Respiratory Syncytial Virus Infections in the Adult Asthmatic - Mechanisms of Host Susceptibility and Viral Subversion

Immunology and Allergy Clinics of North America

Volumn 30, Issue 4, 2010, Pages 523-539

  Westerly, Blair D ^a   Peebles, R Stokes ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adults; Asthma; Respiratory syncytial virus; Wheezing

Indexed keywords

CORTICOSTEROID; CYTOKINE;

ADULT; ASTHMA; CELL TYPE; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; DISEASE PREDISPOSITION; GENOTYPE; HOST RESISTANCE; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IN VITRO STUDY; INFECTION SENSITIVITY; MEDIATOR RELEASE; MORBIDITY; NONHUMAN; PATHOGENESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; REVIEW; SENSITIVITY AND SPECIFICITY; VIRAL BRONCHIOLITIS; VIRUS CELL INTERACTION; VIRUS DETECTION; VIRUS LOAD;

ADULT; ASTHMA; HUMANS; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES;

EID: 77958478339     PISSN: 08898561     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.iac.2010.08.006     Document Type: Review

References (101)

1. Sigurs N., Gustafsson P.M., Bjarnason R., et al. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am J Respir Crit Care Med 2005, 171(2):137-141.
2. Stein R.T., Sherrill D., Morgan W.J., et al. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet 1999, 354(9178):541-545. [see comments].
3. Falsey A.R., Hennessey P.A., Formica M.A., et al. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 2005, 352(17):1749-1759.
4. Beasley R., Coleman E.D., Hermon Y., et al. Viral respiratory tract infection and exacerbations of asthma in adult patients. Thorax 1988, 43(9):679-683.
5. Glezen W.P., Greenberg S.B., Atmar R.L., et al. Impact of respiratory virus infections on persons with chronic underlying conditions. JAMA 2000, 283(4):499-505.
6. Harju T.H., Leinonen M., Nokso-Koivisto J., et al. Pathogenic bacteria and viruses in induced sputum or pharyngeal secretions of adults with stable asthma. Thorax 2006, 61(7):579-584.
7. Teichtahl H., Buckmaster N., Pertnikovs E. The incidence of respiratory tract infection in adults requiring hospitalization for asthma. Chest 1997, 112(3):591-596.
8. Nicholson K.G., Kent J., Ireland D.C. Respiratory viruses and exacerbations of asthma in adults. BMJ 1993, 307(6910):982-986.
9. Sokhandan M., McFadden E.R.J., Huang Y.T., et al. The contribution of respiratory viruses to severe exacerbations of asthma in adults. Chest 1995, 107(6):1570-1574. [see comments].
10. Ayres J.G., Noah N.D., Fleming D.M. Incidence of episodes of acute asthma and acute bronchitis in general practice 1976-87. Br J Gen Pract 1993, 43(374):361-364.
11. Pattemore P.K., Johnston S.L., Bardin P.G. Viruses as precipitants of asthma symptoms. I. Epidemiology. Clin Exp Allergy 1992, 22(3):325-336.
12. Abramson M., Pearson L., Kutin J., et al. Allergies, upper respiratory tract infections, and asthma. J Asthma 1994, 31(5):367-374.
13. Dowell S.F., Anderson L.J., Gary H.E.J., et al. Respiratory syncytial virus is an important cause of community- acquired lower respiratory infection among hospitalized adults. J Infect Dis 1996, 174(3):456-462.
14. Fleming D.M., Cross K.W. Respiratory syncytial virus or influenza?. Lancet 1993, 342(8886-8887):1507-1510.
15. Griffin M.R., Coffey C.S., Neuzil K.M., et al. Winter viruses: influenza- and respiratory syncytial virus-related morbidity in chronic lung disease. Arch Intern Med 2002, 162(11):1229-1236.
16. Hall C.B., Long C.E., Schnabel K.C. Respiratory syncytial virus infections in previously healthy working adults. Clin Infect Dis 2001, 33(6):792-796.
17. Moineddin R., Nie J.X., Domb G., et al. Seasonality of primary care utilization for respiratory diseases in Ontario: a time-series analysis. BMC Health Serv Res 2008, 8:160.
18. Thompson W.W., Shay D.K., Weintraub E., et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003, 289(2):179-186.
19. Zambon M.C., Stockton J.D., Clewley J.P., et al. Contribution of influenza and respiratory syncytial virus to community cases of influenza-like illness: an observational study. Lancet 2001, 358(9291):1410-1416.
20. Guidry G.G., Black-Payne C.A., Payne D.K., et al. Respiratory syncytial virus infection among intubated adults in a university medical intensive care unit. Chest 1991, 100(5):1377-1384.
21. Duncan C.B., Walsh E.E., Peterson D.R., et al. Risk factors for respiratory failure associated with respiratory syncytial virus infection in adults. J Infect Dis 2009, 200(8):1242-1246.
22. Gill M.A., Palucka A.K., Barton T., et al. Mobilization of plasmacytoid and myeloid dendritic cells to mucosal sites in children with respiratory syncytial virus and other viral respiratory infections. J Infect Dis 2005, 191(7):1105-1115.
23. Gill M.A., Long K., Kwon T., et al. Differential recruitment of dendritic cells and monocytes to respiratory mucosal sites in children with influenza virus or respiratory syncytial virus infection. J Infect Dis 2008, 198(11):1667-1676.
24. Henderson F.W., Collier A.M., Clyde W.A., et al. Respiratory-syncytial-virus infections, reinfections and immunity. A prospective, longitudinal study in young children. N Engl J Med 1979, 300(10):530-534.
25. Popow-Kraupp T., Lakits E., Kellner G., et al. Immunoglobulin-class-specific immune response to respiratory syncytial virus structural proteins in infants, children, and adults. J Med Virol 1989, 27(3):215-223.
26. Falsey A.R., Singh H.K., Walsh E.E. Serum antibody decay in adults following natural respiratory syncytial virus infection. J Med Virol 2006, 78(11):1493-1497.
27. Lee F.E., Walsh E.E., Falsey A.R., et al. Experimental infection of humans with A2 respiratory syncytial virus. Antiviral Res 2004, 63(3):191-196.
28. Mills J., Van Kirk J.E., Wright P.F., et al. Experimental respiratory syncytial virus infection of adults. Possible mechanisms of resistance to infection and illness. J Immunol 1971, 107(1):123-130.
29. Walsh E.E., Falsey A.R. Humoral and mucosal immunity in protection from natural respiratory syncytial virus infection in adults. J Infect Dis 2004, 190(2):373-378.
30. Hall C.B., Walsh E.E., Long C.E., et al. Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis 1991, 163(4):693-698.
31. Falsey A.R., Walsh E.E., Looney R.J., et al. Comparison of respiratory syncytial virus humoral immunity and response to infection in young and elderly adults. J Med Virol 1999, 59(2):221-226.
32. Walsh E.E., Falsey A.R. Age related differences in humoral immune response to respiratory syncytial virus infection in adults. J Med Virol 2004, 73(2):295-299.
33. Falsey A.R., McCann R.M., Hall W.J., et al. Acute respiratory tract infection in daycare centers for older persons. J Am Geriatr Soc 1995, 43(1):30-36.
34. Gardner E.M., Murasko D.M. Age-related changes in Type 1 and Type 2 cytokine production in humans. Biogerontology 2002, 3(5):271-290.
35. Looney R.J., Falsey A.R., Walsh E., et al. Effect of aging on cytokine production in response to respiratory syncytial virus infection. J Infect Dis 2002, 185(5):682-685.
36. Po J.L., Gardner E.M., Anaraki F., et al. Age-associated decrease in virus-specific CD8+ T lymphocytes during primary influenza infection. Mech Ageing Dev 2002, 123(8):1167-1181.
37. Zhang Y., Luxon B.A., Casola A., et al. Expression of respiratory syncytial virus-induced chemokine gene networks in lower airway epithelial cells revealed by cDNA microarrays. J Virol 2001, 75(19):9044-9058.
38. Falsey A.R., Walsh E.E. Humoral immunity to respiratory syncytial virus infection in the elderly. J Med Virol 1992, 36(1):39-43.
39. Walsh E.E., Peterson D.R., Falsey A.R. Risk factors for severe respiratory syncytial virus infection in elderly persons. J Infect Dis 2004, 189(2):233-238.
40. Terrosi C., Di G.G., Martorelli B., et al. Humoral immunity to respiratory syncytial virus in young and elderly adults. Epidemiol Infect 2009, 137(12):1684-1686.
41. Ostler T., Davidson W., Ehl S. Virus clearance and immunopathology by CD8(+) T cells during infection with respiratory syncytial virus are mediated by IFN-gamma. Eur J Immunol 2002, 32(8):2117-2123.
42. Cherrie A.H., Anderson K., Wertz G.W., et al. Human cytotoxic T cells stimulated by antigen on dendritic cells recognize the N, SH, F, M, 22K, and 1b proteins of respiratory syncytial virus. J Virol 1992, 66(4):2102-2110.
43. Lee F.E., Walsh E.E., Falsey A.R., et al. The balance between influenza- and RSV-specific CD4 T cells secreting IL-10 or IFNgamma in young and healthy-elderly subjects. Mech Ageing Dev 2005, 126(11):1223-1229.
44. Effros R.B. Replicative senescence of CD8 T cells: effect on human ageing. Exp Gerontol 2004, 39(4):517-524.
45. de Bree G.J., Heidema J., van Leeuwen E.M., et al. Respiratory syncytial virus-specific CD8+ memory T cell responses in elderly persons. J Infect Dis 2005, 191(10):1710-1718.
46. Anderson L.J., Tsou C., Potter C., et al. Cytokine response to respiratory syncytial virus stimulation of human peripheral blood mononuclear cells. J Infect Dis 1994, 170(5):1201-1208.
47. Noah T.L., Becker S. Chemokines in nasal secretions of normal adults experimentally infected with respiratory syncytial virus. Clin Immunol 2000, 97(1):43-49.
48. Groskreutz D.J., Monick M.M., Powers L.S., et al. 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(3):1733-1740.
49. Zhang Y., Wang Y., Gilmore X., et al. An aged mouse model for RSV infection and diminished CD8(+) CTL responses. Exp Biol Med (Maywood) 2002, 227(2):133-140.
50. Gentile D.A., Doyle W.J., Zeevi A., et al. Cytokine gene polymorphisms moderate illness severity in infants with respiratory syncytial virus infection. Hum Immunol 2003, 64(3):338-344.
51. Gentile D.A., Doyle W.J., Zeevi A., et al. Cytokine gene polymorphisms moderate responses to respiratory syncytial virus in adults. Hum Immunol 2003, 64(1):93-98.
52. Genovese M., Van den Bosch F., Roberson S., et al. LY2439821, a humanized anti-IL-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis. Arthritis Rheum 2010, 62(4):929-939.
53. Faden H., Kaul T.N., Ogra P.L. Activation of oxidative and arachidonic acid metabolism in neutrophils by respiratory syncytial virus antibody complexes: possible role in disease. J Infect Dis 1983, 148(1):110-116.
54. Richardson J.Y., Ottolini M.G., Pletneva L., et al. Respiratory syncytial virus (RSV) infection induces cyclooxygenase 2: a potential target for RSV therapy. J Immunol 2005, 174(7):4356-4364.
55. Henderson W.R., Lewis D.B., Albert R.K., et al. The importance of leukotrienes in airway inflammation in a mouse model of asthma. J Exp Med 1996, 184(4):1483-1494.
56. Henderson W.R., Tang L.O., Chu S.J., et al. A role for cysteinyl leukotrienes in airway remodeling in a mouse asthma model. Am J Respir Crit Care Med 2002, 165(1):108-116.
57. Panuska J.R., Midulla F., Cirino N.M., et al. Virus-induced alterations in macrophage production of tumor necrosis factor and prostaglandin E2. Am J Physiol 1990, 259(6 Pt 1):L396-L402.
58. Hart C.M. Nitric oxide in adult lung disease. Chest 1999, 115(5):1407-1417.
59. Kao Y.J., Piedra P.A., Larsen G.L., et al. Induction and regulation of nitric oxide synthase in airway epithelial cells by respiratory syncytial virus. Am J Respir Crit Care Med 2001, 163(2):532-539.
60. Gentile D.A., Doyle W.J., Belenky S., et al. Nasal and oral nitric oxide levels during experimental respiratory syncytial virus infection of adults. Acta Otolaryngol 2002, 122(1):61-66.
61. Kaul P., Singh I., Turner R.B. Effect of nitric oxide on rhinovirus replication and virus-induced interleukin-8 elaboration. Am J Respir Crit Care Med 1999, 159(4 Pt 1):1193-1198.
62. Murphy A.W., Platts-Mills T.A., Lobo M., et al. Respiratory nitric oxide levels in experimental human influenza. Chest 1998, 114(2):452-456.
63. Patel J.A., Kunimoto M., Sim T.C., et al. Interleukin-1 alpha mediates the enhanced expression of intercellular adhesion molecule-1 in pulmonary epithelial cells infected with respiratory syncytial virus. Am J Respir Cell Mol Biol 1995, 13(5):602-609.
64. Becker S., Koren H.S., Henke D.C. Interleukin-8 expression in normal nasal epithelium and its modulation by infection with respiratory syncytial virus and cytokines tumor necrosis factor, interleukin-1, and interleukin-6. Am J Respir Cell Mol Biol 1993, 8(1):20-27.
65. Jamaluddin M., Garofalo R., Ogra P.L., et al. Inducible translational regulation of the NF-IL6 transcription factor by respiratory syncytial virus infection in pulmonary epithelial cells. J Virol 1996, 70(3):1554-1563.
66. Mastronarde J.G., He B., Monick M.M., et al. Induction of interleukin (IL)-8 gene expression by respiratory syncytial virus involves activation of nuclear factor (NF)-kappa B and NF-IL-6. J Infect Dis 1996, 174(2):262-267.
67. Mastronarde J.G., Monick M.M., Mukaida N., et al. Activator protein-1 is the preferred transcription factor for cooperative interaction with nuclear factor-kappaB in respiratory syncytial virus-induced interleukin-8 gene expression in airway epithelium. J Infect Dis 1998, 177(5):1275-1281.
68. Noah T.L., Becker S. Respiratory syncytial virus-induced cytokine production by a human bronchial epithelial cell line. Am J Physiol 1993, 265(5 Pt 1):L472-L478.
69. Mellow T.E., Murphy P.C., Carson J.L., et al. The effect of respiratory synctial virus on chemokine release by differentiated airway epithelium. Exp Lung Res 2004, 30(1):43-57.
70. Noah T.L., Wortman I.A., Becker S. The effect of fluticasone propionate on respiratory syncytial virus-induced chemokine release by a human bronchial epithelial cell line. Immunopharmacology 1998, 39(3):193-199.
71. Becker S., Reed W., Henderson F.W., et al. RSV infection of human airway epithelial cells causes production of the beta-chemokine RANTES. Am J Physiol 1997, 272(3 Pt 1):L512-L520.
72. Gehlhar K., Bilitewski C., Reinitz-Rademacher K., et al. Impaired virus-induced interferon-alpha2 release in adult asthmatic patients. Clin Exp Allergy 2006, 36(3):331-337.
73. Grissell T.V., Powell H., Shafren D.R., et al. Interleukin-10 gene expression in acute virus-induced asthma. Am J Respir Crit Care Med 2005, 172(4):433-439.
74. van Scott M.R., Justice J.P., Bradfield J.F., et al. IL-10 reduces Th2 cytokine production and eosinophilia but augments airway reactivity in allergic mice. Am J Physiol Lung Cell Mol Physiol 2000, 278(4):L667-L674.
75. Hancock G.E., Scheuer C.A., Sierzega R., et al. Adaptive immune responses of patients with asthma to the attachment (G) glycoprotein of respiratory synctial virus. J Infect Dis 2001, 184(12):1589-1593.
76. O'Sullivan S., Cormican L., Faul J.L., et al. Activated, cytotoxic CD8(+) T lymphocytes contribute to the pathology of asthma death. Am J Respir Crit Care Med 2001, 164(4):560-564.
77. Coyle A.J., Erard F., Bertrand C., et al. Virus-specific CD8+ cells can switch to interleukin 5 production and induce airway eosinophilia. J Exp Med 1995, 181(3):1229-1233.
78. Bjornsson E., Hjelm E., Janson C., et al. Serology of respiratory viruses in relation to asthma and bronchial hyperresponsiveness. Ups J Med Sci 1996, 101(2):159-168.
79. Wilkinson T.M., Donaldson G.C., Johnston S.L., et al. Respiratory syncytial virus, airway inflammation, and FEV1 decline in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006, 173(8):871-876.
80. Douville R.N., Bastien N., Li Y., et al. Adult asthmatics display exaggerated IFNgamma responses to human metapneumovirus and respiratory syncytial virus. Biochem Cell Biol 2007, 85(2):252-258.
81. Haynes L.M., Moore D.D., Kurt-Jones E.A., et al. Involvement of toll-like receptor 4 in innate immunity to respiratory syncytial virus. J Virol 2001, 75(22):10730-10737.
82. Skoner D.P., Gentile D.A., Angelini B., et al. Allergy skin test responses during experimental infection with respiratory syncytial virus. Ann Allergy Asthma Immunol 2006, 96(6):834-839.
83. Hirose H., Matsuse H., Tsuchida T., 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(2):149-155.
84. Pala P., Message S.D., Johnston S.L., et al. Increased aeroallergen-specific interleukin-4-producing T cells in asthmatic adults. Clin Exp Allergy 2002, 32(12):1739-1744.
85. Piippo-Savolainen E., Remes S., Korppi M. Does blood eosinophilia in wheezing infants predict later asthma? A prospective 18-20-year follow-up. Allergy Asthma Proc 2007, 28(2):163-169.
86. Piippo-Savolainen E., Korppi M., Korhonen K., et al. Adult asthma after non-respiratory syncytial virus bronchiolitis in infancy: subgroup analysis of the 20-year prospective follow-up study. Pediatr Int 2007, 49(2):190-195.
87. Korppi M., Piippo-Savolainen E., Korhonen K., et al. Respiratory morbidity 20 years after RSV infection in infancy. Pediatr Pulmonol 2004, 38(2):155-160.
88. Welliver R.C. Immunologic mechanisms of virus-induced wheezing and asthma [review]. J Pediatr 1999, 135(2 Pt 2):14-20.
89. Collins P.L., Crowe J.E. Respiratory syncytial virus and metapneumovirus. Fields virology 2007, 1602-1641. Lippincott Williams & Wilkins, Philadelphia. 5th edition. D.M. Knipe, P.M. Howley (Eds.).
90. Takeuchi O., Akira S. MDA5/RIG-I and virus recognition. Curr Opin Immunol 2008, 20(1):17-22.
91. Wilkins C., Gale M. Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 2010, 22(1):41-47.
92. Ling Z., Tran K.C., Teng M.N. Human respiratory syncytial virus nonstructural protein NS2 antagonizes the activation of beta interferon transcription by interacting with RIG-I. J Virol 2009, 83(8):3734-3742.
93. Swedan S., Musiyenko A., Barik S. Respiratory syncytial virus nonstructural proteins decrease levels of multiple members of the cellular interferon pathways. J Virol 2009, 83(19):9682-9693.
94. 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-kappaB, and proinflammatory cytokines. J Virol 2005, 79(9):5353-5362.
95. 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.
96. Lo M.S., Brazas R.M., Holtzman M.J. Respiratory syncytial virus nonstructural proteins NS1 and NS2 mediate inhibition of Stat2 expression and alpha/beta interferon responsiveness. J Virol 2005, 79(14):9315-9319.
97. Ramaswamy M., Shi L., Varga S.M., et al. Respiratory syncytial virus nonstructural protein 2 specifically inhibits type I interferon signal transduction. Virology 2006, 344(2):328-339.
98. Elliott J., Lynch O.T., Suessmuth Y., et al. Respiratory syncytial virus NS1 protein degrades STAT2 by using the Elongin-Cullin E3 ligase. J Virol 2007, 81(7):3428-3436.
99. Munir S., Le N.C., Luongo C., et al. Nonstructural proteins 1 and 2 of respiratory syncytial virus suppress maturation of human dendritic cells. J Virol 2008, 82(17):8780-8796.
100. Bitko V., Shulyayeva O., Mazumder B., et al. Nonstructural proteins of respiratory syncytial virus suppress premature apoptosis by an NF-kappaB-dependent, interferon-independent mechanism and facilitate virus growth. J Virol 2007, 81(4):1786-1795.
101. Kotelkin A., Belyakov I.M., Yang L., et al. The NS2 protein of human respiratory syncytial virus suppresses the cytotoxic T-cell response as a consequence of suppressing the type I interferon response. J Virol 2006, 80(12):5958-5967.