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Infection of Ciliated Cells by Human Parainfluenza Virus Type 3 in an In Vitro Model of Human Airway Epithelium
Open accessAbstract
We constructed a human recombinant parainfluenza virus type 3 (rPIV3) that expresses enhanced green fluorescent protein (GFP) and used this virus, rgPIV3, to characterize PIV3 infection of an established in vitro model of human pseudostratified mucociliary airway epithelium (HAE). The apical surface of HAE was highly susceptible to rgPIV3 infection, whereas only occasional cells were infected when virus was applied to the basolateral surface. Infection involved exclusively ciliated epithelial cells. There was little evidence of virus-mediated cytopathology and no spread of the virus beyond the ciliated cell types. Infection of ciliated cells by rgPIV3 was sensitive to a neuraminidase specific for α2-6-linked sialic acid residues, but not to a neuraminidase that cleaves α2-3- and α2-8-linked sialic acid residues. This provided evidence that rgPIV3 utilizes α2-6-linked sialic acid residues for initiating infection, a specificity also described for human influenza viruses. The PIV3 fusion (F) glycoprotein was trafficked exclusively to the apical surface of ciliated cells, which also was the site of release of progeny virus. F glycoprotein localized predominately to the membranes of the cilial shafts, suggesting that progeny viruses may bud from cilia per se. The polarized trafficking of F glycoprotein to the apical surface also likely restricts its interaction with neighboring cells and could account for the observed lack of cell-cell fusion. HAE derived from cystic fibrosis patients was not more susceptible to rgPIV3 infection but did exhibit limited spread of virus due to impaired movement of lumenal secretions due to compromised function of the cilia.
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“Type III IFNs possess antiviral properties similar to those of type I IFNs but appear to be expressed especially by epithelial cells and consequently exert host protection primarily at epithelial surfaces (8, 9, 335).”
From The airway epithelium: soldier in the fight against respiratory viruses (2011) · cites this paper as [335]
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Cites
Fuerst, T. R., Niles, E. G., Studier, F. W., & Moss, B. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.21.8122 · Cited by 2,078
Summerford, C., & Samulski, R. J. (1998) · Journal of Virology · doi:10.1128/jvi.72.2.1438-1445.1998 · Cited by 1,409
Matsui, H., Grubb, B. R., Tarran, R., Randell, S. H., Gatzy, J. T., Davis, C. W., & Boucher, R. C. (1998) · Cell · doi:10.1016/s0092-8674(00)81724-9 · Cited by 1,168
Nguyen, D., & Hildreth, J. E. K. (2000) · Journal of Virology · doi:10.1128/jvi.74.7.3264-3272.2000 · Cited by 788
Human and avian influenza viruses target different cell types in cultures of human airway epithelium
Matrosovich, M. N., Matrosovich, T. Y., Gray, T. E., Roberts, N. A., & Klenk, H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308001101 · Cited by 777
Zhang, L., Peeples, M. E., Boucher, R. C., Collins, P. L., & Pickles, R. J. (2002) · Journal of Virology · doi:10.1128/jvi.76.11.5654-5666.2002 · Cited by 583
Self-citationDevelopmental changes in heparan sulfate expression: in situ detection with mAbs.
David, G., Bai, X. M., der Schueren, B. V., Cassiman, J. J., & BERGHE, H. V. D. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.119.4.961 · Cited by 479
Pathological changes in virus infections of the lower respiratory tract in children
Aherne, W., Bird, T., Court, S., Gardner, P. S., & McQuillin, J. (1970) · Journal of Clinical Pathology · doi:10.1136/jcp.23.1.7 · Cited by 450
Paramyxovirus Fusion: A Hypothesis for Changes
Lamb, R. A. (1993) · Virology · doi:10.1006/viro.1993.1561 · Cited by 420
Coordinated clearance of periciliary liquid and mucus from airway surfaces.
Matsui, H., Randell, S. H., Peretti, S. W., Davis, C. W., & Boucher, R. C. (1998) · Journal of Clinical Investigation · doi:10.1172/jci2687 · Cited by 397
Walters, R. W., Grunst, T., Bergelson, J. M., Finberg, R. W., Welsh, M. J., & Zabner, J. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.15.10219 · Cited by 372
Glycosaminoglycan Sulfation Requirements for Respiratory Syncytial Virus Infection
Hallak, L. K., Spillmann, D., Collins, P. L., & Peeples, M. E. (2000) · Journal of Virology · doi:10.1128/jvi.74.22.10508-10513.2000 · Cited by 311
Self-citationPickles, R. J., McCarty, D. M., Matsui, H., Hart, P., Randell, S. H., & Boucher, R. C. (1998) · Journal of Virology · doi:10.1128/jvi.72.7.6014-6023.1998 · Cited by 295
Self-citationDechecchi, M. C., Melotti, P., Bonizzato, A., Santacatterina, M., Chilosi, M., & Cabrini, G. (2001) · Journal of Virology · doi:10.1128/jvi.75.18.8772-8780.2001 · Cited by 292
Lipid rafts and HIV-1: from viral entry to assembly of progeny virions
Campbell, S. M., Crowe, S. M., & Mak, J. (2001) · Journal of Clinical Virology · doi:10.1016/s1386-6532(01)00193-7 · Cited by 280
Feldman, S. A., Audet, S. A., & Beeler, J. A. (2000) · Journal of Virology · doi:10.1128/jvi.74.14.6442-6447.2000 · Cited by 270
Heparan Sulfate Glycosaminoglycans Are Involved in Adenovirus Type 5 and 2-Host Cell Interactions
Dechecchi, M. C., Tamanini, A., Bonizzato, A., & Cabrini, G. (2000) · Virology · doi:10.1006/viro.1999.0171 · Cited by 261
Tarran, R., Grubb, B. R., Parsons, D., Picher, M., Hirsh, A. J., Davis, C. W., & Boucher, R. C. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00286-6 · Cited by 259
Hallak, L. K., Collins, P. L., Knudson, W., & Peeples, M. E. (2000) · Virology · doi:10.1006/viro.2000.0293 · Cited by 234
Self-citationHeparin-dependent attachment ofrespiratory syncytial virus (RSV) to host cells
Krusat, T., & Streckert, H. J. (1997) · Archives of Virology · doi:10.1007/s007050050156 · Cited by 225
Manié, S. N., de Breyne, S., Vincent, S., & Gerlier, D. (2000) · Journal of Virology · doi:10.1128/jvi.74.1.305-311.2000 · Cited by 224
Baum, L. G., & Jc, P. (1990) · PubMed · Cited by 198
Human-specific Regulation of α2–6-linked Sialic Acids
Gagneux, P., Cheriyan, M., Hurtado‐Ziola, N., der Linden, E. C. M. B.-V., Anderson, D., McClure, H. M., Varki, A. P., & Varki, N. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m309813200 · Cited by 187
Respiratory syncytial virus matures at the apical surfaces of polarized epithelial cells
Roberts, S. R., Compans, R. W., & Wertz, G. W. (1995) · Journal of Virology · doi:10.1128/jvi.69.4.2667-2673.1995 · Cited by 166
Pickles, R. J., Fahrner, J. A., Petrella, J. M., Boucher, R. C., & Bergelson, J. M. (2000) · Journal of Virology · doi:10.1128/jvi.74.13.6050-6057.2000 · Cited by 160
Self-citationTakimoto, T., Taylor, G. L., Connaris, H., Crennell, S. J., & Portner, A. (2002) · Journal of Virology · doi:10.1128/jvi.76.24.13028-13033.2002 · Cited by 158
Sendai virus utilizes specific sialyloligosaccharides as host cell receptor determinants.
Markwell, M. A. K., & Paulson, J. C. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.10.5693 · Cited by 134
Receptor Specificities of Human Respiroviruses
Suzuki, T., Portner, A., Scroggs, R. A., Uchikawa, M., Koyama, N., Matsuo, K., Suzuki, Y., & Takimoto, T. (2001) · Journal of Virology · doi:10.1128/jvi.75.10.4604-4613.2001 · Cited by 133
Recovery of Infectious Human Parainfluenza Virus Type 3 from cDNA
Durbin, A. P., Hall, S. L., Siew, J. W., Whitehead, S. S., Collins, P. L., & Murphy, B. R. (1997) · Virology · doi:10.1006/viro.1997.8697 · Cited by 111
Self-citationEnhanced Epithelial Gene Transfer by Modulation of Tight Junctions with Sodium Caprate
Coyne, C. B., Kelly, M. M., Boucher, R. C., & Johnson, L. G. (2000) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.23.5.4164 · Cited by 107
Yao, Q. C., Hu, X., & Compans, R. W. (1997) · Journal of Virology · doi:10.1128/jvi.71.1.650-656.1997 · Cited by 98
Stonebraker, J. R., Wagner, D., Lefensty, R. W., Burns, K. A., Gendler, S. J., Bergelson, J. M., Boucher, R. C., O’Neal, W. K., & Pickles, R. J. (2004) · Journal of Virology · doi:10.1128/jvi.78.24.13755-13768.2004 · Cited by 82
Self-citationDurbin, A. P., Siew, J. W., Murphy, B. R., & Collins, P. L. (1997) · Virology · doi:10.1006/viro.1997.8633 · Cited by 76
Self-citationHeminway, B. R., Yu, Y. W., & Galinski, M. S. (1994) · Virus Research · doi:10.1016/0168-1702(94)90066-3 · Cited by 68
Pickles, R. J., Barker, P., Ye, H., & Boucher, R. C. (1996) · Human Gene Therapy · doi:10.1089/hum.1996.7.8-921 · Cited by 64
Self-citationIntracellular trafficking of cell surface sialoglycoconjugates.
Reichner, J. S., Whiteheart, S. W., & Hart, G. W. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)37595-1 · Cited by 61
Hoe, M. H., Slusarewicz, P., Misteli, T., Watson, R., & Warren, G. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.42.25057 · Cited by 56
Attachment of Two Myxoviruses to Ciliated Epithelial Cells
Dourmashkin, R. R., & Tyrrell, D. A. J. (1970) · Journal of General Virology · doi:10.1099/0022-1317-9-1-77 · Cited by 55
Role of Heparan Sulfate in Human Parainfluenza Virus Type 3 Infection
Bose, S., & Banerjee, A. K. (2002) · Virology · doi:10.1006/viro.2002.1484 · Cited by 55
Bose, S., Malur, A. G., & Banerjee, A. K. (2001) · Journal of Virology · doi:10.1128/jvi.75.4.1984-1989.2001 · Cited by 54
Receptor ganglioside content of three hosts for sendai virus: MDBK, HeLa, and MDCK Cells
Markwell, M. A. K., Fredman, P., & Svennerholm, L. (1984) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(84)90228-1 · Cited by 53
Moscona, A., & PELUSO, R. W. (1992) · Journal of Virology · doi:10.1128/jvi.66.11.6280-6287.1992 · Cited by 50
Skiadopoulos, M. H., Surman, S. R., Riggs, J. M., Örvell, C., Collins, P. L., & Murphy, B. R. (2002) · Virology · doi:10.1006/viro.2002.1415 · Cited by 50
Self-citationPerlman, S. L., Jordan, M., Brossmer, R., Greengard, O., & Moscona, A. (1999) · Virology · doi:10.1006/viro.1999.0024 · Cited by 32
Progenitor-Progeny Relationships in Airway Epithelium
Randell, S. H. (1992) · CHEST Journal · doi:10.1378/chest.101.3_supplement.11s · Cited by 31
Barretto, N., Hallak, L. K., & Peeples, M. E. (2003) · Virology · doi:10.1016/s0042-6822(03)00288-5 · Cited by 30
Self-citationCapdeville, Y., & Benwakrim, A. (1996) · PubMed · Cited by 26
Paramecium GPI Proteins: Variability of Expression and Localization
Capdeville, Y. (2000) · Protist · doi:10.1078/1434-4610-00016 · Cited by 15
Interaction of human parainfluenza virus type 3 with the host cell surface
Moscona, A. (1997) · The Pediatric Infectious Disease Journal · doi:10.1097/00006454-199710000-00003 · Cited by 13
Research works printed but not linked: 4
- Chanock R. M. B. R. Murphy and P. L. Collins. 2001. Parainfluenza viruses p. 1341-1380. In D. M. Knipe and P. M. Howley (ed.) Fields virology 4th ed. vol. 1. Lippincott Williams & Wilkins Philadelphia Pa.
- Collins P. L. R. M. Chanock and B. R. Murphy. 2001. Respiratory syncytial virus p. 1443-1485. In D. M. Knipe and P. M. Howley (ed.) Fields virology 4th ed. vol. 1. Lippincott Williams & Wilkins Philadelphia Pa.
- Lamb R. and D. Kolakofsky. 1996. Paramyxoviridae: the viruses and their replication p. 1305-1340. In D. M. Knipe and P. M. Howley (ed.) Fields virology 4th ed. vol. 1. Lippincott Williams & Wilkins Philadelphia Pa.
- Lamb R. A. and R. M. Krug. 2001. Orthomyxoviridae : the viruses and their replication p. 1487-1579. In D. M. Knipe and P. M. Howley (ed.) Fields virology 4th ed. vol. 1. Lippincott Williams and Wilkins Philadelphia Pa.
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Schoggins, J. W., MacDuff, D. A., Imanaka, N., Gainey, M. D., Shrestha, B., Eitson, J. L., Mar, K. B., Richardson, R. B., Ratushny, A. V., Litvak, V., et al. (2014) · Nature · doi:10.1038/nature12862 · Cited by 896
The airway epithelium: soldier in the fight against respiratory viruses
Vareille, M., Kieninger, E., Edwards, M. R., & Regamey, N. (2011) · Clinical Microbiology Reviews · doi:10.1128/cmr.00014-10 · Cited by 655
Respiratory Syncytial Virus: Infection, Detection, and New Options for Prevention and Treatment
Griffiths, C. D., Drews, S. J., & Marchant, D. (2016) · Clinical Microbiology Reviews · doi:10.1128/cmr.00010-16 · Cited by 627
Engineered In Vitro Disease Models
Benam, K. H., Dauth, S., Hassell, B., Herland, A., Jain, A., Jang, K.-J., Karalis, K., Kim, H. J., MacQueen, L., Mahmoodian, R., et al. (2015) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-012414-040418 · Cited by 554
Metadata
- Authors
- Zhang, L., Bukreyev, A., Thompson, C. I., Watson, B., Peeples, M. E., Collins, P. L., & Pickles, R. J.
- Affiliations
- Cystic Fibrosis/Pulmonary Research and Treatment Center
- National Institutes of Health (US)
- Abigail Wexner Research Institute (US)
- University of North Carolina at Chapel Hill (US)
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2005-01-15
- Volume
- 79
- Issue
- 2
- Pages
- 1113-1124
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC538579
- OpenAlex
- W2159953474
- Cited by
- 302
- References
- 50
- Citations by year
- 2026: 12 · 2025: 12 · 2024: 19 · 2023: 13 · 2022: 16 · 2021: 17 · 2020: 19 · 2019: 17 · 2018: 12 · 2017: 9 · 2016: 11 · 2015: 9 · 2014: 16 · 2013: 12 · 2012: 15
- FWCI
- 6.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- National Institutes of Health
- National Heart, Lung, and Blood Institute (P01HL051818, HL 66943-01, HL 51818-09)
- Topics
- Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Keywords
- parainfluenza virus type 3, ciliated epithelial cells, airway epithelium, neuraminidase sensitivity, cell-cell fusion, cystic fibrosis
- MeSH terms
- Bronchi, Cell Differentiation, Cells, Cultured, Cilia, Epithelial Cells, Heparan Sulfate, Heparitin Sulfate, Humans, Neuraminidase, Parainfluenza Virus 3, Human, Trachea, Viral Proteins, Virus Shedding, N-Acetylneuraminic Acid
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