Correspondence to editorial on “Targeting TM4SF1 promotes tumor senescence enhancing CD8+ T cell cytotoxic function in hepatocellular carcinoma”

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Clin Mol Hepatol. 2025;31(2):e197-e199
Publication date (electronic) : 2025 February 5
doi : https://doi.org/10.3350/cmh.2025.0085
1Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China
2Hubei Key Laboratory of Hepato-Pancreato-Biliary Diseases, Wuhan, Hubei, China
3Key Laboratory of Organ Transplantation, Ministry of Education; NHC Key Laboratory of Organ Transplantation; Key Laboratory of Organ Transplantation, Chinese Academy of Medical Sciences, Wuhan, China
Corresponding author : Zhanguo Zhang Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Hubei Province for the Clinical Medicine Research Center of Hepatic Surgery, 1095 Jiefang Avenue, 430000 Wuhan, Hubei Province, China Tel: +86-027-83663400, Fax: +86-027-83662851, E-mail: zhanguo_tjh@hust.edu.cn
Editor: Han Ah Lee, Chung-Ang University College of Medicine, Korea
Received 2025 January 22; Accepted 2025 February 1.

Dear Editor,

We sincerely thank Dr. Valerie Chew for her insightful comments and constructive feedback on our recent study investigating the role of transmembrane 4 L six family member 1 (TM4SF1) in hepatocellular carcinoma (HCC) [1]. As highlighted in our research, TM4SF1 is a key regulator of HCC progression. We demonstrated that targeting TM4SF1 effectively suppressed tumor growth, induced tumor cell senescence, and sensitized tumors to immunotherapy in vivo [2]. These findings provide a novel therapeutic strategy for the treatment of HCC.

TM4SF1 is known to be highly expressed in various malignancies and is closely associated with tumor progression [3]. However, most previous studies have focused on epithelial-derived cancers, leaving the role of TM4SF1 in HCC largely unexplored. In our study, we analyzed multiple HCC databases and found that TM4SF1 is significantly overexpressed in HCC tissues compared to adjacent tissues. High expression of TM4SF1 was also correlated with poor clinical outcomes. Further phenotypic analyses revealed that TM4SF1 promoted tumor cell proliferation and plays a crucial role in regulating cellular senescence. Specifically, TM4SF1 suppressed the expression of senescence markers p21 and p16 and regulated a non-secretory senescence phenotype. Mechanistically, our findings demonstrated that TM4SF1 facilitated the interaction between AKT1 and PDPK1, which enhanced the phosphorylation of the AKT pathway, subsequently promoted tumor cell proliferation while inhibiting cellular senescence. Collectively, these results identify TM4SF1 as a critical driver of HCC progression.

In addition to its intrinsic effects on tumor cells, TM4SF1 has significant influence on tumor microenvironment. Our study revealed that TM4SF1-mediated activation of the AKT signaling pathway upregulated programmed cell death ligand 1 expression while downregulating major histocompatibility complex class I on the tumor cell surface, which was consistent with other studies [4,5]. These changes impaired the cytotoxic function of CD8+ T cells and promoted their exhaustion, contributing to immune evasion. To validate these findings, we utilized an immunocompetent mouse model of HCC established via hydrodynamic tail vein injection. Knockdown of TM4SF1 using three distinct shRNA sequences reduced tumor burden and restored CD8+ T cell cytotoxic function. Co-culture experiments involving human CD8+ T cells and tumor cells confirmed the immunosuppressive effects of TM4SF1. These results exhibit the key role of TM4SF1 in HCC microenvironment.

To explore the therapeutic potential of targeting TM4SF1, we employed adeno-associated virus (AAV) to knock down TM4SF1 expression in vivo. This approach significantly suppressed tumor growth, induced tumor cell senescence, and sensitized tumors to anti-programmed cell death 1 therapy. Additionally, analysis of the clinical cohort undergoing immunotherapy revealed that TM4SF1 expression was elevated in non-responders compared to responders. This finding further underscores the dual role of TM4SF1 as a therapeutic target and a potential biomarker for predicting immunotherapy efficacy.

Our study integrates tumor cell senescence and tumor microenvironment to elucidate the role of TM4SF1 in HCC. These findings provide critical insights into its therapeutic potential. As Dr. Valerie Chew summarized, TM4SF1 is an attractive target for cancer therapy. Previous studies have reported that targeting TM4SF1 using antibody-drug conjugates or antibodies can effectively inhibit tumor progression [6,7]. However, the interplay between TM4SF1-targeted therapies and the immune microenvironment remains to be investigated. In recent years, research on tumor cell senescence has gained considerable attention, particularly in HCC [8,9]. Emerging therapeutic strategies, such as inducing and subsequently eliminating senescent tumor cells, show promising effect in fighting cancer [10]. These approaches, when combined with TM4SF1-targeted therapies, may yield synergistic effects. Moreover, our study has limitations that warrant further investigation. While AAV-based therapy demonstrates effective knockdown of TM4SF1 expression in our study. AAV is also associated with potential risks, including hepatotoxicity, vascular injury, and other adverse effects in animal experiments [11]. These challenges highlight the need for further optimization of AAV. As a membrane protein, the development of specific inhibitors or optimized neutralizing antibodies targeting TM4SF1 holds great promise for clinical applications. Due to the epidemiological characteristics of our cohort, the majority of HCC patients included in our study were HBV-positive. Expanding our research to include HCC cases driven by other etiologies will help validate the broader applicability of our findings. Additionally, we will focus on the mechanisms underlying TM4SF1-mediated HCC progression and immune modulation in greater detail.

In conclusion, we sincerely appreciate Dr. Valerie Chew’s recognition of the significance our findings and grateful for Dr. Valerie Chew’s summary of our work, especially for the beautifully created illustration. Despite certain limitations, our study highlights the potential of targeting TM4SF1 to suppress HCC progression and enhance immunotherapy efficacy. We envision that TM4SF1-targeted therapies, when combined with neoadjuvant therapy or other systemic treatments, could offer new hope for HCC patients.

Notes

Authors’ contribution

Data collection and analysis: All authors. Manuscript drafting and revision: All authors.

Conflicts of Interest

The authors have no conflicts to disclose.

Abbreviations

AAV

adeno-associated virus

HCC

hepatocellular carcinoma

TM4SF1

transmembrane 4 L six family member 1

References

1. Chew V. Targeting TM4SF1 to overcome immunotherapy resistance in hepatocellular carcinoma: Editorial on “Targeting TM4SF1 promotes tumor senescence enhancing CD8+ T cell cytotoxic function in hepatocellular carcinoma”. Clin Mol Hepatol 2025;31:642–645.
2. Zeng W, Liu F, Liu Y, Zhang Z, Hu H, Ning S, et al. Targeting TM4SF1 promotes tumor senescence enhancing CD8+ T cell cytotoxic function in hepatocellular carcinoma. Clin Mol Hepatol 2025;31:489–508.
3. Fu F, Yang X, Zheng M, Zhao Q, Zhang K, Li Z, et al. Role of transmembrane 4 L six family 1 in the development and progression of cancer. Front Mol Biosci 2020;7:202.
4. Zheng X, Chen J, Deng M, Ning K, Peng Y, Liu Z, et al. G3BP1 and SLU7 jointly promote immune evasion by downregulating MHC-I via PI3K/Akt activation in bladder cancer. Adv Sci (Weinh) 2024;11:e2305922.
5. Lastwika KJ, Wilson W 3rd, Li QK, Norris J, Xu H, Ghazarian SR, et al. Control of PD-L1 expression by oncogenic activation of the AKT-mTOR pathway in non-small cell lung cancer. Cancer Res 2016;76:227–238.
6. Chen G, She X, Yin Y, Ma J, Gao Y, Gao H, et al. Targeting TM4SF1 exhibits therapeutic potential via inhibition of cancer stem cells. Signal Transduct Target Ther 2022;7:350.
7. Visintin A, Knowlton K, Tyminski E, Lin CI, Zheng X, Marquette K, et al. Novel anti-TM4SF1 antibody-drug conjugates with activity against tumor cells and tumor vasculature. Mol Cancer Ther 2015;14:1868–1876.
8. Lao Y, Cui X, Xu Z, Yan H, Zhang Z, Zhang Z, et al. GlutarylCoA dehydrogenase suppresses tumor progression and shapes an anti-tumor microenvironment in hepatocellular carcinoma. J Hepatol 2024;81:847–861.
9. Chen HA, Ho YJ, Mezzadra R, Adrover JM, Smolkin R, Zhu C, et al. Senescence rewires microenvironment sensing to facilitate antitumor immunity. Cancer Discov 2023;13:432–453.
10. Schmitt CA, Wang B, Demaria M. Senescence and cancer - role and therapeutic opportunities. Nat Rev Clin Oncol 2022;19:619–636.
11. Wang JH, Gessler DJ, Zhan W, Gallagher TL, Gao G. Adeno-associated virus as a delivery vector for gene therapy of human diseases. Signal Transduct Target Ther 2024;9:78.

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