Top

Published in:

01-03-2020 | Human Papillomavirus | Review

Enteric Virome and Carcinogenesis in the Gut

Authors: Cade Emlet, Mack Ruffin, Regina Lamendella

Published in: Digestive Diseases and Sciences | Issue 3/2020

Abstract

Colorectal cancer (CRC) is a leading cause of cancer-related deaths in both the USA and the world. Recent research has demonstrated the involvement of the gut microbiota in CRC development and progression. Microbial biomarkers of disease have focused primarily on the bacterial component of the microbiome; however, the viral portion of the microbiome, consisting of both bacteriophages and eukaryotic viruses, together known as the virome, has been lesser studied. Here we review the recent advancements in high-throughput sequencing (HTS) technologies and bioinformatics, which have enabled scientists to better understand how viruses might influence the development of colorectal cancer. We discuss the contemporary findings revealing modulations in the virome and their correlation with CRC development and progression. While a variety of challenges still face viral HTS detection in clinical specimens, we consider herein numerous next steps for future basic and clinical research. Clinicians need to move away from a single infectious agent model for disease etiology by grasping new, more encompassing etiological paradigms, in which communities of various microbial components interact with each other and the host. The reporting and indexing of patient health information, socioeconomic data, and other relevant metadata will enable identification of predictive variables and covariates of viral presence and CRC development. Altogether, the virome has a more profound role in carcinogenesis and cancer progression than once thought, and viruses, specific for either human cells or bacteria, are clinically relevant in understanding CRC pathology, patient prognosis, and treatment development.

Pan D, Nolan J, Williams KH, et al. Abundance and distribution of microbial cells and viruses in an alluvial aquifer. Front Microbiol. 2017;8:1199.PubMedPubMedCentral

Rohwer F, Prangishvili D, Lindell D. Roles of viruses in the environment. Environ Microbiol. 2009;11:2771–2774.PubMed

Navarro F, Muniesa M. Phages in the Human Body. Front Microbiol. 2017;8:566.PubMedPubMedCentral

Bekliz M, Colson P, La Scola B. The expanding family of virophages. Viruses. 2016;8:317.PubMedCentral

Caputo M, Zoch-Lesniak B, Karch A, et al. Bacterial community structure and effects of picornavirus infection on the anterior nares microbiome in early childhood. BMC Microbiol. 2019;19:1. https://doi.org/10.1186/s12866-018-1372-8.CrossRefPubMedPubMedCentral

Yinda CK, Vanhulle E, Conceição-Neto N, et al. Gut virome analysis of cameroonians reveals high diversity of enteric viruses, including potential interspecies transmitted viruses. mSphere. 2019;4:e00585-18. https://doi.org/10.1128/mSphere.00585-18.CrossRefPubMedPubMedCentral

Ly M, Abeles SR, Boehm TK, et al. Altered oral viral ecology in association with periodontal disease. mBio. 2014;5:1133. https://doi.org/10.1128/mbio.01133-14.CrossRef

Ungaro F, Massimino L, Furfaro F, et al. Metagenomic analysis of intestinal mucosa revealed a specific eukaryotic gut virome signature in early-diagnosed inflammatory bowel disease. Gut Microbes. 2019;10:149–158. https://doi.org/10.1080/19490976.2018.1511664.CrossRefPubMed

Fernandes MA, Verstraete SG, Phan TG, et al. Enteric virome and bacterial microbiota in children with ulcerative colitis and crohn disease. J Pediatr Gastroenterol Nutr. 2019;68:30–36. https://doi.org/10.1097/MPG.0000000000002140.CrossRefPubMedPubMedCentral

10.

Willner D, Furlan M, Haynes M, et al. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS ONE. 2009;4:e7370. https://doi.org/10.1371/journal.pone.0007370.CrossRefPubMedPubMedCentral

11.

Moran Losada P, Chouvarine P, Dorda M, et al. The cystic fibrosis lower airways microbial metagenome. ERJ Open Res. 2016;2:00096–02015. https://doi.org/10.1183/23120541.00096-2015.CrossRefPubMedPubMedCentral

12.

Santiago-Rodriguez TM, Hollister EB. Human virome and disease: high-throughput sequencing for virus discovery, identification of phage-bacteria dysbiosis and development of therapeutic approaches with emphasis on the human gut. Viruses. 2019;11:E656.PubMed

13.

Plummer M, de Martel C, Vignat J, et al. Global burden of cancers attributable to infections in 2012: a synthetic analysis. Lancet Glob Health. 2016;4:e609–e616.PubMed

14.

Mesri EA, Feitelson MA, Munger K. Human viral oncogenesis: a cancer hallmarks analysis. Cell Host Microbe. 2014;15:266–282.PubMedPubMedCentral

15.

Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–674.PubMed

16.

Monaco CL, Gootenberg DB, Zhao G, et al. Altered virome and bacterial microbiome in human immunodeficiency Virus-Associated Acquired Immunodeficiency Syndrome. Cell Host Microbe. 2016;19:311–322. https://doi.org/10.1016/j.chom.2016.02.011.CrossRefPubMedPubMedCentral

17.

Abeles SR, Ly M, Santiago-Rodriguez TM, et al. Effects of long term antibiotic therapy on human oral and fecal viromes. PLoS ONE. 2015;10:e0134941.PubMedPubMedCentral

18.

Santiago-Rodriguez TM, Ly M, Bonilla N, et al. The human urine virome in association with urinary tract infections. Front Microbiol. 2015;6:14.PubMedPubMedCentral

19.

Norman JM, Handley SA, Baldridge MT, et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell. 2015;160:447–460. https://doi.org/10.1016/j.cell.2015.01.002.CrossRefPubMedPubMedCentral

20.

Bzhalava D, Guan P, Franceschi S, et al. A systematic review of the prevalence of mucosal and cutaneous human papillomavirus types. Virology. 2013;445:224–231.PubMed

21.

Braaten KP, Laufer MR. Human papillomavirus (HPV), HPV-related disease, and the HPV vaccine. Rev Obstet Gynecol. 2008;1:2.PubMedPubMedCentral

22.

Kreimer AR, Clifford GM, Boyle P, et al. Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review. Cancer Epidemiol Biomark Prev. 2005;14:467–475.

23.

D’Souza G, Kreimer AR, Viscidi R, et al. Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med. 2007;356:1944–1956.PubMed

24.

Muñoz N, Bosch X, de Sanjosé S, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003;348:518–527.PubMed

25.

Yin B, Liu W, Yu P, et al. Association between human papillomavirus and prostate cancer: a meta-analysis. Oncol Lett. 2017;14:1855–1865. https://doi.org/10.3892/ol.2017.6367.CrossRefPubMedPubMedCentral

26.

Damin DC, Ziegelmann PK, Damin AP. Human papillomavirus infection and colorectal cancer risk: a meta-analysis. Colorectal Dis. 2013;15:e420–e428.PubMed

27.

Araldi RP, Sant’Ana TA, Módolo DG, et al. The human papillomavirus (HPV)-related cancer biology: an overview. Biomed Pharmacother. 2018;106:1537–1556.PubMed

28.

Lui RN, Tsoi KKF, Ho JMW, et al. Global increasing incidence of young-onset colorectal cancer across 5 continents: a joinpoint regression analysis of 1,922,167 cases. Cancer Epidemiol Biomark Prev. 2019;28:1275–1282.

29.

Doorbar J, Egawa N, Griffin H, et al. Human papillomavirus molecular biology and disease association. Rev Med Virol.. 2015;25:2–23.PubMedPubMedCentral

30.

Bodaghi S. Colorectal papillomavirus infection in patients with colorectal cancer. Clin Cancer Res. 2005;11:2862–2867.PubMedPubMedCentral

31.

De Gascun CF, Carr MJ. Human polyomavirus reactivation: disease pathogenesis and treatment approaches. Clin Dev Immunol. 2013;2013:373579.PubMedPubMedCentral

32.

Prado JCM, Monezi TA, Amorim AT, et al. Human polyomaviruses and cancer: an overview. Clinics (Sao Paulo). 2018;73:e558s. https://doi.org/10.6061/clinics/2018/e558s.CrossRefPubMedCentral

33.

Dalianis T, Hirsch HH. Human polyomaviruses in disease and cancer. Virology. 2013;437:63–72.PubMed

34.

Vilchez RA, Butel JS. Emergent human pathogen simian virus 40 and its role in cancer. Clin Microbiol Rev. 2004;17:495–508.PubMedPubMedCentral

35.

Khabaz MN, Nedjadi T, Gari MA, et al. Simian virus 40 is not likely involved in the development of colorectal adenocarcinoma. Future Virol. 2016;11:175–180.

36.

Rollison DE. JC virus infection. J Clin Gastroenterol. 2010;. https://doi.org/10.1097/mcg.0b013e3181e0084b.CrossRefPubMedPubMedCentral

37.

Khabaz MN, Nedjadi T, Garri MA, et al. BK polyomavirus association with colorectal cancer development. Genet Mol Res. 2016. https://doi.org/10.4238/gmr.15027841.CrossRefPubMed

38.

Cohen LJ. Phages trump bacteria in immune interactions. Sci Transl Med. 2019;11:eaaw5331.

39.

Hannigan GD, Duhaime MB, Ruffin MT 4th, et al. Diagnostic potential and interactive dynamics of the colorectal cancer virome. mBio. 2018;9:e02248-18.PubMedPubMedCentral

40.

Nakatsu G, Zhou H, Wu WKK, et al. Alterations in enteric virome are associated with colorectal cancer and survival outcomes. Gastroenterology. 2018;155:e5.

41.

Sobhani I, Tap J, Roudot-Thoraval F, et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS ONE. 2011;6:e16393. https://doi.org/10.1371/journal.pone.0016393.CrossRefPubMedPubMedCentral

42.

Tilg H, Adolph TE, Gerner RR, et al. The intestinal microbiota in colorectal cancer. Cancer Cell. 2018;33:954–964.PubMed

43.

Schieffer KM, Wright JR, Harris LR, et al. NOD2 genetic variants predispose one of two familial adenomatous polyposis siblings to pouchitis through microbiome dysbiosis. J Crohns Colitis. 2017;11:1393–1397. https://doi.org/10.1093/ecco-jcc/jjx083.CrossRefPubMedPubMedCentral

44.

Gogokhia L, Buhrke K, Bell R, et al. Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Cell Host Microbe. 2019;25:e8.

45.

Sze MA, Baxter NT, Ruffin MT 4th, et al. Normalization of the microbiota in patients after treatment for colonic lesions. Microbiome. 2017;5:150.PubMedPubMedCentral

46.

Baxter NT, Ruffin MT 4th, Rogers MAM, et al. Microbiota-based model improves the sensitivity of fecal immunochemical test for detecting colonic lesions. Genome Med. 2016;8:37.PubMedPubMedCentral

47.

Baxter NT, Koumpouras CC, Rogers MAM, et al. DNA from fecal immunochemical test can replace stool for detection of colonic lesions using a microbiota-based model. Microbiome. 2016;4:59.PubMedPubMedCentral

48.

Zackular JP, Rogers MAM, Ruffin MT 4th, et al. The human gut microbiome as a screening tool for colorectal cancer. Cancer Prev Res. 2014;7:1112–1121.

49.

Geuking MB, Weber J, Dewannieux M, et al. Recombination of retrotransposon and exogenous RNA virus results in nonretroviral cDNA integration. Science. 2009;323:393–396.PubMed

50.

Horie M, Honda T, Suzuki Y, et al. Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature. 2010;463:84–87.PubMedPubMedCentral

51.

Klenerman P, Hengartner H, Zinkernagel RM. A non-retroviral RNA virus persists in DNA form. Nature. 1997;390:298–301.PubMed

52.

Zhdanov VM. Integration of viral genomes. Nature. 1975;256:471–473.PubMed

53.

Enam S, del Valle L, Lara C, et al. Association of human polyomavirus JCV with colon cancer: evidence for interaction of viral T-antigen and beta-catenin. Cancer Res. 2002;62:7093–7101.PubMed

54.

Goel A, Li MS, Nagasaka T, et al. Association of JC virus T-antigen expression with the methylator phenotype in sporadic colorectal cancers. Gastroenterology. 2006;130:1950–1961.PubMed

55.

Hori R, Murai Y, Tsuneyama K, et al. Detection of JC virus DNA sequences in colorectal cancers in Japan. Virchows Arch. 2005;447:723–730.PubMed

56.

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. Tumour Biol.. 2011;32:653–659.PubMed

57.

Mou X, Chen L, Liu F, et al. Prevalence of JC virus in Chinese patients with colorectal cancer. PLoS ONE. 2012;7:e35900. https://doi.org/10.1371/journal.pone.0035900.CrossRefPubMedPubMedCentral

58.

Ouaïssi M, Studer AS, 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. 2014;34:349–353.PubMed

59.

Theodoropoulos G, Panoussopoulos D, Papaconstantinou I, et al. Assessment of JC polyoma virus in colon neoplasms. Dis Colon Rectum. 2005;48:86–91.PubMed

60.

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. 2012;57:79–84. https://doi.org/10.1007/s10620-011-1855-z.CrossRefPubMed

61.

zur Hausen H. Red meat consumption and cancer: reasons to suspect involvement of bovine infectious factors in colorectal cancer. Int J Cancer. 2012;130:2475–2483.PubMed

62.

Boleij A, Hechenbleikner EM, Goodwin AC, et al. The Bacteroides fragilis toxin gene is prevalent in the colon mucosa of colorectal cancer patients. Clin Infect Dis. 2015;60:208–215. https://doi.org/10.1093/cid/ciu787.CrossRefPubMed

63.

Castellarin M, Warren RL, Freeman JD, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22:299–306. https://doi.org/10.1101/gr.126516.111.CrossRefPubMedPubMedCentral

64.

Cuevas-Ramos G, Petit CR, Marcq I, et al. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA. 2010;107:11537–11542. https://doi.org/10.1073/pnas.1001261107.CrossRefPubMedPubMedCentral

65.

Niu YD, McAllister TA, Nash JHE, et al. Four Escherichia coli O157:H7 phages: a new bacteriophage genus and taxonomic classification of T1-like phages. PLoS ONE. 2014;9:e100426.PubMedPubMedCentral

66.

Dejea CM, Wick EC, Hechenbleikner EM, et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci USA. 2014;111:18321–18326. https://doi.org/10.1073/pnas.1406199111.CrossRefPubMedPubMedCentral

67.

Johnson CH, Dejea CM, Edler D, et al. Metabolism links bacterial biofilms and colon carcinogenesis. Cell Metab. 2015;21:891–897. https://doi.org/10.1016/j.cmet.2015.04.011.CrossRefPubMedPubMedCentral

68.

Secor PR, Sweere JM, Michaels LA, et al. Filamentous bacteriophage promote biofilm assembly and function. Cell Host Microbe. 2015;18:549–559. https://doi.org/10.1016/j.chom.2015.10.013.CrossRefPubMedPubMedCentral

69.

Waldor MK, Mekalanos JJ. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science. 1996;272:1910–1914.PubMed

70.

Nguyen S, Baker K, Padman BS, et al. Bacteriophage transcytosis provides a mechanism to cross epithelial cell layers. mBio. 2017;8:e01874-17.PubMedPubMedCentral

71.

Lehti TA, Pajunen MI, Skog MS, et al. Internalization of a polysialic acid-binding Escherichia coli bacteriophage into eukaryotic neuroblastoma cells. Nat Commun. 2017;8:1915.PubMedPubMedCentral

72.

Ogilvie LA, Jones BV. The human gut virome: a multifaceted majority. Front Microbiol. 2015;6:918.PubMedPubMedCentral

73.

Amann RI, Ludwig W, Schleifer KH. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev. 1995;59:143–169.PubMedPubMedCentral

74.

Rappé MS, Giovannoni SJ. The uncultured microbial majority. Annu Rev Microbiol. 2003;57:369–394.PubMed

75.

Edwards RA, Rohwer F. Viral metagenomics. Nat Rev Microbiol. 2005;3:504–510.PubMed

76.

García-Arroyo L, Prim N, Martí N, et al. Benefits and drawbacks of molecular techniques for diagnosis of viral respiratory infections. Experience with two multiplex PCR assays. J Med Virol. 2016;88:45–50.PubMed

77.

Reijans M, Dingemans G, Klaassen CH, et al. RespiFinder: a new multiparameter test to differentially identify fifteen respiratory viruses. J Clin Microbiol. 2008;46:1232–1240. https://doi.org/10.1128/JCM.02294-07.CrossRefPubMedPubMedCentral

78.

Afshar RM, Mollaie HR. Detection of HBV resistance to lamivudine in patients with chronic hepatitis B using Zip nucleic acid probes in Kerman, southeast of Iran. Asian Pac J Cancer Prev. 2012;13:3657–3661.PubMed

79.

Mercier-Delarue S, Vray M, Plantier JC, et al. Higher specificity of nucleic acid sequence-based amplification isothermal technology than of real-time PCR for quantification of HIV-1 RNA on dried blood spots. J Clin Microbiol. 2014;52:52–56. https://doi.org/10.1128/JCM.01848-13.CrossRefPubMedPubMedCentral

80.

Wu D, Liu F, Liu H, et al. Detection of serum HCV RNA in patients with chronic hepatitis C by transcription mediated amplification and real-time reverse transcription polymerase chain reaction. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2014;39:664–672.PubMed

81.

Wylie TN, Wylie KM, Herter BN, et al. Enhanced virome sequencing using targeted sequence capture. Genome Res. 2015;25:1910–1920.PubMedPubMedCentral

82.

Moustafa A, Xie C, Kirkness E, et al. The blood DNA virome in 8,000 humans. PLoS Pathog. 2017;13:e1006292. https://doi.org/10.1371/journal.ppat.1006292.CrossRefPubMedPubMedCentral

83.

Kleiner M, Hooper LV, Duerkop BA. Evaluation of methods to purify virus-like particles for metagenomic sequencing of intestinal viromes. BMC Genom. 2015;16:7.

84.

Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65.PubMedPubMedCentral

85.

Thurber RV, Haynes M, Breitbart M, et al. Laboratory procedures to generate viral metagenomes. Nat Protoc. 2009;4:470–483.PubMed

86.

Reyes A, Semenkovich NP, Whiteson K, et al. Going viral: next-generation sequencing applied to phage populations in the human gut. Nat Rev Microbiol. 2012;10:607–617.PubMedPubMedCentral

87.

Kim K-H, Chang H-W, Nam Y-D, et al. Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl Environ Microbiol. 2008;74:5975–5985.PubMedPubMedCentral

88.

Wang D, Urisman A, Liu YT, et al. Viral discovery and sequence recovery using DNA microarrays. PLoS Biol. 2003;1:E2. https://doi.org/10.1371/journal.pbio.0000002.CrossRefPubMedPubMedCentral

89.

Abbas AA, Diamond JM, Chehoud C, et al. The perioperative lung transplant virome: torque teno viruses are elevated in donor lungs and show divergent dynamics in primary graft dysfunction. Am J Transplant. 2017;17:1313–1324. https://doi.org/10.1111/ajt.14076.CrossRefPubMed

90.

Breitbart M, Hewson I, Felts B, et al. Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol. 2003;185:6220–6223. https://doi.org/10.1128/jb.185.20.6220-6223.2003.CrossRefPubMedPubMedCentral

91.

Reyes A, Haynes M, Hanson N, et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature. 2010;466:334–338. https://doi.org/10.1038/nature09199.CrossRefPubMedPubMedCentral

92.

Kim M-S, Park E-J, Roh SW, et al. Diversity and abundance of single-stranded DNA viruses in human feces. Appl Environ Microbiol. 2011;77:8062–8070.PubMedPubMedCentral

93.

Minot S, Sinha R, Chen J, et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 2011;21:1616–1625. https://doi.org/10.1101/gr.122705.111.CrossRefPubMedPubMedCentral

94.

Handley SA, Devkota S. Going viral: a novel role for bacteriophage in colorectal cancer. mBio. 2019;10:e02626-18.PubMedPubMedCentral

95.

Zheng T, Li J, Ni Y, et al. Mining, analyzing, and integrating viral signals from metagenomic data. Microbiome. 2019;7:42. https://doi.org/10.1186/s40168-019-0657-y.CrossRefPubMedPubMedCentral

96.

Mollerup S, Asplund M, Friis-Nielsen J, et al. High-throughput sequencing-based investigation of viruses in human cancers by multienrichment approach. J Infect Dis. 2019;220:1312–1324. https://doi.org/10.1093/infdis/jiz318.CrossRefPubMedPubMedCentral

97.

Vinner L, Mourier T, Friis-Nielsen J, et al. Investigation of human cancers for retrovirus by low-stringency target enrichment and high-throughput sequencing. Sci Rep. 2015;5:13201. https://doi.org/10.1038/srep13201.CrossRefPubMedPubMedCentral

98.

Mühlemann B, Jones TC, de Barros Damgaard P, et al. Ancient hepatitis B viruses from the Bronze Age to the Medieval period. Nature. 2018;557:418–423.PubMed

99.

Hansen TA, Fridholm H, Frøslev TG, et al. New type of papillomavirus and novel circular single stranded DNA virus discovered in urban Rattus norvegicus using circular DNA enrichment and metagenomics. PLoS ONE. 2015;10:e0141952. https://doi.org/10.1371/journal.pone.0141952.CrossRefPubMedPubMedCentral

100.

Nooij S, Schmitz D, Vennema H, et al. Overview of virus metagenomic classification methods and their biological applications. Front. Microbiol. 2018;9:749.PubMedPubMedCentral

101.

Posada-Cespedes S, Seifert D, Beerenwinkel N. Recent advances in inferring viral diversity from high-throughput sequencing data. Virus Res. 2017;239:17–32.PubMed

102.

Rose R, Constantinides B, Tapinos A, et al. Challenges in the analysis of viral metagenomes. Virus Evol. 2016;2:vew022.PubMedPubMedCentral

103.

Wommack KE, Bhavsar J, Polson SW, et al. VIROME: a standard operating procedure for analysis of viral metagenome sequences. Stand Genom Sci. 2012;6:427–439. https://doi.org/10.4056/sigs.2945050.CrossRef

104.

Roux S, Tournayre J, Mahul A, et al. Metavir 2: new tools for viral metagenome comparison and assembled virome analysis. BMC Bioinform. 2014;15:76.

105.

Scheuch M, Höper D, Beer M. RIEMS: a software pipeline for sensitive and comprehensive taxonomic classification of reads from metagenomics datasets. BMC Bioinform. 2015;16:69.

106.

Norling M, Karlsson-Lindsjö OE, Gourlé H, et al. MetLab: an in silico experimental design, simulation and analysis tool for viral metagenomics studies. PLoS ONE. 2016;11:e0160334.PubMedPubMedCentral

107.

Bhaduri A, Qu K, Lee CS, et al. Rapid identification of non-human sequences in high-throughput sequencing datasets. Bioinformatics. 2012;28:1174–1175.PubMedPubMedCentral

108.

Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 2014;15:R46.PubMedPubMedCentral

109.

Lefkowitz EJ, Dempsey DM, Hendrickson RC, et al. Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucl Acids Res. 2018;46:D708–D717. https://doi.org/10.1093/nar/gkx932.CrossRefPubMed

110.

Aiewsakun P, Adriaenssens EM, Lavigne R, et al. Evaluation of the genomic diversity of viruses infecting bacteria, archaea and eukaryotes using a common bioinformatic platform: steps towards a unified taxonomy. J Gen Virol. 2018;99:1331–1343.PubMedPubMedCentral

111.

Aiewsakun P, Simmonds P. The genomic underpinnings of eukaryotic virus taxonomy: creating a sequence-based framework for family-level virus classification. Microbiome. 2018;6:38.PubMedPubMedCentral

112.

Wommack KE, Bhavsar J, Ravel J. Metagenomics: read length matters. Appl Environ Microbiol. 2008;74:1453–1463.PubMedPubMedCentral

113.

Wooley JC, Ye Y. Metagenomics: facts and artifacts, and computational challenges*. J Comput Sci Technol. 2009;25:71–81.PubMedPubMedCentral

114.

Tang P, Chiu C. Metagenomics for the discovery of novel human viruses. Future Microbiol. 2010;5:177–189.PubMed

115.

Wooley JC, Godzik A, Friedberg I. A primer on metagenomics. PLoS Comput Biol. 2010;6:e1000667.PubMedPubMedCentral

116.

Fancello L, Raoult D, Desnues C. Computational tools for viral metagenomics and their application in clinical research. Virology. 2012;434:162–174.PubMed

117.

Thomas T, Gilbert J, Meyer F. Metagenomics—A guide from sampling to data analysis. Microb Inform Exp. 2012;2:3.PubMedPubMedCentral

118.

Pallen MJ. Diagnostic metagenomics: potential applications to bacterial, viral and parasitic infections. Parasitology. 2014;141:1856–1862.PubMed

119.

Hall RJ, Draper JL, Nielsen FGG, et al. Beyond research: a primer for considerations on using viral metagenomics in the field and clinic. Front Microbiol. 2015;6:224.PubMedPubMedCentral

120.

McIntyre ABR, Ounit R, Afshinnekoo E, et al. Comprehensive benchmarking and ensemble approaches for metagenomic classifiers. Genome Biol. 2017;18:182.PubMedPubMedCentral

121.

Nieuwenhuijse DF, Koopmans MPG. Metagenomic sequencing for surveillance of food- and waterborne viral diseases. Front Microbiol. 2017;8:230.PubMedPubMedCentral

122.

Randle-Boggis RJ, Helgason T, Sapp M, et al. Evaluating techniques for metagenome annotation using simulated sequence data. FEMS Microbiol Ecol. 2016;92:fiw095.PubMedPubMedCentral

123.

Lindgreen S, Adair KL, Gardner PP. An evaluation of the accuracy and speed of metagenome analysis tools. Sci Rep. 2016;6:19233.PubMedPubMedCentral

124.

Treangen TJ, Koren S, Sommer DD, et al. MetAMOS: a modular and open source metagenomic assembly and analysis pipeline. Genome Biol. 2013;14:R2.PubMedPubMedCentral

125.

Scholz M, Lo C-C, Chain PSG. Improved assemblies using a source-agnostic pipeline for MetaGenomic Assembly by Merging (MeGAMerge) of contigs. Sci Rep. 2015;4:6480.

126.

Smits SL, Bodewes R, Ruiz-Gonzalez A, et al. Assembly of viral genomes from metagenomes. Front Microbiol. 2014;5:714. https://doi.org/10.3389/fmicb.2014.00714.CrossRefPubMedPubMedCentral

127.

Vázquez-Castellanos JF, García-López R, Pérez-Brocal V, et al. Comparison of different assembly and annotation tools on analysis of simulated viral metagenomic communities in the gut. BMC Genom. 2014;15:37.

128.

Deng X, Naccache SN, Ng T, et al. An ensemble strategy that significantly improves de novo assembly of microbial genomes from metagenomic next-generation sequencing data. Nucleic Acids Res. 2015;43:e46. https://doi.org/10.1093/nar/gkv002.PubMedPubMedCentral

129.

Henry VJ, Bandrowski AE, Pepin A-S, Gonzalez BJ, Desfeux A. OMICtools: an informative directory for multi-omic data analysis. Database. 2014.

130.

Fredericks DN, Relman DA. Sequence-based identification of microbial pathogens: a reconsideration of Koch’s postulates. Clin Microbiol Rev. 1996;9:18–33.PubMedCentral

131.

Arias M, Fan H. The saga of XMRV: a virus that infects human cells but is not a human virus. Emerg Microbes Infect. 2014;3:1–6.

132.

Alter HJ, Mikovits JA, Switzer WM, et al. A multicenter blinded analysis indicates no association between chronic fatigue syndrome/myalgic encephalomyelitis and either xenotropic murine leukemia virus-related virus or polytropic murine leukemia virus. mBio. 2012;3:e00266-12. https://doi.org/10.1128/mbio.00266-12.CrossRefPubMedPubMedCentral

133.

Erlwein O, et al. DNA extraction columns contaminated with murine sequences. PLoS ONE. 2011;6:e23484.PubMedPubMedCentral

134.

Naccache SN, Greninger AL, Lee D, et al. The perils of pathogen discovery: origin of a novel parvovirus-like hybrid genome traced to nucleic acid extraction spin columns. J Virol. 2013;87:11966–11977. https://doi.org/10.1128/JVI.02323-13.CrossRefPubMedPubMedCentral

135.

Lewandowska DW, Zagordi O, Abinden A, et al. Unbiased metagenomic sequencing complements specific routine diagnostic methods and increases chances to detect rare viral strains. Diagn Microbiol Infect Dis. 2015;83:133–138.PubMedPubMedCentral

136.

Schlaberg R, Chiu CY, Miller S, et al. Validation of metagenomic next-generation sequencing tests for universal pathogen detection. Arch Pathol Lab Med. 2017;141:776–786.PubMed

137.

Kim M-S, Bae J-W. Spatial disturbances in altered mucosal and luminal gut viromes of diet-induced obese mice. Environ Microbiol. 2016;18:1498–1510.PubMed

138.

Minot S, Bryson A, Chehoud C, et al. Rapid evolution of the human gut virome. Proc Natl Acad Sci USA. 2013;110:12450–12455. https://doi.org/10.1073/pnas.1300833110.CrossRefPubMedPubMedCentral

139.

Nagata N, Tohya M, Fukuda S, et al. Effects of bowel preparation on the human gut microbiome and metabolome. Sci Rep. 2019;9:4042. https://doi.org/10.1038/s41598-019-40182-9.CrossRefPubMedPubMedCentral

Title: Enteric Virome and Carcinogenesis in the Gut
Authors: Cade Emlet
Mack Ruffin
Regina Lamendella
Publication date: 01-03-2020
Publisher: Springer US
Keywords: Human Papillomavirus
Colorectal Cancer
Colorectal Cancer
Biomarkers
Published in: Digestive Diseases and Sciences / Issue 3/2020
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI: https://doi.org/10.1007/s10620-020-06126-4

ACC 2024 Congress Coverage

Heart Failure Video

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Enteric Virome and Carcinogenesis in the Gut

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2020

Gut Microbiome Modulates Response to Cancer Immunotherapy

Gut Microbiome and Immune Checkpoint Inhibitor-Induced Enterocolitis

Necrotizing Enterocolitis: A Multi-omic Approach and the Role of the Microbiome

Abnormal Intestinal Microbiome in Medical Disorders and Potential Reversibility by Fecal Microbiota Transplantation

Microbiome Composition in Pediatric Populations from Birth to Adolescence: Impact of Diet and Prebiotic and Probiotic Interventions

Microbiome and Its Role in Irritable Bowel Syndrome

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page