About this Journal Submit a Manuscript Table of Contents
Scientifica
Volume 2013 (2013), Article ID 405876, 12 pages
http://dx.doi.org/10.1155/2013/405876
Review Article

Rhinovirus-Induced Exacerbations of Asthma and COPD

Departments of Pediatrics and Communicable Diseases and Molecular and Integrative Physiology, University of Michigan Medical School, 1150 W. Medical Center Drive, Room 3570B, Medical Science Research Building 2, Ann Arbor, MI 48109-5688, USA

Received 11 December 2012; Accepted 16 January 2013

Academic Editors: P. Borger and R. Teasdale

Copyright © 2013 Marc B. Hershenson. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. A. Halperin, P. A. Eggleston, J. O. Hendley, et al., “Pathogenesis of lower respiratory tract symptoms in experimental rhinovirus infection,” American Review of Respiratory Disease, vol. 128, no. 5, pp. 806–810, 1983. View at Scopus
  2. D. A. J. Tyrrell and R. Parsons, “Some virus isolations from common colds. III. Cytopathic effects in tissue cultures,” The Lancet, vol. 1, no. 7118, pp. 239–242, 1960. View at Scopus
  3. E. J. Stott and G. F. Heath, “Factors affecting the growth of rhinovirus 2 in suspension cultures of L132 cells,” Journal of General Virology, vol. 6, no. 1, pp. 15–24, 1970. View at Scopus
  4. N. Papadopoulos, G. Sanderson, J. Hunter, and S. Johnston, “Rhinoviruses replicate effectively at lower airway temperatures,” Journal of Medical Virology, vol. 58, pp. 100–104, 1999.
  5. G. Sluder, “Asthma as a nasal reflex,” The Journal of the American Medical Association, vol. 73, pp. 589–591, 1919. View at Publisher · View at Google Scholar
  6. P. Small and N. Bisken, “The effects of allergen-induced nasal provocation on pulmonary function in patients with perennial allergic rhinitis,” American Journal of Rhinology, vol. 3, no. 1, pp. 17–20, 1989. View at Publisher · View at Google Scholar
  7. N. T. Littell, C. C. Carlisle, R. P. Millman, and S. S. Braman, “Changes in airway resistance following nasal provocation,” American Review of Respiratory Disease, vol. 141, no. 3, pp. 580–583, 1990. View at Scopus
  8. J. Corren, A. D. Adinoff, and C. G. Irvin, “Changes in bronchial responsiveness following nasal provocation with allergen,” The Journal of Allergy and Clinical Immunology, vol. 89, no. 2, pp. 611–618, 1992. View at Scopus
  9. J. A. Denburg, “The nose, the lung and the bone marrow in allergic inflammation,” Allergy, vol. 54, no. 57, pp. 73–80, 1999. View at Scopus
  10. M. K. Schroth, E. Grimm, P. Frindt et al., “Rhinovirus replication causes RANTES production in primary bronchial epithelial cells,” American Journal of Respiratory Cell and Molecular Biology, vol. 20, no. 6, pp. 1220–1228, 1999. View at Scopus
  11. E. R. McFadden, B. M. Pichurko, H. F. Bowman, et al., “Thermal mapping of the airways in humans,” Journal of Applied Physiology, vol. 58, no. 2, pp. 564–570, 1985. View at Scopus
  12. S. L. Johnston, P. K. Pattemore, G. Sanderson et al., “Community study of role of viral infections in exacerbations of asthma in 9–11 year old children,” British Medical Journal, vol. 310, no. 6989, pp. 1225–1229, 1995. View at Scopus
  13. N. W. Johnston, S. L. Johnston, J. M. Duncan et al., “The September epidemic of asthma exacerbations in children: a search for etiology,” The Journal of Allergy and Clinical Immunology, vol. 115, no. 1, pp. 132–138, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. K. G. Nicholson, J. Kent, and D. C. Ireland, “Respiratory viruses and exacerbations of asthma in adults,” British Medical Journal, vol. 307, no. 6910, pp. 982–986, 1993. View at Scopus
  15. W. C. Tan, X. Xiang, D. Qiu, T. P. Ng, S. F. Lam, and R. G. Hegele, “Epidemiology of respiratory viruses in patients hospitalized with near-fatal asthma, acute exacerbations of asthma, or chronic obstructive pulmonary disease,” American Journal of Medicine, vol. 115, no. 4, pp. 272–277, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. R. M. Green, A. Custovic, G. Sanderson, J. Hunter, S. L. Johnston, and A. Woodcock, “Synergism between allergens and viruses and risk of hospital admission with asthma: case-control study,” British Medical Journal, vol. 324, no. 7340, pp. 763–766, 2002. View at Scopus
  17. A. Kistler, P. C. Avila, S. Rouskin et al., “Pan-viral screening of respiratory tract infections in adults with and without asthma reveals unexpected human coronavirus and human rhinovirus diversity,” Journal of Infectious Diseases, vol. 196, no. 6, pp. 817–825, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. T. H. Harju, M. Leinonen, J. Nokso-Koivisto et al., “Pathogenic bacteria and viruses in induced sputum or pharyngeal secretions of adults with stable asthma,” Thorax, vol. 61, no. 7, pp. 579–584, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. R. L. Atmar, E. Guy, K. K. Guntupalli et al., “Respiratory tract viral infections in inner-city asthmatic adults,” Archives of Internal Medicine, vol. 158, no. 22, pp. 2453–2459, 1998. View at Scopus
  20. N. Khetsuriani, N. N. Kazerouni, D. D. Erdman et al., “Prevalence of viral respiratory tract infections in children with asthma,” The Journal of Allergy and Clinical Immunology, vol. 119, no. 2, pp. 314–321, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. P. W. Heymann, H. T. Carper, D. D. Murphy et al., “Viral infections in relation to age, atopy, and season of admission among children hospitalized for wheezing,” The Journal of Allergy and Clinical Immunology, vol. 114, no. 2, pp. 239–247, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. S. B. Greenberg, M. Allen, J. Wilson, and R. L. Atmar, “Respiratory viral infections in adults with and without chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 162, no. 1, pp. 167–173, 2000. View at Scopus
  23. T. Seemungal, R. Harper-Owen, A. Bhowmik et al., “Respiratory viruses, symptoms, and inflammatory markers in acute exacerbations and stable chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 164, no. 9, pp. 1618–1623, 2001. View at Scopus
  24. G. Rohde, A. Wiethege, I. Borg et al., “Respiratory viruses in exacerbations of chronic obstructive pulmonary disease requiring hospitalisation: a case-control study,” Thorax, vol. 58, no. 1, pp. 37–42, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. F. W. S. Ko, M. Ip, P. K. S. Chan et al., “A 1-year prospective study of the infectious etiology in patients hospitalized with acute exacerbations of COPD,” Chest, vol. 131, no. 1, pp. 44–52, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. T. E. McManus, A.-M. Marley, N. Baxter et al., “Respiratory viral infection in exacerbations of COPD,” Respiratory Medicine, vol. 102, no. 11, pp. 1575–1580, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Kling, H. Donninger, Z. Williams et al., “Persistence of rhinovirus RNA after asthma exacerbation in children,” Clinical and Experimental Allergy, vol. 35, no. 5, pp. 672–678, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. N. W. Johnston, S. L. Johnston, J. M. Duncan et al., “The September epidemic of asthma exacerbations in children: a search for etiology,” The Journal of Allergy and Clinical Immunology, vol. 115, no. 1, pp. 132–138, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. J. E. Gern, D. M. Galagan, N. N. Jarjour, E. C. Dick, and W. W. Busse, “Detection of rhinovirus RNA in lower airway cells during experimentally induced infection,” American Journal of Respiratory and Critical Care Medicine, vol. 155, no. 3, pp. 1159–1161, 1997. View at Scopus
  30. A. G. Mosser, R. Vrtis, L. Burchell et al., “Quantitative and qualitative analysis of rhinovirus infection in bronchial tissues,” American Journal of Respiratory and Critical Care Medicine, vol. 171, no. 6, pp. 645–651, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. N. G. Papadopoulos, P. J. Bates, P. G. Bardin et al., “Rhinoviruses infect the lower airways,” Journal of Infectious Diseases, vol. 181, no. 6, pp. 1875–1884, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Woś, M. Sanak, J. Soja, H. Olechnowicz, W. W. Busse, and A. Szczeklik, “The presence of rhinovirus in lower airways of patients with bronchial asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 177, no. 10, pp. 1082–1089, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. E. Arruda, T. R. Boyle, B. Winther, D. C. Pevear, J. M. Gwaltney, and F. G. Hayden, “Localization of human rhinovirus replication in the upper respiratory tract by in situ hybridization,” Journal of Infectious Diseases, vol. 171, no. 5, pp. 1329–1333, 1995. View at Scopus
  34. A. G. Mosser, R. Brockman-Schneider, S. Amineva et al., “Similar frequency of rhinovirus-infectible cells in upper and lower airway epithelium,” Journal of Infectious Diseases, vol. 185, no. 6, pp. 734–743, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. J. P. DeMore, E. H. Weisshaar, R. F. Vrtis et al., “Similar colds in subjects with allergic asthma and nonatopic subjects after inoculation with rhinovirus-16,” The Journal of Allergy and Clinical Immunology, vol. 124, no. 2, pp. 245.e3–252.e3, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Winther, B. Farr, R. B. Turner, et al., “Histopathologic examination and enumeration of polymorphonuclear leukocytes in the nasal mucosa during experimental rhinovirus colds,” Acta Oto-Laryngologica, vol. 413, pp. 19–24, 1984. View at Scopus
  37. D. J. Fraenkel, P. G. Bardin, G. Sanderson, F. Lampe, S. L. Johnston, and S. T. Holgate, “Lower airways inflammation during rhinovirus colds in normal and in asthmatic subjects,” American Journal of Respiratory and Critical Care Medicine, vol. 151, no. 3, pp. 879–886, 1995. View at Scopus
  38. A. Bossios, S. Psarras, D. Gourgiotis et al., “Rhinovirus infection induces cytotoxicity and delays wound healing in bronchial epithelial cells,” Respiratory Research, vol. 6, article 114, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. M. C. Subauste, D. B. Jacoby, S. M. Richards, and D. Proud, “Infection of a human respiratory epithelial cell line with rhinovirus. Induction of cytokine release and modulation of susceptibility to infection by cytokine exposure,” The Journal of Clinical Investigation, vol. 96, no. 1, pp. 549–557, 1995. View at Scopus
  40. Z. Zhu, W. Tang, J. M. Gwaltney, Y. Wu, and J. A. Elias, “Rhinovirus stimulation of interleukin-8 in vivo and in vitro: role of NF-κB,” American Journal of Physiology, vol. 273, no. 4, pp. L814–L824, 1997. View at Scopus
  41. M. Yamaya, K. Sekizawa, T. Suzuki et al., “Infection of human respiratory submucosal glands with rhinovirus: effects on cytokine and ICAM-1 production,” American Journal of Physiology, vol. 277, no. 2, pp. L362–L371, 1999. View at Scopus
  42. N. G. Papadopoulos, A. Papi, J. Meyer et al., “Rhinovirus infection up-regulates eotaxin and eotaxin-2 expression in bronchial epithelial cells,” Clinical and Experimental Allergy, vol. 31, no. 7, pp. 1060–1066, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. S. D. Griego, C. B. Weston, J. L. Adams, R. Tal-Singer, and S. B. Dillon, “Role of p38 mitogen-activated protein kinase in rhinovirus-induced cytokine production by bronchial epithelial cells,” Journal of Immunology, vol. 165, no. 9, pp. 5211–5220, 2000. View at Scopus
  44. H. Donninger, R. Glashoff, H. M. Haitchi et al., “Rhinovirus induction of the CXC chemokine epithelial-neutrophil activating peptide-78 in bronchial epithelium,” Journal of Infectious Diseases, vol. 187, no. 11, pp. 1809–1817, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. J. C. L. Spurrell, S. Wiehler, R. S. Zaheer, S. P. Sanders, and D. Proud, “Human airway epithelial cells produce IP-10 (CXCL10) in vitro and in vivo upon rhinovirus infection,” American Journal of Physiology, vol. 289, no. 1, pp. L85–L95, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. T. V. Grissell, H. Powell, D. R. Shafren et al., “Interleukin-10 gene expression in acute virus-induced asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 172, no. 4, pp. 433–439, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. J. E. Gern, D. A. French, K. A. Grindle, R. A. Brockman-Schneider, S.-I. Konno, and W. W. Busse, “Double-stranded RNA induces the synthesis of specific chemokines by bronchial epithelial cells,” American Journal of Respiratory Cell and Molecular Biology, vol. 28, no. 6, pp. 731–737, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. D. Proud, R. B. Turner, B. Winther et al., “Gene expression profiles during in vivo human rhinovirus infection insights into the host response,” American Journal of Respiratory and Critical Care Medicine, vol. 178, no. 9, pp. 962–968, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Z. Norzila, K. Fakes, R. L. Henry, J. Simpson, and P. G. Gibson, “Interleukin-8 secretion and neutrophil recruitment accompanies induced sputum eosinophil activation in children with acute asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 161, no. 3 I, pp. 769–774, 2000. View at Scopus
  50. C. L. Ordoñez, T. E. Shaughnessy, M. A. Matthay, and J. V. Fahy, “Increased neutrophil numbers and IL-8 levels in airway secretions in acute severe asthma. Clinical and biologic significance,” American Journal of Respiratory and Critical Care Medicine, vol. 161, no. 4, pp. 1185–1190, 2000. View at Scopus
  51. K. Grünberg, R. F. Sharon, J. K. Sont et al., “Rhinovirus-induced airway inflammation in asthma. Effect of treatment with inhaled corticosteroids before and during experimental infection,” American Journal of Respiratory and Critical Care Medicine, vol. 164, no. 10, pp. 1816–1822, 2001. View at Scopus
  52. R. F. Lemanske, E. C. Dick, C. A. Swenson, R. F. Vrtis, and W. W. Busse, “Rhinovirus upper respiratory infection increases airway hyperreactivity and late asthmatic reactions,” The Journal of Clinical Investigation, vol. 83, no. 1, pp. 1–10, 1989. View at Scopus
  53. W. J. Calhoun, E. C. Dick, L. B. Schwartz, and W. W. Busse, “A common cold virus, rhinovirus 16, potentiates airway inflammation after segmental antigen bronchoprovocation in allergic subjects,” The Journal of Clinical Investigation, vol. 94, no. 6, pp. 2200–2208, 1994. View at Scopus
  54. J. E. Gern, W. Calhoun, C. Swenson, G. Shen, and W. W. Busse, “Rhinovirus infection preferentially increases lower airway responsiveness in allergic subjects,” American Journal of Respiratory and Critical Care Medicine, vol. 155, no. 6, pp. 1872–1876, 1997. View at Scopus
  55. J. de Kluijver, K. Grünberg, D. Pons et al., “Interleukin-1β and interleukin-1ra levels in nasal lavages during experimental rhinovirus infection in asthmatic and non-asthmatic subjects,” Clinical and Experimental Allergy, vol. 33, no. 10, pp. 1415–1418, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. P. K. Jeffery, A. J. Wardlaw, F. C. Nelson, J. V. Collins, and A. B. Kay, “Bronchial biopsies in asthma: an ultrastructural, quantitative study and correlation with hyperreactivity,” American Review of Respiratory Disease, vol. 140, no. 6, pp. 1745–1753, 1989. View at Scopus
  57. A. Barbato, G. Turato, S. Baraldo et al., “Epithelial damage and angiogenesis in the airways of children with asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 174, no. 9, pp. 975–981, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. B. Jakiela, R. Brockman-Schneider, S. Amineva, W.-M. Lee, and J. E. Gern, “Basal cells of differentiated bronchial epithelium are more susceptible to rhinovirus infection,” American Journal of Respiratory Cell and Molecular Biology, vol. 38, no. 5, pp. 517–523, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. M. E. Lachowicz-Scroggins, H. A. Boushey, W. E. Finkbeiner, and J. H. Widdicombe, “Interleukin-13-induced mucous metaplasia increases susceptibility of human airway epithelium to rhinovirus infection,” American Journal of Respiratory Cell and Molecular Biology, vol. 43, no. 6, pp. 652–661, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. J. J. O'Shea, A. Ma, and P. Lipsky, “Cytokines and autoimmunity,” Nature Reviews Immunology, vol. 2, no. 1, pp. 37–45, 2002. View at Scopus
  61. D. E. Parry, W. W. Busse, K. A. Sukow, C. R. Dick, C. Swenson, and J. E. Gern, “Rhinovirus-induced PBMC responses and outcome of experimental infection in allergic subjects,” The Journal of Allergy and Clinical Immunology, vol. 105, no. 4, pp. 692–698, 2000. View at Scopus
  62. J. E. Gern, R. Vrtis, K. A. Grindle, C. Swenson, and W. W. Busse, “Relationship of upper and lower airway cytokines to outcome experimental rhinovirus infection,” American Journal of Respiratory and Critical Care Medicine, vol. 162, no. 6, pp. 2226–2231, 2000. View at Scopus
  63. S. D. Message, V. Laza-Stanca, P. Mallia et al., “Rhinovirus-induced lower respiratory illness is increased in asthma and related to virus load and Th1/2 cytokine and IL-10 production,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 36, pp. 13562–13567, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. P. A. B. Wark, S. L. Johnston, F. Bucchieri et al., “Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus,” Journal of Experimental Medicine, vol. 201, no. 6, pp. 937–947, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Contoli, S. D. Message, V. Laza-Stanca et al., “Role of deficient type III interferon-λ production in asthma exacerbations,” Nature Medicine, vol. 12, no. 9, pp. 1023–1026, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. N. Lopez-Souza, S. Favoreto, H. Wong et al., “In vitro susceptibility to rhinovirus infection is greater for bronchial than for nasal airway epithelial cells in human subjects,” The Journal of Allergy and Clinical Immunology, vol. 123, no. 6, pp. 1384.e2–1390.e2, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. Y. A. Bochkov, K. M. Hanson, S. Keles, R. A. Brockman-Schneider, N. N. Jarjour, and J. E. Gern, “Rhinovirus-induced modulation of gene expression in bronchial epithelial cells from subjects with asthma,” Mucosal Immunology, vol. 3, no. 1, pp. 69–80, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. D. C. Newcomb, U. S. Sajjan, D. R. Nagarkar et al., “Human rhinovirus 1B exposure induces phosphatidylinositol 3-kinase-dependent airway inflammation in mice,” American Journal of Respiratory and Critical Care Medicine, vol. 177, no. 10, pp. 1111–1121, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. U. Sajjan, Q. Wang, Y. Zhao, D. C. Gruenert, and M. B. Hershenson, “Rhinovirus disrupts the barrier function of polarized airway epithelial cells,” American Journal of Respiratory and Critical Care Medicine, vol. 178, no. 12, pp. 1271–1281, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. D. R. Nagarkar, Q. Wang, J. Shim et al., “CXCR2 is required for neutrophilic airway inflammation and hyperresponsiveness in a mouse model of human rhinovirus infection,” Journal of Immunology, vol. 183, no. 10, pp. 6698–6707, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. U. Sajjan, S. Ganesan, A. T. Comstock et al., “Elastase- and LPS-exposed mice display altered responses to rhinovirus infection,” American Journal of Physiology, vol. 297, no. 5, pp. L931–L944, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. D. R. Nagarkar, E. R. Bowman, D. Schneider et al., “Rhinovirus infection of allergen-sensitized and -challenged mice induces eotaxin release from functionally polarized macrophages,” Journal of Immunology, vol. 185, no. 4, pp. 2525–2535, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. Q. Wang, D. R. Nagarkar, E. R. Bowman et al., “Role of double-stranded RNA pattern recognition receptors in rhinovirus-induced airway epithelial cell responses,” Journal of Immunology, vol. 183, no. 11, pp. 6989–6997, 2009. View at Scopus
  74. J. M. Greve, G. Davis, A. M. Meyer et al., “The major human rhinovirus receptor is ICAM-1,” Cell, vol. 56, no. 5, pp. 839–847, 1989. View at Scopus
  75. F. Hofer, M. Gruenberger, H. Kowalski et al., “Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 5, pp. 1839–1842, 1994. View at Scopus
  76. B. L. Unger, A. N. Faris, S. Ganesan, A. T. Comstock, M. B. Hershenson, and U. S. Sajjan, “Rhinovirus attenuates non-typeable Hemophilus influenzae-stimulated IL-8 responses via TLR2-dependent degradation of IRAK-1,” PLOS Pathogens, vol. 8, no. 10, Article ID e1002969, 2012.
  77. K. Andries, B. Dewindt, J. Snoeks et al., “Two groups of rhinoviruses revealed by a panel of antiviral compounds present sequence divergence and differential pathogenicity,” Journal of Virology, vol. 64, no. 3, pp. 1117–1123, 1990. View at Scopus
  78. S. K. P. Lau, C. C. Y. Yip, H.-W. Tsoi et al., “Clinical features and complete genome characterization of a distinct human rhinovirus (HRV) genetic cluster, probably representing a previously undetected HRV species, HRV-C, associated with acute respiratory illness in children,” Journal of Clinical Microbiology, vol. 45, no. 11, pp. 3655–3664, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. S. R. Dominguez, T. Briese, G. Palacios et al., “Multiplex MassTag-PCR for respiratory pathogens in pediatric nasopharyngeal washes negative by conventional diagnostic testing shows a high prevalence of viruses belonging to a newly recognized rhinovirus clade,” Journal of Clinical Virology, vol. 43, no. 2, pp. 219–222, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. P. McErlean, L. A. Shackelton, E. Andrews et al., “Distinguishing molecular features and clinical characteristics of a putative new rhinovirus species, Human rhinovirus C (HRV C),” PLoS ONE, vol. 3, no. 4, Article ID e1847, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. A. C. Palmenberg, D. Spiro, R. Kuzmickas et al., “Sequencing and analyses of all known human rhinovirus genomes reveal structure and evolution,” Science, vol. 324, no. 5923, pp. 55–59, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. H. P. Grunert, K. U. Wolf, K. D. Langner, D. Sawitzky, K. O. Habermehl, and H. Zeichhardt, “Internalization of human rhinovirus 14 into HeLa and ICAM-1-transfected BHK cells,” Medical Microbiology and Immunology, vol. 186, no. 1, pp. 1–9, 1997. View at Publisher · View at Google Scholar · View at Scopus
  83. L. DeTulleo and T. Kirchhausen, “The clathrin endocytic pathway in viral infection,” The EMBO Journal, vol. 17, no. 16, pp. 4585–4593, 1998. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Huber, M. Brabec, N. Bayer, D. Blaas, and R. Fuchs, “Elevated endosomal pH in HeLa cells overexpressing mutant dynamin can affect infection by pH-sensitive viruses,” Traffic, vol. 2, no. 10, pp. 727–736, 2001. View at Publisher · View at Google Scholar · View at Scopus
  85. L. Snyers, H. Zwickl, and D. Blaas, “Human rhinovirus type 2 is internalized by clathrin-mediated endocytosis,” Journal of Virology, vol. 77, no. 9, pp. 5360–5369, 2003. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Yoneyama, M. Kikuchi, T. Natsukawa et al., “The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses,” Nature Immunology, vol. 5, no. 7, pp. 730–737, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Andrejeva, K. S. Childs, D. F. Young et al., “The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, MDA-5, and inhibit its activation of the IFN-β promoter,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 49, pp. 17264–17269, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. T. J. Tuthill, N. G. Papadopoulos, P. Jourdan et al., “Mouse respiratory epithelial cells support efficient replication of human rhinovirus,” Journal of General Virology, vol. 84, no. 10, pp. 2829–2836, 2003. View at Publisher · View at Google Scholar · View at Scopus
  89. Q. Wang, D. J. Miller, E. R. Bowman et al., “MDA5 and TLR3 initiate pro-inflammatory signaling pathways leading to rhinovirus-induced airways inflammation and hyperresponsiveness,” PLoS Pathogens, vol. 7, no. 5, Article ID e1002070, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. N. W. Bartlett, R. P. Walton, M. R. Edwards et al., “Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation,” Nature Medicine, vol. 14, no. 2, pp. 199–204, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. T. Suzuki, M. Yamaya, K. Sekizawa et al., “Bafilomycin A1 inhibits rhinovirus infection in human airway epithelium: effects on endosome and ICAM-1,” American Journal of Physiology, vol. 280, no. 6, pp. L1115–L1127, 2001. View at Scopus
  92. D. C. Newcomb, U. Sajjan, S. Nanua et al., “Phosphatidylinositol 3-kinase is required for rhinovirus-induced airway epithelial cell interleukin-8 expression,” The Journal of Biological Chemistry, vol. 280, no. 44, pp. 36952–36961, 2005. View at Publisher · View at Google Scholar · View at Scopus
  93. J. E. Gern, E. C. Dick, W. M. Lee et al., “Rhinovirus enters but does not replicate inside monocytes and airway macrophages,” Journal of Immunology, vol. 156, no. 2, pp. 621–627, 1996. View at Scopus
  94. V. Laza-Stanca, L. A. Stanciu, S. D. Message, M. R. Edwards, J. E. Gern, and S. L. Johnston, “Rhinovirus replication in human macrophages induces NF-κB-dependent tumor necrosis factor alpha production,” Journal of Virology, vol. 80, no. 16, pp. 8248–8258, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. D. J. Hall, M. E. Bates, L. Guar, M. Cronan, N. Korpi, and P. J. Bertics, “The role of p38 MAPK in rhinovirus-induced monocyte chemoattractant protein-1 production by monocytic-lineage cells,” Journal of Immunology, vol. 174, no. 12, pp. 8056–8063, 2005. View at Scopus
  96. N. L. Korpi-Steiner, M. E. Bates, W.-M. Lee, D. J. Hall, and P. J. Bertics, “Human rhinovirus induces robust IP-10 release by monocytic cells, which is independent of viral replication but linked to type I interferon receptor ligation and STAT1 activation,” Journal of Leukocyte Biology, vol. 80, no. 6, pp. 1364–1374, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. S. L. Johnston, A. Papi, M. M. Monick, and G. W. Hunninghake, “Rhinoviruses induce interleukin-8 mRNA and protein production in human monocytes,” Journal of Infectious Diseases, vol. 175, no. 2, pp. 323–329, 1997. View at Scopus
  98. M. R. Khaitov, V. Laza-Stanca, M. R. Edwards et al., “Respiratory virus induction of alpha-, beta- and lambda-interferons in bronchial epithelial cells and peripheral blood mononuclear cells,” Allergy, vol. 64, no. 3, pp. 375–386, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. F. O. Martinez, L. Helming, and S. Gordon, “Alternative activation of macrophages: an immunologic functional perspective,” Annual Review of Immunology, vol. 27, pp. 451–483, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. K. Moro, T. Yamada, M. Tanabe et al., “Innate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+ lymphoid cells,” Nature, vol. 463, no. 7280, pp. 540–544, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. D. R. Neill, S. H. Wong, A. Bellosi et al., “Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity,” Nature, vol. 464, no. 7293, pp. 1367–1370, 2010. View at Publisher · View at Google Scholar · View at Scopus
  102. Y.-J. Chang, H. Y. Kim, L. A. Albacker et al., “Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity,” Nature Immunology, vol. 12, no. 7, pp. 631–638, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. J. M. Mjosberg, S. Trifari, N. K. Crellin et al., “Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161,” Nature Immunology, vol. 12, pp. 1055–1062, 2011. View at Publisher · View at Google Scholar
  104. H. Y. Kim, Y. J. Chang, S. Subramanian et al., “Innate lymphoid cells responding to IL-33 mediate airway hyperreactivity independently of adaptive immunity,” The Journal of Allergy and Clinical Immunology, vol. 129, no. 1, pp. 216.e6–227.e6, 2012. View at Publisher · View at Google Scholar
  105. J. L. Barlow, A. Bellosi, C. S. Hardman et al., “Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity,” The Journal of Allergy and Clinical Immunology, vol. 129, no. 1, pp. 191.e4–198.e4, 2012. View at Publisher · View at Google Scholar
  106. T. Y. Halim, R. H. Krauss, A. C. Sun, and F. Takei, “Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation,” Immunity, vol. 36, no. 3, pp. 451–463, 2012. View at Publisher · View at Google Scholar
  107. B. C. Petersen, A. L. Budelsky, A. P. Baptist, M. A. Schaller, and N. W. Lukacs, “Interleukin-25 induces type 2 cytokine production in a steroid-resistant interleukin-17RB+ myeloid population that exacerbates asthmatic pathology,” Nature Medicine, vol. 18, pp. 751–758, 2012. View at Publisher · View at Google Scholar
  108. E. K. Miller, J. Z. Hernandez, V. Wimmenauer et al., “A mechanistic role for type III IFN-λ1 in Asthma exacerbations mediated by human rhinoviruses,” American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 5, pp. 508–516, 2012. View at Publisher · View at Google Scholar
  109. V. Bandi, M. A. Apicella, E. Mason et al., “Nontypeable Haemophilus influenzae in the lower respiratory tract of patients with chronic bronchitis,” American Journal of Respiratory and Critical Care Medicine, vol. 164, no. 11, pp. 2114–2119, 2001. View at Scopus
  110. S. Sethi, N. Evans, B. J. B. Grant, and T. F. Murphy, “New strains of bacteria and exacerbations of chronic obstructive pulmonary disease,” The New England Journal of Medicine, vol. 347, no. 7, pp. 465–471, 2002. View at Publisher · View at Google Scholar · View at Scopus
  111. P. Mallia, S. D. Message, V. Gielen et al., “Experimental rhinovirus infection as a human model of chronic obstructive pulmonary disease exacerbation,” American Journal of Respiratory and Critical Care Medicine, vol. 183, no. 6, pp. 734–742, 2011. View at Publisher · View at Google Scholar · View at Scopus
  112. A. Bhowmik, T. A. R. Seemungal, R. J. Sapsford, and J. A. Wedzicha, “Relation of sputum inflammatory markers to symptoms and lung function changes in COPD exacerbations,” Thorax, vol. 55, no. 2, pp. 114–120, 2000. View at Publisher · View at Google Scholar · View at Scopus
  113. Y. Qiu, J. Zhu, V. Bandi et al., “Biopsy neutrophilia, neutrophil chemokine and receptor gene expression in severe exacerbations of chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 168, no. 8, pp. 968–975, 2003. View at Publisher · View at Google Scholar · View at Scopus
  114. S. Gompertz, C. O'Brien, D. L. Bayley, S. L. Hill, and R. A. Stockley, “Changes in bronchial inflammation during acute exacerbations of chronic bronchitis,” European Respiratory Journal, vol. 17, no. 6, pp. 1112–1119, 2001. View at Publisher · View at Google Scholar · View at Scopus
  115. S. W. Crooks, D. L. Bayley, S. L. Hill, and R. A. Stockley, “Bronchial inflammation in acute bacterial exacerbations of chronic bronchitis: the role of leukotriene B4,” European Respiratory Journal, vol. 15, no. 2, pp. 274–280, 2000. View at Publisher · View at Google Scholar · View at Scopus
  116. S. D. Aaron, J. B. Angel, M. Lunau et al., “Granulocyte inflammatory markers and airway infection during acute exacerbation of chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 2, pp. 349–355, 2001. View at Scopus
  117. M. Saetta, G. Turato, P. Maestrelli, C. E. Mapp, and L. M. Fabbri, “Cellular and structural bases of chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 6, pp. 1304–1309, 2001. View at Scopus
  118. P. F. Mercer, J. K. Shute, A. Bhowmik, G. C. Donaldson, J. A. Wedzicha, and J. A. Warner, “MMP-9, TIMP-1 and inflammatory cells in sputum from COPD patients during exacerbation,” Respiratory Research, vol. 6, article 151, 2005. View at Publisher · View at Google Scholar · View at Scopus
  119. W. Wu, K. B. Patel, J. L. Leland Booth, W. Zhang, and J. P. Metcalf, “Cigarette smoke extract suppresses the RIG-I-initiated innate immune response to influenza virus in the human lung,” American Journal of Physiology, vol. 300, no. 6, pp. L821–L830, 2011. View at Publisher · View at Google Scholar · View at Scopus
  120. D. Wat, C. Gelder, S. Hibbitts et al., “The role of respiratory viruses in cystic fibrosis,” Journal of Cystic Fibrosis, vol. 7, no. 4, pp. 320–328, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. A. R. Smyth, R. L. Smyth, C. Y. W. Tong, C. A. Hart, and D. P. Heaf, “Effect of respiratory virus infections including rhinovirus on clinical status in cystic fibrosis,” Archives of Disease in Childhood, vol. 73, no. 2, pp. 117–120, 1995. View at Scopus
  122. J. Collinson, K. G. Nicholson, E. Cancio et al., “Effects of upper respiratory tract infections in patients with cystic fibrosis,” Thorax, vol. 51, no. 11, pp. 1115–1122, 1996. View at Scopus
  123. B. E. van Ewijk, M. M. van der Zalm, T. F. W. Wolfs et al., “Prevalence and impact of respiratory viral infections in young children with cystic fibrosis: prospective cohort study,” Pediatrics, vol. 122, no. 6, pp. 1171–1176, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. R. F. Lemanske, D. J. Jackson, R. E. Gangnon et al., “Rhinovirus illnesses during infancy predict subsequent childhood wheezing,” The Journal of Allergy and Clinical Immunology, vol. 116, no. 3, pp. 571–577, 2005. View at Publisher · View at Google Scholar · View at Scopus
  125. D. J. Jackson, R. E. Gangnon, M. D. Evans et al., “Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children,” American Journal of Respiratory and Critical Care Medicine, vol. 178, no. 7, pp. 667–672, 2008. View at Publisher · View at Google Scholar · View at Scopus
  126. A. Kotaniemi-Syrjänen, R. Vainionpää, T. M. Reijonen, M. Waris, K. Korhonen, and M. Korppi, “Rhinovirus-induced wheezing in infancy—the first sign of childhood asthma?” The Journal of Allergy and Clinical Immunology, vol. 111, no. 1, pp. 66–71, 2003. View at Publisher · View at Google Scholar · View at Scopus
  127. T. M. Reijonen, A. Kotaniemi-Syrjanen, K. Korhonen, and M. Korppi, “Predictors of asthma three years after hospital admission for wheezing in infancy,” Pediatrics, vol. 106, no. 6, pp. 1406–1412, 2000. View at Scopus
  128. D. J. Jackson, M. D. Evans, R. E. Gangnon et al., “Evidence for a causal relationship between allergic sensitization and rhinovirus wheezing in early life,” American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 3, pp. 281–285, 2012. View at Publisher · View at Google Scholar
  129. K. N. Carroll, T. Gebretsadik, P. Minton et al., “Influence of maternal asthma on the cause and severity of infant acute respiratory tract infections,” The Journal of Allergy and Clinical Immunology, vol. 129, no. 5, pp. 1236–1242, 2012. View at Publisher · View at Google Scholar
  130. H. Bisgaard, S. M. Jensen, and K. Bønnelykke, “Interaction between asthma and lung function growth in early life,” American Journal of Respiratory and Critical Care Medicine, vol. 185, pp. 1183–1189, 2012. View at Publisher · View at Google Scholar
  131. D. Schneider, J. Y. Hong, A. P. Popova et al., “Neonatal rhinovirus infection induces persistent mucous metaplasia and airways hyperresponsiveness,” The Journal of Immunology, vol. 188, no. 6, pp. 2894–2904, 2012. View at Publisher · View at Google Scholar
  132. E. Y. Kim, J. T. Battaile, A. C. Patel et al., “Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease,” Nature Medicine, vol. 14, no. 6, pp. 633–640, 2008. View at Publisher · View at Google Scholar · View at Scopus
  133. G. E. Kaiko, S. Phipps, P. Angkasekwinai, C. Dong, and P. S. Foster, “NK cell deficiency predisposes to viral-induced Th2-type allergic inflammation via epithelial-derived IL-25,” Journal of Immunology, vol. 185, no. 8, pp. 4681–4690, 2010. View at Publisher · View at Google Scholar · View at Scopus
  134. L. G. Gregory, S. A. Mathie, S. A. Walker, S. Pegorier, C. P. Jones, and C. M. Lloyd, “Overexpression of Smad2 drives house dust mite-mediated airway remodeling and airway hyperresponsiveness via activin and IL-25,” American Journal of Respiratory and Critical Care Medicine, vol. 182, no. 2, pp. 143–154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  135. A. Kato and R. P. Schleimer, “Beyond inflammation: airway epithelial cells are at the interface of innate and adaptive immunity,” Current Opinion in Immunology, vol. 19, no. 6, pp. 711–720, 2007. View at Publisher · View at Google Scholar · View at Scopus
  136. M. A. Rank, T. Kobayashi, H. Kozaki, K. R. Bartemes, D. L. Squillace, and H. Kita, “IL-33-activated dendritic cells induce an atypical TH2-type response,” The Journal of Allergy and Clinical Immunology, vol. 123, no. 5, pp. 1047–1054, 2009. View at Publisher · View at Google Scholar · View at Scopus
  137. A. Al-Shami, R. Spolski, J. Kelly, A. Keane-Myers, and W. J. Leonard, “A role for TSLP in the development of inflammation in an asthma model,” Journal of Experimental Medicine, vol. 202, no. 6, pp. 829–839, 2005. View at Publisher · View at Google Scholar · View at Scopus
  138. A. Kato, S. Favoreto, P. C. Avila, and R. P. Schleimer, “TLR3- and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells,” Journal of Immunology, vol. 179, no. 2, pp. 1080–1087, 2007. View at Scopus
  139. Y. Nagata, H. Kamijuku, M. Taniguchi, S. Ziegler, and K. I. Seino, “Differential role of thymic stromal lymphopoietin in the induction of airway hyperreactivity and Th2 immune response in antigen-induced asthma with respect to natural killer T cell function,” International Archives of Allergy and Immunology, vol. 144, no. 4, pp. 305–314, 2007. View at Publisher · View at Google Scholar · View at Scopus