Improved Anti-Tumour Adaptive Immunity Can Overcome the Melanoma Immunosuppressive Tumour Microenvironment
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cell Lines and Mice
2.2. B16 Transplantable Tumour Mouse Models
2.3. Active and Passive Immunization
2.4. Flow Cytometry
2.5. In Vitro Adaptive Immunity against Tumour Cells
2.6. Statistics
3. Results
3.1. Disseminated Pulmonary Melanoma Metastasis in Allogenic Balb/c Mice
3.2. Association of Low MHC Class I Expression with Allogenic B16 Melanoma Metastasis
3.3. Evaluation of Active and Passive Immunity in the Treatment of Allogenic B16 Melanoma Metastasis
3.4. Evaluation and Manipulation of the Tumour Microenvironment
3.5. In Vitro Adaptive Immunity-Mediated Anti-Tumour Toxicity
3.6. Th1 Versus Th2 Immune Paradigm
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Keir, M.; Butte, M.; Freeman, G.; Sharpe, A. PD-1 and Its Ligands in Tolerance and Immunity. Annu. Rev. Immunol. 2008, 26, 677–704. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Topalian, S.; Drake, C.; Pardoll, D. Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumour immunity. Curr. Opin. Immunol. 2012, 24, 207–212. [Google Scholar] [CrossRef] [PubMed]
- Mellman, I.; Coukos, G.; Dranoff, G. Cancer immunotherapy comes of age. Nature 2011, 480, 480–489. [Google Scholar] [CrossRef] [PubMed]
- Giraldo, N.A.; Sanchez-Salas, R.; Peske, J.D.; Vano, Y.; Becht, E.; Petitprez, F.; Validire, P.; Ingels, A.; Cathelineau, X.; Fridman, W.H.; et al. The clinical role of the TME in solid cancer. Br. J. Cancer 2018, 120, 45–53. [Google Scholar] [CrossRef]
- Dang, N.; Lin, Y.; Rutgeerts, O.; Sagaert, X.; Billiau, A.D.; Waer, M.; Sprangers, B. Solid tumour-induced immune regulation alters the GvHD/GvT paradigm after allogenic bone marrow transplantation. Cancer Res. 2019, 79, 2709–2721. [Google Scholar] [CrossRef]
- Valastyan, S.; Weinberg, R. Tumour Metastasis: Molecular Insights and Evolving Paradigms. Cell 2011, 147, 275–292. [Google Scholar] [CrossRef]
- Ferrone, S.; Marincola, F. Loss of HLA class I antigens by melanoma cells: Molecular mechanisms, functional significance and clinial relevance. Immunol. Today 1995, 16, 487–494. [Google Scholar] [CrossRef]
- Koopman, L.; Corver, W.; van der Slik, A.; Giphart, M.; Fleuren, G. Multiple Genetic Alterations Cause Frequent and Heterogeneous Human Histocompatibility Leukocyte Antigen Class I Loss in Cervical Cancer. J. Exp. Med. 2000, 191, 961–976. [Google Scholar] [CrossRef]
- McGranahan, N.; Rosenthal, R.; Hiley, C.T.; Rowan, A.J.; Watkins, T.B.; Wilson, G.A.; Birkbak, N.J.; Veeriah, S.; Van Loo, P.; Herrero, J.; et al. Allele-Specific HLA Loss and Immune Escape in Lung Cancer Evolution. Cell 2017, 171, 1259–1271. [Google Scholar] [CrossRef]
- Lanzavecchia, A.; Iezzi, G.; Viola, A. From TCR Engagement to T Cell Activation. Cell 1999, 96, 1–4. [Google Scholar] [CrossRef]
- Maher, J.; Davies, E. Targeting cytotoxic T lymphocytes for cancer immunotherapy. Br. J. Cancer 2004, 91, 817–821. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kawakami, Y. Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumour infiltrating lymphocytes. J. Exp. Med. 1994, 180, 347–352. [Google Scholar] [CrossRef] [PubMed]
- Germeau, C.; Ma, W.; Schiavetti, F.; Lurquin, C.; Henry, E.; Vigneron, N.; Brasseur, F.; Lethé, B.; De Plaen, E.; Velu, T.; et al. High frequency of antitumor T cells in the blood of melanoma patients before and after vaccination with tumour antigens. J. Exp. Med. 2005, 201, 241–248. [Google Scholar] [CrossRef] [PubMed]
- Milling, S.; Silvers, W.; Sai, T.; Mintz, B. Decline in MHC class I expression with increasing thickness of cutaneous melanomas in standard-strain transgenic mouse models. Melanoma Res. 2002, 12, 221–230. [Google Scholar] [CrossRef] [PubMed]
- Ashman, L.K. The immunogenicity of tumour cells. Immunol. Cell Biol. 1987, 65, 271–277. [Google Scholar] [CrossRef]
- Cole, G.; Ostrand-Rosenberg, S. Rejection of allogeneic tumour is not determined by host responses to MHC class I molecules and is mediated by CD4−CD8+ T lymphocytes that are not lytic for the tumour. Cell. Immunol. 1991, 134, 480–490. [Google Scholar] [CrossRef]
- Chaurio, R.A.; Muñoz, L.E.; Maueröder, C.; Janko, C.; Harrer, T.; Fürnrohr, B.G.; Niederweis, M.; Bilyy, R.; Schett, G.; Herrmann, M.; et al. The Progression of Cell Death Affects the Rejection of Allogeneic Tumors in Immune-Competent Mice. Front. Immunol. 2014, 5, 560. [Google Scholar] [CrossRef]
- Fu, Q.; Satterlee, A.; Wang, Y.; Wang, Y.; Wang, D.; Tang, J.; He, Z.; Liu, F. Novel murine tumour models depend on strain and route of inoculation. Int. J. Exp. Pathol. 2016, 97, 351–356. [Google Scholar] [CrossRef]
- Ashley, M.; Kotlarski, I. In vivo H-2K and H-2D antigen expression in two allogeneic mouse tumours of low immunogenicity. Immunol. Cell Biol. 1987, 65, 323–328. [Google Scholar] [CrossRef]
- Garcia-Lora, A.; Algarra, I.; Garrido, F. MHC class I antigens, immune surveillance and tumour immune escape. J. Cell. Physiol. 2003, 195, 346–355. [Google Scholar] [CrossRef]
- Antonia, S.J.; Lopez-Martin, J.A.; Bendell, J.; Ott, P.A.; Taylor, M.; Eder, J.P.; Jager, D.; Pietanza, M.C.; Le, D.T.; de Braud, F.; et al. Nivolumab alone and nivolumab plus ipilimumab in recurrent small-cell lung cancer (CheckMate 032): A multicentre, open-label, phase 1/2 trial. Lancet Oncol. 2016, 17, 883–895. [Google Scholar] [CrossRef]
- Disis, M. Oncogenic proteins as tumour antigens. Curr. Opin. Immunol. 1996, 8, 637–642. [Google Scholar] [CrossRef]
- Manning, T.C.; Rund, L.A.; Gruber, M.M.; Fallarino, F.; Gajewski, T.F.; Kranz, D.M. Antigen recognition and allogeneic tumour rejection in CD8+ TCR transgenic/RAG(-/-) mice. J. Immunol. 1997, 159, 4665–4675. [Google Scholar] [PubMed]
- Korangy, F.; Ormandy, L.A.; Bleck, J.S.; Klempnauer, J.; Wilkens, L.; Manns, M.P.; Greten, T.F. Spontaneous Tumour-Specific Humoral and Cellular Immune Responses to NY-ESO-1 in Hepatocellular Carcinoma. Clin. Cancer Res. 2004, 10, 4332–4341. [Google Scholar] [CrossRef]
- Weigelin, B.; Bolaños, E.; Teijeira, A.; Martinez-Forero, I.; Labiano, S.; Azpilikueta, A.; Morales-Kastresana, A.; Quetglas, J.I.; Wagena, E.; Sánchez-Paulete, A.R.; et al. Focusing and sustaining the antitumor CTL effector killer response by agonist anti-CD137 mAb. Proc. Natl. Acad. Sci. USA 2015, 112, 7551–7556. [Google Scholar] [CrossRef] [Green Version]
- Friedl, P.; Weigelin, B. Interstitial leukocyte migration and immune function. Nat. Immunol. 2008, 9, 960–969. [Google Scholar] [CrossRef]
- De Charette, M.; Marabelle, A.; Houot, R. Turning tumour cells into antigen presenting cells: The next step to improve cancer immunotherapy? Eur. J. Cancer 2016, 68, 134–147. [Google Scholar] [CrossRef]
- Sun, Y. Tumour microenvironment and cancer therapy resistance. Cancer Lett. 2016, 380, 205–215. [Google Scholar] [CrossRef]
- Liu, Y.; Saxena, A.; Zheng, C.; Carlsen, S.; Xiang, J. Combined alpha tumour necrosis factor gene therapy and engineered dendritic cell vaccine in combating well-established tumours. J. Gene Med. 2004, 6, 857–868. [Google Scholar] [CrossRef]
- Hsieh, C.; Pang, V.; Chen, D.; Hwang, L. Regression of Established Mouse Leukemia by GM-CSF-Transduced Tumour Vaccine: Implications for Cytotoxic T Lymphocyte Responses and Tumour Burdens. Hum. Gene Ther. 1997, 8, 1843–1854. [Google Scholar] [CrossRef]
- Perez-Diez, A.; Spiess, P.; Restifo, N.; Matzinger, P.; Marincola, F. Intensity of the Vaccine-Elicited Immune Response Determines Tumour Clearance. J. Immunol. 2002, 168, 338–347. [Google Scholar] [CrossRef] [PubMed]
- Carmi, Y.; Engleman, E. Tumour-binding antibodies and tumour immunity. Oncotarget 2015, 6, 35129–35130. [Google Scholar] [CrossRef] [PubMed]
- Carmi, Y.; Spitzer, M.H.; Linde, I.L.; Burt, B.M.; Prestwood, T.R.; Perlman, N.; Davidson, M.G.; Kenkel, J.A.; Segal, E.; Pusapati, G.V.; et al. Allogeneic IgG combined with dendritic cell stimuli induce antitumour T-cell immunity. Nature 2015, 521, 99–104. [Google Scholar] [CrossRef] [PubMed]
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Dang, N.; Waer, M.; Sprangers, B.; Lin, Y. Improved Anti-Tumour Adaptive Immunity Can Overcome the Melanoma Immunosuppressive Tumour Microenvironment. Cancers 2019, 11, 1694. https://doi.org/10.3390/cancers11111694
Dang N, Waer M, Sprangers B, Lin Y. Improved Anti-Tumour Adaptive Immunity Can Overcome the Melanoma Immunosuppressive Tumour Microenvironment. Cancers. 2019; 11(11):1694. https://doi.org/10.3390/cancers11111694
Chicago/Turabian StyleDang, Nana, Mark Waer, Ben Sprangers, and Yuan Lin. 2019. "Improved Anti-Tumour Adaptive Immunity Can Overcome the Melanoma Immunosuppressive Tumour Microenvironment" Cancers 11, no. 11: 1694. https://doi.org/10.3390/cancers11111694