Four and a half LIM domains 2 (FHL2) attenuates tumorigenesis of gastrointestinal stromal tumors (GISTs) by negatively regulating KIT signaling

Mol Carcinog. 2024 Jul;63(7):1334-1348. doi: 10.1002/mc.23727. Epub 2024 Apr 17.

Abstract

Gastrointestinal stromal tumors (GISTs) are predominately induced by KIT mutants. In this study, we found that four and a half LIM domains 2 (FHL2) was highly expressed in GISTs and KIT signaling dramatically increased FHL2 transcription while FHL2 inhibited KIT transcription. In addition, our results showed that FHL2 associated with KIT and increased the ubiquitination of both wild-type KIT and primary KIT mutants in GISTs, leading to decreased expression and activation of KIT although primary KIT mutants were less inhibited by FHL2 than wild-type KIT. In the animal experiments, loss of FHL2 expression in mice carrying germline KIT/V558A mutation which can develop GISTs resulted in increased tumor growth, but increased sensitivity of GISTs to imatinib treatment which is used as the first-line targeted therapy of GISTs, suggesting that FHL2 plays a role in the response of GISTs to KIT inhibitor. Unlike wild-type KIT and primary KIT mutants, we further found that FHL2 didn't alter the expression and activation of drug-resistant secondary KIT mutants. Taken together, our results indicated that FHL2 acts as the negative feedback of KIT signaling in GISTs while primary KIT mutants are less sensitive and secondary KIT mutants are resistant to the inhibition of FHL2.

Keywords: FHL2; GIST; KIT; imatinib; mutation.

MeSH terms

  • Animals
  • Carcinogenesis / genetics
  • Cell Line, Tumor
  • Gastrointestinal Neoplasms / genetics
  • Gastrointestinal Neoplasms / metabolism
  • Gastrointestinal Neoplasms / pathology
  • Gastrointestinal Stromal Tumors* / genetics
  • Gastrointestinal Stromal Tumors* / metabolism
  • Gastrointestinal Stromal Tumors* / pathology
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Imatinib Mesylate / pharmacology
  • LIM-Homeodomain Proteins* / genetics
  • LIM-Homeodomain Proteins* / metabolism
  • Mice
  • Muscle Proteins* / genetics
  • Muscle Proteins* / metabolism
  • Mutation
  • Proto-Oncogene Proteins c-kit* / genetics
  • Proto-Oncogene Proteins c-kit* / metabolism
  • Signal Transduction*
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism
  • Ubiquitination

Substances

  • Proto-Oncogene Proteins c-kit
  • LIM-Homeodomain Proteins
  • Muscle Proteins
  • Transcription Factors
  • FHL2 protein, human
  • Imatinib Mesylate
  • KIT protein, human