Steven M. Varga, PhD

Portrait
Director, Interdisciplinary Graduate Program in Immunology
Professor of Microbiology and Immunology
Professor of Pathology

Contact Information

Office
3-532 Bowen Science Building
51 Newton Rd
Iowa City, IA 52242
319-335-7784

Lab
3-501 Bowen Science Building
51 Newton Rd
Iowa City, IA 52242
319-335-8433

Education

BS, Biology, University of Notre Dame
PhD, Immunology, University of Massachusetts Medical School
Postdoctoral Fellow, Pulmonary Immunology, Beirne B. Carter Center for Immunology Research, University of Virginia

Education/Training Program Affiliations

Behavioral-Biomedical Interface Training Program, Biomedical Science Program, Department of Microbiology Graduate Program, Interdisciplinary Graduate Program in Immunology, Interdisciplinary Graduate Program in Translational Biomedicine, Medical Scientist Training Program

Center, Program and Institute Affiliations

Center for Immunology and Immune-based Diseases, Helen C. Levitt Center for Viral Pathogenesis, Holden Comprehensive Cancer Center

Research Summary

My laboratory is interested in studying the contribution of virus-specific T lymphocytes to enhanced disease and immunopathology during virus infection. Our laboratory studies the mouse model of respiratory syncytial virus (RSV) infection. RSV is the most common cause of bronchiolitis and pneumonia in young children worldwide. An experimental formalin-inactivated (FI) RSV vaccine developed in the United States during the 1960's led to exacerbated disease in vaccinated infants upon a subsequent natural infection. It is believed that the immune system was largely responsible for the enhanced disease exhibited by the children that received the FI-RSV vaccine. My laboratory is interested in understanding the underlying immunological causes that resulted in the the development of RSV vaccine-enhanced disease. We have recently made significant progress in defining the central role of CD4 T cells in mediating the FI-RSV vaccine-enhanced immunopathology.

We are currently studying the the role of tissue-resident memory T cells in providing protection against RSV infection. Humans experience repeated RSV infections throughout life due to the development of insufficient long-lived immunity. We are trying to gain a better understanding of why immunity to RSV is incomplete. The overall goal of our studies is to gain a better understanding of the immune determinants that lead to protection versus immunopathology so that safer and more effective vaccines can be developed in the future.

Publications

Schmidt, M. E., Varga, S. M. (2018). Cytokines and CD8 T cell immunity during respiratory syncytial virus infection. Cytokine, Epub ahead of print. PMID: 30031680.

Schmidt, M. E., Varga, S. M. (2018). The CD8 T Cell Response to Respiratory Virus Infections. Front Immunol, 9, 678. PMID: 29686673.

Schmidt, M. E., Knudson, C. J., Hartwig, S. M., Pewe, L. L., Meyerholz, D. K., Langlois, R. A., Harty, J. T. & Varga, S. M. (2018). Memory CD8 T cells mediate severe immunopathology following respiratory syncytial virus infection. PLoS Pathog, 14(1), e1006810. PMID: 29293660.

Schmidt, M. E., Oomens, A. G. & Varga, S. M. (2018). Single-cycle respiratory syncytial virus infection induces robust adaptive immune responses and reduces disease severity in mice. pp. Abstract no. 60.2. Immunology 2018.

Shan, Q., Zeng, Z., Xing, S., Li, F., Hartwig, S. M., Gullicksrud, J. A., Kurup, S. P., Van Braekel-Budimir, N., Su, Y., Martin, M. D., Varga, S. M., Taniuchi, I., Harty, J. T., Peng, W., Badovinac, V. P. & Xue, H. H. (2017). The transcription factor Runx3 guards cytotoxic CD8+ effector T cells against deviation towards follicular helper T cell lineage. Nat Immunol, 18(8), 931-939. PMID: 28604718.

Christiaansen, A. F., Dixit, U. G., Coler, R. N., Marie Beckmann, A., Reed, S. G., Winokur, P. L., Zimmerman, M. B., Varga, S. M. & Wilson, M. E. (2017). CD11a and CD49d enhance the detection of antigen-specific T cells following human vaccination. Vaccine, 35(33), 4255-4261. PMID: 28662951.

Christiaansen, A. F., Schmidt, M. E., Hartwig, S. M. & Varga, S. M. (2017). Host genetics play a critical role in controlling CD8 T cell function and lethal immunopathology during chronic viral infection. PLoS Pathog, 13(7), e1006498. PMID: 28715493.

Alsuwaidi, A. R., George, J. A., Almarzooqi, S., Hartwig, S. M., Varga, S. M. & Souid, A. K. (2017). Sirolimus alters lung pathology and viral load following influenza A virus infection. Respir Res, 18(1), 136. PMID: 28693498.

Schmidt, M. E., Varga, S. M. (2017). Modulation of the host immune response by respiratory syncytial virus proteins. J Microbiol., 55(3), 161-171. PMID: 28243940.

Slütter, B., Van Braeckel-Budimir, N., Abboud, G., Varga, S. M., Salek-Ardakani, S. & Harty, J. T. (2017). Dynamics of influenza-induced lung-resident memory T cells underlie waning heterosubtypic immunity. Sci Immunol, 2(7), eaag2031. PMID: 28783666.

Schmidt, M., Knudson, C., Hartwig, S., Pewe, L., Meyerholz, D., Langlois, R., Harty, J. & Varga, S. (2017). Resident memory CD8 T cells provide optimal protection against respiratory syncytial virus infection. pp. Abstract No. 153. 46th Annual Autumn Immunology Conference.

Christiaansen, A. F., Syed, M. A., Ten Eyck, P. P., Hartwig, S. M., Durairaj, L., Kamath, S. S. & Varga, S. M. (2016). Altered Treg and cytokine responses in RSV-infected infants. Pediatr Res, 80(5), 702-709. PMID: 27486703.

Hartwig, S. M., Ketterer, M., Apicella, M. A. & Varga, S. M. (2016). Non-typeable Haemophilus influenzae protects human airway epithelial cells from a subsequent respiratory syncytial virus challenge. Virology, 498, 128-35. PMID: 27573069.

Knudson, C. J., Weiss, K. A., Stoley, M. E. & Varga, S. M. (2016). Evaluation of the Adaptive Immune Response to Respiratory Syncytial Virus. Methods Mol Biol, 1442, 231-43. PMID: 27464699.

Knudson, C. J., Weiss, K. A. & Varga, S. M. (2016). Evaluation of the adaptive immune response to RSV. In R. A. Tripp , P. A. Jorquera (Eds.) Human Respiratory Syncytial Virus. Methods and Protocols. Humana Press.

Stoley, M. E., Knudson, C. J., Pewe, L. L., Meyerholz, D. K., Langlois, R. A., tenOever, B. R., Harty, J. T. & Varga, S. M. (2016). Memory CD8 T cells to RSV infection: friend or foe?. pp. Abstract No. 78.3. Immunology 2016.

Stoley, M., Knudson, C. J., Hartwig, S., Pewe, L., Meyerholz, D., Langlois, R., Harty, J. T. & Varga, S. M. (2016). Memory CD8 T cells mediate sever immunopathology following respiratory syncytial virus infection. pp. Abstract No. 35. 45th Annual Autumn Immunology Conference.

Christiaansen, A., Varga, S. M. & Spencer, J. V. (2015). Viral manipulation of the host immune response. Curr Opin Immunol, 36, 54-60. PMID: 26177523.

(2015). Inflammatory IL-15 is required for optimal memory T cell responses. J Clin Invest, 125(9), 3477-90. PMID: 26241055.

Knudson, C. J., Varga, S. M. (2015). CD8 T-cell response to respiratory syncytial virus infection. Future Virol, 10(6), 779-94. DOI: 10.2217/fvl.15.43.

Knudson, C. J., Hartwig, S. M., Meyerholz, D. K. & Varga, S. M. (2015). RSV vaccine-enhanced disease is orchestrated by the combined actions of distinct CD4 T cell subsets. PLoS Pathog, 11(3), e1004757. PMID: 25769044.

Stoley, M., Varga, S. M. (2015). Identification of respiratory syncytial virus T cell epitopes in C57BL/6 mice. pp. Abstract No. 140. 44th Annual Autumn Immunology Conference.

Christiaansen, A. F., Varga, S. M. (2015). MHC alleles influence CD8 T cell exhaustion and host survival during chronic viral infection. pp. Abstract No. 216.2. Immunology 2015.

Christiaansen, A. F., Varga, S. M. (2015). Profound impact of MHC heterogeneity on CD8 T cell exhaustion and host survival during chronic viral infection. pp. Abstract No. 1019. Keystone Conference Symposia: Viral Immunity.

Knudson, C. J., Varga, S. M. (2015). The relationship between respiratory syncytial virus and asthma. Vet Pathol, 52(1), 97-106. PMID: 24513802.

Christiaansen, A. F., Knudson, C. J., Weiss, K. A. & Varga, S. M. (2014). The CD4 T cell response to respiratory syncytial virus infection. Immunol Res, 59(1-3), 109-17. PMID: 24838148.

Knudson, C. J., Weiss, K. A., Hartwig, S. M. & Varga, S. M. (2014). The pulmonary localization of virus-specific T lymphocytes is governed by the tissue tropism of infection. J Virol, 88(16), 9010-6. PMID: 24899187.

Yang, K., Varga, S. M. (2014). Mucosal vaccines against respiratory syncytial virus. Curr Opin Virol, 6, 78-84. PMID: 24794644.

Christiaansen, A. F., Boggiatto, P. M. & Varga, S. M. (2014). Limitations of Foxp3+ Treg depletion following viral infection in DEREG mice. J Immunol Methods, 406, 58-65. PMID: 24642426.

Alsuwaidi, A. R., Albawardi, A., Almarzooqi, S., Benedict, S., Othman, A. R., Hartwig, S. M., Varga, S. M. & Souid, A. K. (2014). Respiratory syncytial virus increases lung cellular bioenergetics in neonatal C57BL/6 mice. Virology, 454-455, 263-9. PMID: 24725953.

Hartwig, S. M., Holman, K. M. & Varga, S. M. (2014). Depletion of Alveolar Macrophages Ameliorates Virus-Induced Disease following a Pulmonary Coronavirus Infection. PLoS One, 9(3), e90720. PMID: 24608125.

McDermott, D. S., Knudson, C. J. & Varga, S. M. (2014). Determining the breadth of the respiratory syncytial virus-specific T cell response. J Virol, 88(6), 3135-43. PMID: 24371055.

Weiss, K. A., Knudson, C. J., Christiaansen, A. F. & Varga, S. M. (2014). Animal Models of Human Respiratory Viral Infections. In S. K. Singh (Eds.) Human Respiratory Viral Infections. Taylor & Francis Group/CRC Press.

Knudson, C. J., Pewe, L. L., Gibson-Corley, K. N., Meyerholz, D. K., Harty, J. T. & Varga, S. M. (2014). Memory CD8 T cells provide protection against respiratory syncytial virus infection at the cost of severe pulmonary immunopathology. pp. Abstract No. 2018. Keystone Conference Symposia: Pathogenesis of Respiratory Viruses.

Syed, M., Christiaansen, A., Kamath, S., Morriss, F. & Varga, S. M. (2014). Role of T Regulatory Cells in Respiratory Syncytial Virus Infection. pp. Abstract No. 780. Society of Critical Care Medicine 43rd Critical Care Congress.

Christiaansen, A. F., Hartwig, S. M. & Varga, S. M. (2014). The innate immune response differentially regulates chronic viral infection in BALB/c versus C57BL/6 mice. pp. Abstract No. 1028. Keystone Conference Symposia: Innate Immunity to Viral Infections.

Knudson, C., Pewe, L., Meyerholz, D., Gibson-Corley, K., Langlois, R., tenOever, B., Harty, J. T. & Varga, S. M. (2014). Too much of a good thing: CD8 T cell memory to respiratory syncytial virus. pp. Abstract No. 143. 43rd Annual Autumn Immunology Conference.

Weiss, K. A., Knudson, C. J., Hartwig, S. M. & Varga, S. M. (2014). Viral tropism dictates the frequency of effector T cell migration into the lung tissue. pp. Abstract No. 3031. Keystone Conference Symposia: Pathogenesis of Respiratory Viruses.

Dersheid, R. j., Gallup, J. M., Knudson, C. J., Varga, S. M., Grosz, D. D., van Geelen, A., Hostetter, S. J. & Ackermann, M. R. (2013). Effects of Formalin-inactivated Respiratory Syncytial Virus (FI-RSV) in the Perinatal Lamb Model of RSV. PLoS One, 8(12), e81472. PMID: 24324695.

Fulton, R. B., Weiss, K. A., Pewe, L. L., Harty, J. T. & Varga, S. M. (2013). Aged Mice Exhibit a Severely Diminished CD8 T Cell Response following Respiratory Syncytial Virus Infection. J Virol, 87(23), 12694-700. PMID: 24049171.

Alsuwaidi, A. R., Almarzooqi, S., Albawardi, A., Benedict, S., Kochiyil, J., Mustafa, F., Hartwig, S. M., Varga, S. M. & Souid, A. K. (2013). Cellular bioenergetics, caspase activity and glutathione in murine lungs infected with influenza A virus. Virology, 446(1-2), 180-8. PMID: 24074580.

Alsuwaidi, A. R., Benedict, S., Kochiyil, J., Mustafa, F., Hartwig, S. M., Almarzooqi, S., Albawardi, A., Rizvi, T. A., Varga, S. M. & Souid, A. K. (2013). Bioenergetics of murine lungs infected with respiratory syncytial virus. Virol J, 10(1), 22. PMID: 23320837.

Alsuwaidi, A. R., Alsamri, M. T., Alfazari, A. S., Almarzooqi, S., Albawardi, A., Othman, A. R., Pramathan, T., Hartwig, S. M., Varga, S. M. & Souid, A. K. (2013). Lung tissue bioenergetics and caspase activity in rodents. BMC Res Notes, 6, 12. PMID: 23311890.

Klesney-Tait, J., Keck, K., Li, X., Gilfillan, S., Otero, K., Baruah, S., Meyerholz, D. K., Varga, S. M., Knudson, C. J., Moninger, T. O., Moreland, J., Zabner, J. & Colonna, M. (2013). Transepithelial migration of neutrophils into the lung requires TREM-1. J Clin Invest, 123(1), 138-49. PMID: 23241959.

Christiaansen, A. F., Boggiatto, P. M., Hartwig, S. M. & Varga, S. M. (2013). CD8 T cell exhaustion is influenced by genetic background. pp. Abstract No. 49.19. Immunology 2013.

McDermott, D. S., Varga, S. M. (2013). Critical role of PD-L2 in limiting pulmonary immunopathology during RSV infection. pp. Abstract No. 189.6. Immunology 2013.

Weiss, K. A., Fulton, R. B. & Varga, S. M. (2013). Diminished acute CD8 T cell responses with a similar memory response generated in aged mice following RSV infection. pp. Abstract No. 84. 42nd Annual Autumn Immunology Conference.

Knudson, C. J., Hartwig, S. M., Meyerholz, D. K. & Varga, S. M. (2013). Enhanced disease associated with formalin-inactivated respiratory syncytial virus vaccination is not dependent upon eosinophils. RSV Vaccines for the World.

Knudson, C., Gibson-Corley, K., Meyerholz, D. & Varga, S. M. (2013). Memory CD8 T cells provide protection against respiratory syncytial virus infection at the cost of severe pulmonary immunopathology. pp. Abstract No. 83. 42nd Annual Autumn Immunology Conference.

Whitmore, L. C., Hilkin, B. M., Goss, K. L., Wahle, E. M., Colaizy, T. T., Boggiatto, P. M., Varga, S. M., Miller, F. J. & Moreland, J. G. (2013). NOX2 Protects against Prolonged Inflammation, Lung Injury, and Mortality following Systemic Insults. J Innate Immun, 5(6), 565-80. PMID: 23635512.

Weiss, K. A., Varga, S. M. (2013). Respiratory syncytial virus strains induce differential innate immune and CD4 T cell responses. pp. Abstract No. 131.20. Immunology 2013.

Knudson, C. J., Hartwig, S. M., Meyerholz, D. K. & Varga, S. M. (2013). Th2-independent development of vaccine-enhanced disease associated with formalin-inactivated respiratory syncytial virus immunization. pp. Abstract No. 124.2. Immunology 2013.

Varga, S. M., Braciale, T. J. (2013). The adaptive immune response to respiratory syncytial virus. In B. S. Graham , L. J. Anderson (Eds.) Current Topics in Microbiology and Immunology: Challenges and opportunities for respiratory syncytial virus vaccines. pp. 155-71. Springer. PMID: 24362689.

Olson, M. R., McDermott, D. S. & Varga, S. M. (2012). The initial draining lymph node primes the bulk of the CD8 T cell response and influences memory T cell trafficking after a systemic viral infection. PLoS Pathog, 8(12), e1003054. PMID: 23236277.

Alsuwaidi, A. R., Benedict, S., Mustafa, F., Almarzooqi, S., Albawardi, A., Rizvi, T. A., Souid, A. K. & Varga, S. M. (2012). Bioenergetics of murine lung infected with respiratory syncytial virus. pp. Poster #16. 8th Annual Respiratory Syncytial Virus Symposium.

Ackermann, M., Grosz, D., Gallup, J., Van Geelen, A., Varga, S. M. & Dersheid, R. (2012). Effects of formalin-inactivated respiratory syncytial virus (FI-RSV) in the perinatal lamb model of RSV. pp. Poster #64. 8th Annual Respiratory Syncytial Virus Symposium.

Knudson, C. J., Hartwig, S. M., Meyerholz, D. K. & Varga, S. M. (2012). Eosinophils do not contribute to enhanced disease associated with formalin-inactivated respiratory syncytial virus vaccination. pp. Abstract No. 154. 41st Annual Autumn Immunology Conference.

Knudson, C. J., Hartwig, S. M., Meyerholz, D. K. & Varga, S. M. (2012). Eosinophils do not contribute to enhanced disease associated with formalin-inactivated respiratory syncytial virus vaccination. pp. Poster #63. 8th Annual Respiratory Syncytial Virus Symposium.

Weiss, K. A., Christiaansen, A. F., Fulton, R. B., Meyerholz, D. K. & Varga, S. M. (2012). Interleukin-10 limits RSV-induced disease severity by modulating the virus-specific T cell response. pp. Abstract No. 105.4. Immunology 2012.

Weiss, K., Varga, S. M. (2012). Respiratory syncytial virus strains induce differential innate immune responses. pp. Abstract No. 156. 41st Annual Autumn Immunology Conference.

Christiaansen, A. F., Weiss, K. A. & Varga, S. M. (2012). Role of interleukin-15 in Treg expansion following RSV infection. pp. Poster #54. 8th Annual Respiratory Syncytial Virus Symposium.

Weiss, K. A., Dudics, S. R. & Varga, S. M. (2012). The role of respiratory syncytial virus strain variation in the severity of virus-induced immunopathology. pp. Poster #74. 8th Annual Respiratory Syncytial Virus Symposium.

McDermott, D. S., Olson, M. R. & Varga, S. M. (2012). Virus-specific CD62L-memory CD8 T cells are preferentially retained in the draining lymph node following systemic viral infection. pp. Abstract No. 105.28. Immunology 2012.

McDermott, D. S., Varga, S. M. (2011). Quantifying antigen-specific CD4 T cells during a viral infection: CD4 T cell responses are larger than we think. J Immunol, 187(11), 5568-76. PMID: 22043009.

Weiss, K. A., Christiaansen, A. F., Fulton, R. B., Meyerholz, D. K. & Varga, S. M. (2011). Multiple CD4+ T cell subsets produce immunomodulatory IL-10 during respiratory syncytial virus infection. J Immunol, 187(6), 3145-54. PMID: 21844390.

McDermott, D. S., Weiss, K. A., Knudson, C. J. & Varga, S. M. (2011). Central role of dendritic cells in shaping the adaptive immune response during respiratory syncytial virus infection. Future Virol, 6(8), 963-973. PMID: 21887154.

Knudson, C., Varga, S. M. (2011). Eosinophils do not contribute to respiratory syncytial virus vaccine-enhanced disease parameters. pp. Abstract No. 145. 40th Annual Autumn Immunology Conference.

Weiss, K. A., Fulton, R. B. & Varga, S. M. (2011). Multiple CD4+ T cell subsets produce immunomodulatory IL-10 during acute respiratory syncytial virus infection. pp. Abstract No. 338. Keystone Conference Symposia: Immunity in the Respiratory Tract: Challenges of the Lung Environment.

Weiss, K., Christiaansen, A., Fulton, R., Meyerholz, D. & Varga, S. M. (2011). Multiple CD4+ T cell subsets produce interleukin-10 during RSV infection. pp. Abstract No. 146. 40th Annual Autumn Immunology Conference.

McDermott, D., Varga, S. M. (2011). Quantifying antigen-specific CD4 T cells during a viral infection: CD4 T cell responses are larger than we think. pp. Abstract No. 51. 40th Annual Autumn Immunology Conference.

Christiaansen, A., Varga, S. M. (2011). Role of pulmonary DC in modulating Treg expansion following RSV infection. pp. Abstract No. 115. 40th Annual Autumn Immunology Conference.

Boggiatto, P., Varga, S. M. (2011). Role of regulatory T cells during chronic LCMV infection. pp. Abstract No. 47. 40th Annual Autumn Immunology Conference.

Fulton, R. B., Meyerholz, D. K. & Varga, S. M. (2010). Foxp3+ CD4 regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J Immunol, 185(4), 2382-92. PMID: 20639494.

Groskreutz, D. J., Babor, E. C., Monick, M. M., Varga, S. M. & Hunninghake, G. W. (2010). Respiratory syncytial virus limits alpha subunit of eukaryotic translation initiation factor 2 (eIF2alpha) phosphorylation to maintain translation and viral replication. J Biol Chem, 285(31), 24023-31. PMID: 20519500.

Khanolkar, A., Fulton, R. B., Epping, L. L., Pham, N. L., Tifrea, D., Varga, S. M. & Harty, J. T. (2010). T cell epitope specificity and pathogenesis of mouse hepatitis virus-1-induced disease in susceptible and resistant hosts. J Immunol, 185(2), 1132-41. PMID: 20554960.

Fulton, R. B., Varga, S. M. (2010). Editorial: CD8 T cells cut back on calcium intake in the lungs. (Vols. 87). (6), pp. 961-4. J Leukoc Biol. PMID: 20515917.

Weiss, K. A., Fulton, R. B. & Varga, S. M. (2010). Determining the role of interleukin-10 during respiratory syncytial virus infection. pp. Abstract No. 166. 39th Annual Autumn Immunology Conference.

McDermott, D., Varga, S. M. (2010). Establishing the specificity of the entire RSV-specific T cell response. pp. Abstract No. 1397. 7th International Respiratory Syncytial Virus Symposium.

McDermott, D., Varga, S. M. (2010). Examining the specificity of the entire RSV-specific T cell response. pp. Abstract No. 164. 39th Annual Autumn Immunology Conference.

Knudson, C., McDermott, D. & Varga, S. M. (2010). Formalin-inactivation of respiratory syncytial virus alters native T cell epitopes. pp. Abstract No. 165. 39th Annual Autumn Immunology Conference.

Fulton, R. B., Varga, S. M. (2010). Foxp3+ CD4 regulatory T cells limit the magnitude of pulmonary immunopathology following acute respiratory syncytial virus infection. pp. Abstract No. 207. Keystone Symposium: Viral Immunity.

McDermott, D. S., Varga, S. M. (2010). Quantifying the magnitude of antigen-specific CD4 T cell responses. pp. Abstract No. 39.27. Immunology 2010.

Fulton, R. B., Varga, S. M. (2009). Effects of aging on the adaptive immune response to respiratory virus infections. Aging Health, 5(6), 775-87. PMID: 20174457.

Khanolkar, A., Hartwig, S. M., Haag, B. A., Meyerholz, D., Epping, L. L., Haring, J. S., Varga, S. M. & Harty, J. T. (2009). Protective and pathologic roles of the immune response to mouse hepatitis virus type 1: implications for severe acute respiratory syndrome. J Virol, 83(18), 9258-72. PMID: 19570864.

Khanolkar, A., Hartwig, S. M., Haag, B. A., Meyerholz, D., Harty, J. T. & Varga, S. M. (2009). Toll-like receptor 4 deficiency increases disease and mortality after mouse hepatitis virus type 1 infection of susceptible C3H mice. J Virol, 83(17), 8946-56. PMID: 19553337.

Groskreutz, D. J., Monick, M. M., Babor, E. C., Nyunoya, T., Varga, S. M., Look, D. C. & Hunninghake, G. W. (2009). Cigarette smoke alters respiratory syncytial virus-induced apoptosis and replication. Am J Respir Cell Mol Biol, 41(2), 189-98. PMID: 19131644.

Olivier, A., Gallup, J., de Macedo, M. M., Varga, S. M. & Ackermann, M. (2009). Human respiratory syncytial virus A2 strain replicates and induces innate immune responses by respiratory epithelia of neonatal lambs. Int J Exp Pathol, 90(4), 431-8. PMID: 19659901.

Meyerholz, D., Rodgers, J., Castilow, E. M. & Varga, S. M. (2009). Alcian Blue and Pyronine Y histochemical stains permit assessment of multiple parameters in pulmonary disease models. Vet Pathol, 46(2), 325-8. PMID: 19261646.

Olson, M. R., Varga, S. M. (2009). Fas ligand is required for the development of respiratory syncytial virus vaccine-enhanced disease. J Immunol, 182(5), 3024-31. PMID: 19234198.

Meyerholz, D., Griffin, M. A., Castilow, E. M. & Varga, S. M. (2009). Comparison of histochemical methods for murine eosinophil detection in an RSV vaccine-enhanced inflammation model. Toxicol Pathol, 37(2), 249-55. PMID: 19181630.

McDermott, D., Olson, M. & Varga, S. M. (2009). Draining lymph nodes exhibited altered recruitment of CD62L+ memory CD8 T cell. pp. Abstract No. 165. 38th Annual Autumn Immunology Conference.

Varga, S. M. (2009). Fixing a failed vaccine. (Vols. 15). (1), pp. 21-2. Nat Med. PMID: 19129777.

Khanolkar, A., Hartwig, S. M., Pewe, L. L., Varga, S. M. & Harty, J. (2009). Protective and pathologic roles of the immune response to mouse hepatitis virus-1: implications for severe acute respiratory syndrome. pp. Abstract No. 128.8. Immunology 2009.

Fulton, R. B., Olson, M. R. & Varga, S. M. (2009). Regulation of cytokine production by virus-specific T cells in the lungs. pp. Abstract No. 157. Keystone Symposium: Immunologic Memory and Host Defense.

Groskreutz, D. J., Monick, M. M., Babor, E. C., Varga, S. M. & Hunninghake, G. W. (2009). RSV Uses EGFR for viral replication. pp. Abstract No. 55. Central Society for Clinical Research/Midwestern Section American Federation for Medical Research.

Fulton, R., Varga, S. M. (2009). The regulatory CD4 T cell response to respiratory syncytial virus. pp. Abstract No. 163. 38th Annual Autumn Immunology Conference.

Haag, B. A., Hartwig, S. M., Khanolkar, A., Harty, J. T. & Varga, S. M. (2009). TLR4-deficient C3H/HeJ mice exhibit enhanced disease and mortality following intranasal MHV-1 infection. pp. Abstract No. 44.23. Immunology 2009.

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(11), 7958-68. PMID: 19017987.

Castilow, E. M., Legge, K. L. & Varga, S. M. (2008). Cutting edge: Eosinophils do not contribute to respiratory syncytial virus vaccine-enhanced disease. J Immunol, 181(10), 6692-6. PMID: 18981084.

Olson, M. R., Varga, S. M. (2008). Pulmonary immunity and immunopathology: lessons from respiratory syncytial virus. Expert Rev Vaccines, 7(8), 1239-55. PMID: 18844597.

Fulton, R. B., Olson, M. R. & Varga, S. M. (2008). Regulation of cytokine production by virus-specific CD8 T cells in the lungs. J Virol, 82(16), 7799-811. PMID: 18524828.

Castilow, E. M., Olson, M. R., Meyerholz, D. & 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(5), 2196-207. PMID: 18094193.

Wissinger, E. L., Stevens, W. W., Varga, S. M. & Braciale, T. J. (2008). Proliferative expansion and acquisition of effector activity by memory CD4+ T cells in the lungs following pulmonary virus infection. J Immunol, 180(5), 2957-66. PMID: 18292518.

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(4), 2376-84. PMID: 18250447.

Meyerholz, D. K., Rodgers, J. R., Castilow, E. M. & Varga, S. M. (2008). Alcian blue and pyronine Y histochemical stains of paraffin embedded sections provide multi-parameter morphological assessment in experimental models of pulmonary disease. pp. Abstract No. 710.2. Experimental Biology 2008.

Groskreutz, G., Monick, M. M., Barton, J., Babor, E., Varga, S. M., Look, D. & Hunninghake, G. W. (2008). Cigarette smoke extract converts RSV-induced apoptosis to necrosis, potentiating viral replication and local inflammation. pp. Mini Symposium Session C91. American Thoracic Society International Conference.

Fulton, R. B., Olson, M. R. & Varga, S. M. (2008). Inadequate stimulation by tissue APC dictates the effector functions of virus-specific CD8 T cells in the lung. pp. Abstract No. 160. Keystone Symposium: Viral Immunity.

Castilow, E. M., Varga, S. M. (2008). Overcoming T cell-mediated immunopathology to achieve safe RSV vaccination. Future Virol, 3(5), 445-454. PMID: 19057653.

Olson, M. R., Varga, S. M. (2008). Priming of CD8 T cells in the lymph nodes results in accelerated memory development after LCMV infection. pp. Abstract No. 302. Keystone Symposium: Viral Immunity.

Khanolkar, A., Hartwig, S., Pewe, L., Varga, S. M. & Harty, J. (2008). Protective and pathologic roles of the immune response to mouse hepatitis virus-1 (MHV-1): implications for severe acute respiratory syndrome. pp. Abstract No. 48. 37th Annual Autumn Immunology Conference.

Castilow, E. M., Varga, S. M. (2008). Separation of pulmonary and systemic aspects of respiratory syncytial virus vaccine-enhanced disease. pp. Abstract No. 857.20. Experimental Biology 2008.

Haag, B., Hartwig, S., Khanolkar, A., Harty, J. & Varga, S. M. (2008). TLR4-deficient C3H/HeJ mice exhibit enhanced disease following intranasal MHV-1 infection. pp. Abstract No. 47. 37th Annual Autumn Immunology Conference.

Olson, M. R., Varga, S. M. (2007). CD8 T cells inhibit respiratory syncytial virus (RSV) vaccine-enhanced disease. J Immunol, 179(8), 5415-24. PMID: 17911628.

Groskreutz, D. J., Monick, M., Yarovinsky, T. O., Powers, L. S., Quelle, D. E., Varga, S. M., Look, D. C. & Hunninghake, G. W. (2007). Respiratory syncytial virus decreases p53 protein to prolong survival of airway epithelial cells. J Immunol, 179(5), 2741-7. PMID: 17709487.

Monick, M. M., Powers, L. S., Hassan, I., Groskreutz, D., Yarovinsky, T. O., Barrett, C. W., Castilow, E. M., Tifrea, D., Varga, S. M. & Hunninghake, G. W. (2007). Respiratory syncytial virus synergizes with Th2 cytokines to induce optimal levels of TARC/CCL17. J Immunol, 179(3), 1648-58. PMID: 17641031.

Olson, M. R., Varga, S. M. (2007). Accelerated memory CD8 T cell phenotype in the peritoneal cavity. pp. Abstract No. 304. Keystone Symposium: Immunologic Memory.

Olson, M. R., Varga, S. M. (2007). Accelerated T memory development in the peritoneal cavity. (Vols. 178). pp. Abstract No. 85.24. J Immunol.

Olson, M. R., Varga, S. M. (2007). Differential ability of RSV F- and M2-specific CD8 T cells to modulate respiratory syncytial virus (RSV) vaccine-enhanced disease. pp. Abstract No. 80. 6th International Respiratory Syncytial Virus Symposium.

Castilow, E. M., Varga, S. M. (2007). Differential roles of STAT4 and STAT6 during respiratory syncytial virus vaccine-enhanced disease. pp. Abstract No. 51. 36th Annual Autumn Immunology Conference.

Fulton, R. B., Varga, S. M. (2007). Functional impairment of CD8 T cells following acute virus infections. (Vols. 178). pp. Abstract No. 43.32. J Immunol.

Castilow, E. M., Varga, S. M. (2007). IL-13 is required for respiratory syncytial virus vaccine-induced pulmonary eosinophilia. pp. Abstract No. 87. 6th International Respiratory Syncytial Virus Symposium.

Castilow, E. M., Varga, S. M. (2007). Respiratory syncytial virus vaccine-enhanced pulmonary eosinophilia requires IL-13, IL-4Ra, and STAT6. (Vols. 178). pp. Abstract No. 96.6. J Immunol.

Castilow, E. M., Olson, M. R. & Varga, S. M. (2007). Understanding respiratory syncytial virus (RSV) vaccine-enhanced disease. Immunol Res, 39(1-3), 225-39. PMID: 17917067.

Ramaswamy, M., Shi, L., Varga, S. M., Barik, S., Behlke, M. A. & Look, D. C. (2006). Respiratory syncytial virus nonstructural protein 2 specifically inhibits type I interferon signal transduction. Virology, 344(2), 328-39. PMID: 16216295.

Olson, M. R., Varga, S. M. (2006). CD8 T cell inhibition of RSV vaccine-enhanced disease. pp. Abstract No. 46. 35th Annual Autumn Immunology Conference.

Olson, M. R., Varga, S. M. (2006). CD8 T cell modulation of respiratory syncytial virus (RSV) vaccine-enhanced disease. (Vols. 176). pp. S117, Abstract No. 59.6. J Immunol.

Fulton, R. B., Varga, S. M. (2006). Cytokine impairment of pulmonary CD8 T cells following respiratory viral infections. pp. Abstract No. 48. 35th Annual Autumn Immunology Conference.

Castilow, E. M., Olson, M. R. & Varga, S. M. (2006). IFN-? modulates RSV vaccine-enhanced disease mediated by RSV F protein-specific CD4 T cells. (Vols. 176). pp. S89, Abstract No. 55.27. J Immunol.

Castilow, E. M., Varga, S. M. (2006). IL-13 is required for respiratory syncytial virus vaccine-enhanced pulmonary eosinophilia. pp. Abstract No. 22. 35th Annual Autumn Immunology Conference.

Haring, J. S., Badovinac, V., Olson, M. R., Varga, S. M. & Harty, J. T. (2005). In vivo generation of pathogen-specific Th1 cells in the absence of the IFN-gamma receptor. J Immunol, 175(5), 3117-22. PMID: 16116201.

Olson, M. R., Varga, S. M. (2005). CD8 T cell inhibition of RSV vaccine-enhanced disease. pp. Abstract No. 161. 34th Annual Autumn Immunology Conference.

Olson, M. R., Varga, S. M. (2005). CD8 T cell inhibition of RSV vaccine-enhanced disease. (Vols. 19). (4), pp. A396, Abstract No. 261.20. FASEB J.

Olson, M. R., Varga, S. M. (2005). CD8 T cell inhibition of RSV vaccine-enhanced disease. pp. Abstract No. PII=18. RSV Symposium 2005.

Castilow, E. M., Varga, S. M. (2005). Identification of a CD4 T cell epitope within the fusion protein of RSV. pp. Abstract No. 45. 34th Annual Autumn Immunology Conference.

Fischer, A. J., Wohlford-Lenane, C. L., Sinn, P. L., Jia, H. P., Varga, S. M., Davidson, B. L. & McCray, P. B. (2005). RNAi Applications for respiratory epithelia: delivery and efficacy. pp. S317. Molecular Therapy.

Ramaswamy, M., Shi, L., Barik, S. M., Varga, S. M., Hunninghake, G. W. & Look, D. C. (2005). RSV Nonstructural Protein NS2 inhibits Stat2 expression and type 1 interferon-dependent gene expression. (Vols. 2). pp. A261. Proc Am Thor Soc.

Ramaswamy, M., Shi, L., Varga, S. M., Barik, S., Hunninghake, G. W. & Look, D. C. (2005). RSV nonstructural Protein NS2 inhibits type 1 interferon-dependent gene expression by decreasing STAT2 levels. pp. Abstract No. II-1. RSV Symposium 2005.

Varga, S. M. (2005). The role of IL-13 in RSV vaccine-enhanced disease induced by immunization with the attachment (G) protein. (Vols. 19). (4), pp. A408, Abstract No. 261.77. FASEB J.

Johnson, T. R., Varga, S. M., Braciale, T. J. & Graham, B. S. (2004). Vß14+ 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(16), 8753-60. PMID: 15280483.

Olson, M. R., Varga, S. M. (2004). CD8 T cell modulation of RSV vaccine-enhanced disease. pp. Abstract No. 47. 33rd Annual Autumn Immunology Conference.

Wissinger, E. L., Varga, S. M. & Braciale, T. J. (2004). Migration, proliferation, and differentiation of memory G-specific CD4+ T cells following experimental murine RSV infection. pp. Abstract No. LS-33. 12th International Congress of Immunology.

Wissinger, E. L., Varga, S. M. & Braciale, T. J. (2004). Recruitment and proliferation of effector memory CD4+ T cells following experimental murine RSV infection. (Vols. 18). (5), pp. A804, Abstract No. 554.21. FASEB J.

Wissinger, E. L., Varga, S. M. & Braciale, T. J. (2003). Lung infiltration and subsequent proliferation of RSV G-specific memory CD4+ T cells following experimental murine RSV infection. pp. Abstract No. PVIII-23. RSV Symposium 2003.

Wissinger, E. L., Varga, S. M. & Braciale, T. J. (2003). Proliferation and effector activity of memory CD4+ T cells in the lung following experimental murine RSV infection. (Vols. 17). (7), pp. C163, Abstract No. 80.8. FASEB J.

Johnson, T. R., Varga, S. M., Braciale, T. J. & Graham, B. S. (2003). Respiratory syncytial virus (RSV) G-induced vaccine enhanced disease, but not FI-RSV-induced disease, is mediated by Vß14+ T cells. (Vols. 17). (7), pp. C18, Abstract No. 31.14. FASEB J.

Varga, S. M., Braciale, T. J. (2002). RSV-induced immunopathology: dynamic interplay between the virus and host immune response. Virology, 295(2), 203-7. PMID: 12033778.

Varga, S. M., Beckman, N. A., Chu, M. & Braciale, T. J. (2002). Sensitive detection and quantitation of mouse eosinophils in tissues using an enzymatic eosinophil peroxidase assay: its use to rapidly measure pulmonary eosinophilia during experimental respiratory syncytial virus infection of mice. J Immunol Methods, 262(1-2), 111-20. PMID: 11983224.

Varga, S. M., Braciale, T. J. (2002). The role of IL-4 and IL-13 in RSV vaccine-enhanced disease induced by immunization with the attachment (G) protein. (Vols. 16). (5), pp. A1040, Abstract No. 758.5. FASEB J.

Varga, S. M., Braciale, T. J. (2002). The role of IL-4R in RSV vaccine-enhanced disease induced by immunization with the attachment (G) protein. pp. Abstract No. 62. ASM Conference on Immunity to Bacterial, Viral, and Protozoal Pathogens.

Varga, S. M., Wang, X., Welsh, R. M. & Braciale, T. J. (2001). Immunopathology in RSV infection is mediated by a discrete oligoclonal subset of antigen-specific CD4+ T cells. Immunity, 15(4), 637-46. PMID: 11672545.

Varga, S. M., Selin, L. K. & Welsh, R. M. (2001). Independent regulation of lymphocytic choriomeningitis virus-specific T cell memory pools: relative stability of CD4 memory under conditions of CD8 memory T cell loss. J Immunol, 166(3), 1554-61. PMID: 11160196.

Wassinger, E. L., Varga, S. M. & Braciale, T. J. (2001). Recruitment of effector CD4 T cells to the lungs during experimental murine RSV infection. (Vols. 15). (4), pp. A682, Abstract No. 529.20. FASEB J.

Wissinger, E. L., Varga, S. M. & Braciale, T. J. (2001). Recruitment of effector CD4 T cells to the lungs during experimental murine RSV infection. pp. Abstract No. 233. Keystone Symposium: Molecular Aspects of Viral Immunity.

Varga, S. M., Wang, X., Welsh, R. M. & Braciale, T. J. (2001). RSV G-enhanced immunopathology is mediated by a discrete subset of CD4+ T cells with limited TCR diversity. pp. Abstract No. 3.24. RSV After 45 Years.

Braciale, T. J., Varga, S. M. (2001). T lymphocyte effector activity. In K. F. Austen , M. M. Frank (Eds.) Samter's immunological diseases. (6th edition), pp. 195-205. Lippincott Williams & Wilkins.

Varga, S. M., Braciale, T. J. (2001). The role of Vß14+ CD4 T cells in mediating respiratory syncytial virus vaccine-enhanced lung disease. pp. Abstract No. 330. Keystone Symposium: Molecular Aspects of Viral Immunity.

Varga, S. M., Braciale, T. J. (2001). The role of Vß14+ CD4 T cells in the development of immune-mediated pathology during experimental respiratory syncytial virus infection. (Vols. 15). (4), pp. A304, Abstract No. 266.5. FASEB J.

Varga, S. M., Wissinger, E. L. & Braciale, T. J. (2000). The attachment (G) glycoprotein of respiratory syncytial virus contains a single immunodominant epitope that elicits both Th1 and Th2 CD4+ T cell responses. J Immunol, 165(11), 6487-95. PMID: 11086089.

Varga, S. M., Welsh, R. M. (2000). High frequency of virus-specific interleukin-2-producing CD4+ T cells and Th1 dominance during lymphocytic choriomeningitis virus infection. J Virol, 74(9), 4429-32. PMID: 10756059.

Varga, S. M., Wissinger, E. L. & Braciale, T. J. (2000). CD4 T cells directed to the RSV attachment glycoprotein recognize a single dominant epitope and utilize a highly restricted Vß repertoire. (Vols. 14). (6), pp. A1039, Abstract No. 93.16. FASEB J.

Selin, L. K., Lin, M. Y., Varga, S. M. & Welsh, R. M. (2000). CD8 memory to viruses and the T cell network. In M. V. Sitkovsky , P. A. Henkart (Eds.) Cytotoxic cells: basic mechanisms and medical applications. pp. 327-62. Lippincott Williams & Wilkins.

Selin, L. K., Lin, M. Y., Kraemer, K. A., Pardoll, D. M., Schneck, J. P., Varga, S. M., Santolucito, P. A., Pinto, A. K. & Welsh, R. M. (1999). Attrition of T cell memory: selective loss of LCMV epitope-specific memory CD8 T cells following infections with heterologous viruses. Immunity, 11(6), 733-42. PMID: 10626895.

Varga, S. M., Selin, L. K. & Welsh, R. M. (1999). Resistance of virus-specific CD4 T cell precursors to deletion by heterologous viruses. (Vols. 13). (5), pp. A978, Abstract No. 712.5. FASEB J.

Selin, L. K., Varga, S. M., Wong, I. C. & Welsh, R. M. (1998). Protective heterologous antiviral immunity and enhanced immunopathogenesis mediated by memory T cell populations. J Exp Med, 188(9), 1705-15. PMID: 9802982.

Varga, S. M., Welsh, R. M. (1998). Detection of a high frequency of virus-specific CD4+ T cells during acute infection with lymphocytic choriomeningitis virus. J Immunol, 161(7), 3215-8. PMID: 9759834.

Varga, S. M., Welsh, R. M. (1998). Stability of virus-specific CD4+ T cell frequencies from acute infection into long term memory. J Immunol, 161(1), 367-74. PMID: 9647245.

Varga, S. M., Welsh, R. M. (1998). Remarkable stability of virus-specific CD4+ T cell frequencies from acute infection into long term memory. (Vols. 12). (4), pp. A614, Abstract No. 3566. FASEB J.

Varga, S. M., Welsh, R. M. (1998). Stability of virus-specific CD4+ T cell frequencies from acute infection into long term memory. pp. Abstract No. 342. Keystone Symposium: Molecular Aspects of Viral Immunity.

Welsh, R. M., Lin, M. Y., Lohman, B. L., Varga, S. M., Zarozinski, C. C. & Selin, L. K. (1997). Alpha beta and gamma delta T-cell networks and their roles in natural resistance to viral infections. Immunol Rev, 159, 79-93. PMID: 9416504.

Varga, S. M., Welsh, R. M. (1997). Stability of virus-specific CD4+ T cell frequencies from acute infection into long term memory. pp. Abstract No. D6. XXIII New England Immunology Conference Program and Poster Session Abstracts.

Welsh, R. M., Tay, C. H., Varga, S. M., O'Donnell, C. L., Vergilis, K. L. & Selin, L. K. (1996). Lymphocyte-dependent 'natural' immunity to virus infections mediated by both natural killer cells and memory T cells. Semin Virol, 7(2), 95-102.

Varga, S. M., Welsh, R. M. (1996). The CD45RB-associated epitope defined by monoclonal antibody CZ-1 is an activation and memory marker for mouse CD4 T cells. Cell Immunol, 167(1), 56-62. PMID: 8548845.

Varga, S. M., Selin, L. K. & Welsh, R. M. (1996). Enhanced T cell cytokine Production in immune mice challenged with heterologous viruses. (Vols. 10). (6), pp. A1318, Abstract No. 1836. FASEB J.

Varga, S. M., Vergilis, K. L., Welsh, R. M. & Selin, L. K. (1995). Heterologous T cell-mediated immunity to viral infections. pp. Abstract No. 26. XXI New England Immunology Conference Program and Poster Session Abstracts.