Gut microbiota alterations are distinct for primary colorectal cancer and hepatocellular carcinoma

Wei Jia, Cynthia Rajani, Hongxi Xu, Xiaojiao Zheng

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Protein Cell ›› 2021, Vol. 12 ›› Issue (5) : 374-393. DOI: 10.1007/s13238-020-00748-0
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Gut microbiota alterations are distinct for primary colorectal cancer and hepatocellular carcinoma

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Abstract

Colorectal cancer (CRC) and hepatocellular carcinoma (HCC) are the second and third most common causes of death by cancer, respectively. The etiologies of the two cancers are either infectious insult or due to chronic use of alcohol, smoking, diet, obesity and diabetes. Pathological changes in the composition of the gut microbiota that lead to intestinal inflammation are a common factor for both HCC and CRC. However, the gut microbiota of the cancer patient evolves with disease pathogenesis in unique ways that are affected by etiologies and environmental factors. In this review, we examine the changes that occur in the composition of the gut microbiota across the stages of the HCC and CRC. Based on the idea that the gut microbiota are an additional “lifeline” and contribute to the tumor microenvironment, we can observe from previously published literature how the microbiota can cause a shift in the balance from normal → inflammation → diminished inflammation from early to later disease stages. This pattern leads to the hypothesis that tumor survival depends on a less proinflammatory tumor microenvironment. The differences observed in the gut microbiota composition between different disease etiologies as well as between HCC and CRC suggest that the tumor microenvironment is unique for each case.

Keywords

gut microbiota / colorectal cancer / hepatocellular carcinoma

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Wei Jia, Cynthia Rajani, Hongxi Xu, Xiaojiao Zheng. Gut microbiota alterations are distinct for primary colorectal cancer and hepatocellular carcinoma. Protein Cell, 2021, 12(5): 374‒393 https://doi.org/10.1007/s13238-020-00748-0

References

[1]
Aly AM, Adel A, El-Gendy AO, Essam TM, Aziz RK (2016) Gut microbiome alterations in patients with stage 4 hepatitis C. Gut Pathog 8:42
CrossRef Google scholar
[2]
Arthur JC, Perez-Chanona E, Muhlbauer M, Tomkovich S, Uronis JM, Fan TJ, Campbell BJ, Abujamel T, Dogan B, Rogers AB (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338:120–123
CrossRef Google scholar
[3]
Barrett HL, Gomez-Arango LF, Wilkinson SA, McIntyre HD, Callaway LK, Morrison M, Dekker Nitert M (2018) A vegetarian diet is a major determinant of gut microbiota composition in early pregnancy. Nutrients 10:890
CrossRef Google scholar
[4]
Bernstein H, Bernstein C, Payne CM, Dvorakova K, Garewal H (2005) Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res 589:47–65
CrossRef Google scholar
[5]
Bernstein C, Holubec H, Bhattacharyya AK, Nguyen H, Payne CM, Zaitlin B, Bernstein H(2011) Carcinogenicity of deoxycholate, a secondary bile acid. Arch Toxicol 85:863–871
CrossRef Google scholar
[6]
Bluemel S, Wang L, Kuelbs C,Moncera K, Torralba M, Singh H, Fouts DE, Schnabl B (2019) Intestinal and hepatic microbiota changes associated with chronic ethanol administration in mice. Gut Microbes 14:1–11
CrossRef Google scholar
[7]
Boleij A, Hechenbleikner EM, Goodwin AC, Badani R, Stein EM, Lazarev MG, Ellis B, Carroll KC, Albesiano E, Wick EC (2015) The Bacteroides fragilis toxin gene is prevalent in the colon mucosa of colorectal cancer patients. Clin Infect Dis 60:208–215
CrossRef Google scholar
[8]
Chaucer B, Smith N, Beatty D, Yadav M (2018) Multiple hepatic abscess from parvimonas micra: an emerging gastrointestinal microbe. ACG Case Rep J 5:e70
CrossRef Google scholar
[9]
Chen Y, Guo J, Qian G, Fang D, Shi D, Guo L, Li L (2015) Gut dysbiosis in acute-on-chronic liver failure and its predictive value for mortality. J Gastroenterol Hepatol 30:1429–1437
CrossRef Google scholar
[10]
Chen K, Ma J, Jia X, Ai W, Ma Z, Pan Q (2019) Advancing the understanding of NAFLD to hepatocellular carcinoma development: from experimental models to humans. Biochim Biophys Acta Rev Cancer 1871:117–125
CrossRef Google scholar
[11]
Chow MD, Lee YH, Guo GL (2017) The role of bile acids in nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Mol Aspects Med 56:34–44
CrossRef Google scholar
[12]
Chu H, Duan Y, Yang L, Schnabl B (2019) Small metabolites, possible big changes: a microbiota-centered view of nonalcoholic fatty liver disease. Gut 68:359–370
CrossRef Google scholar
[13]
Coppenhagen-Glazer S,Sol A, Abed J,Naor R,Zhang X, Han YW, Bachrach G (2015) Fap2 of Fusobacterium nucleatum is a galactose-inhibitable adhesin involved in coaggregation, cell adhesion, and preterm birth. Infect Immun 83:1104–1113
CrossRef Google scholar
[14]
Cosseau C, Devine DA, Dullaghan E, Gardy JL, Chikatamarla A, Gellatly S, Yu LL, Pistolic J, Falsafi R, Tagg J (2008) The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infect Immun 76:4163–4175
CrossRef Google scholar
[15]
Dai Z, Coker OO, Nakatsu G, Wu WKK, Zhao L, Chen Z, Chan FKL, Kristiansen K, Sung JJY,Wong SH (2018) Multi-cohort analysis of colorectal cancer metagenome identified altered bacteria across populations and universal bacterial markers. Microbiome 6:70
CrossRef Google scholar
[16]
De Simone V, Pallone F,Monteleone G,Stolfi C (2013) Role of TH17 cytokines in the control of colorectal cancer. Oncoimmunology 2: e26617
CrossRef Google scholar
[17]
De Simone V, Franze E, Ronchetti G, Colantoni A,Fantini MC, Di Fusco D, Sica GS, Sileri P, MacDonald TT, Pallone F (2015) Th17-type cytokines, IL-6 and TNF-alpha synergistically activate STAT3 and NF-kB to promote colorectal cancer cell growth. Oncogene 34:3493–3503
CrossRef Google scholar
[18]
Dejong CH, van de Poll MC, Soeters PB, Jalan R, Olde Damink SW (2007) Aromatic amino acid metabolism during liver failure. J Nutr 137:1579S–1585S
CrossRef Google scholar
[19]
Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB (2019) Colorectal cancer. Lancet 394:1467–1480
CrossRef Google scholar
[20]
Despres J, Forano E, Lepercq P, Comtet-Marre S, Jubelin G, Chambon C, Yeoman CJ, Berg Miller ME, Fields CJ, Martens E (2016) Xylan degradation by the human gut Bacteroides xylanisolvens XB1A(T) involves two distinct gene clusters that are linked at the transcriptional level. BMC Genomics 17:326
CrossRef Google scholar
[21]
Feng Q, Liang S, Jia H, Stadlmayr A, Tang L,Lan Z, Zhang D, Xia H, Xu X, Jie Z(2015) Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun 6:6528
CrossRef Google scholar
[22]
Ferreira DM, Afonso MB, Rodrigues PM, Simao AL, Pereira DM, Borralho PM, Rodrigues CM, Castro RE (2014) c-Jun N-terminal kinase 1/c-Jun activation of the p53/microRNA 34a/sirtuin 1 pathway contributes to apoptosis induced by deoxycholic acid in rat liver . Mol Cell Biol 34:1100–1120
CrossRef Google scholar
[23]
Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504:446–450
CrossRef Google scholar
[24]
George J, Pera N, Phung N, Leclercq I, Yun Hou J, Farrell G (2003) Lipid peroxidation, stellate cell activation and hepatic fibrogenesis in a rat model of chronic steatohepatitis. J Hepatol 39:756–764
CrossRef Google scholar
[25]
Giloteaux L, Goodrich JK, Walters WA, Levine SM, Ley RE, Hanson MR (2016) Reduced diversity and altered composition of the gut microbiome in individuals with myalgic encephalomyelitis/chronic fatigue syndrome . Microbiome 4:30
CrossRef Google scholar
[26]
Greathouse KL, Harris CC, Bultman SJ (2015) Dysfunctional families: Clostridium scindens and secondary bile acids inhibit the growth of Clostridium difficile. Cell Metab 21:9–10
CrossRef Google scholar
[27]
Guo W, Tan HY, Wang N, Wang X, Feng Y (2018) Deciphering hepatocellular carcinoma through metabolomics: from biomarker discovery to therapy evaluation. Cancer Manag Res 10:715–734
CrossRef Google scholar
[28]
Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M, Enk J,Bar-On Y, Stanietsky-Kaynan N, Coppenhagen-Glazer S (2015) Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 42:344–355
CrossRef Google scholar
[29]
Heidrich B, Vital M, Plumeier I, Doscher N, Kahl S, Kirschner J, Ziegert S, Solbach P,Lenzen H, Potthoff A(2018) Intestinal microbiota in patients with chronic hepatitis C with and without cirrhosis compared with healthy controls. Liver Int 38:50–58
CrossRef Google scholar
[30]
Hibberd AA, Lyra A, Ouwehand AC, Rolny P, Lindegren H, Cedgard L, Wettergren Y (2017) Intestinal microbiota is altered in patients with colon cancer and modified by probiotic intervention. BMJ Open Gastroenterol 4:e000145
CrossRef Google scholar
[31]
Inoue T, Nakayama J,Moriya K, Kawaratani H, Momoda R, Ito K, Iio E, Nojiri S, Fujiwara K, Yoneda M (2018) Gut dysbiosis associated with hepatitis C virus infection. Clin Infect Dis 67:869–877
CrossRef Google scholar
[32]
Kameyama K, Itoh K (2014) Intestinal colonization by a Lachnospiraceae bacterium contributes to the development of diabetes in obese mice. Microbes Environ 29:427–430
CrossRef Google scholar
[33]
Kim G, Deepinder F, Morales W, Hwang L, Weitsman S, Chang C, Gunsalus R,Pimentel M(2012) Methanobrevibacter smithii is the predominant methanogen in patients with constipation-predominant IBS and methane on breath. Dig Dis Sci 57:3213–3218
CrossRef Google scholar
[34]
Koliaraki V, Pasparakis M, Kollias G (2015) IKKbeta in intestinal mesenchymal cells promotes initiation of colitis-associated cancer . J Exp Med 212:2235–2251
CrossRef Google scholar
[35]
Krenkel O, Tacke F (2017) Liver macrophages in tissue homeostasis and disease. Nat Rev Immunol 17:306–321
CrossRef Google scholar
[36]
La Reau AJ, Suen G (2018) The Ruminococci: key symbionts of the gut ecosystem. J Microbiol 56:199–208
CrossRef Google scholar
[37]
La Rosa SL, Leth ML, Michalak L, Hansen ME, Pudlo NA, Glowacki R, Pereira G,Workman CT , Arntzen MO, Pope PB (2019) The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary beta-mannans. Nat Commun 10:905
CrossRef Google scholar
[38]
Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Starkel P, Windey K, Tremaroli V, Backhed F,Verbeke K (2014) Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci USA 111:E4485–4493
CrossRef Google scholar
[39]
Li J, Stanger BZ (2019) The tumor as organizer model. Science 363:1038–1039
CrossRef Google scholar
[40]
Lin L,Liu A, Peng Z, Lin HJ, Li PK, Li C, Lin J (2011) STAT3 is necessary for proliferation and survival in colon cancer-initiating cells. Cancer Res 71:7226–7237
CrossRef Google scholar
[41]
Liu Q, Li F, Zhuang Y, Xu J, Wang J, Mao X, Zhang Y, Liu X (2019) Alteration in gut microbiota associated with hepatitis B and nonhepatitis virus related hepatocellular carcinoma. Gut Pathog 11:1
CrossRef Google scholar
[42]
Liu X,Cheng Y, Shao L, Ling Z (2020) Alterations of the predominant fecal microbiota and disruption of the gut mucosal barrier in patients with early-stage colorectal cancer. Biomed Res Int 2020:2948282
CrossRef Google scholar
[43]
Long AG, Lundsmith ET, Hamilton KE (2017) Inflammation and colorectal cancer. Curr Colorectal Cancer Rep 13:341–351
CrossRef Google scholar
[44]
Loo TM, Kamachi F, Watanabe Y, Yoshimoto S, Kanda H, Arai Y, Nakajima-Takagi Y, Iwama A, Koga T, Sugimoto Y (2017) Gut microbiota promotes obesity-associated liver cancer through PGE2-mediated suppression of antitumor immunity. Cancer Discov 7:522–538
CrossRef Google scholar
[45]
Lopetuso LR, Scaldaferri F, Petito V, Gasbarrini A (2013) Commensal Clostridia: leading players in the maintenance of gut homeostasis. Gut Pathog 5:23
CrossRef Google scholar
[46]
Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230
CrossRef Google scholar
[47]
Mizutani S, Yamada T, Yachida S (2020) Significance of the gut microbiome in multistep colorectal carcinogenesis. Cancer Sci 111:766–773
CrossRef Google scholar
[48]
Myant KB, Cammareri P, McGhee EJ, Ridgway RA, Huels DJ, Cordero JB, Schwitalla S, Kalna G, Ogg EL, Athineos D (2013) ROS production and NF-kappaB activation triggered by RAC1 facilitate WNT-driven intestinal stem cell proliferation and colorectal cancer initiation. Cell Stem Cell 12:761–773
CrossRef Google scholar
[49]
Nakatsu G, Li X, Zhou H, Sheng J, Wong SH, Wu WK, Ng SC, Tsoi H, Dong Y,Zhang N (2015) Gut mucosal microbiome across stages of colorectal carcinogenesis. Nat Commun 6:8727
CrossRef Google scholar
[50]
O’Callaghan A, van Sinderen D (2016) Bifidobacteria and their role as members of the human gut microbiota. Front Microbiol 7:925
CrossRef Google scholar
[51]
Ohtani N, Kawada N (2019) Role of the gut-liver axis in liver inflammation, fibrosis, and cancer: a special focus on the gut microbiota relationship. Hepatol Commun 3:456–470
CrossRef Google scholar
[52]
Pan HW, Du LT, Li W, Yang YM, Zhang Y, Wang CX (2020) Biodiversity and richness shifts of mucosa-associated gut microbiota with progression of colorectal cancer. Res Microbiol 1:12. https://doi.org/10.1016/j.resmic.2020.01.001
CrossRef Google scholar
[53]
Park CH, Eun CS, Han DS (2018) Intestinal microbiota, chronic inflammation, and colorectal cancer. Intest Res 16:338–345
CrossRef Google scholar
[54]
Patel M, Shariff MI, Ladep NG, Thillainayagam AV, Thomas HC, Khan SA, Taylor-Robinson SD (2012) Hepatocellular carcinoma: diagnostics and screening. J Eval Clin Pract 18:335–342
CrossRef Google scholar
[55]
Pedersen KB, Pulliam CF, Patel A, Del Piero F,Watanabe TTN, Wankhade UD, Shankar K, Hicks C, Ronis MJ (2019) Liver tumorigenesis is promoted by a high saturated fat diet specifically in male mice and is associated with hepatic expression of the proto-oncogene Agap2 and enrichment of the intestinal microbiome with Coprococcus. Carcinogenesis 40:349–359
CrossRef Google scholar
[56]
Petersen C,Round JL (2014) Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol 16:1024–1033
CrossRef Google scholar
[57]
Png CW, Linden SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH (2010) Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 105:2420–2428
CrossRef Google scholar
[58]
Porter NT, Luis AS, Martens EC (2018) Bacteroides thetaiotaomicron. Trends Microbiol 26:966–967
CrossRef Google scholar
[59]
Rao SG, Jackson JG (2016) SASP: tumor suppressor or promoter? Yes! Trends Cancer 2:676–687
CrossRef Google scholar
[60]
Rapozo DC, Bernardazzi C,de Souza HS (2017) Diet and microbiota in inflammatory bowel disease: the gut in disharmony. World J Gastroenterol 23:2124–2140
CrossRef Google scholar
[61]
Rey FE, Faith JJ, Bain J, Muehlbauer MJ, Stevens RD, Newgard CB, Gordon JI (2010) Dissecting the in vivo metabolic potential of two human gut acetogens. J Biol Chem 285:22082–22090
CrossRef Google scholar
[62]
Ridlon JM, Kang DJ, Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47:241–259
CrossRef Google scholar
[63]
Rodier F, Campisi J (2011) Four faces of cellular senescence. J Cell Biol 192:547–556
CrossRef Google scholar
[64]
Rubinstein MR, Wang X, Liu W, Hao Y,Cai G, Han YW (2013) Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe 14:195–206
CrossRef Google scholar
[65]
Saitoh S, Noda S, Aiba Y,Takagi A, Sakamoto M, Benno Y, Koga Y (2002) Bacteroides ovatus as the predominant commensal intestinal microbe causing a systemic antibody response in inflammatory bowel disease. Clin Diagn Lab Immunol 9:54–59
CrossRef Google scholar
[66]
Sakamoto M, Takagaki A, Matsumoto K, Kato Y,Goto K , Benno Y (2009) Butyricimonas synergistica gen. nov., sp. nov. and Butyricimonas virosa sp. nov., butyric acid-producing bacteria in the family ‘Porphyromonadaceae’ isolated from rat faeces. Int J Syst Evol Microbiol 59:1748–1753
CrossRef Google scholar
[67]
Sandhu BK, McBride SM (2018) Clostridioides difficile. Trends Microbiol 26:1049–1050
CrossRef Google scholar
[68]
Schwenger KJP, Chen L, Chelliah A, Da Silva HE, Teterina A, Comelli EM, Taibi A, Arendt BM, Fischer S, Allard JP (2018) Markers of activated inflammatory cells are associated with disease severity and intestinal microbiota in adults with nonalcoholic fatty liver disease. Int J Mol Med 42:2229–2237
CrossRef Google scholar
[69]
Schwitalla S, Fingerle AA, Cammareri P, Nebelsiek T, Goktuna SI, Ziegler PK, Canli O, Heijmans J, Huels DJ, Moreaux G (2013) Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152:25–38
CrossRef Google scholar
[70]
Soeiro C, Quilici IR, Legoff A, Oussalah MB, Morin M, Alauzet C, Charmillon A (2019 ) Hepatic abscess due to Dialister pneumosintes—a case report. Anaerobe 59:35–37
CrossRef Google scholar
[71]
Stenman LK, Holma R, Eggert A, Korpela R (2013) A novel mechanism for gut barrier dysfunction by dietary fat: epithelial disruption by hydrophobic bile acids. Am J Physiol Gastrointest Liver Physiol 304:G227–234
CrossRef Google scholar
[72]
Takeshita K, Mizuno S, Mikami Y, Sujino T, Saigusa K, Matsuoka K, Naganuma M, Sato T, Takada T, Tsuji H (2016) A single species of Clostridium Subcluster XIVa decreased in ulcerative colitis patients. Inflamm Bowel Dis 22:2802–2810
CrossRef Google scholar
[73]
Thota VR, Dacha S, Natarajan A, Nerad J (2011) Eggerthella lenta bacteremia in a Crohn’s disease patient after ileocecal resection. Fut Microbiol 6:595–597
CrossRef Google scholar
[74]
Ullman TA, Itzkowitz SH (2011) Intestinal inflammation and cancer. Gastroenterology 140:1807–1816
CrossRef Google scholar
[75]
Upadhyaya B, McCormack L, Fardin-Kia AR, Juenemann R, Nichenametla S, Clapper J, Specker B, Dey M (2016) Impact of dietary resistant starch type 4 on human gut microbiota and immunometabolic functions. Sci Rep 6:28797
CrossRef Google scholar
[76]
van den Bogert B, Meijerink M, Zoetendal EG, Wells JM, Kleerebezem M (2014) Immunomodulatory properties of Streptococcus and Veillonella isolates from the human small intestine microbiota . PLoS ONE 9:e114277
CrossRef Google scholar
[77]
Voreades N, Kozil A, Weir TL (2014) Diet and the development of the human intestinal microbiome. Front Microbiol 5:494
CrossRef Google scholar
[78]
Wang J, Wang Y, Zhang X, Liu J, Zhang Q, Zhao Y, Peng J, Feng Q, Dai J,Sun S et al (2017) Gut microbial dysbiosis is associated with altered hepatic functions and serum metabolites in chronic hepatitis B patients. Front Microbiol 8:2222
CrossRef Google scholar
[79]
Wang K, Liao M, Zhou N, Bao L, Ma K, Zheng Z, Wang Y, Liu C, Wang W, Wang J(2019) Parabacteroides distasonis alleviates obesity and metabolic dysfunctions via production of succinate and secondary bile acids. Cell Rep 26(222–235):e225
CrossRef Google scholar
[80]
Wexler HM (2007) Bacteroides: the good, the bad, and the nittygritty. Clin Microbiol Rev 20:593–621
CrossRef Google scholar
[81]
Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40:235–243
CrossRef Google scholar
[82]
Wong SH, Zhao L, Zhang X, Nakatsu G, Han J,Xu W, Xiao X, Kwong TNY, Tsoi H, Wu WKK (2017) Gavage of fecal samples from patients with colorectal cancer promotes intestinal carcinogenesis in germ-free and conventional mice. Gastroenterology 153(1621–1633):e1626
CrossRef Google scholar
[83]
Wu P, Wu D, Ni C, Ye J, Chen W, Hu G, Wang Z, Wang C, Zhang Z, Xia W (2014a) gammadeltaT17 cells promote the accumulation and expansion of myeloid-derived suppressor cells in human colorectal cancer. Immunity 40:785–800
CrossRef Google scholar
[84]
Wu YJ, Xu MY, Lu LG (2014b) Clinical advances in fibrosis progression of chronic hepatitis B and C. J Clin Transl Hepatol 2:222–227
[85]
Wu F, Guo X, Zhang J, Zhang M, Ou Z, Peng Y (2017) Phascolarctobacterium faecium abundant colonization in human gastrointestinal tract. Exp Ther Med 14:3122–3126
CrossRef Google scholar
[86]
Wu M, Li P, An Y, Ren J, Yan D, Cui J, Li D, Li M, Wang M, Zhong G (2019) Phloretin ameliorates dextran sulfate sodium-induced ulcerative colitis in mice by regulating the gut microbiota. Pharmacol Res 150:104489
CrossRef Google scholar
[87]
Xavier RJ, Podolsky DK (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448:427–434
CrossRef Google scholar
[88]
Xie G, Wang X, Huang F, Zhao A, Chen W, Yan J, Zhang Y, Lei S, Ge K,Zheng X(2016a) Dysregulated hepatic bile acids collaboratively promote liver carcinogenesis. Int J Cancer 139:1764–1775
CrossRef Google scholar
[89]
Xie G,Wang X, Liu P, Wei R, Chen W, Rajani C, Hernandez BY, Alegado R, Dong B, Li D (2016b) Distinctly altered gut microbiota in the progression of liver disease. Oncotarget 7:19355–19366
CrossRef Google scholar
[90]
Xie YH, Gao QY, Cai GX, Sun XM, Sun XM, Zou TH, Chen HM, Yu SY, Qiu YW, Gu WQ (2017) Fecal Clostridium symbiosum for noninvasive detection of early and advanced colorectal cancer: test and validation studies. EBioMedicine 25:32–40
CrossRef Google scholar
[91]
Yachida S, Mizutani S, Shiroma H, Shiba S, Nakajima T, Sakamoto T, Watanabe H, Masuda K, Nishimoto Y,Kubo M (2019) Metagenomic and metabolomic analyses reveal distinct stagespecific phenotypes of the gut microbiota in colorectal cancer. Nat Med 25:968–976
CrossRef Google scholar
[92]
Yu T, Guo F, Yu Y, Sun T, Ma D, Han J, Qian Y, Kryczek I, Sun D, Nagarsheth N (2017) Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell 170(548–563):e516
CrossRef Google scholar
[93]
Zeng Y, Chen S, Fu Y,Wu W, Chen T, Chen J, Yang B, Ou Q (2020) Gut microbiota dysbiosis in patients with hepatitis B virus-induced chronic liver disease covering chronic hepatitis, liver cirrhosis and hepatocellular carcinoma. J Viral Hepat 27:143–155
CrossRef Google scholar
[94]
Zhang Z, Zhai H, Geng J, Yu R, Ren H, Fan H, Shi P (2013) Largescale survey of gut microbiota associated with MHE Via 16S rRNA-based pyrosequencing. Am J Gastroenterol 108:1601–1611
CrossRef Google scholar
[95]
Zhang Y, Yu X, Yu E, Wang N, Cai Q, Shuai Q, Yan F,Jiang L, Wang H, Liu J (2018) Changes in gut microbiota and plasma inflammatory factors across the stages of colorectal tumorigenesis: a case-control study. BMC Microbiol 18:92
CrossRef Google scholar

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