How rhinovirus infections cause exacerbations of asthma

Clinical and Experimental Allergy

Volumn 45, Issue 1, 2015, Pages 32-42

  Gern, J E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; HOST FACTOR; INTERFERON; VITAMIN D;

ASTHMA; DISEASE EXACERBATION; ENVIRONMENTAL FACTOR; EPITHELIUM CELL; HUMAN; LOWER RESPIRATORY TRACT INFECTION; NONHUMAN; POLLUTANT; PRIORITY JOURNAL; REVIEW; RHINOVIRUS; RHINOVIRUS INFECTION; STRESS; VIRUS VIRULENCE; ANIMAL; COMPLICATION; IMMUNOLOGY; PICORNAVIRUS INFECTION;

ANIMALS; ASTHMA; HUMANS; PICORNAVIRIDAE INFECTIONS; RHINOVIRUS;

EID: 84919772736     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12428     Document Type: Review

References (104)

1. McErlean P, Shackelton LA, Lambert SB, Nissen MD, Sloots TP, Mackay IM. Characterisation of a newly identified human rhinovirus, HRV-QPM, discovered in infants with bronchiolitis. J Clin Virol 2007; 39:67-75.
2. Arden KE, McErlean P, Nissen MD, Sloots TP, Mackay IM. Frequent detection of human rhinoviruses, paramyxoviruses, coronaviruses, and bocavirus during acute respiratory tract infections. J Med Virol 2006; 78:1232-40.
3. Lamson D, Renwick N, Kapoor V et al. MassTag polymerase-chain-reaction detection of respiratory pathogens, including a new rhinovirus genotype, that caused influenza-like illness in New York State during 2004-2005. J Infect Dis 2006; 194:1398-402.
4. Kistler A, Avila PC, Rouskin S et al. Pan-viral screening of respiratory tract infections in adults with and without asthma reveals unexpected human coronavirus and human rhinovirus diversity. J Infect Dis 2007; 196:817-25.
5. Lee WM, Kiesner C, Pappas T et al. A diverse group of previously unrecognized human rhinoviruses are common causes of respiratory illnesses in infants. PLoS ONE 2007; 2:e966.
6. Linder JE, Kraft DC, Mohamed Y et al. Human rhinovirus C: age, season, and lower respiratory illness over the past 3 decades. J Allergy Clin Immunol 2013; 131:69-77 e1-6.
7. Bochkov YA, Palmenberg AC, Lee WM et al. Molecular modeling, organ culture and reverse genetics for a newly identified human rhinovirus C. Nat Med 2011; 17:627-32.
8. Ashraf S, Brockman-Schneider R, Bochkov YA, Pasic TR, Gern JE. Biological characteristics and propagation of human rhinovirus-C in differentiated sinus epithelial cells. Virology 2013; 436:143-9.
9. Hao W, Bernard K, Patel N et al. Infection and propagation of human rhinovirus C in human airway epithelial cells. J Virol 2012; 86:13524-32.
10. Palmenberg AC, Spiro D, Kuzmickas R et al. Sequencing and analyses of all known human rhinovirus genomes reveals structure and evolution. Science 2009; 324:55-9.
11. Liggett SB, Bochkov YA, Pappas T et al. Genome sequences of rhinovirus a isolates from wisconsin pediatric respiratory studies. Genome Announc 2014; 2:pii:e00200-14.
12. Basta HA, Ashraf S, Sgro JY, Bochkov YA, Gern JE, Palmenberg AC. Modeling of the human rhinovirus C capsid suggests possible causes for antiviral drug resistance. Virology 2014; 448:82-90.
13. Basta HA, Sgro JY, Palmenberg AC. Modeling of the human rhinovirus C capsid suggests a novel topography with insights on receptor preference and immunogenicity. Virology 2014; 448:176-84.
14. Bizzintino J, Lee WM, Laing IA et al. Association between human rhinovirus C and severity of acute asthma in children. Eur Respir J 2011; 37:1037-42.
15. Cox DW, Bizzintino J, Ferrari G et al. Human rhinovirus species C infection in young children with acute wheeze is associated with increased acute respiratory hospital admissions. Am J Respir Crit Care Med 2013; 188:1358-64.
16. Iwane MK, Prill MM, Lu X et al. Human rhinovirus species associated with hospitalizations for acute respiratory illness in young US children. J Infect Dis 2011; 204:1702-10.
17. Mak RK, Tse LY, Lam WY, Wong GW, Chan PK, Leung TF. Clinical spectrum of human rhinovirus infections in hospitalized Hong Kong children. Pediatr Infect Dis J 2011; 30:749-53.
18. Drysdale SB, Alcazar M, Wilson T et al. Respiratory outcome of prematurely born infants following human rhinovirus A and C infections. Eur J Pediatr 2014; 173:913-9.
19. Khetsuriani N, Lu X, Teague WG, Kazerouni N, Anderson LJ, Erdman DD. Novel human rhinoviruses and exacerbation of asthma in children. Emerg Infect Dis 2008; 14:1793-6.
20. Arden KE, Chang AB, Lambert SB, Nissen MD, Sloots TP, Mackay IM. Newly identified respiratory viruses in children with asthma exacerbation not requiring admission to hospital. J Med Virol 2010; 82:1458-61.
21. Linsuwanon P, Payungporn S, Samransamruajkit R et al. High prevalence of human rhinovirus C infection in Thai children with acute lower respiratory tract disease. J Infect 2009; 59:115-21.
22. Lee WM, Lemanske RF Jr, Evans MD et al. Human rhinovirus species and season of infection determine illness severity. Am J Respir Crit Care Med 2012; 186:886-91.
23. Papadopoulos NG, Sanderson G, Hunter J, Johnston SL. Rhinoviruses replicate effectively at lower airway temperatures. J Med Virol 1999; 58:100-4.
24. Schroth MK, Grimm E, Frindt P et al. Rhinovirus replication causes RANTES production in primary bronchial epithelial cells. Am J Respir Cell Mol Biol 1999; 20:1220-8.
25. McFadden ER Jr, Pichurko BM, Bowman HF et al. Thermal mapping of the airways in humans. J Appl Physiol 1985; 58:564-70.
26. Nakagome K, Bochkov YA, Ashraf S et al. Effects of rhinovirus species on viral replication and cytokine production. J Allergy Clin Immunol 2014; 134:332-41.
27. Watters K, Palmenberg AC. Differential processing of nuclear pore complex proteins by rhinovirus 2A proteases from different species and serotypes. J Virol 2011; 85:10874-83.
28. Mosser AG, Brockman-Schneider RA, Amineva SP et al. Similar frequency of rhinovirus-infectable cells in upper and lower airway epithelium. J Infect Dis 2002; 185:734-43.
29. Mosser AG, Vrtis R, Burchell L et al. Quantitative and qualitative analysis of rhinovirus infection in bronchial tissues. Am J Respir Crit Care Med 2005; 171:645-51.
30. Sajjan U, Wang Q, Zhao Y, Gruenert DC, Hershenson MB. Rhinovirus disrupts the barrier function of polarized airway epithelial cells. Am J Respir Crit Care Med 2008; 178:1271-81.
31. Proud D, Turner RB, Winther B et al. Gene expression profiles during in vivo human rhinovirus infection: insights into the host response. Am J Respir Crit Care Med 2008; 178:962-8.
32. Lewis TC, Henderson TA, Carpenter AR et al. Nasal cytokine responses to natural colds in asthmatic children. Clin Exp Allergy 2012; 42:1734-44.
33. Konno S, Grindle KA, Lee WM et al. Interferon-g enhances rhinovirus-induced RANTES secretion in human airway epithelial cells. Am J Respir Cell Mol Biol 2002; 26:594-601.
34. Naclerio RM, Proud D, Lichtenstein LM et al. Kinins are generated during experimental rhinovirus colds. J Infect Dis 1988; 157:133-42.
35. Seymour ML, Gilby N, Bardin PG et al. Rhinovirus infection increases 5-lipoxygenase and cyclooxygenase-2 in bronchial biopsy specimens from nonatopic subjects. J Infect Dis 2002; 185:540-4.
36. Naclerio RM, Proud D, Kagey-Sobotka A, Lichtenstein LM, Hendley JO, Gwaltney JM Jr. Is histamine responsible for the symptoms of rhinovirus colds? A look at the inflammatory mediators following infection [published erratum appears in Pediatr Infect Dis J 1988 Oct; 7(10):682]. Pediatr Infect Dis J 1988; 7:218-22.
37. Yuta A, Doyle WJ, Gaumond E et al. Rhinovirus infection induces mucus hypersecretion. Am J Physiol 1998; 274:L1017-23.
38. Gern JE, Brockman-Schneider R, Bhattacharya S, Malter JS, Busse WW. Serum and low-density lipoprotein enhance IL-8 secretion by airway epithelial cells. Am J Respir Cell Mol Biol 2003; 29:483-9.
39. Miller EK, Lu X, Erdman DD et al. New vaccine surveillance N, rhinovirus-associated hospitalizations in young children. J Infect Dis 2007; 195:773-81.
40. DeMore JP, Weisshaar EH, Vrtis RF et al. Similar colds in subjects with allergic asthma and nonatopic subjects after inoculation with rhinovirus-16. J Allergy Clin Immunol 2009; 124:245-52.
41. Message SD, Laza-Stanca V, Mallia P et al. 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 USA 2008; 105:13562-7.
42. Simons E, Schroth MK, Gern JE. Analysis of tracheal secretions for rhinovirus during natural colds. Pediatr Allergy Immunol 2005; 16:276-8.
43. Holgate ST. Epithelium dysfunction in asthma. J Allergy Clin Immunol 2007; 120:1233-44.
44. Lopez-Souza N, Dolganov G, Dubin R et al. Resistance of differentiated human airway epithelium to infection by rhinovirus. Am J Physiol Lung Cell Mol Physiol 2004; 286:L373-81.
45. Jakiela B, Brockman-Schneider R, Amineva S, Lee WM, Gern JE. Basal cells of differentiated bronchial epithelium are more susceptible to rhinovirus infection. Am J Respir Cell Mol Biol 2008; 38:517-23.
46. Yoo JK, Kim TS, Hufford MM, Braciale TJ. Viral infection of the lung: host response and sequelae. J Allergy Clin Immunol 2013; 132:1263-76; quiz 77.
47. MacMicking JD. Interferon-inducible effector mechanisms in cell-autonomous immunity. Nat Rev Immunol 2012; 12:367-82.
48. Copenhaver CC, Gern JE, Li Z et al. Cytokine response patterns, exposure to viruses, and respiratory infections in the first year of life. Am J Respir Crit Care Med 2004; 170:175-80.
49. Gern JE, Brooks GD, Meyer P et al. Bidirectional interactions between viral respiratory illnesses and cytokine responses in the first year of life. J Allergy Clin Immunol 2006; 117:72-8.
50. Isaacs D, Clarke JR, Tyrrell DA, Webster AD, Valman HB. Deficient production of leucocyte interferon (interferon-alpha) in vitro and in vivo in children with recurrent respiratory tract infections. Lancet 1981; 2:950-2.
51. Upham JW, Zhang G, Rate A et al. Plasmacytoid dendritic cells during infancy are inversely associated with childhood respiratory tract infections and wheezing. J Allergy Clin Immunol 2009; 124:707-13 e2.
52. Parry DE, Busse WW, Sukow KA, Dick CR, Swenson C, Gern JE. Rhinovirus-induced PBMC responses and outcome of experimental infection in allergic subjects. J Allergy Clin Immunol 2000; 105:692-8.
53. Gern JE, Vrtis R, Grindle KA, Swenson C, Busse WW. Relationship of upper and lower airway cytokines to outcome of experimental rhinovirus infection. Am J Respir Crit Care Med 2000; 162:2226-31.
54. Papadopoulos NG, Stanciu LA, Papi A, Holgate ST, Johnston SL. Rhinovirus-induced alterations on peripheral blood mononuclear cell phenotype and costimulatory molecule expression in normal and atopic asthmatic subjects. Clin Exp Allergy 2002; 32:537-42.
55. Gehlhar K, Bilitewski C, Reinitz-Rademacher K, Rohde G, Bufe A. Impaired virus-induced interferon-alpha2 release in adult asthmatic patients. Clin Exp Allergy 2006; 36:331-7.
56. Gill MA, Bajwa G, George TA et al. Counterregulation between the FcepsilonRI pathway and antiviral responses in human plasmacytoid dendritic cells. J Immunol 2010; 184:5999-6006.
57. Wark PA, Johnston SL, Bucchieri F et al. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J Exp Med 2005; 201:937-47.
58. Contoli M, Message SD, Laza-Stanca V et al. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat Med 2006; 12:1023-6.
59. Lopez-Souza N, Favoreto S, Wong H et al. In vitro susceptibility to rhinovirus infection is greater for bronchial than for nasal airway epithelial cells in human subjects. J Allergy Clin Immunol 2009; 123:1384-90.
60. Bochkov YA, Hanson KM, Keles S, Brockman-Schneider RA, Jarjour NN, Gern JE. Rhinovirus-induced modulation of gene expression in bronchial epithelial cells from subjects with asthma. Mucosal Immunol 2010; 3:69-80.
61. Kennedy JL, Shaker M, McMeen V et al. Comparison of viral load in individuals with and without asthma during infections with rhinovirus. Am J Respir Crit Care Med 2014; 189:532-9.
62. Sykes A, Macintyre J, Edwards MR et al. Rhinovirus-induced interferon production is not deficient in well controlled asthma. Thorax 2014; 69:240-6.
63. Sykes A, Edwards MR, Macintyre J et al. Rhinovirus 16-induced IFN-alpha and IFN-beta are deficient in bronchoalveolar lavage cells in asthmatic patients. J Allergy Clin Immunol 2012; 129():1506-14 e6.
64. Gern JE. Interferon-lambda1 and viral wheeze in asthma: a Gothic duality? Am J Respir Crit Care Med 2012; 185:468-70.
65. Schwantes EA, Manthei DM, Denlinger LC et al. Interferon gene expression in sputum cells correlates with the asthma index score during virus-induced exacerbations. Clin Exp Allergy 2014; 44:813-21.
66. Miller EK, Hernandez JZ, Wimmenauer V et al. A mechanistic role for type III IFN-lambda1 in asthma exacerbations mediated by human rhinoviruses. Am J Respir Crit Care Med 2012; 185:508-16.
67. Mikus LD, Rosenthal LA, Sorkness RL, Lemanske RF Jr. Reduced interferon-gamma secretion by natural killer cells from rats susceptible to postviral chronic airway dysfunction. Am J Respir Cell Mol Biol 2001; 24:74-82.
68. Kumar A, Sorkness RL, Kaplan MR, Lemanske RF Jr. Chronic, episodic, reversible airway obstruction after viral bronchiolitis in rats. Am J Respir Crit Care Med 1997; 155:130-4.
69. Walter MJ, Morton JD, Kajiwara N, Agapov E, Holtzman MJ. Viral induction of a chronic asthma phenotype and genetic segregation from the acute response. J Clin Invest 2002; 110:165-75.
70. Sorkness RL, Castleman WL, Kumar A, Kaplan MR, Lemanske RF Jr. Prevention of chronic postbronchiolitis airway sequelae with IFN-g treatment in rats. Am J Respir Crit Care Med 1999; 160:705-10.
71. Bartlett NW, Slater L, Glanville N et al. Defining critical roles for NF-kappaB p65 and type I interferon in innate immunity to rhinovirus. EMBO Mol Med 2012; 4:1244-60.
72. Jayaraman A, Jackson DJ, Message SD et al. IL-15 complexes induce NK- and T-cell responses independent of type I IFN signaling during rhinovirus infection. Mucosal Immunol 2014; 7:1151-64.
73. Hong JY, Bentley JK, Chung Y et al. Neonatal rhinovirus induces mucous metaplasia and airways hyperresponsiveness through IL-25 and type 2 innate lymphoid cells. J Allergy Clin Immunol 2014; 134:429-39.
74. Zhu J, Message SD, Qiu Y et al. Airway inflammation and illness severity in response to experimental rhinovirus infection in asthma. Chest 2014; 145:1219-29.
75. Denlinger LC, Sorkness RL, Lee WM et al. Lower airway rhinovirus burden and the seasonal risk of asthma exacerbation. Am J Respir Crit Care Med 2011; 184:1007-14.
76. Rakes GP, Arruda E, Ingram JM et al. Rhinovirus and respiratory syncytial virus in wheezing children requiring emergency care. IgE and eosinophil analyses. Am J Respir Crit Care Med 1999; 159:785-90.
77. Tversky JR, Le TV, Bieneman AP, Chichester KL, Hamilton RG, Schroeder JT. Human blood dendritic cells from allergic subjects have impaired capacity to produce interferon-alpha via Toll-like receptor 9. Clin Exp Allergy 2008; 38:781-8.
78. Durrani SR, Montville DJ, Pratt AS et al. Innate immune responses to rhinovirus are reduced by the high-affinity IgE receptor in allergic asthmatic children. J Allergy Clin Immunol 2012; 130:489-95.
79. Subrata LS, Bizzintino J, Mamessier E et al. Interactions between innate antiviral and atopic immunoinflammatory pathways precipitate and sustain asthma exacerbations in children. J Immunol 2009; 183:2793-800.
80. Corne JM, Marshall C, Smith S et al. Frequency, severity, and duration of rhinovirus infections in asthmatic and non-asthmatic individuals: a longitudinal cohort study. Lancet 2002; 359:831-4.
81. Meyer N, Akdis CA. Vascular endothelial growth factor as a key inducer of angiogenesis in the asthmatic airways. Curr Allergy Asthma Rep 2013; 13:1-9.
82. Tarlo SM, Broder I, Corey P et al. The role of symptomatic colds in asthma exacerbations: influence of outdoor allergens and air pollutants. J Allergy Clin Immunol 2001; 108:52-8.
83. Chauhan AJ, Inskip HM, Linaker CH et al. Personal exposure to nitrogen dioxide (NO2) and the severity of virus-induced asthma in children. Lancet 2003; 361:1939-44.
84. Venarske DL, Busse WW, Griffin MR et al. The relationship of rhinovirus-associated asthma hospitalizations with inhaled corticosteroids and smoking. J Infect Dis 2006; 193:1536-43.
85. Duff AL, Pomeranz ES, Gelber LE et al. Risk factors for acute wheezing in infants in infants and children: viruses, passive smoke, and IgE antibodies to inhalant allergens. Pediatrics 1993; 92:535-40.
86. Murray CS, Poletti G, Kebadze T et al. Study of modifiable risk factors for asthma exacerbations: virus infection and allergen exposure increase the risk of asthma hospital admissions in children. Thorax 2006; 61:376-82.
87. Green RM, Cusotvic A, Sanderson G, Hunter J, Johnston SL, Woodcock A. Synergism between allergens and viruses and risk of hospital admission with asthma: case-control study. Br Med J 2002; 324:763-66A.
88. Hilty M, Burke C, Pedro H et al. Disordered microbial communities in asthmatic airways. PLoS ONE 2010; 5:e8578.
89. Huang YJ, Nelson CE, Brodie EL et al. Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. J Allergy Clin Immunol 2011; 127:372-81.
90. Bisgaard H, Hermansen MN, Buchvald F et al. Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med 2007; 357:1487-95.
91. Bisgaard H, Hermansen MN, Bonnelykke K et al. Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study. BMJ 2010; 341:c4978.
92. Kloepfer KM, Lee WM, Pappas TE et al. Detection of pathogenic bacteria during rhinovirus infection is associated with increased respiratory symptoms and asthma exacerbations. J Allergy Clin Immunol 2014; 133:1301-07 e3.
93. Camargo CA Jr, Rifas-Shiman SL, Litonjua AA et al. Maternal intake of vitamin D during pregnancy and risk of recurrent wheeze in children at 3 y of age. Am J Clin Nutr 2007; 85:788-95.
94. Ginde AA, Mansbach JM, Camargo CA Jr. Association between serum 25-hydroxyvitamin D level and upper respiratory tract infection in the Third National Health and Nutrition Examination Survey. Arch Intern Med 2009; 169:384-90.
95. Brockman-Schneider RA, Pickles RJ, Gern JE. Effects of vitamin D on airway epithelial cell morphology and rhinovirus replication. PLoS ONE 2014; 9:e86755.
96. Hansdottir S, Monick MM. Vitamin D effects on lung immunity and respiratory diseases. Vitam Horm 2011; 86:217-37.
97. Stone AA, Bovbjerg DH, Neale JM et al. Development of common cold symptoms following experimental rhinovirus infection is related to prior stressful life events. Behav Med 1992; 18:115-20.
98. Cohen S. Psychological stress and susceptibility to upper respiratory infections. Am J Respir Crit Care Med 1995; 152:S53-8.
99. Busse WW, Morgan WJ, Gergen PJ et al. Randomized trial of omalizumab (anti-IgE) for asthma in inner-city children. N Engl J Med 2011; 364:1005-15.
100. Haldar P, Brightling CE, Hargadon B et al. Mepolizumab and exacerbations of refractory eosinophilic asthma. N Engl J Med 2009; 360:973-84.
101. Djukanovic R, Harrison T, Johnston SL et al. The Effect of Inhaled IFN-beta on Worsening of Asthma Symptoms Caused by Viral Infections. A Randomized Trial. Am J Respir Crit Care Med 2014; 190:145-54.
102. Papadopoulos NG, Borres M, Gern J, Nieto A. New visions in respiratory allergy (asthma and allergic rhinitis): an iPAC summary and future trends. Pediatr Allergy Immunol 2008; 19(Suppl. 19):51-9.
103. McIntyre CL, Knowles NJ, Simmonds P. Proposals for the classification of human rhinovirus species A, B and C into genotypically assigned types. J Gen Virol 2013; 94:1791-1806.
104. Palmenberg AC, Gern JE. Classification and Evoluaiton in Human Rhinoviruses. In: Ghildyal R ed. Methods in Molecular Virology 2015; 1221:1-10.