Acta Dermato-Venereologica 99-12CompleteContent | Page 34
SHORT COMMUNICATION
Effect of Indoleamine 2,3 Dioxygenase Inhibitor on the Cytotoxic Activity of Tumour-infiltrating
Lymphocytes
Sarah LE NAOUR 1 , Anne-Chantal KNOL 1 , Marie-Christine PANDOLFINO 2 , Amir KHAMMARI 1 and Brigitte DRÉNO 1,2
1
Dermato-Cancerology Department, CHU Nantes, CIC1413, CRCINA, University Nantes, Place Alexis Ricordeau, FR-44093 Nantes, and 2 Cell
and Gene Therapy Unit, CHU Nantes, Nantes, France. E-mail: [email protected]
Accepted Aug 12, 2019; E-published Aug 13, 2019
There have been major therapeutic advances in the treat-
ment of melanoma in recent years (1, 2). Adoptive T-cell
therapy, based on tumour-infiltrating lymphocytes (TILs)
obtained from tumour tissues, has been developed in the
field of immunotherapy. An objective clinical response of
between 40% and 72% in the metastatic stage has been
reported (3, 4) but the clinical response remains limited
in time. In the metastatic stage of melanoma, the clinical
response remains limited and short-term. A major current
challenge is to increase the efficacy of TILs by countering
the immune tolerance of the tumour microenvironment
through identification of the molecules implicated in this
phenomenon. Many factors have been suggested, inclu-
ding indoleamine 2,3 dioxygenase (IDO), an intracellular
enzyme that metabolizes tryptophan to kynurenine. Tryp-
tophan deficiency inhibits the activity and proliferation
of T cells (5). A recent paper (6) has shown that IDO1
expression in metastatic melanoma lymph nodes is as-
sociated with an increased risk of relapse and death. Thus,
we hypothesize that the presence of IDO in the tumour
microenvironment could inhibit the activity of TILs, and
that adding an IDO inhibitor to the TILs could increase
their cytotoxic activity against melanoma cells.
In a first step, the 7 melanoma cell-lines were incubated either
with an IDO inhibitor, 1-methyl-L-tryptophan (1-MT) (in 2 dif-
ferent concentrations), alone or after incubation with interferon
gamma (INF-γ) for mimicking the chronic inflammatory micro-
environment state of a metastasis (associated with an increase
in immune tolerance). In a second step, the 7 melanoma cells
were distributed on a 96-well plate (300,000 cells per well) with
100,000 autologous TILs. Co-cultures were incubated for 6 h at
37°C, 5% CO 2 . Finally, melanoma cells were analysed by flow
cytometry for expression of IDO1, MHC-I, MHC-II and PD-L1
antigens and reactivity of TILs by a double-labelling: membrane
CD3 and intracellular interferon (IFN)-γ. The data were analysed
using CellQuestPro ® software. Tryptophan and kynurenine levels
were determined by enzyme-linked immunoassay (ELISA) (Im-
muSmol (BD Biosciences, San Jose, USA)) in order to calculate
kynurenine/tryptophan ratios.
RESULTS
In the basal state (without INF-γ), IDO1 expression was
shown for 5 melanoma cell-lines (Fig. 1a). MHC-I was
expressed by all the cell-lines. MHC-II was expressed
by only 4 cell-lines. No expression of PD-L1 was noted
in any of the 7 cell-lines. Intracytoplasmic expression of
IFN-γ by TILs was very low in the basal state. Adding
the IDO inhibitor decreased the expression of IDO1 in
a dose-dependent manner (Fig. 1a). For both MHC-I
and MHC-II, IDO inhibitor increased their expression
in a dose-dependent manner (Fig. 1b, c). No effect on
the cytotoxic activity of TILs was found by adding IDO
inhibitor (Fig. 2). The absence of expression of IDO1
by 2 melanoma cell-lines is in agreement with a recent
paper showing that not all melanoma metastases express
IDO (11).
In the inflammatory state (induced by INF-γ), IDO1 was
expressed in all melanoma cell-lines: 2 melanoma cell-
lines not expressing IDO1 in the basal state, and increased
in the other 5 cell-lines in a dose-dependent manner (Fig.
0,00
0,05
0
20
0
0,15
0,10
40
20
0,20
40
d
0,25
80
60
Median
0,30
100
60
b
80
Median
80
70 c
60
50
40
30
20
10
0
Median
120
a
Median
100
To investigate this hypothesis we used the model of co-culture of
a melanoma cell-line and autologous TILs obtained from the same
patient (6), with the addition of IDO inhibitor. The endpoints were
the frequency of reactive autologous T cells among the TILs and
the expression of molecules involved in the recognition of tumour
antigens by T cells with and without IDO inhibitor. Melanoma
cells were derived from patients with metastatic melanoma, who
were previously included in several distinct clinical trials of TILs
(7–10). Seven tumour cell-lines with associated autologous TILs
were selected (4 wild-type cell-lines and 3 cell-lines with positive
BRAF mutational status, but no difference according this muta-
tional status was noted).
MATERIAL AND METHODS
1186
Fig. 1. (a) Kynurenine/tryptophan ratios. (b) Mean fluorescence intensity (MFI) for MHC-I expression. (c) MFI for MHC-II expression. (d) Percentage of
positive cells for PD-L1: results expressed as median, green = basal state, red = inflammatory state.
doi: 10.2340/00015555-3285
Acta Derm Venereol 2019; 99: 1186–1187
This is an open access article under the CC BY-NC license. www.medicaljournals.se/acta
Journal Compilation © 2019 Acta Dermato-Venereologica.