Forces in Mechanics 2 (2021) 100008

Contents lists available at ScienceDirect

Forces in Mechanics
journal homepage: www.elsevier.com/locate/finmec

Analysis of vibration behavior in single strand DNA-wrapped single-walled

carbon nanotubes adhered to lipid membranes
Daisuke Miyashiro a,b,∗, Ryo Hamano a, Hisao Taira c, Kazuo Umemura a
a
Department of Physics, Graduate School of Science, Tokyo University of Science, 1-3 Kagurazaka, Shinjuku-ku, Tokyo, Japan
b
ESTECH CORP., 2-7-31 Fukuura, Kanazawa-ku, Yokohama, Japan
c
Faculty of Education, Hokkaido University of Education, 5-3-1-5 Ainosato, Kita-ku, Sapporo, Hokkaido 002-8502, Japan

a r t i c l e i n f o a b s t r a c t

Keywords: Single strand DNA-wrapped Single-walled carbon nanotubes (ssDNA-SWCNTs) have critical biomedical applica-
Single-walled carbon nanotubes tions such as drug delivery, bio-imaging and bio-sensing; therefore, the mechanical interaction between ssDNA-
Single-stranded DNA SWCNTs and lipid membranes is an important research topic. Several studies have experimentally demonstrated
Lipid membranes
that depending on the length of ssDNA-SWCNTs penetrate the lipid membranes. However, few studies have an-
Vibration behavior
alyzed the mechanism of the mechanical interaction of this process. In addition, simulation approaches, such as
molecule dynamics (MD) with long SWCNTs, are time-consuming. In this study, we examined the mechanical in-
teraction by analyzing the vibration behavior of ssDNA-SWCNTs at difference lengths from 25 to 200 nm adhered
to the lipid membranes considering effect of the damping and mass in water. In order to evaluate the vibration be-
havior between ssDNA-SWCNTs and lipid membranes, the frequency response functions of them was investigated
by the modal analysis method. As a result, we found that ssDNA-SWCNTs shorter than 100 nm can efficiently
transmit force on the lipid membranes. On the other hand, ssDNA-SWCNTs longer than 100 nm interfere with the
efficient transfer of force to the lipid membranes due to the damping resistance in water accompanied by ssDNA
vibration on the SWCNTs.

1. Introduction
Carbon nanotubes (CNTs) have been widely used as composites for
sensor [1], filler material for fiber reinforcement [2], supercapacitances
device and biomedical materials [3,4] due to a dispersion technology
such as various surfactants, nanocellulose [5] and DNA [6,7]. In partic-
ular, single-walled carbon nanotubes (SWCNTs) have uniquely optical
properties such as light emission and absorption in the near infrared
(NIR) region, which is harmless to human body; thus, they are expected
to have for a variety of biomedical applications shown in Fig. 1, such
as drug delivery systems, bio-imaging and sensing technologies. For ex-
ample, SWCNTs can be visualized by computed tomography and NIR
light fluorescence in vivo [8,9], and are shown to be deposited on the
cell surface or penetrating them because of their enhanced permeability
and retention (ERP) effect that enables a nanomaterial of several hun-
dred nm to accumulate in cancer cells [10]. Smith et al. have shown that
SWCNTs are almost exclusively taken up by a single immune cell subset
and delivered to the tumor [11]. However, high aspect ratio materials,
such as SWCNTs taken up by cells, have been shown to cause length-
dependent toxicity in certain cells [12]. Depending on the dimensions
such as the length of SWCNTs, it may damage a cell or cause toxicity.
Becker et al. showed that the DNA wrapped SWCNTs that can stably be
dispersed in water can penetrate the lipid membranes when the length is
under the threshold of 187nm [13]. Furthermore, Kam et al. showed that
the subcellular localization and uptake of carbon nanotubes on the lipid
membranes was strongly dependent on the physical size of the material.
In particular, SWCNTs of lengths 100–200 nm is only internalized in the
cytoplasm, whereas SWCNTs of lengths 50–100 nm reside partly in the
cell nucleus [14]. This implies that short SWCNTs behave as straight
nano-needles and can penetrate lipid membranes more efficiently and
that the natural frequency and vibration amplitude, which are largely
dependent on the length of SWCNTs, are considered to be involved in
these mechanisms. Thus, the length of SWCNTs is an important param-
eter for the toxicity to cells and cancer treatment. To put SWCNTs into
practical use in biomedical applications, understanding the mechanism
of mechanical interaction between SWCNTs and the lipid membranes is
important for ensuring safety and durability toward variety application.
At present, the mechanism of SWCNTs uptake presumed to occur
on the lipid membranes includes endocytosis, phagocytosis, and pas-
sive diffusion. Endocytosis is known to allow cells to take up nanoscale
structures through vesicle formation, while phagocytosis is known to
take up larger particles such as bacteria (1 𝜇m). Passive diffusion may

∗
Corresponding author at: Department of Physics, Graduate School of Science, Tokyo University of Science, 1-3 Kagurazaka, Shinjuku-ku, Tokyo, Japan.
E-mail address: daisuke.miyashiro@estech.co.jp (D. Miyashiro).

https://doi.org/10.1016/j.finmec.2020.100008
Received 4 August 2020; Received in revised form 18 October 2020; Accepted 28 November 2020
Available online 8 December 2020
2666-3597/© 2020 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/)
D. Miyashiro, R. Hamano, H. Taira et al.
Fig. 1. Conceptual diagram biomedical application of ssDNA-SWCNTs.
cause SWCNTs to penetrate the lipid membranes like needles. Various
studies have been conducted with experimental analyses to verify these
hypotheses. Pantarotto et al. concluded that SWNCT uptake occurred by
passive diffusion even when SWCNTs were co-cultured with cells at 4°C
where endocytosis was unlikely since SWCNTs uptake was not prevented
[15]. On the other hand, Kam et al. was shown that SWCNTs were in-
ternalized into cells even when a compound (Filipin, Nystatin) that pre-
vents invasion of a substance by passive diffusion was added together
with SWCNTs [16]. Thus, Kam et al. reported that the major mechanism
by which DNA-SWCNTs were internalized was energy-dependent endo-
cytosis because SWCNTs were observed in endosomes [17]. In addition,
Porter et al. reported that acid-treated SWCNTs are taken up by phago-
cytosis since they can be imaged inside the phagosomes, cytoplasm and
lysosomes [18,19]. These phenomenon by which SWCNTs penetrates
lipid membranes has been studied from various approaches, but the
mechanism remains inconclusive. Although the mechanical interaction
between SWCNTs and lipid membranes is inevitable with either process,
the vibration behavior of their interaction is not well investigated.
The vibration behavior between SWCNTs and the lipid membranes
can be investigated using a numerical simulation study because it is
difficult to extract only the vibrational characteristics and behavior of
SWCNTs from the dispersion liquid containing various impurities, and to
measure the effects of SWCNTs length and adsorbed molecules. Molecu-
lar dynamics (MD) method is a popular method for simulation research
on SWCNTs and lipid membranes. For instance, Zhu et al. [20] and Shi
et al. [21] have investigated the penetration of SWCNTs into lipid mem-
branes using MD method. Furthermore, there is also an interesting ap-
proach using the single-chain mean field theory (SCMF) for cellular up-
take of SWCNTs. Pogodin et al. [22] used SCMF to calculate the energy
cost of penetrating SWCNTs into lipid membranes. However, in these
studies, SWCNTs were treated as short rods, and the effects of different
lengths of SWCNTs were ignored. The calculations using MD methods
for systems in SWCNTs longer than 100nm under water are difficult and
take weeks or more because it takes more than two hours to calculate
a SWCNT of several nanometers in vacuum state [23]. Generally, it is
known that hydrogen bond or steric force works in the range of 1 to 2
nm, van der Waals force and electrostatic force works in the range of 1
to several ten nm in nanostructures under water [24]. Therefore, when
SWCNTs are longer than several ten nm, the influence of these forces
is small and can be relatively ignored owing to the high mechanical
properties of SWCNTs. Our previous study reported that the natural fre-
quency of bending mode and radial breathing mode in ssDNA-SWCNTs
model longer than 100nm is in good agreement with the Bernoulli-Euler
beam theory, MD method, and experimental trends [25]. This study is
limited to the simulation of the free vibration state of ssDNA-SWCNTs
and has not yet examined its interaction with lipid membranes.
In this study, we examined the vibration behavior of ssDNA-SWCNTs
adhered to the lipid membranes considering effect of the damping and
mass in water that is dependent on the length of SWCNTs, by changing
the lengths from 200 to 25 nm. Conventionally, although many studies
have been conducted on the interaction, adsorption process between ss-
2
Forces in Mechanics 2 (2021) 100008
DNA and SWCNTs by the MD method [26, 27], few studies have shown
the vibrational characteristics of interaction between ssDNA-SWCNTs
with various lengths and lipid membranes. The ssDNA-SWCNT, which
is applied to cells as a biomedical application, undergoes the process
of transitioning from the free vibration state outside the cell to the
cantilever state adhered to the lipid membrane. It is thought that the
transition of ssDNA-SWCNTs with various lengths from free vibration to
cantilever adhered to lipid membranes causes a large change in the nat-
ural frequency, resulting in complex vibration characteristics between
ssDNA-SWCNTs and lipid membranes. The understanding of vibrational
behavior of them can contribute to elucidating the mechanism of me-
chanical interactions of ssDNA-SWCNTs and lipid membranes.
2. Materials and methods
We have developed the structural model that can accurately analyze
the vibration behavior of ssDNA-SWCNTs adhered to the lipid mem-
branes. In our previous research [28], we demonstrated the vibrational
characteristics of (6,5) chirality SWCNTs in water using the space frame
structure model proposed by Li et al. [29]. This model is composed of
cylindrical beam elements determined based on the studies of molecu-
lar dynamics [30] and structural mechanics [31]. The ssDNA model is
composed of the solid element based on our previous research [25]. The
mass density of the ssDNA, including 30 nucleotides (10.2nm), was de-
termined as 6450 kg/m3 assuming an average molecular weight per nu-
cleotide of 330 g/mol. The 𝜋-𝜋 stacking interaction between ssDNA and
SWCNT was adsorbed by a linear spring element of 1.0 nN/nm based on
experimental reported by Changhong et al. [32], Iliafar et al. [33]. This
spring load was defined to be evenly distributed at each node consti-
tuting the 6-membered ring as shown in Fig. 2a. The lipid membranes
model developed in this study is composed of the solid element. The
Young’s modulus of the lipid membranes was 15 MPa, measured exper-
imentally by Stetter et al. [34] as shown in Fig. 2b. The mass density
for outside and inside of the lipid membranes was 1000 kg/m3 and 750
kg/m3 , respectively, reported by Muddana et al. [35]. The size of the
lipid membranes used for the calculation was 100 nm × 100 nm, and the
thickness was 5 nm. The edge of the lipid membranes constrains the 6
degrees of freedom (6DOF) of translation and rotation as shown in Fig.
S1. The properties of these models are summarized in Table 1.
The structure model in this study was developed by NASTRAN code
[36] using the commercial NX-Ideas (Siemens PLM) software. The anal-
ysis solver of MSC Nastran uses linear static analysis (SOL101) and
modal frequency response analysis (SOL111). For post-processing, the
frequency analysis output was performed using ESTECH.PathFinder (ES-
TECH CORP.) software. The graphical animation of the model was per-
formed using META 19.1.1 software (BETA CAE Systems).
To express the state of ssDNA-SWCNTs adhered to the lipid mem-
branes, we show the structural model between ssDNA-SWCNTs and the
lipid membranes in Fig. 3a. The adhesion between ssDNA-SWCNTs and
lipid membranes rigidly bound the tip of SWCNTs to the lipid mem-
branes, since Shi et al. experimentally and theoretically showed that
cylindrical CNTs penetrate lipid membranes first from the tip [20]. Fur-
thermore, the effects of the damping and mass in water were added
to the structural model by giving the mass 3.0 × 10−26 kg of water
molecules to all nodes of the model and defining the structural damping
in each model element, as shown in Fig. 3b. Thus, we used the modal
analysis method for analyzing the vibration behavior of ssDNA-SWCNTs
adsorbed to the lipid membranes. The modal analysis method obtains
vibration characteristics by solving and superimposing the natural vi-
bration modes of the structural model system. This method can obtain
their vibrational characteristics faster than the direct analysis method
that solves simultaneous equations according to the degree of freedom
(See chapter 2 of supplementary information).
As shown in Fig. 3a, when the input force at i point of SWCNTs tip is
𝑃𝑖 (𝜔), the amplitude 𝑋𝑖 (𝜔) of the same node for the input force indicates
the drive point frequency response and the different node 𝑋𝑗 (𝜔) (i≠j)
D. Miyashiro, R. Hamano, H. Taira et al. Forces in Mechanics 2 (2021) 100008

Fig. 2. Schematic arrangement of structural

model. (a) ssDNA-SWCNTs. (b) Lipid mem-
branes.

Fig. 3. (a) Schematic illustration of SWCNTs

and the lipid membranes. 𝑃𝑖 (𝜔) is the input
force at the SWCNTs. 𝑋𝑖 (𝜔) is the amplitude on
the input point of SWCNTs. 𝑋𝑗 (𝜔) is the ampli-
tude on the points of ssDNA from input point
(i≠j). (b) ssDNA-SWCNT adhered to lipid mem-
branes with water model. 𝑃𝑘 (𝜔) is the reaction
force at the support point where the SWCNTs
adhered to the lipid membrane.

Table 1
The model parameters of ssDNA-SWCNTs and lipid membranes.

SWCNTs Ref. ssDNA Ref. Lipid membranes Ref.

Thickness [nm] 0.75 [6] 1.00 [6] 5.00 [34,35]

Young’s modulus [GPa] 1040 [40,41] 0.150 [38] 0.015 [34]
Mass density [kg/m3] 1600 [37] 6450 [24] 750-1000 [35]
Model Element Beam [27,28] Solid [24] Solid [35]

3
D. Miyashiro, R. Hamano, H. Taira et al.
Table 2
Structural damping of SWCNTs with and without water.
Conditions Without water
Length of SWCNTs [nm] - 25
Structual damping 0.0025
on ssDNA indicates the transfer frequency response from SWCNTs to
ssDNA. These frequency response functions are expressed as follows:
𝑁
∑ 0.3 nm, b is the internal diameter at 0.45 nm, 𝜆n denotes the nth mode,
𝑋 𝑗 (𝜔 ) 𝜙𝑠𝑗 𝜙𝑠𝑖
= (1)
𝑃 𝑖 (𝜔 ) 𝑠=1 −𝜔2 𝑚𝑠 + 𝑖𝜔𝑏𝑠 + 𝑘𝑠
where 𝜙s denotes the mode shapes, and ms , bs , and ks are the condensed
mass, damping, and stiffness matrix, respectively. The modal viscous
damping bs is represented by the modal structural damping Gs or damp-
ing ratio 𝜁 s . The modal viscous damping bs is expressed as follows:
√ √
𝑏𝑠 = 2𝜁𝑠 𝑚𝑠 𝑘𝑠 = 𝐺𝑠 𝑚𝑠 𝑘𝑠 (2)
where Gs in condition without water was assumed to be 0.0025, which
is smaller than the CFRP obtained from the study by Khan et al. [39].
Gs in the conditions with water is expressed as follows:
2𝑐 4𝜋𝜂𝐿
𝐺𝑠 = = ( ) (3)
𝑐0 𝑙𝑛 𝐿𝑎 − 0.72
where c is damping coefficient, c0 was assumed to be 1, and 𝜂, L, and
a are the viscosity of water, length, and external diameter of SWCNTs,
respectively. This equation shows the damping coefficient that the cylin-
der receives in water [40]. Assuming SWCNTs are mathematically cylin-
drical shape, structure damping Gs corresponding to their lengths was
defined as shown in Table 2. In this manner, the effects of the damping
and mass in water, which have a great influence on the vibrational be-
havior of SWCNTs, are expressed. In addition, when the node connected
the lipid membranes and SWCNTs is k point, reaction forces is expressed
by 𝑃𝑘 (𝜔). The ratio of 𝑃𝑘 (𝜔) to 𝑃𝑖 (𝜔) is vibration transmissibility.
3. Results and discussion
3.1. Model validity of SWCNTs
The validity of the SWCNTs model depends on material properties of
the beam elements composed of space frame structural model. Thus, we
verified the accuracy of our SWCNTs model by calculating static uniaxial
tension and natural frequency of SWCNTs. The boundary conditions for
static uniaxial tension analysis constrain the SWCNTs endpoint to 6DOF,
while axial force was input to the opposite endpoint. Young’s modulus,
E, of SWCNTs can be calculated from the following equation:
𝐹 ∕𝐴0
𝜎
𝐸= = (4)
𝜀 Δ𝐿∕𝐿0
where, F is the total applied force, A0 is the cross-sectional area, L0 is
the initial length, and ΔL represents the elongation of SWCNTs. The
Young’s modulus obtained by our numerical simulation was approxi-
mately 1.04 TPa, regardless of SWCNTs lengths in the range of 25 to
200 nm. These values were within 5% error of Young’s modulus de-
termined by Krishnan et al. experimentally [41] and MD method by
Ogata et al. theoretically [42]; It is shown that the elastic modulus of
our longer SWCNTs model correlates with the elastic properties calcu-
lated by the MD method considering the intermolecular bonding force.
thus, the material properties defined in our SWCNTs model is physically
reasonable. For natural frequency of SWCNTs, we performed the linear
eigenvalue analysis of SWCNTs using the modal analysis method and
compared with the Bernoulli–Euler beam theory expressed by:
√ ( )
𝜆2𝑛 𝐸 𝑎2 + 𝑏2
𝑓𝑛 = , (5)
4𝜋𝐿2 𝜎
Forces in Mechanics 2 (2021) 100008
Water
50 100 150 200
0.0900 0.1500 0.2580 0.3580 0.4520
where L is the length of SWCNTs, E is 1.04 TPa of Young’s modulus
obtained in the uniaxial tension analysis, a is the external diameter at
and fn is the natural frequency of the nth mode. The natural frequency
depends on the boundary conditions. The values for a free vibration
state, cantilever state are 𝜆1 = 4.730, 1.875 respectively. As a result, the
natural frequency of SWCNTs by modal analysis method were consis-
tent with the Bernoulli-Euler beam theory with a 3% error, as shown in
Table S1, Fig. S2. Our numerical simulation can correctly calculate the
vibration characteristics of SWCNTs without water. This indicates that
SWCNTs longer than 25 nm correlate with the vibration characteristics
of the elongated cylinder. In addition, we presume that the major vi-
brational behavior of SWCNTs is little influenced by the intermolecular
interactions occurring in the femtosecond to picosecond range since the
bending vibration modes of the SWCNTs longer than 25 nm is mainly
in the GHz range. In the next section, we also examined the vibrational
behavior of ssDNA-SWCNTs adhered to the lipid membranes in water.
3.2. Vibration analysis of ssDNA-SWCNTs with and without water
In order to understand the vibrational behavior of ssDNA-SWCNTs
in vivo, the natural vibrational mode and frequency response functions
of them with 100nm are shown in Fig. 4 as a typical example. Fig. 4a–c
shows the natural vibration modes in the free vibration mode of SWC-
NTs, the ssDNA vibration mode, and the cantilever mode adhered to
rigid wall respectively. The relationship between the vibration ampli-
tude and natural frequency of these natural vibration modes is clarified
by the frequency response function. Fig. 4d is drive point frequency re-
sponse function in vibration amplitude 𝑋𝑖 (𝜔) at same point from 𝑃𝑖 (𝜔)
on SWCNTs in free state with and without water. The natural frequency
of bending mode in Fig. 4a decreased from 2.408 GHz without water
to 1.018 GHz with the water. In addition, Fig. 4e is transfer frequency
response function in vibration amplitude 𝑋𝑗 (𝜔) at ssDNA from 𝑃𝑖 (𝜔) on
SWCNTs. It is clear from Fig. 4d-e that the ssDNA vibration mode in
Fig. 4b appears at frequency 0.026 GHz sufficiently lower than that of
SWCNTs. On the other hand, Fig. 4f is drive point frequency response
function in 𝑋𝑖 (𝜔) at same point from 𝑃𝑖 (𝜔) on SWCNTs in cantilever state
with and without water. The natural frequency in Fig. 4c decreased from
0.384 GHz without water to 0.165 GHz with the water. The natural fre-
quency of ssDNA-SWCNTs in water increases 6.27-fold from cantilever
mode to free vibration mode. In addition, it is shown that the vibration
amplitude in the cantilever state is significantly smaller than that of the
free vibration state in the frequency range below 0.01 GHz. Thus, it
can be understood that the natural frequency and vibration amplitudes
of cantilever mode dramatically changes depending on their boundary
conditions.
3.3. Vibration behavior of ssDNA-SWCNTs adhered to the lipid membranes
Fig. 5 shows the natural vibration modes and frequency response
functions when ssDNA-SWCNTs with 100nm adhered to the lipid mem-
branes in water. The natural frequency modes of Fig. 5a-c is ssDNA vi-
bration mode, coupled vibration mode between ssDNA vibration and
cantilevered SWCNTs, and bending mode of SWCNTs. Comparing the
cantilever mode from Figs. 4c to 5b, the natural frequency was decreased
from 0.165 GHz to 0.036 GHz due to adhesion to the lipid membranes
compared to the rigid wall. As a result, the coupled vibration mode was
4
D. Miyashiro, R. Hamano, H. Taira et al. Forces in Mechanics 2 (2021) 100008

Fig. 4. Vibration model in ssDNA-SWCNTs of 100nm. (a) Free vibration mode of ssDNA-SWCNTs. (b) ssDNA vibration mode on SWCNTs. (c) Cantilever mode of
ssDNA-SWCNTs adhered to rigid wall. Frequency response function of free vibration state in ssDNA-SWCNTs of 100nm with and without water; (d) Drive point
frequency response of SWCNTs. (e) Transfer function frequency response of ssDNA from SWCNTs. Frequency response function of cantilever state in ssDNA-SWCNTs
of 100nm with and without water; (f) Drive point frequency response of SWCNTs. (e) Transfer function frequency response of ssDNA from SWCNTs.

generated by approaching the cantilever mode to the ssDNA vibration
mode as shown in Fig. 5d-e.
To investigate the effect of coupled vibration between ssDNA and
SWCNTs, we examined the frequency response functions of SWCNTs
with and without ssDNA adhered to lipid membranes. The black line
in Fig. 5d is the drive point response function on bare SWCNTs with-
out ssDNA, which has a peak at 0.031 GHz. On the other hand, in the
ssDNA-SWCNTs indicated by green line, the vibration peak was divided
into two peaks, and their peaks amplitude was reduced by 40% com-
pared to the black line. This indicates that ssDNA acts as a dynamic
absorber for cantilever mode. the effects of the mechanical interaction
between ssDNA wrapped SWCNTs and lipid membranes provide a new
understanding to the surface science of biomedical applications.
Although there are many experimental studies showing that SWC-
NTs shorter than 100 nm are more likely to penetrate lipid membranes
[9–16], no studies quantitatively compare the physical quantities of vi-
brational behavior when SWCNTs at different lengths adhere to lipid
membranes. So far, there have been no research reports on the numer-
ical calculation between ssDNA-SWCNTs longer than 100nm and lipid
membranes because MD method take the huge amount time for calcu-
lation under water. On the other hand, comparing calculation time of
the different method using computers with the same performance, the
calculation of Fig. 5d using the modal analysis method can be calcu-
lated in about 3 hours, while the direct analysis method takes 48 hours
to calculate the same results. The modal analysis method enables many
parameter studies in a practical calculation time while maintaining the
calculation accuracy as shown in the previous section. Therefore, using
the prepared structural model of ssDNA-SWCNTs and lipid membranes,
we investigate the effect of vibration behavior of the ssDNA-SWCNTs
on the lipid membranes when the lengths of the SWCNTs changed from
200 to 25 nm.
3.4. Effect of the SWCNTs length on vibration behavior between
ssDNA-SWCNTs and lipid membranes
Fig. 6a-b demonstrates the drive point frequency responses of ssDNA-
SWCNTs at difference lengths from the 25nm to 200nm range adhered
to the lipid membranes, the transfer function frequency responses of ss-
DNA on the SWCNTs. As the length of the ssDNA-SWCNTs is shortened,
the natural frequency of ssDNA-SWCNTs increases and the vibrational

5
D. Miyashiro, R. Hamano, H. Taira et al.
amplitude decrease, as shown in Fig. 6a. The vibration peaks of can-
tilever mode adhered to the lipid membranes also affect the responses
of ssDNA on SWCNTs, as shown by the black arrows in Fig. 6b. In
the ssDNA-SWCNTs shorter than 100 nm, the natural frequencies be-
tween the cantilever mode and the ssDNA vibration mode of red arrow
in Fig. 6b are separated. On the other hand, it is clear from the fre-
quency response function in Fig. 6a-b that the ssDNA-SWCNTs longer
than 100nm are coupled vibration mode between ssDNA vibration and
cantilevered SWCNTs.
Focusing on the systematic understanding of the relationship be-
tween the length of SWCNTs and these vibration behavior in water, we
calculated the root mean square (RMS) in range from 0.001 to 10 GHz
as an evaluation method that can compare the vibration amplitude of
ssDNA-SWCNTs. The green line in Fig. 6c shows the RMS values when
the lengths of SWCNTs adhered to the lipid membranes were changed
from 25 nm to 200 nm. In addition, the dotted lines show the results
when the bare SWCNTs was adhered to the lipid membranes. By com-
paring SWCNTs with and without ssDNA, the effect of ssDNA on the
vibrational amplitude of SWCNTs can be extracted. In the cantilever
state of SWCNTs adhered to the lipid membranes, the vibration ampli-
6
Forces in Mechanics 2 (2021) 100008
Fig. 5. Vibration mode in ssDNA-SWCNTs of
100nm adhered to the lipid membranes in
water. (a) ssDNA vibration mode. (b) cou-
pled vibration mode between ssDNA vibration
and cantilevered SWCNTs. (c) bending mode
of SWCNTs. Frequency response function in
ssDNA-SWCNTs of 100nm adhered to the lipid
membranes in water; (d) Drive point frequency
response of SWCNTs. (e) Transfer function fre-
quency response of ssDNA from SWCNTs. The
lines of green, black represent ssDNA-SWCNTs,
SWCNTs respectively. (For interpretation of the
references to color in this figure legend, the
reader is referred to the web version of this ar-
ticle.)
tude increases as the SWCNT lengthens. Thus, the difference of RMS in
vibration amplitudes with and without ssDNA was reduced with SWC-
NTs shorter than 100 nm because the natural frequencies of the DNA
vibration mode and cantilevered mode are separated from each other.
Furthermore, in order to investigate the effect of the elastic modu-
lus of the membrane to which ssDNA-SWCNTs adheres, the results of
the vibration amplitude of ssDNA-SWCNTs adhered to the rigid wall are
shown in blue color shown in Fig. 6c. The vibration amplitude signifi-
cantly decreases compared to the cantilever state adhered to the lipid
membranes. In addition, there is almost no difference of RMS value
in the vibration amplitude with and without ssDNA. It is clear from
Fig. S4 that the SWCNTs vibration below 0.03 GHz, which has the ssDNA
vibration mode, has almost constant amplitude because the endpoint of
SWCNTs are constrained in 6 DOF against rigid wall. In contrast, the
RMS value in free vibration state of red color shown in Fig. 6c tends
to increase as SWCNTs is shorter because shorter SWCNTs have smaller
rotational inertia. In the free vibration state, the vibration amplitude
increases at a frequency below 0.03 GHz as shown in Fig. S3, which is
the natural frequency of DNA vibration mode. Thus, the RMS of ssDNA-
SWCNT in solid line decreases by about 20% compared to the bare SWC-
D. Miyashiro, R. Hamano, H. Taira et al.
NTs in the dotted line due to effect of the ssDNA mass. Fig. 6c shows
that the shorter the SWCNT length, the greater the difference in vibra-
tion amplitude when transitioning from the free vibration state to the
cantilevered state. For example, in SWCNTs of 25nm, there is 88.5-fold
difference in RMS value between the free vibration state and the can-
tilever state of adhered to the lipid membranes, while SWCNTs of 100nm
is 8.3-fold difference in RMS values of them. These suggest that shorter
SWCNTs exert greater force on the lipid membranes. When SWCNTs
penetrates the lipid membranes in vivo, it goes through the dynamic
vibration process of free vibration state outside the lipid membranes,
cantilever state adhered to the lipid membranes, and free vibration in-
side the lipid membranes. Here, the vibration modes of ssDNA-SWCNTs
indicated by arrows 1, 3 and 5 in Fig. 6a are shown in Figs. 7a,
Fig. 5b and Fig. 7b respectively. Fig. 7a shows the cantilever modes in
200 nm SWCNTs precede the ssDNA vibrational modes. Fig. 5b shows
a coupled vibration mode between ssDNA vibration and cantilevered
mode in SWCNTs 100 nm. On the other hand, Fig. 7b shows the can-
7
Forces in Mechanics 2 (2021) 100008
Fig. 6. Frequency response functions of ssDNA-SWCNTs adhered
to the lipid membranes in water. (a) Drive point frequency re-
sponse of SWCNTs. (b) Transfer function frequency response of
ssDNA from SWCNTs. Black arrows 1, 2, 3, 4, 5 in Fig. 6a-b are
cantilever mode of ssDNA-SWCNTs adhered to lipid membranes:
200nm, 150nm, 100nm, 50nm, 25nm respectively. Red arrow is
ssDNA vibration mode. (c) Relationship between RMS of 𝑋𝑖 (𝜔) /
𝑃𝑖 (𝜔) and length of SWCNTs: the solid lines indicate the results
of ssDNA-SWCNTs, while the dotted lines indicate the results of
bare SWCNTs. Red lines of diamond represent free vibration state.
Blue lines of circle represent cantilever state adhered to rigid wall.
Green lines of triangle represent ssDNA-SWCNTs adhered to the
lipid membranes. (For interpretation of the references to color in
this figure legend, the reader is referred to the web version of this
article.)
tilever mode in SWCNTs 25 nm. The large difference in the vibration
mode morphology depending on the length of SWCNTs is considered to
be related to the effect on the lipid membranes.
To quantitatively evaluate the force transmitted to the lipid mem-
branes due to the change in the length of SWCNTs, we analyzed the vi-
brational transmissibility frequency response of the reaction force 𝑃𝑘 (𝜔)
to the input force 𝑃𝑖 (𝜔) at the tip of ssDNA-SWCNT as shown in Fig. 3a.
Regarding to vibration transmissibility, longer ssDNA-SWCNTs tend to
attenuate the peak amplitude as shown in Fig. 7c. It is considered that
the longer the ssDNA-SWCNTs are, the more they are affected by the
damping force of water. The amplitudes difference between the vibra-
tion peaks in ssDNA-SWCNTs at 100 nm and 25 nm shown by arrows
in Fig. 7c is 4.2-fold. In particular, ssDNA-SWCNTs longer than 100nm
significantly suppress vibration transmission above 1 GHz.
Fig. 7d shows the relationship between the length of SWCNTs and
the RMS value of the vibration transmissibility. The vibration transmis-
sibility increases as ssDNA-SWCNTs are shorter. As the SWCNT lengths
D. Miyashiro, R. Hamano, H. Taira et al.
decreased from 200 nm to 25 nm, the RMS value increased by approx-
imately 4.55-fold. This indicates that shorter ssDNA-SWCNTs have low
damping resistance in water and more efficiently transmit force to the
lipid membranes. As previous experimental studies have shown that
SWCNTs shorter than 187 nm are taken up by cells [13], the sugges-
tion that shorter SWCNTs exert more force on the passage of the lipid
membranes and longer ones are less likely to transfer force to them is
thought to correlate with our results by the modal analysis method. We
believe that this is the one of the mechanical explanations that shorter
ssDNA-SWCNTs penetrate lipid membranes better. As shown in Fig. 7b,
the bending mode of SWCNTs may be a factor that damages the lipid
membranes. On the other hand, coupled vibration mode in Fig. 7a
suppress the cantilever mode due to the ssDNA vibration. It was also
quantitatively found that ssDNA vibration acts as a dynamic absorber for
SWCNTs of 100nm and reduces the vibration transmissibility by approx-
imately 8% as shown in Fig. 7d. Table 3 summarizes the relationship
between the length of the SWCNTs and the vibrational transmissibility.
In the study by Pogodin et al. 19 , calculations of SCFT showed that the
energy required for SWCNTs to penetrate the phospholipid bilayer was
8
Forces in Mechanics 2 (2021) 100008
Fig. 7. Vibration mode of ssDNA-SWCNTs
at difference lengths adhered to the lipid
membranes in water. (a) 200nm. (b) 25nm.
(c) Vibrational transmissibility frequency re-
sponse between SWCNTs and lipid membranes.
Lines of purple, blue, green, orange, red are
ssDNA-SWCNTs lengths: 25nm, 50nm, 100nm,
150nm, 200nm respectively. (d) Relationship
between RMS of 𝑃𝑘 (𝜔) / 𝑃𝑖 (𝜔) and length of
SWCNTs: the solid lines indicate the results of
ssDNA-SWCNTs, while the dotted lines indicate
the results of bare SWCNTs. Blue lines of cir-
cle represent cantilever state adhered to rigid
wall. Green lines of triangle represent ssDNA-
SWCNTs adhered to the lipid membranes. (For
interpretation of the references to color in this
figure legend, the reader is referred to the web
version of this article.)
1.35-fold higher than that of SWCNTs affected by thermal motion. Thus,
they concluded that cellular uptake of SWCNTs is endocytosis. How-
ever, the SWCNTs were treated as rigid rods, and the effects of elastic
characteristics in SWCNTs at different lengths were ignored. Consider-
ing the vibration behavior of ssDNA-SWCNTs revealed in this study, the
length-dependent vibration transmissibility results provide the possibil-
ity that SWCNTs penetrate lipid membranes by involving both passive
diffusion and endocytosis. Regarding the force of SWCNTs to penetrate
lipid membranes, Vakarelski et al. [43] reported that the force of CNTs
penetration through the lipid membranes was measured as 100 - 200
pN by the AFM equipped with CNTs at the probe tip. However, since
the CNTs used in the experiments were longer and larger in diameter
than SWCNTs, we estimated that the force penetrating SWCNTs would
be less than their report.
For ssDNA-SWCNTs with length 25nm, the RMS of the cantilever
mode adhered to the rigid wall is 2.3-fold larger than that of ssDNA-
SWCNTs adhered to lipid membranes as shown in Fig. 7d. We found
that as the lipid membranes became more rigid, the RMS value of the
vibrational transmissibility between SWCNTs and lipid membranes in-
D. Miyashiro, R. Hamano, H. Taira et al. Forces in Mechanics 2 (2021) 100008

Table 3
Summary of the RMS value of vibrational transmittance between SWCNTs and lipid membranes.

Condition Water

SWCNTs length [nm] 25 50 100 150 200

RMS [m/N] Free state ssDNA-SWCNTs 0.085875 0.038855 0.019465 0.012915 0.009653
Bare SWCNTs 0.097490 0.048477 0.024733 0.016560 0.012385
Cantilever adhere to lipid membranes ssDNA-SWCNTs 0.000971 0.001771 0.002334 0.002986 0.003204
Bare SWCNTs 0.000940 0.001808 0.002939 0.003670 0.003832
Cantilever adhere to rigid wall ssDNA-SWCNTs 0.000034 0.000118 0.000365 0.000661 0.001160
Bare SWCNTs 0.000034 0.000118 0.000368 0.000706 0.001115
RMS [N/N] Cantilever adhere to lipid membranes ssDNA-SWCNTs 1.379922 1.207730 0.731414 0.468559 0.303006
Bare SWCNTs 1.340537 1.233948 0.794011 0.473092 0.306478
Cantilever adhere to rigid wall ssDNA-SWCNTs 3.167044 2.070251 1.205451 0.709398 0.391608
Bare SWCNTs 3.167090 2.070559 1.207169 0.716634 0.450272

creased. These results suggest that the ease of SWCNTs penetration de-
pends on lipid membranes elasticity and corresponds to the results of
SCFT calculations by Guo et al. [44]. Previous experimental studies have
shown some variation in the length of SWCNTs that are easily taken up
by cells. This can be understood as a difference resulting from the cell
types used in the experiments and lipid membranes rigidity, as shown
by studies of the mechanical properties of cancer cells, various other
cells, and muscle cells [45–48]. When nanomaterials such as SWCNTs
reach the application stage, it may be necessary to design the SWCNT
composites mixed various adsorbed molecules, because Hamano et al.
revealed a specific difference in optical response of SWCNTs mixed
with DNA and carboxymethylcellulose [49]. In addition, SWCNTs can
accumulate in cancer cells without penetrating the lipid membranes,
regardless of their lengths, because cancer cells are softer than normal
cells. This phenomenon may also be a result of the mechanical mech-
anisms of the ERP effect. In addition, these phenomena may apply not
only to SWCNTs but to other nanomaterials as well. For example, Bast-
ings et al. [50] conducted a study, which investigated the effects of a
DNA origami shape and cell type on cellular uptake. We believe that the
evaluation of the vibrational behavior using the modal analysis method
can contribute to the elucidation of other nanomaterials.
4. Conclusion
The prepared structural model of ssDNA-SWCNTs can accurately rep-
resent elastic properties and vibration characteristics consistent with the
Bernoulli–Euler beam theory, MD method and experimental. In addi-
tion, we analyzed the vibration behavior between ssDNA-SWCNTs and
lipid membranes by modal analysis method. These interactions were
evaluated by the RMS value in the range of 0.001 to 10 GHz of the
vibration transmissibility in the ssDNA-SWCNTs adhered to the lipid
membranes. As a result, we found that ssDNA-SWCNTs shorter than 100
nm can efficiently transmit force on the lipid membranes. Furthermore,
shortening the lengths of SWCNTs from 200 nm to 25 nm, the RMS of
vibrational transmissibility between ssDNA-SWCNTs and the lipid mem-
branes increased by approximately 4.55-fold, given that viscous damp-
ing depends on the length of SWCNTs. Furthermore, it was found that
the vibration transmissibility dramatically depends on the elastic mod-
ulus of the membrane to be adhered.
Our results analytically suggest that the length of ssDNA-SWCNTs,
their length-dependent viscous damping, and the elastic properties of
the lipid membranes affect the vibration behavior between ssDNA-
SWCNTs and lipid membranes. The results of this study are expected to
contribute significantly to elucidating the mechanical interactions be-
tween ssDNA-SWCNTs and lipid membranes.
Declaration of Competing Interest
The author declares no conflict of interest.
Acknowledgments
This study was partially supported by the ESTECH CORP. and Grants-
in-Aids for Scientific Research from the Ministry of Education, Science,
and Culture of Japan.
This work was supported by JST SICORP Grant Number
JPMJSC19E1, Japan.
Supplementary materials
Supplementary material associated with this article can be found, in
the online version, at doi:10.1016/j.finmec.2020.100008.
References
[1] C. Li, E.T. Thostenson, T.J. Chou, Sensors and actuators based on carbon nanotubes
and their composites: a review, Compos. Sci. Technol. 68 (2008) 1227–1249.
[2] Y. Liu, S. Kumar, Polymer/carbon nanotube nano composite fibers—a review, ACS
Appl. Mater. Interface 6 (2014) 6069–6087.
[3] V. Schroeder, S. Savagatrup, M. He, T.M. Swager, Carbon nanotube chemical sensors,
Chem. Rev. 119 (2019) 599–663.
[4] A. Muhulet, F. Miculescu, S.I. Voicu, F. Schütt, V.K. Thakur, Y.K. Mishra, Fundamen-
tals and scopes of doped carbon nanotubes towards energy and biosensing applica-
tions, Mater. Today Energy 9 (2018) 154–186.
[5] D. Miyashiro, R. Hamano, K. Umemura, A review of applications using mixed mate-
rials of cellulose, nanocellulose and carbon nanotubes, Nanomaterials 10 (2) (2020)
186.
[6] M. Zheng, A. Jagota, E.D. Semke, B.A. Diner, R.S. McLean, S.R. Lustig, R.E. Richard-
son, N.G. Tassi, DNA-assisted dispersion and separation of carbon nanotubes, Nat.
Mater. 2 (2003) 338–342.
[7] N. Nakashima, S. Okuzono, H. Murakami, T. Nakai, K. Yoshikawa, DNA dissolves
single-walled carbon nanotubes in water, Chem. Lett. 32 (2003) 456–457.
[8] S.Y. Hong, G. Tobias, K.T. AI-Jamal, B. Ballesteros, H.A. Boucetta, S.L. Perez,
P.D. Nellist, R.B. Sim, C. Finucane, S.J. Mather, M.L. Green, K. Kostarelos,
B.G.A. Davis, Filled and glycosylated carbon nanotubes for in vivo radioemitter lo-
calization and imaging, Nat. Mat. 9 (2010) 485–490.
[9] Y. Iizumi, M. Yudasaka, J. Kim, H. Sakakita, T. Takeuchi, T. Okazaki, Oxygen-doped
carbon nanotubes for near-infrared fluorescent labels and imaging probes, Sci. Rep.
8 (2018) 6272.
[10] Y. Matsumura, H. Maeda, A new concept for macromolecular therapeutics in cancer
chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitu-
mor agent smancs, Cancer Res. 46 (1986) 6387–6392.
[11] B.R. Smith, E.E.B. Ghosn, H. Rallapalli, J.A. Prescher, T. Larson, L.S. Herzenberg,
S.S. Gambhir, Selective uptake of single-walled carbon nanotubes by circulating
monocytes for enhanced tumour delivery, Nat. Nanotech. 9 (2014) 481–487.
[12] K. Kostarelos, The long and short of carbon nanotube toxicity, Nat. Bio 26 (2008)
774–776.
[13] M.L. Becker, J.A. Fagan, N.D. Gallant, B.J. Bauer, V. Bajpal, E.K. Hobble, S.H. Lac-
erda, K.B. Migler, J.P. Jakupclak, Length‐dependent uptake of DNA‐wrapped sin-
gle‐walled carbon nanotubes, Adv. Mat. 19 (7) (2007) 939–945.
[14] B. Kang, S. Chang, Y. Dai, D. Yu, D. Chen, Cell response to carbon nanotubes: size-de-
pendent intracellular uptake mechanism and subcellular fate, Small 6 (21) (2010)
2362–2366.
[15] D. Pantarotto, J.P. Brland, M. Prato, A. Bianco, Translocation of bioactive peptides
across cell membranes by carbon nanotubes, Chem. Commun. (2004) 16–17.
[16] N.W. Kam, H. Dai, Carbon nanotubes as intracellular protein transporters: generality
and biological functionality, J. Am. Chem. Soc. 127 (16) (2005) 6021–6026.
[17] N.W. Kam, Z. Liu, S. Kam, H. Dai, Carbon nanotubes as intracellular transporters for
proteins and DNA: an investigation of the uptake mechanism and pathway, Angew.
Chem. Int. Ed. Engl. 45 (4) (2006) 577–581.

9
D. Miyashiro, R. Hamano, H. Taira et al.
[18] A.E. Porter, M. Gass, K. Muller, J.N. Skepper, P.A. Midgley, M.M. Welland, S.H. Lac-
erda, K.B Migler, J.P. Jakupclak, Direct imaging of single-walled carbon nanotubes
in cells, Nat. Nanotech. 2 (2007) 713–717.
[19] A.E. Porter, M. Gass, J.S. Bendall, K. Muller, A. Goode, N J, P.A.M. Skepper,
M. Welland, Uptake of noncytotoxic acid-treated single-walled carbon nanotubes
into the cytoplasm of human macrophage cells, ACS Nano 3 (6) (2009) 1485–1492.
[20] X. Shi, A.V.D. Bussche, R.H. Hurt, A.B. Kane, H. Gao, Cell entry of one-dimen-
sional nanomaterials occurs by tip recognition and rotation, Nat. Nanotech. 6 (2011)
714–719.
[21] W. Zhu, A.V.D. Bussche, X. Yi, Y. Qiu, Z. Wang, P. Weston, R.H. Hurt, A.B. Kane,
H. Gao, Nanomechanical mechanism for lipid bilayer damage induced by carbon
nanotubes confined in intracellular vesicles, Proc. Natl. Acad. Sci. 113 (44) (2016)
12347–12379.
[22] S. Pogodin, V.A. Baulin, Can a carbon nanotube pierce through a phospholipid bi-
layer? ACS Nano 4 (9) (2010) 5293–5300.
[23] J.L. Zang, Q. Yuan, F.C. Wang, Y.P. Zhao, A comparative study of Young’s modu-
lus of single-walled carbon nanotube by CPMD, MD and first principle simulations,
Comput. Mater. Sci. 46 (3) (2009) 621–625.
[24] J. Israelachvili, Intermolecular and Surface Force, 2nd ed., Academic Press, London,
1992.
[25] D. Miyashiro, H. Taira, K. Umemura, Vibration analysis of single-stranded
DNA-wrapped single-walled carbon nanotubes using finite element method, Com-
pos. Part B Eng. 173 (2019) 106896.
[26] M.L. Mayo, Z.Q. Chen, S.V. Kilina, Computational studies of nucleotide selectivity
in DNA-carbon nanotube hybrids, J. Phys. Chem. Lett. 3 (2012) 2790–2797.
[27] D. Pramanik, P.K. Maiti, DNA-assisted dispersion of carbon nanotubes and compar-
ison with other dispersing agents, Appl. Mate. Interfaces 9 (2017) 35287–35296.
[28] D. Miyashiro, H. Taira, R. Hamano, R.L. Reserva, K. Umemura, Mechanical vibra-
tion of single-walled carbon nanotubes at different lengths and carbon nanobelts by
modal analysis method, Compos. Part C 2 (2020) 100028.
[29] C. Li, T.W. Chou, A structural mechanics approach for the analysis of carbon nan-
otubes, Int. J. Solid Struct. 40 (2003) 2487–2499.
[30] W.D. Cornell, P. Cieplak, C.I. Bayly, I.R. Gould, K.M. Merz, D.M. Ferguson,
D.C. Spellmeyer, T. Fox, J.W. Caldwell, P.A. Kollman, A second generation force-field
for the simulation of proteins, nucleic acids and organic molecules, J. Am. Chem.
Soc. 117 (1995) 5179–5197.
[31] K.I. Tserpes, P. Papanikos, Finite element modeling of single-walled carbon nan-
otubes, Compos: Part B Eng 36 (5) (2005) 468–477.
[32] K. Changhong, H. Michael, G. Hanna, E. Piotr, Direct measurements of base stacking
interactions in DNA by single-molecule atomic-force spectroscopy, Phys. Rev. Lett.
99 (2007) 018302.
[33] S. Iliafar, J. Mittal, D. Vezenov, A. Jagota, Interaction of single-stranded DNA with
curved carbon nanotube is much stronger than with flat graphite, J. Am. Chem. Soc.
136 (2014) 12947–12957.
10
Forces in Mechanics 2 (2021) 100008
[34] F.W.S. Stetter, T. Hugel, The nanomechanical properties of lipid membranes are
significantly influenced by the presence of ethanol, Biophys. J. 104 (5) (2013)
1049–1055.
[35] H.S. Muddana, R.R. Gullapalli, E. Manias, P.J. Butler, Atomistic simulation of lipid
and DiI dynamics in membrane bilayers under tension, Phys. Chem. Chem. Phys. 13
(2011) 1368–1378.
[36] H MacNeal Richard, The NASTRAN Theoretical Manual, 1972.
[37] E. Santiago, X. Rongsie, F. Martin, C. Richard, H. David, Y. Junwei, R. john, Measure-
ment of area density of vertically aligned carbon nanotube forests by the weight-gain
method, J. Appl. Phys. 113 (2013) 144309.
[38] B. Steven, Y.C. Smith, B. Carlos, Overstretching B-DNA: the elastic response of in-
dividual double-stranded and single-stranded DNA molecules, Science 271 (1996)
795–799.
[39] S.H. Khan, C.Y. Li, N.A. Siddiqui, J.K. Kim, Vibration damping characteristics of car-
bon fiber-reinforced composites containing multi-walled carbon nanotubes, Comps.
Sci. Tech. 71 (2011) 1486–1494.
[40] S. Broersma, Viscous force constant for a closed cylinder, J. Chem. Phys. 32 (1960).
[41] A. Krishnan, E. Dujardin, T.W. Ebbesen, P.N. Yianilos, M.M.J. Treacy, Young’s mod-
ulus of single-walled nanotubes, Phys. Rev. B 58 (1998) 14013.
[42] S. Ogata, Y. Shibutani, Ideal tensile strength and band gap of single-walled carbon
nanotubes, Phys. Rev. B 68 (2003) 165409.
[43] I.U. Vakarelski, S.C. Brown, K. Higashitani, B.M. Moudgil, Penetration of living cell
membranes with fortified carbon nanotube tips, Langmuir 23 (2007) 10893–10896.
[44] Y. Guo, M. Werner, R. Seemann, V.A. Baulin, J.B. Fleury, Tension-induced translo-
cation of an ultrashort carbon nanotube through a phospholipid bilayer, ACS Nano
12 (12) (2018) 12042–12049.
[45] M. Plodinec, M. Loparic, C.A. Monnier, E.C. Obermann, R.Z. Dallenbach, P. Oertle,
J.T. Hyotyla, U. Aebi, M.B. Alj, R.Y.H. Lim, The nanomechanical signature of breast
cancer, Nat. Nanotech. 7 (2012) 757–765.
[46] D. Miyashiro, N. Akiyama, J. Wakayama, Y. Kunioka, T. Yamada, Radial stability of
the actomyosin filament latice in isolated skeletal myofibrils studied using atomic-
force microscopy, J. Physiol. Sci. 63 (2013) 299–310.
[47] D. Miyashiro, N. Ohtsuki, Y. Shimamoto, J. Wakayama, Y. Kunioka, T. Kobayashi,
S. Ishiwata, T. Yamada, Radial stiffness characteristics of the overlap regions of sar-
comeres in isolated skeletal myofibrils in pre-force generating stat, Biophys. Physico.
14 (2017) 207–220.
[48] M. Debashish, P. Soma, S. Sanchit, D. Nilanjan, Carbon nanotubes: evaluation of
toxicity at biointerfaces, J. Pharm. Anal. 9 (2019) 293–300.
[49] R. Hamano, D. Miyashiro, K. Umemura, Study on optical response sensitivity in hy-
brid of single-walled carbon nanotubes mixed with double-stranded DNA and car-
boxymethylcellulose, Opt. Mater. 109 (2020) 110386.
[50] M.M.C. Bastings, F.M. Anastassacos, N. Ponnuswamy, F.G. Leifer, G. Cuneo, C. Lin,
D.E. Ingber, H.J. Ryu, W.M. Shih, Modulation of the cellular uptake of DNA origami
through control over mass and shape, Nano Lett. 18 (6) (2018) 3557–3564.