Lymphocyte migration through the blood-brain barrier (BBB) in feline immunodeficiency virus infection is significantly influenced by the pre-existence of virus and tumour necrosis factor (TNF)-α within the central nervous system (CNS): Studies using an in vitro feline BBB model

Neuropathology and Applied Neurobiology

Volumn 35, Issue 6, 2009, Pages 592-602

  Fletcher, N F ^a   Bexiga, M G ^a,c   Brayden, D J ^a   Brankin, B ^a   Willett, B J ^b   Hosie, M J ^b   Jacque, J M ^a   Callanan, J J ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Blood brain barrier; Feline immunodeficiency virus; Lymphocyte

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CD4+ T LYMPHOCYTE; CELL MIGRATION; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE MODEL; EXPERIMENTAL CAT; FELINE IMMUNODEFICIENCY VIRUS; LENTIVIRINAE; LYMPHOCYTE MIGRATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; VIRUS ENTRY; VIRUS INFECTION;

ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN; CATS; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; CELL MOVEMENT; CELLS, CULTURED; ENDOTHELIAL CELLS; FELINE ACQUIRED IMMUNODEFICIENCY SYNDROME; IMMUNODEFICIENCY VIRUS, FELINE; INTERCELLULAR ADHESION MOLECULE-1; LYMPHOCYTE ACTIVATION; TIGHT JUNCTIONS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; VASCULAR CELL ADHESION MOLECULE-1;

EID: 70449701529     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2009.01031.x     Document Type: Article

References (57)

1. Budka H. Neuropathology of human immunodeficiency virus infection. Brain Pathol 1991 1 : 163 175
2. Kanzer MD. Neuropathology of AIDS. Crit Rev Neurobiol 1990 5 : 313 362
3. Davis LE, Hjelle BL, Miller VE, Palmer DL, Llewellyn AL, Merlin TL, Young SA, Mills RG, Wachsman W, Wiley CA. Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 1992 42 : 1736 1739
4. Gray F, Scaravilli F, Everall I, Chretien F, An S, Boche D, Adle-Biassette H, Wingertsmann L, Durigon M, Hurtrel B, Chiodi F, Bell J, Lantos P. Neuropathology of early HIV-1 infection. Brain Pathol 1996 6 : 1 15
5. Gonzalez-Scarano F, Martin-Garcia J. The neuropathogenesis of AIDS. Nat Rev 2005 5 : 69 81
6. Podell M, March PA, Buck WR, Mathes LE. The feline model of neuroAIDS: understanding the progression towards AIDS dementia. J Psychopharmacol 2000 14 : 205 213
7. Bendinelli M, Pistello M, Lombardi S, Poli A, Garzelli C, Matteucci D, Ceccherini-Nelli L, Malvaldi G, Tozzini F. Feline immunodeficiency virus: an interesting model for AIDS studies and an important cat pathogen. Clin Microbiol Rev 1995 8 : 87 112
8. Dow SW, Dreitz MJ, Hoover EA. Feline immunodeficiency virus neurotropism: evidence that astrocytes and microglia are the primary target cells. Vet Immunol Immunopathol 1992 35 : 23 35
9. Dow SW, Poss ML, Hoover EA. Feline immunodeficiency virus: a neurotropic lentivirus. J Acquir Immune Defic Syndr 1990 3 : 658 668
10. Hurtrel M, Ganiere JP, Guelfi JF, Chakrabarti L, Maire MA, Gray F, Montagnier L, Hurtrel B. Comparison of early and late feline immunodeficiency virus encephalopathies. AIDS 1992 6 : 399 406
11. Podell M, Maruyama K, Smith M, Hayes KA, Buck WR, Ruehlmann DS, Mathes LE. Frontal lobe neuronal injury correlates to altered function in FIV-infected cats. J Acquir Immune Defic Syndr 1999 22 : 10 8
12. Ryan G, Klein D, Knapp E, Hosie MJ, Grimes T, Mabruk MJ, Jarrett O, Callanan JJ. Dynamics of viral and proviral loads of feline immunodeficiency virus within the feline central nervous system during the acute phase following intravenous infection. J Virol 2003 77 : 7477 7485
13. Ryan G, Grimes T, Brankin B, Mabruk MJ, Hosie MJ, Jarrett O, Callanan JJ. Neuropathology associated with feline immunodeficiency virus infection highlights prominent lymphocyte trafficking through both the blood-brain and blood-choroid plexus barriers. J Neurovirol 2005 11 : 337 345
14. Ghafouri M, Amini S, Khalili K, Sawaya BE. HIV-1 associated dementia: symptoms and causes. Retrovirology 2006 3 : 28
15. Anthony IC, Crawford DH, Bell JE. B lymphocytes in the normal brain: contrasts with HIV-associated lymphoid infiltrates and lymphomas. Brain 2003 126 : 1058 1067
16. Lackner AA, Dandekar S, Gardner MB. Neurobiology of simian and feline immunodeficiency virus infections. Brain Pathol 1991 1 : 201 212
17. Petito CK, Adkins B, McCarthy M, Roberts B, Khamis I. CD4+ and CD8+ cells accumulate in the brains of acquired immunodeficiency syndrome patients with human immunodeficiency virus encephalitis. J Neurovirol 2003 9 : 36 44
18. Wekerle H, Schwab M, Linington C, Meyermann R. Antigen presentation in the peripheral nervous system: Schwann cells present endogenous myelin autoantigens to lymphocytes. Eur J Immunol 1986 16 : 1551 1557
19. Dunfee R, Thomas ER, Gorry PR, Wang J, Ancuta P, Gabuzda D. Mechanisms of HIV-1 neurotropism. Curr HIV Res 2006 4 : 267 278
20. Albright AV, Soldan SS, Gonzalez-Scarano F. Pathogenesis of human immunodeficiency virus-induced neurological disease. J Neurovirol 2003 9 : 222 227
21. Katsetos CD, Fincke JE, Legido A, Lischner HW, de Chadarevian JP, Kaye EM, Platsoucas CD, Oleszak EL. Angiocentric CD3(+) T cell infiltrates in human immunodeficiency virus type 1-associated central nervous system disease in children. Clin Diagn Lab Immunol 1999 6 : 105 114
22. Kipar A, Leutenegger CM, Hetzel U, Akens MK, Mislin CN, Reinacher M, Lutz H. Cytokine mRNA levels in isolated feline monocytes. Vet Immunol Immunopathol 2001 78 : 305 315
23. Fiala M, Looney DJ, Stins M, Way DD, Zhang L, Gan X, Chiappelli F, Schweitzer ES, Shapshak P, Weinand M, Graves MC, Witte M, Kim KS. TNF-alpha opens a paracellular route for HIV-1 invasion across the blood-brain barrier. Mol Med 1997 3 : 553 564
24. Croitoru-Lamoury J, Guillemin GJ, Boussin FD, Mognetti B, Gigout LI, Cheret A, Vaslin B, Le Grand R, Brew BJ, Dormont D. Expression of chemokines and their receptors in human and simian astrocytes: evidence for a central role of TNF alpha and IFN gamma in CXCR4 and CCR5 modulation. Glia 2003 41 : 354 370
25. Rostasy K, Gorgun G, Kleyner Y, Garcia A, Kramer M, Melanson SM, Mathys JM, Yiannoutsos C, Skolnik PR, Navia BA. Tumor necrosis factor alpha leads to increased cell surface expression of CXCR4 in SK-N-MC cells. J Neurovirol 2005 11 : 247 255
26. Seilhean D, Kobayashi K, He Y, Uchihara T, Rosenblum O, Katlama C, Bricaire F, Duyckaerts C, Hauw JJ. Tumor necrosis factor-alpha, microglia and astrocytes in AIDS dementia complex. Acta Neuropathol 1997 93 : 508 517
27. Brabers NA, Nottet HS. Role of the pro-inflammatory cytokines TNF-alpha and IL-1beta in HIV-associated dementia. Eur J Clin Invest 2006 36 : 447 458
28. Lawrence CE, Callanan JJ, Willett BJ, Jarrett O. Cytokine production by cats infected with feline immunodeficiency virus: a longitudinal study. Immunology 1995 85 : 568 574
29. Poli A, Pistello M, Carli MA, Abramo F, Mancuso G, Nicoletti E, Bendinelli M. Tumor necrosis factor-alpha and virus expression in the central nervous system of cats infected with feline immunodeficiency virus. J Neurovirol 1999 5 : 465 473
30. Fletcher NF, Brayden DJ, Brankin B, Worrall S, Callanan JJ. Growth and characterisation of a cell culture model of the feline blood-brain barrier. Vet Immunol Immunopathol 2006 109 : 233 244
31. Miyazawa T, Furuya T, Itagaki S, Tohya Y, Takahashi E, Mikami T. Establishment of a feline T-lymphoblastoid cell line highly sensitive for replication of feline immunodeficiency virus. Arch Virol 1989 108 : 131 135
32. Miyazawa T, Kawaguchi Y, Kohmoto M, Sakuragi J, Adachi A, Fukasawa M, Mikami T. Production of feline immunodeficiency virus in feline and non-feline non-lymphoid cell lines by transfection of an infectious molecular clone. J Gen Virol 1992 73 : 1543 1546
33. Strom SC, Michalopoulos G. Collagen as a substrate for cell growth and differentiation. Methods Enzymol 1982 82 : 544 555
34. Artursson P. Epithelial transport of drugs in cell culture. I: a model for studying the passive diffusion of drugs over intestinal absorptive (Caco-2) cells. J Pharm Sci 1990 79 : 476 482 (Pubitemid 20221389)
35. de Parseval A, Chatterji U, Sun P, Elder JH. Feline immunodeficiency virus targets activated CD4+ T cells by using CD134 as a binding receptor. Proc Natl Acad Sci U S A 2004 101 : 13044 13049
36. Hickey WF, Hsu BL, Kimura H. T-lymphocyte entry into the central nervous system. J Neurosci Res 1991 28 : 254 260
37. Kleine TO, Benes L. Immune surveillance of the human central nervous system (CNS): different migration pathways of immune cells through the blood-brain barrier and blood-cerebrospinal fluid barrier in healthy persons. Cytometry A 2006 69 : 147 151
38. Hudson LC, Bragg DC, Tompkins MB, Meeker RB. Astrocytes and microglia differentially regulate trafficking of lymphocyte subsets across brain endothelial cells. Brain Res 2005 1058 : 148 160
39. Kramer-Hammerle S, Rothenaigner I, Wolff H, Bell JE, Brack-Werner R. Cells of the central nervous system as targets and reservoirs of the human immunodeficiency virus. Virus Res 2005 111 : 194 213
40. Banks WA, Ercal N, Price TO. The blood-brain barrier in neuroAIDS. Curr HIV Res 2006 4 : 259 266
41. Nakaoke R, Ryerse JS, Niwa M, Banks WA. Human immunodeficiency virus type 1 transport across the in vitro mouse brain endothelial cell monolayer. Exp Neurol 2005 193 : 101 109
42. Shimojima M, Nishimura Y, Miyazawa T, Tohya Y, Akashi H. Phenotypic changes in CD8+ peripheral blood lymphocytes in cats infected with feline immunodeficiency virus. Microbes Infect 2003 5 : 1171 1176
43. Hosie MJ, Willett BJ, Klein D, Dunsford TH, Cannon C, Shimojima M, Neil JC, Jarrett O. Evolution of replication efficiency following infection with a molecularly cloned feline immunodeficiency virus of low virulence. J Virol 2002 76 : 6062 6072
44. Park HS, Kyaw-Tanner M, Thomas J, Robinson WF. Feline immunodeficiency virus replicates in salivary gland ductular epithelium during the initial phase of infection. Vet Microbiol 1995 46 : 257 267
45. Persidsky Y, Stins M, Way D, Witte MH, Weinand M, Kim KS, Bock P, Gendelman HE, Fiala M. A model for monocyte migration through the blood-brain barrier during HIV-1 encephalitis. J Immunol 1997 158 : 3499 3510
46. Fischer-Smith T, Rappaport J. Evolving paradigms in the pathogenesis of HIV-1-associated dementia. Expert Rev Mol Med 2005 7 : 1 26
47. Lawrence CE, Callanan JJ, Jarrett O. Decreased mitogen responsiveness and elevated tumor necrosis factor production in cats shortly after feline immunodeficiency virus infection. Vet Immunol Immunopathol 1992 35 : 51 9
48. Perrella O, Carrieri PB, Guarnaccia D, Soscia M. Cerebrospinal fluid cytokines in AIDS dementia complex. J Neurol 1992 239 : 387 388
49. Tan SV, Guiloff RJ, Henderson DC, Gazzard BG, Miller R. AIDS-associated vacuolar myelopathy and tumor necrosis factor-alpha (TNF alpha). J Neurol Sci 1996 138 : 134 144
50. Brett J, Gerlach H, Nawroth P, Steinberg S, Godman G, Stern D. Tumor necrosis factor/cachectin increases permeability of endothelial cell monolayers by a mechanism involving regulatory G proteins. J Exp Med 1989 169 : 1977 1991
51. Pober JS, Gimbrone MA Jr., Lapierre LA, Mendrick DL, Fiers W, Rothlein R, Springer TA. Overlapping patterns of activation of human endothelial cells by interleukin 1, tumor necrosis factor, and immune interferon. J Immunol 1986 137 : 1893 1896
52. Madonna R, Massaro M, De Caterina R. Insulin potentiates cytokine-induced VCAM-1 expression in human endothelial cells. Biochim Biophys Acta 2008
53. Cybulsky MI, Iiyama K, Li H, Zhu S, Chen M, Iiyama M, Davis V, Gutierrez-Ramos JC, Connelly PW, Milstone DS. A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest 2001 107 : 1255 1262
54. Warfel JM, D'Agnillo F. Anthrax lethal toxin enhances TNF-induced endothelial VCAM-1 expression via an IFN regulatory factor-1-dependent mechanism. J Immunol 2008 180 : 7516 7524
55. Biber K, de Jong EK, van Weering HR, Boddeke HW. Chemokines and their receptors in central nervous system disease. Curr Drug Targets 2006 7 : 29 46
56. Constantin G. Chemokine signaling and integrin activation in lymphocyte migration into the inflamed brain. J Neuroimmunol 2008 198 : 20 6
57. Frey SC, Hoover EA, Mullins JI. Feline immunodeficiency virus cell entry. J Virol 2001 75 : 5433 5440