Human immunodeficiency virus transmission-Mechanisms underlying the cell-to-cell spread of human immunodeficiency virus.
HIV
HIV-cell interactions
cell-to-cell spread
pathogenesis
Journal
Reviews in medical virology
ISSN: 1099-1654
Titre abrégé: Rev Med Virol
Pays: England
ID NLM: 9112448
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
revised:
25
08
2023
received:
29
06
2023
accepted:
04
09
2023
medline:
6
11
2023
pubmed:
12
9
2023
entrez:
12
9
2023
Statut:
ppublish
Résumé
Despite the success of combined antiretroviral therapy in controlling viral load and reducing the risk of human immunodeficiency virus (HIV) transmission, an estimated 1.5 million new infections occurred worldwide in 2021. These new infections are mainly the result of sexual intercourse and thus involve cells present on the genital mucosa, such as dendritic cells (DCs), macrophages (Mø) and CD4+ T lymphocytes. Understanding the mechanisms by which HIV interacts with these cells and how HIV exploits these interactions to establish infection in a new human host is critical to the development of strategies to prevent and control HIV transmission. In this review, we explore how HIV has evolved to manipulate some of the physiological roles of these cells, thereby gaining access to strategic cellular niches that are critical for the spread and pathogenesis of HIV infection. The interaction of HIV with DCs, Mø and CD4+ T lymphocytes, and the role of the intercellular transfer of viral particles through the establishment of the infectious or virological synapses, but also through membrane protrusions such as filopodia and tunnelling nanotubes (TNTs), and cell fusion or cell engulfment processes are presented and discussed.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2480Subventions
Organisme : Fundação para a Ciência e a Tecnologia
Organisme : Gilead Sciences
Organisme : ADEIM - Associação para o Desenvolvimento do Ensino e Investigação em Microbiologia
Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Shattock RJ, Moore JP. Inhibiting sexual transmission of HIV-1 infection. Nat Rev Microbiol. 2003;1(1):25-34. https://doi.org/10.1038/nrmicro729
Haase AT. Targeting early infection to prevent HIV-1 mucosal transmission. Nature. 2010;464(7286):217-223. https://doi.org/10.1038/nature08757
Nguyen N, Holodniy M. HIV infection in the elderly. Clin Interv Aging. 2008;3(3):453-472. https://doi.org/10.2147/cia.s2086
Burgener A, McGowan I, Klatt NR. HIV and mucosal barrier interactions: consequences for transmission and pathogenesis. Review. Curr Opin Immunol. 2015/10/01/ 2015;36:22-30. https://doi.org/10.1016/j.coi.2015.06.004
UNAIDS. 2022. Data 2022. https://www.unaids.org/sites/default/files/media_asset/2022-global-aids-update-summary_en.pdf
UNAIDS. 2021. Data 2021. https://www.unaids.org/en/resources/documents/2021/2021_unaids_data
Kaul R, Cohen CR, Chege D, et al. Biological factors that may contribute to regional and racial disparities in HIV prevalence. Am J Reprod Immunol. 2011;65(3):317-324. https://doi.org/10.1111/j.1600-0897.2010.00962.x
Shen R, Richter HE, Smith PD. Interactions between HIV-1 and mucosal cells in the female reproductive tract. Am J Reprod Immunol. 2014;71(6):608-617. https://doi.org/10.1111/aji.12244
Margolis L, Shattock R. Selective transmission of CCR5-utilizing HIV-1: the 'gatekeeper' problem resolved? Nat Rev Microbiol. 2006/04/01 2006;4(4):312-317. https://doi.org/10.1038/nrmicro1387
Fletcher PS, Elliott J, Grivel J.-C, et al. Ex vivo culture of human colorectal tissue for the evaluation of candidate microbicides. AIDS. 2006;20(9):1237-1245. https://doi.org/10.1097/01.aids.0000232230.96134.80
Miller CJ, Shattock RJ. Target cells in vaginal HIV transmission. Microbes Infect. 2003;5(1):59-67. https://doi.org/10.1016/s1286-4579(02)00056-4
Pudney J, Quayle AJ, Anderson DJ. Immunological microenvironments in the human vagina and cervix: mediators of cellular immunity are concentrated in the cervical transformation Zone1. Biol Reprod. 2005;73(6):1253-1263. https://doi.org/10.1095/biolreprod.105.043133
Patel P, Borkowf CB, Brooks JT, Lasry A, Lansky A, Mermin J. Estimating per-act HIV transmission risk: a systematic review. AIDS. 2014;28(10):1509-1519. https://doi.org/10.1097/qad.0000000000000298
Mykhalovskiy E, Betteridge G, McLay D. Research on the risk of the sexual transmission of HIV infection and on HIV as a chronic manageable infection. Ontario HIV treatment Network. 2013.
Boily MC, Baggaley RF, Wang L, et al. Heterosexual risk of HIV-1 infection per sexual act: systematic review and meta-analysis of observational studies. Lancet Infect Dis. 2009;9(2):118-129. https://doi.org/10.1016/s1473-3099(09)70021-0
Yasen A, Herrera R, Rosbe K, Lien K, Tugizov SM. Release of HIV-1 sequestered in the vesicles of oral and genital mucosal epithelial cells by epithelial-lymphocyte interaction. PLOS Pathog. 2017;13(2):e1006247. https://doi.org/10.1371/journal.ppat.1006247
Neidleman JA, Chen JC, Kohgadai N, et al. Mucosal stromal fibroblasts markedly enhance HIV infection of CD4+ T cells. PLOS Pathog. 2017;13(2):e1006163. https://doi.org/10.1371/journal.ppat.1006163
Murakami T, Kim J, Li Y, Green GE, Shikanov A, Ono A. Secondary lymphoid organ fibroblastic reticular cells mediate trans-infection of HIV-1 via CD44-hyaluronan interactions. Nat Commun. 2018/06/22 2018;9(1):2436. https://doi.org/10.1038/s41467-018-04846-w
Egedal JH, Xie G, Packard TA, et al. Hyaluronic acid is a negative regulator of mucosal fibroblast-mediated enhancement of HIV infection. Mucosal Immunol. 2021;14(5):1203-1213. https://doi.org/10.1038/s41385-021-00409-3
Pique C, Jones K. Pathways of cell-cell transmission of HTLV-1. Review. Front Microbiol. 2012;3. https://doi.org/10.3389/fmicb.2012.00378
Tugizov S. Human immunodeficiency virus-associated disruption of mucosal barriers and its role in HIV transmission and pathogenesis of HIV/AIDS disease. Tissue Barriers. 2016;4(3):e1159276. https://doi.org/10.1080/21688370.2016.1159276
Doncel GF, Anderson S, Zalenskaya I. Role of semen in modulating the female genital tract microenvironment - implications for HIV transmission. Am J Reprod Immunol. 2014;71(6):564-574. https://doi.org/10.1111/aji.12231
Vitali D, Wessels JM, Kaushic C. Role of sex hormones and the vaginal microbiome in susceptibility and mucosal immunity to HIV-1 in the female genital tract. AIDS Res Ther. 2017/09/12 2017;14(1):39. https://doi.org/10.1186/s12981-017-0169-4
Patterson BK, Landay A, Siegel JN, et al. Susceptibility to human immunodeficiency virus-1 infection of human foreskin and cervical tissue grown in explant culture. Am J Pathol. 2002;161(3):867-873. https://doi.org/10.1016/s0002-9440(10)64247-2
Donoval BA, Landay AL, Moses S, et al. HIV-1 target cells in foreskins of African men with varying histories of sexually transmitted infections. Am J Clin Pathol. 2006;125(3):386-391. https://doi.org/10.1309/jvhqvdjdykm58eph
Zhou Z, Barry De Longchamps N, Schmitt A, et al. HIV-1 efficient entry in inner foreskin is mediated by elevated CCL5/RANTES that recruits T cells and fuels conjugate formation with Langerhans cells. PLoS Pathog. 2011;7(6):e1002100. https://doi.org/10.1371/journal.ppat.1002100
Liu A, Yang Y, Liu L, et al. Differential compartmentalization of HIV-targeting immune cells in inner and outer foreskin tissue. PLOS ONE. 2014;9(1):e85176. https://doi.org/10.1371/journal.pone.0085176
Ganor Y, Zhou Z, Bodo J, et al. The adult penile urethra is a novel entry site for HIV-1 that preferentially targets resident urethral macrophages. Mucosal Immunol. 2013/07/01 2013;6(4):776-786. https://doi.org/10.1038/mi.2012.116
McCoombe SG, Short RV. Potential HIV-1 target cells in the human penis. AIDS. 2006;20(11):1491-1495. https://doi.org/10.1097/01.aids.0000237364.11123.98
Hirbod T, Bailey RC, Agot K, et al. Abundant expression of HIV target cells and C-type lectin receptors in the foreskin tissue of young Kenyan men. Am J Pathology. 2010/06/01/ 2010;176(6):2798-2805. https://doi.org/10.2353/ajpath.2010.090926
Sennepin A, Real F, Duvivier M, et al. The human penis is a genuine immunological effector site. Original research. Front Immunol. 2017;8. https://doi.org/10.3389/fimmu.2017.01732
Pudney J, Anderson DJ. Immunobiology of the human penile urethra. Am J Pathol. 1995;147(1):155-165.
Wawer MJ, Gray RH, Sewankambo NK, et al. Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis. 2005;191(9):1403-1409. https://doi.org/10.1086/429411
Quinn TC. Circumcision and HIV transmission. Curr Opin Infect Dis. 2007;20(1):33-38. https://doi.org/10.1097/QCO.0b013e328012c5bc
Mills E, Cooper C, Anema A, Guyatt G. Male circumcision for the prevention of heterosexually acquired HIV infection: a meta-analysis of randomized trials involving 11 050 men. HIV Med. 2008;9(6):332-335. https://doi.org/10.1111/j.1468-1293.2008.00596.x
Dinh MH, Anderson MR, McRaven MD, et al. Visualization of HIV-1 interactions with penile and foreskin epithelia: clues for female-to-male HIV transmission. PLOS Pathog. 2015;11(3):e1004729. https://doi.org/10.1371/journal.ppat.1004729
Bomsel M. Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat Med. 1997/01/01 1997;3(1):42-47. https://doi.org/10.1038/nm0197-42
Tugizov SM, Herrera R, Veluppillai P, et al. HIV is inactivated after transepithelial migration via adult oral epithelial cells but not fetal epithelial cells. Virology. 2011/01/20/ 2011;409(2):211-222. https://doi.org/10.1016/j.virol.2010.10.004
Bobardt Michael D, Chatterji U, Selvarajah S, et al. Cell-free human immunodeficiency virus type 1 transcytosis through primary genital epithelial cells. J Virol. 2007/01/01 2007;81(1):395-405. https://doi.org/10.1128/JVI.01303-06
Herrera R, Morris M, Rosbe K, Feng Z, Weinberg A, Tugizov S. Human beta-defensins 2 and -3 cointernalize with human immunodeficiency virus via heparan sulfate proteoglycans and reduce infectivity of intracellular virions in tonsil epithelial cells. Virology. 2016/01/01/ 2016;487:172-187. https://doi.org/10.1016/j.virol.2015.09.025
Alfsen A, Bomsel M. HIV-1 gp41 envelope residues 650-685 exposed on native virus act as a lectin to bind epithelial cell galactosyl ceramide. J Biol Chem. 2002/07/12/ 2002;277(28):25649-25659. https://doi.org/10.1074/jbc.M200554200
Meng G, Wei X, Wu X, et al. Primary intestinal epithelial cells selectively transfer R5 HIV-1 to CCR5+ cells. Nat Med. 2002/02/01 2002;8(2):150-156. https://doi.org/10.1038/nm0202-150
Dorosko Stephanie M, Connor Ruth I. Primary human mammary epithelial cells endocytose HIV-1 and facilitate viral infection of CD4+ T lymphocytes. J Virol. 2010/10/15 2010;84(20):10533-10542. https://doi.org/10.1128/JVI.01263-10
Nazli A, Chan O, Dobson-Belaire WN, et al. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLOS Pathog. 2010;6(4):e1000852. https://doi.org/10.1371/journal.ppat.1000852
Sufiawati I, Tugizov SM. HIV-associated disruption of tight and adherens junctions of oral epithelial cells facilitates HSV-1 infection and spread. PLOS ONE. 2014;9(2):e88803. https://doi.org/10.1371/journal.pone.0088803
Pope M, Haase AT. Transmission, acute HIV-1 infection and the quest for strategies to prevent infection. Nat Med. 2003/07/01 2003;9(7):847-852. https://doi.org/10.1038/nm0703-847
Dayanithi G, Yahi N, Baghdiguian S, Fantini J. Intracellular calcium release induced by human immunodeficiency virus type 1 (HIV-1) surface envelope glycoprotein in human intestinal epithelial cells: a putative mechanism for HIV-1 enteropathy. Cell Calcium. 1995/07/01/ 1995;18(1):9-18. https://doi.org/10.1016/0143-4160(95)90041-1
Pu H, Tian J, Andras IE, et al. HIV-1 tat protein-induced alterations of ZO-1 expression are mediated by redox-regulated ERK1/2 activation. J Cerebr Blood Flow Metabol. 2005/10/01 2005;25(10):1325-1335. https://doi.org/10.1038/sj.jcbfm.9600125
Nazli A, Kafka JK, Ferreira VH, et al. HIV-1 gp120 induces TLR2-and TLR4-mediated innate immune activation in human female genital epithelium. J Immunol. 2013;191(8):4246-4258. https://doi.org/10.4049/jimmunol.1301482
Bojarski C, Weiske J, Schöneberg T, et al. The specific fates of tight junction proteins in apoptotic epithelial cells. J Cell Sci. 2004;117(10):2097-2107. https://doi.org/10.1242/jcs.01071
Dutartre H, Clavière M, Journo C, Mahieux R. Cell-free versus cell-to-cell infection by human immunodeficiency virus type 1 and human T-lymphotropic virus type 1: exploring the link among viral source, viral trafficking, and viral replication. J Virol. 2016;90(17):7607-7617. https://doi.org/10.1128/JVI.00407-16
Chen P, Hübner W, Spinelli MA, Chen BK. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J Virol. 2007;81(22):12582-12595. https://doi.org/10.1128/JVI.00381-07
Abela IA, Berlinger L, Schanz M, et al. Cell-cell transmission enables HIV-1 to evade inhibition by potent CD4bs directed antibodies. PLoS Pathog. 2012;8(4):e1002634. https://doi.org/10.1371/journal.ppat.1002634
Jolly C, Booth Nicola J, Neil Stuart JD. Cell-cell spread of human immunodeficiency virus type 1 overcomes tetherin/BST-2-mediated restriction in T cells. J Virol. 2010/12/01 2010;84(23):12185-12199. https://doi.org/10.1128/JVI.01447-10
Casartelli N, Sourisseau M, Feldmann J, et al. Tetherin restricts productive HIV-1 cell-to-cell transmission. PLoS Pathog. 2010;6(6):e1000955. https://doi.org/10.1371/journal.ppat.1000955
Richardson MW, Carroll RG, Stremlau M, et al. Mode of transmission affects the sensitivity of human immunodeficiency virus type 1 to restriction by rhesus TRIM5alpha. J Virol. 2008;82(22):11117-11128. https://doi.org/10.1128/JVI.01046-08
Chen P, Hübner W, Spinelli MA, Chen BK. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J Virol. 2007;81(22):12582-12595. https://doi.org/10.1128/jvi.00381-07
Iwami S, Takeuchi JS, Nakaoka S, et al. Cell-to-cell infection by HIV contributes over half of virus infection. Elife. 2015/10/06 2015;4:e08150. https://doi.org/10.7554/eLife.08150
Calado M, Pires D, Conceição C, et al. Cell-to-Cell transmission of HIV-1 and HIV-2 from infected macrophages and dendritic cells to CD4+ T lymphocytes. Viruses. 2023;15(5):1030. https://doi.org/10.3390/v15051030
Sigal A, Kim JT, Balazs AB, et al. Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy. Nature. 2011;477(7362):95-98. https://doi.org/10.1038/nature10347
Clapham PR, McKnight Á. Cell surface receptors, virus entry and tropism of primate lentiviruses. J Gen Virol. 2002;83(Pt 8):1809-1829. https://doi.org/10.1099/0022-1317-83-8-1809
Calado M, Matoso P, Santos-Costa Q, et al. Coreceptor usage by HIV-1 and HIV-2 primary isolates: the relevance of CCR8 chemokine receptor as an alternative coreceptor. Virology. 2010;408(2):174-182. https://doi.org/10.1016/j.virol.2010.09.020
Jolly C, Kashefi K, Hollinshead M, Sattentau QJ. HIV-1 cell to cell transfer across an env-induced, actin-dependent synapse. J Exp Med. 2004;199(2):283-293. https://doi.org/10.1084/jem.20030648
Jolly C, Mitar I, Sattentau QJ. Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells. J Virol. 2007;81(24):13916-13921. https://doi.org/10.1128/JVI.01585-07
Starling S, Jolly C, Kirchhoff F. LFA-1 engagement triggers T cell polarization at the HIV-1 virological synapse. J Virol. 2016;90(21):9841-9854. https://doi.org/10.1128/JVI.01152-16
Vasiliver-Shamis G, Cho Michael W, Hioe Catarina E, Dustin Michael L. Human immunodeficiency virus type 1 envelope gp120-induced partial T-cell receptor signaling creates an F-Actin-Depleted zone in the virological synapse. J Virol. 2009/11/01 2009;83(21):11341-11355. https://doi.org/10.1128/JVI.01440-09
Dale Benjamin M, McNerney Gregory P, Thompson Deanna L, et al. Cell-to-Cell transfer of HIV-1 via virological synapses leads to endosomal virion maturation that activates viral membrane fusion. Cell Host & Microbe. 2011;10(6):551-562. https://doi.org/10.1016/j.chom.2011.10.015
Jolly C, Kashefi K, Hollinshead M, Sattentau QJ. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J Exp Med. 2004;199(2):283-293. https://doi.org/10.1084/jem.20030648
Hübner W, McNerney GP, Chen P, et al. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science. 2009/03/27 2009;323(5922):1743-1747. https://doi.org/10.1126/science.1167525
Martin N, Welsch S, Jolly C, Briggs John AG, Vaux D, Sattentau Quentin J. Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition. J Virol. 2010/04/01 2010;84(7):3516-3527. https://doi.org/10.1128/JVI.02651-09
Puigdomènech I, Massanella M, Izquierdo-Useros N, et al. HIV transfer between CD4 T cells does not require LFA-1 binding to ICAM-1 and is governed by the interaction of HIV envelope glycoprotein with CD4. Retrovirology. 2008;5(1):32. https://doi.org/10.1186/1742-4690-5-32
Sattentau QJ. Cell-to-Cell spread of retroviruses. Viruses. 2010;2(6):1306-1321. https://doi.org/10.3390/v2061306
McDonald D, Wu L, Bohks SM, KewalRamani VN, Unutmaz D, Hope TJ. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science. 2003;300(5623):1295-1297. https://doi.org/10.1126/science.1084238
Jolly C, Mitar I, Sattentau QJ. Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J Virol. 2007;81(11):5547-5560. https://doi.org/10.1128/JVI.01469-06
Barroca P, Calado M, Azevedo-Pereira JM. HIV/dendritic cell interaction: consequences in the pathogenesis of HIV infection. AIDS Rev. 2014;16(4):223-235.
Pena-Cruz V, Agosto LM, Akiyama H, et al. HIV-1 replicates and persists in vaginal epithelial dendritic cells. J Clin investigation. 2018;128(8):3439-3444. https://doi.org/10.1172/JCI98943
Geijtenbeek TB, Kwon DS, Torensma R, et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell. Mar 3. 2000;100(5):587-597. https://doi.org/10.1016/s0092-8674(00)80694-7
Turville SG, Cameron PU, Handley A, et al. Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol. 2002/10/01 2002;3(10):975-983. https://doi.org/10.1038/ni841
Hammonds JE, Beeman N, Ding L, et al. Siglec-1 initiates formation of the virus-containing compartment and enhances macrophage-to-T cell transmission of HIV-1. PLoS Pathog. 2017;13(1):e1006181. https://doi.org/10.1371/journal.ppat.1006181
Izquierdo-Useros N, Lorizate M, McLaren PJ, Telenti A, Kräusslich H.-G, Martinez-Picado J. HIV-1 capture and transmission by dendritic cells: the role of viral glycolipids and the cellular receptor siglec-1. PLOS Pathog. 2014;10(7):e1004146. https://doi.org/10.1371/journal.ppat.1004146
Puryear WB, Akiyama H, Geer SD, et al. Interferon-inducible mechanism of dendritic cell-mediated HIV-1 dissemination is dependent on Siglec-1/CD169. PLoS Pathog. 2013;9(4):e1003291. https://doi.org/10.1371/journal.ppat.1003291
Zou Z, Chastain A, Moir S, et al. Siglecs facilitate HIV-1 infection of macrophages through adhesion with viral sialic acids. PloS one. 2011;6(9):e24559. https://doi.org/10.1371/journal.pone.0024559
Felts RL, Narayan K, Estes JD, et al. 3D visualization of HIV transfer at the virological synapse between dendritic cells and T cells. Proc Natl Acad Sci USA. 2010/07/27 2010;107(30):13336-13341. https://doi.org/10.1073/pnas.1003040107
Dupont M, Sattentau QJ. Macrophage cell-cell interactions promoting HIV-1 infection. Viruses. 2020;12(5):492. https://doi.org/10.3390/v12050492
Duncan CJA, Williams JP, Schiffner T, et al. High-multiplicity HIV-1 infection and neutralizing antibody evasion mediated by the macrophage-T cell virological synapse. J Virol. 2014;88(4):2025-2034. https://doi.org/10.1128/JVI.03245-13
Rodriguez-Plata MT, Puigdomènech I, Izquierdo-Useros N, et al. The infectious synapse formed between mature dendritic cells and CD4+T cells is independent of the presence of the HIV-1 envelope glycoprotein. Retrovirology. 2013/04/16 2013;10(1):42. https://doi.org/10.1186/1742-4690-10-42
Garcia E, Pion M, Pelchen-Matthews A, et al. HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic. 2005;6(6):488-501. https://doi.org/10.1111/j.1600-0854.2005.00293.x
Orenstein JM. The macrophage in HIV infection. Immunobiology. 2001/01/01/ 2001;204(5):598-602. https://doi.org/10.1078/0171-2985-00098
Deneka M, Pelchen-Matthews A, Byland R, Ruiz-Mateos E, Marsh M. In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. JCB (J Cell Biol). 2007;177(2):329-341. https://doi.org/10.1083/jcb.200609050
Nkwe DO, Pelchen-Matthews A, Burden JJ, Collinson LM, Marsh M. The intracellular plasma membrane-connected compartment in the assembly of HIV-1 in human macrophages. BMC Biol. 2016/06/23 2016;14(1):50. https://doi.org/10.1186/s12915-016-0272-3
Pelchen-Matthews A, Kramer B, MarshInfectious M. HIV-1 assembles in late endosomes in primary macrophages. JCB (J Cell Biol). 2003;162(3):443-455. https://doi.org/10.1083/jcb.200304008
Raposo G, Moore M, Innes D, et al. Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic. 2002;3(10):718-729. https://doi.org/10.1034/j.1600-0854.2002.31004.x
Bennett AE, Narayan K, Shi D, et al. Ion-abrasion scanning electron microscopy reveals surface-connected tubular conduits in HIV-infected macrophages. PLOS Pathog. 2009;5(9):e1000591. https://doi.org/10.1371/journal.ppat.1000591
Welsch S, Keppler OT, Habermann A, Allespach I, Krijnse-Locker J, Kräusslich H.-G. HIV-1 buds predominantly at the plasma membrane of primary human macrophages. PLOS Pathog. 2007;3(3):e36. https://doi.org/10.1371/journal.ppat.0030036
Groot F, Welsch S, Sattentau QJ. Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses. Blood. 2008/05/01/ 2008;111(9):4660-4663. https://doi.org/10.1182/blood-2007-12-130070
Gousset K, Ablan SD, Coren LV, et al. Real-time visualization of HIV-1 GAG trafficking in infected macrophages. PLOS Pathog. 2008;4(3):e1000015. https://doi.org/10.1371/journal.ppat.1000015
Rustom A, Saffrich R, Markovic I, Walther P, Gerdes H.-H. Nanotubular highways for intercellular organelle transport. Science. 2004/02/13 2004;303(5660):1007-1010. https://doi.org/10.1126/science.1093133
Wang Y, Cui J, Sun X, Zhang Y. Tunneling-nanotube development in astrocytes depends on p53 activation. Cell Death & Differ. 2011/04/01 2011;18(4):732-742. https://doi.org/10.1038/cdd.2010.147
Eugenin EA, Gaskill PJ, Berman JW. Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking. Cell Immunol. 2009/01/01/ 2009;254(2):142-148. https://doi.org/10.1016/j.cellimm.2008.08.005
Onfelt B, Nedvetzki S, Yanagi K, Davis DM. Cutting edge: membrane nanotubes connect immune cells. J Immunol. 2004;173(3):1511-1513. https://doi.org/10.4049/jimmunol.173.3.1511
Onfelt B, Nedvetzki S, Benninger RK, et al. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J Immunol. 2006;177(12):8476-8483. https://doi.org/10.4049/jimmunol.177.12.8476
Watkins SC, Salter RD. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity. 2005/09/01/ 2005;23(3):309-318. https://doi.org/10.1016/j.immuni.2005.08.009
Sowinski S, Jolly C, Berninghausen O, et al. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol. 2008/02/01 2008;10(2):211-219. https://doi.org/10.1038/ncb1682
Spees JL, Olson SD, Whitney MJ, Prockop DJ. Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci USA. 2006;103(5):1283-1288. https://doi.org/10.1073/pnas.0510511103
Kadiu I, Gendelman HE. Macrophage bridging conduit trafficking of HIV-1 through the endoplasmic reticulum and Golgi network. J Proteome Res. 2011;10(7):3225-3238. https://doi.org/10.1021/pr200262q
Kadiu I, Gendelman HE. Human immunodeficiency virus type 1 endocytic trafficking through macrophage bridging conduits facilitates spread of infection. J Neuroimmune Pharmacol official J Soc NeuroImmune Pharmacol. 2011;6(4):658-675. https://doi.org/10.1007/s11481-011-9298-z
Hase K, Kimura S, Takatsu H, et al. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat Cell Biol. 2009/12/01 2009;11(12):1427-1432. https://doi.org/10.1038/ncb1990
Hashimoto M, Bhuyan F, Hiyoshi M, et al. Potential role of the formation of tunneling nanotubes in HIV-1 spread in macrophages. J Immunol. 2016;196(4):1832-1841. https://doi.org/10.4049/jimmunol.1500845
Souriant S, Balboa L, Dupont M, et al. Tuberculosis exacerbates HIV-1 infection through IL-10/STAT3-dependent tunneling nanotube formation in macrophages. Cell Rep. 2019;26(13):3586-3599.e7. https://doi.org/10.1016/j.celrep.2019.02.091
Dupont M, Souriant S, Balboa L, et al. Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages. Elife. 2020;9:e52535. https://doi.org/10.7554/eLife.52535
Azevedo-Pereira JM, Pires D, Calado M, Mandal M, Santos-Costa Q, Anes E. HIV/Mtb Co-infection: from the amplification of disease pathogenesis to an “emerging Syndemic&rdquodquo. Microorganisms. 2023;11(4):853. https://doi.org/10.3390/microorganisms11040853
Baxter Amy E, Russell Rebecca A, Duncan Christopher JA, et al. Macrophage infection via selective capture of HIV-1-Infected CD4+ T cells. Cell Host & Microbe. 2014/12/10/ 2014;16(6):711-721. https://doi.org/10.1016/j.chom.2014.10.010
Ladinsky MS, Khamaikawin W, Jung Y, et al. Mechanisms of virus dissemination in bone marrow of HIV-1-infected humanized BLT mice. Elife. 2019/10/28 2019;8:e46916. https://doi.org/10.7554/eLife.46916
Calantone N, Wu F, Klase Z, et al. Tissue myeloid cells in SIV-infected primates acquire viral DNA through phagocytosis of infected T cells. Immunity. 2014/09/18/ 2014;41(3):493-502. https://doi.org/10.1016/j.immuni.2014.08.014
DiNapoli SR, Ortiz AM, Wu F, et al. Tissue-resident macrophages can contain replication-competent virus in antiretroviral-naive, SIV-infected Asian macaques. JCI Insight. 2017;2(4). https://doi.org/10.1172/jci.insight.91214
Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz C, Pypaert M, Mothes W. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat Cell Biol. 2007/03/01 2007;9(3):310-315. https://doi.org/10.1038/ncb1544
Nobile C, Rudnicka D, Hasan M, et al. HIV-1 Nef inhibits ruffles, induces filopodia, and modulates migration of infected lymphocytes. J Virol. 2010/03/01 2010;84(5):2282-2293. https://doi.org/10.1128/JVI.02230-09
Xu W, Santini PA, Sullivan JS, et al. HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat Immunol. 2009;10(9):1008-1017. https://doi.org/10.1038/ni.1753
Nikolic DS, Lehmann M, Felts R, et al. HIV-1 activates Cdc42 and induces membrane extensions in immature dendritic cells to facilitate cell-to-cell virus propagation. Blood. 2011;118(18):4841-4852. https://doi.org/10.1182/blood-2010-09-305417
Aggarwal A, Iemma TL, Shih I, et al. Mobilization of HIV spread by diaphanous 2 dependent filopodia in infected dendritic cells. PLoS Pathog. 2012;8(6):e1002762. https://doi.org/10.1371/journal.ppat.1002762
Schuitemaker H, Kootstra NA, Groenink M, De Goede RE, Miedema F, Tersmette M. Differential tropism of clinical HIV-1 isolates for primary monocytes and promonocytic cell lines. AIDS Res Hum Retroviruses. 1992;8(9):1679-1682. https://doi.org/10.1089/aid.1992.8.1679
Forte SE, Byron KS, Sullivan JL, Somasundaran M. Non-syncytium-inducing HIV type 1 isolated from infected individuals replicates in MT-2 cells. AIDS Res Hum Retroviruses. 1994;10(12):1613-1618. https://doi.org/10.1089/aid.1994.10.1613
Berger EA, Doms RW, Fenyö EM, et al. A new classification for HIV-1. Nature. 1998/01/01 1998;391(6664):240. https://doi.org/10.1038/34571
Lifson JD, Feinberg MB, Reyes GR, et al. Induction of CD4-dependent cell fusion by the HTLV-III/LAV envelope glycoprotein. Nature. 1986;323(6090):725-728. https://doi.org/10.1038/323725a0
Hildreth JEK, Orentas RJ. Involvement of a leukocyte adhesion receptor (LFA-1) in HIV-induced syncytium formation. Science. 1989/06/02 1989;244(4908):1075-1078. https://doi.org/10.1126/science.2543075
Sylwester A, Wessels D, Anderson SA, et al. HIV-induced syncytia of a T cell line form single giant pseudopods and are motile. J Cell Sci. 1993;106(Pt 3):941-953. https://doi.org/10.1242/jcs.106.3.941
Scheller C, Jassoy C. Syncytium formation amplifies apoptotic signals: a new view on apoptosis in HIV infection in vitro. Virology. 2001;282(1):48-55. https://doi.org/10.1006/viro.2000.0811
Castedo M, Roumier T, Blanco J, et al. Sequential involvement of Cdk1, mTOR and p53 in apoptosis induced by the HIV-1 envelope. Embo J. 2002;21(15):4070-4080. https://doi.org/10.1093/emboj/cdf391
Ferri KF, Jacotot E, Blanco J, et al. Apoptosis control in syncytia induced by the HIV type 1-envelope glycoprotein complex: role of mitochondria and caspases. J Exp Med. 2000;192(8):1081-1092. https://doi.org/10.1084/jem.192.8.1081
Sharer LR, Cho ES, Epstein LG. Multinucleated giant cells and HTLV-III in AIDS encephalopathy. Hum Pathol. 1985;16(8):760. https://doi.org/10.1016/s0046-8177(85)80245-8
Witzleben CL, Marshall GS, Wenner W, Piccoli DA, Barbour SD. HIV as a cause of giant cell hepatitis. Hum Pathol. 1988;19(5):603-605. https://doi.org/10.1016/s0046-8177(88)80213-2
Bracq L, Xie M, Lambelé M, et al. T cell-macrophage fusion triggers multinucleated giant cell formation for HIV-1 spreading. J Virol. 2017;91(24):91. https://doi.org/10.1128/jvi.01237-17
Compton AA, Schwartz O. They might Be giants: does syncytium formation sink or spread HIV infection? PLOS Pathog. 2017;13(2):e1006099. https://doi.org/10.1371/journal.ppat.1006099
Murooka TT, Deruaz M, Marangoni F, et al. HIV-infected T cells are migratory vehicles for viral dissemination. Nature. 2012;490(7419):283-287. https://doi.org/10.1038/nature11398
Orenstein JM. In vivo cytolysis and fusion of human immunodeficiency virus type 1-infected lymphocytes in lymphoid tissue. J Infect Dis. 2000;182(1):338-342. https://doi.org/10.1086/315640
Symeonides M, Murooka TT, Bellfy LN, Roy NH, Mempel TR, Thali M. HIV-1-Induced small T cell syncytia can transfer virus particles to target cells through transient contacts. Viruses. 2015;7(12):6590-6603. https://doi.org/10.3390/v7122959