Transgenic expression of IFN-α in the central nervous system of mice protects against lethal neurotropic viral infection but induces inflammation and neurodegeneration

Journal of Immunology

Volumn 161, Issue 9, 1998, Pages 5016-5026

  Akwa, Yvette ^a   Hassett, Daniel E ^a   Eloranta, Maija Leena ^b   Sandberg, Kristian ^c   Masliah, Eliezer ^d   Powell, Henry ^d   Whitton, J Lindsay ^a   Bloom, Floyd E ^a   Campbell, Iain L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c Astra Arcus AB   (Sweden)

^d UNIVERSITY OF SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL PROTECTION; CENTRAL NERVOUS SYSTEM; GLIOSIS; INFLAMMATION; MINERALIZATION; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SURVIVAL RATE; T LYMPHOCYTE ACTIVATION; VIRUS INFECTION; VIRUS REPLICATION;

ANIMALS; ASTROCYTES; B-LYMPHOCYTES; CALCINOSIS; CD4-POSITIVE T-LYMPHOCYTES; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; INTERFERON-ALPHA; LYMPHOCYTIC CHORIOMENINGITIS; MENINGOENCEPHALITIS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; TRANSGENES; VIRAL LOAD;

EID: 0032211097     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Baron, S., S. K. Tyring, W. R. Fleischmann, D. H. Coppenhaver, D. W. Niesel, G. R. Klimpel, G. J. Stanton, and T. K. Hughes. 1991. The interferons: mechanisms of action and clinical applications. J. Am. Med. Assoc. 266:1375.
2. Gutterman, J. U. 1994. Cytokine therapeutics: lessons from interferon α. Proc. Natl. Acad. Sci. USA 91:1198.
3. Pestka, S., J. A. Langer, K. C. Zoon, and C. E. Samuel. 1987. Interferons and their actions. Annu. Rev. Biochem. 56:727.
4. Belardelli, F., and I. Gresser. 1996. The neglected role of type 1 interferon in the T-cell response: implications for its clinical use. Immunol. Today 17:369.
5. Samuel, C. E. 1991. Antiviral actions of interferon: interferon-regulated cellular proteins and their surprisingly selective antiviral activities. Virology 183:1.
6. Muller, U., U. Steinhoff, L. F. L. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918.
7. Sandberg, K., M.-L. Eloranta, and I. L. Campbell. 1994. Expression of α/β interferons (IFN-α/β) and their relationship to IFN-α/β-induced genes in lymphocytic choriomeningitis. J. Virol. 68:7358.
8. Lieberman, A. P., P. M. Pitha, H. S. Shin, and M. L. Shin. 1989. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc. Natl. Acad. Sci. USA 86:6348.
9. Akiyama, H., K. Ikeda, M. Katoh, E. G. McGeer, and P. L. McGeer. 1994. Expression of MRP14, 27E10, interferon-α, and leukocyte common antigen by reactive microglia in postmortem human brain tissue. J. Neuroimmunol. 50:195.
10. Weinstock-Guttman, B., R. M. Ransohoff, R. P. Kinkel, and R. A. Rudick. 1995. The interferons: biological effects, mechanisms of action, and use in multiple sclerosis. Ann. Neurol. 37:7.
11. Bocci, V. 1988. Central nervous system toxicity of interferons and other cytokines. J. Biol. Regul. Homeostat. Agents 2:107.
12. Tolmie, J. L., P. Shillito, R. Hughes-Benzie, and J. B. P. Stephenson. 1995. The Aicardi-Goutières syndrome (familial, early onset encephalopathy with calcifications of the basal ganglia and chronic cerebrospinal fluid lymphocytosis). J. Med. Genet. 32:881.
13. Kumar, D., C. Rittey, A. H. Cameron, and S. Variend. 1998. Recognizable inherited syndrome of progressive central nervous system degeneration and generalized intracranial calcification with overlapping phenotype of the syndrome of Aicardi and Goutières. Am. J. Med. Genet. 75:508.
14. Lebon, P., J. Badoual, G. Ponsot, F. Goutières, F. Hemeury-Cukier, and J. Aicardi. 1988. Intrathecal synthesis of interferon-α in infants with progressive familial encephalopathy. J. Neurol. Sci. 84:201.
15. Black, D. N., G. V. Watters, E. Andermann, C. Dumont, M. E. Kabay, P. Kaplan, K. Meagher-Villemure, J. Michaud, G. O'Gorman, E. Reece, C. Tsoukas, and M. A. Wainberg. 1988. Encephalitis among Cree children in Northern Quebec. Ann. Neurol. 24:483.
16. Campbell, I. L., C. R. Abraham, E. Masliah, P. Kemper, J. D. Inglis, M. B. A. Oldstone, and L. Mucke. 1993. Neurologic disease induced in transgenic mice by the cerebral overexpression of interleukin 6. Proc. Natl. Acad. Sci. USA 90:10061.
17. Chiang, C-S., H. C. Powell, L. Gold, A. Samimi, and I. L. Campbell. 1996. Macrophage/microglial-mediated primary demyelination and motor disease induced by the central nervous system production of interleukin-3 in transgenic mice. J. Clin. Invest. 97:1512.
18. + RNA. BioTechniques 6:114.
19. Benoist, C. O., D. J. Mathis, M. R. Kanter, V. E. Williams, and H. O. McDevitt. 1983. Regions of allelic hypervariability in the murine A α immune response gene. Cell 34:169.
20. Tokunaga, K., H. Taniguchi, K. Yoda, M. Shimizu, and S. Sakiyama. 1986. Nucleotide sequence of a full-length cDNA for mouse cytoskeletal β-actin mRNA. Nucleic Acids Res. 14:2829.
21. Yu, N., J.-L. Martin, N. Stella, and P. J. Magistretti. 1993. Arachidonic acid stimulates glucose uptake in cerebral cortical astrocytes. Proc. Natl. Acad. Sci. USA 90:4042.
22. Riffault, S., M.-L. Eloranta, C. Carrat, K. Sandberg, B. Charley, and G. V. Alm, 1996. Herpes simplex virus induces appearance of interferon-α/β-producing cells and partially interferon-α/β-dependent accumulation of leukocytes in murine regional lymph nodes. J. Interferon Cytokine Res. 16:1007.
23. Wilson, M. C., and G. A. Higgins. 1989. In situ hybridization. Neuromethods 16:239.
24. Dahl, L. K. 1952. A simple and sensitive histochemical method for calcium. Proc. Soc. Exp. Biol. Med. 80:474.
25. Toggas, S. M., E. Masliah, E. M. Rockenstein, G. F. Rall, C. R. Abraham, and L. Mucke. 1994. Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367:188.
26. Dutko, F. J., and M. B. A. Oldstone. 1983. Genomic and biological variation among commonly used lymphocytic choriomeningitis virus strains. J. Gen. Virol. 64:1689.
27. Ahmed, R., A. Salmi, L. D. Butler, J. M. Chiller, and M. B. A. Oldstone. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. J. Exp. Med. 60:521.
28. Byrne, J. A., R. Ahmed, and M. B. A. Oldstone. 1984. Biology of cloned cytotoxic T lymphocytes specific for lymphocytic choriomeningitis virus: generation and recognition of virus strains and H-2b mutants. J. Immunol. 133:433.
29. Moss, J., D. F. Woodrow, J. C. Guillon, and I. Gresser. 1982. Tubular aggregates and interferon. Lancet 2:1277.
30. Luu, J., D. Bockus, F. Remington, M. A. Bean, and S. P. Hammar. 1989. Tubuloreticular structures and cylindrical confronting cisternae. Hum. Pathol. 20: 617.
31. Steffen, B. J., G. Breier, E. C. Butcher, M. Schulz, and B. Engelhardt. 1996. ICAM-1, VCAM-1, and MAdCAM-1 are expressed on choroid plexus epithelium but not endothelium and mediate binding of lymphocytes in vitro. Am. J. Pathol. 148:1819.
32. Butcher, E. C. 1990. Cellular and molecular mechanisms that direct leukocyte traffic. Am. J. Pathol. 136:3.
33. Buchmeier, M. J., R. M. Welsh, F. J. Dutko, and M. B. Oldstone. 1980. The virology and immunobiology of lymphocytic choriomeningitis virus infection. Adv. Immunol. 30:275.
34. Wyss-Coray, T., P. Borrow, M. J. Brooker, and L. Mucke. 1997. Astroglial overproduction of TGF-β1 enhances inflammatory central nervous system disease in transgenic mice. J. Neuroimmunol. 77:45.
35. Dussaix, E., P. Lebon, G. Ponsot, G. Huault, and M. Tardieu. 1985. Intrathecal synthesis of different α-interferons in patients with various neurological diseases. Acta Neurol. Scand. 7:504.
36. Hekman, A. C., J. Trapman, A. H. Mulder, J. L. van Gaalen, and E. C. Zwarthoff. 1988. Interferon expression in the testes of transgenic mice leads to sterility. J. Biol. Chem. 263:12151.
37. Corbin, J. G., D. Kelly, E. M. Rath, K. D. Baerwald, K. Suzuki, and B. Popko. 1996. Targeted CNS expression of interferon-γ in transgenic mice leads to hypomyelination, reactive gliosis, and abnormal cerebellar development. Mol. Cell. Neurosci. 7:354.
38. Horwitz, M. S., C. F. Evans, D. B. McGavern, M. Rodriguez, and M. B. A. Oldstone. 1997. Primary demyelination in transgenic mice expressing IFN-γ. Nat. Med. 3:1037.
39. Moss, J., D. F. Woodrow, J. C. Sloper, Y. Riviere, J. C. Guillon, and I. Gresser. 1982. Interferon as a cause of endoplasmic reticulum abnormalities within hepatocytes in newborn mice. Br. J. Exp. Pathol. 63:43.
40. Grimley, P. M., S. Ray, M. Kostianovsky, B. Rupp, Y.-H. Kang, and D. Feldman. 1988. Tubuloreticular reorganization of cytomembranes in cells treated with human α interferons. Scanning Microsc. 2:2141.
41. Mirra, S. S., and C. del Rio. 1989. The fine structure of acquired immunodeficiency syndrome encephalopathy. Arch. Pathol. Lab. Med. 113:858.
42. Wegiel, J., and H. M. Wisniewski. 1992. Tubuloreticular structures in microglial cells, pericytes, and endothelial cells in Alzheimer's disease. Acta Neuropathol. 83:653.
43. Belardelli, F. 1995. Role of interferons and other cytokines in the regulation of the immune response. APMIS 103:161.
44. Hall, G. L., A. Compston, and N. J. Scolding. 1997. β-interferon and multiple sclerosis. Trends Neurosci. 20:63.
45. Arnason, B. 1995. The role of cytokines in multiple sclerosis. Neurology 45(Suppl. 6):S54.
46. Stewart, T. A., B. Hultgren, X. Huang, S. Pitts-Meek, J. Hully, and N. J. MacLachlan. 1993. Induction of type I diabetes by interferon-α in transgenic mice. Science 260:1942.
47. Aicardi, J., and F. Goutières. 1984. A progressive familial encephalopathy in infancy with calcifications of the basal ganglia and chronic cerebrospinal fluid lymphocytosis. Ann. Neurol. 15:49.
48. Gendelman, H. E., D. R. Skillman, and M. S. Meltzer. 1992. Interferon α (IFN)-macrophage interactions in human immunodeficiency virus (HIV) infection: role of IFN in the tempo and progression of HIV disease. Intern. Rev. Immunol. 8:43.
49. Gresser, I., M. G. Tovey, C. Maury, and M.-T. Bandu. 1976. Role of interferon in the pathogenesis of virus diseases in mice as demonstrated by the use of anti-interferon serum. J. Exp. Med. 144:1316.
50. Baron, S., D. Weigent, G. J. Stanton, and J. Peterson. 1985. The protective role of endogenous interferon in viral, bacterial, and protozoal infections. Antiviral Res. 1:173.
51. Pfau, C. J., I. Gresser, and K. D. Hunt. 1983. Lethal role of interferon in lymphocytic choriomeningitis virus-induced encephalitis. J. Gen. Virol. 64:1827.
52. Sandberg, K., P. Kemper, A. Stalder, J. Zhang, M. V. Hobbs, J. L. Whitton, and I. L. Campbell. 1994. Altered tissue distribution of viral replication and T-cell spreading is pivotal in the protection against fatal lymphocytic choriomeningitis in mice after neutralization of IFN-αβ. J. Immunol. 153:220.
53. Fujii, N. 1994. 2-5A and virus infection. Prog. Mol. Subcell. Biol. 14:150.
54. Baenziger, J., H. Hengartner, R. M. Zinkernagel, and G. A. Cole. 1986. Induction or prevention of immunopathologic disease by cytotoxic T cell lines specific for lymphocytic choriomeningitis virus. Eur. J. Immunol. 16:387.