Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: A potential mechanism for intercellular HIV trafficking
Open accessAbstract
Cell to cell communication is essential for the organization/coordination of multicellular systems and cellular development. Cellular communication is mediated by soluble factors, including growth factors, neurotransmitters, cytokines/chemokines, gap junctions, and the recently described tunneling nanotubes (TNT). TNT are long cytoplasmatic bridges that enable long range directed communication between cells. The proposed function for TNT is the cell-to-cell transfer of large cellular structures such as vesicles and organelles. We demonstrate that HIV-infection of human macrophages results in an increased number of TNT, and show HIV particles within these structures. We propose that HIV "highjacks" TNT communication to spread HIV through an intercellular route between communicated cells, contributing to the pathogenesis of AIDS.
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HIV-1 infection increases the number of short (30 μm) and long (150 μm) TNTs in macrophages; Gag is detected inside short TNTs and on the surface of long TNTs.
“In macrophages, HIV-1 infection increases the number of short (30 μm) and long (150 μm) TNTs; Gag is detected inside the short TNTs, and on the surface of long TNTs [110].”
From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [110]
Results §§3.3–3.4 (pages not provided) report increased short and long TNT formation after HIV infection and lengths of approximately 30 μm and 150 μm. Results §3.5 reports p24-positive viral particles appearing inside short TNTs, but describes their location on long TNTs as uncertain: they might be extracellularly surfing or within stretched cytoplasm. The claim overstates the evidence by saying they are detected on the surface of long TNTs. (LLM, conf=0.88)
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“These results indicate that the ability to form nanotubes is cell specific; this was also shown for HIV infection, where changes in the length of TNTs were not detected in HIV-infected macrophages (47).”
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“Filopodia and nanotubes may also facilitate cell transfer of HIV-1 (131, 132).”
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“This indicates that HIV hijacks TNTs communication to spread the pathogenesis of AIDS (Eugenin et al., 2009).”
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“Unlike in T lymphocytes, the transfer of HIV-1 particles via TNTs has been suggested but not formally demonstrated in macrophages (Dupont et al., 2018; Eugenin et al., 2009; Hashimoto et al., 2016; Okafo et al., 2017).”
Chemotherapy-Induced Tunneling Nanotubes Mediate Intercellular Drug Efflux in Pancreatic Cancer
Desir, S., O’Hare, P., Vogel, R. I., Sperduto, W., Sarkari, A., Dickson, E. L., Wong, P., Nelson, A., Fong, Y., Steer, C. J., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-27649-x · Cited by 120 · see citing works
The HIV-1-containing macrophage compartment: a perfect cellular niche?
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Self-citationRustom, A. (2016) · Open Biology · doi:10.1098/rsob.160057 · Cited by 97 · see citing works
“human macrophages to promote virus propagation between cells [58,59].”
BackgroundKadiu, I., & Gendelman, H. E. (2011) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-011-9298-z · Cited by 100 · see citing works
“…Neuroscience, University of Nebraska Medical Center, 985800 Nebraska Medical Center, Omaha, NE 68198-5800, USA e-mail: hegendel@unmc.edu these represent mature HIV-1 surfing on the conduits or viral particulates sequestered into endocytic compartments (Eugenin et al. 2009a, b; Xu et al. 2009).”
BackgroundInfluentialPotential Modes of Intercellular α-Synuclein Transmission
Valdinocci, D., Radford, R. A. W., Siow, S. M., Chung, R. S., & Pountney, D. L. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18020469 · Cited by 108 · see citing works
Intercellular communication in malignant pleural mesothelioma: properties of tunneling nanotubes
Ady, J., Desir, S., Thayanithy, V., Vogel, R. I., Moreira, A. L., Downey, R. J., Fong, Y., Manova-Todorova, K. O., Moore, M. A. S., & Lou, E. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00400 · Cited by 95 · see citing works
“…variety of non-cancer cell types including dendritic cells and monocytes (Watkins and Salter, 2005; Salter and Watkins, 2006), mature macrophages (Eugenin et al., 2009; Hase et al., 2009), T cells (Sowinski et al., 2008, 2011; Rudnicka et al., 2009), B cells (Xu et al., 2009), neutrophils…”
BackgroundInfluentialTumor exosomes induce tunneling nanotubes in lipid raft-enriched regions of human mesothelioma cells
Thayanithy, V., Babatunde, V., Dickson, E. L., Wong, P., Oh, S., Ke, X., Barlas, A., Fujisawa, S., Romin, Y., Moreira, A. L., et al. (2014) · Experimental Cell Research · doi:10.1016/j.yexcr.2014.01.014 · Cited by 104 · see citing works
Specialized Intercellular Communications via Cytonemes and Nanotubes
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“…et al 2009) HIV-1 (“membrane nanotubes”) HIV-1 protein Gag Jurkat T cells (Sowinski et al 2008) HIV-1 Virus genome Macrophages Virus spreading (Eugenin et al 2009) HIV-1, (“filopodia”) Virions Dendritic Cells to T-cells Virus spreading (Aggarwal et al 2012, Shrivastava et al…”
BackgroundNikolic, D. S., Lehmann, M., Felts, R. L., Garcia, E., Blanchet, F. P., Subramaniam, S., & Piguet, V. (2011) · Blood · doi:10.1182/blood-2010-09-305417 · Cited by 99 · see citing works
Emerging physiological and pathological implications of tunneling nanotubes formation between cells
Sisakhtnezhad, S., & Khosravi, L. (2015) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2015.06.010 · Cited by 113 · see citing works
HIV-1 Nef Inhibits Ruffles, Induces Filopodia, and Modulates Migration of Infected Lymphocytes
Nobile, C., Rudnicka, D., Hasan, M., Aulner, N., Porrot, F., Machu, C., Renaud, O., Prévost, M., Hivroz, C., Schwartz, O., et al. (2009) · Journal of Virology · doi:10.1128/jvi.02230-09 · Cited by 100 · see citing works
“HIV-1 infection of macrophages also enhances filopodium formation and transfer of Nef to neighboring B cells via long-range intercellular conduits (12, 61, 45).”
BackgroundCx43 and Associated Cell Signaling Pathways Regulate Tunneling Nanotubes in Breast Cancer Cells
Tishchenko, A., Azorín, D., Vidal-Brime, L., Muñoz, M. J., Arenas, P. J., Pearce, C., Girão, H., Cajal, S., & Aasen, T. (2020) · Cancers · doi:10.3390/cancers12102798 · Cited by 92 · see citing works
“A wide variety of TNT-mediated cargo transport has been described, including that of ions [22], miRNAs [23], cytosolic proteins [24], and prions [25–27], pathogens, such as viruses [28,29] and bacteria [30], and organelles, such as the endoplasmic reticulum [31], mitochondria [32], Golgi vesicles [31], endosomes [33],…”
BackgroundLipid droplets as a novel cargo of tunnelling nanotubes in endothelial cells
Astanina, K., Koch, M., Jüngst, C., Zumbusch, A., & Kiemer, A. K. (2015) · Scientific Reports · doi:10.1038/srep11453 · Cited by 104 · see citing works
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“Like Pd, TNTs traffic proteins (Onfelt et al., 2005; Davis and Sowinski, 2008; Rustom, 2009) and serve as conduits for pathogens, such as prions (Gerdes, 2009), and, potentially, human immunodeficiency virus (HIV) particles (Eugenin et al., 2009a, 2009b).”
BackgroundValenti, D., Vacca, R. A., Moro, L., & Atlante, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158312 · Cited by 99 · see citing works
Cell membrane biophysics with optical tweezers
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“TNT formation is also induced by HIV virus and facilitates spread of infection (Eugenin et al. 2009; Kadiu and Gendelman 2011).”
BackgroundIntercellular nanotubes: insights from imaging studies and beyond
Hurtig, J., Chiu, D. T., & Önfelt, B. (2010) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.80 · Cited by 85 · see citing works
Transfer of Intracellular HIV Nef to Endothelium Causes Endothelial Dysfunction
Wang, T., Green, L. A., Gupta, S. K., Kim, C., Wang, L., Almodóvar, S., Flores, S. C., Prudovsky, I. A., Jolicoeur, P., Liu, Z., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091063 · Cited by 74 · see citing works
The direct passage of animal viruses between cells
Sattentau, Q. J. (2011) · Current Opinion in Virology · doi:10.1016/j.coviro.2011.09.004 · Cited by 71 · see citing works
Bridging the Gap: Virus Long-Distance Spread via Tunneling Nanotubes
Jansens, R. J. J., Tishchenko, A., & Favoreel, H. W. (2020) · Journal of Virology · doi:10.1128/jvi.02120-19 · Cited by 88 · see citing works
“HIV capping of filopodia depends on the viral Gag polyprotein and the frequency of filopodium formation is enhanced by the viral Nef protein, suggesting functional and/or biochemical similarity to HIV Nef-induced TNTs (54, 55).”
InfluentialThe molecular basis of induction and formation of tunneling nanotubes
Kimura, S., Hase, K., & Ohno, H. (2012) · Cell and Tissue Research · doi:10.1007/s00441-012-1518-1 · Cited by 78 · see citing works
“formation of TNTs and/or TNT-like structures in infected cells (Aggarwal et al., 2012; Eugenin et al., 2009; Nikolic et al., 2011; Nobile et al., 2010; Xu et al., 2009).”
BackgroundImpenetrable barriers or entry portals? The role of cell–cell adhesion during infection
Bonazzi, M., & Cossart, P. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201106011 · Cited by 74 · see citing works
“During viral infections, HIV and murine leukemia virus (MLV) trigger the formation of filopodial bridges that connect infected cells with neighboring non-infected cells, thereby spreading the infection (Sherer et al., 2007; Sowinski et al., 2008; Eugenin et al., 2009; Jin et al., 2009).”
Jansens, R. J. J., Van den Broeck, W., De Pelsmaeker, S., Lamote, J. A. S., Van Waesberghe, C., Couck, L., & Favoreel, H. W. (2017) · Journal of Virology · doi:10.1128/jvi.00749-17 · Cited by 71 · see citing works
“is able to trigger the formation of TNTs via its Nef protein (13).”
BackgroundOmsland, M., Pise-Masison, C., Fujikawa, D., Galli, V., Fenizia, C., Parks, R. W., Gjertsen, B. T., Franchini, G., & Andresen, V. (2018) · Scientific Reports · doi:10.1038/s41598-018-29391-w · Cited by 71 · see citing works
Role of Tunneling Nanotubes in Viral Infection, Neurodegenerative Disease, and Cancer
Tiwari, V., Koganti, R., Russell, G., Sharma, A., & Shukla, D. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.680891 · Cited by 70 · see citing works
“Thicker TNTs contain microtubules and exceed a 7 μm diameter which allows them to transfer organelles such as mitochondria between cells (6, 12).”
BackgroundInfluentialBone degradation machinery of osteoclasts: An HIV-1 target that contributes to bone loss
Raynaud-Messina, B., Bracq, L., Dupont, M., Souriant, S., Usmani, S. M., Proag, A., Pingris, K., Soldan, V., Thibault, C., Capilla, F., et al. (2018) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1713370115 · Cited by 69 · see citing works
HIV-1 cell-to-cell transmission and broadly neutralizing antibodies
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“HIV-1 can use close-ended membrane protrusions called tunneling nanotubes (TNTs) that form between infected and uninfected T cells to spread in a receptor-dependent manner [98] (Fig.”
BackgroundHIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread
Kalinichenko, S., Komkov, D., & Mazurov, D. (2022) · Viruses · doi:10.3390/v14010152 · Cited by 68 · see citing works
“They translocate to recipient cells via TNTs, causing cell anergy and viral escape from immune surveillance [118].”
BackgroundInfluentialRupp, I., Sologub, L., Williamson, K., Scheuermayer, M., Reininger, L., Doerig, C., Ekşi, S., Kombila, D., Frank, M., & Pradel, G. (2010) · Cell Research · doi:10.1038/cr.2010.176 · Cited by 66 · see citing works
Zaccard, C. R., Watkins, S. C., Kaliński, P., Fecek, R. J., Yates, A. L., Salter, R. D., Ayyavoo, V., Rinaldo, C. R., & Mailliard, R. B. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1401832 · Cited by 69 · see citing works
“HIV-1 was shown to induce TNTs in infected macrophages and use them for high-speed transmission to neighboring uninfected macrophages (30, 31).”
BackgroundCivita, P., Leite, D. M., & Pilkington, G. J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20236017 · Cited by 74 · see citing works
Seyed‐Razavi, Y., Hickey, M. J., Kuffová, L., McMenamin, P., & Chinnery, H. (2013) · Immunology and Cell Biology · doi:10.1038/icb.2012.52 · Cited by 63 · see citing works
Tunneling nanotubes: emerging view of their molecular components and formation mechanisms.
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“It is still unclear how HIV-1 overrides this junction and transfers to the bystander cells.”
BackgroundInfluentialLock, J. T., Parker, I., & Smith, I. (2016) · Cell Calcium · doi:10.1016/j.ceca.2016.06.004 · Cited by 61 · see citing works
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“One day later the cells became more motile exhibiting increased plasma membrane movements, in agreement with previous observations [17].”
ResultArchitecture and Regulation of the HIV-1 Assembly and Holding Compartment in Macrophages
Welsch, S., Groot, F., Kräusslich, H., Keppler, O., & Sattentau, Q. (2011) · Journal of Virology · doi:10.1128/jvi.00834-11 · Cited by 59 · see citing works
“shown to upregulate tunneling nanotubes in macrophages (7),”
BackgroundOptimized methods for imaging membrane nanotubes between T cells and trafficking of HIV-1
Sowinski, S., Alakoskela, J.-M. I., Jolly, C. L., & Davis, D. M. (2010) · Methods · doi:10.1016/j.ymeth.2010.04.002 · Cited by 65 · see citing works
Valdebenito, S., Audia, A., Bhat, K., Okafo, G., & Eugenin, E. (2020) · iScience · doi:10.1016/j.isci.2020.101450 · Cited by 58 · see citing works
Self-citationLou, E., Zhai, E., Sarkari, A., Desir, S., Wong, P., Iizuka, Y., Yang, J., Subramanian, S., McCarthy, J., Bazzaro, M., et al. (2018) · Front. Cell Dev. Biol. · doi:10.3389/fcell.2018.00095 · Cited by 58 · see citing works
“Tunneling nanotubes (TNTs) are long filamentous actin-based cellular protrusions that contribute to these interactions, with a special role in longrange communication (Rustom et al., 2004; Onfelt et al., 2005; Eugenin et al., 2009; Gousset et al., 2009, 2013; Chauveau et al., 2010; Plotnikov et al., 2010; Lou et al.,…”
BackgroundViral cell-to-cell spread: Conventional and non-conventional ways
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“Thick TNT are functionally distinguished by the transfer of large organelles, such as lysosomes and mitochondria (Dupont et al., 2018; Eugenin et al., 2009; Hashimoto et al., 2016).”
BackgroundMyosin-X is essential to the intercellular spread of HIV-1 Nef through tunneling nanotubes
Uhl, J., Gujarathi, S., Waheed, A. A., Gordon, A., Freed, E. O., & Gousset, K. (2019) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-018-0493-z · Cited by 57 · see citing works
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The Glutamate System as a Crucial Regulator of CNS Toxicity and Survival of HIV Reservoirs
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Self-citationMechanisms of HIV Neuropathogenesis: Role of Cellular Communication Systems
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“Our laboratory has also documented significant increase in the numbers of TNTs in primary human macrophages upon HIV infection [105].”
BackgroundSelf-citationHIV-1 Trans Infection of CD4 + T Cells by Professional Antigen Presenting Cells
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“Furthermore, HIV-1 may code for its own activation inmacrophages, as suggested by singlestranded RNA of HIV-1 inducing uridine-rich TLR 7/8 ligands that stimulate MyD88-dependent monocyte activation [337].”
BackgroundMacrophages and Cell-Cell Spread of HIV-1
Waki, K., & Freed, E. O. (2010) · Viruses · doi:10.3390/v2081603 · Cited by 47 · see citing works
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“Broad cell-cell contacts, designated virological synapses because of a resemblance to immunological synapses, as well as thin, filopodial or nanotube contacts have been described (8, 12, 14, 26, 30, 33).”
BackgroundMacrophage Cell-Cell Interactions Promoting HIV-1 Infection
Dupont, M., & Sattentau, Q. J. (2020) · Viruses · doi:10.3390/v12050492 · Cited by 55 · see citing works
“, exosomes or VCC), either within or on the outside of the nanotube [97].”
BackgroundDrosophila cells use nanotube-like structures to transfer dsRNA and RNAi machinery between cells
Karlikow, M., Goić, B., Mongelli, V., Salles, A., Schmitt, C., Bonne, I., Zurzolo, C., & Saleh, M.-C. (2016) · Scientific Reports · doi:10.1038/srep27085 · Cited by 48 · see citing works
- Authors
- Eugenin, E. A., Gaskill, P. J., & Berman, J. W.
- Affiliations
- Albert Einstein College of Medicine (US)
- Corresponding author
- Eugenin, E.A.
- Venue
- Cellular Immunology
- Publisher
- Elsevier BV
- Published
- 2009
- Volume
- 254
- Issue
- 2
- Pages
- 142-148
- ISSN
- 0008-8749 (ISSN-L)
- PMC
- PMC2701345
- OpenAlex
- W1998392341
- Cited by
- 304
- References
- 31
- Citations by year
- 2026: 14 · 2025: 7 · 2024: 24 · 2023: 18 · 2022: 31 · 2021: 15 · 2020: 25 · 2019: 21 · 2018: 18 · 2017: 15 · 2016: 16 · 2015: 9 · 2014: 7 · 2013: 22 · 2012: 16
- FWCI
- 5.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cellular Immunology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (MH 070297, K01MH076679, MH075679, R01MH075679, R01MH070297, MH076679)
- National Institute on Drug Abuse (F32DA024965)
- National Institute of Allergy and Infectious Diseases (P30AI051519, AI 051519)
- National Institute of Neurological Disorders and Stroke (T32NS007098, NS 07098)
- Topics
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- tunneling nanotubes, HIV infection, macrophages, cell-to-cell communication, AIDS pathogenesis
- MeSH terms
- Cells, Cultured, HIV, Humans, Macrophages, HIV Core Protein p24
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