A bacterial driver–passenger model for colorectal cancer: beyond the usual suspects

Tjalsma, Harold; Boleij, Annemarie; Marchesi, Julian R.; Dutilh, Bas E.

doi:10.1038/nrmicro2819

Cited by 903Gut microbiota and healthGenetic factors in colorectal cancerOral microbiology and periodontitis research

A bacterial driver–passenger model for colorectal cancer: beyond the usual suspects

Tjalsma, Harold, Boleij, Annemarie, Marchesi, Julian R., Dutilh, Bas E.·2012·Nature Reviews Microbiology

DOI 10.1038/nrmicro2819

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Abstract

Cancer has long been considered a genetic disease. However, accumulating evidence supports the involvement of infectious agents in the development of cancer, especially in those organs that are continuously exposed to microorganisms, such as the large intestine. Recent next-generation sequencing studies of the intestinal microbiota now offer an unprecedented view of the aetiology of sporadic colorectal cancer and have revealed that the microbiota associated with colorectal cancer contains bacterial species that differ in their temporal associations with developing tumours. Here, we propose a bacterial driver-passenger model for microbial involvement in the development of colorectal cancer and suggest that this model be incorporated into the genetic paradigm of cancer progression.

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The driver-passenger model for colorectal cancer proposes that a first hit by indigenous intestinal bacteria ('bacterial drivers') drives DNA damage that contributes to CRC initiation, and that tumorigenesis then induces intestinal niche alterations favouring proliferation of opportunistic bacteria ('bacterial passengers').
“Tjalsma et al90 have also proposed the ‘driver-passenger’ model for CRC: a first hit by indigenous intestinal bacteria (‘bacterial drivers’), which drive the DNA damage that contributes to CRC initiation. Second, tumorigenesis induces intestinal niche alterations that favour the proliferation of opportunistic bacteria (‘bacterial passengers’).”
From The gut microbiota and host health: a new clinical frontier (2016) · cites this paper as [90]

Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008
Ferlay, J., Shin, H.-R., Bray, F., Forman, D., Mathers, C., & Parkin, D. M. (2010) · International Journal of Cancer · doi:10.1002/ijc.25516 · Cited by 22,207 · see citing works
A human gut microbial gene catalogue established by metagenomic sequencing
MetaHIT Consortium, Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., et al. (2010) · Nature · doi:10.1038/nature08821 · Cited by 11,624 · see citing works
Cancer statistics, 2009
Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., & Thun, M. J. (2009) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.20006 · Cited by 9,709 · see citing works
Diversity of the Human Intestinal Microbial Flora
Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S. R., Nelson, K. E., & Relman, D. A. (2005) · Science · doi:10.1126/science.1110591 · Cited by 7,913 · see citing works
Enterotypes of the human gut microbiome
MetaHIT Consortium (additional members), Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., et al. (2011) · Nature · doi:10.1038/nature09944 · Cited by 7,548 · see citing works
Metagenomic Analysis of the Human Distal Gut Microbiome
Gill, S. R., Pop, M., DeBoy, R. T., Eckburg, P. B., Turnbaugh, P. J., Samuel, B. S., Gordon, J. I., Relman, D. A., Fraser-Liggett, C. M., & Nelson, K. E. (2006) · Science · doi:10.1126/science.1124234 · Cited by 4,699 · see citing works
Wnt signalling in stem cells and cancer
Reya, T., & Clevers, H. (2005) · Nature · doi:10.1038/nature03319 · Cited by 3,666 · see citing works
The cancer genome
Stratton, M. R., Campbell, P. J., & Futreal, P. A. (2009) · Nature · doi:10.1038/nature07943 · Cited by 3,458 · see citing works
Bacterial Community Variation in Human Body Habitats Across Space and Time
Costello, E. K., Lauber, C. L., Hamady, M., Fierer, N., Gordon, J. I., & Knight, R. (2009) · Science · doi:10.1126/science.1177486 · Cited by 3,231 · see citing works
Transforming growth factor-β induces development of the TH17 lineage
Mangan, P. R., Harrington, L. E., O'Quinn, D. B., Helms, W. S., Bullard, D. C., Elson, C. O., Hatton, R. D., Wahl, S. M., Schoeb, T. R., & Weaver, C. T. (2006) · Nature · doi:10.1038/nature04754 · Cited by 3,087 · see citing works
Review article: the role of butyrate on colonic function
HAMER, H. M., JONKERS, D., VENEMA, K., VANHOUTVIN, S., TROOST, F. J., & BRUMMER, R. ‐. (2008) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2007.03562.x · Cited by 2,721 · see citing works
Crypt stem cells as the cells-of-origin of intestinal cancer
Barker, N., Ridgway, R. A., van Es, J. H., van de Wetering, M., Begthel, H., van den Born, M., Danenberg, E., Clarke, A. R., Sansom, O. J., & Clevers, H. C. (2008) · Nature · doi:10.1038/nature07602 · Cited by 2,159 · see citing works
Cancer epigenomics: DNA methylomes and histone-modification maps
Esteller, M. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2005 · Cited by 2,150 · see citing works
Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma
Castellarin, M., Warren, R. L., Freeman, J. D., Dreolini, L., Krzywinski, M., Strauss, J., Barnes, R., Watson, P., Allen-Vercoe, E., Moore, R. A., et al. (2012) · Genome Research · doi:10.1101/gr.126516.111 · Cited by 2,043 · see citing works
Genomic analysis identifies association of Fusobacterium with colorectal carcinoma
Kostic, A. D., Gevers, D., Pedamallu, C. S., Michaud, M., Duke, F., Earl, A. M., Ojesina, A. I., Jung, J., Bass, A. J., Tabernero, J., et al. (2012) · Genome Research · doi:10.1101/gr.126573.111 · Cited by 1,960 · see citing works
The multistep nature of cancer
Vogelstein, B., & Kinzler, K. W. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90209-z · Cited by 1,858 · see citing works
A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses
Wu, S., Rhee, K.-J., Albesiano, E., Rabizadeh, S., Wu, X., Yen, H.-R., Huso, D. L., Brancati, F. L., Wick, E., McAllister, F., et al. (2009) · Nature Medicine · doi:10.1038/nm.2015 · Cited by 1,812 · see citing works
Molecular Genetics of Colorectal Cancer
Fearon, E. R. (2011) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-011110-130235 · Cited by 1,805 · see citing works
Composition, variability, and temporal stability of the intestinal microbiota of the elderly
Claesson, M. J., Cusack, S., O'Sullivan, O., Greene-Diniz, R., de Weerd, H., Flannery, E., Marchesi, J. R., Falush, D., Dinan, T., Fitzgerald, G., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000097107 · Cited by 1,754 · see citing works
Self-citation
Dominant and diet-responsive groups of bacteria within the human colonic microbiota
Walker, A. W., Ince, J., Duncan, S. H., Webster, L. M., Holtrop, G., Ze, X., Brown, D., Stares, M. D., Scott, P., Bergerat, A., et al. (2011) · The ISME Journal · doi:10.1038/ismej.2010.118 · Cited by 1,632 · see citing works
Resident Enteric Bacteria Are Necessary for Development of Spontaneous Colitis and Immune System Activation in Interleukin-10-Deficient Mice
Sellon, R. K., Tonkonogy, S., Schultz, M., Dieleman, L. A., Grenther, W., Balish, E., Rennick, D. M., & Sartor, R. B. (1998) · Infection and Immunity · doi:10.1128/iai.66.11.5224-5231.1998 · Cited by 1,483 · see citing works
Oral multispecies biofilm development and the key role of cell–cell distance
Kolenbrander, P. E., Palmer, R. J., Periasamy, S., & Jakubovics, N. S. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2381 · Cited by 1,309 · see citing works
Screening for Colorectal Cancer
Eddy, D. M. (1990) · Annals of Internal Medicine · doi:10.7326/0003-4819-113-5-373 · Cited by 1,207 · see citing works
Escherichia coli Induces DNA Double-Strand Breaks in Eukaryotic Cells
Nougayrède, J.-P., Homburg, S., Taieb, F., Boury, M., Brzuszkiewicz, E., Gottschalk, G., Buchrieser, C., Hacker, J., Dobrindt, U., & Oswald, E. (2006) · Science · doi:10.1126/science.1127059 · Cited by 1,188 · see citing works
The core gut microbiome, energy balance and obesity
Turnbaugh, P. J., & Gordon, J. I. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.174136 · Cited by 993 · see citing works
Quantitative Metabolome Profiling of Colon and Stomach Cancer Microenvironment by Capillary Electrophoresis Time-of-Flight Mass Spectrometry
Hirayama, A., Kami, K., Sugimoto, M., Sugawara, M., Toki, N., Onozuka, H., Kinoshitá, T., Saito, N., Ochiai, A., Tomita, M., et al. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-4806 · Cited by 959 · see citing works
Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells
Cuevas-Ramos, G., Petit, C. R., Marcq, I., Boury, M., Oswald, E., & Nougayrède, J.-P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1001261107 · Cited by 855 · see citing works
The Battle for Iron between Bacterial Pathogens and Their Vertebrate Hosts
Skaar, E. P. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000949 · Cited by 796 · see citing works
Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis -induced colon tumorigenesis
Goodwin, A. C., Shields, C. E. D., Wu, S., Huso, D. L., Wu, X., Murray-Stewart, T. R., Hacker-Prietz, A., Rabizadeh, S., Woster, P. M., Sears, C. L., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010203108 · Cited by 612 · see citing works
Invasive potential of gut mucosa-derived fusobacterium nucleatum positively correlates with IBD status of the host
Strauss, J., Kaplan, G. G., Beck, P. L., Rioux, K. P., Panaccione, R., DeVinney, R., Lynch, T., & Allen‐Vercoe, E. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21606 · Cited by 574 · see citing works
Diversity of the human gastrointestinal tract microbiota revisited
Rajilić‐Stojanović, M., Smidt, H., & De Vos, W. M. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01369.x · Cited by 559 · see citing works
Towards the Human Colorectal Cancer Microbiome
Marchesi, J. R., Dutilh, B. E., Hall, N., Peters, W. H. M., Roelofs, R., Boleij, A., & Tjalsma, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020447 · Cited by 552 · see citing works
Self-citation
Association ofStreptococcus boviswith Carcinoma of the Colon
Klein, R. S., Recco, R. A., Catalano, M. T., Edberg, S. C., Casey, J. I., & Steigbigel, N. H. (1977) · New England Journal of Medicine · doi:10.1056/nejm197710132971503 · Cited by 532 · see citing works
Assembly of the human intestinal microbiota
Dethlefsen, L., Eckburg, P. B., Bik, E. M., & Relman, D. A. (2006) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2006.06.013 · Cited by 509 · see citing works
Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA
Huycke, M. M., Abrams, V., & Moore, D. R. (2002) · Carcinogenesis · doi:10.1093/carcin/23.3.529 · Cited by 489 · see citing works
A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer
Ulger Toprak, N., Yagci, A., Gulluoglu, B. M., Akin, M. L., Demirkalem, P., Celenk, T., & Soyletir, G. (2006) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2006.01494.x · Cited by 454 · see citing works
Risk for colorectal cancer in ulcerative colitis: Changes, causes and management strategies
Lakatos, P. L., & Lakatos, L. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.3937 · Cited by 443 · see citing works
Modulation of the Intestinal Microbiota Alters Colitis-Associated Colorectal Cancer Susceptibility
Uronis, J. M., Mühlbauer, M., Herfarth, H. H., Rubinas, T. C., Jones, G. S., & Jobin, C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006026 · Cited by 425 · see citing works
Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas
Shen, X. J., Rawls, J. F., Randall, T. A., Burcall, L., Mpande, C., Jenkins, N., Jovov, B., Abdo, Z., Sandler, R. S., & Keku, T. O. (2010) · Gut Microbes · doi:10.4161/gmic.1.3.12360 · Cited by 418 · see citing works
Enterotoxigenic Bacteroides fragilis : a Rogue among Symbiotes
Sears, C. L. (2009) · Clinical Microbiology Reviews · doi:10.1128/cmr.00053-08 · Cited by 412 · see citing works
Clinical Importance of Streptococcus gallolyticus infection among colorectal cancer patients: systematic review and meta-analysis
Boleij, A., van Gelder, M. M. H. J., Swinkels, D. W., & Tjalsma, H. (2011) · Clinical Infectious Diseases · doi:10.1093/cid/cir609 · Cited by 377 · see citing works
Self-citation
Genome Sequence and Analysis of the Oral Bacterium Fusobacterium nucleatum Strain ATCC 25586
Kapatral, V., Anderson, I., Ivanova, N., Reznik, G., Los, T., Lykidis, A., Bhattacharyya, A., Bartman, A. E., Gardner, W. L., Grechkin, G., et al. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.7.2005-2018.2002 · Cited by 347 · see citing works
Gastrointestinal microflora, food components and colon cancer prevention
Davis, C. D., & Milner, J. A. (2009) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2009.06.001 · Cited by 335 · see citing works
A two-step model for colon adenoma initiation and progression caused by APC loss
Phelps, R. A., Chidester, S., Dehghanizadeh, S., Phelps, J., Sandoval, I. T., Rai, K., Broadbent, T., Sarkar, S., Burt, R. W., & Jones, D. A. (2009) · Cell · doi:10.1016/j.cell.2009.02.037 · Cited by 286 · see citing works
Screening for Colorectal Cancer
Lieberman, D. A. (2009) · New England Journal of Medicine · doi:10.1056/nejmcp0902176 · Cited by 270 · see citing works
The Human Microbiome Project in 2011 and Beyond
Proctor, L. M. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.10.001 · Cited by 269 · see citing works
Bacteroides fragilis toxin stimulates intestinal epithelial cell shedding and γ-secretase-dependent E-cadherin cleavage
Wu, S., Rhee, K., Zhang, M., Franco, A. A., & Sears, C. L. (2007) · Journal of Cell Science · doi:10.1242/jcs.03455 · Cited by 263 · see citing works
Perspective: Alpha-Bugs, Their Microbial Partners, and the Link to Colon Cancer
Sears, C. L., & Pardoll, D. M. (2011) · The Journal of Infectious Diseases · doi:10.1093/jinfdis/jiq061 · Cited by 259 · see citing works
Colon Cancer: A Civilization Disorder
Watson, A. J. M., & COLLINS, P. D. (2011) · Digestive Diseases · doi:10.1159/000323926 · Cited by 258 · see citing works
Colon cancer stem cells
Ricci‐Vitiani, L., Fabrizi, E., Palio, E., & Maria, R. D. (2009) · Journal of Molecular Medicine · doi:10.1007/s00109-009-0518-4 · Cited by 254 · see citing works
The Fusobacterium nucleatum outer membrane protein RadD is an arginine‐inhibitable adhesin required for inter‐species adherence and the structured architecture of multispecies biofilm
Kaplan, C. W., Lux, R., Haake, S. K., & Shi, W. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06503.x · Cited by 252 · see citing works
Th17 Cytokines and the Gut Mucosal Barrier
Blaschitz, C., & Raffatellu, M. (2010) · Journal of Clinical Immunology · doi:10.1007/s10875-010-9368-7 · Cited by 247 · see citing works
Promotion of intestinal carcinogenesis by Streptococcus bovis
Ellmerich, S., Scholler, M., Duranton, B., Gossé, F., Galluser, M., Klein, J.-P., & Raul, F. (2000) · Carcinogenesis · doi:10.1093/carcin/21.4.753 · Cited by 244 · see citing works
Extracellular Superoxide Production by Enterococcus faecalis Promotes Chromosomal Instability in Mammalian Cells
Wang, X., & Huycke, M. M. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.11.040 · Cited by 243 · see citing works
Molecular detection, quantification, and isolation of Streptococcus gallolyticus bacteria colonizing colorectal tumors: inflammation-driven potential of carcinogenesis via IL-1, COX-2, and IL-8
Abdulamir, A. S., Hafidh, R. R., & Bakar, F. A. (2010) · Molecular Cancer · doi:10.1186/1476-4598-9-249 · Cited by 240 · see citing works
Mucosa-Associated Bacterial Diversity in Relation to Human Terminal Ileum and Colonic Biopsy Samples
Ahmed, S., Macfarlane, G. T., Fite, A., McBain, A. J., Gilbert, P., & Macfarlane, S. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01143-07 · Cited by 227 · see citing works
Epithelial barrier: an interface for the cross‐communication between gut flora and immune system
Goto, Y., & Kiyono, H. (2011) · Immunological Reviews · doi:10.1111/j.1600-065x.2011.01078.x · Cited by 212 · see citing works
Enterococcus faecalis Induces Aneuploidy and Tetraploidy in Colonic Epithelial Cells through a Bystander Effect
Wang, X., Allen, T. D., May, R. J., Lightfoot, S. A., Houchen, C. W., & Huycke, M. M. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-1551 · Cited by 205 · see citing works
Intestinal neoplasia in the ApcMin mouse: independence from the microbial and natural killer (beige locus) status.
Dove, W. F., Clipson, L. J., Gould, K. A., Luongo, C., Marshall, D. J., Moser, A. R., Newton, M. A., & Jacoby, R. F. (1997) · PubMed · Cited by 159 · see citing works
Bacterial Diarrhea
DuPont, H. L. (2009) · New England Journal of Medicine · doi:10.1056/nejmcp0904162 · Cited by 155 · see citing works
Novel Clues on the Specific Association of Streptococcus gallolyticus subsp gallolyticus With Colorectal Cancer
Boleij, A., Muytjens, C. M. J., Bukhari, S. I., Cayet, N., Glaser, P., Hermans, P. W. M., Swinkels, D. W., Bolhuis, A., & Tjalsma, H. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiq169 · Cited by 153 · see citing works
Self-citation
Association of EnterotoxigenicBacteroides fragilisInfection with Inflammatory Diarrhea
Sears, C. L., Islam, S., Saha, A., Jamil, M., Alam, N. H., Faruque, S. M., Salam, M. A., Shin, J. W., Hecht, D. W., Weintraub, A., et al. (2008) · Clinical Infectious Diseases · doi:10.1086/591130 · Cited by 152 · see citing works
Fusobacterium nucleatum
Allen‐Vercoe, E., Strauss, J., & Chadee, K. (2011) · Gut Microbes · doi:10.4161/gmic.2.5.18603 · Cited by 145 · see citing works
Gut bacteria in health and disease: a survey on the interface between intestinal microbiology and colorectal cancer
Boleij, A., & Tjalsma, H. (2012) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2012.00218.x · Cited by 145 · see citing works
Self-citation
Genome Sequence ofStreptococcus gallolyticus: Insights into Its Adaptation to the Bovine Rumen and Its Ability To Cause Endocarditis
Rusniok, C., Couvé, E., Cunha, V. D., Gana, R. E., Zidane, N., Bouchier, C., Poyart, C., Leclercq, R., Trieu‐Cuot, P., & Glaser, P. (2010) · Journal of Bacteriology · doi:10.1128/jb.01659-09 · Cited by 137 · see citing works
Butyrate and Wnt signaling: a possible solution to the puzzle of dietary fiber and colon cancer risk?
Bordonaro, M., Lazarova, D. L., & Sartorelli, A. C. (2008) · Cell Cycle · doi:10.4161/cc.7.9.5818 · Cited by 130 · see citing works
The Search for Infectious Causes of Human Cancers: Where and Why (Nobel Lecture)
Hausen, H. Z. (2009) · Angewandte Chemie International Edition · doi:10.1002/anie.200901917 · Cited by 123 · see citing works
Enterotoxigenic Bacteroides fragilis (ETBF)-mediated colitis in Min ( Apc +/- ) mice: a human commensal-based murine model of colon carcinogenesis
Housseau, F., & Sears, C. L. (2010) · Cell Cycle · doi:10.4161/cc.9.1.10352 · Cited by 110 · see citing works
Pyrosequencing-Based Analysis of the Mucosal Microbiota in Healthy Individuals Reveals Ubiquitous Bacterial Groups and Micro-Heterogeneity
Hong, P., Croix, J. A., Greenberg, E., Gaskins, H. R., & Mackie, R. I. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025042 · Cited by 107 · see citing works
Slackia equolifaciens sp. nov., a human intestinal bacterium capable of producing equol
Jin, J., Kitahara, M., Sakamoto, M., Hattori, M., & Benno, Y. (2009) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.016774-0 · Cited by 104 · see citing works
The Bacteroides fragilis Toxin Binds to a Specific Intestinal Epithelial Cell Receptor
Wu, S., Shin, J. W., Zhang, G., Cohen, M. B., Franco, A. A., & Sears, C. L. (2006) · Infection and Immunity · doi:10.1128/iai.00060-06 · Cited by 103 · see citing works
Profiling the humoral immune response in colon cancer patients: Diagnostic antigens from Streptococcus bovis
Tjalsma, H., Schöller‐Guinard, M., Lasonder, E., Ruers, T. J. M., Willems, H. L., & Swinkels, D. W. (2006) · International Journal of Cancer · doi:10.1002/ijc.22116 · Cited by 97 · see citing works
Self-citation
Human distal gut microbiome
Marchesi, J. R. (2011) · Environmental Microbiology · doi:10.1111/j.1462-2920.2011.02574.x · Cited by 90 · see citing works
Self-citation
Progression of Atrophic Gastritis and Intestinal Metaplasia Drives Helicobacter pylori Out of the Gastric Mucosa
Kang, H. Y., Kim, N., Park, Y. S., Hwang, J., Kim, J., Jeong, S., Lee, D. H., Jung, H. C., & Song, I. S. (2006) · Digestive Diseases and Sciences · doi:10.1007/s10620-006-9276-0 · Cited by 89 · see citing works
Nuclear translocation of beta-catenin in hereditary and carcinogen- induced intestinal adenomas
Sheng, H. (1998) · Carcinogenesis · doi:10.1093/carcin/19.4.543 · Cited by 88 · see citing works
New perspectives on APC control of cell fate and proliferation in colorectal cancer
Phelps, R. A., Broadbent, T. J., Stafforini, D. M., & Jones, D. A. (2009) · Cell Cycle · doi:10.4161/cc.8.16.9278 · Cited by 76 · see citing works
Molecular characterization of the bacteria adherent to human colorectal mucosa
Green, G. L., Brostoff, J., Hudspith, B. N., Michael, M., Mylonaki, M., Rayment, N. B., Staines, N. A., Sanderson, J. D., Rampton, D. S., & Bruce, K. D. (2006) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2005.02783.x · Cited by 75 · see citing works
Adherence to Streptococci Facilitates Fusobacterium nucleatum Integration into an Oral Microbial Community
He, X., Hu, W., Kaplan, C. W., Guo, L., Shi, W., & Lux, R. (2011) · Microbial Ecology · doi:10.1007/s00248-011-9989-2 · Cited by 64 · see citing works
Infectious causes of cancer and their detection
Dalton-Griffin, L., & Kellam, P. (2009) · Journal of Biology · doi:10.1186/jbiol168 · Cited by 64 · see citing works
Increased exposure to bacterial antigen RpL7/L12 in early stage colorectal cancer patients
Boleij, A., Roelofs, R., Schaeps, R. M. J., Schülin, T., Glaser, P., Swinkels, D. W., Kato, I., & Tjalsma, H. (2010) · Cancer · doi:10.1002/cncr.25212 · Cited by 54 · see citing works
Self-citation
Host Genetics and Environmental Factors Regulate Ecological Succession of the Mouse Colon Tissue-Associated Microbiota
SMITH, P. F., Siddharth, J., Pearson, R., Holway, N., Shaxted, M., Butler, M., Clark, N., Jamontt, J., Watson, R. P., Sanmugalingam, D., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030273 · Cited by 52 · see citing works
Unusual Bacterial Infections and Colorectal Carcinoma— Streptococcus bovis and Clostridium septicum : Report of Three Cases
Wentling, G. K., Metzger, P. P., Dozois, E. J., Chua, H. K., & Krishna, M. (2006) · Diseases of the Colon & Rectum · doi:10.1007/s10350-006-0576-4 · Cited by 43 · see citing works
Equol induces apoptosis through cytochrome c-mediated caspases cascade in human breast cancer MDA-MB-453 cells
Choi, E. J., Ahn, W. S., & Bae, S. M. (2008) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2008.09.031 · Cited by 42 · see citing works
Identification of biomarkers for colorectal cancer through proteomics-based approaches
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Authors: Tjalsma, H., Boleij, A., Marchesi, J. R., & Dutilh, B. E.
Affiliations: Radboud University Nijmegen (NL)
Johns Hopkins University (US)
Cardiff University (GB)
San Diego State University (US)
Corresponding author: Tjalsma, Harold
Marchesi, Julian R.
ORCID: Boleij, Annemarie
Marchesi, Julian R.
Dutilh, Bas E.
Venue: Nature Reviews Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2012-06-25
Volume: 10
Issue: 8
Pages: 575-582
ISSN: 1740-1526 (ISSN-L)
1740-1534
DOI: 10.1038/nrmicro2819
OpenAlex: W2101565190
Cited by: 903
References: 92
Citations by year: 2026: 58 · 2025: 66 · 2024: 94 · 2023: 94 · 2022: 96 · 2021: 88 · 2020: 77 · 2019: 66 · 2018: 67 · 2017: 50 · 2016: 44 · 2015: 34 · 2014: 30 · 2013: 28 · 2012: 10
FWCI: 2.97
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Reviews Microbiology (publishedVersion)
PubMed (publishedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Funders: KWF Kankerbestrijding
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Keywords: colorectal cancer, gut microbiota, cancer etiology, tumor progression
MeSH terms: Bacteria, Bacterial Infections, Humans, Models, Biological, Colorectal Neoplasms, Biota

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A bacterial driver–passenger model for colorectal cancer: beyond the usual suspects

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