Blood-brain barrier changes and cell invasion differ between therapeutic immune clearance of neurotrophic virus and CNS autoimmunity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 40, 2008, Pages 15511-15516

  Fabis, Marzena J ^a,b   Phares, Timothy W ^a,c   Kean, Rhonda B ^a,b   Koprowski, Hilary ^a,b   Hooper, D Craig ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

CNS inflammation; Experimental allergic encephalomyelitis; Neuroimmunology; Peroxynitrite dependent radicals; Rabies virus

Indexed keywords

BIOLOGICAL MARKER; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 17; MESSENGER RNA; MYELIN BASIC PROTEIN; PEROXYNITRITE; SCAVENGER; URATE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; BLOOD BRAIN BARRIER; CD4+ T LYMPHOCYTE; CELL ACTIVITY; CELL INVASION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CLEARANCE; CLINICAL FEATURE; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG ACTIVITY; FEMALE; GENE EXPRESSION; IMMUNIZATION; INFLAMMATORY DISEASE; MOUSE; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NONHUMAN; PARENCHYMA; PERMEABILITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABIES; RABIES VIRUS; SPINAL CORD;

ANIMALS; AUTOIMMUNITY; BLOOD-BRAIN BARRIER; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM; CEREBELLUM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FREE RADICAL SCAVENGERS; IMMUNOHISTOCHEMISTRY; INTERFERON-GAMMA; INTERLEUKIN-17; MICE; MICE, INBRED STRAINS; NITRIC OXIDE SYNTHASE; PEROXYNITROUS ACID; RABIES; RABIES VIRUS;

ANIMALIA; MUS; RABIES VIRUS;

EID: 55749111902     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0807656105     Document Type: Article

References (28)

1. Grossman RI, Gonzalez-Scarano F, Atlas SW, Galetta S, Silberberg DH (1986) Multiple sclerosis: Gadolinium enhancement in MR imaging. Radiology 16:721-725.
2. Hooper DC, et al. (2000) Uric acid, a peroxynitrite scavenger, inhibits CNS inflammation, blood-CNS barrier permeability, and tissue damage in amouse model of multiple sclerosis. FASEB J 14:691-698.
3. Kean RB, Spitsin SV, Mikheeva T, Scott GS, Hooper DC (2000) The peroxynitrite scavenger uric acid prevents inflammatory cell invasion into the central nervous system in experimental allergic encephalomyelitis through maintenance of blood-central nervous system barrier integrity. J Immunol 165:6511-6518.
4. Paul C, Bolton C (2002) Modulation of blood-brain barrier dysfunction and neurological deficits during acute experimental allergic encephalomyelitis by the N-methyl-D-aspartate receptor antagonist memantine. J Pharmacol Exp Ther 302:50-57.
5. Floris S, et al. (2004) Blood-brain barrier permeability and monocyte infiltration in experimental allergic encephalomyelitis: A quantitative MRI study. Brain 127:616-627.
6. Fabis MJ, Scott GS, Kean RB, Koprowski H, Hooper DC (2007) Loss of blood-brain barrier integrity in the spinal cord is common to experimental allergic encephalomyelitis in knockout mouse models. Proc Natl Acad Sci USA 104:5656-5661.
7. Hooper DC, et al. (2001) The central nervous system inflammatory response to neurotrophic virus infection is peroxynitrite dependent. J Immunol 167:3470-3477.
8. Phares TW, Kean RB, Mikheeva T, Hooper DC (2006) Regional differences in blood-brain barrier permeability changes and inflammation in the apathogenic clearance of virus from the central nervous system. J Immunol 176:7666-7675.
9. Hooper DC, et al. (1998) Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system. J Virol 72:3711-3719.
10. Juhler M, et al. (1984) Blood-brain and blood-spinal cord barrier permeability during the course of experimental allergic encephalomyelitis in the rat. Brain Res 302:347-355.
11. Patterson CE, Rhoades RA, Garcia JGN (1992) Evans blue dye as a marker of albumin clearance in cultured endothelial monolayer and isolated lung. J Appl Physiol 72:865-873.
12. Phares TW, Fabis MJ, Brimer CM, Kean RB, Hooper DC (2007) A peroxynitrite-dependent pathway is responsible for blood-brain barrier permeability changes during a central nervous system inflammatory response: TNF-α is neither necessary nor sufficient. J Immunol 178:7334-7343.
13. Cross AW, Manning PT, Stern MK, Misko TP (1997) Evidence for the production of peroxynitrite in inflammatory CNS demyelination. J Neuroimmunol 80:121-130.
14. Hooper DC, et al. (1997) Prevention of experimental allergic encephalomyelitis by targeting nitric oxide and peroxynitrite: Implications for the treatment of multiple sclerosis. Proc Natl Acad Sci USA 94:2528-2533.
15. Miljkovic D, Trajkovic V (2004) Inducible nitric oxide synthase activation by interleukin-17. Cytokine Growth Factor Rev 15:21-32.
16. Langrish CL, et al. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation J Exp Med 201:233-240.
17. Squadrito GL, et al. (2000) Reaction of uric acid with peroxynitrite and implications for the mechanism of neuroprotection by uric acid. Arch Biochem Biophys 376:333-337.
18. Hooper DC, et al. (1998) Uric acid, a natural scavenger of peroxynitrite, in experimental allergic encephalomyelitis and multiple sclerosis. Proc Natl Acad Sci USA 95:675-680.
19. Rajagopalan S et al. (1996) Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for artherosclerotic plaque stability. J Clin Invest 98:2572-2579.
20. Trackey JL, Uliasz TF, Hewitt SJ (2001) SIN-1-induced cytotoxicity in mixed cortical cell culture: Peroxynitrite-dependent and -independent induction of excitotoxic cell death. J Neurochem 79:445-455.
21. Scott GS, Virág L, Szabó C, Hooper DC (2003) Peroxynitrite-induced oligodendrocytes-toxicity is not dependent on poly(ADP-ribose) polymerase activity. Glia 41:105-116.
22. Scott GS, Hooper DC (2001) The role of uric acid in protection against peroxynitrite-mediated pathology. Med Hypotheses 56:95-100.
23. Spitsin SV, Scott GS, Kean RB, Mikheeva T, Hooper DC (2000) Protection of myelin basic protein immunized mice from free-radical mediated inflammatory cell invasion of the central nervous system by the natural peroxynitrite scavenger uric acid. Neurosci Lett 292:137-141.
24. Varela-Eschavarria A, Montes de Oca-Luna R, Barrera-Saldana HA (1988) Uricase protein sequences: Conserved during hominid evolution but absent in humans. FASEB J 2:3092-3096.
25. Saria A, Lundberg JM (1983) Evans blue fluorescence: Quantitative and morphological evaluation of vascular permeability in animal tissues. J Neurosci Methods 8:41-49.
26. Hsu HC, et al. (2008) Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat Immunol 9:166-175.
27. Shih SC, Smith LE (2005) Quantitative multi-gene transcriptional profiling using real-time PCR with a master template. Exp Mol Pathol 79:14-22.
28. Scott GS, et al. (2004) ICAM-1 upregulation in the spinal cords of PLSJL mice with experimental allergic encephalomyelitis is dependent upon TNF-α production triggered by the loss of blood-brain barrier integrity. J Neuroimmunol 155:32-42.