Influence of Citrobacter freundii on NINJ2 Expression and Oxaliplatin Resistance in Colorectal Cancer

ABSTRACT Background Oxaliplatin, a third‐generation platinum‐based chemotherapeutic agent, is widely used in the treatment of colorectal cancer (CRC). However, some patients do not respond effectively to oxaliplatin, and intrinsic resistance to the drug poses a significant challenge. Recent studies...

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Main Authors: Reio Ueta, Hiroo Imai, Ken Saijo, Yoshifumi Kawamura, Shuto Kodera, Chikashi Ishioka
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Cancer Medicine
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Online Access:https://doi.org/10.1002/cam4.70940
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author Reio Ueta
Hiroo Imai
Ken Saijo
Yoshifumi Kawamura
Shuto Kodera
Chikashi Ishioka
author_facet Reio Ueta
Hiroo Imai
Ken Saijo
Yoshifumi Kawamura
Shuto Kodera
Chikashi Ishioka
author_sort Reio Ueta
collection DOAJ
description ABSTRACT Background Oxaliplatin, a third‐generation platinum‐based chemotherapeutic agent, is widely used in the treatment of colorectal cancer (CRC). However, some patients do not respond effectively to oxaliplatin, and intrinsic resistance to the drug poses a significant challenge. Recent studies have revealed an association between the gut microbiome and the progression of CRC. We hypothesized that Citrobacter freundii, a component of the gut microbiome, contributes to oxaliplatin resistance by regulating specific gene expression in CRC cells. Methods A bacterial culture filtrate from Citrobacter freundii was employed in the experiments. The CRC cell line RKO, following exposure to this filtrate, was analyzed using high‐throughput RNA sequencing. Candidate genes were identified through MTT assays, siRNA knockdown, and overexpression experiments. Apoptosis and reactive oxygen species (ROS) assays were performed to investigate the underlying mechanisms. Finally, a xenograft mouse model was used to evaluate oxaliplatin resistance in vivo. Results Exposure to bacterial culture filtrate from Citrobacter freundii induced oxaliplatin resistance in RKO cells with downregulation of the NINJ2 gene as a possible molecular mechanism. ReducedNINJ2 gene expression suppressed oxaliplatin‐induced apoptosis and ROS generation. A tendency toward reduced oxaliplatin efficacy was observed in vivo when NINJ2 gene expression was suppressed. Conclusion This study demonstrates that Citrobacter freundii promotes oxaliplatin resistance in CRC through downregulation of NINJ2 gene. NINJ2 gene may serve as a predictive biomarker and therapeutic target to overcome oxaliplatin resistance in CRC.
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spelling doaj-art-c74b47a9459841e58d2f1f9780c81fc92025-08-20T03:58:18ZengWileyCancer Medicine2045-76342025-07-011413n/an/a10.1002/cam4.70940Influence of Citrobacter freundii on NINJ2 Expression and Oxaliplatin Resistance in Colorectal CancerReio Ueta0Hiroo Imai1Ken Saijo2Yoshifumi Kawamura3Shuto Kodera4Chikashi Ishioka5Department of Clinical Oncology Tohoku University Graduate School of Medicine Sendai JapanDepartment of Clinical Oncology Tohoku University Graduate School of Medicine Sendai JapanDepartment of Clinical Oncology Tohoku University Graduate School of Medicine Sendai JapanDepartment of Clinical Oncology Tohoku University Graduate School of Medicine Sendai JapanDepartment of Clinical Oncology Tohoku University Graduate School of Medicine Sendai JapanDepartment of Clinical Oncology Tohoku University Graduate School of Medicine Sendai JapanABSTRACT Background Oxaliplatin, a third‐generation platinum‐based chemotherapeutic agent, is widely used in the treatment of colorectal cancer (CRC). However, some patients do not respond effectively to oxaliplatin, and intrinsic resistance to the drug poses a significant challenge. Recent studies have revealed an association between the gut microbiome and the progression of CRC. We hypothesized that Citrobacter freundii, a component of the gut microbiome, contributes to oxaliplatin resistance by regulating specific gene expression in CRC cells. Methods A bacterial culture filtrate from Citrobacter freundii was employed in the experiments. The CRC cell line RKO, following exposure to this filtrate, was analyzed using high‐throughput RNA sequencing. Candidate genes were identified through MTT assays, siRNA knockdown, and overexpression experiments. Apoptosis and reactive oxygen species (ROS) assays were performed to investigate the underlying mechanisms. Finally, a xenograft mouse model was used to evaluate oxaliplatin resistance in vivo. Results Exposure to bacterial culture filtrate from Citrobacter freundii induced oxaliplatin resistance in RKO cells with downregulation of the NINJ2 gene as a possible molecular mechanism. ReducedNINJ2 gene expression suppressed oxaliplatin‐induced apoptosis and ROS generation. A tendency toward reduced oxaliplatin efficacy was observed in vivo when NINJ2 gene expression was suppressed. Conclusion This study demonstrates that Citrobacter freundii promotes oxaliplatin resistance in CRC through downregulation of NINJ2 gene. NINJ2 gene may serve as a predictive biomarker and therapeutic target to overcome oxaliplatin resistance in CRC.https://doi.org/10.1002/cam4.70940bacterial culture filtrateCitrobacter freundiicolon cancergut microbiomeoxaliplatin
spellingShingle Reio Ueta
Hiroo Imai
Ken Saijo
Yoshifumi Kawamura
Shuto Kodera
Chikashi Ishioka
Influence of Citrobacter freundii on NINJ2 Expression and Oxaliplatin Resistance in Colorectal Cancer
Cancer Medicine
bacterial culture filtrate
Citrobacter freundii
colon cancer
gut microbiome
oxaliplatin
title Influence of Citrobacter freundii on NINJ2 Expression and Oxaliplatin Resistance in Colorectal Cancer
title_full Influence of Citrobacter freundii on NINJ2 Expression and Oxaliplatin Resistance in Colorectal Cancer
title_fullStr Influence of Citrobacter freundii on NINJ2 Expression and Oxaliplatin Resistance in Colorectal Cancer
title_full_unstemmed Influence of Citrobacter freundii on NINJ2 Expression and Oxaliplatin Resistance in Colorectal Cancer
title_short Influence of Citrobacter freundii on NINJ2 Expression and Oxaliplatin Resistance in Colorectal Cancer
title_sort influence of citrobacter freundii on ninj2 expression and oxaliplatin resistance in colorectal cancer
topic bacterial culture filtrate
Citrobacter freundii
colon cancer
gut microbiome
oxaliplatin
url https://doi.org/10.1002/cam4.70940
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