Neuropathologic and neuroinflammatory activities of HIV-1-infected human astrocytes in murine brain

GLIA

Volumn 54, Issue 2, 2006, Pages 81-93

  Dou, Huanyu ^a,b   Morehead, Justin ^a,b   Bradley, Jennifer ^a,b   Gorantla, Santhi ^a,b   Ellison, Brent ^a,b   Kingsley, Jeff ^a,b   Smith, Lynette M ^a   Chao, Wei ^c   Bentsman, Galina ^c   Volsky, David J ^c   Gendelman, Howard E ^a,b,d  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c NewYork Presbyterian Hospital   (United States)

^d NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Astrocytes; HIV 1 associated dementia; Inflammatory; Macrophages; Neurotoxicity; Severe combined immunodeficient mice

Indexed keywords

CD11B ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2;

ARTICLE; ASTROCYTE; BASAL GANGLION; CENTRAL NERVOUS SYSTEM INFECTION; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE DEFICIENCY; IMMUNOHISTOCHEMISTRY; MACROPHAGE; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; VESICULAR STOMATITIS VIRUS; VIRUS INFECTION;

ANIMALS; ASTROCYTES; BRAIN; CELLS, CULTURED; FETUS; HIV INFECTIONS; HIV-1; HUMANS; MALE; MICE; MICE, INBRED ICR; MICE, SCID;

EID: 33746041821     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20358     Document Type: Article

References (83)

1. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol 59:284-291.
2. Anderson ER, Boyle J, Zink WE, Persidsky Y, Gendelman HE, Xiong H. 2003. Hippocampal synaptic dysfunction in a murine model of human immunodeficiency virus type 1 encephalitis. Neuroscience 118:359-369.
3. Araque A, Parpura V, Sanzgiri RP, Haydon PG. 1998. Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur J Neurosci 10:2129-2142.
4. Bartz SR, Rogel ME, Emerman M. 1996. Human immunodeficiency virus type 1 cell cycle control: Vpr is cytostatic and mediates G2 accumulation by a mechanism which differs from DNA damage checkpoint control. J Virol 70:2324-2331.
5. Bencheikh M, Bentsman G, Sarkissian N, Canki M, Volsky DJ. 1999. Replication of different clones of human immunodeficiency virus type 1 in primary fetal human astrocytes: Enhancement of viral gene expression by Nef. J Neurovirol 5:115-124.
6. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A. 2004. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7:613-620.
7. Brack-Werner R. 1999. Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. AIDS 13:1-22.
8. Canki M, Thai JN, Chao W, Ghorpade A, Potash MJ, Volsky DJ. 2001. Highly productive infection with pseudotyped human immunodeficiency virus type 1 (HIV-1) indicates no intracellular restrictions to HIV-1 replication in primary human astrocytes. J Virol 75:7925-7933.
9. Collins KL, Chen BK, Kalams SA, Walker BD, Baltimore D. 1998. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391:397-401.
10. Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, Power C, Gallo RC, Major EO. 1998. Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc Natl Acad Sci USA 95:3117-3121.
11. Conant K, Tornatore C, Atwood W, Meyers K, Traub R, Major EO. 1994. In vivo and in vitro infection of the astrocyte by HIV-1. Adv Neuroimmunol 4:287-289.
12. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
13. Deshpande M, Zheng J, Borgmann K, Persidsky R, Wu L, Schellpeper C, Ghorpade A. 2005. Role of activated astrocytes in neuronal damage: Potential links to HIV-1-associated dementia. Neurotox Res 7:183-192.
14. Dewhurst S, Bresser J, Stevenson M, Sakai K, Evinger-Hodges MJ, Volsky DJ. 1987a. Susceptibility of human glial cells to infection with human immunodeficiency virus (HIV). FEBS Lett 213:138-143.
15. Dewhurst S, Sakai K, Bresser J, Stevenson M, Evinger-Hodges MJ, Volsky DJ. 1987b. Persistent productive infection of human glial cells by human immunodeficiency virus (HIV) and by infectious molecular clones of HIV. J Virol 61:3774-3782.
16. Di Rienzo AM, Aloisi F, Santarcangelo AC, Palladino C, Olivetta E, Genovese D, Verani P, Levi G. 1998. Virological and molecular parameters of HIV-1 infection of human embryonic astrocytes. Arch Virol 143:1599-1615.
17. 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 23:9162-9170.
18. Dou H, Ellison B, Bradley J, Kasiyanov A, Poluektova LY, Xiong H, Maggirwar S, Dewhurst S, Gelbard HA, Gendelman HE. 2005. Neuroprotective mechanisms of lithium in murine human immunodeficiency virus-1 encephalitis. J Neurosci 25:8375-8385.
19. Dreyer EB, Kaiser PK, Offermann JT, Lipton SA. 1990. HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists. Science 248:364-367.
20. Epstein LG. 1998. HIV neuropathogenesis and therapeutic strategies. Acta Paediatr Jpn 40:107-111.
21. Fischer-Smith T, Rappaport J. 2005. Evolving paradigms in the pathogenesis of HIV-1-associated dementia. Expert Rev Mol Med 7:1-26.
22. Galey D, Becker K, Haughey N, Kalehua A, Taub D, Woodward J, Mattson MP, Nath A. 2003. Differential transcriptional regulation by human immunodeficiency virus type 1 and gp120 in human astrocytes. J Neurovirol 9:358-371.
23. Gartner S, Markovits P, Markovitz DM, Betts RF, Popovic M. 1986. Virus isolation from and identification of HTLV-III/LAV-producing cells in brain tissue from a patient with AIDS. JAMA 256:2365-2371.
24. Ge S, Pachter JS. 2004. Caveolin-1 knockdown by small interfering RNA suppresses responses to the chemokine monocyte chemoattractant protein-1 by human astrocytes. J Biol Chem 279:6688-6695.
25. Gendelman HE, Diesing S, Gelbard H, Swindells S. 2003. The neuropathogenesis of HIV-1 infection. In: Wormser GP, editor. AIDS and other manifestations of HIV infection. Amsterdam: Elsevier.
26. Gendelman HE, Lipton SA, Tardieu M, Bukrinsky MI, Nottet HS. 1994. The neuropathogenesis of HIV-1 infection. J Leukoc Biol 56:389-398.
27. Gendelman HE, Persidsky Y, Ghorpade A, Limoges J, Stins M, Fiala M, Morrisett R. 1997. The neuropathogenesis of the AIDS dementia complex. AIDS 11 (Suppl A):S35-S45.
28. Gendelman HE, Orenstein J, Martin MA, Ferrua C, Mitra R, Phipps T, Wahl LA, Lane HC, Fauci AS, Burke D, Skillman D, Meltzer MS. 1988. Efficient isolation and propagation of human immunodeficiency virus on recombinant colony stimulating factor-1-treated monocytes. J Exp Med 167:1428-1441.
29. Ghorpade A, Holter S, Borgmann K, Persidsky R, Wu L. 2003. HIV-1 and IL-1β regulate Fas ligand expression in human astrocytes through the NF-κ B pathway. J Neuroimmunol 141:141-149.
30. Ghorpade A, Nukuna A, Che M, Haggerty S, Persidsky Y, Carter E, Carhart L, Shafer L, Gendelman HE. 1998. Human immunodeficiency virus neurotropism: An analysis of viral replication and cytopathicity for divergent strains in monocytes and microglia. J Virol 72:3340-3350.
31. Glass JD, Fedor H, Wesselingh SL, McArthur JC. 1995. Immunocytochemical quantitation of human immunodeficiency virus in the brain: Correlations with dementia. Ann Neurol 38:755-762.
32. Gorry P, Purcell D, Howard J, McPhee D. 1998. Restricted HIV-1 infection of human astrocytes: Potential role of nef in the regulation of virus replication. J Neurovirol 4:377-386.
33. Gorry PR, Ong C, Thorpe J, Bannwarth S, Thompson KA, Gatignol A, Vesselingh SL, Purcell DF. 2003. Astrocyte infection by HIV-1: Mechanisms of restricted virus replication, and role in the pathogenesis of HIV-1-associated dementia. Curr HIV Res 1:463-473.
34. Gray CW, Patel AJ. 1995. Neurodegeneration mediated by glutamate and β-amyloid peptide: A comparison and possible interaction. Brain Res 691:169-179.
35. Gray F, Scaravilli F, Everall I, Chretien F, An S, Boche D, Adle-Biassette H, Wingertsmann L, Durigon M, Hurtrel B, Chiodi F, Bell J, Lantos P. 1996. Neuropathology of early HIV-1 infection. Brain Pathol 6:1-15.
36. Hao HN, Lyman WD. 1999. HIV infection of fetal human astrocytes: The potential role of a receptor-mediated endocytic pathway. Brain Res 823:24-32.
37. He J, deCastro CM, Vandenbark GR, Busciglio J, Gabuzda D. 1997. Astrocyte apoptosis induced by HIV-1 transactivation of the c-kit protooncogene. Proc Natl Acad Sci USA 94:3954-3959.
38. Heinzinger N, Baca-Regen L, Stevenson M, Gendelman HE. 1995. Efficient synthesis of viral nucleic acids following monocyte infection by HIV-1. Virology 206:731-735.
39. Jiang ZG, Piggee C, Heyes MP, Murphy C, Quearry B, Bauer M, Zheng J, Gendelman HE, Markey SP. 2001. Glutamate is a mediator of neurotoxicity in secretions of activated HIV-1-infected macrophages. J Neuroimmunol 117:97-107.
40. Kang DC, Su ZZ, Sarkar D, Emdad L, Volsky DJ, Fisher PB. 2005. Cloning and characterization of HIV-1-inducible astrocyte elevated gene-1, AEG-1. Gene 353:8-15.
41. Kaul M, Garden GA, Lipton SA. 2001. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988-994.
42. Kim SY, Li J, Bentsman G, Brooks AI, Volsky DJ. 2004. Microarray analysis of changes in cellular gene expression induced by productive infection of primary human astrocytes: Implications for HAD. J Neuroimmunol 157:17-26.
43. 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 233:1089-1093.
44. Koller H, Schaal H, Rosenbaum C, Czardybon M, Von Giesen HJ, Muller HW, Arendt G. 2002. Functional CXCR4 receptor development parallels sensitivity to HIV-1 gp120 in cultured rat astroglial cells but not in cultured rat cortical neurons. J Neurovirol 8:411-419.
45. Krebs FC, Ross H, McAllister J, Wigdahl B. 2000. HIV-1-associated central nervous system dysfunction. Adv Pharmacol 49:315-385.
46. Lawrence DM, Major EO. 2002. HIV-1 and the brain: Connections between HIV-1-associated dementia, neuropathology and neuroimmunology. Microbes Infect 4:301-308.
47. Lee C, Liu QH, Tomkowicz B, Yi Y, Freedman BD, Collman RG. 2003. Macrophage activation through CCR5- and CXCR4-mediated gp120-elicited signaling pathways. J Leukoc Biol 74:676-682.
48. Lee SJ, Zhou T, Choi C, Wang Z, Benveniste EN. 2000. Differential regulation and function of Fas expression on glial cells. J Immunol 164:1277-1285.
49. Limoges J, Persidsky Y, Poluektova L, Rasmussen J, Ratanasuwan W, Zelivyanskaya M, McClernon DR, Lanier ER, Gendelman HE. 2000. Evaluation of antiretroviral drug efficacy for HIV-1 encephalitis in SCID mice. Neurology 54:379-389.
50. Ma M, Geiger JD, Nath A. 1994. Characterization of a novel binding site for the human immunodeficiency virus type 1 envelope protein gp120 on human fetal astrocytes. J Virol 68:6824-6828.
51. Masliah E, Ge N, Mucke L. 1996. Pathogenesis of HIV-1 associated neurodegeneration. Crit Rev Neurobiol 10:57-67.
52. Messam CA, Major EO. 2000. Stages of restricted HIV-1 infection in astrocyte cultures derived from human fetal brain tissue. J Neurovirol 6 (Suppl 1):S90-S94.
53. Nath A, Geiger J. 1998. Neurobiological aspects of human immunodeficiency virus infection: Neurotoxic mechanisms. Prog Neurobiol 54:19-33.
54. Navia BA, Jordan BD, Price RW. 1986. The AIDS dementia complex. I. Clinical features. Ann Neurol 19:517-524.
55. Nuovo GJ, Becker J, Burk MW, Margiotta M, Fuhrer J, Steigbigel RT. 1994. In situ detection of PCR-amplified HIV-1 nucleic acids in lymph nodes and peripheral blood in patients with asymptomatic HIV-1 infection and advanced-stage AIDS. J Acquir Immune Defic Syndr 7:916-923.
56. Oliet SH, Piet R, Poulain DA. 2001. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292:923-926.
57. Ong CL, Thorpe JC, Gorry PR, Bannwarth S, Jaworowski A, Howard JL, Chung S, Campbell S, Christensen HS, Clerzius G, et al. 2005. Low TRBP levels support an innate human immunodeficiency virus type 1 resistance in astrocytes by enhancing the PKR antiviral response. J Virol 79:12763-12772.
58. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG. 1994. Glutamate-mediated astrocyte-neuron signalling. Nature 369:744-774.
59. Patel AJ, Wickenden C, Jen A, de Silva HA. 1996. Glial cell derived neurotrophic factors and Alzheimer's disease. Neurodegeneration 5:489-496.
60. Persidsky Y, Gendelman HE. 2002. Murine models for human immunodeficiency virus type 1-associated dementia: The development of new treatment testing paradigms. J Neurovirol 8 (Suppl 2):49-52.
61. Persidsky Y, Limoges J, McComb R, Bock P, Baldwin T, Tyor W, Patil A, Nottet HS, Epstein L, Gelbard H, et al. 1996. Human immunodeficiency virus encephalitis in SCID mice. Am J Pathol 149:1027-1053.
62. Persidsky Y, Nottet HS, Sasseville VG, Epstein LG, Gendelman HE. 1995. The development of animal model systems for HIV-1 encephalitis and its associated dementia. J Neurovirol 1:229-243.
63. Poluektova LY, Munn DH, Persidsky Y, Gendelman HE. 2002. Generation of cytotoxic T cells against virus-infected human brain macrophages in a murine model of HIV-1 encephalitis. J Immunol 168:3941-3949.
64. Potash MJ, Chao W, Bentsman G, Paris N, Saini M, Nitkiewicz J, Belem P, Sharer L, Brooks AI, Volsky DJ. 2005. A mouse model for study of systemic HIV-1 infection, antiviral immune responses, and neuroinvasiveness. Proc Natl Acad Sci USA 102:3760-3765.
65. Power C, Gill MJ, Johnson RT. 2002. Progress in clinical neurosciences: The neuropathogenesis of HIV infection: Host-virus interaction and the impact of therapy. Can J Neurol Sci 29:19-32.
66. Romero IA, Teixeira A, Strosberg AD, Cazaubon S, Couraud PO. 1998. The HIV-1 nef protein inhibits extracellular signal-regulated kinase-dependent DNA synthesis in a human astrocytic cell line. J Neurochem 70:778-785.
67. Rutka JT, Murakami M, Dirks PB, Hubbard SL, Becker LE, Fukuyama K, Jung S, Tsugu A, Matsuzawa K. 1997. Role of glial filaments in cells and tumors of glial origin: A review. J Neurosurg 87:420-430.
68. Saito Y, Sharer LR, Epstein LG, Michaels J, Mintz M, Louder M, Golding K, Cvetkovich TA, Blumberg BM. 1994. Over expression of nef as a marker for restricted HIV-1 infection of astrocytes in postmortem pediatric central nervous tissues. Neurology 44(3 Part 1):474-481.
69. Schwartz JP, Nishiyama N. 1994. Neurotrophic factor gene expression in astrocytes during development and following injury. Brain Res Bull 35:403-407.
70. Seth P, Major EO. 2005. Human brain derived cell culture models of HIV-1 infection. Neurotox Res 8:83-90.
71. Smith DG, Guillemin GJ, Pemberton L, Kerr S, Nath A, Smythe GA, Brew BJ. 2001. Quinolinic acid is produced by macrophages stimulated by platelet activating factor, Nef and Tat. J Neurovirol 7:56-60.
72. Stitz J, Muhlebach MD, Blomer U, Scherr M, Selbert M, Wehner P, Steidl S, Schmitt I, Konig R, Schweizer M, et al. 2001. A novel lentivirus vector derived from apathogenic simian immunodeficiency virus. Virology 291:191-197.
73. Struzynska L, Bubko I, Walski M, Rafalowska U. 2001. Astroglial reaction during the early phase of acute lead toxicity in the adult rat brain. Toxicology 165:121-131.
74. Su ZZ, Kang DC, Chen Y, Pekarskaya O, Chao W, Volsky DJ, Fisher PB. 2002. Identification and cloning of human astrocyte genes displaying elevated expression after infection with HIV-1 or exposure to HIV-1 envelope glycoprotein by rapid subtraction hybridization, RaSH. Oncogene 21:3592-3602.
75. Su ZZ, Kang DC, Chen Y, Pekarskaya O, Chao W, Volsky DJ, Fisher PB. 2003. Identification of gene products suppressed by human immunodeficiency virus type 1 infection or gp120 exposure of primary human astrocytes by rapid subtraction hybridization. J Neurovirol 9:372-389.
76. 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 immunocytochemistry. Ann Neurol 39:705-711.
77. Tornatore C, Chandra R, Berger JR, Major EO. 1994. HIV-1 infection of subcortical astrocytes in the pediatric central nervous system. Neurology 44(3 Part 1):481-487.
78. Wang Z, Pekarskaya O, Bencheikh M, Chao W, Gelbard HA, Ghorpade A, Rothstein JD, Volsky DJ. 2003. Reduced expression of glutamate transporter EAAT2 and impaired glutamate transport in human primary astrocytes exposed to HIV-1 or gp120. Virology 312:60-73.
79. Wang Z, Trillo-Pazos G, Kim SY, Canki M, Morgello S, Sharer LR, Gelbard HA, Su ZZ, Kang DC, Brooks AI, et al. 2004. Effects of human immunodeficiency virus type 1 on astrocyte gene expression and function: Potential role in neuropathogenesis. J Neurovirol 10 (Suppl 1):25-32.
80. Westmoreland SV, Kolson D, Gonzalez-Scarano F. 1996. Toxicity of TNF-α and platelet activating factor for human NT2N neurons: A tissue culture model for human immunodeficiency virus dementia. J Neurovirol 2:118-126.
81. 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.
82. Yoshioka M, Bradley WG, Shapshak P, Nagano I, Stewart RV, Xin KQ, Srivastava AK, Nakamura S. 1995. Role of immune activation and cytokine expression in HIV-1-associated neurologic diseases. Adv Neuroimmunol 5:335-358.
83. Zheng J, Thylin MR, Ghorpade A, Xiong H, Persidsky Y, Cotter R, Niemann D, Che M, Zeng YC, Gelbard HA, et al. 1999. Intracellular CXCR4 signaling, neuronal apoptosis and neuropathogenic mechanisms of HIV-1-associated dementia. J Neuroimmunol 98:185-200.