ANXA10 sensitizes microsatellite instability-high colorectal cancer to anti-PD-1 immunotherapy via assembly of HLA-DR dimers by regulating CD74

Cell Biol Toxicol. 2025 Jan 10;41(1):25. doi: 10.1007/s10565-024-09982-2.

Abstract

Background: Microsatellite instability-high (MSI-H) metastatic colorectal cancer (CRC) patients are the dominant population in immune checkpoint blockade treatments, while more than half of them could not benefit from single-agent immunotherapy. We tried to identify the biomarker of MSI-H CRC and explore its role and mechanism in anti-PD-1 treatments. Tumor-specific MHC-II was linked to a better response to anti-PD-1 in MSI-H CRC and CD74 promoted assembly and transport of HLA-DR dimers.

Methods: The characteristic gene was screened by data analysis of single-cell and bulk transcriptome sequencing from public datasets. MSI-H CRC cells co-cultured with peripheral blood mononuclear cells and syngeneic model in C57BL/6 mice were performed to detect the sensitivity to anti-PD-1 treatments respectively.

Results: ANXA10 was identified as a characteristic gene of MSI-H CRC and its expression was obviously greater in MSI-H than MSS CRC. ANXA10 significantly sensitized MSI-H CRC to anti-PD-1 treatments in vitro and in vivo. Specifically, ANXA10 promoted HLA-DR dimers in and on the surface of MSI-H CRC by increasing CD74 expression. Besides, this work demonstrated that ANXA10 contributed to better clinical benefits with anti-PD-1 therapy in MSI-H CRC patients.

Conclusions: Our results provided a novel molecular marker ANXA10 to identify benefit population of MSI-H CRC for improving efficacy of anti-PD-1 and contributed to selection of treatment strategies.

Keywords: ANXA10; Microsatellite instability-high colorectal cancer; Sensitivity to anti-PD-1 therapy; Tumor-specific MHC-II.

MeSH terms

  • Animals
  • Antigens, Differentiation, B-Lymphocyte / genetics
  • Antigens, Differentiation, B-Lymphocyte / metabolism
  • Cell Line, Tumor
  • Colorectal Neoplasms* / drug therapy
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / immunology
  • Female
  • HLA-DR Antigens* / genetics
  • HLA-DR Antigens* / metabolism
  • Histocompatibility Antigens Class II / genetics
  • Histocompatibility Antigens Class II / metabolism
  • Humans
  • Immune Checkpoint Inhibitors* / pharmacology
  • Immunotherapy* / methods
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Microsatellite Instability* / drug effects
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / metabolism

Substances

  • Immune Checkpoint Inhibitors
  • HLA-DR Antigens
  • Programmed Cell Death 1 Receptor
  • Antigens, Differentiation, B-Lymphocyte
  • invariant chain
  • Histocompatibility Antigens Class II