Expression and characterization of HPV-16 L1 capsid protein in Pichia pastoris

Archives of Virology

Volumn 154, Issue 10, 2009, Pages 1609-1617

  Bazan, Silvia Boschi ^a,b   de Alencar Muniz Chaves, Agtha ^a   Aires, Karina Araújo ^a   Cianciarullo, Aurora Marques ^a   Garcea, Robert L ^c   Ho, Paulo Lee ^a,b  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; L1 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN;

ARTICLE; GENE EXPRESSION REGULATION; HEMAGGLUTINATION INHIBITION TEST; HUMAN PAPILLOMAVIRUS TYPE 16; ISOLATION AND PURIFICATION; METABOLISM; PAPILLOMAVIRUS INFECTION; PHYSIOLOGY; PICHIA; POLYACRYLAMIDE GEL ELECTROPHORESIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIROLOGY; VIRUS CELL TRANSFORMATION; WESTERN BLOTTING;

BLOTTING, WESTERN; CAPSID PROTEINS; CELL TRANSFORMATION, VIRAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION REGULATION, VIRAL; HEMAGGLUTINATION INHIBITION TESTS; HUMAN PAPILLOMAVIRUS 16; MICROSCOPY, ELECTRON, TRANSMISSION; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; PICHIA;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; MIRIDAE; PAPILLOMAVIRIDAE; PICHIA PASTORIS;

EID: 70350379578     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-009-0484-8     Document Type: Article

References (56)

1. Cates WJ (1999) American Social Health Association Panel: estimates of the incidence and prevalence of sexually transmitted diseases in the United States. Sex Transm Dis 26:2-7.
2. Koutsky LA, Galloway DA, Holmes KK (1988) Epidemiology of genital human papillomavirus infection. Epidemiol Rev 10:122-163.
3. De Villiers EM, Fauquet C, Broker TR, Bernard HU, Zur Hausen H (2004) Classification of papillomaviruses. Virology 324:17-27.
4. De Villiers EM (2001) Taxonomic classification of papillomaviruses. Papillomavirus Rep 12:57-63.
5. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Muñoz N (1999) Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189:12-19.
6. Bosch FX, Manos MM, Muñoz N, Sherman M, Jansen AM, Peto J, Schiffman MH, Moreno V, Kurman R, Shah KV (1995) Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. J Natl Cancer Inst 87:796-802.
7. Bosch FX, Lorincz A, Muñoz N, Meijer CJLM, Shah KV (2002) The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 55:244-265.
8. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT (1992) Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci USA 89:12180-12184.
9. Hagensee ME, Yaegashi N, Galloway DA (1993) Self-assembly of human papillomavirus type 1 capsids by expression of the L1 protein alone or by coexpression of the L1 and L2 capsid proteins. J Virol 67:315-322.
10. Rose RC, Bonnez W, Reichman RC, Garcea RL (1993) Expression of human papillomavirus type 11 L1 protein in insect cells: in vivo and in vitro assembly of virus like particles. J Virol 67:1936-1944.
11. Hofmann KJ, Cook JC, Joyce JG, Brown DR, Schultz LD, George HA, Rosolowsky M, Fife KH, Jansen KU (1995) Sequence determination of human papillomavirus type 6a and assembly of virus-like particles in Saccharomyces cerevisiae. Virology 209:506-518.
12. Sasagawa T, Pushko P, Steers G, Gschmeissner S, Hajibagheri M, Finch J, Crawford L, Tommasino M (1995) Synthesis and assembly of virus-like particles of human papillomaviruses type 6 and type 16 in fission yeast Schizosaccharomyces pombe. Virology 206:126-135.
13. Nardelli-Haefliger D, Roden RBS, Benyacoub J, Sahli R, Kraehembuhl JP, Schiller JT, Lachat P, Potts A, De Grandi P (1997) Human papillomavirus type 16 virus-like particles expressed in attenuated Salmonella typhimurium elicit mucosal and systemic neutralizing antibodies in mice. Infect Immun 65:3328-3336.
14. Kelsall SR, Kulski JK (1995) Expression of the major capsid protein of human papillomavirus type-16 in Escherichia coli. J Virol Methods 53:75-90.
15. Chen XS, Casini G, Harrison SC, Garcea RL (2001) Papillomavirus capsid protein expression in Escherichia coli: purification and assembly of HPV11 and HPV16 L1. J Mol Biol 307:173-182.
16. Yang XF, Qu XZ, Wang K, Zheng J, Si LS, Dong XP, Wang YL (2005) Construction of prophylactic human papillomavirus type 16 L1 capsid protein vaccine delivered by live attenuated Shigella flexneri strain sh42. Acta Biochim Biophys Sin 37(11):743-750.
17. Aires KA, Cianciarullo AM, Carneiro SM, Villa LL, Boccardo E, Pérez-Martinez G, Perez-Arellano I, Oliveira MLS, Ho PL (2006) Production of human papillomavirus type 16 L1 virus-like particles by recombinant Lactobacillus casei cells. Appl Environ Microbiol 72:745-752.
18. Cho HJ, Shin HJ, Han IK, Jung WW, Kim YB, Sul D, Oh YK (2007) Induction of mucosal and systemic immune responses following oral immunization of mice with Lactococcus lactis expressing human papillomavirus type 16 L1. Vaccine 25:8049-8057.
19. Carter JJ, Yaegashi N, Jenison SA, Galloway DA (1991) Expression of human papillomavirus proteins in yeast Saccharomyces cerevisiae. Virology 182:513-521.
20. Park MA, Kim HJ, Kim HJ (2008) Optimum conditions for production and purification of human papillomavirus type 16 L1 protein from Saccharomyces cerevisiae. Protein Expr Purif 59:175-181.
21. Kim SN, Jeong HS, Park SN, Kim HJ (2007) Purification and immunogenicity study of human papillomavirus type 16 L1 protein in Saccharomyces cerevisiae. J Virol Methods 139:24-30.
22. Sasagawa T, Tani M, Basha W, Rose RC, Tohda H, Giga-Hama Y, Azar KK, Yasuda H, Sakai A, Inoue M (2005) A human papillomavirus type 16 vaccine by oral delivery of L1 protein. Virus Res 110:81-90.
23. Le Cann P, Coursaget P, Iochmann S, Touze A (1994) Self-assembly of human papillomavirus type 16 capsids by expression of the L1 protein in insect cells. FEMS Microbiol Lett 117:269-274.
24. Biemelt S, Sonnewald U, Galmbacher P, Willmitzer L, Müller M (2003) Production of human papillomavirus type 16 virus-like particles in transgenic plants. J Virol 77:9211-9220.
25. Mclean CS, Churcher MJ, Meinke J, Smith GL, Higgins G, Stanley M, Minson AC (1990) Production and characterisation of a monoclonal antibody to human papillomavirus type 16 using recombinant vaccinia virus. J Clin Pathol 43:488-492.
26. Lai WB, Middelberg AP (2002) The production of human papillomavirus type 16 L1 vaccine product from Escherichia coli inclusion bodies. Bioprocess Biosyst Eng 25:121-128.
27. Cregg JM, Cereghino JI, Shi J, Higgins DR (2000) Recombinant protein expression in Pichia pastoris. Mol Biotechnol 16:23-52.
28. Villa LL, Costa RL, Petta CA, Andrade RP, Paavonen J, Iversen OE, Olsson SE, Hoye J, Steinwall M, Riis-Johannessen G, Andersson-Ellstrom A, Elfgren K, Krogh G, Lehtinen M, Malm C, Tamms GM, Giacoletti K, Lupinacci L, Railkar R, Taddeo FJ, Bryan J, Esser MT, Sings HL, Saah AJ, Barr E (2006) High sustained efficacy of a prophylactic quadrivalent human papillomavirus types 6/11/16/18 L1 virus-like particle vaccine through 5 years of follow-up. Br J Cancer 95:1459-1466.
29. Schiller JT, Castellsagué X, Villa LL, Hildesheim A (2008) An update of prophylactic human papillomavirus L1 virus-like particles vaccine clinical trial results. Vaccine 26:53-61.
30. Harper DM, Franco EL, Wheeler CM, Moscicki AB, Romanowski B, Roteli-Martins CM, Jenkins D, Schuind A, Clemens SAC, Dubin G (2006) Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomized control trial. Lancet 367:1247-1255.
31. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463-5467.
32. Akada R, Murakane T, Nishizawa Y (2000) DNA extraction method for screening yeast clones by PCR. Biotechniques 28:668-674.
33. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
34. Mccarthy MP, White WI, Palmer-HILL F, Koenig S, Suzich JA (1998) Quantitative disassembly and reassembly of human papillomavirus type 11 virus-like particles in vitro. J Virol 72:32-41.
35. Shi L, Sanyal G, Ni A, Luo Z, Doshna S, Wang B, Graham TL, Wang N, Volkin DB (2005) Stabilization of human papillomavirus virus-like particles by non-ionic surfactants. J Pharm Sci 94:1538-1551.
36. Cook JC, Joyce JG, George HA, Schultz LD, Hurni WM, Keller PM, Lehman ED (1999) Purification of virus-like particles of recombinant human papillomavirus type 11 major capsid protein L1 from Saccharomyces cerevisiae. Protein Expr Purif 17:477-484.
37. Zhang W, Carmichael J, Ferguson J, Inglis S, Ashrafian H, Stanley M (1998) Expression of human papillomavirus type 16 L1 protein in Escherichia coli: denaturation renaturation and self-assembly of virus-like particles in vitro. Virology 243:423-431.
38. Joyce JG, Tung JS, Przysiecki CT, Cook JC, Lehman ED, Sands JA, Jansen KU, Keller PM (1999) The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J Biol Chem 274:5810-5822.
39. Rommel O, Dillner J, Fligge C, Bergsdorf C, Wang X, Selinka H-C, Sapp M (2005) Heparan sulfate proteoglycans interact exclusively with conformationally intact HPV L1 assemblies: basis for a virus-like particle ELISA. J Med Virol 75:114-121.
40. Mach H, Volkin DB, Troutman RD, Wang B, Luo Z, Jansen KU, Shi L (2006) Disassembly and reassembly of yeast-derived recombinant human papillomavirus virus-like particles (HPV VLPs). J Pharm Sci 95:2195-2206.
41. Aral SO, Holmes KK (1999) Social and behavioral determinants of epidemiology of STDs: industrialized and developing countries. In: Holmes KK, Mardh P-A, Sparling PF et al (eds) Sexually transmitted diseases. McGraw-Hill, New York, pp 39-76.
42. Paavonen J, Jenkins D, Bosch FX, Naud P, Salmerón J, Wheeler CM, Chow SN, Apter DL, Kitchener HC, Castellsague X, De Carvalho NS, Skinner SR, Harper DM, Hedrick JA, Jaisamrarn U, Limson GA, Dionne M, Quint W, Spiessens B, Peeters P, Struyf F, Wieting SL, Lehtinen MO, Dubin G, Hpv Patricia Study Group (2007) Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind randomised controlled trial. Lancet 369:2161-2170.
43. Potter KJ, Zhang W, Smith LA, Meagher MM (2000) Production and purification of the heavy chain fragment C of botulinum neurotoxin serotype A, expressed in the methylotrophic yeast Pichia pastoris. Protein Expr Purif 19:393-402.
44. Wang Y, Liang Z-H, Zhang Y-S, Yao S-Y, Xu Y-G, Tang Y-H, Zhu S-Q, Cui D-F, Feng Y-M (2001) Human insulin from a precursor overexpressed in the methylotrophic yeast Pichia pastoris and a simple procedure for purifying the expression product. Biotechnol Bioeng 73:74-79.
45. Schilling BM, Goodrick J, Wan NC (2001) Scale up of a high cell density continuous culture with Pichia pastoris X-33 for the constitutive expression of rh-chitinase. Biotechnol Prog 17:629-633.
46. Outchkourov NS, Stiekema WJ, Jongsma MA (2002) Optimization of the expression of equistatin in Pichia pastoris. Prot Expr Purif 24:18-24.
47. Woo JH, Liu YY, Mathias A, Stavrou S, Wang Z, Thompson J, Neville DM (2002) Gene optimization is necessary to express a bivalent anti-human anti-T cell immunotoxin in Pichia pastoris. Protein Expr Purif 25:270-282.
48. Yadava A, Ockenhouse CF (2003) Effect of codon optimization on expression levels of a functionally folded malaria vaccine candidate in prokaryotic and eukaryotic expression systems. Infect Immun 71:4961-4969.
49. Invitrogen Corporation (2002) A manual of methods for expression of recombinant proteins in Pichia pastoris. Invitrogen Corporation, Carlsbad.
50. Liu Z, Pscheidt B, Avi M, Gaisberger R, Hartner FS, Schuster C, Skranc W, Gruber K, Glieder A (2008) Laboratory evolved biocatalysts for stereoselective syntheses of substituted benzaldehyde cyanohydrins. ChemBioChem 9:58-61.
51. Cregg JM, Barringer KJ, Hessler AY, Madden KR (1985) Pichia pastoris as a host system for transformations. Mol Cell Biol 5:3376-3385.
52. Hong I-P, Anderson S, Choi S-G (2006) Evaluation of a new episomal vector based on the GAP promoter for structural genomics in Pichia pastoris. J Microbiol Biotechnol 16:1362-1368.
53. Porro D, Martegani E, Ranzi BM, Alberghina L (1991) Heterologous gene expression in continuous cultures of budding yeast. Appl Microbiol Biotechnol 34:632-636.
54. Giroglou T, Florin L, Schäfer F, Streeck RE, Sapp M (2001) Human papillomavirus infection requires cell surface heparan sulfate. J Virol 75:1565-1570.
55. Rose RC, White WI, Li M, Suzich JA, Lane C, Garcea RL (1998) Human papillomavirus type 11 recombinant L1 capsomeres induce virus-neutralizing antibodies. J Virol 72:6151-6154.
56. Thönes N, Herreiner A, Schädlich L, Piuko K, Müller M (2008) A direct comparison of human papillomavirus type 16 L1 particles reveals a lower immunogenicity of capsomeres than virus like particles with respect to the induced antibody response. J Virol 82:5472-5485.