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 Borgland, S. L.
Right arrow Articles by Muruve, D. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Borgland, S. L.
Right arrow Articles by Muruve, D. A.

 Previous Article  |  Next Article 

Journal of Virology, May 2000, p. 3941-3947, Vol. 74, No. 9
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Adenovirus Vector-Induced Expression of the C-X-C Chemokine IP-10 Is Mediated through Capsid-Dependent Activation of NF-kappa B

Stephanie L. Borgland,1 Gloria P. Bowen,1 Norman C. W. Wong,1 Towia A. Libermann,2 and Daniel A. Muruve1,*

Department of Medicine, University of Calgary, Calgary, Alberta, Canada,1 and Department of Medicine, Beth Israel Deaconess Medical Center, Harvard University, Boston, Massachusetts2

Received 25 October 1999/Accepted 28 January 2000

The use of adenovirus vectors for gene therapy has been limited by well-defined cellular and humoral immune responses. We have previously shown that adenovirus vectors rapidly induce the expression of the C-X-C chemokine, interferon-inducible protein 10 (IP-10), in vivo. Various first-generation, type 5 adenovirus vectors, including adCMVbeta gal and UV-psoralen-inactivated adenovirus, equally induced the expression of IP-10 mRNA as early as 3 h following infection in mouse renal epithelial cells (REC). Luciferase reporter experiments using deletional mutants of the murine IP-10 5'-flanking region revealed that transcriptional activation of the IP-10 promoter by adCMVbeta gal was dependent on the -161- to -96-bp region upstream of the transcription start site. In electrophoretic mobility shift assays, adCMVbeta gal, adCMV-GFP, FG140, and transcription-defective adenovirus induced protein binding to oligonucleotides containing a consensus sequence for NF-kappa B at position -113 of the IP-10 promoter. Supershift assays confirmed an increase in binding activity of NF-kappa B p65 but not p50 or cRel in REC cells infected with various replication-deficient adenoviruses. Coinfection of REC cells with adCMVbeta gal and an adenoviral vector expressing Ikappa Balpha resulted in suppression of adCMVbeta gal-induced expression of IP-10 at 6 and 16 h, further strengthening the conclusion that adenovirus-induced activation of IP-10 is dependent on NF-kappa B. The induction of IP-10 appeared to be direct because infection with adenovirus vectors failed to induce the expression of the potent IP-10 stimulators, interferon gamma and tumor necrosis factor alpha. Together, these findings demonstrate that adenovirus vectors directly induce the expression of IP-10 through capsid dependent activation of NF-kappa B.


* Corresponding author. Mailing address: Faculty of Medicine, University of Calgary, 3330 Hospital Dr., NW, Calgary, Alberta T2N 4N1, Canada. Phone: (403) 220-8867. Fax: (403) 270-0979. E-mail: dmuruve{at}ucalgary.ca.


Journal of Virology, May 2000, p. 3941-3947, Vol. 74, No. 9
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Sinn, P. L., Arias, A. C., Brogden, K. A., McCray, P. B. Jr. (2008). Lentivirus Vector Can Be Readministered to Nasal Epithelia without Blocking Immune Responses. J. Virol. 82: 10684-10692 [Abstract] [Full Text]  
  • Appledorn, D. M., Patial, S., McBride, A., Godbehere, S., Van Rooijen, N., Parameswaran, N., Amalfitano, A. (2008). Adenovirus Vector-Induced Innate Inflammatory Mediators, MAPK Signaling, As Well As Adaptive Immune Responses Are Dependent upon Both TLR2 and TLR9 In Vivo. J. Immunol. 181: 2134-2144 [Abstract] [Full Text]  
  • Bunting, K., Rao, S., Hardy, K., Woltring, D., Denyer, G. S., Wang, J., Gerondakis, S., Shannon, M. F. (2007). Genome-Wide Analysis of Gene Expression in T Cells to Identify Targets of the NF-{kappa}B Transcription Factor c-Rel. J. Immunol. 178: 7097-7109 [Abstract] [Full Text]  
  • Tomasec, P., Wang, E. C. Y., Groh, V., Spies, T., McSharry, B. P., Aicheler, R. J., Stanton, R. J., Wilkinson, G. W. G. (2007). Adenovirus vector delivery stimulates natural killer cell recognition. J. Gen. Virol. 88: 1103-1108 [Abstract] [Full Text]  
  • Tamanini, A., Nicolis, E., Bonizzato, A., Bezzerri, V., Melotti, P., Assael, B. M., Cabrini, G. (2006). Interaction of Adenovirus Type 5 Fiber with the Coxsackievirus and Adenovirus Receptor Activates Inflammatory Response in Human Respiratory Cells. J. Virol. 80: 11241-11254 [Abstract] [Full Text]  
  • Miller-Jensen, K., Janes, K. A., Wong, Y.-L., Griffith, L. G., Lauffenburger, D. A. (2006). Adenoviral vector saturates Akt pro-survival signaling and blocks insulin-mediated rescue of tumor-necrosis-factor-induced apoptosis. J. Cell Sci. 119: 3788-3798 [Abstract] [Full Text]  
  • Boodoo, S., Spannhake, E. W., Powell, J. D., Horton, M. R. (2006). Differential regulation of hyaluronan-induced IL-8 and IP-10 in airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 291: L479-L486 [Abstract] [Full Text]  
  • Delgado-Lopez, F., Horwitz, M. S. (2006). Adenovirus RID{alpha}{beta} Complex Inhibits Lipopolysaccharide Signaling without Altering TLR4 Cell Surface Expression.. J. Virol. 80: 6378-6386 [Abstract] [Full Text]  
  • Liu, Q., White, L. R., Clark, S. A., Heffner, D. J., Winston, B. W., Tibbles, L. A., Muruve, D. A. (2005). Akt/Protein Kinase B Activation by Adenovirus Vectors Contributes to NF{kappa}B-Dependent CXCL10 Expression. J. Virol. 79: 14507-14515 [Abstract] [Full Text]  
  • Harvey, S. A. K., Romanowski, E. G., Yates, K. A., Gordon, Y. J. (2005). Adenovirus-Directed Ocular Innate Immunity: The Role of Conjunctival Defensin-like Chemokines (IP-10, I-TAC) and Phagocytic Human Defensin-{alpha}. IOVS 46: 3657-3665 [Abstract] [Full Text]  
  • Shayakhmetov, D. M., Li, Z.-Y., Ni, S., Lieber, A. (2005). Interference with the IL-1-Signaling Pathway Improves the Toxicity Profile of Systemically Applied Adenovirus Vectors. J. Immunol. 174: 7310-7319 [Abstract] [Full Text]  
  • Foley, J. F., Yu, C.-R., Solow, R., Yacobucci, M., Peden, K. W. C., Farber, J. M. (2005). Roles for CXC Chemokine Ligands 10 and 11 in Recruiting CD4+ T Cells to HIV-1-Infected Monocyte-Derived Macrophages, Dendritic Cells, and Lymph Nodes. J. Immunol. 174: 4892-4900 [Abstract] [Full Text]  
  • Cuevas, J. M., Moya, A., Sanjuan, R. (2005). Following the very initial growth of biological RNA viral clones. J. Gen. Virol. 86: 435-443 [Abstract] [Full Text]  
  • Shayakhmetov, D. M., Eberly, A. M., Li, Z.-Y., Lieber, A. (2005). Deletion of Penton RGD Motifs Affects the Efficiency of both the Internalization and the Endosome Escape of Viral Particles Containing Adenovirus Serotype 5 or 35 Fiber Knobs. J. Virol. 79: 1053-1061 [Abstract] [Full Text]  
  • Kohrgruber, N., Groger, M., Meraner, P., Kriehuber, E., Petzelbauer, P., Brandt, S., Stingl, G., Rot, A., Maurer, D. (2004). Plasmacytoid Dendritic Cell Recruitment by Immobilized CXCR3 Ligands. J. Immunol. 173: 6592-6602 [Abstract] [Full Text]  
  • Shayakhmetov, D. M., Li, Z.-Y., Ni, S., Lieber, A. (2004). Analysis of Adenovirus Sequestration in the Liver, Transduction of Hepatic Cells, and Innate Toxicity after Injection of Fiber-Modified Vectors. J. Virol. 78: 5368-5381 [Abstract] [Full Text]  
  • Collins, S. E., Noyce, R. S., Mossman, K. L. (2004). Innate Cellular Response to Virus Particle Entry Requires IRF3 but Not Virus Replication. J. Virol. 78: 1706-1717 [Abstract] [Full Text]  
  • Chung, S.-W., Arnott, J. A., Yang, Y., Wong, P. M. C. (2003). Presence of Prepackaged mRNA in Virions of DNA Adenovirus. J. Biol. Chem. 278: 50635-50640 [Abstract] [Full Text]  
  • Stilwell, J. L., McCarty, D. M., Negishi, A., Superfine, R., Samulski, R. J. (2003). Development and Characterization of Novel Empty Adenovirus Capsids and Their Impact on Cellular Gene Expression. J. Virol. 77: 12881-12885 [Abstract] [Full Text]  
  • Molinier-Frenkel, V., Prevost-Blondel, A., Hong, S.-S., Lengagne, R., Boudaly, S., Magnusson, M. K., Boulanger, P., Guillet, J.-G. (2003). The Maturation of Murine Dendritic Cells Induced by Human Adenovirus Is Mediated by the Fiber Knob Domain. J. Biol. Chem. 278: 37175-37182 [Abstract] [Full Text]  
  • Vanbervliet, B., Bendriss-Vermare, N., Massacrier, C., Homey, B., de Bouteiller, O., Briere, F., Trinchieri, G., Caux, C. (2003). The Inducible CXCR3 Ligands Control Plasmacytoid Dendritic Cell Responsiveness to the Constitutive Chemokine Stromal Cell-derived Factor 1 (SDF-1)/CXCL12. JEM 198: 823-830 [Abstract] [Full Text]  
  • Melchjorsen, J., Sorensen, L. N., Paludan, S. R. (2003). Expression and function of chemokines during viral infections: from molecular mechanisms to in vivo function. J. Leukoc. Biol. 74: 331-343 [Abstract] [Full Text]  
  • Le Goffic, R., Mouchel, T., Ruffault, A., Patard, J.-J., Jegou, B., Samson, M. (2003). Mumps Virus Decreases Testosterone Production and Gamma Interferon-Induced Protein 10 Secretion by Human Leydig Cells. J. Virol. 77: 3297-3300 [Abstract] [Full Text]  
  • Lesokhin, A. M., Delgado-Lopez, F., Horwitz, M. S. (2002). Inhibition of Chemokine Expression by Adenovirus Early Region Three (E3) Genes. J. Virol. 76: 8236-8243 [Abstract] [Full Text]  
  • Knuefermann, P., Chen, P., Misra, A., Shi, S.-P., Abdellatif, M., Sivasubramanian, N. (2002). Myotrophin/V-1, a Protein Up-regulated in the Failing Human Heart and in Postnatal Cerebellum, Converts NFkappa B p50-p65 Heterodimers to p50-p50 and p65-p65 Homodimers. J. Biol. Chem. 277: 23888-23897 [Abstract] [Full Text]  
  • Friedman, J. M., Horwitz, M. S. (2002). Inhibition of Tumor Necrosis Factor Alpha-Induced NF-{kappa}B Activation by the Adenovirus E3-10.4/14.5K Complex. J. Virol. 76: 5515-5521 [Abstract] [Full Text]  
  • Zaiss, A.-K., Liu, Q., Bowen, G. P., Wong, N. C. W., Bartlett, J. S., Muruve, D. A. (2002). Differential Activation of Innate Immune Responses by Adenovirus and Adeno-Associated Virus Vectors. J. Virol. 76: 4580-4590 [Abstract] [Full Text]  
  • Thomas, C. E., Edwards, P., Wickham, T. J., Castro, M. G., Lowenstein, P. R. (2002). Adenovirus Binding to the Coxsackievirus and Adenovirus Receptor or Integrins Is Not Required To Elicit Brain Inflammation but Is Necessary To Transduce Specific Neural Cell Types. J. Virol. 76: 3452-3460 [Abstract] [Full Text]  
  • Tibbles, L. A., Spurrell, J. C. L., Bowen, G. P., Liu, Q., Lam, M., Zaiss, A. K., Robbins, S. M., Hollenberg, M. D., Wickham, T. J., Muruve, D. A. (2002). Activation of p38 and ERK Signaling during Adenovirus Vector Cell Entry Lead to Expression of the C-X-C Chemokine IP-10. J. Virol. 76: 1559-1568 [Abstract] [Full Text]  
  • Lyakh, L. A., Koski, G. K., Young, H. A., Spence, S. E., Cohen, P. A., Rice, N. R. (2002). Adenovirus type 5 vectors induce dendritic cell differentiation in human CD14+ monocytes cultured under serum-free conditions. Blood 99: 600-608 [Abstract] [Full Text]  
  • Molinier-Frenkel, V., Lengagne, R., Gaden, F., Hong, S.-S., Choppin, J., Gahery-Segard, H., Boulanger, P., Guillet, J.-G. (2002). Adenovirus Hexon Protein Is a Potent Adjuvant for Activation of a Cellular Immune Response. J. Virol. 76: 127-135 [Abstract] [Full Text]  
  • Alcorn, M. J., Booth, J. L., Coggeshall, K. M., Metcalf, J. P. (2001). Adenovirus Type 7 Induces Interleukin-8 Production via Activation of Extracellular Regulated Kinase 1/2. J. Virol. 75: 6450-6459 [Abstract] [Full Text]  
  • Streetz, K., Fregien, B., Plumpe, J., Korber, K., Kubicka, S., Sass, G., Bischoff, S. C., Manns, M. P., Tiegs, G., Trautwein, C. (2001). Dissection of the Intracellular Pathways in Hepatocytes Suggests a Role for Jun Kinase and IFN Regulatory Factor-1 in Con A-Induced Liver Failure. J. Immunol. 167: 514-523 [Abstract] [Full Text]  
  • Mossman, K. L., Macgregor, P. F., Rozmus, J. J., Goryachev, A. B., Edwards, A. M., Smiley, J. R. (2001). Herpes Simplex Virus Triggers and Then Disarms a Host Antiviral Response. J. Virol. 75: 750-758 [Abstract] [Full Text]  
  • Morelli, A. E., Larregina, A. T., Ganster, R. W., Zahorchak, A. F., Plowey, J. M., Takayama, T., Logar, A. J., Robbins, P. D., Falo, L. D., Thomson, A. W. (2000). Recombinant Adenovirus Induces Maturation of Dendritic Cells via an NF-kappa B-Dependent Pathway. J. Virol. 74: 9617-9628 [Abstract] [Full Text]