Andrew D James1,2, Theresa K Leslie1,2, Marie-Christine BD Labarthe3, Michaela Nelson1, Frank Riemer4, Gabrielle Baxter5, Joshua D Kaggie5, Fiona J Gilbert5, William Brackenbury1,2, and Aneurin J Kennerley2,3
1Biology, University of York, York, United Kingdom, 2York Biomedical Research Institute, University of York, York, United Kingdom, 3Chemistry, University of York, York, United Kingdom, 4MMIV, Haukeland University Hospital, Bergen, Norway, 5Department of Radiology, University of Cambridge, Cambridge, United Kingdom
Synopsis
Here we applied 23Na MRI, as part of a
multiparametric imaging approach to measure ionic sodium concentration ([Na+])
levels in a longitudinal in-vivo mouse model of breast cancer. We investigated tumour
[Na+] in response to neoadjuvant chemotherapy and ion channel
inhibitors as a novel therapeutic means of reducing metastasis. Results show
that [Na+] is decreased in tumour-bearing mice receiving standard
chemotherapy. Data suggest that elevated tumour [Na+] in
breast cancer may represent a potential imaging biomarker for malignancy and
response to chemotherapy.
Introduction
In the
present study we use preclinical 23Na MRI to measure ionic sodium
concentration ([Na+]) levels in a longitudinal in-vivo mouse model
to probe the efficacy of novel treatments targeting the tumour ionic microenviroment.
Clinical intervention in early stage breast cancer is associated with a
high survival rate, with late stage metastatic disease associated with poor
prognosis. While recent progress has been made in understanding the role of the
tumour microenvironment in breast cancer progression, little is known about how
the ionic composition of tumours influences progression, metastasis and therapy
response. Evidence indicates that tumour [Na+] is elevated in
malignant breast tumours compared to surrounding tissue1,2, and this
elevation is reduced following neoadjuvant chemotherapy3. Thus
elevated tumour [Na+] represents an imaging biomarker for breast
cancer lesions and therapy response, and the targeting of Na+
conductance routes through ion channels provides a novel therapeutic means of reducing
metastasis.Methods
Tumour 23Na
content was assessed in a xenograft longitudinal mouse model (female Rag2−/−/Il2rg −/−) of
breast cancer (MDA-MB-231 cells). Following surgery (day 0), mice were split
into 3 groups receiving: standard chemotherapy (docetaxel, 10 mg/kg i.p once
weekly, n=7); a 23Na ion channel inhibitor (eslicarbazepine acetate, 200 mg/kg daily oral gavage, n=7); and vehicle control (n=14). 23Na MRI measurements
were made at 7T in a pre-clinical MRI facility (Bruker BioSpec, 310mm bore)
utilizing a quadrature 1H volume coil and a bespoke single channel 23Na
surface coil. Subjects were scanned at the day 7, 14, and 21 time points. Mice
were anaesthetised with 1-2% isoflurane mixed with 100% O2. Breathing
rate was monitored throughout and body temperature maintained using a
circulating warm water bath. At each time point we performed standard 1H high
resolution (256*256, 40mm fov) T2, T2* structural and EPI-diffusion (single slice
96*64 matrix, 40mm fov, 3 gradient directions, 5 b-values 100-25000 s/mm2)
imaging. 23Na imaging (figure 1a) used a single slice centric
encoded FLASH based approach (32*32 matrix, 40mm fov, TR 50ms, TE 1.5ms, 400
average, and slice thickness 5mm). Data
were compared to post-mortem electrophysiological slice recordings to better
understand the underlying biological mechanisms.Results
Using 23Na MRI, we have established
that tumour [Na+] is decreased in tumour-bearing mice receiving
standard chemotherapy (docetaxel, 10 mg/kg i.p once weekly) after two cycles of
treatment compared with untreated vehicle control (figure 1b). This standard
chemotherapy inhibited tumour growth rate. Whether inhibited growth is a driver
or a consequence to decreased tumour [Na+] compared with untreated
tumours remains under investigation. Measurements of Na+ currents using the whole
cell patch clamp method revealed no difference in Na+ conductance through
voltage gated sodium channels between groups, suggesting that
an alternative mechanism is responsible for the observed differences in
tumour [Na+]. The antiepileptic medication eslicarbazepine
acetate (a specific voltage gate sodium channel blocker, 200 mg/kg p.o. daily) had no effect on tumour
growth, tumour [Na+], or tumour slice Na+ conductance.Conclusion & Discussion
We present data describing [Na+]
measurement in cancer cells using 23Na MRI and complementary assessment of
tumour cellularity via diffusion-weighted imaging and our preliminary findings assessing
the effects of Na+ conductance route inhibitors on tumour [Na+]
using the above approaches. Our results suggest
that elevated tumour [Na+] in breast cancer may represent a
potential imaging biomarker for malignancy and response to chemotherapy.
Moreover, targeting of elevated tumour [Na+] should be investigated
as a potential treatment avenue. Data will be used to
help inform clinical translation of this technology.Acknowledgements
This project was funded by the CRUK (Project # A25922) and Breast Cancer Now (2015NovPhD572):
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