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Perivascular inflammatory cells and their association with pulmonary arterial remodelling in dogs with pulmonary hypertension due to myxomatous mitral valve disease

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Abstract

Pulmonary hypertension (PH), an increase in pulmonary arterial pressure (PAP), may occur in dogs affected with myxomatous mitral valve disease (MMVD). Recent studies suggest that an accumulation of perivascular inflammatory cells may be involved with medial thickening which is a sign of the pulmonary artery remodelling in PH. The aim of this study was to characterise perivascular inflammatory cells in the surrounding pulmonary arteries of dogs with PH due to MMVD compared to MMVD dogs and healthy control dogs. Nineteen lung samples were collected from cadavers of small-breed dogs (control n = 5; MMVD n = 7; MMVD + PH n = 7). Toluidine blue stain and multiple IHC targeting α-SMA, vWF, CD20, CD68 and CD3 was performed to examine intimal and medial thickening, assess muscularisation of the small pulmonary arteries and characterise perivascular leucocytes. Medial thickening without intimal thickening of pulmonary arteries and muscularisation of normally non-muscularised small pulmonary arteries was observed in the MMVD and MMVD + PH groups compared with the control group. The perivascular numbers of B lymphocytes, T lymphocytes and macrophages was significantly increased in the MMVD + PH group compared with the MMVD and control groups. In contrast, the perivascular number of mast cells was significantly higher in the MMVD group compared with the MMVD + PH and control groups. This study suggested that pulmonary artery remodelling as medial thickening and muscularisation of the normally non-muscular small pulmonary arteries is accompanied by the accumulation of perivascular inflammatory cells.

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The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Abid S, Marcos E, Parpaleix A, Amsellem V, Breau M, Houssaini A, Vienney N, Lefevre M, Derumeaux G, Evans S, Hubeau C, Delcroix M, Quarck R, Adnot S, Lipskaia L (2019) CCR2/CCR5-mediated macrophage-smoothmuscle cell crosstalk in pulmonary hypertension. Eur Respir J 54:1802308

    PubMed  Google Scholar 

  • IA Akers M Parsons MR Hill MD Hollenberg S Sanjar GJ Laurent 2000 Mast cell tryptase stimulates human lung fibroblast proliferation via protease-activated receptor-2 Am J Physiol Lung Cell Mol Physiol 278 L193 201

    CAS  PubMed  Google Scholar 

  • V Amsellem S Abid L Poupel A Parpaleix M Rodero G Gary-Bobo 2017 Roles for the CX3CL1/CX3CR1 and CCL2/CCR2 Chemokine Systems in Hypoxic Pulmonary Hypertension Am J Respir Cell Mol Biol 56 597 608

    CAS  PubMed  Google Scholar 

  • L Bacakova M Travnickova E Filova R Matějka J Stepanovska J Musilkova 2018 The role of vascular smooth muscle cells in the physiology and pathophysiology of blood vessels K Sakuma Eds Muscle Cell and Tissue Current Status of Research Field IntechOpen UK 229 257

    Google Scholar 

  • Y Bai HM Wang M Liu Y Wang GC Lian XH Zhang 2014 4-Chloro-DL-phenylalanine protects against monocrotaline-induced pulmonary vascular remodeling and lung inflammation Int J Mol Med 33 373 382

    CAS  PubMed  Google Scholar 

  • A Baňasová H Maxová V Hampl M Vízek V Povýšilová J Novotná 2008 Prevention of Mast Cell Degranulation by Disodium Cromoglycate Attenuates the Development of Hypoxic Pulmonary Hypertension in Rats Exposed to Chronic Hypoxia Respiration 76 102 107

    PubMed  Google Scholar 

  • B Bartelds RLE Loon Van S Mohaupt H Wijnberg MG Dickinson B Boersma 2012 Mast cell inhibition improves pulmonary vascular remodeling in pulmonary hypertension Chest 141 651 660

    CAS  PubMed  Google Scholar 

  • MO Becker A Kill M Kutsche J Guenther A Rose C Tabeling 2014 Vascular receptor autoantibodies in pulmonary arterial hypertension associated with systemic sclerosis Am J Respir Crit Care Med 190 808 817

    CAS  PubMed  Google Scholar 

  • M Borgarelli J Abbott L Braz-Ruivo D Chiavegato S Crosara K Lamb 2015 Prevalence and prognostic importance of pulmonary hypertension in dogs with myxomatous mitral valve disease J Vet Intern Med 29 569 574

    CAS  PubMed  PubMed Central  Google Scholar 

  • M Borgarelli E Zini G D'agnolo A Tarducci RA Santilli D Chiavegato 2004 Comparison of primary mitral valve disease in German Shepherd dogs and in small breeds J Vet Cardiol 6 27 34

    PubMed  Google Scholar 

  • S Breitling Z Hui D Zabini Y Hu J Hoffmann NM Goldenberg 2017 The mast cell-B cell axis in lung vascular remodeling and pulmonary hypertension Am J Physiol Lung Cell Mol Physiol 312 L710 l721

    PubMed  Google Scholar 

  • S Bulfone-Paus R Bahri 2015 Mast Cells as Regulators of T Cell Responses Front Immunol 6 394

    PubMed  PubMed Central  Google Scholar 

  • G Bussone MC Tamby C Calzas N Kherbeck Y Sahbatou C Sanson 2012 IgG from patients with pulmonary arterial hypertension and/or systemic sclerosis binds to vascular smooth muscle cells and induces cell contraction Ann Rheum Dis 71 596 605

    CAS  PubMed  Google Scholar 

  • E Caglayan M Trappiel A Behringer EM Berghausen M Odenthal E Wellnhofer 2019 Pulmonary arterial remodelling by deficiency of peroxisome proliferator-activated receptor-γ in murine vascular smooth muscle cells occurs independently of obesity-related pulmonary hypertension Respir Res 20 42

    PubMed  PubMed Central  Google Scholar 

  • JL Caswell, KJ Williams (2016) Respiratory System. In: Maxie MG, Saunders WB (eds) Jubb, Kennedy and Palmer's Pathology of Domestic Animals: Volume 2, 6th edn. pp 465–591

  • JP Chandler TJ Yang 1981 Identification of canine lymphocyte populations by immunofluorescence surface marker analysis Int Arch Allergy Appl Immunol 65 62 68

    CAS  PubMed  Google Scholar 

  • I Chazova I Robbins J Loyd J Newman V Tapson V Zhdaov 2000 Venous and arterial changes in pulmonary veno-occlusive disease, mitral stenosis and fibrosing mediastinitis Eur Respir J 15 116 122

    CAS  PubMed  Google Scholar 

  • S Chen D Yan A Qiu 2020 The role of macrophages in pulmonary hypertension: Pathogenesis and targeting Int Immunopharmacol 88 106934

    CAS  PubMed  Google Scholar 

  • D Chiavegato M Borgarelli G D'agnolo RA Santilli 2009 Pulmonary hypertension in dogs with mitral regurgitation attributable to myxomatous valve disease Vet Radiol Ultrasound 50 253 258

    PubMed  Google Scholar 

  • P Clark DE Normansell DJ Innes CE Hess 1986 Lymphocyte Subsets in Normal Bone Marrow Blood 67 1600 1606

    CAS  PubMed  Google Scholar 

  • KL Colvin PJ Cripe DD Ivy KR Stenmark ME Yeager 2013 Bronchus-associated lymphoid tissue in pulmonary hypertension produces pathologic autoantibodies Am J Respir Crit Care Med 188 1126 1136

    CAS  PubMed  PubMed Central  Google Scholar 

  • MJ Cuttica T Langenickel A Noguchi RF Machado MT Gladwin M Boehm 2011 Perivascular T-cell infiltration leads to sustained pulmonary artery remodeling after endothelial cell damage Am J Respir Cell Mol Biol 45 62 71

    CAS  PubMed  Google Scholar 

  • BK Dahal D Kosanovic C Kaulen T Cornitescu R Savai J Hoffmann 2011 Involvement of mast cells in monocrotaline-induced pulmonary hypertension in rats Respir Res 12 60

    CAS  PubMed  PubMed Central  Google Scholar 

  • JF Delgado E Conde V Sanchez F Lopez-Rios MA Gomez-Sanchez P Escribano 2005 Pulmonary vascular remodeling in pulmonary hypertension due to chronic heart failure Eur J Heart Fail 7 1011 1016

    PubMed  Google Scholar 

  • S Disatian EJ Ehrhart S Zimmerman EC Orton 2008 Interstitial cells from dogs with naturally occurring myxomatous mitral valve disease undergo phenotype transformation J Heart Valve Dis 17 402 411

    PubMed  Google Scholar 

  • S Disatian C Lacerda EC Orton 2010 Tryptophan hydroxylase 1 expression is increased in phenotype-altered canine and human degenerative myxomatous mitral valves J Heart Valve Dis 19 71 78

    PubMed  Google Scholar 

  • P Dorfmüller F Perros K Balabanian M Humbert 2003 Inflammation in pulmonary arterial hypertension Eur Respir J 22 358 363

    PubMed  Google Scholar 

  • J Florentin E Coppin SB Vasamsetti J Zhao YY Tai Y Tang 2018 Inflammatory Macrophage Expansion in Pulmonary Hypertension Depends upon Mobilization of Blood-Borne Monocytes J Immunol 200 3612 3625

    CAS  PubMed  Google Scholar 

  • MG Frid JA Brunetti DL Burke TC Carpenter NJ Davie JT Reeves 2006 Hypoxia-induced pulmonary vascular remodeling requires recruitment of circulating mesenchymal precursors of a monocyte/macrophage lineage Am J Pathol 168 659 669

    CAS  PubMed  PubMed Central  Google Scholar 

  • MG Frid BA Mckeon JM Thurman BA Maron M Li H Zhang 2020 Immunoglobulin-driven Complement Activation Regulates Proinflammatory Remodeling in Pulmonary Hypertension Am J Respir Crit Care Med 201 224 239

    CAS  PubMed  PubMed Central  Google Scholar 

  • C Gerges M Gerges MB Lang Y Zhang J Jakowitsch P Probst 2013 Diastolic pulmonary vascular pressure gradient: a predictor of prognosis in "out-of-proportion" pulmonary hypertension Chest 143 758 766

    PubMed  Google Scholar 

  • M-R Ghigna P Dorfmüller 2019 Pulmonary vascular disease and pulmonary hypertension Diagn Histopathol 25 304 312

    Google Scholar 

  • M Guazzi N Galiè 2012 Pulmonary hypertension in left heart disease Eur Respir Rev 21 338 346

    PubMed  PubMed Central  Google Scholar 

  • C Guglielmini C Civitella A Diana M Tommaso Di M Cipone A Luciani 2010 Serum cardiac troponin I concentration in dogs with precapillary and postcapillary pulmonary hypertension J Vet Intern Med 24 145 152

    CAS  PubMed  Google Scholar 

  • C Guignabert P Dorfmuller 2013 Pathology and pathobiology of pulmonary hypertension Semin Respir Crit Care Med 34 551 559

    PubMed  Google Scholar 

  • J Hoffmann J Yin M Kukucka N Yin I Saarikko A Sterner-Kock 2011 Mast cells promote lung vascular remodelling in pulmonary hypertension Eur Respir J 37 1400 1410

    CAS  PubMed  Google Scholar 

  • Y Hu L Chi WM Kuebler NM Goldenberg 2020 Perivascular Inflammation in Pulmonary Arterial Hypertension Cells 9 2338

    CAS  PubMed  PubMed Central  Google Scholar 

  • M Humbert C Guignabert S Bonnet P Dorfmüller JR Klinger MR Nicolls 2019 Pathology and pathobiology of pulmonary hypertension: state of the art and research perspectives Eur Respir J 53 1801887

    CAS  PubMed  PubMed Central  Google Scholar 

  • JM Hunt B Bethea X Liu A Gandjeva PPA Mammen E Stacher 2013 Pulmonary veins in the normal lung and pulmonary hypertension due to left heart disease Am J Physiol Lung Cell Mol Physiol 305 L725 L736

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Jennings C Premanandan 2017 Veterinary Histology Ohio State University Libraries

    Google Scholar 

  • BW Keene CE Atkins JD Bonagura PR Fox J Häggström VL Fuentes 2019 ACVIM consensus guidelines for the diagnosis and treatment of myxomatous mitral valve disease in dogs J Vet Intern Med 33 1127 1140

    PubMed  PubMed Central  Google Scholar 

  • HB Kellihan RL Stepien 2010 Pulmonary hypertension in dogs: diagnosis and therapy Vet Clin North Am Small Anim Pract 40 623 641

    PubMed  Google Scholar 

  • HB Kellihan RL Stepien 2012 Pulmonary hypertension in canine degenerative mitral valve disease J Vet Cardiol 14 149 164

    PubMed  Google Scholar 

  • WM Kuebler S Bonnet A Tabuchi 2018 Inflammation and autoimmunity in pulmonary hypertension: is there a role for endothelial adhesion molecules? (2017 Grover Conference Series) Pulm Circ 8 2045893218757596 2045893218757596

    PubMed  PubMed Central  Google Scholar 

  • K Kurakula VFED Smolders O Tura-Ceide JW Jukema PHA Quax M-J Goumans 2021 Endothelial Dysfunction in Pulmonary Hypertension: Cause or Consequence? Biomedicines 9 57

    CAS  PubMed  PubMed Central  Google Scholar 

  • G Kwapiszewska P Markart BK Dahal B Kojonazarov LM Marsh RT Schermuly 2012 PAR-2 Inhibition Reverses Experimental Pulmonary Hypertension Circ Res 110 1179 1191

    CAS  PubMed  Google Scholar 

  • M Lévy C Maurey DS Celermajer PR Vouhé C Danel D Bonnet 2007 Impaired Apoptosis of Pulmonary Endothelial Cells Is Associated With Intimal Proliferation and Irreversibility of Pulmonary Hypertension in Congenital Heart Disease J Am Coll Cardiol 49 803 810

    PubMed  Google Scholar 

  • C Li J Feng L Cai Li M Yan W Ying Wei F Jing 2016 Muscularization of Pulmonary Artery and RhoA/ROCK levels in Rats Exposed to Intermittent Hypoxia Int J Clin Exp Pathol 9 10139 10148

    CAS  Google Scholar 

  • M Li SR Riddle MG Frid KC Kasmi El TA Mckinsey RJ Sokol 2011 Emergence of fibroblasts with a proinflammatory epigenetically altered phenotype in severe hypoxic pulmonary hypertension J Immunol 187 2711 2722

    CAS  PubMed  Google Scholar 

  • M Liu Y Wang HM Wang Y Bai XH Zhang YX Sun 2013 Fluoxetine attenuates chronic methamphetamine-induced pulmonary arterial remodelling: possible involvement of serotonin transporter and serotonin 1B receptor Basic Clin Pharmacol Toxicol 112 77 82

    CAS  PubMed  Google Scholar 

  • R Mathew R (2020) Endothelial Dysfunction and Disruption in Pulmonary Hypertension. In: Abukabda A, Suciu M, Andor MM (eds) Cardiovascular Risk Factors in Pathology. IntechOpen, pp 92177

  • H Maxová M Vasilková J Novotná O Vajnerová A Bansová M Vízek 2010 Prevention of mast cell degranulation by disodium cromoglycate delayed the regression of hypoxic pulmonary hypertension in rats Respiration 80 335 339

    PubMed  Google Scholar 

  • C Medrek F Pontén K Jirström K Leandersson 2012 The presence of tumor associated macrophages in tumor stroma as a prognostic marker for breast cancer patients BMC Cancer 12 306

    CAS  PubMed  PubMed Central  Google Scholar 

  • D Montani F Perros N Gambaryan B Girerd P Dorfmuller LC Price 2011 C-kit-positive cells accumulate in remodeled vessels of idiopathic pulmonary arterial hypertension Am J Respir Crit Care Med 184 116 123

    PubMed  Google Scholar 

  • DL Moraes WS Colucci MM Givertz 2000 Secondary pulmonary hypertension in chronic heart failure: the role of the endothelium in pathophysiology and management Circulation 102 1718 1723

    CAS  PubMed  Google Scholar 

  • M Muñoz-Esquerre M López-Sánchez I Escobar D Huertas R Penín M Molina-Molina 2016 Systemic and pulmonary vascular remodelling in chronic obstructive pulmonary disease PLOS ONE 11 e0152987

    PubMed  PubMed Central  Google Scholar 

  • H Patel M Desai EM Tuzcu B Griffin S Kapadia 2014 Pulmonary hypertension in mitral regurgitation J Am Heart Assoc 3 e000748

    PubMed  PubMed Central  Google Scholar 

  • F Perros P Dorfmüller D Montani H Hammad W Waelput B Girerd 2012 Pulmonary lymphoid neogenesis in idiopathic pulmonary arterial hypertension Am J Respir Crit Care Med 185 311 321

    PubMed  Google Scholar 

  • RF Pinto L Higuchi Mde VD Aiello 2004 Decreased numbers of T-lymphocytes and predominance of recently recruited macrophages in the walls of peripheral pulmonary arteries from 26 patients with pulmonary hypertension secondary to congenital cardiac shunts Cardiovasc Pathol 13 268 275

    PubMed  Google Scholar 

  • LC Price SJ Wort F Perros P Dorfmüller A Huertas D Montani 2012 Inflammation in pulmonary arterial hypertension Chest 141 210 221

    PubMed  Google Scholar 

  • SC Pugliese S Kumar WJ Janssen BB Graham MG Frid SR Riddle 2017 A Time- and Compartment-Specific Activation of Lung Macrophages in Hypoxic Pulmonary Hypertension J Immunol 198 4802 4812

    CAS  PubMed  Google Scholar 

  • TR Quinlan D Li VE Laubach EG Shesely N Zhou RA Johns 2000 eNOS-deficient mice show reduced pulmonary vascular proliferation and remodeling to chronic hypoxia Am J Physiol Lung Cell Mol Physiol 279 L641 650

    CAS  PubMed  Google Scholar 

  • M Rabinovitch C Guignabert M Humbert MR Nicolls 2014 Inflammation and immunity in the pathogenesis of pulmonary arterial hypertension Circ Res 115 165 175

    CAS  PubMed  PubMed Central  Google Scholar 

  • B Ranchoux LD Harvey RJ Ayon A Babicheva S Bonnet SY Chan 2018 Endothelial dysfunction in pulmonary arterial hypertension: an evolving landscape (2017 Grover Conference Series) Pulm Circ 8 2045893217752912

    PubMed  Google Scholar 

  • C Reinero LC Visser HB Kellihan I Masseau E Rozanski C Clercx 2020 ACVIM consensus statement guidelines for the diagnosis, classification, treatment, and monitoring of pulmonary hypertension in dogs J Vet Intern Med 34 549 573

    PubMed  PubMed Central  Google Scholar 

  • S Sakarin A Rungsipipat SD Surachetpong 2021 Histopathological changes of pulmonary vascular remodeling in dogs affected with pulmonary hypertension secondary to degenerative mitral valve disease J Vet Cardiol 36 141 152

    CAS  PubMed  Google Scholar 

  • R Savai SS Pullamsetti J Kolbe E Bieniek R Voswinckel L Fink 2012 Immune and inflammatory cell involvement in the pathology of idiopathic pulmonary arterial hypertension Am J Respir Crit Care Med 186 897 908

    CAS  PubMed  Google Scholar 

  • RT Schermuly KP Kreisselmeier HA Ghofrani A Samidurai S Pullamsetti N Weissmann 2004 Antiremodeling effects of iloprost and the dual-selective phosphodiesterase 3/4 inhibitor tolafentrine in chronic experimental pulmonary hypertension Circ Res 94 1101 1108

    CAS  PubMed  Google Scholar 

  • KE Schober TM Hart JA Stern X Li VF Samii LJ Zekas 2010 Detection of congestive heart failure in dogs by Doppler echocardiography J Vet Intern Med 24 1358 1368

    CAS  PubMed  Google Scholar 

  • FJ Serres V Chetboul R Tissier C Carlos Sampedrano V Gouni AP Nicolle 2006 Doppler echocardiography-derived evidence of pulmonary arterial hypertension in dogs with degenerative mitral valve disease: 86 cases (2001–2005) J Am Vet Med Assoc 229 1772 1778

    PubMed  Google Scholar 

  • Y Song L Coleman J Shi H Beppu K Sato K Walsh 2008 Inflammation, endothelial injury, and persistent pulmonary hypertension in heterozygous BMPR2-mutant mice Am J Physiol Heart Circ Physiol 295 H677 690

    CAS  PubMed  PubMed Central  Google Scholar 

  • S Standring 2020 Gray's Anatomy: The Anatomical Basis of Clinical Practice Elsevier

    Google Scholar 

  • L Taraseviciene-Stewart MR Nicolls D Kraskauskas R Scerbavicius N Burns C Cool 2007 Absence of T cells confers increased pulmonary arterial hypertension and vascular remodeling Am J Respir Crit Care Med 175 1280 1289

    CAS  PubMed  PubMed Central  Google Scholar 

  • MI Townsley 2012 Structure and composition of pulmonary arteries, capillaries, and veins Compr Physiol 2 675 709

    PubMed  PubMed Central  Google Scholar 

  • E Vergadi MS Chang C Lee OD Liang X Liu A Fernandez-Gonzalez 2011 Early macrophage recruitment and alternative activation are critical for the later development of hypoxia-induced pulmonary hypertension Circulation 123 1986 1995

    CAS  PubMed  PubMed Central  Google Scholar 

  • HL Wang LP Peng WJ Chen SH Tang BZ Sun CL Wang 2014 HMGB1 enhances smooth muscle cell proliferation and migration in pulmonary artery remodeling Int J Clin Exp Pathol 7 3836 3844

    CAS  PubMed  PubMed Central  Google Scholar 

  • PS Yang DH Kim YJ Lee SE Lee WJ Kang HJ Chang 2014 Glycyrrhizin, inhibitor of high mobility group box-1, attenuates monocrotaline-induced pulmonary hypertension and vascular remodeling in rats Respir Res 15 148

    PubMed  PubMed Central  Google Scholar 

  • IN Zelko J Zhu JD Ritzenthaler J Roman 2016 Pulmonary hypertension and vascular remodeling in mice exposed to crystalline silica Respir Res 17 160

    PubMed  PubMed Central  Google Scholar 

  • FG Zhai XH Zhang HL Wang 2009 Fluoxetine protects against monocrotaline-induced pulmonary arterial hypertension: potential roles of induction of apoptosis and upregulation of Kv1.5 channels in rats Clin Exp Pharmacol Physiol 36 850 856

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank all staff at the Department of Veterinary Pathology, Faculty of Veterinary Science, Chulalongkorn University, for their help in sample collection and laboratory facility support.

Funding

This research was funded by the 90th Anniversary of Chulalongkorn University Fund (Ratchadaphiseksomphot Endowment Fund) and the 100th Anniversary Chulalongkorn University Fund for Doctoral Scholarship.

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S.S. performed research, wrote original draft of the manuscript and prepared all tables and figures, S.S., S.D.S. and A.R. determined conceptualization, reviewed and edited the manuscript. S.D.S supervised all process of research and manuscript preparation. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Sirilak Disatian Surachetpong.

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Ethical review and approval were waived for this study due to the study was performed on donated cadavers.

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Sakarin, S., Rungsipipat, A. & Surachetpong, S.D. Perivascular inflammatory cells and their association with pulmonary arterial remodelling in dogs with pulmonary hypertension due to myxomatous mitral valve disease. Vet Res Commun 47, 1505–1521 (2023). https://doi.org/10.1007/s11259-023-10106-0

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