Escherichia coli-based cell free production of flagellin and ordered flagellin display on virus-like particles

Biotechnology and Bioengineering

Volumn 110, Issue 8, 2013, Pages 2073-2085

  Lu, Yuan ^a   Welsh, John P ^a   Chan, Wei ^a   Swartz, James R ^a  

^a Stanford University   (United States)

Author keywords

Cell free protein synthesis; Enhanced TLR stimulation; Flagellin; Vaccine adjuvant; Virus like particle; VLP vaccines

Indexed keywords

CELL FREE PROTEIN SYNTHESIS; ENHANCED TLR STIMULATION; FLAGELLIN; VACCINE ADJUVANTS; VIRUS-LIKE PARTICLES;

AMINO ACIDS; CYCLOADDITION; ESCHERICHIA COLI; HYDROCARBONS; SALMONELLA; VACCINES;

VIRUSES;

ALKYNE; AZIDE; FLAGELLIN; TOLL LIKE RECEPTOR 5;

AMBER MUTANT; ARTICLE; BIOLOGICAL ACTIVITY; ESCHERICHIA COLI; HEPATITIS B; NONHUMAN; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; VIRUS LIKE AGENT;

ADJUVANTS, IMMUNOLOGIC; ESCHERICHIA COLI; FLAGELLIN; HEPATITIS B CORE ANTIGENS; HUMANS; SALMONELLA TYPHIMURIUM; TOLL-LIKE RECEPTOR 5; VACCINES, VIRUS-LIKE PARTICLE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SALMONELLA TYPHIMURIUM;

EID: 84879601253     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.24903     Document Type: Article

References (54)

1. Abdulla AA, Alkazaz A, Melconian AK, Saeed AM. 2012. Design and evaluation of a recombinant flagellin-based putative vaccine from Salmonella typhimurium DT104. Int J Sci Res 1(1):1-6.
2. Albayrak C, Swartz JR. 2013. Cell-free co-production of an orthogonal transfer RNA activates efficient site-specific non-natural amino acid incorporation. Nucleic Acids Res, DOI: 10.1093/nar/gkt226.
3. Andersen-Nissen E, Smith KD, Bonneau R, Strong RK, Aderem A. 2007. A conserved surface on Toll-like receptor 5 recognizes bacterial flagellin. J Exp Med 204(2):393-403.
4. Andersen-Nissen E, Smith KD, Strobe KL, Barrett SL, Cookson BT, Logan SM, Aderem A. 2005. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci USA 102(26):9247-9252.
5. Bachmann MF, Zinkernagel RM. 1997. Neutralizing antiviral B cell responses. Ann Rev Immunol 15:235-270.
6. Braga CJM, Massis LM, Alencar BCG, Rodrigues MM, Sbrogio-Almeida ME, Ferreira LCS. 2008. Cytotoxic T cell adjuvant effects of three Salmonella enterica flagellins. Braz J Microbiol 39(1):44-49.
7. Bundy BC, Franciszkowicz MJ, Swartz JR. 2008. Escherichia coli-based cell-free synthesis of virus-like particles. Biotechnol Bioeng 100(1):28-37.
8. Calhoun KA, Swartz JR. 2005. An economical method for cell-free protein synthesis using glucose and nucleoside monophosphates. Biotechnol Prog 21(4):1146-1153.
9. Campodonico VL, Llosa NJ, Grout M, Doring G, Maira-Litran T, Pier GB. 2010. Evaluation of flagella and flagellin of Pseudomonas aeruginosa as vaccines. Infect Immun 78(2):746-755.
10. Deiters A, Schultz PG. 2005. In vivo incorporation of an alkyne into proteins in Escherichia coli. Bioorg Med Chem Lett 15(5):1521-1524.
11. Fedorov OV, Pyatibratov MG, Kostyukova AS, Osina NK, Tarasov VY. 1994. Protofilament as a structural element of flagella of haloalkalophilic archaebacteria. Can J Microbiol 40(1):45-53.
12. Goerke AR. 2008. Cell-free protein synthesis of complex proteins and protein assemblies containing post-translational modification. California, US: Stanford University. p 312.
13. Goerke AR, Swartz JR. 2008. Development of cell-free protein synthesis platforms for disulfide bonded proteins. Biotechnol Bioeng 99(2):351-367.
14. Gruber AR, Lorenz R, Bernhart SH, Neuboock R, Hofacker IL. 2008. The vienna RNA websuite. Nucleic Acids Res 36:W70-W74.
15. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410(6832):1099-1103.
16. Ichiki A, Parish CR. 1972a. Cleavage of bacterial flagellin with proteolytic-enzymes. 1. Physicochemical and antigenic properties of tryptic and peptic peptides. Immunochemistry 9(2):153-167.
17. Ichiki AT, Parish CR. 1972b. Cleavage of bacterial flagellin with proteolytic-enzymes. 2. Induction of enhanced delayed-type hypersensitivity to flagellin by peptic fragments of protein. Cell Immunol 4(3):264-278.
18. Jewett MC, Swartz JR. 2004. Mimicking the Escherichia coli cytoplasmic environment activates long-lived and efficient cell-free protein synthesis. Biotechnol Bioeng 86(1):19-26.
19. Khan MAS, Kang J, Steiner TS. 2004. Enteroaggregative Escherichia coli flagellin-induced interleukin-8 secretion requires toll-like receptor 5-dependent p38 MAP kinase activation. Immunology 112(4):651-660.
20. Kuchenreuther JM, Stapleton JA, Swartz JR. 2009. Tyrosine, cysteine, and s-adenosyl methionine stimulate in vitro [FeFe] hydrogenase activation. Plos ONE 4(10):e7565.
21. Kudla G, Murray AW, Tollervey D, Plotkin JB. 2009. Coding-sequence determinants of gene expression in Escherichia coli. Science 324(5924):255-258.
22. McDermott PF, Ciacci-Woolwine F, Snipes JA, Mizel SB. 2000. High-affinity interaction between gram-negative flagellin and a cell surface polypeptide results in human monocyte activation. Infect Immun 68(10):5525-5529.
23. Mizel SB, Bates JT. 2010. Flagellin as an adjuvant: Cellular mechanisms and potential. J Immunol 185(10):5677-5682.
24. Mizel SB, Honko AN, Moors MA, Smith PS, West AP. 2003. Induction of macrophage nitric oxide production by gram-negative flagellin involves signalling via heteromeric toll-like receptor 5/toll-like receptor 4 complexes. J Immunol 170(12):6217-6223.
25. Oliveira BH, Silva MR, Braga CJM, Massis LM, Ferreira LCS, Sbrogio-Almeida ME, Takagi M. 2011. Production of native flagellin from Salmonella typhimurium in a bioreactor and purification by tangential ultrafiltration. Braz J Chem Eng 28(4):575-584.
26. Patel KG, Swartz JR. 2011. Surface functionalization of virus-like particles by direct conjugation using azide-alkyne click chemistry. Bioconjug Chem 22(3):376-387.
27. Reddy ST, Swartz MA, Hubbell JA. 2006. Targeting dendritic cells with biomaterials: Developing the next generation of vaccines. Trends Immunol 27(12):573-579.
28. Rostovtsev VV, Green LG, Fokin VV, Sharpless KB. 2002. A stepwise huisgen cycloaddition process: Copper(I)-catalyzed regioselective "ligation" of azides and terminal alkynes. Angew Chem Int Ed Engl 41(14):2596-2599.
29. Saha S, Takeshita F, Matsuda T, Jounai N, Kobiyama K, Matsumoto T, Sasaki S, Yoshida A, Xin KQ, Klinman DM, Uematsu S, Ishii KJ, Akira S, Okuda K. 2007. Blocking of the TLR5 activation domain hampers protective potential of flagellin DNA vaccine. J Immunol 179(2):1147-1154.
30. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671-675.
31. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1(6):2856-2860.
32. Skountzou I, Martin Mdel P, Wang B, Ye L, Koutsonanos D, Weldon W, Jacob J, Compans RW. 2010. Salmonella flagellins are potent adjuvants for intranasally administered whole inactivated influenza vaccine. Vaccine 28(24):4103-4112.
33. Smith KD, Andersen-Nissen E, Hayashi F, Strobe K, Bergman MA, Barrett SLR, Cookson BT, Aderem A. 2003. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4(12):1247-1253.
34. Song L, Zhang Y, Yun NE, Poussard AL, Smith JN, Smith JK, Borisevich V, Linde JJ, Zacks MA, Li H, Kavita U, Reiserova L, Liu X, Dumuren K, Balasubramanian B, Weaver B, Parent J, Umlauf S, Liu G, Huleatt J, Tussey L, Paessler S. 2009. Superior efficacy of a recombinant flagellin:H5N1 HA globular head vaccine is determined by the placement of the globular head within flagellin. Vaccine 27(42):5875-5884.
35. Strable E, Prasuhn DE, Udit AK, Brown S, Link AJ, Ngo JT, Lander G, Quispe J, Potter CS, Carragher B, Tirrell DA, Finn MG. 2008. Unnatural amino acid incorporation into virus-like particles. Bioconjug Chem 19(4):866-875.
36. Swartz JR. 2012. Transforming biochemical engineering with cell-free biology. Aiche J 58(1):5-13.
37. Tornoe CW, Christensen C, Meldal M. 2002. Peptidotriazoles on solid phase: [1, 2, 3]-triazoles by regiospecific copper(i)-catalyzed 1, 3-dipolar cycloadditions of terminal alkynes to azides. J Org Chem 67(9):3057-3064.
38. Treanor JJ, Taylor DN, Tussey L, Hay C, Nolan C, Fitzgerald T, Liu G, Kavita U, Song L, Dark I, Shaw A. 2010. Safety and immunogenicity of a recombinant hemagglutinin influenza-flagellin fusion vaccine (VAX125) in healthy young adults. Vaccine 28(52):8268-8274.
39. Vonderviszt F, Aizawa SI, Namba K. 1991. Role of the disordered terminal regions of flagellin in filament formation and stability. J Mol Biol 221(4):1461-1474.
40. Vonderviszt F, Kanto S, Aizawa S, Namba K. 1989. Terminal regions of flagellin are disordered in solution. J Mol Biol 209(1):127-133.
41. Wang BZ, Quan FS, Kang SM, Bozja J, Skountzou I, Compans RW. 2008. Incorporation of membrane-anchored flagellin into influenza virus-like particles enhances the breadth of immune responses. J Virol 82(23):11813-11823.
42. Welsh JP, Lu Y, He X-S, Greenberg HB, Swartz JR. 2012. Cell-free production of trimeric influenza hemagglutinin head domain proteins as vaccine antigens. Biotechnol Bioeng 109(12):2962-2969.
43. Welsh JP, Patel KG, Manthiram K, Swartz JR. 2009. Multiply mutated Gaussia luciferases provide prolonged and intense bioluminescence. Biochem Biophys Res Commun 389(4):563-568.
44. Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF. 1999. Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531-552.
45. Wuu JJ, Swartz JR. 2008. High yield cell-free production of integral membrane proteins without refolding or detergents. Biochimica et Biophysica Acta 1778(5):1237-1250.
46. Yamamoto S, Kutsukake K. 2006. Flja-mediated posttranscriptional control of phase 1 flagellin expression in flagellar phase variation of Salmonella enterica serovar typhimurium. J Bacteriol 188(3):958-967.
47. Yang JH, Kanter G, Voloshin A, Michel-Reydellet N, Velkeen H, Levy R, Swartz JR. 2005. Rapid expression of vaccine proteins for B-cell lymphoma in a cell-free system. Biotechnol Bioeng 89(5):503-511.
48. Yang WC, Patel KG, Lee J, Ghebremariam YT, Wong HE, Cooke JP, Swartz JR. 2009. Cell-free production of transducible transcription factors for nuclear reprogramming. Biotechnol Bioeng 104(6):1047-1058.
49. Yonekura K, Maki-Yonekura S, Namba K. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424(6949):643-650.
50. Yoshida H, Okamoto K, Iwamoto T, Sakai E, Kanaoka K, Hu JP, Shibata M, Hotokezaka H, Nishishita K, Mizuno A, Kato Y. 2006. Pepstatin A, an aspartic proteinase inhibitor, suppresses RANKL-induced osteoclast differentiation. J Biochem 139(3):583-590.
51. Zhang J, Xu KP, Ambati B, Yu FSX. 2003. Toll-like receptor 5-mediated corneal epithelial inflammatory responses to Pseudomonas aeruginosa flagellin. Invest Ophthalmol Vis Sci 44(10):4247-4254.
52. 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(23):7412-7421.
53. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31(13):3406-3415.
54. Zuker M, Stiegler P. 1981. Optimal computer folding of large rna sequences using thermodynamics and auxiliary information. Nucleic Acids Res 9(1):133-148.