Articles
https://doi.org/10.1038/s41565-018-0111-5
Multifunctional biophotonic nanostructures
inspired by the longtail glasswing butterfly
for medical devices
Vinayak Narasimhan
1,4
, Radwanul Hasan Siddique
1,4
, Jeong Oen Lee
1,2
, Shailabh Kumar
1
,
Blaise Ndjamen
1
, Juan Du
3
, Natalie Hong
1
, David Sretavan
3
* and Hyuck Choo
1,2
*
1
Department of Medical Engineering, California Institute of Technology, Pasadena, CA, USA.
2
Department of Electrical Engineering, California Institute
of Technology, Pasadena, CA, USA.
3
Department of Ophthalmology, University of California, San Francisco, San Francisco, CA, USA.
4
These authors
contributed equally: Vinayak Narasimhan, Radwanul Hasan Siddique *e-mail: David.Sretavan@ucsf.edu; hchoo@caltech.edu
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
SUPPLEMENTARY INFORMATION
In the format provided by the authors and unedited.
NatuRe NaNO
te
CHNOLOgy
|
www.nature.com/naturenanotechnology
1
Supplementary Information
M
ultifunctional biophotonic nanostructures
inspired by longtail glasswing butterfly
for
medical devices
Vinayak Narasimhan
†
,
Radwanul Hasan
Siddique
†
,
Jeong
Oen
Lee
,
Shailabh Kumar,
Blaise Ndjamen
,
Juan Du
,
Natalie Hong
,
David
Sretavan
*
,
and Hyuck Choo
*
†
These authors contributed equally to this work.
*
These authors are co
-
corresponding authors.
∗
E
-
mail:
hchoo@caltech.edu
,
David.Sretavan@ucsf.edu
2
Supplementary
Section S
I
1
|
Biophotonic
nanostructures on
C. faunus
butterfly
wing
s
Numerous living organisms possess fascinating structural colo
u
ration. However, transparency
is rare
to observe
among
terrestrial
life
due to significant surface reflections between living tissue
s
and air
1,2
.
In this context, the longtail glasswing
C. faunus
butterfly is an interesting example
given it
posses
ses
the struc
tural basis to support both
reflection
-
based
coloration and
transmission
-
based
transparency.
The transparency of the
postdiscal
area can be well
-
explained by effective medium theory and
a
transfer matrix model similar to other anti
-
reflective subwavelength
nanostructures found in nature
considering
the
low absorption of chitin
2,3
. The subwavelength nanodome
-
shaped
structures of the
postdiscal
area induces a refractive index
with a linear gradient
from
1
for
air to
1.56
for
the chitin
membrane
,
and effectively reduces surface reflect
ion
2,3
.
N
anodome
-
shape
d
structures of the
postdiscal
area are hexagonally arranged
and hence,
a hexagonal unit cell was considered with an area of
A
hex
=
√
3
/2
d
2
where
d
is the center
-
to
-
center distance between adjacent nanodomes. The radius of the
n
anodome
at height
z
was provided by
r
(
z
) =
r
0
√
(
1
–
z
/
ℎ
)
, where
h
is the height of the nanodomes
,
and
r
0
is the base radius
that is
equal to
d
/2. Consequently, the
postdiscal nanodome
area at height
z
is
given by
A
TP
(
z
) = πr
0
2
(1
–
z
/
h
)
,
and the volume fraction of chitin as a function of actual height is given
by:
푓
푇푃
=
1
for
푧
<
0
휋
2
√
3
(
1
−
푧
ℎ
)
for
0
≤
푧
≤
ℎ
0
for
z
>
ℎ
(1)
T
he base of the
nanodom
es
was defined to include the origin of the
z
-
axis at its
centre
. The remaining
fraction of air is given by
f
air
= 1
-
f
TP
. After determining the volume fraction, the effective refractive
index was calculated for any
z
using the well
-
known Maxwell
-
Garnett model. Then, the optical
admittance and the corresponding reflection (
R
) and transmission (
T
) spectra of the stack
ed
thin layers
were calculated using a characteristic matrix method
3
.
The nanostructures of the
basal
area
,
however
,
utilize
a
different physics to remain optically
transparent in the visible spectrum.
The
transparency
occurs due to non
-
resonant forward Mie
scattering from low index
chitin
(
n = 1.56)
4
nanostructures
that can be calculated by
rigorously
solving the Maxwell’s equations
5,6
(See Fig. 2f)
.
Finite
-
difference time
-
domain (
FDTD
)
simulations
were performed using a commercial
FDTD
software (Lumerical Solutions Inc.) to numerically
calculate the reflection
(
R
) and transmission (
T
) of the
basal
area.
In order
to compare the simulated transmission spectra of
postdiscal
and
basal
areas with
experimental
spectra
, the
membrane
absorption and
light
reflections
from
its backside
were
considered assuming the wing membrane was surrounded by nanostructures on both sides.
Considering the thickness of the wing membrane
l
(500 nm)
and
absorption coefficient
α
(
α
=
4π
κ
/
λ
3
where
κ
=
0.008 ± 0.001, the
extinction coefficient considered here for
the chitin
)
, the final
transmittance (
T
F
) can be calculated by
2
:
푇
퐹
=
푇
2
푒
−
훼푙
1
−
푅
2
푒
−
2
훼푙
. (2)
The simulated transmission spectra of both
postdiscal
and
basal
areas were plotted in
Supplementary
Fig.
S2
along with the
experimental outcomes
,
showing
good agreement.
The angle
-
independent scattering properties of the
basal
area
as found in Fig. 2j
are directly correlated
to the isotropic spatial frequency of the short
-
range
-
ordered nanostructures. For example, if we
consid
er light with an incident wave vector
k
i
being scattered to a wave vector
k
s
, the difference
between
k
i
and
k
s
can be provided by the spatial frequency
k
b
of the structure, i.e.
k
s
−
k
i
= k
b
7
. Due to
the isotropic nature of the spatial frequency
k
b
(see
the
FFT diagram in Fig.
2D
in
the
main
manuscript), the
k
s
−
k
i
will remain the same irrespective of the
incident
angle, thereby improving the
angle
-
independent scattering properties.
To elucidat
e the biological significance of the dual nano
-
structural basis for transparency of the
C.
faunus
wing, we illuminated the wings under ultraviolet (UV) light and captured images using a
camera (
Supplementary Fig.
S3). No UV signature in the postdiscal area
s was observed, whereas the
basal areas showed violet
-
coloured
reflectance under UV illumination (
Supplementary Fig.
S
3
). The
short
-
range
-
ordered nanostructures with subwavelength periods in the postdiscal areas exhibited
minimal scattering and high
transparency in the UV
-
VIS light. However, similar nanostructures in the
basal areas with
larger
inter
-
structural spacing comparable to the light wavelength
generated
backscatter
ing in the
UV
range
. The short
-
range order of the nanostructures
in the spatia
l arrangement
introduces a phase correlation in the backscattered light, leading to a coherent reflection peak in the
UV regime
as shown in
Supplementary Fig.
S4
A
. The characteristic length scale of the
nano
structure
s
generates
such strong backward scatter
ing of light within a narrow frequency range
8
.
In general, for
any wave vector of
k
>
k
b
/2, short
-
range structural order introduces a phase correlation of light
scattered by adjacent particles
9
.
k
b
ranges between 0.021 nm
-
1
and 0.032 nm
-
1
in our 2D FFT
calculation of the basal a
rea
and hence
k
b
/2
corresponds to the frequencies in the blue spectrum.
Therefore,
a
coherent
backscattered
peak
should
appear
in the
frequencies higher than the blue
spectrum, i. e. in the
UV regime
, which agrees
with
our experimental outcome
.
Butterflies are known to use
the UV regime as a key spectral range for mating signals
11
–
13
, and the
nanostructures with larger spacing in the b
asal area may play an important role in this regard.
The UV
signature with a peak at a wavelength of 345 nm is confirmed by the optical spectra shown in
Supplementary Fig.
S4A
of the basal area. The total reflection of postdiscal area is remarkably low
over the whole UV
-
V
IS
regime. In order to confirm th
at
the
UV reflection of the basal area
is
structur
e
-
based
, we
remove
d
the structural effect
by soaking the wing in b
romoform (
n
= 1.57)
to
match
the
refractive
index
of the inter
-
structural space to that
of the nanostructures
. After soaking,
we
4
repeated the reflection measurement
and
observed
no reflection
from the basal region confirming the
structural origin of the reflection property (
Supplementary Fig.
S4B
).
Therefore, the short
-
range
-
ordered nanostr
uctures on the
C. faunus
wings produce dual optical
functionality
–
transparency in the visible range and reflectance in the UV regime
-
that assists in
camouflaging
1,14
and mating
11
–
13
while keeping the wings sterile by resisting microbial growth (Figs.
S5 and S6).
Supplementary
Section S
I
2
|
Aspect
-
ratio
optim
is
ation of the
nanostructures
on the
Si
3
N
4
surface
As mentioned in the manuscript, an antifouling approach relying on physical lysis
may
damage
tissues and cells that come in contact with the implant,
which may
not
be
suitable for
some
medical
uses.
T
he
aspect
-
ratio
of
the
nanostructures
was kept
below
1 to
rely
on the hydrophilicity of
the
nanostructured
Si
3
N
4
surfaces to
promote
antifouling through anti
-
adhesion instead of
through
physical lysis.
A
literature
survey on this phenomenon
is summarized in
Table S1, reveal
ing
the
aspect
-
ratio
of 1 or greater
will cause
physically induced lysis
on
both naturally occurring and
synthetic nanostructured surfaces.
With this background in mind,
the
nanostructure
topography
was optimi
s
ed to
an
average
aspect
-
ratio
of 0.45
a
nd
a
flat disk
-
shaped top. This
aspect
-
ratio
was chosen
because
there was no significant
statistical difference in the
anti
-
adhesion properties
between
nanostructured
Si
3
N
4
surfaces with
an
aspect
-
ratio
of
0.45
and those with an
aspect
-
ratio
ranging from 0.45 to 0.9
(
Supplementary Fig.
S7
,
S11 and S16
).
Furthermore, optical simulations
indicate that increasing the
aspect
-
ratio
broade
ns the resonance peak
of the
nanostructured
Si
3
N
4
(
Supplementary Fig.
S
10
).
The flat Si
3
N
4
-
membrane
produces
a ballistic
(specular) transmission peak due to the phase delay introduced by the thin membrane that causes light
interference. The integration of
nanostructures
on the Si
3
N
4
-
membrane broadens the total
transmission
-
peak profile due to the combination of b
allistic (due to the thin membrane) and scattered
transmission (due to the nanostructures)
15
.
Supplementary
Section S
I
3
|
Anti
-
biofouling
properties of the
nanostructured
Si
3
N
4
surface
We describe
in this section
our findings on the impro
ved biocompatibility of the nanostructures: the
nanostructures resist protein adhesion as well as prokaryotic and mammalian eukaryotic biofouling
due to
the surface hydrophilicity and nanostructured topology.
To reach our
c
onclusion, we have
performed
extensive
literature
study
on
t
he mechanism
s
behind
the adhesion of plasma proteins,
prokaryotes
,
and eukaryotes on the surface of implanted biomaterials
; and
also
carried out
a
comprehensive set of experimental measurements and theoretical analysis
performed on the
nanostructured
surfaces
.
5
The adsorption
behaviour
of a protein
on
to a surface is a complex process, which
is influenced by
the
nature of the protein as well as the
properties of the
surface
,
and
it
may involve several steps such as
protein association
-
disassociation, change in conformation, dena
turation
,
and charge interaction
between
neighbouring
proteins
16
–
18
. As a result, there is a huge variation
among
underlying
anti
-
bio
fouling
mechanisms
and
resulting outcomes
of surfaces
that have been
proposed
to
control
biofouling
19
–
21
. In the case of
the
nanostructured
Si
3
N
4
surface
presented in this manuscript,
our
r
esults indicate
that the high degree of wettability
(or hydrophilicity)
acts in concert with
the
nanostructured surface topology
to produce
improved biocompati
b
ility. We discuss this
behaviour
of
the substrate
by considering
energy barriers
in the following paragraphs
.
Let us
consider attachment of a protein to a surface first. The reaction can be represented as:
PL + SL ↔
PS
(3)
Where, protein molecules in an aqueou
s media or liquid (PL) are interacting with a surface submerged
in liquid (SL) and leading to adsorption of protein molecules on the surface represented as PS. The
effective free energy change for this reaction can be represented as ΔG
PS
, which is dependen
t on the
interfacial free energies of protein
-
liquid
(γ
PL
)
, protein
-
surface
(γ
PS
)
,
and surface
-
liquid
(γ
SL
)
22
. This
can be shown as
23
:
ΔG
PS
=
γ
PS
-
(γ
PL
+ γ
SL
)
(4
)
For improved biocompatibility and reduced adsorption, the net energy change for the process should
be positive, i.e. ΔG
PS
> 0, and a hi
gher
value of
ΔG
PS
would imply
an
unstable protein
-
surface
interaction or
a higher resistance to biofouling
due to easy detachment
.
The interfacial free energies
are dependent on the interactions between
(1)
the substrate surface and the liquid media
(governed by
the wettability of the surface)
;
(2)
the protein molecules and the liquid media (governed by the
structure and distribution of hydrophobic/hydrophilic residues on the proteins)
;
and
(3)
the protein
molecules and the surface (dependent on both
of the above factors).
Normally proteins hide their
hydrophobic residues away from water while their charged
,
polar amino
-
acid side
-
chains are exposed
to water
24,25
.
As a result, c
harges on the proteins will also
influence
protein
-
protein
interactions, which
can lead to
an
aggregation of proteins in solution.
Noticeably
hydrophilic surfaces such as
nanostructures
improve the affiliation between
the
surface
and water molecules by lowering γ
SL
, which is
favourable
for
improved biocompatibility. If the
protein has a higher degree of hydrophobic residues or
behaviour
, γ
PS
will be higher
, which is
favourable
,
but γ
PL
will also be higher
, which is
unfavourable
. Decrease in hydrophobicity of the
protein will result in both l
ower
ing the
γ
PS
(
unfavourable
) and γ
PL
(
favourable
). Changes in protein
conformation during the surface adsorp
tion process can also occur
16,17
,
changing the interfacial free
energy
(γ
PS
)
.
6
The surface
-
energy analysis indicates that
in the case of
the
nanostructured
Si
3
N
4
surface
, the
increased hydrophilicity of the substrate
also
increases the energy barrier for protein adsorption on the
surface. That is to say, there is a larger energ
y
barrier to
the
replacement of water molecules in contact
with the
nanostructured
Si
3
N
4
surface
(measured contact angle: 1
7
º) with proteins as compared to a
mildly hydrophilic surface such as flat Si
3
N
4
(measured contact angle:
38
º). However,
it is important
to keep in mind that
the degree of resistance to protein adsorpt
ion
also
depend
s
on factors such as the
structure, sequence
,
and nature of
resultant
charges on the protein molecules.
Previously, h
ydrophilic surfaces
,
which effectively bind water molecules and prevent protein
adsorption
,
have been utilized for improved biocompatibility
such
as immobilized PEG
-
based
films
26,27
and self
-
assembled monolayers (SAMs)
28,29
.
However, the protein resistance of these
surfaces decay over time due to factors such as auto
-
oxidation resulting in the formation of more non
-
polar and less hydrophilic functional groups such as aldehyde
s and ethers
30
. Additionally, these
surfaces are susceptible to physical defects and
therefore
are not suitable for long
-
term usage
31,32
. The
noticeable hydrophilicity of the
nanostructured
Si
3
N
4
surface
results from
the physical topology of the
surface and
is expected to show much better long
-
term
reliability
than
chemical coatings.
To isolate the contribution
from the
improved hydrophilicity
to
the deterrence of protein adhesion,
we
plasma
-
treated flat Si
3
N
4
surfaces (
Supplementary Fig.
S
17
A) and compared them with non
-
treated
flat Si
3
N
4
surfaces.
Decrease in protein adsorption as a function of increasing surface wettab
ility
becomes
evident
when
comparing the results obtained for plasma treated and non
-
pla
sma treated
substrates
, as shown
in
Supplementary Fig.
S
17
B
.
After 2 hours of incubation, the extent of protein
adhesion on the plasma
-
treated Si
3
N
4
and
nanostructured
Si
3
N
4
surfaces
are almost the same. This
could be attributed to the dom
inance of the antifouling contribution from the hydrophilicity as the
length
-
scale of the nanotopology of the
nanostructured
Si
3
N
4
surface
is over an order of magnitude
greater than th
e size of proteins
,
implying that
the nanoscale geometry effect
is possibly negligible.
However, after 24 hours, the
nanostructured
Si
3
N
4
surface
displays
the lowest contact angle and
the
greatest resistance
to
protein adsorption
while the
nonpermanent
plasma
-
treat
ed surface
loses its
hydrophilicity
and its
contact angle
returns
back
to
a
value
close
to
that of
a
non
-
treated flat Si
3
N
4
surface
(
Supplementary Fig.
S
17
A
)
.
When considering the case of cellular adhesion to surfaces, we can consider the
following
reaction:
CL + SL
↔ CS
(
5
)
Where, cell
s
in an aqueous media or liquid (CL) are interacting with a surface submerged in liquid
(SL) and leading to adsorption of cellular molecules
on the surface represented as CS. T
he free en
ergy
change can be expressed as:
ΔG
CS
= γ
CS
-
(γ
CL
+ γ
SL
)
(
6
)
7
The effect of surface wettability on the free energies in this case
is also very similar
to that of
proteins.
Improved hydrophilicity of the surface implies that γ
SL
will be lower, which increases the barrier for
displacement of water molecules on the surface by cells and is
favourable
for improv
ing
biocompatibility. The degree
of improvement will once again be dependent on the other two terms
(γ
CS
and γ
CL
), which are dependent on the nature of charges on the cells and their apparent
hydrophilici
ty or hydrophobicity
(discussed in further detail by Liu
et al
.
)
23
.
Indeed, it has been shown
that increase in surface hydrophobicity (contact angle change from 15º to 100º) correlated directly
with increase in surface adsorption of
bac
teria,
algal spores
,
and eukaryotic cells
33
–
36
.
Our results
(
Supple
mentary Fig.
S
17
C
-
D
) show that there is a significant decrease in cellular adhesion upon
increasing the hydrophilicity of flat silicon nitride surfaces through plasma oxidation, which agrees
with the surface wettability model.
The second
important
contribu
tion towards improved biocompatibility for the
nanostructured
Si
3
N
4
surface
originates
from the nanostructured surface topology.
Being in the same length
-
scale or
more
typically
an order of magnitude smaller than cells, n
anotopology plays a greater role in biofouling
resistance against
bacteria and mammalian cells (
Supplementary Fig.
S
17
C
-
D).
Various reports have
claimed that structured surfaces reduce biofouling as compared to flat substrates
21,33,34
.
Two primary
c
a
s
es
can be considered when cells are interacting with patter
ned substrates.
The first
c
ase
is when
cells can elongate to increase their interaction with the surface and fill the gaps
between
nano
structure
s
37
. This cellular elongation directly leads to
an
increase in surface tension along the cell
membrane and has been
modelled
by Pogodin
et al.
assuming a planar piece of membrane
38
. The
increase in interfacial surface energy is described by
38
,
∆
훾
퐶푆
=
∫
휀
휂
0
푑휎
(
1
+
훼
(
푟
)
)
(
7
)
where
η
0
represents
the
surface dens
ity of adsorption sites on the membrane
;
ε
represents energy
gained per unit of adsorption site
;
α
(
r
) represents the local degree
of
cell
membrane stretching at point
r
; and
dσ
is the elemental surface area
.
The
integration is
performed over
the
total
contact area
between the cell membrane and the nanostructured surface. For high
-
aspect
-
ratio structures such as
the nanopillars (diameter 160 nm, height 200 nm
) described by Pogodin
et al
38
,
stretching of the
membrane can eventually lead t
o
rupture and cell lysis. For low
-
aspect
-
ratio
nanostructures
structures
with an
average
diameter
of
345
nm
and
height
of
150 nm
, our experimental results have not shown
any signs of cell lysis (
Supplementary Fig.
S14
-
16
), ind
icating that while membrane elongation is
likely incr
easing γ
CS
in equation 6
and improving biocompatibility of the substrate, cell membrane
s
are
not
r
u
ptu
ring.
The second possible
case
occurs when the cell membrane does not elongate to fill the gaps in th
e
nano
patterned substrate. It has been shown that this
situation
leads to
a
reduction
in
adhesion points
between the substrate and cells
39
,
leading to poor adhesion of cells on patterned surfaces as compared
8
to a flat surface and consequently easier detachment. Therefore,
nano
topology
-
driven
outcomes
such
as membrane deformation or reduction in adhesion points contrib
ute towards destabilizing
the
interaction between the
cell
membrane
and
substrate
,
improving resistance to cellular adsorption. Our
results demonstrate that
nanostructured
Si
3
N
4
surface
shows a drastic decrease in both prokaryotic and
mammalian cellular ad
hesion as compared to a flat substrate (with or without plasma treatment)
due
to the increased contribution from the nanotopology
(
Supplementary Fig.
S
17
C
-
D
).
This is evident
from the fact that greater cell adhesion resistance is offered by the
nanostructured
Si
3
N
4
surface over
the plasma
-
treated Si
3
N
4
surface of a similar contact angle.
To summaris
e,
based on
evidences found in literature
s
and results obtained from our experiments,
we
have
analysed
the underlying mechanism
that
produced
the
muc
h
improved biocompatibility of the
nanostructured
substrate
: it is
the
combin
ation
of (a)
much
-
improved,
nanopattern
-
based,
hydrophilicity
that
increases the energ
y
barrier for protein and cellular adhesion on the substrate
;
and
(b) nanostructured surface topology, which reduc
es
the energy
barrier
for
detachment
of cells from
the surface
and destabilizes cellular adhesion to the substrate
.
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