Fms-like tyrosine kinase 3 ligand decreases T helper type 17 cells and suppressors of cytokine signaling proteins in the lung of house dust mite-sensitized and -challenged mice

American Journal of Respiratory Cell and Molecular Biology

Volumn 43, Issue 5, 2010, Pages 520-529

  McGee, Halvor S ^a   Stallworth, Arthur L ^a   Agrawal, Tanupriya ^a   Shao, Zhifei ^a   Lorence, Lindsey ^a   Agrawal, Devendra K ^a  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Airway hyperresponsiveness; House dust mite; Retinoic acid related orphan receptor t; Suppressors of cytokine signaling; T helper cell type 17

Indexed keywords

FLT3 LIGAND; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; METHACHOLINE; RETINOIC ACID RECEPTOR GAMMA; SUPPRESSOR OF CYTOKINE SIGNALING; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; SUPPRESSOR OF CYTOKINE SIGNALING 5; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CD4 ANTIGEN; CYTOKINE; FLT3 LIGAND PROTEIN; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN RECEPTOR; MEMBRANE PROTEIN; METHACHOLINE CHLORIDE; RETINOID RELATED ORPHAN RECEPTOR GAMMA;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DERMATOPHAGOIDES FARINAE; DERMATOPHAGOIDES PTERONYSSINUS; DRUG EFFECT; EOSINOPHIL; FEMALE; GENE EXPRESSION; LUNG LAVAGE; LYMPHOCYTE COUNT; MOUSE; NEUTROPHIL; NONHUMAN; PROTEIN EXPRESSION; RESPIRATORY TRACT ALLERGY; SENSITIZATION; TH17 CELL; TH2 CELL; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BRONCHUS HYPERREACTIVITY; CELL COUNT; CELL SEPARATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HELPER CELL; IMMUNIZATION; IMMUNOLOGY; LUNG; METABOLISM; PARASITOLOGY; PATHOLOGY; PYROGLYPHIDAE;

MUS; PYROGLYPHIDAE;

ANIMALS; ANTIGENS, CD4; BRONCHIAL HYPERREACTIVITY; BRONCHOALVEOLAR LAVAGE FLUID; CELL COUNT; CELL SEPARATION; CYTOKINES; GENE EXPRESSION REGULATION; IMMUNIZATION; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LUNG; MEMBRANE PROTEINS; METHACHOLINE CHLORIDE; MICE; MICE, INBRED BALB C; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; PYROGLYPHIDAE; RECEPTORS, INTERLEUKIN; RNA, MESSENGER; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; T-LYMPHOCYTES, HELPER-INDUCER; TH2 CELLS;

EID: 78149343572     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2009-0241OC     Document Type: Article

References (70)

1. Boulet LP. Irreversible airway obstruction in asthma. Curr Allergy Asthma Rep 2009;9:168-173.
2. Meurs H, Gosens R, Zaagsma J. Airway hyperresponsiveness in asthma: lessons from in vitro model systems and animal models. Eur Respir J 2008;32:487-502.
3. Fischer R, Tome D, McGhee JR, Boyaka PN. Th1 and Th2 cells are required for both eosinophil- and neutrophil-associated airway inflammatory responses in mice. Biochem Biophys Res Commun 2007;357:44-49. (Pubitemid 46574498)
4. Hamid QA, Cameron LA. Recruitment of T cells to the lung in response to antigen challenge. J Allergy Clin Immunol 2000;106:S227-S234.
5. Hartenstein B, Teurich S, Hess J, Schenkel J, Schorpp-Kistner M, Angel P. Th2 cell-specific cytokine expression and allergen-induced airway inflammation depend on JunB. EMBO J 2002;21:6321-6329. (Pubitemid 35448410)
6. Zhu J, Paul WE. CD4 T cells: fates, functions, and faults. Blood 2008;112:1557-1569.
7. Awasthi A, Murugaiyan G, Kuchroo VK. Interplay between effector Th17 and regulatory T cells. J Clin Immunol 2008;28:660-670.
8. Lehar SM, Bevan MJ. Immunology: polarizing a T-cell response. Nature 2004;430:150-151.
9. Taylor JJ, Krawczyk CM, Mohrs M, Pearce EJ. Th2 cell hyporesponsiveness during chronic murine schistosomiasis is cell intrinsic and linked to GRAIL expression. J Clin Invest 2009;119:1019-1028.
10. Weaver CT. Th17: the ascent of a new effector T-cell subset. Preface. Eur J Immunol 2009;39:634-636.
11. Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008;28:454-467. (Pubitemid 351471762)
12. McAllister F, Henry A, Kreindler JL, Dubin PJ, Ulrich L, Steele C, Finder JD, Pilewski JM, Carreno BM, Goldman SJ, et al. Role of IL- 17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J Immunol 2005;175:404-412. (Pubitemid 40884344)
13. Al-Ramli W, Prefontaine D, Chouiali F, Martin JG, Olivenstein R, Lemiere C, Hamid QT. (H)17-associated cytokines (IL-17A and IL-17F) in severe asthma. J Allergy Clin Immunol 2009;123:1185-1187.
14. Nistala K, Wedderburn LR. Th17 and regulatory T cells: rebalancing pro- and anti-inflammatory forces in autoimmune arthritis. Rheumatology (Oxford) 2009;48:602-606.
15. Cooke A. Th17 cells in inflammatory conditions. Rev Diabet Stud 2006;3:72-75.
16. Gamelli RL, He LK, Liu H. Recombinant human granulocyte colony-stimulating factor treatment improves macrophage suppression of granulocyte and macrophage growth after burn and burn wound infection. J Trauma 1995;39:1141-1146, discussion 1146-1147. (Pubitemid 26003951)
17. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001;194:519-527.
18. Huang W, Na L, Fidel PL, Schwarzenberger P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 2004;190:624-631. (Pubitemid 38982105)
19. Oukka M. Th17 cells in immunity and autoimmunity. Ann Rheum Dis 2008;67:iii26-iii29.
20. Louten J, Boniface K, de Waal Malefyt R. Development and function of TH17 cells in health and disease. J Allergy Clin Immunol 2009;123:1004-1011.
21. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B, Asher TE, Scheinberg P, Price DA, Hage CA, Kholi LM, et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 2008;112:2826-2835.
22. Klemann C, Raveney BJ, Klemann AK, Ozawa T, von Horsten S, Shudo K, Oki S, Yamamura T. Synthetic retinoid AM80 inhibits Th17 cells and ameliorates experimental autoimmune encephalomyelitis. Am J Pathol 2009;174:2234-2245.
23. Shahrara S, Huang Q, Mandelin AM II, Pope RM. TH-17 cells in rheumatoid arthritis. Arthritis Res Ther 2008;10:R93.
24. Emamaullee JA, Davis J, Merani S, Toso C, Elliott JF, Thiesen A, Shapiro AM. Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes 2009;58:1302-1311.
25. Di Cesare A, Di Meglio P, Nestle FO. A role for Th17 cells in the immunopathogenesis of atopic dermatitis? J Invest Dermatol 2008;128:2569-2571.
26. Falcone M, Bloom BRA. T helper cell 2 (Th2) immune response against non-self antigens modifies the cytokine profile of autoimmune T cells and protects against experimental allergic encephalomyelitis. J Exp Med 1997;185:901-907. (Pubitemid 27119874)
27. Chen CL, Lee CT, Liu YC, Wang JY, Lei HY, Yu CK. House dust mite Dermatophagoides farinae augments proinflammatory mediator productions and accessory function of alveolar macrophages: implications for allergic sensitization and inflammation. J Immunol 2003;170:528-536.
28. Chang JW, Lin CY, Chen WL, Chen CT. Higher incidence of Dermatophagoides pteronyssinus allergy in children of Taipei city than in children of rural areas. J Microbiol Immunol Infect 2006;39:316-320.
29. Huss K, Adkinson NF Jr, Eggleston PA, Dawson C, Van Natta ML, Hamilton RG. House dust mite and cockroach exposure are strong risk factors for positive allergy skin test responses in the Childhood Asthma Management Program. J Allergy Clin Immunol 2001;107:48-54. (Pubitemid 32105243)
30. Platts-Mills TA, Rakes G, Heymann PW. The relevance of allergen exposure to the development of asthma in childhood. J Allergy Clin Immunol 2000;105:S503-S508. (Pubitemid 30109016)
31. Nuhoglu Y, Ozumut SS, Ozdemir C, Ozdemir M, Nuhoglu C, Erguven M. Sublingual immunotherapy to house dust mite in pediatric patients with allergic rhinitis and asthma: a retrospective analysis of clinical course over a 3-year follow-up period. J Investig Allergol Clin Immunol 2007;17:375-378. (Pubitemid 350232561)
32. Arshad SH. Indoor allergen exposure in the development of allergy and asthma. Curr Allergy Asthma Rep 2003;3:115-120. (Pubitemid 39467924)
33. Schei MA, Hessen JO, Lund E. House-dust mites and mattresses. Allergy 2002;57:538-542.
34. Asadi A, Hedman E, Widen C, Zilliacus J, Gustafsson JA, Wikstrom AC. FMS-like tyrosine kinase 3 interacts with the glucocorticoid receptor complex and affects glucocorticoid dependent signaling. Biochem Biophys Res Commun 2008;368:569-574.
35. Namikawa R, Muench MO, Roncarolo MG. Regulatory roles of the ligand for Flk2/Flt3 tyrosine kinase receptor on human hematopoiesis. Stem Cells 1996;14:388-395. (Pubitemid 26286260)
36. Rosnet O, Marchetto S, deLapeyriere O, Birnbaum D. Murine Flt3, a gene encoding a novel tyrosine kinase receptor of the PDGFR/CSF1R family. Oncogene 1991;6:1641-1650.
37. Scheijen B, Griffin JD. Tyrosine kinase oncogenes in normal hematopoiesis and hematological disease. Oncogene 2002;21:3314-3333. (Pubitemid 34587706)
38. Lyman SD, James L, Johnson L, Brasel K, de Vries P, Escobar SS, Downey H, Splett RR, Beckmann MP, McKenna HJ. Cloning of the human homologue of the murine flt3 ligand: a growth factor for early hematopoietic progenitor cells. Blood 1994;83:2795-2801. (Pubitemid 24978048)
39. Hannum C, Culpepper J, Campbell D, McClanahan T, Zurawski S, Bazan JF, Kastelein R, Hudak S, Wagner J, Mattson J, et al. Ligand for FLT3/FLK2 receptor tyrosine kinase regulates growth of haematopoietic stem cells and is encoded by variant RNAs. Nature 1994;368:643-648.
40. Maraskovsky E, Brasel K, Teepe M, Roux ER, Lyman SD, Shortman K, McKenna HJ. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J Exp Med 1996;184:1953-1962.
41. Maraskovsky E, Daro E, Roux E, Teepe M, Maliszewski CR, Hoek J, Caron D, Lebsack ME, McKenna HJ. In vivo generation of human dendritic cell subsets by Flt3 ligand. Blood 2000;96:878-884.
42. Edwan JH, Perry G, Talmadge JE, Agrawal DK. Flt-3 ligand reverses late allergic response and airway hyper-responsiveness in a mouse model of allergic inflammation. J Immunol 2004;172:5016-5023.
43. + cells in the lung of cockroach-sensitized and challenged mice. Am J Respir Cell Mol Biol 2009;42:331-340.
44. Alexander WS, Hilton DJ. The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu Rev Immunol 2004;22:503-529.
45. Senn JJ, Klover PJ, Nowak IA, Zimmers TA, Koniaris LG, Furlanetto RW, Mooney RA. Suppressor of cytokine signaling-3 (SOCS-3), a potential mediator of interleukin-6-dependent insulin resistance in hepatocytes. J Biol Chem 2003;278:13740-13746.
46. Chen Z, Laurence A, Kanno Y, Pacher-Zavisin M, Zhu BM, Tato C, Yoshimura A, Hennighausen L, O'Shea JJ. Selective regulatory function of SOCS3 in the formation of IL-17-secreting T cells. Proc Natl Acad Sci USA 2006;103:8137-8142.
47. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity 2004;21:467-476.
48. Molet S, Hamid Q, Davoine F, Nutku E, Taha R, Page N, Olivenstein R, Elias J, Chakir J. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J Allergy Clin Immunol 2001;108:430-438.
49. Sun YC, Zhou QT, Yao WZ. Sputum interleukin-17 is increased and associated with airway neutrophilia in patients with severe asthma. Chin Med J (Engl) 2005;118:953-956.
50. Ferretti S, Bonneau O, Dubois GR, Jones CE, Trifilieff A. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J Immunol 2003;170:2106-2112.
51. + T lymphocytes in acute liver inflammation and injury after ischemia-reperfusion. Am J Physiol Gastrointest Liver Physiol 2005;289:G969-G976.
52. Miyamoto M, Prause O, Sjostrand M, Laan M, Lotvall J, Linden A. Endogenous IL-17 as a mediator of neutrophil recruitment caused by endotoxin exposure in mouse airways. J Immunol 2003;170:4665-4672.
53. Woolard MD, Hensley LL, Kawula TH, Frelinger JA. Respiratory Francisella tularensis live vaccine strain infection induces Th17 cells and prostaglandin E2, which inhibits generation of gamma interferon-positive T cells. Infect Immun 2008;76:2651-2659.
54. Fielding CA, McLoughlin RM, McLeod L, Colmont CS, Najdovska M, Grail D, Ernst M, Jones SA, Topley N, Jenkins BJ. IL-6 regulates neutrophil trafficking during acute inflammation via STAT3. J Immunol 2008;181:2189-2195.
55. Yoshimura T, Sonoda KH, Ohguro N, Ohsugi Y, Ishibashi T, Cua DJ, Kobayashi T, Yoshida H, Yoshimura A. Involvement of Th17 cells and the effect of anti-IL-6 therapy in autoimmune uveitis. Rheumatology (Oxford) 2009;48:347-354.
56. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235-238.
57. Wan H, Winton HL, Soeller C, Gruenert DC, Thompson PJ, Cannell MB, Stewart GA, Garrod DR, Robinson C. Quantitative structural and biochemical analyses of tight junction dynamics following exposure of epithelial cells to house dust mite allergen Der p 1. Clin Exp Allergy 2000;30:685-698.
58. Wan H, Winton HL, Soeller C, Tovey ER, Gruenert DC, Thompson PJ, Stewart GA, Taylor GW, Garrod DR, Cannell MB, et al. Der p 1 facilitates transepithelial allergen delivery by disruption of tight junctions. J Clin Invest 1999;104:123-133.
59. Donnelly S, Dalton JP, Loukas A. Proteases in helminth- and allergen-induced inflammatory responses. Chem Immunol Allergy 2006;90:45-64.
60. D'Andrea MR, Derian CK, Leturcq D, Baker SM, Brunmark A, Ling P, Darrow AL, Santulli RJ, Brass LF, Andrade-Gordon P. Characterization of protease-activated receptor-2 immunoreactivity in normal human tissues. J Histochem Cytochem 1998;46:157-164.
61. Kauffman HF, Tamm M, Timmerman JA, Borger P. House dust mite major allergens Der p 1 and Der p 5 activate human airway-derived epithelial cells by protease-dependent and protease-independent mechanisms. Clin Mol Allergy 2006;4:5.
62. Gordon JR. TGFbeta1 and TNFalpha secreted by mast cells stimulated via the FcepsilonRI activate fibroblasts for high-level production of monocyte chemoattractant protein-1 (MCP-1). Cell Immunol 2000;201:42-49.
63. Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S, Menon S, Seymour B, Jackson C, Kung TT, et al. New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J Immunol 2002;169:443-453.
64. Fasshauer M, Kralisch S, Klier M, Lossner U, Bluher M, Klein J, Paschke R. Insulin resistance-inducing cytokines differentially regulate SOCS mRNA expression via growth factor- and Jak/Stat-signaling pathways in 3T3-L1 adipocytes. J Endocrinol 2004;181:129-138.
65. Neuwirt H, Puhr M, Cavarretta I, Mitterberger M, Hobisch A, Culig Z. Suppressor of cytokine signalling is up-regulated by androgen in prostate cancer cell lines and inhibits androgen mediated proliferation and secretion. Endocrine-Related Cancer 2007;14:1007-1019. (Pubitemid 351252432)
66. Yoshimura A, Naka T, Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol 2007;7:454-465. (Pubitemid 46834848)
67. Kubo M, Inoue H. Suppressor of cytokine signaling 3 (SOCS3) in Th2 cells evokes Th2 cytokines, IgE, and eosinophilia. Curr Allergy Asthma Rep 2006;6:32-39.
68. Kinjyo I, Inoue H, Ohishi M, Hamano S, Fukuyama S, Yoshimura T, Koga K, Takakis H, Himeno K, Takaesu G, et al. Loss of SOCS3 in T helper cells resulted in reduced immune responses and hyperproduction of interleukin 10 and transforming growth factor-β 1. J Exp Med 2006;203:1021-1031.
69. Sonderegger I, Iezzi G, Maier R, Schmitz N, Kurrer M, Kopf M. GM-CSF mediates autoimmunity by enhancing IL-6-dependent Th17 cell development and survival. J Exp Med 2008;205:2281-2294.
70. Brender C, Columbus R, Metcalf D, Handman E, Starr R, Huntington N, Tarlinton D, Odum N, Nicholson SE, Nicola NA, et al. SOCS5 is expressed in primary B and T lymphoid cells but is dispensable for lymphocyte production and function. Mol Cell Biol 2004;24:6094-6103. (Pubitemid 38787992)