Co-culture of human bronchial fibroblasts and CD4+ T cells increases Th17 cytokine signature

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Loubaki, Lionel ^a   Hadj Salem, Ikhlass ^a   Fakhfakh, Raouia ^a   Jacques, Eric ^a   Plante, Sophie ^a   Boisvert, Marc ^b   Aoudjit, Fawzi ^b   Chakir, Jamila ^a  

^a LAVAL UNIVERSITY   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR6; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 6; RETINOID RELATED ORPHAN RECEPTOR GAMMA; RETINOID RELATED ORPHAN RECEPTOR GAMMA T; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ARTICLE; BRONCHIAL FIBROBLAST; BRONCHUS; CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL INTERACTION; CELL ISOLATION; CELLULAR IMMUNITY; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOREGULATION; INFLAMMATION; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RORC GENE; TH17 CELL; WESTERN BLOTTING;

ADULT; ASTHMA; BRONCHI; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CELLULAR MICROENVIRONMENT; COCULTURE TECHNIQUES; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-17; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKINS; MALE; MIDDLE AGED; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; PHOSPHORYLATION; PRIMARY CELL CULTURE; RECEPTORS, CCR6; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

EID: 84891907114     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081983     Document Type: Article

References (45)

1. Weaver CT, Harrington LE, Mangan PR, Gavrieli M, Murphy KM (2006) Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24(6): 677-688. doi:10.1016/j.immuni.2006.06.002. PubMed: 16782025. (Pubitemid 43867371)
2. McGeachy MJ, Cua DJ (2008) Th17 cell differentiation: the long and winding road. Immunity 28(4): 445-453. doi:10.1016/j.immuni. 2008.03.001. PubMed: 18400187. (Pubitemid 351467042)
3. Molet S, Hamid Q, Davoine F, Nutku E, Taha R et al. (2001) IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J Allergy Clin Immunol 108(3): 430-438. doi:10.1067/mai.2001. 117929. PubMed: 11544464. (Pubitemid 32881066)
4. Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T et al. (2003) Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 198(12): 1951-1957. doi: 10.1084/jem. 20030896. PubMed: 14662908. (Pubitemid 38032126)
5. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B et al. (2003) Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421(6924): 744-748. doi: 10.1038/nature01355. PubMed: 12610626. (Pubitemid 36227625)
6. Zheng Y, Danilenko DM, Valdez P, Kasman I, Eastham-Anderson J et al. (2007) Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445(7128): 648-651. doi: 10.1038/nature05505. PubMed: 17187052. (Pubitemid 46232884)
7. Hashimoto T, Akiyama K, Kobayashi N, Mori A (2005) Comparison of IL-17 production by helper T cells among atopic and nonatopic asthmatics and control subjects. Int Arch Allergy Immunol 137 Suppl 1: 51-54. doi:10.1159/000085432. PubMed: 15947485. (Pubitemid 40868774)
8. Matsunaga K, Yanagisawa S, Ichikawa T, Ueshima K, Akamatsu K et al. (2006) Airway cytokine expression measured by means of protein array in exhaled breath condensate: correlation with physiologic properties in asthmatic patients. J Allergy Clin Immunol 118(1): 84-90. doi:10.1016/j.jaci.2006.04.020. PubMed: 16815142. (Pubitemid 43949586)
9. Schnyder-Candrian S, Togbe D, Couillin I, Mercier I, Brombacher F et al. (2006) Interleukin-17 is a negative regulator of established allergic asthma. J Exp Med 203(12): 2715-2725. doi:10.1084/jem.20061401. PubMed: 17101734. (Pubitemid 44833347)
10. Wilson RH, Whitehead GS, Nakano H, Free ME, Kolls JK et al. (2009) Allergic sensitization through the airway primes Th17-dependent neutrophilia and airway hyperresponsiveness. Am J Respir Crit Care Med 180(8): 720-730. doi:10.1164/rccm.200904-0573OC. PubMed: 19661246.
11. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M et al. (2002) Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17(3): 375-387. doi:10.1016/S1074-7613(02)00391-6. PubMed: 12354389. (Pubitemid 35279557)
12. Hamilton LM, Davies DE, Wilson SJ, Kimber I, Dearman RJ et al. (2001) The bronchial epithelium in asthma-much more than a passive barrier. Monaldi Arch Chest Dis 56(1): 48-54. PubMed: 11407210. (Pubitemid 32457890)
13. Plante S, Semlali A, Joubert P, Bissonnette E, Laviolette M et al. (2006) Mast cells regulate procollagen I (alpha 1) production by bronchial fibroblasts derived from subjects with asthma through IL-4/IL-4 delta 2 ratio. J Allergy Clin Immunol 117(6): 1321-1327. doi:10.1016/j.jaci. 2005.12.1349. PubMed: 16750993. (Pubitemid 43795731)
14. Egan PJ, van Nieuwenhuijze A, Campbell IK, Wicks IP (2008) Promotion of the local differentiation of murine Th17 cells by synovial macrophages during acute inflammatory arthritis. Arthritis Rheum 58(12): 3720-3729. doi:10.1002/art.24075. PubMed: 19035489.
15. Schirmer C, Klein C, von Bergen M, Simon JC, Saalbach A (2010) Human fibroblasts support the expansion of IL-17-producing T cells via up-regulation of IL-23 production by dendritic cells. Blood 116(10): 1715-1725. doi:10.1182/blood-2010-01-263509. PubMed: 20538798.
16. Smith RS, Smith TJ, Blieden TM, Phipps RP (1997) Fibroblasts as sentinel cells. Synthesis of chemokines and regulation of inflammation. Am J Pathol 151(2): 317-322. PubMed: 9250144.
17. Brouty-Boyé D, Pottin-Clémenceau C, Doucet C, Jasmin C, Azzarone B (2000) Chemokines and CD40 expression in human fibroblasts. Eur J Immunol 30: 914-919. doi:10.1002/1521-4141(200003)30:3. PubMed: 10741409. (Pubitemid 30216266)
18. Darveau ME, Jacques E, Rouabhia M, Hamid Q, Chakir J (2008) Increased T-cell survival by structural bronchial cells derived from asthmatic subjects cultured in an engineered human mucosa. J Allergy Clin Immunol 121(3): 696-699.
19. Molet S, Hamid Q, Davoine F, Nutku E, Taha R et al. (2001) IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J Allergy Clin Immunol 108: 430-438. doi:10.1067/mai.2001. 117929. PubMed: 11544464. (Pubitemid 32881066)
20. Kim KW, Cho ML, Kim HR, Ju JH, Park MK et al. (2007) Up-regulation of stromal cell-derived factor 1 (CXCL12) production in rheumatoid synovial fibroblasts through interactions with T lymphocytes: role of interleukin-17 and CD40L-CD40 interaction. Arthritis Rheum 56(4): 1076-1086. doi:10.1002/art.22439. PubMed: 17393416.
21. Loubaki L, Semlali A, Boisvert M, Jacques E, Plante S et al. (2010) Crosstalk between T cells and bronchial fibroblasts obtained from asthmatic subjects involves CD40L/alpha 5 beta 1 interaction. Mol Immunol 47(11-12): 2112-2118. doi:10.1016/j.molimm.2010.03.011. PubMed: 20471683.
22. Gardner RM, Hankinson JL (1988) Standardization of spirometry-1987 ATS update (American Thoracic Society). J Occup Med 30(3): 272-273. PubMed: 3361365.
23. Chakir J, Pagé N, Hamid Q, Laviolette M, Boulet LP et al. (2001) Bronchial mucosa produced by tissue engineering: a new tool to study cellular interactions in asthma. J Allergy Clin Immunol 107(1): 36-40. doi:10.1067/mai.2001.111929. PubMed: 11149988. (Pubitemid 32105241)
24. Chakir J, Laviolette M, Boutet M, Laliberté R, Dubé J et al. (1996) Lower airways remodeling in nonasthmatic subjects with allergic rhinitis. Lab Invest 75(5): 735-744. PubMed: 8941218. (Pubitemid 26392803)
25. Dubé J, Chakir J, Laviolette M, Saint MS, Boutet M et al. (1998) In vitro procollagen synthesis and proliferative phenotype of bronchial fibroblasts from normal and asthmatic subjects. Lab Invest 78(3): 297-307. PubMed: 9520943. (Pubitemid 28128893)
26. Loubaki L, Semlali A, Boisvert M, Jacques E, Plante S et al. (2010) Crosstalk between T cells and bronchial fibroblasts obtained from asthmatic subjects involves CD40L/alpha 5 beta 1 interaction. Mol Immunol 47(11-12): 2112-2118. doi:10.1016/j.molimm.2010.03.011. PubMed: 20471683.
27. Zhang K, Phan SH (1996) Cytokines and pulmonary fibrosis. Biol Signals 5(4): 232-239. doi:10.1159/000109195. PubMed: 8891199. (Pubitemid 26325353)
28. Vancheri C, Mastruzzo C, Tomaselli V, Sortino MA, D'Amico L et al. (2001) Normal human lung fibroblasts differently modulate interleukin-10 and interleukin-12 production by monocytes: implications for an altered immune response in pulmonary chronic inflammation. Am J Respir Cell Mol Biol 25(5): 592-599. doi:10.1165/ajrcmb.25.5.4609. PubMed: 11713101. (Pubitemid 33087110)
29. Pap T, Müller-Ladner U, Gay RE, Gay S (2000) Fibroblast biology. Role of synovial fibroblasts in the pathogenesis of rheumatoid arthritis. Arthritis Res 2(5): 361-367. doi:10.1186/ar113. PubMed: 11094449. (Pubitemid 32223765)
30. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB et al. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441(7090): 235-238. doi:10.1038/nature04753. PubMed: 16648838.
31. Zhou L, Lopes JE, Chong MM, Ivanov II, Min R et al. (2008) TGF-betainduced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 453(7192): 236-240. doi:10.1038/nature06878. PubMed: 18368049. (Pubitemid 351667978)
32. McGeachy MJ, Chen Y, Tato CM, Laurence A, Joyce-Shaikh B et al. (2009) The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol 10(3): 314-324. doi:10.1038/ni.1698. PubMed: 19182808.
33. Korn T, Bettelli E, Gao W, Awasthi A, Jäger A et al. (2007) IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448(7152): 484-487. doi:10.1038/nature05970. PubMed: 17581588. (Pubitemid 47123515)
34. Yang L, Anderson DE, Baecher-Allan C, Hastings WD, Bettelli E et al. (2008) IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 454(7202): 350-352. doi:10.1038/nature07021. PubMed: 18469800.
35. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A et al. (2006) The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126(6): 1121-1133. doi:10.1016/j.cell.2006.07.035. PubMed: 16990136. (Pubitemid 44380299)
36. Harris TJ, Grosso JF, Yen HR, Xin H, Kortylewski M et al. (2007) Cutting edge: An in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J Immunol 179(7): 4313-4317. PubMed: 17878325.
37. Yang XO, Panopoulos AD, Nurieva R, Chang SH, Wang D et al. (2007) STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 282(13): 9358-9363. doi:10.1074/jbc.C600321200. PubMed: 17277312. (Pubitemid 47104613)
38. Buckley CD, Pilling D, Lord JM, Akbar AN, Scheel-Toellner D et al. (2001) Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation. Trends Immunol 22(4): 199-204. doi:10.1016/S1471-4906(01)01863-4. PubMed: 11274925. (Pubitemid 32673659)
39. Parsonage G, Falciani F, Burman A, Filer A, Ross E et al. (2003) Global gene expression profiles in fibroblasts from synovial, skin and lymphoid tissue reveals distinct cytokine and chemokine expression patterns. Thromb Haemost 90(4): 688-697. PubMed: 14515190. (Pubitemid 37287637)
40. Gabay C (2006) Interleukin-6 and chronic inflammation. Arthritis Res Ther 8 Suppl 2: S3. doi:10.1186/ar1851. PubMed: 16899107.
41. Kolb M, Margetts PJ, Anthony DC, Pitossi F, Gauldie J (2001) Transient expression of IL-1beta induces acute lung injury and chronic repair leading to pulmonary fibrosis. J Clin Invest 107(12): 1529-1536. doi:10.1172/JCI12568. PubMed: 11413160. (Pubitemid 32574639)
42. Lappalainen U, Whitsett JA, Wert SE, Tichelaar JW, Bry K (2005) Interleukin-1beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung. Am J Respir Cell Mol Biol 32(4): 311-318. doi:10.1165/rcmb.2004-0309OC. PubMed: 15668323. (Pubitemid 40478306)
43. Oppmann B, Lesley R, Blom B, Timans JC, Xu Y et al. (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13(5): 715-725. doi:10.1016/S1074-7613(00)00070-4. PubMed: 11114383.
44. Boniface K, Bak-Jensen KS, Li Y, Blumenschein WM, McGeachy MJ et al. (2009) Prostaglandin E2 regulates Th17 cell differentiation and function through cyclic AMP and EP2/EP4 receptor signaling. J Exp Med 206(3): 535-548. doi:10.1084/jem.20082293. PubMed: 19273625.
45. Chizzolini C, Chicheportiche R, Alvarez M, de Rham C, Roux-Lombard P et al. (2008) Prostaglandin E2 synergistically with interleukin-23 favors human Th17 expansion. Blood 112(9): 3696-3703. doi:10.1182/blood-2008-05-155408. PubMed: 18698005.