© 1998 American Heart Association, Inc.
Original Contributions |
Pulsatile Stretch in Coronary Arteries Elicits Release of Endothelium-Derived Hyperpolarizing Factor
A Modulator of Arterial Compliance
From the Institut für Kardiovaskuläre Physiologie, Klinikum der J.W. Goethe-Universität, Frankfurt, Germany.
Correspondence to Dr Rüdiger Popp, Institut für Kardiovaskuläre Physiologie, Klinikum der J. W. Goethe-Universität, Theodor-Stern-Kai 7, D-60590 Frankfurt am Main, Germany. E-mail r.popp{at}em.uni-frankfurt.de
Abstract—To date, the release of the endothelium-derived hyperpolarizing factor (EDHF) has been demonstrated only in response to receptor-dependent Ca2+-elevating agonists. Since endothelial cells in situ are continuously subjected to rhythmic distension, we investigated the effect of rhythmic stretch on the release of EDHF from isolated porcine coronary arteries. In the combined presence of diclofenac and NG-nitro-L-arginine (L-NNA), sinusoidal pressure oscillations (from 40 to 50 mm Hg, 4 minutes, 1.5 Hz) led to simultaneous oscillations in the external diameter of coronary artery segments, the amplitude of which were decreased by iberiotoxin and apamin and also by endothelial denudation. In order to directly demonstrate the release of EDHF, the intraluminal solution from endothelium-intact coronary segments exposed to pulsatile stretch was applied to detector rat aortic smooth muscle cells, the membrane potential of which was continuously measured using the patch-clamp technique. The hyperpolarization of detector cells induced by the intraluminal solution was proportional to the amplitude of the pressure oscillations applied to the donor artery and was attenuated by either preincubation of donor arteries with 17-octadecynoic acid or application of either tetrabutylammonium or iberiotoxin to detector cells. In contrast to the bradykinin-induced release of EDHF, the EDHF synthesized in response to pulsatile stretch did not exhibit any tachyphylaxis. These findings demonstrate for the first time that the synthesis of EDHF in coronary arteries can be mechanically stimulated by rhythmic vessel wall distension and suggest that the continuous release of EDHF may contribute to the adjustment of an adequate vascular compliance and to the control of coronary blood flow.
Key Words: mechanotransduction • endothelium-derived hyperpolarizing factor • cytochrome P-450 • transmural pressure • coronary artery
This article has been cited by other articles:
 |
|
 |
|
  A. E. Loot, R. Popp, B. Fisslthaler, J. Vriens, B. Nilius, and I. Fleming Role of cytochrome P450-dependent transient receptor potential V4 activation in flow-induced vasodilatation Cardiovasc Res, December 1, 2008; 80(3): 445 - 452. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. H. Walpoth, M. Schmid, A. Schwab, A. Bosshard, F. Eckstein, T. Carrel, and O. M. Hess Vascular adaptation of the internal thoracic artery graft early and late after bypass surgery. J. Thorac. Cardiovasc. Surg., October 1, 2008; 136(4): 876 - 883. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. Fleming, A. Rueben, R. Popp, B. Fisslthaler, S. Schrodt, A. Sander, J. Haendeler, J. R. Falck, C. Morisseau, B. D. Hammock, et al. Epoxyeicosatrienoic Acids Regulate Trp Channel Dependent Ca2+ Signaling and Hyperpolarization in Endothelial Cells Arterioscler. Thromb. Vasc. Biol., December 1, 2007; 27(12): 2612 - 2618. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. B. Campbell and J. R. Falck Arachidonic Acid Metabolites as Endothelium-Derived Hyperpolarizing Factors Hypertension, March 1, 2007; 49(3): 590 - 596. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Adlam, J. K. Bendall, J. P. De Bono, N. J. Alp, J. Khoo, T. Nicoli, M. Yokoyama, S. Kawashima, and K. M. Channon Cardiovascular Control: Relationships between nitric oxide-mediated endothelial function, eNOS coupling and blood pressure revealed by eNOS-GTP cyclohydrolase 1 double transgenic mice Exp Physiol, January 1, 2007; 92(1): 119 - 126. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Westerhof, C. Boer, R. R. Lamberts, and P. Sipkema Cross-talk between cardiac muscle and coronary vasculature. Physiol Rev, October 1, 2006; 86(4): 1263 - 1308. [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]
|
|
|
|
|
|
I. A. Arenas, Y. Xu, and S. T. Davidge Age-associated impairment in vasorelaxation to fluid shear stress in the female vasculature is improved by TNF-{alpha} antagonism Am J Physiol Heart Circ Physiol, March 1, 2006; 290(3): H1259 - H1263. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Radaelli, P. Castiglioni, M. Centola, F. Cesana, G. Balestri, A. U. Ferrari, and M. Di Rienzo Adrenergic origin of very low-frequency blood pressure oscillations in the unanesthetized rat Am J Physiol Heart Circ Physiol, January 1, 2006; 290(1): H357 - H364. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Bellien, R. Joannides, M. Iacob, P. Arnaud, and C. Thuillez Calcium-Activated Potassium Channels and NO Regulate Human Peripheral Conduit Artery Mechanics Hypertension, July 1, 2005; 46(1): 210 - 216. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Zheng, L. P. Christensen, and R. J. Tomanek Stretch induces upregulation of key tyrosine kinase receptors in microvascular endothelial cells Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2739 - H2745. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. D. Tune, M. W. Gorman, and E. O. Feigl Matching coronary blood flow to myocardial oxygen consumption J Appl Physiol, July 1, 2004; 97(1): 404 - 415. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Merkus, B. Houweling, A. Zarbanoui, and D. J. Duncker Interaction between prostanoids and nitric oxide in regulation of systemic, pulmonary, and coronary vascular tone in exercising swine Am J Physiol Heart Circ Physiol, March 1, 2004; 286(3): H1114 - H1123. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Viswanathan, B. D. Hammock, J. W. Newman, P. Meerarani, M. Toborek, and B. Hennig Involvement of CYP 2C9 in Mediating the Proinflammatory Effects of Linoleic Acid in Vascular Endothelial Cells J. Am. Coll. Nutr., December 1, 2003; 22(6): 502 - 510. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Merkus, D. B. Haitsma, T.-Y. Fung, Y. J. Assen, P. D. Verdouw, and D. J. Duncker Coronary blood flow regulation in exercising swine involves parallel rather than redundant vasodilator pathways Am J Physiol Heart Circ Physiol, June 5, 2003; 285(1): H424 - H433. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Gschwend, H. Buikema, R. H. Henning, Y. M. Pinto, D. de Zeeuw, and W. H. van Gilst Endothelial dysfunction and infarct-size relate to impaired EDHF response in rat experimental chronic heart failure Eur J Heart Fail, March 1, 2003; 5(2): 147 - 154. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Hillig, P. Krustrup, I. Fleming, T. Osada, B. Saltin, and Y. Hellsten Cytochrome P450 2C9 plays an important role in the regulation of exercise-induced skeletal muscle blood flow and oxygen uptake in humans J. Physiol., January 1, 2003; 546(1): 307 - 314. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Fisslthaler, R. Popp, U. R. Michaelis, L. Kiss, I. Fleming, and R. Busse Cyclic Stretch Enhances the Expression and Activity of Coronary Endothelium-Derived Hyperpolarizing Factor Synthase Hypertension, December 1, 2001; 38(6): 1427 - 1432. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. Fleming Cytochrome P450 and Vascular Homeostasis Circ. Res., October 26, 2001; 89(9): 753 - 762. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Huang, D. Sun, M. A. Carroll, H. Jiang, C. J. Smith, J. A. Connetta, J. R. Falck, E. G. Shesely, A. Koller, and G. Kaley EDHF mediates flow-induced dilation in skeletal muscle arterioles of female eNOS-KO mice Am J Physiol Heart Circ Physiol, June 1, 2001; 280(6): H2462 - H2469. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Rastaldo, N. Paolocci, A. Chiribiri, C. Penna, D. Gattullo, and P. Pagliaro Cytochrome P-450 metabolite of arachidonic acid mediates bradykinin-induced negative inotropic effect Am J Physiol Heart Circ Physiol, June 1, 2001; 280(6): H2823 - H2832. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Fleming, U. R. Michaelis, D. Bredenkotter, B. Fisslthaler, F. Dehghani, R. P. Brandes, and R. Busse Endothelium-Derived Hyperpolarizing Factor Synthase (Cytochrome P450 2C9) Is a Functionally Significant Source of Reactive Oxygen Species in Coronary Arteries Circ. Res., January 19, 2001; 88(1): 44 - 51. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Paolocci, P. Pagliaro, T. Isoda, F. W. Saavedra, and D. A. Kass Role of Calcium-Sensitive K+ Channels and Nitric Oxide in In Vivo Coronary Vasodilation From Enhanced Perfusion Pulsatility Circulation, January 2, 2001; 103(1): 119 - 124. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Oike, C. Kimura, T. Koyama, M. Yoshikawa, and Y. Ito Hypotonic stress-induced dual Ca2+ responses in bovine aortic endothelial cells Am J Physiol Heart Circ Physiol, August 1, 2000; 279(2): H630 - H638. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. C. Garcia, V. M. Stiffel, and R. D. Gilbert Effects of Long-Term High-Altitude Hypoxia on Ioslated Fetal Ovine Coronary Arteries Reproductive Sciences, July 1, 2000; 7(4): 211 - 217. [Abstract] [PDF]
|
|
|
|
 |
|
 J.J.D. Lucca, A.S.O. Adeagbo, and N.L. Alsip Influence of oestrous cycle and pregnancy on the reactivity of the rat mesenteric vascular bed Hum. Reprod., April 1, 2000; 15(4): 961 - 968. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Hecker Endothelium-Derived Hyperpolarizing Factor--Fact or Fiction? Physiology, February 1, 2000; 15(1): 1 - 5. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Pagliaro, H. Senzaki, N. Paolocci, T. Isoda, G. Sunagawa, F. A Recchia, and D. A Kass Specificity of synergistic coronary flow enhancement by adenosine and pulsatile perfusion in the dog J. Physiol., October 1, 1999; 520(1): 271 - 280. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. Traub, T. Ishida, M. Ishida, J. C. Tupper, and B. C. Berk Shear Stress-mediated Extracellular Signal-regulated Kinase Activation Is Regulated by Sodium in Endothelial Cells. POTENTIAL ROLE FOR A VOLTAGE-DEPENDENT SODIUM CHANNEL J. Biol. Chem., July 16, 1999; 274(29): 20144 - 20150. [Abstract] [Full Text] [PDF]
|
|