Cellular and humoral immunity of virus-induced asthma

Frontiers in Microbiology

Volumn 4, Issue AUG, 2013, Pages

  Okayama, Yoshimichi ^a  

^a NIHON UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cellular immunity; Human rhinovirus; Humoral immunity; Respiratory syncytial virus; Virus induced asthma

Indexed keywords

CD11B ANTIGEN; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 8; INTERLEUKIN 9; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OX40 LIGAND; PALIVIZUMAB; RANTES; STAT PROTEIN; THYMIC STROMAL LYMPHOPOIETIN; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; VITAMIN D RECEPTOR;

ARTICLE; ASTHMA; BRONCHIOLITIS; CELLULAR IMMUNITY; DENDRITIC CELL; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; HUMAN RHINOVIRUS; HUMORAL IMMUNITY; INNATE IMMUNITY; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY TRACT ALLERGY; SINGLE NUCLEOTIDE POLYMORPHISM;

HUMAN RHINOVIRUS SP.; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 84884221102     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00252     Document Type: Article

References (76)

1. Aberle, J. H., Aberle, S. W., Dworzak, M. N., Mandl, C. W., Rebhandl, W., Vollnhofer, G., et al. (1999). Reduced interferon-gamma expression in peripheral blood mononuclear cells of infants with severe respiratory syncytial virus disease. Am. J. Respir. Crit. Care Med. 160, 126-31268. doi: 10.1164/ajrccm.160.4.9812025
2. Bartlett, N. W., Walton, R. P., Edwards, M. R., Aniscenko, J., Caramori, G., Zhu, J., et al. (2008). Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation. Nat. Med. 14, 199-204. doi: 10.1038/nm1713
3. Bendelja, K., Gagro, A., Bace, A., Lokar-Kolbas, R., Krsulovic-Hresic, V., Drazenovic, V., et al. (2000). Predominant type-2 response in infants with respiratory syncytial virus (RSV) infection demonstrated by cytokine flow cytometry. Clin. Exp. Immunol. 121, 332-338. doi: 10.1046/j.1365-2249.2000.01297.x
4. Bennett, B. L., Garofalo, R. P., Cron, S. G., Hosakote, Y. M., Atmar, R. L., Macias, C. G., et al. (2007). Immunopathogenesis of respiratory syncytial virus bronchiolitis. J. Infect. Dis. 195, 1532-1540. doi: 10.1086/515575
5. Bermejo-Martin, J. F., Garcia-Arevalo, M. C., De Lejarazu, R. O., Ardura, J., Eiros, J. M., Alonso, A., et al. (2007). 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. 18, 162-167.
6. Bont, L., Heijnen, C. J., Kavelaars, A., van Aalderen, W. M., Brus, F., Draaisma, J., et al. (1999). Peripheral blood cytokine responses and disease severity in respiratory syncytial virus bronchiolitis. Eur. Respir. J. 14, 144-149. doi: 10.1034/j.1399-3003.1999.14a24.x
7. Bont, L., Heijnen, C. J., Kavelaars, A., van Aalderen, W. M., Brus, F., Draaisma, J., et al. (2001). Local interferon-gamma levels during respiratory syncytial virus lower respiratory tract infection are associated with disease severity. J. Infect. Dis. 184, 355-358. doi: 10.1086/322035
8. Brandenburg, A. H., Groen, J., van Steensel-Moll, H. A., Claas, E. C., Rothbarth, P. H., Neijens, H. J., et al. (1997). Respiratory syncytial virus specific serum antibodies in infants under six months of age: limited serological response upon infection. J. Med. Virol. 52, 97-104. doi: 10.1002/(SICI)1096-9071(199705)52:1
9. Bui, R. H., Molinaro, G. A., Kettering, J. D., Heiner, D. C., Imagawa, D. T., and St Geme, J. W. Jr. (1987). Virus-specific IgE and IgG4 antibodies in serum of children infected with respiratory syncytial virus. J. Pediatr. 110, 87-90. doi: 10.1016/S0022-3476(87)80295-0
10. Caliskan, M., Bochkov, Y. A., Kreiner-Moller, E., Bonnelykke, K., Stein, M. M., Du, G., et al. (2013). Rhinovirus wheezing illness and genetic risk of childhood-onset asthma. N. Engl. J. Med. 368, 1398-1407. doi: 10.1056/NEJMoa1211592
11. Chavez-Bueno, S., Mejias, A., Gomez, A. M., Olsen, K. D., Rios, A. M., Fonseca-Aten, M., et al. (2005). Respiratory syncytial virus-induced acute and chronic airway disease is independent of genetic background: an experimental murine model. Virol. J. 2, 46. doi: 10.1186/1743-422X-2-46
12. Culley, F. J., Pollott, J., and Openshaw, P. J. (2002). Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J. Exp. Med. 196, 1381-1386. doi: 10.1084/jem.20020943
13. Dakhama, A., Lee, Y. M., Ohnishi, H., Jing, X., Balhorn, A., Takeda, K., et al. (2009). Virus-specific IgE enhances airway responsiveness on reinfection with respiratory syncytial virus in newborn mice. J. Allergy Clin. Immunol. 123, 138-145.e135. doi: 10.1016/j.jaci.2008.10.012
14. Dakhama, A.,Park, J. W., Taube, C., Joetham, A., Balhorn, A., Miyahara, N., et al. (2005). 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. 175, 1876-1883.
15. De Alarcon, A., Walsh, E. E., Carper, H. T., La Russa, J. B., Evans, B. A., Rakes, G. P., et al. (2001). Detection of IgA and IgG but not IgE antibody to respiratory syncytial virus in nasal washes and sera from infants with wheezing. J. Pediatr. 138, 311-317. doi: 10.1067/mpd.2001.111277
16. Delgado, M. F., Coviello, S., Monsalvo, A. C., Melendi, G. A., Hernandez, J. Z., Batalle, J. P., et al. (2009). Lack of antibody affinity maturation due to poor Toll-like receptor stimulation leads to enhanced respiratory syncytial virus disease. Nat. Med. 15, 34-41. doi: 10.1038/nm.1894
17. Durbin, J. E., Johnson, T. R., Durbin, R. K., Mertz, S. E., Morotti, R. A., Peebles, R. S., et al. (2002). The role of IFN in respiratory syncytial virus pathogenesis. J. Immunol. 168, 2944-2952.
18. Durrani, S. R., Montville, D. J., Pratt, A. S., Sahu, S., DeVries, M. K., Rajamanickam, V., et al. (2012). Innate immune responses to rhinovirus are reduced by the high -affinity IgE receptor in allergic asthmatic children. J. Allergy Clin. Immunol. 130, 489-495. doi: 10.1016/j.jaci.2012.05.023
19. Feltes, T. F., Cabalka, A. K., Meissner, H. C., Piazza, F. M., Carlin, D. A., Top, F. H., et al. (2003). Palivizumab prophylaxis reduces hospitalization due to respiratory syncytial virus in young children with hemodynamically significant congenital heart disease. J. Pediatr. 143, 532-540. doi: 10.1067/S0022-3476(03)00454-2
20. Fitzpatrick, A. M., Teague, W. G., Meyers, D. A., Peters, S. P., Li, X., Li, H., et al. (2011). Heterogeneity of severe asthma in childhood: confirmation by cluster analysis of children in the National Institutes of Health/National Heart, Lung, and Blood Institute Severe Asthma Research Program. J. Allergy Clin. Immunol. 127, 382-389.e381-313. doi: 10.1016/j.jaci.2010.11.015
21. Garcia, C., Soriano-Fallas, A., Lozano, J., Leos, N., Gomez, A. M., Ramilo, O., et al. (2012). Decreased innate immune cytokine responses correlate with disease severity in children with respiratory syncytial virus and human rhinovirus bronchiolitis. Pediatr. Infect. Dis. J. 31, 86-89. doi: 10.1097/INF.0b013e31822dc8c1
22. Garofalo, R. P., Patti, J., Hintz, K. A., Hill, V., Ogra, P. L., and Welliver, R. C. (2001). Macrophage inflammatory protein-1alpha (not T helper type 2 cytokines) is associated with severe forms of respiratory syncytial virus bronchiolitis. J. Infect. Dis. 184, 393-399. doi: 10.1086/322788
23. Glezen, W. P., Paredes, A., Allison, J. E., Taber, L. H., and Frank, A. L. (1981). Risk of respiratory syncytial virus infection for infants from low-income families in relationship to age, sex, ethnic group, and maternal antibody level. J. Pediatr. 98, 708-715. doi: 10.1016/S0022-3476(81)80829-3
24. Han, J., Dakhama, A., Jia, Y., Wang, M., Zeng, W., Takeda, K., et al. (2012). Responsiveness to respiratory syncytial virus in neonates is mediated through thymic stromal lymphopoietin and OX40 ligand. J. Allergy Clin. Immunol. 130, 1175-1186.e1179. doi: 10.1016/j.jaci.2012.08.033
25. Heilman, C. A. (1990). From the National Institute of Allergy and Infectious Diseases and the World Health Organization. Respiratory syncytial and parainfluenza viruses. J. Infect. Dis. 161, 402-406. doi: 10.1093/infdis/161.3.402
26. Henderson, F. W., Clyde, W. A. Jr., Collier, A. M., Denny, F. W., Senior, R. J., Sheaffer, C. I., et al. (1979). The etiologic and epidemiologic spectrum of bronchiolitis in pediatric practice. J. Pediatr. 95, 183-190. doi: 10.1016/S0022-3476(79)80647-2
27. Holberg, C. J., Wright, A. L., Martinez, F. D., Ray, C. G., Taussig, L. M., and Lebowitz, M. D. (1991). Risk factors for respiratory syncytial virus-associated lower respiratory illnesses in the first year of life. Am. J. Epidemiol. 133, 1135-1151.
28. Huckabee, M. M., and Peebles, R. S. Jr. (2009). Novel concepts in virally induced asthma. Clin. Mol. Allergy 7, 2. doi: 10.1186/1476-7961-7-2
29. Jackson, D. J., Evans, M. D., Gangnon, R. E., Tisler, C. J., Pappas, T. E., Lee, W., et al. (2013). Evidence for a causal relationship between allergic sensitization and rhinovirus wheezing in early life. Am. J. Respir. Crit. Care Med. 185, 281-285. doi: 10.1164/rccm.201104-0660OC
30. Jackson, D. J., Gangnon, R. E., Evans, M. D., Roberg, K. A., Anderson, E. L., Pappas, T. E., et al. (2008). Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am. J. Respir. Crit. Care Med. 178, 667-672. doi: 10.1164/rccm.200802-309OC
31. Janssen, R., Bont, L., Siezen, C. L., Hodemaekers, H. M., Ermers, M. J., Doornbos, G., et al. (2007). Genetic susceptibility to respiratory syncytial virus bronchiolitis is predominantly associated with innate immune genes. J. Infect. Dis. 196, 826-834. doi: 10.1086/520886
32. Joshi, P., Shaw, A., Kakakios, A., and Isaacs, D. (2003). Interferon-gamma levels in nasopharyngeal secretions of infants with respiratory syncytial virus and other respiratory viral infections. Clin. Exp. Immunol. 131, 143-147. doi: 10.1046/j.1365-2249.2003.02039.x
33. Kato, A., Favoreto, S. Jr., Avila, P. C., and Schleimer, R. P. (2007). TLR3- and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells. J. Immunol. 179, 1080-1087.
34. Krishnamoorthy, N., Khare, A., Oriss, T. B., Raundhal, M., Morse, C., Yarlagadda, M., et al. (2012). Early infection with respiratory syncytial virus impairs regulatory T cell function and increases susceptibility to allergic asthma. Nat. Med. 18, 1525-1530. doi: 10.1038/nm.2896
35. Kristjansson, S., Bjarnarson, S. P., Wennergren, G., Palsdottir, A. H., Arnadottir, T., Haraldsson, A., et al. (2005). Respiratory syncytial virus and other respiratory viruses during the first 3 months of life promote a local TH2-like response. J. Allergy Clin. Immunol. 116, 805-811. doi: 10.1016/j.jaci.2005.07.012
36. Kusel, M. M.,de Klerk, N. H., Kebadze, T., Vohma, V., Holt, P. G., Johnston, S. L., et al. (2007). Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J. Allergy Clin. Immunol. 119, 1105-1110. doi: 10.1016/j.jaci.2006.12.669
37. Lee, Y. M., Miyahara, N., Takeda, K., Prpich, J., Oh, A., Balhorn, A., et al. (2008). IFN-gamma production during initial infection determines the outcome of reinfection with respiratory syncytial virus. Am. J. Respir. Crit. Care Med. 177, 208-218. doi: 10.1164/rccm.200612-1890OC
38. Legg, J. P., Hussain, I. R., Warner, J. A., Johnston, S. L., and Warner, J. O. (2003). Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am. J. Respir. Crit. Care Med. 168, 633-639. doi: 10.1164/rccm.200210-1148OC
39. Legge, K. L., and Braciale, T. J. (2003). Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18, 265-277. doi: 10.1016/S1074-7613(03)00023-2
40. Lemanske, R. F. Jr., Jackson, D. J., Gangnon, R. E., Evans, M. D., Li, Z., Shult, P. A., et al. (2005). Rhinovirus illnesses during infancy predict subsequent childhood wheezing. J. Allergy Clin. Immunol. 116, 571-577. doi: 10.1016/j.jaci.2005.06.024
41. Martinez, F. D. (2003). Respiratory syncytial virus bronchiolitis and the pathogenesis of childhood asthma. Pediatr. Infect. Dis. J. 22(Suppl. 2), S76-S82. doi: 10.1097/01.inf.0000053889.39392.a7
42. Message, S. D., Laza-Stanca, V., Mallia, P., Parker, H. L., Zhu, J., Kebadze, T., et al. (2008). Rhinovirus-induced lower respiratory illness is increased in asthma and related to virus load and Th1/2 cytokine and IL-10 production. Proc. Natl. Acad. Sci. U.S.A. 105, 13562-13567. doi: 10.1073/pnas.0804181105
43. Mold, J. E., Michaelsson, J., Burt, T. D., Muench, M. O., Beckerman, K. P., Busch, M. P., et al. (2008). Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322, 1562-1565. doi: 10.1126/science.1164511
44. Mold, J. E., Venkatasubrahmanyam, S., Burt, T. D., Michaelsson, J., Rivera, J. M., Galkina, S. A., et al. (2010). Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science 330, 1695-1699. doi: 10.1126/science.1196509
45. Murphy, B. R., Alling, D. W., Snyder, M. H., Walsh, E. E., Prince, G. A., Chanock, R. M., et al. (1986). Effect of age and preexisting antibody on serum antibody response of infants and children to the F and G glycoproteins during respiratory syncytial virus infection. J. Clin. Microbiol. 24, 894-898.
46. Ochola, R., Sande, C., Fegan, G., Scott, P. D., Medley, G. F., Cane, P. A., et al. (2009). The level and duration of RSV-specific maternal IgG in infants in Kilifi Kenya. PLoS ONE 4:e8088. doi: 10.1371/journal.pone.0008088
47. Pala, P., Bjarnason, R., Sigurbergsson, F., Metcalfe, C., Sigurs, N., and Openshaw, P. J. (2002). Enhanced IL-4 responses in children with a history of respiratory syncytial virus bronchiolitis in infancy. Eur. Respir. J. 20, 376-382. doi: 10.1183/09031936.02.00249902
48. Peebles, R. S. Jr., Sheller, J. R., Collins, R. D., Jarzecka, A. K., Mitchell, D. B., Parker, R. A., et al. (2001). Respiratory syncytial virus infection does not increase allergen-induced type 2 cytokine production, yet increases airway hyperresponsiveness in mice. J. Med. Virol. 63, 178-188. doi: 10.1002/1096-9071(20000201)63:2
49. Piedra, P. A., Jewell, A. M., Cron, S. G., Atmar, R. L., and Glezen, W. P. (2003). Correlates of immunity to respiratory syncytial virus (RSV) associatedhospitalization: establishment of minimum protective threshold levels of serum neutralizing antibodies. Vaccine 21, 3479-3482. doi: 10.1016/S0264-410X(03) 00355-4
50. Polte, T., and Hansen, G. (2008). Maternal tolerance achieved during pregnancy is transferred to the offspring via breast milk and persistently protects the offspring from allergic asthma. Clin. Exp. Allergy 38, 1950-1958. doi: 10.1111/j.1365-2222.2008.03096.x
51. Rabatic, S., Gagro, A., Lokar-Kolbas, R., Krsulovic-Hresic, V., Vrtar, Z., Popow-Kraupp, T., et al. (1997). Increase in CD23+ B cells in infants with bronchiolitis is accompanied by appearance of IgE and IgG4 antibodies specific for respiratory syncytial virus. J. Infect. Dis. 175, 32-37. doi: 10.1093/infdis/175.1.32
52. Rakes, G. P., Arruda, E., Ingram, J. M., Hoover, G. E., Zambrano, J. C., Hayden, F. G., et al. (1999). Rhinovirus and respiratory syncytial virus in wheezing children requiring emergency care. IgE and eosinophil analyses. Am. J. Respir. Crit. Care Med. 159, 785-790. doi: 10.1164/ajrccm.159.3.9801052
53. Renzi, P. M., Turgeon, J. P., Marcotte, J. E., Drblik, S. P., Berube, D., Gagnon, M. F., et al. (1999). Reduced interferon-gamma production in infants with bronchiolitis and asthma. Am. J. Respir. Crit. Care Med. 159(5 Pt 1), 1417-1422. doi: 10.1164/ajrccm.159.5.9805080
54. Renzi, P. M., Turgeon, J. P., Yang, J. P., Drblik, S. P., Marcotte, J. E., Pedneault, L., et al. (1997). Cellular immunity is activated and a TH-2 response is associated with early wheezing in infants after bronchiolitis. J. Pediatr. 130, 584-593. doi: 10.1016/S0022-3476(97)70243-9
55. Roca, A., Abacassamo, F., Loscertales, M. P., Quinto, L., Gomez-Olive, X., Fenwick, F., et al. (2002). Prevalence of respiratory syncytial virus IgG antibodies in infants living in a rural area of Mozambique. J. Med. Virol. 67, 616-623. doi: 10.1002/jmv.10148
56. Roman, M., Calhoun, W. J., Hinton, K. L., Avendano, L. F., Simon, V., Escobar, A. M., et al. (1997). Respiratory syncytial virus infection in infants is associated with predominant Th-2-like response. Am. J. Respir. Crit. Care Med. 156, 190-195. doi: 10.1164/ajrccm.156.1.9611050
57. Russi, J. C.,Delfraro, A., Borthagaray, M. D., Velazquez, B., Garcia-Barreno, B., and Hortal, M. (1993). Evaluation of immunoglobulin E-specific antibodies and viral antigens in nasopharyngeal secretions of children with respiratory syncytial virus infections. J. Clin. Microbiol. 31, 819-823.
58. Schauer, U., Hoffjan, S., Bittscheidt, J., Kochling, A., Hemmis, S., Bongartz, S., et al. (2002). RSV bronchiolitis and risk of wheeze and allergic sensitisation in the first year of life. Eur. Respir. J. 20, 1277-1283. doi: 10.1183/09031936.02.00019902
59. Sigurs, N., Bjarnason, R., Sigurbergsson, F., and Kjellman, B. (2000). Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am. J. Respir. Crit. Care Med. 161, 1501-1507. doi: 10.1164/ajrccm.161.5.9906076
60. Simoes, E. A., Carbonell-Estrany, X., Rieger, C. H., Mitchell, I., Fredrick, L., and Groothuis, J. R. (2010). The effect of respiratory syncytial virus on subsequent recurrent wheezing in atopic and nonatopic children. J. Allergy Clin. Immunol. 126, 256-262. doi: 10.1016/j.jaci.2010.05.026
61. Simoes, E. A., Groothuis, J. R., Carbonell-Estrany, X., Rieger, C. H., Mitchell, I., Fredrick, L. M., et al. (2007). Palivizumab prophylaxis, respiratory syncytial virus, and subsequent recurrent wheezing. J. Pediatr. 151, 34-42, 42.e31.
62. Sly, P. D., Boner, A. L., Bjorksten, B., Bush, A., Custovic, A., Eigenmann, P. A., et al. (2008). Early identification of atopy in the prediction of persistent asthma in children. Lancet 372, 1100-1106. doi: 10.1016/S0140-6736(08)61451-8
63. Stensballe, L. G., Ravn, H., Kristensen, K., Agerskov, K., Meakins, T., Aaby, P., et al. (2009). Respiratory syncytial virus neutralizing antibodies in cord blood, respiratory syncytial virus hospitalization, and recurrent wheeze. J. Allergy Clin. Immunol. 123, 398-403. doi: 10.1016/j.jaci.2008.10.043
64. Stern, D. A., Morgan, W. J., Halonen, M., Wright, A. L., and Martinez, F. D. (2008). Wheezing and bronchial hyper-responsiveness in early childhood as predictors of newly diagnosed asthma in early adulthood: a longitudinal birth-cohort study. Lancet 372, 1058-1064. doi: 10.1016/S0140-6736(08)61447-6
65. Subrata, L. S., Bizzintino, J., Mamessier, E., Bosco, A., McKenna, K. L., Wikstrom, M. E., et al. (2009). Interactions between innate antiviral and atopic immunoinflammatory pathways precipitate and sustain asthma exacerbations in children. J. Immunol. 183, 2793-2800. doi: 10.4049/jimmunol.0900695
66. Tekkanat, K. K., Maassab, H., Berlin, A. A., Lincoln, P. M., Evanoff, H. L., Kaplan, M. H., et al. (2001). Role of interleukin-12 and stat-4 in the regulation of airway inflammation and hyperreactivity in respiratory syncytial virus infection. Am. J. Pathol. 159, 631-638. doi: 10.1016/S0002-9440(10)61734-8
67. van der Sande, M. A., Kidd, I. M., Goetghebuer, T., Martynoga, R. A., Magnusen, A., Allen, S., et al. (2002). Severe respiratory syncytial virus infection in early life is associated with increased type 2 cytokine production in Gambian children. Clin. Exp. Allergy 32, 1430-1435. doi: 10.1046/j.1365-2745.2002.01521.x
68. Verhasselt, V., Milcent, V., Cazareth, J., Kanda, A., Fleury, S., Dombrowicz, D., et al. (2008). Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nat. Med. 14, 170-175. doi: 10.1038/nm1718
69. Wang, S. Z., Bao, Y. X., Rosenberger, C. L., Tesfaigzi, Y., Stark, J. M., and Harrod, K. S. (2004). IL-12p40 and IL-18 modulate inflammatory and immune responses to respiratory syncytial virus infection. J. Immunol. 173, 4040-4049.
70. Wark, P. A., Johnston, S. L., Bucchieri, F., Powell, R., Puddicombe, S., Laza-Stanca, V., et al. (2005). Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J. Exp. Med. 201, 937-947. doi: 10.1084/jem.20041901
71. Weitkamp, J. H., Lafleur, B. J., Greenberg, H. B., and Crowe, J. E. Jr. (2005). Natural evolution of a human virus-specific antibody gene repertoire by somatic hypermutation requires both hotspot-directed and randomly-directed processes. Hum. Immunol. 66, 666-676. doi: 10.1016/j.humimm.2005.02.008
72. Welliver, R. C., Sun, M., Hildreth, S. W., Arumugham, R., and Ogra, P. L. (1989). Respiratory syncytial virus-specific antibody responses in immunoglobulin A and E isotypes to the F and G proteins and to intact virus after natural infection. J. Clin. Microbiol. 27, 295-299.
73. Welliver, R. C., Wong, D. T., Sun, M., Middleton, E. Jr., Vaughan, R. S., and Ogra, P. L. (1981). The development of respiratory syncytial virus-specific IgE and the release of histamine in nasopharyngeal secretions after infection. N. Engl. J. Med. 305, 841-846. doi: 10.1056/NEJM198110083051501
74. Wilczynski, J., Lukasik, B., Torbicka, E., Tranda, I., and Brzozowska-Binda, A. (1994). The immune response of small children by antibodies of different classes to respiratory syncytial virus (RSV) proteins. Acta Microbiol. Pol. 43, 369-379.
75. Williams, J. V., Weitkamp, J. H., Blum, D. L., LaFleur, B. J., and Crowe, J. E. Jr. (2009). The human neonatal B cell response to respiratory syncytial virus uses a biased antibody variable gene repertoire that lacks somatic mutations. Mol. Immunol. 47, 407-414. doi: 10.1016/j.molimm.2009.08.024
76. Wos, M., Sanak, M., Soja, J., Olechnowicz, H., Busse, W. W., and Szczeklik, A. (2008). The presence of rhinovirus in lower airways of patients with bronchial asthma. Am. J. Respir. Crit. Care Med. 177, 1082-1089. doi: 10.1164/rccm.200607-973OC