Resistance to dengue virus infection in mice is potentiated by CXCL10 and is independent of CXCL10-mediated leukocyte recruitment

Journal of Immunology

Volumn 184, Issue 10, 2010, Pages 5705-5714

  Ip, Peng Peng ^a   Liao, Fang ^a,b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEPARAN SULFATE; VIRUS RECEPTOR; CXCL10 PROTEIN, MOUSE;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DENGUE; EFFECTOR CELL; LYMPHOCYTE COUNT; LYMPHOCYTE MIGRATION; LYMPHOCYTIC INFILTRATION; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS CELL INTERACTION; VIRUS LOAD; VIRUS RESISTANCE; AEDES; ANIMAL; BRAIN; CELL CULTURE; CELL LINE; CELL MOTION; DENGUE VIRUS; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MORTALITY; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; RNA INTERFERENCE; TUMOR CELL LINE; VIROLOGY;

AEDES; ANIMALS; BRAIN; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CXCL10; DENGUE; DENGUE VIRUS; IMMUNITY, INNATE; MICE; MICE, KNOCKOUT; NEURONS; RNA INTERFERENCE;

EID: 77954723683     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903484     Document Type: Article

References (54)

1. Guzmán, M. G., and G. Kourí. 2002. Dengue: an update. Lancet Infect. Dis. 2: 33-42.
2. Clarke, T. 2002. Dengue virus: break-bone fever. Nature 416: 672-674.
3. Wilder-Smith, A., and E. Schwartz. 2005. Dengue in travelers. N. Engl. J. Med. 353: 924-932.
4. Rothman, A. L. 2004. Dengue: defining protective versus pathologic immunity. J. Clin. Invest. 113: 946-951.
5. Lum, L. C., S. K. Lam, Y. S. Choy, R. George, and F. Harun. 1996. Dengue encephalitis: a true entity? Am. J. Trop. Med. Hyg. 54: 256-259.
6. Solomon, T., N. M. Dung, D. W. Vaughn, R. Kneen, L. T. Thao, B. Raengsakulrach, H. T. Loan, N. P. Day, J. Farrar, K. S. Myint, et al. 2000. Neurological manifestations of dengue infection. Lancet 355: 1053-1059.
7. Kho, L. K., H. Sumarmo, E. C. Wulur, Jahja, and D. J. Gubler. 1981. Dengue hemorrhagic fever accompanied by encephalopathy in Jakarta. Southeast Asian J. Trop. Med. Public Health 12: 83-86.
8. Misra, U. K., J. Kalita, U. K. Syam, and T. N. Dhole. 2006. Neurological manifestations of dengue virus infection. J. Neurol. Sci. 244: 117-122.
9. Leão, R. N., T. Oikawa, E. S. Rosa, J. T. Yamaki, S. G. Rodrigues, H. B. Vasconcelos, M. R. Sousa, J. K. Tsukimata, R. S. Azevedo, and P. F. Vasconcelos. 2002. Isolation of dengue 2 virus from a patient with central nervous system involvement (transverse myelitis). Rev. Soc. Bras. Med. Trop. 35: 401-404.
10. Puccioni-Sohler, M., C. N. Soares, R. Papaiz-Alvarenga, M. J. Castro, L. C. Faria, and J. M. Peralta. 2009. Neurologic dengue manifestations associated with intrathecal specific immune response. Neurology 73: 1413-1417.
11. Chen, Y. C., and S. Y. Wang. 2002. Activation of terminally differentiated human monocytes/macrophages by dengue virus: productive infection, hierarchical production of innate cytokines and chemokines, and the synergistic effect of lipopolysaccharide. J. Virol. 76: 9877-9887.
12. Bosch, I., K. Xhaja, L. Estevez, G. Raines, H. Melichar, R. V. Warke, M. V. Fournier, F. A. Ennis, and A. L. Rothman. 2002. Increased production of interleukin-8 in primary human monocytes and in human epithelial and endothelial cell lines after dengue virus challenge. J. Virol. 76: 5588-5597.
13. Juffrie, M., G.M. van DerMeer, C. E. Hack, K. Haasnoot, Sutaryo, A. J. Veerman, and L. G. Thijs. 2000. Inflammatory mediators in dengue virus infection in children: interleukin-8 and its relationship to neutrophil degranulation. Infect. Immun. 68: 702-707.
14. Avirutnan, P., P. Malasit, B. Seliger, S. Bhakdi, and M. Husmann. 1998. Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. J. Immunol. 161: 6338-6346. (Pubitemid 28536010)
15. King, C. A., R. Anderson, and J. S. Marshall. 2002. Dengue virus selectively induces human mast cell chemokine production. J. Virol. 76: 8408-8419.
16. Spain-Santana, T. A., S. Marglin, F. A. Ennis, and A. L. Rothman. 2001. MIP-1α and MIP-1b induction by dengue virus. J. Med. Virol. 65: 324-330.
17. Hsieh, M. F., S. L. Lai, J. P. Chen, J. M. Sung,Y. L. Lin, B.A.Wu-Hsieh, C. Gerard, A. Luster, and F. Liao. 2006. Both CXCR3 and CXCL10/IFN-inducible protein 10 are required for resistance to primary infection by dengue virus. J. Immunol. 177: 1855-1863.
18. Loetscher, M., B. Gerber, P. Loetscher, S. A. Jones, L. Piali, I. Clark-Lewis, M. Baggiolini, and B. Moser. 1996. Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. [see comments] J. Exp. Med. 184: 963-969.
19. Dufour, J. H., M. Dziejman, M. T. Liu, J. H. Leung, T. E. Lane, and A. D. Luster. 2002. IFN-γ-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J. Immunol. 168: 3195-3204.
20. Patterson, C. E., J. K. Daley, L. A. Echols, T. E. Lane, and G. F. Rall. 2003. Measles virus infectioninduces chemokine synthesisby neurons. J. Immunol. 171: 3102-3109.
21. + T-cell recruitment and control of West Nile virus encephalitis. J. Virol. 79: 11457-11466.
22. Walsh, K. B., R. A. Edwards, K. M. Romero, M. V. Kotlajich, S. A. Stohlman, and T. E. Lane. 2007. Expression of CXC chemokine ligand 10 from the mouse hepatitis virus genome results in protection from viral-induced neurological and liver disease. J. Immunol. 179: 1155-1165.
23. Thapa, M., and D. J. Carr. 2008. Herpes simplex virus type 2-induced mortality following genital infection is blocked by anti-tumor necrosis factor a antibody in CXCL10-deficient mice. J. Virol. 82: 10295-10301.
24. Wuest, T. R., and D. J. Carr. 2008. Dysregulation of CXCR3 signaling due to CXCL10 deficiency impairs the antiviral response to herpes simplex virus 1 infection. J. Immunol. 181: 7985-7993.
25. Christensen, J. E., S. Simonsen, C. Fenger, M. R. Sørensen, T. Moos, J. P. Christensen, B. Finsen, and A. R. Thomsen. 2009. Fulminant lymphocytic choriomeningitis virus-induced inflammation of the CNS involves a cytokinechemokine- cytokine-chemokine cascade. J. Immunol. 182: 1079-1087.
26. Fink, J., F. Gu, L. Ling, T. Tolfvenstam, F. Olfat, K. C. Chin, P. Aw, J. George, V. A. Kuznetsov, M. Schreiber, et al. 2007. Host gene expression profiling of dengue virus infection in cell lines and patients. PLoS Negl. Trop. Dis. 1: e86.
27. Warke, R. V., A. Becerra, A. Zawadzka, D. J. Schmidt, K. J. Martin, K. Giaya, J. H. Dinsmore, M. Woda, G. Hendricks, T. Levine, et al. 2008. Efficient dengue virus (DENV) infection of human muscle satellite cells upregulates type I interferon response genes and differentially modulates MHC I expression on bystander and DENV-infected cells. J. Gen. Virol. 89: 1605-1615.
28. Becerra, A., R. V. Warke, K. Martin, K. Xhaja, N. de Bosch, A. L. Rothman, and I. Bosch. 2009. Gene expression profiling of dengue infected human primary cells identifies secreted mediators in vivo. J. Med. Virol. 81: 1403-1411.
29. Igarashi, A. 1978. Isolation of a Singh's Aedes albopictus cell clone sensitive to Dengue and Chikungunya viruses. J. Gen. Virol. 40: 531-544.
30. Houng, H. H., D. Hritz, and N. Kanesa-thasan. 2000. Quantitative detection of dengue 2 virus using fluorogenic RT-PCR based on 39-noncoding sequence. J. Virol. Methods 86: 1-11.
31. Chen, J. P., H. L. Lu, S. L. Lai, G. S. Campanella, J. M. Sung, M. Y. Lu, B. A. Wu-Hsieh, Y. L. Lin, T. E. Lane, A. D. Luster, and F. Liao. 2006. Dengue virus induces expression of CXC chemokine ligand 10/IFN-γ-inducible protein 10, which competitively inhibits viral binding to cell surface heparan sulfate. J. Immunol. 177: 3185-3192.
32. Campanella, G. S., E. M. Lee, J. Sun, and A. D. Luster. 2003. CXCR3 and heparin binding sites of the chemokine IP-10 (CXCL10). J. Biol. Chem. 278: 17066-17074.
33. Brewer,G. J., J. R. Torricelli, E. K. Evege, and P. J. Price. 1993.Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serumfree medium combination. J. Neurosci. Res. 35: 567-576.
34. Klein, R. S. 2004. Regulation of neuroinflammation: the role of CXCL10 in lymphocyte infiltration during autoimmune encephalomyelitis. J. Cell. Biochem. 92: 213-222.
35. Klein, R. S., L. Izikson, T. Means, H. D. Gibson, E. Lin, R. A. Sobel, H. L. Weiner, and A. D. Luster. 2004. IFN-inducible protein 10/CXC chemokine ligand 10-independent induction of experimental autoimmune encephalomyelitis. J. Immunol. 172: 550-559.
36. Campanella, G. S., A. M. Tager, J. K. El Khoury, S. Y. Thomas, T. A. Abrazinski, L. A. Manice, R. A. Colvin, and A. D. Luster. 2008. Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria. Proc. Natl. Acad. Sci. USA 105: 4814-4819.
37. Zhang, B., Y. K. Chan, B. Lu, M. S. Diamond, and R. S. Klein. 2008. CXCR3 mediates region-specific antiviral T cell trafficking within the central nervous system during West Nile virus encephalitis. J. Immunol. 180: 2641-2649.
38. Hauser, A. E., G. F. Debes, S. Arce, G. Cassese, A. Hamann, A. Radbruch, and R. A. Manz. 2002. Chemotactic responsiveness toward ligands for CXCR3 and CXCR4 is regulated on plasma blasts during the time course of a memory immune response. J. Immunol. 169: 1277-1282.
39. Muehlinghaus, G., L. Cigliano, S. Huehn, A. Peddinghaus, H. Leyendeckers, A. E. Hauser, F. Hiepe, A. Radbruch, S. Arce, and R. A. Manz. 2005. Regulation of CXCR3 and CXCR4 expression during terminal differentiation of memory B cells into plasma cells. Blood 105: 3965-3971.
40. Odendahl, M., H. Mei, B. F. Hoyer, A. M. Jacobi, A. Hansen, G. Muehlinghaus, C. Berek, F. Hiepe, R. Manz, A. Radbruch, and T. Dörner. 2005. Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response. Blood 105: 1614-1621.
41. Sallusto, F., and C. R. Mackay. 2004. Chemoattractants and their receptors in homeostasis and inflammation. Curr. Opin. Immunol. 16: 724-731.
42. + effector T cells involved in immune surveillance of the lymphocytic choriomeningitis virus-infected central nervous system. J. Immunol. 176: 4235-4243.
43. Thapa, M., R. S. Welner, R. Pelayo, and D. J. Carr. 2008. CXCL9 and CXCL10 expression are critical for control of genital herpes simplex virus type 2 infection through mobilization of HSV-specific CTL and NK cells to the nervous system. J. Immunol. 180: 1098-1106.
44. Chen, Y., T. Maguire, R. E. Hileman, J. R. Fromm, J. D. Esko, R. J. Linhardt, and R. M. Marks. 1997. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3: 866-871.
45. Germi, R., J. M. Crance, D. Garin, J. Guimet, H. Lortat-Jacob, R. W. Ruigrok, J. P. Zarski, and E. Drouet. 2002. Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus. Virology 292: 162-168.
46. Hilgard, P., and R. Stockert. 2000. Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology 32: 1069-1077.
47. Prestwood, T. R., D. M. Prigozhin, K. L. Sharar, R. M. Zellweger, and S. Shresta. 2008. A mouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads. J. Virol. 82: 8411-8421.
48. Añez, G., R. Men, K. H. Eckels, and C. J. Lai. 2009. Passage of dengue virus type 4 vaccine candidates in fetal rhesus lung cells selects heparin-sensitive variants that result in loss of infectivity and immunogenicity in rhesus macaques. J. Virol. 83: 10384-10394.
49. Biber, K., I. Dijkstra, C. Trebst, C. J. De Groot, R. M. Ransohoff, and H. W. Boddeke. 2002. Functional expression of CXCR3 in cultured mouse and human astrocytes and microglia. Neuroscience 112: 487-497. (Pubitemid 34634144)
50. Li, H., Z. Gang, H. Yuling, X. Luokun, X. Jie, L. Hao, W. Li, H. Chunsong, L. Junyan, J. Mingshen, et al. 2006. Different neurotropic pathogens elicit neurotoxic CCR9- or neurosupportive CXCR3-expressing microglia. J. Immunol. 177: 3644-3656.
51. Rappert, A., I. Bechmann, T. Pivneva, J. Mahlo, K. Biber, C. Nolte, A. D. Kovac, C. Gerard, H. W. Boddeke, R. Nitsch, and H. Kettenmann. 2004. CXCR3-dependent microglial recruitment is essential for dendrite loss after brain lesion. J. Neurosci. 24: 8500-8509.
52. Szabo, S. J., B. M. Sullivan, C. Stemmann, A. R. Satoskar, B. P. Sleckman, and L. H. Glimcher. 2002. Distinct effects of T-bet in TH1 lineage commitment and IFN-γ production in CD4 and CD8 T cells. Science 295: 338-342.
53. + T-cell trafficking. Blood 106: 3432-3439.
54. Tschen, S. I., S. A. Stohlman, C. Ramakrishna, D. R. Hinton, R. D. Atkinson, and C. C. Bergmann. 2006. CNS viral infection diverts homing of antibodysecreting cells from lymphoid organs to the CNS. Eur. J. Immunol. 36: 603-612.