Fusion of C3d molecule with neutralization epitope(s) of hepatitis E virus enhances antibody avidity maturation and neutralizing activity following DNA immunization

Virus Research

Volumn 151, Issue 2, 2010, Pages 162-169

  Yang, Shucai ^a   Wang, Chunling ^a   Fang, Xuefeng ^a   Zhai, Lijie ^a   Dong, Chen ^a   Ding, Lei ^a   Meng, Jihong ^a   Wang, Lixin ^a  

^a MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

Author keywords

C3d; Chinese epidemic strain; DNA vaccine; Hepatitis E virus (HEV); Neutralizing antibodies

Indexed keywords

DNA VACCINE; HEPATITIS E VACCINE; NEUTRALIZING ANTIBODY; P179 DNA VACCINE; TPA P179 C3D3 DNA VACCINE; TPA P179 DNA VACCINE; UNCLASSIFIED DRUG; COMPLEMENT COMPONENT C3D; EPITOPE; HEPATITIS VACCINE; RECOMBINANT VACCINE; TISSUE PLASMINOGEN ACTIVATOR; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DNA IMMUNIZATION; DRUG EFFECT; DRUG EFFICACY; FEMALE; HEPATITIS E VIRUS; IMMUNE RESPONSE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VIRUS NEUTRALIZATION; ANIMAL; ANTIBODY AFFINITY; BAGG ALBINO MOUSE; BLOOD; GENETICS; HEPATITIS E; HUMAN; IMMUNOLOGY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; COMPLEMENT C3D; EPITOPES; FEMALE; HEPATITIS E; HEPATITIS E VIRUS; HUMANS; MICE; MICE, INBRED BALB C; TISSUE PLASMINOGEN ACTIVATOR; VACCINES, DNA; VACCINES, SYNTHETIC; VIRAL HEPATITIS VACCINES;

HEPATITIS E VIRUS; MURINAE; MUS;

EID: 77954218133     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2010.04.011     Document Type: Article

References (66)

1. Aggarwal R., McCaustland K.A., Dilawari J.B., Sinha S.D., Robertson B.H. Genetic variability of hepatitis E virus within and between three epidemics in India. Virus Res. 1999, 59:35-48.
2. Aggarwal R., Nail S. Epidemiology of hepatitis E: current status. J. Gastroenterol. Hepatol. 2009, 24:1484-1493.
3. Amon J.J., Drobeniuc J., Bower W.A., Magaña J.C., Escobedo M.A., Williams I.T., Bell B.P., Armstrong G.L. Locally acquired hepatitis E virus infection, El Paso, Texas. J. Med. Virol. 2006, 78:741-746.
4. Aye T.T., Uchida T., Ma X.Z., Iida F., Shikata T., Zhuang H., Win K.M. Complete nucleotide sequence of a hepatitis E virus isolated from the Xinjiang epidemic (1986-1988) of China. Nucleic Acids Res. 1992, 20:3512.
5. Aye T.T., Uchida T., Ma X., Iida F., Shikata T., Zhuang H., Win K.M. Sequence comparison of the capsid region of hepatitis E viruses isolated from Myanmar and China. Microbiol. Immunol. 1992, 36:615-621.
6. Boccia D., Guthmann J.P., Klovstad H., Hamid N., Tatay M., Ciglenecki I., Nizou J.Y., Nicand E., Guerin P.J. High mortality associated with an outbreak of hepatitis E among displaced persons in Darfur, Sudan. Clin. Infect. Dis. 2006, 42:1679-1684.
7. Caron M., Enouf V., Than S.C., Dellamonica L., Buisson Y., Nicand E. Identification of genotype 1 hepatitis E virus in samples from swine in Cambodia. J. Med. Microbiol. 2006, 44:3440-3442.
8. Cooper K., Huang F., Batista L., Rayo C.D., Bezanilla J.C., Toth T.E., Meng X.J. Identification of genotype 3 hepatitis E virus (HEV) in serum and fecal samples from pigs in Thailand and Mexico, where genotype 1 and 2 HEV strains are prevalent in the respective human populations. J. Clin. Microbiol. 2005, 43:1684-1688.
9. Costa S.M., Paes M.V., Barreto D.F., Pinhão A.T., Barth O.M., Queiroz J.L., Armôa G.R., Freire M.S., Alves A.M. Protection against dengue type 2 virus induced in mice immunized with a DNA plasmid encoding the non-structural 1 (NS1) gene fused to the tissue plasminogen activator signal sequence. Vaccine 2006, 24:195-205.
10. Dempsey P.W., Allison M.E., Akkaraju S., Goodnow C.C., Fearon D.T. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 1996, 271:348-350.
11. Deshmukh T.M., Lole K.S., Tripathy A.S., Arankalle V.A. Immunogenicity of candidate hepatitis E virus DNA vaccine expressing complete and truncated ORF2 in mice. Vaccine 2007, 25:4350-4360.
12. Dong C., Meng J.H. Expression, purification and immunogenicity of a novel hepatitis E virus-like particle. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 2006, 22:339-342. (in Chinese).
13. Dong C., Dai X., Meng J.H. The first experimental study on a candidate combined vaccine against hepatitis A and hepatitis E. Vaccine 2007, 25:1662-1668.
14. Emerson S.U., Clemente-Casares P., Moiduddin N., Arankalle V.A., Torian U., Purcell R.H. Putative neutralization epitopes and broad cross-genotype neutralization of Hepatitis E virus confirmed by a quantitative cell-culture assay. J. Gen. Virol. 2006, 87:697-704.
15. Fang X.F., Wang L.X., Meng J.H., Dong C., Tian H., Zhai L.J. Effects of different vectors and gene fragments on antigen expression of hepatitis E virus DNA immunization. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 2006, 22:22-25. (in Chinese).
16. Green T.D., Newton B.P., Rota P.A., Xu Y., Robinson H.L., Ross T.M. C3d enhancement of neutralizing antibodies to measles hemagglutinin. Vaccine 2001, 20:242-248.
17. Green T.D., Montefiori D.C., Ross T.M. Enhancement of antibodies to the human immunodeficiency virus type 1 envelope by using the molecular adjuvant C3d. J. Virol. 2003, 77:2046-2055.
18. Haagsman A., Reuter G., Duizer E., Nagy G., Herremans T., Koopmans M., Szücs G. Seroepidemiology of hepatitis E virus in patients with non-A, non-B, non-C hepatitis in Hungary. J. Med. Virol. 2007, 79:927-930.
19. Huang C.C., Nguyen D., Fernandez J., Yun K.Y., Fry K.E., Bradley D.W., Tam A.W., Reyes G.R. Molecular cloning and sequencing of the Mexico isolate of hepatitis E virus (HEV). Virology 1992, 191:550-558.
20. Huang R., Nakazono N., Ishii K., Kawamata O., Kawaguchi R., Tsukada Y. Existing variations on the gene structure of hepatitis E virus strains from some regions of China. J. Med. Microbiol. 1995, 47:303-308.
21. Kamili S., Spelbring J., Krawczynski K. DNA vaccination against hepatitis E virus infection in cynomolgus macaques. J. Gastroenterol. Hepatol. 2002, 17(Suppl. 3):S365-S369.
22. Kamili S., Spelbring J., Carson D., Krawczynski K. Protective efficacy of hepatitis E virus DNA vaccine administered by gene gun in the cynomolgus macaque model of infection. J. Infect. Dis. 2004, 189:258-264.
23. Khuroo M.S., Kamili S. Aetiology, clinical course and outcome of sporadic acute viral hepatitis in pregnancy. J. Viral. Hepat. 2003, 10:61-69.
24. Khuroo M.S., Kamili S., Khuroo M.S. Clinical course and duration of viremia in vertically transmitted hepatitis E virus (HEV) infection in babies born to HEV-infected mothers. J. Viral. Hepat. 2009, 16:519-523.
25. Koizumi Y., Isoda N., Sato Y., Iwaki T., Ono K., Ido K., Sugano K., Takahashi M., Nishizawa T., Okamoto H. Infection of a Japanese patient by genotype 4 hepatitis e virus while traveling in Vietnam. J. Clin. Microbiol. 2004, 8:3883-3885.
26. Krawczynski K., Kamili S., Aggarwal R. Global epidemiology and medical aspects of hepatitis E. Forum (Genova) 2001, 11:166-179.
27. Lewis H.C., Boisson S., Ijaz S., Hewitt K., Ngui S.L., Boxall E., Teo C.G., Morgan D. Hepatitis E in England and Wales. Emerg. Infect. Dis. 2008, 14:165-167.
28. Li F., Loke P., Healy A., Lightowlers M.W., Gauci C.G., Purcell D.F., Anderson D.A. The effect of antigen targeting sequences on antibody responses to hepatitis E virus DNA vaccines in rats and sheep. Vaccine 2006, 24:1367-1377.
29. Li R.C., Ge S.X., Li Y.P., Zheng Y.J., Nong Y., Guo Q.S., Zhang J., Ng M.H., Xia N.S. Seroprevalence of hepatitis E virus infection, rural southern People's Republic of China. Emerg. Infect. Dis. 2006, 12:1682-1688.
30. Liang R., van den Hurk J.V., Zheng C., Yu H., Pontarollo R.A., Babiuk L.A., van Drunen Littel-van den Hurk S. Immunization with plasmid DNA encoding a truncated, secreted form of the bovine viral diarrhea virus E2 protein elicits strong humoral and cellular immune responses. Vaccine 2005, 23:5252-5262.
31. Liu Z., Chi B., Takahashi K., Mishiro S. A genotype IV hepatitis E virus strain that may be indigenous to Changchun, China. Intervirology 2003, 46:252-256.
32. Mansuy J.M., Peron J.M., Abravanel F., Poirson H., Dubois M., Miedouge M., Vischi F., Alric L., Vinel J.P., Izopet J. Hepatitis E in the south west of France in individuals who have never visited an endemic area. J. Med. Virol. 2004, 74:419-424.
33. Mansuy J.M., Legrand-Abravanel F., Calot J.P., Peron J.M., Alric L., Agudo S., Rech H., Destruel F., Izopet J. High prevalence of antihepatitis E virus antibodies in blood donors from South West France. J. Med. Virol. 2008, 80:289-293.
34. Meng J.H., Dubreuil P., Pillot J. A new PCR-based seroneutralization assay in cell culture for diagnosis of hepatitis E. J. Clin. Microbiol. 1997, 35:1373-1377.
35. Meng J.H., Pillot J., Dai X., Fields H.A., Khudyakov Y.E. Neutralization of different geographic strains of the hepatitis E virus with anti-hepatitis E virus positive serum samples obtained from different sources. Virology 1998, 249:316-324.
36. Meng J.H., Dai X., Chang, Joy C., Lopareva E., Pillot J., Fields H.A., Khudyakov Y.E. Identification and characterization of the neutralization epitope(s) of the hepatitis E virus. Virology 2001, 88:203-211.
37. Mitchell J.A., Green T.D., Bright R.A., Ross T.M. Induction of heterosubtypic immunity to influenza A virus using a DNA vaccine expressing hemagglutinin-C3d fusion proteins. Vaccine 2003, 21:902-914.
38. Mizuo H., Yazaki Y., Sugawara K., Tsuda F., Takahashi M., Nishizawa T., Okamoto H. Possible risk factors for the transmission of hepatitis E virus and for the severe form of hepatitis E acquired locally in Hokkaido, Japan. J. Med. Virol. 2005, 76:341-349.
39. Mkrtichyan M., Ghochikyan A., Movsesyan N., Karapetyan A., Begoyan G., Yu J., Glenn G.M., Ross T.M., Agadjanyan M.G., Cribbs D.H. Immunostimulant adjuvant patch enhances humoral and cellular immune responses to DNA immunization. DNA Cell Biol. 2008, 27:19-24.
40. Ning H., Niu Z., Yu R., Zhang P., Dong S., Li Z. Identification of genotype 3 hepatitis E virus in faecal samples from a pig farm located in a Shanghai suburb. Vet. Microbiol. 2007, 121:125-130.
41. Panda S.K., Thakral D., Rehman S. Hepatitis E virus. Rev. Med. Virol. 2007, 17:151-180.
42. Péron J.M., Bureau C., Poirson H., Mansuy J.M., Alric L., Selves J., Dupuis E., Izopet J., Vinel J.P. Fulminant liver failure from acute autochthonous hepatitis E in France: description of seven patients with acute hepatitis E and encephalopathy. J. Viral. Hepat. 2007, 14:298-303.
43. Renoux V.M., Fleury M.J., Bousarghin L., Gaitan J., Sizaret P.Y., Touzé A., Coursaget P. Induction of antibody response against hepatitis E virus (HEV) with recombinant human papillomavirus pseudoviruses expressing truncated HEV capsid proteins in mice. Vaccine 1998, 26:6602-6607.
44. Richmond J.F., Lu S., Santoro J.C., Weng J., Hu S.L., Montefiori D.C., Robinson H.L. Studies of the neutralizing activity and avidity of anti-human immunodeficiency virus type 1 Env antibody elicited by DNA priming and protein boosting. J. Virol. 1998, 72:9092-9100.
45. Ross T.M., Xu Y., Bright R.A., Robinson H.L. C3d enhancement of antibodies to hemagglutinin accelerates protection against influenza virus challenge. Nat. Immunol. 2000, 1:127-131.
46. Ross T.M., Xu Y., Green T.D., Montefiori D.C., Robinson H.L. Enhanced avidity maturation of antibody to human immunodeficiency virus envelope: DNA vaccination with gp120-C3d fusion proteins. AIDS. Res. Hum. Retroviruses 2001, 17:829-835.
47. Sadler G.J., Mells G.F., Shah N.H., Chesner I.M., Walt R.P. UK acquired hepatitis E-an emerging problem?. J. Med. Virol. 2006, 78:473-475.
48. Said B., Ijaz S., Kafatos G., Booth L., Thomas H.L., Walsh A., Ramsay M., Morgan D. Hepatitis E outbreak on cruise ship. Emerg. Infect. Dis. 2009, 11:1738-1744.
49. Schlauder G.G., Mushahwar I.K. Genetic heterogeneity of hepatitis E virus. J. Med. Virol. 2001, 65:282-292.
50. Simmons M., Porter K.R., Hayes C.G., Vaughn D.W., Putnak R. Characterization of antibody responses to combinations of a dengue virus type 2 DNA vaccine and two dengue virus type 2 protein vaccines in rhesus macaques. J. Virol. 2006, 80:9577-9585.
51. Skidmore S. Overview of hepatitis E virus. Curr. Infect. Dis. Rep. 2002, 4:118-123.
52. Takahashi M., Nishizawa T., Okamoto H. Identification of a genotype III swine hepatitis E virus that was isolated from a Japanese pig born in 1990 and that is most closely related to Japanese isolates of human hepatitis E virus. J. Clin. Microbiol. 2003, 41:1342-1343.
53. Tanaka T., Takahashi M., Kusano E., Okamoto H. Development and evaluation of an efficient cell-culture system for hepatitis E virus. J. Gen. Virol. 2007, 88:903-911.
54. Tsarev S.A., Tsareva T.S., Emerson S.U., Govindarajan S., Shapiro M., Gerin J.L., Purcell R.H. Recombinant vaccine against hepatitis E: dose response and protection against heterologous challenge. Vaccine 1997, 15:1834-1838.
55. Wang L.X., Xu W., Guan Q.D., Chu Y.W., Wang Y., Xiong S.D. Contribution of C3d-P28 repeats to enhancement of immune responses against HBV-preS2/S induced by gene immunization. World J. Gastroenterol. 2004, 10:2072-2077.
56. Wang L., Zhuang H. Hepatitis E: an overview and recent advances in vaccine research. World J. Gastroenterol. 2004, 10:2157-2162.
57. Wang S., Heilman D., Liu F., Giehl T., Joshi S., Huang X., Chou T.H., Goguen J., Lu S. A DNA vaccine producing LcrV antigen in oligomers is effective in protecting mice from lethal mucosal challenge of plague. Vaccine 2004, 22:3348-3357.
58. Wang X.L., Li D.J., Yuan M.M., Yu M., Yao X.Y. Enhancement of humoral immunity to the hCG beta protein antigen by fusing a molecular adjuvant C3d3. J. Reprod. Immunol. 2004, 63:97-110.
59. Wang Y., Zhang H., Li Z., Gu W., Lan H., Hao W., Ling R., Li H., Harrison T.J. Detection of sporadic cases of hepatitis E virus (HEV) infection in China using immunoassays based on recombinant open reading frame 2 and 3 polypeptides from HEV genotype 4. J. Clin. Microbiol. 2001, 39:4370-4379.
60. Watanabe I., Ross T.M., Tamura S., Ichinohe T., Ito S., Takahashi H., Sawa H., Chiba J., Kurata T., Sata T., Hasegawa H. Protection against influenza virus infection by intranasal administration of C3d-fused hemagglutinin. Vaccine 2003, 21:4532-4538.
61. Yan Y., Zhang W., Shen Q., Cui L., Hua X.G. Prevalence of four different subgenotypes of genotype 4 hepatitis E virus among swine in the Shanghai area of China. Acta Vet. Scand. 2008, 50:12-19.
62. Zhai L.J., Dai X., Meng J.H. Hepatitis E virus genotyping based on full-length genome and partial genomic regions. Virus Res. 2006, 120:57-69.
63. Zhang M., Emerson S.U., Nguyen H., Engle R., Govindarajan S., Blackwelder W.C., Gerin J., Purcell R.H. Recombinant vaccine against hepatitis E: duration of protective immunity in rhesus macaques. Vaccine 2002, 20:3285-3291.
64. Zhou E.M., Guo H., Huang F.F., Sun Z.F., Meng X.J. Identification of two neutralization epitopes on the capsid protein of avian hepatitis E virus. J. Gen. Virol. 2008, 89:500-508.
65. Zhou Y., Purcell R.H., Emerson S.U. A truncated ORF2 protein contains the most immunogenic site on ORF2: antibody responses to non-vaccine sequences following challenge of vaccinated and non-vaccinated macaques with hepatitis E virus. Vaccine 2005, 23:3157-3165.
66. Zhuang H., Cao X.Y., Liu C.B., Wang G.M. Epidemiology of hepatitis E in China. Gastroenterol. Jpn. 1991, 26(Suppl.):135-138.