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The Development of Bioadhesives Based on Recombinant Analogues of Spider Web Proteins

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Abstract

It has been shown that recombinant spidroins rS1/9 and rS2/12 that we previously developed exhibit adhesive properties with respect to both inorganic and organic substrates. It is well known that the adhesive properties of mussel foot proteins are associated with the level of DOPA, which is formed as a result of the post-translational modification of tyrosine residues by the tyrosinase enzyme. Therefore, we used recombinant tyrosinase for in vitro modification of tyrosine residues in the recombinant rS1/9 and rS2/12 spidroins to increase their adhesion capacity. As expected, the conversion of tyrosine residues into DOPA led to an increase in the adhesion properties of these proteins, which was demonstrated in experiments on gluing plates of polyvinyl chloride, aluminum, polylactic acid, and tubular pork bone. The molecules of recombinant spidroins retained their inherent properties to form supramolecular structures, hydrogels (microgels), transparent films, and 3D matrices. Interestingly, tyrosinase-modified proteins exhibited increased cohesion in experiments on bonding different materials in the presence of water.

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REFERENCES

  1. Danner, E.W., Kan,Y., Hammer, M.U., et al., Adhesion of mussel foot protein Mefp-5 to mica: an underwater superglue, Biochemistry, 2012, vol. 51, no. 33, pp. 6511–6518. https://doi.org/10.1021/bi3002538

    Article  CAS  Google Scholar 

  2. Waite, J.H. and Tanzer, M.L., Polyphenolic substance of Mytilus edulis: novel adhesive containing L-dopa and hydroxyproline, Science, 1981, vol. 212, no. 4498, pp. 1038–1040. https://doi.org/10.1126/science.212.4498.1038

    Article  CAS  Google Scholar 

  3. Catron, N.D., Lee, H., and Messersmith, P.B., Enhancement of poly(ethylene glycol) mucoadsorption by biomimetic end group functionalization, Biointerphases, 2006, vol. 1, no. 4, pp. 134–141. https://doi.org/10.1116/1.2422894

    Article  CAS  Google Scholar 

  4. Chirdon, W.M., O’Brien, W.J., and Robertson, R.E., Adsorption of catechol and comparative solutes on hydroxyapatite, J. Biomed. Mater. Res., 2003, vol. 66B, no. 2, pp. 532–538. https://doi.org/10.1002/jbm.b.10041

    Article  CAS  Google Scholar 

  5. Waiter, J.H., Reverse engineering of bioadhesion in marine mussels, Ann. N.Y. Acad. Sci., 1999, vol. 875, no. 1, pp. 301–309. https://doi.org/10.1111/j.1749-6632.1999.tb08513.x

    Article  Google Scholar 

  6. Lu, Q., Oh, D.X., Lee, Y., et al., Nanomechanics of cation-π interactions in aqueous solution, Angew. Chem. Int. Ed., 2013, vol. 52, no. 14, pp. 3944–3948. https://doi.org/10.1002/anie.201210365

    Article  CAS  Google Scholar 

  7. Sever, M.J. and Wilker, J.J., Absorption spectroscopy and binding constants for first-row transition metal complexes of a DOPA-containing peptide, Dalton Trans., 2006, vol. 6, pp. 813–822. https://doi.org/10.1039/b509586g

    Article  CAS  Google Scholar 

  8. Lee, B.P., Chao, C.-Y., Nunalee, F.N., et al., Rapid gel formation and adhesion in photocurable and biodegradable block copolymers with high DOPA content, Macromolecules, 2006, vol. 39, no. 5, pp. 1740–1748. https://doi.org/10.1021/ma0518959

    Article  CAS  Google Scholar 

  9. Dalsin, J.L., Lin, L., Tosatti, S., et al., Protein resistance of titanium oxide surfaces modified by biologically inspired mPEG-DOPA, Langmuir, 2005, vol. 21, pp. 640–646. https://doi.org/10.1021/la048626g

    Article  CAS  Google Scholar 

  10. Bogush, V.G., Sokolova, O.S., Davydova, L.I., et al., A novel model system for design of biomaterials, based on recombinant analogs of spider silk protein, J. Neuroimmune Pharmacol., 2009, vol. 4, no. 1, pp. 17–27. https://www.ncbi.nlm.nih.gov/pubmed/18839314.

    Article  Google Scholar 

  11. Nosenko, M.A., Moysenovich, A.M., Zvartsev, R.V., et al., Novel biodegradable polymeric microparticles facilitate scarless wound healing by promoting re-epithelialization and inhibiting fibrosis, Front. Immunol., 2018, vol. 4, no. 9, p. 2851. https://doi.org/10.3389/fimmu.2018.02851

    Article  CAS  Google Scholar 

  12. Baklaushev, V.P., Bogush, V.G., Kalsin, V.A., et al., Tissue engineered neural constructs composed of neural precursor cells, recombinant spidroin and PRP for neural tissue regeneration, Sci. Rep., 2019, vol. 9, no. 1, pp. 3161–3169. https://doi.org/10.1038/s41598-019-39341-9

    Article  CAS  Google Scholar 

  13. Moysenovich, A.M., Moisenovich, M.M., Sudina, A.K., et al., Recombinant spidroin films attenuate individual markers of glucose induced aging in NIH 3T3 fibroblasts, Biochemistry (Moscow), 2020, vol. 85, no. 7, pp. 808–819. https://doi.org/10.1134/S0006297920070093

    Article  CAS  Google Scholar 

  14. Moisenovich, M.M., Silachev, D.N., Moysenovich, A.M., et al., Effects of recombinant spidroin rS1/9 on brain neural progenitors after photothrombosis-induced ischemia, Front. Cell Dev. Biol., 2020, vol. 8, p. 823. https://doi.org/10.3389/fcell.2020.00823

    Article  Google Scholar 

  15. Aksambayeva, A.S., Zhaparova, L.R., Shagyrova, Zh.S., et al., Recombinant tyrosinase from Verrucomicrobium spinosum: isolation, characteristics and use for production of protein with adhesive properties, Biotekhnologiya, 2017, vol. 33, no. 6, pp. 12–27. https://doi.org/10.21519/0234-2758-2017-33-6-12-27

    Article  Google Scholar 

  16. Sidoruk, K.V., Davydova, L.I., Kozlov, D.G., et al., Fermentation optimization of a Saccharomyces cerevisiae strain producing 1F9 recombinant spidroin, Appl. Biochem. Microbiol., 2015, vol. 51, no. 7, pp. 766–773. https://doi.org/10.1134/S0003683815070066

    Article  CAS  Google Scholar 

  17. Issopoulos, P.B., Sensitive colorimetric assay of carbidopa and methyldopa using tetrazolium blue chloride in pharmaceutical products, Pharm. Weekbl. Sci., 1989, vol. 11, no. 6, pp. 213–217. https://doi.org/10.1007/BF01959413

    Article  CAS  Google Scholar 

  18. Lancaster, J.F., The use of adhesives for making structural joints, in Metallurgy of Welding, Woodhead Publishing, 1999, 6th ed., vols. 54–84. https://doi.org/10.1533/9781845694869.54

  19. https://web.expasy.org/cgi-bin/protparam/protparam.

  20. Bagrov, D.V., Prokhorov, V.V., Klinov, D.V., Agapov, I.I., et al., A study of lamellas of the web recombinant protein by atomic force microscopy, Biophysics (Moscow), 2011, vol. 56, no. 1, pp. 7–12. PMID: .21442880

    Article  CAS  Google Scholar 

  21. Antonenko, Yu.N., Perevoshchikova, I.V., Davydova, L.I., et al., Interaction of recombinant analogs of spider silk proteins 1F9 and 2E12 with phospholipid membranes, Biochim. Biophys. Acta, 2010, vol. 1798, no. 6, pp. 1172–1178. https://www.ncbi.nlm.nih.gov/pubmed/20214876.

    Article  CAS  Google Scholar 

  22. Sokolova, O.S., Bogush, V.G., Davydova, L.I., et al., The formation of a quaternary structure by recombinant analogs of spider silk proteins, Mol. Biol. (Moscow), 2010, vol. 44, no. 1, pp. 150–157. https://doi.org/10.1134/S0026893310010188

    Article  CAS  Google Scholar 

  23. Rising, A., Nimmervoll, H., Grip, S., et al., Spider silk proteins—mechanical property and gene sequence, Zool. Sci., 2005, vol. 22, pp. 273–281. https://doi.org/10.2108/zsj.22.273

    Article  CAS  Google Scholar 

  24. Harris, T.I., Gaztambide, D.A., Day, B.A., et al., Sticky situation: an investigation of robust aqueous-based recombinant spider silk protein coatings and adhesives, Biomacromolecules, 2016, vol. 17, no. 11, pp. 3761–3772. https://doi.org/10.1021/acs.biomac.6b01267

    Article  CAS  Google Scholar 

  25. Aich, P., An, J., Yang, B., et al., Self-assembled adhesive biomaterials formed by a genetically designed fusion protein, Chem. Commun. (Cambr.), 2018, vol. 54, pp. 12642–12645. https://doi.org/10.1039/c8cc07475e

    Article  CAS  Google Scholar 

  26. Mason, H.S., Oxidases, Annu. Rev. Biochem., 1965, vol. 34, pp. 595–634. https://doi.org/10.1146/annurev.bi.34.070165.003115

    Article  CAS  Google Scholar 

  27. Lee, B.P., Dalsin, J.L., and Messersmith, P.B., Synthesis and gelation of DOPA-modified poly(ethylene glycol) hydrogels, Biomacromolecules, 2002, vol. 3, no. 5, pp. 1038–1047. https://doi.org/10.1021/bm025546n

    Article  CAS  Google Scholar 

  28. Yu J., Wei W., Menyo M.S., et al. Adhesion of mussel foot protein-3 to TiO2 surfaces: the effect of pH, Biomacromolecules, 2013, vol. 14, no. 4, pp. 1072–1077. https://doi.org/10.1021/bm301908y

    Article  CAS  Google Scholar 

  29. Sogawa, H., Ifuku, N., and Numata, K., 3,4-Dihydroxyphenylalanine (DOPA)-containing silk fibroin: its enzymatic synthesis and adhesion properties, ACS Biomater. Sci. Eng., 2019, vol. 5, no. 11, pp. 5644–5651. https://doi.org/10.1021/acsbiomaterials.8b01309

    Article  CAS  Google Scholar 

  30. Roberts, A.D., Finnigan, W., Kelly, P.P., et al., Non-covalent protein-based adhesives for transparent substrates – bovine serum albumin vs. recombinant spider silk, Mater. Today Bio, 2020, vol. 7, p. 100068. https://doi.org/10.1016/j.mtbio.2020.100068

    Article  CAS  Google Scholar 

  31. Cheng, P.-N., Pham, J.D, and Nowick, J.S., The supramolecular chemistry of β-sheets, J. Am. Chem. Soc., 2013, vol. 135, pp. 5477–5492. https://doi.org/10.1021/ja3088407

    Article  CAS  Google Scholar 

  32. Forooshani, P.K. and Lee, B.P., Recent approaches in designing bioadhesive materials inspired by mussel adhesive protein, J. Polym. Sci. A Polym. Chem., 2017, vol. 55, pp. 9–33. https://doi.org/10.1002/pola.28368

    Article  CAS  Google Scholar 

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Funding

The work was supported by a state assignment no. АААА-А20-120093090015-2.

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Authors and Affiliations

  1. Kurchatov Institute, GOSNIIGENETIKA National Research Center, 123182, Moscow, Russia

    V. G. Bogush, L. I. Davydova, V. S. Shulyakov, K. V. Sidoruk, S. V. Krasheninnikov, M. A. Bychkova & V. G. Debabov

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  1. V. G. Bogush
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  2. L. I. Davydova
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  3. V. S. Shulyakov
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  4. K. V. Sidoruk
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  5. S. V. Krasheninnikov
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  6. M. A. Bychkova
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  7. V. G. Debabov
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Correspondence to V. G. Bogush.

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The authors declare that they have no conflicts of interest.

This article does not contain any studies involving animals performed by any of the authors.

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Translated by I. Gordon

Abbreviations: DOPA, L-3,4-dihydroxy-phenylalanine; EDTA, ethylenediamine tetraacetic acid; GRAVY, grand average of hydropathicity; GTC, guanidine thiocyanate; MFP, mussel foot proteins; MW, molecular weight; NBT, nitro blue tetrazolium; PAGE, polyacrylamide gel electrophoresis; PBS, phosphate-buffered saline; PVC, polyvinyl chloride; SDS, sodium dodecyl sulfate; WDA, sequential wetting, drying and adhesion; θ, wetting contact angle, degrees.

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Bogush, V.G., Davydova, L.I., Shulyakov, V.S. et al. The Development of Bioadhesives Based on Recombinant Analogues of Spider Web Proteins. Appl Biochem Microbiol 58, 842–853 (2022). https://doi.org/10.1134/S000368382207002X

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