Cited by 762HIV Research and TreatmentCellular transport and secretionExtracellular vesicles in disease

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Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission

Sowinski, Stefanie, Jolly, Clare, Berninghausen, Otto, Purbhoo, Marco A., Chauveau, Anne, Köhler, Karsten, Oddos, Stephane, Eissmann, Philipp, Brodsky, Frances M., Hopkins, Colin, Önfelt, Björn, Sattentau, Quentin, Davis, Daniel M.·2008·Nature Cell Biology

DOI 10.1038/ncb1682

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Abstract

Transmission of HIV-1 via intercellular connections has been estimated as 100-1000 times more efficient than a cell-free process, perhaps in part explaining persistent viral spread in the presence of neutralizing antibodies. Such effective intercellular transfer of HIV-1 could occur through virological synapses or target-cell filopodia connected to infected cells. Here we report that membrane nanotubes, formed when T cells make contact and subsequently part, provide a new route for HIV-1 transmission. Membrane nanotubes are known to connect various cell types, including neuronal and immune cells, and allow calcium-mediated signals to spread between connected myeloid cells. However, T-cell nanotubes are distinct from open-ended membranous tethers between other cell types, as a dynamic junction persists within T-cell nanotubes or at their contact with cell bodies. We also report that an extracellular matrix scaffold allows T-cell nanotubes to adopt variably shaped contours. HIV-1 transfers to uninfected T cells through nanotubes in a receptor-dependent manner. These data lead us to propose that HIV-1 can spread using nanotubular connections formed by short-term intercellular unions in which T cells specialize.

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Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection
Mattapallil, J. J., Douek, D. C., Hill, B. J., Nishimura, Y., Martin, M. A., & Roederer, M. (2005) · Nature · doi:10.1038/nature03501 · Cited by 1,269
Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells
Li, Q., Duan, L., Estes, J. D., Ma, Z.-M., Rourke, T., Wang, Y., Reilly, C., Carlis, J. V., Miller, C. J., & Haase, A. T. (2005) · Nature · doi:10.1038/nature03513 · Cited by 942
The Immunological Synapse of CTL Contains a Secretory Domain and Membrane Bridges
Stinchcombe, J. C., Bossi, G., Booth, S., & Griffiths, G. M. (2001) · Immunity · doi:10.1016/s1074-7613(01)00234-5 · Cited by 817
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Allen, C. D. C., Okada, T., Tang, H. L., & Cyster, J. G. (2006) · Science · doi:10.1126/science.1136736 · Cited by 784
HIV-1 Gag proteins: diverse functions in the virus life cycle
Freed, E. O. (1998) · Virology · doi:10.1006/viro.1998.9398 · Cited by 717
Recruitment of HIV and Its Receptors to Dendritic Cell-T Cell Junctions
McDonald, D., Wu, L., Bohks, S. M., KewalRamani, V. N., Unutmaz, D., & Hope, T. J. (2003) · Science · doi:10.1126/science.1084238 · Cited by 707
HIV-1 Cell to Cell Transfer across an Env-induced, Actin-dependent Synapse
Jolly, C., Kashefi, K., Hollinshead, M., & Sattentau, Q. J. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20030648 · Cited by 623
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Imaging the Single Cell Dynamics of CD4+ T Cell Activation by Dendritic Cells in Lymph Nodes
Miller, M. J., Safrina, O., Parker, I., & Cahalan, M. D. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20041236 · Cited by 545
GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission
Roux, A., Uyhazi, K., Frost, A., & Camilli, P. D. (2006) · Nature · doi:10.1038/nature04718 · Cited by 524

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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
In vivo imaging of virological synapses
Sewald, X., Gonzalez, D. G., Haberman, A. M., & Mothes, W. (2012) · Nature Communications · doi:10.1038/ncomms2338 · Cited by 71
Viral cell-to-cell spread: Conventional and non-conventional ways
Cifuentes-Muñoz, N., Najjar, F. E., & Dutch, R. (2020) · Advances in virus research · doi:10.1016/bs.aivir.2020.09.002 · Cited by 71
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 72
Self-citation
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Do, T., Murphy, G. E., Earl, L. A., Prete, G. Q. D., Grandinetti, G., Li, G., Estes, J. D., Rao, P., Trubey, C. M., Thomas, J. A., et al. (2014) · Journal of Virology · doi:10.1128/jvi.00788-14 · Cited by 73
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Omsland, 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
C5aR inhibition of nonimmune cells suppresses inflammation and maintains epithelial integrity in SARS-CoV-2–infected primary human airway epithelia
Posch, W., Vosper, J., Noureen, A., Zaderer, V., Witting, C., Bertacchi, G., Gstir, R., Filipek, P. A., Bonn, G. K., Huber, L. A., et al. (2021) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2021.03.038 · Cited by 68
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Role of HIV-1 Vpu protein for virus spread and pathogenesis
Nomaguchi, M., Fujita, M., & Adachi, A. (2008) · Microbes and Infection · doi:10.1016/j.micinf.2008.07.006 · Cited by 72
The junctions that don’t fit the scheme: special symmetrical cell-cell junctions of their own kind
Franke, W. W., Rickelt, S., Barth, M., & Pieperhoff, S. (2009) · Cell and Tissue Research · doi:10.1007/s00441-009-0849-z · Cited by 72
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Eugenín, E. A., Gaskill, P. J., & Berman, J. W. (2009) · Communicative & Integrative Biology · doi:10.4161/cib.2.3.8165 · Cited by 72
HIV-1 cell-to-cell transmission and broadly neutralizing antibodies
Dufloo, J., Bruel, T., & Schwartz, O. (2018) · Retrovirology · doi:10.1186/s12977-018-0434-1 · Cited by 69
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Kalinichenko, S., Komkov, D., & Mazurov, D. (2022) · Viruses · doi:10.3390/v14010152 · Cited by 68
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Background
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Seyed‐Razavi, Y., Hickey, M. J., Kuffová, L., McMenamin, P. G., & Chinnery, H. R. (2012) · Immunology and Cell Biology · doi:10.1038/icb.2012.52 · Cited by 70
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Pluta, K. D., & Kacprzak, M. M. (2009) · Acta Biochimica Polonica · doi:10.18388/abp.2009_2490 · Cited by 76
Adding new dimensions: towards an integrative understanding of HIV-1 spread
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Springer, D. J., Ren, P., Raina, R., Dong, Y., Behr, M. J., McEwen, B. F., Bowser, S. S., Samsonoff, W. A., Chaturvedi, S., & Chaturvedi, V. P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010978 · Cited by 69
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Autophagy-associated dengue vesicles promote viral transmission avoiding antibody neutralization
Wu, Y., Mettling, C., Wu, S.-R., Yu, C.-Y., Perng, G., Lin, Y.-S., & Lin, Y. (2016) · Scientific Reports · doi:10.1038/srep32243 · Cited by 66
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Kolodkin‐Gal, D., Hulot, S. L., Korioth-Schmitz, B., Gombos, R. B., Zheng, Y. Z., Owuor, J. O., Lifton, M. A., Ayeni, C., Najarían, R. M., Yeh, W. W., et al. (2013) · Journal of Virology · doi:10.1128/jvi.03108-12 · Cited by 65
Tunneling nanotubes: Emerging view of their molecular components and formation mechanisms
Kimura, S., Hase, K., & Ohno, H. (2012) · Experimental Cell Research · doi:10.1016/j.yexcr.2012.05.013 · Cited by 70
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Lock, J. T., Parker, I., & Smith, I. (2016) · Cell Calcium · doi:10.1016/j.ceca.2016.06.004 · Cited by 61
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Schiller, C., Huber, J. E., Diakopoulos, K. N., & Weiss, E. H. (2012) · Human Immunology · doi:10.1016/j.humimm.2012.11.026 · Cited by 64
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Sowinski, S., Alakoskela, J.-M. I., Jolly, C. L., & Davis, D. M. (2010) · Methods · doi:10.1016/j.ymeth.2010.04.002 · Cited by 67
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Rainy, N., Chetrit, D., Rouger, V., Vernitsky, H., Rechavi, O., Marguet, D., Goldstein, I., Ehrlich, M., & Kloog, Y. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.245 · Cited by 67
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Reichert, D., Scheinpflug, J., Karbanová, J., Freund, D., Bornhäuser, M., & Corbeil, D. (2016) · Experimental Hematology · doi:10.1016/j.exphem.2016.07.006 · Cited by 64
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Wang, Z., Liu, S., Tian, Z., Zhang, Z., Tang, H., & Pang, D. (2012) · ACS Nano · doi:10.1021/nn303729r · Cited by 60
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Chang, Y., Huang, Y.-H., Li, Z.-L., & Chen, C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035123 · Cited by 63
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Vasiliver-Shamis, G., Tuen, M., Wu, T. W., Starr, T., Cameron, T. O., Thomson, R. P., Kaur, G., Liu, J., Visciano, M. L., Li, H., et al. (2008) · Journal of Virology · doi:10.1128/jvi.00835-08 · Cited by 67
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Rehman, Z. U., Sjollema, K. A., Kuipers, J., Hoekstra, D., & Zuhorn, I. S. (2012) · ACS Nano · doi:10.1021/nn3028562 · Cited by 64
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Yang, H., Borg, T. K., Ma, Z., Xu, M., Wetzel, G., Saraf, L. V., Markwald, R. R., Runyan, R. B., & Gao, B. Z. (2016) · Biofabrication · doi:10.1088/1758-5090/8/1/015012 · Cited by 60
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Matejka, N., & Reindl, J. (2019) · Radiation Oncology · doi:10.1186/s13014-019-1416-8 · Cited by 58
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Matula, Z., Németh, A., Lőrincz, P., Szepesi, Á., Brózik, A., Buzás, E. I., Lőw, P., Német, K., Uher, F., & Urbán, V. S. (2016) · Stem Cells and Development · doi:10.1089/scd.2016.0086 · Cited by 55
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Luo, X., & He, J. J. (2014) · Journal of NeuroVirology · doi:10.1007/s13365-014-0304-0 · Cited by 56
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Wang, H.-Y., Jia, H.-R., Lu, X.-L., Chen, B., Zhou, G.-X., He, N., Chen, Z., & Wu, F.-G. (2015) · Journal of materials chemistry. B · doi:10.1039/c5tb00930h · Cited by 39
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Zani, B. G., & Edelman, E. R. (2010) · Communicative & Integrative Biology · doi:10.4161/cib.3.3.11659 · Cited by 52
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Schara, K., Janša, V., Šuštar, V., Dolinar, D., Pavlič, J., Lokar, M., Kralj‐Iglič, V., Veranič, P., & Iglič, A. (2009) · Cellular & Molecular Biology Letters · doi:10.2478/s11658-009-0018-0 · Cited by 57
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Salter, R. D., & Watkins, S. C. (2009) · Immunological Reviews · doi:10.1111/j.1600-065x.2009.00806.x · Cited by 53
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Boullé, M., Müller, T. G., Dähling, S., Ganga, Y., Jackson, L., Mahamed, D., Lance, O., Lustig, G., Neher, R. A., & Sigal, A. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005964 · Cited by 52
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Lehmann, M., Nikolic, D. S., & Piguet, V. (2011) · Viruses · doi:10.3390/v3091757 · Cited by 51
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Lee, J. (2014) · Plant Science · doi:10.1016/j.plantsci.2014.01.006 · Cited by 48
Sec6p anchors the assembled exocyst complex at sites of secretion.
Songer, J., & Munson, M. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-09-0968 · Cited by 58
Membrane dynamics associated with viral infection
de Armas‐Rillo, L., Valera, M., Marrero‐Hernández, S., & Valenzuela-Fernández, A. (2016) · Reviews in Medical Virology · doi:10.1002/rmv.1872 · Cited by 50
Tunneling nanotubes: an alternate route for propagation of the bystander effect following oncolytic viral infection
Ady, J., Thayanithy, V., Mojica, K. M., Wong, P., Carson, J. S., Rao, P., Fong, Y., & Lou, E. (2016) · Molecular Therapy — Oncolytics · doi:10.1038/mto.2016.29 · Cited by 48
Differential Exchange of Multifunctional Liposomes Between Glioblastoma Cells and Healthy Astrocytes via Tunneling Nanotubes
Formicola, B., D’Aloia, A., Magro, R. D., Stucchi, S., Rigolio, R., Ceriani, M., & Re, F. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00403 · Cited by 48
Tunneling Nanotube-Mediated Communication: A Mechanism of Intercellular Nucleic Acid Transfer
Driscoll, J., Gondaliya, P., & Patel, T. C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23105487 · Cited by 50
Directional Spread of Surface-Associated Retroviruses Regulated by Differential Virus-Cell Interactions
Sherer, N. M., Jin, J., & Mothes, W. (2010) · Journal of Virology · doi:10.1128/jvi.02155-09 · Cited by 52
Fas Signalling Promotes Intercellular Communication in T Cells
Luchetti, F., Canonico, B., Arcangeletti, M., Guescini, M., Cesarini, E., Stocchi, V., Esposti, M. D., & Papa, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035766 · Cited by 49
HIV-1 Nef-induced cardiotoxicity through dysregulation of autophagy
Gupta, M., Kaminski, R., Mullen, B., Gordon, J., Burdo, T. H., Cheung, J. Y., Feldman, A. M., Madesh, M., & Khalili, K. (2017) · Scientific Reports · doi:10.1038/s41598-017-08736-x · Cited by 48
Macrophages and Cell-Cell Spread of HIV-1
Waki, K., & Freed, E. O. (2010) · Viruses · doi:10.3390/v2081603 · Cited by 49
RNA transfer through tunneling nanotubes.
Haimovich, G., Dasgupta, S., & Gerst, J. (2020) · Biochemical Society Transactions · doi:10.1042/bst20200113 · Cited by 31
Rab8a/Rab11a regulate intercellular communications between neural cells via tunneling nanotubes
Zhu, H., Xue, C., Xu, X., Guo, Y., Li, X., Lu, J., Ju, S., Wang, Y., Cao, Z., & Gu, X. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.441 · Cited by 45
How do PrPSc Prions Spread between Host Species, and within Hosts?
Mabbott, N. A. (2017) · Pathogens · doi:10.3390/pathogens6040060 · Cited by 46
Opportunities and Challenges in Tunneling Nanotubes Research: How Far from Clinical Application?
Han, X., & Wang, X. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052306 · Cited by 46
Nanotube Action between Human Mesothelial Cells Reveals Novel Aspects of Inflammatory Responses
Ranzinger, J., Rustom, A., Abel, M., Leyh, J., Kihm, L., Witkowski, M., Scheurich, P., Zeier, M., & Schwenger, V. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029537 · Cited by 42
HIV-1 at the immunological and T-lymphocytic virological synapse
Haller, C., & Fackler, O. (2008) · Biological Chemistry · doi:10.1515/bc.2008.143 · Cited by 45
Controlling Chemistry by Geometry in Nanoscale Systems
Lizana, L., Konkoli, Z., Bauer, B., Jesorka, A., & Orwar, O. (2008) · Annual Review of Physical Chemistry · doi:10.1146/annurev.physchem.040808.090255 · Cited by 45
The secret life of extracellular vesicles in metal homeostasis and neurodegeneration
Bellingham, S. A., Guo, B. B., & Hill, A. F. (2015) · Biology of the Cell · doi:10.1111/boc.201500030 · Cited by 45
Intercellular Connections Related to Cell-Cell Crosstalk Specifically Recognized by an Aptamer.
Zhang, N., Bing, T., Shen, L., Song, R.-S., Wang, L.-L., Liu, X.-J., Liu, M., Li, J., Tan, W.-H., & Shangguan, D.-H. (2016) · Angewandte Chemie · doi:10.1002/anie.201510786 · Cited by 38
Preferential Transfer of Certain Plasma Membrane Proteins onto T and B Cells by Trogocytosis
Daubeuf, S., Aucher, A., Bordier, C., Salles, A., Serre, L., Gaibelet, G., Faye, J., Favre, G., Joly, E., & Hudrisier, D. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008716 · Cited by 47
On the steps of cell-to-cell HIV transmission between CD4 T cells
Puigdomènech, I., Massanella, M., Cabrera, C., Clotet, B., & Blanco, J. (2009) · Retrovirology · doi:10.1186/1742-4690-6-89 · Cited by 46
Protective Role of the M-Sec–Tunneling Nanotube System in Podocytes
Barutta, F., Kimura, S., Hase, K., Bellini, S., Corbetta, B., Corbelli, A., Fiordaliso, F., Barreca, A., Papotti, M. G., Ghiggeri, G. M., et al. (2021) · Journal of the American Society of Nephrology · doi:10.1681/asn.2020071076 · Cited by 44

Authors: Sowinski, S., Jolly, C., Berninghausen, O., Purbhoo, M. A., Chauveau, A., Köhler, K., Oddos, S., Eissmann, P., Brodsky, F. M., Hopkins, C., Önfelt, B., Sattentau, Q., & Davis, D. M.
Affiliations: Imperial College London (GB)
University of Oxford (GB)
University of California, San Francisco (US)
Karolinska Institutet (SE)
Corresponding author: Davis, Daniel M.
ORCID: Jolly, Clare
Berninghausen, Otto
Purbhoo, Marco A.
Brodsky, Frances M.
Önfelt, Björn
Sattentau, Quentin
Davis, Daniel M.
Venue: Nature Cell Biology
Publisher: Springer Science and Business Media LLC
Published: 2008-01-13
Volume: 10
Issue: 2
Pages: 211-219
ISSN: 1465-7392 (ISSN-L)
1476-4679
DOI: 10.1038/ncb1682
OpenAlex: W2088757776
Cited by: 754
References: 31
Citations by year: 2026: 22 · 2025: 19 · 2024: 30 · 2023: 24 · 2022: 38 · 2021: 45 · 2020: 47 · 2019: 37 · 2018: 46 · 2017: 41 · 2016: 48 · 2015: 35 · 2014: 38 · 2013: 32 · 2012: 58
FWCI: 20.05
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Cell Biology (publishedVersion)
PubMed (publishedVersion)
Research Explorer (The University of Manchester) (publishedVersion)
UCL Discovery (University College London) (submittedVersion)
Funders: Wellcome Trust
Biotechnology and Biological Sciences Research Council (BB/D011663/1)
National Institute of Allergy and Infectious Diseases (P01AI064520)
Topics: Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords: tunneling nanotubes, HIV-1 transmission, T cells, cell-cell contact, virological synapse, extracellular matrix scaffolds, calcium signaling
MeSH terms: Humans, Intercellular Junctions, T-Lymphocytes, Virulence, HIV-1, Jurkat Cells, Cell Surface Extensions

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Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission

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