Circulation Research. 2004
Published online before print October 7, 2004, doi: 10.1161/01.RES.0000147311.54833.03
Published online before print October 7, 2004, doi: 10.1161/01.RES.0000147311.54833.03
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Submitted on June 25, 2004
Revised on September 24, 2004
Accepted on September 27, 2004
Critical Role for Transient Receptor Potential Channel TRPM4 in Myogenic Constriction of Cerebral Arteries
Scott Earley *;
From the Department of Pharmacology, University of Vermont College of Medicine, Burlington.
* To whom correspondence should be addressed. E-mail: Scott.Earley{at}uvm.edu.
Local control of cerebral blood flow is regulated in part through myogenic constriction of resistance arteries. Although this response requires Ca2+ influx via voltage-dependent Ca2+ channels secondary to smooth muscle cell depolarization, the mechanisms responsible for alteration of vascular smooth muscle (VSM) cell membrane potential are not fully understood. A previous study from our laboratory demonstrated a critical role for a member of the transient receptor potential (TRP) superfamily of ion channels, TRPC6, in this response. Several other of the approximately 22 identified TRP proteins are also present in cerebral arteries, but their functions have not been elucidated. Two of these channels, TRPM4 and TRPM5, exhibit biophysical properties that are consistent with a role for control of membrane potential of excitable cells. We hypothesized that TRPM4/TRPM5-dependent currents contribute to myogenic vasoconstriction of cerebral arteries. Cation channels with unitary conductance, ion selectivity and Ca2+-dependence similar to those of cloned TRPM4 and TRPM5 were present in freshly isolated VSM cells. We found that TRPM4 mRNA was detected in both whole cerebral arteries and in isolated VSM cells whereas TRPM5 message was absent from cerebral artery myocytes. We also found that pressure-induced smooth muscle cell depolarization was attenuated in isolated cerebral arteries treated with TRPM4 antisense oligodeoxynucleotides to downregulate channel subunit expression. In agreement with these data, myogenic vasoconstriction of intact cerebral arteries administered TRPM4 antisense was attenuated compared with controls, whereas KCl-induced constriction did not differ between groups. We concluded that activation of TRPM4-dependent currents contributed to myogenic vasoconstriction of cerebral arteries.
Key words: TRP channels • cerebral circulation • cation channels • vasoconstriction
This article has been cited by other articles:
 |
|
 |
|
  Y. Itoh, N. Hatano, H. Hayashi, K. Onozaki, K. Miyazawa, and K. Muraki An environmental sensor, TRPV4 is a novel regulator of intracellular Ca2+ in human synoviocytes Am J Physiol Cell Physiol, November 1, 2009; 297(5): C1082 - C1090. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Z. Guan, J. S. Pollock, A. K. Cook, J. L. Hobbs, and E. W. Inscho Effect of Epithelial Sodium Channel Blockade on the Myogenic Response of Rat Juxtamedullary Afferent Arterioles Hypertension, November 1, 2009; 54(5): 1062 - 1069. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Yang, T. V. Murphy, S. R. Ella, T. H. Grayson, R. Haddock, Y. T. Hwang, A. P. Braun, G. Peichun, R. J. Korthuis, M. J. Davis, et al. Heterogeneity in function of small artery smooth muscle BKCa: involvement of the \#946;1-subunit J. Physiol., June 15, 2009; 587(12): 3025 - 3044. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Earley, A. L. Gonzales, and R. Crnich Endothelium-Dependent Cerebral Artery Dilation Mediated by TRPA1 and Ca2+-Activated K+ Channels Circ. Res., April 24, 2009; 104(8): 987 - 994. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Morin, M. Sirois, V. Echave, and E. Rousseau CPI-17 Silencing-Reduced Responsiveness in Control and TNF-{alpha}-Treated Human Bronchi Am. J. Respir. Cell Mol. Biol., December 1, 2008; 39(6): 638 - 643. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Gomis, S. Soriano, C. Belmonte, and F. Viana Hypoosmotic- and pressure-induced membrane stretch activate TRPC5 channels J. Physiol., December 1, 2008; 586(23): 5633 - 5649. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. E. Link, K. Murakami, M. Beem-Miller, B. I. Tranmer, and G. C. Wellman Oxyhemoglobin-Induced Expression of R-Type Ca2+ Channels in Cerebral Arteries Stroke, July 1, 2008; 39(7): 2122 - 2128. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Q. Xi, A. Adebiyi, G. Zhao, K. E. Chapman, C. M. Waters, A. Hassid, and J. H. Jaggar IP3 Constricts Cerebral Arteries via IP3 Receptor-Mediated TRPC3 Channel Activation and Independently of Sarcoplasmic Reticulum Ca2+ Release Circ. Res., May 9, 2008; 102(9): 1118 - 1126. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Raina, S. R. Ella, and M. A. Hill Decreased activity of the smooth muscle Na+/Ca2+ exchanger impairs arteriolar myogenic reactivity J. Physiol., March 15, 2008; 586(6): 1669 - 1681. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. M. Touyz Transient receptor potential melastatin 6 and 7 channels, magnesium transport, and vascular biology: implications in hypertension Am J Physiol Heart Circ Physiol, March 1, 2008; 294(3): H1103 - H1118. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. A. Drummond, S. C. Grifoni, and N. L. Jernigan A New Trick for an Old Dogma: ENaC Proteins as Mechanotransducers in Vascular Smooth Muscle Physiology, February 1, 2008; 23(1): 23 - 31. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Schubert, D. Lidington, and S.-S. Bolz The emerging role of Ca2+ sensitivity regulation in promoting myogenic vasoconstriction Cardiovasc Res, January 1, 2008; 77(1): 8 - 18. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. A. Reading and J. E. Brayden Central Role of TRPM4 Channels in Cerebral Blood Flow Regulation Stroke, August 1, 2007; 38(8): 2322 - 2328. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Earley, S. V. Straub, and J. E. Brayden Protein kinase C regulates vascular myogenic tone through activation of TRPM4 Am J Physiol Heart Circ Physiol, June 1, 2007; 292(6): H2613 - H2622. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Hill and M. J. Davis Coupling a change in intraluminal pressure to vascular smooth muscle depolarization: still stretching for an explanation Am J Physiol Heart Circ Physiol, June 1, 2007; 292(6): H2570 - H2572. [Full Text] [PDF]
|
|
|
|
 |
|
 B. Nilius, G. Owsianik, T. Voets, and J. A. Peters Transient Receptor Potential Cation Channels in Disease Physiol Rev, January 1, 2007; 87(1): 165 - 217. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Numata, T. Shimizu, and Y. Okada TRPM7 is a stretch- and swelling-activated cation channel involved in volume regulation in human epithelial cells Am J Physiol Cell Physiol, January 1, 2007; 292(1): C460 - C467. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Ito, Y. P. R. Jarajapu, M. B Grant, and H. J Knot Characteristics of myogenic tone in the rat ophthalmic artery Am J Physiol Heart Circ Physiol, January 1, 2007; 292(1): H360 - H368. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Zhang, R. Berra-Romani, M. J. Sinnegger-Brauns, J. Striessnig, M. P. Blaustein, and D. R. Matteson Role of Cav1.2 L-type Ca2+ channels in vascular tone: effects of nifedipine and Mg2+ Am J Physiol Heart Circ Physiol, January 1, 2007; 292(1): H415 - H425. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. L. Jernigan and H. A. Drummond Myogenic vasoconstriction in mouse renal interlobar arteries: role of endogenous beta and {gamma}ENaC Am J Physiol Renal Physiol, December 1, 2006; 291(6): F1184 - F1191. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Guinamard, M. Demion, C. Magaud, D. Potreau, and P. Bois Functional Expression of the TRPM4 Cationic Current in Ventricular Cardiomyocytes From Spontaneously Hypertensive Rats Hypertension, October 1, 2006; 48(4): 587 - 594. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Inoue, L. J. Jensen, J. Shi, H. Morita, M. Nishida, A. Honda, and Y. Ito Transient Receptor Potential Channels in Cardiovascular Function and Disease Circ. Res., July 21, 2006; 99(2): 119 - 131. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. V. Straub and M. T. Nelson Molecular Coding of Kv1 Channels to Oppose Myogenic Constriction Circ. Res., July 7, 2006; 99(1): 13 - 14. [Full Text] [PDF]
|
|
|
|
|
|
S. Earley Molecular Diversity of Receptor Operated Channels in Vascular Smooth Muscle: A Role for Heteromultimeric TRP Channels? Circ. Res., June 23, 2006; 98(12): 1462 - 1464. [Full Text] [PDF]
|
|
|
|
|
|
Y. Maruyama, Y. Nakanishi, E. J. Walsh, D. P. Wilson, D. G. Welsh, and W. C. Cole Heteromultimeric TRPC6-TRPC7 Channels Contribute to Arginine Vasopressin-Induced Cation Current of A7r5 Vascular Smooth Muscle Cells Circ. Res., June 23, 2006; 98(12): 1520 - 1527. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-Z. Xu, K. Muraki, F. Zeng, J. Li, P. Sukumar, S. Shah, A. M. Dedman, P. K. Flemming, D. McHugh, J. Naylor, et al. A Sphingosine-1-Phosphate-Activated Calcium Channel Controlling Vascular Smooth Muscle Cell Motility Circ. Res., June 9, 2006; 98(11): 1381 - 1389. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X.-R. Yang, M.-J. Lin, L. S. McIntosh, and J. S. K. Sham Functional expression of transient receptor potential melastatin- and vanilloid-related channels in pulmonary arterial and aortic smooth muscle Am J Physiol Lung Cell Mol Physiol, June 1, 2006; 290(6): L1267 - L1276. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Earley, T. J. Heppner, M. T. Nelson, and J. E. Brayden TRPV4 Forms a Novel Ca2+ Signaling Complex With Ryanodine Receptors and BKCa Channels Circ. Res., December 9, 2005; 97(12): 1270 - 1279. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. E. Clapham, D. Julius, C. Montell, and G. Schultz International Union of Pharmacology. XLIX. Nomenclature and Structure-Function Relationships of Transient Receptor Potential Channels Pharmacol. Rev., December 1, 2005; 57(4): 427 - 450. [Full Text] [PDF]
|
|
|
|
 |
|
 Z. Zhang, H. Okawa, Y. Wang, and E. R. Liman Phosphatidylinositol 4,5-Bisphosphate Rescues TRPM4 Channels from Desensitization J. Biol. Chem., November 25, 2005; 280(47): 39185 - 39192. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. Yao and C. J. Garland Recent Developments in Vascular Endothelial Cell Transient Receptor Potential Channels Circ. Res., October 28, 2005; 97(9): 853 - 863. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Dietrich, M. Mederos y Schnitzler, M. Gollasch, V. Gross, U. Storch, G. Dubrovska, M. Obst, E. Yildirim, B. Salanova, H. Kalwa, et al. Increased Vascular Smooth Muscle Contractility in TRPC6-/- Mice Mol. Cell. Biol., August 15, 2005; 25(16): 6980 - 6989. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Nilius, T. Voets, and J. Peters TRP Channels in Disease Sci. Signal., August 2, 2005; 2005(295): re8 - re8. [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]
|
|
|
|
|
|
B. Nilius, J. Prenen, A. Janssens, G. Owsianik, C. Wang, M. X. Zhu, and T. Voets The Selectivity Filter of the Cation Channel TRPM4 J. Biol. Chem., June 17, 2005; 280(24): 22899 - 22906. [Abstract] [Full Text] [PDF]
|
|