A VLP Library of C-Terminally Truncated Hepatitis B Core Proteins: Correlation of RNA Encapsidation with a Th1/Th2 Switch in the Immune Responses of Mice

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Sominskaya, Irina ^a   Skrastina, Dace ^a   Petrovskis, Ivars ^a   Dishlers, Andris ^a   Berza, Ieva ^a   Mihailova, Maria ^a   Jansons, Juris ^a   Akopjana, Inara ^a   Stahovska, Irina ^a   Dreilina, Dzidra ^a   Ose, Velta ^a   Pumpens, Paul ^a  

^a LATVIAN BIOMEDICAL RESEARCH AND STUDY CENTRE   (Latvia)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; HEPATITIS B CORE ANTIBODY; MONOCLONAL ANTIBODY; NUCLEIC ACID; VIRUS RNA;

ANIMAL CELL; ANTIGENICITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA LIBRARY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETIC VARIABILITY; HBC GENE; IMMUNE RESPONSE; IMMUNOGENICITY; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PROMOTER REGION; RNA BINDING; RNA ENCAPSIDATION; RNA STRUCTURE; TH1 CELL; TH2 CELL; VIRUS GENE; VIRUS LIKE AGENT;

ANIMALS; CHROMATOGRAPHY, GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; GENE LIBRARY; GENETIC ENGINEERING; HEPATITIS B CORE ANTIGENS; MICE; MICE, INBRED BALB C; MICROSCOPY, ELECTRON; PROTEIN BINDING; RNA-BINDING PROTEINS; VIRION;

EID: 84884527479     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075938     Document Type: Article

References (55)

1. Pushko P, Pumpens P, Grens E,; Pushko P, Pumpens P, Grens E, (2013) Development of virus-like particle technology from small highly symmetric to large complex virus-like particle structures. Intervirology 56: 141-165. doi:10.1159/000346773. PubMed: 23594863. PII]:000346773; [doi]: 10.1159/000346773. PubMed: 23594863. doi:10.1159/000346773. PubMed: 23594863.
2. Zeltins A, (2013) Construction and characterization of virus-like particles: a review. Mol Biotechnol 53: 92-107. doi:10.1007/s12033-012-9598-4. PubMed: 23001867. doi:10.1007/s12033-012-9598-4. PubMed: 23001867.
3. Cardinale D, Carette N, Michon T,; Cardinale D, Carette N, Michon T, (2012) Virus scaffolds as enzyme nano-carriers. Trends Biotechnol 30: 369-376. doi:10.1016/j.tibtech.2012.04.001. PubMed: 22560649. PII]:S0167-7799(12)00050-9; [doi]: 10.1016/j.tibtech.2012.04.001. PubMed: 22560649. doi:10.1016/j.tibtech.2012.04.001. PubMed: 22560649.
4. Whitacre DC, Lee BO, Milich DR, (2009) Use of hepadnavirus core proteins as vaccine platforms. Expert Rev Vaccines 8: 1565-1573. doi:10.1586/erv.09.121. PubMed: 19863249. doi:10.1586/erv.09.121. PubMed: 19863249.
5. Borisova GP, Pumpen PP, Bychko VV, Pushko PM, Kalis IaV, (1984) [Structure and expression in Escherichia coli cells of the core antigen gene of the human hepatitis B virus (HBV)]. Dokl Akad Nauk SSSR 279: 1245-1249. PubMed: 6394254.
6. Edman JC, Hallewell RA, Valenzuela P, Goodman HM, Rutter WJ, (1981) Synthesis of hepatitis B surface and core antigens in E. coli. Nature 291: 503-506. doi:10.1038/291503a0. PubMed: 6262658.
7. Nassal M, (1988) Total chemical synthesis of a gene for hepatitis B virus core protein and its functional characterization. Gene 66: 279-294. doi:10.1016/0378-1119(88)90364-2. PubMed: 2901997.
8. Pasek M, Goto T, Gilbert W, Zink B, Schaller H, et al. (1979) Hepatitis B virus genes and their expression in E. coli. Nature 282: 575-579. doi:10.1038/282575a0. PubMed: 399329.
9. Kniskern PJ, Hagopian A, Montgomery DL, Burke P, Dunn NR, et al. (1986) Unusually high-level expression of a foreign gene (hepatitis B virus core antigen) in Saccharomyces cerevisiae. Gene 46: 135-141. doi:10.1016/0378-1119(86)90177-0. PubMed: 3542716.
10. Miyanohara A, Imamura T, Araki M, Sugawara K, Ohtomo N, et al. (1986) Expression of hepatitis B virus core antigen gene in Saccharomyces cerevisiae: synthesis of two polypeptides translated from different initiation codons. J Virol 59: 176-180. PubMed: 3520012.
11. Freivalds J, Dislers A, Ose V, Pumpens P, Tars K, et al.; Freivalds J, Dislers A, Ose V, Pumpens P, Tars K, Kazaks A, (2011) Highly efficient production of phosphorylated hepatitis B core particles in yeast Pichia pastoris. Protein Expr Purif 75: 218-224. doi:10.1016/j.pep.2010.09.010. PubMed: 20854910. PII]:S1046-5928(10)00258-5; [doi]: 10.1016/j.pep.2010.09.010. PubMed: 20854910. doi:10.1016/j.pep.2010.09.010. PubMed: 20854910.
12. Rolland D, Gauthier M, Dugua JM, Fournier C, Delpech L, et al. (2001) Purification of recombinant HBc antigen expressed in Escherichia coli and Pichia pastoris: comparison of size-exclusion chromatography and ultracentrifugation. J Chromatogr B Biomed Sci Appl 753: 51-65. doi:10.1016/S0378-4347(00)00538-7. PubMed: 11302448.
13. Mechtcheriakova IA, Eldarov MA, Nicholson L, Shanks M, Skryabin KG, et al.; Mechtcheriakova IA, Eldarov MA, Nicholson L, Shanks M, Skryabin KG, Lomonossoff GP, (2006) The use of viral vectors to produce hepatitis B virus core particles in plants. J Virol Methods 131: 10-15. doi:10.1016/j.jviromet.2005.06.020. PubMed: 16112207. PII]:S0166-0934(05)00217-X; [doi]: 10.1016/j.jviromet.2005.06.020. PubMed: 16112207. doi:10.1016/j.jviromet.2005.06.020. PubMed: 16112207.
14. Tsuda S, Yoshioka K, Tanaka T, Iwata A, Yoshikawa A, et al. (1998) Application of the human hepatitis B virus core antigen from transgenic tobacco plants for serological diagnosis. Vox Sang 74: 148-155. doi:10.1046/j.1423-0410.1998.7430148.x. PubMed: 9595641. PII]:vox74148. PubMed: 9595641.
15. Hilditch CM, Rogers LJ, Bishop DH, (1990) Physicochemical analysis of the hepatitis B virus core antigen produced by a baculovirus expression vector. J Gen Virol 71(11):: 2755-2759. doi:10.1099/0022-1317-71-11-2755. PubMed: 2254755.
16. Lanford RE, Notvall L, (1990) Expression of hepatitis B virus core and precore antigens in insect cells and characterization of a core-associated kinase activity. Virology 176: 222-233. doi:10.1016/0042-6822(90)90247-O. PubMed: 2158690.
17. Takehara K, Ireland D, Bishop DH, (1988) Co-expression of the hepatitis B surface and core antigens using baculovirus multiple expression vectors. J Gen Virol 69(11):: 2763-2777. doi:10.1099/0022-1317-69-11-2763. PubMed: 3053987.
18. Zhou S, Standring DN, (1992) Hepatitis B virus capsid particles are assembled from core-protein dimer precursors. Proc Natl Acad Sci U S A 89: 10046-10050. doi:10.1073/pnas.89.21.10046. PubMed: 1438193.
19. Crowther RA, Kiselev NA, Böttcher B, Berriman JA, Borisova GP, et al. (1994) Three-dimensional structure of hepatitis B virus core particles determined by electron cryomicroscopy. Cell 77: 943-950. doi:10.1016/0092-8674(94)90142-2. PubMed: 8004680.
20. Roseman AM, Borschukova O, Berriman JA, Wynne SA, Pumpens P, et al.; Roseman AM, Borschukova O, Berriman JA, Wynne SA, Pumpens P, Crowther RA, (2012) Structures of hepatitis B virus cores presenting a model epitope and their complexes with antibodies. J Mol Biol 423: 63-78. doi:10.1016/j.jmb.2012.06.032. PubMed: 22750730. PII]:S0022-2836(12)00524-4; [doi]: 10.1016/j.jmb.2012.06.032. PubMed: 22750730. doi:10.1016/j.jmb.2012.06.032. PubMed: 22750730.
21. Wynne SA, Crowther RA, Leslie AG, (1999) The crystal structure of the human hepatitis B virus capsid. Mol Cell 3: 771-780. [pii]: S1097-2765(01)80009-5 doi:10.1016/S1097-2765(01)80009-5. PubMed: 10394365.
22. Kenney JM, von Bonsdorff CH, Nassal M, Fuller SD, (1995) Evolutionary conservation in the hepatitis B virus core structure: comparison of human and duck cores. Structure 3: 1009-1019. doi:10.1016/S0969-2126(01)00237-4. PubMed: 8589996.
23. Roseman AM, Berriman JA, Wynne SA, Butler PJ, Crowther RA,; Roseman AM, Berriman JA, Wynne SA, Butler PJ, Crowther RA, (2005) A structural model for maturation of the hepatitis B virus core. Proc Natl Acad Sci U S A 102: 15821-15826. doi:10.1073/pnas.0504874102. PubMed: 16247012. PII]:0504874102; [doi]: 10.1073/pnas.0504874102. PubMed: 16247012. doi:10.1073/pnas.0504874102. PubMed: 16247012.
24. Birnbaum F, Nassal M, (1990) Hepatitis B virus nucleocapsid assembly: primary structure requirements in the core protein. J Virol 64: 3319-3330. PubMed: 2191149.
25. Nassal M, (1992) The arginine-rich domain of the hepatitis B virus core protein is required for pregenome encapsidation and productive viral positive-strand DNA synthesis but not for virus assembly. J Virol 66: 4107-4116. PubMed: 1602535.
26. Machida A, Ohnuma H, Tsuda F, Yoshikawa A, Hoshi Y, et al. (1991) Phosphorylation in the carboxyl-terminal domain of the capsid protein of hepatitis B virus: evaluation with a monoclonal antibody. J Virol 65: 6024-6030. PubMed: 1717713.
27. Kann M, Sodeik B, Vlachou A, Gerlich WH, Helenius A, (1999) Phosphorylation-dependent binding of hepatitis B virus core particles to the nuclear pore complex. J Cell Biol 145: 45-55. doi:10.1083/jcb.145.1.45. PubMed: 10189367.
28. Weigand K, Knaust A, Schaller H,; Weigand K, Knaust A, Schaller H, (2010) Assembly and export determine the intracellular distribution of hepatitis B virus core protein subunits. J Gen Virol 91: 59-67. doi:10.1099/vir.0.013698-0. PubMed: 19741067. PII]:vir.0.013698-0;[doi]: 10.1099/vir.0.013698-0. PubMed: 19741067. doi:10.1099/vir.0.013698-0. PubMed: 19741067.
29. Hatton T, Zhou S, Standring DN, (1992) RNA- and DNA-binding activities in hepatitis B virus capsid protein: a model for their roles in viral replication. J Virol 66: 5232-5241. PubMed: 1501273.
30. Borisova GP, Kalis IaV, Pushko PM, Tsibinogin VV, Loseva VIa, (1988) [Genetically engineered mutants of the core antigen of the human hepatitis B virus preserving the ability for native self-assembly]. Dokl Akad Nauk SSSR 298: 1474-1478. PubMed: 2837379.
31. Gallina A, Bonelli F, Zentilin L, Rindi G, Muttini M, et al. (1989) A recombinant hepatitis B core antigen polypeptide with the protamine-like domain deleted self-assembles into capsid particles but fails to bind nucleic acids. J Virol 63: 4645-4652. PubMed: 2677399.
32. Beames B, Lanford RE, (1993) Carboxy-terminal truncations of the HBV core protein affect capsid formation and the apparent size of encapsidated HBV RNA. Virology 194: 597-607. [pii]: S0042-6822(83)71299-7 doi:10.1006/viro.1993.1299. PubMed: 7684872. doi:10.1006/viro.1993.1299. PubMed: 7684872.
33. Wingfield PT, Stahl SJ, Williams RW, Steven AC, (1995) Hepatitis core antigen produced in Escherichia coli: subunit composition, conformational analysis, and in vitro capsid assembly. Biochemistry 34: 4919-4932. doi:10.1021/bi00015a003. PubMed: 7711014.
34. Zlotnick A, Cheng N, Conway JF, Booy FP, Steven AC, et al.; Zlotnick A, Cheng N, Conway JF, Booy FP, Steven AC, Stahl SJ, Wingfield PT, (1996) Dimorphism of hepatitis B virus capsids is strongly influenced by the C-terminus of the capsid protein. Biochemistry 35: 7412-7421. doi:10.1021/bi9604800. PubMed: 8652518. PII]:bi9604800; [doi]: 10.1021/bi9604800. PubMed: 8652518. doi:10.1021/bi9604800. PubMed: 8652518.
35. Riedl P, Buschle M, Reimann J, Schirmbeck R, (2002) Binding immune-stimulating oligonucleotides to cationic peptides from viral core antigen enhances their potency as adjuvants. Eur J Immunol 32: 1709-1716. doi:10.1002/1521-4141(200206)32:6. PubMed: 12115654. doi:10.1002/1521-4141(200206)32:6<1709::AID-IMMU1709>3.0.CO;2-D. PubMed: 12115654.
36. Riedl P, Stober D, Oehninger C, Melber K, Reimann J, et al. (2002) Priming Th1 immunity to viral core particles is facilitated by trace amounts of RNA bound to its arginine-rich domain. J Immunol 168: 4951-4959. PubMed: 11994446.
37. Machida A, Ohnuma H, Takai E, Tsuda F, Tanaka T, et al. (1989) Antigenic sites on the arginine-rich carboxyl-terminal domain of the capsid protein of hepatitis B virus distinct from hepatitis B core or e antigen. Mol Immunol 26: 413-421. doi:10.1016/0161-5890(89)90130-2. PubMed: 2469950.
38. Bundule MA, Bychko VV, Saulitis IuB, Liepin'sh EE, Borisova GP, et al. (1990) [C-terminal polyarginine tract of hepatitis B core antigen is located on the outer capsid surface]. Dokl Akad Nauk SSSR 312: 993-996. PubMed: 2226141.
39. Vanlandschoot P, Van Houtte F, Serruys B, Leroux-Roels G,; Vanlandschoot P, Van Houtte F, Serruys B, Leroux-Roels G, (2005) The arginine-rich carboxy-terminal domain of the hepatitis B virus core protein mediates attachment of nucleocapsids to cell-surface-expressed heparan sulfate. J Gen Virol 86: 75-84. PubMed: 15604433: [pii]:75-84. 86/1/75; [doi]: 10.1099/vir.0.80580-0. PubMed: 15604433. PubMed: 15604433.
40. Seifer M, Standring DN, (1994) A protease-sensitive hinge linking the two domains of the hepatitis B virus core protein is exposed on the viral capsid surface. J Virol 68: 5548-5555. PubMed: 7520091.
41. Watts NR, Conway JF, Cheng N, Stahl SJ, Belnap DM, et al. (2002) The morphogenic linker peptide of HBV capsid protein forms a mobile array on the interior surface. EMBO J 21: 876-884. doi:10.1093/emboj/21.5.876. PubMed: 11867516. doi:10.1093/emboj/21.5.876. PubMed: 11867516.
42. Dislers A, Sominska I, Kazaks A, Petrovskis I, Zarina I, inventors; (2008) Expression system for producing recombinant virus-like particles. Latvian patent LV 13587 (B) of 20 (08-02-20). International classification IPC1-7:A61K39/29; C12N15/71.
43. Bichko V, Pushko P, Dreilina D, Pumpen P, Gren E, (1985) Subtype ayw variant of hepatitis B virus. DNA primary structure analysis. FEBS Lett 185: 208-212. doi:10.1016/0014-5793(85)80771-7. PubMed: 3996597.
44. Bichko V, Schödel F, Nassal M, Gren E, Berzinsh I, et al. (1993) Epitopes recognized by antibodies to denatured core protein of hepatitis B virus. Mol Immunol 30: 221-231. doi:10.1016/0161-5890(93)90051-C. PubMed: 7679466.
45. Ouchterlony O, (1949) Antigen-antibody reactions in gels. Acta Pathol Microbiol Scand 26: 507-515. PubMed: 18143039.
46. Pushko P, Sallberg M, Borisova G, Ruden U, Bichko V, et al. (1994) Identification of hepatitis B virus core protein regions exposed or internalized at the surface of HBcAg particles by scanning with monoclonal antibodies. Virology 202: 912-920. doi:10.1006/viro.1994.1413. PubMed: 8030252. PII]:S0042-6822(84)71413-9; [doi]: 10.1006/viro. 1994(1413). PubMed: 8030252.
47. Sominskaya I, Skrastina D, Dislers A, Vasiljev D, Mihailova M, et al.; Sominskaya I, Skrastina D, Dislers A, Vasiljev D, Mihailova M, Ose V, Dreilina D, Pumpens P, (2010) Construction and immunological evaluation of multivalent hepatitis B virus (HBV) core virus-like particles carrying HBV and HCV epitopes. Clin Vaccine Immunol 17: 1027-1033. doi:10.1128/CVI.00468-09. PubMed: 20410327. PII]:CVI.00468-09; [doi]: 10.1128/CVI.00468-09. PubMed: 20410327. doi:10.1128/CVI.00468-09. PubMed: 20410327.
48. Milich DR, Peterson DL, Schödel F, Jones JE, Hughes JL, (1995) Preferential recognition of hepatitis B nucleocapsid antigens by Th1 or Th2 cells is epitope and major histocompatibility complex dependent. J Virol 69: 2776-2785. PubMed: 7535865.
49. Skrastina D, Bulavaite A, Sominskaya I, Kovalevska L, Ose V, et al.; Skrastina D, Bulavaite A, Sominskaya I, Kovalevska L, Ose V, Priede D, Pumpens P, Sasnauskas K, (2008) High immunogenicity of a hydrophilic component of the hepatitis B virus preS1 sequence exposed on the surface of three virus-like particle carriers. Vaccine 26: 1972-1981. doi:10.1016/j.vaccine.2008.02.030. PubMed: 18343539. PII]:S0264-410X(08)00161-8; [doi]: 10.1016/j.vaccine.2008.02.030. PubMed: 18343539. doi:10.1016/j.vaccine.2008.02.030. PubMed: 18343539.
50. Cao T, Lazdina U, Desombere I, Vanlandschoot P, Milich DR, et al. (2001) Hepatitis B virus core antigen binds and activates naive human B cells in vivo: studies with a human PBL-NOD/SCID mouse model. J Virol 75: 6359-6366. doi:10.1128/JVI.75.14.6359-6366.2001. PubMed: 11413302.
51. Milich DR, Chen M, Schödel F, Peterson DL, Jones JE, et al. (1997) Role of B cells in antigen presentation of the hepatitis B core. Proc Natl Acad Sci U S A 94: 14648-14653. doi:10.1073/pnas.94.26.14648. PubMed: 9405667.
52. Cooper A, Tal G, Lider O, Shaul Y, (2005) Cytokine induction by the hepatitis B virus capsid in macrophages is facilitated by membrane heparan sulfate and involves TLR2. J Immunol 175: 3165-3176. PubMed: 16116207. PII]:175/5/3165. PubMed: 16116207.
53. Lee BO, Tucker A, Frelin L, Sallberg M, Jones J, et al.; Lee BO, Tucker A, Frelin L, Sallberg M, Jones J, Peters C, Hughes J, Whitacre D, Darsow B, Peterson DL, Milich DR, (2009) Interaction of the hepatitis B core antigen and the innate immune system. J Immunol 182: 6670-6681. doi:10.4049/jimmunol.0803683. PubMed: 19454661. PII]:182/11/6670; [doi]: 10.4049/jimmunol.0803683. PubMed: 19454661. doi:10.4049/jimmunol.0803683. PubMed: 19454661.
54. Missale G, Redeker A, Person J, Fowler P, Guilhot S, et al. (1993) HLA-A31- and HLA-Aw68-restricted cytotoxic T cell responses to a single hepatitis B virus nucleocapsid epitope during acute viral hepatitis. J Exp Med 177: 751-762. doi:10.1084/jem.177.3.751. PubMed: 7679709.
55. Pumpens P, Ulrich R, Sasnauskas K, Kazaks A, Ose V, et al. (2008) Construction of novel vaccines on the basis of the virus-like particles: Hepatitis B virus proteins as vaccine carriers. In: Khudyakov Y, eds. Medicinal Protein Engineering. Boca Raton, London, NY: CRC Press, Taylor & Francis Group. pp. pp. 205-248.