The role of cytokines and chemokines in severe respiratory syncytial virus infection and subsequent asthma

Cytokine

Volumn 53, Issue 1, 2011, Pages 1-7

  Zeng, Ruihong ^a   Li, Caixia ^a   Li, Na ^a,b   Wei, Lin ^a   Cui, YuXiu ^a  

^a HEBEI MEDICAL UNIVERSITY   (China)

^b Xingtai Medical College   (China)

Author keywords

Asthma; Chemokine; Cytokine; Lower respiratory tract infection; Respiratory syncytial virus

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CHEMOKINE; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ASTHMA; BIOLOGICAL ACTIVITY; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE SEVERITY; HEREDITY; HUMAN; IMMUNOPATHOLOGY; INNATE IMMUNITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY SYNCYTIAL VIRUS INFECTION; REVIEW; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE ACTIVATION; TH17 CELL; TH2 CELL;

ASTHMA; CHEMOKINES; HUMANS; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS;

RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 78349313856     PISSN: 10434666     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cyto.2010.09.011     Document Type: Review

References (99)

1. Collins PL, Chanock RM, Murphy BR. In: Knipe D, Howley P, editors. Respiratory syncytial virus disease, 4th ed. Fields in virology. Philadelphia, Pennsylvania. USA: Lippincott Williams & Wilkins; 2001. p. 1443-86.
2. Kusel M.M., de Klerk N.H., Kebadze T., Vohma V., Holt P.G., Johnston S.L., et al. Early life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J Allergy Clin Immunol 2007, 119:1105-1110.
3. Stensballe L.G., Simonsen J.B., Thomsen S.F., Larsen A.H., Lysdal S.H., Aaby P., et al. The causal direction in the association between respiratory syncytial virus hospitalization and asthma. J Allergy Clin Immunol 2009, 123:131-137.
4. Sigurs N., Gustafsson P.M., Bjarnason R., Lundberg F., Schmidt S., Sigurbergsson F., et al. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am J Respir Crit Care Med 2005, 171:137-141.
5. Sigurs N., Bjarnason R., Sigurbergsson F., Kjellman B. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am J Respir Crit Care Med 2000, 161:1501-1507.
6. Puthothu B., Bierbaum S., Kopp M.V., Forster J., Heinze J., Weckmann M., et al. Association of TNF-alpha with severe respiratory syncytial virus infection and bronchial asthma. Pediatr Allergy Immunol 2009, 20(2):157-163.
7. Siezen C.L., Bont L., Hodemaekers H.M., Ermers M.J., Doornbos G., Slot R., et al. Genetic susceptibility to respiratory syncytial virus bronchiolitis in preterm children is associated with airway remodeling genes and innate immune genes. Pediatr Infect Dis J 2009, 28:333-335.
8. Janssen R., Bont L., Siezen C.L., Hodemaekers H.M., Ermers M.J., Doornbos G., et al. Genetic susceptibility to respiratory syncytial virus bronchiolitis is predominantly associated with innate immune genes. J Infect Dis 2007, 196:826-834.
9. Gentile D.A., Doyle W.J., Zeevi A., Howe-Adams J., Kapadia S., Trecki J., et al. Cytokine gene polymorphisms moderate illness severity in infants with respiratory syncytial virus infection. Hum Immunol 2003, 64:338-344.
10. LaPorte S.L., Juo Z.S., Vaclavikova J., Colf L.A., Qi X., Heller N.M., et al. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 2008, 132:259-272.
11. Ermers M.J., Hoebee B., Hodemaekers H.M., Kimman T.G., Kimpen J.L., Bont L. IL-13 genetic polymorphism identifies children with late wheezing after respiratory syncytial virus infection. J Allergy Clin Immunol 2007, 119:1086-1091.
12. Choi E.H., Lee H.J., Yoo T., Chanock S.J. A common haplotype of interleukin-4 gene IL4 is associated with severe respiratory syncytial virus disease in korean children. J Infect Dis 2002, 186:1207-1211.
13. Forton J.T., Rowlands K., Rockett K., Hanchard N., Herbert M., Kwiatkowski D.P., et al. Genetic association study for RSV bronchiolitis in infancy at the 5q31 cytokine cluster. Thorax 2009, 64:345-352.
14. Amanatidou V., Sourvinos G., Apostolakis S., Neonaki P., Tsilimigaki A., Krambovitis E., et al. RANTES promoter gene polymorphisms and susceptibility to severe respiratory syncytial virus-induced bronchiolitis. Pediatr Infect Dis J 2008, 27:38-42.
15. Tian M., Liu F., Wen G.Y., Shi S.Y., Chen R.H., Zhao D.Y. Effect of variation in RANTES promoter on serum RANTES levels and risk of recurrent wheezing after RSV bronchiolitis in children from Han, Southern China. Eur J Pediatr 2009, 168:963-967.
16. Kunkel S.L., Standiford T., Kasahara K., Strieter R.M., et al. Interleukin-8 (IL-8): the major neutrophil chemotactic factor in the lung. Exp Lung Res 1991, 17:17-23.
17. Becker S., Quay J., Soukup J. Cytokine (tumor necrosis factor, IL-6, IL-8) production by respiratory syncytial virus-infected human alveolar macrophages. J Immunol 1991, 147:4307-4312.
18. Arnold R., Humbert B., Werchau H., Gallati H., Konig W. Interleukin-8, interleukin-6, and soluble tumour necrosis factor receptor type 1 release from a human pulmonary epithelial cell line (A549) exposed to respiratory syncytial virus. Immunology 1994, 82:126-133.
19. Abu-Harb M., Bell F., Finn A., Rao W.H., Nixon L., Shale D., et al. IL-8 and neutrophil elastase levels in the respiratory tract of infants with RSV bronchiolitis. Eur Respir J 1999, 14:139-143.
20. Norzila M.Z., Fakes K., Henry R.L., Simpson J., Gibson P.G. Interleukin-8 secretion and neutrophil recruitment accompanies induced sputum eosinophil activation in children with acute asthma. Am J Respir Crit Care Med 2000, 161:769-774.
21. Hull J., Thomson A., Kwiatkowski D. Association of respiratory syncytial virus bronchiolitis with the interleukin 8 gene region in UK families. Thorax 2000, 55:1023-1027.
22. Heinzmann A., Ahlert I., Kurz T., Berner R., Deichmann K.A. Association study suggests opposite effects of polymorphisms within IL8 on bronchial asthma and respiratory syncytial virus bronchiolitis. J Allergy Clin Immunol 2004, 114(3):671-676.
23. Puthothu B., Krueger M., Heinze J., Forster J., Heinzmann A. Impact of IL8 and IL8-receptor alpha polymorphisms on the genetics of bronchial asthma and severe RSV infections. Clin Mol Allergy 2006, 4:2-7.
24. Lu A., Wang L., Zhang X. Haplotype of IL-8-251T and 781C is associated with the susceptibility to respiratory syncytial virus. J Trop Pediatr 2010 Aug, 56(4):242-246.
25. Juntti H., Osterlund P., Kokkonen J., Dunder T., Renko M., Pokka T., et al. Cytokine responses in cord blood predict the severity of later respiratory syncytial virus infection. J Allergy Clin Immunol 2009, 124(1):52-58.
26. Gern J.E., Brooks G.D., Meyer P., Chang A., Shen K., Evans M.D., et al. Bidirectional interactions between viral respiratory illnesses and cytokine responses in the first year of life. J Allergy Clin Immunol 2006, 117:72-78.
27. Macaubas C., de Klerk N., Holt B., Wee C., Kendall G., Firth M., et al. Association between antenatal cytokine production and the development of atopy and asthma at age 6years. Lancet 2003, 362:1192-1197.
28. Kurt-Jones E.A., Popova L., Kwinn L., Haynes L.M., Jones L.P., Tripp R.A., et al. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat Immunol 2000, 1:398-401.
29. Murawski M.R., Bowen G.N., Cerny A.M., Anderson L.J., Haynes L.M., Tripp R.A., et al. Respiratory syncytial virus activates innate immunity through toll-like receptor 2. J Virol 2009, 83:1492-1500.
30. Groskreutz D.J., Monick M.M., Powers L.S., Yarovinsky T.O., Look D.C., Hunninghake G.W. Respiratory syncytial virus induces TLR3 protein and protein kinase R, leading to increased double stranded RNA responsiveness in airway epithelial cells. J Immunol 2006, 176:1733-1740.
31. Lukacs N.W., Smit J.J., Mukherjee S., Morris S.B., Nunez G., Lindell D.M. Respiratory virus-induced TLR7 activation controls IL-17-associated increased mucus via IL-23 regulation. J Immunol 2010, 185(4):2231-2239.
32. Kolumam G., Thomas S., Thompson L., Sprent J., Murali-Krishna K. Type I IFNs act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 2005, 202:637-650.
33. Thompson L., Kolumam G., Thomas S., Murali-Krishna K. Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J Immunol 2006, 177:1746-1754.
34. Boogaard I., van Oosten M., van Rijt L.S., Muskens F., Kimman T.G., Lambrecht B.N., et al. Respiratory syncytial virus differentially activates murine myeloid and plasmacytoid dendritic cells. Immunology 2007, 122:65-72.
35. Jewell N.A., Vaghefi N., Mertz S.E., Akter P., Peebles R.S., Bakaletz L.O., et al. Differential type I interferon induction by respiratory syncytial virus and influenza A virus in vivo. J Virol 2007, 81:9790-9800.
36. Zhang W., Boyapalle S., Cao X., Wang J., Lockey R.F., Mohapatra S.S., et al. RSV NS1 protein blocks the IFN response by blocking RIG-I interaction with the mitochondrial antiviral signaling protein, MAVS. J Allergy Clin Immunol 2009, 123:S208.
37. Pletneva L.M., Haller O., Porter D.D., Prince G.A., Blanco J.C.G. Induction of type I interferons and interferon inducible Mx genes during respiratory syncytial virus infection and reinfection in cotton rats. J Gen Virol 2008, 89:261-270.
38. Spann K.M., Tran K.C., Collins P.L. Effects of nonstructural proteins NS1 and NS2 of human respiratory syncytial virus on interferon regulatory factor 3, NF-κB, and proinflammatory cytokines. J Virol 2005, 79(9):5353-5362.
39. Moore E.C., Barber J., Tripp R.A. Respiratory syncytial virus (RSV) attachment and nonstructural proteins modify the type I interferon response associated with suppressor of cytokine signaling (SOCS) proteins and IFN-stimulated gene-15 (ISG15). Virol J 2008, 5:116-126.
40. Shinga M., Azuma M., Ebihara T., Sasai M., Funami K., Ayata M., et al. Soluble G protein of respiratory syncytial virus inhibits Toll-like receptor 3/4-mediated IFN-beta induction. Int Immunol 2008, 20(9):1169-1180.
41. Israele V., Polack N.R., Kleeberger S.R., Polack F.P., Melendi G.A., Laham F.R., et al. Cytokine profiles in the respiratory tract during primary infection with human metapneumovirus, respiratory syncytial virus, or influenza virus in infants. Pediatrics 2007, 120:e410-e415.
42. Nouën C.L., Munir S., Losq S., Winter C.C., McCarty T., Stephany D.A., et al. Infection and maturation of monocyte-derived human dendritic cells by human respiratory syncytial virus, human metapneumovirus, and human parainfluenza virus type 3. Virolology 2009, 385:169-182.
43. Semple M.G., Dankert H.M., Ebrahimi B., Correia J.B., Booth J.A., Stewart J.P., et al. Severe respiratory syncytial virus bronchiolitis in infants is associated with reduced airway interferon gamma and substance P. PloS ONE 2007, 2(10):e1038-e1045.
44. Legg J.P., Hussain I.R., Warner J.A., Johnston S.L., Warner J.O. Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am J Respir Crit Care Med 2003, 168:633-639.
45. Lee F.E., Walsh E.E., Falsey A.R., Lumb M.E., Okam N.V., Liu N., et al. Human infant respiratory syncytial virus (RSV)-specific type 1 and 2 cytokine responses ex vivo during primary RSV infection. J Infect Dis 2007, 195:1779-1788.
46. Lee Y.M., Miyahara N., Takeda K., Prpich J., Oh A., Balhorn A., et al. IFN-γ production during initial infection determines the outcome of reinfection with respiratory syncytial virus. Am J Respir Crit Care Med 2008, 177:208-218.
47. Harker J.A., Lee D.C., Yamaguchi Y., Wang B., Bukreyev A., Collins P.L., et al. The delivery of cytokines by recombinant virus in early life alters the immune response to adult lung infection. J Virol 2010, 84(10):5294-5302.
48. Murai H., Terada A., Mizuno M., Asai M., Hirabayashi Y., Shimizu S., et al. IL-10 and RANTES are elevated in nasopharyngeal secretions of children with respiratory syncytial virus infection. Allergol Int 2007, 56:157-163.
49. Tekkanat K.K., Maassab H.F., Cho D.S., Lai J.J., John A., Berlin A., et al. IL-13-induced airway hyperreactivity during respiratory syncytial virus infection is STAT6 dependent. J Immunol 2001, 166:3542-3548.
50. Bermejo-Martin J.F., Garcia-Arevalo M.C., Alonso A., De Lejarazu R.O., Pino M., Resino S., et al. Persistence of proinflammatory response after severe respiratory syncytial virus disease in children. J Allergy Clin Immunol 2007, 119(6):1547-1550.
51. Fischer J.E., Johnson J.E., Kuli-Zade R.K., Johnson T.R., Aung S., Parker R.A., et al. Overexpression of interleukin-4 delays virus clearance in mice infected with respiratory syncytial virus. J Virol 1997, 71:8672-8677.
52. Zhou W., Hashimoto K., Moore M.L., Elias J.A., Zhu Z., Durbin J., et al. IL-13 is associated with reduced illness and replication in primary respiratory syncytial virus infection in the mouse. Microbes Infect 2006, 8:2880-2889.
53. Fujino S., Andoh A., Bamba S., Ogawa A., Hata K., Araki Y., et al. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 2003, 52:65-70.
54. Larranaga C.L., Ampuero S.L., Luchsinger V.F., Carrion F.A., Aguilar N.V., Morales P.R., et al. Impaired immune response in severe human lower tract respiratory infection by respiratory syncytial virus. Pediatr Infect Dis J 2009, 28(10):867-873.
55. Miller A.L., Bowlin T.L., Lukacs N.W. Respiratory syncytial virus induced chemokine production: linking viral replication to chemokine production in vitro and in vivo. J Infect Dis 2004, 189:1419-1430.
56. Oshansky C.M., Barber J.P., Crabtree J., Tripp R.A. Respiratory syncytial virus F and G proteins induce interleukin 1alpha, CC, and CXC chemokine responses by normal human bronchoepithelial cells. J Infect Dis 2010, 201(8):1201-1207.
57. Bermejo-Martin J.F., Garcia-Arevalo M.C., De Lejarazu R.O., Ardura J., Eiros J.M., Alonso A., et al. Predominance of Th2 cytokines, CXC chemokines and innate immunity mediators at the mucosal level during severe respiratory syncytial virus infection in children. Eur Cytokine Netw 2007, 18:162-167.
58. Morrison P.T., Sharland M., Thomas L.H., Manna S., Handforth J., Tibby S., et al. Chemokine-receptor upregulation and disease severity in respiratory syncytial virus infection. Clin Immunol 2008, 128:85-93.
59. Morrison P.T., Thomas L.H., Sharland M., Friedland J.S. RSV-infected airway epithelial cells cause biphasic upregulation of CCR1 expression on human monocytes. J Leukoc Biol 2007, 81:1487-1495.
60. Cepika A.M., Gagro A., Bace A., Tjesic-Drinkovic D., Kelecic J., Baricic-Voskresensky T., et al. Expression of chemokine receptor CX3CR1 in infants with respiratory syncytial virus bronchiolitis. Pediatr Allergy Immunol 2008, 19:148-156.
61. Pribul P.K., Harker J., Wang B., Wang H.W., Tregoning J.S., Schwarze J.R., et al. Alveolar macrophages are a major determinant of early responses to viral ling infection but do not influence subsequent disease development. J Virol 2008, 82:4441-4448.
62. Culley F.J., Pennycook A.M., Tregoning J.S., Hussell T., Openshaw P.J. Differential chemokine expression following respiratory virus infection reflects Th1- or Th2-biased immunopathology. J Virol 2006, 80:4521-4527.
63. Tregoning J.S., Pribul P.K., Pennycook A.M.J., Hussell T., Wang B., et al. The chemokine MIP1a/CCL3 determines pathology in primary RSV infection by regulating the balance of T cell populations in the murine lung. PLoS ONE 2010, 5(2):e9381-e9388.
64. Lindell D.M., Lane T.E., Lukacs N.W. CXCL10/CXCR3-mediated responses promote immunity to respiratory syncytial virus infection by augmenting dendritic cell and CD8(+) T cell efficacy. Eur J Immunol 2008, 38:2168-2179.
65. Matthews S.P., Tregoning J.S., Coyle A.J., Hussell T., Openshaw P.J. Role of CCL11 in eosinophilic lung disease during respiratory syncytial virus infection. J Virol 2005, 79:2050-2057.
66. Miller A.L., Strieter R.M., Gruber A.D., Ho S.B., Lukacs N.W. CXCR2 regulates respiratory syncytial virus-induced airway hyperreactivity and mucus overproduction. J Immunol 2003, 170:3348-3356.
67. Miller A.L., Gerard C., Schaller M., Gruber A.D., Humbles A.A., Lukacs N.W. Deletion of CCR1 attenuates pathophysiologic responses during respiratory syncytial virus infection. J Immunol 2006, 176(4):2562-2567.
68. Wenzel S.E. Asthma: defining of the persistent adult phenotypes. Lancet 2006, 368:804-813.
69. Mohapatra S.S., Boyapalle S. Epidemiologic, experimental, and clinical links between respiratory syncytial virus infection and asthma. Clin Microbiol Rev 2008, 21:495-504.
70. Carroll K.N., Wu P., Gebretsadik T., Griffin M.R., Dupont W.D., Mitchel E.F., et al. The severity-dependent relationship of infant bronchiolitis on the risk and morbidity of early childhood asthma. J Allergy Clin Immunol 2009, 123:1055-1061.
71. Sly P.D., Kusel M., Holt P.G. Do early-life viral infections cause asthma?. J Allergy Clin Immunol 2010, [Epub ahead of print].
72. Singh A.M., Moore P.E., Gern J.E., Lemanske R.F., Hartert T.V. Bronchiolitis to asthma: a review and call for studies of gene-virus interactions in asthma causation. Am J Respir Crit Care Med 2007, 175:108-119.
73. Oh J.W., Lee H.B., Park I.K., Kang J.O. Interleukin-6, interleukin-8, interleukin-11, and interferon-gamma levels in nasopharyngeal aspirates from wheezing children with respiratory syncytial virus or influenza A virus infection. Pediatr Allergy Immunol 2002, 13:350-356.
74. Schaller M., Hogaboam C.M., Lukacs N., Kunkel S.L. Respiratory viral infections drive chemokine expression and exacerbate the asthmatic response. J Allergy Clin Immunol 2006, 118:295-302.
75. Matsuse H., Behera A.K., Kumar M., Rabb H., Lockey R.F., Mohapatra S.S. Recurrent respiratory syncytial virus infections in allergen-sensitized mice lead to persistent airway inflammation and hyperresponsiveness. J Immunol 2000, 164:6583-6592.
76. John A.E., Berlin A.A., Lukacs N.W. Respiratory syncytial virus-induced CCL5/RANTES contributes to exacerbation of allergic airway inflammation. Eur J Immunol 2003, 33:1677-1685.
77. Schaller M.A., Kallal L.E., Lukacs N.W. A key role for CC chemokine receptor 1 in T-cell-mediated respiratory inflammation. Am J Pathol 2008, 172:386-394.
78. John A.E., Gerard C.J., Schaller M., Miller A.L., Berlin A.A., Humbles A.A., et al. Respiratory syncytial virus-induced exaggeration of allergic airway disease is dependent upon CCR1-associated immune responses. Eur J Immunol 2005, 35:108-116.
79. Barends M., de Rond L.G., Dormans J., van O.M., Boelen A., Neijens H.J., et al. Respiratory syncytial virus, pneumonia virus of mice, and influenza A virus differently affect respiratory allergy in mice. Clin Exp Allergy 2004, 34:488-496.
80. Dakhama A., Park J.W., Taube C., Joetham A., Balhorn A., Miyahara N., et al. The enhancement or prevention of airway hyperresponsiveness during reinfection with respiratory syncytial virus is critically dependent on the age at first infection and IL-13 production. J Immunol 2005, 175:1876-1883.
81. Pala P., Bjarnason R., Sigurbergsson F., Metcalfe C., Sigurs N., Openshaw P.J. Enhanced IL-4 responses in children with a history of respiratory syncytial virus bronchiolitis in infancy. Eur Respir J 2002, 20:376-382.
82. Dakhama A., Lee Y.M., Ohnishi H., Jing X., Balhorn A., Takeda K., et al. Virus-specific IgE enhances airway responsiveness on reinfection with respiratory syncytial virus in newborn mice. J Allergy Clin Immunol 2009, 123:138-145.
83. Siegle J.S., Hansbro N., Herbert C., Rosenberg H.F., Domachowske J.B., Asquith K.L., et al. Early-life viral infection and allergen exposure interact to induce an asthmatic phenotype in mice. Respir Res 2010, 11:14.
84. Schwarze J., Cieslewicz G., Hamelmann E., Joetham A., Shultz L., Lamers M., et al. IL-5 and eosinophils are essential for the development of airway hyperresponsiveness following acute respiratory syncytial virus infection. J Immunol 1999, 162:2997-3004.
85. Truyen E., Coteur L., Dilissen E., Overbergh L., Dupont L., Ceuppens J., et al. Evaluation of airway inflammation by quantitative Th1/Th2 cytokine mRNA measurement in sputum of asthma patients. Thorax 2006, 61:202-208.
86. van Schaik S.M., Tristram D.A., Nagpal I.S., Hintz K.M., Welliver R.C., Welliver R.C. Increased production of IFN-γ and cysteinyl leukotrienes in virus-induced wheezing. J Allergy Clin Immunol 1999, 103:630-636.
87. Douville R.N., Bastien N., Li Y., Simons F.E.R., Hayqlass K.T. Adult asthmatics display exaggerated IFN-γ responses to human metapneumovirus and respiratory syncytial virus. Biochem Cell Biol 2007, 85:252-258.
88. Hirose H., Matsuse H., Tsuchida T., Fukahori S., Fukushima C., Mizuta Y., et al. Cytokine production from peripheral blood mononuclear cells of mite allergen-sensitized atopic adults stimulated with respiratory syncytial virus and mite allergen. Int Arch Allergy Immunol 2008, 146:149-155.
89. Chabaud M., Fossiez F., Taupin J.L., Miossec P. Enhancing effect of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor pro duction by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines. J Immunol 1998, 161:409-414.
90. Matusevicius D., Kivisakk P., He B., Kostulas N., Ozenci V., Fredrikson S. Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis. Mult Scler 1999, 5:101-104.
91. Agache I., Ciobanu C., Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med 2010, 104(8):1131-1137.
92. Hellings P.W., Kasran A., Liu Z., Vandekerckhove P., Wuyts A., Overbergh L., et al. Interleukin-17 orchestrates the granulocyte influx into airways after allergen inhalation in a mouse model of allergic asthma. Am J Respir Cell Mol Biol 2003, 28:42-50.
93. Zhao Y., Yang J., Gao Y., Guo W.T. H17 immunity in patients with allergic asthma. Int Arch Allergy Immunol 2010, 151:297-307.
94. Park S.J., Lee K.S., Kim S.R., Min K.H., Moon H., Lee M.H., et al. Phosphoinositide 3-kinase delta inhibitor suppresses IL-17 expression in a murine asthma model. Eur Respir J 2010, [Epub ahead of print].
95. Nakae S., Komiyama Y., Nambu A., Sudo K., Iwase M., Homma I., et al. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002, 17:375-387.
96. Laan M., Cui Z.H., Hoshino H., Lotvall J., Sjostrand M., Gruenert D.C., et al. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol 1999, 162:2347-2352.
97. Jones C.E., Chan K. Interleukin-17 stimulates the expression of interleukin-8, growth-related oncogene-α, and granulocyte-colony-stimulating factor by human airway epithelial cells. Am J Respir Cell Mol Biol 2002, 26(6):748-753.
98. Hashimoto K., Graham B.S., Ho S.B., Adler K.B., Collins R.D., Olson S.J., et al. Respiratory syncytial virus in allergic lung inflammation increases Muc5ac and Gob-5. Am J Respir Crit Care Med 2004, 170:306-312.
99. Hashimoto K., Durbin J.E., Zhou W., Collins R.D., Ho S.B., Kolls J.K., et al. Respiratory syncytial virus infection in the absence of STAT 1 results in airway dysfunction, airway mucus, and augmented IL-17 levels. J Allergy Clin Immunol 2005, 116(3):550-557.