Skip to main content

Advertisement

Log in

Infection of the choroid plexus by feline immunodeficiency virus

  • Published:
Journal of NeuroVirology Aims and scope Submit manuscript

Abstract

The human, simian, and feline immunodeficiency viruses rapidly penetrate into the brain and trigger an inflammatory process that can lead to significant neurologic disease. However, the mechanisms that permit efficient trafficking of macrophage-tropic and the more neurotoxic lymphocytotropic isolates are still poorly understood. One potential source of virus entry may be the blood-CSF barrier provided by the choroid plexus. Infected cells are often detected within the choroid plexus but it is unclear whether this reflects trafficking cells or infection of the large macrophage population within the choroidal stroma. To address this issue, we cultured fetal feline choroid plexus and evaluated the ability of feline immunodeficiency virus (FIV) to establish a primary infection. Significant provirus was detected in macrophage-enriche d choroid plexus cultures as well as in the choroid plexus of cats infected in vivo. FIV p24 antigen production in vitro was very low but detectable. Addition of a feline T-cell line to macrophages inoculated with FIV resulted in a dense clustering of the T cells over macrophages with dendritic cell-like morphologies and a robust productive infection. The direct infection of choroid plexus macrophages with FIV, the efficient transfer of the infection to T cells indicate that the choroid plexus can be a highly efficient site of viral infection and perhaps trafficking of both macrophage-tropic and T-cell-tropic viruses into the CNS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albright AV, Shieh JT, Itoh T, Lee B, Pleasure D, O’Connor MJ, Doms RW, Gonzalez-Scarano F (1999). Microglia express CCR5, CXCR4, and CCR3, but of these, CCR5 is the principal coreceptor for human immunodeficiency virus type 1 dementia isolates. J Virol 73: 205–213.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Armitage RJ, Fanslow WC, Strockbine L, Sato TA, Clifford KN, Macduff BM, Anderson DM, Gimpel SD, Davis-Smith T, Maliszewski CR (1992). Molecular and biological characterization of a murine ligand for CD40. Nature 357: 80–82.

    Article  CAS  PubMed  Google Scholar 

  • Ayehunie S, Garcia-Zepeda EA, Hoxie JA, Horuk R, Kupper TS, Luster AD, Ruprecht RM (1997). Human immunodeficiency virus-1 entry into purified blood dendritic cells through CC and CXC chemokine coreceptors. Blood 90: 1379–1386.

    CAS  PubMed  Google Scholar 

  • Bagasra O, Lavi E, Bobroski L, Khalili K, Pestaner JP, Tawadros R, Pomerantz RJ (1996). Cellular reservoirs of HIV-1 in the central nervous system of infected individuals: identification by the combination of in situ polymerase chain reaction and immunohistochemistry. AIDS 10: 573–585.

    Article  CAS  PubMed  Google Scholar 

  • Banchereau J, Steinman RM (1998). Dendritic cells and the control of immunity. Nature 392: 245–252.

    Article  CAS  PubMed  Google Scholar 

  • Barr MC, Huitron-Resendiz S, Selway DR, Henriksen SJ, Phillips TR (2000). Exogenous glucocorticoids alter parameters of early feline immunodeficiency virus infection. J Infect Dis 181: 576–586.

    Article  CAS  PubMed  Google Scholar 

  • 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: 3080–3091.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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: 180–188.

    Article  CAS  PubMed  Google Scholar 

  • Blauvelt A, Asada H, Saville MW, Klaus-Kovtun V, Altman DJ, Yarchoan R, Katz SI (1997). Productive infection of dendritic cells by HIV-1 and their ability to capture virus are mediated through separate pathways. J Clin Invest 100: 2043–2053.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cameron P, Pope M, Granelli-Piperno A, Steinman RM (1996). Dendritic cells and the replication of HIV-1. J Leukoc Biol 59: 158–171.

    CAS  PubMed  Google Scholar 

  • Cameron PU, Freudenthal PS, Barker JM, Gezelter S, Inaba K, Steinman RM (1992). Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 257: 383–387.

    Article  CAS  PubMed  Google Scholar 

  • Cameron PU, Lowe MG, Crowe SM, O’Doherty U, Pope M, Gezelter S, Steinman RM (1994). Susceptibility of dendritic cells to HIV-1 infection in vitro. J Leukoc Biol 56: 257–265.

    CAS  PubMed  Google Scholar 

  • Caux C, Massacrier C, Vanbervliet B, Dubois B, Van Kooten C, Durand I, Banchereau J (1994). Activation of human dendritic cells through CD40 cross-linking. J Exp Med 180: 1263–1272.

    Article  CAS  PubMed  Google Scholar 

  • 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 NeuroVirol 6: 498–506.

    Article  CAS  PubMed  Google Scholar 

  • Clark EA (1996). HIV: dendritic cells as embers for the infectious fire. Curr Biol 6: 655–657.

    Article  CAS  PubMed  Google Scholar 

  • Czub S, Muller JG, Czub M, Muller-Hermelink HK (1996a). Nature and sequence of simian immunodeficiency virus-induced central nervous system lesions: a kinetic study. Acta Neuropathol (Berl) 92: 487–498.

    Article  CAS  Google Scholar 

  • Czub S, Muller JG, Czub M, Muller-Hermelink HK (1996b). Impact of various simian immunodeficiency virus variants on induction and nature of neuropathology in macaques. Res Virol 147: 165–170.

    Article  CAS  PubMed  Google Scholar 

  • Dean AF, Montgomery M, Baskerville A, Cook RW, Cranage MP, Sharpe SA, Dennis MJ, Luthert PJ, Hou S-T, Lantos PL (1993). Different patterns of neuropathological disease in rhesus monkeys infected by simian immunodeficiency virus, and their relation to the humoral immune response. Neuropathol Appl Neurobiol 19: 336–345.

    Article  CAS  PubMed  Google Scholar 

  • Dean GA, Himathongkham S, Sparger EE (1999). Differential cell tropism of feline immunodeficiency virus molecular clones in vivo. J Virol 73: 2596–2603.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dow S, Poss M, Hoover E (1990). Feline immunodeficiency virus: a neurotropic lentivirus. J AIDS 3: 658–668.

    CAS  Google Scholar 

  • Dow SW, Mathiason CK, Hoover EA (1999). In vivo monocyte tropism of pathogenic feline immunodeficiency viruses. J Virol 73: 6852–6861.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Eggers CC, van Lunzen J, Buhk T, Stellbrink HJ (1999). HIV infection of the central nervous system is characterized by rapid turnover of viral RNA in cerebrospinal fluid. J Acquir Immune Defic Syndr Hum Retrovirol 20: 259–264.

    Article  CAS  PubMed  Google Scholar 

  • Ellis RJ, Hsia K, Spector SA, Nelson JA, Heaton RK, Wallace MR, Abramson I, Atkinson JH, Grant I, McCutchan JA (1997). Cerebrospinal fluid human immunodeficiency virus type 1 RNA levels are elevated in neurocognitively impaired individuals with acquired immunodeficiency syndrome. HIV Neurobehavioral Research Center Group. Ann Neurol 42: 679–688.

    Article  CAS  PubMed  Google Scholar 

  • Endo Y, Mizuno T, Nishimura Y, Goto Y, Watari T, Tsujimoto H, Hasegawa A (1998). Molecular cloning of feline CC-chemokine cDNAs. Vet Immunol Immunopathol 65: 113–123.

    Article  CAS  PubMed  Google Scholar 

  • English R, Johnson C, Gebhard DH, Tompkins MB (1993). in vivo lymphocyte tropism of feline immunodeficiency virus. J Virol 67: 5175–5186.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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: 497–503.

    Article  CAS  Google Scholar 

  • Flechner ER, Freudenthal PS, Kaplan G, Steinman RM (1988). Antigen-specific T lymphocytes efficiently cluster with dendritic cells in the human primary mixed-leukocyte reaction. Cell Immunol 111: 183–195.

    Article  CAS  PubMed  Google Scholar 

  • Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y (2000). DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587–597.

    Article  CAS  PubMed  Google Scholar 

  • Gisslen M, Fuchs D, Svennerholm B, Hagberg L (1999). Cerebrospinal fluid viral load, intrathecal immunoactivation, and cerebrospinal fluid monocytic cell count in HIV-1 infection. J Acquir Immune Defic Syndr 21: 271–276.

    Article  CAS  PubMed  Google Scholar 

  • Granelli-Piperno A, Delgado E, Finkel V, Paxton W, Steinman RM (1998). Immature dendritic cells selectively replicate macrophagetropi c (M-tropic) human immunodeficiency virus type 1, while mature cells efficiently transmit both M- and T-tropic virus to T cells. J Virol 72: 2733–2737.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grouard G, Clark EA (1997). Role of dendritic and follicular dendritic cells in HIV infection and pathogenesis. Curr Opin Immunol 9: 563–567.

    Article  CAS  PubMed  Google Scholar 

  • Gruol DL, Yu N, Parsons KL, Billaud JN, Elder JH, Phillips TR (1998). Neurotoxic effects of feline immunodeficiency virus, FIV-PPR. J Neuro Virol 4: 415–425.

    CAS  Google Scholar 

  • Haase AT, Henry K, Zupancic M, Sedgewick G, Faust RA, Melroe H, Cavert W, Gebhard K, Staskus K, Zhang ZQ, Dailey PJ, Balfour HH, Erice A, Perelson AS (1996). Quantitative image analysis of HIV-1 infection in lymphoid tissue. Science 274: 985–989.

    Article  CAS  PubMed  Google Scholar 

  • Hanly A, Petito CK (1998). HLA-DR-positive dendritic cells of the normal human choroid plexus. A potential reservoir of HIV in the central nervous system. Human Pathol 29: 88–93.

    Article  CAS  Google Scholar 

  • Harouse JM, Wroblewska Z, Laughlin MA, Hickey WF, Schonwetter BS, Gonzalez-Scarano F (1989). Human choroid plexus cells can be latently infected with human immunodeficiency virus. Ann Neurol 25: 406–411.

    Article  CAS  PubMed  Google Scholar 

  • He J, Chen Y, Farzan M, Choe H, Ohagen A, Gartner S, Busciglio J, Yang X, Hofmann W, Newman W, Mackay CR, Sodroski J, Gabuzda D (1997). CCR3 and CCR5 are coreceptors for HIV-1 infection of microglia. Nature 385: 645–649.

    Article  CAS  PubMed  Google Scholar 

  • Janssen RS (1991). Nomenclature and research case definitions for neurologic manifestations of human immunodeficiency virus-type 1 (HIV-1) infection. Neurology 41: 778–785.

    Article  Google Scholar 

  • Kelder W, McArthur JC, Nance-Sproson T, McClernon D, Griffin DE (1998). Beta-chemokines MCP-1 and RANTES are selectively increased in cerebrospinal fluid of patients with human immunodeficiency virus-associated dementia. Ann Neurol 44: 831–835.

    Article  CAS  PubMed  Google Scholar 

  • Knight SC, Patterson S (1997). Bone marrow-derived dendritic cells, infection with human immunodeficiency virus, and immunopathology. Annu Rev Immunol 15: 593–615.

    Article  CAS  PubMed  Google Scholar 

  • Lackner AA, Smith MO, Munn RJ, Martfeld DJ, Gardner MB, Marx PA, Dandekar S (1991). Localization of simian immunodeficiency virus in the central nervous system of rhesus monkeys. Am J Pathol 139: 609–621.

    CAS  PubMed  Google Scholar 

  • Lane JH, Tarantal AF, Pauley D, Marthas M, Miller CJ, Lackner AA (1996). Localization of simian immunodeficiency virus nucleic acid and antigen in brains of fetal macaques inoculated in utero. Am J Pathol 149: 1097–1104.

    CAS  PubMed  Google Scholar 

  • Letendre SL, Lanier ER, McCutchan JA (1999). Cerebrospinal fluid beta chemokine concentrations in neurocognitively impaired individuals infected with human immunodeficiency virus type 1. J Infect Dis 180: 310–319.

    Article  CAS  PubMed  Google Scholar 

  • Ling EA (1979). Ultrastructure and origin of epiplexus cells in the telencephalic choroid plexus of postnatal rats studied by intravenous injection of carbon particles. J Anat 129: 479–492.

    CAS  PubMed  Google Scholar 

  • Ling EA (1981). Ultrastructure and mode of formation of epiplexus cells in the choroid plexus in the lateral ventricles of the monkey (Macaca fascicularis). J Anat 133: 555–569.

    CAS  PubMed  Google Scholar 

  • Ling EA (1983). Scanning electron microscopic study of epiplexus cells in the lateral ventricles of the monkey (Macaca fascicularis). J Anat 137(Pt 4): 645–652.

    PubMed  Google Scholar 

  • Liu Y, Tang XP, McArthur JC, Scott J, Gartner S (2000). Analysis of human immunodeficiency virus type 1 gp160 sequences from a patient with HIV dementia: evidence for monocyte trafficking into brain. J Neuro Virol 6 Suppl 1: S70-S81.

    CAS  Google Scholar 

  • Marker O, Scheynius A, Christensen JP, Thomsen AR (1995). Virus-activated T cells regulate expression of adhesion molecules on endothelial cells in sites of infection. J Neuroimmunol 62: 35–42.

    Article  CAS  PubMed  Google Scholar 

  • Martin C, Albert J, Hansson P, Pehrsson P, Link H, Sonnerborg A (1998). Cerebrospinal fluid mononuclear cell counts influence CSF HIV-1 RNA levels. J Acquir Immune Defic Syndr Hum Retrovirol 17: 214–219.

    Article  CAS  PubMed  Google Scholar 

  • Matyszak MK, Perry V (1996). The potential role of dendritic cells in immune-mediated inflammatory diseases of the central nervous system. Neuroscience 74: 599–608.

    Article  CAS  PubMed  Google Scholar 

  • McArthur JC, Sipos E, Cornblath DR, Welch D, Chupp M, Griffin DE, Johnson RT (1989). Identification of mononuclear cells in CSF of patients with HIV infection. Neurology 39: 66–70.

    Article  CAS  PubMed  Google Scholar 

  • McMenamin PG (1999). Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges, and choroid plexus of the rat brain as demonstrated in wholemount preparations. J Comp Neurol 405: 553–562.

    Article  CAS  PubMed  Google Scholar 

  • Meeker RB, Azuma Y, Bragg DC, English RV, Tompkins M (1999). Microglial proliferation in cortical neural cultures exposed to feline immunodeficiency virus. J Neuroimmunol 101: 15–26.

    Article  CAS  PubMed  Google Scholar 

  • Meeker RB, English R, Tompkins M (1996). Enhanced excitotoxicity in primary feline neural cultures exposed to feline immunodeficiency virus (FIV). J Neuro AIDS 1: 1–27.

    Article  Google Scholar 

  • 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 Retroviruses 13: 1131–1140.

    Article  CAS  PubMed  Google Scholar 

  • Pantaleo G, Graziosi C, Demarest JF, Butini L, Montroni M, Fox CH, Orenstein JM, Kotler DP, Fauci AS (1993). HIV infection is active and progressive in lymphoid tissue during the clinically latent stage of disease. Nature 362: 355–358.

    Article  CAS  PubMed  Google Scholar 

  • 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 Neuro Virol 5: 670–677.

    CAS  Google Scholar 

  • 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 General Virol 75: 979–987.

    Article  CAS  Google Scholar 

  • 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 Neuro Virol 2: 388–396.

    CAS  Google Scholar 

  • 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: 332–340.

    Article  CAS  PubMed  Google Scholar 

  • 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: 10–18.

    Article  CAS  PubMed  Google Scholar 

  • 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: 758–771.

    CAS  Google Scholar 

  • Pope M (1999). Mucosal dendritic cells and immunodeficiency viruses. J Infect Dis 179 Suppl 3: S427-S430.

    Article  PubMed  Google Scholar 

  • Pope M, Betjes MG, Romani N, Hirmand H, Hoffman L, Gezelter S, Schuler G, Cameron PU, Steinman RM (1995a). Dendritic cell-T cell conjugates that migrate from normal human skin are an explosive site of infection for HIV-1. Adv Exp Med Biol 378: 457–460.

    Article  CAS  PubMed  Google Scholar 

  • Pope M, Gezelter S, Gallo N, Hoffman L, Steinman RM (1995b). Low levels of HIV-1 infection in cutaneous dendritic cells promote extensive viral replication upon binding to memory CD4+ T cells. J Exp Med 182: 2045–2056.

    Article  CAS  PubMed  Google Scholar 

  • 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 USA 91: 12947–12951.

    Article  CAS  PubMed  Google Scholar 

  • Rubbert A, Combadiere C, Ostrowski M, Arthos J, Dybul M, Machado E, Cohn MA, Hoxie JA, Murphy PM, Fauci AS, Weissman D (1998). Dendritic cells express multiple chemokine receptors used as coreceptors for HIV entry. J Immunol 160: 3933–3941.

    CAS  PubMed  Google Scholar 

  • Schmitz J, van Lunzen J, Tenner-Racz K, Grossschupff G, Racz P, Schmitz H, Dietrich M, Hufert F (1994). Follicular dendritic cells (FDC) are not productively infected with HIV-1 in vivo. Adv Exp Med Biol 355: 165–168.

    Article  CAS  PubMed  Google Scholar 

  • Schuurman HJ, Joling P, van Wichen DF, Rademakers LH, Broekhuizen R, de Weger RA, van den Tweel JG, Goudsmit J (1995). Follicular dendritic cells and infection by human immunodeficiency virus type 1—a crucial target cell and virus reservoir. Curr Top Microbiol Immunol 201: 161–188.

    CAS  PubMed  Google Scholar 

  • Serot JM, Bene MC, Foliguet B, Faure GC (2000). Monocyte-derived IL-10-secreting dendritic cells in choroid plexus epithelium. J Neuroimmunol 105: 115–119.

    Article  CAS  PubMed  Google Scholar 

  • Serot JM, Foliguet B, Bene MC, Faure GC (1997). Ultrastructural and immunohistological evidence for dendritic-like cells within human choroid plexus epithelium. NeuroReport 8: 1995–1998.

    Article  CAS  PubMed  Google Scholar 

  • Serot JM, Foliguet B, Bene MC, Faure GC (1998). Intraepithelial and stromal dendritic cells in human choroid plexus. Hum Pathol 29: 1174–1175.

    Article  CAS  PubMed  Google Scholar 

  • Shieh JT, Albright AV, Sharron M, Gartner S, Strizki J, Doms RW, Gonzalez-Scarano F (1998). Chemokine receptor utilization by human immunodeficiency virus type 1 isolates that replicate in microglia. J Virol 72: 4243–4249.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sozzani S, Luini W, Borsatti A, Polentarutti N, Zhou D, Piemonti L, D’Amico G, Power CA, Wells TN, Gobbi M, Allavena P, Mantovani A (1997). Receptor expression and responsiveness of human dendritic cells to a defined set of CC and CXC chemokines. J Immunol 159: 1993–2000.

    CAS  PubMed  Google Scholar 

  • 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: 1819–1838.

    CAS  PubMed  Google Scholar 

  • 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: 411–419.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Wesselingh SL, Griffin DE, McArthur JC, Johnson RT, Glass JD (1996). Localization of HIV-1 in human brain using polymerase chain reaction/in situ hybridization and immunohistochemistry. Ann Neurol 39: 705–711.

    Article  CAS  PubMed  Google Scholar 

  • Tenner-Racz K, von Stemm AM, Guhlk B, Schmitz J, Racz P (1994). Are follicular dendritic cells, macrophages and interdigitating cells of the lymphoid tissue productively infected by HIV? Res Virol 145: 177–182.

    Article  CAS  PubMed  Google Scholar 

  • Wiley CA, Schrier RD, Nelson JA, Lampert PW, Oldstone MB (1986). Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc Natl Acad Sci USA 83: 7089–7093.

    Article  CAS  PubMed  Google Scholar 

  • Wolburg K, Gerhardt H, Schulz M, Wolburg H, Engelhardt B (1999). Ultrastructural localization of adhesion molecules in the healthy and inflamed choroid plexus of the mouse. Cell Tissue Res 296: 259–269.

    Article  CAS  PubMed  Google Scholar 

  • Yang J-S, English RV, Ritchey JW, Davidson MG, Wasmoen T, Levy JK, Gebhard DH, Tompkins MB, Tompkins WAF (1996). Molecularly cloned feline immunodeficiency virus NCSUl JSY3 induces immunodeficiency in specific-pathogen-free cats. J Virol 70: 3011–3017.

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. B. Meeker.

Additional information

This work was supported by Public Health Service Grant NS33408 from the National Institute of Neurological Disorders and Stroke and the UNC Center for AIDS Research 9P30 AI50410.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bragg, D.C., Childers, T.A., Tompkins, M.B. et al. Infection of the choroid plexus by feline immunodeficiency virus. Journal of NeuroVirology 8, 211–224 (2002). https://doi.org/10.1080/13550280290049688

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1080/13550280290049688

Keywords

Navigation