{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T23:51:59Z","timestamp":1791244319635,"version":"4.1.0"},"reference-count":61,"publisher":"Radiation Research Society","issue":"4","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Radiation Research"],"published-print":{"date-parts":[[2025,8,1]]},"abstract":"<jats:p>Radiation-induced lung injury (RILI) includes early acute phase radiation pneumonitis (RP), and late chronic phase radiation-induced pulmonary fibrosis (RIPF). There is increasing evidence that ionizing radiation-induced cellular senescence is associated with pulmonary fibrosis. We have recently reported that biomarkers of senescence and, specifically, tyrosine kinase Fgr are induced in mouse RIPF, human idiopathic pulmonary fibrosis (IPF), and in human RIPF. We also reported that treatment with an Fgr inhibitor significantly reduced fibrosis of irradiated mouse lungs. Here, we investigated the association of senescence and tyrosine kinase Fgr in non-human primate (NHP) lung fibrosis and determined whether lung fibrosis can be predicted by analyzing the bronchoalveolar lavage (BAL) cells and fluid at early time points after irradiation. We found that markers of senescence (p16, p21) and expression of Fgr are induced in the lungs of NHP with RILI. That fibrosis can be predicted by analyzing BAL cells prior to the appearance of pulmonary fibrosis. We also induced senescence and expression of Fgr in irradiated normal human primary airway epithelial cells in vitro. In a transwell culture system, we established that senescent human airway epithelial cells induced fibrosis biomarkers collagen1, collagen 3, and alpha-smooth-muscle actin in target human primary lung fibroblasts. Whole-thorax lung irradiated (WTLI) NHPs in this study developed moderate to severe pneumonitis and marked variations in the magnitude of RIPF as measured by trichrome staining. In BAL fluid that was collected from WTLI NHP senescence-associated secretory proteins (SASP) were significantly induced, compared to the BAL fluid collected from control non-irradiated NHPs. Moreover, the levels of Fgr and biomarkers of senescence were significantly higher in NHPs with severely injured lungs compared to those with mildly or moderately injured lungs as indicated by fibrosis. Proinflammatory SASP cytokines increased to levels that correlated with the severity of RILI. The results show that senescent cells with induction of Fgr, and SASP cytokines are detectable in NHPs prior to RIPF and suggest that analysis of these proteins can predict the severity of RIPF prior to fully formed fibrosis.<\/jats:p>","DOI":"10.1667\/rade-23-00224.1","type":"journal-article","created":{"date-parts":[[2025,8,1]],"date-time":"2025-08-01T03:52:46Z","timestamp":1754020366000},"page":"354-368","source":"Crossref","is-referenced-by-count":4,"title":["Radiation-induced Lung Injury (RILI) in Non-human Primates (NHPs) Induces Cellular Senescence and Upregulation of Tyrosine Kinase Fgr, which is Detectable in Bronchoalveolar Lavage"],"prefix":"10.1667","volume":"204","author":[{"given":"George W.","family":"Schaaf","sequence":"first","affiliation":[{"name":"Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John D.","family":"Olson","sequence":"additional","affiliation":[{"name":"Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Baher A.","family":"Elgohari","sequence":"additional","affiliation":[{"name":"Department of Radiation Oncology, UPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, Pennsylvania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael W.","family":"Epperly","sequence":"additional","affiliation":[{"name":"Department of Radiation Oncology, UPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, Pennsylvania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen","family":"Hou","sequence":"additional","affiliation":[{"name":"Department of Radiation Oncology, UPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, Pennsylvania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hong","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Biostatistics, University of Pittsburgh, Pittsburgh, Pennsylvania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J. Mark","family":"Cline","sequence":"additional","affiliation":[{"name":"Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joel S.","family":"Greenberger","sequence":"additional","affiliation":[{"name":"Department of Radiation Oncology, UPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, Pennsylvania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amitava","family":"Mukherjee","sequence":"additional","affiliation":[{"name":"Department of Radiation Oncology, UPMC Hillman Cancer Center, University of Pittsburgh, Pittsburgh, Pennsylvania"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1243","reference":[{"key":"2","doi-asserted-by":"crossref","unstructured":"Y Yan, J Fu, RO Kowalchuk, et al.  \"Transl Lung Cancer Res.\"  11, \"Exploration of radiation-induced lung injury, from mechanism to treatment: a narrative review.\" 307 (2022)","DOI":"10.21037\/tlcr-22-108"},{"key":"4","doi-asserted-by":"crossref","unstructured":"Y Ohe, S Yamamoto, K Suzuki, et al.  \"Eur J Cancer.\"  37, \"Risk factors of treatment-related death in chemotherapy and thoracic radiotherapy for lung cancer\" 54 (2001)","DOI":"10.1016\/S0959-8049(00)00350-6"},{"key":"5","doi-asserted-by":"crossref","unstructured":"R Mazeron, B Etienne-Mastroianni, D P\u00e9rol, et al.  \"Int J Radiat Oncol Biol Phys.\"  77, \"Predictive factors of late radiation fibrosis: a prospective study in non-small cell lung cancer.\" 38 (2010)","DOI":"10.1016\/j.ijrobp.2009.04.019"},{"key":"6","doi-asserted-by":"crossref","unstructured":"G Raghu  and M Selman  \"Am J Respir Crit Care Med.\"  191, \"Nintedanib and pirfenidone. 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MnTnHex-2-PyP(5+), mitigates radiation injury in the lungs of non-human primates after whole-thorax exposure to ionizing radiation.\" (2018)","DOI":"10.3390\/antiox7030040"},{"key":"33","doi-asserted-by":"crossref","unstructured":"C Hansel, V Jendrossek, D Klein,  \"Int J Mol Sci.\"  21, \"Cellular senescence in the lung: The central role of senescent epithelial cells.\" 3279 (2020)","DOI":"10.3390\/ijms21093279"},{"key":"34","doi-asserted-by":"crossref","unstructured":"L Su, Y Dong, Y Wang, et al.  \"Cell Death Dis.\"  12, \"Potential role of senescent macrophages in radiation-induced pulmonary fibrosis.\" 527 (2021)","DOI":"10.1038\/s41419-021-03811-8"},{"key":"35","doi-asserted-by":"crossref","unstructured":"A Ejaz, MW Epperly, W Hou, et al.  \"Stem Cells.\"  37, \"Adipose-derived stem cell therapy ameliorates ionizing irradiation fibrosis via hepatocyte growth factor-mediated transforming growth factor-beta downregulation and recruitment of bone marrow cells.\" 791 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in the pathogenesis of pulmonary fibrosis.\" 52 (2021)","DOI":"10.1038\/s41420-021-00437-9"},{"key":"56","doi-asserted-by":"crossref","unstructured":"R Ac\u00edn-P\u00e9rez, S Iborra, Y Mart\u00ed-Mateos, et al.  \"Nat Metab.\"  2, \"Fgr kinase is required for proinflammatory macrophage activation during diet-induced obesity.\" 974 (2020)","DOI":"10.1038\/s42255-020-00273-8"},{"key":"57","doi-asserted-by":"crossref","unstructured":"P Mazzi, E Caveggion, JA Lapinet-Vera, et al.  \"J Immunol.\"  195, \"The Src-family kinases Hck and Fgr regulate early Lipopolysaccharide-induced myeloid cell recruitment into the lung and their ability to secrete chemokines.\" 2383 (2015)","DOI":"10.4049\/jimmunol.1402011"},{"key":"58","doi-asserted-by":"crossref","unstructured":"H Zhang, Y Yang, Y Cao, et al.  \"Respir Res.\"  25, \"IPF-related new macrophage subpopulations and diagnostic biomarker identification - combine machine learning with single-cell analysis.\" 241 (2024)","DOI":"10.1186\/s12931-024-02845-8"},{"key":"61","doi-asserted-by":"crossref","unstructured":"L Lipskaia, P Maisonnasse, C Fouillade, et al.  \"Am J Respir Cell Mol Biol.\"  66, \"Evidence that SARS-CoV-2 induces lung cell senescence: Potential impact on COVID-19 lung disease.\" 107 (2022)","DOI":"10.1165\/rcmb.2021-0205LE"},{"key":"55","doi-asserted-by":"crossref","unstructured":"AL DiCarlo, IL Jackson, JR Shah, et al.  \"Radiat Res.\"  177, \"Development and licensure of medical countermeasures to treat lung damage resulting from a radiological or nuclear incident.\" 717 (2012)","DOI":"10.1667\/RR2881.1"},{"key":"3","doi-asserted-by":"crossref","unstructured":"LB Marks, M Fan, R Clough, et al.  \"Int J Radiat Biol.\"  76, \"Radiation-induced pulmonary injury: Symptomatic versus subclinical endpoints.\" 469 (2000)","DOI":"10.1080\/095530000138466"},{"key":"24","doi-asserted-by":"crossref","unstructured":"J Van Dyk, TJ Keane, S Kan, et al.  \"Int J Radiat Oncol Biol Phys.\"  7, 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Ly-6C(high) monocytes in CCR2-dependent lung fibrosis following gene-targeted alveolar injury.\" 3447 (2013)","DOI":"10.4049\/jimmunol.1200604"},{"key":"60","doi-asserted-by":"crossref","unstructured":"DE Citrin, U Shankavaram, JA Horton, et al.  \"J Natl Cancer Inst.\"  105, \"Role of type II pneumocyte senescence in radiation-induced lung fibrosis.\" 1474 (2013)","DOI":"10.1093\/jnci\/djt212"},{"key":"51","doi-asserted-by":"crossref","unstructured":"J-P Coppe, P-Y Desprez, A Krtolica, et al.  \"Annu Rev Pathol.\"  5, \"The senescence-associated secretory phenotype: The dark side of tumor suppression.\" 99 (2010)","DOI":"10.1146\/annurev-pathol-121808-102144"},{"key":"36","doi-asserted-by":"crossref","unstructured":"KJ Livak  and TD Schmittgen  \"Methods.\"  25, \"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.\" 402 (2001)","DOI":"10.1006\/meth.2001.1262"},{"key":"25","doi-asserted-by":"crossref","unstructured":"M Garofalo, A Bennett, AM Farese, et al.  \"Health Phys.\"  106, \"The delayed pulmonary syndrome following acute high-dose irradiation: a rhesus macaque model.\" 56 (2014)","DOI":"10.1097\/HP.0b013e3182a32b3f"},{"key":"37","doi-asserted-by":"crossref","unstructured":"T Ashcroft, JM Simpson, V Timbrell,  \"J Clin Pathol.\"  41, \"Simple method of estimating severity of pulmonary fibrosis on a numerical scale.\" 467 (1988)","DOI":"10.1136\/jcp.41.4.467"},{"key":"29","doi-asserted-by":"publisher","unstructured":"TJ Macvittie, AM Farese, GA Parker, et al.  \"Health Phys.\"  119, \"Acute radiation-induced lung injury in the non-human primate: A review and comparison of mortality and co-morbidities using models of partial-body irradiation with marginal bone marrow sparing and whole thorax lung irradiation.\" 559 (2020)","DOI":"10.1097\/HP.0000000000001346"},{"key":"30","doi-asserted-by":"crossref","unstructured":"P Thakur, R DeBo, GO Dugan, et al.  \"Int J Radiat Oncol Biol Phys.\"  111, \"Clinicopathologic and Transcriptomic Analysis of Radiation-Induced Lung Injury in Nonhuman Primates.\" 249 (2021)","DOI":"10.1016\/j.ijrobp.2021.03.058"},{"key":"9","doi-asserted-by":"crossref","unstructured":"TA Beach, CJ Johnston, AM Groves, et al.  \"Exp Lung Res.\"  43, \"Radiation induced pulmonary fibrosis as a model of progressive fibrosis: Contributions of DNA damage, inflammatory response and cellular senescence genes.\" 134 (2017)","DOI":"10.1080\/01902148.2017.1318975"},{"key":"22","doi-asserted-by":"crossref","unstructured":"NN Vellichirammal, S Sethi, S Pandey, et al.  \"Mol Ther Nucleic Acids.\"  29, \"Lung transcriptome of nonhuman primates exposed to total- and partial-body irradiation.\" 584 (2022)","DOI":"10.1016\/j.omtn.2022.08.006"},{"key":"23","doi-asserted-by":"crossref","unstructured":"PGS Prasanna, M Aryankalayil, DE Citrin, et al.  \"Int J Radiat Biol.\"  99, \"Radiation-induced pulmonary fibrosis: roles of therapy-induced senescence and microRNAs.\" 1027 (2023)","DOI":"10.1080\/09553002.2023.2177768"},{"key":"32","doi-asserted-by":"crossref","unstructured":"Y Chen, P Rubin, J Williams, et al.  \"Int J Radiat Oncol Biol Phys.\"  49, \"Circulating IL-6 as a predictor of radiation pneumonitis.\" 641 (2001)","DOI":"10.1016\/S0360-3016(00)01445-0"}],"container-title":["Radiation Research"],"original-title":[],"link":[{"URL":"https:\/\/meridian.allenpress.com\/radiation-research\/article-pdf\/doi\/10.1667\/RADE-23-00224.1\/3533144\/10.1667_rade-23-00224.1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/meridian.allenpress.com\/radiation-research\/article-pdf\/doi\/10.1667\/RADE-23-00224.1\/3533144\/10.1667_rade-23-00224.1.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T22:57:26Z","timestamp":1791241046000},"score":1,"resource":{"primary":{"URL":"https:\/\/bioone.org\/journals\/radiation-research\/volume-204\/issue-4\/RADE-23-00224.1\/Radiation-induced-Lung-Injury-RILI-in-Non-human-Primates-NHPs\/10.1667\/RADE-23-00224.1.full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,8,1]]},"references-count":61,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2025,10,1]]}},"URL":"https:\/\/doi.org\/10.1667\/rade-23-00224.1","relation":{},"ISSN":["0033-7587","1938-5404"],"issn-type":[{"value":"0033-7587","type":"print"},{"value":"1938-5404","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,8,1]]}}}