1887

Abstract

Human rhinoviruses (HRV) are responsible for the majority of virus infections of the upper respiratory tract. Furthermore, HRV infection is associated with acute exacerbation of asthma and other chronic respiratory diseases of the lower respiratory tract. A small animal model of HRV-induced disease is required for the development of new therapies. However, existing mouse models of HRV infection are difficult to work with and until recently mouse cell lines were thought to be generally non-permissive for HRV replication . In this report we demonstrate that a virus of the minor receptor group, HRV1B, can infect and replicate in a mouse respiratory epithelial cell line (LA-4) more efficiently than in a mouse fibroblast cell line (L). The major receptor group virus HRV16 requires human intercellular adhesion molecule-1 (ICAM-1) for cell entry and therefore cannot infect LA-4 cells. However, transfection of -transcribed HRV16 RNA resulted in the replication of viral RNA and production of infectious virus. Expression of a chimeric ICAM-1 molecule, comprising mouse ICAM-1 with extracellular domains 1 and 2 replaced by the equivalent human domains, rendered the otherwise non-permissive mouse respiratory epithelial cell line susceptible to entry and efficient replication of HRV16. These observations suggest that the development of mouse models of respiratory tract infection by major as well as minor group HRV should be pursued.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.19109-0
2003-10-01
2019-12-14
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/10/vir842829.html?itemId=/content/journal/jgv/10.1099/vir.0.19109-0&mimeType=html&fmt=ahah

References

  1. Arruda, E., Boyle, T. R., Winther, B., Pevear, D. C., Gwaltney, J. M., Jr & Hayden, F. G. ( 1995; ). Localization of human rhinovirus replication in the upper respiratory tract by in situ hybridization. J Infect Dis 171, 1329–1333.[CrossRef]
    [Google Scholar]
  2. Bella, J., Kolatkar, P. R., Marlor, C. W., Greve, J. M. & Rossmann, M. G. ( 1998; ). The structure of the two amino-terminal domains of human ICAM-1 suggests how it functions as a rhinovirus receptor and as an LFA-1 integrin ligand. Proc Natl Acad Sci U S A 95, 4140–4145.[CrossRef]
    [Google Scholar]
  3. Greve, J. M., Davis, G., Meyer, A. M., Forte, C. P., Yost, S. C., Marlor, C. W., Kamarck, M. E. & McClelland, A. ( 1989; ). The major human rhinovirus receptor is ICAM-1. Cell 56, 839–847.[CrossRef]
    [Google Scholar]
  4. Grunert, H. P., Wolf, K. U., Langner, K. D., Sawitzky, D., Habermehl, K. O. & Zeichhardt, H. ( 1997; ). Internalization of human rhinovirus 14 into HeLa and ICAM-1-transfected BHK cells. Med Microbiol Immunol (Berl) 186, 1–9.[CrossRef]
    [Google Scholar]
  5. Harris, J. R. & Racaniello, V. R. ( 2003; ). Changes in rhinovirus protein 2C allow efficient replication in mouse cells. J Virol 77, 4773–4780.[CrossRef]
    [Google Scholar]
  6. Hofer, F., Berger, B., Gruenberger, M., Machat, H., Dernick, R., Tessmer, U., Kuechler, E. & Blaas, D. ( 1992; ). Shedding of a rhinovirus minor group binding protein: evidence for a Ca2+-dependent process. J Gen Virol 73, 627–632.[CrossRef]
    [Google Scholar]
  7. Johnston, S. L. ( 1998; ). Viruses and asthma. Allergy 53, 922–932.[CrossRef]
    [Google Scholar]
  8. Johnston, S. L., Sanderson, G., Pattemore, P. K., Smith, S., Bardin, P. G., Bruce, C. B., Lambden, P. R., Tyrrell, D. A. & Holgate, S. T. ( 1993; ). Use of polymerase chain reaction for diagnosis of picornavirus infection in subjects with and without respiratory symptoms. J Clin Microbiol 31, 111–117.
    [Google Scholar]
  9. Johnston, S. L., Pattemore, P. K., Sanderson, G. & 8 other authors ( 1995; ). Community study of role of viral infections in exacerbations of asthma in 9–11 year old children. BMJ 310, 1225–1229.[CrossRef]
    [Google Scholar]
  10. Johnston, S. L., Papi, A., Bates, P. J., Mastronarde, J. G., Monick, M. M. & Hunninghake, G. W. ( 1998; ). Low grade rhinovirus infection induces a prolonged release of IL-8 in pulmonary epithelium. J Immunol 160, 6172–6181.
    [Google Scholar]
  11. Koike, S., Taya, C., Kurata, T., Abe, S., Ise, I., Yonekawa, H. & Nomoto, A. ( 1991; ). Transgenic mice susceptible to poliovirus. Proc Natl Acad Sci U S A 88, 951–955.[CrossRef]
    [Google Scholar]
  12. Lomax, N. B. & Yin, F. H. ( 1989; ). Evidence for the role of the P2 protein of human rhinovirus in its host range change. J Virol 63, 2396–2399.
    [Google Scholar]
  13. Makgoba, M. W., Sanders, M. E., Ginther Luce, G. E., Dustin, M. L., Springer, T. A., Clark, E. A., Mannoni, P. & Shaw, S. ( 1988; ). ICAM-1 a ligand for LFA-1-dependent adhesion of B, T and myeloid cells. Nature 331, 86–88.[CrossRef]
    [Google Scholar]
  14. Marlovits, T. C., Abrahamsberg, C. & Blaas, D. ( 1998; ). Very-low-density lipoprotein receptor fragment shed from HeLa cells inhibits human rhinovirus infection. J Virol 72, 10246–10250.
    [Google Scholar]
  15. McKnight, K. L. & Lemon, S. M. ( 1996; ). Capsid coding sequence is required for efficient replication of human rhinovirus 14 RNA. J Virol 70, 1941–1952.
    [Google Scholar]
  16. Mosser, A. G., Brockman-Schneider, R., Amineva, S., Burchell, L., Sedgwick, J. B., Busse, W. W. & Gern, J. E. ( 2002; ). Similar frequency of rhinovirus-infectible cells in upper and lower airway epithelium. J Infect Dis 185, 734–743.[CrossRef]
    [Google Scholar]
  17. Papadopoulos, N. G., Bates, P. J., Bardin, P. G. & 8 other authors ( 2000; ). Rhinoviruses infect the lower airways. J Infect Dis 181, 1875–1884.[CrossRef]
    [Google Scholar]
  18. Papi, A., Stanciu, L. A., Papadopoulos, N. G., Teran, L. M., Holgate, S. T. & Johnston, S. L. ( 2000; ). Rhinovirus infection induces major histocompatibility complex class I and costimulatory molecule upregulation on respiratory epithelial cells. J Infect Dis 181, 1780–1784.[CrossRef]
    [Google Scholar]
  19. Register, R. B., Uncapher, C. R., Naylor, A. M., Lineberger, D. W. & Colonno, R. J. ( 1991; ). Human–mouse chimeras of ICAM-1 identify amino acid residues critical for rhinovirus and antibody binding. J Virol 65, 6589–6596.
    [Google Scholar]
  20. Reischl, A., Reithmayer, M., Winsauer, G., Moser, R., Gosler, I. & Blaas, D. ( 2001; ). Viral evolution toward change in receptor usage: adaptation of a major group human rhinovirus to grow in ICAM-1-negative cells. J Virol 75, 9312–9319.[CrossRef]
    [Google Scholar]
  21. Reithmayer, M., Reischl, A., Snyers, L. & Blaas, D. ( 2002; ). Species-specific receptor recognition by a minor-group human rhinovirus (HRV): HRV serotype 1A distinguishes between the mouse and the human low-density lipoprotein receptor. J Virol 76, 6957–6965.[CrossRef]
    [Google Scholar]
  22. Ren, R. B., Costantini, F., Gorgacz, E. J., Lee, J. J. & Racaniello, V. R. ( 1990; ). Transgenic mice expressing a human poliovirus receptor: a new model for poliomyelitis. Cell 63, 353–362.[CrossRef]
    [Google Scholar]
  23. Seemungal, T., Harper-Owen, R., Bhowmik, A. & 8 other authors ( 2001; ). Respiratory viruses, symptoms, and inflammatory markers in acute exacerbations and stable chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164, 1618–1623.[CrossRef]
    [Google Scholar]
  24. Shafren, D. R., Dorahy, D. J., Greive, S. J., Burns, G. F. & Barry, R. D. ( 1997; ). Mouse cells expressing human intercellular adhesion molecule-1 are susceptible to infection by coxsackievirus A21. J Virol 71, 785–789.
    [Google Scholar]
  25. Siu, G., Hedrick, S. M. & Brian, A. A. ( 1989; ). Isolation of the mouse intercellular adhesion molecule 1 (ICAM-1) gene. ICAM-1 enhances antigen-specific T cell activation. J Immunol 143, 3813–3820.
    [Google Scholar]
  26. Staunton, D. E., Merluzzi, V. J., Rothlein, R., Barton, R., Marlin, S. D. & Springer, T. A. ( 1989; ). A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56, 849–853.[CrossRef]
    [Google Scholar]
  27. Staunton, D. E., Dustin, M. L., Erickson, H. P. & Springer, T. A. ( 1990; ). The arrangement of the immunoglobulin-like domains of ICAM-1 and the binding sites for LFA-1 and rhinovirus. Cell 61, 243–254.[CrossRef]
    [Google Scholar]
  28. Staunton, D. E., Gaur, A., Chan, P. Y. & Springer, T. A. ( 1992; ). Internalization of a major group human rhinovirus does not require cytoplasmic or transmembrane domains of ICAM-1. J Immunol 148, 3271–3274.
    [Google Scholar]
  29. Tomassini, J. E., Graham, D., DeWitt, C. M., Lineberger, D. W., Rodkey, J. A. & Colonno, R. J. ( 1989; ). cDNA cloning reveals that the major group rhinovirus receptor on HeLa cells is intercellular adhesion molecule 1. Proc Natl Acad Sci U S A 86, 4907–4911.[CrossRef]
    [Google Scholar]
  30. Uncapher, C. R., DeWitt, C. M. & Colonno, R. J. ( 1991; ). The major and minor group receptor families contain all but one human rhinovirus serotype. Virology 180, 814–817.[CrossRef]
    [Google Scholar]
  31. Yin, F. H. & Lomax, N. B. ( 1983; ). Host range mutants of human rhinovirus in which nonstructural proteins are altered. J Virol 48, 410–418.
    [Google Scholar]
  32. Yin, F. H. & Lomax, N. B. ( 1986; ). Establishment of a mouse model for human rhinovirus infection. J Gen Virol 67, 2335–2340.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.19109-0
Loading
/content/journal/jgv/10.1099/vir.0.19109-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error