Skip to main content
Log in

Vasomotion has chloride-dependency in rat mesenteric small arteries

  • Ion Channels, Receptors and Transporters
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

The possibility that Ca2+-activated Cl conductances (CaCCs) contribute to oscillations in vascular tone (vasomotion) is tested in isolated mesenteric small arteries from rats where cGMP independent (I Cl(Ca)) and cGMP-dependent (I Cl(Ca,cGMP)) chloride conductances are important. The effect of anion substitution and Cl channel blockers on noradrenaline (NA)-stimulated tension in isometrically mounted mesenteric arteries and for chloride conductance of smooth muscle cells isolated from these arteries were assessed electrophysiologically. Cl o replacement with aspartate blocked vasomotion while 36mM SCN o (substituted for Cl) was sufficient to inhibit vasomotion. Oscillations in tone, membrane potential, and [Ca2+]i disappeared with 36mM SCN. DIDS and Zn2+ blocked I Cl(Ca,cGMP) but not I Cl(Ca). Vasomotion was not sensitive to DIDS and Zn2+, and DIDS and Zn2+ induce vasomotion in arteries without endothelium. The vasomotion in the presence of DIDS and Zn2+ was sensitive to 36mM SCN o. The anion substitution data indicate that Cl is crucial for the V m and [Ca2+]i oscillations underlying vasomotion. The Cl channel blocker data are consistent with both CaCCs being important.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  1. Large WA, Wang Q (1996) Characteristics and physiological role of the Ca2+-activated Cl conductance in smooth muscle. Am J Physiol 271:C435–C454

    PubMed  CAS  Google Scholar 

  2. Chipperfield AR, Harper AA (2000) Chloride in smooth muscle. Prog Biophys Mol Biol 74:175–221

    Article  PubMed  CAS  Google Scholar 

  3. Kitamura K, Yamazaki J (2001) Chloride channels and their functional roles in smooth muscle tone in the vasculature. Jpn J Pharmacol 85:351–357

    Article  PubMed  CAS  Google Scholar 

  4. Piper AS, Large WA (2004) Single cGMP-activated Ca2+-dependent Cl channels in rat mesenteric artery smooth muscle cells. J Physiol 555:397–408

    Article  PubMed  CAS  Google Scholar 

  5. 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 123:121–134

    Article  PubMed  CAS  Google Scholar 

  6. Aalkjaer C, Nilsson H (2005) Vasomotion: cellular background for the oscillator and for the synchronization of smooth muscle cells. Br J Pharmacol 144:605–616

    Article  CAS  PubMed  Google Scholar 

  7. Haddock RE, Hill CE (2005) Rhythmicity in arterial smooth muscle. J Physiol 566:645–656

    Article  PubMed  CAS  Google Scholar 

  8. Peng H, Matchkov V, Ivarsen A, Aalkjaer C, Nilsson H (2001) Hypothesis for the initiation of vasomotion. Circ Res 88:810–815

    Article  PubMed  CAS  Google Scholar 

  9. Jacobsen JC, Aalkjaer C, Nilsson H, Matchkov V, Freiberg J, Holstein-Rathlou NH (2007) A model of smooth muscle cell synchronization in the arterial wall. Am J Physiol 293:H229–H237

    CAS  Google Scholar 

  10. Mulvany MJ, Halpern W (1977) Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ Res 41:19–26

    PubMed  CAS  Google Scholar 

  11. Aalkjaer C, Cragoe EJ (1988) Intracellular pH regulation in resting and contracting segments of rat mesenteric resistance vessels. J Physiol 402:391–410

    PubMed  CAS  Google Scholar 

  12. Mulvany MJ, Nilsson H, Flatman JA (1982) Role of membrane potential in the response of rat small mesenteric arteries to exogenous noradrenaline stimulation. J Physiol 332:363–373

    PubMed  CAS  Google Scholar 

  13. Nilsson H, Videbaek LM, Toma C, Mulvany MJ (1998) Role of intracellular calcium for noradrenaline-induced depolarization in rat mesenteric small arteries. J Vasc Res 35:36–44

    Article  PubMed  CAS  Google Scholar 

  14. Matchkov VV, Aalkjaer C, Nilsson H (2005) Distribution of cGMP-dependent and cGMP-independent Ca2+-activated Cl conductances in smooth muscle cells from different vascular beds and colon. Pflugers Arch 451:371–379

    Article  PubMed  CAS  Google Scholar 

  15. Matchkov VV, Rahman A, Bakker LM, Griffith TM, Nilsson H, Aalkjaer C (2006) Analysis of effects of connexin-mimetic peptides in rat mesenteric small arteries. Am J Physiol Heart Circ Physiol 291:H357–H367

    Article  PubMed  CAS  Google Scholar 

  16. Chaytor AT, Evans WH, Griffith TM (1997) Peptides homologous to extracellular loop motifs of connexin 43 reversibly abolish rhythmic contractile activity in rabbit arteries. J Physiol 503:99–110

    Article  PubMed  CAS  Google Scholar 

  17. Matchkov VV, Rahman A, Peng H, Nilsson H, Aalkjaer C (2004) Junctional and nonjunctional effects of heptanol and glycyrrhetinic acid derivates in rat mesenteric small arteries. Br J Pharmacol 142:961–972

    Article  PubMed  CAS  Google Scholar 

  18. Gustafsson H, Nilsson H (1993) Rhythmic contractions of isolated small arteries from rat: role of calcium. Acta Physiol Scand 149:283–291

    Article  PubMed  CAS  Google Scholar 

  19. Aalkjaer C, Hughes A (1991) Chloride and bicarbonate transport in rat resistance arteries. J Physiol 436:57–73

    PubMed  CAS  Google Scholar 

  20. Qu Z, Hartzell HC (2001) Functional geometry of the permeation pathway of Ca2+-activated Cl channels inferred from analysis of voltage-dependent block. J Biol Chem 276:18423–18429

    Article  PubMed  CAS  Google Scholar 

  21. Piper AS, Greenwood IA, Large WA (2002) Dual effect of blocking agents on Ca2+-activated Cl currents in rabbit pulmonary artery smooth muscle cells. J Physiol 539:119–131

    Article  PubMed  CAS  Google Scholar 

  22. Jacobsen JC, Aalkjaer C, Nilsson H, Matchkov V, Freiberg J, Holstein-Rathlou NH (2007) Activation of a cGMP-sensitive calcium-dependent chloride channel may cause transition from calcium waves to whole-cell oscillations in smooth muscle cells. Am J Physiol 293:H215–H228

    CAS  Google Scholar 

  23. Dawson DC, Smith SS, Mansoura MK (1999) CFTR: mechanism of anion conduction. Physiol Rev 79:S47–S75

    PubMed  CAS  Google Scholar 

  24. 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 534:395–408

    Article  PubMed  CAS  Google Scholar 

  25. Saleh SN, Greenwood IA (2005) Activation of chloride currents in murine portal vein smooth muscle cells by membrane depolarization involves intracellular calcium release. Am J Physiol Cell Physiol 288:C122–C131

    PubMed  CAS  Google Scholar 

  26. Amedee T, Large WA, Wang Q (1990) Characteristics of chloride currents activated by noradrenaline in rabbit ear artery cells. J Physiol 428:501–516

    PubMed  CAS  Google Scholar 

  27. Greenwood IA, Leblanc N (2007) Overlapping pharmacology of Ca2+-activated Cl- and K+ channels. Trends Pharmacol Sci 28:1–5

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The current work was supported by grants from Lundbeck and the Karen Elise Jensen fund. Donna Briggs Boedtkjer was supported by a Ph.D. stipend from the Danish Cardiovascular Research Academy. The authors wish to acknowledge the technical assistance provided by Kirsten Skaarup, Jørgen Andresen, and Trine Rohde.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. M. Briggs Boedtkjer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boedtkjer, D.M.B., Matchkov, V.V., Boedtkjer, E. et al. Vasomotion has chloride-dependency in rat mesenteric small arteries. Pflugers Arch - Eur J Physiol 457, 389–404 (2008). https://doi.org/10.1007/s00424-008-0532-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-008-0532-3

Keywords

Navigation