Skip to main content
Top
Published in: Archives of Virology 2/2019

Open Access 01-02-2019 | Original Article

No detection of CD4-independent human immunodeficiency virus 1 envelope glycoproteins in brain tissue of patients with or without neurological complications

Authors: Briana Quitadamo, Paul J. Peters, Matthew Koch, Katherine Luzuriaga, Cecilia Cheng-Mayer, Paul R. Clapham, Maria Paz Gonzalez-Perez

Published in: Archives of Virology | Issue 2/2019

Login to get access

Abstract

Macrophage (mac)-tropic human immnunodeficiency virus type 1 (HIV-1) and simian immnunodeficiency virus (SIV) in brain are associated with neurological disease. Mac-tropic HIV-1 evolves enhanced CD4 interactions that enable macrophage infection via CD4, which is in low abundance. In contrast, mac-tropic SIV is associated with CD4-independent infection via direct CCR5 binding. Recently, mac-tropic simian-human immunodeficiency virus (SHIV) from macaque brain was also reported to infect cells via CCR5 without CD4. Since SHIV envelope proteins (Envs) are derived from HIV-1, we tested more than 100 HIV-1 clade B Envs for infection of CD4-negative, CCR5+ Cf2Th/CCR5 cells. However, no infection was detected. Our data suggest that there are differences in the evolution of mac-tropism in SIV and SHIV compared to HIV-1 clade B due to enhanced interactions with CCR5 and CD4, respectively.
Literature
1.
go back to reference An SF, Groves M, Giometto B, Beckett AA, Scaravilli F (1999) Detection and localisation of HIV-1 DNA and RNA in fixed adult AIDS brain by polymerase chain reaction/in situ hybridisation technique. Acta Neuropathol (Berl) 98:481–487CrossRef An SF, Groves M, Giometto B, Beckett AA, Scaravilli F (1999) Detection and localisation of HIV-1 DNA and RNA in fixed adult AIDS brain by polymerase chain reaction/in situ hybridisation technique. Acta Neuropathol (Berl) 98:481–487CrossRef
2.
go back to reference Bannert N, Schenten D, Craig S, Sodroski J (2000) The level of CD4 expression limits infection of primary rhesus monkey macrophages by a T-tropic simian immunodeficiency virus and macrophagetropic human immunodeficiency viruses. J Virol 74:10984–10993CrossRefPubMedPubMedCentral Bannert N, Schenten D, Craig S, Sodroski J (2000) The level of CD4 expression limits infection of primary rhesus monkey macrophages by a T-tropic simian immunodeficiency virus and macrophagetropic human immunodeficiency viruses. J Virol 74:10984–10993CrossRefPubMedPubMedCentral
3.
go back to reference Bell JE, Busuttil A, Ironside JW, Rebus S, Donaldson YK, Simmonds P, Peutherer JF (1993) Human immunodeficiency virus and the brain: investigation of virus load and neuropathologic changes in pre-AIDS subjects. J Infect Dis 168:818–824CrossRefPubMed Bell JE, Busuttil A, Ironside JW, Rebus S, Donaldson YK, Simmonds P, Peutherer JF (1993) Human immunodeficiency virus and the brain: investigation of virus load and neuropathologic changes in pre-AIDS subjects. J Infect Dis 168:818–824CrossRefPubMed
4.
go back to reference Bissel SJ, Wang G, Trichel AM, Murphey-Corb M, Wiley CA (2006) Longitudinal analysis of monocyte/macrophage infection in simian immunodeficiency virus-infected, CD8+ T-cell-depleted macaques that develop lentiviral encephalitis. Am J Pathol 168:1553–1569CrossRefPubMedPubMedCentral Bissel SJ, Wang G, Trichel AM, Murphey-Corb M, Wiley CA (2006) Longitudinal analysis of monocyte/macrophage infection in simian immunodeficiency virus-infected, CD8+ T-cell-depleted macaques that develop lentiviral encephalitis. Am J Pathol 168:1553–1569CrossRefPubMedPubMedCentral
5.
go back to reference Boyd DF, Peterson D, Haggarty BS, Jordan AP, Hogan MJ, Goo L, Hoxie JA, Overbaugh J (2015) Mutations in HIV-1 envelope that enhance entry with the macaque CD4 receptor alter antibody recognition by disrupting quaternary interactions within the trimer. J Virol 89:894–907CrossRefPubMed Boyd DF, Peterson D, Haggarty BS, Jordan AP, Hogan MJ, Goo L, Hoxie JA, Overbaugh J (2015) Mutations in HIV-1 envelope that enhance entry with the macaque CD4 receptor alter antibody recognition by disrupting quaternary interactions within the trimer. J Virol 89:894–907CrossRefPubMed
6.
go back to reference Carroll A, Brew B (2017) HIV-associated neurocognitive disorders: recent advances in pathogenesis, biomarkers, and treatment. F1000Res 6:312 Carroll A, Brew B (2017) HIV-associated neurocognitive disorders: recent advances in pathogenesis, biomarkers, and treatment. F1000Res 6:312
7.
go back to reference Churchill MJ, Wesselingh SL, Cowley D, Pardo CA, McArthur JC, Brew BJ, Gorry PR (2009) Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann Neurol 66:253–258CrossRefPubMed Churchill MJ, Wesselingh SL, Cowley D, Pardo CA, McArthur JC, Brew BJ, Gorry PR (2009) Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann Neurol 66:253–258CrossRefPubMed
8.
go back to reference Clapham PR, McKnight A, Weiss RA (1992) Human immunodeficiency virus type 2 infection and fusion of CD4-negative human cell lines: induction and enhancement by soluble CD4. J Virol 66:3531–3537PubMedPubMedCentral Clapham PR, McKnight A, Weiss RA (1992) Human immunodeficiency virus type 2 infection and fusion of CD4-negative human cell lines: induction and enhancement by soluble CD4. J Virol 66:3531–3537PubMedPubMedCentral
9.
go back to reference Cosenza MA, Zhao ML, Si Q, Lee SC (2002) Human brain parenchymal microglia express CD14 and CD45 and are productively infected by HIV-1 in HIV-1 encephalitis. Brain Pathol 12:442–455CrossRefPubMed Cosenza MA, Zhao ML, Si Q, Lee SC (2002) Human brain parenchymal microglia express CD14 and CD45 and are productively infected by HIV-1 in HIV-1 encephalitis. Brain Pathol 12:442–455CrossRefPubMed
10.
go back to reference Coutu M, Finzi A (2015) HIV-1 gp120 dimers decrease the overall affinity of gp120 preparations for CD4-induced ligands. J Virol Methods 215–216:37–44CrossRefPubMed Coutu M, Finzi A (2015) HIV-1 gp120 dimers decrease the overall affinity of gp120 preparations for CD4-induced ligands. J Virol Methods 215–216:37–44CrossRefPubMed
11.
go back to reference Davis LE, Hjelle BL, Miller VE, Palmer DL, Llewellyn AL, Merlin TL, Young SA, Mills RG, Wachsman W, Wiley CA (1992) Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 42:1736–1739CrossRefPubMed Davis LE, Hjelle BL, Miller VE, Palmer DL, Llewellyn AL, Merlin TL, Young SA, Mills RG, Wachsman W, Wiley CA (1992) Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 42:1736–1739CrossRefPubMed
12.
go back to reference Donaldson YK, Bell JE, Ironside JW, Brettle RP, Robertson JR, Busuttil A, Simmonds P (1994) Redistribution of HIV outside the lymphoid system with onset of AIDS. Lancet 343:383–385CrossRefPubMed Donaldson YK, Bell JE, Ironside JW, Brettle RP, Robertson JR, Busuttil A, Simmonds P (1994) Redistribution of HIV outside the lymphoid system with onset of AIDS. Lancet 343:383–385CrossRefPubMed
13.
go back to reference Duenas-Decamp MJ, Peters PJ, Burton D, Clapham PR (2009) Determinants flanking the CD4 binding loop modulate macrophage tropism of human immunodeficiency virus type 1 R5 envelopes. J Virol 83:2575–2583CrossRefPubMedPubMedCentral Duenas-Decamp MJ, Peters PJ, Burton D, Clapham PR (2009) Determinants flanking the CD4 binding loop modulate macrophage tropism of human immunodeficiency virus type 1 R5 envelopes. J Virol 83:2575–2583CrossRefPubMedPubMedCentral
14.
go back to reference Duenas-Decamp MJ, Clapham PR (2010) HIV-1 gp120 determinants proximal to the CD4 binding site shift protective glycans that are targeted by monoclonal antibody, 2G12. J Virol 84:9608–9612CrossRefPubMedPubMedCentral Duenas-Decamp MJ, Clapham PR (2010) HIV-1 gp120 determinants proximal to the CD4 binding site shift protective glycans that are targeted by monoclonal antibody, 2G12. J Virol 84:9608–9612CrossRefPubMedPubMedCentral
15.
go back to reference Dunfee RL, Thomas ER, Gorry PR, Wang J, Taylor J, Kunstman K, Wolinsky SM, Gabuzda D (2006) The HIV Env variant N283 enhances macrophage tropism and is associated with brain infection and dementia. Proc Natl Acad Sci USA 103:15160–15165CrossRefPubMed Dunfee RL, Thomas ER, Gorry PR, Wang J, Taylor J, Kunstman K, Wolinsky SM, Gabuzda D (2006) The HIV Env variant N283 enhances macrophage tropism and is associated with brain infection and dementia. Proc Natl Acad Sci USA 103:15160–15165CrossRefPubMed
16.
go back to reference Fischer-Smith T, Croul S, Sverstiuk AE, Capini C, L’Heureux D, Regulier EG, Richardson MW, Amini S, Morgello S, Khalili K, Rappaport J (2001) CNS invasion by CD14+/CD16+ peripheral blood-derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection. J Neurovirol 7:528–541CrossRefPubMed Fischer-Smith T, Croul S, Sverstiuk AE, Capini C, L’Heureux D, Regulier EG, Richardson MW, Amini S, Morgello S, Khalili K, Rappaport J (2001) CNS invasion by CD14+/CD16+ peripheral blood-derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection. J Neurovirol 7:528–541CrossRefPubMed
17.
go back to reference Fischer-Smith T, Croul S, Adeniyi A, Rybicka K, Morgello S, Khalili K, Rappaport J (2004) Macrophage/microglial accumulation and proliferating cell nuclear antigen expression in the central nervous system in human immunodeficiency virus encephalopathy. Am J Pathol 164:2089–2099CrossRefPubMedPubMedCentral Fischer-Smith T, Croul S, Adeniyi A, Rybicka K, Morgello S, Khalili K, Rappaport J (2004) Macrophage/microglial accumulation and proliferating cell nuclear antigen expression in the central nervous system in human immunodeficiency virus encephalopathy. Am J Pathol 164:2089–2099CrossRefPubMedPubMedCentral
18.
go back to reference Flaherty MT, Hauer DA, Mankowski JL, Zink MC, Clements JE (1997) Molecular and biological characterization of a neurovirulent molecular clone of simian immunodeficiency virus. J Virol 71:5790–5798PubMedPubMedCentral Flaherty MT, Hauer DA, Mankowski JL, Zink MC, Clements JE (1997) Molecular and biological characterization of a neurovirulent molecular clone of simian immunodeficiency virus. J Virol 71:5790–5798PubMedPubMedCentral
19.
go back to reference Glass JD, Fedor H, Wesselingh SL, McArthur JC (1995) Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 38:755–762CrossRefPubMed Glass JD, Fedor H, Wesselingh SL, McArthur JC (1995) Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 38:755–762CrossRefPubMed
20.
go back to reference Gonzalez-Perez MP, O’Connell O, Lin R, Sullivan WM, Bell J, Simmonds P, Clapham PR (2012) Independent evolution of macrophage-tropism and increased charge between HIV-1 R5 envelopes present in brain and immune tissue. Retrovirology 9:20CrossRefPubMedPubMedCentral Gonzalez-Perez MP, O’Connell O, Lin R, Sullivan WM, Bell J, Simmonds P, Clapham PR (2012) Independent evolution of macrophage-tropism and increased charge between HIV-1 R5 envelopes present in brain and immune tissue. Retrovirology 9:20CrossRefPubMedPubMedCentral
21.
go back to reference Gonzalez-Perez MP, Peters PJ, O’Connell O, Silva N, Harbison C, Cummings Macri S, Kaliyaperumal S, Luzuriaga K, Clapham PR (2017) Identification of emerging macrophage-tropic HIV-1 R5 variants in brain tissue of AIDS patients without severe neurological complications. J Virol 91:e00755-00717CrossRef Gonzalez-Perez MP, Peters PJ, O’Connell O, Silva N, Harbison C, Cummings Macri S, Kaliyaperumal S, Luzuriaga K, Clapham PR (2017) Identification of emerging macrophage-tropic HIV-1 R5 variants in brain tissue of AIDS patients without severe neurological complications. J Virol 91:e00755-00717CrossRef
22.
go back to reference Gonzalez-Scarano F, Martin-Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5:69–81CrossRefPubMed Gonzalez-Scarano F, Martin-Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5:69–81CrossRefPubMed
23.
go back to reference Goodenow MM, Collman RG (2006) HIV-1 coreceptor preference is distinct from target cell tropism: a dual-parameter nomenclature to define viral phenotypes. J Leukoc Biol 80:965–972CrossRefPubMed Goodenow MM, Collman RG (2006) HIV-1 coreceptor preference is distinct from target cell tropism: a dual-parameter nomenclature to define viral phenotypes. J Leukoc Biol 80:965–972CrossRefPubMed
24.
go back to reference Gorry PR, Bristol G, Zack JA, Ritola K, Swanstrom R, Birch CJ, Bell JE, Bannert N, Crawford K, Wang H, Schols D, De Clercq E, Kunstman K, Wolinsky SM, Gabuzda D (2001) Macrophage tropism of human immunodeficiency virus type 1 isolates from brain and lymphoid tissues predicts neurotropism independent of coreceptor specificity. J Virol 75:10073–10089CrossRefPubMedPubMedCentral Gorry PR, Bristol G, Zack JA, Ritola K, Swanstrom R, Birch CJ, Bell JE, Bannert N, Crawford K, Wang H, Schols D, De Clercq E, Kunstman K, Wolinsky SM, Gabuzda D (2001) Macrophage tropism of human immunodeficiency virus type 1 isolates from brain and lymphoid tissues predicts neurotropism independent of coreceptor specificity. J Virol 75:10073–10089CrossRefPubMedPubMedCentral
25.
go back to reference Gorry PR, Taylor J, Holm GH, Mehle A, Morgan T, Cayabyab M, Farzan M, Wang H, Bell JE, Kunstman K, Moore JP, Wolinsky SM, Gabuzda D (2002) Increased CCR5 affinity and reduced CCR5/CD4 dependence of a neurovirulent primary human immunodeficiency virus type 1 isolate. J Virol 76:6277–6292CrossRefPubMedPubMedCentral Gorry PR, Taylor J, Holm GH, Mehle A, Morgan T, Cayabyab M, Farzan M, Wang H, Bell JE, Kunstman K, Moore JP, Wolinsky SM, Gabuzda D (2002) Increased CCR5 affinity and reduced CCR5/CD4 dependence of a neurovirulent primary human immunodeficiency virus type 1 isolate. J Virol 76:6277–6292CrossRefPubMedPubMedCentral
26.
go back to reference Guo J, Wang W, Yu D, Wu Y (2011) Spinoculation triggers dynamic actin and cofilin activity that facilitates HIV-1 infection of transformed and resting CD4 T cells. J Virol 85:9824–9833CrossRefPubMedPubMedCentral Guo J, Wang W, Yu D, Wu Y (2011) Spinoculation triggers dynamic actin and cofilin activity that facilitates HIV-1 infection of transformed and resting CD4 T cells. J Virol 85:9824–9833CrossRefPubMedPubMedCentral
27.
go back to reference Joseph SB, Arrildt KT, Swanstrom AE, Schnell G, Lee B, Hoxie JA, Swanstrom R (2014) Quantification of entry phenotypes of macrophage-tropic HIV-1 across a wide range of CD4 densities. J Virol 88:1858–1869CrossRefPubMedPubMedCentral Joseph SB, Arrildt KT, Swanstrom AE, Schnell G, Lee B, Hoxie JA, Swanstrom R (2014) Quantification of entry phenotypes of macrophage-tropic HIV-1 across a wide range of CD4 densities. J Virol 88:1858–1869CrossRefPubMedPubMedCentral
28.
go back to reference Kolchinsky P, Mirzabekov T, Farzan M, Kiprilov E, Cayabyab M, Mooney LJ, Choe H, Sodroski J (1999) Adaptation of a CCR5-using, primary human immunodeficiency virus type 1 isolate for CD4-independent replication. J Virol 73:8120–8126PubMedPubMedCentral Kolchinsky P, Mirzabekov T, Farzan M, Kiprilov E, Cayabyab M, Mooney LJ, Choe H, Sodroski J (1999) Adaptation of a CCR5-using, primary human immunodeficiency virus type 1 isolate for CD4-independent replication. J Virol 73:8120–8126PubMedPubMedCentral
29.
go back to reference Lane JH, Sasseville VG, Smith MO, Vogel P, Pauley DR, Heyes MP, Lackner AA (1996) Neuroinvasion by simian immunodeficiency virus coincides with increased numbers of perivascular macrophages/microglia and intrathecal immune activation. J Neurovirol 2:423–432CrossRefPubMed Lane JH, Sasseville VG, Smith MO, Vogel P, Pauley DR, Heyes MP, Lackner AA (1996) Neuroinvasion by simian immunodeficiency virus coincides with increased numbers of perivascular macrophages/microglia and intrathecal immune activation. J Neurovirol 2:423–432CrossRefPubMed
30.
go back to reference Lee B, Sharron M, Montaner LJ, Weissman D, Doms RW (1999) Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc Natl Acad Sci USA 96:5215–5220CrossRefPubMed Lee B, Sharron M, Montaner LJ, Weissman D, Doms RW (1999) Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc Natl Acad Sci USA 96:5215–5220CrossRefPubMed
31.
go back to reference Lu S, Manning S, Arthos J (1999) Antigen engineering in DNA immunization. Methods Mol Med (Humana Press Inc, Totowa, NJ) 29:355–374 Lu S, Manning S, Arthos J (1999) Antigen engineering in DNA immunization. Methods Mol Med (Humana Press Inc, Totowa, NJ) 29:355–374
33.
go back to reference McCoy LE, McKnight A (2017) Lessons learned from humoral responses of HIV patients. Curr Opin HIV AIDS 12:195–202CrossRefPubMed McCoy LE, McKnight A (2017) Lessons learned from humoral responses of HIV patients. Curr Opin HIV AIDS 12:195–202CrossRefPubMed
34.
go back to reference McCrossan M, Marsden M, Carnie FW, Minnis S, Hansoti B, Anthony IC, Brettle RP, Bell JE, Simmonds P (2006) An immune control model for viral replication in the CNS during presymptomatic HIV infection. Brain J Neurol 129:503–516CrossRef McCrossan M, Marsden M, Carnie FW, Minnis S, Hansoti B, Anthony IC, Brettle RP, Bell JE, Simmonds P (2006) An immune control model for viral replication in the CNS during presymptomatic HIV infection. Brain J Neurol 129:503–516CrossRef
35.
go back to reference Mori K, Rosenzweig M, Desrosiers RC (2000) Mechanisms for adaptation of simian immunodeficiency virus to replication in alveolar macrophages. J Virol 74:10852–10859CrossRefPubMedPubMedCentral Mori K, Rosenzweig M, Desrosiers RC (2000) Mechanisms for adaptation of simian immunodeficiency virus to replication in alveolar macrophages. J Virol 74:10852–10859CrossRefPubMedPubMedCentral
36.
go back to reference Morner A, Thomas JA, Bjorling E, Munson PJ, Lucas SB, McKnight A (2003) Productive HIV-2 infection in the brain is restricted to macrophages/microglia. AIDS 17:1451–1455CrossRefPubMed Morner A, Thomas JA, Bjorling E, Munson PJ, Lucas SB, McKnight A (2003) Productive HIV-2 infection in the brain is restricted to macrophages/microglia. AIDS 17:1451–1455CrossRefPubMed
37.
go back to reference O’Connell O, Repik A, Reeves JD, Gonzalez-Perez MP, Quitadamo B, Anton ED, Duenas-Decamp M, Peters P, Lin R, Zolla-Pazner S, Corti D, Wallace A, Wang S, Kong XP, Lu S, Clapham PR (2013) Efficiency of bridging-sheet recruitment explains HIV-1 R5 envelope glycoprotein sensitivity to soluble CD4 and macrophage tropism. J Virol 87:187–198CrossRefPubMedPubMedCentral O’Connell O, Repik A, Reeves JD, Gonzalez-Perez MP, Quitadamo B, Anton ED, Duenas-Decamp M, Peters P, Lin R, Zolla-Pazner S, Corti D, Wallace A, Wang S, Kong XP, Lu S, Clapham PR (2013) Efficiency of bridging-sheet recruitment explains HIV-1 R5 envelope glycoprotein sensitivity to soluble CD4 and macrophage tropism. J Virol 87:187–198CrossRefPubMedPubMedCentral
38.
go back to reference O’Doherty U, Swiggard WJ, Malim MH (2000) Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J Virol 74:10074–10080CrossRefPubMedPubMedCentral O’Doherty U, Swiggard WJ, Malim MH (2000) Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J Virol 74:10074–10080CrossRefPubMedPubMedCentral
39.
go back to reference Peters PJ, Bhattacharya J, Hibbitts S, Dittmar MT, Simmons G, Bell J, Simmonds P, Clapham PR (2004) Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J Virol 78:6915–6926CrossRefPubMedPubMedCentral Peters PJ, Bhattacharya J, Hibbitts S, Dittmar MT, Simmons G, Bell J, Simmonds P, Clapham PR (2004) Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J Virol 78:6915–6926CrossRefPubMedPubMedCentral
40.
go back to reference Peters PJ, Sullivan WM, Duenas-Decamp MJ, Bhattacharya J, Ankghuambom C, Brown R, Luzuriaga K, Bell J, Simmonds P, Ball J, Clapham PR (2006) Non-macrophage-tropic human immunodeficiency virus type 1 R5 envelopes predominate in blood, lymph nodes, and semen: implications for transmission and pathogenesis. J Virol 80:6324–6332CrossRefPubMedPubMedCentral Peters PJ, Sullivan WM, Duenas-Decamp MJ, Bhattacharya J, Ankghuambom C, Brown R, Luzuriaga K, Bell J, Simmonds P, Ball J, Clapham PR (2006) Non-macrophage-tropic human immunodeficiency virus type 1 R5 envelopes predominate in blood, lymph nodes, and semen: implications for transmission and pathogenesis. J Virol 80:6324–6332CrossRefPubMedPubMedCentral
41.
go back to reference Peters PJ, Duenas-Decamp MJ, Sullivan WM, Brown R, Ankghuambom C, Luzuriaga K, Robinson J, Burton DR, Bell J, Simmonds P, Ball J, Clapham P (2008) Variation in HIV-1 R5 macrophage-tropism correlates with sensitivity to reagents that block envelope: CD4 interactions but not with sensitivity to other entry inhibitors. Retrovirology 5:5CrossRefPubMedPubMedCentral Peters PJ, Duenas-Decamp MJ, Sullivan WM, Brown R, Ankghuambom C, Luzuriaga K, Robinson J, Burton DR, Bell J, Simmonds P, Ball J, Clapham P (2008) Variation in HIV-1 R5 macrophage-tropism correlates with sensitivity to reagents that block envelope: CD4 interactions but not with sensitivity to other entry inhibitors. Retrovirology 5:5CrossRefPubMedPubMedCentral
42.
go back to reference Puffer BA, Pohlmann S, Edinger AL, Carlin D, Sanchez MD, Reitter J, Watry DD, Fox HS, Desrosiers RC, Doms RW (2002) CD4 independence of simian immunodeficiency virus Envs is associated with macrophage tropism, neutralization sensitivity, and attenuated pathogenicity. J Virol 76:2595–2605CrossRefPubMedPubMedCentral Puffer BA, Pohlmann S, Edinger AL, Carlin D, Sanchez MD, Reitter J, Watry DD, Fox HS, Desrosiers RC, Doms RW (2002) CD4 independence of simian immunodeficiency virus Envs is associated with macrophage tropism, neutralization sensitivity, and attenuated pathogenicity. J Virol 76:2595–2605CrossRefPubMedPubMedCentral
43.
go back to reference Quitadamo B, Peters PJ, Repik A, O’Connell O, Mou Z, Koch M, Somasundaran M, Brody R, Luzuriaga K, Wallace A, Wang S, Lu S, McCauley S, Luban J, Duenas-Decamp M, Gonzalez-Perez MP, Clapham P (2018) HIV-1 R5 macrophage-tropic envelope glycoprotein trimers bind CD4 with high affinity, while the CD4 binding site on non-macrophage-tropic, T- tropic R5 envelopes is occluded. J Virol 92:e00841-17CrossRefPubMedPubMedCentral Quitadamo B, Peters PJ, Repik A, O’Connell O, Mou Z, Koch M, Somasundaran M, Brody R, Luzuriaga K, Wallace A, Wang S, Lu S, McCauley S, Luban J, Duenas-Decamp M, Gonzalez-Perez MP, Clapham P (2018) HIV-1 R5 macrophage-tropic envelope glycoprotein trimers bind CD4 with high affinity, while the CD4 binding site on non-macrophage-tropic, T- tropic R5 envelopes is occluded. J Virol 92:e00841-17CrossRefPubMedPubMedCentral
44.
go back to reference Ranki A, Nyberg M, Ovod V, Haltia M, Elovaara I, Raininko R, Haapasalo H, Krohn K (1995) Abundant expression of HIV Nef and Rev proteins in brain astrocytes in vivo is associated with dementia. AIDS 9:1001–1008CrossRefPubMed Ranki A, Nyberg M, Ovod V, Haltia M, Elovaara I, Raininko R, Haapasalo H, Krohn K (1995) Abundant expression of HIV Nef and Rev proteins in brain astrocytes in vivo is associated with dementia. AIDS 9:1001–1008CrossRefPubMed
45.
go back to reference Reeves JD, Hibbitts S, Simmons G, McKnight A, Azevedo-Pereira JM, Moniz-Pereira J, Clapham PR (1999) Primary human immunodeficiency virus type 2 (HIV-2) isolates infect CD4- negative cells via CCR5 and CXCR4: comparison with HIV-1 and simian immunodeficiency virus and relevance to cell tropism In vivo. J Virol 73:7795–7804PubMedPubMedCentral Reeves JD, Hibbitts S, Simmons G, McKnight A, Azevedo-Pereira JM, Moniz-Pereira J, Clapham PR (1999) Primary human immunodeficiency virus type 2 (HIV-2) isolates infect CD4- negative cells via CCR5 and CXCR4: comparison with HIV-1 and simian immunodeficiency virus and relevance to cell tropism In vivo. J Virol 73:7795–7804PubMedPubMedCentral
46.
go back to reference Roche M, Jakobsen MR, Sterjovski J, Ellett A, Posta F, Lee B, Jubb B, Westby M, Lewin SR, Ramsland PA, Churchill MJ, Gorry PR (2011) HIV-1 escape from the CCR5 antagonist maraviroc associated with an altered and less-efficient mechanism of gp120-CCR5 engagement that attenuates macrophage tropism. J Virol 85:4330–4342CrossRefPubMedPubMedCentral Roche M, Jakobsen MR, Sterjovski J, Ellett A, Posta F, Lee B, Jubb B, Westby M, Lewin SR, Ramsland PA, Churchill MJ, Gorry PR (2011) HIV-1 escape from the CCR5 antagonist maraviroc associated with an altered and less-efficient mechanism of gp120-CCR5 engagement that attenuates macrophage tropism. J Virol 85:4330–4342CrossRefPubMedPubMedCentral
47.
go back to reference Saito Y, Sharer LR, Epstein LG, Michaels J, Mintz M, Louder M, Golding K, Cvetkovich TA, Blumberg BM (1994) Overexpression of nef as a marker for restricted HIV-1 infection of astrocytes in postmortem pediatric central nervous tissues. Neurology 44:474–481CrossRefPubMed Saito Y, Sharer LR, Epstein LG, Michaels J, Mintz M, Louder M, Golding K, Cvetkovich TA, Blumberg BM (1994) Overexpression of nef as a marker for restricted HIV-1 infection of astrocytes in postmortem pediatric central nervous tissues. Neurology 44:474–481CrossRefPubMed
48.
go back to reference Salimi H, Roche M, Webb N, Gray LR, Chikere K, Sterjovski J, Ellett A, Wesselingh SL, Ramsland PA, Lee B, Churchill MJ, Gorry PR (2013) Macrophage-tropic HIV-1 variants from brain demonstrate alterations in the way gp120 engages both CD4 and CCR5. J Leukoc Biol 93:113–126CrossRefPubMedPubMedCentral Salimi H, Roche M, Webb N, Gray LR, Chikere K, Sterjovski J, Ellett A, Wesselingh SL, Ramsland PA, Lee B, Churchill MJ, Gorry PR (2013) Macrophage-tropic HIV-1 variants from brain demonstrate alterations in the way gp120 engages both CD4 and CCR5. J Leukoc Biol 93:113–126CrossRefPubMedPubMedCentral
49.
go back to reference Schnell G, Joseph S, Spudich S, Price RW, Swanstrom R (2011) HIV-1 replication in the central nervous system occurs in two distinct cell types. PLoS Pathog 7:e1002286CrossRefPubMedPubMedCentral Schnell G, Joseph S, Spudich S, Price RW, Swanstrom R (2011) HIV-1 replication in the central nervous system occurs in two distinct cell types. PLoS Pathog 7:e1002286CrossRefPubMedPubMedCentral
50.
go back to reference Sharer LR, Saito Y, Epstein LG, Blumberg BM (1994) Detection of HIV-1 DNA in pediatric AIDS brain tissue by two-step ISPCR. Adv Neuroimmunol 4:283–285CrossRefPubMed Sharer LR, Saito Y, Epstein LG, Blumberg BM (1994) Detection of HIV-1 DNA in pediatric AIDS brain tissue by two-step ISPCR. Adv Neuroimmunol 4:283–285CrossRefPubMed
51.
go back to reference Sterjovski J, Roche M, Churchill MJ, Ellett A, Farrugia W, Gray LR, Cowley D, Poumbourios P, Lee B, Wesselingh SL, Cunningham AL, Ramsland PA, Gorry PR (2010) An altered and more efficient mechanism of CCR5 engagement contributes to macrophage tropism of CCR5-using HIV-1 envelopes. Virology 404:269–278CrossRefPubMedPubMedCentral Sterjovski J, Roche M, Churchill MJ, Ellett A, Farrugia W, Gray LR, Cowley D, Poumbourios P, Lee B, Wesselingh SL, Cunningham AL, Ramsland PA, Gorry PR (2010) An altered and more efficient mechanism of CCR5 engagement contributes to macrophage tropism of CCR5-using HIV-1 envelopes. Virology 404:269–278CrossRefPubMedPubMedCentral
52.
go back to reference 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 39:705–711CrossRefPubMed 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 39:705–711CrossRefPubMed
53.
go back to reference Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRef Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRef
54.
go back to reference Tan Q, Zhu Y, Li J, Chen Z, Han GW, Kufareva I, Li T, Ma L, Fenalti G, Li J, Zhang W, Xie X, Yang H, Jiang H, Cherezov V, Liu H, Stevens RC, Zhao Q, Wu B (2013) Structure of the CCR5 chemokine receptor-HIV entry inhibitor maraviroc complex. Science 341:1387–1390CrossRefPubMed Tan Q, Zhu Y, Li J, Chen Z, Han GW, Kufareva I, Li T, Ma L, Fenalti G, Li J, Zhang W, Xie X, Yang H, Jiang H, Cherezov V, Liu H, Stevens RC, Zhao Q, Wu B (2013) Structure of the CCR5 chemokine receptor-HIV entry inhibitor maraviroc complex. Science 341:1387–1390CrossRefPubMed
55.
go back to reference Thomas ER, Shotton C, Weiss RA, Clapham PR, McKnight A (2003) CD4-dependent and CD4-independent HIV-2: consequences for neutralization. AIDS 17:291–300CrossRefPubMed Thomas ER, Shotton C, Weiss RA, Clapham PR, McKnight A (2003) CD4-dependent and CD4-independent HIV-2: consequences for neutralization. AIDS 17:291–300CrossRefPubMed
56.
go back to reference Tornatore C, Chandra R, Berger JR, Major EO (1994) HIV-1 infection of subcortical astrocytes in the pediatric central nervous system. Neurology 44:481–487CrossRefPubMed Tornatore C, Chandra R, Berger JR, Major EO (1994) HIV-1 infection of subcortical astrocytes in the pediatric central nervous system. Neurology 44:481–487CrossRefPubMed
57.
go back to reference Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, Saag MS, Wu X, Shaw GM, Kappes JC (2002) Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46:1896–1905CrossRefPubMedPubMedCentral Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, Saag MS, Wu X, Shaw GM, Kappes JC (2002) Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46:1896–1905CrossRefPubMedPubMedCentral
58.
go back to reference Wilen CB, Tilton JC, Doms RW (2012) Molecular mechanisms of HIV entry. Adv Exp Med Biol 726:223–242CrossRefPubMed Wilen CB, Tilton JC, Doms RW (2012) Molecular mechanisms of HIV entry. Adv Exp Med Biol 726:223–242CrossRefPubMed
60.
go back to reference Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, deBakker C, Alvarez X, Lackner AA (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 193:905–915CrossRefPubMedPubMedCentral Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, deBakker C, Alvarez X, Lackner AA (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 193:905–915CrossRefPubMedPubMedCentral
61.
go back to reference Yen PJ, Mefford ME, Hoxie JA, Williams KC, Desrosiers RC, Gabuzda D (2014) Identification and characterization of a macrophage-tropic SIV envelope glycoprotein variant in blood from early infection in SIVmac251-infected macaques. Virology 458–459:53–68CrossRefPubMed Yen PJ, Mefford ME, Hoxie JA, Williams KC, Desrosiers RC, Gabuzda D (2014) Identification and characterization of a macrophage-tropic SIV envelope glycoprotein variant in blood from early infection in SIVmac251-infected macaques. Virology 458–459:53–68CrossRefPubMed
62.
go back to reference Zhuang K, Leda AR, Tsai L, Knight H, Harbison C, Gettie A, Blanchard J, Westmoreland S, Cheng-Mayer C (2014) Emergence of CD4 independence envelopes and astrocyte infection in R5 simian-human immunodeficiency virus model of encephalitis. J Virol 88:8407–8420CrossRefPubMedPubMedCentral Zhuang K, Leda AR, Tsai L, Knight H, Harbison C, Gettie A, Blanchard J, Westmoreland S, Cheng-Mayer C (2014) Emergence of CD4 independence envelopes and astrocyte infection in R5 simian-human immunodeficiency virus model of encephalitis. J Virol 88:8407–8420CrossRefPubMedPubMedCentral
Metadata
Title
No detection of CD4-independent human immunodeficiency virus 1 envelope glycoproteins in brain tissue of patients with or without neurological complications
Authors
Briana Quitadamo
Paul J. Peters
Matthew Koch
Katherine Luzuriaga
Cecilia Cheng-Mayer
Paul R. Clapham
Maria Paz Gonzalez-Perez
Publication date
01-02-2019
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 2/2019
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-018-4094-1

Other articles of this Issue 2/2019

Archives of Virology 2/2019 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.