Login Register Cart 0
Generic placeholder image

Current Topics in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Nanoscale Structures and Materials from the Self-assembly of Polypeptides and DNA

Author(s): Julio Bernal-Chanchavac, Md. Al-Amin and Nicholas Stephanopoulos*

Volume 22, Issue 8, 2022

Published on: 03 January, 2022

Page: [699 - 712] Pages: 14

DOI: 10.2174/1568026621666211215142916

Price: $65

Abstract

The use of biological molecules with programmable self-assembly properties is an attractive route to functional nanomaterials. Proteins and peptides have been used extensively for these systems due to their biological relevance and a large number of supramolecular motifs, but it is still difficult to build highly anisotropic and programmable nanostructures due to their high complexity. Oligonucleotides, by contrast, have the advantage of programmability and reliable assembly, but lack biological and chemical diversity. In this review, we discuss systems that merge protein or peptide self-assembly with the addressability of DNA. We outline the various self-assembly motifs used, the chemistry for linking polypeptides with DNA, and the resulting nanostructures that can be formed by the interplay of these two molecules. Finally, we close by suggesting some interesting future directions in hybrid polypeptide-DNA nanomaterials, and potential applications for these exciting hybrids.

Keywords: Proteins, Peptides, DNA nanotechnology, Self-assembly, Biomaterials, Nanotechnology.

« Previous
Graphical Abstract

[1]
Huang, P-S.; Boyken, S.E.; Baker, D. The coming of age of de novo protein design. Nature, 2016, 537(7620), 320-327.
[http://dx.doi.org/10.1038/nature19946] [PMID: 27629638]
[2]
Stephanopoulos, N.; Ortony, J.H.; Stupp, S.I. Self-assembly for the synthesis of functional biomaterials. Acta Mater., 2013, 61(3), 912-930.
[http://dx.doi.org/10.1016/j.actamat.2012.10.046] [PMID: 23457423]
[3]
Jumper, J.; Evans, R.; Pritzel, A.; Green, T.; Figurnov, M.; Ronneberger, O.; Tunyasuvunakool, K.; Bates, R.; Žídek, A.; Potapenko, A.; Bridgland, A.; Meyer, C.; Kohl, S.A.A.; Ballard, A.J.; Cowie, A.; Romera-Paredes, B.; Nikolov, S.; Jain, R.; Adler, J.; Back, T.; Petersen, S.; Reiman, D.; Clancy, E.; Zielinski, M.; Steinegger, M.; Pacholska, M.; Berghammer, T.; Bodenstein, S.; Silver, D.; Vinyals, O.; Senior, A.W.; Kavukcuoglu, K.; Kohli, P.; Hassabis, D. Highly accurate protein structure prediction with AlphaFold. Nature, 2021, 596(7873), 583-589.
[http://dx.doi.org/10.1038/s41586-021-03819-2] [PMID: 34265844]
[4]
Baek, M.; DiMaio, F.; Anishchenko, I.; Dauparas, J.; Ovchinnikov, S.; Lee, G.R.; Wang, J.; Cong, Q.; Kinch, L.N.; Schaeffer, R.D.; Millán, C.; Park, H.; Adams, C.; Glassman, C.R.; DeGiovanni, A.; Pereira, J.H.; Rodrigues, A.V.; van Dijk, A.A.; Ebrecht, A.C.; Opperman, D.J.; Sagmeister, T.; Buhlheller, C.; Pavkov-Keller, T.; Rathinaswamy, M.K.; Dalwadi, U.; Yip, C.K.; Burke, J.E.; Garcia, K.C.; Grishin, N.V.; Adams, P.D.; Read, R.J.; Baker, D. Accurate prediction of protein structures and interactions using a three-track neural network. Science, 2021, 373(6557), 871-876.
[http://dx.doi.org/10.1126/science.abj8754] [PMID: 34282049]
[5]
Ong, L.L.; Hanikel, N.; Yaghi, O.K.; Grun, C.; Strauss, M.T.; Bron, P.; Lai-Kee-Him, J.; Schueder, F.; Wang, B.; Wang, P.; Kishi, J.Y.; Myhrvold, C.; Zhu, A.; Jungmann, R.; Bellot, G.; Ke, Y.; Yin, P. Programmable self-assembly of three-dimensional nanostructures from 10,000 unique components. Nature, 2017, 552(7683), 72-77.
[http://dx.doi.org/10.1038/nature24648] [PMID: 29219968]
[6]
Hong, F.; Zhang, F.; Liu, Y.; Yan, H. DNA origami: scaffolds for creating higher order structures. Chem. Rev., 2017, 117(20), 12584-12640.
[http://dx.doi.org/10.1021/acs.chemrev.6b00825] [PMID: 28605177]
[7]
Seeman, N.C.; Sleiman, H.F. DNA nanotechnology. Nat. Rev. Mater., 2017, 3, 1-23.
[8]
Goodman, R.P.; Schaap, I.A.; Tardin, C.F.; Erben, C.M.; Berry, R.M.; Schmidt, C.F.; Turberfield, A.J. Rapid chiral assembly of rigid DNA building blocks for molecular nanofabrication. Science, 2005, 310(5754), 1661-1665.
[http://dx.doi.org/10.1126/science.1120367] [PMID: 16339440]
[9]
He, Y.; Ye, T.; Su, M.; Zhang, C.; Ribbe, A.E.; Jiang, W.; Mao, C. Hierarchical self-assembly of DNA into symmetric supramolecular polyhedra. Nature, 2008, 452(7184), 198-201.
[http://dx.doi.org/10.1038/nature06597] [PMID: 18337818]
[10]
Winfree, E.; Liu, F.; Wenzler, L.A.; Seeman, N.C. Design and self-assembly of two-dimensional DNA crystals. Nature, 1998, 394(6693), 539-544.
[http://dx.doi.org/10.1038/28998] [PMID: 9707114]
[11]
Yan, H.; Park, S.H.; Finkelstein, G.; Reif, J.H.; LaBean, T.H. DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science, 2003, 301(5641), 1882-1884.
[http://dx.doi.org/10.1126/science.1089389] [PMID: 14512621]
[12]
Rothemund, P.W.K.; Ekani-Nkodo, A.; Papadakis, N.; Kumar, A.; Fygenson, D.K.; Winfree, E. Design and characterization of programmable DNA nanotubes. J. Am. Chem. Soc., 2004, 126(50), 16344-16352.
[http://dx.doi.org/10.1021/ja044319l] [PMID: 15600335]
[13]
Rothemund, P.W.K. Folding DNA to create nanoscale shapes and patterns. Nature, 2006, 440(7082), 297-302.
[http://dx.doi.org/10.1038/nature04586] [PMID: 16541064]
[14]
Douglas, S.M.; Dietz, H.; Liedl, T.; Högberg, B.; Graf, F.; Shih, W.M. Self-assembly of DNA into nanoscale three-dimensional shapes. Nature, 2009, 459(7245), 414-418.
[http://dx.doi.org/10.1038/nature08016] [PMID: 19458720]
[15]
Dietz, H.; Douglas, S.M.; Shih, W.M. Folding DNA into twisted and curved nanoscale shapes. Science, 2009, 325(5941), 725-730.
[http://dx.doi.org/10.1126/science.1174251] [PMID: 19661424]
[16]
Ke, Y.; Ong, L.L.; Shih, W.M.; Yin, P. Three-dimensional structures self-assembled from DNA bricks. Science, 2012, 338(6111), 1177-1183.
[http://dx.doi.org/10.1126/science.1227268] [PMID: 23197527]
[17]
Douglas, S.M.; Marblestone, A.H.; Teerapittayanon, S.; Vazquez, A.; Church, G.M.; Shih, W.M. Rapid prototyping of 3D DNA-origami shapes with caDNAno. Nucleic Acids Res., 2009, 37(15), 5001-5006.
[http://dx.doi.org/10.1093/nar/gkp436] [PMID: 19531737]
[18]
Huang, C-M.; Kucinic, A.; Johnson, J.A.; Su, H-J.; Castro, C.E. Integrated computer-aided engineering and design for DNA assemblies. Nat. Mater., 2021, 20(9), 1264-1271.
[http://dx.doi.org/10.1038/s41563-021-00978-5] [PMID: 33875848]
[19]
Weiden, J.; Bastings, M.M.C. DNA origami nanostructures for controlled therapeutic drug delivery. Curr. Opin. Colloid Interface Sci., 2021, 52, 101411.
[http://dx.doi.org/10.1016/j.cocis.2020.101411]
[20]
MacCulloch, T.; Buchberger, A.; Stephanopoulos, N. Emerging applications of peptide-oligonucleotide conjugates: bioactive scaffolds, self-assembling systems, and hybrid nanomaterials. Org. Biomol. Chem., 2019, 17(7), 1668-1682.
[http://dx.doi.org/10.1039/C8OB02436G] [PMID: 30483688]
[21]
Roviello, G.N.; Roviello, G.; Musumeci, D.; Bucci, E.M.; Pedone, C. Dakin-West reaction on 1-thyminyl acetic acid for the synthesis of 1,3-bis(1-thyminyl)-2-propanone, a heteroaromatic compound with nucleopeptide-binding properties. Amino Acids, 2012, 43(4), 1615-1623.
[http://dx.doi.org/10.1007/s00726-012-1237-7] [PMID: 22349760]
[22]
Scognamiglio, P.L.; Platella, C.; Napolitano, E.; Musumeci, D.; Roviello, G.N. From prebiotic chemistry to supramolecular biomedical materials: exploring the properties of self-assembling nucleobase-containing peptides. Molecules, 2021, 26(12), 3558.
[http://dx.doi.org/10.3390/molecules26123558] [PMID: 34200901]
[23]
Cai, J.; Rosenzweig, B.A.; Hamilton, A.D. Inhibition of chymotrypsin by a self-assembled DNA quadruplex functionalized with cyclic peptide binding fragments. Chemistry, 2009, 15(2), 328-332.
[http://dx.doi.org/10.1002/chem.200801637] [PMID: 19053105]
[24]
Ghosh, P.S.; Hamilton, A.D. Noncovalent template-assisted mimicry of multiloop protein surfaces: assembling discontinuous and functional domains. J. Am. Chem. Soc., 2012, 134(32), 13208-13211.
[http://dx.doi.org/10.1021/ja305360q] [PMID: 22839643]
[25]
Liu, Q.; Wang, H.; Shi, X.; Wang, Z-G.; Ding, B. Self-assembled DNA/peptide-based nanoparticle exhibiting synergistic enzymatic activity. ACS Nano, 2017, 11(7), 7251-7258.
[http://dx.doi.org/10.1021/acsnano.7b03195] [PMID: 28657711]
[26]
Wang, Z-G. Designed self-assembly of peptides with g-quadruplex/hemin dnazyme into nanofibrils possessing enzyme-mimicking active sites and catalytic functions. ACS Catal., 2018, 8, 7016-7024.
[http://dx.doi.org/10.1021/acscatal.8b00896]
[27]
Merrifield, R. B. Solid phase peptide synthesis .1. synthesis of a tetrapeptide. J. Am. Chem. Soc., 1963, 85, 2149.
[http://dx.doi.org/10.1021/ja00897a025]
[28]
Behrendt, R.; White, P.; Offer, J. Advances in Fmoc solid-phase peptide synthesis. J. Pept. Sci., 2016, 22(1), 4-27.
[http://dx.doi.org/10.1002/psc.2836] [PMID: 26785684]
[29]
Fields, G.B.; Noble, R.L. Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res., 1990, 35(3), 161-214.
[http://dx.doi.org/10.1111/j.1399-3011.1990.tb00939.x] [PMID: 2191922]
[30]
Levin, A. Biomimetic peptide self-assembly for functional materials. Nat. Rev. Chem., 2020, 4, 615-634.
[http://dx.doi.org/10.1038/s41570-020-0215-y]
[31]
Aronsson, C.; Dånmark, S.; Zhou, F.; Öberg, P.; Enander, K.; Su, H.; Aili, D. Self-sorting heterodimeric coiled coil peptides with defined and tuneable self-assembly properties. Sci. Rep., 2015, 5, 14063.
[http://dx.doi.org/10.1038/srep14063] [PMID: 26370878]
[32]
Ruff, Y.; Moyer, T.; Newcomb, C.J.; Demeler, B.; Stupp, S.I. Precision templating with DNA of a virus-like particle with peptide nanostructures. J. Am. Chem. Soc., 2013, 135(16), 6211-6219.
[http://dx.doi.org/10.1021/ja4008003] [PMID: 23574404]
[33]
Lou, C.; Martos-Maldonado, M.C.; Madsen, C.S.; Thomsen, R.P.; Midtgaard, S.R.; Christensen, N.J.; Kjems, J.; Thulstrup, P.W.; Wengel, J.; Jensen, K.J. Peptide-oligonucleotide conjugates as nanoscale building blocks for assembly of an artificial three-helix protein mimic. Nat. Commun., 2016, 7, 12294.
[http://dx.doi.org/10.1038/ncomms12294] [PMID: 27464951]
[34]
Lou, C.; Christensen, N.J.; Martos-Maldonado, M.C.; Midtgaard, S.R.; Ejlersen, M.; Thulstrup, P.W.; Sørensen, K.K.; Jensen, K.J.; Wengel, J. Folding topology of a short coiled-coil peptide structure templated by an oligonucleotide triplex. Chemistry, 2017, 23(39), 9297-9305.
[http://dx.doi.org/10.1002/chem.201700971] [PMID: 28383784]
[35]
Jin, J.; Baker, E.G.; Wood, C.W.; Bath, J.; Woolfson, D.N.; Turberfield, A.J. Peptide assembly directed and quantified using megadalton dna nanostructures. ACS Nano, 2019, 13(9), 9927-9935.
[http://dx.doi.org/10.1021/acsnano.9b04251] [PMID: 31381314]
[36]
Buchberger, A.; Simmons, C.R.; Fahmi, N.E.; Freeman, R.; Stephanopoulos, N. Hierarchical assembly of nucleic acid/coiled-coil peptide nanostructures. J. Am. Chem. Soc., 2020, 142(3), 1406-1416.
[http://dx.doi.org/10.1021/jacs.9b11158] [PMID: 31820959]
[37]
Jiang, T.; Meyer, T.A.; Modlin, C.; Zuo, X.; Conticello, V.P.; Ke, Y. Structurally ordered nanowire formation from co-assembly of DNA origami and collagen-mimetic peptides. J. Am. Chem. Soc., 2017, 139(40), 14025-14028.
[http://dx.doi.org/10.1021/jacs.7b08087] [PMID: 28949522]
[38]
Smith, C.K.; Regan, L. Construction and design of β-sheets. Acc. Chem. Res., 1997, 30, 153-161.
[http://dx.doi.org/10.1021/ar9601048]
[39]
Kye, M.; Lim, Y-B. Reciprocal self-assembly of peptide-dna conjugates into a programmable sub-10-nm supramolecular deoxyribonucleoprotein. Angew. Chem. Int. Ed. Engl., 2016, 55(39), 12003-12007.
[http://dx.doi.org/10.1002/anie.201605696] [PMID: 27553897]
[40]
Chotera, A.; Sadihov, H.; Cohen-Luria, R.; Monnard, P-A.; Ashkenasy, G. Functional assemblies emerging in complex mixtures of peptides and nucleic acid-peptide chimeras. Chemistry, 2018, 24, 10128-10135.
[http://dx.doi.org/10.1002/chem.201800500] [PMID: 29732630]
[41]
Ni, R.; Chau, Y. Nanoassembly of oligopeptides and dna mimics the sequential disassembly of a spherical virus. Angew. Chem. Int. Ed. Engl., 2020, 59(9), 3578-3584.
[http://dx.doi.org/10.1002/anie.201913611] [PMID: 31749269]
[42]
Kim, C-J.; Park, J-E.; Hu, X.; Albert, S.K.; Park, S-J. Peptide-driven shape control of low-dimensional DNA nanostructures. ACS Nano, 2020, 14(2), 2276-2284.
[http://dx.doi.org/10.1021/acsnano.9b09312] [PMID: 31962047]
[43]
Albert, S.K.; Lee, S.; Durai, P.; Hu, X.; Jeong, B.; Park, K.; Park, S.J. Janus nanosheets with face-selective molecular recognition properties from DNA-peptide conjugates. Small, 2021, 17(12), e2006110.
[http://dx.doi.org/10.1002/smll.202006110] [PMID: 33721400]
[44]
Murai, K. Mineralization of magnetic nano-tape in self-organized nanospace composed of nucleopeptides and peptides. CrystEngComm, 2019, 21, 3557-3567.
[http://dx.doi.org/10.1039/C9CE00146H]
[45]
Hendricks, M.P.; Sato, K.; Palmer, L.C.; Stupp, S.I. Supramolecular assembly of peptide amphiphiles. Acc. Chem. Res., 2017, 50(10), 2440-2448.
[http://dx.doi.org/10.1021/acs.accounts.7b00297] [PMID: 28876055]
[46]
Higashi, S.L.; Shibata, A.; Kitamura, Y.; Hirosawa, K.M.; Suzuki, K.G.N.; Matsuura, K.; Ikeda, M. Hybrid soft nanomaterials composed of DNA microspheres and supramolecular nanostructures of semi-artificial glycopeptides. Chemistry, 2019, 25(51), 11955-11962.
[http://dx.doi.org/10.1002/chem.201902421] [PMID: 31268200]
[47]
Freeman, R. Reversible self-assembly of superstructured networks. Science, 2018, 362, 808.
[http://dx.doi.org/10.1126/science.aat6141]
[48]
Daly, M.L.; Gao, Y.; Freeman, R. Encoding reversible hierarchical structures with supramolecular peptide-DNA materials. Bioconjug. Chem., 2019, 30(7), 1864-1869.
[http://dx.doi.org/10.1021/acs.bioconjchem.9b00271] [PMID: 31181892]
[49]
Kashiwagi, D.; Sim, S.; Niwa, T.; Taguchi, H.; Aida, T. Protein nanotube selectively cleavable with dna: supramolecular polymerization of “DNA-appended molecular chaperones”. J. Am. Chem. Soc., 2018, 140(1), 26-29.
[http://dx.doi.org/10.1021/jacs.7b09892] [PMID: 29226681]
[50]
McMillan, J.R.; Mirkin, C.A. DNA-functionalized, bivalent proteins. J. Am. Chem. Soc., 2018, 140(22), 6776-6779.
[http://dx.doi.org/10.1021/jacs.8b03403] [PMID: 29799197]
[51]
McMillan, J.R.; Hayes, O.G.; Remis, J.P.; Mirkin, C.A. Programming protein polymerization with DNA. J. Am. Chem. Soc., 2018, 140(46), 15950-15956.
[http://dx.doi.org/10.1021/jacs.8b10011] [PMID: 30407003]
[52]
Brodin, J.D.; Auyeung, E.; Mirkin, C.A. DNA-mediated engineering of multicomponent enzyme crystals. Proc. Natl. Acad. Sci. USA, 2015, 112(15), 4564-4569.
[http://dx.doi.org/10.1073/pnas.1503533112] [PMID: 25831510]
[53]
McMillan, J.R.; Brodin, J.D.; Millan, J.A.; Lee, B.; Olvera de la Cruz, M.; Mirkin, C.A. Modulating nanoparticle superlattice structure using proteins with tunable bond distributions. J. Am. Chem. Soc., 2017, 139(5), 1754-1757.
[http://dx.doi.org/10.1021/jacs.6b11893] [PMID: 28121437]
[54]
Hayes, O.G.; McMillan, J.R.; Lee, B.; Mirkin, C.A. DNA-encoded protein janus nanoparticles. J. Am. Chem. Soc., 2018, 140(29), 9269-9274.
[http://dx.doi.org/10.1021/jacs.8b05640] [PMID: 29989807]
[55]
Subramanian, R.H.; Smith, S.J.; Alberstein, R.G.; Bailey, J.B.; Zhang, L.; Cardone, G.; Suominen, L.; Chami, M.; Stahlberg, H.; Baker, T.S.; Tezcan, F.A. Self-assembly of a designed nucleoprotein architecture through multimodal interactions. ACS Cent. Sci., 2018, 4(11), 1578-1586.
[http://dx.doi.org/10.1021/acscentsci.8b00745] [PMID: 30555911]
[56]
Mou, Y.; Yu, J-Y.; Wannier, T.M.; Guo, C-L.; Mayo, S.L. Computational design of co-assembling protein-DNA nanowires. Nature, 2015, 525(7568), 230-233.
[http://dx.doi.org/10.1038/nature14874] [PMID: 26331548]
[57]
Zhou, K.; Ke, Y.; Wang, Q. Selective in situ assembly of viral protein onto DNA origami. J. Am. Chem. Soc., 2018, 140(26), 8074-8077.
[http://dx.doi.org/10.1021/jacs.8b03914] [PMID: 29932333]
[58]
Zhou, K.; Zhou, Y.; Pan, V.; Wang, Q.; Ke, Y. Programming dynamic assembly of viral proteins with DNA origami. J. Am. Chem. Soc., 2020, 142(13), 5929-5932.
[http://dx.doi.org/10.1021/jacs.9b13773] [PMID: 32191463]
[59]
Praetorius, F.; Dietz, H. Self-assembly of genetically encoded DNA-protein hybrid nanoscale shapes. Science, 2017, 355(6331), eaam5488.
[http://dx.doi.org/10.1126/science.aam5488] [PMID: 28336611]
[60]
Zhang, C.; Tian, C.; Guo, F.; Liu, Z.; Jiang, W.; Mao, C. DNA-directed three-dimensional protein organization. Angew. Chem. Int. Ed. Engl., 2012, 51(14), 3382-3385.
[http://dx.doi.org/10.1002/anie.201108710] [PMID: 22374892]
[61]
Xu, Y.; Jiang, S.; Simmons, C.R.; Narayanan, R.P.; Zhang, F.; Aziz, A.M.; Yan, H.; Stephanopoulos, N. Tunable nanoscale cages from self-assembling DNA and protein building blocks. ACS Nano, 2019, 13(3), 3545-3554.
[http://dx.doi.org/10.1021/acsnano.8b09798] [PMID: 30835439]
[62]
Procyk, J.; Poppleton, E.; Šulc, P. Coarse-grained nucleic acid-protein model for hybrid nanotechnology. Soft Matter, 2021, 17(13), 3586-3593.
[http://dx.doi.org/10.1039/D0SM01639J] [PMID: 33398312]
[63]
Goetzfried, M.A.; Vogele, K.; Mückl, A.; Kaiser, M.; Holland, N.B.; Simmel, F.C.; Pirzer, T. Periodic operation of a dynamic DNA origami structure utilizing the hydrophilic-hydrophobic phase-transition of stimulus-sensitive polypeptides. Small, 2019, 15(45), e1903541.
[http://dx.doi.org/10.1002/smll.201903541] [PMID: 31531953]
[64]
Teller, C.; Willner, I. Organizing protein-DNA hybrids as nanostructures with programmed functionalities. Trends Biotechnol., 2010, 28(12), 619-628.
[http://dx.doi.org/10.1016/j.tibtech.2010.09.005] [PMID: 21035218]
[65]
Linko, V.; Nummelin, S.; Aarnos, L.; Tapio, K.; Toppari, J.J.; Kostiainen, M.A. DNA-based enzyme reactors and systems. Nanomaterials (Basel), 2016, 6(8), 139.
[http://dx.doi.org/10.3390/nano6080139] [PMID: 28335267]
[66]
Rajendran, A.; Nakata, E.; Nakano, S.; Morii, T. Nucleic-acid-templated enzyme cascades. ChemBioChem, 2017, 18(8), 696-716.
[http://dx.doi.org/10.1002/cbic.201600703] [PMID: 28150909]

Rights & Permissions Print Cite
Article Metrics
40
1
World Chagas Disease
© 2024 Bentham Science Publishers | Privacy Policy