Over-expressed Phospholamban in Cancer-associated Fibroblasts Is a Driver for CMS4 Subtype Colorectal Cancer FormationSummary

Background & Aims: Heterogeneity is the malignancy feature of colorectal cancer (CRC), which augments the difficulty of CRC treatment. Consensus molecular subtypes (CMSs) classified CRC into 4 subtypes. CMS4 is the most aggressive subtype, characterized with epithelial mesenchymal transition...

Full description

Saved in:
Bibliographic Details
Main Authors: Tao Li, Yuxiang Fei, Xu Sun, Jun Zhu, Xin Fang, Fanjun Meng, Danyi Wang, Xu Zhang, Chao Liu, Qianming Du
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Cellular and Molecular Gastroenterology and Hepatology
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352345X25000657
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850113503061344256
author Tao Li
Yuxiang Fei
Xu Sun
Jun Zhu
Xin Fang
Fanjun Meng
Danyi Wang
Xu Zhang
Chao Liu
Qianming Du
author_facet Tao Li
Yuxiang Fei
Xu Sun
Jun Zhu
Xin Fang
Fanjun Meng
Danyi Wang
Xu Zhang
Chao Liu
Qianming Du
author_sort Tao Li
collection DOAJ
description Background &amp; Aims: Heterogeneity is the malignancy feature of colorectal cancer (CRC), which augments the difficulty of CRC treatment. Consensus molecular subtypes (CMSs) classified CRC into 4 subtypes. CMS4 is the most aggressive subtype, characterized with epithelial mesenchymal transition (EMT) and angiogenesis activation. However, the mechanism of CMS4 formation still remains unclear. We aimed to investigate the role of phospholamban (PLN) on CMS4 formation. Methods: Immunohistochemistry and Western blotting were used to detected PLN expressions. Transwell and wound-healing assays were used to evaluate migration and invasion of HCT116 and HT29. Tube formation assay was used to evaluate angiogenesis of HUVECs. GST pull-down was used to detected the interaction between PLN and AXIN2. The CAF-CT26 spleen co-transplantation mouse model was built to evaluate PLN’s effects on CRC metastasis. Results: PLN knockdown reversed CAFs’ conditional medium (CM)-induced EMT, cell migration, and angiogenesis (P < .01). PLN strongly bound to AXIN2, the main component of β-catenin degradation complex, and PLN knockdown increased β-catenin ubiquitination in CAFs (P < .01). PLN knockdown blocked GREM1 secretion (P < .01), and PLN overexpression-induced EMT, cell migration, and angiogenesis were blocked by anti-GREM1 neutralizing antibody (P < .01). Knockdown of BMP2 and VEGFR2 reversed CAFs’ CM induced EMT and angiogenesis effects, respectively (P < .01). PLN knockdown attenuated CAFs mediated tumor promoting effects in vivo (P < .01). Conclusions: PLN competitively binds with AXIN2 to increase β-catenin activity in CAFs. β-catenin signal induces GREM1 secretion, driving EMT and angiogenesis via BMP2 and VEGFR2, respectively. These findings demonstrate that PLN is a driver for CMS4 formation.
format Article
id doaj-art-54d221cd3b694d13b377fd1bf6fcc8c8
institution OA Journals
issn 2352-345X
language English
publishDate 2025-01-01
publisher Elsevier
record_format Article
series Cellular and Molecular Gastroenterology and Hepatology
spelling doaj-art-54d221cd3b694d13b377fd1bf6fcc8c82025-08-20T02:37:09ZengElsevierCellular and Molecular Gastroenterology and Hepatology2352-345X2025-01-0119910152410.1016/j.jcmgh.2025.101524Over-expressed Phospholamban in Cancer-associated Fibroblasts Is a Driver for CMS4 Subtype Colorectal Cancer FormationSummaryTao Li0Yuxiang Fei1Xu Sun2Jun Zhu3Xin Fang4Fanjun Meng5Danyi Wang6Xu Zhang7Chao Liu8Qianming Du9General Clinical Research Center, Nanjing First Hospital, Nanjing Medical University, Nanjing, P.R. China; School of Basic Medicine and Clinical Pharmacy, China Pharmaceutical University, Nanjing, P.R. China; Nanjing First Hospital, Nanjing University of Chinese Medicine, Nanjing, P.R. ChinaSchool of Basic Medicine and Clinical Pharmacy, China Pharmaceutical University, Nanjing, P.R. China; Department of Pharmacy, Nanjing First Hospital, Nanjing Medical University, Nanjing, P.R. China; Nanjing First Hospital, Nanjing University of Chinese Medicine, Nanjing, P.R. ChinaDepartment of Pharmacy, Nanjing Luhe People’s Hospital, Nanjing, China; Department of Pharmacy, Nanjing Luhe People’s Hospital, Yangzhou University, Nanjing, P.R. ChinaDepartment of Pharmacy, Nanjing Luhe People’s Hospital, Nanjing, China; Department of Pharmacy, Nanjing Luhe People’s Hospital, Yangzhou University, Nanjing, P.R. ChinaSchool of Basic Medicine and Clinical Pharmacy, China Pharmaceutical University, Nanjing, P.R. ChinaSchool of Basic Medicine and Clinical Pharmacy, China Pharmaceutical University, Nanjing, P.R. ChinaSchool of Basic Medicine and Clinical Pharmacy, China Pharmaceutical University, Nanjing, P.R. ChinaDepartment of Pharmacy, Chengdu Integrated TCM &amp; Western Medicine Hospital, Chengdu University of TCM, Chengdu, P. R. China; Xu Zhang, PhD, Department of Pharmacy, Chengdu Integrated TCM &amp; Western Medicine Hospital, Chengdu University of TCM, 18# Wanxiang East Road, Chengdu, 610041, P. R.China.School of Basic Medicine and Clinical Pharmacy, China Pharmaceutical University, Nanjing, P.R. China; Department of Pharmacy, Nanjing First Hospital, Nanjing Medical University, Nanjing, P.R. China; Nanjing First Hospital, Nanjing University of Chinese Medicine, Nanjing, P.R. China; Chao Liu, PhD, Department of Pharmacy, Nanjing First Hospital, Nanjing Medical University, Nanjing 210029, P.R. China.General Clinical Research Center, Nanjing First Hospital, Nanjing Medical University, Nanjing, P.R. China; School of Basic Medicine and Clinical Pharmacy, China Pharmaceutical University, Nanjing, P.R. China; Nanjing First Hospital, Nanjing University of Chinese Medicine, Nanjing, P.R. China; Correspondence Address correspondence to: Qianming Du, PhD, General Clinical Research Center, Nanjing First Hospital, Nanjing Medical University, Nanjing 210006, P.R. China.Background &amp; Aims: Heterogeneity is the malignancy feature of colorectal cancer (CRC), which augments the difficulty of CRC treatment. Consensus molecular subtypes (CMSs) classified CRC into 4 subtypes. CMS4 is the most aggressive subtype, characterized with epithelial mesenchymal transition (EMT) and angiogenesis activation. However, the mechanism of CMS4 formation still remains unclear. We aimed to investigate the role of phospholamban (PLN) on CMS4 formation. Methods: Immunohistochemistry and Western blotting were used to detected PLN expressions. Transwell and wound-healing assays were used to evaluate migration and invasion of HCT116 and HT29. Tube formation assay was used to evaluate angiogenesis of HUVECs. GST pull-down was used to detected the interaction between PLN and AXIN2. The CAF-CT26 spleen co-transplantation mouse model was built to evaluate PLN’s effects on CRC metastasis. Results: PLN knockdown reversed CAFs’ conditional medium (CM)-induced EMT, cell migration, and angiogenesis (P < .01). PLN strongly bound to AXIN2, the main component of β-catenin degradation complex, and PLN knockdown increased β-catenin ubiquitination in CAFs (P < .01). PLN knockdown blocked GREM1 secretion (P < .01), and PLN overexpression-induced EMT, cell migration, and angiogenesis were blocked by anti-GREM1 neutralizing antibody (P < .01). Knockdown of BMP2 and VEGFR2 reversed CAFs’ CM induced EMT and angiogenesis effects, respectively (P < .01). PLN knockdown attenuated CAFs mediated tumor promoting effects in vivo (P < .01). Conclusions: PLN competitively binds with AXIN2 to increase β-catenin activity in CAFs. β-catenin signal induces GREM1 secretion, driving EMT and angiogenesis via BMP2 and VEGFR2, respectively. These findings demonstrate that PLN is a driver for CMS4 formation.http://www.sciencedirect.com/science/article/pii/S2352345X25000657AngiogenesisCancer-associated FibroblastsColorectal CancerEpithelial Mesenchymal TransitionPhospholamban
spellingShingle Tao Li
Yuxiang Fei
Xu Sun
Jun Zhu
Xin Fang
Fanjun Meng
Danyi Wang
Xu Zhang
Chao Liu
Qianming Du
Over-expressed Phospholamban in Cancer-associated Fibroblasts Is a Driver for CMS4 Subtype Colorectal Cancer FormationSummary
Cellular and Molecular Gastroenterology and Hepatology
Angiogenesis
Cancer-associated Fibroblasts
Colorectal Cancer
Epithelial Mesenchymal Transition
Phospholamban
title Over-expressed Phospholamban in Cancer-associated Fibroblasts Is a Driver for CMS4 Subtype Colorectal Cancer FormationSummary
title_full Over-expressed Phospholamban in Cancer-associated Fibroblasts Is a Driver for CMS4 Subtype Colorectal Cancer FormationSummary
title_fullStr Over-expressed Phospholamban in Cancer-associated Fibroblasts Is a Driver for CMS4 Subtype Colorectal Cancer FormationSummary
title_full_unstemmed Over-expressed Phospholamban in Cancer-associated Fibroblasts Is a Driver for CMS4 Subtype Colorectal Cancer FormationSummary
title_short Over-expressed Phospholamban in Cancer-associated Fibroblasts Is a Driver for CMS4 Subtype Colorectal Cancer FormationSummary
title_sort over expressed phospholamban in cancer associated fibroblasts is a driver for cms4 subtype colorectal cancer formationsummary
topic Angiogenesis
Cancer-associated Fibroblasts
Colorectal Cancer
Epithelial Mesenchymal Transition
Phospholamban
url http://www.sciencedirect.com/science/article/pii/S2352345X25000657
work_keys_str_mv AT taoli overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary
AT yuxiangfei overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary
AT xusun overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary
AT junzhu overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary
AT xinfang overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary
AT fanjunmeng overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary
AT danyiwang overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary
AT xuzhang overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary
AT chaoliu overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary
AT qianmingdu overexpressedphospholambanincancerassociatedfibroblastsisadriverforcms4subtypecolorectalcancerformationsummary