Skip to main content

Physiology and Pathophysiology of Electrolyte Transport in the Epididymis

  • Conference paper
Spermatogenesis — Fertilization — Contraception

Part of the book series: Schering Foundation Workshop ((SCHERING FOUND,volume 4))

Abstract

Although it was eighty years ago that early investigators of the func- tions of the epididymis noted certain differences in the characteristics of the spermatozoa obtained from different regions and proposed that spermatozoa undergo a ‘ripening’ process during their epididymal passage (Tournade 1913), it was not until fifty-five years later that the principle of epididymal maturation of spermatozoa was refined with solid experimental supports (Bedford 1967; Orgebin-Crist 1967, 1969). It is now clear that important maturation changes take place in spermatozoa in the epididymis of most mammals including man and that these changes confer on the sperm the ability to fertilize eggs. Despite this, the mechanisms underlying sperm maturation are still obscure. To date, technological advances have made possible the study of epididymal functions at a cellular and molecular level and have brought light to our understanding of the underlying processes. Significant progress has been made in the area of androgen-regulated genes that control the biosynthesis and secretion of epididymal-specific macromolecules which are integral to the maturation of sperm plasma membrane. Interested readers are referred to the following excellent papers on this topic: Brooks 1987; Ghyselinck et al. 1990; Walker et al. 1990. The present chapter describes some studies made in our own laboratory on epididymal transport of electrolytes and fluid. Undoubtedly, this aspect of epididymal function is equally important for the maintenance of a favourable fluid environment on which sperm maturation and storage depend (Wong et al. 1982; Wong 1986). The introduction of cell culture techniques for the rat (Kierzenbaum et al. 1981, Beyers et al. 1986) and human (Cooper et al. 1990) epididymis facilitated study of the mechanism and regulation of electrolyte transport by the epididymis by the formation of an epithelial sheet on which transepithelial electrical (Cuthbert and Wong 1986; Wong 1988a, 1988b, 1988c), isotope flux (Fu et al. 1990) and microfluorescence (Wong and Huang 1990) measurements can be made on single cells as well as on cell monolayers. Furthermore, epididymal cell culture also permits access of patch-clamp pipettes to the luminal side of the epithelium so that the conductive properties of this membrane and its activation by intracellular messengers can be studied (Cook et a1.1990; Wong 1990c).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Anderson MP, Rich DP, Gregory RJ, Smith AE, Welsh MJ (1991) Generation of cAMP-oporated chloride currents by expression of CFTR. Science 251: 679–682

    Article  PubMed  CAS  Google Scholar 

  • Au CL, Ngai HK, Yeung CH, Wong PYD (1978) Effect of adrenalectomy and hormone replacement on sodium and water transport in the perfused rat cauda epididymidis. J Endocrinol 77: 265–266

    Article  PubMed  CAS  Google Scholar 

  • Bedford JM (1967) Effects of duct ligation on the fertilizing ability of spermatozoa from different regions of the rabbit epididymis. J Exp Zool 166: 271–282

    Article  PubMed  CAS  Google Scholar 

  • Berger HA, Anderson MP, Gregory RJ, Smith AE, Welsh MJ (1991) The single channel basis of CFTR generated chloride currents. Pediatric Pulmonology Supp16: 250

    Google Scholar 

  • Beyers SW, Hadley MA, Djakiew D, Dym M (1986) Growth and characterization of polarized monolayers of epididymal epithelial cells and Sertoli cells in dual environment chambers. J Androl 7: 59–68

    Google Scholar 

  • Boucher RC, Cheng EHC, Paradiso AM, Stutts MJ, Knowles MR, Earp HS (1989) Chloride secretory response in cystic fibrosis human airway epithelia. Preservation of calcium but not protein kinase C and A dependent mechanisms. J Clin Invest 84: 1424–1431

    Google Scholar 

  • Brooks DE (1987) Developmental expression and androgenic regulation of the messenger RNA for major secretory proteins of the rat epididymis. Mol Cell Endocrinol 53: 59–66

    Article  PubMed  CAS  Google Scholar 

  • Cliff WH, Frizzell RA (1990) Seperate Cl-conductances activated by cAMP and Cat+ in Cf -secreting epithelial cells. Proc Natl Acad Sci USA 87: 4956–4960

    Article  PubMed  CAS  Google Scholar 

  • Cohn JA, Melhus O, Vigna SR, Rigby MR, Marino CR. (1991) Immunocytochemical and phosphorylation studies of Cl-TR. Pediatr Pulmonol Supp16: 229

    Google Scholar 

  • Coleman L, Harris A (1991) Immortalization of male genital duct epithelium: an assay system for the cystic fibrosis gene. J. Cell Sci 98: 85–89

    PubMed  Google Scholar 

  • Cook DI, Huang SJ, Wilson SM, Wong PYD, Young JA (1990) Ion channels in the apical membrane of the rat cauda epididymides. J Physiol 423: 57 P

    Google Scholar 

  • Cooper TG, Yeung CH, Meyer R, Schulze S (1990) Maintenance of human epididymal epithelial cell function in monolayer culture. J Reprod Fertil 90: 81–91

    Article  PubMed  CAS  Google Scholar 

  • Cotton CU, Stutts MJ, Knowles MR, Gatzy JT, Boucher RC (1987) Abnormal apical cell membrane in cystic fibrosis respiratory epithelium. An in vitro electrophysiological analysis. J Clin Invest 79: 80–85

    Article  PubMed  CAS  Google Scholar 

  • Cuthbert AW, Wong PYD (1986) Electrogenic anion secretion in cultured rat epididymal epithelium. J Physiol 378: 335–346

    PubMed  CAS  Google Scholar 

  • Di Sant’Agnese PA, Talamo RC (1967) Pathogenesis and physiopathology of cystic fibrosis of the pancreas: fibrocystic disease of the pancreas (mucoviscidosis). N Engl J Med 277: 1287–1294

    Article  PubMed  Google Scholar 

  • Donowitz M, Welsh MJ (1986) Ca and cyclic AMP in regulation of intestinal Na, K, and.Cl transport. Annu Rev Physiol 48: 135–150

    Google Scholar 

  • El-Badawi A, Schenk EA (1967) The distribution of cholinergic and adrenergic nerves in the mammalian epididymis. Am J Anat 121: 1–14

    Article  PubMed  CAS  Google Scholar 

  • Frizzell RA, Rechkemmer G, Shoemaker RL (1986) Altered regulation of air- way epithelial cell chloride channels in cystic fibrosis. Science 233: 558–560

    Article  PubMed  CAS  Google Scholar 

  • Fu WO, Huang SJ, Wilson SM, Wong PYD. (1990) Adrenaline stimulates Rb+ efflux from the apical and basolateral membranes of the cultured epididymal monolayers. J Physiol 423: 50 P

    Google Scholar 

  • Ghyselinck NB, Jimenez C, Lefrancois AM, Dufaure JP (1990) Molecular cloning of cDNA for androgen-regulated proteins secreted by the mouse epididymis. J Mol Endocrinol 4: 5–12

    Article  PubMed  CAS  Google Scholar 

  • Gray MA, Greenwell JR, Argent BE (1988) Secretin-regulated chloride channel on the apical plasma membrane of pancreatic duct cells. J Membr Biol 105: 131–142

    Article  PubMed  CAS  Google Scholar 

  • Gray MA, Pollard CE, Harris A, Colemen L, Greenwell JR, Argent BE (1990) Anion selectivity and block of the small conductance chloride channel on pancreatic duct cells. Am J Physiol 259: 752–761

    Google Scholar 

  • Handelsman DJ, Conway AJ, Boylan LM, Turtle JR (1984) Young’s syndrome: obstructive azoospermia and chronic sinopulmonary infections. N Engl J Med 310: 3–9

    Article  PubMed  CAS  Google Scholar 

  • Hanley MR, Jackson TR, Cheung WT, Dreher M, Gatti A, Hawkins P, Patterson SI, Vallejo M, Dawson, AP, Thastrup 0 (1988) Molecular mechanisms of phospholipid signaling pathways in mammalian nerve cells. Cold Spring Harbor Symp Quant Biol 53: 435–445

    Article  CAS  Google Scholar 

  • Hendry WF, Knight RK, Whitfield HN, Stanfield AG, Pryse-Davies J, Ryder TA, Pavia D, Bateman JR, Clarke SW (1978) Obstructive azoospermia: respiratory function tests, electron microscopy and the results of surgery. B J Urol 50: 598–604

    Article  CAS  Google Scholar 

  • Huang SJ, Fu WO, Chung YW, Leung AYH, Wong PYD (1991) Adrenaline stimulates whole-cell chloride current in cultured rat epididymal cells. In: Murakami M, Seo Y, Kuwahara A, Watari H (eds) Ionic basis and energy metabolism of epithelial transport–hot aspects from exocrine secretion. National Institute for Physiological Sciences, Okazaki, Japan, pp. 229–230

    Google Scholar 

  • Kaplan E, Shwachman H, Perlmutter AD, Rule A, Khaw KT, Holsclaw DS (1968) Reproductive failure in males with cystic fibrosis. N Engl J Med 279: 65–69

    Article  PubMed  CAS  Google Scholar 

  • Kerem B, Rommens JM, Buchanan JA, et al. (1989) Identification of the cystic fibrosis gene: genetic analysis. Science 245: 1073–1080

    Article  PubMed  CAS  Google Scholar 

  • Kierzenbaum AL, Lea O, Petrusz P, French FS, Tres LL (1981) Isolation, culture, and immunocytochemical characterization of epididymal epithelial cells from pubertal and adult rats. Proc Natl Acad Sci USA 78: 1675–1679

    Article  Google Scholar 

  • Liedtke C (1989) Regulation of chloride transport in epithelia, Annu Rev Physiol 51: 143–160

    Article  PubMed  CAS  Google Scholar 

  • Leung AYH, Leung PY, Cheng-Chew SB, Wong PYD (1992) The role of calcitonin gene-related peptide in the regulation of anion secretion by the rat and human epididymis. J Endocrinol (in press)

    Google Scholar 

  • Levine N, Marsh DJ (1971) Micropuncture studies of the electrochemical aspects of fluid and electrolyte transport in individual seminiferous tubules, the epididymis and vas deferens in rats. J Physiol 213: 557–570

    PubMed  CAS  Google Scholar 

  • McCann JD, Matsuda J, Garcia M, Kaczorowski G, Welsh MJ (1990) Basolateral K+ channels in airway epithelia. I. Regulation by Cat+ and blocked by charybdotoxin. Am J Physiol 258: L334–342

    PubMed  CAS  Google Scholar 

  • Neville E, Brewis R, Yeates WK, Burridge A (1983) Respiratory tract disease and obstructive azoospermia. Thorax 38: 929–933

    Article  PubMed  CAS  Google Scholar 

  • Orgebin-Crist M-C (1967) Sperm maturation in rabbit epididymis. Nature 216: 816–818

    Article  PubMed  CAS  Google Scholar 

  • Orgebin-Crist M-C (1969) Studies on the function of the epididymis. Biol Re-prod 1: 155–175

    Article  Google Scholar 

  • Pollard CE, Harris A, Coleman L, Argent BE (1992) Chloride channels on epi- thelial cells cultured from human fetal epididymis. J Mem Biol (in press)

    Google Scholar 

  • Puchelle E, Gaillard D, Hinnrasky J, Fuchey C, Boutterin MC, Jallat J, Slos P, et al. (1991) Immunocytochemical localization of CFTR in normal and CF human respiratory epithelium. Pediatr Pulmonol Suppl 6: 257

    Google Scholar 

  • Putney JW Jr (1985) Identification of cellular activation mechanisms associated with salivary secretion. Ann Rev Physiol 48: 75–88

    Article  Google Scholar 

  • Reddy MM, Bell CL, Quinton PM (1991) Anion selectivity of Cl-conductance affected by cystic fibrosis as an in vitro diagonstic tool. Pediatric Pulmonology Suppl 6: 251

    Google Scholar 

  • Rich DP, Anderson MP, Gregory RJ, Cheng SH, Paul S, Jefferson DM et al. (1990) Expression of cystic fibrosis transmembrane conductance regulator corrects defective chloride channel regulation in cystic fibrosis airway epithelial cells. Nature 347: 358–363

    Article  PubMed  CAS  Google Scholar 

  • Riordan JR, Rommens JM, Kerem B, Zielenski J, Lok S, Playsic N, Chou JL, Drumm ML, Iannuzzi MC et al. (1989) Identification of the cystic fibrosis gene: cloning and charcaterization of the complementary DNA. Science 245: 1066–1072

    Article  PubMed  CAS  Google Scholar 

  • Rommens JM, Iannuzzi MC, Kerem B et al. (1989) Identification of the cystic fibrosis gene: chromosomal walking and jumping. Science 243: 1059–1065

    Article  Google Scholar 

  • Schoumacher RA, Shoemaker RL, Halm DR, Tallant EA, Wallace RW, Frizzell RA (1987) Phosphorylation fails to activate chloride channels from cystic fibrosis airway cells. Nature 330: 752–754

    Article  PubMed  CAS  Google Scholar 

  • Seale TW, Flux M, Rennert OM (1985) Reproductive defects in patients of both sexes with cystic fibrosis: a review. Am Clin Lab Sci 15: 152–158

    CAS  Google Scholar 

  • Sjöstrand NO (1965) The adrenergic innervation of the vas deferens and the accessory male genital glands. Acta Physiol Scand 65 Suppl 257

    Google Scholar 

  • Thastrup 0, Dawson AP, Scharff O, Foder B, Cullen PJ, Drobak BK, Bjerrum PJ, Christensen SB, Hanley MR (1989) Thapsigargin, a novel molecular probe for studying intracellular calcium release and storage. Agents Action 27: 17–23

    Article  CAS  Google Scholar 

  • Tournade A (1913) Différence de motilité des spermatozoides prélevés dans les divers segments de l’épididyme. Comptes Rendu de la Soc de Biologie, Paris 74: 738–740

    Google Scholar 

  • Turner TT, Hartmann PK, Howards SS (1977) In vivo sodium, potassium, and sperm concentrations in the rat epididymis. Fert Steril 28: 191–194

    Google Scholar 

  • Walker JE, Jones R, Moore A, Hamilton, DW, Hall L (1990) Analysis of major androgen-regulated cDNA clones from the rat epididymis. Mol Cell Endocrinol 74: 61–68

    Article  PubMed  CAS  Google Scholar 

  • Wang C, So SY, Wong KK, So WWK, Chan SYW (1987) Chronic sinopulmonary disease in Chinese patients with obstructive azoospermia. J Androl 8: 225–229

    PubMed  CAS  Google Scholar 

  • Welsh MJ (1987) Electrolyte transport by airway epithelia. Physiol Rev 67: 1143–1184

    PubMed  CAS  Google Scholar 

  • Welsh MJ, Liedtke CM (1986) Chloride and potassium channels in cystic fibrosis airway epithelia. Nature 322: 467–470

    Article  PubMed  CAS  Google Scholar 

  • Wen RQ, Wong PYD (1988) Reserpine treatment increases viscosity of fluid in the epididymis of rats. Biol Reprod 38: 969–974

    Article  PubMed  CAS  Google Scholar 

  • Widdicombe JH, Welsh MJ, Finkbeiner WE (1985) Cystic fibrosis decreases the apical membrane chloride permeability of monolayers cultured from cells of tracheal epithelium. Proc Natl Acad Sci 82: 6167–6171

    Article  PubMed  CAS  Google Scholar 

  • Wong PYD (1986) Fluid transport and sperm maturation in the epididymis. Biomed Res 7, Suppl 2: 233–240

    Google Scholar 

  • Wong PYD (1988a) Mechanism of adrenergic stimulation of anion secretion in cultured rat epididymal epithelium. Am J Physiol 254: F121 - F133

    PubMed  CAS  Google Scholar 

  • Wong PYD (1988b) Inhibition by chloride channel blockers of anion secretion in cultured rat epididymal epithelium. Brit J Pharmacol 94: 155–163

    Article  CAS  Google Scholar 

  • Wong PYD (1988c) Control of anion and fluid secretion by apical P2-purinoceptors in the rat epididymis. Brit J Pharmacol 95: 1315–1312

    Article  CAS  Google Scholar 

  • Wong PYD (1989) Potassium channel blockers inhibit anion secretion in cultured rat epididymal epithelium. Jap J Physiol 39: 595–607

    Article  CAS  Google Scholar 

  • Wong PYD (1990) Electrolyte and fluid transport in the epididymis. In: Young JA, Wong PYD (eds) Epithelial secretion of water and electrolytes. Springer Verlag, Berlin, Heidelberg, pp 333–347

    Google Scholar 

  • Wong PYD, Chan TPT (1988) Adrenergic control of electrogenic anion secretion by primary cultures of rat epididymal cells. In: Davison JS, Shaffer EA (eds) Gastrointestinal and hepatic secretion. University of Calgary Press, Canada, pp. 216–219

    Google Scholar 

  • Wong PYD, Huang SJ (1989) Intracellular pH measurement in primary mono-layer cultures of rat epididymal cells. Pflügers Arch 413: 414–421

    Article  PubMed  CAS  Google Scholar 

  • Wong PYD, Huang SJ (1990) Secretory agonists stimulate a rise in intracellular cyclic AMP but not Cat+ and inositol phosphates in cultured rat epididymal epithelium. Expl Physiol 75: 321–337

    CAS  Google Scholar 

  • Wong PYD, Uchendu CN (1990) The role of angiotensin-converting enzyme in the rat epididymis. J Endocrinol 125: 457–465

    Article  PubMed  CAS  Google Scholar 

  • Wong PYD, Uchendu CN (1991) Studies of the renin-angiotensin system in primary cultures of the rat epididymis. J Endocrinol, 131: 287–293

    Article  PubMed  CAS  Google Scholar 

  • Wong PYD, Yeung CH (1976) Inhibition by amiloride of the sodium dependent fluid reabsorption in isolated rat cauda epididymidis. Brit. J. Pharmac. 58, 529–532

    Google Scholar 

  • Wong PYD, Yeung CH (1977a) Hormonal regulation of fluid reabsorption in isolated rat cauda epididymidis. Endocrinol 101: 1391–1397

    Article  CAS  Google Scholar 

  • Wong PYD, Yeung CH (1977b) Inhibition by a-chlorohydrin of fluid reabsorption in the rat cauda epididymidis. J Reprod Fert 51: 469–471

    Article  CAS  Google Scholar 

  • Wong PYD, Yeung CH (1977c) Fluid reabsorption in isolated duct of the rat cauda epididymidis. J Reprod Fert 49: 77–81

    Article  CAS  Google Scholar 

  • Wong PYD, Yeung CH (1978) Absorptive and secretory functions of the per-fused rat cauda epididymidis. J Physiol 275: 13–26

    PubMed  CAS  Google Scholar 

  • Wong PYD, Yeung CH, Ngai HK (1977) Effect of a-chlorohydrin on transport processes in perfused rat cauda epididymidis. Contraception 16: 637642

    Google Scholar 

  • Wong PYD, Au CL, Bedford JM (1982) Biology of the scrotum ( II) Suppression by abdominal temperature of transepithelial ion and water transport in the cauda epididymidis. Biol Reprod 26: 683–689

    Google Scholar 

  • Wong PYD, Fu WO, Huang SJ (1989) Endothelin stimulates anion secretion in a cultured epithelium. Br J Pharmacol 98: 191–196

    Article  Google Scholar 

  • Wong PYD, Fu WO, Huang SJ (1990a) Measurement of chloride transport pool in rat epididymal cells using short circuit current transients after bumetanide. In: Wong, PYD, Young JA (eds) Exocrine Secretion H. International Symposium on Exocrine Secretion, Hong Kong, pp 133–138

    Google Scholar 

  • Wong PYD, Huang SJ, Fu WO, Law WK (1990b) Effect of angiotensins on electrogenic anion transport in monolayer cultures of rat epididymis. J Endocrinol 125: 448–456

    Google Scholar 

  • Wong PYD, Huang SJ, Jones AO, Cook DI, Young JA (1990c) A large conductance K channel from the apical membrane of the rat epididymal epithelium. Pediatric Pulmonology Suppl 5: 215

    Google Scholar 

  • Wong PYD, Cheng-Chew SB, Leung PY, Qin DN (1991a) Functional study and immunocytochemical identification of endothelin in cultured epididymal cells and intact epididymis of the rat. J Cardio Pharmacol 17 Suppl 7: S241–244

    Google Scholar 

  • Wong PYD, Huang SJ, Leung AYH, Fu WO, Chung YW, Chan PSF (1991b) Adrenaline stimulates short-circuit current and whole-cell chloride current in cultured human epididymal cells. Pediatric Pulmonology Suppl 6: 262

    Google Scholar 

  • Wong PYD, Uchendu CN, Huang SJ, Fu WO, Leung AYH, Chung YW (1991c) Local regulation of of ion transport in the epididymis. In: Murakami M, Seo Y, Kuwahara A, Watari H (eds) Ionic basis and energy metabolism of epithelial transport–hot aspects from exocrine secretion. National Institute for Physiological Sciences, Okazaki Japan, pp 153–156

    Google Scholar 

  • Wong YC, Wong PYD, Yeung CH (1978) Ultrastructural correlation of water reabsorption in isolated rat cauda epididymidis. Experentia 34: 485–487

    Article  CAS  Google Scholar 

  • Young D (1970) Surgical treatment of male infertility. J Reprod Fertil 23: 541542

    Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1992 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Wong, P.Y.D. et al. (1992). Physiology and Pathophysiology of Electrolyte Transport in the Epididymis. In: Nieschlag, E., Habenicht, UF. (eds) Spermatogenesis — Fertilization — Contraception. Schering Foundation Workshop, vol 4. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-02815-5_13

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-02815-5_13

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-02817-9

  • Online ISBN: 978-3-662-02815-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics