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      A Potential Protein Adjuvant Derived from Mycobacterium tuberculosis Rv0652 Enhances Dendritic Cells-Based Tumor Immunotherapy

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          Abstract

          A key factor in dendritic cell (DC)-based tumor immunotherapy is the identification of an immunoadjuvant capable of inducing DC maturation to enhance cellular immunity. The efficacy of a 50S ribosomal protein L7/L12 (rplL) from Mycobacterium tuberculosis Rv0652, as an immunoadjuvant for DC-based tumor immunotherapy, and its capacity for inducing DC maturation was investigated. In this study, we showed that Rv0652 is recognized by Toll-like receptor 4 (TLR4) to induce DC maturation, and pro-inflammatory cytokine production (TNF-alpha, IL-1beta, and IL-6) that is partially modulated by both MyD88 and TRIF signaling pathways. Rv0652-activated DCs could activate naïve T cells, effectively polarize CD4 + and CD8 + T cells to secrete IFN-gamma, and induce T cell-mediated-cytotoxicity. Immunization of mice with Rv0652-stimulated ovalbumin (OVA)-pulsed DCs resulted in induction of a potent OVA-specific CD8 + T cell response, slowed tumor growth, and promoted long-term survival in a murine OVA-expressing E.G7 thymoma model. These findings suggest that Rv0652 enhances the polarization of T effector cells toward a Th1 phenotype through DC maturation, and that Rv0652 may be an effective adjuvant for enhancing the therapeutic response to DC-based tumor immunotherapy.

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          Most cited references37

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          T cell receptor antagonist peptides induce positive selection.

          Kristin A. Hogquist, Stephen C. Jameson, William R. Heath … (1994)
          We have used organ culture of fetal thymic lobes from T cell receptor (TCR) transgenic beta 2M(-/-) mice to study the role of peptides in positive selection. The TCR used was from a CD8+ T cell specific for ovalbumin 257-264 in the context of Kb. Several peptides with the ability to induce positive selection were identified. These peptide-selected thymocytes have the same phenotype as mature CD8+ T cells and can respond to antigen. Those peptides with the ability to induce positive selection were all variants of the antigenic peptide and were identified as TCR antagonist peptides for this receptor. One peptide tested, E1, induced positive selection on the beta 2M(-/-) background but negative selection on the beta 2M(+/-) background. These results show that the process of positive selection is exquisitely peptide specific and sensitive to extremely low ligand density and support the notion that low efficacy ligands mediate positive selection.
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            Dendritic cell regulation of TH1-TH2 development.

            M. Moser, K Murphy (2000)
            Understanding the control exerted by cytokines on T helper cell subsets 1 and 2 (TH1-TH2) development has progressed to a fairly satisfying knowledge of intracellular signals and transcription factors. Less is understood about the molecular basis of TH1-TH2 development exerted by other parameters, such as how the antigen presenting cell can influence this process. Recent work suggests that dendritic cell subsets contribute significant polarizing influences on T helper differentiation, but how this comes about is less clear. In some cases known pathways may be used, as in the dendritic cell subset 1 exerting TH1 polarization by interleukin 12 (IL-12) production and STAT4 activation. In others, the effects are still in need of explanation.
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              Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos.

              Sudhanshu Agrawal, Jay Doughty, Anshu Agrawal … (2003)
              Dendritic cells (DCs) are pivotal in determining the class of an adaptive immune response. However, the molecular mechanisms within DCs that determine this decision-making process are unknown. Here, we demonstrate that distinct Toll-like receptor (TLR) ligands instruct human DCs to induce distinct Th cell responses by differentially modulating mitogen-activated protein kinase signaling. Thus, Escherichia coli LPS and flagellin, which trigger TLR4 and TLR5, respectively, instruct DCs to stimulate Th1 responses via IL-12p70 production, which depends on the phosphorylation of p38 and c-Jun N-terminal kinase 1/2. In contrast, the TLR2 agonist, Pam3cys, and the Th2 stimulus, schistosome egg Ags: 1) barely induce IL-12p70; 2) stimulate sustained duration and magnitude of extracellular signal-regulated kinase 1/2 phosphorylation, which results in stabilization of the transcription factor c-Fos, a suppressor of IL-12; and 3) yield a Th2 bias. Thus, distinct TLR agonists differentially modulate extracellular signal-regulated kinase signaling, c-Fos activity, and cytokine responses in DCs to stimulate different Th responses.
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                Author and article information

                Contributors
                Jian-Xin Gao: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2014
                Publication date (Electronic): 7 August 2014
                Volume: 9
                Issue: 8
                Electronic Location Identifier: e104351
                Affiliations
                [1 ]Department of Immunology, Lab of Dendritic Cell Differentiation & Regulation, School of Medicine, Konkuk University, Chungju, South Korea
                [2 ]Department of Microbiology, Institute for Immunology and Immunological Diseases, Brain Korea 21 PLUS Project for Medical Science, Yonsei University College of Medicine, Seoul, South Korea
                [3 ]Department of Physiology, College of Medicine, Korea University, Seoul, South Korea
                [4 ]Department of Physiology, School of Medicine, Kangwon National University, Chuncheon, South Korea
                [5 ]Department of Biochemistry, College of Medicine, Seonam University, Namwon, Jeonbuk, South Korea
                [6 ]Division of Biotechnology, Advanced Institute of Environment and Bioscience, College of Environmental & Bioresources Sciences, Chonbuk National University, Iksan, South Korea
                [7 ]Department of Pharmacology, College of Medicine, Chung-Ang University, Seoul, South Korea
                [8 ]Department of Agricultural Biotechnology, and Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, South Korea
                Shanghai Jiao Tong University School of Medicine, China
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Performed the experiments: SJL SJS MHL WSP BYS JHP HWK IDJ YMP. Analyzed the data: SJL SJS MGL YKS CHY IDJ YMP. Contributed reagents/materials/analysis tools: SJS MGL THK YKS CHY IDJ YMP. Wrote the paper: MGL CHY IDJ YMP.

                Article
                Publisher ID: PONE-D-13-54738
                DOI: 10.1371/journal.pone.0104351
                PMC ID: 4125215
                PubMed ID: 25102137
                SO-VID: bc911831-0788-4ef1-bf4a-141f7367b90f
                Copyright statement: Copyright @ 2014
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 1 January 2014
                Date accepted : 13 July 2014
                Page count
                Pages: 11
                Funding
                This study was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean Government (NRF-2012R1A2A1A03008433, NRF-2012R1A1A4A01007325, and NRF-2011-0028573), a grant from the National R&D Program for Cancer Control, Ministry for Health and Welfare, Republic of Korea (1120390). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Cell Biology
                Subject: Cellular Types
                Subject: Animal Cells
                Subject: Immune Cells
                Subject: Molecular Cell Biology
                Subject: Immunology
                Subject: Immunity
                Subject: Immune Activation
                Subject: Antigen Processing and Recognition
                Subject: Clinical Immunology
                Subject: Immune Response
                Subject: Immune System
                Subject: Immunomodulation
                Subject: Vaccination and Immunization
                Subject: Microbiology
                Subject: Physiology
                Subject: Immune Physiology
                Subject: Medicine and Health Sciences

                ScienceOpen disciplines: Uncategorized
                Data availability:
                ScienceOpen disciplines: Uncategorized

                Comments

                added an editorial note to Cancer Immunotherapy
                This article was selected by ScienceOpen Consulting Editor, Richard Gallagher, to appear in the Collection entitled Cancer Immunotherapy which can be found here http://ow.ly/Jy1HH. 1. Why this article was chosen: it shows that an immunostimulatory adjuvant enhances dendritic cell maturation, potentially generating antitumor immune responses in patients that are as effective as those in animal models. 2. What this article shows: a mycobacteria protein, rRv0652, induces antigen-specific antitumor effects by triggering DC maturation, which improves the efficacy of DC-based antitumor immunotherapy. 3. A key quote from the article: “Notably, Rv0652 mediated a strong induction of Ag-specific, CD8+ class I-restricted, CTL responses, and E.G7 tumor regression in vivo.” 4. Corresponding authors: In Duk Jung and Yeong-Min Park are at the Department of Immunology, Konkuk University, South Korea.
                2015-02-24 02:41 UTC
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