1921
Volume 92, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

We have previously shown that anti–dengue virus nonstructural protein 1 (anti-DENV NS1) antibodies cross-react with endothelial cells, and several autoantigens have been identified. This study shows that the antibody levels against these self-proteins are higher in sera from patients with dengue hemorrhagic fever (DHF) than those in control sera. Anti–protein disulfide isomerase (PDI) and anti–heat shock protein 60 (anti-HSP60) IgM levels correlated with both anti–endothelial cells and anti-DENV NS1 IgM titers. A cross-reactive epitope on the NS1 amino acid residues 311–330 (P311–330) had been predicted. We further found that there were higher IgM and IgG levels against P311–330 in DHF patients' sera than those in the control sera. In addition, correlations were observed between anti-PDI with anti-P311–330 IgM and IgG levels, respectively. Therefore, our results indicate that DENV NS1 P311–330 is a major epitope for cross-reactive antibodies to PDI on the endothelial cell surface, which may play an important role in DENV infection–induced autoimmunity.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.14-0162
2015-05-06
2017-11-24
Loading full text...

Full text loading...

/deliver/fulltext/14761645/92/5/989.html?itemId=/content/journals/10.4269/ajtmh.14-0162&mimeType=html&fmt=ahah

References

  1. Halstead SB, , 2002. Dengue. Curr Opin Infect Dis 15: 471476.[Crossref]
  2. Halstead SB, , 2007. Dengue. Lancet 370: 16441652.[Crossref]
  3. Green S, Rothman A, , 2006. Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr Opin Infect Dis 19: 429436.[Crossref]
  4. Kyle JL, Harris E, , 2008. Global spread and persistence of dengue. Annu Rev Microbiol 62: 7192.[Crossref]
  5. 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: 504507.[Crossref]
  6. 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: S7S16.[Crossref]
  7. Lin CC, Huang YH, Shu PY, Wu HS, Lin YS, Yeh TM, Liu HS, Liu CC, Lei HY, , 2010. Characteristic of dengue disease in Taiwan: 2002–2007. Am J Trop Med Hyg 82: 731739.[Crossref]
  8. Simmons CP, Farrar JJ, Nguyen vV, Wills B, , 2012. Dengue. N Engl J Med 366: 14231432.[Crossref]
  9. Whitehead SS, Blaney JE, Durbin AP, Murphy BR, , 2007. Prospects for a dengue virus vaccine. Nat Rev Microbiol 5: 518528.[Crossref]
  10. Webster DP, Farrar J, Rowland-Jones S, , 2009. Progress towards a dengue vaccine. Lancet Infect Dis 9: 678687.[Crossref]
  11. Thomas SJ, Endy TP, , 2011. Critical issues in dengue vaccine development. Curr Opin Infect Dis 24: 442450.[Crossref]
  12. Coller BA, Clements DE, , 2011. Dengue vaccines: progress and challenges. Curr Opin Immunol 23: 391398.[Crossref]
  13. Sabchareon A, Wallace D, Sirivichayakul C, Limkittikul K, Chanthavanich P, Suvannadabba S, Jiwariyavej V, Dulyachai W, Pengsaa K, Wartel TA, Moureau A, Saville M, Bouckenooghe A, Viviani S, Tornieporth NG, Lang J, , 2012. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380: 15591567.[Crossref]
  14. Durbin AP, Wright PF, Cox A, Kagucia W, Elwood D, Henderson S, Wanionek K, Speicher J, Whitehead SS, Pletnev AG, , 2013. The live attenuated chimeric vaccine rWN/DEN4Δ30 is well-tolerated and immunogenic in healthy flavivirus-naïve adult volunteers. Vaccine 31: 57725777.[Crossref]
  15. Dayan GH, Garbes P, Noriega F, de Sadovsky ADI, Rodrigues PM, Giuberti C, Dietze R, , 2013. Immunogenicity and safety of a recombinant tetravalent dengue vaccine in children and adolescents ages 9–16 years in Brazil. Am J Trop Med Hyg 89: 10581065.[Crossref]
  16. Wan SW, Lin CF, Wang S, Chen YH, Yeh TM, Liu HS, Anderson R, Lin YS, , 2013. Current progress in dengue vaccines. J Biomed Sci 20: 37.[Crossref]
  17. Halstead SB, , 2013. Identifying protective dengue vaccines: guide to mastering an empirical process. Vaccine 31: 45014507.[Crossref]
  18. Halstead SB, O'Rourke EJ, , 1977. Antibody-enhanced dengue virus infection in primate leukocytes. Nature 265: 739741.[Crossref]
  19. Halstead SB, , 1988. Pathogenesis of dengue: challenges to molecular biology. Science 239: 476481.[Crossref]
  20. Goncalvez AP, Engle RE, St Claire M, 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 USA 104: 94229427.[Crossref]
  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.[Crossref]
  22. Martina BEE, Koraka P, Osterhaus ADME, , 2009. Dengue virus pathogenesis: an integrated view. Clin Microbiol Rev 22: 564581.[Crossref]
  23. Herrero LJ, Zakhary A, Gahan ME, Nelson MA, Herring BL, Hapel AJ, Keller PA, Obeysekera M, Chen W, Sheng KC, Taylor A, Wolf S, Bettadapura J, Broor S, Dar L, Mahalingam S, , 2013. Dengue virus therapeutic intervention strategies based on viral, vector and host factors involved in disease pathogenesis. Pharmacol Ther 137: 266282.[Crossref]
  24. Lei HY, Yeh TM, Liu HS, Lin YS, Chen SH, Liu CC, , 2001. Immunopathogenesis of dengue virus infection. J Biomed Sci 8: 377388.[Crossref]
  25. Lei HY, , 2009. Transient hemophagocytic activity in dengue immunopathogenesis. J Formos Med Assoc 108: 595598.[Crossref]
  26. Nielsen DG, , 2009. The relationship of interacting immunological components in dengue pathogenesis. Virol J 6: 211217.[Crossref]
  27. Gubler DJ, , 1998. Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11: 480496.
  28. Clyde K, Kyle JL, Harris E, , 2006. Recent advances in deciphering viral and host determinants of dengue virus replication and pathogenesis. J Virol 80: 1141811431.[Crossref]
  29. Srikiatkhachorn A, , 2009. Plasma leakage in dengue haemorrhagic fever. Thromb Haemost 102: 10421049.
  30. Basu A, Chaturvedi UC, , 2008. Vascular endothelium: the battlefield of dengue viruses. FEMS Immunol Med Microbiol 53: 287299.[Crossref]
  31. 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: 143149.[Crossref]
  32. 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: 8290.[Crossref]
  33. 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: 897916.[Crossref]
  34. Falconar AK, , 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: 493504.[Crossref]
  35. Lin CF, Lei HY, Shiau AL, Liu HS, Yeh TM, Chen SH, Liu CC, Chiu SC, Lin YS, , 2002. Endothelial cell apoptosis induced by antibodies against dengue virus nonstructural protein 1 via production of nitric oxide. J Immunol 169: 657664.[Crossref]
  36. Lin CF, Chiu SC, Hsiao YL, Wan SW, Lei HY, Shiau AL, Liu HS, Yeh TM, Chen SH, Liu CC, Lin YS, , 2005. Expression of cytokine, chemokine, and adhesion molecules during endothelial cell activation induced by antibodies against dengue virus nonstructural protein 1. J Immunol 174: 395403.[Crossref]
  37. Lin CF, Lei HY, Liu CC, Liu HS, Yeh TM, Anderson R, Lin YS, , 2008. Patient and mouse antibodies against dengue virus nonstructural protein 1 cross-react with platelets and cause their dysfunction or depletion. Am J Infect Dis 4: 6975.[Crossref]
  38. 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: 97269736.[Crossref]
  39. 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: 311.[Crossref]
  40. Cheng HJ, Lin CF, Lei HY, Liu HS, Yeh TM, Luo YH, Lin YS, , 2009. Proteomic analysis of endothelial cell autoantigens recognized by anti-dengue virus nonstructural protein 1 antibodies. Exp Biol Med 234: 6373.[Crossref]
  41. 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: 398406.[Crossref]
  42. Wan SW, Lin CF, Chen MC, Lei HY, Liu HS, Yeh TM, Liu CC, Lin YS, , 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: 8591.[Crossref]
  43. World Health Organization, 1997. Dengue Hemorrhagic Fever: Diagnosis, Treatment, Prevention and Control. 2nd ed. Geneva, Switzerland: World Health Organization.
  44. Hung NT, Lei HY, Lan NT, Lin YS, Huang KJ, Lien LB, Lin CF, Yeh TM, Ha DQ, Huong VTQ, Chen LC, Huang JH, My LY, Liu CC, Halstead SB, , 2004. Dengue hemorrhagic fever in infants: a study of clinical and cytokine profiles. J Infect Dis 189: 221232.[Crossref]
  45. Hung NT, Lan NT, Lei HY, Lin YS, Lien LB, Huang KJ, Lin CF, Ha DQ, Huong VTQ, My LT, Yeh TM, Huang JH, Liu CC, Halstead SB, , 2006. Volume replacement in infants with dengue hemorrhagic fever/dengue shock syndrome. Am J Trop Med Hyg 74: 684691.
  46. Shu PY, Chang SF, Kuo YC, Yueh YY, Chien LJ, Sue CL, Lin TH, Huang JH, , 2003. Development of group- and serotype-specific one-step SYBR green I real-time reverse transcription-PCR assay for dengue virus. J Clin Microbiol 41: 24082416.[Crossref]
  47. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, Bosse DC, Lawley TJ, , 1992. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 99: 683690.[Crossref]
  48. Galbraith S, Daniel JA, Vissel B, , 2010. A study of clustered data and approaches to its analysis. J Neurosci 30: 1060110608.[Crossref]
  49. Shu PY, Chen LK, Chang SF, Yueh YY, Chow L, Chien LJ, Chin C, Lin TH, Huang JH, , 2000. Dengue NS1-specific antibody responses: isotype distribution and serotyping in patients with dengue fever and dengue hemorrhagic fever. J Med Virol 62: 224232.[Crossref]
  50. Zandman-Goddard G, Shoenfeld Y, , 2002. HIV and autoimmunity. Autoimmun Rev 1: 329337.[Crossref]
  51. Wickham S, Carr DJ, , 2004. Molecular mimicry versus bystander activation: herpetic stromal keratitis. Autoimmunity 37: 393397.[Crossref]
  52. Lin YS, Lin CF, Fang YT, Kuo YM, Liao PC, Yeh TM, Hwa KY, Shieh CC, Yen JH, Wang HJ, Su IJ, Lei HY, , 2005. Antibody to severe acute respiratory syndrome (SARS)-associated coronavirus spike protein domain 2 cross-reacts with lung epithelial cells and causes cytotoxicity. Clin Exp Immunol 141: 500508.[Crossref]
  53. Molina V, Shoenfeld Y, , 2005. Infection, vaccines and other environmental triggers of autoimmunity. Autoimmunity 38: 235245.[Crossref]
  54. Maya R, Gershwin ME, Shoenfeld Y, , 2008. Hepatitis B virus (HBV) and autoimmune disease. Clin Rev Allergy Immunol 34: 85102.[Crossref]
  55. Buskila D, , 2009. Hepatitis C-associated rheumatic disorders. Rheum Dis Clin North Am 35: 111123.[Crossref]
  56. Pohl D, , 2009. Epstein-Barr virus and multiple sclerosis. J Neurol Sci 286: 6264.[Crossref]
  57. Varani S, Frascaroli G, Landini MP, Söderberg-Nauclér C, , 2009. Human cytomegalovirus targets different subsets of antigen-presenting cells with pathological consequences for host immunity: implications for immunosuppression, chronic inflammation and autoimmunity. Rev Med Virol 19: 131145.[Crossref]
  58. Zhao ZS, Granucci F, Yeh L, Schaffer PA, Cantor H, , 1998. Molecular mimicry by herpes simplex virus-type 1: autoimmune disease after viral infection. Science 279: 13441347.[Crossref]
  59. McClain MT, Heinlen LD, Dennis GJ, Roebuck J, Harley JB, James JA, , 2005. Early events in lupus humoral autoimmunity suggest initiation through molecular mimicry. Nat Med 11: 8589.[Crossref]
  60. Fujinami RS, von Herrath MG, Christen U, Whitton JL, , 2006. Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin Microbiol Rev 19: 8094.[Crossref]
  61. Kim B, Kaistha SD, Rouse BT, , 2006. Viruses and autoimmunity. Autoimmunity 39: 7177.[Crossref]
  62. Sfriso P, Ghirardello A, Botsios C, Tonon M, Zen M, Bassi N, Bassetto F, Doria A, , 2009. Infections and autoimmunity: the multifaceted relationship. J Leukoc Biol 87: 385395.[Crossref]
  63. 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 236: 515523.[Crossref]
  64. Saito M, Oishi K, Inoue S, Dimaano EM, Alera MT, Robles AM, Estrella BD, Jr Kumatori A, Moji K, Alonzo MT, Buerano CC, Matias RR, Morita K, Natividad FF, Nagatake T, , 2004. Association of increased platelet-associated immunoglobulins with thrombocytopenia and the severity of disease in secondary dengue virus infections. Clin Exp Immunol 138: 299303.[Crossref]
  65. 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: 17971803.[Crossref]
  66. Wan SW, Lin CF, Lu YT, Lei HY, Anderson R, Lin YS, , 2012. Endothelial cell surface expression of protein disulfide isomerase activates β1 and β3 integrins and facilitates dengue virus infection. J Cell Biochem 113: 16811691.
  67. Immenschuh S, Rahayu P, Bayat B, Saragih H, Rachman A, Santoso S, , 2013. Antibodies against dengue virus nonstructural protein-1 induce heme oxygenase-1 via a redox-dependent pathway in human endothelial cells. Free Radic Biol Med 54: 8592.[Crossref]
  68. Rothman AL, , 2011. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat Rev Immunol 11: 532543.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.14-0162
Loading
/content/journals/10.4269/ajtmh.14-0162
Loading

Data & Media loading...

Supplementary Data

Supplementary PDF

  • Received : 18 Mar 2014
  • Accepted : 05 Jan 2015

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error