Infection of Dendritic Cells (DCs), Not DC-SIGN-Mediated Internalization of Human Immunodeficiency Virus, Is Required for Long-Term Transfer of Virus to T Cells
Open accessAbstract
The C-type lectin DC-SIGN expressed on immature dendritic cells (DCs) captures human immunodeficiency virus (HIV) particles and enhances the infection of CD4 + T cells. This process, known as trans -enhancement of T-cell infection, has been related to HIV endocytosis. It has been proposed that DC-SIGN targets HIV to a nondegradative compartment within DCs and DC-SIGN-expressing cells, allowing incoming virus to persist for several days before infecting target cells. In this study, we provide several lines of evidence suggesting that intracellular storage of intact virions does not contribute to HIV transmission. We show that endocytosis-defective DC-SIGN molecules enhance T-cell infection as efficiently as their wild-type counterparts, indicating that DC-SIGN-mediated HIV internalization is dispensable for trans -enhancement. Furthermore, using immature DCs that are genetically resistant to infection, we demonstrate that several days after viral uptake, HIV transfer from DCs to T cells requires viral fusion and occurs exclusively through DC infection and transmission of newly synthesized viral particles. Importantly, our results suggest that DC-SIGN participates in this process by cooperating with the HIV entry receptors to facilitate cis -infection of immature DCs and subsequent viral transfer to T cells. We suggest that such a mechanism, rather than intracellular storage of incoming virus, accounts for the long-term transfer of HIV to CD4 + T cells and may contribute to the spread of infection by DCs.
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Later, immature DCs become productively infected and transmit viral particles produced de novo to T cells in the cis-infection process.
“Later, immature DCs become productively infected, and transmit viral particles produced de novo to T cells in the cis-infection process [66,67,69,70].”
From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [69]
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“, by becoming productively infected and passing virus to T cells (11, 35, 38, 47, 66), by transmitting virus through an infectious synapse of DCs and T cells (1, 45), or by capturing virions in the absence of productive infection and transferring the virus to CD4 T cells in trans (3, 26, 27, 29, 30, 65, 68, 70, 71).”
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“DC-SIGN can also markedly enhance the efficiency of HIV infection in cis when DC-SIGN is present on cells that express limiting levels of CD4 and a coreceptor (11, 28, 36).”
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Hijazi, K., Wang, Y., Scala, C., Jeffs, S. A., Longstaff, C., Stieh, D. J., Haggarty, B., Vanham, G., Schols, D., Balzarini, J. M., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028307 · Cited by 39 · see citing works
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“Immature DCs allow productive HIV-1 replication and long-term viral dissemination [6-8].”
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“The LL sequence was demonstrated previously to be an internalization or endocytic motif for DC-SIGN [12, 13, 17].”
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“mucosal surfaces or in lymphnodes (28).”
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“Trans-infection mediated by DCs can occur across infectious synapses [8,9,11] and via exocytosis of virusassociated exosomes [36], whereas the cis-infection route relies on de novo virus infection of DCs and long-term transmission of HIV-1 [7,9,37,38].”
BackgroundVirion-Associated Vpr Alleviates a Postintegration Block to HIV-1 Infection of Dendritic Cells
Miller, C. M., Akiyama, H., Agosto, L. M., Emery, A., Ettinger, C. R., Swanstrom, R. I., Henderson, A. J., & Gummuluru, S. (2017) · Journal of Virology · doi:10.1128/jvi.00051-17 · Cited by 34 · see citing works
Mercier, S. K., Donaghy, H., Botting, R., Turville, S., Harman, A., Nasr, N., Ji, H., Kusebauch, U., Mendoza, L., Shteynberg, D. D., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003700 · Cited by 35 · see citing works
“Both immature and mature DCs are able to transfer HIV-1 to T lymphocytes by different mechanisms during 2 sequential phases of uptake, the first following vesicular uptake and the second after de novo infection of DCs transfer [18–21].”
BackgroundThe multiple facets of HIV attachment to dendritic cell lectins
Tsegaye, T., & Pöhlmann, S. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2010.01519.x · Cited by 35 · see citing works
“Irrespective of the route of HIV trafficking, there is ample evidence that HIV capture does not preserve viral infectivity (Turville et al., 2004; Nobile et al., 2005; Burleigh et al., 2006; Wang et al., 2007a) , with the initially postulated conservation of viral infectivity likely being due to productive infection o…”
BackgroundStefanidou, M., Herrera, C., Armanasco, N., & Shattock, R. J. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00399-12 · Cited by 24 · see citing works
Janas, A. M., Dong, C., Wang, J.-H., & Wu, L. (2008) · Virology · doi:10.1016/j.virol.2008.01.044 · Cited by 33 · see citing works
“HIV-1 infection of DCs can lead to virus production and long-term viral transmission (Burleigh et al., 2006; Dong et al., 2007; Ganesh et al., 2004; Granelli-Piperno et al., 1998; Lore et al., 2005; Nobile et al., 2005; Smed-Sorensen et al., 2005; Turville et al., 2004), suggesting that…”
BackgroundInfluentialHIV endocytosis after dendritic cell to T cell viral transfer leads to productive virus infection.
Clotet-Codina, I., Bosch, B., Senserrich, J., Férnandez-Figueras, M., Peña, R., Ballana, E., Bofill, M., Clotet, B., & Esté, J. (2009) · Antiviral Research · doi:10.1016/j.antiviral.2009.03.009 · Cited by 31 · see citing works
Role of macrophages in HIV infection and persistence
Venzke, S., & Keppler, O. (2006) · Expert Review of Clinical Immunology · doi:10.1586/1744666x.2.4.613 · Cited by 30 · see citing works
Dufrançais, O., Mascarau, R., Poincloux, R., Maridonneau‐Parini, I., Raynaud‐Messina, B., & Vérollet, C. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03875-x · Cited by 40 · see citing works
Gelais, C. S., Coleman, C. M., Wang, J., & Wu, L. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034521 · Cited by 28 · see citing works
“Immature DCs allow productive HIV-1 replication and long-term viral dissemination [5,6,7,8,9].”
BackgroundExtracellular ATP reduces HIV-1 transfer from immature dendritic cells to CD4+ T lymphocytes
Barat, C., Gilbert, C., Imbeault, M., & Tremblay, M. (2008) · Retrovirology · doi:10.1186/1742-4690-5-30 · Cited by 27 · see citing works
“In Raji-DC-SIGN cells, viruses are transferred exclusively through DC-SIGN binding and only DC-bound viruses are transferred, whereas several studies suggest that in human primary iDCs internalized viruses are transferred [7-11] and not exclusively through DC-SIGN binding [5, 16 ].”
BackgroundInfluentialPeressin, M., Holl, V., Schmidt, S., Decoville, T., Mirisky, D., Lederle, A., Delaporte, M., Xu, K., Aubertin, A., & Moog, C. (2010) · Journal of Virology · doi:10.1128/jvi.01619-10 · Cited by 26 · see citing works
“DC-SIGN efficiently binds HIV particles; this binding may favor close proximity between HIV and neighboring CD4 receptors and, in this way, trigger virus fusion (5).”
BackgroundFrank, I., Stossel, H., Gettie, A., Turville, S., Bess, J., Lifson, J., Sivin, I., Romani, N., & Robbiani, M. (2008) · Journal of Virology · doi:10.1128/jvi.01987-07 · Cited by 26 · see citing works
“The second phase involves de novo replication of CCR5-tropic viruses (R5 viruses) in infected immature DCs and probably serves as a longer lasting source of infectious virus (7, 42, 63).”
BackgroundPeering into the HIV reservoir
García, M., Buzón, M. J., Benito, J. M., & Rallón, N. I. (2018) · Reviews in Medical Virology · doi:10.1002/rmv.1981 · Cited by 29 · see citing works
González, N., Bermejo, M., Calonge, E., Jolly, C., Arenzana-Seisdedos, F., Pablos, J., Sattentau, Q., & Alcamí, J. (2010) · Journal of Virology · doi:10.1128/jvi.02449-09 · Cited by 25 · see citing works
“A two-phase transfer of HIV-1 from MDDCs to lymphocytes has been previously described elsewhere as follows: an early short-term phase of viral transfer in trans, caused by the direct binding of viral particles to DC-SIGN or other molecules at the surfaces of the MDDCs, and then a later long-term transfer phase (from 4…”
BackgroundSelf-citationHIV microbicides: state-of-the-art and new perspectives on the development of entry inhibitors.
Reina, J., Bernardi, A., Clerici, M., & Rojo, J. (2010) · Future Medicinal Chemistry · doi:10.4155/fmc.10.203 · Cited by 24 · see citing works
Modulation of HIV and SIV neutralization sensitivity by DC-SIGN and mannose-binding lectin.
Marzi, A., Mitchell, D., Chaipan, C., Fisch, T., Doms, R., Carrington, M., Desrosiers, R., & Pöhlmann, S. (2007) · Virology · doi:10.1016/j.virol.2007.07.004 · Cited by 24 · see citing works
“Moreover, it should be noted that DC-SIGN can augment cisand trans-infection (Burleigh et al., 2006; Lee et al., 2001; Nobile et al., 2005; Turville et al., 2004) and it can not be excluded that a minor part of the transmission activity of the BTHP cell lines examined here was due to progeny virus released from infect…”
BackgroundRole of Glycosphingolipids in Dendritic Cell-Mediated HIV-1 Trans-infection
Puryear, W. B., & Gummuluru, S. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-4433-6_5 · Cited by 26 · see citing works
“Productive or cis-infection of DCs, though feasible (Burleigh et al. 2006; Turville et al. 2004; Cameron et al. 2007), is ineffective for a myriad of reasons, including low CD4/CCR5 levels on the DC surface (Lee et al. 1999), as well as the presence of potent interferondependent (Granelli-Piperno…”
BackgroundCorrection: Listeria monocytogenes Traffics from Maternal Organs to the Placenta and Back
Bakardjiev, A., Theriot, J., & Portnoy, D. (2006) · PLoS Pathogens · doi:10.1371/journal.ppat.0020080 · Cited by 19
“Recent evidence suggests that infection of DC cells is required for efficient transfer of HIV-1 to other cells [122].”
Regulatory T Cells Diminish HIV Infection in Dendritic Cells – Conventional CD4+ T Cell Clusters
Moreno-Fernandez, M. E., Joedicke, J. J., & Chougnet, C. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00199 · Cited by 18 · see citing works
“Additionally, DCs can transmit virus to CD4 T cells, without being themselves productively infected, through a process called trans-infection (4).”
Younan, P., Kowalski, J. P., & Kiem, H. (2014) · Molecular Therapy · doi:10.1038/mt.2013.264 · Cited by 18 · see citing works
Jan, M., Upadhyay, C., & Hioe, C. E. (2019) · iScience · doi:10.1016/j.isci.2019.10.030 · Cited by 18 · see citing works
Protective role of DC-SIGN (CD209) neck-region alleles with <5 repeat units in HIV-1 transmission.
Zhang, J., Zhang, X.-S., Fu, J.-H., Bi, Z., Arheart, K., Barreiro, L. B., Quintana-Murci, L., Pahwa, S., & Liu, H.-L. (2008) · Journal of Infectious Diseases · doi:10.1086/588710 · Cited by 17
“to HIV-1 dissemination and persistence of infection in vivo [3].”
BackgroundPathogenesis of HIV-1 infection – chosen aspects
Knysz, B., Szetela, B., & Gładysz, A. (2007) · HIV & AIDS Review · doi:10.1016/s1730-1270(10)60035-5 · Cited by 16 · see citing works
PolyICLC Exerts Pro- and Anti-HIV Effects on the DC-T Cell Milieu In Vitro and In Vivo
Aravantinou, M., Frank, I., Hallor, M., Singer, R., Tharinger, H., Kenney, J., Gettie, A., Grasperge, B., Blanchard, J., Salazar, A., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161730 · Cited by 15 · see citing works
“Cis transfer is thought to contribute especially to long-term viral transmission [11, 12, 14, 15].”
BackgroundTsunetsugu‐Yokota, Y., & Muhsen, M. (2013) · Frontiers in Microbiology · doi:10.3389/fmicb.2013.00178 · Cited by 19 · see citing works
“…2013 | Volume 4 | Article 178 | 4 “fmicb-04-00178” — 2013/7/5 — 20:51 — page 5 — #5 On the other hand, HIV-1 replication in DCs, but not DCSIGN, is required for long-term transfer of HIV from DCs to CD4+ T cells (Lore et al., 2005; Nobile et al., 2005; Burleigh et al., 2006; Wang et al., 2007).”
BackgroundImpact of human immune deficiency virus infection on hepatitis C virus infection and replication.
Parodi, C., Belmonte, L., Baré, P., de Bracco, M. D., & Ruibal-Ares, B. (2007) · Current HIV Research · doi:10.2174/157016207779316341 · Cited by 13 · see citing works
Milk Transmission of Mammalian Retroviruses
Kemeter, L. M., Birzer, A., Heym, S., & Thoma‐Kress, A. K. (2023) · Microorganisms · doi:10.3390/microorganisms11071777 · Cited by 12 · see citing works
Hertoghs, N., Geijtenbeek, T. B. H., & Ribeiro, C. M. S. (2017) · Current Opinion in Virology · doi:10.1016/j.coviro.2017.01.001 · Cited by 14 · see citing works
Dendritic Cells in HIV-1 and HCV Infection: Can They Help Win the Battle?
Sehgal, M., Khan, Z. K., Talal, A. H., & Jain, P. (2013) · Virology Research and Treatment · doi:10.4137/vrt.s11046 · Cited by 12 · see citing works
Barat, C., Gilbert, C., & Tremblay, M. (2008) · Journal of Virology · doi:10.1128/jvi.01420-08 · Cited by 12
“In fact, CD4 T-cell infection through transfer from DC leads to a more robust replication than direct infection of such cells (4, 12, 13).”
Background
- Authors
- Burleigh, L., Lozach, P.-Y., Schiffer, C., Staropoli, I., Pezo, V., Porrot, F., Canque, B., Virelizier, J.-L., Arenzana-Seisdedos, F., & Amara, A.
- Affiliations
- Unité d'Immunologie Virale
- Centre National de la Recherche Scientifique (FR)
- CNRS UMR 7151 IUH, Centre Hayem, Hôpital Saint Louis, 1 avenue Claude Vellefaux, 75475 Paris Cedex 10, France
- Institut Curie INSERM U520, 12 rue Lhomond, 75005 Paris, France
- Groupe Virus et Immunité, Institut Pasteur, 28 rue du Dr. Roux, 75724 Paris, France
- Corresponding author
- Amara, Ali
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2006-03-15
- Volume
- 80
- Issue
- 6
- Pages
- 2949-2957
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC1395470
- OpenAlex
- W1983080372
- Cited by
- 151
- References
- 0
- Citations by year
- 2025: 2 · 2023: 2 · 2022: 2 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 5 · 2017: 6 · 2016: 6 · 2015: 4 · 2014: 7 · 2013: 9 · 2012: 12
- FWCI
- 8.10
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Journal of Virology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Health Sciences › Medicine › Infectious Diseases › HIV/AIDS Research and Interventions
- Keywords
- HIV, dendritic cells, DC-SIGN, endocytosis, viral internalization, viral fusion, CD4+ T cells, HIV transmission, C-type lectin
- MeSH terms
- DC-Specific ICAM-3 Grabbing Nonintegrin, Amino Acid Sequence, Animals, Cell Line, Dendritic Cells, Humans, Molecular Sequence Data, Receptors, Cell Surface, CD4-Positive T-Lymphocytes, HIV-1, HIV Infections, Cell Adhesion Molecules, Lectins, C-Type
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