A special o-dialdehyde fluorescent probe simultaneously sensing Hcy, GSH and its application in living cells and zebrafish imaging

Article abstract of DOI:10.1016/j.cclet.2021.05.016

The development of fluorescent probes enabling to distinguish Cys, Hcy and GSH has always been a considerable challenge, in particular the distinction of Hcy and other two biothiols, because Hcy has a very similar structure with Cys and a relatively lower concentration in living organisms. In this work, a special o-dialdehyde fluorescent probe, quinoline-2,3-dicarboxaldehyde (QDA), has been synthesized and demonstrated superior performance in differentiating detection of Hcy and GSH, which is different from the previous reported o-dialdehyde probes specifically detecting GSH. Furthermore, the probe can selectively distinguish Hcy and GSH from different signal channels in living cells and zebrafish, meaning it has great potential in biological applications. This finding will provide a novel idea for the design of fluorescent probes to distinguish biothiols.

Full text of DOI:10.1016/j.cclet.2021.05.016

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Contents lists available at ScienceDirect
Chinese Chemical Letters
journal homepage: www.elsevier.com/locate/cclet
Communication
A special o-dialdehyde fluorescent probe simultaneously sensing Hcy,
GSH and its application in living cells and zebrafish imaging
a
a,b
c
d
a
b,c,∗
Yongbin Zhang , Yu Zhang , Yongkang Yue , Jianbin Chao , Fangjun Huo , Caixia Yin
a
Shanxi Key Laboratory of Functional Molecules, Research Institute of Applied Chemistry, Shanxi University, Taiyuan 030006, China
b
School of Chemistry and Chemical Engineering, Shanxi University, Taiyuan 030006, China
c
Key Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Institute of Molecular Science, Shanxi University, Taiyuan 030006,
China
d
Scientific Instrument Center, Shanxi University, Taiyuan 030006, China
a r t i c l e i n f o
a b s t r a c t
Article history:
The development of fluorescent probes enabling to distinguish Cys, Hcy and GSH has always been a con-
siderable challenge, in particular the distinction of Hcy and other two biothiols, because Hcy has a very
similar structure with Cys-and a relatively lower concentration in living organisms. In this work, a special
o-dialdehyde fluorescent probe, quinoline-2,3-dicarboxaldehyde (QDA), has been synthesized and demon-
strated superior performance in differentiating detection of Hcy and GSH, which is different from the
previous reported o-dialdehyde probes specifically detecting GSH. Furthermore, the probe can selectively
distinguish Hcy and GSH from different signal channels in living cells and zebrafish, meaning it has great
potential in biological applications. This finding will provide a novel idea for the design of fluorescent
probes to distinguish biothiols.
Received 16 February 2021
Revised 8 May 2021
Accepted 13 May 2021
Available online xxx
Keywords:
o-Dialdehyde
Distinguish
Hcy
GSH
Bioimaging
© 2021 Published by Elsevier B.V. on behalf of Chinese Chemical Society and Institute of Materia
Medica, Chinese Academy of Medical Sciences.
Nowadays, with the in-depth study of life science, people have
gradually realized the importance of many active small molecules
in life processes, but how to accurately monitor the concentra-
tion and metabolic process of these active small molecules has al-
ways been a challenging scientific problem. As an important part
of active small molecules, biothiols such as glutathione (GSH), cys-
teine (Cys) and homocysteine (Hcy) play a crucial role in vari-
ous physiological and pathological processes [1–3]. GSH, which is
the most abundant thiol in cells, plays a major anti-oxidation role
in maintaining intracellular redox activities and regulating genes
in cellular functions, and its abnormal concentration can cause
atherosclerosis, lung damage, Alzheimer’s disease and cancer [4–8].
As a precursor of GSH synthesis, Cys-participates in protein syn-
thesis, detoxification and metabolism [9,10], and its abnormal level
can give rise to hematopoietic dysfunction, neurotoxicity, lethargy
and AIDS [11–15]. Hcy is an intermediate product in methionine
metabolism to produce Cys, and it can directly or indirectly accel-
erate thrombosis so that high level of Hcy can lead to cardiovas-
cular disease, osteoporosis, inflammatory bowel disease, pregnancy
complications [16–18]. Therefore, each biothiol can be regarded as
a marker of disease, and their differential detection and metabolic
process monitoring are of great value for the diagnosis and treat-
ment of related diseases.
Compared with the traditional analytical methods, fluorescent
probes have been proved to be a very effective tool for detecting
and visualizing small biological molecules in cells due to their ad-
vantages of high spatial and temporal resolution, non-invasiveness,
high sensitivity and wide dynamic response range [19–22]. So far,
many multi-signal fluorescent probes have been reported in dis-
criminatively detecting different biothiols, and applied to multi-
color imaging of cells or living tissues by means of confocal flu-
orescence imaging technology [23–34]. However, due to the simi-
lar structures and properties of different biothiols, especially only
a single methylene unit difference in the structure of Hcy and Cys,
and the concentration of Cys-and Hcy far lower than the level of
GSH in biological body [35–37], it is greatly difficult to distinguish
Hcy and Cys, or Hcy/Cys-and GSH, resulting in the reported fluo-
rescent probes possessing the ability to simultaneously distinguish
GSH, Hcy and Cys-were extremely limited [38–40]. Therefore, the
development of fluorescent probes that can distinguish GSH, Hcy
and Cys-is still a hot topic for researchers in this field.
As early as 1989, the Neuschochocho-Tetri group had reported
that o-phthaldialdehyde (OPA) reacted with GSH to generate a
highly fluorescent cyclized adduct, and established a HPLC sepa-
ration and fluorometric detection method for GSH [41]. Later, the
∗
Corresponding author.
E-mail address: yincx@sxu.edu.cn (C. Yin).
https://doi.org/10.1016/j.cclet.2021.05.016
1001-8417/© 2021 Published by Elsevier B.V. on behalf of Chinese Chemical Society and Institute of Materia Medica, Chinese Academy of Medical Sciences.
Please cite this article as: Y. Zhang, Y. Zhang, Y. Yue et al., A special o-dialdehyde fluorescent probe simultaneously sensing Hcy, GSH
and its application in living cells and zebrafish imaging, Chinese Chemical Letters, https://doi.org/10.1016/j.cclet.2021.05.016

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O
1) n-BuLi, THF
CHO
Cl
CHO
1
) NaI
O
2) DMF
2
) TsOH,HO OH
3) HCl, THF
N
N
I
N
CHO
1
QDA
Scheme 1. The synthetic route of QDA.
Fig. 1. UV–vis (a) and fluorescent (b) spectra of QDA (30 μmol/L) upon the addition of GSH, Hcy and Cys (10 equiv.) in DMSO-PBS (1/1, v/v, pH 7.4). λex = 470 nm, slit:
nm/10 nm. Inset: visual (a) and fluorescent (b) color change of QDA after adding GSH, Hcy and Cys-under ambient light (a) and 365 nm UV lamp light (b).
5
Orwar group developed a 2,3-naphthalenedicarboxaldehyde- based
fluorescence detection method for GSH, and realized quantitative
detection of GSH in single cells [42]. After decades of development,
many GSH detection methods based on this strategy and their ap-
plications in food and biological samples have been reported. In
upon addition of GSH (ꢀ = 0.033), while the addition of Hcy could
produce a strong green fluorescence at 530 nm (ꢀ = 0.086), and
no fluorescence was observed with the treatment of Cys, which
showed that QDA could distinguish GSH and Hcy by means of flu-
orescence method. Here we explained the reason why 470 nm was
selected as the excitation wavelength in the fluorescence spectrum
of QDA to Hcy, because it could be seen from the excitation spec-
trum that 470 nm was the best excitation wavelength (Fig. S2 in
Supporting information). To see how the three biothiols compete
with one another in the reaction with QDA, the fluorescent spec-
trum of QDA upon addition of a mixture of the physiological con-
centration of three biothiols was measured, and the result showed
that a new fluorescence emission peak at 572 nm appeared, which
was actually a superposition of the fluorescence emission peaks at
530 nm and 586 nm (Fig. S3 in Supporting information). This indi-
cated that both Hcy and GSH in the mixed system could respond
to QDA simultaneously.
2
018, our group, in cooperation with the Yoon group, reported the
Naphthalene dicarboxaldehyde-based fluorescence probes for GSH
and their applications in the diagnosis and mortality prediction of
patients with sepsis [43]. In this work, we designed and synthe-
sized a fluorescent probe based on quinoline-2,3-dicarboxaldehyde
(
QDA). Different from the previously reported o-dialdehyde probes,
QDA can not only generate cyclized adduct emitting orange fluo-
rescence at 586 nm with GSH, but also produce another cyclized
adduct emitting green fluorescence at 530 nm with Hcy. Therefore,
QDA can realize the selective differentiation of GSH and Hcy in liv-
ing cells at different signal channels, which has important guiding
significance for the early diagnosis of diseases related to different
biothiols.
To further explore the sensitivity of QDA to GSH and Hcy, flu-
orescent titration experiments were studied in detail. It could be
seen from Fig. S4 (Supporting information) that the fluorescent in-
tensity at 586 nm gradually enhanced as the concentration of GSH
increased, and there was a good linear relationship (R2 = 0.9979)
when the concentration of GSH was between 0 and 200 μmol/L,
and the detection limit was measured to be 0.25 μmol/L. For Hcy,
in the same way, a good linear relationship (R2 = 0.9976) was also
obtained between the fluorescence intensity at 530 nm and the
concentration of Hcy (0–200 μmol/L) with the detection limit of
0.35 μmol/L (Fig. S5 in Supporting information). The above results
displayed that QDA could specifically and quantitatively detected
GSH and Hcy.
The synthetic route of QDA was depicted in Scheme 1. QDA was
prepared following the methods in the literature [44] and its struc-
ture was confirmed by NMR and MS analysis (Fig. S1 in Supporting
information).
At the beginning, we measured the spectroscopic responses of
QDA to different biothiols including GSH, Cys-and Hcy in DMSO-
PBS (1/1, v/v, pH 7.4). The solution of QDA was colorless and had a
moderate absorption in 290–320 nm. The addition of GSH caused
several strong absorptions in 294–351 nm and 470 nm, and the
color of the solution changed to light orange. Likewise, Hcy also
produced a strong absorption in 292 nm and a weak absorption
in 558 nm, but the addition of Cys-did not change the absorption
spectrum of QDA (Fig. 1a). These results indicated that QDA was
almost inert to Cys, and reacted with GSH and Hcy to generate
different species. Subsequently, the fluorescent responses of QDA
to different biothiols were carried out. As represented in Fig. 1b,
QDA itself had little fluorescence at excitation of 470 nm. There
was a unique orange fluorescent emission appearing at 586 nm
To gain the optimum detection conditions of QDA to GSH and
Hcy, time-dependent and pH-selective fluorescence experiments
were performed. Fig. S6a (Supporting information) showed that
the fluorescent signal at 586 nm reached the maximum within
8 min in the presence of GSH (10 equiv.), and the intensity was
basically stable for a long period of time. QDA reacted slightly
2

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Scheme 2. The response mechanism of QDA to GSH and Hcy.
Fig. 2. Confocal images of QDA responding to endogenous and exogenous GSH and Hcy in A549 cells. (A1-A3) A549 cells incubated with QDA (20 μmol/L) for 20 min.
B1-B3) A549 cells pretreated with NEM (1 mmol/L) for 30 min and then incubated with QDA (20 μmol/L) for 20 min. (C1–C3) A549 cells pretreated with NEM (1 mmol/L)
(
for 30 min, then incubated with GSH (20 μmol/L) for 30 min, and finally incubated with QDA (20 μmol/L) for 20 min. (D1-D3) A549 cells pretreated with NEM (1 mmol/L)
for 30 min, then incubated with Hcy (20 μmol/L) for 30 min, and finally incubated with QDA (20 μmol/L) for 20 min. Green channel: λem = 510–550 nm (λex = 458 nm);
red channel: λem = 600–630 nm (λex = 488 nm). Scale bar: 20 μm.
−
−
2− 2−
, CO3 ). As shown in Fig. S8 (Supporting informa-
slower with Hcy (10 equiv.) than GSH, and the fluorescent signal
at 530 nm was maximized within 30 min (Fig. S6b in Support-
ing information). Therefore, in the spectroscopic test experiments,
the response times of QDA to GSH and Hcy were set at 8 min
and 30 min, respectively. Furthermore, the fluorescent responses
of QDA to GSH and Hcy at different pH values (2.0–10.0) were car-
ried out (Fig. S7 in Supporting information). In the absence of GSH
or Hcy, QDA had basically no fluorescence, and the fluorescent in-
tensity of QDA was almost unchanged in the entire pH range. How-
ever, in the presence of GSH or Hcy, there was a significant fluores-
cent enhancement in the pH range of 6.0 to 10.0. In addition, the
mixture solution had the strongest fluorescent intensity around pH
I , Br , SO
4
tion), only GSH and Hcy could cause drastic fluorescent emission
(586 nm for GSH, 530 nm for Hcy), while other amino acids and
ions had almost no effect on the fluorescent spectrum of QDA. In
addition, the competitive experiments also displayed that other an-
alytes didn’t interfere with the detection of QDA to GSH and Hcy
(Fig. S9 in Supporting information), which proved that QDA had
high selectivity to GSH and Hcy and the potential to be applied in
complex biological systems.
The response mechanism of QDA to GSH and Hcy was as-
sumed as represented in Scheme 2. According to the reported re-
action mechanism of OPA and GSH [45], we speculated that QDA
ꢀ
ꢀ
7
.4 compared to other pH. The results indicated that QDA had the
could react with GSH or Hcy to form thiazino[3 ,2 :1,2]pyrrolo[3,4-
b]quinoline derivatives due to amino and sulfhydryl functional
group of GSH or Hcy possessing the reactivity with aldehyde, and
the supposed mechanism was further confirmed by 1H NMR and
MS analysis of adduct of QDA and GSH (or Hcy). As shown in Fig.
S10 (Supporting information), the protons of aldehyde groups of
QDA appeared at 10.67 and 10.26 ppm in 1H NMR spectrum. When
GSH or Hcy was added to the DMSO–d6 solution of QDA, the pro-
ton signals of aldehyde groups disappeared and new proton sig-
ability to detect GSH and Hcy under physiological environment.
In order to expand the application of QDA in biological systems,
it is necessary to verify the specific selection of QDA to GSH and
Hcy in a complex environment. We have researched the fluores-
cent response of QDA towards various biologically relevant species,
including amino acids (Ala, Glu, Asp, Leu, Ile, Lys, Gly, Gln, Tyr, His,
Trp, Thr, Phe, Asn, Met, Val, Pro, Ser, Arg) and some common ions
+ 2+ 2+ + 2+ 2+ 2+ 3− − − −
(
Na , Ca , Mg , K , Cu , Mn , Zn , PO4 , HSO3 , HS , Cl ,
3

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Fig. 3. Confocal images of QDA responding to endogenous and exogenous Hcy and GSH in zebrafish. (A-D) Zebrafish pretreated with QDA (20 μmol/L, 30 min). (E-H)
Zebrafish pretreated with NEM (200 μmol/L, 30 min) and then incubated with QDA (20 μmol/L, 30 min). (I-T) Zebrafish pretreated with NEM (200 μmol/L, 30 min),
and then respectively incubated with Cys, Hcy and GSH (20 μmol/L, 30 min), and finally incubated with QDA (20 μmol/L, 30 min). Green channel: λem = 510–550 nm
(
λ
ex = 458 nm); red channel: λem = 600–630 nm (λex = 488 nm). Scale bar: 200 μm.
nals appeared at 6.54–6.11 ppm, which indicated that both alde-
hyde groups of QDA were involved in the reaction. Moreover, MS
analysis of the adduct of QDA with GSH also supported the gen-
treated with NEM were incubated with Hcy (20 μmol/L, 30 min)
and QDA (20 μmol/L, 20 min), a significant fluorescence enhance-
ment in green channel was observed. The above experimental re-
sults showed that red fluorescence emission was generated by
the adduct of QDA with intracellular GSH, and green fluorescence
emission was attributed to intracellular Hcy. Hence, QDA could dis-
tinguish the imaging of GSH and Hcy inside cells in different fluo-
rescent channels.
ꢀ
ꢀ
eration of thiazino[3 ,2 :1,2]pyrrolo[3,4-b]quinoline derivative, the
peak at m/z 457.1199 was observed (Fig. S11 in Supporting informa-
+
tion), corresponding to [QDA-GSH + H] , calcd. for C21H21N O S:
4
6
4
57.1176. Similarly, a peak of m/z 285.0705 was observed from
MS spectrum of the adduct of QDA with Hcy (Fig. S12 in Sup-
+
porting information), corresponding to [QDA-Hcy + H] , calcd. for
Based on the excellent imaging results of QDA to intracellu-
lar GSH and Hcy, QDA was further used for zebrafish imaging.
As shown in Fig. 3, a significant fluorescence was observed in
green channel and red channel after zebrafish was incubated with
QDA (20 μmol/L) for 30 min. Nevertheless, zebrafish pretreated
with NEM (200 μmol/L) was loaded with QDA (20 μmol/L) for
30 min, there was no fluorescence emission in green channel
and red channel, which displayed that the fluorescence emission
of Figs. 3B-D were caused by the adducts of QDA and biothiols
in zebrafish. When zebrafish pretreated with NEM (200 μmol/L,
30 min) and Cys (20 μmol/L, 30 min) was loaded with QDA (20
μmol/L, 30 min), all the same no fluorescence was observed. How-
ever, zebrafish pretreated with NEM (200 μmol/L, 30 min) and Hcy
(20 μmol/L, 30 min) was loaded with QDA (20 μmol/L, 30 min),
only green fluorescence emission was observed in green chan-
nel. Similarly, only red fluorescence emission was observed in red
channel after zebrafish was continuously loaded with NEM (200
μmol/L, 30 min), GSH (20 μmol/L, 30 min) and QDA (20 μmol/L,
30 min). These results indicated that QDA could be used to differ-
C
H N O S: 285.0692. Therefore, the speculated mechanism was
13 2 2
15
correct and supported the spectral experimental results.
Inspired by excellent performance of QDA in distinguishing
GSH and Hcy in vitro, we further evaluated the applicability of
QDA in biological systems. First, the toxicity of QDA was tested
by methyl thiazolyl tetrazolium (MTT) assay [46], and the results
demonstrated that QDA was low cytotoxic to A549 cells below
2
0 μmol/L concentration within 10 h (Fig. S13 in Supporting in-
formation). Next, the confocal images of QDA to GSH and Hcy in
A549 cells were investigated. As shown in Fig. 2, the cells were
incubated with QDA (20 μmol/L) for 20 min, there was conspicu-
ous fluorescence in green channel and red channel. Moreover, the
cells were pretreated with NEM (1 mmol/L) for 30 min and in-
cubated with QDA (20 μmol/L) for 20 min, the fluorescent inten-
sity of green channel and red channel became weak. However, the
cells pre-treated with NEM were incubated with GSH (20 μmol/L,
3
0 min) and QDA (20 μmol/L, 20 min), a significant fluorescence
enhancement in red channel was observed. Likewise, the cells pre-
4

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Supplementary materials
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found, in the online version, at doi:10.1016/j.cclet.2021.05.016.
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