A Photostable AIEgen for Specific and Real-time Monitoring of Lysosomal Processes

Article abstract of DOI:10.1002/asia.201801676

Lysosomes are recognized as advanced organelles involved in many cellular processes and are also considered as crucial regulators of cell homeostasis. The current strategies for monitoring activities of lysosomes exhibit some limitations. Herein, we synthesized a novel fluorescent probe named 2M-DPAS with AIE characteristics, which was proved to have significant advantages of good biocompatibility, high selectivity, bright emission and excellent photostability. Based on those, 2M-DPAS can be used to continuously monitor the dynamic changes of lysosomes, including autophagy and mitophagy, as well as to track the process of endocytosis of macromolecules in lysosomes, which are of benefit to better know about the lysosomes-related diseases.

Full text of DOI:10.1002/asia.201801676

CHEMISTRY
AN ASIAN JOURNAL
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Accepted Article
Title: A Photostable AIEgen for Specific and Real-time Monitoring of
Lysosomal Processes
Authors: Zhiming Wang, Weijie Zhang, Fan Zhou, Jian Du, Zujin Zhao,
Anjun Qin, and Ben Zhong Tang
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To be cited as: Chem. Asian J. 10.1002/asia.201801676
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A Photostable AIEgen for Specific and Real-time Monitoring of
Lysosomal Processes
Weijie Zhang,#[a, b, d] Fan Zhou,#[c] Zhiming Wang,*[a, c] Zujin Zhao, [c] Anjun Qin,[c] and Ben Zhong
Tang,*[a, c, d]
Abstract: Lysosomes are recognized as advanced organelles
involved in many cellular processes, and are also considered as
crucial regulators of cell homeostasis. The current strategies for
monitoring activities of lysosomes exhibit some limitations. Herein, we
synthesized a novel fluorescent probe named 2M-DPAS with AIE
characteristics, which was proved to have significant advantages of
good biocompatibility, high selectivity, bright emission and excellent
photostability. Based on those, 2M-DPAS can be used to continuously
monitor the dynamic changes of lysosomes including autophagy and
mitophagy, as well as to track the process of endocytosis of
macromolecules in lysosomes, which are benefit to better know about
the lysosomes-related diseases.
Importantly, lysosomal dysfunction causes many diseases, such
as cancer and Alzheimer's disease.[5] In view of the essential
functions of lysosomes, imaging and monitoring the dynamic
changes of lysosomal morphology and spatial distribution are
highly useful in the management of lysosomal related diseases.
Lysosomes are the main digestive organelles in almost all
eukaryotic cells and were first discovered by Christian de Duve in
the 1950s.[1] They are contained by a single phospholipid-bilayer
of 7–10 nm in which more than 25 membrane proteins have been
identified.[2] The lumen of lysosomes contains more than 50 acid
hydrolases, which are readily attached to alkaline substances.[3]
The basic function of lysosomes is to digest extracellular
macromolecules that have been internalized by endocytosis and
intracellular metabolic organelles such as mitochondria that have
been sequestered by autophagy.[4] To achieve these functions,
lysosomes are continuously changing their morphology and
spatial distribution, with their shapes ranging from spherical to
tubular. Therefore, lysosomal disturbance has profound effects on
cell homeostasis. Recently, it has been found that the positioning
of lysosomes could be precisely controlled to meet the changing
cellular needs. For example, under nutrient deprivation conditions,
lysosomes could be rapidly recruited to the perinuclear region.
Figure 1. (A) The chemical structure of DPAS and 2M-DPAS. (B) PL
spectra of 2M-DPAS in THF/water mixtures with different water fractions.
[2M-DPAS] = 10 µM. (Inset: fluorescent images at fw = 0% and fw ≈ 99%
)
The most common strategies used to visualize and
monitor lysosomes apply compounds whose pH-dependent
fluorescence is weak in basic and neutral conditions but can
be “turned on” in acidic environments, such as the
LysoSensor™ pH Indicator used as a commercial dye.[6]
Other examples of labeling lysosomes include neutral red,[7]
acridine orange,[8] LysoTracker,[9] dextran labeled with a
fluorophore[10] and nanoparticles.[11] Although these probes
track the lysosomes effectively, they suffer many limitations.
For example, the low specificity of neutral red and acridine
[a]
Dr. W. Zhang, Dr. Z. Wang, Prof. B. Tang
HKUST-Shenzhen Research Institute
Nanshan, Shenzhen, 518057 (China)
E-mail: wangzhiming@scut.edu.cn
orange
for
lysosomes, rapid
photobleaching
of
LysoTracker,[9] and high cytotoxicity of nanoparticles and
dextran,[10] limit their applications considerably. It is thus
imperative to develop a new probe to image lysosomes with
tangbenz@ust.hk
[b]
[c]
Dr. W. Zhang
Urinary surgery, Affiliated first hospital
Soochow University
Pinghai Road, Suzhou, 215006 (China)
F. Zhou, Dr. Z. Wang, Prof. A. Qin, Prof. B. Tang
State Key Laboratory of Luminescent Materials and Devices, Centre
for Aggregation-Induced Emission,
high
specificity,
good
biocompatibility,
excellent
photostability and a high signal-to-noise ratio.
A novel photophysical phenomenon of aggregation-induced
emission (AIE) was developed in our group since 2001.[12]
Fluorogens with AIE (AIEgens) properties are highly emissive in
the aggregation state but demonstrate faint emission in dilute
solution, which is ideal for imaging and biosensing because of
most organic emitters based on conjugated aromatic structure
suffered from aggregation-caused quenching effect.[13] Restricted
intramolecular motion (RIM) of AIEgens in the aggregation state
was the main mechanism of the AIE effect by lots of experiments
and calculation,[14] so, many AIEgens were developed via utilizing
this nature to image intramolecular organelles, but few of them
were used to track and monitor lysosomes with their physiological
processes.[15]
South China University of Technology
Wushan Road, Guangzhou, 510640 (China)
E-mail: msqinaj@scut.edu.cn
[d]
#
Dr. W. Zhang, Prof. B. Tang
Department of Chemistry and Department of Chemical and
Biological Engineering
The Hong Kong University of Science and Technology
Clear Water Bay, Kowloon, Hong Kong, China
These authors have contributed equally to the work and then query
the author if this is correct at proof stage
Supporting information for this article is given via a link at the end of
the document.
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10.1002/asia.201801676
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We have previously reported on lipid droplets-targeting
fluorescence from LTR are clearly visualized, respectively. The
merged image shows that the distribution of 2M-DPAS in cells is
totally consistent with that of LTR (Figure 2D). The Pearson’s
correlation coefficient, which describes the degree of linear
dependence between two variables, is 0.96, suggesting that 2M-
DPAS specifically targets lysosomes. Additionally, 2M-DPAS
showed a higher contrast than LTR under the same incubation
time, which can be attributed to the bright emission and high
selectivity of 2M-DPAS. Furthermore, the PL intensity of 2M-
DPAS was tested in different pH buffered solutions. Besides,
there was not a larger shift in emission peak location in aqueous
solution and in lysosomes of Hela cells, implying its pH-
independent properties (Figure S4).
DPAS
(2-(((diphenylmethylene)hydrazono)-methyl)-phenol),
which has excellent biocompatibility and monitoring dynamics.[16]
In this work, we designed and synthesized a novel AIE fluorogen,
namely 2M-DPAS, based on DPAS (Figure 1A), and its synthetic
route and analysis data are shown in Scheme S1 and Figure S1,
S2. The chain length of six carbons ensure probe flexibility and
the two basic morpholine groups allow 2M-DPAS to easily target
lysosomes which contain many acid hydrolases. As discussed
further below, in our investigation of the potential of 2M-DPAS in
monitoring the dynamic changes of lysosomes with autophagy,
mitophagy and phagocytosis of macromolecules, 2M-DPAS
consistently showed excellent performance.
0
B
A
100
80
20
40
60
60
40
80
20
0
100
5
10
15
20
30
0
25
0
1
5
10
20
30
No. of scan
Concentration (μM)
Figure 3. (A) Signal loss (%) of fluorescent emission of 2M-DPAS (red circles)
and LTR (black squares) with increasing number of scans. (B) Cell viability of
2M-DABS evaluated on HeLa cells by MTT assay.
Figure 2. (A) Bright field and (B) fluorescent images of HeLa cells stained with
2M-DPAS (10 M, 30 min) or (C) Lysotracker Red (75 nm, 30 min). (D) A
superimposed image from (B) and (C). Scale bar = 30 µm.
The photophysical properties of 2M-DPAS were studied first.
The absorption band of 2M-DPAS peaked at 415 nm in THF
solution (Figure S3) while its emission peak location was
observed at 550 nm (Figure 1B). Thanks for its classical ESIPT
emission process, the Stokes-shift of 2M-DPAS reaches to 135
nm, which is benfit to high quality imaging. In fact, 2M-DPAS
emitted faintly in pure THF solutions, and its emission remained
low even the solution contained a large amount of water (50 vol%).
However, with further increase of the water fraction, 2M-DPAS
fluoresced more strongly at 550 nm with a light yellow color, a
clear property of AIE, thus avoiding the ACQ problem with most
of the conventional fluorescent probes of lysosomes. Obviously,
the weak emission of 2M-DPAS in pure THF solutions was due to
non-radiative decay caused by dynamic intramolecular motion,
while in the aggregated state, the ESIPT process was activated
and the strong emission from keto-form was shown due to the
restricted intramolecular hydrogen bond motion.
With DPAS specifically targeting lipid droplets, the specificity
of 2M-DPAS in cells was explored as well. We speculated that the
basicity of the two morpholine groups would enable 2M-DPAS to
accumulate in the acidic environments of lysosomes (pH 4.5–5.0).
Thus, the well-known commercial lysosome-targeting dye
Lysotracker Red (LTR) was co-stained with 2M-DPAS. As shown
in Figure 2, green fluorescence from 2M-DPAS and red
Figure 4. (A–C) Bright field and (D–F) fluorescent images of HeLa cells stained
with 10 µM 2M-DPAS: (A, D) before treatment, (B, E) after treatment of
rapamycin and (C, F) after treatment of rapamycin and 3-MA. Scale bar = 30
µm.
Besides selectivity, photostability is considered one of the
key factors in evaluating the performance of fluorescent imaging
probes. The photostability of HeLa cells co-stained with 2M-DPAS
and LTR was investigated by monitoring the fluorescence
intensity before and after 30 consecutive scans by a confocal
microscopy. As shown in Figure 3A, the signal loss of 2M-DPAS
was less than 15% of the original intensity after 30 scans. In
contrast, the fluorescence signal loss of LTR reached up to 95%.
There were no significant differences observed between the first
and the 30th fluorescence images of 2M-DPAS, whereas no
fluorescence was observed in the 30th fluorescence image of LTR
(Figure S5). The main reason was the difference in working
concentrations of different fluorescent probes for lysosomal
imaging due to their own properties. Truly, the working
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10.1002/asia.201801676
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concentration of 2M-DPAS is up to 133 times that of LTR,
resulting in higher brightness and photostability of 2M-DPAS in
lysosomal imaging. If the LTR reached this concentration, the
fluorescence intensity would decrease greatly because its ACQ
effect was activated. Thanks for the AIE nature of 2M-DPAS, the
excellent photostability was realized, and the long-term lysosomal
imaging could become possible.
rapamycin (mTOR) is an important suppressor of autophagy
functioning upstream of the autophagy protein,[17] inhibition of
mTOR potently up-regulates autophagy during the cellular
response to the specific mTOR inhibitor, rapamycin.[18] As shown
in Figure 4 (D–F), the lysosomes of HeLa cells can be clearly
visualized, with each green spot representing a lysosome under
the fluorescence microscope. First, we found that the lysosomes
increased in quantity and were widely distributed intracellularly
after HeLa cells were treated with rapamycin (50 μg/mL),
suggesting that the process of autophagy was monitored in real
time (Figure 4E). Meanwhile, we also used 3-MA, a well
characterized inhibitor of the early stage of autophagy.[19] As
illustrated in Figure 4F, no obvious changes were observed in the
quantity and spatial distribution of lysosomes 30 min after
simultaneously adding 3-MA (10 mM) and rapamycin (50 μg/mL)
into the culture medium of 2M-DPAS stained HeLa cells. This
resulted from the addition of 3-MA to the HeLa cells, inhibiting the
initial stage of autophagy despite the presence of rapamycin.
Therefore, 2M-DPAS can accurately monitor the process of
autophagy in real time, which, along with its high selectivity for
lysosomes and excellent photostability, make it an excellent
choice for investigating the process of autophagy.
In addition, the cytotoxicity of 2M-DPAS on HeLa cells was
assessed using MTT assay to confirm the safety of 2M-DPAS in
visualizing lysosomes. As illustrated in Figure 3B, when the cells
were incubated with up to 20 mM of 2M-DPAS for 24 h, the cell
viability remained above 80%. Even at concentration as high as
30 mM, the cell growth was not greatly impaired, indicating a weak
effect of 2M-DPAS on cell growth. The excellent biocompatibility
and photostability of 2M-DPAS therefore renders it a useful
fluorescent probe for dynamically monitoring lysosomes during
different physiological processes.
Figure 5. Fluorescent images of HeLa cells at different layers stained with 10
µM 2M-DPAS and 50 nM MTR (A-F) before treatment of rapamycin; Fluorescent
images of HeLa cells at different layers stained with 10 µM 2M-DPAS and 50
nM MTR (G-L) after treatment of rapamycin. Scale bar = 20 µm.
Figure 6. Fluorescent images of HMCs after treatment of 2 µM FAM-Aβ for 1 h
(A) or 24 h (D), followed by 10 µM 2M-DPAS for 30 min (B, E). Merged
fluorescent images of HMCs treatment and 2M-DPAS (C, F); Fluorescent
images of HMCs after treatment of 2 µM FAM-Aβ for 1 h (G) or 24 h (J), followed
by 50 nM LTR for 30 min (H, K) Merged fluorescent images of HMCs treatment
and LTR (I, L). The yellow arrows indicate the locations of FAM-Aβ. Scale bar =
10 µm.
Autophagy is a process that transports damaged cells,
degenerated or aging proteins, and organelles to the lysosomes
for digestion and degradation. Visualizing and tracking activities
of lysosomes enrich the insight into the process of autophagy
given the close association of lysosomes and autophagy.
Considering that 2M-DPAS has high specificity for lysosomes and
strong photostability, the ability of real-time monitoring of dynamic
changes of autophagy was tested. Since mammalian target of
Autophagy is a non-selective process whereby mitochondria
are the targets of autophagy. Therefore, mitophagy can also be
triggered by rapamycin.[20] As shown in Figure 5, different layers
of mitochondria could be clearly captured by confocal microscopy
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10.1002/asia.201801676
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in HeLa cells co-stained with 2M-DPAS and MitoTracker Red
(MTR) after treatment without or with rapamycin. The long
filamentous structures of mitochondria were clearly shown in red
from MTR while the punctate structures of lysosomes were well
portrayed as green spots from 2M-DPAS. Compared with Hela
cells cultured without rapamycin (Figure 5A-F) and with
rapamycin (Figure 5G-L) (50 μg/mL) to induce mitophagy,
pronounced changes had taken place in the quantity and spatial
distribution of lysosomes and the morphology of mitochondria (Fig.
5). The network structures of mitochondria appeared broken and
punctate, and numerous lysosomes could be seen distributed
widely in the three-dimensional layer of one mitochondrion. In
addition, the coincidence degree between lysosomes and
mitochondria increased markedly. Therefore, the process of
mitophagy was effectively monitored in the presence of 2M-DPAS
and MTR, further demonstrating the superiority of 2M-DPAS in
monitoring the dynamics of lysosomes.
(201804010218), Science and Technology Plan of Shenzhen
(JCYJ20160428150429072 and JCYJ20160229205601482), the
Innovation and Technology Commission of Hong Kong (ITC-
CNERC14S01), and the Fundamental Research Funds for the
Central Universities (2015ZY013, 2017JQ013 and 2017B0036).
Conflicts of interests
There are no conflicts to declare.
Keywords: Lysosomes • Aggregation-induced emission •
Monitoring • Autophagy • Phagocytosis of macromolecules
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In summary, we have reported a novel fluorescent probe 2M-
DPAS with AIE characteristics for specific lysosomal imaging. Its
good biocompatibility, high selectivity, bright emission, pH-
independence and excellent photostability enable continuous
monitoring of the dynamic changes of lysosomes in real time. This
probe has been demonstrated to effectively monitor and track the
processes of autophagy, mitophagy and phagocytosis of
macromolecules in lysosomes in real time. Importantly, 2M-DPAS
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Acknowledgements
This work is financially supported by National Natural
Science Foundation of China (21788102, 51673118, 81472401
and 51603127), Science & Technology Program of Guangzhou
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2M-DPAS, as a specific probe
for lysosome, can be used to
Weijie Zhang,#[a, b, d] Fan Zhou,#[c]
Zhiming Wang,*[a, c] Zujin Zhao, [c] Anjun
Qin,[c] and Ben Zhong Tang#[a,c, d]
continuously
dynamic changes of lysosomes
including autophagy and
monitor
the
Page No. – Page No.
mitophagy, as well as to track
the process of endocytosis of
macromolecules in lysosomes
with significant advantages of
good biocompatibility, high
selectivity, bright emission and
excellent photostability.
Photostable AIEgen for Specific and
Real-time Monitoring of Lysosomal
Processes
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