Coronary Microvascular Dysfunction and Heart Failure with Preserved Ejection Fraction - implications for Chronic Inflammatory Mechanisms | Bentham Science
Generic placeholder image

Current Cardiology Reviews

Editor-in-Chief

ISSN (Print): 1573-403X
ISSN (Online): 1875-6557

Mini-Review Article

Coronary Microvascular Dysfunction and Heart Failure with Preserved Ejection Fraction - implications for Chronic Inflammatory Mechanisms

Author(s): Katie Anne Fopiano, Sawan Jalnapurkar, Alec C. Davila, Vishal Arora* and Zsolt Bagi*

Volume 18, Issue 2, 2022

Published on: 08 December, 2021

Article ID: e310821195986 Pages: 9

DOI: 10.2174/1573403X17666210831144651

Price: $65

Open Access Journals Promotions 2
Abstract

Coronary Microvascular Dysfunction (CMD) is now considered one of the key underlying pathologies responsible for the development of both acute and chronic cardiac complications. It has been long recognized that CMD contributes to coronary no-reflow, which occurs as an acute complication during percutaneous coronary interventions. More recently, CMD was proposed to play a mechanistic role in the development of left ventricle diastolic dysfunction in heart failure with preserved ejection fraction (HFpEF). Emerging evidence indicates that a chronic low-grade pro-inflammatory activation predisposes patients to both acute and chronic cardiovascular complications raising the possibility that pro-inflammatory mediators serve as a mechanistic link in HFpEF. Few recent studies have evaluated the role of the hyaluronan-CD44 axis in inflammation-related cardiovascular pathologies, thus warranting further investigations. This review article summarizes current evidence for the role of CMD in the development of HFpEF, focusing on molecular mediators of chronic proinflammatory as well as oxidative stress mechanisms and possible therapeutic approaches to consider for treatment and prevention.

Keywords: Heart failure, preserved ejection fraction, microvascular dysfunction, inflammation, oxidative stress, coronary arteries.

Graphical Abstract
[1]
Salazar J, Rojas-Quintero J, Cano C, et al. Neprilysin: A potential therapeutic target of arterial hypertension? Curr Cardiol Rev 2020; 16(1): 25-35.
[http://dx.doi.org/10.2174/1573403X15666190625160352] [PMID: 31241018]
[2]
Oktay AA, Rich JD, Shah SJ. The emerging epidemic of heart failure with preserved ejection fraction. Curr Heart Fail Rep 2013; 10(4): 401-10.
[http://dx.doi.org/10.1007/s11897-013-0155-7] [PMID: 24078336]
[3]
Scheffer M, Driessen-Waaijer A, Hamdani N, et al. Stratified treatment of heart failure with preserved ejection fraction: Rationale and design of the STADIA-HFpEF trial. ESC Heart Fail 2020; 7(6): 4478-87.
[http://dx.doi.org/10.1002/ehf2.13055] [PMID: 33073523]
[4]
Dryer K, Gajjar M, Narang N, et al. Coronary microvascular dysfunction in patients with heart failure with preserved ejection fraction. Am J Physiol Heart Circ Physiol 2018; 314(5): H1033-42.
[http://dx.doi.org/10.1152/ajpheart.00680.2017] [PMID: 29424571]
[5]
Shah SJ, Lam CSP, Svedlund S, et al. Prevalence and correlates of coronary microvascular dysfunction in heart failure with preserved ejection fraction: PROMIS-HFpEF. Eur Heart J 2018; 39(37): 3439-50.
[http://dx.doi.org/10.1093/eurheartj/ehy531] [PMID: 30165580]
[6]
Paulus WJ, Tschöpe C. A novel paradigm for heart failure with preserved ejection fraction: Comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation. J Am Coll Cardiol 2013; 62(4): 263-71.
[http://dx.doi.org/10.1016/j.jacc.2013.02.092] [PMID: 23684677]
[7]
Franssen C, Chen S, Unger A, et al. Myocardial microvascular inflammatory endothelial activation in heart failure with preserved ejection fraction. JACC Heart Fail 2016; 4(4): 312-24.
[http://dx.doi.org/10.1016/j.jchf.2015.10.007] [PMID: 26682792]
[8]
Prasad M, Matteson EL, Herrmann J, et al. Uric acid is associated with inflammation, coronary microvascular dysfunction, and adverse outcomes in postmenopausal women. Hypertension 2017; 69(2): 236-42.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.116.08436] [PMID: 27993955]
[9]
Long M, Huang Z, Zhuang X, et al. Association of inflammation and endothelial dysfunction with coronary microvascular resistance in patients with cardiac syndrome X. Arq Bras Cardiol 2017; 109(5): 397-403.
[http://dx.doi.org/10.5935/abc.20170149] [PMID: 29069202]
[10]
Ridker PM, Everett BM, Thuren T, et al. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med 2017; 377(12): 1119-31.
[http://dx.doi.org/10.1056/NEJMoa1707914] [PMID: 28845751]
[11]
Tardif JC, Kouz S, Waters DD, et al. Efficacy and safety of low- dose colchicine after myocardial infarction. N Engl J Med 2019; 381(26): 2497-505.
[http://dx.doi.org/10.1056/NEJMoa1912388] [PMID: 31733140]
[12]
Chilian WM. Coronary microcirculation in health and disease. Summary of an NHLBI workshop. Circulation 1997; 95(2): 522-8.
[http://dx.doi.org/10.1161/01.CIR.95.2.522] [PMID: 9008472]
[13]
Jones CJ, Kuo L, Davis MJ, Chilian WM. Regulation of coronary blood flow: Coordination of heterogeneous control mechanisms in vascular microdomains. Cardiovasc Res 1995; 29(5): 585-96.
[http://dx.doi.org/10.1016/S0008-6363(96)88626-3] [PMID: 7606744]
[14]
Pries AR, Badimon L, Bugiardini R, et al. Coronary vascular regulation, remodelling, and collateralization: Mechanisms and clinical implications on behalf of the working group on coronary pathophysiology and microcirculation. Eur Heart J 2015; 36(45): 3134-46.
[http://dx.doi.org/10.1093/eurheartj/ehv100] [PMID: 26112888]
[15]
Crea F, Camici PG, Bairey Merz CN. Coronary microvascular dysfunction: An update. Eur Heart J 2014; 35(17): 1101-11.
[http://dx.doi.org/10.1093/eurheartj/eht513] [PMID: 24366916]
[16]
Taqueti VR, Di Carli MF. Coronary microvascular disease pathogenic mechanisms and therapeutic options: JACC state-of-the-art review. J Am Coll Cardiol 2018; 72(21): 2625-41.
[http://dx.doi.org/10.1016/j.jacc.2018.09.042] [PMID: 30466521]
[17]
Spoladore R, Fisicaro A, Faccini A, Camici PG. Coronary microvascular dysfunction in primary cardiomyopathies. Heart 2014; 100(10): 806-13.
[http://dx.doi.org/10.1136/heartjnl-2013-304291] [PMID: 23904360]
[18]
Shimokawa H, Suda A, Takahashi J, et al. Clinical characteristics and prognosis of patients with microvascular angina: An international and prospective cohort study by the Coronary Vasomotor Disorders International Study (COVADIS) Group. Eur Heart J 2021; ehab282.
[http://dx.doi.org/10.1093/eurheartj/ehab282] [PMID: 34038937]
[19]
Hage C, Michaëlsson E, Kull B, et al. Myeloperoxidase and related biomarkers are suggestive footprints of endothelial microvascular inflammation in HFpEF patients. ESC Heart Fail 2020; 7(4): 1534-46.
[http://dx.doi.org/10.1002/ehf2.12700] [PMID: 32424988]
[20]
Feher A, Broskova Z, Bagi Z. Age-related impairment of conducted dilation in human coronary arterioles. Am J Physiol Heart Circ Physiol 2014; 306(12): H1595-601.
[http://dx.doi.org/10.1152/ajpheart.00179.2014] [PMID: 24778172]
[21]
van de Hoef TP, Echavarria-Pinto M, Meuwissen M, Stegehuis VE, Escaned J, Piek JJ. Contribution of age-related microvascular dysfunction to abnormal coronary: Hemodynamics in patients with ischemic heart disease. JACC Cardiovasc Interv 2020; 13(1): 20-9.
[http://dx.doi.org/10.1016/j.jcin.2019.08.052] [PMID: 31918939]
[22]
Pirmohamed A, Kitzman DW, Maurer MS. Heart failure in older adults: Embracing complexity. J Geriatr Cardiol 2016; 13(1): 8-14.
[PMID: 26918007]
[23]
Conceição G, Heinonen I, Lourenço AP, Duncker DJ, Falcão-Pires I. Animal models of heart failure with preserved ejection fraction. Neth Heart J 2016; 24(4): 275-86.
[http://dx.doi.org/10.1007/s12471-016-0815-9] [PMID: 26936157]
[24]
Munagala VK, Hart CY, Burnett JC Jr, Meyer DM, Redfield MM. Ventricular structure and function in aged dogs with renal hypertension: A model of experimental diastolic heart failure. Circulation 2005; 111(9): 1128-35.
[http://dx.doi.org/10.1161/01.CIR.0000157183.21404.63] [PMID: 15723971]
[25]
Davila A, Tian Y, Czikora I, et al. Adenosine kinase inhibition augments conducted vasodilation and prevents left ventricle diastolic dysfunction in heart failure with preserved ejection fraction. Circ Heart Fail 2019; 12(8): e005762.
[http://dx.doi.org/10.1161/CIRCHEARTFAILURE.118.005762] [PMID: 31525084]
[26]
Dou H, Feher A, Davila AC, et al. Role of adipose tissue endothelial ADAM17 in age-related coronary microvascular dysfunction. Arterioscler Thromb Vasc Biol 2017; 37(6): 1180-93.
[http://dx.doi.org/10.1161/ATVBAHA.117.309430] [PMID: 28473444]
[27]
Cassuto J, Dou H, Czikora I, et al. Peroxynitrite disrupts endothelial caveolae leading to eNOS uncoupling and diminished flow- mediated dilation in coronary arterioles of diabetic patients. Diabetes 2014; 63(4): 1381-93.
[http://dx.doi.org/10.2337/db13-0577] [PMID: 24353182]
[28]
Niccoli G, Scalone G, Lerman A, Crea F. Coronary microvascular obstruction in acute myocardial infarction. Eur Heart J 2016; 37(13): 1024-33.
[http://dx.doi.org/10.1093/eurheartj/ehv484] [PMID: 26364289]
[29]
Henderson KK, Turk JR, Rush JW, Laughlin MH. Endothelial function in coronary arterioles from pigs with early-stage coronary disease induced by high-fat, high-cholesterol diet: Effect of exercise. J Appl Physiol 2004; 97(3): 1159-68.
[http://dx.doi.org/10.1152/japplphysiol.00261.2004] [PMID: 15208294]
[30]
Redfield MM, Anstrom KJ, Levine JA, et al. Isosorbide mononitrate in heart failure with preserved ejection fraction. N Engl J Med 2015; 373(24): 2314-24.
[http://dx.doi.org/10.1056/NEJMoa1510774] [PMID: 26549714]
[31]
Redfield MM, Chen HH, Borlaug BA, et al. Effect of phosphodiesterase-5 inhibition on exercise capacity and clinical status in heart failure with preserved ejection fraction: A randomized clinical trial. JAMA 2013; 309(12): 1268-77.
[http://dx.doi.org/10.1001/jama.2013.2024] [PMID: 23478662]
[32]
Shah SJ, Voors AA, McMurray JJV, et al. Effect of neladenoson bialanate on exercise capacity among patients with heart failure with preserved ejection fraction: A randomized clinical trial. JAMA 2019; 321(21): 2101-12.
[http://dx.doi.org/10.1001/jama.2019.6717] [PMID: 31162568]
[33]
Miura H, Bosnjak JJ, Ning G, Saito T, Miura M, Gutterman DD. Role for hydrogen peroxide in flow-induced dilation of human coronary arterioles. Circ Res 2003; 92(2): e31-40.
[http://dx.doi.org/10.1161/01.RES.0000054200.44505.AB] [PMID: 12574154]
[34]
Szerafin T, Erdei N, Fülöp T, et al. Increased cyclooxygenase-2 expression and prostaglandin-mediated dilation in coronary arterioles of patients with diabetes mellitus. Circ Res 2006; 99(5): e12-7.
[http://dx.doi.org/10.1161/01.RES.0000241051.83067.62] [PMID: 16917094]
[35]
Ohta M, Toyama K, Gutterman DD, et al. Ecto-5′-nucleotidase, CD73, is an endothelium-derived hyperpolarizing factor synthase. Arterioscler Thromb Vasc Biol 2013; 33(3): 629-36.
[http://dx.doi.org/10.1161/ATVBAHA.112.300600] [PMID: 23288168]
[36]
Félétou M, Vanhoutte PM. Endothelium-derived hyperpolarizing factor: Where are we now? Arterioscler Thromb Vasc Biol 2006; 26(6): 1215-25.
[http://dx.doi.org/10.1161/01.ATV.0000217611.81085.c5] [PMID: 16543495]
[37]
Fukuta H, Goto T, Wakami K, Kamiya T, Ohte N. Effect of renin-angiotensin system inhibition on cardiac structure and function and exercise capacity in heart failure with preserved ejection fraction: A meta-analysis of randomized controlled trials. Heart Fail Rev 2020.
[http://dx.doi.org/10.1007/s10741-020-09969-1] [PMID: 32562021]
[38]
Solomon SD, Claggett B, Desai AS, et al. Influence of ejection fraction on outcomes and efficacy of sacubitril/valsartan (LCZ696) in heart failure with reduced ejection fraction: The prospective comparison of ARNI with ACEI to determine impact on global mortality and morbidity in heart failure (PARADIGM-HF) trial. Circ Heart Fail 2016; 9(3): e002744.
[http://dx.doi.org/10.1161/CIRCHEARTFAILURE.115.002744] [PMID: 26915374]
[39]
McMurray JJV, Jackson AM, Lam CSP, et al. Effects of sacubitril-valsartan versus valsartan in women compared with men with heart failure and preserved ejection fraction: Insights from PARAGON-HF. Circulation 2020; 141(5): 338-51.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.119.044491] [PMID: 31736337]
[40]
Solomon SD, Vaduganathan M, L Claggett B, et al. Sacubitril/valsartan across the spectrum of ejection fraction in heart failure. Circulation 2020; 141(5): 352-61.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.119.044586] [PMID: 31736342]
[41]
Valero-Munoz M, Li S, Wilson RM, Boldbaatar B, Iglarz M, Sam F. Dual endothelin-A/endothelin-B receptor blockade and cardiac remodeling in heart failure with preserved ejection fraction. Circ Heart Fail 2016; 9(11): e003381.
[http://dx.doi.org/10.1161/CIRCHEARTFAILURE.116.003381] [PMID: 27810862]
[42]
Zile MR, Bourge RC, Redfield MM, Zhou D, Baicu CF, Little WC. Randomized, double-blind, placebo-controlled study of sitaxsentan to improve impaired exercise tolerance in patients with heart failure and a preserved ejection fraction. JACC Heart Fail 2014; 2(2): 123-30.
[http://dx.doi.org/10.1016/j.jchf.2013.12.002] [PMID: 24720918]
[43]
Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation 2002; 105(9): 1135-43.
[http://dx.doi.org/10.1161/hc0902.104353] [PMID: 11877368]
[44]
Gonzalez MA, Selwyn AP. Endothelial function, inflammation, and prognosis in cardiovascular disease. Am J Med 2003; 115(Suppl. 8A): 99S-106S.
[http://dx.doi.org/10.1016/j.amjmed.2003.09.016] [PMID: 14678874]
[45]
Vasan RS, Sullivan LM, Roubenoff R, et al. Inflammatory markers and risk of heart failure in elderly subjects without prior myocardial infarction: The Framingham Heart Study. Circulation 2003; 107(11): 1486-91.
[http://dx.doi.org/10.1161/01.CIR.0000057810.48709.F6] [PMID: 12654604]
[46]
Crea F, Libby P. Acute coronary syndromes: The way forward from mechanisms to precision treatment. Circulation 2017; 136(12): 1155-66.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.117.029870] [PMID: 28923905]
[47]
Harrington RA. Targeting inflammation in coronary artery disease. N Engl J Med 2017; 377(12): 1197-8.
[http://dx.doi.org/10.1056/NEJMe1709904] [PMID: 28844177]
[48]
Zanatta E, Colombo C, D’Amico G, d’Humières T, Dal Lin C, Tona F. Inflammation and coronary microvascular dysfunction in autoimmune rheumatic diseases. Int J Mol Sci 2019; 20(22): E5563.
[http://dx.doi.org/10.3390/ijms20225563] [PMID: 31703406]
[49]
Vaccarino V, Khan D, Votaw J, et al. Inflammation is related to coronary flow reserve detected by positron emission tomography in asymptomatic male twins. J Am Coll Cardiol 2011; 57(11): 1271-9.
[http://dx.doi.org/10.1016/j.jacc.2010.09.074] [PMID: 21392641]
[50]
Suhrs HE, Schroder J, Bové KB, et al. Inflammation, non-endothelial dependent coronary microvascular function and diastolic function-Are they linked? PLoS One 2020; 15(7): e0236035.
[http://dx.doi.org/10.1371/journal.pone.0236035] [PMID: 32673354]
[51]
Taqueti VR, Ridker PM. Inflammation, coronary flow reserve, and microvascular dysfunction: Moving beyond cardiac syndrome X. JACC Cardiovasc Imaging 2013; 6(6): 668-71.
[http://dx.doi.org/10.1016/j.jcmg.2013.02.005] [PMID: 23764095]
[52]
Ter Maaten JM, Damman K, Verhaar MC, et al. Connecting heart failure with preserved ejection fraction and renal dysfunction: The role of endothelial dysfunction and inflammation. Eur J Heart Fail 2016; 18(6): 588-98.
[http://dx.doi.org/10.1002/ejhf.497] [PMID: 26861140]
[53]
Kuruvilla S, Kramer CM. Coronary microvascular dysfunction in women: An overview of diagnostic strategies. Expert Rev Cardiovasc Ther 2013; 11(11): 1515-25.
[http://dx.doi.org/10.1586/14779072.2013.833854] [PMID: 24160578]
[54]
DuBrock HM, AbouEzzeddine OF, Redfield MM. High-sensitivity C-reactive protein in heart failure with preserved ejection fraction. PLoS One 2018; 13(8): e0201836.
[http://dx.doi.org/10.1371/journal.pone.0201836] [PMID: 30114262]
[55]
Gallet R, de Couto G, Simsolo E, et al. Cardiosphere-derived cells reverse heart failure with preserved ejection fraction (HFpEF) in rats by decreasing fibrosis and inflammation. JACC Basic Transl Sci 2016; 1(1-2): 14-28.
[http://dx.doi.org/10.1016/j.jacbts.2016.01.003] [PMID: 27104217]
[56]
Packer M, Lam CSP, Lund LH, Maurer MS, Borlaug BA. Characterization of the inflammatory-metabolic phenotype of heart failure with a preserved ejection fraction: A hypothesis to explain influence of sex on the evolution and potential treatment of the disease. Eur J Heart Fail 2020; 22(9): 1551-67.
[http://dx.doi.org/10.1002/ejhf.1902] [PMID: 32441863]
[57]
Nguyen ITN, Brandt MM, van de Wouw J, et al. Both male and female obese ZSF1 rats develop cardiac dysfunction in obesity-induced heart failure with preserved ejection fraction. PLoS One 2020; 15(5): e0232399.
[http://dx.doi.org/10.1371/journal.pone.0232399] [PMID: 32374790]
[58]
van Heerebeek L, Hamdani N, Falcão-Pires I, et al. Low myocardial protein kinase G activity in heart failure with preserved ejection fraction. Circulation 2012; 126(7): 830-9.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.111.076075] [PMID: 22806632]
[59]
Westermann D, Lindner D, Kasner M, et al. Cardiac inflammation contributes to changes in the extracellular matrix in patients with heart failure and normal ejection fraction. Circ Heart Fail 2011; 4(1): 44-52.
[http://dx.doi.org/10.1161/CIRCHEARTFAILURE.109.931451] [PMID: 21075869]
[60]
Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: Role in cardiovascular biology and disease. Circ Res 2000; 86(5): 494-501.
[http://dx.doi.org/10.1161/01.RES.86.5.494] [PMID: 10720409]
[61]
Gao X, Belmadani S, Picchi A, et al. Tumor necrosis factor-alpha induces endothelial dysfunction in Lepr(db) mice. Circulation 2007; 115(2): 245-54.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.650671] [PMID: 17200442]
[62]
Muzaffar S, Jeremy JY, Angelini GD, Stuart-Smith K, Shukla N. Role of the endothelium and nitric oxide synthases in modulating superoxide formation induced by endotoxin and cytokines in porcine pulmonary arteries. Thorax 2003; 58(7): 598-604.
[http://dx.doi.org/10.1136/thorax.58.7.598] [PMID: 12832676]
[63]
Yang B, Rizzo V. TNF-alpha potentiates protein-tyrosine nitration through activation of NADPH oxidase and eNOS localized in membrane rafts and caveolae of bovine aortic endothelial cells. Am J Physiol Heart Circ Physiol 2007; 292(2): H954-62.
[http://dx.doi.org/10.1152/ajpheart.00758.2006] [PMID: 17028163]
[64]
Aoki N, Siegfried M, Lefer AM. Anti-EDRF effect of tumor necrosis factor in isolated, perfused cat carotid arteries. Am J Physiol 1989; 256(5 Pt 2): H1509-12.
[PMID: 2785770]
[65]
Czikora I, Alli A, Bao HF, et al. A novel tumor necrosis factor-mediated mechanism of direct epithelial sodium channel activation. Am J Respir Crit Care Med 2014; 190(5): 522-32.
[http://dx.doi.org/10.1164/rccm.201405-0833OC] [PMID: 25029038]
[66]
Myers PR, Wright TF, Tanner MA, Adams HR. EDRF and nitric oxide production in cultured endothelial cells: Direct inhibition by E. coli endotoxin. Am J Physiol 1992; 262(3 Pt 2): H710-8.
[PMID: 1558180]
[67]
Neumann P, Gertzberg N, Johnson A. TNF-alpha induces a decrease in eNOS promoter activity. Am J Physiol Lung Cell Mol Physiol 2004; 286(2): L452-9.
[http://dx.doi.org/10.1152/ajplung.00378.2002] [PMID: 14555463]
[68]
Seidel M, Billert H, Kurpisz M. Regulation of eNOS expression in HCAEC cell line treated with opioids and proinflammatory cytokines. Kardiol Pol 2006; 64(2): 153-8.
[PMID: 16502366]
[69]
Valerio A, Cardile A, Cozzi V, et al. TNF-alpha downregulates eNOS expression and mitochondrial biogenesis in fat and muscle of obese rodents. J Clin Invest 2006; 116(10): 2791-8.
[http://dx.doi.org/10.1172/JCI28570.] [PMID: 16981010]
[70]
Yan G, You B, Chen SP, Liao JK, Sun J. Tumor necrosis factor-alpha downregulates endothelial nitric oxide synthase mRNA stability via translation elongation factor 1-alpha 1. Circ Res 2008; 103(6): 591-7.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.173963] [PMID: 18688046]
[71]
Huang A, Yang YM, Feher A, Bagi Z, Kaley G, Sun D. Exacerbation of endothelial dysfunction during the progression of diabetes: Role of oxidative stress. Am J Physiol Regul Integr Comp Physiol 2012; 302(6): R674-81.
[http://dx.doi.org/10.1152/ajpregu.00699.2011] [PMID: 22262308]
[72]
Kennard S, Ruan L, Buffett RJ, Fulton D, Venema RC. TNFα reduces eNOS activity in endothelial cells through serine 116 phosphorylation and Pin1 binding: Confirmation of a direct, inhibitory interaction of Pin1 with eNOS. Vascul Pharmacol 2016; 81: 61-8.
[http://dx.doi.org/10.1016/j.vph.2016.04.003] [PMID: 27073025]
[73]
Kou R, Greif D, Michel T. Dephosphorylation of endothelial nitric-oxide synthase by vascular endothelial growth factor. Implications for the vascular responses to cyclosporin A. J Biol Chem 2002; 277(33): 29669-73.
[http://dx.doi.org/10.1074/jbc.M204519200] [PMID: 12050171]
[74]
Ruan L, Torres CM, Qian J, et al. Pin1 prolyl isomerase regulates endothelial nitric oxide synthase. Arterioscler Thromb Vasc Biol 2011; 31(2): 392-8.
[http://dx.doi.org/10.1161/ATVBAHA.110.213181] [PMID: 21051667]
[75]
Misra S, Hascall VC, Markwald RR, Ghatak S. Interactions between hyaluronan and its receptors (CD44, RHAMM) regulate the activities of inflammation and cancer. Front Immunol 2015; 6: 201.
[http://dx.doi.org/10.3389/fimmu.2015.00201] [PMID: 25999946]
[76]
Farb A, Kolodgie FD, Hwang JY, et al. Extracellular matrix changes in stented human coronary arteries. Circulation 2004; 110(8): 940-7.
[http://dx.doi.org/10.1161/01.CIR.0000139337.56084.30] [PMID: 15302784]
[77]
Pedicino D, Vinci R, Giglio AF, et al. Alterations of hyaluronan metabolism in acute coronary syndrome: Implications for plaque erosion. J Am Coll Cardiol 2018; 72(13): 1490-503.
[http://dx.doi.org/10.1016/j.jacc.2018.06.072] [PMID: 30236312]
[78]
Slevin M, Krupinski J, Gaffney J, et al. Hyaluronan-mediated angiogenesis in vascular disease: Uncovering RHAMM and CD44 receptor signaling pathways. Matrix Biol 2007; 26(1): 58-68.
[http://dx.doi.org/10.1016/j.matbio.2006.08.261] [PMID: 17055233]
[79]
Litwiniuk M, Krejner A, Speyrer MS, Gauto AR, Grzela T. Hyaluronic acid in inflammation and tissue regeneration. Wounds 2016; 28(3): 78-88.
[PMID: 26978861]
[80]
Jordan AR, Racine RR, Hennig MJ, Lokeshwar VB. The role of CD44 in disease pathophysiology and targeted treatment. Front Immunol 2015; 6: 182.
[http://dx.doi.org/10.3389/fimmu.2015.00182] [PMID: 25954275]
[81]
Krolikoski M, Monslow J, Puré E. The CD44-HA axis and inflammation in atherosclerosis: A temporal perspective. Matrix Biol 2019; 78-79: 201-18.
[http://dx.doi.org/10.1016/j.matbio.2018.05.007] [PMID: 29792915]
[82]
Suwannakul N, Ma N, Thanan R, et al. Overexpression of CD44 variant 9: A novel cancer stem cell marker in human cholangiocarcinoma in relation to inflammation. Mediators Inflamm 2018; 2018: 4867234.
[http://dx.doi.org/10.1155/2018/4867234] [PMID: 30402042]
[83]
Wittig B, Seiter S, Schmidt DS, Zuber M, Neurath M, Zöller M. CD44 variant isoforms on blood leukocytes in chronic inflammatory bowel disease and other systemic autoimmune diseases. Lab Invest 1999; 79(6): 747-59.
[PMID: 10378517]
[84]
Suleiman M, Abdulrahman N, Yalcin H, Mraiche F. The role of CD44, hyaluronan and NHE1 in cardiac remodeling. Life Sci 2018; 209: 197-201.
[http://dx.doi.org/10.1016/j.lfs.2018.08.009] [PMID: 30089233]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy