TY - JOUR
T1 - Modulating tumor immunity using advanced microbiome therapeutics producing an indole metabolite
AU - Vaaben, Troels Holger
AU - Lützhøft, Ditte Olsen
AU - Koulouktsis, Andreas
AU - Dawoodi, Ida Melisa
AU - Stavnsbjerg, Camilla
AU - Kvich, Lasse
AU - Gögenur, Ismail
AU - Vazquez-Uribe, Ruben
AU - Sommer, Morten Otto Alexander
N1 - © 2025. The Author(s).
PY - 2025/4
Y1 - 2025/4
N2 - The gut microbiome has emerged as a key player in modulating immune responses against cancer, suggesting that microbial interventions can enhance treatment outcomes. Indole metabolites produced by probiotic bacteria activate the aryl hydrocarbon receptor (AhR), a transcription factor important for immune cell regulation. Cancer patients with high plasma concentrations of these metabolites have shown improved survival. Building on these findings, we have engineered Escherichia coli Nissle 1917 to produce the AhR agonist indole-3-acetic acid. Delivery of indole-3-acetic acid by tumor-colonizing bacteria changes the tumor microenvironment in a murine model, significantly increasing levels of CXCL9 and IFN-γ and elevating tumor-infiltrating T-cell abundance and activation. Treatment with our engineered strain inhibits tumor growth, improves survival in syngeneic tumor models, and leads to long-lasting immunity in a tumor rechallenge experiment. Further investigation indicates that this immune modulation is driven by the direct activation of AhR by indole-3-acetic acid, leading to differential cytokine expression and a shift in immune cell composition within the tumor. This study highlights the importance of microbial metabolites in immune modulation and supports exploring microbiome-based therapies in oncology.
AB - The gut microbiome has emerged as a key player in modulating immune responses against cancer, suggesting that microbial interventions can enhance treatment outcomes. Indole metabolites produced by probiotic bacteria activate the aryl hydrocarbon receptor (AhR), a transcription factor important for immune cell regulation. Cancer patients with high plasma concentrations of these metabolites have shown improved survival. Building on these findings, we have engineered Escherichia coli Nissle 1917 to produce the AhR agonist indole-3-acetic acid. Delivery of indole-3-acetic acid by tumor-colonizing bacteria changes the tumor microenvironment in a murine model, significantly increasing levels of CXCL9 and IFN-γ and elevating tumor-infiltrating T-cell abundance and activation. Treatment with our engineered strain inhibits tumor growth, improves survival in syngeneic tumor models, and leads to long-lasting immunity in a tumor rechallenge experiment. Further investigation indicates that this immune modulation is driven by the direct activation of AhR by indole-3-acetic acid, leading to differential cytokine expression and a shift in immune cell composition within the tumor. This study highlights the importance of microbial metabolites in immune modulation and supports exploring microbiome-based therapies in oncology.
KW - Animals
KW - Cell Line, Tumor
KW - Escherichia coli/metabolism
KW - Female
KW - Gastrointestinal Microbiome
KW - Humans
KW - Indoleacetic Acids/metabolism
KW - Indoles/metabolism
KW - Mice
KW - Mice, Inbred C57BL
KW - Microbiota
KW - Neoplasms/immunology
KW - Probiotics
KW - Receptors, Aryl Hydrocarbon/agonists
KW - Tumor Microenvironment/drug effects
KW - Microbiome Therapeutics
KW - Tumor Immunomodulation
KW - Aryl Hydrocarbon Receptor
KW - Synthetic Biology
KW - Indole-3-Acetic Acid
UR - https://www.scopus.com/pages/publications/105000070277
U2 - 10.1038/s44319-025-00386-9
DO - 10.1038/s44319-025-00386-9
M3 - Journal article
C2 - 40055466
SN - 1469-221X
VL - 26
SP - 1688
EP - 1708
JO - EMBO Reports
JF - EMBO Reports
IS - 7
ER -