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Volume 21
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10.3390/ijms21072573
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Article

Sublethal Radiation Affects Antigen Processing and Presentation Genes to Enhance Immunogenicity of Cancer Cells

by
Achamaporn Punnanitinont
1,
Eric D. Kannisto
1,
Junko Matsuzaki
2,
Kunle Odunsi
2,
Sai Yendamuri
1,
Anurag K. Singh
3,* and
Santosh K. Patnaik
1,*
1
Department of Thoracic Surgery, Roswell Park Comprehensive Cancer Center, Elm and Carlton Streets, Buffalo, NY 14263, USA
2
Department of Gynecologic Oncology, and Center for Cancer Immunotherapy, Roswell Park Comprehensive Cancer Center, Elm and Carlton Streets, Buffalo, NY 14263, USA
3
Department of Radiation Medicine, Roswell Park Comprehensive Cancer Center, Elm and Carlton Streets, Buffalo, NY 14263, USA
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2020, 21(7), 2573; https://doi.org/10.3390/ijms21072573
Submission received: 11 March 2020 / Revised: 4 April 2020 / Accepted: 6 April 2020 / Published: 7 April 2020
(This article belongs to the Special Issue Radiation in Multimodal Tumor Immune Therapies – Mechanisms and Application)
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Abstract

While immunotherapy in cancer is designed to stimulate effector T cell response, tumor-associated antigens have to be presented on malignant cells at a sufficient level for recognition of cancer by T cells. Recent studies suggest that radiotherapy enhances the anti-cancer immune response and also improves the efficacy of immunotherapy. To understand the molecular basis of such observations, we examined the effect of ionizing X-rays on tumor antigens and their presentation in a set of nine human cell lines representing cancers of the esophagus, lung, and head and neck. A single dose of 7.5 or 15 Gy radiation enhanced the New York esophageal squamous cell carcinoma 1 (NY-ESO-1) tumor-antigen-mediated recognition of cancer cells by NY-ESO-1-specific CD8+ T cells. Irradiation led to significant enlargement of live cells after four days, and microscopy and flow cytometry revealed multinucleation and polyploidy in the cells because of dysregulated mitosis, which was also revealed in RNA-sequencing-based transcriptome profiles of cells. Transcriptome analyses also showed that while radiation had no universal effect on genes encoding tumor antigens, it upregulated the expression of numerous genes involved in antigen processing and presentation pathways in all cell lines. This effect may explain the immunostimulatory role of cancer radiotherapy.
Keywords: antigen presentation; cancer cell line; gene expression; lung cancer; head and neck cancer; radiation; tumor antigen antigen presentation; cancer cell line; gene expression; lung cancer; head and neck cancer; radiation; tumor antigen

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MDPI and ACS Style

Punnanitinont, A.; Kannisto, E.D.; Matsuzaki, J.; Odunsi, K.; Yendamuri, S.; Singh, A.K.; Patnaik, S.K. Sublethal Radiation Affects Antigen Processing and Presentation Genes to Enhance Immunogenicity of Cancer Cells. Int. J. Mol. Sci. 2020, 21, 2573. https://doi.org/10.3390/ijms21072573

AMA Style

Punnanitinont A, Kannisto ED, Matsuzaki J, Odunsi K, Yendamuri S, Singh AK, Patnaik SK. Sublethal Radiation Affects Antigen Processing and Presentation Genes to Enhance Immunogenicity of Cancer Cells. International Journal of Molecular Sciences. 2020; 21(7):2573. https://doi.org/10.3390/ijms21072573

Chicago/Turabian Style

Punnanitinont, Achamaporn, Eric D. Kannisto, Junko Matsuzaki, Kunle Odunsi, Sai Yendamuri, Anurag K. Singh, and Santosh K. Patnaik. 2020. "Sublethal Radiation Affects Antigen Processing and Presentation Genes to Enhance Immunogenicity of Cancer Cells" International Journal of Molecular Sciences 21, no. 7: 2573. https://doi.org/10.3390/ijms21072573

APA Style

Punnanitinont, A., Kannisto, E. D., Matsuzaki, J., Odunsi, K., Yendamuri, S., Singh, A. K., & Patnaik, S. K. (2020). Sublethal Radiation Affects Antigen Processing and Presentation Genes to Enhance Immunogenicity of Cancer Cells. International Journal of Molecular Sciences, 21(7), 2573. https://doi.org/10.3390/ijms21072573

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