Self-aggregation of synthetic zinc 3-hydroxymethyl-purpurin-18 and N-hexylimide methyl esters in an aqueous solution as models of green photosynthetic bacterial chlorosomes

Article abstract of DOI:10.1246/cl.2005.1344

Zinc 3¹-hydroxy-13¹-oxo-chlorins possessing a six-membered exo-ring attached at the 13- and 15-positions were prepared by modifying purpurin-18. These synthetic anhydride and imide self-aggregated in an aqueous THF solution to give large oligomers (J-aggregates) similarly with the corresponding natural and artificial chlorophylls possessing a five-membered E-ring. Copyright

Full text of DOI:10.1246/cl.2005.1344

1
344
Chemistry Letters Vol.34, No.10 (2005)
Self-aggregation of Synthetic Zinc 3-Hydroxymethyl-purpurin-18 and N-Hexylimide Methyl
Esters in an Aqueous Solution as Models of Green Photosynthetic Bacterial Chlorosomes
ꢀ
y
y
Hitoshi Tamiaki, Yasuhide Shimamura, Hideaki Yoshimura, Suresh K. Pandey, and Ravindra K. Pandey
Department of Bioscience and Biotechnology, Faculty of Science and Engineering, Ritsumeikan University, Kusatsu, Shiga 525-8577
y
PTD Center, Roswell Park Cancer Institute, Buffalo, New York 14263, U. S. A.
(Received June 23, 2005; CL-050806)
1
1
9
Zinc 3 -hydroxy-13 -oxo-chlorins possessing a six-mem-
bered exo-ring attached at the 13- and 15-positions were pre-
pared by modifying purpurin-18. These synthetic anhydride
and imide self-aggregated in an aqueous THF solution to give
large oligomers (J-aggregates) similarly with the corresponding
natural and artificial chlorophylls possessing a five-membered
E-ring.
Purpurin-18 was afforded by air-oxidation of pheophor-
bide-a prepared from Chl-a (see Supporting Information
1
0
for the present synthetic route). After methyl esterification of
2
11
the 17 -carboxy group, the 3-vinyl group was oxidatively
2
1
cleaved, the resulting 3-formyl group was selectively re-
1
2
12
duced, and then zinc-metallation gave desired zinc 3-hy-
1
3
droxymethyl-purpurin-18 methyl ester 1. The anhydride moie-
ty of purpurin-18 methyl ester was transformed to the corre-
1
1
sponding N-hexylimide and the imide was modified similarly
as the above synthesis of 1 to yield zinc 3-hydroxymethyl-pur-
purin-N-hexylimide methyl ester 2. Reference compound 3,
zinc 3-hydroxymethyl-pyropheophorbide-a methyl ester was
Self-assemblies of ꢀ-conjugated moieties attract much at-
tention from the viewpoints of chemistry, biology, and material
science. Such assemblies are observed in various natural sys-
tems, especially (bacterio)chlorophylls [= (B)Chls] stacked in
photosynthetic organisms. X-ray crystallographic structure anal-
yses of some (B)Chl-containing proteins have clearly shown ꢀ–
ꢀ stacking of (B)Chls. On the other hand, self-aggregates of
chlorophyllous pigments are found in main light-harvesting an-
1
3
1
4
prepared according to reported procedures.
In THF, anhydride 1 formed monomeric 5-coordinated zinc
species with a THF molecule as an axial ligand to give sharp and
intense Qy and Soret bands at 665 and 421 nm, respectively (bro-
ken line of Figure 2A upper). The Qy peak was shifted to a 9-nm
longer wavelength than that of keto-type 3 (646 nm, see Table 1),
which was due to the substituent effect of the E-ring on the Qy
axis. Such a THF solution containing monomeric 1 was diluted
with water and broad absorption bands appeared in the red-shift-
ed regions. In 6% (v/v) THF–water, a Qy maximum was ob-
2
3
tennas of green photosynthetic bacteria (= chlorosomes). The
1
1
composite Chls are characterized by 3 -hydroxy and 13 -oxo
groups as shown in the left drawing of Figure 1. As one of the
1
1
model pigments, zinc 3 -hydroxy-13 -oxo-chlorin 3 (middle
drawing of Figure 1) was reported and self-aggregated similarly
under various conditions. All natural and artificial chlorosomal
Chls had a five-membered exo-ring (E-ring) and a keto (or for-
4
14
served at 753 nm (solid line of Figure 2A upper), which was
ꢁ1
a 1760 cm bathochromic shift compared with the monomeric
(see Table 1). In the red-shifted regions, intense CD bands were
recorded, while the monomeric 1 gave smaller CD peaks
(Figure 2A lower). These changes (broadening and red-shift in
electronic absorption bands and enlargement in CD bands) were
observed in natural chlorosomes and their artificial models,3 in-
dicating that 1 self-aggregated in the aqueous solution to form
similar large oligomers (J-aggregates). Moreover, the shape of
broadened and red-shifted Qy band in self-aggregates of 1 and
the reverse S-shape of the pronounced CD band at the red-shifted
Qy region are almost the same as those in 3 (see Supporting In-
formation), and the red-shift value in 1 is comparable to that of 3
myl) carbonyl group on the Qy axis (N21–N23) has been requi-
5
site for chlorosomal self-aggregation so far. Here, we report the
1
1
synthesis of zinc 3 -hydroxy-13 -oxo-chlorins 1 and 2 (right
drawing of Figure 1) where the 15-methylene group of 3 was for-
mally substituted with –COO– and –CON(C6H13)–, respective-
ly, and chlorosome-like self-aggregation of synthetic anhydride
and imide 2 possessing a six-membered exo-ring in an aqueous
solution. An aqueous solution containing 6% (v/v) THF was re-
ported to be one of the effective environments for self-aggrega-
,4
1
6
–8
tion of chlorosomal Chls and was used in this study.
ꢁ1
OH
OH
OH
(1780 cm ). In the self-aggregation, the anhydride moiety in the
E-ring of 1 functioned as the keto-carbonyl moiety in the E-ring
of chlorosomal Chls and their model pigments including BChl-d
and 3. The 13-carbonyl group in the anhydride moiety on the Qy
31
31
*
1
3
3
N21 22N
N
N
N
N
N
N
N
N
Mg
Zn
Zn
ꢁ1
Table 1. Qy maxima ꢁmax (nm) and the red-shifts ꢀ (cm ) by
self-aggregation
N24 23N
17 15
1
5
13
a
E
31
E
131
1
172
E
X
ꢁ
max
32
1
O
O
ꢀb
O
O
THF
6%(v/v)THF–water
COO-farnesyl
COOCH3
COOMe
1
2
(X =O)
(X = NC H13)
BChl-d
3
1 (anhydride)
2 (imide)
665
671
646
753
729
730
1760
1190
1780
6
3
(ketone)
Figure 1. Molecular structures of a naturally occurring chloro-
somal Chl, one of BChl-d homologs (left), its synthetic model 3
aIn ca. 5 mM. ꢀ ¼ ½1=ꢁmax(THF) ꢁ 1=ꢁmaxð6%THFꢁ
b
7
(
middle), and 1/2 (right).
waterÞꢂ ꢃ 10 .
Copyright ꢀ 2005 The Chemical Society of Japan

Chemistry Letters Vol.34, No.10 (2005)
1345
2
self-aggregates of 13 -methoxycarbonylated 3 (zinc 3-hydroxy-
methyl-pheophorbide-a methyl ester) gave a less red-shifted Qy
ꢁ
1
6
1
band at 697 nm (ꢀ ¼ 1230 cm ). It is noteworthy that 3 -
methylated 3 (zinc bacteriopheophorbide-d methyl ester) gave
a similar red-shift value (1200 cm ) by its self-aggregation.8
In self-aggregative pigments, therefore, six-membered anhy-
dride and imide rings fused at 13- and 15-positions could be al-
ternated for the five-membered E-ring possessing a keto-carbon-
yl group as seen in all natural chlorosomal Chls and their model
pigments; anhydride and imide carbonyl groups as well as keto-
C=O are effective for chlorosomal self-aggregation.
ꢁ
1
1
1
As reported earlier, anhydride- and imide-type Chls as in 1
and 2 were more stable in their monomeric states than the corre-
sponding keto-type as in 3, while all the self-aggregates of 1–3
were fairly stable even in an aerated solution under irradiation
with visible light. Such chemical stabilities of anhydrides and
imides are advantageous for preparation of self-aggregative
pigments and their further modification. The hexyl group on
the imide nitrogen of 2 slightly suppressed the self-aggregation
but could still construct a similar large oligomer. Any functional
groups can be easily substituted on the nitrogen as in 21
1,16
and
various functions including energy-donating and accepting
groups would be introduced to self-aggregates of imides. Prepa-
ration of such functional supramolecules is now in progress.
This work was partially supported by Grant-in-Aid for
Scientific Research (No. 17029065) on Priority Areas (417) from
MEXT and for Scientific Research (B) (No. 15350107) from
JSPS, by ‘‘Academic Frontier’’ Project for Private Universities:
matching fund subsidy from MEXT, 2004–2008, and by a
NIH grant (CA55792).
References and Notes
1
F. J. M. Hoeben, P. Johkheijm, E. W. Meijer, and A. P. H. J. Schenning,
Chem. Rev., 105, 1869 (2005).
Figure 2. Electronic (upper) and CD absorption spectra (lower)
of ca. 5 mM solutions of 1 (A) and 2 (B) in THF (broken) and 6%
2
3
T. Oba and H. Tamiaki, Bioorg. Med. Chem., 13, (2005), in press.
H. Tamiaki, Coord. Chem. Rev., 148, 183 (1996); J. M. Olson, Photo-
chem. Photobiol., 67, 61 (1998).
(
v/v) THF–water (solid).
axis would hydrogen-bond intramolecularly with zinc-coordi-
1
4
H. Tamiaki, M. Amakawa, Y. Shimono, R. Tanikaga, A. R. Holzwarth,
and K. Schaffner, Photochem. Photobiol., 63, 92 (1996).
S. Yagai, T. Miyatake, and H. Tamiaki, J. Org. Chem., 67, 49 (2002).
T. Oba and H. Tamiaki, Photosynth. Res., 61, 23 (1999).
H. Tamiaki, M. Kubo, and T. Oba, Tetrahedron, 56, 6245 (2000).
S. Sasaki and H. Tamiaki, Bull. Chem. Soc. Jpn., 77, 797 (2004).
A. S. Brandis, A. N. Kozyrev, and A. F. Mironov, Tetrahedron, 48,
nated 3 -hydroxy group to form highly ordered supramolecules
3
,4
as well as the keto-carbonyl groups did. The 15-carbonyl
group of 1 parallel to the Qx axis (N22–N24) would not disturb
the self-aggregation, which is consistent with the fact that no
5
6
7
8
9
7-formyl group could perturb self-aggregation in natural and
artificial systems.
7,15
6
485 (1992).
Imide 2 was monomeric in THF and gave a sharp 671-nm
Qy maximum (broken line of Figure 2B upper), which was shift-
ed to a longer wavelength than those of 1 and 3. In 6% (v/v)
THF–water, 2 also self-aggregated to afford a broadened and
1
1
0
1
N. Kosaka and H. Tamiaki, Eur. J. Org. Chem., 2004, 2325.
G. Zfeng, W. R. Potter, S. H. Camacho, J. R. Missert, G. Wang,
D. A. Bellnier, B. W. Henderson, M. A. J. Rodgers, T. J. Dougherty,
and R. K. Pandey, J. Med. Chem., 44, 1540 (2001).
1
4
red-shifted Qy band at 729 nm and a reverse S-shaped CD
couplet (solid lines of Figure 2B). The Qy peak position in
self-aggregates of 2 was comparable to that of 3 and shifted to
a 24-nm shorter wavelength than that of 1. The value in the
12 H. Tamiaki, S. Miyata, Y. Kureishi, and R. Tanikaga, Tetrahedron, 52,
2421 (1996).
1
All zinc complexes 1–3 were purified with HPLC and identified from
1
3
1
visible absorption, H NMR and MS spectra. See Supporting Informa-
tion for spectral data of 1 and 2.
ꢁ1
red-shift by self-aggregation of 2 was 1190 cm and smaller
than those of 1 and 3. Although supramolecule-forming motifs
1
4
In 6%(v/v)THF–water, ca. 1 mM solutions of 1 and 2 gave the same
shapes of electronic absorption bands as in the solid lines of
Figures 2A and 2B upper (ca. 5 mM), respectively.
H. Tamiaki, Photochem. Photobiol. Sci., 4, (2005), in press.
Substitution at the 7- and 8-positions and the 17-propionate on the Qx
axis of a (bacterio)chlorin moiety were also useful for such modifica-
tion; see Refs. 15 and 17.
3
,4
(
13-C=OꢄꢄꢄH–OꢄꢄꢄZn and ꢀ–ꢀ interaction) would be the same
1
1
5
6
among self-aggregates of 1–3, imide 2 slightly disturbed the in-
termolecular interaction to give a less red-shifted Qy band in
self-aggregates than anhydride 1 and keto 3. The slight suppres-
sion in 2 was ascribed to the steric interference of the hexyl
group on the imide nitrogen neighbor to the interactive 13-car-
bonyl group. This interpretation was consistent with the fact that
1
7
T. Miyatake, H. Tamiaki, A. R. Holzwarth, and K. Schaffner, Photo-
chem. Photobiol., 69, 448 (1999); T. Miyatake, H. Tamiaki, M.
Fujiwara, and T. Matsushita, Bioorg. Med. Chem., 12, 2173 (2004).
Published on the web (Advance View) September 10, 2005; DOI 10.1246/cl.2005.1344