Neuroinflammation and sympathetic overactivity: Mechanisms and implications in hypertension

Essential hypertension is a multifactorial disorder with a strong genetic predisposition. Although anti-hypertensive medications have drastically reduced cardiovascular diseases mortality and morbidity rates, a significant percentage of hypertensive individuals currently on anti-hypertensive therapy, remain hypertensive. In spite of the emergence of transgenic animals and sophisticated tools to study the pathophysiology of hypertension, unraveling the causal mechanisms remains a challenge. Research on borderline hypertensive humans and/or prehypertensive rat models revealed an elevation in centrally-mediated sympathetic activity and a heightened neuroinflammatory state. Hyperactive brain renin angiotensin system (RAS), oxidative stress and neuroinflammation in brainstem cardiovascular centers and other brain regions are implicated as key factors in augmenting sympathetic activity in hypertension and other cardiovascular abnormalities. Angiotensin (Ang) II, the main RAS effector peptide, has been shown to trigger significant upsurges in pro-inflammatory cytokines and reactive oxygen species (ROS). Both microglial and astroglial cells, via a host of different mechanisms, contribute to pro-inflammatory states and ROS generation in the brain. Hence, it becomes essential to understand the impact of Ang II and neuroinflammatory mediators on the impairment of cardioregulatory centers in the brain, and to investigate the role of glia in Ang II-mediated sympathoexcitation. Understanding the mechanisms leading to an elevation in neuroinflammatory states, and the possible ways of counteracting it, could aid in devising better therapeutic strategies for the treatment of cardiovascular diseases and hypertension. This review primarily focuses on the molecular aspects of hypertension from a neuroinflammatory standpoint within brainstem cardiovascular centers.

[1]  B. Lernfelt,et al.  15-year longitudinal study of blood pressure and dementia , 1996, The Lancet.

[2]  W. De,et al.  Inflammatory cytokines in paraventricular nucleus modulate sympathetic activity and cardiac sympathetic afferent reflex in rats , 2011, Acta physiologica.

[3]  L. Graham,et al.  Sympathetic Drive in Anterior and Inferior Uncomplicated Acute Myocardial Infarction , 2004, Circulation.

[4]  G. Grassi,et al.  Sympathetic activation in the pathogenesis of hypertension and progression of organ damage. , 1999, Hypertension.

[5]  N. V. Kuzmenko,et al.  Arterial Baroreceptor Reflex Counteracts Long-Term Blood Pressure Increase in the Rat Model of Renovascular Hypertension , 2013, PloS one.

[6]  S. Carlson,et al.  Neurohormonal regulation of the sympathetic nervous system: New insights into central mechanisms of action , 2008, Current hypertension reports.

[7]  G. Speretta,et al.  Increased Expression of Macrophage Migration Inhibitory Factor in the Nucleus of the Solitary Tract Attenuates Renovascular Hypertension in Rats , 2017, American journal of hypertension.

[8]  D. Nation,et al.  Memory is preserved in older adults taking AT1 receptor blockers , 2017, Alzheimer's Research & Therapy.

[9]  F. Abboud,et al.  PERIPHERAL CENTRAL MECHANISMS OF BAROREFLEX RESETTING , 1989 .

[10]  J. Tschopp,et al.  A role for mitochondria in NLRP3 inflammasome activation , 2011, Nature.

[11]  J. Paton,et al.  Contributions of vascular inflammation in the brainstem for neurogenic hypertension , 2011, Respiratory Physiology & Neurobiology.

[12]  K. Miura,et al.  Maintenance of Neuronal Glutathione by Glial Cells , 1993, Journal of neurochemistry.

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

[14]  T. Thrasher,et al.  Baroreceptors, baroreceptor unloading, and the long-term control of blood pressure. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[15]  B. Folkow Physiological aspects of primary hypertension. , 1982, Physiological reviews.

[16]  S. Doggrell,et al.  Rat models of hypertension, cardiac hypertrophy and failure. , 1998, Cardiovascular research.

[17]  C. Sobey,et al.  Roles of Inflammation, Oxidative Stress, and Vascular Dysfunction in Hypertension , 2014, BioMed research international.

[18]  R. Dampney,et al.  Functional organization of central pathways regulating the cardiovascular system. , 1994, Physiological reviews.

[19]  J. P. Gilmore,et al.  Sino‐aortic denervation in the monkey. , 1985, The Journal of physiology.

[20]  R. Iliescu,et al.  The Baroreflex as a Long-Term Controller of Arterial Pressure , 2022 .

[21]  Panagiotis Kougias,et al.  Arterial baroreceptors in the management of systemic hypertension. , 2010, Medical science monitor : international medical journal of experimental and clinical research.

[22]  P. Korner,et al.  Sympathoadrenal system is critical for structural changes in genetic hypertension. , 1993, Hypertension.

[23]  Immunohistochemical evidence of tissue hypoxia and astrogliosis in the rostral ventrolateral medulla of spontaneously hypertensive rats , 2016, Brain Research.

[24]  M. Safar,et al.  Rilmenidine: a novel approach to first-line treatment of hypertension. , 1992, American journal of hypertension.

[25]  G. Fink,et al.  Region‐specific changes in sympathetic nerve activity in angiotensin II–salt hypertension in the rat , 2010, Experimental physiology.

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

[27]  G. Mancia,et al.  Carotid Sinus Baroreceptor Control of Arterial Pressure in Renovascular Hypertensive Subjects , 1982, Hypertension.

[28]  A. Sved,et al.  Pressure to change? Re-evaluating the role of baroreceptors in the long-term control of arterial pressure. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[29]  J S Floras,et al.  Paroxysmal hypertension due to sinoaortic baroreceptor denervation in humans. , 1987, Hypertension.

[30]  A. Takeshita,et al.  Overexpression of eNOS in the RVLM Causes Hypotension and Bradycardia Via GABA Release , 2001, Hypertension.

[31]  J. Floras,et al.  Simvastatin reduces sympathetic outflow and augments endothelium-independent dilation in non-hyperlipidaemic primary hypertension , 2012, Heart.

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

[33]  Kenji Sunagawa,et al.  Mitochondria-derived reactive oxygen species mediate sympathoexcitation induced by angiotensin II in the rostral ventrolateral medulla , 2008, Journal of hypertension.

[34]  Jaakko Tuomilehto,et al.  The prevention of dementia with antihypertensive treatment: new evidence from the Systolic Hypertension in Europe (Syst-Eur) study. , 2002 .

[35]  M. Raizada,et al.  Novel role of macrophage migration inhibitory factor in angiotensin II regulation of neuromodulation in rat brain. , 2001, Endocrinology.

[36]  J. Keller,et al.  Chronic exercise modulates RAS components and improves balance between pro- and anti-inflammatory cytokines in the brain of SHR , 2011, Basic Research in Cardiology.

[37]  Mazen S. Albaghdadi,et al.  Baroreflex control of long-term arterial pressure , 2007 .

[38]  M. Clark,et al.  MAPK activation patterns of AT1R and CB1R in SHR versus Wistar astrocytes: Evidence of CB1R hypofunction and crosstalk between AT1R and CB1R. , 2017, Cellular signalling.

[39]  Pamela L. Follett,et al.  Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J. Paton,et al.  Gene expression profiles of major cytokines in the nucleus tractus solitarii of the spontaneously hypertensive rat , 2008, Autonomic Neuroscience.

[41]  J F R Paton,et al.  The sympathetic nervous system and blood pressure in humans: implications for hypertension , 2012, Journal of Human Hypertension.

[42]  I. Tikkanen,et al.  Role of angiotensin II in blood pressure regulation and in the pathophysiology of cardiovascular disorders. , 1995, Journal of human hypertension.

[43]  K. Sunagawa,et al.  Angiotensin II type 1 receptor expression in astrocytes is upregulated leading to increased mortality in mice with myocardial infarction-induced heart failure. , 2014, American journal of physiology. Heart and circulatory physiology.

[44]  K. Mackie,et al.  Endocannabinoids Acting at Cannabinoid-1 Receptors Regulate Cardiovascular Function in Hypertension , 2004, Circulation.

[45]  M. Clark,et al.  Angiotensin II induces interleukin-6 expression in astrocytes: Role of reactive oxygen species and NF-κB , 2016, Molecular and Cellular Endocrinology.

[46]  Hynek Pikhart,et al.  Worldwide trends in blood pressure from 1975 to 2015: a pooled analysis of 1479 population-based measurement studies with 19·1 million participants , 2017, The Lancet.

[47]  M. Clark,et al.  Angiotensin II activates JAK2/STAT3 pathway and induces interleukin-6 production in cultured rat brainstem astrocytes , 2010, Regulatory Peptides.

[48]  J. Stern,et al.  Compromised blood–brain barrier permeability: novel mechanism by which circulating angiotensin II signals to sympathoexcitatory centres during hypertension , 2016, The Journal of physiology.

[49]  K. Tu,et al.  Mortality among patients with hypertension from 1995 to 2005: a population-based study , 2008, Canadian Medical Association Journal.

[50]  J. Francis,et al.  Cytokine blockade attenuates sympathoexcitation in heart failure: Cross‐talk between nNOS, AT‐1R and cytokines in the hypothalamic paraventricular nucleus , 2008, European journal of heart failure.

[51]  A. J. Honour,et al.  Diminished Baroreflex Sensitivity in High Blood Pressure , 1969, Circulation.

[52]  John Q. Wang,et al.  Expression of angiotensin II type 1 (AT(1)) receptor in the rostral ventrolateral medulla in rats. , 2002, Journal of applied physiology.

[53]  N. Schork,et al.  Hyperkinetic borderline hypertension in Tecumseh, Michigan , 1991, Journal of hypertension.

[54]  M. Mogi,et al.  Roles of Brain Angiotensin II in Cognitive Function and Dementia , 2012, International journal of hypertension.

[55]  S. Tonstad Rimonabant: a cannabinoid receptor blocker for the treatment of metabolic and cardiovascular risk factors. , 2006, Nutrition, metabolism, and cardiovascular diseases : NMCD.

[56]  Sreedhar Bodiga,et al.  Renin Angiotensin System in Cognitive Function and Dementia , 2013 .

[57]  J. Paton,et al.  Sympathetic overactivity occurs before hypertension in the two‐kidney, one‐clip model , 2016, Experimental physiology.

[58]  P. Sleight What is hypertension? , 1971, British heart journal.

[59]  N. Terui,et al.  Absence of sustained hypertension in sinoaortic-denervated rabbits. , 1986, The American journal of physiology.

[60]  Jillian L. Stobart,et al.  Multifunctional role of astrocytes as gatekeepers of neuronal energy supply , 2013, Front. Cell. Neurosci..

[61]  N. Abbott,et al.  Astrocyte–endothelial interactions and blood–brain barrier permeability * , 2002 .

[62]  Hiroaki Shimokawa,et al.  Increased Reactive Oxygen Species in Rostral Ventrolateral Medulla Contribute to Neural Mechanisms of Hypertension in Stroke-Prone Spontaneously Hypertensive Rats , 2003, Circulation.

[63]  B. Levine,et al.  Persistent Sympathetic Activation During Chronic Antihypertensive Therapy: A Potential Mechanism for Long Term Morbidity? , 2005, Hypertension.

[64]  G. Mancia,et al.  Effect of chronic angiotensin converting enzyme inhibition on sympathetic nerve traffic and baroreflex control of the circulation in essential hypertension , 1998, Journal of hypertension.

[65]  Filippo Caraci,et al.  New pharmacological strategies for treatment of Alzheimer's disease: focus on disease modifying drugs. , 2012, British journal of clinical pharmacology.

[66]  M. Nagarkatti,et al.  Cannabinoids as novel anti-inflammatory drugs. , 2009, Future medicinal chemistry.

[67]  K. Reynolds,et al.  Global burden of hypertension: analysis of worldwide data , 2005, The Lancet.

[68]  M. Clark,et al.  Angiotensin III induces signal transducer and activator of transcription 3 and interleukin-6 mRNA levels in cultured rat astrocytes , 2015, Journal of the renin-angiotensin-aldosterone system : JRAAS.

[69]  J. Karemaker,et al.  Denervation of Carotid Baro‐ and Chemoreceptors in Humans , 2003, The Journal of physiology.

[70]  F. Staal,et al.  Separation of oxidant-initiated and redox-regulated steps in the NF-kappa B signal transduction pathway. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[71]  H. Waki Central mechanisms of cardiovascular regulation during exercise : Integrative functions of the nucleus of the solitary tract , 2012 .

[72]  L. Weiss Long-term treatment with antihypertensive drugs in spontaneously hypertensive rats (SHR). Effects on blood pressure, survival rate and cardiovascular design. , 1974, Acta physiologica Scandinavica.

[73]  N. Kaplan The control of hypertension: a therapeutic breakthrough. , 1980, American scientist.

[74]  Guido Grassi,et al.  The ‘neuroadrenergic hypothesis’ in hypertension: current evidence , 2010, Experimental physiology.

[75]  M. Rattazzi,et al.  Inflammation and hypertension: the search for a link. , 2006, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[76]  S. Julius,et al.  Autonomic nervous cardiovascular regulation in borderline hypertension. , 1975, The American journal of cardiology.

[77]  M. Esler,et al.  Point: Chronic activation of the sympathetic nervous system is the dominant contributor to systemic hypertension. , 2010, Journal of applied physiology.

[78]  R. Frackowiak,et al.  Cardiopulmonary blood volume in borderline hypertension. , 1974, Clinical science and molecular medicine.

[79]  D. Goff,et al.  Resistant hypertension: diagnosis, evaluation, and treatment: a scientific statement from the American Heart Association Professional Education Committee of the Council for High Blood Pressure Research. , 2008, Circulation.

[80]  Nikolaus Marx,et al.  Improvement of cardiovascular risk markers by pioglitazone is independent from glycemic control: results from the pioneer study. , 2005, Journal of the American College of Cardiology.

[81]  M. Raizada,et al.  Brain cytokines as neuromodulators in cardiovascular control , 2010, Clinical and experimental pharmacology & physiology.

[82]  A. Takeshita,et al.  Cardiovascular Effects of Overexpression of Endothelial Nitric Oxide Synthase in the Rostral Ventrolateral Medulla in Stroke-Prone Spontaneously Hypertensive Rats , 2002, Hypertension.

[83]  S. Harrap,et al.  Brief Angiotensin Converting Enzyme Inhibitor Treatment in Young Spontaneously Hypertensive Rats Reduces Blood Pressure Long‐term , 1990, Hypertension.

[84]  G. Guyatt,et al.  Effects of centrally acting ACE inhibitors on the rate of cognitive decline in dementia , 2013, BMJ Open.

[85]  B. Szabo Imidazoline antihypertensive drugs: a critical review on their mechanism of action. , 2002, Pharmacology & therapeutics.

[86]  F. Ruschitzka,et al.  Novel anti-inflammatory drugs in hypertension. , 2006, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[87]  M. Szczyrek,et al.  Hypertension – The Silent Killer , 2011 .

[88]  A. Hao,et al.  Toll-like receptor 4 mediates microglial activation and production of inflammatory mediators in neonatal rat brain following hypoxia: role of TLR4 in hypoxic microglia , 2013, Journal of Neuroinflammation.

[89]  P. Magistretti,et al.  The role of astroglia in neuroprotection , 2009, Dialogues in clinical neuroscience.

[90]  J. Paton,et al.  Brainstem Hypoxia Contributes to the Development of Hypertension in the Spontaneously Hypertensive Rat , 2015, Hypertension.

[91]  A. Gourine,et al.  Purinergic signalling in the rostral ventro-lateral medulla controls sympathetic drive and contributes to the progression of heart failure following myocardial infarction in rats , 2012, Basic Research in Cardiology.

[92]  Paul A. Smith,et al.  Relationship between central sympathetic activity and stages of human hypertension. , 2004, American journal of hypertension.

[93]  D. Goldstein,et al.  Plasma catecholamines and essential hypertension. An analytical review. , 1983, Hypertension.

[94]  Y. Hirooka,et al.  Oxidative stress in the brain causes hypertension via sympathoexcitation , 2012, Front. Physio..

[95]  Christophe Tzourio,et al.  Hypertension, cognitive decline, and dementia: an epidemiological perspective , 2007, Dialogues in clinical neuroscience.

[96]  Lie Gao,et al.  Sympathoexcitation by central ANG II: roles for AT1 receptor upregulation and NAD(P)H oxidase in RVLM. , 2005, American journal of physiology. Heart and circulatory physiology.

[97]  P. May,et al.  Sustained Activation of the Central Baroreceptor Pathway in Angiotensin Hypertension , 2002, Hypertension.

[98]  M. Yassuda,et al.  Hypertension Severity Is Associated With Impaired Cognitive Performance , 2017, Journal of the American Heart Association.

[99]  J. Chan,et al.  Neuroinflammation and oxidative stress in rostral ventrolateral medulla contribute to neurogenic hypertension induced by systemic inflammation , 2012, Journal of Neuroinflammation.

[100]  J. Osborn Neural, Hormonal and Renal Interactions in Long-Term Blood Pressure Control 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 , 2005 .

[101]  M. Raizada,et al.  Brain Microglial Cytokines in Neurogenic Hypertension , 2010, Hypertension.

[102]  A. Takeshita,et al.  Reduced Nitric Oxide Synthase in the Brainstem Contributes to Enhanced Sympathetic Drive in Rats with Heart Failure , 2003, Journal of cardiovascular pharmacology.

[103]  T. Thrasher Unloading arterial baroreceptors causes neurogenic hypertension. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[104]  P. Fadel,et al.  Central sympathetic overactivity: Maladies and mechanisms , 2009, Autonomic Neuroscience.

[105]  J. Filosa,et al.  Circulating Angiotensin II Gains Access to the Hypothalamus and Brain Stem During Hypertension via Breakdown of the Blood–Brain Barrier , 2014, Hypertension.

[106]  R. McAllen,et al.  Baroreceptor inhibition of subretrofacial neurons: evidence from intracellular recordings in the cat , 1990, Neuroscience Letters.

[107]  D. Harron,et al.  The effects of rilmenidine on tests of autonomic function in humans , 1992, Clinical pharmacology and therapeutics.

[108]  W. Judy,et al.  Sympathetic Nerve Activity and Blood Pressure in Normotensive Backcross Rats Genetically Related to the Spontaneously Hypertensive Rat , 1979, Hypertension.

[109]  B. Fiser,et al.  Baroreflex sensitivity and essential hypertension in adolescents. , 2009, Physiological research.

[110]  P. Korner Circulatory control and the supercontrollers. , 1995, Journal of hypertension.

[111]  A. Sved,et al.  Excitatory amino acids in the rostral ventrolateral medulla support blood pressure in spontaneously hypertensive rats. , 2000, Hypertension.

[112]  High Rates of Uncontrolled Blood Pressure in the United States: Does This Represent a Missed Opportunity for Healthcare Providers? , 2013, Journal of clinical hypertension.

[113]  A. M. Reilly,et al.  Central Mechanisms Underlying Short‐ And Long‐Term Regulation Of The Cardiovascular System , 2002, Clinical and experimental pharmacology & physiology.

[114]  S. Kjeldsen,et al.  Adjusted Drug Treatment Is Superior to Renal Sympathetic Denervation in Patients With True Treatment-Resistant Hypertension , 2014, Hypertension.

[115]  J. Widimský,et al.  Changes of cardiac output in hypertensive disease. , 1957, Cardiologia.

[116]  D. Colombari,et al.  Macrophage migration inhibitory factor in the nucleus of solitary tract decreases blood pressure in SHRs. , 2013, Cardiovascular research.

[117]  E. Scott,et al.  Impact of Type 2 Diabetes Mellitus on Sympathetic Neural Mechanisms in Hypertension , 2003, Circulation.

[118]  A. Nishiyama,et al.  Angiotensin II induces human astrocyte senescence through reactive oxygen species production , 2011, Hypertension Research.

[119]  E A Anderson,et al.  Elevated Sympathetic Nerve Activity in Borderline Hypertensive Humans Evidence From Direct Intraneural Recordings , 1989, Hypertension.

[120]  L. Leng,et al.  Macrophage Migration Inhibitory Factor: An Intracellular Inhibitor of Angiotensin II-Induced Increases in Neuronal Activity , 2004, The Journal of Neuroscience.

[121]  F. Ayan,et al.  Short-term effects of rilmenidine on left ventricular hypertrophy and systolic and diastolic function in patients with essential hypertension: comparison with an angiotensin converting enzyme inhibitor and a calcium antagonist. , 2003, Japanese heart journal.

[122]  D. Harrison,et al.  The central nervous system and inflammation in hypertension. , 2011, Current opinion in pharmacology.

[123]  J. Axelrod,et al.  Adrenaline-forming enzyme in brainstem: elevation in genetic and experimental hypertension. , 2003, Science.

[124]  B. S. Zanutto,et al.  Neural set point for the control of arterial pressure: role of the nucleus tractus solitarius , 2010, Biomedical engineering online.

[125]  S. Gouraud,et al.  Brain inflammation in neurogenic hypertension , 2014 .

[126]  Kenji Sunagawa,et al.  Angiotensin II Type 1 Receptor–Activated Caspase-3 Through Ras/Mitogen-Activated Protein Kinase/Extracellular Signal-Regulated Kinase in the Rostral Ventrolateral Medulla Is Involved in Sympathoexcitation in Stroke-Prone Spontaneously Hypertensive Rats , 2010, Hypertension.

[127]  K. Sandberg,et al.  Sex differences in primary hypertension , 2012, Biology of Sex Differences.

[128]  W. Anderson,et al.  Assessment of human sympathetic nervous system activity from measurements of norepinephrine turnover. , 1988, Hypertension.

[129]  Arun Chockalingam,et al.  Impact of World Hypertension Day. , 2007, The Canadian journal of cardiology.

[130]  E. Colombari,et al.  Role of the medulla oblongata in hypertension. , 2001, Hypertension.

[131]  Naji Tabet,et al.  Hypertension and inflammation in Alzheimer's disease: close partners in disease development and progression! , 2014, Journal of Alzheimer's disease : JAD.

[132]  K. Inenaga,et al.  Angiotensin II sensitive neurons in the supraoptic nucleus, subfornical organ and anteroventral third ventricle of rats in vitro , 1987, Brain Research.

[133]  T. Saruta,et al.  Importance of rostral ventrolateral medulla neurons in determining efferent sympathetic nerve activity and blood pressure , 2011, Hypertension Research.

[134]  P. Fadel,et al.  Therapeutic strategies for targeting excessive central sympathetic activation in human hypertension , 2010, Experimental physiology.

[135]  Urszula Demkow,et al.  Brain inflammation and hypertension: the chicken or the egg? , 2015, Journal of Neuroinflammation.

[136]  J. Paton,et al.  Specific inflammatory condition in nucleus tractus solitarii of the SHR: Novel insight for neurogenic hypertension? , 2008, Autonomic Neuroscience.

[137]  J. Paton,et al.  Is neurogenic hypertension related to vascular inflammation of the brainstem? , 2009, Neuroscience & Biobehavioral Reviews.

[138]  M. Raizada,et al.  Brain renin–angiotensin system dysfunction in hypertension: recent advances and perspectives , 2003, British journal of pharmacology.

[139]  J. Seagard,et al.  Differential endocannabinoid regulation of baroreflex-evoked sympathoinhibition in normotensive versus hypertensive rats , 2009, Autonomic Neuroscience.

[140]  A Pedotti,et al.  Blood Pressure and Heart Rate Variabilities in Normotensive and Hypertensive Human Beings , 1983, Circulation research.

[141]  J. Francis,et al.  Toll-like receptor 4 inhibition within the paraventricular nucleus attenuates blood pressure and inflammatory response in a genetic model of hypertension , 2015, Journal of Neuroinflammation.

[142]  A. Mark,et al.  Direct evidence from intraneural recordings for increased central sympathetic outflow in patients with heart failure. , 1986, Circulation.

[143]  M. Clark,et al.  Heterologous regulation of the cannabinoid type 1 receptor by angiotensin II in astrocytes of spontaneously hypertensive rats , 2016, Journal of neurochemistry.

[144]  G. Mancia,et al.  Neuroadrenergic and reflex abnormalities in patients with metabolic syndrome , 2005, Diabetologia.

[145]  S. Biswas Does the Interdependence between Oxidative Stress and Inflammation Explain the Antioxidant Paradox? , 2016, Oxidative medicine and cellular longevity.