Supramolecular Architectures of Nucleic Acid/Peptide Hybrids
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International Journal of Molecular Sciences Review Supramolecular Architectures of Nucleic Acid/Peptide Hybrids Sayuri L. Higashi 1, Normazida Rozi 2, Sharina Abu Hanifah 2 and Masato Ikeda 1,3,4,5,* 1 United Graduate School of Drug Discovery and Medical Information Sciences, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan; [email protected] 2 Department of Chemical Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, Bangi 43600, Selangor, Malaysia; [email protected] (N.R.); [email protected] (S.A.H.) 3 Department of Chemistry and Biomolecular Science, Faculty of Engineering, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan 4 Center for Highly Advanced Integration of Nano and Life Sciences, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan 5 Institute for Glyco-Core Research (iGCORE), Gifu University, Furo-cho, Chikusa-ku, Nagoya 464-8603, Japan * Correspondence: [email protected]; Tel.: +81-58-293-2639 Received: 16 November 2020; Accepted: 9 December 2020; Published: 12 December 2020 Abstract: Supramolecular architectures that are built artificially from biomolecules, such as nucleic acids or peptides, with structural hierarchical orders ranging from the molecular to nano-scales have attracted increased attention in molecular science research fields. The engineering of nanostructures with such biomolecule-based supramolecular architectures could offer an opportunity for the development of biocompatible supramolecular (nano)materials. In this review, we highlighted a variety of supramolecular architectures that were assembled from both nucleic acids and peptides through the non-covalent interactions between them or the covalently conjugated molecular hybrids between them. Keywords: supramolecular architectures; self-assembly; nanostructures; nucleic acids; peptides; molecular hybrid 1. Introduction The construction of supramolecular architectures comprising nucleic acids as well as peptides (including oligopeptides and polypeptides in this paper) has greatly progressed recently [1–3]. Particularly, deoxyribonucleic acid (DNA) nanotechnology, a concept that was introduced by Seeman in the 1980s [4,5], has greatly expanded the range of rationally designed nanostructures (Figure1A). For instance, the DNA origami technology, which was invented by Rothemund [6,7], is widely accepted as a promising strategy to construct supramolecular architectures with custom nanoscale shapes via the bottom-up approach. Therein, a long single-stranded DNA (ssDNA) was folded by the addition of hundreds of short ssDNAs, namely, staple strands, followed by one-pot thermal annealing to obtain the rationally designed shape of the supramolecular architectures (the DNA origami). Apart from the DNA origami technology, the DNA tiles and bricks (in which the long ssDNAs are not prerequisite but the sequence-designed ssDNAs with the characteristic structural motif like the holiday junction [8–11] are required) offer supramolecular architectures with various morphology such as fibers [12–14], tubes [15–20], and polyhedrons [21–23]. Evidently, the high fidelity of the predictable Watson–Crick (WC) base pairings and the regular formation of the well-defined double-stranded DNA (dsDNA) structures are indispensable to the design and construction of such beautiful supramolecular architectures based on DNA nanotechnology. Int. J. Mol. Sci. 2020, 21, 9458; doi:10.3390/ijms21249458 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, 9458 2 of 25 Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 25 TheseThese DNADNA nanostructures nanostructures o ffofferer a varietya variety of of bio-applications, bio-applications, such such as scaas ffscaffoldsolds for enzymesfor enzymes in the in constructionthe construction of bioreactors of bioreactors [24,25 [24,25],], vehicles vehicles for drug for delivery drug delivery [26], biosensors [26], biosen [27sors], and [27], robotics and robotics [28–31]. Despite[28–31]. theseDespite promising these promising functionsand functions advantages and ofadvantages DNA nanostructures, of DNA nanostructures, several drawbacks several are directlydrawbacks related are todirectly the intrinsic related propertiesto the intrinsic of DNA. properties One of theof DNA. most fundamentalOne of the most drawbacks fundamental is the relativelydrawbacks low is stabilitythe relatively of DNA low against stability nucleases of DNA that against exist rathernucleases abundantly that exist under rather physiological abundantly conditionsunder physiological or in biological conditions fluids [32 or,33 ].in Furthermore, biological severalfluids [32,33]. DNA nanostructures Furthermore, require several high DNA salt concentrations,nanostructures whichrequire are occasionallyhigh salt concentrations, incompatible with which biosystems are occasionally and/or deviate incompatible significantly fromwith thebiosystems standard and/or salt concentration deviate significantly for biological from fluids the standard or cell culture salt concentration media [34]. However,for biological to overcome fluids or thesecell culture drawbacks, media a [34]. variety However, of strategies, to overcome including thes moleculare drawbacks, hybrid a variety approaches of strategies, that are describedincluding herein,molecular has hybrid been proposed approaches and that investigated are described [35–40 herein,]. has been proposed and investigated [35–40]. TheThe self-assemblyself-assembly of of oligopeptides oligopeptides or or polypeptides polypeptides is also is also an actively an actively investigated investigated research research topic intopic the in field the field of biomolecular of biomolecular science science (Figure (Figure1B) [1B)41 –[41–43].43]. For For example, example, the the self-assembled self-assembled fibrousfibrous nanostructuresnanostructures ofof proteins,proteins, suchsuch asas actinactin filamentsfilaments andand microtubules,microtubules, areare keyskeys toto cellularcellular movementmovement andand elasticityelasticity [ 44[44].]. Such Such fibrous fibrous self-assembled self-assembled nanostructures nanostructures of peptidesof peptides are presentare present both both inside inside and outsideand outside living living cells [45cells]. Particularly,[45]. Particularly, amyloid amyloid fibril formations fibril formations are beneficial are beneficial research research targets because targets ofbecause their severeof their pathological severe pathological outcomes outcomes [46]. Very [4 recently,6]. Very the recently, detailed the structure detailed of structure the amyloid- of theβ peptideamyloid- inβ peptide the potentially in the potentially pathological pathological self-assembled self-assembled state was state successfully was successfully solved solved at the atomat the levelatom bylevel cryogenic by cryogenic transmission transmission electron electron microscopy microscopy (cryoTEM) (cryoTEM) techniques techniques [47]. As [47]. shown As shown there, mostthere, of most the amyloidof the amyloid fibril comprisedfibril comprised the β-sheet the β-sheet structures, structures, that is, that the is, cross- the cross-β structures.β structures. In the In cross-the cross-β structuralβ structural motif, motif, the the peptide peptide strands strands folded folded into into (at (at least least partially) partially) elongated elongatedβ β-strands-strands toto self-assembleself-assemble intointo (or(or stack)stack) fibrousfibrous structuresstructures inin whichwhich thethe longlong axisaxis ofof thethe peptidepeptide strandsstrands waswas perpendicularperpendicular toto thatthat ofof thethe fibrousfibrous structures.structures. Conversely, veryvery recently,recently, self-assembledself-assembled fibrousfibrous nanostructuresnanostructures comprisingcomprising anan αα-helix-folded-helix-folded peptidepeptide (the(the cross-cross-αα structures)structures) werewere observedobserved forfor thethe firstfirst timetime [[48,49].48,49]. ThisThis uniqueunique findingfinding andand thethe otherother structuralstructural motifsmotifs ofof thethe peptidepeptide self-assembliesself-assemblies underunder investigation,investigation, suchsuch asas thethe coiled-coilcoiled-coil structuresstructures [[50–52],50–52], couldcould furtherfurther elucidateelucidate thethe designdesign ofof supramolecularsupramolecular peptidepeptide architectures.architectures. FigureFigure 1.1. ((AA)) DNADNAand and ( B(B)) peptide peptide nanotechnologies. nanotechnologies. RepresentativeRepresentative supramolecularsupramolecular architecturesarchitectures (nanostructures)(nanostructures) andand theirtheir typicaltypical component component structuralstructural motifs motifs are are shown. shown. TheThe aboveabove brieflybriefly mentioned mentioned supramolecular supramolecular architectures architectures that that are are composed composed of nucleicof nucleic acids acids or peptidesor peptides could could show show several several advantages advantages in the in research the research fields offields supramolecular of supramolecular architectures. architectures. First of all,First biomolecules of all, biomolecules bear potential bear potential biocompatibility biocompatibility and biodegradability and biodegradability as well as as they well are as versatilethey are andversatile sustainable. and sustainable. In addition, In reliableaddition, automatic reliable automatic synthesis forsynthesis nucleic for acids nucleic and peptidesacids and have peptides been have been established [53–56] so that those with designated length and sequence can be synthesized Int.