Early innate immunity to bacterial infection in the lung is regulated systemically by the commensal microbiota via Nod-like receptor ligands

Infection and Immunity

Volumn 82, Issue 11, 2014, Pages 4596-4606

  Clarke, Thomas B ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; CASPASE RECRUITMENT DOMAIN PROTEIN 4; INTERLEUKIN 6; METRONIDAZOLE; MURAMYL DIPEPTIDE; NEOMYCIN; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; VANCOMYCIN; LIGAND; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL IMMUNITY; BACTERIAL INFECTION; BACTERIAL LOAD; BACTERICIDAL ACTIVITY; CELL WALL; COMMENSAL; COMMENSAL MICROBIOTA; CONTROLLED STUDY; EX VIVO STUDY; GASTROINTESTINAL TRACT; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IN VIVO STUDY; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE MUCOSA; KLEBSIELLA PNEUMONIAE; LUNG ALVEOLUS MACROPHAGE; LUNG INFECTION; MICROFLORA; MOUSE; NONHUMAN; PATHOGENESIS; RESPIRATORY TRACT INFECTION; UPPER RESPIRATORY TRACT; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; IMMUNOLOGY; INTESTINE; KLEBSIELLA INFECTION; LUNG DISEASE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SYMBIOSIS;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; ANIMALS; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; INTESTINES; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LIGANDS; LUNG DISEASES; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; NOD SIGNALING ADAPTOR PROTEINS; REACTIVE OXYGEN SPECIES; SYMBIOSIS;

EID: 84907960584     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02212-14     Document Type: Article

References (69)

1. Honda K, Littman DR. 2012. The microbiome in infectious disease and inflammation. Annu. Rev. Immunol. 30:759-795. http://dx.doi.org/10.1146/annurev-immunol-020711-074937.
2. Hooper LV, Littman DR, Macpherson AJ. 2012. Interactions between the microbiota and the immune system. Science 336:1268-1273. http://dx.doi.org/10.1126/science.1223490.
3. Ley RE, Peterson DA, Gordon JI. 2006. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837-848. http://dx.doi.org/10.1016/j.cell.2006.02.017.
4. Abt MC, Artis D. 2013. The dynamic influence of commensal bacteria on the immune response to pathogens. Curr. Opin. Microbiol. 16:4-9. http://dx.doi.org/10.1016/j.mib.2012.12.002.
5. Berer K, Krishnamoorthy G. 2014. Microbial view of central nervous system autoimmunity. FEBS Lett. http://dx.doi.org/10.1016/j.febslet.2014.04.007.
6. Chu H, Mazmanian SK. 2013. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat. Immunol. 14:668-675. http://dx.doi.org/10.1038/ni.2635.
7. Erturk-Hasdemir D, Kasper DL. 2013. Resident commensals shaping immunity. Curr. Opin. Immunol. 25:450-455. http://dx.doi.org/10.1016/j.coi.2013.06.001.
8. Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S, Dai RM, Kiu H, Cardone M, Naik S, Patri AK, Wang E, Marincola FM, Frank KM, Belkaid Y, Trinchieri G, Goldszmid RS. 2013. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342:967-970. http://dx.doi.org/10.1126/science.1240527.
9. Khosravi A, Mazmanian SK. 2013. Disruption of the gut microbiome as a risk factor for microbial infections. Curr. Opin. Microbiol. 16:221-227. http://dx.doi.org/10.1016/j.mib.2013.03.009.
10. Molloy MJ, Bouladoux N, Belkaid Y. 2012. Intestinal microbiota: shaping local and systemic immune responses. Semin. Immunol. 24:58-66. http://dx.doi.org/10.1016/j.smim.2011.11.008.
11. Naik S, Bouladoux N, Wilhelm C, Molloy MJ, Salcedo R, Kastenmuller W, Deming C, Quinones M, Koo L, Conlan S, Spencer S, Hall JA, Dzutsev A, Kong H, Campbell DJ, Trinchieri G, Segre JA, Belkaid Y. 2012. Compartmentalized control of skin immunity by resident commensals. Science 337:1115-1119. http://dx.doi.org/10.1126/science.1225152.
12. Rakoff-Nahoum S, Medzhitov R. 2007. Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88. Science 317:124-127. http://dx.doi.org/10.1126/science.1140488.
13. Round JL, Mazmanian SK. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9:313-323. http://dx.doi.org/10.1038/nri2515.
14. Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, Littman DR, Benoist C, Mathis D. 2010. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32:815-827. http://dx.doi.org/10.1016/j.immuni.2010.06.001.
15. Rakoff-Nahoum S, Hao L, Medzhitov R. 2006. Role of toll-like receptors in spontaneous commensal-dependent colitis. Immunity 25:319-329. http://dx.doi.org/10.1016/j.immuni.2006.06.010.
16. Abt MC, Osborne LC, Monticelli LA, Doering TA, Alenghat T, Sonnenberg GF, Paley MA, Antenus M, Williams KL, Erikson J, Wherry EJ, Artis D. 2012. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37:158-170. http://dx.doi.org/10.1016/j.immuni.2012.04.011.
17. Brandl K, Plitas G, Mihu CN, Ubeda C, Jia T, Fleisher M, Schnabl B, DeMatteo RP, Pamer EG. 2008. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455:804-807. http://dx.doi.org/10.1038/nature07250.
18. Deshmukh HS, Liu Y, Menkiti OR, Mei J, Dai N, O'Leary CE, Oliver PM, Kolls JK, Weiser JN, Worthen GS. 2014. The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice. Nat. Med. 20:524-530. http://dx.doi.org/10.1038/nm.3542.
19. Didierlaurent A, Goulding J, Patel S, Snelgrove R, Low L, Bebien M, Lawrence T, van Rijt LS, Lambrecht BN, Sirard JC, Hussell T. 2008. Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J. Exp. Med. 205:323-329. http://dx.doi.org/10.1084/jem.20070891.
20. Duarte R, Silva AM, Vieira LQ, Afonso LC, Nicoli JR. 2004. Influence of normal microbiota on some aspects of the immune response during experimental infection with Trypanosoma cruzi in mice. J. Med. Microbiol. 53:741-748. http://dx.doi.org/10.1099/jmm.0.45657-0.
21. Fagundes CT, Amaral FA, Vieira AT, Soares AC, Pinho V, Nicoli JR, Vieira LQ, Teixeira MM, Souza DG. 2012. Transient TLR activation restores inflammatory response and ability to control pulmonary bacterial infection in germfree mice. J. Immunol. 188:1411-1420. http://dx.doi.org/10.4049/jimmunol.1101682.
22. Ganal SC, Sanos SL, Kallfass C, Oberle K, Johner C, Kirschning C, Lienenklaus S, Weiss S, Staeheli P, Aichele P, Diefenbach A. 2012. Priming of natural killer cells by nonmucosal mononuclear phagocytes requires instructive signals from commensal microbiota. Immunity 37:171-186. http://dx.doi.org/10.1016/j.immuni.2012.05.020.
23. Inagaki H, Suzuki T, Nomoto K, Yoshikai Y. 1996. Increased susceptibility to primary infection with Listeria monocytogenes in germfree mice may be due to lack of accumulation of L-selectin+CD44+T cells in sites of inflammation. Infect. Immun. 64:3280-3287.
24. Khosravi A, Yanez A, Price JG, Chow A, Merad M, Goodridge HS, Mazmanian SK. 2014. Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe 15:374-381. http://dx.doi.org/10.1016/j.chom.2014.02.006.
25. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118:229-241. http://dx.doi.org/10.1016/j.cell.2004.07.002.
26. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, Tanoue T, Imaoka A, Itoh K, Takeda K, Umesaki Y, Honda K, Littman DR. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139:485-498. http://dx.doi.org/10.1016/j.cell.2009.09.033.
27. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K, Kim S, Fritz JV, Wilmes P, Ueha S, Matsushima K, Ohno H, Olle B, Sakaguchi S, Taniguchi T, Morita H, Hattori M, Honda K. 2013. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500:232-236. http://dx.doi.org/10.1038/nature12331.
28. Round JL, Mazmanian SK. 2010. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. U. S. A. 107:12204-12209. http://dx.doi.org/10.1073/pnas.0909122107.
29. Stecher B, Hardt WD. 2008. The role of microbiota in infectious disease. Trends Microbiol. 16:107-114. http://dx.doi.org/10.1016/j.tim.2007.12.008.
30. Stecher B, Hardt WD. 2011. Mechanisms controlling pathogen colonization of the gut. Curr. Opin. Microbiol. 14:82-91. http://dx.doi.org/10.1016/j.mib.2010.10.003.
31. Spees AM, Lopez CA, Kingsbury DD, Winter SE, Baumler AJ. 2013. Colonization resistance: battle of the bugs or menage a trois with the host? PLoS Pathog. 9:e1003730. http://dx.doi.org/10.1371/journal.ppat.1003730.
32. Pang IK, Iwasaki A. 2012. Control of antiviral immunity by pattern recognition and the microbiome. Immunol. Rev. 245:209-226. http://dx.doi.org/10.1111/j.1600-065X.2011.01073.x.
33. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, Iwasaki A. 2011. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. U. S. A. 108:5354-5359. http://dx.doi.org/10.1073/pnas.1019378108.
34. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. 2010. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16:228-231. http://dx.doi.org/10.1038/nm.2087.
35. Hill DA, Hoffmann C, Abt MC, Du Y, Kobuley D, Kirn TJ, Bushman FD, Artis D. 2010. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol. 3:148-158. http://dx.doi.org/10.1038/mi.2009.132.
36. Zurita E, Moreno G, Errea A, Ormazabal M, Rumbo M, Hozbor D. 2013. The stimulated innate resistance event in Bordetella pertussis infection is dependent on reactive oxygen species production. Infect. Immun. 81:2371-2378. http://dx.doi.org/10.1128/IAI.00336-13.
37. Zhang X, Goncalves R, Mosser DM. 2008. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. Chapter 14:Unit 14.11. http://dx.doi.org/10.1002/0471142735.im1401s83.
38. Hickman-Davis JM, O'Reilly P, Davis IC, Peti-Peterdi J, Davis G, Young KR, Devlin RB, Matalon S. 2002. Killing of Klebsiella pneumoniae by human alveolar macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 282:L944-L956.
39. Mancuso P, Peters-Golden M. 2000. Modulation of alveolar macrophage phagocytosis by leukotrienes is Fc receptor-mediated and protein kinase C-dependent. Am. J. Respir. Cell Mol. Biol. 23:727-733. http://dx.doi.org/10.1165/ajrcmb.23.6.4246.
40. Serezani CH, Aronoff DM, Jancar S, Mancuso P, Peters-Golden M. 2005. Leukotrienes enhance the bactericidal activity of alveolar macrophages against Klebsiella pneumoniae through the activation of NADPH oxidase. Blood 106:1067-1075. http://dx.doi.org/10.1182/blood-2004-08-3323.
41. Kim YG, Udayanga KG, Totsuka N, Weinberg JB, Nunez G, Shibuya A. 2014. Gut dysbiosis promotes M2 macrophage polarization and allergic airway inflammation via fungi-induced PGE(2). Cell Host Microbe 15:95-102. http://dx.doi.org/10.1016/j.chom.2013.12.010.
42. Wang J, Li F, Sun R, Gao X, Wei H, Li LJ, Tian Z. 2013. Bacterial colonization dampens influenza-mediated acute lung injury via induction of M2 alveolar macrophages. Nat. Commun. 4:2106. http://dx.doi.org/10.1038/ncomms3106.
43. Clarke TB, Francella N, Huegel A, Weiser JN. 2011. Invasive bacterial pathogens exploit TLR-mediated downregulation of tight junction components to facilitate translocation across the epithelium. Cell Host Microbe 9:404-414. http://dx.doi.org/10.1016/j.chom.2011.04.012.
44. Beisswenger C, Coyne CB, Shchepetov M, Weiser JN. 2007. Role of p38 MAP kinase and transforming growth factor-beta signaling in transepithelial migration of invasive bacterial pathogens. J. Biol. Chem. 282:28700-28708. http://dx.doi.org/10.1074/jbc.M703576200.
45. Klein RA, Hartmann R, Egge H, Behr T, Fischer W. 1994. The aqueous solution structure of the tetrasaccharide-ribitol repeat-unit from the lipoteichoic acid of Streptococcus pneumoniae strain R6 determined using a combination of NMR spectroscopy and computer calculations. Carbohydr. Res. 256:189-222. http://dx.doi.org/10.1016/0008-6215(94)84209-4.
46. Dalpke A, Frank J, Peter M, Heeg K. 2006. Activation of toll-like receptor 9 by DNA from different bacterial species. Infect. Immun. 74:940-946. http://dx.doi.org/10.1128/IAI.74.2.940-946.2006.
47. Clarke TB, Kawai F, Park SY, Tame JR, Dowson CG, Roper DI. 2009. Mutational analysis of the substrate specificity of Escherichia coli penicillin binding protein 4. Biochemistry 48:2675-2683. http://dx.doi.org/10.1021/bi801993x.
48. Medzhitov R. 2008. Origin and physiological roles of inflammation. Nature 454:428-435. http://dx.doi.org/10.1038/nature07201.
49. Kim OY, Monsel A, Bertrand M, Cavaillon JM, Coriat P, Adib-Conquy M. 2009. Translocation of bacterial NOD2 agonist and its link with inflammation. Crit. Care 13:R124. http://dx.doi.org/10.1186/cc7980.
50. Xu XL, Lee RT, Fang HM, Wang YM, Li R, Zou H, Zhu Y, Wang Y. 2008. Bacterial peptidoglycan triggers Candida albicans hyphal growth by directly activating the adenylyl cyclase Cyr1p. Cell Host Microbe 4:28-39. http://dx.doi.org/10.1016/j.chom.2008.05.014.
51. Chaudhuri N, Sabroe I. 2008. Basic science of the innate immune system and the lung. Paediatr. Respir. Rev. 9:236-242. http://dx.doi.org/10.1016/j.prrv.2008.03.002.
52. Eddens T, Kolls JK. 2012. Host defenses against bacterial lower respiratory tract infection. Curr. Opin. Immunol. 24:424-430. http://dx.doi.org/10.1016/j.coi.2012.07.005.
53. Rosenberger CM, Finlay BB. 2003. Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat. Rev. Mol. Cell Biol. 4:385-396. http://dx.doi.org/10.1038/nrm1104.
54. Forman HJ, Torres M. 2002. Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am. J. Respir. Crit. Care Med. 166:S4-S8. http://dx.doi.org/10.1164/rccm.2206007.
55. Olofsson AC, Hermansson M, Elwing H. 2003. N-acetyl-L-cysteine affects growth, extracellular polysaccharide production, and bacterial biofilm formation on solid surfaces. Appl. Environ. Microbiol. 69:4814-4822. http://dx.doi.org/10.1128/AEM.69.8.4814-4822.2003.
56. Medzhitov R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449:819-826. http://dx.doi.org/10.1038/nature06246.
57. Medzhitov R. 2010. Inflammation 2010: new adventures of an old flame. Cell 140:771-776. http://dx.doi.org/10.1016/j.cell.2010.03.006.
58. Dowling DK, Simmons LW. 2009. Reactive oxygen species as universal constraints in life-history evolution. Proc. Biol. Sci. 276:1737-1745. http://dx.doi.org/10.1098/rspb.2008.1791.
59. Nathan C. 2002. Points of control in inflammation. Nature 420:846-852. http://dx.doi.org/10.1038/nature01320.
60. Jarchum I, Pamer EG. 2011. Regulation of innate and adaptive immunity by the commensal microbiota. Curr. Opin. Immunol. 23:353-360. http://dx.doi.org/10.1016/j.coi.2011.03.001.
61. Chen LW, Chen PH, Hsu CM. 2011. Commensal microflora contribute to host defense against Escherichia coli pneumonia through Toll-like receptors. Shock 36:67-75. http://dx.doi.org/10.1097/SHK.0b013e3182184ee7.
62. Hussell T, Bell TJ. 2014. Alveolar macrophages: plasticity in a tissuespecific context. Nat. Rev. Immunol. 14:81-93. http://dx.doi.org/10.1038/nri3600.
63. Bergendi L, Benes L, Durackova Z, Ferencik M. 1999. Chemistry, physiology and pathology of free radicals. Life Sci. 65:1865-1874. http://dx.doi.org/10.1016/S0024-3205(99)00439-7.
64. Yasuda Y, Matsumura Y, Kasahara K, Ouji N, Sugiura S, Mikasa K, Kita E. 2010. Microbial exposure early in life regulates airway inflammation in mice after infection with Streptococcus pneumoniae with enhancement of local resistance. Am. J. Physiol. Lung Cell. Mol. Physiol. 298:L67-L78. http://dx.doi.org/10.1152/ajplung.00193.2009.
65. Abreu MT, Fukata M, Arditi M. 2005. TLR signaling in the gut in health and disease. J. Immunol. 174:4453-4460. http://dx.doi.org/10.4049/jimmunol.174.8.4453.
66. Werts C, Rubino S, Ling A, Girardin SE, Philpott DJ. 2011. Nod-like receptors in intestinal homeostasis, inflammation, and cancer. J. Leukoc. Biol. 90:471-482. http://dx.doi.org/10.1189/jlb.0411183.
67. Medzhitov R, Janeway CA, Jr. 1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295-298. http://dx.doi.org/10.1016/S0092-8674(00)80412-2.
68. Bouskra D, Brezillon C, Berard M, Werts C, Varona R, Boneca IG, Eberl G. 2008. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456:507-510. http://dx.doi.org/10.1038/nature07450.
69. Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, Mazmanian SK. 2011. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332:974-977. http://dx.doi.org/10.1126/science.1206095.