SPG21, a potential oncogene targeted by miR-128-3p, amplifies HBx-induced carcinogenesis and chemoresistance via activation of TRPM7-mediated JNK pathway in hepatocellular carcinoma

Cell Oncol (Dordr). 2024 Oct;47(5):1757-1778. doi: 10.1007/s13402-024-00955-5. Epub 2024 May 16.

Abstract

Purpose: Chronic hepatitis B virus (HBV) infection is the primary risk factor for the malignant progression of hepatocellular carcinoma (HCC). It has been reported that HBV X protein (HBx) possesses oncogenic properties, promoting hepatocarcinogenesis and chemoresistance. However, the detailed molecular mechanisms are not fully understood. Here, we aim to investigate the effects of miR-128-3p/SPG21 axis on HBx-induced hepatocarcinogenesis and chemoresistance.

Methods: The expression of SPG21 in HCC was determined using bioinformatics analysis, quantitative real-time PCR (qRT-PCR), western blotting, and immunohistochemistry (IHC). The roles of SPG21 in HCC were elucidated through a series of in vitro and in vivo experiments, including real-time cellular analysis (RTCA), matrigel invasion assay, and xenograft mouse model. Pharmacologic treatment and flow cytometry were performed to demonstrate the potential mechanism of SPG21 in HCC.

Results: SPG21 expression was elevated in HCC tissues compared to adjacent non-tumor tissues (NTs). Moreover, higher SPG21 expression correlated with poor overall survival. Functional assays revealed that SPG21 fostered HCC tumorigenesis and invasion. MiR-128-3p, which targeted SPG21, was downregulated in HCC tissues. Subsequent analyses showed that HBx amplified TRPM7-mediated calcium influx via miR-128-3p/SPG21, thereby activating the c-Jun N-terminal kinase (JNK) pathway. Furthermore, HBx inhibited doxorubicin-induced apoptosis by engaging the JNK pathway through miR-128-3p/SPG21.

Conclusion: The study suggested that SPG21, targeted by miR-128-3p, might be involved in enhancing HBx-induced carcinogenesis and doxorubicin resistance in HCC via the TRPM7/Ca2+/JNK signaling pathway. This insight suggested that SPG21 could be recognized as a potential oncogene, offering a novel perspective on its role as a prognostic factor and a therapeutic target in the context of HCC.

Keywords: HBx; Hepatocellular carcinoma; JNK pathway; SPG21; TRPM7; miR-128-3p.

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Carcinogenesis* / genetics
  • Carcinoma, Hepatocellular* / genetics
  • Carcinoma, Hepatocellular* / metabolism
  • Carcinoma, Hepatocellular* / pathology
  • Carcinoma, Hepatocellular* / virology
  • Cell Line, Tumor
  • Cell Proliferation
  • Doxorubicin / pharmacology
  • Doxorubicin / therapeutic use
  • Drug Resistance, Neoplasm* / genetics
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Hep G2 Cells
  • Humans
  • Liver Neoplasms* / genetics
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / pathology
  • Liver Neoplasms* / virology
  • MAP Kinase Signaling System* / genetics
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude*
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Middle Aged
  • Oncogenes / genetics
  • Protein Serine-Threonine Kinases
  • TRPM Cation Channels* / genetics
  • TRPM Cation Channels* / metabolism
  • Trans-Activators* / genetics
  • Trans-Activators* / metabolism
  • Viral Regulatory and Accessory Proteins*

Substances

  • MicroRNAs
  • hepatitis B virus X protein
  • Viral Regulatory and Accessory Proteins
  • Trans-Activators
  • TRPM Cation Channels
  • MIRN128 microRNA, human
  • TRPM7 protein, human
  • Doxorubicin
  • Protein Serine-Threonine Kinases