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Dengue Virus Infection: Immune Response and Therapeutic Targets
Ngo Tin Ern
Ngo Tin Ern
Infection and Immunity Research Strength, Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Bandar Sunway, Malaysia
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Thamil Vaani Komarasamy
Thamil Vaani Komarasamy
Infection and Immunity Research Strength, Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Bandar Sunway, Malaysia
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Nur Amelia Azreen Adnan
Nur Amelia Azreen Adnan
Infection and Immunity Research Strength, Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Bandar Sunway, Malaysia
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Vinod R. M. T. Balasubramaniam
vinod.balasubramaniam@monash.edu
Vinod R. M. T. Balasubramaniam
Infection and Immunity Research Strength, Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Bandar Sunway, Malaysia
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ABSTRACT.
Flavivirus infection, especially dengue virus infection caused by DENV, is known to be a significant health concern globally owing to the high incidence and mortality rate. The expanding and increasing disease burden calls for the need to develop an effective treatment and prevent the event of fatal complications, including dengue hemorrhagic fever/dengue shock syndrome. The DENV-induced immune response has been described as paradoxical because it has a protective role in viral clearance but, at the same time, causes more severe infection through viral-specific immunity. This is further complicated by high homology and cross-reactivity between different serotypes of DENV, causing a more severe disease presentation during secondary infection by a heterologous serotype. This serotype complexity poses a challenge for the development of a universal flavivirus vaccine. This review highlights the significance of high motility group box 1 (HMGB1) and nucleotide-binding oligomerization domain, leucine rich repeat and pyrin domain containing 3 (NLRP3) inflammasome activation pathways in initiating an inflammatory response through the downstream activation of nuclear factor κB and proinflammatory cytokine Interleukin (IL)-1B, IL-18 release in DENV infection. It also discusses the role of NLRP3 in activating cellular apoptosis and pyroptosis leading to systemic failure, especially in peripheral tissues. Over the decades, there has been much progress in understanding the immunopathogenesis of DENV infection. Researchers have been studying key pathogenic molecules for potential therapeutic targets including HMGB1 and NLRP3 inflammasome inhibitors, which is explored in this review. Ultimately, although there is not yet an effective antiviral or vaccine for DENV, immunomodulators continue to pave the way to decrease disease severity in infected individuals.
- Supplemental Materials (PDF 90.545 KB)
Author Notes
Current contact information: Ngo Tin Ern, Thamil Vaani Komarasamy, Nur Amelia Azreen Adnan, and Vinod R. M. T. Balasubramaniam, Infection and Immunity Research Strength, Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Bandar Sunway, Malaysia, E-mails: tngo0006@student.monash.edu, thamil.komarasamy@monash.edu, amelia.azreen@monash.edu, and vinod.balasubramaniam@monash.edu
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Pierson TC, Diamond MS, 2020. The continued threat of emerging flaviviruses. Nat Microbiol 5: 796–812.
-
2.
Zhao R, Wang M, Cao J, Shen J, Zhou X, Wang D, Cao J, 2021. Flavivirus: From structure to therapeutics development. Life (Basel) 11: 615.
-
3.
Chen HR, Lai YC, Yeh TM, 2018. Dengue virus non-structural protein 1: A pathogenic factor, therapeutic target, and vaccine candidate. J Biomed Sci 25: 58.
-
4.
Scherwitzl I, Mongkolsapaja J, Screaton G, 2017. Recent advances in human flavivirus vaccines. Curr Opin Virol 23: 95–101.
-
5.
Silva NM, Santos NC, Martins IC, 2020. Dengue and Zika viruses: Epidemiological history, potential therapies, and promising vaccines. Trop Med Infect Dis 5: 150.
-
6.
Shrivastava G, Valenzuela Leon PC, Calvo E, 2020. Inflammasome fuels dengue severity. Front Cell Infect Microbiol 10: 489.
-
7.
St John AL, Rathore APS, 2019. Adaptive immune responses to primary and secondary dengue virus infections. Nat Rev Immunol 19: 218–230.
-
8.
Izmirly AM, Alturki SO, Alturki SO, Connors J, Haddad EK, 2020. Challenges in dengue vaccines development: Pre-existing infections and cross-reactivity. Front Immunol 11: 1055.
-
9.
Kao YT, Lai MMC, Yu CY, 2018. How dengue virus circumvents innate immunity. Front Immunol 9: 2860.
-
10.
Costa VV, Fagundes CT, Souza DG, Teixeira MM, 2013. Inflammatory and innate immune responses in dengue infection: Protection versus disease induction. Am J Pathol 182: 1950–1961.
-
11.
Srikiatkhachorn A, Mathew A, Rothman AL, 2017. Immune-mediated cytokine storm and its role in severe dengue. Semin Immunopathol 39: 563–574.
-
12.
Oliveira ERA, et al., 2017. Dengue fatal cases present virus-specific HMGB1 response in peripheral organs. Sci Rep 7: 16011.
-
13.
Andersson U, Ottestad W, Tracey KJ, 2020. Extracellular HMGB1: A therapeutic target in severe pulmonary inflammation including COVID-19? Mol Med 26: 42.
-
14.
Yang H, et al., 2015. MD-2 is required for disulfide HMGB1-dependent TLR4 signaling. J Exp Med 212: 5–14.
-
14.
Yang H, Wang H, Andersson U, 2020. Targeting inflammation driven by HMGB1. Front Immunol 11: 484.
-
16.
Zhao C, Zhao W, 2020. NLRP3 inflammasome-A key player in antiviral responses. Front Immunol 11: 211.
-
17.
Pan P, et al., 2019. Dengue virus M protein promotes NLRP3 inflammasome activation to induce vascular leakage in mice. J Virol 93: e00996-19.
-
18.
Screaton G, Mongkolsapaya J, Yacoub S, Roberts C, 2015. New insights into the immunopathology and control of dengue virus infection. Nat Rev Immunol 15: 745–759.
-
19.
Slon Campos JL, Mongkolsapaya J, Screaton GR, 2018. The immune response against flaviviruses. Nat Immunol 19: 1189–1198.
-
20.
Tian Y, Grifoni A, Sette A, Weiskopf D, 2019. Human T cell response to dengue virus infection. Front Immunol 10: 2125.
-
21.
Mathew A, West K, Kalayanarooj S, Gibbons RV, Srikiatkhachorn A, Green S, Libraty D, Jaiswal S, Rothman AL, 2011. B-cell responses during primary and secondary dengue virus infections in humans. J Infect Dis 204: 1514–1522.
-
22.
Bos S, et al., 2024. Protection against symptomatic dengue infection by neutralizing antibodies varies by infection history and infecting serotype. Nat Commun 15: 382.
-
23.
Jayathilaka D, et al., 2018. Role of NS1 antibodies in the pathogenesis of acute secondary dengue infection. Nat Commun 9: 5242.
-
24.
Dayarathna S, et al., 2020. Similarities and differences between the ‘cytokine storms’ in acute dengue and COVID-19. Sci Rep 10: 19839.
-
25.
Imrie A, Meeks J, Gurary A, Sukhbaatar M, Truong TT, Cropp CB, Effler P, 2007. Antibody to dengue 1 detected more than 60 years after infection. Viral Immunol 20: 672–675.
-
26.
Narayan R, Tripathi S, 2020. Intrinsic ADE: The dark side of antibody dependent enhancement during dengue infection. Front Cell Infect Microbiol 10: 580096.
-
27.
Shukla R, Ramasamy V, Shanmugam RK, Ahuja R, Khanna N, 2020. Antibody-dependent enhancement: A challenge for developing a safe dengue vaccine. Front Cell Infect Microbiol 10: 572681.
-
28.
Ramasamy V, et al., 2018. A tetravalent virus-like particle vaccine designed to display domain III of dengue envelope proteins induces multi-serotype neutralizing antibodies in mice and macaques which confer protection against antibody dependent enhancement in AG129 mice. PLoS Negl Trop Dis 12: e0006191.
-
29.
Sirohi D, Chen Z, Sun L, Klose T, Pierson TC, Rossmann MG, Kuhn RJ, 2016. The 3.8 A resolution cryo-EM structure of Zika virus. Science 352: 467–470.
-
30.
Montecillo-Aguado MR, et al., 2019. Cross-reaction, enhancement, and neutralization activity of dengue virus antibodies against Zika virus: A study in the Mexican population. J Immunol Res 2019: 7239347.
-
31.
Nogueira ML, et al., 2018. Adverse birth outcomes associated with Zika virus exposure during pregnancy in Sao Jose do Rio Preto, Brazil. Clin Microbiol Infect 24: 646–652.
-
32.
Katzelnick LC, Gresh L, Halloran ME, Mercado JC, Kuan G, Gordon A, Balmaseda A, Harris E, 2017. Antibody-dependent enhancement of severe dengue disease in humans. Science 358: 929–932.
-
33.
Vo HTM, et al., 2022. Temporal patterns of functional anti-dengue antibodies in dengue infected individuals with different disease outcome or infection history. Sci Rep 12: 17863.
-
34.
Lien TS, Sun DS, Wu CY, Chang HH, 2021. Exposure to dengue envelope protein Domain III induces Nlrp3 inflammasome-dependent endothelial dysfunction and hemorrhage in mice. Front Immunol 12: 617251.
-
35.
Low JG, Ooi EE, Vasudevan SG, 2017. Current status of dengue therapeutics research and development. J Infect Dis 215: S96–S102.
-
36.
Low JG, Gatsinga R, Vasudevan SG, Sampath A, 2018. Dengue antiviral development: A continuing journey. Adv Exp Med Biol 1062: 319–332.
-
37.
Soe HJ, Manikam R, Raju CS, Khan MA, Sekaran SD, 2020. Correlation of host inflammatory cytokines and immune-related metabolites, but not viral NS1 protein, with disease severity of dengue virus infection. PLoS One 15: e0237141.
-
38.
Best SM, 2017. The many faces of the Flavivirus NS5 protein in antagonism of type I interferon signaling. J Virol 91: e01970-16.
-
39.
Thurmond S, Wang B, Song J, Hai R, 2018. Suppression of type I interferon signaling by Flavivirus NS5. Viruses 10: 712.
-
40.
Ashour J, et al., 2010. Mouse STAT2 restricts early dengue virus replication. Cell Host Microbe 8: 410–421.
-
41.
Fernandes PO, Chagas MA, Rocha WR, Moraes AH, 2021. Non-structural protein 5 (NS5) as a target for antiviral development against established and emergent flaviviruses. Curr Opin Virol 50: 30–39.
-
42.
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