{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T01:17:00Z","timestamp":1790126220680,"version":"4.0.1"},"reference-count":36,"publisher":"Springer Science and Business Media LLC","issue":"6","license":[{"start":{"date-parts":[[2024,4,11]],"date-time":"2024-04-11T00:00:00Z","timestamp":1712793600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2024,4,11]],"date-time":"2024-04-11T00:00:00Z","timestamp":1712793600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"funder":[{"name":"JSPS KAKENHI","award":["JP19K09314"],"award-info":[{"award-number":["JP19K09314"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Int J Clin Oncol"],"published-print":{"date-parts":[[2024,6]]},"DOI":"10.1007\/s10147-024-02507-1","type":"journal-article","created":{"date-parts":[[2024,4,10]],"date-time":"2024-04-10T23:30:52Z","timestamp":1712791852000},"page":"771-779","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Progressive changes in the protein expression profile of alveolar septa in early-stage lung adenocarcinoma"],"prefix":"10.1007","volume":"29","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4504-232X","authenticated-orcid":false,"given":"Toru","family":"Kimura","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takashi","family":"Akazawa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Mizote","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Harumi","family":"Nakamura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miki","family":"Sakaue","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomohiro","family":"Maniwa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasushi","family":"Shintani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Keiichiro","family":"Honma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hideaki","family":"Tahara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiro","family":"Okami","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,4,11]]},"reference":[{"key":"2507_CR1","doi-asserted-by":"publisher","first-page":"102237","DOI":"10.1016\/j.ctrv.2021.102237","volume":"99","author":"L Succony","year":"2021","unstructured":"Succony L, Rassl DM, Barker AP et al (2021) Adenocarcinoma spectrum lesions of the lung: detection, pathology and treatment strategies. Cancer Treat Rev 99:102237","journal-title":"Cancer Treat Rev"},{"key":"2507_CR2","unstructured":"World Health Organization (2021). Thoracic tumours, WHO classification of Tumours, 5th Edition, Volume 5. International Agency for Research on Cancer"},{"key":"2507_CR3","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1007\/s10555-010-9210-y","volume":"29","author":"M Noguchi","year":"2010","unstructured":"Noguchi M (2010) Stepwise progression of pulmonary adenocarcinoma-clinical and molecular implications. Cancer Metastasis Rev 29:15\u201321","journal-title":"Cancer Metastasis Rev"},{"key":"2507_CR4","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1097\/JTO.0b013e318206a221","volume":"6","author":"WD Travis","year":"2011","unstructured":"Travis WD, Brambilla E, Noguchi M et al (2011) International association for the study of lung cancer\/american thoracic society\/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol 6:244\u2013285","journal-title":"J Thorac Oncol"},{"key":"2507_CR5","doi-asserted-by":"publisher","first-page":"392","DOI":"10.1038\/nrc1877","volume":"6","author":"R Kalluri","year":"2006","unstructured":"Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. Nat Rev Cancer 6:392\u2013401","journal-title":"Nat Rev Cancer"},{"key":"2507_CR6","doi-asserted-by":"publisher","first-page":"792","DOI":"10.1038\/s41571-021-00546-5","volume":"18","author":"Y Chen","year":"2021","unstructured":"Chen Y, McAndrews KM, Kalluri R (2021) Clinical and therapeutic relevance of cancer-associated fibroblasts. Nat Rev Clin Oncol 18:792\u2013804","journal-title":"Nat Rev Clin Oncol"},{"key":"2507_CR7","doi-asserted-by":"publisher","first-page":"22288","DOI":"10.1038\/srep22288","volume":"6","author":"K Maeda","year":"2016","unstructured":"Maeda K, Enomoto A, Hara A et al (2016) Identification of Meflin as a potential marker for mesenchymal stromal cells. Sci Rep 6:22288","journal-title":"Sci Rep"},{"key":"2507_CR8","doi-asserted-by":"publisher","first-page":"1224","DOI":"10.1053\/j.gastro.2020.11.011","volume":"160","author":"H Kobayashi","year":"2021","unstructured":"Kobayashi H, Gieniec KA, Wright JA (2021) The balance of stromal BMP signaling mediated by GREM1 and ISLR drives colorectal carcinogenesis. Gastroenterology 160:1224-1239.e30","journal-title":"Gastroenterology"},{"key":"2507_CR9","doi-asserted-by":"publisher","first-page":"5367","DOI":"10.1158\/0008-5472.CAN-19-0454","volume":"79","author":"Y Mizutani","year":"2019","unstructured":"Mizutani Y, Kobayashi H, Iida T et al (2019) Meflin-positive cancer-associated fibroblasts inhibit pancreatic carcinogenesis. Cancer Res 79:5367\u20135381","journal-title":"Cancer Res"},{"key":"2507_CR10","doi-asserted-by":"publisher","first-page":"e202101230","DOI":"10.26508\/lsa.202101230","volume":"5","author":"Y Miyai","year":"2022","unstructured":"Miyai Y, Sugiyama D, Hase T et al (2022) Meflin-positive cancer-associated fibroblasts enhance tumor response to immune checkpoint blockade. Life Sci Alliance 5:e202101230","journal-title":"Life Sci Alliance"},{"key":"2507_CR11","doi-asserted-by":"publisher","first-page":"62","DOI":"10.3389\/fonc.2014.00062","volume":"4","author":"M Augsten","year":"2014","unstructured":"Augsten M (2014) Cancer-associated fibroblasts as another polarized cell type of the tumor microenvironment. Front Oncol 4:62","journal-title":"Front Oncol"},{"key":"2507_CR12","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1016\/j.matbio.2017.12.003","volume":"67","author":"D Avery","year":"2018","unstructured":"Avery D, Govindaraju P, Jacob M et al (2018) Extracellular matrix directs phenotypic heterogeneity of activated fibroblasts. Matrix Biol 67:90\u2013106","journal-title":"Matrix Biol"},{"key":"2507_CR13","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1084\/jem.20162024","volume":"214","author":"D \u00d6hlund","year":"2017","unstructured":"\u00d6hlund D, Handly-Santana A, Biffi G et al (2017) Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer. J Exp Med 214:579\u2013596","journal-title":"J Exp Med"},{"key":"2507_CR14","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1016\/0888-7543(95)80157-H","volume":"25","author":"S Mathew","year":"1995","unstructured":"Mathew S, Scanlan MJ, Mohan Raj BK et al (1995) The gene for fibroblast activation protein \u03b1 (FAP), a putative cell surface-bound serine protease expressed in cancer stroma and wound healing, maps to chromosome band 2q23. Genomics 25:335\u2013337","journal-title":"Genomics"},{"key":"2507_CR15","doi-asserted-by":"publisher","first-page":"L271","DOI":"10.1152\/ajplung.00071.2019","volume":"317","author":"T Kimura","year":"2019","unstructured":"Kimura T, Monslow J, Klampatsa A et al (2019) Loss of cells expressing fibroblast activation protein has variable effects in models of TGF-\u03b2 and chronic bleomycin-induced fibrosis. Am J Physiol Lung Cell Mol Physiol 317:L271\u2013L282","journal-title":"Am J Physiol Lung Cell Mol Physiol"},{"key":"2507_CR16","doi-asserted-by":"publisher","first-page":"4343","DOI":"10.1038\/s41388-018-0275-3","volume":"37","author":"E Pur\u00e9","year":"2018","unstructured":"Pur\u00e9 E, Blomberg R (2018) Pro-tumorigenic roles of fibroblast activation protein in cancer: back to the basics. Oncogene 37:4343\u20134357","journal-title":"Oncogene"},{"key":"2507_CR17","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1007\/s10555-020-09909-3","volume":"39","author":"AA Fitzgerald","year":"2020","unstructured":"Fitzgerald AA, Weiner LM (2020) The role of fibroblast activation protein in health and malignancy. Cancer Metastasis Rev 39:783\u2013803","journal-title":"Cancer Metastasis Rev"},{"key":"2507_CR18","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1016\/j.lungcan.2021.02.028","volume":"155","author":"P Moreno-Ruiz","year":"2021","unstructured":"Moreno-Ruiz P, Corvigno S, te Grootenhuis NC et al (2021) Stromal FAP is an independent poor prognosis marker in non-small cell lung adenocarcinoma and associated with p53 mutation. Lung Cancer 155:10\u201319","journal-title":"Lung Cancer"},{"key":"2507_CR19","doi-asserted-by":"publisher","first-page":"1523","DOI":"10.1007\/s00432-013-1471-8","volume":"139","author":"Y Liao","year":"2013","unstructured":"Liao Y, Ni Y, He R et al (2013) Clinical implications of fibroblast activation protein-\u03b1 in non-small cell lung cancer after curative resection: a new predictor for prognosis. J Cancer Res Clin Oncol 139:1523\u20131528","journal-title":"J Cancer Res Clin Oncol"},{"key":"2507_CR20","doi-asserted-by":"publisher","first-page":"16779","DOI":"10.1038\/s41598-021-96344-1","volume":"11","author":"KW Min","year":"2021","unstructured":"Min KW, Kim DH, Noh YK et al (2021) Cancer-associated fibroblasts are associated with poor prognosis in solid type of lung adenocarcinoma in a machine learning analysis. Sci Rep 11:16779","journal-title":"Sci Rep"},{"key":"2507_CR21","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1093\/jnci\/djac178","volume":"115","author":"T Pellinen","year":"2023","unstructured":"Pellinen T, Paavolainen L, Mart\u00edn-Bernab\u00e9 A et al (2023) Fibroblast subsets in non-small cell lung cancer: associations with survival, mutations, and immune features. J Natl Cancer Inst 115:71\u201382","journal-title":"J Natl Cancer Inst"},{"key":"2507_CR22","doi-asserted-by":"publisher","first-page":"1906","DOI":"10.1007\/s00259-023-06144-0","volume":"50","author":"BM Priv\u00e9","year":"2023","unstructured":"Priv\u00e9 BM, Boussihmad MA, Timmermans B et al (2023) Fibroblast activation protein-targeted radionuclide therapy: background, opportunities, and challenges of first (pre)clinical studies. Eur J Nucl Med Mol Imaging 50:1906\u20131918","journal-title":"Eur J Nucl Med Mol Imaging"},{"key":"2507_CR23","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1186\/s13550-021-00761-2","volume":"11","author":"P Windisch","year":"2021","unstructured":"Windisch P, Zwahlen DR, Giesel FL et al (2021) Clinical results of fibroblast activation protein (FAP) specific PET for non-malignant indications: systematic review. EJNMMI Res 11:18","journal-title":"EJNMMI Res"},{"key":"2507_CR24","doi-asserted-by":"publisher","first-page":"201","DOI":"10.2967\/jnumed.120.245084","volume":"62","author":"FL Giesel","year":"2021","unstructured":"Giesel FL, Adeberg S, Syed M et al (2021) FAPI-74 PET\/CT using either 18F-AlF or cold-kit 68Ga labeling: biodistribution, radiation dosimetry, and tumor delineation in lung cancer patients. J Nucl Med 62:201\u2013207","journal-title":"J Nucl Med"},{"key":"2507_CR25","doi-asserted-by":"publisher","first-page":"2800","DOI":"10.1158\/0008-5472.CAN-14-3041","volume":"75","author":"A Lo","year":"2015","unstructured":"Lo A, Wang LS, Scholler J et al (2015) Tumor-promoting desmoplasia is disrupted by depleting FAP-expressing stromal cells. Cancer Res 75:2800\u20132810","journal-title":"Cancer Res"},{"key":"2507_CR26","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1158\/2326-6066.CIR-13-0027","volume":"2","author":"LCS Wang","year":"2014","unstructured":"Wang LCS, Lo A, Scholler J et al (2014) Targeting fibroblast activation protein in tumor stroma with chimeric antigen receptor T cells can inhibit tumor growth and augment host immunity without severe toxicity. Cancer Immunol Res 2:154\u2013166","journal-title":"Cancer Immunol Res"},{"key":"2507_CR27","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1038\/s41586-019-1546-z","volume":"573","author":"H Aghajanian","year":"2019","unstructured":"Aghajanian H, Kimura T, Rurik JG et al (2019) Targeting cardiac fibrosis with engineered T cells. Nature 573:430\u2013433","journal-title":"Nature"},{"key":"2507_CR28","doi-asserted-by":"publisher","first-page":"815","DOI":"10.1038\/s42003-021-02275-y","volume":"4","author":"S Kostrikov","year":"2021","unstructured":"Kostrikov S, Johnsen KB, Braunstein TH et al (2021) Optical tissue clearing and machine learning can precisely characterize extravasation and blood vessel architecture in brain tumors. Commun Biol 4:815","journal-title":"Commun Biol"},{"key":"2507_CR29","doi-asserted-by":"publisher","first-page":"452","DOI":"10.1038\/bmt.2012.244","volume":"48","author":"Y Kanda","year":"2013","unstructured":"Kanda Y (2013) Investigation of the freely available easy-to-use software \u201cEZR\u201d for medical statistics. Bone Marrow Transplant 48:452\u2013458","journal-title":"Bone Marrow Transplant"},{"key":"2507_CR30","doi-asserted-by":"publisher","first-page":"895","DOI":"10.1002\/ijc.32193","volume":"146","author":"M Nurmik","year":"2020","unstructured":"Nurmik M, Ullmann P, Rodriguez F et al (2020) In search of definitions: cancer-associated fibroblasts and their markers. Int J Cancer 146:895\u2013905","journal-title":"Int J Cancer"},{"key":"2507_CR31","doi-asserted-by":"publisher","first-page":"6119","DOI":"10.1158\/0008-5472.CAN-17-1605","volume":"77","author":"S Sivakumar","year":"2017","unstructured":"Sivakumar S, San Lucas FA, McDowell TL et al (2017) Genomic landscape of atypical adenomatous hyperplasia reveals divergent modes to lung adenocarcinoma. Cancer Res 77:6119\u20136130","journal-title":"Cancer Res"},{"key":"2507_CR32","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1016\/j.humpath.2005.11.020","volume":"37","author":"PS Acharya","year":"2006","unstructured":"Acharya PS, Zukas A, Chandan V et al (2006) Fibroblast activation protein: a serine protease expressed at the remodeling interface in idiopathic pulmonary fibrosis. Hum Pathol 37:352\u2013360","journal-title":"Hum Pathol"},{"key":"2507_CR33","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1016\/j.lungcan.2020.04.023","volume":"145","author":"M Yotsukura","year":"2020","unstructured":"Yotsukura M, Asamura H, Suzuki S et al (2020) Prognostic impact of cancer-associated active fibroblasts and invasive architectural patterns on early-stage lung adenocarcinoma. Lung Cancer 145:158\u2013166","journal-title":"Lung Cancer"},{"key":"2507_CR34","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1038\/s43018-022-00411-z","volume":"3","author":"D Lavie","year":"2022","unstructured":"Lavie D, Ben-Shmuel A, Erez N et al (2022) Cancer-associated fibroblasts in the single-cell era. Nat Cancer 3:793\u2013807","journal-title":"Nat Cancer"},{"key":"2507_CR35","doi-asserted-by":"publisher","first-page":"8070","DOI":"10.1074\/jbc.M115.701433","volume":"291","author":"MH Fan","year":"2016","unstructured":"Fan MH, Zhu Q, Li HH et al (2016) Fibroblast activation protein (FAP) accelerates collagen degradation and clearance from lungs in mice. J Biol Chem 291:8070\u20138089","journal-title":"J Biol Chem"},{"key":"2507_CR36","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1074\/mcp.RA118.001046","volume":"18","author":"HE Zhang","year":"2019","unstructured":"Zhang HE, Hamson EJ, Koczorowska MM et al (2019) Identification of novel natural substrates of fibroblast activation protein-alpha by differential degradomics and proteomics. Mol Cell Proteomics 18:65\u201385","journal-title":"Mol Cell Proteomics"}],"container-title":["International Journal of Clinical Oncology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10147-024-02507-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s10147-024-02507-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10147-024-02507-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,27]],"date-time":"2024-05-27T04:24:02Z","timestamp":1716783842000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s10147-024-02507-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,11]]},"references-count":36,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2024,6]]}},"alternative-id":["2507"],"URL":"https:\/\/doi.org\/10.1007\/s10147-024-02507-1","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-3063817\/v1","asserted-by":"object"},{"id-type":"doi","id":"10.21203\/rs.3.rs-3595444\/v1","asserted-by":"object"}]},"ISSN":["1341-9625","1437-7772"],"issn-type":[{"value":"1341-9625","type":"print"},{"value":"1437-7772","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,11]]},"assertion":[{"value":"8 November 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 March 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 April 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors have declared that no competing interest exists.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"This study was performed in line with the principles of the Declaration of Helsinki. The study was approved by the Institutional Review Board of the Osaka International Cancer Institute (June 12, 2019. Approval No. 19050). Written informed consent was obtained from all patients.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}}]}}