Alveolar macrophages contribute to respiratory tolerance by inducing FoxP3 expression in naive T cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 48, Issue 6, 2013, Pages 773-780

  Coleman, Michelle M ^a,b   Ruane, Darren ^a   Moran, Barry ^a   Dunne, Pádraic J ^b   Keane, Joseph ^b   Mills, Kingston H G ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ST JAMES S HOSPITAL   (Ireland)

Author keywords

Alveolar macrophages; FoxP3; Retinoic acid; TGF 1

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN E; INTERLEUKIN 10; OVALBUMIN; RECEPTOR BLOCKING AGENT; RETINOIC ACID; RETINOIC ACID RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE;

AEROSOL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BORDETELLA PERTUSSIS; CD4+ T LYMPHOCYTE; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MOUSE; NONHUMAN; NORMAL HUMAN; PERTUSSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; VACCINATION; ANIMAL; BAGG ALBINO MOUSE; CELL COUNT; CELL CULTURE; DRUG ANTAGONISM; GENETICS; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; LUNG; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PROTEIN BINDING;

ADMINISTRATION, INTRANASAL; ANIMALS; BORDETELLA PERTUSSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL COUNT; CELLS, CULTURED; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNE TOLERANCE; LUNG; LYMPHOCYTE ACTIVATION; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED BALB C; OVALBUMIN; PROTEIN BINDING; RECEPTORS, RETINOIC ACID; TRANSFORMING GROWTH FACTOR BETA1; VACCINATION;

MLCS; MLOWN;

EID: 84881018661     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2012-0263OC     Document Type: Article

References (49)

1. Medoff BD, Thomas SY, Banerji A, Wain JC, Zhang H, Lilly CM, Ginns LC, LusterAD. Pathogenic T-cell recruitment into the airway in human disease. Ann N Y Acad Sci 2005;1062: 220-241.
2. Holt PG. Regulation of antigen-presenting cell function(s) in lung and airway tissues. Eur Respir J 1993;6: 120-129.
3. Holt PG. Pulmonary dendritic cell populations. Adv Exp Med Biol 1993; 329: 557-562.
4. Wilsher ML, Hughes DA, Haslam PL. Immunoregulatory properties of pulmonary surfactant: effect of lung lining fluid on proliferation of human blood lymphocytes. Thorax 1988;43: 354-359.
5. Paine R, 3rd, Chavis A, Gaposchkin D, Christensen P, Mody CH, Turka LA, Toews GB. A factor secreted by a human pulmonary alveolar epithelial-like cell line blocks T-cell proliferation between G1 and S phase. Am J Respir Cell Mol Biol 1992;6: 658-666.
6. Strickland D, Kees UR, Holt PG. Regulation of T-cell activation in the lung: alveolar macrophages induce reversible T-cell anergy in vitro associated with inhibition of interleukin-2 receptor signal transduction. Immunology 1996;87: 250-258.
7. Ettensohn DB, Lalor PA, Roberts NJ Jr. Human alveolar macrophage regulation of lymphocyte proliferation. Am Rev Respir Dis 1986;133: 1091-1096.
8. McCombs CC, Michalski JP, Westerfield BT, Light RW. Human alveolar macrophages suppress the proliferative response of peripheral blood lymphocytes. Chest 1982;82: 266-271.
9. Rich EA, Cooper C, Toossi Z, Leonard ML, Stucky RM, Wiblin RT, Ellner JJ. Requirement for cell-to-cell contact for the immunosuppressive activity of human alveolar macrophages. Am J Respir Cell Mol Biol 1991;4: 287-294.
10. Schauble TL, Boom WH, Finegan CK, Rich EA. Characterization of suppressor function of human alveolar macrophages for T lymphocyte responses to phytohemagglutinin: cellular selectivity, reversibility, and early events in T cell activation. Am J Respir Cell Mol Biol 1993;8: 89-97.
11. Toews GB, Vial WC, Dunn MM, Guzzetta P, Nunez G, Stastny P, Lipscomb MF. The accessory cell function of human alveolar macrophages in specific T cell proliferation. J Immunol 1984;132: 181-186.
12. Upham JW, Strickland DH, Bilyk N, Robinson BW, Holt PG. Alveolar macrophages from humans and rodents selectively inhibit T-cell proliferation but permit T-cell activation and cytokine secretion. Immunology 1995;84: 142-147.
13. Upham JW, Strickland DH, Robinson BW, Holt PG. Selective inhibition of T cell proliferation but not expression of effector function by human alveolar macrophages. Thorax 1997;52: 786-795.
14. Rola-Pleszczynski M, Lemaire I. Leukotrienes augment interleukin 1 production by human monocytes. J Immunol 1985;135: 3958-3961.
15. Moore SA, Strieter RM, Rolfe MW, Standiford TJ, Burdick MD, Kunkel SL. Expression and regulation of human alveolar macrophage-derived interleukin-1 receptor antagonist. Am J Respir Cell Mol Biol 1992;6: 569-575.
16. Schwartz RH. Acquisition of immunologic self-tolerance. Cell 1989;57: 1073-1081.
17. Holt PG, Strickland DH, Wikstrom ME, Jahnsen FL. Regulation of immunological homeostasis in the respiratory tract. Nat Rev Immunol 2008;8: 142-152.
18. Strickland D, Kees UR, Holt PG. Regulation of T-cell activation in the lung: isolated lung T cells exhibit surface phenotypic characteristics of recent activation including down-modulated T-cell receptors, but are locked into the G0/G1 phase of the cell cycle. Immunology 1996;87: 242-249.
19. Holt PG, Kees UR, Shon-Hegrad MA, Rose A, Ford J, Bilyk N, Bowman R, Robinson BW. Limiting-dilution analysis of T cells extracted from solid human lung tissue: comparison of precursor frequencies for proliferative responses and lymphokine production between lung and blood T cells from individual donors. Immunology 1988;64: 649-654.
20. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic selftolerance maintained by activated T cells expressing IL-2 receptor alphachains (CD25): breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995;155: 1151-1164.
21. Hafler DA, Kent SC, Pietrusewicz MJ, Khoury SJ, Weiner HL, Fukaura H. Oral administration of myelin induces antigen-specific TGF-beta 1 secreting T cells in patients with multiple sclerosis. Ann N Y Acad Sci 1997;835: 120-131.
22. McGuirk P, McCann C, Mills KH. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper Type 1 responses by Bordetella pertussis. J Exp Med 2002;195: 221-231.
23. Ono M, Shimizu J, Miyachi Y, Sakaguchi S. Control of autoimmune myocarditis and multiorgan inflammation by glucocorticoid-induced TNF receptor family-related protein(high), FoxP3-expressing CD251 and CD252 regulatory T cells. J Immunol 2006;176: 4748-4756.
24. Patel DD. Escape from tolerance in the human X-linked autoimmunity-allergic disregulation syndrome and the Scurfy mouse. J Clin Invest 2001;107: 155-157.
25. Fontenot JD, Gavin MA, Rudensky AY. FoxP3 programs the development and function of CD41CD251 regulatory T cells. Nat Immunol 2003;4: 330-336.
26. Fontenot JD, Rasmussen JP,Williams LM, Dooley JL, Farr AG, Rudensky AY. Regulatory T cell lineage specification by the Forkhead transcription factor FoxP3. Immunity 2005;22: 329-341.
27. Coleman MM, Finlay CM, Moran B, Keane J, Dunne PJ, Mills KH. The immunoregulatory role of CD4(1) FoxP3(1) CD25(2) regulatory T cells in lungs of mice infected with Bordetella pertussis. FEMS Immunol Med Microbiol 2012;64: 413-424.
28. Benson MJ, Pino-Lagos K, Rosemblatt M, Noelle RJ. All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J Exp Med 2007; 204: 1765-1774.
29. Mucida D, Park Y, Kim G, Turovskaya O, Scott I, Kronenberg M, Cheroutre H. Reciprocal Th17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007;317: 256-260.
30. Thornton AM, Shevach EM. CD41CD251 immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 1998;188: 287-296.
31. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, Belkaid Y, Powrie F. A functionally specialized population of mucosal CD1031 DCs induces FoxP31 regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J ExpMed 2007;204: 1757-1764.
32. Manicassamy S, Pulendran B. Retinoic acid-dependent regulation of immune responses by dendritic cells and macrophages. Semin Immunol 2009;21: 22-27.
33. van Halteren AG, van der Cammen MJ, Cooper D, Savelkoul HF, Kraal G, Holt PG. Regulation of antigen-specific IgE, IgG1, and mast cell responses to ingested allergen by mucosal tolerance induction. J Immunol 1997;159: 3009-3015.
34. Garside P, Steel M, Liew FY, Mowat AM. CD41 but not CD81 T cells are required for the induction of oral tolerance. Int Immunol 1995;7: 501-504.
35. Hoyne GF, Askonas BA, Hetzel C, Thomas WR, Lamb Jr. A.Regulation of house dust mite responses by intranasally administered peptide: transient activation of CD41 T cells precedes the development of tolerance in vivo. Int Immunol 1996;8: 335-342.
36. McMenamin C, Pimm C, McKersey M, Holt PG. Regulation of IgE responses to inhaled antigen in mice by antigen-specific gamma delta T cells. Science 1994;265: 1869-1871.
37. Thepen T, McMenamin C,Oliver J, KraalG,Holt PG. Regulation of immune response to inhaled antigen by alveolar macrophages: differential effects of in vivo alveolar macrophage elimination on the induction of tolerance vs. immunity. Eur J Immunol 1991;21: 2845-2850.
38. Strickland DH, Thepen T, Kees UR, Kraal G, Holt PG. Regulation of T-cell function in lung tissue by pulmonary alveolar macrophages. Immunology 1993;80: 266-372.
39. McGuirk P, Mahon BP, Griffin F, Mills KH. Compartmentalization of T cell responses following respiratory infection with Bordetella pertussis: hyporesponsiveness of lung T cells is associated with modulated expression of the co-stimulatory molecule CD28. Eur J Immunol 1998;28: 153-163.
40. Jaensson E, Uronen-Hansson H, Pabst O, Eksteen B, Tian J, Coombes JL, Berg PL, Davidsson T, Powrie F, Johansson-Lindbom B, et al. Small intestinal CD1031 dendritic cells display unique functional properties that are conserved between mice and humans. J Exp Med 2008;205: 2139-2149.
41. Manicassamy S, Ravindran R, Deng J, Oluoch H, Denning TL, Kasturi SP, Rosenthal KM, Evavold BD, Pulendran B. Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat Med 2009; 15: 401-409.
42. Wang G, Zhong A, Wang S, Dong N, Sun Z, Xia J. Retinoic acid attenuates acute heart rejection by increasing regulatory T cell and repressing differentiation of Th17 cell in the presence of TGF-beta. Transplant Int 2010;23: 986-997.
43. Nichol KL, Mendelman PM, Mallon KP, Jackson LA, Gorse GJ, Belshe RB, Glezen WP, Wittes J. Effectiveness of live, attenuated intranasal influenza virus vaccine in healthy, working adults: a randomized controlled trial. JAMA 1999;282: 137-144.
44. Petukhova G, Naikhin A, Chirkova T, Donina S, Korenkov D, Rudenko L. Comparative studies of local antibody and cellular immune responses to influenza infection and vaccination with live attenuated reassortant influenza vaccine (LAIV) utilizing a mouse nasal-associated lymphoid tissue (NALT) separation method. Vaccine 2009;27: 2580-2587.
45. Chen L, Wang J, Zganiacz A, Xing Z. Single intranasal mucosal Mycobacterium bovis BCG vaccination confers improved protection compared to subcutaneous vaccination against pulmonary tuberculosis. Infect Immun 2004;72: 238-246.
46. Klavinskis LS, Barnfield C, Gao L, Parker S. Intranasal immunization with plasmid DNA-lipid complexes elicits mucosal immunity in the female genital and rectal tracts. J Immunol 1999;162: 254-262.
47. Snapper CM, Paul WE. Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 1987; 236: 944-947.
48. Hind M, Corcoran J, Maden M. Alveolar proliferation, retinoid synthesizing enzymes, and endogenous retinoids in the postnatal mouse lung: different roles for ALDH-1 and RALDH-2. Am J Respir CellMol Biol 2002;26: 67-73.
49. Thepen T, McMenamin C, Girn B, Kraal G, Holt PG. Regulation of IgE production in pre-sensitized animals: in vivo elimination of alveolar macrophages preferentially increases IgE responses to inhaled allergen. Clin Exp Allergy 1992;22: 1107-1114.