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DNA-based assembly lines and nanofactoriesFriedrich C Simmel

Available online at www.sciencedirect.com

With the invention of the DNA origami technique, DNA self-

assembly has reached a new level of sophistication. DNA can

now be used to arrange molecules and other nanoscale

components into almost arbitrary geometries — in two and

even three dimensions and with nanometer precision. One

exciting prospect is the realization of dynamic systems based

on DNA, in which chemical reactions are precisely controlled by

the spatial arrangement of components, ultimately resulting in

nanoscale analogs of molecular assembly lines or

‘nanofactories’. This review will discuss recent progress toward

this goal, ranging from DNA-templated synthesis over artificial

DNA-based enzyme cascades to first examples of ‘molecular

robots’.

Address

Lehrstuhl fur Bioelektronik, Physik-Department der TU Munchen,

Germany

Corresponding author: Simmel, Friedrich C ([email protected])

Current Opinion in Biotechnology 2012, 23:1–6

This review comes from a themed issue on

Nanobiotechnology

Edited by Fernando de la Cruz and Geoffrey Gadd

0958-1669/$ – see front matter

Published by Elsevier Ltd.

DOI 10.1016/j.copbio.2011.12.024

Introduction: DNA nanotechnologyAlready in the early 1980s, Nadrian Seeman realized that

DNA might also be used in a non-biological context — as

a material for molecular ‘construction’ [1]. The basis of

DNA nanotechnology is the well-known fact that two

molecules of DNA pair up to form a double helix, when

their base sequences are complementary. DNA duplexes

are relatively rigid molecules on the nanoscale and hence

are used as molecular ‘beams’ for nanoconstruction

(Figure 1a). Linear assemblies are only of limited use,

and so a variety of branched DNA structures have been

developed for DNA nanotechnology. Many DNA ‘lat-

tices’ are based on DNA four-way junctions, which are

derived from the biological ‘Holliday crossover’ struc-

tures. One of the milestones of the field was the creation

of extended DNA lattices from DNA ‘tiles’ that were

formed from two such crossover structures fused together

[2]. Later on, more complicated structures such as

‘crossbar tiles’ were developed that allowed for larger

assemblies (Figure 1b) [3,4]. DNA nanotechnology has

Please cite this article in press as: Simmel FC. DNA-based assembly lines and nanofactories, Cu

www.sciencedirect.com

significantly gained momentum since the demonstration

of the ‘origami’ technique by Rothemund in 2006 [5��]. In

contrast to previous DNA assembly strategies that were

based on the association of many short oligonucleotides to

create a larger structure, DNA origami utilizes a long

single-stranded DNA ‘scaffold strand’ (Figure 1c). A large

number of rationally chosen ‘staple strands’ is added to

the scaffold and crosslinks it to fold into a specific mol-

ecular shape. This approach has turned out to be extra-

ordinarily robust and efficient. Variations of the basic

origami principle have been later adopted for the con-

struction of objects in 3D [6��,7�,8–10].

The specific mechanical properties of DNA molecules

together with ‘reversible’ hybridization reactions have

also been utilized for the construction of various

machine-like molecular assemblies [11] that can be con-

trollably switched between several conformations or

‘states’. Such DNA-based switches are expected to find

application as autonomous biosensors in biomedicine, or

as actuators for DNA-based molecular motors and robots.

Using chemically modified DNA strands, DNA assem-

blies can be used to arrange nanoscale objects or mol-

ecules into well-defined geometries, with nanoscale

precision. One promising application is to use this capa-

bility for the precise control and optimization of chemical

reactions, and the realization of molecular ‘nanofactories’.

Reaction kinetics: proximity and geometryIn biology many chemical processes occur with extraordi-

nary specificity and efficiency. One aspect that markedly

differentiates biological processes from conventional

chemistry ‘in a beaker’ is spatial organization and com-

partmentalization. Spatial organization may influence

reaction kinetics in a variety of ways. Holding two com-

pounds in close proximity will increase the rate at which

they attempt to react with each other. This is important

for reactions with high activation barrier, or when the

reactants are only present at low concentrations and have

a low probability to meet in the first place. If in addition

one can control the orientation of reactants with respect to

each other, these may be arranged in an optimum geo-

metry to facilitate bond formation.

A more complicated situation arises when reaction cas-

cades with several consecutive steps and intermediate

compounds are considered. Such intermediates can be

unstable or toxic; they can diffuse away or react with other

species. Compartmentalization and spatial organization is

thought to prevent side-reactions and to increase local

concentrations of reactants and therefore improve the

rr Opin Biotechnol (2012), doi:10.1016/j.copbio.2011.12.024


http://dx.doi.org/10.1016/j.copbio.2011.12.024

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2 Nanobiotechnology


Figure 1

(a) (b)

2 nm 17.6 nm 10.9 nm

(c)

Current Opinion in Biotechnology

DNA as a nanoscale building material. (a) DNA double helices are structurally rigid on the nanometer scale. (b) Many short DNA molecules can be

‘woven together’ to form supramolecular lattices. (c) In DNA origami, many short ‘staple strands’ (green/blue) hold together a long single-stranded

‘scaffold strand’ (gray). For clarity the double helical nature of DNA is not shown in detail here.

reaction flux through such cascades. In the context of

multi-enzyme complexes, these effects have been termed

‘metabolic channeling’ [12�].

The effect of spatial arrangement strongly depends on the

physical process under consideration. Formation of

covalent bonds takes place on a sub-nm scale — this level

of control corresponds to the organization of ‘active

centers’ of many enzymes. Electron transfer reactions

that involve tunneling of electrons typically occur over

the distance of one or a few nanometers, energy transfer

between electric dipoles has a longer range and occurs on

a scale of several nanometers. For diffusive processes one

has to consider reactant concentrations and typical time

scales of a system. Quite generally, spatial arrangement

for reactions involving diffusion is only expected to play a

role for low concentrations and small diffusion coeffi-

cients — or in crowded environments [13].

DNA-directed synthesisThere are different levels of organization that DNA

nanotechnology may provide for the control of chemical

reactions: proximity, spatial order in one dimension, and

geometrical arrangement in two or even three dimen-

sions. In DNA-directed synthesis, two DNA-linked reac-

tants are brought into close proximity by hybridization to

a complementary template strand (Figure 2a). This

increases the effective concentration of the reagents

and therefore their reaction rate [14,15]. In principle,

DNA-directed synthesis can also be used to translate

a DNA sequence into artificial sequences composed

of other molecules. This has been employed for

sequence-controlled multistep synthesis [16] and also

for the realization of small-molecule libraries for combi-

natorial chemistry [17–21]. In DNA-templated synthesis,

the reactants are not held firmly in place — they simply



sample conformations and orientations by diffusion until

they react. This is somewhat controlled by the point of

attachment, the length and mechanical properties of the

linker through which the reactants are connected to the

DNA scaffold. The extreme specificity of many naturally

occurring enzymes arises from the precise spatial arrange-

ment of the reactants to each other, which results from the

binding of substrates to the enzymes’ catalytic center. In

principle it should be possible to also construct ‘artificial

binding pockets’ using the three-dimensional origami

technique. Chemically modified DNA staple strands

could present functional groups that arrange and orient

reactants for a reaction within the pocket.

Reaction cascades and multi-enzymesystems in biologyMany chemical systems in biology are organized on a

scale larger than the reactive centers of single enzymes,

for instance within multi-enzyme complexes. A variety of

such complexes are known to carry out intricate biosyn-

thetic tasks, for which several catalytic steps have to be

performed ‘in series’, and the substrate is passed from one

catalytic site to the next without escaping to the bulk

phase. Such ‘channeled’ intermediates cannot participate

in competing reaction pathways, and they are present in a

higher local concentration than in the bulk. Arrangement

of enzymes tightly links the catalytic steps and therefore

also balances the flux through an enzyme cascade.

As a famous example, tryptophan synthase catalyzes the

formation of tryptophan from indole-3-glycerol phos-

phate in two catalytic steps. The two catalytic sites are

connected via an intramolecular tunnel of �2 nm length,

through which indole — the reaction intermediate — is

transferred [22,23]. Another example for multistep cata-

lysis in a closed enzyme complex is found in fatty acid




DNA-based assembly lines and nanofactories Simmel 3


Figure 2

(a)

AB BA

(b)


Arranging chemical components with DNA molecules into close proximity allows for the control of chemical and enzymatic reactions. (a) Principle of

DNA-directed synthesis: DNA strands are modified with chemical moieties A and B. Hybridization to a complementary scaffold places A and B next to

each other and allows them to react. (b) The turnover of a multi-enzyme reaction can be enhanced by placing the enzymes into close proximity.

synthesis. Fungal fatty acid synthase, for example, is a

barrel-shaped reaction compartment, which contains all

the catalytic subunits required for the synthesis of fatty

acids [24]. While metabolic channeling undoubtedly

plays a role in such ‘closed’ complexes, it is less obvious

whether it is also important for enzymes that are simply

co-localized, and where intermediates can diffuse away

and mix with the bulk.

Apart from kinetic considerations, another benefit of

spatial arrangement of enzymes can be the concerted

action of several complementary enzymes to synergisti-

cally perform a complex chemical task. A well-known

example for this is the cellulosome — a huge enzyme

complex found in anaerobic bacteria that breaks down

plant cell walls [25].

Other examples of spatial organization are found in

signaling cascades, where molecular signals progress

along a chain of kinases that are aligned on scaffold

proteins [26]. Similar to the case of metabolic cascades,

the benefits of spatial organization are reduction of

crosstalk, context-dependent response, and speedy

transmission. Finally, another type of spatial position-

ing is found in photosynthetic light-harvesting and

reaction complexes, where efficient charge and energy

transfer reactions are achieved by the precise tuning of

distances and energies of chlorophylls and other mol-

ecules [27].



Artificial enzyme cascadesThe idea of artificially co-localizing enzymes to improve

reaction flux has already been attempted using a variety

of different approaches. Enzyme systems have been

immobilized on a variety of solid matrices, resulting in

an improved transfer of intermediate substrates under

certain conditions [28,29]. Other attempts were made to

enforce co-localization by chemically linking several

enzymes of interest to scaffolds, by recombinant engin-

eering of fusion proteins [30�], or by the utilization of

protein–protein interaction domains [31].

In the past decade, there have also been first attempts to

utilize DNA scaffolding for the creation of artificial multi-

enzyme systems (Figure 2b). Niemeyer and coworkers

[32�] first arranged NADH:FMN oxidoreductase and

luciferase onto double-stranded DNA scaffolds using

biotin–streptavidin linkages, later they also used enzymes

covalently linked to DNA to produce systems from glu-

cose oxidase (GOX) and horseradish peroxidase (HRP)

[33]. In each case, an improved performance was observed

when the cooperating enzymes were held in proximity.

The first example of enzyme systems arranged on a larger

supramolecular DNA scaffold was demonstrated by Will-

ner and coworkers [34�]. Also using the GOX/HRP sys-

tem, they reported a significant increase in overall

activity, when the two enzymes were placed in close

proximity. In addition, they also immobilized glucose

dehydrogenase and its tethered cofactor NAD+ on the




4 Nanobiotechnology


Figure 3

(a)

(c)

(b)


DNA nanostructures such as DNA origami provide a higher level of spatial control than simple arrangements along linear scaffolds. (a) Components of

a more complex pathway can be arranged into close proximity on DNA origami (DNA double helices are represented as bars here). Choosing the

correct ‘stoichiometry’ on the platform may help to balance reaction fluxes. (b) To avoid diffusive loss of reaction intermediates to the bulk,

components may also be encapsulated into artificial reaction chambers (here a chamber made of a multi-helix bundle is indicated). (c) Many different

components can be brought together in an origami-based ‘nanofactory’. Here, molecular walkers transport components between two reaction centers

to prevent loss by diffusion. Other components such as nanoparticles are easily integrated into such assemblies.

scaffold, and observed different activities for different

tether lengths and distances. As could be expected,

researchers are now beginning to study enzymes

immobilized on origami structures [35]. Another impress-

ive recent achievement in this context is the assembly of a

multi-enzyme complex along an aptamer-containing

RNA scaffold in Escherichia coli [36��].

What advantages does DNA scaffolding have to offer over

approaches such as direct chemical linking of enzymes or

protein engineering? For one, DNA assembly is very

flexible — it is straightforward to systematically vary dis-

tances between enzymes, their order and stoichiometry

on a DNA scaffold. This could be used for ‘fast proto-

typing’ of enzyme cascades to find optimum configur-

ations. One major strength of DNA-based assembly is its

potential to produce two-dimensional and even three-

dimensional arrangements. Rather than only placing

enzymes into close proximity, DNA could help to pre-

cisely define the geometry of multi-enzyme assemblies

(Figure 3a). For instance, a ‘donor’ enzyme could be

surrounded by other ‘acceptor’ enzymes to increase the

capture probability of diffusing intermediates, or one

could tether a substrate carrying ‘arm’ close to a row of



enzymes that consecutively modify the substrate. With

3D origami it should even be possible to mimic closed

enzyme assemblies such as fatty acid synthase, in which

all members of an enzyme-cascade reside within a supra-

molecular reaction chamber (Figure 3b).

An important advantage of enzyme cascades based on

fusion proteins is their use within metabolically engin-

eered cells [30�]. In contrast to chemical methods —

including DNA self-assembly — once a successful

multi-enzyme construct has been realized, its synthesis

can be easily scaled up for large-scale production using

biotechnological tools. With the further development of

in vivo RNA nanotechnology [36��,37], however, the

benefits of the two different approaches may actually

be combined.

Controlling charge and energy transferOrganization of molecules along a DNA scaffold may also

be used to control other physicochemical processes that

may play a role in future ‘nanofactories’. One of the

visions here is to mimic biological light-harvesting com-

plexes and also photocatalytic energy conversion such as

in photosynthetic reaction centers. There are a large




DNA-based assembly lines and nanofactories Simmel 5


number of publications on the organization of chromo-

phores and energy transfer along linear DNA scaffolds

(e.g. [38,39]), and there have been many studies on charge

transport through DNA [40]. These studies have

been recently extended to more elaborate DNA nano-

constructs. For instance, Dwyer et al. studied energy

transfer between three chromophores immobilized on

a self-assembled DNA grid [41], while Tinnefeld and

coworkers demonstrated FRET cascades with four fluor-

ophores on a planar DNA origami structure [42]. More

recently, Liu and coworkers reported on the fabrication

of a ‘light-harvesting system’ based on fluorophores

assembled around a DNA helix bundle [43�].

Molecular robots and assembly linesAn exciting development of the past years are first

attempts to couple the mechanical motion of DNA-based

nanodevices to chemical synthesis. For instance, Chen

and Mao showed that mechanical switching of a DNA

nanodevice can be used to ‘choose’ between two alterna-

tive reactions [44]. More recently, He and Liu demon-

strated how a DNA ‘walker’ autonomously performed

DNA-templated multistep synthesis by carrying a DNA-

linked compound through a series of reactive ‘sites’

arranged along a track [45�]. Their system worked faster

and more efficiently than previous DNA-directed multi-

step syntheses. Also using a DNA walking device, Gu

et al. constructed an origami-based ‘molecular assembly

line’ that could programmably collect different combi-

nations of gold nanoparticles [46��]. Their combination of

mechanical motion and programmable assembly already

very much resembles macroscale production lines, along

which programmable industrial robots put together parts

to manufacture a composite product. In this sense, these

recent developments are more ‘technomimetic’ than

‘biomimetic’.

ConclusionsIn the past years, DNA has been proven to be an extra-

ordinary material for the assembly of complex molecular

architectures. Moreover, DNA has also been shown to be

capable of directing chemical reactions resulting in

increased reaction efficiencies and a new approach for

combinatorial chemistry. Researchers have begun to

arrange enzymes into artificial reaction complexes, and

DNA nanomachines have been used to control chemical

synthesis and assembly processes. With the power of

DNA origami, much more complex systems seem to be

feasible in the future.

Probably the main strength of DNA-based assembly

is its flexibility in design. As indicated in this review,

DNA self-assembly could be utilized to integrate many

different components and physicochemical processes

within one system. For instance, multi-enzyme systems

could be arranged within artificial origami-based

reaction chambers, and their reactions could be coupled



to photo-induced electron and energy-transfer processes,

which progress along artificial DNA-based antenna sys-

tems and electron transport chains. Programmable DNA-

based motors and machines could then help to shuttle

molecular components between such reaction centers,

making the vision of a nanofactory quite seizable

(Figure 3c).

Potential applications of such ‘nanofactories’ can be

found in many different areas. Optimized enzymatic

reaction pathways might be used for the production of

novel drugs or biofuels, or for biodegradation. Integration

with sensor and computational functions may result in

‘autonomous’ nanodevices that are capable of context-

dependent behavior, with possible applications in nano-

medicine or in other complex, changing environments.

For practical use, many of these applications will require a

reduction in cost of DNA nanostructures and strategies

for scaling up their synthesis. This might be achieved by a

more extensive utilization of biotechnological tools, for

example, for in vivo production of nucleic acid scaffolds,

or by a standardization of origami ‘parts’.

AcknowledgementsThe author acknowledges support through the DFG Cluster of ExcellenceNanosystems Initiative Munich (NIM).

References and recommended readingPapers of particular interest, published within the period of review,have been highlighted as:

� of special interest

�� of outstanding interest

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6 Nanobiotechnology


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46.��

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