Mineralocorticoid-induced sodium appetite and renal salt retention: Evidence for common signaling and effector mechanisms

Nephron - Physiology

Volumn 128, Issue 1-2, 2014, Pages 8-16

  Fu, Yiling ^a,b   Vallon, Volker ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Aldosterone; Angiotensin II; Brain; ENaC; Hypertension; Kidney; Mineralocorticoid receptor; NEDD4 2; Salt appetite; Salt intake; SGK1; Sodium reabsorption; Tongue

Indexed keywords

ALDOSTERONE; ANGIOTENSIN 2 RECEPTOR ANTAGONIST; ANGIOTENSIN II; BENZAMIL; CAPTOPRIL; EPITHELIAL SODIUM CHANNEL; EPITHELIAL SODIUM CHANNEL BLOCKING AGENT; MINERALOCORTICOID ANTAGONIST; MINERALOCORTICOID RECEPTOR; OXPRENOATE POTASSIUM; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; SPIRONOLACTONE; UBIQUITIN PROTEIN LIGASE NEDD4; MINERALOCORTICOID; SODIUM CHLORIDE;

BRAIN; GUSTATORY SYSTEM; HUMAN; HYPERNATREMIA; HYPERTENSION; KIDNEY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SALT INTAKE; SIGNAL TRANSDUCTION; SODIUM ABSORPTION; SODIUM APPETITE; SODIUM DEPLETION; SODIUM EXCRETION; SODIUM INTAKE; SODIUM RETENTION; TONGUE; ANIMAL; APPETITE; BLOOD PRESSURE; ELECTROLYTE BALANCE; METABOLISM; PHYSIOLOGY;

ALDOSTERONE; ANGIOTENSIN II; ANIMALS; APPETITE; BLOOD PRESSURE; EPITHELIAL SODIUM CHANNELS; HUMANS; HYPERTENSION; KIDNEY; MINERALOCORTICOID RECEPTOR ANTAGONISTS; MINERALOCORTICOIDS; RECEPTORS, MINERALOCORTICOID; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; WATER-ELECTROLYTE BALANCE;

EID: 84928325521     PISSN: None     EISSN: 16602137     Source Type: Journal    
DOI: 10.1159/000368264     Document Type: Review

References (101)

1. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, Moy CS, Mozaffarian D, Mussolino ME, Nichol G, Paynter NP, Soliman EZ, Sorlie PD, Sotoodehnia N, Turan TN, Virani SS, Wong ND, Woo D, Turner MB: Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 2012; 125:e2-e220.
2. Anderson CA, Ix JH: Sodium reduction in CKD: suggestively hazardous or intuitively advantageous? J Am Soc Nephrol 2013; 24: 1931-1933.
3. Vallon V, Thomson SC: Anomalous role for dietary salt in diabetes mellitus? Nat Rev Endocrinol 2011; 7: 377-378.
4. Geerling JC, Loewy AD: Central regulation of sodium appetite. Exp Physiol 2008; 93: 177-209.
5. Krause EG, Sakai RR: Richter and sodium appetite: from adrenalectomy to molecular biology. Appetite 2007; 49: 353-367.
6. Korhonen MH, Litmanen H, Rauramaa R, Vaisanen SB, Niskanen L, Uusitupa M: Adherence to the salt restriction diet among people with mildly elevated blood pressure. Eur J Clin Nutr 1999; 53: 880-885.
7. Ohta Y, Tsuchihashi T, Ueno M, Kajioka T, Onaka U, Tominaga M, Eto K: Relationship between the awareness of salt restriction and the actual salt intake in hypertensive patients. Hypertens Res 2004; 27: 243-246.
8. Langford HG, Watson RL, Thomas JG: Salt intake and the treatment of hypertension. Am Heart J 1977; 93: 531-532.
9. DiNicolantonio R, Hutchinson JS, Mendelsohn FA: Exaggerated salt appetite of spontaneously hypertensive rats is decreased by central angiotensin-converting enzyme blockade. Nature 1982; 298: 846-848.
10. Hurley RS, Hebert LA, Rypien AB: A comparison of taste acuity for salt in renal patients vs. normal subjects. J Am Diet Assoc 1987; 87: 1531-1534.
11. Leshem M, Rudoy J: Hemodialysis increases the preference for salt in soup. Physiol Behav 1997; 61: 65-69.
12. Francis J, Weiss RM, Wei SG, Johnson AK, Beltz TG, Zimmerman K, Felder RB: Central mineralocorticoid receptor blockade improves volume regulation and reduces sympathetic drive in heart failure. Am J Physiol Heart Circ Physiol 2001; 281:H2241-H2251.
13. Denton DA, Blair-West JR, McBurnie M, Osborne PG, Tarjan E, Williams RM, Weisinger RS: Angiotensin and salt appetite of BALB/c mice. Am J Physiol 1990; 259:R729-R735.
14. Richter CP: Increased salt appetite in adrenalectomized rats. Am J Physiol 1936; 115: 155-161.
15. Takamata A, Mack GW, Gillen CM, Nadel ER: Sodium appetite, thirst, and body fluid regulation in humans during rehydration without sodium replacement. Am J Physiol 1994; 266:R1493-R1502.
16. Cruz DN, Simon DB, Nelson-Williams C, Farhi A, Finberg K, Burleson L, Gill JR, Lifton RP: Mutations in the NaCl cotransporter reduce blood pressure in humans. Hypertension 2001; 37: 1458-1464.
17. Kochli A, Tenenbaum-Rakover Y, Leshem M: Increased salt appetite in patients with congenital adrenal hyperplasia 21-hydroxylase deficiency. Am J Physiol Regul Integr Comp Physiol 2005; 288:R1673-R1681.
18. Wilkins L, Richter CP: A great craving for salt by a child with cortico-adrenal insufficiency. JAMA 1940; 114: 866-868.
19. Conover KL, Woodside B, Shizgal P: Effects of sodium depletion on competition and summation between rewarding effects of salt and lateral hypothalamic stimulation in the rat. Behav Neurosci 1994; 108: 549-558.
20. Richter CP, Eckert JF: Mineral metabolism of adrenalectomized rats studied by the appetite method. Endocrinology 1938; 22: 214-224.
21. Nachman M: Taste preferences for sodium salts by adrenalectomized rats. J Comp Physiol Psychol 1962; 55: 1124-1129.
22. Doi Y, Nose H, Morimoto T: Changes in Na concentration in cerebrospinal fluid during acute hypernatremia and their effect on drinking in juvenile rats. Physiol Behav 1992; 52: 499-504.
23. Andersson B: Regulation of water intake. Physiol Rev 1978; 58: 582.
24. Weisinger RS, Considine P, Denton DA, McKinley MJ: Rapid effect of change in cerebrospinal fluid sodium concentration on salt appetite. Nature 1979; 280: 490-491.
25. Weisinger RS, Considine P, Denton DA, Leksell L, McKinley MJ, Mouw DR, Muller AF, Tarjan E: Role of sodium concentration of the cerebrospinal fluid in the salt appetite of sheep. Am J Physiol 1982; 242:R51-R63.
26. Chiaraviglio E, Perez Guaita MF: The effect of intracerebroventricular hypertonic infusion on sodium appetite in rats after peritoneal dialysis. Physiol Behav 1986; 37: 695-699.
27. Noda M: The subfornical organ, a specialized sodium channel, and the sensing of sodium levels in the brain. Neuroscientist 2006; 12: 80-91.
28. Watanabe E, Fujikawa A, Matsunaga H, Yasoshima Y, Sako N, Yamamoto T, Saegusa C, Noda M: Nav2/NaG channel is involved in control of salt-intake behavior in the CNS. J Neurosci 2000; 20: 7743-7751.
29. Watanabe E, Hiyama TY, Shimizu H, Kodama R, Hayashi N, Miyata S, Yanagawa Y, Obata K, Noda M: Sodium-level-sensitive sodium channel Na(x) is expressed in glial laminate processes in the sensory circumventricular organs. Am J Physiol Regul Integr Comp Physiol 2006; 290:R568-R576.
30. Hiyama TY, Watanabe E, Ono K, Inenaga K, Tamkun MM, Yoshida S, Noda M: Na(x) channel involved in CNS sodium-level sensing. Nat Neurosci 2002; 5: 511-512.
31. Hiyama TY, Watanabe E, Okado H, Noda M: The subfornical organ is the primary locus of sodium-level sensing by Na(x) sodium channels for the control of salt-intake behavior. J Neurosci 2004; 24: 9276-9281.
32. Grob M, Drolet G, Mouginot D: Specific Na + sensors are functionally expressed in a neuronal population of the median preoptic nucleus of the rat. J Neurosci 2004; 24: 3974-3984.
33. Weisinger RS, Denton DA, McKinley MJ, Muller AF, Tarjan E: Cerebrospinal fluid sodium concentration and salt appetite. Brain Res 1985; 326: 95-105.
34. Denton DA, McKinley MJ, Weisinger RS: Hypothalamic integration of body fluid regulation. Proc Natl Acad Sci USA 1996; 93: 7397-7404.
35. Denton DA, McKinley MJ, Nelson JF, Osborne P, Simpson J, Tarjan E, Weisinger RS: Species differences in the effect of decreased CSF sodium concentration on salt appetite. J Physiol (Paris) 1984; 79: 499-504.
36. Frankmann SP, Sakai RR, Simpson JB: Sodium appetite and cerebrospinal fluid sodium concentration during hypovolemia. Appetite 1987; 9: 57-64.
37. Osborne PG, Blair-West JR, Denton DA, Mc-Burnie M, Tarjan E, Williams RM, Weisinger RS: Decreased cerebral sodium concentration and sodium appetite in BALB/c mice. Am J Physiol 1990; 259:R741-R744.
38. Wolf G: Effect of deoxycorticosterone on sodium appetite of intact and adrenalectomized rats. Am J Physiol 1965; 208: 1281-1285.
39. Fregly MJ, Waters IW: Effect of spironolactone on spontaneous NaCl intake of adrenalectomized rats. Proc Soc Exp Biol Med 1966; 123: 971-975.
40. Okubo S, Niimura F, Nishimura H, Takemoto F, Fogo A, Matsusaka T, Ichikawa I: Angiotensin-independent mechanism for aldosterone synthesis during chronic extracellular fluid volume depletion. J Clin Invest 1997; 99: 855-860.
41. Makhanova N, Sequeira-Lopez ML, Gomez RA, Kim HS, Smithies O: Disturbed homeostasis in sodium-restricted mice heterozygous and homozygous for aldosterone synthase gene disruption. Hypertension 2006; 48: 1151-1159.
42. Bojensen E: Concentration of aldosterone and corticosterone in peripheral plasma of rats the effects of salt depletion, salt repletion, potassium loading and intravenous injection of renin and angiotensin II. Eur J Steroids 1966; 1: 145-169.
43. Thomas CP, Itani OA: New insights into epithelial sodium channel function in the kidney: site of action, regulation by ubiquitin ligases, serum-and glucocorticoid-inducible kinase and proteolysis. Curr Opin Nephrol Hypertens 2004; 13: 541-548.
44. Vandewalle A, Farman N, Bencsath P, Bonvalet JP: Aldosterone binding along the rabbit nephron: an autoradiographic study on isolated tubules. Am J Physiol 1981; 240:F172-F179.
45. Lombes M, Farman N, Oblin ME, Baulieu EE, Bonvalet JP, Erlanger BF, Gasc JM: Immunohistochemical localization of renal mineralocorticoid receptor by using an anti-idiotypic antibody that is an internal image of aldosterone. Proc Natl Acad Sci USA 1990; 87: 1086-1088.
46. Soundararajan R, Lu M, Pearce D: Organization of the ENaC-regulatory machinery. Crit Rev Biochem Mol Biol 2012; 47: 349-359.
47. Lang F, Bohmer C, Palmada M, Seebohm G, Strutz-Seebohm N, Vallon V: (Patho)physiological significance of the serum-and glucocorticoid-inducible kinase isoforms. Physiol Rev 2006; 86: 1151-1178.
48. Zhang W, Xia X, Reisenauer MR, Rieg T, Lang F, Kuhl D, Vallon V, Kone BC: Aldosteroneinduced Sgk1 relieves Dot1a-Af9-mediated transcriptional repression of epithelial Na + channel ?. J Clin Invest 2007; 117: 773-783.
49. Rotin D, Staub O: Role of the ubiquitin system in regulating ion transport. Pflugers Arch 2011; 461: 1-21.
50. Arroyo JP, Lagnaz D, Ronzaud C, Vazquez N, Ko BS, Moddes L, Ruffieux-Daidie D, Hausel P, Koesters R, Yang B, Stokes JB, Hoover RS, Gamba G, Staub O: Nedd4-2 modulates renal Na +-Cl-cotransporter via the aldosterone-SGK1-Nedd4-2 pathway. J Am Soc Nephrol 2011; 22: 1707-1719.
51. Wall SM, Weinstein AM: Cortical distal nephron Cl-transport in volume homeostasis and blood pressure regulation. Am J Physiol Renal Physiol 2013; 305:F427-F438.
52. Vallon V, Schroth J, Lang F, Kuhl D, Uchida S: Expression and phosphorylation of the Na +-Cl-cotransporter NCC in vivo is regulated by dietary salt, potassium, and SGK1. Am J Physiol Renal Physiol 2009; 297:F704-F712.
53. McEwen BS, Lambdin LT, Rainbow TC, De Nicola AF: Aldosterone effects on salt appetite in adrenalectomized rats. Neuroendocrinology 1986; 43: 38-43.
54. Tordoff MG, Hughes RL, Pilchak DM: Different effects of three aldosterone treatments on plasma aldosterone and salt intake. Physiol Behav 1993; 54: 129-134.
55. Fregly MJ, Waters IW: Effect of mineralocorticoids on spontaneous sodium chloride appetite of adrenalectomized rats. Physiol Behav 1966; 1: 65-74.
56. Geerling JC, Loewy AD: Aldosterone-sensitive NTS neurons are inhibited by saline ingestion during chronic mineralocorticoid treatment. Brain Res 2006; 1115: 54-64.
57. Weisinger RS, Woods SC: Aldosterone-elicited sodium appetite. Endocrinology 1971; 89: 538-544.
58. Blair-West JR, Denton DA, McBurnie M, Tarjan E, Weisinger RS: Influence of adrenal steroid hormones on sodium appetite of BALB/c mice. Appetite 1995; 24: 11-24.
59. Vallon V, Huang DY, Grahammer F, Wyatt AW, Osswald H, Wulff P, Kuhl D, Lang F: SGK1 as a determinant of kidney function and salt intake in response to mineralocorticoid excess. Am J Physiol Regul Integr Comp Physiol 2005; 289:R395-R401.
60. Shade RE, Blair-West JR, Carey KD, Madden LJ, Weisinger RS, Denton DA: Synergy between angiotensin and aldosterone in evoking sodium appetite in baboons. Am J Physiol Regul Integr Comp Physiol 2002; 283:R1070-R1078.
61. Leshem M, Abutbul A, Eilon R: Exercise increases the preference for salt in humans. Appetite 1999; 32: 251-260.
62. Pimenta E, Gordon RD, Stowasser M: Salt, aldosterone and hypertension. J Hum Hypertens 2013; 27: 1-6.
63. Weisinger RS, Denton DA, McKinley MJ: Self-administered intravenous infusion of hypertonic solutions and sodium appetite of sheep. Behav Neurosci 1983; 97: 433-444.
64. Blackburn RE, Samson WK, Fulton RJ, Stricker EM, Verbalis JG: Central oxytocin and ANP receptors mediate osmotic inhibition of salt appetite in rats. Am J Physiol 1995; 269: R245-R251.
65. Ahima R, Krozowski Z, Harlan R: Type I corticosteroid receptor-like immunoreactivity in the rat CNS: distribution and regulation by corticosteroids. J Comp Neurol 1991; 313: 522-538.
66. Gomez-Sanchez CE, de Rodriguez AF, Romero DG, Estess J, Warden MP, Gomez-Sanchez MT, Gomez-Sanchez EP: Development of a panel of monoclonal antibodies against the mineralocorticoid receptor. Endocrinology 2006; 147: 1343-1348.
67. Amin MS, Wang HW, Reza E, Whitman SC, Tuana BS, Leenen FH: Distribution of epithelial sodium channels and mineralocorticoid receptors in cardiovascular regulatory centers in rat brain. Am J Physiol Regul Integr Comp Physiol 2005; 289:R1787-R1797.
68. Formenti S, Bassi M, Nakamura NB, Schoorlemmer GH, Menani JV, Colombari E: Hindbrain mineralocorticoid mechanisms on sodium appetite. Am J Physiol Regul Integr Comp Physiol 2013; 304:R252-R259.
69. Sullivan MJ, Hasser EM, Moffitt JA, Bruno SB, Cunningham JT: Rats exhibit aldosterone-dependent sodium appetite during 24 h hindlimb unloading. J Physiol 2004; 557: 661-670.
70. Sakai RR, McEwen BS, Fluharty SJ, Ma LY: The amygdala: site of genomic and nongenomic arousal of aldosterone-induced sodium intake. Kidney Int 2000; 57: 1337-1345.
71. Sakai RR, Nicolaidis S, Epstein AN: Salt appetite is suppressed by interference with angiotensin II and aldosterone. Am J Physiol 1986; 251:R762-R768.
72. Fluharty SJ, Epstein AN: Sodium appetite elicited by intracerebroventricular infusion of angiotensin II in the rat. II. Synergistic interaction with systemic mineralocorticoids. Behav Neurosci 1983; 97: 746-758.
73. Zhang DM, Stellar E, Epstein AN: Together intracranial angiotensin and systemic mineralocorticoid produce avidity for salt in the rat. Physiol Behav 1984; 32: 677-681.
74. Massi M, Epstein AN: Angiotensin/aldosterone synergy governs the salt appetite of the pigeon. Appetite 1990; 14: 181-192.
75. Epstein AN: Mineralocorticoids and cerebral angiotensin may act together to produce sodium appetite. Peptides 1982; 3: 493-494.
76. Daniels D, Yee DK, Faulconbridge LF, Fluharty SJ: Divergent behavioral roles of angiotensin receptor intracellular signaling cascades. Endocrinology 2005; 146: 5552-5560.
77. Wolf G, McGovern JF, Dicara LV: Sodium appetite: Some conceptual and methodologic aspects of a model drive system. Behav Biol 1974; 10: 27-42.
78. Yang J, Young MJ: The mineralocorticoid receptor and its coregulators. J Mol Endocrinol 2009; 43: 53-64.
79. Ingram MC, Wallace AM, Collier A, Fraser R, Connell JM: Sodium status, corticosteroid metabolism and blood pressure in normal human subjects and in a patient with abnormal salt appetite. Clin Exp Pharmacol Physiol 1996; 23: 375-378.
80. Roland BL, Li KX, Funder JW: Hybridization histochemical localization of 11?-hydro xysteroid dehydrogenase type 2 in rat brain. Endocrinology 1995; 136: 4697-4700.
81. Robson AC, Leckie CM, Seckl JR, Holmes MC: 11?-Hydroxysteroid dehydrogenase type 2 in the postnatal and adult rat brain. Brain Res Mol Brain Res 1998; 61: 1-10.
82. Holmes MC, Sangra M, French KL, Whittle IR, Paterson J, Mullins JJ, Seckl JR: 11?-Hydroxysteroid dehydrogenase type 2 protects the neonatal cerebellum from deleterious effects of glucocorticoids. Neuroscience 2006; 137: 865-873.
83. Geerling JC, Loewy AD: Aldosterone in the brain. Am J Physiol Renal Physiol 2009; 297:F559-F576.
84. Geerling JC, Engeland WC, Kawata M, Loewy AD: Aldosterone target neurons in the nucleus tractus solitarius drive sodium appetite. J Neurosci 2006; 26: 411-417.
85. Warntges S, Friedrich B, Henke G, Duranton C, Lang PA, Waldegger S, Meyermann R, Kuhl D, Speckmann EJ, Obermuller N, Witzgall R, Mack AF, Wagner HJ, Wagner A, Broer S, Lang F: Cerebral localization and regulation of the cell volume-sensitive serumand glucocorticoid-dependent kinase SGK1. Pflugers Arch 2002; 443: 617-624.
86. Lang F, Strutz-Seebohm N, Seebohm G, Lang UE: Significance of SGK1 in the regulation of neuronal function. J Physiol 2010; 588: 3349-3354.
87. Nakano M, Hirooka Y, Matsukawa R, Ito K, Sunagawa K: Mineralocorticoid receptors/epithelial Na + channels in the choroid plexus are involved in hypertensive mechanisms in stroke-prone spontaneously hypertensive rats. Hypertens Res 2013; 36: 277-284.
88. Umbach AT, Pathare G, Foller M, Brosens JJ, Artunc F, Lang F: SGK1-dependent salt appetite in pregnant mice. Acta Physiol (Oxf) 2011; 202: 39-45.
89. Giraldez T, Rojas P, Jou J, Flores C, Alvarez de la Rosa D: The epithelial sodium channel ?-subunit: new notes for an old song. Am J Physiol Renal Physiol 2012; 303:F328-F338.
90. Teruyama R, Sakuraba M, Wilson LL, Wandrey NE, Armstrong WE: Epithelial Na + sodium channels in magnocellular cells of the rat supraoptic and paraventricular nuclei. Am J Physiol Endocrinol Metab 2012; 302:E273-E285.
91. Van Huysse JW, Amin MS, Yang B, Leenen FH: Salt-induced hypertension in a mouse model of Liddle syndrome is mediated by epithelial sodium channels in the brain. Hypertension 2012; 60: 691-696.
92. Shi PP, Cao XR, Sweezer EM, Kinney TS, Williams NR, Husted RF, Nair R, Weiss RM, Williamson RA, Sigmund CD, Snyder PM, Staub O, Stokes JB, Yang B: Salt-sensitive hypertension and cardiac hypertrophy in mice deficient in the ubiquitin ligase Nedd4-2. Am J Physiol Renal Physiol 2008; 295:F462-F470.
93. Wang H, Leenen FH: Brain sodium channels mediate increases in brain 'ouabain' and blood pressure in Dahl S rats. Hypertension 2002; 40: 96-100.
94. Huang BS, Van Vliet BN, Leenen FH: Increases in CSF [Na +[ precede the increases in blood pressure in Dahl S rats and SHR on a high-salt diet. Am J Physiol Heart Circ Physiol 2004; 287:H1160-H1166.
95. Huang BS, Wang H, Leenen FH: Enhanced sympathoexcitatory and pressor responses to central Na + in Dahl salt-sensitive versus-resistant rats. Am J Physiol Heart Circ Physiol 2001; 281:H1881-H1889.
96. Pochynyuk O, Rieg T, Bugaj V, Schroth J, Fridman A, Boss GR, Insel PA, Stockand JD, Vallon V: Dietary Na + inhibits the open probability of the epithelial sodium channel in the kidney by enhancing apical P2Y2-receptor tone. FASEB J 2010; 24: 2056-2065.
97. Bernstein IL, Hennessy CJ: Amiloride-sensitive sodium channels and expression of sodium appetite in rats. Am J Physiol 1987; 253:R371-R374.
98. McCutcheon NB: Sodium-deficient rats are unmotivated by sodium chloride solutions mixed with the sodium channel blocker amiloride. Behav Neurosci 1991; 105: 764-766.
99. Roitman MF, Bernstein IL: Amiloride-sensitive sodium signals and salt appetite: multiple gustatory pathways. Am J Physiol 1999; 276:R1732-R1738.
100. Chandrashekar J, Kuhn C, Oka Y, Yarmolinsky DA, Hummler E, Ryba NJ, Zuker CS: The cells and peripheral representation of sodium taste in mice. Nature 2010; 464: 297-301.
101. Geerling JC, Loewy AD: Aldosterone-sensitive neurons in the nucleus of the solitary tract: efferent projections. J Comp Neurol 2006; 497: 223-250.