A salt-induced reno-cerebral reflex activates renin-angiotensin systems and promotes CKD progression

Journal of the American Society of Nephrology

Volumn 26, Issue 7, 2015, Pages 1619-1633

  Cao, Wei ^a   Li, Aiqing ^a   Wang, Liangliang ^a   Zhou, Zhanmei ^a   Su, Zhengxiu ^a   Bin, Wei ^a   Wilcox, Christopher S ^b   Hou, Fan Fan ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; CLONIDINE; HYDRALAZINE; LOSARTAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SODIUM CHLORIDE; TEMPOL; TYROSINE 3 MONOOXYGENASE;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; DEAFFERENTATION; DISEASE COURSE; ELEVATED BLOOD PRESSURE; FOREBRAIN; KIDNEY DENERVATION; KIDNEY FIBROSIS; KIDNEY TUBULE CELL; MALE; NEPHRITIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SALT INTAKE; SYMPATHETIC NERVE; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROSIS; HYPERTENSION; KIDNEY CIRCULATION; METABOLISM; NEPHRECTOMY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; RANDOMIZATION; REAL TIME POLYMERASE CHAIN REACTION; REFERENCE VALUE; REFLEX; RENAL INSUFFICIENCY, CHRONIC; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; BRAIN; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROSIS; HYDRALAZINE; HYPERTENSION; MALE; NEPHRECTOMY; OXIDATIVE STRESS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; REFERENCE VALUES; REFLEX; RENAL CIRCULATION; RENAL INSUFFICIENCY, CHRONIC; RENIN-ANGIOTENSIN SYSTEM; SODIUM CHLORIDE;

EID: 84934758249     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014050518     Document Type: Article

References (71)

1. ZeisbergM, Neilson EG:Mechanisms of tubulointerstitial fibrosis. J Am Soc Nephrol 21: 1819-1834, 2010
2. Nangaku M: Mechanisms of tubulointerstitial injury in the kidney: Final common pathways to end-stage renal failure. Intern Med 43: 9-17, 2004
3. Wynn TA: Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat Rev Immunol 4: 583-594, 2004
4. Eddy AA, Neilson EG: Chronic kidney disease progression. J Am Soc Nephrol 17: 2964-2966, 2006
5. Speed JS, Pollock DM: Endothelin, kidney disease, and hypertension. Hypertension 61: 1142-1145, 2013
6. Ljutic D, Kes P: The role of arterial hypertension in the progression of non-diabetic glomerular diseases.NephrolDial Transplant 18[Suppl 5]: v28-v30, 2003
7. SchlaichMP, Socratous F,Hennebry S, EikelisN, Lambert EA, Straznicky N, Esler MD, Lambert GW: Sympathetic activation in chronic renal failure. J Am Soc Nephrol 20: 933-939, 2009
8. DiBona GF: Sympathetic nervous system and hypertension. Hypertension 61: 556-560, 2013
9. Lai EY, Luo Z, Onozato ML, Rudolph EH, Solis G, Jose PA, Wellstein A, Aslam S, Quinn MT, Griendling K, Le T, Li P, Palm F, Welch WJ, Wilcox CS: Effects of the antioxidant drug tempol on renal oxygenation in mice with reduced renal mass. Am J Physiol Renal Physiol 303: F64-F74, 2012
10. Cao W, Xu J, Zhou ZM, Wang GB, Hou FF, Nie J: Advanced oxidation protein products activate intrarenal renin-angiotensin system via a CD36-mediated, redox-dependent pathway. Antioxid Redox Signal 18: 19-35, 2013
11. Campese VM, Ye S, Zhong H: Downregulation of neuronal nitric oxide synthase and interleukin-1beta mediates angiotensin II-dependent stimulation of sympathetic nerve activity. Hypertension 39: 519-524, 2002
12. Crowley SD, Coffman TM: Recent advances involving the reninangiotensin system. Exp Cell Res 318: 1049-1056, 2012
13. Kotchen TA, Cowley AW Jr, Frohlich ED: Salt in health and disease-A delicate balance. N Engl J Med 368: 1229-1237, 2013
14. LambersHeerspinkHJ,NavisG,RitzE:Salt intake in kidneydisease-amissed therapeutic opportunity? Nephrol Dial Transplant 27: 3435-3442, 2012
15. Krikken JA, Laverman GD, Navis G: Benefits of dietary sodium restriction in the management of chronic kidney disease. Curr Opin Nephrol Hypertens 18: 531-538, 2009
16. LipkowitzMS,Wilcox CS:What level of dietary salt intake worsens renal outcomes? Am J Hypertens 27: 1243-1244, 2014
17. Weir MR, Fink JC: Salt intake and progression of chronic kidney disease: An overlooked modifiable exposure? A commentary. Am J Kidney Dis 45: 176-188, 2005
18. Johnson RJ, Herrera-Acosta J, Schreiner GF, Rodriguez-Iturbe B: Subtle acquired renal injury as a mechanism of salt-sensitive hypertension. N Engl J Med 346: 913-923, 2002
19. Weir MR, Dengel DR, Behrens MT, Goldberg AP: Salt-induced increases in systolic blood pressure affect renal hemodynamics and proteinuria. Hypertension 25: 1339-1344, 1995
20. Vogt L, Waanders F, Boomsma F, de Zeeuw D, Navis G: Effects of dietary sodiumand hydrochlorothiazide on the antiproteinuric efficacy of losartan. J Am Soc Nephrol 19: 999-1007, 2008
21. Bigazzi R, Bianchi S, Baldari D, Sgherri G, Baldari G, Campese VM: Microalbuminuria in salt-sensitive patients. A marker for renal and cardiovascular risk factors. Hypertension 23: 195-199, 1994
22. Swift PA,Markandu ND, Sagnella GA, He FJ, MacGregor GA: Modest salt reduction reduces blood pressure and urine protein excretion in black hypertensives:Arandomized control trial. Hypertension 46: 308-312, 2005
23. Coffman TM: Under pressure: The search for the essential mechanisms of hypertension. Nat Med 17: 1402-1409, 2011
24. Kolmakova EV, Haller ST, Kennedy DJ, Isachkina AN, Budny GV, Frolova EV, PiechaG,Nikitina ER,Malhotra D, FedorovaOV, Shapiro JI, Bagrov AY: Endogenous cardiotonic steroids in chronic renal failure. Nephrol Dial Transplant 26: 2912-2919, 2011
25. Sanders PW: Vascular consequences of dietary salt intake. Am J Physiol Renal Physiol 297: F237-F243, 2009
26. Kobori H, Nishiyama A, Abe Y, Navar LG: Enhancement of intrarenal angiotensinogen in Dahl salt-sensitive rats on high salt diet. Hypertension 41: 592-597, 2003
27. Konishi Y, Nishiyama A,Morikawa T, Kitabayashi C, ShibataM,Hamada M, KishidaM,HitomiH, Kiyomoto H,Miyashita T,Mori N, Urushihara M, Kobori H, Imanishi M: Relationship between urinary angiotensinogen and salt sensitivity of blood pressure in patients with IgA nephropathy. Hypertension 58: 205-211, 2011
28. Velez JC: The importance of the intrarenal renin-angiotensin system. Nat Clin Pract Nephrol 5: 89-100, 2009
29. Veerasingham SJ, Raizada MK: Brain renin-angiotensin system dysfunction in hypertension: Recent advances and perspectives. Br J Pharmacol 139: 191-202, 2003
30. Hutchinson JS, Mendelsohn FA: Hypotensive effects of captopril administered centrally in intact conscious spontaneously hypertensive rats and peripherally in anephric anaesthetized spontaneously hypertensive rats. Clin Exp Pharmacol Physiol 7: 555-558, 1980
31. Campese VM: A new model of neurogenic hypertension caused by renal injury: Pathophysiology and therapeutic implications. Clin Exp Nephrol 7: 167-171, 2003
32. Ye S, Zhong H, Duong VN, Campese VM: Losartan reduces central and peripheral sympathetic nerve activity in a rat model of neurogenic hypertension. Hypertension 39: 1101-1106, 2002
33. Kobori H, Nangaku M, Navar LG, Nishiyama A: The intrarenal reninangiotensin system: From physiology to the pathobiology of hypertension and kidney disease. Pharmacol Rev 59: 251-287, 2007
34. McKinleyMJ, Albiston AL, AllenAM,MathaiML,May CN,McAllen RM, Oldfield BJ, Mendelsohn FA, Chai SY: The brain renin-angiotensin system: Location and physiological roles. Int J Biochem Cell Biol 35: 901-918, 2003
35. Wilcox CS, Pearlman A: Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev 60: 418-469, 2008
36. Jo H, Yang EK, Lee WJ, Park KY, Kim HJ, Park JS: Gene expression of central and peripheral renin-angiotensin system components upon dietary sodium intake in rats. Regul Pept 67: 115-121, 1996
37. Hettinger U, Lukasova M, Lewicka S, Hilgenfeldt U: Regulatory effects of salt diet on renal renin-angiotensin-aldosterone, and kallikrein-kinin systems. Int Immunopharmacol 2: 1975-1980, 2002
38. Chandramohan G, Bai Y, Norris K, Rodriguez-Iturbe B, Vaziri ND: Effects of dietary salt on intrarenal angiotensin system, NAD(P)H oxidase, COX-2, MCP-1 and PAI-1 expressions and NF-kappaB activity in saltsensitive and-resistant rat kidneys. Am J Nephrol 28: 158-167, 2008
39. Suzuki H, Yamamoto T, Ikegaya N, Hishida A: Dietary salt intake modulates progression of antithymocyte serum nephritis through alteration of glomerular angiotensin II receptor expression. Am J Physiol Renal Physiol 286: F267-F277, 2004
40. Kobori H, Ozawa Y, Suzaki Y, Prieto-Carrasquero MC, Nishiyama A, Shoji T, Cohen EP, Navar LG: Young Scholars Award Lecture: Intratubular angiotensinogen in hypertension and kidney diseases. Am J Hypertens 19: 541-550, 2006
41. Schunkert H, Ingelfinger JR, Jacob H, Jackson B, Bouyounes B, Dzau VJ: Reciprocal feedback regulation of kidney angiotensinogen and renin mRNA expressions by angiotensin II. AmJ Physiol 263: E863-E869, 1992
42. Navar LG, Von Thun AM, Zou L, el-Dahr SS,Mitchell KD: Enhancement of intrarenal angiotensin II levels in 2 kidney 1 clip and angiotensin II induced hypertension. Blood Press Suppl 2: 88-92, 1995
43. Singh R, Singh AK, Leehey DJ: A novel mechanism for angiotensin II formation in streptozotocin-diabetic rat glomeruli. Am J Physiol Renal Physiol 288: F1183-F1190, 2005
44. Onozato ML, Tojo A, Goto A, Fujita T, Wilcox CS: Oxidative stress and nitric oxide synthase in rat diabetic nephropathy: Effects of ACEI and ARB. Kidney Int 61: 186-194, 2002
45. Ito S, Hiratsuka M, Komatsu K, Tsukamoto K, Kanmatsuse K, Sved AF: Ventrolateral medulla AT1 receptors support arterial pressure in Dahl salt-sensitive rats. Hypertension 41: 744-750, 2003
46. Pedrino GR, Calderon AS, Andrade MA, Cravo SL, Toney GM: Discharge of RVLM vasomotor neurons is not increased in anesthetized angiotensin II-salt hypertensive rats. Am J Physiol Heart Circ Physiol 305: H1781-H1789, 2013
47. Lob HE, Schultz D, Marvar PJ, Davisson RL, Harrison DG: Role of the NADPH oxidases in the subfornical organ in angiotensin II-induced hypertension. Hypertension 61: 382-387, 2013
48. Huang BS, Leenen FH: Both brain angiotensin II and "ouabain" contribute to sympathoexcitation and hypertension in Dahl S rats on high salt intake. Hypertension 32: 1028-1033, 1998
49. Fujita M, Ando K, Kawarazaki H, Kawarasaki C, Muraoka K, Ohtsu H, Shimizu H, Fujita T: Sympathoexcitation by brain oxidative stress mediates arterial pressure elevation in salt-induced chronic kidney disease. Hypertension 59: 105-112, 2012
50. Ye S, Zhong H, Yanamadala S, Campese VM:Oxidative stressmediates the stimulation of sympathetic nerve activity in the phenol renal injury model of hypertension. Hypertension 48: 309-315, 2006
51. Xu H, Fink GD, Chen A, Watts S, Galligan JJ: Nitric oxide-independent effects of tempol on sympathetic nerve activity and blood pressure in normotensive rats.AmJ PhysiolHeartCirc Physiol 281:H975-H980, 2001
52. Patel K,Chen Y, Dennehy K, Blau J, Connors S,MendoncaM, Tarpey M, Krishna M, Mitchell JB, Welch WJ, Wilcox CS: Acute antihypertensive action of nitroxides in the spontaneously hypertensive rat.AmJ Physiol Regul Integr Comp Physiol 290: R37-R43, 2006
53. Converse RL Jr, Jacobsen TN, Toto RD, Jost CM, Cosentino F, Fouad-Tarazi F, Victor RG: Sympathetic overactivity in patients with chronic renal failure. N Engl JMed 327: 1912-1918, 1992
54. Klahr S, Levey AS, Beck GJ, Caggiula AW, Hunsicker L, Kusek JW, Striker G; Modification of Diet in Renal Disease Study Group: The effects of dietary protein restriction and blood-pressure control on the progression of chronic renal disease.NEngl J Med330: 877-884, 1994
55. Wright JT Jr, Bakris G, Greene T, Agodoa LY, Appel LJ, Charleston J, Cheek D, Douglas-Baltimore JG, Gassman J, Glassock R, Hebert L, Jamerson K, Lewis J, Phillips RA, Toto RD, Middleton JP, Rostand SG; African American Study of Kidney Disease and Hypertension Study Group: Effect of blood pressure lowering and antihypertensive drug class on progression of hypertensive kidney disease: Results from the AASK trial. JAMA 288: 2421-2431, 2002
56. Chabrashvili T, Kitiyakara C, Blau J, Karber A, Aslam S, Welch WJ, Wilcox CS: Effects of ANG II type 1 and 2 receptors on oxidative stress, renal NADPH oxidase, and SOD expression. Am J Physiol Regul Integr Comp Physiol 285: R117-R124, 2003
57. Kitiyakara C, Chabrashvili T, Chen Y, Blau J, Karber A, Aslam S, Welch WJ, Wilcox CS: Salt intake, oxidative stress, and renal expression of NADPH oxidase and superoxide dismutase. J Am Soc Nephrol 14: 2775-2782, 2003
58. Kopp UC, Cicha MZ, Smith LA: Differential effects of endothelin on activation of renal mechanosensory nerves: Stimulatory in high-sodium diet and inhibitory in low-sodiumdiet. AmJ Physiol Regul Integr Comp Physiol 291: R1545-R1556, 2006
59. Wang TT,Wu XH, Zhang SL, Chan JS:Molecularmechanism(s) of action of norepinephrine on the expression of the angiotensinogen gene in opossum kidney cells. Kidney Int 54: 785-795, 1998
60. Kamiyama M, Urushihara M, Morikawa T, Konishi Y, Imanishi M, Nishiyama A, Kobori H: Oxidative stress/angiotensinogen/reninangiotensin system axis in patients with diabetic nephropathy. Int JMol Sci 14: 23045-23062, 2013
61. Li HY, Hou FF, Zhang X, Chen PY, Liu SX, Feng JX, Liu ZQ, Shan YX, Wang GB, Zhou ZM, Tian JW, Xie D: Advanced oxidation protein products accelerate renal fibrosis in a remnant kidney model. J AmSoc Nephrol 18: 528-538, 2007
62. Fujihara CK, VelhoM,Malheiros DM, Zatz R: An extremely high dose of losartan affords superior renoprotection in the remnant model. Kidney Int 67: 1913-1924, 2005
63. Veelken R, Vogel EM, Hilgers K, Amann K, Hartner A, SassG,Neuhuber W, Tiegs G: Autonomic renal denervation ameliorates experimental glomerulonephritis. J Am Soc Nephrol 19: 1371-1378, 2008
64. Ye S, Ozgur B, Campese VM: Renal afferent impulses, the posterior hypothalamus, and hypertension in rats with chronic renal failure. Kidney Int 51: 722-727, 1997
65. Xavier LL, Viola GG, Ferraz AC, Da Cunha C, Deonizio JM, Netto CA, Achaval M: A simple and fast densitometric method for the analysis of tyrosine hydroxylase immunoreactivity in the substantia nigra pars compacta and in the ventral tegmental area. Brain Res Brain Res Protoc 16: 58-64, 2005
66. Cao W, Zhou QG, Nie J, Wang GB, Liu Y, Zhou ZM, Hou FF: Albumin overload activates intrarenal renin-angiotensin system through protein kinase C and NADPH oxidase-dependent pathway. J Hypertens 29: 1411-1421, 2011
67. Xiao HB, Liu RH, Ling GH, Xiao L, Xia YC, Liu FY, Li J, Liu YH, Chen QK, Lv JL, Zhan M, Yang SK, Kanwar YS, Sun L: HSP47 regulates ECM accumulation in renal proximal tubular cells induced by TGF-b1 through ERK1/2 and JNK MAPK pathways. Am J Physiol Renal Physiol 303: F757-F765, 2012
68. Pupilli C, Chevalier RL, Carey RM, Gomez RA: Distribution and content of renin and renin mRNA in remnant kidney of adult rat. Am J Physiol 263: F731-F738, 1992
69. Friedland J, Silverstein E: A sensitive fluorimetric assay for serum angiotensin-converting enzyme. Am J Clin Pathol 66: 416-424, 1976
70. Fabris B, Candido R, Carraro M, Fior F, Artero M, Zennaro C, CattinMR, Fiorotto A, Bortoletto M, Millevoi C, Bardelli M, Faccini L, Carretta R: Modulation of incipient glomerular lesions in experimental diabetic nephropathy by hypotensive and subhypotensive dosages of an ACE inhibitor. Diabetes 50: 2619-2624, 2001
71. Yao ST, May CN: Intra-carotid angiotensin II activates tyrosine hydroxylase-expressing rostral ventrolateral medulla neurons following blood-brain barrier disruption in rats. Neuroscience 245: 148-156, 2013