Effect of epithelial sodium channel blockade on the myogenic response of rat juxtamedullary afferent arterioles

Hypertension

Volumn 54, Issue 5, 2009, Pages 1062-1069

  Guan, Zhengrong ^a   Pollock, Jennifer S ^a   Cook, Anthony K ^a   Hobbs, Janet L ^a   Inscho, Edward W ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Amiloride; Autoregulatory response; Benzamil; Epithelial sodium channel; Juxtamedullary nephrons; Myogenic response

Indexed keywords

AMILORIDE; BENZAMIL; EPITHELIAL SODIUM CHANNEL; POTASSIUM CHLORIDE; DRUG DERIVATIVE; SODIUM CHANNEL BLOCKING AGENT;

ALPHA CHAIN; ANIMAL CELL; ANIMAL MODEL; ARTERIOLE; ARTERY DIAMETER; ARTICLE; AUTOREGULATION; BETA CHAIN; CONTROLLED STUDY; DRUG EFFECT; FEEDBACK SYSTEM; GAMMA CHAIN; IMMUNOFLUORESCENCE; JUXTAGLOMEDULLARY AFFERENT ARTERIOLE; JUXTAGLOMERULAR CELL; MALE; MEMBRANE DEPOLARIZATION; MUSCLE DEVELOPMENT; NEPHRON; NONHUMAN; PAPILLECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; RAT; SMOOTH MUSCLE FIBER; SURGICAL TECHNIQUE; VASOCONSTRICTION; ANALYSIS OF VARIANCE; ANIMAL; COMPARATIVE STUDY; DISEASE MODEL; JUXTAGLOMERULAR APPARATUS; PHYSIOLOGY; PROBABILITY; RANDOMIZATION; REFERENCE VALUE; SPRAGUE DAWLEY RAT; VASCULAR SMOOTH MUSCLE; VASCULARIZATION; VASODILATATION;

AMILORIDE; ANALYSIS OF VARIANCE; ANIMALS; ARTERIOLES; DISEASE MODELS, ANIMAL; JUXTAGLOMERULAR APPARATUS; MALE; MUSCLE, SMOOTH, VASCULAR; PROBABILITY; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; REFERENCE VALUES; SODIUM CHANNEL BLOCKERS; VASOCONSTRICTION; VASODILATION;

EID: 70449709436     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.109.137992     Document Type: Article

References (62)

1. Palmer BF. Impaired renal autoregulation: implications for the genesis of hypertension and hypertension-induced renal injury. Am J Med Sci. 2001; 321:388-400.
2. Bidani AK, Griffin KA. Pathophysiology of hypertensive renal damage: implications for therapy. Hypertension. 2004;44:595-601.
3. Loutzenhiser R, Griffin K, Williamson G, Bidani A. Renal autoregulation: new perspectives regarding the protective and regulatory roles of the underlying mechanisms. Am J Physiol Regul Integr Comp Physiol. 2006;290:R1153-R1167.
4. Navar LG, Inscho EW, Majid SA, Imig JD, Harrison-Bernard LM, Mitchell KD. Paracrine regulation of the renal microcirculation. Physiol Rev. 1996;76:425-536.
5. Bell PD, Lapointe JY, Peti-Peterdi J. Macula densa cell signaling. Annu Rev Physiol. 2003;65:481-500.
6. Carmines PK, Inscho EW, Gensure RC. Arterial pressure effects on preglomerular microvasculature of juxtamedullary nephrons. Am J Physiol Renal Physiol. 1990;258:F94-F102.
7. Davis MJ, Hill MA. Signaling mechanisms underlying the vascular myogenic response. Physiol Rev. 1999;79:387-423.
8. Hill MA, Davis MJ, Meininger GA, Potocnik SJ, Murphy TV. Arteriolar myogenic signalling mechanisms: implications for local vascular function. Clin Hemorheol Microcirc. 2006;34:67-79.
9. Raina H, Ella SR, Hill MA. Decreased activity of the smooth muscle Na+/Ca2+ exchanger impairs arteriolar myogenic reactivity. J Physiol. 2008;586:1669-1681.
10. Cohen AJ, Fray JC. Calcium ion dependence of myogenic renal plasma flow autoregulation: evidence from the isolated perfused rat kidney. J Physiol. 1982;330:449-460.
11. Harder DR. Pressure-dependent membrane depolarization in cat middle cerebral artery. Circ Res. 1984;55:197-202.
12. Casellas D, Carmines PK, Dupont M, Redon P, Moore LC. Arteriolar renin and vascular effects of angiotensin II in juxtamedullary nephrons. Kidney Int Suppl. 1990;30:S60-S64.
13. Inscho EW, Imig JD, Cook AK. Afferent and efferent arteriolar vasoconstriction to angiotensin II and norepinephrine involves release of Ca2+ from intracellular stores. Hypertension. 1997;29:222-227.
14. Drummond HA, Gebremedhin D, Harder DR. Degenerin/epithelial Na+ channel proteins: components of a vascular mechanosensor. Hypertension. 2004;44:643-648.
15. Jernigan NL, Drummond HA. Vascular ENaC proteins are required for renal myogenic constriction. Am J Physiol Renal Physiol. 2005;289: F891-F901.
16. Balasubramanian L, Ahmed A, Lo CM, Sham JS, Yip KP. Integrin-mediated mechanotransduction in renal vascular smooth muscle cells: activation of calcium sparks. Am J Physiol Regul Integr Comp Physiol. 2007;293:R1586-R1594.
17. Takenaka T, Suzuki H, Okada H, Hayashi K, Kanno Y, Saruta T. Mechanosensitive cation channels mediate afferent arteriolar myogenic constriction in the isolated rat kidney. J Physiol. 1998;511:245-253. (Pubitemid 28421327)
18. Watanabe J, Horiguchi S, Keitoku M, Karibe A, Takeuchi M, Suzuki S, Satoh S, Shirato K. The role of extracellular cations in the development of myogenic contraction in isolated rat small arteries. Jpn Circ J. 1996; 60:239-246.
19. Nelson MT, Conway MA, Knot HJ, Brayden JE. Chloride channel blockers inhibit myogenic tone in rat cerebral arteries. J Physiol. 1997; 502:259-264.
20. Wang X, Takeya K, Aaronson PI, Loutzenhiser K, Loutzenhiser R. Effects of amiloride, benzamil, and alterations in extracellular Na+ on the rat afferent arteriole and its myogenic response. Am J Physiol Renal Physiol. 2008;295:F272-F282.
21. Canessa CM, Schild L, Buell G, Thorens B, Gautschi I, Horisberger JD, Rossier BC. Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature. 1994;367:463-467.
22. Garty H, Palmer LG. Epithelial sodium channels: function, structure, and regulation. Physiol Rev. 1997;77:359-396.
23. Driscoll M, Chalfie M. The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature. 1991;349:588-593.
24. Huang M, Chalfie M. Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. Nature. 1994;367:467-470.
25. Lane JW, McBride DW Jr, Hamill OP. Amiloride block of the mechanosensitive cation channel in Xenopus oocytes. J Physiol. 1991;441: 347-366.
26. Canessa CM, Horisberger JD, Rossier BC. Epithelial sodium channel related to proteins involved in neurodegeneration. Nature. 1993;361: 467-470.
27. Drummond HA, Price MP, Welsh MJ, Abboud FM. A molecular component of the arterial baroreceptor mechanotransducer. Neuron. 1998;21: 1435-1441.
28. Furness DN, Hackney CM, Benos DJ. The binding site on cochlear stereocilia for antisera raised against renal Na+ channels is blocked by amiloride and dihydrostreptomycin. Hear Res. 1996;93:136-146.
29. Welsh MJ, Price MP, Xie J. Biochemical basis of touch perception: mechanosensory function of degenerin/epithelial Na+ channels. J Biol Chem. 2002;277:2369-2372.
30. Du S, Araki I, Mikami Y, Zakoji H, Beppu M, Yoshiyama M, Takeda M. Amiloride-sensitive ion channels in urinary bladder epithelium involved in mechanosensory transduction by modulating stretch-evoked adenosine triphosphate release. Urology. 2007;69:590-595.
31. Drummond HA, Grifoni SC, Jernigan NL. A new trick for an old dogma: ENaC proteins as mechanotransducers in vascular smooth muscle. Physiology (Bethesda). 2008;23:23-31.
32. Jernigan NL, Drummond HA. Myogenic vasoconstriction in mouse renal interlobar arteries: role of endogenous beta and gamma ENaC. Am J Physiol Renal Physiol. 2006;291:F1184-F1191.
33. Henrion D, Laher I, Klaasen A, Bevan JA. Myogenic tone of rabbit facial vein and posterior cerebral artery is influenced by changes in extracellular sodium. Am J Physiol Heart Circ Physiol. 1994;266:H377-H383.
34. Oyabe A, Masumoto N, Ueta K, Nakayama K. Amiloride-sensitive pressure-induced myogenic contraction in rat cerebral artery. Fundam Clin Pharmacol. 2000;14:369-377.
35. Casellas D, Navar LG. In vitro perfusion of juxtamedullary nephrons in rats. Am J Physiol Renal Physiol. 1984;246:F349-F358.
36. Inscho EW, Imig JD, Deichmann PC, Cook AK Candesartan cilexetil protects against loss of autoregulatory efficiency in angiotensin II-infused rats. J Am Soc Nephrol. 1999;10 Suppl 11:S178-S183.
37. Carmines PK, Navar LG. Disparate effects of Ca2+ channel blockade on afferent and efferent arteriolar responses to Ang II. Am J Physiol Renal Physiol. 1989;256:F1015-F1020.
38. Takenaka T, Harrison-Bernard LM, Inscho EW, Carmines PK, Navar LG. Autoregulation of afferent arteriolar blood flow in juxtamedullary nephrons. Am J Physiol Renal Physiol. 1994;267:F879-F887.
39. Walker II, M, Harrison-Bernard LM, Cook AK, Navar LG. Dynamic interaction between myogenic and TGF mechanisms in afferent arteriolar. blood flow autoregulation. Am J Physiol Renal Physiol. 2000;279: F858-F865.
40. Inscho EW, Cook AK, Imig JD, Vial C, Evans RJ. Physiological role for P2X1 receptors in renal microvascular autoregulatory behavior. J Clin Invest. 2003;112:1895-1905.
41. Zhao X, Cook AK, Field M, Edwards B, Zhang S, Zhang Z, Pollock JS, Imig JD, Inscho EW. Impaired Ca2+ signaling attenuates P2X receptor-mediated vasoconstriction of afferent arterioles in angiotensin II hypertension. Hypertension. 2005;46:562-568.
42. Berry DA, Ayers GD. Symmetrized percent changes for treatment comparisons. Am Statistician. 2006;60:27-31.
43. Tang CM, Presser F, Morad M. Amiloride selectively blocks the low threshold (T) calcium channel. Science. 1988;240:213-215.
44. Garcia ML, King VF, Shevell JL, Slaughter RS, Suarez-Kurtz G, Winquist RJ, Kaczorowski GJ. Amiloride analogs inhibit L-type calcium channels and display calcium entry blocker activity. J Biol Chem. 1990; 265:3763-3771.
45. Kleyman TR, Yulo T, Ashbaugh C, Landry D, Cragoe E Jr, Karlin A, Al-Awqati Q. Photoaffinity labeling of the epithelial sodium channel. J Biol Chem. 1986;261:2839-2843.
46. Soltoff SP, Mandel LJ. Amiloride directly inhibits the Na,K-ATPase activity of rabbit kidney proximal tubules. Science. 1983;220:957-958.
47. Teiwes J, Toto RD. Epithelial sodium channel inhibition in cardiovascular disease. A potential role for amiloride. Am J Hypertens. 2007;20: 109-117.
48. Kellenberger S, Schild L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev. 2002;82:735-767.
49. Waldmann R, Bassilana F, de Weille J, Champigny G, Heurteaux C, Lazdunski M. Molecular cloning of a non-inactivating proton-gated Na+ channel specific for sensory neurons. J Biol Chem. 1997;272: 20975-20978.
50. Kleyman TR, Cragoe EJ Jr. The mechanism of action of amiloride. Semin Nephrol. 1988;8:242-248.
51. Kashlan OB, Sheng S, Kleyman TR. On the interaction between amiloride and its putative alpha-subunit epithelial Na+ channel binding site. J Biol Chem. 2005;280:26206-26215.
52. Kleyman TR, Cragoe EJ Jr. Amiloride and its analogs as tools in the study of ion transport. J Membr Biol. 1988;105:1-21.
53. Boron WF, Boulpaep EL. Intracellular pH regulation in the renal proximal tubule of the salamander. Na-H exchange. J Gen Physiol. 1983;81:29-52.
54. Inoue R, Okada T, Onoue H, Hara Y, Shimizu S, Naitoh S, Ito Y, Mori Y. The transient receptor potential protein homologue TRP6 is the essential component of vascular alpha 1-adrenoceptor-activated Ca2+-permeable cation channel. Circ Res. 2001;88:325-332.
55. Dai XQ, Ramji A, Liu Y, Li Q, Karpinski E, Chen XZ. Inhibition of TRPP3 channel by amiloride and analogs. Mol Pharmacol. 2007;72: 1576-1585.
56. Foller M, Kasinathan RS, Koka S, Lang C, Shumilina E, Birnbaumer L, Lang F, Huber SM. TRPC6 contributes to the Ca2+ leak of human erythrocytes. Cell Physiol Biochem. 2008;21:183-192.
57. Welsh DG, Morielli AD, Nelson MT, Brayden JE. Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ Res. 2002;90:248-250.
58. 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.
59. Sharif-Naeini R, Dedman A, Folgering JH, Duprat F, Patel A, Nilius B, Honore E. TRP channels and mechanosensory transduction: insights into the arterial myogenic response. Pflugers Arch. 2008;456:529-540.
60. Folgering JH, Sharif-Naeini R, Dedman A, Patel A, Delmas P, Honore E. Molecular basis of the mammalian pressure-sensitive ion channels: focus on vascular mechanotransduction. Prog Biophys Mol Biol. 2008;72: 180-195.
61. Fellner SK, Arendshorst WJ. Angiotensin II-stimulated Ca2+ entry mechanisms in afferent arterioles: role of transient receptor potential canonical channels and reverse Na+/Ca2+ exchange. Am J Physiol Renal Physiol. 2008;294:F212-F219.
62. Perez FR, Venegas F, Gonzalez M, Andres S, Vallejos C, Riquelme G, Sierralta J, Michea L. Endothelial epithelial sodium channel inhibition activates endothelial nitric oxide synthase via phosphoinositide 3-ki-nase/Akt in small-diameter mesenteric arteries. Hypertension. 2009;53: 1000-1007