Apoptosis characterization in mononuclear blood leukocytes of HIV patients during dengue acute disease.
Acute Disease
/ epidemiology
Adult
Aged
Apoptosis
/ genetics
Brazil
/ epidemiology
CD4-CD8 Ratio
CD8-Positive T-Lymphocytes
/ immunology
Coinfection
/ blood
Dengue
/ blood
Dengue Virus
/ pathogenicity
Female
HIV
/ pathogenicity
HIV Infections
/ blood
Humans
Leukocytes, Mononuclear
/ virology
Lymphocyte Activation
/ genetics
Male
Middle Aged
Proto-Oncogene Proteins c-bcl-2
/ genetics
T-Lymphocyte Subsets
/ immunology
Young Adult
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
14 04 2020
14 04 2020
Historique:
received:
02
09
2019
accepted:
18
03
2020
entrez:
15
4
2020
pubmed:
15
4
2020
medline:
1
12
2020
Statut:
epublish
Résumé
Dengue virus (DENV) co-circulation in Brazil represents a challenge for treatment and vaccine development. Despite public health impact, the occurrence of coinfections with other viruses is a common event. Increased T cell activation and altered inflammatory response are found during DENV coinfection with Human Immunodeficiency Virus (HIV) impacting HIV-pathogenesis. Even with Antiretroviral therapy (ART), HIV- treated patients had chronic immune activation and lymphocyte apoptosis. However, apoptotic mechanisms have not been investigated during coinfection with DENV. Our attention was attracted to apoptotic cell markers expressions in PBMCs from DENV and DENV/HIV coinfected patients. We found CD4/CD8 ratio inversion in most coinfected patients. CD4 T and CD8 T-cell subsets from DENV and DENV/HIV groups expressed low levels of anti-apoptotic protein Bcl-2. Furthermore, CD8 CD95 double positive cells frequency expressing low levels of Bcl-2 were significantly higher in these patients. Additionally, the density of Bcl-2 on classical monocytes (CD14
Identifiants
pubmed: 32286360
doi: 10.1038/s41598-020-62776-4
pii: 10.1038/s41598-020-62776-4
pmc: PMC7156518
doi:
Substances chimiques
BCL2 protein, human
0
Proto-Oncogene Proteins c-bcl-2
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6351Références
WHO/TDR. Dengue: guidelines for diagnosis, treatment, prevention and control–New edition. World Health Organization (WHO) and the Special Programme for Research and Training in Tropical Diseases (TDR), http://whqlibdoc.who.int/publications/2009/9789241547871_eng.pdf . (2009).
Freed, E. O. HIV-1 and the host cell: an intimate association. Trends Microbiol 12, 170–177 (2004).
pubmed: 15051067
doi: 10.1016/j.tim.2004.02.001
pmcid: 15051067
Nagata, S. & Tanaka, M. Programmed cell death and the immune system. Nat Rev Immunol 17, 333–340 (2017).
pubmed: 28163302
doi: 10.1038/nri.2016.153
pmcid: 28163302
Youle, R. J. & Strasser, A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9, 47–59 (2008).
pubmed: 18097445
doi: 10.1038/nrm2308
pmcid: 18097445
Yatim, N. & Albert, M. L. Dying to replicate: the orchestration of the viral life cycle, cell death pathways, and immunity. Immunity 35, 478–490 (2011).
pubmed: 22035840
doi: 10.1016/j.immuni.2011.10.010
pmcid: 22035840
Simonelli, C. et al. Prognostic factors in human herpesvirus 8-related lymphoproliferative disorders associated with HIV infection. J Clin Oncol 24, 209; author reply 209–210 (2006).
Azeredo, E. L. et al. Activated peripheral lymphocytes with increased expression of cell adhesion molecules and cytotoxic markers are associated with dengue fever disease. Mem Inst Oswaldo Cruz 101, 437–449 (2006).
pubmed: 16951817
doi: 10.1590/S0074-02762006000400016
pmcid: 16951817
Green, S. et al. Early CD69 expression on peripheral blood lymphocytes from children with dengue hemorrhagic fever. J Infect Dis 180, 1429–1435 (1999).
pubmed: 10515800
doi: 10.1086/315072
pmcid: 10515800
de-Oliveira-Pinto, L. M. et al. Regulation of inflammatory chemokine receptors on blood T cells associated to the circulating versus liver chemokines in dengue fever. PLoS One 7, e38527 (2012).
pubmed: 22815692
pmcid: 3398008
doi: 10.1371/journal.pone.0038527
Limonta, D., Capo, V., Torres, G., Perez, A. B. & Guzman, M. G. Apoptosis in tissues from fatal dengue shock syndrome. J Clin Virol 40, 50–54 (2007).
pubmed: 17693133
doi: 10.1016/j.jcv.2007.04.024
pmcid: 17693133
Castillo, J. A. & Urcuqui-Inchima, S. Mechanisms of monocyte cell death triggered by dengue virus infection. Apoptosis 23, 576–586 (2018).
pubmed: 30267240
doi: 10.1007/s10495-018-1488-1
pmcid: 30267240
Torrentes-Carvalho, A. et al. Dengue-2 infection and the induction of apoptosis in human primary monocytes. Mem Inst Oswaldo Cruz 104, 1091–1099 (2009).
pubmed: 20140369
doi: 10.1590/S0074-02762009000800005
pmcid: 20140369
Torrentes-Carvalho, A. et al. Regulation of T lymphocyte apoptotic markers is associated to cell activation during the acute phase of dengue. Immunobiology 219, 329–340 (2014).
pubmed: 24508270
doi: 10.1016/j.imbio.2013.11.002
pmcid: 24508270
Torrentes-Carvalho, A. et al. Characterization of clinical and immunological features in patients coinfected with dengue virus and HIV. Clin Immunol 164, 95–105 (2016).
pubmed: 26826597
doi: 10.1016/j.clim.2016.01.005
pmcid: 26826597
Lanciotti, R. S., Calisher, C. H., Gubler, D. J., Chang, G. J. & Vorndam, A. V. Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J Clin Microbiol 30, 545–551 (1992).
pubmed: 1372617
pmcid: 265106
doi: 10.1128/JCM.30.3.545-551.1992
Warnes, G. R. et al. Various R Programming Tools for Plotting Data. R Package Version 2.17. 0. Pittsford, NY: Computer software. [Google Scholar] (2015).
Team, R. C. A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing;. [Google Scholar] (2018).
Ryota Suzuki, Y. T. A. H. S. Hierarchical Clustering with P-Values via Multiscale Bootstrap Resampling. R package version 2.2-0, https://CRAN.R-project.org/package=pvclust (2019).
Jari Oksanen, F. G. B. et al. Community Ecology Package. R package version 2.5-6, https://CRAN.R-project.org/package=vegan (2019).
Boudet, F., Lecoeur, H. & Gougeon, M. L. Apoptosis associated with ex vivo down-regulation of Bcl-2 and up-regulation of Fas in potential cytotoxic CD8+ T lymphocytes during HIV infection. J Immunol 156, 2282–2293 (1996).
pubmed: 8690919
pmcid: 8690919
Ziegler-Heitbrock, L. Blood Monocytes and Their Subsets: Established Features and Open Questions. Front Immunol 6, 423 (2015).
pubmed: 26347746
pmcid: 4538304
doi: 10.3389/fimmu.2015.00423
Castillo, J. A., Naranjo, J. S., Rojas, M., Castano, D. & Velilla, P. A. Role of Monocytes in the Pathogenesis of Dengue. Arch Immunol Ther Exp (Warsz) 67, 27–40 (2019).
doi: 10.1007/s00005-018-0525-7
Redza-Dutordoir, M. & Averill-Bates, D. A. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta 1863, 2977–2992 (2016).
pubmed: 27646922
doi: 10.1016/j.bbamcr.2016.09.012
pmcid: 27646922
Sepasi Tehrani, H. & Moosavi-Movahedi, A. A. Catalase and its mysteries. Prog Biophys Mol Biol 140, 5–12 (2018).
pubmed: 29530789
doi: 10.1016/j.pbiomolbio.2018.03.001
pmcid: 29530789
Donalisio, M. R., Freitas, A. R. R. & Zuben, A. Arboviruses emerging in Brazil: challenges for clinic and implications for public health. Rev Saude Publica 51, 30 (2017).
pubmed: 28423140
pmcid: 5396504
doi: 10.1590/s1518-8787.2017051006889
Hottz, E. D. et al. Platelet function in HIV plus dengue coinfection associates with reduced inflammation and milder dengue illness. Sci Rep 9, 7096 (2019).
pubmed: 31068600
pmcid: 6506591
doi: 10.1038/s41598-019-43275-7
Pang, J., Thein, T. L., Lye, D. C. & Leo, Y. S. Differential clinical outcome of dengue infection among patients with and without HIV infection: a matched case-control study. Am J Trop Med Hyg 92, 1156–1162 (2015).
pubmed: 25825389
pmcid: 4458819
doi: 10.4269/ajtmh.15-0031
Azeredo, E. L. et al. Characterisation of lymphocyte response and cytokine patterns in patients with dengue fever. Immunobiology 204, 494–507 (2001).
pubmed: 11776403
doi: 10.1078/0171-2985-00058
pmcid: 11776403
Pereira, M. F., Luz, E., Netto, E. M., Barbosa, M. H. F. & Brites, C. Low variation in initial CD4 cell count in a HIV referral center, in Salvador, Brazil, from 2002 to 2015. Braz J Infect Dis 22, 245–247 (2018).
pubmed: 29883585
doi: 10.1016/j.bjid.2018.05.005
pmcid: 29883585
Khoury, Z., Silva, R. S. & Villela, W. Factors associated with a delay in seeking HIV/AIDS treatment in Sao Paulo, Brazil. AIDS Behav 19, 679–683 (2015).
pubmed: 25210003
doi: 10.1007/s10461-014-0885-x
pmcid: 25210003
Souza, P. R. Jr., Szwarcwald, C. L. & Castilho, E. A. Delay in introducing antiretroviral therapy in patients infected by HIV in Brazil, 2003–2006. Clinics (Sao Paulo) 62, 579–584 (2007).
doi: 10.1590/S1807-59322007000500008
Serrano-Villar, S. et al. HIV-infected individuals with low CD4/CD8 ratio despite effective antiretroviral therapy exhibit altered T cell subsets, heightened CD8+ T cell activation, and increased risk of non-AIDS morbidity and mortality. PLoS Pathog 10, e1004078 (2014).
pubmed: 24831517
pmcid: 4022662
doi: 10.1371/journal.ppat.1004078
Bruno, G., Saracino, A., Monno, L. & Angarano, G. The Revival of an “Old” Marker: CD4/CD8 Ratio. AIDS Rev 19, 81–88 (2017).
pubmed: 28182620
pmcid: 28182620
Mongkolsapaya, J. et al. T cell responses in dengue hemorrhagic fever: are cross-reactive T cells suboptimal? Journal of immunology 176, 3821–3829 (2006).
doi: 10.4049/jimmunol.176.6.3821
Limonta, D. et al. Apoptotic mediators in patients with severe and non-severe dengue from Brazil. J Med Virol 86, 1437–1447 (2014).
pubmed: 24170344
doi: 10.1002/jmv.23832
pmcid: 24170344
Limjindaporn, T. et al. Sensitization to Fas-mediated apoptosis by dengue virus capsid protein. Biochemical and biophysical research communications 362, 334–339 (2007).
pubmed: 17707345
doi: 10.1016/j.bbrc.2007.07.194
pmcid: 17707345
Mongkolsapaya, J. et al. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 9, 921–927 (2003).
pubmed: 12808447
doi: 10.1038/nm887
pmcid: 12808447
Tillmann, H. L. et al. Infection with GB virus C and reduced mortality among HIV-infected patients. N Engl J Med 345, 715–724 (2001).
pubmed: 11547740
doi: 10.1056/NEJMoa010398
pmcid: 11547740
Moenkemeyer, M., Schmidt, R. E., Wedemeyer, H., Tillmann, H. L. & Heiken, H. GBV-C coinfection is negatively correlated to Fas expression and Fas-mediated apoptosis in HIV-1 infected patients. J Med Virol 80, 1933–1940 (2008).
pubmed: 18814245
doi: 10.1002/jmv.21305
pmcid: 18814245
Wong, M. E., Jaworowski, A. & Hearps, A. C. The HIV Reservoir in Monocytes and Macrophages. Front Immunol 10, 1435 (2019).
pubmed: 31297114
pmcid: 6607932
doi: 10.3389/fimmu.2019.01435
Kwissa, M. et al. Dengue virus infection induces expansion of a CD14(+)CD16(+) monocyte population that stimulates plasmablast differentiation. Cell Host Microbe 16, 115–127 (2014).
pubmed: 24981333
pmcid: 4116428
doi: 10.1016/j.chom.2014.06.001
Azeredo, E. L. et al. Differential regulation of toll-like receptor-2, toll-like receptor-4, CD16 and human leucocyte antigen-DR on peripheral blood monocytes during mild and severe dengue fever. Immunology 130, 202–216 (2010).
pubmed: 20113369
pmcid: 2878465
doi: 10.1111/j.1365-2567.2009.03224.x
Younas, M., Psomas, C., Reynes, J. & Corbeau, P. Immune activation in the course of HIV-1 infection: Causes, phenotypes and persistence under therapy. HIV Med 17, 89–105 (2016).
pubmed: 26452565
doi: 10.1111/hiv.12310
pmcid: 26452565
Chen, P. et al. Perturbations of Monocyte Subsets and Their Association with T Helper Cell Differentiation in Acute and Chronic HIV-1-Infected Patients. Front Immunol 8, 272 (2017).
pubmed: 28348563
pmcid: 5347116
Arias, J. et al. Increased expression of cytokines, soluble cytokine receptors, soluble apoptosis ligand and apoptosis in dengue. Virology 452–453, 42–51 (2014).
pubmed: 24606681
doi: 10.1016/j.virol.2013.12.027
pmcid: 24606681
Suzuki, T. et al. Infection with flaviviruses requires BCLXL for cell survival. PLoS Pathog 14, e1007299 (2018).
pubmed: 30261081
pmcid: 6177207
doi: 10.1371/journal.ppat.1007299
Matsuda, T. et al. Dengue virus-induced apoptosis in hepatic cells is partly mediated by Apo2 ligand/tumour necrosis factor-related apoptosis-inducing ligand. J Gen Virol 86, 1055–1065 (2005).
pubmed: 15784899
pmcid: 2917180
doi: 10.1099/vir.0.80531-0
Liao, H., Xu, J. & Huang, J. FasL/Fas pathway is involved in dengue virus induced apoptosis of the vascular endothelial cells. J Med Virol 82, 1392–1399 (2010).
pubmed: 20572077
doi: 10.1002/jmv.21815
pmcid: 20572077
Cummins, N. W. & Badley, A. D. Mechanisms of HIV-associated lymphocyte apoptosis: 2010. Cell Death Dis 1, e99 (2010).
pubmed: 21368875
pmcid: 3032328
doi: 10.1038/cddis.2010.77
Massanella, M. et al. Assessing main death pathways in T lymphocytes from HIV infected individuals. Cytometry A 83, 648–658 (2013).
pubmed: 23650261
doi: 10.1002/cyto.a.22299
pmcid: 23650261
Rizza, S. A. & Badley, A. D. HIV protease inhibitors impact on apoptosis. Med Chem 4, 75–79, https://doi.org/10.2174/157340608783331443 (2008).
doi: 10.2174/157340608783331443
pubmed: 18220972
pmcid: 3149800
Badley, A. D. et al. In vivo analysis of Fas/FasL interactions in HIV-infected patients. J Clin Invest 102, 79–87 (1998).
pubmed: 9649560
pmcid: 509068
doi: 10.1172/JCI2691
Badley, A. D. et al. Dynamic correlation of apoptosis and immune activation during treatment of HIV infection. Cell Death Differ 6, 420–432, https://doi.org/10.1038/sj.cdd.4400509 (1999).
doi: 10.1038/sj.cdd.4400509
pubmed: 10381636
pmcid: 10381636
Ehrhard, S. et al. Effect of antiretroviral therapy on apoptosis markers and morphology in peripheral lymph nodes of HIV-infected individuals. Infection 36, 120–129 (2008).
pubmed: 18379725
doi: 10.1007/s15010-008-7368-9
pmcid: 18379725
Sevilya, Z. et al. Killing of Latently HIV-Infected CD4 T Cells by Autologous CD8 T Cells Is Modulated by Nef. Front Immunol 9, 2068 (2018).
pubmed: 30254642
pmcid: 6141733
doi: 10.3389/fimmu.2018.02068
Verhagen, A. M. et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102, 43–53 (2000).
pubmed: 10929712
doi: 10.1016/S0092-8674(00)00009-X
pmcid: 10929712
Verhagen, A. M. et al. HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J Biol Chem 277, 445–454 (2002).
pubmed: 11604410
doi: 10.1074/jbc.M109891200
pmcid: 11604410
Vasudevan, D. & Ryoo, H. D. Regulation of Cell Death by IAPs and Their Antagonists. Curr Top Dev Biol 114, 185–208 (2015).
pubmed: 26431568
pmcid: 4861076
doi: 10.1016/bs.ctdb.2015.07.026
Schimmer, A. D. Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res 64, 7183–7190 (2004).
pubmed: 15492230
doi: 10.1158/0008-5472.CAN-04-1918
pmcid: 15492230