Bacteriophage and the Innate Immune System: Access and Signaling

Microorganisms - Tập 7 Số 12 - Trang 625
Amanda Carroll‐Portillo1, Henry C. Lin1,2
1Division of Gastroenterology and Hepatology, University of New Mexico, Albuquerque, NM 87131, USA
2Medicine Service, New Mexico VA Health Care System, Albuquerque, NM 87108, USA

Tóm tắt

Bacteriophage and the bacteria they infect are the dominant members of the gastrointestinal microbiome. While bacteria are known to be central to maintenance of the structure, function, and health of the microbiome, it has only recently been recognized that phage too might serve a critical function. Along these lines, bacteria are not the only cells that are influenced by bacteriophage, and there is growing evidence of bacteriophage effects on epithelial, endothelial, and immune cells. The innate immune system is essential to protecting the Eukaryotic host from invading microorganisms, and bacteriophage have been demonstrated to interact with innate immune cells regularly. Here, we conduct a systematic review of the varying mechanisms allowing bacteriophage to access and interact with cells of the innate immune system and propose the potential importance of these interactions.

Từ khóa


Tài liệu tham khảo

Andrew, M.Q., King, M.J.A., Eric, B.C., and Elliot, J.L. (2011). Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier.

Breitbart, 2005, Here a virus, there a virus, everywhere the same virus?, Trends Microbiol., 13, 278, 10.1016/j.tim.2005.04.003

Manrique, 2016, Healthy human gut phageome, Proc. Natl. Acad. Sci. USA, 113, 10400, 10.1073/pnas.1601060113

Salmond, 2015, A century of the phage: Past, present and future, Nat. Rev. Microbiol., 13, 777, 10.1038/nrmicro3564

Rabinovich, 2012, Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence, Cell, 150, 792, 10.1016/j.cell.2012.06.036

Knowles, 2016, Lytic to temperate switching of viral communities, Nature, 531, 466, 10.1038/nature17193

Lee, 2018, The Developmental Switch in Bacteriophage lambda: A Critical Role of the Cro Protein, J. Mol. Biol., 430, 58, 10.1016/j.jmb.2017.11.005

Nanda, 2015, Impact of spontaneous prophage induction on the fitness of bacterial populations and host-microbe interactions, J. Bacteriol., 197, 410, 10.1128/JB.02230-14

Abeles, S.R., Ly, M., Santiago-Rodriguez, T.M., and Pride, D.T. (2015). Effects of Long Term Antibiotic Therapy on Human Oral and Fecal Viromes. PLoS ONE, 10.

Brussow, 2004, Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion, Microbiol. Mol. Biol. Rev., 68, 560, 10.1128/MMBR.68.3.560-602.2004

Enault, 2017, Phages rarely encode antibiotic resistance genes: A cautionary tale for virome analyses, ISME J., 11, 237, 10.1038/ismej.2016.90

Fortier, 2013, Importance of prophages to evolution and virulence of bacterial pathogens, Virulence, 4, 354, 10.4161/viru.24498

Lopez, 2012, Phage-mediated acquisition of a type III secreted effector protein boosts growth of salmonella by nitrate respiration, MBio, 3, e00143-12, 10.1128/mBio.00143-12

Modi, 2013, Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome, Nature, 499, 219, 10.1038/nature12212

Wommack, 2000, Virioplankton: Viruses in aquatic ecosystems, Microbiol. Mol. Biol. Rev., 64, 69, 10.1128/MMBR.64.1.69-114.2000

Bergh, 1989, High abundance of viruses found in aquatic environments, Nature, 340, 467, 10.1038/340467a0

Paul, 2008, Prophages in marine bacteria: Dangerous molecular time bombs or the key to survival in the seas?, ISME J., 2, 579, 10.1038/ismej.2008.35

Minot, 2011, The human gut virome: Inter-individual variation and dynamic response to diet, Genome Res., 21, 1616, 10.1101/gr.122705.111

Reyes, 2010, Viruses in the faecal microbiota of monozygotic twins and their mothers, Nature, 466, 334, 10.1038/nature09199

Keen, 2018, Close Encounters of Three Kinds: Bacteriophages, commensal Bacteria, and Host Immunity, Trends Microbiol., 26, 943, 10.1016/j.tim.2018.05.009

Kim, 2018, Lysogeny is prevalent and widely distributed in the murine gut microbiota, ISME J., 12, 1127, 10.1038/s41396-018-0061-9

Mills, 2013, Movers and shakers: Influence of bacteriophages in shaping the mammalian gut microbiota, Gut Microbes, 4, 4, 10.4161/gmic.22371

Van Belleghem, J.D., Dąbrowska, K., Vaneechoutte, M., Barr, J.J., and Bollyky, P.L. (2018). Interactions between Bacteriophage, Bacteria, and the Mammalian Immune System. Viruses, 11.

Barr, 2013, Bacteriophage adhering to mucus provide a non-host-derived immunity, Proc. Natl. Acad. Sci. USA, 110, 10771, 10.1073/pnas.1305923110

Gorski, 2006, Bacteriophage translocation, FEMS Immunol. Med. Microbiol., 46, 313, 10.1111/j.1574-695X.2006.00044.x

Moustafa, A., Xie, C., Kirkness, E., Biggs, W., Wong, E., Turpaz, Y., Bloom, K., Delwart, E., Nelson, K.E., and Venter, J.C. (2017). The blood DNA virome in 8000 humans. PLoS Pathog., 13.

Holers, 2014, Complement and its receptors: New insights into human disease, Annu. Rev. Immunol., 32, 433, 10.1146/annurev-immunol-032713-120154

Blasius, 2010, Intracellular toll-like receptors, Immunity, 32, 305, 10.1016/j.immuni.2010.03.012

Kawai, 2011, Toll-like receptors and their crosstalk with other innate receptors in infection and immunity, Immunity, 34, 637, 10.1016/j.immuni.2011.05.006

Chen, 2016, Regulation and function of the cGAS-STING pathway of cytosolic DNA sensing, Nat. Immunol., 17, 1142, 10.1038/ni.3558

Ori, 2017, Cytosolic nucleic acid sensors and innate immune regulation, Int. Rev. Immunol., 36, 74, 10.1080/08830185.2017.1298749

Xiao, 2015, The nucleic acid-sensing inflammasomes, Immunol. Rev., 265, 103, 10.1111/imr.12281

Kieser, 2017, Multi-receptor detection of individual bacterial products by the innate immune system, Nat. Rev. Immunol., 17, 376, 10.1038/nri.2017.25

Thaiss, 2016, The microbiome and innate immunity, Nature, 535, 65, 10.1038/nature18847

Bieghs, 2014, Innate immune signaling and gut-liver interactions in non-alcoholic fatty liver disease, Hepatobiliary Surg. Nutr., 3, 377

Gordon, 2002, Pattern recognition receptors: Doubling up for the innate immune response, Cell, 111, 927, 10.1016/S0092-8674(02)01201-1

Opitz, 2007, Extra- and intracellular innate immune recognition in endothelial cells, Thromb. Haemost., 98, 319, 10.1160/TH06-12-0694

Letkiewicz, 2017, Antiphage activity of sera during phage therapy in relation to its outcome, Future Microbiol., 12, 109, 10.2217/fmb-2016-0156

Dabrowska, 2014, Immunogenicity studies of proteins forming the T4 phage head surface, J. Virol., 88, 12551, 10.1128/JVI.02043-14

Dabrowska, 2005, Bacteriophage penetration in vertebrates, J. Appl. Microbiol., 98, 7, 10.1111/j.1365-2672.2004.02422.x

Jerne, 1956, The presence in normal serum of specific antibody against bacteriophage T4 and its increase during the earliest stages of immunization, J. Immunol., 76, 209, 10.4049/jimmunol.76.3.209

Tuma, 2003, Transcytosis: Crossing cellular barriers, Physiol. Rev., 83, 871, 10.1152/physrev.00001.2003

Aronow, 1964, Electron Microscopy of in Vitro Endocytosis of T2 Phage by Cells from Rabbit Peritoneal Exudate, J. Exp. Med., 120, 943, 10.1084/jem.120.5.943

Barr, 2017, A bacteriophages journey through the human body, Immunol. Rev., 279, 106, 10.1111/imr.12565

Duerkop, 2013, Resident viruses and their interactions with the immune system, Nat. Immunol., 14, 654, 10.1038/ni.2614

Tian, 2015, Probing the endocytic pathways of the filamentous bacteriophage in live cells using ratiometric pH fluorescent indicator, Adv. Healthc. Mater., 4, 413, 10.1002/adhm.201400508

Hsia, 2000, Phage infection of the obligate intracellular bacterium, Chlamydia psittaci strain guinea pig inclusion conjunctivitis, Microbes Infect., 2, 761, 10.1016/S1286-4579(00)90356-3

2015, Vascular permeability—The essentials, Upsala J. Med. Sci., 120, 135, 10.3109/03009734.2015.1064501

Huh, 2019, Bacteriophage interactions with mammalian tissue: Therapeutic applications, Adv. Drug Deliv. Rev, 145, 4, 10.1016/j.addr.2019.01.003

Nguyen, 2017, Bacteriophage Transcytosis Provides a Mechanism To Cross Epithelial Cell Layers, MBio, 8, e01874-17, 10.1128/mBio.01874-17

Ivanenkov, 1999, Uptake and intracellular fate of phage display vectors in mammalian cells, Biochim. Biophys. Acta, 1448, 450, 10.1016/S0167-4889(98)00162-1

Shan, 2018, Bacteriophages are more virulent to bacteria with human cells than they are in bacterial culture; insights from HT-29 cells, Sci. Rep., 8, 5091, 10.1038/s41598-018-23418-y

Kucharzik, 2000, Role of M cells in intestinal barrier function, Annu. N. Y. Acad. Sci., 915, 171, 10.1111/j.1749-6632.2000.tb05240.x

Petris, 2007, Bacterial transcytosis across conjunctival M cells, Investig. Ophthalmol. Vis. Sci., 48, 2172, 10.1167/iovs.06-1202

Bille, E., Meyer, J., Jamet, A., Euphrasie, D., Barnier, J.P., Brissac, T., Larsen, A., Pelissier, P., and Nassif, X. (2017). A virulence-associated filamentous bacteriophage of Neisseria meningitidis increases host-cell colonisation. PLoS Pathog., 13.

Boyd, 2012, Bacteriophage-encoded bacterial virulence factors and phage-pathogenicity island interactions, Adv. Virus Res., 82, 91, 10.1016/B978-0-12-394621-8.00014-5

Wagner, 2002, Bacteriophage control of bacterial virulence, Infect. Immun., 70, 3985, 10.1128/IAI.70.8.3985-3993.2002

Farache, 2013, Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation, Immunity, 38, 581, 10.1016/j.immuni.2013.01.009

Lelouard, 2012, Peyer’s patch dendritic cells sample antigens by extending dendrites through M cell-specific transcellular pores, Gastroenterology, 142, 592, 10.1053/j.gastro.2011.11.039

Barfoot, 1989, Some properties of dendritic macrophages from peripheral lymph, Immunology, 68, 233

Roxas, 2018, Modulation of Intestinal Paracellular Transport by Bacterial Pathogens, Compr. Physiol., 8, 823, 10.1002/cphy.c170034

Tetz, 2016, Bacteriophage infections of microbiota can lead to leaky gut in an experimental rodent model, Gut Pathog., 8, 33, 10.1186/s13099-016-0109-1

Przerwa, 2006, Effects of bacteriophages on free radical production and phagocytic functions, Med. Microbiol. Immunol., 195, 143, 10.1007/s00430-006-0011-4

Miernikiewicz, 2016, T4 Phage Tail Adhesin Gp12 Counteracts LPS-Induced Inflammation In vivo, Front. Microbiol., 7, 1112, 10.3389/fmicb.2016.01112

Xiong, 2014, Titer dynamic analysis of D29 within MTB-infected macrophages and effect on immune function of macrophages, Exp. Lung Res., 40, 86, 10.3109/01902148.2013.873841

Gorski, 2003, New insights into the possible role of bacteriophages in host defense and disease, Med. Immunol., 2, 2, 10.1186/1476-9433-2-2

Wenger, 1978, The cytogenetic, proliferative and viability effects of four bacteriophages on human lymphocytes, In Vitro, 14, 543, 10.1007/BF02616097

Nykvist, 2001, The cell adhesion domain of type XVII collagen promotes integrin-mediated cell spreading by a novel mechanism, J. Biol. Chem., 276, 38673, 10.1074/jbc.M102589200

Prasad, 2003, Soluble CD40 ligand induces beta3 integrin tyrosine phosphorylation and triggers platelet activation by outside-in signaling, Proc. Natl. Acad. Sci. USA, 100, 12367, 10.1073/pnas.2032886100

Fraser, 2006, Ig-like domains on bacteriophages: A tale of promiscuity and deceit, J. Mol. Biol., 359, 496, 10.1016/j.jmb.2006.03.043

Sathaliyawala, 2010, Functional analysis of the highly antigenic outer capsid protein, Hoc, a virus decoration protein from T4-like bacteriophages, Mol. Microbiol., 77, 444, 10.1111/j.1365-2958.2010.07219.x

Bork, 1994, The immunoglobulin fold. Structural classification, sequence patterns and common core, J. Mol. Biol., 242, 309

Halaby, 1998, The immunoglobulin superfamily: An insight on its tissular, species, and functional diversity, J. Mol. Evol., 46, 389, 10.1007/PL00006318

Miernikiewicz, 2015, Mammalian Host-Versus-Phage immune response determines phage fate in vivo, Sci. Rep., 5, 14802, 10.1038/srep14802

Kazmierczak, 2014, Molecular imaging of T4 phage in mammalian tissues and cells, Bacteriophage, 4, e28364, 10.4161/bact.28364

Akira, 2006, Pathogen recognition and innate immunity, Cell, 124, 783, 10.1016/j.cell.2006.02.015

Kawai, 2009, The roles of TLRs, RLRs and NLRs in pathogen recognition, Int. Immunol., 21, 317, 10.1093/intimm/dxp017

Noppert, 2007, The role of type I interferons in TLR responses, Immunol. Cell Biol., 85, 446, 10.1038/sj.icb.7100099

Gogokhia, 2019, Expansion of Bacteriophages Is Linked to Aggravated Intestinal Inflammation and Colitis, Cell Host Microbe, 25, 285, 10.1016/j.chom.2019.01.008

Sweere, 2019, Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection, Science, 363, eaat9691, 10.1126/science.aat9691

Pjanova, 2019, Comparison of the effects of bacteriophage-derived dsRNA and poly(I:C) on ex vivo cultivated peripheral blood mononuclear cells, Immunol. Lett., 212, 114, 10.1016/j.imlet.2019.06.010

Diner, 2013, The innate immune DNA sensor cGAS produces a noncanonical cyclic dinucleotide that activates human STING, Cell Rep., 3, 1355, 10.1016/j.celrep.2013.05.009

McCartney, 2009, Viral sensors: Diversity in pathogen recognition, Immunol. Rev., 227, 87, 10.1111/j.1600-065X.2008.00726.x

Cohen, 2019, Cyclic GMP-AMP signalling protects bacteria against viral infection, Nature, 574, 691, 10.1038/s41586-019-1605-5

Jensen, 2012, Sensing of RNA viruses: A review of innate immune receptors involved in recognizing RNA virus invasion, J. Virol., 86, 2900, 10.1128/JVI.05738-11

Rosenwald, 2014, Evidence for horizontal gene transfer between Chlamydophila pneumoniae and Chlamydia phage, Bacteriophage, 4, e965076, 10.4161/21597073.2014.965076

Metcalf, 2014, Antibacterial gene transfer across the tree of life, Elife, 3, e04266, 10.7554/eLife.04266

Moran, 2012, Recurrent horizontal transfer of bacterial toxin genes to eukaryotes, Mol. Biol. Evol., 29, 2223, 10.1093/molbev/mss089

Bordenstein, 2016, Eukaryotic association module in phage WO genomes from Wolbachia, Nat. Commun., 7, 13155, 10.1038/ncomms13155

Chatterjee, 2018, Beyond Bacteria: Bacteriophage-Eukaryotic Host Interactions Reveal Emerging Paradigms of Health and Disease, Front. Microbiol., 9, 1394, 10.3389/fmicb.2018.01394

Gorski, 2019, Phage-specific diverse effects of bacterial viruses on the immune system, Future Microbiol., 14, 1171, 10.2217/fmb-2019-0222

Ross, 2016, More Is Better: Selecting for Broad Host Range Bacteriophages, Front. Microbiol., 7, 1352, 10.3389/fmicb.2016.01352

Sergueev, K.V., Filippov, A.A., Farlow, J., Su, W., Kvachadze, L., Balarjishvili, N., Kutateladze, M., and Nikolich, M.P. (2019). Correlation of Host Range Expansion of Therapeutic Bacteriophage Sb-1 with Allele State at a Hypervariable Repeat Locus. Appl. Environ. Microbiol., 85.

Burrowes, B.H., Molineux, I.J., and Fralick, J.A. (2019). Directed in Vitro Evolution of Therapeutic Bacteriophages: The Appelmans Protocol. Viruses, 11.

Nobrega, 2019, Molecular and Evolutionary Determinants of Bacteriophage Host Range, Trends Microbiol., 27, 51, 10.1016/j.tim.2018.08.006