This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Johnson, T. R.
Right arrow Articles by Graham, B. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Johnson, T. R.
Right arrow Articles by Graham, B. S.

 Previous Article  |  Next Article 

J Virol, April 1998, p. 2871-2880, Vol. 72, No. 4
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Priming with Secreted Glycoprotein G of Respiratory Syncytial Virus (RSV) Augments Interleukin-5 Production and Tissue Eosinophilia after RSV Challenge

Teresa R. Johnson,1 Joyce E. Johnson,2 Sharon R. Roberts,3 Gail W. Wertz,4 Robert A. Parker,5 and Barney S. Graham1,6,*

Departments of Microbiology and Immunology,1 Pathology,2 and Medicine,6 Vanderbilt University School of Medicine, Nashville, Tennessee; Department of Botany and Microbiology, Auburn University, Auburn,3 and Department of Microbiology, University of Alabama at Birmingham, Birmingham,4 Alabama; and Department of Medicine (Biostatistics), Harvard University School of Medicine, Boston, Massachusetts5

Received 12 September 1997/Accepted 22 December 1997

The respiratory syncytial virus (RSV) G glycoprotein promotes differentiation of type 2 CD4+ T lymphocytes and induces an eosinophilic response in lungs of RSV-infected mice. A unique feature of G is that a second initiation codon in the transmembrane region of the glycoprotein results in secretion of soluble protein from infected cells. Recombinant vaccinia viruses that express wild-type G (vvWT G), only secreted G (vvM48), or only membrane-anchored G (vvM48I) were used to define the influence of G priming on immunopathogenesis. Mice immunized with vvM48 had more severe illness following RSV challenge than did mice primed with vvWT G or vvM48I. Coadministration of purified G during priming with the construct expressing membrane-anchored G shifted immune responses following RSV challenge to a more Th2-like response. This was characterized by increased interleukin-5 in lung supernatants and an increase in G-specific immunoglobulin G1 antibodies. Eosinophils were present in the infiltrate of all mice primed with G-containing vectors but were greatest in mice primed with regimens including secreted G. These data suggest the form of G protein available for initial antigen processing and presentation is an important factor in promoting Th2-like immune responses, including the induction of lung eosinophilia. The ability of RSV to secrete G protein may therefore represent a viral strategy for immunomodulation and be a key determinant of disease pathogenesis.

* Corresponding author. Mailing address: A-4103 MCN, Vanderbilt University School of Medicine, 1161 21st Ave., Nashville, TN 37232-2582. Phone: (615) 343-3717. Fax: (615) 322-8222. E-mail: Barney.Graham{at}mcmail.vanderbilt.edu.




This article has been cited by other articles:

  • Percopo, C. M., Qiu, Z., Phipps, S., Foster, P. S., Domachowske, J. B., Rosenberg, H. F. (2009). Pulmonary Eosinophils and Their Role in Immunopathologic Responses to Formalin-Inactivated Pneumonia Virus of Mice. J. Immunol. 183: 604-612 [Abstract] [Full Text]  
  • Olson, M. R., Hartwig, S. M., Varga, S. M. (2008). The Number of Respiratory Syncytial Virus (RSV)-Specific Memory CD8 T Cells in the Lung Is Critical for Their Ability to Inhibit RSV Vaccine-Enhanced Pulmonary Eosinophilia. J. Immunol. 181: 7958-7968 [Abstract] [Full Text]  
  • Yasui, F., Kai, C., Kitabatake, M., Inoue, S., Yoneda, M., Yokochi, S., Kase, R., Sekiguchi, S., Morita, K., Hishima, T., Suzuki, H., Karamatsu, K., Yasutomi, Y., Shida, H., Kidokoro, M., Mizuno, K., Matsushima, K., Kohara, M. (2008). Prior Immunization with Severe Acute Respiratory Syndrome (SARS)-Associated Coronavirus (SARS-CoV) Nucleocapsid Protein Causes Severe Pneumonia in Mice Infected with SARS-CoV. J. Immunol. 181: 6337-6348 [Abstract] [Full Text]  
  • Johnson, T. R., Rothenberg, M. E., Graham, B. S. (2008). Pulmonary eosinophilia requires interleukin-5, eotaxin-1, and CD4+ T cells in mice immunized with respiratory syncytial virus G glycoprotein. J. Leukoc. Biol. 84: 748-759 [Abstract] [Full Text]  
  • Ward, T. M., Traina-Dorge, V., Davis, K. A., Gray, W. L. (2008). Recombinant simian varicella viruses expressing respiratory syncytial virus antigens are immunogenic. J. Gen. Virol. 89: 741-750 [Abstract] [Full Text]  
  • Collins, P. L., Graham, B. S. (2008). Viral and Host Factors in Human Respiratory Syncytial Virus Pathogenesis. J. Virol. 82: 2040-2055 [Full Text]  
  • Yu, J.-R., Kim, S., Lee, J.-B., Chang, J. (2008). Single Intranasal Immunization with Recombinant Adenovirus-Based Vaccine Induces Protective Immunity against Respiratory Syncytial Virus Infection. J. Virol. 82: 2350-2357 [Abstract] [Full Text]  
  • Castilow, E. M., Olson, M. R., Meyerholz, D. K., Varga, S. M. (2008). Differential Role of Gamma Interferon in Inhibiting Pulmonary Eosinophilia and Exacerbating Systemic Disease in Fusion Protein-Immunized Mice Undergoing Challenge Infection with Respiratory Syncytial Virus. J. Virol. 82: 2196-2207 [Abstract] [Full Text]  
  • Castilow, E. M., Meyerholz, D. K., Varga, S. M. (2008). IL-13 Is Required for Eosinophil Entry into the Lung during Respiratory Syncytial Virus Vaccine-Enhanced Disease. J. Immunol. 180: 2376-2384 [Abstract] [Full Text]  
  • Mok, H., Lee, S., Utley, T. J., Shepherd, B. E., Polosukhin, V. V., Collier, M. L., Davis, N. L., Johnston, R. E., Crowe, J. E. Jr. (2007). Venezuelan Equine Encephalitis Virus Replicon Particles Encoding Respiratory Syncytial Virus Surface Glycoproteins Induce Protective Mucosal Responses in Mice and Cotton Rats. J. Virol. 81: 13710-13722 [Abstract] [Full Text]  
  • Olson, M. R., Varga, S. M. (2007). CD8 T Cells Inhibit Respiratory Syncytial Virus (RSV) Vaccine-Enhanced Disease. J. Immunol. 179: 5415-5424 [Abstract] [Full Text]  
  • Singh, A. M., Moore, P. E., Gern, J. E., Lemanske, R. F. Jr., Hartert, T. V. (2007). Bronchiolitis to Asthma: A Review and Call for Studies of Gene-Virus Interactions in Asthma Causation. Am. J. Respir. Crit. Care Med. 175: 108-119 [Abstract] [Full Text]  
  • Lukacs, N. W., Moore, M. L., Rudd, B. D., Berlin, A. A., Collins, R. D., Olson, S. J., Ho, S. B., Peebles, R. S. Jr (2006). Differential Immune Responses and Pulmonary Pathophysiology Are Induced by Two Different Strains of Respiratory Syncytial Virus. Am. J. Pathol. 169: 977-986 [Abstract] [Full Text]  
  • Milstone, A. P., Brumble, L. M., Barnes, J., Estes, W., Loyd, J. E., Pierson, R. N. III, Dummer, S. (2006). A single-season prospective study of respiratory viral infections in lung transplant recipients. Eur Respir J 28: 131-137 [Abstract] [Full Text]  
  • Peebles, R. S. Jr., Graham, B. S. (2005). Pathogenesis of Respiratory Syncytial Virus Infection in the Murine Model. Proc Am Thorac Soc 2: 110-115 [Abstract] [Full Text]  
  • Collins, P. L., Murphy, B. R. (2005). New Generation Live Vaccines against Human Respiratory Syncytial Virus Designed by Reverse Genetics. Proc Am Thorac Soc 2: 166-173 [Abstract] [Full Text]  
  • Openshaw, P. J. M., Tregoning, J. S. (2005). Immune Responses and Disease Enhancement during Respiratory Syncytial Virus Infection. Clin. Microbiol. Rev. 18: 541-555 [Abstract] [Full Text]  
  • McCurdy, L. H., Rutigliano, J. A., Johnson, T. R., Chen, M., Graham, B. S. (2004). Modified Vaccinia Virus Ankara Immunization Protects against Lethal Challenge with Recombinant Vaccinia Virus Expressing Murine Interleukin-4. J. Virol. 78: 12471-12479 [Abstract] [Full Text]  
  • Johnson, T. R., Varga, S. M., Braciale, T. J., Graham, B. S. (2004). V{beta}14+ T Cells Mediate the Vaccine-Enhanced Disease Induced by Immunization with Respiratory Syncytial Virus (RSV) G Glycoprotein but Not with Formalin-Inactivated RSV. J. Virol. 78: 8753-8760 [Abstract] [Full Text]  
  • Johnson, T. R., Teng, M. N., Collins, P. L., Graham, B. S. (2004). Respiratory Syncytial Virus (RSV) G Glycoprotein Is Not Necessary for Vaccine-Enhanced Disease Induced by Immunization with Formalin-Inactivated RSV. J. Virol. 78: 6024-6032 [Abstract] [Full Text]  
  • Schwarze, J, Schauer, U (2004). Enhanced virulence, airway inflammation and impaired lung function induced by respiratory syncytial virus deficient in secreted G protein. Thorax 59: 517-521 [Abstract] [Full Text]  
  • Easton, A. J., Domachowske, J. B., Rosenberg, H. F. (2004). Animal Pneumoviruses: Molecular Genetics and Pathogenesis. Clin. Microbiol. Rev. 17: 390-412 [Abstract] [Full Text]  
  • Rutigliano, J. A., Johnson, T. R., Hollinger, T. N., Fischer, J. E., Aung, S., Graham, B. S. (2004). Treatment with Anti-LFA-1 Delays the CD8+ Cytotoxic-T-Lymphocyte Response and Viral Clearance in Mice with Primary Respiratory Syncytial Virus Infection. J. Virol. 78: 3014-3023 [Abstract] [Full Text]  
  • Chang, J., Choi, S. Y., Jin, H. T., Sung, Y. C., Braciale, T. J. (2004). Improved Effector Activity and Memory CD8 T Cell Development by IL-2 Expression during Experimental Respiratory Syncytial Virus Infection. J. Immunol. 172: 503-508 [Abstract] [Full Text]  
  • Haynes, L. M., Jones, L. P., Barskey, A., Anderson, L. J., Tripp, R. A. (2003). Enhanced Disease and Pulmonary Eosinophilia Associated with Formalin-Inactivated Respiratory Syncytial Virus Vaccination Are Linked to G Glycoprotein CX3C-CX3CR1 Interaction and Expression of Substance P. J. Virol. 77: 9831-9844 [Abstract] [Full Text]  
  • Johnson, T. R., Parker, R. A., Johnson, J. E., Graham, B. S. (2003). IL-13 Is Sufficient for Respiratory Syncytial Virus G Glycoprotein-Induced Eosinophilia After Respiratory Syncytial Virus Challenge. J. Immunol. 170: 2037-2045 [Abstract] [Full Text]  
  • Schmidt, U., Beyer, J., Polster, U., Gershwin, L. J., Buchholz, U. J. (2002). Mucosal Immunization with Live Recombinant Bovine Respiratory Syncytial Virus (BRSV) and Recombinant BRSV Lacking the Envelope Glycoprotein G Protects against Challenge with Wild-Type BRSV. J. Virol. 76: 12355-12359 [Abstract] [Full Text]  
  • Lee, C. G., Homer, R. J., Cohn, L., Link, H., Jung, S., Craft, J. E., Graham, B. S., Johnson, T. R., Elias, J. A. (2002). Transgenic Overexpression of Interleukin (IL)-10 in the Lung Causes Mucus Metaplasia, Tissue Inflammation, and Airway Remodeling via IL-13-dependent and -independent Pathways. J. Biol. Chem. 277: 35466-35474 [Abstract] [Full Text]  
  • Johnson, T. R., Hong, S., Van Kaer, L., Koezuka, Y., Graham, B. S. (2002). NK T Cells Contribute to Expansion of CD8+ T Cells and Amplification of Antiviral Immune Responses to Respiratory Syncytial Virus. J. Virol. 76: 4294-4303 [Abstract] [Full Text]  
  • Durbin, J. E., Johnson, T. R., Durbin, R. K., Mertz, S. E., Morotti, R. A., Peebles, R. S., Graham, B. S. (2002). The Role of IFN in Respiratory Syncytial Virus Pathogenesis. J. Immunol. 168: 2944-2952 [Abstract] [Full Text]  
  • Schlender, J., Walliser, G., Fricke, J., Conzelmann, K.-K. (2002). Respiratory Syncytial Virus Fusion Protein Mediates Inhibition of Mitogen-Induced T-Cell Proliferation by Contact. J. Virol. 76: 1163-1170 [Abstract] [Full Text]  
  • Holtzman, M. J., Morton, J. D., Shornick, L. P., Tyner, J. W., O'Sullivan, M. P., Antao, A., Lo, M., Castro, M., Walter, M. J. (2002). Immunity, Inflammation, and Remodeling in the Airway Epithelial Barrier: Epithelial-Viral-Allergic Paradigm. Physiol. Rev. 82: 19-46 [Abstract] [Full Text]  
  • Prince, G. A., Curtis, S. J., Yim, K. C., Porter, D. D. (2001). Vaccine-enhanced respiratory syncytial virus disease in cotton rats following immunization with Lot 100 or a newly prepared reference vaccine. J. Gen. Virol. 82: 2881-2888 [Abstract] [Full Text]  
  • Haynes, L. M., Moore, D. D., Kurt-Jones, E. A., Finberg, R. W., Anderson, L. J., Tripp, R. A. (2001). Involvement of Toll-Like Receptor 4 in Innate Immunity to Respiratory Syncytial Virus. J. Virol. 75: 10730-10737 [Abstract] [Full Text]  
  • Johnson, T. R., Fischer, J. E., Graham, B. S. (2001). Construction and characterization of recombinant vaccinia viruses co-expressing a respiratory syncytial virus protein and a cytokine. J. Gen. Virol. 82: 2107-2116 [Abstract] [Full Text]  
  • Lu, Y. E., Eng, C. H., Shome, S. G., Kielian, M. (2001). In Vivo Generation and Characterization of a Soluble Form of the Semliki Forest Virus Fusion Protein. J. Virol. 75: 8329-8339 [Abstract] [Full Text]  
  • Simmons, C. P., Hussell, T., Sparer, T., Walzl, G., Openshaw, P., Dougan, G. (2001). Mucosal Delivery of a Respiratory Syncytial Virus CTL Peptide with Enterotoxin-Based Adjuvants Elicits Protective, Immunopathogenic, and Immunoregulatory Antiviral CD8+ T Cell Responses. J. Immunol. 166: 1106-1113 [Abstract] [Full Text]  
  • Yamamoto, N., Suzuki, S., Suzuki, Y., Shirai, A., Nakazawa, M., Suzuki, M., Takamasu, T., Nagashima, Y., Minami, M., Ishigatsubo, Y. (2001). Immune Response Induced by Airway Sensitization after Influenza A Virus Infection Depends on Timing of Antigen Exposure in Mice. J. Virol. 75: 499-505 [Abstract] [Full Text]  
  • Barr, F. E., Pedigo, H., Johnson, T. R., Shepherd, V. L. (2000). Surfactant Protein-A Enhances Uptake of Respiratory Syncytial Virus by Monocytes and U937 Macrophages. Am. J. Respir. Cell Mol. Bio. 23: 586-592 [Abstract] [Full Text]  
  • Smith, P. M., Zhang, Y., Grafton, W. D., Jennings, S. R., O'Callaghan, D. J. (2000). Severe Murine Lung Immunopathology Elicited by the Pathogenic Equine Herpesvirus 1 Strain RacL11 Correlates with Early Production of Macrophage Inflammatory Proteins 1alpha , 1beta , and 2 and Tumor Necrosis Factor Alpha. J. Virol. 74: 10034-10040 [Abstract] [Full Text]  
  • Tripp, R. A., Jones, L., Anderson, L. J. (2000). Respiratory Syncytial Virus G and/or SH Glycoproteins Modify CC and CXC Chemokine mRNA Expression in the BALB/c Mouse. J. Virol. 74: 6227-6229 [Abstract] [Full Text]  
  • Tripp, R. A., Moore, D., Winter, J., Anderson, L. J. (2000). Respiratory Syncytial Virus Infection and G and/or SH Protein Expression Contribute to Substance P, Which Mediates Inflammation and Enhanced Pulmonary Disease in BALB/c Mice. J. Virol. 74: 1614-1622 [Abstract] [Full Text]  
  • Sullender, W. M. (2000). Respiratory Syncytial Virus Genetic and Antigenic Diversity. Clin. Microbiol. Rev. 13: 1-15 [Abstract] [Full Text]  
  • Bembridge, G. P., Lopez, J. A., Bustos, R., Melero, J. A., Cook, R., Mason, H., Taylor, G. (1999). Priming with a Secreted Form of the Fusion Protein of Respiratory Syncytial Virus (RSV) Promotes Interleukin-4 (IL-4) and IL-5 Production but Not Pulmonary Eosinophilia following RSV Challenge. J. Virol. 73: 10086-10094 [Abstract] [Full Text]  
  • Johnson, T. R., Graham, B. S. (1999). Secreted Respiratory Syncytial Virus G Glycoprotein Induces Interleukin-5 (IL-5), IL-13, and Eosinophilia by an IL-4-Independent Mechanism. J. Virol. 73: 8485-8495 [Abstract] [Full Text]  
  • Tripp, R. A., Moore, D., Jones, L., Sullender, W., Winter, J., Anderson, L. J. (1999). Respiratory Syncytial Virus G and/or SH Protein Alters Th1 Cytokines, Natural Killer Cells, and Neutrophils Responding to Pulmonary Infection in BALB/c Mice. J. Virol. 73: 7099-7107 [Abstract] [Full Text]  
  • Srikiatkhachorn, A., Chang, W., Braciale, T. J. (1999). Induction of Th-1 and Th-2 Responses by Respiratory Syncytial Virus Attachment Glycoprotein Is Epitope and Major Histocompatibility Complex Independent. J. Virol. 73: 6590-6597 [Abstract] [Full Text]  
  • Feldman, S. A., Hendry, R. M., Beeler, J. A. (1999). Identification of a Linear Heparin Binding Domain for Human Respiratory Syncytial Virus Attachment Glycoprotein G. J. Virol. 73: 6610-6617 [Abstract] [Full Text]  
  • Fearon, D.T. (1999). Innate immunity and the biological relevance of the acquired immune response. QJM 92: 235-237 [Full Text]  
  • Hussell, T., Georgiou, A., Sparer, T. E., Matthews, S., Pala, P., Openshaw, P. J. M. (1998). Host Genetic Determinants of Vaccine-Induced Eosinophilia During Respiratory Syncytial Virus Infection. J. Immunol. 161: 6215-6222 [Abstract] [Full Text]  
  • Tebbey, P. W., Hagen, M., Hancock, G. E. (1998). Atypical Pulmonary Eosinophilia Is Mediated by a Specific Amino Acid Sequence of the Attachment (G) Protein of Respiratory Syncytial Virus. JEM 188: 1967-1972 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»