TLR-7 activation enhances IL-22-mediated colonization resistance against vancomycin-resistant enterococcus

Science Translational Medicine

Volumn 8, Issue 327, 2016, Pages

  Abt, Michael C ^a   Buffie, Charlie G ^a   Sušac, Bože ^a   Becattini, Simone ^a   Carter, Rebecca A ^a   Leiner, Ingrid ^a   Keith, James W ^a   Artis, David ^b   Osborne, Lisa C ^c   Pamer, Eric G ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; C TYPE LECTIN REGENERATING ISLET DERIVED 3 GAMMA; GARDIQUIMOD; GLYCOPROTEIN P 15095; IMIQUIMOD; INTERLEUKIN 1; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 7 RECEPTOR; LECTIN; MESSENGER RNA; METRONIDAZOLE; NEOMYCIN; RESIQUIMOD; THY 1 ANTIGEN; TOLL LIKE RECEPTOR 7; UNCLASSIFIED DRUG; VANCOMYCIN; IMIDAZOLE DERIVATIVE; INTERFERON; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; LIGAND; PROTEIN; REG3G PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; COLONIZATION RESISTANCE; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HOST RESISTANCE; IMMUNOSTIMULATION; INNATE IMMUNITY; INTESTINAL COLONIZATION; INTESTINE; INTRACELLULAR SIGNALING; LYMPHOID CELL; MICROBIAL COMMUNITY; MOUSE; MURINE NOROVIRUS INFECTION; NONHUMAN; NOROVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA TRANSCRIPTION; SINGLE DRUG DOSE; TRANSCRIPTION REGULATION; VANCOMYCIN RESISTANT ENTEROCOCCUS; VIRUS TITRATION; ANIMAL; ANTIBIOTIC RESISTANCE; BACTERIAL COUNT; C57BL MOUSE; CALICIVIRUS INFECTION; COMPLICATION; DENDRITIC CELL; DRUG EFFECTS; ENTEROCOCCUS; GASTROENTERITIS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NOROVIRUS; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIROLOGY;

AMPICILLIN; ANIMALS; ANTIGENS, CD11C; CALICIVIRIDAE INFECTIONS; COLONY COUNT, MICROBIAL; DENDRITIC CELLS; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS; GASTROENTERITIS; IMIDAZOLES; INTERFERON TYPE I; INTERLEUKIN-1; INTERLEUKIN-23; INTERLEUKINS; LIGANDS; MICE, INBRED C57BL; NOROVIRUS; PROTEINS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 7; VANCOMYCIN;

EID: 84959431760     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aad6663     Document Type: Article

References (54)

1. Antibiotic Resistance Threats in the United States, 2013 (Centers for Disease Control and Prevention, Atlanta, GA, 2014).
2. B. Spellberg, R. Guidos, D. Gilbert, J. Bradley, H. W. Boucher, W. M. Scheld, J. G. Bartlett, J. Edwards Jr.; Infectious Diseases Society of America, The epidemic of antibiotic-resistant infections: A call to action for the medical community from the Infectious Diseases Society of America. Clin. Infect. Dis. 46, 155-164 (2008).
3. P. B. Eckburg, E.M. Bik, C. N. Bernstein, E. Purdom, L.Dethlefsen,M. Sargent, S. R. Gill, K. E. Nelson, D. A. Relman, Diversity of the human intestinal microbial flora. Science 308, 1635-1638 (2005).
4. C. A. Arias, B. E. Murray, Emergence and management of drug-resistant enterococcal infections. Expert Rev. Anti Infect. Ther. 6, 637-655 (2008).
5. C. A. Arias, B. E. Murray, The rise of the Enterococcus: Beyond vancomycin resistance. Nat. Rev. Microbiol. 10, 266-278 (2012).
6. C. J. Donskey, T. K. Chowdhry, M. T. Hecker, C. K. Hoyen, J. A. Hanrahan, A. M. Hujer, R. A. Hutton-Thomas, C. C. Whalen, R. A. Bonomo, L. B. Rice, Effect of antibiotic therapy on the density of vancomycin-resistant enterococci in the stool of colonized patients. N. Engl. J. Med. 343, 1925-1932 (2000).
7. C. Ubeda, Y. Taur, R. R. Jenq, M. J. Equinda, T. Son, M. Samstein, A. Viale, N. D. Socci, M. R. M. Van den Brink, M. Kamboj, E. G. Pamer, Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J. Clin. Invest. 120, 4332-4341 (2010).
8. Y. Taur, R. R. Jenq, M.-A. Perales, E. R. Littmann, S. Morjaria, L. Ling, D. No, A. Gobourne, A. Viale, P. B. Dahi, D. M. Ponce, J. N. Barker, S. Giralt, M. Van den Brink, E. G. Pamer, The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood 124, 1174-1182 (2014).
9. Y. Taur, J. B. Xavier, L. Lipuma, C. Ubeda, J. Goldberg, A. Gobourne, Y. J. Lee, K. A. Dubin, N. D. Socci, A. Viale, M.-A. Perales, R. R. Jenq, M. R. M. Van den Brink, E. G. Pamer, Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin. Infect. Dis. 55, 905-914 (2012).
10. C. E. Magauran, C. D. Salgado, Challenges and advances in infection control of hematopoietic stem cell transplant recipients. Infect. Disord. Drug Targets 11, 18-26 (2011).
11. D. M. Weinstock, M. Conlon, C. Iovino, T. Aubrey, C. Gudiol, E. Riedel, J. W. Young, T. E. Kiehn, G. Zuccotti, Colonization, bloodstreaminfection, andmortality caused by vancomycin-resistant enterococcus early after allogeneic hematopoietic stem cell transplant. Biol. Blood Marrow Transplant. 13, 615-621 (2007).
12. C. G. Buffie, E. G. Pamer, Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13, 790-801 (2013).
13. M. C. Abt, E. G. Pamer, Commensal bacteria mediated defenses against pathogens. Curr. Opin. Immunol. 29, 16-22 (2014).
14. H. L. Cash, C. V. Whitham, C. L. Behrendt, L. V. Hooper, Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313, 1126-1130 (2006).
15. K. S. Kobayashi, M. Chamaillard, Y. Ogura, O. Henegariu, N. Inohara, G. Nuñez, R. A. Flavell, Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307, 731-734 (2005).
16. M. Rupnik, M. H. Wilcox, D. N. Gerding, Clostridium difficile infection: New developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7, 526-536 (2009).
17. M. Wlodarska, B. Willing, K. M. Keeney, A. Menendez, K. S. Bergstrom, N. Gill, S. L. Russell, B. A. Vallance, B. B. Finlay, Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 79, 1536-1545 (2011).
18. R. B. R. Ferreira, N. Gill, B. P. Willing, L. C. M. Antunes, S. L. Russell, M. A. Croxen, B. B. Finlay, The intestinal microbiota plays a role in Salmonella-induced colitis independent of pathogen colonization. PLOS One 6, e20338 (2011).
19. M. Bohnhoff, C. P. Miller, W. R. Martin, Resistance of the mouse's intestinal tract to experimental Salmonella infection. I. Factors which interfere with the initiation of infection by oral inoculation. J. Exp. Med. 120, 805-816 (1964).
20. E. Van Nood, A. Vrieze, M. Nieuwdorp, S. Fuentes, E. G. Zoetendal, W. M. De Vos, C. E. Visser, E. J. Kuijper, J. F. W. M. Bartelsman, J. G. P. Tijssen, P. Speelman, M. G. W. Dijkgraaf, J. J. Keller, Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J.Med. 368, 407-415 (2013).
21. E. G. Pamer, Fecal microbiota transplantation: Effectiveness, complexities, and lingering concerns. Mucosal Immunol. 7, 210-214 (2014).
22. A. Reyes, M. Haynes, N. Hanson, F. E. Angly, A. C. Heath, F. Rohwer, J. I. Gordon, Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334-338 (2010).
23. H. W. Virgin, The virome in mammalian physiology and disease. Cell 157, 142-150 (2014).
24. E. S. Barton, D.W. White, J. S. Cathelyn, K. A. Brett-McClellan, M. Engle,M. S. Diamond, V. L. Miller, H.W. Virgin IV, Herpesvirus latency confers symbiotic protection frombacterial infection. Nature 447, 326-329 (2007).
25. E. Kernbauer, Y. Ding, K. Cadwell, An enteric virus can replace the beneficial function of commensal bacteria. Nature 516, 94-98 (2014).
26. P. P. Hernández, T. Mahlakõiv, I. Yang, V. Schwierzeck, N. Nguyen, F. Guendel, K. Gronke, B. Ryffel, C. Hölscher, L. Dumoutier, J.-C. Renauld, S. Suerbaum, P. Staeheli, A. Diefenbach, Interferon-l and interleukin 22 act synergistically for the induction of interferon-stimulated genes and control of rotavirus infection. Nat. Immunol. 16, 698-707 (2015).
27. H. Hemmi, T. Kaisho, O. Takeuchi, S. Sato, H. Sanjo, K. Hoshino, T. Horiuchi, H. Tomizawa, K. Takeda, S. Akira, Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3, 196-200 (2002).
28. D. H. Dockrell, G. R. Kinghorn, Imiquimod and resiquimod as novel immunomodulators. J. Antimicrob. Chemother. 48, 751-755 (2001).
29. L. Edwards, A. Ferenczy, L. Eron, D. Baker,M. L.Owens, T. L. Fox, A. J. Hougham, K. A. Schmitt; HPV Study Group, Self-administered topical 5% imiquimod cream for external anogenital warts. Arch. Dermatol. 134, 25-30 (1998).
30. K. R. Beutner, S. K. Tyring, K. F. Trofatter Jr., J. M. Douglas Jr., S. Spruance, M. L. Owens, T. L. Fox, A. J. Hougham, K. A. Schmitt, Imiquimod, a patient-applied immune-response modifier for treatment of external genital warts. Antimicrob. Agents Chemother. 42, 789-794 (1998).
31. K. R. Beutner, S. L. Spruance, A. J. Hougham, T. L. Fox, M. L. Owens, J. M. Douglas Jr., Treatment of genital warts with an immune-response modifier (imiquimod). J. Am. Acad. Dermatol. 38, 230-239 (1998).
32. S. Caballero, R. Carter, X. Ke, B. Sušac, I. M. Leiner, G. J. Kim, L. Miller, L. Ling, K. Manova, E. G. Pamer, Distinct but spatially overlapping intestinal niches for vancomycin-resistant Enterococcus faecium and carbapenem-resistant Klebsiella pneumoniae. PLOS Pathog. 11, e1005132 (2015).
33. M. Kane, L. K. Case, K. Kopaskie, A. Kozlova, C. MacDearmid, A. V. Chervonsky, T. V. Golovkina, Successful transmission of a retrovirus depends on the commensal microbiota. Science 334, 245-249 (2011).
34. S. K. Kuss, G. T. Best, C. A. Etheredge, A. J. Pruijssers, J. M. Frierson, L. V. Hooper, T. S. Dermody, J. K. Pfeiffer, Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334, 249-252 (2011).
35. M. T. Baldridge, T. J. Nice, B. T.McCune, C. C. Yokoyama, A. Kambal, M.Wheadon,M. S. Diamond, Y. Ivanova, M. Artyomov, H. W. Virgin, Commensal microbes and interferon-l determine persistence of enteric murine norovirus infection. Science 347, 266-269 (2015).
36. K. Brandl, G. Plitas, C. N. Mihu, C. Ubeda, T. Jia,M. Fleisher, B. Schnabl, R. P.DeMatteo, E. G. Pamer, Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455, 804-807 (2008).
37. M. A. Kinnebrew, C. Ubeda, L. A. Zenewicz, N. Smith, R. A. Flavell, E. G. Pamer, Bacterial flagellin stimulates toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection. J. Infect. Dis. 201, 534-543 (2010).
38. T. Kawai, S. Akira, Toll-like receptor and RIG-1-like receptor signaling. Ann. N. Y. Acad. Sci. 1143, 1-20 (2008).
39. S. J. Gibson, J. M. Lindh, T. R. Riter, R. M. Gleason, L. M. Rogers, A. E. Fuller, J. L. Oesterich, K. B. Gorden, X. Qiu, S. W. McKane, R. J. Noelle, R. L. Miller, R. M. Kedl, P. Fitzgerald-Bocarsly, M. A. Tomai, J. P. Vasilakos, Plasmacytoid dendritic cells produce cytokines and mature in response to the TLR7 agonists, imiquimod and resiquimod. Cell. Immunol. 218, 74-86 (2002).
40. A. B. Van Belle, M. De Heusch, M.M. Lemaire, E. Hendrickx, G.Warnier, K. Dunussi-Joannopoulos, L. A. Fouser, J.-C. Renauld, L. Dumoutier, IL-22 is required for imiquimod-induced psoriasiform skin inflammation in mice. J. Immunol. 188, 462-469 (2012).
41. L. Van Der Fits, S. Mourits, J. S. A. Voerman, M. Kant, L. Boon, J. D. Laman, F. Cornelissen, A.-M. Mus, E. Florencia, E. P. Prens, E. Lubberts, Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J. Immunol. 182, 5836-5845 (2009).
42. M. A. Kinnebrew, C. G. Buffie, G. E. Diehl, L. A. Zenewicz, I. Leiner, T. M. Hohl, R. A. Flavell, D. R. Littman, E. G. Pamer, Interleukin 23 production by intestinal CD103+CD11b+ dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity 36, 276-287 (2012).
43. Y. Zheng, P. A. Valdez, D. M. Danilenko, Y. Hu, S. M. Sa, Q. Gong, A. R. Abbas, Z. Modrusan, N. Ghilardi, F. J. De Sauvage, W. Ouyang, Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14, 282-289 (2008).
44. C. E. Sutton, S. J. Lalor, C. M. Sweeney, C. F. Brereton, E. C. Lavelle, K. H. G. Mills, Interleukin-1 and IL-23 induce innate IL-17 production from gd T cells, amplifying Th17 responses and autoimmunity. Immunity 31, 331-341 (2009).
45. A. M. Hanash, J. A. Dudakov, G. Hua, M. H. O'Connor, L. F. Young, N. V. Singer, M. L. West, R. R. Jenq, A. M. Holland, L. W. Kappel, A. Ghosh, J. J. Tsai, U. K. Rao, N. L. Yim, O. M. Smith, E. Velardi, E. B. Hawryluk, G. F. Murphy, C. Liu, L. A. Fouser, R. Kolesnick, B. R. Blazar, M. R. M. Van den Brink, Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 37, 339-350 (2012).
46. S. Milling, U. Yrlid, V. Cerovic, G. MacPherson, Subsets of migrating intestinal dendritic cells. Immunol. Rev. 234, 259-267 (2010).
47. R. E. Roses, S. Xu, M. Xu, U. Koldovsky, G. Koski, B. J. Czerniecki, Differential production of IL-23 and IL-12 by myeloid-derived dendritic cells in response to TLR agonists. J. Immunol. 181, 5120-5127 (2008).
48. B. A. Duerkop, C. V. Clements, D. Rollins, J. L. M. Rodrigues, L. V. Hooper, A composite bacteriophage alters colonization by an intestinal commensal bacterium. Proc. Natl. Acad. Sci. U.S.A. 109, 17621-17626 (2012).
49. D. J. Hentges, R. Freter, In vivo and in vitro antagonism of intestinal bacteria against Shigella flexneri. I. Correlation between various tests. J. Infect. Dis. 110, 30-37 (1962).
50. P. J. Pockros, D. Guyader, H. Patton, M. J. Tong, T. Wright, J. G. McHutchison, T.-C. Meng, Oral resiquimod in chronic HCV infection: Safety and efficacy in 2 placebo-controlled, doubleblind phase IIa studies. J. Hepatol. 47, 174-182 (2007).
51. V. T. Tomov, L. C. Osborne, D. V. Dolfi, G. F. Sonnenberg, L. A.Monticelli, K.Mansfield, H.W. Virgin, D. Artis, E. J. Wherry, Persistent enteric murine norovirus infection is associated with functionally suboptimal virus-specific CD8 T cell responses. J. Virol. 87, 7015-7031 (2013).
52. S. Vaishnava, M. Yamamoto, K. M. Severson, K. A. Ruhn, X. Yu, O. Koren, R. Ley, E. K. Wakeland, L. V. Hooper, The antibacterial lectin RegIIIg promotes the spatial segregation of microbiota and host in the intestine. Science 334, 255-258 (2011).
53. A. Swidsinski, V. Loening-Baucke, H. Lochs, L. P. Hale, Spatial organization of bacterial flora in normal and inflamed intestine: A fluorescence in situ hybridization study in mice. World J. Gastroenterol. 11, 1131-1140 (2005).
54. K. Waar, J. E. Degener, M. J. Van Luyn, H. J. M. Harmsen, Fluorescent in situ hybridization with specific DNA probes offers adequate detection of Enterococcus faecalis and Enterococcus faecium in clinical samples. J. Med. Microbiol. 54, 937-944 (2005).