Cytokines (interleukin-9, IL-17, IL-22, IL-25 and IL-33) and asthma

Authors
Rahim Farahani 1
Roya Sherkat 2
Mazdak Ganjalikhani Hakemi 3
Nahid Eskandari 1
Reza Yazdani 4
1 Department of Immunology, Faculty of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran
2 Aquired Immunodeficiency Research Center, Infectious Disease Research Center, Isfahan University of Medical Sciences, Isfahan, Iran
3 Cellular and Molecular Immunology Research Center, Isfahan University of Medical Sciences, Isfahan, Iran
4 Department of Immunology, Faculty of Medicine; Applied Physiology Research Center, Isfahan University of Medical Sciences, Isfahan, Iran
Abstract
Asthma is a reversible airway obstruction that is characterized by constriction of airway smooth muscle, hyper secretion of mucus, edema and airway hyper responsiveness (AHR), mucus secretion and thickening of the basement membrane underlying the airway epithelium. During the process of airway inflammation, complex interactions of innate and adaptive immune cells as well as structural cells and their cytokines have many important roles. It was believed that airway inflammation is orchestrated by allergen specific T helper (Th) 2 cells, which recruit and accumulate in the lungs and produce a range of different effector cytokines. However, more recent studies have revealed the potential collaboration of other helper T cells and their cytokines in this process. Th17 cell may have a role in severe asthma and chronic obstructive pulmonary disease (COPD). Interleukin (IL)-9-producing subset called Th9 cell, Th22 cells which primarily secrete IL-22, IL-13 and tumor necrosis factor-α and Th25 cells via producing IL-25 are believed to be important for initiating allergic reactions and developing airway inflammation. Cytokines are important in asthma and play a critical role in orchestrating the allergic inflammatory response, although the precise role of each cytokine remains to be determined. The aim of this review is to summarize the current knowledge about the possible roles of newly identified helper T cells derived cytokines (IL-9, 17, 22, 25 and IL-33) in asthma. The potential therapeutic applications emerging from the roles of these cytokines will be discussed as well.

Keywords

1. National Health Interview Survey (NHIS) Data. Atlanta: Centers for Disease Control and Prevention; 2011. [Last cited on 2013 Jun 25 ].  Back to cited text no. 1
    
2. Barnes PJ. Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol 2008;8:183-92.  Back to cited text no. 2
[PUBMED]    
3. Kim SH, Kim BK, Lee YC. Effects of Corni fructus on ovalbumin-induced airway inflammation and airway hyper-responsiveness in a mouse model of allergic asthma. J Inflamm (Lond) 2012;9:9.  Back to cited text no. 3
    
4. Steinman L. A brief history of T (H) 17, the first major revision in the T (H) 1/T (H) 2 hypothesis of T cell-mediated tissue damage. Nat Med 2007;13:139-45.  Back to cited text no. 4
[PUBMED]    
5. Taube C, Tertilt C, Gyülveszi G, Dehzad N, Kreymborg K, Schneeweiss K, et al. IL-22 is produced by innate lymphoid cells and limits inflammation in allergic airway disease. PLoS One 2011;6:e21799.  Back to cited text no. 5
    
6. Webb DC, McKenzie AN, Koskinen AM, Yang M, Mattes J, Foster PS. Integrated signals between IL-13, IL-4, and IL-5 regulate airways hyperreactivity. J Immunol 2000;165:108-13.  Back to cited text no. 6
    
7. Fort MM, Cheung J, Yen D, Li J, Zurawski SM, Lo S, et al. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 2001;15:985-95.  Back to cited text no. 7
    
8. Maneechotesuwan K, Xin Y, Ito K, Jazrawi E, Lee KY, Usmani OS, et al. Regulation of Th2 cytokine genes by p38 MAPK-mediated phosphorylation of GATA-3. J Immunol 2007;178:2491-8.  Back to cited text no. 8
    
9. Kearley J, Erjefalt JS, Andersson C, Benjamin E, Jones CP, Robichaud A, et al. IL-9 governs allergen-induced mast cell numbers in the lung and chronic remodeling of the airways. Am J Respir Crit Care Med 2011;183:865-75.  Back to cited text no. 9
    
10. Louahed J, Kermouni A, Van Snick J, Renauld JC. IL-9 induces expression of granzymes and high-affinity IgE receptor in murine T helper clones. J Immunol 1995;154:5061-70.  Back to cited text no. 10
    
11. Dugas B, Renauld JC, Pène J, Bonnefoy JY, Peti-Frère C, Braquet P, et al. Interleukin-9 potentiates the interleukin-4-induced immunoglobulin (IgG, IgM and IgE) production by normal human B lymphocytes. Eur J Immunol 1993;23:1687-92.  Back to cited text no. 11
    
12. Kearley J, Buckland KF, Mathie SA, Lloyd CM. Resolution of allergic inflammation and airway hyperreactivity is dependent upon disruption of the T1/ST2-IL-33 pathway. Am J Respir Crit Care Med 2009;179:772-81.  Back to cited text no. 12
    
13. Scanlon ST, McKenzie AN. Type 2 innate lymphoid cells: New players in asthma and allergy. Curr Opin Immunol 2012;24:707-12.  Back to cited text no. 13
    
14. Mjösberg J, Spits H. Type 2 innate lymphoid cells-new members of the "type 2 franchise" that mediate allergic airway inflammation. Eur J Immunol 2012;42:1093-6.  Back to cited text no. 14
    
15. Chang HC, Sehra S, Goswami R, Yao W, Yu Q, Stritesky GL, et al. The transcription factor PU.1 is required for the development of IL-9-producing T cells and allergic inflammation. Nat Immunol 2010;11:527-34.  Back to cited text no. 15
    
16. Moseley TA, Haudenschild DR, Rose L, Reddi AH. Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev 2003;14:155-74.  Back to cited text no. 16
    
17. Adibrad M, Deyhimi P, Ganjalikhani Hakemi M, Behfarnia P, Shahabuei M, Rafiee L. Signs of the presence of Th17 cells in chronic periodontal disease. J Periodontal Res 2012;47:525-31.  Back to cited text no. 17
    
18. Ganjalikhani Hakemi M, Ghaedi K, Andalib A, Hosseini M, Rezaei A. Optimization of human Th17 cell differentiation in vitro: Evaluating different polarizing factors. in vitro Cell Dev Biol Anim 2011;47:581-92.  Back to cited text no. 18
    
19. Newcomb DC, Peebles RS Jr. Th17-mediated inflammation in asthma. Curr Opin Immunol 2013; [Epub ahead of print].  Back to cited text no. 19
    
20. Song C, Luo L, Lei Z, Li B, Liang Z, Liu G, et al. IL-17-producing alveolar macrophages mediate allergic lung inflammation related to asthma. J Immunol 2008;181:6117-24.  Back to cited text no. 20
    
21. Manel N, Unutmaz D, Littman DR. The differentiation of human T (H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol 2008;9:641-9.  Back to cited text no. 21
    
22. Behfarnia P, Birang R, Pishva SS, Hakemi MG, Khorasani MM. Expression levels of th-2 and th-17 characteristic genes in healthy tissue versus periodontitis. J Dent (Tehran) 2013;10:23-31.  Back to cited text no. 22
    
23. Bullens DM, Truyen E, Coteur L, Dilissen E, Hellings PW, Dupont LJ, et al. IL-17 mRNA in sputum of asthmatic patients: Linking T cell driven inflammation and granulocytic influx? Respir Res 2006;7:135.  Back to cited text no. 23
    
24. Agache I, Ciobanu C, Agache C, Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med 2010;104:1131-7.  Back to cited text no. 24
    
25. Lu H, Liu L, Cheng H, Zhang Y, Hua S. Expression of interleukin 17 and IgE, and its significance in patients with bronchial asthma. Afr J Pharm Pharmacol 2012;6:2828-31.  Back to cited text no. 25
    
26. Ji X, Li J, Xu L, Wang W, Luo M, Luo S, et al. IL4 and IL-17A provide a Th2/Th17-polarized inflammatory milieu in favor of TGF-β1 to induce bronchial epithelial-mesenchymal transition (EMT). Int J Clin Exp Pathol 2013;6:1481-92.  Back to cited text no. 26
    
27. Schmidt-Weber CB, Akdis M, Akdis CA. TH17 cells in the big picture of immunology. J Allergy Clin Immunol 2007;120:247-54.  Back to cited text no. 27
    
28. Kobayashi T, Iijima K, Checkel JL, Kita H. Interleukin-1-Family cytokines drive T Helper 2 and 17 cells to innocuous airborne antigens. Am J Respir Cell Mol Biol 2013; [Epub ahead of print].  Back to cited text no. 28
    
29. Wang YH, Voo KS, Liu B, Chen CY, Uygungil B, Spoede W, 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;207:2479-91.  Back to cited text no. 29
    
30. Cosmi L, Liotta F, Maggi E, Romagnani S, Annunziato F. Th17 cells: New players in asthma pathogenesis. Allergy 2011;66:989-98.  Back to cited text no. 30
    
31. Rocha B. Comment on "Thymic origin of intestinal alphabeta T cells revealed by fate mapping of RORgammat+cells". Science 2005;308:1553.  Back to cited text no. 31
[PUBMED]    
32. Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R. IL-22 increases the innate immunity of tissues. Immunity 2004;21:241-54.  Back to cited text no. 32
    
33. Wolk K, Kunz S, Asadullah K, Sabat R. Cutting edge: Immune cells as sources and targets of the IL-10 family members? J Immunol 2002;168:5397-402.  Back to cited text no. 33
    
34. Hirose K, Takahashi K, Nakajima H. Roles of IL-22 in allergic airway inflammation. J Allergy (Cairo) 2013;2013:260518.  Back to cited text no. 34
    
35. Takahashi K, Hirose K, Kawashima S, Niwa Y, Wakashin H, Iwata A, et al. IL-22 attenuates IL-25 production by lung epithelial cells and inhibits antigen-induced eosinophilic airway inflammation. J Allergy Clin Immunol 2011;128:1067-761.  Back to cited text no. 35
    
36. Akdis M, Palomares O, van de Veen W, van Splunter M, Akdis CA. TH17 and TH22 cells: A confusion of antimicrobial response with tissue inflammation versus protection. J Allergy Clin Immunol 2012;129:1438-49.  Back to cited text no. 36
    
37. Eyerich S, Eyerich K, Pennino D, Carbone T, Nasorri F, Pallotta S, et al. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest 2009;119:3573-85.  Back to cited text no. 37
    
38. Farfariello V, Amantini C, Nabissi M, Morelli MB, Aperio C, Caprodossi S, et al. IL-22 mRNA in peripheral blood mononuclear cells from allergic rhinitic and asthmatic pediatric patients. Pediatr Allergy Immunol 2011;22:419-23.  Back to cited text no. 38
    
39. Chang Y, Al-Alwan L, Risse PA, Halayko AJ, Martin JG, Baglole CJ, et al. Th17-associated cytokines promote human airway smooth muscle cell proliferation. FASEB J 2012;26:5152-60.  Back to cited text no. 39
    
40. Ballantyne SJ, Barlow JL, Jolin HE, Nath P, Williams AS, Chung KF, et al. Blocking IL-25 prevents airway hyperresponsiveness in allergic asthma. J Allergy Clin Immunol 2007;120:1324-31.  Back to cited text no. 40
    
41. Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S, 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;169:443-53.  Back to cited text no. 41
    
42. Afran L. Asthma and allergy: IL-25-responsive myeloid cells promote type 2 lung pathology. Nat Rev Immunol 2012;12:398.  Back to cited text no. 42
    
43. Angkasekwinai P, Park H, Wang YH, Wang YH, Chang SH, Corry DB, et al. Interleukin 25 promotes the initiation of proallergic type 2 responses. J Exp Med 2007;204:1509-17.  Back to cited text no. 43
    
44. Angkasekwinai P. The Role of IL-25 in Allergic Lung Disease. Houston: The University of Texas Graduate School of Biomedical Sciences; 2009.  Back to cited text no. 44
    
45. Gregory LG, Jones CP, Walker SA, Sawant D, Gowers KH, Campbell GA, et al. IL-25 drives remodelling in allergic airways disease induced by house dust mite. Thora×2013;68:82-90.  Back to cited text no. 45
    
46. Petersen BC, Budelsky AL, Baptist AP, Schaller MA, Lukacs NW. Interleukin-25 induces type 2 cytokine production in a steroid-resistant interleukin-17RB+myeloid population that exacerbates asthmatic pathology. Nat Med 2012;18:751-8.  Back to cited text no. 46
    
47. Seys S, Adriaensen W, Dilissen E, Grabowski M, Decraene A, Vanoirbeek J, et al. Sputum "IL-5, IL17-A and IL-25" pattern is associated with uncontrolled asthma and worse lung function. 2012;43:1009-17.  Back to cited text no. 47
    
48. Corrigan CJ, Wang W, Meng Q, Fang C, Eid G, Caballero MR, et al. Allergen-induced expression of IL-25 and IL-25 receptor in atopic asthmatic airways and late-phase cutaneous responses. J Allergy Clin Immunol 2011;128:116-24.  Back to cited text no. 48
    
49. Sims JE, Nicklin MJ, Bazan JF, Barton JL, Busfield SJ, Ford JE, et al. A new nomenclature for IL-1-family genes. Trends Immunol 2001;22:536-7.  Back to cited text no. 49
    
50. Borish L, Steinke JW. Interleukin-33 in asthma: How big of a role does it play? Curr Allergy Asthma Rep 2011;11:7-11.  Back to cited text no. 50
    
51. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005;23:479-90.  Back to cited text no. 51
    
52. Klemenz R, Hoffmann S, Werenskiold AK. Serum-and oncoprotein-mediated induction of a gene with sequence similarity to the gene encoding carcinoembryonic antigen. Proc Natl Acad Sci U S A 1989;86:5708-12.  Back to cited text no. 52
    
53. Tominaga S. A putative protein of a growth specific cDNA from BALB/c-3T3 cells is highly similar to the extracellular portion of mouse interleukin 1 receptor. FEBS Lett 1989;258:301-4.  Back to cited text no. 53
    
54. Yanagisawa K, Naito Y, Kuroiwa K, Arai T, Furukawa Y, Tomizuka H, et al. The expression of ST2 gene in helper T cells and the binding of ST2 protein to myeloma-derived RPMI8226 cells. J Biochem 1997;121:95-103.  Back to cited text no. 54
    
55. Pecaric-Petkovic T, Didichenko SA, Kaempfer S, Spiegl N, Dahinden CA. Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 2009;113:1526-34.  Back to cited text no. 55
    
56. Smithgall MD, Comeau MR, Yoon BR, Kaufman D, Armitage R, Smith DE. IL-33 amplifies both Th1-and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int Immunol 2008;20:1019-30.  Back to cited text no. 56
    
57. Löhning M, Stroehmann A, Coyle AJ, Grogan JL, Lin S, Gutierrez-Ramos JC, et al. T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function. Proc Natl Acad Sci U S A 1998;95:6930-5.  Back to cited text no. 57
    
58. Kurowska-Stolarska M, Kewin P, Murphy G, Russo RC, Stolarski B, Garcia CC, et al. IL-33 induces antigen-specific IL-5+T cells and promotes allergic-induced airway inflammation independent of IL-4. J Immunol 2008;181:4780-90.  Back to cited text no. 58
    
59. Komai-Koma M, Xu D, Li Y, McKenzie AN, McInnes IB, Liew FY. IL-33 is a chemoattractant for human Th2 cells. Eur J Immunol 2007;37:2779-86.  Back to cited text no. 59
    
60. Rank MA, Kobayashi T, Kozaki H, Bartemes KR, Squillace DL, Kita H. IL-33-activated dendritic cells induce an atypical TH2-type response. J Allergy Clin Immunol 2009;123:1047-54.  Back to cited text no. 60
    
61. Iikura M, Suto H, Kajiwara N, Oboki K, Ohno T, Okayama Y, et al. IL-33 can promote survival, adhesion and cytokine production in human mast cells. Lab Invest 2007;87:971-8.  Back to cited text no. 61
    
62. Allakhverdi Z, Smith DE, Comeau MR, Delespesse G. Cutting edge: The ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J Immunol 2007;179:2051-4.  Back to cited text no. 62
    
63. Ho LH, Ohno T, Oboki K, Kajiwara N, Suto H, Iikura M, et al. IL-33 induces IL-13 production by mouse mast cells independently of IgE-FcepsilonRI signals. J Leukoc Biol 2007;82:1481-90.  Back to cited text no. 63
    
64. Moulin D, Donzé O, Talabot-Ayer D, Mézin F, Palmer G, Gabay C. Interleukin (IL)-33 induces the release of pro-inflammatory mediators by mast cells. Cytokine 2007;40:216-25.  Back to cited text no. 64
    
65. Drube S, Heink S, Walter S, Löhn T, Grusser M, Gerbaulet A, et al. The receptor tyrosine kinase c-Kit controls IL-33 receptor signaling in mast cells. Blood 2010;115:3899-906.  Back to cited text no. 65
    
66. Kondo Y, Yoshimoto T, Yasuda K, Futatsugi-Yumikura S, Morimoto M, Hayashi N, et al. Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int Immunol 2008;20:791-800.  Back to cited text no. 66
    
67. Schneider E, Petit-Bertron AF, Bricard R, Levasseur M, Ramadan A, Girard JP, et al. IL-33 activates unprimed murine basophils directly in vitro and induces their in vivo expansion indirectly by promoting hematopoietic growth factor production. J Immunol 2009;183:3591-7.  Back to cited text no. 67
    
68. Pushparaj PN, Tay HK, H'ng SC, Pitman N, Xu D, McKenzie A, et al. The cytokine interleukin-33 mediates anaphylactic shock. Proc Natl Acad Sci U S A 2009;106:9773-8.  Back to cited text no. 68
    
69. Chu DK, Llop-Guevara A, Walker TD, Flader K, Goncharova S, Boudreau JE, et al. IL-33, but not thymic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization. J Allergy Clin Immunol 2013;131:187-2001.  Back to cited text no. 69
    
70. Cherry WB, Yoon J, Bartemes KR, Iijima K, Kita H. A novel IL-1 family cytokine, IL-33, potently activates human eosinophils. J Allergy Clin Immunol 2008;121:1484-90.  Back to cited text no. 70
    
71. Chow JY, Wong CK, Cheung PF, Lam CW. Intracellular signaling mechanisms regulating the activation of human eosinophils by the novel Th2 cytokine IL-33: Implications for allergic inflammation. Cell Mol Immunol 2010;7:26-34.  Back to cited text no. 71
    
72. Prefontaine D, Al-Awan L, Mogas A, Audusseau S, Lajoie-Kadoch S, Olivenstein R, et al. Interleukin-33 in asthma: insights into pro-inflammatory roles of airway structural cells. Allergy Asthma Clin Immunol 2010;6 Suppl 1:P20.  Back to cited text no. 72
    
73. Borish L, Steinke JW. Interleukin-33 in asthma: How big of a role does it play? Current allergy and asthma reports. 2011;11:7-11.  Back to cited text no. 73
    
74. Saglani S, Lui S, Ullmann N, Campbell GA, Sherburn RT, Mathie SA, et al. IL-33 promotes airway remodeling in pediatric patients with severe steroid-resistant asthma. J Allergy Clin Immunol 2013;132:676-68513.  Back to cited text no. 74
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