Targeting intercellular adhesion molecule-1 (ICAM-1) to reduce rhinovirus-induced acute exacerbations in chronic respiratory diseases.
Acute exacerbations
Airway epithelium
Asthma
COPD
ICAM-1
Respiratory infections
Journal
Inflammopharmacology
ISSN: 1568-5608
Titre abrégé: Inflammopharmacology
Pays: Switzerland
ID NLM: 9112626
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
16
06
2021
accepted:
24
02
2022
pubmed:
23
3
2022
medline:
31
5
2022
entrez:
22
3
2022
Statut:
ppublish
Résumé
The chronic respiratory non-communicable diseases, asthma and chronic obstructive pulmonary disease (COPD) are among the leading causes of global mortality and morbidity. Individuals suffering from these diseases are particularly susceptible to respiratory infections caused by bacterial and/or viral pathogens, which frequently result in exacerbation of symptoms, lung function decline, frequent hospital emergency visits and increased socioeconomic burden. Human rhinoviruses (HRV) remain the major viral pathogen group implicated in exacerbations of both asthma and COPD. The rhinoviral entry into the host lung epithelium is facilitated primarily by the adhesion site ("receptor") intercellular adhesion molecule-1 (ICAM-1), coincidentally expressed on the respiratory epithelium in these conditions. Multiple observations of increased airway ICAM-1 protein in asthmatics, smokers and smoking-related COPD have been recorded in the literature. However, the lack of robust therapies for COPD in particular has triggered a renewed interest in assessing receptor antagonism-based anti-viral strategies for treatment of intercurrent viral infections in those with pre-existing chronic lung diseases. Given the crucial role ICAM-1 plays in facilitating HRV adhesion and, thus, transmissibility to the host respiratory system, as well as the up-regulation of ICAM-1 by smoking, we summarize the role of HRV in smoking-induced COPD and especially highlight the role of ICAM-1 in epithelial viral adhesion and chronic lung disease progression. Further, the review also sheds light specifically on evolving precision therapeutic strategies in blocking ICAM-1 for preventing viral adhesion and exacerbations of COPD.
Identifiants
pubmed: 35316427
doi: 10.1007/s10787-022-00968-2
pii: 10.1007/s10787-022-00968-2
pmc: PMC8938636
doi:
Substances chimiques
Intercellular Adhesion Molecule-1
126547-89-5
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
725-735Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2022. The Author(s).
Références
Bai J, Smock SL, Jackson GR Jr, MacIsaac KD, Huang Y, Mankus C, Oldach J, Roberts B, Ma YL, Klappenbach JA, Crackower MA, Alves SE, Hayden PJ (2015) Phenotypic responses of differentiated asthmatic human airway epithelial cultures to rhinovirus. PLoS ONE 10(2):e0118286
pubmed: 25706956
pmcid: 4338293
Bentley AM, Durham SR, Robinson DS, Menz G, Storz C, Cromwell O, Kay AB, Wardlaw AJ (1993) Expression of endothelial and leukocyte adhesion molecules interacellular adhesion molecule-1, E-selectin, and vascular cell adhesion molecule-1 in the bronchial mucosa in steady-state and allergen-induced asthma. J Allergy Clin Immunol 92(6):857–868
pubmed: 7505008
Bhalla K, Chugh M, Mehrotra S, Rathore S, Tousif S, Prakash Dwivedi V, Prakash P, Kumar Samuchiwal S, Kumar S, Kumar Singh D, Ghanwat S, Kumar D, Das G, Mohmmed A, Malhotra P, Ranganathan A (2015) Host ICAMs play a role in cell invasion by Mycobacterium tuberculosis and Plasmodium falciparum. Nat Commun 6:6049
pubmed: 25586702
Bochkov YA, Gern JE (2016) Rhinoviruses and their receptors: implications for allergic disease. Curr Allergy Asthma Rep 16(4):30
pubmed: 26960297
pmcid: 4854667
Bochkov YA, Watters K, Ashraf S, Griggs TF, Devries MK, Jackson DJ, Palmenberg AC, Gern JE (2015) Cadherin-related family member 3, a childhood asthma susceptibility gene product, mediates rhinovirus C binding and replication. Proc Natl Acad Sci USA 112(17):5485–5490
pubmed: 25848009
pmcid: 4418890
Chan SCH, Shum DKY, Tipoe GL, Mak JCW, Leung ETM, Ip MSM (2008) Upregulation of ICAM-1 expression in bronchial epithelial cells by airway secretions in bronchiectasis. Respir Med 102(2):287–298
pubmed: 17931847
Chihara J, Yamamoto T, Kurachi D, Kakazu T, Higashimoto I, Nakajima S (1995) Possible release of eosinophil granule proteins in response to signaling from intercellular adhesion molecule-1 and its ligands. Int Arch Allergy Immunol 108(Suppl 1):52–54
pubmed: 7549525
Ciprandi G, Pronzato C, Ricca V, Passalacqua G, Bagnasco M, Canonica GW (1994) Allergen-specific challenge induces intercellular adhesion molecule 1 (ICAM-1 or CD54) on nasal epithelial cells in allergic subjects. Relationships with early and late inflammatory phenomena. Am J Respir Crit Care Med 150(6 Pt 1):1653–1659
pubmed: 7524984
Colonno RJ (1992) Virus receptors: the achilles’ heel of human rhinoviruses. In: Block TM, Jungkind D, Crowell RL, Denison M, Walsh LR (eds) Innovations in antiviral development and the detection of virus infections. Springer US, Boston, pp 61–70
Cox DW, Bizzintino J, Ferrari G, Khoo SK, Zhang G, Whelan S, Lee WM, Bochkov YA, Geelhoed GC, Goldblatt J, Gern JE, Laing IA, Le Souëf PN (2013) 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 188(11):1358–1364
pubmed: 23992536
pmcid: 5447292
de Pablo R, Monserrat J, Reyes E, Díaz D, Rodríguez-Zapata M, de la Hera A, Prieto A, Álvarez-Mon M (2013) Circulating sICAM-1 and sE-Selectin as biomarker of infection and prognosis in patients with systemic inflammatory response syndrome. Eur J Intern Med 24(2):132–138
pubmed: 23352000
Drake MG, Lebold KM, Roth-Carter QR, Pincus AB, Blum ED, Proskocil BJ, Jacoby DB, Fryer AD, Nie Z (2018) Eosinophil and airway nerve interactions in asthma. J Leukoc Biol 104(1):61–67
pubmed: 29633324
Engels R, Falk L, Albanese M, Keppler OT, Sewald X (2022) LFA1 and ICAM1 are critical for fusion and spread of murine leukemia virus in vivo. Cell Rep 38(3):110279
pubmed: 35045303
Finney L, Belchamber K, Kemp S, Donaldson G, Mallia P, Johnston S, Wedzicha J (2017) P56 Human rhinovirus impairs phagocytosis of haemophilus influenzae in alveolar macrophages in chronic obstructive pulmonary disease. Thorax 72(Suppl 3):A112–A112
Galanter J, Choudhry S, Eng C, Nazario S, Rodríguez-Santana JR, Casal J, Torres-Palacios A, Salas J, Chapela R, Watson HG, Meade K, LeNoir M, Rodríguez-Cintrón W, Avila PC, Burchard EG (2008) ORMDL3 gene is associated with asthma in three ethnically diverse populations. Am J Respir Crit Care Med 177(11):1194–1200
pubmed: 18310477
pmcid: 2408437
George SN, Garcha DS, Mackay AJ, Patel AR, Singh R, Sapsford RJ, Donaldson GC, Wedzicha JA (2014) Human rhinovirus infection during naturally occurring COPD exacerbations. Eur Respir J 44(1):87–96
pubmed: 24627537
Global Strategy for the Diagnosis M. a. P. o. C (2015) Global initiative for chronic obstructive lung disease (GOLD). News & events from around the world
Gorska-Ciebiada M, Ciebiada M, Gorska MM, Gorski P, Grzelewska-Rzymowska I (2006) Intercellular adhesion molecule 1 and tumor necrosis factor alpha in asthma and persistent allergic rhinitis: relationship with disease severity. Ann Allergy Asthma Immunol 97(1):66–72
pubmed: 16892784
Greve JM, Davis G, Meyer AM, Forte CP, Yost SC, Marlor CW, Kamarck ME, McClelland A (1989) The major human rhinovirus receptor is ICAM-1. Cell 56(5):839–847
pubmed: 2538243
Hayden FG (2004) Rhinovirus and the lower respiratory tract. Rev Med Virol 14(1):17–31
pubmed: 14716689
pmcid: 7169234
Hayden FG, Gwaltney JM Jr, Colonno RJ (1988) Modification of experimental rhinovirus colds by receptor blockade. Antivir Res 9(4):233–247
pubmed: 2849376
Hubbard AK, Rothlein R (2000) Intercellular adhesion molecule-1 (ICAM-1) expression and cell signaling cascades. Free Radic Biol Med 28(9):1379–1386
pubmed: 10924857
Jahnke A, Van de Stolpe A, Caldenhoven E, Johnson JP (1995) Constitutive expression of human intercellular adhesion molecule-1 (ICAM-1) is regulated by differentially active enhancing and silencing elements. Eur J Biochem 228(2):439–446
pubmed: 7705360
Johnston NW, Johnston SL, Duncan JM, Greene JM, Kebadze T, Keith PK, Roy M, Waserman S, Sears MR (2005) The September epidemic of asthma exacerbations in children: a search for etiology. J Allergy Clin Immunol 115(1):132–138
pubmed: 15637559
Johnston NW, Olsson M, Edsbacker S, Gerhardsson de Verdier M, Gustafson P, McCrae C, Coyle PV, McIvor RA (2017) Colds as predictors of the onset and severity of COPD exacerbations. Int J Chron Obstruct Pulmon Dis 12:839–848
pubmed: 28331305
pmcid: 5354536
Kherad O, Kaiser L, Bridevaux PO, Sarasin F, Thomas Y, Janssens JP, Rutschmann OT (2010) Upper-respiratory viral infection, biomarkers, and COPD exacerbations. Chest 138(4):896–904
pubmed: 20435659
Kim J, Jung YK, Kim C, Shin JS, Scheers E, Lee JY, Han SB, Lee CK, Neyts J, Ha JD, Jung YS (2017) A novel series of highly potent small molecule inhibitors of rhinovirus replication. J Med Chem 60(13):5472–5492
pubmed: 28581749
Kim J, Shin JS, Ahn S, Han SB, Jung YS (2018) 3-Aryl-1,2,4-oxadiazole derivatives active against human rhinovirus. ACS Med Chem Lett 9(7):667–672
pubmed: 30034598
pmcid: 6047043
Ko FW, Chan PK, Chan RWY, Chan KP, Ip A, Kwok A, Ngai JC, Ng SS, On CT, Hui DS (2019) Molecular detection of respiratory pathogens and typing of human rhinovirus of adults hospitalized for exacerbation of asthma and chronic obstructive pulmonary disease. Respir Res 20(1):210
pubmed: 31519188
pmcid: 6743175
Kuroda M, Niwa S, Sekizuka T, Tsukagoshi H, Yokoyama M, Ryo A, Sato H, Kiyota N, Noda M, Kozawa K, Shirabe K, Kusaka T, Shimojo N, Hasegawa S, Sugai K, Obuchi M, Tashiro M, Oishi K, Ishii H, Kimura H (2015) Molecular evolution of the VP1, VP2, and VP3 genes in human rhinovirus species C. Sci Rep 5:1–10
Ledford RM, Patel NR, Demenczuk TM, Watanyar A, Herbertz T, Collett MS, Pevear DC (2004) VP1 sequencing of all human rhinovirus serotypes: insights into genus phylogeny and susceptibility to antiviral capsid-binding compounds. J Virol 78(7):3663–3674
pubmed: 15016887
pmcid: 371056
Lehmann JCU, Jablonski-Westrich D, Haubold U, Gutierrez-Ramos J-C, Springer T, Hamann A (2003) Overlapping and selective roles of endothelial intercellular adhesion molecule-1 (ICAM-1) and ICAM-2 in lymphocyte trafficking. J Immunol 171(5):2588–2593
pubmed: 12928410
Lin SJ, Chang LY, Yan DC, Huang YJ, Lin TJ, Lin TY (2003) Decreased intercellular adhesion molecule-1 (CD54) and L-selectin (CD62L) expression on peripheral blood natural killer cells in asthmatic children with acute exacerbation. Allergy 58(1):67–71
pubmed: 12580810
Liu Y, Bochkov YA, Eickhoff JC, Hu T, Zumwalde NA, Tan JW, Lopez C, Fichtinger PS, Reddy TR, Overmyer KA, Gumperz JE, Coon J, Mathur SK, Gern JE, Smith JA (2020) Orosomucoid-like 3 supports rhinovirus replication in human epithelial cells. Am J Respir Cell Mol Biol 62(6):783–792
pubmed: 32078788
pmcid: 7258826
Lopez-Campos JL, Calero C, Arellano-Orden E, Marquez-Martin E, Cejudo-Ramos P, Ortega Ruiz F, Montes-Worboys A (2012) Increased levels of soluble ICAM-1 in chronic obstructive pulmonary disease and resistant smokers are related to active smoking. Biomark Med 6(6):805–811
pubmed: 23227846
Mallia P, Message SD, Gielen V, Contoli M, Gray K, Kebadze T, Aniscenko J, Laza-Stanca V, Edwards MR, Slater L, Papi A, Stanciu LA, Kon OM, Johnson M, Johnston SL (2011) Experimental rhinovirus infection as a human model of chronic obstructive pulmonary disease exacerbation. Am J Respir Crit Care Med 183(6):734–742
pubmed: 20889904
Malmstrom K, Pitkaranta A, Carpen O, Pelkonen A, Malmberg LP, Turpeinen M, Kajosaari M, Sarna S, Lindahl H, Haahtela T, Makela MJ (2006) Human rhinovirus in bronchial epithelium of infants with recurrent respiratory symptoms. J Allergy Clin Immunol 118(3):591–596
pubmed: 16950276
Marlin SD, Staunton DE, Springer TA, Stratowa C, Sommergruber W, Merluzzi VJ (1990) A soluble form of intercellular adhesion molecule-1 inhibits rhinovirus infection. Nature 344(6261):70–72
pubmed: 1968231
McIntyre CL, Savolainen-Kopra C, Hovi T, Simmonds P (2013) Recombination in the evolution of human rhinovirus genomes. Arch Virol 158(7):1497–1515
pubmed: 23443931
Mendez MP, Monroy YK, Du M, Preston AM, Tolle L, Lin Y, VanDussen KL, Samuelson LC, Standiford TJ, Curtis JL, Beck JM, Christensen PJ, Paine R 3rd (2011) Overexpression of sICAM-1 in the alveolar epithelial space results in an exaggerated inflammatory response and early death in Gram negative pneumonia. Respir Res 12(1):12
pubmed: 21247482
pmcid: 3034680
Miller M, Tam AB, Cho JY, Doherty TA, Pham A, Khorram N, Rosenthal P, Mueller JL, Hoffman HM, Suzukawa M, Niwa M, Broide DH (2012) ORMDL3 is an inducible lung epithelial gene regulating metalloproteases, chemokines, OAS, and ATF6. Proc Natl Acad Sci USA 109(41):16648–16653
pubmed: 23011799
pmcid: 3478632
Mosser AG, Vrtis R, Burchell L, Lee WM, Dick CR, Weisshaar E, Bock D, Swenson CA, Cornwell RD, Meyer KC, Jarjour NN, Busse WW, Gern JE (2005) Quantitative and qualitative analysis of rhinovirus infection in bronchial tissues. Am J Respir Crit Care Med 171(6):645–651
pubmed: 15591468
Novotny LA, Bakaletz LO (2016) Intercellular adhesion molecule 1 serves as a primary cognate receptor for the Type IV pilus of nontypeable Haemophilus influenzae. Cell Microbiol 18(8):1043–1055
pubmed: 26857242
pmcid: 4959963
Othumpangat S, Noti JD, McMillen CM, Beezhold DH (2016) ICAM-1 regulates the survival of influenza virus in lung epithelial cells during the early stages of infection. Virology 487:85–94
pubmed: 26499045
Palmenberg AC, Rathe JA, Liggett SB (2010) Analysis of the complete genome sequences of human rhinovirus. J Allergy Clin Immunol 125(6):1190–1199 (quiz 1191–1200)
pubmed: 20471068
pmcid: 2893015
Pang B, Hong W, West-Barnette SL, Kock ND, Swords WE (2008) Diminished ICAM-1 expression and impaired pulmonary clearance of nontypeable Haemophilus influenzae in a mouse model of chronic obstructive pulmonary disease/emphysema. Infect Immun 76(11):4959–4967
pubmed: 18794286
pmcid: 2573371
Papi A, Johnston SL (1999) Rhinovirus infection induces expression of its own receptor intercellular adhesion molecule 1 (ICAM-1) via increased NF-kappaB-mediated transcription. J Biol Chem 274(14):9707–9720
pubmed: 10092659
Papi A, Brightling C, Pedersen SE, Reddel HK (2018) Asthma. Lancet (london, England) 391(10122):783–800
Patick AK, Brothers MA, Maldonado F, Binford S, Maldonado O, Fuhrman S, Petersen A, Smith GJ 3rd, Zalman LS, Burns-Naas LA, Tran JQ (2005) In vitro antiviral activity and single-dose pharmacokinetics in humans of a novel, orally bioavailable inhibitor of human rhinovirus 3C protease. Antimicrob Agents Chemother 49(6):2267–2275
pubmed: 15917520
pmcid: 1140523
Quint JK, Donaldson GC, Goldring JJ, Baghai-Ravary R, Hurst JR, Wedzicha JA (2010) Serum IP-10 as a biomarker of human rhinovirus infection at exacerbation of COPD. Chest 137(4):812–822
pubmed: 19837822
Qureshi H, Sharafkhaneh A, Hanania NA (2014) Chronic obstructive pulmonary disease exacerbations: latest evidence and clinical implications. Ther Adv Chronic Dis 5(5):212–227
pubmed: 25177479
pmcid: 4131503
Roebuck KA, Finnegan A (1999) Regulation of intercellular adhesion molecule-1 (CD54) gene expression. J Leukoc Biol 66(6):876–888
pubmed: 10614768
Rohde G, Wiethege A, Borg I, Kauth M, Bauer T, Gillissen A, Bufe A, Schultze-Werningh G (2003) Respiratory viruses in exacerbations of chronic obstructive pulmonary disease requiring hospitalisation: a case-control study. Thorax 58(1):37–42
pubmed: 12511718
pmcid: 1746460
Rusznak C, Mills PR, Devalia JL, Sapsford RJ, Davies RJ, Lozewicz S (2000) Effect of cigarette smoke on the permeability and IL-1beta and sICAM-1 release from cultured human bronchial epithelial cells of never-smokers, smokers, and patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 23(4):530–536
pubmed: 11017919
Schroth MK, Grimm E, Frindt P, Galagan DM, Konno SI, Love R, Gern JE (1999) Rhinovirus replication causes RANTES production in primary bronchial epithelial cells. Am J Respir Cell Mol Biol 20(6):1220–1228
pubmed: 10340941
Seemungal TA, Donaldson GC, Bhowmik A, Jeffries DJ, Wedzicha JA (2000) Time course and recovery of exacerbations in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 161(5):1608–1613
pubmed: 10806163
Seemungal T, Harper-Owen R, Bhowmik A, Moric I, Sanderson G, Message S, Maccallum P, Meade TW, Jeffries DJ, Johnston SL, Wedzicha JA (2001) Respiratory viruses, symptoms, and inflammatory markers in acute exacerbations and stable chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164(9):1618–1623
pubmed: 11719299
Sethi S, Murphy TF (2008) Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N Engl J Med 359(22):2355–2365
pubmed: 19038881
Shukla SD, Hansbro PM, Walters EH (2017a) Blocking rhinoviral adhesion molecule (ICAM-1): potential to prevent COPD exacerbations. Int J Chron Obstruct Pulmon Dis 12:1413–1414
pubmed: 28546749
pmcid: 5436784
Shukla SD, Mahmood MQ, Weston S, Latham R, Muller HK, Sohal SS, Walters EH (2017b) The main rhinovirus respiratory tract adhesion site (ICAM-1) is upregulated in smokers and patients with chronic airflow limitation (CAL). Respir Res 18(1):6
pubmed: 28056984
pmcid: 5217320
Springer TA (1990) Adhesion receptors of the immune system. Nature 346(6283):425–434
pubmed: 1974032
Stanciu LA, Djukanovic R (1998) The role of ICAM-1 on T-cells in the pathogenesis of asthma. Eur Respir J 11(4):949–957
pubmed: 9623703
Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD, Springer TA (1989) A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56(5):849–853
pubmed: 2538244
Sykes A, Mallia P, Johnston SL (2007) Diagnosis of pathogens in exacerbations of chronic obstructive pulmonary disease. Proc Am Thorac Soc 4(8):642–646
pubmed: 18073396
Takizawa H, Tanaka M, Takami K, Ohtoshi T, Ito K, Satoh M, Okada Y, Yamasawa F, Umeda A (2000) Increased expression of inflammatory mediators in small-airway epithelium from tobacco smokers. Am J Physiol Lung Cell Mol Physiol 278(5):L906-913
pubmed: 10781420
Taylor S, Lopez P, Weckx L, Borja-Tabora C, Ulloa-Gutierrez R, Lazcano-Ponce E, Kerdpanich A, Weber MAR, de Los Santos AM, Tinoco JC, Safadi MA, Lim FS, de Mezerville MH, Faingezicht I, Cruz-Valdez A, Feng Y, Li P, Durviaux S, Haars G, Roy-Ghanta S, Vaughn DW, Nolan T (2017) Respiratory viruses and influenza-like illness: epidemiology and outcomes in children aged 6 months to 10 years in a multi-country population sample. J Infect 74(1):29–41
pubmed: 27667752
Terajima M, Yamaya M, Sekizawa K, Okinaga S, Suzuki T, Yamada N, Nakayama K, Ohrui T, Oshima T, Numazaki Y, Sasaki H (1997) Rhinovirus infection of primary cultures of human tracheal epithelium: role of ICAM-1 and IL-1beta. Am J Physiol 273(4 Pt 1):L749-759
pubmed: 9357849
Traub S, Nikonova A, Carruthers A, Dunmore R, Vousden KA, Gogsadze L, Hao W, Zhu Q, Bernard K, Zhu J, Dymond M, McLean GR, Walton RP, Glanville N, Humbles A, Khaitov M, Wells T, Kolbeck R, Leishman AJ, Sleeman MA, Bartlett NW, Johnston SL (2013) An anti-human ICAM-1 antibody inhibits rhinovirus-induced exacerbations of lung inflammation. PLoS Pathog 9(8):e1003520
pubmed: 23935498
pmcid: 3731244
Turner RB, Wecker MT, Pohl G, Witek TJ, McNally E, St R, George BW, Hayden FG (1999) Efficacy of tremacamra, a soluble intercellular adhesion molecule 1, for experimental rhinovirus infectiona randomized clinical trial. JAMA 281(19):1797–1804
pubmed: 10340366
van de Stolpe A, van der Saag PT (1996) Intercellular adhesion molecule-1. J Mol Med (berl) 74(1):13–33
Wedzicha JA (2004) Role of viruses in exacerbations of chronic obstructive pulmonary disease. Proc Am Thorac Soc 1(2):115–120
pubmed: 16113423
Wegner CD, Gundel RH, Reilly P, Haynes N, Letts LG, Rothlein R (1990) Intercellular adhesion molecule-1 (ICAM-1) in the pathogenesis of asthma. Science 247(4941):456–459
pubmed: 1967851
WHO (2014) The top 10 causes of death
Winther B (2011) Rhinovirus infections in the upper airway. Proc Am Thorac Soc 8(1):79–89
pubmed: 21364225
Winther B, Brofeldt S, Christensen B, Mygind N (1984) Light and scanning electron microscopy of nasal biopsy material from patients with naturally acquired common colds. Acta Otolaryngol 97(3–4):309–318
pubmed: 6720308
Wos M, Sanak M, Soja J, Olechnowicz H, Busse WW, Szczeklik A (2008) The presence of rhinovirus in lower airways of patients with bronchial asthma. Am J Respir Crit Care Med 177(10):1082–1089
pubmed: 18276945
pmcid: 2383991
Zhang Y, Willis-Owen SAG, Spiegel S, Lloyd CM, Moffatt MF, Cookson W (2019) The ORMDL3 asthma gene regulates ICAM1 and has multiple effects on cellular inflammation. Am J Respir Crit Care Med 199(4):478–488
pubmed: 30339462
pmcid: 6376621