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References

  1. Mach H, Volkin DB, Troutman RD, Wang B, Luo Z, Jansen KU, et al. 2006. Disassembly and reassembly of yeast‐derived recombinant human papillomavirus virus‐like particles (HPV VLPs). J. Pharm. Sci. 95: 2195-2206.
  2. Braaten KP, Laufer MR. 2008. Human papillomavirus (HPV), HPV-related disease, and the HPV vaccine. Rev. Obstet. Gynecol. 1: 2.
  3. Mustopa AZ, Meilina L, Irawan S, Ekawati N, Fathurahman AT, Triratna L, et al. 2022. Construction, expression, and in vitro assembly of virus-like particles of L1 protein of human papillomavirus type 52 in Escherichia coli BL21 DE3. J. Genet. Eng. Biotechnol. 20: 19.
  4. Forman D, De Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J, Bruni L, et al. 2012. Global burden of human papillomavirus and related diseases. Vaccine 30: F12-F23.
  5. Le DT, Müller KM. 2021. In vitro assembly of virus-like particles and their applications. Life 11: 334.
  6. Chen XS, Garcea RL, Goldberg I, Casini G, Harrison SC. 2000. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol. Cell 5: 557-567.
  7. Zhao Q, Modis Y, High K, Towne V, Meng Y, Wang Y, et al. 2012. Disassembly and reassembly of human papillomavirus virus-like particles produces more virion-like antibody reactivity. Virol. J. 9: 52.
  8. Buck CB, Day PM, Trus BL. 2013. The papillomavirus major capsid protein L1. Virology 445: 169-174.
  9. Hagensee ME, Yaegashi N, Galloway D. 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. Nooraei S, Bahrulolum H, Hoseini ZS, Katalani C, Hajizade A, Easton AJ, et al. 2021. Virus-like particles: preparation, immunogenicity and their roles as nanovaccines and drug nanocarriers. J. Nanobiotechnology 19: 59.
  11. Zeltins A. 2013. Construction and characterization of virus-like particles: a review. Mol. Biotechnol. 53: 92-107.
  12. Franco EL, Harper DM. 2005. Vaccination against human papillomavirus infection: a new paradigm in cervical cancer control. Vaccine 23: 2388-2394.
  13. Zaman R, Islam RA, Ibnat N, Othman I, Zaini A, Lee CY, et al. 2019. Current strategies in extending half-lives of therapeutic proteins. J. Control. Release 301: 176-189.
  14. Lim SI, Hahn YS, Kwon I. 2015. Site-specific albumination of a therapeutic protein with multi-subunit to prolong activity in vivo. J. Control. Release 207: 93-100.
  15. Yang B, Kwon I. 2021. Multivalent albumin-neonatal Fc receptor interactions mediate a prominent extension of the serum half-life of a therapeutic protein. Mol. Pharm. 18: 2397-2405.
  16. Dennis MS, Zhang M, Meng YG, Kadkhodayan M, Kirchhofer D, Combs D, et al. 2002. Albumin binding as a general strategy for improving the pharmacokinetics of proteins. J. Biol. Chem. 277: 35035-35043.
  17. Cho J, Lim SI, Yang BS, Hahn YS, Kwon I. 2017. Generation of therapeutic protein variants with the human serum albumin binding capacity via site-specific fatty acid conjugation. Sci. Rep. 7: 18041.
  18. Chin JW. 2017. Expanding and reprogramming the genetic code. Nature 550: 53-60.
  19. Shandell MA, Tan Z, Cornish VW. 2021. Genetic code expansion: a brief history and perspective. Biochemistry 60: 3455-3469.
  20. Wang N, Li Y, Niu W, Sun M, Cerny R, Li Q, et al. 2014. Construction of a live‐attenuated HIV‐1 vaccine through genetic code expansion. Angewandte Chemie 126: 4967-4971.
  21. Cho H, Daniel T, Buechler YJ, Litzinger DC, Maio Z, Putnam A-MH, et al. 2011. Optimized clinical performance of growth hormone with an expanded genetic code. Proc. Natl. Acad. Sci. USA 108: 9060-9065.
  22. Luo X, Zambaldo C, Liu T, Zhang Y, Xuan W, Wang C, et al. 2016. Recombinant thiopeptides containing noncanonical amino acids. Proc. Natl. Acad. Sci. USA 113: 3615-3620.
  23. Yao T, Zhou X, Zhang C, Yu X, Tian Z, Zhang L, et al. 2017. Site-specific PEGylated adeno-associated viruses with increased serum stability and reduced immunogenicity. Molecules 22: 1155.
  24. Zhang B, Xu H, Chen J, Zheng Y, Wu Y, Si L, et al. 2015. Development of next generation of therapeutic IFN-α2b via genetic code expansion. Acta Biomater. 19: 100-111.
  25. Wang L, Brock A, Herberich B, Schultz PG. 2001. Expanding the genetic code of Escherichia coli. Science 292: 498-500.
  26. Davis L, Chin JW. 2012. Designer proteins: applications of genetic code expansion in cell biology. Nat. Rev. Mol. Cell Biol. 13: 168-182.
  27. Young TS, Ahmad I, Yin JA, Schultz PG. 2010. An enhanced system for unnatural amino acid mutagenesis in E. coli. J. Mol. Biol. 395: 361-374.
  28. Kim J, Choi J-I. 2022. Expression of green fluorescence proteins with non-canonical amino acids in different Escherichia coli strains.
  29. Lee D, Kim MK, Choi JI. 2023. Development of orthogonal aminoacyl tRNA synthetase mutant with enhanced incorporation ability with para-azido-L-phenylalanine. Biotechnol. Bioprocess Eng. 28: 398-405.
  30. Bang HB, Lee YH, Lee YJ, Jeong KJ. 2016. High-level production of human papillomavirus (HPV) type 16 L1 in Escherichia coli. J. Microbiol.Biotechnol. 26: 356-363.
  31. Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, et al. 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596: 583-589.
  32. Delano WL. 2002. Pymol: an open-source molecular graphics tool. CCP4 Newsl. Protein Crystallogr. 40: 82-92.
  33. Wischke C, Borchert HH. 2006. Fluorescein isothiocyanate labelled bovine serum albumin (FITC-BSA) as a model protein drug:opportunities and drawbacks. Pharmazie 61: 770-774.
  34. Wei M, Wang D, Li Z, Song S, Kong X, Mo X, et al. 2018. N-terminal truncations on L1 proteins of human papillomaviruses promote their soluble expression in Escherichia coli and self-assembly in vitro. Emerg. Microbes Infect. 7: 160.
  35. Huang X, Wang X, Zhang J, Xia N, Zhao Q. 2017. Escherichia coli-derived virus-like particles in vaccine development. NPJ Vaccines 2: 3.
  36. Terpe K. 2006. Overview of bacterial expression systems for heterologous protein production: from molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol. 72: 211-222.
  37. Cho HJ, Sun Hahm M, Kuk Kim M, Han IK, Jung WW, Choi HG, et al. 2007. Expression, purification, and antibody binding activity of human papillomavirus 16 L1 protein fused to maltose binding protein. Protein Pept. Lett. 14: 417-424.
  38. Wang Q, Parrish AR, Wang L. 2009. Expanding the genetic code for biological studies. Chem. Biol. 16: 323-336.
  39. Liu CC, Schultz PG. 2010. Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79: 413-444.
  40. Lee D, Kim JG, Kim TW, Choi J. 2024. Development of orthogonal aminoacyl-tRNA synthetase mutant for incorporating a noncanonical amino acid. AMB Express 14: 60.
  41. Wang JW, Roden RB. 2013. Virus-like particles for the prevention of human papillomavirus-associated malignancies. Expert. Rev. Vaccines 12: 129-141.

Article

Research article

J. Microbiol. Biotechnol. 2024; 34(9): 1926-1932

Published online September 28, 2024 https://doi.org/10.4014/jmb.2407.07033

Copyright © The Korean Society for Microbiology and Biotechnology.

Engineering of Recombinant Human Papillomavirus 16 L1 Protein for Incorporation with para-Azido-L-Phenylalanine

Jinhyeon Kim1, Ki Jun Jeong2, Geun-Joong Kim3, and Jong-il Choi1*

1Department of Biotechnology and Bioengineering, Chonnam National University, Gwangju 61186, Republic of Korea
2Department of Chemical and Biomolecular Engineering, KAIST, Daejeon 34141, Republic of Korea
3Department of Biological Sciences and Research Center of Ecomimetics, Chonnam National University, Gwangju 61186, Republic of Korea

Correspondence to:Jong-il Choi,         choiji01@chonnam.ac.kr

Received: July 19, 2024; Revised: July 30, 2024; Accepted: July 30, 2024

Abstract

Human papillomavirus (HPV) L1 capsid protein were produced in several host systems, but few studies have focused on enhancing the properties of the L1 protein. In this study, we aimed to produce recombinant Human papillomavirus (HPV) L1 capsid protein containing para-azido-L-phenylalanine (pAzF) in Escherichia coli. First, we expressed the maltose-binding protein (MBP)-fused HPV16 L1, and 5 residues in HPV16 L1 protein were selected by the in silico modeling for amber codon substitution. Among the variants of the five locations, we identified a candidate that exhibited significant differences in expression with and without pAzF via genetic code expansion (GCE). The expressed recombinant MBP-HPV16L1 protein was confirmed for incorporation of pAzF and the formation of VLPs was tested in vitro.

Keywords: Human papillomavirus L1 protein, site-directed mutagenesis, para-azido-L-phenylalanine, viruslike particle, Escherichia coli

References

  1. Mach H, Volkin DB, Troutman RD, Wang B, Luo Z, Jansen KU, et al. 2006. Disassembly and reassembly of yeast‐derived recombinant human papillomavirus virus‐like particles (HPV VLPs). J. Pharm. Sci. 95: 2195-2206.
  2. Braaten KP, Laufer MR. 2008. Human papillomavirus (HPV), HPV-related disease, and the HPV vaccine. Rev. Obstet. Gynecol. 1: 2.
  3. Mustopa AZ, Meilina L, Irawan S, Ekawati N, Fathurahman AT, Triratna L, et al. 2022. Construction, expression, and in vitro assembly of virus-like particles of L1 protein of human papillomavirus type 52 in Escherichia coli BL21 DE3. J. Genet. Eng. Biotechnol. 20: 19.
  4. Forman D, De Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J, Bruni L, et al. 2012. Global burden of human papillomavirus and related diseases. Vaccine 30: F12-F23.
  5. Le DT, Müller KM. 2021. In vitro assembly of virus-like particles and their applications. Life 11: 334.
  6. Chen XS, Garcea RL, Goldberg I, Casini G, Harrison SC. 2000. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol. Cell 5: 557-567.
  7. Zhao Q, Modis Y, High K, Towne V, Meng Y, Wang Y, et al. 2012. Disassembly and reassembly of human papillomavirus virus-like particles produces more virion-like antibody reactivity. Virol. J. 9: 52.
  8. Buck CB, Day PM, Trus BL. 2013. The papillomavirus major capsid protein L1. Virology 445: 169-174.
  9. Hagensee ME, Yaegashi N, Galloway D. 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. Nooraei S, Bahrulolum H, Hoseini ZS, Katalani C, Hajizade A, Easton AJ, et al. 2021. Virus-like particles: preparation, immunogenicity and their roles as nanovaccines and drug nanocarriers. J. Nanobiotechnology 19: 59.
  11. Zeltins A. 2013. Construction and characterization of virus-like particles: a review. Mol. Biotechnol. 53: 92-107.
  12. Franco EL, Harper DM. 2005. Vaccination against human papillomavirus infection: a new paradigm in cervical cancer control. Vaccine 23: 2388-2394.
  13. Zaman R, Islam RA, Ibnat N, Othman I, Zaini A, Lee CY, et al. 2019. Current strategies in extending half-lives of therapeutic proteins. J. Control. Release 301: 176-189.
  14. Lim SI, Hahn YS, Kwon I. 2015. Site-specific albumination of a therapeutic protein with multi-subunit to prolong activity in vivo. J. Control. Release 207: 93-100.
  15. Yang B, Kwon I. 2021. Multivalent albumin-neonatal Fc receptor interactions mediate a prominent extension of the serum half-life of a therapeutic protein. Mol. Pharm. 18: 2397-2405.
  16. Dennis MS, Zhang M, Meng YG, Kadkhodayan M, Kirchhofer D, Combs D, et al. 2002. Albumin binding as a general strategy for improving the pharmacokinetics of proteins. J. Biol. Chem. 277: 35035-35043.
  17. Cho J, Lim SI, Yang BS, Hahn YS, Kwon I. 2017. Generation of therapeutic protein variants with the human serum albumin binding capacity via site-specific fatty acid conjugation. Sci. Rep. 7: 18041.
  18. Chin JW. 2017. Expanding and reprogramming the genetic code. Nature 550: 53-60.
  19. Shandell MA, Tan Z, Cornish VW. 2021. Genetic code expansion: a brief history and perspective. Biochemistry 60: 3455-3469.
  20. Wang N, Li Y, Niu W, Sun M, Cerny R, Li Q, et al. 2014. Construction of a live‐attenuated HIV‐1 vaccine through genetic code expansion. Angewandte Chemie 126: 4967-4971.
  21. Cho H, Daniel T, Buechler YJ, Litzinger DC, Maio Z, Putnam A-MH, et al. 2011. Optimized clinical performance of growth hormone with an expanded genetic code. Proc. Natl. Acad. Sci. USA 108: 9060-9065.
  22. Luo X, Zambaldo C, Liu T, Zhang Y, Xuan W, Wang C, et al. 2016. Recombinant thiopeptides containing noncanonical amino acids. Proc. Natl. Acad. Sci. USA 113: 3615-3620.
  23. Yao T, Zhou X, Zhang C, Yu X, Tian Z, Zhang L, et al. 2017. Site-specific PEGylated adeno-associated viruses with increased serum stability and reduced immunogenicity. Molecules 22: 1155.
  24. Zhang B, Xu H, Chen J, Zheng Y, Wu Y, Si L, et al. 2015. Development of next generation of therapeutic IFN-α2b via genetic code expansion. Acta Biomater. 19: 100-111.
  25. Wang L, Brock A, Herberich B, Schultz PG. 2001. Expanding the genetic code of Escherichia coli. Science 292: 498-500.
  26. Davis L, Chin JW. 2012. Designer proteins: applications of genetic code expansion in cell biology. Nat. Rev. Mol. Cell Biol. 13: 168-182.
  27. Young TS, Ahmad I, Yin JA, Schultz PG. 2010. An enhanced system for unnatural amino acid mutagenesis in E. coli. J. Mol. Biol. 395: 361-374.
  28. Kim J, Choi J-I. 2022. Expression of green fluorescence proteins with non-canonical amino acids in different Escherichia coli strains.
  29. Lee D, Kim MK, Choi JI. 2023. Development of orthogonal aminoacyl tRNA synthetase mutant with enhanced incorporation ability with para-azido-L-phenylalanine. Biotechnol. Bioprocess Eng. 28: 398-405.
  30. Bang HB, Lee YH, Lee YJ, Jeong KJ. 2016. High-level production of human papillomavirus (HPV) type 16 L1 in Escherichia coli. J. Microbiol.Biotechnol. 26: 356-363.
  31. Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, et al. 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596: 583-589.
  32. Delano WL. 2002. Pymol: an open-source molecular graphics tool. CCP4 Newsl. Protein Crystallogr. 40: 82-92.
  33. Wischke C, Borchert HH. 2006. Fluorescein isothiocyanate labelled bovine serum albumin (FITC-BSA) as a model protein drug:opportunities and drawbacks. Pharmazie 61: 770-774.
  34. Wei M, Wang D, Li Z, Song S, Kong X, Mo X, et al. 2018. N-terminal truncations on L1 proteins of human papillomaviruses promote their soluble expression in Escherichia coli and self-assembly in vitro. Emerg. Microbes Infect. 7: 160.
  35. Huang X, Wang X, Zhang J, Xia N, Zhao Q. 2017. Escherichia coli-derived virus-like particles in vaccine development. NPJ Vaccines 2: 3.
  36. Terpe K. 2006. Overview of bacterial expression systems for heterologous protein production: from molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol. 72: 211-222.
  37. Cho HJ, Sun Hahm M, Kuk Kim M, Han IK, Jung WW, Choi HG, et al. 2007. Expression, purification, and antibody binding activity of human papillomavirus 16 L1 protein fused to maltose binding protein. Protein Pept. Lett. 14: 417-424.
  38. Wang Q, Parrish AR, Wang L. 2009. Expanding the genetic code for biological studies. Chem. Biol. 16: 323-336.
  39. Liu CC, Schultz PG. 2010. Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79: 413-444.
  40. Lee D, Kim JG, Kim TW, Choi J. 2024. Development of orthogonal aminoacyl-tRNA synthetase mutant for incorporating a noncanonical amino acid. AMB Express 14: 60.
  41. Wang JW, Roden RB. 2013. Virus-like particles for the prevention of human papillomavirus-associated malignancies. Expert. Rev. Vaccines 12: 129-141.