Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection

Background: HIV-1 induces an uncontrolled inflammatory response of several immune components, such as inflammasomes. These molecular complexes, associated with Toll-like receptor (TLR) activity, induce the maturation and release of IL-1 and IL-18 and eventually induce pyroptosis. It has been previou...

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Autores:
Feria Garzón, Manuel Gerónimo
Rugeles López, María Teresa
Hernández López, Juan Carlos
Lujan, Jorge A.
Taborda, Natalia Andrea
Tipo de recurso:
Article of journal
Fecha de publicación:
2019
Institución:
Universidad Cooperativa de Colombia
Repositorio:
Repositorio UCC
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OAI Identifier:
oai:repository.ucc.edu.co:20.500.12494/16029
Acceso en línea:
https://hdl.handle.net/20.500.12494/16029
Palabra clave:
inflammasomes
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openAccess
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oai_identifier_str oai:repository.ucc.edu.co:20.500.12494/16029
network_acronym_str COOPER2
network_name_str Repositorio UCC
repository_id_str
dc.title.spa.fl_str_mv Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection
title Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection
spellingShingle Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection
inflammasomes
title_short Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection
title_full Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection
title_fullStr Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection
title_full_unstemmed Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection
title_sort Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection
dc.creator.fl_str_mv Feria Garzón, Manuel Gerónimo
Rugeles López, María Teresa
Hernández López, Juan Carlos
Lujan, Jorge A.
Taborda, Natalia Andrea
dc.contributor.author.none.fl_str_mv Feria Garzón, Manuel Gerónimo
Rugeles López, María Teresa
Hernández López, Juan Carlos
Lujan, Jorge A.
Taborda, Natalia Andrea
dc.subject.spa.fl_str_mv inflammasomes
topic inflammasomes
description Background: HIV-1 induces an uncontrolled inflammatory response of several immune components, such as inflammasomes. These molecular complexes, associated with Toll-like receptor (TLR) activity, induce the maturation and release of IL-1 and IL-18 and eventually induce pyroptosis. It has been previously demonstrated that HIV induces inflammasome activation, which is significantly lower in the gastrointestinal tissue and blood from people living with HIV-1 with spontaneous control of viral replication. Therefore, immunomodulatory agents could be useful in improving HIV prognosis. Objective: To evaluate the potential inhibitory e ect of sulfasalazine (SSZ) on inflammasomes and TLRs in peripheral blood mononuclear cells (PBMCs) from people living with HIV and healthy donors. Methods: PBMCs were obtained from 15 people living with HIV and 15 healthy donors. Cells were stimulated with agonists of TLRs and inflammasomes and subsequently treated with SSZ. The concentration of IL-1 and the relative expression of NLRP3, NLRC4, NLRP1, AIM2, ASC, Caspase-1, IL-1 , and IL-18 were quantified. Results: Cells treated with SSZ exhibited a decreased IL-1 production after inflammasome and TLR stimulation, as well as regulation of inflammasome-related genes, in both people with HIV and healthy individuals. The concentration of IL-1 was positively correlated with the CD4+ T-cell count and negatively with the viral load. Conclusion: Our results suggest that SSZ has an immunomodulatory effect on inflammasome and TLR activation that depends on the clinical HIV status.
publishDate 2019
dc.date.issued.none.fl_str_mv 2019-09-11
dc.date.accessioned.none.fl_str_mv 2020-01-16T23:42:48Z
dc.date.available.none.fl_str_mv 2020-01-16T23:42:48Z
dc.type.none.fl_str_mv Artículo
dc.type.coar.fl_str_mv http://purl.org/coar/resource_type/c_2df8fbb1
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status_str publishedVersion
dc.identifier.issn.spa.fl_str_mv 1422-0067
dc.identifier.uri.spa.fl_str_mv 10.3390/ijms20184476
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12494/16029
dc.identifier.bibliographicCitation.spa.fl_str_mv Feria-Garzón, M.G., Rugeles, M.T., Hernandez, J.C., Lujan, J. A. and Taborda, N.A. (2019). Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection. Int. J. Mol. Sci. 2019, 20, 4476; doi:10.3390/ijms20184476. Recuperado de:
identifier_str_mv 1422-0067
10.3390/ijms20184476
Feria-Garzón, M.G., Rugeles, M.T., Hernandez, J.C., Lujan, J. A. and Taborda, N.A. (2019). Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection. Int. J. Mol. Sci. 2019, 20, 4476; doi:10.3390/ijms20184476. Recuperado de:
url https://hdl.handle.net/20.500.12494/16029
dc.relation.isversionof.spa.fl_str_mv https://www.ncbi.nlm.nih.gov/pubmed/31514274
dc.relation.ispartofjournal.spa.fl_str_mv International Journal of Molecular Sciences
dc.relation.references.spa.fl_str_mv 1. Lawrence T., Gilroy D.W. Chronic inflammation: A failure of resolution? Int. J. Exp. Pathol. 2007;88:85–94. doi: 10.1111/j.1365-2613.2006.00507.x.
2. Paiardini M., Muller-Trutwin M. HIV-associated chronic immune activation. Immunol. Rev. 2013;254:78–101. doi: 10.1111/imr.12079.
3. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat. Immunol. 2010;11:373–384. doi: 10.1038/ni.1863.
4. Kanneganti T.D., Lamkanfi M., Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity. 2007;27:549–559. doi: 10.1016/j.immuni.2007.10.002.
5. Acosta-Rodriguez E.V., Napolitani G., Lanzavecchia A., Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 2007;8:942–949. doi: 10.1038/ni1496.
6. Jain A., Song R., Wakeland E.K., Pasare C. T cell-intrinsic IL-1R signaling licenses effector cytokine production by memory CD4 T cells. Nat. Commun. 2018;9:3185. doi: 10.1038/s41467-018-05489-7.
7. Revu S., Wu J., Henkel M., Rittenhouse N., Menk A., Delgoffe G.M., Poholek A.C., McGeachy M.J. IL-23 and IL-1β Drive Human Th17 Cell Differentiation and Metabolic Reprogramming in Absence of CD28 Costimulation. Cell Rep. 2018;22:2642–2653. doi: 10.1016/j.celrep.2018.02.044.
8. Coccia M., Harrison O.J., Schiering C., Asquith M.J., Becher B., Powrie F., Maloy K.J. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4(+) Th17 cells. J. Exp. Med. 2012;209:1595–1609. doi: 10.1084/jem.20111453.
9. Hernández López J.C., Urcuqui Inchima S. Activación y regulación del inflamasoma NLRP3 en las enfermedades infecciosas. Iatreia. 2012;25:380–390.
10. Yerramothu P., Vijay A.K., Willcox M.D.P. Inflammasomes, the eye and anti-inflammasome therapy. Eye (Lond.) 2018;32:491–505. doi: 10.1038/eye.2017.241.
11. Place D.E., Kanneganti T.D. Recent advances in inflammasome biology. Curr. Opin. Immunol. 2017;50:32–38. doi: 10.1016/j.coi.2017.10.011.
12. Hernandez J., Sirois C., Latz E. Activation and Regulation of the NLRP3 Inflammasome. Progress in Inflammation Research. Springer; Basel, Switzerland: 2011. pp. 197–208.
13. Broz P., Dixit V.M. Inflammasomes: Mechanism of assembly, regulation and signalling. Nat. Rev. Immunol. 2016;16:407–420. doi: 10.1038/nri.2016.58.
14. Hernandez J.C., Latz E., Urcuqui-Inchima S. HIV-1 induces the first signal to activate the NLRP3 inflammasome in monocyte-derived macrophages. Intervirology. 2014;57:36–42. doi: 10.1159/000353902.
15. Feria M.G., Taborda N.A., Hernandez J.C., Rugeles M.T. HIV replication is associated to inflammasomes activation, IL-1beta, IL-18 and caspase-1 expression in GALT and peripheral blood. PLoS ONE. 2018;13:e0192845. doi: 10.1371/journal.pone.0192845.
16. Plosker G.L., Croom K.F. Sulfasalazine: A review of its use in the management of rheumatoid arthritis. Drugs. 2015;65:1825–1849. doi: 10.2165/00003495-200565130-00008.
17. Mijiyawa M., David M. Beneficial effect of sulfasalazine in spondylarthropathy in 2 patients with HIV infection. Rev. Rhum. Ed. Fr. 1993;60:527–529.
18. Youssef P.P., Bertouch J.V., Jones P.D. Successful treatment of human immunodeficiency virus-associated Reiter’s syndrome with sulfasalazine. Arthritis Rheum. 1992;35:723–724. doi: 10.1002/art.1780350620.
19. Hunt P.W. HIV and inflammation: Mechanisms and consequences. Curr. Hiv/Aids Rep. 2012;9:139–147. doi: 10.1007/s11904-012-0118-8.
20. Wahl C., Liptay S., Adler G., Schmid R.M. Sulfasalazine: A potent and specific inhibitor of nuclear factor kappa B. J. Clin. Invest. 1998;101:1163–1174. doi: 10.1172/JCI992.
21. Bauernfeind F.G., Horvath G., Stutz A., Alnemri E.S., MacDonald K., Speert D., Fernandes-Alnemri T., Wu J., Monks B.G., Fitzgerald K.A., et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 2009;183:787–791. doi: 10.4049/jimmunol.0901363.
22. Rodenburg R.J., Ganga A., van Lent P.L., van de Putte L.B., van Venrooij W.J. The antiinflammatory drug sulfasalazine inhibits tumor necrosis factor alpha expression in macrophages by inducing apoptosis. Arthritis Rheum. 2000;43:1941–1950. doi: 10.1002/1529-0131(200009)43:9<1941::AID-ANR4>3.0.CO;2-O.
23. Volin M.V., Campbell P.L., Connors M.A., Woodruff D.C., Koch A.E. The effect of sulfasalazine on rheumatoid arthritic synovial tissue chemokine production. Exp Mol. Pathol. 2002;73:84–92. doi: 10.1006/exmp.2002.2460.
24. Perdomo-Celis F., Feria M.G., Taborda N.A., Rugeles M.T. A Low Frequency of IL-17-Producing CD8(+) T-Cells Is Associated With Persistent Immune Activation in People Living With HIV Despite HAART-Induced Viral Suppression. Front. Immunol. 2018;9:2502. doi: 10.3389/fimmu.2018.02502.
25. Anders H.J. Of Inflammasomes and Alarmins: IL-1beta and IL-1alpha in Kidney Disease. J. Am. Soc. Nephrol. 2016;27:2564–2575. doi: 10.1681/ASN.2016020177.
26. Jo E.K., Kim J.K., Shin D.M., Sasakawa C. Molecular mechanisms regulating NLRP3 inflammasome activation. Cell Mol. Immunol. 2016;13:148–159. doi: 10.1038/cmi.2015.95.
27. Groslambert M., Py B.F. Spotlight on the NLRP3 inflammasome pathway. J. Inflamm Res. 2018;11:359–374. doi: 10.2147/JIR.S141220.
28. Chang J.J., Altfeld M. Immune activation and the role of TLRs and TLR agonists in the pathogenesis of HIV-1 infection in the humanized mouse model. J. Infect. Dis. 2013;208(Suppl. 2):S145–S149. doi: 10.1093/infdis/jit402.
29. Meier A., Altfeld M. Toll-like receptor signaling in HIV-1 infection: A potential target for therapy? Expert Rev. Anti-Infect Ther. 2007;5:323–326. doi: 10.1586/14787210.5.3.323.
30. Yang J., Liu Z., Xiao T.S. Post-translational regulation of inflammasomes. Cell Mol. Immunol. 2017;14:65–79. doi: 10.1038/cmi.2016.29.
31. Zhong Z., Umemura A., Sanchez-Lopez E., Liang S., Shalapour S., Wong J., He F., Boassa D., Perkins G., Ali S.R., et al. NF-kappaB Restricts Inflammasome Activation via Elimination of Damaged Mitochondria. Cell. 2016;164:896–910. doi: 10.1016/j.cell.2015.12.057.
32. Nakahira K., Haspel J.A., Rathinam V.A., Lee S.J., Dolinay T., Lam H.C., Englert J.A., Rabinovitch M., Cernadas M., Kim H.P., et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 2011;12:222–230. doi: 10.1038/ni.1980.
33. Komatsu M., Kageyama S., Ichimura Y. p62/SQSTM1/A170: Physiology and pathology. Pharm. Res. 2012;66:457–462. doi: 10.1016/j.phrs.2012.07.004.
34. Funderburg N.T., Jiang Y., Debanne S.M., Labbato D., Juchnowski S., Ferrari B., Clagett B., Robinson J., Lederman M.M., McComsey G.A. Rosuvastatin reduces vascular inflammation and T-cell and monocyte activation in HIV-infected subjects on antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 2015;68:396–404. doi: 10.1097/QAI.0000000000000478.
35. Funderburg N.T., Jiang Y., Debanne S.M., Storer N., Labbato D., Clagett B., Robinson J., Lederman M.M., McComsey G.A. Rosuvastatin treatment reduces markers of monocyte activation in HIV-infected subjects on antiretroviral therapy. Clin. Infect. Dis. 2014;58:588–595. doi: 10.1093/cid/cit748.
36. Piconi S., Parisotto S., Rizzardini G., Passerini S., Terzi R., Argenteri B., Meraviglia P., Capetti A., Biasin M., Trabattoni D., et al. Hydroxychloroquine drastically reduces immune activation in HIV-infected, antiretroviral therapy-treated immunologic nonresponders. Blood. 2011;118:3263–3272. doi: 10.1182/blood-2011-01-329060.
37. O’Brien M., Montenont E., Hu L., Nardi M.A., Valdes V., Merolla M., Gettenberg G., Cavanagh K., Aberg J.A., Bhardwaj N., et al. Aspirin attenuates platelet activation and immune activation in HIV-1-infected subjects on antiretroviral therapy: A pilot study. J. Acquir. Immune Defic. Syndr. 2013;63:280–288. doi: 10.1097/QAI.0b013e31828a292c.
38. Cuesta E., Boada J., Perales J.C., Roig T., Bermudez J. Aspirin inhibits NF-kappaB activation in a glycolysis-depleted lung epithelial cell line. Eur. J. Pharm. 2005;517:158–164. doi: 10.1016/j.ejphar.2005.05.024.
39. Chen Y., Zhang J., Ge X., Du J., Deb D.K., Li Y.C. Vitamin D receptor inhibits nuclear factor kappaB activation by interacting with IkappaB kinase beta protein. J. Biol. Chem. 2013;288:19450–19458. doi: 10.1074/jbc.M113.467670.
40. Opravil M., Ledergerber B., Furrer H., Hirschel B., Imhof A., Gallant S., Wagels T., Bernasconi E., Meienberg F., Rickenbach M., et al. Clinical efficacy of early initiation of HAART in patients with asymptomatic HIV infection and CD4 cell count > 350 × 10(6)/l. AIDS. 2002;16:1371–1381. doi: 10.1097/00002030-200207050-00009.
41. Arcia D., Ochoa R., Hernandez J.C., Álvarez C.M., Díaz F.J., Velilla P.A., Acevedo-Sáenz L. Potential immune escape mutations under inferred selection pressure in HIV-1 strains circulating in Medellín, Colombia. Infect. Genet. Evol. 2019;69:267–278. doi: 10.1016/j.meegid.2018.07.001.
42. Shoji K.F., Debure L. Fluorometric Methods for Detection of Mitochondrial Membrane Depolarization Induced by CD95 Activation. Methods Mol. Biol. 2017;1557:49–62.
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spelling Feria Garzón, Manuel GerónimoRugeles López, María TeresaHernández López, Juan CarlosLujan, Jorge A.Taborda, Natalia Andrea20, 44762020-01-16T23:42:48Z2020-01-16T23:42:48Z2019-09-111422-006710.3390/ijms20184476https://hdl.handle.net/20.500.12494/16029Feria-Garzón, M.G., Rugeles, M.T., Hernandez, J.C., Lujan, J. A. and Taborda, N.A. (2019). Sulfasalazine as an Immunomodulator of the Inflammatory Process during HIV-1 Infection. Int. J. Mol. Sci. 2019, 20, 4476; doi:10.3390/ijms20184476. Recuperado de:Background: HIV-1 induces an uncontrolled inflammatory response of several immune components, such as inflammasomes. These molecular complexes, associated with Toll-like receptor (TLR) activity, induce the maturation and release of IL-1 and IL-18 and eventually induce pyroptosis. It has been previously demonstrated that HIV induces inflammasome activation, which is significantly lower in the gastrointestinal tissue and blood from people living with HIV-1 with spontaneous control of viral replication. Therefore, immunomodulatory agents could be useful in improving HIV prognosis. Objective: To evaluate the potential inhibitory e ect of sulfasalazine (SSZ) on inflammasomes and TLRs in peripheral blood mononuclear cells (PBMCs) from people living with HIV and healthy donors. Methods: PBMCs were obtained from 15 people living with HIV and 15 healthy donors. Cells were stimulated with agonists of TLRs and inflammasomes and subsequently treated with SSZ. The concentration of IL-1 and the relative expression of NLRP3, NLRC4, NLRP1, AIM2, ASC, Caspase-1, IL-1 , and IL-18 were quantified. Results: Cells treated with SSZ exhibited a decreased IL-1 production after inflammasome and TLR stimulation, as well as regulation of inflammasome-related genes, in both people with HIV and healthy individuals. The concentration of IL-1 was positively correlated with the CD4+ T-cell count and negatively with the viral load. Conclusion: Our results suggest that SSZ has an immunomodulatory effect on inflammasome and TLR activation that depends on the clinical HIV status.https://scienti.colciencias.gov.co/cvlac/visualizador/generarCurriculoCv.do?cod_rh=0000283088http://orcid.org/0000-0002-9200-5698https://scienti.colciencias.gov.co/gruplac/jsp/visualiza/visualizagr.jsp?nro=00000000011355juanc.hernandezl@campusucc.edu.co11Universidad Cooperativa de Colombia, Facultad de Ciencias de la Salud, Medicina, Medellín y EnvigadoMedicinaMedellínhttps://www.ncbi.nlm.nih.gov/pubmed/31514274International Journal of Molecular Sciences1. Lawrence T., Gilroy D.W. Chronic inflammation: A failure of resolution? Int. J. Exp. Pathol. 2007;88:85–94. doi: 10.1111/j.1365-2613.2006.00507.x.2. Paiardini M., Muller-Trutwin M. HIV-associated chronic immune activation. Immunol. Rev. 2013;254:78–101. doi: 10.1111/imr.12079.3. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat. Immunol. 2010;11:373–384. doi: 10.1038/ni.1863.4. Kanneganti T.D., Lamkanfi M., Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity. 2007;27:549–559. doi: 10.1016/j.immuni.2007.10.002.5. Acosta-Rodriguez E.V., Napolitani G., Lanzavecchia A., Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 2007;8:942–949. doi: 10.1038/ni1496.6. Jain A., Song R., Wakeland E.K., Pasare C. T cell-intrinsic IL-1R signaling licenses effector cytokine production by memory CD4 T cells. Nat. Commun. 2018;9:3185. doi: 10.1038/s41467-018-05489-7.7. Revu S., Wu J., Henkel M., Rittenhouse N., Menk A., Delgoffe G.M., Poholek A.C., McGeachy M.J. IL-23 and IL-1β Drive Human Th17 Cell Differentiation and Metabolic Reprogramming in Absence of CD28 Costimulation. Cell Rep. 2018;22:2642–2653. doi: 10.1016/j.celrep.2018.02.044.8. Coccia M., Harrison O.J., Schiering C., Asquith M.J., Becher B., Powrie F., Maloy K.J. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4(+) Th17 cells. J. Exp. Med. 2012;209:1595–1609. doi: 10.1084/jem.20111453.9. Hernández López J.C., Urcuqui Inchima S. Activación y regulación del inflamasoma NLRP3 en las enfermedades infecciosas. Iatreia. 2012;25:380–390.10. Yerramothu P., Vijay A.K., Willcox M.D.P. Inflammasomes, the eye and anti-inflammasome therapy. Eye (Lond.) 2018;32:491–505. doi: 10.1038/eye.2017.241.11. Place D.E., Kanneganti T.D. Recent advances in inflammasome biology. Curr. Opin. Immunol. 2017;50:32–38. doi: 10.1016/j.coi.2017.10.011.12. Hernandez J., Sirois C., Latz E. Activation and Regulation of the NLRP3 Inflammasome. Progress in Inflammation Research. Springer; Basel, Switzerland: 2011. pp. 197–208.13. Broz P., Dixit V.M. Inflammasomes: Mechanism of assembly, regulation and signalling. Nat. Rev. Immunol. 2016;16:407–420. doi: 10.1038/nri.2016.58.14. Hernandez J.C., Latz E., Urcuqui-Inchima S. HIV-1 induces the first signal to activate the NLRP3 inflammasome in monocyte-derived macrophages. Intervirology. 2014;57:36–42. doi: 10.1159/000353902.15. Feria M.G., Taborda N.A., Hernandez J.C., Rugeles M.T. HIV replication is associated to inflammasomes activation, IL-1beta, IL-18 and caspase-1 expression in GALT and peripheral blood. PLoS ONE. 2018;13:e0192845. doi: 10.1371/journal.pone.0192845.16. Plosker G.L., Croom K.F. Sulfasalazine: A review of its use in the management of rheumatoid arthritis. Drugs. 2015;65:1825–1849. doi: 10.2165/00003495-200565130-00008.17. Mijiyawa M., David M. Beneficial effect of sulfasalazine in spondylarthropathy in 2 patients with HIV infection. Rev. Rhum. Ed. Fr. 1993;60:527–529.18. Youssef P.P., Bertouch J.V., Jones P.D. Successful treatment of human immunodeficiency virus-associated Reiter’s syndrome with sulfasalazine. Arthritis Rheum. 1992;35:723–724. doi: 10.1002/art.1780350620.19. Hunt P.W. HIV and inflammation: Mechanisms and consequences. Curr. Hiv/Aids Rep. 2012;9:139–147. doi: 10.1007/s11904-012-0118-8.20. Wahl C., Liptay S., Adler G., Schmid R.M. Sulfasalazine: A potent and specific inhibitor of nuclear factor kappa B. J. Clin. Invest. 1998;101:1163–1174. doi: 10.1172/JCI992.21. Bauernfeind F.G., Horvath G., Stutz A., Alnemri E.S., MacDonald K., Speert D., Fernandes-Alnemri T., Wu J., Monks B.G., Fitzgerald K.A., et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 2009;183:787–791. doi: 10.4049/jimmunol.0901363.22. Rodenburg R.J., Ganga A., van Lent P.L., van de Putte L.B., van Venrooij W.J. The antiinflammatory drug sulfasalazine inhibits tumor necrosis factor alpha expression in macrophages by inducing apoptosis. Arthritis Rheum. 2000;43:1941–1950. doi: 10.1002/1529-0131(200009)43:9<1941::AID-ANR4>3.0.CO;2-O.23. Volin M.V., Campbell P.L., Connors M.A., Woodruff D.C., Koch A.E. The effect of sulfasalazine on rheumatoid arthritic synovial tissue chemokine production. Exp Mol. Pathol. 2002;73:84–92. doi: 10.1006/exmp.2002.2460.24. Perdomo-Celis F., Feria M.G., Taborda N.A., Rugeles M.T. A Low Frequency of IL-17-Producing CD8(+) T-Cells Is Associated With Persistent Immune Activation in People Living With HIV Despite HAART-Induced Viral Suppression. Front. 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