An off-the-shelf sensor for colourimetric detection of sulfide

Article abstract of DOI:10.1016/j.tetlet.2016.11.040

The cheap, accessible spiropyran nitroBIPS is a sensitive, selective colourimetric sensor for quantitative determination of sulfide in aqueous media at neutral pH.

Full text of DOI:10.1016/j.tetlet.2016.11.040

Tetrahedron Letters xxx (2016) xxx–xxx
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Tetrahedron Letters
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An off-the-shelf sensor for colourimetric detection of sulfide
⇑
Alexis Perry , Daniel Miles
Biosciences, Geoffrey Pope Building, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
a r t i c l e i n f o
a b s t r a c t
Article history:
The cheap, accessible spiropyran nitroBIPS is a sensitive, selective colourimetric sensor for quantitative
determination of sulfide in aqueous media at neutral pH.
Received 14 September 2016
Revised 4 November 2016
Accepted 8 November 2016
Available online xxxx
Ó 2016 Elsevier Ltd. All rights reserved.
Keywords:
Hydrogen sulfide
Sensor
Spiropyran
NitroBIPS
Introduction
access to specialist synthetic chemistry facilities. Recent develop-
ment of
a benzofurazan-based sulfide reporter has, in part,
There is now considerable evidence that supports hydrogen sul-
fide as being a third physiological gasotransmitter, alongside nitric
oxide and carbon monoxide.1–3 Contemporary research has impli-
cated endogenous hydrogen sulfide release in many important
pathologies4–7 and various hydrogen sulfide donor molecules are
undergoing scrutiny as therapeutic agents.8,9 To support this
expanding research field, there has been a tandem development
in methods for the detection and quantification of hydrogen sulfide
in solution.10–12 Perhaps the key approach to this goal has been the
synthesis of small molecule probes which enable colourimetric
and/or fluorimetric measurement of hydrogen sulfide concentra-
tion in solution.11,12 Although the challenges that this presents
are manifold, the principal difficulty that an effective probe mole-
cule must overcome is that physiologically relevant hydrogen sul-
addressed this requirement;15 herein we present a complementary
approach.
Spiropyrans (e.g. SP-1; Scheme 1) are a class of spiro-fused
indolochromene photochromes, commonly deployed in molecu-
lar/optical switching and sensing applications.16–18 The pho-
tochromic behaviour displayed by a spiropyran is based upon the
light-dependent equilibrium with its zwitterionic merocyanine
isomer (e.g. MC-1): whereas spiropyrans are usually colourless in
solution, merocyanines are fully conjugated, highly coloured and
fluorescent (Scheme 1). Spiropyran/merocyanine-based H2S
probes, such as 2 (Fig. 1),19 rely upon nucleophilic attack of HSꢀ
upon the iminium ion present within the merocyanine structure,
with the consequent disruption of the extended merocyanine con-
jugation resulting in reduced visible absorption/fluorescence emis-
sion (Scheme 1). As such, spiropyran/merocyanine-based H2S
sensors are often ‘‘switch-off” in nature. Such probes discriminate
between H2S and biologically competitive thiols on the basis of
acidity: at physiological pH the lower pKa value of H2S (ꢁ7.0) com-
pared with other biologically competitive thiols (e.g. cysteine, glu-
tathione, pKa > 8.5) ensures a greater degree of dissociation, hence
a high concentration of strongly nucleophilic HSꢀ.
fide concentrations are low (<1 l
M)13 and occur against a high
background concentration of molecules that present similar chem-
ical reactivity (e.g. thiols such as cysteine, homocysteine and glu-
tathione; intracellular glutathione concentration is in the mM
range).14 Several classes of small molecule hydrogen sulfide probe
have recently emerged which meet these stringent requirements
for selectivity and sensitivity and have been employed with rea-
sonable success in biological media;11,12 nevertheless, none of
these molecules have been adopted widely. We speculate that this
is a matter of cost and convenience; there is a need for cheap, ‘‘off-
the-shelf” probes for the majority of workers, who do not have
10,30-Dihydro-10,30,30-trimethyl-6-nitrospiro[2H-1-benzopyran-
2,20-(2H)-indole] 1, commonly known as nitroBIPS, is a cheap and
readily accessible spiropyran, available both commercially or
through facile synthesis.20 Although the response of nitroBIPS to
H2S has not been investigated, the same molecule has been used
as a sensitive, selective probe for anionic cyanide.21 In this capac-
ity, nitroBIPS could accurately detect [CNꢀ] to a minimum of
⇑
Corresponding author.
E-mail address: A.Perry@exeter.ac.uk (A. Perry).
http://dx.doi.org/10.1016/j.tetlet.2016.11.040
0040-4039/Ó 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Perry A., Miles D.. Tetrahedron Lett. (2016), http://dx.doi.org/10.1016/j.tetlet.2016.11.040

2
A. Perry, D. Miles / Tetrahedron Letters xxx (2016) xxx–xxx
NO2
Preparation of a 0.1 mM solution of nitroBIPS in 1:1 acetoni-
trile–water (PBS 5 mM; pH = 7.4) resulted in a pink solution which
displayed a strong absorbance in the visible region (518 nm), cor-
responding to the merocyanine isomer MC-1. This solution deco-
lourised when exposed to standard ambient light for 10 min,
with the corresponding loss of the 518 nm absorption band attrib-
uted to complete isomerisation to spiropyran SP-1. If the initially
pink solution was kept in darkness, the initial merocyanine con-
centration remained approximately constant over 30 min. Conse-
quently, we adopted dark conditions for the use of nitroBIPS as a
sensor molecule in acetonitrile–water. This contrasts somewhat
with previous work, where nitroBIPS in 1:1 acetonitrile–water
(CHES 100 mM; pH = 9.3) required UV irradiation to ensure the
presence of merocyanine; only spiropyran was present in
darkness.21
hυ
N
O
NO2
visible
light
N
O
nitroBIPS spiropyran isomer
(SP-1): λmax = 380 nm
nitroBIPS merocyanine isomer
(MC-1): λmax = 520 nm
X
NO2
1-CN
X = CN;
X = SH; 1-SH
λmax = 420 nm
N
X
O
NitroBIPS was then assessed as a sulfide sensor, as follows. Aqu-
eous solutions of sulfide or other potentially competitive species
(50 equiv.) were added to individual aliquots containing nitroBIPS
(0.1 mM in 1:1 acetonitrile–water; PBS 5 mM; pH = 7.4) then left in
darkness for 30 min before being analysed by UV–visible spec-
troscopy. From the results shown in Fig. 2, it is apparent that nitro-
BIPS is unreactive towards most nucleophiles under these
conditions: solutions were produced that reflected modulation of
the spiropyran-merocyanine equilibrium but did not suggest
nucleophilic addition (addition of sodium sulfite resulted in a
change in absorbance line shape but without apparent erosion of
spiropyran or merocyanine absorbance and without appearance
of further visible absorbance peaks). In contrast, in the presence
of cyanide, a yellow solution was produced which absorbed
strongly at 418 nm and displayed no merocyanine absorbance. A
similar result was observed when nitroBIPS was treated with sul-
fide; however, the resulting solution displayed a further absor-
bance at 286 nm. On the basis of these results, nitroBIPS can be
viewed as a selective sensor for sulfide; competition is only
observed from cyanide (with weak interference from sulfite), and
sulfide addition can be distinguished from that of cyanide by
observation of the k286 absorbance. It is important to note that
quantitative sulfide detection in the presence of cyanide is not pos-
sible under these conditions, which would result in depletion of
MC-1 by cyanide and hence under-reporting of the k286 absor-
bance. NitroBIPS is reactive towards sulfide but shows no reactivity
towards apparently similar sulfur-based nucleophiles such as mer-
captoethanol, mercaptopropionic acid, cysteine and glutathione.
This distinction is absolutely crucial because cellular sulfide deter-
mination must occur against a high background concentration of
cysteine and glutathione.
Scheme 1. Spiropyran-merocyanine equilibrium and reaction with cyanide/sulfide.
O
N
N
O
N
I
O
2
NEt2
Fig. 1. Sulfide probe based upon a merocyanine-coumarin conjugate.
1.7
lM in 1:1 acetonitrile–water and showed a high degree of
selectivity for cyanide against a range of potentially competitive
anions. It is notable, however, that HSꢀ was not included and that
these experiments were buffered to pH = 9.3 (the authors noted
that sensitivity to NCꢀ was considerably diminished at neutral
pH). The product of cyanide addition to nitroBIPS displayed a
strong, blue-shifted absorbance distinct from that of the merocya-
nine; hence the cyanide response could be quantified either by a
reduction in merocyanine absorbance and fluorescence (as a
switch-off sensor) or by an increase in addition product absorbance
(switch-on).
In light of the above studies, nitroBIPS presented an obvious
candidate for investigation as an easily-accessible colourimetric/
fluorimetric hydrogen sulfide probe. In this work, we assess the
performance of nitroBIPS as a colourimetric probe for hydrogen
sulfide in aqueous solution at physiological pH.
Results and discussion
Quantitative determination of sulfide concentration was
achieved by titration of sulfide against nitroBIPS and ratiometric
analysis of the characteristic absorbance peaks assigned to 1-SH
(286 nm) and MC-1 (518 nm). A linear relationship (R2 = 0.9927)
between Na2S and 1-SH/MC-1 was observed, indicating that accu-
rate measurement of sulfide is possible in this range (Fig. 3). The
lower limit of detection was defined by the average of 5 repetitions
of the blank experiment (i.e. in the absence of sulfide) + 3 standard
deviations from the mean. In this instance, with [nitroBIPS]
= 0.1 mM, this corresponded to a limit of detection of [HSꢀ]
NitroBIPS was synthesised via the straightforward condensation
of tetramethylindolium iodide 3 and nitrosalicylaldehyde 4 in
ethanol at reflux (Scheme 2).20 The merocyanine isomer precipi-
tated from the reaction mixture in excellent yield and high purity
and following filtration, no further purification was necessary.
Given the photochromic nature of nitroBIPS and that previous
work has identified the merocyanine isomer, and not the spiropy-
ran, as the sole reactive electrophile in detection of cyanide,21 our
initial investigations identified appropriate conditions for use of
nitroBIPS as a sulfide sensor by promoting merocyanine formation.
= 10.7 lM or, to provide generality in terms of sensor probe con-
centration, 1 equivalent of nitroBIPS provides a limit of detection
of 0.11 equivalents sulfide. Ultimately, the absolute lower limit
of detection will depend upon the lowest possible [nitroBIPS]
detectable by the spectrophotometer. Using an entry level spec-
trophotometer (Jenway 7315), nitroBIPS could be detected to a
NO2
H
EtOH
NO2
O
+
N
Δ
18 h
N
O
HO
I
minimum concentration of 5 lM, at which point sulfide detection
remained effective (Fig. 2, inset). Consequently, applying our lower
limit of detection to this experiment, we anticipate that statisti-
cally relevant detection of [SHꢀ] = 550 nM is possible.
3
4
MC-1
; 99%
Scheme 2. Synthesis of nitroBIPS.
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A. Perry, D. Miles / Tetrahedron Letters xxx (2016) xxx–xxx
3
Fig. 2. Selectivity and (inset) sensitivity of nitroBIPS as a sulfide sensor. (Main plot) Absorbance spectra of 1 (0.1 mM in 1:1 acetonitrile–water; PBS 5 mM; pH = 7.4) following
addition of biologically relevant species (100 L of 0.1 M solutions in water, 50 equiv.; final concentration = 5 mM) or water control (100 L) and 30 min in darkness. Red
line = nBuNH4CN; blue line = Na2Sꢂ9H2O; green line = Na2SO3; grey lines = no additive, NaCl, KF, KBr, KI, NH4OAc, NaH2PO4ꢂ2H2O, Na2SO4ꢂ10H2O, NaNO3, NaSCNÅH20, SIN-
M in 1:1 acetonitrile–water; PBS 5 mM; pH = 7.4);
l
l
1ÅHCl, 3-mercaptopropionic acid, 2-mercaptoethanol, cysteine, glutathione. (Inset) Grey line = absorbance spectra of 1 (5
l
blue line = following addition of Na2Sꢂ9H2O (25
lL of 20 mM aqueous solution, 50 equiv.; final concentration = 250
l
M) and 30 min in darkness.
14
12
10
8
R2 = 0.9927
6
4
2
0
0
100
200
300
400
500
600
700
800
900
1000
[sodium sulfide] / μM
Fig. 3. Change in the absorbance ratio (A286/A518) of 1-SH and MC-1 with sulfide concentration. Individual samples of 1 (0.1 mM in 1:1 acetonitrile–water; PBS 5 mM;
pH = 7.4) and Na2Sꢂ9H2O (0–1000 M) were placed in darkness for 1 h then analysed by UV–visible spectroscopy.
l
For a sulfide probe to have biological utility, detection of micro-
molar sulfide against a background of millimolar glutathione is
essential. Consequently, we validated of the utility of nitroBIPS as
a sulfide probe by quantification of its response to sulfide in the
At higher sulfide concentrations, reaction with nitroBIPS became
effective and gave a linear ratiometric response (A420/A518) to
10 lM increments in sulfide concentration (Fig. 4, inset). We sur-
mise that this apparent reduction in sulfide sensitivity is actually
a reflection of the HSꢀ available to react with nitroBIPS. We suggest
that glutathione has no direct impact upon nitroBIPS but that it
modifies the sulfide pool equilibria in such a way as to reduce
[HSꢀ]; perhaps through reaction of the persulfide anion with
reduced glutathione.22 We observed a similar, apparently reduced
response to sulfide in the presence of cysteine, and reduced sulfide
sensitivity in the presence of glutathione and cysteine has been
reported with other sulfide probes.15
presence of 5 mM glutathione, using 10 lM nitroBIPS (Fig. 4). Ini-
tially, we ascertained that nitroBIPS displayed no reactivity
towards glutathione (despite the 500-fold excess of the latter),
by comparison with a glutathione-free control (Fig. 4; dark and
light blue lines). Subsequent introduction of sulfide (25 equiv.,
250 lM) had minimal impact upon the system; a somewhat sur-
prising result given that previously, in the absence of glutathione,
similar conditions resulted in formation of 1-SH (see Figs. 2 and 3).
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A. Perry, D. Miles / Tetrahedron Letters xxx (2016) xxx–xxx
Fig. 4. Quantification of [sulfide] using nitroBIPS in the presence of glutathione. (Main plot) Absorbance spectra of 1 (10
dark blue line = control; all other lines represent samples containing glutathione (5 mM) and Na2Sꢂ9H2O (0–300 M as follows) recorded after 30 min in darkness: light
blue = 0 M; green = 250 M; yellow = 260 M; orange = 270 m; red = 280 m; purple = 290 M; pink = 300 M. (Inset) Change in the absorbance ratio (A420/A518) of 1-SH
and MC-1 with sulfide concentration in the presence of glutathione, extracted from the spectra above.
lM in 1:1 acetonitrile–water; PBS 5 mM; pH = 7.4):
l
l
l
l
l
l
l
l
All analyses to this point were conducted in a mixed solvent
system to mitigate against the low solubility of nitroBIPS in water.
Given our interest in sulfide detection in biological media, we
briefly examined the effectiveness of nitroBIPS as a sulfide sensor
in biologically compatible solvents. NitroBIPS is partially soluble
in water at 0.1 mM and further dilution does not prevent partial
precipitation. Presumably, this reflects the equilibrium between
neutral, insoluble spiro- and zwitterionic, soluble mero-forms. Con-
sequently, equilibrium driven-precipitation of spiropyran will
always prevent full solubilisation. Despite this, sufficient merocya-
nine remains in solution for nitroBIPS to function as a sulfide sen-
sor in water: addition of Na2Sꢂ9H2O (50 equiv.) to a 0.1 mM
suspension of nitroBIPS in water, followed by standing in darkness,
resulted in complete conversion of MC-1 to 1-SH (Fig. 5). As such,
nitroBIPS is a useful qualitative sulfide probe in water, but is not
suitable for quantitative analysis. On the other hand, nitroBIPS is
soluble in 1%(v/v) aqueous DMSO at 0.1 mM and can be used to
determine sulfide concentration in this medium.
Following these initial studies, the interactions of nitroBIPS
with cyanide and sulfide were compared in greater depth to iden-
tify conditions that would enable quantitative determination of
sulfide in the presence of cyanide. At pH = 9.3, cyanide addition
to nitroBIPS is light-reversible (hence the sensor can be regener-
ated with white light)21 and we observed similar behaviour at
pH = 7.4 with both cyanide and sulfide. Solutions of 1-SH and 1-
CN were prepared by sulfide or cyanide addition, respectively, to
solutions of nitroBIPS, then kept in darkness for 30 min. These
solutions were then irradiated with white light for 30 min. Both
solutions displayed a degree of photoreversion, and although this
effect was more pronounced in the cyanide case (UV–visible spec-
troscopy showed 60%/30% decline in 518 nm absorbance for
cyanide/sulfide samples, respectively), the limited extent of this
differential reactivity is not analytically useful in distinguishing
sulfide from cyanide.
Shiraishi and co-workers demonstrated that cyanide addition
could only occur via the merocyanine isomer of nitroBIPS and
therefore employed UV irradiation to ensure a high merocyanine
concentration.21 Conversely, we investigated the addition of cya-
nide and sulfide to nitroBIPS under conditions in which the mero-
cyanine concentration was minimised, in order to exploit the
greater nucleophilicity of sulfide over cyanide. Solutions of nitro-
BIPS were irradiated with white light for 1 min to produce solely
the spiropyran isomer, before adding cyanide/sulfide and placing
in darkness. In both cases, addition of the anion to nitroBIPS
occurred slowly; however, whereas cyanide addition was negligi-
ble after 2 h, sulfide addition was significantly more effective
(Fig. 6). To validate this encouraging result, the same illumina-
tion/addition protocol was followed to give a nitroBIPS solution
containing both cyanide and sulfide. Gratifyingly, this displayed
near-identical behaviour to that containing sulfide alone, confirm-
ing the negligible effect of cyanide under these conditions (Fig. 6,
inset). Consequently, although a long (2 h) measurement time is
necessary, nitroBIPS can function as a sensor for sulfide in the pres-
ence of cyanide, provided that the merocyanine isomer is elimi-
nated from the system as a starting position by irradiation with
Fig. 5. Absorbance spectra of
pH = 7.4): (a) before addition of Na2S (grey line); (b) following addition of Na2-
Sꢂ9H2O (100 L of 0.1 M solution in water, 50 equiv.) and standing in darkness for
30 min (blue line).
1 (0.1 mM suspension) in water (PBS 10 mM;
l
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A. Perry, D. Miles / Tetrahedron Letters xxx (2016) xxx–xxx
5
Fig. 6. Absorbance spectra of 1 (0.1 mM in 1:1 acetonitrile–water; PBS 5 mM; pH = 7.4) following 1 min irradiation with white light: (a) before sulfide/cyanide addition (black
line); (b) following addition of Bu4NCN (200
L of 0.05 M solution in water, 50 equiv.) and standing in darkness for 2 h (red line); (c) following addition of Na2Sꢂ9H2O (200
of 0.05 M solution in water, 50 equiv.) and standing in darkness for 2 h (blue line). (Inset) Change in absorbance intensity at 418 nm over time (samples placed in darkness):
(a) following addition of Na2Sꢂ9H2O (200 L of 0.05 M solution in water, 50 equiv.) (blue line); (b) following addition of Na2Sꢂ9H2O (100 L of 0.1 M solution in water, 50
equiv.) and Bu4NCN (100 L of 0.1 M solution in water, 50 equiv.) (green line).
l
lL
l
l
l
white light: quantitative determination of [SHꢀ] can be achieved
through ratiometric analysis of 1-SH (286 or 418 nm) and SP-1
(348 nm), as opposed to MC-1 as used previously.
typical cellular concentrations). NitroBIPS suffers from competition
with cyanide; however: (i) cyanide is rarely present in biological
samples; (ii) selectivity for sulfide over cyanide can be established
through simple modulation of the spiro-mero equilibrium.
Although nitroBIPS is an effective sulfide probe in aqueous media
and can be used in 1% aqueous DMSO, its limited water solubility
precludes quantitative sulfide determination in the absence of
organic solvents (though qualitative detection is effective under
these conditions). Future research will seek to identify fully water
soluble analogues and to elucidate the mechanism(s) by which sul-
fide interacts with nitroBIPS.
Previous work has shown that addition of sulfide19 or cyanide21
to merocyanines operates through nucleophilic attack upon the
iminium ion to give clean conversion to the corresponding quater-
nary adduct (Scheme 1). The addition of sulfide to nitroBIPS,
although superficially similar, is considerably less straightforward.
1H and 13C NMR analysis of the sulfide addition product revealed a
complex mixture of products with little useful structural informa-
tion. UV–visible spectroscopy suggests that a major component of
addition is similar to the corresponding cyanide adduct 1-CN
(k418); however, the presence of further absorption peaks corrobo-
rates NMR evidence for alternative reaction pathways. In the
absence of concrete evidence, it is perhaps unhelpful to speculate
upon the outcome of this reaction; however, it is pertinent to note
that in addition to direct attack upon the iminium ion, conjugate
addition of sulfide to MC-1 is plausible: conjugate addition of
water to nitroBIPS derivatives has been observed over extended
reaction times23 and conjugate addition of sulfur-based nucle-
ophiles to structurally similar cyanine dyes has been reported.24–
Acknowledgements
We would like to thank Dr. Mark Wood and Dr. Steve Green for
valuable and insightful discussions and Prof. Matt Whiteman for
providing samples of SIN-1 and glutathione.
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26
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