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Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Review Article

Roles of Gut Microbiota in Colorectal Carcinogenesis Providing a Perspective for Early Diagnosis and Treatment

Author(s): Roghayeh Nouri, Alka Hasani, Mohammad Asgharzadeh, Fatemeh Yeganeh Sefidan, Fatemeh Hemmati and Mohammad Ahangarzadeh Rezaee*

Volume 23, Issue 13, 2022

Published on: 21 April, 2022

Page: [1569 - 1580] Pages: 12

DOI: 10.2174/1389201023666220307112413

Price: $65

Abstract

Colorectal cancer (CRC) is the third most prevalent malignant neoplasm in the world. CRC is influenced by both environmental and genetic factors. Through toxin-mediated DNA damage and the promotion of persistent dysregulated inflammation, the gut microbiota plays a crucial role in the development of CRC. In this review, we discussed the correlation between the bacterial microbiota and CRC carcinogenesis as well as the mechanism by which Streptococcus bovis/gallolyticus, Fusobacterium nucleatum, Bacteroides fragilis, and Escherichia coli can cause CRC.

Keywords: Gut microbiota, bacteria, colorectal cancer, carcinogenesis, inflammation, genotoxicity.

Graphical Abstract

[1]
Saus, E.; Iraola-Guzmán, S.; Willis, J.R.; Brunet-Vega, A.; Gabaldón, T. Microbiome and colorectal cancer: Roles in carcinogenesis and clinical potential. Mol. Aspects Med., 2019, 69, 93-106.
[http://dx.doi.org/10.1016/j.mam.2019.05.001] [PMID: 31082399]
[2]
Bundgaard-Nielsen, C.; Baandrup, U.T.; Nielsen, L.P.; Sørensen, S. The presence of bacteria varies between colorectal adenocarcinomas, precursor lesions and non-malignant tissue. BMC Cancer, 2019, 19(1), 399.
[http://dx.doi.org/10.1186/s12885-019-5571-y] [PMID: 31035942]
[3]
Al-Sohaily, S.; Biankin, A.; Leong, R.; Kohonen-Corish, M.; Warusavitarne, J. Molecular pathways in colorectal cancer. J. Gastroenterol. Hepatol., 2012, 27(9), 1423-1431.
[http://dx.doi.org/10.1111/j.1440-1746.2012.07200.x] [PMID: 22694276]
[4]
Vivarelli, S.; Salemi, R.; Candido, S.; Falzone, L.; Santagati, M.; Stefani, S.; Torino, F.; Banna, G.L.; Tonini, G.; Libra, M. Gut microbiota and cancer: From pathogenesis to therapy. Cancers (Basel), 2019, 11(1), 38.
[http://dx.doi.org/10.3390/cancers11010038] [PMID: 30609850]
[5]
Koliarakis, I.; Messaritakis, I.; Nikolouzakis, T.K.; Hamilos, G.; Souglakos, J.; Tsiaoussis, J. Oral bacteria and intestinal dysbiosis in colo-rectal cancer. Int. J. Mol. Sci., 2019, 20(17), 4146.
[http://dx.doi.org/10.3390/ijms20174146] [PMID: 31450675]
[6]
Chen, G.Y. The role of the gut microbiome in colorectal cancer. Clin. Colon Rectal Surg., 2018, 31(3), 192-198.
[http://dx.doi.org/10.1055/s-0037-1602239] [PMID: 29720905]
[7]
Kong, F.; Cai, Y. Study insights into gastrointestinal cancer through the gut microbiota. BioMed Res. Int., 2019, 2019, 8721503.
[http://dx.doi.org/10.1155/2019/8721503] [PMID: 31341907]
[8]
Chen, J.; Domingue, J.C.; Sears, C.L. Microbiota dysbiosis in select human cancers: evidence of association and causality. In: Semin. Im-munol; Elsevier, 2017, pp. 25-34.
[http://dx.doi.org/10.1016/j.smim.2017.08.001]
[9]
Gao, R.; Wang, Z.; Li, H.; Cao, Z.; Gao, Z.; Chen, H.; Zhang, X.; Pan, D.; Yang, R.; Zhong, H.; Shen, R.; Yin, L.; Jia, Z.; Shen, T.; Qin, N.; Hu, Z.; Qin, H. Gut microbiota dysbiosis signature is associated with the colorectal carcinogenesis sequence and improves the diagnosis of colorectal lesions. J. Gastroenterol. Hepatol., 2020, 35(12), 2109-2121.
[http://dx.doi.org/10.1111/jgh.15077] [PMID: 32337748]
[10]
Vacante, M.; Ciuni, R.; Basile, F.; Biondi, A. Gut microbiota and colorectal cancer development: A closer look to the adenoma-carcinoma sequence. Biomedicines, 2020, 8(11), 489.
[http://dx.doi.org/10.3390/biomedicines8110489] [PMID: 33182693]
[11]
Haghi, F.; Goli, E.; Mirzaei, B.; Zeighami, H. The association between fecal enterotoxigenic B. fragilis with colorectal cancer. BMC Cancer, 2019, 19(1), 879.
[http://dx.doi.org/10.1186/s12885-019-6115-1] [PMID: 31488085]
[12]
Kostic, A.D.; Chun, E.; Robertson, L.; Glickman, J.N.; Gallini, C.A.; Michaud, M.; Clancy, T.E.; Chung, D.C.; Lochhead, P.; Hold, G.L.; El-Omar, E.M.; Brenner, D.; Fuchs, C.S.; Meyerson, M.; Garrett, W.S. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe, 2013, 14(2), 207-215.
[http://dx.doi.org/10.1016/j.chom.2013.07.007] [PMID: 23954159]
[13]
Thiele Orberg, E.; Fan, H.; Tam, A.J.; Dejea, C.M.; Destefano Shields, C.E.; Wu, S.; Chung, L.; Finard, B.B.; Wu, X.; Fathi, P.; Ganguly, S.; Fu, J.; Pardoll, D.M.; Sears, C.L.; Housseau, F. The myeloid immune signature of enterotoxigenic Bacteroides fragilis-induced murine co-lon tumorigenesis. Mucosal Immunol., 2017, 10(2), 421-433.
[http://dx.doi.org/10.1038/mi.2016.53] [PMID: 27301879]
[14]
Bonnet, M.; Buc, E.; Sauvanet, P.; Darcha, C.; Dubois, D.; Pereira, B.; Déchelotte, P.; Bonnet, R.; Pezet, D.; Darfeuille-Michaud, A. Coloni-zation of the human gut by E. coli and colorectal cancer risk. Clin. Cancer Res., 2014, 20(4), 859-867.
[http://dx.doi.org/10.1158/1078-0432.CCR-13-1343] [PMID: 24334760]
[15]
Lopès, A.; Billard, E.; Casse, A.H.; Villéger, R.; Veziant, J.; Roche, G.; Carrier, G.; Sauvanet, P.; Briat, A.; Pagès, F.; Naimi, S.; Pezet, D.; Barnich, N.; Dumas, B.; Bonnet, M. Colibactin-positive Escherichia coli induce a procarcinogenic immune environment leading to immu-notherapy resistance in colorectal cancer. Int. J. Cancer, 2020, 146(11), 3147-3159.
[http://dx.doi.org/10.1002/ijc.32920] [PMID: 32037530]
[16]
Wei, Z.; Cao, S.; Liu, S.; Yao, Z.; Sun, T.; Li, Y.; Li, J.; Zhang, D.; Zhou, Y. Could gut microbiota serve as prognostic biomarker associat-ed with colorectal cancer patients’ survival? A pilot study on relevant mechanism. Oncotarget, 2016, 7(29), 46158-46172.
[http://dx.doi.org/10.18632/oncotarget.10064] [PMID: 27323816]
[17]
Temraz, S.; Nassar, F.; Nasr, R.; Charafeddine, M.; Mukherji, D.; Shamseddine, A. Gut microbiome: A promising biomarker for immuno-therapy in colorectal cancer. Int. J. Mol. Sci., 2019, 20(17), 4155.
[http://dx.doi.org/10.3390/ijms20174155] [PMID: 31450712]
[18]
Ai, D.; Pan, H.; Han, R.; Li, X.; Liu, G.; Xia, L.C. Using decision tree aggregation with random forest model to identify gut microbes asso-ciated with colorectal cancer. Genes (Basel), 2019, 10(2), 112.
[http://dx.doi.org/10.3390/genes10020112] [PMID: 30717284]
[19]
Flemer, B.; Lynch, D.B.; Brown, J.M.; Jeffery, I.B.; Ryan, F.J.; Claesson, M.J.; O’Riordain, M.; Shanahan, F.; O’Toole, P.W. Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut, 2017, 66(4), 633-643.
[http://dx.doi.org/10.1136/gutjnl-2015-309595] [PMID: 26992426]
[20]
Wu, J.; Li, Q.; Fu, X. Fusobacterium nucleatum contributes to the carcinogenesis of colorectal cancer by inducing inflammation and sup-pressing host immunity. Transl. Oncol., 2019, 12(6), 846-851.
[http://dx.doi.org/10.1016/j.tranon.2019.03.003] [PMID: 30986689]
[21]
Wei, T-T.; Lin, Y-T.; Tseng, R-Y.; Shun, C-T.; Lin, Y-C.; Wu, M-S.; Fang, J-M.; Chen, C-C. Prevention of colitis and colitis-associated colorectal cancer by a novel polypharmacological histone deacetylase inhibitor. Clin. Cancer Res., 2016, 22(16), 4158-4169.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-2379] [PMID: 27528734]
[22]
Mármol, I.; Sánchez-de-Diego, C.; Pradilla Dieste, A.; Cerrada, E.; Rodriguez Yoldi, M.J. Colorectal carcinoma: A general overview and future perspectives in colorectal cancer. Int. J. Mol. Sci., 2017, 18(1), 197.
[http://dx.doi.org/10.3390/ijms18010197] [PMID: 28106826]
[23]
Gao, Z.; Guo, B.; Gao, R.; Zhu, Q.; Qin, H. Microbiota disbiosis is associated with colorectal cancer. Front. Microbiol., 2015, 6, 20.
[http://dx.doi.org/10.3389/fmicb.2015.00020] [PMID: 25699023]
[24]
Lu, Y.; Chen, J.; Zheng, J.; Hu, G.; Wang, J.; Huang, C.; Lou, L.; Wang, X.; Zeng, Y. Mucosal adherent bacterial dysbiosis in patients with colorectal adenomas. Sci. Rep., 2016, 6(1), 26337.
[http://dx.doi.org/10.1038/srep26337] [PMID: 27194068]
[25]
Candela, M.; Turroni, S.; Biagi, E.; Carbonero, F.; Rampelli, S.; Fiorentini, C.; Brigidi, P. Inflammation and colorectal cancer, when micro-biota-host mutualism breaks. World J. Gastroenterol., 2014, 20(4), 908-922.
[http://dx.doi.org/10.3748/wjg.v20.i4.908] [PMID: 24574765]
[26]
Xie, X.; He, Y.; Li, H.; Yu, D.; Na, L.; Sun, T.; Zhang, D.; Shi, X.; Xia, Y.; Jiang, T.; Rong, S.; Yang, S.; Ma, X.; Xu, G. Effects of prebiot-ics on immunologic indicators and intestinal microbiota structure in perioperative colorectal cancer patients. Nutrition, 2019, 61, 132-142.
[http://dx.doi.org/10.1016/j.nut.2018.10.038] [PMID: 30711862]
[27]
Gao, R.; Kong, C.; Li, H.; Huang, L.; Qu, X.; Qin, N.; Qin, H. Dysbiosis signature of mycobiota in colon polyp and colorectal cancer. Eur. J. Clin. Microbiol. Infect. Dis., 2017, 36(12), 2457-2468.
[http://dx.doi.org/10.1007/s10096-017-3085-6] [PMID: 28821976]
[28]
Sobhani, I.; Tap, J.; Roudot-Thoraval, F.; Roperch, J.P.; Letulle, S.; Langella, P.; Corthier, G.; Tran Van Nhieu, J.; Furet, J.P. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One, 2011, 6(1), e16393.
[http://dx.doi.org/10.1371/journal.pone.0016393] [PMID: 21297998]
[29]
Ganesan, K.; Guo, S.; Fayyaz, S.; Zhang, G.; Xu, B. Targeting programmed Fusobacterium nucleatum Fap2 for colorectal cancer therapy. Cancers (Basel), 2019, 11(10), 1592.
[http://dx.doi.org/10.3390/cancers11101592] [PMID: 31635333]
[30]
Swidsinski, A.; Khilkin, M.; Kerjaschki, D.; Schreiber, S.; Ortner, M.; Weber, J.; Lochs, H. Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology, 1998, 115(2), 281-286.
[http://dx.doi.org/10.1016/S0016-5085(98)70194-5] [PMID: 9679033]
[31]
Gold, J.S.; Bayar, S.; Salem, R.R. Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Arch. Surg., 2004, 139(7), 760-765.
[http://dx.doi.org/10.1001/archsurg.139.7.760] [PMID: 15249410]
[32]
Liu, I.L.; Tsai, C-H.; Hsu, C-H.; Hu, J-M.; Chen, Y-C.; Tian, Y-F.; You, S-L.; Chen, C-Y.; Hsiao, C-W.; Lin, C-Y.; Chou, Y.C.; Sun, C.A. Helicobacter pylori infection and the risk of colorectal cancer: a nationwide population-based cohort study. QJM, 2019, 112(10), 787-792.
[http://dx.doi.org/10.1093/qjmed/hcz157] [PMID: 31250012]
[33]
Li, Y-Y.; Ge, Q-X.; Cao, J.; Zhou, Y-J.; Du, Y-L.; Shen, B.; Wan, Y-J.Y.; Nie, Y-Q. Association of Fusobacterium nucleatum infection with colorectal cancer in Chinese patients. World J. Gastroenterol., 2016, 22(11), 3227-3233.
[http://dx.doi.org/10.3748/wjg.v22.i11.3227] [PMID: 27004000]
[34]
Saeed, A.; Eshrat, F.F.; Umar, S.; Saeed, A. The duplex interaction of microbiome with chemoradiation and immunotherapy: potential implications for colorectal cancer. Curr. Colorectal Cancer Rep., 2019, 15(3), 98-104.
[http://dx.doi.org/10.1007/s11888-019-00435-1] [PMID: 31680787]
[35]
Collins, D.; Hogan, A.M.; Winter, D.C. Microbial and viral pathogens in colorectal cancer. Lancet Oncol., 2011, 12(5), 504-512.
[http://dx.doi.org/10.1016/S1470-2045(10)70186-8] [PMID: 21067973]
[36]
Gagnière, J.; Raisch, J.; Veziant, J.; Barnich, N.; Bonnet, R.; Buc, E.; Bringer, M-A.; Pezet, D.; Bonnet, M. Gut microbiota imbalance and colorectal cancer. World J. Gastroenterol., 2016, 22(2), 501-518.
[http://dx.doi.org/10.3748/wjg.v22.i2.501] [PMID: 26811603]
[37]
Purcell, R.V.; Pearson, J.; Aitchison, A.; Dixon, L.; Frizelle, F.A.; Keenan, J.I. Colonization with enterotoxigenic Bacteroides fragilis is associated with early-stage colorectal neoplasia. PLoS One, 2017, 12(2), e0171602.
[http://dx.doi.org/10.1371/journal.pone.0171602] [PMID: 28151975]
[38]
Arthur, J.C.; Jobin, C. The complex interplay between inflammation, the microbiota and colorectal cancer. Gut Microbes, 2013, 4(3), 253-258.
[http://dx.doi.org/10.4161/gmic.24220] [PMID: 23549517]
[39]
Goodwin, A.C.; Destefano Shields, C.E.; Wu, S.; Huso, D.L.; Wu, X.; Murray-Stewart, T.R.; Hacker-Prietz, A.; Rabizadeh, S.; Woster, P.M.; Sears, C.L.; Casero, R.A. Jr Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc. Natl. Acad. Sci. USA, 2011, 108(37), 15354-15359.
[http://dx.doi.org/10.1073/pnas.1010203108] [PMID: 21876161]
[40]
Yang, Z.; Ji, G. Fusobacterium nucleatum-positive colorectal cancer. Oncol. Lett., 2019, 18(2), 975-982.
[PMID: 31423156]
[41]
Kumar, R.; Herold, J.L.; Taylor, J.; Xu, J.; Xu, Y. Variations among Streptococcus gallolyticus subsp. gallolyticus strains in connection with colorectal cancer. Sci. Rep., 2018, 8(1), 1514.
[http://dx.doi.org/10.1038/s41598-018-19941-7] [PMID: 29367658]
[42]
Paritsky, M.; Pastukh, N.; Brodsky, D.; Isakovich, N.; Peretz, A. Association of Streptococcus bovis presence in colonic content with ad-vanced colonic lesion. World J. Gastroenterol., 2015, 21(18), 5663-5667.
[http://dx.doi.org/10.3748/wjg.v21.i18.5663] [PMID: 25987793]
[43]
Tsai, C-E.; Chiu, C-T.; Rayner, C.K.; Wu, K-L.; Chiu, Y-C.; Hu, M-L.; Chuah, S-K.; Tai, W-C.; Liang, C-M.; Wang, H-M. Associated fac-tors in Streptococcus bovis bacteremia and colorectal cancer. Kaohsiung J. Med. Sci., 2016, 32(4), 196-200.
[http://dx.doi.org/10.1016/j.kjms.2016.03.003] [PMID: 27185602]
[44]
Abdulamir, A.S.; Hafidh, R.R.; Abu Bakar, F. The association of Streptococcus bovis/gallolyticus with colorectal tumors: the nature and the underlying mechanisms of its etiological role. J. Exp. Clin. Cancer Res., 2011, 30(1), 11.
[http://dx.doi.org/10.1186/1756-9966-30-11] [PMID: 21247505]
[45]
Abdulamir, A.S.; Hafidh, R.R.; Bakar, F.A. Molecular detection, quantification, and isolation of Streptococcus gallolyticus bacteria colo-nizing colorectal tumors: Inflammation-driven potential of carcinogenesis via IL-1, COX-2, and IL-8. Mol. Cancer, 2010, 9(1), 249.
[http://dx.doi.org/10.1186/1476-4598-9-249] [PMID: 20846456]
[46]
Ellmerich, S.; Djouder, N.; Schöller, M.; Klein, J-P. Production of cytokines by monocytes, epithelial and endothelial cells activated by Streptococcus bovis. Cytokine, 2000, 12(1), 26-31.
[http://dx.doi.org/10.1006/cyto.1999.0521] [PMID: 10623439]
[47]
Lucas, C.; Barnich, N.; Nguyen, H.T.T. Microbiota, inflammation and colorectal cancer. Int. J. Mol. Sci., 2017, 18(6), 1310.
[http://dx.doi.org/10.3390/ijms18061310] [PMID: 28632155]
[48]
Abdulamir, A.S.; Hafidh, R.R.; Mahdi, L.K.; Al-jeboori, T.; Abubaker, F. Investigation into the controversial association of Streptococcus gallolyticus with colorectal cancer and adenoma. BMC Cancer, 2009, 9(1), 403.
[http://dx.doi.org/10.1186/1471-2407-9-403] [PMID: 19925668]
[49]
Darjee, R.; Gibb, A.P. Serological investigation into the association between Streptococcus bovis and colonic cancer. J. Clin. Pathol., 1993, 46(12), 1116-1119.
[http://dx.doi.org/10.1136/jcp.46.12.1116] [PMID: 8282836]
[50]
Feng, Y.Y.; Zeng, D.Z.; Tong, Y.N.; Lu, X.X.; Dun, G.D.; Tang, B.; Zhang, Z.J.; Ye, X.L.; Li, Q.; Xie, J.P.; Mao, X.H. Alteration of mi-croRNA-4474/4717 expression and CREB-binding protein in human colorectal cancer tissues infected with Fusobacterium nucleatum. PLoS One, 2019, 14(4), e0215088.
[http://dx.doi.org/10.1371/journal.pone.0215088] [PMID: 30951563]
[51]
Lee, S.A.; Liu, F.; Riordan, S.M.; Lee, C.S.; Zhang, L. Global investigations of Fusobacterium nucleatum in human colorectal cancer. Front. Oncol., 2019, 9, 566.
[http://dx.doi.org/10.3389/fonc.2019.00566] [PMID: 31334107]
[52]
Shariati, A.; Razavi, S.; Ghaznavi-Rad, E.; Jahanbin, B.; Akbari, A.; Norzaee, S.; Darban-Sarokhalil, D. Association between colorectal cancer and Fusobacterium nucleatum and Bacteroides fragilis bacteria in Iranian patients: A preliminary study. Infect. Agent. Cancer, 2021, 16(1), 41.
[http://dx.doi.org/10.1186/s13027-021-00381-4] [PMID: 34108031]
[53]
Cuellar-Gómez, H.; Ocharán-Hernández, M.; Calzada-Mendoza, C.; Comoto-Santacruz, D. Association of Fusobacterium nucleatum infec-tion and colorectal cancer: A mexican study. Rev. Gastroenterol. Mex., 2021, RGMXEN-720.
[54]
Yamaoka, Y.; Suehiro, Y.; Hashimoto, S.; Hoshida, T.; Fujimoto, M.; Watanabe, M.; Imanaga, D.; Sakai, K.; Matsumoto, T.; Nishioka, M.; Takami, T.; Suzuki, N.; Hazama, S.; Nagano, H.; Sakaida, I.; Yamasaki, T. Fusobacterium nucleatum as a prognostic marker of colorectal cancer in a Japanese population. J. Gastroenterol., 2018, 53(4), 517-524.
[http://dx.doi.org/10.1007/s00535-017-1382-6] [PMID: 28823057]
[55]
Kumar, R.; Herold, J.L.; Schady, D.; Davis, J.; Kopetz, S.; Martinez-Moczygemba, M.; Murray, B.E.; Han, F.; Li, Y.; Callaway, E.; Chap-kin, R.S.; Dashwood, W.M.; Dashwood, R.H.; Berry, T.; Mackenzie, C.; Xu, Y. Streptococcus gallolyticus subsp. gallolyticus promotes colorectal tumor development. PLoS Pathog., 2017, 13(7), e1006440.
[http://dx.doi.org/10.1371/journal.ppat.1006440] [PMID: 28704539]
[56]
Castellarin, M.; Warren, R.L.; Freeman, J.D.; Dreolini, L.; Krzywinski, M.; Strauss, J.; Barnes, R.; Watson, P.; Allen-Vercoe, E.; Moore, R.A.; Holt, R.A. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res., 2012, 22(2), 299-306.
[http://dx.doi.org/10.1101/gr.126516.111] [PMID: 22009989]
[57]
Wu, N.; Yang, X.; Zhang, R.; Li, J.; Xiao, X.; Hu, Y.; Chen, Y.; Yang, F.; Lu, N.; Wang, Z.; Luan, C.; Liu, Y.; Wang, B.; Xiang, C.; Wang, Y.; Zhao, F.; Gao, G.F.; Wang, S.; Li, L.; Zhang, H.; Zhu, B. Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb. Ecol., 2013, 66(2), 462-470.
[http://dx.doi.org/10.1007/s00248-013-0245-9] [PMID: 23733170]
[58]
Mira-Pascual, L.; Cabrera-Rubio, R.; Ocon, S.; Costales, P.; Parra, A.; Suarez, A.; Moris, F.; Rodrigo, L.; Mira, A.; Collado, M.C. Microbial mucosal colonic shifts associated with the development of colorectal cancer reveal the presence of different bacterial and archaeal bi-omarkers. J. Gastroenterol., 2015, 50(2), 167-179.
[http://dx.doi.org/10.1007/s00535-014-0963-x] [PMID: 24811328]
[59]
Burns, M.B.; Lynch, J.; Starr, T.K.; Knights, D.; Blekhman, R. Virulence genes are a signature of the microbiome in the colorectal tumor microenvironment. Genome Med., 2015, 7(1), 55.
[http://dx.doi.org/10.1186/s13073-015-0177-8] [PMID: 26170900]
[60]
Legakis, N.; Ioannides, H.; Tzannetis, S.; Golematis, B.; Papavassiliou, J. Faecal bacterial flora in patients with colon cancer and control subjects. Zentralblatt für Bakteriologie, Mikrobiologie und Hygiene 1 Abt Originale A, Medizinische Mikrobiologie. Infektionskrankheiten und Parasitologie, 1981, 251(1), 54-61.
[61]
Wang, T.; Cai, G.; Qiu, Y.; Fei, N.; Zhang, M.; Pang, X.; Jia, W.; Cai, S.; Zhao, L. Structural segregation of gut microbiota between colorec-tal cancer patients and healthy volunteers. ISME J., 2012, 6(2), 320-329.
[http://dx.doi.org/10.1038/ismej.2011.109] [PMID: 21850056]
[62]
Zeller, G.; Tap, J.; Voigt, A.Y.; Sunagawa, S.; Kultima, J.R.; Costea, P.I.; Amiot, A.; Böhm, J.; Brunetti, F.; Habermann, N.; Hercog, R.; Koch, M.; Luciani, A.; Mende, D.R.; Schneider, M.A.; Schrotz-King, P.; Tournigand, C.; Tran Van Nhieu, J.; Yamada, T.; Zimmermann, J.; Benes, V.; Kloor, M.; Ulrich, C.M.; von Knebel Doeberitz, M.; Sobhani, I.; Bork, P. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol. Syst. Biol., 2014, 10(11), 766.
[http://dx.doi.org/10.15252/msb.20145645] [PMID: 25432777]
[63]
Nakatsu, G.; Li, X.; Zhou, H.; Sheng, J.; Wong, S.H.; Wu, W.K.K.; Ng, S.C.; Tsoi, H.; Dong, Y.; Zhang, N.; He, Y.; Kang, Q.; Cao, L.; Wang, K.; Zhang, J.; Liang, Q.; Yu, J.; Sung, J.J. Gut mucosal microbiome across stages of colorectal carcinogenesis. Nat. Commun., 2015, 6(1), 8727.
[http://dx.doi.org/10.1038/ncomms9727] [PMID: 26515465]
[64]
Zhou, Y.; He, H.; Xu, H.; Li, Y.; Li, Z.; Du, Y.; He, J.; Zhou, Y.; Wang, H.; Nie, Y. Association of oncogenic bacteria with colorectal can-cer in South China. Oncotarget, 2016, 7(49), 80794-80802.
[http://dx.doi.org/10.18632/oncotarget.13094] [PMID: 27821805]
[65]
Dai, Z.; Coker, O.O.; Nakatsu, G.; Wu, W.K.K.; Zhao, L.; Chen, Z.; Chan, F.K.L.; Kristiansen, K.; Sung, J.J.Y.; Wong, S.H.; Yu, J. Multi-cohort analysis of colorectal cancer metagenome identified altered bacteria across populations and universal bacterial markers. Microbiome, 2018, 6(1), 70.
[http://dx.doi.org/10.1186/s40168-018-0451-2] [PMID: 29642940]
[66]
Iyadorai, T.; Mariappan, V.; Vellasamy, K.M.; Wanyiri, J.W.; Roslani, A.C.; Lee, G.K.; Sears, C.; Vadivelu, J. Prevalence and association of pks+ Escherichia coli with colorectal cancer in patients at the University Malaya Medical Centre, Malaysia. PLoS One, 2020, 15(1), e0228217.
[http://dx.doi.org/10.1371/journal.pone.0228217] [PMID: 31990962]
[67]
Rubinstein, M.R.; Wang, X.; Liu, W.; Hao, Y.; Cai, G.; Han, Y.W. Fusobacterium nucleatum promotes colorectal carcinogenesis by modu-lating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe, 2013, 14(2), 195-206.
[http://dx.doi.org/10.1016/j.chom.2013.07.012] [PMID: 23954158]
[68]
Zhang, S.; Cai, S.; Ma, Y. Association between Fusobacterium nucleatum and colorectal cancer: Progress and future directions. J. Cancer, 2018, 9(9), 1652-1659.
[http://dx.doi.org/10.7150/jca.24048] [PMID: 29760804]
[69]
Shang, F-M.; Liu, H-L. Fusobacterium nucleatum and colorectal cancer: A review. World J. Gastrointest. Oncol., 2018, 10(3), 71-81.
[http://dx.doi.org/10.4251/wjgo.v10.i3.71] [PMID: 29564037]
[70]
Luo, K.; Zhang, Y.; Xv, C.; Ji, J.; Lou, G.; Guo, X.; Chen, M.; Zhang, Y.; Wei, H.; Guo, M.; Huang, R.; Yu, S. Fusobacterium nucleatum, the communication with colorectal cancer. Biomed. Pharmacother., 2019, 116, 108988.
[http://dx.doi.org/10.1016/j.biopha.2019.108988] [PMID: 31112873]
[71]
Yang, Y.; Weng, W.; Peng, J.; Hong, L.; Yang, L.; Toiyama, Y.; Gao, R.; Liu, M.; Yin, M.; Pan, C. Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating Toll-like receptor 4 signaling to nuclear Factor− κB, and up-regulating expression of microRNA-21. Gastroenterology, 2017, 152(4), 851-866. e824.
[72]
Li, C.; Zhao, L.; Chen, Y.; He, T.; Chen, X.; Mao, J.; Li, C.; Lyu, J.; Meng, Q.H. MicroRNA-21 promotes proliferation, migration, and invasion of colorectal cancer, and tumor growth associated with down-regulation of sec23a expression. BMC Cancer, 2016, 16(1), 605.
[http://dx.doi.org/10.1186/s12885-016-2628-z] [PMID: 27495250]
[73]
Gur, C.; Ibrahim, Y.; Isaacson, B.; Yamin, R.; Abed, J.; Gamliel, M.; Enk, J.; Bar-On, Y.; Stanietsky-Kaynan, N.; Coppenhagen-Glazer, S.; Shussman, N.; Almogy, G.; Cuapio, A.; Hofer, E.; Mevorach, D.; Tabib, A.; Ortenberg, R.; Markel, G.; Miklić, K.; Jonjic, S.; Brennan, C.A.; Garrett, W.S.; Bachrach, G.; Mandelboim, O. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity, 2015, 42(2), 344-355.
[http://dx.doi.org/10.1016/j.immuni.2015.01.010] [PMID: 25680274]
[74]
Wang, H-F.; Li, L-F.; Guo, S-H.; Zeng, Q-Y.; Ning, F.; Liu, W-L.; Zhang, G. Evaluation of antibody level against Fusobacterium nucleatum in the serological diagnosis of colorectal cancer. Sci. Rep., 2016, 6(1), 33440.
[http://dx.doi.org/10.1038/srep33440] [PMID: 27678333]
[75]
Yu, T.; Guo, F.; Yu, Y.; Sun, T.; Ma, D.; Han, J.; Qian, Y.; Kryczek, I.; Sun, D.; Nagarsheth, N. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell., 2017, 170, (3)548-563. e516.
[http://dx.doi.org/10.1016/j.cell.2017.07.008]
[76]
Sittipo, P.; Lobionda, S.; Choi, K.; Sari, I.N.; Kwon, H.Y.; Lee, Y.K. Toll-like receptor 2-mediated suppression of colorectal cancer patho-genesis by polysaccharide A from Bacteroides fragilis. Front. Microbiol., 2018, 9, 1588.
[http://dx.doi.org/10.3389/fmicb.2018.01588] [PMID: 30065713]
[77]
Butt, J.; Jenab, M.; Werner, J.; Fedirko, V.; Weiderpass, E.; Dahm, C.C.; Tjønneland, A.; Olsen, A.; Boutron-Ruault, M-C.; Rothwell, J.A.; Severi, G.; Kaaks, R.; Turzanski-Fortner, R.; Aleksandrova, K.; Schulze, M.; Palli, D.; Pala, V.; Panico, S.; Tumino, R.; Sacerdote, C. Bue-no-de-Mesquita, B.; Van Gils, C.H.; Gram, I.T.; Lukic, M.; Sala, N.; Sánchez Pérez, M.J.; Ardanaz, E.; Chirlaque, M.D.; Palmquist, R.; Löwenmark, T.; Travis, R.C.; Heath, A.; Cross, A.J.; Freisling, H.; Zouiouich, S.; Aglago, E.; Waterboer, T.; Hughes, D.J. Association of Pre-diagnostic Antibody Responses to Escherichia coli and Bacteroides fragilis Toxin Proteins with Colorectal Cancer in a European Co-hort. Gut Microbes, 2021, 13(1), 1-14.
[http://dx.doi.org/10.1080/19490976.2021.1903825] [PMID: 33874856]
[78]
Xie, X.; Jiang, D.; Zhou, X.; Ye, X.; Yang, P.; He, Y. Recombinant Bacteroides fragilis enterotoxin-1 (rBFT-1) promotes proliferation of colorectal cancer via CCL3-related molecular pathways. Open Life Sci., 2021, 16(1), 408-418.
[http://dx.doi.org/10.1515/biol-2021-0043] [PMID: 33981848]
[79]
Zhang, J.; Lu, X.; Zhao, G.; Shi, H.; Geng, Y.; Zhong, W.; Dong, L. Relationships between the enrichment of ETBF, Fn, Hp in intestinal and colorectal cancer. Chin. J. Oncol., 2018, 40(2), 99-104.
[80]
Boleij, A.; Hechenbleikner, E.M.; Goodwin, A.C.; Badani, R.; Stein, E.M.; Lazarev, M.G.; Ellis, B.; Carroll, K.C.; Albesiano, E.; Wick, E.C.; Platz, E.A.; Pardoll, D.M.; Sears, C.L. The Bacteroides fragilis toxin gene is prevalent in the colon mucosa of colorectal cancer pa-tients. Clin. Infect. Dis., 2015, 60(2), 208-215.
[http://dx.doi.org/10.1093/cid/ciu787] [PMID: 25305284]
[81]
Purcell, R.V.; Pearson, J.; Frizelle, F.A.; Keenan, J.I. Comparison of standard, quantitative and digital PCR in the detection of enterotoxi-genic Bacteroides fragilis. Sci. Rep., 2016, 6(1), 34554.
[http://dx.doi.org/10.1038/srep34554] [PMID: 27686415]
[82]
Toprak, N.U.; Yagci, A.; Gulluoglu, B.M.; Akin, M.L.; Demirkalem, P.; Celenk, T.; Soyletir, G. A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin. Microbiol. Infect., 2006, 12(8), 782-786.
[http://dx.doi.org/10.1111/j.1469-0691.2006.01494.x] [PMID: 16842574]
[83]
Viljoen, K.S.; Dakshinamurthy, A.; Goldberg, P.; Blackburn, J.M. Quantitative profiling of colorectal cancer-associated bacteria reveals associations between fusobacterium spp., enterotoxigenic Bacteroides fragilis (ETBF) and clinicopathological features of colorectal cancer. PLoS One, 2015, 10(3), e0119462.
[http://dx.doi.org/10.1371/journal.pone.0119462] [PMID: 25751261]
[84]
Wu, S.; Morin, P.J.; Maouyo, D.; Sears, C.L. Bacteroides fragilis enterotoxin induces c-Myc expression and cellular proliferation. Gastroenterology, 2003, 124(2), 392-400.
[http://dx.doi.org/10.1053/gast.2003.50047] [PMID: 12557145]
[85]
Wu, S.; Rhee, K-J.; Albesiano, E.; Rabizadeh, S.; Wu, X.; Yen, H-R.; Huso, D.L.; Brancati, F.L.; Wick, E.; McAllister, F.; Housseau, F.; Pardoll, D.M.; Sears, C.L. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat. Med., 2009, 15(9), 1016-1022.
[http://dx.doi.org/10.1038/nm.2015] [PMID: 19701202]
[86]
Wick, E.C.; Rabizadeh, S.; Albesiano, E.; Wu, X.; Wu, S.; Chan, J.; Rhee, K-J.; Ortega, G.; Huso, D.L.; Pardoll, D.; Housseau, F.; Sears, C.L. Stat3 activation in murine colitis induced by enterotoxigenic Bacteroides fragilis. Inflamm. Bowel Dis., 2014, 20(5), 821-834.
[http://dx.doi.org/10.1097/MIB.0000000000000019] [PMID: 24704822]
[87]
Babbar, N.; Casero, R.A., Jr Tumor necrosis factor-α increases reactive oxygen species by inducing spermine oxidase in human lung epi-thelial cells: A potential mechanism for inflammation-induced carcinogenesis. Cancer Res., 2006, 66(23), 11125-11130.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-3174] [PMID: 17145855]
[88]
Battaglia, V.; DeStefano Shields, C.; Murray-Stewart, T.; Casero, R.A., Jr Polyamine catabolism in carcinogenesis: Potential targets for chemotherapy and chemoprevention. Amino Acids, 2014, 46(3), 511-519.
[http://dx.doi.org/10.1007/s00726-013-1529-6] [PMID: 23771789]
[89]
Keenan, J.I.; Frizelle, F.A. Bacteria flying under the radar: Linking a bacterial infection to colon carcinogenesis. Infect. Agent. Cancer, 2014, 9(1), 31.
[http://dx.doi.org/10.1186/1750-9378-9-31] [PMID: 25225573]
[90]
Wassenaar, T.M.E.E. coli and colorectal cancer: A complex relationship that deserves a critical mindset. Crit. Rev. Microbiol., 2018, 44(5), 619-632.
[http://dx.doi.org/10.1080/1040841X.2018.1481013] [PMID: 29909724]
[91]
Amarsy, R.; Guéret, D.; Benmansour, H.; Flicoteaux, R.; Berçot, B.; Meunier, F.; Mougari, F.; Jacquier, H.; Pean de Ponfilly, G.; Clermont, O.; Denamur, E.; Teixeira, A.; Cambau, E. Determination of Escherichia coli phylogroups in elderly patients with urinary tract infection or asymptomatic bacteriuria. Clin. Microbiol. Infect., 2019, 25(7), 839-844.
[http://dx.doi.org/10.1016/j.cmi.2018.12.032] [PMID: 30648603]
[92]
Buc, E.; Dubois, D.; Sauvanet, P.; Raisch, J.; Delmas, J.; Darfeuille-Michaud, A.; Pezet, D.; Bonnet, R. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One, 2013, 8(2), e56964.
[http://dx.doi.org/10.1371/journal.pone.0056964] [PMID: 23457644]
[93]
Raisch, J.; Buc, E.; Bonnet, M.; Sauvanet, P.; Vazeille, E.; de Vallée, A.; Déchelotte, P.; Darcha, C.; Pezet, D.; Bonnet, R.; Bringer, M.A.; Darfeuille-Michaud, A. Colon cancer-associated B2 Escherichia coli colonize gut mucosa and promote cell proliferation. World J. Gastroenterol., 2014, 20(21), 6560-6572.
[http://dx.doi.org/10.3748/wjg.v20.i21.6560] [PMID: 24914378]
[94]
Martin, H.M.; Campbell, B.J.; Hart, C.A.; Mpofu, C.; Nayar, M.; Singh, R.; Englyst, H.; Williams, H.F.; Rhodes, J.M. Enhanced Escherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterology, 2004, 127(1), 80-93.
[http://dx.doi.org/10.1053/j.gastro.2004.03.054] [PMID: 15236175]
[95]
Prorok-Hamon, M.; Friswell, M.K.; Alswied, A.; Roberts, C.L.; Song, F.; Flanagan, P.K.; Knight, P.; Codling, C.; Marchesi, J.R.; Winstan-ley, C.; Hall, N.; Rhodes, J.M.; Campbell, B.J. Colonic mucosa-associated diffusely adherent afaC+ Escherichia coli expressing lpfA and pks are increased in inflammatory bowel disease and colon cancer. Gut, 2014, 63(5), 761-770.
[http://dx.doi.org/10.1136/gutjnl-2013-304739] [PMID: 23846483]
[96]
Faïs, T.; Delmas, J.; Barnich, N.; Bonnet, R.; Dalmasso, G. Colibactin: More than a new bacterial toxin. Toxins (Basel), 2018, 10(4), 151.
[http://dx.doi.org/10.3390/toxins10040151] [PMID: 29642622]
[97]
Borges-Canha, M.; Portela-Cidade, J.P.; Dinis-Ribeiro, M.; Leite-Moreira, A.F.; Pimentel-Nunes, P. Role of colonic microbiota in colorectal carcinogenesis: A systematic review. Rev. Esp. Enferm. Dig., 2015, 107(11), 659-671.
[http://dx.doi.org/10.17235/reed.2015.3830/2015] [PMID: 26541655]
[98]
Payros, D.; Secher, T.; Boury, M.; Brehin, C.; Ménard, S.; Salvador-Cartier, C.; Cuevas-Ramos, G.; Watrin, C.; Marcq, I.; Nougayrède, J-P.; Dubois, D.; Bedu, A.; Garnier, F.; Clermont, O.; Denamur, E.; Plaisancié, P.; Theodorou, V.; Fioramonti, J.; Olier, M.; Oswald, E. Ma-ternally acquired genotoxic Escherichia coli alters offspring’s intestinal homeostasis. Gut Microbes, 2014, 5(3), 313-325.
[http://dx.doi.org/10.4161/gmic.28932] [PMID: 24971581]
[99]
Park, C.H.; Eun, C.S.; Han, D.S. Intestinal microbiota, chronic inflammation, and colorectal cancer. Intest. Res., 2018, 16(3), 338-345.
[http://dx.doi.org/10.5217/ir.2018.16.3.338] [PMID: 30090032]
[100]
Arthur, J.C.; Perez-Chanona, E.; Mühlbauer, M.; Tomkovich, S.; Uronis, J.M.; Fan, T-J.; Campbell, B.J.; Abujamel, T.; Dogan, B.; Rogers, A.B.; Rhodes, J.M.; Stintzi, A.; Simpson, K.W.; Hansen, J.J.; Keku, T.O.; Fodor, A.A.; Jobin, C. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science, 2012, 338(6103), 120-123.
[http://dx.doi.org/10.1126/science.1224820] [PMID: 22903521]
[101]
Johnson, J.R.; Johnston, B.; Kuskowski, M.A.; Nougayrede, J-P.; Oswald, E. Molecular epidemiology and phylogenetic distribution of the Escherichia coli pks genomic island. J. Clin. Microbiol., 2008, 46(12), 3906-3911.
[http://dx.doi.org/10.1128/JCM.00949-08] [PMID: 18945841]
[102]
Shimpoh, T.; Hirata, Y.; Ihara, S.; Suzuki, N.; Kinoshita, H.; Hayakawa, Y.; Ota, Y.; Narita, A.; Yoshida, S.; Yamada, A.; Koike, K.; Ihara, S.; Suzuki, N.; Kinoshita, H.; Hayakawa, Y.; Ota, Y.; Narita, A.; Yoshida, S.; Yamada, A. Prevalence of pks-positive Escherichia coli in Japanese patients with or without colorectal cancer. Gut Pathog., 2017, 9(1), 1-8.
[http://dx.doi.org/10.1186/s13099-017-0185-x]
[103]
Secher, T.; Samba-Louaka, A.; Oswald, E.; Nougayrède, J-P. Escherichia coli producing colibactin triggers premature and transmissible senescence in mammalian cells. PLoS One, 2013, 8(10), e77157.
[http://dx.doi.org/10.1371/journal.pone.0077157] [PMID: 24116215]
[104]
Cougnoux, A.; Dalmasso, G.; Martinez, R.; Buc, E.; Delmas, J.; Gibold, L.; Sauvanet, P.; Darcha, C.; Déchelotte, P.; Bonnet, M.; Pezet, D.; Wodrich, H.; Darfeuille-Michaud, A.; Bonnet, R. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut, 2014, 63(12), 1932-1942.
[http://dx.doi.org/10.1136/gutjnl-2013-305257] [PMID: 24658599]
[105]
Iftekhar, A.; Berger, H.; Bouznad, N.; Heuberger, J.; Boccellato, F.; Dobrindt, U.; Hermeking, H.; Sigal, M.; Meyer, T.F. Genomic aberra-tions after short-term exposure to colibactin-producing E. coli transform primary colon epithelial cells. Nat. Commun., 2021, 12(1), 1003.
[http://dx.doi.org/10.1038/s41467-021-21162-y] [PMID: 33579932]
[106]
Salesse, L.; Lucas, C.; Hoang, M.H.T.; Sauvanet, P.; Rezard, A.; Rosenstiel, P.; Damon-Soubeyrand, C.; Barnich, N.; Godfraind, C.; Dal-masso, G.; Nguyen, H.T.T. Colibactin-Producing Escherichia coli Induce the Formation of Invasive Carcinomas in a Chronic Inflamma-tion-Associated Mouse Model. Cancers (Basel), 2021, 13(9), 2060.
[http://dx.doi.org/10.3390/cancers13092060] [PMID: 33923277]
[107]
Gao, R.; Gao, Z.; Huang, L.; Qin, H. Gut microbiota and colorectal cancer. Eur. J. Clin. Microbiol. Infect. Dis., 2017, 36(5), 757-769.
[http://dx.doi.org/10.1007/s10096-016-2881-8] [PMID: 28063002]
[108]
Perillo, F.; Amoroso, C.; Strati, F.; Giuffrè, M.R.; Díaz-Basabe, A.; Lattanzi, G.; Facciotti, F. Gut microbiota manipulation as a tool for colorectal cancer management: Recent advances in its use for therapeutic purposes. Int. J. Mol. Sci., 2020, 21(15), 5389.
[http://dx.doi.org/10.3390/ijms21155389] [PMID: 32751239]
[109]
Huang, K.; Wu, L.; Yang, Y. Gut microbiota: An emerging biological diagnostic and treatment approach for gastrointestinal diseases. JGH Open, 2021, 5(9), 973-975.
[http://dx.doi.org/10.1002/jgh3.12659] [PMID: 34584963]
[110]
Kaźmierczak-Siedlecka, K.; Daca, A.; Fic, M.; van de Wetering, T.; Folwarski, M.; Makarewicz, W. Therapeutic methods of gut microbiota modification in colorectal cancer management - fecal microbiota transplantation, prebiotics, probiotics, and synbiotics. Gut Microbes, 2020, 11(6), 1518-1530.
[http://dx.doi.org/10.1080/19490976.2020.1764309] [PMID: 32453670]
[111]
Raman, M.; Ambalam, P.; Kondepudi, K.K.; Pithva, S.; Kothari, C.; Patel, A.T.; Purama, R.K.; Dave, J.M.; Vyas, B.R. Potential of probiot-ics, prebiotics and synbiotics for management of colorectal cancer. Gut Microbes, 2013, 4(3), 181-192.
[http://dx.doi.org/10.4161/gmic.23919] [PMID: 23511582]
[112]
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.
[http://dx.doi.org/10.1002/ijc.32003] [PMID: 30458058]
[113]
Keku, T.O.; Dulal, S.; Deveaux, A.; Jovov, B.; Han, X. The gastrointestinal microbiota and colorectal cancer. Am. J. Physiol. Gastrointest. Liver Physiol., 2015, 308(5), G351-G363.
[http://dx.doi.org/10.1152/ajpgi.00360.2012] [PMID: 25540232]
[114]
Yang, J.; Yu, J. The association of diet, gut microbiota and colorectal cancer: What we eat may imply what we get. Protein Cell, 2018, 9(5), 474-487.
[http://dx.doi.org/10.1007/s13238-018-0543-6] [PMID: 29713943]
[115]
Tripathy, A.; Dash, J.; Kancharla, S.; Kolli, P.; Mahajan, D.; Senapati, S.; Jena, M.K. Probiotics: A promising candidate for management of colorectal cancer. Cancers (Basel), 2021, 13(13), 3178.
[http://dx.doi.org/10.3390/cancers13133178] [PMID: 34202265]
[116]
Torres-Maravilla, E.; Boucard, A-S.; Mohseni, A.H.; Taghinezhad-S, S.; Cortes-Perez, N.G.; Bermúdez-Humarán, L.G. Role of gut micro-biota and probiotics in colorectal cancer: Onset and progression. Microorganisms, 2021, 9(5), 1021.
[http://dx.doi.org/10.3390/microorganisms9051021] [PMID: 34068653]
[117]
Ljungh, A.; Wadström, T. Lactic acid bacteria as probiotics. Curr. Issues Intest. Microbiol., 2006, 7(2), 73-89.
[PMID: 16875422]
[118]
Zhong, L.; Zhang, X.; Covasa, M. Emerging roles of lactic acid bacteria in protection against colorectal cancer. World J. Gastroenterol., 2014, 20(24), 7878-7886.
[http://dx.doi.org/10.3748/wjg.v20.i24.7878] [PMID: 24976724]
[119]
Saeed, M.; Shoaib, A.; Kandimalla, R.; Javed, S.; Almatroudi, A.; Gupta, R.; Aqil, F. Microbe-based therapies for colorectal cancer: Ad-vantages and limitations. Semin. Cancer Biol., 2021.

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