1887

Journal of General Virology header logo

Volume 95, Issue 4

Differential induction of CCL5 by pathogenic and non-pathogenic strains of West Nile virus in brain endothelial cells and astrocytes Open Access

Abstract

The neuroinflammatory response to West Nile virus (WNV) infection can be either protective or pathological depending on the context. Although several studies have examined chemokine profiles within brains of WNV-infected mice, little is known about how various cell types within the central nervous system (CNS) contribute to chemokine expression. Here, we assessed chemokine expression in brain microvascular endothelial cells and astrocytes, which comprise the major components of the blood–brain barrier (BBB), in response to a non-pathogenic (WNV-MAD78) and a highly pathogenic (WNV-NY) strain of WNV. Higher levels of the chemokine CCL5 were detected in WNV-MAD78-infected brain endothelial monolayers compared with WNV-NY-infected cells. However, the opposite profile was observed in WNV-infected astrocytes, indicating that pathogenic and non-pathogenic strains of WNV provoke different CCL5 profiles at the BBB. Thus, cells comprising the BBB may contribute to a dynamic pro-inflammatory response within the CNS that evolves as WNV infection progresses.

  • Received:
  • Accepted:
  • Published Online:
© 2014 SGM
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.060558-0
2014-04-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/4/862.html?itemId=/content/journal/jgv/10.1099/vir.0.060558-0&mimeType=html&fmt=ahah

References

  1. Beasley D. W., Li L., Suderman M. T., Barrett A. D. 2002; Mouse neuroinvasive phenotype of West Nile virus strains varies depending upon virus genotype. Virology 296:17–23 [View Article][PubMed]
     [Google Scholar]
  2. Bruno V., Copani A., Besong G., Scoto G., Nicoletti F. 2000; Neuroprotective activity of chemokines against N-methyl-d-aspartate or β-amyloid-induced toxicity in culture. Eur J Pharmacol 399:117–121 [View Article][PubMed]
     [Google Scholar]
  3. Carman C. V. 2009; Mechanisms for transcellular diapedesis: probing and pathfinding by ‘invadosome-like protrusions’. J Cell Sci 122:3025–3035 [View Article][PubMed]
     [Google Scholar]
  4. Cheeran M. C., Hu S., Sheng W. S., Rashid A., Peterson P. K., Lokensgard J. R. 2005; Differential responses of human brain cells to West Nile virus infection. J Neurovirol 11:512–524 [View Article][PubMed]
     [Google Scholar]
  5. Chui R., Dorovini-Zis K. 2010; Regulation of CCL2 and CCL3 expression in human brain endothelial cells by cytokines and lipopolysaccharide. J Neuroinflammation 7:1 [View Article][PubMed]
     [Google Scholar]
  6. Eugenin E. A., Clements J. E., Zink M. C., Berman J. W. 2011; Human immunodeficiency virus infection of human astrocytes disrupts blood–brain barrier integrity by a gap junction-dependent mechanism. J Neurosci 31:9456–9465 [View Article][PubMed]
     [Google Scholar]
  7. Glass W. G., Lim J. K., Cholera R., Pletnev A. G., Gao J. L., Murphy P. M. 2005; Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J Exp Med 202:1087–1098 [View Article][PubMed]
     [Google Scholar]
  8. Hussmann K. L., Samuel M. A., Kim K. S., Diamond M. S., Fredericksen B. L. 2013; Differential replication of pathogenic and nonpathogenic strains of West Nile virus within astrocytes. J Virol 87:2814–2822 [View Article][PubMed]
     [Google Scholar]
  9. Klein R. S., Lin E., Zhang B., Luster A. D., Tollett J., Samuel M. A., Engle M., Diamond M. S. 2005; Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J Virol 79:11457–11466 [View Article][PubMed]
     [Google Scholar]
  10. Lim J. K., Obara C. J., Rivollier A., Pletnev A. G., Kelsall B. L., Murphy P. M. 2011; Chemokine receptor Ccr2 is critical for monocyte accumulation and survival in West Nile virus encephalitis. J Immunol 186:471–478 [View Article][PubMed]
     [Google Scholar]
  11. Liu K. K., Dorovini-Zis K. 2012; Differential regulation of CD4+ T cell adhesion to cerebral microvascular endothelium by the β-chemokines CCL2 and CCL3. Int J Mol Sci 13:16119–16140 [View Article][PubMed]
     [Google Scholar]
  12. Louboutin J. P., Strayer D. S. 2012; Blood–brain barrier abnormalities caused by HIV-1 gp120: mechanistic and therapeutic implications. ScientificWorldJournal 2012:482575 [View Article][PubMed]
     [Google Scholar]
  13. Middleton J., Patterson A. M., Gardner L., Schmutz C., Ashton B. A. 2002; Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 100:3853–3860 [View Article][PubMed]
     [Google Scholar]
  14. Nakayama T., Shirane J., Hieshima K., Shibano M., Watanabe M., Jin Z., Nagakubo D., Saito T., Shimomura Y., Yoshie O. 2006; Novel antiviral activity of chemokines. Virology 350:484–492 [View Article][PubMed]
     [Google Scholar]
  15. Omalu B. I., Shakir A. A., Wang G., Lipkin W. I., Wiley C. A. 2003; Fatal fulminant pan-meningo-polioencephalitis due to West Nile virus. Brain Pathol 13:465–472 [View Article][PubMed]
     [Google Scholar]
  16. Papa A., Danis K., Baka A., Bakas A., Dougas G., Lytras T., Theocharopoulos G., Chrysagis D., Vassiliadou E.other authors 2010; Ongoing outbreak of West Nile virus infections in humans in Greece, July-August 2010. Euro Surveill 15:[PubMed]
     [Google Scholar]
  17. Papa A., Bakonyi T., Xanthopoulou K., Vázquez A., Tenorio A., Nowotny N. 2011; Genetic characterization of West Nile virus lineage 2, Greece, 2010. Emerg Infect Dis 17:920–922 [View Article][PubMed]
     [Google Scholar]
  18. Pozner R. G., Collado S., Jaquenod de Giusti C., Ure A. E., Biedma M. E., Romanowski V., Schattner M., Gómez R. M. 2008; Astrocyte response to Junín virus infection. Neurosci Lett 445:31–35 [View Article][PubMed]
     [Google Scholar]
  19. Roberts T. K., Eugenin E. A., Lopez L., Romero I. A., Weksler B. B., Couraud P. O., Berman J. W. 2012; CCL2 disrupts the adherens junction: implications for neuroinflammation. Lab Invest 92:1213–1233 [View Article][PubMed]
     [Google Scholar]
  20. Roe K., Kumar M., Lum S., Orillo B., Nerurkar V. R., Verma S. 2012; West Nile virus-induced disruption of the blood–brain barrier in mice is characterized by the degradation of the junctional complex proteins and increase in multiple matrix metalloproteinases. J Gen Virol 93:1193–1203 [View Article][PubMed]
     [Google Scholar]
  21. Schneider C. A., Rasband W. S., Eliceiri K. W. 2012; NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675 [View Article][PubMed]
     [Google Scholar]
  22. Shi P. Y., Tilgner M., Lo M. K., Kent K. A., Bernard K. A. 2002; Infectious cDNA clone of the epidemic West Nile virus from New York City. J Virol 76:5847–5856 [View Article][PubMed]
     [Google Scholar]
  23. Shirato K., Kimura T., Mizutani T., Kariwa H., Takashima J. 2004; Different chemokine expression in lethal and non-lethal murine West Nile virus infection. J Med Virol 74:507–513 [View Article][PubMed]
     [Google Scholar]
  24. Spindler K. R., Hsu T. H. 2012; Viral disruption of the blood–brain barrier. Trends Microbiol 20:282–290 [View Article][PubMed]
     [Google Scholar]
  25. Stins M. F., Badger J., Sik Kim K. 2001; Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb Pathog 30:19–28 [View Article][PubMed]
     [Google Scholar]
  26. Swan C. H., Bühler B., Steinberger P., Tschan M. P., Barbas C. F. III, Torbett B. E. 2006; T-cell protection and enrichment through lentiviral CCR5 intrabody gene delivery. Gene Ther 13:1480–1492 [View Article][PubMed]
     [Google Scholar]
  27. van Marle G., Antony J., Ostermann H., Dunham C., Hunt T., Halliday W., Maingat F., Urbanowski M. D., Hobman T.other authors 2007; West Nile virus-induced neuroinflammation: glial infection and capsid protein-mediated neurovirulence. J Virol 81:10933–10949 [View Article][PubMed]
     [Google Scholar]
  28. Verma S., Lo Y., Chapagain M., Lum S., Kumar M., Gurjav U., Luo H., Nakatsuka A., Nerurkar V. R. 2009; West Nile virus infection modulates human brain microvascular endothelial cells tight junction proteins and cell adhesion molecules: transmigration across the in vitro blood–brain barrier. Virology 385:425–433 [View Article][PubMed]
     [Google Scholar]
  29. Verma S., Kumar M., Gurjav U., Lum S., Nerurkar V. R. 2010; Reversal of West Nile virus-induced blood–brain barrier disruption and tight junction proteins degradation by matrix metalloproteinases inhibitor. Virology 397:130–138 [View Article][PubMed]
     [Google Scholar]
  30. Wang T., Town T., Alexopoulou L., Anderson J. F., Fikrig E., Flavell R. A. 2004; Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10:1366–1373 [View Article][PubMed]
     [Google Scholar]
  31. Wang P., Dai J., Bai F., Kong K. F., Wong S. J., Montgomery R. R., Madri J. A., Fikrig E. 2008; Matrix metalloproteinase 9 facilitates West Nile virus entry into the brain. J Virol 82:8978–8985 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.060558-0
Loading
Differential induction of CCL5 by pathogenic and non-pathogenic strains of West Nile virus in brain endothelial cells and astrocytes
J. Gen. Virol. 95, 862 (2014); https://doi.org/10.1099/vir.0.060558-0
/content/journal/jgv/10.1099/vir.0.060558-0
/content/journal/jgv/10.1099/vir.0.060558-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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