A novel MCT1 and MCT4 dual inhibitor reduces mitochondrial metabolism and inhibits tumour growth of feline oral squamous cell carcinoma

Vet Comp Oncol. 2020 Sep;18(3):324-341. doi: 10.1111/vco.12551. Epub 2019 Nov 19.

Abstract

Monocarboxylate transporters (MCTs) support tumour growth by regulating the transport of metabolites in the tumour microenvironment. High MCT1 or MCT4 expression is correlated with poor outcomes in human patients with head and neck squamous cell carcinoma (HNSCC). Recently, drugs targeting these transporters have been developed and may prove to be an effective treatment strategy for HNSCC. Feline oral squamous cell carcinoma (OSCC) is an aggressive and treatment-resistant malignancy resembling advanced or recurrent HNSCC. The goals of this study were to investigate the effects of a previously characterized dual MCT1 and MCT4 inhibitor, MD-1, in OSCC as a novel treatment approach for feline oral cancer. We also sought to determine the potential of feline OSCC as a large animal model for the further development of MCT inhibitors to treat human HNSCC. In vitro, MD-1 reduced the viability of feline OSCC and human HNSCC cell lines, altered glycolytic and mitochondrial metabolism and synergized with platinum-based chemotherapies. While MD-1 treatment increased lactate concentrations in an HNSCC cell line, the inhibitor failed to alter lactate levels in feline OSCC cells, suggesting an MCT-independent activity. In vivo, MD-1 significantly inhibited tumour growth in a subcutaneous xenograft model and prolonged overall survival in an orthotopic model of feline OSCC. Our results show that MD-1 may be an effective therapy for the treatment of feline oral cancer. Our findings also support the further investigation of feline OSCC as a large animal model to inform the development of MCT inhibitors and future clinical studies in human HNSCC.

Keywords: Feline oral squamous cell carcinoma; Head and neck cancer; MCT1; MCT4; metabolic coupling; metabolism.

MeSH terms

  • Amino Acid Transport Systems, Neutral / genetics
  • Amino Acid Transport Systems, Neutral / pharmacology
  • Animals
  • Cat Diseases / drug therapy*
  • Cats
  • Cell Line, Tumor
  • Humans
  • Mitochondria / drug effects
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / pharmacology*
  • Monocarboxylic Acid Transporters / genetics
  • Monocarboxylic Acid Transporters / pharmacology*
  • Mouth Neoplasms / drug therapy
  • Mouth Neoplasms / veterinary*
  • Muscle Proteins / genetics
  • Muscle Proteins / pharmacology
  • Sequence Analysis, RNA
  • Squamous Cell Carcinoma of Head and Neck / drug therapy
  • Squamous Cell Carcinoma of Head and Neck / veterinary*

Substances

  • Amino Acid Transport Systems, Neutral
  • Mitochondrial Proteins
  • Monocarboxylic Acid Transporters
  • Muscle Proteins
  • SLC16A10 protein, human
  • SLC16A4 protein, human