Qualitative Ras pathway signature for cetuximab therapy reveals resistant mechanism in colorectal cancer

FEBS J. 2020 Dec;287(23):5236-5248. doi: 10.1111/febs.15306. Epub 2020 Apr 20.

Abstract

Cetuximab therapy, which heavily relies on the activation of Ras pathway, has been used in KRAS, NRAS, BRAF, and PIK3CA wild-type colorectal cancer (CRC) (Ras-normal). However, the response rate only reached 60%, due to false-negative mutation detection and mutation-like transcriptome features in wild-type patients. Herein, by integrating RNA-seq, microarray, and mutation data, we developed a Ras pathway signature by characterizing KRAS/NRAS/BRAF/PIK3CA mutations to identify the hidden nonresponders from the Ras-normal patients by mutation detection. Using public and in-house data of CRC patients treated with cetuximab, discovery of the signature could identify cetuximab-resistant samples from the Ras-normal samples. Cetuximab resistance-related genes, such as PTEN, were significantly and frequently mutated in the identified Ras-activated samples, whereas two cetuximab sensitivity-related genes, APC and TP53, showed comutation and significantly higher mutation frequencies in the remaining Ras-normal samples. Furthermore, all the NF1- and BCL2L1-mutated samples were identified as Ras-activated from the Ras-normal samples by the Ras pathway signature with significantly under-regulated expression. Genes co-expressed with the two genes were both involved in Ras signaling pathway, the out-of-control of which could be attributed by the genes' loss-of-function mutations. To improve the treatment of cetuximab in CRC, NF1 and BCL2L1 could be used as complementary detection technique to those applied in clinical. In conclusion, the proposed Ras pathway signature could identify the hidden CRC patients resistant to cetuximab therapy and help to reveal resistance mechanisms.

Keywords: KRAS/NRAS/BRAF/PIK3CA mutation; NF1 loss-of-function; Ras pathway activation; cetuximab; colorectal cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents, Immunological / pharmacology
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism*
  • Cetuximab / pharmacology*
  • Class I Phosphatidylinositol 3-Kinases / genetics
  • Class I Phosphatidylinositol 3-Kinases / metabolism
  • Cohort Studies
  • Colorectal Neoplasms / drug therapy*
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / metabolism
  • Colorectal Neoplasms / pathology
  • Drug Resistance, Neoplasm / genetics*
  • GTP Phosphohydrolases / genetics
  • GTP Phosphohydrolases / metabolism*
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Humans
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mutation
  • Prognosis
  • Proto-Oncogene Proteins B-raf / genetics
  • Proto-Oncogene Proteins B-raf / metabolism
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Proto-Oncogene Proteins p21(ras) / metabolism*
  • Survival Rate

Substances

  • Antineoplastic Agents, Immunological
  • Biomarkers, Tumor
  • KRAS protein, human
  • Membrane Proteins
  • Class I Phosphatidylinositol 3-Kinases
  • PIK3CA protein, human
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf
  • GTP Phosphohydrolases
  • NRAS protein, human
  • Proto-Oncogene Proteins p21(ras)
  • Cetuximab