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      Indoleamine 2,3-dioxygenase (IDO) is frequently expressed in stromal cells of Hodgkin lymphoma and is associated with adverse clinical features: a retrospective cohort study

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          Abstract

          Background

          Regulation of tumor microenvironment is closely involved in the prognosis of Hodgkin lymphoma (HL). Indoleamine 2,3-dioxygenase (IDO) is an enzyme acting as immune modulator through suppression of T-cell immunity. This study aims to investigate role of IDO in the microenvironment of HL.

          Methods

          A total of 121 cases of HL were enrolled to do immunohistochemistry for IDO, CD163, CD68, CD4, CD8, and FoxP3. Positivity was evaluated from area fractions or numbers of positive cells using automated image analyzer. Correlations between IDO expression and various cellular infiltrates and clinicopathologic parameters were examined and survival analyses were performed.

          Results

          IDO was expressed in histiocytes, dendritic cells and some endothelial cells with variable degrees, but not in tumor cells. IDO positive cells were more frequently found in mixed cellularity type than other histologic types, and in cases with EBV+, high Ann Arbor stages, B symptoms, and high IPS (all p < 0.05). High IDO expression was associated with inferior survival (p < 0.001) and reflects an independent prognostic factor in nodular sclerosis HL.

          Conclusions

          This is the first study suggesting that IDO is the principle immunomodulator and is involved to adverse clinical outcomes of HL.

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          Most cited references17

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          Indoleamine 2,3-dioxygenase expression in human cancers: clinical and immunologic perspectives.

          Jessica Godin-Ethier, Laïla-Aïcha Hanafi, Ciriaco Piccirillo … (2011)
          Indoleamine 2,3-dioxygenase (IDO) is a tryptophan-catabolizing enzyme with immune-regulating activities in many contexts, such as fetal protection, allograft protection, and cancer progression. Clinical trials are currently evaluating IDO inhibition with 1-methyltryptophan in cancer immunotherapy. However, the exact role of tryptophan catabolism by IDO in human cancers remains poorly understood. Here, we review several studies that correlate IDO expression in human cancer samples and tumor-draining lymph nodes, with relevant clinical or immunologic parameters. IDO expression in various histologic cancer types seems to decrease tumor infiltration of immune cells and to increase the proportion of regulatory T lymphocytes in the infiltrate. The impact of IDO on different immune cell infiltration leads to the conclusion that IDO negatively regulates the recruitment of antitumor immune cells. In addition, increased IDO expression correlates with diverse tumor progression parameters and shorter patient survival. In summary, in the vast majority of the reported studies, IDO expression is correlated with a less favorable prognosis. As we may see results from the first clinical trials with 1-methyltryptophan in years to come, this review brings together IDO studies from human studies and aims to help appreciate outcomes from current and future trials. Consequently, IDO inhibition seems a promising approach for cancer immunotherapy.
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            Role of the immunosuppressive enzyme indoleamine 2,3-dioxygenase in the progression of ovarian carcinoma.

            Tomoko Inaba, Kazuhiko Ino, Hiroaki Kajiyama … (2009)
            Indoleamine 2,3-dioxygenase (IDO) is a tryptophan-catabolizing enzyme that induces immune tolerance. The purpose of the present study is to investigate IDO expression and its functional role in ovarian cancer cells in vitro and in vivo. IDO expression was immunohistochemically scored in surgically-resected ovarian cancer tissues (n=60), and its association with tumor-infiltrating lymphocyte (TIL) count or patient survival was analyzed. Next, IDO cDNA was transfected into the human ovarian carcinoma cell line SKOV3, establishing stable clones of IDO-overexpressing cells (SK-IDO). SK-IDO cells were characterized in vitro as well as in vivo using a nude mouse xenograft model. High IDO expression in tumor cells was found in 34 (56.7%) cases and was correlated with a reduced number of CD8+ TIL. Patients with high IDO expression had significantly impaired overall and progression-free survival compared to patients with no or low IDO expression. There were no significant differences in in vitro cell proliferation, migration, invasion, or chemosensitivity to paclitaxel between the SK-IDO and control vector-transfected (SK-pcDNA) cells. However, tumor peritoneal dissemination was significantly increased in SK-IDO-xenografted mice compared to SK-pcDNA-xenografted mice. This tumor-progressive effect in SK-IDO-xenografted mice was abrogated by oral administration of the IDO inhibitor 1-methyl-tryptophan (1-MT). Finally, treatment with weekly i.p. paclitaxel combined with daily administration of 1-MT significantly prolonged the survival of the SK-IDO-xenografted mice compared to treatment with paclitaxel alone. These results suggest that IDO is involved in ovarian cancer progression in vivo and may be a promising therapeutic target for advanced ovarian cancer.
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              The role of indoleamine 2,3-dioxygenase in the induction of immune tolerance: focus on hematology.

              Antonio Curti, Valentina Salvestrini, Sara Trabanelli … (2009)
              The regulation of the interaction between the immune system and antigens, which may lead to the induction of immune tolerance, is critical both under physiologic conditions and in different pathological settings. In the past few years, major strides have been made in our understanding of the molecular and cellular bases of this process. Novel pathways have been identified and several novel therapeutic agents are currently under clinical investigation for those diseases in which the normal balance between activation and suppression of the immune response is altered. The tryptophan catabolic enzyme, indoleamine 2,3-dioxygenase (IDO), is one of the key players involved in the inhibition of cell proliferation, including that of activated T cells. Recent works have demonstrated a crucial role for IDO in the induction of immune tolerance during infection, pregnancy, transplantation, autoimmunity, and neoplasias, including hematologic malignancies. In this review, the role of IDO in the induction of immunologic tolerance is addressed with a specific focus on its recently discovered effect on hematologic malignancies.
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                Author and article information

                Contributors
                Ji-Young Choe
                Ji Yun Yun
                Yoon Kyoung Jeon
                Se Hoon Kim
                Gyeongsin Park
                Joo Ryoung Huh
                Sohee Oh
                Ji Eun Kim
                Journal
                Journal ID (nlm-ta): BMC Cancer
                Journal ID (iso-abbrev): BMC Cancer
                Title: BMC Cancer
                Publisher: BioMed Central
                ISSN (Electronic): 1471-2407
                Publication date Collection: 2014
                Publication date (Electronic): 15 May 2014
                Volume: 14
                Page: 335
                Affiliations
                [1 ]Department of Pathology, Seoul National University Bundang Hospital, Seongnam-si, Korea
                [2 ]Department of Pathology, Seoul National University Hospital, Seoul, Korea
                [3 ]Department of Pathology, Yonsei University College of Medicine, Seoul, Korea
                [4 ]Department of Pathology, Seoul St. Mary’s Hospital, The Catholic University of Korea, Seoul, Korea
                [5 ]Department of Pathology, Asan Medical Center, Seoul, Korea
                [6 ]Department of Biostatistics, Seoul National University Boramae Hospital, Seoul, Korea
                [7 ]Department of Pathology, Seoul National University Boramae Hospital, Seoul, Korea
                Article
                Publisher ID: 1471-2407-14-335
                DOI: 10.1186/1471-2407-14-335
                PMC ID: 4026588
                PubMed ID: 24886161
                SO-VID: 6315f6ed-02f1-4b3d-8e03-c3085ca2c090
                Copyright © Copyright © 2014 Choe et al.; licensee BioMed Central Ltd.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.

                History
                Date received : 2 September 2013
                Date accepted : 2 May 2014
                Categories
                Subject: Research Article

                ScienceOpen disciplines: Oncology & Radiotherapy
                Keywords: hodgkin disease,indoleamine-pyrrole 2,3-dioxygenase,macrophages,stromal cells,tumor microenvironment,epstein-barr virus infections,pathology
                Data availability:
                ScienceOpen disciplines: Oncology & Radiotherapy
                Keywords: hodgkin disease, indoleamine-pyrrole 2,3-dioxygenase, macrophages, stromal cells, tumor microenvironment, epstein-barr virus infections, pathology

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