Intra-tumoral delivery of CXCL11 via a vaccinia virus, but not by modified T cells, enhances the efficacy of adoptive T cell therapy and vaccines

Moon, Edmund K.; Wang, Liang-Chuan S.; Bekdache, Kheng; Lynn, Rachel C.; Lo, Albert; Thorne, Stephen H.; Albelda, Steven M.

doi:10.1080/2162402x.2017.1395997

Cited by 174Chemokine receptors and signalingImmunotherapy and Immune ResponsesVirus-based gene therapy research

Intra-tumoral delivery of CXCL11 via a vaccinia virus, but not by modified T cells, enhances the efficacy of adoptive T cell therapy and vaccines

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Moon, Edmund K., Wang, Liang-Chuan S., Bekdache, Kheng, Lynn, Rachel C., Lo, Albert, Thorne, Stephen H., Albelda, Steven M.·2018·OncoImmunology

DOI 10.1080/2162402x.2017.1395997PMC PMC5790399

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Abstract

T cell trafficking into tumors depends on a "match" between chemokine receptors on effector cells (e.g., CXCR3 and CCR5) and tumor-secreted chemokines. There is often a chemokine/chemokine receptor "mismatch", with tumors producing minute amounts of chemokines, resulting in inefficient targeting of effectors to tumors. We aimed to alter tumors to produce higher levels of CXCL11, a CXCR3 ligand, to attract more effector cells following immunotherapy. Mice bearing established subcutaneous tumors were studied. In our first approach, we used modified chimeric antigen receptor (CAR)-transduced human T cells to deliver CXCL11 (CAR/CXCL11) into tumors. In our second approach, we intravenously (iv) administered a modified oncolytic vaccinia virus (VV) engineered to produce CXCL11 (VV.CXCL11). The effect of these treatments on T cell trafficking into the tumors and anti-tumor efficacy after subsequent CAR T cell injections or anti-tumor vaccines was determined. CAR/CXCL11 and VV.CXCL11 significantly increased CXCL11 protein levels within tumors. For CAR/CXCL11, injection of a subsequent dose of CAR T cells did not result in increased intra-tumoral trafficking, and appeared to decrease the function of the injected CAR T cells. In contrast, VV.CXCL11 increased the number of total and antigen-specific T cells within tumors after CAR T cell injection or vaccination and significantly enhanced anti-tumor efficacy. Both approaches were successful in increasing CXCL11 levels within the tumors; however, only the vaccinia approach was successful in recruiting T cells and augmenting anti-tumor efficacy. VV.CXCL11 should be considered as a potential approach to augment adoptive T cell transfer or vaccine immunotherapy.

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The CXCL9/10/11-CXCR3 pathway is well known for recruiting and activating cytotoxic T cells.
“The relevance of the CXCL9/10/11-CXCR3 pathway for recruiting and triggering cytotoxic T cells is well known (47-50,64).”
From Exercise Training Improves Tumor Control by Increasing CD8+ T-cell Infiltration via CXCR3 Signaling and Sensitizes Breast Cancer to Immune Checkpoint Blockade (2021) · cites this paper as [49]
Radiation, chemotherapy, and vaccination are among approaches tested to exploit this pathway for attracting more CD8+ T cells.
“Several therapeutic approaches have been tested to leverage this pathway to attract more CD8+ T cells, including radiation, chemotherapy (50), and vaccination (49).”
From Exercise Training Improves Tumor Control by Increasing CD8+ T-cell Infiltration via CXCR3 Signaling and Sensitizes Breast Cancer to Immune Checkpoint Blockade (2021) · cites this paper as [49]

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Authors: Moon, E. K., Wang, L.-C. S., Bekdache, K., Lynn, R. C., Lo, A., Thorne, S. H., & Albelda, S. M.
Affiliations: University of Pennsylvania (US)
University of Pittsburgh (US)
,
ORCID: Moon, Edmund K.
Lynn, Rachel C.
Lo, Albert
Thorne, Stephen H.
Venue: OncoImmunology
Publisher: Informa UK Limited
Published: 2018-01-09
Volume: 7
Issue: 3
Pages: e1395997-e1395997
ISSN: 2162-4011 (ISSN-L)
2162-402X
DOI: 10.1080/2162402x.2017.1395997
PMC: PMC5790399
OpenAlex: W2780294317
Cited by: 174
References: 49
Citations by year: 2026: 19 · 2025: 22 · 2024: 17 · 2023: 21 · 2022: 24 · 2021: 28 · 2020: 27 · 2019: 12 · 2018: 4
FWCI: 5.18
Type: journal article
Language: en
Open access: gold
doi.org
Locations: OncoImmunology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: NCI/NIH (P01 CA66726)
Topics: Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
Keywords: CXCL11, oncolytic vaccinia virus, chimeric antigen receptor T cells, adoptive T cell therapy, cancer vaccines, T cell migration, CXCR3, antitumor immunity

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Intra-tumoral delivery of CXCL11 via a vaccinia virus, but not by modified T cells, enhances the efficacy of adoptive T cell therapy and vaccines

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