An enteric virus can replace the beneficial function of commensal bacteria

Nature

Volumn 516, Issue 729, 2014, Pages 94-98

  Kernbauer, Elisabeth ^a   Ding, Yi ^a,b   Cadwell, Ken ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK PRESBYTERIAN HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; INTERLEUKIN 13; INTERLEUKIN 22; TRANSCRIPTION FACTOR GATA 3; ANTIINFECTIVE AGENT; INTERFERON;

BACTERIAL DISEASE; BACTERIUM; COMMENSAL; HOMEOSTASIS; IMMUNITY; MUCUS; RNA; RODENT; VIRUS;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL FLORA; BACTERIAL VIRULENCE; BACTEROIDES THETAIOTAOMICRON; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CITROBACTER RODENTIUM; COMMENSAL; CONTROLLED STUDY; ENTERIC VIRUS; FEMALE; GENE EXPRESSION; LACTOBACILLUS JOHNSONII; LYMPHOCYTE FUNCTION; MALE; METABOLISM; MICROBIAL COMMUNITY; MOUSE; NONHUMAN; NOROVIRUS; PANETH CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; VIRUS STRAIN; ANIMAL; BACTERIAL PHENOMENA AND FUNCTIONS; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; ENTEROBACTERIACEAE INFECTION; ENTEROVIRUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GERMFREE ANIMAL; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE MUCOSA; MOLECULAR GENETICS; MUCOSAL IMMUNITY; PHYSIOLOGY; VIROLOGY;

BACTERIA (MICROORGANISMS); EUKARYOTA; MURINE NOROVIRUS; MUS; RNA VIRUSES;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PHYSIOLOGICAL PHENOMENA; CITROBACTER RODENTIUM; ENTEROBACTERIACEAE INFECTIONS; ENTEROVIRUS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INTERFERON TYPE I; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NOROVIRUS; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 84920929686     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13960     Document Type: Article

References (38)

1. Honda, K.&Littman, D. R. The microbiome in infectious disease and inflammation. Annu. Rev. Immunol. 30, 759-795 (2012).
2. Duerkop, B. A. & Hooper, L. V. Resident viruses and their interactions with the immune system. Nature Immunol. 14, 654-659 (2013).
3. Virgin, H. W.The virome inmammalian physiology and disease. Cell157,142-150 (2014).
4. Norman, J. M., Handley, S. A.& Virgin, H. W. Kingdom-agnostic metagenomics and the importance of complete characterization of enteric microbial communities. Gastroenterology 146, 1459-1469 (2014).
5. Donaldson, E. F., Lindesmith, L. C., Lobue, A. D. & Baric, R. S. Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations. Immunol. Rev. 225, 190-211 (2008).
6. Popgeorgiev, N., Temmam, S., Raoult, D. & Desnues, C. Describing the silent human virome with an emphasis on giant viruses. Intervirology 56, 395-412 (2013).
7. Ninomiya, M., Takahashi, M., Nishizawa, T., Shimosegawa, T. & Okamoto, H. Development of PCR assays with nested primers specific for differential detection of three human anellovirusesandearly acquisitionofdual or triple infectionduring infancy. J. Clin. Microbiol. 46, 507-514 (2008).
8. Ott, C. et al. Use of a TT virus ORF1 recombinant protein to detect anti-TT virus antibodies in human sera. J. Gen. Virol. 81, 2949-2958 (2000).
9. Minot, S. et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 21, 1616-1625 (2011).
10. Modi, S. R., Lee, H. H., Spina, C. S. & Collins, J. J. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499, 219-222 (2013).
11. Reyes, A. et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334-338 (2010).
12. Handley, S. A. et al. Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 151, 253-266 (2012).
13. Karst, S. M., Wobus, C. E., Lay, M., Davidson, J. & Virgin, H. W. IV STAT1-dependent innate immunity to a Norwalk-like virus. Science 299, 1575-1578 (2003).
14. Wobus, C. E. et al. Replication of norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2, e432 (2004).
15. Cadwell, K. et al. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 141, 1135-1145 (2010).
16. Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nature Rev. Immunol. 9, 313-323 (2009).
17. Kuss, S. K. et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334, 249-252 (2011).
18. Kane, M. et al. Successful transmission of a retrovirus depends on the commensal microbiota. Science 334, 245-249 (2011).
19. Olszak, T. et al. Microbial exposureduring early life has persistent effects onnatural killer T cell function. Science 336, 489-493 (2012).
20. Thackray, L. B. et al. Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence. J. Virol. 81, 10460-10473 (2007).
21. Mortha, A. et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343, 1249288 (2014).
22. Wlodarska, M. et al. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 79, 1536-1545 (2011).
23. Kamada, N. et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336, 1325-1329 (2012).
24. Grohmann, G. et al. Outbreak of human calicivirus gastroenteritis in a day-care center in Sydney, Australia. J. Clin. Microbiol. 29, 544-550 (1991).
25. Matson, D. O., Estes, M. K., Tanaka, T., Bartlett, A. V.& Pickering, L. K. Asymptomatic human calicivirus infection in a day care center. Pediatr. Infect. Dis. J. 9, 190-195 (1990).
26. González-Navajas, J. M.,Lee, J.,David,M.&Raz, E.Immunomodulatory functions of type I interferons. Nature Rev. Immunol. 12, 125-135 (2012).
27. Basic, M. et al. Norovirus triggered microbiota-driven mucosal inflammation in interleukin 10-deficient mice. Inflamm. Bowel Dis. 20, 431-443 (2014).
28. Lipkin, W. I. & Firth, C. Viral surveillance and discovery. Curr Opin Virol 3, 199-204 (2013).
29. Marchiando, A. M. et al. A deficiency in the autophagy gene Atg16L1 enhances resistance to enteric bacterial infection. Cell Host Microbe 14, 216-224 (2013).
30. Strong, D. W., Thackray, L. B., Smith, T. J. & Virgin, H. W. Protruding domain of capsid protein is necessary and sufficient to determine murine norovirus replication and pathogenesis in vivo. J. Virol. 86, 2950-2958 (2012).
31. Gonzalez-Hernandez, M. B., Bragazzi Cunha, J. & Wobus, C. E. Plaque assay for murine norovirus. J. Vis. Exp. e4297 (2012).
32. Cadwell, K. et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456, 259-263 (2008).
33. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
34. Huang, D. W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large genelists usingDAVIDbioinformatics resources.Nature Protocols 4,44-57 (2009).
35. Tajima, M., Kotani, Y., Kurosawa, T. & Miyasaka, M. Pitfalls in mouse norovirus (MNV) detection in fecal samples using RT-PCR, and construction of new MNV-specific primers. Exp. Anim. 62, 127-135 (2013).
36. Kim, M., Lee, H., Chang, K. O. & Ko, G. Molecular characterization of murine norovirus isolates from South Korea. Virus Res. 147, 1-6 (2010).
37. Izcue, A. et al. Interleukin-23 restrains regulatory T cell activity to drive T celldependent colitis. Immunity 28, 559-570 (2008).
38. Mumphrey, S. M. et al. Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is preventedbySTAT1-dependent interferonresponses. J. Virol.81,3251-3263(2007).