Modulation of epithelial biology by rhinovirus infection: Role in inflammatory airway diseases

Future Virology

Volumn 6, Issue 3, 2011, Pages 375-386

  Leigh, Richard ^a   Proud, David ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

antivirals; asthma; chemokines; chronic obstructive pulmonary disease; cytokines; epithelial cell; growth factors; rhinovirus

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERCELLULAR ADHESION MOLECULE 1; INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; INTERLEUKIN 8; RANTES; TOLL LIKE RECEPTOR 3;

AIRWAY REMODELING; ASTHMA; CHRONIC OBSTRUCTIVE LUNG DISEASE; CIGARETTE SMOKING; DISEASE EXACERBATION; ENVIRONMENTAL FACTOR; EPITHELIUM CELL; HOST RESISTANCE; HUMAN; IMMUNOMODULATION; INNATE IMMUNITY; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT INFLAMMATION; REVIEW; RHINOVIRUS INFECTION; VIRUS REPLICATION;

HUMAN RHINOVIRUS SP.; RHINOVIRUS;

EID: 79953312109     PISSN: 17460794     EISSN: None     Source Type: Journal    
DOI: 10.2217/fvl.11.9     Document Type: Review

References (89)

1. Proud D, Chow C-W: Role of viral infections in asthma and chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol. 35, 513-518 (2006).
2. Traves SL, Proud D: Viral-associated exacerbations of asthma and COPD. Curr. Opin. Pharmacol. 7, 252-258 (2007).
3. Nicholson KG, Kent J, Ireland DC: Respiratory viruses and exacerbations of asthma in adults. Br. Med. J. 307, 982-986 (1993).
4. Johnston SL, Pattemore PK, Sanderson G et al.: Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. Br. Med. J. 310, 1225-1229 (1995).
5. Khetsuriani N, Kazerouni NN, Erdman DD et al.: Prevalence of viral respiratory tract infections in children with asthma. J. Allergy Clin. Immunol. 119, 314-321 (2007).
6. Seemungal T, Harper-Owen R, Bhowmik A et al.: Respiratory viruses, symptoms and inflammatory markers in acute exacerbations and stable chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 164, 1618-1623 (2001).
7. Rohde G, Wiethege A, Borg I et al.: Respiratory viruses in exacerbations of chronic obstructive pulmonary disease requiring hospitalisation: a case - control study. Thorax 58, 37-42 (2003).
8. Smith DH, Malone DC, Lawson KA, Okamoto LJ, Battista C, Saunders WB: A national estimate of the economic costs of asthma. Am. J. Respir. Crit. Care Med. 156, 787-793 (1997).
9. Pauwels RA, Buist AS, Calverley PM, Jenkins CR, Hurd SS: Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO global initiative for chronic obstructive lung disease (GOLD) workshop summary. Am. J. Respir. Crit. Care Med. 163, 1256-1276 (2001).
10. Schroth MK, Grimm E, Frindt P et al.: Rhinovirus replication causes RANTES production in primary bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 20, 1220-1228 (1999).
11. Mosser AG, Vrtis R, Burchell L et al.: Quantitative and qualitative analysis of rhinovirus infection in bronchial tissues. Am. J. Respir. Crit. Care Med. 171, 645-651 (2005).
12. Papadopoulos NG, Bates PJ, Bardin PG et al.: Rhinoviruses infect the lower airways. J. Infect. Dis. 181, 1875-1884 (2000).
13. Sanders SP, Siekierski ES, Porter JD, Richards SM, Proud D: Nitric oxide inhibits rhinovirus-induced cytokine production and viral replication in a human respiratory epithelial cell line. J. Virol. 72, 934-942 (1998).
14. Donninger H, Glashoff R, Haitchi H-M, Syce JA, Ghildyal R, Bardin PG: Rhinovirus induction of the CXC chemokine epithelialneutrophil activating peptide-78 in bronchial epithelium. J. Infect. Dis. 187, 1809-1817 (2003).
15. Spurrell JC, Wiehler S, Zaheer RS, Sanders SP, Proud D: Human airway epithelial cells produce IP-10 (CXCL10) in vitro and in vivo upon rhinovirus infection. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L85-L95 (2005).
16. Proud D, Gwaltney JM Jr, Hendley JO, Dinarello CA, Gillis S, Schleimer RP: Increased levels of interleukin-1 are detected in nasal secretions of volunteers during experimental rhinovirus colds. J. Infect. Dis. 169, 1007-1013 (1994).
17. Teran LM, Seminario MC, Shute JK et al.: RANTES, macrophage-inhibitory protein 1a, and the eosinophil product major basic protein are released into upper respiratory secretions during virus-induced asthma exacerbations in children. J. Infect. Dis. 179, 677-681 (1999).
18. Psarras S, Volonaki E, Skevaki CL et al.: Vascular endothelial growth factor-mediated induction of angiogenesis by human rhinovirus. J. Allergy Clin. Immunol. 117, 291-297 (2006).
19. Leigh R, Oyelusi W, Wiehler S et al.: Human rhinovirus infection enhances airway epithelial cell production of growth factors involved in airway remodeling. J. Allergy Clin. Immunol. 121, 1238-1245 (2008). Provided clear evidence that human rhinovirus (HRV)-infection of epithelial cells induces production of growth factors that could contribute to several aspects of airway remodeling.
20. Tacon CE, Wiehler S, Holden NS, Newton R, Proud D, Leigh R: Human rhinovirus infection of airway epithelial cells upregulates MMP-9 production via NF-κB. Am. J. Respir. Cell Mol. Biol. 43, 201-209 (2010).
21. Grissell TV, Powell H, Shafren DR et al.: Interleukin-10 gene expression in acute virus-induced asthma. Am. J. Respir. Crit. Care Med. 172, 433-439 (2005).
22. Newcomb DC, Sajjan U, Nanua S et al.: Phosphatidylinositol 3-kinase is required for rhinovirus-induced airway epithelial cell interleukin-8 expression. J. Biol. Chem. 280, 36952-36961 (2005).
23. Baggiolini M, Dewald B, Moser B: Human chemokines: an update. Annu. Rev. Immunol. 15, 675-705 (1997).
24. Kobayashi Y: Neutrophil infiltration and chemokines. Crit. Rev. Immunol. 26, 307-316 (2006).
25. Kishimoto T: The biology of interleukin-6. Blood 74, 1-10 (1989).
26. Scheller J, Rose-John S: Interleukin-6 and its receptor: from bench to bedside. Med. Microbiol. Immunol. 195, 175-183 (2006).
27. Dufour JH, Dziejman M, Liu MT, Leung JH, Jane TE, Luster AD: IFN-g-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T-cell generation and trafficking. J. Immunol. 168, 3915-3204 (2002).
28. Nickel R, Beck LA, Stellato C, Schleimer RP: Chemokines and allergic disease. J. Allergy Clin. Immunol. 104, 723-742 (1999).
29. Palmenberg AC, Spiro D, Kuzmickas R et al.: Sequencing and analysis of all known human rhinovirus genomes reveal structure and evolution. Science 324, 55-59 (2009).
30. Gern JE: The ABCs of rhinoviruses, wheezing, and asthma. J. Virol. 84, 7418-7426 (2010).
31. Wiehler S, Proud D: Interleukin-17A modulates human airway epithelial responses to human rhinovirus infection. Am. J. Physiol. Cell. Mol. Physiol. 293, L505-L515 (2007).
32. Wang X, Lau C, Wiehler S et al.: Syk is downstream of intercellular adhesion molecule-1 and mediates human rhinovirus activation of p38 MAPK in airway epithelial cells. J. Immunol. 177, 6859-6870 (2006). Provided first rational explanation for ICAM-1-mediated signaling after HRV binding.
33. Lau C, Wang X, Song L et al.: Syk associates with clathrin and mediates phosphatidylinositol 3-kinase activation during human rhinovirus internalization. J. Immunol. 180, 870-880 (2008). Extended earlier observations to link Syk to internalization of HRV in epithelial cells.
34. Bentley JK, Newcomb DC, Goldsmith AM, Jia Y, Sajjan US, Hershenson MB: Rhinovirus activates interleukin-8 expression via a Src/p110β phosphatylinositol 3-kinase pathway in human airway epithelial cells. J. Virol. 81, 1186-1194 (2007).
35. Edelmann KH, Richardson-Burns S, Alexopoulou L, Tyler KL, Flavell RA, Oldstone MB: Does Toll-like receptor 3 play a biological role in virus infections? Virology 322, 231-238 (2004).
36. Kato H, Takeuchi O, Mikamo-Satoh E et al.: Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205, 1601-1610 (2008).
37. Kato H, Takeuchi O, Sato S et al.: Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 414, 101-105 (2006).
38. Wang Q, Nagarker DR, Bowman ER et al.: Role of double-stranded RNA pattern recognition receptors in rhinovirus-induced airway epithelial cell responses. J. Immunol. 183, 6989-6997 (2009).
39. Takeuchi O, Akira S: Innate immunity to virus infection. Immunol. Rev. 227, 75-86 (2009).
40. Koetzler R, Zaheer RS, Newton R, Proud D: Nitric oxide inhibits IFN regulatory factor 1 and nuclear factor-κB pathways in rhinovirusinfected epithelial cells. J. Allergy Clin. Immunol. 124, 551-557 (2009).
41. Edwards MR, Hewson CA, Laza-Stanca V et al.: Protein kinase R, IκB kinase-β and NF-κB are required for human rhinovirus induced proinflammatory cytokine production in bronchial epithelial cells. Mol. Immunol. 44, 1587-1597 (2007).
42. Nakhaei P, Genin P, Civas A, Hiscott J: RIG-I-like receptors: Sensing and responding to RNA virus infection. Semin. Immunol. 21, 215-222 (2009).
43. Kotla S, Peng T, Bumgarner RE, Gustin KE: Attenuation of the type I interferon response in cells infected with human rhinovirus. Virology 374, 399-410 (2008).
44. Schneider D, Ganesan S, Comstock AT et al.: Increased cytokine response of rhinovirusinfected airway epithelial cells in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 182, 332-340 (2010).
45. Zaheer RS, Proud D: Human rhinovirus-induced epithelial production of CXCL10 is dependent upon IFN regulatory factor-1. Am. J. Respir. Cell Mol. Biol. 43, 413-421 (2010).
46. Stirnweiss A, Ksienzyk A, Klages K et al.: IFN regulatory factor-1 bypassess IFN-mediated antiviral effects through viperin gene induction. J. Immunol. 184, 5179-5185 (2010).
47. Zaheer RS, Koetzler R, Holden NS, Wiehler S, Proud D: Selective transcriptional down-regulation of human rhinovirus- induced production of CXCL10 from airway epithelial cells via the MEK1 pathway. J. Immunol. 182, 4854-4864 (2009).
48. Amineva SP, Aminev AG, Palmenberg AC, Gern JE: Rhinovirus 3C protease precursors 3CD and 3CD? localize to the nuclei of infected cells. J. Gen. Virol. 85, 2969-2979 (2004).
49. Ghildyal R, Jordan B, Li D et al.: Rhinovirus 3C protease can localize to the nucleus and alter active and passive nucleocytoplasmic transport. J. Virol. 83, 7349-7352 (2009).
50. Proud D, Sanders SP, Wiehler S: Human rhinovirus infection induces airway epithelial cell production of human β-defensin-2 both in vitro and in vivo. J. Immunol. 172, 4637-4645 (2004).
51. 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. 178, 962-968 (2008). First comprehensive analysis of epithelial gene expression during in vivo experimental HRV infection. Established viperin as a component of host defense to HRV.
52. 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. 201, 937-947 (2005).
53. Contoli M, Message SD, Laza-Stanca V et al.: Role of deficient type-III interferon-l production in asthma exacerbations. Nat. Med. 12, 1023-1026 (2006).
54. 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. 123, 1384-1390 (2009).
55. 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. 3, 69-80 (2010).
56. Schmid S, Mordstein M, Kochs G, García-Sastre A, Tenoever BR: Transcription factor redundancy ensures induction of the antiviral state. J. Biol. Chem. 285, 42013-42022 (2010). Provided definitive evidence of interferon (IFN)-independent viral induction of a panel of 'IFN-stimulated genes' in cells lacking receptors for type I and type III IFNs.
57. Zhang Y, Burke CW, Ryman KD, Klimstra WB: Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J. Virol. 81, 11246-11255 (2007).
58. Wang X, Hinson ER, Cresswell P: The interferon-inducible protein viperin inhibits influenza virus release by perturbing lipid rafts. Cell Host Microbe 2, 96-105 (2007).
59. Shaveta G, Shi J, Chow VT, Song J: Structural characterization reveals that viperin is a radical S-adenosyl-l-methionine (SAM) enzyme. Biochem. Biophys. Res. Commun. 391, 1390-1395 (2010).
60. Sanders SP, Siekierski ES, Richards SM, Porter JD, Imani F, Proud D: Rhinovirus infection induces expression of type 2 nitric oxide synthase in human respiratory epithelial cells in vitro and in vivo. J. Allergy Clin. Immunol. 107, 235-243 (2001).
61. Sanders SP, Proud D, Siekierski ES, Yachechko R, Liu MC: Role of nasal nitric oxide in the resolution of experimental rhinovirus infection. J. Allergy Clin. Immunol. 113, 697-702 (2004).
62. Koetzler R, Zaheer RS, Wiehler S, Holden NS, Giembycz MA, Proud D: Nitric oxide inhibits human rhinovirus-induced transcriptional activation of CXCL10 in airway epithelial cells. J. Allergy Clin. Immunol. 123, 201-208 (2009).
63. James AL, Wenzel S: Clinical relevance of airway remodelling in airway diseases. Eur. Respir. J. 30, 134-155 (2007).
64. Pohunek P, Warner JO, Turzíková J, Kudrmann J, Roche WR: Markers of eosinophilic inflammation and tissue re-modelling in children before clinically diagnosed bronchial asthma. Pediatr. Allergy Immunol. 16, 43-51 (2005).
65. Saglani S, Malmström K, Pelkonen AS et al.: Airway remodeling and inflammation in symptomatic infants with reversible airflow obstruction. Am. J. Respir. Crit. Care Med. 171, 722-727 (2005).
66. Saglani S, Payne DN, Zhu J, Nicholson AG, Bush A, Jeffery PK: Early detection of airway wall remodeling and eosinophilic inflammation in preschool wheezers. Am. J. Respir. Crit. Care Med. 176, 858-864 (2007).
67. Jackson DJ, Gangnon RD, Evans MD et al.: Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am. J. Respir. Crit. Care Med. 178, 667-672 (2008). Established role of HRV-induced wheezing episodes in early life as a risk factor for the development of asthma.
68. Jartti T, Lee W-M, Pappas T, Evans M, Lemanske RF, Gern JE: Serial viral infections in infants with recurrent respiratory illnesses. Eur. Respir. J. 32, 314-320 (2008). Clearly demonstrated that children can have numerous episodes of wheezing triggered by serial infections with different strains of HRV in a given year.
69. Holgate ST: Epithelium dysfunction in asthma. J. Allergy Clin. Immunol. 120, 1233-1244 (2007).
70. 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. 178, 1271-1281 (2008).
71. Inoue D, Yamaya M, Kubo H et al.: Mechanisms of mucin production by rhinovirus infection in cultured human airway epithelial cells. Respir. Physiol. Neurobiol. 154, 484-499 (2006).
72. Zhu L, Lee P, Lee W-M, Zhao Y, Yu D, Chen Y: Rhinovirus-induced major airway mucin production involves a novel TLR3-EGFR-dependent pathway. Am. J. Respir. Cell Mol. Biol. 40, 610-619 (2009).
73. Hewson CA, Haas JJ, Bartlett NW et al.: Rhinovirus induces MUC5AC in a human infection model and in vitro via NF-kB and EGFR pathways. Eur. Respir. J. 36, 1425-1435 (2010).
74. Enomoto Y, Orihara K, Takamasu T et al.: Tissue remodeling induced by hypersecreted epidermal growth factor and amphiregulin in the airway after an acute asthma attack. J. Allergy Clin. Immunol. 124, 913-920 (2009).
75. Gregory LG, Mathie SA, Walker SA, Pegorier S, Jones CP, Lloyd CM: Overexpression of Smad2 drives house dust mite-mediated airway remodeling and airway hyperresponsiveness via activin and IL-25. Am. J. Respir. Crit. Care Med. 182, 143-154 (2010).
76. De Silva D, Dagher H, Ghildyal R et al.: Vascular endothelial growth factor induction by rhinovirus infection. J. Med. Virol. 78, 666-672 (2006).
77. Lee CG, Yoon HJ, Zhu Z et al.: Respiratory syncytial virus stimulation of vascular endothelial growth factor/vascular permeability factor. Am. J. Respir. Cell Mol. Biol. 23, 662-669 (2000).
78. Erlwyn-Lajeunesse MD, Hunt LP, Pohunek P et al.: Bronchoalveolar lavage MMP-9 and TIMP-1 in preschool wheezers and their relationship to persitent wheeze. Pediatr. Res. 64, 194-199 (2008).
79. Broide DH: Immunologic and inflammatory mechanisms that drive asthma progression to remodeling. J. Allergy Clin. Immunol. 121, 560-570 (2008).
80. Lachowicz-Scroggins ME, Boushey HA, Finkbeiner WE, Widdicombe JH: Interleukin-13 induced mucous metaplasia increases susceptibility of human airway epithelium to rhinovirus infection. Am. J. Respir. Cell Mol. Biol. 43, 652-661 (2010).
81. Alcorn JF, Crowe CR, Kolls JK: TH17 cells in asthma and COPD. Annu. Rev. Physiol. 72, 495-516 (2010).
82. Qiu Y, Bandi V, Atmar RL, Hattotuwa K, Guntupalli KK, Jeffery PK: Biopsy neutrophilia, neutrophil chemokine and receptor gene expression in severe exacerbations of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 168, 968-975 (2003).
83. Wark PA, Johnston SL, Moric I, Simpson JL, Hensley MJ, Gibson PG: Neutrophil degranulation and cell lysis is associated with clinical severity in virus-induced asthma. Eur. Respir. J. 19, 68-75 (2002).
84. Green RH, Brightling CE, Woltmann G, Parker D, Wardlaw AJ, Pavord ID: Analysis of induced sputum in adults with asthma: identification of subgroup with isolated sputum neutrophilia and poor response to inhaled corticosteroids. Thorax 57, 875-879 (2002).
85. McLeish AC, Zvolensky MJ: Asthma and cigarette smoking: a review of the empirical literature. J. Asthma 47, 345-361 (2010).
86. Cohen S, Tyrrell DA, Russell MA, Jarvis MJ, Smith AP: Smoking, alcohol consumption, and susceptibility to the common cold. Am. J. Public Health 83, 1277-1283 (1993).
87. Blake GH, Abell TD, Stanley WG: Cigarette smoking and upper respiratory infection among recruits in basic combat training. Ann. Intern. Med. 109, 198-202 (1988).
88. Hudy MH, Traves SL, Wiehler S, Proud D: Cigarette smoke modulates rhinovirusinduced airway epithelial chemokine production. Eur. Respir. J. 35, 1256-1263 (2010). First demonstration that cigarette smoke exposure alters the pattern of inflammatory chemokines induced in HRV-infected epithelial cells and provided initial mechanistic insights.
89. Eddleston J, Lee RU, Doerner AM, Herschbach J, Zuraw BL: Cigarette smoke decreases the innate responses of epithelial cells to rhinovirus infection. Am. J. Respir. Cell Mol. Biol. 44, 118-126 (2011).