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DOI: 10.1039/C9FD00111E

White graphene quantum dots as electrochemical sensing platform for ferritin

Mayank Garg1, 2, Reetu Rani1, 2, Amit L. Sharma1, 2, Suman Singh1, 2*

1CSIR- Central Scientific Instruments Organisation, Sector 30-C, Chandigarh-160030, India
2Academy of Scientific and Innovative Research (AcSIR), Ghaziabad-201002, India
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*Corresponding author: ssingh@csio.res.in

Abstract:

The use of hexagonal boron nitride quantum dots (hBN QDs) as an electrochemical sensor for
ferritin is reported for the first time in this manuscript. These QDs were synthesized using simple
method of liquid exfoliation. The synthesized material was characterized using analytical
techniques such as UV-Visible, Fourier Transform Infrared (FTIR) and Raman spectroscopy, X-
Ray Diffraction (XRD), and High-Resolution Transmission Electron Microscopy (HR-TEM)
wherein the different aspects of the QDs were studied. These QDs were explored for their plausible
application as a platform for the electrochemical detection of ferritin. For this, the electrochemical
impedance spectroscopy is used as sensing technique and disposable hBN
QDs functionalized screen printed electrodes were used as sensing platform. The developed
immunosensor had a dynamic linear range from 10-2000 ng.mL-1 of ferritin concentration with a
limit of detection of 1.306 ng.mL-1. The immunosensor was highly selective, not deviated in the
presence of interfering agents and also highly reproducible.

Keywords
Hexagonal boron nitride, white graphene, quantum dots, ferritin, electrochemical immunosensor
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1. Introduction
2-dimesnional layered materials have been long explored and developed for various applications
such as electronics, optical, opto-electronic, and sensors 1. With the help of powerful computing,
various new 2-dimenisonal materials were discovered 2. Transition metal dichalcogenides (TMDs)
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such as WS2, MoS2, WSe2 etc., hexagonal boron nitride (hBN) are examples of some the 2-D
layered materials other than graphene 3. Till now, majorly TMDs and graphene based devices have
been developed and have been the center of focus for the researchers of this field which can be
adjudged by the ever growing publications from this area4, 5. Hexagonal boron nitride (hBN) is one
such 2-D layered material which has not yet received the global attention. It is one of the crystalline
form of boron nitride which is stable at room temperature and is popularly regarded as the white
graphene because of the its structural resemblance with the graphene 6,7, 8. Although similar to
graphene, hBN is very unique. It is chemically inert, thermally stable and has high mechanical
strength and thus finds its use in many electronics and opto-electronic applications 9. Because of
these properties, hBN is a suitable candidate to be used alone as well as in association with other
2-D materials 10.
Use of hBN in electrochemistry is a new field and very few reports exist. It has been used for
the electrochemical detection of dopamine 11, 12, vitamin C 13, organophosphorus pesticides 14 and
ascorbic acid 15. The application of hBN quantum dots as an electrochemical biosensing platform
for disease biomarkers is rare with the detection of cardiac troponin-I being the sole report 16. With
the aim of exploring the use of hBN QDs as in immunosensing application, the current study
focusses to employ this material for the detection of ferritin as a model biomarker of clinical
relevance. Ferritin is an important iron storing protein present in almost all living organisms. Its
role is to maintain the levels of iron in the human body 17. Its deficiency and elevated levels are
known to cause many serious diseases. The normal levels for ferritin in males and females should
be between 15-200 ng.mL-1 in males and 15-150 ng.mL-1 respectively as prescribed by World
Health Organization. Its deficiency and elevated levels are known to cause many serious diseases.
The conventional methods of detection such as ELISA based or radioimmunoassay based methods
have various drawbacks such as use of radiolabels, high cost, laborious experimentation and use
of sophisticated instruments. Therefore, the need is to develop a highly sensitive and selective
method for the detection of ferritin which is easy to fabricate and easy to operate.
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Nowadays, using screen printed electrodes (SPEs) as electrochemical platform has become a
trend but for bio-immunosensing and other biological applications, their surface should have some
functionalities to facilitate biological interactions. For this, various materials are used and since
this work reports application of hBN QDs, the surface of SPE is modified with this material. These
hBN QDs functionalized screen printed electrodes (SPE) were used for ferritin detection using the
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electrochemical impedance spectroscopy (EIS). Anti-ferritin antibodies on the hBN QDs modified
SPE ensured selectivity towards ferritin antigen. The immunosensor was found to be highly
sensitive, selective and reproducible for estimation of ferritin.

2. Material and Methods

2.1. Materials

Boron nitride powder (~1 μm, 98 %) purchased from Sigma-Aldrich (India) was used to synthesize
hexagonal boron nitride quantum dots. Polyclonal anti-ferritin human antibodies, ferritin antigen,
hemoglobin, phosphate buffered saline tablets were purchased from Sigma Aldrich (India).
Potassium ferrocyanide [K4Fe(CN)6], potassium ferricyanide [K3Fe(CN)6], Streptavidin and
Bovine Serum Albumin (BSA) were purchased from HiMedia, Mumbai (India). Screen printed
carbon electrodes (SPE) from Zensor (Taiwan) were used having surface area of 0.071 cm2. AR
Grade DMF was procured from Loba Chemie (India). All the solutions were made using Milli-Q
water obtained from Millipore Water Purification System [Model Integral System].

2.2. Instrumentation

UV-Vis spectrophotometer (Hitachi, U 3900 H, Japan) was used to analyze the optical properties
of the hexagonal boron nitride quantum dots in the range of 275-600 nm. SpectraMax i3x
(Molecular Devices, USA) was used to study the fluorescence properties of the hBN QDs. FT-IR
spectrometer (Perkin Elmer Spectrum II, USA) was used to obtain the FTIR spectrum of the
synthesized material in the range of 4000-400 cm-1. Bruker D8 Advance (Germany) was employed
to study the diffraction pattern of boron nitride powder and hBN QDs in 5 to 70o 2θ range. Raman
analyzer from Renishaw, UK) equipped with a He-Ne laser having an excitation wavelength of
785 nm was used to acquire Raman measurements. High Resolution Transmission Electron
Microscopic (HR-TEM) image was obtained using FEI, Model TECNAI G2F-20, USA. Prior to
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recording the data, baseline corrections were made. Electrochemical analyzer (CH Instruments,
CHI660C, USA) was used for the electrochemical studies.

2.3. Synthesis of hexagonal boron nitride quantum dots (hBN QDs)

To synthesize hBN QDs, protocol developed by Lei et al. was used with some modifications 18.
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Briefly, 500 mg of boron nitride powder was dispersed in 50 mL DMF. The suspension was bath
sonicated for 4 hours followed by 1 hour of probe sonication. After sonication, the top half of the
dispersion was taken in a separate flask wherein it was subjected to stirring at 140 oC for 24 hours.
This suspension was centrifuged at 8,000 rpm for 20 minutes to separate the supernatant from the
pellet having unexfoliated boron nitride powder. The faint yellow colored supernatant containing
the hBN QDs was filtered. The solvent was changed from DMF to water by evaporation of DMF
followed by addition of water. Throughout the manuscript, the QDs thus synthesized are referred
to as hBN QDs. The QDs thus obtained were fully characterized for their morphology,
crystallinity, size, etc. Afterwards these were explored as an electrochemical sensor of ferritin.

1.4. Electrochemical detection of ferritin

Ferritin was detected electrochemically using screen printed electrodes modified with hBN QDs
and referred to as hBN QDs/SPE. Electrochemical Impedance Spectroscopy (EIS) was used as a
technique for the electrochemical characterization as well as sensing applications. Phosphate
buffer containing 1.0 mM Fe(CN)63− /Fe(CN)64− was taken as redox marker. The bare screen
printed carbon electrode was modified with the synthesized hBN QDs by simple drop casting
method followed by air drying the electrode. The modified hBN QDs/SPE provides a platform for
the attachment of anti-ferritin antibodies on its surface and is termed as hBN QDs/SPE/FtAb. This
sequentially modified electrode was used for ferritin detection. Effect of different concentrations
of ferritin, dynamic linear range, pH, and reproducibility and selectivity studies also performed.
10 ng.mL-1 to 2000 ng.mL-1 as a dynamic linear range was studied for ferritin. 5.5 to 9.0 range at
intervals of 0.5 was considered as the pH range under study. Response from 5 identical electrodes
prepared in the same fashion were recorded to determine the reproducibility of the developed
immunosensor. Streptavidin, bovine serum albumin (BSA) and hemoglobin (Hb) using 2000
ng.mL-1 concentration were used for the selectivity studies.
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3. Results and Discussion

Once the hBN QDs were synthesized, these were characterized and analyzed using analytical
techniques such as UV-Visible, fluorescence, FTIR, Raman spectroscopy, X-ray diffraction and
transmission electron microscopy.
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3.1. Spectroscopic Characterization:

The UV-Vis absorption spectrum is shown in the Figure 1 (a) below. The spectrum shows a hump
around 280-320 nm which is a characteristic peak for the hBN QDs and matches well with the
previous report18, 19. This absorption can be attributed to the π electron transitions occurring due to
the introduction of defects caused by oxygen in the nitrogen and boron system in the hBN QDs 20.
The fluorescence properties of the synthesized hBN QDs were also studied as is shown in the
figure 1 (b). The hBN QDs were subjected to an incremental excitation wavelength from 300-400
nm and its emission spectra was recorded. It was observed that with increase in excitation
wavelength from 300 nm to 360 nm, continuous increase in the emission intensity of the hBN QDs
was observed. But from 370 nm to 400 nm excitation wavelength, the emission intensity decreased.
This matches very well with the previous report 18. Maximum fluorescence emission peak for the
hBN QDs was found to be around 442 nm.
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Figure 1: (a) UV- Vis spectrum of hBN QDs (b) Fluorescence spectra of hBN QDs (c) FTIR
spectra (d) Raman spectra (e) XRD spectra of bulk hBN and hBN QDs (f) TEM image of
hBN QDs
Figure 1 (c) shows the FTIR spectrum of both the bulk BN powder and hBN QDs. The FTIR
spectrum shows the presence of peaks around 1358 and 768 cm-1 in both the bulk BN powder and
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hBN QDs which is attributed to the B-N vibrations 18. Additionally, new peaks in the region of
750-500, 1000-1270, 1500-1700 cm-1 are observed in the hBN QDs which can be due to O-B-O
vibrations, N-B-O vibrations, and C-(BN) vibrations respectively 19, 21. Also, the presence of amine
groups is evident from the peaks around 2750-3000 cm-1. In Raman study, the bulk BN powder
showed a prominent E2g phonon mode around 1340-1345 cm-1 18 (figure 1 (d)). However, the hBN
QDs exhibited a much weaker E2g phonon mode as compared to the bulk material indicating the
formation of monolayer BN22, 23.

3.2. XRD and Morphological study using HRTEM:

The XRD pattern in the Figure 1 (e) shows the characteristic peaks of the bulk BN powder. The
main peak is obtained at around 27o which is (002) face of the BN powder. Other peaks are
obtained at around 42, 45 and 55o which correspond to (100), (101) and (004) faces of the BN
respectively 18. Upon exfoliation of the BN powder to the hBN QDs, the intensity of the main face
along with other peaks decreases sharply indicating the formation of a highly exfoliated material21,
24. The high resolution transmission microscopic image shows formation of hBN QDs in the size
range of 3-6 nm (figure 1 (f)). The d spacing for the hBN QDs was found to be 0.21 nm which
corresponds to BN crystal having (100) face as reported by previous report 18.

3.3. Electrochemical Characterization:

Electrochemical impedance spectroscopy (EIS) was employed for the electrochemical

characterization of the serially modified electrodes as well as for the estimation of ferritin in the
later sections. EIS data is recorded in the form of Nyquist plot or Bode plot. Bode plots show the
frequency response of a system. There are two Bode plots one for gain (or magnitude) and one for
phase. The Nyquist plot combines gain and phase into one plot in the complex plane. As compared
to the Bode plot, the Nyquist plot is more complex, but is more popular in electrochemistry due to
its high sensitivity towards minor changes and information on some parameters can directly be
deduced directly from the plot. In an electron transfer limited process, Nyquist Plot is a semi-circle,
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whereas in reactions, which are both electron transfer limited and diffusion limited, the semicircle
is followed by a linear portion which is referred as Warburg impedance. The diameter of semi-
circle gives direct information about the extent of resistance. Higher the resistance to the electron
transfer, bigger will be the diameter of the semi-circle. Charge transfer resistance (Rct) is calculated
from the Nyquist plot by fitting into Randles equivalent circuit. Usually, Rct is expressed as a sum
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of solution resistance (Rs) and polarization resistance (Rp). The Fe3+/2+ as redox marker prepared
in phosphate buffer solution was chosen as the electrolyte for the studies.
Figure 2 (a) shows impedance spectra of sequentially modified electrodes. The bare SPE
had an Rct value of 1108.1 Ω.

Figure 2: (a) Impedance spectra of sequentially modified electrodes (b) Effect of pH

on impedance behavior in presence of ferritin (c) Effect of ferritin concentration on of hBN
QDs/SPE/FtAb electrodes (d) Linearity curve
Upon modification of SPE working surface by the hBN QDs, the current in the system increased
which is reflected as a decrease in the semi-circle diameter in the EIS graph (Rct= 1050.8 Ω). A
similar increase in the current and reduction in impedance is also demonstrated in work done by
Yola et al 16. This increase in the current can be due to the electrostatic interactions taking place
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between the surface functional groups of the hBN QDs and the target molecules 25. It has been
shown in the past work also that use of 2D- hBN nanosheets resulted in an increase in the current
which can also be a contributing factor for the increase in current shown by hBN QDs 11, in present
study. This hBN QDs/SPE was further modified by attaching anti-ferritin antibodies by drop-
casting method. This hBN QDs/SPE/FtAb modified electrode showed a decrease in the value of the
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current which is indicated by the increase in the resistance value from the larger diameter of the
semi-circle (Rct= 1299.9 Ω). This is a well-known fact that antibodies being biomolecules are
insulating in nature and hence leads to increased resistance on the electrode surface 26. Upon the
addition of ferritin antigen, antigen-antibody interactions take place, which adds to the already
insulating antibodies present on the electrode surface leading to an increased resistance (Rct=
1576.5 Ω) 27.

3.4. hBN QDs/SPE as immunosensor for detection of ferritin:

Before estimation of the ferritin using the developed immunosensor, sensors robustness towards
pH variation was evaluated. pH was varied from 5.5-9.0 at an interval of 0.5. This was done to
check the sensors performance in the slightly acidic, neutral and basic pH conditions. It was
observed that the Rct value of the sensor decreased from pH 5.5 to pH 7.5 and then started to
increase from pH 8.0 to pH 9.0 (figure 2 (b)). Since the acidic or basic conditions tend to damage
the immobilized proteins, a near neutral pH condition is always favorable for the maximum
stability of the protein structures and hence, pH 7.5 was chosen as the optimum value and
considered for experiments to follow.

Followed by variation of pH conditions, the effect of sensor was checked for different
ferritin concentrations (10-2000 ng.mL-1), figure 2 (c-d). It was observed that on increasing the
concentration of the antigen on the surface, the Rct value increased gradually. This is because of
the formation of the insulating antigen-antibody complex, on the electrode surface leading to
resistance for the flow of Fe3+/Fe2+ ions. The limit of the detection was calculated to be 1.306
ng.mL-1 using the formula: LOD = 3.3 x Standard Deviation/slope.
No significant deviation of the sensors response towards presence of the interfering agents
(hemoglobin, BSA and avidin) was observed indicating a very robust immunosensor capable of
selectively detecting ferritin (figure 3 a-b). The reproducibility of the developed immunosensor
was evaluated by the checking the response from 5 identically prepared electrodes (figure 3 c-d).
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Almost identical EIS response was obtained from all the electrodes with a percentage coefficient
(% CV) of variation of 0.641% in the Rct values.
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Figure 3: (a, c) Nyquist Plot showing effect of interferents and reproducibility respectively
(b, d) column graph showing the variation of Rct value for the interferents and
reproducibility respectively

4. Conclusion:

The use of hBN QDs popularly referred to as “white graphene” as an immunosensor is

demonstrated in the current work. hBN QDs have been explored relatively less as compared to the
other 2-D layered materials as electrochemical platforms for the detection of biomarkers. The hBN
QDs were synthesized using simple synthesis steps. Immobilization of the anti-ferritin antibodies
to the surface of the electrode modified by the hBN QDs provided an immunosensor capable of
sensing ferritin antigen. The sensor was found to give a linear response, was selective and highly
reproducible.
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Acknowledgement

The authors acknowledge the support of Director, CSIR-CSIO for his constant encouragement.
Mayank Garg and Reetu Rani acknowledges SRF-GATE fellowship and SRF fellowship
respectively from Council of Scientific and Industrial Research (CSIR-HRDG), New Delhi.
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Conflict of interest: Authors declare no conflict of interest

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