Research article

Gut mucosal microbiota profiles linked to development of positional-specific human colorectal cancer

  • Received: 19 March 2024 Revised: 03 September 2024 Accepted: 09 September 2024 Published: 24 September 2024
  • Colorectal cancer (CRC) continuously ranks as the third most common cause of cancer-related deaths worldwide. Based on anatomical classifications and clinical diagnoses, CRC is classified into right-sided, left-sided, and rectal CRC. Importantly, the three types of positional-specific CRC affect the prognosis outcomes, thus indicating that positional-specific treatments for CRC are required. Emerging evidence suggests that besides host genetic and epigenetic alterations, gut mucosal microbiota is linked to gut inflammation, CRC occurrence, and prognoses. However, gut mucosal microbiota associated with positional-specific CRC are poorly investigated. Here, we report the gut mucosal microbiota profiles associated with these three types of CRC. Our analysis showed that the unique composition and biodiversity of bacterial taxa are linked to positional-specific CRC. We found that a combination of bacterial taxa can serve as potential biomarkers to distinguish the three types of CRC. Further investigations of the physiological roles of bacteria associated with positional-specific CRC may help understand the mechanism of CRC progression in different anatomical locations under the impact of gut mucosal microbiota.

    Citation: Chunze Zhang, Mingqian Ma, Zhenying Zhao, Zhiqiang Feng, Tianhao Chu, Yijia Wang, Jun Liu, Xuehua Wan. Gut mucosal microbiota profiles linked to development of positional-specific human colorectal cancer[J]. AIMS Microbiology, 2024, 10(4): 812-832. doi: 10.3934/microbiol.2024035

    Related Papers:

  • Colorectal cancer (CRC) continuously ranks as the third most common cause of cancer-related deaths worldwide. Based on anatomical classifications and clinical diagnoses, CRC is classified into right-sided, left-sided, and rectal CRC. Importantly, the three types of positional-specific CRC affect the prognosis outcomes, thus indicating that positional-specific treatments for CRC are required. Emerging evidence suggests that besides host genetic and epigenetic alterations, gut mucosal microbiota is linked to gut inflammation, CRC occurrence, and prognoses. However, gut mucosal microbiota associated with positional-specific CRC are poorly investigated. Here, we report the gut mucosal microbiota profiles associated with these three types of CRC. Our analysis showed that the unique composition and biodiversity of bacterial taxa are linked to positional-specific CRC. We found that a combination of bacterial taxa can serve as potential biomarkers to distinguish the three types of CRC. Further investigations of the physiological roles of bacteria associated with positional-specific CRC may help understand the mechanism of CRC progression in different anatomical locations under the impact of gut mucosal microbiota.



    加载中


    Conflict of interest



    The authors declare no conflict of interest.

    Author contributions



    Conceptualization, J.L. and X.W.; investigation, C.Z., M.M., Z.F., T.C. and Y.W.; writing—original draft preparation, C.Z.; writing—review and editing, J.L. and X.W.; funding acquisition, J.L. and X.W.

    Funding



    This work was funded by the Natural Science Foundation of China, grant number 12174203, and Natural Science Foundation of Tianjin, grant number 21JCYBJC00120.

    [1] Sung H, Ferlay J, Siegel RL, et al. (2021) Global cancer statistics 2020: Globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71: 209-249. https://doi.org/10.3322/caac.21660
    [2] Schwabe RF, Jobin C (2013) The microbiome and cancer. Nat Rev Cancer 13: 800-812. https://doi.org/10.1038/nrc3610
    [3] Irrazábal T, Belcheva A, Girardin SE, et al. (2014) The multifaceted role of the intestinal microbiota in colon cancer. Mol Cell 54: 309-320. https://doi.org/10.1016/j.molcel.2014.03.039
    [4] Sillo TO, Beggs AD, Middleton G, et al. (2023) The gut microbiome, microsatellite status and the response to immunotherapy in colorectal cancer. Int J Mol Sci 24: 5767. https://doi.org/10.3390/ijms24065767
    [5] Ng C, Li H, Wu WKK, et al. (2019) Genomics and metagenomics of colorectal cancer. J Gastrointest Oncol 10: 1164-1170. https://doi.org/10.21037/jgo.2019.06.04
    [6] Rajilić-Stojanović M, de Vos WM (2014) The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev 38: 996-1047. https://doi.org/10.1111/1574-6976.12075
    [7] Nakatsu G, Li X, Zhou H, et al. (2015) Gut mucosal microbiome across stages of colorectal carcinogenesis. Nat Commun 6: 8727. https://doi.org/10.1038/ncomms9727
    [8] Zhang S, Cai S, Ma Y (2018) Association between Fusobacterium nucleatum and colorectal cancer: Progress and future directions. J Cancer 9: 1652-1659. https://doi.org/10.7150/jca.24048
    [9] Long X, Wong CC, Tong L, et al. (2019) Peptostreptococcus anaerobius promotes colorectal carcinogenesis and modulates tumour immunity. Nat Microbiol 4: 2319-2330. https://doi.org/10.1038/s41564-019-0541-3
    [10] Rhee KJ, Wu S, Wu X, et al. (2009) Induction of persistent colitis by a human commensal, enterotoxigenic Bacteroides fragilis, in wild-type C57BL/6 mice. Infect Immun 77: 1708-1718. https://doi.org/10.1128/IAI.00814-08
    [11] Wang Y, Wan X, Wu X, et al. (2021) Eubacterium rectale contributes to colorectal cancer initiation via promoting colitis. Gut Pathog 13: 2. https://doi.org/10.1186/s13099-020-00396-z
    [12] Elmentaite R, Kumasaka N, Roberts K, et al. (2021) Cells of the human intestinal tract mapped across space and time. Nature 597: 250-255. https://doi.org/10.1038/s41586-021-03852-1
    [13] Hickey JW, Becker WR, Nevins SA, et al. (2023) Organization of the human intestine at single-cell resolution. Nature 619: 572-584. https://doi.org/10.1038/s41586-023-05915-x
    [14] Liu LU, Holt PR, Krivosheyev V, et al. (1999) Human right and left colon differ in epithelial cell apoptosis and in expression of Bak, a pro-apoptotic Bcl-2 homologue. Gut 45: 45-50. https://doi.org/10.1136/gut.45.1.45
    [15] Guo W, Zhang C, Wang X, et al. (2022) Resolving the difference between left-sided and right-sided colorectal cancer by single-cell sequencing. JCI Insight 7: e152616. https://doi.org/10.1172/jci.insight.152616
    [16] Venook AP, Niedzwiecki D, Lenz HJ, et al. (2014) CALGB/SWOG 80405: Phase III trial of irinotecan/5-FU/leucovorin (FOLFIRI) or oxaliplatin/5-FU/leucovorin (mFOLFOX6) with bevacizumab (BV) or cetuximab (CET) for patients (pts) with KRAS wild-type (wt) untreated metastatic adenocarcinoma of the colon or rectum (MCRC). J Clin Oncol 32. https://doi.org/10.1200/jco.2014.32.15_suppl.lba3
    [17] Hong TS, Clark JW, Haigis KM (2012) Cancers of the colon and rectum: Identical or fraternal twins?. Cancer Discovery 2: 117-121. https://doi.org/10.1158/2159-8290.CD-11-0315
    [18] Bufill JA (1990) Colorectal cancer: Evidence for distinct genetic categories based on proximal or distal tumor location. Ann Intern Med 113: 779-788. https://doi.org/10.7326/0003-4819-113-10-779
    [19] Distler P, Holt PR (1997) Are right- and left-sided colon neoplasms distinct tumors?. Dig Dis 15: 302-311. https://doi.org/10.1159/000171605
    [20] Hutchins G, Southward K, Handley K, et al. (2011) Value of mismatch repair, KRAS, and BRAF mutations in predicting recurrence and benefits from chemotherapy in colorectal cancer. J Clin Oncol 29: 1261-1270. https://doi.org/10.1200/JCO.2010.30.1366
    [21] Miyake T, Mori H, Yasukawa D, et al. (2021) The comparison of fecal microbiota in left-side and right-side human colorectal cancer. Eur Surg Res 62: 248-254. https://doi.org/10.1159/000516922
    [22] Phipps O, Quraishi MN, Dickson EA, et al. (2021) Differences in the on- and off-tumor microbiota between right- and left-sided colorectal cancer. Microorganisms 9: 1108. https://doi.org/10.3390/microorganisms9051108
    [23] Masella AP, Bartram AK, Truszkowski JM, et al. (2012) PANDAseq: paired-end assembler for illumina sequences. BMC Bioinf 13: 31. https://doi.org/10.1186/1471-2105-13-31
    [24] Caporaso JG, Kuczynski J, Stombaugh J, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336. https://doi.org/10.1038/nmeth.f.303
    [25] Lê S, Josse J, Husson F (2008) FactoMineR: An R package for multivariate analysis. J Stat Software 25: 1-18. https://doi.org/10.18637/jss.v025.i01
    [26] Chong J, Liu P, Zhou G, et al. (2020) Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat Protoc 15: 799-821. https://doi.org/10.1038/s41596-019-0264-1
    [27] Dhariwal A, Chong J, Habib S, et al. (2017) MicrobiomeAnalyst: A web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 45: W180-W188. https://doi.org/10.1093/nar/gkx295
    [28] Bardou P, Mariette J, Escudié F, et al. (2014) Jvenn: An interactive venn diagram viewer. BMC Bioinf 15: 293. https://doi.org/10.1186/1471-2105-15-293
    [29] Kostouros A, Koliarakis I, Natsis K, et al. (2020) Large intestine embryogenesis: Molecular pathways and related disorders (review). Int J Mol Med 46: 27-57. https://doi.org/10.3892/ijmm.2020.4583
    [30] Baran B, Mert Ozupek N, Yerli Tetik N, et al. (2018) Difference between left-sided and right-sided colorectal cancer: A focused review of literature. Gastroenterol Res 11: 264-273. https://doi.org/10.14740/gr1062w
    [31] Moore WE, Moore LV (1994) The bacteria of periodontal diseases. Periodontol 2000 5: 66-77. https://doi.org/10.1111/j.1600-0757.1994.tb00019.x
    [32] Kostic AD, Chun E, Robertson L, et al. (2013) Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14: 207-215. https://doi.org/10.1016/j.chom.2013.07.007
    [33] Mima K, Nishihara R, Qian ZR, et al. (2016) Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 65: 1973-1980. https://doi.org/10.1136/gutjnl-2015-310101
    [34] Mima K, Sukawa Y, Nishihara R, et al. (2015) Fusobacterium nucleatum and T cells in colorectal carcinoma. JAMA Oncol 1: 653-661. https://doi.org/10.1001/jamaoncol.2015.1377
    [35] Rubinstein MR, Wang X, Liu W, et al. (2013) Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe 14: 195-206. https://doi.org/10.1016/j.chom.2013.07.012
    [36] Casasanta MA, Yoo CC, Udayasuryan B, et al. (2020) Fusobacterium nucleatum host-cell binding and invasion induces IL-8 and CXCL1 secretion that drives colorectal cancer cell migration. Sci Signal 13: eaba9157. https://doi.org/10.1126/scisignal.aba9157
    [37] Pleguezuelos-Manzano C, Puschhof J, Rosendahl Huber A, et al. (2020) Mutational signature in colorectal cancer caused by genotoxic pks+ E. coli. Nature 580: 269-273. https://doi.org/10.1038/s41586-020-2080-8
    [38] Kwong TNY, Wang X, Nakatsu G, et al. (2018) Association between bacteremia from specific microbes and subsequent diagnosis of colorectal cancer. Gastroenterology 155: 383-390.e8. https://doi.org/10.1053/j.gastro.2018.04.028
    [39] Biberstein EL (1990) Our understanding of the Pasteurellaceae. Can J Vet Res 54: S78-S82. https://europepmc.org/article/MED/2193710
    [40] Bottone EJ (2010) Bacillus cereus, a volatile human pathogen. Clin Microbiol Rev 23: 382-398. https://doi.org/10.1128/cmr.00073-09
    [41] Watanabe T, Hara Y, Yoshimi Y, et al. (2020) Clinical characteristics of bloodstream infection by Parvimonas micra: Retrospective case series and literature review. BMC Infect Dis 20: 578. https://doi.org/10.1186/s12879-020-05305-y
    [42] Dong Y, Zhu J, Zhang M, et al. (2020) Probiotic Lactobacillus salivarius Ren prevent dimethylhydrazine-induced colorectal cancer through protein kinase B inhibition. Appl Microbiol Biotechnol 104: 7377-7389. https://doi.org/10.1007/s00253-020-10775-w
    [43] Gamit HA, Amaresan N (2022) Isolation and identification of Beijerinckia. Practical Handbook on Agricultural Microbiology. New York: Springer 119-125. https://doi.org/10.1007/978-1-0716-1724-3_15
    [44] Riahi HS, Heidarieh P, Fatahi-Bafghi M (2022) Genus Pseudonocardia: what we know about its biological properties, abilities and current application in biotechnology. J Appl Microbiol 132: 890-906. https://doi.org/10.1111/jam.15271
    [45] Mori K, Yamaguchi K, Sakiyama Y, et al. (2009) Caldisericum exile gen. nov., sp. nov., an anaerobic, thermophilic, filamentous bacterium of a novel bacterial phylum, Caldiserica phyl. nov., originally called the candidate phylum OP5, and description of Caldisericaceae fam. nov., Caldisericales ord. nov. and Caldisericia classis nov. Int J Syst Evol Microbiol 59: 2894-2898. https://doi.org/10.1099/ijs.0.010033-0
    [46] Wang YN, Tian WY, He WH, et al. (2015) Methylopila henanense sp. nov., a novel methylotrophic bacterium isolated from tribenuron methyl-contaminated wheat soil. Antonie Van Leeuwenhoek 107: 329-336. https://doi.org/10.1007/s10482-014-0331-0
    [47] Edwards MS, McLaughlin RW, Li J, et al. (2019) Putative virulence factors of Plesiomonas shigelloides. Antonie Van Leeuwenhoek 112: 1815-1826. https://doi.org/10.1007/s10482-019-01303-6
    [48] Cho GS, Ritzmann F, Eckstein MT, et al. (2016) Quantification of Slackia and Eggerthella spp. in human feces and adhesion of representatives strains to Caco-2 cells. Front Microbiol 7: 658. https://doi.org/10.3389/fmicb.2016.00658
    [49] Alkandari SA, Bhardwaj RG, Ellepola A, et al. (2020) Proteomics of extracellular vesicles produced by Granulicatella adiacens, which causes infective endocarditis. PLoS One 15: e0227657. https://doi.org/10.1371/journal.pone.0227657
    [50] Al-Lozi A, Cai S, Chen X, et al. (2022) Granulicatella adiacens as an unusual cause of microbial keratitis and endophthalmitis: A case series and literature review. Ocul Immunol Inflammation 30: 1181-1185. https://doi.org/10.1080/09273948.2020.1860233
    [51] Gentile GL, Rupert AS, Carrasco LI, et al. (2020) Identification of a cytopathogenic toxin from Sneathia amnii. J Bacteriol 202: e00162-e00220. https://doi.org/10.1128/jb.00162-20
    [52] Vong L, Pinnell LJ, Määttänen P, et al. (2015) Selective enrichment of commensal gut bacteria protects against Citrobacter rodentium-induced colitis. Am J Physiol Gastrointest Liver Physiol 309: G181-G192. https://doi.org/10.1152/ajpgi.00053.2015
    [53] Matsuo T, Mori N, Kawai F, et al. (2021) Vagococcus fluvialis as a causative pathogen of bloodstream and decubitus ulcer infection: Case report and systematic review of the literature. J Infect Chemother 27: 359-363. https://doi.org/10.1016/j.jiac.2020.09.019
    [54] Warren RL, Freeman DJ, Pleasance S, et al. (2013) Co-occurrence of anaerobic bacteria in colorectal carcinomas. Microbiome 1: 16. https://doi.org/10.1186/2049-2618-1-16
    [55] Levine M, Collins LM, Lohinai Z (2021) Zinc chloride inhibits lysine decarboxylase production from Eikenella corrodens in vitro and its therapeutic implications. J Dent 104: 103533. https://doi.org/10.1016/j.jdent.2020.103533
    [56] Brüggemann H, Jensen A, Nazipi S, et al. (2018) Pan-genome analysis of the genus Finegoldia identifies two distinct clades, strain-specific heterogeneity, and putative virulence factors. Sci Rep 8: 266. https://doi.org/10.1038/s41598-017-18661-8
    [57] de Moreuil C, Héry-Arnaud G, David CH, et al. (2015) Finegoldia magna, not a well-known infectious agent of bacteriemic post-sternotomy mediastinitis. Anaerobe 32: 32-33. https://doi.org/10.1016/j.anaerobe.2014.11.012
    [58] Kosumi K, Hamada T, Koh H, et al. (2018) The amount of Bifidobacterium genus in colorectal carcinoma tissue in relation to tumor characteristics and clinical outcome. Am J Pathol 188: 2839-2852. https://doi.org/10.1016/j.ajpath.2018.08.015
    [59] Fahmy CA, Gamal-Eldeen AM, El-Hussieny EA, et al. (2019) Bifidobacterium longum suppresses murine colorectal cancer through the modulation of oncomiRs and tumor suppressor miRNAs. Nutr Cancer 71: 688-700. https://doi.org/10.1080/01635581.2019.1577984
    [60] Zhang Q, Zhao H, Wu D, et al. (2020) A comprehensive analysis of the microbiota composition and gene expression in colorectal cancer. BMC Microbiol 20: 308. https://doi.org/10.1186/s12866-020-01938-w
    [61] Islam MS, Kawasaki H, Nakagawa Y, et al. (2007) Labrys okinawensis sp. nov. and Labrys miyagiensis sp. nov., budding bacteria isolated from rhizosphere habitats in Japan, and emended descriptions of the genus Labrys and Labrys monachus. Int J Syst Evol Microbiol 57: 552-557. https://doi.org/10.1099/ijs.0.64239-0
    [62] Maki JJ, Looft T (2018) Megasphaera stantonii sp. nov., a butyrate-producing bacterium isolated from the cecum of a healthy chicken. Int J Syst Evol Microbiol 68: 3409-3415. https://doi.org/10.1099/ijsem.0.002991
    [63] Gough EK, Stephens DA, Moodie EE, et al. (2015) Linear growth faltering in infants is associated with Acidaminococcus sp. and community-level changes in the gut microbiota. Microbiome 3: 24. https://doi.org/10.1186/s40168-015-0089-2
    [64] Lilja S, Stoll C, Krammer U, et al. (2021) Five days periodic fasting elevates levels of longevity related Christensenella and Sirtuin expression in humans. Int J Mol Sci 22: 2331. https://doi.org/10.3390/ijms22052331
    [65] Ge T, Ekbataniamiri F, Johnson SB, et al. (2021) Interaction between Dickeya dianthicola and Pectobacterium parmentieri in potato infection under field conditions. Microorganisms 9: 316. https://doi.org/10.3390/microorganisms9020316
    [66] Cuív PÓ, Klaassens ES, Durkin AS, et al. (2011) Draft genome sequence of Turicibacter sanguinis PC909, isolated from human feces. J Bacteriol 193: 1288-1289. https://doi.org/10.1128/JB.01328-10
  • microbiol-10-04-035-s001.pdf
  • Reader Comments
  • © 2024 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(502) PDF downloads(56) Cited by(0)

Article outline

Figures and Tables

Figures(7)  /  Tables(1)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog