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Respiratory Research
Published in: Respiratory Research 1/2018

Open Access 01-12-2018 | Review

Modulation of airway hyperresponsiveness by rhinovirus exposure

Authors: Dennis Lo, Joshua L. Kennedy, Richard C. Kurten, Reynold A. Panettieri Jr, Cynthia J. Koziol-White

Published in: Respiratory Research | Issue 1/2018

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Abstract

Rhinovirus (RV) exposure has been implicated in childhood development of wheeze evoking asthma and exacerbations of underlying airways disease. Studies such as the Copenhagen Prospective Studies on Asthma in Childhood (COPSAC) and Childhood Origins of ASThma (COAST) have identified RV as a pathogen inducing severe respiratory disease. RVs also modulate airway hyperresponsiveness (AHR), a key characteristic of such diseases. Although potential factors underlying mechanisms by which RV induces AHR have been postulated, the precise mechanisms of AHR following RV exposure remain elusive.
A challenge to RV-related research stems from inadequate models for study. While human models raise ethical concerns and are relatively difficult in terms of subject recruitment, murine models are limited by susceptibility of infection to the relatively uncommon minor group (RV-B) serotypes, strains that are generally associated with infrequent clinical respiratory virus infections. Although a transgenic mouse strain that has been developed has enhanced susceptibility for infection with the common major group (RV-A) serotypes, few studies have focused on RV in the context of allergic airways disease rather than understanding RV-induced AHR. Recently, the receptor for the virulent RV-C CDHR3, was identified, but a dearth of studies have examined RV-C-induced effects in humans.
Currently, the mechanisms by which RV infections modulate airway smooth muscle (ASM) shortening or excitation-contraction coupling remain elusive. Further, only one study has investigated the effects of RV on bronchodilatory mechanisms, with only speculation as to mechanisms underlying RV-mediated modulation of bronchoconstriction.
Literature
1.
Postma DS, Kerstjens HA. Characteristics of airway hyperresponsiveness in asthma and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998;158:S187–92.PubMedCrossRef
2.
Jude J, Koziol-White C, Scala J, Yoo E, Jester W, Maute C, Dalton P, Panettieri R Jr. Formaldehyde induces rho-associated kinase activity to evoke airway Hyperresponsiveness. Am J Respir Cell Mol Biol. 2016;55:542–53.PubMedPubMedCentralCrossRef
3.
Cho HY, Zhang LY, Kleeberger SR. Ozone-induced lung inflammation and hyperreactivity are mediated via tumor necrosis factor-alpha receptors. Am J Physiol Lung Cell Mol Physiol. 2001;280:L537–46.PubMedCrossRef
4.
Roux E, Guibert C, Crevel H, Savineau JP, Marthan R. Human and rat airway smooth muscle responsiveness after ozone exposure in vitro. Am J Phys. 1996;271:L631–6.
5.
Seltzer J, Bigby BG, Stulbarg M, Holtzman MJ, Nadel JA, Ueki IF, Leikauf GD, Goetzl EJ, Boushey HA. O3-induced change in bronchial reactivity to methacholine and airway inflammation in humans. J Appl Physiol (1985). 1986;60:1321–6.CrossRef
6.
Cooper PR, Lamb R, Day ND, Branigan PJ, Kajekar R, San Mateo L, Hornby PJ, Panettieri RA Jr. TLR3 activation stimulates cytokine secretion without altering agonist-induced human small airway contraction or relaxation. Am J Physiol Lung Cell Mol Physiol. 2009;297:L530–7.PubMedCrossRef
7.
McGraw DW, Elwing JM, Fogel KM, Wang WC, Glinka CB, Mihlbachler KA, Rothenberg ME, Liggett SB. Crosstalk between Gi and Gq/Gs pathways in airway smooth muscle regulates bronchial contractility and relaxation. J Clin Invest. 2007;117:1391–8.PubMedPubMedCentralCrossRef
8.
Risse PA, Jo T, Suarez F, Hirota N, Tolloczko B, Ferraro P, Grutter P, Martin JG. Interleukin-13 inhibits proliferation and enhances contractility of human airway smooth muscle cells without change in contractile phenotype. Am J Physiol Lung Cell Mol Physiol. 2011;300:L958–66.PubMedCrossRef
9.
Tliba O, Deshpande D, Chen H, Van Besien C, Kannan M, Panettieri RA Jr, Amrani Y. IL-13 enhances agonist-evoked calcium signals and contractile responses in airway smooth muscle. Br J Pharmacol. 2003;140:1159–62.PubMedPubMedCentralCrossRef
10.
Amrani Y, Martinet N, Bronner C. Potentiation by tumour necrosis factor-alpha of calcium signals induced by bradykinin and carbachol in human tracheal smooth muscle cells. Br J Pharmacol. 1995;114:4–5.PubMedPubMedCentralCrossRef
11.
Hotta K, Emala CW, Hirshman CA. TNF-alpha upregulates Gialpha and Gqalpha protein expression and function in human airway smooth muscle cells. Am J Phys. 1999;276:L405–11.
12.
Freymuth F, Vabret A, Brouard J, Toutain F, Verdon R, Petitjean J, Gouarin S, Duhamel JF, Guillois B. Detection of viral, chlamydia pneumoniae and mycoplasma pneumoniae infections in exacerbations of asthma in children. J Clin Virol. 1999;13:131–9.PubMedCrossRefPubMedCentral
13.
Johnston SL, Pattemore PK, Sanderson G, Smith S, Lampe F, Josephs L, Symington P, O'Toole S, Myint SH, Tyrrell DA, et al. Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. BMJ. 1995;310:1225–9.PubMedPubMedCentralCrossRef
14.
Miller EK, Lu X, Erdman DD, Poehling KA, Zhu Y, Griffin MR, Hartert TV, Anderson LJ, Weinberg GA, Hall CB, et al. Rhinovirus-associated hospitalizations in young children. J Infect Dis. 2007;195:773–81.PubMedCrossRef
15.
Bisgaard H. The Copenhagen prospective study on asthma in childhood (COPSAC): design, rationale, and baseline data from a longitudinal birth cohort study. Ann Allergy Asthma Immunol. 2004;93:381–9.PubMedCrossRef
16.
Lemanske RF Jr. The childhood origins of asthma (COAST) study. Pediatr Allergy Immunol. 2002;13(Suppl 15):38–43.PubMedCrossRef
17.
Heymann PW, Carper HT, Murphy DD, Platts-Mills TA, Patrie J, McLaughlin AP, Erwin EA, Shaker MS, Hellems M, Peerzada J, et al. Viral infections in relation to age, atopy, and season of admission among children hospitalized for wheezing. J Allergy Clin Immunol. 2004;114:239–47.PubMedCrossRefPubMedCentral
18.
Kennedy JL, Shaker M, McMeen V, Gern J, Carper H, Murphy D, Lee WM, Bochkov YA, Vrtis RF, Platts-Mills T, 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.PubMedPubMedCentralCrossRef
19.
Rakes GP, Arruda E, Ingram JM, Hoover GE, Zambrano JC, Hayden FG, Platts-Mills TA, Heymann PW. 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.PubMedCrossRef
20.
Soto-Quiros M, Avila L, Platts-Mills TA, Hunt JF, Erdman DD, Carper H, Murphy DD, Odio S, James HR, Patrie JT, et al. High titers of IgE antibody to dust mite allergen and risk for wheezing among asthmatic children infected with rhinovirus. J Allergy Clin Immunol. 2012;129:1499–505 e1495.PubMedPubMedCentralCrossRef
21.
de Kluijver J, Grunberg K, Sont JK, Hoogeveen M, van Schadewijk WA, de Klerk EP, Dick CR, van Krieken JH, Sterk PJ. Rhinovirus infection in nonasthmatic subjects: effects on intrapulmonary airways. Eur Respir J. 2002;20:274–9.PubMedCrossRef
22.
Grunberg K, Timmers MC, Smits HH, de Klerk EP, Dick EC, Spaan WJ, Hiemstra PS, Sterk PJ. Effect of experimental rhinovirus 16 colds on airway hyperresponsiveness to histamine and interleukin-8 in nasal lavage in asthmatic subjects in vivo. Clin Exp Allergy. 1997;27:36–45.PubMedCrossRefPubMedCentral
23.
Grunstein MM, Hakonarson H, Whelan R, Yu Z, Grunstein JS, Chuang S. Rhinovirus elicits proasthmatic changes in airway responsiveness independently of viral infection. J Allergy Clin Immunol. 2001;108:997–1004.PubMedCrossRef
24.
Kennedy JL, Koziol-White CJ, Jeffus S, Rettiganti MR, Fisher P, Kurten M, Eze A, House S, Sikes JD, Askew E, et al. Effects of rhinovirus 39 infection on airway hyperresponsiveness to carbachol in human airways precision cut lung slices. J Allergy Clin Immunol. 2018;141:1887–90 e1881.PubMedCrossRefPubMedCentral
25.
Zambrano JC, Carper HT, Rakes GP, Patrie J, Murphy DD, Platts-Mills TA, Hayden FG, Gwaltney JM Jr, Hatley TK, Owens AM, Heymann PW. Experimental rhinovirus challenges in adults with mild asthma: response to infection in relation to IgE. J Allergy Clin Immunol. 2003;111:1008–16.PubMedCrossRef
26.
Mertens TCJ, Karmouty-Quintana H, Taube C, Hiemstra PS. Use of airway epithelial cell culture to unravel the pathogenesis and study treatment in obstructive airway diseases. Pulm Pharmacol Ther. 2017;45:101–13.PubMedCrossRef
27.
Bartlett NW, Walton RP, Edwards MR, Aniscenko J, Caramori G, Zhu J, Glanville N, Choy KJ, Jourdan P, Burnet J, et al. Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation. Nat Med. 2008;14:199–204.PubMedPubMedCentralCrossRef
28.
Tuthill TJ, Papadopoulos NG, Jourdan P, Challinor LJ, Sharp NA, Plumpton C, Shah K, Barnard S, Dash L, Burnet J, et al. Mouse respiratory epithelial cells support efficient replication of human rhinovirus. J Gen Virol. 2003;84:2829–36.PubMedCrossRef
29.
Yin FH, Lomax NB. Establishment of a mouse model for human rhinovirus infection. J Gen Virol. 1986;67(Pt 11):2335–40.PubMedCrossRef
30.
Saturni S, Contoli M, Spanevello A, Papi A. Models of respiratory infections: virus-induced asthma exacerbations and beyond. Allergy Asthma Immunol Res. 2015;7:525–33.PubMedPubMedCentralCrossRef
31.
Meurs H, Gosens R, Zaagsma J. Airway hyperresponsiveness in asthma: lessons from in vitro model systems and animal models. Eur Respir J. 2008;32:487–502.PubMedCrossRef
32.
Register RB, Uncapher CR, Naylor AM, Lineberger DW, Colonno RJ. Human-murine chimeras of ICAM-1 identify amino acid residues critical for rhinovirus and antibody binding. J Virol. 1991;65:6589–96.PubMedPubMedCentral
33.
Bizzintino J, Lee WM, Laing IA, Vang F, Pappas T, Zhang G, Martin AC, Khoo SK, Cox DW, Geelhoed GC, et al. Association between human rhinovirus C and severity of acute asthma in children. Eur Respir J. 2011;37:1037–42.PubMedCrossRef
34.
Calvo C, Garcia ML, Pozo F, Reyes N, Perez-Brena P, Casas I. Role of rhinovirus C in apparently life-threatening events in infants, Spain. Emerg Infect Dis. 2009;15:1506–8.PubMedPubMedCentralCrossRef
35.
Lau SK, Yip CC, Lin AW, Lee RA, So LY, Lau YL, Chan KH, Woo PC, Yuen KY. Clinical and molecular epidemiology of human rhinovirus C in children and adults in Hong Kong reveals a possible distinct human rhinovirus C subgroup. J Infect Dis. 2009;200:1096–103.PubMedCrossRef
36.
Miller EK, Edwards KM, Weinberg GA, Iwane MK, Griffin MR, Hall CB, Zhu Y, Szilagyi PG, Morin LL, Heil LH, et al. A novel group of rhinoviruses is associated with asthma hospitalizations. J Allergy Clin Immunol. 2009;123:98–104 e101.PubMedCrossRef
37.
Iwane MK, Prill MM, Lu X, Miller EK, Edwards KM, Hall CB, Griffin MR, Staat MA, Anderson LJ, Williams JV, et al. Human rhinovirus species associated with hospitalizations for acute respiratory illness in young US children. J Infect Dis. 2011;204:1702–10.PubMedCrossRef
38.
Lee WM, Lemanske RF Jr, Evans MD, Vang F, Pappas T, Gangnon R, Jackson DJ, Gern JE. Human rhinovirus species and season of infection determine illness severity. Am J Respir Crit Care Med. 2012;186:886–91.PubMedPubMedCentralCrossRef
39.
Linsuwanon P, Payungporn S, Samransamruajkit R, Posuwan N, Makkoch J, Theanboonlers A, Poovorawan Y. High prevalence of human rhinovirus C infection in Thai children with acute lower respiratory tract disease. J Inf Secur. 2009;59:115–21.
40.
Xiang Z, Gonzalez R, Xie Z, Xiao Y, Liu J, Chen L, Liu C, Zhang J, Ren L, Vernet G, et al. Human rhinovirus C infections mirror those of human rhinovirus a in children with community-acquired pneumonia. J Clin Virol. 2010;49:94–9.PubMedCrossRefPubMedCentral
41.
Bartlett NW, Singanayagam A, Johnston SL. Mouse models of rhinovirus infection and airways disease. Methods Mol Biol. 2015;1221:181–8.PubMedCrossRef
42.
Singanayagam A, Glanville N, Walton RP, Aniscenko J, Pearson RM, Pinkerton JW, Horvat JC, Hansbro PM, Bartlett NW, Johnston SL. A short-term mouse model that reproduces the immunopathological features of rhinovirus-induced exacerbation of COPD. Clin Sci (Lond). 2015;129:245–58.CrossRef
43.
Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol. 2004;172:2731–8.PubMedCrossRef
44.
45.
Bates JH, Irvin CG. Measuring lung function in mice: the phenotyping uncertainty principle. J Appl Physiol (1985). 2003;94:1297–306.CrossRef
46.
Hao W, Bernard K, Patel N, Ulbrandt N, Feng H, Svabek C, Wilson S, Stracener C, Wang K, Suzich J, et al. Infection and propagation of human rhinovirus C in human airway epithelial cells. J Virol. 2012;86:13524–32.PubMedPubMedCentralCrossRef
47.
Bochkov YA, Watters K, Ashraf S, Griggs TF, Devries MK, Jackson DJ, Palmenberg AC, Gern JE. Cadherin-related family member 3, a childhood asthma susceptibility gene product, mediates rhinovirus C binding and replication. Proc Natl Acad Sci U S A. 2015;112:5485–90.PubMedPubMedCentralCrossRef
48.
Damera G, Zhao H, Wang M, Smith M, Kirby C, Jester WF, Lawson JA, Panettieri RA Jr. Ozone modulates IL-6 secretion in human airway epithelial and smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2009;296:L674–83.PubMedPubMedCentralCrossRef
49.
Malavia NK, Raub CB, Mahon SB, Brenner M, Panettieri RA Jr, George SC. Airway epithelium stimulates smooth muscle proliferation. Am J Respir Cell Mol Biol. 2009;41:297–304.PubMedPubMedCentralCrossRef
50.
Van Ly D, Faiz A, Jenkins C, Crossett B, Black JL, McParland B, Burgess JK, Oliver BG. Characterising the mechanism of airway smooth muscle beta2 adrenoceptor desensitization by rhinovirus infected bronchial epithelial cells. PLoS One. 2013;8:e56058.PubMedPubMedCentralCrossRef
51.
Rajan D, Gaston KA, McCracken CE, Erdman DD, Anderson LJ. Response to rhinovirus infection by human airway epithelial cells and peripheral blood mononuclear cells in an in vitro two-chamber tissue culture system. PLoS One. 2013;8:e66600.PubMedPubMedCentralCrossRef
52.
Korpi-Steiner NL, Valkenaar SM, Bates ME, Evans MD, Gern JE, Bertics PJ. Human monocytic cells direct the robust release of CXCL10 by bronchial epithelial cells during rhinovirus infection. Clin Exp Allergy. 2010;40:1203–13.PubMedPubMedCentralCrossRef
53.
Shariff S, Shelfoon C, Holden NS, Traves SL, Wiehler S, Kooi C, Proud D, Leigh R. Human rhinovirus infection of epithelial cells modulates airway smooth muscle migration. Am J Respir Cell Mol Biol. 2017;56:796–803.PubMedCrossRef
54.
Pezzulo AA, Starner TD, Scheetz TE, Traver GL, Tilley AE, Harvey BG, Crystal RG, McCray PB Jr, Zabner J. The air-liquid interface and use of primary cell cultures are important to recapitulate the transcriptional profile of in vivo airway epithelia. Am J Physiol Lung Cell Mol Physiol. 2011;300:L25–31.PubMedCrossRef
55.
Sun Y, Jain D, Koziol-White CJ, Genoyer E, Gilbert M, Tapia K, Panettieri RA Jr, Hodinka RL, Lopez CB. Immunostimulatory defective viral genomes from respiratory syncytial virus promote a strong innate antiviral response during infection in mice and humans. PLoS Pathog. 2015;11:e1005122.PubMedPubMedCentralCrossRef
56.
Avgousti DC, Herrmann C, Kulej K, Pancholi NJ, Sekulic N, Petrescu J, Molden RC, Blumenthal D, Paris AJ, Reyes ED, et al. A core viral protein binds host nucleosomes to sequester immune danger signals. Nature. 2016;535:173–7.PubMedPubMedCentralCrossRef
57.
Kim WK, Jain D, Sanchez MD, Koziol-White CJ, Matthews K, Ge MQ, Haczku A, Panettieri RA Jr, Frieman MB, Lopez CB. Deficiency of melanoma differentiation-associated protein 5 results in exacerbated chronic postviral lung inflammation. Am J Respir Crit Care Med. 2014;189:437–48.PubMedPubMedCentralCrossRef
58.
Ressmeyer AR, Larsson AK, Vollmer E, Dahlen SE, Uhlig S, Martin C. Characterisation of Guinea pig precision-cut lung slices: comparison with human tissues. Eur Respir J. 2006;28:603–11.PubMedCrossRef
59.
Henjakovic M, Martin C, Hoymann HG, Sewald K, Ressmeyer AR, Dassow C, Pohlmann G, Krug N, Uhlig S, Braun A. Ex vivo lung function measurements in precision-cut lung slices (PCLS) from chemical allergen-sensitized mice represent a suitable alternative to in vivo studies. Toxicol Sci. 2008;106:444–53.PubMedCrossRef
60.
Fox J: Utility of the precision cut lung slice model to investigate airway smooth muscle contraction. University of Nottingham, 2011.
61.
Xepapadaki P, Papadopoulos NG, Bossios A, Manoussakis E, Manousakas T, Saxoni-Papageorgiou P. Duration of postviral airway hyperresponsiveness in children with asthma: effect of atopy. J Allergy Clin Immunol. 2005;116:299–304.PubMedCrossRefPubMedCentral
62.
Proud D, Turner RB, Winther B, Wiehler S, Tiesman JP, Reichling TD, Juhlin KD, Fulmer AW, Ho BY, Walanski AA, 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.PubMedCrossRef
63.
Beale J, Jayaraman A, Jackson DJ, Macintyre JDR, Edwards MR, Walton RP, Zhu J, Man Ching Y, Shamji B, Edwards M, et al. Rhinovirus-induced IL-25 in asthma exacerbation drives type 2 immunity and allergic pulmonary inflammation. Sci Transl Med. 2014;6:256ra134.PubMedPubMedCentralCrossRef
64.
Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, Printz MC, Lee WM, Shult PA, Reisdorf E, et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med. 2008;178:667–72.PubMedPubMedCentralCrossRef
65.
66.
67.
Kohrogi H, Graf PD, Sekizawa K, Borson DB, Nadel JA. Neutral endopeptidase inhibitors potentiate substance P- and capsaicin-induced cough in awake Guinea pigs. J Clin Invest. 1988;82:2063–8.PubMedPubMedCentralCrossRef
68.
Katsumata U, Sekizawa K, Inoue H, Sasaki H, Takishima T. Inhibitory actions of procaterol, a beta-2 stimulant, on substance P-induced cough in normal subjects during upper respiratory tract infection. Tohoku J Exp Med. 1989;158:105–6.PubMedCrossRef
69.
Hu C, Wedde-Beer K, Auais A, Rodriguez MM, Piedimonte G. Nerve growth factor and nerve growth factor receptors in respiratory syncytial virus-infected lungs. Am J Physiol Lung Cell Mol Physiol. 2002;283:L494–502.PubMedCrossRef
70.
Piedimonte G, Rodriguez MM, King KA, McLean S, Jiang X. Respiratory syncytial virus upregulates expression of the substance P receptor in rat lungs. Am J Phys. 1999;277:L831–40.
71.
Abdullah H, Heaney LG, Cosby SL, McGarvey LP. Rhinovirus upregulates transient receptor potential channels in a human neuronal cell line: implications for respiratory virus-induced cough reflex sensitivity. Thorax. 2014;69:46–54.PubMedCrossRef
72.
73.
Hakonarson H, Maskeri N, Carter C, Hodinka RL, Campbell D, Grunstein MM. Mechanism of rhinovirus-induced changes in airway smooth muscle responsiveness. J Clin Invest. 1998;102:1732–41.PubMedPubMedCentralCrossRef
74.
75.
Chiba Y, Sakai H, Misawa M. Possible involvement of G(i3) protein in augmented contraction of bronchial smooth muscle from antigen-induced airway hyperresponsive rats. Biochem Pharmacol. 2001;61:921–4.PubMedCrossRef
76.
Hirshman CA, Emala CW. Actin reorganization in airway smooth muscle cells involves Gq and Gi-2 activation of rho. Am J Phys. 1999;277:L653–61.
77.
van Unen J, Reinhard NR, Yin T, Wu YI, Postma M, Gadella TW, Goedhart J. Plasma membrane restricted RhoGEF activity is sufficient for RhoA-mediated actin polymerization. Sci Rep. 2015;5:14693.PubMedPubMedCentralCrossRef
78.
Croxton TL, Lande B, Hirshman CA. Role of G proteins in agonist-induced Ca2+ sensitization of tracheal smooth muscle. Am J Phys. 1998;275:L748–55.CrossRef
79.
Hakonarson H, Carter C, Maskeri N, Hodinka R, Grunstein MM. Rhinovirus-mediated changes in airway smooth muscle responsiveness: induced autocrine role of interleukin-1beta. Am J Phys. 1999;277:L13–21.
80.
Kotaniemi-Syrjanen A, Vainionpaa R, Reijonen TM, Waris M, Korhonen K, Korppi M. Rhinovirus-induced wheezing in infancy--the first sign of childhood asthma? J Allergy Clin Immunol. 2003;111:66–71.PubMedCrossRefPubMedCentral
81.
Anderson HM, Lemanske RF Jr, Evans MD, Gangnon RE, Pappas T, Grindle K, Bochkov YA, Gern JE, Jackson DJ. Assessment of wheezing frequency and viral etiology on childhood and adolescent asthma risk. J Allergy Clin Immunol. 2017;139:692–4.PubMedCrossRef
82.
Guilbert TW, Singh AM, Danov Z, Evans MD, Jackson DJ, Burton R, Roberg KA, Anderson EL, Pappas TE, Gangnon R, et al. Decreased lung function after preschool wheezing rhinovirus illnesses in children at risk to develop asthma. J Allergy Clin Immunol. 2011;128:532–538 e531–510.PubMedPubMedCentralCrossRef
83.
Lemanske RF Jr, Jackson DJ, Gangnon RE, Evans MD, Li Z, Shult PA, Kirk CJ, Reisdorf E, Roberg KA, Anderson EL, et al. Rhinovirus illnesses during infancy predict subsequent childhood wheezing. J Allergy Clin Immunol. 2005;116:571–7.PubMedCrossRef
84.
Rubner FJ, Jackson DJ, Evans MD, Gangnon RE, Tisler CJ, Pappas TE, Gern JE, Lemanske RF Jr. Early life rhinovirus wheezing, allergic sensitization, and asthma risk at adolescence. J Allergy Clin Immunol. 2017;139:501–7.PubMedCrossRef
85.
Kusel MM, de Klerk NH, Kebadze T, Vohma V, Holt PG, Johnston SL, Sly PD. Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J Allergy Clin Immunol. 2007;119:1105–10.CrossRefPubMedPubMedCentral
86.
Liu L, Pan Y, Zhu Y, Song Y, Su X, Yang L, Li M. Association between rhinovirus wheezing illness and the development of childhood asthma: a meta-analysis. BMJ Open. 2017;7:e013034.PubMedPubMedCentralCrossRef
87.
Lukkarinen M, Koistinen A, Turunen R, Lehtinen P, Vuorinen T, Jartti T. Rhinovirus-induced first wheezing episode predicts atopic but not nonatopic asthma at school age. J Allergy Clin Immunol. 2017;140:988–95.PubMedCrossRefPubMedCentral
88.
Jartti T, Kuusipalo H, Vuorinen T, Soderlund-Venermo M, Allander T, Waris M, Hartiala J, Ruuskanen O. Allergic sensitization is associated with rhinovirus-, but not other virus-, induced wheezing in children. Pediatr Allergy Immunol. 2010;21:1008–14.PubMedCrossRefPubMedCentral
89.
Caliskan M, Bochkov YA, Kreiner-Moller E, Bonnelykke K, Stein MM, Du G, Bisgaard H, Jackson DJ, Gern JE, Lemanske RF Jr, et al. Rhinovirus wheezing illness and genetic risk of childhood-onset asthma. N Engl J Med. 2013;368:1398–407.PubMedPubMedCentralCrossRef
90.
Binia A, Khorasani N, Bhavsar PK, Adcock I, Brightling CE, Chung KF, Cookson WO, Moffatt MF. Chromosome 17q21 SNP and severe asthma. J Hum Genet. 2011;56:97–8.PubMedCrossRef
91.
Moffatt MF, Kabesch M, Liang L, Dixon AL, Strachan D, Heath S, Depner M, von Berg A, Bufe A, Rietschel E, et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature. 2007;448:470–3.CrossRefPubMed
92.
Bonnelykke K, Coleman AT, Evans MD, Thorsen J, Waage J, Vissing NH, Carlsson CJ, Stokholm J, Chawes BL, Jessen LE, et al. Cadherin-related family member 3 genetics and rhinovirus C respiratory illnesses. Am J Respir Crit Care Med. 2018;197:589–94.PubMedCrossRefPubMedCentral
93.
94.
Marin J, Jeler-Kacar D, Levstek V, Macek V. Persistence of viruses in upper respiratory tract of children with asthma. J Inf Secur. 2000;41:69–72.
95.
Corne JM, Marshall C, Smith S, Schreiber J, Sanderson G, Holgate ST, Johnston SL. Frequency, severity, and duration of rhinovirus infections in asthmatic and non-asthmatic individuals: a longitudinal cohort study. Lancet. 2002;359:831–4.PubMedCrossRef
96.
Schneider D, Ganesan S, Comstock AT, Meldrum CA, Mahidhara R, Goldsmith AM, Curtis JL, Martinez FJ, Hershenson MB, Sajjan U. Increased cytokine response of rhinovirus-infected airway epithelial cells in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2010;182:332–40.PubMedPubMedCentralCrossRef
97.
Wark PA, Johnston SL, Bucchieri F, Powell R, Puddicombe S, Laza-Stanca V, Holgate ST, Davies DE. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J Exp Med. 2005;201:937–47.PubMedPubMedCentralCrossRef
98.
Message SD, Laza-Stanca V, Mallia P, Parker HL, Zhu J, Kebadze T, Contoli M, Sanderson G, Kon OM, Papi A, 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 U S A. 2008;105:13562–7.PubMedPubMedCentralCrossRef
99.
Sykes A, Edwards MR, Macintyre J, del Rosario A, Bakhsoliani E, Trujillo-Torralbo MB, Kon OM, Mallia P, McHale M, Johnston SL. 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 e1506.PubMedCrossRef
100.
Arroyave WD, Rabito FA, Carlson JC, Sever ML, Lefante J. Asthma severity, not asthma control, is worse in atopic compared with nonatopic adolescents with asthma. Ann Allergy Asthma Immunol. 2016;116:18–25.PubMedCrossRef
101.
Carroll WD, Lenney W, Child F, Strange RC, Jones PW, Whyte MK, Primhak RA, Fryer AA. Asthma severity and atopy: how clear is the relationship? Arch Dis Child. 2006;91:405–9.PubMedPubMedCentralCrossRef
102.
Sarria EE, Mattiello R, Yao W, Chakr V, Tiller CJ, Kisling J, Tabbey R, Yu Z, Kaplan MH, Tepper RS. Atopy, cytokine production, and airway reactivity as predictors of pre-school asthma and airway responsiveness. Pediatr Pulmonol. 2014;49:132–9.PubMedCrossRef
103.
Baraldo S, Contoli M, Bazzan E, Turato G, Padovani A, Marku B, Calabrese F, Caramori G, Ballarin A, Snijders D, et al. Deficient antiviral immune responses in childhood: distinct roles of atopy and asthma. J Allergy Clin Immunol. 2012;130:1307–14.PubMedCrossRef
104.
Pritchard AL, White OJ, Burel JG, Carroll ML, Phipps S, Upham JW. Asthma is associated with multiple alterations in anti-viral innate signalling pathways. PLoS One. 2014;9:e106501.PubMedPubMedCentralCrossRef
105.
Miller EK, Hernandez JZ, Wimmenauer V, Shepherd BE, Hijano D, Libster R, Serra ME, Bhat N, Batalle JP, Mohamed Y, 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.PubMedPubMedCentralCrossRef
106.
Gern JE, Calhoun W, Swenson C, Shen G, Busse WW. Rhinovirus infection preferentially increases lower airway responsiveness in allergic subjects. Am J Respir Crit Care Med. 1997;155:1872–6.PubMedCrossRef
107.
Green RM, Custovic A, Sanderson G, Hunter J, Johnston SL, Woodcock A. Synergism between allergens and viruses and risk of hospital admission with asthma: case-control study. BMJ. 2002;324:763.PubMedPubMedCentralCrossRef
108.
de Kluijver J, Evertse CE, Sont JK, Schrumpf JA, van Zeijl-van der Ham CJ, Dick CR, Rabe KF, Hiemstra PS, Sterk PJ. Are rhinovirus-induced airway responses in asthma aggravated by chronic allergen exposure? Am J Respir Crit Care Med. 2003;168:1174–80.PubMedCrossRef
109.
DeMore JP, Weisshaar EH, Vrtis RF, Swenson CA, Evans MD, Morin A, Hazel E, Bork JA, Kakumanu S, Sorkness R, et al. Similar colds in subjects with allergic asthma and nonatopic subjects after inoculation with rhinovirus-16. J Allergy Clin Immunol. 2009;124:245–52 252 e241–243.PubMedPubMedCentralCrossRef
110.
Silkoff PE, Flavin S, Gordon R, Loza MJ, Sterk PJ, Lutter R, Diamant Z, Turner RB, Lipworth BJ, Proud D, et al. Toll-like receptor 3 blockade in rhinovirus-induced experimental asthma exacerbations: a randomized controlled study. J Allergy Clin Immunol. 2018;141:1220–30.PubMedCrossRef
111.
Grunberg K, Sharon RF, Hiltermann TJ, Brahim JJ, Dick EC, Sterk PJ, Van Krieken JH. Experimental rhinovirus 16 infection increases intercellular adhesion molecule-1 expression in bronchial epithelium of asthmatics regardless of inhaled steroid treatment. Clin Exp Allergy. 2000;30:1015–23.PubMedCrossRef
112.
Grunberg K, Sharon RF, Sont JK, In't Veen JC, Van Schadewijk WA, De Klerk EP, Dick CR, Van Krieken JH, Sterk PJ. Rhinovirus-induced airway inflammation in asthma: effect of treatment with inhaled corticosteroids before and during experimental infection. Am J Respir Crit Care Med. 2001;164:1816–22.PubMedCrossRef
113.
Eddleston J, Lee RU, Doerner AM, Herschbach J, Zuraw BL. Cigarette smoke decreases innate responses of epithelial cells to rhinovirus infection. Am J Respir Cell Mol Biol. 2011;44:118–26.PubMedCrossRef
114.
Logan J, Chen L, Gangell C, Sly PD, Fantino E, Liu K. Brief exposure to cigarette smoke impairs airway epithelial cell innate anti-viral defence. Toxicol in Vitro. 2014;28:1430–5.PubMedCrossRef
115.
Hudy MH, Traves SL, Wiehler S, Proud D. Cigarette smoke modulates rhinovirus-induced airway epithelial cell chemokine production. Eur Respir J. 2010;35:1256–63.PubMedCrossRef
116.
Proud D, Hudy MH, Wiehler S, Zaheer RS, Amin MA, Pelikan JB, Tacon CE, Tonsaker TO, Walker BL, Kooi C, et al. Cigarette smoke modulates expression of human rhinovirus-induced airway epithelial host defense genes. PLoS One. 2012;7:e40762.PubMedPubMedCentralCrossRef
117.
Hudy MH, Proud D. Cigarette smoke enhances human rhinovirus-induced CXCL8 production via HuR-mediated mRNA stabilization in human airway epithelial cells. Respir Res. 2013;14:88.PubMedPubMedCentralCrossRef
118.
Capistrano SJ, Zakarya R, Chen H, Oliver BG. Biomass smoke exposure enhances rhinovirus-induced inflammation in primary lung fibroblasts. Int J Mol Sci. 2016;17.PubMedCentralCrossRef
119.
Spannhake EW, Reddy SP, Jacoby DB, Yu XY, Saatian B, Tian J. Synergism between rhinovirus infection and oxidant pollutant exposure enhances airway epithelial cell cytokine production. Environ Health Perspect. 2002;110:665–70.PubMedPubMedCentralCrossRef
120.
Henderson FW, Dubovi EJ, Harder S, Seal E Jr, Graham D. Experimental rhinovirus infection in human volunteers exposed to ozone. Am Rev Respir Dis. 1988;137:1124–8.PubMedCrossRef
121.
Vempilly J, Abejie B, Diep V, Gushiken M, Rawat M, Tyner TR. The synergetic effect of ambient PM2.5 exposure and rhinovirus infection in airway dysfunction in asthma: a pilot observational study from the Central Valley of California. Exp Lung Res. 2013;39:434–40.PubMedCrossRef
122.
Ito T, Okumura H, Tsukue N, Kobayashi T, Honda K, Sekizawa K. Effect of diesel exhaust particles on mRNA expression of viral and bacterial receptors in rat lung epithelial L2 cells. Toxicol Lett. 2006;165:66–70.PubMedCrossRef
Metadata
Title
Modulation of airway hyperresponsiveness by rhinovirus exposure
Authors
Dennis Lo
Joshua L. Kennedy
Richard C. Kurten
Reynold A. Panettieri Jr
Cynthia J. Koziol-White
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2018
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-018-0914-9

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