Comparison of demetalation properties between zinc chlorin and zinc porphyrin derivatives: Effect of macrocyclic structures

Article abstract of DOI:10.1016/j.bmc.2010.06.019

Metalloporphyrins and metallochlorins are important biological molecules in nature. To examine the effect of macrocyclic structures on removal of central metals from these cyclic tetrapyrrole molecules without peripheral substitution effects, demetalation of zinc methyl pyropheophorbide a (zinc chlorin 1) and zinc methyl protopyropheophorbide a (zinc porphyrin 2) was kinetically analyzed under acidic conditions. Both 1 and 2 exhibited gradual spectral changes from zinc complexes to free-base forms with several isosbectic points in acetone/water (10:1) at the proton concentration of 6.1 × 10^-3 M. Demetalation of zinc porphyrin 2 was slower than that of zinc chlorin 1 in the temperature range between 15 and 35 °C. This indicates that the porphyrin macrocycle provides tolerance to removal of the central metal from cyclic tetrapyrrole ligands compared with the chlorin macrocycle.

Full text of DOI:10.1016/j.bmc.2010.06.019

Bioorganic & Medicinal Chemistry 18 (2010) 5697–5700
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Bioorganic & Medicinal Chemistry
journal homepage: www.elsevier.com/locate/bmc
Comparison of demetalation properties between zinc chlorin and zinc
porphyrin derivatives: Effect of macrocyclic structures
*
Yoshitaka Saga , Sayaka Hojo, Yuki Hirai
Department of Chemistry, Faculty of Science and Engineering, Kinki University, Higashi-Osaka, Osaka 577-8502, Japan
a r t i c l e i n f o
a b s t r a c t
Article history:
Metalloporphyrins and metallochlorins are important biological molecules in nature. To examine the
effect of macrocyclic structures on removal of central metals from these cyclic tetrapyrrole molecules
without peripheral substitution effects, demetalation of zinc methyl pyropheophorbide a (zinc chlorin
1) and zinc methyl protopyropheophorbide a (zinc porphyrin 2) was kinetically analyzed under acidic
conditions. Both 1 and 2 exhibited gradual spectral changes from zinc complexes to free-base forms with
several isosbectic points in acetone/water (10:1) at the proton concentration of 6.1 ꢀ 10ꢁ3 M. Demetala-
tion of zinc porphyrin 2 was slower than that of zinc chlorin 1 in the temperature range between 15 and
35 °C. This indicates that the porphyrin macrocycle provides tolerance to removal of the central metal
from cyclic tetrapyrrole ligands compared with the chlorin macrocycle.
Received 20 April 2010
Revised 4 June 2010
Accepted 5 June 2010
Available online 18 June 2010
Keywords:
Chlorin
Chlorophyll
Demetalation
Porphyrin
Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction
investigated demetalation of several Chl derivatives under various
conditions.18–20 Watanabe and co-workers studied physicochemi-
Metalloporphyrins and metallochlorins (metal complexes of
17,18-dihydroporphyrins) play important roles in biological sys-
tems.1–3 Heme and chlorophyll (Chl) are famous naturally occurring
metalloporphyrins and metallochlorins, respectively. Metallopor-
phyrins mainly function as key cofactors in enzymes and oxygen-
transporting proteins. In contrast, metallochlorins are major
photosynthetic pigments in nature. In some cases, metalloporphy-
rins are also found in photosynthetic chlorophyllous molecules:
Chls c are antenna photosynthetic pigments in chromophyte algae
and some prokaryotes,4 and protochlorophyllides are known to be
important intermediates in the Chl biosynthetic pathway.5 The
cal properties of demetalation of Chls a, b, and their epimers (Chls
a0 and b0, respectively) in detail.21,22 After the discovery of naturally
occurring zinc bacteriochlorophyll (BChl) a in the purple photosyn-
thetic bacterium, Acidiphilium rubrum,28–31 demetalation kinetics of
this pigment was thoroughly examined by Kobayashi et al.23,24 Zn
BChl a was found to show higher resistance to demetalation than
BChl a possessing a magnesium as the central metal.23,24 Such a
property of Zn BChl a could be preferable to Acidiphilium rubrum,
which grows in acidic conditions. Recently, we reported demetala-
tion properties of light-harvesting BChls, c, d, and e in green sulfur
photosynthetic bacteria25,26 and Chl d in a cyanobacterium Acary-
ochloris marina.27
difference of the cyclic tetrapyrrole
p-systems in metalloporphy-
rins and metallochlorins affects their spectral and physicochemical
properties.
Several works indicated that peripheral substituents in
cyclic tetrapyrrole rings of these molecules affected demetala-
tion properties of both metalloporphyrins and metallochlo-
rins.11,13,15–17,21,25–27 However, there is no study, to our best
knowledge, on direct comparison of demetalation properties
between metalloporphyrin and metallochlorin without substitu-
tion effects of the cyclic tetrapyrrole moieties. In the present study,
we first report the effect of macrocyclic structures on demetalation
kinetics of metallochlorin and metalloporphyrin possessing the
same peripheral substituents. The molecular structures of metallo-
porphyrin and metallochlorin used in the present study are
depicted in Figure 1. Zinc methyl pyropheophorbide a (denoted
as zinc chlorin 1), whose photofunctional moiety is the chlorin
macrocycle, possesses similar peripheral substituents to naturally
occurring Chl a. Zinc methyl protopyropheophorbide a (denoted
as zinc porphyrin 2) has the same molecular structure as zinc
The stability of metalloporphyrins and metallochlorins has
attracted much attention. Removal of central metals from these
molecules is one of the major degradation reactions. In addition,
demetalation of metallochlorins and metalloporphyrins in
photosynthetic systems could be a key reaction in the early process
of in vivo chlorophyll degradation.6–9 From these viewpoints,
demetalation properties of metalloporphyrins10–15 and metallo-
chlorins16–27 have been extensively investigated in vitro. In the
cases of naturally occurring metallochlorins, Mackinney and Joslyn
reported demetalation kinetics of natural chlorophyllous pigments,
Chls a and b, in the early 1940s.16,17 Subsequently, some groups
* Corresponding author. Tel.: +81 6 6730 5880; fax: +81 6 6723 2721.
E-mail address: saga@chem.kindai.ac.jp (Y. Saga).
0968-0896/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.bmc.2010.06.019

5698
Y. Saga et al. / Bioorg. Med. Chem. 18 (2010) 5697–5700
1.2
1.0
0.8
0.6
0.4
0.2
A
B
N
N
N
N
Zn
18
17
0.0
1.2
O
O
O CH3
1.0
Figure 1. Molecular structures of zinc methyl pyropheophorbide a (zinc chlorin 1,
single bond between 17-C and 18-C atoms) and zinc methyl protopyropheophor-
bide a (zinc porphyrin 2, double bond between 17-C and 18-C atoms).
0.8
0.6
0.4
0.2
0.0
chlorin 1 except for the bond between 17-C and 18-C atoms, and
can be a good model compound of porphyrin-type photosynthetic
pigments, protochlorophyllide a, which is an important intermedi-
ate molecule in the biosynthetic pathway of Chl a.32,33 It is worth
noting that neither zinc chlorin nor zinc porphyrin have been
found as natural photosynthetic pigments although Zn BChl a
was discovered in Acidiphilium rubrum.28–31 Comparison of
demetalation kinetics between 1 and 2 enables us to unravel the
effect of macrocyclic structures without peripheral substitution
effects of the cyclic tetrapyrroles.
400
500
600
700
800
Wavelength / nm
Figure 2. Spectral changes of zinc chlorin 1 (A) and zinc porphyrin 2 (B) in acetone/
water (10:1, vol/vol) at the proton concentration of 6.1 ꢀ 10ꢁ3
M at 25 °C.
Compound 1: spectra from 0 to 15 min at 5-min intervals. Compound 2: spectra
from 0 to 30 min at 5-min intervals. Arrows show the direction of the absorbance
changes.
2. Results and discussion
Zinc chlorin 1 and zinc porphyrin 2 were synthesized from nat-
urally occurring Chl a according to previous reports,33,34 and puri-
fied by reverse-phase high-performance liquid chromatography
(HPLC) before measurement of demetalation kinetics. Demetala-
tion properties of 1 and 2 were examined under acidic aqueous
acetone as described previously.21–23,25–27 Figure 2 shows spectral
changes of zinc chlorin 1 and zinc porphyrin 2 during demetalation
processes in acetone/water (10:1, vol/vol) at the proton concentra-
tion of 6.1 ꢀ 10ꢁ3 M at 25 °C. Zinc chlorin 1 exhibited intense Soret
and Qy bands at 429 and 658 nm, respectively, in this solution.
These absorption bands decreased by incubation under the acidic
condition, and a new Soret absorption band appeared at 411 nm,
which was characteristic of the demetalation form of zinc chlorin
1. Small absorption bands in the range between 500 and 600 nm
were gradually changed in acidic aqueous acetone. The isosbestic
points could be clearly observed at 420, 453, 553, and 666 nm dur-
ing the demetalation reaction.
Similar spectral changes occurred during the demetalation pro-
cess of zinc porphyrin 2 under the acidic condition. The Soret band
of zinc porphyrin 2 at 431 nm decreased and a new Soret band of
the demetalation form of zinc porphyrin 2 appeared at 415 nm.
The isosbestic points could also be observed at 422, 457, 536,
551, 600, and 635 nm during the demetalation reactions of zinc
porphyrin 2.
Demetalation reactions can be quantitatively analyzed by
monitoring absorbance changes at the Soret peak positions of 1
and 2.21–23,25–27 Time courses of Soret peak absorbance of zinc chlo-
rin 1 and zinc porphyrin 2 incubated in aqueous acetone at the pro-
ton concentration of 6.1 ꢀ 10ꢁ3 M at 25 °C are shown in Figure 3.
The logarithm of Soret peak absorbance in the demetalation reac-
tions of both 1 and 2 exhibited linear time dependence. The
demetalation reactions of 1 and 2, therefore, can be regarded as
pseudo-first-order reactions.21–23,25–27 This is consistent with
the reaction condition in which the proton concentration
0.0
-0.5
-1.0
-1.5
-2.0
-2.5
-3.0
0
5
10
15
20
Time / min
Figure 3. Kinetic plots for demetalation of zinc chlorin 1 (open circle) and zinc
porphyrin 2 (open square) in acetone/water (10:1, vol/vol) at the proton concen-
tration of 6.1 ꢀ 10ꢁ3 M at 25 °C. Absorbance changes were monitored at 429 and
430 nm for 1 and 2, respectively. A0, A, and A1 are Soret absorbances of 1 and 2 at
the onset of measurement, at time t, and at the complete demetalation,
respectively.
(6.1 ꢀ 10ꢁ3 M) was much higher than the concentration of 1 and
2 (<10ꢁ5 M).21–23,25–27 In the demetalation processes, the reaction
rate constant, k, can be obtained by fitting the time courses of Soret
absorbance of 1 and 2 to the following kinetic equation:
lnðA ꢁ A1Þ=ðA0 ꢁ A1Þ ¼ ꢁkt;
where A0, A, and A1 are Soret absorbances of 1 and 2 at the onset of
measurement, at time t, and at the complete demetalation, respec-
tively.21–23,25–27 The demetalation rate constants of zinc chlorin 1
and zinc porphyrin 2 in acetone/water (10:1, vol/vol) at the proton
concentration of 6.1 ꢀ 10ꢁ3 M at 25 °C were estimated to be

Y. Saga et al. / Bioorg. Med. Chem. 18 (2010) 5697–5700
5699
The difference of demetalation properties between zinc chlorin
1 and zinc porphyrin 2 could be discussed in terms of redox poten-
tials of chlorin and porphyrin macrocycles. We recently reported
that resistance of demetalation of natural Chls possessing a formyl
group was correlated with their oxidation potentials27: the order of
resistance of demetalation, Chl b > Chl d > Chl a, was consistent
with the order of their oxidation potentials (Chl b (+0.94 V vs
SHE) > Chl d (+0.88 V) > Chl a (+0.81 V) in acetonitrile35). The
0.0
-0.5
-1.0
-1.5
-2.0
-2.5
-3.0
-3.5
electron densities of tetrapyrrole
p-systems, which shift redox
potentials of cyclic tetrapyrrole molecules, would affect the
demetalation properties. In comparison of oxidation potentials
between porphyrin and chlorin p-systems, the oxidation potential
of porphyrin molecules tended to shift positively compared with
chlorin molecules.36,37 Further physicochemical studies will be
necessary to understand thoroughly demetalation properties of
cyclic tetrapyrrole molecules.
The products after demetalation reaction under the present
condition were analyzed by reverse-phase HPLC. The main product
by demetalation of 1 exhibited a visible absorption spectrum of the
demetalated form of 1, methyl pyropheophorbide a (the Soret and
Qy bands were positioned at 408 and 666 nm, respectively, in the
HPLC eluent). Few other products were detected after the demeta-
lation reaction of 1. In the case of zinc porphyrin 2, the main prod-
uct after the reaction was assigned to the demetalated form of 2,
methyl protopyropheophorbide a (the Soret band was positioned
at 415 nm in the HPLC eluent), and other products were hardly ob-
servable. These indicate that little side reaction occurred through
demetalation of 1 and 2 under the present reaction conditions.
Comparison of demetalation properties between zinc chlorin 1
and zinc porphyrin 2 might be in line with the early processes of
the degradation of biological cyclic tetrapyrrole molecules. In the
degradation pathway of Chl a, demetalation occurs prior to oxida-
tive cleavage of the meso-position of the chlorin macrocycle by
pheophorbide a oxygenase.6–9,38,39 Therefore, smooth removal of
central magnesium from the chlorin macrocycle would be impor-
tant in the Chl degradation, although the in vivo demetalation
mechanism of natural Chls or chlorophyllides has not been thor-
oughly unraveled.40–42 It might be worth noting that one of the
famous metalloporphyrins, heme, breaks down into biliverdin by
heme oxygenase, followed by release of central iron.43,44
3.20
3.30
3.40
3.50
T-1 /10-3 K -1
Figure 4. Arrhenius plots over temperature range of 15–35 °C for the reduction rate
constants of zinc chlorin 1 (open circle) and zinc porphyrin 2 (open square) in
acetone/water (10:1, vol/vol) at the proton concentration of 6.1 ꢀ 10ꢁ3 M.
2.5 ꢀ 10ꢁ1 and 1.5 ꢀ 10ꢁ1 minꢁ1, respectively (the average of 3–5
independent measurements). The demetalation rate constant of
zinc chlorin 1 was 1.7-times larger than that of zinc porphyrin 2.
These indicate that the macrocyclic
p-system affects demetalation
properties of cyclic tetrapyrrole molecules possessing a central me-
tal. Comparison of demetalation properties between chlorin-type
and bacteriochlorin-type pigments by Kobayashi et al.23 which indi-
cated that Mg BChl a and Zn BChl a had higher resistance than Mg
Chl a and Zn Chl a, respectively, also suggest the effect of the mac-
rocyclic structures on removal of central metal, although the substi-
tuent at the 3-position of BChl a was not the same as that of Chl a.
Temperature dependence of demetalation rate constants of zinc
chlorin 1 and zinc porphyrin 2 at the proton concentration of
6.1 ꢀ 10ꢁ3 M was examined between 15 and 35 °C at 10 °C inter-
vals. Demetalation of both 1 and 2 slowed with decrease of the
reaction temperature. The logarithm of Soret absorbance of 1 and
2 was linearly changed against reaction time in this temperature
range, indicating that these demetalation reactions could be ana-
lyzed as pseudo-first-order reactions. Therefore, the demetalation
rate constants in this temperature range were estimated by fitting
the time course of Soret absorbance of 1 and 2 to the above kinetic
equation. Figure 4 depicts Arrhenius plots of the demetalation rate
constants of zinc chlorin 1 and zinc porphyrin 2 in acetone/water
(10:1, vol/vol) at the proton concentration of 6.1 ꢀ 10ꢁ3 M in the
temperature range between 15 and 35 °C. The activation energies
To summarize, the present kinetic analyses directly revealed the
difference of physicochemical properties on the removal of central
metal from the tetrapyrrole macrocycles between porphyrin and
chlorin
p-systems without effects of their peripheral substituents
on the cyclic tetrapyrrole rings. The porphyrin-type macrocycle
was more tolerant to demetalation than the chlorin-type macrocy-
cle. These results should be useful in chemistry and biochemistry
of cyclic tetrapyrrole molecules.
3. Experimental
3.1. Apparatus
Visible absorption spectra were measured with a Shimadzu
UV-2450 spectrophotometer, where the reaction temperature
was regulated with a Shimadzu thermo-electric temperature-con-
trolled cell holder TCC-240A. Mass spectra were measured with a
Shimadzu KOMPACT MALDI 4 spectrometer. HPLC was performed
with a Shimadzu LC-20AT pump and an SPD-M20A or SPD-20AV
detector.
of demetalation of
1 and 2 were estimated to be 95 and
101 kJ molꢁ1, respectively, from the Arrhenius plots in Figure 4.
These values were larger than the reported activation energies of
natural Chl a, 47.4 kJ molꢁ1, in acetone/water (3:1, vol/vol) at the
proton concentration of 3.7 ꢀ 10ꢁ4 M.21 This would be mainly
ascribable to the difference of central metals in the macrocycles,
since Zn Chl a has higher resistance to demetalation than Chl a pos-
sessing a central magnesium.23,24
3.2. Measurements of demetalation kinetics
Measurements of demetalation kinetics of
1 and 2 were
performed in the similar procedure to previous reports.21–23,25–27

5700
Y. Saga et al. / Bioorg. Med. Chem. 18 (2010) 5697–5700
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A 3 mL acetone solution of 1 and 2 (Soret absorbance = 1.0) was
mixed with 0.28 mL of distilled water. In kinetic analysis of
demetalation processes, 20 lL of aqueous 1 M HCl solution was
added to the pigment solution, and absorbance at the Soret peak
position of pigments was measured under the control of reaction
temperatures between 15 and 35 °C.
3.3. Materials
Zinc methyl pyropheophorbide a (1) and zinc methyl protopyr-
opheophorbide a (2) were synthesized from naturally occurring
Chl a according to previous reports.33,34 General synthetic proce-
dures of these compounds were as follows. Methyl pyropheophor-
bide a was synthesized through three steps from Chl a, which was
extracted from Spirulina geitleri. A methanol solution saturated with
Zn(CH3COO)2ꢂ2H2O was added to a dichloromethane solution of
methyl pyropheophorbide a, and the solution was stirred at room
temperature for ca. 2 h to afford zinc methyl pyropheophorbide a
(1).33,34 Zinc methyl pyropheophorbide a (1) was reacted with 2,3-
dichloro-5,6-dicyano-p-benzoquinone (1.1 equiv) in distilled ace-
tone for ca. 5 min to give zinc methyl protopyropheophorbide a
(2).33 Zinc complexes 1 and 2 were purified by reverse-phase HPLC.
3.4. Spectral data
29. Kobayashi, M.; Akiyama, M.; Kise, H.; Takaichi, S.; Watanabe, T.; Shimada, K.;
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3.4.1. Zinc methyl pyropheophorbide a (1)
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32. Helfrich, M.; Schoch, S.; Schäfer, W.; Ryberg, M.; Rüdiger, W. J. Am. Chem. Soc.
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UV–vis (acetone) kmax = 655 (relative intensity, 0.68), 608 (0.12),
567 (0.07), 524 (0.04), 426 (1.00), 405 nm (0.61). MS (MALDI):
found: m/z 611.2, calcd for C34H35N4O3Zn (MH+), 611.2. See also
Ref. 33.
3.4.2. Zinc methyl protopyropheophorbide a (2)
UV–vis (acetone) kmax = 613 (relative intensity, 0.13), 563
(0.05), 428 nm (1.00). MS (MALDI): found: m/z 609.6, calcd for
C
34H33N4O3Zn (MH+), 609.2. See also Ref. 33.
34. Tamiaki, H.; Amakawa, M.; Shimono, Y.; Tanikaga, R.; Holzwarth, A. R.;
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