{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T18:52:50Z","timestamp":1781635970641,"version":"3.54.5"},"reference-count":26,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,2,10]],"date-time":"2026-02-10T00:00:00Z","timestamp":1770681600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,3,16]],"date-time":"2026-03-16T00:00:00Z","timestamp":1773619200000},"content-version":"vor","delay-in-days":34,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Grant-in-Aid for Young Researchers from Saitama Medical University International Medical Center","award":["4-D-1-04"],"award-info":[{"award-number":["4-D-1-04"]}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["25K11939"],"award-info":[{"award-number":["25K11939"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Gastroenterol"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Cisplatin plus 5-fluorouracil (CF) remains a cornerstone of treatment for locally-advanced esophageal cancer (EC). However, resistance to CF-based neoadjuvant chemotherapy (NAC) remains a major clinical challenge. Clarifying whether resistance-associated molecular features are induced by treatment or already present before therapy is crucial for improving patient stratification.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      RNA sequencing was performed on paired tumor specimens from patients with EC treated with CF-based NAC, including pre-treatment biopsies (PreNAC) and post-treatment surgical samples (PostNAC) (\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u200915; recurrence,\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u20097; non-recurrence,\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u20098). Differential gene expression analysis was conducted across four groups defined by sample timing (Pre vs. PostNAC) and recurrence status.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>PostNAC transcriptional changes in recurrent tumors were relatively limited, with only 53 genes upregulated and 54 genes downregulated compared with PreNAC samples. Notably, genes involved in glutathione metabolism emerged as the dominant resistance-associated pathway and were consistently enriched in recurrent tumors at both PreNAC and PostNAC stages. Key glutathione-related genes, including GSTP1 and GPX2, were highly expressed in recurrent cases, indicating that major resistance-associated molecular features are often already established prior to chemotherapy rather than being newly acquired during NAC.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Our findings suggest that the molecular characteristics associated with CF resistance are frequently present before the initiation of chemotherapy. These results highlight the clinical potential of pretreatment molecular profiling as a strategy to guide therapeutic decision-making and optimize CF-based NAC in EC.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12876-026-04664-1","type":"journal-article","created":{"date-parts":[[2026,2,10]],"date-time":"2026-02-10T08:48:30Z","timestamp":1770713310000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Glutathione metabolism\u2013associated resistance to cisplatin and 5-FU in esophageal cancer: a paired transcriptomic study"],"prefix":"10.1186","volume":"26","author":[{"given":"Masataka","family":"Hirasaki","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yutaka","family":"Miyawaki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasuo","family":"Kamakura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomonori","family":"Kawasaki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoshi","family":"Yamasaki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hisayo","family":"Fukushima","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshinori","family":"Makino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hiroshi","family":"Sato","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tetsuya","family":"Hamaguchi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,2,10]]},"reference":[{"key":"4664_CR1","first-page":"209","volume":"71","author":"H Sung","year":"2021","unstructured":"Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209\u201349.","journal-title":"CA Cancer J Clin"},{"key":"4664_CR2","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s10388-018-0641-9","volume":"16","author":"Y Kitagawa","year":"2019","unstructured":"Kitagawa Y, Uno T, Oyama T, Kato K, Kato H, Kawakubo H, et al. Esophageal cancer practice guidelines 2017 edited by the Japan esophageal society: part 1. Esophagus. 2019;16:1\u201324.","journal-title":"Esophagus"},{"key":"4664_CR3","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1200\/JCO.2022.40.4_suppl.238","volume":"40","author":"K Kato","year":"2022","unstructured":"Kato K, Ito Y, Daiko H, Ozawa S, Ogata T, Hara H, et al. A randomized controlled phase III trial comparing two chemotherapy regimen and chemoradiotherapy regimen as neoadjuvant treatment for locally advanced esophageal cancer, JCOG1109 next study. JCO. 2022;40:238.","journal-title":"JCO"},{"key":"4664_CR4","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1007\/s10388-023-00993-2","volume":"20","author":"Y Kitagawa","year":"2023","unstructured":"Kitagawa Y, Ishihara R, Ishikawa H, Ito Y, Oyama T, Oyama T, et al. Esophageal cancer practice guidelines 2022 edited by the Japan esophageal society: part 1. Esophagus. 2023;20:343\u201372.","journal-title":"Esophagus"},{"key":"4664_CR5","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1056\/NEJMoa2111380","volume":"386","author":"Y Doki","year":"2022","unstructured":"Doki Y, Ajani JA, Kato K, Xu J, Wyrwicz L, Motoyama S, et al. Nivolumab combination therapy in advanced esophageal squamous-cell carcinoma. N Engl J Med. 2022;386:449\u201362.","journal-title":"N Engl J Med"},{"key":"4664_CR6","doi-asserted-by":"publisher","first-page":"759","DOI":"10.1016\/S0140-6736(21)01234-4","volume":"398","author":"J-M Sun","year":"2021","unstructured":"Sun J-M, Shen L, Shah MA, Enzinger P, Adenis A, Doi T, et al. Pembrolizumab plus chemotherapy versus chemotherapy alone for first-line treatment of advanced oesophageal cancer (KEYNOTE-590): a randomised, placebo-controlled, phase 3 study. Lancet. 2021;398:759\u201371.","journal-title":"Lancet"},{"key":"4664_CR7","doi-asserted-by":"publisher","first-page":"393","DOI":"10.6004\/jnccn.2023.0019","volume":"21","author":"JA Ajani","year":"2023","unstructured":"Ajani JA, D\u2019Amico TA, Bentrem DJ, Cooke D, Corvera C, Das P, et al. Esophageal and esophagogastric junction cancers, version 2. 2023, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2023;21:393\u2013422.","journal-title":"J Natl Compr Canc Netw"},{"key":"4664_CR8","doi-asserted-by":"publisher","first-page":"1349","DOI":"10.3390\/cells8111349","volume":"8","author":"SN Devenport","year":"2019","unstructured":"Devenport SN, Shah YM. Functions and implications of autophagy in colon cancer. Cells. 2019;8:1349.","journal-title":"Cells"},{"key":"4664_CR9","doi-asserted-by":"publisher","first-page":"413","DOI":"10.3389\/fcell.2020.00413","volume":"8","author":"Y Wang","year":"2020","unstructured":"Wang Y, Liu HH, Cao YT, Zhang LL, Huang F, Yi C. The role of mitochondrial dynamics and mitophagy in carcinogenesis, metastasis and therapy. Front Cell Dev Biol. 2020;8:413.","journal-title":"Front Cell Dev Biol"},{"key":"4664_CR10","doi-asserted-by":"publisher","first-page":"4025","DOI":"10.1245\/s10434-017-6096-8","volume":"24","author":"K Yamashita","year":"2017","unstructured":"Yamashita K, Miyata H, Makino T, Masuike Y, Furukawa H, Tanaka K, et al. High expression of the mitophagy-related protein Pink1 is associated with a poor response to chemotherapy and a poor prognosis for patients treated with neoadjuvant chemotherapy for esophageal squamous cell carcinoma. Ann Surg Oncol. 2017;24:4025\u201332.","journal-title":"Ann Surg Oncol"},{"key":"4664_CR11","doi-asserted-by":"publisher","first-page":"491","DOI":"10.1007\/s13577-023-01020-3","volume":"37","author":"T Fuchino","year":"2024","unstructured":"Fuchino T, Kurogi S, Tsukamoto Y, Shibata T, Fumoto S, Fujishima H, et al. Characterization of residual cancer by comparison of a pair of organoids established from a patient with esophageal squamous cell carcinoma before and after neoadjuvant chemotherapy. Hum Cell. 2024;37:491\u2013501.","journal-title":"Hum Cell"},{"key":"4664_CR12","doi-asserted-by":"publisher","first-page":"25669","DOI":"10.1038\/s41598-025-11252-y","volume":"15","author":"Y Miyawaki","year":"2025","unstructured":"Miyawaki Y, Hirasaki M, Kamakura Y, Kawasaki T, Baba Y, Sato T, et al. Developing a machine-learning model to enable treatment selection for neoadjuvant chemotherapy for esophageal cancer. Sci Rep. 2025;15:25669.","journal-title":"Sci Rep"},{"key":"4664_CR13","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1111\/pin.13350","volume":"73","author":"Y Ichinose","year":"2023","unstructured":"Ichinose Y, Hasebe T, Hirasaki M, Sakakibara A, Yokogawa H, Nukui A, et al. Vimentin-positive invasive breast carcinoma of no special type: a breast carcinoma with lethal biological characteristics. Pathol Int. 2023;73:413\u201333.","journal-title":"Pathol Int"},{"key":"4664_CR14","doi-asserted-by":"publisher","first-page":"104810","DOI":"10.1016\/j.jbc.2023.104810","volume":"299","author":"K Etoh","year":"2023","unstructured":"Etoh K, Nakao M. A web-based integrative transcriptome analysis, RNAseqChef, uncovers the cell\/tissue type-dependent action of Sulforaphane. J Biol Chem. 2023;299:104810.","journal-title":"J Biol Chem"},{"key":"4664_CR15","doi-asserted-by":"publisher","first-page":"e164","DOI":"10.1093\/nar\/gkq603","volume":"38","author":"K Wang","year":"2010","unstructured":"Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38:e164.","journal-title":"Nucleic Acids Res"},{"key":"4664_CR16","doi-asserted-by":"publisher","first-page":"1297","DOI":"10.1101\/gr.107524.110","volume":"20","author":"A McKenna","year":"2010","unstructured":"McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297\u2013303.","journal-title":"Genome Res"},{"key":"4664_CR17","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/S0753-3322(03)00043-X","volume":"57","author":"DM Townsend","year":"2003","unstructured":"Townsend DM, Tew KD, Tapiero H. The importance of glutathione in human disease. Biomed Pharmacother. 2003;57:145\u201355.","journal-title":"Biomed Pharmacother"},{"key":"4664_CR18","doi-asserted-by":"publisher","first-page":"e81162","DOI":"10.1371\/journal.pone.0081162","volume":"8","author":"R Marullo","year":"2013","unstructured":"Marullo R, Werner E, Degtyareva N, Moore B, Altavilla G, Ramalingam SS, et al. Cisplatin induces a mitochondrial-ROS response that contributes to cytotoxicity depending on mitochondrial redox status and bioenergetic functions. PLoS ONE. 2013;8:e81162.","journal-title":"PLoS ONE"},{"key":"4664_CR19","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1007\/s11010-017-3147-1","volume":"439","author":"HA Deveci","year":"2018","unstructured":"Deveci HA, Naz\u0131ro\u011flu M, Nur G. 5-fluorouracil-induced mitochondrial oxidative cytotoxicity and apoptosis are increased in MCF-7 human breast cancer cells by TRPV1 channel activation but not hypericum perforatum treatment. Mol Cell Biochem. 2018;439:189\u201398.","journal-title":"Mol Cell Biochem"},{"key":"4664_CR20","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1186\/s13046-016-0349-4","volume":"35","author":"Z Hu","year":"2016","unstructured":"Hu Z, Lv G, Li Y, Li E, Li H, Zhou Q, et al. Enhancement of anti-tumor effects of 5-fluorouracil on hepatocellular carcinoma by low-intensity ultrasound. J Exp Clin Cancer Res. 2016;35:71.","journal-title":"J Exp Clin Cancer Res"},{"key":"4664_CR21","doi-asserted-by":"publisher","first-page":"207","DOI":"10.3892\/or.2022.8422","volume":"48","author":"M Wang","year":"2022","unstructured":"Wang M, Chen X, Fu G, Ge M. Glutathione peroxidase 2 overexpression promotes malignant progression and cisplatin resistance of KRAS-mutated lung cancer cells. Oncol Rep. 2022;48:207.","journal-title":"Oncol Rep"},{"key":"4664_CR22","doi-asserted-by":"publisher","first-page":"7370157","DOI":"10.1155\/2020\/7370157","volume":"2020","author":"H Du","year":"2020","unstructured":"Du H, Chen B, Jiao NL, Liu YH, Sun SY, Zhang YW. Elevated glutathione peroxidase 2 expression promotes cisplatin resistance in lung adenocarcinoma. Oxid Med Cell Longev. 2020;2020:7370157.","journal-title":"Oxid Med Cell Longev"},{"key":"4664_CR23","doi-asserted-by":"publisher","first-page":"1639","DOI":"10.1038\/sj.onc.1209373","volume":"25","author":"CC Mcilwain","year":"2006","unstructured":"Mcilwain CC, Townsend DM, Tew KD. Glutathione S-transferase polymorphisms: cancer incidence and therapy. Oncogene. 2006;25:1639\u201348.","journal-title":"Oncogene"},{"key":"4664_CR24","doi-asserted-by":"publisher","first-page":"1687","DOI":"10.3892\/or.2013.2606","volume":"30","author":"Y Yamamoto","year":"2013","unstructured":"Yamamoto Y, Konishi H, Ichikawa D, Arita T, Shoda K, Komatsu S, et al. Significance of GSTP1 for predicting the prognosis and chemotherapeutic efficacy in esophageal squamous cell carcinoma. Oncol Rep. 2013;30:1687\u201394.","journal-title":"Oncol Rep"},{"key":"4664_CR25","doi-asserted-by":"publisher","first-page":"795","DOI":"10.1111\/cas.13896","volume":"110","author":"S Ogino","year":"2019","unstructured":"Ogino S, Konishi H, Ichikawa D, Matsubara D, Shoda K, Arita T, et al. Glutathione S-transferase Pi 1 is a valuable predictor for cancer drug resistance in esophageal squamous cell carcinoma. Cancer Sci. 2019;110:795\u2013804.","journal-title":"Cancer Sci"},{"key":"4664_CR26","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1158\/2159-8290.CD-15-0412","volume":"5","author":"N Murugaesu","year":"2015","unstructured":"Murugaesu N, Wilson GA, Birkbak NJ, Watkins T, McGranahan N, Kumar S, et al. Tracking the genomic evolution of esophageal adenocarcinoma through neoadjuvant chemotherapy. Cancer Discov. 2015;5:821\u201331.","journal-title":"Cancer Discov"}],"container-title":["BMC Gastroenterology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12876-026-04664-1","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12876-026-04664-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12876-026-04664-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T18:00:59Z","timestamp":1781632859000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1186\/s12876-026-04664-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,10]]},"references-count":26,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,12]]}},"alternative-id":["4664"],"URL":"https:\/\/doi.org\/10.1186\/s12876-026-04664-1","relation":{},"ISSN":["1471-230X"],"issn-type":[{"value":"1471-230X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,10]]},"assertion":[{"value":"4 November 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 January 2026","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 February 2026","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 entire study followed the ethical standards of the Declaration of Helsinki and its later amendments. It was approved by the Institutional Review Board of Saitama Medical University International Medical Center (2022-113 and 2024-055). The requirement for informed consent was waived by the Institutional Review Board of Saitama Medical University International Medical Center (2022-113 and 2024-055) in view of the retrospective nature of this study.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"169"}}