In vivo fluorescent imaging of tumor bombesin and transferrin receptor expression as early indicators of sorafenib efficacy in small animal models

In vivo fluorescent imaging of tumor bombesin and
transferrin receptor expression as early indicators of
sorafenib efficacy in small animal models
Jen-Chieh Tseng and Jeffrey D. Peterson. Life Sciences and Technology,
PerkinElmer Inc., Hopkinton, MA
Metabolic tumor imaging of the sorafenib dose response
2 using fluorescent imaging agents
1
HCT116/luc tumor is responsive to sorafenib
treatment by BLI and tumor volume assessment
A. Bioluminescence imaging of tumor viability
A.
Fluorescence molecular tomographic (FMT) imaging of tumor metabolic
changes in response to sorafenib treatment
Day 2 BombesinRSense 680
n=5
n=5
#
#
#
To more accurately assess the impact of treatment between day 1 and day 3,
taking into account modest increases in tumor size, the quantitative BLI and FLI
results were normalized to tumor volume. A. Tumor volume during the first three
days of treatments. B. BLI signals normalized against tumor volume data. C.
BR680 epi-FLI signals normalized against tumor volume data (t-test, n = 5, bar:
s.e.m.). D. TfV750 epi-FLI signal normalized against tumor volume (t-test, n = 5,
bar: s.e.m.). *p < 0.01.
B. Longitudinal Imaging
#
*
**
**
**
BombesinRSense 680 (BR680) and Transferrin-Vivo 750 (TfV750) detect early tumor
metabolic changes in response to sorafenib treatment. A. PerkinElmer’s FMT® 4000
fluorescence molecular tomography imaging system was used to detect BR680 or
TfV750 uptake in the HCT116-luc tumors treated with different doses of sorafenib
(t-test, bar: s.e.m.). B. FMT imaging of BR680 and TfV750 tumor signals in
subcutaneous HCT116-luc tumors treated with vehicle or 120 mg/kg sorafenib daily
(t-test, bar: s.e.m.). Graphs represent longitudinal metabolic changes in HCT116luc tumors in response to the treatment. #p < 0.05; *p < 0.01; **p < 0.001.
FLI,
but
not
BLI,
detects
early
tumor
metabolic
3
changes from moderate dose sorafenib treatment
Day 2
Day 9
Day 1
Vehicle
Day 2
Sorafenib 40 mg/kg
Radiance (109)
0.5
6.0
0.5
3.0
2.0
1.0
7.0
C. Early detection of dosedependent responses
5.0
3.0
#
**
1.0
Radiant Efficiency (108)
C. Transferrin-Vivo 750 imaging
***
***
***
***
ns
#
*
D. Histology validation
Sorafenib
*
H&E
TfV750 Epi-FLI
50 mm
There are several tumor biological changes during disease progression and in
response to targeted anti-cancer drug. Without treatment, the cancer cells actively
divide and increase its metabolic activity and tumor volume. Active cancer cell
proliferation also triggers new vasculature formation in tumor (angiogenesis) that is
critical for tumor growth. On the other hand, treatment with sorafenib suppresses
metabolic activities, inhibits angiogenesis, and triggers inflammatory responses and
recruitment of granulocytes and macrophages. These changes can occur prior to
overt death or regression of the tumor.
Summary
D. Quantification
A. Longitudinal bioluminescence imaging (BLI) of HCT116-luc tumors in response to
daily treatments of 120, 80 or 40 mg/kg sorafenib using the IVIS® Spectrum CT
preclinical optical imaging system. Oral gavage treatments were given daily on day
0-4 and day 7-11. B. Relative tumor BLI signals and tumor volumes of each
treatment group were calculated using the day 0 signals as 100% (p-value
calculated by two-way ANOVA, bar: s.e.m.). C. Relative BLI signals of each dose
group on day 2 (t-test, bar: s.e.m.); relative tumor volumes on day 2 (one-way
ANOVA, bar: s.e.m.). D. H&E staining of tumor tissue sections harvested from the
vehicle and sorafenib-treated (120 mg/kg) tumors on day 10. The drug effectively
induced necrosis and regression in tumors. Bar: 50 mm. #p < 0.05; **p < 0.001;
***p < 0.0001.
Late
B. BombesinRSense 680 imaging
4.0
Vehicle
Early
2.0
5.0
B. Sorafenib suppresses
tumor growth
No Treatment
Day 9
1.0
1.0
Sorafenib
Treatment
A. Luciferase BLI imaging
1.5
1.5
Model
for
concepts
in
molecular
imaging
of
5
metabolism in cancer
Tumor Biology Changes in Progression and Treatment
Day 1
3.0
Day 2 Transferrin-Vivo 750
Radiance (109)
Targeted cancer therapy aims to block key signaling pathways that are
critical for tumor cell growth and survival. The blockage eventually
results in cell death via apoptosis and eventual tumor growth
suppression. This strategy has proven to be quite effective, and the
FDA has approved several targeted therapeutics in the past decade.
Encouraged by the success in clinical development, many academic and
pharmaceutical researchers are in active pursuit of improved next
generation targeted anti-cancer drugs. As a result, many new chemical
and biological entities are emerging from initial screening of in vitro, in
vitro and/or in silico selection processes. From the perspective of drug
development, it poses a great challenge for the next stage of in vivo
validation and demands a robust, accurate, and efficient method for
assessment of these candidates in living animal models.
Cancer cells are known to have abnormally increased cellular
metabolism, and in the early stages of effective drug treatment, cancer
cells show decreased metabolism and proliferation. These events occur
prior to overt signs of cell destruction, and often multiple days or weeks
of treatment are required to see overt changes in tumor size. In some
instances, bioluminescence imaging can be used to detect early
changes in tumor viability in response to targeted therapy when using
luciferase-expressing tumor cell lines, however, with many therapeutic
treatments these early changes in tumor viability cannot be seen by
bioluminescence imaging. To assess whether molecular imaging of
biomarkers related to tumor metabolic state would be useful in early
detection of treatment efficacy, the utility of non-invasive near infrared
(NIR) fluorescence imaging, using NIR fluorescent imaging agents, was
assessed. Highly metabolic cancer cells have accompanying elevations
in receptors for bombesin and transferrin on their surface that can be
readily imaged using targeted fluorescent agents (BombesinRSenseTM
680 [BR680] and Transferrin-VivoTM 750 [TfV750]; PerkinElmer Inc.).
In this report, we demonstrate the synergistic use of fluorescence (FLI)
and bioluminescence imaging (BLI) to profile tumor metabolism and
viability, respectively, in response to a targeted anti-cancer drug,
sorafenib. Sorafenib is a clinically approved tyrosine kinase inhibitor
that effectively blocks VEGFR, PDGFR and Raf signaling in cancer. At
Sorafenib doses ranging from 40-120 mg/kg, there was a dosedependent decrease in viability of HCT116-luc human colon xenograft
tumors evident as early as 2 days at the higher doses but only after
several days for low doses. Interestingly, even at a lower dose of 40
mg/kg, both BR680 and TfV750 signal reduction can still be observed
as early as 48 hours, a time/dose in which no significant reduction of
tumor viability or size was observed.
These results suggest the potential use of metabolic fluorescent
imaging agents as sensitive and efficient and early biomarkers for preclinical assessment of targeted cancer drugs.
Radiant Efficiency (108)
Abstract
4 Quantification of the early therapeutic response to
40 mg/kg sorafenib with tumor size normalization
**
Vehicle
40 mg/kg
**
BLI and FLI monitoring of tumor changes in response to a moderate dose of
sorafenib. A. BLI imaging of tumors in animals treated with vehicle or 40 mg/kg
sorafenib (bar: s.e.m.) using PerkinElmer’s IVIS Spectrum CT imaging system. B.
Epi-fluorescence imaging (epi-FLI) of BR680 uptake in tumors showing images and
quantification (t-test, bar: s.e.m.). C. Epi-FLI of TfV750 uptake in tumors showing
images and quantification (t-test, bar: s.e.m.). #p < 0.05; **p < 0.001; ***p <
0.0001; ns = not significant.
In these studies, we demonstrated that bioluminescence and fluorescence imaging
can work synergistically in order to obtain a comprehensive picture of tumor
viability and metabolic status. PerkinElmer’s IVIS imaging systems have been
widely adopted for pre-clinical imaging of bioluminescent tumor xenografts that
stably express firefly luciferase. Since firefly luciferase is only expressed in tumor
cells but not present in any normal tissues, bioluminescence imaging (BLI) shows
high sensitivity, broad dynamic range and excellent specificity. More importantly,
the need of ATP for luciferase-mediated light production can make BLI a useful
indicator for assessing tumor viability in response to different anti-cancer
treatments, especially when conventional tumor volume measurement fails to
indicate any difference. In this report, we used BLI imaging to perform a dosetitration study and identified the minimal effective dosage of sorafenib that
suppresses but does not reduce tumor burden or viability (assessed by BLI).
Statistically significant changes were seen on day 2 post-treatment with 80-120
mg/kg sorafenib treatment, with 40 mg/kg showing little or no effect on tumor
burden at this time point.
For visualizing early metabolic changes in tumors, we used non-invasive near
infrared (NIR) fluorescence imaging agents to monitor tumor’s metabolic responses
to a targeted therapeutics. Due to the spectral wavelength in the NIR, and the
accompanying low tissue absorbance, NIR fluorescent imaging generall shows
enhanced deep tissue penetration. Bombesin- and transferrin-targeted (BRS680 and
TfV750, respectively) imaging agents, showed the ability to detect day 2 sorafenib
efficacy at a dose of 40 mg/kg, lower than needed for BLI detection. BR680 signal
reduction can still be observed early within 48 hours, but no significant reduction of
tumor size or BLI signal was observed until a week later. In addition to metabolic
imaging, PerkinElmer provides a variety of NIR fluorescent imaging agents for
multiplex imaging of biophysiological changes in tumor. We believe the collaborative
use of both imaging methods is of significant benefit for pre-clinical anti-cancer drug
development.
PerkinElmer, Inc., 68 Elm Street, Hopkinton, MA USA (800) 762-4000 or
(+1) 203 925-4602 www.perkinelmer.com