Nano Express

PAPER • OPEN ACCESS

Photoluminescent properties of liposome-encapsulated amine-

functionalized nanodiamonds
To cite this article: J Douda et al 2020 Nano Ex. 1 030009

View the article online for updates and enhancements.

This content was downloaded from IP address 187.178.206.161 on 27/10/2020 at 16:43

 Nano Express 1 (2020) 030009 https://doi.org/10.1088/2632-959X/abc1c5

PAPER

Photoluminescent properties of liposome-encapsulated amine-

OPEN ACCESS
functionalized nanodiamonds
RECEIVED
22 September 2020
J Douda1 , C R González-Vargas1,2 , I I Mota-Díaz1 , E V Basiuk3 , X A Hernández-Contreras1,
REVISED
12 October 2020
J A Fuentes-García1,4 , J Bornacelli5 and C Torres-Torres5
1
UPIITA—Instituto Politécnico Nacional/Othón Mendizábal S/N, La Escalera, 07320, Cd., México
ACCEPTED FOR PUBLICATION
2
15 October 2020 ISMO—Institut des Sciences Moléculaires d’Orsay, CNRS, Université Paris-Saclay, 91405 Orsay, France
3
ICAT—Instituto de Ciencias Aplicadas y Tecnología, Universidad Nacional Autónoma de México, Circuito Exterior C.U. 04510 Cd.,
PUBLISHED
27 October 2020 México
4
INMA—Instituto de Nanociencia y Materiales de Aragón, Universidad de Zaragoza, Mariano Esquillor s/n 50018, Zaragoza, Spain
5
ESIME-Zac—Instituto Politécnico Nacional/Othón Mendizábal S/N, La Escalera, 07738, Cd., México
Original content from this
work may be used under E-mail: [email protected] and [email protected]
the terms of the Creative
Commons Attribution 4.0 Keywords: nanodiamonds, biosensors, theranostic liposome, photoluminescence, all-optical sensors
licence.
Any further distribution of
this work must maintain
attribution to the Abstract
author(s) and the title of
the work, journal citation In the present work, amine-functionalized nanodiamonds (NDs) have been encapsulated in liposomes
and DOI. and studied in order to observe the modification of their photoluminescence properties. NDs were
functionalized with aromatic amines such as 1-aminopyrene and 2-aminofluorene, and the aliphatic
amine 1-octadecylamine. Morphology, structural and optical properties of NDs and amine-modified
NDs were analyzed by transmission electron microscopy, atomic force microscopy, scanning electron
microscopy, and photoluminescence. The amine-functionalized NDs were successfully encapsulated
in lecithin liposomes prepared by the green and conventional methods. The obtained results show
significant changes in photoluminescent properties of functionalized NDs, and were more
potentialized after liposome encapsulation. Our findings could be applied in the development of new
kinds of water-dispersible fluorescent hybrids, liposome-NDs, with the capability of drug encapsula-
tion for use in diagnostics and therapy (theragnostic liposomes). All-optical sensors with possibilities
for tailoring their response for other biomedical applications can be also contemplated.

1. Introduction

The combination of optical properties such as Raman gain, strong linear and nonlinear refractive index, wide
bandgap, and high stability of emission (Laube et al 2019), makes nanodiamonds (NDs) a very promising
material for research and technological applications. Besides, the large surface area derived by surface
modification or doping, promotes a reduced cytotoxicity in NDs with a crucial potential in sensing and
instrumentation fields. Nanoelectromechanical systems (NEMS), magnetic and electric field sensors, integrated
Raman lasers, frequency combs, bio-medicine probes, bio-sensors, bio-imaging by cell labeling/monitoring,
and drug delivery systems are some attractive examples for NDs applications (Loncar and Faraon 2013, Kumar
et al 2013, Xiao et al 2015, Lake and Bouchard 2017, Pichot et al 2017, Tinwala and Wairkar 2019).
Diverse biomedical functions can be better explored or handled by using dispersible NDs in stable aqueous
solutions. Therefore, the application of liposomes to encapsulate NDs seems to be a suitable area of research.
Above all, it is well-known that liposomes allow encapsulation of drugs or other substances. The liposomes
consist of phospholipid bilayers that self-close to form spherical nanoparticles. Due to the presence of
hydrophilic internal volume and phospholipid bilayers, amphiphilic substances can be delivered by liposomes.
Recent developments of theragnostic medicine combine therapy and diagnostic in the same vehicle for
developing optical methods of detection (Pham et al 2017, Seleci et al 2017, and references therein). The
theragnostic applications of liposomes can be particularly useful for drug delivery associated with cancer and
other diseases therapy (Turcheniuk and Mochalin 2017, Morales-Zavala et al 2018, Patra et al 2018). The new

© 2020 The Author(s). Published by IOP Publishing Ltd

Nano Express 1 (2020) 030009 J Douda et al

theragnostic medicine permits monitoring in vitro and in vivo drug pharmacokinetics and pharmacologic
efficiency studies (Jia et al 2019). The theragnostic liposomes with the NDs applications may improve their
optical properties, specially for applications related to nano biosensors, and optoelectronic devices. Another
advantage of the liposomes concerns the potential conjugation of their surface with other molecules as target
agents (peptides, antibodies, cations), resulting in selectivity, or their targeted delivery into cells, systems, and
organs of the body; and stability in biologic media.
Therefore, the hypothesis of this study is that the NDs with different amines on their surfaces, and liposome-
encapsulated, can give modification of the optical properties up to enhanced luminescence. And this in turn, can
allow luminescence detection of these hybrids for their application in theragnostic liposomes and biosensors.
Multiple applications of NDs are based on the chemical and structural properties of NDs. The diamond core
is composed of sp3, and the amorphous shell by sp2 hybridized carbon atoms (Zhang et al 2018). The dense
packing of sp3 in the core of NDs is responsible for their chemical and photostability (Giulia 2010, Hemelaar et al
2017, Laube et al 2019). The sp2 hybridization in NDs surface leads to a versatile chemical nature and makes this
nanomaterial suitable for chemical functionalization (Pichot et al 2017).
Therefore, in this work, we analyzed the influence of functionalization and encapsulation of NDs in their
optical properties. Herein is identified for the first time the signature that corresponds to optical emission of this
type of hybrids based on liposomes with pristine and functionalized NDs encapsulates. To our knowledge, there
are no reports where the encapsulation of NDs is presented, nor of their amino-functionalized versions in
liposomes and their PL properties for applications in theragnostic liposomes and the possibility for revealing
them by this method. This also includes fluorescent microscopy, which is used for imaging and emission in areas
of biology and medicine. Thus, the role of liposome encapsulation of amine-functionalized NDs seems to be a
key aspect for developing tailored nanoprobes using fluorescent NDs. And, as already mentioned, the liposome
encapsulation of NDs may offer their water dispersibility for biomedical applications as biomarkers in
theragnostic liposomes.
Different synthesis methods of NDs have been reported, but only the main detonation techniques that
correspond to laser ablation, and high-energy ball milling of high-pressure with high-temperature are being
used commercially (Fang et al 2013, Guillou et al 2007) . The pristine NDs possess a large bandgap of 5.5 eV, and
like all semiconductor quantum dots, they possess high photostability and bright multicolor fluorescence;
however, their core emission may increase up to 8.8–9.1eV by decreasing their particle size (Mochalin et al
2012).
The optical properties of doped NDs are highly dependent on their synthesis methods and on the nature of
the dopant (Fokin and Schreiner 2009). The color centers are developed due to a compression in NDs structure
by an impurity atom (N, Si, B or Cr), a vacant lattice site, or a trapped electron, and due to that, the energy gap
can be decreased to the similar value of bulk diamonds (Dolenko et al 2012). The dominant impurity on NDs is
nitrogen, forming vacancies adjacent to the substitutional nitrogen atoms color centers (NV) of 2p origin (Fokin
and Schreiner 2009, Kovalenko et al 2012). And, because of this, HOMO and LUMO of nitrogen p-electrons by
the addition of new levels may reduce the band gap in NDs. This in turn, becomes one of the most important
properties of NV in NDs: an easily detectable luminescence in visible spectra, highly desired for biomedical
applications with no photo-bleaching or blinking (Loncar and Faraon 2013, Lake and Bouchard 2017).
However, frequency-selective photonic control is still a challenge due to the NV broadband fluorescence
emission compared to other quantum emitters at room temperature. Thus, the H3 defect center (N-V-N) in 35
nm size diamonds has green emission (at 531 nm), and NDs functionalized with octadecylamine (ODA) present
additional blue emission (at 480 nm) to the set of red and green colors of pristine NDs (Mochalin and
Gogotsi 2009).
Also, the pristine NDs surface containing disordered carbon, and small graphitic nanoclusters, may add
excitation levels in the NDs due to structural inhomogeneity, defects, and mixture (Mona et al 2012, Treussart
and Vlasov 2017). The amorphous core´s fluorescence could be enhanced due to the surface functionalization,
the surrounding medium, and pH (Mona et al 2012, Mochalin et al 2012). The theoretical simulations of band
gaps have been performed for NDs particles of sizes from 1 to 3.3 nm, and it has been identified that the quantum
confinement effects strongly dependent on particle size, morphology, shape, and the incorporation of
heteroatom functionalities (Drummond et al 2005, Barnard 2009, Fokin and Schreiner 2009). The broadband
between 400–600 nm is also observed for almost all nanocrystalline diamonds with sp2 phase between and on the
nanocrystal surfaces, where the band at 430 nm (in the blue spectral region) corresponds to volume defects,
recently assigned to –OH bonds; and at around 520 nm to –COOH and C–O–C groups (Xiao et al 2015, Stehlik
et al 2016, and references therein). The NDs surface often has charge traps that involve non-radiative
recombination pathways. Upon introduction of the coating of the molecule, such traps are suppressed, and
several non-radiative recombination channels are eliminated. However, a priori measurements indicate that the
quantum efficiency of a single NV center in a NDs is not unity, and it can be significantly improved by using a
coating with organic molecules, resulting in brighter fluorescent NDs (Bray et al 2015, and references therein).

2
Nano Express 1 (2020) 030009 J Douda et al

Changes in shape and spectral positions of the NDs PL band have been observed and found to depend on the
excitation wavelength. With this motivation, we employed a standard 355 nm excitation wavelength for PL
measurements in this work; this wavelength has not been used in comparative publications. Emission peaks of
high energy, related to this double modification of NDs surfaces by the assistance of amine-functionalization,
and liposome encapsulation were analyzed.
Amplification in PL phenomena in encapsulated NDs can be associated with surface energy traps
elimination and transfer between proteins and surface nanostructures, particularly the graphite-like
nanoclusters. These considerations are important for biological and medical applications of NDs used as a
biocompatible label (Perevedentseva et al 2011).
As we mentioned before, the organic fluorophores may promote quenching by resonance energy transfer to
the non-fluorescent group (Lakowicz 1999). Thus, fluorene-based conjugated compounds have emerged for the
use as light-emitting diodes due to their high PL and electroluminescence quantum efficiencies, easy film-
forming, thermal stability, good solubility, and ready color-tuning through the incorporation of low-band-gap
co-monomers. Several approaches based on local electromagnetic environment modifications have been
explored to tune the energy of emitted photons. The modifications in the spectral shifts and intensity increase in
PL signals could be induced, enhanced, and controlled by attaching different organic molecules, halogens, and
surrounding media variations (Mochalin et al 2012, Mona et al 2012, Hasanzadeh et al 2019).
In addition, other poly-nuclear aromatic hydrocarbons may form excimers (the dimer components in the
excited states, or their complexes) and upgrade non-linear optical response (Rourke et al 2011, Du et al 2015).
The hyposochromic shift of energy (up to higher energies) in the PL spectra of NDs could be obtained from
removing the amorphous carbon and surrounding the crystalline NDs due to their interaction with 1-undecene
(Kompan et al 1997).
Based on our previous studies on other biomarkers encapsulated in liposomes, we know that the liposome
encapsulation of semiconductor quantum dots of CdSe and CdSe/ZnS may produce additional surface tension,
and subsequently, luminescence properties enhancement (Douda et al 2018 and 2019a). Recently we reported
studies on optical properties modification of graphene oxide chemically functionalized by amine molecules
(Douda et al 2019b).
It is worth mentioning that in the references about the NDs PL, the excitation only up to 405 nm and lower
have been employed (Chung et al 2007, Mona et al 2012, Turcheniuk and Mochalin 2017, Afandi et al 2018). Su
and coworkers (2016), report transient fluorescence properties of the NDs under excitation at 280 nm
wavelength of PL decay curves, and only aliphatic amine 1-octadecylamine (ODA) and 1-undecene
functionalized NDs (Mochalin and Gogotsi 2009, Astuti et al 2014), respectively.
In the present work, we studied the optical properties of the pristine and amine-functionalized NDs before
and after encapsulation in liposomes; a 355 nm laser beamline was used to excite the NDs samples.
NDs were functionalized with two aromatic amines: 1-aminopyrene (AP) and 2-aminofluorene (AF), and
one aliphatic amine, ODA by method for chemical functionalization widely used by Basiuk and collaborators to
functionalize carbon nanomaterials (Basiuk et al 2012 , 2013, and references therein).
After that, the NDs pristine and amine-functionalized were encapsulated in liposomes, prepared from
soybean lecithin by two different methods. The optical properties of the obtained samples were systematically
studied by PL measurements. The PL spectra of all functionalized materials showed significant changes
dependent on the amine structure attached to NDs surfaces, and they were more pronounced after the liposome
encapsulation. We highlight that no change between PL results for both encapsulation methods (conventional
and green) were observed, which suggest that any type of liposomes can give the effect of increasing emission
energy in NDs PL. We state that PL properties of NDs can be tuned through chemical functionalization of NDs
with amine molecules and subsequent liposome-encapsulation, which opens the door to further development of
new theragnostic liposomes, light-emitting devices, and nano biosensors based on such systems.

2. Materials and methods

NDs samples featuring a 6 nm average size and functionalized with AP, AF, and ODA by method widely reported
(Alzate-Carvajal et al 2016), and amino-functionalized ND samples were obtained: ND-AP, ND-AF and ND-
ODA, respectively.
The liposomes encapsulation of NDs was performed by a ‘green’ method (without organic solvent
application), reported before ( Douda et al 2019a ) from commercial soybean lecithin (liquid and dried). Briefly,
the dispersion of soybean lecithin (120 g l−1 g) in an aqueous solution of 10−5 M NaCl was swollen during 24 h.
For each sample, 60 μg of the lecithin previously prepared, a lecithin solution was taken, mixed with the NDs
samples and (phosphate buffer saline) PBS to obtain a total amount of 500 μl. The liposome-encapsulated NDs
samples obtained by the ‘green’ method were: LND, LND-ODA, LND-AP, LND-AF.

3
Nano Express 1 (2020) 030009 J Douda et al

The sonication process was carried out with ultrasonic equipment (Sonics and Materials, VCX-130) at 20
kHz equipped with a Titanium Probe (6 mm in diameter) for 20 min. Preselected cycles of 5-s alternate on-off
program with a total treatment time of 5 min were applied. The NDs and their functionalized samples were
added to the dried phospholipids bilayer before rehydration by PBS (pH=7.4). Cooling up to −20 °C was
applied after all sonication processes and the samples were delivered to ambient temperatures before further
sonication. The process was repeated 3 times for all samples prepared by triplicate.
The conventional method of liposomes preparation is known as the lipid bilayer rehydration method
(Amselem et al 1990). A solution of 100mg of soybean lecithin powder in 10 ml of chloroform/methanol (9:1, v:
v) was prepared, 400 μl of this solution was taken in a round bottom tube to which one of the NDs was added. A
vacuum atmosphere was employed until the organic solvents were completely evaporated. The thin lipid bilayer
obtained was left vacuumed overnight to remove traces of solvent. The resulting thin film was hydrated with 2
ml of PBS (pH=7.4), and sonicated for 30 min with a power output of 65 W. The solution obtained was
extruded in a mini Extruder Avanti Polar Lipid with a 0.1 μm polycarbonate membrane 11 times. Subsequently,
it was centrifuged at 38 000 RPM for 60 min in the ultracentrifuge Beckman Coultier 90L, and the obtained
pellet was resuspended in PBS. The solution was stored in refrigeration for further analysis. The liposomes
prepared by conventional methods for NDs encapsulation were: pure liposome, L*ND, L*ND-AP, L*ND-AF.
For the morphology characterization, SEM observations of sample powder were performed in a JEOL JSM-
6510LV at low voltage (5 kV), while for TEM images, samples diluted in ethanol were deposited as droplets in
Lacey copper grids and were observed in a Tecnai F30 high-resolution analytical transmission electron
microscope (300 kV). The atomic force microscopy (AFM) measurements were made by using an AFM multi-
mode system in taping mode.
The PL spectra were measured by exciting the samples with the third harmonic of a Nd:YAG laser (λ=355
nm, 25 ps ) at 300 K using a UV-VIS spectrometer (USB2000+Ocean Optics) connected to an optical fiber. For
most of the samples studied in this work, PL emissions were visible to the naked eye. This PL condition made the
implementation of our experimental setup easy in different directions of the emission. The PL light coming from
the samples was collected with a convex lens of 5 cm in diameter, in order to acquire the PL light in our
experimental setup. The optical fiber was carefully placed in the convex lens focus and coupled to the acceptance
angle of the fiber. The PL measurements were performed on liquid samples for ‘green’ liposomes. For the
conventional method of liposome preparation, the suspensions of pristine and functionalized NDs in PBS or
ethanol were dried in the form of droplets on Si substrate. For liquid samples, the PL emissions were detected in a
right-angle configuration to avoid the reflected laser signal. In the case of deposited samples on Si substrate the
PL signal was collected from the side of the incident laser and a long wave pass filter was used to avoid laser
reflections. In both cases, the samples were positioned in an XYZ stage and different samples were excited at the
same incident and detection angles, in order to get confident comparative measurements of absolute PL
intensity of a set of samples. PL intensity as a function of laser pump energy per area unit at 355 nm was also
measured. Samples were excited to reach the saturation level required for the emitted PL intensity. In a two-level
model (Wojdak et al 2004), it is expected that the saturation regime of the PL intensity only depends on the
quantum efficiency of the samples, and this allows us estimating the absolute increase of the PL intensity. The
spot size was around 4 mm and the pump energy per area unit used was below 300 μJcm−2 to avoid heating
effects.
For further investigating the processing of photonic signals in the L*NDs, a standard two-wave mixing
experiment of the pump and probe beams was conducted with an intensity rate 1:1 with our Nd:YAG laser
system. The polarization of the incident beams was linear and the geometric angle between the incident beams
was close to 30° just before the interaction with the sample. A total maximum irradiance of 100 MW cm−2 in
single-shot mode was used for the experiments. A CS2 sample with a nonlinear refractive index n2=4×10−14
cm2 W−1 was employed for the calibration of the experimental setup. The rotation of the polarization of the
probe beam was measured by using a cross-polarized analyzer behind the sample.

3. Results and discussion

In figure 1, the schematic structure of amine-functionalized NDs is presented. The suggested chemical reactions
of amine NDs functionalization with amines have been proposed before (Alzate-Carvajal et al 2016).
Comparative SEM images of NDs pristine and functionalized (ND-AP, ND-AF, and ND-ODA) are shown in
figure 2. Figure 2(a) revealed large agglomerates of NDs of 20–30 nm size. Dried NDs could be re-aggregated due
to capillary forces pulling the individual nanoparticles together; also, attractive van der Waals forces promote the
mentioned process as previously reported (Mochalin et al 2012). Organic amine functionalization altered in an
evident way the morphology of ND-ODA samples (figure 2(b)), and larger agglomerates of about 1–5 μm were
formed due to the stronger inter-particle interactions caused by the covalent functionalization with long

4
Nano Express 1 (2020) 030009 J Douda et al

Figure 1. Schematic chemical structures of organic amines attached to NDs surfaces: (a) ND-AF, (b) ND-AP, and (c) ND-ODA.

Figure 2. SEM images of: (a) commercial pristine NDs powder, (b) ND-AF, (c) ND-AP, and (d) ND-ODA samples Scale bar: 5 μm.

Figure 3. TEM images and histograms of NDs samples before amine modification (a); (b) zoom and corresponding simulated
diffraction pattern; (c) ND-AF; (d) ND-AP; (e) ND-ODA.

hydrophobic radicals of ODA. The aggregation of NDs can be prevented by ultrasound treatment in NaCl
solution (Bondar´ and Puzyr´ 2004), or by centrifugation.
Representative TEM images of our NDs samples are shown in figure 3. The pristine NDs particle average size
was around 4.2 nm (figure 3(a)). Figure 3(b) reveals the crystalline structure of pristine samples (Fayos 1999); the
distance between planes (3.6 Å) corresponds to the (110) orientation of diamond (sp3 hybridization) of cubic
shape (Barnard 2009). The simulated diffraction pattern obtained and observed using the Fast Fourier

5
Nano Express 1 (2020) 030009 J Douda et al

Figure 4. Cryo-TEM micrograph of lecithin liposomes.

Figure 5. Tapping-mode AFM micrograph of lecithin liposomes.

Transform (FFT) in DigitalMicrograph software confirms an oriented array of the core and two points of
diffraction.
However, some dispersion of the brilliant points suggests the presence of an amorphous shell (sp2
hybridization) characteristic of the surface of NDs. The amine-functionalized samples particle sizes were slightly
increased in all cases and the biggest particles (of 7.2 nm) observed for ND-ODA samples (figure 3(e)) are
strongly dependent on the amine structure attached to NDs surfaces as revealed in SEM images. For ND-ODA
the increase in the size of the agglomerates may be due to the interactions between the particles, covered with
long aliphatic chains, and the interaction of woolly spheres.
In the ND-AP sample, the intensity was increased. This can be attributed to an excimer or oxidative debris
formation after the NDs functionalization with aromatic amines (AF and AP) due to π-π interactions of poly-
aromatic fragments (Rourke et al 2011). This effect has been described in graphene oxide (GO) studies (Douda
et al 2019b). This type of agglomerate can change average size, thus, resulting in a modification of the optical
properties of amine-functionalized NDs.
The lecithin liposome average size was evaluated by the Cryo-TEM micrograph and Tapping-mode AFM
micrograph and corresponds to 80–200 nm. The respective images are presented in figures 4 and 5, respectively.
The comparison of studied PL spectra of NDs and amine-functionalized samples, before and after
functionalization, is illustrated in figure 6(I), and the same samples after ‘green’ liposome encapsulation in
figure 6(II).

6
Nano Express 1 (2020) 030009 J Douda et al

Figure 6. Normalized PL spectra excited at 355 nm in solutions of: (I) NDs; (II) LNDs.

Table 1. PL peaks positions for NDs before (ND, ND-

ODA, ND-AF, ND-AP) and after (LND, LND-ODA,
LND-AF, LND-AP) liposome encapsulation.

Sample PL2, nm PL3, nm PL4, nm

ND 431 477 529

LND 423 465 508
ND-ODA 425 480 526
LND-ODA 424 466 515
ND-AF 426 482 534
LND-AF 424 462 512
ND-AP 433 467 520
LND-AP 428 459 514

The NDs samples produced a broadband PL spectrum in the range of 380–700 nm excited at the ultraviolet
wavelength (355nm). The deconvolution of this band showed four peaks at 402, 431, 477, and 527 nm (PL1, PL2,
PL3, and PL4, respectively), see figure 6(I), and table 1. The intensities of pure amines were extremely low in
comparison to typical NDs samples.
Except for ND-AP, in all functionalized samples, the first peak (at 402 nm), which tentatively corresponded
to the diamond core emission, did not change its position. However, the adjacent peaks (PL2–PL4) show
variations in all samples. The peak at 420 nm is expected to correspond to volume defects in NDs, and the peak at
530 nm to –COOH, or –C–O–C functional groups. However, this peak can also be attributed to: (i) structural
disorder on the diamond surface; (ii) presence of carbon in the threefold-coordinated state; (iii) dangling bonds
on the surface of the nanoclusters, and (iv) intrinsic defects of a single–crystal diamond ( Kompan et al 1997),
and/or, to the presence of an amorphous sp2 shell.
In the PL spectra of NDs functionalized with 1-aminopyrene (ND-AP) the first peak at the blue region is not
present. The subsequent three peaks show hyposochromic s hift from 431 nm to 433 nm, from 477 to 467 nm,
and the last one from 529 to 520 nm, if compared to pristine NDs spectra. For ND-AF samples the second peak
has a significant hyposochromic shift of energy (from 431 to 426 nm), and for the next two peaks the
bathochromic shift from 477 to 482 nm, and 529 to 534 nm. The ND-ODA samples show a hyposochromic shift
of the second and fourth peaks (from 431 to 423 nm, and 529 to 526 nm, respectively), and the bathochromic
shift (to lowest energy) of the third peak from 477 to 480 nm; it corresponds to a slight intensity increase in
comparison to pristine NDs spectra.
Also, the PL spectra for non-encapsulated NDs samples measured in ethanol solutions demonstrated the
quenching effect of the solvent (not presented here), with the intensities of the emissions several orders of
magnitude smaller, and all observed energies presented the red shift for functionalized samples in comparison to
pristine NDs spectra.
Liposome encapsulated (by the ‘green’ method) amino-functionalized NDs samples showed hyposochromic
effect for all samples (figures 6(II) and 9, table 1). The first peak at 402 nm disappears, and the second one

7
Nano Express 1 (2020) 030009 J Douda et al

Figure 7. (a) Emitted photons of PL spectra excited at 355 nm of LNDs, LND-ODA, LND-AP and LND-AF; (b) Absorbed photons
related to the UV-VIS spectra of LNDs, LND-ODA, LND-AP and LND-AF (c) Normalized integrated PL intensity of pu re Liposomes,
L*NDs, L*ND-AP and L*ND-AF as a function of laser energy per unit of area; (d) Non- linear PL emission exhibited by L*NDs.

emerges at 423 nm. Also, the PL intensity for liposome-encapsulated samples was enhanced in comparison to
non-encapsulated NDs, with the exception to LND-AP. It is worth noting that the same effect has been observed
in NDs samples encapsulated in liposomes prepared by the conventional method. Also, the spectral
characteristic of the conventionally prepared liposomes keeps unchanged when they are deposited on silicon
substrates, which is important for developing light-emitting and optoelectronics devices.
A direct determination of the quantum yield in the samples was obtained by measuring the number of
emitted photons (see figure 7(a)) and the number of absorbed photons (figure 7(b)). The quantum yield for the
different samples corresponds to the following values: LND=0.1185, LND-AF=0.0198, LND-AP=0.0324
and LND-ODA=0.0489. These results are in good agreement with previous quantum yields reported in NDs
(Bradac et al 2019).
Also, the PL of NDs functionalized with amines and encapsulated in liposomes by the conventional method
was analyzed as a function of the incident laser pulse energy. The PL intensity from L*ND-AP was higher in
respect to pure liposomes, pristine L*NDs, and other amine-functionalized samples.
At lower laser energy the PL increases linearly for all samples. However, the slope of the plot is higher for the
functionalized samples in comparison to L*NDs (figure 7(c)). This indicates that the excitation cross-section of
the functionalized samples has increased when comparing them to the pure liposome and the NDs. In particular,
the L*ND-AP sample has a more pronounced slope, almost 6-fold enhanced in contrast with the L*NDs
samples. The excitation cross-section for L*ND-AF and L*NDs samples have almost the same value but
enhanced by a factor of 2 with reference to the pure liposome samples. The PL enhancement at the saturation
regimen pointed out that for the L*ND-ODA sample the PL quantum efficiency increases by a factor of about 4
in comparison to L*NDs. In contrast, t he enhancement factor of the PL quantum efficiency for L*ND-AF and
L*ND-AP samples are about twice and three times higher than L*NDs.
Saturation in the PL emission as a function of the incide nt irradiance was measured between 60 MW cm−2
and 100 MW cm−2 in the L*NDs, as shown in figure 7(d). In the nonlinear regime, the results show no
modification in the location of the peaks of emission, as well as a lack of photothermal or ablation actions.
Therefore, it can be stated that an induced transparenc y is present under excitation of the sample by picosecond
pulses.
Multi-photonic effects in L*NDs indicate the possibility to fully occupy quantum levels by nonlinear optical
signals in the sample. Thus, the potential control of information and energy transfer in NDs can be considered
for encoding information in light by all-optical modulation mechanisms assisted by encapsulation processes.

8
Nano Express 1 (2020) 030009 J Douda et al

Figure 8. Optical phase-change induced by a two-wave mixing in an optical probe signal for L*NDs.

Two-wave mixing experiments were undertaken to explore any potential induced birefringence on the
propagation of the beams interacting in the L*NDs samples studied. The evolution of the phase-change in the
sample as a function of the estimated nonlinear refractive index n2=−2×10−13 cm2/W for the L*NDs is
shown in figure 8.
Figure 8 clearly describes that the incident irradiance of the pump beam can modify the optical phase in the
probe beam in our sample. A polarization-resolved effect can be also observed regarding that the superposition
of the incident beams is able to generate an irradiance interference pattern that automatically modulates the
polarization and the phase of the probe beam in the interaction. Light controlled by light in a two-wave mixing
configuration can be useful for developing quantum functions in an ultrafast temporal regime.
In this work, a clear indication of the modification in PL and nonlinear optical phenomena derived by the
encapsulation of NDs was analyzed. The results highlight the evolution of the nonlinear optical signals induced
in encapsulated and functionalized NDs samples. The NDs seem to be dominantly responsible for multi-
photonic effects in all cases in our study. But functionalization and encapsulation can play an important role in
the potential functions of this nonlinear response. We report that optical phase-changes generated by a two-
wave mixing can be employed for immediate all-optical applications. The understanding of simple third-order
optical nonlinearities proposed in this manuscript can be a base for developing future research of nanostructures
that can be related to instrumentation and sensing functions.
The effect of wavelength-shift of emission energy and intensity after NDs encapsulation in liposomes
prepared by both methods (green end conventional) and measured in solution or silica surface cannot be
attributed to the presence of a solvent, silica, or the method of liposome preparation. Thus, amine
functionalization offers surface modification due to amidation reactions (Astuti et al 2014, Alzate-Carvajal et al
2016, Alzate-Carvajal et al 2018, and references therein). Also, the studied aromatic and aliphatic amine-
functionalized samples together with highly oxidized fragments (oxidative debris), provoke planar conjugated
domains (Rourke et al 2011, Kumar et al 2012), or formation of the interaction of woolly spheres, and produce
new effects and tension forces, and effectively reduce the sp2 surface defects. These effects are likely to be
involved in the change of the PL properties observed in figure 6(I).
On the other hand, as it was reported by Mona et al 2012, the PL enhancement may be caused by the
combination of the intrinsic PL of NDs core with trapped excitation originated from surface defects (disordered
carbon, graphite, and other sp2 hybridized peculiarities) that can be transferred to the set of energy levels. From
figure 9, a comparative PL modification in NDs can be visualized, considering that amine-functionalization and
liposome encapsulation may reduce some surface defects and induce additional levels in the band gap in
comparison to pristine diamonds, and doped NDs. Also, Fokin and Schreiner (2009) concluded that the band
gap in NDs is determined only by the nature of dopant rather than the size in the cage. This is due to the
dominant contributions of the atomic orbitals of the dopant into the HOMOs and the LUMOs.
It is worth mentioning that other important phenomena are suitable to be assigned to the encapsulation of
the NDs in liposomes (figure 6(II)). For instance, when NDs are encapsulated in a lipid bilayer, additional
compressive stress can be incorporated on the NDs, and this results in a modification of their optical pr operties.
The liposome bilayer width in our case is estimated to be around 5 nm but it may vary with the type of

9
Nano Express 1 (2020) 030009 J Douda et al

Figure 9. Graphical representation of PL modification of diamonds upon their structural modifications among bulk diamonds, NDs,
amine-functionalized and liposome-encapsulated NDs, reported in this work.

phospholipids used. The hydrophobic particles of small size, like N Ds (4–6 nm), may be enclosed on a lipid
bilayer because of their hydrophobicity. Consequently, a larger additional tension, and respectively, an increased
emission energy can be expected (figure 9). Also, to be considered, soybean lecithin phospholipids in liposomes
are charged molecules and induce the electric charge in the surface area of NDs, which in turn produce higher
energy gap changes for applied NDs.
Amine-functionalized and liposome-encapsulated NDs show promising properties for improving quantum
yields and tuning PL of NDs for their application as multifunctional biomedical imaging fluorescent markers.
The mechanism of the PL enhancement of NDs functionalized with amine molecules is not clear yet and
engineering their respo nse is still a challenge. However, there is experimental evidence on altering the
transition-energy levels in nanostructures by using organic amines, liposomes, and solvents for NDs PL
modification. Different organic amines have been eval uated as PL tuning agents and the responses are strongly
dependent on the hydrocarbon structure and functional groups on NDs surfaces.
The surface-to-volume ratio in nanomaterials is a fundamental advantage for designing nanoscale effects
because they are strongly sensitive to their size, the presence of impurity atoms and the shape of NDs
nanostructures. Any slight modifications of their surface may produce considerable modifications in their
emission properties. Changes in the atomic dipole moment can be explained by the electromagnetic field
allowed near and out of the surface of nanoparticles. And an important influence can be expected from the
surrounding of NDs in the electronic dynamics governing the physical mechanisms responsible for their
photonic phenomena. Particularly, the participation of functionalization processes in NDs may derive in
changes in population loss through radiative and non-radiative processes of the upper quantum level of
excitation, and also a modification in the polarization loss that describes the evolution of a nanostructured
system. Analogically with the semiconductors, nanometric diamonds may show a band gap modification effect
(Wu et al 2010, Perevedentseva et al 2011, Mochalin et al 2012, Osipov et al 2020). It is well known, that due to
the effective particle size reduction, the quantum confinement effect can increase (Kryshtab et al 2012, Polupan
et al 2017), and eventually, a reduction in semiconductor nanoparticles effective sizes may be derived from
liposome encapsulation (Douda et al 2018, and 2019a). These considerations allowed us to contemplate
encapsulated NDs with PL tuning advantages. The original approach combining nanotechnology and solid-state
chemistry methods opens the way to the building of innovative materials for integration and multifunctionality.
These are two fundamental points in multidisciplinary fields of applications such as electronics,
telecommunications, optics, environment, and biomedical functions (Liu et al 2013, Torres Sangiao et al 2019).
The main value of our work is based on the evaluation, for the first time, of the PL phenomena exhibited by
functionalized NDs and their modification by the liposome encapsulation. The PL spectra of the NDs were
measured before and after their encapsulation in liposomes, prepared by two comparative methods starting
from soybean lecithin. These emission effects can be analyzed by a straightforward PL technique without any
special preparation, in contrast with the common conditions currently mandatory in clinical laboratories (Patra
et al 2018, Bamburowicz-Klimkowska et al 2019, Torres Sangiao et al 2019). It can be considered that
theragnostic liposomes containing NDs with enhanced optical properties are quite viable, due to their
biocompatibility and potential assistance in fluorescence microscopy. Besides, encapsulated NDs-based samples
can be a useful tool for sensing and instrumentation of signals in biomedical sciences.

10
Nano Express 1 (2020) 030009 J Douda et al

4. Conclusions

Pristine and amine-functionalized NDs have been encapsulated in soybean liposomes prepared systematically
by two different methods in this work by means of PL studies. The structure of applied amine promotes different
modifications in effective size and luminescence response of NDs. The liposome encapsulation increases the
optical response of both: the intensity and maximum emission energy. The obtained optical function
modifications in the synthetized NDs-liposome hybrids may play a crucial role in the development of
theragnostic liposomes and all-optical sensors, opening the possibility for their usefulness in other biomedical
applications.

Acknowledgments

The financial support from the Instituto Politécnico Nacional (grants SIP-IPN, Mexico), Universidad Nacional
Autónoma de México (grant DGAPAIN101118), and Consejo Nacional de Ciencia y Tecnología (postdoctoral
grants 711124 and 2019-000019-01NACV-00297) was fundamental for the development of this work. The
authors kindly appreciate the scientific support from Dr V A Basiuk (Instituto de Ciencias Nucleares, UNAM)
for sharing the functionalized ND samples, and Victor Meza Laguna for SEM images. Authors would like to
acknowledge the use of Servicio General de Apoyo a la Investigación-SAI, Universidad de Zaragoza, and LMA
microscopy laboratory at INA for the facilities in TEM.
The data that support the findings of this study are openly available under request to the corresponding
author.

ORCID iDs

J Douda https://orcid.org/0000-0002-5316-7088
C R González-Vargas https://orcid.org/0000-0002-5132-2662
I I Mota-Díaz https://orcid.org/0000-0002-1802-9886
E V Basiuk https://orcid.org/0000-0003-0877-242X
J A Fuentes-García https://orcid.org/0000-0003-4952-3702
J Bornacelli https://orcid.org/0000-0001-6500-9485
C Torres-Torres https://orcid.org/0000-0001-9255-2416

References
Afandi A, Howkins A, Boyd I W and Jackman R B 2018 Nanodiamonds for device applications: an investigation of the properties of boron-
doped detonation nanodiamonds Sci. Rep. 8 3270 1–10
Alzate-Carvajal N, Basiuk E V, Meza-Laguna V, Puente-Lee I, Farías M H, Bogdanchikova N and Basiuk V A 2016 Solvent-free one-step
covalent functionalization of graphene oxide and nanodiamond with amines RSC Adv. 6 113596–610
Alzate-Carvajal N, Basiuk E V, Meza-Laguna V, Farías M H, Pérez-Rey L A, Abarca-Morales E, GarcíaRamírez V A, Basiuk V A and
Basiuk E V 2018 One-step nondestructive functionalization of graphene oxide paper with amines RSC Adv. 8 15253–65
Amselem S, Gabizon A and Barenho Y 1990 Optimization and upscaling of doxorubicin-containing liposomes for clinical use J. Pharm. Sci.
79 1045–52
Astuti Y, Poolton N R J, Butenko Y V and Šillern L 2014 Evaporation and alignment of 1-undecene functionalised nanodiamonds J of
Luminescence 156 41–8
Bamburowicz-Klimkowska M, Poplawska M and Grudzinski I P 2019 Nanocomposites as biomolecules delivery agents in nanomedicine
J. Nanobiotechnol. 17 48
Basiuk E V, Basiuk V A, Meza-Laguna V, Contreras-Torres F F, Martinez M, Rojas-Aguilar A, Salerno M, Zavala G, Falqui A and Brescia R
2012 Solvent free covalent functionalization of multiwalled carbon nanotubes and nanodiamond with diamines: looking for cross-
linking nanotubes and nanodiamond with diamines: looking for cross-linking effect Appl. Surf. Sci. 259 465–76
Basiuk E V, Santamaria-Bonfil A, Meza-Laguna A V, Gromovoy T Y, Alvarez-Zauco E, Contreras-Torres F F, Rizo J, Zavala G and
Basiuk V A 2013 Solvent-free covalent functionalization of nanodiamonds with amines Appl. Surf. Sci. 275 324–34
Barnard A 2009 Shape-dependent confinement of the nanodiamond band gap Crystal Growth & Design 9 4860–3
Bondar´ V S and Puzyr´ A P 2004 Nanodiamonds for biological investigations Phys. Solid State 46 716–9
Bradac C, Gao W, Forneris J, Trusheim M E and Aharonovich I 2019 Quantum nanophotonics with group IV defects in diamond Nat.
Commun. 10 5625
Bray K, Rodolfo Previdi R, Gibson B C, Shimoni O and Aharonovich I 2015 Enhanced photoluminescence from single nitrogen-vacancy
defects in nanodiamonds coated with phenol-ionic complexes Nanoscale 7 4869–74
Chung P-H, Perevedentseva E and Cheng C-L 2007 The particle size-dependent photoluminescence of nanodiamonds Surf. Sci. 601
3866–70
Dolenko T A, Burikov S A, Rosenholm J M, Shenderova O A and Vlasov I I 2012 Diamond-water coupling effects in raman and
photoluminescence spectra of nanodiamond colloidal suspensions J. Phys. Chem. C 116 24314–9
Douda J, Miranda Calderón L G, Kryshtab T, Arias Cerón J S and Kryvko A 2018 Synthesis and characterization of II–VI (CdSe) quantum
dot encapsulated liposomes J. Mater. Sci.: Mater. Electron. 29 15570–8

11
Nano Express 1 (2020) 030009 J Douda et al

Douda J, González Vargas C R, Vega- Macotela L G and Vallejo Cardona A A 2019a Modifications of the Optical Properties of Quantum
Dots on Liposome Encapsulation for Applications in Theranostic Liposomes Appl Nanosci 9 925–35
Douda J, González Vargas C R, Basiuk E V, Diaz Cano A I, Fuentes Garcia J A and Hernandez Contreras X A 2019b Optical properties of
amine-functionalized graphene oxide Applied Nanoscience 9 557–78
Drummond N D, Williamson A J, Needs R J and Galli G 2005 Electron emission from diamondoids: a diffusion quantum Monte Carlo study
Phys. Rev. Lett. 95 096801
Du D, Song H, Nie Y, Sun X, Chen X and Ouyang J 2015 Photoluminescence of graphene oxide in visible range arising from excimer
formation J. Phys. Chem. C 119 20085–90
Fayos J 1999 Possible 3D carbon structures as progressive intermediates in graphite to diamond phase transition J Sol St Chem. 148
199278–85
Fang L, Ohfuji H and Irifune T 2013 A novel technique for the synthesis of nanodiamond powder J. Nanomater. 2013 201845 4pages
Fokin A A and Schreiner P R 2009 Gap tuning in nanodiamonds: first principle computational studies Mol. Phys. 107 823–30
Giulia G 2010 Structure, stability and electronic properties of nanodiamonds ed L Colombo and A Fasolino Computer-Based Modeling of
Novel Carbon Systems and Their Properties (Netherlands: Springer) 37–56
Guillou C L, Brunet F, Irifune T, Ohfuji H and Rouzaud J N 2007 Nanodiamond nucleation below 2273 K at 15 GPa from carbons with
different structural organizations Carbon 45 636–48
Hasanzadeh A, Radmanesh F, Kiani J, Bayandori M, Fatahi Y, Aref A R and Karimi M 2019 Photoluminescent functionalized carbon dots for
CRISPR delivery: synthesis, optimization and cellular investigation Nanotechnology 30 135101
Hemelaar S R, Nagl A, Bigot F, Rodríguez-García M M, De Vries M P, Chipaux M and Schirhagl R 2017 The interaction of fluorescent
nanodiamond probes with cellular media Mikrochim. Acta 184 1001–9
Jia J et al 2019 Novel nanomedicine with a chemical-exchange saturation transfer effect for breast cancer treatment in vivo J. Nanobiotechnol.
17 1–14
Kompan M E, Terukov E I, Gordeev S K, Zhukov S G and Nikolayev Y A 1997 Photoluminescence spectra of ultradisperse diamond Phys Sol
State 39 1928–9
Kovalenko A, Petrakova V, Ashcheulov P, Zalis S, Nesladek M, Kraus I and Kratochvilllova I 2012 Parameters affecting the luminescence of
nanodiamond particles: quantum chemical calculations Phys Stat Sol A 209 1769–73
Kryshtab T G et al 2012 The effect of bio-conjugation on aging of the photoluminescence in CdSeTe–ZnS core–shell quantum dots
Superlattices Microstruct. 51 353–62
Kumar P, Meena R, Paulraj R, Chanchal A, Verma A K and Bohidar H B 2012 Fluorescence behavior of nonfunctionalized carbon
nanoparticles and them in vitro applications in imaging and cytotoxic analysis of cancer cells Colloids Surf. B 91 34–40
Kumar A, Lin A P, Xue A, Hao B, Yap Y K and Sankaran M R 2013 Formation of nanodiamonds at near-ambient conditions via microplasma
dissociation of ethanol vapour Nat. Commun. 4 2618 (1–9)
Lake M P and Bouchard L S 2017 Targeted nanodiamonds for identification of subcellular protein assemblies in mammalian cells PLoS One
12 0179295
Lakowicz J R 1999 Principles of Fluorescence Spectroscopy 2nd edn (NY: Kluwer Academic/Plenum Publishers) (https://doi.org/10.1007/
978-0-387-46312-4)
Laube C, Oeckinghaus T, Lehnert J, Griebel J, Knolle W, Denisenko A, Kahnt A, Meijer J, Wrachtrupc J and Abel B 2019 Controlling the
fluorescence properties of nitrogen vacancy centers in nanodiamonds Nanoscale 11 1770–83
Liu H, Hu L, Watanabe K, Hu X, Dierre B, Kim B, Sekiguchi T and Fang X 2013 Cathodoluminescence modulation of ZnS nanostructures by
morphology, doping, and temperature Adv Funct Matter 23 3701–9
Loncar M and Faraon A 2013 Quantum photonic networks in fluorescent nanodiamonds MRS Bull. 38 144–8
Mochalin V N and Gogotsi Y 2009 Wet chemistry route to hydrophobic blue fluorescent nanodiamond J. Am. Chem. Soc. 131 4594–5
Mochalin V N, Shenderova O, Ho D and Gogotsi Y 2012 The properties and applications of nanodiamonds Nat. Nanotechnology 7 1–13
Mona J, Tu J-S, Kang T-Y, Tsai C-Y, Perevedentseva E and Cheng C-L 2012 Surface modification of nanodiamond: photoluminescence and
Raman studies Diam. Relat. Mater. 24 134–8
Morales-Zavala F et al 2018 Functionalization of stable fluorescent nanodiamonds towards reliable detection of biomarkers for Alzheimer
disease J. Nanobiotechnol. 16 60
Osipov V Y, Treussart F, Zargaleh S A, Takai K, Shakhov F M, Hogan B T and Baldycheva A 2020 Photoluminescence from NV− centres in 5
nm detonation nanodiamonds: identification and high sensitivity to magnetic field Nanoscale Res. Lett. (2019) 14 279
Patra J K et al 2018 Nano based drug delivery systems: recent developments and future prospects J. Nanobiotechnol. 16 71
Perevedentseva E, Melnik N, Tsai C-Y, Lin Y-C, Kazarian M and Cheng C-L 2011 Effect of surface adsorbed proteins on the
photoluminescence of nanodiamond J. Appl. Phys. 109 034704
Pham X-M, Halm E, Kim T H, Kim H-M, Lee S H, Lee Y-S, Jeong D H and Jun B-U 2017 Adenosine-triphosphate-encapsulated liposomes
with plasmonic nanoparticles for surface enhanced Raman scattering-based immunoassays Sensors 17 1480
Pichot V, Muller O, Seve A, Yvon A, Merlat L and Spitzer D 2017 Optical properties of functionalized nanodiamonds Sci. Rep. 7 14086
Polupan G, Torchynska T V, Jaramillo Gomez J A and Douda J 2017 Aspects of emission variation in CdSeTe/ZnS quantum dots conjugated
to antibodies J. Mater. Sci.: Mater. Electron. 28 7047–52
Rourke J P, Pandey P A, Moore J J, Bates M, Kinloch I A, Young R J, Neil R and Wilson N R 2011 The real graphene oxide revealed: stripping
the oxidative debris from the graphene‐ like sheets Angew. Chem. 50 3173–7
Seleci M, Seleci D A, Scheper T and Stahl F 2017 Theranostic liposome-nanoparticle hybrids for drug delivery and bioimaging Int. J. Mol. Sci.
18 1415
Stehlik S, Ondik L, Berhane A M, Aharonovich I, Girard H A, Arnault J-C and Rezek B 2016 Photoluminescence of nanodiamonds
influenced by charge transfer from silicon and metal substrates Diamond Relat. Mater. 63 91–6
Su L-X, Lou Q, Jiao Z and Shan C-X 2016 Plant cell imaging based on nanodiamonds with excitation-dependent fluorescence Nanoscale Res.
Lett. 11 425
Tinwala H and Wairkar S 2019 Production, surface modification and biomedical applications of nanodiamonds: a sparkling tool for
theranostics Mater Sci Eng C Mater Biol Appl. 97 913–31
Torres Sangiao E, Holban A M and Cartelle Gestal M 2019 Applications of nanodiamonds in the detection and therapy of infectious diseases
(review) Materials 12 1639
Treussart F and Vlasov I I 2017 Photoluminescence of color centers in nanodiamonds ed J C Arnault Nanodiamonds, Advanced Material
Analysis, Properties and Applications (Amsterdam: Elsevier) pp 155–81
Turcheniuk K and Mochalin V N 2017 Biomedical applications of nanodiamond (review) Nanotechnology 28 252001

12
Nano Express 1 (2020) 030009 J Douda et al

Wojdak M, Klik M, Forcales M, Gusev O B, Gregorkiewicz T, Pacifici Franzò D G, Priolo F and Iacona F 2004 Sensitization of Er
luminescence by Si nanoclusters Phys. Rev. B 69 23
Wu M, Mukherjee P, Lamont N D and Waldeck D H 2010 Electron transfer and fluorescence quenching of nanoparticle assemblies J. Phys.
Chem. C 114 5751–9
Xiao J, Liu P, Li L and Yang G 2015 Fluorescence origin of nanodiamonds J. Phys. Chem. C 119 2239–48
Zhang Y, Rhee K Y, Hui D and Park S J 2018 A critical review of nanodiamond based nanocomposites: synthesis, properties and applications
Compos Part B-Eng 143 19–27

13