Intestinal commensal bacteria mediate lung mucosal immunity and promote resistance of newborn mice to infection

Science Translational Medicine

Volumn 9, Issue 376, 2017, Pages

  Gray, Jerilyn ^a   Oehrle, Katherine ^a   Worthen, George ^b   Alenghat, Theresa ^a   Whitsett, Jeffrey ^a   Deshmukh, Hitesh ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CHEMOKINE RECEPTOR CCR4; INTERLEUKIN 22; CCR4 PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; LEUKOCYTE ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL PNEUMONIA; CELL MIGRATION; CLINICAL ARTICLE; COMMENSAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; EMBRYO; FEMALE; HOST RESISTANCE; HUMAN; INTESTINE FLORA; LYMPHOID CELL; MALE; MOUSE; MUCOSAL IMMUNITY; NEWBORN; NONHUMAN; STREPTOCOCCUS PNEUMONIA; ANIMAL; BACTERIAL COUNT; BACTERIUM; C57BL MOUSE; CELL MOTION; DEMOGRAPHY; DISEASE PREDISPOSITION; DISEASE RESISTANCE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INTESTINE; LUNG; LYMPHOCYTE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PNEUMONIA; SYMBIOSIS;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD; BACTERIA; CELL MOVEMENT; COLONY COUNT, MICROBIAL; DEMOGRAPHY; DENDRITIC CELLS; DISEASE RESISTANCE; DISEASE SUSCEPTIBILITY; FEMALE; HUMANS; IMMUNITY, MUCOSAL; INFANT, NEWBORN; INTERLEUKINS; INTESTINES; LUNG; LYMPHOCYTES; MALE; MICE, INBRED C57BL; PNEUMONIA; RECEPTORS, CCR4; SYMBIOSIS;

EID: 85012883069     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaf9412     Document Type: Article

References (91)

1. D. J. Dowling, O. Levy, Ontogeny of early life immunity. Trends Immunol. 35, 299-310 (2014).
2. A. Marchant, T. R. Kollmann, Understanding the ontogeny of the immune system to promote immune-mediated health for life. Front. Immunol. 6, 77 (2015).
3. D. M. MacGillivray, T. R. Kollmann, The role of environmental factors in modulating immune responses in early life. Front. Immunol. 5, 434 (2014).
4. 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).
5. E. Elinav, T. Strowig, J. Henao-Mejia, R. A. Flavell, Regulation of the antimicrobial response by NLR proteins. Immunity 34, 665-679 (2011).
6. S. K. Lathrop, S. M. Bloom, S. M. Rao, K. Nutsch, C.-W. Lio, N. Santacruz, D. A. Peterson, T. S. Stappenbeck, C.-S. Hsieh, Peripheral education of the immune system by colonic commensal microbiota. Nature 478, 250-254 (2011).
7. M. Gomez de Agüero, S. C. Ganal-Vonarburg, T. Fuhrer, S. Rupp, Y. Uchimura, H. Li, A. Steinert, M. Heikenwalder, S. Hapfelmeier, U. Sauer, K. D. McCoy, A. J. Macpherson, The maternal microbiota drives early postnatal innate immune development. Science 351, 1296-1302 (2016).
8. C. Palmer, E. M. Bik, D. B. DiGiulio, D. A. Relman, P. O. Brown, Development of the human infant intestinal microbiota. Plos Biol. 5, e177 (2007).
9. J. Penders, C. Thijs, C. Vink, F. F. Stelma, B. Snijders, I. Kummeling, P. A. van den Brandt, E. E. Stobberingh, Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118, 511-521 (2006).
10. S. Arboleya, B. Sánchez, C. Milani, S. Duranti, G. Solís, N. Fernández, C. G. de los Reyes-Gavilán, M. Ventura, A. Margolles, M. Gueimonde, Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J. Pediatr. 166, 538-544 (2015).
11. V. S. Kuppala, J. Meinzen-Derr, A. L. Morrow, K. R. Schibler, Prolonged initial empirical antibiotic treatment is associated with adverse outcomes in premature infants. J. Pediatr. 159, 720-725 (2011).
12. R. H. Clark, B. T. Bloom, A. R. Spitzer, D. R. Gerstmann, Empiric use of ampicillin and cefotaxime, compared with ampicillin and gentamicin, for neonates at risk for sepsis is associated with an increased risk of neonatal death. Pediatrics 117, 67-74 (2006).
13. C. M. Cotten, S. Taylor, B. Stoll, R. N. Goldberg, N. I. Hansen, P. J. Sánchez, N. Ambalavanan, D. K. Benjamin Jr.; NICHD Neonatal Research Network, Prolonged duration of initial empirical antibiotic treatment is associated with increased rates of necrotizing enterocolitis and death for extremely low birth weight infants. Pediatrics 123, 58-66 (2009).
14. V. Mai, R. M. Torrazza, M. Ukhanova, X. Wang, Y. Sun, N. Li, J. Shuster, R. Sharma, M. L. Hudak, J. Neu, Distortions in development of intestinal microbiota associated with late onset sepsis in preterm infants. PLOS ONE 8, e52876 (2013).
15. T. Ichinohe, I. K. Pang, Y. Kumamoto, D. R. Peaper, J. H. Ho, T. S. Murray, A. Iwasaki, Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. U.S.A. 108, 5354-5359 (2011).
16. C. T. Fagundes, F. A. Amaral, A. T. Vieira, A. C. Soares, V. Pinho, J. R. Nicoli, L. Q. Vieira, M. M. Teixeira, D. G. Souza, Transient TLR activation restores inflammatory response and ability to control pulmonary bacterial infection in germfree mice. J. Immunol. 188, 1411-1420 (2012).
17. R. P. Dickson, J. R. Erb-Downward, G. B. Huffnagle, The role of the bacterial microbiome in lung disease. Expert Rev. Respir. Med. 7, 245-257 (2013).
18. M. G. Dominguez-Bello, E. K. Costello, M. Contreras, M. Magris, G. Hidalgo, N. Fierer, R. Knight, Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. U.S.A. 107, 11971-11975 (2010).
19. M. B. Azad, T. Konya, R. R. Persaud, D. S. Guttman, R. S. Chari, C. J. Field, M. R. Sears, P. J. Mandhane, S. E. Turvey, P. Subbarao, A. B. Becker, J. A. Scott, A. L. Kozyrskyj; CHILD Study Investigators, Impact of maternal intrapartum antibiotics, method of birth and breastfeeding on gut microbiota during the first year of life: A prospective cohort study. BJOG 123, 983-993 (2016).
20. T. S. Glasgow, P. C. Young, J. Wallin, C. Kwok, G. Stoddard, S. Firth, M. Samore, C. L. Byington, Association of intrapartum antibiotic exposure and late-onset serious bacterial infections in infants. Pediatrics 116, 696-702 (2005).
21. A. T. N. Tita, M. B. Landon, C. Y. Spong, Y. Lai, K. J. Leveno, M. W. Varner, A. H. Moawad, S. N. Caritis, P. J. Meis, R. J. Wapner, Y. Sorokin, M. Miodovnik, M. Carpenter, A. M. Peaceman, M. J. O'Sullivan, B. M. Sibai, O. Langer, J. M. Thorp, S. M. Ramin, B. M. Mercer; Eunice Kennedy Shriver NICHD Maternal-Fetal Medicine Units Network, Timing of elective repeat cesarean delivery at term and neonatal outcomes. N. Engl. J. Med. 360, 111-120 (2009).
22. N. Tripathi, C. M. Cotten, P. B. Smith, Antibiotic use and misuse in the neonatal intensive care unit. Clin. Perinatol. 39, 61-68 (2012).
23. S. L. Kaplan, W. J. Barson, P. L. Lin, S. H. Stovall, J. S. Bradley, T. Q. Tan, J. A. Hoffman, L. B. Givner, E. O. Mason Jr., Serotype 19A is the most common serotype causing invasive pneumococcal infections in children. Pediatrics 125, 429-436 (2010).
24. B. J. Stoll, N. Hansen, A. A. Fanaroff, L. L. Wright, W. A. Carlo, R. A. Ehrenkranz, J. A. Lemons, E. F. Donovan, A. R. Stark, J. E. Tyson, W. Oh, C. R. Bauer, S. B. Korones, S. Shankaran, A. R. Laptook, D. K. Stevenson, L.-A. Papile, W. K. Poole, Changes in pathogens causing early-onset sepsis in very-low-birth-weight infants. N. Engl. J. Med. 347, 240-247 (2002).
25. S. L. Russell, M. J. Gold, M. Hartmann, B. P. Willing, L. Thorson, M. Wlodarska, N. Gill, M.-R. Blanchet, W. W. Mohn, K. M. McNagny, B. B. Finlay, Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 13, 440-447 (2012).
26. T. Olszak, D. An, S. Zeissig, M. P. Vera, J. Richter, A. Franke, J. N. Glickman, R. Siebert, R. M. Baron, D. L. Kasper, R. S. Blumberg, Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336, 489-493 (2012).
27. T. J. Schuijt, J. M. Lankelma, B. P. Scicluna, F. de Sousa e Melo, J. J. T. H. Roelofs, J. D. de Boer, A. J. Hoogendijk, R. de Beer, A. de Vos, C. Belzer, W. M. de Vos, T. van der Poll, W. J. Wiersinga, The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut 65, 575-583 (2016).
28. J. Mei, Y. Liu, N. Dai, C. Hoffmann, K. M. Hudock, P. Zhang, S. H. Guttentag, J. K. Kolls, P. M. Oliver, F. D. Bushman, G. S. Worthen, Cxcr2 and Cxcl5 regulate the IL-17/G-CSF axis and neutrophil homeostasis in mice. J. Clin. Invest. 122, 974-986 (2012).
29. H. S. Deshmukh, Y. Liu, O. R. Menkiti, J. Mei, N. Dai, C. E. O'Leary, P. M. Oliver, J. K. Kolls, J. N. Weiser, G. S. Worthen, The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice. Nat. Med. 20, 524-530 (2014).
30. Y. J. Huang, E. S. Charlson, R. G. Collman, S. Colombini-Hatch, F. D. Martinez, R. M. Senior, The role of the lung microbiome in health and disease. A National Heart, Lung, and Blood Institute workshop report. Am. J. Respir. Crit. Care Med. 187, 1382-1387 (2013).
31. R. P. Dickson, G. B. Huffnagle, The lung microbiome: New principles for respiratory bacteriology in health and disease. Plos Pathog. 11, e1004923 (2015).
32. S. J. Aujla, Y. R. Chan, M. Zheng, M. Fei, D. J. Askew, D. A. Pociask, T. A. Reinhart, F. McAllister, J. Edeal, K. Gaus, S. Husain, J. L. Kreindler, P. J. Dubin, J. M. Pilewski, M. M. Myerburg, C. A. Mason, Y. Iwakura, J. K. Kolls, IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat. Med. 14, 275-281 (2008).
33. 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).
34. M. A. Gessner, J. L. Werner, L. M. Lilly, M. P. Nelson, A. E. Metz, C. W. Dunaway, Y. R. Chan, W. Ouyang, G. D. Brown, C. T. Weaver, C. Steele, Dectin-1-dependent interleukin-22 contributes to early innate lung defense against Aspergillus fumigatus. Infect. Immun. 80, 410-417 (2012).
35. J. B. Mear, P. Gosset, E. Kipnis, E. Faure, R. Dessein, S. Jawhara, C. Fradin, K. Faure, D. Poulain, B. Sendid, B. Guery, Candida albicans airway exposure primes the lung innate immune response against Pseudomonas aeruginosa infection through innate lymphoid cell recruitment and interleukin-22-Associated mucosal response. Infect. Immun. 82, 306-315 (2014).
36. C. Wang, L. Wu, K. Bulek, B. N. Martin, J. A. Zepp, Z. Kang, C. Liu, T. Herjan, S. Misra, J. A. Carman, J. Gao, A. Dongre, S. Han, K. D. Bunting, J. S. Ko, H. Xiao, V. K. Kuchroo, W. Ouyang, X. Li, The psoriasis-Associated D10N variant of the adaptor Act1 with impaired regulation by the molecular chaperone hsp90. Nat. Immunol. 14, 72-81 (2013).
37. M.-H. Xie, S. Aggarwal, W.-H. Ho, J. Foster, Z. Zhang, J. Stinson, W. I. Wood, A. D. Goddard, A. L. Gurney, Interleukin (IL)-22, a novel human cytokine that signals through the interferon receptor-related proteins CRF2-4 and IL-22R. J. Biol. Chem. 275, 31335-31339 (2000).
38. M. Wang, K. C. Jeng, L. I. Ping, Exogenous cytokine modulation or neutralization of interleukin-10 enhance survival in lipopolysaccharide-hyporesponsive C3H/HeJ mice with Klebsiella infection. Immunology 98, 90-97 (1999).
39. D. A. Pociask, E. V. Scheller, S. Mandalapu, K. J. McHugh, R. I. Enelow, C. L. Fattman, J. K. Kolls, J. F. Alcorn, IL-22 is essential for lung epithelial repair following influenza infection. Am. J. Pathol. 182, 1286-1296 (2013).
40. J. C. J. Martin, G. Bériou, M. Heslan, C. Chauvin, L. Utriainen, A. Aumeunier, C. L. Scott, A. Mowat, V. Cerovic, S. A. Houston, M. Leboeuf, F. X. Hubert, C. Hémont, M. Merad, S. Milling, R. Josien, Interleukin-22 binding protein (IL-22BP) is constitutively expressed by a subset of conventional dendritic cells and is strongly induced by retinoic acid. Mucosal Immunol. 7, 101-113 (2014).
41. X. Xu, I. D. Weiss, H. H. Zhang, S. P. Singh, T. A. Wynn, M. S. Wilson, J. M. Farber, Conventional NK cells can produce IL-22 and promote host defense in Klebsiella pneumoniae pneumonia. J. Immunol. 192, 1778-1786 (2014).
42. G. F. Sonnenberg, M. G. Nair, T. J. Kirn, C. Zaph, L. A. Fouser, D. Artis, Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A. J. Exp. Med. 207, 1293-1305 (2010).
43. P. L. Simonian, F. Wehrmann, C. L. Roark, W. K. Born, R. L. O'Brien, A. P. Fontenot, d T cells protect against lung fibrosis via IL-22. J. Exp. Med. 207, 2239-2253 (2010).
44. G. Eberl, S. Marmon, M.-J. Sunshine, P. D. Rennert, Y. Choi, D. R. Littman, An essential function for the nuclear receptor RORgt in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5, 64-73 (2004).
45. N. Satoh-Takayama, C. A. J. Vosshenrich, S. Lesjean-Pottier, S. Sawa, M. Lochner, F. Rattis, J.-J. Mention, K. Thiam, N. Cerf-Bensussan, O. Mandelboim, G. Eberl, J. P. Di Santo, Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29, 958-970 (2008).
46. G. Eberl, D. R. Littman, Thymic origin of intestinal ab T cells revealed by fate mapping of RORgt+ cells. Science 305, 248-251 (2004).
47. T. Buch, F. L. Heppner, C. Tertilt, T. J. A. J. Heinen, M. Kremer, F. T. Wunderlich, S. Jung, A. Waisman, A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2, 419-426 (2005).
48. L. Van Maele, C. Carnoy, D. Cayet, S. Ivanov, R. Porte, E. Deruy, J. A. Chabalgoity, J.-C. Renauld, G. Eberl, A. G. Benecke, F. Trottein, C. Faveeuw, J.-C. Sirard, Activation of Type 3 innate lymphoid cells and interleukin 22 secretion in the lungs during Streptococcus pneumoniae infection. J. Infect. Dis. 210, 493-503 (2014).
49. E. J. Villablanca, J. R. Mora, Competitive homing assays to study gut-Tropic T cell migration. J. Vis. Exp. 2011, e2619 (2011).
50. M. H. Kim, E. J. Taparowsky, C. H. Kim, Retinoic acid differentially regulates the migration of innate lymphoid cell subsets to the gut. Immunity 43, 107-119 (2015).
51. E. C. Mackley, S. Houston, C. L. Marriott, E. E. Halford, B. Lucas, V. Cerovic, K. J. Filbey, R. M. Maizels, M. R. Hepworth, G. F. Sonnenberg, S. Milling, D. R. Withers, CCR7-dependent trafficking of RORg+ ILCs creates a unique microenvironment within mucosal draining lymph nodes. Nat. Commun. 6, 5862 (2015).
52. J. W. Griffith, C. L. Sokol, A. D. Luster, Chemokines and chemokine receptors: Positioning cells for host defense and immunity. Annu. Rev. Immunol. 32, 659-702 (2014).
53. Z. Mikhak, J. P. Strassner, A. D. Luster, Lung dendritic cells imprint T cell lung homing and promote lung immunity through the chemokine receptor CCR4. J. Exp. Med. 210, 1855-1869 (2013).
54. B. D. Sather, P. Treuting, N. Perdue, M. Miazgowicz, J. D. Fontenot, A. Y. Rudensky, D. J. Campbell, Altering the distribution of Foxp3+ regulatory T cells results in tissue-specific inflammatory disease. J. Exp. Med. 204, 1335-1347 (2007).
55. T. Sekiya, M. Miyamasu, M. Imanishi, H. Yamada, T. Nakajima, M. Yamaguchi, T. Fujisawa, R. Pawankar, Y. Sano, K. Ohta, A. Ishii, Y. Morita, K. Yamamoto, K. Matsushima, O. Yoshie, K. Hirai, Inducible expression of a Th2-Type CC chemokine thymus-And activation-regulated chemokine by human bronchial epithelial cells. J. Immunol. 165, 2205-2213 (2000).
56. G. Magri, M. Miyajima, S. Bascones, A. Mortha, I. Puga, L. Cassis, C. M. Barra, L. Comerma, A. Chudnovskiy, M. Gentile, D. Llige, M. Cols, S. Serrano, J. I. Aróstegui, M. Juan, J. Yagüe, M. Merad, S. Fagarasan, A. Cerutti, Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat. Immunol. 15, 354-364 (2014).
57. M. Merad, P. Sathe, J. Helft, J. Miller, A. Mortha, The dendritic cell lineage: Ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31, 563-604 (2013).
58. J. Ermann, T. Staton, J. N. Glickman, R. de Waal Malefyt, L. H. Glimcher, Nod/Ripk2 signaling in dendritic cells activates IL-17A-secreting innate lymphoid cells and drives colitis in T-bet-/-.Rag2-/- (TRUC) mice. Proc. Natl. Acad. Sci. U.S.A. 111, E2559-E2566 (2014).
59. 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).
60. M. M. Meredith, K. Liu, G. Darrasse-Jeze, A. O. Kamphorst, H. A. Schreiber, P. Guermonprez, J. Idoyaga, C. Cheong, K.-H. Yao, R. E. Niec, M. C. Nussenzweig, Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 209, 1153-1165 (2012).
61. A. T. Satpathy, KC Wumesh, J. C. Albring, B. T. Edelson, N. M. Kretzer, D. Bhattacharya, T. L. Murphy, K. M. Murphy, Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209, 1135-1152 (2012).
62. B. Z. Igyártó, K. Haley, D. Ortner, A. Bobr, M. Gerami-Nejad, B. T. Edelson, S. M. Zurawski, B. Malissen, G. Zurawski, J. Berman, D. H. Kaplan, Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 35, 260-272 (2011).
63. A. R. B. M. Muzaki, P. Tetlak, J. Sheng, S. C. Loh, Y. A. Setiagani, M. Poidinger, F. Zolezzi, K. Karjalainen, C. Ruedl, Intestinal CD103+CD11b- dendritic cells restrain colitis via IFN-g-induced anti-inflammatory response in epithelial cells. Mucosal Immunol. 9, 336-351 (2016).
64. X. Hao, T. S. Kim, T. J. Braciale, Differential response of respiratory dendritic cell subsets to influenza virus infection. J. Virol. 82, 4908-4919 (2008).
65. X. Roux, A. Remot, A. Petit-Camurdan, M.-A. Nahori, H. Kiefer-Biasizzo, G. Marchal, M. Lagranderie, S. Riffault, Neonatal lung immune responses show a shift of cytokines and transcription factors toward Th2 and a deficit in conventional and plasmacytoid dendritic cells. Eur. J. Immunol. 41, 2852-2861 (2011).
66. A. Mortha, A. Chudnovskiy, D. Hashimoto, M. Bogunovic, S. P. Spencer, Y. Belkaid, M. Merad, Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343, 1249288 (2014).
67. R. S. Longman, G. E. Diehl, D. A. Victorio, J. R. Huh, C. Galan, E. R. Miraldi, A. Swaminath, R. Bonneau, E. J. Scherl, D. R. Littman, CX3CR1+ mononuclear phagocytes support colitis-Associated innate lymphoid cell production of IL-22. J. Exp. Med. 211, 1571-1583 (2014).
68. Y. Belkaid, T. W. Hand, Role of the microbiota in immunity and inflammation. Cell 157, 121-141 (2014).
69. C. Taube, C. Tertilt, G. Gyülveszi, N. Dehzad, K. Kreymborg, K. Schneeweiss, E. Michel, S. Reuter, J.-C. Renauld, D. Arnold-Schild, H. Schild, R. Buhl, B. Becher, IL-22 is produced by innate lymphoid cells and limits inflammation in allergic airway disease. PLOS ONE 6, e21799 (2011).
70. L. A. Monticelli, G. F. Sonnenberg, M. C. Abt, T. Alenghat, C. G. K. Ziegler, T. A. Doering, J. M. Angelosanto, B. J. Laidlaw, C. Y. Yang, T. Sathaliyawala, M. Kubota, D. Turner, J. M. Diamond, A. W. Goldrath, D. L. Farber, R. G. Collman, E. J. Wherry, D. Artis, Innate lymphoid cells promote lung-Tissue homeostasis after infection with influenza virus. Nat. Immunol. 12, 1045-1054 (2011).
71. H. Y. Kim, H. J. Lee, Y.-J. Chang, M. Pichavant, S. A. Shore, K. A. Fitzgerald, Y. Iwakura, E. Israel, K. Bolger, J. Faul, R. H. DeKruyff, D. T. Umetsu, Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-Associated airway hyperreactivity. Nat. Med. 20, 54-61 (2014).
72. F. M. Collier, M. L. K. Tang, D. Martino, R. Saffery, J. Carlin, K. Jachno, S. Ranganathan, D. Burgner, K. J. Allen, P. Vuillermin, A.-L. Ponsonby, The ontogeny of naïve and regulatory CD4+ T-cell subsets during the first postnatal year: A cohort study. Clin. Transl. Immunol. 4, e34 (2015).
73. J. P. Ridge, E. J. Fuchs, P. Matzinger, Neonatal tolerance revisited: Turning on newborn T cells with dendritic cells. Science 271, 1723-1726 (1996).
74. N. Satoh-Takayama, S. Lesjean-Pottier, P. Vieira, S. Sawa, G. Eberl, C. A. J. Vosshenrich, J. P. Di Santo, IL-7 and IL-15 independently program the differentiation of intestinal CD3-NKp46+ cell subsets from Id2-dependent precursors. J. Exp. Med. 207, 273-280 (2010).
75. S. L. Sanos, V. L. Bui, A. Mortha, K. Oberle, C. Heners, C. Johner, A. Diefenbach, RORgt and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat. Immunol. 10, 83-91 (2009).
76. D. Bouskra, C. Brézillon, M. Bérard, C. Werts, R. Varona, I. G. Boneca, G. Eberl, Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456, 507-510 (2008).
77. J. S. Lee, M. Cella, K. G. McDonald, C. Garlanda, G. D. Kennedy, M. Nukaya, A. Mantovani, R. Kopan, C. A. Bradfield, R. D. Newberry, M. Colonna, AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 13, 144-151 (2012).
78. G. Gasteiger, X. Fan, S. Dikiy, S. Y. Lee, A. Y. Rudensky, Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science 350, 981-985 (2015).
79. Y. Nie, J. Waite, F. Brewer, M.-J. Sunshine, D. R. Littman, Y.-R. Zou, The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J. Exp. Med. 200, 1145-1156 (2004).
80. C. L. Scott, A. M. Aumeunier, A. M. Mowat, Intestinal CD103+ dendritic cells: Master regulators of tolerance? Trends Immunol. 32, 412-419 (2011).
81. L. G. Stensballe, J. Simonsen, S. M. Jensen, K. Bønnelykke, H. Bisgaard, Use of antibiotics during pregnancy increases the risk of asthma in early childhood. J. Pediatr. 162, 832-838.e3 (2013).
82. G. Pluschke, S. Pelkonen, Host factors in the resistance of newborn mice to K1 Escherichia coli infection. Microb. Pathog. 4, 93-102 (1988).
83. S. M. Atif, S. Uematsu, S. Akira, S. J. McSorley, CD103-CD11b+ dendritic cells regulate the sensitivity of CD4 T-cell responses to bacterial flagellin. Mucosal Immunol. 7, 68-77 (2014).
84. J. H. Campbell, C. M. Foster, T. Vishnivetskaya, A. G. Campbell, Z. K. Yang, A. Wymore, A. V. Palumbo, E. J. Chesler, M. Podar, Host genetic and environmental effects on mouse intestinal microbiota. ISME J. 6, 2033-2044 (2012).
85. K. K. Barfod, M. Roggenbuck, L. H. Hansen, S. Schjørring, S. T. Larsen, S. J. Sørensen, K. A. Krogfelt, The murine lung microbiome in relation to the intestinal and vaginal bacterial communities. BMC Microbiol. 13, 303 (2013).
86. D. A. Hill, C. Hoffmann, M. C. Abt, Y. Du, D. Kobuley, T. J. Kirn, F. D. Bushman, D. Artis, Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol. 3, 148-158 (2010).
87. S. J. Salter, M. J. Cox, E. M. Turek, S. T. Calus, W. O. Cookson, M. F. Moffatt, P. Turner, J. Parkhill, N. J. Loman, A. W. Walker, Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 12, 87 (2014).
88. J. G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, G. A. Huttley, S. T. Kelley, D. Knights, J. E. Koenig, R. E. Ley, C. A. Lozupone, D. McDonald, B. D. Muegge, M. Pirrung, J. Reeder, J. R. Sevinsky, P. J. Turnbaugh, W. A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld, R. Knight, QIIME allows analysis of high-Throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
89. N. Salomonis, C. R. Schlieve, L. Pereira, C. Wahlquist, A. Colas, A. C. Zambon, K. Vranizan, M. J. Spindler, A. R. Pico, M. S. Cline, T. A. Clark, A. Williams, J. E. Blume, E. Samal, M. Mercola, B. J. Merrill, B. R. Conklin, Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proc. Natl. Acad. Sci. U.S.A. 107, 10514-10519 (2010).
90. J. Bocsi, S. Melzer, I. Dähnert, A. Tárnok, OMIP-023: 10-color, 13 antibody panel for in-depth phenotyping of human peripheral blood leukocytes. Cytometry A 85, 781-784 (2014).
91. T. J. Scriba, B. Kalsdorf, D.-A. Abrahams, F. Isaacs, J. Hofmeister, G. Black, H. Y. Hassan, R. J. Wilkinson, G. Walzl, S. J. Gelderbloem, H. Mahomed, G. D. Hussey, W. A. Hanekom, Distinct, specific IL-17-And IL-22-producing CD4+ T cell subsets contribute to the human anti-mycobacterial immune response. J. Immunol. 180, 1962-1970 (2008).