Hyperthermia Stimulates HIV-1 Replication
Publication Date
July 12, 2012
Journal
PLOS Pathogens
Authors
Ferdinand Roesch, Oussama Meziane, Anna Kula, Sébastien Nisole, et al
Volume
8
Issue
7
Pages
e1002792
DOI
http://doi.org/10.1371/journal.ppat.1002792
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1002792
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22807676
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3395604
Europe PMC
http://europepmc.org/abstract/MED/22807676
Scopus
84864628996
Mendeley
http://www.mendeley.com/research/hyperthermia-stimulates-hiv1-replication
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Mendeley | Further Information

{"title"=>"Hyperthermia stimulates HIV-1 replication", "type"=>"journal", "authors"=>[{"first_name"=>"Ferdinand", "last_name"=>"Roesch", "scopus_author_id"=>"35485598300"}, {"first_name"=>"Oussama", "last_name"=>"Meziane", "scopus_author_id"=>"26424720300"}, {"first_name"=>"Anna", "last_name"=>"Kula", "scopus_author_id"=>"56623511900"}, {"first_name"=>"Sébastien", "last_name"=>"Nisole", "scopus_author_id"=>"55975958300"}, {"first_name"=>"Françoise", "last_name"=>"Porrot", "scopus_author_id"=>"6602764759"}, {"first_name"=>"Ian", "last_name"=>"Anderson", "scopus_author_id"=>"56457542200"}, {"first_name"=>"Fabrizio", "last_name"=>"Mammano", "scopus_author_id"=>"7006987415"}, {"first_name"=>"Ariberto", "last_name"=>"Fassati", "scopus_author_id"=>"6701807360"}, {"first_name"=>"Alessandro", "last_name"=>"Marcello", "scopus_author_id"=>"7004565839"}, {"first_name"=>"Monsef", "last_name"=>"Benkirane", "scopus_author_id"=>"55987792500"}, {"first_name"=>"Olivier", "last_name"=>"Schwartz", "scopus_author_id"=>"7006284121"}], "year"=>2012, "source"=>"PLoS Pathogens", "identifiers"=>{"scopus"=>"2-s2.0-84864628996", "issn"=>"15537366", "pui"=>"365384963", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "doi"=>"10.1371/journal.ppat.1002792", "pmid"=>"22807676", "sgr"=>"84864628996"}, "id"=>"9d79d846-eea9-3bcb-8305-98e6a4a43dc1", "abstract"=>"HIV-infected individuals may experience fever episodes. Fever is an elevation of the body temperature accompanied by inflammation. It is usually beneficial for the host through enhancement of immunological defenses. In cultures, transient non-physiological heat shock (42-45°C) and Heat Shock Proteins (HSPs) modulate HIV-1 replication, through poorly defined mechanisms. The effect of physiological hyperthermia (38-40°C) on HIV-1 infection has not been extensively investigated. Here, we show that culturing primary CD4+ T lymphocytes and cell lines at a fever-like temperature (39.5°C) increased the efficiency of HIV-1 replication by 2 to 7 fold. Hyperthermia did not facilitate viral entry nor reverse transcription, but increased Tat transactivation of the LTR viral promoter. Hyperthermia also boosted HIV-1 reactivation in a model of latently-infected cells. By imaging HIV-1 transcription, we further show that Hsp90 co-localized with actively transcribing provirus, and this phenomenon was enhanced at 39.5°C. The Hsp90 inhibitor 17-AAG abrogated the increase of HIV-1 replication in hyperthermic cells. Altogether, our results indicate that fever may directly stimulate HIV-1 replication, in a process involving Hsp90 and facilitation of Tat-mediated LTR activity.", "link"=>"http://www.mendeley.com/research/hyperthermia-stimulates-hiv1-replication", "reader_count"=>49, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>17, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>5, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>17, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>5, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>28, "Medicine and Dentistry"=>7, "Chemistry"=>2, "Social Sciences"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Chemistry"=>{"Chemistry"=>2}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>28}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>1, "United Kingdom"=>1}, "group_count"=>1}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/610652"], "description"=>"<p>A: Experimental Outline. Jurkat or primary CD4+ T cells were infected with HIV-1 NL4-3 for 2 hours at 37°C and grown at either 37°C or 39.5°C for up to 10 days. B, D. Representative experiments with Jurkat and primary CD4+ T cells, respectively. The levels of intracellular Gag were measured by flow cytometry at the indicated time points. C, E: Mean ± SD of 5 independent experiments in Jurkat and primary CD4+ T cells, respectively. The area under the curve was calculated for all time points in Jurkat cells, and for time points occurring until the appearance of the peak at 39.5°C in primary CD4+ T cells. Statistical significance was assessed by the Wilcoxon test. p<0.05(*).</p>", "links"=>[], "tags"=>["enhances", "hiv"], "article_id"=>281142, "categories"=>["Virology", "Infectious Diseases"], "users"=>["Ferdinand Roesch", "Oussama Meziane", "Anna Kula", "Sébastien Nisole", "Françoise Porrot", "Ian Anderson", "Fabrizio Mammano", "Ariberto Fassati", "Alessandro Marcello", "Monsef Benkirane", "Olivier Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002792.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hyperthermia_enhances_HIV_replication_/281142", "title"=>"Hyperthermia enhances HIV replication.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-12 00:19:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/610874"], "description"=>"<p>A: Infection of Jurkat cells with single-cycle HIV. One representative experiment is shown. Cells were infected with 5, 20, or 100 ng Gag p24 of Δ<i>env</i>(VSV)/mL/10<sup>6</sup> cells for 2 hours at 37°C or 39.5°C, washed, and grown at 37°C or 39.5°C. Gag levels were assessed by flow cytometry at 24 hours p.i. B: Infection of P4C5 cells with single-cycle HIV. One representative experiment is shown. 8×10<sup>4</sup> P4C5 cells were plated in 96-well plates. Cells were infected in triplicates with 1 or 5 ng Gag p24 of Δ<i>env</i>(VSV) and grown at 37°C or 39.5°<i>C</i>. Infection was assessed 36 hours p.i. by measuring β-Galactosidase activity (570 nm OD). C: Mean ± SD of 4 independent experiments. P4C5 cells were infected with 1 ng Gag p24 of the indicated HIV strains. Statistical significance was assessed by the Mann-Withney test. p<0.05(*). D: Infection of P4C5 cells at different temperatures. One of two representative experiments is shown. Data are mean ± SD of triplicates. Using the same protocol as in B, cells were infected with 5 ng Gag p24 of NL4-3 and grown at the indicated temperatures. E: Transduction of P4C5 and Jurkat cells with a GFP expressing lentivector (LV-GFP). One of three representative experiments is shown. P4C5 or Jurkat cells were transduced with 1, 10 or 100 ng Gag p24/mL/10<sup>6</sup> cells of LV-GFP. GFP levels were measured 24 hours later by flow cytometry.</p>", "links"=>[], "tags"=>["increases", "single-cycle", "hiv-1", "gfp"], "article_id"=>281353, "categories"=>["Virology", "Infectious Diseases"], "users"=>["Ferdinand Roesch", "Oussama Meziane", "Anna Kula", "Sébastien Nisole", "Françoise Porrot", "Ian Anderson", "Fabrizio Mammano", "Ariberto Fassati", "Alessandro Marcello", "Monsef Benkirane", "Olivier Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002792.g003", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hyperthermia_increases_infection_with_single_cycle_HIV_1_but_not_with_a_GFP_lentivector_/281353", "title"=>"Hyperthermia increases infection with single-cycle HIV-1 but not with a GFP lentivector.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-12 00:22:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/318147", "https://ndownloader.figshare.com/files/318174"], "description"=>"<div><p>HIV-infected individuals may experience fever episodes. Fever is an elevation of the body temperature accompanied by inflammation. It is usually beneficial for the host through enhancement of immunological defenses. In cultures, transient non-physiological heat shock (42–45°C) and Heat Shock Proteins (HSPs) modulate HIV-1 replication, through poorly defined mechanisms. The effect of physiological hyperthermia (38–40°C) on HIV-1 infection has not been extensively investigated. Here, we show that culturing primary CD4+ T lymphocytes and cell lines at a fever-like temperature (39.5°C) increased the efficiency of HIV-1 replication by 2 to 7 fold. Hyperthermia did not facilitate viral entry nor reverse transcription, but increased Tat transactivation of the LTR viral promoter. Hyperthermia also boosted HIV-1 reactivation in a model of latently-infected cells. By imaging HIV-1 transcription, we further show that Hsp90 co-localized with actively transcribing provirus, and this phenomenon was enhanced at 39.5°C. The Hsp90 inhibitor 17-AAG abrogated the increase of HIV-1 replication in hyperthermic cells. Altogether, our results indicate that fever may directly stimulate HIV-1 replication, in a process involving Hsp90 and facilitation of Tat-mediated LTR activity.</p> </div>", "links"=>[], "tags"=>["hyperthermia", "stimulates", "hiv-1", "replication"], "article_id"=>122796, "categories"=>["Cancer"], "users"=>["Ferdinand Roesch", "Oussama Meziane", "Anna Kula", "Sébastien Nisole", "Françoise Porrot", "Ian Anderson", "Fabrizio Mammano", "Ariberto Fassati", "Alessandro Marcello", "Monsef Benkirane", "Olivier Schwartz"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002792.s001", "https://dx.doi.org/10.1371/journal.ppat.1002792.s002"], "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Hyperthermia_Stimulates_HIV_1_Replication/122796", "title"=>"Hyperthermia Stimulates HIV-1 Replication", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-07-12 00:46:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/611325"], "description"=>"<p>A: Visualization of HIV transcription sites in U2OS HIVexo cells. One representative cell (at 37°C), displaying a co-localization of Hsp90 and nascent HIV RNA (followed with a YFP-MS2nls reporter protein) is shown. 2.5×10<sup>5</sup> U2OS HIVexo cells were plated on coverslips and grown overnight at 37°C. Cells were transfected with 50 ng of Tat and 300 ng of YFP-MS2nls. After 4 hours, cells were washed and grown overnight at 37°C or 39.5°C. B: Mean ± SD of 3 independent experiments. Cells showing a transcription spot were scored for their co-localization with Hsp90. The percentage corresponds to cells in which HIV transcription sites co-localize with Hsp90. Statistical significance was assessed by an unpaired t test p<0.05(*). C: effect of the Hsp90 inhibitor 17-AAG on single-cycle HIV infection in P4C5 cells. Mean ± SD of 4 independent experiments is shown. 2×10<sup>5</sup> P4C5 cells were infected with 30 ng Gag p24 of Δ<i>env</i>(VSV) for 2 hours at 37°C or 39.5°C, in presence of the indicated doses of 17-AAG. Cells were washed and grown at 37°C or 39.5°C at the indicated doses of 17-AAG. Cells were harvested 24 hours p.i. and Gag levels were assessed by flow cytometry. As a negative control, we used DMSO at a concentration corresponding to 250 nM 17-AAG.</p>", "links"=>[], "tags"=>["hsp90", "hiv-1", "transcription"], "article_id"=>281806, "categories"=>["Virology", "Infectious Diseases"], "users"=>["Ferdinand Roesch", "Oussama Meziane", "Anna Kula", "Sébastien Nisole", "Françoise Porrot", "Ian Anderson", "Fabrizio Mammano", "Ariberto Fassati", "Alessandro Marcello", "Monsef Benkirane", "Olivier Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002792.g007", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Role_of_Hsp90_during_HIV_1_transcription_and_replication_/281806", "title"=>"Role of Hsp90 during HIV-1 transcription and replication.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-12 00:30:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/610794"], "description"=>"<p>A: Primary CD4+ T cells were grown at 37°C or 39.5°C for 3 days. Cell growth was assessed every day by direct counting of living cells (Trypan blue exclusion). B: Primary CD4+ T cells were incubated 8 hours at 37°C or 39.5°C. Cell lysates were collected and probed by Western Blot for Hsp90, Hsp70 and Actin. C: Primary CD4+ T cells were grown at 37°C (blue line) or 39.5°C (red line) for 3 days. Cells were stained for the indicated surface markers and fixed in PFA. Isotype-matched monoclonal antibodies were used as negative controls (grey line).</p>", "links"=>[], "tags"=>["molecules", "hyperthermic"], "article_id"=>281278, "categories"=>["Virology", "Infectious Diseases"], "users"=>["Ferdinand Roesch", "Oussama Meziane", "Anna Kula", "Sébastien Nisole", "Françoise Porrot", "Ian Anderson", "Fabrizio Mammano", "Ariberto Fassati", "Alessandro Marcello", "Monsef Benkirane", "Olivier Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002792.g002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cell_growth_and_expression_of_Hsp70_Hsp90_and_surface_molecules_in_hyperthermic_T_cells_/281278", "title"=>"Cell growth and expression of Hsp70, Hsp90, and surface molecules in hyperthermic T cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-12 00:21:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/611210"], "description"=>"<p>A: Experimental outline. J-Lat 10.6 are Jurkat-derived cells carrying a latent, integrated, provirus, encoding <i>gfp</i> instead of <i>nef</i>. Stimulation of J-Lat 10.6 cells with TNFα triggers HIV-1 reactivation and GFP expression. B: Reactivation of J-Lat 10.6 cells with various stimuli. One representative experiment is shown. J-Lat 10.6 cells were treated with either TNFα, supernatants from IL-2 treated or PHA-activated PBMCs, or co-cultivated with IL-2-treated PBMCs for 48 hours at 37°C or 39.5°C. Viral reactivation was assessed by measuring GFP levels by flow cytometry. C: Mean ± SD of 4 independent experiments. Statistical significance was assessed by a paired t test. p<0.05(*).</p>", "links"=>[], "tags"=>["increases", "viral", "reactivation", "j-lat"], "article_id"=>281686, "categories"=>["Virology", "Infectious Diseases"], "users"=>["Ferdinand Roesch", "Oussama Meziane", "Anna Kula", "Sébastien Nisole", "Françoise Porrot", "Ian Anderson", "Fabrizio Mammano", "Ariberto Fassati", "Alessandro Marcello", "Monsef Benkirane", "Olivier Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002792.g006", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hyperthermia_increases_viral_reactivation_in_J_Lat_10_6_cells_/281686", "title"=>"Hyperthermia increases viral reactivation in J-Lat 10.6 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-12 00:28:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/610979"], "description"=>"<p>A: Viral fusion assay. One representative experiment is shown. Jurkat cells were exposed for 2 hours at 37°C or 39.5°C to 5 or 100 ng Gag p24/10<sup>5</sup> cells/0.1 mL of either WT, or a non fusogenic <i>env</i> mutant (F552Y) NL4-3, both bearing the chimeric protein β-lactamase-Vpr. Viral access to the cytoplasm was assessed by flow cytometry, using the ability of β-lactamase to cleave CCF2-AM, a fluorogenic substrate. B: Mean ± SD of 3 independent experiments. C: In vitro assessment of RT activity. Mean ± SD of 2 independent experiments is shown. HIV-1 NL4-3 virions were lysed and incubated at 37°C or 39.5°C for 1 h or 3 h. RT activity was measured with the Innovagen RetroSys RT Activity Kit (405 nm OD). D: Viral DNA synthesis in Jurkat cells. Mean ± SD of 3 independent experiments is shown. Jurkat cells were infected with 50 ng or 250 ng Gag p24 of Δ<i>env</i>(VSV)//mL/10<sup>6</sup> cells for 2 hours at 37°C or 39.5°C, washed, and grown at 37°C or 39.5°C. 8 hours p.i., cells were harvested and viral DNA was measured by quantitative PCR. As a control, the RT inhibitor nevirapine (NVP) was added during infection.</p>", "links"=>[], "tags"=>["viral", "fusion"], "article_id"=>281470, "categories"=>["Virology", "Infectious Diseases"], "users"=>["Ferdinand Roesch", "Oussama Meziane", "Anna Kula", "Sébastien Nisole", "Françoise Porrot", "Ian Anderson", "Fabrizio Mammano", "Ariberto Fassati", "Alessandro Marcello", "Monsef Benkirane", "Olivier Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002792.g004", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hyperthermia_does_not_stimulate_viral_fusion_and_reverse_transcription_/281470", "title"=>"Hyperthermia does not stimulate viral fusion and reverse transcription.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-12 00:24:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/611085"], "description"=>"<p>A: Levels of Tat in HeLa-LTR-Luc cells. Cells were transfected with 20 ng of Tat-Flag. After 4 hours at 37°C, cells were washed and grown at 37°C or 39.5°C for 48 hours. Tat-Flag and tubulin levels were assessed by Western Blot. B: LTR activity in HeLa cells at 37°C or 39.5°C. HeLa-LTR-Luc and HeLa-LTRΔTAR-Luc cells were transfected with 4 ng or 20 ng of Tat-Flag. After 4 hours at 37°C, cells were washed and grown at 37°C or 39.5°C. 48 hours later, luciferase levels were measured and normalized to protein concentration. Data are mean ± SD of 3 independent experiments. Statistical significance was assessed by the Mann-Withney test. p<0.05(*).</p>", "links"=>[], "tags"=>["enhances", "tat-dependent", "ltr"], "article_id"=>281567, "categories"=>["Virology", "Infectious Diseases"], "users"=>["Ferdinand Roesch", "Oussama Meziane", "Anna Kula", "Sébastien Nisole", "Françoise Porrot", "Ian Anderson", "Fabrizio Mammano", "Ariberto Fassati", "Alessandro Marcello", "Monsef Benkirane", "Olivier Schwartz"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002792.g005", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hyperthermia_enhances_Tat_dependent_LTR_transcription_/281567", "title"=>"Hyperthermia enhances Tat-dependent LTR transcription.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-07-12 00:26:07"}

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Relative Metric

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