Neonatal lung immune responses show a shift of cytokines and transcription factors toward Th2 and a deficit in conventional and plasmacytoid dendritic cells

European Journal of Immunology

Volumn 41, Issue 10, 2011, Pages 2852-2861

  Roux, Xavier ^a,b   Remot, Aude ^a,b   Petit Camurdan, Agnès ^a   Nahori, Marie Anne ^b   Kiefer Biasizzo, Hélène ^b   Marchal, Gilles ^b   Lagranderie, Micheline ^b   Riffault, Sabine ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

DCs; Lung; Neonates; Th2

Indexed keywords

B7 ANTIGEN; BCG VACCINE; CD103 ANTIGEN; CD11B ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CD8 ANTIGEN; CD86 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 5; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COUNT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EXPLANT; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INCIDENCE; LUNG; LYMPH NODE; MOUSE; NEWBORN; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT INFECTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD; ANTIGENS, CD11B; ANTIGENS, CD3; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; GATA3 TRANSCRIPTION FACTOR; INTEGRIN ALPHA CHAINS; LUNG; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MICE; MICE, INBRED BALB C; MYCOBACTERIUM BOVIS; TH2 CELLS; TRANSCRIPTION FACTORS;

EID: 80053164804     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201041224     Document Type: Article

References (39)

1. Benguigui, Y., Lopez-Antunano, F., Schmunis, G. and Yunes, J., Respiratory infections in children. Pan American Health Organization Washington DC 1999.
2. Zaghouani, H., Hoeman, C. M. and Adkins, B., Neonatal immunity: faulty T-helpers and the shortcomings of dendritic cells. Trends Immunol. 2009. 30: 585-591.
3. Adkins, B., Bu, Y. and Guevara, P., Murine neonatal CD4+ lymph node cells are highly deficient in the development of antigen-specific Th1 function in adoptive adult hosts. J. Immunol. 2002. 169: 4998-5004.
4. Rose, S., Lichtenheld, M., Foote, M. R. and Adkins, B., Murine neonatal CD4+cells are poised for rapid Th2 effector-like function. J. Immunol. 2007. 178: 2667-2678.
5. Lee, H. H., Hoeman, C. M., Hardaway, J. C., Guloglu, F. B., Ellis, J. S., Jain, R., Divekar, R. et al., Delayed maturation of an IL-12-producing dendritic cell subset explains the early Th2 bias in neonatal immunity. J Exp Med 2008. 205: 2269-2280.
6. Ridge, J. P., Fuchs, E. J. and Matzinger, P., Neonatal tolerance revisited: turning on newborn T cells with dendritic cells. Science 1996. 271: 1723-1726.
7. Kovarik, J., Bozzotti, P., Love-Homan, L., Pihlgren, M., Davis, H. L., Lambert, P. H., Krieg, A. M. and Siegrist, C. A., CpG oligodeoxynucleotides can circumvent the Th2 polarization of neonatal responses to vaccines but may fail to fully redirect Th2 responses established by neonatal priming. J. Immunol. 1999. 162: 1611-1617.
8. Zhu, J. and Paul, W. E., CD4 T cells: fates, functions, and faults. Blood 2008. 112: 1557-1569.
9. Nelson, D. J., McMenamin, C., McWilliam, A. S., Brenan, M. and Holt, P. G., Development of the airway intraepithelial dendritic cell network in the rat from class II major histocompatibility (Ia)-negative precursors: differential regulation of Ia expression at different levels of the respiratory tract. J. Exp. Med. 1994. 179: 203-212.
10. Smit, J. J., Lindell, D. M., Boon, L., Kool, M., Lambrecht, B. N. and Lukacs, N. W., The balance between plasmacytoid DC versus conventional DC determines pulmonary immunity to virus infections. PLoS One 2008. 3: e1720.
11. de Heer, H. J., Hammad, H., Soullie, T., Hijdra, D., Vos, N., Willart, M. A., Hoogsteden, H. C. and Lambrecht, B. N., Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 2004. 200: 89-98.
12. Edelson, B. T., Kc, W., Juang, R., Kohyama, M., Benoit, L. A., Klekotka, P. A., Moon, C. et al., Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J. Exp. Med. 2010. 207: 823-836.
13. Geissmann, F., Manz, M. G., Jung, S., Sieweke, M. H., Merad, M. and Ley, K., Development of monocytes, macrophages, and dendritic cells. Science 2010. 327: 656-661.
14. Lagranderie, M., Nahori, M. A., Balazuc, A. M., Kiefer-Biasizzo, H., Lapa e Silva, J. R., Milon, G., Marchal, G. and Vargaftig, B. B., Dendritic cells recruited to the lung shortly after intranasal delivery of Mycobacterium bovis BCG drive the primary immune response towards a type 1 cytokine production. Immunology 2003. 108: 352-364.
15. Ginhoux, F., Liu, K., Helft, J., Bogunovic, M., Greter, M., Hashimoto, D., Price, J. et al., The origin and development of nonlymphoid tissue CD103+DCs. J. Exp. Med. 2009. 206: 3115-3130.
16. Forster, R., Davalos-Misslitz, A. C. and Rot, A., CCR7 and its ligands: balancing immunity and tolerance. Nat. Rev. Immunol. 2008. 8: 362-371.
17. Jiao, X., Lo-Man, R., Guermonprez, P., Fiette, L., Deriaud, E., Burgaud, S., Gicquel, B. et al., Dendritic cells are host cells for mycobacteria in vivo that trigger innate and acquired immunity. J. Immunol. 2002. 168: 1294-1301.
18. Abolhassani, M., Lagranderie, M., Caminshi, I., Romain, F., Balazuc, A. M., Wagner, M. C., Tanguy, M. et al., Similar functional activity of dendritic cells recruited to the mesenteric lymph nodes of newborn and adult mice after the rectal delivery of Mycobacterium bovis BCG. Microbes Infect. 2006. 8: 2341-2351.
19. Dadaglio, G., Sun, C. M., Lo-Man, R., Siegrist, C. A. and Leclerc, C., Efficient in vivo priming of specific cytotoxic T cell responses by neonatal dendritic cells. J. Immunol. 2002. 168: 2219-2224.
20. Dodd, J., Riffault, S., Kodituwakku, J. S., Hayday, A. C. and Openshaw, P. J., Pulmonary V gamma 4+ gamma delta T cells have proinflammatory and antiviral effects in viral lung disease. J. Immunol. 2009. 182: 1174-1181.
21. Chang, Y. J., Kim, H. Y., Albacker, L. A., Lee, H. H., Baumgarth, N., Akira, S., Savage, P. B. et al., Influenza infection in suckling mice expands an NKT cell subset that protects against airway hyperreactivity. J. Clin. Invest. 2011. 121: 57-69.
22. Thomson, C. W., Lee, B. P. and Zhang, L., Double-negative regulatory T cells: non-conventional regulators. Immunol. Res. 2006. 35: 163-178.
23. Voelkl, S., Gary, R. and Mackensen, A., Characterization of the immunoregulatory function of human TCR-alphabeta+ CD4- CD8- double-negative T cells. Eur. J. Immunol. 2011. 41: 739-748.
24. Wang, Y. H., Voo, K. S., Liu, B., Chen, C. Y., Uygungil, B., Spoede, W., Bernstein, J. A. et al., A novel subset of CD4(+) T(H)2 memory/effector cells that produce inflammatory IL-17 cytokine and promote the exacerbation of chronic allergic asthma. J. Exp. Med. 2010. 207: 2479-2491.
25. Sun, C. M., Fiette, L., Tanguy, M., Leclerc, C. and Lo-Man, R., Ontogeny and innate properties of neonatal dendritic cells. Blood 2003. 102: 585-591.
26. Seth, S., Oberdorfer, L., Hyde, R., Hoff, K., Thies, V., Worbs, T., Schmitz, S. and Forster, R., CCR7 essentially contributes to the homing of plasmacytoid dendritic cells to lymph nodes under steady-state as well as inflammatory conditions. J. Immunol. 2011. 186: 3364-3372.
27. Smit, J. J., Rudd, B. D. and Lukacs, N. W., Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J. Exp. Med. 2006. 203: 1153-1159.
28. You, D., Ripple, M., Balakrishna, S., Troxclair, D., Sandquist, D., Ding, L., Ahlert, T. A. and Cormier, S. A., Inchoate CD8+ T cell responses in neonatal mice permit influenza-induced persistent pulmonary dysfunction. J. Immunol. 2008. 181: 3486-3494.
29. Vollstedt, S., Franchini, M., Hefti, H. P., Odermatt, B., O'Keeffe, M., Alber, G., Glanzmann, B. et al., Flt3 ligand-treated neonatal mice have increased innate immunity against intracellular pathogens and efficiently control virus infections. J. Exp. Med. 2003. 197: 575-584.
30. Vollstedt, S., O'Keeffe, M., Odermatt, B., Beat, R., Glanzmann, B., Riesen, M., Shortman, K. and Suter, M., Treatment of neonatal mice with Flt3 ligand leads to changes in dendritic cell subpopulations associated with enhanced IL-12 and IFN-alpha production. Eur. J. Immunol. 2004. 34: 1849-1860.
31. Peng, Y., Latchman, Y. and Elkon, K. B., Ly6C(low) monocytes differentiate into dendritic cells and cross-tolerize T cells through PDL-1. J. Immunol. 2009. 182: 2777-2785.
32. Jakubzick, C., Tacke, F., Ginhoux, F., Wagers, A. J., van Rooijen, N., Mack, M., Merad, M. and Randolph, G. J., Blood monocyte subsets differentially give rise to CD103+and CD103- pulmonary dendritic cell populations. J. Immunol. 2008. 180: 3019-3027.
33. Brombacher, F., Kastelein, R. A. and Alber, G., Novel IL-12 family members shed light on the orchestration of Th1 responses. Trends Immunol. 2003. 24: 207-212.
34. Vekemans, J., Amedei, A., Ota, M. O., D'Elios, M. M., Goetghebuer, T., Ismaili, J., Newport, M. J. et al., Neonatal bacillus Calmette-Guerin vaccination induces adult-like IFN-gamma production by CD4+T lymphocytes. Eur J. Immunol. 2001. 31: 1531-1535.
35. Culley, F. J., Pollott, J. and Openshaw, P. J., Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J. Exp. Med. 2002. 196: 1381-1386.
36. Tregoning, J. S., Yamaguchi, Y., Wang, B., Mihm, D., Harker, J. A., Bushell, E. S., Zheng, M. et al., Genetic susceptibility to the delayed sequelae of neonatal respiratory syncytial virus infection is MHC dependent. J. Immunol. 2010. 185: 5384-5391.
37. Ripple, M. J., You, D., Honnegowda, S., Giaimo, J. D., Sewell, A. B., Becnel, D. M. and Cormier, S. A., Immunomodulation with IL-4R alpha antisense oligonucleotide prevents respiratory syncytial virus-mediated pulmonary disease. J. Immunol. 2010. 185: 4804-4811.
38. Gheorghiu, M., Lagrange, P. H., Lagranderie, M. and Balazuc, A. M., The effects of dispersed or surface grown cultures, manufacture and control methods on BCG standardization. Dev. Biol. Stand. 1986. 58: 191-205.
39. Lagranderie, M., Abolhassani, M., Vanoirbeek, J. A., Lima, C., Balazuc, A. M., Vargaftig, B. B. and Marchal, G., Mycobacterium bovis bacillus Calmette-Guerin killed by extended freeze-drying targets plasmacytoid dendritic cells to regulate lung inflammation. J. Immunol. 2010. 184: 1062-1070.