Role of the kidney in the pathogenesis of hypertension: Time for a neo-guytonian paradigm or a paradigm shift?

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 310, Issue 3, 2016, Pages R217-R229

  Evans, Roger G ^a   Bie, Peter ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Arthur Guyton; Pressure natriuresis; Thomas Coleman; Water and electrolyte homeostasis; Whole body autoregulation

Indexed keywords

CARDIOVASCULAR AUTOREGULATION; ESSENTIAL HYPERTENSION; EXTRACELLULAR SPACE; FEEDBACK SYSTEM; HEART OUTPUT; HOMEOSTASIS; HUMAN; HYPERTENSION; KIDNEY; MEAN ARTERIAL PRESSURE; NATRIURESIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SALT INTAKE; SALT LOADING; SODIUM URINE LEVEL; URINARY EXCRETION; VASCULAR RESISTANCE; ANIMAL; ARTERIAL PRESSURE; BIOLOGICAL MODEL; DISEASE MODEL; ELECTROLYTE BALANCE; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; ARTERIAL PRESSURE; DISEASE MODELS, ANIMAL; FEEDBACK, PHYSIOLOGICAL; HUMANS; HYPERTENSION; KIDNEY; MODELS, CARDIOVASCULAR; NATRIURESIS; WATER-ELECTROLYTE BALANCE;

EID: 84956927047     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00254.2015     Document Type: Review

References (108)

1. Andersen LJ, Andersen JL, Pump B, Bie P. Natriuresis induced by mild hypernatremia in humans. Am J Physiol Regul Integr Comp Physiol 282: R1754–R1761, 2002.
2. Antonios TF, Singer DR, Markandu ND, Mortimer PS, MacGregor GA. Rarefaction of skin capillaries in borderline essential hypertension suggests an early structural abnormality. Hypertension 34: 655–658, 1999.
3. Antonios TF, Singer DR, Markandu ND, Mortimer PS, MacGregor GA. Structural skin capillary rarefaction in essential hypertension. Hypertension 33: 998–1001, 1999.
4. Averina VA, Othmer HG, Fink GD, Osborn JW. A mathematical model of salt-sensitive hypertension: the neurogenic hypothesis. J Physiol 593: 3065–3075, 2015.
5. Averina VA, Othmer HG, Fink GD, Osborn JW. A new conceptual paradigm for the haemodynamics of salt-sensitive hypertension: a mathematical modelling approach. J Physiol 590: 5975–5992, 2012.
6. Battegay EJ, de Miguel LS, Petrimpol M, Humar R. Effects of anti-hypertensive drugs on vessel rarefaction. Current Opinion Pharmacol 7: 151–157, 2007.
7. Beard DA. Tautology vs. physiology in the etiology of hypertension. Physiology (Bethesda) 28: 270–271, 2013.
8. Berecek KH, Bohr DF. Whole body vascular reactivity during the development of deoxycorticosterone acetate hypertension in the pig. Circ Res 42: 764–771, 1978.
9. Bianchi G, Tenconi LT, Lucca R. Effect in the conscious dog of constriction of the renal artery to a sole remaining kidney on haemodynamics, sodium balance, body fluid volumes, plasma renin concentration and pressor responsiveness to angiotensin. Clin Sci 38: 741–766, 1970.
10. Bie P. Blood volume, blood pressure and total body sodium: internal signalling and output control. Acta Physiol (Oxf) 195: 187–196, 2009.
11. Bie P, Damkjaer M. Renin secretion and total body sodium: pathways of integrative control. Clin Exp Pharmacol Physiol 37: e34–e42, 2010.
12. Bie P, Wamberg S, Kjolby M. Volume natriuresis vs. pressure natriuresis. Acta Physiol Scand 181: 495–503, 2004.
13. Blaustein MP, Leenen FH, Chen L, Golovina VA, Hamlyn JM, Pallone TL, Van Huysse JW, Zhang J, Wier WG. How NaCl raises blood pressure: a new paradigm for the pathogenesis of salt-dependent hypertension. Am J Physiol Heart Circ Physiol 302: H1031–H1049, 2012.
14. Chade AR. Renal vascular structure and rarefaction. Compr Physiol 3: 817–831, 2013.
15. Coffman TM. Under pressure: the search for the essential mechanisms of hypertension. Nature Med 17: 1402–1409, 2011.
16. Coleman TG, Bower JD, Langford HG, Guyton AC. Regulation of arterial pressure in the anephric state. Circulation 42: 509–514, 1970.
17. Coleman TG, Granger HJ, Guyton AC. Whole-body circulatory autoregulation and hypertension. Circ Res 28, Suppl 2: 76–87, 1971.
18. Coleman TG, Guyton AC. Hypertension caused by salt loading in the dog. 3 Onset transients of cardiac output and other circulatory variables. Circ Res 25: 153–160, 1969.
19. Conway J. Changes in sodium balance and hemodynamics during development of experimental renal hypertension in dogs. Circ Res 22: 763–767, 1968.
20. Conway J. Hemodynamic aspects of essential hypertension in humans. Physiol Rev 64: 617–660, 1984.
21. Conway J, Lauwers P. Hemodynamic and hypotensive effects of long-term therapy with chlorothiazide. Circulation 21: 21–27, 1960.
22. Cowley AW Jr. Genetic and nongenetic determinants of salt sensitivity and blood pressure. Am J Clin Nutr 65: 587S–593S, 1997.
23. Cowley AW Jr. Long-term control of arterial blood pressure. Physiol Rev 72: 231–300, 1992.
24. Crowley SD, Coffman TM. The inextricable role of the kidney in hypertension. J Clin Invest 124: 2341–2347, 2014.
25. Damkjaer M, Isaksson GL, Stubbe J, Jensen BL, Assersen K, Bie P. Renal renin secretion as regulator of body fluid homeostasis. Pflügers Arch 465: 153–165, 2013.
26. Damkjaer M, Jensen PH, Schwammle V, Sprenger RR, Jacobsen IA, Jensen ON, Bie P. Selective renal vasoconstriction, exaggerated natriuresis and excretion rates of exosomic proteins in essential hypertension. Acta Physiol (Oxf) 212: 106–118, 2014.
27. Davis JO. The pathogenesis of chronic renovascular hypertension. Circ Res 40: 439–444, 1977.
28. Douglas BH, Guyton AC, Langston JB, Bishop VS. Hypertension caused by salt loading. II. Fluid volume and tissue pressure changes. Am J Physiol 207: 669–671, 1964.
29. Doyle AE. Sir Horace Smirk. Pioneer in drug treatment of hypertension. Hypertension 17: 247–250, 1991.
30. Evans RG, Majid DS, Eppel GA. Mechanisms mediating pressure natriuresis: what we know and what we need to find out. Clin Exp Pharmacol Physiol 32: 400–409, 2005.
31. Feihl F, Liaudet L, Waeber B. The macrocirculation and microcirculation of hypertension. Curr Hypertens Rep 11: 182–189, 2009.
32. Ferrario CM. Contribution of cardiac output and peripheral resistance to experimental renal hypertension. Am J Physiol 226: 711–717, 1974.
33. Ferrario CM, Page IH. Current views concerning cardiac output in the genesis of experimental hypertension. Circ Res 43: 821–831, 1978.
34. Ferrario CM, Page IH, McCubbin JW. Increased cardiac output as a contributory factor in experimental renal hypertension in dogs. Circ Res 27: 799–810, 1970.
35. Fine DM, Ariza-Nieto P, Osborn JW. Does whole body autoregulation mediate the hemodynamic responses to increased dietary salt in rats with clamped ANG II? Am J Physiol Heart Circ Physiol 285: H2670–H2678, 2003.
36. Fletcher PJ, Korner PI, Angus JA, Oliver JR. Cardiac output changes during experimental renal hypertension in the rabbit. Clin Sci Molec Med Suppl 3: 137s–139s, 1976.
37. Foss JD, Fink GD, Osborn JW. Reversal of genetic salt-sensitive hypertension by targeted sympathetic ablation. Hypertension 61: 806–811, 2013.
38. Freeman RH, Davis JO, Watkins BE. Development of chronic perinephritic hypertension in dogs without volume expansion. Am J Physiol Renal Fluid Electrolyte Physiol 233: F278–F281, 1977.
39. Frohlich ED, Schnaper HW, Wilson IM, Freis ED. Hemodynamic alterations in hypertensive patients due to chlorothiazide. N Engl J Med 262: 1261–1263, 1960.
40. Ganguli M, Tobian L, Iwai J. Cardiac output and peripheral resistance in strains of rats sensitive and resistant to NaCl hypertension. Hypertension 1: 3–7, 1979.
41. Granger HJ, Guyton AC. Autoregulation of the total systemic circulation following destruction of the central nervous system in the dog. Circ Res 25: 379–388, 1969.
42. Greene AS, Lombard JH, Cowley AW Jr, Hansen-Smith FM. Microvessel changes in hypertension measured by Griffonia simplicifolia I lectin. Hypertension 15: 779–783, 1990.
43. Greene AS, Tonellato PJ, Lui J, Lombard JH, Cowley AW Jr. Microvascular rarefaction and tissue vascular resistance in hypertension. Am J Physiol Heart Circ Physiol 256: H126–H131, 1989.
44. Greene AS, Yu ZY, Roman RJ, Cowley AW Jr. Role of blood volume expansion in Dahl rat model of hypertension. Am J Physiol Heart Circ Physiol 258: H508–H514, 1990.
45. Guyton AC. Circulatory Physiology III. Arterial Pressure and Hypertension. Philadelphia, PA: Saunders, 1980.
46. Guyton AC. The surprising kidney-fluid mechanism for pressure control–its infinite gain! Hypertension 16: 725–730, 1990.
47. Guyton AC, Coleman TG, Cowley AV Jr, Scheel KW, Manning RD Jr, Norman RA Jr. Arterial pressure regulation. Overriding dominance of the kidneys in long-term regulation and in hypertension. Am J Med 52: 584–594, 1972.
48. Hall JE, Granger JP, do Carmo JM, da Silva AA, Dubinion J, George E, Hamza S, Speed J, Hall ME. Hypertension: physiology and pathophysiology. Compr Physiol 2: 2393–2442, 2012.
49. Hall JE, Guyton AC, Brands MW. Pressure-volume regulation in hypertension. Kidney Int Suppl 55: S35–S41, 1996.
50. Hall JE, Mizelle HL, Woods LL, Montani JP. Pressure natriuresis and control of arterial pressure during chronic norepinephrine infusion. J Hypertens 6: 723–731, 1988.
51. Hallback M, Gothberg G, Lundin S, Ricksten SE, Folkow B. Hemodynamic consequences of resistance vessel rarification and of changes in smooth muscle sensitivity. Acta Physiol Scand 97: 233–240, 1976.
52. Hansen-Smith F, Greene AS, Cowley AW Jr, Lombard JH. Structural changes during microvascular rarefaction in chronic hypertension. Hypertension 15: 922–928, 1990.
53. Hansen-Smith FM, Morris LW, Greene AS, Lombard JH. Rapid microvessel rarefaction with elevated salt intake and reduced renal mass hypertension in rats. Circ Res 79: 324–330, 1996.
54. Harrison DG, Gongora MC. Oxidative stress and hypertension. Med Clin North Am 93: 621–635, 2009.
55. Hinojosa-Laborde C, Frohlich BH, Cowley AW Jr. Contribution of regional vascular responses to whole body autoregulation in conscious areflexic rats. Hypertension 17: 1078–1084, 1991.
56. Hinojosa-Laborde C, Greene AS, Cowley AW Jr. Autoregulation of the systemic circulation in conscious rats. Hypertension 11: 685–691, 1988.
57. Hinojosa-Laborde C, Greene AS, Cowley AW Jr. Whole body autoregulation in conscious areflexic rats during hypoxia and hyperoxia. Am J Physiol Heart Circ Physiol 256: H1023–H1029, 1989.
58. Hinojosa-Laborde C, Thunhorst RL, Cowley AW Jr. Vasoconstriction during volume expansion is independent of central control. Hypertension 15: 712–717, 1990.
59. Isaksson GL, Stubbe J, Lyngs Hansen P, Jensen BL, Bie P. Salt sensitivity of renin secretion, glomerular filtration rate and blood pressure in conscious Sprague-Dawley rats. Acta Physiol (Oxf) 446–454, 2014.
60. Johnson RJ, Lanaspa MA, Gabriela Sanchez-Lozada L, Rodriguez- Iturbe B. The discovery of hypertension: evolving views on the role of the kidneys, and current hot topics. Am J Physiol Renal Physiol 308: F167–F178, 2015.
61. Julius S, Conway J. Hemodynamic studies in patients with borderline blood pressure elevation. Circulation 38: 282–288, 1968.
62. Just A. Mechanisms of renal blood flow autoregulation: dynamics and contributions. Am J Physiol Regul Integr Comp Physiol 292: R1–R17, 2007.
63. Kim KE, Onesti G, DelGuercio ET, Greco J, Fernandes M, Eidelson B, Swartz C. Sequential hemodynamic changes in end-stage renal disease and the anephric state during volume expansion. Hypertension 2: 102–110, 1980.
64. Kjolby M, Bie P. Chronic activation of plasma renin is log-linearly related to dietary sodium and eliminates natriuresis in response to a pulse change in total body sodium. Am J Physiol Regul Integr Comp Physiol 294: R17–R25, 2008.
65. Korner PI. Essential Hypertension and Its Causes. Neural and Non- Neural Mechanisms. Oxford: Oxford University, 2007.
66. Krieger JE, Cowley AW Jr. Prevention of salt angiotensin II hypertension by servo control of body water. Am J Physiol Heart Circ Physiol 258: H994–H1003, 1990.
67. Krieger JE, Liard JF, Cowley AW Jr. Hemodynamics, fluid volume, and hormonal responses to chronic high-salt intake in dogs. Am J Physiol Heart Circ Physiol 259: H1629–H1636, 1990.
68. Krieger JE, Roman RJ, Cowley AW Jr. Hemodynamics and blood volume in angiotensin II salt-dependent hypertension in dogs. Am J Physiol Heart Circ Physiol 257: H1402–H1412, 1989.
69. Kuhn TS. The Essential Tension: Selected Studies in Scientific Tradition and Change. Chicago, IL: The University of Chicago Press, 1977.
70. Kuhn TS. The Structure of Scientific Revolutions. Chicago, IL: University of Chicago Press, 1962.
71. Kurtz TW, Dominiczak AF, DiCarlo SE, Pravenec M, Morris RC Jr. Molecular-based mechanisms of mendelian forms of salt-dependent hypertension: questioning the prevailing theory. Hypertension 65: 932–941, 2015.
72. Ledingham JM, Cohen RD. Changes in the extracellular fluid volume and cardiac output during the development of experimental renal hypertension. Canadian Med Assoc J 90: 292–294, 1964.
73. Ledingham JM, Cohen RD. The role of the heart in the pathogenesis of renal hypertension. Lancet 2: 979–981, 1963.
74. Lewis LK, Yandle TG, Hilton PJ, Jensen BP, Begg EJ, Nicholls MG. Endogenous ouabain is not ouabain. Hypertension 64: 680–683, 2014.
75. + signaling in human arterial myocytes: a mechanism that links salt to increased vascular resistance? Am J Physiol Heart Circ Physiol 303: H784–H794, 2012.
76. + signaling, vasoconstriction, and myogenic reactivity in Milan hypertensive rats. Am J Physiol Heart Circ Physiol 302: H611–H620, 2012.
77. Lohmeier TE, Iliescu R. The baroreflex as a long-term controller of arterial pressure. Physiology (Bethesda) 30: 148–158, 2015.
78. Lombard JH, Hinojosa-Laborde C, Cowley AW Jr. Hemodynamics and microcirculatory alterations in reduced renal mass hypertension. Hypertension 13: 128–138, 1989.
79. Lund-Johansen P. Hemodynamic patterns in the natural history of borderline hypertension. J Cardiovasc Pharmacol 8, Suppl 5: S8–S14, 1986.
80. McMaster WG, Kirabo A, Madhur MS, Harrison DG. Inflammation, immunity, and hypertensive end-organ damage. Circ Res 116: 1022–1033, 2015.
81. Metting PJ, Strader JR, Britton SL. Evaluation of whole body autoregulation in conscious dogs. Am J Physiol Heart Circ Physiol 255: H44–H52, 1988.
82. Mizelle HL, Montani JP, Hester RL, Didlake RH, Hall JE. Role of pressure natriuresis in long-term control of renal electrolyte excretion. Hypertension 22: 102–110, 1993.
83. Montani JP, Van Vliet BN. Understanding the contribution of Guyton’s large circulatory model to long-term control of arterial pressure. Exp Physiol 94: 382–388, 2009.
84. Moretti JL, Burke SL, Evans RG, Lambert GW, Head GA. Enhanced responses to ganglion blockade do not reflect sympathetic nervous system contribution to angiotensin II-induced hypertension. J Hypertens 27: 1838–1848, 2009.
85. Morgan DA, DiBona GF, Mark AL. Effects of interstrain renal transplantation on NaCl-induced hypertension in Dahl rats. Hypertension 15: 436–442, 1990.
86. Noon JP, Walker BR, Webb DJ, Shore AC, Holton DW, Edwards HV, Watt GC. Impaired microvascular dilatation and capillary rarefaction in young adults with a predisposition to high blood pressure. J Clin Invest 99: 1873–1879, 1997.
87. Olmsted F, Page IH. Hemodynamic changes in trained dogs during experimental renal hypertension. Circ Res 16: 134–139, 1965.
88. Onesti G, Kim KE, Greco JA, del Guercio ET, Fernandes M, Swartz C. Blood pressure regulation in end-stage renal disease and anephric man. Circ Res 36: 145–152, 1975.
89. Osborn JW. Hypothesis: set-points and long-term control of arterial pressure. A theoretical argument for a long-term arterial pressure control system in the brain rather than the kidney. Clin Exp Pharmacol Physiol 32: 384–393, 2005.
90. Osborn JW, Averina VA, Fink GD. Commentary on “Understanding the contribution of Guyton’s large circulatory model to long-term control of arterial pressure”. Exp Physiol 94: 388–389, 2009.
91. Osborn JW, Averina VA, Fink GD. Current computational models do not reveal the importance of the nervous system in long-term control of arterial pressure. Exp Physiol 94: 389–396, 2009.
92. Ott CE, Welch WJ, Lorenz JN, Whitescarver SA, Kotchen TA. Effect of salt deprivation on blood pressure in rats. Am J Physiol Heart Circ Physiol 256: H1426–H1431, 1989.
93. + channels: is membrane depolarization the signal? Circ Res 94: e97–e104, 2004.
94. + exchanger-1 and TRPC/Oraicontaining channels: key players in arterial hypertension. Adv Exp Med Biol 961: 365–374, 2013.
95. Qi N, Rapp JP, Brand PH, Metting PJ, Britton SL. Body fluid expansion is not essential for salt-induced hypertension in SS/Jr rats. Am J Physiol Regul Integr Comp Physiol 277: R1392–R1400, 1999.
96. Rakova N, Juttner K, Dahlmann A, Schroder A, Linz P, Kopp C, Rauh M, Goller U, Beck L, Agureev A, Vassilieva G, Lenkova L, Johannes B, Wabel P, Moissl U, Vienken J, Gerzer R, Eckardt KU, Muller DN, Kirsch K, Morukov B, Luft FC, Titze J. Long-term space flight simulation reveals infradian rhythmicity in human Na(+) balance. Cell Metab 17: 125–131, 2013.
97. Reinhardt HW, Corea M, Boemke W, Pettker R, Rothermund L, Scholz A, Schwietzer G, Persson PB. Resetting of 24-h sodium and water balance during 4 days of servo-controlled reduction of renal perfusion pressure. Am J Physiol Heart Circ Physiol 266: H650–H657, 1994.
98. Schalekamp MA, Man in’t Veld AJ, Wenting GJ. The second Sir George Pickering memorial lecture. What regulates whole body autoregulation? Clinical observations. J Hypertens 3: 97–108, 1985.
99. Schmidlin O, Forman A, Leone A, Sebastian A, Morris RC Jr. Salt sensitivity in blacks: evidence that the initial pressor effect of NaCl involves inhibition of vasodilatation by asymmetrical dimethylarginine. Hypertension 58: 380–385, 2011.
100. Seeliger E, Wronski T, Ladwig M, Rebeschke T, Persson PB, Reinhardt HW. The “body fluid pressure control system” relies on the renin-angiotensin-aldosterone system: balance studies in freely moving dogs. Clin Exp Pharmacol Physiol 32: 394–399, 2005.
101. Shepherd AP, Granger HJ, Smith EE, Guyton AC. Local control of tissue oxygen delivery and its contribution to the regulation of cardiac output. Am J Physiol 225: 747–755, 1973.
102. Simchon S, Manger WM, Brown TW. Dual hemodynamic mechanisms for salt-induced hypertension in Dahl salt-sensitive rats. Hypertension 17: 1063–1071, 1991.
103. Smirk FH. Hypotensive actions of hexamethonium bromide and some of its homologues; their use in high blood-pressure. Lancet 2: 1002–1005, 1952.
104. Thrasher TN. Arterial baroreceptor input contributes to long-term control of blood pressure. Curr Hypertens Rep 8: 249–254, 2006.
105. Titze J. Sodium balance is not just a renal affair. Curr Opin Nephrol Hypertens 23: 101–105, 2014.
106. Wirth A, Benyo Z, Lukasova M, Leutgeb B, Wettschureck N, Gorbey S, Orsy P, Horvath B, Maser-Gluth C, Greiner E, Lemmer B, Schutz G, Gutkind JS, Offermanns S. G12–G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nature Med 14: 64–68, 2008.
107. Wright CE, Angus JA. Enhanced total peripheral vascular responsiveness in hypertension accords with the amplifier hypothesis. J Hypertens 17: 1687–1696, 1999.
108. Wright CE, Angus JA, Korner PI. Structural factors increase blood pressure through the interaction of resistance vessel geometry with neurohumoral and local factors: estimates in rabbits with renal cellophane- wrap hypertension with intact effectors and during neurohumoral blockade. J Hypertens 20: 471–483, 2002.