Non-genomic regulation and disruption of spermatozoal in vitro hyperactivation by oviductal hormones
Tóm tắt
During capacitation, motility of mammalian spermatozoon is changed from a state of “activation” to “hyperactivation.” Recently, it has been suggested that some hormones present in the oviduct are involved in the regulation of this hyperactivation in vitro. Progesterone, melatonin, and serotonin enhance hyperactivation through specific membrane receptors, and 17β-estradiol suppresses this enhancement by progesterone and melatonin via a membrane estrogen receptor. Moreover, γ-aminobutyric acid suppresses progesterone-enhanced hyperactivation through the γ-aminobutyric acid receptor. These hormones dose-dependently affect hyperactivation. Although the complete signaling pathway is not clear, progesterone activates phospholipase C and protein kinases and enhances tyrosine phosphorylation. Moreover, tyrosine phosphorylation is suppressed by 17β-estradiol. This regulation of spermatozoal hyperactivation by steroids is also disrupted by diethylstilbestrol. The in vitro experiments reviewed here suggest that mammalian spermatozoa are able to respond to effects of oviductal hormones. We therefore assume that the enhancement of spermatozoal hyperactivation is also regulated by oviductal hormones in vivo.
Tài liệu tham khảo
Yanagimachi R (1994) Mammalian fertilization. In: Knobil E, Neill JD (eds) The physiology of reproduction, vol 1, 2nd edn. Raven Press, New York
Fujinoki M (2009) Non-genomic regulation of mammalian sperm hyperactivation. Reprod Med Biol 8:47–52
Mohri H, Inaba K, Ishijima S, Baba SA (2012) Tubulin-dynein system in flagellar and ciliary movement. Proc Jpn Acad Ser B 88:397–415
Schillo KK (2009) Reproductive physiology of mammals: from farm to field and beyond. Delmar, New York
Yudin AI, Gottlieb W, Meizel S (1988) Ultrastructural studies of the early events of the human sperm acrosome reaction as initiated by human follicular fluid. Gamete Res 20:11–24
Alasmari W, Barratt CLR, Publicover SJ, Whalley KM, Foster E, Kay V, da Silve SM, Oxenham SK (2013) The clinical significance of calcium-signaling pathways mediating human sperm hyperactivation. Hum Reprod 28:866–876
Suarez SS, Ho HC (2003) Hyperactivated motility in sperm. Reprod Domest Anim 38:119–124
Coy P, García-Vázquez FA, Visconti PE, Avilés M (2012) Roles of the oviduct in mammalian fertilization. Reproduction 144:649–660
Ho HC, Suarez SS (2001) Hyperactivation of mammalian spermatozoa: function and regulation. Reproduction 122:519–526
Langlais J, Roberts KD (1985) A molecular membrane model of sperm capacitation and the acrosome reaction of mammalian spermatozoa. Gamete Res 13:183–224
Noguchi T, Fujinoki M, Kitazawa M, Inaba N (2008) Regulation of hyperactivation of hamster spermatozoa by progesterone. Reprod Med Biol 7:63–74
Fujinoki M (2008) Melatonin-enhanced hyperactivation of hamster sperm. Reproduction 136:533–541
Fujinoki M (2011) Serotonin-enhanced hyperactivation of hamster sperm. Reproduction 142:255–266
Visconti PE, Kopf GS (1998) Regulation of protein phosphorylation during sperm capacitation. Biol Reprod 59:1–6
Visconti PE, Galantino-Homer H, Ning X, Fornes MW, Moore GD, Bailey JL, Kopf GS (1998) The molecular basis of capacitation. J Androl 19:242–248
Ho HC, Suarez SS (2001) An inositol 1,4,5-trisphoshate receptor-gated intracellular Ca2+ store is involved in regulating sperm hyperactivated motility. Biol Reprod 65:1606–1616
Ho HC, Granish KA, Suarez SS (2002) Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP. Dev Biol 250:208–217
Okamura N, Tajima Y, Soejima A, Masuda H, Sugita Y (1985) Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through the direct activation of adenylate cyclase. J Biol Chem 260:9699–9705
Fujinoki M, Suzuki T, Takayama T, Shibahara H, Ohtake H (2006) Profiling of proteins phosphorylated or dephosphorylated during hyperactivation on hamster spermatozoa. Reprod Med Biol 5:123–135
Suzuki T, Fujinoki M, Shibahara H, Suzuki M (2010) Regulation of hyperactivation by PPP2 in hamster spermatozoa. Reproduction 139:847–856
Carrera A, Gerton GL, Moss SB (1994) The major fibrous sheath polypeptide of mouse sperm: structural and functional similarities to the A-kinase anchoring proteins. Dev Biol 165:272–284
Osman RA, Andria ML, Jones AD, Meizel S (1989) Steroid induced exocytosis: the human sperm acrosome reaction. Biochem Biophys Res Commun 160:828–833
Baldi E, Luconi M, Bonaccorsi L, Forti G (1998) Nongenomic effects of progesterone on spermatozoa: mechanisms of signal transduction and clinical implications. Front Biosci 3:1051–1059
Luconi M, Francavilla F, Porazzi I, Macerola B, Forti G, Baldi E (2004) Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens. Steroids 69:553–559
Libersky EA, Boatman DE (1995) Effects of progesterone on in vitro sperm capacitation and egg penetration in the golden hamster. Biol Reprod 53:483–487
Llanos MN, Anabalon MC (1996) Studies related to progesterone-induced hamster sperm acrosome reaction. Mol Reprod Dev 45:313–319
Sabeur K, Edwards DP, Meizel S (1996) Human sperm plasma membrane progesterone receptor(s) and the acrosome reaction. Biol Reprod 54:993–1001
Jang S, Yi LSH (2005) Identification of a 71-kDa protein as a putative non-genomic membrane progesterone receptor in boar spermatozoa. J Endocrinol 184:417–425
Baldi E, Luconi M, Muratori M, Forti G (2000) A novel functional estrogen receptor on human sperm membrane interferes with progesterone effects. Mol Cell Endocrinol 161:31–35
Baldi E, Luconi M, Muratori M, Marchiani S, Tamburrino L, Forti G (2009) Nongenomic activation of spermatozoa by steroid hormones: facts and fictions. Mol Cell Endocrinol 308:39–46
Luconi M, Muratori M, Forti G, Baldi E (1999) Identification and characterization of a novel functional estrogen receptor on human sperm membrane that interferes with progesterone effects. J Clin Endocrinol Metabol 84:1670–1678
Fujinoki M (2010) Suppression of progesterone enhanced hyperactivation in hamster spermatozoa by estrogen. Reproduction 140:453–464
du Plessis SS, Hagenaar K, Lampiao F (2010) The in vitro effects of melatonin on human sperm function and its scavenging activities on NO and ROS. Andrologia 42:112–116
Fujinoki M, Takei GL (2015) Estrogen suppresses melatonin-enhanced hyperactivation of hamster spermatozoa. J Reprd Dev 61:287–295
Calogero AE, Hall J, Fishel S, Green S, Hunter A, D’Agata R (1996) Effects of γ-aminobutyric acid on human sperm motility and hyperactivation. Mol Hum Reprod 2:733–738
de las Heras MA, Valcarcel A, Perez LJ (1997) In vitro capacitating effect of gamma-aminobutyric acid in ram spermatozoa. Biol Reprod 56:964–968
Ritta MN, Calamera JC, Bas DE (1998) Occurrence of GABA and GABA receptors in human spermatozoa. Mol Hum Reprod 4:769–773
Jin J-Y, Chen W-Y, Zhou CX, Chen Z-H, Yuan Y-Y, Ni Y, Chan HC, Shi Q-X (2009) Activation of GABAA receptor/Cl− channel and capacitation in rat spermatozoa: HCO3 − and Cl− are essential. Syst Biol Reprod Med 55:97–108
Kon H, Takei GL, Fujinoki M, Shinoda M (2014) Suppression of progesterone-enhanced hyperactivation in hamster spermatozoa by γ-aminobutyric acid. J Reprod Dev 60:202–209
Meizel S, Turner KO (1983) Serotonin or its agonist 5-methoxytryptamine can stimulate hamster sperm acrosome reactions in a more direct manner than catecholamines. J Exp Zool 226:171–174
Libersky EA, Boatman DE (1995) Progesterone concentration in serum, follicular fluid, and oviductal fluid of the golden hamster during the periovulatory period. Biol Reprod 53:477–482
Lösel R, Wehling M (2003) Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol 4:46–56
Harper CV, Barratt CLR, Publicover SJ (2004) Stimulation of human spermatozoa with progesterone gradients to stimulate approach to the oocyte. J Biol Chem 279:46315–46325
Lishko PV, Botchkina IL, Kirichok Y (2011) Progesterone activates the principal Ca2+ channel of human sperm. Nature 471:387–391
Strünker T, Goodwin N, Brenker C, Kashikar ND, Weyand I, Seifert R, Kaupp UB (2011) The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature 471:382–386
Gadkar S, Shah CA, Sachdeva G, Samant U, Puri CP (2002) Progesterone receptor as an indicator of sperm function. Biol Reprod 67:1327–1336
Fukami K, Yoshida M, Inoue T, Kurokawa M, Fissore RA, Yoshida N, Mikoshiba K, Takenawa T (2003) Phospholipase Cδ4 is required for Ca2+ mobilization essential for acrosome reaction in sperm. J Cell Biol 161:79–88
Harrison DA, Carr DW, 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
Fujinoki M (2013) Progesterone-enhanced sperm hyperactivation through IP3-PKC and PKA signals. Reprod Med Biol 12:27–33
Ignotz GG, Suarez SS (2005) Calcium/calmodulin and calmodulin kinase II stimulate hyperactivation in demembranated bovine sperm. Biol Reprod 73:519–526
Fujinoki M (2014) Regulation and disruption of hamster sperm hyperactivation by progesterone, 17β-estradiol and diethylstilbestrol. Reprod Med Biol 13:143–152
Iguchi T, Watanabe H, Katsu Y, Mizutani T, Miyagawa S, Suzuki A, Kohno S, Sone K, Kato H (2002) Developmental toxicity of estrogenic chemicals on rodents and other species. Congenit Anom 42:94–105
Iguchi T, Watanabe H, Ohta Y, Blumberg B (2008) Developmental effects: oestrogen-induced vaginal changes and organotin-induced adipogenesis. Intern J Androl 31:263–268
Casao A, Mendoza N, Pérez-Pé R, Grasa P, Abecia J-A, Forcada F, Cebrián-Pérez JA, Muino-Blanco T (2010) Melatonin prevents capacitation and apoptotic-like changes of ram spermatozoa and increases fertility rate. J Pineal Res 48:39–46
Espino J, Bejarano I, Ortiz A, Lozano GM, García JF, Pariente JA, Rodríguez AB (2010) Melatonin as a potential tool against oxidative damage and apoptosis in ejaculated human spermatozoa. Fertil Steril 94:1915–1917
Ortiz A, Espino J, Bejarano I, Lozano GM, Mollor F, García JF, Pariente JA, Rodríguez AB (2011) High endogenous melatonin concentrations enhance sperm quality and short-term in vitro exposure to melatonin improves aspects of sperm motility. J Pineal Res 50:132–139
Succu S, Berlinguer F, Pasciu V, Satta V, Leoni GG, Naitana S (2011) Melatonin protects ram spermatozoa from cryopreservation injuries in a dose-dependent manner. J Pineal Res 50:310–318
O’Flaherty C, de Lamirande E, Gagnon C (2006) Positive role of reactive oxygen species in mammalian sperm capacitation: triggering and modulation of phosphorylation events. Free Rad Biol Med 41:528–540
Agarwal A, Makker K, Sharma R (2008) Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immun 59:2–11
de Lamirande E, O’Flaherty C (2008) Sperm activation: role of reactive oxygen species and kinases. Biochim Biophys Acta 1784:106–115
Iwasaki A, Gagnon C (1992) Formation of reactive oxygen species in spermatozoa of infertile patients. Fertil Steril 57:409–416
Bronson FH, Heideman PD (1994) Seasonal regulation of reproduction in mammals. In: Knobil E, Neill JD (eds) The physiology of reproduction, vol 2, 2nd edn. Raven Press, New York
Turek FW, Van Cauter E (1994) Rhythms in reproduction. In: Knobil E, Neill JD (eds) The physiology of reproduction, vol 2, 2nd edn. Raven Press, New York
Noda M, Higashida H, Aoki S, Wada K (2004) Multiple signal transduction pathways mediated by 5-HT receptors. Mol Neurobiol 29:31–39
Ganong WF (2005) Reviews of medical physiology, 22nd edn. McGraw-Hill, New York
Hu JH, He XB, Wu Q, Yan YC, Koide SS (2002) Biphasic effect of GABA on rat sperm acrosome reaction: involvement of GABAA and GABAB receptors. Arch Androl 48:369–378
He X, Zhang Y, Yan Y, Li Y, Koide SS (2003) Identification of GABABR2 in rat testis and sperm. J Reprod Dev 49:397–402
Kanbara K, Okamoto K, Nomura S, Kaneko T, Shigemoto R, Azuma H, Katsuoka Y, Watanabe M (2005) Cellular localization of GABA and GABAB receptor subunit proteins during spermatogenesis in rat testis. J Androl 26:485–493
del Rio RM (1981) Gamma-aminobutyric acid system in rat oviduct. J Biol Chem 256:9816–9819
Louzan P, Gallardo MGP, Tramezzani JH (1986) Gamma-aminobutyric acid in the genital tract of the rat during the oestrous cycle. J Reprod Fertil 77:499–524