Quantitative functionalization of biosynthetic caged protein materials

Quan Cheng, Xuan Wang, Xian-En Zhang, Chengchen Xu, Feng Li

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Quant. Biol. ›› 2023, Vol. 11 ›› Issue (1) : 1-14. DOI: 10.15302/J-QB-022-0306
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Quantitative functionalization of biosynthetic caged protein materials

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Abstract

Background: As one of the representative protein materials, protein nanocages (PNCs) are self-assembled supramolecular structures with multiple advantages, such as good monodispersity, biocompatibility, structural addressability, and facile production. Precise quantitative functionalization is essential to the construction of PNCs with designed purposes.

Results: With three modifiable interfaces, the interior surface, outer surface, and interfaces between building blocks, PNCs can serve as an ideal platform for precise multi-functionalization studies and applications. This review summarizes the currently available methods for precise quantitative functionalization of PNCs and highlights the significance of precise quantitative control in fabricating PNC-based materials or devices. These methods can be categorized into three groups, genetic, chemical, and combined modification.

Conclusion: This review would be constructive for those who work with biosynthetic PNCs in diverse fields.

Author summary

Protein nanocages (PNCs) are a group of self-assembling biomacromolecules that have been recognized as natural nanomaterials and are attracting increasing interest in multidisciplinary fields. Various strategies have been developed to modify and functionalize PNCs for tailored applications. This review aims to summarize the currently available methods for PNC modification with emphasis on the significance of quantitative control of functionalization.

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Keywords

protein nanocages / virus-like particles / functionalization / genetic modification / chemical modification

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Quan Cheng, Xuan Wang, Xian-En Zhang, Chengchen Xu, Feng Li. Quantitative functionalization of biosynthetic caged protein materials. Quant. Biol., 2023, 11(1): 1‒14 https://doi.org/10.15302/J-QB-022-0306

References

[1]
Li, F., Wang, D., Zhou, J., Men, D. Zhan, X. (2020). Design and biosynthesis of functional protein nanostructures. Sci. China Life Sci., 63: 1142–1158
CrossRef Google scholar
[2]
Nooraei, S., Bahrulolum, H., Hoseini, Z. S., Katalani, C., Hajizade, A., Easton, A. J. (2021). Virus-like particles: preparation, immunogenicity and their roles as nanovaccines and drug nanocarriers. J. Nanobiotechnology, 19: 59
CrossRef Google scholar
[3]
Divine, R., Dang, H. V., Ueda, G., Fallas, J. A., Vulovic, I., Sheffler, W., Saini, S., Zhao, Y. T., Raj, I. X., Morawski, P. A. . (2021). Designed proteins assemble antibodies into modular nanocages. Science, 372: abd9994
CrossRef Google scholar
[4]
Korpi, A., Anaya-Plaza, E., ki, S. (2020). Highly ordered protein cage assemblies: a toolkit for new materials. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 12: e1578
CrossRef Google scholar
[5]
Aoust, M. A., Couture, M. M., Charland, N., panier, S., Landry, N., Ors, F. zina, L. (2010). The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol. J., 8: 607–619
CrossRef Google scholar
[6]
Naskalska, A., cka-Solarz, K., ycki, J., Stupka, I., Bochenek, M., Pyza, E. Heddle, J. (2021). Artificial protein cage delivers active protein cargos to the cell interior. Biomacromolecules, 22: 4146–4154
CrossRef Google scholar
[7]
Williams, S. M. (2021). An overview of Dps: dual acting nanovehicles in prokaryotes with DNA binding and ferroxidation properties. Subcell. Biochem., 96: 177–216
CrossRef Google scholar
[8]
Aumiller, W. M., Uchida, M. (2018). Protein cage assembly across multiple length scales. Chem. Soc. Rev., 47: 3433–3469
CrossRef Google scholar
[9]
Uchida, M., McCoy, K., Fukuto, M., Yang, L., Yoshimura, H., Miettinen, H. M., LaFrance, B., Patterson, D. P., Schwarz, B., Karty, J. A. . (2018). Modular self-assembly of protein cage lattices for multistep catalysis. ACS Nano, 12: 942–953
CrossRef Google scholar
[10]
Raeeszadeh-Sarmazdeh, M., Hartzell, E., Price, J. V. (2016). Protein nanoparticles as multifunctional biocatalysts and health assessment sensors. Curr. Opin. Chem. Eng., 13: 109–118
CrossRef Google scholar
[11]
Lin, X., Xie, J., Niu, G., Zhang, F., Gao, H., Yang, M., Quan, Q., Aronova, M. A., Zhang, G., Lee, S. . (2011). Chimeric ferritin nanocages for multiple function loading and multimodal imaging. Nano Lett., 11: 814–819
CrossRef Google scholar
[12]
Molino, N. M. Wang, S. (2014). Caged protein nanoparticles for drug delivery. Curr. Opin. Biotechnol., 28: 75–82
CrossRef Google scholar
[13]
Moon, H., Lee, J., Kim, H., Heo, S., Min, J. (2014). Genetically engineering encapsulin protein cage nanoparticle as a SCC-7 cell targeting optical nanoprobe. Biomater. Res., 18: 21
CrossRef Google scholar
[14]
Hamby, S. E. Hirst, J. (2008). Prediction of glycosylation sites using random forests. BMC Bioinformatics, 9: 500
CrossRef Google scholar
[15]
Schwarzer, J., Rapp, E. (2008). N-glycan analysis by CGE-LIF: profiling influenza A virus hemagglutinin N-glycosylation during vaccine production. Electrophoresis, 29: 4203–4214
CrossRef Google scholar
[16]
Hyakumura, M., Walsh, R., Thaysen-Andersen, M., Kingston, N. J., La, M., Lu, L., Lovrecz, G., Packer, N. H., Locarnini, S. Netter, H. (2015). Modification of asparagine-linked glycan density for the design of hepatitis B virus virus-like particles with enhanced immunogenicity. J. Virol., 89: 11312–11322
CrossRef Google scholar
[17]
Joe, C. C. D., Chatterjee, S., Lovrecz, G., Adams, T. E., Thaysen-Andersen, M., Walsh, R., Locarnini, S. A., Smooker, P. Netter, H. (2020). Glycoengineered hepatitis B virus-like particles with enhanced immunogenicity. Vaccine, 38: 3892–3901
CrossRef Google scholar
[18]
De Filette, M., Min Jou, W., Birkett, A., Lyons, K., Schultz, B., Tonkyro, A., Resch, S. (2005). Universal influenza A vaccine: optimization of M2-based constructs. Virology, 337: 149–161
CrossRef Google scholar
[19]
Ling, S., Yang, S., Hu, X., Yin, D., Dai, Y., Qian, X., Wang, D., Pan, X., Hong, J., Sun, X. . (2021). Lentiviral delivery of co-packaged Cas9 mRNA and a Vegfa-targeting guide RNA prevents wet age-related macular degeneration in mice. Nat. Biomed. Eng., 5: 144–156
CrossRef Google scholar
[20]
Levasseur, M. D., Mantri, S., Hayashi, T., Reichenbach, M., Hehn, S., Waeckerle-Men, Y., Johansen, P. (2021). Cell-specific delivery using an engineered protein nanocage. ACS Chem. Biol., 16: 838–843
CrossRef Google scholar
[21]
Wang, Z., Zhao, Y., Zhang, S., Chen, X., Sun, G., Zhang, B., Jiang, B., Yang, Y., Yan, X. (2022). Re-engineering the inner surface of ferritin nanocage enables dual drug payloads for synergistic tumor therapy. Theranostics, 12: 1800–1815
CrossRef Google scholar
[22]
Martino, M. L., Crooke, S. N., Manchester, M. Finn, M. (2021). Single-point mutations in Qβ virus-like particles change binding to cells. Biomacromolecules, 22: 3332–3341
CrossRef Google scholar
[23]
Edwardson, T. G. W., Mori, T. (2018). Rational engineering of a designed protein cage for siRNA delivery. J. Am. Chem. Soc., 140: 10439–10442
CrossRef Google scholar
[24]
Patterson, D., Schwarz, B., Avera, J., Western, B., Hicks, M., Krugler, P., Terra, M., Uchida, M., McCoy, K. (2017). Sortase-mediated ligation as a modular approach for the covalent attachment of proteins to the exterior of the bacteriophage P22 virus-like particle. Bioconjug. Chem., 28: 2114–2124
CrossRef Google scholar
[25]
Peabody, D. (1997). Subunit fusion confers tolerance to peptide insertions in a virus coat protein. Arch. Biochem. Biophys., 347: 85–92
CrossRef Google scholar
[26]
Aanei, I. L., Huynh, T., Seo, Y. Francis, M. (2018). Vascular cell adhesion molecule-targeted MS2 viral capsids for the detection of early-stage atherosclerotic plaques. Bioconjug. Chem., 29: 2526–2530
CrossRef Google scholar
[27]
Tong, G. J., Hsiao, S. C., Carrico, Z. M. Francis, M. (2009). Viral capsid DNA aptamer conjugates as multivalent cell-targeting vehicles. J. Am. Chem. Soc., 131: 11174–11178
CrossRef Google scholar
[28]
Stephanopoulos, N., Tong, G. J., Hsiao, S. C. Francis, M. (2010). Dual-surface modified virus capsids for targeted delivery of photodynamic agents to cancer cells. ACS Nano, 4: 6014–6020
CrossRef Google scholar
[29]
Brauer, D. D., Hartman, E. C., Bader, D. L. V., Merz, Z. N., Tullman-Ercek, D. Francis, M. (2019). Systematic engineering of a protein nanocage for high-yield, site-specific modification. J. Am. Chem. Soc., 141: 3875–3884
CrossRef Google scholar
[30]
Karpenko, L. I., Ivanisenko, V. A., Pika, I. A., Chikaev, N. A., Eroshkin, A. M., Veremeiko, T. A. Ilyichev, A. (2000). Insertion of foreign epitopes in HBcAg: how to make the chimeric particle assemble. Amino Acids, 18: 329–337
CrossRef Google scholar
[31]
Takahashi, R. U., Kanesashi, S. N., Inoue, T., Enomoto, T., Kawano, M. A., Tsukamoto, H., Takeshita, F., Imai, T., Ochiya, T., Kataoka, K. . (2008). Presentation of functional foreign peptides on the surface of SV40 virus-like particles. J. Biotechnol., 135: 385–392
CrossRef Google scholar
[32]
Zhang, Y. L., Guo, Y. J., Wang, K. Y., Lu, K., Li, K., Zhu, Y. Sun, S. (2007). Enhanced immunogenicity of modified hepatitis B virus core particle fused with multiepitopes of foot-and-mouth disease virus. Scand. J. Immunol., 65: 320–328
CrossRef Google scholar
[33]
CalendarR.. (2006) The Bacteriophages. 2nd ed. 457−468. New York: Oxford University Press
[34]
Mao, H., Hart, S. A., Schink, A. Pollok, B. (2004). Sortase-mediated protein ligation: a new method for protein engineering. J. Am. Chem. Soc., 126: 2670–2671
CrossRef Google scholar
[35]
Schoonen, L., Pille, J., Borrmann, A., Nolte, R. J. van Hest, J. (2015). Sortase a-mediated N-terminal modification of cowpea chlorotic mottle virus for highly efficient cargo loading. Bioconjug. Chem., 26: 2429–2434
CrossRef Google scholar
[36]
Schoonen, L. van Hest, J. C. (2018). Modification of CCMV nanocages for enzyme encapsulation. Methods Mol. Biol., 1798: 69–83
CrossRef Google scholar
[37]
Keeble, A. H. (2020). Power to the protein: enhancing and combining activities using the Spy toolbox. Chem. Sci. (Camb.), 11: 7281–7291
CrossRef Google scholar
[38]
Sun, F. Zhang, W. (2017). Unleashing chemical power from protein sequence space toward genetically encoded “click” chemistry. Chin. Chem. Lett., 28: 2078–2084
CrossRef Google scholar
[39]
hl, P. M., Tissot, A. C., Fulurija, A., Maurer, P., Nussberger, J., Sabat, R., Nief, V., Schellekens, C., Sladko, K., Roubicek, K. . (2007). A vaccine for hypertension based on virus-like particles: preclinical efficacy and phase I safety and immunogenicity. J. Hypertens., 25: 63–72
CrossRef Google scholar
[40]
Jegerlehner, A., Storni, T., Lipowsky, G., Schmid, M., Pumpens, P. Bachmann, M. (2002). Regulation of IgG antibody responses by epitope density and CD21-mediated costimulation. Eur. J. Immunol., 32: 3305–3314
CrossRef Google scholar
[41]
Gautam, A., Beiss, V., Wang, C., Wang, L. Steinmetz, N. (2021). Plant viral nanoparticle conjugated with anti-PD-1 peptide for ovarian cancer immunotherapy. Int. J. Mol. Sci., 22: 9733
CrossRef Google scholar
[42]
Anand, P., Neil, A., Lin, E., Douglas, T. (2015). Tailored delivery of analgesic ziconotide across a blood brain barrier model using viral nanocontainers. Sci. Rep., 5: 12497
CrossRef Google scholar
[43]
Galaway, F. A. Stockley, P. (2013). MS2 viruslike particles: a robust, semisynthetic targeted drug delivery platform. Mol. Pharm., 10: 59–68
CrossRef Google scholar
[44]
Patel, K. G. Swartz, J. (2011). Surface functionalization of virus-like particles by direct conjugation using azide-alkyne click chemistry. Bioconjug. Chem., 22: 376–387
CrossRef Google scholar
[45]
Gillitzer, E., Suci, P., Young, M. (2006). Controlled ligand display on a symmetrical protein-cage architecture through mixed assembly. Small, 2: 962–966
CrossRef Google scholar
[46]
Brunel, F. M., Lewis, J. D., Destito, G., Steinmetz, N. F., Manchester, M., Stuhlmann, H. Dawson, P. (2010). Hydrazone ligation strategy to assemble multifunctional viral nanoparticles for cell imaging and tumor targeting. Nano Lett., 10: 1093–1097
CrossRef Google scholar
[47]
Li, Y., Hu, Y., Xiao, J., Liu, G., Li, X., Zhao, Y., Tan, H., Shi, H. (2016). Investigation of SP94 peptide as a specific probe for hepatocellular carcinoma imaging and Therapy. Sci. Rep., 6: 33511
CrossRef Google scholar
[48]
Nie, X., Liu, Y., Li, M., Yu, X., Yuan, W., Huang, S., Ren, D., Wang, Y. (2020). Sp94 peptide-functionalized PEG-PLGA nanoparticle loading with cryptotanshinone for targeting therapy of hepatocellular carcinoma. AAPS PharmSciTech, 21: 124
CrossRef Google scholar
[49]
Ashley, C. E., Carnes, E. C., Phillips, G. K., Durfee, P. N., Buley, M. D., Lino, C. A., Padilla, D. P., Phillips, B., Carter, M. B., Willman, C. L. . (2011). Cell-specific delivery of diverse cargos by bacteriophage MS2 virus-like particles. ACS Nano, 5: 5729–5745
CrossRef Google scholar
[50]
Gao, R., Tan, H., Li, S., Ma, S., Tang, Y., Zhang, K., Zhang, Z., Fan, Q., Yang, J., Zhang, X. E. . (2022). A prototype protein nanocage minimized from carboxysomes with gated oxygen permeability. Proc. Natl. Acad. Sci. USA, 119: 2104964119
CrossRef Google scholar
[51]
Li, F., Chen, Y., Chen, H., He, W., Zhang, Z. P., Zhang, X. E. (2011). Monofunctionalization of protein nanocages. J. Am. Chem. Soc., 133: 20040–20043
CrossRef Google scholar
[52]
Steinmetz, N. F., Hong, V., Spoerke, E. D., Lu, P., Breitenkamp, K., Finn, M. G. (2009). Buckyballs meet viral nanoparticles: candidates for biomedicine. J. Am. Chem. Soc., 131: 17093–17095
CrossRef Google scholar
[53]
Steinmetz, N. F., Lomonossoff, G. P. Evans, D. (2006). Cowpea mosaic virus for material fabrication: addressable carboxylate groups on a programmable nanoscaffold. Langmuir, 22: 3488–3490
CrossRef Google scholar
[54]
Aljabali, A. A., Shukla, S., Lomonossoff, G. P., Steinmetz, N. F. Evans, D. (2013). CPMV-DOX delivers. Mol. Pharm., 10: 3–10
CrossRef Google scholar
[55]
Koho, T., Ihalainen, T. O., Stark, M., Uusi-Kerttula, H., Wieneke, R., Rahikainen, R., Blazevic, V., ki, V., Kulomaa, M. S. . (2015). His-tagged norovirus-like particles: a versatile platform for cellular delivery and surface display. Eur. J. Pharm. Biopharm., 96: 22–31
CrossRef Google scholar
[56]
Meunier, S., Strable, E. Finn, M. (2004). Crosslinking of and coupling to viral capsid proteins by tyrosine oxidation. Chem. Biol., 11: 319–326
CrossRef Google scholar
[57]
Hooker, J. M., Datta, A., Botta, M., Raymond, K. N. Francis, M. (2007). Magnetic resonance contrast agents from viral capsid shells: a comparison of exterior and interior cargo strategies. Nano Lett., 7: 2207–2210
CrossRef Google scholar
[58]
Kovacs, E. W., Hooker, J. M., Romanini, D. W., Holder, P. G., Berry, K. E. Francis, M. (2007). Dual-surface-modified bacteriophage MS2 as an ideal scaffold for a viral capsid-based drug delivery system. Bioconjug. Chem., 18: 1140–1147
CrossRef Google scholar
[59]
Strable, E., Prasuhn, D. E. Udit, A. K., Brown, S., Link, A. J., Ngo, J. T., Lander, G., Quispe, J., Potter, C. S., Carragher, B. . (2008). Unnatural amino acid incorporation into virus-like particles. Bioconjug. Chem., 19: 866–875
CrossRef Google scholar
[60]
CrichtonR.. (2019) Biological inorganic chemistry. 3rd ed. 517−544. Cambridge: Academic Press
[61]
Douglas, T. Stark, V. (2000). Nanophase cobalt oxyhydroxide mineral synthesized within the protein cage of ferritin. Inorg. Chem., 39: 1828–1830
CrossRef Google scholar
[62]
Du, P., Liu, R., Sun, S., Dong, H., Zhao, R., Tang, R., Dai, J., Yin, H., Luo, J., Liu, Z. . (2019). Biomineralization improves the thermostability of foot-and-mouth disease virus-like particles and the protective immune response induced. Nanoscale, 11: 22748–22761
CrossRef Google scholar
[63]
Li, F., Zhang, Z. P., Peng, J., Cui, Z. Q., Pang, D. W., Li, K., Wei, H. P., Zhou, Y. F., Wen, J. K. Zhang, X. (2009). Imaging viral behavior in Mammalian cells with self-assembled capsid-quantum-dot hybrid particles. Small, 5: 718–726
CrossRef Google scholar
[64]
Li, F., Li, K., Cui, Z. Q., Zhang, Z. P., Wei, H. P., Gao, D., Deng, J. Y. Zhang, X. (2010). Viral coat proteins as flexible nano-building-blocks for nanoparticle encapsulation. Small, 6: 2301–2308
CrossRef Google scholar
[65]
rfer, B., Pianowski, Z. (2012). Efficient in vitro encapsulation of protein cargo by an engineered protein container. J. Am. Chem. Soc., 134: 909–911
CrossRef Google scholar
[66]
Tan, R. Frankel, A. (1995). Structural variety of arginine-rich RNA-binding peptides. Proc. Natl. Acad. Sci. USA., 92: 5282–5286
CrossRef Google scholar
[67]
Brasch, M., Putri, R. M., de Ruiter, M. V., Luque, D., Koay, M. S., Cornelissen, J. (2017). Assembling enzymatic cascade pathways inside virus-based nanocages using dual-tasking nucleic acid tags. J. Am. Chem. Soc., 139: 1512–1519
CrossRef Google scholar
[68]
Vervoort, D. F. M., Heiringhoff, R., Timmermans, S. B. P. E., van Stevendaal, M. H. M. E. van Hest, J. C. (2021). Dual site-selective presentation of functional handles on protein-engineered cowpea chlorotic mottle virus-like particles. Bioconjug. Chem., 32: 958–963
CrossRef Google scholar
[69]
Fang, T., Zhu, W., Li, C., Zhang, F., Gao, D., Zhang, Z. P., Liang, A., Zhang, X. E. (2019). Role of surface RGD patterns on protein nanocages in tumor targeting revealed using precise discrete models. Small, 15: e1904838
CrossRef Google scholar
[70]
Douglas, T., Strable, E., Willits, D., Aitouchen, A., Libera, M. (2002). Protein engineering of a viral cage for constrained nanomaterials synthesis. Adv. Mater., 14: 415–418
CrossRef Google scholar
[71]
Li, K., Zhang, Z. P., Luo, M., Yu, X., Han, Y., Wei, H. P., Cui, Z. Q. Zhang, X. (2012). Multifunctional ferritin cage nanostructures for fluorescence and MR imaging of tumor cells. Nanoscale, 4: 188–193
CrossRef Google scholar
[72]
Yang, M., Sunderland, K. (2017). Virus-derived peptides for clinical applications. Chem. Rev., 117: 10377–10402
CrossRef Google scholar
[73]
Gandra, N., Wang, D. D., Zhu, Y. (2013). Virus-mimetic cytoplasm-cleavable magnetic/silica nanoclusters for enhanced gene delivery to mesenchymal stem cells. Angew. Chem. Int. Ed. Engl., 52: 11278–11281
CrossRef Google scholar

ACKNOWLEDGEMENTS

This work was funded by the National Natural Science Foundation of China (Nos. 31771103 and 31800650), the Chinese Academy of Sciences (CAS) Emergency Project of African Swine Fever (ASF) Research (No. KJZD-SW-L06), Department of Education of Hubei Province (No. Q20221103), and Heath Commission of Hubei Province (No. WJ2021M214).

COMPLIANCE WITH ETHICS GUIDELINES

The authors Quan Cheng, Xuan Wang, Xian-En Zhang, Chengchen Xu and Feng Li declare that they have no conflict of interests.
This article is a review article and does not contain any studies with human or animal subjects performed by any of the authors.

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