Cell-to-cell infection by HIV contributes over half of virus infection
Open accessAbstract
Cell-to-cell viral infection, in which viruses spread through contact of infected cell with surrounding uninfected cells, has been considered as a critical mode of virus infection. However, since it is technically difficult to experimentally discriminate the two modes of viral infection, namely cell-free infection and cell-to-cell infection, the quantitative information that underlies cell-to-cell infection has yet to be elucidated, and its impact on virus spread remains unclear. To address this fundamental question in virology, we quantitatively analyzed the dynamics of cell-to-cell and cell-free human immunodeficiency virus type 1 (HIV-1) infections through experimental-mathematical investigation. Our analyses demonstrated that the cell-to-cell infection mode accounts for approximately 60% of viral infection, and this infection mode shortens the generation time of viruses by 0.9 times and increases the viral fitness by 3.9 times. Our results suggest that even a complete block of the cell-free infection would provide only a limited impact on HIV-1 spread.
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Monitoring dynamics of virus spread in Jurkat cells infected with HIV-1 under static or shaking conditions revealed cell-to-cell transmission causes 60% of viral infection, shortens generation time 1.1-fold, and increases viral fitness 3.9-fold.
“Monitoring of the dynamics of virus spread in Jurkat cells infected with HIV-1, and cultivated under static or shaking conditions, revealed that cell-to-cell transmission causes 60% of viral infection, shortens the generation time of the virus 1.1-fold, and increases the viral fitness 3.9-fold.”
From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [25]
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Cites
Avoiding the void: Cell-to-cell spread of human viruses
Sattentau, Q. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1972 · Cited by 614 · see citing works
Flagged first, then by citations
Research works printed but not linked: 31
- Adachi A Gendelman HE Koenig S Folks T Willey R Rabson A Martin MA 1986 Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone Journal of Virology 59 284 291 3016298 PMC253077
- Agosto LM Zhong P Munro J Mothes W 2014 Highly active antiretroviral therapies are effective against HIV-1 cell-to-cell transmission PLOS Pathogens 10 e1003982 10.1371/journal.ppat.1003982 24586176 PMC3937346 · DOI
- Carr JM Hocking H Li P Burrell CJ 1999 Rapid and efficient cell-to-cell transmission of human immunodeficiency virus infection from monocyte-derived macrophages to peripheral blood lymphocytes Virology 265 319 329 10.1006/viro.1999.0047 10600603 · DOI
- Chen P Hübner W Spinelli MA Chen BK 2007 Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses Journal of Virology 81 12582 12595 10.1128/JVI.00381-07 17728240 PMC2169007 · DOI · Paper page
- Dimitrov DS Willey RL Sato H Chang LJ Blumenthal R Martin MA 1993 Quantitation of human immunodeficiency virus type 1 infection kinetics Journal of Virology 67 2182 2190 8445728 PMC240333
- Fukuhara M Iwami S Sato K Nishimura Y Shimizu H Aihara K Koyanagi Y 2013 Quantification of the dynamics of enterovirus 71 infection by experimental-mathematical investigation Journal of Virology 87 701 705 10.1128/JVI.01453-12 23097444 PMC3536373 · DOI
- Inaba H 2012 On a new perspective of the basic reproduction number in heterogeneous environments Journal of Mathematical Biology 65 309 348 10.1007/s00285-011-0463-z 21842424 · DOI
- Iwami S Holder BP Beauchemin CA Morita S Tada T Sato K Igarashi T Miura T 2012a Quantification system for the viral dynamics of a highly pathogenic simian/human immunodeficiency virus based on an in vitro experiment and a mathematical model Retrovirology 9 18 10.1186/1742-4690-9-18 22364292 PMC3305505 · DOI
- Iwami S Sato K De Boer RJ Aihara K Miura T Koyanagi Y 2012b Identifying viral parameters from in vitro cell cultures Frontiers in Microbiology 3 319 10.3389/fmicb.2012.00319 22969758 PMC3432869 · DOI
- Kakizoe Y Morita S Nakaoka S Takeuchi Y Sato K Miura T Beauchemin CA Iwami S 2015 A conservation law for virus infection kinetics in vitro Journal of Theoretical Biology 376 39 47 10.1016/j.jtbi.2015.03.034 25882746 · DOI
- Komarova NL Anghelina D Voznesensky I Trinité B Levy DN Wodarz D 2013a Relative contribution of free-virus and synaptic transmission to the spread of HIV-1 through target cell populations Biology Letters 9 20121049 10.1098/rsbl.2012.1049 23269844 PMC3565528 · DOI
- Komarova NL Levy DN Wodarz D 2013b Synaptic transmission and the susceptibility of HIV infection to anti-viral drugs Scientific Reports 3 2103 10.1038/srep02103 23811684 PMC3696900 · DOI
- Komarova NL Wodarz D 2013 Virus dynamics in the presence of synaptic transmission Mathematical Biosciences 242 161 171 10.1016/j.mbs.2013.01.003 23357287 PMC4122664 · DOI
- Martin N Sattentau Q 2009 Cell-to-cell HIV-1 spread and its implications for immune evasion Current Opinion in HIV and AIDS 4 143 149 10.1097/COH.0b013e328322f94a 19339954 · DOI
- Monel B Beaumont E Vendrame D Schwartz O Brand D Mammano F 2012 HIV cell-to-cell transmission requires the production of infectious virus particles and does not proceed through env-mediated fusion pores Journal of Virology 86 3924 3933 10.1128/JVI.06478-11 22258237 PMC3302491 · DOI
- Murooka TT Deruaz M Marangoni F Vrbanac VD Seung E von Andrian UH Tager AM Luster AD Mempel TR 2012 HIV-infected T cells are migratory vehicles for viral dissemination Nature 490 283 287 10.1038/nature11398 22854780 PMC3470742 · DOI · Paper page
- Nowak M May RM 2000 Virus dynamics: mathematical principles of immunology and virology: mathematical principles of immunology and virology Oxford University Press
- Nowak MA 2006 Evolutionary dynamics Harvard University Press
- Perelson AS Nelson PW 1999 Mathematical analysis of HIV-1 dynamics in vivo SIAM Review 41 3 44 10.1137/S0036144598335107 · DOI
- Perelson AS 2002 Modelling viral and immune system dynamics Nature Reviews Immunology 2 28 36 10.1038/nri700 11905835 · DOI
- Sato H Orenstein J Dimitrov D Martin M 1992 Cell-to-cell spread of HIV-1 occurs within minutes and may not involve the participation of virus particles Virology 186 712 724 10.1016/0042-6822(92)90038-Q 1370739 · DOI
- Sato K Izumi T Misawa N Kobayashi T Yamashita Y Ohmichi M Ito M Takaori-Kondo A Koyanagi Y 2010 Remarkable lethal G-to-A mutations in vif-proficient HIV-1 provirus by individual APOBEC3 proteins in humanized mice Journal of Virology 84 9546 9556 10.1128/JVI.00823-10 20610708 PMC2937654 · DOI
- Sato K Misawa N Nie C Satou Y Iwakiri D Matsuoka M Takahashi R Kuzushima K Ito M Takada K Koyanagi Y 2011 A novel animal model of Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis in humanized mice Blood 117 5663 5673 10.1182/blood-2010-09-305979 21467545 · DOI
- Sato K Misawa N Iwami S Satou Y Matsuoka M Ishizaka Y Ito M Aihara K An DS Koyanagi Y 2013 HIV-1 Vpr accelerates viral replication during acute infection by exploitation of proliferating CD4+ T cells in vivo PLOS Pathogens 9 e1003812 10.1371/journal.ppat.1003812 24339781 PMC3855622 · DOI
- Sato K Takeuchi JS Misawa N Izumi T Kobayashi T Kimura Y Iwami S Takaori-Kondo A Hu WS Aihara K Ito M An DS Pathak VK Koyanagi Y 2014 APOBEC3D and APOBEC3F potently promote HIV-1 diversification and evolution in humanized mouse model PLOS Pathogens 10 e1004453 10.1371/journal.ppat.1004453 25330146 PMC4199767 · DOI
- Sigal A Kim JT Balazs AB Dekel E Mayo A Milo R Baltimore D 2011 Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy Nature 477 95 98 10.1038/nature10347 21849975 · DOI
- Sourisseau M Sol-Foulon N Porrot F Blanchet F Schwartz O 2007 Inefficient human immunodeficiency virus replication in mobile lymphocytes Journal of Virology 81 1000 1012 10.1128/JVI.01629-06 17079292 PMC1797449 · DOI · Paper page
- Talbert-Slagle K Atkins KE Yan KK Khurana E Gerstein M Bradley EH Berg D Galvani AP Townsend JP 2014 Cellular superspreaders: an epidemiological perspective on HIV infection inside the body PLOS Pathogens 10 e1004092 10.1371/journal.ppat.1004092 24811311 PMC4014458 · DOI
- Titanji BK Aasa-Chapman M Pillay D Jolly C 2013 Protease inhibitors effectively block cell-to-cell spread of HIV-1 between T cells Retrovirology 10 161 10.1186/1742-4690-10-161 24364896 PMC3877983 · DOI
- Watanabe T Urano E Miyauchi K Ichikawa R Hamatake M Misawa N Sato K Ebina H Koyanagi Y Komano J 2012 The hematopoietic cell-specific Rho GTPase inhibitor ARHGDIB/D4GDI limits HIV type 1 replication AIDS Research and Human Retroviruses 28 913 922 10.1089/AID.2011.0180 21936715 · DOI
- Zhong P Agosto LM Ilinskaya A Dorjbal B Truong R Derse D Uchil PD Heidecker G Mothes W 2013 Cell-to-cell transmission can overcome multiple donor and target cell barriers imposed on cell-free HIV PLOS ONE 8 e53138 10.1371/journal.pone.0053138 23308151 PMC3538641 · DOI
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Sorted by citations
HIV-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
“Similarly, gentle shaking to inhibit cell contact formation has been utilized for the quantitative evaluation of viral transmission using experimental– mathematical modeling [25].”
Method
- Authors
- Iwami, S., Takeuchi, J. S., Nakaoka, S., Mammano, F., Clavel, F., Inaba, H., Kobayashi, T., Misawa, N., Aihara, K., Koyanagi, Y., & Sato, K.
- Affiliations
- Kyushu University (JP)
- Kyoto University (JP)
- The University of Tokyo (JP)
- Inserm (FR)
- Tokyo University of Agriculture (JP)
- Institute of Industrial Science, The University of Tokyo (JP)
- Corresponding author
- Iwami, Shingo
- Sato, Kei
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2015-10-06
- Volume
- 4
- Pages
- e08150
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC4592948
- OpenAlex
- W2196026454
- Cited by
- 161
- References
- 1
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 12 · 2023: 17 · 2022: 18 · 2021: 19 · 2020: 31 · 2019: 14 · 2018: 15 · 2017: 6 · 2016: 13 · 2015: 1
- FWCI
- 5.90
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Institutional Repositories DataBase (IRDB) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Kyoto University Research Information Repository (Kyoto University) (submittedVersion, cc-by)
- Funders
- Japan Science and Technology Agency
- Topics
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mathematical and Theoretical Epidemiology and Ecology Models
- Health Sciences › Medicine › Infectious Diseases › HIV/AIDS Research and Interventions
- Keywords
- HIV-1, virus transmission, viral fitness, mathematical modeling of viral dynamics, HIV transmission
- MeSH terms
- Humans, Models, Theoretical, HIV-1, HIV Infections, Jurkat Cells, Virus Internalization, Virus Release
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