Bacteriophages in the human gut: Our fellow travelers throughout life and potential biomarkers of heath or disease

Allen, 2011, Antibiotics in feed induce prophages in swine fecal microbiomes, MBio, 2, e00211, 10.1128/mBio.00260-11 Andoh, 2011, Comparison of the fecal microbiota profiles between ulcerative colitis and Crohn’s disease using terminal restriction fragment length polymorphism analysis, J. Gastroenterol., 46, 479, 10.1007/s00535-010-0368-4 Angly, 2005, PHACCS, an online tool for estimating the structure and diversity of uncultured viral communities using metagenomic information, BMC Bioinf., 6, 41, 10.1186/1471-2105-6-41 Barr, 2013, Innate and acquired bacteriophage-mediated immunity, Bacteriophage, 3, 10771, 10.4161/bact.25857 Bedi, 2011, Delivery of siRNA into breast cancer cells via phage fusion protein-targeted liposomes, Nanomed. Nanotechnol. Biol. Med., 7, 315, 10.1016/j.nano.2010.10.004 Bedi, 2013, Targeted delivery of siRNA into breast cancer cells via phage fusion proteins, Mol. Pharm., 10, 551, 10.1021/mp3006006 Bondy-Denomy, 2013, Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system, Nature, 493, 429, 10.1038/nature11723 Breitbart, 2008, Viral diversity and dynamics in an infant gut, Res. Microbiol., 159, 367, 10.1016/j.resmic.2008.04.006 Broaders, 2013, Mobile genetic elements of the human gastrointestinal tract: potential for spread of antibiotic resistance genes, Gut Microbes, 4, 271, 10.4161/gmic.24627 Cadwell, 2015, Expanding the role of the virome: commensalism in the gut, J. Virol., 89, 1951, 10.1128/JVI.02966-14 Cao, 2016, Phage as a genetically modifiable supramacromolecule in chemistry, materials and medicine, Acc. Chem. Res., 49, 1111, 10.1021/acs.accounts.5b00557 Carlton, 1999, Phage therapy: past history and future prospects, Archivum Immunologiae Et Therapiae Experimentalis-English Edition, 47, 267 Chibani-Chennoufi, 2004, Phage-host interaction: an ecological perspective, J. Bacteriol., 186, 3677, 10.1128/JB.186.12.3677-3686.2004 Cho, 2017, Development of a novel imaging agent using peptide-coated gold nanoparticles toward brain glioma stem cell marker CD133, Acta Biomater., 47, 182, 10.1016/j.actbio.2016.10.009 Columpsi, 2016, Beyond the gut bacterial microbiota: the gut virome, J. Med. Virol., 88, 1467, 10.1002/jmv.24508 Cui, 2013, Phage-displayed specific polypeptide antigens induce significant protective immunity against Trichinella spiralis infection in BALB/c mice, Vaccine, 31, 1171, 10.1016/j.vaccine.2012.12.070 Dalmasso, 2014, Exploiting gut bacteriophages for human health, Trends Microbiol., 22, 399, 10.1016/j.tim.2014.02.010 Duerkop, 2013, Resident viruses and their interactions with the immune system, Nat. Immunol., 14, 654, 10.1038/ni.2614 Frenkel, 2003, Reduction of β-amyloid plaques in brain of transgenic mouse model of Alzheimer’s disease by EFRH-phage immunization, Vaccine, 21, 1060, 10.1016/S0264-410X(02)00609-6 Furuse, 1983, Bacteriophage distribution in human faeces: continuous survey of healthy subjects and patients with internal and leukaemic diseases, J. Gen. Virol., 64, 2039, 10.1099/0022-1317-64-9-2039 Gandra, 2013, Bacteriophage bionanowire as a carrier for both cancer-targeting peptides and photosensitizers and its use in selective cancer cell killing by photodynamic therapy, Small, 9, 215, 10.1002/smll.201202090 Giang, 2012, Human broadly neutralizing antibodies to the envelope glycoprotein complex of hepatitis C virus, Proc. Natl. Acad. Sci., 109, 6205, 10.1073/pnas.1114927109 Gupta, 2016, Fecal microbiota transplantation: in perspective, Therapeut. Adv. Gastroenterol., 9, 229, 10.1177/1756283X15607414 Hsiung, 2008, Detection of colonic dysplasia in vivo using a targeted heptapeptide and confocal microendoscopy, Nat. Med., 14, 454, 10.1038/nm1692 Huddleston, 2014, Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes, Infect. Drug Resist., 7, 167, 10.2147/IDR.S48820 Huddleston, 2014, Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes, Infect. Drug Resist., 7, 167, 10.2147/IDR.S48820 Janardhanan, 2010, Architectonics of phage-liposome nanowebs as optimized photosensitizer vehicles for photodynamic cancer therapy, Mol. Cancer Ther., 9, 2524, 10.1158/1535-7163.MCT-10-0253 Keen, 2015, A century of phage research: bacteriophages and the shaping of modern biology, Bioessays, 37, 6, 10.1002/bies.201400152 Kelly, 2006, In vivo imaging of molecularly targeted phage, Neoplasia, 8, 1011, 10.1593/neo.06610 Larimer, 2014, Development of a peptide by phage display for SPECT imaging of resistance-susceptible breast cancer, Am. J. Nucl. Med. Mol. Imaging, 4, 435 Leib-Mösch, 1990, Endogenous retroviral elements in human DNA, Cancer Res., 50, 5636s Lepage, 2008, Dysbiosis in inflammatory bowel disease: a role for bacteriophages?, Gut, 57, 424, 10.1136/gut.2007.134668 Licznerska, 2015, Oxidative stress in Shiga toxin production by enterohemorrhagic Escherichia coli, Oxid. Med. Cell. Longevity, 2016 Liu, 2006, Protein repertoire of double-stranded DNA bacteriophages, Virus Res., 117, 68, 10.1016/j.virusres.2006.01.015 Lysholm, 2012, Characterization of the viral microbiome in patients with severe lower respiratory tract infections, using metagenomic sequencing, PLoS One, 7, e30875, 10.1371/journal.pone.0030875 Malito, 2013, Defining a protective epitope on factor H binding protein, a key meningococcal virulence factor and vaccine antigen, Proc. Natl. Acad. Sci., 110, 3304, 10.1073/pnas.1222845110 Manrique, 2016, Healthy human gut phageome, Proc. Natl. Acad. Sci., 201601060 Manrique, 2017, The human gut phage community and its implications for health and disease, Viruses, 9, 141, 10.3390/v9060141 Melzer, 2002, Antigenicity and immunogenicity of phage library-selected peptide mimics of the major surface proteophosphoglycan antigens of Entamoeba histolytica, Parasite Immunol., 24, 321, 10.1046/j.1365-3024.2002.00463.x Mills, 2013, Movers and shakers: influence of bacteriophages in shaping the mammalian gut microbiota, Gut Microbes, 4, 4, 10.4161/gmic.22371 Min, 2013, Implementation of P22 viral capsids as intravascular magnetic resonance T 1 contrast conjugates via site-selective attachment of Gd (III)-chelating agents, Biomacromolecules, 14, 2332, 10.1021/bm400461j Minot, 2011, The human gut virome: inter-individual variation and dynamic response to diet, Genome Res., 21, 1616, 10.1101/gr.122705.111 Minot, 2012, Hypervariable loci in the human gut virome, Proc. Natl. Acad. Sci., 109, 3962, 10.1073/pnas.1119061109 Modi, 2013, Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome, Nature, 499, 219, 10.1038/nature12212 Moelling, 2016, Fecal microbiota transplantation to fight Clostridium difficile infections and other intestinal diseases, Bacteriophage, 6, e1251380, 10.1080/21597081.2016.1251380 Mokili, 2012, Metagenomics and future perspectives in virus discovery, Curr. Opin. Virol., 2, 63, 10.1016/j.coviro.2011.12.004 Moran, 2005, The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes, Proc. Natl. Acad. Sci. U. S. A., 102, 16919, 10.1073/pnas.0507029102 Ogilvie, 2014, The human gut virome: a multifaceted majority, Front. Microbiol., 6, 918 Oliver, 2009, Bacteriophages encode factors required for protection in a symbiotic mutualism, Science, 325, 992, 10.1126/science.1174463 Ott, 2017, Efficacy of sterile fecal filtrate transfer for treating patients with Clostridium difficile infection, Gastroenterology, 152, 799, 10.1053/j.gastro.2016.11.010 Pérez-Brocal, 2013, Study of the viral and microbial communities associated with Crohn’s disease: a metagenomic approach, Clin. Trans. Gastroenterol., 4, e36, 10.1038/ctg.2013.9 Palmer, 2007, Development of the human infant intestinal microbiota, PLoS Biol., 5, e177, 10.1371/journal.pbio.0050177 Paterson, 2010, Antagonistic coevolution accelerates molecular evolution, Nature, 464, 275, 10.1038/nature08798 Popgeorgiev, 2013, Describing the silent human virome with an emphasis on giant viruses, Intervirology, 56, 395, 10.1159/000354561 Reyes, 2010, Viruses in the faecal microbiota of monozygotic twins and their mothers, Nature, 466, 334, 10.1038/nature09199 Reyes, 2012, Going viral: next-generation sequencing applied to phage populations in the human gut, Nat. Rev. Microbiol., 10, 607, 10.1038/nrmicro2853 Rodriguez-Valera, 2009, Explaining microbial population genomics through phage predation, Nat. Rev. Microbiol., 7, 828, 10.1038/nrmicro2235 Ruthruff, 2007, Clinical review of Crohn’s disease, J. Am. Ass. Nurse Pract., 19, 392, 10.1111/j.1745-7599.2007.00242.x Salmond, 2015, A century of the phage: past, present and future, Nat. Rev. Microbiol., 13, 777, 10.1038/nrmicro3564 Samson, 2013, Revenge of the phages: defeating bacterial defences, Nat. Rev. Microbiol., 11, 675, 10.1038/nrmicro3096 Sanger, 1977 Sharon, 2013, Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization, Genome Res., 23, 111, 10.1101/gr.142315.112 Shterzer, 2015, The animal gut as a melting pot for horizontal gene transfer 1, Can. J. Microbiol., 61, 603, 10.1139/cjm-2015-0049 Smith, 1985, Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface, Science, 228, 1315, 10.1126/science.4001944 Solomon, 2008, Filamentous bacteriophage as a novel therapeutic tool for Alzheimer's disease treatment, J. Alzheimer's Dis., 15, 193, 10.3233/JAD-2008-15205 Souza, 2006, Networks of gold nanoparticles and bacteriophage as biological sensors and cell-targeting agents, Proc. Natl. Acad. Sci., 103, 1215, 10.1073/pnas.0509739103 Stern, 2011, The phage-host arms race: shaping the evolution of microbes, Bioessays, 33, 43, 10.1002/bies.201000071 Stern, 2012, CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome, Genome Res., 22, 1985, 10.1101/gr.138297.112 Sunderland, 2016 Suthiwangcharoen, 2011, M13 bacteriophage-polymer nanoassemblies as drug delivery vehicles, Nano Res., 4, 483, 10.1007/s12274-011-0104-2 Thingstad, 2000, Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems, Limnol. Oceanogr., 45, 1320, 10.4319/lo.2000.45.6.1320 Twort, 1915, An investigation on the nature of ultra-microscopic viruses, Lancet, 186, 1241, 10.1016/S0140-6736(01)20383-3 Ursell, 2012, Defining the human microbiome, Nutr. Rev., 70, S38, 10.1111/j.1753-4887.2012.00493.x Vinay, 2015, Phage-based fluorescent biosensor prototypes to specifically detect enteric bacteria such as E. coli and Salmonella enterica typhimurium, PLoS One, 10, e0131466, 10.1371/journal.pone.0131466 Virgin, 2009, Redefining chronic viral infection, Cell, 138, 30, 10.1016/j.cell.2009.06.036 Virgin, 2014, The virome in mammalian physiology and disease, Cell, 157, 142, 10.1016/j.cell.2014.02.032 Wagner, 2013, Bacteriophages in gut samples from pediatric Crohn’s disease patients: metagenomic analysis using 454 pyrosequencing, Inflamm. Bowel Dis., 19, 1598, 10.1097/MIB.0b013e318292477c Wang, 2010, Cryptic prophages help bacteria cope with adverse environments, Nat. Commun., 1, 147, 10.1038/ncomms1146 Wang, 2014, Untangling the effects of peptide sequences and nanotopographies in a biomimetic niche for directed differentiation of iPSCs by assemblies of genetically engineered viral nanofibers, Nano Lett., 14, 6850, 10.1021/nl504358j Wang, 2014, Phage nanofibers induce vascularized osteogenesis in 3D printed bone scaffolds, Adv. Mater., 26, 4961, 10.1002/adma.201400154 Wang, 2015, Ultrasensitive rapid detection of human serum antibody biomarkers by biomarker-capturing viral nanofibers, ACS Nano, 9, 4475, 10.1021/acsnano.5b01074 Winter, 2010, Trade-offs between competition and defense specialists among unicellular planktonic organisms: the killing the winner hypothesis revisited, Microbiol. Mol. Biol. Rev., 74, 42, 10.1128/MMBR.00034-09 Yacoby, 2006, Targeting antibacterial agents by using drug-carrying filamentous bacteriophages, Antimicrob. Agents Chemother., 50, 2087, 10.1128/AAC.00169-06 Yeh, 2016, Peptide-conjugated nanoparticles for targeted imaging and therapy of prostate cancer, Biomaterials, 99, 1, 10.1016/j.biomaterials.2016.05.015 Zhou, 2015, Phage-mediated counting by the naked eye of miRNA molecules at attomolar concentrations in a Petri dish, Nat. Mater., 14, 1058, 10.1038/nmat4377 d’Herelle, 1917, Sur un microbe invisible antagoniste des bacilles dysent’riques, CR Acad. Sci. Paris, 165, 373