Bicarbonate secretion by the female reproductive tract and its impact on sperm fertilizing capacity

( views:96, downloads:0 )
Author:
ZHOU Chen-Xi()
WANG Xiao-fei()
CHAN Hsiao-Chang()
Journal Title:
ACTA PHYSIOLOGICA SINICA
Issue:
Volume 57, Issue 02, 2005
DOI:
Key Word:
endometrium;epithelium;secretion;bicarbonate;spermmatozoa

Abstract: The luminal fluid environment of the female reproductive tract is considered critical for the sperm to undergo a series of molecular events leading to the final acquisition of their fertilizing capacity. It has been shown that the fluid in the female reproductive tract contains high content of HCO3- and it plays an important role in sperm functions including sperm motility, capacitation, hyperactivation and acrosome reaction. This review summarizes the effects of HCO3- on sperm functions occurring in the female reproductive tract and discusses the transport mechanisms involved in mediating uterine HCO3- secretion. New evidence is also presented to show possible cause of female infertility due to defective HCO3- transporting mechanism.

  • [1]Levine N, Marsh DJ. Micropuncture studies of the electrochemical aspects of fluid and electrolyte transport in individual seminiferous tubules, the epididymis and the vas deferens in rats. J Physiol 1971; 213(3): 557-570.
  • [2]Levine N, Kelly H. Measurement of pH in the rat epididymis in vivo. J Reprod Fertil 1978; 52(2): 333-335.
  • [3]Caflisch CR, DuBose TD Jr. Effect of vasectomy on in situ pH in rat testis and epididymis. Contraception 1990; 42(5): 589-595.
  • [4]Rodriguez-Martinez H, Ekstedt E, Einarsson S. Acidification of epididymal fluid in the boar. Int J Androl 1990; 13(3): 238-243.
  • [5]Okamura N, Tajima Y, Soejima A, Masuda H, Sugita Y. Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase.J Biol Chem 1985; 260(17): 9699-9705.
  • [6]Jensen LJ, Stuart-Tilley AK, Peters LL, Lux SE, Alper SL, Breton S.Immunolocalization of AE2 anion exchanger in rat and mouse epididymis.Biol Reprod 1999;61(4):973-980.
  • [7]Vishwakarma P. The pH and bicarbonate-ion content of the oviduct and uterine fluids. Fertil Steril 1962; 13:481-485.
  • [8]Murdoch RN, White IG. The influence of the female genital tract on the metabolism of rabbit spermatozoa. I. Direct effect of tubal and uterine fluids, bicarbonate, and other factors. Aust J Biol Sci 1968; 21(5): 961-972.
  • [9]Visconti PE, Stewart-Savage J, Blasco A, Battaglia L, Miranda P,Kopf GS, Tezon JG. Roles of bicarbonate, cAMP, and protein tyrosine phosphorylation on capacitation and the spontaneous acrosome reaction of hamster sperm. Biol Reprod 1999; 61(1):76-84.
  • [10]Okamura N, Sugita Y. Activation of spermatozoan adenylate cyclase by a low molecular weight factor in porcine seminal plasma. J Biol Chem 1983; 258(21): 13056-13062.
  • [11]Tajima Y, Okamura N, Sugita Y. The activating effects of bicarbonate on sperm motility and respiration at ejaculation. Biochim Biophys Acta 1987; 924(3): 519-529.
  • [12]Mann T, Lutwak-Mann C. Passage of chemicals into human and animal semen: mechanisms and significance. Crit Rev Toxicol 1982; 11(1): 1-14.
  • [13]Jones RC, Murdoch RN. Regulation of the motility and metabolism of spermatozoa for storage in the epididymis of eutherian and marsupial mammals. Reprod Fertil Dev 1996; 8(4): 553-568.
  • [14]Abaigar T, Holt WV, Harrison RA, del Barrio G. Sperm subpopulations in boar (Sus scrofa) and gazelle (Gazella dama mhorr)semen as revealed by pattern analysis of computer-assisted motility assessments. Biol Reprod 1999; 60(1): 32-41.
  • [15]Holt WV, Harrison RA. Bicarbonate stimulation of boar sperm motility via a protein kinase A-dependent pathway: betweencell and between-ejaculate differences are not due to deficiencies in protein kinase A activation. J Androl 2002; 23(4): 557-565.
  • [16]Wennemuth G, Carlson AE, Harper AJ, Babcock DF. Bicarbonate actions on flagellar and Ca2+-channel responses: initial events in sperm activation. Development 2003; 130(7): 1317-1326.
  • [17]Aitken RJ. Possible redox regulation of sperm motility activation.J Andro12000; 21(4): 491-496.
  • [18]Armstrong VL, Clulow J, Murdoch RN, Jones RC. Intracellular signal transduction mechanisms of rat epididymal spermatozoa and their relationship to motility and metabolism. Mol Reprod Dev 1994; 38(1): 77-84.
  • [19]Wennemuth G. Bicarbonate action on early events in sperm activation. Ann Anat 2004; 186(4): 293-294.
  • [20]Aitken RJ, Harkiss D, Knox W, Paterson M, Irvine S. On the cellular mechanisms by which the bicarbonate ion mediates the extragenomic action of progesterone on human spermatozoa.Biol Reprod 1998; 58(1): 186-196.
  • [21]Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 2000; 289(5479): 625-628.
  • [22]Jaiswal BS, Conti M. Identification and functional analysis of splice variants of the germ cell soluble adenylyl cyclase. J Biol Chem 2001; 276(34): 31698-31708.
  • [23]Gross MK, Toscano DG, Toscano WA Jr. Calmodulin-mediated adenylate cyclase from mammalian sperm. J Biol Chem 1987;262(18): 8672-8676.
  • [24]Wennemuth G, Westenbroek RE, Xu T, Hille B, Babcock DF.CaV2.2 and CaV2.3 (N- and R-type) Ca2+ channels in depolarization-evoked entry of Ca2+ into mouse sperm. J Biol Chem 2000;275(28): 21210-21217.
  • [25]Esposito G, Jaiswal BS, Xie F, Krajnc-Franken MA, Robben TJ, Strik AM, Kuil C, Philipsen RL, van Duin M, Conti M,Gossen JA, Jaiswal BS. Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc Natl Acad Sci USA 2004; 101(9): 2993-2998.
  • [26]Austin CR. The development of pro-nuclei in the rat egg, with particular reference to quantitative relations. Aust J Sci Res 1952;5(3): 354-365.
  • [27]Chang MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 1951; 168(4277): 697-698.
  • [28]Lee MA, Storey BT. Bicarbonate is essential for fertilization of mouse eggs: mouse sperm require it to undergo the acrosome reaction. Biol Reprod 1986; 34(2): 349-356.
  • [29]Neill JM, Olds-Clarke P. A computer-assisted assay for mouse sperm hyperactivation demonstrates that bicarbonate but not bovine serum albumin is required. Gamete Res 1987; 18(2): 121-140.
  • [30]Shi QX, Roldan ER. Bicarbonate/CO2 is not required for zona pellucida- or progesterone-induced acrosomal exocytosis of mouse spermatozoa but is essential for capacitation. Biol Reprod 1995;52(3): 540-546.
  • [31]Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation.Development 1995; 121(4): 1129-1137.
  • [32]Boatman DE. Responses of gametes to the oviductal environment.Hum Reprod 1997; 12(11 Suppl): 133-149.
  • [33]Vishwakarma P. The pH and bicarbonate-ion content of the oviduct and uterine fluids. Fertil Steril 1962; 13: 481-485.
  • [34]Murdoch RN, White IG. The influence of the female genital tract on the metabolism of rabbit spermatozoa. I. Direct effect of tubal and uterine fluids, bicarbonate, and other factors. Aust J Biol Sci 1968; 21(5): 961-972.
  • [35]Uguz C, Vredenburgh WL, Parrish JJ. Heparin-induced capacitation but not intracellular alkalinization of bovine sperm is inhibited by Rp-adenosine-3',5'-cyclic monophosphorothioate. Biol Reprod 1994; 51(5): 1031-1039.
  • [36]Zeng Y, Oberdorf JA, Florman HM. pH regulation in mouse sperm: identification of Na+-, C1--, and HCO3-dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Dev Biol 1996;173(2): 510-520.
  • [37]Meizel S, Deamer DW. The pH of the hamster sperm acrosome.J Histochem Cytochem 1978; 26(2): 98-105.
  • [38]Parrish JJ, Susko-Parrish JL, First NL. Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH. Biol Reprod 1989; 41(4): 683-699.
  • [39]Harrison RA, Ashworth PJ, Miller NG. Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev 1996; 45(3): 378-391.
  • [40]Ashworth PJ, Harrison RA, Miller NG, Plummer JM, Watson PF. Flow cytometric detection of bicarbonate-induced changes in lectin binding in boar and ram sperm populations. Mol Reprod Dev 1995; 40(2): 164-176.
  • [41]Gadella BM, Harrison RA. The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. Development 2000; 127(11): 2407-2420.
  • [42]Zeng Y, Clark EN, Florman HM. Sperm membrane potential:hyperpolarization during capacitation regulates zona pellucidadependent acrosomal secretion. Dev Biol 1995; 171(2): 554-563.
  • [43]Demarco IA, Espinosa F, Edwards J, Sosnik J, De La VegaBeltran JL, Hockensmith JW, Kopf GS, Darszon A, Visconti PE. Involvement of a Na+/HCO3- cotransporter in mouse sperm capacitation. J Biol Chem 2003; 278(9): 7001-7009.
  • [44]Garty NB, Salomon Y. Stimulation of partially purified adenylate cyclase from bull sperm by bicarbonate. FEBS Lett 1987;218(1): 148-152.
  • [45]Visconti PE, Muschietti JP, Flawia MM, Tezon JG. Bicarbonate dependence of cAMP accumulation induced by phorbol esters in hamster spermatozoa. Biochim Biophys Acta 1990; 1054(2): 231-236.
  • [46]Weyand I, Godde M, Frings S, Weiner J, Muller F, Altenhofen W, Hatt H, Kaupp UB. Cloning and functional expression of a cyclic-nucleotide-gated channel from mammalian sperm. Nature 1994; 368(6474): 859-863.
  • [47]Cook SP, Babcock DF. Activation of Ca2+ permeability by cAMP is coordinated through the pHi increase induced by speract. J Biol Chem 1993; 268(30): 22408-22413.
  • [48]Yanagimachi R. Mammalian fertilization. The physiology of reproduction. New York: Raven Press Ltd., 1994.
  • [49]Neill JM, Olds-Clarke P. A computer-assisted assay for mouse sperm hyperactivation demonstrates that bicarbonate but not bovine serum albumin is required. Gamete Res 1987; 18(2): 121-140.
  • [50]Suarez SS. Hyperactivated motility in sperm. J Androl 1996; 17(4): 331-335.
  • [51]Suarez SS, Katz DF, Owen DH, Andrew JB, Powell RL. Evidence for the function of hyperactivated motility in sperm. Biol Reprod 1991; 44(2): 375-381.
  • [52]Pacey AA, Davies N, Warren MA, Barratt CL, Cooke ID.Hyperactivation may assist human spermatozoa to detach from intimate association with the endosalpinx. Hum Reprod 1995;10(10): 2603-2609.
  • [53]Ho HC, Suarez SS. Hyperactivation of mammalian spermatozoa:function and regulation. Reproduction 2001; 122(4): 519-526.
  • [54]Stauss CR, Votta TJ, Suarez SS. Sperm motility hyperactivation facilitates penetration of the hamster zona pellucida. Biol Reprod 1995; 53(6): 1280-1285.
  • [55]Boatman DE, Robbins RS. Bicarbonate: carbon-dioxide regulation of sperm capacitation, hyperactivated motility, and acrosome reactions. Biol Reprod 1991; 44(5): 806-813.
  • [56]Sabeur K, Meizel S. Importance of bicarbonate to the progesterone-initiated human sperm acrosome reaction. J Androl 1995; 16(3): 266-271.
  • [57]Harrison RA, Ashworth PJ, Miller NG. Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev 1996; 45(3): 378-391.
  • [58]Kulanand J, Shivaji S. Capacitation-associated changes in protein tyrosine phosphorylation, hyperactivation and acrosome reaction in hamster spermatozoa. Andrologia 2001; 33(2): 95-104.
  • [59]Spira B, Breitbart H. The role of anion channels in the mechanism of acrosome reaction in bull spermatozoa. Biochim Biophys Acta 1992; 1109(1): 65-73.
  • [60]Murdoch RN, Davis WD. Effects of bicarbonate on the respiration and glycolytic activity of boar spermatozoa. Aust J Biol Sci 1978; 31(4): 385-394.
  • [61]Okamura N, Tajima Y, Sugita Y. Decrease in bicarbonate transport activities during epididymal maturation of porcine sperm.Biochem Biophys Res Commun 1988; 157(3): 1280-1287.
  • [62]Hyne RV. Bicarbonate- and calcium-dependent induction of rapid guinea pig sperm acrosome reactions by monovalent ionophores.Biol Reprod 1984; 31(2): 312-323.
  • [63]Tajima Y, Okamura N. The enhancing effects of anion channel blockers on sperm activation by bicarbonate. Biochim Biophys Acta 1990; 1034(3): 326-332.
  • [64]Lorenson MY, Lee YC, Jacobs LS. Identification and characterization of an anion-sensitive Mg2+-ATPase in pituitary secretory granule membranes. J Biol Chem 1981; 256(24): 12802-12810.
  • [65]Demarco IA, Espinosa F, Edwards J, Sosnik J, De La VegaBeltran JL, Hockensmith JW, Kopf GS, Darszon A, Visconti PE. Involvement of a Na+/HCO3- cotransporter in mouse sperm capacitation. J Biol Chem 2003; 278(9): 7001-7009.
  • [66]Blandau R, Jensen L, Rumery R. Determination of the pH values of the reproductive-tract fluids of the rat during heat. Fertil Steril 1958; 9(3): 207-214.
  • [67]Matthews CJ, Redfern CP, Hirst BH, Thomas EJ. Characterization of human purified epithelial and stromal cells from endometrium and endometriosis in tissue culture. Fertil Steril 1992;57(5): 990-997.
  • [68]Levin RJ, Phillips JC. Rat endometrial bioelectric activity in vivo and in vitro: effects of adrenaline. J Physiol 1983; 336: 465-478.
  • [69]Vetter AE, O'Grady SM. Mechanisms of electrolyte transport across the endometrium. Ⅱ. Regulation by GRP and substance P.Am J Physiol 1997; 273(1 Pt 1): C67-C76.
  • [70]Chan HC, Fong SK, So SC, Chung YW, Wong PY. Stimulation of anion secretion by beta-adrenoceptors in the mouse endometrial epithelium. J Physiol 1997 15; 501 (Pt 3): 517-525.
  • [71]Fong SK, Liu CQ, Chan HC. Cellular mechanisms of adrenalinestimulated anion secretion by the mouse endometrial epithelium.Biol Reprod 1998; 59(6): 1342-1348.
  • [72]Wang XF, Yu MK, Leung KM, Yip CY, Ko WH, Liu CQ, Chan HC. Involvement of Na+-HCO3- cotransporter in mediating cyclic adenosine 3',5'-monophosphate-dependent HCO3- secretion by mouse endometrial epithelium. Biol Reprod 2002; 66(6): 1846-1852.
  • [73]Wang XF, Yu MK, Lam SY, Leung KM, Jiang JL, Leung PS, Ko WH, Leung PY, Chew SB, Liu CQ, Tse CM, Chan HC.Expression, immunolocalization, and functional activity of Na+/H+ exchanger isoforms in mouse endometrial epithelium. Biol Reprod 2003; 68(1): 302-308.
  • [74]Quinton PM. Physiological basis of cystic fibrosis: a historical perspective. Physiol Rev 1999; 79(1 Suppl): S3-S22.
  • [75]Choi JY, Muallem D, Kiselyov K, Lee MG, Thomas PJ, Muallem S. Aberrant CFTR-dependent HCO3- transport in mutations associated with cystic fibrosis. Nature 2001; 410: 94-97.
  • [76]Schultz BD, Singh AK, Devor DC, Bridges RJ. Pharmacology of CFTR chloride channel activity. Physiol Rev 1999; 79(1 Suppl):S109-S144.
  • [77]Chan LN, Tsang LL, Rowlands DK, Rochelle LG, Boucher RC,Liu CQ, Chan HC. Distribution and regulation of ENaC subunit and CFTR mRNA expression in murine female reproductive tract. J Membr Bio12002; 185(2): 165-176.
  • [78]Oppenheimer EA, Case AL, Esterly JR, Rothberg RM. Cervical mucus in cystic fibrosis: a possible cause of infertility. Am J Obstet Gynecol 1970; 108: 673-674.
  • [79]Epelboin S, Hubert D, Patrat C, Abirached F, Bienvenu T, Lepercq J. Management of assisted reproductive technologies in women with cystic fibrosis. Fertil Steri12001; 76: 1280-1281.
WanfangData CO.,Ltd All Rights Reserved
About WanfangData | Contact US
Healthcare Department, Fuxing Road NO.15, Haidian District Beijing, 100038 P.R.China
Tel:+86-010-58882616 Fax:+86-010-58882615 Email:yiyao@wanfangdata.com.cn