Macrophage immune modulation: TGF-β1's influence on IL-1β dynamics in dengue virus infection
DOI:
https://doi.org/10.5281/zenodo.13741644Keywords:
dengue, macrophage, IL-1ß, TGF-ß1, inflammation, innate immunityAbstract
Introduction: several pathogenic mechanisms contribute to the severity of dengue virus infection. These include viral cytotoxicity, host genetics, and comorbidities such as diabetes and dyslipidemia. Patients with severe dengue show an uncontrolled immune response with high levels of proinflammatory cytokines (TNF, IL-1β, IL8, IL-6) and chemokines, which damage the microvascular endothelium. Inflammatory cytokines (IL-4, IL-10, TGF-β1) are also increased. The role of TGF-β1in dengue remains unclear. Few studies exist, and most of them use serum data from patients. These suggest both protective and harmful effects.
Objective: this study aimed to evaluate how TGF-1β regulates IL-1β secretion in dengue-infected macrophages in vitro; this was carried out in the laboratory of innate immunity, at the Autonomous University of the State of Morelos, Mexico.
Method: THP-1 cell line was treated with recombinant TGF-β before or after dengue virus (DENV) infection. Cells were differentiated into macrophages by PMA. Data were obtained by RT-PCR, IFA and ELISA assays. Variables analyzed included IL-1β expression and secretion. Statistical analysis included student t-tests.
Results: RT-PCR showed that IL-1β expression was similar in pretreated and control cells. However, IL-1β secretion decreased only when cells were stimulated with TGF-β1 (SB505124) before TGF-β1 treatment and DENV infection abrogated the inhibitory effect of TGF-β1.
Conclusions: these findings suggest that DENV might regulate TGF-β1 function in macrophages. Negative regulation of the TGF-β1 pathway is potentially a mechanism by which DENV evades the immune response. This could contribute to immunopathology.
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References
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17. Yeo ASL, Azhar NA, Yeow W, Talbot CC, Khan MA, Shankar EM, et al. Lack of clinical manifestations in asymptomatic dengue infection is attributed to broad down-regulation and selective up-regulation of host defence response genes. PloS One [Internet]. 2014 [cited 14 May 2024]; 9(4):e92240. DOI: https://doi.org/10.1371/journal.pone.0092240
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21. Tsatsanis C, Androulidaki A, Dermitzaki E, Gravanis A, Margioris AN. Corticotropin releasing factor receptor 1 (CRF1) and CRF2 agonists exert an anti-inflammatory effect during the early phase of inflammation suppressing LPS-induced TNF-alpha release from macrophages via induction of COX-2 and PGE2. J Cell Physiol [Internet]. 2007 [cited 14 May 2024]; 210(3):774–83. DOI: https://doi.org/10.1002/jcp.20900
22. Pang T, Cardosa MJ, Guzman MG. Of cascades and perfect storms: the immunopathogenesis of dengue haemorrhagic fever-dengue shock syndrome (DHF/DSS). Immunol Cell Biol [Internet]. 2007 Jan [cited 14 May 2024]; 85(1):43–5. DOI: https://doi.org/10.1038/sj.icb.7100008
23. Yacoub S, Wills B. Predicting outcome from dengue. BMC Med [Internet]. 2014 Dec [cited 14 May 2024]; 12(1):1–10. DOI: https://doi.org/10.1186/s12916-014-0147-9
24. John DV, Lin YS, Perng GC. Biomarkers of severe dengue disease – a review. J Biomed Sci [Internet]. 2015 Oct [cited 14 May 2024]; 22:83. DOI: https://doi.org/10.1186/s12929-015-0191-6
25. Letterio JJ, Roberts AB. Regulation of immune responses by TGF-beta. Annu Rev Immunol [Internet]. 1998 [cited 14 May 2024]; 16:137–61. DOI: https://doi.org/10.1146/annurev.immunol.16.1.137
26. Djamiatun K, Faradz SMH, Setiati TE, Netea MG, van der Ven AJAM, Dolmans WMV. Increase of plasminogen activator inhibitor-1 and decrease of transforming growth factor-b1 in children with dengue haemorrhagic fever in Indonesia. J Trop Pediatr [Internet]. 2011 Dec [cited 14 May 2024]; 57(6):424–32. DOI: https://doi.org/10.1093/tropej/fmq122
27. Sierra B, Perez AB, Vogt K, Garcia G, Schmolke K, Aguirre E, et al. Secondary heterologous dengue infection risk: Disequilibrium between immune regulation and inflammation? Cell Immunol [Internet]. 2010 [cited 14 May 2024]; 262(2):134–40. DOI: https://doi.org/10.1016/j.cellimm.2010.02.005
28. Chen W, Ten Dijke P. Immunoregulation by members of the TGFβ superfamily. Nat Rev Immunol [Internet]. 2016 Nov [cited 14 May 2024]; 16(12):723–40. DOI: https://doi.org/10.1038/nri.2016.112
29. Li MO, Flavell RA. TGF-beta, T-cell tolerance and immunotherapy of autoimmune diseases and cancer. Expert Rev Clin Immunol [Internet]. 2006 Mar [cited 14 May 2024]; 2(2):257–65. DOI: https://doi.org/10.1586/1744666x.2.2.257
30. Travis MA, Sheppard D. TGF-β activation and function in immunity. Annu Rev Immunol [Internet]. 2014 [cited 14 May 2024]; 32:51–82. DOI: https://doi.org/10.1146/annurev-immunol-032713-120257
31. Callaway JB, Smith SA, McKinnon KP, de Silva AM, Crowe JE, Ting JPY. Spleen Tyrosine Kinase (Syk) Mediates IL-1β Induction by Primary Human Monocytes during Antibody-enhanced Dengue Virus Infection. J Biol Chem [Internet]. 2015 Jul 10 [cited 14 May 2024]; 290(28):17306–20. DOI: https://doi.org/10.1074/jbc.m115.664136
32. Kwon YJ, Heo J, Wong HEE, Cruz DJM, Velumani S, da Silva CT, et al. Kinome siRNA screen identifies novel cell-type specific dengue host target genes. Antiviral Res [Internet]. 2014 Oct [cited 14 May 2024]; 110:20–30. DOI: https://doi.org/10.1016/j.antiviral.2014.07.006
33. Brough D, Pelegrin P, Nickel W. An emerging case for membrane pore formation as a common mechanism for the unconventional secretion of FGF2 and IL-1β. J Cell Sci [Internet]. 2017 Oct [cited 14 May 2024]; 130(19):3197–202. DOI: https://doi.org/10.1242/jcs.204206
34. New J, Thomas SM. Autophagy-dependent secretion: mechanism, factors secreted, and disease implications. Autophagy [Internet]. 2019 Oct [cited 14 May 2024]; 15(10):1682–93. DOI: https://doi.org/10.1080/15548627.2019.1596479
35. Wu MF, Chen ST, Yang AH, Lin WW, Lin YL, Chen NJ, et al. CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. Blood [Internet]. 2013 Jan 3 [cited 14 May 2024]; 121(1):95–106. DOI: https://doi.org/10.1182/blood-2012-05-430090
36. Tan TY, Chu JJH. Dengue virus-infected human monocytes trigger late activation of caspase-1, which mediates pro-inflammatory IL-1β secretion and pyroptosis. J Gen Virol [Internet]. 2013 Oct [cited 14 May 2024]; 94(Pt 10):2215–20. DOI: https://doi.org/10.1099/vir.0.055277-0
37. Cheung KT, Sze DMY, Chan KH, Leung PHM. Involvement of caspase-4 in IL-1 beta production and pyroptosis in human macrophages during dengue virus infection. Immunobiology [Internet]. 2018 [cited 14 May 2024]; 223(4–5):356–64. DOI: https://doi.org/10.1016/j.imbio.2017.10.044
38. Netea MG, Veerdonk FL van de, Meer JWM van der, Dinarello CA, Joosten LAB. Inflammasome-Independent Regulation of IL-1-Family Cytokines. Annu Rev Immunol [Internet]. 2015 Mar [cited 14 May 2024]; 33:49–77.DOI: https://doi.org/10.1146/annurev-immunol-032414-112306
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40. Harris J. Autophagy and IL-1 Family Cytokines. Front Immunol [Internet]. 2013 Apr 5 [cited 14 May 2024]; 4:83. DOI: https://doi.org/10.3389/fimmu.2013.00083
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42. Heaton NS, Randall G. Dengue virus and autophagy. Viruses [Internet]. 2011 Aug [cited 14 May 2024]; 3(8):1332–41. DOI: https://doi.org/10.3390/v3081332
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3. Martinez JD, Garza JAC de la, Cuellar-Barboza A. Going Viral 2019: Zika, Chikungunya, and Dengue. Dermatol Clin [Internet]. 2019 Jan [cited 14 May 2024]; 37(1):95–105. DOI: https://doi.org/10.1016/j.det.2018.07.008
4. Wilder-Smith A, Ooi EE, Horstick O, Wills B. Dengue. Lancet Lond Engl [Internet]. 2019 Jan 26 [cited 14 May 2024]; 393(10169):350–63. DOI: https://doi.org/10.1016/s0140-6736(18)32560-1
5. Pandey N, Jain A, Garg RK, Kumar R, Agrawal OP, Lakshmana Rao PV. Serum levels of IL-8, IFNγ, IL-10, and TGF β and their gene expression levels in severe and non-severe cases of dengue virus infection. Arch Virol [Internet]. 2015 Jun [cited 14 May 2024]; 160(6):1463–75. DOI: https://doi.org/10.1007/s00705-015-2410-6
6. Patra G, Mallik S, Saha B, Mukhopadhyay S. Assessment of chemokine and cytokine signatures in patients with dengue infection: A hospital-based study in Kolkata, India. Acta Trop [Internet]. 2019 Feb [cited 14 May 2024]; 190:73–9. DOI: https://doi.org/10.1016/j.actatropica.2018.10.017
7. Soo KM, Khalid B, Ching SM, Tham CL, Basir R, Chee HY. Meta-analysis of biomarkers for severe dengue infections. PeerJ [Internet]. 2017 Sep [cited 14 May 2024]; 5:e3589. DOI: https://doi.org/10.7717/peerj.3589
8. Srikiatkhachorn A, Mathew A, Rothman AL. Immune-mediated cytokine storm and its role in severe dengue. Semin Immunopathol [Internet]. 2017 Jul [cited 14 May 2024]; 39(5):563–74. DOI: https://doi.org/10.1007/s00281-017-0625-1
9. Palmal S, Kundu S, Ganguly S, Dey JB, Sandhukhan S, Pattanayak AK. Immunologic Crosstalk and Host-Specific Immune Signature Associated with Dengue. ACS Omega [Internet]. 2024 Aug [cited 30 Dic 2024]; 9(36):37418–29. DOI: https://doi.org/10.1021/acsomega.4c02506
10. St. John AL, Rathore APS. Adaptive immune responses to primary and secondary dengue virus infections. Nat Rev Immunol [Internet]. 2019 Apr [cited 14 May 2024]; 19(4):218–30. DOI: https://doi.org/10.1038/s41577-019-0123-x
11. Bozza FA, Cruz OG, Zagne SM, Azeredo EL, Nogueira RM, Assis EF, Bozza PT, Kubelka CF. Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity. BMC Infect Dis [Internet]. 2008 Jun [cited 14 May 2024]; 8:86. DOI: https://doi.org/10.1186/1471-2334-8-86
12. Chaturvedi UC, Nagar R, Shrivastava R. Macrophage and dengue virus: friend or foe? Indian J Med Res [Internet]. 2006 Jul [cited 14 May 2024]; 124(1):23–40. Disponible en: https://pubmed.ncbi.nlm.nih.gov/16926454/
13. Huyen TB, Trieu HT, Vuong NL, Minh Nguyet N, Tam DTH, McBride A, et al. Anakinra for dengue patients with hyperinflammation: protocol for a randomized double-blind placebo-controlled trial. Wellcome Open Res [Internet]. 2024 [cited 30 Dic 2024]; 9:689. DOI: https://doi.org/10.12688/wellcomeopenres.21017.1
14. Agarwal R, Elbishbishi EA, Chaturvedi UC, Nagar R, Mustafa AS. Profile of transforming growth factor-beta 1 in patients with dengue haemorrhagic fever. Int J Exp Pathol [Internet]. 1999 Jun [cited 14 May 2024]; 80(3):143–9. DOI: https://doi.org/10.1046/j.1365-2613.1999.00107.x
15. Laur F, Murgue B, Deparis X, Roche C, Cassar O, Chungue E. Plasma levels of tumour necrosis factor a and transforming growth factor β-1 in children with dengue 2 virus infection in French Polynesia. Trans R Soc Trop Med Hyg [Internet]. 1998 [cited 14 May 2024]; 92(6):654–6. DOI: https://doi.org/10.1016/s0035-9203(98)90800-8
16. Perez AB, Sierra B, Garcia G, Aguirre E, Babel N, Alvarez M, et al. Tumor necrosis factor-alpha, transforming growth factor-β1, and interleukin-10 gene polymorphisms: implication in protection or susceptibility to dengue hemorrhagic fever. Hum Immunol [Internet]. 2010 Nov [cited 14 May 2024]; 71(11):1135–40. DOI: https://doi.org/10.1016/j.humimm.2010.08.004
17. Yeo ASL, Azhar NA, Yeow W, Talbot CC, Khan MA, Shankar EM, et al. Lack of clinical manifestations in asymptomatic dengue infection is attributed to broad down-regulation and selective up-regulation of host defence response genes. PloS One [Internet]. 2014 [cited 14 May 2024]; 9(4):e92240. DOI: https://doi.org/10.1371/journal.pone.0092240
18. Tillu H, Tripathy AS, Reshmi PV, Cecilia D. Altered profile of regulatory T cells and associated cytokines in mild and moderate dengue. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol [Internet]. 2016 Mar [cited 14 May 2024]; 35(3):453–61. DOI: https://doi.org/10.1007/s10096-015-2561-0
19. Lee YS, Kim JH, Kim ST, Kwon JY, Hong S, Kim SJ, et al. Smad7 and Smad6 bind to discrete regions of Pellino-1 via their MH2 domains to mediate TGF-beta1-induced negative regulation of IL-1R/TLR signaling. Biochem Biophys Res Commun [Internet]. 2010 Mar 19 [cited 14 May 2024]; 393(4):836–43. DOI: https://doi.org/10.1016/j.bbrc.2010.02.094
20. Imai K, Takeshita A, Hanazawa S. Transforming Growth Factor-β Inhibits Lipopolysaccharide-Stimulated Expression of Inflammatory Cytokines in Mouse Macrophages through Downregulation of Activation Protein 1 and CD14 Receptor Expression. Infect Immun [Internet]. 2000 May [cited 14 May 2024]; 68(5):2418–23. DOI: https://doi.org/10.1128/iai.68.5.2418-2423.2000
21. Tsatsanis C, Androulidaki A, Dermitzaki E, Gravanis A, Margioris AN. Corticotropin releasing factor receptor 1 (CRF1) and CRF2 agonists exert an anti-inflammatory effect during the early phase of inflammation suppressing LPS-induced TNF-alpha release from macrophages via induction of COX-2 and PGE2. J Cell Physiol [Internet]. 2007 [cited 14 May 2024]; 210(3):774–83. DOI: https://doi.org/10.1002/jcp.20900
22. Pang T, Cardosa MJ, Guzman MG. Of cascades and perfect storms: the immunopathogenesis of dengue haemorrhagic fever-dengue shock syndrome (DHF/DSS). Immunol Cell Biol [Internet]. 2007 Jan [cited 14 May 2024]; 85(1):43–5. DOI: https://doi.org/10.1038/sj.icb.7100008
23. Yacoub S, Wills B. Predicting outcome from dengue. BMC Med [Internet]. 2014 Dec [cited 14 May 2024]; 12(1):1–10. DOI: https://doi.org/10.1186/s12916-014-0147-9
24. John DV, Lin YS, Perng GC. Biomarkers of severe dengue disease – a review. J Biomed Sci [Internet]. 2015 Oct [cited 14 May 2024]; 22:83. DOI: https://doi.org/10.1186/s12929-015-0191-6
25. Letterio JJ, Roberts AB. Regulation of immune responses by TGF-beta. Annu Rev Immunol [Internet]. 1998 [cited 14 May 2024]; 16:137–61. DOI: https://doi.org/10.1146/annurev.immunol.16.1.137
26. Djamiatun K, Faradz SMH, Setiati TE, Netea MG, van der Ven AJAM, Dolmans WMV. Increase of plasminogen activator inhibitor-1 and decrease of transforming growth factor-b1 in children with dengue haemorrhagic fever in Indonesia. J Trop Pediatr [Internet]. 2011 Dec [cited 14 May 2024]; 57(6):424–32. DOI: https://doi.org/10.1093/tropej/fmq122
27. Sierra B, Perez AB, Vogt K, Garcia G, Schmolke K, Aguirre E, et al. Secondary heterologous dengue infection risk: Disequilibrium between immune regulation and inflammation? Cell Immunol [Internet]. 2010 [cited 14 May 2024]; 262(2):134–40. DOI: https://doi.org/10.1016/j.cellimm.2010.02.005
28. Chen W, Ten Dijke P. Immunoregulation by members of the TGFβ superfamily. Nat Rev Immunol [Internet]. 2016 Nov [cited 14 May 2024]; 16(12):723–40. DOI: https://doi.org/10.1038/nri.2016.112
29. Li MO, Flavell RA. TGF-beta, T-cell tolerance and immunotherapy of autoimmune diseases and cancer. Expert Rev Clin Immunol [Internet]. 2006 Mar [cited 14 May 2024]; 2(2):257–65. DOI: https://doi.org/10.1586/1744666x.2.2.257
30. Travis MA, Sheppard D. TGF-β activation and function in immunity. Annu Rev Immunol [Internet]. 2014 [cited 14 May 2024]; 32:51–82. DOI: https://doi.org/10.1146/annurev-immunol-032713-120257
31. Callaway JB, Smith SA, McKinnon KP, de Silva AM, Crowe JE, Ting JPY. Spleen Tyrosine Kinase (Syk) Mediates IL-1β Induction by Primary Human Monocytes during Antibody-enhanced Dengue Virus Infection. J Biol Chem [Internet]. 2015 Jul 10 [cited 14 May 2024]; 290(28):17306–20. DOI: https://doi.org/10.1074/jbc.m115.664136
32. Kwon YJ, Heo J, Wong HEE, Cruz DJM, Velumani S, da Silva CT, et al. Kinome siRNA screen identifies novel cell-type specific dengue host target genes. Antiviral Res [Internet]. 2014 Oct [cited 14 May 2024]; 110:20–30. DOI: https://doi.org/10.1016/j.antiviral.2014.07.006
33. Brough D, Pelegrin P, Nickel W. An emerging case for membrane pore formation as a common mechanism for the unconventional secretion of FGF2 and IL-1β. J Cell Sci [Internet]. 2017 Oct [cited 14 May 2024]; 130(19):3197–202. DOI: https://doi.org/10.1242/jcs.204206
34. New J, Thomas SM. Autophagy-dependent secretion: mechanism, factors secreted, and disease implications. Autophagy [Internet]. 2019 Oct [cited 14 May 2024]; 15(10):1682–93. DOI: https://doi.org/10.1080/15548627.2019.1596479
35. Wu MF, Chen ST, Yang AH, Lin WW, Lin YL, Chen NJ, et al. CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. Blood [Internet]. 2013 Jan 3 [cited 14 May 2024]; 121(1):95–106. DOI: https://doi.org/10.1182/blood-2012-05-430090
36. Tan TY, Chu JJH. Dengue virus-infected human monocytes trigger late activation of caspase-1, which mediates pro-inflammatory IL-1β secretion and pyroptosis. J Gen Virol [Internet]. 2013 Oct [cited 14 May 2024]; 94(Pt 10):2215–20. DOI: https://doi.org/10.1099/vir.0.055277-0
37. Cheung KT, Sze DMY, Chan KH, Leung PHM. Involvement of caspase-4 in IL-1 beta production and pyroptosis in human macrophages during dengue virus infection. Immunobiology [Internet]. 2018 [cited 14 May 2024]; 223(4–5):356–64. DOI: https://doi.org/10.1016/j.imbio.2017.10.044
38. Netea MG, Veerdonk FL van de, Meer JWM van der, Dinarello CA, Joosten LAB. Inflammasome-Independent Regulation of IL-1-Family Cytokines. Annu Rev Immunol [Internet]. 2015 Mar [cited 14 May 2024]; 33:49–77.DOI: https://doi.org/10.1146/annurev-immunol-032414-112306
39. Harris J. Autophagy and cytokines. Cytokine [Internet]. 2011 Nov [cited 14 May 2024]; 56(2):140–4. DOI: https://doi.org/10.1016/j.cyto.2011.08.022
40. Harris J. Autophagy and IL-1 Family Cytokines. Front Immunol [Internet]. 2013 Apr 5 [cited 14 May 2024]; 4:83. DOI: https://doi.org/10.3389/fimmu.2013.00083
41. Datan E, Roy SG, Germain G, Zali N, McLean JE, Golshan G, et al. Dengue-induced autophagy, virus replication and protection from cell death require ER stress (PERK) pathway activation. Cell Death Dis [Internet]. 2016 Mar [cited 14 May 2024]; 7(3):e2127–e2127. DOI: https://doi.org/10.1038/cddis.2015.409
42. Heaton NS, Randall G. Dengue virus and autophagy. Viruses [Internet]. 2011 Aug [cited 14 May 2024]; 3(8):1332–41. DOI: https://doi.org/10.3390/v3081332
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2025-03-20
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Serrato Salas J, Ramírez Agüero B, Montiel Hernández JL, González Christen J. Macrophage immune modulation: TGF-β1’s influence on IL-1β dynamics in dengue virus infection. Rev Inf Cient [Internet]. 2025 Mar. 20 [cited 2025 Apr. 4];104:e4791. Available from: https://revinfcientifica.sld.cu/index.php/ric/article/view/4791
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Copyright (c) 2025 Javier Serrato Salas, Brenda Ramírez Agüero, José Luis Montiel Hernández, Judith González Christen
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