Role of Stromelysin 2 (Matrix Metalloproteinase 10) as a Novel Mediator of Vascular Remodeling Underlying Pulmonary Hypertension Associated With Systemic Sclerosis

Arthritis and Rheumatology

Volumn 69, Issue 11, 2017, Pages 2209-2221

  Avouac, Jérôme ^a   Guignabert, Christophe ^b   Hoffmann Vold, Anna Maria ^c   Ruiz, Barbara ^a   Dorfmuller, Peter ^b   Pezet, Sonia ^a   Amar, Olivia ^a   Tu, Ly ^b   Van Wassenhove, Jérôme ^a   Sadoine, Jérémy ^d   Launay, David ^e   Elhai, Muriel ^a   Cauvet, Anne ^a   Subramaniam, Arun ^f   Resnick, Robert ^f   Hachulla, Eric ^e   Molberg, Øyvind ^c   Kahan, André ^a   Humbert, Marc ^g   Allanore, Yannick ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b INSERM   (France)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d France   (France)

^e UNIV LILLE   (France)

^f SANOFI   (France)

^g Universite Paris Sud   (France)

Author keywords

[No Author keywords available]

Indexed keywords

STROMELYSIN 2; TRANSCRIPTION FACTOR FRA 2; FOSL2 PROTEIN, HUMAN; MMP10 PROTEIN, HUMAN; NEUTRALIZING ANTIBODY; PLATELET DERIVED GROWTH FACTOR;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DOUBLE ANTIBODY SANDWICH ENZYME LINKED IMMUNOSORBENT ASSAY; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; FEMALE; GENE IDENTIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LONGITUDINAL STUDY; LUNG PARENCHYMA; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROSPECTIVE STUDY; PULMONARY ARTERY; PULMONARY HYPERTENSION; SYSTEMIC SCLEROSIS; UPREGULATION; VASCULAR REMODELING; ANIMAL; CASE CONTROL STUDY; CELL PROLIFERATION; CELL SURVIVAL; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; HYPERTENSION, PULMONARY; IMMUNOLOGY; LUNG; METABOLISM; MIDDLE AGED; PULMONARY FIBROSIS; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ADULT; AGED; ANIMALS; ANTIBODIES, NEUTRALIZING; CASE-CONTROL STUDIES; CELL PROLIFERATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENDOTHELIAL PROGENITOR CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FOS-RELATED ANTIGEN-2; HUMANS; HYPERTENSION, PULMONARY; LUNG; MALE; MATRIX METALLOPROTEINASE 10; MICE; MICE, TRANSGENIC; MICROARRAY ANALYSIS; MIDDLE AGED; PLATELET-DERIVED GROWTH FACTOR; PULMONARY ARTERY; PULMONARY FIBROSIS; SCLERODERMA, SYSTEMIC; SIGNAL TRANSDUCTION; VASCULAR REMODELING;

EID: 85031684555     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.40229     Document Type: Article

References (48)

1. Avouac J, Airo P, Meune C, Beretta L, Dieude P, Caramaschi P, et al. Prevalence of pulmonary hypertension in systemic sclerosis in European Caucasians and metaanalysis of 5 studies. J Rheumatol 2010;37:2290–8.
2. Humbert M, Sitbon O, Chaouat A, Bertocchi M, Habib G, Gressin V, et al. Survival in patients with idiopathic, familial, and anorexigen-associated pulmonary arterial hypertension in the modern management era. Circulation 2010;122:156–63.
3. Tyndall AJ, Bannert B, Vonk M, Airo P, Cozzi F, Carreira PE, et al. Causes and risk factors for death in systemic sclerosis: a study from the EULAR Scleroderma Trials and Research (EUSTAR) database. Ann Rheum Dis 2010;69:1809–15.
4. Galie N, Humbert M, Vachiery JL, Gibbs S, Lang I, Torbicki A, et al, and the Joint Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS). 2015 ESC/ERS guidelines for the diagnosis and treatment of pulmonary hypertension. Eur Respir J 2015;46:903–75.
5. Humbert M, Sitbon O, Yaici A, Montani D, O'Callaghan DS, Jais X, et al. Survival in incident and prevalent cohorts of patients with pulmonary arterial hypertension. Eur Respir J 2010;36:549–55.
6. Humbert M, Lau EM, Montani D, Jais X, Sitbon O, Simonneau G. Advances in therapeutic interventions for patients with pulmonary arterial hypertension. Circulation 2014;130:2189–208.
7. Guignabert C, Tu L, Girerd B, Ricard N, Huertas A, Montani D, et al. New molecular targets of pulmonary vascular remodeling in pulmonary arterial hypertension: importance of endothelial communication. Chest 2015;147:529–37.
8. Huertas A, Perros F, Tu L, Cohen-Kaminsky S, Montani D, Dorfmuller P, et al. Immune dysregulation and endothelial dysfunction in pulmonary arterial hypertension: a complex interplay. Circulation 2014;129:1332–40.
9. Tuder RM, Archer SL, Dorfmuller P, Erzurum SC, Guignabert C, Michelakis E, et al. Relevant issues in the pathology and pathobiology of pulmonary hypertension. J Am Coll Cardiol 2013;62 Suppl:D4–12.
10. Avouac J, Juin F, Wipff J, Couraud PO, Chiocchia G, Kahan A, et al. Circulating endothelial progenitor cells in systemic sclerosis: association with disease severity. Ann Rheum Dis 2008;67:1455–60.
11. Avouac J, Wipff J, Goldman O, Ruiz B, Couraud PO, Chiocchia G, et al. Angiogenesis in systemic sclerosis: impaired expression of vascular endothelial growth factor receptor 1 in endothelial progenitor–derived cells under hypoxic conditions. Arthritis Rheum 2008;58:3550–61.
12. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 2004;104:2752–60.
13. Sieveking DP, Buckle A, Celermajer DS, Ng MK. Strikingly different angiogenic properties of endothelial progenitor cell subpopulations: insights from a novel human angiogenesis assay. J Am Coll Cardiol 2008;51:660–8.
14. Avouac J, Cagnard N, Distler JH, Schoindre Y, Ruiz B, Couraud PO, et al. Insights into the pathogenesis of systemic sclerosis based on the gene expression profile of progenitor-derived endothelial cells. Arthritis Rheum 2011;63:3552–62.
15. Toshner M, Voswinckel R, Southwood M, Al-Lamki R, Howard LS, Marchesan D, et al. Evidence of dysfunction of endothelial progenitors in pulmonary arterial hypertension. Am J Respir Crit Care Med 2009;180:780–7.
16. Yeager ME, Frid MG, Stenmark KR. Progenitor cells in pulmonary vascular remodeling. Pulm Circ 2011;1:3–16.
17. Elhai M, Avouac J, Hoffmann-Vold AM, Ruzehaji N, Amiar O, Ruiz B, et al. OX40L blockade protects against inflammation-driven fibrosis. Proc Natl Acad Sci U S A 2016;113:E3901–10.
18. Gomez-Arroyo J, Saleem SJ, Mizuno S, Syed AA, Bogaard HJ, Abbate A, et al. A brief overview of mouse models of pulmonary arterial hypertension: problems and prospects. Am J Physiol Lung Cell Mol Physiol 2012;302:L977–91.
19. Maurer B, Busch N, Jungel A, Pileckyte M, Gay RE, Michel BA, et al. Transcription factor Fos-related antigen-2 induces progressive peripheral vasculopathy in mice closely resembling human systemic sclerosis. Circulation 2009;120:2367–76.
20. Maurer B, Reich N, Juengel A, Kriegsmann J, Gay RE, Schett G, et al. Fra-2 transgenic mice as a novel model of pulmonary hypertension associated with systemic sclerosis. Ann Rheum Dis 2012;71:1382–7.
21. Subcommittee for Scleroderma Criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. Preliminary criteria for the classification of systemic sclerosis (scleroderma). Arthritis Rheum 1980;23:581–90.
22. Hoffmann-Vold AM, Aaløkken TM, Lund MB, Garen T, Midtvedt O, Brunborg C, et al. Predictive value of serial high-resolution computed tomography analyses and concurrent lung function tests in systemic sclerosis. Arthritis Rheumatol 2015;67:2205–12.
23. Hoffmann-Vold AM, Gunnarsson R, Garen T, Midtvedt O, Molberg O. Performance of the 2013 American College of Rheumatology/European League Against Rheumatism classification criteria for systemic sclerosis (SSc) in large, well-defined cohorts of SSc and mixed connective tissue disease. J Rheumatol 2015;42:60–3.
24. Guignabert C, Alvira CM, Alastalo TP, Sawada H, Hansmann G, Zhao M, et al. Tie2-mediated loss of peroxisome proliferator-activated receptor-γ in mice causes PDGF receptor-β-dependent pulmonary arterial muscularization. Am J Physiol Lung Cell Mol Physiol 2009;297:L1082–90.
25. Ricard N, Tu L, Le Hiress M, Huertas A, Phan C, Thuillet R, et al. Increased pericyte coverage mediated by endothelial-derived fibroblast growth factor-2 and interleukin-6 is a source of smooth muscle-like cells in pulmonary hypertension. Circulation 2014;129:1586–97.
26. Huertas A, Tu L, Thuillet R, Le Hiress M, Phan C, Ricard N, et al. Leptin signalling system as a target for pulmonary arterial hypertension therapy. Eur Respir J 2015;45:1066–80.
27. Le Hiress M, Tu L, Ricard N, Phan C, Thuillet R, Fadel E, et al. 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.
28. Ashcroft T, Simpson JM, Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol 1988;41:467–70.
29. Avouac J, Elhai M, Tomcik M, Ruiz B, Friese M, Piedavent M, et al. Critical role of the adhesion receptor DNAX accessory molecule-1 (DNAM-1) in the development of inflammation-driven dermal fibrosis in a mouse model of systemic sclerosis. Ann Rheum Dis 2013;72:1089–98.
30. Ponsoye M, Frantz C, Ruzehaji N, Nicco C, Elhai M, Ruiz B, et al. Treatment with abatacept prevents experimental dermal fibrosis and induces regression of established inflammation-driven fibrosis. Ann Rheum Dis 2016;75:2142–9.
31. Heo SH, Choi YJ, Ryoo HM, Cho JY. Expression profiling of ETS and MMP factors in VEGF-activated endothelial cells: role of MMP-10 in VEGF-induced angiogenesis. J Cell Physiol 2010;224:734–42.
32. Overbeek MJ, Boonstra A, Voskuyl AE, Vonk MC, Vonk-Noordegraaf A, van Berkel MP, et al. Platelet-derived growth factor receptor-β and epidermal growth factor receptor in pulmonary vasculature of systemic sclerosis-associated pulmonary arterial hypertension versus idiopathic pulmonary arterial hypertension and pulmonary veno-occlusive disease: a case-control study. Arthritis Res Ther 2011;13:R61.
33. Batra J, Robinson J, Soares AS, Fields AP, Radisky DC, Radisky ES. Matrix metalloproteinase-10 (MMP-10) interaction with tissue inhibitors of metalloproteinases TIMP-1 and TIMP-2: binding studies and crystal structure. J Biol Chem 2012;287:15935–46.
34. Montani D, Perros F, Gambaryan N, Girerd B, Dorfmuller P, Price LC, et al. C-kit-positive cells accumulate in remodeled vessels of idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med 2011;184:116–23.
35. Chelladurai P, Seeger W, Pullamsetti SS. Matrix metalloproteinases and their inhibitors in pulmonary hypertension. Eur Respir J 2012;40:766–82.
36. Matsui K, Takano Y, Yu ZX, Hi JE, Stetler-Stevenson WG, Travis WD, et al. Immunohistochemical study of endothelin-1 and matrix metalloproteinases in plexogenic pulmonary arteriopathy. Pathol Res Pract 2002;198:403–12.
37. Lepetit H, Eddahibi S, Fadel E, Frisdal E, Munaut C, Noel A, et al. Smooth muscle cell matrix metalloproteinases in idiopathic pulmonary arterial hypertension. Eur Respir J 2005;25:834–42.
38. Hoffmann J, Marsh LM, Pieper M, Stacher E, Ghanim B, Kovacs G, et al. Compartment-specific expression of collagens and their processing enzymes in intrapulmonary arteries of IPAH patients. Am J Physiol Lung Cell Mol Physiol 2015;308:L1002–13.
39. Wei P, Yang Y, Guo X, Hei N, Lai S, Assassi S, et al. Identification of an association of TNFAIP3 polymorphisms with matrix metalloproteinase expression in fibroblasts in an integrative study of systemic sclerosis–associated genetic and environmental factors. Arthritis Rheumatol 2016;68:749–60.
40. Rabinovitch M. Pathobiology of pulmonary hypertension: extracellular matrix. Clin Chest Med 2001;22:433–49, viii.
41. Grigoryev DN, Mathai SC, Fisher MR, Girgis RE, Zaiman AL, Housten-Harris T, et al. Identification of candidate genes in scleroderma-related pulmonary arterial hypertension. Transl Res 2008;151:197–207.
42. Fessing MY, Atoyan R, Shander B, Mardaryev AN, Botchkarev VV Jr, Poterlowicz K, et al. BMP signaling induces cell-type-specific changes in gene expression programs of human keratinocytes and fibroblasts. J Invest Dermatol 2010;130:398–404.
43. Martinez ML, Lopes LF, Coelho EB, Nobre F, Rocha JB, Gerlach RF, et al. Lercanidipine reduces matrix metalloproteinase-9 activity in patients with hypertension. J Cardiovasc Pharmacol 2006;47:117–22.
44. Benisty JI, Folkman J, Zurakowski D, Louis G, Rich S, Langleben D, et al. Matrix metalloproteinases in the urine of patients with pulmonary arterial hypertension. Chest 2005;128 Suppl:572S.
45. Zempo N, Koyama N, Kenagy RD, Lea HJ, Clowes AW. Regulation of vascular smooth muscle cell migration and proliferation in vitro and in injured rat arteries by a synthetic matrix metalloproteinase inhibitor. Arterioscler Thromb Vasc Biol 1996;16:28–33.
46. Sokai A, Handa T, Tanizawa K, Oga T, Uno K, Tsuruyama T, et al. Matrix metalloproteinase-10: a novel biomarker for idiopathic pulmonary fibrosis. Respir Res 2015;16:120.
47. Pullamsetti S, Krick S, Yilmaz H, Ghofrani HA, Schudt C, Weissmann N, et al. Inhaled tolafentrine reverses pulmonary vascular remodeling via inhibition of smooth muscle cell migration. Respir Res 2005;6:128.
48. Antoniu SA. Targeting PDGF pathway in pulmonary arterial hypertension. Expert Opin Ther Targets 2012;16:1055–63.