Emerging clinical relevance of microbiome in cancer: promising biomarkers and therapeutic targets

doi:10.1093/procel/pwad052

Protein Cell

2024, Vol. 15

Issue (4) : 239-260 https://doi.org/10.1093/procel/pwad052

Emerging clinical relevance of microbiome in cancer: promising biomarkers and therapeutic targets

Jia-Hao Dai, Xi-Rong Tan, Han Qiao, Na Liu(

)

State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer Center, Guangzhou 510050, China

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Abstract

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.

Keywords microbiome cancer diagnosis prognosis therapy

Corresponding Author(s): Na Liu

Issue Date: 11 April 2024

Cite this article:

Jia-Hao Dai,Xi-Rong Tan,Han Qiao, et al. Emerging clinical relevance of microbiome in cancer: promising biomarkers and therapeutic targets[J]. Protein Cell, 2024, 15(4): 239-260.

URL:

https://academic.hep.com.cn/pac/EN/10.1093/procel/pwad052
https://academic.hep.com.cn/pac/EN/Y2024/V15/I4/239

1	A Almeida, S Nayfach, M Boland et al. A unified catalog of 204,938 reference genomes from the human gut microbiome. Nat Biotechnol 2021;39:105–14. https://doi.org/10.1038/s41587-020-0603-3
2	EN Baruch, I Youngster, G Ben-Betzalel et al. Fecal microbiota transplant promotes response in immunotherapy-refractory melanoma patients. Science 2021;371:602–9. https://doi.org/10.1126/science.abb5920
3	M Batten, ER Shanahan, IP Silva 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. https://doi.org/10.1158/1538-7445.AM2019-2822
4	KE Beck, JA Blansfield, KQ Tran et al. Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 2006;24:2283–9. https://doi.org/10.1200/JCO.2005.04.5716
5	MJ Bender, AC McPherson, CM Phelps et al. Dietary tryptophan metabolite released by intratumoral Lactobacillus reuteri facilitates immune checkpoint inhibitor treatment. Cell 2023;186:1846–1862.e26. https://doi.org/10.1016/j.cell.2023.03.011
6	AP Bhatt, SJ Pellock, KA Biernat et al. Targeted inhibition of gut bacterial beta-glucuronidase activity enhances anticancer drug efficacy. Proc Natl Acad Sci USA 2020;117:7374–81. https://doi.org/10.1073/pnas.1918095117
7	M Bretthauer, M. Kalager Principles, effectiveness and caveats in screening for cancer. Br J Surg 2013;100:55–65. https://doi.org/10.1002/bjs.8995
8	FP Canale, C Basso, G Antonini et al. Metabolic modulation of tumours with engineered bacteria for immunotherapy. Nature 2021;598:662–6. https://doi.org/10.1038/s41586-021-04003-2
9	AN Chamseddine, M Ducreux, JP Armand et al. Intestinal bacterial beta-glucuronidase as a possible predictive biomarker of irinotecan-induced diarrhea severity. Pharmacol Ther 2019;199:1–5. https://doi.org/10.1016/j.pharmthera.2019.03.002
10	D Chandra, A Jahangir, W Quispe-Tintaya 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. https://doi.org/10.1038/bjc.2013.206
11	N Chaput, P Lepage, C Coutzac et al. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol 2017;28:1368–79. https://doi.org/10.1093/annonc/mdx108
12	W Chen, Y Wang, M Qin et al. Bacteria-driven hypoxia targeting for combined biotherapy and photothermal therapy. ACS Nano 2018;12:5995–6005. https://doi.org/10.1021/acsnano.8b02235
13	J Chen, K Zhao, L. Vitetta Effects of intestinal microbial-elaborated butyrate on oncogenic signaling pathways. Nutrients 2019;11:1026. https://doi.org/10.3390/nu11051026
14	S Chen, W Chieng, S Huang 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. https://doi.org/10.1038/s41598-020-77322-5
15	Y Chen, J Ma, Y Dong et al. Characteristics of gut microbiota in patients with clear cell renal cell carcinoma. Front Microbiol 2022a;13:913718. https://doi.org/10.3389/fmicb.2022.913718
16	F Chen, X Dai, C-C Zhou 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. https://doi.org/10.1136/gutjnl-2020-323476
17	X Chen, S Li, C Lin et al. Isomaltooligosaccharides inhibit early colorectal carcinogenesis in a 1,2-dimethylhydrazine-induced rat model. Front Nutr 2022c;9:995126. https://doi.org/10.3389/fnut.2022.995126
18	YE Chen, D Bousbaine, A Veinbachs et al. Engineered skin bacteria induce antitumor T cell responses against melanoma. Science 2023;380:203–10. https://doi.org/10.1126/science.abp9563
19	Y Cheng, J Du, J Han et al. Polymyxin Battenuates LPS-induced death butaggravates radiation-induced death via TLR4-Myd88-IL-6 pathway. Cell Physiol Biochem 2017;42:1120–6. https://doi.org/10.1159/000478767
20	W Cheng, W Xiang, S Wang et al. Tanshinone IIA ameliorates oxaliplatin-induced neurotoxicity via mitochondrial protection and autophagy promotion. Am J Transl Res 2019;11:3140–9.
21	MA Ciorba, TE Riehl, MS Rao et al. Lactobacillus probiotic protects intestinal epithelium from radiation injury in a TLR-2/cyclo-oxygenase-2-dependent manner. Gut 2012;61:829–38. https://doi.org/10.1136/gutjnl-2011-300367
22	OO Coker, G Nakatsu, RZ Dai et al. Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer. Gut 2019;68:654–62. https://doi.org/10.1136/gutjnl-2018-317178
23	OO Coker, WKK Wu, SH Wong et al. Altered gut archaea composition and interaction with bacteria are associated with colorectal cancer. Gastroenterology 2020;159:1459–1470.e5. https://doi.org/10.1053/j.gastro.2020.06.042
24	OO Coker, C Liu, WKK Wu et al. Altered gut metabolites and microbiota interactions are implicated in colorectal carcinogenesis and can be non-invasive diagnostic biomarkers. Microbiome 2022;10:35. https://doi.org/10.1186/s40168-021-01208-5
25	PA Crawford, JI. Gordon Microbial regulation of intestinal radiosensitivity. Proc Natl Acad Sci USA 2005;102:13254–9. https://doi.org/10.1073/pnas.0504830102
26	M Cui, H Xiao, Y Li et al. Faecal microbiota transplantation protects against radiation-induced toxicity. EMBO Mol Med 2017;9:448–61. https://doi.org/10.15252/emmm.201606932
27	R Daillere, M Vétizou, N Waldschmitt et al. Enterococcus hirae and Barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects. Immunity 2016;45:931–43. https://doi.org/10.1016/j.immuni.2016.09.009
28	D Davar, AK Dzutsev, JA McCulloch et al. Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science 2021;371:595–602. https://doi.org/10.1126/science.abf3363
29	C de Martel, D Georges, F Bray et al. Global burden of cancer attributable to infections in 2018: a worldwide incidence analysis. Lancet Glob Health 2020;8:e180–90. https://doi.org/10.1016/S2214-109X(19)30488-7
30	L Derosa, MD Hellmann, M Spaziano 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. https://doi.org/10.1093/annonc/mdy103
31	D De Ruysscher, G Niedermann, NG Burnet et al. Radiotherapy toxicity. Nat Rev Dis Primers 2019;5:15. https://doi.org/10.1038/s41572-019-0073-4
32	G Deshpande, G Athalye-Jape, S. Patole Para-probiotics for preterm neonates-the next frontier. Nutrients 2018;10:871. https://doi.org/10.3390/nu10070871
33	Y Ding, Y Yan, D Chen 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. https://doi.org/10.1039/C9FO00638A
34	X Ding, Q Li, P Li et al. Fecal microbiota transplantation: a promising treatment for radiation enteritis? Radiother Oncol 2020;143:12–8. https://doi.org/10.1016/j.radonc.2020.01.011
35	AB Dohlman, J Klug, M Mesko et al. A pan-cancer mycobiome analysis reveals fungal involvement in gastrointestinal and lung tumors. Cell 2022;185:3807–3822.e12. https://doi.org/10.1016/j.cell.2022.09.015
36	X Dong, P Pan, D-W Zheng et al. Bioinorganic hybrid bacteriophage for modulation of intestinal microbiota to remodel tumor-immune microenvironment against colorectal cancer. Sci Adv 2020;6:eaba1590. https://doi.org/10.1126/sciadv.aba1590
37	K Dubin, MK Callahan, B Ren et al. Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nat Commun 2016;7:10391. https://doi.org/10.1038/ncomms10391
38	LJ Egan, L Eckmann, FR Greten 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. https://doi.org/10.1073/pnas.0306734101
39	R Eisenhofer, JJ Minich, C Marotz et al. Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends Microbiol 2019;27:105–17. https://doi.org/10.1016/j.tim.2018.11.003
40	JR Erb-Downward, NR Falkowski, JC D’Souza et al. Critical relevance of stochastic effects on low-bacterial-biomass 16S rRNA gene analysis. mBio 2020;11:e00258–20. https://doi.org/10.1128/mBio.00258-20
41	S Federici, S Kredo-Russo, R Valdés-Mas 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	B Flemer, RD Warren, MP Barrett et al. The oral microbiota in colorectal cancer is distinctive and predictive. Gut 2018;67:1454–63. https://doi.org/10.1136/gutjnl-2017-314814
43	LT Geller, M Barzily-Rokni, T Danino et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science 2017;357:1156–60. https://doi.org/10.1126/science.aah5043
44	GR Gibson, R Hutkins, ME Sanders 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. https://doi.org/10.1038/nrgastro.2017.75
45	L Gogokhia, K Buhrke, R Bell et al. Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Cell Host Microbe 2019;25:285–299.e8. https://doi.org/10.1016/j.chom.2019.01.008
46	V Gopalakrishnan, CN Spencer, L Nezi et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 2018;359:97–103. https://doi.org/10.1126/science.aan4236
47	M Guenther, M Haas, V Heinemann 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. https://doi.org/10.1038/s41416-020-01029-7
48	J Guo, Y Chen, X Lei et al. Monophosphoryl lipid a attenuates radiation injury through TLR4 activation. Oncotarget 2017;8:86031–42. https://doi.org/10.18632/oncotarget.20907
49	J Han, Z-H Tao, J-L Wang et al. Microbiota-derived tryptophan catabolites mediate the chemopreventive effects of statins on colorectal cancer. Nat Microbiol 2023;8:919–33. https://doi.org/10.1038/s41564-023-01363-5
50	Y He, W Wu, H-M Zheng et al. Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat Med 2018;24:1532–5. https://doi.org/10.1038/s41591-018-0164-x
51	L He, H Yang, J Tang 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. https://doi.org/10.1186/s13036-019-0189-9
52	K Hezaveh, RS Shinde, A Klötgen 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. https://doi.org/10.1016/j.immuni.2022.01.006
53	ZC Holmes, MM Villa, HK Durand et al. Microbiota responses to different prebiotics are conserved within individuals and associated with habitual fiber intake. Microbiome 2022;10:114. https://doi.org/10.1186/s40168-022-01307-x
54	B Hong, T Sobue, L Choquette et al. Chemotherapy-induced oral mucositis is associated with detrimental bacterial dysbiosis. Microbiome 2019;7:1–18. https://doi.org/10.1186/s40168-019-0679-5
55	Y Hsieh, S-Y Tung, H-Y Pan et al. Fusobacterium nucleatum colonization is associated with decreased survival of Helicobacter pylori-positive gastric cancer patients. World J Gastroenterol 2021;27:7311–23. https://doi.org/10.3748/wjg.v27.i42.7311
56	C Hsueh, H-C Lau, Q Huang 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. https://doi.org/10.1002/cncr.34338
57	S Huang, J Chen, L-Y Lian et al. Intratumoral levels and prognostic significance of Fusobacterium nucleatum in cervical carcinoma. Aging 2020;12:23337–50. https://doi.org/10.18632/aging.104188
58	E Hughes, M Scurr, E Campbell et al. T-cell modulation by cyclophosphamide for tumour therapy. Immunology 2018;154:62–8. https://doi.org/10.1111/imm.12913
59	N Iida, A Dzutsev, CA Stewart et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 2013;342:967–70. https://doi.org/10.1126/science.1240527
60	G Kang, D-R Jung, YH Lee et al. Dynamics of fecal microbiota with and without invasive cervical cancer and its application in early diagnosis. Cancers 2020;12:3800. https://doi.org/10.3390/cancers12123800
61	G Kang, D-R Jung, YH Lee et al. Potential association between vaginal microbiota and cervical carcinogenesis in Korean women: a cohort study. Microorganisms 2021;9:294. https://doi.org/10.3390/microorganisms9020294
62	E Kartal, TSB Schmidt, E Molina-Montes et al. MAGIC Study investigators. A faecal microbiota signature with high specificity for pancreatic cancer. Gut 2022;71:1359–72. https://doi.org/10.1136/gutjnl-2021-324755
63	S Kato, N Hamouda, Y Kano 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. https://doi.org/10.1111/1440-1681.12792
64	T Kodawara, T Higashi, Y Negoro 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. https://doi.org/10.1111/bcpt.12511
65	TNY Kwong, X Wang, G Nakatsu et al. Association between bacteremia from specific microbes and subsequent diagnosis of colorectal cancer. Gastroenterology 2018;155:383–390.e8. https://doi.org/10.1053/j.gastro.2018.04.028
66	S Lee, S-Y Cho, Y Yoon et al. Bifidobacterium bifidum strains synergize with immune checkpoint inhibitors to reduce tumour burden in mice. Nat Microbiol 2021;6:277–88. https://doi.org/10.1038/s41564-020-00831-6
67	HL Li, L Lu, XS Wang et al. Alteration of gut microbiota and inflammatory cytokine/chemokine profiles in 5-fluorouracil induced intestinal mucositis. Front Cell Infect Microbiol 2017;7:455. https://doi.org/10.3389/fcimb.2017.00455
68	Z Li, R Fu, X Wen 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. https://doi.org/10.3389/fphys.2022.1089539
69	JQ Liang, SH Wong, CH Szeto et al. Fecal microbial DNA markers serve for screening colorectal neoplasm in asymptomatic subjects. J Gastroenterol Hepatol 2021;36:1035–43. https://doi.org/10.1111/jgh.15171
70	MY Lim, S Hong, KH Hwang et al. Diagnostic and prognostic potential of the oral and gut microbiome for lung adenocarcinoma. Clin Transl Med 2021;11:e508. https://doi.org/10.1002/ctm2.508
71	Y Lin, HC Lau, Y Liu 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. https://doi.org/10.1053/j.gastro.2022.06.038
72	YH Linn, KK Thu, NHH. Win 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. https://doi.org/10.1007/s12602-018-9408-9
73	D Liu, Y Hu, Y Guo et al. Mycoplasma-associated multi-drug resistance of hepatocarcinoma cells requires the interaction of P37 and Annexin A2. PLoS One 2017;12:e0184578. https://doi.org/10.1371/journal.pone.0184578
74	N Liu, N Jiao, J-C Tan et al. Multi-kingdom microbiota analyses identify bacterial-fungal interactions and biomarkers of colorectal cancer across cohorts. Nat Microbiol 2022;7:238–50. https://doi.org/10.1038/s41564-021-01030-7
75	Y Lu, X Yuan, M Wang et al. Gut microbiota influence immunotherapy responses: mechanisms and therapeutic strategies. J Hematol Oncol 2022;15:47. https://doi.org/10.1186/s13045-022-01273-9
76	C Ma, M Han, B Heinrich et al. Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science 2018;360:eaan5931. https://doi.org/10.1126/science.aan5931
77	C Ma, K Chen, Y Wang et al. Establishing a novel colorectal cancer predictive model based on unique gut microbial single nucleotide variant markers. Gut Microbes 2021;13:1–6. https://doi.org/10.1080/19490976.2020.1869505
78	DJ Mandell, MJ Lajoie, MT Mee et al. Biocontainment of genetically modified organisms by synthetic protein design. Nature 2015;518:55–60. https://doi.org/10.1038/nature14121
79	C Manichanh, E Varela, C Martinez et al. The gut microbiota predispose to the pathophysiology of acute postradiotherapy diarrhea. Am J Gastroenterol 2008;103:1754–61. https://doi.org/10.1111/j.1572-0241.2008.01868.x
80	O Manor, CL Dai, SA Kornilov et al. Health and disease markers correlate with gut microbiome composition across thousands of people. Nat Commun 2020;11:5206. https://doi.org/10.1038/s41467-020-18871-1
81	C Marcella, B Cui, CR Kelly 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. https://doi.org/10.1111/apt.16148
82	JA McCulloch, D Davar, RR Rodrigues 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. https://doi.org/10.1038/s41591-022-01698-2
83	K Mima, R Nishihara, ZR Qian et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 2016;65:1973–80. https://doi.org/10.1136/gutjnl-2015-310101
84	N Nagata, S Nishijima, Y Kojima et al. Metagenomic identification of microbial signatures predicting pancreatic cancer from a multinational study. Gastroenterology 2022;163:222–38. https://doi.org/10.1053/j.gastro.2022.03.054
85	G Nakatsu, H Zhou, WKK Wu et al. Alterations in enteric virome are associated with colorectal cancer and survival outcomes. Gastroenterology 2018;155:529–541.e5. https://doi.org/10.1053/j.gastro.2018.04.018
86	L Narunsky-Haziza, GD Sepich-Poore, I Livyatan et al. Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions. Cell 2022;185:3789–3806.e17. https://doi.org/10.1016/j.cell.2022.09.005
87	D Nejman, I Livyatan, G Fuks et al. The human tumor microbiome is composed of tumor type-specific intracellular bacteria. Science 2020;368:973–80. https://doi.org/10.1126/science.aay9189
88	JLG Nino, H Wu, KD LaCourse et al. Effect of the intratumoral microbiota on spatial and cellular heterogeneity in cancer. Nature 2022;611:810. https://doi.org/10.1038/s41586-022-05435-0
89	EM Park, M Chelvanambi, N Bhutiani et al. Targeting the gut and tumor microbiota in cancer. Nat Med 2022;28:690–703. https://doi.org/10.1038/s41591-022-01779-2
90	Z Peng, S Cheng, Y Kou 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. https://doi.org/10.1158/2326-6066.CIR-19-1014
91	DE Peterson, CB Boers-Doets, RJ Bensadoun 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. https://doi.org/10.1093/annonc/mdv202
92	M Picard, S Yonekura, K Slowicka et al. Ileal immune tonus is a prognosis marker of proximal colon cancer in mice and patients. Cell Death Differ 2021;28:1532–47. https://doi.org/10.1038/s41418-020-00684-w
93	N Pique, M Berlanga, D. Minana-Galbis Health benefits of heat-killed (Tyndallized) probiotics: an overview. Int J Mol Sci 2019;20:2534. https://doi.org/10.3390/ijms20102534
94	GD Poore, E Kopylova, Q Zhu et al. Microbiome analyses of blood and tissues suggest cancer diagnostic approach. Nature 2020;579:567–74. https://doi.org/10.1038/s41586-020-2095-1
95	N Principi, E Silvestri, S. Esposito Advantages and limitations of bacteriophages for the treatment of bacterial infections. Front Pharmacol 2019;10:513. https://doi.org/10.3389/fphar.2019.00513
96	T Pulingam, T Parumasivam, AM Gazzali et al. Antimicrobial resistance: prevalence, economic burden, mechanisms of resistance and strategies to overcome. Eur J Pharm Sci 2022;170:106103. https://doi.org/10.1016/j.ejps.2021.106103
97	H Qiao, X-R Tan, H Li et al. Association of intratumoral microbiota with prognosis in patients with nasopharyngeal carcinoma from 2 hospitals in China. JAMA Oncol 2022;8:1301. https://doi.org/10.1001/jamaoncol.2022.2810
98	W Quispe-Tintaya, D Chandra, A Jahangir et al. Nontoxic radioactive Listeria(at) is a highly effective therapy against metastatic pancreatic cancer. Proc Natl Acad Sci USA 2013;110:8668–73. https://doi.org/10.1073/pnas.1211287110
99	Z Ren, A Li, J Jiang et al. Gut microbiome analysis as a tool towards targeted non-invasive biomarkers for early hepatocellular carcinoma. Gut 2019;68:1014–23. https://doi.org/10.1136/gutjnl-2017-315084
100	Z Ren, S Chen, H Lv 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. https://doi.org/10.1016/j.phrs.2022.106406
101	T Riehl, S Cohn, T Tessner et al. Lipopolysaccharide is radioprotective in the mouse intestine through a prostaglandin-mediated mechanism. Gastroenterology 2000;118:1106–16. https://doi.org/10.1016/S0016-5085(00)70363-5
102	TE Riehl, RD Newberry, RG Lorenz et al. TNFR1 mediates the radioprotective effects of lipopolysaccharide in the mouse intestine. Am J Physiol Gastrointest Liver Physiol 2004;286:G166–73. https://doi.org/10.1152/ajpgi.00537.2002
103	E Riquelme, Y Zhang, L Zhang et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell 2019;178:795–806.e12. https://doi.org/10.1016/j.cell.2019.07.008
104	B Routy, E Le Chatelier, L Derosa et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 2018;359:91–7. https://doi.org/10.1126/science.aan3706
105	AJ Rovner, AD Haimovich, SR Katz et al. Recoded organisms engineered to depend on synthetic amino acids. Nature 2015;518:89–93. https://doi.org/10.1038/nature14095
106	S Salminen, MC Collado, A Endo 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. https://doi.org/10.1038/s41575-021-00440-6
107	SJ Salter, MJ Cox, EM Turek et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 2014;12:87. https://doi.org/10.1186/s12915-014-0087-z
108	TSB Schmidt, SS Li, OM Maistrenko et al. Drivers and determinants of strain dynamics following fecal microbiota transplantation. Nat Med 2022;28:1902–12. https://doi.org/10.1038/s41591-022-01913-0
109	S Shen, G Lim, Z You et al. Gut microbiota is critical for the induction of chemotherapy-induced pain. Nat Neurosci 2017;20:1213–6. https://doi.org/10.1038/nn.4606
110	SL Shiao, KM Kershaw, JJ Limon et al. Commensal bacteria and fungi differentially regulate tumor responses to radiation therapy. Cancer Cell 2021;39:1202–1213.e6. https://doi.org/10.1016/j.ccell.2021.07.002
111	TT Sims, MB El Alam, TV Karpinets et al. Gut microbiome diversity is an independent predictor of survival in cervical cancer patients receiving chemoradiation. Commun Biol 2021;4:237. https://doi.org/10.1038/s42003-021-01741-x
112	V Singh, BS Yeoh, B Chassaing et al. Dysregulated microbial fermentation of soluble fiber induces cholestatic liver cancer. Cell 2018;175:679–694.e22. https://doi.org/10.1016/j.cell.2018.09.004
113	AD Singhi, EJ Koay, ST Chari et al. Early detection of pancreatic cancer: opportunities and challenges. Gastroenterology 2019;156:2024–40. https://doi.org/10.1053/j.gastro.2019.01.259
114	P Spanogiannopoulos, TS Kyaw, BGH Guthrie et al. Host and gut bacteria share metabolic pathways for anti-cancer drug metabolism. Nat Microbiol 2022;7:1605–20. https://doi.org/10.1038/s41564-022-01226-5
115	CN Spencer, JL McQuade, V Gopalakrishnan et al. Dietary fiber and probiotics influence the gut microbiome and melanoma immunotherapy response. Science 2021;374:1632–40. https://doi.org/10.1126/science.aaz7015
116	F Stirling, L Bitzan, S O’Keefe et al. Rational design of evolutionarily stable microbial kill switches. Mol Cell 2017;68:686–697.e3. https://doi.org/10.1016/j.molcel.2017.10.033
117	V Stojanovska, M Prakash, R McQuade et al. Oxaliplatin treatment alters systemic immune responses. Biomed Res Int 2019;2019:4650695. https://doi.org/10.1155/2019/4650695
118	S Su, L-C Chang, H-D Huang et al. Oral microbial dysbiosis and its performance in predicting oral cancer. Carcinogenesis 2021;42:127–35. https://doi.org/10.1093/carcin/bgaa062
119	S Terrisse, L Derosa, V Iebba et al. Intestinal microbiota influences clinical outcome and side effects of early breast cancer treatment. Cell Death Differ 2021;28:2778–96. https://doi.org/10.1038/s41418-021-00784-1
120	J Tintelnot, Y Xu, TR Lesker et al. Microbiota-derived 3-IAA influences chemotherapy efficacy in pancreatic cancer. Nature 2023;615:168–74. https://doi.org/10.1038/s41586-023-05728-y
121	Y Touchefeu, E Montassier, K Nieman 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. https://doi.org/10.1111/apt.12878
122	JJ Tsay, BG Wu, I Sulaiman et al. Lower airway dysbiosis affects lung cancer progression. Cancer Discov 2021;11:293–307. https://doi.org/10.1158/2159-8290.CD-20-0263
123	J Vande Voorde, S Sabuncuoğlu, S Noppen 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. https://doi.org/10.1074/jbc.M114.558924
124	S Viaud, F Saccheri, G Mignot et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 2013;342:971–6. https://doi.org/10.1126/science.1240537
125	BD Wallace, H Wang, KT Lane et al. Alleviating cancer drug toxicity by inhibiting a bacterial enzyme. Science 2010;330:831–5. https://doi.org/10.1126/science.1191175
126	Y Wan, T. Zuo Interplays between drugs and the gut microbiome. Gastroenterol Rep 2022;10:goac009. https://doi.org/10.1093/gastro/goac009
127	SB Wang, XH Liu, B Li et al. Bacteria-assisted selective photothermal therapy for precise tumor inhibition. Adv Funct Mater 2019;29:1904093. https://doi.org/10.1002/adfm.201904093
128	A Wang, Z Ling, Z Yang et al. Gut microbial dysbiosis may predict diarrhea and fatigue in patients undergoing pelvic cancer radiotherapy: a pilot study. PLoS One 2015;10:e0126312. https://doi.org/10.1371/journal.pone.0126312
129	Y Wang, DH Wiesnoski, BA Helmink et al. Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis. Nat Med 2018;24:1804–8. https://doi.org/10.1038/s41591-018-0238-9
130	M Wang, B Rousseau, K Qiu et al. Killing tumor-associated bacteria with a liposomal antibiotic generates neoantigens that induce anti-tumor immune responses. Nat Biotechnol 2023. https://doi.org/10.1038/s41587-023-01957-8
131	T Watanabe, Y Nadatani, W Suda 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. https://doi.org/10.1007/s10120-020-01141-w
132	M Weniger, T Hank, M Qadan et al. Influence of Klebsiella pneumoniae and quinolone treatment on prognosis in patients with pancreatic cancer. Br J Surg 2021;108:709–16. https://doi.org/10.1002/bjs.12003
133	SH Wong, TNY Kwong, T-C Chow et al. Quantitation of faecal Fusobacterium improves faecal immunochemical test in detecting advanced colorectal neoplasia. Gut 2017;66:1441–8. https://doi.org/10.1136/gutjnl-2016-312766
134	P Wu, G Zhang, J Zhao et al. Profiling the urinary microbiota in male patients with bladder cancer in China. Front Cell Infect Microbiol 2018;8:167. https://doi.org/10.3389/fcimb.2018.00167
135	Y Wu, N Jiao, R Zhu et al. Identification of microbial markers across populations in early detection of colorectal cancer. Nat Commun 2021;12. https://doi.org/10.1038/s41467-021-23265-y
136	M Yadav, NS. Chauhan Microbiome therapeutics: exploring the present scenario and challenges. Gastroenterol Rep 2022;10:goab046. https://doi.org/10.1093/gastro/goab046
137	K Yamamura, Y Baba, S Nakagawa et al. Human microbiome Fusobacterium nucleatum in esophageal cancer tissue is associated with prognosis. Clin Cancer Res 2016;22:5574–81. https://doi.org/10.1158/1078-0432.CCR-16-1786
138	L Yan, Y Chen, F Chen 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. https://doi.org/10.1053/j.gastro.2022.03.039
139	C Yeung, W-T Chan, C-B Jiang et al. Amelioration of chemotherapy-induced intestinal mucositis by orally administered probiotics in a mouse model. PLoS One 2015;10:e0141402. https://doi.org/10.1371/journal.pone.0141402
140	Y Yoon, G Kim, B Jeon et al. Bifidobacterium strain-specific enhances the efficacy of cancer therapeutics in tumor-bearing mice. Cancers 2021;13:957. https://doi.org/10.3390/cancers13050957
141	T Yu, F Guo, Y Yu et al. Fusobacterium nucleatum promotes Chemoresistance to colorectal cancer by modulating autophagy. Cell 2017;170:548–563.e16. https://doi.org/10.1016/j.cell.2017.07.008
142	L Yuan, S Zhang, H Li et al. The influence of gut microbiota dysbiosis to the efficacy of 5-Fluorouracil treatment on colorectal cancer. Biomed Pharmacother 2018;108:184–93. https://doi.org/10.1016/j.biopha.2018.08.165
143	W Yuan, X Xiao, X Yu et al. Probiotic Therapy (BIO-THREE) mitigates intestinal microbial imbalance and intestinal damage caused by oxaliplatin. Probiotics Antimicrob Proteins 2022;14:60–71. https://doi.org/10.1007/s12602-021-09795-3
144	Y Zhang, Y Zhang, L Xia 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. https://doi.org/10.1128/AEM.01390-12
145	S Zhang, C Kong, Y Yang et al. Human oral microbiome dysbiosis as a novel non-invasive biomarker in detection of colorectal cancer. Theranostics 2020a;10:11595–606. https://doi.org/10.7150/thno.49515
146	T Zhang, G Lu, Z Zhao et al. Washed microbiota transplantation vs manual fecal microbiota transplantation: clinical findings, animal studies and in vitro screening. Protein Cell 2020b;11:251–66. https://doi.org/10.1007/s13238-019-00684-8
147	X Zhang, Y Zhang, X Gui et al. Salivary Fusobacterium nucleatum serves as a potential biomarker for colorectal cancer. iScience 2022;25:104203. https://doi.org/10.1016/j.isci.2022.104203
148	Q Zhang, Q Zhao, T Li 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. https://doi.org/10.1016/j.cmet.2023.04.015
149	D Zheng, X Dong, P Pan 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. https://doi.org/10.1038/s41551-019-0423-2
150	Y Zheng, Z Fang, Y Xue et al. Specific gut microbiome signature predicts the early-stage lung cancer. Gut Microbes 2020;11:1030–42. https://doi.org/10.1080/19490976.2020.1737487
151	D Zhu, J Zhang, G Luo et al. Bright bacterium for hypoxia-tolerant photodynamic therapy against orthotopic colon tumors by an interventional method. Adv Sci 2021;8:e2004769. https://doi.org/10.1002/advs.202004769

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