Substitution effects in the A- and B-rings of the chlorin macrocycle on demetalation properties of zinc chlorophyll derivatives

Article abstract of DOI:10.1021/jp1117486

Effects of peripheral substituents in the A- and B-rings of the chlorin macrocycle on demetalation of zinc chlorophyll derivatives were examined. The demetalation rate constants of zinc 8-formyl-chlorin (1) were comparable to those of zinc 3-formyl-chlorin (2). Both 1 and 2 exhibited significantly slower demetalation kinetics than the corresponding zinc chlorin 3, which had no formyl group. Comparison of demetalation kinetics between zinc 3-ethyl-chlorin (3) and zinc 3-vinyl-chlorin (4) indicated that the substitution at the 3-position of the chlorin macrocycle from a vinyl to an ethyl group accelerated removal of the central zinc. Activation energies of demetalation of zinc chlorins 1, 2, and 5 possessing a formyl group in the A- or B-ring of the chlorin macrocycle were larger than those of zinc chlorins 3 and 4 lacking a formyl group. These results indicate that the formyl groups in the A- or B-ring provide tolerance to demetalation of chlorin molecules due to their electron-withdrawing effects.

Full text of DOI:10.1021/jp1117486

ARTICLE
pubs.acs.org/JPCB
Substitution Effects in the A- and B-Rings of the Chlorin Macrocycle on
Demetalation Properties of Zinc Chlorophyll Derivatives
Yuki Hirai,† Shin-ichi Sasaki,‡,§ Hitoshi Tamiaki,‡ Shigenori Kashimura,† and Yoshitaka Saga*,†
†Department of Chemistry, Faculty of Science and Engineering, Kinki University, Higashi-Osaka, Osaka 577-8502, Japan
‡Department of Bioscience and Biotechnology, Faculty of Science and Engineering, Ritsumeikan University, Kusatsu, Shiga 525-8577,
Japan
§Nagahama Institute of Bio-Science and Technology, Nagahama, Shiga 526-0829, Japan
ABSTRACT: Effects of peripheral substituents in the A- and B-rings of the
chlorin macrocycle on demetalation of zinc chlorophyll derivatives were
examined. The demetalation rate constants of zinc 8-formyl-chlorin (1)
were comparable to those of zinc 3-formyl-chlorin (2). Both 1 and 2
exhibited significantly slower demetalation kinetics than the corresponding
zinc chlorin 3, which had no formyl group. Comparison of demetalation
kinetics between zinc 3-ethyl-chlorin (3) and zinc 3-vinyl-chlorin (4)
indicated that the substitution at the 3-position of the chlorin macrocycle
from a vinyl to an ethyl group accelerated removal of the central zinc. Activation energies of demetalation of zinc chlorins 1, 2, and 5
possessing a formyl group in the A- or B-ring of the chlorin macrocycle were larger than those of zinc chlorins 3 and 4 lacking a
formyl group. These results indicate that the formyl groups in the A- or B-ring provide tolerance to demetalation of chlorin
molecules due to their electron-withdrawing effects.
’ INTRODUCTION
Chl degradation10-16 and formation of (B)Phe molecules that
function in PS II-type reaction centers. Therefore, demetalation of
chlorophyllous pigments is important, and the physicochemical
properties of demetalation of natural Chls and synthetic metallo-
chlorins have been extensively investigated.17-30
Chlorophyll (Chl) molecules are major photosynthetic pig-
ments in nature. The photofunctional cores of Chls are tetra-
pyrrole macrocycles, and peripheral substituents of the cyclic
tetrapyrrole moieties provide their structural diversity.1
Figure 1A shows molecular structures of naturally occurring
Chls in oxygenic photosynthetic organisms. The difference of
molecular structures between Chls a and b is the substituent at
the 7-position of the chlorin macrocycle: the substituents are
methyl and formyl groups, respectively. The 7-formyl group of
Chl b causes bathochromic and hypsochromic shifts of Soret and
Qy absorption bands, and Chl b can capture photons that are
scarcely absorbed by Chl a in photosynthetic light-harvesting
complexes. Chlorophyll d, a major photosynthetic pigment in a
cyanobacterium Acaryochloris (A.) marina, has a formyl group at
the 3-position (Figure 1A), resulting in the large red shift of the
Qy absorption band of Chl d compared with that of Chl a. Such a
spectral property enables A. marina to use longer wavelength
light for its photosynthetic activity. Recently, a new Chl posses-
sing a formyl group at the 2-position, which was designated to
Chl f (Figure 1A), was reported by Chen et al.2 Qy absorption and
fluorescence emission bands of Chl f are considerably red-shifted
compared with other Chls.
Some of these works indicated that natural Chls possessing a
formyl group, namely Chl b, Chl d, and BChl e, had tolerance to
removal of central magnesium due to the electron-withdrawing
effect of the formyl group.17-19,23,26-28,30 Recently, we showed
that 7-formylated Chl b exhibited higher resistance to demetala-
tion than 3-formylated Chl d.28 Such difference might be
rationalized in terms of the π-electron densities of the chlorin
macrocycle, which are reflected in the redox potentials of Chls a,
b, and d.23,28,31 Chl b, whose oxidation potential is most
positive,32 exhibits the slowest demetalation kinetics among
the three Chls. In contrast, Chl a, whose oxidation potential is
most negative,32 shows the fastest pheophytinization. Systematic
studies of metallochlorins possessing a formyl group in the A-
and B-rings of the chlorin macrocycle will be necessary to unravel
demetalation properties of formylated chlorins thoroughly. Here
we examine demetalation kinetics of Zn 8-formyl-chlorin 1 (zinc
methyl 8-deethyl-8-formyl-mesopyropheophorbide a) and Zn
3-formyl-chlorin (2) (zinc methyl pyropheophorbide d) as
shown in Figure 1B and compare these properties with those
of Zn chlorin 3 (zinc methyl mesopyropheophorbide a), as well as
Zn chlorins 4(zinc methyl pyropheophorbide a) and5(zincmethyl
pyropheophorbide b) in our previous report.30 8-Formyl-chlorins
Almost all naturally occurring Chls have central magnesium in the
cyclic tetrapyrroles,1 except for zinc bacteriochlorophyll (BChl) a in
Acidiphilium rubrum.3-5 Demetalation compounds of Chls and
BChls, namely pheophytin(Phe)s and bacteriopheophytin(BPhe)s,
respectively, function as the primary electron acceptors in photo-
system (PS) II-type reaction centers.6-9 Removal of central metals
from chlorophyllous pigments is a key reaction in the early process of
Received: December 10, 2010
Revised:
February 9, 2011
Published: February 28, 2011
r
2011 American Chemical Society
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ARTICLE
Figure 1. Molecular structures of Chls a, b, d, and f (A) and synthetic Zn
chlorins 1-5 (B).
have been synthesized as analogues of 7-formyl-BChls such as BChls
e and f, and are appropriate to examine the effect of formyl groups in
the B-ring on visible absorption spectra and self-aggregation.33,34
3-Formyl- and 7-formyl-chlorins are good model compounds of
Chls d and b, respectively. Comparison of Zn chlorins 1 and 2 is
appropriate to study the substituent effects of formyl groups
conjugated to the A- and B-rings of the chlorin macrocycle on
demetalation in detail without other effects, since both are regioi-
somers (1, 3-ethyl-8-formyl; 2, 3-formyl-8-ethyl). In the present
study, we targeted demetalation properties of these chlorins to
investigate the effects of formyl groups directly conjugated to the
A- and B-rings on removal of the central zinc metal.
Figure 2. Spectral changes of Zn chlorins 1 (A), 2 (B), and 3 (C) in
acetone/water (3/1, vol/vol) at the proton concentrations of 3.75 ꢀ
10-2, 3.75 ꢀ 10-2, and 6.25 ꢀ 10-3 M at 25 ꢀC. 1: Spectra from 0 to 16
h at 30 min intervals. 2: Spectra from 0 to 15 h at 30 min intervals. 3:
Spectra from 0 to 150 min at 5 min intervals. Arrows show the direction
of the spectral changes.
’ EXPERIMENTAL SECTION
Apparatus. Visible absorption spectra were measured using a
Shimadzu UV-2450 spectrophotometer, where the reaction
temperatures were regulated with a Shimadzu thermoelectric
temperature-controlled cell holder TCC-240A. High-perfor-
mance liquid chromatography (HPLC) was carried out using a
Shimadzu LC-20AT pump and SPD-M20A or SPD-20A
detectors.
acetone/water (3/1, vol/vol) at the proton concentration of 3.75
ꢀ 10-2, 3.75 ꢀ 10-2, and 6.25 ꢀ 10-3 M, respectively, at 25 ꢀC.
Zn chlorin 1 exhibited intense Soret and Qy bands at 450 and
660 nm, respectively, before demetalation. The Soret absorption
band gradually disappeared under the acidic condition and a new
peak characteristic of the free-base form of 1 appeared at 432 nm.
Small absorption bands of 1 in the range between 500 and
600 nm were also gradually changed, and the isosbestic points
could be observed at 441, 478, 543, 586, 595, 608, 658, and
662 nm. The Qy peak position of 1 was not shifted, and the Qy
bandwidth became sharp in the demetalation process. In deme-
talation of Zn chlorin 2, Soret and Qy absorption bands at 450
and 688 nm, respectively, decreased with an appearance of new
bands of the free-base form at 427 and 692 nm. The isosbestic
points were also observed at 439, 479, and 572 nm through the
demetalation reaction of 2. In the case of demetalation of Zn
chlorin 3, Soret and Qy absorption bands at 424 and 648 nm,
respectively, decreased with the appearance of new bands at 407
and 655 nm, which were ascribed to a demetalation product of 3.
The isosbestic points were positioned at 416, 447, 551, and
655 nm through the demetalation process.
Materials. Zn chlorins 1-3 were synthesized according to
previous works33-38 and were purified on a reverse-phase HPLC
column 5C18-AR-II (10 mm i.d. ꢀ 250 mm, Nacalai Tesque)
with methanol at a flow rate of 1.0 mL min-1
.
Measurements of Demetalation Processes. Demetalation
reaction was done in essentially the same procedure as previous
works.22-30 Soret peak absorbances of Zn chlorins 1-3 were
adjusted to 1.0 in 3.0 mL of acetone and the solution was mixed
with 975 μL of distilled water. Twenty-five μL of 6.0 M aqueous
hydrochloric acid was added to the solution and mixed immedi-
ately, and Soret peak absorbance was monitored in measure-
ments of demetalation kinetics. Spectral changes of 3
(Figure 2C) were measured by changing the concentration of
the aqueous hydrochloric acid from 6.0 to 1.0 M.
’ RESULTS
Demetalation Kinetics. Soret peak positions of Zn chlorins
1-3 were clearly different from those of the corresponding free-
base forms. Therefore, demetalation kinetics of these Zn chlorins
Spectral Changes through Demetalation. Figure 2 shows
spectral changes through demetalation of Zn chlorins 1-3 in
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ARTICLE
Figure 3. Kinetic plots for demetalation of Zn chlorins 1 (open circles),
2 (open triangles), and 3 (open squares) in acetone/water (3/1, vol/
vol) at the proton concentration of 3.75 ꢀ 10-2 M at 25 ꢀC. Absorbance
changes were monitored at 450, 450, and 424 nm for 1, 2, and 3,
respectively. A0, A, and A¥ are Soret absorbances of 1-3 at the onset of
measurement, at time t, at the complete demetalation, respectively.
Inset: magnified kinetic plot of 3.
can be quantitatively analyzed by monitoring absorbance
changes at Soret peak positions of the Zn complexes. Figure 3
depicts the time dependency of Soret peak absorbances of 1-3
through demetalation at 25 ꢀC. The logarithms of the Soret
absorbances of 1-3 exhibited linear time dependence, indicating
that the demetalation reactions of 1-3 could be regarded as
pseudo-first-order reactions. This is in line with the reaction
conditions under which the proton concentration (3.75 ꢀ 10-2
M) was much higher than that of Zn chlorins (<10-5 M).22-30
Figure 3 clearly demonstrates that removal of central zinc from 1
and 2, which possessed the 8-formyl and the 3-formyl group,
respectively, was significantly slower than that from 3 possessing
no formyl group.
Figure 4. Arrhenius plots over temperature range of 15-35 ꢀC for
demetalation reaction of Zn chlorins 1 (open circles), 2 (open triangles),
and 3 (open squares) in acetone/water (3/1, vol/vol) at the proton
concentration of 3.75 ꢀ 10-2 M.
ln k ¼ - ðE=RTÞ þ B
ð2Þ
where R is the gas constant. The Arrhenius plots in Figure 4 gave
E-values of 99, 99, and 81 kJ mol-1 for 1-3, respectively. The
difference of the activation energies between 1 and 3 was 18 kJ
mol-1, which was the same as that between 2 and 3. These
indicated that Zn chlorins possessing a formyl group in the A- or
B-ring had higher activation energies of demetalation reaction
than that of the compound lacking a formyl group.
Demetalation rate constants, k, were obtained by fitting the
time courses of Soret peak absorbances as shown in Figure 3 to
the following kinetic equation
’ DISCUSSION
ln½ðA - A¥Þ=ðA0 - A¥Þꢁ ¼ - kt
ð1Þ
The present study indicates that regioisomeric Zn chlorins 1
and 2 possessing a formyl group at the 3- or 8-position,
respectively, exhibited significantly slower demetalation kinetics
than the reference compound 3 lacking a formyl group. Effects of
substituents in the A- and B-rings of the chlorin macrocycle on
removal of central zinc are discussed as follows, based on the
present results and the previous report on 4 (zinc methyl
pyropheophorbide a) and 5 (zinc methyl pyropheophorbide
b).30
Effect of 3-Ethyl and 3-Vinyl Groups. First, the 3-ethyl and
vinyl effects on demetalation kinetics should be discussed to
clearly understand substitution effects of formyl groups in chlorin
molecules. Comparison of demetalation kinetics between Zn
chlorins 3 and 4 revealed that transformation of the 3-ethyl to
3-vinyl group decreased the demetalation rate constants (k(4)/
k(3) = 1.5 ꢀ 10-1 at 25 ꢀC) . This would originate from the
difference of electronegativity between a vinyl group and an ethyl
group.39 The effect of the 3-vinyl group on demetalation of
chlorophyllous pigments was first clarified in the present study,
and should be taken into account for unraveling demetalation
properties of cyclic tetrapyrrole molecules including natural Chls.
We previously reported that demetalation kinetics of Chl b
possessing the 7-formyl group was slower than that of Chl d
possessing the 3-formyl group (k(Chl b)/k(Chl d) = 1.8 ꢀ 10-1
at the proton concentration of 1.2 ꢀ 10-3 M at 25 ꢀC), and this
difference was interpreted to be mainly due to the substitution
where A0, A, and A¥ are Soret peak absorbances of Zn chlorins
1-3 at the onset of measurements, at time t, and the complete
demetalation, respectively.22-30 The k-values of 1-3 were
determined to be 3.2 ꢀ 10-3, 3.8 ꢀ 10-3, and 2.2 min-1
,
respectively, in aqueous acetone at the proton concentration of
3.75 ꢀ 10-2 M at 25 ꢀC. These values were the averages of more
than three independent measurements, and the standard devia-
tions were 3.0, 1.6, and 2.9% of the average values for 1-3,
respectively.
The averages of k-values of 1 and 2 were 690- and 580-fold
smaller than that of 3, respectively. Comparison of the k-values
between regioisomers 1 and 2 indicated that the 8-formyl group
provided slightly higher resistance to demetalation than did the
3-formyl group.
Temperature Dependence of Demetalation Rate Con-
stants. Demetalation rate constants of Zn chlorins 1-3 were
measured at 15, 25, and 35 ꢀC, where measurements at each
temperature were carried out more than three times. Demetala-
tion rate constants of 1-3 became small with a decrease of the
reaction temperature. Figure 4 shows Arrhenius plots of the
averaged k-values of 1-3 in the temperature range between 15
and 35 ꢀC. Activation energies, E, of demetalation were estimated
by fitting the temperature-dependent k-values to the following
Arrhenius equation
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ARTICLE
Table 1. Summary of Demetalation Properties of Zn Chlorins 1-5 in Acetone/Water (3/1, vol/vol) at the Proton Concentration
of 3.75 ꢀ 10-2 M
compd
R3
R7
R8
rate const at 25 ꢀC k/min-1
activation energy E/kJ mol-1
1
2
3
4
5
CH2CH3
CHO
CH3
CH3
CH3
CH3
CHO
CHO
3.2 ꢀ 10-3
3.8 ꢀ 10-3
2.2
99
99
81
84
96
this work
this work
this work
ref 30
CH2CH3
CH2CH3
CH2CH3
CH2CH3
CH2CH3
CHdCH2
CHdCH2
3.4 ꢀ 10-1
7.9 ꢀ 10-4
ref 30
effects of the 3-formyl and 7-formyl groups in the chlorin
macrocycle.28 However, the effect of the 3-vinyl group of Chl b
cannot be ruled out in discussing the difference of demetalation
properties between Chls b and d. The ratio of demetalation
constants of Chl b to Chl d, k(Chl b)/k(Chl d), was close to that
of 4 to 3, k(4)/k(3), suggesting that the 3-vinyl effect was
concerned in slower demetalation kinetics of Chl b than Chl d.
Effect of 7-Formyl and 8-Formyl Groups. Our present and
previous studies26-28,30 indicate that both the 7- and 8-formyl
groups provide resistance to demetalation of chlorin molecules.
The ratio of demetalation rate constants of 7-formyl-chlorin 5 to
7-methyl-chlorin 4, k(5)/k(4), is 2.3 ꢀ 10-3, whereas the ratio of
The activation energy of demetalation of 1 (99 kJ mol-1) was
similar to the reported value of 5 (96 kJ mol-1).30 These suggest
that effects of the 8-formyl group on demetalation properties are
analogous to those of the 7-formyl group. Electron-withdrawing
properties of the formyl groups in the B-ring would result in
resistance of demetalation of chlorin molecules in a similar
manner.
withdrawing 3-, 7-, and 8-formyl groups of chlorin molecules
had essentially similar effects on removal of central metal from
the chlorin macrocycle, although the formyl groups in the B-ring
might have a slightly larger effect than that in the A-ring.
’ AUTHOR INFORMATION
Corresponding Author
*Phone: þ81-6-6730-5880. Fax: þ81-6-6723-2721. E-mail: sa-
ga@chem.kindai.ac.jp.
’ ACKNOWLEDGMENT
8-formyl-chlorin 1 to 8-ethyl-chlorin 3, k(1)/k(3), is 1.5 ꢀ 10-3
.
We thank Ms. Aimi Sakamoto and Mr. Yasuhiro Iida, Kinki
University, for their experimental assistance. This work was
partially supported by Grants-in-Aid for Scientific Research (B)
for Young Scientists (Nos. 20750143 and 21750154) from the
Japan Society for the Promotion of Science.
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tion properties of metallochlorins to those in the B-ring.
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