Molecular mimicry between dengue virus and coagulation factors induces antibodies to inhibit thrombin activity and enhance fibrinolysis

Journal of Virology

Volumn 88, Issue 23, 2014, Pages 13759-13768

  Chuang, Yung Chun ^a   Lin, Yee Shin ^a   Liu, Hsiao Sheng ^a   Yeh, Trai Ming ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; BLOOD CLOTTING FACTOR; CROSS REACTING ANTIBODY; DENGUE VACCINE; NONSTRUCTURAL PROTEIN 1; PLASMINOGEN; THROMBIN; VIRUS ANTIBODY; PROTEIN BINDING; VIRUS ANTIGEN;

ADSORPTION KINETICS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY AFFINITY; ANTIBODY PRODUCTION; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; CROSS REACTION; DENGUE; FEMALE; FIBRINOLYSIS; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; INHIBITION KINETICS; MOLECULAR MIMICRY; MOUSE; NONHUMAN; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BLOOD; DENGUE VIRUS; IMMUNOLOGY; METABOLISM; RABBIT;

DENGUE VIRUS;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; AUTOANTIBODIES; CROSS REACTIONS; DENGUE VIRUS; MICE, INBRED BALB C; MOLECULAR MIMICRY; PLASMINOGEN; PROTEIN BINDING; RABBITS; THROMBIN;

EID: 84911406544     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02166-14     Document Type: Article

References (48)

1. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, Hunsperger E, Kroeger A, Margolis HS, Martinez E, Nathan MB, Pelegrino JL, Simmons C, Yoksan S, Peeling RW. 2010. Dengue: a continuing global threat. Nat. Rev. Microbiol. 8:S7-S16. http://dx.doi.org /10.1038/nrmicro2460.
2. Young PR, Hilditch PA, Bletchly C, Halloran W. 2000. An antigen capture enzyme-linked immunosorbent assay reveals high levels of the dengue virus protein NS1 in the sera of infected patients. J. Clin. Microbiol. 38:1053-1057.
3. Alcon S, Talarmin A, Debruyne M, Falconar A, Deubel V, Flamand M. 2002. Enzyme-linked immunosorbent assay specific to dengue virus type 1 nonstructural protein NS1 reveals circulation of the antigen in the blood during the acute phase of disease in patients experiencing primary or secondary infections. J. Clin. Microbiol. 40:376-381. http://dx.doi.org/10 .1128/JCM.40.02.376-381.2002.
4. Guzman MG, Kouri G. 2002. Dengue: an update. Lancet Infect. Dis. 2:33-42. http://dx.doi.org/10.1016/S1473-3099(01)00171-2.
5. Halstead SB. 1982. Dengue: hematologic aspects. Semin. Hematol. 19: 116-131.
6. Rothman AL. 2004. Dengue: defining protective versus pathologic immunity. J. Clin. Invest. 113:946-951. http://dx.doi.org/10.1172/JCI21512.
7. Chuansumrit A, Puripokai C, Butthep P, Wongtiraporn W, Sasanakul W, Tangnararatchakit K, Chunhakan S, Yoksan S. 2010. Laboratory predictors of dengue shock syndrome during the febrile stage. Southeast Asian J. Trop. Med. Public Health 41:326-332.
8. Srikiatkhachorn A, Krautrachue A, Ratanaprakarn W, Wongtapradit L, Nithipanya N, Kalayanarooj S, Nisalak A, Thomas SJ, Gibbons RV, Mammen M P, 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. 26:283-290. http://dx.doi .org/10.1097/01.inf.0000258612.26743.10.
9. Marchi R, Nagaswami C, Weisel JW. 2009. Fibrin formation and lysis studies in dengue virus infection. Blood Coagul. Fibrinolysis 20:575-582. http://dx.doi.org/10.1097/MBC.0b013e32832fb1cf.
10. Halstead SB, O'Rourke EJ. 1977. Antibody-enhanced dengue virus infection in primate leukocytes. Nature 265:739-741. http://dx.doi.org/10 .1038/265739a0.
11. Halstead SB, O'Rourke EJ. 1977. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J. Exp. Med. 146:201-217.
12. Whitehead SS, Blaney JE, Durbin AP, Murphy BR. 2007. Prospects for a dengue virus vaccine. Nat. Rev. Microbiol. 5:518-528. http://dx.doi.org /10.1038/nrmicro1690.
13. Yacoub S, Mongkolsapaya J, Screaton G. 2013. The pathogenesis of dengue. Curr. Opin. Infect. Dis. 26:284-289. http://dx.doi.org/10.1097 /QCO.0b013e32835fb938.
14. Lei HY, Yeh TM, Liu HS, Lin YS, Chen SH, Liu CC. 2001. Immunopathogenesis of dengue virus infection. J. Biomed. Sci. 8:377-388. http: //dx.doi.org/10.1007/BF02255946.
15. Wan SW, Lin CF, Yeh TM, Liu CC, Liu HS, Wang S, Ling P, Anderson R, Lei HY, Lin YS. 2013. Autoimmunity in dengue pathogenesis. J. Formos. Med. Assoc. 112:3-11. http://dx.doi.org/10.1016/j .jfma.2012.11.006.
16. Cheng HJ, Lin CF, Lei HY, Liu HS, Yeh TM, Luo YH, Lin YS. 2009. Proteomic analysis of endothelial cell autoantigens recognized by antidengue virus nonstructural protein 1 antibodies. Exp. Biol. Med. (Maywood, NJ) 234:63-73. http://dx.doi.org/10.3181/0805-RM-147.
17. Rai CI, Lei HY, Lin YS, Liu HS, Chen SH, Chen LC, Yeh TM. 2008. Epitope mapping of dengue-virus-enhancing monoclonal-antibody using phage display peptide library. Am. J. Infect. Dis. 4:75-84. http://dx.doi .org/10.3844/ajidsp.2008.76.84.
18. Chen MC, Lin CF, Lei HY, Lin SC, Liu HS, Yeh TM, Anderson R, Lin YS. 2009. Deletion of the C-terminal region of dengue virus nonstructural protein 1 (NS1) abolishes anti-NS1-mediated platelet dysfunction and bleeding tendency. J. Immunol. 183:1797-1803. http://dx.doi.org/10 .4049/jimmunol.0800672.
19. Lin CF, Lei HY, Liu CC, Liu HS, Yeh TM, Wang ST, Yang TI, Sheu FC, Kuo CF, Lin YS. 2001. Generation of IgM anti-platelet autoantibody in dengue patients. J. Med. Virol. 63:143-149. http://dx.doi.org/10.1002 /1096-9071(20000201)63:2<143::AID-JMV1009>3.0.CO;2-L.
20. Lin CF, Lei HY, Shiau AL, Liu CC, Liu HS, Yeh TM, Chen SH, Lin YS. 2003. Antibodies from dengue patient sera cross-react with endothelial cells and induce damage. J. Med. Virol. 69:82-90. http://dx.doi.org/10 .1002/jmv.10261.
21. Lin CF, Wan SW, Chen MC, Lin SC, Cheng CC, Chiu SC, Hsiao YL, Lei HY, Liu HS, Yeh TM, Lin YS. 2008. Liver injury caused by antibodies against dengue virus nonstructural protein 1 in a murine model. Lab. Invest. 88:1079-1089. http://dx.doi.org/10.1038/labinvest.2008.70.
22. Versteeg HH, Heemskerk JW, Levi M, Reitsma PH. 2013. New fundamentals in hemostasis. Physiol. Rev. 93:327-358. http://dx.doi.org/10 .1152/physrev.00016.2011.
23. Albuquerque LM, Trugilho MR, Chapeaurouge A, Jurgilas PB, Bozza PT, Bozza FA, Perales J, Neves-Ferreira AG. 2009. Two-dimensional difference gel electrophoresis (DiGE) analysis of plasmas from dengue fever patients. J. Proteome Res. 8:5431-5441. http://dx.doi.org/10.1021 /pr900236f.
24. Huang YH, Liu CC, Wang ST, Lei HY, Liu HL, Lin YS, Wu HL, Yeh TM. 2001. Activation of coagulation and fibrinolysis during dengue virus infection. J. Med. Virol. 63:247-251. http://dx.doi.org/10.1002/1096 -9071(200103)63:3<247::AID-JMV1008>3.0.CO;2-F.
25. Wills BA, Oragui EE, Stephens AC, Daramola OA, Dung NM, Loan HT, Chau NV, Chambers M, Stepniewska K, Farrar JJ, Levin M. 2002. Coagulation abnormalities in dengue hemorrhagic fever: serial investigations in 167 Vietnamese children with Dengue shock syndrome. Clin. Infect. Dis. 35:277-285. http://dx.doi.org/10.1086/341410.
26. Avila-Aguero ML, Avila-Aguero CR, Um SL, Soriano-Fallas A, Canas- Coto A, Yan SB. 2004. Systemic host inflammatory and coagulation response in the Dengue virus primo-infection. Cytokine 27:173-179. http: //dx.doi.org/10.1016/j.cyto.2004.05.007.
27. Oldstone MB. 2005. Molecular mimicry, microbial infection, and autoimmune disease: evolution of the concept. Curr. Top. Microbiol. Immunol. 296:1-17. http://dx.doi.org/10.1007/3-540-30791-5_1.
28. Srinivasappa J, Saegusa J, Prabhakar BS, Gentry MK, Buchmeier MJ, Wiktor TJ, Koprowski H, Oldstone MB, Notkins AL. 1986. Molecular mimicry: frequency of reactivity of monoclonal antiviral antibodies with normal tissues. J. Virol. 57:397-401.
29. Markoff LJ, Innis BL, Houghten R, Henchal LS. 1991. Development of cross-reactive antibodies to plasminogen during the immune response to dengue virus infection. J. Infect. Dis. 164:294-301. http://dx.doi.org/10 .1093/infdis/164.2.294.
30. Chungue E, Poli L, Roche C, Gestas P, Glaziou P, Markoff LJ. 1994. Correlation between detection of plasminogen cross-reactive antibodies and hemorrhage in dengue virus infection. J. Infect. Dis. 170:1304-1307. http://dx.doi.org/10.1093/infdis/170.5.1304.
31. Chuang YC, Lin YS, Liu HS, Wang JR, Yeh TM. 2013. Antibodies against thrombin in dengue patients contain both anti-thrombotic and pro-fibrinolytic activities. Thromb. Haemost. 110:358-365. http://dx.doi .org/10.1160/TH13-02-0149.
32. Lin YS, Yeh TM, Lin CF, Wan SW, Chuang YC, Hsu TK, Liu HS, Liu CC, Anderson R, Lei HY. 2011. Molecular mimicry between virus and host and its implications for dengue disease pathogenesis. Exp. Biol. Med. (Maywood, NJ) 236:515-523. http://dx.doi.org/10.1258/ebm.2011.010339.
33. Oldstone MB. 1998. Molecular mimicry and immune-mediated diseases. FASEB J. 12:1255-1265.
34. Zhou ZH, Tzioufas AG, Notkins AL. 2007. Properties and function of polyreactive antibodies and polyreactive antigen-binding B cells. J. Autoimmun. 29:219-228. http://dx.doi.org/10.1016/j.jaut.2007.07.015.
35. Tracy SI, Kakalacheva K, Lunemann JD, Luzuriaga K, Middeldorp J, Thorley-Lawson DA. 2012. Persistence of Epstein-Barr virus in selfreactive memory B cells. J. Virol. 86:12330-12340. http://dx.doi.org/10 .1128/JVI.01699-12.
36. Chuang YC, Lei HY, Lin YS, Liu HS, Wu HL, Yeh TM. 2011. Dengue virus-induced autoantibodies bind to plasminogen and enhance its activation. J. Immunol. 187:6483-6490. http://dx.doi.org/10.4049/jimmunol .1102218.
37. Lin SW, Chuang YC, Lin YS, Lei HY, Liu HS, Yeh TM. 2012. Dengue virus nonstructural protein NS1 binds to prothrombin/thrombin and inhibits prothrombin activation. J. Infect. 64:325-334. http://dx.doi.org/10 .1016/j.jinf.2011.11.023.
38. Huber-Lang M, Sarma JV, Zetoune FS, Rittirsch D, Neff TA, McGuire SR, Lambris JD, Warner RL, Flierl MA, Hoesel LM, Gebhard F, Younger JG, Drouin SM, Wetsel RA, Ward PA. 2006. Generation of C5a in the absence of C3: a new complement activation pathway. Nat. Med. 12:682-687. http://dx.doi.org/10.1038/nm1419.
39. Falconar AK. 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. http: //dx.doi.org/10.1007/s007050050127.
40. Liu IJ, Chiu CY, Chen YC, Wu HC. 2011. Molecular mimicry of human endothelial cell antigen by autoantibodies to nonstructural protein 1 of dengue virus. J. Biol. Chem. 286:9726-9736. http://dx.doi.org/10.1074 /jbc.M110.170993.
41. Oldstone MB. 2014. Molecular mimicry: its evolution from concept to mechanism as a cause of autoimmune diseases. Monoclon. Antib. Immunodiagn. Immunother. 33:158-165. http://dx.doi.org/10.1089/mab.2013 .0090.
42. Van Parijs L, Abbas AK. 1998. Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science 280:243-248. http://dx .doi.org/10.1126/science.280.5361.243.
43. Anonymous. 1973. Pathogenetic mechanisms in dengue haemorrhagic fever: report of an international collaborative study. Bull. World Health Organ. 48:117-133.
44. Cheng HJ, Lei HY, Lin CF, Luo YH, Wan SW, Liu HS, Yeh TM, Lin YS. 2009. Anti-dengue virus nonstructural protein 1 antibodies recognize protein disulfide isomerase on platelets and inhibit platelet aggregation. Mol. Immunol. 47:398-406. http://dx.doi.org/10.1016/j.molimm.2009 .08.033.
45. 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. Am. J. Trop. Med. Hyg. 74:142-147.
46. Nguyen TH, Lei HY, Nguyen TL, Lin YS, Huang KJ, Le BL, 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. http://dx.doi.org/10.1086 /380762.
47. Avirutnan P, Zhang L, Punyadee N, Manuyakorn A, Puttikhunt C, Kasinrerk W, Malasit P, Atkinson JP, Diamond MS. 2007. Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E. PLoS Pathog. 3:e183. http://dx.doi .org/10.1371/journal.ppat.0030183.
48. Avirutnan P, Fuchs A, Hauhart RE, Somnuke P, Youn S, Diamond MS, Atkinson JP. 2010. Antagonism of the complement component C4 by flavivirus nonstructural protein NS1. J. Exp. Med. 207:793-806. http://dx .doi.org/10.1084/jem.20092545.