Improved pulmonary vascular reactivity and decreased hypertrophic remodeling during nonhypercapnic acidosis in experimental pulmonary hypertension.

Pulmonary hypertension (PH) is characterized by pulmonary arteriolar remodeling with excessive pulmonary vascular smooth muscle cell (VSMC) proliferation. This results in decreased responsiveness of pulmonary circulation to vasodilator therapies. We have shown that extracellular acidosis inhibits VSMC proliferation and migration in vitro. Here we tested whether induction of nonhypercapnic acidosis in vivo ameliorates PH and the underlying pulmonary vascular remodeling and dysfunction. Adult male Sprague-Dawley rats were exposed to hypoxia (8.5% O(2)) for 2 wk, or injected subcutaneously with monocrotaline (MCT, 60 mg/kg) to develop PH. Acidosis was induced with NH(4)Cl (1.5%) in the drinking water 5 days prior to and during the 2 wk of hypoxic exposure (prevention protocol), or after MCT injection from day 21 to 28 (reversal protocol). Right ventricular systolic pressure (RVSP) and Fulton's index were measured, and pulmonary arteriolar remodeling was analyzed. Pulmonary and mesenteric artery contraction to phenylephrine (Phe) and high KCl, and relaxation to acetylcholine (ACh) and sodium nitroprusside (SNP) were examined ex vivo. Hypoxic and MCT-treated rats demonstrated increased RVSP, Fulton's index, and pulmonary arteriolar thickening. In pulmonary arteries of hypoxic and MCT rats there was reduced contraction to Phe and KCl and reduced vasodilation to ACh and SNP. Acidosis prevented hypoxia-induced PH, reversed MCT-induced PH, and resulted in reduction in all indexes of PH including RVSP, Fulton's index, and pulmonary arteriolar remodeling. Pulmonary artery contraction to Phe and KCl was preserved or improved, and relaxation to ACh and SNP was enhanced in NH(4)Cl-treated PH animals. Acidosis alone did not affect the hemodynamics or pulmonary vascular function. Phe and KCl contraction and ACh and SNP relaxation were not different in mesenteric arteries of all groups. Thus nonhypercapnic acidosis ameliorates experimental PH, attenuates pulmonary arteriolar thickening, and enhances pulmonary vascular responsiveness to vasoconstrictor and vasodilator stimuli. Together with our finding that acidosis decreases VSMC proliferation, the results are consistent with the possibility that nonhypercapnic acidosis promotes differentiation of pulmonary VSMCs to a more contractile phenotype, which may enhance the effectiveness of vasodilator therapies in PH.

[1]  J. Westwick,et al.  A novel murine model of severe pulmonary arterial hypertension. , 2011, American journal of respiratory and critical care medicine.

[2]  P. Aaronson,et al.  Key role of the RhoA/Rho kinase system in pulmonary hypertension. , 2011, Pulmonary pharmacology & therapeutics.

[3]  H. Christou,et al.  Heme Oxygenase-1 Does Not Mediate the Effects of Extracellular Acidosis on Vascular Smooth Muscle Cell Proliferation, Migration, and Susceptibility to Apoptosis , 2011, Journal of Vascular Research.

[4]  C. Wagner,et al.  Induction of Metabolic Acidosis with Ammonium Chloride (NH4Cl) in Mice and Rats – Species Differences and Technical Considerations , 2011, Cellular Physiology and Biochemistry.

[5]  P. McNamara,et al.  Rescue treatment with a Rho-kinase inhibitor normalizes right ventricular function and reverses remodeling in juvenile rats with chronic pulmonary hypertension. , 2010, American journal of physiology. Heart and circulatory physiology.

[6]  R. Khalil,et al.  Sex hormones and vascular protection in pulmonary arterial hypertension. , 2010, Journal of cardiovascular pharmacology.

[7]  M. Humbert,et al.  Long-term response to calcium-channel blockers in non-idiopathic pulmonary arterial hypertension. , 2010, European heart journal.

[8]  Horst Olschewski,et al.  Addition of inhaled treprostinil to oral therapy for pulmonary arterial hypertension: a randomized controlled clinical trial. , 2010, Journal of the American College of Cardiology.

[9]  N. Voelkel,et al.  Formation of Plexiform Lesions in Experimental Severe Pulmonary Arterial Hypertension , 2010, Circulation.

[10]  G. Raskob,et al.  Pulmonary arterial hypertension: baseline characteristics from the REVEAL Registry. , 2010, Chest.

[11]  Sally H Vitali,et al.  Impaired Vasoconstriction and Nitric Oxide-Mediated Relaxation in Pulmonary Arteries of Hypoxia- and Monocrotaline-Induced Pulmonary Hypertensive Rats , 2010, Journal of Pharmacology and Experimental Therapeutics.

[12]  M. Frid,et al.  Sustained hypoxia leads to the emergence of cells with enhanced growth, migratory, and promitogenic potentials within the distal pulmonary artery wall. , 2009, American journal of physiology. Lung cellular and molecular physiology.

[13]  Kurt R Stenmark,et al.  Animal models of pulmonary arterial hypertension: the hope for etiological discovery and pharmacological cure. , 2009, American journal of physiology. Lung cellular and molecular physiology.

[14]  Chengqun Huang,et al.  NOTCH3 SIGNALING IS REQUIRED FOR THE DEVELOPMENT OF PULMONARY ARTERIAL HYPERTENSION , 2009, Nature Medicine.

[15]  F. McGowan,et al.  Divergent Cardiopulmonary Actions of Heme Oxygenase Enzymatic Products in Chronic Hypoxia , 2009, PloS one.

[16]  A. Pries,et al.  Inhaled nitric oxide versus aerosolized iloprost for the treatment of pulmonary hypertension with left heart disease* , 2009, Critical care medicine.

[17]  J. Stehlik,et al.  Combined use of PDE5 inhibitors and nitrates in the treatment of pulmonary arterial hypertension in patients with heart failure. , 2009, Journal of cardiac failure.

[18]  E. Mark,et al.  Interleukin-6 Overexpression Induces Pulmonary Hypertension , 2009, Circulation research.

[19]  C. Burger Pulmonary Hypertension in COPD: A Review and Consideration of the Role of Arterial Vasodilators , 2009, COPD.

[20]  T. Murata,et al.  Time-dependent phenotypic and contractile changes of pulmonary artery in chronic hypoxia-induced pulmonary hypertension. , 2009, Journal of pharmacological sciences.

[21]  J. Guan,et al.  The p38 mitogen‐activated protein kinase pathway is involved in the regulation of heme oxygenase‐1 by acidic extracellular pH in aortic smooth muscle cells , 2008, Journal of cellular biochemistry.

[22]  C. Knoderer,et al.  Use of Sildenafil to Facilitate Weaning From Inhaled Nitric Oxide in Children With Pulmonary Hypertension Following Surgery for Congenital Heart Disease , 2008, Journal of intensive care medicine.

[23]  H. Farber The Status of Pulmonary Arterial Hypertension in 2008 , 2008, Circulation.

[24]  V. Kurup,et al.  Pulmonary arterial remodeling induced by a Th2 immune response , 2008, The Journal of experimental medicine.

[25]  N. Ambartsumian,et al.  Reactivation of gammaHV68 induces neointimal lesions in pulmonary arteries of S100A4/Mts1-overexpressing mice in association with degradation of elastin. , 2008, American journal of physiology. Lung cellular and molecular physiology.

[26]  Manching Ku,et al.  Control of Phenotypic Plasticity of Smooth Muscle Cells by Bone Morphogenetic Protein Signaling through the Myocardin-related Transcription Factors* , 2007, Journal of Biological Chemistry.

[27]  M. Oka,et al.  Endothelin-1 and Serotonin are Involved in Activation of RhoA/Rho Kinase Signaling in the Chronically Hypoxic Hypertensive Rat Pulmonary Circulation , 2007, Journal of cardiovascular pharmacology.

[28]  U. Ikeda,et al.  Interleukin-10 Expression Mediated by an Adeno-Associated Virus Vector Prevents Monocrotaline-Induced Pulmonary Arterial Hypertension in Rats , 2007, Circulation research.

[29]  U. Christians,et al.  Serotonin transporter protein in pulmonary hypertensive rats treated with atorvastatin. , 2007, American journal of physiology. Lung cellular and molecular physiology.

[30]  Christine M. Miller,et al.  Plexiform-like lesions and increased tissue factor expression in a rat model of severe pulmonary arterial hypertension. , 2007, American journal of physiology. Lung cellular and molecular physiology.

[31]  I. McMurtry,et al.  Rodent models of PAH: are we there yet? , 2007, American journal of physiology. Lung cellular and molecular physiology.

[32]  C. Rohlicek,et al.  Decreased left ventricular function, myocarditis, and coronary arteriolar medial thickening following monocrotaline administration in adult rats. , 2007, Journal of applied physiology.

[33]  N. Voelkel,et al.  Absence of T cells confers increased pulmonary arterial hypertension and vascular remodeling. , 2007, American journal of respiratory and critical care medicine.

[34]  Y. Shang,et al.  Transplantation of autologous endothelial progenitor cells may be beneficial in patients with idiopathic pulmonary arterial hypertension: a pilot randomized controlled trial. , 2007, Journal of the American College of Cardiology.

[35]  K. Stenmark,et al.  Rosiglitazone attenuates hypoxia-induced pulmonary arterial remodeling. , 2007, American journal of physiology. Lung cellular and molecular physiology.

[36]  N. Voelkel,et al.  Rho Kinase-Mediated Vasoconstriction Is Important in Severe Occlusive Pulmonary Arterial Hypertension in Rats , 2007, Circulation research.

[37]  S. N. Murthy,et al.  Intratracheal mesenchymal stem cell administration attenuates monocrotaline-induced pulmonary hypertension and endothelial dysfunction. , 2007, American journal of physiology. Heart and circulatory physiology.

[38]  P. McNamara,et al.  Therapeutic hypercapnia prevents chronic hypoxia-induced pulmonary hypertension in the newborn rat. , 2006, American journal of physiology. Lung cellular and molecular physiology.

[39]  R. Jones,et al.  The influence of sex hormones on pulmonary vascular reactivity: possible vasodilator therapies for the treatment of pulmonary hypertension. , 2006, Current vascular pharmacology.

[40]  P. Pacaud,et al.  Inhibition of RhoA/Rho kinase pathway is involved in the beneficial effect of sildenafil on pulmonary hypertension , 2005, British journal of pharmacology.

[41]  T. Welte,et al.  Goal-oriented treatment and combination therapy for pulmonary arterial hypertension , 2005, European Respiratory Journal.

[42]  W. Seeger,et al.  Reversal of experimental pulmonary hypertension by PDGF inhibition. , 2005, The Journal of clinical investigation.

[43]  Marguerite Hatch,et al.  Ethylene glycol induces hyperoxaluria without metabolic acidosis in rats. , 2005, American journal of physiology. Renal physiology.

[44]  M. Humbert,et al.  Long-Term Response to Calcium Channel Blockers in Idiopathic Pulmonary Arterial Hypertension , 2005, Circulation.

[45]  D. Ivy,et al.  Development of Occlusive Neointimal Lesions in Distal Pulmonary Arteries of Endothelin B Receptor—Deficient Rats: A New Model of Severe Pulmonary Arterial Hypertension , 2005, Circulation.

[46]  S. Kourembanas,et al.  Extracellular acidosis induces heme oxygenase-1 expression in vascular smooth muscle cells. , 2005, American journal of physiology. Heart and circulatory physiology.

[47]  S. Archer,et al.  Gene therapy targeting survivin selectively induces pulmonary vascular apoptosis and reverses pulmonary arterial hypertension. , 2005, The Journal of clinical investigation.

[48]  J. Loscalzo,et al.  Pulmonary arterial hypertension , 2006, The New England journal of medicine.

[49]  K. Morris,et al.  Attenuation of acute hypoxic pulmonary vasoconstriction and hypoxic pulmonary hypertension in mice by inhibition of Rho-kinase. , 2004, American journal of physiology. Lung cellular and molecular physiology.

[50]  R. Budhiraja,et al.  Endothelial Dysfunction in Pulmonary Hypertension , 2004, Circulation.

[51]  H. Farber,et al.  Pulmonary hypertension as a risk factor for death in patients with sickle cell disease. , 2004, The New England journal of medicine.

[52]  N. Ambartsumian,et al.  S100A4/Mts1 produces murine pulmonary artery changes resembling plexogenic arteriopathy and is increased in human plexogenic arteriopathy. , 2004, The American journal of pathology.

[53]  W. Seeger,et al.  Chronic sildenafil treatment inhibits monocrotaline-induced pulmonary hypertension in rats. , 2004, American journal of respiratory and critical care medicine.

[54]  P. D. del Nido,et al.  Hypoxia and Stretch Regulate Intercellular Communication in Vascular Smooth Muscle Cells Through Reactive Oxygen Species Formation , 2003, Arteriosclerosis, thrombosis, and vascular biology.

[55]  G. Berry,et al.  Simvastatin Rescues Rats From Fatal Pulmonary Hypertension by Inducing Apoptosis of Neointimal Smooth Muscle Cells , 2003, Circulation.

[56]  E. Chang,et al.  Metabolic acidosis in rats increases intestinal NHE2 and NHE3 expression and function. , 2002, American journal of physiology. Gastrointestinal and liver physiology.

[57]  M. Yanagisawa,et al.  Exaggerated hypoxic pulmonary hypertension in endothelin B receptor-deficient rats. , 2002, American journal of physiology. Lung cellular and molecular physiology.

[58]  S. Narumiya,et al.  Prostacyclin receptor-dependent modulation of pulmonary vascular remodeling. , 2001, American journal of respiratory and critical care medicine.

[59]  M. Yanagisawa,et al.  Endothelin B receptor deficiency potentiates ET-1 and hypoxic pulmonary vasoconstriction. , 2001, American journal of physiology. Lung cellular and molecular physiology.

[60]  P. Hirth,et al.  Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death‐dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[61]  R. Nagai,et al.  Vascular smooth muscle cell phenotypes in primary pulmonary hypertension. , 2001, The European respiratory journal.

[62]  R. Rabkin,et al.  Effect of metabolic acidosis on the insulin-like growth factor-I system and cathepsins B and L gene expression in the kidney. , 2000, The Journal of laboratory and clinical medicine.

[63]  C. Kleeman,et al.  Chronic metabolic acidosis in azotemic rats on a high-phosphate diet halts the progression of renal disease. , 2000, Kidney international.

[64]  P. McLoughlin,et al.  Chronic hypercapnia inhibits hypoxic pulmonary vascular remodeling. , 2000, American journal of physiology. Heart and circulatory physiology.

[65]  L. Shimoda,et al.  Altered pulmonary vasoreactivity in the chronically hypoxic lung. , 2000, Physiological research.

[66]  H. Itoh,et al.  Effects of the endothelin ET(A) receptor antagonist, TA-0201, on pulmonary arteries isolated from hypoxic rats. , 1999, European journal of pharmacology.

[67]  N. Voelkel,et al.  Pulmonary prostacyclin synthase overexpression in transgenic mice protects against development of hypoxic pulmonary hypertension. , 1999, The Journal of clinical investigation.

[68]  R Busse,et al.  NO: the primary EDRF. , 1999, Journal of molecular and cellular cardiology.

[69]  B. Thompson,et al.  Amiloride analogs inhibit chronic hypoxic pulmonary hypertension. , 1998, American journal of respiratory and critical care medicine.

[70]  Wei Zhang,et al.  Pulmonary hemodynamics modify the rat pulmonary artery response to injury. A neointimal model of pulmonary hypertension. , 1997, The American journal of pathology.

[71]  C. Hsieh,et al.  Prevention of Hypoxia-Induced Pulmonary Hypertension by Enhancement of Endogenous Heme Oxygenase-1 in the Rat. • 238 , 1997, Pediatric Research.

[72]  B. Thompson,et al.  The role of Na+/H+ exchange and growth factors in pulmonary artery smooth muscle cell proliferation. , 1996, American journal of respiratory cell and molecular biology.

[73]  R. McIntyre,et al.  Mechanistic imbalance of pulmonary vasomotor control in progressive lung injury. , 1996, Surgery.

[74]  B. Thompson,et al.  Na+/H+ exchange in pulmonary artery smooth muscle from spontaneously hypertensive and Wistar-Kyoto rats. , 1995, The American journal of physiology.

[75]  G. Pietra Histopathology of primary pulmonary hypertension. , 1994, Chest.

[76]  S. Rich,et al.  The effect of high doses of calcium-channel blockers on survival in primary pulmonary hypertension. , 1992, The New England journal of medicine.

[77]  B. Thompson,et al.  Contribution of Na+/H+ exchange to pH regulation in pulmonary artery smooth muscle cells. , 1991, American journal of respiratory cell and molecular biology.

[78]  P. Braquet,et al.  Loss of endothelium-dependent relaxant activity in the pulmonary circulation of rats exposed to chronic hypoxia. , 1991, The Journal of clinical investigation.

[79]  L. Ignarro Nitric oxide. A novel signal transduction mechanism for transcellular communication. , 1990, Hypertension.

[80]  B. Groves,et al.  Histopathology of primary pulmonary hypertension. A qualitative and quantitative study of pulmonary blood vessels from 58 patients in the National Heart, Lung, and Blood Institute, Primary Pulmonary Hypertension Registry. , 1989, Circulation.

[81]  R. Khalil,et al.  Sustained contraction of vascular smooth muscle: calcium influx or C-kinase activation? , 1988, The Journal of pharmacology and experimental therapeutics.

[82]  M. Gillespie,et al.  Vascular hyperresponsiveness in perfused lungs from monocrotaline-treated rats. , 1986, The American journal of physiology.