Microbial metabolites and immunotherapy: Basic rationale and clinical indications

Seminars in Immunology - Tập 67 - Trang 101755 - 2023
Larisa V. Kovtonyuk1, Kathy D. McCoy1
1Department of Physiology & Pharmacology, Calvin, Phoebe and Joan Snyder Institute for Chronic Diseases, Cumming School of Medicine, University of Calgary, Calgary, AB T2N 4A1, Canada

Tài liệu tham khảo

Belkaid, 2017, Homeostatic Immunity and the Microbiota, Immunity, 46, 562, 10.1016/j.immuni.2017.04.008 Cullin, 2021, Microbiome and cancer, Cancer Cell, 39, 1317, 10.1016/j.ccell.2021.08.006 Gopalakrishnan, 2018, Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients, Science, 359, 97, 10.1126/science.aan4236 Matson, 2018, The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients, Science, 359, 104, 10.1126/science.aao3290 Routy, 2018, Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors, Science, 359, 91, 10.1126/science.aan3706 Baruch, 2021, Fecal microbiota transplant promotes response in immunotherapy-refractory melanoma patients, Science, 371, 602, 10.1126/science.abb5920 Davar, 2021, Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients, Science, 371, 595, 10.1126/science.abf3363 Helmink, 2019, The microbiome, cancer, and cancer therapy, Nat. Med, 25, 377, 10.1038/s41591-019-0377-7 Capietto, 2017, Characterizing neoantigens for personalized cancer immunotherapy, Curr. Opin. Immunol., 46, 58, 10.1016/j.coi.2017.04.007 Yi, 2018, The role of neoantigen in immune checkpoint blockade therapy, Exp. Hematol. Oncol., 7, 28, 10.1186/s40164-018-0120-y Kim, 2016, Immune escape to PD-L1/PD-1 blockade: seven steps to success (or failure), Ann. Oncol., 27, 1492, 10.1093/annonc/mdw217 Schreiber, 2011, Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion, Science, 331, 1565, 10.1126/science.1203486 Mariathasan, 2018, TGFbeta attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells, Nature, 554, 544, 10.1038/nature25501 Sivan, 2015, Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy, Science, 350, 1084, 10.1126/science.aac4255 Vetizou, 2015, Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota, Science, 350, 1079, 10.1126/science.aad1329 Andrews, 2021, Gut microbiota signatures are associated with toxicity to combined CTLA-4 and PD-1 blockade, Nat. Med, 27, 1432, 10.1038/s41591-021-01406-6 Masetti, 2021, Microbiome-derived metabolites in allogeneic hematopoietic stem cell transplantation, Int J. Mol. Sci., 22, 10.3390/ijms22031197 Shono, 2018, Gut microbiota injury in allogeneic haematopoietic stem cell transplantation, Nat. Rev. Cancer, 18, 283, 10.1038/nrc.2018.10 Iida, 2013, Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment, Science, 342, 967, 10.1126/science.1240527 Pflug, 2016, Efficacy of antineoplastic treatment is associated with the use of antibiotics that modulate intestinal microbiota, Oncoimmunology, 5, 10.1080/2162402X.2016.1150399 Smith, 2022, Gut microbiome correlates of response and toxicity following anti-CD19 CAR T cell therapy, Nat. Med, 28, 713, 10.1038/s41591-022-01702-9 Mager, 2020, Microbiome-derived inosine modulates response to checkpoint inhibitor immunotherapy, Science, 369, 1481, 10.1126/science.abc3421 Renga, 2022, Optimizing therapeutic outcomes of immune checkpoint blockade by a microbial tryptophan metabolite, J. Immunother. Cancer, 10, 10.1136/jitc-2021-003725 He, 2021, Gut microbial metabolites facilitate anticancer therapy efficacy by modulating cytotoxic CD8(+) T cell immunity, Cell Metab., 33, 988, 10.1016/j.cmet.2021.03.002 Lam, 2021, Microbiota triggers STING-type I IFN-dependent monocyte reprogramming of the tumor microenvironment, Cell, 184, 5338, 10.1016/j.cell.2021.09.019 Luu, 2021, Microbial short-chain fatty acids modulate CD8(+) T cell responses and improve adoptive immunotherapy for cancer, Nat. Commun., 12, 4077, 10.1038/s41467-021-24331-1 Bishai, 2021, Small molecule metabolites at the host-microbiota interface, J. Immunol., 207, 1725, 10.4049/jimmunol.2100528 Twomey, 2021, Cancer immunotherapy update: FDA-Approved checkpoint inhibitors and companion diagnostics, AAPS J., 23, 39, 10.1208/s12248-021-00574-0 Welihinda, 2018, Enhancement of inosine-mediated A2AR signaling through positive allosteric modulation, Cell Signal, 42, 227, 10.1016/j.cellsig.2017.11.002 Hasko, 2000, Inosine inhibits inflammatory cytokine production by a posttranscriptional mechanism and protects against endotoxin-induced shock, J. Immunol., 164, 1013, 10.4049/jimmunol.164.2.1013 Liaudet, 2002, Inosine exerts a broad range of antiinflammatory effects in a murine model of acute lung injury, Ann. Surg., 235, 568, 10.1097/00000658-200204000-00016 Mabley, 2003, Inosine reduces inflammation and improves survival in a murine model of colitis, Am. J. Physiol. Gastrointest. Liver Physiol., 284, G138, 10.1152/ajpgi.00060.2002 Azambuja, 2019, Inhibition of the adenosinergic pathway in cancer rejuvenates innate and adaptive immunity, Int J. Mol. Sci., 20, 10.3390/ijms20225698 Leone, 2015, A2aR antagonists: Next generation checkpoint blockade for cancer immunotherapy, Comput. Struct. Biotechnol. J., 13, 265, 10.1016/j.csbj.2015.03.008 Vigano, 2019, Targeting adenosine in cancer immunotherapy to enhance T-cell function, Front Immunol., 10, 925, 10.3389/fimmu.2019.00925 Fiorucci, 2018, Bile acids activated receptors regulate innate immunity, Front Immunol., 9, 1853, 10.3389/fimmu.2018.01853 Jones, 2008, Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome, Proc. Natl. Acad. Sci. USA, 105, 13580, 10.1073/pnas.0804437105 Vavassori, 2009, The bile acid receptor FXR is a modulator of intestinal innate immunity, J. Immunol., 183, 6251, 10.4049/jimmunol.0803978 Mencarelli, 2009, The bile acid sensor farnesoid X receptor is a modulator of liver immunity in a rodent model of acute hepatitis, J. Immunol., 183, 6657, 10.4049/jimmunol.0901347 Cipriani, 2011, The bile acid receptor GPBAR-1 (TGR5) modulates integrity of intestinal barrier and immune response to experimental colitis, PLoS One, 6, 10.1371/journal.pone.0025637 Skelly, 2019, Mining the microbiota for microbial and metabolite-based immunotherapies, Nat. Rev. Immunol., 19, 305, 10.1038/s41577-019-0144-5 Guo, 2016, Bile acids control inflammation and metabolic disorder through inhibition of NLRP3 inflammasome, Immunity, 45, 802, 10.1016/j.immuni.2016.09.008 Hao, 2017, Farnesoid X receptor regulation of the NLRP3 inflammasome underlies cholestasis-associated sepsis, Cell Metab., 25, 856, 10.1016/j.cmet.2017.03.007 Ma, 2018, Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells, Science, 360, 10.1126/science.aan5931 Mirji, 2022, The microbiome-derived metabolite TMAO drives immune activation and boosts responses to immune checkpoint blockade in pancreatic cancer, Sci. Immunol., 7, eabn0704, 10.1126/sciimmunol.abn0704 Wang, 2022, The microbial metabolite trimethylamine N-oxide promotes antitumor immunity in triple-negative breast cancer, Cell Metab., 34, 581, 10.1016/j.cmet.2022.02.010 Met, 2019, Principles of adoptive T cell therapy in cancer, Semin Immunopathol., 41, 49, 10.1007/s00281-018-0703-z Chong, 2021, P. Lymphoma program investigators at the University of, five-year outcomes for refractory B-Cell lymphomas with CAR T-cell therapy, New Engl. J. Med, 384, 673, 10.1056/NEJMc2030164 Santomasso, 2019, The other side of CAR T-cell therapy: cytokine release syndrome neurologic toxicity, and financial burden, Am. Soc. Clin. Oncol. Educ. Book, 39, 433, 10.1200/EDBK_238691 Rooks, 2016, Gut microbiota, metabolites and host immunity, Nat. Rev. Immunol., 16, 341, 10.1038/nri.2016.42 Cummings, 1987, Short chain fatty acids in human large intestine, portal, hepatic and venous blood, Gut, 28, 1221, 10.1136/gut.28.10.1221 Arpaia, 2013, Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation, Nature, 504, 451, 10.1038/nature12726 Furusawa, 2013, Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells, Nature, 504, 446, 10.1038/nature12721 Kim, 2016, Gut microbial metabolites fuel host antibody responses, Cell Host Microbe, 20, 202, 10.1016/j.chom.2016.07.001 Chun, 2019, Metabolite-sensing receptor Ffar2 regulates colonic group 3 innate lymphoid cells and gut immunity, Immunity, 51, 871, 10.1016/j.immuni.2019.09.014 Usami, 2008, Butyrate and trichostatin A attenuate nuclear factor kappaB activation and tumor necrosis factor alpha secretion and increase prostaglandin E2 secretion in human peripheral blood mononuclear cells, Nutr. Res, 28, 321, 10.1016/j.nutres.2008.02.012 Chang, 2014, The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition, Proc. Natl. Acad. Sci. USA, 111, 2247, 10.1073/pnas.1322269111 Singh, 2010, Blockade of dendritic cell development by bacterial fermentation products butyrate and propionate through a transporter (Slc5a8)-dependent inhibition of histone deacetylases, J. Biol. Chem., 285, 27601, 10.1074/jbc.M110.102947 Luu, 2018, Regulation of the effector function of CD8(+) T cells by gut microbiota-derived metabolite butyrate, Sci. Rep., 8, 14430, 10.1038/s41598-018-32860-x Bachem, 2019, Microbiota-derived short-chain fatty acids promote the memory potential of antigen-activated CD8(+) T Cells, Immunity, 51, 285, 10.1016/j.immuni.2019.06.002 Trompette, 2014, Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis, Nat. Med, 20, 159, 10.1038/nm.3444 Hagihara, 2020, Clostridium butyricum modulates the microbiome to protect intestinal barrier function in mice with antibiotic-induced dysbiosis, Iscience, 23, 10.1016/j.isci.2019.100772 Tomita, 2020, Association of Probiotic Clostridium butyricum Therapy with Survival and Response to Immune Checkpoint Blockade in Patients with Lung Cancer, Cancer Immunol. Res, 8, 1236, 10.1158/2326-6066.CIR-20-0051 Dizman, 2022, Nivolumab plus ipilimumab with or without live bacterial supplementation in metastatic renal cell carcinoma: a randomized phase 1 trial, Nat. Med, 28, 704, 10.1038/s41591-022-01694-6 Docampo, 2022, Alloreactive T cells deficient of the short-chain fatty acid receptor GPR109A induce less graft-versus-host disease, Blood, 139, 2392, 10.1182/blood.2021010719 Wang, 2020, Inosine is an alternative carbon source for CD8(+)-T-cell function under glucose restriction, Nat. Metab., 2, 635, 10.1038/s42255-020-0219-4 Apetoh, 2007, Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy, Nat. Med, 13, 1050, 10.1038/nm1622 Ghiringhelli, 2009, Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors, Nat. Med, 15, 1170, 10.1038/nm.2028 Corrales, 2016, Endogenous and pharmacologic targeting of the STING pathway in cancer immunotherapy, Cytokine, 77, 245, 10.1016/j.cyto.2015.08.258 Woo, 2014, STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors, Immunity, 41, 830, 10.1016/j.immuni.2014.10.017 Tanaka, 2012, STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway, Sci. Signal, 5, ra20, 10.1126/scisignal.2002521 Fitzgerald, 2003, IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway, Nat. Immunol., 4, 491, 10.1038/ni921 Ishikawa, 2008, STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling, Nature, 455, 674, 10.1038/nature07317 Dunn, 2006, Interferons, immunity and cancer immunoediting, Nat. Rev. Immunol., 6, 836, 10.1038/nri1961 Fuertes, 2013, Type I interferon response and innate immune sensing of cancer, Trends Immunol., 34, 67, 10.1016/j.it.2012.10.004 Atarashi, 2008, ATP drives lamina propria T(H)17 cell differentiation, Nature, 455, 808, 10.1038/nature07240 Ganal, 2012, Priming of natural killer cells by nonmucosal mononuclear phagocytes requires instructive signals from commensal microbiota, Immunity, 37, 171, 10.1016/j.immuni.2012.05.020 Erttmann, 2022, The gut microbiota prime systemic antiviral immunity via the cGAS-STING-IFN-I axis, Immunity, 55, 847, 10.1016/j.immuni.2022.04.006 Li, 2020, Prebiotic-induced anti-tumor immunity attenuates tumor growth, Cell Rep., 30, 1753, 10.1016/j.celrep.2020.01.035 Leventhal, 2020, Immunotherapy with engineered bacteria by targeting the STING pathway for anti-tumor immunity, Nat. Commun., 11, 2739, 10.1038/s41467-020-16602-0 Riese, 2021, 500 SYNB1891, a bacterium engineered to produce a STING agonist, demonstrates target engagement in humans following intratumoral injection, J. Immunother. Cancer, 9, 10.1136/jitc-2021-SITC2021.500 Chao, 2019, Therapeutic targeting of the macrophage immune checkpoint CD47 in myeloid malignancies, Front Oncol., 9, 1380, 10.3389/fonc.2019.01380 Chao, 2012, The CD47-SIRPalpha pathway in cancer immune evasion and potential therapeutic implications, Curr. Opin. Immunol., 24, 225, 10.1016/j.coi.2012.01.010 Liu, 2015, CD47 blockade triggers T cell-mediated destruction of immunogenic tumors, Nat. Med., 21, 1209, 10.1038/nm.3931 Deng, 2014, STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors, Immunity, 41, 843, 10.1016/j.immuni.2014.10.019 Chen, 2016, Regulation and function of the cGAS-STING pathway of cytosolic DNA sensing, Nat. Immunol., 17, 1142, 10.1038/ni.3558 Shi, 2020, Intratumoral accumulation of gut microbiota facilitates CD47-based immunotherapy via STING signaling, J. Exp. Med, 217, 10.1084/jem.20192282 Conroy, 2022, Immune-related adverse events and the balancing act of immunotherapy, Nat. Commun., 13, 392, 10.1038/s41467-022-27960-2 Wang, 2018, Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis, Nat. Med, 24, 1804, 10.1038/s41591-018-0238-9 Krautkramer, 2021, Gut microbial metabolites as multi-kingdom intermediates, Nat. Rev. Microbiol, 19, 77, 10.1038/s41579-020-0438-4 Roager, 2018, Microbial tryptophan catabolites in health and disease, Nat. Commun., 9, 3294, 10.1038/s41467-018-05470-4 Zelante, 2013, Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22, Immunity, 39, 372, 10.1016/j.immuni.2013.08.003 Stockinger, 2014, The aryl hydrocarbon receptor: multitasking in the immune system, Annu Rev. Immunol., 32, 403, 10.1146/annurev-immunol-032713-120245 Quintana, 2008, Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor, Nature, 453, 65, 10.1038/nature06880 Bessede, 2014, Aryl hydrocarbon receptor control of a disease tolerance defence pathway, Nature, 511, 184, 10.1038/nature13323 Gandhi, 2010, Activation of the aryl hydrocarbon receptor induces human type 1 regulatory T cell-like and Foxp3(+) regulatory T cells, Nat. Immunol., 11, 846, 10.1038/ni.1915 Cervantes-Barragan, 2017, Lactobacillus reuteri induces gut intraepithelial CD4(+)CD8alphaalpha(+) T cells, Science, 357, 806, 10.1126/science.aah5825 Wilck, 2017, Salt-responsive gut commensal modulates TH17 axis and disease, Nature, 551, 585, 10.1038/nature24628 Sugimura, 2021, Lactobacillus gallinarum modulates the gut microbiota and produces anti-cancer metabolites to protect against colorectal tumourigenesis, Gut, 71, 2011, 10.1136/gutjnl-2020-323951 Agus, 2018, Gut microbiota regulation of tryptophan metabolism in health and disease, Cell Host Microbe, 23, 716, 10.1016/j.chom.2018.05.003 Zou, 2016, PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: Mechanisms, response biomarkers, and combinations, Sci. Transl. Med, 8, 328rv4, 10.1126/scitranslmed.aad7118 Hatae, 2020, Combination of host immune metabolic biomarkers for the PD-1 blockade cancer immunotherapy, JCI Insight, 5, 10.1172/jci.insight.133501 Wikoff, 2009, Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites, Proc. Natl. Acad. Sci. USA, 106, 3698, 10.1073/pnas.0812874106