Identification of cancer-associated fibrolast subtypes and distinctive role of MFAP5 in CT-detected extramural venous invasion in gastric cancer

Extramural venous invasion (EMVI) detected by computed tomography has been identified as an independent risk factor for distant metastasis in patients with advanced gastric cancer (GC). Cancer-associated fibroblasts (CAFs) are critical for remodeling the tumor microenvironment in GCs. Here, we repor...

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Main Authors: Bo Gao, Xinyi Gou, Caizhen Feng, Yinli Zhang, Huining Gu, Fan Chai, Yi Wang, Yingjiang Ye, Nan Hong, Guohua Hu, Boshi Sun, Jin Cheng, Hao Yang
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Translational Oncology
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Online Access:http://www.sciencedirect.com/science/article/pii/S1936523324003140
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author Bo Gao
Xinyi Gou
Caizhen Feng
Yinli Zhang
Huining Gu
Fan Chai
Yi Wang
Yingjiang Ye
Nan Hong
Guohua Hu
Boshi Sun
Jin Cheng
Hao Yang
author_facet Bo Gao
Xinyi Gou
Caizhen Feng
Yinli Zhang
Huining Gu
Fan Chai
Yi Wang
Yingjiang Ye
Nan Hong
Guohua Hu
Boshi Sun
Jin Cheng
Hao Yang
author_sort Bo Gao
collection DOAJ
description Extramural venous invasion (EMVI) detected by computed tomography has been identified as an independent risk factor for distant metastasis in patients with advanced gastric cancer (GC). Cancer-associated fibroblasts (CAFs) are critical for remodeling the tumor microenvironment in GCs. Here, we report that MFAP5+ CAFs promote the formation of EMVI imaging in GC. We detected gene expression in pathological samples from 13 advanced GC patients with EMVI. Radiogenomics results showed the degree of CAFs infiltration was directly proportional to the EMVI score and EMT pathway in GC patients. Single-cell sequencing data analysis results showed that MFAP5+CAFs subtypes in GC were negatively correlated with patient prognosis and were enriched in tumor lactylation modification and EMT pathways. Immunohistochemistry results showed that the expression of MFAP5, L-lactyl and EMT markers in GC tissues was proportional to the EMVI score. CAF from gastric cancer tissue was extracted using collagenase method and co-cultured with GC cell line in vitro. After lentivirus knockdown of MFAP5 in CAFs, the levels of L-lactoyl and histone lactylation modifications were significantly reduced, and the sphere-forming and vascularization abilities of CAFs were significantly inhibited. Cell function experiments showed that MFAP5+ CAFs can affect the EMT, metastasis and invasion capabilities of GC cells. In vivo experimental results of the nude mouse in situ EMVI model suggest that MFAP5+ CAF may promote the formation of EMVI imaging features in GC by regulating lactylation modification. This innovative work may provide important new references for the diagnosis and treatment of GC.
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spelling doaj-art-e65d5f029bed46faa05e657a236575dc2024-12-09T04:27:07ZengElsevierTranslational Oncology1936-52332025-01-0151102188Identification of cancer-associated fibrolast subtypes and distinctive role of MFAP5 in CT-detected extramural venous invasion in gastric cancerBo Gao0Xinyi Gou1Caizhen Feng2Yinli Zhang3Huining Gu4Fan Chai5Yi Wang6Yingjiang Ye7Nan Hong8Guohua Hu9Boshi Sun10Jin Cheng11Hao Yang12Department of Hernia and Abdominal Wall Surgery, Peking University People's Hospital, Peking University Health Science Center, Beijing, ChinaDepartment of Radiology, Peking University People's Hospital, Peking University Health Science Center, Beijing, ChinaDepartment of Radiology, Peking University People's Hospital, Peking University Health Science Center, Beijing, ChinaDepartment of Pathology, Peking University People's Hospital, Peking University Health Science Center, Beijing, ChinaDepartment of Immunology, School of Basic Medical Sciences, Peking University and NHC Key Laboratory of Medical Immunology, Peking University, Beijing, ChinaDepartment of Radiology, Peking University People's Hospital, Peking University Health Science Center, Beijing, ChinaDepartment of Radiology, Peking University People's Hospital, Peking University Health Science Center, Beijing, ChinaDepartment of Gastrointestinal Surgery, Peking University People's Hospital, Peking University Health Science Center, Beijing, ChinaDepartment of Radiology, Peking University People's Hospital, Peking University Health Science Center, Beijing, ChinaDepartment of Hernia and Abdominal Wall Surgery, Peking University People's Hospital, Peking University Health Science Center, Beijing, ChinaDepartment of General Surgery, The Second Affiliated Hospital of Harbin Medical University, Harbin, China; Corresponding authors.Department of Radiology, Peking University People's Hospital, Peking University Health Science Center, Beijing, China; Corresponding authors.Department of Oncology Surgery, Harbin Medical University Cancer Hospital, Harbin, China; Corresponding authors.Extramural venous invasion (EMVI) detected by computed tomography has been identified as an independent risk factor for distant metastasis in patients with advanced gastric cancer (GC). Cancer-associated fibroblasts (CAFs) are critical for remodeling the tumor microenvironment in GCs. Here, we report that MFAP5+ CAFs promote the formation of EMVI imaging in GC. We detected gene expression in pathological samples from 13 advanced GC patients with EMVI. Radiogenomics results showed the degree of CAFs infiltration was directly proportional to the EMVI score and EMT pathway in GC patients. Single-cell sequencing data analysis results showed that MFAP5+CAFs subtypes in GC were negatively correlated with patient prognosis and were enriched in tumor lactylation modification and EMT pathways. Immunohistochemistry results showed that the expression of MFAP5, L-lactyl and EMT markers in GC tissues was proportional to the EMVI score. CAF from gastric cancer tissue was extracted using collagenase method and co-cultured with GC cell line in vitro. After lentivirus knockdown of MFAP5 in CAFs, the levels of L-lactoyl and histone lactylation modifications were significantly reduced, and the sphere-forming and vascularization abilities of CAFs were significantly inhibited. Cell function experiments showed that MFAP5+ CAFs can affect the EMT, metastasis and invasion capabilities of GC cells. In vivo experimental results of the nude mouse in situ EMVI model suggest that MFAP5+ CAF may promote the formation of EMVI imaging features in GC by regulating lactylation modification. This innovative work may provide important new references for the diagnosis and treatment of GC.http://www.sciencedirect.com/science/article/pii/S1936523324003140Gastric cancerTumor microenviromentMFAP5+ cancer-associated fibroblastsLactylation modificationExtramural venous invasion
spellingShingle Bo Gao
Xinyi Gou
Caizhen Feng
Yinli Zhang
Huining Gu
Fan Chai
Yi Wang
Yingjiang Ye
Nan Hong
Guohua Hu
Boshi Sun
Jin Cheng
Hao Yang
Identification of cancer-associated fibrolast subtypes and distinctive role of MFAP5 in CT-detected extramural venous invasion in gastric cancer
Translational Oncology
Gastric cancer
Tumor microenviroment
MFAP5+ cancer-associated fibroblasts
Lactylation modification
Extramural venous invasion
title Identification of cancer-associated fibrolast subtypes and distinctive role of MFAP5 in CT-detected extramural venous invasion in gastric cancer
title_full Identification of cancer-associated fibrolast subtypes and distinctive role of MFAP5 in CT-detected extramural venous invasion in gastric cancer
title_fullStr Identification of cancer-associated fibrolast subtypes and distinctive role of MFAP5 in CT-detected extramural venous invasion in gastric cancer
title_full_unstemmed Identification of cancer-associated fibrolast subtypes and distinctive role of MFAP5 in CT-detected extramural venous invasion in gastric cancer
title_short Identification of cancer-associated fibrolast subtypes and distinctive role of MFAP5 in CT-detected extramural venous invasion in gastric cancer
title_sort identification of cancer associated fibrolast subtypes and distinctive role of mfap5 in ct detected extramural venous invasion in gastric cancer
topic Gastric cancer
Tumor microenviroment
MFAP5+ cancer-associated fibroblasts
Lactylation modification
Extramural venous invasion
url http://www.sciencedirect.com/science/article/pii/S1936523324003140
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