Is there a role for T- type Ca2+ channels in regulation of vasomotor tone in mesenteric arterioles?

Canadian Journal of Physiology and Pharmacology

Volumn 87, Issue 1, 2009, Pages 8-20

  Jensen, Lars Jørn ^a   Holstein Rathlou, Niels Henrik ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Conducted vasomotor response; Endothelium; Microcirculation; Pharmacology; T Type channel; Vascular smooth muscle; Voltage dependent ca2+ channel

Indexed keywords

CALCIUM CHANNEL T TYPE; VOLTAGE GATED CALCIUM CHANNEL;

ARTERIOLE; BLOOD VESSEL TONE; CALCIUM CURRENT; HUMAN; MESENTERIC ARTERY; MICROCIRCULATION; MICROVASCULARIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SMOOTH MUSCLE CONTRACTION; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE; VASOMOTOR REFLEX;

ANIMALS; ARTERIOLES; CALCIUM; CALCIUM CHANNELS, T-TYPE; ENDOTHELIUM, VASCULAR; HUMANS; MESENTERIC ARTERIES; MUSCLE, SMOOTH, VASCULAR; VASOCONSTRICTION;

EID: 65249182068     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/Y08-101     Document Type: Review

References (71)

1. Akaike, N., Kanaide, H., Kuga, T., Nakamura, M., Sadoshima, J., and Tomoike, H. 1989. Low-voltage-activated calcium current in rat aorta smooth muscle cells in primary culture. J. Physiol. 416: 141-160. PMID:2558173.
2. 2+ signaling during terminal differentiation (fusion) of human myoblasts. Proc. Natl. Acad. Sci. U.S.A. 97: 7627-7632. doi:10.1073/pnas.97.13.7627. PMID:10861024.
3. Bradley, J.E., Anderson, U.A., Woolsey, S.M., Thornbury, K.D., McHale, N.G., and Hollywood, M.A. 2004. Characterization of T-type calcium current and its contribution to electrical activity in rabbit urethra. Am. J. Physiol. Cell Physiol. 286: C1078- C1088. doi:10.1152/ajpcell.00463.2003. PMID:15075207.
4. Braunstein, T.H., Inoue, R., Cribbs, L., Oike, M., Ito, Y., Holstein- Rathlou, N.H., and Jensen, L.J. 2009. The role of L- and T- type channels in local and remote calcium responses in rat mesenteric terminal arterioles. J. Vasc. Res. 46: 138-151. doi:10.1159/000151767.
5. Brueggemann, L.I., Martin, B.L., Barakat, J., Byron, K.L., and Cribbs, L.L. 2005. Low voltage-activated calcium channels in vascular smooth muscle: T- type channels and AVP- stimulated calcium spiking. Am. J. Physiol. Heart Circ. Physiol. 288:H923-H935. doi:10.1152/ajpheart.01126.2003. PMID:15498818.
6. 2+ channels. Annu. Rev. Cell Dev. Biol. 16: 521-555. doi:10.1146/annurev.cellbio.16.1.521. PMID:11031246.
7. Catterall, W.A., Striessnig, J., Snutch, T.P., and Perez-Reyes, E. 2003. International Union of Pharmacology. XL. Compendium of voltage-gated ion channels: calcium channels. Pharmacol. Rev. 55: 579-581. doi:10.1124/pr.55.4.8. PMID:14657414.
8. 2+ channel gating properties. Biophys. J. 80: 1238-1250. PMID:11222288.
9. 2+ channels. Science, 302: 1416-1418. doi:10.1126/science.1089268. PMID:14631046.
10. Cribbs, L.L. 2006. T-type Ca2+ channels in vascular smooth muscle: multiple functions. Cell Calcium, 40: 221-230. doi:10.1016/j.ceca.2006. 04.026. PMID:16797699.
11. Dalton, S., Takahashi, S.X., Miriyala, J., and Colecraft, H.M. 2005. A single CaVbeta can reconstitute both trafficking and macroscopic conductance of voltage-dependent calcium channels. J. Physiol. 567: 757-769. doi:10.1113/jphysiol.2005.093195. PMID:16020456.
12. de Weille, J.R., Schweitz, H., Maes, P., Tartar, A., and Lazdunski, M. 1991. Calciseptine, a peptide isolated from black mamba venom, is a specific blocker of the L- type calcium channel. Proc. Natl. Acad. Sci. U.S.A. 88: 2437-2440. doi:10.1073/pnas.88.6. 2437. PMID:1848702.
13. Emerick, M.C., Stein, R., Kunze, R., McNulty, M.M., Regan, M.R., Hanck, D.A., et al. 2006. Profiling the array of Ca(v)3.1 variants from the human T- type calcium channel gene CACNA1G: alternative structures, developmental expression, and biophysical variations. Proteins, 64: 320-342. doi:10.1002/prot.20877. PMID:16671074.
14. Feng, Z.P., Doering, C.J., Winkfein, R.J., Beedle, A.M., Spafford, J.D., and Zamponi, G.W. 2003. Determinants of inhibition of transiently expressed voltage-gated calcium channels by omega- conotoxins GVIA and MVIIA. J. Biol. Chem. 278: 20171-20178. doi:10.1074/jbc.M300581200. PMID:12654924.
15. Feng, M.G., Li, M., and Navar, L.G. 2004. T- type calcium channels in the regulation of afferent and efferent arterioles in rats. Am. J. Physiol. Renal Physiol. 286: F331-F337. doi:10.1152/ ajprenal.00251.2003. PMID:14583435.
16. Figueroa, X.F., Chen, C.C., Campbell, K.P., Damon, D.N., Day, K.H., Ramos, S., et al. 2007. Are voltage-dependent ion channels involved in the endothelial cell control of vasomotor tone? Am. J. Physiol. Heart Circ. Physiol. 293: H1371-H1383. doi:10. 1152/ajpheart.01368.2006. PMID:17513486.
17. Fisher, A.B., Al-Mehdi, A.B., and Manevich, Y. 2002. Shear stress and endothelial cell activation. Crit. Care Med. 30: S192-S197. doi:10.1097/00003246-200205001-00004. PMID:12004235.
18. 2+ channels. Br. J. Pharmacol. 143: 1050-1057. doi:10.1038/sj.bjp.0705944. PMID:15545287.
19. Gustafsson, F., and Holstein-Rathlou, N. 1999. Conducted vasomo- tor responses in arterioles: characteristics, mechanisms and physiological significance. Acta Physiol. Scand. 167: 11-21. doi:10. 1046/j.1365-201x.1999.00582.x. PMID:10519972.
20. 2+ channels. Am. J. Physiol. Heart Circ. Physiol. 280: H582-H590. PMID:11158955.
21. 2+ channel, and it is functionally important in renal afferent arterioles. Circ. Res. 87:896-902. PMID:11073885.
22. Hansen, P.B., Jensen, B.L., Andreasen, D., and Skott, O. 2001. Differential expression of T- and L- type voltage-dependent calcium channels in renal resistance vessels. Circ. Res. 89: 630-638. doi:10.1161/hh1901. 097126. PMID:11577029.
23. 2+ channel subtypes and pharmacology in the kidney. Circ. Res. 100: 342-353. doi:10.1161/01.RES. 0000256155.31133.49. PMID:17307972.
24. Hobom, M., Dai, S., Marais, E., Lacinova, L., Hofmann, F., and Klugbauer, N. 2000. Neuronal distribution and functional characterization of the calcium channel alpha2delta-2 subunit. Eur. J. Neurosci. 12: 1217-1226. doi:10.1046/j.1460-9568.2000. 01009.x. PMID:10762351.
25. Huang, L., Keyser, B.M., Tagmose, T.M., Hansen, J.B., Taylor, J.T., Zhuang, H., et al. 2004. NNC 55-0396 [(1S,2S)-2-(2-(N- [(3-benzimidazol-2-yl) propyl]-N-methylamino)ethyl)-6-fluo ro- 1,2,3,4-tetrahydro-1-isopropyl-2-naphtyl cyclopropanecarboxy- late dihydrochloride]: a new selective inhibitor of T-type calcium channels. J. Pharmacol. Exp. Ther. 309: 193-199. doi:10. 1124/jpet.103.060814. PMID:14718587.
26. Inoue, R., and Mori, Y. 2003. New target molecules in the drug control of blood pressure and circulation. Curr. Drug Targets Cardiovasc. Haematol. Disord. 3: 59-72. doi:10.2174/1568006033337348. PMID:12769645.
27. 2+ channel current in PC12 cells. Eur. J. Pharmacol. 314: 143-150. doi:10.1016/S0014-2999(96)00500-6. PMID:8957230.
28. 2+ channel to diameter regulation in rabbit mesenteric artery. Life Sci. 72: 487-500. doi:10.1016/S0024-3205(02)02286-5. PMID:12467889.
29. Jensen, L.J., Salomonsson, M., Jensen, B.L., and Holstein- Rathlou, N.H. 2004. Depolarization-induced calcium influx in rat mesen- teric small arterioles is mediated exclusively via mibefradil- sensitive calcium channels. Br. J. Pharmacol. 142: 709-718. doi:10.1038/sj.bjp.0705841. PMID:15172957.
30. Jimenez, C., Bourinet, E., Leuranguer, V., Richard, S., Snutch, T.P., and Nargeot, J. 2000. Determinants of voltage-dependent inactivation affect Mibefradil block of calcium channels. Neuropharmacology, 39: 1-10. doi:10.1016/S0028-3908(99)00153-7. PMID:10665814.
31. Kaku, T., Lee, T.S., Arita, M., Hadama, T., and Ono, K. 2003. The gating and conductance properties of CaV3.2 low-voltage-activated T- type calcium channels. Jpn. J. Physiol. 53: 165-172. doi:10.2170/jjphysiol.53.165. PMID:14529577.
32. Klugbauer, N., Marais, E., Lacinova, L., and Hofmann, F. 1999. A T- type calcium channel from mouse brain. Pflugers Arch. 437:710-715. doi:10.1007/s004240050836. PMID:10087148.
33. 2+] in cerebral arteries of rat by membrane potential and intravascular pressure. J. Physiol. 508(Pt 1): 199-209. PMID:9490839.
34. Krotz, F., Sohn, H.Y., Keller, M., Gloe, T., Bolz, S.S., Becker, B.F., et al. 2002. Depolarization of endothelial cells enhances platelet aggregation through oxidative inactivation of endothelial NTPDase. Arterioscler. Thromb. Vasc. Biol. 22: 2003-2009. doi:10.1161/01.ATV.0000043454.08172.51. PMID:12482826.
35. Lee, J.H., Gomora, J.C., Cribbs, L.L., and Perez-Reyes, E. 1999. Nickel block of three cloned T- type calcium channels: low concentrations selectively block alpha1H. Biophys. J. 77: 3034-3042. PMID:10585925.
36. Lee, T.S., Kaku, T., Takebayashi, S., Uchino, T., Miyamoto, S., Hadama, T., et al. 2006. Actions of mibefradil, efonidipine and nifedipine block of recombinant T- and L-type Ca channels with distinct inhibitory mechanisms. Pharmacology, 78: 11-20. doi:10.1159/000094900. PMID:16899990.
37. Lory, P., Bidaud, I., and Chemin, J. 2006. T- type calcium channels in differentiation and proliferation. Cell Calcium, 40: 135-146. doi:10.1016/j.ceca.2006.04.017. PMID:16797068.
38. Loutzenhiser, R., Chilton, L., and Trottier, G. 1997. Membrane potential measurements in renal afferent and efferent arterioles: actions of angiotensin II. Am. J. Physiol. 273: F307-F314. PMID:9277592.
39. 2+ stores to smooth muscle contraction in arteries and arterioles of rat, guinea-pig, dog and rabbit. Clin. Exp. Pharmacol. Physiol. 23: 310-316. doi:10.1111/j.1440-1681.1996.tb02829.x. PMID:8717067.
40. Martin, R.L., Lee, J.H., Cribbs, L.L., Perez-Reyes, E., and Hanck, D.A. 2000. Mibefradil block of cloned T- type calcium channels. J. Pharmacol. Exp. Ther. 295: 302-308. PMID:10991994.
41. 2+ current by efonidipine in cardiomyocytes. Life Sci. 68: 345-351. doi:10.1016/S0024-3205(00) 00932-2. PMID:11191650.
42. McDonald, T.F., Pelzer, S., Trautwein, W., and Pelzer, D.J. 1994. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol. Rev. 74: 365-507. PMID:8171118.
43. Mintz, I.M., Venema, V.J., Swiderek, K.M., Lee, T.D., Bean, B.P., and Adams, M.E. 1992. P-type calcium channels blocked by the spider toxin omega- Aga- IVA. Nature, 355: 827-829. doi:10.1038/355827a0. PMID:1311418.
44. Moosmang, S., Haider, N., Bruderl, B., Welling, A., and Hofmann, F. 2006. Antihypertensive effects of the putative T- type calcium channel antagonist mibefradil are mediated by the L- type cacium channel Cav1.2. Circ. Res. 98: 105-110. doi:10.1161/01. RES.0000197851.11031.9c. PMID:16306443.
45. Morel, N., Buryi, V., Feron, O., Gomez, J.P., Christen, M.O., and Godfraind, T. 1998. The action of calcium channel blockers on recombinant L- type calcium channel alpha1-subunits. Br. J. Pharmacol. 125: 1005-1012. doi:10.1038/sj.bjp.0702162. PMID:9846638.
46. 2+ channels in the terminal mesenteric artery of guinea pig. Circ. Res. 85: 596-605. PMID:10506484.
47. 2+ currents in the rat terminal mesenteric artery. Br. J. Pharmacol. 137: 467-476. doi:10.1038/sj.bjp.0704892. PMID:12359628.
48. 2+ channel beta3 subunit. J. Biol. Chem. 278: 43261-43267. doi:10.1074/jbc. M211380200. PMID:12920136.
49. Navedo, M.F., Amberg, G.C., Westenbroek, R.E., Sinnegger- Brauns, M.J., Catterall, W.A., Striessnig, J., et al. 2007. CaV1.3 channels produce persistent calcium sparklets, but CaV1.2 channels are responsible for sparklets in mouse arterial smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 293: H1359-H1370. doi:10.1152/ajpheart.00450.2007. PMID:17526649.
50. Nelson, M.T., Patlak, J.B., Worley, J.F., and Standen, N.B. 1990. Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am. J. Physiol. 259: C3-C18. PMID:2164782.
51. Newcomb, R., Szoke, B., Palma, A., Wang, G., Chen, X., Hopkins, W., et al. 1998. Selective peptide antagonist of the class E calcium channel from the venom of the tarantula Hysterocrates gigas. Biochemistry, 37: 15353-15362. doi:10.1021/bi981255g. PMID:9799496.
52. 2+- and volume-activated Cl- channels in macrovascular endothelial cells. Br. J. Pharmacol. 121: 547-555. doi:10.1038/sj.bjp.0701140. PMID:9179399.
53. Oshima, T., Ozono, R., Yano, Y., Higashi, Y., Teragawa, H., Miho, N., et al. 2005. Beneficial effect of T- type calcium channel blockers on endothelial function in patients with essential hypertension. Hypertens. Res. 28: 889-894. doi:10.1291/hypres.28. 889. PMID:16555577.
54. Perez-Reyes, E. 2003. Molecular physiology of low-voltage-activated t- type calcium channels. Physiol. Rev. 83: 117-161. PMID:12506128.
55. Perez-Reyes, E. 2006. Molecular characterization of T- type calcium channels. Cell Calcium, 40: 89-96. doi:10.1016/j.ceca. 2006.04.012. PMID:16759699.
56. Potocnik, S.J., Murphy, T.V., Kotecha, N., and Hill, M.A. 2000. Effects of mibefradil and nifedipine on arteriolar myogenic responsiveness and intracellular Ca2+. Br. J. Pharmacol. 131:1065-1072. doi:10.1038/sj.bjp. 0703650. PMID:11082112.
57. Salomonsson, M., Gustafsson, F., Andreasen, D., Jensen, B.L., and Holstein- Rathlou, N.H. 2002. Local electric stimulation causes conducted calcium response in rat interlobular arteries. Am. J. Physiol. Renal Physiol. 283: F473-F480. PMID:12167598. Santi, C.M., Cayabyab, F.S., Sutton, K.G., McRory, J.E., Me- zeyova, J., Hamming, K.S., et al. 2002. Differential inhibition of T- type calcium channels by neuroleptics. J. Neurosci. 22:396-403. PMID:11784784.
58. Segal, S.S. 2005. Regulation of blood flow in the microcirculation. Microcirculation, 12: 33-45. doi:10.1080/10739680590895028. PMID:15804972.
59. Segal, S.S., Damon, D.N., and Duling, B.R. 1989. Propagation of vasomotor responses coordinates arteriolar resistances. Am. J. Physiol. 256: H832-H837. PMID:2923241.
60. 2+ currents in single myocytes from human mesenteric arteries: evidence for a physiological role of L-type channels. J. Physiol. 457: 455-475. PMID:1338463.
61. Song, C., Al-Mehdi, A.B., and Fisher, A.B. 2001. An immediate endothelial cell signaling response to lung ischemia. Am. J. Physiol. Lung Cell. Mol. Physiol. 281: L993-L1000. PMID:11557603.
62. Stekiel, W.J., Contney, S.J., and Lombard, J.H. 1986. Small vessel membrane potential, sympathetic input, and electrogenic pump rate in SHR. Am. J. Physiol. 250: C547-C556. PMID:3008565.
63. van Breemen, C., Chen, Q., and Laher, I. 1995. Superficial buffer barrier function of smooth muscle sarcoplasmic reticulum. Trends Pharmacol. Sci. 16: 98-105. doi:10.1016/S0165- 6147(00)88990-7. PMID:7792935.
64. VanBavel, E., Sorop, O., Andreasen, D., Pfaffendorf, M., and Jensen, B.L. 2002. Role of T- type calcium channels in myogenic tone of skeletal muscle resistance arteries. Am. J. Physiol. Heart Circ. Physiol. 283: H2239-H2243. PMID:12388244.
65. Walker, D., and De Waard, M. 1998. Subunit interaction sites in voltage-dependent Ca2+ channels: role in channel function. Trends Neurosci. 21: 148-154. doi:10.1016/S0166-2236(97) 01200-9. PMID:9554724.
66. 2+ flux through voltage-gated channels with flow cessation in pulmonary microvascular endothelial cells. Micro- circulation, 11: 517-526. doi:10.1080/10739680490476367. PMID:15371132.
67. 2+ channels mediate vaso- occlusion of sickled erythrocytes in lung microcirculation. Circ. Res. 93: 346-353. doi:10.1161/01.RES.0000087148. 75363. 8F. PMID:12869394.
68. 2+ channel subunits on native Ca2+ channel currents in undifferentiated mammalian NG108-15 cells. J. Physiol. 510(Pt 2): 347-360. doi:10.1111/j.1469-7793.1998.347bk.x. PMID:9705988.
69. 2+ channels in murine HL-1 cells. J. Mol. Cell. Cardiol. 36:111-119. doi:10.1016/j.yjmcc.2003.10.007. PMID:14734053.
70. Zhou, C., and Wu, S. 2006. T-type calcium channels in pulmonary vascular endothelium. Microcirculation, 13: 645-656. doi:10.1080/ 10739680600930289. PMID:17085425.
71. Zhou, C., Chen, H., Lu, F., Sellak, H., Daigle, J.A., Alexeyev, M.F., et al. 2007. Cav3.1 (alpha1G) controls von Willebrand factor secretion in rat pulmonary microvascular endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 292: L833-L844. doi:10.1152/ajplung.00377.2006. PMID:17172292.