Clinical and Molecular Hepatology

"Ju-Seog Lee"

Original Article

Integrative multi-omics profiling identifies infiltrative hepatocellular carcinoma as an immunotherapy-resistant subtype with distinct molecular features: Won Suk Lee, Seonjeong Woo, Sung Hwan Lee, Gae Hoon Jo, Ilhwan Kim, Hyeyeong Kim, Chansik An, Sanghoon Jung, Gwangil Kim, Haeyoun Kang, Beodeul Kang, Jung Sun Kim, Ho Yeong Lim, Incheon Kang, Hannah Yang, So Jung Kong, Dahyeon Son, Dong Jun Shin, Woo Young Kwon, Da-Yeon Lee, Ju-Seog Lee, Junho Park, Youngsoo Kim, Sohyun Hwang, Chan Kim, Hong Jae Chon; Clin Mol Hepatol 2026;32(1):258-275.
Published online October 27, 2025; DOI: https://doi.org/10.3350/cmh.2025.0792

Background/Aims
Hepatocellular carcinoma (HCC) exhibits substantial morphological and biological heterogeneity. Clinical and molecular relevance of the infiltrative subtype remains poorly defined in the context of cancer immunotherapy. We aimed to evaluate the prognostic impact and molecular features of infiltrative HCC in patients treated with first-line atezolizumab plus bevacizumab (Ate/Bev).
Methods
We included 307 patients with advanced HCC treated with Ate/Bev and classified them into four gross morphological types based on imaging. Multi-omics profiling was conducted on tumor samples. Type IV infiltrative signature was derived and externally validated using five independent HCC cohorts, including IMbrave150.
Results
Infiltrative morphology, encompassing pure and mixed forms, was present in 42.7% of advanced HCC and associated with advanced disease features and compromised liver function. Patients with type IV infiltrative HCC showed lowest
objective
response rate (14.6%) and worst progression-free (median, 2.8 months) and overall survival (median, 7.1 months). Infiltrative morphology remained an independent predictor of poor outcomes after multivariable adjustment for confounders, including intrahepatic tumor extent. Genomic profiling revealed enriched TP53 and ATM loss-of-function mutations in type IV infiltrative HCC. Transcriptomic and proteomic analyses identified consistent activation of tumor proliferation, epithelial-mesenchymal transition, TGF-β signaling, and immunosuppressive pathways in type IV infiltrative HCC. Type IV infiltrative signature was significantly associated with poor survival across external datasets and retained independent prognostic value.
Conclusions
Infiltrative HCC is a clinically aggressive and molecularly distinct subtype of advanced HCC. Morphological classification and type IV infiltrative signatures may guide risk stratification and therapeutic decision-making in advanced HCC treated with immunotherapy.

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Prognostic Significance of Glypican-3 Expression in Hepatocellular Carcinoma Treated with Atezolizumab-Bevacizumab
Ji Hoon Kim, Ji Won Han, Hee Sun Cho, Jeong Won Jang, Kwon Yong Tak, Pil Soo Sung
Cancers.2025; 17(24): 3967. CrossRef

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Erratum

Hepatic neoplasm

Erratum to ‘Genomic biomarkers to predict response to atezolizumab plus bevacizumab immunotherapy in hepatocellular carcinoma: Insights from the IMbrave150 trial’ [Clin Mol Hepatol 2024;30:807-823]: Sun Young Yim, Sung Hwan Lee, Seung-Woo Baek, Bohwa Sohn, Yun Seong Jeong, Sang-Hee Kang, Kena Park, Hyewon Park, Sunyoung S. Lee, Ahmed O. Kaseb, Young Nyun Park, Sun-Hee Leem, Michael A. Curran, Ji Hoon Kim, Ju-Seog Lee; Clin Mol Hepatol 2025;31(2):669-670.
Published online February 27, 2025; DOI: https://doi.org/10.3350/cmh.2024.0333e; Corrects: Clin Mol Hepatol 2024;30(4):807

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Correspondences

Hepatic neoplasm

Correspondence to editorial 2 on “Genomic biomarkers to predict response to atezolizumab plus bevacizumab immunotherapy in hepatocellular carcinoma: insights from the IMbrave150 trial”: Sun Young Yim, Sung Hwan Lee, Ji Hoon Kim, Sunyoung S Lee, Ahmed O Kaseb, Ju-Seog Lee; Clin Mol Hepatol 2025;31(1):e84-e86.
Published online October 7, 2024; DOI: https://doi.org/10.3350/cmh.2024.0830

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Hepatic neoplasm

Correspondence to editorial 1 on “Genomic biomarkers to predict response to atezolizumab plus bevacizumab immunotherapy in hepatocellular carcinoma: insights from the IMbrave150 Trial”: Sung Hwan Lee, Sun Young Yim, Ji Hoon Kim, Sunyoung S. Lee, Ahmed O. Kaseb, Ju-Seog Lee; Clin Mol Hepatol 2025;31(1):e81-e83.
Published online October 7, 2024; DOI: https://doi.org/10.3350/cmh.2024.0829

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Reply to correspondence on “Genomic biomarkers to predict response to atezolizumab plus bevacizumab immunotherapy in hepatocellular carcinoma: Insights from the IMbrave150 trial”
Hiroaki Kanzaki, Yujin Hoshida
Clinical and Molecular Hepatology.2025; 31(1): e121. CrossRef

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Crossref

Hepatic neoplasm

Correspondence to letter to the editor on “Genomic biomarkers to predict response to atezolizumab plus bevacizumab immunotherapy in hepatocellular carcinoma: Insights from the IMbrave150 trial”: Sung Hwan Lee, Sun Young Yim, Ji Hoon Kim, Sunyoung S Lee, Ahmed O Kaseb, Peng Wei, Ju-Seog Lee; Clin Mol Hepatol 2025;31(1):e110-e112.
Published online October 2, 2024; DOI: https://doi.org/10.3350/cmh.2024.0828

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Original Article

Hepatic neoplasm

Genomic biomarkers to predict response to atezolizumab plus bevacizumab immunotherapy in hepatocellular carcinoma: Insights from the IMbrave150 trial: Sun Young Yim, Sung Hwan Lee, Seung-Woo Baek, Bohwa Sohn, Yun Seong Jeong, Sang-Hee Kang, Kena Park, Hyewon Park, Sunyoung S. Lee, Ahmed O. Kaseb, Young Nyun Park, Sun-Hee Leem, Michael A. Curran, Ji Hoon Kim, Ju-Seog Lee; Clin Mol Hepatol 2024;30(4):807-823.
Published online July 23, 2024; DOI: https://doi.org/10.3350/cmh.2024.0333

Background/Aims
Combination immunotherapy, exemplified by atezolizumab plus bevacizumab, has become the standard of care for inoperable hepatocellular carcinoma (HCC). However, the lack of predictive biomarkers and limited understanding of response mechanisms remain a challenge.
Methods
Using data from the IMbrave150plus cohort, we applied an immune signature score (ISS) predictor to stratify HCC patients treated with atezolizumab plus bevacizumab or with sorafenib alone into potential high and low response groups. By applying multiple statistical approaches including a Bayesian covariate prediction algorithm, we refined the signature to 10 key genes (ISS10) for clinical use while maintaining similar predictive power to the full model. We further validated ISS10 in an independent HCC cohort treated with nivolumab plus ipilimumab.
Results
The study identified a significant association between the ISS and treatment response. Among patients classified as high responders, those treated with the atezolizumab plus bevacizumab combination exhibited improved overall and progression-free survival as well as better
objective
response rate compared to those treated with sorafenib. We also observed a significant correlation between ISS10 and response to nivolumab plus ipilimumab treatment. Analysis of immune cell subpopulations revealed distinct characteristics associated with ISS subtypes. In particular, the ISS10 high subtype displayed a more favorable immune environment with higher proportions of antitumor macrophages and activated T-cells, potentially explaining its better response.
Conclusions
Our study suggests that ISS and ISS10 are promising predictive biomarkers for enhanced therapeutic outcomes in HCC patients undergoing combination immunotherapy. These markers are crucial for refining patient stratification and personalized treatment approaches to advance the effectiveness of standard-of-care regimens.

Citations

Citations to this article as recorded by

Targeting TIME in advanced hepatocellular carcinoma: Mechanisms of drug resistance and treatment strategies
Xinyi Ye, Xizhu Fang, Fangfang Li, Dan Jin
Critical Reviews in Oncology/Hematology.2025; 211: 104735. CrossRef
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Eun Ji Jang, Ho Joong Choi, Young Kyoung You, Deok Hwa Seo, Mi Hyun Kwon, Keungmo Yang, Jaejun Lee, Jeong Won Jang, Seung Kew Yoon, Ji Won Han, Pil Soo Sung
Cancers.2025; 17(9): 1548. CrossRef
Advances in cancer immunotherapy: historical perspectives, current developments, and future directions
Meiyin Zhang, Chaojun Liu, Jing Tu, Min Tang, Milad Ashrafizadeh, Noushin Nabavi, Gautam Sethi, Peiqing Zhao, Shijian Liu
Molecular Cancer.2025;[Epub] CrossRef
Management and Outcomes of Adverse Events Following Immune Checkpoint Inhibitor Treatment in Patients with Hepatocellular Carcinoma
Soon Kyu Lee, Bo Hyun Kim
Journal of Digestive Cancer Research.2025; 13(1): 65. CrossRef
Managing hepatocellular carcinoma recurrence after liver transplantation: emerging role of immune checkpoint inhibitors
Mohammad Saeid Rezaee-Zavareh, Soo Young Hwang, Naomy Kim, Hasmik Adetyan, Nguyen H. Tran, Ju Dong Yang
Discover Oncology.2025;[Epub] CrossRef
Hepatic Metabolic Signature and Its Association with the Response to Immunotherapy in Hepatocellular Carcinoma
Hyewon Park, Sowon Park, Kena Park, Sun Young Yim, Ju-Seog Lee, Sung Hwan Lee
ImmunoTargets and Therapy.2025; Volume 14: 787. CrossRef
Development and validation of a risk prediction model for patients with hepatocellular carcinoma receiving atezolizumab–bevacizumab
Heechul Nam, Dong Yun Kim, Do Young Kim, Ji Hoon Kim, Chang Wook Kim, Jaejun Lee, Keungmo Yang, Ji Won Han, Pil Soo Sung, Seung Kew Yoon, Hee Sun Cho, Hyun Yang, Si Hyun Bae, Soon Kyu Lee, Jung Hyun Kwon, Soon Woo Nam, Ahlim Lee, Do Seon Song, U Im Chang,
Hepatology.2025;[Epub] CrossRef
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Efficacy and Safety of Different Doses of Bevacizumab Combined with Atezolizumab in Unresectable Hepatocellular Carcinoma
Shaobo Zhang, Jiabei Wang, Zebin Zhu, Peng Ji, Yanli Wang, Kun Cheng, Björn Nashan, Lianxin Liu, Shugeng Zhang
Journal of Hepatocellular Carcinoma.2025; Volume 12: 2007. CrossRef
Ultrasounic-radiomics models for predicting the response to Atezolizumab plus Bevacizumab in patients with unresectable hepatocellular carcinoma
Yiran Li, Zonghan Liu, Yi Qian, Kang Wang, Yijun Gu, Yan Chen, Haozheng Jiang, Shuqun Cheng, Dong Jiang, Xinjun Lu
PLOS One.2025; 20(10): e0334099. CrossRef
Prognostic Significance of Glypican-3 Expression in Hepatocellular Carcinoma Treated with Atezolizumab-Bevacizumab
Ji Hoon Kim, Ji Won Han, Hee Sun Cho, Jeong Won Jang, Kwon Yong Tak, Pil Soo Sung
Cancers.2025; 17(24): 3967. CrossRef
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Soon Kyu Lee, Soon Woo Nam, Ji Won Han, Jung Hyun Kwon
Cancers.2024; 16(20): 3543. CrossRef
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Mo-Wei Kong, Yang Yu, Ying Wan, Yu Gao, Chun-Xiang Zhang
World Journal of Gastrointestinal Oncology.2024; 16(11): 4518. CrossRef

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Review

Hepatic neoplasm

The mutational landscape of hepatocellular carcinoma: Ju-Seog Lee; Clin Mol Hepatol 2015;21(3):220-229.
Published online September 30, 2015; DOI: https://doi.org/10.3350/cmh.2015.21.3.220

Abstract
PDF

The development of hepatocellular carcinoma (HCC) is a complex process, and HCC arises from the accumulation of multiple genetic alterations leading to changes in the genomic landscape. Current advances in genomic technologies have revolutionized the search for genetic alterations in cancer genomes. Recent studies in which all coding exons in HCC were sequenced have shed new light on the genomic landscape of this malignant disease. Catalogues of these somatic mutations and systematic analysis of catalogued mutations will lead us to uncover candidate HCC driver genes, although further functional validation is needed to determine whether these genes play a causal role in the development of HCC. This review provides an overview of previously known oncogenes and new oncogene candidates in HCC that were uncovered from recent exome or whole-genome sequencing studies. This knowledge provides direction for future personalized treatment approaches for patients with HCC.

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