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Proteins and peptides for functional nanomaterials: Current efforts and new opportunities

Published online by Cambridge University Press:  10 December 2020

Hasti Iranmanesh ,
Bijil Subhash ,
Dominic J. Glover  and
Nicholas M. Bedford
Hasti Iranmanesh
Affiliation:
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Australia; hasti.iranmanesh@unsw.edu.au
Bijil Subhash
Affiliation:
School of Chemical Engineering, University of New South Wales, Australia; b.subhash@unsw.edu.au
Dominic J. Glover
Affiliation:
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Australia; d.glover@unsw.edu.au
Nicholas M. Bedford
Affiliation:
School of Chemical Engineering, University of New South Wales, Australia; n.bedford@unsw.edu.au
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Abstract

The ability to synthesize and assemble functional nanomaterials using proteins and peptides is an area of active research, merging various methodologies common in biochemistry and molecular biology to create a wide range of nanoscale materials with intriguing properties. These “bioenabled” nanomaterials have distinct advantages over their nonbiological counterparts, including diverse/precise chemical functionalization, benign aqueous-based processing conditions, and the inherent high specificity for targeted substrates. In parallel, the advent of synthetic biology is providing avenues to engineer novel protein chemistry and functionality, leading to commercialization in the startup sector. In this article, we provide a prospective review for fusing established methods in protein-enabled nanomaterials with those found commonly in synthetic biology. We first summarize significant findings and outcomes from the peptide and protein-enabled nanomaterials literature. The application of synthetic biology methodologies toward research areas of tangential similarity will also be summarized, including the directed evolution of enzymes for bioinorganic reactions, noncanonical amino acid engineering in proteins, and the incorporation of electrical active elements into anisotropic proteins. To conclude, we will suggest avenues for new research directions for protein-enabled nanomaterials that fully exploit the power of synthetic biology.

Type
Engineered Proteins as Multifunctional Materials
Information
MRS Bulletin , Volume 45 , Issue 12: Engineered Proteins as Multifunctional Materials , December 2020 , pp. 1005 - 1016
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Copyright
Copyright © The Author(s), 2020, published on behalf of Materials Research Society by Cambridge University Press

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References

Faivre, D., Schüler, D., Chem. Rev. 108, 4875 (2008).CrossRefGoogle Scholar
Dickerson, M.B., Sandhage, K.H., Naik, R.R., Chem. Rev. 108, 4935 (2008).CrossRefGoogle Scholar
Gahlawat, G., Choudhury, A.R., RSC Adv. 9, 12944 (2019).CrossRefGoogle Scholar
Walsh, T.R., Knecht, M.R., Chem. Rev. 117, 12641 (2017).CrossRefGoogle Scholar
Kröger, N., Deutzmann, R., Bergsdorf, C., Sumper, M., Proc. Natl. Acad. Sci. U.S.A. 97, 14133 (2000).CrossRefGoogle Scholar
Kröger, N., Deutzmann, R., Sumper, M., Science 286, 1129 (1999).Google Scholar
Kröger, N., Dickerson, M.B., Ahmad, G., Cai, Y., Haluska, M.S., Sandhage, K.H., Poulsen, N., Sheppard, V.C., Angew. Chem. Int. Ed. 45, 7239 (2006).CrossRefGoogle Scholar
Kisailus, D., Choi, J.H., Weaver, J.C., Yang, W., Morse, D.E., Adv. Mater. 17, 314 (2005).CrossRefGoogle Scholar
Singh, V., Syst. Synth. Biol. 8, 271 (2014).CrossRefGoogle Scholar
McLuskey, J.B., Clark, D.S., Glover, D.J., Trends Biotechnol. 38, 976 (2020).CrossRefGoogle Scholar
Glover, D.J., Giger, L., Kim, S.S., Naik, R.R., Clark, D.S., Nat. Commun. 7, 11771 (2016).CrossRefGoogle Scholar
Glover, D.J., Lim, S., Xu, D., Sloan, N.B., Zhang, Y., Clark, D.S., ACS Synth. Biol. 7, 2447 (2018).CrossRefGoogle Scholar
Lim, S., Jung, G.A., Glover, D.J., Clark, D.S., Small 15, 1805558 (2019).CrossRefGoogle ScholarPubMed
Glover, D.J., Clark, D.S., ACS Cent. Sci. 2, 438 (2016).CrossRefGoogle Scholar
Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A., Zhang, F., Science 339, 819 (2013).CrossRefGoogle Scholar
Bloom, J.D., Meyer, M.M., Meinhold, P., Otey, C.R., MacMillan, D., Arnold, F.H., Curr. Opin. Struct. Biol. 15, 447 (2005).CrossRefGoogle Scholar
Arnold, F.H., Angew. Chem. Int. Ed. 57, 4143 (2018).CrossRefGoogle Scholar
Dahl, R.H., Zhang, F., Alonso-Gutierrez, J., Baidoo, E., Batth, T.S., Redding-Johanson, A.M., Petzold, C.J., Mukhopadhyay, A., Lee, T.S., Adams, P.D., Keasling, J.D., Nat. Biotechnol. 31, 1039 (2013).CrossRefGoogle Scholar
Glover, D.J., Ng, S.M., Mechler, A., Martin, L.L., Jans, D.A., FASEB J. 23, 2996 (2009).CrossRefGoogle Scholar
Keasling, J.D., ACS Chem. Biol. 3, 64 (2008).CrossRefGoogle Scholar
Carlson, E.D., Gan, R., Hodgman, C.E., Jewett, M.C., Biotechnol. Adv. 30, 1185 (2012).CrossRefGoogle Scholar
Kwon, Y.-C., Jewett, M.C., Sci. Rep. 5, 8663 (2015).CrossRefGoogle Scholar
Hildebrand, M., Chem. Rev. 108, 4855 (2008).CrossRefGoogle Scholar
Xia, L., Li, Z., Langmuir 27, 1116 (2011).CrossRefGoogle Scholar
Drummond, C., McCann, R., Patwardhan, S.V., Chem. Eng. J. 244, 483 (2014).CrossRefGoogle Scholar
Ragni, R., Cicco, S.R., Vona, D., Farinola, G.M., Adv. Mater. 30, 1704289 (2018).CrossRefGoogle Scholar
Brown, S., Proc. Natl. Acad. Sci. U.S.A. 89, 8651 (1992).CrossRefGoogle Scholar
Brown, S., Sarikaya, M., Johnson, E., J. Mol. Biol. 299, 725 (2000).CrossRefGoogle Scholar
Li, Y., Whyburn, G.P., Huang, Y., J. Am. Chem. Soc. 131, 15998 (2009).CrossRefGoogle Scholar
Chiu, C.-Y., Li, Y., Ruan, L., Ye, X., Murray, C.B., Huang, Y., Nat. Chem. 3, 393 (2011).CrossRefGoogle Scholar
Pacardo, D.B., Sethi, M., Jones, S.E., Naik, R.R., Knecht, M.R., ACS Nano 3, 1288 (2009).CrossRefGoogle Scholar
Hnilova, M., Oren, E.E., Seker, U.O.S., Wilson, B.R., Collino, S., Evans, J.S., Tamerler, C., Sarikaya, M., Langmuir 24, 12440 (2008).CrossRefGoogle Scholar
Naik, R.R., Stringer, S.J., Agarwal, G., Jones, S.E., Stone, M.O., Nat. Mater. 1, 169 (2002).CrossRefGoogle Scholar
Liang, M.-K., Deschaume, O., Patwardhan, S.V., Perry, C.C., J. Mater. Chem. 21, 80 (2011).CrossRefGoogle Scholar
Patwardhan, S.V., Emami, F.S., Berry, R.J., Jones, S.E., Naik, R.R., Deschaume, O., Heinz, H., Perry, C.C., J. Am. Chem. Soc. 134, 6244 (2012).CrossRefGoogle Scholar
Mao, C., Solis, D.J., Reiss, B.D., Kottmann, S.T., Sweeney, R.Y., Hayhurst, A., Georgiou, G., Iverson, B., Belcher, A.M., Science 303, 213 (2004).CrossRefGoogle Scholar
Cui, Y., Kim, S.N., Jones, S.E., Wissler, L.L., Naik, R.R., McAlpine, M.C., Nano Lett. 10, 4559 (2010).CrossRefGoogle Scholar
So, C.R., Hayamizu, Y., Yazici, H., Gresswell, C., Khatayevich, D., Tamerler, C., Sarikaya, M., ACS Nano 6, 1648 (2012).CrossRefGoogle Scholar
Muratore, C., Juhl, A.T., Stroud, A.J., Lai, D.W., Jawaid, A.M., Burzynski, K.M., Dagher, J.M., Leuty, G.M., Harsch, C., Kim, S.S., Ngo, Y.H., Glavin, N.R., Berry, R.J., Durstock, M.F., Derosa, P.A., Roy, A.K., Heckman, E.M., Naik, R.R., Appl. Phys. Lett. 112, 233704 (2018).CrossRefGoogle Scholar
Chen, J., Zhu, E., Liu, J., Zhang, S., Lin, Z., Duan, X., Heinz, H., Huang, Y., De Yoreo, J.J., Science 362, 1135 (2018).CrossRefGoogle Scholar
Zhang, H., Yamazaki, T., Zhi, C., Hanagata, N., Nanoscale 4, 6343 (2012).CrossRefGoogle ScholarPubMed
Naik, R.R., Jones, S.E., Murray, C.J., McAuliffe, J.C., Vaia, R.A., Stone, M.O., Adv. Funct. Mater. 14, 25 (2004).CrossRefGoogle Scholar
Schüler, T., Renkel, J., Hobe, S., Susewind, M., Jacob, D.E., Panthöfer, M., Hoffmann-Röder, A., Paulsen, H., Tremel, W., J. Mater. Chem. B 2, 3511 (2014).CrossRefGoogle Scholar
Whaley, S.R., English, D.S., Hu, E.L., Barbara, P.F., Belcher, A.M., Nature 405, 665 (2000).CrossRefGoogle Scholar
Zin, M.T., Munro, A.M., Gungormus, M., Wong, N.-Y., Ma, H., Tamerler, C., Ginger, D.S., Sarikaya, M., Jen, A.K.Y., J. Mater. Chem. 17, 866 (2007).CrossRefGoogle Scholar
Tamerler, C., Sarikaya, M., MRS Bull. 33, 504 (2008).CrossRefGoogle Scholar
Zhu, E., Yan, X., Wang, S., Xu, M., Wang, C., Liu, H., Huang, J., Xue, W., Cai, J., Heinz, H., Li, Y., Huang, Y., Nano Lett. 19, 3730 (2019).CrossRefGoogle Scholar
Bedford, N.M., Ramezani-Dakhel, H., Slocik, J.M., Briggs, B.D., Ren, Y., Frenkel, A.I., Petkov, V., Heinz, H., Naik, R.R., Knecht, M.R., ACS Nano 9, 5082 (2015).CrossRefGoogle Scholar
Nuraje, N., Dang, X., Qi, J., Allen, M.A., Lei, Y., Belcher, A.M., Adv. Mater. 24, 2885 (2012).CrossRefGoogle Scholar
Nam, K.T., Kim, D.-W., Yoo, P.J., Chiang, C.-Y., Meethong, N., Hammond, P.T., Chiang, Y.-M., Belcher, A.M., Science 312, 885 (2006).CrossRefGoogle Scholar
Slocik, J.M., Zabinski, J.S. Jr., Phillips, D.M., Naik, R.R., Small 4, 548 (2008).CrossRefGoogle Scholar
Kim, S.N., Kuang, Z., Slocik, J.M., Jones, S.E., Cui, Y., Farmer, B.L., McAlpine, M.C., Naik, R.R., J. Am. Chem. Soc. 133, 14480 (2011).CrossRefGoogle Scholar
Briggs, B.D., Palafox-Hernandez, J.P., Li, Y., Lim, C.-K., Woehl, T.J., Bedford, N.M., Seifert, S., Swihart, M.T., Prasad, P.N., Walsh, T.R., Knecht, M.R., Phys. Chem. Chem. Phys. 18, 30845 (2016).CrossRefGoogle Scholar
Meldrum, F.C., Wade, V.J., Nimmo, D.L., Heywood, B.R., Mann, S., Nature 349, 684 (1991).CrossRefGoogle Scholar
Li, F., Wang, Q., Small 10, 230 (2014).CrossRefGoogle ScholarPubMed
Kramer, R.M., Li, C., Carter, D.C., Stone, M.O., Naik, R.R., J. Am. Chem. Soc. 126, 13282 (2004).CrossRefGoogle Scholar
Klem, M.T., Willits, D., Solis, D.J., Belcher, A.M., Young, M., Douglas, T., Adv. Funct. Mater. 15, 1489 (2005).CrossRefGoogle Scholar
McMillan, R.A., Paavola, C.D., Howard, J., Chan, S.L., Zaluzec, N.J., Trent, J.D., Nat. Mater. 1, 247 (2002).CrossRefGoogle Scholar
McMillan, R.A., Howard, J., Zaluzec, N.J., Kagawa, H.K., Mogul, R., Li, Y.-F., Paavola, C.D., Trent, J.D., J. Am. Chem. Soc. 127, 2800 (2005).CrossRefGoogle Scholar
Schoen, A.P., Schoen, D.T., Huggins, K.N.L., Arunagirinathan, M.A., Heilshorn, S.C., J. Am. Chem. Soc. 133, 18202 (2011).CrossRefGoogle Scholar
Huggins, K.N.L., Schoen, A.P., Arunagirinathan, M.A., Heilshorn, S.C., Adv. Funct. Mater. 24, 7737 (2014).CrossRefGoogle Scholar
Lee, Y.J., Yi, H., Kim, W.-J., Kang, K., Yun, D.S., Strano, M.S., Ceder, G., Belcher, A.M., Science 324, 1051 (2009).Google Scholar
Loke, D.K., Clausen, G.J., Ohmura, J.F., Chong, T.-C., Belcher, A.M., ACS Appl. Nano Mater. 1, 6556 (2018).CrossRefGoogle Scholar
Records, W.C., Yoon, Y., Ohmura, J.F., Chanut, N., Belcher, A.M., Nano Energy 58, 167 (2019).CrossRefGoogle Scholar
Aljabali, A.A.A., Barclay, J.E., Lomonossoff, G.P., Evans, D.J., Nanoscale 2, 2596 (2010).CrossRefGoogle Scholar
Aljabali, A.A.A., Lomonossoff, G.P., Evans, D.J., Biomacromolecules 12, 2723 (2011).CrossRefGoogle Scholar
Steinmetz, N.F., Shah, S.N., Barclay, J.E., Rallapalli, G., Lomonossoff, G.P., Evans, D.J., Small 5, 813 (2009).CrossRefGoogle Scholar
Reith, F., Etschmann, B., Grosse, C., Moors, H., Benotmane, M.A., Monsieurs, P., Grass, G., Doonan, C., Vogt, S., Lai, B., Martinez-Criado, G., George, G.N., Nies, D.H., Mergeay, M., Pring, A., Southam, G., Brugger, J., Proc. Natl. Acad. Sci. U.S.A. 106, 17757 (2009).CrossRefGoogle Scholar
He, S., Guo, Z., Zhang, Y., Zhang, S., Wang, J., Gu, N., Mater. Lett. 6, 3984 (2007).CrossRefGoogle Scholar
Johnston, C.W., Wyatt, M.A., Li, X., Ibrahim, A., Shuster, J., Southam, G., Magarvey, N.A., Nat. Chem. Biol. 9, 241 (2013).CrossRefGoogle Scholar
Cobo, I., Li, M., Sumerlin, B.S., Perrier, S., Nat. Mater. 14, 143 (2015).CrossRefGoogle Scholar
Chari, R.V.J., Miller, M.L., Widdison, W.C., Angew. Chem. Int. Ed. 53, 3796 (2014).CrossRefGoogle Scholar
Hermanson, G.T., “Functional Targets for Bioconjugation,” in Bioconjugate Techniques, 3rd ed., Hermanson, G.T., Ed. (Academic Press, Boston, 2013), p. 127.CrossRefGoogle Scholar
de Graaf, A.J., Kooijman, M., Hennink, W.E., Mastrobattista, E., Bioconj. Chem. 20, 1281 (2009).CrossRefGoogle Scholar
Kolb, H.C., Finn, M.G., Sharpless, K.B., Angew. Chem. Int. Ed. 40, 2004 (2001).3.0.CO;2-5>CrossRefGoogle Scholar
Rostovtsev, V.V., Green, L.G., Fokin, V.V., Sharpless, K.B., Angew. Chem. Int. Ed. 41, 2596 (2002).3.0.CO;2-4>CrossRefGoogle Scholar
Tornøe, C.W., Christensen, C., Meldal, M.. J. Org. Chem. 67, 3057 (2002).CrossRefGoogle Scholar
Meldal, M., Tornøe, C.W., Chem. Rev. 108, 2952 (2008).CrossRefGoogle Scholar
Prescher, J.A., Bertozzi, C.R., Nat. Chem. Biol. 1, 13 (2005).CrossRefGoogle Scholar
Jewett, J.C., Bertozzi, C.R., Chem. Soc. Rev. 39, 1272 (2010).CrossRefGoogle Scholar
Young, D.D., Schultz, P.G., ACS Chem. Biol. 13, 854 (2018).CrossRefGoogle Scholar
Wang, L., Brock, A., Herberich, B., Schultz, P.G., Science 292, 498 (2001).CrossRefGoogle Scholar
Korkmaz, G., Holm, M., Wiens, T., Sanyal, S., J. Biol. Chem. 289, 30334 (2014).CrossRefGoogle Scholar
Lang, K., Davis, L., Chin, J.W., Methods Mol. Biol. 1266, 217 (2015).CrossRefGoogle Scholar
Chatterjee, A., Sun, S.B., Furman, J.L., Xiao, H., Schultz, P.G., Biochemistry 52, 1828 (2013).CrossRefGoogle Scholar
Bryson, D.I., Fan, C., Guo, L.T., Miller, C., Söll, D., Liu, D.R., Nat. Chem. Biol. 13, 1253 (2017).CrossRefGoogle Scholar
Pirman, N.L., Barber, K.W., Aerni, H.R., Ma, N.J., Haimovich, A.D., Rogulina, S., Isaacs, F.J., Rinehart, J., Nat. Commun. 6, 8130 (2015).CrossRefGoogle Scholar
Mehl, R.A., Anderson, J.C., Santoro, S.W., Wang, L., Martin, A.B., King, D.S., Horn, D.M., Schultz, P.G., J. Am. Chem. Soc. 125, 935 (2003).CrossRefGoogle Scholar
Hodgman, C.E., Jewett, M.C., Metab. Eng. 14, 261 (2012).CrossRefGoogle Scholar
Silverman, A.D., Karim, A.S., Jewett, M.C., Nat. Rev. Genet. 21, 151 (2020).CrossRefGoogle Scholar
Hong, S.H., Ntai, I., Haimovich, A.D., Kelleher, N.L., Isaacs, F.J., Jewett, M.C., ACS Synth. Biol. 3, 398 (2014).CrossRefGoogle Scholar
Gao, W., Cho, E., Liu, Y., Lu, Y., Front. Pharmacol. 10, 611 (2019).CrossRefGoogle Scholar
Wen, J., Xu, Y., Li, H., Lu, A., Sun, S., Chem. Commun. 51, 11346 (2015).CrossRefGoogle Scholar
Huang, X., Yin, Z., Wu, S., Qi, X., He, Q., Zhang, Q., Yan, Q., Boey, F., Zhang, H., Small 7, 1876 (2011).CrossRefGoogle ScholarPubMed
De Leo, F., Magistrato, A., Bonifazi, D., Chem. Soc. Rev. 44, 6916 (2015).CrossRefGoogle Scholar
Li, Y., Yang, C., Guo, X., Acc. Chem. Res. 53, 159 (2020).CrossRefGoogle Scholar
Su, T.A., Neupane, M., Steigerwald, M.L., Venkataraman, L., Nuckolls, C., Nat. Rev. Mater. 1, 16002 (2016).CrossRefGoogle Scholar
Freeley, M., Worthy, H.L., Ahmed, R., Bowen, B., Watkins, D., Macdonald, J.E., Zheng, M., Jones, D.D., Palma, M., J. Am. Chem. Soc. 139, 17834 (2017).CrossRefGoogle Scholar
Pédelacq, J.-D., Cabantous, S., Tran, T., Terwilliger, T.C., Waldo, G.S., Nat. Biotechnol. 24, 79 (2006).CrossRefGoogle Scholar
Choi, J.-W., Nam, Y.-S., Oh, B.-K., Lee, W.H., Fujihira, M., Synth. Met. 117, 241 (2001).CrossRefGoogle Scholar
Thomas, S.K., Jamieson, W.D., Gwyther, R.E.A., Bowen, B.J., Beachey, A., Worthy, H.L., Macdonald, J.E., Elliott, M., Castell, O.K., Jones, D.D., Bioconjug. Chem. 31, 584 (2020).CrossRefGoogle Scholar
Shinobu, A., Agmon, N., J. Chem. Theory Comput. 13, 353 (2017).CrossRefGoogle Scholar
Albayrak, C., Swartz, J.R., ACS Synth. Biol. 3, 353 (2014).CrossRefGoogle Scholar
Banhart, F., Kotakoski, J., Krasheninnikov, A.V., ACS Nano 5, 26 (2011).CrossRefGoogle Scholar
Li, D., Zhang, W., Yu, X., Wang, Z., Su, Z., Wei, G., Nanoscale 8, 19491 (2016).CrossRefGoogle ScholarPubMed
Bräse, S., Gil, C., Knepper, K., Zimmermann, V., Angew. Chem. Int. Ed. 44, 5188 (2005).CrossRefGoogle Scholar
Zaki, A.J., Hartley, Andrew M., Reddington, S.C., Thomas, S.K., Watson, P., Hayes, A., Moskalenko, A.V., Craciun, M.F., Macdonald, J.E., Jones, D.D., Elliott, M., RSC Adv. 8, 5768 (2018).CrossRefGoogle Scholar
Park, J., Yan, M., Acc. Chem. Res. 46, 181 (2013).CrossRefGoogle Scholar
Rasmussen, M., Abdellaoui, S., Minteer, S.D., Biosens. Bioelectron. 76, 91 (2016).CrossRefGoogle Scholar
Xiao, X., Xia, H.-q., Wu, R., Bai, L., Yan, L., Magner, E., Cosnier, S., Lojou, E., Zhu, Z., Liu, A., Chem. Rev. 119, 9509 (2019).CrossRefGoogle Scholar
Cooney, M.J., Svoboda, V., Lau, C., Martin, G., Minteer, S.D., Energy Environ. Sci. 1, 320 (2008).CrossRefGoogle Scholar
Ghindilis, A.L., Atanasov, P., Wilkins, E., Electroanalysis 9, 661 (1997).CrossRefGoogle Scholar
Falk, M., Blum, Z., Shleev, S., Electrochim. Acta 82, 191 (2012).CrossRefGoogle Scholar
Meredith, M.T., Minteer, S.D., Annu. Rev. Anal. Chem. (Palo Alto, CA) 5, 157 (2012).CrossRefGoogle Scholar
Amir, L., Carnally, S.A., Rayo, J., Rosenne, S., Melamed Yerushalmi, S., Schlesinger, O., Meijler, M.M., Alfonta, L., J. Am. Chem. Soc. 135, 70 (2013).CrossRefGoogle Scholar
Onoda, A., Inoue, N., Campidelli, S., Hayashi, T.. RSC Adv. 6, 65936 (2016).CrossRefGoogle Scholar
Schlesinger, O., Pasi, M., Dandela, R., Meijler, M.M., Alfonta, L., Phys. Chem. Chem. Phys. 20, 6159 (2018).CrossRefGoogle Scholar
Osman, D., Cavet, J., Adv. Appl. Microbiol. 65, 217 (2008).CrossRefGoogle Scholar
Nies, D.H., Herzberg, M., Mol. Microbiol. 87, 447 (2013).CrossRefGoogle Scholar
Xia, L., Han, M.J., Zhou, L., Huang, A., Yang, Z., Wang, T., Li, F., Yu, L., Tian, C., Zang, Z., Yang, Q.Z., Liu, C., Hong, W., Lu, Y., Alfonta, L., Wang, J., Angew. Chem. Int. Ed. 58, 16480 (2019).CrossRefGoogle Scholar
Drienovská, I., Roelfes, G., Nat. Catal. 3, 193 (2020).CrossRefGoogle Scholar
Almhjell, P.J., Boville, C.E., Arnold, F.H., Chem. Soc. Rev. 47, 8980 (2018).CrossRefGoogle Scholar
Sheldon, R.A., Brady, D., ChemSusChem 12, 2859 (2019).CrossRefGoogle Scholar
Bloom, J.D., Arnold, F.H., Proc. Natl. Acad. Sci. U.S.A. 106, 9995 (2009).CrossRefGoogle Scholar
Turner, N.J., Nat. Chem. Biol. 5, 567 (2009).CrossRefGoogle Scholar
Khersonsky, O., Tawfik, D.S., Annu. Rev. Biochem. 79, 471 (2010).Google Scholar
Denard, C.A., Ren, H., Zhao, H., Curr. Opin. Chem. Biol. 25, 55 (2015).CrossRefGoogle Scholar
Kan, S.B.J., Lewis, R.D., Chen, K., Arnold, F.H., Science 354, 1048 (2016).CrossRefGoogle Scholar
Wang, Z.J., Peck, N.E., Renata, H., Arnold, F.H., Chem. Sci. 5, 598 (2014).CrossRefGoogle Scholar
Tyagi, V., Bonn, R.B., Fasan, R., Chem. Sci. 6, 2488 (2015).CrossRefGoogle Scholar
Gu, Y., Natoli, S.N., Liu, Z., Clark, D.S., Hartwig, J.F., Angew. Chem. Int. Ed. 58, 13954 (2019).CrossRefGoogle Scholar
Dydio, P., Key, H.M., Hayashi, H., Clark, D.S., Hartwig, J.F., J. Am. Chem. Soc. 139, 1750 (2017).CrossRefGoogle Scholar
Meister, M., eLife 5, e17210 (2016).CrossRefGoogle Scholar
Liu, X., Lopez, P.A., Giessen, T.W., Giles, M., Way, J.C., Silver, P.A., Sci. Rep. 6, 38019 (2016).CrossRefGoogle Scholar
Stanley, S.A., Kelly, L., Latcha, K.N., Schmidt, S.F., Yu, X., Nectow, A.R., Sauer, J., Dyke, J.P., Dordick, J.S., Friedman, J.M., Nature 531, 647 (2016).CrossRefGoogle Scholar
Prasad, J., Viollet, S., Gurunatha, K.L., Urvoas, A., Fournier, A.C., Valerio-Lepiniec, M., Marcelot, C., Baris, B., Minard, P., Dujardin, E., Nanoscale 11, 17485 (2019).CrossRefGoogle Scholar
Malvankar, N.S., Vargas, M., Nevin, K.P., Franks, A.E., Leang, C., Kim, B.-C., Inoue, K., Mester, T., Covalla, S.F., Johnson, J.P., Rotello, V.M., Tuominen, M.T., Lovley, D.R., Nat. Nanotechnol. 6, 573 (2011).CrossRefGoogle Scholar
Ing, N.L., El-Naggar, M.Y., Hochbaum, A.I., J. Phys. Chem. B 122, 10403 (2018).CrossRefGoogle Scholar
Reardon, P.N., Mueller, K.T., J. Biol. Chem. 288, 29260 (2013).CrossRefGoogle Scholar
Wang, F., Gu, Y., O'Brien, J.P., Yi, S.M., Yalcin, S.E., Srikanth, V., Shen, C., Vu, D., Ing, N.L., Hochbaum, A.I., Egelman, E.H., Malvankar, N.S., Cell 177, 361 (2019).CrossRefGoogle Scholar
Ing, N.L., Spencer, R.K., Luong, S.H., Nguyen, H.D., Hochbaum, A.I., ACS Nano 12, 2652 (2018).CrossRefGoogle Scholar
Creasey, R.C.G., Mostert, A.B., Solemanifar, A., Nguyen, T.A.H., Virdis, B., Freguia, S., Laycock, B., ACS Omega 4, 1748 (2019).CrossRefGoogle Scholar
Altamura, L., Horvath, C., Rengaraj, S., Rongier, A., Elouarzaki, K., Gondran, C., Maçon, A.L., Vendrely, C., Bouchiat, V., Fontecave, M., Mariolle, D., Rannou, P., Le Goff, A., Duraffourg, N., Holzinger, M., Forge, V., Nat. Chem. 9, 157 (2017).CrossRefGoogle Scholar
Chen, Y.X., Ing, N.L., Wang, F., Xu, D., Sloan, N.B., Lam, N.T., Winter, D.L., Egelman, E.H., Hochbaum, A.I., Clark, D.S., Glover, D.J., ACS Nano 14, 6559 (2020).CrossRefGoogle Scholar
Liu, J., Zheng, Q., Deng, Y., Kallenbach, N.R., Lu, M., J. Mol. Biol. 361, 168 (2006).CrossRefGoogle Scholar
Glover, D.J., Clark, D.S., FEBS J. 282, 2985 (2015).CrossRefGoogle Scholar
Glover, D.J., Giger, L., Kim, J.R., Clark, D.S., Biotechnol. J. 8, 228 (2013).CrossRefGoogle Scholar
Lim, S., Jung, G.A., Muckom, R.J., Glover, D.J., Clark, D.S., Chem. Commun. 55, 806 (2019).CrossRefGoogle Scholar
Costa, S.A., Simon, J.R., Amiram, M., Tang, L., Zauscher, S., Brustad, E.M., Isaacs, F.J., Chilkoti, A., Adv. Mater. 30, 1704878 (2018).CrossRefGoogle Scholar
Bedford, N.M., Showalter, A.R., Woehl, T.J., Hughes, Z.E., Lee, S., Reinhart, B., Ertem, S.P., Coughlin, E.B., Ren, Y., Walsh, T.R., Bunker, B.A., ACS Nano 10, 8645 (2016).CrossRefGoogle Scholar
Glover, D.J., Xu, D., Clark, D.S., Biochemistry 58, 1019 (2019).CrossRefGoogle Scholar
Whang, D., Jin, S., Wu, Y., Lieber, C.M., Nano Lett. 3, 1255 (2003).CrossRefGoogle Scholar
Nguyen, T.-D., Tran, T.-H., RSC Adv. 4, 916 (2014).CrossRefGoogle Scholar
Ye, R., Zhao, J., Wickemeyer, B.B., Toste, F.D., Somorjai, G.A., Nat. Catal. 1, 318 (2018).CrossRefGoogle Scholar
Shi, D., Bedford, N.M., Cho, H.-S., Small 7, 2549 (2011).CrossRefGoogle ScholarPubMed