{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T01:30:11Z","timestamp":1792805411488,"version":"4.5.0"},"reference-count":130,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2023,2,3]],"date-time":"2023-02-03T00:00:00Z","timestamp":1675382400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"NIH","award":["K24AR060297"],"award-info":[{"award-number":["K24AR060297"]}]},{"name":"NIH","award":["R01HL153195"],"award-info":[{"award-number":["R01HL153195"]}]},{"name":"National Scleroderma Foundation","award":["K24AR060297"],"award-info":[{"award-number":["K24AR060297"]}],"id":[{"id":"https:\/\/ror.org\/04g20q935","id-type":"ROR","asserted-by":"crossref"}]},{"name":"National Scleroderma Foundation","award":["R01HL153195"],"award-info":[{"award-number":["R01HL153195"]}],"id":[{"id":"https:\/\/ror.org\/04g20q935","id-type":"ROR","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Systemic sclerosis (SSc), also known as scleroderma, is an autoimmune disorder that affects the connective tissues and has the highest mortality rate among the rheumatic diseases. One of the hallmarks of SSc is fibrosis, which may develop systemically, affecting the skin and virtually any visceral organ in the body. Fibrosis of the lungs leads to interstitial lung disease (ILD), which is currently the leading cause of death in SSc. The identification of effective treatments to stop or reverse lung fibrosis has been the main challenge in reducing SSc mortality and improving patient outcomes and quality of life. Thus, understanding the molecular mechanisms, altered pathways, and their potential interactions in SSc lung fibrosis is key to developing potential therapies. In this review, we discuss the diverse molecular mechanisms involved in SSc-related lung fibrosis to provide insights into the altered homeostasis state inherent to this fatal disease complication.<\/jats:p>","DOI":"10.3390\/ijms24032963","type":"journal-article","created":{"date-parts":[[2023,2,3]],"date-time":"2023-02-03T02:35:10Z","timestamp":1675391710000},"page":"2963","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":34,"title":["The Molecular Mechanisms of Systemic Sclerosis-Associated Lung Fibrosis"],"prefix":"10.3390","volume":"24","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1309-2621","authenticated-orcid":false,"given":"Joe E.","family":"Mouawad","sequence":"first","affiliation":[{"name":"Division of Rheumatology & Immunology, Department of Medicine, Medical University of South Carolina, Charleston, SC 29425, USA"},{"name":"Medical Scientist Training Program, Medical University of South Carolina, Charleston, SC 29425, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6750-6407","authenticated-orcid":false,"given":"Carol","family":"Feghali-Bostwick","sequence":"additional","affiliation":[{"name":"Division of Rheumatology & Immunology, Department of Medicine, Medical University of South Carolina, Charleston, SC 29425, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1685","DOI":"10.1016\/S0140-6736(17)30933-9","article-title":"Systemic sclerosis","volume":"390","author":"Denton","year":"2017","journal-title":"Lancet"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1038\/nrrheum.2014.53","article-title":"Fibrosis-A lethal component of systemic sclerosis","volume":"10","author":"Ho","year":"2014","journal-title":"Nat. Rev. Rheumatol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1016\/S2213-2600(19)30480-1","article-title":"Systemic sclerosis-associated interstitial lung disease","volume":"8","author":"Perelas","year":"2020","journal-title":"Lancet Respir. Med."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"940","DOI":"10.1136\/ard.2006.066068","article-title":"Changes in causes of death in systemic sclerosis, 1972\u20132002","volume":"66","author":"Steen","year":"2007","journal-title":"Ann. Rheum. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1016\/S2213-2600(20)30318-0","article-title":"Tocilizumab in systemic sclerosis: A randomised, double-blind, placebo-controlled, phase 3 trial","volume":"8","author":"Khanna","year":"2020","journal-title":"Lancet Respir. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2518","DOI":"10.1056\/NEJMoa1903076","article-title":"Nintedanib for Systemic Sclerosis\u2013Associated Interstitial Lung Disease","volume":"380","author":"Distler","year":"2019","journal-title":"New Engl. J. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s12931-019-0980-7","article-title":"Interstitial lung disease associated with systemic sclerosis (SSc-ILD)","volume":"20","author":"Cottin","year":"2019","journal-title":"Respir. Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1038\/s41584-018-0062-0","article-title":"Major lung complications of systemic sclerosis","volume":"14","author":"Denton","year":"2018","journal-title":"Nat. Rev. Rheumatol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1002\/art.30159","article-title":"Lung tissues in patients with systemic sclerosis have gene expression patterns unique to pulmonary fibrosis and pulmonary hypertension","volume":"63","author":"Hsu","year":"2011","journal-title":"Arthritis Rheum."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"383","DOI":"10.3389\/fimmu.2020.00383","article-title":"Prominence of IL6, IGF, TLR, and Bioenergetics Pathway Perturbation in Lung Tissues of Scleroderma Patients With Pulmonary Fibrosis","volume":"11","author":"Renaud","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"714","DOI":"10.1002\/art.38288","article-title":"Association of Interferon- and Transforming Growth Factor \u03b2-Regulated Genes and Macrophage Activation With Systemic Sclerosis-Related Progressive Lung Fibrosis","volume":"66","author":"Christmann","year":"2014","journal-title":"Arthritis Rheumatol."},{"key":"ref_12","first-page":"69","article-title":"The mighty fibroblast and its utility in scleroderma research","volume":"2","author":"Garrett","year":"2017","journal-title":"J. Scleroderma Relat. Disord."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1379","DOI":"10.1136\/annrheumdis-2018-214865","article-title":"Single-cell analysis reveals fibroblast heterogeneity and myofibroblasts in systemic sclerosis-associated interstitial lung disease","volume":"78","author":"Valenzi","year":"2019","journal-title":"Ann. Rheum. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Mouawad, J.E., Sharma, S., Renaud, L., Pilewski, J.M., Nadig, S.N., and Feghali-Bostwick, C. (2022). Reduced Cathepsin L Expression and Secretion into the Extracellular Milieu Contribute to Lung Fibrosis in Systemic Sclerosis. Rheumatology, keac411.","DOI":"10.1093\/rheumatology\/keac411"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1016\/j.molcel.2015.04.005","article-title":"The Technology and Biology of Single-Cell RNA Sequencing","volume":"58","author":"Kolodziejczyk","year":"2015","journal-title":"Mol. Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1517","DOI":"10.1164\/rccm.201712-2410OC","article-title":"Single-Cell Transcriptomic Analysis of Human Lung Provides Insights into the Pathobiology of Pulmonary Fibrosis","volume":"199","author":"Reyfman","year":"2019","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1165\/rcmb.2018-0313OC","article-title":"Defining the Activated Fibroblast Population in Lung Fibrosis Using Single-Cell Sequencing","volume":"61","author":"Peyser","year":"2019","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"616","DOI":"10.1038\/nrm3434","article-title":"TGF\u03b2 signalling in context","volume":"13","year":"2012","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1038\/nrneph.2016.48","article-title":"TGF-beta: The master regulator of fibrosis","volume":"12","author":"Meng","year":"2016","journal-title":"Nat. Rev. Nephrol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1002\/jcb.21501","article-title":"TGF-\u03b2 signaling: A tale of two responses","volume":"102","author":"Rahimi","year":"2007","journal-title":"J. Cell. Biochem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2811","DOI":"10.1016\/j.febslet.2006.04.033","article-title":"The logic of TGF\u03b2 signaling","volume":"580","author":"Gomis","year":"2006","journal-title":"FEBS Lett."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e20190103","DOI":"10.1084\/jem.20190103","article-title":"Transforming growth factor\u2013\u03b2 in tissue fibrosis","volume":"217","author":"Frangogiannis","year":"2020","journal-title":"J. Exp. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1038\/ki.2014.287","article-title":"Origin of myofibroblasts and cellular events triggering fibrosis","volume":"87","author":"Mack","year":"2015","journal-title":"Kidney Int."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"706","DOI":"10.1038\/nrrheum.2014.137","article-title":"Transforming growth factor beta--at the centre of systemic sclerosis","volume":"10","author":"Lafyatis","year":"2014","journal-title":"Nat. Rev. Rheumatol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3","DOI":"10.7555\/JBR.31.20170034","article-title":"Transforming growth factor-\u03b2 signaling in systemic sclerosis","volume":"32","author":"Ayers","year":"2018","journal-title":"J. Biomed. Res."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Garrett, S.M., Hsu, E., Thomas, J.M., Pilewski, J.M., and Feghali-Bostwick, C. (2019). Insulin-like growth factor (IGF)-II-mediated fibrosis in pathogenic lung conditions. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0225422"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1038\/mt.2016.36","article-title":"Chop Deficiency Protects Mice Against Bleomycin-induced Pulmonary Fibrosis by Attenuating M2 Macrophage Production","volume":"24","author":"Yao","year":"2016","journal-title":"Mol. Ther."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"eabb6075","DOI":"10.1126\/sciadv.abb6075","article-title":"MBD2 serves as a viable target against pulmonary fibrosis by inhibiting macrophage M2 program","volume":"7","author":"Wang","year":"2021","journal-title":"Sci. Adv."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"4404","DOI":"10.1038\/s41467-021-24601-y","article-title":"TGF\u03b2 promotes fibrosis by MYST1-dependent epigenetic regulation of autophagy","volume":"12","author":"Zehender","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Saito, A., Horie, M., and Nagase, T. (2018). TGF-\u03b2 Signaling in Lung Health and Disease. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19082460"},{"key":"ref_31","first-page":"8","article-title":"Targeting TGF-\u03b2 signaling for the treatment of fibrosis","volume":"68\u201369","author":"Matei","year":"2018","journal-title":"Matrix Biol. J. Int. Soc. Matrix Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"jcs234039","DOI":"10.1242\/jcs.234039","article-title":"TGF-\u03b2 family ligands exhibit distinct signalling dynamics that are driven by receptor localisation","volume":"132","author":"Miller","year":"2019","journal-title":"J. Cell Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.mam.2017.11.008","article-title":"PDGF in organ fibrosis","volume":"62","author":"Klinkhammer","year":"2018","journal-title":"Mol. Aspects Med."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1276","DOI":"10.1101\/gad.1653708","article-title":"Role of platelet-derived growth factors in physiology and medicine","volume":"22","author":"Andrae","year":"2008","journal-title":"Genes Dev."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1002\/bdrc.10030","article-title":"Biology of platelet-derived growth factors in development","volume":"69","author":"Betsholtz","year":"2003","journal-title":"Birth Defects Res. C Embryo Today"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"745308","DOI":"10.3389\/fimmu.2021.745308","article-title":"PDGF Promotes Dermal Fibroblast Activation via a Novel Mechanism Mediated by Signaling Through MCHR1","volume":"12","author":"Takamura","year":"2021","journal-title":"Front. Immunol."},{"key":"ref_37","first-page":"1876","article-title":"Elevated levels of platelet derived growth factor and transforming growth factor-beta 1 in bronchoalveolar lavage fluid from patients with scleroderma","volume":"22","author":"Ludwicka","year":"1995","journal-title":"J. Rheumatol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"v2","DOI":"10.1093\/rheumatology\/ken265","article-title":"Role of PDGF in fibrotic diseases and systemic sclerosis","volume":"47","author":"Trojanowska","year":"2008","journal-title":"Rheumatology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1963","DOI":"10.1093\/rheumatology\/ket254","article-title":"Alteration of circulating miRNAs in SSc: miR-30b regulates the expression of PDGF receptor \u03b2","volume":"52","author":"Tanaka","year":"2013","journal-title":"Rheumatology"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1891","DOI":"10.1002\/art.39125","article-title":"Epitope specificity determines pathogenicity and detectability of anti-PDGFR\u03b1 autoantibodies in systemic sclerosis","volume":"67","author":"Moroncini","year":"2015","journal-title":"Arthritis Rheumatol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.autrev.2007.02.020","article-title":"Stimulatory autoantibodies to the PDGF receptor: A link to fibrosis in scleroderma and a pathway for novel therapeutic targets","volume":"7","author":"Gabrielli","year":"2007","journal-title":"Autoimmun. Rev."},{"key":"ref_42","first-page":"75","article-title":"Agonistic Anti-PDGF Receptor Autoantibodies from Patients with Systemic Sclerosis Impact Human Pulmonary Artery Smooth Muscle Cells Function In Vitro","volume":"8","author":"Svegliati","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Paolini, C., Agarbati, S., Benfaremo, D., Mozzicafreddo, M., Svegliati, S., and Moroncini, G. (2022). PDGF\/PDGFR: A Possible Molecular Target in Scleroderma Fibrosis. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23073904"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1124\/jpet.113.208223","article-title":"Antifibrotic and anti-inflammatory activity of the tyrosine kinase inhibitor nintedanib in experimental models of lung fibrosis","volume":"349","author":"Wollin","year":"2014","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1002\/wdev.176","article-title":"The Fibroblast Growth Factor signaling pathway","volume":"4","author":"Ornitz","year":"2015","journal-title":"WIREs Dev. Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"34226","DOI":"10.1074\/jbc.M303183200","article-title":"Fibroblast growth factor (FGF) homologous factors share structural but not functional homology with FGFs","volume":"278","author":"Olsen","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"210356","DOI":"10.1098\/rsob.210356","article-title":"Functions of exogenous FGF signals in regulation of fibroblast to myofibroblast differentiation and extracellular matrix protein expression","volume":"12","author":"Sun","year":"2022","journal-title":"Open. Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1159\/000501145","article-title":"Fibroblast Growth Factors: A Controlling Mechanism of Skin Aging","volume":"32","author":"Trindade","year":"2019","journal-title":"Ski. Pharmacol. Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1165\/rcmb.2021-0246OC","article-title":"FGF19 Is Downregulated in Idiopathic Pulmonary Fibrosis and Inhibits Lung Fibrosis in Mice","volume":"67","author":"Justet","year":"2022","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"eaaz5506","DOI":"10.1126\/scitranslmed.aaz5506","article-title":"Fibroblast growth factor receptor 3 activates a network of profibrotic signaling pathways to promote fibrosis in systemic sclerosis","volume":"12","author":"Chakraborty","year":"2020","journal-title":"Sci. Transl. Med."},{"key":"ref_51","first-page":"960","article-title":"Targeting the Wnt Signaling Pathway in Liver Fibrosis for Drug Options: An Update","volume":"9","author":"Duspara","year":"2021","journal-title":"J. Clin. Transl. Hepatol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1002\/med.21853","article-title":"The role of Wnt signaling in skin fibrosis","volume":"42","author":"Griffin","year":"2022","journal-title":"Med. Res. Rev."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1165\/rcmb.2020-0499OC","article-title":"Noncanonical Wnt Signaling Promotes Myofibroblast Differentiation in Pulmonary Fibrosis","volume":"65","author":"Liu","year":"2021","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"14886","DOI":"10.1038\/s41598-021-94169-6","article-title":"Inhibition of the canonical Wnt signaling pathway by a \u03b2-catenin\/CBP inhibitor prevents heart failure by ameliorating cardiac hypertrophy and fibrosis","volume":"11","author":"Methatham","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"5598","DOI":"10.1002\/jcp.26265","article-title":"The roles of Wnt\/\u03b2-catenin pathway in tissue development and regenerative medicine","volume":"233","author":"Majidinia","year":"2018","journal-title":"J. Cell. Physiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1038\/ncomms1734","article-title":"Activation of canonical Wnt signalling is required for TGF-\u03b2-mediated fibrosis","volume":"3","author":"Akhmetshina","year":"2012","journal-title":"Nat. Commun."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1165\/rcmb.2010-0113OC","article-title":"Nuclear \u03b2-catenin is increased in systemic sclerosis pulmonary fibrosis and promotes lung fibroblast migration and proliferation","volume":"45","author":"Lam","year":"2011","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"5164","DOI":"10.1074\/jbc.M111.322123","article-title":"Axin pathway activity regulates in vivo pY654-\u03b2-catenin accumulation and pulmonary fibrosis","volume":"287","author":"Ulsamer","year":"2012","journal-title":"J. Biol. Chem."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1038\/labinvest.2015.154","article-title":"Canonical Wnt signaling in systemic sclerosis","volume":"96","author":"Bergmann","year":"2016","journal-title":"Lab. Investig."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1002\/art.42063","article-title":"Involvement of Multiple Variants of Soluble CD146 in Systemic Sclerosis: Identification of a Novel Profibrotic Factor","volume":"74","author":"Nollet","year":"2022","journal-title":"Arthritis Rheumatol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1136\/annrheumdis-2011-200568","article-title":"\u03b2-catenin is a central mediator of pro-fibrotic Wnt signaling in systemic sclerosis","volume":"71","author":"Beyer","year":"2012","journal-title":"Ann. Rheum. Dis."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"984","DOI":"10.1016\/j.jaci.2016.06.033","article-title":"Interleukins (from IL-1 to IL-38), interferons, transforming growth factor \u03b2, and TNF-\u03b1: Receptors, functions, and roles in diseases","volume":"138","author":"Akdis","year":"2016","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1186\/1479-7364-5-1-30","article-title":"Evolutionary divergence and functions of the human interleukin (IL) gene family","volume":"5","author":"Brocker","year":"2010","journal-title":"Hum. Genom."},{"key":"ref_64","unstructured":"Vaillant, J.A.A., and Qurie, A. (2021). Interleukin, StatPearls Publishing."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1038\/s41420-021-00437-9","article-title":"Role of interleukins in the pathogenesis of pulmonary fibrosis","volume":"7","author":"She","year":"2021","journal-title":"Cell Death Discov."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"309","DOI":"10.3109\/08916939409010671","article-title":"Control of Il-6 Expression and Response in Fibroblasts from Patients with Systemic Sclerosis","volume":"17","author":"Feghali","year":"1994","journal-title":"Autoimmunity"},{"key":"ref_67","first-page":"308","article-title":"Serum levels of interleukin 6 (IL-6), oncostatin M, soluble IL-6 receptor, and soluble gp130 in patients with systemic sclerosis","volume":"25","author":"Hasegawa","year":"1998","journal-title":"J. Rheumatol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/S0923-1811(01)00128-1","article-title":"Serum levels of interleukin-6 and interleukin-10 correlate with total skin thickness score in patients with systemic sclerosis","volume":"27","author":"Sato","year":"2001","journal-title":"J. Dermatol. Sci."},{"key":"ref_69","first-page":"1207","article-title":"Mechanisms of pathogenesis in scleroderma. I. Overproduction of interleukin 6 by fibroblasts cultured from affected skin sites of patients with scleroderma","volume":"19","author":"Feghali","year":"1992","journal-title":"J. Rheumatol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.ejcdt.2014.10.004","article-title":"Interleukin-6 in systemic sclerosis and potential correlation with pulmonary involvement","volume":"64","author":"Yousif","year":"2015","journal-title":"Egypt. J. Chest Dis. Tuberc."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"L29","DOI":"10.1152\/ajplung.00173.2020","article-title":"Lysyl oxidase directly contributes to extracellular matrix production and fibrosis in systemic sclerosis","volume":"320","author":"Nguyen","year":"2021","journal-title":"Am. J. Physiol. Lung Cell Mol. Physiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1002\/art.41668","article-title":"Tocilizumab Prevents Progression of Early Systemic Sclerosis-Associated Interstitial Lung Disease","volume":"73","author":"Roofeh","year":"2021","journal-title":"Arthritis Rheumatol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1164\/rccm.202103-0714OC","article-title":"Long-Term Safety and Efficacy of Tocilizumab in Early Systemic Sclerosis-Interstitial Lung Disease: Open-Label Extension of a Phase 3 Randomized Controlled Trial","volume":"205","author":"Khanna","year":"2022","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"2625","DOI":"10.1093\/rheumatology\/keaa195","article-title":"Interleukin-31 promotes pathogenic mechanisms underlying skin and lung fibrosis in scleroderma","volume":"59","author":"Yaseen","year":"2020","journal-title":"Rheumatology"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1186\/1465-9921-14-80","article-title":"Microarray profiling reveals suppressed interferon stimulated gene program in fibroblasts from scleroderma-associated interstitial lung disease","volume":"14","author":"Lindahl","year":"2013","journal-title":"Respir. Res."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1146\/annurev-med-041818-011649","article-title":"Hiding in Plain Sight: Interleukin-11 Emerges as a Master Regulator of Fibrosis, Tissue Integrity, and Stromal Inflammation","volume":"71","author":"Cook","year":"2020","journal-title":"Annu. Rev. Med."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"11802","DOI":"10.1096\/fj.202001045RR","article-title":"Fibroblast-specific IL11 signaling is required for lung fibrosis and inflammation","volume":"34","author":"Ng","year":"2020","journal-title":"FASEB J."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1186\/s13075-017-1331-z","article-title":"Mir-155 is overexpressed in systemic sclerosis fibroblasts and is required for NLRP3 inflammasome-mediated collagen synthesis during fibrosis","volume":"19","author":"Artlett","year":"2017","journal-title":"Arthritis Res. Ther."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1135","DOI":"10.1007\/s00296-019-04317-5","article-title":"Interleukin-17 pathways in systemic sclerosis-associated fibrosis","volume":"39","author":"Ahmed","year":"2019","journal-title":"Rheumatol. Int."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1216","DOI":"10.1111\/1346-8138.14538","article-title":"Serum interleukin-34 levels in patients with systemic sclerosis: Clinical association with interstitial lung disease","volume":"45","author":"Kuzumi","year":"2018","journal-title":"J. Dermatol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"825567","DOI":"10.3389\/fmed.2022.825567","article-title":"IL-13 and IL-33 Serum Levels Are Increased in Systemic Sclerosis Patients With Interstitial Lung Disease","volume":"9","author":"Versace","year":"2022","journal-title":"Front. Med."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"107","DOI":"10.4103\/injr.injr_106_17","article-title":"Serum Interleukin-6, Interleukin-17A, and transforming growth factor beta are raised in systemic sclerosis with interstitial lung disease","volume":"13","author":"Wakhlu","year":"2018","journal-title":"Indian J. Rheumatol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1042\/cs0860141","article-title":"Insulin\u2014Like Growth Factor-1 is Partially Responsible for Fibroblast Proliferation Induced by Bronchoalveolar Lavage Fluid from Patients with Systemic Sclerosis","volume":"86","author":"Harrison","year":"1994","journal-title":"Clin. Sci."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1580","DOI":"10.2353\/ajpath.2008.071021","article-title":"Insulin-like growth factor-II is increased in systemic sclerosis-associated pulmonary fibrosis and contributes to the fibrotic process via Jun N-terminal kinase- and phosphatidylinositol-3 kinase-dependent pathways","volume":"172","author":"Hsu","year":"2008","journal-title":"Am. J. Pathol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1016\/S0002-9440(10)62263-8","article-title":"Insulin-Like Growth Factor Binding Proteins 3 and 5 Are Overexpressed in Idiopathic Pulmonary Fibrosis and Contribute to Extracellular Matrix Deposition","volume":"166","author":"Pilewski","year":"2005","journal-title":"Am. J. Pathol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1002\/art.30647","article-title":"Localized expression of tenascin in systemic sclerosis-associated pulmonary fibrosis and its regulation by insulin-like growth factor binding protein 3","volume":"64","author":"Brissett","year":"2012","journal-title":"Arthritis Rheum."},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Ruiz, X.D., Mlakar, L.R., Yamaguchi, Y., Su, Y., Larregina, A.T., Pilewski, J.M., and Feghali-Bostwick, C.A. (2012). Syndecan-2 is a novel target of insulin-like growth factor binding protein-3 and is over-expressed in fibrosis. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0043049"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"601","DOI":"10.3389\/fendo.2018.00601","article-title":"IGFBP-5 Promotes Fibrosis via Increasing Its Own Expression and That of Other Pro-fibrotic Mediators","volume":"9","author":"Nguyen","year":"2018","journal-title":"Front. Endocrinol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1165\/rcmb.2008-0211OC","article-title":"The Pro-Fibrotic Factor IGFBP-5 Induces Lung Fibroblast and Mononuclear Cell Migration","volume":"41","author":"Yasuoka","year":"2009","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Nguyen, X.X., Sanderson, M., Helke, K., and Feghali-Bostwick, C. (2020). Phenotypic Characterization of Transgenic Mice Expressing Human IGFBP-5. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22010335"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"10882","DOI":"10.1038\/s41598-021-90333-0","article-title":"Serum IGFBP-2 in systemic sclerosis as a prognostic factor of lung dysfunction","volume":"11","author":"Guiot","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"862","DOI":"10.1101\/gad.1909210","article-title":"The Hippo-YAP pathway in organ size control and tumorigenesis: An updated version","volume":"24","author":"Zhao","year":"2010","journal-title":"Genes Dev."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"5798","DOI":"10.1111\/febs.16091","article-title":"Role of the Hippo pathway and mechanisms for controlling cellular localization of YAP\/TAZ","volume":"289","author":"Kwon","year":"2022","journal-title":"FEBS J."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1743","DOI":"10.1038\/onc.2011.363","article-title":"Integrating developmental signals: A Hippo in the (path)way","volume":"31","author":"Mauviel","year":"2012","journal-title":"Oncogene"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"L344","DOI":"10.1152\/ajplung.00300.2014","article-title":"Mechanosignaling through YAP and TAZ drives fibroblast activation and fibrosis","volume":"308","author":"Liu","year":"2015","journal-title":"Am. J. Physiol. Lung Cell. Mol. Physiol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"e146243","DOI":"10.1172\/jci.insight.146243","article-title":"Myofibroblast YAP\/TAZ activation is a key step in organ fibrogenesis","volume":"7","author":"He","year":"2022","journal-title":"JCI Insight"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.jid.2017.08.024","article-title":"Therapeutic Targeting of TAZ and YAP by Dimethyl Fumarate in Systemic Sclerosis Fibrosis","volume":"138","author":"Toyama","year":"2018","journal-title":"J. Investig. Dermatol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"106257","DOI":"10.1016\/j.biocel.2022.106257","article-title":"Single-cell sequencing reveals the antifibrotic effects of YAP\/TAZ in systemic sclerosis","volume":"149","author":"Wu","year":"2022","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1146\/annurev.immunol.22.012703.104543","article-title":"Chemokines in innate and adaptive host defense: Basic chemokinese grammar for immune cells","volume":"22","author":"Rot","year":"2004","journal-title":"Annu. Rev. Immunol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1115","DOI":"10.1136\/ard.2010.137349","article-title":"An investigation of the inflammatory cytokine and chemokine network in systemic sclerosis","volume":"70","author":"Codullo","year":"2011","journal-title":"Ann. Rheum. Dis."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"R111","DOI":"10.1186\/ar2766","article-title":"Bronchoalveoloar lavage fluid cytokines and chemokines as markers and predictors for the outcome of interstitial lung disease in systemic sclerosis patients","volume":"11","author":"Schmidt","year":"2009","journal-title":"Arthritis Res. Ther."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"2917","DOI":"10.1002\/art.38101","article-title":"Skin gene expression correlates of severity of interstitial lung disease in systemic sclerosis","volume":"65","author":"Assassi","year":"2013","journal-title":"Arthritis Rheum."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"1871","DOI":"10.1002\/art.40171","article-title":"CCL2 in the Circulation Predicts Long-Term Progression of Interstitial Lung Disease in Patients With Early Systemic Sclerosis: Data From Two Independent Cohorts","volume":"69","author":"Wu","year":"2017","journal-title":"Arthritis Rheumatol."},{"key":"ref_104","first-page":"433","article-title":"Proteome-wide Analysis and CXCL4 as a Biomarker in Systemic Sclerosis","volume":"370","author":"Affandi","year":"2013","journal-title":"N. Engl. J. Med."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"110189","DOI":"10.1016\/j.celrep.2021.110189","article-title":"CXCL4 drives fibrosis by promoting several key cellular and molecular processes","volume":"38","author":"Affandi","year":"2022","journal-title":"Cell Rep."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1186\/s13075-018-1545-8","article-title":"Antibodies against chemokine receptors CXCR3 and CXCR4 predict progressive deterioration of lung function in patients with systemic sclerosis","volume":"20","author":"Weigold","year":"2018","journal-title":"Arthritis Res. Ther."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"972","DOI":"10.1002\/art.40815","article-title":"Performance of Candidate Serum Biomarkers for Systemic Sclerosis-Associated Interstitial Lung Disease","volume":"71","author":"Elhai","year":"2019","journal-title":"Arthritis Rheumatol."},{"key":"ref_108","doi-asserted-by":"crossref","unstructured":"Yadati, T., Houben, T., Bitorina, A., and Shiri-Sverdlov, R. (2020). The Ins and Outs of Cathepsins: Physiological Function and Role in Disease Management. Cells, 9.","DOI":"10.3390\/cells9071679"},{"key":"ref_109","doi-asserted-by":"crossref","unstructured":"Vidak, E., Javor\u0161ek, U., Vizovi\u0161ek, M., and Turk, B. (2019). Cysteine Cathepsins and their Extracellular Roles: Shaping the Microenvironment. Cells, 8.","DOI":"10.3390\/cells8030264"},{"key":"ref_110","first-page":"141","article-title":"Cysteine cathepsins in extracellular matrix remodeling: Extracellular matrix degradation and beyond","volume":"75\u201376","author":"Turk","year":"2019","journal-title":"Matrix Biol. J. Int. Soc. Matrix Biol."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1111\/1346-8138.15458","article-title":"Decreased serum cathepsin S levels in patients with systemic sclerosis-associated interstitial lung disease","volume":"47","author":"Toyama","year":"2020","journal-title":"J. Dermatol."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"136ra171","DOI":"10.1126\/scitranslmed.3003421","article-title":"A peptide derived from endostatin ameliorates organ fibrosis","volume":"4","author":"Yamaguchi","year":"2012","journal-title":"Sci. Transl. Med."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1111\/iwj.12882","article-title":"Serum level of endostatin and digital ulcers in systemic sclerosis patients","volume":"15","author":"Gigante","year":"2018","journal-title":"Int. Wound J."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1136\/thx.2008.102814","article-title":"Soluble endostatin is a novel inhibitor of epithelial repair in idiopathic pulmonary fibrosis","volume":"64","author":"Richter","year":"2009","journal-title":"Thorax"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"714","DOI":"10.1124\/pharmrev.121.000349","article-title":"Matrix metalloproteinases: From molecular mechanisms to physiology, pathophysiology, and pharmacology","volume":"74","author":"Thode","year":"2022","journal-title":"Pharmacol. Rev."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"L511","DOI":"10.1152\/ajplung.00043.2014","article-title":"Matrix metalloproteinase (MMP)-19-deficient fibroblasts display a profibrotic phenotype","volume":"308","author":"Jara","year":"2015","journal-title":"Am. J. Physiology. Lung Cell. Mol. Physiol."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1164\/rccm.201202-0302OC","article-title":"Matrix metalloproteinase-19 is a key regulator of lung fibrosis in mice and humans","volume":"186","author":"Yu","year":"2012","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"e144935","DOI":"10.1172\/jci.insight.144935","article-title":"E4 engages uPAR and enolase-1 and activates urokinase to exert antifibrotic effects","volume":"6","author":"Sharma","year":"2021","journal-title":"JCI Insight"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1165\/rcmb.2016-0192OC","article-title":"Sirtuin1 Protects against Systemic Sclerosis\u2013related Pulmonary Fibrosis by Decreasing Proinflammatory and Profibrotic Processes","volume":"58","author":"Chu","year":"2017","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"69321","DOI":"10.18632\/oncotarget.12504","article-title":"SIRT3 is attenuated in systemic sclerosis skin and lungs, and its pharmacologic activation mitigates organ fibrosis","volume":"7","author":"Akamata","year":"2016","journal-title":"Oncotarget"},{"key":"ref_121","doi-asserted-by":"crossref","unstructured":"Manetti, M., Rosa, I., Fioretto, B.S., Matucci-Cerinic, M., and Romano, E. (2022). Decreased Serum Levels of SIRT1 and SIRT3 Correlate with Severity of Skin and Lung Fibrosis and Peripheral Microvasculopathy in Systemic Sclerosis. J. Clin. Med., 11.","DOI":"10.3390\/jcm11051362"},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"L945","DOI":"10.1152\/ajplung.00473.2016","article-title":"Sirtuin 7 is decreased in pulmonary fibrosis and regulates the fibrotic phenotype of lung fibroblasts","volume":"312","author":"Wyman","year":"2017","journal-title":"Am. J. Physiology. Lung Cell. Mol. Physiol."},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1096\/fba.2018-00015","article-title":"Insulin-like growth factor binding protein-4 exerts antifibrotic activity by reducing levels of connective tissue growth factor and the C-X-C chemokine receptor 4","volume":"1","author":"Su","year":"2019","journal-title":"FASEB Bioadvances"},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/j.lfs.2018.12.041","article-title":"Dynamic decreased expression and hypermethylation of secreted frizzled-related protein 1 and 4 over the course of pulmonary fibrosis in mice","volume":"218","author":"Zhou","year":"2019","journal-title":"Life Sci."},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"1232","DOI":"10.1136\/annrheumdis-2012-203194","article-title":"The Wnt antagonists DKK1 and SFRP1 are downregulated by promoter hypermethylation in systemic sclerosis","volume":"73","author":"Dees","year":"2014","journal-title":"Ann. Rheum. Dis."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1093\/rheumatology\/key327","article-title":"Methyl cap binding protein 2: A key epigenetic protein in systemic sclerosis","volume":"58","author":"Henderson","year":"2018","journal-title":"Rheumatology"},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"576362","DOI":"10.3389\/fonc.2020.576362","article-title":"Identification of Novel MeCP2 Cancer-Associated Target Genes and Post-Translational Modifications","volume":"10","author":"Vartak","year":"2020","journal-title":"Front. Oncol."},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"808","DOI":"10.1080\/15592294.2020.1827715","article-title":"microRNA27a-3p mediates reduction of the Wnt antagonist sFRP-1 in systemic sclerosis","volume":"16","author":"Henderson","year":"2021","journal-title":"Epigenetics"},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"3603","DOI":"10.1111\/febs.16039","article-title":"Collagen VI as a driver and disease biomarker in human fibrosis","volume":"289","author":"Williams","year":"2022","journal-title":"Febs J."},{"key":"ref_130","first-page":"176","article-title":"Extracellular matrix-derived peptides in tissue remodeling and fibrosis","volume":"91\u201392","author":"Frangogiannis","year":"2020","journal-title":"Matrix Biol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/3\/2963\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:23:00Z","timestamp":1760120580000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/3\/2963"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,3]]},"references-count":130,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["ijms24032963"],"URL":"https:\/\/doi.org\/10.3390\/ijms24032963","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,3]]}}}