Interleukin-13: Prospects for new treatments

Clinical and Experimental Allergy

Volumn 40, Issue 1, 2010, Pages 42-49

  Brightling, C E ^a   Saha, S ^a   Hollins, F ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALTRAKINCEPT; AMG 317; INTERLEUKIN 13; INTERLEUKIN 13 ANTIBODY; INTERLEUKIN 13 RECEPTOR; INTERLEUKIN 4 ANTIBODY; INTERLEUKIN 4 RECEPTOR ALPHA ANTIBODY; MESSENGER RNA; PITRAKINRA; UNCLASSIFIED DRUG;

AIRWAY; ASTHMA; BLOOD; BRONCHUS MUCOSA; CHRONIC OBSTRUCTIVE LUNG DISEASE; DISEASE COURSE; DISEASE SEVERITY; DRUG EFFICACY; GENETIC POLYMORPHISM; HUMAN; LUNG LAVAGE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SPUTUM; UPREGULATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ASTHMA; BRONCHI; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; HUMANS; INTERLEUKIN-13; POLYMORPHISM, GENETIC; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY MUCOSA; SPUTUM; UP-REGULATION;

EID: 72949108441     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/j.1365-2222.2009.03383.x     Document Type: Review

References (92)

1. Minty A, Chalon P, Derocq JM et al. Interleukin-13 is a new human lymphokine regulating inflammatory and immune responses. Nature 1993 362 : 248 250.
2. Punnonen J, Aversa G, Cocks BG et al. Interleukin 13 induces interleukin 4-independent IgG4 and IgE synthesis and CD23 expression by human B cells. Proc Natl Acad Sci USA 1993 90 : 3730 3734.
3. Grunig G, Warnock M, Wakil AE et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 1998 282 : 2261 2263.
4. Wills-Karp M, Luyimbazi J, Xu X et al. Interleukin-13: central mediator of allergic asthma. Science 1998 282 : 2258 2261.
5. Zheng T, Zhu Z, Wang Z et al. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J Clin Invest 2000 106 : 1081 1093.
6. Jaffe JS, Raible DG, Post TJ et al. Human lung mast cell activation leads to IL-13 mRNA expression and protein release. Am J Respir Cell Mol Biol 1996 15 : 473 481.
7. Kim EY, Battaile JT, Patel AC et al. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat Med 2008 14 : 633 640.
8. Schmid-Grendelmeier P, Altznauer F, Fischer B et al. Eosinophils express functional IL-13 in eosinophilic inflammatory diseases. J Immunol 2002 169 : 1021 1027.
9. LaPorte SL, Juo ZS, Vaclavikova J et al. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 2008 132 : 259 272.
10. Wang IM, Lin H, Goldman SJ, Kobayashi M. STAT-1 is activated by IL-4 and IL-13 in multiple cell types. Mol Immunol 2004 41 : 873 884.
11. Lordan JL, Bucchieri F, Richter A et al. Cooperative effects of Th2 cytokines and allergen on normal and asthmatic bronchial epithelial cells. J Immunol 2002 169 : 407 414.
12. Murata T, Husain SR, Mohri H, Puri RK. Two different IL-13 receptor chains are expressed in normal human skin fibroblasts, and IL-4 and IL-13 mediate signal transduction through a common pathway. Int Immunol 1998 10 : 1103 1110.
13. Laporte JC, Moore PE, Baraldo S et al. Direct effects of interleukin-13 on signaling pathways for physiological responses in cultured human airway smooth muscle cells. Am J Respir Crit Care Med 2001 164 : 141 148.
14. Kaur D, Hollins F, Woodman L et al. Mast cells express IL-13Ralpha1: IL-13 promotes human lung mast cell proliferation and FcepsilonRI expression. Allergy 2006 61 : 1047 1053.
15. Wang Y, Malabarba MG, Nagy ZS, Kirken RA. Interleukin 4 regulates phosphorylation of serine 756 in the transactivation domain of Stat6. Roles for multiple phosphorylation sites and Stat6 function. J Biol Chem 2004 279 : 25196 25203.
16. Andrews AL, Nasir T, Bucchieri F, Holloway JW, Holgate ST, Davies DE. IL-13 receptor alpha 2: a regulator of IL-13 and IL-4 signal transduction in primary human fibroblasts. J Allergy Clin Immunol 2006 118 : 858 865.
17. Zheng T, Liu W, Oh SY et al. IL-13 receptor alpha2 selectively inhibits IL-13-induced responses in the murine lung. J Immunol 2008 180 : 522 529.
18. Fichtner-Feigl S, Strober W, Kawakami K, Puri RK, Kitani A. IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat Med 2006 12 : 99 106.
19. Kuperman DA, Huang X, Koth LL et al. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat Med 2002 8 : 885 889.
20. Tliba O, Deshpande D, Chen H et al. IL-13 enhances agonist-evoked calcium signals and contractile responses in airway smooth muscle. Br J Pharmacol 2003 140 : 1159 1162.
21. Vercelli D. Advances in asthma and allergy genetics in 2007. J Allergy Clin Immunol 2008 122 : 267 271.
22. Howard TD, Whittaker PA, Zaiman AL et al. Identification and association of polymorphisms in the interleukin-13 gene with asthma and atopy in a Dutch population. Am J Respir Cell Mol Biol 2001 25 : 377 384.
23. van der Pouw Kraan TC, van Veen A, Boeije LC et al. An IL-13 promoter polymorphism associated with increased risk of allergic asthma. Genes Immun 1999 1 : 61 5.
24. Heinzmann A, Mao XQ, Akaiwa M et al. Genetic variants of IL-13 signalling and human asthma and atopy. Hum Mol Genet 2000 9 : 549 559.
25. Graves PE, Kabesch M, Halonen M et al. A cluster of seven tightly linked polymorphisms in the IL-13 gene is associated with total serum IgE levels in three populations of white children. J Allergy Clin Immunol 2000 105 : 506 513.
26. Reglier H, Arce-Vicioso M, Fay M, Gougerot-Pocidalo MA, Chollet-Martin S. Lack of IL-10 and IL-13 production by human polymorphonuclear neutrophils. Cytokine 1998 10 : 192 198.
27. Gibbs BF, Haas H, Falcone FH et al. Purified human peripheral blood basophils release interleukin-13 and preformed interleukin-4 following immunological activation. Eur J Immunol 1996 26 : 2493 2498.
28. Ochensberger B, Daepp GC, Rihs S, Dahinden CA. Human blood basophils produce interleukin-13 in response to IgE-receptor-dependent and -independent activation. Blood 1996 88 : 3028 3037.
29. Wong CK, Ho CY, Ko FW et al. Proinflammatory cytokines (IL-17, IL-6, IL-18 and IL-12) and Th cytokines (IFN-gamma, IL-4, IL-10 and IL-13) in patients with allergic asthma. Clin Exp Immunol 2001 125 : 177 183.
30. Silvestri M, Bontempelli M, Giacomelli M et al. High serum levels of tumour necrosis factor-alpha and interleukin-8 in severe asthm: markers of systemic inflammation? Clin Exp Allergy 2006 36 : 1373 1381.
31. Lee YC, Lee KH, Lee HB, Rhee YK. Serum levels of interleukins (IL)-4, IL-5, IL-13, and interferon-gamma in acute asthma. J Asthma 2001 38 : 665 671.
32. Brightling CE, Ward R, Goh KL, Wardlaw AJ, Pavord ID. Eosinophilic bronchitis is an important cause of chronic cough. Am J Respir Crit Care Med 1999 160 : 406 410.
33. Berger P, Girodet PO, Begueret H et al. Tryptase-stimulated human airway smooth muscle cells induce cytokine synthesis and mast cell chemotaxis. FASEB J 2003 17 : 2139 2141.
34. Brightling CE, Bradding P, Symon FA, Holgate ST, Wardlaw AJ, Pavord ID. Mast-cell infiltration of airway smooth muscle in asthma. N Engl J Med 2002 346 : 1699 1705.
35. Saha SK, Berry MA, Parker D et al. Increased sputum and bronchial biopsy IL-13 expression in severe asthma. J Allergy Clin Immunol 2008 121 : 685 691.
36. Siddiqui S, Mistry V, Doe C et al. Airway hyperresponsiveness is dissociated from airway wall structural remodeling. J Allergy Clin Immunol 2008 122 : 335 341.
37. Park SW, Jangm HK, An MH et al. Interleukin-13 and interleukin-5 in induced sputum of eosinophilic bronchitis: comparison with asthma. Chest 2005 128 : 1921 1927.
38. Siddiqui S, Cruse G, McKenna S et al. IL-13 expression by blood T cells and not eosinophils is increased in asthma compared to non-asthmatic eosinphilic bronchitis. BMC Pulm Med 2009 9 : 34.
39. Till S, Durham S, Dickason R et al. IL-13 production by allergen-stimulated T cells is increased in allergic disease and associated with IL-5 but not IFN-gamma expression. Immunology 1997 91 : 53 7.
40. Hashimoto T, Akiyama K, Kawaguchi H et al. Correlation of allergen-induced IL-5 and IL-13 production by peripheral blood T cells of asthma patients. Int Arch Allergy Immunol 2004 134 (Suppl. 1) : 7 11.
41. Berry MA, Parker D, Neale N et al. Sputum and bronchial submucosal IL-13 expression in asthma and eosinophilic bronchitis. J Allergy Clin Immunol 2004 114 : 1106 1109.
42. Truyen E, Coteur L, Dilissen E et al. Evaluation of airway inflammation by quantitative Th1/Th2 cytokine mRNA measurement in sputum of asthma patients. Thorax 2006 61 : 202 208.
43. Boniface S, Koscher V, Mamessier E et al. Assessment of T lymphocyte cytokine production in induced sputum from asthmatics: a flow cytometry study. Clin Exp Allergy 2003 33 : 1238 1243.
44. Huang SK, Xiao HQ, Kleine-Tebbe J et al. IL-13 expression at the sites of allergen challenge in patients with asthma. J Immunol 1995 155 : 2688 2694.
45. Kroegel C, Julius P, Matthys H, Virchow JC Jr., Luttmann W. Endobronchial secretion of interleukin-13 following local allergen challenge in atopic asthma: relationship to interleukin-4 and eosinophil counts. Eur Respir J 1996 9 : 899 904.
46. Bodey KJ, Semper AE, Redington AE et al. Cytokine profiles of BAL T cells and T-cell clones obtained from human asthmatic airways after local allergen challenge. Allergy 1999 54 : 1083 1093.
47. Barcelo B, Pons J, Fuster A et al. Intracellular cytokine profile of T lymphocytes in patients with chronic obstructive pulmonary disease. Clin Exp Immunol 2006 145 : 474 479.
48. Prieto J, Lensmar C, Roquet A et al. Increased interleukin-13 mRNA expression in bronchoalveolar lavage cells of atopic patients with mild asthma after repeated low-dose allergen provocations. Respir Med 2000 94 : 806 814.
49. Kraft M, Hamid Q, Chrousos GP, Martin RJ, Leung DY. Decreased steroid responsiveness at night in nocturnal asthma. Is the macrophage responsible? Am J Respir Crit Care Med 2001 163 : 1219 1225.
50. Spahn JD, Szefler SJ, Surs W, Doherty DE, Nimmagadda SR, Leung DY. A novel action of IL-13: induction of diminished monocyte glucocorticoid receptor-binding affinity. J Immunol 1996 157 : 2654 2659.
51. Kotsimbos TC, Ernst P, Hamid QA. Interleukin-13 and interleukin-4 are coexpressed in atopic asthma. Proc Assoc Am Phys 1996 108 : 368 373.
52. Naseer T, Minshall EM, Leung DY et al. Expression of IL-12 and IL-13 mRNA in asthma and their modulation in response to steroid therapy. Am J Respir Crit Care Med 1997 155 : 845 851. (Pubitemid 27133392)
53. Saha S, Mistry V, Siva R et al. Induced sputum and bronchial mucosal expression of interleukin-13 is not increased in chronic obstructive pulmonary disease. Allergy 2008 63 : 1239 1243.
54. Humbert M, Durham SR, Kimmitt P et al. Elevated expression of messenger ribonucleic acid encoding IL-13 in the bronchial mucosa of atopic and nonatopic subjects with asthma. J Allergy Clin Immunol 1997 99 : 657 665.
55. Brightling CE, Symon FA, Holgate ST, Wardlaw AJ, Pavord ID, Bradding P. Interleukin-4 and -13 expression is co-localized to mast cells within the airway smooth muscle in asthma. Clin Exp Allergy 2003 33 : 1711 1716.
56. Hoshino T, Kato S, Oka N et al. Pulmonary inflammation and emphysema: role of the cytokines IL-18 and IL-13. Am J Respir Crit Care Med 2007 176 : 49 62.
57. van der Pouw Kraan TC, Kucukaycan M, Bakker AM et al. Chronic obstructive pulmonary disease is associated with the -1055 IL-13 promoter polymorphism. Genes Immun 2002 3 : 436 439. (Pubitemid 41656545)
58. Sadeghnejad A, Meyers DA, Bottai M, Sterling DA, Bleecker ER, Ohar JA. IL13 promoter polymorphism 1112C/T modulates the adverse effect of tobacco smoking on lung function. Am J Respir Crit Care Med 2007 176 : 748 752.
59. Lee JS, Rosengart MR, Kondragunta V et al. Inverse association of plasma IL-13 and inflammatory chemokines with lung function impairment in stable COPD: a cross-sectional cohort study. Respir Res 2007 8 : 64.
60. Imaoka H, Hoshino T, Takei S et al. Interleukin-18 production and pulmonary function in COPD. Eur Respir J 2008 31 : 287 297.
61. Meuronen A, Majuri ML, Alenius H et al. Decreased cytokine and chemokine mRNA expression in bronchoalveolar lavage in asymptomatic smoking subjects. Respiration 2008 75 : 450 458.
62. Miotto D, Ruggieri MP, Boschetto P et al. Interleukin-13 and -4 expression in the central airways of smokers with chronic bronchitis. Eur Respir J 2003 22 : 602 608.
63. Boutten A, Bonay M, Laribe S et al. Decreased expression of interleukin 13 in human lung emphysema. Thorax 2004 59 : 850 854.
64. Haldar P, Brightling CE, Hargadon B et al. Mepolizumab and exacerbations of refractory eosinophilic asthma. N Engl J Med 2009 360 : 973 984.
65. Nair P, Pizzichini MM, Kjarsgaard M et al. Mepolizumab for prednisone-dependent asthma with sputum eosinophilia. N Engl J Med 2009 360 : 985 993.
66. Woltmann G, McNulty CA, Dewson G, Symon FA, Wardlaw AJ. Interleukin-13 induces PSGL-1/P-selectin-dependent adhesion of eosinophils, but not neutrophils, to human umbilical vein endothelial cells under flow. Blood 2000 95 : 3146 3152.
67. Horie S, Okubo Y, Hossain M et al. Interleukin-13 but not interleukin-4 prolongs eosinophil survival and induces eosinophil chemotaxis. Intern Med 1997 36 : 179 185.
68. Luttmann W, Knoechel B, Foerster M, Matthys H, Virchow JC Jr., Kroegel C. Activation of human eosinophils by IL-13. Induction of CD69 surface antigen, its relationship to messenger RNA expression, and promotion of cellular viability. J Immunol 1996 157 : 1678 1683.
69. Zurawski G, de Vries JE. Interleukin 13 elicits a subset of the activities of its close relative interleukin 4. Stem Cells 1994 12 : 169 174.
70. Endo T, Ogushi F, Sone S. LPS-dependent cyclooxygenase-2 induction in human monocytes is down-regulated by IL-13, but not by IFN-gamma. J Immunol 1996 156 : 2240 2246.
71. Sozzani P, Cambon C, Vita N et al. Interleukin-13 inhibits protein kinase C-triggered respiratory burst in human monocytes. Role of calcium and cyclic AMP. J Biol Chem 1995 270 : 5084 5088.
72. Lentsch AB, Shanley TP, Sarma V, Ward PA. In vivo suppression of NF-kappa B and preservation of I kappa B alpha by interleukin-10 and interleukin-13. J Clin Invest 1997 100 : 2443 2448.
73. Ahdieh M, Vandenbos T, Youakim A. Lung epithelial barrier function and wound healing are decreased by IL-4 and IL-13 and enhanced by IFN-gamma. Am J Physiol Cell Physiol 2001 281 : C2029 38.
74. Danahay H, Atherton H, Jones G, Bridges RJ, Poll CT. Interleukin-13 induces a hypersecretory ion transport phenotype in human bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 2002 282 : L226 36.
75. Richter A, Puddicombe SM, Lordan JL et al. The contribution of interleukin (IL)-4 and IL-13 to the epithelial-mesenchymal trophic unit in asthma. Am J Respir Cell Mol Biol 2001 25 : 385 391.
76. Hashimoto S, Gon Y, Takeshita I, Maruoka S, Horie T. IL-4 and IL-13 induce myofibroblastic phenotype of human lung fibroblasts through c-Jun NH2-terminal kinase-dependent pathway. J Allergy Clin Immunol 2001 107 : 1001 1008.
77. Doucet C, Brouty-Boye D, Pottin-Clemenceau C, Jasmin C, Canonica GW, Azzarone B. IL-4 and IL-13 specifically increase adhesion molecule and inflammatory cytokine expression in human lung fibroblasts. Int Immunol 1998 10 : 1421 1433.
78. Grunstein MM, Hakonarson H, Leiter J et al. IL-13-dependent autocrine signaling mediates altered responsiveness of IgE-sensitized airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2002 282 : L520 8.
79. Moore PE, Church TL, Chism DD, Panettieri RA Jr., Shore SA. IL-13 and IL-4 cause eotaxin release in human airway smooth muscle cells: a role for ERK. Am J Physiol Lung Cell Mol Physiol 2002 282 : L847 53.
80. Baraldo S, Faffe DS, Moore PE et al. Interleukin-9 influences chemokine release in airway smooth muscle: role of ERK. Am J Physiol Lung Cell Mol Physiol 2003 284 : L1093 102.
81. Sutcliffe A, Kaur D, Page S et al. Mast cell migration to Th2 stimulated airway smooth muscle from asthmatics. Thorax 2006 61 : 657 662.
82. Chan V, Burgess JK, Ratoff JC et al. Extracellular matrix regulates enhanced eotaxin expression in asthmatic airway smooth muscle cells. Am J Respir Crit Care Med 2006 174 : 379 385.
83. Brightling CE, Ammit AJ, Kaur D et al. The CXCL10/CXCR3 axis mediates human lung mast cell migration to asthmatic airway smooth muscle. Am J Respir Crit Care Med 2005 171 : 1103 1108.
84. Borish LC, Nelson HS, Corren J et al. Efficacy of soluble IL-4 receptor for the treatment of adults with asthma. J Allergy Clin Immunol 2001 107 : 963 970.
85. Wenzel S, Wilbraham D, Fuller R, Getz EB, Longphre M. Effect of an interleukin-4 variant on late phase asthmatic response to allergen challenge in asthmatic patients: results of two phase 2a studies. Lancet 2007 370 : 1422 1431.
86. Getz EB, Wilbraham D, Lalor C, Longphre M, Fuller R. Pharmacokinetics and local tolerance of an IL-4/IL-13 antagonist inhalation powder in humans. ERS Abstract, 2008.
87. Gauvreau GM, Boulet LP, Fitzgerald JM et al. The effects of IMA-638 on allergen induced airway responses in subjects with mild atopic asthma. ERS Abstract, 2008.
88. Bhowmick B, Singh D, Molfino N et al. A double-blind, placebo-controlled, study to assess the pharmacokinetics, safety and tolerability of multiple ascending intravenous doses of CAT 354, a recombinant human anti-IL13 antibody, in subjects with moderate asthma. ERS Abstract, 2008.
89. Banfield C, Vincent M, Kakkar T et al. Multiple-dose study of AMG317 in adults with asthma: pharmacokinetics and safety. ATS Abstract, 2008.
90. Adcock IM, Caramori G, Chung KF. New targets for drug development in asthma. Lancet 2008 372 : 1073 1087.
91. Cox G, Thomson NC, Rubin AS et al. Asthma control during the year after bronchial thermoplasty. N Engl J Med 2007 356 : 1327 1337.
92. Haldar P, Pavord ID, Shaw DE et al. Cluster analysis and clinical asthma phenotypes. Am J Respir Crit Care Med 2008 178 : 218 224.