Infection of neonatal mice with sindbis virus results in a systemic inflammatory response syndrome

Journal of Virology

Volumn 73, Issue 12, 1999, Pages 10387-10398

  Klimstra, W B ^a   Ryman, K D ^a   Bernard, K A ^a   Nguyen, K B ^b   Biron, C A ^b   Johnston, R E ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; COMPLEMENTARY DNA; CORTICOSTERONE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; GAMMA INTERFERON; HEPARAN SULFATE; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRAIN BHK; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HISTOPATHOLOGY; IN SITU HYBRIDIZATION; MOLECULAR CLONING; MORTALITY; MOUSE; NEWBORN; NEWBORN INFECTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SEPTIC SHOCK; SINDBIS VIRUS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; VIRUS ENCEPHALITIS; VIRUS INFECTION; VIRUS ISOLATION; VIRUS VIRULENCE;

EID: 0032757364     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.12.10387-10398.1999     Document Type: Article

References (64)

1. American College of Chest Physicians/Society of Critical Care Medicine. 1992. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit. Care Med. 1992:864-874.
2. Billiau, A., and F. Vandekerckhove. 1991. Cytokines and their interactions with other inflammatory mediators in the pathogenesis of sepsis and septic shock. Eur. J. Clin. Investig. 21:559-573.
3. Bohlinger, I., M. Leist, F. Gantner, S. Angelmuller, G. Tiegs, and A. Wendel. 1996. DNA fragmentation in mouse organs during endotoxic shock. Am. J. Pathol. 149:1381-1393.
4. Calandra, T., J.-D. Baumgartner, G. E. Grau, M.-M. Wu, P.-H. Lambert, J. Schellekens, J. Verhoef, M. P. Glauser, and The Swiss-Dutch J5 Immunoglobulin Study Group. 1990. Prognostic values of tumor necrosis factor/cachectin, interleukin-1, interferon-alpha, and interferon-gamma in the serum of patients with septic shock. J. Infect. Dis. 161:982-987.
5. Davies, M. G., and P.-O. Hagen. 1997. Systemic inflammatory response syndrome. Br. J. Surg. 84:920-935.
6. Dealtry, G. B., M. S. Naylor, W. Fiers, and F. R. Balkwill. 1987. DNA fragmentation and cytotoxicity caused by tumor necrosis factor is enhanced by interferon-gamma. Eur. J. Immunol. 17:689-693.
7. Doherty, G. M., J. R. Lange, H. N. Langstein, H. R. Alexander, C. M. Buresh, and J. A. Norton. 1992. Evidence for IFN-gamma as a mediator of the lethality of endotoxin and tumor necrosis factor-alpha. J. Immunol. 149: 1666-1670.
8. Grau, G., L. F. Fajardo, P.-F. Piguet, B. Allet, P.-H. Lambert, and P. Vassalli. 1987. Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science 237:210-213.
9. Gresser, I., D. Woodrow, J. Moss, C. Maury, J. Tavernier, and W. Fiers. 1987. Toxic effects of recombinant tumor necrosis factor in suckling mice. Am. J. Pathol. 128:13-18.
10. Gutierrez-Ramos, J. C., and H. Bluethmann. 1997. Molecules and mechanisms operating in septic shock: lessons from knockout mice. Immunol. Today 18:329-334.
11. Halmovitzfriedman, A., C. Cordoncardo, S. Bayoumy, M. Garzotto, M. McLoughlin, R. Gallily, C. K. Edwards, E. H. Schuchman, Z. Fuks, and R. Kolesnick. 1997. Lipopolysaccharide induces disseminated endothelial apoptosis requiring ceramide generation. J. Exp. Med. 186:1831-1841.
12. Hernandez-Caselles, T., and O. Stutman. 1993. Immune functions of tumor necrosis factor. I. Tumor necrosis factor induces apoptosis of mouse thymocytes and can also stimulate or inhibit IL-6-induced proliferation depending on the type of mitogenic costimulation. J. Immunol. 151:3999-4012.
13. Jan, J. T., A. P. Byrnes, and D. E. Giffin. 1999. Characterization of a Chinese hamster ovary cell line developed by retroviral insertional mutagenesis that is resistant to Sindbis virus infection. J. Virol. 73:4919-4924.
14. Johnson, R. T. 1965. Virus invasion of the central nervous system: a study of Sindbis virus infection of the mouse using fluorescent antibody. Am. J. Pathol. 46:929-943.
15. Johnson, R. T., H. F. McFarland, and S. E. Levy. 1972. Age-dependent resistance to viral encephalitis: studies of infections due to Sindbis virus in mice. J. Infect. Dis. 125:257-262.
16. Kato, Y., A. Morikawa, T. Sugiyama, N. Kolde, G.-Z. Jiang, T. Lwin, T. Yoshida, and T. Yokochi. 1997. Augmentation of lipopolysaccharide-induced thymocyte apoptosis by interferon-gamma. Cell. Immunol. 177:103-108.
17. Kato, Y., A. Morikawa, T. Sugiyama, N. Koide, G.-Z. Jiang, T. Takahashi, and T. Yokochi. 1995. Role of tumor necrosis factor-alpha and glucocorticoid on lipopolysaccharide (LPS)-induced apoptosis of thymocytes. FEMS Immunol. Med. Microbiol. 12:195-204.
18. Klimstra, W. B., H. W. Heidner, and R. E. Johnston. 1999. The furin protease cleavage recognition sequence of Sindbis virus PE2 can mediate virion attachment to cell surface heparan sulfate. J. Virol. 73:6299-6306.
19. Klimstra, W. B., K. D. Ryman, and R. E. Johnston. 1998. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J. Virol. 72:7357-7366.
20. Koff, W. C., and A. V. Fann. 1986. Human tumor necrosis factor-alpha kills herpesvirus-infected but not normal cells. Lymphokine Res. 5:215-221.
21. Krause, P. J., J. Kristie, W. P. Wang, L. Eisenfeld, V. C. Herson, E. G. Maderazo, K. Jozaki, and D. L. Kreutzer. 1987. Pentoxifylline enhancement of defective neutrophil function and host defense in neonatal mice. Am. J. Pathol. 129:217-222.
22. Laster, S. M., J. G. Wood, and L. R. Gooding. 1988. Tumor necrosis factor can induce both apoptotic and necrotic forms of cell lysis. J. Immunol. 141:2629-2634.
23. Levine, B., J. E. Goldman, H. H. Jiang, D. E. Griffin, and J. M. Hardwick. 1996. Bcl-2 protects mice against fatal alphavirus encephalitis. Proc. Natl. Acad. Sci. USA 93:4810-4815.
24. Levine, B., and D. E. Griffin. 1993. Molecular analysis of neurovirulent strains of Sindbis virus that evolve during persistent infection of scid mice. J. Virol. 67:6872-6875.
25. Li, P., H. Allen, S. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfield, E. Towne, D. Tracey, S. Wardwell, F.-Y. Wei, W. Wong, R. Kamen, and T. Seshardi. 1995. Mice deficient in IL-1B-converting enzyme are defective in production of mature IL-1B and resistant to endotoxic shock. Cell 80:401-411.
26. Liechty, K. W., K. R. Schibler, R. K. Ohls, S. L. Perkins, and R. D. Christensen. 1993. The failure of newborn mice infected with Escherichia coli to accelerate neutrophil production correlates with their failure to increase transcripts for granulocyte-colony stimulating factor and interleukin-6. Biol. Neonate 64:331-340.
27. Lustig, S., H. D. Danenberg, Y. Kafri, D. Kobiler, and D. Ben-Nathan. 1992. Viral neuroinvasion and encephalitis induced by lipopolysaccharide and its mediators. J. Exp. Med. 176:707-712.
28. Lustig, S., A. C. Jackson, C. S. Hahn, D. E. Griffin, E. G. Strauss, and J. H. Strauss. 1988. Molecular basis of Sindbis virus neurovirulence in mice. J. Virol. 62:2329-2336.
29. Mahlerbe, H., M. Strickland-Chomley, and A. L. Jackson. 1963 Sindbis virus infection in man: report of a case with recovery of virus from skin lesions. S. Afr. Med. J. 37:547-552.
30. Martin, T. R., J. T. Ruzinski, C. B. Wilson, and S. J. Skerrett. 1995. Effects of endotoxin in the lungs of neonatal rats: age-dependent impairment of the inflammatory response. J. Infect. Dis. 171:131-144.
31. McKnight, K. L., D. A. Simpson, S. C. Lin, T. A. Knott, J. M. Polo, D. F. Pence, D. B. Johannsen, H. W. Heidner, N. L. Davis, and R. E. Johnston. 1996. Deduced consensus sequence of Sindbis virus strain AR339: mutations contained in laboratory strains which affect cell culture and in vivo phenotypes. J. Virol. 70:1981-1989.
32. Merry, C., P. Puri, and D. J. Reen. 1996. Defective neutrophil actin polymerization and chemotaxis in stressed newborns. J. Pediatr. Surg. 31:481-485.
33. Morikawa, A., T. Sugiyama, Y. Kato, N. Kiode, G.-Z. Jiang, K. Takahashi, Y. Tamada, and T. Yokochi. 1996. Apoptotic cell death in the response of D-galactosamine-sensitized mice to lipopolysaccharide as an experimental endotoxic shock model. Infect. Immun. 64:734-738.
34. Nagano, I., S. Nakamura, M. Yoshioka, J. Onodera, K. Kogure, and Y. Itoyama. 1994. Expression of cytokines in brain lesions in subacute sclerosing panencephalitis. Neurology 44:710-715.
35. Nava, V. E., A. Rosen, M. A. Veliuona, R. J. Clem, B. Levine, and J. M. Hardwick. 1997. Sindbis virus induces apoptosis through a caspase-dependent CrmA-sensitive pathway. J. Virol. 72:452-459.
36. Nguyen, K. B., and C. A. Biron. 1999. Synergism for cytokine-mediated disease during concurrent endotoxin and viral challenges: role for NK and T cell IFN-γ production. J. Immunol. 162:5238-5246.
37. Ohno, K., T. Nakano, Y. Matsumoto, T. Watari, R. Goitsuka, H. Nakayama, H. Tsujimoto, and A. Hasegawa. 1993. Apoptosis induced by tumor necrosis factor in cells chronically infected with feline immunodeficiency virus. J. Virol. 67:2429-2433.
38. Orange, J. S., and C. A. Biron. 1996. An absolute and restricted requirement for IL-12 in natural killer cell IFN-gamma production and antiviral defense. J. Immunol. 156:1138-1142.
39. Orange, J. S., T. P. Salazar-Mather, S. M. Opal, and C. A. Biron. 1997. Mechanisms for virus-induced liver disease: tumor necrosis factor-mediated pathology independent of natural killer and T cells during murine cytomegalovirus infection. J. Virol. 71:9248-9258.
40. Polo, J. M., and R. E. Johnston. 1990. Attenuating mutations in glycoproteins E1 and E2 of Sindbis virus produce a highly attenuated strain when combined in vitro. J. Virol. 64:4438-4444.
41. Quagliarello, V. J., B. Wispelwey, W. J. J. Long, and W. M. Scheld. 1991. Recombinant interleukin-1 induces meningitis and blood brain barrier injury in the rat. Characterization and comparison with tumor necrosis factor. J. Clin. Investig. 87:1360-1366.
42. Relton, J. K., and N. J. Rothwell. 1992. Interleukin-1 receptor antagonist inhibits ischemic and excitotoxic neuronal damage in the rat. Brain Res. Bull. 29:243-246.
43. Rice, C. M., R. Levis, J. H. Strauss, and H. V. Huang. 1987. Production of infectious RNA transcripts from Sindbis virus cDNA clones: mapping of lethal mutations, rescue of a temperature-sensitive marker, and in vitro mutagenesis to generate defined mutants. J. Virol. 61:3809-3819.
44. Rood, P. A., R. M. Lorence, and K. W. Kelley. 1990. Serine protease inhibitor abrogation of Newcastle disease virus enhancement of cytolysis by recombinant tumor necrosis factors alpha and beta. J. Natl. Cancer Inst. 82:213-217.
45. Ruddle, N. H., C. M. Bergman, K. M. McGrath, E. G. Lingenheld, M. L. Grunnet, and S. J. Padula. 1990. An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J. Exp. Med. 172:1193-1200.
46. Ruzek, M. C., A. H. Miller, S. M. Opal, B. D. Pearce, and C. A. Biron. 1997. Characterization of early cytokine responses and an IL-6-dependent pathway of endogenous glucocorticoid induction during murine cytomegalovirus infection. J. Exp. Med. 185:1185-1192.
47. Ruzek, M. C., B. D. Pearce, A. H. Miller, and C. A. Biron. 1999. Endogenous glucocorticoids protect against cytokine-mediated lethality during viral infection. J. Immunol. 162:3527-3533.
48. Ryman, K. D., and R. E. Johnston. 1997. Unpublished observations.
49. Saukkonen, K., S. Sande, C. Cloffe, S. Wolpe, B. Sherry, A. Cerami, and E. Toumanan. 1990. The role of cytokines in the generation of inflammation and tissue damage in experimental gram-positive meningitis. J. Exp. Med. 171:439-448.
50. Shapria, L., W. A. Soskolne, Y. Houri, V. Barak, A. Halabi, and A. Stabholz. 1996. Protection against endotoxic shock and lipopolysaccharide-induced local inflammation by tetracycline: correlation with inhibition of cytokine secretion. Infect. Immun. 64:825-828.
51. Sherman, L. A., and D. E. Griffin. 1990. Pathogenesis of encephalitis induced in newborn mice by virulent and avirulent strains of Sindbis virus. J. Virol. 64:2041-2046.
52. Simpson, D. A., N. L. Davis, S. C. Lin, D. Russell, and R. E. Johnston. 1996. Complete nucleotide sequence and full-length cDNA clone of S.A.AR86, a South African alphavirus related to Sindbis. Virology 222:464-469.
53. Skultetyova, I., D. I. Tokarev, and D. Jezova. 1993. Albumin content in the developing rat brain in relation to the blood-brain barrier. Endocr. Regul. 27:209-213.
54. Slowik, M. R., W. Min, T. Ardito, A. Karsan, M. Kashagarian, and J. S. Pober. 1997. Evidence that tumor necrosis factor triggers apoptosis in human endothelial cells by interleukin-1-converting enzyme-like protease-depenO dent and -independent pathways. Lab. Investig. 77:257-267.
55. Strauss, J. H., and E. G. Strauss. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
56. Talley, A., S. Perry, L. G. Epstein, and H. A. Gelbard. 1994. TNFa-mediated apoptosis in SK-N-MC neuroblastoma cells: a model for neuronal cell loss in HIV-1-associated dementia. Ann. Neurol. 36:506-507.
57. Taylor, R. M., H. S. Hurlbut, T. H. Work, J. R. Kingston, and T. E. Rothingham. 1955. Sindbis virus: a newly recognized arthropod-transmitted virus. Am. J. Trop. Med. Hyg. 4:844-862.
58. Torti, F. M., B. Dieckmann, B. Beutler, A. Cerami, and G. M. Ringold. 1985. A macrophage factor inhibits adipocyte gene expression: an in vitro model of cachexia. Science 229:867-869.
59. Tracey, K. J., B. Beutler, S. F. Lowry, J. Merryweather, S. Wolpe, I. W. Mllsark, R. J. Hariri, T. J. Fahey, A. Zentella, J. D. Albert, G. T. Shires, and A. Cerami. 1986. Shock and tissue injury induced by recombinant human cachectin. Science 234:470-474.
60. Tracey, K. J., Y. Fong, D. G. Hesse, K. R. Manogue, A. T. Lee, G. C. Kuo, S. F. Lowry, and A. Cerami. 1987. Anti cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia. Nature 330:662-664.
61. Trgovcich, J., J. F. Aronson, and R. E. Johnston. 1996. Fatal Sindbis virus infection of neonatal mice in the absence of encephalitis. Virology 224:73-83.
62. Trgovcich, J., and R. E. Johnston. TNF α, interferon and stress response induction as a function of age-related susceptibility to fatal Sindbis virus infection of mice. Virology, in press.
63. Trgovcich, J., K. Ryman, P. Extrom, J. C. Eldridge, J. F. Aronson, and R. E. Johnston. 1997. Sindbis virus infection of neonatal mice results in a severe stress response. Virology 227:234-238.
64. Tucker, P. C., E. G. Strauss, R. J. Kuhn, J. H. Strauss, and D. E. Griffin. 1993. Viral determinants of age-dependent virulence of Sindbis virus for mice. J. Virol. 67:4605-4610.