Rhinovirus C targets ciliated airway epithelial cells

Respiratory Research

Volumn 18, Issue 1, 2017, Pages

  Griggs, Theodor F ^a,b,c   Bochkov, Yury A ^a   Basnet, Sarmila ^a   Pasic, Thomas R ^a   Brockman Schneider, Rebecca A ^a   Palmenberg, Ann C ^d   Gern, James E ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b Molecular and Cellular Pharmacology Program   (United States)

^c Medical Scientist Training Program   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Air liquid interface; Bronchial epithelium; CDHR3; Ciliated cells; Rhinovirus C

Indexed keywords

ALPHA TUBULIN; CADHERIN; CADHERIN RELATED FAMILY MEMBER 3; UNCLASSIFIED DRUG;

AIRWAY EPITHELIUM CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL SPECIFICITY; CELL STRUCTURE; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE SEVERITY; GOBLET CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NONHUMAN; PROTEIN EXPRESSION; RHINOVIRUS; RHINOVIRUS C; RHINOVIRUS INFECTION; STAINING; VIRUS ATTACHMENT; VIRUS REPLICATION; VIRUS SHEDDING; BRONCHUS; CILIUM; CYTOLOGY; ENTEROVIRUS; EPITHELIUM CELL; PHYSIOLOGY; ULTRASTRUCTURE; VIROLOGY; VIRUS ENTRY;

BRONCHI; CELLS, CULTURED; CILIA; ENTEROVIRUS; EPITHELIAL CELLS; HUMANS; VIRUS INTERNALIZATION; VIRUS REPLICATION; VIRUS SHEDDING;

EID: 85018793729     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/s12931-017-0567-0     Document Type: Article

References (57)

1. Fendrick AM, Monto AS, Nightengale B, Sarnes M. The economic burden of non-influenza-related viral respiratory tract infection in the United States. Arch Intern Med. 2003;163(4):487-94.
2. Jakab GJ. Mechanisms of bacterial superinfections in viral pneumonias. Schweiz Med Wochenschr. 1985;115(3):75-86.
3. Monto AS, Bryan ER, Ohmit S. Rhinovirus infections in Tecumseh, Michigan: frequency of illness and number of serotypes. J Infect Dis. 1987;156(1):43-9.
4. Hament J-M, Kimpen JL, Fleer A, Wolfs TF. Respiratory viral infection predisposing for bacterial disease: a concise review. FEMS Immunol Med Microbiol. 1999;26(3-4):189-95.
5. Ishizuka S, Yamaya M, Suzuki T, Takahashi H, Ida S, Sasaki T, et al. Effects of rhinovirus infection on the adherence of Streptococcus pneumoniae to cultured human airway epithelial cells. J Infect Dis. 2003;188(12):1928-39.
6. Monto AS. Epidemiology of viral respiratory infections. Dis Mon. 2003;49(3):160-74.
7. Bosch AATM, Biesbroek G, Trzcinski K, Sanders EAM, Bogaert D. Viral and Bacterial Interactions in the Upper Respiratory Tract. PLoS Pathog. 2013;9(1), e1003057.
8. Johnston SL, Pattemore PK, Sanderson G, Smith S, Lampe F, Josephs L, et al. Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. BMJ. 1995;310(6989):1225-9.
9. Friedlander SL, Busse WW. The role of rhinovirus in asthma exacerbations. J Allergy Clin Immunol. 2005;116(2):267-73.
10. Miller EK, Lu X, Erdman DD, Poehling KA, Zhu Y, Griffin MR, et al. Rhinovirus-associated hospitalizations in young children. J Infect Dis. 2007;195(6):773-81.
11. Brownlee JW, Turner RB. New developments in the epidemiology and clinical spectrum of rhinovirus infections. Curr Opin Pediatr. 2008;20(1):67-71.
12. Peltola V, Waris M, Osterback R, Susi P, Ruuskanen O, Hyypiä T. Rhinovirus transmission within families with children: incidence of symptomatic and asymptomatic infections. J Infect Dis. 2008;197(3):382-9.
13. Gern JE. The ABCs of rhinoviruses, wheezing, and asthma. J Virol. 2010;84(15):7418-26.
14. Cox DW, Bizzintino J, Ferrari G, Khoo SK, Zhang G, Whelan S, et al. Human rhinovirus species C infection in young children with acute wheeze is associated with increased acute respiratory hospital admissions. Am J Respir Crit Care Med. 2013;188(11):1358-64.
15. Gern JE, Busse WW. Relationship of viral infections to wheezing illnesses and asthma. Nat Rev Immunol. 2002;2(2):132-8.
16. Lemanske Jr RF, Jackson DJ, Gangnon RE, Evans MD, Li Z, Shult PA, et al. Rhinovirus illnesses during infancy predict subsequent childhood wheezing. J Allergy Clin Immunol. 2005;116(3):571-7.
17. Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med. 2008;178(7):667-72.
18. Walton RP, Johnston SL. Role of respiratory viral infections in the development of atopic conditions. Curr Opin Allergy Clin Immunol. 2008;8(2):150-3.
19. Jackson DJ, Evans MD, Gangnon RE, Tisler CJ, Pappas TE, Lee W-M, et al. Evidence for a Causal Relationship between Allergic Sensitization and Rhinovirus Wheezing in Early Life. Am J Respir Crit Care Med. 2012;185(3):281-5.
20. Lee W-M, Lemanske RF, Evans MD, Vang F, Pappas T, Gangnon R, et al. Human rhinovirus species and season of infection determine illness severity. Am J Respir Crit Care Med. 2012;186(9):886-91.
21. Nakagome K, Bochkov YA, Ashraf S, Brockman-Schneider RA, Evans MD, Pasic TR, et al. Effects of rhinovirus species on viral replication and cytokine production. J Allergy Clin Immunol. 2014;134(2):332-41.
22. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk H-D. Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A. 2004;101(13):4620-4.
23. Mounts AW, Kwong H, Izurieta HS, Ho Y, Au T, Lee M, et al. Case-control study of risk factors for avian influenza A (H5N1) disease, Hong Kong, 1997. J Infect Dis. 1999;180(2):505-8.
24. Centers for Disease Control and Prevention (CDC). Update: influenza activity--United States and worldwide, 2002-03 season, and composition of the 2003-04 influenza vaccine. MMWR Morb Mortal Wkly Rep. 2003;52(22):516-21.
25. Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, et al. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol. 2000;74(18):8502-12.
26. Matrosovich M, Matrosovich T, Uhlendorff J, Garten W, Klenk H-D. Avian-virus-like receptor specificity of the hemagglutinin impedes influenza virus replication in cultures of human airway epithelium. Virology. 2007;361(2):384-90.
27. Sims AC, Baric RS, Yount B, Burkett SE, Collins PL, Pickles RJ. Severe acute respiratory syndrome coronavirus infection of human ciliated airway epithelia: role of ciliated cells in viral spread in the conducting airways of the lungs. J Virol. 2005;79(24):15511-24.
28. Chan RWY, Chan MCW, Agnihothram S, Chan LLY, Kuok DIT, Fong JHM, et al. Tropism of and innate immune responses to the novel human betacoronavirus lineage C virus in human ex vivo respiratory organ cultures. J Virol. 2013;87(12):6604-14.
29. To KF, Tong JHM, Chan PKS, Au FWL, Chim SSC, Chan KCA, et al. Tissue and cellular tropism of the coronavirus associated with severe acute respiratory syndrome: an in-situ hybridization study of fatal cases. J Pathol. 2004;202(2):157-63.
30. Matsuyama S, Nagata N, Shirato K, Kawase M, Takeda M, Taguchi F. Efficient Activation of the Severe Acute Respiratory Syndrome Coronavirus Spike Protein by the Transmembrane Protease TMPRSS2. J Virol. 2010;84(24):12658-64.
31. de Arruda E, Mifflin TE, Gwaltney JM, Winther B, Hayden FG. Localization of rhinovirus replication in vitro with in situ hybridization. J Med Virol. 1991;34(1):38-44.
32. Winther B, Greve JM, Gwaltney JM, Innes DJ, Eastham JR, McClelland A, et al. Surface expression of intercellular adhesion molecule 1 on epithelial cells in the human adenoid. J Infect Dis. 1997;176(2):523-5.
33. Jakiela B, Brockman-Schneider R, Amineva S, Lee W-M, Gern JE. Basal cells of differentiated bronchial epithelium are more susceptible to rhinovirus infection. Am J Respir Cell Mol Biol. 2008;38(5):517-23.
34. 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. 2010;43(6):652-61.
35. Jakiela B, Gielicz A, Plutecka H, Hubalewska-Mazgaj M, Mastalerz L, Bochenek G, et al. Th2-type cytokine-induced mucus metaplasia decreases susceptibility of human bronchial epithelium to rhinovirus infection. Am J Respir Cell Mol Biol. 2014;51(2):229-41.
36. Zhu J, Rogers AV, Burke-Gaffney A, Hellewell PG, Jeffery PK. Cytokine-induced airway epithelial ICAM-1 upregulation: quantification by high-resolution scanning and transmission electron microscopy. Eur Respir J. 1999;13(6):1318-28.
37. Bochkov YA, Palmenberg AC, Lee W-M, Rathe JA, Amineva SP, Sun X, et al. Molecular modeling, organ culture and reverse genetics for a newly identified human rhinovirus C. Nat Med. 2011;17(5):627-32.
38. Bochkov YA, Watters K, Ashraf S, Griggs TF, Devries MK, Jackson DJ, et al. 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(17):5484-90.
39. Griggs TF, Bochkov YA, Nakagome K, Palmenberg AC, Gern JE. Production, purification, and capsid stability of rhinovirus C types. J Virol Methods. 2015;217:18-23.
40. Ashraf S, Brockman-Schneider R, Bochkov YA, Pasic TR, Gern JE. Biological characteristics and propagation of human rhinovirus-C in differentiated sinus epithelial cells. Virology. 2013;436(1):143-9.
41. Hao W, Bernard K, Patel N, Ulbrandt N, Feng H, Svabek C, et al. Infection and propagation of human rhinovirus C in human airway epithelial cells. J Virol. 2012;86(24):13524-32.
42. Bochkov YA, Gern JE. Clinical and molecular features of human rhinovirus C. Microbes Infect Inst Pasteur. 2012;14(6):485-94.
43. Wadsworth SJ, Riedel M, Afshari AE, Louis S, Dorscheid D. PneumaCultTM-ALI: an improved media for mucociliary differentiation of primary human bronchial epithelial cells. Am J Respir Crit Care Med. 2012;185:A6345.
44. Villenave R, Shields MD, Power UF. Respiratory syncytial virus interaction with human airway epithelium. Trends Microbiol. 2013;21(5):238-44.
45. Zhang L, Peeples ME, Boucher RC, Collins PL, Pickles RJ. Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. J Virol. 2002;76(11):5654-66.
46. Zhang L, Collins PL, Lamb RA, Pickles RJ. Comparison of differing cytopathic effects in human airway epithelium of parainfluenza virus 5 (W3A), parainfluenza virus type 3, and respiratory syncytial virus. Virology. 2011;421(1):67-77.
47. Smith CM, Kulkarni H, Radhakrishnan P, Rutman A, Bankart MJ, Williams G, et al. Ciliary dyskinesia is an early feature of respiratory syncytial virus infection. Eur Respir J. 2014;43(2):485-96.
48. Mata M, Sarrion I, Armengot M, Carda C, Martinez I, Melero JA, et al. Respiratory syncytial virus inhibits ciliagenesis in differentiated normal human bronchial epithelial cells: effectiveness of N-acetylcysteine. PloS One. 2012;7(10), e48037.
49. Villenave R, Thavagnanam S, Sarlang S, Parker J, Douglas I, Skibinski G, et al. In vitro modeling of respiratory syncytial virus infection of pediatric bronchial epithelium, the primary target of infection in vivo. Proc Natl Acad Sci U S A. 2012;109(13):5040-5.
50. Bønnelykke K, Sleiman P, Nielsen K, Kreiner-Møller E, Mercader JM, Belgrave D, et al. A genome-wide association study identifies CDHR3 as a susceptibility locus for early childhood asthma with severe exacerbations. Nat Genet. 2014;46(1):51-5.
51. Tesfaigzi Y. Regulation of mucous cell metaplasia in bronchial asthma. Curr Mol Med. 2008;8(5):408-15.
52. Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM, Hooper LV, et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science. 2011;334(6053):249-52.
53. Robinson CM, Jesudhasan PR, Pfeiffer JK. Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell Host Microbe. 2014;15(1):36-46.
54. Nawijn MC, Hackett TL, Postma DS, van Oosterhout AJM, Heijink IH. E-cadherin: gatekeeper of airway mucosa and allergic sensitization. Trends Immunol. 2011;32(6):248-55.
55. Patel AC, Brody SL, Stappenbeck TS, Holtzman MJ. Tracking cell lineage to rediscover (again) the switch from ciliated to mucous cells. Am J Respir Cell Mol Biol. 2011;44(3):261-3.
56. Bermbach S, Weinhold K, Roeder T, Petersen F, Kugler C, Goldmann T, et al. Mechanisms of Cilia-Driven Transport in the Airways in the Absence of Mucus. Am J Respir Cell Mol Biol. 2014;51(1):56-67.
57. Sajjan U, Wang Q, Zhao Y, Gruenert DC, Hershenson MB. Rhinovirus Disrupts the Barrier Function of Polarized Airway Epithelial Cells. Am J Respir Crit Care Med. 2008;178(12):1271-81.