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01-07-2017 | Review

Immune-mediated cytokine storm and its role in severe dengue

Authors: Anon Srikiatkhachorn, Anuja Mathew, Alan L. Rothman

Published in: Seminars in Immunopathology | Issue 5/2017

Abstract

Dengue remains one of the most important mosquito-borne diseases worldwide. Infection with one of the serologically related dengue viruses (DENVs) can lead to a wide range of clinical manifestations and severity. Severe dengue is characterized by plasma leakage and abnormal bleeding that can lead to shock and death. There is currently no specific treatment for severe dengue due to gaps in understanding of the underlying mechanisms. The transient period of vascular leakage is usually followed by a rapid recovery and is suggestive of the effects of short-lived biological mediators. Both the innate and the adaptive immune systems are activated in severe dengue and contribute to the cytokine production. We discuss the immunological events elicited during a DENV infection and identify candidate cytokines that may play a key role in the severe manifestations of dengue and possible interventions.

Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI (2013) The global distribution and burden of dengue. Nature 496(7446):504–507. doi:10.1038/nature12060 PubMedPubMedCentralCrossRef

Amarasinghe A, Letson GW (2012) Dengue in the Middle East: a neglected, emerging disease of importance. Trans R Soc Trop Med Hyg 106(1):1–2. doi:10.1016/j.trstmh.2011.08.014 PubMedCrossRef

Baruah K, Singh PK, Mohalia MM, Dhariwal AC (2010) A study on dengue outbreak during 2009 in Bhopal and Indore districts of Madhya Pradesh, India. J Commun Dis 42(4):273–279PubMed

Franco C, Hynes NA, Bouri N, Henderson DA (2010) The dengue threat to the United States. Biosecur Bioterror 8(3):273–276. doi:10.1089/bsp.2010.0032 PubMedCrossRef

Morens DM, Fauci AS (2008) Dengue and hemorrhagic fever: a potential threat to public health in the United States. JAMA 299(2):214–216PubMedCrossRef

Nimmannitya S (1993) Clinical manifestations of dengue/dengue haemorrhagic fever. In: Thongcharoen P (ed) Monograph on dengue/dengue haemorrhagic fever. World Health Organization, New Delhi, pp 48–57

Gubler D, Kuno G, Markoff L (2007) Flavivirus, Fields virology, vol 5th. 5th edn. Lippincott Williams & Wilkins

Lindenbach BD, Thiel H-J, Rice CM (2007) Flaviviridae: the viruses and their replication, Fields virology, vol 5th. Lippincott Williams & Wilkins

Leitmeyer KC, Vaughn DW, Watts DM, Salas R, Villalobos I, de C, Ramos C, Rico-Hesse R (1999) Dengue virus structural differences that correlate with pathogenesis. J Virol 73(6):4738–4747PubMedPubMedCentral

10.

Modis Y, Ogata S, Clements D, Harrison SC (2004) Structure of the dengue virus envelope protein after membrane fusion. Nature 427(6972):313–319PubMedCrossRef

11.

Tassaneetrithep B, Burgess TH, Granelli-Piperno A, Trumpfheller C, Finke J, Sun W, Eller MA, Pattanapanyasat K, Sarasombath S, Birx DL, Steinman RM, Schlesinger S, Marovich MA (2003) DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197(7):823–829PubMedPubMedCentralCrossRef

12.

Jones M, Davidson A, Hibbert L, Gruenwald P, Schlaak J, Ball S, Foster GR, Jacobs M (2005) Dengue virus inhibits alpha interferon signaling by reducing STAT2 expression. J Virol 79(9):5414–5420PubMedPubMedCentralCrossRef

13.

Munoz-Jordan JL, Laurent-Rolle M, Ashour J, Martinez-Sobrido L, Ashok M, Lipkin WI, Garcia-Sastre A (2005) Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses. J Virol 79(13):8004–8013PubMedPubMedCentralCrossRef

14.

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(2):326–337. doi:10.1016/j.virol.2011.10.030 PubMedCrossRef

15.

Medin CL, Fitzgerald KA, Rothman AL (2005) Dengue virus nonstructural protein NS5 induces interleukin-8 transcription and secretion. J Virol 79(17):11053–11061PubMedPubMedCentralCrossRef

16.

Rothman AL (2009) T lymphocyte responses to heterologous secondary dengue virus infections. Ann N Y Acad Sci 1171(Suppl 1):E36–E41. doi:10.1111/j.1749-6632.2009.05055.x PubMedCrossRef

17.

Arevalo MT, Simpson-Haidaris PJ, Kou Z, Schlesinger JJ, Jin X (2009) Primary human endothelial cells support direct but not antibody-dependent enhancement of dengue viral infection. J Med Virol 81(3):519–528. doi:10.1002/jmv.21408 PubMedCrossRef

18.

Basu A, Jain P, Sarkar P, Gangodkar S, Deshpande D, Ganti K, Shetty S, Ghosh K (2011) Dengue virus infection of SK Hep1 cells: inhibition of in vitro angiogenesis and altered cytomorphology by expressed viral envelope glycoprotein. FEMS Immunol Med Microbiol 62(2):140–147. doi:10.1111/j.1574-695X.2011.00794.x PubMedCrossRef

19.

Brown MG, Hermann LL, Issekutz AC, Marshall JS, Rowter D, Al-Afif A, Anderson R (2011) Dengue virus infection of mast cells triggers endothelial cell activation. J Virol 85(2):1145–1150. doi:10.1128/JVI.01630-10 PubMedCrossRef

20.

Paes MV, Lenzi HL, Nogueira AC, Nuovo GJ, Pinhao AT, Mota EM, Basilio-de-Oliveira CA, Schatzmayr H, Barth OM, Alves AM (2009) Hepatic damage associated with dengue-2 virus replication in liver cells of BALB/c mice. Laboratory investigation; a journal of technical methods and pathology 89(10):1140–1151. doi:10.1038/labinvest.2009.83 PubMedCrossRef

21.

Salgado DM, Eltit JM, Mansfield K, Panqueba C, Castro D, Vega MR, Xhaja K, Schmidt D, Martin KJ, Allen PD, Rodriguez JA, Dinsmore JH, Lopez JR, Bosch I (2010) Heart and skeletal muscle are targets of dengue virus infection. Pediatr Infect Dis J 29(3):238–242. doi:10.1097/INF.0b013e3181bc3c5b PubMedPubMedCentralCrossRef

22.

Chen ST, Lin YL, Huang MT, Wu MF, Cheng SC, Lei HY, Lee CK, Chiou TW, Wong CH, Hsieh SL (2008) CLEC5A is critical for dengue-virus-induced lethal disease. Nature 453(7195):672–676. doi:10.1038/nature07013 PubMedCrossRef

23.

Lozach PY, Burleigh L, Staropoli I, Navarro-Sanchez E, Harriague J, Virelizier JL, Rey FA, Despres P, Arenzana-Seisdedos F, Amara A (2005) Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN)-mediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals. J Biol Chem 280(25):23698–23708PubMedCrossRef

24.

Rigau-Perez JG, Laufer MK (2006) Dengue-related deaths in Puerto Rico, 1992-1996: diagnosis and clinical alarm signals. Clin Infect Dis 42(9):1241–1246PubMedCrossRef

25.

WHO (1997) Dengue hemorrhagic fever: diagnosis, treatment, prevention and control, 2nd edn. WHO, Geneva

26.

Dengue, guidelines for diagnosis, treatment, prevention and control (2009). World Health Organization

27.

Srikiatkhachorn A, Krautrachue A, Ratanaprakarn W, Wongtapradit L, Nithipanya N, Kalayanarooj S, Nisalak A, Thomas SJ, Gibbons RV, Mammen MP Jr, Libraty DH, Ennis FA, Rothman AL, Green S (2007) Natural history of plasma leakage in dengue hemorrhagic fever: a serial ultrasonographic study. Pediatr Infect Dis J 26(4):283–290 discussion 291-282 PubMedCrossRef

28.

Burke DS, Nisalak A, Johnson DE, Scott RM (1988) A prospective study of dengue infections in Bangkok. AmJTrop Med Hyg 38(1):172–180CrossRef

29.

Sangkawibha N, Rojanasuphot S, Ahandrik S, Viriyapongse S, Jatanasen S, Salitul V, Phanthumachinda B, Halstead SB (1984) Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 120(5):653–669PubMedCrossRef

30.

Avirutnan P, Malasit P, Seliger B, Bhakdi S, Husmann M (1998) Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. J Immunol 161(11):6338–6346PubMed

31.

Dalrymple NA, Mackow ER (2012) Endothelial cells elicit immune-enhancing responses to dengue virus infection. J Virol 86(12):6408–6415. doi:10.1128/JVI.00213-12 PubMedPubMedCentralCrossRef

32.

Luplertlop N, Misse D, Bray D, Deleuze V, Gonzalez JP, Leardkamolkarn V, Yssel H, Veas F (2006) Dengue-virus-infected dendritic cells trigger vascular leakage through metalloproteinase overproduction. EMBO Rep 7(11):1176–1181PubMedCrossRef

33.

Limon-Flores AY, Perez-Tapia M, Estrada-Garcia I, Vaughan G, Escobar-Gutierrez A, Calderon-Amador J, Herrera-Rodriguez SE, Brizuela-Garcia A, Heras-Chavarria M, Flores-Langarica A, Cedillo-Barron L, Flores-Romo L (2005) Dengue virus inoculation to human skin explants: an effective approach to assess in situ the early infection and the effects on cutaneous dendritic cells. Int J Exp Pathol 86(5):323–334. doi:10.1111/j.0959-9673.2005.00445.x PubMedPubMedCentralCrossRef

34.

Wu SJ, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E, Putvatana R, Louder MK, Filgueira L, Marovich MA, Wong HK, Blauvelt A, Murphy GS, Robb ML, Innes BL, Birx DL, Hayes CG, Frankel SS (2000) Human skin Langerhans cells are targets of dengue virus infection. Nat Med 6(7):816–820PubMedCrossRef

35.

Freire M, Marchevsky R, Almeida L, Yamamura A, Caride E, Brindeiro P, Motta M, Nogueira R, Kubelka C, Bonaldo M, Galler R (2007) Wild dengue virus types 1, 2 and 3 viremia in rhesus monkeys. Memorias do Instituto Oswaldo Cruz 102(2):203–208PubMedCrossRef

36.

Kraiselburd E, Gubler DJ, Kessler MJ (1985) Quantity of dengue virus required to infect rhesus monkeys. Trans R Soc Trop Med Hyg 79(2):248–251PubMedCrossRef

37.

Onlamoon N, Noisakran S, Hsiao HM, Duncan A, Villinger F, Ansari AA, Perng GC (2010) Dengue virus-induced hemorrhage in a nonhuman primate model. Blood 115(9):1823–1834. doi:10.1182/blood-2009-09-242990 PubMedPubMedCentralCrossRef

38.

Jaiswal S, Pazoles P, Woda M, Shultz LD, Greiner DL, Brehm MA, Mathew A (2012) Enhanced humoral and HLA-A2-restricted dengue virus-specific T-cell responses in humanized BLT NSG mice. Immunology 136(3):334–343. doi:10.1111/j.1365-2567.2012.03585.x PubMedPubMedCentralCrossRef

39.

Akkina R (2013) Human immune responses and potential for vaccine assessment in humanized mice. Curr Opin Immunol 25(3):403–409. doi:10.1016/j.coi.2013.03.009 PubMedPubMedCentralCrossRef

40.

Mota J, Rico-Hesse R (2011) Dengue virus tropism in humanized mice recapitulates human dengue fever. PLoS One 6(6):e20762. doi:10.1371/journal.pone.0020762 PubMedPubMedCentralCrossRef

41.

Christofferson RC, McCracken MK, Johnson AM, Chisenhall DM, Mores CN (2013) Development of a transmission model for dengue virus. Virol J 10:127. doi:10.1186/1743-422X-10-127 PubMedPubMedCentralCrossRef

42.

Prestwood TR, Prigozhin DM, Sharar KL, Zellweger RM, Shresta S (2008) A mouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads. J Virol 82(17):8411–8421. doi:10.1128/JVI.00611-08 PubMedPubMedCentralCrossRef

43.

Shresta S, Sharar KL, Prigozhin DM, Beatty PR, Harris E (2006) Murine model for dengue virus-induced lethal disease with increased vascular permeability. J Virol 80(20):10208–10217PubMedPubMedCentralCrossRef

44.

Tan GK, Ng JK, Trasti SL, Schul W, Yip G, Alonso S (2010) A non mouse-adapted dengue virus strain as a new model of severe dengue infection in AG129 mice. PLoS Negl Trop Dis 4(4):e672. doi:10.1371/journal.pntd.0000672 PubMedPubMedCentralCrossRef

45.

Wu-Hsieh BA, Yen YT, Chen HC (2009) Dengue hemorrhage in a mouse model. Ann N Y Acad Sci 1171(Suppl 1):E42–E47. doi:10.1111/j.1749-6632.2009.05053.x PubMedCrossRef

46.

Yen YT, Chen HC, Lin YD, Shieh CC, Wu-Hsieh BA (2008) Enhancement by tumor necrosis factor alpha of dengue virus-induced endothelial cell production of reactive nitrogen and oxygen species is key to hemorrhage development. J Virol 82(24):12312–12324PubMedPubMedCentralCrossRef

47.

Srikiatkhachorn A, Green S (2010) Markers of dengue disease severity. Curr Top Microbiol Immunol 338:67–82. doi:10.1007/978-3-642-02215-9_6 PubMed

48.

Banks RE, Forbes MA, Kinsey SE, Stanley A, Ingham E, Walters C, Selby PJ (1998) Release of the angiogenic cytokine vascular endothelial growth factor (VEGF) from platelets: significance for VEGF measurements and cancer biology. Br J Cancer 77(6):956–964PubMedPubMedCentralCrossRef

49.

Harrison S, Vavken P, Kevy S, Jacobson M, Zurakowski D, Murray MM (2011) Platelet activation by collagen provides sustained release of anabolic cytokines. Am J Sports Med 39(4):729–734. doi:10.1177/0363546511401576 PubMedPubMedCentralCrossRef

50.

Jessie K, Fong MY, Devi S, Lam SK, Wong KT (2004) Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J Infect Dis 189(8):1411–1418PubMedCrossRef

51.

Balsitis SJ, Coloma J, Castro G, Alava A, Flores D, McKerrow JH, Beatty PR, Harris E (2009) Tropism of dengue virus in mice and humans defined by viral nonstructural protein 3-specific immunostaining. AmJTrop Med Hyg 80(3):416–424

52.

Bhamarapravati N, Tuchinda P, Boonyapaknavik V (1967) Pathology of Thailand haemorrhagic fever: a study of 100 autopsy cases. Ann Trop Med Parasitol 61(4):500–510PubMedCrossRef

53.

Couvelard A, Marianneau P, Bedel C, Drouet MT, Vachon F, Henin D, Deubel V (1999) Report of a fatal case of dengue infection with hepatitis: demonstration of dengue antigens in hepatocytes and liver apoptosis. Hum Pathol 30(9):1106–1110PubMedCrossRef

54.

Limonta D, Capo V, Torres G, Perez AB, Guzman MG (2007) Apoptosis in tissues from fatal dengue shock syndrome. J Clin Virol 40(1):50–54PubMedCrossRef

55.

Taweechaisupapong S, Sriurairatana S, Angsubhakorn S, Yoksan S, Bhamarapravati N (1996) In vivo and in vitro studies on the morphological change in the monkey epidermal Langerhans cells following exposure to dengue 2 (16681) virus. Southeast Asian J Trop Med Public Health 27(4):664–672PubMed

56.

Libraty DH, Pichyangkul S, Ajariyakhajorn C, Endy TP, Ennis FA (2001) Human dendritic cells are activated by dengue virus infection: enhancement by gamma interferon and implications for disease pathogenesis. J Virol 75(8):3501–3508PubMedPubMedCentralCrossRef

57.

Marovich M, Grouard-Vogel G, Louder M, Eller M, Sun W, Wu SJ, Putvatana R, Murphy G, Tassaneetrithep B, Burgess T, Birx D, Hayes C, Schlesinger-Frankel S, Mascola J (2001) Human dendritic cells as targets of dengue virus infection. J Investig Dermatol Symp Proc 6(3):219–224PubMedCrossRef

58.

Chuang YC, Lei HY, Liu HS, Lin YS, Fu TF, Yeh TM (2011) Macrophage migration inhibitory factor induced by dengue virus infection increases vascular permeability. Cytokine 54(2):222–231. doi:10.1016/j.cyto.2011.01.013 PubMedCrossRef

59.

St John AL, Rathore AP, Raghavan B, Ng ML, Abraham SN (2013) Contributions of mast cells and vasoactive products, leukotrienes and chymase, to dengue virus-induced vascular leakage. elife 2:e00481. doi:10.7554/eLife.00481 PubMedPubMedCentralCrossRef

60.

St John AL, Rathore AP, Yap H, Ng ML, Metcalfe DD, Vasudevan SG, Abraham SN (2011) Immune surveillance by mast cells during dengue infection promotes natural killer (NK) and NKT-cell recruitment and viral clearance. Proc Natl Acad Sci U S A 108(22):9190–9195. doi:10.1073/pnas.1105079108 PubMedPubMedCentralCrossRef

61.

Libraty DH, Young PR, Pickering D, Endy TP, Kalayanarooj S, Green S, Vaughn DW, Nisalak A, Ennis FA, Rothman AL (2002) High circulating levels of the dengue virus nonstructural protein NS1 early in dengue illness correlate with the development of dengue hemorrhagic fever. J Infect Dis 186(8):1165–1168PubMedCrossRef

62.

Pichyangkul S, Endy TP, Kalayanarooj S, Nisalak A, Yongvanitchit K, Green S, Rothman AL, Ennis FA, Libraty DH (2003) A blunted blood plasmacytoid dendritic cell response to an acute systemic viral infection is associated with increased disease severity. J Immunol 171(10):5571–5578PubMedCrossRef

63.

Sun P, Garcia J, Comach G, Vahey MT, Wang Z, Forshey BM, Morrison AC, Sierra G, Bazan I, Rocha C, Vilcarromero S, Blair PJ, Scott TW, Camacho DE, Ockenhouse CF, Halsey ES, Kochel TJ (2013) Sequential waves of gene expression in patients with clinically defined dengue illnesses reveal subtle disease phases and predict disease severity. PLoS Negl Trop Dis 7(7):e2298. doi:10.1371/journal.pntd.0002298 PubMedPubMedCentralCrossRef

64.

Libraty DH, Endy TP, Houng HS, Green S, Kalayanarooj S, Suntayakorn S, Chansiriwongs W, Vaughn DW, Nisalak A, Ennis FA, Rothman AL (2002) Differing influences of virus burden and immune activation on disease severity in secondary dengue-3 virus infections. J Infect Dis 185(9):1213–1221PubMedCrossRef

65.

Modhiran N, Watterson D, Muller DA, Panetta AK, Sester DP, Liu L, Hume DA, Stacey KJ, Young PR (2015) Dengue virus NS1 protein activates cells via Toll-like receptor 4 and disrupts endothelial cell monolayer integrity. Sci Transl Med 7(304):304ra142. doi:10.1126/scitranslmed.aaa3863 PubMedCrossRef

66.

Chen HR, Chuang YC, Lin YS, Liu HS, Liu CC, Perng GC, Yeh TM (2016) Dengue virus nonstructural protein 1 induces vascular leakage through macrophage migration inhibitory factor and autophagy. PLoS Negl Trop Dis 10(7):e0004828. doi:10.1371/journal.pntd.0004828 PubMedPubMedCentralCrossRef

67.

Beatty PR, Puerta-Guardo H, Killingbeck SS, Glasner DR, Hopkins K, Harris E (2015) Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination. Sci Transl Med 7(304):304ra141. doi:10.1126/scitranslmed.aaa3787 PubMedCrossRef

68.

Green S, Pichyangkul S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Nisalak A, Kurane I, Rothman AL, Ennis FA (1999) Early CD69 expression on peripheral blood lymphocytes from children with dengue hemorrhagic fever. J Infect Dis 180(5):1429–1435PubMedCrossRef

69.

Lim DS, Yawata N, Selva KJ, Li N, Tsai CY, Yeong LH, Liong KH, Ooi EE, Chong MK, Ng ML, Leo YS, Yawata M, Wong SB (2014) The combination of type I IFN, TNF-alpha, and cell surface receptor engagement with dendritic cells enables NK cells to overcome immune evasion by dengue virus. J Immunol 193(10):5065–5075. doi:10.4049/jimmunol.1302240 PubMedCrossRef

70.

Azeredo EL, De Oliveira-Pinto LM, Zagne SM, Cerqueira DI, Nogueira RM, Kubelka CF (2006) NK cells, displaying early activation, cytotoxicity and adhesion molecules, are associated with mild dengue disease. Clin Exp Immunol 143(2):345–356. doi:10.1111/j.1365-2249.2006.02996.x PubMedPubMedCentralCrossRef

71.

Sung JM, Lee CK, Wu-Hsieh BA (2012) Intrahepatic infiltrating NK and CD8 T cells cause liver cell death in different phases of dengue virus infection. PLoS One 7(9):e46292. doi:10.1371/journal.pone.0046292 PubMedPubMedCentralCrossRef

72.

Kalayanarooj S, Vaughn DW, Nimmannitya S, Green S, Suntayakorn S, Kunentrasai N, Viramitrachai W, Ratanachu-eke S, Kiatpolpoj S, Innis BL, Rothman AL, Nisalak A, Ennis FA (1997) Early clinical and laboratory indicators of acute dengue illness. J Infect Dis 176(2):313–321PubMedCrossRef

73.

Matangkasombut P, Chan-In W, Opasawaschai A, Pongchaikul P, Tangthawornchaikul N, Vasanawathana S, Limpitikul W, Malasit P, Duangchinda T, Screaton G, Mongkolsapaya J (2014) Invariant NKT cell response to dengue virus infection in human. PLoS Negl Trop Dis 8(6):e2955. doi:10.1371/journal.pntd.0002955 PubMedPubMedCentralCrossRef

74.

Juno JA, Keynan Y, Fowke KR (2012) Invariant NKT cells: regulation and function during viral infection. PLoS Pathog 8(8):e1002838. doi:10.1371/journal.ppat.1002838 PubMedPubMedCentralCrossRef

75.

Renneson J, Guabiraba R, Maillet I, Marques RE, Ivanov S, Fontaine J, Paget C, Quesniaux V, Faveeuw C, Ryffel B, Teixeira MM, Trottein F (2011) A detrimental role for invariant natural killer T cells in the pathogenesis of experimental dengue virus infection. Am J Pathol 179(4):1872–1883. doi:10.1016/j.ajpath.2011.06.023 PubMedPubMedCentralCrossRef

76.

Calvert JK, Helbig KJ, Dimasi D, Cockshell M, Beard MR, Pitson SM, Bonder CS, Carr JM (2015) Dengue virus infection of primary endothelial cells induces innate immune responses, changes in endothelial cells function and is restricted by interferon-stimulated responses. J Interf Cytokine Res 35(8):654–665. doi:10.1089/jir.2014.0195 CrossRef

77.

Warke RV, Xhaja K, Martin KJ, Fournier MF, Shaw SK, Brizuela N, de Bosch N, Lapointe D, Ennis FA, Rothman AL, Bosch I (2003) Dengue virus induces novel changes in gene expression of human umbilical vein endothelial cells. J Virol 77(21):11822–11832PubMedPubMedCentralCrossRef

78.

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(2):171–180PubMedCrossRef

79.

Liu P, Woda M, Ennis FA, Libraty DH (2009) Dengue virus infection differentially regulates endothelial barrier function over time through type I interferon effects. J Infect Dis 200(2):191–201. doi:10.1086/599795 PubMedCrossRef

80.

Srikiatkhachorn A, Ajariyakhajorn C, Endy TP, Kalayanarooj S, Libraty DH, Green S, Ennis FA, Rothman AL (2007) Virus-induced decline in soluble vascular endothelial growth receptor 2 is associated with plasma leakage in dengue hemorrhagic fever. J Virol 81(4):1592–1600. doi:10.1128/JVI.01642-06 PubMedCrossRef

81.

Bravo JR, Guzman MG, Kouri GP (1987) Why dengue haemorrhagic fever in Cuba? 1. Individual risk factors for dengue haemorrhagic fever/dengue shock syndrome (DHF/DSS). Trans R Soc Trop Med Hyg 81(5):816–820PubMedCrossRef

82.

Rothman AL (2011) Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat Rev Immunol 11(8):532–543. doi:10.1038/nri3014 PubMedCrossRef

83.

Rivino L, Kumaran EA, Jovanovic V, Nadua K, Teo EW, Pang SW, Teo GH, Gan VC, Lye DC, Leo YS, Hanson BJ, Smith KG, Bertoletti A, Kemeny DM, MacAry PA (2013) Differential targeting of viral components by CD4+ versus CD8+ T lymphocytes in dengue virus infection. J Virol 87(5):2693–2706. doi:10.1128/JVI.02675-12 PubMedPubMedCentralCrossRef

84.

Weiskopf D, Cerpas C, Angelo MA, Bangs DJ, Sidney J, Paul S, Peters B, Sanches FP, Silvera CG, Costa PR, Kallas EG, Gresh L, de Silva AD, Balmaseda A, Harris E, Sette A (2015) Human CD8+ T-cell responses against the 4 dengue virus serotypes are associated with distinct patterns of protein targets. J Infect Dis 212(11):1743–1751. doi:10.1093/infdis/jiv289 PubMedPubMedCentralCrossRef

85.

Friberg H, Burns L, Woda M, Kalayanarooj S, Endy TP, Stephens HA, Green S, Rothman AL, Mathew A (2011) Memory CD8+ T cells from naturally acquired primary dengue virus infection are highly cross-reactive. Immunol Cell Biol 89(1):122–129. doi:10.1038/icb.2010.61 PubMedCrossRef

86.

Mongkolsapaya J, Duangchinda T, Dejnirattisai W, Vasanawathana S, Avirutnan P, Jairungsri A, Khemnu N, Tangthawornchaikul N, Chotiyarnwong P, Sae-Jang K, Koch M, Jones Y, McMichael A, Xu X, Malasit P, Screaton G (2006) T cell responses in dengue hemorrhagic fever: are cross-reactive T cells suboptimal? J Immunol 176(6):3821–3829PubMedCrossRef

87.

Mongkolsapaya J, Dejnirattisai W, Xu XN, Vasanawathana S, Tangthawornchaikul N, Chairunsri A, Sawasdivorn S, Duangchinda T, Dong T, Rowland-Jones S, Yenchitsomanus PT, McMichael A, Malasit P, Screaton G (2003) Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 9(7):921–927PubMedCrossRef

88.

Townsley E, Woda M, Thomas SJ, Kalayanarooj S, Gibbons RV, Nisalak A, Srikiatkhachorn A, Green S, Stephens HA, Rothman AL, Mathew A (2013) Distinct activation phenotype of a highly conserved novel HLA-B57-restricted epitope during dengue virus infection. Immunology. doi:10.1111/imm.12161 PubMedCentral

89.

Braga EL, Moura P, Pinto LM, Ignacio SR, Oliveira MJ, Cordeiro MT, Kubelka CF (2001) Detection of circulant tumor necrosis factor-alpha, soluble tumor necrosis factor p75 and interferon-gamma in Brazilian patients with dengue fever and dengue hemorrhagic fever. Memorias do Instituto Oswaldo Cruz 96(2):229–232PubMedCrossRef

90.

Green S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Suntayakorn S, Nisalak A, Lew R, Innis BL, Kurane I, Rothman AL, Ennis FA (1999) Early immune activation in acute dengue illness is related to development of plasma leakage and disease severity. J Infect Dis 179(4):755–762. doi:10.1086/314680 PubMedCrossRef

91.

Lok SM (2016) The interplay of dengue virus morphological diversity and human antibodies. Trends Microbiol 24(4):284–293. doi:10.1016/j.tim.2015.12.004 PubMedCrossRef

92.

Ubol S, Phuklia W, Kalayanarooj S, Modhiran N (2010) Mechanisms of immune evasion induced by a complex of dengue virus and preexisting enhancing antibodies. J Infect Dis 201(6):923–935. doi:10.1086/651018 PubMedCrossRef

93.

Green S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Suntayakorn S, Nisalak A, Rothman AL, Ennis FA (1999) Elevated plasma interleukin-10 levels in acute dengue correlate with disease severity. J Med Virol 59(3):329–334PubMedCrossRef

94.

Huang X, Yue Y, Li D, Zhao Y, Qiu L, Chen J, Pan Y, Xi J, Wang X, Sun Q, Li Q (2016) Antibody-dependent enhancement of dengue virus infection inhibits RLR-mediated type-I IFN-independent signalling through upregulation of cellular autophagy. Sci Rep 6:22303. doi:10.1038/srep22303 PubMedPubMedCentralCrossRef

95.

Xu M, Hadinoto V, Appanna R, Joensson K, Toh YX, Balakrishnan T, Ong SH, Warter L, Leo YS, Wang CI, Fink K (2012) Plasmablasts generated during repeated dengue infection are virus glycoprotein-specific and bind to multiple virus serotypes. J Immunol 189(12):5877–5885. doi:10.4049/jimmunol.1201688 PubMedCrossRef

96.

Priyamvada L, Cho A, Onlamoon N, Zheng NY, Huang M, Kovalenkov Y, Chokephaibulkit K, Angkasekwinai N, Pattanapanyasat K, Ahmed R, Wilson PC, Wrammert J (2016) B cell responses during secondary dengue virus infection are dominated by highly cross-reactive, memory-derived plasmablasts. J Virol 90(12):5574–5585. doi:10.1128/JVI.03203-15 PubMedPubMedCentralCrossRef

97.

Garcia-Bates TM, Cordeiro MT, Nascimento EJ, Smith AP, Soares de Melo KM, McBurney SP, Evans JD, Marques ET Jr, Barratt-Boyes SM (2013) Association between magnitude of the virus-specific plasmablast response and disease severity in dengue patients. J Immunol 190(1):80–87. doi:10.4049/jimmunol.1103350 PubMedCrossRef

98.

Woda M, Friberg H, Currier JR, Srikiatkhachorn A, Macareo LR, Green S, Jarman RG, Rothman AL, Mathew A (2016) Dynamics of dengue virus (DENV)-specific B cells in the response to DENV serotype 1 infections, using flow cytometry with labeled virions. J Infect Dis 214(7):1001–1009. doi:10.1093/infdis/jiw308 PubMedCrossRef

99.

Shen P, Fillatreau S (2015) Antibody-independent functions of B cells: a focus on cytokines. Nat Rev Immunol 15(7):441–451. doi:10.1038/nri3857 PubMedCrossRef

100.

Lopez-Ramirez MA, Fischer R, Torres-Badillo CC, Davies HA, Logan K, Pfizenmaier K, Male DK, Sharrack B, Romero IA (2012) Role of caspases in cytokine-induced barrier breakdown in human brain endothelial cells. J Immunol 189(6):3130–3139. doi:10.4049/jimmunol.1103460 PubMedCrossRef

101.

Mangada MM, Endy TP, Nisalak A, Chunsuttiwat S, Vaughn DW, Libraty DH, Green S, Ennis FA, Rothman AL (2002) Dengue-specific T cell responses in peripheral blood mononuclear cells obtained prior to secondary dengue virus infections in Thai schoolchildren. J Infect Dis 185(12):1697–1703. doi:10.1086/340822 PubMedCrossRef

102.

Ali T, Kaitha S, Mahmood S, Ftesi A, Stone J, Bronze MS (2013) Clinical use of anti-TNF therapy and increased risk of infections. Drug, healthcare and patient safety 5:79–99. doi:10.2147/DHPS.S28801 PubMedPubMedCentralCrossRef

103.

Augustin HG, Koh GY, Thurston G, Alitalo K (2009) Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 10(3):165–177. doi:10.1038/nrm2639 PubMedCrossRef

104.

Gavard J, Patel V, Gutkind JS (2008) Angiopoietin-1 prevents VEGF-induced endothelial permeability by sequestering Src through mDia. Dev Cell 14(1):25–36PubMedCrossRef

105.

Michels M, van der Ven AJ, Djamiatun K, Fijnheer R, de Groot PG, Griffioen AW, Sebastian S, Faradz SM, de Mast Q (2012) Imbalance of angiopoietin-1 and angiopoetin-2 in severe dengue and relationship with thrombocytopenia, endothelial activation, and vascular stability. AmJTrop Med Hyg 87(5):943–946. doi:10.4269/ajtmh.2012.12-0020 CrossRef

106.

Kim I, Oh JL, Ryu YS, So JN, Sessa WC, Walsh K, Koh GY (2002) Angiopoietin-1 negatively regulates expression and activity of tissue factor in endothelial cells. FASEB J 16(1):126–128. doi:10.1096/fj.01-0556fje PubMed

107.

Chen LC, Lei HY, Liu CC, Shiesh SC, Chen SH, Liu HS, Lin YS, Wang ST, Shyu HW, Yeh TM (2006) Correlation of serum levels of macrophage migration inhibitory factor with disease severity and clinical outcome in dengue patients. AmJTrop Med Hyg 74(1):142–147

108.

Ferreira RA, de Oliveira SA, Gandini M, Ferreira Lda C, Correa G, Abiraude FM, Reid MM, Cruz OG, Kubelka CF (2015) Circulating cytokines and chemokines associated with plasma leakage and hepatic dysfunction in Brazilian children with dengue fever. Acta Trop 149:138–147. doi:10.1016/j.actatropica.2015.04.023 PubMedCrossRef

109.

Boonnak K, Dambach KM, Donofrio GC, Tassaneetrithep B, Marovich MA (2011) Cell type specificity and host genetic polymorphisms influence antibody-dependent enhancement of dengue virus infection. J Virol 85(4):1671–1683. doi:10.1128/JVI.00220-10 PubMedCrossRef

110.

Luhn K, Simmons CP, Moran E, Dung NT, Chau TN, Quyen NT, Thao le TT, Van Ngoc T, Dung NM, Wills B, Farrar J, McMichael AJ, Dong T, Rowland-Jones S (2007) Increased frequencies of CD4+ CD25(high) regulatory T cells in acute dengue infection. J Exp Med 204(5):979–985. doi:10.1084/jem.20061381 PubMedPubMedCentralCrossRef

Title: Immune-mediated cytokine storm and its role in severe dengue
Authors: Anon Srikiatkhachorn
Anuja Mathew
Alan L. Rothman
Publication date: 01-07-2017
Publisher: Springer Berlin Heidelberg
Published in: Seminars in Immunopathology / Issue 5/2017
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI: https://doi.org/10.1007/s00281-017-0625-1

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