Low-level HIV replication in mixed glial cultures is associated with alterations in the processing of p55Gag

Virology

Volumn 325, Issue 2, 2004, Pages 328-339

  Albright, Andrew V ^a   Vos, Robin M ^a   González Scarano, Francisco ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Glial cultures; HIV replication; Microglia; p55Gag

Indexed keywords

CYTOKINE; GAG PROTEIN; GROWTH FACTOR; PROTEIN P55; VIRUS PROTEIN;

ADULT; ARTICLE; CELL CULTURE; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; INTEGRATION; LATENT PERIOD; MICROGLIA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVERSE TRANSCRIPTION; VIRUS INFECTIVITY; VIRUS MUTATION; VIRUS REPLICATION;

CELLS, CULTURED; CULTURE MEDIA; GENE PRODUCTS, GAG; HIV-1; HUMANS; MICROSCOPY, FLUORESCENCE; NEUROGLIA; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 3142634784     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2004.04.028     Document Type: Article

References (82)

1. Albright A.V., Strizki J., Harouse J.M., Lavi E., O'Connor M., Gonzalez-Scarano F. HIV-1 infection of cultured human adult oligodendrocytes. Virology. 217(1):1996;211-219
2. Albright A.V., Shieh J.T., Itoh T., Lee B., Pleasure D., O'Connor M.J., Doms R.W., Gonzalez-Scarano F. 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(1):1999;205-213
3. Albright A.V., Erickson-Viitanen S., O'Connor M., Frank I., Rayner M.M., Gonzalez-Scarano F. Efavirenz is a potent nonnucleoside reverse transcriptase inhibitor of HIV type 1 replication in microglia in vitro. AIDS Res. Hum. Retroviruses. 16(15):2000;1527-1537
4. Albright A.V., Shieh J.T., O'Connor M.J., Gonzalez-Scarano F. Characterization of cultured microglia that can be infected by HIV-1. J. NeuroVirol. 6(Suppl. 1):2000;S53-60
5. Bagasra O., Lavi E., Bobroski L., Khalili K., Pestaner J.P., Tawadros R., Pomerantz R.J. 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(6):1996;573-585
6. Blankson J.N., Finzi D., Pierson T.C., Sabundayo B.P., Chadwick K., Margolick J.B., Quinn T.C., Siliciano R.F. Biphasic decay of latently infected CD4+ T cells in acute human immunodeficiency virus type 1 infection. J. Infect. Dis. 182(6):2000;1636-1642
7. Butera S.T. Therapeutic targeting of human immunodeficiency virus type-1 latency: current clinical realities and future scientific possibilities. Antiviral Res. 48(3):2000;143-176
8. Cavert W., Haase A.T. A national tissue bank to track HIV eradication and immune reconstruction. Science. 280(5371):1998;1865-1866
9. Cavert W., Notermans D.W., Staskus K., Wietgrefe S.W., Zupancic M., Gebhard K., Henry K., Zhang Z.Q., Mills R., McDade H., Schuwirth C.M., Goudsmit J., Danner S.A., Haase A.T. Kinetics of response in lymphoid tissues to antiretroviral therapy of HIV-1 infection. Science. 276(5314):1997;960-964
10. Chun T.W., Finzi D., Margolick J., Chadwick K., Schwartz D., Siliciano R.F. In vivo fate of HIV-1-infected T cells: quantitative analysis of the transition to stable latency. Nat. Med. 1(12):1995;1284-1290
11. Chun T.W., Carruth L., Finzi D., Shen X., DiGiuseppe J.A., Taylor H., Hermankova M., Chadwick K., Margolick J., Quinn T.C., Kuo Y.H., Brookmeyer R., Zeiger M.A., Barditch-Crovo P., Siliciano R.F. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature. 387(6629):1997;183-188
12. Chun T.W., Stuyver L., Mizell S.B., Ehler L.A., Mican J.A., Baseler M., Lloyd A.L., Nowak M.A., Fauci A.S. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc. Natl. Acad. Sci. U.S.A. 94(24):1997;13193-13197
13. Crowe S.M., Sonza S. HIV-1 can be recovered from a variety of cells including peripheral blood monocytes of patients receiving highly active antiretroviral therapy: a further obstacle to eradication. J. Leukocyte Biol. 68(3):2000;345-350
14. De Luca A., Ciancio B.C., Larussa D., Murri R., Cingolani A., Rizzo M.G., Giancola M.L., Ammassari A., Ortona L. Correlates of independent HIV-1 replication in the CNS and of its control by antiretrovirals. Neurology. 59(3):2002;342-347
15. Demirov D.G., Orenstein J.M., Freed E.O. The late domain of human immunodeficiency virus type 1 p6 promotes virus release in a cell type-dependent manner. J. Virol. 76(1):2002;105-117
16. Demoustier A., Gubler B., Lambotte O., de Goer M.G., Wallon C., Goujard C., Delfraissy J.F., Taoufik Y. In patients on prolonged HAART, a significant pool of HIV infected CD4 T cells are HIV-specific. AIDS. 16(13):2002;1749-1754
17. Dore G.J., Correll P.K., Li Y., Kaldor J.M., Cooper D.A., Brew B.J. Changes to AIDS dementia complex in the era of highly active antiretroviral therapy. AIDS. 13(10):1999;1249-1253
18. Fouchier R.A., Meyer B.E., Simon J.H., Fischer U., Malim M.H. HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for Gag processing but not for post-entry nuclear import. EMBO J. 16(15):1997;4531-4539
19. Gartner S., Markovits P., Markovitz D.M., Kaplan M.H., Gallo R.C., Popovic M. The role of mononuclear phagocytes in HTLV-III/LAV infection. Science. 233(4760):1986;215-219
20. Geijtenbeek T.B., Kwon D.S., Torensma R., van Vliet S.J., van Duijnhoven G.C., Middel J., Cornelissen I.L., Nottet H.S., KewalRamani V.N., Littman D.R., Figdor C.G., van Kooyk Y. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell. 100(5):2000;587-597
21. Glass J.D., Fedor H., Wesselingh S.L., McArthur J.C. Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann. Neurol. 38(5):1995;755-762
22. Gulick R.M., Mellors J.W., Havlir D., Eron J.J., Gonzalez C., McMahon D., Richman D.D., Valentine F.T., Jonas L., Meibohm A., Emini E.A., Chodakewitz J.A. Treatment with indinavir, zidovudine, and lamivudine in adults with human immunodeficiency virus infection and prior antiretroviral therapy. N. Engl. J. Med. 337(11):1997;734-739
23. Hammer S.M., Squires K.E., Hughes M.D., Grimes J.M., Demeter L.M., Currier J.S., Eron J.J. Jr., Feinberg J.E., Balfour H.H. Jr., Deyton L.R., Chodakewitz J.A., Fischl M.A. A controlled trial of two nucleoside analogues plus indinavir in persons with human immunodeficiency virus infection and CD4 cell counts of 200 per cubic millimeter or less. AIDS Clinical Trials Group 320 Study Team. N. Engl. J. Med. 337(11):1997;725-733
24. Ho D.D., Neumann A.U., Perelson A.S., Chen W., Leonard J.M., Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 373(6510):1995;123-126
25. Jordan C.A., Watkins B.A., Kufta C., Dubois-Dalcq M. Infection of brain microglial cells by human immunodeficiency virus type 1 is CD4 dependent. J. Virol. 65(2):1991;736-742
26. Jordan A., Bisgrove D., Verdin E. HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. EMBO J. 22(8):2003;1868-1877
27. Kaplan A.H., Swanstrom R. Human immunodeficiency virus type 1 Gag proteins are processed in two cellular compartments. Proc. Natl. Acad. Sci. U.S.A. 88(10):1991;4528-4532
28. Kaul M., Garden G.A., Lipton S.A. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature. 410(6831):2001;988-994
29. Kedzierska K., Crowe S.M. The role of monocytes and macrophages in the pathogenesis of HIV-1 infection. Curr. Med. Chem. 9(21):2002;1893-1903
30. Kikonyogo A., Bouamr F., Vana M.L., Xiang Y., Aiyar A., Carter C., Leis J. Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc. Natl. Acad. Sci. U.S.A. 98(20):2001;11199-11204
31. Koenig S., Gendelman H.E., Orenstein J.M., Dal Canto M.C., Pezeshkpour G.H., Yungbluth M., Janotta F., Aksamit A., Martin M.A., Fauci A.S. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science. 233(4768):1986;1089-1093
32. Krausslich H.G. Specific inhibitor of human immunodeficiency virus proteinase prevents the cytotoxic effects of a single-chain proteinase dimer and restores particle formation. J. Virol. 66(1):1992;567-572
33. Kutsch O., Benveniste E.N., Shaw G.M., Levy D.N. Direct and quantitative single-cell analysis of human immunodeficiency virus type 1 reactivation from latency. J. Virol. 76(17):2002;8776-8786
34. Laurence J. Reservoirs of HIV infection or carriage: monocytic, dendritic, follicular dendritic, and B cells. Ann. N. Y. Acad. Sci. 693:1993;52-64
35. Lawson L.J., Perry V.H., Gordon S. Turnover of resident microglia in the normal adult mouse brain. Neuroscience. 48(2):1992;405-415
36. Lebargy F., Branellec A., Deforges L., Bignon J., Bernaudin J.F. HIV-1 in human alveolar macrophages from infected patients is latent in vivo but replicates after in vitro stimulation. Am. J. Respir. Cell Mol. Biol. 10(1):1994;72-78
37. Li Y., Kappes J.C., Conway J.A., Price R.W., Shaw G.M., Hahn B.H. Molecular characterization of human immunodeficiency virus type 1 cloned directly from uncultured human brain tissue: identification of replication-competent and -defective viral genomes. J. Virol. 65(8):1991;3973-3985
38. McIlroy D., Autran B., Cheynier R., Clauvel J.P., Oksenhendler E., Debre P., Hosmalin A. Low infection frequency of macrophages in the spleens of HIV+ patients. Res. Virol. 147(2-3):1996;115-121
39. Meltzer M.S., Skillman D.R., Gomatos P.J., Kalter D.C., Gendelman H.E. Role of mononuclear phagocytes in the pathogenesis of human immunodeficiency virus infection. Annu. Rev. Immunol. 8:1990;169-194
40. Mikovits J.A., Lohrey N.C., Schulof R., Courtless J., Ruscetti F.W. Activation of infectious virus from latent human immunodeficiency virus infection of monocytes in vivo. J. Clin. Invest. 90(4):1992;1486-1491
41. Nau G.J., Richmond J.F., Schlesinger A., Jennings E.G., Lander E.S., Young R.A. Human macrophage activation programs induced by bacterial pathogens. Proc. Natl. Acad. Sci. U.S.A. 99(3):2002;1503-1508
42. Neuenburg J.K., Brodt H.R., Herndier B.G., Bickel M., Bacchetti P., Price R.W., Grant R.M., Schlote W. HIV-related neuropathology, 1985 to 1999: rising prevalence of HIV encephalopathy in the era of highly active antiretroviral therapy. J. Acquired Immune Defic. Syndr. 31(2):2002;171-177
43. Ono A., Freed E.O. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body. J. Virol. 78(3):2004;1552-1563
44. Palella F.J. Jr., Delaney K.M., Moorman A.C., Loveless M.O., Fuhrer J., Satten G.A., Aschman D.J., Holmberg S.D. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV outpatient study investigators. N. Engl. J. Med. 338(13):1998;853-860
45. Pelchen-Matthews A., Kramer B., Marsh M. Infectious HIV-1 assembles in late endosomes in primary macrophages. J. Cell Biol. 162(3):2003;443-455
46. Perelson A.S., Neumann A.U., Markowitz M., Leonard J.M., Ho D.D. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science. 271(5255):1996;1582-1586
47. Perelson A.S., Essunger P., Cao Y., Vesanen M., Hurley A., Saksela K., Markowitz M., Ho D.D. Decay characteristics of HIV-1-infected compartments during combination therapy. Nature. 387(6629):1997;188-191
48. Persaud D., Pierson T., Ruff C., Finzi D., Chadwick K.R., Margolick J.B., Ruff A., Hutton N., Ray S., Siliciano R.F. A stable latent reservoir for HIV-1 in resting CD4(+) T lymphocytes in infected children. J. Clin. Invest. 105(7):2000;995-1003
49. Pierson T., McArthur J., Siliciano R.F. Reservoirs for HIV-1: mechanisms for viral persistence in the presence of antiviral immune responses and antiretroviral therapy. Annu. Rev. Immunol. 18:2000;665-708
50. Pierson T.C., Zhou Y., Kieffer T.L., Ruff C.T., Buck C., Siliciano R.F. Molecular characterization of preintegration latency in human immunodeficiency virus type 1 infection. J. Virol. 76(17):2002;8518-8531
51. Pomerantz R.J. Eliminating HIV-1 reservoirs. Curr. Opin. Invest. Drugs. 3(8):2002;1133-1137
52. Popovic M., Gartner S. Isolation of HIV-1 from monocytes but not T lymphocytes. Lancet. 2(8564):1987;916
53. Quivy V., Van Lint C. Diversity of acetylation targets and roles in transcriptional regulation: the human immunodeficiency virus type 1 promoter as a model system. Biochem. Pharmacol. 64(5-6):2002;925-934
54. Raposo G., Moore M., Innes D., Leijendekker R., Leigh-Brown A., Benaroch P., Geuze H. Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic. 3(10):2002;718-729
55. Roberts B.D., Fang G., Butera S.T. Influence of cell cycle on HIV-1 expression differs among various models of chronic infection. Arch. Virol. 142(6):1997;1087-1099
56. Roy S., Wainberg M.A. Role of the mononuclear phagocyte system in the development of acquired immunodeficiency syndrome (AIDS). J. Leukocyte Biol. 43(1):1988;91-97
57. Ryzhova E.V., Crino P., Shawver L., Westmoreland S.V., Lackner A.A., Gonzalez-Scarano F. Simian immunodeficiency virus encephalitis: analysis of envelope sequences from individual brain multinucleated giant cells and tissue samples. Virology. 297(1):2002;57-67
58. Sacktor N., McDermott M.P., Marder K., Schifitto G., Selnes O.A., McArthur J.C., Stern Y., Albert S., Palumbo D., Kieburtz K., De Marcaida J.A., Cohen B., Epstein L. HIV-associated cognitive impairment before and after the advent of combination therapy. J. NeuroVirol. 8(2):2002;136-142
59. Schmidtmayerova H., Alfano M., Nuovo G., Bukrinsky M. Human immunodeficiency virus type 1 T-lymphotropic strains enter macrophages via a CD4- and CXCR4-mediated pathway: replication is restricted at a postentry level. J. Virol. 72(6):1998;4633-4642
60. Schrager L.K., D'Souza M.P. Cellular and anatomical reservoirs of HIV-1 in patients receiving potent antiretroviral combination therapy. JAMA. 280(1):1998;67-71
61. Schroder A.R., Shinn P., Chen H., Berry C., Ecker J.R., Bushman F. HIV-1 integration in the human genome favors active genes and local hotspots. Cell. 110(4):2002;521-529
62. Shawver L., Baribaud R., Doms R.W., Pardo-Villamizar D., McArthur J., Gonzalez-Scarano F. Expression of DC-SIGN in cultured microglia and in the CNS of individuals with and without HIV dementia (HIV-D). 9th Conference on Retroviruses and Opportunistic Infections:2000
63. Shieh J.T., Albright A.V., Sharron M., Gartner S., Strizki J., Doms R.W., Gonzalez-Scarano F. Chemokine receptor utilization by human immunodeficiency virus type 1 isolates that replicate in microglia. J. Virol. 72(5):1998;4243-4249
64. Si Q., Cosenza M., Zhao M.L., Goldstein H., Lee S.C. GM-CSF and M-CSF modulate beta-chemokine and HIV-1 expression in microglia. Glia. 39(2):2002;174-183
65. Sierra-Madero J.G., Toossi Z., Hom D.L., Finegan C.K., Hoenig E., Rich E.A. Relationship between load of virus in alveolar macrophages from human immunodeficiency virus type 1-infected persons, production of cytokines, and clinical status. J. Infect. Dis. 169(1):1994;18-27
66. Sokal R.R., Rohlf F.J. Biometry: The Principles and Practice of Statistics in Biological Research. 1995;Freeman, New York, NY
67. Sonza S., Maerz A., Deacon N., Meanger J., Mills J., Crowe S. Human immunodeficiency virus type 1 replication is blocked prior to reverse transcription and integration in freshly isolated peripheral blood monocytes. J. Virol. 70(6):1996;3863-3869
68. Sonza S., Mutimer H.P., Oelrichs R., Jardine D., Harvey K., Dunne A., Purcell D.F., Birch C., Crowe S.M. Monocytes harbour replication-competent, non-latent HIV-1 in patients on highly active antiretroviral therapy. AIDS. 15(1):2001;17-22
69. Spiegel H., Herbst H., Niedobitek G., Foss H.D., Stein H. Follicular dendritic cells are a major reservoir for human immunodeficiency virus type 1 in lymphoid tissues facilitating infection of CD4+ T-helper cells. Am. J. Pathol. 140(1):1992;15-22
70. Sternstein M. Statistics. 1994;Barron's, Hauppage, NY
71. Strack B., Calistri A., Accola M.A., Palu G., Gottlinger H.G. A role for ubiquitin ligase recruitment in retrovirus release. Proc. Natl. Acad. Sci. U.S.A. 97(24):2000;13063-13068
72. Strizki J.M., Albright A.V., Sheng H., O'Connor M., Perrin L., Gonzalez-Scarano F. Infection of primary human microglia and monocyte-derived macrophages with human immunodeficiency virus type 1 isolates: evidence of differential tropism. J. Virol. 70(11):1996;7654-7662
73. Tyor W.R., Glass J.D., Griffin J.W., Becker P.S., McArthur J.C., Bezman L., Griffin D.E. Cytokine expression in the brain during the acquired immunodeficiency syndrome. Ann. Neurol. 31(4):1992;349-360
74. van Furth R. Origin and turnover of monocytes and macrophages. Curr. Top. Pathol. 79:1989;125-150
75. Vass K., Hickey W.F., Schmidt R.E., Lassmann H. Bone marrow-derived elements in the peripheral nervous system. An immunohistochemical and ultrastructural investigation in chimeric rats. Lab. Invest. 69(3):1993;275-282
76. Vodicka M.A., Goh W.C., Wu L.I., Rogel M.E., Bartz S.R., Schweickart V.L., Raport C.J., Emerman M. Indicator cell lines for detection of primary strains of human and simian immunodeficiency viruses. Virology. 233(1):1997;193-198
77. Watkins B.A., Dorn H.H., Kelly W.B., Armstrong R.C., Potts B.J., Michaels F., Kufta C.V., Dubois-Dalcq M. Specific tropism of HIV-1 for microglial cells in primary human brain cultures. Science. 249(4968):1990;549-553
78. Wei X., Ghosh S.K., Taylor M.E., Johnson V.A., Emini E.A., Deutsch P., Lifson J.D., Bonhoeffer S., Nowak M.A., Hahn B.H., et al. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 373(6510):1995;117-122
79. Wesselingh S.L., Power C., Glass J.D., Tyor W.R., McArthur J.C., Farber J.M., Griffin J.W., Griffin D.E. Intracerebral cytokine messenger RNA expression in acquired immunodeficiency syndrome dementia. Ann. Neurol. 33(6):1993;576-582
80. Wiley C.A., Schrier R.D., Nelson J.A., Lampert P.W., Oldstone M.B. Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc. Natl. Acad. Sci. U.S.A. 83(18):1986;7089-7093
81. Winston B.W., Krein P.M., Mowat C., Huang Y. Cytokine-induced macrophage differentiation: a tale of 2 genes. Clin. Invest. Med. 22(6):1999;236-255
82. Yong V.W., Antel J.P. Culture of glial cells from human brain biopsies. Fedoroff S., Richardson A. Protocols for Neural Cell Culture. 1992;81-96 Humana Press, Totowa, NJ