KHDRBS3 promotes multi-drug resistance and anchorage-independent growth in colorectal cancer

Cancer Sci. 2021 Mar;112(3):1196-1208. doi: 10.1111/cas.14805. Epub 2021 Feb 2.

Abstract

5-Fluorouracil (5-FU) is one of the most frequently used pharmacological agents in the treatment of colorectal cancer (CRC). Resistance to chemotherapy is a major cause of treatment failure of CRC, and it is a well known fact that cancer stem cells play a significant role in the acquisition of drug resistance. In this study, we focused on the KHDRBS3 gene that encodes KH RNA Binding Domain Containing, Signal Transduction Associated 3. We first clarified the relationship between KHDRBS3 and 5-FU resistance. We then observed higher expression levels of KHDRBS3 in KRAS-mutant organoids and cell lines in comparison with KRAS wild-type organoids and cell lines. Immunohistochemical analysis using CRC cases revealed that the prognosis of KHDRBS3-positive patients was significantly worse compared with that of KHDRBS3-negative patients. Univariate and multivariate Cox proportional hazards analyses showed that KHDRBS3 was an independent prognostic factor in patients with CRC. We determined that KHDRBS3 might play a crucial role in the acquisition of stem cell properties, such as drug resistance and spheroid/organoid formation, by regulating CD44 variant expression and the Wnt signaling pathway. In an immunodeficient mouse model, KHDRBS3-positive cells showed efficient tumor formation and formed metastatic lesions in the lungs. These results indicated that KHDRBS3 plays a crucial role in drug resistance and anchorage-independent growth by maintaining stem cell-like features in CRC cells. KHDRBS3 could be a promising candidate marker for predicting chemotherapeutic effect and prognosis in CRC patients.

Keywords: 5-FU; KHDRBS3; cancer stem cell; colorectal cancer; drug resistance.

MeSH terms

  • Aged
  • Aged, 80 and over
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Cell Line, Tumor
  • Colectomy
  • Colon / pathology
  • Colon / surgery
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / mortality
  • Colorectal Neoplasms / pathology
  • Colorectal Neoplasms / therapy*
  • Drug Resistance, Multiple / genetics*
  • Drug Resistance, Neoplasm / genetics*
  • Female
  • Fluorouracil / pharmacology
  • Fluorouracil / therapeutic use
  • Gene Expression Regulation, Neoplastic
  • Gene Knockout Techniques
  • Humans
  • Hyaluronan Receptors / genetics
  • Male
  • Mice
  • Middle Aged
  • Mutation
  • Neoplastic Stem Cells / pathology
  • Organoids / drug effects
  • Organoids / metabolism
  • Prognosis
  • Proto-Oncogene Proteins p21(ras) / genetics
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Survival Analysis
  • Wnt Signaling Pathway / genetics
  • Xenograft Model Antitumor Assays

Substances

  • CD44 protein, human
  • Hyaluronan Receptors
  • KHDRBS3 protein, human
  • KRAS protein, human
  • RNA-Binding Proteins
  • Proto-Oncogene Proteins p21(ras)
  • Fluorouracil