TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels

Circulation Research

Volumn 97, Issue 12, 2005, Pages 1270-1279

  Earley, Scott ^a,b   Heppner, Thomas J ^a   Nelson, Mark T ^a   Brayden, Joseph E ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Ca2+ sparks; Ca2+ transients; Eicosanoids; Ion channels; Ryanodine receptor; Vascular smooth muscle; Vasodilation

Indexed keywords

11,12 EPOXY 5,8,14 ICOSATRIENOIC ACID; 4ALPHA PHORBOL DIDECANOATE; CALCIUM ION; EPOXYICOSATRIENOIC ACID; RYANODINE RECEPTOR; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 4; VANILLOID RECEPTOR 4 AGONIST; VOLTAGE GATED CALCIUM CHANNEL; 11,12 EPOXY 5,8,14 EICOSATRIENOIC ACID; 11,12-EPOXY-5,8,14-EICOSATRIENOIC ACID; CALCIUM; DIHOMO GAMMA LINOLENIC ACID; DRUG DERIVATIVE; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; TRPV4 PROTEIN, RAT; VANILLOID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY DILATATION; ARTICLE; BLOOD PRESSURE REGULATION; BRAIN ARTERY; CALCIUM CONDUCTANCE; CALCIUM TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM CELL; HYPERPOLARIZATION; LASER MICROSCOPY; MALE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SARCOLEMMA; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE; VASODILATATION; ANIMAL; CALCIUM SIGNALING; CHEMISTRY; DRUG EFFECT; METABOLISM; PHYSIOLOGY; SMOOTH MUSCLE FIBER; SPRAGUE DAWLEY RAT;

8,11,14-EICOSATRIENOIC ACID; ANIMALS; CALCIUM; CALCIUM SIGNALING; CEREBRAL ARTERIES; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MALE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; RATS; RATS, SPRAGUE-DAWLEY; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; TRPV CATION CHANNELS; VASODILATION;

EID: 33644671418     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000194321.60300.d6     Document Type: Article

References (34)

1. Roman RJ. P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev. 2002;82:131-185.
2. Campbell WB, Gebremedhin D, Pratt PF, Harder DR. Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors. Circ Res. 1996;78:415-423.
3. Fisslthaler B, Popp R, Kiss L, Potente M, Harder DR, Fleming I, Busse R. Cytochrome P450 2C is an EDHF synthase in coronary arteries. Nature. 1999;401:493-497.
4. Zou AP, Fleming JT, Falck JR, Jacobs ER, Gebremedhin D, Harder DR, Roman RJ. Stereospecific effects of epoxyeicosatrienoic acids on renal vascular tone and K(+)-channel activity. Am J Physiol. 1996;270:F822-F832.
5. Clapham DE. TRP channels as cellular sensors. Nature. 2003;426:517-524.
6. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature. 2003;424:434-438.
7. Fang X, Weintraub NL, Stoll LL, Spector AA. Epoxyeicosatrienoic acids increase intracellular calcium concentration in vascular smooth muscle cells. Hypertension. 1999;34:1242-1246.
8. Watanabe H, Davis JB, Smart D, Jerman JC, Smith GD, Hayes P, Vriens J, Cairns W, Wissenbach U, Prenen J, Flockerzi V, Droogmans G, Benham CD, Nilius B. Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem. 2002;277:13569-13577.
9. Jia Y, Wang X, Varty L, Rizzo CA, Yang R, Correll CC, Phelps PT, Egan RW, Hey JA. Functional TRPV4 channels are expressed in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2004;287:L272-L278.
10. Nelson MT, Cheng H, Rubart M, Santana LF, Bonev AD, Knot HJ, Lederer WJ. Relaxation of arterial smooth muscle by calcium sparks. Science. 1995;270:633-637.
11. Herrmann-Frank A, Darling E, Meissner G. Functional characterization of the Ca(2+)-gated Ca2+ release channel of vascular smooth muscle sarcoplasmic reticulum. Pflugers Arch. 1991;418:353-359.
12. ZhuGe R, Tuft RA, Fogarty KE, Bellve K, Fay FS, Walsh JV Jr. The influence of sarcoplasmic reticulum Ca2+ concentration on Ca2+ sparks and spontaneous transient outward currents in single smooth muscle cells. J Gen Physiol. 1999;113:215-228.
13. Endo M, Tanaka M, Ogawa Y. Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres. Nature. 1970;228:34-36.
14. Ford LE, Podolsky RJ. Regenerative calcium release within muscle cells. Science. 1970;167:58-59.
15. Heppner TJ, Bonev AD, Santana LF, Nelson MT. Alkaline pH shifts Ca2+ sparks to Ca2+ waves in smooth muscle cells of pressurized cerebral arteries. Am J Physiol Heart Circ Physiol. 2002;283:H2169-H2176.
16. Perez GJ, Bonev AD, Patlak JB, Nelson MT. Functional coupling of ryanodine receptors to KCa channels in smooth muscle cells from rat cerebral arteries. J Gen Physiol. 1999;113:229-238.
17. Alessandri-Haber N, Dina OA, Yeh JJ, Parada CA, Reichling DB, Levine JD. Transient receptor potential vanilloid 4 is essential in chemotherapy-induced neuropathic pain in the rat. J Neurosci. 2004;24:4444-4452.
18. Lesh RE, Somlyo AP, Owens GK, Somlyo AV. Reversible permeabilization. A novel technique for the intracellular introduction of antisense oligodeoxynucleotides into intact smooth muscle. Circ Res. 1995;77:220-230.
19. Bergdahl A, Gomez MF, Wihlborg AK, Erlinge D, Eyjolfson A, Xu SZ, Beech DJ, Dreja K, Hellstrand P. Plasticity of TRPC expression in arterial smooth muscle: correlation with store-operated Ca2+ entry. Am J Physiol Cell Physiol. 2005;288:C872-C880.
20. Reading SA, Earley S, Waldron BJ, Welsh DG, Brayden JE. TRPC3 mediates pyrimidine receptor-induced depolarization of cerebral arteries. Am J Physiol Heart Circ Physiol. 2005;288:H2055-H2061.
21. Welsh DG, Morielli AD, Nelson MT, Brayden JE. Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ Res. 2002;90:248-250.
22. Earley S, Waldron BJ, Brayden JE. Critical role for transient receptor potential channel TRPM4 in myogenic constriction of cerebral arteries. Circ Res. 2004;95:922-929.
23. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol. 2000;2:695-702.
24. Earley S, Pastuszyn A, Walker BR. Cytochrome p-450 epoxygenase products contribute to attenuated vasoconstriction after chronic hypoxia. Am J Physiol Heart Circ Physiol. 2003;285:H127-H136.
25. Ye D, Zhou W, Lee HC. Activation of rat mesenteric arterial KATP channels by 11,12-epoxyeicosatrienoic acid. Am J Physiol Heart Circ Physiol. 2005;288:H358-H364.
26. Dumoulin M, Salvail D, Gaudreault SB, Cadieux A, Rousseau E. Epoxyeicosatrienoic acids relax airway smooth muscles and directly activate reconstituted KCa channels. Am J Physiol. 1998;275:L423-L431.
27. Gebremedhin D, Ma YH, Falck JR, Roman RJ, VanRollins M, Harder DR. Mechanism of action of cerebral epoxyeicosatrienoic acids on cerebral arterial smooth muscle. Am J Physiol. 1992;263:H519-H525.
28. Li PL, Campbell WB. Epoxyeicosatrienoic acids activate K+ channels in coronary smooth muscle through a guanine nucleotide binding protein. Circ Res. 1997;80:877-884.
29. Niggli E, Lederer WJ. Voltage-independent calcium release in heart muscle. Science. 1990;250:565-568.
30. Ouyang K, Wu C, Cheng H. CA2+-induced CA2+ release in sensory neurons: low-gain amplification confers intrinsic stability. J Biol Chem. 2005;280:15898-15902.
31. Lemmens R, Larsson O, Berggren PO, Islam MS. Ca2+-induced Ca2+ release from the endoplasmic reticulum amplifies the Ca2+ signal mediated by activation of voltage-gated L-type Ca2+ channels in pancreatic beta-cells. J Biol Chem. 2001;276:9971-9977.
32. Jaggar JH, Porter VA, Lederer WJ, Nelson MT. Calcium sparks in smooth muscle. Am J Physiol Cell Physiol. 2000;278:C235-C256.
33. Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B. Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem. 2002;277:47044-47051.
34. Kahn-Kirby AH, Dantzker JL, Apicella AJ, Schafer WR, Browse J, Bargmann CI, Watts JL. Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo. Cell. 2004;119:889-900.