Circulating angiotensin II and dietary salt: Converging signals for neurogenic hypertension

Circulating angiotensin II (Ang II) combined with high salt intake increases sympathetic nerve activity (SNA) in some forms of hypertension. Ang II-induced increases in SNA are modest, delayed, and specific to certain vascular beds. The brain targets for circulating Ang II are neurons in the area postrema (AP), subfornical organ (SFO), and possibly other circumventricular organs. Ang II signaling is integrated with sodium-sensitive neurons in the SFO and/or organum vasculosum of the lamina terminalis (OVLT) and drives sympathetic premotor neurons in the rostral ventrolateral medulla (RVLM) via the paraventricular nucleus (PVN). It is likely that, over time, new patterns of gene expression emerge within neurons of the SFO-PVN-RVLM pathway that transform their signaling properties. This transformation is critical in maintaining increased SNA. Identification of a novel gene supporting this process may provide new targets for treatment of neurogenic hypertension.

[1]  E. Ogata,et al.  Role of Chloride in Angiotensin II-Induced Salt-Sensitive Hypertension , 1991, Hypertension.

[2]  J. Wyss,et al.  Increased PI3-Kinase in Presympathetic Brain Areas of the Spontaneously Hypertensive Rat , 2005, Circulation research.

[3]  P. Guyenet,et al.  Medullospinal sympathoexcitatory neurons in normotensive and spontaneously hypertensive rats. , 1986, The American journal of physiology.

[4]  J. Osborn,et al.  Does whole body autoregulation mediate the hemodynamic responses to increased dietary salt in rats with clamped ANG II? , 2003, American journal of physiology. Heart and circulatory physiology.

[5]  R. Schmieder,et al.  Central blood volume: a determinant of early cardiac adaptation in arterial hypertension? , 1995, Journal of the American College of Cardiology.

[6]  S. Nesbitt,et al.  Sympathetic overactivity in hypertension. A moving target. , 1996, American journal of hypertension.

[7]  T. Lohmeier,et al.  Chronic angiotensin II infusion decreases renal norepinephrine overflow in conscious dogs. , 1984, Hypertension.

[8]  J. Osborn,et al.  Angiotensin And Osmoreceptor Inputs To The Area Postrema: Role In Long‐Term Control Of Fluid Homeostasis And Arterial Pressure , 2000, Clinical and experimental pharmacology & physiology.

[9]  G. Fink,et al.  Area postrema is critical for angiotensin-induced hypertension in rats. , 1987, Hypertension.

[10]  T. Saruta,et al.  Rostral Ventrolateral Medulla Neurons of Neonatal Wistar-Kyoto and Spontaneously Hypertensive Rats , 2002, Hypertension.

[11]  K. Kanmatsuse,et al.  Ventrolateral Medulla AT1 Receptors Support Arterial Pressure in Dahl Salt-Sensitive Rats , 2003, Hypertension.

[12]  M. Raizada,et al.  Novel mechanism of brain soluble epoxide hydrolase‐mediated blood pressure regulation in the spontaneously hypertensive rat , 2005, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[13]  G. Fink,et al.  Subfornical organ. Does it protect against angiotensin II-induced hypertension in the rat? , 1985, Circulation research.

[14]  R. Prewitt,et al.  Hemodynamic characteristics of sodium-sensitive human subjects. , 1987, Hypertension.

[15]  G. Fink LONG‐TERM SYMPATHO‐EXCITATORY EFFECT OF ANGIOTENSIN II: A MECHANISM OF SPONTANEOUS AND RENOVASCULAR HYPERTENSION , 1997, Clinical and experimental pharmacology & physiology.

[16]  F. Luft Salt and hypertension: recent advances and perspectives. , 1989, The Journal of laboratory and clinical medicine.

[17]  C. Bourque,et al.  Excitatory peptides and osmotic pressure modulate mechanosensitive cation channels in concert , 2000, Nature Neuroscience.

[18]  A. Sved,et al.  Brainstem mechanisms of hypertension: Role of the rostral ventrolateral medulla , 2003, Current hypertension reports.

[19]  P. Guyenet The sympathetic control of blood pressure , 2006, Nature Reviews Neuroscience.

[20]  A. Sved,et al.  Acute sympathoexcitatory action of angiotensin II in conscious baroreceptor-denervated rats. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[21]  M. Elam,et al.  Differentiated Response of the Sympathetic Nervous System to Angiotensin-Converting Enzyme Inhibition in Hypertension , 2000, Hypertension.

[22]  A. Sved,et al.  Dietary salt intake alters cardiovascular responses evoked from the rostral ventrolateral medulla. , 1999, American journal of physiology. Regulatory, integrative and comparative physiology.

[23]  C. Bourque,et al.  Molecular Transient Receptor Potential Vanilloid 1 Is Required for Intrinsic Osmoreception in Organum Vasculosum Lamina Terminalis Neurons and for Normal Thirst Responses to Systemic Hyperosmolality , 2006 .

[24]  Elisabeth Lambert,et al.  Mechanisms of sympathetic activation in obesity-related hypertension. , 2006, Hypertension.

[25]  J. Collister,et al.  Role of the Subfornical Organ in the Chronic Hypotensive Response to Losartan in Normal Rats , 2003, Hypertension.

[26]  W. Lautt,et al.  Blood volume, the venous system, preload, and cardiac output. , 1986, Canadian journal of physiology and pharmacology.

[27]  C. Dodt,et al.  Effects of selective angiotensin II receptor blockade on sympathetic nerve activity in primary hypertensive subjects , 2002, Journal of hypertension.

[28]  G. Fink,et al.  Chronic Low-Dose Angiotensin II Infusion Increases Venomotor Tone by Neurogenic Mechanisms , 2006, Hypertension.

[29]  Luft Fc Salt and hypertension: recent advances and perspectives. , 1989 .

[30]  M. Safar,et al.  Arterial and venous compliance in sustained essential hypertension. , 1987, Hypertension.

[31]  L. Petrocellis,et al.  Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain , 2006, Neuroscience.

[32]  K. King,et al.  Direct and indirect effects of angiotensin II on venous tone in conscious rats. , 1992, European journal of pharmacology.

[33]  M. Brody,et al.  The role of the anteroventral third ventricle (AV3V) region in experimental hypertension , 1978 .

[34]  A. Allen Inhibition of the Hypothalamic Paraventricular Nucleus in Spontaneously Hypertensive Rats Dramatically Reduces Sympathetic Vasomotor Tone , 2002, Hypertension.

[35]  A. K. Johnson,et al.  Subfornical organ-median preoptic connections and drinking and pressor responses to angiotensin II , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  A. C. Guyton Dominant role of the kidneys and accessory role of whole-body autoregulation in the pathogenesis of hypertension. , 1989, American journal of hypertension.

[37]  S. Malpas,et al.  What Sets the Long-Term Level of Renal Sympathetic Nerve Activity: A Role for Angiotensin II and Baroreflexes? , 2003, Circulation research.

[38]  G. Simon,et al.  Effect of neonatal sympathectomy on the development of structural vascular changes in angiotensin II‐treated rats , 1998, Journal of hypertension.

[39]  M. Raizada,et al.  Functional genomics as an emerging strategy for the investigation of central mechanisms in experimental hypertension. , 2004, Progress in biophysics and molecular biology.

[40]  M. Esler Differentiation in the effects of the angiotensin II receptor blocker class on autonomic function. , 2002, Journal of hypertension. Supplement : official journal of the International Society of Hypertension.

[41]  G. Mogenson,et al.  Effects of plasma angiotensin II and hypernatremia on subfornical organ neurons. , 1988, The American journal of physiology.

[42]  J. Anderson,et al.  Intrinsic osmosensitivity of subfornical organ neurons , 2000, Neuroscience.

[43]  G. Toney,et al.  Median preoptic neurones projecting to the hypothalamic paraventricular nucleus respond to osmotic, circulating Ang II and baroreceptor input in the rat , 2005, The Journal of physiology.

[44]  C. Bourque,et al.  Stretch-inactivated cation channels: cellular targets for modulation of osmosensitivity in supraoptic neurons. , 2002, Progress in brain research.

[45]  E. Jackson,et al.  Caffeine enhances the slow-pressor response to angiotensin II in rats. Evidence for a caffeine-angiotensin II interaction with the sympathetic nervous system. , 1987, The Journal of clinical investigation.

[46]  J. Osborn,et al.  Hormonal-sympathetic interactions in long-term regulation of arterial pressure: an hypothesis. , 1995, The American journal of physiology.

[47]  C. Ferrario Neurogenic Actions of Angiotensin II , 1983, Hypertension.

[48]  A. K. Johnson,et al.  In vitro sensitivity of median preoptic neurons to angiotensin II, osmotic pressure, and temperature. , 1993, The American journal of physiology.

[49]  J. Krieger,et al.  Hemodynamics, fluid volume, and hormonal responses to chronic high-salt intake in dogs. , 1990, The American journal of physiology.

[50]  G. Toney,et al.  Vagal afferent input alters the discharge of osmotic and ANG II-responsive median preoptic neurons projecting to the hypothalamic paraventricular nucleus , 2007, Brain Research.

[51]  R. Kline,et al.  Noradrenergic Mechanisms in the Brain and Peripheral Organs of Normotensive and Spontaneously Hypertensive Rats at Various Ages , 1981, Hypertension.

[52]  M. Elam,et al.  Increased sympathetic nerve activity in renovascular hypertension. , 1999, Circulation.

[53]  J. Krieger,et al.  Hemodynamics and blood volume in angiotensin II salt-dependent hypertension in dogs. , 1989, The American journal of physiology.

[54]  R. Kline,et al.  Does enhanced sympathetic tone contribute to angiotensin II hypertension in rats? , 1990, European journal of pharmacology.

[55]  J. Bains,et al.  Electrophysiology of the Circumventricular Organs , 1996, Frontiers in Neuroendocrinology.

[56]  P. Séguéla,et al.  An N-terminal variant of Trpv1 channel is required for osmosensory transduction , 2006, Nature Neuroscience.

[57]  T. Lohmeier Interactions between angiotensin II and baroreflexes in long-term regulation of renal sympathetic nerve activity. , 2003, Circulation research.

[58]  S. Nicolaidis,et al.  Converging projections of hydromineral imbalances and hormonal co-action upon neurons surrounding the anterior wall of the third ventricle. , 1984, Journal de physiologie.

[59]  G. Toney,et al.  Central osmotic regulation of sympathetic nerve activity. , 2003, Acta physiologica Scandinavica.