Improved fusion tag cleavage strategies in the downstream processing of self-assembling virus-like particle vaccines

Food and Bioproducts Processing

Volumn 92, Issue 2, 2014, Pages 143-151

  Connors, Natalie K ^a   Wu, Yang ^a   Lua, Linda H L ^a   Middelberg, Anton P J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Enzyme; GST; Murine polyomavirus; TEVp; Thrombin; Virus like particles

Indexed keywords

VACCINES; VIRUSES;

GST; POLYOMAVIRUS; TEVP; THROMBIN; VIRUS-LIKE PARTICLES;

ENZYMES;

MURINE POLYOMAVIRUS; NICOTIANA TABACUM; POLYOMAVIRUS; TOBACCO ETCH VIRUS;

EID: 84898938331     PISSN: 09603085     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fbp.2013.08.012     Document Type: Article

References (56)

1. U. Arora, P. Tyagi, S. Swaminathan, and N. Khanna Chimeric hepatitis B core antigen virus-like particles displaying the envelope domain III of dengue virus type 2 J. Nanobiotechnol. 10 30 2012 1 6
2. A. Bertolotti-Ciarlet, M. Ciarlet, S.E. Crawford, M.E. Conner, and M.K. Estes Immunogenicity and protective efficacy of rotavirus 2/6-virus-like particles produced by a dual baculovirus expression vector and administered intramuscularly, intranasally, or orally to mice Vaccine 21 2003 3885 3900
3. W. Bode Structure and interaction modes of thrombin Blood Cells Mol. Dis. 36 2006 122 130
4. B.C. Buckland The process development challenge for a new vaccine Nat. Med. 11 2005 S16 S19
5. L.D. Cabrita, D. Gilis, A.L. Robertson, Y. Dehouck, M. Rooman, and S.P. Bottomley Enhancing the stability and solubility of TEV protease using in silico design Protein Sci. 16 2007 2360 2367
6. J.C. Carrington, and W.G. Dougherty Small nuclear inclusion protein encoded by a plant potyvirus genome is a protease J. Virol. 61 1987 2540 2548
7. B. Chackerian, D.R. Lowy, and J.T. Schiller Conjugation of a self-antigen to papillomavirus-like particles allows for efficient induction of protective autoantibodies J. Clin. Invest. 108 2001 415 423
8. J.Y. Chang Thrombin specificity - requirement for apolar amino-acids adjacent to the thrombin cleavage site of polypeptide substrate Eur. J. Biochem. 151 1985 217 224
9. C.S. Chen, S.Y. Suen, S.Y. Lai, G.R.L. Chang, T.C. Lu, M.S. Lee, and M.Y. Wang Purification of capsid-like particles of infectious bursal disease virus (IBDV) VP2 expressed in E. coli with a metal-ion affinity membrane system J. Virol. Methods 130 2005 51 58
10. Y.P. Chuan, Y.Y. Fan, L. Lua, and A.P.J. Middelberg Quantitative analysis of virus-like particle size and distribution by field-flow fractionation Biotechnol. Bioeng. 99 2008 1425 1433
11. Y.P. Chuan, L.H.L. Lua, and A.P.J. Middelberg High-level expression of soluble viral structural protein in Escherichia coli J. Biotechnol. 134 2008 64 71
12. Y.P. Chuan, T. Rivera-Hernandez, N. Wibowo, N.K. Connors, Y. Wu, F.K. Hughes, L.H. Lua, and A.P. Middelberg Effects of pre-existing anti-carrier immunity and antigenic element multiplicity on efficacy of a modular virus-like particle vaccine Biotechnol. Bioeng. 2013 (in press)
13. M. Ciarlet, S.E. Crawford, C. Barone, A. Bertolotti-Ciarlet, R.F. Ramig, M.K. Estes, and M.E. Conner Subunit rotavirus vaccine administered parenterally to rabbits induces active protective immunity J. Virol. 72 1998 9233 9246
14. L.A. Collins-Racie, J.M. McColgan, K.L. Grant, E.A. Diblasiosmith, J.M. McCoy, and E.R. Lavallie Production of recombinant bovine enterokinase catalytic subunit in Escherichia coli using the novel secretory fusion partner Dsba Bio-Technology 13 1995 982 987
15. N. Connors Identification of Properties that Affect in vitro Virus-Like Particle Assembly 2011 The University of Queensland Brisbane, Australia (PhD thesis)
16. W.G. Dougherty, and T.D. Parks Posttranslational processing of the tobacco etch virus 49-kda small nuclear inclusion polyprotein - identification of an internal cleavage site and delimitation of vpg and proteinase domains Virology 183 1991 449 456
17. C.J. Fee Size-exclusion reaction chromatography (SERC): a new technique for protein PEGylation Biotechnol. Bioeng. 82 2003 200 206
18. J.L. Foo, C.B. Ching, M.W. Chang, and S.S.J. Leong The imminent role of protein engineering in synthetic biology Biotechnol. Adv. 30 2012 541 549
19. R.L. Garcea, D.M. Salunke, and D.L.D. Caspar Site-directed mutation affecting polyomavirus capsid self-assembly in vitro Nature 329 1987 86 88
20. E. Gasteiger, A. Gattiker, C. Hoogland, I. Ivanyi, R.D. Appel, and A. Bairoch ExPASy: the proteomics server for in-depth protein knowledge and analysis Nucl. Acids Res. 31 2003 3784 3788
21. M. Goujon, H. McWilliam, W. Li, F. Valentin, S. Squizzato, J. Paern, and R. Lopez A new bioinformatics analysis tools framework at EMBL-EBI Nucl. Acids Res. 38 2010 W695 W699
22. S.J. Hanslip, N.R. Zaccai, A.P.J. Middelberg, and R.J. Falconer Assembly of human papillomavirus type-16 virus-like particles: multifactorial study of assembly and competing aggregation Biotechnol. Progr. 22 2006 554 560
23. S.J. Hanslip, N.R. Zaccai, A.P.J. Middelberg, and R.J. Falconer Intrinsic fluorescence as an analytical probe of virus-like particle assembly and maturation Biochem. Biophys. Res. Commun. 375 2008 351 355
24. M. Herbst-Kralovetz, H.S. Mason, and Q. Chen Norwalk virus-like particles as vaccines Exp. Rev. Vaccines 9 2010 299 307
25. T. Hosfield, and Q. Lu Influence of the amino acid residue downstream of (Asp)(4)Lys on enterokinase cleavage of a fusion protein Anal. Biochem. 269 1999 10 16
26. G.T. Jennings, and M.F. Bachmann Coming of age of virus-like particle vaccines Biol. Chem. 389 2008 521 536
27. R.J. Jenny, K.G. Mann, and R.L. Lundblad A critical review of the methods for cleavage of fusion proteins with thrombin and factor Xa Protein Exp. Purif. 31 2003 1 11
28. R.B. Kapust, J. Tozser, T.D. Copeland, and D.S. Waugh The P1′ specificity of tobacco etch virus protease Biochem. Biophys. Res. Commun. 294 2002 949 955
29. R.B. Kapust, J. Tozser, J.D. Fox, D.E. Anderson, S. Cherry, T.D. Copeland, and D.S. Waugh Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency Protein Eng. 14 2001 993 1000
30. F. Krammer, and R. Grabherr Alternative influenza vaccines made by insect cells Trends Mol. Med. 16 2010 313 320
31. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
32. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, and D.G. Higgins Clustal W and clustal X version 2.0 Bioinformatics 23 2007 2947 2948
33. X. Li, Y.G. Qu, P. Jia, L.M. Liu, H.F. Ji, D.Y. He, N.Y. Jin, and B.R. Chi Expression and characterization of a recombinant truncated capsid protein of hepatitis E virus Chem. J. Chin. Univ. 33 2012 2481 2485
34. M.W.O. Liew, A. Rajendran, and A.P.J. Middelberg Microbial production of virus-like particle vaccine protein at gram-per-litre levels J. Biotechnol. 150 2010 224 231
35. D.I. Lipin, L.H.L. Lua, and A.P.J. Middelberg Quaternary size distribution of soluble aggregates of glutathione-S-transferase-purified viral protein as determined by asymmetrical flow field flow fractionation and dynamic light scattering J. Chromatogr. A 1190 2008 204 214
36. D.I. Lipin, A. Raj, L.H.L. Lua, and A.P.J. Middelberg Affinity purification of viral protein having heterogeneous quaternary structure: modeling the impact of soluble aggregates on chromatographic performance J. Chromatogr. A 1216 2009 5696 5708
37. J.D. Lonsdale-Eccles, D.H. Hogg, and D.T. Elmore The hydrolysis of chemically modified proteins by factor-xa and thrombin Biochim. Biophys. Acta 612 1980 401 409
38. Z. Marcekova, I. Psikal, E. Kosinova, O. Benada, P. Sebo, and L. Bumba Heterologous expression of full-length capsid protein of porcine circovirus 2 in Escherichia coli and its potential use for detection of antibodies J. Virol. Methods 162 2009 133 141
39. W.J. McAleer, E.B. Buynak, R.Z. Maigetter, D.E. Wampler, W.J. Miller, and M.R. Hilleman Human hepatitis-B vaccine from recombinant yeast Nature 307 1984 178 180
40. A.P.J. Middelberg, T. Rivera-Hernandez, N. Wibowo, L.H.L. Lua, Y.Y. Fan, G. Magor, C. Chang, Y.P. Chuan, M.F. Good, and M.R. Batzloff A microbial platform for rapid and low-cost virus-like particle and capsomere vaccines Vaccine 29 2011 7154 7162
41. B.K. Nfor, P.D.E.M. Verhaert, L.A.M. van der Wielen, J. Hubbuch, and M. Ottens Rational and systematic protein purification process development: the next generation Trends Biotechnol. 27 2009 673 679
42. F.A. Ofosu, S. Crean, and M.W. Reynolds A safety review of topical bovine thrombin-induced generation of antibodies to bovine proteins Clin. Ther. 31 2009 679 691
43. J. Paavonen, P. Naud, J. Salmeron, C.M. Wheeler, S.N. Chow, D. Apter, H. Kitchener, X. Castellsague, J.C. Teixeira, S.R. Skinner, J. Hedrick, U. Jaisamrarn, G. Limson, S. Garland, A. Szarewski, B. Romanowski, F.Y. Aoki, T.F. Schwarz, W.A.J. Poppe, F.X. Bosch, D. Jenkins, K. Hardt, T. Zahaf, D. Descamps, F. Struyf, M. Lehtinen, G. Dubin, and H.P.S. Group Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women Lancet 374 2009 301 314
44. L.K. Pattenden, A.P.J. Middelberg, M. Niebert, and D.I. Lipin Towards the preparative and large-scale precision manufacture of virus-like particles Trends Biotechnol. 23 2005 523 529
45. D.A. Polayes, T.D. Parks, S.A. Johnston, and W.G. Dougherty Application of TEV protease in protein production Methods Mol. Med. 13 1998 169 183
46. F.S. Quan, A. Vunnava, R.W. Compans, and S.M. Kang Virus-like particle vaccine protects against 2009 H1N1 pandemic influenza virus in mice PloS One 5 2 2010 e9161
47. T. Rivera-Hernandez, J. Hartas, Y. Wu, Y.P. Chuan, L.H.L. Lua, M. Good, M.R. Batzloff, and A.P.J. Middelberg Self-adjuvanting modular virus-like particles for mucosal vaccination against group A streptococcus (GAS) Vaccine 31 2013 1950 1955
48. S. Rollié, M. Mangold, and K. Sundmacher Designing biological systems: systems engineering meets synthetic biology Chem. Eng. Sci. 69 2012 1 29
49. G.v. Rossum, and J.d. Boer Interactively testing remote servers using the python programming language CWI Quart. 4 1991 283 303
50. I. Schechter, and A. Berger On the size of the active site in proteases. I. Papain Biochem. Biophys. Res. Commun. 27 1967 157 162
51. K. Slupetzky, S. Shafti-Keramat, P. Lenz, S. Brandt, A. Grassauer, M. Sara, and R. Kirnbauer Chimeric papillomavirus-like particles expressing a foreign epitope on capsid surface loops J. Gen. Virol. 82 2001 2799 2804
52. L.L. Villa, R.L.R. Costa, C.A. Petta, R.P. Andrade, K.A. Ault, A.R. Giuliano, C.M. Wheeler, L.A. Koutsky, C. Malm, M. Lehtinen, F.E. Skjeldestad, S.E. Olsson, M. Steinwall, D.R. Brown, R. Kurman, B.M. Ronnett, M.H. Stoler, A. Ferenczy, D.M. Harper, G.M. Tamms, J. Yu, L. Lupinacci, R. Railkar, F.J. Taddeo, K.U. Jansen, M.T. Esser, H.L. Sings, and A.J. Saah Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial Lancet Oncol. 6 2005 271 278
53. K. Wada, K. Kimura, A. Hasegawa, K. Fukuyama, and K. Nagasaki Establishment of a bacterial expression system and immunoassay platform for the major capsid protein of HcRNAV, a dinoflagellate-infecting RNA virus Microb. Environ. 27 2012 483 489
54. D.S. Waugh An overview of enzymatic reagents for the removal of affinity tags Protein Exp. Purif. 80 2011 283 293
55. N. Wibowo, Y.P. Chuan, L.H.L. Lua, and A.P.J. Middelberg Modular engineering of a microbially-produced viral capsomere vaccine for influenza Chem. Eng. Sci. 2012 10.1016/j.ces.2012.04.001
56. K.R. Young, S.P. McBurney, L.U. Karkhanis, and T.M. Ross Virus-like particles: designing an effective AIDS vaccine Methods 40 2006 98 117