HIV-1 Tat protein induces DNA damage in human peripheral blood B-lymphocytes via mitochondrial ROS production
Human immunodeficiency virus (HIV) infection is associated with B-cell malignancies in patients though HIV-1 is not able to infect B-cells. The rate of B-cell lymphomas in HIV-infected individuals remains high even under the combined antiretroviral therapy (cART) that reconstitutes the immune functi...
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| Published in | Redox biology Vol. 15; no. C; pp. 97 - 108 |
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| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier B.V
01.05.2018
Elsevier |
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| Abstract | Human immunodeficiency virus (HIV) infection is associated with B-cell malignancies in patients though HIV-1 is not able to infect B-cells. The rate of B-cell lymphomas in HIV-infected individuals remains high even under the combined antiretroviral therapy (cART) that reconstitutes the immune function. Thus, the contribution of HIV-1 to B-cell oncogenesis remains enigmatic. HIV-1 induces oxidative stress and DNA damage in infected cells via multiple mechanisms, including viral Tat protein. We have detected elevated levels of reactive oxygen species (ROS) and DNA damage in B-cells of HIV-infected individuals. As Tat is present in blood of infected individuals and is able to transduce cells, we hypothesized that it could induce oxidative DNA damage in B-cells promoting genetic instability and malignant transformation. Indeed, incubation of B-cells isolated from healthy donors with purified Tat protein led to oxidative stress, a decrease in the glutathione (GSH) levels, DNA damage and appearance of chromosomal aberrations. The effects of Tat relied on its transcriptional activity and were mediated by NF-κB activation. Tat stimulated oxidative stress in B-cells mostly via mitochondrial ROS production which depended on the reverse electron flow in Complex I of respiratory chain. We propose that Tat-induced oxidative stress, DNA damage and chromosomal aberrations are novel oncogenic factors favoring B-cell lymphomas in HIV-1 infected individuals.
[Display omitted]
•B-cells of HIV-infected individuals exhibit elevated levels of oxidative stress, DNA damage and chromosomal aberrations.•Purified HIV-1 Tat protein reproduces this effect and induces oxidative stress and DNA damage in B-cells.•HIV-1 Tat induces mitochondrial oxidative stress and activates NF-kB in B-cells.•This condition increases the risk of developing chromosomal abnormalities and translocations. |
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| AbstractList | Human immunodeficiency virus (HIV) infection is associated with B-cell malignancies in patients though HIV-1 is not able to infect B-cells. The rate of B-cell lymphomas in HIV-infected individuals remains high even under the combined antiretroviral therapy (cART) that reconstitutes the immune function. Thus, the contribution of HIV-1 to B-cell oncogenesis remains enigmatic. HIV-1 induces oxidative stress and DNA damage in infected cells via multiple mechanisms, including viral Tat protein. We have detected elevated levels of reactive oxygen species (ROS) and DNA damage in B-cells of HIV-infected individuals. As Tat is present in blood of infected individuals and is able to transduce cells, we hypothesized that it could induce oxidative DNA damage in B-cells promoting genetic instability and malignant transformation. Indeed, incubation of B-cells isolated from healthy donors with purified Tat protein led to oxidative stress, a decrease in the glutathione (GSH) levels, DNA damage and appearance of chromosomal aberrations. The effects of Tat relied on its transcriptional activity and were mediated by NF-κB activation. Tat stimulated oxidative stress in B-cells mostly via mitochondrial ROS production which depended on the reverse electron flow in Complex I of respiratory chain. We propose that Tat-induced oxidative stress, DNA damage and chromosomal aberrations are novel oncogenic factors favoring B-cell lymphomas in HIV-1 infected individuals. Human immunodeficiency virus (HIV) infection is associated with B-cell malignancies in patients though HIV-1 is not able to infect B-cells. The rate of B-cell lymphomas in HIV-infected individuals remains high even under the combined antiretroviral therapy (cART) that reconstitutes the immune function. Thus, the contribution of HIV-1 to B-cell oncogenesis remains enigmatic. HIV-1 induces oxidative stress and DNA damage in infected cells via multiple mechanisms, including viral Tat protein. We have detected elevated levels of reactive oxygen species (ROS) and DNA damage in B-cells of HIV-infected individuals. As Tat is present in blood of infected individuals and is able to transduce cells, we hypothesized that it could induce oxidative DNA damage in B-cells promoting genetic instability and malignant transformation. Indeed, incubation of B-cells isolated from healthy donors with purified Tat protein led to oxidative stress, a decrease in the glutathione (GSH) levels, DNA damage and appearance of chromosomal aberrations. The effects of Tat relied on its transcriptional activity and were mediated by NF-κB activation. Tat stimulated oxidative stress in B-cells mostly via mitochondrial ROS production which depended on the reverse electron flow in Complex I of respiratory chain. We propose that Tat-induced oxidative stress, DNA damage and chromosomal aberrations are novel oncogenic factors favoring B-cell lymphomas in HIV-1 infected individuals. fx1 • B-cells of HIV-infected individuals exhibit elevated levels of oxidative stress, DNA damage and chromosomal aberrations. • Purified HIV-1 Tat protein reproduces this effect and induces oxidative stress and DNA damage in B-cells. • HIV-1 Tat induces mitochondrial oxidative stress and activates NF-kB in B-cells. • This condition increases the risk of developing chromosomal abnormalities and translocations. Human immunodeficiency virus (HIV) infection is associated with B-cell malignancies in patients though HIV-1 is not able to infect B-cells. The rate of B-cell lymphomas in HIV-infected individuals remains high even under the combined antiretroviral therapy (cART) that reconstitutes the immune function. Thus, the contribution of HIV-1 to B-cell oncogenesis remains enigmatic. HIV-1 induces oxidative stress and DNA damage in infected cells via multiple mechanisms, including viral Tat protein. We have detected elevated levels of reactive oxygen species (ROS) and DNA damage in B-cells of HIV-infected individuals. As Tat is present in blood of infected individuals and is able to transduce cells, we hypothesized that it could induce oxidative DNA damage in B-cells promoting genetic instability and malignant transformation. Indeed, incubation of B-cells isolated from healthy donors with purified Tat protein led to oxidative stress, a decrease in the glutathione (GSH) levels, DNA damage and appearance of chromosomal aberrations. The effects of Tat relied on its transcriptional activity and were mediated by NF-κB activation. Tat stimulated oxidative stress in B-cells mostly via mitochondrial ROS production which depended on the reverse electron flow in Complex I of respiratory chain. We propose that Tat-induced oxidative stress, DNA damage and chromosomal aberrations are novel oncogenic factors favoring B-cell lymphomas in HIV-1 infected individuals. [Display omitted] •B-cells of HIV-infected individuals exhibit elevated levels of oxidative stress, DNA damage and chromosomal aberrations.•Purified HIV-1 Tat protein reproduces this effect and induces oxidative stress and DNA damage in B-cells.•HIV-1 Tat induces mitochondrial oxidative stress and activates NF-kB in B-cells.•This condition increases the risk of developing chromosomal abnormalities and translocations. |
| Author | Lipinski, Marс Oksenhendler, Eric Chernyak, Boris V. Germini, Diego Sheval, Eugene V. El-Amine, Rawan Dupuy, Corinne Tsfasman, Tatyana Vassetzky, Yegor S. Bilhou-Nabera, Chrystèle Hamade, Aline Najjar, Fadia Louzada, Ruy A.N. Zakharova, Vlada V. |
| AuthorAffiliation | d Doctoral school of Sciences and Technology (EDST), Lebanese University, Hadath, Lebanon g UMR 8200, Institut Gustave Roussy, CNRS, Villejuif 94805, France a UMR 8126, Paris Saclay University, Paris-Sud University, Institut Gustave Roussy, CNRS, Villejuif 94805, France f Department of Chemistry and Biochemistry, Faculty of Sciences II/EDST, Lebanese University, Jdeidet El Metn-Fanar, Lebanon c A.N. Belozersky Institute of Physico-Chemical Biology, M.V. Lomonosov Moscow State University, 119992 Moscow, Russia i Biological Hematology Service-U.F. of Onco-Hematology Cytogenetics-Hôpital Saint-Antoine, 75012 Paris, France e Department of Life and Earth Sciences, Faculty of Sciences II/Doctoral School of Sciences and Technology (EDST), Lebanese University, Jdeidet El Metn-Fanar, Lebanon h Department of Clinical Immunology, Hôpital Saint-Louis, 75010 Paris, France b LIA 1066 LFR2O French-Russian Joint Cancer Research Laboratory, 94805 Villejuif, France, 119334 Moscow, Russia |
| AuthorAffiliation_xml | – name: h Department of Clinical Immunology, Hôpital Saint-Louis, 75010 Paris, France – name: a UMR 8126, Paris Saclay University, Paris-Sud University, Institut Gustave Roussy, CNRS, Villejuif 94805, France – name: f Department of Chemistry and Biochemistry, Faculty of Sciences II/EDST, Lebanese University, Jdeidet El Metn-Fanar, Lebanon – name: b LIA 1066 LFR2O French-Russian Joint Cancer Research Laboratory, 94805 Villejuif, France, 119334 Moscow, Russia – name: c A.N. Belozersky Institute of Physico-Chemical Biology, M.V. Lomonosov Moscow State University, 119992 Moscow, Russia – name: d Doctoral school of Sciences and Technology (EDST), Lebanese University, Hadath, Lebanon – name: i Biological Hematology Service-U.F. of Onco-Hematology Cytogenetics-Hôpital Saint-Antoine, 75012 Paris, France – name: e Department of Life and Earth Sciences, Faculty of Sciences II/Doctoral School of Sciences and Technology (EDST), Lebanese University, Jdeidet El Metn-Fanar, Lebanon – name: g UMR 8200, Institut Gustave Roussy, CNRS, Villejuif 94805, France |
| Author_xml | – sequence: 1 givenname: Rawan surname: El-Amine fullname: El-Amine, Rawan organization: UMR 8126, Paris Saclay University, Paris-Sud University, Institut Gustave Roussy, CNRS, Villejuif 94805, France – sequence: 2 givenname: Diego surname: Germini fullname: Germini, Diego organization: UMR 8126, Paris Saclay University, Paris-Sud University, Institut Gustave Roussy, CNRS, Villejuif 94805, France – sequence: 3 givenname: Vlada V. surname: Zakharova fullname: Zakharova, Vlada V. organization: UMR 8126, Paris Saclay University, Paris-Sud University, Institut Gustave Roussy, CNRS, Villejuif 94805, France – sequence: 4 givenname: Tatyana surname: Tsfasman fullname: Tsfasman, Tatyana organization: UMR 8126, Paris Saclay University, Paris-Sud University, Institut Gustave Roussy, CNRS, Villejuif 94805, France – sequence: 5 givenname: Eugene V. surname: Sheval fullname: Sheval, Eugene V. organization: LIA 1066 LFR2O French-Russian Joint Cancer Research Laboratory, 94805 Villejuif, France, 119334 Moscow, Russia – sequence: 6 givenname: Ruy A.N. surname: Louzada fullname: Louzada, Ruy A.N. organization: UMR 8200, Institut Gustave Roussy, CNRS, Villejuif 94805, France – sequence: 7 givenname: Corinne surname: Dupuy fullname: Dupuy, Corinne organization: UMR 8200, Institut Gustave Roussy, CNRS, Villejuif 94805, France – sequence: 8 givenname: Chrystèle surname: Bilhou-Nabera fullname: Bilhou-Nabera, Chrystèle organization: Biological Hematology Service-U.F. of Onco-Hematology Cytogenetics-Hôpital Saint-Antoine, 75012 Paris, France – sequence: 9 givenname: Aline surname: Hamade fullname: Hamade, Aline organization: Department of Life and Earth Sciences, Faculty of Sciences II/Doctoral School of Sciences and Technology (EDST), Lebanese University, Jdeidet El Metn-Fanar, Lebanon – sequence: 10 givenname: Fadia surname: Najjar fullname: Najjar, Fadia organization: Department of Chemistry and Biochemistry, Faculty of Sciences II/EDST, Lebanese University, Jdeidet El Metn-Fanar, Lebanon – sequence: 11 givenname: Eric surname: Oksenhendler fullname: Oksenhendler, Eric organization: Department of Clinical Immunology, Hôpital Saint-Louis, 75010 Paris, France – sequence: 12 givenname: Marс surname: Lipinski fullname: Lipinski, Marс organization: UMR 8126, Paris Saclay University, Paris-Sud University, Institut Gustave Roussy, CNRS, Villejuif 94805, France – sequence: 13 givenname: Boris V. surname: Chernyak fullname: Chernyak, Boris V. organization: LIA 1066 LFR2O French-Russian Joint Cancer Research Laboratory, 94805 Villejuif, France, 119334 Moscow, Russia – sequence: 14 givenname: Yegor S. surname: Vassetzky fullname: Vassetzky, Yegor S. email: vassetzky@igr.fr organization: UMR 8126, Paris Saclay University, Paris-Sud University, Institut Gustave Roussy, CNRS, Villejuif 94805, France |
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| Keywords | HIV-1 Oxidative stress Mitochondria B-cell lymphomas Tat DNA damage |
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| Snippet | Human immunodeficiency virus (HIV) infection is associated with B-cell malignancies in patients though HIV-1 is not able to infect B-cells. The rate of B-cell... |
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| SubjectTerms | B-cell lymphomas B-Lymphocytes - pathology B-Lymphocytes - virology Cancer DNA damage DNA Damage - genetics Glutathione - metabolism HIV-1 HIV-1 - genetics HIV-1 - pathogenicity Humans Life Sciences Mitochondria Mitochondria - genetics Mitochondria - pathology NF-kappa B - genetics Oxidative stress Oxidative Stress - genetics Reactive Oxygen Species - metabolism Research Paper Signal Transduction Tat tat Gene Products, Human Immunodeficiency Virus - genetics tat Gene Products, Human Immunodeficiency Virus - metabolism |
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| Title | HIV-1 Tat protein induces DNA damage in human peripheral blood B-lymphocytes via mitochondrial ROS production |
| URI | https://dx.doi.org/10.1016/j.redox.2017.11.024 https://www.ncbi.nlm.nih.gov/pubmed/29220699 https://search.proquest.com/docview/1975034416 https://hal.science/hal-02323187 https://pubmed.ncbi.nlm.nih.gov/PMC5725280 https://doaj.org/article/af92cfdf1eaf4a13bc6ee3de81d4d529 |
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