Alterations in Enteric Virome Are Associated With Colorectal Cancer and Survival Outcomes

Gastroenterology

Volumn 155, Issue 2, 2018, Pages 529-541.e5

  Nakatsu, Geicho ^a   Zhou, Haokui ^a   Wu, William Ka Kei ^a   Wong, Sunny Hei ^a   Coker, Olabisi Oluwabukola ^a   Dai, Zhenwei ^a   Li, Xiangchun ^a   Szeto, Chun Ho ^a   Sugimura, Naoki ^a   Lam, Thomas Yuen Tung ^a   Yu, Allen Chi Shing ^a   Wang, Xiansong ^a   Chen, Zigui ^a   Wong, Martin Chi Sang ^a   Ng, Siew Chien ^a   Chan, Matthew Tak Vai ^a   Chan, Paul Kay Sheung ^a   Chan, Francis Ka Leung ^a   Sung, Joseph Jao Yiu ^a   Yu, Jun ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Colorectal Cancer; Microbiome; Sequencing; Stool

Indexed keywords

ADULT; AREA UNDER THE CURVE; ARTICLE; AUSTRIA; BACTERIOPHAGE; BETABACULOVIRUS; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; COHORT ANALYSIS; COLORECTAL CARCINOMA; COMMENSAL; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DYSBIOSIS; EARLY CANCER; ENTEROCOCCUS; ERWINIA; FECES ANALYSIS; FEMALE; FRANCE; GERMANY; HONG KONG; HUMAN; INTESTINE FLORA; LACTOBACILLUS; LAMBDALIKEVIRUS; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; METAGENOME; METAGENOMICS; MICROBIAL COMMUNITY; MOUTH FLORA; MULIKEVIRUS; NOCARDIA; NONHUMAN; ORTHOBUNYAVIRUS; PARABACTEROIDES; PHIKZLIKEVIRUS; PRIORITY JOURNAL; PUNALIKEVIRUS; RECEIVER OPERATING CHARACTERISTIC; SP6 LIKE VIRUS; STREPTOCOCCUS PHAGE; SURVIVAL TIME; TAXONOMY; TUNALIKEVIRUS; VIRUS GENOME; CASE CONTROL STUDY; COLONOSCOPY; COLORECTAL TUMOR; DIAGNOSTIC IMAGING; EPIDEMIOLOGY; FECES; GENETICS; MIDDLE AGED; MORTALITY; PATHOLOGY; SENSITIVITY AND SPECIFICITY; SURVIVAL ANALYSIS; VALIDATION STUDY; VIROLOGY; VIRUS;

TUMOR MARKER;

AUSTRIA; BIOMARKERS, TUMOR; CASE-CONTROL STUDIES; COHORT STUDIES; COLONOSCOPY; COLORECTAL NEOPLASMS; CROSS-SECTIONAL STUDIES; DYSBIOSIS; FECES; FEMALE; FRANCE; GASTROINTESTINAL MICROBIOME; GERMANY; HONG KONG; HUMANS; MALE; METAGENOMICS; MIDDLE AGED; SENSITIVITY AND SPECIFICITY; SURVIVAL ANALYSIS; VIRUSES;

EID: 85050483352     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2018.04.018     Document Type: Article

References (85)

1. Baxter, N.T., Ruffin, M.T., Rogers, M.A.M., et al. Microbiota-based model improves the sensitivity of fecal immunochemical test for detecting colonic lesions. Genome Med, 8, 2016, 37.
2. Feng, Q., Liang, S., Jia, H., Stadlmayr, A., Tang, L., et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun, 6, 2015, 6528.
3. Yu, J., Feng, Q., Wong, S.H., Zhang, D., Liang, Q., et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut 66 (2017), 70–78.
4. Zackular, J.P., Rogers, M.A.M., Ruffin, M.T., et al. The human gut microbiome as a screening tool for colorectal cancer. Cancer Prev Res 7 (2014), 1112–1121.
5. Zeller, G., Tap, J., Voigt, A.Y., et al. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol, 10, 2014, 766.
6. Wong, S.H., Kwong, T.N.Y., Chow, T.-C., et al. Quantitation of faecal Fusobacterium improves faecal immunochemical test in detecting advanced colorectal neoplasia. Gut 66 (2017), 1441–1448.
7. Norman, J.M., Handley, S.A., Virgin, H.W., Kingdom-agnostic metagenomics and the importance of complete characterization of enteric microbial communities. Gastroenterology 146 (2014), 1459–1469.
8. Mar Rodríguez, M., Pérez, D., Javier Chaves, F., et al. Obesity changes the human gut mycobiome. Sci Rep, 5, 2015, 14600.
9. Atkinson, R.L., Viruses as an etiology of obesity. Mayo Clin Proc 82 (2007), 1192–1198.
10. Orlich, M.J., Singh, P.N., Sabaté J., et al. Vegetarian dietary patterns and the risk of colorectal cancers. JAMA Intern Med 175 (2015), 767–776.
11. Kim, M.S., Bae, J.W., Spatial disturbances in altered mucosal and luminal gut viromes of diet-induced obese mice. Environ Microbiol 18 (2016), 1498–1510.
12. Minot, S., Bryson, A., Chehoud, C., et al. Rapid evolution of the human gut virome. Proc Natl Acad Sci U S A 110 (2013), 12450–12455.
13. Minot, S., Sinha, R., Chen, J., et al. The human gut virome: Inter-individual variation and dynamic response to diet. Genome Res 21 (2011), 1616–1625.
14. Reyes, A., Blanton, L.V., Cao, S., et al. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc Natl Acad Sci U S A 112 (2015), 11941–11946.
15. Subramanian, S., Huq, S., Yatsunenko, T., et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510 (2014), 417–421.
16. Smith, M.I., Yatsunenko, T., Manary, M.J., et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339 (2013), 548–554.
17. Lim, E.S., Zhou, Y., Zhao, G., et al. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat Med 21 (2015), 1228–1234.
18. Cinek, O., Witsø E., Jeansson, S., et al. Longitudinal observation of enterovirus and adenovirus in stool samples from Norwegian infants with the highest genetic risk of type 1 diabetes. J Clin Virol 35 (2006), 33–40.
19. Foxman, E.F., Iwasaki, A., Genome-virome interactions: examining the role of common viral infections in complex disease. Nat Rev Microbiol 9 (2011), 254–264.
20. Hober, D., Sauter, P., Pathogenesis of type 1 diabetes mellitus: interplay between enterovirus and host. Nat Rev Endocrinol 6 (2010), 279–289.
21. Oikarinen, M., Tauriainen, S., Honkanen, T., et al. Detection of enteroviruses in the intestine of type 1 diabetic patients. Clin Exp Immunol 151 (2008), 71–75.
22. Oikarinen, M., Tauriainen, S., Oikarinen, S., et al. Type 1 diabetes is associated with enterovirus infection in gut mucosa. Diabetes 61 (2012), 687–691.
23. Norman, J.M., Handley, S.A., Baldridge, M.T., et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160 (2015), 447–460.
24. Wu, C.W., Ng, S.C., Dong, Y., et al. Identification of microRNA-135b in stool as a potential noninvasive biomarker for colorectal cancer and adenoma. Clin Cancer Res 20 (2014), 2994–3002.
25. Huttenhower, C., Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486 (2012), 207–214.
26. Karlsson, F.H., Tremaroli, V., Nookaew, I., et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498 (2013), 99–103.
27. Chatelier E Le, Nielsen, T., Qin, J., Prifti, E., et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500 (2013), 541–546.
28. Li, J., Jia, H., Cai, X., Zhong, H., Feng, Q., et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol 32 (2014), 834–841.
29. Nielsen, H.B., Almeida, M., Juncker, A.S., et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat Biotechnol 32 (2014), 822–832.
30. Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (2012), 55–60.
31. Qin, N., Yang, F., Li, A., Prifti, E., Chen, Y., Shao, L., et al. Alterations of the human gut microbiome in liver cirrhosis. Nature 513 (2014), 59–64.
32. Zhang, X., Zhang, D., Jia, H., Feng, Q., Wang, D., Liang, D., et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med 21 (2015), 895–905.
33. Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 (2014), 2114–2120.
34. Wood, D.E., Salzberg, S.L., Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol, 15, 2014, R46.
35. Marçais, G., Kingsford, C., A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27 (2011), 764–770.
36. Morgulis, A., Gertz, E.M., Schäffer, A.A., et al. A fast and symmetric DUST implementation to mask low-complexity DNA sequences. J Comput Biol 13 (2006), 1028–1040.
37. Paulson, J.N., Stine, O.C., Bravo, H.C., et al. Differential abundance analysis for microbial marker-gene surveys. Nat Methods 10 (2013), 1200–1202.
38. Breiman, L., Random forests. Mach Learn 45 (2001), 5–32.
39. Mason, S.J., Graham, N.E., Areas beneath the relative operating characteristics (ROC) and relative operating levels (ROL) curves: statistical significance and interpretation. Q J R Meteorol Soc 128 (2002), 2145–2166.
40. Holmes, I., Harris, K., Quince, C., Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS One, 7, 2012, e30126.
41. Ren, B., Bacallado, S., Favaro, S., et al. Bayesian nonparametric ordination for the analysis of microbial communities. J Am Stat Assoc 112 (2017), 1430–1442.
42. Ishwaran, H., Kogalur, U.B., Blackstone, E.H., et al. Random survival forests. Ann Appl Stat 2 (2008), 841–860.
43. Friedman, J., Hastie, T., Tibshirani, R., Sparse inverse covariance estimation with the graphical lasso. Biostatistics 9 (2008), 432–441.
44. Zhao, T., Liu, H., Roeder, K., et al. The huge package for high-dimensional undirected graph estimation in R. J Mach Learn Res 13 (2012), 1059–1062.
45. Chen, J., Chen, Z., Extended Bayesian information criteria for model selection with large model spaces. Biometrika 95 (2008), 759–771.
46. Diedenhofen, B., Musch, J., Cocor: a comprehensive solution for the statistical comparison of correlations. PLoS One, 2015, 10.
47. Csárdi, G., Nepusz, T., The igraph software package for complex network research. InterJournal 1695 (2006), 1–9.
48. Chen, T., Yu, W.-H., Izard, J., et al. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford), 2010, 2010, baq013.
49. Elliott, R.M., Orthobunyaviruses: recent genetic and structural insights. Nat Rev Microbiol 12 (2014), 673–685.
50. Geuking, M.B., Weber, J., Dewannieux, M., et al. Recombination of retrotransposon and exogenous RNA virus results in nonretroviral cDNA integration. Science 323 (2009), 393–396.
51. Horie, M., Honda, T., Suzuki, Y., et al. Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463 (2010), 84–87.
52. Klenerman, P., Hengartner, H., Zinkernagel, R.M., A non-retroviral RNA virus persists in DNA form. Nature 390 (1997), 298–301.
53. Zhdanov, V., Integration of viral genomes. Nature 256 (1975), 471–473.
54. Bodaghi, S., Yamanegi, K., Xiao, S.-Y., et al. Colorectal papillomavirus infection in patients with colorectal cancer. Clin Cancer Res 11 (2005), 2862–2867.
55. Enam, S., Valle L Del, Lara, C., et al. Association of human polyomavirus JCV with colon cancer: Evidence for interaction of viral T-antigen and β-catenin. Cancer Res 62 (2002), 7093–7101.
56. Goel, A., Li, M.S., Nagasaka, T., et al. Association of JC virus T-antigen expression with the methylator phenotype in sporadic colorectal cancers. Gastroenterology 130 (2006), 1950–1961.
57. Hori, R., Murai, Y., Tsuneyama, K., et al. Detection of JC virus DNA sequences in colorectal cancers in Japan. Virchows Arch 447 (2005), 723–730.
58. Karpinski, P., Myszka, A., Ramsey, D., et al. Detection of viral DNA sequences in sporadic colorectal cancers in relation to CpG island methylation and methylator phenotype. Tumor Biol 32 (2011), 653–659.
59. Mou, X., Chen, L., Liu, F., et al. Prevalence of JC virus in Chinese patients with colorectal cancer. PLoS One, 7, 2012, e35900.
60. Ouaïssi, M., Studer, A.-S., Mege, D., et al. Characteristics and natural history of patients with colorectal cancer complicated by infectious endocarditis. Case control study of 25 patients. Anticancer Res 34 (2014), 349–353.
61. Theodoropoulos, G., Panoussopoulos, D., Papaconstantinou, I., et al. Assessment of JC polyoma virus in colon neoplasms. Dis Colon Rectum 48 (2005), 86–91.
62. Vilkin, A., Ronen, Z., Levi, Z., et al. Presence of JC virus DNA in the tumor tissue and normal mucosa of patients with sporadic colorectal cancer (CRC) or with positive family history and Bethesda criteria. Dig Dis Sci 57 (2012), 79–84.
63. zur Hausen, H., Red meat consumption and cancer: Reasons to suspect involvement of bovine infectious factors in colorectal cancer. Int J Cancer 130 (2012), 2475–2483.
64. Boleij, A., Hechenbleikner, E.M., Goodwin, A.C., et al. The bacteroides fragilis toxin gene is prevalent in the colon mucosa of colorectal cancer patients. Clin Infect Dis 60 (2015), 208–215.
65. Castellarin, M., Warren, R.L., Freeman, J.D., et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22 (2012), 299–306.
66. Cuevas-Ramos, G., Petit, C.R., Marcq, I., et al. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci U S A 107 (2010), 11537–11542.
67. Niu, Y.D., McAllister, T.A., Nash, J.H.E., et al. Four Escherichia coli O157:H7 phages: a new bacteriophage genus and taxonomic classification of T1-like phages. PLoS One, 9, 2014.
68. Dejea, C.M., Wick, E.C., Hechenbleikner, E.M., et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A 111 (2014), 18321–18326.
69. Johnson, C.H., Dejea, C.M., Edler, D., et al. Metabolism links bacterial biofilms and colon carcinogenesis. Cell Metab 21 (2015), 891–897.
70. Secor, P.R., Sweere, J.M., Michaels, L.A., et al. Filamentous bacteriophage promote biofilm assembly and function. Cell Host Microbe 18 (2015), 549–559.
71. Waldor, M., Mekalanos, J., Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272 (1996), 1910–1914.
72. Burstein, D., Sun, C.L., Brown, C.T., et al. Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems. Nat Commun, 7, 2016, 10613.
73. Tjalsma, H., Boleij, A., Marchesi, J.R., et al. A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol 10 (2012), 575–582.
74. Teraishi, F., Shimamura, H., Suzuki, T., et al. Cytomegalovirus colitis after systemic chemotherapy in a patient with recurrent colon cancer: a case report. J Med Case Reports, 2, 2008, 289.
75. Chen, H.P., Jiang, J.K., Lai, P.Y., et al. Tumoral presence of human cytomegalovirus is associated with shorter disease-free survival in elderly patients with colorectal cancer and higher levels of intratumoral interleukin-17. Clin Microbiol Infect 20 (2014), 664–671.
76. Dimberg, J., Trinh Hong, T., Skarstedt, M., et al. Detection of cytomegalovirus DNA in colorectal tissue from Swedish and Vietnamese patients with colorectal cancer. Anticancer Res 33 (2013), 4947–4950.
77. Assinger, A., Kral, J.B., Yaiw, K.C., et al. Human cytomegalovirus-platelet interaction triggers toll-like receptor 2-dependent proinflammatory and proangiogenic responses. Arterioscler Thromb Vasc Biol 34 (2014), 801–809.
78. Courivaud, C., Bamoulid, J., Chalopin, J.-M., et al. Cytomegalovirus exposure and cardiovascular disease in kidney transplant recipients. J Infect Dis 207 (2013), 1569–1575.
79. Yaiw, K.-C., Ovchinnikova, O., Taher, C., et al. High prevalence of human cytomegalovirus in carotid atherosclerotic plaques obtained from Russian patients undergoing carotid endarterectomy. Herpesviridae, 4, 2013, 3.
80. 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, 30, 2011, 11.
81. Boleij, A., Gelder MMHJ van, Swinkels, D.W., et al. Clinical importance of Streptococcus gallolyticus infection among colorectal cancer patients: systematic review and meta-analysis. Clin Infect Dis 53 (2011), 870–878.
82. Kleiner, M., Hooper, L.V., Duerkop, B.A., Evaluation of methods to purify virus-like particles for metagenomic sequencing of intestinal viromes. BMC Genomics, 16, 2015, 7.
83. Paez-Espino, D., Eloe-Fadrosh, E.A., Pavlopoulos, G.A., et al. Uncovering Earth's virome. Nature 536 (2016), 425–430.
84. Nguyen, S., Baker, K., Padman, B.S., et al. Bacteriophage transcytosis provides a mechanism to cross epithelial cell layers. mBio 8 (2017), e01874–e01917.
85. Lehti, T.A., Pajunen, M.I., Skog, M.S., et al. Internalization of a polysialic acid-binding Escherichia coli bacteriophage into eukaryotic neuroblastoma cells. Nat Commun, 8, 2017, 1915.