© 2000 American Heart Association, Inc.
Integrative Physiology |
Integrated Ca2+ Signaling Between Smooth Muscle and Endothelium of Resistance Vessels
From the First Department of Physiology (Y.Y.), Shinshu University School of Medicine, Matsumoto, Japan, and Department of Molecular Physiology and Biological Physics (B.R.D.), University of Virginia Health Sciences Center, Charlottesville, Va.
Correspondence to Dr Brian R. Duling, Department of Molecular Physiology and Biological Physics, University of Virginia Health Sciences Center, PO Box 800736, Charlottesville, VA 22908-0736. E-mail brd{at}virginia.edu
Abstract—Cell-cell communication in the arteriolar wall was examined using the Ca2+-sensitive indicator fura-2 and the Ca2+ buffer BAPTA as means of measuring and buffering cellular Ca2+. The experiments focused on the role of endothelial cell [Ca2+]i in modulating phenylephrine (PE)-induced contractions in in vitro arterioles of the hamster cremaster. Fura-2-AM and BAPTA-AM were applied intraluminally to accomplish endothelium-specific loading. PE was applied to short segments of arterioles using pressure-pulse ejection from a micropipette. Under control conditions at the site of stimulation, PE elicited a strong vasoconstriction preceded by an increase in endothelial cell [Ca2+]i. A very small biphasic conducted response was observed at sites upstream from the stimulation site. BAPTA sharply reduced the measured Ca2+ response in the endothelium. This was associated with an enhanced local contractile response. In addition, the biphasic conducted response was converted into a strong conducted vasoconstriction. PE caused an initial rise in smooth muscle [Ca2+]i at the stimulated site, which was followed by a rapid decrease below baseline. Endothelial cell loading of BAPTA had minimal effect on the initial [Ca2+]i peak but eliminated the secondary decrease in smooth muscle [Ca2+]i. Intraluminal application of charybdotoxin plus apamin mimicked the change in vasomotor state induced by BAPTA. These data lead us to hypothesize that, after smooth muscle stimulation, intercellular Ca2+ signaling between smooth muscle and endothelium causes a secondary rise in endothelial cell Ca2+, which triggers a hyperpolarizing event and initiates a conducted vasodilation. We conclude that smooth muscle and endothelium operate as a functional unit in these vessels.
Key Words: phenylephrine • gap junctions • endothelium • [Ca2+]i • hyperpolarization
This article has been cited by other articles:
 |
|
 |
|
  C. H. T. Tran, E. J. Vigmond, F. Plane, and D. G. Welsh Mechanistic basis of differential conduction in skeletal muscle arteries J. Physiol., March 15, 2009; 587(6): 1301 - 1318. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. E. Isakson Localized expression of an Ins(1,4,5)P3 receptor at the myoendothelial junction selectively regulates heterocellular Ca2+ communication J. Cell Sci., November 1, 2008; 121(21): 3664 - 3673. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X. F. Figueroa, C.-C. Chen, K. P. Campbell, D. N. Damon, K. H. Day, S. Ramos, and B. R. Duling Are voltage-dependent ion channels involved in the endothelial cell control of vasomotor tone? Am J Physiol Heart Circ Physiol, September 1, 2007; 293(3): H1371 - H1383. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. C. Brennan, L. Beltran-Parrazal, H. E. Lopez-Valdes, J. Theriot, A. W. Toga, and A. C. Charles Distinct Vascular Conduction With Cortical Spreading Depression J Neurophysiol, June 1, 2007; 97(6): 4143 - 4151. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. R. Uhrenholt, T. L. Domeier, and S. S. Segal Propagation of calcium waves along endothelium of hamster feed arteries Am J Physiol Heart Circ Physiol, March 1, 2007; 292(3): H1634 - H1640. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. E. Isakson, S. I. Ramos, and B. R. Duling Ca2+ and Inositol 1,4,5-Trisphosphate-Mediated Signaling Across the Myoendothelial Junction Circ. Res., February 2, 2007; 100(2): 246 - 254. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. C. Jantzi, S. E. Brett, W. F. Jackson, R. Corteling, E. J. Vigmond, and D. G. Welsh Inward rectifying potassium channels facilitate cell-to-cell communication in hamster retractor muscle feed arteries Am J Physiol Heart Circ Physiol, September 1, 2006; 291(3): H1319 - H1328. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. F. Brekke, W. F. Jackson, and S. S. Segal Arteriolar smooth muscle Ca2+ dynamics during blood flow control in hamster cheek pouch J Appl Physiol, July 1, 2006; 101(1): 307 - 315. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. V. Matchkov, A. Rahman, L. M. Bakker, T. M. Griffith, H. Nilsson, and C. Aalkjaer Analysis of effects of connexin-mimetic peptides in rat mesenteric small arteries Am J Physiol Heart Circ Physiol, July 1, 2006; 291(1): H357 - H367. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. I. Gokina and T. Goecks Upregulation of endothelial cell Ca2+ signaling contributes to pregnancy-enhanced vasodilation of rat uteroplacental arteries Am J Physiol Heart Circ Physiol, May 1, 2006; 290(5): H2124 - H2135. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. E. Isakson, D. N. Damon, K. H. Day, Y. Liao, and B. R. Duling Connexin40 and connexin43 in mouse aortic endothelium: evidence for coordinated regulation Am J Physiol Heart Circ Physiol, March 1, 2006; 290(3): H1199 - H1205. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. K Diep, E. J Vigmond, S. S Segal, and D. G Welsh Defining electrical communication in skeletal muscle resistance arteries: a computational approach J. Physiol., October 1, 2005; 568(1): 267 - 281. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. E Haddock and C. E Hill Rhythmicity in arterial smooth muscle J. Physiol., August 1, 2005; 566(3): 645 - 656. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. T. Kurjiaka, S. B. Bender, D. D. Nye, W. B. Wiehler, and D. G. Welsh Hypertension attenuates cell-to-cell communication in hamster retractor muscle feed arteries Am J Physiol Heart Circ Physiol, February 1, 2005; 288(2): H861 - H870. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Earley, T. C. Resta, and B. R. Walker Disruption of smooth muscle gap junctions attenuates myogenic vasoconstriction of mesenteric resistance arteries Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2677 - H2686. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Boitano, Z. Safdar, D. G. Welsh, J. Bhattacharya, and M. Koval Cell-cell interactions in regulating lung function Am J Physiol Lung Cell Mol Physiol, September 1, 2004; 287(3): L455 - L459. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. D. Thomas and S. S. Segal Neural control of muscle blood flow during exercise J Appl Physiol, August 1, 2004; 97(2): 731 - 738. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. R. H. Mauban and W. G. Wier Essential role of EDHF in the initiation and maintenance of adrenergic vasomotion in rat mesenteric arteries Am J Physiol Heart Circ Physiol, August 1, 2004; 287(2): H608 - H616. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. L. Sandow, R. Looft-Wilson, B. Doran, T.H. Grayson, S. S. Segal, and C. E. Hill Expression of homocellular and heterocellular gap junctions in hamster arterioles and feed arteries Cardiovasc Res, December 1, 2003; 60(3): 643 - 653. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Fleming Bobbing Along on the Crest of a Wave: NO Ascends Hamster Cheek Pouch Arterioles Circ. Res., July 11, 2003; 93(1): 9 - 11. [Full Text] [PDF]
|
|
|
|
|
|
S. Budel, I. S. Bartlett, and S. S. Segal Homocellular Conduction Along Endothelium and Smooth Muscle of Arterioles in Hamster Cheek Pouch: Unmasking an NO Wave Circ. Res., July 11, 2003; 93(1): 61 - 68. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. A. Dora, J. Xia, and B. R. Duling Endothelial cell signaling during conducted vasomotor responses Am J Physiol Heart Circ Physiol, June 5, 2003; 285(1): H119 - H126. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Yashiro and B. R. Duling Participation of intracellular Ca2+ stores in arteriolar conducted responses Am J Physiol Heart Circ Physiol, June 5, 2003; 285(1): H65 - H73. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. F. Figueroa, D. L. Paul, A. M. Simon, D. A. Goodenough, K. H. Day, D. N. Damon, and B. R. Duling Central Role of Connexin40 in the Propagation of Electrically Activated Vasodilation in Mouse Cremasteric Arterioles In Vivo Circ. Res., April 18, 2003; 92(7): 793 - 800. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Salomonsson, F. Gustafsson, D. Andreasen, B. L. Jensen, and N.-H. Holstein-Rathlou Local electric stimulation causes conducted calcium response in rat interlobular arteries Am J Physiol Renal Physiol, September 1, 2002; 283(3): F473 - F480. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. Ungvari, A. Csiszar, and A. Koller Increases in endothelial Ca2+ activate KCa channels and elicit EDHF-type arteriolar dilation via gap junctions Am J Physiol Heart Circ Physiol, May 1, 2002; 282(5): H1760 - H1767. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Choi, L. W. Hammer, and R. L. Hester Calcium-Dependent Synthesis of Prostacyclin in ATP-Stimulated Venous Endothelial Cells Hypertension, February 1, 2002; 39(2): 581 - 585. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Budel, A. Schuster, N. Stergiopoulos, J.-J. Meister, and J.-L. Beny Role of smooth muscle cells on endothelial cell cytosolic free calcium in porcine coronary arteries Am J Physiol Heart Circ Physiol, September 1, 2001; 281(3): H1156 - H1162. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Tyml, X. Wang, D. Lidington, and Y. Ouellette Lipopolysaccharide reduces intercellular coupling in vitro and arteriolar conducted response in vivo Am J Physiol Heart Circ Physiol, September 1, 2001; 281(3): H1397 - H1406. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Tuttle and J. C. Falcone Nitric oxide release during {alpha}1-adrenoceptor-mediated constriction of arterioles Am J Physiol Heart Circ Physiol, August 1, 2001; 281(2): H873 - H881. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H.-Z. Wang, N. Day, M. Valcic, K. Hsieh, S. Serels, P. R. Brink, and G. J. Christ Intercellular communication in cultured human vascular smooth muscle cells Am J Physiol Cell Physiol, July 1, 2001; 281(1): C75 - C88. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Vequaud and E. Thorin Endothelial G Protein {beta}-Subunits Trigger Nitric Oxide- but not Endothelium-Derived Hyperpolarizing Factor-Dependent Dilation in Rabbit Resistance Arteries Circ. Res., October 12, 2001; 89(8): 716 - 722. [Abstract] [Full Text] [PDF]
|
|