Journal of Neuroimmune Pharmacology

, Volume 2, Issue 2, pp 154–170 | Cite as

Feline Immunodeficiency Virus Neuropathogenesis: From Cats to Calcium

Invited Review
First Online:
Received:
Accepted:

Abstract

Invasion of human immunodeficiency virus (HIV) into the central and peripheral nervous system produces a wide range of neurological symptoms, which continue to persist even with adequate therapeutic suppression of the systemic viremia. The development of therapies designed to prevent the neurological complications of HIV require a detailed understanding of the mechanisms of virus penetration into the nervous system, infection, and subsequent neuropathogenesis. These processes, however, are difficult to study in humans. The identification of animal lentiviruses similar to HIV has provided useful models of HIV infection that have greatly facilitated these efforts. This review summarizes contributions made from in vitro and in vivo studies on the infectious and pathological interactions of feline immunodeficiency virus (FIV) with the nervous system. In vivo studies on FIV have provided insights into the natural progression of CNS disease as well as the contribution of various risk factors. In vitro studies have contributed to our understanding of immune cell trafficking, CNS infection and neuropathogenesis. Together, these studies have made unique contributions to our understanding of (1) lentiviral interactions at the blood–cerebrospinal fluid (CSF) barrier within the choroid plexus, (2) early FIV invasion and pathogenesis in the brain, and (3) lentiviral effects on intracellular calcium deregulation and neuronal dysfunction. The ability to combine in vitro and in vivo studies on FIV offers enormous potential to explore neuropathogenic mechanisms and generate information necessary for the development of effective therapeutic interventions.

Keywords

AIDS dementia human immunodeficiency virus neurons microglia astrocytes 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgment

This study was supported by NIMH Grant R01 MH063646.

References

  1. Abramo F, Bo S, Canese MG, Poli A (1995) Regional distribution of lesions in the central nervous system of cats infected with feline immunodeficiency virus. AIDS Res Hum Retrovir 11:1247–1253PubMedGoogle Scholar
  2. Ackley CD, Yamamoto JK, Levy N, Pedersen NC, Cooper MD (1990) Immunologic abnormalities in pathogen-free cats experimentally infected with feline immunodeficiency virus. J Virol 64:5652–5655PubMedGoogle Scholar
  3. Allison RW, Hoover EA (2003a) Covert vertical transmission of feline immunodeficiency virus. AIDS Res Hum Retrovir 19:421–434PubMedGoogle Scholar
  4. Allison RW, Hoover EA (2003b) Feline immunodeficiency virus is concentrated in milk early in lactation. AIDS Res Hum Retrovir 19:245–253PubMedGoogle Scholar
  5. Anthony IC, Ramage SN, Carnie FW, Simmonds P, Bell JE (2005) Influence of HAART on HIV-related CNS disease and neuroinflammation. J Neuropathol Exp Neurol 64:529–536PubMedGoogle Scholar
  6. Arai M, Earl DD, Yamamoto JK (2002) Is AZT/3TC therapy effective against FIV infection or immunopathogenesis? Vet Immunol Immunopathol 85:189–204PubMedGoogle Scholar
  7. Barr MC, Billaud JN, Selway DR, Huitron-Resendiz S, Osborn KG, Henriksen SJ, Phillips TR (2000) Effects of multiple acute morphine exposures on feline immunodeficiency virus disease progression. J Infect Dis 182:725–732PubMedGoogle Scholar
  8. Barr MC, Huitron-Resendiz S, Sanchez-Alavez M, Henriksen SJ, Phillips TR (2003) Escalating morphine exposures followed by withdrawal in feline immunodeficiency virus-infected cats: a model for HIV infection in chronic opiate abusers. Drug Alcohol Depend 72:141–149PubMedGoogle Scholar
  9. Beebe AM, Dua N, Faith TG, Moore PF, Pedersen NC, Dandekar S (1994) Primary stage of feline immunodeficiency virus infection: viral dissemination and cellular targets. J Virol 68:3080–3091PubMedGoogle Scholar
  10. Billaud JN, Selway D, Yu N, Phillips TR (2000) Replication rate of feline immunodeficiency virus in astrocytes is envelope dependent: implications for glutamate uptake. Virology 266:180–188PubMedGoogle Scholar
  11. Bisset LR, Lutz H, Boni J, Hofmann-Lehmann R, Luthy R, Schupbach J (2002) Combined effect of zidovudine (ZDV), lamivudine (3TC) and abacavir (ABC) antiretroviral therapy in suppressing in vitro FIV replication. Antiviral Res 53:35–45PubMedGoogle Scholar
  12. Boche D, Hurtrel M, Gray F, Claessens-Maire MA, Ganiere JP, Montagnier, Hurtrel B (1996) Virus load and neuropathology in the FIV model. J Neurovirology 2:377–387Google Scholar
  13. Bragg D, Childers T, Tompkins M, Tompkins W, Meeker R (2002a) Infection of the choroid plexus by feline immunodeficiency virus. J Neurovirology 8:211–224Google Scholar
  14. Bragg D, Hudson L, Liang Y, Tompkins M, Fernandes A, Meeker R (2002b) Choroid plexus macrophages proliferate and release toxic factors in response to feline immunodeficiency virus. J Neurovirology 8:225–239Google Scholar
  15. Bragg DC, Boles JC, Meeker RB (2002c) Destabilization of neuronal calcium homeostasis by factors secreted from choroid plexus macrophage cultures in response to feline immunodeficiency virus. Neurobiol Dis 9:173–186PubMedGoogle Scholar
  16. Bragg DC, Meeker RB, Duff BA, English RV, Tompkins MB (1999) Neurotoxicity of FIV and FIV envelope protein in feline cortical cultures. Brain Res 816:431–437PubMedGoogle Scholar
  17. Brinkmann R, Schwinn A, Muller J, Stahl-Hennig C, Coulibaly C, Hunsmann G, Czub S, Rethwilm A, Dorries R, Ter MV (1993) In vitro and in vivo infection of rhesus monkey microglial cells by simian immunodeficiency virus. Virology 195:561–568PubMedGoogle Scholar
  18. Brown WC, Bissey L, Logan KS, Pedersen NC, Elder JH, Collisson EW (1991) Feline immunodeficiency virus infects both CD4+ and CD8+ T lymphocytes. J Virol 65:3359–3364PubMedGoogle Scholar
  19. Brunner D, Pedersen NC (1989) Infection of peritoneal macrophages in vitro and in vivo with feline immunodeficiency virus. J Virol 63:5483–5488PubMedGoogle Scholar
  20. Bucci JG, English RV, Jordan HL, Childers TA, Tompkins MB, Tompkins WA (1998) Mucosally transmitted feline immunodeficiency virus induces a CD8+ antiviral response that correlates with reduction of cell-associated virus. J Infect Dis 177:18–25PubMedGoogle Scholar
  21. Burkhard MJ, Dean GA (2003) Transmission and immunopathogenesis of FIV in cats as a model for HIV. Curr HIV Res 1:15–29PubMedGoogle Scholar
  22. Burkhard MJ, Mathiason CK, O’Halloran K, Hoover EA (2002) Kinetics of early FIV infection in cats exposed via the vaginal versus intravenous route. AIDS Res Hum Retrovir 18:217–226PubMedGoogle Scholar
  23. Carpenter MA, O’Brien SJ (1995) Coadaptation and immunodeficiency virus: lessons from the Felidae. Curr Opin Genet Dev 5:739–745PubMedGoogle Scholar
  24. Chen H, Wood C, Petito CK (2000) Comparisons of HIV-1 viral sequences in brain, choroid plexus and spleen: potential role of choroid plexus in the pathogenesis of HIV encephalitis. J Neurovirology 6:498–506Google Scholar
  25. Cloak CC, Chang L, Ernst T, Barr MC, Huitron-Resendiz S, Sanchez-Alavez M, Phillips TR, Henriksen S (2004) Methamphetamine and AIDS: 1HMRS studies in a feline model of human disease. J Neuroimmunol 147:16–20PubMedGoogle Scholar
  26. Cysique LA, Brew BJ, Halman M, Catalan J, Sacktor N, Price RW, Brown S, Atkinson JH, Clifford DB, Simpson D, Torres G, Hall C, Power C, Marder K, McArthur JC, Symonds W, Romero C (2005) Undetectable cerebrospinal fluid HIV RNA and beta-2 microglobulin do not indicate inactive AIDS dementia complex in highly active antiretroviral therapy-treated patients. J Acquir Immune Defic Syndr 39:426–429PubMedGoogle Scholar
  27. D’Cruz OJ, Waurzyniak B, Uckun FM (2004) Antiretroviral spermicide WHI-07 prevents vaginal and rectal transmission of feline immunodeficiency virus in domestic cats. Antimicrob Agents Chemother 48:1082–1088PubMedGoogle Scholar
  28. Danave IR, Tiffany Castiglioni E, Zenger E, Barhoumi R, Burghardt RC, Collisson EW (1994) Feline immunodeficiency virus decreases cell–cell communication and mitochondrial membrane potential. J Virol 68:6745–6750PubMedGoogle Scholar
  29. de Parseval A, Chatterji U, Sun P, Elder JH (2004) Feline immunodeficiency virus targets activated CD4+ T cells by using CD134 as a binding receptor. Proc Natl Acad Sci USA 101:13044–13049PubMedGoogle Scholar
  30. de Ronde A, Stam JG, Boers P, Langedijk H, Meloen R, Hesselink W, Keldermans LC, van Vliet A, Verschoor EJ, Horzinek MC (1994) Antibody response in cats to the envelope proteins of feline immunodeficiency virus: identification of an immunodominant neutralization domain. Virology 198:257–264PubMedGoogle Scholar
  31. de Rozieres S, Swan CH, Sheeter DA, Clingerman KJ, Lin YC, Huitron-Resendiz S, Henriksen S, Torbett BE, Elder JH (2004) Assessment of FIV-C infection of cats as a function of treatment with the protease inhibitor, TL-3. Retrovirology 1:38PubMedGoogle Scholar
  32. Del Mauro D, Matteucci D, Giannecchini S, Maggi F, Pistello M, Bendinelli M (1998) Autologous and heterologous neutralization analyses of primary feline immunodeficiency virus isolates. J Virol 72:2199–2207PubMedGoogle Scholar
  33. Dou H, Birusingh K, Faraci J, Gorantla S, Poluektova LY, Maggirwar SB, Dewhurst S, Gelbard HA, Gendelman HE (2003) Neuroprotective activities of sodium valproate in a murine model of human immunodeficiency virus-1 encephalitis. J Neurosci 23:9162–9170PubMedGoogle Scholar
  34. Dow S, Poss M, Hoover E (1990) Feline immunodeficiency virus: a neurotropic lentivirus. J AIDS 3:658–668Google Scholar
  35. Dow SW, Dreitz MJ, Hoover EA (1992) Feline immunodeficiency virus neurotropism: evidence that astrocytes and microglia are the primary target cells. Vet Immunol Immunopathol 35:23–35PubMedGoogle Scholar
  36. Dow SW, Mathiason CK, Hoover EA (1999) In vivo monocyte tropism of pathogenic feline immunodeficiency viruses. J Virol 73:6852–6861PubMedGoogle Scholar
  37. Egberink H, Borst M, Niphuis H, Balzarini J, Neu H, Schellekens H, De Clercq E, Horzinek M, Koolen M (1990) Suppression of feline immunodeficiency virus infection in vivo by 9-(2-phosphonomethoxyethyl)adenine. Proc Natl Acad Sci USA 87:3087–3091PubMedGoogle Scholar
  38. Egberink HF, De Clercq E, van Vliet AL, Balzarini J, Bridger GJ, Henson G, Horzinek MC, Schols D (1999) Bicyclams, selective antagonists of the human chemokine receptor CXCR4, potently inhibit feline immunodeficiency virus replication. J Virol 73:6346–6352PubMedGoogle Scholar
  39. Elder JH, Phillips TR (1993) Molecular properties of feline immunodeficiency virus (FIV). Infect Agents Dis 2:361–374PubMedGoogle Scholar
  40. Ellis RJ, Gamst AC, Capparelli E, Spector SA, Hsia K, Wolfson T, Abramson I, Grant I, McCutchan JA (2000) Cerebrospinal fluid HIV RNA originates from both local CNS and systemic sources. Neurology 54:927–936PubMedGoogle Scholar
  41. English R, Johnson C, Gebhard DH, Tompkins MB (1993) In vivo lymphocyte tropism of feline immunodeficiency virus. J Virol 67:5175–5186PubMedGoogle Scholar
  42. English RV, Nelson P, Johnson CM, Nasisse M, Tompkins WA, Tompkins MB (1994) Development of clinical disease in cats experimentally infected with feline immunodeficiency virus. J Infect Dis 170:543–552PubMedGoogle Scholar
  43. Epstein LG, Gelbard HA (1999) HIV-1-induced neuronal injury in the developing brain. J Leukoc Biol 65:453–457PubMedGoogle Scholar
  44. Falangola MF, Hanly A, Galvao-Castro B, Petito CK (1995) HIV infection of human choroid plexus: a possible mechanism of viral entry into the CNS. J Neuropathol Exp Sci 54:497–503Google Scholar
  45. Fine SM, Angel RA, Perry SW, Epstein LG, Rothstein JD, Dewhurst S, Gelbard HA (1996) Tumor necrosis factor alpha inhibits glutamate uptake by primary human astrocytes. Implications for pathogenesis of HIV-1 dementia. J Biol Chem 271:15303–15306PubMedGoogle Scholar
  46. Fischer-Smith T, Croul S, Sverstiuk AE, Capini C, L’Heureux D, Regulier EG, Richardson MW, Amini S, Morgello S, Khalili K, Rappaport J (2001) CNS invasion by CD14+/CD16+ peripheral blood-derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection. J Neurovirology 7:528–541Google Scholar
  47. Garg H, Fuller FJ, Tompkins WA (2004) Mechanism of feline immunodeficiency virus envelope glycoprotein-mediated fusion. Virology 321:274–286PubMedGoogle Scholar
  48. Gavrilin MA, Mathes LE, Podell M (2002) Methamphetamine enhances cell-associated feline immunodeficiency virus replication in astrocytes. J Neurovirology 8:240–249Google Scholar
  49. Gebhard DH, Dow JL, Childers TA, Alvelo JI, Tompkins MB, Tompkins WA (1999) Progressive expansion of an l-selectin-negative CD8 cell with anti-feline immunodeficiency virus (FIV) suppressor function in the circulation of FIV-infected cats. J Infect Dis 180:1503–1513PubMedGoogle Scholar
  50. Gemignani A, Paudice P, Pittaluga A, Raiteri M (2000) The HIV-1 coat protein gp120 and some of its fragments potently activate native cerebral NMDA receptors mediating neuropeptide release. Eur J Neurosci 12:2839–2846PubMedGoogle Scholar
  51. Gendelman HE, Lipton SA, Epstein LG, Swindells S (2005) The Neurology of AIDS, 2nd edn.: Oxford University PressGoogle Scholar
  52. Giulian D, Vaca K, Noonan CA (1990) Secretion of neurotoxins by mononuclear phagocytes infected with HIV-1. Science 250:1593–1596PubMedGoogle Scholar
  53. Gonzalez-Scarano F, Martin-Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5:69–81PubMedGoogle Scholar
  54. Gorry PR, Bristol G, Zack JA, Ritola K, Swanstrom R, Birch CJ, Bell JE, Bannert N, Crawford K, Wang H, Schols D, De Clercq E, Kunstman K, Wolinsky SM, Gabuzda D (2001) Macrophage tropism of human immunodeficiency virus type 1 isolates from brain and lymphoid tissues predicts neurotropism independent of coreceptor specificity. J Virol 75:10073–10089PubMedGoogle Scholar
  55. Gruol DL, Yu N, Parsons KL, Billaud JN, Elder JH, Phillips TR (1998) Neurotoxic effects of feline immunodeficiency virus, FIV-PPR. J Neurovirology 4:415–425Google Scholar
  56. Hartmann K, Donath A, Beer B, Egberink HF, Horzinek MC, Lutz H, Hoffmann-Fezer G, Thum I, Thefeld S (1992) Use of two virustatica (AZT, PMEA) in the treatment of FIV and of FeLV seropositive cats with clinical symptoms. Vet Immunol Immunopathol 35:167–175PubMedGoogle Scholar
  57. Haughey NJ, Holden CP, Nath A, Geiger JD (1999) Involvement of inositol 1,4,5-trisphosphate-regulated stores of intracellular calcium in calcium dysregulation and neuron cell death caused by HIV-1 protein tat. J Neurochem 73:1363–1374PubMedGoogle Scholar
  58. Haughey NJ, Nath A, Mattson MP, Slevin JT, Geiger JD (2001) HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J Neurochem 78:457–467PubMedGoogle Scholar
  59. Hayes KA, Wilkinson JG, Frick R, Francke S, Mathes LE (1995) Early suppression of viremia by ZDV does not alter the spread of feline immunodeficiency virus infection in cats. J Acquir Immune Defic Syndr Hum Retrovirol 9:114–122PubMedGoogle Scholar
  60. Hegg CC, Thayer SA (1999) Monocytic cells secrete factors that evoke excitatory synaptic activity in rat hippocampal cultures. Eur J Pharmacol 385:231–237PubMedGoogle Scholar
  61. Hein A, Martin JP, Dorries R (2001) In vitro activation of feline immunodeficiency virus in ramified microglial cells from asymptomatically infected cats. J Virol 75:8090–8095PubMedGoogle Scholar
  62. Hein A, Martin JP, Koehren F, Bingen A, Dorries R (2000) In vivo infection of ramified microglia from adult cat central nervous system by feline immunodeficiency virus. Virology 268:420–429PubMedGoogle Scholar
  63. Hoffmann-Fezer G, Thum J, Ackley C, Herbold M, Mysliwietz J, Thefeld S, Hartmann K, Kraft W (1992) Decline in CD4+ cell numbers in cats with naturally acquired feline immunodeficiency virus infection. J Virol 66:1484–1488PubMedGoogle Scholar
  64. Hohdatsu T, Fujimori S, Maeki M, Suma N, Motokawa K, Okada S, Koyama H (1997) Virus neutralizing antibody titer to feline immunodeficiency virus isolates of subtypes A, B and D in experimentally or naturally infected cats. J Vet Med Sci 59:377–381PubMedGoogle Scholar
  65. Hohdatsu T, Miyagawa N, Ohkubo M, Kida K, Koyama H (2000) Studies on feline CD8+ T cell non-cytolytic anti-feline immunodeficiency virus (FIV) activity. Arch Virol 145:2525–2538PubMedGoogle Scholar
  66. Hohdatsu T, Sasagawa T, Yamazaki A, Motokawa K, Kusuhara H, Kaneshima T, Koyama H (2002) CD8+ T cells from feline immunodeficiency virus (FIV) infected cats suppress exogenous FIV replication of their peripheral blood mononuclear cells in vitro. Arch Virol 147:1517–1529PubMedGoogle Scholar
  67. Holden CP, Haughey NJ, Nath A, Geiger JD (1999) Role of Na+/H+ exchangers, excitatory amino acid receptors and voltage-operated Ca2+ channels in human immunodeficiency virus type 1 gp120-mediated increases in intracellular Ca2+ in human neurons and astrocytes. Neuroscience 91:1369–1378PubMedGoogle Scholar
  68. Hosie MJ, Broere N, Hesselgesser J, Turner JD, Hoxie JA, Neil JC, Willett BJ (1998) Modulation of feline immunodeficiency virus infection by stromal cell-derived factor. J Virol 72:2097–2104PubMedGoogle Scholar
  69. Huang C, Conlee D, Loop J, Champ D, Gill M, Chu HJ (2004) Efficacy and safety of a feline immunodeficiency virus vaccine. Anim Health Res Rev 5:295–300PubMedGoogle Scholar
  70. Hudson LC, Bragg DC, Tompkins MB, Meeker RB (2005) Astrocytes and microglia differentially regulate trafficking of lymphocyte subsets across brain endothelial cells. Brain Res 1058:148–160PubMedGoogle Scholar
  71. Hurtrel M, Ganiere J, Guelifi J, Chakrabarti L, Maire M, Gray F, Montagnier L, Hurtrel B (1992) Comparison of early and late feline immunodeficiency virus encephalopathies. AIDS 6:399–406PubMedGoogle Scholar
  72. Jacobson S, Henricksen SJ, Prospero-Garcia O, Phillips TR, Elder JH, Young WG, Bloom FE, Fox HS (1997) Cortical neuronal cytoskeletal changes associated with FIV infection. Journal Neurovirology 3:283–289Google Scholar
  73. Johnston JB, Power C (2002) Feline immunodeficiency virus xenoinfection: the role of chemokine receptors and envelope diversity. J Virol 76:3626–3636PubMedGoogle Scholar
  74. Jones G, Power C (2006) Regulation of neural cell survival by HIV-1 infection. Neurobiol Dis 21:1–17PubMedGoogle Scholar
  75. Jordan HL, Howard JG, Bucci JG, Butterworth JL, English R, Kennedy-Stoskopf S, Tompkins MB, Tompkins WA (1998) Horizontal transmission of feline immunodeficiency virus with semen from seropositive cats. J Reprod Immunol 41:341–357PubMedGoogle Scholar
  76. Kanki PJ, McLane MF, King NW Jr, Letvin NL, Hunt RD, Sehgal P, Daniel MD, Desrosiers RC, Essex M (1985) Serologic identification and characterization of a macaque T-lymphotropic retrovirus closely related to HTLV-III. Science 228:1199–1201PubMedGoogle Scholar
  77. Kawaguchi Y, Maeda K, Tohya Y, Furuya T, Miyazawa T, Horimoto T, Norimine J, Kai C, Mikami T (1992) Replicative difference in early-passage feline brain cells among feline immunodeficiency virus isolates. Arch Virol 125:347–354PubMedGoogle Scholar
  78. Koenig S, Gendelman HE, Orenstein JM, Dal Canto MC, Pezeshkpour GH, Yungbluth M, Janotta F, Aksamit A, Martin MA, Fauci AS (1986) Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233:1089–1093PubMedGoogle Scholar
  79. Koirala TR, Nakagaki K, Ishida T, Nonaka S, Morikawa S, Tabira T (2001) Decreased expression of MAP-2 and GAD in the brain of cats infected with feline immunodeficiency virus. Tohoku J Exp Med 195:141–151PubMedGoogle Scholar
  80. Kolson DL (2002) Neuropathogenesis of central nervous system HIV-1 infection. Clin Lab Med 22:703–717PubMedGoogle Scholar
  81. Kovacs EM, Baxter GD, Robinson WF (1999) Feline peripheral blood mononuclear cells express message for both CXC and CC type chemokine receptors. Arch Virol 144:273–285PubMedGoogle Scholar
  82. Lane JH, Sasseville VG, Smith MO, Vogel P, Pauley DR, Heyes MP, Lackner AA (1996) Neuroinvasion by simian immunodeficiency virus coincides with increased numbers of perivascular macrophages/microglia and intrathecal immune activation. J Neurovirology 2:423–432Google Scholar
  83. Lerner DL, Elder JH (2000) Expanded host cell tropism and cytopathic properties of feline immunodeficiency virus strain PPR subsequent to passage through interleukin-2-independent T cells. J Virol 74:1854–1863PubMedGoogle Scholar
  84. Levy JA (1993) Pathogenesis of human immunodeficiency virus infection. Microbiol Rev 57:183–289PubMedGoogle Scholar
  85. Lipton S (1992) Models of neuronal injury in AIDS: another role for the NMDA receptor? TINS 15:75–80PubMedGoogle Scholar
  86. Lipton S, Sucher N, Kaiser P, Dreyer E (1991) Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron 7:111–118PubMedGoogle Scholar
  87. Liu P, Hudson LC, Tompkins MB, Vahlenkamp TW, Colby B, Rundle C, Meeker RB (2006a) Cerebrospinal fluid is an efficient route for establishing brain infection with feline immunodeficiency virus and transferring infectious virus to the periphery. J Neurovirology 12:294–306Google Scholar
  88. Liu P, Hudson LC, Tompkins MB, Vahlenkamp TW, Meeker RB (2006b) Compartmentalization and evolution of feline immunodeficiency virus between the central nervous system and periphery following intracerebroventricular or systemic inoculation. J Neurovirology 12:307–321Google Scholar
  89. Livingstone WJ, Moore M, Innes D, Bell JE, Simmonds P (1996) Frequent infection of peripheral blood CD8-positive T-lymphocytes with HIV-1. Edinburgh Heterosexual Transmission Study Group. Lancet 348:649–654PubMedGoogle Scholar
  90. Lo TK, Fallert CJ, Piser TM, Thayer SA (1992) HIV-1 envelope protein evokes intracellular calcium oscillations in rat hippocampal neurons. Brain Res 594:189–196PubMedGoogle Scholar
  91. Lombardi S, Massi C, Tozzini F, Zaccaro L, Bazzichi A, Bandecchi P, La Rosa C, Bendinelli M, Garzelli C (1995) Epitope mapping of the V3 domain of feline immunodeficiency virus envelope glycoprotein by monoclonal antibodies. J Gen Virol 76 (Pt 8):1893–1899PubMedGoogle Scholar
  92. Macchi S, Maggi F, Di Iorio C, Poli A, Bendinelli M, Pistello M (1998) Detection of feline immunodeficiency proviral sequences in lymphoid tissues and the central nervous system by in situ gene amplification. J Virol Methods 73:109–119PubMedGoogle Scholar
  93. Masliah E, Heaton RK, Marcotte TD, Ellis RJ, Wiley CA, Mallory M, Achim CL, McCutchan JA, Nelson JA, Atkinson JH, Grant I (1997) Dendritic injury is a pathological substrate for human immunodeficiency virus-related cognitive disorders. HNRC Group. The HIV Neurobehavioral Research Center. Ann Neurol 42:963–972PubMedGoogle Scholar
  94. McArthur JC, Brew BJ, Nath A (2005) Neurological complications of HIV infection. Lancet Neurol 4:543–555PubMedGoogle Scholar
  95. Meeker R, English R, Tompkins M (1996) Enhanced excitotoxicity in primary feline neural cultures exposed to feline immunodeficiency virus (FIV). J Neuro-AIDS 1:1–27Google Scholar
  96. Meeker RB, Azuma Y, Bragg DC, English RV, Tompkins M (1999a) Microglial proliferation in cortical neural cultures exposed to feline immunodeficiency virus. J Neuroimmunol 101:15–26PubMedGoogle Scholar
  97. Meeker RB, Boles JC, Robertson KR, Hall CD (2005) Cerebrospinal fluid from human immunodeficiency virus-infected individuals facilitates neurotoxicity by suppressing intracellular calcium recovery. J Neurovirology 11:144–156Google Scholar
  98. Meeker RB, Robertson K, Barry T, Hall C (1999b) Neurotoxicity of CSF from HIV-infected humans. J Neurovirology 5:507–518Google Scholar
  99. Meeker RB, Thiede BA, Hall C, English R, Tompkins M (1997) Cortical cell loss in asymptomatic cats experimentally infected with feline immunodeficiency virus. AIDS Res Hum Retrovir 13:1131–1140PubMedCrossRefGoogle Scholar
  100. Mitchell TW, Buckmaster PS, Hoover EA, Whalen LR, Dudek FE (1999) Neuron loss and axon reorganization in the dentate gyrus of cats infected with the feline immunodeficiency virus. J Comp Neurol 411:563–577PubMedGoogle Scholar
  101. Nagra RM, Masliah E, Wiley CA (1993) Synaptic and dendritic pathology in murine retroviral encephalitis. Exp Neurol 124:283–288PubMedGoogle Scholar
  102. Nakagaki K, Nakagaki K, Takahashi K, Schols D, De Clercq E, Tabira T (2001) CXCR4 is the primary receptor for feline immunodeficiency virus in astrocytes. J Neurovirology 7:487–492Google Scholar
  103. Neuenburg JK, Brodt HR, Herndier BG, Bickel M, Bacchetti P, Price RW, Grant RM, Schlote W (2002) HIV-related neuropathology, 1985 to 1999: rising prevalence of HIV encephalopathy in the era of highly active antiretroviral therapy. J Acquir Immune Defic Syndr 31:171–177PubMedGoogle Scholar
  104. Novotney C, English R, Housman J, Davidson M, Nasisse M, Jeng CR, Davis W, Tompkins M (1990) Lymphocyte population changes in cats naturally infected with feline immunodeficiency virus. AIDS 4:1213–1218PubMedGoogle Scholar
  105. O’Neil LL, Burkhard MJ, Hoover EA (1996) Frequent perinatal transmission of feline immunodeficiency virus by chronically infected cats. J Virol 70:2894–2901PubMedGoogle Scholar
  106. Obert LA, Hoover EA (2002) Early pathogenesis of transmucosal feline immunodeficiency virus infection. J Virol 76:6311–6322PubMedGoogle Scholar
  107. Olmsted R, Hirsch V, Purcell R, Johnson P (1989) Nucleotide sequence analysis of feline immunodeficiency virus:genome organization and relationship to other lentiviruses. Proc Natl Acad Sci 86:8088–8092PubMedGoogle Scholar
  108. Osborne R, Rigby M, Siebelink K, Neil JC, Jarrett O (1994) Virus neutralization reveals antigenic variation among feline immunodeficiency virus isolates. J Gen Virol 75 (Pt 12):3641–3645PubMedGoogle Scholar
  109. Pedersen NC, Ho EW, Brown ML, Yamamoto JK (1987) Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science 235:790–793PubMedGoogle Scholar
  110. Perry SW, Norman JP, Gelbard HA (2005) Adjunctive therapies for HIV-1 associated neurologic disease. Neurotox Res 8:161–166PubMedGoogle Scholar
  111. Persidsky Y, Stins M, Way D, Witte MH, Weinand M, Kim KS, Bock P, Gendelman HE, Fiala M (1997) A model for monocyte migration through the blood–brain barrier during HIV-1 encephalitis. J Immunol 158:3499–3510PubMedGoogle Scholar
  112. Petito CK (2004) Human immunodeficiency virus type 1 compartmentalization in the central nervous system. J Neurovirology 10 Suppl 1:21–24Google Scholar
  113. Petito CK, Chen H, Mastri AR, Torres-Munoz J, Roberts B, Wood C (1999) HIV infection of choroid plexus in AIDS and asymptomatic HIV-infected patients suggests that the choroid plexus may be a reservoir of productive infection. J Neurovirology 5:670–677Google Scholar
  114. Phillips T, Prospero-Garcia O, Puaoi D, Lerner D, Fox H, Olmsted R, Bloom F, Heriksen S, Elder J (1994) Neurological abnormalities associated with feline immunodeficiency virus infection. J Gen Virol 75:979–987PubMedGoogle Scholar
  115. Phillips TR, Prospero-Garcia O, Wheeler DW, Wagaman P, Lerner DL, Fox HS, Whalen LR, Bloom FE, Elder JH, Henricksen SJ (1996) Neurologic dysfunctions caused by a molecular clone of feline immunodeficiency virus, FIV-PPR. J Neurovirology 2:388–396Google Scholar
  116. Phipps AJ, Hayes KA, Buck WR, Podell M, Mathes LE (2000) Neurophysiologic and immunologic abnormalities associated with feline immunodeficiency virus molecular clone FIV-PPR DNA inoculation. J Acquir Immune Defic Syndr 23:8–16PubMedGoogle Scholar
  117. Pistello M, Menzo S, Giorgi M, Da Prato L, Cammarota G, Clementi M, Bendinelli M (1994) Competitive polymerase chain reaction for quantitating feline immunodeficiency virus load in infected cat tissues. Mol Cell Probes 8:229–234PubMedGoogle Scholar
  118. Podell M, Hayes K, Oglesbee M, Mathes L (1997) Progressive encephalopathy associated with CD4/CD8 inversion in adult FIV-infected cats. J Acquir Immune Defic Syndr Hum Retrovirol 15:332–340PubMedGoogle Scholar
  119. Podell M, Maruyama K, Smith M, Hayes KA, Buck WR, Ruehlmann DS, Mathes LE (1999) Frontal lobe neuronal injury correlates to altered function in FIV-infected cats. J Acquir Immune Defic Syndr 22:10–18PubMedGoogle Scholar
  120. Podell M, Oglesbee M, Mathes L, Krakowka S, Olmstead R, Lafrado L (1993) AIDS-associated encephalopathy with experimental feline immunodeficiency virus Infection. J AIDS 6:758–771Google Scholar
  121. Poli A, Abramo F, Di Iorio C, Cantile C, Carli MA, Pollera C, Vago L, Tosoni A, Costanzi G (1997) Neuropathology in cats experimentally infected with feline immunodeficiency virus: a morphological, immunocytochemical and morphometric study. J Neurovirology 3:361–368CrossRefGoogle Scholar
  122. Poli A, Pistello M, Carli MA, Abramo F, Mancuso G, Nicoletti E, Bendinelli M (1999) Tumor necrosis factor-alpha and virus expression in the central nervous system of cats infected with feline immunodeficiency virus. J Neurovirology 5:465–473Google Scholar
  123. Potter SJ, Dwyer DE, Saksena NK (2003) Differential cellular distribution of HIV-1 drug resistance in vivo: evidence for infection of CD8+ T cells during HAART. Virology 305:339–352PubMedGoogle Scholar
  124. Power C, Buist R, Johnston JB, Del Bigio MR, Ni W, Dawood MR, Peeling J (1998) Neurovirulence in feline immunodeficiency virus-infected neonatal cats is viral strain specific and dependent on systemic immune suppression. J Virol 72:9109–9115PubMedGoogle Scholar
  125. Power C, Moench T, Peeling J, Kong PA, Langelier T (1997) Feline immunodeficiency virus causes increased glutamate levels and neuronal loss in brain. Neuroscience 77:1175–1185PubMedGoogle Scholar
  126. Prospero-Garcia O, Herold N, Phillips T, Elder J, Bloom F, Henriksen S (1994) Sleep patterns are disturbed in cats infected with feline immunodeficiency virus. Proc Natl Acad Sci 91:12947–12951PubMedGoogle Scholar
  127. Pu R, Coleman J, Omori M, Arai M, Hohdatsu T, Huang C, Tanabe T, Yamamoto JK (2001) Dual-subtype FIV vaccine protects cats against in vivo swarms of both homologous and heterologous subtype FIV isolates. AIDS 15:1225–1237PubMedGoogle Scholar
  128. Pulliam L, Herndier BG, Tang NM, McGrath MS (1991) Human immunodeficiency virus-infected macrophages produce soluble factors that cause histological and neurochemical alterations in cultured human brains. J Clin Invest 87:503–512PubMedGoogle Scholar
  129. Richardson J, Fossati I, Moraillon A, Castelot S, Sonigo P, Pancino G (1996) Neutralization sensitivity and accessibility of continuous B cell epitopes of the feline immunodeficiency virus envelope. J Gen Virol 77 (Pt 4):759–771PubMedGoogle Scholar
  130. Richardson J, Pancino G, Merat R, Leste-Lasserre T, Moraillon A, Schneider-Mergener J, Alizon M, Sonigo P, Heveker N (1999) Shared usage of the chemokine receptor CXCR4 by primary and laboratory-adapted strains of feline immunodeficiency virus. J Virol 73:3661–3671PubMedGoogle Scholar
  131. Ryan G, Grimes T, Brankin B, Mabruk MJ, Hosie MJ, Jarrett O, Callanan JJ (2005) Neuropathology associated with feline immunodeficiency virus infection highlights prominent lymphocyte trafficking through both the blood–brain and blood–choroid plexus barriers. J Neurovirology 11:337–345Google Scholar
  132. Ryan G, Klein D, Knapp E, Hosie MJ, Grimes T, Mabruk MJ, Jarrett O, Callanan JJ (2003) 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 77:7477–7485PubMedGoogle Scholar
  133. Sacktor N, McDermott MP, Marder K, Schifitto G, Selnes OA, McArthur JC, Stern Y, Albert S, Palumbo D, Kieburtz K, De Marcaida JA, Cohen B, Epstein L (2002) HIV-associated cognitive impairment before and after the advent of combination therapy. J Neurovirology 8:136–142Google Scholar
  134. Self RL, Mulholland PJ, Nath A, Harris BR, Prendergast MA (2004) The human immunodeficiency virus type-1 transcription factor Tat produces elevations in intracellular Ca2+ that require function of an N-methyl-d-aspartate receptor polyamine-sensitive site. Brain Res 995:39–45PubMedGoogle Scholar
  135. Shimojima M, Miyazawa T, Ikeda Y, McMonagle EL, Haining H, Akashi H, Takeuchi Y, Hosie MJ, Willett BJ (2004) Use of CD134 as a primary receptor by the feline immunodeficiency virus. Science 303:1192–1195PubMedGoogle Scholar
  136. Siebelink KH, Bosch ML, Rimmelzwaan GF, Meloen RH, Osterhaus AD (1995) Two different mutations in the envelope protein of feline immunodeficiency virus allow the virus to escape from neutralization by feline serum antibodies. Vet Immunol Immunopathol 46:51–59PubMedGoogle Scholar
  137. Silvotti L, Corradi A, Brandi G, Cabassi A, Bendinelli M, Magnan M, Piedimonte G (1997) FIV induced encephalopathy: early brain lesions in the absence of viral replication in monocyte/macrophages. A pathogenetic model. Vet Immunol Immunopathol 55:263–271PubMedGoogle Scholar
  138. Steffan AM, Lafon ME, Gendrault JL, Koehren F, De Monte M, Royer C, Kirn A, Gut JP (1994) Feline immunodeficiency virus can productively infect cultured endothelial cells from cat brain microvessels. J Gen Virol 75:3647–3653PubMedCrossRefGoogle Scholar
  139. Steffen BJ, Breier G, Butcher EC, Schulz M, Engelhardt B (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 148:1819–1838PubMedGoogle Scholar
  140. Steigerwald ES, Sarter M, March P, Podell M (1999) Effects of feline immunodeficiency virus on cognition and behavioral function in cats. J Acquir Immune Defic Syndr Hum Retrovirol 20:411–419PubMedGoogle Scholar
  141. Strain MC, Letendre S, Pillai SK, Russell T, Ignacio CC, Gunthard HF, Good B, Smith DM, Wolinksy SM, Furtado M, Marquie-Beck J, Durelle J, Grant I, Richman DD, Marcotte T, McCutchan JA, Ellis RJ, Wong JK (2005) Genetic composition of human immunodeficiency virus type 1 in cerebrospinal fluid and blood without treatment and during failing antiretroviral therapy. J Virol 79:1772–1788PubMedGoogle Scholar
  142. Talbott RL, Sparger EE, Lovelace KM, Fitch WM, Pedersen NC, Luciw PA, Elder JH (1989) Nucleotide sequence and genomic organization of feline immunodeficiency virus. Proc Natl Acad Sci USA 86:5743–5747PubMedGoogle Scholar
  143. Toggas SM, Masliah E, Mucke L (1996) Prevention of HIV-1 gp120-induced neuronal damage in the central nervous system of transgenic mice by the NMDA receptor antagonist memantine. Brain Res 706:303–307PubMedGoogle Scholar
  144. Tompkins MB, Nelson PD, English RV, Novotney C (1991) Early events in the immunopathogenesis of feline retrovirus infections. JAVMA 199:1311–1315PubMedGoogle Scholar
  145. Torten M, Franchini M, Barlough JE, George JW, Mozes E, Lutz H, Pedersen NC (1991) Progressive immune dysfunction in cats experimentally infected with feline immunodeficiency virus. J Virol 65:2225–2230PubMedGoogle Scholar
  146. Turchan J, Sacktor N, Wojna V, Conant K, Nath A (2003) Neuroprotective therapy for HIV dementia. Curr HIV Res 1:373–383PubMedGoogle Scholar
  147. Tymianski M (1996) Cytosolic calcium concentrations and cell death in vitro. Adv Neurol 71:85–105PubMedGoogle Scholar
  148. Tymianski M, Charlton MP, Carlen PL, Tator CH (1993) Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J Neurosci 13:2085–2104PubMedGoogle Scholar
  149. Uhl EW, Heaton-Jones TG, Pu R, Yamamoto JK (2002) FIV vaccine development and its importance to veterinary and human medicine: a review FIV vaccine 2002 update and review. Vet Immunol Immunopathol 90:113–132PubMedGoogle Scholar
  150. Vahlenkamp TW, Tompkins MB, Tompkins WA (2005) The role of CD4+CD25+ regulatory T cells in viral infections. Vet Immunol Immunopathol 108:219–225PubMedGoogle Scholar
  151. Wasmoen T, Armiger-Luhman S, Egan C, Hall V, Chu HJ, Chavez L, Acree W (1992) Transmission of feline immunodeficiency virus from infected queens to kittens. Vet Immunol Immunopathol 35:83–93PubMedGoogle Scholar
  152. Wiley C, Masliah E, Morey M, Lemere C, DeTeresa R, Grafe M, Hansen L, Terry R (1991) Neocortical damage during HIV infection. Ann Neurol 29:651–657PubMedGoogle Scholar
  153. Willett BJ, Cannon CA, Hosie MJ (2002) Upregulation of surface feline CXCR4 expression following ectopic expression of CCR5: implications for studies of the cell tropism of feline immunodeficiency virus. J Virol 76:9242–9252PubMedGoogle Scholar
  154. Willett BJ, Hosie MJ, Callanan JJ, Neil JC, Jarrett O (1993) Infection with feline immunodeficiency virus is followed by the rapid expansion of a CD8+ lymphocyte subset. Immunology 78:1–6PubMedGoogle Scholar
  155. Willett BJ, Picard L, Hosie MJ, Turner JD, Adema K, Clapham PR (1997) Shared usage of the chemokine receptor CXCR4 by the feline and human immunodeficiency viruses. J Virol 71:6407–6415PubMedGoogle Scholar
  156. Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, deBakker C, Alvarez X, Lackner AA (2001) Perivascular macrophages are the primary cell type productively infected by simian immunodeficiency virus in the brains of macaques: implications for the neuropathogenesis of AIDS. J Exp Med 193:905–915PubMedGoogle Scholar
  157. Xiong H, Zheng J, Thylin M, Gendelman HE (1999) Unraveling the mechanisms of neurotoxicity in HIV type 1-associated dementia: inhibition of neuronal synaptic transmission by macrophage secretory products. AIDS Res Hum Retrovir 15:57–63PubMedGoogle Scholar
  158. Yeh MW, Kaul M, Zheng J, Nottet HS, Thylin M, Gendelman HE, Lipton SA (2000) Cytokine-stimulated, but not HIV-infected, human monocyte-derived macrophages produce neurotoxic levels of l-cysteine. J Immunol 164:4265–4270PubMedGoogle Scholar
  159. Yu N, Billaud JN, Phillips TR (1998) Effects of feline immunodeficiency virus on astrocyte glutamate uptake: implications for lentivirus-induced central nervous system diseases. Proc Natl Acad Sci USA 95:2624–2629PubMedGoogle Scholar
  160. Zenger E, Collisson EW, Barhoumi R, Burghardt RC, Danave IR, Tiffany-Castiglioni E (1995) Laser cytometric analysis of FIV-induced injury in astroglia. Glia 13:92–100PubMedGoogle Scholar
  161. Zenger E, Tiffany-Castiglioni E, Collisson EW (1997) Cellular mechanisms of feline immunodeficiency virus (FIV)-induced neuropathogenesis. Front Biosci 2:d527–d537PubMedGoogle Scholar
  162. Zheng J, Ghorpade A, Niemann D, Cotter RL, Thylin MR, Epstein L, Swartz JM, Shepard RB, Liu X, Nukuna A, Gendelman HE (1999a) Lymphotropic virions affect chemokine receptor-mediated neural signaling and apoptosis: implications for human immunodeficiency virus type 1-associated dementia. J Virol 73:8256–8267PubMedGoogle Scholar
  163. Zheng J, Thylin MR, Cotter RL, Lopez AL, Ghorpade A, Persidsky Y, Xiong H, Leisman GB, Che MH, Gendelman HE (2001) HIV-1 infected and immune competent mononuclear phagocytes induce quantitative alterations in neuronal dendritic arbor: relevance for HIV-1-associated dementia. Neurotox Res 3:443–459PubMedCrossRefGoogle Scholar
  164. Zheng J, Thylin MR, Ghorpade A, Xiong H, Persidsky Y, Cotter R, Niemann D, Che M, Zeng YC, Gelbard HA, Shepard RB, Swartz JM, Gendelman HE (1999b) Intracellular CXCR4 signaling, neuronal apoptosis and neuropathogenic mechanisms of HIV-1-associated dementia. J Neuroimmunol 98:185–200PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Department of NeurologyUniversity of North CarolinaChapel HillUSA

Personalised recommendations