IL-1R1 signaling regulates CXCL12-mediated T cell localization and fate within the central nervous system during West Nile Virus encephalitis

Journal of Immunology

Volumn 193, Issue 8, 2014, Pages 4095-4106

  Durrant, Douglas M ^a   Daniels, Brian P ^a   Klein, Robyn S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; CD69 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; STROMAL CELL DERIVED FACTOR 1; CCL2 PROTEIN, MOUSE; CCL5 PROTEIN, MOUSE; CXCL10 PROTEIN, MOUSE; CXCL12 PROTEIN, MOUSE; CXCR4 PROTEIN, MOUSE; IL1B PROTEIN, MOUSE; IL1R1 PROTEIN, MOUSE; LECTIN; LEUKOCYTE ANTIGEN; T LYMPHOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY ENDOTHELIAL CELL; CELL FATE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; IN VITRO STUDY; LEUKOCYTE ADHERENCE; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION; VIRUS ENCEPHALITIS; VIRUS IMMUNITY; WEST NILE FLAVIVIRUS; ANIMAL; BIOSYNTHESIS; BRAIN; C57BL MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ADHESION; ENDOTHELIUM CELL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; VASCULARIZATION; VIROLOGY; WEST NILE FEVER;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; BLOOD-BRAIN BARRIER; BRAIN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CHEMOKINE CCL2; CHEMOKINE CCL5; CHEMOKINE CXCL10; CHEMOKINE CXCL12; ENDOTHELIAL CELLS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; LECTINS, C-TYPE; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CXCR4; RECEPTORS, INTERLEUKIN-1 TYPE I; SIGNAL TRANSDUCTION; WEST NILE FEVER; WEST NILE VIRUS;

EID: 84907494134     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401192     Document Type: Article

References (84)

1. Engelhardt, B., and C. Coisne. 2011. Fluids and barriers of the CNS establish immune privilege by confining immune surveillance to a two-walled castle moat surrounding the CNS castle. Fluids Barriers CNS 8: 4.
2. McCandless, E. E., L. Piccio, B. M. Woerner, R. E. Schmidt, J. B. Rubin, A. H. Cross, and R. S. Klein. 2008. Pathological expression of CXCL12 at the blood-brain barrier correlates with severity of multiple sclerosis. Am. J. Pathol. 172: 799-808.
3. McCandless, E. E., Q. Wang, B. M. Woerner, J. M. Harper, and R. S. Klein. 2006. CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J. Immunol. 177: 8053-8064.
4. McCandless, E. E., B. Zhang, M. S. Diamond, and R. S. Klein. 2008. CXCR4 antagonism increases T cell trafficking in the central nervous system and improves survival from West Nile virus encephalitis. Proc. Natl. Acad. Sci. USA 105: 11270-11275.
5. Bouffard, J. P., M.A. Riudavets, R. Holman, and E. J. Rushing. 2004. Neuropathology of the brain and spinal cord in human West Nile virus infection. Clin. Neuropathol. 23: 59-61.
6. Cruz-Orengo, L., D. W. Holman, D. Dorsey, L. Zhou, P. Zhang, M. Wright, E. E. McCandless, J.R. Patel, G. D. Luker, D. R. Littman, et al. 2011. CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity. J. Exp. Med. 208: 327-339.
7. Bartholomäus, I., N. Kawakami, F. Odoardi, C. Schläger, D. Miljkovic, J. W. Ellwart, W. E. Klinkert, C. Flügel-Koch, T. B. Issekutz, H. Wekerle, and A. Flügel. 2009. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462: 94-98.
8. Anandasabapathy, N., G. D. Victora, M. Meredith, R. Feder, B. Dong, C. Kluger, K. Yao, M. L. Dustin, M. C. Nussenzweig, R. M. Steinman, and K. Liu. 2011. Flt3L controls the development of radiosensitive dendritic cells in the meninges and choroid plexus of the steady-state mouse brain. J. Exp. Med. 208: 1695-1705.
9. Hausmann, J., A. Pagenstecher, K. Baur, K. Richter, H. J. Rziha, and P. Staeheli. 2005. CD8 T cells require g interferon to clear Borna disease virus from the brain and prevent immune system-mediated neuronal damage. J. Virol. 79: 13509-13518.
10. Mendez-Fernandez, Y. V., A. J. Johnson, M. Rodriguez, and L. R. Pease. 2003. Clearance of Theiler's virus infection depends on the ability to generate a CD8+ T cell response against a single immunodominant viral peptide. Eur. J. Immunol. 33: 2501-2510.
11. Samuel, M.A., and M. S. Diamond. 2006. Pathogenesis of West Nile virus infection: a balance between virulence, innate and adaptive immunity, and viral evasion. J. Virol. 80: 9349-9360.
12. Davis, L. E., R. DeBiasi, D. E. Goade, K. Y. Haaland, J. A. Harrington, J. B. Harnar, S. A. Pergam, M. K. King, B. K. DeMasters, and K. L. Tyler. 2006. West Nile virus neuroinvasive disease. Ann. Neurol. 60: 286-300.
13. Sejvar, J. J., M. B. Haddad, B. C. Tierney, G. L. Campbell, A. A. Marfin, J. A. Van Gerpen, A. Fleischauer, A. A. Leis, D. S. Stokic, and L. R. Petersen. 2003. Neurologic manifestations and outcome of West Nile virus infection. JAMA 290: 511-515.
14. Kleinschmidt-DeMasters, B. K., B. A. Marder, M. E. Levi, S. P. Laird, J. T. McNutt, E. J. Escott, G. T. Everson, and K. L. Tyler. 2004. Naturally acquired West Nile virus encephalomyelitis in transplant recipients: clinical, laboratory, diagnostic, and neuropathological features. Arch. Neurol. 61: 1210-1220.
15. Shrestha, B., D. Gottlieb, and M. S. Diamond. 2003. Infection and injury of neurons by West Nile encephalitis virus. J. Virol. 77: 13203-13213.
16. Diamond, M. S., B. Shrestha, E. Mehlhop, E. Sitati, and M. Engle. 2003. Innate and adaptive immune responses determine protection against disseminated infection by West Nile encephalitis virus. Viral Immunol. 16: 259-278.
17. Brien, J. D., J. L. Uhrlaub, and J. Nikolich-Zugich. 2008. West Nile virusspecific CD4 T cells exhibit direct antiviral cytokine secretion and cytotoxicity and are sufficient for antiviral protection. J. Immunol. 181: 8568-8575.
18. Klein, R. S., E. Lin, B. Zhang, A. D. Luster, J. Tollett, M.A. Samuel, M. Engle, and M. S. Diamond. 2005. Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J. Virol. 79: 11457-11466.
19. Shrestha, B., and M. S. Diamond. 2004. Role of CD8+ T cells in control of West Nile virus infection. J. Virol. 78: 8312-8321.
20. Sitati, E. M., and M. S. Diamond. 2006. CD4+ T-cell responses are required for clearance of West Nile virus from the central nervous system. J. Virol. 80: 12060-12069.
21. Diamond, M. S., B. Shrestha, A. Marri, D. Mahan, and M. Engle. 2003. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J. Virol. 77: 2578-2586.
22. Shrestha, B., M.A. Samuel, and M. S. Diamond. 2006. CD8+ T cells require perforin to clear West Nile virus from infected neurons. J. Virol. 80: 119-129.
23. Shrestha, B., T. Wang, M.A. Samuel, K. Whitby, J. Craft, E. Fikrig, and M. S. Diamond. 2006. Gamma interferon plays a crucial early antiviral role in protection against West Nile virus infection. J. Virol. 80: 5338-5348.
24. Wang, Y., M. Lobigs, E. Lee, and A. Müllbacher. 2003. CD8+ T cells mediate recovery and immunopathology in West Nile virus encephalitis. J. Virol. 77: 13323-13334.
25. Shrestha, B., B. Zhang, W. E. Purtha, R. S. Klein, and M. S. Diamond. 2008. Tumor necrosis factor a protects against lethal West Nile virus infection by promoting trafficking of mononuclear leukocytes into the central nervous system. J. Virol. 82: 8956-8964.
26. Durrant, D. M., M. L. Robinette, and R. S. Klein. 2013. IL-1R1 is required for dendritic cell-mediated T cell reactivation within the CNS during West Nile virus encephalitis. J. Exp. Med. 210: 503-516.
27. Stohlman, S. A., C. C. Bergmann, M. T. Lin, D. J. Cua, and D. R. Hinton. 1998. CTL effector function within the central nervous system requires CD4+ T cells. J. Immunol. 160: 2896-2904.
28. Phares, T. W., S. A. Stohlman, M. Hwang, B. Min, D. R. Hinton, and C. C. Bergmann. 2012. CD4 T cells promote CD8 T cell immunity at the priming and effector site during viral encephalitis. J. Virol. 86: 2416-2427.
29. Dinarello, C. A. 2011. A clinical perspective of IL-1β as the gatekeeper of inflammation. Eur. J. Immunol. 41: 1203-1217.
30. Dinarello, C. A., A. Simon, and J. W. van der Meer. 2012. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat. Rev. Drug Discov. 11: 633-652.
31. Kanneganti, T. D. 2010. Central roles of NLRs and inflammasomes in viral infection. Nat. Rev. Immunol. 10: 688-698.
32. Schmitz, N., M. Kurrer, M. F. Bachmann, and M. Kopf. 2005. Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J. Virol. 79: 6441-6448.
33. Sergerie, Y., S. Rivest, and G. Boivin. 2007. Tumor necrosis factor-a and interleukin- 1b play a critical role in the resistance against lethal herpes simplex virus encephalitis. J. Infect. Dis. 196: 853-860.
34. Liang, X. H., L. K. Kleeman, H. H. Jiang, G. Gordon, J. E. Goldman, G. Berry, B. Herman, and B. Levine. 1998. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 72: 8586-8596.
35. Prow, N. A., and D. N. Irani. 2008. The inflammatory cytokine, interleukin-1b, mediates loss of astroglial glutamate transport and drives excitotoxic motor neuron injury in the spinal cord during acute viral encephalomyelitis. J. Neurochem. 105: 1276-1286.
36. Kim, B. S., Y. H. Jin, L. Meng, W. Hou, H. S. Kang, H. S. Park, and C. S. Koh. 2012. IL-1 signal affects both protection and pathogenesis of virus-induced chronic CNS demyelinating disease. J. Neuroinflammation 9: 217.
37. Peng, H., N. Erdmann, N. Whitney, H. Dou, S. Gorantla, H. E. Gendelman, A. Ghorpade, and J. Zheng. 2006. HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1β. Glia 54: 619-629.
38. McCandless, E. E., M. Budde, J.R. Lees, D. Dorsey, E. Lyng, and R. S. Klein. 2009. IL-1R signaling within the central nervous system regulates CXCL12 expression at the blood-brain barrier and disease severity during experimental autoimmune encephalomyelitis. J. Immunol. 183: 613-620.
39. Ramos, H. J., M. C. Lanteri, G. Blahnik, A. Negash, M. S. Suthar, M. M. Brassil, K. Sodhi, P. M. Treuting, M. P. Busch, P. J. Norris, and M. Gale, Jr. 2012. IL-1β signaling promotes CNS-intrinsic immune control of West Nile virus infection. PLoS Pathog. 8: e1003039.
40. Ebel, G. D., A. P. Dupuis, II, K. Ngo, D. Nicholas, E. Kauffman, S. A. Jones, D. Young, J. Maffei, P. Y. Shi, K. Bernard, and L. D. Kramer. 2001. Partial genetic characterization of West Nile virus strains, New York State, 2000. Emerg. Infect. Dis. 7: 650-653.
41. Engle, M. J., and M. S. Diamond. 2003. Antibody prophylaxis and therapy against West Nile virus infection in wild-type and immunodeficient mice. J. Virol. 77: 12941-12949.
42. Samuel, M.A., K. Whitby, B. C. Keller, A. Marri, W. Barchet, B. R. Williams, R. H. Silverman, M. Gale, Jr., and M. S. Diamond. 2006. PKR and RNase L contribute to protection against lethal West Nile virus infection by controlling early viral spread in the periphery and replication in neurons. J. Virol. 80: 7009-7019.
43. Purtha, W. E., N. Myers, V. Mitaksov, E. Sitati, J. Connolly, D. H. Fremont, T. H. Hansen, and M. S. Diamond. 2007. Antigen-specific cytotoxic T lymphocytes protect against lethal West Nile virus encephalitis. Eur. J. Immunol. 37: 1845-1854.
44. Daniels, B. P., L. Cruz-Orengo, T. J. Pasieka, P. O. Couraud, I. A. Romero, B. Weksler, J. A. Cooper, T. L. Doering, and R. S. Klein. 2013. Immortalized human cerebral microvascular endothelial cells maintain the properties of primary cells in an in vitro model of immune migration across the blood brain barrier. J. Neurosci. Methods 212: 173-179.
45. Eriksson, C., A. M. Van Dam, P. J. Lucassen, J. G. Bol, B. Winblad, and M. Schultzberg. 1999. Immunohistochemical localization of interleukin-1b, interleukin-1 receptor antagonist and interleukin-1b converting enzyme/caspase- 1 in the rat brain after peripheral administration of kainic acid. Neuroscience 93: 915-930.
46. Vela, J. M., E. Molina-Holgado, A. Arévalo-Martín, G. Almazán, and C. Guaza. 2002. Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Mol. Cell. Neurosci. 20: 489-502.
47. Higgins, G. A., and J. A. Olschowka. 1991. Induction of interleukin-1b mRNA in adult rat brain. Brain Res. Mol. Brain Res. 9: 143-148.
48. Shaftel, S. S., W. S. Griffin, and M. K. O'Banion. 2008. The role of interleukin-1 in neuroinflammation and Alzheimer disease: an evolving perspective. J. Neuroinflammation 5: 7.
49. Klein, R. S., and M. S. Diamond. 2008. Immunological headgear: antiviral immune responses protect against neuroinvasive West Nile virus. Trends Mol. Med. 14: 286-294.
50. Hosking, M. P., and T. E. Lane. 2010. The role of chemokines during viral infection of the CNS. PLoS Pathog. 6: e1000937.
51. 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.
52. Glass, W. G., J. K. Lim, R. Cholera, A. G. Pletnev, J. L. Gao, and P. M. Murphy. 2005. Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J. Exp. Med. 202: 1087-1098.
53. Szretter, K. J., S. Daffis, J. Patel, M. S. Suthar, R. S. Klein, M. Gale, Jr., and M. S. Diamond. 2010. The innate immune adaptor molecule MyD88 restricts West Nile virus replication and spread in neurons of the central nervous system. J. Virol. 84: 12125-12138.
54. Dheen, S. T., C. Kaur, and E. A. Ling. 2007. Microglial activation and its implications in the brain diseases. Curr. Med. Chem. 14: 1189-1197.
55. King, N. J., D. R. Getts, M. T. Getts, S. Rana, B. Shrestha, and A. M. Kesson. 2007. Immunopathology of flavivirus infections. Immunol. Cell Biol. 85: 33-42.
56. Hatse, S., K. Princen, G. Bridger, E. De Clercq, and D. Schols. 2002. Chemokine receptor inhibition by AMD3100 is strictly confined to CXCR4. FEBS Lett. 527: 255-262.
57. Stumm, R. K., J. Rummel, V. Junker, C. Culmsee, M. Pfeiffer, J. Krieglstein, V. Höllt, and S. Schulz. 2002. A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia. J. Neurosci. 22: 5865-5878.
58. Calderon, T. M., E. A. Eugenin, L. Lopez, S. S. Kumar, J. Hesselgesser, C. S. Raine, and J. W. Berman. 2006. A role for CXCL12 (SDF-1a) in the pathogenesis of multiple sclerosis: regulation of CXCL12 expression in astrocytes by soluble myelin basic protein. J. Neuroimmunol. 177: 27-39.
59. Burns, J. M., B. C. Summers, Y. Wang, A. Melikian, R. Berahovich, Z. Miao, M. E. Penfold, M. J. Sunshine, D. R. Littman, C. J. Kuo, et al. 2006. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J. Exp. Med. 203: 2201-2213.
60. Burger, J. A., and T. J. Kipps. 2006. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 107: 1761-1767.
61. Lundquist, S., and M. Renftel. 2002. The use of in vitro cell culture models for mechanistic studies and as permeability screens for the blood-brain barrier in the pharmaceutical industry: background and current status in the drug discovery process. Vascul. Pharmacol. 38: 355-364.
62. Pinto, A. K., S. Daffis, J. D. Brien, M. D. Gainey, W. M. Yokoyama, K. C. Sheehan, K. M. Murphy, R. D. Schreiber, and M. S. Diamond. 2011. A temporal role of type I interferon signaling in CD8+ T cell maturation during acute West Nile virus infection. PLoS Pathog. 7: e1002407.
63. Ching, S., H. Zhang, N. Belevych, L. He, W. Lai, X. A. Pu, L. B. Jaeger, Q. Chen, and N. Quan. 2007. Endothelial-specific knockdown of interleukin-1 (IL-1) type 1 receptor differentially alters CNS responses to IL-1 depending on its route of administration. J. Neurosci. 27: 10476-10486.
64. Ericsson, A., C. Liu, R. P. Hart, and P. E. Sawchenko. 1995. Type 1 interleukin-1 receptor in the rat brain: distribution, regulation, and relationship to sites of IL-1- induced cellular activation. J. Comp. Neurol. 361: 681-698.
65. Subramaniam, S., C. Stansberg, and C. Cunningham. 2004. The interleukin 1 receptor family. Dev. Comp. Immunol. 28: 415-428.
66. Allan, S. M., P. J. Tyrrell, and N. J. Rothwell. 2005. Interleukin-1 and neuronal injury. Nat. Rev. Immunol. 5: 629-640.
67. Proescholdt, M. G., S. Chakravarty, J. A. Foster, S. B. Foti, E. M. Briley, and M. Herkenham. 2002. Intracerebroventricular but not intravenous interleukin-1β induces widespread vascular-mediated leukocyte infiltration and immune signal mRNA expression followed by brain-wide glial activation. Neuroscience 112: 731-749.
68. Hubbard, A. K., and R. Rothlein. 2000. Intercellular adhesion molecule-1 (ICAM-1) expression and cell signaling cascades. Free Radic. Biol. Med. 28: 1379-1386.
69. Ching, S., L. He, W. Lai, and N. Quan. 2005. IL-1 type I receptor plays a key role in mediating the recruitment of leukocytes into the central nervous system. Brain Behav. Immun. 19: 127-137.
70. Li, Q., N. Powell, H. Zhang, N. Belevych, S. Ching, Q. Chen, J. Sheridan, C. Whitacre, and N. Quan. 2011. Endothelial IL-1R1 is a critical mediator of EAE pathogenesis. Brain Behav. Immun. 25: 160-167.
71. Brosnan, C. F., B. Cannella, L. Battistini, and C. S. Raine. 1995. Cytokine localization in multiple sclerosis lesions: correlation with adhesion molecule expression and reactive nitrogen species. Neurology 45(6, Suppl. 6): S16-S21.
72. Cannella, B., and C. S. Raine. 1995. The adhesion molecule and cytokine profile of multiple sclerosis lesions. Ann. Neurol. 37: 424-435.
73. Deckert, M., S. Virna, M. Sakowicz-Burkiewicz, S. Lütjen, S. Soltek, H. Bluethmann, and D. Schlüter. 2007. Interleukin-1 receptor type 1 is essential for control of cerebral but not systemic listeriosis. Am. J. Pathol. 170: 990-1002.
74. Getts, D. R., R. L. Terry, M. T. Getts, M. Müller, S. Rana, B. Shrestha, J. Radford, N. Van Rooijen, I. L. Campbell, and N. J. King. 2008. Ly6c+ "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J. Exp. Med. 205: 2319-2337.
75. Lim, J. K., D. H. McDermott, A. Lisco, G. A. Foster, D. Krysztof, D. Follmann, S. L. Stramer, and P. M. Murphy. 2010. CCR5 deficiency is a risk factor for early clinical manifestations of West Nile virus infection but not for viral transmission. J. Infect. Dis. 201: 178-185.
76. Lim, J. K., and P. M. Murphy. 2011. Chemokine control of West Nile virus infection. Exp. Cell Res. 317: 569-574.
77. Savarin, C., S. A. Stohlman, R. Atkinson, R. M. Ransohoff, and C. C. Bergmann. 2010. Monocytes regulate T cell migration through the glia limitans during acute viral encephalitis. J. Virol. 84: 4878-4888.
78. Ahn, B. J., H. J. Lee, M. W. Shin, J. H. Choi, J. W. Jeong, and K. W. Kim. 2009. Ninjurin1 is expressed in myeloid cells and mediates endothelium adhesion in the brains of EAE rats. Biochem. Biophys. Res. Commun. 387: 321-325.
79. Ahn, B. J., H. Le, M. W. Shin, S. J. Bae, E. J. Lee, H. J. Wee, J. H. Cha, J. H. Park, H. S. Lee, H. J. Lee, et al. 2012. The N-terminal ectodomain of Ninjurin1 liberated by MMP9 has chemotactic activity. Biochem. Biophys. Res. Commun. 428: 438-444.
80. Chang, D. M., and M. F. Shaio. 1994. Production of interleukin-1 (IL-1) and IL-1 inhibitor by human monocytes exposed to dengue virus. J. Infect. Dis. 170: 811-817.
81. Barros, V. E., B. R. Ferreira, M. Livonesi, and L. T. Figueiredo. 2009. Cytokine and nitric oxide production by mouse macrophages infected with Brazilian flaviviruses. Rev. Inst. Med. Trop. Sao Paulo 51: 141-147.
82. Ben-Sasson, S. Z., A. Hogg, J. Hu-Li, P. Wingfield, X. Chen, M. Crank, S. Caucheteux, M. Ratner-Hurevich, J. A. Berzofsky, R. Nir-Paz, and W. E. Paul. 2013. IL-1 enhances expansion, effector function, tissue localization, and memory response of antigen-specific CD8 T cells. J. Exp. Med. 210: 491-502.
83. Phares, T. W., S. A. Stohlman, D. R. Hinton, and C. C. Bergmann. 2012. Enhanced CD8 T-cell anti-viral function and clinical disease in B7-H1-deficient mice requires CD4 T cells during encephalomyelitis. J. Neuroinflammation 9: 269.
84. Saxena, A., W. Chen, Y. Su, V. Rai, O. U. Uche, N. Li, and N. G. Frangogiannis. 2013. IL-1 induces proinflammatory leukocyte infiltration and regulates fibroblast phenotype in the infarcted myocardium. J. Immunol. 191: 4838-4848.