ASCL1 Restrains ERK1/2 to Promote Survival of a Subset of Neuroendocrine Lung Cancers

Mol Cancer Ther. 2024 Dec 3;23(12):1789-1800. doi: 10.1158/1535-7163.MCT-24-0355.

Abstract

The transcription factor achaete-scute complexhomolog 1 (ASCL1) is a lineage oncogene that is central in growth and survival of the majority of small cell lung cancers and neuroendocrine (NE) non-small cell lung cancers (NSCLC) that express it. Targeting ASCL1, or its downstream pathways, remains a challenge. Small cell lung cancers and NSCLC-NE that express ASCL1 exhibit relatively low ERK1/2 activity, in dramatic contrast to NSCLCs in which the ERK pathway plays a major role in pathogenesis. ERK1/2 inhibition in ASCL1-expressing lung tumor cells revealed downregulation of ERK1/2 pathway suppressors SPRY4, SPRED1, DUSP6, and the transcription factor ETV5, which regulates DUSP6. Chromatin immunoprecipitation sequencing demonstrated that these genes are bound by ASCL1. Availability of a pharmacologic inhibitor directed mechanistic studies toward DUSP6, an ERK1/2-selective phosphatase, in a subset of ASCL1-high NE lung tumors. Inhibition of DUSP6 increased active ERK1/2, which accumulated in the nucleus. Pharmacologic and genetic inhibition of DUSP6 reduced proliferation and survival of these cancers. Resistance developed in DUSP6-knockout cells, indicating a bypass mechanism. Although targeting ASCL1 remains a challenge, our findings suggest that expression of ASCL1, DUSP6, and low phospho-ERK1/2 identifies NE lung cancers for which DUSP6 may be a therapeutic target.

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors* / genetics
  • Basic Helix-Loop-Helix Transcription Factors* / metabolism
  • Cell Line, Tumor
  • Cell Proliferation
  • Cell Survival / drug effects
  • Dual Specificity Phosphatase 6 / genetics
  • Dual Specificity Phosphatase 6 / metabolism
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Lung Neoplasms* / drug therapy
  • Lung Neoplasms* / genetics
  • Lung Neoplasms* / metabolism
  • Lung Neoplasms* / pathology
  • MAP Kinase Signaling System
  • Mice
  • Mitogen-Activated Protein Kinase 1 / genetics
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / genetics
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Neuroendocrine Tumors / drug therapy
  • Neuroendocrine Tumors / genetics
  • Neuroendocrine Tumors / metabolism
  • Neuroendocrine Tumors / pathology

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • ASCL1 protein, human
  • Dual Specificity Phosphatase 6
  • DUSP6 protein, human
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinase 1