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Mast cell‐dependent CD8+ T‐cell recruitment mediates immune surveillance of intestinal tumors in ApcMin/+ mice

Bodduluri, Sobha R., Mathis, Steven, Maturu, Paramahamsa, Krishnan, Elangovan, Satpathy, Shuchismita R., Chilton, Paula M., Mitchell, Thomas C., Lira, Sergio, Locati, Massimo, Mantovani, Alberto, Jala, Venkatakrishna R., Haribabu, Bodduluri·2018·Cancer Immunology Research
DOI 10.1158/2326-6066.cir-17-0424PMC PMC9580996

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Abstract

The presence of mast cells in some human colorectal cancers is a positive prognostic factor, but the basis for this association is incompletely understood. Here, we found that mice with a heterozygous mutation in the adenomatous polyposis coli gene (ApcMin/+) displayed reduced intestinal tumor burdens and increased survival in a chemokine decoy receptor, ACKR2-null background, which led to discovery of a critical role for mast cells in tumor defense. ACKR2–/–ApcMin/+ tumors showed increased infiltration of mast cells, their survival advantage was lost in mast cell–deficient ACKR2–/–SA–/–ApcMin/+ mice as the tumors grew rapidly, and adoptive transfer of mast cells restored control of tumor growth. Mast cells from ACKR2–/– mice showed elevated CCR2 and CCR5 expression and were also efficient in antigen presentation and activation of CD8+ T cells. Mast cell–derived leukotriene B4 (LTB4) was found to be required for CD8+ T lymphocyte recruitment, as mice lacking the LTB4 receptor (ACKR2–/–BLT1–/–ApcMin/+) were highly susceptible to intestinal tumor-induced mortality. Taken together, these data demonstrate that chemokine-mediated recruitment of mast cells is essential for initiating LTB4/BLT1-regulated CD8+ T-cell homing and generation of effective antitumor immunity against intestinal tumors. We speculate that the pathway reported here underlies the positive prognostic significance of mast cells in selected human tumors. Cancer Immunol Res; 6(3); 332–47. ©2018 AACR.

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Metadata

Authors
Bodduluri, S. R., Mathis, S., Maturu, P., Krishnan, E., Satpathy, S. R., Chilton, P. M., Mitchell, T. C., Lira, S., Locati, M., Mantovani, A., Jala, V. R., & Haribabu, B.
Affiliations
  • 1James Graham Brown Cancer Center, University of Louisville Health Sciences Center, Louisville, Kentucky.
  • 2Department of Microbiology and Immunology, University of Louisville Health Sciences Center, Louisville, Kentucky.
  • 4Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, New York.
  • 5Humanitas Clinical and Research Center, University of Milan, Milan, Italy.
Venue
Cancer Immunology Research
Publisher
American Association for Cancer Research (AACR)
Published
2018-02-28
Volume
6
Issue
3
Pages
332-347
ISSN
  • 2326-6066
  • 2326-6074
DOI
10.1158/2326-6066.cir-17-0424
PMC
PMC9580996
Cited by
45
References
1
Language
en
Funders
  • HHS | NIH | National Cancer Institute (NCI) (CA-138623)
  • HHS | NIH | National Center for Research Resources (NCRR) (P20RR018733, P20RR016481)

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