The DOI matches its Crossref record; 81 of the 82 references it cites were found in a registry or an index.
Massive Secretion by T Cells Is Caused by HIV Nef in Infected Cells and by Nef Transfer to Bystander Cells
Open accessAbstract
The HIV Nef protein mediates endocytosis of surface receptors that correlates with disease progression, but the link between this Nef function and HIV pathogenesis is not clear. Here, we report that Nef-mediated activation of membrane trafficking is bidirectional, connecting endocytosis with exocytosis as occurs in activated T cells. Nef expression induced an extensive secretory activity in infected and, surprisingly, also in noninfected T cells, leading to the massive release of microvesicle clusters, a phenotype observed in vitro and in 36%-87% of primary CD4 T cells from HIV-infected individuals. Consistent with exocytosis in noninfected cells, Nef is transferred to bystander cells upon cell-to-cell contact and subsequently induces secretion in an Erk1/2-dependent manner. Thus, HIV Nef alters membrane dynamics, mimicking those of activated T cells and causing a transfer of infected cell signaling (TOS) to bystander cells. This mechanism may help explain the detrimental effect on bystander cells seen in HIV infection.
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“One common feature in these studies is that the MVBs involved may not be classical late-endosomes.”
From GAPDH controls extracellular vesicle biogenesis and enhances the therapeutic potential of EV mediated siRNA delivery to the brain (2021) · cites this paper as [64]
In the citing paper
“Indeed, clustered ILVs have been observed in other cell types in mammals and nematodes in the absence of DCGs and in specific pathological scenarios36,64.”
From GAPDH controls extracellular vesicle biogenesis and enhances the therapeutic potential of EV mediated siRNA delivery to the brain (2021) · cites this paper as [64]
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“The convergence of exosome and HIV biogenesis at the level of the endosomal sorting complex required for transport (ESCRT) [10] implies the possibility that viral products incorporate in exosomes, as already proven for both Gag [11] and Nef [12,13] HIV-1 proteins.”
BackgroundSelf-citationNemeth, J., Vongrad, V., Metzner, K. J., Strouvelle, V. P., Weber, R. K., Pedrioli, P. G. A., Aebersold, R. H., Günthard, H. F., & Collins, B. C. (2017) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m116.065235 · Cited by 20
“Indeed, NEF induces a massive secretory state not only in HIV-1-infected cells but also bystander cells (29).”
BackgroundDirect binding to GABARAP family members is essential for HIV-1 Nef plasma membrane localization
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“NAKC assembly is best known to mediate the enhancement of HIV transcription (19, 47, 71–73) as well as the release of extracellular vesicles with proinflammatory molecules (74, 75) by Nef.”
BackgroundExtracellular Vesicles in Viral Pathogenesis: A Case of Dr. Jekyll and Mr. Hyde
Purvinsh, L. V., Gorshkov, A. N., Brodskaia, A. V., & Vasin, A. V. (2021) · Life · doi:10.3390/life11010045 · Cited by 18
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Lee, J. (2023) · BMB Reports · doi:10.5483/bmbrep.2023-0073 · Cited by 17
“high levels in the blood plasma of individuals with HIV-1 (40, 41).”
Nef, the shuttling molecular adaptor of HIV, influences the cytokine network
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“T cells and causing a transfer of infected cell signaling to bystander cells [92].”
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Self-citationShuwari, N., Inoue, C., Ishigami, I., et al. (2024) · Journal of Controlled Release · doi:10.1016/j.jconrel.2024.07.079 · Cited by 15
Exogenous HIV-1 Nef Upsets the IFN-γ-Induced Impairment of Human Intestinal Epithelial Integrity
Quaranta, M. G., Vincentini, O., Felli, C., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023442 · Cited by 15
“However, Nef is known to be secreted from infected cells [16] in association with small membrane-bound vescicles [17,18].”
BackgroundThe GABARAP Co-Secretome Identified by APEX2-GABARAP Proximity Labelling of Extracellular Vesicles
Sanwald, J. L., Poschmann, G., Stühler, K., Behrends, C., Hoffmann, S., & Willbold, D. (2020) · Cells · doi:10.3390/cells9061468 · Cited by 13
Counteracting Akt Activation by HIV Protease Inhibitors in Monocytes/Macrophages
Pasquereau, S., Kumar, A., Abbas, W., & Herbein, G. (2018) · Viruses · doi:10.3390/v10040190 · Cited by 14
Stenovec, M., Lasič, E., Dominkuš, P. P., Bobnar, S. T., Zorec, R., Lenassi, M., & Kreft, M. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1072-2 · Cited by 15
Implications of HIV-1 Nef for “Shock and Kill” Strategies to Eliminate Latent Viral Reservoirs
Kuang, X. T., & Brockman, M. A. (2018) · Viruses · doi:10.3390/v10120677 · Cited by 15
“Additionally, Nef has been shown to increase exosome release, which presumably enhances the transfer of Nef-associated signaling activities to nearby cells [95].”
BackgroundMartínez, L. E., Lensing, S., Chang, D., Magpantay, L. I., Mitsuyasu, R. T., Ambinder, R. F., Sparano, J. A., Martı́nez-Maza, O., & Epeldegui, M. (2022) · Scientific Reports · doi:10.1038/s41598-022-13101-8 · Cited by 13
Contributions of HIV-1 Nef to immune dysregulation in HIV-infected patients: a therapeutic target?
Witkowski, W., & Verhasselt, B. (2013) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2013.830712 · Cited by 14
“Aside from direct intracellular effects and those resulting from close cell--cell contacts, Nef can act on bystander cells by inducing secretion of soluble factors [56] or exosomes recently described in this context [40-42].”
BackgroundGonzalez, G., Vituret, C., Pietro, A. D., Chanson, M., Boulanger, P. A., & Hong, S. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052326 · Cited by 13
“In general, MPs carry with them membrane and cytosolic components specific of their cellular origin [26], including proteins and nucleic acids, such as mRNAs and microRNAs [7,11,27–30], and are capable of transferring their cargo to recipient cells [16,29,31–34].”
BackgroundShete, A., Suryawanshi, P. V., Godbole, S., et al. (2016) · Scandinavian Journal of Immunology · doi:10.1111/sji.12422 · Cited by 10
Exosome-mediated regulation of inflammatory pathway during respiratory viral disease
Gheitasi, H., Sabbaghian, M., Shekarchi, A. A., Mirmazhary, A., & Poortahmasebi, V. (2024) · Virology Journal · doi:10.1186/s12985-024-02297-y · Cited by 11
“For instance, the incorporation of the Nef protein of human immunodeficiency virus (HIV) into the exosomes derived from HIV-infected cells [88], as well as Nef-transformed T cells [84, 85], stimulates the release of Nef from cells [89] and cell death of bystander CD4 + T lymphocytes.”
MethodPAK in pathogen-host interactions
Semblat, J., & Doerig, C. (2012) · Cellular Logistics · doi:10.4161/cl.20222 · Cited by 9
“There are even cases where virus-infected cells secrete viral proteins to the extracellular medium, from which they are taken up by bystander cells where they subvert signaling pathways; for example, cells infected by the human immunodeficiency virus HIV secrete the virally-encoded Tat and Nef proteins, which find the…”
BackgroundHIV-1 Intersection with CD4 T Cell Vesicle Exocytosis: Intercellular Communication Goes Viral
Soares, H. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00454 · Cited by 9
“The HIV-1 protein Nef causes massive secretion of extracellular vesicles (15) including Nef containing ones (16, 39).”
BackgroundHallmarks of HIV-1 pathogenesis are modulated by Nef’s Secretion Modification Region
Konadu, K. A. (2015) · Journal of AIDS & Clinical Research · doi:10.4172/2155-6113.1000476 · Cited by 8
“Nef is known to be released in exosomes from HIV-infected and nef-transfected cells [30-33].”
BackgroundCantres-Rosario, Y. M., Wojna, V., Ruíz, R., Díaz, B., Matos, M. R., Rodríguez-Benítez, R. J., Rodríguez, E. S., Skolasky, R. L., & Gerena, Y. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.809956 · Cited by 8
Modulation of HIV Pathogenesis and T-cell Signaling by HIV-1 Nef
Saxena, S. K., Shrivastava, G., Tiwari, S., Swamy, M. A., & Nair, M. (2012) · Future Virology · doi:10.2217/fvl.12.42 · Cited by 8
“Nef functions, such as virus transfer via cell–cell transmission, signaling and exosome formation provide new ways of understanding its complex role in HIV pathogenesis [116–120].”
BackgroundChandrasekaran, P., Buckley, M. W., Moore, V., Wang, L. Q., Kehrl, J. H., & Venkatesan, S. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.361782 · Cited by 8
Tartaglia, N. R., Jaular, L. M., Joliot, A., & Théry, C. (2025) · Cells and Development · doi:10.1016/j.cdev.2025.204054 · Cited by 6
Doroudchi, M., Yegorov, O., Baumgartner, T., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049562 · Cited by 6
“Nef protein induces its own secretion in bioactive micro vesicles by infected cells [9,10], or is transferred to bystander cells through cell-cell contact [11].”
BackgroundExogenous Nef Induces Proinflammatory Signaling Events in Murine Macrophages
Mangino, G., Serra, V., Borghi, P., Percario, Z. A., Horenkamp, F. A., Geyer, M., & Affabris, E. (2012) · Viral Immunology · doi:10.1089/vim.2011.0082 · Cited by 6
de Almeida, A. L. T., da Costa, I. P. S., Garcia, M. D. D. N., et al. (2025) · Viruses · doi:10.3390/v17030373 · Cited by 5
“In light of the immune evasion capabilities and trafficking of various biomolecules, including pro-inflammatory cytokines, as demonstrated in a study on EBOV [66], research on EVs is critical due to their potential therapeutic applications and roles as biomarkers [67].”
Takahashi, N., Eltalkhawy, Y. M., Nasu, K., Abdelnaser, R. A., Monde, K., Habash, S. A., Nasser, H., Hiyoshi, M., Ishimoto, T., & Suzu, S. (2024) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.150342 · Cited by 5
From Virus-like Particles to Engineered Exosomes for a New Generation of Vaccines
Federico, M. (2012) · Future Virology · doi:10.2217/fvl.12.29 · Cited by 5
“For instance, HIV-1-infected lymphocytes can release exosomes with proapoptotic activity on uninfected bystander T cells [58].”
BackgroundSelf-citationRaymond, A., Lang, M. J., Chu, J., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/708719 · Cited by 5
The impact of HIV-1 Nef on CD4 + T cells
Yaseen, M. M., Abuharfeil, N. M., & Darmani, H. (2026) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2025.2599773 · Cited by 3
“…of this pathway, which is central to viral replication and persistence (Arhel et al. 2009; Pan et al. 2012; Schrager et al. 2002; Manninen et al. 2000; wu and Marsh 2001; Muratori et al. 2009). the physiological relevance of this mechanism extends to both early and latent phases of Hiv-1 infection.”
Aiello, A., Giannessi, F., Percario, Z. A., Fecchi, K., Arenaccio, C., Leone, S., Carollo, M., D’Aversa, E., Chaperot, L., Gambari, R., et al. (2021) · Viruses · doi:10.3390/v14010074 · Cited by 4
“Despite the consistently reported association of Nef with EVs, it still remains unclear which type of EVs are involved, since, according to the cell type, Nef was found to be associated with small or large vesicles [23,33,35].”
BackgroundIntercellular Epigenomic Signalling via Extracellular Vesicles During B Cell Maturation
Yim, K. H. W., Hrout, A. A., & Chahwan, R. (2025) · Journal of Extracellular Vesicles · doi:10.1002/jev2.70040 · Cited by 4
“…of particle release was also observed in viral infected T cells, colorectal cancer cells, cardiac telocytes and gastrointestinal stromal tumours (Muratori et al. 2009; Valcz et al. 2019; Fertig, Gherghiceanu, and Popescu 2014; Junquera et al. 2016), we are the first to report such mode of…”
Chase, A. J., Wombacher, R., & Fackler, O. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.002794 · Cited by 4
The HIV-1 Virulence Factor Nef as a New Therapeutic Target Against HIV/AIDS
Kim, J.-A., Shin, Y., & Yoon, C. (2020) · Journal of Bacteriology and Virology · doi:10.4167/jbv.2020.50.3.187 · Cited by 4
“Nef induces membrane trafficking modification to promote secretory activity (13).”
BackgroundNasi, A., Amu, S., Göthlin, M., Jansson, M., Nagy, N., Chiodi, F., & Réthi, B. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00244 · Cited by 4
Lentiviral Nef Proteins Differentially Govern the Establishment of Viral Latency
Carlin, E., Greer, B. D., Lowman, K. E., Dalecki, A. G., Duverger, A. E., Wagner, F., & Kutsch, O. (2022) · Journal of Virology · doi:10.1128/jvi.02206-21 · Cited by 3
Go, S., Li, H. L., Chang, J., Verhoeven, A. J., & Elferink, R. P. J. O. (2023) · Traffic · doi:10.1111/tra.12904 · Cited by 3
“Finally, a third mechanism of microvesicular secretion is that of direct release of clustered submembranous vesicles as observed by Muratori et al.(68) Although this mechanism was primarily observed in HIV-infected cells it might also function at low rates in other cells and this would markedly coincide with our obser…”
ResultVirus Immune Evasion: New Mechanism and Implications in Disease Outcome
Draenert, R., Frater, J., & Prado, J. G. (2012) · Advances in Virology · doi:10.1155/2012/490549 · Cited by 2
Martínez, L. E., Lensing, S., Chang, D., Magpantay, L. I., Guo, Y., Mitsuyasu, R. T., Ambinder, R. F., Sparano, J. A., Martı́nez-Maza, O., & Epeldegui, M. (2025) · Scientific Reports · doi:10.1038/s41598-025-11128-1 · Cited by 2
Lavrin, T., Loboda, J., Ferdin, J., Levak, V., Sitar, S., Holcar, M., Resnik, N., Stenovec, M., Bakija, A. T., Veranič, P., et al. (2025) · Extracellular Vesicles and Circulating Nucleic Acids · doi:10.20517/evcna.2025.106 · Cited by 2
Miyakawa, K., Nishi, M., Jeremiah, S. S., Morikawa, Y., & Ryo, A. (2022) · Frontiers in Virology · doi:10.3389/fviro.2022.836125 · Cited by 2
Curry, B. J. (2014) · Cited by 2
HIV-1 Nef Transfer and Intracellular Signalling in Uninfected Cells
Zulema, A. P., Mangino, G., Gallo, V., Chiantore, M. V., Fiorucci, G., Romeo, G., & Affabris, E. (2011) · InTech eBooks · doi:10.5772/21623 · Cited by 2
“, 2006) and recently it has been provided experimental evidencies that it can be transferred to uninfected cells from the infected ones via cellular protrusions and/or exosomes (Lenassi et al., 2010; Muratori et al., 2009; Xu et al., 2009) opening a new road to deepen our insight on the roles of this multifunctional p…”
BackgroundUncovering the Role of Defective HIV-1 in Spreading Viral Infection
Arenaccio, C., Manfredi, F., Anticoli, S., Chiozzini, C., & Federico, M. (2015) · Future Virology · doi:10.2217/fvl.15.10 · Cited by 1
Self-citationExtracellular Vesicles and Particles Modulate Proton Secretion in a Model of Human Parietal Cells
Reiner, A. T., Sterneder, S., Reipert, S., Wolske, S., & Somoza, V. (2023) · ACS Omega · doi:10.1021/acsomega.2c06442 · Cited by 1
Loots, S. (2013) · SUNScholar (Stellenbosch University) · Cited by 1
HIV-1-Infected Cells Transiently Express Lentiviral RNA Shuttled by Exosomes
Arenaccio, C., Cabezas, S. C., & Federico, M. (2014) · Future Virology · doi:10.2217/fvl.13.126
Self-citationCellsby the Integral MAL Protein in T Cutting Edge: Regulation of Exosome
Martínez-Menárguez, A., Andrés, G., Martínez-Alonso, M. A., et al. (2015)
Le rôle du DCIR dans la libération des exosomes dans le contexte de l'infection par le VIH-1
Mfunyi, C. M. (2013) · Corpus Université Laval (Université Laval)
Investigating the role of HIV-1 Nef during reactivation of latent viral reservoirs
Kuang, X. T. (2018) · Summit (Simon Fraser University)
Investigating the Role of Vaccinia Virus-derived Small Extracellular Vesicle Cargo in Infection
McKay, H. E. (2019) · uO Research (University of Ottawa) · doi:10.20381/ruor-23723
Mechanisms by which HIV-1 Nef disrupts the intracellular trafficking of host proteins
Leonard, J. A. (2011) · Deep Blue (University of Michigan)
Baldari, C. T., & Finetti, F. (2017) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.718505292.793537779
Intercellular epigenomic signaling during B cell maturationPreprint
Yim, K. H. W., Hrout, A. A., & Chahwan, R. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.24.595740
“…form of particle release was also observed in viral infected T cells, colorectal cancer cells, cardiac telocytes and gastrointestinal stromal tumors(32– 35), we are the first to report such mode of secretion of EVs under physiological condition from B cells, possibly to enhance protection and…”
BackgroundMorath, K., Stolp, B., Rosenbauer, J., Mahnke, K., Platten, M., & Fackler, O. (2025) · SSRN Electronic Journal · doi:10.1101/2025.08.14.670333
DNA vaccination amplifiers HLA-DR cross-restricted public TCR clonotypes shared with HIV controllers
Mukhopadhyay, M. (2017) · theses.fr (ABES) · doi:10.70675/a42f696ez8360z43b6z95a3z984bca393809
HIV-1 Nef inhibits the JAK/STAT signaling pathway by inducing proteasomal degradation of STAT1
Rodrigues, R. L., da Silva-Januário, M. E., Apolloni, V. B., Espada, C. E., Ricciardi-Jorge, T., Tavares, L., de Carvalho, A. N., Souza, J. P., Arruda, E., Assunção‐Miranda, I., et al. (2026) · PLoS ONE · doi:10.1371/journal.pone.0352649
Metadata
- Authors
- Muratori, C., Cavallin, L. E., Krätzel, K., Tinari, A., De Milito, A., Fais, S., D'Aloja, P., Federico, M., Vullo, V., Fomina, A., Mesri, E. A., Superti, F., & Baur, A. S.
- Affiliations
- University of Miami (US)
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- Istituto Superiore di Sanità (IT)
- Sapienza University of Rome (IT)
- University of California, Davis (US)
- Corresponding author
- Baur, Andreas S.
- ORCID
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2009-09
- Volume
- 6
- Issue
- 3
- Pages
- 218-230
- ISSN
- 1931-3128 (ISSN-L)
- OpenAlex
- W1983073673
- Semantic Scholar
- 4882f11c55140c561fa862059b7d2ec9e08c0fa5
- Cited by
- 164
- References
- 82
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 4 · 2023: 5 · 2022: 7 · 2021: 8 · 2020: 9 · 2019: 13 · 2018: 17 · 2017: 12 · 2016: 15 · 2015: 13 · 2014: 11 · 2013: 8 · 2012: 19
- FWCI
- 4.06
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1415 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell Host & Microbe (publishedVersion)
- PubMed (publishedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Funders
- National Cancer Institute (CA 75918, R01CA075918)
- 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 › Immunology and Microbiology › Immunology › T-cell and Retrovirus Studies
- Keywords
- HIV Nef, exocytosis, endocytosis, microvesicles, bystander cells, cell-to-cell transmission, ERK signaling, membrane trafficking, CD4+ T cells, HIV pathogenesis
- MeSH terms
- Cells, Cultured, Endocytosis, Exocytosis, Humans, Lymphocyte Activation, T-Lymphocytes, HIV-1, HIV Infections, Protein Transport, Secretory Vesicles, Bystander Effect, nef Gene Products, Human Immunodeficiency Virus, Host-Pathogen Interactions, Secretory Pathway
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