Retinal vasculopathy is reduced by dietary salt restriction: Involvement of glia, ENaCα, and the renin-angiotensin-aldosterone system

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 9, 2014, Pages 2033-2041

  Deliyanti, Devy ^a   Armani, Roksana ^a   Casely, David ^b   Figgett, William A ^a   Agrotis, Alex ^a   Wilkinson Berka, Jennifer L ^a  

^a MONASH UNIVERSITY   (Australia)

^b Prosearch International   (Australia)

Author keywords

aldosterone; ion channel

Indexed keywords

ALDOSTERONE; ANGIOGENIC FACTOR; ANGIOTENSIN 1 RECEPTOR; EPITHELIAL SODIUM CHANNEL; ERYTHROPOIETIN; MESSENGER RNA; MINERALOCORTICOID RECEPTOR; RENIN; SODIUM CHLORIDE; TUMOR NECROSIS FACTOR; VASCULOTROPIN;

ALDOSTERONE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; GLIA CELL; GLIOSIS; MICROGLIA; MUELLER CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; RETINA ISCHEMIA; RETINA NEOVASCULARIZATION; SALT INTAKE; SODIUM RESTRICTION;

ALDOSTERONE; ION CHANNEL;

ADAPTOR PROTEIN COMPLEX 1; ALDOSTERONE; ANIMALS; ANIMALS, NEWBORN; AQUAPORIN 4; BODY WEIGHT; CELLS, CULTURED; DIET, SODIUM-RESTRICTED; DISEASE MODELS, ANIMAL; DRINKING BEHAVIOR; EPENDYMOGLIAL CELLS; EPITHELIAL SODIUM CHANNELS; ERYTHROPOIETIN; GLIOSIS; HEMATOCRIT; ION TRANSPORT; ISCHEMIA; KIDNEY GLOMERULUS; MAP KINASE SIGNALING SYSTEM; MICROGLIA; PHOSPHORYLATION; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; RENIN-ANGIOTENSIN SYSTEM; RETINAL GANGLION CELLS; RETINAL NEOVASCULARIZATION; RETINOPATHY OF PREMATURITY; SODIUM; SODIUM CHLORIDE, DIETARY; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84906940552     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.303792     Document Type: Article

References (61)

1. Whelton PK, Appel LJ, Sacco RL, et al. Sodium, blood pressure, and cardiovascular disease: further evidence supporting the American Heart Association sodium reduction recommendations. Circulation. 2012;126:2880-2889.
2. Shay CM, Ning H, Daniels SR, Rooks CR, Gidding SS, Lloyd-Jones DM. Status of cardiovascular health in US adolescents: prevalence estimates from the National Health and Nutrition Examination Surveys (NHANES) 2005-2010. Circulation. 2013;127:1369-1376.
3. Lloyd-Jones D, Adams RJ, Brown TM, et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Executive summary: heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation. 2010;121:948-954.
4. Ricchiuti V, Lapointe N, Pojoga L, Yao T, Tran L, Williams GH, Adler GK. Dietary sodium intake regulates angiotensin II type 1, mineralocorticoid receptor, and associated signaling proteins in heart. J Endocrinol. 2011;211:47-54.
5. Williams GH, Hollenberg NK, Braley LM. Influence of sodium intake on vascular and adrenal angiotensin II receptors. Endocrinology. 1976;98:1343-1350.
6. Bellucci A, Wilkes BM. Mechanism of sodium modulation of glomerular angiotensin receptors in the rat. J Clin Invest. 1984;74:1593-1600.
7. Aguilera G, Catt K. Regulation of vascular angiotensin II receptors in the rat during altered sodium intake. Circ Res. 1981;49:751-758.
8. Wilkinson-Berka JL, Agrotis A, Deliyanti D. The retinal reninangiotensin system: roles of angiotensin II and aldosterone. Peptides. 2012;36:142-150.
9. Chaturvedi N, Porta M, Klein R, Orchard T, Fuller J, Parving HH, Bilous R, Sjølie AK; DIRECT Programme Study Group. Effect of candesartan on prevention (DIRECT-Prevent 1) and progression (DIRECT-Protect 1) of retinopathy in type 1 diabetes: randomised, placebo-controlled trials. Lancet. 2008;372:1394-1402.
10. Zhao M, Célérier I, Bousquet E, Jeanny JC, Jonet L, Savoldelli M, Offret O, Curan A, Farman N, Jaisser F, Behar-Cohen F. Mineralocorticoid receptor is involved in rat and human ocular chorioretinopathy. J Clin Invest. 2012;122:2672-2679.
11. Moravski CJ, Kelly DJ, Cooper ME, Gilbert RE, Bertram JF, Shahinfar S, Skinner SL, Wilkinson-Berka JL. Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension. 2000;36:1099-1104.
12. Wilkinson-Berka JL, Tan G, Jaworski K, Miller AG. Identification of a retinal aldosterone system and the protective effects of mineralocorticoid receptor antagonism on retinal vascular pathology. Circ Res. 2009;104:124-133.
13. Berka JL, Stubbs AJ, Wang DZ, DiNicolantonio R, Alcorn D, Campbell DJ, Skinner SL. Renin-containing Müller cells of the retina display endocrine features. Invest Ophthalmol Vis Sci. 1995;36:1450-1458.
14. Sarlos S, Wilkinson-Berka JL. The renin-angiotensin system and the developing retinal vasculature. Invest Ophthalmol Vis Sci. 2005;46:1069-1077.
15. Sapieha P, Joyal JS, Rivera JC, Kermorvant-Duchemin E, Sennlaub F, Hardy P, Lachapelle P, Chemtob S. Retinopathy of prematurity: understanding ischemic retinal vasculopathies at an extreme of life. J Clin Invest. 2010;120:3022-3032.
16. Gariano RF, Gardner TW. Retinal angiogenesis in development and disease. Nature. 2005;438:960-966.
17. Reichenbach A, Wurm A, Pannicke T, Iandiev I, Wiedemann P, Bringmann A. Müller cells as players in retinal degeneration and edema. Graefes Arch Clin Exp Ophthalmol. 2007;245:627-636.
18. Ritter MR, Banin E, Moreno SK, Aguilar E, Dorrell MI, Friedlander M. Myeloid progenitors differentiate into microglia and promote vascular repair in a model of ischemic retinopathy. J Clin Invest. 2006;116:3266-3276.
19. Sivakumar V, Foulds WS, Luu CD, Ling EA, Kaur C. Retinal ganglion cell death is induced by microglia derived pro-inflammatory cytokines in the hypoxic neonatal retina. J Pathol. 2011;224:245-260.
20. Wang J, Xu X, Elliott MH, Zhu M, Le YZ. Müller cell-derived VEGF is essential for diabetes-induced retinal inflammation and vascular leakage. Diabetes. 2010;59:2297-2305.
21. Vessey KA, Wilkinson-Berka JL, Fletcher EL. Characterization of retinal function and glial cell response in a mouse model of oxygen-induced retinopathy. J Comp Neurol. 2011;519:506-527.
22. Connor KM, SanGiovanni JP, Lofqvist C, et al. Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med. 2007;13:868-873.
23. Deliyanti D, Miller AG, Tan G, Binger KJ, Samson AL, Wilkinson-Berka JL. Neovascularization is attenuated with aldosterone synthase inhibition in rats with retinopathy. Hypertension. 2012;59:607-613.
24. Brockway LM, Zhou ZH, Bubien JK, Jovov B, Benos DJ, Keyser KT. Rabbit retinal neurons and glia express a variety of ENaC/DEG subunits. Am J Physiol Cell Physiol. 2002;283:C126-C134.
25. Adair TH, Montani JP. Angiogenesis. Chapter 4. Regulation: Mechanical Factors: San Rafael, CA: Morgan & Claypool Life Sciences; 2011.
26. Wang S, Meng F, Mohan S, Champaneri B, Gu Y. Functional ENaC channels expressed in endothelial cells: a new candidate for mediating shear force. Microcirculation. 2009;16:276-287.
27. Chen W, Valamanesh F, Mirshahi T, Soria J, Tang R, Agarwal MK, Mirshahi M. Aldosterone signaling modifies capillary formation by human bone marrow endothelial cells. Vascul Pharmacol. 2004;40:269-277.
28. Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LE. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci U S A. 1995;92:905-909.
29. Chen J, Connor KM, Aderman CM, Willett KL, Aspegren OP, Smith LE. Suppression of retinal neovascularization by erythropoietin siRNA in a mouse model of proliferative retinopathy. Invest Ophthalmol Vis Sci. 2009;50:1329-1335.
30. Bullard LE, Qi X, Penn JS. Role for extracellular signal-responsive kinase-1 and -2 in retinal angiogenesis. Invest Ophthalmol Vis Sci. 2003;44:1722-1731.
31. Miura Y, Miura O, Ihle JN, Aoki N. Activation of the mitogen-activated protein kinase pathway by the erythropoietin receptor. J Biol Chem. 1994;269:29962-29969.
32. DeNiro M, Al-Mohanna FH, Al-Mohanna FA. Inhibition of reactive gliosis prevents neovascular growth in the mouse model of oxygen-induced retinopathy. PLoS One. 2011;6:e22244.
33. Tout S, Chan-Ling T, Holländer H, Stone J. The role of Müller cells in the formation of the blood-retinal barrier. Neuroscience. 1993;55:291-301.
34. Kleinewietfeld M, Manzel A, Titze J, Kvakan H, Yosef N, Linker RA, Muller DN, Hafler DA. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature. 2013;496:518-522.
35. Machnik A, Neuhofer W, Jantsch J, et al. Macrophages regulate saltdependent volume and blood pressure by a vascular endothelial growth factor-C-dependent buffering mechanism. Nat Med. 2009;15:545-552.
36. Koleganova N, Piecha G, Ritz E, Becker LE, Müller A, Weckbach M, Nyengaard JR, Schirmacher P, Gross-Weissmann ML. Both high and low maternal salt intake in pregnancy alter kidney development in the offspring. Am J Physiol Renal Physiol. 2011;301:F344-F354.
37. Golestaneh N, De Kozak Y, Klein C, Mirshahi M. Epithelial sodium channel and the mineralocorticoid receptor in cultured rat Müller glial cells. Glia. 2001;33:160-168.
38. Zhao M, Valamanesh F, Celerier I, Savoldelli M, Jonet L, Jeanny JC, Jaisser F, Farman N, Behar-Cohen F. The neuroretina is a novel mineralocorticoid target: aldosterone up-regulates ion and water channels in Müller glial cells. FASEB J. 2010;24:3405-3415.
39. Rugale C, Delbosc S, Cristol JP, Mimran A, Jover B. Sodium restriction prevents cardiac hypertrophy and oxidative stress in angiotensin II hypertension. Am J Physiol Heart Circ Physiol. 2003;284:H1744-H1750.
40. Oudot C, Lajoix AD, Jover B, Rugale C. Dietary sodium restriction prevents kidney damage in high fructose-fed rats. Kidney Int. 2013;83:674-683.
41. Jo CH, Kim S, Park JS, Kim GH. Effects of dietary salt restriction on puromycin aminonucleoside nephrosis: preliminary data. Electrolyte Blood Press. 2011;9:55-62.
42. Dlouha H, Erdösova R, Kraus M, Skopkova J. The effect of sodium intake on maternal milk electrolytes and aldosterone, corticosterone and 18-hydroxydeoxy-corticosterone production in the offspring of rats. Biol Neonate. 1973;22:38-49.
43. Holmes JM, Duffner LA. The effect of postnatal growth retardation on abnormal neovascularization in the oxygen exposed neonatal rat. Curr Eye Res. 1996;15:403-409.
44. Stahl A, Chen J, Sapieha P, Seaward MR, Krah NM, Dennison RJ, Favazza T, Bucher F, Löfqvist C, Ong H, Hellström A, Chemtob S, Akula JD, Smith LE. Postnatal weight gain modifies severity and functional outcome of oxygen-induced proliferative retinopathy. Am J Pathol. 2010;177:2715-2723.
45. Martus W, Kim D, Garvin JL, Beierwaltes WH. Commercial rodent diets contain more sodium than rats need. Am J Physiol Renal Physiol. 2005;288:F428-F431.
46. Lange C, Ehlken C, Stahl A, Martin G, Hansen L, Agostini HT. Kinetics of retinal vaso-obliteration and neovascularisation in the oxygen-induced retinopathy (OIR) mouse model. Graefes Arch Clin Exp Ophthalmol. 2009;247:1205-1211.
47. Davies MH, Eubanks JP, Powers MR. Microglia and macrophages are increased in response to ischemia-induced retinopathy in the mouse retina. Mol Vis. 2006;12:467-477.
48. Tu YF, Lu PJ, Huang CC, Ho CJ, Chou YP. Moderate dietary restriction reduces p53-mediated neurovascular damage and microglia activation after hypoxic ischemia in neonatal brain. Stroke. 2012;43:491-498.
49. Sandberg K, Ji H, Catt KJ. Regulation of angiotensin II receptors in rat brain during dietary sodium changes. Hypertension. 1994;23(1 suppl):I137-I141.
50. Shao W, Seth DM, Prieto MC, Kobori H, Navar LG. Activation of the renin-angiotensin system by a low-salt diet does not augment intratubular angiotensinogen and angiotensin II in rats. Am J Physiol Renal Physiol. 2013;304:F505-F514.
51. Tikellis C, Pickering RJ, Tsorotes D, Huet O, Chin-Dusting J, Cooper ME, Thomas MC. Activation of the Renin-Angiotensin system mediates the effects of dietary salt intake on atherogenesis in the apolipoprotein E knockout mouse. Hypertension. 2012;60:98-105.
52. Martinerie L, Pussard E, Foix-L'Hélias L, Petit F, Cosson C, Boileau P, Lombès M. Physiological partial aldosterone resistance in human newborns. Pediatr Res. 2009;66:323-328.
53. Soundararajan R, Pearce D, Ziera T. The role of the ENaC-regulatory complex in aldosterone-mediated sodium transport. Mol Cell Endocrinol. 2012;350:242-247.
54. Brockway LM, Benos DJ, Keyser KT, Kraft TW. Blockade of amiloridesensitive sodium channels alters multiple components of the mammalian electroretinogram. Vis Neurosci. 2005;22:143-151.
55. Newman EA. Inward-rectifying potassium channels in retinal glial (Müller) cells. J Neurosci. 1993;13:3333-3345.
56. Ishii M, Horio Y, Tada Y, Hibino H, Inanobe A, Ito M, Yamada M, Gotow T, Uchiyama Y, Kurachi Y. Expression and clustered distribution of an inwardly rectifying potassium channel, KAB-2/Kir4.1, on mammalian retinal Müller cell membrane: their regulation by insulin and laminin signals. J Neurosci. 1997;17:7725-7735.
57. Goodyear MJ, Crewther SG, Junghans BM. A role for aquaporin-4 in fluid regulation in the inner retina. Vis Neurosci. 2009;26:159-165.
58. Nagelhus EA, Horio Y, Inanobe A, Fujita A, Haug FM, Nielsen S, Kurachi Y, Ottersen OP. Immunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Müller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains. Glia. 1999;26:47-54.
59. Pannicke T, Iandiev I, Uckermann O, Biedermann B, Kutzera F, Wiedemann P, Wolburg H, Reichenbach A, Bringmann A. A potassium channel-linked mechanism of glial cell swelling in the postischemic retina. Mol Cell Neurosci. 2004;26:493-502.
60. Bringmann A, Uckermann O, Pannicke T, Iandiev I, Reichenbach A, Wiedemann P. Neuronal versus glial cell swelling in the ischaemic retina. Acta Ophthalmol Scand. 2005;83:528-538.
61. Roy MS, Janal MN. High caloric and sodium intakes as risk factors for progression of retinopathy in type 1 diabetes mellitus. Arch Ophthalmol. 2010;128:33-39.