Mitochondrial fusion heterogeneity drives bidirectional tumor phenotypic transition in combined hepatocellular–cholangiocarcinoma

L Lin Chen D Dalin Wang (State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University) W Weidong Qin (Department of Health Statistics, School of Preventive Medicine, Fourth Military Medical University) G Gang Wang D Dan Wu (Key Laboratory of Freshwater Fish Reproduction and Development, Ministry of Education, State Key Laboratory Breeding Base of Eco-Environments and Bio-Resources of the Three Gorges Reservoir Region, School of Life Sciences, Southwest University) J Jiaying Li X Xingchen Wang (State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University) Y Yinping Wang (State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University) X Xiacheng Sun (State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University) J Jing Zhao S Shanshan Guo (State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University) L Lele Ji (National Demonstration Center for Experimental Basic Medical Science Education, Fourth Military Medical University) J Jiming Tian (State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University) R Rui Ding Y Yongzhan Nie (National Clinical Research Center for Digestive Diseases, Xijing Hospital, Fourth Military Medical University) J Jinliang Xing (State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University) Q Qichao Huang (State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University)

Abstract

Dysregulation of mitochondrial dynamics modulates malignant cell fate; however, the substantial heterogeneity in mitochondrial dynamics among tumor cells within individual tumor nodules and the resultant functional consequences remain inadequately characterized. In this study, we induced mosaic impairment of mitochondrial fusion in mouse liver under tumorigenic conditions and unexpectedly identified the formation of combined hepatocellular-cholangiocarcinoma (cHC), a monoclonal tumor displaying features of both hepatocellular carcinoma (HCC) and intrahepatic cholangiocarcinoma (ICC). Restoration of the mitochondrial fusion protein MFN1 effectively suppressed cHC development. Analysis of human cHC samples revealed that ICC-like cells exhibit more pronounced mitochondrial fusion impairment compared to HCC-like cells. Mechanistically, increasing impairment of mitochondrial fusion resulted in a dose-dependent elevation of reactive oxygen species (ROS). Low levels of ROS upregulated HNF4α, promoting HCC-like differentiation, whereas high ROS levels activated HES1, facilitating ICC-like differentiation. Collectively, these results demonstrate that heterogeneity in mitochondrial dynamics is a critical determinant of cHC path-ogenesis.

Article Details

Volume / Issue Vol. 123, Issue 18
Published May 05, 2026
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (17)

L

Lin Chen

D

Dalin Wang

State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University

W

Weidong Qin

Department of Health Statistics, School of Preventive Medicine, Fourth Military Medical University

G

Gang Wang

D

Dan Wu

Key Laboratory of Freshwater Fish Reproduction and Development, Ministry of Education, State Key Laboratory Breeding Base of Eco-Environments and Bio-Resources of the Three Gorges Reservoir Region, School of Life Sciences, Southwest University

J

Jiaying Li

X

Xingchen Wang

State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University

Y

Yinping Wang

State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University

X

Xiacheng Sun

State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University

J

Jing Zhao

S

Shanshan Guo

State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University

L

Lele Ji

National Demonstration Center for Experimental Basic Medical Science Education, Fourth Military Medical University

J

Jiming Tian

State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University

R

Rui Ding

Y

Yongzhan Nie

National Clinical Research Center for Digestive Diseases, Xijing Hospital, Fourth Military Medical University

J

Jinliang Xing

State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University

Q

Qichao Huang

State Key Laboratory of Holistic Integrative Management of Gastrointestinal Cancers and Department of Physiology and Pathophysiology, Fourth Military Medical University