Enzyme Catalysis To Power Micro/Nanomachines

Abstract

Enzymes play a crucial role in many biological processes which require harnessing and converting free chemical energy into kinetic forces in order to accomplish tasks. Enzymes are considered to be molecular machines, not only because of their capability of energy conversion in biological systems but also because enzymatic catalysis can result in enhanced diffusion of enzymes at a molecular level. Enlightened by nature's design of biological machinery, researchers have investigated various types of synthetic micro/nanomachines by using enzymatic reactions to achieve self-propulsion of micro/nanoarchitectures. Yet, the mechanism of motion is still under debate in current literature. Versatile proof-of-concept applications of these enzyme-powered micro/nanodevices have been recently demonstrated. In this review, we focus on discussing enzymes not only as stochastic swimmers but also as nanoengines to power self-propelled synthetic motors. We present an overview on different enzyme-powered micro/nanomachines, the current debate on their motion mechanism, methods to provide motion and speed control, and an outlook of the future potentials of this multidisciplinary field.

Keywords: enzyme catalysis; micro/nanomachines; nanomotors; self-propulsion; synthetic motors.

Scheme 1. Schematic Illustration of Enzyme-Powered Micro/Nanomachines

Figure 1

(A) ATP synthase 3D structure. Reprinted with permission from ref (31). Copyright 2001 Nature Publishing Group. (B) Direct observation of F1-ATPase rotation movement by coupling a fluorescence actin filament. Reprinted with permission from ref (35). Copyright 1998 American Association for the Advancement of Science. (C) Conformational changes during ATP synthesis. Reprinted with permission from ref (39). Copyright 2013 Nature Publishing Group. (D) Schematic representation of urease self-diffusion enhancement by catalysis and diffusion coefficients of urease when exposed to increasing substrate concentrations. Reprinted from ref (3). Copyright 2010 American Chemical Society. (E) Conformational changes of adenylate cyclase measured by single-molecule force spectroscopy. Reprinted with permission from ref (49). Copyright 2016 Nature Publishing Group. (F) Diffusion coefficient of catalase as a function of the laser power (402 nm) and schematic representation of enzyme motion driven by chemoacoustic effect. Reprinted with permission from ref (5). Copyright 2014 Nature Publishing Group.

Figure 2

DNA-based micro/nanomotors powered and controlled by different classes of enzymes. (A) DNA rolling motor (a) with motion powered by RNase H (b). Reprinted with permission from ref (13). Copyright 2015 Nature Publishing Group. (B) Control of cargo loading and release by a pH-sensitive DNA switch using proton-producing/proton-consuming enzymes. Reprinted from ref (55). Copyright 2015 American Chemical Society.

Figure 3

Enzyme-powered nanomotors. (A) Janus hollow mesoporous silica nanomotors powered by individual enzymes: (a) TEM and (b) SEM images of HMSNPs; (c) SEM image of JHMSNP-catalase; (d) schematic illustration of the force measurement by optical tweezers and (e) force spectral density as a function of frequency for JHMSNP-catalase nanomotors. Reprinted from ref (60). Copyright 2015 American Chemical Society. (B) Supramolecular assembly of the enzyme-driven polymeric stomatocyte nanomotors; inset is the TEM image of the polymeric stomatocytes (scale bar: 200 nm). Reprinted from ref (14). Copyright 2016 American Chemical Society.

Figure 4

Enzyme-powered micromotors. (A) (a) Enzymatic micromotor fully coated with catalase or urease. Reprinted from ref (16). Copyright 2015 American Chemical Society. (b) Janus microparticle half-coated with (iii) catalase/(iv) GOx (scale bar: 1 μm). Reprinted from ref (65). Copyright 2015 American Chemical Society. (B) (a) Schematic illustration and urea-dependent velocity of biocompatible Janus microcapsule motors. Inset is a SEM image of a single Janus microcapsule motor. Reprinted from ref (66). Copyright 2016 American Chemical Society. (b) Schematic illustration of a phoretic micromotor driven by asymmetric enzymatic reactions. Reprinted with permission from ref (43). Copyright 2005 American Physical Society. (C) Enzyme catalase-based bubble propulsion of (a) rolling up microtubular motor (reprinted from ref (67); copyright 2010 American Chemical Society); (b) Janus mesoporous silica cluster motor (reprinted with permission from ref (57); copyright 2015 Royal Society of Chemistry), and (c) Janus self-assembled polymeric capsule motor (reprinted from ref (72); copyright 2014 American Chemical Society).

Figure 5

Motion control of enzymatic micro/nanomotors. (A) Schematic of microfluidic setup showing corresponding chemotaxis shifting of catalase and urease motors toward the high concentration area of corresponding fuels. Reprinted from ref (4). Copyright 2013 American Chemical Society. (B) (a) Schematic illustration and plots of motion control on urea-powered microcapsule motors by inhibiting and reactivating the enzymatic activity; (b) directional guidance on the microcapsule motors by remote magnetic control. Reproduced from ref (66). Copyright 2016 American Chemical Society.

Figure 6

Fluid flow induced by enzymatic pumping and enzymatic pumps as environmental sensors. (A) Schematic design of an enzymatic pump setup is presented: the enzyme is conjugated onto a gold pattern through a SAM, and tracer particles of a known size are used to determine the fluid flow. Reprinted with permission from ref (17). Copyright 2014 Nature Publishing Group. (B) Proposed mechanisms of fluid convection in enzyme-powered micropumps. Reprinted with permission from ref (80). Copyright 2016 Proceedings of the National Academy of Sciences of the United States of America. (C) Inverted setup is presented, giving insight into the pumping mechanism. Reprinted from ref (78). Copyright 2014 American Chemical Society with permission.