Impairment of blood-cerebrospinal fluid barrier properties by retrovirus-activated T lymphocytes: Reduction in cerebrospinal fluid-to-blood efflux of prostaglandin E2

Journal of Neurochemistry

Volumn 94, Issue 6, 2005, Pages 1580-1593

  Khuth, Seng Thuon ^a   Strazielle, Nathalie ^a   Giraudon, Pascale ^a   Belin, Marie Françoise ^a   Ghersi Egea, Jean François ^a  

^a UNIVERSITÉ LYON 1   (France)

Author keywords

Blood brain barrier; Choroid plexus; Cytokine; Neuroinflammation; Prostaglandin

Indexed keywords

CYTOKINE; FREE RADICAL; INTERLEUKIN 1; MATRIX METALLOPROTEINASE; PROSTAGLANDIN E2; TAX PROTEIN; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANION TRANSPORT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN INFECTION; CELL MEMBRANE PERMEABILITY; CHOROID PLEXUS; ENCEPHALITIS; HUMAN; HUMAN CELL; ILLNESS BEHAVIOR; INFLAMMATORY DISEASE; NONHUMAN; PRIORITY JOURNAL; RAT; RETROVIRUS; RETROVIRUS INFECTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TIGHT JUNCTION;

ANIMALS; ANIMALS, NEWBORN; BLOOD-BRAIN BARRIER; CELL COMMUNICATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM VIRAL DISEASES; CEREBROSPINAL FLUID; CHOROID PLEXUS; COCULTURE TECHNIQUES; DINOPROSTONE; ENCEPHALITIS; EPITHELIAL CELLS; FREE RADICALS; GENE PRODUCTS, TAX; INFLAMMATION MEDIATORS; LYMPHOCYTE ACTIVATION; MATRIX METALLOPROTEINASES; RATS; RETROVIRIDAE; RETROVIRIDAE INFECTIONS; T-LYMPHOCYTES; VIRUS SHEDDING;

EID: 24944477301     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03309.x     Document Type: Article

References (58)

1. Alebouyeh M., Takeda M., Onozato M. L. et al. (2003) Expression of human organic anion transporters in the choroid plexus and their interactions with neurotransmitter metabolites. J. Pharmacol. Sci. 93, 430-436.
2. Azzi A., Montecucco C. and Richter C. (1975) The use of acerylated ferricytochrome c for the detection of superoxide radicals produced in biological membranes. Biochem. Biophys. Res. Commun 65, 597-603.
3. Biddison W. E., Kubota R., Kawanishi T., Taub D. D., Cruikshank W. W., Center D. M., Connor E. W., Utz U. and Jacobson S. (1997) Human T cell leukemia virus type 1 (HTLV-1)-specific CD8+CTL clones from patients with HTLV-I-associated neurologic disease secrete proinflammatory cytokines, chemokines, and matrix metalloproteinase. J. Immunol. 159, 2018-2025.
4. Boje K. M., Jaworowicz D. Jr and Raybon J. J. (2003) Neuroinflammatory role of prostaglandins during experimental meningitis: evidence suggestive of an in vivo relationship between nitric oxide and prostaglandins. J. Pharmacol. Exp. Ther. 304, 319-325.
5. Bragg D. C., Childers T. A., Tompkins M. B., Tompkins W. A. and Meeker R. B. (2002) Infection of the choroid plexus by feline immunodeficiency virus. J. Neurovirol. 8, 211-224.
6. Cattori V., van Montfoort J. E., Stieger B., Landmann L., Meijer D. K., Winterhalter K. H., Meier P. J. and Hagenbuch B. (2001) Localization of organic anion transporting polypeptide 4 (Oatp4) in rat liver and comparison of its substrate specificity with Oatp1, Oatp2 and Oatp3. Pflugers Arch. 443, 188-195.
7. Daval J. L., Ghersi-Egea J. F., Oillet J. and Koziel V. (1995) A simple method for evaluation of superoxide radical production in neural cells under various culture conditions: application to hypoxia. J. Cereb. Blood Flow Metab. 15, 71-77.
8. Davson H. and Segal M. B. (1996) Physiology of the CSF and the Blood-Brain Barriers, pp. 822. CRC Press, Boca Raton, New York, London, Tokyo.
9. DiBenedetto F. E. and Bito L. Z. (1986) Transport of prostaglandins and other eicosanoids by the choroid plexus: its characterization and physiological significance. J. Neurochem. 46, 1725-1731.
10. Diem R., Hobom M., Grotsch P., Kramer B. and Bahr M. (2003) Interleukin-1β protects neurons via the interleukin-1 (IL-1) receptor-mediated Akt pathway and by IL-1 receptor-independent decrease of transmembrane currents in vivo. Mol. Cell Neurosci. 22, 487-500.
11. Engblom D., Saha S., Engstrom L., Westman M., Audoly L. P., Jakobsson P. J. and Blomqvist A. (2003) Microsomal prostaglandin E synthase-1 is the central switch during immune-induced pyresis. Nat. Neurosci. 6, 1137-1138.
12. Falangola M. F., Hanly A., Galvao-Castro B. and Petito C. K. (1995) HIV infection of human choroid plexus: a possible mechanism of viral entry into the CNS. J. Neuropathol. Exp. Neurol. 54, 497-503.
13. Gessain A., Barin F., Vernant J. C., Gout O., Maurs L., Calender A. and de The G. (1985) Antibodies to human T-lymphotropic virus type-1 in patients with tropical spastic paraparesis. Lancet 2, 407-410.
14. Giraudon P., Szymocha R., Buart S., Bernard A., Cartier L., Belin M. F. and Akaoka H. (2000) T lymphocytes activated by persistent viral infection differentially modify the expression of metalloproteinases and their endogenous inhibitors. TIMPs, in human astrocytes: relevance to HTLV-I-induced neurological disease. J. Immunol. 164, 2718-2727.
15. Grant C., Barmak K., Alefantis T., Yao J., Jacobson S. and Wigdahl B. (2002) Human T cell leukemia virus type I and neurologic disease: events in bone marrow, peripheral blood, and central nervous system during normal immune surveillance and neuroinflammation. J. Cell Physiol. 190, 133-159.
16. Griffin D. E., Wesselingh S. L. and McArthur J. C. (1994) Elevated central nervous system prostaglandins in human immunodeficiency virus-associated dementia. Ann. Neurol. 35, 592-597.
17. 2 response in the central nervous system associated with the induction of microsomal prostaglandin E2 synthase-1. J. Biol. Chem. 24, 24.
18. Hakvoort A., Haselbach M. and Galla H. J. (1998) Active transport properties of porcine choroid plexus cells in culture. Brain Res. 795, 247-256.
19. Hartmann G., Cheung A. K. and Piquette-Miller M. (2002) Inflammatory cytokines, but not bile acids, regulate expression of murine hepatic an ion transporters in endotoxemia. J. Pharmacol. Exp. Ther. 303, 273-281.
20. Hollsberg P. (1999) Mechanisms of T-cell activation by human T-cell lymphotropic virus type I. Microbiol. Mol. Biol. Rev. 63, 308-333.
21. Ivanov A. I., Scheck A. C. and Romanovsky A. A. (2003) Expression of genes controlling transport and catabolism of prostaglandin E2 in lipopolysaccharide fever. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284, R698-R706.
22. Kanai N., Lu R., Satriano J. A., Bao Y., Wolkoff A. W. and Schuster V. L. (1995) Identification and characterization of a prostaglandin transporter. Science 268, 866-869.
23. Kimura H., Takeda M., Narikawa S., Enomoto A., Ichida K., and Endou H. (2002) Human organic anion transporters and human organic cation transporters mediate renal transport of prostaglandins. J. Pharmacol. Exp. Ther. 301, 293-298.
24. Konsman J. P., Parnet P. and Dantzer R. (2002) Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci. 25, 154-159.
25. Krunic N., Adamson S. L. and Coceani F. (2000) Differential uptake and catabolism of prostaglandin (PG)E(2) versus PGF (2α) in the sheep choroid plexus during development. Brain Res. Dev. Brain Res. 119, 11-19.
26. Lacroix S., Vallieres L. and Rivest S. (1996) C-fos mRNA pattern and corticotropin-releasing factor neuronal activity throughout the brain of rats injected centrally with a prostaglandin of E2 type. J. Neuroimmunol. 70, 163-179.
27. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 221, 680-685.
28. Lane J. H., Tarantal A. F., Pauley D., Marthas M., Miller C. J. and Lackner A. A. (1996) Localization of simian immunodeficiency virus nucleic acid and antigen in brains of fetal macaques inoculated in utero. Am. J. Pathol. 149, 1097-1104.
29. Leggas M., Adachi M., Scheffer G. L. et al. (2004) Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol. Cell Biol. 24, 7612-7621.
30. Levine S. (1987) Choroid plexus: target for systemic disease and pathway to the brain. Lab. Invest 56, 231-233.
31. Lindhohn P. F., Reid R. L. and Brady J. N. (1992) Extracellular Taxi protein stimulates tumor necrosis factor-β and immunoglobulin κ light chain expression in lymphoid cells. J. Virol. 66, 1294-1302.
32. Lioehev S. I. and Fridovich I. (1999) Superoxide and iron: partners in crime. IUBMB Life 48, 157-161.
33. Lippoldt A., Liebner S., Andbjer B., Kalbachcr H., Wolbung H., Haller H. and Fuxe K. (2000) Organization of choroid plexus epithelial and endothelial cell tight junctions and regulation of claudin-1, -2 and -5 expression by protein kinase C. Neuroreport 11, 1427-1431.
34. Mun-Bryce S. and Rosenberg G. A. (1998) Gelatinase B modulates selective opening of the blood-brain barrier during inflammation. Am. J. Physiol. 274, R1203-R1211.
35. Mustafa M. M., Ramilo O., Saez-Llorens X., Olsen K., D., Magness R. R. and McCracken G. H. Jr (1990) Cerebrospinal fluid prostaglandins, interleukin 1β, and tumor necrosis factor in bacterial meningitis. Clinical and laboratory correlations in placebo-treated and dexamethasone-treated patients. Am. J. Dis. Child. 144, 883-887.
36. Nakamura J., Nishida T., Hayashi K., Kawada N., Ueshima S., Sugiyama Y., Ito T., Sobue K. and Matsuda H. (1999) Kupffer cell-mediated down regulation of rat hepatic CMOAT/MRP2 gene expression. Biochem. Biophys. Res. Commun. 255, 143-149.
37. Nicholson C. (1999) Signals that go with the (low. Trends Neurosci. 22, 143-145.
38. Nitta T., Hata M., Gotoh S., Seo Y., Sasaki H., Hashimoto N., Furuse M. and Tsukita S. (2003) Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 161, 653-660.
39. Osame M., Usuku K., Izumo S., Ijichi N., Amitani H., Igata A., Matsumoto M. and Tara M. (1986) HTLV-1 associated myelopathy, a new clinical entity. Lancet 1, 1031-1032.
40. Peters A., Palay S. L. and Webster H. D. (1991) The Fine Structure of the Nervous System. Neurons and Their Supporting Cells. 3rd edn. pp. 494. Oxford University Press. New York.
41. Petito C. K. (2004) Human immunodeficiency vims type 1 compartmentalization in the central nervous system. J. Neurovirol. 10, 21-24.
42. Popovic M., Lange-Wantzin G., Sarin P. S., Mann D. and Gallo R. C. (1983) Transformation of human umbilical cord blood T cells by human T-cell leukemia/lymphoma vims. Proc. Natl Acad. Sci. USA 80, 5402-5406.
43. Reid G., Wielinga P., Zelcer N., van der Heijden I., Kuil A., de Haas M., Wijnholds J. and Borst P. (2003) The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by non-steroidal antiinflammatory drugs. Proc. Natl Acad. Sci. USA 100, 9244-9249. Epub. June 2003 9230.
44. Rosenberg G. A., Kornfeld M., Estrada E., Kelley R. O., Liotta L. A. and Stetler-Stevenson W. G. (1992) TIMP-2 reduces proteolytic opening of blood-brain barrier by type IV collagenase. Brain Res. 576, 203-207.
45. Rosenberg G. A., Estrada E. Y., Deneoff J. E. and Stetler-Stevenson W. G. (1995) Tumor necrosis factor-α-induced gelatinase B causes delayed opening of the blood-brain barrier, an expanded therapeutic window. brain Res. 703, 151-155.
46. Schuster V. L. (2002) Prostaglandin transport. Prostaglandins Other Lipid Med. 68-69, 633-647.
47. Sekine T., Watanabe N., Hosoyamada M., Kanai Y. and Endou H. (1997) Expression cloning and characterization of a novel multispecific organic anion transporter. J. Biol. Chem. 272, 18 526-18 529.
48. Spector R. and Goetzl E. J. (1985) Leukotriene C4 transport by the choroid plexus in vitro. Science 228, 325-327.
49. Strazielle N. and Ghersi-Egea J. F. (1999) Demonstration of a coupled metabolism-efflux process at the choroid plexus as a mechanism of brain protection toward xenobiotics. J. Neurosci. 19, 6275-6289.
50. Strazielle N. and Ghersi-Egea J. F. (2000) Choroid plexus in the central nervous system: biology and physiopathology. J. Neuropathol. Exp. Neurol. 59, 561-574.
51. Strazielle N. and Preston J. E. (2003) Transport across the choroid plexuses in vivo and in vitro. Meth. Mol. Med. 89, 291-304.
52. Strazielle N., Belin M. F. and Ghersi-Egea J. F. (2003a) Choroid plexus controls brain availability of anti-HIV nucleoside analogs via pharmacologically inhibitable organic anion transporters. Aids 17, 1473-1485.
53. Strazielle N., Khuth S. T., Murat A., Chalon A., Giraudon P., Belin M. F. and Ghersi-Egea J. F. (2003b) Pro-inflammatory cytokines modulate matrix metalloproteinase secretion and organic anion transport at the blood-cerebrospinal fluid barrier. J. Neuropathol. Exp. Neurol. 62, 1254-1264.
54. Strazielle N., Khuth S. T. and Ghersi-Egea J. F. (2004) Detoxification systems, passive and specific transport for drugs at the blood-CSF barrier in normal and pathological situation. Adv. Drug Deliv. Rev. 56, 1717-1740.
55. Szymocha R., Akaoka H., Dutuit M., Malcus C., Didier-Bazes M., Belin M. F. and Giraudon P. (2000) Human T-cell lymphotropic virus type I-infected T lymphocytes impair catabolism and uptake of glutamate by astrocytes via Tax-1 and tumor necrosis factor α J. Virol. 74, 6433-6441.
56. Touzani O., Boutin H., LeFeuvre R., Parker L., Miller A., Luheshi G. and Rothwell N. (2002) Interleukin-1 influences ischemic brain damage in the mouse independently of the interleukin-1 type 1 receptor. J. Neurosci. 22, 38-43.
57. Van den Steen P. E., Proost P., Wuyts A., Van Damme J. and Opdenakker G. (2000) Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-α and leaves RANTES and MCP-2 intact. Blood 96, 2673-2681.
58. Wucherpfennig K. W., Hollsberg P., Richardson J. H., Benjamin D. and Hafler D. A. (1992) T-cell activation by autologous human T-cell leukemia virus type I-infected T-cell clones. Proc. Natl Acad. Sci. USA 89, 2110-2114.