Self-aggregation of a synthetic zinc chlorophyll derivative possessing a 131-dicyanomethylene group as a light-harvesting antenna model

Article abstract of DOI:10.1016/j.tetlet.2014.03.071

Zinc methyl 3-hydroxymethyl-13¹-dicyanomethylene- pyropheophorbide-a, one of the bacteriochlorophyll-d analogs, was prepared by modifying chlorophyll-a. The semi-synthetic compound self-aggregated in an aqueous Triton X-100 solution to give large oligomers with red-shifted and broadened electronic absorption bands. The J-aggregates were similar to self-aggregates of bacteriochlorophyll-d molecules in natural light-harvesting antennas of green photosynthetic bacteria. The strongly electron-withdrawing dicyanomethylene group was an alternative functional moiety of the hydrogen-bond accepting 13¹-oxo group which had been necessary for such self-aggregation.

Full text of DOI:10.1016/j.tetlet.2014.03.071

Tetrahedron Letters 55 (2014) 2825–2828
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Tetrahedron Letters
journal homepage: www.elsevier.com/locate/tetlet
Self-aggregation of a synthetic zinc chlorophyll derivative possessing
a 131-dicyanomethylene group as a light-harvesting antenna model
⇑
Hitoshi Tamiaki , Masaki Kuno, Michio Kunieda
Graduate School of Life Sciences, Ritsumeikan University, Kusatsu, Shiga 525-8577, Japan
a r t i c l e i n f o
a b s t r a c t
Zinc methyl 3-hydroxymethyl-131-dicyanomethylene-pyropheophorbide-a, one of the bacteriochloro-
phyll-d analogs, was prepared by modifying chlorophyll-a. The semi-synthetic compound self-aggregated
in an aqueous Triton X-100 solution to give large oligomers with red-shifted and broadened electronic
absorption bands. The J-aggregates were similar to self-aggregates of bacteriochlorophyll-d molecules
in natural light-harvesting antennas of green photosynthetic bacteria. The strongly electron-withdrawing
dicyanomethylene group was an alternative functional moiety of the hydrogen-bond accepting 131-oxo
group which had been necessary for such self-aggregation.
Article history:
Received 14 February 2014
Revised 13 March 2014
Accepted 17 March 2014
Available online 21 March 2014
Keywords:
Bacteriochlorophyll
Chlorosome
Ó 2014 Elsevier Ltd. All rights reserved.
J-aggregate
Photosynthesis
Light-harvesting antenna systems are essential for natural
photosynthesis.1 Most of the systems are constructed by specific
interaction of pigments with peptides and some models using
chlorophyll pigments and helical peptides have been already
reported.2 In contrast, self-aggregates of chlorophylls are available
in the main antenna complexes of green photosynthetic bacteria,
called chlorosomes.3 Self-assemblies of chlorosomal chlorophylls
and their model compounds have been reported and are promising
for artificial antenna systems.4 Bacteriochlorophyll(BChl)-d is one
of the naturally occurring chlorosomal chlorophylls (see the left
drawing of Fig. 1)5 and zinc chlorophyll derivatives 4a/4a0 (right
drawing of Fig. 1) were effective for their synthetic models.6,7 Al-
most all the self-aggregative models reported to date are coordin-
atable metal complexes of cyclic tetrapyrroles bearing 31-hydroxy
and 131-oxo groups and the three linearly situated moieties were
specifically interacted to form chlorosomal J-aggregates:
Mꢀ ꢀ ꢀOAHꢀ ꢀ ꢀO@C. Zinc 31-hydroxy-chlorins 4a/4a0 possessing the
131-oxo moiety aggregated in a non-polar organic solvent, an
aqueous micelle solution, and the solid thin film to form large olig-
omers with red-shifted and broadened electronic absorption
bands, but the analog 5a/5a0 lacking the 131-oxo moiety could
not self-aggregate under the same conditions.6,8 In the supramo-
lecular structures of chlorosomal self-aggregates, the 131-oxo
group of a molecule was hydrogen-bonded with the 31-hydroxy
group of another molecule (vide supra). The 131-hydroxylated
analogs including 6a have been reported to be partially effective
Figure 1. Molecular structures of one of the chlorosomal chlorophyll homologs,
farnesylated 8-ethyl-12-methyl-bacteriochlorophyll-d (left), and its synthetic ana-
logs, zinc methyl 31-hydroxy-pyropheophorbide-a derivatives (right).
for the alternative models of chlorosomal chlorophylls due to the
hydrogen-bond accepting ability of the 131-O moiety.9
The central metal of porphyrinoids was coordinated with the
oxygen atom of the 31-hydroxy group to form the chlorosomal
self-aggregates mentioned above. The electron-withdrawing car-
bonyl group at the 13-position enhanced the coordinated ability
of the metals including zinc.10 Therefore, the 13-C@O provides dual
functions for chlorosomal self-aggregation. Here, a dicyanomethyl-
ene group was introduced at the 131-position of 4a to give 1a and
⇑
Corresponding author. Tel.: +81 77 561 2765; fax: +81 77 561 2659.
E-mail address: tamiaki@fc.ritsumei.ac.jp (H. Tamiaki).
http://dx.doi.org/10.1016/j.tetlet.2014.03.071
0040-4039/Ó 2014 Elsevier Ltd. All rights reserved.

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H. Tamiaki et al. / Tetrahedron Letters 55 (2014) 2825–2828
its self-aggregation was examined in an aqueous micelle solution
and the solid film by visible, near infrared, and infrared absorption
as well as circular dichroism (CD) spectroscopies. The dicyano-
methylene moiety is a strongly electron-withdrawing functional
group but has less ability as a hydrogen-bonding acceptor. It is
discussed whether the dicyanomethylene could be an alternative
functional group of the 131-oxo moiety in chlorosomal
chlorophylls.
(v)], Knoevenagel reaction of 131-oxo to dicyanomethylene group
[3b ? 2b, step (i)], and zinc-metallation of 2b to 1b [step (iv)].
When zinc 31-hydroxy-131-dicyanomethylene-chlorin 1a was
dissolved in THF, a bright-green colored solution was obtained.
The diluted THF solution (10 lM) gave an intense absorption band
at 696 nm and four peaks at 455, 436, 386, and 348 nm (see the
blue broken line of Fig. 2A): the former and latter are called Qy
and Soret bands, respectively. The solution showed small CD bands
(see the blue broken line of Fig. 2B), and especially a weak negative
peak was observed at the Qy position. Compared to reported data
of the related compounds,6,11 1a was axially coordinated to a THF
molecule to be a monomeric species in the solution. A THF solution
of 1a containing Triton X-100 was diluted with 99-fold water at
room temperature to give a pale-green colored solution: the final
According to reported procedures,11 the 131-oxo group of
methyl pyropheophorbide-a (3c) prepared by modifying chloro-
phyll-a was transformed into a dicyanomethylene group as in 2c
by Knoevenagel reaction with malononitrile and the 3-vinyl group
of 2c was converted to a formyl group as in 2d by Lemieux–John-
son oxidation [see steps (i) and (ii) in Scheme 1]. The 3-formyl
group of 2d was selectively reduced by tert-butylamine borane
complex6 to give 3-hydroxymethyl-131-dicyanomethylene-chlorin
2a in an excellent yield [93%, step (iii)].12 The resulting free base 2a
was treated with zinc acetate to afford the corresponding zinc
complex 1a in an excellent yield [92%, step (iv)].12 The 3-ethyl ana-
log of 1a as in 1b was produced by the following sequential
steps:12 hydrogenation of 3-vinyl to ethyl group [3c ? 3b, step
concentrations of 1a, THF, and Triton X-100 were 10 lM, 1%
(v/v), and 0.025% (wt/v), respectively. The aqueous solution
showed red-shifted and broadened bands compared with the
monomeric THF solution (Fig. 2A). The Qy band was shifted from
696 to 804 nm and the full width at half maximum increased from
530 to 860 cm–1 (see also Table 1). The red-shift value
D was
1920 cm–1 and the bandwidth was 1.6 times wider. In the Soret
bands, similar changes were obtained. In the aqueous solution,
large CD bands were observed and particularly an intense S-shaped
signal was measured at the red-shifted Qy region.
The spectral changes in 1a were similar to those by chlorosomal
self-aggregation of 4a reported earlier6,13 (see Fig. 3A and Table 1;
D
= 1980 cm–1 and 1.8 times broadening), so 1a self-aggregated in
the aqueous micelle solution to give large oligomers with
p–p
stacking of chlorin chromophores. Zinc 3-ethyl-131-dicyanometh-
ylene-chlorin 1b afforded less red-shifted bands in the aqueous
solution (Fig. 3B), while both 1a and 1b showed almost the same
absorption bands in THF. The
D-value of 1b was estimated to be
190 cm–1 and 10 times smaller than that of 1a. The small but
apparent shift could be due to the environmental effect. Therefore
no chlorosomal aggregation of 1b was observed under the present
conditions. Metal-free form 2a of 1a also showed slight red-shifts
(Fig. 3C) and could not give chlorosomal self-aggregates. Lack of
the 31-hydroxy group or the central zinc metal completely
Scheme 1. Synthesis of zinc methyl 131-dicyanomethylene-pyropheophorbides
1a/b from methyl pyropheophorbide-a (3c): (i) CH2(CN)2, Et3N/THF, reflux; (ii) OsO4,
NaIO4/aq AcOH–THF; (iii) (CH3)3CNH2ꢀBH3/CH2Cl2; (iv) Zn(OAc)2ꢀ2H2O/CHCl3–
pyridine, reflux for 1a and /CH2Cl2–MeOH, rt for 1b; (v) H2, Pd-C/acetone.
Figure 2. Electronic absorption (A) and CD spectra (B) of zinc 3-hydroxymethyl-
131-dicyanomethylene-pyropheophorbide-a (1a) in THF (blue broken line) and an
aqueous 1% (v/v) THF solution containing 0.025% (wt/v) Triton X-100 (red solid
line): [1a] = 10 lM.

H. Tamiaki et al. / Tetrahedron Letters 55 (2014) 2825–2828
2827
Table 1
Electronic absorption maxima k of (zinc) methyl pyropheophorbides in a solutiona and red-shift values
D
of Qy maximab
Compound
k (nm)
D
(cm–1
)
In THF
In aq micellec
Soret
Qy
Soret
Qy
1a [Zn/31-OH/131@C(CN)2]
1b [Zn/31-CH3/131@C(CN)2]
2a [2H/31-OH/131@C(CN)2]
4a [Zn/31-OH/131@O]
436
436
448
424
696 (530)
694 (520)
696 (430)
646 (320)
462
440
455 (sh)
450
804 (860)
703
703
1920
190
150
741 (560)
1980
a
b
c
The values in parentheses show a full width at half maximum (cm–1).
D
In an aqueous solution containing 1% (v/v) THF and 0.025% (wt/v) Triton X-100.
= [1/k(in THF) – 1/k(in aq micelle)] ꢁ 107.
Figure 4. Electronic absorption spectra of (zinc) methyl pyropheophorbides 1a (red
solid line), 1b (blue broken line), and 2a (black dotted line) in solid thin films. The
spectra were normalized at the Qy peaks.
Figure 3. Electronic absorption spectra of (zinc) methyl pyropheophorbides 4a (A),
1b (B), and 2a (C) in THF (blue broken line) and an aqueous 1% (v/v) THF solution
containing 0.025% (wt/v) Triton X-100 (red solid line): [4a] = [1b] = [2a] = 10 lM.
suppressed the formation of large self-aggregates. Coordination
of the 31-OH to Zn in a supramolecule was necessary for the
chlorosomal self-aggregation. It was reported that hydrogen-bond
of the 31-OH with 131@O was an additional requisite for chlorosomal
aggregation of 4a and specific bonds of Znꢀ ꢀ ꢀOAHꢀ ꢀ ꢀO@C were
Figure 5. Infrared absorption spectra of (zinc) methyl pyropheophorbides 1a (red
solid line), 1b (blue broken line), and 2a (black dotted line) in solid thin films: in
vibrational regions of hydroxy (A), cyano (B), and ester carbonyl groups (C). The
spectra were normalized at the cyano peaks and the spectra in (A) were enlarged
three times. The broad bands at around 3500 cm–1 may be ascribable to moisture in
the solid films. An about 60-cm–1 lower shift of the 31-O–H band in the top to
bottom spectra of (A) might be ascribable to the coordination of OH to Zn in (1a)n.
conserved.6,13 In the present system, such
a hydrogen-bond
seemed to be unnecessary for the chlorosomal aggregation.
In the solid thin film, each 131-dicyanomethylene-chlorin 1a,
1b, or 2a gave a similar electronic absorption spectrum as in aque-
ous micelle solution (Fig. 4), so 1a self-aggregated in the solid
states but neither 1b nor 2a afforded chlorosomal self-aggregates.
In all three solids, almost the same vibrational bands of C„N
2218 cm–1 (2a). Their ester carbonyl stretching peaks in the solid
states were also situated at almost the same position (Fig. 5C):
stretching were measured as shown in Fig. 5B:
(for 1a), 2215 (for 1b), and 2217 cm–1 (for 2a). The bands were con-
sistent with those in THF: (C„N) = 2215 (1a), 2215 (1b), and
m(C„N) = 2218
m
(C@O) = 1732 (1a), 1737 (1b), and 1735 cm–1 (2a). A relatively
sharp O–H vibrational band was observed at 3340 cm–1 in the solid
m

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H. Tamiaki et al. / Tetrahedron Letters 55 (2014) 2825–2828
coordination. A strongly electron-withdrawing dicyanomethylene
group at the 131-position was recognized to be an alternative func-
tional moiety to the oxo moiety used usually. It was reported that
the 31-methoxy analogs of 4a possessing long chains at the 17-pro-
pionate residue self-aggregated in a specific environment to give
models of chlorosomal aggregates and hydrogen bonding was not
always necessary for such J-aggregation.14 The present system is
consistent with the previous ones utilizing no hydrogen-bond
donating moiety at the 31-position, and 1a was the first model of
chlorosomal chlorophylls which no longer performed hydrogen-
bond accepting role at the 131-position.
Acknowledgements
This work was partially supported by Grants-in-Aid for
Scientific Research (A) (No. 22245030) as well as on Innovative
Areas ‘Artificial Photosynthesis (AnApple)’ (No. 24107002) from
the Japan Society for the Promotion of Science (JSPS).
Supplementary data
Supplementary data (synthesis of Chl derivatives 1/2a,b and
their spectral data as well as preparation procedures of aqueous
Chl solutions) associated with this article can be found, in the
online version, at http://dx.doi.org/10.1016/j.tetlet.2014.03.071.
Figure 6. Electronic absorption spectral changes of zinc methyl 3-hydroxymethyl-
pyropheophorbides 1a (A) and 4a (B) in an aqueous 1% (v/v) THF by addition of
Triton X-100: [1a] = [4a] = 10 lM and [Triton X-100] = 0.025 (red solid line), 0.1.
0.2, 0.4, 0.6, 0.8 (black to gray broken lines), and 1.0% (wt/v) (blue solid line).
References and notes
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firmed in self-aggregates of 1a.
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Deaggregation of self-aggregates of 1a in an aqueous micelle
solution was examined by addition of Triton X-100. Successive
addition of Triton X-100 to the aqueous micelle solution gradually
decreased the Qy peak of self-aggregated 1a at 804 nm and con-
comitantly exposed its monomeric Qy band at 706 nm (Fig 6A).
At 1.0% (wt/v) concentration of Triton X-100, the aggregated Qy
peak was primary and its monomeric peak was less intense. In con-
trast, self-aggregated 4a completely changed to the monomeric
species at the same concentration (Fig. 6B). In spite of the absence
of a hydrogen-bond in self-aggregated 1a, a stronger aggregation of
1a was observed than of 4a. This was ascribable to the stronger
coordination of 31-O to Zn and tighter
p-stacking of chlorin
chromophores, since the strongly electron-withdrawing 131-dicya-
nomethylene group produced a more electron-deficient zinc site
and further extended
a p-conjugated system. Its strongly
electron-withdrawing effect may reinforce polarization of the
macrocycle, and the polarization may facilitate stacking of the
macrocycles.
12. Synthetic procedures of all the new compounds 1a/b and 2a/b and their
spectral data are shown in electronic supporting material.
In conclusion, zinc 3-hydroxymethyl-131-dicyanomethylene-
chlorophyll derivative 1a self-aggregated in a J-type fashion to give
chlorosomal self-aggregates inside an aqueous micelle. The
synthetic compound was not hydrogen-bonded in the J-aggregates,
which had been a requisite for chlorosomal self-aggregation, but
did produce more tightly stacked supramolecules with powerful
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