Neurotoxicity Research

, 8:107

The role of monocytes and perivascular macrophages in HIV and SIV neuropathogenesis: Information from non-human primate models

Part II Experimental Models of Had

Abstract

Perivascular macrophages are located in the perivascular space of cerebral microvessels and thus uniquely situated at the intersection between the brain parenchyma and blood. Connections between the nervous and immune systems are mediated in part through these cells that are ideally located to sense perturbations in the periphery and turnover by cells entering the central nervous system (CNS) from the circulation. It has become clear that unique subsets of brain macrophages exist in normal and SIV- or HIV-infected brains, and perivascular macrophages and similar cells in the meninges and choroid plexus play a central role in lentiviral neuropathogenesis. Common to all these cell populations is their likely replacement within the CNS by monocytes. Studies of SIV-infected non-human primates and HIV-infected humans underscore the importance of virus-infected and activated monocytes, which traffic to the CNS from blood to become perivascular macrophages, potentially drive blood-brain barrier damage and cause neuronal injury. This review summarizes what we know about SIV- and HIV-induced neuropathogenesis focusing on brain perivascular macrophages and their precursors in blood that may mediate HIV infection and injury in the CNS.

Keywords

Perivascular macrophages Monocytes HIV SIV Blood-brain barrier CNS 

References

  1. Aguirre K and S Miller (2002) MHC class II-positive perivascular microglial cells mediate resistance toCryptococcus neoformans brain infection.Glia 39, 184–188.PubMedCrossRefGoogle Scholar
  2. Amirayan-Chevillard N, H Tissot-Dupont, C Capo, C Brunet and F Dignat-George (2000) Impact of highly active anti-retroviral therapy (HARRT) on cytokine production and monocyte subsets in HIV-infected patients.Clin. Exp. Immunol. 120, 107–112.PubMedCrossRefGoogle Scholar
  3. Ancuta P, R Rao, A Moses, A Mehle, SK Shaw, FW Luscinskas and D Gabuzda (2003) Fractalkine preferentially mediates arrest and migration of CD16+ monocytes.J. Exp. Med. 197, 1701–1707.PubMedCrossRefGoogle Scholar
  4. Ancuta P, A Moses and D Gabuzda (2004) Transendothelial migration of CD16+ monocytes in response to fractalkine under constitutive and inflammatory conditions.Immunobiology 209, 11–20.PubMedCrossRefGoogle Scholar
  5. Avison MJ, A Nath, R Greene-Avison, FA Schmitt, RA Bales, A Ethisham, RN Greenberg and JR Berger (2004a) Inflammatory changes and breakdown of microvascular integrity in early human immunodeficiency virus dementia.J. Neurovirol. 10, 223–232.PubMedCrossRefGoogle Scholar
  6. Avison MJ, A Nath, R Greene-Avison, FA Schmitt, RN Greenberg and JR Berger (2004b) Neuroimaging correlates of HIV-associated BBB compromise.J. Neuroimmunol. 157, 140–146.PubMedCrossRefGoogle Scholar
  7. Barrow AD, SC Burgess, K Howes and VK Nair (2003) Monocytosis is associated with the onset of leukocyte and viral infiltration of the brain in chickens infected with the very virulent Marek’s disease virus strain C12/130.Avian Pathol. 32, 183–191.PubMedCrossRefGoogle Scholar
  8. Becher B and J Antel (1996) Comparison of phenotypic and functional properties of immediatelyex vivo and cultured human adult microglia.Glia 18, 1–10.PubMedCrossRefGoogle Scholar
  9. Boche D, F Gray, L Chakrabarti, M Hurtrel, L Montagnier and B Hurtrel (1995) Low susceptibility of resident microglia to simian immunodeficiency virus replication during the early stages of infection.Neuropathol. Appl. Neurobiol. 21, 535–539.PubMedCrossRefGoogle Scholar
  10. Boven LA, J Middel, J Verhoef, CJA De Groot and HSLM Nottet (2000) Monocyte infiltration is highly associated with loss of the tight junction protein zonula occludens in HIV-1-associated dementia.Neuropathol. Appl. Neurobiol. 26, 356–360.PubMedCrossRefGoogle Scholar
  11. Buch S, Y Sui, R Potula, D Pinson, I Adany, Z Li, M Huang, S Li, N Dhillon, E Major and O Narayan (2004) Role of interleukin-4 and monocyte chemoattractant protein-1 in the neuropathogenesis of X4 simian human immunodeficiency virus infection in macaques.J. Neurovirol. 10 Suppl.1, 118–124.Google Scholar
  12. Budka H (1986) Multinucleated giant cells in brain: a hallmark of the acquired immune deficiency syndrome (AIDS).Acta Neuropathol. 69, 253–258.PubMedCrossRefGoogle Scholar
  13. Bukrinsky MI, H Nottet, H Schmidtmayerova, L Dubrovsky, CR Flanagan, ME Mullins, SA Lipton and HE Gendelman (1995) Regulation of nitric oxide synthase activity in human immunodeficiency virus type 1 (HIV-1)-infected monocytes: implications for HIV-associated neurological disease.J. Exp. Med. 181, 735–745.PubMedCrossRefGoogle Scholar
  14. Burudi EME, MCG Marcondes, DD Watry, M Zandonatti, MA Taffe and HS Fox (2002) Regulation of indoleamine 2,3-dioxygenase expression in simian immunodeficiency virusinfected monkey brains.J. Virol. 76, 12233–12241.PubMedCrossRefGoogle Scholar
  15. Chakrabarti L, M Hurtrel, MA Maire, R Vazeux, D Dormont, L Montagnier and B Hurtrel (1991) Early viral replication in the brain of SIV-infected rhesus monkeys.Am. J. Pathol. 139, 1273–1280.PubMedGoogle Scholar
  16. Dallasta LM, LA Pisarov, JE Esplen, JV Werley, AV Moses, JA Nelson and CL Achim (1999) Blood-brain barrier tight junction disruption in human immunodeficiency virus-1 encephalitis.Am. J. Pathol. 155, 1915–1927.PubMedGoogle Scholar
  17. Davis LE, BL Hjelle, VE Miller, DL Palmer, AL Llewellyn, TL Merlin, SA Young, RG Mills, W Wachsman and CA Wiley (1992) Early viral brain invasion in iatrogenic human immunodeficiency virus infection.Neurology 42, 1736–1739.PubMedGoogle Scholar
  18. Depboylu C, TA Reinhart, O Takikawa, Y Imai, H Maeda, H Mitsuya, D Rausch, LE Eiden and E Weihe (2004) Brain virus burden and indoleamine-2,3-dioxygenase expression during lentiviral infection of rhesus monkey are concomitantly lowered by 6-chloro-2’,3’-dideoxyguanosine.Eur. J. Neurosci. 19, 2997–3005.PubMedCrossRefGoogle Scholar
  19. Desrosiers RC, A Hansen-Moosa, K Mori, DP Bouvier, NW King, MD Daniel and DJ Ringler (1991) Macrophage-tropic variants of SIV are associated with specific AIDS-related lesions but are not essential for the development of AIDS.Am. J. Pathol. 139, 29–35.PubMedGoogle Scholar
  20. Dick AD, M Pell, BJ Brew, E Foulcher and JD Sedgwick (1997) Directex vivo flow cytometric analysis of human microglial cell CD4 expression: examination of central nervous system biopsy specimens from HIV-seropositive patients and patients with other neurological disease.AIDS 11, 1699–1708.PubMedCrossRefGoogle Scholar
  21. Dunne J, C Feighery and A Whelan (1996) Beta-2-microglobulin, neopterin and monocyte Fc gamma receptors in opportunistic infections of HIV-positive patients.Br. J. Biomed. Sci. 53, 263–269.PubMedGoogle Scholar
  22. Durrbaum-Landmann I, E Kaltenhauser, HD Flad and M Ernst (1994) HIV-1 envelope protein gp120 affects phenotype and function of monocytesin vitro. J. Leukoc. Biol.55, 545–551.PubMedGoogle Scholar
  23. Ellery P, S Sonza, J Mills and S Crowe (2003) Monocyte subsets and HIV reservoirs in patients on HAART.10th Conference on Retroviruses and Opportunistic Infections Abstr.468. Google Scholar
  24. Elmquist JK, CD Breder, JE Sherin, TE Scammell, WF Hickey, D Dewitt and CB Saper (1997) Intravenous lipopolysaccharide induces cyclooxygenase 2-like immunoreactivity in rat brain perivascular microglia and meningeal macrophages.J. Comp. Neurol. 381, 119–129.PubMedCrossRefGoogle Scholar
  25. Esiri MM and D Gay (1990) Immunological and neuropathological significance of the Virchow-Robin space.J. Neurol. Sci. 100, 3–8.PubMedCrossRefGoogle Scholar
  26. Evers S, D Nabavi, A Rahmann, C Heese, D Reichelt and IW Husstedt (2003) Ischaemic cerebrovascular events in HIV infection: a cohort study.Cerebrovasc. Dis. 15, 199–205.PubMedCrossRefGoogle Scholar
  27. Fabriek BO, ES Van Haastert, I Galea, MM Polfliet, ED Dopp, MM Van Den Heuvel, TK Van Den Berg, CJ De Groot, P Van Der Valk and CD Dijkstra (2005) CD163-positive perivascular macrophages in the human CNS express molecules for antigen recognition and presentation.Glia [Apr. 21, Epub ahead of print].Google Scholar
  28. Fiala M, QN Liu, J Sayre, V Pop, V Brahmandam, MC Graves and HV Vinters (2002) Cyclooxygenase-2-positive macrophages infiltrate the Alzheimer’s disease brain and damage the bloodbrain barrier.Eur. J. Clin. Invest. 32, 360–371.PubMedCrossRefGoogle Scholar
  29. Fischer-Smith T, S Croul, AE Sverstiuk, C Capini, D L’Heureux, EG Regulier, MW Richardson, S Amini, S Morgello, K Khalili and J Rappaport (2001) CNS invasion by CD14+/CD16+ peripheral blood-derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection.J. Neurovirol. 7, 528–541.PubMedCrossRefGoogle Scholar
  30. Ford AL, AL Goodsall, WF Hickey and JD Sedgwick (1995) Normal adult rat microglia seperated from other CNS macrophages by flow cytomteric sorting. Phenotypic differences defined and directex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared.J. Immunol. 154, 4309–4321.PubMedGoogle Scholar
  31. Gabuzda DH, DD Ho, S de la Monte, MS Hirsch, TR Rota and RA Sobel (1986) Immunohistochemical identification of HTLVIII antigen in brains of patients with AIDS.Ann. Neurol. 20, 289–295.PubMedCrossRefGoogle Scholar
  32. Galimi F, RG Summers, H van Praag, IM Verma and FH Gage (2005) A role for bone marrow-derived cells in the vasculature of noninjured CNS.Blood 105, 2400–2402.PubMedCrossRefGoogle Scholar
  33. Geissmann F, S Jung and DR Littman (2003) Blood monocytes consist of two principal subsets with distinct migratory properties.Immunity 19, 71–82.PubMedCrossRefGoogle Scholar
  34. Gendelman HE, O Narayan, S Kennedy-Stoskopf, PG Kennedy, Z Ghotbi, JE Clements, J Stanley and G Pezeshkpour (1986) Tropism of sheep lentiviruses for monocytes: susceptibility to infection and virus gene expression increase during maturation of monocytes to macrophages.J. Virol. 58, 67–74.PubMedGoogle Scholar
  35. Ghorpade A, R Persidskaia, R Suryadevara, M Che, XJ Liu, Y Persidsky and HE Gendelman (2001) Mononuclear phagocyte differentiation, activation, and viral infection regulate matrix metalloproteinase expression: implications for human immunodeficiency virus type 1-associated dementia.J. Virol. 75, 6572–6583.PubMedCrossRefGoogle Scholar
  36. Gray F, MC Lescs, C Keohane, F Paraire, B Marc, M Durigon and R Gherardi (1992) Early brain changes in HIV infection: neuropathological study of 11 HIV seropositive, non-AIDS cases.J. Neuropathol. Exp. Neurol. 51, 177–185.PubMedCrossRefGoogle Scholar
  37. Green DA, E Masliah, HV Vinters, P Beizai, DJ Moore and CL Achim (2005) Brain deposition of beta-amyloid is a common pathologic feature in HIV positive patients.AIDS 19, 407–411.PubMedCrossRefGoogle Scholar
  38. Hess DC, T Abe, WD Hill, AM Studdard, J Carothers, M Masuya, PA Fleming, CJ Drake and M Ogawa (2004) Hematopoietic origin of microglial and perivascular cells in brain.Exp. Neurol. 186, 134–144.PubMedCrossRefGoogle Scholar
  39. Hickey WF and H Kimura (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigenin vivo. Science239, 290–292.PubMedCrossRefGoogle Scholar
  40. Ho DD, TR Rota and MS Hirsch (1986) Infection of monocyte/ macrophages by human T lymphotropic virus type III.J. Clin. Invest. 77, 1712–1715.PubMedCrossRefGoogle Scholar
  41. Hofmann N, N Lachnit, M Streppel, B Witter, W Neiss, O Guntinas-Lichius and D Angelov (2002) Increased expression of ICAM-1, VCAM-1, MCP-1, and MIP-1alpha by spinal perivascular macrophages during experimental allergic encephalomyelitis in rats.BMC Immunology 3, 11.PubMedCrossRefGoogle Scholar
  42. Hughes ES, JE Bell and P Simmonds (1997) Investigation of the dynamics of the spread of human immunodeficiency virus to brain and other tissues by evolutionary analysis of sequences from the p17gag and env genes.J. Virol. 71, 1272–1280.PubMedGoogle Scholar
  43. Hurtrel B, L Chakrabarti, M Hurtrel and L Montagnier (1993) Target cells during early SIV encephalopathy.Res. Virol. 144, 41–46.PubMedCrossRefGoogle Scholar
  44. Hurwitz AA, JW Berman and WD Lyman (1994) The role of the blood-brain barrier in HIV infection of the central nervous system.Adv. Neuroimmunol. 4, 249–256.PubMedCrossRefGoogle Scholar
  45. Hutchings M and RO Weller (1986) Anatomical relationships of the pia mater to cerebral blood vessels in man.J. Neurosurg. 65, 316–325.PubMedGoogle Scholar
  46. Ichimura T, PA Fraser and H Cserr (1991) Distribution of extracellular tracers in the perivascular spaces of the rat brain.Brain Res. 545, 103–113.PubMedCrossRefGoogle Scholar
  47. Innocenti P, M Ottmann, P Morand, P Leclercq and JM Seigneurin (1992) HIV-1 in blood monocytes: frequency of detection of proviral DNA using PCR and comparison with the total CD4 count.AIDS Res. Hum. Retroviruses 8, 261–268.PubMedCrossRefGoogle Scholar
  48. Izycka-Swieszewska E, A Zoltowska, R Rzepko, M Gross and J Borowska-Lehman (2000) Vasculopathy and amyloid beta reactivity in brains of patients with acquired immune deficiency (AIDS).Folia Neuropathol. 38, 175–182.PubMedGoogle Scholar
  49. Jones M, K Olafson, MR Del Bigio, J Peeling and A Nath (1998) Intraventricular injection of human immunodeficiency virus type 1 (HIV-1) tat protein causes inflammation, gliosis, apoptosis, and ventricular enlargement.J. Neuropathol. Exp. Neurol. 57, 563–570.PubMedCrossRefGoogle Scholar
  50. Jones MV, JE Bell and A Nath (2000) Immunolocalization of HIV envelope gp120 in HIV encephalitis with dementia.AIDS 14, 2709–2713.PubMedCrossRefGoogle Scholar
  51. Kalebic T, L Masiero, M Onisto and S Garbisa (1994) HIV-1 modulates the expression of gelatinase A and B in monocytic cells.Biochem. Biophys. Res. Commun. 205, 1243–1249.PubMedCrossRefGoogle Scholar
  52. Kennedy DW and JL Abkowitz (1997) Kinetics of central nervous system microglial and macrophage engraftment: analysis using a transgenic bone marrow transplantation model.Blood 90, 986–993.PubMedGoogle Scholar
  53. Kim WK, S Corey, X Alvarez and K Williams (2003a) Monocyte/ macrophage traffic in HIV and SIV encephalitis.J. Leukoc. Biol. 74, 650–656.PubMedCrossRefGoogle Scholar
  54. Kim WK, E Ratai, MR Lentz, JB Greco, RF Schinazi, P Autissier, RA Fuller, JP Kim, J He, SV Westmoreland, M Piatak, JD Lifson, RG Gonzalez and KC Williams (2003b) Monocyte activation and infection with SIV neuropathogenesis.J. Neurovirol. 9 Suppl. 3, 119.Google Scholar
  55. Kim WK, X Alvarez and K Williams (2005) CD163: marker for perivascular macrophages and virus infected cells in human and monkey encephalitic brains.Keystone Symposia (Central Nervous System Inflammation: Mechanisms, Consequences and Therapeutic Strategies), Abstr.132. Google Scholar
  56. Kodama T, K Mori, T Kawahara, DJ Ringler and RC Desrosiers (1993) Analysis of simian immunodeficiency virus sequence variation in tissues of rhesus macaques with AIDS.J. Virol. 67, 6522–6534.PubMedGoogle Scholar
  57. Kusdra L, D McGuire and L Pulliam (2002) Changes in monocyte/ macrophage neurotoxicity in the era of HAART: implications for HIV-associated dementia.AIDS 16, 31–38.PubMedCrossRefGoogle Scholar
  58. Lackner AA, MO Smith, RJ Munn, DJ Martfeld, MB Gardner, PA Marx and S Dandekar (1991) Localization of simian immunodeficiency virus in the central nervous system of rhesus monkeys.Am. J. Pathol. 139, 609–621.PubMedGoogle Scholar
  59. Laman JD, M van Meurs, MM Schellekens, M de Boer, B Melchers, L Massacesi, H Lassmann, E Claassen and BA ‘t Hart (1998) Expression of accessory molecules and cytokines in acute EAE in marmoset monkeys (Callithrix jacchus).J. Neuroimmunol. 86, 30–45.PubMedCrossRefGoogle Scholar
  60. Lane JH, VG Sasseville, MO Smith, P Vogel, DR Pauley, MP Heyes and AA Lackner (1996) Neuroinvasion by simian immunodeficiency virus coincides with increased numbers of perivascular macrophages/microglia and intrathecal immune activation.J. Neurovirol. 2, 423–432.PubMedCrossRefGoogle Scholar
  61. Lassmann H, M Schmied, K Vass and WF Hickey (1993) Bone marrow derived elements and resident microglia in brain inflammation.Glia 7, 19–24.PubMedCrossRefGoogle Scholar
  62. Li Q, LE Eiden, W Cavert, TA Reinhart, DM Rausch, EA Murray, E Weihe and AT Haase (1999) Increased expression of nitric oxide synthase and dendritic injury in simian immunodeficiency virus encephalitis.J. Hum. Virol. 2, 139–145.PubMedGoogle Scholar
  63. Liu Y, XP Tang, JC McArthur, J Scott and S Gartner (2000) Analysis of human immunodeficiency virus type 1 gp160 sequences from a patient with HIV dementia: evidence for monocyte trafficking into brain.J. Neurovirol. 6 Suppl. 1, S70-S81.PubMedGoogle Scholar
  64. Locher C, G Vanham, L Kestens, M Kruger, JL Ceuppens, J Vingerhoets and P Gigase (1994) Expression patterns of Fc gamma receptors, HLA-DR and selected adhesion molecules on monocytes from normal and HIV-infected individuals.Clin. Exp. Immunol. 98, 115–122.PubMedGoogle Scholar
  65. Luabeya M-K, LM Dallasta, CL Achim, CD Pauza and RL Hamilton (2000) Blood-brain barrier disruption in simian immunodeficiency virus encephalitis.Neuropathol. Appl. Neurobiol. 26, 454–462.PubMedCrossRefGoogle Scholar
  66. MacLean AG, TA Rasmussen, D Bieniemy and AA Lackner (2004a) Activation of the blood-brain barrier by SIV (simian immunodeficiency virus) requires cell-associated virus and is not restricted to endothelial cell activation.Biochem. Soc. Trans. 32, 750–752.CrossRefGoogle Scholar
  67. MacLean AG, TA Rasmussen, DN Bieniemy, X Alvarez and AA Lackner (2004b) SIV-induced activation of the blood-brain barrier requires cell-associated virus and is not restricted to endothelial cell activation.J. Med. Primatol. 33, 236–242.CrossRefGoogle Scholar
  68. Mankowski JL, SE Queen, LM Kirstein, JP Spelman, J Laterra, IA Simpson, RJ Adams, JE Clements and MC Zink (1999) Alterations in blood-brain barrier glucose transport in SIVinfected macaques.J. Neurovirol. 5, 695–702.PubMedCrossRefGoogle Scholar
  69. McElrath MJ, RM Steinman and ZA Cohn (1991) Latent HIV-1 infection in enriched populations of blood monocytes and T cells from seropositive patients.J. Clin. Invest. 87, 27–30.PubMedCrossRefGoogle Scholar
  70. Mesquita R, E Castanos-Velez, P Biberfeld, RM Troian and MM de Siqueira (1998) Measles virus antigen in macrophage/microglial cells and astrocytes of subacute sclerosing panencephalitis.APMIS 106, 553–561.PubMedGoogle Scholar
  71. Mizusawa H, A Hirano, JF Llena and M Shintaku (1988) Cerebrovascular lesions in acquired immune deficiency syndrome (AIDS).Acta Neuropathol. (Berl.) 76, 451–457.CrossRefGoogle Scholar
  72. Mordelet E, K Kissa, A Cressant, F Gray, S Ozden, C Vidal, P Charneau and S Granon (2004) Histopathological and cognitive defects induced by Nef in the brain.FASEB J. 18, 1851–1861.PubMedCrossRefGoogle Scholar
  73. Nockher WA, L Bergmann and JE Scherberich (1994) Increased soluble CD14 serum levels and altered CD14 expression of peripheral blood monocytes in HIV-infected patients.Clin. Exp. Immunol. 98, 369–374.PubMedGoogle Scholar
  74. Peluso R, A Haase, L Stowring, M Edwards and P Ventura (1985) A Trojan Horse mechanism for the spread of visna virus in monocytes.Virology 147, 231–236.PubMedCrossRefGoogle Scholar
  75. Persidsky Y, J Zheng, D Miller and HE Gendelman (2000) Mononuclear phagocytes mediate blood-brain barrier compromise and neuronal injury during HIV-1-associated dementia.J. Leukoc. Biol. 68, 413–422.PubMedGoogle Scholar
  76. Petito CK and KS Cash (1992) Blood-brain barrier abnormalities in the acquired immunodeficiency syndrome: immunohistochemical localization of serum proteins inpostmortem brain.Ann. Neurol. 32, 658–666.PubMedCrossRefGoogle Scholar
  77. Polfliet MM, PJ Zwijnenburg, AM van Furth, T van der Poll, EA Dopp, C Renardel de Lavalette, EM van Kesteren-Hendrikx, N van Rooijen, CD Dijkstra and TK van den Berg (2001) Meningeal and perivascular macrophages of the central nervous system play a protective role during bacterial meningitis.J. Immunol. 167, 4644–4650.PubMedGoogle Scholar
  78. Polfliet MM, F van de Veerdonk, EA Dopp, EM van Kesteren-Hendrikx, N van Rooijen, CD Dijkstra and TK van den Berg (2002) The role of perivascular and meningeal macrophages in experimental allergic encephalomyelitis.J. Neuroimmunol. 122, 1–8.PubMedCrossRefGoogle Scholar
  79. Power C, P-A Kong, TO Crawford, S Wesselingh, JD Glass, JC McArthur and BD Trapp (1993) Cerebral white matter changes in acquired immunodeficiency syndrome dementia: alterations of the blood brain-barrier.Ann. Neurol. 34, 339–350.PubMedCrossRefGoogle Scholar
  80. Pu H, J Tian, G Flora, Y Woo Lee, A Nath, B Hennig and M Toborek (2003) HIV-1 tat protein upregulates inflammatory mediators and induces monocyte invasion into the brain.Mol. Cell. Neurosci. 24, 224–237.PubMedCrossRefGoogle Scholar
  81. Pulliam L, R Gascon, M Stubblebine, D McGuire andMS McGrath (1997) Unique monocyte subset in patients with AIDS dementia.Lancet 349, 692–695.PubMedCrossRefGoogle Scholar
  82. Pumarola-Sune T, BA Navia, C Cordon-Cardo, ES Cho and RW Price (1987) HIV antigen in the brains of patients with the AIDS dementia complex.Ann. Neurol. 21, 490–496.PubMedCrossRefGoogle Scholar
  83. Ransohoff RM, P Kivisakk and G Kidd (2003) Three or more routes for leukocyte migration into the central nervous system.Nat. Rev. Immunol. 3, 569–581.PubMedCrossRefGoogle Scholar
  84. Reuter JD, DL Gomez, JH Wilson and AN van den Pol (2004) Systemic immune deficiency necessary for cytomegalovirus invasion of the mature brain.J. Virol. 78, 1473–1487.PubMedCrossRefGoogle Scholar
  85. Rhodes RH (1991) Evidence of serum-protein leakage across the blood brain barrier in the acquired immunodeficiency syndrome.J. Neuropath. Exp. Neurol. 50, 171–183.PubMedCrossRefGoogle Scholar
  86. Rosenberg GA, N Sullivan and MM Esiri (2001) White matter damage is associated with matrix metalloproteinases in vascular dementia.Stroke 32, 1162–1168.PubMedGoogle Scholar
  87. Rostasy K, L Monti, C Yiannoutsos, M Kneissl, J Bell, TL Kemper, JC Hedreen and BA Navia (1999) Human immunodeficiency virus infection, inducible nitric oxide synthase expression, and microglial activation: pathogenetic relationship to the acquired immunodeficiency syndrome dementia complex.Ann. Neurol. 46, 207–216.PubMedCrossRefGoogle Scholar
  88. Salemi M, S Lamers, S Yu, T de Oliveira, W Fitch and M McGrath (2005a) Phylodynamic Analysis of HIV-1 in the Brain. 12th Conference on Retroviruses and Opportunistic Infections Abstr.375. Google Scholar
  89. Salemi M, SL Lamers, S Yu, T de Oliveira, WM Fitchand MS McGrath (2005b) HIV-1 phylodynamic analysis in distinct brain compartments provides a model for the neuropathogenesis of AIDS.J. Virol. 79, 11343–11352.CrossRefGoogle Scholar
  90. Scaravilli F, SE Daniel, N Harcourt-Webster and RJ Guiloff (1989) Chronic basal meningitis and vasculitis in acquired immunodeficiency syndrome. A possible role for human immunodeficiency virus.Arch. Pathol. Lab. Med. 113, 192–195.PubMedGoogle Scholar
  91. Schiltz JC and PE Sawchenko (2002) Distinct brain vascular cell types manifest inducible cyclooxygenase expression as a function of the strength and nature of immune insults.J. Neurosci. 22, 5606–5618.PubMedGoogle Scholar
  92. Schindelmeiser J and F Gullotta (1991) HIV-p24-antigen-bearing macrophages are only present in brains of HIV-seropositive patients with AIDS-encephalopathy.Clin. Neuropathol. 10, 109–111.PubMedGoogle Scholar
  93. Shiramizu B, S Gartner, A Williams, C Shikuma, S Ratto-Kim, M Watters, J Aguon and V Valcour (2005) Circulating proviral HIV DNA and HIV-associated dementia.AIDS 19, 45–52.PubMedCrossRefGoogle Scholar
  94. Simon MA, LV Chalifoux and DJ Ringler (1992) Pathologic features of SIV-induced disease and the association of macrophage infection with disease evolution.AIDS Res. Hum. Retroviruses 8, 327–337.PubMedGoogle Scholar
  95. Smith MO, MP Heyes and AA Lackner (1995) Early intrathecal events in rhesus macaques (Macaca mulatta) infected with pathogenic or nonpathogenic molecular clones of simian immunodeficiency virus.Lab. Invest. 72, 547–558.PubMedGoogle Scholar
  96. Smith MS, Y Niu, Z Li, I Adany, DM Pinson, ZQ Liu, T Berry D Sheffer, F Jia and O Narayan (2002) Systemic infection and limited replication of SHIV vaccine virus in brains of macaques inoculated intracerebrally with infectious viral DNA.Virology 301, 130–135.PubMedCrossRefGoogle Scholar
  97. Smith TW, U DeGirolami, D Henin, F Bolgert and J-J Hauw (1990) Human immunodeficiency virus (HIV) leukoencephalopathy and the microcirculation.J. Neuropathol. Exp. Neurol. 49, 357–370.PubMedCrossRefGoogle Scholar
  98. Sonza S, HP Mutimer, R Oelrichs, D Jardine, K Harvey, A Dunne, DF Purcell, C Birch and SM Crowe (2001) Monocytes harbour replication-competent, non-latent HIV in patients on highly active antiretroviral therapy.AIDS 15, 17–22.PubMedCrossRefGoogle Scholar
  99. Stephens EB, DK Singh, ME Kohler, M Jackson, E Pacyniak and NE Berman (2003) The primary phase of infection by pathogenic simian-human immunodeficiency virus results in disruption of the blood-brain barrier.AIDS Res. Hum. Retroviruses 19, 837–846.PubMedCrossRefGoogle Scholar
  100. Streit WJ and MB Graeber (1993) Heterogeneity of microglial and perivascular cell populations: insights gained from the facial nucleus paradigm.Glia 7, 68–74.PubMedCrossRefGoogle Scholar
  101. Teo I, C Veryard, H Barnes, SF An, M Jones, PL Lantos, P Luthert and S Shaunak (1997) Circular forms of unintegrated human immunodeficiency virus type 1 DNA and high levels of viral protein expression: association with dementia and multinucleated giant cells in the brains of patients with AIDS.J. Virol. 71, 2928–2933.PubMedGoogle Scholar
  102. Thieblemont N, L Weiss, HM Sadeghi, C Estcourt and N Haeffner-Cavaillon (1995) CD14lowCD16high: a cytokine-producing monocyte subset which expands during human immunodeficiency virus infection.Eur. J. Immunol. 25, 3418–3424.PubMedCrossRefGoogle Scholar
  103. Tracey I, LM Hamberg, AR Guimaraes, G Hunter, I Chang, BA Navia and RG Gonzalez (1998) Increased cerebral blood volume in HIV-positive patients detected by functional MRI.Neurology 50, 1821–1826.PubMedGoogle Scholar
  104. Vallieres L and PE Sawchenko (2003) Bone marrow-derived cells that populate the adult mouse brain preserve their hematopoietic identity.J. Neurosci. 23, 5197–5207.PubMedGoogle Scholar
  105. Vehmas A, J Lieu, CA Pardo, JC McArthur and S Gartner (2004) Amyloid precursor protein expression in circulating monocytes and brain macrophages from patients with HIV-associated cognitive impairment.J. Neuroimmunol. 157, 99–110.PubMedCrossRefGoogle Scholar
  106. Venkateshan CN, R Narayanan, MG Espey, JR Moffett, DC Gajdusek, CJ Gibbs Jr and MAA Namboodiri (1996) Immunocytochemical localization of the endogenous neuroexcitotoxin quinolinate in human peripheral blood monocytes/macrophages and the effect of human T-cell lymphotropic virus type I infection.Proc. Natl. Acad. Sci. USA 93, 1636–1641.PubMedCrossRefGoogle Scholar
  107. Walker WS (1999) Separate precursor cells for macrophages and microglia in mouse brain: immunophenotypic and immunoregulatory properties of the progeny.J. Neuroimmunol. 94, 127–133.PubMedCrossRefGoogle Scholar
  108. Wang TH, YK Donaldson, RP Brettle, JE Bell and P Simmonds (2001) Identification of shared populations of human immunodeficiency virus type 1 infecting microglia and tissue macrophages outside the central nervous system.J. Virol. 75, 11686–11699.PubMedCrossRefGoogle Scholar
  109. Ward JM, TJ O’Leary, GB Baskin, R Benveniste, CA Harris, PL Nara and RH Rhodes (1987) Immunohistochemical localization of human and simian immunodeficiency viral antigens in fixed tissue sections.Am. J. Pathol. 127, 199–205.PubMedGoogle Scholar
  110. Weis S, H Haug and H Budka (1996) Vascular changes in the cerebral cortex in HIV-1 infection: I. A morphometric investigation by light and electron microscopy.Clin. Neuropathol. 15, 361–366.PubMedGoogle Scholar
  111. Williams AE and WF Blakemore (1990) Monocyte-mediated entry of pathogens into the central nervous system.Neuropathol. Appl. Neurobiol. 16, 377–392.PubMedCrossRefGoogle Scholar
  112. Williams KC, S Corey, SV Westmoreland, D Pauley, H Knight, C deBakker, X Alvarez and AA Lackner (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, 905–915.PubMedCrossRefGoogle Scholar
  113. Williams K, S Westmoreland, J Greco, E Ratai, M Lentz, WK Kim, RA Fuller, JP Kim, P Autissier, PK Sehgal, RF Schinazi, N Bischofberger, M Piatak Jr, JD Lifson, E Masliah and RG González (2005) Magnetic resonance spectroscopy reveals a role of activated monocytes contributing to neuronal injury in simian immunodeficiency virus neuroAIDS.J. Clin. Invest. 115, 2534–2545.PubMedCrossRefGoogle Scholar
  114. Zembala M, S Bach, A Szczepanek, G Mancino and V Colizzi (1997) Phenotypic changes of monocytes induced by HIV-1 gp120 molecule and its fragments.Immunobiology 197, 110–121.PubMedGoogle Scholar
  115. Zhu T, D Muthui, S Holte, D Nickle, F Feng, S Brodie, Y Hwangbo, JI Mullins and L Corey (2002) Evidence for human immunodeficiency virus type 1 replicationin vivo in CD14+ monocytes and its potential role as a source of virus in patients on highly active antiretroviral therapy.J. Virol. 76, 707–716.PubMedCrossRefGoogle Scholar
  116. Ziegler-Heitbrock HW (2000) Definition of human blood monocytes.J. Leukoc. Biol. 67, 603–606.PubMedGoogle Scholar
  117. Ziegler-Heitbrock HW and RJ Ulevitch (1993) CD14: cell surface receptor and differentiation marker.Immunol. Today 14, 121–125.PubMedCrossRefGoogle Scholar
  118. Ziegler-Heitbrock HW, M Strobel, G Fingerle, T Schlunck, A Pforte, M Blumenstein and JG Haas (1991) Small (CD14+/CD16+) monocytes and regular monocytes in human blood.Pathobiology 59, 127–130.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Woong-Ki Kim
    • 1
  • Xavier Alvarez
    • 2
  • Kenneth Williams
    • 1
  1. 1.Division of Viral Pathogenesis,Beth Israel Deaconess Medical CenterHarvard Medical SchoolBostonUSA
  2. 2.Division of Comparative Pathology, Tulane National Primate Research CenterTulane UniversityCovingtonUSA

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