Journal of Neuroimmunology
Volume 178, Issue 1 , Pages 87-99 , September 2006

Modulation of astrocyte proliferation by HIV-1: Differential effects in productively infected, uninfected, and Nef-expressing cells

  • Melissa A. Cosenza-Nashat

      Affiliations

    • Borough of Manhattan Community College, City University of New York, Department of Science, New York, NY 10007, United States
  • ,
  • Qiusheng Si

      Affiliations

    • Department of Pathology F717, Albert Einstein College of Medicine, 1300 Morris Park Avenue Bronx NY 10461, United States
  • ,
  • Meng-Liang Zhao

      Affiliations

    • Department of Pathology F717, Albert Einstein College of Medicine, 1300 Morris Park Avenue Bronx NY 10461, United States
  • ,
  • Sunhee C. Lee

      Affiliations

    • Department of Pathology F717, Albert Einstein College of Medicine, 1300 Morris Park Avenue Bronx NY 10461, United States
    • Corresponding Author InformationCorresponding author. Tel.: +1 718 430 2666; fax: +1 718 430 8867.

Received 23 March 2005 ,Revised 11 April 2006 ,Accepted 16 May 2006.

References 

  1. Amini S, Khalili K, Sawaya BE. Effect of HIV-1 Vpr on cell cycle regulators. DNA Cell Biol. 2004;23:249–260
  2. Andersen JL, Planelles V. The role of Vpr in HIV-1 pathogenesis. Curr. HIV Res. 2005;3:43–51
  3. Anderson CE, Tomlinson GS, Pauly B, Brannan FW, Chiswick A, Brack-Werner R, et al. Relationship of Nef-positive and GFAP-reactive astrocytes to drug use in early and late HIV infection. Neuropathol. Appl. Neurobiol. 2003;29:378–388
  4. Ayyavoo V, Mahalingam S, Rafaeli Y, Kudchodkar S, Chang D, Nagashunmugam T, et al. HIV-1 viral protein R (Vpr) regulates viral replication and cellular proliferation in T cells and monocytoid cells in vitro. J. Leukoc. Biol. 1997;62:93–99
  5. Bagasra O, Lavi E, Bobroski L, Khalili K, Pestaner JP, Tawadros R, et al. 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. 1996;10:573–585
  6. Benveniste EN, Shrikant P, Patton KS, Benos DJ. Neuroimmunologic mechanisms for disease in AIDS: the role of the astrocyte. In:  Gendelman HE,  Lipton SA,  Epstein L,  Swindells S editor. The Neurology of AIDS. New York: Chapman & Hall; 1998;130 pp.
  7. Boven LA, Middel J, Portegies P, Verhoef J, Jansen GH, Nottet HS. Overexpression of nerve growth factor and basic fibroblast growth factor in AIDS dementia complex. J. Neuroimmunol. 1999;97:154–162
  8. Brack-Werner R. Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. AIDS. 1999;13:1–22
  9. Brack-Werner R, Kleinschmidt A, Ludvigsen A, Mellert W, Neumann M, Herrmann R, et al. Infection of human brain cells by HIV-1: restricted virus production in chronically infected human glial cell lines. AIDS. 1992;6:273–285
  10. Brew BJ, Rosenblum M, Cronin K, Price RW. AIDS dementia complex and HIV-1 brain infection: clinical-virological correlations. Ann. Neurol. 1995;38:563–570
  11. Canki M, Thai JN, Chao W, Ghorpade A, Potash MJ, Volsky DJ. 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. 2001;75:7925–7933
  12. Carroll-Anzinger D, Al Harthi L. Gamma interferon primes productive human immunodeficiency virus infection in astrocytes. J. Virol. 2006;80:541–544
  13. Chen Y, Swanson RA. Astrocytes and brain injury. J. Cereb. Blood Flow Metab. 2003;23:137–149
  14. Clapham PR, Weber JN, Whitby D, McIntosh K, Dalgleish AG, Maddon PJ, et al. Soluble CD4 blocks the infectivity of diverse strains of HIV and SIV for T cells and monocytes but not for brain and muscle cells. Nature. 1989;337:368–370
  15. Colodner KJ, Montana RA, Anthony DC, Folkerth RD, De Girolami U, Feany MB. Proliferative potential of human astrocytes. J. Neuropathol. Exp. Neurol. 2005;64:163–169
  16. Conant K, Major EO. Astrocytes as mediators of CNS injury in AIDS. In:  Gendelman HE,  Lipton SA,  Epstein L editor. The Neurology of AIDS. New York: Chapman & Hall; 1998;147 pp.
  17. Connor RI, Chen BK, Choe S, Landau NR. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology. 1995;206:935–944
  18. Dewhurst S, Sakai K, Bresser J, Stevenson M, Evinger-Hodges MJ, Volsky DJ. Persistent productive infection of human glial cells by human immunodeficiency virus (HIV) and by infectious molecular clones of HIV. J. Virol. 1987;61:3774–3782
  19. Di Rienzo AM, Aloisi F, Santarcangelo AC, Palladino C, Olivetta E, Genovese D, et al. Virological and molecular parameters of HIV-1 infection of human embryonic astrocytes. Arch. Virol. 1998;143:1599–1615
  20. Erfle V, Stoeckbauer P, Kleinschmidt A, Kohleisen B, Mellert W, Stavrou D, et al. Target cells for HIV in the central nervous system: macrophages or glial cells. Res Virol. 1991;142:139–144
  21. Gerdes J, Schwab U, Lemke H, Stein H. Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int. J. Cancer. 1983;31:13–20
  22. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 1984;133:1710–1715
  23. Gorry PR, Howard JL, Churchill MJ, Anderson JL, Cunningham A, Adrian D, et al. Diminished production of human immunodeficiency virus type 1 in astrocytes results from inefficient translation of gag, env, and nef mRNAs despite efficient expression of Tat and Rev. J. Virol. 1999;73:352–361
  24. Gosztonyi G, Artigas J, Lamperth L, Webster HD. Human immunodeficiency virus (HIV) distribution in HIV encephalitis: study of 19 cases with combined use of in situ hybridization and immunocytochemistry. J. Neuropathol. Exp. Neurol. 1994;53:521–534
  25. Guillemin G, Croitoru J, Le Grand RL, Franck-Duchenne M, Dormont D, Boussin FD. Simian immunodeficiency virus mac251 infection of astrocytes. J. Neurovirol. 2000;6:173–186
  26. Hao HN, Lyman WD. HIV infection of fetal human astrocytes: the potential role of a receptor-mediated endocytic pathway. Brain Res. 1999;823:24–32
  27. Jicha GA, Lane E, Vincent I, Otvos L, Hoffmann R, Davies P. A conformation- and phosphorylation-dependent antibody recognizing the paired helical filaments of Alzheimer's disease. J. Neurochem. 1997;69:2087–2095
  28. Kim SY, Li J, Bentsman G, Brooks AI, Volsky DJ. Microarray analysis of changes in cellular gene expression induced by productive infection of primary human astrocytes: implications for HAD. J. Neuroimmunol. 2004;157:17–26
  29. Kundu M, Sharma S, de Luca A, Giordano A, Rappaport J, Khalili K, et al. HIV-1 Tat elongates the G1 phase and indirectly promotes HIV-1 gene expression in cells of glial origin. J. Biol. Chem. 1998;273:8130–8136
  30. Kunsch C, Hartle HT, Wigdahl B. Infection of human fetal dorsal root ganglion glial cells with human immunodeficiency virus type 1 involves an entry mechanism independent of the CD4 T4A epitope. J. Virol. 1989;63:5054–5061
  31. Lee SC, Brosnan CF. Molecular biology of glia: astrocytes. In:  Russell WC editors. Molecular Biology of Multiple Sclerosis. Chichester, England: John Wiley & Sons, Ltd.; 1997;71 pp.
  32. Lee SC, Liu W, Brosnan CF, Dickson DW. Characterization of human fetal dissociated CNS cultures with an emphasis on microglia. Lab. Invest. 1992;67:465–475
  33. Lee SC, Cosenza MA, Si Q, Rivieccio M, Brosnan CF. The CNS: cells, tissues and reactions to insult. In:  Ransohoff RM,  Benveniste EN editor. Cytokines and the CNS. Boca Raton, FL: CRC Press; 2005;
  34. Li J, Liu Y, Park IW, He JJ. Expression of exogenous Sam68, the 68-kilodalton SRC-associated protein in mitosis, is able to alleviate impaired Rev function in astrocytes. J. Virol. 2002;76:4526–4535
  35. Liu Y, Liu H, Kim BO, Gattone VH, Li J, Nath A, et al. CD4-independent infection of astrocytes by human immunodeficiency virus type 1: requirement for the human mannose receptor. J. Virol. 2004;78:4120–4133
  36. Lopez F, Belloc F, Lacombe F, Dumain P, Reiffers J, Bernard P, et al. Modalities of synthesis of Ki67 antigen during the stimulation of lymphocytes. Cytometry. 1991;12:42–49
  37. Ludwig E, Silberstein FC, van Empel J, Erfle V, Neumann M, Brack-Werner R. Diminished rev-mediated stimulation of human immunodeficiency virus type 1 protein synthesis is a hallmark of human astrocytes. J. Virol. 1999;73:8279–8289
  38. Ma M, Geiger JD, Nath A. Characterization of a novel binding site for the human immunodeficiency virus type 1 envelope protein gp120 on human fetal astrocytes. J. Virol. 1994;68:6824–6828
  39. Morris CS, Esiri MM, Sprinkle TJ, Gregson N. Oligodendrocyte reactions and cell proliferation markers in human demyelinating diseases. Neuropathol. Appl. Neurobiol. 1994;20:272–281
  40. Nath A, Hartloper V, Furer M, Fowke KR. Infection of human fetal astrocytes with HIV-1: viral tropism and the role of cell to cell contact in viral transmission. J. Neuropathol. Exp. Neurol. 1995;54:320–330
  41. Ndolo T, Dhillon NK, Nguyen H, Guadalupe M, Mudryj M, Dandekar S. Simian immunodeficiency virus Nef protein delays the progression of CD4+ T cells through G1/S phase of the cell cycle. J. Virol. 2002;76:3587–3595
  42. Neumann M, Afonina E, Ceccherini-Silberstein F, Schlicht S, Erfle V, Pavlakis GN, et al. Nucleocytoplasmic transport in human astrocytes: decreased nuclear uptake of the HIV Rev shuttle protein. J. Cell Sci. 2001;114:1717–1729
  43. Rytik PG, Eremin VF, Kvacheva ZB, Poleschuk NN, Popov SA, Schroder HC, et al. Susceptibility of primary human glial fibrillary acidic protein-positive brain cells to human immunodeficiency virus infection in vitro: anti-HIV activity of memantine. AIDS Res. Hum. Retrovir. 1991;7:89–95
  44. Sabri F, Tresoldi E, Di Stefano M, Polo S, Monaco MC, Verani A, et al. Nonproductive human immunodeficiency virus type 1 infection of human fetal astrocytes: independence from CD4 and major chemokine receptors. Virology. 1999;264:370–384
  45. Saito Y, Sharer LR, Epstein LG, Michaelis J, Mintz M, Louder M, et al. Overexpression of nef as a marker for restricted HIV-1 infection of astrocytes in postmortem pediatric central nervous tissues. Neurology. 1994;44:474–481
  46. Schafer KA. The cell cycle: a review. Vet. Pathol. 1998;35:461–478
  47. Schweighardt B, Atwood WJ. HIV type 1 infection of human astrocytes is restricted by inefficient viral entry. AIDS Res. Hum. Retrovir. 2001;17:1133–1142
  48. Shaw GM, Harper ME, Hahn BH, Epstein LG, Gajdusek DC, Price RW, et al. HTLV-III infection in brains of children and adults with AIDS encephalopathy. Science. 1985;227:177–182
  49. Sherman MP, De Noronha CM, Williams SA, Greene WC. Insights into the biology of HIV-1 viral protein R. DNA Cell Biol. 2002;21:679–688
  50. Soontornniyomkij V, Wang G, Pittman CA, Wiley CA, Achim CL. Expression of brain-derived neurotrophic factor protein in activated microglia of human immunodeficiency virus type 1 encephalitis. Neuropathol. Appl. Neurobiol. 1998;24:453–460
  51. Subbramanian RA, Kessous-Elbaz A, Lodge R, Forget J, Yao XJ, Bergeron D, et al. Human immunodeficiency virus type 1 Vpr is a positive regulator of viral transcription and infectivity in primary human macrophages. J. Exp. Med. 1998;187:1103–1111
  52. Swingler S, Mann A, Jacque J, Brichacek B, Sasseville VG, Williams K, et al. HIV-1 Nef mediates lymphocyte chemotaxis and activation by infected macrophages. Nat. Med. 1999;5:997–1003
  53. Takahashi K, Wesselingh SL, Griffin DE, McArthur JC, Johnson RT, Glass JD. Localization of HIV-1 in human brain using polymerase chain reaction/in situ hybridization and immunocytochemistry. Ann. Neurol. 1996;39:705–711
  54. Thompson KA, McArthur JC, Wesselingh SL. Correlation between neurological progression and astrocyte apoptosis in HIV-associated dementia. Ann. Neurol. 2001;49:745–752
  55. Tornatore C, Nath A, Amemiya K, Major EO. Persistent human immunodeficiencey virus type I infection in human fetal glial cells reactivated by T-cell factor(s) or by the cytokines tumor necrosis factor alpha and interleukin-1 beta. J. Virol. 1991;65:6094–6100
  56. Tornatore C, Chandra R, Berger JR, Major EO. HIV-1 infection of subcortical astrocytes in the pediatric central nervous system. Neurol. 1994;44:481–487
  57. Tornatore C, Meyers K, Atwood W, Conant K, Major E. Temporal patterns of human immunodeficiency virus type I transcripts in human fetal astrocytes. J. Virol. 1994;68:93–102
  58. Vincent I, Zheng JH, Dickson DW, Kress Y, Davies P. Mitotic phosphoepitopes precede paired helical filaments in Alzheimer's disease. Neurobiol. Aging. 1998;19:287–296
  59. Wang Z, Trillo-Pazos G, Kim SY, Canki M, Morgello S, Sharer LR, et al. Effects of human immunodeficiency virus type 1 on astrocyte gene expression and function: potential role in neuropathogenesis. J. Neurovirol. 2004;10(Suppl 1):25–32
  60. Weis S, Haug H, Budka H. Astroglial changes in the cerebral cortex of AIDS brains: a morphometric and immunohistochemical investigation. Neuropathol. Appl. Neurobiol. 1993;19:329–335
  61. Zhou BY, He JJ. Proliferation inhibition of astrocytes, neurons, and non-glial cells by intracellularly expressed human immunodeficiency virus type 1 (HIV-1) Tat protein. Neurosci. Lett. 2004;359:155–158

PII: S0165-5728(06)00193-7

doi: 10.1016/j.jneuroim.2006.05.020

Journal of Neuroimmunology
Volume 178, Issue 1 , Pages 87-99 , September 2006