Study of radiotherapy resistance associated to

Study of radiotherapy resistance associated to
EGFR/MAPK signaling pathway and its application in
the rational design of a treatment with
simvastatin in combination with cetuximab and
radiotherapy (in experimental models of carcinoma)
Lara Isabel de Llobet Cucalón
Aquesta tesi doctoral està subjecta a la llicència Reconeixement 3.0. Espanya de Creative
Commons.
Esta tesis doctoral está sujeta a la licencia Reconocimiento 3.0.
Commons.
España de Creative
This doctoral thesis is licensed under the Creative Commons Attribution 3.0. Spain License.
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Clin Transl Oncol (2013) 15:189–197
DOI 10.1007/s12094-012-0898-8
RESEARCH ARTICLE
Development and characterization of an isogenic cell line
with a radioresistant phenotype
Lara I. de Llobet • Marta Baro • Agnès Figueras •
Ignasi Modolell • Maria V. Da Silva • Purificación Muñoz
Arturo Navarro • Ricard Mesia • Josep Balart
•
Received: 25 January 2012 / Accepted: 22 May 2012 / Published online: 24 July 2012
Ó Federación de Sociedades Españolas de Oncologı́a (FESEO) 2012
Abstract
Introduction Radiation resistance is a major cause of
death in cancer patients. Cancer cells react during radiotherapy by re-programming specific cell functions that may
confer resistance to radiation. The understanding of this
complex process is hindered due to the lack of appropriate
study models. We describe an experimental development of
a radioresistant isogenic cancer cell line, and its molecular
characterization.
L. I. de Llobet M. Baro A. Figueras J. Balart (&)
Translational Research Laboratory, Catalan Institute
of Oncology – IDIBELL, Avda Gran Via de l’Hospitalet,
199-203, 08907 L’Hospitalet de Llobregat, Spain
e-mail: [email protected]; [email protected]
I. Modolell
Department of Radiophysics and Radioprotection,
Catalan Institute of Oncology – IDIBELL,
L’Hospitalet de Llobregat, Spain
M. V. Da Silva P. Muñoz
Cancer Biology and Epigenetics Laboratory,
IDIBELL, L’Hospitalet de Llobregat, Spain
A. Navarro
Department of Radiation Oncology,
Catalan Institute of Oncology – IDIBELL,
L’Hospitalet de Llobregat, Spain
Materials and methods A431-cultured cells were irradiated for 7 month until 85 Gy. Then, a selected single cell
was left to grow as stable A431-R cell line. Clonogenic
assay was used to determine cell survival, the a and b
parameters of the LQ model, and the mean inactivation
dose. The DNA repair ability of cells was evaluated by
pulsed-field electrophoresis method. Differential effect of
fractionated radiation was ultimately tested in xenografts.
Furthermore, we used a wound healing assay, Western blot
for EGFR, AKT and ERK1/2 and ELISA test for vascular
endothelial growth factor (VEGF) secretion. Finally we
explored CD44 marker and cell cycle distribution.
Results The established A431-R cell line showed radiation resistance in clonogenic assays, repair of radiationinduced DNA fragmentation and xenografted tumours. The
radiation resistance was associated with in vitro higher cell
growth and migration, increased levels of former oncoproteins, and secretion of VEGF.
Conclusions In this model, the emergence of radiation
resistance was associated with the acquisition of biological
traits that support more aggressive behaviour of cancer
cells. We have generated a model that will be useful for
mechanistic studies and development of rational treatments
against radiation resistance in cancer.
Keywords Development of isogenic cell line model Emergence of radiation resistance Aggressive phenotype
R. Mesia
Department of Medical Oncology,
Catalan Institute of Oncology – IDIBELL,
L’Hospitalet de Llobregat, Spain
Introduction
Present Address:
J. Balart
Department of Radiation Oncology,
Hospital de la Santa Creu i Sant Pau,
C/Sant Antoni Ma Claret, 167, 08025 Barcelona, Spain
In the modern era of radiation oncology, curative potential of
radiotherapy has significantly increased due to new techniques in imaging diagnosis and radiation delivery. However, locoregional relapses post-radiotherapy treatments are
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still a major cause of death in cancer patients. One explanation for local recurrences is the acquisition by a small
proportion of cancer cells of a radioresistant pattern [1–6].
Furthermore, the cells exposed to ionizing radiation may
develop adaptive molecular mechanisms to become resistant
to radiotherapy [7, 8]. The primary resistance and the
acquisition of effective mechanisms of resistance, together
with the biological pressure of genotoxic effects of radiation,
push irradiated cells through a selective process in which the
most resistant genotypes will be selected in a Darwinian
manner. In the end, it may enable specific genetic, as well as
epigenetic programs that will confer cytoprotective properties in the cells that survive. Several observations suggest
that tumour adaptation to radiotherapy induces the emergence of radiation resistance and higher malignant phenotypes that can ultimately determine the clinical outcome of
recurrences after radiotherapy [9–11].
The study of the mechanisms involved in the acquisition
of an aggressive resistant phenotype is complex. In part,
the difficulties are due to the lack of appropriate models in
which the emergence of resistance can be directly attributed to specific changes that happen during radiotherapy. In
the present report, we describe the process of generating an
isogenic cancer cell line that has a decreased response to
radiotherapy. Furthermore, relevant novel properties of the
biology of this resistant cell line are discussed.
Clin Transl Oncol (2013) 15:189–197
Estimation of radiosensitivity and LQ model
To determine the radiation sensitivity of the cells, clonogenic assays were performed. Briefly, cells were planted in
60-mm dishes 24 h before receiving irradiation in single
doses of 0, 2, 4, 6 or 8 Gy. Cells were allowed to proliferate for 14 days and then stained with crystal violet. The
respective surviving fractions (SF) were calculated as the
ratio between the number of colonies following irradiation
and the number of cells plated, which were then normalized by the clonogenic efficiency of non-irradiated cells.
To estimate the a and b parameters of the LQ model, we
used the least square regression method of the function
Y = -(aD ? bD2) from the natural logarithm of surviving
fractions. We evaluated differential radiosensitivity by
means of the surviving fraction after 2 Gy (SF2), LQ
model, and mean inactivation dose (D) between 0 and 8 Gy
as described by Tucker [12].
Pulsed-field gel electrophoresis
Cell cultures were irradiated with 45 Gy, and then cells were
mixed with 1 % agarose at 0, 1, 2, 4, 8 or 24 h after irradiation to form cell plugs. Cell plugs were lysed and loaded
into a gel to determine residual—post-repair—radiationinduced DNA fragments using pulsed-field electrophoresis
method (PFGE), as we described previously [13].
Materials and methods
Tumour xenografts
Cancer cell lines
To generate tumour xenografts, 106 A431-WT or 106 A431R cells suspended in 100 lL of medium were injected into
subcutaneous tissues on the right thigh of athymic mice.
Previously, cultures were trypsinized, cells counted and
properly diluted in growth medium for injection and kept on
ice. Tumour growth was measured twice weekly until
tumours reached 1,500 mm3 in size. Tumour size was calculated using the formula: p/6 9 (large diameter) 9 (small
diameter)2. Animal models used in this study were
approved by the institutional animal care and ethics committee and in accordance with its guidelines. Six- to eightweek-old female athymic Swiss nu/nu mice were purchased
from Harlan (Gannat, France) and were housed under
pathogen-free conditions at our facilities (AAALAC
accreditation number 1,155).
The human epidermoid carcinoma cell line A431 from the
American Type Cell Collection (LGC Promochem, Barcelona, Spain) was used in this study. Cells were maintained
as a monolayer under standard cell culture conditions. We
denominated them as A431-WT cells in our study. Cells
growing in 100-mm plastic dishes were irradiated at room
temperature (RT) using 6-MV X-rays at dose rate of
2.7 Gy/min. Cultures were progressively treated with daily
rounds of radiation over a 7-month period of time, starting
with 0.75 Gy/fraction and ending with 3 Gy/fraction. Irradiation was stopped, as necessary, in order to allow for cell
monolayer recovery. The procedure was continued until a
total of 85 Gy had been delivered. Next, single cell suspension (1,000 cells per 60-mm dishes) were plated and
allowed to grow as macroscopic colonies. We next grew the
cells from the colony that showed the most vigorous growth
to the confluence and expanded them while the remainder of
the cells was not further characterized. These selected cells
were used for the present study and were denominated as
A431-R and were compared to the parental A431-WT from
which they were derived.
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Irradiation of xenoimplanted tumours
To irradiate the tumours (n = 5 for A431-WT and 5 for
A431-R), we used a 6-MV photon beam from a Varian
Clinac 2100 linear accelerator delivering 10 fractions of
3 Gy each in 2 weeks, starting on Monday and ending on
Friday. This dose of 30 Gy was delivered at 2.7 Gy/min at
Clin Transl Oncol (2013) 15:189–197
the isocenter of the beam. Appropriated bolus was provided
for electronic equilibrium at the entrance and the exit of
beam. Radiotherapy was limited to the right thigh. In vivo
dosimetry was performed by means of radiochromic films
which showed less than 3 % variation in the prescribed
dose. Prior to tumour irradiation, the mice were anaesthetized by an intraperitoneal injection (1 mL/kg of each
solution: 50 mg/mL ketamine and 1 mg/mL medetomidine). Upon completion, 5 mg/mL atipamezole was delivered to reverse the effects of the anaesthesia [14]. A
complete mock process was performed on non-irradiated
mice that served as experimental controls (n = 5 for A431WT and 5 for A431-R).
Wound healing assay
A431-WT and A431-R cells were seeded in 6 cm diameter
plates and cultured until confluent. After 12 h of culture in
foetal bovine serum (FBS)-free medium, the petri dishes
were scratched with a 200 lL pipette tip to imitate a
wound. After several washing and removal of floating cells,
the distances between cell margins were measured at 0, 1,
2, 3, 6 and 24 h using specialized software (Leica, Wetzar,
Germany). Three independent assays, done in duplicate,
were conducted.
Immunoblotting
We performed a standard Western blot method to determine
levels of specific proteins. Cultures were maintained without
FBS for 24 h before treatment with radiation or epidermal
growth factor (EGF) ligand (Sigma-Aldrich, St. Louis, MO,
USA). Following treatment, equal amounts of protein
(30 lg) were separated by SDS-PAGE and blotted onto
nitrocellulose membranes, which were incubated with a
rabbit anti-phosphorylated (Tyr992) EGFR antibody (EGFR
pY992) (Sigma-Aldrich) at a 1:1,000 dilution; mouse antiphosphorylated (Thr183 and Tyr185) MAP kinase ERK1/2
monoclonal antibody (pERK1/2) (Sigma-Aldrich) at a
1:5,000 dilution, and a rabbit anti-phosphorylated (Ser473)
AKT polyclonal antibody (Cell Signaling, Danvers, MA,
USA) at a 1:500 dilution in blocking solution overnight at
4 °C, as previously described [11]. Optical densitometry
quantification of the Western blot protein levels was performed using Quantity One Software (Bio-Rad Laboratories, Hercules, CA, USA), then the results were represented
on a histogram.
Levels of VEGF secretion
To measure the levels of vascular endothelial growth factor
(VEGF) secretion, cells were plated in 6-mm dishes
(1 9 106 cells per dish) and allowed to grow in a complete
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medium for 24 h. Next, cultures were rinsed twice with
PBS buffer and incubated in FBS-free medium for 24 h.
The cells were then irradiated with a single 8 Gy dose.
Supernatants were collected at 0, 24 and 48 h. VEGF was
determined in the supernatants by means of an enzymelinked immunoabsorbent assay ELISA (R&D Systems Inc,
Minneapolis, MN, USA) as described by Pueyo et al. [11].
CD44 determination
The cell surface marker, CD44, was determined by a standard IF process. Sterilized cover slips were put into 60-mm
petri dishes, and then A431-WT or A431-R cells were
seeded and cultured in full medium. After 48 h, the cells
were fixed with 4 % neutral buffered formaldehyde, washed
(0.1 % triton in PBS for 10 min) and incubated for 1 h with
a protein-blocking solution (20 % serum goat and 20 %
serum horse in 1X PBS). Next, the slides were incubated
with a mouse anti-CD44 (156-3C11) monoclonal antibody
(Cell Signaling) at 1:100 dilution overnight at 4 °C. To
detect primary antibody, cover slips were incubated with
Alexa Fluor 488-conjugated goat anti-mouse secondary
antibody (Invitrogen, Carlsbad, CA, USA) at a 1:1,000
dilution for 1 h at RT. Counterstaining and fluorescence
images were produced using a previously described method
[13]. Additionally, CD44 detection was measured by flow
cytometry using anti CD44-APC (1:12.5; BD Biosciences
Pharmingen, San Diego, CA, USA) antibody in 100 lL
PBS 0.5 % BSA and 2 mM EDTA. After incubation for
30 min at 4 °C, cells were washed with 0.5 % BSA 2 mM
EDTA, and then the cells were re-suspended in 300 lL
PBS, 2 % FBS and 2 mM EDTA. Flow cytometry quantification of CD44 positive cells was performed with a BD
FACSaria III cell sorter and BD FACSDiva software (BD
Biosciences Pharmingen).
Cell cycle analysis
A standard iodine propidium staining method was used to
assess the cell cycle phase distribution of A431-WT and
A431-R cells. Flow cytometry analysis was performed with
a BD FACSCalibur cell sorter, and BD Cellquest Pro plus
(BD Biosciences Pharmingen) and ModFit LT3.2 (Verity
Software House, Topsham, ME, USA) softwares.
Statistics
Results were expressed as mean ± standard error (SE).
Statistically significant differences in-between-group
comparisons were defined using a two-tailed significance
level of p \ 0.05. The Statistical Package for Social Sciences, version 13.0 (IBM, Madrid, Spain) was used for data
analysis.
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Results
Fractionated irradiation and clonal selection induced
radiation resistance in the A431 cell line
Radiosensitivity was significantly decreased in the new
A431-R cell line. The initial shape of survival curve for
A431-R cells showed a higher shoulder than parental
A431-WT cells (Fig. 1a), and the mean SF2 value rose
from 0.62 to 0.75 (p = 0.024). The potential effect of
successive fractions of 2 Gy is illustrated in Fig. 1a, where
the effect of a single dose of 2 Gy is repeated 4 times,
assuming that no additional repair took place between
fractions in either type of cells. To further evaluate variations in radiosensitivity, the a/b ratio of LQ model and the
mean inactivation dose were calculated from the surviving
fractions after single doses of 0, 2, 4, 6 or 8 Gy. The a/b
ratio was reduced from 12 Gy for parental cells to 4.6 Gy for
the resistant cells, at the expense of decreasing a-component
and increasing b-component, indicating a higher ability to
repair sub-lethal damage in the A431-R cells, and thus,
having increased resistance to radiotherapy (Fig. 1b). The
mean inactivation dose was also increased from 3 to 3.5 Gy
in A431 cells.
In light of these results, and, because DNA repair is a
crucial determinant of radiosensitivity, we decided to
determine whether A431-R cells acquired an increased
ability to repair DNA. In A431-R cells, we found a
significant diminution of residual DNA fragments, measured by PFGE, indicating that in these cells the rejoining of radiation-induced DNA fragments was more
efficient than A431-WT cells (Fig. 2). This functional
finding provides further support to radiation resistance in
A431-R cells.
Fig. 1 The radiosensitivity of
A431-R cells was lower than
A431-WT. a Representation of
cell response to radiation after
four separated doses of 2 Gy
each for A431-WT cells
(circles) and A431-R cells
(squares). b Radiosensitivity of
A431-WT versus A431-R cell
lines. Values indicate the mean
of nine experiments done in
triplicate, and bars show the
standard error (*p \ 0.05;
Mann–Whitney test)
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Clin Transl Oncol (2013) 15:189–197
Finally, to validate the in vitro findings and definitively
establish relative radiation resistance in A431-R cells, we
evaluated the effect of fractionated radiotherapy on the
growth of xenografted tumours. Seven days after cell
injection all animals exhibited tumour growth in the subcutaneous tissues of the right thigh. The average tumour
size (n = 20) was of 51.30 ± 8.8 (in mm3) for A431-WT
cells and 30.73 ± 7.4 for A431-R cells (p = 0.11). At this
point in time—just before radiotherapy—no significant
differences were found in the size of tumours irrespectively
of the treatment (non-irradiated vs. irradiated) or origin of
the cells (parental vs. resistant).
Without irradiation, tumours exponentially grew as a
function of time showing a similar pattern for both types of
cells. At day 21, the parental tumours measured 1,120 ±
151.4 and those from resistant cells 1,092 ± 250.5. In
contrast, the size of the tumours that received radiation was
significantly decreased to 226.4 ± 43.6 and to 401.6 ±
53.4, respectively. This observation indicates that tumour
growth was inhibited by radiation in both types of cells.
Importantly, at the ending of radiotherapy the size of
resistant tumours was 1.8 (401.6/226.4) times larger than
that of tumours from parental cells. This difference was
maintained or increased during the follow-up, which was
calculated to show statistical significance (Fig. 3). Greater
growth delay and slower re-growth were observed in the
parental tumours compared to tumours derived from
resistant cells, although the differences in these cases did
not reach a p value below 0.05 (see Fig. 3 for explanations). These results indicate that tumours derived from
A431-R cells were less affected by radiation, allowing the
cells to proliferate, and together with the earlier in vitro
findings, there is a strong suggestion that these cells are
effectively radiation resistant.
Clin Transl Oncol (2013) 15:189–197
193
Fig. 2 The ability of rejoining radiation-induced DNA fragments was
higher in A431-R cells. a Representative pictures from PFGE
showing different degrees of DNA breakage as smears of variable
intensity. To permit DNA repair, cells were cultured as adherent
monolayer for 0, 1, 2, 4, 8 or 24 h after irradiation (45 Gy).
b Rejoining was normalized to untreated cells. A431-WT cells
(circles) versus A431-R cells (squares). AU stands for arbitrary units.
Values indicate the mean of three independent experiments and bars
show the standard error (*p \ 0.05; Mann–Whitney test)
Fig. 3 The effect of radiation therapy was lower in xenografts
derived from A431-R cells. Tumour growths corresponding to A431WT cells (circles) and A431-R cells (squares) are shown for nonirradiated (unshaded) and irradiated tumours (solid symbols). 30 Gy
in 2 weeks, 5 fractions of 3 Gy/week, was administered using 6 MV
X-rays, from day 7 to day 21. In the growth curves, symbols indicate
the mean of five tumours and bars show the standard error (*p \ 0.05
compared to parental tumours; Mann–Whitney test)
Changes involved in the radioresistant phenotype
of A431-R cell line
as single cells. In addition to an increased ability to
anchorage and succeed as a cell culture, the A431-R cells
formed colonies of remarkable size—most of them with a
lower staining, which suggested an increase in the cytoplasm rather than a greater number of cells—, as depicted
in Fig. 4a, which together with clonogenic efficiency,
suggested that theses cells could be potentially more
aggressive than were earlier. To further explore the emergence of cellular traits that enable cells to exhibit malignant type of behaviour, we decided to determine the ability
Since we observed that A431-R cells were less radiosensitive than A431-WT cells, we decided to further characterize the phenotype of these resistant cells. The baseline
clonogenic efficiency of the A431-R cells was 0.19 ± 0.01
compared to 0.12 ± 0.02 of parental wild type cells
(A431-WT) (p \ 0.05; Mann–Whitney test), indicating
that A431-R cells had slightly greater capacity of surviving
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Clin Transl Oncol (2013) 15:189–197
Fig. 4 In vitro, A431-R cells showed a higher growth and faster
migration than the parental cells. a Illustrative photographs of the
colonies. The zoom shows the size of colonies and the intensity of the
staining in detail. b Representative microphotographs of the wound
healing assay at time-points 0, 5 and 24 h (bars 200 lm). Distance
shortening in the wound healing was normalized to the initial distance
between borders of each respective wound, and was represented as the
percentage of the initial wound size. Values indicate the mean of three
independent experiments done in duplicate and bars show the
standard error (*p \ 0.05; Mann–Whitney test)
of migration of these A431-R cells. Experimental findings
with the conventional wound healing assay confirmed that
A431-R cells had acquired kinetic powers during selection
process that allow them to migrate and heal the wound in a
shorter period of time than the parental cells, a behaviour
clearly consistent with the acquisition of an aggressive
phenotype (Fig. 4b).
Due to the presence of cellular traits that are linked to
sustained proliferative cell signalling, and, because, A431
parental cells overexpress the receptor of EGF, a major cell
signal emitter, we looked into this cellular pathway to
unravel possible changes that may be involved during the
development of A431-R cell line. The most remarkable
finding was that A431-R cells presented higher baseline
levels of phosphorylated EGF receptor, and the AKT and
ERK1/2 transducers (Fig. 5a), linchpin proteins that are
involved in cell growth, mitogenesis, survival, DNA repair
ability, and cell migration [15]. After cell stimulation by
the presence of EGF ligand, both types of cell lines reacted
by increasing levels of former oncoproteins, prominently
pERK1/2. When A431-WT cells were treated with ionizing
radiation, they reacted by increasing the levels of phosphorylated ERK1/2 proteins, a response that was seen
irrespectively of EGF presence. However, in the A431-R
cells, irradiation was not followed by a rise in the phosphorylated levels of EGFR, AKT or ERK1/2. In fact, a
diminution relative to their baseline levels was observed,
especially with respect to EGFR. We speculated whether
A431-R cells did not need to further activate these oncoproteins which were already hyperactivated at the baseline
conditions (Fig 5a).
To further evaluate distinct aspects of the radioresistant
phenotype, we assessed the levels of VEGF, a crucial
factor in tumour-associated angiogenesis and efficient
tumour blood supply, secretion of which may also be
regulated by EGFR and ionizing radiation [11, 16]. Both
types of cells respond to radiation by increasing the
secretion of VEGF (Fig. 5b). However, as suspected, the
release of VEGF in response to radiation was more efficiently in the A431-R cells. Thus, we concluded that these
cells were better adapted to resist strenuous conditions,
such as the oxidative stress induced by radiotherapy, and
able to promote angiogenesis to facilitate their oncogenic
potential.
Recently, the cell surface antigen CD44, a putative stem
cell marker, has been functionally validated as a biomarker
to predict local control for early laryngeal cancer treated
with radiotherapy, which suggests that this antigen could
be a proper surrogate indicator for radioresistant phenotypes [17]. Nevertheless, we did not find differential
expression of CD44 antigen in the two A431 cell lines
(Fig. 6). Thus, this infers that this protein was constitutively expressed in the parental and, hence, its derived
resistant cell line, irrespectively of their grade of radiation
sensitivity.
Finally, because cell cycle distribution can influence in
radiation sensitivity, the distribution of cell cycle phases
was examined. We found that G1 phase was 63.1 versus
67.9 %, S phase was 28.3 versus 19.8 % and G2/M phase
was 8.5 versus 12.1 %, for A431-WT and A431-R cell
population, respectively, suggesting a non-relevant variation in cell cycle between cell types.
123
Clin Transl Oncol (2013) 15:189–197
195
Fig. 5 A431-R sustained proliferative signalling through high levels
of phosphorylated EGFR, AKT and ERK1/2 proteins and radiationinduced secretion of VEGF. a Proteins were determined by Western
blot in cells under baseline culture conditions (B), EGF stimulation
(E) or ionizing radiation (5 Gy). Before cell lysis, cells were treated
with 10 ng/mL EGF for 10 min or 6 MV X-rays. a-Tubulin was used
as internal control. Bar chart shows specific protein levels normalized
by untreated A431-WT cells (white bars) versus A431-R cells (black
bars). Values indicate the mean of three independent experiments and
bars show the standard error (*p \ 0.05; Mann–Whitney test).
b VEGF was determined by the ELISA method at different interval
times after 8 Gy. Cells were left to grow without FBS for 24 h before
collecting supernatants at time 0, 24 and 48 h in A431-WT (white
bars) and A431-R cells (black bars). VEGF values were normalized
to the cell numbers per dish. Data were obtained from two
independent experiments
Fig. 6 CD44 antigen expression of A431-WT and A431-R cells
remained unchanged. a Illustrative immunofluorescence microphotographs of the surface marker CD44 under baseline culture conditions.
b Flow cytometry detection of CD44 marker. The x axis shows
negative and positive gates for CD44 marker in both types of cells,
while the y axis shows the number of events. AU stands for arbitrary
units
Discussion
of this study was to develop an isogenic resistant cell line
which could be used to identify molecular changes associated with acquired resistance to radiation and tumour
aggressiveness in cancer. The identification and understanding such mechanisms is of valuable interest, not only
In this study, we demonstrated that, by subjecting culture
cells to fractionated radiation and clonal selection, we were
able to obtain a modified cohort of cells. The ultimate aim
123
196
in overcoming radiation resistance, but also, underpinning
the biology of recurrent cancer after radiotherapy. Hence,
based on this knowledge, specific therapies for cancer
could be devised. In this regard, our study showed that,
indeed, using this model, relevant mechanisms associated
with resistance to radiation were activated. We observed
greater DNA repair, in vitro growth, cell migration, and
oncoprotein levels, mechanisms that may provide potential
targets to improve the efficacy of radiotherapy.
We developed the stable isogenic resistant A431-R cell
line from parental A431 cells. The diminution of radiosensitivity in A431-R cells was found to be comparable to
other published studies. Similar decreases in SF2 and
a-component of LQ model were reported in radioresistant
isogenic cells derived from OE33 esophagal adenocarcinoma cells. These changes were associated with an
increased efficiency in DNA repair [18]. Equivalent levels
of acquired tolerance to radiation were also found in the
resistant version of the human lung adenocarcinoma cell
line, Anip973 [19]. In these already published studies, as
well as our own, radioresistant cells showed moderate levels
of radiation desensitization. However, it should be taken
into account that in fractionated radiotherapy a small variation in radiosensitivity could have a greater effect on the
ultimate resistance than the simple difference in SF2, as
shown in Fig. 2.
Besides radiation resistance, we demonstrated that
A431-R cells acquired higher cloning efficiency and in vitro
faster growth and migration ability; these properties were
observed to be associated with remarkable baseline levels of
relevant oncoproteins and elevated angiogenic capabilities.
Earlier, our group described that radiation was found to
induce the emergence of aggressive tumour growth in A431
cells. We identified that the addiction to EGFR was associated with this malignant phenotype and tumour-associated
angiogenesis [11]. Recently, similar phenotype was elicited
by radiation-induced cell signalling involving the protein
encoded by c-Met [9]. These findings strongly suggest that
cancer cells may develop adaptive responses to damaging
agents, such as ionizing radiation, leading to the gain of
molecular mechanisms to protect themselves from the lethal
effects of these agents. Cellular stress regulates distinct
genetic and epigenetic programs that may determine the
acquisition of tolerance to radiation and the biology of
cancer cells, as consequence, re-programming their cellular
machinery. This notion is supported by new discoveries in
radiation resistance. Also, the acquisition of resistance to
radiation was found to be associated with increased levels
of reduced state of glutathione, pointing at a better
expression of genes encoding enzymes that maintain glutathione operative [18]. Similar meaning would be ascribed
to the low levels of intracellular-free radical observed in
123
Clin Transl Oncol (2013) 15:189–197
isogenic resistant human non-small cell lung cancer cells
[20]. In these adjustments, glutathione levels may be a
reflection of re-programming energy metabolism in cancer
cells leading to higher utilization of glucose and enhancing
NADPH production, ready to be used in glutathione synthesis [21]. The participation of oncogenic proteins such as
AKT (through mTOR), RAS or HIF1a in glycolytic fuelling
as a response to oxidative stress [22, 23] gives additional
support to the notion that global changes are induced by
radiation, and goes beyond the idea of an isolated phenomenon of resistance.
Radiation-induced resistant cells have also revealed
changes attributed to radiation in transciptome. Upregulation or downregulation of genes encoding proteins that are
involved in DNA repair and anti-apoptosis, as well as in
motility, invasion and angiogenesis have been reported.
However, the representation of the genes involved in
resistance varies, depending on the authors [19, 20, 24].
Variations in the genetic origin of cells, methods used to
generate the experimental model and the technical differences to analyse gene expression may all have influenced
the diversity of findings. Experimental design based on
isogenic cells, such as the A431-WT and A431-R pair,
could make it more suitable to directly attribute changes in
gene regulation to ionizing radiation because isogenic cells
have the same genetic background. However, it should be
mentioned that the findings using cultured cells growing on
plastic culture dishes are not influenced by factors such as
tumour hypoxia, microenvironment (including tumourstroma heterotypic interaction) and angiogenesis that occur
in true oncogenesis. In this regard, these factors could have
contributed to the observation that the growth of nonirradiated tumours that were derived from A431-WT cells
showed similar pattern of growth as those tumours from
A431-R cells, a finding that was not observed in vitro. To
improve in vitro limitations, further efforts are needed to
characterize in vivo experimental tumour models.
In conclusion, in this article we have presented an
effective method to develop a radioresistant cell line, and
showed that the emergence of tolerance to radiation was
associated with the acquisition of an aggressive phenotype.
In our opinion, this methodology may provide useful
experimental models in order to gain insights into the
biology of acquired radiation resistance.
Acknowledgments The authors would like to acknowledge the
financial support of the Spanish Association against Cancer, Barcelona Committee, and the Merck KGaA company. We are grateful to
Scientific Services of the University of Barcelona for cytometry
assistance in cell cycle evaluation, and Jo Ellen Klaustermeier for her
excellent assistance with the manuscript elaboration.
Conflict of interest
None.
Clin Transl Oncol (2013) 15:189–197
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2. Abbott A (2006) Cancer: the root of the problem. Nature 442:742–743
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8. Toulany M, Schickfluss TA, Fattah KR et al (2011) Function of erbB receptors
and DNA-PKcs on phosphorylation of cytoplasmic and nuclear Akt at S473
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10. Park CM, Park MJ, Kwak HJ et al (2006) Ionizing radiation enhances matrix
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13. Balart J, Pueyo G, de Llobet LI et al (2011) The use of caspase inhibitors in
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17. de Jong MC, Pramana J, van der Wal JE et al (2010) CD44 expression predicts
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123
Published online on 21 June 2012 Lab Anim, doi: 10.1258/la.2012.011147
Short Report
Development and refinement of a technique using a medical
radiation therapy facility to irradiate immunodeficient mice
bearing xenografted human tumours
Marta Baro1 , Lara I de Llobet1 , Ignasi Modolell2, Ferran Guedea3, Joana Visa4
and Josep Balart1,5
1
Translational Research Laboratory, Catalan Institute of Oncology and IDIBELL, Avinguda Gran Via de l’Hospitalet, 199-203, 08907
l’Hospitalet de Llobregat, Spain; 2Medical Physics and Radioprotection Department, Catalan Institute of Oncology and IDIBELL, Avinguda
Gran Via de l’Hospitalet, 199-203, 08907 l’Hospitalet de Llobregat, Spain; 3Radiation Oncology Department, Catalan Institute of Oncology
and IDIBELL, Avinguda Gran Via de l’Hospitalet, 199-203, 08907 l’Hospitalet de Llobregat, Spain; 4Animal Facility, IDIBELL, Avinguda
Gran Via de l’Hospitalet, 199-203, 08907 l’Hospitalet de Llobregat, Spain; 5Radiation Oncology Department, Hospital de la Santa Creu i
Sant Pau, Sant Antoni M Claret, 167, 08025 Barcelona, Spain
Corresponding author: J Balart. Laboratori de Recerca Translacional, Institut Català d’Oncologia-IDIBELL, Avinguda Gran Via de
l’Hospitalet, 199-203, 08907 l’Hospitalet de Llobregat, Spain. Email: [email protected]
Abstract
The need for using immunodeficient mice for xenoimplantation of tumours is increasing in translational research in radiation
oncology. However, adverse effects of radiation and infectious diseases may ruin the experimental work, in particular when
appropriate facilities are not available. In this report, we describe a procedure to deliver fractionated radiotherapy to
xenoimplanted tumours in immunodeficient mice using a medical linear accelerator, a method that was devised as an
alternative to the lack of facilities devoted to radiation research. The mice were irradiated under anaesthesia and aseptic
conditions. Thirty Gray in 10 days using a 6 MV photon beam were delivered only to the right thigh of the mice where tumours
were implanted. The mice were evaluated twice a week up to planned euthanasia. The follow-up of mice was completed
without premature interruption due to toxicities or infectious diseases, an observation which demonstrates the feasibility of
the method.
Keywords: Xenografted tumours, immunodeficient mice, local fractionated radiotherapy, medical linear accelerator
Laboratory Animals 2012: 1 –4. DOI: 10.1258/la.2012.011147
Every year, millions of cancer patients around the world
undergo radiotherapy, alone or in combination with
drugs. The rise in radiotherapy use, together with an
avenue of novel drugs that modulate radiotherapy action,
has prompted an increased interest in radiation oncology
research. An important part of this research is based on
the irradiation of human tumours grown in mice.1,2
However, such experimental models are associated with a
number of difficulties that can ruin the experimental outcomes. First, it is difficult to shield radiosensitive healthy
tissues from the radiation field and avoid its adverse
effects in the absence of appropriate equipment to irradiate
mice, such as an orthovoltage X-ray treatment machine.3
Second, to prevent the tumour rejection mediated by a
Marta Baro and Lara I de Llobet contributed equally to this work
and should be considered co-first authors
normal immune system, human tumour cells have to be
implanted in immunodeficient mice which are prone to
lethal infectious diseases. Third, there is a general lack of
specific pathogen free (SPF) facilities to irradiate mice.
Since these have to be transferred from the SPF colony to
medical radiotherapy units, the risk of infectious outbreaks
is greatly increased. Finally, to make matters even more
complex, often experimental design requires multiple fractions of radiotherapy, which exposes mice to pathogens
more frequently.
In this short report, we describe the experimental procedure
and the refinements we applied to successfully deliver high
doses of fractionated radiotherapy to xenoimplanted human
tumours, protect radiosensitive tissues and decrease the microbiological risk when irradiating immunodeficient mice using a
medical linear accelerator. Importantly, we devised this procedure as an alternative to the lack of experimental facilities
devoted to radiation research in immunodeficient mice.
Laboratory Animals 2012: 1– 4
Copyright 2012 by the Laboratory Animals Limited
2
Laboratory Animals
................................................................................................................................................
All experimental methods were approved in accordance
with our own institutional IDIBELL guidelines for animal
care and ethics. Six to eight-week-old female athymic mice
(Athymic Nude-Foxn1nu, Harlan, Gannat, France) were
used. Complete health reports, especially the microbiological
status of the animals based on the Federation of European
Laboratory Animal Science Associations (FELASA) recommendations, were certified by the vendor. Tumours
were generated by injecting one million human cancer cells
delivered in 100 mL into the subcutaneous tissue. The mice
were intraperitoneally anaesthetized (1 mL/kg of each solution: 50 mg/mL ketamine and 1 mg/mL medetomidine
with 5 mg/mL atipamezole for the reversal of the anaesthesia effects) in order to precisely control the area in which the
cells were to be injected and to obtain homogenous growth
of tumours. We decided to inject the cells in the right
thigh of the mice, which allowed us to irradiate exclusively
a limited part of the body. This decision served to protect
the rest of the animal body from radiation.
At a suitable tumour size, and two days before
irradiation, the mice were moved from the SPF area to a
quarantine room so they can adapt to the new housing conditions, and where the animals were to be permanently
housed in closed autoclaved plastic cages (5 mice per
cage). In this room, the mice were manipulated under a
laminar flow hood using aseptic conditions. Before each
radiotherapy session, they were anaesthetized, as mentioned above, and transported to the radiotherapy unit in
clean autoclaved closed cages covered with a drape to
conceal the animals from plain view.
Upon arrival at the radiotherapy room, the treatment
table was disinfected with alcohol and covered with sterile
drapes. Surgical caps, masks and sterile gloves were worn.
Figure 1 shows the scheme of how an appropriate setting
for selectively irradiating tumours and reducing infections
in the mice was achieved. Of note is the placement of the
thigh on the edge of the radiation beam to allow sufficient
coverage of the tumour, while protecting the body of the
mice as much as possible.
To irradiate the animals, as shown in Figure 1, a 6 MV
photon beam from a Varian Clinac 2100 linear accelerator
was used. A total dose of 30 Gray (Gy) in fractions of
3 Gy, separated by 24 h, excluding Saturdays and Sundays
was administrated. The dose rate was 2.7 Gy per minute.
In order to verify the dose that the tumours received, as
well as the precision of the set-up used, an in vivo dosimetry
was performed by means of radiochromic films (Gafchromic
EBT, International Specialty Products, Wayne, NJ, USA). In
total, 40 dose measurements were carried out during four
separate days. Films were placed in contact with the
tumour at the beam entrance. We found less than 3% variation in the doses received by different mice on the same
sessions and less than 1.5% variation between different
days. The mean deviation in absorbed dose in the
tumours was 2.3% of the prescribed dose. The aforementioned results confirmed that our experimental set-up was
homogeneous and reproducible.
The mice were evaluated twice a week. Table 1 describes
the animals’ health during the radiotherapy period and
follow-up. Non-irradiated mice were subjected to the same
procedures. No animals were excluded or had received
less than 30 Gy in 10 fractions. After radiotherapy,
tumours grew more slowly and took twice the time to
reach a volume equivalent to non-irradiated animals. The
most severe observation was always registered, whether it
was reversible or not. The greatest adverse effect of
Figure 1 Scheme used for localized irradiation of xenografted tumours in multiple fractions. Tumours (T) were placed into the gap created by two polymethyl
methacrylate (PMMA) plates (b), each were 35 cm 35 cm 1 cm in size, separated by a smaller plate (30 cm 30 cm 1 cm). The edge of the beam was
adjusted to cover the tumour with 1 cm margin, assuring that PMMA plates were included into the beam. The thighs were kept in place using an adhesive
tape, while the body of animals was maintained out of the beam. Sterile drape that cover the treatment table (a) and wrapped PMMA plates are represented
by the grey lines. Dotted line illustrates the sterile transparent film put on to the mice, protecting them from the non-sterile top PMMA plate, as it can also be
observed in the pictures on the right. The source-plate distance was set to 100 cm on the centre of the top plate. Note that dimensions in the diagram are
not to scale
Baro et al.
3
Irradiation of xenografted human tumours
................................................................................................................................................
Table 1 Quality of life of the mice during and after localized irradiation in multiple fractions
Control mice (non-irradiated)
X-ray-treated mice
Post-therapy period
(n 5 12)
Therapy period (n 5 13)
Grade score (%)
Post-therapy period
(n 5 31)
Therapy period (n 5 32)
Grade score (%)
Grade score (%)
Grade score (%)
Supervision parameters
0
1
2
3
0
1
2
3
0
1
2
3
0
1
2
3
Weight loss†
Physical aspects‡
Clinical signals}
Behaviour alterations#
Infections††
Stools‡‡
Tumour necrosis}}
Local radiation toxicity##
76.9
100
100
100
100
100
100
100
15.4
0
0
0
0
0
0
0
7.7
0
0
0
0
0
–
0
0
0
0
0
–
–
–
0
83.3
100
100
100
100
100
91.7
100
8.3
0
0
0
0
0
8.3
0
8.3
0
0
0
0
0
–
0
0
0
0
0
–
–
–
0
43.8
100
100
100
100
100
100
100
46.9
0
0
0
0
0
0
0
9.4
0
0
0
0
0
–
0
0
0
0
0
–
–
–
0
61.3
100
100
87.1
100
100
100
100
35.5
0
0
12.9
0
0
0
0
3.2
0
0
0
0
0
–
0
0
0
0
0
–
–
–
0
Values are the proportion of an observation expressed in grades related to the total number of animals (n) within the period of follow-up
†
Weight loss. Grades: 0 no weight loss; 1 less than 10%; 2 between 10 and 20%; 3 more than 20%
‡
Physical appearance. Grades: 0 normal; 1 changes in skin colour; 2 paleness and cyanosis; 3 hunching and loss of muscular mass
}
Clinical signals. Grades: 0 no presence; 1 hypothermia; 2 bleeding or mucosal secretion in any orifice; 3 abdominal strain and cachexia
#
Behaviour alterations. Grades: 0 no alterations; 1 unable to move normally; 2 impossible to arrive to food/drink; 3 unconsciousness and no response to stimuli
††
Percentage of animals with infectious disease. Grades: 0 no infections; 1 animals infected that survived; 2 animals infected that died. Grade 3 not evaluated (NA)
‡‡
Stools appearance. Grades: 0 normal; 1 soft stools; 2 visible blood. Grade 3 NA
}}
Percentage of tumour necrosis. Grades: 0 no tumour necrosis; 1 tumour necrosis. Grades 2 and 3 NA
##
Local radiation-induced toxicity. Grades: 0 no presence; 1 erythema; 2 exudative lesion; 3 necrosis
radiation was the diminution in the initial weight, which we
ascribed to the partial exposure of the inferior right hemiabdomen, which was much too close to the tumour to be completely protected from the radiation beam. However, the
weight loss was not remarkable and was limited to grade
1, transitory and not associated with physical or clinical
signs of disease. Also, in the irradiated group, two
animals (12.9%) moved abnormally due to tumour
growth, but not to local reaction because of the radiation.
Interestingly, in non-irradiated mice greater weight loss
was observed, which was attributable to uncontrolled
tumour growth. Differences in weight loss between
groups, however, were not significant (chi-square and
Mann-Whitney U test). No infections were observed.
Euthanasia using intraperitoneal pentobarbital solution
(4.5 mL/kg dose of 200 mg/mL of Dolethal) was planned
at day þ90, or, before, in cases where more than one
grade 2 or one grade 3 event was observed, or when the
tumour size reached more than 1500 mm3; however, only
the last criterion had had to be applied. We applied these
criteria following the international guidelines for the
welfare and use of animals in cancer research.4
In this report, four objectives were considered during
radiotherapy design. First, minimize irradiation of healthy
tissues around the tumour. Second, fulfil the standard
irradiation principles for human treatment.5,6 Third,
reduce time and increase efficiency by irradiating several
mice at a time. Finally, be easy to reproduce and repeat on
a daily basis by only two people. We demonstrated the
feasibility of fractionated irradiation using immunodeficient
mice to evaluate the role of radiotherapy on experimental
tumours simulating a clinical setting. The major contribution of this study, however, was to demonstrate that
general or local effects of irradiation did not jeopardize
the tumour radiation –response observation over a long
follow-up. In addition, the absence of infect –contagious diseases was particularly decisive for the success of
experiments. This provided evidence that the barrier protections used accomplished the goal of preventing microbiological diseases in these animals. Since cancer patients are
often immunosuppressed, concerns about zoonoses should
not be ignored. Nevertheless, it should be emphasized
that the potential risk of zoonoses is extremely low when
good laboratory practices and healthy athymic mice are
used. To our knowledge, there is no report in the medical
literature about the incidence of opportunistic zoonoses in
patients treated in such radiation oncology departments.
In conclusion, this study describes an effective method to
irradiate human tumours implanted in immunodeficient
mice which allows monitoring of tumour responses
without interference from the adverse effects of radiation
and infection. We demonstrate the feasibility of delivering
fractionated radiotherapy using a medical accelerator
when a specific experimental facility is not available for
radiation research.
ACKNOWLEDGEMENT
The authors would like to acknowledge the financial
support of the Spanish Association Against Cancer,
Barcelona Committee.
Conflict of interest: Actual or potential conflicts of interest
do not exist.
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