Nef Secretion into Extracellular Vesicles or Exosomes Is Conserved across Human and Simian Immunodeficiency Viruses
Open accessAbstract
Extracellular vesicles (EVs) or exosomes have been implicated in the pathophysiology of infections and cancer. The negative regulatory factor (Nef) encoded by simian immunodeficiency virus (SIV) and human immunodeficiency virus (HIV) plays a critical role in the progression to AIDS and impairs endosomal trafficking. Whether HIV-1 Nef can be loaded into EVs has been the subject of controversy, and nothing is known about the connection between SIV Nef and EVs. We find that both SIV and HIV-1 Nef proteins are present in affinity-purified EVs derived from cultured cells, as well as in EVs from SIV-infected macaques. Nef-positive EVs were functional, i.e., capable of membrane fusion and depositing their content into recipient cells. The EVs were able to transfer Nef into recipient cells. This suggests that Nef readily enters the exosome biogenesis pathway, whereas HIV virions are assembled at the plasma membrane. It suggests a novel mechanism by which lentiviruses can influence uninfected and uninfectable, i.e., CD4-negative, cells. IMPORTANCE Extracellular vesicles (EVs) transfer biologically active materials from one cell to another, either within the adjacent microenvironment or further removed. EVs also package viral RNAs, microRNAs, and proteins, which contributes to the pathophysiology of infection. In this report, we show that both human immunodeficiency virus (HIV) and simian immunodeficiency virus (SIV) incorporate the virus-encoded Nef protein into EVs, including EVs circulating in the blood of SIV-infected macaques and that this presents a novel mechanism of Nef transfer to naive and even otherwise non-infectable cells. Nef is dispensable for viral replication but essential for AIDS progression in vivo . Demonstrating that Nef incorporation into EVs is conserved across species implicates EVs as novel mediators of the pathophysiology of HIV. It could help explain the biological effects that HIV has on CD4-negative cells and EVs could become biomarkers of disease progression.
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Heterogeneity of EV fractions was confirmed by probing for different vesicular protein markers.
“Heterogeneity of these different fractions was confirmed by probing for different vesicular protein markers that are present in all types of EVs and larger vesicle fractions (Flotillin-1) (Kowal et al., 2016), those typically associated with exosomes and absent in 2,000 × g (ALIX and TSG101), and GAPDH found to be enriched in the 2,000 × g and cellular fraction (McNamara et al., 2018).”
From Glioblastoma-Associated Microglia Reprogramming Is Mediated by Functional Transfer of Extracellular miR-21 (2019) · cites this paper as McNamara et al., 2018
The Materials and Methods section (“Protein analysis”; page unavailable) says the authors immunoblotted EV and control fractions using an antibody to GAPDH. It does not report GAPDH enrichment in a 2,000 × g fraction or show that this marker confirmed heterogeneity among the fractions in the citing sentence. The “EV isolation” section instead describes centrifugation at 800 × g and 16,000 × g. (LLM, conf=0.84)
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Designer Exosomes: A New Platform for Biotechnology Therapeutics
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Modern Techniques for the Isolation of Extracellular Vesicles and Viruses
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Extracellular vesicles carrying HIV-1 Nef induce long-term hyperreactivity of myeloid cells
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Inhibition of HIV Replication by Apolipoprotein A-I Binding Protein Targeting the Lipid Rafts
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Viral Membrane Fusion Proteins and RNA Sorting Mechanisms for the Molecular Delivery by Exosomes
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Self-citationExosomes in Clinical Laboratory: From Biomarker Discovery to Diagnostic Implementation
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Self-citationEngineered Extracellular Vesicles/Exosomes as a New Tool against Neurodegenerative Diseases
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Extracellular Vesicles and Their Use as Vehicles of Immunogens
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Romero‐Castillo, I., López‐García, A., Diebold, Y., & García-Posadas, L. (2024) · Scientific Reports · doi:10.1038/s41598-024-79481-1 · Cited by 2 · see citing works
EMAPII: A Key Player in HIV-Nef–induced Pulmonary Vasculopathy
Shamskhou, E. A., Verghese, L., Yuan, K., & Pérez, V. D. J. (2018) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2018-0327ed · Cited by 2 · see citing works
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Scott‐Weathers, C., King, K., Baisa, G. A., Hural, J., & Luke, K. (2025) · Extracellular Vesicle · doi:10.1016/j.vesic.2025.100084 · Cited by 1 · see citing works
Nef as a driver of immunodeficiency and HIV-associated diseases: insights from mouse models
Yakovleva, A. S., Gorshkova, E. A., Gubernatorova, E. O., Bukrinsky, M., Недоспасов, С. А., & Drutskaya, M. S. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1837301 · Cited by 1 · see citing works
Goody, P. R., Jansen, F., & Nickenig, G. (2019) · Circulation Research · doi:10.1161/circresaha.119.315908 · Cited by 1 · see citing works
Nynatten, L. R. V., Johnson, A. L., Dirk, B. S., Pawlak, E. N., Jacob, R. A., Haeryfar, S. M. M., & Dikeakos, J. D. (2018) · Viruses · doi:10.3390/v10090493
- Authors
- McNamara, R. P., Costantini, L. M., Myers, T. A., Schouest, B., Maness, N. J., Griffith, J. D., Damania, B. A., MacLean, A. G., & Dittmer, D. P.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Tulane National Primate Research Center, Tulane University, Covington, Louisiana, USA
- Tulane University (US)
- Corresponding author
- MacLean, Andrew G.
- Dittmer, Dirk P.
- ORCID
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2018-03-07
- Volume
- 9
- Issue
- 1
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- PMC
- PMC5801467
- OpenAlex
- W2790992461
- Cited by
- 109
- References
- 85
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 9 · 2023: 8 · 2022: 12 · 2021: 16 · 2020: 19 · 2019: 17 · 2018: 10
- FWCI
- 5.51
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- HHS | NIH | National Cancer Institute (CA016086)
- HHS | National Institutes of Health (OD11104, K12GM000678)
- HHS | NIH | National Institute of Allergy and Infectious Diseases (T32AI007151)
- HHS | NIH | National Institute of General Medical Sciences (MH07544)
- HHS| NIH| National Institute of General Medical Sciences (MH113517)
- HHS | NIH | National Institute on Drug Abuse (DA040394)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- HIV-1 Nef, extracellular vesicles, exosomes, exosome biogenesis, HIV pathogenesis, CD4-negative cells, AIDS progression, intercellular protein transfer
- MeSH terms
- Animals, Cells, Cultured, Humans, Macaca, Simian Immunodeficiency Virus, HIV-1, Gene Products, nef, Protein Transport, Exosomes
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