Molecular and Clinical Determinants of Acquired Resistance and Treatment Duration for Targeted Therapies in Colorectal Cancer

Clin Cancer Res. 2024 Jun 14;30(12):2672-2683. doi: 10.1158/1078-0432.CCR-23-4005.

Abstract

Purpose: Targeted therapies have improved outcomes for patients with metastatic colorectal cancer, but their impact is limited by rapid emergence of resistance. We hypothesized that an understanding of the underlying genetic mechanisms and intrinsic tumor features that mediate resistance to therapy will guide new therapeutic strategies and ultimately allow the prevention of resistance.

Experimental design: We assembled a series of 52 patients with paired pretreatment and progression samples who received therapy targeting EGFR (n = 17), BRAF V600E (n = 17), KRAS G12C (n = 15), or amplified HER2 (n = 3) to identify molecular and clinical factors associated with time on treatment (TOT).

Results: All patients stopped treatment for progression and TOT did not vary by oncogenic driver (P = 0.5). Baseline disease burden (≥3 vs. <3 sites, P = 0.02), the presence of hepatic metastases (P = 0.02), and gene amplification on baseline tissue (P = 0.03) were each associated with shorter TOT. We found evidence of chromosomal instability (CIN) at progression in patients with baseline MAPK pathway amplifications and those with acquired gene amplifications. At resistance, copy-number changes (P = 0.008) and high number (≥5) of acquired alterations (P = 0.04) were associated with shorter TOT. Patients with hepatic metastases demonstrated both higher number of emergent alterations at resistance and enrichment of mutations involving receptor tyrosine kinases.

Conclusions: Our genomic analysis suggests that high baseline CIN or effective induction of enhanced mutagenesis on targeted therapy underlies rapid progression. Longer response appears to result from a progressive acquisition of genomic or chromosomal instability in the underlying cancer or from the chance event of a new resistance alteration.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Chromosomal Instability
  • Colorectal Neoplasms* / drug therapy
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / pathology
  • Disease Progression
  • Drug Resistance, Neoplasm* / genetics
  • ErbB Receptors / antagonists & inhibitors
  • ErbB Receptors / genetics
  • Female
  • Gene Amplification
  • Humans
  • Male
  • Middle Aged
  • Molecular Targeted Therapy*
  • Mutation
  • Proto-Oncogene Proteins B-raf* / genetics
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Receptor, ErbB-2 / genetics
  • Receptor, ErbB-2 / metabolism

Substances

  • Proto-Oncogene Proteins B-raf
  • Proto-Oncogene Proteins p21(ras)
  • BRAF protein, human
  • Receptor, ErbB-2
  • KRAS protein, human
  • ErbB Receptors
  • ERBB2 protein, human