Plasmacytoid dendritic cells protect from viral bronchiolitis and asthma through semaphorin 4a-mediated T reg expansion

Journal of Experimental Medicine

Volumn 215, Issue 2, 2018, Pages 537-557

  Lynch, Jason P ^a,c,d,k   Werder, Rhiannon B ^a,k   Loh, Zhixuan ^a   Sikder, Md Al Amin ^a,k   Curren, Bodie ^a,k   Zhang, Vivian ^a,k   Rogers, Matthew J ^a   Lane, Katie ^a   Simpson, Jennifer ^a,k   Mazzone, Stuart B ^a,e   Spann, Kirsten ^b   Hayball, John ^f,g   Diener, Kerrilyn ^f,g   Everard, Mark L ^h   Blyth, Christopher C ^h,i,j   Forstner, Christian ^a   Dennis, Paul G ^a   Murtaza, Nida ^a   Morrison, Mark ^a   Cuív, Páraic Ó ^a   Zhang, Ping ^k   Haque, Ashraful ^a,k   Hill, Geoffrey R ^a,k   Sly, Peter D ^a   Upham, John W ^a   Phipps, Simon ^a,k   more..

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^g UNIVERSITY OF ADELAIDE   (Australia)

^h UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

ⁱ PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

^j UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^k QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; AMPICILLIN; CD11B ANTIGEN; CD4 ANTIGEN; CD45RA ANTIGEN; EOTAXIN 2; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 25; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; METRONIDAZOLE; NEOMYCIN; NEUROPILIN 1; PROPIONIC ACID; SEMAPHORIN; SEMAPHORIN 4A; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; VANCOMYCIN; ALPHA BETA INTERFERON RECEPTOR; IFNAR1 PROTEIN, MOUSE; IL10 PROTEIN, MOUSE; SEMA4A PROTEIN, MOUSE; VOLATILE FATTY ACID;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC THERAPY; ARTICLE; ASTHMA; CELL EXPANSION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DISEASE SEVERITY; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOPATHOLOGY; INTERFERON PRODUCTION; MALE; MICROBIAL COLONIZATION; MICROBIOME; MOUSE; NEWBORN; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PNEUMOVIRUS INFECTION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REINFECTION; VIRAL BRONCHIOLITIS; VIRUS LOAD; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; CHILD; COMPLICATION; CYTOLOGY; DENDRITIC CELL; DISEASE MODEL; FEMALE; HUMAN; IMMUNOLOGY; METABOLISM; MICROFLORA; PRESCHOOL CHILD; RESPIRATORY SYNCYTIAL VIRUS INFECTION; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; ASTHMA; BRONCHIOLITIS, VIRAL; CHILD; CHILD, PRESCHOOL; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FATTY ACIDS, VOLATILE; FEMALE; HUMANS; INTERLEUKIN-10; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROBIOTA; RECEPTOR, INTERFERON ALPHA-BETA; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; SEMAPHORINS; T-LYMPHOCYTES, REGULATORY;

EID: 85041423642     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20170298     Document Type: Article

References (65)

1. Abrahamsson, T.R., H.E. Jakobsson, A.F. Andersson, B. Bjorksten, L. Engstrand, and M.C. Jenmalm. 2014. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin. Exp. Allergy. 44:842-850. https ://doi. org /10. 1111 /cea. 12253
2. Arpaia, N., C. Campbell, X. Fan, S. Dikiy, J. van der Veeken, P. deRoos, H. Liu, J.R. Cross, K. Pfeffer, P.J. Coffer, and A.Y. Rudensky. 2013. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 504:451-455. https ://doi. org /10. 1038 /nature12726
3. Arrieta, M.-C., L.T. Stiemsma, P.A. Dimitriu, L. Thorson, S. Russell, S. Yurist-Doutsch, B. Kuzeljevic, M.J. Gold, H.M. Britton, D.L. Lefebvre, et al. 2015. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 7:307ra152. https ://doi. org /10. 1126 /scitranslmed. aab2271
4. Bendelja, K., A. Gagro, A. Bace, R. Lokar-Kolbas, V. Kršulovic-Hrešic, V. Drazenovic, G. Mlinaric-Galinovic, and S. Rabatic. 2000. Predominant type-2 response in infants with respiratory syncytial virus (RSV) infection demonstrated by cytokine flow cytometry. Clin. Exp. Immunol. 121:332-338. https ://doi. org /10. 1046 /j. 1365-2249. 2000. 01297. x
5. Blyth, C.C., P. Jacoby, P.V. Effler, H. Kelly, D.W. Smith, C. Robins, G.A. Willis, A. Levy, A.D. Keil, and P.C. Richmond. WAI VE Study Team. 2014. Effectiveness of trivalent flu vaccine in healthy young children. Pediatrics. 133:e1218-e1225. https ://doi. org /10. 1542 /peds. 2013-3707
6. Blyth, C.C., P. Jacoby, P.V. Effler, H. Kelly, D.W. Smith, M.L. Borland, G.A. Willis, A. Levy, A.D. Keil, and P.C. Richmond. WAI VE Study Team. 2016. Influenza vaccine effectiveness and uptake in children at risk of severe disease. Pediatr. Infect. Dis. J. 35:309-315. https ://doi. org /10. 1097 /INF. 0000000000000999
7. Caballero, M.T., M.E. Serra, P.L. Acosta, J. Marzec, L. Gibbons, M. Salim, A. Rodriguez, A. Reynaldi, A. Garcia, D. Bado, et al. 2015. TLR4 genotype and environmental LPS mediate RSV bronchiolitis through Th2 polarization. J. Clin. Invest. 125:571-582. https ://doi. org /10. 1172 /JCI75183
8. Christiaansen, A.F., M.A. Syed, P.P. Ten Eyck, S.M. Hartwig, L. Durairaj, S.S. Kamath, and S.M. Varga. 2016. Altered Treg and cytokine responses in RSV-infected infants. Pediatr. Res. 80:702-709. https ://doi. org /10. 1038 /pr. 2016. 130
9. Davidson, S., G. Kaiko, Z. Loh, A. Lalwani, V. Zhang, K. Spann, S.Y. Foo, N. Hansbro, S. Uematsu, S. Akira, et al. 2011. Plasmacytoid dendritic cells promote host defense against acute pneumovirus infection via the TLR7-MyD88-dependent signaling pathway. J. Immunol. 186:5938-5948. https ://doi. org /10. 4049 /jimmunol. 1002635
10. de Heer, H.J., H. Hammad, T. Soullié, D. Hijdra, N. Vos, M.A. Willart, H.C. Hoogsteden, and B.N. Lambrecht. 2004. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 200:89-98. https ://doi. org /10. 1084 /jem. 20040035
11. Delgoffe, G.M., S.R. Woo, M.E. Turnis, D.M. Gravano, C. Guy, A.E. Overacre, M.L. Bettini, P. Vogel, D. Finkelstein, J. Bonnevier, et al. 2013. Stability and function of regulatory T cells is maintained by a neuropilin-1-semaphorin-4a axis. Nature. 501:252-256. https ://doi. org /10. 1038 / nature12428
12. Edwards, C.L., V. Zhang, R.B. Werder, S.E. Best, I. Sebina, K.R. James, R.J. Faleiro, F. de Labastida Rivera, F.H. Amante, C.R. Engwerda, et al. 2015. Coinfection with blood-stage plasmodium promotes systemic type I interferon production during pneumovirus infection but impairs inflammation and viral control in the lung. Clin. Vaccine Immunol. 22:477-483. https ://doi. org /10. 1128 /CVI. 00051-15
13. Feldman, A.S., Y. He, M.L. Moore, M.B. Hershenson, and T.V. Hartert. 2015. Toward primary prevention of asthma. Reviewing the evidence for early-life respiratory viral infections as modifiable risk factors to prevent childhood asthma. Am. J. Respir. Crit. Care Med. 191:34-44. https ://doi. org /10. 1164 /rccm. 201405-0901PP
14. Furusawa, Y., Y. Obata, S. Fukuda, T.A. Endo, G. Nakato, D. Takahashi, Y. Nakanishi, C. Uetake, K. Kato, T. Kato, et al. 2013. Commensal microbederived butyrate induces the differentiation of colonic regulatory T cells. Nature. 504:446-450. https ://doi. org /10. 1038 /nature12721
15. Gollwitzer, E.S., S. Saglani, A. Trompette, K. Yadava, R. Sherburn, K.D. McCoy, L.P. Nicod, C.M. Lloyd, and B.J. Marsland. 2014. Lung microbiota promotes tolerance to allergens in neonates via PD-L1. Nat. Med. 20:642-647. https ://doi. org /10. 1038 /nm. 3568
16. Greenberg, A.E., L.S. Clescerl, and A.D. Eaton, editors. 1992. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC
17. Guerrero-Plata, A., A. Casola, G. Suarez, X. Yu, L. Spetch, M.E. Peeples, and R.P. Garofalo. 2006. Differential response of dendritic cells to human metapneumovirus and respiratory syncytial virus. Am. J. Respir. Cell Mol. Biol. 34:320-329. https ://doi. org /10. 1165 /rcmb. 2005-0287OC
18. Hall, C.B. 2001. Respiratory syncytial virus and parainfluenza virus. N. Engl. J. Med. 344:1917-1928. https ://doi. org /10. 1056 / NEJM200106213442507
19. Herbst, T., A. Sichelstiel, C. Schär, K. Yadava, K. Bürki, J. Cahenzli, K. McCoy, B.J. Marsland, and N.L. Harris. 2011. Dysregulation of allergic airway inflammation in the absence of microbial colonization. Am. J. Respir. Crit. Care Med. 184:198-205. https ://doi. org /10. 1164 /rccm. 201010-1574OC
20. Hill, D.A., M.C. Siracusa, M.C. Abt, B.S. Kim, D. Kobuley, M. Kubo, T. Kambayashi, D.F. Larosa, E.D. Renner, J.S. Orange, et al. 2012. Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat. Med. 18:538-546. https ://doi. org /10. 1038 /nm. 2657
21. Hooper, L.V., D.R. Littman, and A.J. Macpherson. 2012. Interactions between the microbiota and the immune system. Science. 336:1268-1273. https :// doi. org /10. 1126 /science. 1223490
22. Hornung, V., J. Schlender, M. Guenthner-Biller, S. Rothenfusser, S. Endres, K.K. Conzelmann, and G. Hartmann. 2004. Replication-dependent potent IFN-alpha induction in human plasmacytoid dendritic cells by a single-stranded RNA virus. J. Immunol. 173:5935-5943. https ://doi. org /10. 4049 /jimmunol. 173. 10. 5935
23. Huang, Y., L. Guo, J. Qiu, X. Chen, J. Hu-Li, U. Siebenlist, P.R. Williamson, J.F. Urban Jr., and W.E. Paul. 2015. IL-25-responsive, lineage-negative KLRG1(hi) cells are multipotential 'inflammatory' type 2 innate lymphoid cells. Nat. Immunol. 16:161-169. https ://doi. org /10. 1038 /ni. 3078
24. James, K.M., T. Gebretsadik, G.J. Escobar, P. Wu, K.N. Carroll, S.X. Li, E.M. Walsh, E.F. Mitchel, C. Sloan, and T.V. Hartert. 2013. Risk of childhood asthma following infant bronchiolitis during the respiratory syncytial virus season. J. Allergy Clin. Immunol. 132:227-229. https ://doi. org /10. 1016 /j. jaci. 2013. 01. 009
25. Johnson, J.E., R.A. Gonzales, S.J. Olson, P.F. Wright, and B.S. Graham. 2007. The histopathology of fatal untreated human respiratory syncytial virus infection. Mod. Pathol. 20:108-119. https ://doi. org /10. 1038 /modpathol. 3800725
26. Kaiko, G.E., Z. Loh, K. Spann, J.P. Lynch, A. Lalwani, Z. Zheng, S. Davidson, S. Uematsu, S. Akira, J. Hayball, et al. 2013. Toll-like receptor 7 gene deficiency and early-life Pneumovirus infection interact to predispose toward the development of asthma-like pathology in mice. J. Allergy Clin. Immunol. 131:1331-9.e10. https ://doi. org /10. 1016 /j. jaci. 2013. 02. 041
27. Kamanaka, M., S.T. Kim, Y.Y. Wan, F.S. Sutterwala, M. Lara-Tejero, J.E. Galán, E. Harhaj, and R.A. Flavell. 2006. Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity. 25:941-952. https ://doi. org /10. 1016 /j. immuni. 2006. 09. 013
28. Krishnamoorthy, N., A. Khare, T.B. Oriss, M. Raundhal, C. Morse, M. Yarlagadda, S.E. Wenzel, M.L. Moore, R.S. Peebles Jr., A. Ray, and P. Ray. 2012. Early infection with respiratory syncytial virus impairs regulatory T cell function and increases susceptibility to allergic asthma. Nat. Med. 18:1525-1530. https ://doi. org /10. 1038 /nm. 2896
29. Lin, W., N. Truong, W.J. Grossman, D. Haribhai, C.B. Williams, J. Wang, M.G. Martín, and T.A. Chatila. 2005. Allergic dysregulation and hyperimmunoglobulinemia E in Foxp3 mutant mice. J. Allergy Clin. Immunol. 116:1106-1115. https ://doi. org /10. 1016 /j. jaci. 2005. 08. 046
30. Lynch, J.P., S.B. Mazzone, M.J. Rogers, J.J. Arikkatt, Z. Loh, A.L. Pritchard, J.W. Upham, and S. Phipps. 2014. The plasmacytoid dendritic cell: at the cross-roads in asthma. Eur. Respir. J. 43:264-275. https ://doi. org /10. 1183 /09031936. 00203412
31. Mansbach, J.M., K. Hasegawa, D.M. Henke, N.J. Ajami, J.F. Petrosino, C.A. Shaw, P.A. Piedra, A.F. Sullivan, J.A. Espinola, and C.A. Camargo Jr. 2016. Respiratory syncytial virus and rhinovirus severe bronchiolitis are associated with distinct nasopharyngeal microbiota. J. Allergy Clin. Immunol. 137:1909-1913.e4. https ://doi. org /10. 1016 /j. jaci. 2016. 01. 036
32. Marsland, B.J., and E.S. Gollwitzer. 2014. Host-microorganism interactions in lung diseases. Nat. Rev. Immunol. 14:827-835. https ://doi. org /10. 1038 / nri3769
33. Martín-Gayo, E., E. Sierra-Filardi, A.L. Corbí, and M.L. Toribio. 2010. Plasmacytoid dendritic cells resident in human thymus drive natural Treg cell development. Blood. 115:5366-5375. https ://doi. org /10. 1182 /blood-2009-10-248260
34. Møller-Larsen, S., M. Nyegaard, A. Haagerup, J. Vestbo, T.A. Kruse, and A.D. Børglum. 2008. Association analysis identifies TLR7 and TLR8 as novel risk genes in asthma and related disorders. Thorax. 63:1064-1069. https ://doi. org /10. 1136 /thx. 2007. 094128
35. Moon, C., M.T. Baldridge, M.A. Wallace, C.A. D, H.W. Burnham, Virgin, and T.S. Stappenbeck. 2015. Vertically transmitted faecal IgA levels determine extra-chromosomal phenotypic variation. Nature. 521:90-93. https :// doi. org /10. 1038 /nature14139
36. Nair, H., D.J. Nokes, B.D. Gessner, M. Dherani, S.A. Madhi, R.J. Singleton, K.L. O'Brien, A. Roca, P.F. Wright, N. Bruce, et al. 2010. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: A systematic review and meta-analysis. Lancet. 375:1545-1555. https ://doi. org /10. 1016 /S0140-6736(10)60206-1
37. Palomares, O., B. Ruckert, T. Jartti, U.C. Kucuksezer, T. Puhakka, E. Gomez, H.B. Fahrner, A. Speiser, A. Jung, W.W. Kwok, et al. 2012. Induction and maintenance of allergen-specific FOXP3+ Treg cells in human tonsils as potential first-line organs of oral tolerance. J. Allergy Clin. Immunol. 129:510-520.e9. https ://doi. org /10. 1016 /j. jaci. 2011. 09. 031
38. Pantoja-Feliciano, I.G., J.C. Clemente, E.K. Costello, M.E. Perez, M.J. Blaser, R. Knight, and M.G. Dominguez-Bello. 2013. Biphasic assembly of the murine intestinal microbiota during early development. ISME J. 7:1112-1115. https ://doi. org /10. 1038 /ismej. 2013. 15
39. Phipps, S., C.E. Lam, G.E. Kaiko, S.Y. Foo, A. Collison, J. Mattes, J. Barry, S. Davidson, K. Oreo, L. Smith, et al. 2009. Toll/IL-1 signaling is critical for house dust mite-specific helper Th1 and Th2 responses. Am. J. Respir. Crit. Care Med. 179:883-893. https ://doi. org /10. 1164 /rccm. 200806-974OC
40. Planer, J.D., Y. Peng, A.L. Kau, L.V. Blanton, I.M. Ndao, P.I. Tarr, B.B. Warner, and J.I. Gordon. 2016. Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice. Nature. 534:263-266
41. Plantinga, M., M. Guilliams, M. Vanheerswynghels, K. Deswarte, F. Branco-Madeira, W. Toussaint, L. Vanhoutte, K. Neyt, N. Killeen, B. Malissen, et al. 2013. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity. 38:322-335. https ://doi. org /10. 1016 /j. immuni. 2012. 10. 016
42. Pritchard, A.L., M.L. Carroll, J.G. Burel, O.J. White, S. Phipps, and J.W. Upham. 2012. Innate IFNs and plasmacytoid dendritic cells constrain Th2 cytokine responses to rhinovirus: A regulatory mechanism with relevance to asthma. J. Immunol. 188:5898-5905. https ://doi. org /10. 4049 /jimmunol. 1103507
43. Raiden, S., J. Pandolfi, F. Payasliàn, M. Anderson, N. Rivarola, F. Ferrero, M. Urtasun, L. Fainboim, J. Geffner, and L. Arruvito. 2014. Depletion of circulating regulatory T cells during severe respiratory syncytial virus infection in young children. Am. J. Respir. Crit. Care Med. 189:865-868. https ://doi. org /10. 1164 /rccm. 201311-1977LE
44. Roponen, M., S.T. Yerkovich, E. Hollams, P.D. Sly, P.G. Holt, and J.W. Upham. 2010. Toll-like receptor 7 function is reduced in adolescents with asthma. Eur. Respir. J. 35:64-71. https ://doi. org /10. 1183 /09031936. 00172008
45. Rosas-Salazar, C., M.H. Shilts, A. Tovchigrechko, J.D. Chappell, E.K. Larkin, K.E. Nelson, M.L. Moore, L.J. Anderson, S.R. Das, and T.V. Hartert. 2016. Nasopharyngeal microbiome in respiratory syncytial virus resembles profile associated with increased childhood asthma risk. Am. J. Respir. Crit. Care Med. 193:1180-1183. https ://doi. org /10. 1164 /rccm. 201512-2350LE
46. Russell, S.L., M.J. Gold, M. Hartmann, B.P. Willing, L. Thorson, M. Wlodarska, N. Gill, M.R. Blanchet, W.W. Mohn, K.M. McNagny, and B.B. Finlay. 2012. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 13:440-447. https ://doi. org /10. 1038 /embor. 2012. 32
47. Schijf, M.A., M.V. Lukens, D. Kruijsen, N.O.P. van Uden, J. Garssen, F.E.J. Coenjaerts, B. Van't Land, and G.M. van Bleek. 2013. Respiratory syncytial virus induced type I IFN production by pDC is regulated by RSV-infected airway epithelial cells, RSV-exposed monocytes and virus specific antibodies. PLoS One. 8:e81695. https ://doi. org /10. 1371 /journal. pone. 0081695
48. Schlender, J., V. Hornung, S. Finke, M. Günthner-Biller, S. Marozin, K. Brzózka, S. Moghim, S. Endres, G. Hartmann, and K.K. Conzelmann. 2005. Inhibition of Toll-like receptor 7-and 9-mediated alpha/ beta interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. J. Virol. 79:5507-5515. https ://doi. org /10. 1128 /JVI. 79. 9. 5507-5515. 2005
49. Sharma, M.D., B. Baban, P. Chandler, D.Y. Hou, N. Singh, H. Yagita, M. Azuma, B.R. Blazar, A.L. Mellor, and D.H. Munn. 2007. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J. Clin. Invest. 117:2570-2582. https ://doi. org /10. 1172 /JCI31911
50. Sheppard, P., W. Kindsvogel, W. Xu, K. Henderson, S. Schlutsmeyer, T.E. Whitmore, R. Kuestner, U. Garrigues, C. Birks, J. Roraback, et al. 2003. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 4:63-68. https ://doi. org /10. 1038 /ni873
51. Silver, E., H. Yin-DeClue, K.B. Schechtman, M.H. Grayson, L.B. Bacharier, and M. Castro. 2009. Lower levels of plasmacytoid dendritic cells in peripheral blood are associated with a diagnosis of asthma 6 yr after severe respiratory syncytial virus bronchiolitis. Pediatr. Allergy Immunol. 20:471-476. https ://doi. org /10. 1111 /j. 1399-3038. 2008. 00818. x
52. Smit, J.J., B.D. Rudd, and N.W. Lukacs. 2006. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J. Exp. Med. 203:1153-1159. https ://doi. org /10. 1084 /jem. 20052359
53. Swiecki, M., and M. Colonna. 2015. The multifaceted biology of plasmacytoid dendritic cells. Nat. Rev. Immunol. 15:471-485. https ://doi. org /10. 1038 /nri3865
54. Swiecki, M., S. Gilfillan, W. Vermi, Y. Wang, and M. Colonna. 2010. Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8(+) T cell accrual. Immunity. 33:955-966. https ://doi. org /10. 1016 /j. immuni. 2010. 11. 020
55. Tao, R., E.F. de Zoeten, E. Ozkaynak, C. Chen, L. Wang, P.M. Porrett, B. Li, L.A. Turka, E.N. Olson, M.I. Greene, et al. 2007. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat. Med. 13:1299-1307. https ://doi. org /10. 1038 /nm1652
56. Tarbell, K.V., L. Petit, X. Zuo, P. Toy, X. Luo, A. Mqadmi, H. Yang, M. Suthanthiran, S. Mojsov, and R.M. Steinman. 2007. Dendritic cell-expanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J. Exp. Med. 204:191-201. https ://doi. org /10. 1084 /jem. 20061631
57. Teo, S.M., D. Mok, K. Pham, M. Kusel, M. Serralha, N. Troy, B.J. Holt, B.J. Hales, M.L. Walker, E. Hollams, et al. 2015. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe. 17:704-715. https ://doi. org /10. 1016 /j. chom. 2015. 03. 008
58. Trompette, A., E.S. Gollwitzer, K. Yadava, A.K. Sichelstiel, N. Sprenger, C. Ngom-Bru, C. Blanchard, T. Junt, L.P. Nicod, N.L. Harris, and B.J. Marsland. 2014. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20:159-166. https ://doi. org /10. 1038 /nm. 3444
59. Upham, J.W., G. Zhang, A. Rate, S.T. Yerkovich, M. Kusel, P.D. Sly, and P.G. Holt. 2009. Plasmacytoid dendritic cells during infancy are inversely associated with childhood respiratory tract infections and wheezing. J. Allergy Clin. Immunol. 124:707-13.e2. https ://doi. org /10. 1016 /j. jaci. 2009. 07. 009
60. Wang, H., N. Peters, and J. Schwarze. 2006. Plasmacytoid dendritic cells limit viral replication, pulmonary inflammation, and airway hyperresponsiveness in respiratory syncytial virus infection. J. Immunol. 177:6263-6270. https ://doi. org /10. 4049 /jimmunol. 177. 9. 6263
61. Weiss, J.M., A.M. Bilate, M. Gobert, Y. Ding, M.A. Curotto de Lafaille, C.N. Parkhurst, H. Xiong, J. Dolpady, A.B. Frey, M.G. Ruocco, et al. 2012. Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J. Exp. Med. 209:1723-1742. https ://doi. org /10. 1084 /jem. 20120914
62. Yadav, M., C. Louvet, D. Davini, J.M. Gardner, M. Martinez-Llordella, S. Bailey-Bucktrout, B.A. Anthony, F.M. Sverdrup, R. Head, D.J. Kuster, et al. 2012. Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J. Exp. Med. 209:1713-1722. https ://doi. org /10. 1084 /jem. 20120822
63. Yatsunenko, T., F.E. Rey, M.J. Manary, I. Trehan, M.G. Dominguez-Bello, M. Contreras, M. Magris, G. Hidalgo, R.N. Baldassano, A.P. Anokhin, et al. 2012. Human gut microbiome viewed across age and geography. Nature. 486:222-227
64. Yu, Z., and M. Morrison. 2004. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques. 36:808-812
65. Zhou, Y., L.B. Bacharier, M. Isaacson-Schmid, J. Baty, K.B. Schechtman, G. Sajol, K. Wylie, G.A. Storch, M. Castro, and A. Beigelman. 2016. Azithromycin therapy during respiratory syncytial virus bronchiolitis: Upper airway microbiome alterations and subsequent recurrent wheeze. J. Allergy Clin. Immunol. 138:1215-1219.e5. https ://doi. org /10. 1016 /j. jaci. 2016. 03. 054