|
|
|
Quantitative functionalization of biosynthetic caged protein materials |
Quan Cheng1,2, Xuan Wang1, Xian-En Zhang3,4,5, Chengchen Xu1( ), Feng Li2,5() |
1. College of Life Sciences and Health, Wuhan University of Science and Technology, Wuhan 430065, China
2. State Key Laboratory of Virology, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan 430071, China
3. Faculty of Synthetic Biology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
4. National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
5. University of Chinese Academy of Sciences, Beijing 100049, China |
|
|
|
|
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.
|
| Keywords
protein nanocages
virus-like particles
functionalization
genetic modification
chemical modification
|
|
Corresponding Author(s):
Chengchen Xu,Feng Li
|
|
Online First Date: 13 January 2023
Issue Date: 13 March 2023
|
|
| 1 |
F., Li, D., Wang, J., Zhou, D. Men, X. Zhan, (2020). Design and biosynthesis of functional protein nanostructures. Sci. China Life Sci., 63: 1142–1158
https://doi.org/10.1007/s11427-019-1641-6
|
| 2 |
S., Nooraei, H., Bahrulolum, Z. S., Hoseini, C., Katalani, A., Hajizade, A. J. Easton, (2021). Virus-like particles: preparation, immunogenicity and their roles as nanovaccines and drug nanocarriers. J. Nanobiotechnology, 19: 59
https://doi.org/10.1186/s12951-021-00806-7
|
| 3 |
R., Divine, H. V., Dang, G., Ueda, J. A., Fallas, I., Vulovic, W., Sheffler, S., Saini, Y. T., Zhao, I. X., Raj, P. A. Morawski, et al.. (2021). Designed proteins assemble antibodies into modular nanocages. Science, 372: abd9994
https://doi.org/10.1126/science.abd9994
|
| 4 |
A., Korpi, E., Anaya-Plaza, S. ki, (2020). Highly ordered protein cage assemblies: a toolkit for new materials. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 12: e1578
https://doi.org/10.1002/wnan.1578
|
| 5 |
M. A., Aoust, M. M., Couture, N., Charland, S., panier, N., Landry, F. Ors, L. zina, (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
https://doi.org/10.1111/j.1467-7652.2009.00496.x
|
| 6 |
A., Naskalska, K., cka-Solarz, J., ycki, I., Stupka, M., Bochenek, E. Pyza, J. Heddle, (2021). Artificial protein cage delivers active protein cargos to the cell interior. Biomacromolecules, 22: 4146–4154
https://doi.org/10.1021/acs.biomac.1c00630
|
| 7 |
S. M. Williams, (2021). An overview of Dps: dual acting nanovehicles in prokaryotes with DNA binding and ferroxidation properties. Subcell. Biochem., 96: 177–216
https://doi.org/10.1007/978-3-030-58971-4_3
|
| 8 |
W. M., Aumiller, M. Uchida, (2018). Protein cage assembly across multiple length scales. Chem. Soc. Rev., 47: 3433–3469
https://doi.org/10.1039/C7CS00818J
|
| 9 |
M., Uchida, K., McCoy, M., Fukuto, L., Yang, H., Yoshimura, H. M., Miettinen, B., LaFrance, D. P., Patterson, B., Schwarz, J. A. Karty, et al.. (2018). Modular self-assembly of protein cage lattices for multistep catalysis. ACS Nano, 12: 942–953
https://doi.org/10.1021/acsnano.7b06049
|
| 10 |
M., Raeeszadeh-Sarmazdeh, E., Hartzell, J. V. Price, (2016). Protein nanoparticles as multifunctional biocatalysts and health assessment sensors. Curr. Opin. Chem. Eng., 13: 109–118
https://doi.org/10.1016/j.coche.2016.08.016
|
| 11 |
X., Lin, J., Xie, G., Niu, F., Zhang, H., Gao, M., Yang, Q., Quan, M. A., Aronova, G., Zhang, S. Lee, et al.. (2011). Chimeric ferritin nanocages for multiple function loading and multimodal imaging. Nano Lett., 11: 814–819
https://doi.org/10.1021/nl104141g
|
| 12 |
N. M. Molino, S. Wang, (2014). Caged protein nanoparticles for drug delivery. Curr. Opin. Biotechnol., 28: 75–82
https://doi.org/10.1016/j.copbio.2013.12.007
|
| 13 |
H., Moon, J., Lee, H., Kim, S., Heo, J. Min, (2014). Genetically engineering encapsulin protein cage nanoparticle as a SCC-7 cell targeting optical nanoprobe. Biomater. Res., 18: 21
https://doi.org/10.1186/2055-7124-18-21
|
| 14 |
S. E. Hamby, J. Hirst, (2008). Prediction of glycosylation sites using random forests. BMC Bioinformatics, 9: 500
https://doi.org/10.1186/1471-2105-9-500
|
| 15 |
J., Schwarzer, E. Rapp, (2008). N-glycan analysis by CGE-LIF: profiling influenza A virus hemagglutinin N-glycosylation during vaccine production. Electrophoresis, 29: 4203–4214
https://doi.org/10.1002/elps.200800042
|
| 16 |
M., Hyakumura, R., Walsh, M., Thaysen-Andersen, N. J., Kingston, M., La, L., Lu, G., Lovrecz, N. H., Packer, S. Locarnini, H. Netter, (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
https://doi.org/10.1128/JVI.01123-15
|
| 17 |
C. C. D., Joe, S., Chatterjee, G., Lovrecz, T. E., Adams, M., Thaysen-Andersen, R., Walsh, S. A., Locarnini, P. Smooker, H. Netter, (2020). Glycoengineered hepatitis B virus-like particles with enhanced immunogenicity. Vaccine, 38: 3892–3901
https://doi.org/10.1016/j.vaccine.2020.03.007
|
| 18 |
M., De Filette, W., Min Jou, A., Birkett, K., Lyons, B., Schultz, A., Tonkyro, S. Resch, (2005). Universal influenza A vaccine: optimization of M2-based constructs. Virology, 337: 149–161
https://doi.org/10.1016/j.virol.2005.04.004
|
| 19 |
S., Ling, S., Yang, X., Hu, D., Yin, Y., Dai, X., Qian, D., Wang, X., Pan, J., Hong, X. Sun, et al.. (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
https://doi.org/10.1038/s41551-020-00656-y
|
| 20 |
M. D., Levasseur, S., Mantri, T., Hayashi, M., Reichenbach, S., Hehn, Y., Waeckerle-Men, P. Johansen, (2021). Cell-specific delivery using an engineered protein nanocage. ACS Chem. Biol., 16: 838–843
https://doi.org/10.1021/acschembio.1c00007
|
| 21 |
Z., Wang, Y., Zhao, S., Zhang, X., Chen, G., Sun, B., Zhang, B., Jiang, Y., Yang, X. Yan, (2022). Re-engineering the inner surface of ferritin nanocage enables dual drug payloads for synergistic tumor therapy. Theranostics, 12: 1800–1815
https://doi.org/10.7150/thno.68459
|
| 22 |
M. L., Martino, S. N., Crooke, M. Manchester, M. Finn, (2021). Single-point mutations in Qβ virus-like particles change binding to cells. Biomacromolecules, 22: 3332–3341
https://doi.org/10.1021/acs.biomac.1c00443
|
| 23 |
T. G. W., Edwardson, T. Mori, (2018). Rational engineering of a designed protein cage for siRNA delivery. J. Am. Chem. Soc., 140: 10439–10442
https://doi.org/10.1021/jacs.8b06442
|
| 24 |
D., Patterson, B., Schwarz, J., Avera, B., Western, M., Hicks, P., Krugler, M., Terra, M., Uchida, K. McCoy, (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
https://doi.org/10.1021/acs.bioconjchem.7b00296
|
| 25 |
D. Peabody, (1997). Subunit fusion confers tolerance to peptide insertions in a virus coat protein. Arch. Biochem. Biophys., 347: 85–92
https://doi.org/10.1006/abbi.1997.0312
|
| 26 |
I. L., Aanei, T., Huynh, Y. Seo, M. Francis, (2018). Vascular cell adhesion molecule-targeted MS2 viral capsids for the detection of early-stage atherosclerotic plaques. Bioconjug. Chem., 29: 2526–2530
https://doi.org/10.1021/acs.bioconjchem.8b00453
|
| 27 |
G. J., Tong, S. C., Hsiao, Z. M. Carrico, M. Francis, (2009). Viral capsid DNA aptamer conjugates as multivalent cell-targeting vehicles. J. Am. Chem. Soc., 131: 11174–11178
https://doi.org/10.1021/ja903857f
|
| 28 |
N., Stephanopoulos, G. J., Tong, S. C. Hsiao, M. Francis, (2010). Dual-surface modified virus capsids for targeted delivery of photodynamic agents to cancer cells. ACS Nano, 4: 6014–6020
https://doi.org/10.1021/nn1014769
|
| 29 |
D. D., Brauer, E. C., Hartman, D. L. V., Bader, Z. N., Merz, D. Tullman-Ercek, M. Francis, (2019). Systematic engineering of a protein nanocage for high-yield, site-specific modification. J. Am. Chem. Soc., 141: 3875–3884
https://doi.org/10.1021/jacs.8b10734
|
| 30 |
L. I., Karpenko, V. A., Ivanisenko, I. A., Pika, N. A., Chikaev, A. M., Eroshkin, T. A. Veremeiko, A. Ilyichev, (2000). Insertion of foreign epitopes in HBcAg: how to make the chimeric particle assemble. Amino Acids, 18: 329–337
https://doi.org/10.1007/s007260070072
|
| 31 |
R. U., Takahashi, S. N., Kanesashi, T., Inoue, T., Enomoto, M. A., Kawano, H., Tsukamoto, F., Takeshita, T., Imai, T., Ochiya, K. Kataoka, et al.. (2008). Presentation of functional foreign peptides on the surface of SV40 virus-like particles. J. Biotechnol., 135: 385–392
https://doi.org/10.1016/j.jbiotec.2008.05.012
|
| 32 |
Y. L., Zhang, Y. J., Guo, K. Y., Wang, K., Lu, K., Li, Y. Zhu, S. Sun, (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
https://doi.org/10.1111/j.1365-3083.2007.01900.x
|
| 33 |
R. Calendar. (2006) The Bacteriophages. 2nd ed. 457−468. New York: Oxford University Press
|
| 34 |
H., Mao, S. A., Hart, A. Schink, B. Pollok, (2004). Sortase-mediated protein ligation: a new method for protein engineering. J. Am. Chem. Soc., 126: 2670–2671
https://doi.org/10.1021/ja039915e
|
| 35 |
L., Schoonen, J., Pille, A., Borrmann, R. J. Nolte, J. van Hest, (2015). Sortase a-mediated N-terminal modification of cowpea chlorotic mottle virus for highly efficient cargo loading. Bioconjug. Chem., 26: 2429–2434
https://doi.org/10.1021/acs.bioconjchem.5b00485
|
| 36 |
L. Schoonen, J. C. van Hest, (2018). Modification of CCMV nanocages for enzyme encapsulation. Methods Mol. Biol., 1798: 69–83
https://doi.org/10.1007/978-1-4939-7893-9_6
|
| 37 |
A. H. Keeble, (2020). Power to the protein: enhancing and combining activities using the Spy toolbox. Chem. Sci. (Camb.), 11: 7281–7291
https://doi.org/10.1039/D0SC01878C
|
| 38 |
F. Sun, W. Zhang, (2017). Unleashing chemical power from protein sequence space toward genetically encoded “click” chemistry. Chin. Chem. Lett., 28: 2078–2084
https://doi.org/10.1016/j.cclet.2017.08.052
|
| 39 |
P. M., hl, A. C., Tissot, A., Fulurija, P., Maurer, J., Nussberger, R., Sabat, V., Nief, C., Schellekens, K., Sladko, K. Roubicek, et al.. (2007). A vaccine for hypertension based on virus-like particles: preclinical efficacy and phase I safety and immunogenicity. J. Hypertens., 25: 63–72
https://doi.org/10.1097/HJH.0b013e32800ff5d6
|
| 40 |
A., Jegerlehner, T., Storni, G., Lipowsky, M., Schmid, P. Pumpens, M. Bachmann, (2002). Regulation of IgG antibody responses by epitope density and CD21-mediated costimulation. Eur. J. Immunol., 32: 3305–3314
https://doi.org/10.1002/1521-4141(200211)32:11<3305::AID-IMMU3305>3.0.CO;2-J
|
| 41 |
A., Gautam, V., Beiss, C., Wang, L. Wang, N. Steinmetz, (2021). Plant viral nanoparticle conjugated with anti-PD-1 peptide for ovarian cancer immunotherapy. Int. J. Mol. Sci., 22: 9733
https://doi.org/10.3390/ijms22189733
|
| 42 |
P., Anand, A., Neil, E., Lin, T. Douglas, (2015). Tailored delivery of analgesic ziconotide across a blood brain barrier model using viral nanocontainers. Sci. Rep., 5: 12497
https://doi.org/10.1038/srep12497
|
| 43 |
F. A. Galaway, P. Stockley, (2013). MS2 viruslike particles: a robust, semisynthetic targeted drug delivery platform. Mol. Pharm., 10: 59–68
https://doi.org/10.1021/mp3003368
|
| 44 |
K. G. Patel, J. Swartz, (2011). Surface functionalization of virus-like particles by direct conjugation using azide-alkyne click chemistry. Bioconjug. Chem., 22: 376–387
https://doi.org/10.1021/bc100367u
|
| 45 |
E., Gillitzer, P., Suci, M. Young, (2006). Controlled ligand display on a symmetrical protein-cage architecture through mixed assembly. Small, 2: 962–966
https://doi.org/10.1002/smll.200500433
|
| 46 |
F. M., Brunel, J. D., Lewis, G., Destito, N. F., Steinmetz, M., Manchester, H. Stuhlmann, P. Dawson, (2010). Hydrazone ligation strategy to assemble multifunctional viral nanoparticles for cell imaging and tumor targeting. Nano Lett., 10: 1093–1097
https://doi.org/10.1021/nl1002526
|
| 47 |
Y., Li, Y., Hu, J., Xiao, G., Liu, X., Li, Y., Zhao, H., Tan, H. Shi, (2016). Investigation of SP94 peptide as a specific probe for hepatocellular carcinoma imaging and Therapy. Sci. Rep., 6: 33511
https://doi.org/10.1038/srep33511
|
| 48 |
X., Nie, Y., Liu, M., Li, X., Yu, W., Yuan, S., Huang, D., Ren, Y. Wang, (2020). Sp94 peptide-functionalized PEG-PLGA nanoparticle loading with cryptotanshinone for targeting therapy of hepatocellular carcinoma. AAPS PharmSciTech, 21: 124
https://doi.org/10.1208/s12249-020-01655-7
|
| 49 |
C. E., Ashley, E. C., Carnes, G. K., Phillips, P. N., Durfee, M. D., Buley, C. A., Lino, D. P., Padilla, B., Phillips, M. B., Carter, C. L. Willman, et al.. (2011). Cell-specific delivery of diverse cargos by bacteriophage MS2 virus-like particles. ACS Nano, 5: 5729–5745
https://doi.org/10.1021/nn201397z
|
| 50 |
R., Gao, H., Tan, S., Li, S., Ma, Y., Tang, K., Zhang, Z., Zhang, Q., Fan, J., Yang, X. E. Zhang, et al.. (2022). A prototype protein nanocage minimized from carboxysomes with gated oxygen permeability. Proc. Natl. Acad. Sci. USA, 119: 2104964119
https://doi.org/10.1073/pnas.2104964119
|
| 51 |
F., Li, Y., Chen, H., Chen, W., He, Z. P., Zhang, X. E. Zhang, (2011). Monofunctionalization of protein nanocages. J. Am. Chem. Soc., 133: 20040–20043
https://doi.org/10.1021/ja207276g
|
| 52 |
N. F., Steinmetz, V., Hong, E. D., Spoerke, P., Lu, K., Breitenkamp, M. G. Finn, (2009). Buckyballs meet viral nanoparticles: candidates for biomedicine. J. Am. Chem. Soc., 131: 17093–17095
https://doi.org/10.1021/ja902293w
|
| 53 |
N. F., Steinmetz, G. P. Lomonossoff, D. Evans, (2006). Cowpea mosaic virus for material fabrication: addressable carboxylate groups on a programmable nanoscaffold. Langmuir, 22: 3488–3490
https://doi.org/10.1021/la060078e
|
| 54 |
A. A., Aljabali, S., Shukla, G. P., Lomonossoff, N. F. Steinmetz, D. Evans, (2013). CPMV-DOX delivers. Mol. Pharm., 10: 3–10
https://doi.org/10.1021/mp3002057
|
| 55 |
T., Koho, T. O., Ihalainen, M., Stark, H., Uusi-Kerttula, R., Wieneke, R., Rahikainen, V., Blazevic, V., ki, M. S. Kulomaa, et al.. (2015). His-tagged norovirus-like particles: a versatile platform for cellular delivery and surface display. Eur. J. Pharm. Biopharm., 96: 22–31
https://doi.org/10.1016/j.ejpb.2015.07.002
|
| 56 |
S., Meunier, E. Strable, M. Finn, (2004). Crosslinking of and coupling to viral capsid proteins by tyrosine oxidation. Chem. Biol., 11: 319–326
https://doi.org/10.1016/j.chembiol.2004.02.019
|
| 57 |
J. M., Hooker, A., Datta, M., Botta, K. N. Raymond, M. Francis, (2007). Magnetic resonance contrast agents from viral capsid shells: a comparison of exterior and interior cargo strategies. Nano Lett., 7: 2207–2210
https://doi.org/10.1021/nl070512c
|
| 58 |
E. W., Kovacs, J. M., Hooker, D. W., Romanini, P. G., Holder, K. E. Berry, M. Francis, (2007). Dual-surface-modified bacteriophage MS2 as an ideal scaffold for a viral capsid-based drug delivery system. Bioconjug. Chem., 18: 1140–1147
https://doi.org/10.1021/bc070006e
|
| 59 |
E., Strable, D. E. Prasuhn, A. K., Udit, S., Brown, A. J., Link, J. T., Ngo, G., Lander, J., Quispe, C. S., Potter, B. Carragher, et al.. (2008). Unnatural amino acid incorporation into virus-like particles. Bioconjug. Chem., 19: 866–875
https://doi.org/10.1021/bc700390r
|
| 60 |
R. Crichton. (2019) Biological inorganic chemistry. 3rd ed. 517−544. Cambridge: Academic Press
|
| 61 |
T. Douglas, V. Stark, (2000). Nanophase cobalt oxyhydroxide mineral synthesized within the protein cage of ferritin. Inorg. Chem., 39: 1828–1830
https://doi.org/10.1021/ic991269q
|
| 62 |
P., Du, R., Liu, S., Sun, H., Dong, R., Zhao, R., Tang, J., Dai, H., Yin, J., Luo, Z. Liu, et al.. (2019). Biomineralization improves the thermostability of foot-and-mouth disease virus-like particles and the protective immune response induced. Nanoscale, 11: 22748–22761
https://doi.org/10.1039/C9NR05549E
|
| 63 |
F., Li, Z. P., Zhang, J., Peng, Z. Q., Cui, D. W., Pang, K., Li, H. P., Wei, Y. F., Zhou, J. K. Wen, X. Zhang, (2009). Imaging viral behavior in Mammalian cells with self-assembled capsid-quantum-dot hybrid particles. Small, 5: 718–726
https://doi.org/10.1002/smll.200801303
|
| 64 |
F., Li, K., Li, Z. Q., Cui, Z. P., Zhang, H. P., Wei, D., Gao, J. Y. Deng, X. Zhang, (2010). Viral coat proteins as flexible nano-building-blocks for nanoparticle encapsulation. Small, 6: 2301–2308
https://doi.org/10.1002/smll.201001078
|
| 65 |
B., rfer, Z. Pianowski, (2012). Efficient in vitro encapsulation of protein cargo by an engineered protein container. J. Am. Chem. Soc., 134: 909–911
https://doi.org/10.1021/ja211011k
|
| 66 |
R. Tan, A. Frankel, (1995). Structural variety of arginine-rich RNA-binding peptides. Proc. Natl. Acad. Sci. USA., 92: 5282–5286
https://doi.org/10.1073/pnas.92.12.5282
|
| 67 |
M., Brasch, R. M., Putri, M. V., de Ruiter, D., Luque, M. S., Koay, J. Cornelissen, (2017). Assembling enzymatic cascade pathways inside virus-based nanocages using dual-tasking nucleic acid tags. J. Am. Chem. Soc., 139: 1512–1519
https://doi.org/10.1021/jacs.6b10948
|
| 68 |
D. F. M., Vervoort, R., Heiringhoff, S. B. P. E., Timmermans, M. H. M. E. van Stevendaal, J. C. van Hest, (2021). Dual site-selective presentation of functional handles on protein-engineered cowpea chlorotic mottle virus-like particles. Bioconjug. Chem., 32: 958–963
https://doi.org/10.1021/acs.bioconjchem.1c00108
|
| 69 |
T., Fang, W., Zhu, C., Li, F., Zhang, D., Gao, Z. P., Zhang, A., Liang, X. E. Zhang, (2019). Role of surface RGD patterns on protein nanocages in tumor targeting revealed using precise discrete models. Small, 15: e1904838
https://doi.org/10.1002/smll.201904838
|
| 70 |
T., Douglas, E., Strable, D., Willits, A., Aitouchen, M. Libera, (2002). Protein engineering of a viral cage for constrained nanomaterials synthesis. Adv. Mater., 14: 415–418
https://doi.org/10.1002/1521-4095(20020318)14:6<415::AID-ADMA415>3.0.CO;2-W
|
| 71 |
K., Li, Z. P., Zhang, M., Luo, X., Yu, Y., Han, H. P., Wei, Z. Q. Cui, X. Zhang, (2012). Multifunctional ferritin cage nanostructures for fluorescence and MR imaging of tumor cells. Nanoscale, 4: 188–193
https://doi.org/10.1039/C1NR11132A
|
| 72 |
M., Yang, K. Sunderland, (2017). Virus-derived peptides for clinical applications. Chem. Rev., 117: 10377–10402
https://doi.org/10.1021/acs.chemrev.7b00100
|
| 73 |
N., Gandra, D. D., Wang, Y. Zhu, (2013). Virus-mimetic cytoplasm-cleavable magnetic/silica nanoclusters for enhanced gene delivery to mesenchymal stem cells. Angew. Chem. Int. Ed. Engl., 52: 11278–11281
https://doi.org/10.1002/anie.201301113
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
