Cross Talk Between Plasma Membrane Na(+)/Ca (2+) Exchanger-1 and TRPC/Orai-containing Channels: Key Players in Arterial Hypertension

Overview

Journal Adv Exp Med Biol

Specialties Biology
General Medicine

Date 2012 Dec 11

PMID 23224895

Citations 16

Authors

Maria V Pulina

A Zulian

Sergey G Baryshnikov

Cristina I Linde

Eiji Karashima

John M Hamlyn

Patrizia Ferrari

Mordecai P Blaustein

Vera A Golovina

Affiliations

Soon will be listed here.

Abstract

Arterial smooth muscle (ASM) Na(+)/Ca(2+) exchanger type 1 (NCX1) and TRPC/Orai-containing receptor/store-operated cation channels (ROC/SOC) are clustered with α2 Na(+) pumps in plasma membrane microdomains adjacent to the underlying junctional sarcoplasmic reticulum. This arrangement enables these transport proteins to function as integrated units to help regulate local Na(+) metabolism, Ca(2+) signaling, and arterial tone. They thus influence vascular resistance and blood pressure (BP). For instance, upregulation of NCX1 and TRPC6 has been implicated in the pathogenesis of high BP in several models of essential hypertension. The models include ouabain-induced hypertensive rats, Milan hypertensive rats, and Dahl salt-sensitive hypertensive rats, all of which exhibit elevated plasma ouabain levels. We suggest that these molecular mechanisms are key contributors to the increased vascular resistance ("whole body autoregulation") that elevates BP in essential hypertension. Enhanced expression and function of ASM NCX1 and TRPC/Orai1-containing channels in hypertension implies that these proteins are potential targets for pharmacological intervention.

Citing Articles

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References

Poburko D, Liao C, Lemos V, Lin E, Maruyama Y, Cole W . Transient receptor potential channel 6-mediated, localized cytosolic [Na+] transients drive Na+/Ca2+ exchanger-mediated Ca2+ entry in purinergically stimulated aorta smooth muscle cells. Circ Res. 2007; 101(10):1030-8. DOI: 10.1161/CIRCRESAHA.107.155531. View

Welsh D, Morielli A, Nelson M, Brayden J . Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ Res. 2002; 90(3):248-50. DOI: 10.1161/hh0302.105662. View

Krep H, Price D, Soszynski P, Tao Q, Graves S, Hollenberg N . Volume sensitive hypertension and the digoxin-like factor. Reversal by a Fab directed against digoxin in DOCA-salt hypertensive rats. Am J Hypertens. 1995; 8(9):921-7. DOI: 10.1016/0895-7061(95)00181-N. View

OBrien W, Lingrel J, Wallick E . Ouabain binding kinetics of the rat alpha two and alpha three isoforms of the sodium-potassium adenosine triphosphate. Arch Biochem Biophys. 1994; 310(1):32-9. DOI: 10.1006/abbi.1994.1136. View

Lee M, Song H, Nakai J, Ohkura M, Kotlikoff M, Kinsey S . Local subplasma membrane Ca2+ signals detected by a tethered Ca2+ sensor. Proc Natl Acad Sci U S A. 2006; 103(35):13232-7. PMC: 1559782. DOI: 10.1073/pnas.0605757103. View

Manunta P, Rogowski A, Hamilton B, Hamlyn J . Ouabain-induced hypertension in the rat: relationships among plasma and tissue ouabain and blood pressure. J Hypertens. 1994; 12(5):549-60. View

Zhang S, Yu Y, Roos J, Kozak J, Deerinck T, Ellisman M . STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature. 2005; 437(7060):902-5. PMC: 1618826. DOI: 10.1038/nature04147. View

Ferrandi M, Tripodi G, Salardi S, Florio M, Modica R, Barassi P . Renal Na,K-ATPase in genetic hypertension. Hypertension. 1996; 28(6):1018-25. DOI: 10.1161/01.hyp.28.6.1018. View

Giachini F, Chiao C, Carneiro F, Lima V, Carneiro Z, Dorrance A . Increased activation of stromal interaction molecule-1/Orai-1 in aorta from hypertensive rats: a novel insight into vascular dysfunction. Hypertension. 2008; 53(2):409-16. PMC: 2753260. DOI: 10.1161/HYPERTENSIONAHA.108.124404. View

10.

Blaustein M, Lederer W . Sodium/calcium exchange: its physiological implications. Physiol Rev. 1999; 79(3):763-854. DOI: 10.1152/physrev.1999.79.3.763. View

11.

Juhaszova M, Blaustein M . Na+ pump low and high ouabain affinity alpha subunit isoforms are differently distributed in cells. Proc Natl Acad Sci U S A. 1997; 94(5):1800-5. PMC: 19997. DOI: 10.1073/pnas.94.5.1800. View

12.

Yu Y, Keller S, Remillard C, Safrina O, Nicholson A, Zhang S . A functional single-nucleotide polymorphism in the TRPC6 gene promoter associated with idiopathic pulmonary arterial hypertension. Circulation. 2009; 119(17):2313-22. PMC: 2749566. DOI: 10.1161/CIRCULATIONAHA.108.782458. View

13.

Brayden J, Earley S, Nelson M, Reading S . Transient receptor potential (TRP) channels, vascular tone and autoregulation of cerebral blood flow. Clin Exp Pharmacol Physiol. 2008; 35(9):1116-20. PMC: 4193799. DOI: 10.1111/j.1440-1681.2007.04855.x. View

14.

Zulian A, Baryshnikov S, Linde C, Hamlyn J, Ferrari P, Golovina V . Upregulation of Na+/Ca2+ exchanger and TRPC6 contributes to abnormal Ca2+ homeostasis in arterial smooth muscle cells from Milan hypertensive rats. Am J Physiol Heart Circ Physiol. 2010; 299(3):H624-33. PMC: 2944478. DOI: 10.1152/ajpheart.00356.2010. View

15.

van Breemen C, Chen Q, Laher I . Superficial buffer barrier function of smooth muscle sarcoplasmic reticulum. Trends Pharmacol Sci. 1995; 16(3):98-105. DOI: 10.1016/s0165-6147(00)88990-7. View

16.

Beech D, Muraki K, Flemming R . Non-selective cationic channels of smooth muscle and the mammalian homologues of Drosophila TRP. J Physiol. 2004; 559(Pt 3):685-706. PMC: 1665181. DOI: 10.1113/jphysiol.2004.068734. View

17.

Blaustein M, Zhang J, Chen L, Song H, Raina H, Kinsey S . The pump, the exchanger, and endogenous ouabain: signaling mechanisms that link salt retention to hypertension. Hypertension. 2008; 53(2):291-8. PMC: 2727927. DOI: 10.1161/HYPERTENSIONAHA.108.119974. View

18.

Yeromin A, Zhang S, Jiang W, Yu Y, Safrina O, Cahalan M . Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature. 2006; 443(7108):226-9. PMC: 2756048. DOI: 10.1038/nature05108. View

19.

Liu D, Yang D, He H, Chen X, Cao T, Feng X . Increased transient receptor potential canonical type 3 channels in vasculature from hypertensive rats. Hypertension. 2008; 53(1):70-6. DOI: 10.1161/HYPERTENSIONAHA.108.116947. View

20.

Cowley Jr A . Long-term control of arterial blood pressure. Physiol Rev. 1992; 72(1):231-300. DOI: 10.1152/physrev.1992.72.1.231. View