Inflammation in Pulmonary Arterial Hypertension.
Immune cells
Innate and adaptive immune response
Pulmonary arterial hypertension
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2021
2021
Historique:
entrez:
31
3
2021
pubmed:
1
4
2021
medline:
7
4
2021
Statut:
ppublish
Résumé
Pulmonary artery hypertension (PAH) is a devastating cardiopulmonary disease characterized by vascular remodeling and obliteration of the precapillary pulmonary arterioles. Alterations in the structure and function of pulmonary vessels result in the resistance of blood flow and can progress to right-sided heart failure, causing significant morbidity and mortality. There are several types of PAH, and the disease can be familial or secondary to an underlying medical condition such as a connective tissue disorder or infection. Regardless of the cause, the exact pathophysiology and cellular interactions responsible for disease development and progression are largely unknown.There is significant evidence to suggest altered immune and vascular cells directly participate in disease progression. Inflammation has long been hypothesized to play a vital role in the development of PAH, as an altered or skewed immune response favoring a proinflammatory environment that can lead to the infiltration of cells such as lymphocytes, macrophages, and neutrophils. Current treatment strategies focus on the dilation of partially occluded vessels; however, such techniques have not resulted in an effective strategy to reverse or prevent vascular remodeling. Therefore, current studies in human and animal models have attempted to understand the underlying pathophysiology of pulmonary hypertension (PH), specifically focusing on the inflammatory cascade predisposing patients to disease so that better therapeutic targets can be developed to potentially reverse or prevent disease progression.The purpose of this chapter is to provide a comprehensive review of the expanding literature on the inflammatory process that participates in PH development while highlighting important and current studies in both animal and human models. While our primary focus will be on cells found in the adaptive and innate immune system, we will review all potential causes of PAH, including cells of the endothelium, pulmonary lymphatics, and genetic mutations predisposing patients. In addition, we will discuss current therapeutic options while highlighting potential future treatments and the questions that still remain unanswered.
Identifiants
pubmed: 33788202
doi: 10.1007/978-3-030-63046-1_19
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
351-372Subventions
Organisme : NHLBI NIH HHS
ID : R01 HL150106
Pays : United States
Références
Tamosiuniene R, Nicolls MR. Regulatory T cells and pulmonary hypertension. Trends Cardiovasc Med. 2011;21:166–71.
pubmed: 22814424
pmcid: 3401377
doi: 10.1016/j.tcm.2012.05.004
Soon E, Holmes AM, Treacy CM, Doughty NJ, Southgate L, Machado RD, Trembath RC, Jennings S, Barker L, Nicklin P, Walker C, Budd DC, Pepke-Zaba J, Morrell NW. Elevated levels of inflammatory cytokines predict survival in idiopathic and familial pulmonary arterial hypertension. Circulation. 2010;122:920–7.
pubmed: 20713898
doi: 10.1161/CIRCULATIONAHA.109.933762
Cracowski JL, Chabot F, Labarere J, Faure P, Degano B, Schwebel C, Chaouat A, Reynaud-Gaubert M, Cracowski C, Sitbon O, Yaici A, Simonneau G, Humbert M. Proinflammatory cytokine levels are linked to death in pulmonary arterial hypertension. Eur Respir J. 2014;43:915–7.
pubmed: 24232704
doi: 10.1183/09031936.00151313
McKinley L, Logar AJ, McAllister F, Zheng M, Steele C, Kolls JK. Regulatory T cells dampen pulmonary inflammation and lung injury in an animal model of pneumocystis pneumonia. J Immunol. 2006;177:6215–26.
pubmed: 17056551
pmcid: 3912571
doi: 10.4049/jimmunol.177.9.6215
Mathai SC, Hassoun PM. Pulmonary arterial hypertension in connective tissue diseases. Heart Fail Clin. 2012;8:413–25.
pubmed: 22748903
pmcid: 3389609
doi: 10.1016/j.hfc.2012.04.001
Dib H, Tamby MC, Bussone G, Regent A, Berezne A, Lafine C, Broussard C, Simonneau G, Guillevin L, Witko-Sarsat V, Humbert M, Mouthon L. Targets of anti-endothelial cell antibodies in pulmonary hypertension and scleroderma. Eur Respir J. 2012;39:1405–14.
pubmed: 22005913
doi: 10.1183/09031936.00181410
Rawson AJ, Woske HM. A study of etiologic factors in so-called primary pulmonary hypertension. Arch Intern Med. 1960;105:233–43.
pubmed: 14436605
doi: 10.1001/archinte.1960.00270140055006
Isern RA, Yaneva M, Weiner E, Parke A, Rothfield N, Dantzker D, Rich S, Arnett FC. Autoantibodies in patients with primary pulmonary hypertension: association with anti-Ku. Am J Med. 1992;93:307–12.
pubmed: 1524083
doi: 10.1016/0002-9343(92)90238-7
Rich S, Kieras K, Hart K, Groves BM, Stobo JD, Brundage BH. Antinuclear antibodies in primary pulmonary hypertension. J Am Coll Cardiol. 1986;8:1307–11.
pubmed: 2431019
doi: 10.1016/S0735-1097(86)80301-1
Sakaguchi S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol. 2005;6:345–52.
pubmed: 15785760
doi: 10.1038/ni1178
pmcid: 15785760
Austin ED, Loyd JE. The genetics of pulmonary arterial hypertension. Circ Res. 2014;115:189–202.
pubmed: 24951767
pmcid: 4137413
doi: 10.1161/CIRCRESAHA.115.303404
Cao X, Cai SF, Fehniger TA, Song J, Collins LI, Piwnica-Worms DR, Ley TJ. Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity. 2007;27:635–46.
pubmed: 17919943
doi: 10.1016/j.immuni.2007.08.014
pmcid: 17919943
Sziksz E, Pap D, Lippai R, Beres NJ, Fekete A, Szabo AJ, Vannay A. Fibrosis related inflammatory mediators: role of the IL-10 cytokine family. Mediat Inflamm. 2015;2015:764641.
doi: 10.1155/2015/764641
Perry JSA, Lio CJ, Kau AL, Nutsch K, Yang Z, Gordon JI, Murphy KM, Hsieh CS. Distinct contributions of Aire and antigen-presenting-cell subsets to the generation of self-tolerance in the thymus. Immunity. 2014;41:414–26.
pubmed: 25220213
pmcid: 4175925
doi: 10.1016/j.immuni.2014.08.007
Qiu H, He Y, Ouyang F, Jiang P, Guo S, Guo Y. The role of regulatory T cells in pulmonary arterial hypertension. J Am Heart Assoc. 2019;8:e014201.
pubmed: 31771439
pmcid: 6912965
doi: 10.1161/JAHA.119.014201
Taraseviciene-Stewart L, Nicolls MR, Kraskauskas D, Scerbavicius R, Burns N, Cool C, Wood K, Parr JE, Boackle SA, Voelkel NF. Absence of T cells confers increased pulmonary arterial hypertension and vascular remodeling. Am J Respir Crit Care Med. 2007;175:1280–9.
pubmed: 17413127
pmcid: 2176089
doi: 10.1164/rccm.200608-1189OC
Tamosiuniene R, Tian W, Dhillon G, Wang L, Sung YK, Gera L, Patterson AJ, Agrawal R, Rabinovitch M, Ambler K, Long CS, Voelkel NF, Nicolls MR. Regulatory T cells limit vascular endothelial injury and prevent pulmonary hypertension. Circ Res. 2011;109:867–79.
pubmed: 21868697
pmcid: 3204361
doi: 10.1161/CIRCRESAHA.110.236927
Tamosiuniene R, Manouvakhova O, Mesange P, Saito T, Qian J, Sanyal M, Lin YC, Nguyen LP, Luria A, Tu AB, Sante JM, Rabinovitch M, Fitzgerald DJ, Graham BB, Habtezion A, Voelkel NF, Aurelian L, Nicolls MR. Dominant role for regulatory T cells in protecting females against pulmonary hypertension. Circ Res. 2018;122:1689–702.
pubmed: 29545367
pmcid: 5993601
doi: 10.1161/CIRCRESAHA.117.312058
Chu Y, Xiangli X, Xiao W. Regulatory T cells protect against hypoxia-induced pulmonary arterial hypertension in mice. Mol Med Rep. 2015;11:3181–7.
pubmed: 25523119
doi: 10.3892/mmr.2014.3106
pmcid: 25523119
Li C, Liu PP, Tang DD, Song R, Zhang YQ, Lei S, Wu SJ. Targeting the RhoA-ROCK pathway to regulate T-cell homeostasis in hypoxia-induced pulmonary arterial hypertension. Pulm Pharmacol Ther. 2018;50:111–22.
pubmed: 29673911
doi: 10.1016/j.pupt.2018.04.004
pmcid: 29673911
Voelkel NF, Tamosiuniene R, Nicolls MR. Challenges and opportunities in treating inflammation associated with pulmonary hypertension. Expert Rev Cardiovasc Ther. 2016;14:939–51.
pubmed: 27096622
pmcid: 5085832
doi: 10.1080/14779072.2016.1180976
Huertas A, Tu L, Gambaryan N, Girerd B, Perros F, Montani D, Fabre D, Fadel E, Eddahibi S, Cohen-Kaminsky S, Guignabert C, Humbert M. Leptin and regulatory T-lymphocytes in idiopathic pulmonary arterial hypertension. Eur Respir J. 2012;40:895–904.
pubmed: 22362850
doi: 10.1183/09031936.00159911
pmcid: 22362850
Peng X, Moore MW, Peng H, Sun H, Gan Y, Homer RJ, Herzog EL. CD4+CD25+FoxP3+ regulatory Tregs inhibit fibrocyte recruitment and fibrosis via suppression of FGF-9 production in the TGF-beta1 exposed murine lung. Front Pharmacol. 2014;5:80.
pubmed: 24904415
pmcid: 4032896
doi: 10.3389/fphar.2014.00080
MacDonald KP, Blazar BR, Hill GR. Cytokine mediators of chronic graft-versus-host disease. J Clin Invest. 2017;127:2452–63.
pubmed: 28665299
pmcid: 5490762
doi: 10.1172/JCI90593
Garibaldi BT, D'Alessio FR, Mock JR, Files DC, Chau E, Eto Y, Drummond MB, Aggarwal NR, Sidhaye V, King LS. Regulatory T cells reduce acute lung injury fibroproliferation by decreasing fibrocyte recruitment. Am J Respir Cell Mol Biol. 2013;48:35–43.
pubmed: 23002097
pmcid: 3547087
doi: 10.1165/rcmb.2012-0198OC
Cao Y, Xu W, Xiong S. Adoptive transfer of regulatory T cells protects against Coxsackievirus B3-induced cardiac fibrosis. PLoS One. 2013;8:e74955.
pubmed: 24023968
pmcid: 3762771
doi: 10.1371/journal.pone.0074955
Austin ED, Rock MT, Mosse CA, Vnencak-Jones CL, Yoder SM, Robbins IM, Loyd JE, Meyrick BO. T lymphocyte subset abnormalities in the blood and lung in pulmonary arterial hypertension. Respir Med. 2010;104:454–62.
pubmed: 19880300
doi: 10.1016/j.rmed.2009.10.004
pmcid: 19880300
Ulrich S, Nicolls MR, Taraseviciene L, Speich R, Voelkel N. Increased regulatory and decreased CD8+ cytotoxic T cells in the blood of patients with idiopathic pulmonary arterial hypertension. Respiration. 2008;75:272–80.
pubmed: 18025812
doi: 10.1159/000111548
Gaowa S, Zhou W, Yu L, Zhou X, Liao K, Yang K, Lu Z, Jiang H, Chen X. Effect of Th17 and Treg axis disorder on outcomes of pulmonary arterial hypertension in connective tissue diseases. Mediat Inflamm. 2014;2014:247372.
doi: 10.1155/2014/247372
Hautefort A, Girerd B, Montani D, Cohen-Kaminsky S, Price L, Lambrecht BN, Humbert M, Perros F. T-helper 17 cell polarization in pulmonary arterial hypertension. Chest. 2015;147:1610–20.
pubmed: 25429518
doi: 10.1378/chest.14-1678
pmcid: 25429518
Serezani CH, Kane S, Collins L, Morato-Marques M, Osterholzer JJ, Peters-Golden M. Macrophage dectin-1 expression is controlled by leukotriene B4 via a GM-CSF/PU.1 axis. J Immunol. 2012;189:906–15.
pubmed: 22696442
pmcid: 3392366
doi: 10.4049/jimmunol.1200257
Hashimoto-Kataoka T, Hosen N, Sonobe T, Arita Y, Yasui T, Masaki T, Minami M, Inagaki T, Miyagawa S, Sawa Y, Murakami M, Kumanogoh A, Yamauchi-Takihara K, Okumura M, Kishimoto T, Komuro I, Shirai M, Sakata Y, Nakaoka Y. Interleukin-6/interleukin-21 signaling axis is critical in the pathogenesis of pulmonary arterial hypertension. Proc Natl Acad Sci USA. 2015;112:E2677–86.
pubmed: 25941359
doi: 10.1073/pnas.1424774112
pmcid: 25941359
Maston LD, Jones DT, Giermakowska W, Howard TA, Cannon JL, Wang W, Wei Y, Xuan W, Resta TC, Gonzalez Bosc LV. Central role of T helper 17 cells in chronic hypoxia-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2017;312:L609–L24.
pubmed: 28213473
pmcid: 5451600
doi: 10.1152/ajplung.00531.2016
Kumar R, Mickael C, Kassa B, Sanders L, Koyanagi D, Hernandez-Saavedra D, Freeman S, Morales-Cano D, Cogolludo A, McKee AS, Fontenot AP, Butrous G, Tuder RM, Graham BB. Th2 CD4(+) T cells are necessary and sufficient for Schistosoma-pulmonary hypertension. J Am Heart Assoc. 2019;8:e013111.
pubmed: 31339057
pmcid: 6761627
Chen G, Zuo S, Tang J, Zuo C, Jia D, Liu Q, Liu G, Zhu Q, Wang Y, Zhang J, Shen Y, Chen D, Yuan P, Qin Z, Ruan C, Ye J, Wang X-J, Zhou Y, Gao P, Zhang P, Liu J, Jing Z-C, Lu A, Yu Y. Inhibition of CRTH2-mediated Th2 activation attenuates pulmonary hypertension in mice. J Exp Med. 2018;215:2175–95.
pubmed: 29970474
pmcid: 6080901
doi: 10.1084/jem.20171767
Wherry EJ. T cell exhaustion. Nat Immunol. 2011;12:492–9.
pubmed: 21739672
doi: 10.1038/ni.2035
pmcid: 21739672
Edwards AL, Gunningham SP, Clare GC, Hayman MW, Smith M, Frampton CM, Robinson BA, Troughton RW, Beckert LE. Professional killer cell deficiencies and decreased survival in pulmonary arterial hypertension. Respirology. 2013;18:1271–7.
pubmed: 23819819
doi: 10.1111/resp.12152
Ulrich S, Nicolls MR, Taraseviciene L, Speich R, Voelkel N. Increased regulatory and decreased CD8+ cytotoxic T cells in the blood of patients with idiopathic pulmonary arterial hypertension. Respiration. 2008;75:272–80.
pubmed: 18025812
doi: 10.1159/000111548
Savai R, Pullamsetti SS, Kolbe J, Bieniek E, Voswinckel R, Fink L, Scheed A, Ritter C, Dahal BK, Vater A, Klussmann S, Ghofrani HA, Weissmann N, Klepetko W, Banat GA, Seeger W, Grimminger F, Schermuly RT. Immune and inflammatory cell involvement in the pathology of idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med. 2012;186:897–908.
pubmed: 22955318
doi: 10.1164/rccm.201202-0335OC
Taylor S, Dirir O, Zamanian RT, Rabinovitch M, Thompson AAR. The role of neutrophils and neutrophil elastase in pulmonary arterial hypertension. Front Med (Lausanne). 2018;5:217.
doi: 10.3389/fmed.2018.00217
Frid MG, Brunetti JA, Burke DL, Carpenter TC, Davie NJ, Reeves JT, Roedersheimer MT, van Rooijen N, Stenmark KR. Hypoxia-induced pulmonary vascular remodeling requires recruitment of circulating mesenchymal precursors of a monocyte/macrophage lineage. Am J Pathol. 2006;168:659–69.
pubmed: 16436679
pmcid: 1606508
doi: 10.2353/ajpath.2006.050599
Schultze AE, Wagner JG, White SM, Roth RA. Early indications of monocrotaline pyrrole-induced lung injury in rats. Toxicol Appl Pharmacol. 1991;109:41–50.
pubmed: 2038748
doi: 10.1016/0041-008X(91)90189-L
Yildiz A, Kaya H, Ertas F, Oylumlu M, Bilik MZ, Yuksel M, Polat N, Akil MA, Atilgan Z, Ulgen MS. Association between neutrophil to lymphocyte ratio and pulmonary arterial hypertension. Turk Kardiyol Dern Ars. 2013;41:604–9.
pubmed: 24164991
doi: 10.5543/tkda.2013.13265
pmcid: 24164991
Zhu L, Wigle D, Hinek A, Kobayashi J, Ye C, Zuker M, Dodo H, Keeley FW, Rabinovitch M. The endogenous vascular elastase that governs development and progression of monocrotaline-induced pulmonary hypertension in rats is a novel enzyme related to the serine proteinase adipsin. J Clin Invest. 1994;94:1163–71.
pubmed: 8083356
pmcid: 295188
doi: 10.1172/JCI117432
Rose F, Hattar K, Gakisch S, Grimminger F, Olschewski H, Seeger W, Tschuschner A, Schermuly RT, Weissmann N, Hanze J, Sibelius U, Ghofrani HA. Increased neutrophil mediator release in patients with pulmonary hypertension−suppression by inhaled iloprost. Thromb Haemost. 2003;90:1141–9.
pubmed: 14652649
doi: 10.1160/TH03-03-0173
pmcid: 14652649
Kim YM, Haghighat L, Spiekerkoetter E, Sawada H, Alvira CM, Wang L, Acharya S, Rodriguez-Colon G, Orton A, Zhao M, Rabinovitch M. Neutrophil elastase is produced by pulmonary artery smooth muscle cells and is linked to neointimal lesions. Am J Pathol. 2011;179:1560–72.
pubmed: 21763677
pmcid: 3157285
doi: 10.1016/j.ajpath.2011.05.051
Spiekerkoetter E, Alvira CM, Kim YM, Bruneau A, Pricola KL, Wang L, Ambartsumian N, Rabinovitch M. Reactivation of gammaHV68 induces neointimal lesions in pulmonary arteries of S100A4/Mts1-overexpressing mice in association with degradation of elastin. Am J Physiol Lung Cell Mol Physiol. 2008;294:L276–89.
pubmed: 18083765
doi: 10.1152/ajplung.00414.2007
pmcid: 18083765
Cowan KN, Heilbut A, Humpl T, Lam C, Ito S, Rabinovitch M. Complete reversal of fatal pulmonary hypertension in rats by a serine elastase inhibitor. Nat Med. 2000;6:698–702.
pubmed: 10835689
doi: 10.1038/76282
pmcid: 10835689
Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science. 2004;303:1532–5.
pubmed: 15001782
doi: 10.1126/science.1092385
pmcid: 15001782
Aldabbous L, Abdul-Salam V, McKinnon T, Duluc L, Pepke-Zaba J, Southwood M, Ainscough AJ, Hadinnapola C, Wilkins MR, Toshner M, Wojciak-Stothard B. Neutrophil extracellular traps promote angiogenesis: evidence from vascular pathology in pulmonary hypertension. Arterioscler Thromb Vasc Biol. 2016;36:2078–87.
pubmed: 27470511
doi: 10.1161/ATVBAHA.116.307634
pmcid: 27470511
Borissoff JI, Joosen IA, Versteylen MO, Brill A, Fuchs TA, Savchenko AS, Gallant M, Martinod K, Ten Cate H, Hofstra L, Crijns HJ, Wagner DD, Kietselaer B. Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state. Arterioscler Thromb Vasc Biol. 2013;33:2032–40.
pubmed: 23818485
pmcid: 3806482
doi: 10.1161/ATVBAHA.113.301627
Nickel NP, Spiekerkoetter E, Gu M, Li CG, Li H, Kaschwich M, Diebold I, Hennigs JK, Kim KY, Miyagawa K, Wang L, Cao A, Sa S, Jiang X, Stockstill RW, Nicolls MR, Zamanian RT, Bland RD, Rabinovitch M. Elafin reverses pulmonary hypertension via Caveolin-1-dependent bone morphogenetic protein signaling. Am J Respir Crit Care Med. 2015;191:1273–86.
pubmed: 25853696
pmcid: 4476518
doi: 10.1164/rccm.201412-2291OC
Tuder RM, Groves B, Badesch DB, Voelkel NF. Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension. Am J Pathol. 1994;144:275–85.
pubmed: 7508683
pmcid: 1887146
Vergadi E, Chang MS, Lee C, Liang OD, Liu X, Fernandez-Gonzalez A, Mitsialis SA, Kourembanas S. Early macrophage recruitment and alternative activation are critical for the later development of hypoxia-induced pulmonary hypertension. Circulation. 2011;123:1986–95.
pubmed: 21518986
pmcid: 3125055
doi: 10.1161/CIRCULATIONAHA.110.978627
Thenappan T, Goel A, Marsboom G, Fang YH, Toth PT, Zhang HJ, Kajimoto H, Hong Z, Paul J, Wietholt C, Pogoriler J, Piao L, Rehman J, Archer SL. A central role for CD68(+) macrophages in hepatopulmonary syndrome. Reversal by macrophage depletion. Am J Respir Crit Care Med. 2011;183:1080–91.
pubmed: 21148721
doi: 10.1164/rccm.201008-1303OC
pmcid: 21148721
Tian W, Jiang X, Tamosiuniene R, Sung YK, Qian J, Dhillon G, Gera L, Farkas L, Rabinovitch M, Zamanian RT, Inayathullah M, Fridlib M, Rajadas J, Peters-Golden M, Voelkel NF, Nicolls MR. Blocking macrophage leukotriene b4 prevents endothelial injury and reverses pulmonary hypertension. Sci Transl Med. 2013;5:200ra117.
pubmed: 23986401
pmcid: 4016764
doi: 10.1126/scitranslmed.3006674
Florentin J, Coppin E, Vasamsetti SB, Zhao J, Tai Y-Y, Tang Y, Zhang Y, Watson A, Sembrat J, Rojas M, Vargas SO, Chan SY, Dutta P. Inflammatory macrophage expansion in pulmonary hypertension depends upon mobilization of blood-borne monocytes. J immunol. 2018;1950(200):3612–25.
doi: 10.4049/jimmunol.1701287
Zaloudikova M, Vytasek R, Vajnerova O, Hnilickova O, Vizek M, Hampl V, Herget J. Depletion of alveolar macrophages attenuates hypoxic pulmonary hypertension but not hypoxia-induced increase in serum concentration of MCP-1. Physiol Res. 2016;65:763–8.
pubmed: 27429111
doi: 10.33549/physiolres.933187
pmcid: 27429111
Li M, Riddle SR, Frid MG, El Kasmi KC, McKinsey TA, Sokol RJ, Strassheim D, Meyrick B, Yeager ME, Flockton AR, McKeon BA, Lemon DD, Horn TR, Anwar A, Barajas C, Stenmark KR. Emergence of fibroblasts with a proinflammatory epigenetically altered phenotype in severe hypoxic pulmonary hypertension. J Immunol. 2011;187:2711–22.
pubmed: 21813768
pmcid: 3159707
doi: 10.4049/jimmunol.1100479
Li C, Liu P, Song R, Zhang Y, Lei S, Wu S. Immune cells and autoantibodies in pulmonary arterial hypertension. Acta Biochim Biophys Sin. 2017;49:1047–57.
pubmed: 29036539
doi: 10.1093/abbs/gmx095
pmcid: 29036539
van Rijt LS, Lambrecht BN. Dendritic cells in asthma: a function beyond sensitization. Clin Exp Allergy. 2005;35:1125–34.
pubmed: 16164437
doi: 10.1111/j.1365-2222.2005.02321.x
pmcid: 16164437
Palucka AK, Blanck J-P, Bennett L, Pascual V, Banchereau J. Cross-regulation of TNF and IFN-α in autoimmune diseases. Proc Natl Acad Sci USA. 2005;102:3372–7.
pubmed: 15728381
doi: 10.1073/pnas.0408506102
pmcid: 15728381
Gabrilovich D, Ishida T, Oyama T, Ran S, Kravtsov V, Nadaf S, Carbone DP. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood. 1998;92:4150–66.
pubmed: 9834220
doi: 10.1182/blood.V92.11.4150
pmcid: 9834220
Perros F, Dorfmuller P, Souza R, Durand-Gasselin I, Mussot S, Mazmanian M, Herve P, Emilie D, Simonneau G, Humbert M. Dendritic cell recruitment in lesions of human and experimental pulmonary hypertension. Eur Respir J. 2007;29:462–8.
pubmed: 17107989
doi: 10.1183/09031936.00094706
Cool CD, Kennedy D, Voelkel NF, Tuder RM. Pathogenesis and evolution of plexiform lesions in pulmonary hypertension associated with scleroderma and human immunodeficiency virus infection. Hum Pathol. 1997;28:434–42.
pubmed: 9104943
doi: 10.1016/S0046-8177(97)90032-0
pmcid: 9104943
Perros F, Dorfmuller P, Montani D, Hammad H, Waelput W, Girerd B, Raymond N, Mercier O, Mussot S, Cohen-Kaminsky S, Humbert M, Lambrecht BN. Pulmonary lymphoid neogenesis in idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med. 2012;185:311–21.
pubmed: 22108206
doi: 10.1164/rccm.201105-0927OC
Wang W, Yan H, Zhu W, Cui Y, Chen J, Wang X, Li S, Zhu J. Impairment of monocyte-derived dendritic cells in idiopathic pulmonary arterial hypertension. J Clin Immunol. 2009;29:705–13.
pubmed: 19693657
doi: 10.1007/s10875-009-9322-8
Marsh LM, Jandl K, Grunig G, Foris V, Bashir M, Ghanim B, Klepetko W, Olschewski H, Olschewski A, Kwapiszewska G. The inflammatory cell landscape in the lungs of patients with idiopathic pulmonary arterial hypertension. Eur Respir J. 2018;51
Yang T, Li ZN, Chen G, Gu Q, Ni XH, Zhao ZH, Ye J, Meng XM, Liu ZH, Xiong CM, He JG. Increased levels of plasma CXC-chemokine ligand 10, 12 and 16 are associated with right ventricular function in patients with idiopathic pulmonary arterial hypertension. Heart Lung. 2014;43:322–7.
pubmed: 24856224
doi: 10.1016/j.hrtlng.2014.04.016
Itoh T, Nagaya N, Ishibashi-Ueda H, Kyotani S, Oya H, Sakamaki F, Kimura H, Nakanishi N. Increased plasma monocyte chemoattractant protein-1 level in idiopathic pulmonary arterial hypertension. Respirology. 2006;11:158–63.
pubmed: 16548900
doi: 10.1111/j.1440-1843.2006.00821.x
Ribatti D, Vacca A, Nico B, Crivellato E, Roncali L, Dammacco F. The role of mast cells in tumour angiogenesis. Br J Haematol. 2001;115:514–21.
pubmed: 11736931
doi: 10.1046/j.1365-2141.2001.03202.x
Mitani Y, Ueda M, Maruyama K, Shimpo H, Kojima A, Matsumura M, Aoki K, Sakurai M. Mast cell chymase in pulmonary hypertension. Thorax. 1999;54:88–90.
pubmed: 10343640
pmcid: 1745338
doi: 10.1136/thx.54.1.88
Hamada H, Terai M, Kimura H, Hirano K, Oana S, Niimi H. Increased expression of mast cell chymase in the lungs of patients with congenital heart disease associated with early pulmonary vascular disease. Am J Respir Crit Care Med. 1999;160:1303–8.
pubmed: 10508822
doi: 10.1164/ajrccm.160.4.9810058
Farha S, Sharp J, Asosingh K, Park M, Comhair SA, Tang WH, Thomas J, Farver C, Hsieh F, Loyd JE, Erzurum SC. Mast cell number, phenotype, and function in human pulmonary arterial hypertension. Pulm Circ. 2012;2:220–8.
pubmed: 22837863
pmcid: 3401876
doi: 10.4103/2045-8932.97609
Gilfillan AM, Rivera J. The tyrosine kinase network regulating mast cell activation. Immunol Rev. 2009;228:149–69.
pubmed: 19290926
pmcid: 2669301
doi: 10.1111/j.1600-065X.2008.00742.x
Bartelds B, van Loon RLE, Mohaupt S, Wijnberg H, Dickinson MG, Boersma B, Takens J, van Albada M, Berger RMF. Mast cell inhibition improves pulmonary vascular remodeling in pulmonary hypertension. Chest. 2012;141:651–60.
pubmed: 21940767
doi: 10.1378/chest.11-0663
Caughey GH. Mast cell tryptases and chymases in inflammation and host defense. Immunol Rev. 2007;217:141–54.
pubmed: 17498057
pmcid: 2275918
doi: 10.1111/j.1600-065X.2007.00509.x
Kwapiszewska G, Markart P, Dahal BK, Kojonazarov B, Marsh LM, Schermuly RT, Taube C, Meinhardt A, Ghofrani HA, Steinhoff M, Seeger W, Preissner KT, Olschewski A, Weissmann N, Wygrecka M. PAR-2 inhibition reverses experimental pulmonary hypertension. Circ Res. 2012;110:1179–91.
pubmed: 22461388
doi: 10.1161/CIRCRESAHA.111.257568
Farha S, Dweik R, Rahaghi F, Benza R, Hassoun P, Frantz R, Torres F, Quinn DA, Comhair S, Erzurum S, Asosingh K. Imatinib in pulmonary arterial hypertension: c-Kit inhibition. Pulm Circ. 2014;4:452–5.
pubmed: 25621158
pmcid: 4278604
doi: 10.1086/677359
Colvin KL, Cripe PJ, Ivy DD, Stenmark KR, Yeager ME. Bronchus-associated lymphoid tissue in pulmonary hypertension produces pathologic autoantibodies. Am J Respir Crit Care Med. 2013;188:1126–36.
pubmed: 24093638
pmcid: 3863738
doi: 10.1164/rccm.201302-0403OC
Breitling S, Hui Z, Zabini D, Hu Y, Hoffmann J, Goldenberg NM, Tabuchi A, Buelow R, Dos Santos C, Kuebler WM. The mast cell-B cell axis in lung vascular remodeling and pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2017;312:L710–L21.
pubmed: 28235950
doi: 10.1152/ajplung.00311.2016
pmcid: 28235950
Bulfone-Paus S, Bahri R. Mast cells as regulators of T cell responses. Front Immunol. 2015;6:394.
pubmed: 26300882
pmcid: 4528181
doi: 10.3389/fimmu.2015.00394
Price LC, Wort SJ, Perros F, Dorfmuller P, Huertas A, Montani D, Cohen-Kaminsky S, Humbert M. Inflammation in pulmonary arterial hypertension. Chest. 2012;141:210–21.
pubmed: 22215829
doi: 10.1378/chest.11-0793
Groth A, Vrugt B, Brock M, Speich R, Ulrich S, Huber LC. Inflammatory cytokines in pulmonary hypertension. Respir Res. 2014;15:47.
pubmed: 24739042
pmcid: 4002553
doi: 10.1186/1465-9921-15-47
Kimura A, Kishimoto T. IL-6: regulator of Treg/Th17 balance. Eur J Immunol. 2010;40:1830–5.
doi: 10.1002/eji.201040391
pubmed: 20583029
Steiner MK, Syrkina OL, Kolliputi N, Mark EJ, Hales CA, Waxman AB. Interleukin-6 overexpression induces pulmonary hypertension. Circ Res. 2009;104:236–44, 28p following 44.
Heresi GA, Aytekin M, Hammel JP, Wang S, Chatterjee S, Dweik RA. Plasma interleukin-6 adds prognostic information in pulmonary arterial hypertension. Eur Respir J. 2014;43:912–4.
pubmed: 24136333
doi: 10.1183/09031936.00164713
Golembeski SM, West J, Tada Y, Fagan KA. Interleukin-6 causes mild pulmonary hypertension and augments hypoxia-induced pulmonary hypertension in mice. Chest. 2005;128:572S–3S.
pubmed: 16373831
doi: 10.1378/chest.128.6_suppl.572S-a
Miyata M, Sakuma F, Yoshimura A, Ishikawa H, Nishimaki T, Kasukawa R. Pulmonary hypertension in rats. 2. Role of interleukin-6. Int Arch Allergy Immunol. 1995;108:287–91.
pubmed: 7580295
doi: 10.1159/000237166
Itoh A, Nishihira J, Makita H, Miyamoto K, Yamaguchi E, Nishimura M. Effects of IL-1beta, TNF-alpha, and macrophage migration inhibitory factor on prostacyclin synthesis in rat pulmonary artery smooth muscle cells. Respirology. 2003;8:467–72.
pubmed: 14629650
doi: 10.1046/j.1440-1843.2003.00491.x
pmcid: 14629650
Voelkel NF, Tuder RM, Bridges J, Arend WP. Interleukin-1 receptor antagonist treatment reduces pulmonary hypertension generated in rats by monocrotaline. Am J Respir Cell Mol Biol. 1994;11:664–75.
pubmed: 7946395
doi: 10.1165/ajrcmb.11.6.7946395
Ross DJ, Strieter RM, Fishbein MC, Ardehali A, Belperio JA. Type I immune response cytokine-chemokine cascade is associated with pulmonary arterial hypertension. J Heart Lung Transplant. 2012;31:865–73.
pubmed: 22658713
doi: 10.1016/j.healun.2012.04.008
Li A, Varney ML, Valasek J, Godfrey M, Dave BJ, Singh RK. Autocrine role of interleukin-8 in induction of endothelial cell proliferation, survival, migration and MMP-2 production and angiogenesis. Angiogenesis. 2005;8:63–71.
pubmed: 16132619
doi: 10.1007/s10456-005-5208-4
pmcid: 16132619
Stevens T, Janssen PL, Tucker A. Acute and long-term TNF-alpha administration increases pulmonary vascular reactivity in isolated rat lungs. J Appl Physiol. 1985;1992(73):708–12.
Costello CM, McCullagh B, Howell K, Sands M, Belperio JA, Keane MP, Gaine S, McLoughlin P. A role for the CXCL12 receptor, CXCR7, in the pathogenesis of human pulmonary vascular disease. Eur Respir J. 2012;39:1415–24.
pubmed: 22088972
doi: 10.1183/09031936.00044911
McCullagh BN, Costello CM, Li L, O’Connell C, Codd M, Lawrie A, Morton A, Kiely DG, Condliffe R, Elliot C, McLoughlin P, Gaine S. Elevated plasma CXCL12alpha is associated with a poorer prognosis in pulmonary arterial hypertension. PLoS One. 2015;10:e0123709.
pubmed: 25856504
pmcid: 4391833
doi: 10.1371/journal.pone.0123709
Lei Y, Zhen J, Ming XL, Jian HK. Induction of higher expression of IL-beta and TNF-alpha, lower expression of IL-10 and cyclic guanosine monophosphate by pulmonary arterial hypertension following cardiopulmonary bypass. Asian J Surg. 2002;25:203–8.
pubmed: 12376215
doi: 10.1016/S1015-9584(09)60176-7
Condliffe R, Pickworth JA, Hopkinson K, Walker SJ, Hameed AG, Suntharaligam J, Soon E, Treacy C, Pepke-Zaba J, Francis SE, Crossman DC, Newman CM, Elliot CA, Morton AC, Morrell NW, Kiely DG, Lawrie A. Serum osteoprotegerin is increased and predicts survival in idiopathic pulmonary arterial hypertension. Pulm Circ. 2012;2:21–7.
pubmed: 22558516
pmcid: 3342744
doi: 10.4103/2045-8932.94819
Lawrie A, Waterman E, Southwood M, Evans D, Suntharalingam J, Francis S, Crossman D, Croucher P, Morrell N, Newman C. Evidence of a role for osteoprotegerin in the pathogenesis of pulmonary arterial hypertension. Am J Pathol. 2008;172:256–64.
pubmed: 18156213
pmcid: 2189625
doi: 10.2353/ajpath.2008.070395
Sweatt AJ, Hedlin HK, Balasubramanian V, Hsi A, Blum LK, Robinson WH, Haddad F, Hickey PM, Condliffe R, Lawrie A, Nicolls MR, Rabinovitch M, Khatri P, Zamanian RT. Discovery of distinct immune phenotypes using machine learning in pulmonary arterial hypertension. Circ Res. 2019;124:904–19.
pubmed: 30661465
pmcid: 6428071
doi: 10.1161/CIRCRESAHA.118.313911
Teichert-Kuliszewska K, Kutryk MJ, Kuliszewski MA, Karoubi G, Courtman DW, Zucco L, Granton J, Stewart DJ. Bone morphogenetic protein receptor-2 signaling promotes pulmonary arterial endothelial cell survival: implications for loss-of-function mutations in the pathogenesis of pulmonary hypertension. Circ Res. 2006;98:209–17.
pubmed: 16357305
doi: 10.1161/01.RES.0000200180.01710.e6
pmcid: 16357305
Morrell NW, Aldred MA, Chung WK, Elliott CG, Nichols WC, Soubrier F, Trembath RC, Loyd JE. Genetics and genomics of pulmonary arterial hypertension. Eur Respir J. 2019;53:1801899.
pubmed: 30545973
pmcid: 6351337
doi: 10.1183/13993003.01899-2018
McDonald PP, Fadok VA, Bratton D, Henson PM. Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-beta in macrophages that have ingested apoptotic cells. J Immunol. 1999;163:6164–72.
pubmed: 10570307
pmcid: 10570307
Morrell NW. Pulmonary hypertension due to BMPR2 mutation: a new paradigm for tissue remodeling? Proc Am Thorac Soc. 2006;3:680–6.
pubmed: 17065373
doi: 10.1513/pats.200605-118SF
pmcid: 17065373
Schraufnagel DE. Lung lymphatic anatomy and correlates. Pathophysiology. 2010;17:337–43.
pubmed: 20004086
doi: 10.1016/j.pathophys.2009.10.008
pmcid: 20004086
Reed HO, Wang L, Sonett J, Chen M, Yang J, Li L, Aradi P, Jakus Z, D'Armiento J, Hancock WW, Kahn ML. Lymphatic impairment leads to pulmonary tertiary lymphoid organ formation and alveolar damage. J Clin Invest. 2019;129:2514–26.
pubmed: 30946031
pmcid: 6546450
doi: 10.1172/JCI125044
Cui Y, Liu K, Lamattina AM, Visner G, El-Chemaly S. Lymphatic vessels: the next frontier in lung transplant. Ann Am Thorac Soc. 2017;14:S226–S32.
pubmed: 28945468
pmcid: 5711339
doi: 10.1513/AnnalsATS.201606-465MG
Sakao S, Tatsumi K, Voelkel NF. Endothelial cells and pulmonary arterial hypertension: apoptosis, proliferation, interaction and transdifferentiation. Respir Res. 2009;10:95.
pubmed: 19825167
pmcid: 2768704
doi: 10.1186/1465-9921-10-95
Perros F, Ranchoux B, Izikki M, Bentebbal S, Happe C, Antigny F, Jourdon P, Dorfmuller P, Lecerf F, Fadel E, Simonneau G, Humbert M, Bogaard HJ, Eddahibi S. Nebivolol for improving endothelial dysfunction, pulmonary vascular remodeling, and right heart function in pulmonary hypertension. J Am Coll Cardiol. 2015;65:668–80.
pubmed: 25677428
doi: 10.1016/j.jacc.2014.11.050
pmcid: 25677428
Pietra GG, Edwards WD, Kay JM, Rich S, Kernis J, Schloo B, Ayres SM, Bergofsky EH, Brundage BH, Detre KM, 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. Circulation. 1989;80:1198–206.
pubmed: 2805258
doi: 10.1161/01.CIR.80.5.1198
Abe K, Toba M, Alzoubi A, Ito M, Fagan KA, Cool CD, Voelkel NF, McMurtry IF, Oka M. Formation of plexiform lesions in experimental severe pulmonary arterial hypertension. Circulation. 2010;121:2747–54.
pubmed: 20547927
doi: 10.1161/CIRCULATIONAHA.109.927681
Jonigk D, Golpon H, Bockmeyer CL, Maegel L, Hoeper MM, Gottlieb J, Nickel N, Hussein K, Maus U, Lehmann U, Janciauskiene S, Welte T, Haverich A, Rische J, Kreipe H, Laenger F. Plexiform lesions in pulmonary arterial hypertension composition, architecture, and microenvironment. Am J Pathol. 2011;179:167–79.
pubmed: 21703400
pmcid: 3123793
doi: 10.1016/j.ajpath.2011.03.040
Zhou C, Townsley MI, Alexeyev M, Voelkel NF, Stevens T. Endothelial hyperpermeability in severe pulmonary arterial hypertension: role of store-operated calcium entry. Am J Physiol Lung Cell Mol Physiol. 2016;311:L560–9.
pubmed: 27422996
pmcid: 5142214
doi: 10.1152/ajplung.00057.2016
Francis M, Xu N, Zhou C, Stevens T. Transient receptor potential channel 4 encodes a vascular permeability defect and high-frequency Ca(2+) transients in severe pulmonary arterial hypertension. Am J Pathol. 2016;186:1701–9.
pubmed: 27083517
pmcid: 4901130
doi: 10.1016/j.ajpath.2016.02.002
Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7:678–89.
pubmed: 17717539
doi: 10.1038/nri2156
Yaoita N, Shirakawa R, Fukumoto Y, Sugimura K, Miyata S, Miura Y, Nochioka K, Miura M, Tatebe S, Aoki T, Yamamoto S, Satoh K, Kimura T, Shimokawa H, Horiuchi H. Platelets are highly activated in patients of chronic thromboembolic pulmonary hypertension. Arterioscler Thromb Vasc Biol. 2014;34:2486–94.
pubmed: 25169936
doi: 10.1161/ATVBAHA.114.304404
Sakamaki F, Kyotani S, Nagaya N, Sato N, Oya H, Satoh T, Nakanishi N. Increased plasma P-selectin and decreased thrombomodulin in pulmonary arterial hypertension were improved by continuous prostacyclin therapy. Circulation. 2000;102:2720–5.
pubmed: 11094038
doi: 10.1161/01.CIR.102.22.2720
Hironaka E, Hongo M, Sakai A, Mawatari E, Terasawa F, Okumura N, Yamazaki A, Ushiyama Y, Yazaki Y, Kinoshita O. Serotonin receptor antagonist inhibits monocrotaline-induced pulmonary hypertension and prolongs survival in rats. Cardiovasc Res. 2003;60:692–9.
pubmed: 14659815
doi: 10.1016/j.cardiores.2003.09.023
Vengethasamy L, Hautefort A, Tielemans B, Belge C, Perros F, Verleden S, Fadel E, Van Raemdonck D, Delcroix M, Quarck R. BMPRII influences the response of pulmonary microvascular endothelial cells to inflammatory mediators. Pflugers Arch. 2016;468:1969–83.
pubmed: 27816994
doi: 10.1007/s00424-016-1899-1
Le Hiress M, Tu L, Ricard N, Phan C, Thuillet R, Fadel E, Dorfmuller P, Montani D, de Man F, Humbert M, Huertas A, Guignabert C. Proinflammatory signature of the dysfunctional endothelium in pulmonary hypertension. Role of the macrophage migration inhibitory factor/CD74 complex. Am J Respir Crit Care Med. 2015;192:983–97.
pubmed: 26203495
doi: 10.1164/rccm.201402-0322OC
pmcid: 26203495
Diller GP, Thum T, Wilkins MR, Wharton J. Endothelial progenitor cells in pulmonary arterial hypertension. Trends Cardiovasc Med. 2010;20:22–9.
pubmed: 20685574
doi: 10.1016/j.tcm.2010.03.003
pmcid: 20685574
Spees JL, Whitney MJ, Sullivan DE, Lasky JA, Laboy M, Ylostalo J, Prockop DJ. Bone marrow progenitor cells contribute to repair and remodeling of the lung and heart in a rat model of progressive pulmonary hypertension. FASEB J. 2008;22:1226–36.
pubmed: 18032636
doi: 10.1096/fj.07-8076com
pmcid: 18032636
Stewart DJ, Zhao YD, Courtman DW. Cell therapy for pulmonary hypertension: what is the true potential of endothelial progenitor cells? Circulation 2004;109:e172–3. Author reply e-3.
Zhao YD, Courtman DW, Deng Y, Kugathasan L, Zhang Q, Stewart DJ. Rescue of monocrotaline-induced pulmonary arterial hypertension using bone marrow-derived endothelial-like progenitor cells: efficacy of combined cell and eNOS gene therapy in established disease. Circ Res. 2005;96:442–50.
pubmed: 15692087
doi: 10.1161/01.RES.0000157672.70560.7b
Yuan K, Orcholski ME, Panaroni C, Shuffle EM, Huang NF, Jiang X, Tian W, Vladar EK, Wang L, Nicolls MR, Wu JY, de Jesus Perez VA. Activation of the Wnt/planar cell polarity pathway is required for pericyte recruitment during pulmonary angiogenesis. Am J Pathol. 2015;185:69–84.
pubmed: 25447046
pmcid: 4278244
doi: 10.1016/j.ajpath.2014.09.013
Yuan K, Liu Y, Zhang Y, Nathan A, Tian W, Yu J, Sweatt AJ, Shamshou EA, Condon D, Chakraborty A, Agarwal S, Auer N, Zhang S, Wu JC, Zamanian RT, Nicolls MR, de Jesus Perez VA. Mural cell SDF1 signaling is associated with the pathogenesis of pulmonary arterial hypertension. Am J Respir Cell Mol Biol. 2020;62:747–59.
pubmed: 32084325
doi: 10.1165/rcmb.2019-0401OC
Yuan K, Shamskhou EA, Orcholski ME, Nathan A, Reddy S, Honda H, Mani V, Zeng Y, Ozen MO, Wang L, Demirci U, Tian W, Nicolls MR, de Jesus Perez VA. Loss of endothelium-derived Wnt5a is associated with reduced Pericyte recruitment and small vessel loss in pulmonary arterial hypertension. Circulation. 2019;139:1710–24.
pubmed: 30586764
pmcid: 6443444
doi: 10.1161/CIRCULATIONAHA.118.037642
Balabanov R, Washington R, Wagnerova J, Dore-Duffy P. CNS microvascular pericytes express macrophage-like function, cell surface integrin alpha M, and macrophage marker ED-2. Microvasc Res. 1996;52:127–42.
pubmed: 8901442
doi: 10.1006/mvre.1996.0049
pmcid: 8901442
Edelman DA, Jiang Y, Tyburski J, Wilson RF, Steffes C. Toll-like receptor-4 message is up-regulated in lipopolysaccharide-exposed rat lung pericytes. J Surg Res. 2006;134:22–7.
pubmed: 16631199
doi: 10.1016/j.jss.2006.03.007
pmcid: 16631199
Edelman DA, Jiang Y, Tyburski JG, Wilson RF, Steffes CP. Lipopolysaccharide up-regulates heat shock protein expression in rat lung pericytes. J Surg Res. 2007;140:171–6.
pubmed: 17509261
doi: 10.1016/j.jss.2006.12.560
Edelman DA, Jiang Y, Tyburski JG, Wilson RF, Steffes CP. Cytokine production in lipopolysaccharide-exposed rat lung pericytes. J Trauma. 2007;62:89–93.
pubmed: 17215738
doi: 10.1097/TA.0b013e31802dd712
pmcid: 17215738
Speyer CL, Steffes CP, Tyburski JG, Ram JL. Lipopolysaccharide induces relaxation in lung pericytes by an iNOS-independent mechanism. Am J Physiol Lung Cell Mol Physiol. 2000;278:L880–7.
pubmed: 10781417
doi: 10.1152/ajplung.2000.278.5.L880
pmcid: 10781417
Donoghue L, Tyburski JG, Steffes CP, Wilson RF. Vascular endothelial growth factor modulates contractile response in microvascular lung pericytes. Am J Surg. 2006;191:349–52.
pubmed: 16490545
doi: 10.1016/j.amjsurg.2005.10.034
pmcid: 16490545
Muller WA. Mechanisms of transendothelial migration of leukocytes. Circ Res. 2009;105:223–30.
pubmed: 19644057
pmcid: 2739407
doi: 10.1161/CIRCRESAHA.109.200717
Wang S, Voisin MB, Larbi KY, Dangerfield J, Scheiermann C, Tran M, Maxwell PH, Sorokin L, Nourshargh S. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J Exp Med. 2006;203:1519–32.
pubmed: 16754715
pmcid: 2118318
doi: 10.1084/jem.20051210
Voisin MB, Woodfin A, Nourshargh S. Monocytes and neutrophils exhibit both distinct and common mechanisms in penetrating the vascular basement membrane in vivo. Arterioscler Thromb Vasc Biol. 2009;29:1193–9.
pubmed: 19498176
pmcid: 2712455
doi: 10.1161/ATVBAHA.109.187450
Ayres-Sander CE, Lauridsen H, Maier CL, Sava P, Pober JS, Gonzalez AL. Transendothelial migration enables subsequent transmigration of neutrophils through underlying pericytes. PLoS One. 2013;8:e60025.
pubmed: 23555870
pmcid: 3608600
doi: 10.1371/journal.pone.0060025
Lauridsen HM, Pober JS, Gonzalez AL. A composite model of the human postcapillary venule for investigation of microvascular leukocyte recruitment. FASEB J. 2014;28:1166–80.
pubmed: 24297702
pmcid: 3929680
doi: 10.1096/fj.13-240986
Stark K, Eckart A, Haidari S, Tirniceriu A, Lorenz M, von Bruhl ML, Gartner F, Khandoga AG, Legate KR, Pless R, Hepper I, Lauber K, Walzog B, Massberg S. Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct' them with pattern-recognition and motility programs. Nat Immunol. 2013;14:41–51.
pubmed: 23179077
doi: 10.1038/ni.2477
pmcid: 23179077
Proebstl D, Voisin MB, Woodfin A, Whiteford J, D'Acquisto F, Jones GE, Rowe D, Nourshargh S. Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo. J Exp Med. 2012;209:1219–34.
pubmed: 22615129
pmcid: 3371725
doi: 10.1084/jem.20111622
Hung CF, Mittelsteadt KL, Brauer R, McKinney BL, Hallstrand TS, Parks WC, Chen P, Schnapp LM, Liles WC, Duffield JS, Altemeier WA. Lung pericyte-like cells are functional interstitial immune sentinel cells. Am J Physiol Lung Cell Mol Physiol. 2017;312:L556–L67.
pubmed: 28188224
pmcid: 5407093
doi: 10.1152/ajplung.00349.2016
Burke DL, Frid MG, Kunrath CL, Karoor V, Anwar A, Wagner BD, Strassheim D, Stenmark KR. Sustained hypoxia promotes the development of a pulmonary artery-specific chronic inflammatory microenvironment. Am J Physiol Lung Cell Mol Physiol. 2009;297:L238–50.
pubmed: 19465514
pmcid: 2742800
doi: 10.1152/ajplung.90591.2008
Farha S, Asosingh K, Xu W, Sharp J, George D, Comhair S, Park M, Tang WH, Loyd JE, Theil K, Tubbs R, Hsi E, Lichtin A, Erzurum SC. Hypoxia-inducible factors in human pulmonary arterial hypertension: a link to the intrinsic myeloid abnormalities. Blood. 2011;117:3485–93.
pubmed: 21258008
pmcid: 3072874
doi: 10.1182/blood-2010-09-306357
Stenmark KR, Frid MG, Graham BB, Tuder RM. Dynamic and diverse changes in the functional properties of vascular smooth muscle cells in pulmonary hypertension. Cardiovasc Res. 2018;114:551–64.
pubmed: 29385432
pmcid: 5852549
doi: 10.1093/cvr/cvy004
Hoeper MM, Barst RJ, Bourge RC, Feldman J, Frost AE, Galie N, Gomez-Sanchez MA, Grimminger F, Grunig E, Hassoun PM, Morrell NW, Peacock AJ, Satoh T, Simonneau G, Tapson VF, Torres F, Lawrence D, Quinn DA, Ghofrani HA. Imatinib mesylate as add-on therapy for pulmonary arterial hypertension: results of the randomized IMPRES study. Circulation. 2013;127:1128–38.
pubmed: 23403476
doi: 10.1161/CIRCULATIONAHA.112.000765
pmcid: 23403476
Schermuly RT, Dony E, Ghofrani HA, Pullamsetti S, Savai R, Roth M, Sydykov A, Lai YJ, Weissmann N, Seeger W, Grimminger F. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest. 2005;115:2811–21.
pubmed: 16200212
pmcid: 1236676
doi: 10.1172/JCI24838
Panzhinskiy E, Zawada WM, Stenmark KR, Das M. Hypoxia induces unique proliferative response in adventitial fibroblasts by activating PDGFbeta receptor-JNK1 signalling. Cardiovasc Res. 2012;95:356–65.
pubmed: 22735370
pmcid: 3400360
doi: 10.1093/cvr/cvs194
Das M, Burns N, Wilson SJ, Zawada WM, Stenmark KR. Hypoxia exposure induces the emergence of fibroblasts lacking replication repressor signals of PKCzeta in the pulmonary artery adventitia. Cardiovasc Res. 2008;78:440–8.
pubmed: 18218684
doi: 10.1093/cvr/cvn014
pmcid: 18218684
El Kasmi KC, Pugliese SC, Riddle SR, Poth JM, Anderson AL, Frid MG, Li M, Pullamsetti SS, Savai R, Nagel MA, Fini MA, Graham BB, Tuder RM, Friedman JE, Eltzschig HK, Sokol RJ, Stenmark KR. Adventitial fibroblasts induce a distinct proinflammatory/profibrotic macrophage phenotype in pulmonary hypertension. J Immunol. 2014;193:597–609.
pubmed: 24928992
pmcid: 4100597
doi: 10.4049/jimmunol.1303048
Plecitá-Hlavatá L, Tauber J, Li M, Zhang H, Flockton AR, Pullamsetti SS, Chelladurai P, D'Alessandro A, El Kasmi KC, Ježek P, Stenmark KR. Constitutive reprogramming of fibroblast mitochondrial metabolism in pulmonary hypertension. Am J Respir Cell Mol Biol. 2016;55:47–57.
pubmed: 26699943
pmcid: 4942204
doi: 10.1165/rcmb.2015-0142OC
Woo KV, Weinheimer C, Kovacs A, Ornitz D. Impact of endothelial fibroblast growth factors on pulmonary hypertension. J Am Coll Cardiol. 2017;69:1901.
doi: 10.1016/S0735-1097(17)35290-7
Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol. 2007;170:1807–16.
pubmed: 17525249
pmcid: 1899462
doi: 10.2353/ajpath.2007.070112
Maruoka M, Sakao S, Kantake M, Tanabe N, Kasahara Y, Kurosu K, Takiguchi Y, Masuda M, Yoshino I, Voelkel NF, Tatsumi K. Characterization of myofibroblasts in chronic thromboembolic pulmonary hypertension. Int J Cardiol. 2012;159:119–27.
pubmed: 21406312
doi: 10.1016/j.ijcard.2011.02.037
pmcid: 21406312
Qiu H, He Y, Ouyang F, Jiang P, Guo S, Guo Y. The role of regulatory T cells in pulmonary arterial hypertension. J Am Heart Assoc. 2019;8:e014201.
pubmed: 31771439
pmcid: 6912965
doi: 10.1161/JAHA.119.014201