Emerging clinical relevance of microbiome in cancer: promising biomarkers and therapeutic targets
Received date: 31 Aug 2023
Accepted date: 22 Oct 2023
Published date: 15 Apr 2024
Copyright
The profound influence of microbiota in cancer initiation and progression has been under the spotlight for years, leading to numerous researches on cancer microbiome entering clinical evaluation. As promising biomarkers and therapeutic targets, the critical involvement of microbiota in cancer clinical practice has been increasingly appreciated. Here, recent progress in this field is reviewed. We describe the potential of tumor-associated microbiota as effective diagnostic and prognostic biomarkers, respectively. In addition, we highlight the relationship between microbiota and the therapeutic efficacy, toxicity, or side effects of commonly utilized treatments for cancer, including chemotherapy, radiotherapy, and immunotherapy. Given that microbial factors influence the cancer treatment outcome, we further summarize some dominating microbial interventions and discuss the hidden risks of these strategies. This review aims to provide an overview of the applications and advancements of microbes in cancer clinical relevance.
Key words: microbiome; cancer; diagnosis; prognosis; therapy
Jia-Hao Dai , Xi-Rong Tan , Han Qiao , Na Liu . Emerging clinical relevance of microbiome in cancer: promising biomarkers and therapeutic targets[J]. Protein & Cell, 2024 , 15(4) : 239 -260 . DOI: 10.1093/procel/pwad052
1 |
Almeida A, Nayfach S, Boland M et al. A unified catalog of 204,938 reference genomes from the human gut microbiome. Nat Biotechnol 2021;39:105–14.
|
2 |
Baruch EN, Youngster I, Ben-Betzalel G et al. Fecal microbiota transplant promotes response in immunotherapy-refractory melanoma patients. Science 2021;371:602–9.
|
3 |
Batten M, Shanahan ER, Silva IP et al. Low intestinal microbial diversity is associated with severe immune-related adverse events and lack of response to neoadjuvant combination antiPD1, anti-CTLA4 immunotherapy. Cancer Res 2019;79:2822.
|
4 |
Beck KE, Blansfield JA, Tran KQ et al. Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 2006;24:2283–9.
|
5 |
Bender MJ, McPherson AC, Phelps CM et al. Dietary tryptophan metabolite released by intratumoral Lactobacillus reuteri facilitates immune checkpoint inhibitor treatment. Cell 2023;186:1846–1862.e26.
|
6 |
Bhatt AP, Pellock SJ, Biernat KA et al. Targeted inhibition of gut bacterial beta-glucuronidase activity enhances anticancer drug efficacy. Proc Natl Acad Sci USA 2020;117:7374–81.
|
7 |
Bretthauer M, Kalager M. Principles, effectiveness and caveats in screening for cancer. Br J Surg 2013;100:55–65.
|
8 |
Canale FP, Basso C, Antonini G et al. Metabolic modulation of tumours with engineered bacteria for immunotherapy. Nature 2021;598:662–6.
|
9 |
Chamseddine AN, Ducreux M, Armand JP et al. Intestinal bacterial beta-glucuronidase as a possible predictive biomarker of irinotecan-induced diarrhea severity. Pharmacol Ther 2019;199:1–5.
|
10 |
Chandra D, Jahangir A, Quispe-Tintaya W et al. Myeloid-derived suppressor cells have a central role in attenuated Listeria monocytogenes-based immunotherapy against metastatic breast cancer in young and old mice. Br J Cancer 2013;108:2281–90.
|
11 |
Chaput N, Lepage P, Coutzac C et al. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol 2017;28:1368–79.
|
12 |
Chen W, Wang Y, Qin M et al. Bacteria-driven hypoxia targeting for combined biotherapy and photothermal therapy. ACS Nano 2018;12:5995–6005.
|
13 |
Chen J, Zhao K, Vitetta L. Effects of intestinal microbial-elaborated butyrate on oncogenic signaling pathways. Nutrients 2019;11:1026.
|
14 |
Chen S, Chieng W, Huang S et al. The synergistic tumor growth-inhibitory effect of probiotic Lactobacillus on transgenic mouse model of pancreatic cancer treated with gemcitabine. Sci Rep 2020;10:20319.
|
15 |
Chen Y, Ma J, Dong Y et al. Characteristics of gut microbiota in patients with clear cell renal cell carcinoma. Front Microbiol 2022a;13:913718.
|
16 |
Chen F, Dai X, Zhou C-C et al. Integrated analysis of the faecal metagenome and serum metabolome reveals the role of gut microbiome-associated metabolites in the detection of colorectal cancer and adenoma. Gut 2022b;71:1315–25.
|
17 |
Chen X, Li S, Lin C et al. Isomaltooligosaccharides inhibit early colorectal carcinogenesis in a 1,2-dimethylhydrazine-induced rat model. Front Nutr 2022c;9:995126.
|
18 |
Chen YE, Bousbaine D, Veinbachs A et al. Engineered skin bacteria induce antitumor T cell responses against melanoma. Science 2023;380:203–10.
|
19 |
Cheng Y, Du J, Han J et al. Polymyxin Battenuates LPS-induced death butaggravates radiation-induced death via TLR4-Myd88-IL-6 pathway. Cell Physiol Biochem 2017;42:1120–6.
|
20 |
Cheng W, Xiang W, Wang S et al. Tanshinone IIA ameliorates oxaliplatin-induced neurotoxicity via mitochondrial protection and autophagy promotion. Am J Transl Res 2019;11:3140–9.
|
21 |
Ciorba MA, Riehl TE, Rao MS et al. Lactobacillus probiotic protects intestinal epithelium from radiation injury in a TLR-2/cyclo-oxygenase-2-dependent manner. Gut 2012;61:829–38.
|
22 |
Coker OO, Nakatsu G, Dai RZ et al. Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer. Gut 2019;68:654–62.
|
23 |
Coker OO, Wu WKK, Wong SH et al. Altered gut archaea composition and interaction with bacteria are associated with colorectal cancer. Gastroenterology 2020;159:1459–1470.e5.
|
24 |
Coker OO, Liu C, Wu WKK et al. Altered gut metabolites and microbiota interactions are implicated in colorectal carcinogenesis and can be non-invasive diagnostic biomarkers. Microbiome 2022;10:35.
|
25 |
Crawford PA, Gordon JI. Microbial regulation of intestinal radiosensitivity. Proc Natl Acad Sci USA 2005;102:13254–9.
|
26 |
Cui M, Xiao H, Li Y et al. Faecal microbiota transplantation protects against radiation-induced toxicity. EMBO Mol Med 2017;9:448–61.
|
27 |
Daillere R, Vétizou M, Waldschmitt N et al. Enterococcus hirae and Barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects. Immunity 2016;45:931–43.
|
28 |
Davar D, Dzutsev AK, McCulloch JA et al. Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science 2021;371:595–602.
|
29 |
de Martel C, Georges D, Bray F et al. Global burden of cancer attributable to infections in 2018: a worldwide incidence analysis. Lancet Glob Health 2020;8:e180–90.
|
30 |
Derosa L, Hellmann MD, Spaziano M et al. Negative association of antibiotics on clinical activity of immune check-point inhibitors in patients with advanced renal cell and non-small-cell lung cancer. Ann Oncol 2018;29:1437–44.
|
31 |
De Ruysscher D, Niedermann G, Burnet NG et al. Radiotherapy toxicity. Nat Rev Dis Primers 2019;5:15.
|
32 |
Deshpande G, Athalye-Jape G, Patole S. Para-probiotics for preterm neonates-the next frontier. Nutrients 2018;10:871.
|
33 |
Ding Y, Yan Y, Chen D et al. Modulating effects of polysaccharides from the fruits of Lycium barbarum on the immune response and gut microbiota in cyclophosphamide-treated mice. Food Funct 2019;10:3671–83.
|
34 |
Ding X, Li Q, Li P et al. Fecal microbiota transplantation: a promising treatment for radiation enteritis? Radiother Oncol 2020;143:12–8.
|
35 |
Dohlman AB, Klug J, Mesko M et al. A pan-cancer mycobiome analysis reveals fungal involvement in gastrointestinal and lung tumors. Cell 2022;185:3807–3822.e12.
|
36 |
Dong X, Pan P, Zheng D-W et al. Bioinorganic hybrid bacteriophage for modulation of intestinal microbiota to remodel tumor-immune microenvironment against colorectal cancer. Sci Adv 2020;6:eaba1590.
|
37 |
Dubin K, Callahan MK, Ren B et al. Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nat Commun 2016;7:10391.
|
38 |
Egan LJ, Eckmann L, Greten FR et al. I kappa B-kinase beta-dependent NF-kappa B activation provides radio-protection to the intestinal epithelium. Proc Natl Acad Sci USA 2004;101:2452–7.
|
39 |
Eisenhofer R, Minich JJ, Marotz C et al. Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends Microbiol 2019;27:105–17.
|
40 |
Erb-Downward JR, Falkowski NR, D’Souza JC et al. Critical relevance of stochastic effects on low-bacterial-biomass 16S rRNA gene analysis. mBio 2020;11:e00258–20.
|
41 |
Federici S, Kredo-Russo S, Valdés-Mas R et al. Targeted suppression of human IBD-associated gut microbiota commensals by phage consortia for treatment of intestinal inflammation. Cell 2022;185:2879–2898.e24.
|
42 |
Flemer B, Warren RD, Barrett MP et al. The oral microbiota in colorectal cancer is distinctive and predictive. Gut 2018;67:1454–63.
|
43 |
Geller LT, Barzily-Rokni M, Danino T et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science 2017;357:1156–60.
|
44 |
Gibson GR, Hutkins R, Sanders ME et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 2017;14:491–502.
|
45 |
Gogokhia L, Buhrke K, Bell R et al. Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Cell Host Microbe 2019;25:285–299.e8.
|
46 |
Gopalakrishnan V, Spencer CN, Nezi L et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 2018;359:97–103.
|
47 |
Guenther M, Haas M, Heinemann V et al. Bacterial lipopolysaccharide as negative predictor of gemcitabine efficacy in advanced pancreatic cancer - translational results from the AIO-PK0104 Phase 3 study. Br J Cancer 2020;123:1370–6.
|
48 |
Guo J, Chen Y, Lei X et al. Monophosphoryl lipid a attenuates radiation injury through TLR4 activation. Oncotarget 2017;8:86031–42.
|
49 |
Han J, Tao Z-H, Wang J-L et al. Microbiota-derived tryptophan catabolites mediate the chemopreventive effects of statins on colorectal cancer. Nat Microbiol 2023;8:919–33.
|
50 |
He Y, Wu W, Zheng H-M et al. Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat Med 2018;24:1532–5.
|
51 |
He L, Yang H, Tang J et al. Intestinal probiotics E. coli Nissle 1917 as a targeted vehicle for delivery of p53 and Tum-5 to solid tumors for cancer therapy. J Biol Eng 2019;13:58.
|
52 |
Hezaveh K, Shinde RS, Klötgen A et al. Tryptophan-derived microbial metabolites activate the aryl hydrocarbon receptor in tumor-associated macrophages to suppress anti-tumor immunity. Immunity 2022;55:324–40.e8.
|
53 |
Holmes ZC, Villa MM, Durand HK et al. Microbiota responses to different prebiotics are conserved within individuals and associated with habitual fiber intake. Microbiome 2022;10:114.
|
54 |
Hong B, Sobue T, Choquette L et al. Chemotherapy-induced oral mucositis is associated with detrimental bacterial dysbiosis. Microbiome 2019;7:1–18.
|
55 |
Hsieh Y, Tung S-Y, Pan H-Y et al. Fusobacterium nucleatum colonization is associated with decreased survival of Helicobacter pylori-positive gastric cancer patients. World J Gastroenterol 2021;27:7311–23.
|
56 |
Hsueh C, Lau H-C, Huang Q et al. Fusobacterium nucleatum impairs DNA mismatch repair and stability in patients with squamous cell carcinoma of the head and neck. Cancer 2022;128:3170–84.
|
57 |
Huang S, Chen J, Lian L-Y et al. Intratumoral levels and prognostic significance of Fusobacterium nucleatum in cervical carcinoma. Aging 2020;12:23337–50.
|
58 |
Hughes E, Scurr M, Campbell E et al. T-cell modulation by cyclophosphamide for tumour therapy. Immunology 2018;154:62–8.
|
59 |
Iida N, Dzutsev A, Stewart CA et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 2013;342:967–70.
|
60 |
Kang G, Jung D-R, Lee YH et al. Dynamics of fecal microbiota with and without invasive cervical cancer and its application in early diagnosis. Cancers 2020;12:3800.
|
61 |
Kang G, Jung D-R, Lee YH et al. Potential association between vaginal microbiota and cervical carcinogenesis in Korean women: a cohort study. Microorganisms 2021;9:294.
|
62 |
Kartal E, Schmidt TSB, Molina-Montes E et al. MAGIC Study investigators. A faecal microbiota signature with high specificity for pancreatic cancer. Gut 2022;71:1359–72.
|
63 |
Kato S, Hamouda N, Kano Y et al. Probiotic Bifidobacterium bifidum G9-1 attenuates 5-fluorouracil-induced intestinal mucositis in mice via suppression of dysbiosis-related secondary inflammatory responses. Clin Exp Pharmacol Physiol 2017;44:1017–25.
|
64 |
Kodawara T, Higashi T, Negoro Y et al. The inhibitory effect of ciprofloxacin on the beta-glucuronidase-mediated deconjugation of the irinotecan metabolite SN-38-G. Basic Clin Pharmacol 2016;118:333–7.
|
65 |
Kwong TNY, Wang X, Nakatsu G et al. Association between bacteremia from specific microbes and subsequent diagnosis of colorectal cancer. Gastroenterology 2018;155:383–390.e8.
|
66 |
Lee S, Cho S-Y, Yoon Y et al. Bifidobacterium bifidum strains synergize with immune checkpoint inhibitors to reduce tumour burden in mice. Nat Microbiol 2021;6:277–88.
|
67 |
Li HL, Lu L, Wang XS et al. Alteration of gut microbiota and inflammatory cytokine/chemokine profiles in 5-fluorouracil induced intestinal mucositis. Front Cell Infect Microbiol 2017;7:455.
|
68 |
Li Z, Fu R, Wen X et al. The significant clinical correlation of the intratumor oral microbiome in oral squamous cell carcinoma based on tissue-derived sequencing. Front Physiol 2023;13:1089539.
|
69 |
Liang JQ, Wong SH, Szeto CH et al. Fecal microbial DNA markers serve for screening colorectal neoplasm in asymptomatic subjects. J Gastroenterol Hepatol 2021;36:1035–43.
|
70 |
Lim MY, Hong S, Hwang KH et al. Diagnostic and prognostic potential of the oral and gut microbiome for lung adenocarcinoma. Clin Transl Med 2021;11:e508.
|
71 |
Lin Y, Lau HC, Liu Y et al. Altered mycobiota signatures and enriched pathogenic Aspergillus rambellii are associated with colorectal cancer based on multi-cohort fecal metagenomic analyses. Gastroenterology 2022;163:908–21.
|
72 |
Linn YH, Thu KK, Win NHH. Effect of probiotics for the prevention of acute radiation-induced diarrhoea among cervical cancer patients: a randomized double-blind placebo-controlled study. Probiotics Antimicrob Proteins 2019;11:638–47.
|
73 |
Liu D, Hu Y, Guo Y et al. Mycoplasma-associated multi-drug resistance of hepatocarcinoma cells requires the interaction of P37 and Annexin A2. PLoS One 2017;12:e0184578.
|
74 |
Liu N, Jiao N, Tan J-C et al. Multi-kingdom microbiota analyses identify bacterial-fungal interactions and biomarkers of colorectal cancer across cohorts. Nat Microbiol 2022;7:238–50.
|
75 |
Lu Y, Yuan X, Wang M et al. Gut microbiota influence immunotherapy responses: mechanisms and therapeutic strategies. J Hematol Oncol 2022;15:47.
|
76 |
Ma C, Han M, Heinrich B et al. Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science 2018;360:eaan5931.
|
77 |
Ma C, Chen K, Wang Y et al. Establishing a novel colorectal cancer predictive model based on unique gut microbial single nucleotide variant markers. Gut Microbes 2021;13:1–6.
|
78 |
Mandell DJ, Lajoie MJ, Mee MT et al. Biocontainment of genetically modified organisms by synthetic protein design. Nature 2015;518:55–60.
|
79 |
Manichanh C, Varela E, Martinez C et al. The gut microbiota predispose to the pathophysiology of acute postradiotherapy diarrhea. Am J Gastroenterol 2008;103:1754–61.
|
80 |
Manor O, Dai CL, Kornilov SA et al. Health and disease markers correlate with gut microbiome composition across thousands of people. Nat Commun 2020;11:5206.
|
81 |
Marcella C, Cui B, Kelly CR et al. Systematic review: the global incidence of faecal microbiota transplantation-related adverse events from 2000 to 2020. Aliment Pharmacol Ther 2021;53:33–42.
|
82 |
McCulloch JA, Davar D, Rodrigues RR et al. Intestinal microbiota signatures of clinical response and immune-related adverse events in melanoma patients treated with anti-PD-1. Nat Med 2022;28:545–56.
|
83 |
Mima K, Nishihara R, Qian ZR et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 2016;65:1973–80.
|
84 |
Nagata N, Nishijima S, Kojima Y et al. Metagenomic identification of microbial signatures predicting pancreatic cancer from a multinational study. Gastroenterology 2022;163:222–38.
|
85 |
Nakatsu G, Zhou H, Wu WKK et al. Alterations in enteric virome are associated with colorectal cancer and survival outcomes. Gastroenterology 2018;155:529–541.e5.
|
86 |
Narunsky-Haziza L, Sepich-Poore GD, Livyatan I et al. Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions. Cell 2022;185:3789–3806.e17.
|
87 |
Nejman D, Livyatan I, Fuks G et al. The human tumor microbiome is composed of tumor type-specific intracellular bacteria. Science 2020;368:973–80.
|
88 |
Nino JLG, Wu H, LaCourse KD et al. Effect of the intratumoral microbiota on spatial and cellular heterogeneity in cancer. Nature 2022;611:810.
|
89 |
Park EM, Chelvanambi M, Bhutiani N et al. Targeting the gut and tumor microbiota in cancer. Nat Med 2022;28:690–703.
|
90 |
Peng Z, Cheng S, Kou Y et al. The gut microbiome is associated with clinical response to anti-PD-1/PD-L1 immunotherapy in gastrointestinal cancer. Cancer Immunol Res 2020;8:1251–61.
|
91 |
Peterson DE, Boers-Doets CB, Bensadoun RJ et al. ESMO Guidelines Committee. Management of oral and gastrointestinal mucosal injury: ESMO Clinical Practice Guidelines for diagnosis, treatment, and follow-up(aEuro). Ann Oncol 2015;26:v139–51.
|
92 |
Picard M, Yonekura S, Slowicka K et al. Ileal immune tonus is a prognosis marker of proximal colon cancer in mice and patients. Cell Death Differ 2021;28:1532–47.
|
93 |
Pique N, Berlanga M, Minana-Galbis D. Health benefits of heat-killed (Tyndallized) probiotics: an overview. Int J Mol Sci 2019;20:2534.
|
94 |
Poore GD, Kopylova E, Zhu Q et al. Microbiome analyses of blood and tissues suggest cancer diagnostic approach. Nature 2020;579:567–74.
|
95 |
Principi N, Silvestri E, Esposito S. Advantages and limitations of bacteriophages for the treatment of bacterial infections. Front Pharmacol 2019;10:513.
|
96 |
Pulingam T, Parumasivam T, Gazzali AM et al. Antimicrobial resistance: prevalence, economic burden, mechanisms of resistance and strategies to overcome. Eur J Pharm Sci 2022;170:106103.
|
97 |
Qiao H, Tan X-R, Li H et al. Association of intratumoral microbiota with prognosis in patients with nasopharyngeal carcinoma from 2 hospitals in China. JAMA Oncol 2022;8:1301.
|
98 |
Quispe-Tintaya W, Chandra D, Jahangir A et al. Nontoxic radioactive Listeria(at) is a highly effective therapy against metastatic pancreatic cancer. Proc Natl Acad Sci USA 2013;110:8668–73.
|
99 |
Ren Z, Li A, Jiang J et al. Gut microbiome analysis as a tool towards targeted non-invasive biomarkers for early hepatocellular carcinoma. Gut 2019;68:1014–23.
|
100 |
Ren Z, Chen S, Lv H et al. Effect of Bifidobacterium animalis subsp lactis SF on enhancing the tumor suppression of irinotecan by regulating the intestinal flora. Pharmacol Res 2022;184:106406.
|
101 |
Riehl T, Cohn S, Tessner T et al. Lipopolysaccharide is radioprotective in the mouse intestine through a prostaglandin-mediated mechanism. Gastroenterology 2000;118:1106–16.
|
102 |
Riehl TE, Newberry RD, Lorenz RG et al. TNFR1 mediates the radioprotective effects of lipopolysaccharide in the mouse intestine. Am J Physiol Gastrointest Liver Physiol 2004;286:G166–73.
|
103 |
Riquelme E, Zhang Y, Zhang L et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell 2019;178:795–806.e12.
|
104 |
Routy B, Le Chatelier E, Derosa L et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 2018;359:91–7.
|
105 |
Rovner AJ, Haimovich AD, Katz SR et al. Recoded organisms engineered to depend on synthetic amino acids. Nature 2015;518:89–93.
|
106 |
Salminen S, Collado MC, Endo A et al. The International Scientific Association of Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of postbiotics. Nat Rev Gastroenterol Hepatol 2021;18:649–67.
|
107 |
Salter SJ, Cox MJ, Turek EM et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 2014;12:87.
|
108 |
Schmidt TSB, Li SS, Maistrenko OM et al. Drivers and determinants of strain dynamics following fecal microbiota transplantation. Nat Med 2022;28:1902–12.
|
109 |
Shen S, Lim G, You Z et al. Gut microbiota is critical for the induction of chemotherapy-induced pain. Nat Neurosci 2017;20:1213–6.
|
110 |
Shiao SL, Kershaw KM, Limon JJ et al. Commensal bacteria and fungi differentially regulate tumor responses to radiation therapy. Cancer Cell 2021;39:1202–1213.e6.
|
111 |
Sims TT, El Alam MB, Karpinets TV et al. Gut microbiome diversity is an independent predictor of survival in cervical cancer patients receiving chemoradiation. Commun Biol 2021;4:237.
|
112 |
Singh V, Yeoh BS, Chassaing B et al. Dysregulated microbial fermentation of soluble fiber induces cholestatic liver cancer. Cell 2018;175:679–694.e22.
|
113 |
Singhi AD, Koay EJ, Chari ST et al. Early detection of pancreatic cancer: opportunities and challenges. Gastroenterology 2019;156:2024–40.
|
114 |
Spanogiannopoulos P, Kyaw TS, Guthrie BGH et al. Host and gut bacteria share metabolic pathways for anti-cancer drug metabolism. Nat Microbiol 2022;7:1605–20.
|
115 |
Spencer CN, McQuade JL, Gopalakrishnan V et al. Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response. Science 2021;374:1632–40.
|
116 |
Stirling F, Bitzan L, O’Keefe S et al. Rational design of evolutionarily stable microbial kill switches. Mol Cell 2017;68:686–697.e3.
|
117 |
Stojanovska V, Prakash M, McQuade R et al. Oxaliplatin treatment alters systemic immune responses. Biomed Res Int 2019;2019:4650695.
|
118 |
Su S, Chang L-C, Huang H-D et al. Oral microbial dysbiosis and its performance in predicting oral cancer. Carcinogenesis 2021;42:127–35.
|
119 |
Terrisse S, Derosa L, Iebba V et al. Intestinal microbiota influences clinical outcome and side effects of early breast cancer treatment. Cell Death Differ 2021;28:2778–96.
|
120 |
Tintelnot J, Xu Y, Lesker TR et al. Microbiota-derived 3-IAA influences chemotherapy efficacy in pancreatic cancer. Nature 2023;615:168–74.
|
121 |
Touchefeu Y, Montassier E, Nieman K et al. Systematic review: the role of the gut microbiota in chemotherapyor radiation-induced gastrointestinal mucositis - current evidence and potential clinical applications. Aliment Pharmacol Ther 2014;40:409–21.
|
122 |
Tsay JJ, Wu BG, Sulaiman I et al. Lower airway dysbiosis affects lung cancer progression. Cancer Discov 2021;11:293–307.
|
123 |
Vande Voorde J, Sabuncuoğlu S, Noppen S et al. Nucleoside-catabolizing enzymes in mycoplasma-infected tumor cell cultures compromise the cytostatic activity of the anticancer drug gemcitabine. J Biol Chem 2014;289:13054–65.
|
124 |
Viaud S, Saccheri F, Mignot G et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 2013;342:971–6.
|
125 |
Wallace BD, Wang H, Lane KT et al. Alleviating cancer drug toxicity by inhibiting a bacterial enzyme. Science 2010;330:831–5.
|
126 |
Wan Y, Zuo T. Interplays between drugs and the gut microbiome. Gastroenterol Rep 2022;10:goac009.
|
127 |
Wang SB, Liu XH, Li B et al. Bacteria-assisted selective photothermal therapy for precise tumor inhibition. Adv Funct Mater 2019;29:1904093.
|
128 |
Wang A, Ling Z, Yang Z et al. Gut microbial dysbiosis may predict diarrhea and fatigue in patients undergoing pelvic cancer radiotherapy: a pilot study. PLoS One 2015;10:e0126312.
|
129 |
Wang Y, Wiesnoski DH, Helmink BA et al. Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis. Nat Med 2018;24:1804–8.
|
130 |
Wang M, Rousseau B, Qiu K et al. Killing tumor-associated bacteria with a liposomal antibiotic generates neoantigens that induce anti-tumor immune responses. Nat Biotechnol 2023.
|
131 |
Watanabe T, Nadatani Y, Suda W et al. Long-term persistence of gastric dysbiosis after eradication of Helicobacter pylori in patients who underwent endoscopic submucosal dissection for early gastric cancer. Gastric Cancer 2021;24:710–20.
|
132 |
Weniger M, Hank T, Qadan M et al. Influence of Klebsiella pneumoniae and quinolone treatment on prognosis in patients with pancreatic cancer. Br J Surg 2021;108:709–16.
|
133 |
Wong SH, Kwong TNY, Chow T-C et al. Quantitation of faecal Fusobacterium improves faecal immunochemical test in detecting advanced colorectal neoplasia. Gut 2017;66:1441–8.
|
134 |
Wu P, Zhang G, Zhao J et al. Profiling the urinary microbiota in male patients with bladder cancer in China. Front Cell Infect Microbiol 2018;8:167.
|
135 |
Wu Y, Jiao N, Zhu R et al. Identification of microbial markers across populations in early detection of colorectal cancer. Nat Commun 2021;12.
|
136 |
Yadav M, Chauhan NS. Microbiome therapeutics: exploring the present scenario and challenges. Gastroenterol Rep 2022;10:goab046.
|
137 |
Yamamura K, Baba Y, Nakagawa S et al. Human microbiome Fusobacterium nucleatum in esophageal cancer tissue is associated with prognosis. Clin Cancer Res 2016;22:5574–81.
|
138 |
Yan L, Chen Y, Chen F et al. Effect of Helicobacter pylori eradication on gastric cancer prevention: updated report from a randomized controlled trial with 265 years of follow-up. Gastroenterology 2022;163:154–162.e3.
|
139 |
Yeung C, Chan W-T, Jiang C-B et al. Amelioration of chemotherapy-induced intestinal mucositis by orally administered probiotics in a mouse model. PLoS One 2015;10:e0141402.
|
140 |
Yoon Y, Kim G, Jeon B et al. Bifidobacterium strain-specific enhances the efficacy of cancer therapeutics in tumor-bearing mice. Cancers 2021;13:957.
|
141 |
Yu T, Guo F, Yu Y et al. Fusobacterium nucleatum promotes Chemoresistance to colorectal cancer by modulating autophagy. Cell 2017;170:548–563.e16.
|
142 |
Yuan L, Zhang S, Li H et al. The influence of gut microbiota dysbiosis to the efficacy of 5-Fluorouracil treatment on colorectal cancer. Biomed Pharmacother 2018;108:184–93.
|
143 |
Yuan W, Xiao X, Yu X et al. Probiotic Therapy (BIO-THREE) mitigates intestinal microbial imbalance and intestinal damage caused by oxaliplatin. Probiotics Antimicrob Proteins 2022;14:60–71.
|
144 |
Zhang Y, Zhang Y, Xia L et al. Escherichia coli Nissle 1917 targets and restrains mouse B16 melanoma and 4T1 breast tumors through expression of Azurin Protein. Appl Environ Microbiol 2012;78:7603–10.
|
145 |
Zhang S, Kong C, Yang Y et al. Human oral microbiome dysbiosis as a novel non-invasive biomarker in detection of colorectal cancer. Theranostics 2020a;10:11595–606.
|
146 |
Zhang T, Lu G, Zhao Z et al. Washed microbiota transplantation vs manual fecal microbiota transplantation: clinical findings, animal studies and in vitro screening. Protein Cell 2020b;11:251–66.
|
147 |
Zhang X, Zhang Y, Gui X et al. Salivary Fusobacterium nucleatum serves as a potential biomarker for colorectal cancer. iScience 2022;25:104203.
|
148 |
Zhang Q, Zhao Q, Li T et al. Lactobacillus plantarum-derived indole-3-lactic acid ameliorates colorectal tumorigenesis via epigenetic regulation of CD8+ T cell immunity. Cell Metab 2023;35:943–960.e9.
|
149 |
Zheng D, Dong X, Pan P et al. Phage-guided modulation of the gut microbiota of mouse models of colorectal cancer augments their responses to chemotherapy. Nat Biomed Eng 2019;3:717–28.
|
150 |
Zheng Y, Fang Z, Xue Y et al. Specific gut microbiome signature predicts the early-stage lung cancer. Gut Microbes 2020;11:1030–42.
|
151 |
Zhu D, Zhang J, Luo G et al. Bright bacterium for hypoxia-tolerant photodynamic therapy against orthotopic colon tumors by an interventional method. Adv Sci 2021;8:e2004769.
|
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