Protection against dengue virus infection in mice by administration of antibodies against modified nonstructural protein 1

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Wan, Shu Wen ^a,b   Lu, Yi Tien ^b   Huang, Chia Hui ^b   Lin, Chiou Feng ^a,b   Anderson, Robert ^c   Liu, Hsiao Sheng ^a,b   Yeh, Trai Ming ^a,b   Yen, Yu Ting ^d   Wu Hsieh, Betty A ^a   Lin, Yee Shin ^a,b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c DALHOUSIE UNIVERSITY   (Canada)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; DELTAC NSI ANTIBODY; DENV NS1 ANTIBODY; DJ NS1 ANTIBODY; NONSTRUCTURAL PROTEIN 1; PROTEIN ANTIBODY; UNCLASSIFIED DRUG; VIRUS ANTIBODY; NS1 PROTEIN, DENGUE VIRUS TYPE 2; PEPTIDE FRAGMENT; VIRUS PROTEIN;

ACTIVE IMMUNIZATION; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; BLEEDING TIME; CARBOXY TERMINAL SEQUENCE; CELL INFILTRATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; CROSS REACTION; DENGUE; DENGUE VIRUS; DISEASE MODEL; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INOCULATION; JAPANESE ENCEPHALITIS VIRUS; MACROPHAGE INFILTRATION; MACROPHAGE MIGRATION INHIBITION; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PROTEIN STRUCTURE; SKIN BLEEDING; THROMBOCYTE; VACCINATION; VIRUS INHIBITION; VIRUS LOAD; VIRUS REPLICATION; ANIMAL; C3H MOUSE; DRUG EFFECTS; HEMORRHAGE; IMMUNOLOGY;

ANIMALS; ANTIBODIES, VIRAL; BLOOD PLATELETS; CROSS REACTIONS; DENGUE; DENGUE VIRUS; HEMORRHAGE; HUMANS; MICE, INBRED C3H; PEPTIDE FRAGMENTS; VACCINATION; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84899123513     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092495     Document Type: Article

References (56)

1. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, et al. (2010) Dengue: a continuing global threat. Nat Rev Microbiol 8: S7-S16.
2. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, et al. (2013) The global distrubution and burden of dengue. Nature 496: 504-507.
3. Simmons CP, Farrar JJ, Nguyen vV, Wills B (2012) Dengue. N Engl J Med 366: 1423-1432.
4. Halstead SB (2007) Dengue. Lancet 370: 1644-1652.
5. Yauch LE, Shresta S (2008) Mouse models of dengue virus infection and disease. Antiviral Res 80: 87-93.
6. Chen HC, Hofman FM, Kung JT, Lin YD, Wu-Hsieh BA (2007) Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage. J Virol 81: 5518-5526. (Pubitemid 46846992)
7. 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: 12312-12324.
8. Wu-Hsieh BA, Yen YT, Chen HC (2009) Dengue hemorrhage in a mouse model. Ann N Y Acad Sci 1171 Suppl 1: E42-E47.
9. Halstead SB (1998) Pathogenesis of dengue: challenges to molecular biology. Science 239: 476-481.
10. Morens DM (1994) Antibody-dependent enhancement of infection and the pathogenesis of viral disease. Clin Infect Dis 19: 500-512.
11. Halstead SB (2002) Dengue. Curr Opin Infect Dis 15: 471-476.
12. Halstead SB (2003) Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 60: 421-467.
13. Huang KJ, Yang YC, Lin YS, Huang JH, Liu HS, et al. (2006) The dual-specific binding of dengue virus and target cells for the antibody-dependent enhancement of dengue virus infection. J Immunol 176: 2825-2832.
14. 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: 9422-9427. (Pubitemid 47185795)
15. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL, et al. (2010) Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6: e1000790.
16. Schlesinger JJ, Brandriss MW, Walsh EE (1987) Protection of mice against dengue 2 virus encephalitis by immunization with the dengue 2 virus nonstructural glycoprotein NS1. J Gen Virol 68 (Pt 3): 853-857. (Pubitemid 17021460)
17. Amorim JH, Diniz MO, Cariri FA, Rodrigues JF, Bizerra RS, et al. (2012) Protective immunity to DENV2 after immunization with a recombinant NS1 protein using a genetically detoxified heat-labile toxin as an adjuvant. Vaccine 30: 837-845.
18. Henchal EA, Henchal LS, Schlesinger JJ (1998) Synergistic interactions of anti-NS1 monoclonal antibodies protect passively immunized mice from lethal challenge with dengue 2 virus. J Gen Virol 69 (Pt 8): 2101-2107.
19. Wu SF, Liao C L, Lin YL, Yeh CT, Chen LK, et al. (2003) Evaluation of protective efficacy and immune mechanisms of using a non-structural protein NS1 in DNA vaccine against dengue 2 virus in mice. Vaccine 21: 3919-3929.
20. Costa SM, Azevedo AS, Paes MV, Sarges FS, Freire MS, et al. (2007) DNA vaccines against dengue virus based on the ns1 gene: the influence of different signal sequences on the protein expression and its correlation to the immune response elicited in mice. Virology 358: 413-423. (Pubitemid 46138117)
21. 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.
22. 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: 493-504.
23. 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.
24. Lin YS, Yeh TM, Lin CF, Wan SW, Chuang YC, et al. (2011) Molecular mimicry between virus and host and its implications for dengue disease pathogenesis. Exp Biol Med 236: 515-523.
25. Lin CF, Lei HY, Liu CC, Liu HS, Yeh TM, et al. (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: 69-75.
26. Lin CF, Lei HY, Shiau AL, Liu HS, Yeh TM, 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.
27. Lin CF, Chiu SC, Hsiao YL, Wan SW, Lei HY, et al. (2005) Expression of cytokine, chemokine, and adhesion molecules during endothelial cell activation induced by antibodies against dengue virus nonstructural protein 1. J Immunol 174: 395-403.
28. Cheng HJ, Lin CF, Lei HY, Liu HS, Yeh TM, et al. (2009) Proteomic analysis of endothelial cell autoantigens recognized by anti-dengue virus nonstructural protein 1 antibodies. Exp Biol Med 234: 63-73.
29. Chen MC, Lin CF, Lei HY, Lin SC, Liu HS, et al. (2009) Deletion of the Cterminal region of dengue virus nonstructural protein 1 (NS1) abolishes anti- NS1-mediated platelet dysfunction and bleeding tendency. J. Immunol 183: 1797-1803.
30. Séverin S, Gratacap MP, Lenain N, Alvarez L, Hollande E, et al. (2007) Deficiency of Src homology 2 domain-containing inositol 5-phosphatase 1 affects platelet responses and thrombus growth. J Clin Invest 117: 944-952. (Pubitemid 46556750)
31. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, et al. (1992) HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 99: 683-690. (Pubitemid 23002027)
32. Huang KJ, Li SY, Chen SC, Liu HS, Lin YS, et al. (2000) Manifestation of thrombocytopenia in dengue-2-virus-infected mice. J Gen Virol 81: 2177-2182.
33. Wan SW, Lin CF, Chen MC, Lei HY, Liu HS, et al. (2008) C-terminal region of dengue virus nonstructural protein 1 is involved in endothelial cell crossreactivity via molecular mimicry. Am J Infect Dis 4: 85-91.
34. 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.
35. Schlesinger JJ, Brandriss MW, Walsh EE (1985) Protection against 17D yellow fever encephalitis in mice by passive transfer of monoclonal antibodies to the nonstructural glycoprotein gp48 and by active immunization with gp48. J Immunol 135: 2805-2809. (Pubitemid 16217156)
36. Lin YL, Chen LK, Liao CL, Yeh CT, Ma SH, et al. (1998) DNA immunization with Japanese encephalitis virus nonstructural protein NS1 elicits protective immunity in mice. J Virol 72: 191-200.
37. Krishna VD, Rangappa M, Satchidanandam V (2009) Virus-specific cytolytic antibodies to nonstructural protein 1 of Japanese encephalitis virus effect reduction of virus output from infected cells. J Virol 83: 4766-4777.
38. Kitai Y, Kondo T, Konishi E (2010) Complement-dependent cytotoxicity assay for differentiating West Nile virus from Japanese encephalitis virus infections in horses. Clin Vaccine Immunol 17: 875-878.
39. Anderson R, Wang S, Osiowy C, Issekutz AC (1997) Activation of endothelial cells via antibody-enhanced dengue virus infection of peripheral blood monocytes. J Virol 71: 4226-4232. (Pubitemid 27204108)
40. Schlesinger JJ, Foltzer M, Chapman S (1993) The Fc portion of antibody to yellow fever virus NS1 is a determinant of protection against YF encephalitis in mice. Virology 192: 132-141.
41. Lin CW, Liu KT, Huang HD, Chen WJ (2008) Protective immunity of E. coli-synthesized NS1 protein of Japanese encephalitis virus. Biotechnol Lett 30: 205-214.
42. Chung KM, Nybakken GE, Thompson BS, Engle MJ, Marri A, et al. (2006) Antibodies against West Nile Virus nonstructural protein NS1 prevent lethal infection through Fc gamma receptor-dependent and -independent mechanisms. J Virol 80: 1340-1351. (Pubitemid 43134091)
43. Diamond MS, Pierson TC, Fremont DH (2008) The structural immunology of antibody protection against West Nile virus. Immunol Rev 225: 212-225.
44. Falgout B, Bray M, Schlesinger JJ, Lai CJ (1990) Immunization of mice with recombinant vaccinia virus expressing authentic dengue virus nonstructural protein NS1 protects against lethal dengue virus encephalitis. J Virol 64: 4356-4363. (Pubitemid 20279846)
45. Chung KM, Thompson BS, Fremont DH, Diamond MS (2007) Antibody recognition of cell surface-associated NS1 triggers Fc-gamma receptor-mediated phagocytosis and clearance of West Nile Virus-infected cells. J Virol 81: 9551-9555. (Pubitemid 47311499)
46. Cheng HJ, Lei HY, Lin CF, Luo YH, Wan SW, 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.
47. Heinz FX, Stiasny K (2012) Flaviviruses and flavivirus vaccines. Vaccine 30: 4301-4306.
48. Swaminathan S, Batra G, Khanna N (2010) Dengue vaccines: state of the art. Expert Opin Ther Pat 20: 819-835.
49. Coller BA, Clements DE (2011) Dengue vaccines: progress and challenges. Curr Opin Immunol 23: 391-398.
50. Murrell S, Wu SC, Butler M (2011) Review of dengue virus and the development of a vaccine. Biotechnol Adv 29: 239-247.
51. Thomas SJ, Endy TP (2011) Critical issues in dengue vaccine development. Curr Opin Infect Dis 24: 442-450.
52. Perng GC, Lei HY, Lin YS, Chokephaibulkit K (2011) Dengue vaccines: challenge and confrontation. World J Vaccines 1: 109-130.
53. Sabchareon A, Wallace D, Sirivichayakul C, Limkittikul K, Chanthavanich P, et al. (2012) Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380: 1559-1567.
54. Teoh EP, Kukkaro P, Teo EW, Lim APC, Tan TT, et al. (2012) The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci Transl Med 4: 139ra83.
55. Li PC, Liao MY, Cheng PC, Liang JJ, Liu IJ, et al. (2012) Development of a humanized antibody with high therapeutic potential against dengue virus type 2. PLoS Negl Trop Dis 6: e1636.
56. Henriques HR, Rampazo EV, Gonçalves AJS, Vicentin ECM, Amorim JH, et al. (2013) Targeting the non-structural protein 1 from dengue virus to a dendritic cell population confers protective immunity to lethal virus challenge. PLoS Negl Trop Dis 7: e2330.