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Immune evasion from macrophages by NEAT1-induced CD24 in liver cancer

Oncogene volume 44, pages 3652–3664 (2025)Cite this article

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Abstract

The limited efficacy of immune checkpoint inhibitors in hepatocellular carcinoma (HCC) can arise from the involvement of immunosuppressive cells, such as macrophages. In the present study, we found that the long noncoding RNA NEAT1, particularly its short isoform (NEAT1v1) induced the expression of CD24, which is known as an immune checkpoint molecule for macrophages. Mechanistically, NEAT1v1 sponged miR-320a-3p to upregulate the transcription factor SP1, which in turn, activated CD24 transcription. A spheroid co-culture of primary or THP-1-derived macrophages with HCC cells revealed that NEAT1v1 suppressed M1 marker expression and phagocytic activity in macrophages. In a syngeneic subcutaneous model of HCC, Neat1v1 increased the tumor infiltration of M2-like macrophages and induced resistance to anti-Pd-1 antibody, while combination of the anti-Pd-1 and anti-Cd24 antibodies significantly suppressed the tumor growth. Finally, NEAT1, SP1, and CD24 expression increased in tumor tissues from patients with HCC, compared to adjacent normal tissues, whereas miR-320a-3p was significantly downregulated. Moreover, plasma NEAT1 cell-free RNA was significantly decreased after therapeutic intervention. Taken together, NEAT1v1 protects HCC cells from macrophages by sending a “Don’t Eat Me” signal via CD24, and is therefore, a potential target molecule for the treatment and diagnosis of HCC.

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Fig. 1: Upregulation of CD24 in liver cancer cells by NEAT1v1.
Fig. 2: Inhibition of phagocytosis by NEAT1v1 through CD24.
Fig. 3: Promotion of M2-like macrophage polarization by NEAT1v1 through CD24.
Fig. 4: Upregulation of CD24 by NEAT1v1 through SP1.
Fig. 5: NEAT1v1-mediated suppression of miR-320a-3p by acting as a ceRNA.
Fig. 6: Promotion of tumor growth and M2-like TAM polarization by Neat1v1.

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All raw data are available in the manuscript and its supplementary files or from the corresponding author upon reasonable request.

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Acknowledgements

We thank Dr. Mirco Castoldi (University Hospital of Düsseldorf) for technical advice on miQPCR. This research was partly performed at Research Initiative Center, Tottori University, and the Tottori Bio Frontier managed by Tottori prefecture. The authors would like to thank Enago (www.enago.jp) for the English language review.

Funding

This work was supported by JSPS KAKENHI Grant Number 23K07437 (HT).

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Authors and Affiliations

  1. Division of Regenerative Medicine and Therapeutics, Department of Genomic Medicine and Regenerative Therapy, Faculty of Medicine, Tottori University, Yonago, Japan

    Hiroyuki Tsuchiya & Daisuke Nanba

  2. Division of Gastrointestinal and Pediatric Surgery, Department of Surgery, Faculty of Medicine, Tottori University, Yonago, Japan

    Takehiko Hanaki, Naruo Tokuyasu & Yoshiyuki Fujiwara

  3. Division of Medical Education, Department of Medical Education, Faculty of Medicine, Tottori University, Yonago, Japan

    Takehiko Hanaki

  4. Division of Organ Pathology, Department of Pathology, Faculty of Medicine, Tottori University, Yonago, Japan

    Tomohiko Sakabe & Yoshihisa Umekita

  5. Division of Gastroenterology and Nephrology, Department of Multidisciplinary Internal Medicine, Faculty of Medicine, Tottori University, Yonago, Japan

    Takakazu Nagahara & Hajime Isomoto

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  1. Hiroyuki Tsuchiya
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Contributions

HT performed most of the experiments, analyzed the data, and wrote the manuscript. TH, NT, and TN contributed to the collection of liver and blood samples and the curation of clinical information. TS and YU conducted immunohistochemistry and its quantitative analysis. HI and YF conceptualized and supervised the project. DN supervised the project, and reviewed and edited the manuscript. All authors have read and approved the final manuscript.

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Correspondence to Hiroyuki Tsuchiya.

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Tsuchiya, H., Hanaki, T., Sakabe, T. et al. Immune evasion from macrophages by NEAT1-induced CD24 in liver cancer. Oncogene 44, 3652–3664 (2025). https://doi.org/10.1038/s41388-025-03537-3

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