Angewandte
Communications
Chemie
How to cite: Angew. Chem. Int. Ed. 2021, 60, 10563–10567
Biosupercapacitors
Hot Paper
Implantable Biosupercapacitor Inspired by the Cellular Redox System
Yongwoo Jang+, Taegyu Park+, Eunyoung Kim, Jong Woo Park, Dong Yeop Lee, and
Abstract: The carbon nanotube (CNT) yarn supercapacitor
has high potential for in vivo energy storage because it can be
used in aqueous environments and stitched to inner parts of the
body, such as blood vessels. The biocompatibility issue for
frequently used pseudocapacitive materials, such as metal
oxides, is controversial in the human body. Here, we report an
implantable CNT yarn supercapacitor inspired by the cellular
redox system. In all living cells, nicotinamide adenine dinucle-
otide (NAD) is a key redox biomolecule responsible for
cellular energy transduction to produce adenosine triphosphate
(ATP). Based on this redox system, CNT yarn electrodes were
fabricated by inserting a twist in CNT sheets with electro-
chemically deposited NAD and benzoquinone for redox
shuttling. Consequently, the NAD/BQ/CNT yarn electrodes
described a DNA-based supercapacitor that was fabricated
from a poly(3,4-ethylenedioxythiophene):poly(styrenesulfo-
nate) (PEDOT:PSS)-coated DNA hydrogel on gold foil.[5]
The DNA-based supercapacitor showed capacitive perfor-
mance in biological fluids, such as artificial urine and
phosphate buffered saline (PBS). More recently, Sim et al.
utilized a ferritin protein as a guest as a supercapacitor. The
ferritin-composite supercapacitor was biscrolled with
PEDOT:PSS in the CNT (carbon nanotube) yarn, which
exhibited the electrical performance of a supercapacitor in
PBS and after in vivo implantation into the abdominal cavity
of a mouse.[6] These supercapacitors are mainly based on
charged biomolecules, such as DNA and ferritin, to increase
their intrinsic capacitance.[7] In the current study, we under-
took the challenge of applying redox-mediated biomolecules
as a pseudocapacitive material, such as metal oxides for
a redox supercapacitor.
In cellular energy transduction, nicotinamide adenine
dinucleotide (NAD) is an essential cofactor and is an electron
carrier in redox reactions.[8] In general, NAD+ is reduced to
NADH during glycolysis in the cytoplasm, and cytosolic
NADH is oxidized by transferring electrons to the electron
transport chain of mitochondria.[8] The conversion of NAD+
to NADH is reversibly regulated by a certain specific enzyme
without a net loss of NAD.[8] Consequently, redox shuttling of
NAD is critical to generate adenosine triphosphate (ATP) in
energy production in all living cells.[9] In fact, NAD-depen-
dent enzymes, such as NAD-dependent glucose dehydrogen-
ase and malate dehydrogenase, have been employed as
anodes for oxidation in enzymatic biofuel cells.[10] As an
enzyme-independent mechanism, benzoquinones (BQs) have
been known to facilitate the oxidation of NADH from 0.0745
to 9220 MÀ1 sÀ1.[11]
In the present study, we describe a flexible biosupercapa-
citor fiber based on the redox system of NAD for implantable
devices. The yarn electrodes for the biosupercapacitor are
fabricated by a biscrolling process inserting a twist in a host
CNT sheet that is overlaid with NAD+ and benzoquinone as
guests. The areal capacitance of the biosupercapacitor is
55.73 mFcmÀ2 in PBS. The areal energy density and power
density are 19.81 mWhcmÀ2 and 446 WcmÀ2, respectively,
which are approximately 27.5 times higher than those of the
guest-free CNT yarn. When operated in the abdominal cavity
of rats, the implanted biosupercapacitor exhibit electrochem-
ical performances similar to the in vitro results in PBS.
The fabrication of NAD/BQ/CNT yarn electrodes is
illustrated in Figure 1A. The yarn biscrolled from the CNT
sheet serves as a current collector and a host material. To
improve the intrinsic capacitance in biological conditions,
a redox molecule, NAD+ was used as a guest material. In
redox reactions, the reduction of two electrons and a proton
exhibited the maximum area capacitance (55.73 mFcmÀ2
)
under physiological conditions, such as phosphate-buffered
saline and serum. In addition, the yarn electrodes showed
a negligible loss of capacitance after 10000 repeated charge/
discharge cycles and deformation tests (bending/knotting).
More importantly, NAD/BQ/CNT yarn electrodes implanted
into the abdominal cavity of a ratꢀs skin exhibited the stable in
vivo electrical performance of a supercapacitor. Therefore,
these findings demonstrate a redox biomolecule-applied plat-
form for implantable energy storage devices.
T
he recent development of wearable electronic devices
enables a platform for monitoring diverse surroundings and
physiological signals on the body.[1] In step with this growth,
flexible and stretchable supercapacitors have been developed
to maintain stable performance and safety.[2] For implantable
electronics, further considerations, such as reliable compati-
bility and stability in biological fluids, are needed in current
supercapacitors. To improve intrinsic capacitance, transition
metal oxides, such as MnO2 and NiO2, have been frequently
used as a pseudocapacitive material.[3] Although these metal
oxides are highly attractive as supercapacitors, they still have
a disadvantage in applications in implantable electronics due
to their poor biocompatibility.[4]
To overcome this biocompatibility issue, several studies
have attempted to apply biomolecules to a supercapacitor to
improve its performance. For example, Hur and colleagues
[*] Y. Jang,[+] T. Park,[+] E. Kim, J. W. Park, D. Y. Lee, Prof. S. J. Kim
Center for Self-powered Actuation and Department of Biomedical
Engineering, Hanyang University
Seoul 04736 (Korea)
E-mail: sjk@hanyang.ac.kr
[+] These authors contributed equally to this work.
Supporting information and the ORCID identification number(s) for
the author(s) of this article can be found under:
Angew. Chem. Int. Ed. 2021, 60, 10563 –10567
ꢀ 2021 Wiley-VCH GmbH
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