Open Access
Open access

Intracellular Salmonella delivery of an exogenous immunization antigen refocuses CD8 T cells against cancer cells, eliminates pancreatic tumors and forms antitumor immunity

Vishnu Raman 1, 2
Lars M Howell 1
Shoshana M. K. Bloom 1
Christopher L Hall 1, 2
Victoria E Wetherby 2
Lisa M. Minter 3, 4, 5
Ashish A Kulkarni 1, 5
Neil S Forbes 1, 3, 5
Publication typeJournal Article
Publication date2023-10-05
scimago Q1
wos Q1
SJR1.941
CiteScore10.8
Impact factor5.9
ISSN16643224
Immunology
Immunology and Allergy
Abstract
Introduction

Immunotherapies have shown great promise, but are not effective for all tumors types and are effective in less than 3% of patients with pancreatic ductal adenocarcinomas (PDAC). To make an immune treatment that is effective for more cancer patients and those with PDAC specifically, we genetically engineered Salmonella to deliver exogenous antigens directly into the cytoplasm of tumor cells. We hypothesized that intracellular delivery of an exogenous immunization antigen would activate antigen-specific CD8 T cells and reduce tumors in immunized mice.

Methods

To test this hypothesis, we administered intracellular delivering (ID) Salmonella that deliver ovalbumin as a model antigen into tumor-bearing, ovalbumin-vaccinated mice. ID Salmonella delivers antigens by autonomously lysing in cells after the induction of cell invasion.

Results

We showed that the delivered ovalbumin disperses throughout the cytoplasm of cells in culture and in tumors. This delivery into the cytoplasm is essential for antigen cross-presentation. We showed that co-culture of ovalbumin-recipient cancer cells with ovalbumin-specific CD8 T cells triggered a cytotoxic T cell response. After the adoptive transfer of OT-I CD8 T cells, intracellular delivery of ovalbumin reduced tumor growth and eliminated tumors. This effect was dependent on the presence of the ovalbumin-specific T cells. Following vaccination with the exogenous antigen in mice, intracellular delivery of the antigen cleared 43% of established KPC pancreatic tumors, increased survival, and prevented tumor re-implantation.

Discussion

This response in the immunosuppressive KPC model demonstrates the potential to treat tumors that do not respond to checkpoint inhibitors, and the response to re-challenge indicates that new immunity was established against intrinsic tumor antigens. In the clinic, ID Salmonella could be used to deliver a protein antigen from a childhood immunization to refocus pre-existing T cell immunity against tumors. As an off-the-shelf immunotherapy, this bacterial system has the potential to be effective in a broad range of cancer patients.

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GOST Copy
Raman V. et al. Intracellular Salmonella delivery of an exogenous immunization antigen refocuses CD8 T cells against cancer cells, eliminates pancreatic tumors and forms antitumor immunity // Frontiers in Immunology. 2023. Vol. 14.
GOST all authors (up to 50) Copy
Raman V., Howell L. M., Bloom S. M. K., Hall C. L., Wetherby V. E., Minter L. M., Kulkarni A. A., Forbes N. S. Intracellular Salmonella delivery of an exogenous immunization antigen refocuses CD8 T cells against cancer cells, eliminates pancreatic tumors and forms antitumor immunity // Frontiers in Immunology. 2023. Vol. 14.
RIS |
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RIS Copy
TY - JOUR
DO - 10.3389/fimmu.2023.1228532
UR - https://doi.org/10.3389/fimmu.2023.1228532
TI - Intracellular Salmonella delivery of an exogenous immunization antigen refocuses CD8 T cells against cancer cells, eliminates pancreatic tumors and forms antitumor immunity
T2 - Frontiers in Immunology
AU - Raman, Vishnu
AU - Howell, Lars M
AU - Bloom, Shoshana M. K.
AU - Hall, Christopher L
AU - Wetherby, Victoria E
AU - Minter, Lisa M.
AU - Kulkarni, Ashish A
AU - Forbes, Neil S
PY - 2023
DA - 2023/10/05
PB - Frontiers Media S.A.
VL - 14
PMID - 37868996
SN - 1664-3224
ER -
BibTex
Cite this
BibTex (up to 50 authors) Copy
@article{2023_Raman,
author = {Vishnu Raman and Lars M Howell and Shoshana M. K. Bloom and Christopher L Hall and Victoria E Wetherby and Lisa M. Minter and Ashish A Kulkarni and Neil S Forbes},
title = {Intracellular Salmonella delivery of an exogenous immunization antigen refocuses CD8 T cells against cancer cells, eliminates pancreatic tumors and forms antitumor immunity},
journal = {Frontiers in Immunology},
year = {2023},
volume = {14},
publisher = {Frontiers Media S.A.},
month = {oct},
url = {https://doi.org/10.3389/fimmu.2023.1228532},
doi = {10.3389/fimmu.2023.1228532}
}