Interleukin-1 mediates a rapid inflammatory response after injection of adenoviral vectors into the brain

Journal of Neuroscience

Volumn 19, Issue 4, 1999, Pages 1517-1523

  Cartmell, Tammy ^a   Southgate, Tom ^a   Rees, Gwen S ^b   Castro, Maria G ^a   Lowenstein, Pedro R ^a   Luheshi, Giamal N ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

Adenovirus; Brain; Cytokines; Fever; Inflammation; Rat

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; VIRUS VECTOR;

ADENOVIRUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; BRAIN VENTRICLE; CYTOKINE RELEASE; ENCEPHALITIS; FEVER; GENE EXPRESSION; GENE TRANSFER; MALE; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSGENE;

EID: 0033557657     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-04-01517.1999     Document Type: Article

References (44)

1. Adesanya MR, Redman RS, Baum BJ, O'Connell BC (1996) Immediate inflammatory responses to adenovirus-mediated gene transfer in rat salivary glands. Hum Gene Ther 7:1085-1093.
2. Alcami A, Smith GL (1996) A mechanism for the inhibition of fever by a virus. Proc Natl Acad Sci USA 93:11029-11034.
3. Bajocchi G, Feldman SH, Crystal RG, Mastrangeli A (1993) Direct in vivo gene transfer to ependymal cells in the central nervous system using recombinant adenovirus vectors. Nat Genet 3:229-234.
4. Blomer U, Naldini L, Kafri T, Trono D, Verma IM, Gage FH (1997) Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. J Virol 71:6641-6649.
5. Bruder JT, Kovesdi I (1997) Adenovirus infection stimulates the Raf/ MAPK signaling pathway and induces interleukin-8 expression. J Virol 71:398-404.
6. Byrnes AP, MacLaren RE, Charlton HM (1996a) Immunological instability of persistent adenovirus vectors in the brain: peripheral exposure to vector leads to renewed inflammation, reduced gene expression, and demyelination. J Neurosci 16:3045-3055.
7. Byrnes AP, Wood MJ, Charlton HM (1996b) Role of T cells in inflammation caused by adenovirus vectors in the brain. Gene Ther 3:644-651.
8. Chen SH, Shine HD, Goodman JC, Grossman JC, Grossman RG, Woo SLC (1994) Gene therapy for brain tumors. Regression of experimental gliomas by adenovirus-mediated gene transfer in vivo. Proc Natl Acad Sci USA 91:3054-3057.
9. Choi-Lundberg DL, Lin Q, Chang YN, Chiang YL, Hay CM, Mohajeri H, Davidson BL, Bohn MC (1997) Dopaminergic neurons protected from degradation by GDNF gene therapy. Science 275:838-841.
10. Cotten M, Baker A, Saltik M, Wagner E, Buschle M (1994) Lipopolysaccharide is a frequent contaminant of plasmid DNA preparations and can be toxic to primary human cells in the presence of adenovirus. Gene Ther 1:239-246.
11. David A, Chetritt J, Coupel H, Tesson L, Cassard A, Blancho G, Charreau B, Charreau JB, Sigalla J, Buzelin F, Le Mauff B, Soulillou JP, Anegon I (1997) Adenovirus-mediated gene transfer in rat liver of interleukin 4 but not interleukin 10 produces severe acute hepatitis. Cytokine 9:818-829.
12. Devergne O, Peuchmaur M, Humbert M, Navratil E, Leger-Ravet MB, Crevon MC, Petit MA, Galanaud P, Emilie D (1991) In vivo expression of IL-1 beta and IL-6 genes during viral infections in human. Eur Cytokine Netw 2:183-194.
13. Dewey RA, Southgate T, Morelli A, Klatzmann D, Castro MG, Lowenstein PR (1998) Adenoviral-mediated suicide gene therapy using the CNS-1 rat glioma model. Soc Neurosci Abstr 24:859.9.
14. Eck SL, Alavi JB, Alavi A, Davis A, Hackney D, Judy K, Mollman J, Phillips PC, Wheeldon EB, Wilson JM (1996) Treatment of advanced CNS malignancies with the recombinant adenovirus H5.010RSVTK: a phase 1 trial. Hum Gene Ther 7:1465-1482.
15. Eisenberg SP, Evans RJ, Arend WP, Verderber E, Brewer MT, Hannum CH, Thompson RC (1990) Primary structure and functional expression from complementary DNA of a human interleukin-1 receptor antagonist. Nature 343:341-346.
16. Elkon KB, Liu CC, Gall JG, Trevejo J, Marino MW, Abrahamsen KA, Song X, Zhou JL, Old LJ, Crystral RG, Falck-Pedersen E (1997) Tumor necrosis factor alpha plays a central role in immune-mediated clearance of adenoviral vectors. Proc Natl Acad Sci USA 94:9814-9819.
17. Elmquist JK, Scammell TE, Saper CB (1997) Mechanisms of CNS response to systemic immune challenge: the febrile response. Trends Neurosci 20:565-570.
18. Geddes BJ, Harding TC, Lightman SL, Uney JB (1997) Long-term gene therapy in the CNS: reversal of hypothalamic diabetes insipidus in Brattleboro rat by using an adenovirus expressing arginine vasopressin. Nat Med 3:1402-1404.
19. Ginsberg HS, Moldawer LL, Sehgal PB, Redington M, Kilian PL, Chanock RM, Prince GA (1991) A mouse model for investigating the molecular pathogenesis of adenovirus pneumonia. Proc Natl Acad Sci USA 88:1651-1655.
20. Hermens WT, Verhaagen J (1997) Adenoviral vector-mediated gene expression in the nervous system of immunocompetent Wistar and T cell-deficient nude rats: preferential survival of transduced astroglial cells in nude rats. Hum Gene Ther 8:1049-1063.
21. Klir JJ, Roth J, Szelenyi Z, McClellan JL, Kluger MJ (1993) Role of hypothalamic interleukin-6 and tumor necrosis factor-α in LPS-fever in rat. Am J Physiol 265:R512-R517.
22. Klir JJ, McClellan JL, Kluger MJ (1994) Interleukin-1β causes the increase in anterior hypothalamic interleukin-6 during LPS-induced fever in rats. Am J Physiol 266:R1845-R1848.
23. Kluger MJ (1991) Fever: the role of pyrogens and cryogens. Physiol Rev 71:93-127.
24. Lieber A, He CY, Meuse L, Schowalter D, Kirillowva I, Winther B, Kay MA (1997) The role of Kupffer cell activation and viral gene expression in early liver toxicity after infusion of recombinant adenovirus vectors. J Virol 71:8798-8807.
25. Liu J, Marino MW, Wong G, Grail D, Dunn A, Bettadapura J, Slavin AJ, Old L, Bernard CC (1998) TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat Med 4:78-83.
26. Lowenstein PR, Wilkinson GWG, Castro MG, Shering AF, Fooks AR, Bain D (1996) Non-neurotropic adenovirus: a vector for gene transfer to the brain and possible gene therapy of neurological disorders. In: Genetic manipulation of the nervous system (Latchman DS, ed), pp 11-39. London: Academic.
27. Luheshi GN, Stefferl A, Turnbull AV, Dascombe MJ, Brouwer S, Hopkins SJ, Rothwell NJ (1997) Febrile response to tissue inflammation involves both peripheral and brain IL-1 and TNF-α in the rat. Am J Physiol 272:R862-R868.
28. McCoy RD, Davidson BL, Roessler BJ, Huffnagle GB, Janich SL, Laing TJ, Simon RH (1995) Pulmonary inflammation induced by incomplete or inactivated adenoviral particles. Hum Gene Ther 6:1553-1560.
29. Morelli AE, Larregina AT, Smith-Arica J, Dewey RA, Southgate TD, Ambar B, Fontana A, Castro MG, Lowenstein PR (1999) Neuronal and glial cell-type specific promoters within adenovirus recombinants restrict the expression of the apoptosis inducing molecule Fas ligand to predetermined brain cell types, and abolish peripheral liver toxicity. J Gen Virol, in press.
30. Paxinos G, Watson C (1986) The rat brain in stereotaxic co-ordinates. Sydney: Academic.
31. Rees GS, Ball C, Ward HL, Gee CK, Tarrant G, Mistry Y, Poole S, Bristow AF (1998) Rat interleukin 6: expression in recombinant Eschenchia coli, purification and development of a novel ELISA. Cytokine, in press.
32. Safieh-Garahedian B, Poole S, Allchorne A, Winter J, Woolf CJ (1995) Contribution of interleukin-1β to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br J Pharmacol 115:1265-1275.
33. Shering AF, Bain D, Stewart S, Epstein AL, Castro MG, Wilkinson GWG, Lowenstein PR (1997) Cell type-specific expression in brain cell cultures from a short human cytomegalovirus major immediate early promoter depends on whether it is inserted into herpesvirus or adenovirus vectors. J Gen Virol 78:445-459.
34. Stefferl A, Hopkins SJ, Rothwell NJ, Luheshi GN (1996) The role of TNF-α in fever: opposing actions of human and murine TNF-α and interactions with IL-1β in the rat. Br J Pharmacol 118:1919-1924.
35. Stevenson PG, Freeman S, Bangham CR, Hawke S (1997a) Virus dissemination through the brain parenchyma without immunologic control. J Immunol 159:1876-1884.
36. Stevenson PG, Hawke S, Sloan DJ, Bangham CR (1997b) The immunogenicity of intracerebral virus infection depends on anatomical site. J Virol 71:145-151.
37. Takao T, Tracey DE, Mitchell WM, De Souza EB (1990) Interleukin-1 receptors in mouse brain: characterisation and neuronal localization. Endocrinology 127:3070-3078.
38. Tringali G, Mancuso C, Mirtella A, Pozzoli G, Parente L, Preziosi P, Navarra P (1996) Evidence for the neuronal origin of immunoreactive interleukin-1 beta released by rat hypothalamic explants. Neurosci Lett 219:143-146.
39. Wilkinson GW, Akrigg A (1992) Constitutive and enhanced expression from the CMV major IE promoter in a defective adenovirus vector. Nucleic Acids Res 20:2233-2239.
40. Wood MJ, Charlton HM, Wood KJ, Kajiwara K, Byrnes AP (1996) Immune responses to adenovirus vectors in the nervous system. Trends Neurosci 19:497-501.
41. Worgall S, Wolff G, Falck-Pedersen E, Crystal RG (1997) Innate immune mechanisms dominate elimination of adenoviral vectors following in vivo administration. Hum Gene Ther 8:37-44.
42. Yabuuchi K, Minami M, Katsumata S, Satoh M (1994) Localization of type I interleukin-1 receptor mRNA in the rat brain. Mol Brain Res 27:27-36.
43. Zampronio AR, Souza GE, Silva CA, Cunha FQ, Ferreira SH (1994) Interleukin-8 induces fever by a proslaglandin-independent mechanism. Am J Physiol 266:R1670-R1674.
44. Zsengeller ZK, Wert SE, Hull WM, Hu X, Yei S, Trapnell BC, Whitsett JA (1995) Persistence of replication-deficient adenovirus-mediated gene transfer in lungs of immune-deficient (nu/nu) mice. Hum Gene Ther 6:457-467.