Intratumor lactate levels reflect HER2 addiction status in HER2-positive breast cancer

J Cell Physiol. 2019 Feb;234(2):1768-1779. doi: 10.1002/jcp.27049. Epub 2018 Aug 21.

Abstract

Despite different molecular tumor profiles indicate that human epidermal growth factor receptor 2 (HER2) messenger RNA (mRNA) levels mirror HER2 addiction and trastuzumab benefit in HER2-positive breast cancer (BC), the identification of noninvasive clinical predictors of trastuzumab sensitivity remains an unmet clinical need. In the current study, we investigated whether intratumor lactate levels reflect HER2 addiction and, in turn, trastuzumab susceptibility. Accordingly, the gene expression profiles of transgenic murine BC cell lines expressing the human d16HER2 variant (HER2-addicted) or human full-length HER2 (WTHER2; HER2-nonaddicted) revealed a significant enrichment of glycolysis-related gene pathways in HER2-addicted cells. We studied the metabolic content of 22 human HER2-positive BC by quantitative nuclear magnetic resonance spectroscopy and found that those cases with higher lactate levels were characterized by higher HER2 transcript levels. Moreover, gene expression analyses of HER2-positive BC samples from a TCGA data set revealed a significant enrichment in glycolysis-related pathways in high/HER2-addicted tumors. These data were confirmed by metabolic analyses of human HER2-positive BC cell lines with high or low HER2 transcript levels, which revealed significantly more active glycolytic metabolism in high HER2 transcript than in low HER2 transcript cells. Overall, our results provide evidence for noninvasive intratumor lactate detection as a potential metabolic biomarker of HER2 addiction and trastuzumab response suggesting the possibility to use in vivo imaging to assess lactate levels and, in turn, select HER2-positive BC patients who are more likely to benefit from anti-HER2 treatments.

Keywords: HER2; breast cancer; glycolysis; lactate; oncogene addiction.

Publication types

  • Multicenter Study
  • Observational Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents, Immunological / therapeutic use
  • Biomarkers, Tumor / antagonists & inhibitors
  • Biomarkers, Tumor / genetics*
  • Biomarkers, Tumor / metabolism*
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Chemotherapy, Adjuvant
  • Female
  • Gene Expression Regulation, Neoplastic
  • Glycolysis*
  • Humans
  • Italy
  • Lactic Acid / metabolism*
  • Lapatinib / pharmacology
  • Magnetic Resonance Spectroscopy
  • Mice
  • Oncogene Addiction*
  • Patient Selection
  • Precision Medicine
  • Protein Kinase Inhibitors / therapeutic use
  • Receptor, ErbB-2 / antagonists & inhibitors
  • Receptor, ErbB-2 / genetics*
  • Receptor, ErbB-2 / metabolism
  • Retrospective Studies
  • Trastuzumab / therapeutic use
  • Treatment Outcome
  • Up-Regulation

Substances

  • Antineoplastic Agents, Immunological
  • Biomarkers, Tumor
  • Protein Kinase Inhibitors
  • Lapatinib
  • Lactic Acid
  • ERBB2 protein, human
  • Receptor, ErbB-2
  • Trastuzumab