First messenger regulation of capacitation via G protein-coupled mechanisms: A tale of serendipity and discovery

Molecular Human Reproduction

Volumn 9, Issue 12, 2003, Pages 739-748

  Fraser, Lynn R ^a   Adeoya Osiguwa, Susan A ^a   Baxendale, Rhona W ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Adenosine; Adenylyl cyclase; Calcitonin; cAMP; FPP; Receptors

Indexed keywords

ADENOSINE A1 RECEPTOR AGONIST; ADENOSINE A2A RECEPTOR; ADENOSINE RECEPTOR; ADENYLATE CYCLASE; ANTIBODY; CALCITONIN RECEPTOR; CHOLERA TOXIN; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; ISOENZYME; PEPTIDE; PERTUSSIS TOXIN; PROTEIN SUBUNIT; RECEPTOR PROTEIN; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ACROSOME REACTION; CELL FUNCTION; ENZYME REGULATION; FERTILIZATION; HUMAN; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SOMATIC CELL; SPERMATOZOON; SPERMATOZOON CAPACITATION;

ADENOSINE; ADENYLATE CYCLASE; ANIMALS; CALCITONIN; CYCLIC AMP; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; HETEROTRIMERIC GTP-BINDING PROTEINS; HUMANS; MALE; MICE; PYRROLIDONECARBOXYLIC ACID; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PURINERGIC P1; SIGNAL TRANSDUCTION; SPERM CAPACITATION; SPERMATOZOA; THYROTROPIN-RELEASING HORMONE;

MAMMALIA;

EID: 0344896692     PISSN: 13609947     EISSN: None     Source Type: Journal    
DOI: 10.1093/molehr/gag097     Document Type: Review

References (73)

1. Adeoya-Osiguwa, S.A. and Fraser, L,R. (2000) Fertilization promoting peptide and adenosine, acting as first messengers, regulate cAMP production and consequent protein tyrosine phosphorylation in a capacitation-dependent manner. Mol. Reprod. Dev., 57, 384-392.
2. Adeoya-Osiguwa, S.A. and Fraser, LR. (2002) Capacitation state-dependent changes in adenosine receptors and their regulation of adenylyl cyclase/cAMP. Mol. Reprod. Dev., 63, 245-255.
3. Adeoya-Osiguwa, S.A. and Fraser, L.R. (2003) Calcitonin acts as a first messenger to regulate adenylyl cyclase/cAMP and mammalian sperm function. Mol. Reprod. Dev., 65, 228-236.
4. Adeoya-Osiguwa, S.A., Dudley, R.K., Hosseini, R. and Fraser, L.R. (1998) FPP modulates mammalian sperm function via TCP-11 and the adenylyl cyclase/cAMP pathway. Mol. Reprod Dev., 51, 468-476.
5. i2 protein subunit, has a capacitative effect on human spermatozoa. Biol. Reprod, 64, 1653-1659.
6. 2 is present in rat anterior and posterior pituitary gland. J. Endocrinol., 129, R1-R4.
7. Austin, C.R. (1952) The 'capacitation' of the mammalian sperm. Nature, 170, 326.
8. Bakalyar, H.A. and Reed, R.R. (1990) Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science, 250, 1403-1406.
9. Baxendale, R.W. and Fraser, L.R. (2003a) Evidence for multiple distinctly localized adenylyl cyclase isoforms in mammalian spermatozoa. Mol. Reprod. Dev., 66, 181-189.
10. s. Mol. Reprod. Dev., 65, 104-113.
11. Bentley, J.K., Garbers, D.L., Domino, S.E., Noland, T.D. and Van Dop, C. (1986) Spermatozoa contain a guanine nucleotide-binding protein ADP-ribosylated by pertussis toxin. Biochem. Biophys. Res. Commun., 138, 728-734.
12. Buck, J., Sinclair, M.L., Schapal, L., Cann, M.J. and Levin, L.R. (1999) Cytosolic adenylyl cyclase defines a unique signalling molecule in mammals. Proc. Natl Acad. Sci. USA, 96, 79-84.
13. Chen, Y., Cann, M.J., Litvin, T.N., Iourgenko, V., Sinclair, M.L., Levin, L.R. and Buck, J. (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science, 289, 625-628.
14. Cockle, S.M., Aitken, A., Beg, F. and Smyth, D.G. (1989) A novel peptide, pyroglutamylglutamylprolineamide, in the rabbit prostate, structurally related to TRH. J. Biol. Chem., 264, 7788-7791.
15. Cremades, A., Renafiel, R., Rausell, V., Del Rio-Garcia, J. and Smyth, D.G. (1998) The thyrotrophin-releasing hormone-like peptides pGlu-Phe-Pro amide and pGlu-Glu-Pro amide increase plasma triiodothyronine levels in the mouse; the activity is sensitive to testosterone. Eur. J. Pharmacol., 358, 63-67.
16. Cuellar-Mata, P., Martinez-Cadena, G., Castellano, L.E., Aldana-Veloz, G., Novoa-Martinez, G., Vargas, I., Darszon, A. and Garcia-Soto, J. (1995) Multiple GTP-binding proteins in sea urchin sperm: evidence for Gs and small G-proteins. Dev. Growth Differ., 37, 173-181.
17. 2+-related changes in the capacitation state of human spermatozoa assessed by a chlortetracycline fluorescence assay. J. Reprod. Fertil., 99, 135-143.
18. Defer, N., Marinx, O., Poyard, M., Lienard, M.O., Jegou, B. and Hanoune, J. (1998) The olfactory adenylyl cyclase type 3 is expressed in male germ cells. FEBS Lett., 424, 216-220.
19. Defer, N., Best-Belpomme, M. and Hanoune, J. (2000) Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. Am. J. Physiol. Renal Physiol., 279, F400-F416.
20. de Lamirande, E., Leclerc, P. and Gagnon, C. (1997) Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol. Hum. Reprod., 3, 175-194.
21. Endo, Y., Lee, M.A. and Kopf, G.S. (1987) Evidence for the role of a guanine nucleotide-binding regulatory protein in the zona pellucida-induced mouse sperm acrosome reaction. Dev. Biol., 119, 210-216.
22. Fabiani, R. and Ronquist, G. (1995) Abundance of guanine, guanosine, inosine and adenosine in human seminal plasma. Int. J. Clin. Lab. Res., 25, 47-51.
23. Fenichel, P., Gharib, A., Emiliozzi, C., Donzeau, M. and Menezo, Y. (1996) Stimulation of human sperm during capacitation in vitro by an adenosine agonist with specificity for A2 receptors. Biol. Reprod., 54, 1405-1411.
24. 2+ is required for mouse sperm capacitation and fertilization in vitro. J. Androl., 3, 412-419.
25. 2 receptors, stimulate mouse sperm fertilizing ability during early stages of capacitation. J. Reprod Fertil., 89, 463-476.
26. Fraser, L.R. (1993) In vitro capacitation and fertilization. In Wasserman, P.M. and DePamphilis, M.L. (eds), Guide to Techniques in Mouse Development. Methods Enzymol., 225, 239-253.
27. Fraser, L.R. and Adeoya-Osiguwa, S.A. (1999) Modulation of adenylyl cyclase by FPP and adenosine involves stimulatory and inhibitory adenosine receptors and G proteins. Mol. Reprod. Dev., 53, 459-471.
28. Fraser, L.R. and Adeoya-Osiguwa, S.A. (2001) Fertilization promoting peptide - a possible regulator of sperm function. Vitam. Horm., 63, 1-28.
29. Fraser, L.R. and Dudley, R.K. (1999) New insights into the t-complex and control of sperm function. Bioessays, 21, 304-312.
30. 2 receptors bind to mouse spermatozoa and stimulate adenylate cyclase activity in uncapacitated suspensions. J. Reprod. Fertil., 98, 187-194.
31. Fraser, L.R., Harrison R.A.P. and Herod J.E. (1990) Characterization of a decapacitation factor associated with epididymal mouse spermatozoa. J. Reprod. Fertil., 89, 135-148.
32. 2+-regulating mechanisms that modulate bull sperm capacitation and acrosomal exocytosis as determined by chlortetracycline analysis. Mol. Reprod. Dev., 40, 233-241.
33. Fraser, L.R., Hanyaloglu, A. and Cockle, S.M. (1997a) A fertilization promoting peptide (FPP)-related tripeptide competitively inhibits responses to FPP: a cause of male subfertility? Mol. Reprod. Dev., 48, 529-535.
34. Fraser, L.R., Hosseini, R., Hanyaloglu, A., Talmor, A. and Dudley, R.K. (1997b) TCP-11, the product of a mouse t-complex gene, plays a role in stimulation of capacitation and inhibition of the spontaneous acrosome reaction. Mol. Reprod. Dev., 48, 375-382.
35. Fraser, L.R., Pondel, M.C. and Vinson, G.P. (2001) Calcitonin, angiotensin II and FPP significantly modulate mouse sperm function. Mol. Hum. Reprod., 7, 245-253.
36. Funahashi, H., Fujuwara, T. and Nagai, T. (2000a) Modulation of the function of boar spermatozoa via adenosine and fertilization promoting peptide receptors reduce the incidence of polyspermic penetration into porcine oocytes. Biol. Reprod., 63, 1157-1163.
37. Funahashi, H., Asano, A., Fujiwara, T., Nagai, T., Niwa, K. and Fraser, L.R. (2000b) Both fertilization promoting peptide and adenosine stimulate capacitation but inhibit spontaneous acrosome loss in boar spermatozoa in vitro. Mol. Reprod. Dev., 55, 117-124.
38. Gautier-Courteille, C., Salanova, M. and Conti, M. (1998) The olfactory adenylyl cyclase III is expressed in rat germ cells during spermiogenesis. Endocrinology, 139, 2588-2599.
39. Glassner, M., Jones, J., Kligman, I., Woolkalis, M.J., Gerton, G.L. and Kopf, G.S. (1991) Immunocytochemical and biochemical characterization of guanine nucleotide-binding regulatory proteins in mammalian spermatozoa. Dev. Biol., 146, 438-450.
40. Green, C.M., Cockle, S.M., Watson, P.F. and Fraser, L.R. (1994) Stimulating effect of pyroglutamylglutamylprolineamide, a prostatic, TRH-related tripeptide, on mouse sperm capacitation and fertilizing ability in vitro. Mol. Reprod Dev., 38, 215-221.
41. Green, C.M., Cockle, S.M., Watson, P.F. and Fraser, L.R. (1996a) Fertilization promoting peptide, a tripeptide similar to thyrotrophin-releasing hormone, stimulates the capacitation and fertilizing ability of human spermatozoa in vitro. Hum. Reprod., 11, 830-836.
42. Green, C.M., Cockle, S.M., Watson, P.F. and Fraser, L.R. (1996b) A possible mechanism of action for fertilization promoting peptide, a TRH-related tripeptide that promotes capacitation and fertilizing ability in mammalian spermatozoa. Mol. Reprod Dev., 45, 244-252.
43. Green, C.M., Cockle, S.M., Fraser, L.R. and Watson, P.F. (1996c) The effect of FPP on the motility characteristics of mouse spermatozoa. J. Reprod. Fertil. Abstr. Ser., 17, 31.
44. Harrison, R.A.P. (2003) Cyclic AMP signalling during mammalian sperm capacitation - still largely terra incognita. Reprod. Domest. Anim., 38, 102-110.
45. Harvey, S., Trudeau, V.L., Ashworth, R.J. and Cockle, S.M. (1993) pGlutamylgluamylprolineamide modulation of growth hormone secretion in domestic fowls: Antagonism of thyrotrophin-releasing hormone action? J. Endocrinol., 138, 137-147.
46. Hildebrandt, J.D., Codina, J., Tash, J.S., Kirchick, H.J., Lipschultz, L., Sekura, R.D. and Birnbaumer, L. (1985) The membrane-bound spermatozoal adenylyl cyclase system does not share coupling characteristics with somatic cell adenylyl cyclases. Endocrinology, 116, 1357-1366.
47. Hinsch, K.D., Hinsch, E., Aumuller, G., Tychowiecka, I., Schultz, G. and Schill, W.B. (1992) Immunological identification of G protein α- and β-subunits in tail membranes of bovine spermatozoa. Biol. Reprod., 47, 337-346.
48. Hinsch, K.D., Schwerdel, C., Habermann, B., Schill, W.B., Muller-Schlosser, F. and Hinsch, E. (1995) Identification of heterotrimeric G proteins in human sperm tail membranes. Mol. Reprod. Dev., 40, 345-354.
49. Hosseini, R., Ruddy, S., Bains, S., Hynes, G., Marsh, P., Pizzey, J. and Dudley, K. (1994) The mouse t-complex gene, Tcp-11, is under translational control. Mech. Dev., 47, 73-80.
50. Kopf, G.S., Woolkalis, M.J. and Gerton, G.L. (1986) Evidence for a guanine nucleotide-binding regulatory protein in invertebrate and mammalian sperm. Identification by islet-activating protein-catalyzed ADP-ribosylation and immunochemical methods. J. Biol. Chem., 261, 7327-7331.
51. Leclerc, P. and Kopf, G.S. (1995) Mouse sperm adenylyl cyclase: general properties and regulation by the zona pellucida. Biol. Reprod., 52, 1227-1233.
52. Leclerc, P. and Kopf, G.S. (1999) Evidence for the role of heterotrimeric guanine nucleotide-binding regulatory proteins in the regulation of the mouse sperm adenylyl cyclase by the egg's zona pellucida. J. Androl., 20, 126-134.
53. 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.
54. Ma, Y., Zhang, S., Xia, Q., Zhang, G., Huang, X., Huang, M., Xiao, C., Pan, A., Sun, Y., Lebo, R. and Milunsky, A. (2002) Molecular characterization of the TCP11 gene which is the human homologue of the mouse gene encoding the receptor of fertilization promoting peptide. Mol. Hum. Reprod., 8, 24-31.
55. Mazarakis, N.D., Nelki, D., Lyon, M.F., Ruddy, S., Evans, E.P., Freemont, P. and Dudley, K. (1991) Isolation and characterisation of a testis-expressed developmentally regulated gene from the distal inversion of the mouse t-complex. Development, 111, 561-571.
56. Merlet, F., Weinstein, L.S., Goldsmith, P.K., Rarick, T., Hall, J.L., Bisson, J.P. and de Mazancourt, P. (1999) Identification and localization of G protein subunits in human spermatozoa. Mol. Hum. Reprod., 5, 38-45.
57. Minelli, A., Allegrucci, C., Piomboni, P., Mannucci, R., Lluis, C. and Franco, R. (2000) Immunolocalization of A1 adenosine receptors in mammalian spermatozoa. J. Histochem. Cytochem., 48, 1163-1171.
58. -s) variants of the stimulatory guanine nucleotide-binding protein. Do they behave in an identical way? J. Mol. Endocrinol., 20, 163-173.
59. Oberländer, G., Yeung, C.H. and Cooper, T.G. (1996) Influence of oral administration of ornidazole on capacitation and the activity of some glycolytic enzymes of rat spermatozoa. J. Reprod. Fertil., 106, 231-239.
60. Ohta, K., Sato, C., Matsuda, T., Toriyama, M., Vacquier, V.D., Lennarz, W.J. and Kitajima, K. (2000) Co-localization of receptor and transducer proteins in the glycosphingolipid-enriched, low density, detergent-insoluble membrane fraction of sea urchin sperm. Glycoconj. J., 17, 205-214.
61. O'Toole, C.M.B., Roldan, E.R.S. and Fraser, L.R. (1996) A role for diacylglycerol in human sperm acrosomal exocytosis. Mol. Hum. Reprod., 2, 317-326.
62. Palmer, T.M. and Stiles, G.L. (1995) Neurotransmitter receptors VII: Adenosine receptors. Neuropharmacology, 34, 683-694.
63. Pondel, M. (2000) Calcitonin and calcitonin receptors: bone and beyond. Int. J. Exp. Pathol., 81, 405-422.
64. Ragoussis, J., Senger, G., Mockridge, I., Sanseau, P., Ruddy, S., Dudley, K., Sheer, D. and Trowsdale, J. (1992) A testis expressed zinc finger gene ZNF76 in human 6p21.3 centromeric to the MHC is closely linked to the human homologue of the t-complex gene Tcp-11. Genomics, 14, 673-479.
65. Rakha, A.M., Adeoya-Osiguwa, S.A. and Fraser, L.R. (2000) Purification of a mouse sperm decapacitation factor and its receptor. J. Reprod. Fertil. Abstr. Ser., 26, 25.
66. sα through limited proteolysis by calpain. Biochem. J., 347, 733-740.
67. Sjöberg, H., Arver, S. and Bucht, E. (1980) High concentration of immunoreactive calcitonin of prostatic origin in human semen. Acta Physiol. Scand., 110, 101-102.
68. Silvestroni, L., Menditto, A., Frajese, G. and Gnessi, G. (1987) Identification of calcitonin receptors in human spermatozoa. J. Clin. Endocrinol. Metabol., 65, 742-746.
69. Spehr, M., Gisselmann, G., Poplawski, A., Riffell, J.A., Wetzel, C.H., Zimmer, R.K. and Hatt, H. (2003) Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science, 299, 2054-2058.
70. Stein, D.M., Fraser, L.R. and Monks, N.J. (1986) Adenosine and Gpp(NH)p modulate mouse sperm adenylate cyclase. Gamete Res., 13, 151-158.
71. Wang, W.H., Abeydeera, L.R., Fraser, L.R. and Niwa, K. (1995) Functional analysis using chlortetracycline fluorescence and in vitro fertilization of frozen-thawed ejaculated boar spermatozoa incubated in a protein-free chemically defined medium. J. Reprod. Fertil., 104, 305-313.
72. Ward, C.R. and Storey, B.T. (1984) Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline, fluorescence assay. Dev. Biol., 104, 287-296.
73. Yanagimachi, R. (1994) Mammalian fertilization: In Knobil, E. and Neill, J.D. (eds), The Physiology of Reproduction, 2nd Edn. Raven Press, New York, pp. 189-317.