Characterization of HIV variants from paired Cerebrospinal fluid and Plasma samples in primary microglia and CD4
CSF
Compartmentalization
HIV
Microglia
Plasma
Journal
Journal of neurovirology
ISSN: 1538-2443
Titre abrégé: J Neurovirol
Pays: United States
ID NLM: 9508123
Informations de publication
Date de publication:
07 May 2024
07 May 2024
Historique:
received:
25
06
2023
accepted:
03
04
2024
revised:
30
03
2024
medline:
7
5
2024
pubmed:
7
5
2024
entrez:
7
5
2024
Statut:
aheadofprint
Résumé
Despite antiretroviral therapy (ART), HIV persistence in the central nervous system (CNS) continues to cause a range of cognitive impairments in people living with HIV (PLWH). Upon disease progression, transmigrating CCR5-using T-cell tropic viruses are hypothesized to evolve into macrophage-tropic viruses in the CNS that can efficiently infect low CD4-expressing cells, such as microglia. We examined HIV-1 RNA concentration, co-receptor usage, and CSF compartmentalization in paired CSF and blood samples from 19 adults not on treatment. Full-length envelope CSF- and plasma-derived reporter viruses were generated from 3 subjects and phenotypically characterized in human primary CD4
Identifiants
pubmed: 38713307
doi: 10.1007/s13365-024-01207-w
pii: 10.1007/s13365-024-01207-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Aidsfonds
ID : P-13204
Organisme : Aidsfonds
ID : P-37203
Informations de copyright
© 2024. The Author(s).
Références
Arrildt KT, LaBranche CC, Joseph SB, Dukhovlinova EN, Graham WD, Ping LH, Schnell G, Sturdevant CB, Kincer LP, Mallewa M, Heyderman RS, Van Rie A, Cohen MS, Spudich S, Price RW, Montefiori DC, Swanstrom R (2015) Phenotypic correlates of HIV-1 macrophage tropism. J Virol 89:11294–11311. https://doi.org/10.1128/jvi.00946-15
doi: 10.1128/jvi.00946-15
pubmed: 26339058
pmcid: 4645658
Bai F, Iannuzzi F, Merlini E, Borghi L, Tincati C, Trunfio M, Bini T, d’Arminio Monforte A, Marchetti G (2017) Clinical and viro-immunological correlates of HIV associated neurocognitive disorders (HAND) in a cohort of antiretroviral-naïve HIV-infected patients. AIDS 31:311–314. https://doi.org/10.1097/QAD.0000000000001346
doi: 10.1097/QAD.0000000000001346
pubmed: 28005574
Bednar MM, Sturdevant CB, Tompkins LA, Arrildt KT, Dukhovlinova E, Kincer LP, Swanstrom R (2015) Compartmentalization, viral evolution, and viral latency of HIV in the CNS. Curr HIV/AIDS Rep 12:262–271. https://doi.org/10.1007/s11904-015-0265-9
doi: 10.1007/s11904-015-0265-9
pubmed: 25914150
pmcid: 4431548
Boom R, Sol JA, Salimans MMM, Jansen CL, Wertheim-Van Dillen PME, Van Der Noordaa J (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28:495–503
doi: 10.1128/jcm.28.3.495-503.1990
pubmed: 1691208
pmcid: 269651
Borrajo A, Svicher V, Salpini R, Pellegrino M, Aquaro S (2021) Crucial role of central nervous system as a viral anatomical compartment for hiv-1 infection. Microorganisms 9:2537. https://doi.org/10.3390/microorganisms9122537
doi: 10.3390/microorganisms9122537
pubmed: 34946138
pmcid: 8705402
Brese RL, Gonzalez-Perez MP, Koch M, O’Connell O, Luzuriaga K, Somasundaran M, Clapham PR, Dollar JJ, Nolan DJ, Rose R, Lamers SL (2018) Ultradeep single-molecule real-time sequencing of HIV envelope reveals complete compartmentalization of highly macrophage-tropic R5 proviral variants in brain and CXCR4-using variants in immune and peripheral tissues. J Neurovirol 24:439–453. https://doi.org/10.1007/s13365-018-0633-5
doi: 10.1007/s13365-018-0633-5
pubmed: 29687407
pmcid: 7281851
Chan P, Spudich S (2022) HIV compartmentalization in the CNS and its impact in treatment outcomes and cure strategies. Curr HIV/AIDS Rep 19:207–216. https://doi.org/10.1007/s11904-022-00605-1
doi: 10.1007/s11904-022-00605-1
pubmed: 35536438
pmcid: 10590959
Clifford DB, Ances BM (2013) HIV-associated neurocognitive disorder. Lancet Infect Dis 13:976–986
doi: 10.1016/S1473-3099(13)70269-X
pubmed: 24156898
pmcid: 4108270
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 83:2575–2583. https://doi.org/10.1128/jvi.02133-08
doi: 10.1128/jvi.02133-08
pubmed: 19129457
pmcid: 2648272
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. PNAS 103:15160–15165
doi: 10.1073/pnas.0605513103
pubmed: 17015824
pmcid: 1586182
Dunfee RL, Thomas ER, Wang J, Kunstman K, Wolinsky SM, Gabuzda D (2007) Loss of the N-linked glycosylation site at position 386 in the HIV envelope V4 region enhances macrophage tropism and is associated with dementia. Virology 367:222–234. https://doi.org/10.1016/j.virol.2007.05.029
doi: 10.1016/j.virol.2007.05.029
pubmed: 17599380
Gartner S, Markovits P, Markovitz DM, Kaplan MH (1986) The role of mononuclear phagocytes in HTLV-III/LAV infection. Science 233:215–219. https://doi.org/10.1126/science.3014648
doi: 10.1126/science.3014648
pubmed: 3014648
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 9:20. https://doi.org/10.1186/1742-4690-9-20
doi: 10.1186/1742-4690-9-20
pubmed: 22420378
pmcid: 3362761
Gumbs SBH, Kübler R, Gharu L, Schipper PJ, Borst AL, Snijders GJLJ, Ormel PR, van Berlekom AB, Wensing AMJ, de Witte LD, Nijhuis M (2022) Human microglial models to study HIV infection and neuropathogenesis: a literature overview and comparative analyses. J Neurovirol 28:64–91. https://doi.org/10.1007/s13365-021-01049-w
doi: 10.1007/s13365-021-01049-w
pubmed: 35138593
pmcid: 9076745
Han M, Cantaloube-Ferrieu V, Xie M, Armani-Tourret M, Woottum M, Pagès JC, Colin P, Lagane B, Benichou S (2022) HIV-1 cell-to-cell spread overcomes the virus entry block of non-macrophage-tropic strains in macrophages. PLoS Pathog 18(5):e1010335. https://doi.org/10.1371/journal.ppat.1010335
doi: 10.1371/journal.ppat.1010335
pubmed: 35622876
pmcid: 9182568
Heaton RK, Clifford DB, Franklin DR, Woods BSP, Ake PC, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Rivera-Mindt M, Vigil OR, Taylor MJ, Collier AC, Marra CM, Gelman BB, Mcarthur JC, Morgello MS, Simpson DM, Grant I (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy CHARTER Study. Neurology 75:2087–2096
doi: 10.1212/WNL.0b013e318200d727
pubmed: 21135382
pmcid: 2995535
Hudson RR (2000) A New Statistic for detecting genetic differentiation. Genetics 155:2011–2014
doi: 10.1093/genetics/155.4.2011
pubmed: 10924493
pmcid: 1461195
Hudson RR, Slatkint M, Maddison WP (1992) Estimation of levels of Gene Flow from DNA sequence data. Genetics 132:583–589
doi: 10.1093/genetics/132.2.583
pubmed: 1427045
pmcid: 1205159
Jadhav S, Nema V (2021) HIV-Associated neurotoxicity: the interplay of host and viral proteins. Mediators Inflamm. https://doi.org/10.1155/2021/1267041
doi: 10.1155/2021/1267041
pubmed: 34483726
pmcid: 8410439
Joseph SB, Swanstrom R (2018) The evolution of HIV-1 entry phenotypes as a guide to changing target cells. J Leukoc Biol 103:421–431. https://doi.org/10.1002/JLB.2RI0517-200R
doi: 10.1002/JLB.2RI0517-200R
pubmed: 29389021
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 88:1858–1869. https://doi.org/10.1128/jvi.02477-13
doi: 10.1128/jvi.02477-13
pubmed: 24307580
pmcid: 3911544
Joseph SB, Arrildt KT, Sturdevant CB, Swanstrom R (2015) HIV-1 target cells in the CNS. J Neurovirol 21:276–289. https://doi.org/10.1007/s13365-014-0287-x
doi: 10.1007/s13365-014-0287-x
pubmed: 25236812
Katoh K, Rozewicki J, Yamada KD (2018) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108
doi: 10.1093/bib/bbx108
Ko A, Kang G, Hattler JB, Galadima HI, Zhang J, Li Q, Kim WK (2019) Macrophages but not astrocytes Harbor HIV DNA in the brains of HIV-1-Infected aviremic individuals on suppressive antiretroviral therapy. J Neuroimmune Pharmacol 14:110–119. https://doi.org/10.1007/s11481-018-9809-2
doi: 10.1007/s11481-018-9809-2
pubmed: 30194646
Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679. https://doi.org/10.1093/bioinformatics/bti079
doi: 10.1093/bioinformatics/bti079
Lamers SL, Rose R, Maidji E, Agsalda-Garcia M, Nolan DJ, Fogel GB, Salemi M, Garcia DL, Bracci P, Yong W, Commins D, Said J, Khanlou N, Hinkin CH, Sueiras MV, Mathisen G, Donovan S, Shiramizu B, Stoddart CA, Singer EJ (2016) HIV DNA is frequently present within Pathologic Tissues Evaluated at autopsy from combined antiretroviral therapy-treated patients with undetectable viral loads. J Virol 90:8968–8983. https://doi.org/10.1128/jvi.00674-16
doi: 10.1128/jvi.00674-16
pubmed: 27466426
pmcid: 5044815
Li Y, Kappes JC, Conway JA, Price RW, Shaw GM, Hahn BH (1991) 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 65:3973–3985
doi: 10.1128/jvi.65.8.3973-3985.1991
pubmed: 1830110
pmcid: 248827
López-Huertas MR, Jiménez-Tormo L, Madrid-Elena N, Gutiérrez C, Vivancos MJ, Luna L, Moreno S (2020) Maraviroc reactivates HIV with potency similar to that of other latency reversing drugs without inducing toxicity in CD8 T cells. Biochem Pharmacol 182:114231. https://doi.org/10.1016/j.bcp.2020.114231
doi: 10.1016/j.bcp.2020.114231
pubmed: 32979351
Madrid-Elena N, Laura García-Bermejo M, Serrano-Villar S, Díaz-De Santiago A, Sastre B, Gutiérrez C, Dronda F, Díaz MC, Domínguez E, Rosa López-Huertas M, Hernández-Novoa B, Moreno S (2018) Maraviroc is Associated with latent HIV-1 reactivation through NF-B activation in resting CD4 T cells from HIV-Infected individuals on suppressive antiretroviral therapy. J Virol 92:e01931–e01917. https://doi.org/10.1128/JVI.01931-17
doi: 10.1128/JVI.01931-17
pubmed: 29444937
pmcid: 5899181
Mattei D, Ivanov A, van Oostrum M, Pantelyushin S, Richetto J, Mueller F, Beffinger M, Schellhammer L, vom Berg J, Wollscheid B, Beule D, Paolicelli RC, Meyer U (2020) Enzymatic dissociation induces transcriptional and proteotype bias in brain cell populations. Int J Mol Sci 21:1–20. https://doi.org/10.3390/ijms21217944
doi: 10.3390/ijms21217944
Musich T, Peters PJ, Duenas-Decamp MJ, Gonzalez-Perez MP, Robinson J, Zolla-Pazner S, Ball JK, Luzuriaga K, Clapham PR (2011) A conserved determinant in the V1 Loop of HIV-1 modulates the V3 Loop to Prime low CD4 use and macrophage infection. J Virol 85:2397–2405. https://doi.org/10.1128/jvi.02187-10
doi: 10.1128/jvi.02187-10
pubmed: 21159865
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:e1002286. https://doi.org/10.1371/journal.ppat.1002286
doi: 10.1371/journal.ppat.1002286
pubmed: 22007152
pmcid: 3188520
Slatkin M, Maddison WP (1989) A cladistic measure of Gene Flow inferred from the phylogenies of alleles. Genetics 123:603–613
doi: 10.1093/genetics/123.3.603
pubmed: 2599370
pmcid: 1203833
Sturdevant CB, Dow A, Jabara CB, Joseph SB, Schnell G, Takamune N, Mallewa M, Heyderman RS, Van Rie A, Swanstrom R (2012) Central Nervous System compartmentalization of HIV-1 subtype C variants early and late in infection in Young Children. PLoS Pathog 8:e1003094. https://doi.org/10.1371/journal.ppat.1003094
doi: 10.1371/journal.ppat.1003094
pubmed: 23300446
pmcid: 3531524
Sturdevant CB, Joseph SB, Schnell G, Price RW, Swanstrom R, Spudich S (2015) Compartmentalized replication of R5 T cell-tropic HIV-1 in the Central Nervous System early in the course of infection. PLoS Pathog 11:1–24. https://doi.org/10.1371/journal.ppat.1004720
doi: 10.1371/journal.ppat.1004720
Swenson LC, Mo T, Dong WWY, Zhong X, Woods CK, Jensen MA, Thielen A, Chapman D, Lewis M, James I, Heera J, Valdez H, Harrigan PR (2011) Deep sequencing to infer HIV-1 co-receptor usage: application to three clinical trials of maraviroc in treatment-experienced patients. J Infect Dis 203:237–245. https://doi.org/10.1093/infdis/jiq030
doi: 10.1093/infdis/jiq030
pubmed: 21288824
pmcid: 3071057
Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
doi: 10.1093/molbev/msab120
pubmed: 33892491
pmcid: 8233496
Tso FY, Kang G, Kwon EH, Julius P, Li Q, West JT, Wood C (2018) Brain is a potential sanctuary for subtype C HIV-1 irrespective of ART treatment outcome. PLoS ONE 13:e0201325. https://doi.org/10.1371/journal.pone.0201325
doi: 10.1371/journal.pone.0201325
pubmed: 30040863
pmcid: 6057662
Ulfhammer G, Edén A, Antinori A, Brew BJ, Calcagno A, Cinque P, De Zan V, Hagberg L, Lin A, Nilsson S, Oprea C, Pinnetti C, Spudich S, Trunfio M, Winston A, Price RW, Gisslén M (2022) Cerebrospinal fluid viral load across the spectrum of untreated human immunodeficiency virus type 1 (HIV-1) infection: a cross-sectional Multicenter Study. Clin Infect Dis 75:493–502. https://doi.org/10.1093/cid/ciab943
doi: 10.1093/cid/ciab943
pubmed: 34747481
Valcour V, Chalermchai T, Sailasuta N, Marovich M, Lerdlum S, Suttichom D, Suwanwela NC, Jagodzinski L, Michael N, Spudich S, Van Griensven F, De Souza M, Kim J, Ananworanich J (2012) Central nervous system viral invasion and inflammation during acute HIV infection. J Infect Dis 206:275–282. https://doi.org/10.1093/infdis/jis326
doi: 10.1093/infdis/jis326
pubmed: 22551810
pmcid: 3490695
Wallet C, De Rovere M, Van Assche J, Daouad F, De Wit S, Gautier V, Mallon PWG, Marcello A, Van Lint C, Rohr O, Schwartz C (2019) Microglial cells: the Main HIV-1 Reservoir in the brain. Front Cell Infect Microbiol 9:362. https://doi.org/10.3389/fcimb.2019.00362
doi: 10.3389/fcimb.2019.00362
pubmed: 31709195
pmcid: 6821723
Wang Y, Liu M, Lu Q, Farrell M, Lappin JM, Shi J, Lu L, Bao Y (2020) Global prevalence and burden of HIV-associated neurocognitive disorder: a meta-analysis. Neurology 95:E2610–E2621. https://doi.org/10.1212/WNL.0000000000010752
doi: 10.1212/WNL.0000000000010752
pubmed: 32887786
Woodburn BM, Kanchi K, Zhou S, Colaianni N, Joseph SB, Swanstrom R (2022) Characterization of macrophage-tropic HIV-1 infection of Central Nervous System cells and the influence of inflammation. J Virol. https://doi.org/10.1128/jvi.00957-22
doi: 10.1128/jvi.00957-22
pubmed: 35975998
pmcid: 9472603
Zárate S, Pond SLK, Shapshak P, Frost SDW (2007) Comparative study of methods for detecting sequence compartmentalization in human immunodeficiency virus type 1. J Virol 81:6643–6651. https://doi.org/10.1128/jvi.02268-06
doi: 10.1128/jvi.02268-06
pubmed: 17428864
pmcid: 1900087