PDI of
Abstract
The activity of singlet-oxygen sensitizers for photodynamic inactivation (PDI) of microorganisms and photodynamic therapy of tumor cells has been evaluated using Escherichia coli, Saccharomyces cerevisiae, and human cancer cell lines. In this chapter, drug resistance of E. coli was examined based on the PDI activity of a variety of RPy-P-porphyrin sensitizers with different number of ionic valence and different hydrophobic characters. The PDI activities toward E. coli were evaluated using the minimum effective concentrations ([P]) of the porphyrin sensitizers. It was found that the [P] value for E. coli was larger than that for S. cerevisiae. E. coli has drug-resistance toward hydrophobic and mono-cationic porphyrins. However, E. coli has weak drug-resistance toward the porphyrins with both polycationic character and hydrophobicity. Since the outer membrane mainly consists of lipopolysaccharides and phospholipids that are negatively charged, cationic porphyrins are able to adsorb to the outer leaflet. Then the cationic porphyrins with hydrophobic character can interact with not only the outer leaflet but also inner leaflet of the outer membrane and the plasma membrane. Thus, porphyrins may be incorporated inside E. coli cells via the self-promoted uptake pathway. Moreover, polycationic porphyrins can interact with DNA and proteins by strong binding affinities.
Keywords
- PDT sensitizer
- singlet oxygen
- porphyrins
- PDI activity
- Escherichia coli
- Saccharomyces cerevisiae
1. Introduction
Singlet-oxygen (1O2) sensitizers for photodynamic inactivation (PDI) of microorganisms and photodynamic therapy of tumor cells have been developed using
PDI refers to the use of a visible-light source, oxidizing agents (e.g., O2), and photosensitizers. Photosensitizers absorb light energy that causes an energy transfer to O2, which leads to the formation of reactive oxygen such as 1O2, thereby inactivating cells and bacteria. Preliminary studies on the photodynamic action for biological systems started in the 1930s by PDI of phages using methylene blue [6, 7]. PDI of bacteria has received considerable attention as a methodology leading to the medical application of infection therapy beyond antimicrobial resistance. Among the large variety of photosensitizers developed for PDI over the last 60 years, porphyrins and metalloporphyrins became attractive sensitizers owing to their strong absorption band in the visible-light region [8, 9, 10, 11].
In the case of porphyrin sensitizers, their solubilities in water are an important characteristic for handling them as aqueous solutions, since porphyrin derivatives, in general, are poorly soluble in water. The most popular method to improve the solubility in water is the introduction of ionic groups to the porphyrin ring. Especially, the introduction of an alkylpyridinium (RPy) group into porphyrins is a useful method to make porphyrins water-soluble [12, 13]. A typical RPy-bonded porphyrin is represented by
We have interested in axially RPy-bonded tricationic P-porphyrins and their PDI activity [22, 23, 24, 25, 26]. It is advantageous that the water solubilization is easily achieved through the modification of the axial ligands of P-porphyrins. It is expected that polycationic porphyrins have strong binding affinities to DNA [27, 28, 29, 30, 31, 32]. In this chapter, drug resistance of
2. Materials and methods
2.1 Axially RPy-bonded tricationic P-porphyrins: (RPy3)2P(Tpp)3+
The preparation of tricationic bis[3-(1-alkyl-4-pyridinio)propoxo]tetraphenylporphyrinatophosphorus(V) complex, (RPy3)2P(Tpp)3+ (Tpp = tetraphenylporphyrinato group), was performed as follows [22]. Dichloro(tetraphenylporphyrinato)phosphorus chloride ([Cl2P(Tpp)]Cl [33], 300 mg) was reacted with 3-(4-pyridyl)-1-propanol (5.0 mL) in MeCN (30 mL) at reflux temperature for about 24 h until the Soret band shifted from 435 to 428 nm. Bis[3-(4-pyridyl)propoxo]tetraphenylporphyrinatophosphorus(V) chloride, (Py3)2P(Tpp)+, was produced in 47% yield. The (Py3)2P(Tpp)+ (50 mg) was reacted with alkyl halides (1.0 mL) in MeCN (25 mL) at reflux temperature for about 24 h to give (RPy3)2P(Tpp)3+ [22]. The yields of (RPy3)2P(Tpp)3+ are listed in Table 1.
Sensitizers | Metal | ||||||
---|---|---|---|---|---|---|---|
Soret | Q | ||||||
(MePy3)2P(tpp) | 1 | +3 | P | 95 | 26.9 | 1.38 | 3.4 |
(BuPy3)2P(tpp) | 4 | +3 | P | 93 | 23.1 | 1.18 | 6.1 |
(PentPy3)2P(tpp) | 5 | +3 | P | 32 | 27.2 | 1.32 | 3.8 |
(HexPy3)2P(tpp) | 6 | +3 | P | 47 | 31.3 | 1.45 | 5.8 |
(HeptPy3)2P(tpp) | 7 | +3 | P | 32 | 26.7 | 1.26 | 6.0 |
(OctPy3)2P(tpp) | 8 | +3 | P | 48 | 18.7 | 0.97 | 3.8 |
(HexPy3)2Sb(tpp) | 6 | +3 | Sb | 35 | 16.3 | 4.18 | 11.1 |
(MePy3)Sb(tpp) | 1 | +2 | Sb | 42 | 12.7 | 4.45 | 2.4 |
(HexPy3)Sb(tpp) | 6 | +2 | Sb | 25 | 15.1 | 4.48 | 5.2 |
(MePy5)2P(tpp) | 1 | +3 | P | 73 | 28.2 | 1.36 | >120 |
(EtPy5)2P(tpp) | 2 | +3 | P | 58 | 29.6 | 1.40 | >120 |
(ButPy5)2P(tpp) | 4 | +3 | P | 44 | 25.3 | 1.29 | 112 |
(HexPy5)2P(tpp) | 6 | +3 | P | 44 | 24.7 | 1.22 | 64 |
(4EtPy5)2P(tpp) | 2 | +3 | P | 72 | 12.7 e | 0.57 e | >120 |
(Me)2P(PyHex) | 6 | +2 | P | 57 | 22.6 | 1.31 | 5.0 |
(Me |
6 | +2 | P | 78 | 14.1 | 0.89 | 11.4 |
(Bu |
1 | +2 | P | 94 | 18.1 | 1.01 | 13.6 |
(Bu |
1 | +2 | P | 32 | 21.7 | 1.21 | 13.0 |
(Hex |
1 | +2 | P | 45 | 28.6 | 1.63 | 8.0 |
2.2 Axially RPy-bonded polycationic Sb-porphyrins
Axially RPy-bonded polycationic Sb-porphyrins were prepared using dibromo(tetraphenylporphyrinato)antimony bromide ([Br2Sb(Tpp)]Br) as the starting material [34]. The partial methanolysis of [Br2Sb(Tpp)]Br (1.077 g) was performed in MeOH-MeCN (1:1, 160 mL) in the presence of pyridine (0.75 mL) at 80°C until the Soret band shifted from 427 to 423 nm. Bromo(methoxo)-(tetraphenylporphyrinato)antimony bromide ([MeO(Br)Sb(Tpp)]Br, 520 mg) was formed in 61% yield [35]. An MeCN (20 mL) solution of [Br2Sb(Tpp)]Br (150 mg) and [MeO(Br)Sb(Tpp)]Br (180 mg) was heated with 3-(4-pyridyl)-1-propanol (3.7 mL) at refluxing temperature for about 24 h until the Soret band shifted to 418 nm, respectively. Thus, bis[3-(4-pyridyl)propoxo]tetraphenyl-porphyrinatoantimony (V) bromide ((Py3)2Sb(Tpp)+, 83 mg) and 3-(4-pyridyl)propoxo(methoxo)tetraphenylporphyrinatoantimony (V) bromide (Py3Sb(Tpp)+, 90 mg) were obtained in 50% and 43% yields, respectively. (Py3)2Sb(Tpp)+ (50 mg) was reacted with 1-bromohexane (0.5 mL) in MeCN (13 mL) at reflux temperature for about 24 h to give bis[3-(1-hexyl-4-pyridinio)-1-propoxo]-5,10,15,20-tetraphenylporphyrinatoantimony (V) tribromide ((HexPy3)2Sb(Tpp)3+, 20 mg, 35%). The reaction of (Py3Sb(Tpp)+, 50 mg) with MeI and 1-bromohexane (0.5 mL in MeCN (13 mL) at reflux temperature for about 24 h gave α-(methoxo)-β-[3(1-methyl-4-pyridinio)-1-propoxo]-5,10,15,20-tetraphenylporphyrinatoantimony (V) dibromide (MePy3Sb(Tpp)2+, 25 mg, 42%) and α-(methoxo)-β-[3 (1-hexyl-4-pyridinio)-1-propoxo]-5,10,15,20-tetraphenyl-porphyrinatoantimony (V) dibromide (HexPy3Sb(Tpp)2+, 20 mg, 25%), respectively [24].
2.3 Axially RPy-bonded tricationic P-porphyrins: (RPy5)2P(Tpp)3+
Bis[5-(3-alkyl-1-pyridinio)-3-oxapentyloxo]tetraphenylporphyrinato-phosphorus(V) dibromide, chloride ((RPy5)2P(Tpp)3+) was prepared from dihydroxo(tetraphenylporphyrinato)phosphorus chloride ([(HO)2P(Tpp)]Cl), which was prepared by hydrolysis of [Cl2P(Tpp)]Cl (300 mg) by refluxing in a mixed solvent of MeCN (160 mL) with pyridine (60 mL) and H2O (60 mL) [22]. Alkylation of [(HO)2P(Tpp)]Cl (80 mg) with di(2-bromoethyl) ether (1 mL) was performed in the presence of K2CO3 (19 mg) and 18-crown-6 ether (4.2 mg) in MeCN (5 mL) at 50°C to give bis(5-bromo-3-oxa-pentyloxo)tetraphenyl-porphyrinatophosphorus(V) chloride ((Br5)2P(Tpp)+). The (Br5)2P(Tpp)+ (50 mg) was reacted with 3-alkylpyridine (1.0 mL) in MeCN (10 mL) under heating at 100°C for 20–68 h for the preparations of (RPy5)2P(Tpp)3+ [22]. Similarly, bis[5-(4-ethyl-1-pyridinio)-3-oxapentyloxo]tetraphenylporphyrinatophosphorus(V) dibromide, chloride, (4EtPy5)2P(Tpp)3+ was prepared via the reaction of (Br5)2P(Tpp)+ (63 mg) with 4-ethylpyridine (1.0 mL) in dry MeCN (10 mL) at 100°C for 20 h.
2.4 RPy-bonded dicationic P-porphyrins at meso position: (R’m )2P(RPyTpp)2+
At first, 5,10,15-triphenyl-20-(4-pyridinyl)porphyrin (PyTpp) was prepared by reaction of pyrrole (1.55 mL), benzaldehyde (1.83 mL), and 4-formylpyridine (0.56 mL) in propanoic acid (100 mL) in an oil bath heated at 140°C for 1 h to give PyTpp (533 mg, 14%) [24]. PyTpp (101 mg) was reacted with phosphoryl chloride (POCl3, 2.0 mL) in pyridine (10 mL) in a pressure bottle heated at 180°C for 1 day to give dichloro[triphenyl(4-pyridinyl)porphyrinato]phosphorus chloride ([Cl2P(PyTpp)]Cl, 99.0 mg) in 81% yield. Substitution of the axial chloro ligand with a methoxo group was performed by refluxing [Cl2P(PyTpp)]Cl (82.7 mg) in MeOH (20 mL)-pyridine (0.25 mL) for 3 days until the Soret band shifted from 435 to 424 nm. Dimethoxo[5-(1-hexyl-4-pyridinio)-10,15,20-triphenyl-porphyrinato]phosphorus (V) dichloride ((Me)2P(HexPyTpp)2+) was prepared by reaction of [(MeO)2P(PyTpp)]Cl (62.0 mg) with 1-iodohexane (2 mL) in DMF (5 mL) in the presence of K2CO3 (19 mg) at 100°C for 2 h. (Me)2P(HexPyTpp)2+ was purified through anion exchange with chloride ions, as follows. An aqueous solution (10 mL) of AgBF4 (115 mg) was added to a MeCN-MeOH (1:1 v/v, 20 mL) solution of the porphyrins. After stirring for 24 h at room temperature, the solution was washed with water (100 mL) and an aqueous NaCl solution (100 mL) three times and subjected to precipitation with hexane (200 mL) [24].
[Cl2P(PyTpp)]Cl (78–100 mg) was reacted with ethylene glycol derivatives (H(OCH2CH2)
2.5 Preparation of E. coli suspension
2.6 PDI of E. coli
PDI of
The amount of the living cells (
2.7 Fluorescence imaging
Incorporation of porphyrin sensitizers inside cells can be examined by fluorescence microscopy images of
3. Results
3.1 Properties of RPy-bonded P-porphyrins
Figure 2 shows the structures of the prepared porphyrins, which were water soluble due to cationic complexes. The water solubility (
3.2 Results of PDI of E. coli
Results of PDI of
Sensitizers | Amount of bacteria ([ |
|||||||
---|---|---|---|---|---|---|---|---|
20 | 40 | 60 | 80 | 100 | 120 | |||
(MePy3)2P(tpp) | 2.0 | 512 ± 22 | 450 ± 14 | 383 ± 13 | 344 ± 20 | 198 ± 13 | 103 ± 4.5 | 27 ± 1.2 |
(BuPy3)2P(tpp) | 2.0 | 377 ± 56 | 216 ± 10 | 105 ± 9.9 | 39 ± 5.3 | 18 ± 3.2 | 6.0 ± 2.7 | 2.3 ± 0.6 |
(PentPy3)2P(tpp) | 0.5 | 105 ± 12 | 65 ± 12 | 36 ± 4.6 | 19 ± 3.8 | 14 ± 4.0 | 11 ± 3.1 | 7.0 ± 2.0 |
(HexPy3)2P(tpp) | 0.5 | 243 ± 23 | 156 ± 5.2 | 125 ± 5.8 | 86 ± 3.1 | 77 ± 7.5 | 60 ± 1.2 | 17 ± 6.0 |
(HeptPy3)2P(tpp) | 0.4 | 203 ± 16 | 117 ± 9.1 | 53 ± 3.8 | 39 ± 3.1 | 15 ± 1.2 | 4.7 ± 2.1 | 3.0 ± 0 |
(OctPy3)2P(tpp) | 0.5 | 294 ± 14 | 215 ± 15 | 194 ± 12 | 136 ± 16 | 103 ± 9.9 | 76 ± 10 | 44 ± 8.0 |
(HexPy3)2Sb(tpp) | 1.0 | 152 ± 7.1 | 110 ± 4.7 | 76 ± 17 | 49 ± 4.2 | 36 ± 15 | 21 ± 4.5 | 45 ± 8.7 |
(MePy3)Sb(tpp) | 1.0 | 170 ± 13 | 167 ± 17 | 134 ± 8.0 | 126 ± 6.8 | 102 ± 17 | 108 ± 26 | 113 ± 13 |
(HexPy3)Sb(tpp) | 1.0 | 131 ± 28 | 120 ± 14 | 75 ± 11 | 55 ± 16 | 36 ± 11 | 23 ± 3.5 | 13 ± 1.7 |
(MePy5)2P(tpp) | 1.0 | 29 ± 6.4 | 16 ± 4.2 | 12 ± 5.6 | 10 ± 1.0 | 13 ± 2.3 | 6.7 ± 2.1 | 6.7 ± 1.5 |
(EtPy5)2P(tpp) | 0.25 | 167 ± 14 | 141 ± 18 | 59 ± 9.0 | 5.7 ± 0.6 | 1.7 ± 1.5 | 0.3 ± 0.6 | 0 |
(BuPy5)2P(tpp) | 0.25 | 145 ± 11 | 123 ± 7.6 | 92 ± 7.5 | 63 ± 4.6 | 33 ± 8.4 | 6.7 ± 4.9 | 4.7 ± 0.6 |
(HexPy5)2P(tpp) | 0.25 | 213 ± 10 | 213 ± 9.5 | 176 ± 16 | 166 ± 6.8 | 140 ± 8.2 | 132 ± 12 | 97 ± 4.4 |
(4-EtPy5)2P(tpp) | 0.5 | 139 ± 14 | 85 ± 13 | 88 ± 16 | 62 ± 6.0 | 42 ± 8.7 | 32 ± 7.0 | 33 ± 1.5 |
(Me)2P(PyHex) | 2.0 | 90 ± 13 | 88 ± 17 | 49 ± 7.8 | 27 ± 6.2 | 17 ± 5.1 | 13 ± 1.5 | 15 ± 3.1 |
(Me |
0.5 | 89 ± 2.7 | 57 ± 2.9 | 42 ± 7.2 | 18 ± 3.5 | 16 ± 2.9 | 8.3 ± 4.0 | 5.7 ± 1.2 |
(Me |
0.5 | 109 ± 26 | 99 ± 13 | 59 ± 12 | 64 ± 10 | 65 ± 165 | 59 ± 42 | 41 ± 9.6 |
(Bu |
0.5 | 24 ± 3.6 | 20 ± 4.5 | 13 ± 3.0 | 12 ± 1.2 | 7.3 ± 2.9 | 3.7 ± 2.1 | 4.7 ± 1.2 |
(Bu |
0.5 | 34 ± 5.0 | 25 ± 3.5 | 28 ± 6.1 | 31 ± 3.5 | 25 ± 1.5 | 20 ± 2.7 | 19 ± 2.1 |
(Bu |
2.0 | 126 ± 14 | 56 ± 3.8 | 21 ± 4.9 | 8.7 ± 2.1 | 3.3 ± 3.5 | 1.7 ± 0.6 | 2.3 ± 2.1 |
(Bu |
2.0 | 150 ± 13 | 141 ± 5.5 | 129 ± 8.3 | 124 ± 11 | 116 ± 13 | 84 ± 14 | 94 ± 12 |
(Hex |
1.0 | 63 ± 5.9 | 50 ± 7.5 | 56 ± 2.1 | 45 ± 8.1 | 39 ± 9.1 | 35 ± 6.1 | 33 ± 12 |
Based on Table 2, the survival ratios were calculated as 100
Sensitizera | Metal | [ |
||||
---|---|---|---|---|---|---|
(MePy3)2P(tpp) | +3 | P | 1 | 2.0 | 66 | 0.5 |
(BuPy3)2P(tpp) | +3 | P | 4 | 2.0 | 27 | 1.1 |
(PentPy3)2P(tpp) | +3 | P | 5 | 0.5 | 29 | 4.1 |
(HexPy3)2P(tpp) | +3 | P | 6 | 0.5 | 31 | 3.8 |
(HeptPy3)2P(tpp) | +3 | P | 7 | 0.4 | 24 | 6.3 |
(OctPy3)2P(tpp) | +3 | P | 8 | 0.5 | 63 | 1.9 |
(HexPy3)2Sb(tpp) | +3 | Sb | 6 | 1.0 | 36 | 1.7 |
(MePy3)Sb(tpp) | +2 | Sb | 1 | 1.0 | 106 | 0.6 |
(HexPy3)Sb(tpp) | +2 | Sb | 6 | 1.0 | 68 | 0.9 |
(MePy5)2P(tpp) | +3 | P | 1 | 1.0 | 40 | 1.5 |
(EtPy5)2P(tpp) | +3 | P | 2 | 0.25 | 32 | 7.5 |
(ButPy5)2P(tpp) | +3 | P | 4 | 0.25 | 53 | 4.5 |
(HexPy5)2P(tpp) | +3 | P | 6 | 0.25 | 120 | 2.0 |
(4EtPy5)2P(tpp) | +3 | P | 2 | 0.5 | 50 | 2.4 |
(Me)2P(PyHex) | +2 | P | 6 | 2.0 | 45 | 0.7 |
(Me |
+2 | P | 6 | 0.5 | 37 | 3.2 |
(Bu |
+2 | P | 1 | 0.5 | 55 | 2.2 |
(Bu |
+2 | P | 1 | 2.0 | 23 | 1.3 |
(Hex |
+2 | P | 1 | 1.0 | 116 | 0.5 |
3.3 PDI activity of the porphyrin sensitizers toward E. coli
As shown in Table 3, the
Figure 5 shows the fluorescence images of
3.4 Comparison of the PDI activity in E. coli with the PDI activity in Saccharomyces cerevisiae
For comparison of the PDI activity in
4. Discussion
The mechanism behind the PDI activity in
5. Conclusion
PDI of
Acknowledgments
We thank Mr. Tomohiko Shinbara, Mr. Hiroki Kanemaru, Mr. Yusaku Suemoto, Mr. Kyosuke Takemori, Mr. Masato Shigehara, Mr. Kou Suzuki, Ms. Akari Miyamoto, and Hidekazu Uezono for their efforts on PDI of
AF | PDI activity (in μM−1 h−1): AF = 60/([P] × T1/2) |
B | mount of bacteria |
B0 | initial amount of bacteria |
CFU | colony formation unit |
CW | water solubility |
ε | molar absorption coefficient |
LB | Luria-Bertani medium |
m | number of ethylene glycol unit |
n | carbon number of the alkyl chain on the Ap |
[P] | minimum effective concentrations of sensitizer |
PDI | photodynamic inactivation |
RPy | N-alkylpyridinium group |
t | irradiation time |
T1/2 | half-life time required to reduce B from B0 to 0.5B0 |
Z | valence number of the porphyrin complex |
(Br5)2P(Tpp)+ | bis(5-bromo-3-oxapentyloxo)tetraphenylporphyrinato-phosphorus chloride |
(Py3)2P(Tpp)+ | bis[3-(4-pyridyl)propoxo]tetraphenylporphyrinato-phosphorus chloride |
(Py3)2Sb(Tpp)+ | bis[3-(4-pyridyl)propoxo]tetraphenylporphyrinato-antimony bromide |
Py3Sb(Tpp)+ | 3-(4-Pyridyl)propoxo(methoxo)tetraphenylporphyrinatoantimony bromide |
PyTpp | triphenyl(4-pyridinyl)porphyrin |
(RPy3)2P(Tpp)3+ | bis[3-(1-alkyl-4-pyridinio)propoxo]tetraphenylpor-phyrinatophosphorus chloride, dihalide |
(RPy3)2Sb(Tpp)3+ | bis[3-(1-alkyl-4-pyridinio)propoxo]tetraphenylpor-phyrinatoantimony tribromide |
(RPy5)2P(Tpp)3+ | bis[5-(3-alkyl-1-pyridinio)-3-oxapentyloxo]tetraphenyl-porphyrinatophosphorus dibromide, chloride |
RPy3Sb(Tpp)2+ | α-(methoxo)-β-[3-(1-hexyl-4-pyridinio)-1-propoxo]-5,10,15,20-tetraphenylporphyrinatoantimony (V) dibromide |
(R’m)2P(RPyTpp)2+ | bis(2-alkyloxyethoxo)-5-(1-alkyl-4-pyridinio)-10,15,20-triphenylporphyrinatophosphorus (V) dichloride |
TMP | meso-tetra[4-(1-methylpyridinium)]porphyrin |
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