βenac is a molecular component of a VSMC mechanotransducer that contributes to renal blood flow regulation, protection from renal injury, and hypertension

Frontiers in Physiology

Volumn 3 AUG, Issue , 2012, Pages

  Drummond, Heather A ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Baroreflex; Degenerin; Epithelial na+ channel; Hypertension; Mechanotransduction; Myogenic constriction; Renal blood flow; Renal injury

Indexed keywords

EID: 84866489434     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00341     Document Type: Review

References (71)

1. Amasheh, S., Barmeyer, C., Koch, C. S., Tavalali, S., Mankertz, J., Epple, H. J., Gehring, M. M., Florian, P., Kroesen, A. J., Zeitz, M., Fromm, M., and Schulzke, J. D. (2004). Cytokine-dependent transcriptional down-regulation of epithelial sodium channel in ulcer-ative colitis. Gastroenterology 126, 1711-1720.
2. Arnadottir, J., and Chalfie, M. (2010). Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39, 111-137.
3. Barmeyer, C., Amasheh, S., Tavalali, S., Mankertz, J., Zeitz, M., Fromm, M., and Schulzke, J. D. (2004). IL-1beta and TNFalpha regulate sodium absorption in rat distal colon. Biochem. Biophys. Res. Commun. 317,500-507.
4. Bayliss, W. M. (1902). On the local reactions of the arterial wall to changes of internal pressure. J. Physiol. 28, 220-231.
5. Benos, D. J., Awayda, M. S., Ismailov, I. I., and Johnson, J. P. (1995). Structure and function of amiloride-sensitive Na+ channels. J. Membr. Biol. 143, 1-18.
6. Benos, D. J., and Stanton, B. A. (1999). Functional domains within the degenerin/epithelial sodium channel (Deg/ENaC) superfamily of ion channels. J. Physiol. 520(Pt 3), 631-644.
7. Beutler, K. T., Masilamani, S., Turban, S., Nielsen, J., Brooks, H. L., Ageloff, S., Fenton, R. A., Packer, R. K., and Knepper, M. A. (2003). Long-term regulation of ENaC expression in kidney by angiotensin II. Hypertension 41, 1143-1150.
8. Bidani, A. K., Hacioglu, R., Abu-Amarah, I., Williamson, G. A., Loutzenhiser, R., and Griffin, K. A. (2003). "Step" vs. "dynamic" autoregulation: implications for susceptibility to hypertensive injury. Am. J. Physiol. Renal Physiol. 285, F113-F120.
9. Bidani, A. K., Picken, M., Hacioglu, R., Williamson, G., and Griffin, K. A. (2007). Spontaneously reduced blood pressure load in the rat streptozotocin-induced diabetes model: potential pathogenetic relevance. Am. J. Physiol. Renal Physiol. 292, F647-F654.
10. Bonny, O., Chraibi, A., Loffing, J., Jaeger, N. F., Grunder, S., Horisberger, J. D., and Rossier, B. C. (1999). Functional expression of a pseudohypoaldosteronism type I mutated epithelial Na+ channel lacking the pore-forming region of its alpha subunit.J. Clin. Invest. 104, 967-974.
11. Braga, V. A., Burmeister, M. A., Sharma, R. V., and Davisson, R. L. (2008). Cardiovascular responses to peripheral chemoreflex activation and comparison of different methods to evaluate baroreflex gain in conscious mice using telemetry. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1168-R1174.
12. Carattino, M. D., Sheng, S., and Kleyman, T. R. (2004). Epithelial Na+ channels are activated by laminar shear stress. J. Biol. Chem. 279,4120-4126.
13. Chung, W S., Farley, J. M., and Drummond, H. A. (2011). ASIC-like currents in freshly isolated cerebral artery smooth muscle cells are inhibited by endogenous oxidase activity. Cell. Physiol. Biochem. 27, 129-138.
14. Cowley, A. W. Jr., Liard, J. F., and Guyton, A. C. (1973). Role of baroreceptor reflex in daily control of arterial blood pressure and other variables in dogs. Circ. Res. 32, 564-576.
15. Cupples, W. A., and Braam, B. (2007). Assessment of renal autoregulation. Am. J. Physiol. Renal Physiol. 292, F1105-F1123.
16. Cupples, W. A., Novak, P., Novak, V., and Salevsky, F. C. (1996). Spontaneous blood pressure fluctuations and renal blood flow dynamics. Am. J. Physiol. 270(1 Pt 2), F82-F89.
17. Davis, M. J., and Hill, M. A. (1999). Signaling mechanisms underlying the vascular myogenic response. Physiol Rev. 79, 387-423.
18. Davis, M. J., Wu, X., Nurkiewicz, T. R., Kawasaki, J., Davis, G. E., Hill, M. A., and Meininger, G. A. (2001). Integrins and mechanotransduction of the vascular myogenic response. Am. J. Physiol Heart Circ. Physiol. 280, H1427-H1433.
19. Drummond, H. A., Abboud, F. M., and Welsh, M. J. (2000). Localization of beta and gamma subunits of ENaC in sensory nerve endings in the rat foot pad. Brain Res. 884, 1-12.
20. Drummond, H. A., Furtado, M. M., Myers, S., Grifoni, S., Parker, K. A., Hoover, A., and Stec, D. E. (2006). ENaC proteins are required for NGF-induced neurite growth. Am. J. Physiol Cell Physiol. 290, C404-C410.
21. Drummond, H. A., Gebremedhin, D., and Harder, D. R. (2004). Degenerin/epithelial Na+ channel proteins: components of a vascular mechanosensor. Hypertension 44, 643-648.
22. Drummond, H. A., Grifoni, S. C., Abu-Zaid, A., Gousset, M., Chiposi, R., Barnard, J. M., Murphey, B., and Stec, D. E. (2011). Renal inflammation and elevated blood pressure in a mouse model of reduced {beta}-ENaC. Am. J. Physiol. Renal Physiol. 301, F443-F449.
23. Drummond, H. A., Welsh, M. J., and Abboud, F. M. (2001). ENaC sub-units are molecular components of the arterial baroreceptor complex. Ann. N.Y.Acad. Sci. 940, 42-47.
24. Ge, Y., Gannon, K. P., Gousset, M., Liu, R., Murphey, B., and Drummond, H. A. (2012). Impaired myogenic constriction of the renal afferent arteriole in a mouse model of reduced βENaC expression. Am. J. Physiol. Renal Physiol. 302, F1486-F1493.
25. Gilmore, E. S., Stutts, M. J., and Milgram, S. L. (2001). SRC family kinases mediate epithelial Na+ channel inhibition by endothelin. J. Biol. Chem. 276,42610-42617.
26. Giraldez, T., Rojas, P., Jou, J., Flores, C., and Alvarez de la Rosa, D. (2012). Invited review- the epithelial sodium channel delta subunit: new notes for an old song. Am. J. Physiol. Renal Physiol. 303, F328-F338.
27. Goodman, M. B., and Schwarz, E. M. (2003). Transducing touch in Caenorhabditis elegans. Annu. Rev. Physiol. 65, 429-452.
28. Griffin, K. A., Hacioglu, R., Abu-Amarah, I., Loutzenhiser, R., Williamson, G. A., and Bidani, A. K. (2004). Effects of calcium channel blockers on "dynamic" and "steady-state step" renal autoregulation. Am. J. Physiol. Renal Physiol. 286, F1136-F1143.
29. Grifoni, S. C., Chiposi, R., McKey, S. E., Ryan, M. J., and Drummond, H. A. (2010). Altered whole kidney blood flow autoregulation in a mouse model of reduced beta-ENaC. Am. J. Physiol. Renal Physiol. 298, F285-F292.
30. Guan, Z., Pollock, J. S., Cook, A. K., Hobbs, J. L., and Inscho, E. W. (2009). Effect of epithelial sodium channel blockade on the myogenic response of rat juxtamedullary afferent arterioles. Hypertension 54, 1062-1069.
31. Helms, M. N., Jain, L., Self, J. L., and Eaton, D. C. (2008). Redox regulation of epithelial sodium channels examined in alveolar type 1 and 2 cells patch-clamped in lung slice tissue. J. Biol. Chem. 283, 22875-22883.
32. Heo, K. S., Fujiwara, K., and Abe, J. (2011). Disturbed-flow-mediated vascular reactive oxygen species induce endothelial dysfunction. Circ. J. 75, 2722-2730.
33. Hill, M. A., Davis, M. J., Meininger, G. A., Potocnik, S. J., and Murphy, T. V. (2006). Arteriolar myogenic signalling mechanisms: implications for local vascular function. Clin. Hemorheol. Microcirc. 34, 67-79.
34. Hill, M. A., Zou, H., Potocnik, S. J., Meininger, G. A., and Davis, M. J. (2001). Invited review: arteriolar smooth muscle mechanotransduction: Ca(2+) signaling pathways underlying myogenic reactivity. J. Appl. Physiol. 91,973-983.
35. Iliescu, R. (2007). Increased blood pressure variability and impaired renal autoregulation in obese Zucker rats. FASEBJ. 21, 892.13.
36. Jernigan, N. L., and Drummond, H. A. (2005). Vascular ENaC proteins are required for renal myogenic constriction. Am. J. Physiol. Renal Physiol. 289, F891-F901.
37. Jernigan, N. L., and Drummond, H. A. (2006). Myogenic vasoconstric-tion in mouse renal interlobar arteries: role of endogenous beta and gammaENaC. Am. J. Physiol. Renal Physiol. 291, F1184-F1191.
38. Jernigan, N. L., LaMarca, B., Speed, J., Galmiche, L., Granger, J. P., and Drummond, H. A. (2008). Dietary salt enhances benzamil-sensitive component of myogenic constriction in mesenteric arteries. Am. J. Physiol. Heart Circ. Physiol. 294, H409-H420.
39. Jernigan, N. L., Speed, J., LaMarca, B., Granger, J. P., and Drummond, H. A. (2009). Angiotensin II regulation of renal vascular ENaC proteins. Am. J. Hypertens. 22, 593-597.
40. Johnson, B. D., Mather, K. J., and Wallace, J. P. (2011). Mechanotransduction of shear in the endothelium: basic studies and clinical implications. Vasc. Med. 16, 365-377.
41. Just, A., and Arendshorst, W J. (2003). Dynamics and contribution of mechanisms mediating renal blood flow autoregulation. Am. J. Physiol. Regul Integr. Comp. Physiol. 285, R619-R631.
42. Just, A., and Arendshorst, W. J. (2007). A novel mechanism of renal blood flow autoregulation and the autoregulatory role of A1 adenosine receptors in mice. Am. J. Physiol. Renal Physiol. 293, F1489-F1500.
43. Kapoor, N., Bartoszewski, R., Qadri, Y. J., Bebok, Z., Bubien, J. K., Fuller, C. M., and Benos, D. J. (2009). Knockdown of ASIC1 and epithelial sodium channel subunits inhibits glioblastoma whole cell current and cell migration. J. Biol. Chem. 284, 24526-24541.
44. Kellenberger, S., and Schild, L. (2002). Epithelial sodium chan-nel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 82, 735-767.
45. Kizer, N., Guo, X. L., and Hruska, K. (1997). Reconstitution of stretch-activated cation channels by expression of the alpha-subunit of the epithelial sodium channel cloned from osteoblasts. Proc. Natl. Acad. Sci. U.S.A. 94, 1013-1018.
46. Lai, C. C., Hong, K., Kinnell, M., Chalfie, M., and Driscoll, M. (1996). Sequence and transmem-brane topology of MEC-4, an ion channel subunit required for mechanotransduction in Caenorhabditis elegans. J. Cell Biol. 133, 1071-1081.
47. Loutzenhiser, R., Bidani, A., and Chilton, L. (2002). Renal myogenic response: kinetic attributes and physiological role. Circ. Res. 90, 1316-1324.
48. Loutzenhiser, R., Griffin, K. A., and Bidani, A. K. (2006). Systolic blood pressure as the trigger for the renal myogenic response: protective or autoregulatory? Curr. Opin. Nephrol. Hypertens. 15, 41-49.
49. Mamet, J., Baron, A., Lazdunski, M., and Voilley, N. (2002). Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J. Neurosci. 22, 10662-10670.
50. Mamet, J., Lazdunski, M., and Voilley, N. (2003). How nerve growth factor drives physiological and inflammatory expressions of acid-sensing ion channel 3 in sensory neurons. J. Biol. Chem. 278, 48907-48913.
51. Mano, I., and Driscoll, M. (1999). DEG/ENaC channels: a touchy superfamily that watches its salt. Bioessays 21, 568-578.
52. Marsh, D. J., Sosnovtseva, O. V., Pavlov, A. N., Yip, K. P., and Holstein-Rathlou, N. H. (2005). Frequency encoding in renal blood flow regulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R1160-R1167.
53. Mauro, T., Guitard, M., Behne, M., Oda, Y., Crumrine, D., Komuves, L., Rassner, U., Elias, P. M., and Hummler, E. (2002). The ENaC channel is required for normal epidermal differentiation. J. Invest. Dermatol. 118,589-594.
54. + channel in mice: hyperkalemia and neonatal death associated with a pseudohypoaldosteronism pheno-type. Proc. Natl. Acad. Sci. U.S.A. 96, 1727-1731.
55. Montell, C. (2005). The TRP super-family of cation channels. Sci. STKE 2005, re3.
56. Navar, L. G. (1978). Renal autoregulation: perspectives from whole kidney and single nephron studies. Am. J. Physiol. 234, F357-F370.
57. Navar, L. G., Marsh, D. J., Blantz, R. C., Hall, J., Ploth, D. W., and Nasjletti, A. (1982). Intrinsic control of renal hemodynamics. Fed. Proc. 41, 3022-3030.
58. Pavlov, T. S., Chahdi, A., Ilatovskaya, D. V., Levchenko, V., Vandewalle, A., Pochynyuk, O., Sorokin, A., and Staruschenko, A. (2010). Endothelin-1 inhibits the epithelial Na+ channel through betaPix/14-3-3/Nedd4-2.J. Am. Soc. Nephrol. 21, 833-843.
59. Pradervand, S., Barker, P. M., Wang, Q., Ernst, S. A., Beermann, F., Grubb, B. R., Burnier, M., Schmidt, A., Bindels, R. J., Gatzy, J. T., Rossier, B. C., and Hummler, E. (1999). Salt restriction induces pseudohypoaldosteronism type 1 in mice expressing low levels of the beta-subunit of the amiloride-sensitive epithelial sodium channel. Proc. Natl. Acad. Sci. U.S.A. 96, 1732-1737.
60. Satlin, L. M., Sheng, S., Woda, C. B., and Kleyman, T. R. (2001). Epithelial Na(+) channels are regulated by flow. Am. J. Physiol. Renal Physiol. 280, F1010-F1018.
61. Shin, H. K., Nishimura, M., Jones, P. B., Ay, H., Boas, D. A., Moskowitz, M. A., and Ayata, C. (2008). Mild induced hypertension improves blood flow and oxygen metabolism in transient focal cerebral ischemia. Stroke 39, 1548-1555.
62. Syntichaki, P., and Tavernarakis, N. (2004). Genetic models of mechan-otransduction: the nematode Caenorhabditis elegans. Physiol Rev. 84,1097-1153.
63. Tavernarakis, N., and Driscoll, M. (1997). Molecular modeling of mechanotransduction in the nematode Caenorhabditis elegans. Annu. Rev. Physiol. 59, 659-689.
64. Tavernarakis, N., and Driscoll, M. (2001). Degenerins. At the core of the metazoan mechanotrans-ducer? Ann. N.Y. Acad. Sci. 940, 28-41.
65. + exchangers in healthy and arthritic chondrocytes. Histol. Histopathol. 14, 1023-1031.
66. USRDS. (2008). Economic costs of ESRD, 2008. Bethesda, MD: National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases.
67. USRDS. (2010). Incidence and prevalence of ESRD, 2010. Bethesda, MD: National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases.
68. VanLandingham, L. G., Gannon, K. P., and Drummond, H. A. (2009). Pressure-induced constriction is inhibited in a mouse model of reduced betaENaC. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R723-R728.
69. Waldmann, R., Champigny, G., Bassilana, F., Voilley, N., and Lazdunski, M. (1995). Molecular cloning and functional expression of a novel amiloride-sensitive Na+ channel. J. Biol. Chem. 270, 27411-27414.
70. Wang, S., Meng, F., Mohan, S., Champaneri, B., and Gu, Y. (2009). Functional ENaC channels expressed in endothelial cells: a new candidate for mediating shear force. Microcirculation 16, 276-287.
71. Wang, X., Takeya, K., Aaronson, P. I., Loutzenhiser, K., and Loutzenhiser, R. (2008). Effects of amiloride, benzamil, and alterations in extracellular Na+ on the rat afferent arteriole and its myogenic response. Am. J. Physiol. Renal Physiol. 295, F272-F282.