Skip to main content

Advertisement

Log in

Mechanisms of monocyte cell death triggered by dengue virus infection

  • Review
  • Published:
Apoptosis Aims and scope Submit manuscript

Abstract

Arthropod-borne viral diseases caused by dengue virus (DENV) are major re-emerging public health problem worldwide. In spite of intense research, DENV pathogenesis is not fully understood and remains enigmatic; however, current evidence suggests that dengue progression is associated with an inflammatory response, mainly in patients suffering from a second DENV infection. Monocytes are one of the main target cells of DENV infection and play an important role in pathogenesis since they are known to produce several inflammatory cytokines that can lead to endothelial dysfunction and therefore vascular leak. In addition, monocytes play an important role in antibody dependent enhancement, infection with consequences in viral load and immune response. Despite the physiological functions of monocytes in immune response, their life span in the bloodstream is very short, and activation of monocytes by DENV infection can trigger different types of cell death. For example, DENV can induce apoptosis in monocytes related with the production of Tumor necrosis factor alpha (TNF-α). Additionally, recent studies have shown that DENV-infected monocytes also exhibit a cell death process mediated by caspase-1 activation together with IL-1 production, referred to as pyroptosis. Taken together, the aforementioned studies strongly depict that multiple cell death pathways may be occurring in monocytes upon DENV-2 infection. This review provides insight into mechanisms of DENV-induced death of both monocytes and other cell types for a better understanding of this process. Further knowledge in cell death induced by DENV will help in the developing novel strategies to prevent disease progression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Halstead SB (2007) Dengue. Lancet 370:1644–1652. https://doi.org/10.1016/S0140-6736(07)61687-0

    Article  PubMed  Google Scholar 

  2. Simmons C, Farrar J, van Vinh Chau N, Wills B (2012) Dengue. N Engl J Med 366:1423–1432

    Article  CAS  Google Scholar 

  3. Murray NEA, Quam MB, Wilder-Smith A (2013) Epidemiology of dengue: past, present and future prospects. Clin Epidemiol 5:299–309. https://doi.org/10.2147/CLEP.S34440

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bhatt S, Gething PW, Brady OJ et al (2013) The global distribution and burden of dengue. Nature 496:504–507. https://doi.org/10.1038/nature12060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. 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. https://doi.org/10.1016/j.ajpath.2013.02.027

    Article  CAS  PubMed  Google Scholar 

  6. Guzman MG, Harris E (2014) Dengue Lancet 6736:1–13. https://doi.org/10.1016/S0140-6736(14)60572-9

    Article  Google Scholar 

  7. Sun P, Kochel TJ (2013) The battle between infection and host immune responses of dengue virus and its implication in dengue disease pathogenesis. ScientificWorldJournal 2013:1–11. https://doi.org/10.1155/2013/843469

    Article  CAS  Google Scholar 

  8. Kamaladasa A, Gomes L, Jeewandara C et al (2016) Lipopolysaccharide acts synergistically with the dengue virus to induce monocyte production of platelet activating factor and other inflammatory mediators. Antiviral Res 133:183–190. https://doi.org/10.1016/j.antiviral.2016.07.016

    Article  CAS  PubMed  Google Scholar 

  9. Lauvau G, Chorro L, Spaulding E, Soudja SM (2014) Inflammatory monocyte effector mechanisms. Cell Immunol. https://doi.org/10.1016/j.cellimm.2014.07.007

    Article  PubMed  PubMed Central  Google Scholar 

  10. Kelley JF, Kaufusi PH, Nerurkar VR (2012) Dengue hemorrhagic fever-associated immunomediators induced via maturation of dengue virus nonstructural 4B protein in monocytes modulate endothelial cell adhesion molecules and human microvascular endothelial cells permeability. Virology 422:326–337. https://doi.org/10.1016/j.virol.2011.10.030

    Article  CAS  PubMed  Google Scholar 

  11. Dewi BE, Takasaki T, Kurane I (2004) In vitro assessment of human endothelial cell permeability: effects of inflammatory cytokines and dengue virus infection. J Virol Methods 121:171–180. https://doi.org/10.1016/j.jviromet.2004.06.013

    Article  CAS  PubMed  Google Scholar 

  12. Cruz-Oliveira C, Freire JM, Conceição TM et al (2015) Receptors and routes of dengue virus entry into the host cells. FEMS Microbiol Rev 39:155–170. https://doi.org/10.1093/femsre/fuu004

    Article  CAS  PubMed  Google Scholar 

  13. Arboleda Alzate JF, Rodenhuis-Zybert IA, Hernández JC et al (2017) Human macrophages differentiated in the presence of vitamin D3restrict dengue virus infection and innate responses by downregulating mannose receptor expression. PLoS Negl Trop Dis 11:1–18. https://doi.org/10.1371/journal.pntd.0005904

    Article  Google Scholar 

  14. Torres S, Hernández JC, Giraldo D et al (2013) Differential expression of toll-like receptors in dendritic cells of patients with dengue during early and late acute phases of the disease. PLoS Negl Trop Dis. https://doi.org/10.1371/journal.pntd.0002060

    Article  PubMed  PubMed Central  Google Scholar 

  15. Chen YC, Wang SY, King CC (1999) Bacterial lipopolysaccharide inhibits dengue virus infection of primary human monocytes/macrophages by blockade of virus entry via a CD14-dependent mechanism. J Virol 73:2650–2657

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Mukhopadhyay S, Kuhn RJ, Rossmann MG (2005) A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 3:13–22. https://doi.org/10.1038/nrmicro1067

    Article  CAS  PubMed  Google Scholar 

  17. Perera R, Kuhn RJ (2008) Structural proteomics of dengue virus. Curr Opin Microbiol 11:369–377. https://doi.org/10.1016/j.mib.2008.06.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Urcuqui-Inchima S, Patiño C, Torres S et al (2010) Recent developments in understanding dengue virus replication. Adv Virus Res 77:1–39

    Article  CAS  Google Scholar 

  19. Martina BEE, Koraka P, Osterhaus ADME (2009) Dengue virus pathogenesis: an integrated view. Clin Microbiol Rev 22:564–581. https://doi.org/10.1128/CMR.00035-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jessie K, Fong MY, Devi S et al (2004) Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J Infect Dis 189:1411–1418. https://doi.org/10.1086/383043

    Article  PubMed  Google Scholar 

  21. Aye KS, Charngkaew K, Win N et al (2014) Pathologic highlights of dengue hemorrhagic fever in 13 autopsy cases from Myanmar. Hum Pathol 45:1221–1233. https://doi.org/10.1016/j.humpath.2014.01.022

    Article  PubMed  Google Scholar 

  22. Halstead SB, O´rourke E (1977) Dengue viruses and mononuclear phagocytes. Infection enhacement by non-neutralizing antibody. J Exp Med 146:201–217

    Article  CAS  Google Scholar 

  23. Nielsen DG (2009) The relationship of interacting immunological components in dengue pathogenesis. Virol J 6:211. https://doi.org/10.1186/1743-422X-6-211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Halstead SB (2003) Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 60:421–467

    Article  CAS  Google Scholar 

  25. Flipse J, Wilschut J, Smit JM (2013) Molecular mechanisms involved in antibody-dependent enhancement of dengue virus infection in humans. Traffic 14:25–35. https://doi.org/10.1111/tra.12012

    Article  CAS  PubMed  Google Scholar 

  26. Dejnirattisai W, Jumnainsong A, Onsirisakul N et al (2010) Cross-reacting antibodies enhance dengue virus infection in humans. Science 328:745–748

    Article  CAS  Google Scholar 

  27. Goncalvez AP, Engle RE, Claire MS et al (2007) Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA 104:1–6

    Article  Google Scholar 

  28. da Silva Voorham JM, Rodenhuis-Zybert I, Nuñez A NV, et al (2012) Antibodies against the envelope glycoprotein promote infectivity of immature dengue virus serotype 2. PLoS ONE 7:e29957. https://doi.org/10.1371/journal.pone.0029957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Halstead SB (1979) In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 140:527–533

    Article  CAS  Google Scholar 

  30. Chau TNB, Quyen NTH, Thuy TT et al (2008) Dengue in vietnamese infants—results of infection-enhancement assays correlate with age-related disease epidemiology, and cellular immune responses correlate with disease severity. J Infect Dis 198:516–524. https://doi.org/10.1086/590117

    Article  PubMed  PubMed Central  Google Scholar 

  31. Clapham H, Cummings DAT, Nisalak A et al (2015) Epidemiology of infant dengue cases illuminates serotype-specificity in the interaction between immunity and disease, and changes in transmission dynamics. PLoS Negl Trop Dis 9:1–10. https://doi.org/10.1371/journal.pntd.0004262

    Article  CAS  Google Scholar 

  32. Wang M, Yang F, Huang D et al (2017) Anti-idiotypic antibodies specific to prM monoantibody prevent antibody dependent enhancement of dengue virus infection. Front Cell Infect Microbiol 7:1–11. https://doi.org/10.3389/fcimb.2017.00157

    Article  Google Scholar 

  33. Balsitis SJ, Williams KL, Lachica R et al (2010) Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6:e1000790. https://doi.org/10.1371/journal.ppat.1000790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Martínez Gómez JM, Ong LC, Lam JH et al (2016) Maternal antibody-mediated disease enhancement in type i interferon-deficient mice leads to lethal disease associated with liver damage. PLoS Negl Trop Dis 10:1–22. https://doi.org/10.1371/journal.pntd.0004536

    Article  CAS  Google Scholar 

  35. Ng JKW, Zhang SL, Tan HC et al (2014) First experimental in vivo model of enhanced dengue disease severity through maternally acquired heterotypic dengue antibodies. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1004031

    Article  PubMed  PubMed Central  Google Scholar 

  36. Falconar AKI (2007) Antibody responses are generated to immunodominant ELK/KLE-type motifs on the nonstructural-1 glycoprotein during live dengue virus infections in mice and humans: implications for diagnosis, pathogenesis, and vaccine design. Clin Vaccine Immunol 14:493–504. https://doi.org/10.1128/CVI.00371-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lin CF, Lei HY, Shiau AL et al (2002) Endothelial cell apoptosis induced by antibodies against dengue virus nonstructural protein 1 via production of nitric oxide. J Immunol 169:657–664. https://doi.org/10.4049/jimmunol.169.2.657

    Article  CAS  PubMed  Google Scholar 

  38. Falconar AKI (1997) The dengue virus nonstructural-1 protein (NS1) generates antibodies to common epitopes on human blood clotting, integrin/adhesin proteins and binds to human endothelial cells: potential implications in haemorrhagic fever pathogenesis. Arch Virol 142:897–916

    Article  CAS  Google Scholar 

  39. Wan SW, Lin CF, Yeh TM et al (2013) Autoimmunity in dengue pathogenesis. J Formos Med Assoc 112:3–11. https://doi.org/10.1016/j.jfma.2012.11.006

    Article  CAS  PubMed  Google Scholar 

  40. Cheng HJ, Lei HY, Lin CF et al (2009) Anti-dengue virus nonstructural protein 1 antibodies recognize protein disulfide isomerase on platelets and inhibit platelet aggregation. Mol Immunol 47:398–406. https://doi.org/10.1016/j.molimm.2009.08.033

    Article  CAS  PubMed  Google Scholar 

  41. Wan SW, Lin CF, Chen MC et al (2008) C-terminal region of dengue virus nonstructural protein 1 is involved in endothelial cell cross-reactivity via molecular mimicry. Am J Infect Dis 4:85–91. https://doi.org/10.3844/ajidsp.2008.85.91

    Article  CAS  Google Scholar 

  42. Modhiran N, Watterson D, Muller D et al (2015) Dengue virus NS1 protein activates cells via Toll-like receptor 4 and disrupts endothelial cell monolayer integrity. Sci Transl Med 7:304ra142–304ra142. https://doi.org/10.1126/scitranslmed.aaa3863

    Article  CAS  PubMed  Google Scholar 

  43. Beatty PR, Puerta-Guardo H, Killingbeck SS et al (2015) Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination. Sci Transl Med 7:304ra141–304ra141. https://doi.org/10.1126/scitranslmed.aaa3787

    Article  CAS  PubMed  Google Scholar 

  44. Muller DA, Young PR (2013) The flavivirus NS1 protein: molecular and structural biology, immunology, role in pathogenesis and application as a diagnostic biomarker. Antiviral Res 98:192–208. https://doi.org/10.1016/j.antiviral.2013.03.008

    Article  CAS  PubMed  Google Scholar 

  45. Adikari TN, Gomes L, Wickramasinghe N et al (2016) Dengue NS1 antigen contributes to disease severity by inducing interleukin (IL)-10 by monocytes. Clin Exp Immunol 184:90–100. https://doi.org/10.1111/cei.12747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Malavige GN, Gomes L, Alles L et al (2013) Serum IL-10 as a marker of severe dengue infection. BMC Infect Dis 13:341. https://doi.org/10.1186/1471-2334-13-341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Pérez AB, García G, Sierra B et al (2004) IL-10 levels in dengue patients: some findings from the exceptional epidemiological conditions in Cuba. J Med Virol 73:230–234. https://doi.org/10.1002/jmv.20080

    Article  CAS  PubMed  Google Scholar 

  48. Nguyen TH, Nguyen TL, Lei H-Y et al (2005) Association between sex, nutritional status, severity of dengue hemorrhagic fever, and immune status in infants with dengue hemorrhagic fever. Am J Trop Med Hyg 72:370–374

    Article  Google Scholar 

  49. Chakravarti A, Kumaria R (2006) Circulating levels of tumour necrosis factor- α & interferon- γ in patients with dengue & dengue haemorrhagic fever during an outbreak. 25–30

  50. Kumar Y, Liang C, Bo Z et al (2012) Serum proteome and cytokine analysis in a longitudinal cohort of adults with primary dengue infection reveals predictive markers of DHF. PLoS Negl Trop Dis 6:e1887. https://doi.org/10.1371/journal.pntd.0001887

    Article  PubMed  PubMed Central  Google Scholar 

  51. Restrepo BN, Isaza DM, Salazar CL et al (2008) Serum levels of interleukin-6, tumor necrosis factor-alpha and interferon-gama in infants with and without dengue Níveis séricos de interleucina-6, fator de necrose tumoral-alfa e interferon-gama em crianças menores de um ano com e sem dengue. Rev Soc Bras Med Trop 41:6–10

    Article  Google Scholar 

  52. Beltrán D, López-Vergès S (2014) NK cells during dengue disease and their recognition of dengue virus-infected cells. Front Immunol 5:192. https://doi.org/10.3389/fimmu.2014.00192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Chen Y, Wang S (2002) Activation of terminally differentiated human monocytes/macrophages by dengue virus: productive infection, hierarchical production of innate cytokines and chemokines, and the synergistic effect of lipopolysaccharide. J Virol 76:9877–9887. https://doi.org/10.1128/JVI.76.19.9877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Mongkolsapaya J, Dejnirattisai W, Xu X et al (2003) Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 9:921–927. https://doi.org/10.1038/nm887

    Article  CAS  PubMed  Google Scholar 

  55. Pawlowski NA, Abraham EL, Pontier S et al (1985) Human monocyte-endothelial cell interaction in vitro. Proc Natl Acad Sci USA 82:8208–8212

    Article  CAS  Google Scholar 

  56. Wong KL, Tai JJ, Wong W et al (2011) Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood 118:16–31. https://doi.org/10.1182/blood-2010-12-326355.The

    Article  Google Scholar 

  57. Wong KL, Yeap WH, Tai JJY et al (2012) The three human monocyte subsets: implications for health and disease. Immunol Res 53:41–57. https://doi.org/10.1007/s12026-012-8297-3

    Article  CAS  Google Scholar 

  58. Ziegler-Heitbrock HW (2000) Definition of human blood monocytes. J Leukoc Biol 67:603–606

    Article  CAS  Google Scholar 

  59. Auffray C, Sieweke MH, Geissmann F (2009) Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol 27:669–692. https://doi.org/10.1146/annurev.immunol.021908.132557

    Article  CAS  Google Scholar 

  60. Azeredo EL, Neves-Souza PC, Alvarenga AR et al (2010) 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. https://doi.org/10.1111/j.1365-2567.2009.03224.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Halstead SB, O´Rourke EJ, Allison AC (1977) Dengue viruses and mononuclear phagocytes II: identity of blood and tissue leukocytes supporting in vitro infection. J Exp Med 146:218–229

    Article  CAS  Google Scholar 

  62. Neves-Souza PCF, Azeredo EL, Zagne SMO et al (2005) Inducible nitric oxide synthase (iNOS) expression in monocytes during acute dengue fever in patients and during in vitro infection. BMC Infect Dis 5:64. https://doi.org/10.1186/1471-2334-5-64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Durbin AP, Vargas MJ, Wanionek K et al (2008) Phenotyping of peripheral blood mononuclear cells during acute dengue illness demonstrates infection and increased activation of monocytes in severe cases compared to classic dengue fever. Virology 376:429–435. https://doi.org/10.1016/j.virol.2008.03.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Kou Z, Quinn M, Chen H et al (2008) Monocytes, but not T or B cells, are the principal target cells for dengue virus (DV) infection among human peripheral blood mononuclear cells. J Med Virol 146:134–146. https://doi.org/10.1002/jmv

    Article  Google Scholar 

  65. Lee YR, Liu MT, Lei HY et al (2006) MCP1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol 87:3623–3630. https://doi.org/10.1099/vir.0.82093-0

    Article  CAS  PubMed  Google Scholar 

  66. Ong SP, Lee LM, Leong YFI et al (2012) Dengue virus infection mediates HMGB1 release from monocytes involving PCAF acetylase complex and induces vascular leakage in endothelial cells. PLoS ONE 7:e41932. https://doi.org/10.1371/journal.pone.0041932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Bosch I, Xhaja K, Estevez L et al (2002) Increased production of interleukin-8 in primary human monocytes and in human epithelial and endothelial cell lines after dengue virus challenge. J Virol 76:5588–5597. https://doi.org/10.1128/JVI.76.11.5588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Callaway JB, Smith SA, McKinnon KP et al (2015) Spleen tyrosine kinase (Syk) mediates IL-1B induction by primary human monocytes during antibody-enhanced dengue virus infection. J Biol Chem 290:17306–17320. https://doi.org/10.1074/jbc.M115.664136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Callaway JB, Smith SA, Widman DG et al (2015) Source and purity of dengue-viral preparations impact requirement for enhancing antibody to induce elevated IL-1β secretion: a primary human monocyte model. PLoS ONE 10:1–26. https://doi.org/10.1371/journal.pone.0136708

    Article  CAS  Google Scholar 

  70. Tan TY, Chu JJH (2013) Dengue virus-infected human monocytes trigger late activation of caspase-1, which mediates pro-inflammatory IL-1β secretion and pyroptosis. J Gen Virol 94:2215–2220. https://doi.org/10.1099/vir.0.055277-0

    Article  CAS  PubMed  Google Scholar 

  71. Burke-Gaffney A, Keenan AK (1993) Modulation of human endothelial cell permeability by combinations of the cytokines interleukin-1 alpha/beta, tumor necrosis factor-alpha and interferon-gamma. Immunopharmacology 25:1–9

    Article  CAS  Google Scholar 

  72. Melorose J, Perroy R, Careas S (2015) The origin and kinetics of mononuclear phagocytes. J Exp Med 1:415–435

    Google Scholar 

  73. Yona S, Kim KW, Wolf Y et al (2013) Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38:79–91. https://doi.org/10.1016/j.immuni.2012.12.001

    Article  CAS  Google Scholar 

  74. Man SM, Kanneganti T-D (2016) Converging roles of caspases in inflammasome activation, cell death and innate immunity. Nat Rev Immunol 16:7–21. https://doi.org/10.1038/nri.2015.7

    Article  CAS  PubMed  Google Scholar 

  75. Gonzalez-Mejia M, Elba. Doself A (2009) Regulation of monocytes and macrophages cell fate. Front Biosci 14:2413–2431

    Article  CAS  Google Scholar 

  76. Parihar A, Eubank TD, Doseff AI (2010) Monocytes and macrophages regulate immunity through dynamic networks of survival and cell death. J Innate Immun 2:204–215. https://doi.org/10.1159/000296507

    Article  PubMed  PubMed Central  Google Scholar 

  77. Lanneau D, Brunet M, Frisan E et al (2008) Heat shock proteins: essential proteins for apoptosis regulation. J Cell Mol Med 12:743–761. https://doi.org/10.1111/j.1582-4934.2008.00273.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Espina LM, Valero NJ, Hernández JM, Mosquera J (2003) Increased apoptosis and expression of tumor necrosis factor-alpha caused by infection of cultured human monocytes with dengue virus. Am J Trop Med Hyg 68:48–53

    Article  Google Scholar 

  79. Torrentes-Carvalho A, Azeredo EL, Reis SRI et al (2009) Dengue-2 infection and the induction of apoptosis in human primary monocytes. Mem Inst Oswaldo Cruz 104:1091–1099

    Article  CAS  Google Scholar 

  80. Arias J, Valero N, Mosquera J et al (2015) Corrigendum to “increased expression of cytokines, soluble cytokine receptors, soluble apoptosis ligand and apoptosis in dengue” [Virology 452–453 (2014) 42–51]. Virology. https://doi.org/10.1016/j.virol.2013.12.027

    Article  PubMed  Google Scholar 

  81. Cabal-Hierro L, Lazo PS (2012) Signal transduction by tumor necrosis factor receptors. Cell Signal 24:1297–1305. https://doi.org/10.1016/j.cellsig.2012.02.006

    Article  CAS  PubMed  Google Scholar 

  82. Lin G, Hoxie J (2003) The TNF receptor 1: a split complex. Cell 114:148–150

    Article  Google Scholar 

  83. Castellanos JE, Neissa JI, Camacho S (2016) La infección con virus dengue induce apoptosis en células de neuroblastoma humano SH-SY5Y. Biomedica 36:1–36. https://doi.org/10.1017/CBO9781107415324.004

    Article  Google Scholar 

  84. Klomporn P, Panyasrivanit M, Wikan N, Smith DR (2011) Dengue infection of monocytic cells activates ER stress pathways, but apoptosis is induced through both extrinsic and intrinsic pathways. Virology 409:189–197. https://doi.org/10.1016/j.virol.2010.10.010

    Article  CAS  PubMed  Google Scholar 

  85. Thepparit C, Khakpoor A, Khongwichit S et al (2013) Dengue 2 infection of HepG2 liver cells results in endoplasmic reticulum stress and induction of multiple pathways of cell death. BMC Res Notes. https://doi.org/10.1186/1756-0500-6-372

    Article  PubMed  PubMed Central  Google Scholar 

  86. Wu SJ, Grouard-Vogel G, Sun W et al (2000) Human skin Langerhans cells are targets of dengue virus infection. Nat Med 6:816–820. https://doi.org/10.1038/77553

    Article  CAS  PubMed  Google Scholar 

  87. Ho L, Wang J, Shaio M et al (2001) Infection of human dendritic cells by dengue virus causes cell maturation and cytokine production. J Immunol 166:1499–1506. https://doi.org/10.4049/jimmunol.166.3.1499

    Article  CAS  PubMed  Google Scholar 

  88. Olagnier D, Peri S, Steel C et al (2014) Cellular oxidative stress response controls the antiviral and apoptotic programs in dengue virus-infected dendritic cells. PLoS Pathog 10:1–18. https://doi.org/10.1371/journal.ppat.1004566

    Article  CAS  Google Scholar 

  89. Appanna R, Wang SM, Ponnampalavanar S, a et al (2012) Cytokine factors present in dengue patient sera induces alterations of junctional proteins in human endothelial cells. Am J Trop Med Hyg 87:936–942. https://doi.org/10.4269/ajtmh.2012.11-0606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Lin C-F, Lei H-Y, Shiau A-L et al (2003) Antibodies from dengue patient sera cross-react with endothelial cells and induce damage. J Med Virol 69:82–90. https://doi.org/10.1002/jmv.10261

    Article  CAS  PubMed  Google Scholar 

  91. Long X, Li Y, Qi Y et al (2013) XAF1 contributes to dengue virus-induced apoptosis in vascular endothelial cells. FASEB J 27:1062–1073. https://doi.org/10.1096/fj.12-213967

    Article  CAS  PubMed  Google Scholar 

  92. Lin J-C, Lin S-C, Chen W-Y et al (2014) Dengue viral protease interaction with NF- B inhibitor/results in endothelial cell apoptosis and hemorrhage development. J Immunol 193:1258–1267. https://doi.org/10.4049/jimmunol.1302675

    Article  CAS  PubMed  Google Scholar 

  93. Liu Y, Liu H, Zou J et al (2014) Dengue virus subgenomic RNA induces apoptosis through the Bcl-2-mediated PI3k/Akt signaling pathway. Virology 448:15–25. https://doi.org/10.1016/j.virol.2013.09.016

    Article  CAS  PubMed  Google Scholar 

  94. Pijlman GP, Funk A, Kondratieva N et al (2008) A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 4:579–591. https://doi.org/10.1016/j.chom.2008.10.007

    Article  CAS  PubMed  Google Scholar 

  95. Qi Y, Li Y, Zhang Y et al (2015) IFI6 inhibits apoptosis via mitochondrial-dependent pathway in dengue virus 2 infected vascular endothelial cells. PLoS ONE 10:1–14. https://doi.org/10.1371/journal.pone.0132743

    Article  CAS  Google Scholar 

  96. Shi J, Gao W, Shao F (2016) Pyroptosis: gasdermin-mediated programmed necrotic cell death. Trends Biochem Sci. https://doi.org/10.1016/j.tibs.2016.10.004

    Article  PubMed  Google Scholar 

  97. Wu M-F, Chen S-T, Yang A-H et al (2013) CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. Blood 121:95–106. https://doi.org/10.1182/blood-2012-05-430090

    Article  CAS  PubMed  Google Scholar 

  98. Chen ST, Lin YL, Huang MT et al (2008) CLEC5A is critical for dengue-virus-induced lethal disease. Nature 453:672–676. https://doi.org/10.1038/nature07013

    Article  CAS  PubMed  Google Scholar 

  99. Cheng YL, Lin YS, Chen CL et al (2016) Activation of Nrf2 by the dengue virus causes an increase in CLEC5A, which enhances TNF-α production by mononuclear phagocytes. Sci Rep 6:1–15. https://doi.org/10.1038/srep32000

    Article  CAS  Google Scholar 

  100. Cheung KT, Sze DMY, Chan KH, Leung PHM (2018) Involvement of caspase-4 in IL-1 beta production and pyroptosis in human macrophages during dengue virus infection. Immunobiology 223:356–364. https://doi.org/10.1016/j.imbio.2017.10.044

    Article  CAS  PubMed  Google Scholar 

  101. White GE, McNeill E, Channon KM, Greaves DR (2014) Fractalkine promotes human monocyte survival via a reduction in oxidative stress. Arterioscler Thromb Vasc Biol 34:2554–2562. https://doi.org/10.1161/ATVBAHA.114.304717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Castaño D. Garcia L. Rojas M (2011) Increased frequency and cell death of CD16 + monocytes with mycobacterium tuberculosis infection. Tuberculosis 91:348–360

    Article  Google Scholar 

  103. Scheller C, Knöferle J, Ullrich A et al (2006) Caspase inhibition in apoptotic T cells triggers necrotic cell death depending on the cell type and the proapoptotic stimulus. J Cell Biochem 97:1350–1361. https://doi.org/10.1002/jcb.20670

    Article  CAS  PubMed  Google Scholar 

  104. Oliva-Martin MJ, Sanchez-Abarca LI, Rodhe J et al (2016) Caspase-8 inhibition represses initial human monocyte activation in septic shock model. Oncotarget. https://doi.org/10.18632/oncotarget.9648

    Article  PubMed  PubMed Central  Google Scholar 

  105. Kearney CJ, Cullen SP, Tynan G et al (2015) Necroptosis suppresses inflammation via termination of TNF- or LPS-induced cytokine and chemokine production. Cell Death Differ 22:1313–1327. https://doi.org/10.1038/cdd.2014.222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the help of Anne-Lise Haenni for their critical reading and review of the manuscript and Universidad de Antioquia, UdeA.

Funding

The authors hereby disclose receipt of the following financial support for the research, authorship, and/or publication of this article. This study was funded by Universidad de Antioquia, UdeA. The funders had no role in the study design, data collection and analysis, manuscript preparation or the decision to publish.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Silvio Urcuqui-Inchima.

Ethics declarations

Conflict of interest

The authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castillo, J.A., Urcuqui-Inchima, S. Mechanisms of monocyte cell death triggered by dengue virus infection. Apoptosis 23, 576–586 (2018). https://doi.org/10.1007/s10495-018-1488-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10495-018-1488-1

Keywords

Navigation