Mouse respiratory tract dendritic cell subsets and the immunological fate of inhaled antigens

Immunology and Cell Biology

Volumn 85, Issue 3, 2007, Pages 182-188

  Wikstrom, Matthew E ^a,c   Stumbles, Philip A ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b MURDOCH UNIVERSITY   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Airway; Antigen; Dendritic cell; Lung; Mouse

Indexed keywords

ANTIGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; B LYMPHOCYTE; BAGG ALBINO MOUSE; CD4+ T LYMPHOCYTE; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; IMMUNOLOGY; IMMUNOSURVEILLANCE; LYMPH NODE; NONHUMAN; PHENOTYPE; RAT STRAIN; RESPIRATORY SYSTEM; REVIEW; RODENT; SHEEP; T LYMPHOCYTE;

ANIMALS; ANTIGENS; DENDRITIC CELLS; HUMANS; MICE; RESPIRATORY SYSTEM;

ANIMALIA; MUS; RODENTIA;

EID: 34247854952     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/sj.icb.7100039     Document Type: Review

References (69)

1. Hastings RH, Folkesson HG, Matthay MA. Mechanisms of alveolar protein clearance in the intact lung. Am J Physiol Lung Cell Mol Physiol 2004; 286: L679-L689.
2. Hiemstra PS, Bals R. Series introduction: innate host defense of the respiratory epithelium. J Leukoc Biol 2004; 75: 3-4.
3. Whitsett JA. Series introduction: Intrinsic and innate defenses in the lung: intersection of pathways regulating lung morphogenesis, host defense, and repair. J Clin Invest 2002; 109: 565-569.
4. Lohmann-Matthes ML, Steinmuller C, Franke-Ullmann G. Pulmonary macrophages. Eur Respir J 1994; 7: 1678-1689.
5. Peters-Golden M. The alveolar macrophage: the forgotten cell in asthma. Am J Respir Cell Mol Biol 2004; 31: 3-7.
6. Holt PG, Stumbles PA. Regulation of immunologic homeostasis in peripheral tissues by dendritic cells: the respiratory tract as a paradigm. J Allergy Clin Immunol 2000; 105: 421-429.
7. Vermaelen K, Pauwels R. Pulmonary dendritic cells. Am J Respir Crit Care Med 2005; 172: 530-551.
8. Holt PG, Schon-Hegrad MA, Phillips MJ, McMenamin PG. Ia-positive dendritic cells form a tightly meshed network within the human airway epithelium. Clin Exp Allergy 1989; 19: 597-601.
9. Schon-Hegrad MA, Oliver J, McMenamin PG, Holt PG. Studies on the density, distribution, and surface phenotype of intraepithelial class II major histocompatibility complex antigen (Ia)-bearing dendritic cells (DC) in the conducting airways. J Exp Med 1991; 173: 1345-1356.
10. Sertl K, Takemura T, Tschachler E, Ferrans VJ, Kaliner MA, Shevach EM. Dendritic cells with antigen-presenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. J Exp Med 1986; 163: 436-451.
11. Holt PG, Oliver J, Bilyk N, McMenamin C, McMenamin PG, Kraal G et al. Down-regulation of the antigen presenting cell function(s) of pulmonary dendritic cells in vivo by resident alveolar macrophages. J Exp Med 1993; 177: 397-407.
12. Holt PG, Schon-Hegrad MA. Localization of T cells, macrophages and dendritic cells in rat respiratory tract tissue: implications for immune function studies. Immunology 1987; 62: 349-356.
13. von Garnier C, Filgueira L, Wikstrom M, Smith M, Thomas JA, Strickland DH et al. Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract. J Immunol 2005; 175: 1609-1618.
14. Masten BJ, Lipscomb MF. Comparison of lung dendritic cells and B cells in stimulating naive antigen-specific T cells. J Immunol 1999; 162: 1310-1317.
15. Swanson KA, Zheng Y, Heidler KM, Zhang Z-D, Webb TJ, Wilkes DS. Flt3-ligand, IL-4, GM-CSF, and adherence-mediated isolation of murine lung dendritic cells: assessment of isolation technique on phenotype and function. J Immunol 2004; 173: 4875-4881.
16. Vermaelen KY, Carro-Muino I, Lambrecht BN, Pauwels RA. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J Exp Med 2001; 193: 51-60.
17. Anjuere F, Martin P, Ferrero I, Fraga ML, del Hoyo GM, Wright N et al. Definition of dendritic cell subpopulations present in the spleen, peyer's patches, lymph nodes, and skin of the mouse. Blood 1999; 93: 590-598.
18. Soos TJ, Sims TN, Barisoni L, Lin K, Littman DR, Dustin ML et al. CX3CR1+ interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney Int 2006; 70: 591.
19. Pillarisetty VG, Shah AB, Miller G, Bleier JI, DeMatteo RP. Liver dendritic cells are less immunogenic than spleen dendritic cells because of differences in subtype composition. J Immunol 2004; 172: 1009-1017.
20. Iwasaki A, Kelsall BL. Unique functions of CD11b+, CD8alpha+, and double-negative Peyer's patch dendritic cells. J Immunol 2001; 166: 4884-4890.
21. Niess JH, Brand S, Gu X, Landsman L, Jung S, McCormick BA et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005; 307: 254-258.
22. Sung SJ, Fu SM, Rose Jr CE, Gaskin F, Ju S, Beaty SR. A major lung CD103 (aE)-b7 integrin-positive epithelial dendritic cell population expressing langerin and tight junction proteins. J Immunol 2006; 176: 2161-2172.
23. Julia V, Hessel EM, Malherbe L, Glaichenhaus N, O'Garra A, Coffman RL. A restricted subset of dendritic cells captures airborne antigens and remains able to activate specific T cells long after antigen exposure. Immunity 2002; 16: 271-283.
24. Annacker O, Coombes JL, Malmstrom V, Uhlig HH, Bourne T, Johansson-Lindbom B et al. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J Exp Med 2005; 202: 1051-1061.
25. Johansson-Lindbom B, Svensson M, Pabst O, Palmqvist C, Marquez G, Forster R et al. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med 2005; 202: 1063-1073.
26. de Heer HJ, Hammad H, Soullie T, Hijdra D, Vos N, Willart MA et al. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J Exp Med 2004; 200: 89-98.
27. Smit JJ, Rudd BD, Lukacs NW. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J Exp Med 2006; 203: 1153-1159.
28. Asselin-Paturel C, Brizard G, Pin JJ, Briere F, Trinchieri G. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J Immunol 2003; 171: 6466-6477.
29. Colonna M, Trinchieri G, Liu Y-J. Plasmacytoid dendritic cells in immunity. Nat Immunol 2004; 5: 1219.
30. Byersdorfer CA, Chaplin DD. Visualization of early APC/T cell interactions in the mouse lung following intranasal challenge. J Immunol 2001; 167: 6756-6764.
31. Xia W, Pinto CE, Kradin RL. The antigen-presenting activities of Ia+ dendritic cells shift dynamically from lung to lymph node after an airway challenge with soluble antigen. J Exp Med 1995; 181: 1275-1283.
32. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001; 2: 361-367.
33. Steinman RM. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 1991; 9: 271-296.
34. + T cell activation during the primary response to airborne allergen. J Immunol 2006; 177: 913-924.
35. Southam DS, Dolovich M, O'Byrne PM, Inman MD. Distribution of intranasal instillations in mice: effects of volume, time, body position, and anesthesia. Am J Physiol Lung Cell Mol Physiol 2002; 282: L833-L839.
36. Holt PG, Haining S, Nelson DJ, Sedgwick JD. Origin and steady-state turnover of class II MHC-bearing dendritic cells in the epithelium of the conducting airways. J Immunol 1994; 153: 256-261.
37. McWilliam AS, Nelson D, Thomas JA, Holt PG. Rapid dendritic cell recruitment is a hallmark of the acute inflammatory response at mucosal surfaces. J Exp Med 1994; 179: 1331-1336.
38. Hammad H, de Heer HJ, Soullie T, Hoogsteden HC, Trottein F, Lambrecht BN. Prostaglandin D2 inhibits airway dendritic cell migration and function in steady state conditions by selective activation of the D prostanoid receptor 1. J Immunol 2003; 171: 3936-3940.
39. Idzko M, Hammad H, van Nimwegen M, Kool M, Muller T, Soullie T et al. Local application of FTY720 to the lung abrogates experimental asthma by altering dendritic cell function. J Clin Invest 2006; 116: 2935-2944.
40. Bensch KG, Dominguez E, Liebow AA. Absorption of intact protein molecules across the pulmonary air-tissue barrier. Science 1967; 157: 1204-1206.
41. Folkesson HG, Westrom BR, Pierzynowski SG, Karlsson BW. Lung to blood passage of different-sized molecules during lung inflammation in the rat. J Appl Physiol 1991; 71: 1106-1111.
42. Hubbard RC, Casolaro MA, Mitchell M, Sellers SE, Arabia F, Matthay MA et al. Fate of aerosolized recombinant DNA-produced alpha 1-antitrypsin: use of the epithelial surface of the lower respiratory tract to administer proteins of therapeutic importance. Proc Natl Acad Sci USA 1989; 86: 680-684.
43. Meyer EC, Ottaviano R, Higgins JJ. Albumin clearance from alveoli: tissue permeation vs airway displacement. J Appl Physiol 1977; 43: 487-497.
44. Belz GT, Smith CM, Kleinert L, Reading P, Brooks A, Shortman K et al. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc Natl Acad Sci USA 2004; 101: 8670-8675.
45. Itano AA, Jenkins MC. Antigen presentation to naive CD4 T cells in the lymph node. Nat Immunol 2003; 4: 733-739.
46. Itano AA, McSorley SJ, Reinhardt RL, Ehst BD, Ingulli E, Rudensky AY et al. Distinct dendritic cell populations sequentially present antigen to CD4T cells and stimulate different aspects of cell-mediated immunity. Immunity 2003; 19: 47-57.
47. Shortman K, Liu Y-J. Mouse and human dendritic cell subtypes. Nat Immunol 2002; 2: 151-161.
48. Vermaelen K, Pauwels R. Accelerated airway dendritic cell maturation, trafficking, and elimination in a mouse model of asthma. Am J Respir Cell Mol Biol 2003; 29: 405-409.
49. Gretz JE, Norbury CC, Anderson AO, Proudfoot AE, Shaw S. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J Exp Med 2000; 192: 1425-1440.
50. Sixt M, Kanazawa N, Selg M, Samson T, Roos G, Reinhardt DP et al. The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node [see comment]. Immunity 2005; 22: 19-29.
51. Yrlid U, Cerovic V, Milling S, Jenkins CD, Zhang J, Crocker PR et al. Plasmacytoid dendritic cells do not migrate in intestinal or hepatic lymph. J Immunol 2006; 177: 6115-6121.
52. Linton P-J, Bautista B, Biederman E, Bradley ES, Harbertson J, Kondrack RM et al. Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo. J Exp Med 2003; 197: 875-883.
53. Linton P-J, Harbertson J, Bradley LM. A critical role for b cells in the development of memory CD4 cells. J Immunol 2000; 165: 5558-5565.
54. Inaba K, Turley S, Yamaide F, Iyoda T, Mahnke K, Inaba M et al. Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J Exp Med 1998; 188: 2163-2173.
55. Allan RS, Waithman J, Bedoui S, Jones CM, Villadangos JA, Zhan Y et al. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006; 25: 153-162.
56. Angeli V, Ginhoux F, Llodra J, Quemeneur L, Frenette PS, Skobe M et al. B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity 2006; 24: 203-215.
57. Thery C, Duban L, Segura E, Veron P, Lantz O, Amigorena S. Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol 2002; 3: 1156-1162.
58. Randolph GJ. Migratory dendritic cells: sometimes simply ferries? Immunity 2006; 25: 15-18.
59. Lawrence CW, Braciale TJ. Activation, differentiation, and migration of naive virus-specific CD8+ T cells during pulmonary influenza virus infection. J Immunol 2004; 173: 1209-1218.
60. Jelley-Gibbs DM, Brown DM, Dibble JP, Haynes L, Eaton SM, Swain SL. Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J Exp Med 2005; 202: 697-706.
61. Zammit DJ, Turner DL, Klonowski KD, Lefrancois L, Cauley LS. Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity 2006; 24: 439-449.
62. Cauley LS, Cookenham T, Miller TB, Adams PS, Vignali KM, Vignali DAA et al. Cutting edge: virus-specific CD4+ memory T cells in nonlymphoid tissues express a highly activated phenotype. J Immunol 2002; 169: 6655-6658.
63. Hogan RJ, Zhong W, Usherwood EJ, Cookenham T, Roberts AD, Woodland DL. Protection from respiratory virus infections can be mediated by antigen-specific CD4+ T cells that persist in the lungs. J Exp Med 2001; 193: 981-986.
64. Storni T, Ruedl C, Renner WA, Bachmann MF. Innate immunity together with duration of antigen persistence regulate effector T cell induction. J Immunol 2003; 171: 795-801.
65. Catron DM, Rusch LK, Hataye J, Itano AA, Jenkins MK. CD4+ T cells that enter the draining lymph nodes after antigen injection participate in the primary response and become central-memory cells. J Exp Med 2006; 203: 1045-1054.
66. Hammad H, de Vries VC, Maldonado-Lopez R, Moser M, Maliszewski C, Hoogsteden HC et al. Differential capacity of CD8+ alpha or CD8- alpha dendritic cell subsets to prime for eosinophilic airway inflammation in the T-helper type 2-prone milieu of the lung. Clin Exp Allergy 2004; 34: 1834-1840.
67. Maldonado-Lopez R, De Smedt T, Michel P, Godfroid J, Pajak B, Heirman C et al. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J Exp Med 1999; 189: 587-592.
68. Pulendran B, Smith JL, Caspary G, Brasel K, Pettit D, Maraskovsky E et al. Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc Natl Acad Sci USA 1999; 96: 1036-1041.
69. van Rijt LS, Jung S, Kleinjan A, Vos N, Willart M, Duez C et al. In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma. J Exp Med 2005; 201: 981-991.