STING activation normalizes the intraperitoneal vascular-immune microenvironment and suppresses peritoneal carcinomatosis of colon cancer
Open accessAbstract
Background: Peritoneal carcinomatosis is a fatal clinical presentation of colon cancer, characterized by unresponsiveness to conventional anticancer therapies, including immune checkpoint inhibitors. Here, we elucidated the immune-evasion mechanisms during the peritoneal carcinomatosis of colon cancer and developed a novel immunotherapy by activating the stimulator of interferon genes (STING) pathway. Methods: We generated a syngeneic peritoneal carcinomatosis model of colon cancer. Mice were intraperitoneally treated with either STING agonist (MIW815, also known as ADU-S100) or PD-1 blockade or both. The tumor microenvironment was comprehensively analyzed using multiplexed immunofluorescence imaging, flow cytometry, and NanoString immune profiling. Results: Intraperitoneal colon cancer cells induce a massive influx of immunosuppressive M2-like macrophages, upregulate immune checkpoints, and impair effector T cell functions during peritoneal dissemination; these collectively create a highly angiogenic and immunosuppressive milieu that is resistant to anti-PD-1 monotherapy. Intraperitoneal administration of a STING agonist suppressed aberrant angiogenesis, increased pericyte coverage, and normalized tumor vessels, thereby facilitating the infiltration of activated CD8 + T cells into peritoneal tumor nodules. Moreover, STING activation reprogramed tumor-associated macrophages toward the M1 phenotype. STING activation converted immunologically cold peritoneal tumors into T-cell-inflamed tumors in a type-I interferon-dependent manner. Lastly, the STING agonist synergistically cooperated with PD-1 and/or COX2 blockade to further suppress the peritoneal dissemination of colon cancer, resulting in complete eradication of tumor and ascites, and inducing durable antitumor immunity. Conclusions: STING activation can normalize the peritoneal vascular and immune microenvironment, providing a rationale for a novel combination therapeutic strategy for peritoneal carcinomatosis in colon cancer.
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Accumulating evidence indicates that chemotherapy, radiotherapy, angiogenesis inhibitor, STING agonist, FMT, epigenetic modulators, or other immunomodulators could synergize α-PD-1/PD-L1, by enhancing cancer antigen release, APC function, or effector activity.
“Accumulating evidence indicates that chemotherapy, radiotherapy, angiogenesis inhibitor, stimulator of interferon genes (STING) agonist, fecal microbiota transplantation (FMT), epigenetic modulators, or other immunomodulators could synergize α-PD-1/PD-L1, by enhancing cancer antigen release, APC function, or effector activity [22–31].”
From Combination strategies with PD-1/PD-L1 blockade: current advances and future directions (2022) · cites this paper as [25]
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- Authors
- Lee, S. J., Yang, H., Kim, W. R., Lee, Y. S., Lee, W. S., Kong, S. J., Lee, H. J., Kim, J. H., Cheon, J., Kang, B., Chon, H. J., & Kim, C.
- Affiliations
- CHA University (KR)
- CHA University Bundang Medical Center (KR)
- Corresponding author
- Chon, Hong Jae
- Kim, Chan
- ORCID
- Venue
- Journal for ImmunoTherapy of Cancer
- Publisher
- BMJ
- Published
- 2021-06
- Volume
- 9
- Issue
- 6
- Pages
- e002195
- ISSN
- 2051-1426 (ISSN-L)
- PMC
- PMC8215239
- OpenAlex
- W3168539558
- Cited by
- 118
- References
- 50
- Citations by year
- 2026: 24 · 2025: 23 · 2024: 24 · 2023: 24 · 2022: 19 · 2021: 4
- FWCI
- 6.47
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal for ImmunoTherapy of Cancer (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Korea Medical Device Development Fund (202012D21-01)
- National Research Foundation of Korea (NRF-2020R1A2C2004530, NRF-2020R1C1C1010722)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Health Sciences › Medicine › Surgery › Intraperitoneal and Appendiceal Malignancies
- Keywords
- STING activation, peritoneal carcinomatosis, colon cancer, vascular normalization, tumor microenvironment, M2 macrophages, M1 macrophage polarization, anti-PD-1 therapy, type I interferon, angiogenesis, pericyte coverage, CD8+ T cell infiltration, immune evasion, immunotherapy
- MeSH terms
- STING Protein, Animals, Colonic Neoplasms, Disease Models, Animal, Humans, Immunotherapy, Membrane Proteins, Peritoneal Neoplasms, Cell Line, Tumor, Mice, Tumor Microenvironment
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