Key role of the endothelial TGF-β/ALK1/endoglin signaling pathway in humans and rodents pulmonary hypertension

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Gore, Benoît ^a   Izikki, Mohamed ^a   Mercier, Olaf ^c   Dewachter, Laurence ^b   Fadel, Elie ^c   Humbert, Marc ^a   Dartevelle, Philippe ^c   Simonneau, Gerald ^a   Naeije, Robert ^b   Lebrin, Franck ^d   Eddahibi, Saadia ^a,c  

^a Universite Paris Sud   (France)

^b FREE UNIVERSITY OF BRUSSELS   (Belgium)

^c CENTRE CHIRURGICAL MARIE LANNELONGUE   (France)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; CANCER GROWTH FACTOR; CYTOKINE; ENDOGLIN; ENDOTHELIN 1; FIBROBLAST GROWTH FACTOR 2; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR B; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TUMOR GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ACTIVIN RECEPTOR 2; ACVRL1 PROTEIN, HUMAN; ENDOGLIN PROTEIN, MOUSE; SIGNAL PEPTIDE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PARAMETERS; CELL COUNT; CELL GROWTH; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HEART RIGHT VENTRICLE PRESSURE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERTROPHY; HYPOXIA; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PULMONARY BLOOD VESSEL DENSITY; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION; SYSTOLIC BLOOD PRESSURE; WILD TYPE; ANIMAL; C57BL MOUSE; CASE CONTROL STUDY; CELL CULTURE; CELL PROLIFERATION; COMPARATIVE STUDY; CYTOLOGY; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FOLLOW UP; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROGNOSIS; PULMONARY ARTERY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

ACTIVIN RECEPTORS, TYPE II; ANIMALS; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ENZYME-LINKED IMMUNOSORBENT ASSAY; FAMILIAL PRIMARY PULMONARY HYPERTENSION; FEMALE; FOLLOW-UP STUDIES; HUMANS; HYPERTENSION, PULMONARY; IMMUNOENZYME TECHNIQUES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; PROGNOSIS; PULMONARY ARTERY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84903535162     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100310     Document Type: Article

References (32)

1. Galie N, Hoeper MM, Humbert M, Torbicki A, Vachiery JL, et al. (2009) Guidelines for the diagnosis and treatment of pulmonary hypertension: the Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS), endorsed by the International Society of Heart and Lung Transplantation (ISHLT). Eur Heart J 30: 2493-2537.
2. Machado RD, Eickelberg O, Elliott CG, Geraci MW, Hanaoka M, et al. (2009) Genetics and genomics of pulmonary arterial hypertension. J Am Coll Cardiol 54: S32-42.
3. Massague J (1998) TGF-beta signal transduction. Annu Rev Biochem 67: 753-791.
4. Goumans MJ, Lebrin F, Valdimarsdottir G (2003) Controlling the angiogenic switch: a balance between two distinct TGF-b receptor signaling pathways. Trends Cardiovasc Med 13: 301-307. (Pubitemid 37159396)
5. Eddahibi S, Guignabert C, Barlier-Mur AM, Dewachter L, Fadel E, et al. (2006) Cross talk between endothelial and smooth muscle cells in pulmonary hypertension: critical role for serotonin-induced smooth muscle hyperplasia. Circulation 113: 1857-1864. (Pubitemid 43739397)
6. Eddahibi S, Humbert M, Fadel E, Raffestin B, Darmon M, et al. (2001) Serotonin transporter overexpression is responsible for pulmonary artery smooth muscle hyperplasia in primary pulmonary hypertension. J Clin Invest 108: 1141-1150. (Pubitemid 32995372)
7. Torsney E, Charlton R, Diamond AG, Burn J, Soames JV, et al. (2003) Mouse model for hereditary hemorrhagic telangiectasia has a generalized vascular abnormality. Circulation 107: 1653-1657. (Pubitemid 36397335)
8. Eddahibi S, Hanoun N, Lanfumey L, Lesch KP, Raffestin B, et al. (2000) Attenuated hypoxic pulmonary hypertension in mice lacking the 5-hydroxytryptamine transporter gene. J Clin Invest 105: 1555-1562. (Pubitemid 30390306)
9. Rajkumar R, Konishi K, Richards TJ, Ishizawar DC, Wiechert AC, et al. (2010) Genomewide RNA expression profiling in lung identifies distinct signatures in idiopathic pulmonary arterial hypertension and secondary pulmonary hypertension. Am J Physiol Heart Circ Physiol 298: H1235-1248.
10. Selimovic N, Bergh CH, Andersson B, Sakiniene E, Carlsten H, et al. (2009) Growth factors and interleukin-6 across the lung circulation in pulmonary hypertension. Eur Respir J 34: 662-668.
11. Botney MD, Bahadori L, Gold LI (1994) Vascular remodeling in primary pulmonary hypertension. Potential role for transforming growth factor-beta. Am J Pathol 144: 286-295. (Pubitemid 24165949)
12. Ambalavanan N, Nicola T, Hagood J, Bulger A, Serra R, et al. (2008) Transforming growth factor-beta signaling mediates hypoxia-induced pulmonary arterial remodeling and inhibition of alveolar development in newborn mouse lung. Am J Physiol Lung Cell Mol Physiol 295: L86-95.
13. Long L, Crosby A, Yang X, Southwood M, Upton PD, et al. (2009) Altered bone morphogenetic protein and transforming growth factor-beta signaling in rat models of pulmonary hypertension: potential for activin receptor-like kinase-5 inhibition in prevention and progression of disease. Circulation 119: 566-576.
14. Chen YF, Feng JA, Li P, Xing D, Zhang Y, et al. (2006) Dominant negative mutation of the TGF-beta receptor blocks hypoxia-induced pulmonary vascular remodeling. J Appl Physiol 100: 564-571. (Pubitemid 43671609)
15. Megalou AJ, Glava C, Oikonomidis DL, Vilaeti A, Agelaki MG, et al. (2010) Transforming growth factor-beta inhibition attenuates pulmonary arterial hypertension in rats. Int J Clin Exp Med 3: 332-340.
16. Girerd B, Montani D, Coulet F, Sztrymf B, Yaici A, et al. (2010) Clinical outcomes of pulmonary arterial hypertension in patients carrying an ACVRL1 (ALK1) mutation. Am J Respir Crit Care Med 181: 851-861.
17. Shintani M, Yagi H, Nakayama T, Saji T, Matsuoka R (2009) A new nonsense mutation of SMAD8 associated with pulmonary arterial hypertension. J Med Genet 46: 331-337.
18. Ramos MF, Lame MW, Segall HJ, Wilson DW (2008) Smad signaling in the rat model of monocrotaline pulmonary hypertension. Toxicol Pathol 36: 311-320. (Pubitemid 351534477)
19. Mata-Greenwood E, Meyrick B, Steinhorn RH, Fineman JR, Black SM (2003) Alterations in TGF-beta1 expression in lambs with increased pulmonary blood flow and pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 285: L209-221. (Pubitemid 36736484)
20. Zakrzewicz A, Kouri FM, Nejman B, Kwapiszewska G, Hecker M, et al. (2007) The transforming growth factor-beta/Smad2,3 signalling axis is impaired in experimental pulmonary hypertension. Eur Respir J 29: 1094-1104. (Pubitemid 46895367)
21. Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, et al. (2004) Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J 23: 4018-4028. (Pubitemid 39472423)
22. Hassoun PM, Mouthon L, Barbera JA, Eddahibi S, Flores SC, et al. (2009) Inflammation, growth factors, and pulmonary vascular remodeling. J Am Coll Cardiol 54: S10-19.
23. Humbert M, Morrell NW, Archer SL, Stenmark KR, MacLean MR, et al. (2004) Cellular and molecular pathobiology of pulmonary arterial hypertension. J Am Coll Cardiol 43: 13S-24S. (Pubitemid 38759713)
24. Izikki M, Guignabert C, Fadel E, Humbert M, Tu L, et al. (2009) Endothelial-derived FGF2 contributes to the progression of pulmonary hypertension in humans and rodents. J Clin Invest 119: 512-523.
25. Castanares C, Redondo-Horcajo M, Magan-Marchal N, ten Dijke P, Lamas S, et al. (2007) Signaling by ALK5 mediates TGF-beta-induced ET-1 expression in endothelial cells: a role for migration and proliferation. J Cell Sci 120: 1256-1266. (Pubitemid 46711844)
26. Star GP, Giovinazzo M, Langleben D (2010) Bone morphogenic protein-9 stimulates endothelin-1 release from human pulmonary microvascular endothelial cells: a potential mechanism for elevated ET-1 levels in pulmonary arterial hypertension. Microvasc Res 80: 349-354.
27. Chen Q, Chen L, Liu B, Vialli C, Stone P, et al. (2010) The role of autocrine TGFbeta1 in endothelial cell activation induced by phagocytosis of necrotic trophoblasts: a possible role in the pathogenesis of pre-eclampsia. J Pathol 221: 87-95.
28. Jiang BH, Tardif JC, Sauvageau S, Ducharme A, Shi Y, et al. (2010) Beneficial effects of atorvastatin on lung structural remodeling and function in ischemic heart failure. J Card Fail 16: 679-688.
29. Burton VJ, Ciuclan LI, Holmes AM, Rodman DM, Walker C, et al. (2011) Bone morphogenetic protein receptor II regulates pulmonary artery endothelial cell barrier function. Blood 117: 333-341.
30. Ardelean DS, Yin M, Jerkic M, Peter M, Ngan B, et al. (2014) Anti-VEGF therapy reduces intestinal inflammation in Endoglin heterozygous mice subjected to experimental colitis. Angiogenesis.
31. Perros F, Dorfmuller P, Montani D, Hammad H, Waelput W, et al. (2012) Pulmonary Lymphoid Neogenesis in Idiopathic Pulmonary Arterial Hypertension. Am J Respir Crit Care Med.
32. Tu L, Dewachter L, Gore B, Fadel E, Dartevelle P, et al. (2011) Autocrine fibroblast growth factor-2 signaling contributes to altered endothelial phenotype in pulmonary hypertension. Am J Respir Cell Mol Biol 45: 311-322.