Radiolysis and photolysis studies on active transient species of berberine

Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 124 (2014) 670–676

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Radiolysis and photolysis studies on active transient species of berberine Ling-Li Cheng a, Yu-Jia Wang a, Da-Hong Huang a, Si-De Yao b, Guo-Ji Ding a, Shi-Long Wang b,⇑, Zheng Jiao a,⇑ a b

School of Environmental and Chemical Engineering, Shanghai University, Shanghai 200444, China School of Life Science and Technology, Tongji University, Shanghai 200092, China

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

 BBR could be reduced by e aq . 

 BBR can react with OH through one-

electron oxidation process.   BBR(–H) react with dGMP via electron transfer to give dGMP(–H).   BBR(–H) can selectively oxidize the DNA at guanine moiety.   The reaction mechanisms of BBR(–H) and 3BBR* with DNA were confirmed.

a r t i c l e

i n f o

Article history: Received 5 December 2013 Received in revised form 14 January 2014 Accepted 19 January 2014 Available online 27 January 2014 Keywords: Berberine Pulse radiolysis Laser flash photolysis DNA photodamage

a b s t r a c t In this paper, the photochemical and photobiological characters of the active radicals of berberine (BBR) was investigated for finding an efficient and safe photosensitizer with highly active transient products using in Photodynamic therapy (PDT) study. The active species of BBR was generated and identified by using pulse radiolysis method. In neutral aqueous solution, BBR react with hydrated electron and hydroxyl radical, forming the radical anion and neutral radical of BBR, and the related reaction rates were determined as 3.5  1010 and 6.7  109 M1 s1, respectively. Further, the capability of BBR to photosensitize DNA cleavage was testified by laser flash photolysis (LFP) method, the results demonstrated that BBR neutral radical could react with guanine mononucleotide (K = 1.9  109 M1 s1) via electron transfer to give the guanine neutral radical. Additionally BBR selective cleavage single and double strand DNA at guanine moiety was observed. Finally, combining with the thermodynamic calculation, the possible photodamage mechanism of dGMP and DNA induced by BBR was clarified. Ó 2014 Elsevier B.V. All rights reserved.

Introduction Photodynamic therapy (PDT) is a non-surgical, minimally invasive approach, which can be defined as the administration of a non-toxic drug or dye known as a photo-sensitizer (PS) either ⇑ Corresponding authors. Tel./fax: +86 21 66137803 (Z. Jiao). Tel.: +86 21 65982595; fax: +86 21 65982286 (S.-L. Wang). E-mail addresses: [email protected] (S.-L. Wang), [email protected] (Z. Jiao). http://dx.doi.org/10.1016/j.saa.2014.01.085 1386-1425/Ó 2014 Elsevier B.V. All rights reserved.

systemically, locally, or topically to a patient lesion, which is frequently, but not always cancer [1–3]. PDT is based on the photo-activation of PS when irradiated by light in a special wavelength window (generally the maximum absorption band of the PS compound). The light-excited PS generates reactive oxygen species (ROS) that induce reduction or destruction of the patient lesion by mainly two kinds of reactions [4]. In a Type I reaction, it can react directly with a substrate, such as the cell membrane or a molecule, and transfer a proton or an electron to form a radical anion

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or cation, respectively. These radicals may further react with oxygen to produce ROS. Alternatively in a Type II reaction, the light-excited PS can transfer its energy directly to molecular oxygen (itself a triplet in the ground state), to form excited state singlet oxygen. Both Type I and Type II reactions can occur simultaneously, and the ratio between these processes depends on the type of PS used, as well as the concentrations of substrate and oxygen [5,6]. Currently, the design and development of DNA-targeted PS with a valuable property of photo-cleavage of nucleic acid is receiving widespread interest, since it allows using light as a trigger of the nuclease activity [7]. By attaching the PS, such as ellipticine, psoralens, anthraquinones and porphyrins, to short oligonucleotides fragments bound to corresponding sequence of duplex DNA or messenger RNA of tumor cells forms local triple helices with the desired sequences [8–13]. Under light irradiation (in general, k > 300 nm where nucleic acids and most proteins are transparent), the PS is selectively excited to form active species, such as excited state or radical, which can induce site-specific cleavage of nucleic acid chains and cause damage to tumor cells [9]. Berberine (BBR, Scheme 1), an alkaloid, was initially isolated from a Chinese herbal medicine and used as an antibiotic. BBR’s antibacterial activity has been demonstrated against many bacterial species [14,15]. This drug was subsequently screened for anticancer activity following evidence of antineoplastic properties [16–18]. It has been discovered that BBR inhibits a number of enzymes, e.g. NADH oxidase, reverse transcriptase and diaminooxidase, topoisomerase; activator protein 1 and cyclooxygenase-2. BBR interacts in vitro with DNA, poly (A) fragments of mRNA and tRNA by intercalation and induces apoptosis through a mitochondria/caspase pathway in human hepatoma cells [19]. BBR has also been reported to be a photosensitive agent, which can produce singlet oxygen and radical species in the presence of UVA irradiation [20–22]. In our previous studies [23–25], we have identified that BBR can be excited by both 355 nm and 266 nm laser to produce BBR excited state (3BBR*), BBR radical anion (BBR) and BBR radical cation (BBR+). And the related photophysical and photochemical behaviors of them was also studied by time-resolved laser flash photolysis (LFP). All previous results show that BBR might be a new type of DNA-targeted PS using in PDT. Although BBR has potential importance as a PS in photobiology and photomedicine, few studies of DNA photo-damage initiated by BBR have been carried out. In this paper the photochemical and photobiological characters of BBR were studied in details to gain further insight into the important biological process and the pharmacological mechanism under physiological conditions. Its transient species were further identified and the related reaction kinetics was determined by use of time-resolved pulse radiolysis technique [26,27]. Furthermore, the possible photo-damage mechanisms of BBR to dGMP

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and DNA were studied by LFP, and the related photodynamic parameters were also obtained [28]. Experimental Materials BBR, 20 -deoxyguanosine 50 -monophosphate (dGMP) and calf thymus DNA were purchased from Sigma and used as received. Single strand DNA (ssDNA) was prepared by heating calf thymus DNA in neutral aqueous solution at 90 °C for 10 min following by chilling in an ice-salt bath [29]. Tert-Butyl alcohol (t-BuOH) was distilled before use. All solvents were of the highest available commercial grade except the water, which was triply distilled. The samples were prepared in 2 mM sodium phosphate buffer (pH 7.0) or in its mixture with acetonitrile, and purged with nitrogen (N2) or oxygen (O2) or nitrous oxide (N2O) for 20 min in different experimental situation. All experiments were carried out at room temperature. Pulse radiolysis Pulse radiolysis experiments were conducted using a linear accelerator providing an 8 MeV electron pulse determined by a thiocyanate dosimeter containing 20 mM KSCN solution saturated 3 1 with N2O, and by taking e cm1 at 480 nm. ðSCNÞ2 ¼ 7600 dm mol The light source used for the analysis was a 300 W Xenon lamp. The electron beam and the light beam pass perpendicularly through a quartz cell with an optical length of 10 mm. The transmitted light enter a monochromator equipped with a photomultiplier (Hamamatsu R955). Detailed descriptions of the setup of the pulse radiolysis equipment and experimental conditions have been given elsewhere [30]. In dilute aqueous solution, upon pulse radiolysis, three primary highly reactive species, hydrated electron (e aq ), hydroxyl radical (OH) and hydrogen atom (H), are produced with yields (G values) of 0.28, 0.28 and 0.06 lmol J1, respectively, in addition to the formation of other less reactive or inert molecular products (Hþ aq , H2 and H2O2) [31]. To create a reducing environment, t-BuOH was used to scavenge the OH [32], and e aq that remained. To create an almost uniform OH radical oxidizing solution environment, the sample solution was saturated with N2O before pulse radioly sis, where e aq is converted to OH [33], based on the reactions below: Radiolysis

H2 O ƒƒƒ! eaq ;  OH; H;Hþaq ; H2 ; H2 O2 

ð1Þ

OH þ ðCH3 Þ3 COH ! CH2 ðCH3 Þ2 COH þ H2 O k ¼ 6  108 M1 s1

eaq þ N2 O þ H2 O !  OH þ OH þ N2

k ¼ 9:1  109 M1 s1

ð2Þ ð3Þ

Laser flash photolysis

Scheme 1. Molecular structures of BBR.

LFP experiments were carried out using Nd:YAG laser of 355 nm light pulses with a duration of 5 ns and the energy of 60 mJ per pulse used as the pump light source. A 250 W Xenon lamp was employed as detecting light source. The laser and analyzing light beam passed perpendicularly through a quartz cell with an optical path length of 10 mm. The transmitted light entered a monochromator equipped with an R955 photomultiplier. The output signal from the Agilent 54830B digital oscillograph was transferred to a personal computer for data treatment. The LFP setup has been previously described [24].

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Results and discussion

to be one-electron reduction species, BBR [26]. And the related reaction mechanism could be supposed as bellow:

Generation of BBR radical anion by pulse radiolysis

eaq þ BBR ! BBR

ð310 nmÞ

To study the radical anion of BBR (BBR), pulse radiolytic experiments were carried out in neutral, N2 saturated, oxygen-free BBR solutions with an addition of 0.5 M t-BuOH to scavenge OH. A very strong broad band characterized by the peak at 700 nm (as shown in Fig. 1A) can be observed immediately after electron beam pulse. Furthermore, a new transient species with maximum absorption at 310 nm for BBR forms up accompanying with the decay of e aq . As shown in the inset of Fig. 1A, the formation process observed at 310 nm is synchronous with the decay of e aq recorded at 680 nm as here the signal is very strong with the transient absorption of hydrated electron. When the solution was saturated with N2O, all of them disappeared. Thus the new absorption at 310 nm is attributed

ð4Þ

The decay kinetics for e aq were monitored at 680 nm on the microsecond time scale with initial BBR concentrations ranging from 0.01 to 0.05 mM, see Fig. 1B. The decay curves were fitted to pseudo-first-order exponential kinetics and the second-order linear plot was shown in the inset of Fig. 1B. The slope of such a plot is the second-order rate constant for e aq reduction of BBR obtained as 3.5  1010 M1 s1. Generation of BBR radical cation by pulse radiolysis The transient absorption spectra with kmax = 460 nm obtained in pulse radiolysis of N2O-saturated aqueous solution containing

Fig. 1. (A) Transient absorption spectra from pulse radiolysis of N2-saturated aqueous solution containing 0.05 mM BBR and 0.5 M t-BuOH at pH = 7 recorded at: (j) 500 ns, (d) 1 ls, (N) 5 ls. Inset: The absorption-time profile at 310 nm (j) and 680 nm (s), respectively. (B) The absorption-time profiles at 680 nm with different concentrations of BBR. Inset: The observed e aq decay first-order rate constant (Kobs) recorded at 680 nm against BBR ground state concentration.

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0.10 mM BBR buffered with 2 mM phosphate is displayed in Fig. 2. The transient absorption band will disappear in the presence of tBuOH as an efficient OH scavenger. With combination of the absorption-time profile of 460 nm as shown in the inset of Fig. 2, it could be derived that the transient absorption with maximum absorption at 460 nm is from contribution of reaction of OH with BBR [34]. The OH is an unselective radical and reacts with substrates by multiple mechanisms such as electron transfer, addition and hydrogen abstraction [33,35,36]. Therefore, it is possible that the transient intermediates observed in the case of BBR could be an OH adduct or a one-electron oxidation product of BBR, or both. In order to understand the nature of the transient intermediate from OH with BBR, we compared the transient absorption spectra of the reaction between BBR and OH (Fig. 2) with the transient absorption of the BBR neutral radical (BBR(–H)), the product of rapid deprotonation of BBR+, obtained from one-electron oxidation by SO 4 in LFP experiment [25]. The result shows the same maximum absorption peak, which suggests that OH reacts with BBR through one-electron oxidation process. The related formation mechanism could be shown as bellows: 

OH þ BBR ! BBRþ þ OH pK a ¼4:6

BBRþ ƒƒƒ! BBRðHÞ þHþ

ð5Þ ð6Þ

ð460 nmÞ

From kinetic analysis of the growth trace of BBR(–H) at 460 nm, the observed first-order rate constant was obtained. By varying the concentration of BBR, a series of observed constants were obtained as shown in the inset b of Fig. 2, and the rate constant for reaction of OH with BBR was derived to be 6.7  109 M1 s1.

673

(4:1) mixtures, and the BBR(–H) was produced from rapid deprotonation of BBR+ generated by direct 355 nm photoionization [24,25]. Under this condition, only BBR(–H) could be detected, because 3BBR* (if it existed) would be quenched by oxygen and the electron should be trapped by acetonitrile to give a dimmer radical anion that did not absorb appreciably below 750 nm [40]. As shown in Fig. 3A, the transient absorption spectra after LFP of the BBR (0.05 mM) containing dGMP (0.1 mM) were obtained. On the basis of the molar absorption coefficient of dGMP at 355 nm is much less than that of BBR, the photon directly absorbed be dGMP can be neglected, which is further verified by performing a blank experiment. After the laser pulse (100 ns), the transient spectrum characterized be absorption maximum at 460 nm should be assigned to BBR(–H), which was identified by the reaction of OH with BBR in the former experiment. Accompanying the decay of BBR(–H), a new intermediate with absorption peaks at approximately 320 nm appeared. Owing to its similarity to the literature [41], it was assigned to the neutral radical of dGMP (dGMP(–H)), which was produced through one-electron oxidation of dGMP by BBR(–H) followed by deprotonation. As shown in the inset of Fig. 3A, the growth of the trace at 320 nm occurs exactly in the same time interval as the trace at 460 nm decay, which also indicates that BBR(–H) is the precursor of dGMP(–H). In addition, enhancement of the BBR(–H) decay was observed in the presence of dGMP, with rates roughly proportional to the concentration of dGMP (Fig. 3B). The bimolecular rate constant for the reaction of BBR(–H) with dGMP was determined to be 1.9  109 M1 s1 (the inset of Fig. 3B), and the related reaction mechanism could be shown as bellows: hv

ISC

BBR ! 1 BBR ! 3 BBR

ðPhotoexcitationÞ

Interaction of BBR(–H) with dGMP and DNA

BBR ! BBRþ þ eaq

DNA and its bases are the most important substrates in biological systems, guanine is the most easily oxidized base of them, and the photosensitized products of DNA mainly end up at guanine residues [37–39]. So dGMP and DNA were added as potential quencher of BBR(–H), respectively. Experiments were carried out in O2-saturated 2 mM phosphate buffer (pH 7.0)/acetonitrile

eaq þ 2CH3 CN ! ðCH3 CNÞ 2

hv

3

pK a ¼4:6

! ðBBR  HÞ

BBR þ O2 ! 1 O2 þ BBR

ðPhotoionizationÞ

ðEnergy transferÞ

dGMP þ 1 O2 ! Oxidation Product

ð7Þ ð8Þ ð9Þ ð10Þ ð11Þ

Fig. 2. Transient absorption spectra obtained in pulse radiolysis of N2O-saturated aqueous solution containing 0.10 mM BBR at pH 7.0 recorded at: (j) 100 ns, (d) 2.0 ls, (N) 35 ls. Inset: (a) The absorption-time profile at 460 nm. (b) The observed BBR(–H) set up first-order rate constant (Kobs) recorded at 460 nm against BBR ground state concentration.

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Fig. 3. (A) Transient absorption spectra from 355 nm excitation of 0.05 mM BBR in O2-saturated 2 mM phosphate buffer (pH 7.0)/acetonitrile (4:1) mixtures containing 0.1 mM dGMP, recorded at 100 ns (h) and 5 ls (d) after laser pulse. Inset: The absorption-time profile at 460 nm (j) and 320 nm (d), respectively; (B) Decay profiles of BBR(–H) observed at 460 nm in the presence of different concentrations of dGMP. Inset: Dependence of Kobs for BBR(–H) at 460 nm on concentration of dGMP. 



dGMP þ ðBBR  HÞ ! ðdGMP  HÞ þBBR ð320 nmÞ 9

k ¼ 1:9  10 M

1

1

s

ð12Þ

In order to have a better understanding of the mechanism of DNA photo-damage caused by BBR, LFP measurements were carried out on the interaction of BBR(–H) with DNA. Our results indicate that the decay of BBR(–H) were accelerated by addition both ssDNA and dsDNA. As shown in Fig. 4, the absorption spectra produced immediately after the laser pulse 100 ns were ascribed to BBR(–H), subsequently, the new transient species appeared after BBR(–H) decay in Fig. 4A and B should be from ssDNA and dsDNA, respectively. On the basis of the similarity of the transient absorption spectra of the radical species produced from the interaction of BBR(–H) with ssDNA and dsDNA to that of dGMP, it is concluded that BBR selective cleavage DNA at guanine moiety and the ultimate photo-damage species produced in ssDNA and dsDNA are DNA-guanyl radicals. The dependence of Kobs of BBR(–H) on concentrations of ssDNA and dsDNA was linear, and the bimolecular rate constants of the electron transfer reactions were determined to be 1.2  108 and 5.6  107 M1 s1, respectively. There are evidences showing that BBR can intercalate into DNA [19], which means the intramolecular photoinduced electron transfer should also be existent. However the electron transfer rate of this process is too quickly to be detected be nanosecond LFP,

Fig. 4. Transient absorption spectra from 355 nm excitation of 0.05 mM BBR in O2saturated 2 mM phosphate buffer (pH 7.0)/acetonitrile (4:1) mixtures containing (A) 1.2 mM ssDNA at delays of 100 ns (j), 10 ls (s), (B) 1.2 mM dsDNA at delays of 100 ns (j), 10 ls (s).

which should be detected by femtosecond LFP [42]. Therefore, the bimolecular rate constants of the electron transfer between BBR and DNA determined in our work is just the intermolecular electron transfer process. And the related reaction mechanism could be supposed as bellow:

ssDNA þ ðBBR  HÞ ! ðssDNA  Gua  HÞ þ BBR k ¼ 1:2  108 M1 s1

ð13Þ 

dsDNA þ ðBBR  HÞ ! ðdsDNA  Gua  HÞ þ BBR k ¼ 5:6  107 M1 s1

ð14Þ

In our previous work [24], the 3BBR* was identified under 355 nm laser excitation, which is the precursor of the singlet oxygen (1O2). And there are several report that the electron spin resonance (ESR) associated with spin-trapping techniques were used to detect 1 O2 generated by irradiation of BBR [19,21,43]. So the photo-damage of DNA should be caused by both BBR(–H) and active oxygen radicals, which means the set up profiles observed in the inset of Fig. 3A should be attribute to the associative reaction of BBR(–H) and 1O2. However in our experiment, the Kobs of BBR(–H) were used to determine the bimolecular rate constants, which exclude the effect of 1O2, and only concentrate on the reactive activity of BBR(–H) to biological molecules.

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Scheme 2. The possible interactions in the photosensitization of dGMP and DNA by BBR.

Reaction mechanism between BBR and DNA In our work, BBR absorbed UVA and visible light and was turned into 3BBR* and BBR(–H). The energy of the excited triplet state (ET) of BBR is 243 kJ/mol [24,44], while the ET of dGMP is 317 mJ/mol [45]. Consequently, energy transfer from 3BBR* to dGMP is unlikely to occur. However, the thermodynamic calculation shows that 3 BBR* is able to oxidize dGMP by electron transfer reaction. The standard free energy change (DG) in the process is calculated to be 16.4 kJ/mol, a highly exothermic process, according to the Rehm–Weller equation [46]:

DG ¼ 96:48ðEox  Ered  e2 =ea Þ  DE0;0 where e2/ea is the Coulombic term and can be neglected in aqueous solution, DE0,0 is the energy level of the excited triplet state, and Eox and Ered are the half-wave potentials in volts for the oxidation of electron donor and the reduction of an electron acceptor. It should be mentioned that the redox potentials of BBR/BBR and dGMP (–H)/dGMP are 1.06 V and 1.29 V (vs. NHE), respectively [47,48]. Therefore, it is obvious that photoinduced electron transfer is thermodynamically favored from dGMP to 3BBR*. Furthermore, it is also evident that 3BBR* can oxidize the guanine moiety of DNA through electron transfer process. The supposed reactions are shown as belows:

demonstrate that BBR owns the high electron affinity, as well as it can react with OH through one-electron oxidation process to produce its corresponding oxidized transient products efficiently. Then the photooxidation of dGMP and DNA in the presence of BBR was studied by using time-resolved photolysis. The results showed that BBR could cause photo-damage to DNA directly, and selective cleavage DNA at guanine moiety. Kinetic results suggested BBR(–H) could oxidize dGMP, ssDNA, and dsDNA via an electron transfer mechanism with rate constants 1.9  109, 1.2  108, and 5.6  107 M1 s1, respectively. Moreover, through thermodynamic calculation, the reaction mechanisms between 3 BBR* and dGMP or DNA were determined to be electron transfer process. Under aerobic condition, the photooxidation of dGMP and DNA by BBR involves both Type I and Type II processes. Photoinduced reactions of BBR with dGMP and DNA can occur through different pathways in different conditions (Scheme 2). All These results provide obvious implications for understanding the mode of BBR photodynamic action. Acknowledgments

3

BBR þ dGMP ! BBR þ dGMPðHÞ þ Hþ

ð15Þ

This work was supported by the National Natural Science Foundation of China (No. 11105089), Science Foundation for the Excellent Youth Scholars of Higher Education of Shanghai (No. ZZSD13020), and Innovation Fund of Shanghai University (No. SDCX2013034).

3

BBR þ DNA ! BBR þ ðDNA  Gua  HÞ þ Hþ

ð16Þ

References

3

*

Under the aerobic condition, BBR can be efficiently quenched by O2 (ET = 94 kJ/mol) via energy transfer to generate 1O2 [49–51]. As we know, 1O2 is a strong oxidizing agent and can induce further oxidation of DNA (Type II mechanism). Under the irradiation, BBR can also be photoionized to generate BBR(–H), especially in the polar solvents [25]. In this paper, the electron transfer from dGMP and the guanine moiety of DNA to BBR(–H) has been observed, which means BBR(–H) can oxidize DNA directly (Type I mechanism). Therefore, in the presence of O2, the photooxidation DNA involves both Type I and Type II processes, and Type I mechanism is competitive with 1O2. Which reaction is major pathway is dependent on the concentrations of O2 and the polar of the solvent. The possible mechanism of interactions in the photosensitization of dGMP and DNA by BBR was shown in Scheme 2. Conclusions In this work the time-resolved pulse radiolysis was used to observe the set up process of BBR and BBR(–H) directly, and the related set up rate constants have been obtained, which

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