Lineage plasticity in cancer: a shared pathway of therapeutic resistance

Nat Rev Clin Oncol. 2020 Jun;17(6):360-371. doi: 10.1038/s41571-020-0340-z. Epub 2020 Mar 9.

Abstract

Lineage plasticity, the ability of cells to transition from one committed developmental pathway to another, has been proposed as a source of intratumoural heterogeneity and of tumour adaptation to an adverse tumour microenvironment including exposure to targeted anticancer treatments. Tumour cell conversion into a different histological subtype has been associated with a loss of dependency on the original oncogenic driver, leading to therapeutic resistance. A well-known pathway of lineage plasticity in cancer - the histological transformation of adenocarcinomas to aggressive neuroendocrine derivatives - was initially described in lung cancers harbouring an EGFR mutation, and was subsequently reported in multiple other adenocarcinomas, including prostate cancer in the presence of antiandrogens. Squamous transformation is a subsequently identified and less well-characterized pathway of adenocarcinoma escape from suppressive anticancer therapy. The increased practice of tumour re-biopsy upon disease progression has increased the recognition of these mechanisms of resistance and has improved our understanding of the underlying biology. In this Review, we provide an overview of the impact of lineage plasticity on cancer progression and therapy resistance, with a focus on neuroendocrine transformation in lung and prostate tumours. We discuss the current understanding of the molecular drivers of this phenomenon, emerging management strategies and open questions in the field.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Adenocarcinoma / drug therapy
  • Adenocarcinoma / genetics*
  • Adenocarcinoma / pathology
  • Androgen Antagonists / therapeutic use
  • Cell Lineage / genetics*
  • Cell Plasticity / genetics*
  • Drug Resistance, Neoplasm / genetics*
  • Epithelial-Mesenchymal Transition
  • ErbB Receptors / genetics
  • Humans
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / genetics*
  • Lung Neoplasms / pathology
  • Male
  • Neuroendocrine Tumors / genetics*
  • Neuroendocrine Tumors / pathology
  • PTEN Phosphohydrolase / genetics
  • Prostatic Neoplasms / drug therapy
  • Prostatic Neoplasms / genetics*
  • Prostatic Neoplasms / pathology
  • Prostatic Neoplasms, Castration-Resistant / drug therapy
  • Prostatic Neoplasms, Castration-Resistant / genetics
  • Prostatic Neoplasms, Castration-Resistant / pathology
  • Protein Kinase Inhibitors / therapeutic use
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-myc / genetics
  • Retinoblastoma Binding Proteins / genetics
  • SOX Transcription Factors
  • Tumor Microenvironment
  • Tumor Suppressor Protein p53 / genetics
  • Ubiquitin-Protein Ligases / genetics

Substances

  • Androgen Antagonists
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins c-myc
  • RB1 protein, human
  • Retinoblastoma Binding Proteins
  • SOX Transcription Factors
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Ubiquitin-Protein Ligases
  • EGFR protein, human
  • ErbB Receptors
  • Proto-Oncogene Proteins c-akt
  • PTEN Phosphohydrolase
  • PTEN protein, human