Functional and pharmacological consequences of the distribution of voltage-gated calcium channels inthe renal blood vessels

Acta Physiologica

Volumn 207, Issue 4, 2013, Pages 690-699

  Hansen, P B L ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Blood vessels; Calcium channels; Kidney

Indexed keywords

AGATOXIN; AMLODIPINE; BENIDIPINE; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; EFONIDIPINE; FELODIPINE; ISRADIPINE; MIBEFRADIL; NIFEDIPINE; NILVADIPINE; NITRENDIPINE; VOLTAGE GATED CALCIUM CHANNEL;

ARTERIOLE; ARTERY CONSTRICTION; BLOOD PRESSURE REGULATION; EFFECTOR ARTERIOLE; GLOMERULUS; HUMAN; HYPERTENSION; KIDNEY BLOOD VESSEL; KIDNEY FUNCTION; PRIORITY JOURNAL; PROTEINURIA; RENAL PROTECTION; REVIEW; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VASODILATATION;

ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CALCIUM CHANNELS, L-TYPE; CALCIUM CHANNELS, T-TYPE; DISEASE MODELS, ANIMAL; GLOMERULAR FILTRATION RATE; HUMANS; HYPERTENSION; MICE; RATS; RENAL ARTERY;

EID: 84874737051     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12070     Document Type: Review

References (84)

1. Altier, C. & Zamponi, G.W. 2004. Targeting Ca2+ channels to treat pain: T-type versus N-type. Trends Pharmacol Sci 25, 465-470.
2. Andreasen, D., Jensen, B.L., Hansen, P.B., Kwon, T.H., Nielsen, S. & Skott, O. 2000. The alpha(1G)-subunit of a voltage-dependent Ca(2+) channel is localized in rat distal nephron and collecting duct. Am J Physiol Renal Physiol 279, F997-F1005.
3. Andreasen, D., Friis, U.G., Uhrenholt, T.R., Jensen, B.L., Skott, O. & Hansen, P.B. 2006. Coexpression of voltage-dependent calcium channels Cav1.2, 2.1a, and 2.1b in vascular myocytes. Hypertension 47, 735-741.
4. Arima, S., Ito, S., Omata, K., Tsunoda, K., Yaoita, H. & Abe, K. 1996. Diverse effects of calcium antagonists on glomerular hemodynamics. Kidney Int Suppl 55, S132-S134.
5. Ball, C.J., Wilson, D.P., Turner, S.P., Saint, D.A. & Beltrame, J.F. 2009. Heterogeneity of L- and T-channels in the vasculature: rationale for the efficacy of combined L- and T-blockade. Hypertension 53, 654-660.
6. Birnbaumer, L., Campbell, K.P., Catterall, W.A., Harpold, M.M., Hofmann, F., Horne, W.A., Mori, Y., Schwartz, A., Snutch, T.P., Tanabe, T. & Tsien, R.W. 1994. The naming of voltage-gated calcium channels. Neuron 13, 505-506.
7. Braunstein, T.H., Inoue, R., Cribbs, L., Oike, M., Ito, Y., Holstein-Rathlou, N.H. & Jensen, L.J. 2008. The role of L- and T-type calcium channels in local and remote calcium responses in rat mesenteric terminal arterioles. J Vasc Res 46, 138-151.
8. Carmines, P.K. & Navar, L.G. 1989. Disparate effects of Ca channel blockade on afferent and efferent arteriolar responses to ANG II. Am J Physiol 256, F1015-F1020.
9. Carmines, P.K., Fowler, B.C. & Bell, P.D. 1993. Segmentally distinct effects of depolarization on intracellular [Ca2+] in renal arterioles. Am J Physiol 265, F677-F685.
10. Chen, X.L., Bayliss, D.A., Fern, R.J. & Barrett, P.Q. 1999. A role for T-type Ca2+ channels in the synergistic control of aldosterone production by ANG II and K+. Am J Physiol 276, F674-F683.
11. Chen, C.C., Lamping, K.G., Nuno, D.W., Barresi, R., Prouty, S.J., Lavoie, J.L., Cribbs, L.L., England, S.K., Sigmund, C.D., Weiss, R.M., Williamson, R.A., Hill, J.A. & Campbell, K.P. 2003. Abnormal coronary function in mice deficient in alpha1H T-type Ca2+ channels. Science 302, 1416-1418.
12. Clozel, J.P., Ertel, E.A. & Ertel, S.I. 1997. Discovery and main pharmacological properties of mibefradil (Ro 40-5967), the first selective T-type calcium channel blocker. J Hypertens Suppl 15, S17-S25.
13. Cribbs, L.L., Lee, J.H., Yang, J., Satin, J., Zhang, Y., Daud, A., Barclay, J., Williamson, M.P., Fox, M., Rees, M. & Perez-Reyes, E. 1998. Cloning and characterization of alpha1H from human heart, a member of the T-type Ca2+ channel gene family. Circ Res 83, 103-109.
14. Dilley, J.R., Stier, C.T. Jr & Arendshorst, W.J. 1984. Abnormalities in glomerular function in rats developing spontaneous hypertension. Am J Physiol 246, F12-F20.
15. Diochot, S., Richard, S., Baldy-Moulinier, M., Nargeot, J. & Valmier, J. 1995. Dihydropyridines, phenylalkylamines and benzothiazepines block N-, P/Q- and R-type calcium currents. Pflugers Arch 431, 10-19.
16. Edwards, R.M. 1983. Segmental effects of norepinephrine and angiotensin II on isolated renal microvessels. Am J Physiol 244, F526-F534.
17. Ertel, E.A., Campbell, K.P., Harpold, M.M., Hofmann, F., Mori, Y., Perez-Reyes, E., Schwartz, A., Snutch, T.P., Tanabe, T., Birnbaumer, L., Tsien, R.W. & Catterall, W.A. 2000. Nomenclature of voltage-gated calcium channels. Neuron 25, 533-535.
18. Feng, M.G., Li, M. & 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.
19. Fenoy, F.J., Kauker, M.L., Milicic, I. & Roman, R.J. 1992. Normalization of pressure-natriuresis by nisoldipine in spontaneously hypertensive rats. Hypertension 19, 49-55.
20. Furukawa, T., Yamakawa, T., Midera, T., Sagawa, T., Mori, Y. & Nukada, T. 1999. Selectivities of dihydropyridine derivatives in blocking Ca(2+) channel subtypes expressed in Xenopus oocytes. J Pharmacol Exp Ther 291, 464-473.
21. Furukawa, T., Nukada, T., Miura, R., Ooga, K., Honda, M., Watanabe, S., Koganesawa, S. & Isshiki, T. 2005. Differential blocking action of dihydropyridine Ca2+ antagonists on a T-type Ca2+ channel (alpha1G) expressed in Xenopus oocytes. J Cardiovasc Pharmacol 45, 241-246.
22. Furukawa, T., Nukada, T., Namiki, Y., Miyashita, Y., Hatsuno, K., Ueno, Y., Yamakawa, T. & Isshiki, T. 2009. Five different profiles of dihydropyridines in blocking T-type Ca(2+) channel subtypes (Ca(v)3.1 (alpha(1G)), Ca(v)3.2 (alpha(1H)), and Ca(v)3.3 (alpha(1I))) expressed in Xenopus oocytes. Eur J Pharmacol 613, 100-107.
23. Gordienko, D.V., Clausen, C. & Goligorsky, M.S. 1994. Ionic currents and endothelin signaling in smooth muscle cells from rat renal resistance arteries. Am J Physiol 266, F325-F341.
24. Hansell, P., Nygren, A. & Ueda, J. 1990. Influence of verapamil on regional renal blood flow: a study using multichannel laser-Doppler flowmetry. Acta Physiol Scand 139, 15-20.
25. Hansen, P.B., Jensen, B.L., Andreasen, D., Friis, U.G. & Skott, O. 2000. Vascular smooth muscle cells express the alpha(1A) subunit of a P-/Q-type voltage-dependent Ca(2+)Channel, and It is functionally important in renal afferent arterioles. Circ Res 87, 896-902.
26. Hansen, P.B., Jensen, B.L., Andreasen, D. & Skott, O. 2001. Differential expression of T- and L-type voltage-dependent calcium channels in renal resistance vessels. Circ Res 89, 630-638.
27. Hansen, P.B., Poulsen, C.B., Walter, S., Marcussen, N., Cribbs, L.L., Skott, O. & Jensen, B.L. 2011. Functional importance of L- and P/Q-type voltage-gated calcium channels in human renal vasculature. Hypertension, 58, 464-470.
28. Hart, P.D. & Bakris, G.L. 2010. Hypertensive nephropathy: prevention and treatment recommendations. Expert Opin Pharmacother 11, 2675-2686.
29. Hayashi, K., Nagahama, T., Oka, K., Epstein, M. & Saruta, T. 1996. Disparate effects of calcium antagonists on renal microcirculation. Hypertens Res 19, 31-36.
30. Hayashi, K., Kumagai, H. & Saruta, T. 2003a. Effect of efonidipine and ACE inhibitors on proteinuria in human hypertension with renal impairment. Am J Hypertens 16, 116-122.
31. Hayashi, K., Ozawa, Y., Wakino, S., Kanda, T., Homma, K., Takamatsu, I., Tatematsu, S. & Saruta, T. 2003b. Cellular mechanism for mibefradil-induced vasodilation of renal microcirculation: studies in the isolated perfused hydronephrotic kidney. J Cardiovasc Pharmacol 42, 697-702.
32. Hayashi, K., Wakino, S., Sugano, N., Ozawa, Y., Homma, K. & Saruta, T. 2007. Ca2+ channel subtypes and pharmacology in the kidney. Circ Res 100, 342-353.
33. Helou, C.M. & Marchetti, J. 1997. Morphological heterogeneity of renal glomerular arterioles and distinct [Ca2+]i responses to ANG II. Am J Physiol 273, F84-F96.
34. Hofmann, F., Lacinova, L. & Klugbauer, N. 1999. Voltage-dependent calcium channels: from structure to function. Rev Physiol Biochem Pharmacol 139, 33-87.
35. Honda, M., Hayashi, K., Matsuda, H., Kubota, E., Tokuyama, H., Okubo, K., Takamatsu, I., Ozawa, Y. & Saruta, T. 2001. Divergent renal vasodilator action of L- and T-type calcium antagonists in vivo. J Hypertens 19, 2031-2037.
36. Hu, C., Mori, T., Lu, Y., Guo, Q., Sun, Y., Yoneki, Y., Ohsaki, Y., Nakamichi, T., Oba, I., Sato, E. et al. 2012. Role of specific T-type calcium channel blocker R(-) efonidipine in the regulation of renal medullary circulation. J Hypertens, 30, 1620-1631.
37. Huguenard, J.R. 1996. Low-threshold calcium currents in central nervous system neurons. Annu Rev Physiol 58, 329-348.
38. Inscho, E.W., Imig, J.D. & Cook, A.K. 1997. Afferent and efferent arteriolar vasoconstriction to angiotensin II and norepinephrine involves release of Ca2+ from intracellular stores. Hypertension 29, 222-227.
39. Jensen, L.J., Salomonsson, M., Jensen, B.L. & Holstein-Rathlou, N.H. 2004. Depolarization-induced calcium influx in rat mesenteric small arterioles is mediated exclusively via mibefradil-sensitive calcium channels. Br J Pharmacol 142, 709-718.
40. Karam, H., Clozel, J.P., Bruneval, P., Gonzalez, M.F. & Menard, J. 1999. Contrasting effects of selective T- and L-type calcium channel blockade on glomerular damage in DOCA hypertensive rats. Hypertension 34, 673-678.
41. Kim, D., Song, I., Keum, S., Lee, T., Jeong, M.J., Kim, S.S., McEnery, M.W. & Shin, H.S. 2001. Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca(2+) channels. Neuron 31, 35-45.
42. Klockner, U., Lee, J.H., Cribbs, L.L., Daud, A., Hescheler, J., Pereverzev, A., Perez-Reyes, E. & Schneider, T. 1999. Comparison of the Ca2 + currents induced by expression of three cloned alpha1 subunits, alpha1G, alpha1H and alpha1I, of low-voltage-activated T-type Ca2 + channels. Eur J Neurosci 11, 4171-4178.
43. Klugbauer, N., Marais, E., Lacinova, L. & Hofmann, F. 1999. A T-type calcium channel from mouse brain. Pflugers Arch 437, 710-715.
44. Kuo, I.Y., Ellis, A., Seymour, V.A., Sandow, S.L. & Hill, C.E. 2010. Dihydropyridine-insensitive calcium currents contribute to function of small cerebral arteries. J Cereb Blood Flow Metab 30, 1226-1239.
45. Kuo, I.Y., Wolfle, S.E. & Hill, C.E. 2011. T-type calcium channels and vascular function: the new kid on the block? J Physiol 589, 783-795.
46. Lee, J.H., Gomora, J.C., Cribbs, L.L. & Perez-Reyes, E. 1999. Nickel block of three cloned T-type calcium channels: low concentrations selectively block alpha1H. Biophys J 77, 3034-3042.
47. Loutzenhiser, K. & Loutzenhiser, R. 2000. Angiotensin II-induced Ca(2+) influx in renal afferent and efferent arterioles: differing roles of voltage-gated and store-operated Ca(2+) entry. Circ Res 87, 551-557.
48. Loutzenhiser, R., Hayashi, K. & Epstein, M. 1988. Atrial natriuretic peptide reverses afferent arteriolar vasoconstriction and potentiates efferent arteriolar vasoconstriction in the isolated perfused rat kidney. J Pharmacol Exp Ther 246, 522-528.
49. Loutzenhiser, R., Hayashi, K. & Epstein, M. 1989. Divergent effects of KCl-induced depolarization on afferent and efferent arterioles. Am J Physiol 257, F561-F564.
50. Loutzenhiser, R., Chilton, L. & Trottier, G. 1997. Membrane potential measurements in renal afferent and efferent arterioles: actions of angiotensin II. Am J Physiol 273, F307-F314.
51. Mangoni, M.E., Traboulsie, A., Leoni, A.L., Couette, B., Marger, L., Le Quang, K., Kupfer, E., Cohen-Solal, A., Vilar, J., Shin, H.S., Escande, D., Charpentier, F., Nargeot, J. & Lory, P. 2006. Bradycardia and slowing of the atrioventricular conduction in mice lacking CaV3.1/alpha1G T-type calcium channels. Circ Res 98, 1422-1430.
52. McDonough, S.I. & Bean, B.P. 1998. Mibefradil inhibition of T-type calcium channels in cerebellar purkinje neurons. Mol Pharmacol 54, 1080-1087.
53. Mintz, I.M. 1994. Block of Ca channels in rat central neurons by the spider toxin omega-Aga-IIIA. J Neurosci 14, 2844-2853.
54. Monteil, A., Chemin, J., Bourinet, E., Mennessier, G., Lory, P. & Nargeot, J. 2000. Molecular and functional properties of the human alpha(1G) subunit that forms T-type calcium channels. J Biol Chem 275, 6090-6100.
55. Moosmang, S., Haider, N., Bruderl, B., Welling, A. & Hofmann, F. 2006. Antihypertensive effects of the putative T-type calcium channel antagonist mibefradil are mediated by the L-type calcium channel Cav1.2. Circ Res 98, 105-110.
56. Nathan, S., Pepine, C.J. & Bakris, G.L. 2005. Calcium antagonists: effects on cardio-renal risk in hypertensive patients. Hypertension 46, 637-642.
57. Navar, L.G., Inscho, E.W., Majid, S.A., Imig, J.D., Harrison-Bernard, L.M. & Mitchell, K.D. 1996. Paracrine regulation of the renal microcirculation. Physiol Rev 76, 425-536.
58. Navar, L.G., Inscho, E.W., Imig, J.D. & Mitchell, K.D. 1998. Heterogeneous activation mechanisms in the renal microvasculature. Kidney Int Suppl 67, S17-S21.
59. Ohishi, M., Takagi, T., Ito, N., Terai, M., Tatara, Y., Hayashi, N., Shiota, A., Katsuya, T., Rakugi, H. & Ogihara, T. 2007. Renal-protective effect of T-and L-type calcium channel blockers in hypertensive patients: an Amlodipine-to-Benidipine Changeover (ABC) study. Hypertens Res 30, 797-806.
60. Ohta, M., Sugawara, S., Sato, N., Kuriyama, C., Hoshino, C. & Kikuchi, A. 2009. Effects of benidipine, a long-acting T-type calcium channel blocker, on home blood pressure and renal function in patients with essential hypertension: a retrospective, 'real-world' comparison with amlodipine. Clin Drug Investig 29, 739-746.
61. Okayama, S., Imagawa, K., Naya, N., Iwama, H., Somekawa, S., Kawata, H., Horii, M., Nakajima, T., Uemura, S. & Saito, Y. 2006. Blocking T-type Ca2+ channels with efonidipine decreased plasma aldosterone concentration in healthy volunteers. Hypertens Res 29, 493-497.
62. Ozawa, Y., Hayashi, K., Nagahama, T., Fujiwara, K. & Saruta, T. 2001. Effect of T-type selective calcium antagonist on renal microcirculation: studies in the isolated perfused hydronephrotic kidney. Hypertension 38, 343-347.
63. Perez-Reyes, E. 2003. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83, 117-161.
64. Perez-Reyes, E., Van Deusen, A.L. & Vitko, I. 2009. Molecular pharmacology of human Cav3.2 T-type Ca2+ channels: block by antihypertensives, antiarrhythmics, and their analogs. J Pharmacol Exp Ther 328, 621-627.
65. Poulsen, C.B., Al-Mashhadi, R.H., Cribbs, L.L., Skott, O. & Hansen, P.B. 2011. T-type voltage-gated calcium channels regulate the tone of mouse efferent arterioles. Kidney Int, 79, 443-451.
66. Rossier, M.F., Ertel, E.A., Vallotton, M.B. & Capponi, A.M. 1998. Inhibitory action of mibefradil on calcium signaling and aldosterone synthesis in bovine adrenal glomerulosa cells. J Pharmacol Exp Ther 287, 824-831.
67. Salemme, S., Rebolledo, A., Speroni, F., Petruccelli, S. & Milesi, V. 2007. L, P-/Q- and T-type Ca2+ channels in smooth muscle cells from human umbilical artery. Cell Physiol Biochem 20, 55-64.
68. Sasaki, H., Saiki, A., Endo, K., Ban, N., Yamaguchi, T., Kawana, H., Nagayama, D., Ohhira, M., Oyama, T., Miyashita, Y. & Shirai, K. 2009. Protective effects of efonidipine, a T- and L-type calcium channel blocker, on renal function and arterial stiffness in type 2 diabetic patients with hypertension and nephropathy. J Atheroscler Thromb 16, 568-575.
69. Simms, B.A. & Zamponi, G.W. 2012. Trafficking and stability of voltage-gated calcium channels. Cell Mol Life Sci 69, 843-856.
70. Skogstrand, T., Leh, S., Paliege, A., Reed, R.K., Vikse, B.E., Bachmann, S., Iversen, B.M.L. & Hultstrom, M. 2013. Arterial damage precedes the development of interstitial damage in the nonclipped kidney of two-kidney, one-clip hypertensive rats. J Hypertens, 31, 152-159.
71. Skov, K., Mulvany, M.J. & Korsgaard, N. 1992. Morphology of renal afferent arterioles in spontaneously hypertensive rats. Hypertension 20, 821-827.
72. Turner, R.W., Anderson, D. & Zamponi, G.W. 2011. Signaling complexes of voltage-gated calcium channels. Channels (Austin) 5, 440-448.
73. Wagner, C., Kramer, B.K., Hinder, M., Kieninger, M. & Kurtz, A. 1998. T-type and L-type calcium channel blockers exert opposite effects on renin secretion and renin gene expression in conscious rats. Br J Pharmacol 124, 579-585.
74. Williams, M.E., Washburn, M.S., Hans, M., Urrutia, A., Brust, P.F., Prodanovich, P., Harpold, M.M. & Stauderman, K.A. 1999. Structure and functional characterization of a novel human low-voltage activated calcium channel. J Neurochem 72, 791-799.
75. Wolfe, J.T., Wang, H., Perez-Reyes, E. & Barrett, P.Q. 2002. Stimulation of recombinant Ca(v)3.2, T-type, Ca(2+) channel currents by CaMKIIgamma(C). J Physiol 538, 343-355.
76. Wolfe, J.T., Wang, H., Howard, J., Garrison, J.C. & Barrett, P.Q. 2003. T-type calcium channel regulation by specific G-protein betagamma subunits. Nature 424, 209-213.
77. Wu, S., Haynes, J. Jr, Taylor, J.T., Obiako, B.O., Stubbs, J.R., Li, M. & Stevens, T. 2003. Cav3.1 (alpha1G) T-type Ca2+ channels mediate vaso-occlusion of sickled erythrocytes in lung microcirculation. Circ Res 93, 346-353.
78. Yagil, Y., Miyamoto, M., Frasier, L., Oizumi, K. & Koike, H. 1994. Effects of CS-905, a novel dihydropyridine calcium channel blocker, on arterial pressure, renal excretory function, and inner medullary blood flow in the rat. Am J Hypertens 7, 637-646.
79. Yamamoto, T., Hayashi, K., Matsuda, H., Kubota, E., Tanaka, H., Ogasawara, Y., Nakamoto, H., Suzuki, H., Saruta, T. & Kajiya, F. 2001. In vivo visualization of angiotensin II- and tubuloglomerular feedback-mediated renal vasoconstriction. Kidney Int 60, 364-369.
80. Yokoyama, T., Masuda, Y., Sakai, T., Tanaka, S. & Tomita, K. 1992. Effects of NZ-105, a new calcium antagonist, on renal function in anesthetized spontaneously hypertensive rats. J Cardiovasc Pharmacol 19, 851-856.
81. Zamponi, G.W. & Snutch, T.P. 1998. Modulation of voltage-dependent calcium channels by G proteins. Curr Opin Neurobiol 8, 351-356.
82. Zhang, Z., Rhinehart, K. & Pallone, T.L. 2002. Membrane potential controls calcium entry into descending vasa recta pericytes. Am J Physiol Regul Integr Comp Physiol 283, R949-R957.
83. Zhang, Z., Lin, H., Cao, C., Khurana, S. & Pallone, T.L. 2010. Voltage-gated divalent currents in descending vasa recta pericytes. Am J Physiol Renal Physiol, 299, F862-F871.
84. Zhao, P.L., Wang, X.T., Zhang, X.M., Cebotaru, V., Cebotaru, L., Guo, G., Morales, M. & Guggino, S.E. 2002. Tubular and cellular localization of the cardiac L-type calcium channel in rat kidney. Kidney Int 61, 1393-1406.