. [Abstract] [Full Text] [PDF]

				M. Shimada, Y. Yanai, T. Okazaki, N. Noma, I. Kawashima, T. Mori, and J. S. Richards Hyaluronan fragments generated by sperm-secreted hyaluronidase stimulate cytokine/chemokine production via the TLR2 and TLR4 pathway in cumulus cells of ovulated COCs, which may enhance fertilization Development, June 1, 2008; 135(11): 2001 - 2011. [Abstract] [Full Text] [PDF]

				C. Lawson, V. Dorval, S. Goupil, and P. Leclerc Identification and localisation of SERCA 2 isoforms in mammalian sperm Mol. Hum. Reprod., May 1, 2007; 13(5): 307 - 316. [Abstract] [Full Text] [PDF]

				L. Lefievre, K. Bedu-Addo, S. J Conner, G. S M Machado-Oliveira, Y. Chen, J. C Kirkman-Brown, M. A Afnan, S. J Publicover, W C. L Ford, and C. L R Barratt Counting sperm does not add up any more: time for a new equation? Reproduction, April 1, 2007; 133(4): 675 - 684. [Abstract] [Full Text] [PDF]

				Y.-Q. Su, M. Nyegaard, M. T. Overgaard, J. Qiao, and L. C. Giudice Participation of Mitogen-Activated Protein Kinase in Luteinizing Hormone-Induced Differential Regulation of Steroidogenesis and Steroidogenic Gene Expression in Mural and Cumulus Granulosa Cells of Mouse Preovulatory Follicles Biol Reprod, December 1, 2006; 75(6): 859 - 867. [Abstract] [Full Text] [PDF]

				C. V. Harper, C. L.R. Barratt, S. J. Publicover, and J. C. Kirkman-Brown Kinetics of the Progesterone-Induced Acrosome Reaction and Its Relation to Intracellular Calcium Responses in Individual Human Spermatozoa Biol Reprod, December 1, 2006; 75(6): 933 - 939. [Abstract] [Full Text] [PDF]

				A. Darszon, J. J Acevedo, B. E Galindo, E. O Hernandez-Gonzalez, T. Nishigaki, C. L Trevino, C. Wood, and C. Beltran Sperm channel diversity and functional multiplicity. Reproduction, June 1, 2006; 131(6): 977 - 988. [Abstract] [Full Text] [PDF]

				C. Jimenez-Gonzalez, F. Michelangeli, C.V. Harper, C.L.R. Barratt, and S.J. Publicover Calcium signalling in human spermatozoa: a specialized 'toolkit' of channels, transporters and stores Hum. Reprod. Update, May 1, 2006; 12(3): 253 - 267. [Abstract] [Full Text] [PDF]

				G. M. Gibbs, M. J. Scanlon, J. Swarbrick, S. Curtis, E. Gallant, A. F. Dulhunty, and M. K. O'Bryan The Cysteine-rich Secretory Protein Domain of Tpx-1 Is Related to Ion Channel Toxins and Regulates Ryanodine Receptor Ca2+ Signaling J. Biol. Chem., February 17, 2006; 281(7): 4156 - 4163. [Abstract] [Full Text] [PDF]

				C. V. Harper and S. J. Publicover Reassessing the role of progesterone in fertilization--compartmentalized calcium signalling in human spermatozoa? Hum. Reprod., October 1, 2005; 20(10): 2675 - 2680. [Abstract] [Full Text] [PDF]

				V. Vasta, W. K. Sonnenburg, C. Yan, S. H. Soderling, M. Shimizu-Albergine, and J. A. Beavo Identification of a New Variant of PDE1A Calmodulin-Stimulated Cyclic Nucleotide Phosphodiesterase Expressed in Mouse Sperm Biol Reprod, October 1, 2005; 73(4): 598 - 609. [Abstract] [Full Text] [PDF]

				P. Kumar and S. Meizel Nicotinic Acetylcholine Receptor Subunits and Associated Proteins in Human Sperm J. Biol. Chem., July 8, 2005; 280(27): 25928 - 25935. [Abstract] [Full Text] [PDF]

				C. De Jonge Biological basis for human capacitation Hum. Reprod. Update, May 1, 2005; 11(3): 205 - 214. [Abstract] [Full Text] [PDF]

				C. Harper, L. Wootton, F. Michelangeli, L. Lefievre, C. Barratt, and S. Publicover Secretory pathway Ca2+-ATPase (SPCA1) Ca2+ pumps, not SERCAs, regulate complex [Ca2+]i signals in human spermatozoa J. Cell Sci., April 15, 2005; 118(8): 1673 - 1685. [Abstract] [Full Text] [PDF]