The cytokine response of U937-derived macrophages infected through antibody-dependent enhancement of dengue virus disrupts cell apical-junction complexes and increases vascular permeability

Journal of Virology

Volumn 87, Issue 13, 2013, Pages 7486-7501

  Puerta Guardo, Henry ^a   Raya Sandino, Arturo ^a   González Mariscal, Lorenza ^a   Rosales, Victor H ^b   Ayala Dávila, José ^a   Chávez Mungía, Bibiana ^a   Martínez Fong, Daniel ^a   Medina, Fernando ^a   Ludert, Juan E ^a   del Angel, Rosa María ^a  

^a Department of Infectomics and Molecular Pathogenesis ^*  (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12P70; INTERLEUKIN 6; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APICAL MEMBRANE; ARTICLE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DENGUE; DENGUE VIRUS; ELECTRIC RESISTANCE; HUMAN; HUMAN CELL; KIDNEY CELL CULTURE; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; TIGHT JUNCTION;

ANALYSIS OF VARIANCE; ANIMALS; ANTIBODY-DEPENDENT ENHANCEMENT; BLOTTING, WESTERN; CAPILLARY PERMEABILITY; CELL SURVIVAL; CULTURE MEDIA, CONDITIONED; CYTOKINES; DENGUE; DENGUE VIRUS; DOGS; ELECTRIC IMPEDANCE; EVANS BLUE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MACROPHAGES; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; TIGHT JUNCTIONS; U937 CELLS;

EID: 84880336701     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00085-13     Document Type: Article

References (78)

1. WHO 2009. Dengue guidelines for diagnosis, treatment, prevention and control. Fact sheet no. 117. WHO, Geneva, Switzerland. http://www.who.int/mediacentre/factsheets/fs117/en/. Accessed 16 October 2012.
2. Modis Y, Ogata S, Clements D, Harrison SC. 2003. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 100:6986-6991.
3. Zhang Y, Corver J, Chipman PR, Zhang W, Pletnev SV, Sedlak D, Baker TS, Strauss JH, Kuhn RJ, Rossmann MG. 2003. Structures of immature flavivirus particles. EMBO J. 22:2604-2613.
4. Martina BE, Koraka P, Osterhaus AD. 2009. Dengue virus pathogenesis: an integrated view. Clin. Microbiol. Rev. 22:564-581.
5. Alcaraz-Estrada SL, Yocupicio-Monroy M, del Angel RM. 2010. Insights into dengue virus genome replication. Future Virol. 5:575-592.
6. Welsch S, Miller S, Romero-Brey I, Merz A, Bleck CK, Walther P, Fuller SD, Antony C, Krijnse-Locker J, Bartenschlager R. 2009. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 23:365-375.
7. Welsch S, Miller S, Romero-Brey I, Merz A, Bleck CK, Walther P, Fuller SD, Antony C, Krijnse-Locker J, Bartenschlager R. 2009. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 23:365-375.
8. Basu A, Chaturvedi UC. 2008. Vascular endothelium: the battle field of dengue viruses. FEMS Immunol. Med. Microbiol. 53:287-299.
9. Walleza B, Huber P. 2008. Endothelial adherens and tight junctions in vascular homeostasis, inflammation and angiogenesis. Biochim. Biophys. Acta 1778:794-809.
10. Halstead SB, O'Rourke E. 1977. Antibody-enhanced dengue virus infection in primate leukocytes. Nature 265:739-741.
11. Ubol S, Halstead SB. 2010. How innate immune mechanisms contribute to antibody-enhanced viral infections. Clin. Vaccine Immunol. 17:1829-1835.
12. Goncálvez AP, Engle RE, Claire MS, Purcell RH, Lai CJ. 2007. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc. Natl. Acad. Sci. U.S.A. 104:9422-9427.
13. Morens D, Halstead SB. 1990. Measurement of antibody-dependent infection enhancement of four dengue virus serotypes by monoclonal and polyclonal antibodies. J. Gen. Virol. 71:2909-2914.
14. Halstead SB, O'Rourke EJ. 1977. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J. Exp. Med. 146:201-217.
15. Kliks SC, Nisalak A, Brandt WE, Wahl L, Burke DS. 1989. Antibodydependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am. J. Trop. Med. Hyg. 40:444-451.
16. Puerta-Guardo H, Mosso C, Medina F, Liprandi F, Ludert JE, del Angel RM. 2010. Antibody-dependent enhancement of dengue virus infection in U937 cells requires cholesterol-rich membrane microdomains. J. Gen. Virol. 91:394-403.
17. Chaturvedi UC, Agarwal R, Elbishbishi EA, Mustafa AS. 2000. Cytokine cascade in dengue hemorrhagic fever: implications for pathogenesis. FEMS Immunol. Med. Microbiol. 28:183-188.
18. Green S, Rothman A. 2006. Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr. Opin. Infect. Dis. 19:429-436.
19. Halstead S. 1989. Antibody, macrophages, dengue virus infection, shock and hemorrhage: a pathogenic cascade. Rev. Infect. Dis. 11:S830-S839.
20. Rothman AL. 2011. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat. Rev. Immunol. 11:532-543.
21. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL, Mehlhop E, Johnson S, Diamond MS, Beatty PR, Harris E. 2010. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog. 6:e1000790. doi:10.1371/journal.ppat.1000790.
22. Chareonsirisuthigul T, Kalayanarooj S, Ubol S. 2007. Dengue virus(DENV) antibody-dependent enhancement of infection upregulates the production of anti-inflammatory cytokines, but suppresses anti-DENV free radical and pro-inflammatory cytokine production, in THP-1 cells. J. Gen. Virol. 88:365-375.
23. 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. 201:923-935.
24. Boonnak K, Slike BM, Burgess TH, Mason RM, Wu SJ, Sun P, Porter K, Rudiman IF, Yuwono D, Puthavathana P, Marovich MA. 2008. Role of dendritic cells in antibody-dependent enhancement of dengue virus infection. J. Virol. 82:3939-3951.
25. Boonnak K, Dambach KM, Donofrio GC, Tassaneetrithep B. 2011. Cell type specific and host polymorphisms influence antibody dependent enhancement of dengue virus infection. J. Virol. 85:1671-1683.
26. Simmons CP, Farrar JJ, van Vinh Chau N, Wills B. 2012. Dengue. N. Engl. J. Med. 366:1423-1432.
27. Gonzalez-Mariscal L, Chávez de Ramírez B, Cereijido M. 1985. Tight junction formation in cultured epithelial cells (MDCK). J. Membr. Biol.86:113-125.
28. Mosso C, Galván-Mendoza IJ, Ludert JE, del Angel RM. 2008. Endocytic pathway followed by dengue virus to infect the mosquito cell line C6/36 HT. Virology 378:193-199.
29. Manaenkoa A, Chena H, Kammerd J, Zhanga JH, Tanga J. 2011. Comparison Evans Blue injection routes: intravenous versus intraperitoneal, for measurement of blood-brain barrier in a mice hemorrhage model. J. Neurosci. Methods 195:206-210.
30. Peng X, Hassoun PM, Sammani S, McVerry BJ, Burne MJ, Rabb H, Pearse D, Tuder RM, Garcia JGN. 2004. Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am. J. Respir. Crit. Care Med. 169:1245-1251.
31. Flipse J, Wilschut J, Smit JM. 2012. Molecular mechanisms involved in antibody-dependent enhancement of dengue virus infection in humans. Traffic. doi:10.1111/tra.12012.
32. Modhiran N, Kalayanarooj S, Ubol S. 2010. Subversion of innate defenses by the interplay between DENV and pre-existing enhancing antibodies: TLRs signaling collapse. PLoS Negl. Trop. Dis. 4:e924. doi:10.1371/journal.pntd.0000924.
33. Nguyen TH, Lei HY, Nguyen TL, Lin YS, Huang KJ, Lien LB, Lin CF, Yeh TM, Do QH, Vu TQ, Chen LC, Huang JH, Lam TM, Liu CC, Halstead SB. 2004. Dengue hemorrhagic fever in infants: a study of clinical and cytokine profiles. J. Infect. Dis. 189:221-232.
34. 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. 179:755-762.
35. Ubol S, Masrinoul P, Chaijaruwanich J, Kalayanarooj S, Charoensirisuthikul T, Kasisith J. 2008. Differences in global gene expression in peripheral blood mononuclear cells indicate a significant role of the innate responses in progression of dengue fever but not dengue hemorrhagic fever. J. Infect. Dis. 197:1459-1467.
36. Bozza FA, Cruz OG, Zagne S, Azeredo E, Nogueira R, Assis EF, Bozza PT, Kubelka CF. 2008. Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity. BMC Infect. Dis. 8:86. doi:10.1186/1471-2334-8-86.
37. Restrepo BN, Ramirez RE, Arboleda M, Alvarez G, Ospina M, Diaz FJ. 2008. Serum levels of cytokines in two ethnic groups with dengue virus infection. Am. J. Trop. Med. Hyg. 79:673-677.
38. Clark IA. 2007. The advent of the cytokine storm. Immunol. Cell Biol. 85:271-273.
39. Hober D, Poli L, Roblin B, Gestas P, Chungue E, Granic G, Imbert P, Pecarere JL, Vergez-Pascal R, Wattre P, Maniez-Montreuil M. 1993. Serum levels of tumor necrosis factor-alpha (TNF-alpha), interleukin-6(IL-6), and interleukin-1 beta (IL-1 beta) in dengue-infected patients. Am. J. Trop. Med. Hyg. 48:324-331.
40. Chakravarti A, Kumaria R. 2006. Circulating levels of tumour necrosis factor-alpha & interferon-gamma in patients with dengue & dengue haemorrhagic fever during an outbreak. Indian J. Med. Res. 123:25-30.
41. Pérez AB, García G, Sierra B, Alvarez M, Vázquez S, Cabrera MV, Rodríguez R, Rosario D, Martínez E, Denny T, Guzmán MG. 2004. IL-10 levels in dengue patients: some findings from the exceptional epidemiological conditions in Cuba. J. Med. Virol. 73:230-234.
42. Bethell DB, Flobbe K, Cao XT, Day NP, Pham TP, Buurman WA, Cardosa WJ, White NJ, Kwiatkowski D. 1998. Pathophysiologic and prognostic role of cytokines in dengue hemorrhagic fever. J. Infect. Dis. 177:778-782.
43. Fernandez-Mestre MT, Gendzekhadze K, Rivas-Vetencourt P, Layrisse Z. 2004. TNF-alpha-308A allele, a possible severity risk factor of hemorrhagic manifestation in dengue fever patients. Tissue Antigens 64:469-472.
44. Perez AB, Sierra B, Garcia G, Aguirre E, Babel N, Alvarez M, Sanchez L, Valdés L, Volk H, Guzman MG. 2010. TNF-alpha, TGF-beta 1 and IL-10 gene polymorphisms: implication in protection or susceptibility to dengue hemorrhagic fever. Hum. Immunol. 71:1135-1140.
45. Raghupathy R, Chaturvedi UC, Al-Sayer H, Elbishbishi EA, Agarwal R, Nagar R, Kapoor RS, Misra A, Mathur A, Nusrat H, Azizieh F, Khan MAY, Mustafa AS. 1998. Elevated levels of IL-8 in dengue hemorrhagic fever. J. Med. Virol. 56:280-285.
46. Bosch I, Xhaja K, Estevez L, Raines G, Melichar H, Warke RV, Fournier MV, Ennis FA, Rothman AI. 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.
47. Pacsa AS, Agarwal R, Elbishbishi EA, Chaturvedi UC, Nagar R, Mustafa AS. 2000. Role of interleukin-12 in patients with dengue hemorrhagic fever. FEMS Immunol. Med. Microbiol. 28:151-155.
48. Cardier JE, Mariño E, Romano E, Taylor P, Liprandi F, Bosch N, Rothman AI. 2005. Proinflammatory factors present in sera from patients with acute dengue infection induce activation and apoptosis of human microvascular endothelial cells: possible role of TNF-α in endothelial cell damage in dengue. Cytokine 30:359-365.
49. Wu WL, Ho LJ, Chang DM, Chen CH, Lail JH. 2009. Triggering of DC migration by dengue virus stimulation of COX-2-dependent signaling cascades in vitro highlights the significance of these cascades beyond inflammation. Eur. J. Immunol. 39:3413-3422.
50. Chaturvedi UC. 2009. Shift to Th2 cytokine response in dengue haemorrhagic fever. Indian J. Med. Res. 129:1-3.
51. Carr JM, Hocking H, Bunting K, Wright PJ, Davidson A, Gamble J, Burrell CJ, Li P. 2003. Supernatants from dengue virus type-2 infected macrophages induce permeability changes in endothelial cell monolayers. J. Med. Virol. 69:521-528.
52. Dewi BE, Takasaki T, Kurane I. 2008. Peripheral blood mononuclear cells increase the permeability of dengue virus-infected endothelial cells in association with down-regulation of vascular endothelial cadherin. J. Gen. Virol. 89:642-652.
53. Ong SP, Lee LM, Leong YFI, Ng ML, Chu JJH. 2012. Dengue virus infection mediates HMGB1 release from monocytes involving PCAF acetylase complex and induces vascular leakage in endothelial cells. PLoS One 7:e41932. doi:10.1371/journal.pone.0041932.
54. 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 54:222-231.
55. Talavera D, Castillo AM, Dominguez MC, Escobar-Gutierrez A, Meza I. 2004. IL8 release, tight junction and cytoskeleton dynamic reorganization conducive to permeability increase are induced by dengue virus infectionof microvascular endothelial monolayers. J. Gen. Virol. 85:1801-1813.
56. Luplertlop N, Missé 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. 7:1176-1181.
57. Kelley JF, Kaufusi PH, Nerurkar VR. 2012. Dengue hemorrhagic feverassociated 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.
58. 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.
59. Jacobs M, Levin M. 2002. An improved endothelial barrier model to investigate dengue haemorrhagic fever. J. Virol. Methods 104:173-185.
60. Bonner SM, O'Sullivan MA. 1998. Endothelial cell monolayers as a model system to investigate dengue shock syndrome. J. Virol. Methods 71:159-167.
61. Montesano R, Soulie P, Eble JA, Carrozzino F. 2005. Tumor necrosis factor alpha confers an invasive, transformed phenotype in mammalian epithelial cells. J. Cell Sci. 118:3487-3500.
62. Jones SA, Horiuchi S, Topley N, Yamamoto N, Fuller GM. 2001. The soluble interleukin 6 receptor: mechanisms of production and implications in disease. FASEB J. 15:43-58.
63. Appanna R, Wang SM, Ponnampalavanar SA, Lum LC, Sekaran SD. 2012. Cytokine factors present in dengue patient sera induces alterationsof junctional proteins in human endothelial cells. Am. J. Trop. Med. Hyg.87:936-942.
64. González-Mariscal L, Tapia R, Chamorro D. 2008. Crosstalk of tight junction components with signaling pathways. Biochim. Biophys. Acta 1778:729-756.
65. Meza I, Sabanero M, Stefani E, Cereijido M. 1982. Occluding junctions in MDCK cells: modulation of transepithelial permeability by the cytoskeleton. J. Cell. Biochem. 18:407-421.
66. Clayburgh DR, Barrett TA, Tang Y, Meddings JB, Van Eldik LJ, Watterson DM, Clarke LL, Mrsny RJ, Turner JR. 2005. Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation- induced diarrhea in vivo. J. Clin. Invest. 115:2702-2715.
67. Blair SA, Kane SV, Clayburgh DR, Turner JR. 2006. Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease. Lab. Invest. 86:191-201.
68. Matsuda M, Kubo A, Furuse M, Tsukita S. 2004. A peculiar internalization of claudins, tight junction specific adhesion molecules, during the intercellular movement of epithelial cells. J. Cell Sci. 117:1247-1257.
69. Utech M, Mennigen R, Bruewer M. 2010. Endocytosis and recycling of tight junction proteins in inflammation. J. Biomed. Biotechnol. 2010:484987. doi:10.1155/2010/484987.
70. Ivanov AI, Nusrat A, Parkos CA. 2004. Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol. Biol. Cell 15:176-188.
71. Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JR. 2010. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J. Cell Biol. 189:111-126.
72. Shen L, Turner JR. 2005. Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol. Biol. Cell 16:3919-3936.
73. Bojarski C, Weiske J, Schüneberg T, Schrüder W, Mankertz J, Schulzke JD, Florian P, Fromm M, Tauber R, Huber T. 2004. The specific fates of tight junction proteins in apoptotic epithelial cells. J. Cell Sci. 117:2097-2107.
74. Medigeshi GR, Hirsch AJ, Brien JD, Uhrlaub JL, Mason PW, Wiley C, Nikolich-Zugish J, Nelson JA. 2009. West Nile virus capsid degradation of claudin proteins disrupts epithelial barrier function. J. Virol. 83:6125-6134.
75. Xu Z, Waeckerlin R, Urbanowski MD, van Marle G, Hobman TC. 2012. West Nile virus infection causes endocytosis of a specific subset of tight junction membrane proteins. PLoS One 7:e37886. doi:10.1371/journal.pone.0037886.
76. Patkar C, Giaya K, Libraty DH. 2013. Dengue virus type 2 modulates endothelial barrier function through CD73. Am. J. Trop. Med. Hyg. 88:89-94.
77. Dejana E. 2004. Endothelial cell-cell junctions: happy together. Nat. Rev. 5:261-270.
78. Niessen CM. 2007. Tight junctions/adherens junctions: basic structure and function. J. Investig. Dermatol. 127:2525-2532.