Pflügers Archiv

, Volume 451, Issue 2, pp 371–379 | Cite as

Distribution of cGMP-dependent and cGMP-independent Ca2+-activated Cl− conductances in smooth muscle cells from different vascular beds and colon

  • Vladimir V. Matchkov
  • Christian Aalkjær
  • Holger Nilsson
Ion Channels, Transporters
First Online:
Received:
Accepted:

Abstract

In the present patch-clamp study we have, for the first time, shown the tissue distribution of a recently characterized cGMP-dependent Ca2+-activated Cl− conductance [18] in smooth muscle cells freshly isolated from different regions: aorta, pulmonary artery, tail artery, femoral artery, femoral vein, middle cerebral artery, renal artery, portal vein, superior mesenteric artery, mesenteric small artery and colon. The cGMP-dependent Cl− conductance has properties distinct from those of the ‘classical’ Ca2+-activated Cl− conductances; their different sensitivities to niflumic acid and zinc were here utilized to distinguish them. They were found to be co-expressed in different patterns in smooth muscle cells of different origins. The cGMP-dependent conductance was greater in myocytes from cerebral artery and femoral vein and was greater in the renal artery, aorta, mesenteric small artery, femoral artery and the superior mesenteric artery. The presence of the cGMP-dependent Ca2+-activated Cl− current in smooth muscle cells isolated from the colon demonstrates that this conductance is not limited to the vasculature. The ‘classical’ Ca2+-activated Cl− conductance was strongly expressed in smooth muscle cells from the portal vein and the tail artery, and noticeably higher in the pulmonary artery.

Keywords

Smooth muscle Blood vessel Colon Chloride channel cGMP Niflumic acid Zinc Intracellular calcium 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

The work was supported by the Danish Heart Foundation. The Water and Salt Research Center at the University of Aarhus is established and supported by the Danish National Research Foundation (Danmarks Grundforskningsfond).

References

  1. 1.
    Arreola J, Melvin JE, Begenisich T (1996) Activation of calcium-dependent chloride channels in rat parotid acinar cells. J Gen Physiol 108:35–47CrossRefPubMedGoogle Scholar
  2. 2.
    Britton FC, Ohya S, Horowitz B, Greenwood IA (2002) Comparison of the properties of CLCA1 generated currents and ICl(Ca) in murine portal vein smooth muscle cells. J Physiol 539:107–117Google Scholar
  3. 3.
    Chipperfield AR Harper AA (2000) Chloride in smooth muscle. Prog Biophys Mol Biol 74:175–221CrossRefPubMedGoogle Scholar
  4. 4.
    Cruickshank SF, Baxter LM, Drummond RM (2003) The Cl− channel blocker niflumic acid releases Ca2+ from an intracellular store in rat pulmonary artery smooth muscle cells. Br J Pharmacol 140:1442–1450Google Scholar
  5. 5.
    Cunningham SA, Awayda MS, Bubien JK, Ismailov II, Arrate MP, Berdiev BK, Benos DJ, Fuller CM (1995) Cloning of an epithelial chloride channel from bovine trachea. J Biol Chem 270:31016–31026CrossRefPubMedGoogle Scholar
  6. 6.
    Duta V, Szkotak AJ, Nahirney D, Duszyk M (2004) The role of bestrophin in airway epithelial ion transport. FEBS Lett 577:551–554CrossRefPubMedGoogle Scholar
  7. 7.
    Frings S, Reuter D, Kleene SJ (2000) Neuronal Ca2+-activated Cl− channels-homing in on an elusive channel species. Prog Neurobiol 60:247–289CrossRefPubMedGoogle Scholar
  8. 8.
    Greenwood IA, Large WA (1995) Comparison of the effects of fenamates on Ca2+-activated chloride and potassium currents in rabbit portal vein smooth muscle cells. Br J Pharmacol 116:2939–2948PubMedGoogle Scholar
  9. 9.
    Greenwood IA, Ledoux J, Leblanc N (2001) Differential regulation of Ca2+-activated Cl− currents in rabbit arterial and portal vein smooth muscle cells by Ca2+-calmodulin dependent kinase. J Physiol 534:395–408Google Scholar
  10. 10.
    Hartzell C, Putzier I, Arreola J (2005) Calcium-activated chloride channels. Annu Rev Physiol 67:719–758CrossRefPubMedGoogle Scholar
  11. 11.
    Hirakawa Y, Gericke M, Cohen RA, Bolotina VM (1999) Ca2+-dependent Cl− channels in mouse and rabbit aortic smooth muscle cells: regulation by intracellular Ca2+ and NO. Am J Physiol 277:H1732-H1744PubMedGoogle Scholar
  12. 12.
    Hogg RC, Wang Q, Large WA (1994) Action of niflumic acid on evoked and spontaneous calcium-activated chloride and potassium currents in smooth muscle cells from rabbit portal vein. Br J Pharmacol 112:977–984PubMedGoogle Scholar
  13. 13.
    Hogg RC, Wang Q, Large WA (1994) Effects of Cl channel blockers on Ca-activated chloride and potassium currents in smooth muscle cells from rabbit portal vein. Br J Pharmacol 111:1333–1341Google Scholar
  14. 14.
    Jentsch TJ, Stein V, Weinreich F, Zdebik AA (2002) Molecular structure and physiological function of chloride channels. Physiol Rev 82:503–568PubMedGoogle Scholar
  15. 15.
    Kitamura K, Yamazaki J (2001) Chloride channels and their functional roles in smooth muscle tone in the vasculature. Jpn J Pharmacol 85:351–357CrossRefPubMedGoogle Scholar
  16. 16.
    Large WA, Wang Q (1996) Characteristics and physiological role of the Ca2+-activated Cl− conductance in smooth muscle. Am J Physiol 271:C435-C454PubMedGoogle Scholar
  17. 17.
    Matchkov V, Aalkjaer C, Nilsson H (2003) A novel cGMP-dependent calcium-activated chloride current from the mesenteric resistance artery. J Gen Physiol 122:40aGoogle Scholar
  18. 18.
    Matchkov VV, Aalkjaer C, Nilsson H (2004) A cyclic GMP-dependent calcium-activated chloride current in smooth-muscle cells from rat mesenteric resistance arteries. J Gen Physiol 123:121–134CrossRefPubMedGoogle Scholar
  19. 19.
    Nelson MT, Conway MA, Knot HJ, Brayden JE (1997) Chloride channel blockers inhibit myogenic tone in rat cerebral arteries. J Physiol 502:259–264CrossRefPubMedGoogle Scholar
  20. 20.
    Nilius B, Prenen J, Voets T, Van den BK, Eggermont J, Droogmans G (1997) Kinetic and pharmacological properties of the calcium-activated chloride-current in macrovascular endothelial cells. Cell Calcium 22:53–63CrossRefPubMedGoogle Scholar
  21. 21.
    Peng H, Matchkov V, Ivarsen A, Aalkjaer C, Nilsson H (2001) Hypothesis for the initiation of vasomotion. Circ Res 88:810–815PubMedGoogle Scholar
  22. 22.
    Piper AS, Large WA (2003) Multiple conductance states of single Ca2+-activated Cl− channels in rabbit pulmonary artery smooth muscle cells. J Physiol 547:181–196Google Scholar
  23. 23.
    Piper AS, Large WA (2004) Direct effect of Ca2+/calmodulin on cGMP-activated Ca2+-dependent Cl− channels in rat mesenteric artery myocytes. J Physiol 559:449–457Google Scholar
  24. 24.
    Piper AS, Large WA (2004) Single cGMP-activated Ca2+-dependent Cl− channels in rat mesenteric artery smooth muscle cells. J Physiol 555:397–408CrossRefPubMedGoogle Scholar
  25. 25.
    Pusch M (2004) Ca2+-activated chloride channels go molecular. J Gen Physiol 123:323–325CrossRefPubMedGoogle Scholar
  26. 26.
    Qu Z, Fischmeister R, Hartzell C (2004) Mouse bestrophin-2 is a bona fide Cl− channel: identification of a residue important in anion binding and conduction. J Gen Physiol 123:327–340CrossRefPubMedGoogle Scholar
  27. 27.
    Qu Z, Hartzell C (2004) Determinants of anion permeation in the second transmembrane domain of the mouse bestrophin-2 chloride channel. J Gen Physiol 124:371–382CrossRefPubMedGoogle Scholar
  28. 28.
    Qu Z, Hartzell HC (2000) Anion permeation in Ca2+-activated Cl− channels. J Gen Physiol 116:825–844CrossRefPubMedGoogle Scholar
  29. 29.
    Qu Z, Wei RW, Mann W, Hartzell HC (2003) Two bestrophins cloned from Xenopus laevis Oocytes express Ca2+-activated Cl− currents. J Biol Chem 278:49563–49572CrossRefPubMedGoogle Scholar
  30. 30.
    Ran S, Fuller CM, Arrate MP, Latorre R, Benos DJ (1992) Functional reconstitution of a chloride channel protein from bovine trachea. J Biol Chem 267:20630–20637PubMedGoogle Scholar
  31. 31.
    Strauss O, Rosenthal R (2005) Function of bestrophin. Ophthalmologe 102(2):122–126CrossRefPubMedGoogle Scholar
  32. 32.
    Sun H, Tsunenari T, Yau KW, Nathans J (2002) The vitelliform macular dystrophy protein defines a new family of chloride channels. Proc Natl Acad Sci USA 99:4008–4013CrossRefPubMedGoogle Scholar
  33. 33.
    Toma C, Greenwood IA, Helliwell RM, Large WA (1996) Activation of potassium currents by inhibitors of calcium-activated chloride conductance in rabbit portal vein smooth muscle cells. Br J Pharmacol 118:513–520Google Scholar
  34. 34.
    Tsunenari T, Sun H, Williams J, Cahill H, Smallwood P, Yau KW, Nathans J (2003) Structure-function analysis of the bestrophin family of anion channels. J Biol Chem 278:41114–41125CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Vladimir V. Matchkov
    • 1
  • Christian Aalkjær
    • 1
  • Holger Nilsson
    • 1
  1. 1.The Water and Salt Research Center, Institute of Physiology and Biophysics, Department of PhysiologyUniversity of AarhusAarhusDenmark

Personalised recommendations