Propolis increases Foxp3 expression and lymphocyte proliferation in HIV-infected people: A randomized, double blind, parallel-group and placebo-controlled study

UNAIDS : Joint United Nations Programme on HIV/AIDS. Global HIV & AIDS statistics - 2020 fact sheet. https://www.unaids.org/en/resources/fact-sheet. (Accessed 15 April 2021.). Hunt, 2003, T Cell activation is associated with lower CD4+ T cell gains in human immunodeficiency virus-infected patients with sustained viral suppression during antiretroviral therapy, J. Infect. Dis., 187, 1534, 10.1086/374786 French, 2009, Serum immune activation markers are persistently increased in patients with HIV infection after 6 years of antiretroviral therapy despite suppression of viral replication and reconstitution of CD4+ T cells, J. Infect. Dis., 200, 1212, 10.1086/605890 Tien, 2010, Inflammation and mortality in HIV-infected adults: analysis of the FRAM study cohort, J. Acquir Immune Defic. Syndr., 55, 316, 10.1097/QAI.0b013e3181e66216 Deeks, 2011, HIV Infection, inflammation, immunosenescence, and aging, Ann. Rev. Med., 62, 141, 10.1146/annurev-med-042909-093756 Kamat, 2012, A plasma biomarker signature of immune activation in HIV patients on antiretroviral therapy, PLoS One, 7, 1, 10.1371/journal.pone.0030881 Zicari, 2019, Immune activation, inflammation, and non-AIDS co-morbidities in HIV-infected patients under long-term ART, Viruses, 11, 200, 10.3390/v11030200 Eggena, 2005, Depletion of regulatory T cells in HIV infection is associated with immune activation, J. Immunol., 174, 4407, 10.4049/jimmunol.174.7.4407 Hsu, 2013, Serious Non-AIDS events: Immunopathogenesis and interventional strategies, AIDS Res Ther., 10, 1, 10.1186/1742-6405-10-29 Guaraldi, 2011, Premature age-related comorbidities among HIV-infected persons compared with the general population, Clin. Infect. Dis., 53, 1120, 10.1093/cid/cir627 Venkataramana, 2013, A study of biological markers in HIV disease progression and management in the highly active antiretroviral therapy (HAART) era, Am. J. Biosci. Bioeng., 1, 24 Ramana, 2014, Effect of highly active antiretroviral therapy (HAART) on human immunodeficiency virus disease pathogenesis and progression, Am. J. Public Health Res., 2, 68, 10.12691/ajphr-2-3-1 Bankova, 2005, Recent trends and important developments in propolis research, Evid. Based Complement. Alternat. Med., 2, 29, 10.1093/ecam/neh059 Bankova, 2000, Propolis: recent advances in chemistry and plant origin, Apidologie, 31, 3, 10.1051/apido:2000102 Braakhuis, 2019, Evidence on the health benefits of supplemental propolis, Nutrients, 11, 1, 10.3390/nu11112705 Berretta, 2012, Propolis standardized extract (EPP-AF®), an innovative chemically and biologically reproducible pharmaceutical compound for treating wounds, Int. J. Biol. Sci., 8, 512, 10.7150/ijbs.3641 Sforcin, 2016, Biological properties and therapeutic applications of propolis, Phytother. Res., 30, 894, 10.1002/ptr.5605 Gekker, 2005, Anti-HIV-1 activity of propolis in CD4+ lymphocyte and microglial cell cultures, J. Ethnopharmacol., 102, 158, 10.1016/j.jep.2005.05.045 V.R. Pasupuleti , L. Sammugam , N. Ramesh , S.H. Gan. Honey , Propolis, and Royal Jelly: A comprehensive review of their biological actions and health benefits. 2017 (2017) 1–21. https://doi.org/10.1155/2017/1259510. C.C.F. da Silva , A. Salatino , L.B. da Motta , G. Negri , M.L.F. Salatino . Chemical characterization, antioxidant and anti-HIV activities of a Brazilian propolis from Ceará state. 29 (2019) 309–318. https://doi.org/10.1016/j.bjp.2019.04.001. Al-Hariri, 2019, Immune’s-boosting agent: immunomodulation potentials of propolis, J. Fam. Community Med, 26, 57, 10.4103/jfcm.JFCM_46_18 Khayyal, 2003, A clinical pharmacological study of the potential beneficial effects of a propolis food product as an adjuvant in asthmatic patients, Fundam. Clin. Pharm., 17, 93, 10.1046/j.1472-8206.2003.00117.x Conti, 2015, Modulatory effects of propolis samples from Latin America (Brazil, Cuba and Mexico) on cytokine production by human monocytes, J. Pharm. Pharmacol., 67, 1431, 10.1111/jphp.12431 Bueno-Silva, 2015, Brazilian red propolis attenuates inflammatory signaling cascade in LPS-activated macrophages, PLoS One, 10, 1, 10.1371/journal.pone.0144954 Shang, 2020, Effect of propolis supplementation on C-reactive protein levels and other inflammatory factors: a systematic review and meta-analysis of randomized controlled trials, J. King Saud. Univ. Sci., 32, 1694, 10.1016/j.jksus.2020.01.003 Song, 2002, Ethanol extract of propolis inhibits nitric oxide synthase gene expression and enzyme activity, J. Ethnopharmacol., 80, 155, 10.1016/S0378-8741(02)00023-5 Hori, 2013, The inhibition of inflammasome by Brazilian propolis (EPP-AF), Evid. Based Complement. Alternat. Med., 2013, 1, 10.1155/2013/418508 Bueno-Silva, 2016, Main pathways of action of Brazilian red propolis on the modulation of neutrophils migration in the inflammatory process, Phytomedicine, 23, 1583, 10.1016/j.phymed.2016.09.009 Chan, 2013, The immunomodulatory and anticancer properties of propolis, Clin. Rev. Allergy Immunol., 44, 262, 10.1007/s12016-012-8322-2 Al Ghamdi, 2015, Oral supplementation of diabetic mice with propolis restores the proliferation capacity and chemotaxis of B and T lymphocytes towards CCL21 and CXCL12 by modulating the lipid profile, the pro-inflammatory cytokine levels and oxidative stress, BMC Immunol., 16, 1, 10.1186/s12865-015-0117-9 Silveira, 2019, Effects of Brazilian green propolis on proteinuria and renal function in patients with chronic kidney disease: a randomized, double-blind, placebo-controlled trial, BMC Nephrol., 20, 1, 10.1186/s12882-019-1337-7 Larionov, 2005, A standard curve based method for relative real time PCR data processing, BMC Bioinformatics, 6, 1, 10.1186/1471-2105-6-62 K.I. Tasca , F.L. Conte , A.C.M.M. Alves , K.B. Santiago , E.O. Cardoso , L.B. Sacilotto , B.J. Conti , J.E. Corrente , A.A. Berretta , L.R. Souza , J.M. Sforcin . Propolis intake by people living with HIV: biochemical profile, nutritional status and safety. A randomized, double-blinded, placebo-controlled clinical study. Phytother Res. Submitted. Tasca, 2012, Immunovirological parameters and cytokines in HIV infection, Rev. Soc. Bras. Med. Trop., 45, 663, 10.1590/S0037-86822012000600002 Hernandez, 2014, . HIV-1 induces the first signal to activate the NLRP3 inflammasome in monocyte-derived macrophages, Intervirology, 57, 36, 10.1159/000353902 Wacleche, 2017, The Th17 lineage: from barrier surfaces homeostasis to autoimmunity, cancer, and HIV-1 pathogenesis, Viruses, 9, 303, 10.3390/v9100303 Pina, 2018, Non-polarized cytokine profile of a long-term non-progressor HIV infected patient, Braz. J. Infect. Dis., 22, 142, 10.1016/j.bjid.2018.01.003 Gorenec, 2016, The comparison of Th1, Th2, Th9, Th17 and Th22 cytokine profiles in acute and chronic HIV-1 infection, Microb. Pathog., 97, 125, 10.1016/j.micpath.2016.06.008 Raphael, 2015, T cell subsets and their signature cytokines in autoimmune and inflammatory diseases, Cytokine, 74, 5, 10.1016/j.cyto.2014.09.011 Tien, 2010, Inflammation and mortality in HIV-infected adults: analysis of the FRAM study cohort, J. Acquir Immune Defic. Syndr., 55, 316, 10.1097/QAI.0b013e3181e66216 Pott, 2007, Effect of a four-week course of interleukin-10 on cytokine production in a placebo-controlled study of HIV-1-infected subjects, Eur. Cytokine Netw., 18, 49 Nna, 2018, Antioxidant, anti-inflammatory and synergistic anti-hyperglycemic effects of Malaysian propolis and metformin in streptozotocin–induced diabetic rats, Food Chem. Toxicol., 120, 305, 10.1016/j.fct.2018.07.028 Korish, 2011, Propolis derivatives inhibit the systemic inflammatory response and protect hepatic and neuronal cells in acute septic shock, Braz. J. Infect. Dis., 15, 332, 10.1016/S1413-8670(11)70201-X Clerici, 1993, . A Th1 → Th2 switch is a critical step in the etiology of HIV infection, Immunol. Today, 14, 1, 10.1016/0167-5699(93)90208-3 Orsilles, 2006, IL-2 and IL-10 serum levels in HIV-1-infected patients with or without active antiretroviral therapy, APMIS, 114, 55, 10.1111/j.1600-0463.2006.apm_108.x Nunnari, 2016, CD4+ T-cell gene expression of healthy donors, HIV-1 and elite controllers: immunological chaos, Cytokine, 83, 127, 10.1016/j.cyto.2016.04.007 Prendergast, 2010, HIV-1 infection is characterized by profound depletion of CD161+ Th17 cells and gradual decline in regulatory T cells, AIDS, 24, 491, 10.1097/QAD.0b013e3283344895 Piñeros, 2020, Green propolis increases myeloid suppressor cells and CD4+Foxp3+ cells and reduces Th2 inflammation in the lungs after allergen exposure, J. Ethnopharmacol., 252, 1, 10.1016/j.jep.2019.112496 Okamoto, 2012, Brazilian propolis inhibits the differentiation of Th17 cells by inhibition of interleukin-6-induced phosphorylation of signal transducer and activator of transcription 3, Immunopharmacol. Immunotoxicol., 34, 803, 10.3109/08923973.2012.657304 Okamoto, 2013, Brazilian propolis ameliorates trinitrobenzene sulfonic acid-induced colitis in mice by inhibiting Th1 differentiation, Int Immunopharmacol., 16, 178, 10.1016/j.intimp.2013.04.004 Gutiérrez, 2019, Analysis of the dysregulation between regulatory B and T cells (Breg and Treg) in human immunodeficiency virus (HIV)-infected patients, PLoS One, 1 Korencak, 2019, Effect of HIV infection and antiretroviral therapy on immune cellular functions, JCI Insight, 4, 10.1172/jci.insight.126675 Kimoto, 1998, Apoptosis and suppression of tumor growth by artepillin C extracted from Brazilian propolis, Cancer Detect. Prev., 22, 506, 10.1046/j.1525-1500.1998.00020.x Park, 2004, Immunomodulatory effect of caffeic acid phenethyl ester in Balb/c mice, Int. Immunopharmacol., 4, 429, 10.1016/j.intimp.2004.01.013 Takagi, 2005, Immune activation and radioprotection by propolis, Am. J. Chin. Med, 33, 231, 10.1142/S0192415X05002886 Azad, 2005, Novel drugs and vaccines based on the structure and function of HIV pathogenic proteins including nef, Ann. N.Y. Acad. Sci., 1056, 279, 10.1196/annals.1352.013 Mojarab, 2020, Immune responses to HIV-1 polytope vaccine candidate formulated in aqueous and alcoholic extracts of Propolis: comparable immune responses to Alum and Freund adjuvants, Microb. Pathog., 140, 10.1016/j.micpath.2019.103932 Sforcin, 2007, Propolis and the immune system: a review, J. Ethnopharmacol., 113, 1, 10.1016/j.jep.2007.05.012 Orsi, 2000, Immunomodulatory action of propolis on macrophage activation, J. Venom. Anim. Toxins, 6, 205, 10.1590/S0104-79302000000200006 Orsatti, 2010, Th1/Th2 cytokines’ expression and production by propolis-treated mice, J. Ethnopharmacol., 129, 314, 10.1016/j.jep.2010.03.030 Búfalo, 2014, The immunomodulatory effect of propolis on receptors expression, cytokine production and fungicidal activity of human monocytes, J. Pharm. Pharmacol., 66, 1497, 10.1111/jphp.12279 Conti, 2016, Propolis modulates miRNAs involved in TLR-4 pathway, NF-κB activation, cytokine production and in the bactericidal activity of human dendritic cells, J. Pharm. Pharmacol., 68, 1604, 10.1111/jphp.12628 Cardoso, 2017, Phenolic compounds alone or in combination may be involved in propolis effects on human monocytes, J. Pharm. Pharmacol., 69, 99, 10.1111/jphp.12660 Conte, 2021, Propolis from southeastern Brazil produced by Apis mellifera affects innate immunity by modulating cell marker expression, cytokine production and intracellular pathways in human monocytes, J. Pharm. Pharmacol., 73, 135, 10.1093/jpp/rgaa023