Skip to main content
Log in

Chloride channels in the luminal membrane of the rectal gland of the dogfish (Squalus acanthias)

Properties of the “larger” conductance channel

  • Transport Processes, Metabolism and Endocrinology; Kidney, Gastrointestinal Tract, and Exocrine Glands
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

The rectal gland of the dogfish (Squalus acanthias) secretes chloride via a chloride channel present in the apical cell membrane. Using the patch clamp technique in isolated perfused rectal gland tubules [7], two types of chloride channels are demonstrable in the apical membrane of cyclic AMP treated tubule segments. A small channel of about 11 pS and another channel of 40–50 pS are present. The small channel is described in the succeeding report. With NaCl on both sides (excised patches) the current amplitude of the larger channel is an almost linear function of the voltage (±50 mV). However, the open probability of this channel is grossly reduced at negative clamp potentials (corresponding to cell hyperpolarization). Therefore, the macroscopic Cl current through this channel is reduced with hyperpolarization on the cytosolic side. An analysis of time constants of this channel reveals that at depolarized voltages two open and two closed time constants of about 1 ms and of about 10 ms, respectively, are demonstrable. With hyperpolarized voltages the larger open state time constant is reduced significantly. This type of chloride channel is blocked reversibly by diphenylamine-2-carboxylate (10−4 mol/l) and by 5-nitro-2-(3-phenylpropylamino)-benzoate (10−5 mol/l). The channel is selective for Cl over Na and K as well as over Br. It is, however, permeable for NO -3 . Since this channel is very rare or absent in nonstimulated rectal gland tubules, it is very likely that this type of channel is responsible for hormone and cAMP dependent chloride secretion in this organ.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Blatz L, Magleby KL (1983) Single voltage-dependent chlorideselective channels of large conductance in cultured rat muscle. Biophys J 43:237–241

    Google Scholar 

  2. Chesnoy-Marchais D, Evans MG (1984) Two types of chloride channels in outside-out patches from Aplysia neurones. J Physiol 357:64P

    Google Scholar 

  3. DiStefano A, Wittner M, schlatter E, Lang HJ, Englert H, Greger R (1985) Diphenylamine-2-carboxylate, a blocker of the Cl-conductive pathway in Cl-transporting epithelia. Pflügers Arch (Suppl 1):S95-S100

    Google Scholar 

  4. Epstein FH (1979) The shark rectal gland: a model for the active transport of chloride. Yale J Biol Med 52:517–523

    Google Scholar 

  5. Geletyuk VI, Kazachenko VN (1985) Single Cl channels in melluscan neurones: multiplicity of the conductance states. J Membr Biol 86:9–15

    Google Scholar 

  6. Gögelein H, Greger R (1986) A voltage-dependent channel in the basolateral membrane of late proximal tubules of the rabbit kidney. Pflügers Arch (Suppl 2): S142-S148

    Google Scholar 

  7. Greger R, Schlatter E (1984) Mechanism of NaCl secretion in the rectal gland of spiny dogfish (Squalus acanthias). I. Experiments in isolated in vitro perfused rectal gland tubules. Pflügers Arch 402:63–75

    Google Scholar 

  8. Greger R, Schlatter E (1984) Mechanism of NaCl secretion in rectal gland tubules of spiny dogfish (Squalus acanthias). II. Effects of inhibitors. Pflügers Arch 402:364–375

    Google Scholar 

  9. Greger R, Schlatter R, Wang F, Forrest JN Jr (1984) Mechanism of NaCl secretion in rectal gland tubules of spiny dogfish (Spualus acanthias). III. Effects of stimulation of secretion by cyclic AMP. Pflügers Arch 402:376–384

    Google Scholar 

  10. Greger R, Schlatter E, Gögelein H (1985) Cl channels in the apical cell membrane of the rectal gland “induced” by cAMP. Pflügers Arch 403:446–448

    Google Scholar 

  11. Gögelein H, Schlatter E, Greger R (1987) The “small” conductance chloride channel in the luminal membrane of the rectal gland of the dogfish (Squalus acanthias). Pflügers Arch 409:122–125

    Google Scholar 

  12. Greger R, Gögelein H, Schlatter E (1987) Potassium channels in the basolateral membrane of the rectal gland of the dogfish (Squalus acanthias). Pflügers Arch 409:100–106

    Google Scholar 

  13. Halm D, Rechkemmer G, Frizzell R (1986) Single-channel recording from a secretory epithelial cell line, T84. Fed Proc 45:741

    Google Scholar 

  14. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85–100

    Google Scholar 

  15. Hanrahan JW, Alles WP, Lewis SA (1985) Single anionselective channels in basolateral membrane of a mammalian tight epithelium. Proc Natl Acad Sci USA 82:7791–7795

    Google Scholar 

  16. Kolb HA, Brown CDA, Murer H (1985) Identification of a voltage-dependent anion channel in the apical membrane of a Cl-secretory epithelium (MDCK). Pflügers Arch 403:262–265

    Google Scholar 

  17. Krouse ME, Schneider GT, Gage PW (1986) A large anionselective channel has seven conductance levels. Nature 319:58–60

    Google Scholar 

  18. Miller C (1982) Open-state substructure of single chloride channels from Torpedo electroplax. Philos Trans R Soc Lond B299:401–414

    Google Scholar 

  19. Nelson DJ, Tang JM, Palmer LG (1984) Single-channel recordings of apical membrane chloride conductance in A6 epithelial cells. J Membr Biol 80:81–89

    Google Scholar 

  20. schneider GT, Cook DI, Gage PW, Young JA (1985) Voltage sensitive, high-conductance chloride channels in the luminal membrane of cultured pulmonary alveolar (type II) cells. Pflügers Arch 404:354–357

    Google Scholar 

  21. Shoemaker RL, Frizzell RA, Dwyer TM, Farley JM (1986) Single chloride channel currents from canine tracheal epithelial cells. Biochim Biophys Acta 858:235–242

    Google Scholar 

  22. Sigworth F (1983) An example of analysis. In: Sakmann B, Neher E (eds) Single channel recording. Plenum Press, New York London, pp 301–322

    Google Scholar 

  23. Silva P, Stoff J, Field M, Fine L, Forrest JN, Epstein FH (1977) Mechanism of active chloride secretion by shark rectal gland: role of Na-K-ATPase in chloride transport. Am J Physiol 233(4):F298-F306

    Google Scholar 

  24. Wangemann P, Wittner M, DiStefano A, Englert HC, Lang HJ, Schlatter E, Greger R (1986) Cl-channel blockers in the thick ascending limb of the loop of Henle. Structure activity relationship. Pflügers Arch 407 (Suppl 2):S128-S141

    Google Scholar 

  25. Welsh MJ (1986) Single apical membrane anion channels in primary cultures of canine tracheal epithelium. Pflügers Arch 407 (Suppl 2):S116-S122

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by Deutsche Forschungsgemeinschaft Gr 480 and by NSF and NIH grants to the MDIBL

Rights and permissions

Reprints and permissions

About this article

Cite this article

Greger, R., Schlatter, E. & Gögelein, H. Chloride channels in the luminal membrane of the rectal gland of the dogfish (Squalus acanthias). Pflugers Arch. 409, 114–121 (1987). https://doi.org/10.1007/BF00584757

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00584757

Key words

Navigation