The critical role of tumor microbiome in cancer immunotherapy

References

• Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39(1):1–11. doi:10.1016/j.immuni.2013.07.012.
   PubMed Web of Science ®Google Scholar
• McCarthy EF. The toxins of William B. Coley and the treatment of bone and soft-tissue sarcomas. Iowa Orthop J. 2006;26:154–158.
   PubMedGoogle Scholar
• Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell. 2015;27(4):450–461. doi:10.1016/j.ccell.2015.03.001.
   PubMed Web of Science ®Google Scholar
• Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science. 2018;359(6382):1350–1355. doi:10.1126/science.aar4060.
   PubMed Web of Science ®Google Scholar
• Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–723. doi:10.1056/NEJMoa1003466.
   PubMed Web of Science ®Google Scholar
• Postow MA, Sidlow R, Hellmann MD, Longo DL. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med. 2018;378(2):158–168. doi:10.1056/NEJMra1703481.
   PubMed Web of Science ®Google Scholar
• Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets T, Prieto PA, Vicente D, Hoffman K, Wei SC, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018;359(6371):97–103. doi:10.1126/science.aan4236.
   PubMed Web of Science ®Google Scholar
• Boesch M, Horvath L, Baty F, Pircher A, Wolf D, Spahn S, Straussman R, Tilg H, Brutsche MH. Compartmentalization of the host microbiome: how tumor microbiota shapes checkpoint immunotherapy outcome and offers therapeutic prospects. J Immunother Cancer. 2022;10(11):e005401. doi:10.1136/jitc-2022-005401.
   PubMed Web of Science ®Google Scholar
• Nejman D, Livyatan I, Fuks G, Gavert, N, Zwang, Y, Geller, LT, Rotter-Maskowitz, A, Weiser, R, Mallel, G, Gigi, E, et al. The human tumor microbiome is composed of tumor type-specific intracellular bacteria. Science. 2020;368(6494):973–980. doi:10.1126/science.aay9189.
   PubMed Web of Science ®Google Scholar
• Gopalakrishnan V, Helmink BA, Spencer CN, Reuben A, Wargo JA. The influence of the gut microbiome on cancer, immunity, and cancer immunotherapy. Cancer Cell. 2018;33(4):570–580. doi:10.1016/j.ccell.2018.03.015.
   PubMed Web of Science ®Google Scholar
• Roy S, Trinchieri G. Microbiota: a key orchestrator of cancer therapy. Nat Rev Cancer. 2017;17(5):271–285. doi:10.1038/nrc.2017.13.
   PubMed Web of Science ®Google Scholar
• Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CPM, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350(6264):1079–1084. doi:10.1126/science.aad1329.
   PubMed Web of Science ®Google Scholar
• Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre M-L, Luke JJ, Gajewski TF. The commensal microbiome is associated with anti–PD-1 efficacy in metastatic melanoma patients. Science. 2018;359(6371):104–108. doi:10.1126/science.aao3290.
   PubMed Web of Science ®Google Scholar
• Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, Gavert N, Zwang Y, Cooper ZA, Shee K, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science. 2017;357(6356):1156–1160. doi:10.1126/science.aah5043.
   PubMed Web of Science ®Google Scholar
• Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, Ojesina AI, Jung J, Bass AJ, Tabernero J, et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 2012;22(2):292–298. doi:10.1101/gr.126573.111.
   PubMed Web of Science ®Google Scholar
• Urbaniak C, Gloor GB, Brackstone M, Scott L, Tangney M, Reid G. The microbiota of breast tissue and its association with breast cancer. Appl Environ Microbiol. 2016;82(16):5039–5048. doi:10.1128/AEM.01235-16.
   PubMed Web of Science ®Google Scholar
• Thomas AM, Manghi P, Asnicar F, Pasolli E, Armanini F, Zolfo M, Beghini F, Manara S, Karcher N, Pozzi C, et al. Metagenomic analysis of colorectal cancer datasets identifies cross-cohort microbial diagnostic signatures and a link with choline degradation. Nat Med. 2019;25(4):667–678. doi:10.1038/s41591-019-0405-7.
   PubMed Web of Science ®Google Scholar
• Dzutsev A, Goldszmid RS, Viaud S, Zitvogel L, Trinchieri G. The role of the microbiota in inflammation, carcinogenesis, and cancer therapy. Eur J Immunol. 2015;45(1):17–31. doi:10.1002/eji.201444972.
   PubMed Web of Science ®Google Scholar
• Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013;342(6161):967–970. doi:10.1126/science.1240527.
   PubMed Web of Science ®Google Scholar
• Spencer CN, McQuade JL, Gopalakrishnan V, McCulloch JA, Vetizou M, Cogdill AP, Khan MAW, Zhang X, White MG, Peterson CB, et al. Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response. Science. 2021;374(6575):1632–1640. doi:10.1126/science.aaz7015.
   PubMed Web of Science ®Google Scholar
• Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, Glickman JN, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341(6145):569–573. doi:10.1126/science.1241165.
   PubMed Web of Science ®Google Scholar
• Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Man Lei Y, Jabri B, Alegre M-L, et al. Commensal bifidobacterium promotes antitumor immunity and facilitates anti–PD-L1 efficacy. Science. 2015;350(6264):1084–1089. doi:10.1126/science.aac4255.
   PubMed Web of Science ®Google Scholar
• Pushalkar S, Hundeyin M, Daley D, Zambirinis CP, Kurz E, Mishra A, Mohan N, Aykut B, Usyk M, Torres LE, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov. 2018;8(4):403–416. doi:10.1158/2159-8290.CD-17-1134.
   PubMed Web of Science ®Google Scholar
• Wastyk HC, Fragiadakis GK, Perelman D, Dahan, D, Merrill, BD, Feiqiao, BY, Topf, M, Gonzalez, CG, Van Treuren, W, Han, S, et al. Gut-microbiota-targeted diets modulate human immune status. Cell. 2021;184(16):4137–4153.e4114. doi:10.1016/j.cell.2021.06.019.
   PubMed Web of Science ®Google Scholar
• Sepich-Poore GD, Zitvogel L, Straussman R, Hasty J, Wargo JA, Knight R. The microbiome and human cancer. Science. 2021;371(6536). doi:10.1126/science.abc4552.
   PubMed Web of Science ®Google Scholar
• Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, Taniguchi K, Yu G-Y, Österreicher CH, Hung KE, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature. 2012;491(7423):254–258. doi:10.1038/nature11465.
   PubMed Web of Science ®Google Scholar
• Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X, Cai D, Neuberg D, Huang K, Guevara F, Nelson T, et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science. 2017;358(6369):1443–1448. doi:10.1126/science.aal5240.
   PubMed Web of Science ®Google Scholar
• Nougayrède JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, Buchrieser C, Hacker J, Dobrindt U, Oswald E, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 2006;313(5788):848–851. doi:10.1126/science.1127059.
   PubMed Web of Science ®Google Scholar
• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252–264. doi:10.1038/nrc3239.
   PubMed Web of Science ®Google Scholar
• Routy B, Le Chatelier E, Derosa L, Duong, CP, Alou, MT, Daillère, R, Fluckiger, A, Messaoudene, M, Rauber, C, Roberti, MP et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018;359(6371):91–97. doi:10.1126/science.aan3706.
   PubMed Web of Science ®Google Scholar
• Sterner RC, Sterner RM. CAR-T cell therapy: current limitations and potential strategies. Blood Cancer J. 2021;11(4):69. doi:10.1038/s41408-021-00459-7.
   PubMed Web of Science ®Google Scholar
• Schuster SJ, Bishop MR, Tam CS, Waller EK, Borchmann P, McGuirk JP, Jäger U, Jaglowski S, Andreadis C, Westin JR, et al. Tisagenlecleucel in adult relapsed or refractory diffuse large B-Cell lymphoma. N Engl J Med. 2019;380(1):45–56. doi:10.1056/NEJMoa1804980.
   PubMed Web of Science ®Google Scholar
• Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, Citrin DE, Restifo NP, Robbins PF, Wunderlich JR, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res. 2011;17(13):4550–4557. doi:10.1158/1078-0432.CCR-11-0116.
   PubMed Web of Science ®Google Scholar
• Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157(1):121–141. doi:10.1016/j.cell.2014.03.011.
   PubMed Web of Science ®Google Scholar
• Ganal-Vonarburg SC, Hornef MW, Macpherson AJ. Microbial-host molecular exchange and its functional consequences in early mammalian life. Science. 2020;368(6491):604–607. doi:10.1126/science.aba0478.
   PubMed Web of Science ®Google Scholar
• Böttcher JP, Bonavita E, Chakravarty P, Blees H, Cabeza-Cabrerizo M, Sammicheli S, Rogers NC, Sahai E, Zelenay S, Reis e Sousa C. NK Cells Stimulate Recruitment of cDC1 into the Tumor Microenvironment Promoting Cancer Immune Control. Cell. 2018;172(5):1022–1037.e1014. doi:10.1016/j.cell.2018.01.004.
   PubMed Web of Science ®Google Scholar
• Finn OJ. Cancer vaccines: between the idea and the reality. Nat Rev Immunol. 2003;3(8):630–641. doi:10.1038/nri1150.
   PubMed Web of Science ®Google Scholar
• Goradel NH, Baker AT, Arashkia A, Ebrahimi N, Ghorghanlu S, Negahdari B. Oncolytic virotherapy: Challenges and solutions. Curr Probl Cancer. 2021;45(1):100639. doi:10.1016/j.currproblcancer.2020.100639.
   PubMed Web of Science ®Google Scholar
• Duerkop BA, Hooper LV. Resident viruses and their interactions with the immune system. Nat Immunol. 2013;14(7):654–659. doi:10.1038/ni.2614.
   PubMed Web of Science ®Google Scholar
• Kuczma MP, Ding ZC, Li T, Habtetsion T, Chen T, Hao Z, Bryan L, Singh N, Kochenderfer JN, Zhou G, et al. The impact of antibiotic usage on the efficacy of chemoimmunotherapy is contingent on the source of tumor-reactive T cells. Oncotarget. 2017;8(67):111931–111942. doi:10.18632/oncotarget.22953.
   PubMedGoogle Scholar
• Lynch SV, Pedersen O, Phimister EG. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375(24):2369–2379. doi:10.1056/NEJMra1600266.
   PubMed Web of Science ®Google Scholar
• Zitvogel L, Ma Y, Raoult D, Kroemer G, Gajewski TF. The microbiome in cancer immunotherapy: diagnostic tools and therapeutic strategies. Science. 2018;359(6382):1366–1370. doi:10.1126/science.aar6918.
   PubMed Web of Science ®Google Scholar
• Baruch EN, Youngster I, Ben-Betzalel G, Ortenberg R, Lahat A, Katz L, Adler K, Dick-Necula D, Raskin S, Bloch N, et al. Fecal microbiota transplant promotes response in immunotherapy-refractory melanoma patients. Science. 2021;371(6529):602–609. doi:10.1126/science.abb5920.
   PubMed Web of Science ®Google Scholar
• Suez J, Zmora N, Zilberman-Schapira G, Mor, U, Dori-Bachash, M, Bashiardes, S, Zur, M, Regev-Lehavi, D, Brik, RBZ, Federici, S, et al. Post-Antibiotic Gut Mucosal Microbiome Reconstitution Is Impaired by Probiotics and Improved by Autologous FMT. Cell. 2018;174(6):1406–1423.e1416. doi:10.1016/j.cell.2018.08.047.
   PubMed Web of Science ®Google Scholar
• Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C, Debelius J, Gonzalez A, Kosciolek T, McCall L-I, McDonald D, et al. Best practices for analysing microbiomes. Nat Rev Microbiol. 2018;16(7):410–422. doi:10.1038/s41579-018-0029-9.
   PubMed Web of Science ®Google Scholar
• Franzosa EA, Hsu T, Sirota-Madi A, Shafquat, A, Abu-Ali, G, Morgan, XC, Huttenhower, C Sequencing and beyond: integrating molecular ‘omics’ for microbial community profiling. Nat Rev Microbiol. 2015;13(6):360–372. doi:10.1038/nrmicro3451.
   PubMed Web of Science ®Google Scholar
• Lloyd-Price J, Arze C, Ananthakrishnan AN, Schirmer M, Avila-Pacheco J, Poon TW, Andrews E, Ajami NJ, Bonham KS, Brislawn CJ, et al. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature. 2019;569(7758):655–662. doi:10.1038/s41586-019-1237-9.
   PubMed Web of Science ®Google Scholar
• Rooks MG, Garrett WS. Gut microbiota, metabolites and host immunity. Nat Rev Immunol. 2016;16(6):341–352. doi:10.1038/nri.2016.42.
   PubMed Web of Science ®Google Scholar
• Doron S, Snydman DR. Risk and safety of probiotics. Clin Infect Dis. 2015;60(Suppl 2):S129–134. doi:10.1093/cid/civ085.
   PubMed Web of Science ®Google Scholar
• Pires DP, Vilas Boas D, Sillankorva S, Azeredo J. Phage therapy: a step forward in the treatment of Pseudomonas aeruginosa infections. J Virol. 2015;89(15):7449–7456. doi:10.1128/JVI.00385-15.
   PubMed Web of Science ®Google Scholar
• Lim WA, June CH. The principles of engineering immune cells to treat cancer. Cell. 2017;168(4):724–740. doi:10.1016/j.cell.2017.01.016.
   PubMed Web of Science ®Google Scholar
• Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, et al. Expert consensus document. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506–514. doi:10.1038/nrgastro.2014.66.
   PubMed Web of Science ®Google Scholar
• Zitvogel L, Daillère R, Roberti MP, Routy B, Kroemer G. Anticancer effects of the microbiome and its products. Nat Rev Microbiol. 2017;15(8):465–478. doi:10.1038/nrmicro.2017.44.
   PubMed Web of Science ®Google Scholar
• Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14(8):491–502. doi:10.1038/nrgastro.2017.75.
   PubMed Web of Science ®Google Scholar
• Tsilingiri K, Rescigno M. Postbiotics: what else? Benef Microbes. 2013;4(1):101–107. doi:10.3920/BM2012.0046.
   PubMed Web of Science ®Google Scholar
• Cammarota G, Ianiro G, Gasbarrini A. Fecal microbiota transplantation for the treatment of clostridium difficile infection: a systematic review. J Clin Gastroenterol. 2014;48(8):693–702. doi:10.1097/MCG.0000000000000046.
   PubMed Web of Science ®Google Scholar
• Routy B, Gopalakrishnan V, Daillère R, Zitvogel L, Wargo JA, Kroemer G. The gut microbiota influences anticancer immunosurveillance and general health. Nat Rev Clin Oncol. 2018;15(6):382–396. doi:10.1038/s41571-018-0006-2.
   PubMed Web of Science ®Google Scholar
• Davar D, Dzutsev AK, McCulloch JA, Rodrigues, RR, Chauvin, JM, Morrison, RM, Deblasio, RN, Menna, C, Ding, Q, Pagliano, O, et al. Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science. 2021;371(6529):595–602. doi:10.1126/science.abf3363.
   PubMed Web of Science ®Google Scholar
• Alexander JL, Wilson ID, Teare J, Marchesi JR, Nicholson JK, Kinross JM. Gut microbiota modulation of chemotherapy efficacy and toxicity. Nat Rev Gastroenterol Hepatol. 2017;14(6):356–365. doi:10.1038/nrgastro.2017.20.
   PubMed Web of Science ®Google Scholar
• Chen D, Wu J, Jin D, Wang, B, Cao, H. Fecal microbiota transplantation in cancer management: Current status and perspectives. Int J Cancer. 2019;145(8):2021–2031. doi:10.1002/ijc.32003.
   PubMed Web of Science ®Google Scholar
• Krieg AM. CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol. 2002;20(1):709–760. doi:10.1146/annurev.immunol.20.100301.064842.
   PubMed Web of Science ®Google Scholar
• Vijay-Kumar M, Gewirtz AT. Flagellin: key target of mucosal innate immunity. Mucosal Immunol. 2009;2(3):197–205. doi:10.1038/mi.2009.9.
   PubMed Web of Science ®Google Scholar
• Lichty BD, Breitbach CJ, Stojdl DF, Bell JC. Going viral with cancer immunotherapy. Nat Rev Cancer. 2014;14(8):559–567. doi:10.1038/nrc3770.
   PubMed Web of Science ®Google Scholar
• Andtbacka RH, Kaufman HL, Collichio F, Amatruda T, Senzer N, Chesney J, Delman KA, Spitler LE, Puzanov I, Agarwala SS, et al. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J Clin Oncol. 2015;33(25):2780–2788. doi:10.1200/JCO.2014.58.3377.
   PubMed Web of Science ®Google Scholar
• The Integrative HMP (iHMP) Research Network Consortium. The Integrative Human Microbiome Project. Nature. 2019;569:641–648. doi:10.1038/s41586-019-1238-8.
   PubMed Web of Science ®Google Scholar
• Bikel S, Valdez-Lara A, Cornejo-Granados F, Rico, K, Canizales-Quinteros, S, Soberón, X, Del Pozo-Yauner, L, Ochoa-Leyva, A Combining metagenomics, metatranscriptomics and viromics to explore novel microbial interactions: towards a systems-level understanding of human microbiome. Comput Struct Biotechnol J. 2015;13:390–401. 10.1016/j.csbj.2015.06.001.
   PubMed Web of Science ®Google Scholar
• Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng J-F, Darling A, Malfatti S, Swan BK, Gies EA, et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature. 2013;499(7459):431–437. doi:10.1038/nature12352.
   PubMed Web of Science ®Google Scholar
• Pasolli E, Truong DT, Malik F, Waldron L, Segata N. Machine learning meta-analysis of large metagenomic datasets: tools and biological insights. PLoS Comput Biol. 2016;12(7):e1004977. doi:10.1371/journal.pcbi.1004977.
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. doi:10.1016/j.cell.2011.02.013.
   PubMed Web of Science ®Google Scholar
• Boesch M, Baty F, Rothschild SI, Tamm M, Joerger M, Früh M, Brutsche MH. Tumour neoantigen mimicry by microbial species in cancer immunotherapy. Br J Cancer. 2021;125(3):313–323. doi:10.1038/s41416-021-01365-2.
   PubMed Web of Science ®Google Scholar
• Poore GD, Kopylova E, Zhu Q, Carpenter C, Fraraccio S, Wandro S, Kosciolek T, Janssen S, Metcalf J, Song SJ, et al. Microbiome analyses of blood and tissues suggest cancer diagnostic approach. Nature. 2020;579(7800):567–574. doi:10.1038/s41586-020-2095-1.
   PubMed Web of Science ®Google Scholar
• Blanco E, Shen H, Ferrari M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol. 2015;33(9):941–951. doi:10.1038/nbt.3330.
   PubMed Web of Science ®Google Scholar
• Kitano H. Systems biology: a brief overview. Science. 2002;295(5560):1662–1664. doi:10.1126/science.1069492.
   PubMed Web of Science ®Google Scholar