TREM2 deficiency reprograms intestinal macrophages and microbiota to enhance anti–PD-1 tumor immunotherapy
Open accessAbstract
The gut microbiota and tumor-associated macrophages (TAMs) affect tumor responses to anti–programmed cell death protein 1 (PD-1) immune checkpoint blockade. Reprogramming TAM by either blocking or deleting the macrophage receptor triggering receptor on myeloid cells 2 (TREM2) attenuates tumor growth, and lack of functional TREM2 enhances tumor elimination by anti–PD-1. Here, we found that anti–PD-1 treatment combined with TREM2 deficiency in mice induces proinflammatory programs in intestinal macrophages and a concomitant expansion of Ruminococcus gnavus in the gut microbiota. Gavage of wild-type mice with R. gnavus enhanced anti–PD-1–mediated tumor elimination, recapitulating the effect occurring in the absence of TREM2. A proinflammatory intestinal environment coincided with expansion, increased circulation, and migration of TNF-producing CD4 + T cells to the tumor bed. Thus, TREM2 remotely controls anti–PD-1 immune checkpoint blockade through modulation of the intestinal immune environment and microbiota, with R. gnavus emerging as a potential probiotic agent for increasing responsiveness to anti-PD-1.
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Migration of immune cells from the gut to the tumor mediates gut microbiota effects on extraintestinal tumors.
“the migration of immune cells from the gut to the tumor 39,63,64”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [64]
Gut dysbiosis can cause regulatory enterotropic immune cells to migrate to the tumor microenvironment.
“Gut dysbiosis can induce emigration of regulatory enterotropic immunocytes to the tumor microenvironment, as shown using mice expressing a photoconvertible fluorescent protein (Kaede or Kikume green-red (KikGR)).”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [64]
Macrophages and B and T cell subsets move from the gut to the tumor microenvironment by disrupting α4β7-MAdCAM-1 interactions or via migration-stimulatory factors such as CXCR3, CCL2, or S1PR.
“Macrophages and B cell and T cell subsets emigrate from the gut to the tumor microenvironment through the disruption of α 4 β 7 -MAdCAM-1 interactions or migration-stimulatory factors including CXCR3, CCL2 or S1PR.”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [64]
TREM2 blockade increased pro-inflammatory macrophages in the lamina propria, leading to dominance of Mediterraneibacter gnavus and migration of TNF+ CD4+ T cells into tumors.
“TREM2 blockade increased pro-inflammatory macrophages in the lamina propria, culminating in the relative dominance of Mediterraneibacter gnavus and the emigration of TNF + CD4 + T cells into tumors 64 .”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [64]
Gut dysbiosis can cause regulatory enterotropic immunocytes to emigrate to the tumor microenvironment.
“Gut dysbiosis can induce emigration of regulatory enterotropic immunocytes to the tumor microenvironment, as shown using mice expressing a photoconvertible fluorescent protein (Kaede or Kikume green-red (KikGR)).”
From Impact of the ONCOBIOME network in cancer microbiome research (2025) · cites this paper as [64]
Bacteroides ovatus, Prevotella copri, Ruminococcus gnavus, and Clostridium symbiosum are negatively correlated with immune checkpoint blockade efficacy in certain contexts, despite associations with positive outcomes with chemotherapy or other monoclonal antibody therapies in other studies.
“Similarly, Bacteroides ovatus, Prevotella copri (renamed Segatella copri), Ruminococcus gnavus (renamed Mediterraneibacter gnavus), and Clostridiumsymbiosum are negatively correlated with ICB efficacy in certain contexts, despite associations with positive outcomes with chemotherapy or other monoclonal antibody therapies in other studies (Di Luccia et al., 2024; Peters et al., 2019; Routy et al.,”
From Microbiota-centered interventions to boost immune checkpoint blockade therapies (2025) · cites this paper as Di Luccia et al., 2024
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- Authors
- Di Luccia, B., Molgora, M., Khantakova, D., Jaeger, N., Chang, H.-W., Czepielewski, R. S., Helmink, B. A., Onufer, E. J., Fachi, J. L., Bhattarai, B., Trsan, T., Rodrigues, P. F., Hou, J., Bando, J. K., da Silva, C. S., Cella, M., Gilfillan, S., Schreiber, R. D., Gordon, J. I., & Colonna, M.
- Affiliations
- Department of Pathology and Immunology, Washington University School of Medicine in Saint Louis, St. Louis, MO 63110, USA.
- Washington University in St. Louis (US)
- Corresponding author
- Molgora, Martina
- Khantakova, Darya
- Colonna, Marco
- ORCID
- Di Luccia, Blanda
- Molgora, Martina
- Khantakova, Darya
- Jaeger, Natalia
- Chang, Hao-Wei
- Czepielewski, Rafael S.
- Helmink, Beth A.
- Onufer, Emily J.
- Fachi, José L.
- Bhattarai, Bishan
- Trsan, Tihana
- Rodrigues, Patrick F.
- Hou, JinChao
- Bando, Jennifer K.
- da Silva, Cristiane Sécca
- Cella, Marina
- Gilfillan, Susan
- Schreiber, Robert D.
- Gordon, Jeffrey I.
- Colonna, Marco
- Venue
- Science Immunology
- Published
- 2024-05-17
- Volume
- 9
- Issue
- 95
- Pages
- eadi5374-eadi5374
- ISSN
- 2470-9468 (ISSN-L)
- PMC
- PMC11299520
- OpenAlex
- W4397023331
- Cited by
- 59
- References
- 32
- Citations by year
- 2026: 28 · 2025: 27 · 2024: 4
- FWCI
- 10.04
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science Immunology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Cancer Research Institute
- American Gastroenterological Association
- Crohn's and Colitis Foundation (938100)
- National Institutes of Health (UL1TR002345)
- National Cancer Institute (P30CA091842, R01CA262684)
- National Institute of Diabetes and Digestive and Kidney Diseases (R00DK118110, P30DK056341, R01DK030292, R01DK119147)
- National Center for Advancing Translational Sciences
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- TREM2, tumor-associated macrophages, intestinal macrophages, gut microbiota, Ruminococcus gnavus, anti-PD-1 therapy, immune checkpoint blockade, cancer immunotherapy, CD4+ T cells, TNF-α, probiotics, macrophage reprogramming
- MeSH terms
- Gastrointestinal Microbiome, Immune Checkpoint Inhibitors, Animals, Immunotherapy, Intestines, Macrophages, Membrane Glycoproteins, Mice, Inbred C57BL, Receptors, Immunologic, Mice, Knockout, Mice, Programmed Cell Death 1 Receptor
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