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Responsive Materials Through DNA- functionalized Cores for Sensor Applications

Hyunseo Kim,1 Youngeun Kim1,2,*

1Department of Materials Science and Engineering, Seoul National University, Seoul, Republic of Korea 08826
2Research Institute of Advanced Materials, Seoul National University, Seoul, Republic of Korea 08826

Material Matters™ 2024, 19.1

DNA Strands as Nanostructure Building Blocks

DNA, or deoxyribonucleic acid, has revolutionized the field of nanotechnology, offering many advantages for various applications.1 Its unique properties make it an exceptional building block for precisely engineering intricate nanostructures.

One of the most significant advantages of DNA is its programmability. DNA molecules consist of a linear sequence of nucleotide bases—adenine (A), cytosine (C), guanine (G), and thymine (T)—that exhibit specific base-pairing interactions. This characteristic allows for highly precise design and control of DNA sequences. By strategically arranging these nucleotide bases, researchers can create highly specific and complex nanostructures with precise control over their shape and functionality.2

A notable application of DNA’s programmability in nanotechnology is the synthesis of DNA origami structures. DNA origami refers to the folding of a long single-stranded DNA template into complex two- and three-dimensional shapes by utilizing short “staple” strands that bind to the template through complementary base pairing.3 This technique enables the construction of nanostructures with extraordinary precision, including nanoboxes, nanotubes, and even intricate patterns such as smiley faces and maps.3

The programmability of DNA extends beyond origami structures. Researchers can engineer dynamic and functional nanoarchitectures with specific properties and interactions by manipulating the sequence and arrangement of DNA strands. This programmability enables the precise assembly of DNA- functionalized nanoparticles,4,5 where DNA strands are attached to the surface of nanoparticles. These DNA-functionalized nanoparticles can be organized into hierarchical structures through complementary base pairing, creating complex assemblies with enhanced properties and functionalities.

DNA-functionalized Nanoparticles: Synthesis and Functionalization Methods

Nanoparticles are a versatile platform for various nanotechnological applications due to their unique size-dependent properties. Different types of nanoparticles can be employed based on their core compositions, each offering distinct characteristics and functionalities (Figure 1). In the context of DNA-functionalized nanoparticles, several core compositions have gained prominence. Here, we discuss the most prominent types of particles used for DNA functionalization.

The image illustrates the combination of spherical core particles with zig-zag DNA strands to form DNA-functionalized core particles. This visual representation offers insights into the process of functionalizing core particles with DNA strands, a crucial step in the development of advanced materials for various applications, including biosensing, drug delivery, and nanotechnology.
 The illustration depicts four types of DNA-functionalized core particles labeled A, B, C, and D in various colors, showcasing the diversity of DNA-functionalized core particles. These different types of functionalized core particles represent a range of materials, including metallic nanoparticles, MOF structures, hydrogels, proteins, etc., highlighting their potential for tailored applications in nanotechnology, biotechnology, and materials science.
The image presents DNA-functionalized nanoparticles arranged in four lattice structures: face-centered cubic (FCC), body-centered cubic (BCC), hexagonal close-packed (HCP), and simple cubic (SC) lattices. This visual depiction provides valuable insights into the assembly of DNA-functionalized nanoparticles into different crystalline lattice shapes, demonstrating the potential for diverse sensing applications and the creation of advanced materials with tailored structural and functional properties.

Figure 1.Functionalization of different core particles with DNA strands. A,B) Different types of cores (metallic nanoparticles, MOF structures, hydrogels, proteins, etc.) can become densely functionalized with DNA strands. C) DNA-functionalized cores can then become assembled into different crystalline lattice shapes of particle lattices, which then may be used for different sensing applications.

DNA-functionalized Gold Nanoparticles

DNA-functionalized gold nanoparticles have found widespread utility in various fields due to their unique properties and versatility. Gold nanoparticles, typically range from 2 to 100 nanometers, when functionalized with DNA strands, allowing for easy penetration into biological systems, making them valuable tools in targeted drug delivery, biosensing, and imaging applications.6–10

Additionally, the optical properties of gold nanoparticles, such as their surface plasmon resonance, make them excellent candidates for applications in diagnostics, therapeutics, and nanoscale optical devices.11,12

Alivisatos et al. used gold nanoparticles of about 1.4 nm to construct nanoscale crystals.6 In this work, single-stranded DNA strands were adhered to small nanocrystals, and when complementary DNA strands were added, the nanocrystals assembled to form aggregates. Similarly, Mirkin et al. used 13 nm gold nanoparticles and functionalized them with non-complementary DNA strands that contained thiol groups.8 This work emphasized the reversible nature of aggregation of DNA-functionalized nanoparticles. For example, the particles can self-assemble into aggregates when complementary DNA strands are added, and the disassembly process can occur by simply heating the sample.

Macfarlane et al. utilized alkyl thiol-modified oligonucleotides to link 5–80 nm gold nanoparticles to obtain crystalline lattices.11 This work experimentally determined the ‘zone of crystallization,’ which portrayed a precise theoretical relationship between DNA length and gold nanoparticle size, leading to successful crystallization. Another work by Macfarlane et al. suggested six design rules to synthesize nine different structures of crystalline lattices composed of gold nanoparticles (5–60 nm) linked via DNA strands.12 This work demonstrates a way to control particle size, periodicity, and distance between the nanoparticles independently, being one of the first pioneering works to develop DNA-functionalized nanoparticle crystalline superlattices a priori. In a similar work, Nykypanchuk et al. utilized 11.4 nm and 12.5 nm gold nanoparticles linked by complementary DNA strands to form three-dimensional crystalline lattices.9

Sharma et. al. used gold nanoparticles (5–15 nm) to construct “DNA nanotubes”.13 In this work, the authors discovered that different tube shapes could be obtained by changing the sizes of the nanoparticles, therefore leading to a conformational transition between different tube structures. Deng et al. used mono-DNA- functionalized gold nanoparticles of about 5 nm.7 They developed a simple method to assemble DNA-functionalized nanoparticles into one-dimensional arrays a few microns long. Wang et al. utilized 20 nm gold nanoparticles to synthesize a single crystalline, multilayer thin film or glassy film.14 They obtained 3-D nanoparticle structures of arbitrary geometry and dimension.

The functionalization of gold nanoparticles with DNA strands can be achieved through various synthesis methods, offering precise control over their surface properties and interactions. One commonly used method is the covalent attachment of DNA to gold nanoparticles via thiol chemistry.6,8 In this approach, gold nanoparticles are functionalized with thiol-modified DNA strands, which readily bind to the gold surface by forming strong gold-sulfur bonds. Another approach involves electrostatic interactions,6,11 where DNA molecules are adsorbed onto the gold nanoparticle surface through charge-charge interactions. Additionally, non- covalent strategies such as DNA hybridization can be employed, where complementary DNA strands bind to the surface-bound DNA, enabling the attachment of DNA molecules to the gold nanoparticles.

DNA-functionalized Magnetic Nanoparticles

DNA-functionalized magnetic nanoparticles represent a distinct class of nanomaterials that offer unique advantages compared to other metallic nanoparticles. Unlike non-magnetic metallic nanoparticles such as gold or silver, magnetic nanoparticles possess magnetic properties, enabling them to respond to external magnetic fields. This characteristic opens up new possibilities for applications in targeted drug delivery, magnetic resonance imaging (MRI), hyperthermia therapy, and magnetic separation techniques.9,10,15,16

Zhang et al. expanded the scope of core nanoparticles that could be used by developing a generalized technique for attaching DNA strands onto different nanoparticles that are not simply gold nanoparticles.17 This work overcomes the limitation by covering nanoparticles between 7 and 11.7 nm with a coating of amphiphilic polymers containing azide groups. By attaching nucleic acids to the polymer molecules via click chemistry, Zhang et al. first demonstrated that any arbitrary composition of nanoparticles can become densely coated with DNA strands. Zhang et al. continued their research by constructing hybrid crystalline lattices with different compositions of nanoparticles.17 Unlike previous studies on single-component systems, Zhang et al. presented a generalized technique to synthesize binary (heterogeneous) nanoparticle superlattices. The nanoparticles used in this work included plasmonic, magnetic, catalytic, and luminescent particles of about 10 nm.

Feng et al. used streptavidin-functionalized magnetic micrometer- scale beads (also known as dynabeads) of about 1–2.8 um.18 Unlike DNA-functionalized nanoparticles, which are more in the nanometer-scale regime, this work emphasized larger-sized core particles that extend the size regime of DNA-functionalized cores. Further, Feng et al. developed a simple method to produce large quantities of micrometer-sized patchy DNA particles with over 76% yield in just a few hours, which had not been done before.

Functionalizing magnetic nanoparticles with DNA strands involves various methods to achieve precise attachment and control over their surface properties. One common approach is the use of covalent bonding through a linker molecule. A linker molecule with a reactive group, such as amino or carboxyl groups, is first attached to the surface of the magnetic nanoparticles. The DNA strands, modified with a complementary reactive group, are then introduced and allowed to react with the linker molecules, forming stable covalent bonds.

DNA-functionalized Proteins and Enzymes

DNA-functionalized proteins have gained significant attention in biotechnology due to their diverse applications, controlled functionalities, and precise targeting capabilities.2,19–21 DNA- functionalized proteins find utility in targeted drug delivery, biosensing, molecular imaging, and protein engineering. The size ranges of DNA-functionalized proteins can vary depending on the specific protein of interest, spanning from small peptides to large multi-domain proteins. Functionalization methods involve site-specific conjugation of DNA strands to proteins through bioconjugation techniques, such as chemical modification of reactive groups or genetic fusion strategies.

McMillan et al. attached DNA strands onto β-galactosidase of about 17 x 12 x 8 nm.21 The bivalent conjugate contained two DNA strands located on opposite faces, from which a periodic one- dimensional superstructure of proteins could be obtained. Hayes et al. incorporated DNA ligands onto ~10 nm proteins.19 By doing so, Hayes et al. regulated the hierarchical assembly of proteins to obtain various three-dimensional, ordered structures.

Fu et al. demonstrated an interesting experiment of attaching glucose oxidase and horseradish peroxidase enzyme pairs on DNA origami tiles (60 x 80 nm) via complementary DNA strands.22 After varying the distance between the enzymes by 10, 20, 45, and 65 nm to experimentally test the activities of enzymes, they discovered that the activity is enhanced for closely spaced enzymes (at 20 nm).

DNA-functionalized Gels, Lipid Structures, and Cells

DNA-functionalized hydrogels, cells, and lipid structures have emerged as promising platforms in biomaterials and bioengineering. By incorporating DNA strands into these systems,

  1. DNA-functionalized hydrogels offer the ability to precisely control their mechanical properties, swelling behavior, and drug release kinetics through DNA hybridization and self-assembly processes,
  2. DNA-functionalized cells allow for targeted interactions, enhanced cell signaling, and controlled cellular behavior; and 3) DNA-functionalized lipid structures, including liposomes and lipid nanoparticles, offer advantages in drug delivery, gene therapy, and biosensing applications.

Todhunter et al. used cells about 10–20 μm in size and functionalized with degradable oligonucleotide ‘velcro.’23 By doing so, a DNA-programmed cell assembly (DPAC) was made that could quickly and reversibly stick small molecules or other types of cells to the cell surface covered with complementary DNA strands. Li et al. constructed a DNA nanoarchitecture with which they functionalized cells about 15 μm in size.20 As the extracellular environment changes, DNA nanoarchitectures attached to the exterior of the cell membrane could receive cellular stimuli and initiate intercellular reactions.

Qi et al. demonstrated a technique to form an assembly of hydrogel cuboids in 30 μm, 200 μm, 500 μm, and 1 mm.24 This work succeeds in synthesizing diverse assemblies of hydrogel cubes in aqueous and interfacial systems. Li et al. used photopolymerizable prepolymer to generate 100 μm microtissues.25 The microtissues contained various types of cells and were self-assembled via DNA hybridization. Sontakke et al. used polyacrylamide hydrogel blocks in 1–2 mm sizes and suggested a post-polymerization coupling strategy to functionalize hydrogels with DNA strands.26 By adding and removing additional DNA strands, reversible assembly and disassembly of hydrogel blocks were made possible.

According to Stengel et al., although lipid vesicles are crucial for manufacturing membrane protein arrays, the physical properties of lipids make it a demanding task.27 This work was a pioneer in programmable fusing of lipid vesicles via binding of complementary DNA strands. Yang et al. suggested an experimental technique to obtain highly monodispersed liposomes in predesigned 29, 46, 60, and 94 nm sizes.28 Precisely adjusting the liposome’s dimension and shape with preexisting techniques was a demanding task, as Yang et al. insist. This work overcame the bottleneck by attaching lipid molecules to the interior surface of the DNA- origami nanostructures, which led to vesicle formation inside the structure.

DNA-functionalized Metal-Organic Framework (MOF) structures

DNA-functionalized MOFs offer advantages such as enhanced stability, improved selectivity, and controlled release properties.29 These hybrid structures find applications in gas storage and separation, drug delivery, catalysis, and sensing. The DNA functionalization allows for precise targeting, controlled loading and release of guest molecules, and the potential for dynamic structural transformations.

Wang et al. demonstrated the first work using MOF nanoparticles to construct DNA-MOF nanoparticle crystalline superlattices.29By attaching DNA strands to MOF nanoparticles, Wang et al. could generate “single-component MOF superlattices, binary MOF-Au single crystals, and two-dimensional MOF nanorod assemblies.” In another work, Wang et al. suggested that previous techniques using covalent conjugation or DNA modification for attaching DNA strands to MOFs are quite inefficient.30 Instead, their work utilized the interactions between phosphate groups of DNA strands and Zr sites on MOFs to mediate linkage between DNA strands and MOFs.

DNA-functionalized Microparticles

DNA-functionalized microparticles are a versatile class of biomaterials with a wide range of applications. These microparticles, typically ranging in size from a few micrometers to hundreds of micrometers, are functionalized with DNA strands that enable specific binding, controlled interactions, and targeted functionalities.15,31–34 DNA-functionalized microparticles find utility in various fields, including biosensing, drug delivery, and tissue engineering. The DNA strands can act as gatekeepers, controlling the release of encapsulated drugs or therapeutic agents from microparticles. In addition, the large surface area of microparticles provides ample space for DNA functionalization, enabling multiplexing and simultaneous detection or delivery of multiple targets.

Dreyfus et al. used 1.05 um polystyrene Dynabeads coated with DNA strands with sticky ends, DNA strands with nonsticky ends, and polymer brushes that sterically stabilize nanoparticles.35 This work offered a quantitative model of the interactions and thermodynamics of DNA-mediated assembly of colloids, which was insufficient beforehand. Dreyfus et al. emphasized that the entropy cost occurs during colloidal network formation because the configurational freedom of hybridized DNA strands decreases.

Zhang et al. used 3.7–4.7 μm colloidal particles (droplets).36 This work established a technique for obtaining sequential self or directed assemblies of droplets linked with DNA strands. Tang et al. investigated DNA-mediated self-assembly of 6 μm polystyrene microspheres.33 Their work discovered that a DNA strand length of 50 bp showed maximum efficiency of self-assembly and that the reaction can be driven almost entirely by using stoichiometric excess of microspheres.

Gartner et al. used cells of about 10–12 μm, densely functionalized with oligonucleotides.37 In this work, cell-to-cell adhesion was made possible by hybridization between complementary DNA strands, and a technique to formulate a paracrine signaling network was suggested.

DNA-mediated Self-assembly and the Formation of Superlattice Structures

Lattice Structures Synthesized from DNA-functionalized Cores

DNA-functionalized nanoparticles can undergo programmed self- assembly driven by the specific base-pairing interactions of DNA strands. By designing complementary DNA sequences on different nanoparticles, they can selectively bind to each other and form well-defined superlattice structures. The programmability of DNA allows for the precise control of particle arrangement, creating intricate patterns and architectures. DNA-functionalized nanoparticles can form a wide variety of lattice structures, such as face-centered cubic (FCC), body-centered cubic (BCC), hexagonal close-packed (HCP), and simple cubic (SC) lattices, by carefully designing the complementary DNA sequences and controlling the assembly conditions.4,5,12,15,16,38,39 These superlattice structures offer unique geometric arrangements and present distinct material properties, including photonic bandgaps, plasmonic coupling, and electronic transport phenomena.

Control Over Lattice Structures and Interparticle Distances

The precise control over superlattice structures and interparticle distances is crucial for tailoring the properties and functionalities of DNA-functionalized nanoparticle assemblies. Factors such as the length and flexibility of the DNA strands, the ratio of different nanoparticle types, and the assembly conditions, including temperature and ionic strength, influence the resulting superlattice structure. By adjusting the DNA strand lengths, researchers can tune the interparticle distances, leading to changes in the optical, electronic, and magnetic properties of the superlattice.39 Additionally, introducing DNA linkers of different lengths or incorporating DNA spacers between nanoparticles can further modify the interparticle spacing and arrangement.4–42

In addition to interparticle distances, the orientation and alignment of the nanoparticles within the superlattice can be controlled. By designing the DNA sequences to have different binding affinities, selective binding of nanoparticles can be achieved, allowing for the formation of anisotropic superlattice structures. These anisotropic assemblies exhibit unique properties in specific directions, enabling tailored material properties for desired applications.38

Jones et al. assembled anisotropic particles that were functionalized with DNA strands.38 In this work, DNA strands were attached on the surface of ~50 nm anisotropic particles, in the shapes of a rod, a prism, a rhombic dodecahedron, and octahedra. These inherent shapes and DNA interactions directed anisotropic particles to assemble into 1D, 2D, and 3D structures previously unachievable using spherical particles.

Lee et al. constructed a DNA-mediated CsCl-type colloidal superlattice using polystyrene-b-poly(ethylene oxide) in the range of 55–150 nm.43 The DNA-polymer particles with complementary DNA sequences were assembled and disassembled. Lin et al. used triangular bipyramid particles as particle cores and attached DNA strands.31 By doing so, Lin et al. obtained at least three different clathrate structures. Ducrot et al. used preassembled colloids (500–700 nm) with tetrahedral or spherical shapes to construct superstructures.44

Conclusion and Future Perspectives

One of the remarkable features of DNA-functionalized nanoparticles is their stimuli-responsive behavior, which allows for dynamic control and manipulation of their properties and interactions. By exploiting the inherent properties of DNA and the responsiveness of certain stimuli, researchers have developed DNA-functionalized nanoparticles that can undergo structural changes on demand, exhibit stimuli-responsive lattice changes, and enable dynamic control over their properties. The reversible nature of DNA hybridization41 allows for the formation and dissociation of these cores in response to changes in their environment, such as changes in temperature40 or pH.42 These stimuli-responsive, dynamic systems offer opportunities for applications in areas such as biosensing, drug delivery, smart materials, and nanoscale devices. The ability to finely tune the properties and interactions of DNA-functionalized nanoparticles in response to external stimuli opens exciting avenues for developing advanced and intelligent nanotechnology solutions.

While DNA-functionalized nanoparticles hold great promise for various applications, several challenges still need to be addressed to fully realize their potential. One of the key challenges in using DNA-functionalized nanoparticles is their stability and susceptibility to degradation, especially in biological environments. Another challenge in DNA-functionalized nanoparticles is the scalability and manufacturing of these complex structures on larger scales. Furthermore, it would be interesting to expand the library of cores beyond solid materials to become functionalized with DNA strands. For example, attaching DNA strands onto cellulose, paper, smaller framework structures,29 or even liquid metal may lead to new and exciting discoveries and applications.

With continued research and development, DNA-functionalized nanoparticles are poised to play a pivotal role in advancing nanotechnology and creating next-generation smart and responsive materials and devices.

Acknowledgment

This work was supported by the New Faculty Startup Fund from Seoul National University and the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (NRF-0417-20220165).

 

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