Delivery-corrected imaging of fluorescently-labeled glucose reveals distinct metabolic phenotypes in murine breast cancer

PLoS One. 2014 Dec 19;9(12):e115529. doi: 10.1371/journal.pone.0115529. eCollection 2014.

Abstract

When monitoring response to cancer therapy, it is important to differentiate changes in glucose tracer uptake caused by altered delivery versus a true metabolic shift. Here, we propose an optical imaging method to quantify glucose uptake and correct for in vivo delivery effects. Glucose uptake was measured using a fluorescent D-glucose derivative 2-(N-(7-Nitrobenz-2-oxa-1,3-diazol-4-yl)Amino)-2-deoxy-D-glucose (2-NBDG) in mice implanted with dorsal skin flap window chambers. Additionally, vascular oxygenation (SO2) was calculated using only endogenous hemoglobin contrast. Results showed that the delivery factor proposed for correction, "RD", reported on red blood cell velocity and injected 2-NBDG dose. Delivery-corrected 2-NBDG uptake (2-NBDG60/RD) inversely correlated with blood glucose in normal tissue, indicating sensitivity to glucose demand. We further applied our method in metastatic 4T1 and nonmetastatic 4T07 murine mammary adenocarcinomas. The ratio 2-NBDG60/RD was increased in 4T1 tumors relative to 4T07 tumors yet average SO2 was comparable, suggesting a shift toward a "Warburgian" (aerobic glycolysis) metabolism in the metastatic 4T1 line. In heterogeneous regions of both 4T1 and 4T07, 2-NBDG60/RD increased slightly but significantly as vascular oxygenation decreased, indicative of the Pasteur effect in both tumors. These data demonstrate the utility of delivery-corrected 2-NBDG and vascular oxygenation imaging for differentiating metabolic phenotypes in vivo.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • 4-Chloro-7-nitrobenzofurazan / administration & dosage
  • 4-Chloro-7-nitrobenzofurazan / analogs & derivatives*
  • 4-Chloro-7-nitrobenzofurazan / metabolism
  • Adenocarcinoma / blood supply
  • Adenocarcinoma / metabolism
  • Adenocarcinoma / pathology*
  • Animals
  • Blood Glucose / metabolism
  • Breast Neoplasms / blood supply
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology*
  • Cell Line, Tumor
  • Deoxyglucose / administration & dosage
  • Deoxyglucose / analogs & derivatives*
  • Deoxyglucose / metabolism
  • Female
  • Fluorescent Dyes / administration & dosage
  • Fluorescent Dyes / metabolism*
  • Mice
  • Neoplasm Metastasis
  • Neoplasm Transplantation
  • Optical Imaging / methods*
  • Oxygen Consumption

Substances

  • Blood Glucose
  • Fluorescent Dyes
  • Deoxyglucose
  • 4-Chloro-7-nitrobenzofurazan
  • 2-(N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)amino)-2-deoxyglucose

Grants and funding

This research was supported by generous funding from the National Science Foundation Graduate Research Fellowship Program (www.nsf.gov/grfp; AEF) and the Department of Defense Era of Hope Scholar Awards (http://cdmrp.army.mil/bcrp/era; W81XWH-09-1-0410; PI: N. Ramanujam and W81XWH-05-1-0363; PI: N. Ramanujam). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.