Density functional theory study on hydrogen bonding interaction of luteolin–(H2O)n

Journal of Molecular Structure: THEOCHEM 911 (2009) 98–104

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Density functional theory study on hydrogen bonding interaction of luteolin–(H2O)n Lai-Cai Li a,*, Feng Hu a, Wan-Fei Cai a, An-Min Tian b, Ning-Bew Wong c a

Department of Chemistry, Sichuan Normal University, Chengdu 610066, People’s Republic of China Department of Chemistry, Sichuan University, Chengdu 610064, People’s Republic of China c Department of Biology and Chemistry, City University of Hong Kong, Kowloon, Hong Kong b

a r t i c l e

i n f o

Article history: Received 3 December 2008 Received in revised form 24 June 2009 Accepted 5 July 2009 Available online 10 July 2009 Keywords: Density functional theory Luteolin Hydrogen bond Natural bond orbital analysis Basis set superposition error

a b s t r a c t Density functional B3LYP method with 6-31++G  basis set is applied to optimize the geometries of the luteolin, water and luteolin–(H2O)n complexes. The vibrational frequencies are also studied at the same level to analyze these complexes. We obtained four steady luteolin–H2O, nine steady luteolin–(H2O)2 and ten steady luteolin–(H2O)3, respectively. Theories of atoms in molecules (AIM) and natural bond orbital (NBO) are used to investigate the hydrogen bonds involved in all the systems. The interaction energies of all the complexes corrected by basis set superposition error, are within 13.7 to 82.5 kJ/mol. The strong hydrogen bonding mainly contribute to the interaction energies, Natural bond orbital analysis is performed to reveal the origin of the interaction. All calculations also indicate that there are strong hydrogen bonding interactions in luteolin–(H2O)n complexes. The OAH stretching modes of complexes are redshifted relative to those of the monomer. Crown Copyright Ó 2009 Published by Elsevier B.V. All rights reserved.

1. Introduction Intermolecular hydrogen bonding interaction plays an important part in determining the structures and activities of organic, organometallic and biological molecules. The interaction between solute and solvent is especially significant in biological processes for pharmaceutical molecule [1–3]. For example, the stronger hydrogen bond is often associated with a higher and longer retention in background tissues, including blood. This indirect evidence suggests the activity of pharmaceutical molecule is also activated or restrained as well as the change of the structure in certain pharmacological processes by the hydrogen bond formation. Luteolin is one of the important polyphenols compounds. It has many biological and pharmacological activities including antioxidant, anti-inflammatory and anti-tumor effects which recently received considerable attention [4–8,3,9]. Luteolin is characterized by the presence of four hydroxyl groups, which can participate in hydrogen bond formations. These hydrogen bonds could stabilize the luteolin–solvent and luteolin–DNA interactions and play a crucial role in physiological processes. However, most studies have focused on the synthesis of novel luteolin derivatives which are more biological effective, higher energetic and low sensitive to the development of new synthetic schemes; and on the theoretical studies of structure, energy and stability in gas phase [10–12]. Recently, many theoretical studies have also been carried out to investigate the structures and activ* Corresponding author. Fax: +86 028 84761942. E-mail address: [email protected] (L.-C. Li).

ities of luteolin in solutions. Tsimogiannis and Oreopoulou [13] and his colleagues have calculated the spin density and ionization potential of luteolin in water by using density functional theory (DFT) methods. The results reveal that the biological activity of luteolin is associated to the structures and solvent effects. Amat et al. [14] have also used MP2 and DFT methods to investigate stabilities and solvent effects of luteolin, suggesting that solvent effects play an important role in the relative stability of luteolin in solutions. To our knowledge, intermolecular hydrogen bonding interaction between luteolin and solvent molecule has not been studied theoretically. Luteolin is a typical polyphenolic compounds which consists of OAH groups at different position of benzene ring, and water is one of the simplest and most important polar solvents. Thus, complex of luteolin–water can serve as a model system for luteolin–solvent interaction. Theoretical investigation on these intermolecular hydrogen bonding interactions can provide many important facts revealing the nature of the interaction for luteolin–solvent system. This paper will examine the intermolecular hydrogen bonding interactions of luteolin with water and probe the origin of the interactions. These must be very useful to study structures and pharmacological activities in physiological processes for luteolin pharmaceutical molecules.

2. Computational details It has been demonstrated that density functional theory (DFT) method is more reliable than ab initio for the computation of

0166-1280/$ - see front matter Crown Copyright Ó 2009 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.theochem.2009.07.004

L.-C. Li et al. / Journal of Molecular Structure: THEOCHEM 911 (2009) 98–104 Table 1 Main optimized geometrical parameters of luteolin at different level of theory (bond length in nm). Bond 7

11

C AC C7AC10 C10AO13 C21AO25

B3LYP/6-31++G 

B3LYP/6-31+G [16]

Exp [22]

0.1406 0.1465 0.1374 0.1360

0.1409 0.1470 0.1365 0.1364

0.1384 0.1458 0.1377 0.1349

molecular structures, vibrational frequencies and energies [15]. All the possible orientations of water towards luteolin have been fully optimized at B3LYP/6-31++G level and twenty-three complexes

99

corresponding to the minimum energy points have been got. Meanwhile, the frequency analyses of the 23 complexes have been carried out and the result indicates that there is no imaginary frequency. To further insight into the nature of hydrogen bonding interaction, AIM analysis is performed by using AIM2000 [16]. The analyses of the charge distribution and charge-transfer processes have been carried out with the NBO partitioning scheme [17]. The hydrogen bonding interaction energies are corrected for the basis set superposition errors (BSSE). The BSSE has been evaluated by using the counterpoise (CP) method proposed by Boys and Bernardi. The uncorrected (De) and corrected (DeBSSE) interaction energies [18] can be evaluated using Eqs (1–3).

Fig. 1. Hydrogen bonding structures of the luteolin–(H2O)n at B3LYP/ 6-31++G** level. abond length(nm); bbond angle(°); ccharge density q in the bond critical point (a.u.).

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Fig. 1. (continued)

a b De ¼ Eab AB ðABÞ-EA ðAÞ-EB ðBÞ h i h i ab b BSSE ¼ EaA ðABÞ-Eab A ðABÞ þ EB ðABÞ-EB ðABÞ BSSE

De

¼ De þ BSSE

ð1Þ ð2Þ

3. Results and discussion 3.1. Geometries of the complexes

ð3Þ

where the subscripts A, B, and AB denote the molecular systems, the superscripts a, b, and ab denote the monomer- and dimer-centered basis sets, and the notations in round brackets denote that they are calculated at the optimized geometry of the (sub)system A, B and AB, respectively. For example, Eab A ðABÞ is the energy of A at the equilibrium of AB, and calculated in the dimer-centered basis sets. All calculations are carried out by using the Gaussian 03 program [19].

The optimized geometry parameters of luteolin at different level of theory and the X-ray data available for luteolin are reported in Table 1. It can be seen that the main optimized geometry parameters of luteolin obtained by the various level are approximately similar. But theory bond distances are longer than the experimental ones. This may be due to the neglect of the electron correlation; on the other hand, experimental bond distances come from crystal structure data instead of those in gas phase. From our calculations,

L.-C. Li et al. / Journal of Molecular Structure: THEOCHEM 911 (2009) 98–104

101

Fig. 1. (continued)

geometric parameters obtained by using B3LYP at 6-31++G basis set level reproduces the experimental values most satisfactorily for the luteolin. B3LYP/6-31++G geometry optimizations and frequency calculations are performed for the luteolin–waters complexes, so various stable structures are obtained based on the structures with

real frequencies. Their fully optimized geometry parameters are also shown in Fig. 1. AIM provides a way of mapping topological properties of the electron density to Lewis structure representations of molecules. The nature of bonding between atoms can be characterized by the value of the electron density at the bond critical point (BCP).

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Table 2 Interaction energies without (DE) and with the BSSE correction (DE0 , kJ/mol) for all the complexes, calculated at the B3LYP/6-311++G  level. Species

BSSE

DE

DE0

Species

BSSE

DE

DE0

B D F J I L N Q T S U X

0.000833 0.000970 0.001822 0.003247 0.002738 0.003492 0.003682 0.004524 0.004628 0.003763 0.004729 0.004112

15.9 24.3 41.0 53.9 51.5 58.3 62.9 76.3 84.2 81.7 87.6 101.3

13.7 21.8 36.2 42.1 44.3 49.1 53.2 56.3 64.1 71.8 75.2 82.5

C E G H K M O P R V W

0.000898 0.001860 0.002858 0.002628 0.003739 0.002825 0.003761 0.003452 0.003657 0.005402 0.004106

17.6 40.4 50.7 50.7 57.4 59.4 67.5 67.1 79.9 96.5 98.3

15.2 35.5 39.8 43.8 44.6 52.0 49.6 58.1 70.3 74.3 79.6

Large q (r) values represent shared interactions, characteristic of covalent bonds. In contrast, low q (r) values are indicative of closed-shell interactions typically found in ionic bonds and hydrogen bonds as well as in van der Waals interactions. Koch and Popelier propose the criteria of hydrogen bonding, which is the value of q(r) at BCP of H. . .Y lies within the range of 0.002–0.040 a.u [20,21]. From Fig. 1 it can be seen that the values of q (r) for each complex are in the range of 0.0100–0.0400 a.u. The optimized structures of the luteolin–H2O are illustrated in Fig. 1. For complexes (E), the distance of hydrogen bond (0.1797 nm) is relatively short, the bond angle (177.9°) and electron density at the bond critical point (0.0335 a.u) are larger than others. The interaction energy of complex (E) is the largest (see Table 2), and it is the most stable one in those complexes. After corrected by the basis set superposition errors, the interaction

energies are in the order: E > D > C > B. Thus it can be seen that the interaction energies and the strength of hydrogen bonds are in the same order, and the hydrogen bonds play an important role in intermolecular interaction. We got nine complexes of luteolin–(H2O)2 through the calculation, they are F, G, H, I, J, K,L,M,N listed in Fig. 1., respectively. The lower the energies of these complexes are, the higher the interaction energies of them are. The OAH. . .O hydrogen bonds formed in those complexes, the bond distance, bond angle and electron density at the bond critical point for each of them are within the rang of 0.1700–0.2400 nm, 152.0°–178.0° and 0.0100–0.0400 a.u., respectively. It means that the OAH. . .O hydrogen bond between water and luteolin is strong. In the minima G, J and K, a cycle hydrogen bonding network is formed, and the hydrogen bonding distance is close to the standard hydrogen bond length. For complex (N), the hydrogen bonding interaction is the strongest, the bond distances of O32. . .H29 and O34. . .H6 are 0.1832 nm and 0.1803 nm; bond angles are176.8° and 177.6°; electron densities at the bond critical point are 0.0312, 0.0329 a.u. For complex (F), the hydrogen bonding interaction is the weakest. From the Fig. 1, we can see the distance of O33. . .H26 (0.1984 nm) and O25. . .H35 (0.2036 nm) are relatively longer, the bond angles (153.2° and 159.7°) and electron densities at the bond critical point (0.0223 and 0.0203 a.u) are relatively smaller. As we can see from Table 2, the complex (N) is the most stable one in those complexes. However, the complex (F) is on the contrary. We have got ten complexes of luteolin–(H2O)3 through the same method, the interaction energies are reported using ascending order. And calculations indicated that the complex (X) have strong hydrogenbonding interaction, and the complex have a OAH. . .O hydrogen bond and a chain of water molecules which is terminated by a OAH. . .C hydrogen bond. From data of Table 2, we discovered that

Table 3 Electron donor orbital, electron acceptor orbital and their corresponding second-order interaction energies E(2). Species

Donor

Acceptor

E(2) kJ/mol

Species

Donor

Acceptor

E(2) kJ/mol

B D F

LP(1)O25 LP(1)O26 LP(1)O26 LP(1)O25

BD (1)O32AH33 BD (1) O32AH33 BD (1) O32AH33 BD (1) O34AH35

14.14 15.98 14.18 15.67

C E G

H

LP(2)O26 LP(2)O34 LP(2)O32 LP(2)O34 LP(1)O12 LP(2)O32 LP(2)O34 LP(1)O32 LP(2)O34

BD (1)O32AH33 BD (1) O12AH14 BD (1)C11AH16 BD (1)O32AH33 BD (1)O34AH35 BD (1) O12AH14 BD (1) O3AH6 BD (1)O25AH29 BD (1)O3AH6

14.97 42.80 15.78 33.05 15.56 40.04 39.62 37.20 49.96

I

P

LP(1)O26 LP(2)O25 LP(2)O36

BD (1)O32AH33 BD (1)O34AH35 BD (1)O12AH14

18.56 16.45 43.39

Q

R

LP(1)O26 LP(2)O25 LP(2)O36 LP(1)O26 LP(2)O34 LP(2)O36 LP(1)O3 LP(1)O32 LP(1)O34 LP(1)O36 LP(1)O3 LP(2)O32 LP(2)O36 LP(1)O34 LP(1)O36

BD (1)O32AH33 BD (1) O34AH35 BD (1) O3AH6 BD (1)O32AH33 BD (1)O12AH14 BD (1) O34AH35 BD (1)O36AH37 BD (1)O25AH29 BD (1)O12AH14 BD (1)O34AH35 BD (1)O36AH37 BD (1)O12AH14 BD (1)O34AH35 BD (1)O3AH6 BD (1)C2AH1

15.75 16.73 40.08 17.55 45.19 32.17 14.05 36.02 44.18 30.38 15.06 40.56 31.38 55.48 15.63

S

LP(2)O12 LP(2)O32 LP(2)O25 LP(2)O32 LP(2)O34 LP(2)O32 LP(2)O12 LP(2)O32 LP(2)O35 LP(1)O3 LP(1)O26 LP(1)O34 LP(1)O26 LP(2)O25 LP(1)O36 LP(1)O25 LP(2)O32 LP(2)O34 LP(2)O36 LP(1)O26 LP(2)O12 LP(2)O36 LP(2)O32 LP(2)O12 LP(2)O36

BD (1)O32AH33 BD (1) O3AH6 BD (1) O32AH33 BD (1) O34AH35 BD (1)C19AH23 BD (1) O25AH29 BD (1) O34AH35 BD (1)O12AH14 BD (1)O32AH34 BD (1)O35AH36 BD (1) O32AH33 BD (1) O3AH6 BD (1)O32AH33 BD (1)O34AH35 BD (1)C19AH23 BD (1)O32AH33 BD (1) O34AH35 BD (1)C19AH23 BD  (1) O12AH14 BD (1)O32AH33 BD (1)O34AH35 BD (1) O3AH6 BD (1)O25AH29 BD (1)O34AH35 BD (1)O3AH6

15.23 41.17 17.36 30.08 14.36 35.77 18.12 46.58 32.17 15.68 24.28 41.17 15.73 14.65 15.29 18.67 30.08 18.25 43.31 15.62 19.23 41.1 38.16 39.92 39.62

LP(1)O25 LP(2)O32 LP(1)O34 LP(2)O36

BD (1)O32AH33 BD (1)O34AH35 BD (1)O36AH37 BD (1)C11AH16

17.87 37.03 32.43 16.69

J

L N

T

V

X

K

M O

U

W

103

L.-C. Li et al. / Journal of Molecular Structure: THEOCHEM 911 (2009) 98–104 Table 4 The change of corresponding stretching vibration (cm1) and infrared intensities (km/mol) for the main OAH bond. Species B D F H J L N P

R

T

V

X

DtOAH

OAH. . .O 32

33

25

DIOAH

Species

O AH . . .O O32AH33. . .O26 O32AH33. . .O26 O34AH35. . .O25 O32AH33. . .O26 O12AH14 . . .O34 O32AH33 . . .O34 O34AH35 . . .O12 O12AH14. . .O32 O3AH6. . .O34 O25AH29. . .O32 O3AH6 . . .O34

88.7 128.8 89.2 120.4 124.2 254.6 312.6 179.7 258.6 253.5 207.3 241.7

108.6 164.0 104.8 232.1 267.2 1103.7 383.7 366.4 924.7 1094.7 858.3 1336.8

C E

O32AH33. . .O26 O34AH35. . .O25 O12AH14 . . .O36 O32AH33. . .O26 O34AH35. . .O25 O3AH6 . . .O36 O32AH33. . .O26 O12AH14. . .O34 O36AH37 . . .O3 O25AH29. . .O32 O12AH14. . .O34 O36AH37 . . .O3 O12AH14. . .O32 O34AH35. . .O36 O3AH6 . . .O34

164.4 102.3 309.4 124.4 92.7 248.9 124.9 341.6 142.7 203.4 327.7 155.8 259.3 199.7 427.8

291.8 214.1 1082.5 241.8 118.9 1255.5 252.7 1310.1 528.7 973.0 1179.4 550.4 847.3 373.7 1662.7

Q

the interaction energies of 1:2 and 1:3 complexes are 1.5 and 1.7 times of 1:1 complexes. It indicates bonding energy has the additive property when water affects the different hydroxyl function of luteolin, which is in agreement with the conclusion of the Refs. [22,23]. As is known, cooperativity effects play an important part in studying the hydrogen bond. Yanez et al. [24,25] have investigated the cooperativity effects in water trimers, it has been found that the cooperativity effect enhances significantly the hydrogen bond; Yanez [26,27] and his colleagues also have investigated the cooperativity effects of AHXHYH3 (A = F, Cl; X = F, Cl; Y = N, P) hydrogen bonding complexes, and get the same conclusion. In our paper, A cycle hydrogen bonding network is formed in complexes G, J, K, O, Q, T, V, W, and X, respectively. In order to discuss cooperative effects we have evaluated additive interaction energies at the B3LYP/6-311++G level, which are defined by the equation [28]:

DEadd ¼ DEABC  DEAB  DEBC  DEAC The values of the additive interaction energies are summarized in Table 2, which clearly show the enhancement of hydrogen bond by cooperativity effects. And the conclusion is in agreement with that of the Refs. [24–27]. 3.2. NBO analysis The role of hydrogen bonds is to exert external electric field on the luteolin elements, which cause the separation of charge within molecules and lead to changes in the structure of molecules. Natural bond orbital analysis was performed to reveal the nature of the interaction. Electron donor orbital (i), electron acceptor orbital (j) and their corresponding second-order interaction energies E(2) of the luteolin–(H2O)n are listed at Table 3. The higher the E(2) is, the stronger the interaction between (i) and (j) is, which means that (i) is easier to provide electron to (j) [29,30]. From Table 3 and Fig. 1 we can conclude that the interaction where the oxygen of water offers lone pairs to the contacting OAH anti-bond orbital of the luteolin is stronger, and E(2) lies

G I K M O

S

U

W

OAH. . .O 32

33

12

O AH . . .O O3AH6 . . .O32 O32AH33. . .O25 O34AH35. . .O32 O25AH29. . .O32 O34AH35. . .O12 O12AH14 . . .O32 O32AH34. . .O35 O32AH33 . . .O26 O3AH6 . . .O34 O32AH33. . .O26 O34AH35. . .O25 O36AH37 . . .O34 O32AH33. . .O25 O34AAH35. . .O32 O12AH14 . . .O36 O32AH33. . .O26 O34AH35. . .O12 O3AH6 . . .O36 O25AH29. . .O32 O34AH35. . .O12 O3AH6 . . .O36 O32AH33. . .O25 O34AH35. . .O32 O36AH37 . . .O34

DtOAH

DIOAH

97.4 255.6 130.0 214.1 203.9 96.9 254.6 216.2 125.2 256.3 88.9 104.0 173.8 136.9 218.8 305.8 127.6 95.6 283.9 206.8 283.3 233.9 149.8 280.5 217.2

104.1 1347.0 432.4 299.7 959.4 123.6 916.6 373.6 267.5 1273.4 162.3 315.4 218.8 434.1 247.6 1403.2 272.9 128.1 1387.5 798.1 953.8 1259.3 386.0 610.9 408.4

within the range of 35.77–55.48 kJ/mol. but the interaction where the oxygen of luteolin offers lone pairs to the contacting OAH antibond orbital of the water is smaller than the former, the corresponding E(2) lies within the range of 14.14–25.00 kJ/mol. This indicates the oxygen of water is liable to offer electrons to the luteolin than the oxygen of luteolin, and the formed hydrogen bonding interaction is strong, and the corresponding complex is stable. The interaction between oxygen lone pairs in water and the contacting OAH anti-bond orbital of the luteolin exists in the most stable complexes E N and X, and E(2) are 41.17, 37.20 and 49.96 kJ/mol, a bit higher. Hydrogen bonding interaction in E and N are stronger, which is consistent with the former analyzed structure data and energy analysis. We can also conclude that the interaction between oxygen lone pairs in luteolin and the contacting OAH anti-bond orbital of the water exists in the instable complexes C and F, and E(2) are lower than 16.00 kJ/mol. Hydrogen bonding interactions in C and F are weaker, the stabilities are lower. Through analysis, we have found the same features exist in complexes of luteolin– (H2O)3. 3.3. Vibrational frequencies We calculated the stretching vibrational frequencies of OAH bond at the B3LYP/6-31++G levels. From Table 3, it can be seen that the OAH stretching vibrational frequencies move to the low wave number direction and the corresponding stretching vibration intensity is larger than that in the monomer. The most stable complexes is (E), (N) and (X) for luteolin–H2O, luteolin–(H2O)2, luteolin–(H2O)3, respectively. The interaction energies of them becomes higher gradually and they are 35.5, 53.2 and 82.5 kJ/mol, respectively; And it is clear that the calculated frequency of OAH stretching in complexes (E), (N) and (X) is obviously decreased, compared with that of the monomer. From Table 4, we can know the change tendency of red-shift and interaction energies are in the same order. This shows that the stronger the hydrogen bonding interaction in complexes is, the bigger its affection on vibrational frequencies is.

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4. Conclusions Density functional B3LYP method with 6-31++G basis set is applied to optimize the geometries of the luteolin–(H2O)n complexes. The vibrational frequencies are also studied at the same level to analyze these complexes. We have obtained four stable luteolin–H2O, nine stable luteolin–(H2O)2 and ten stable luteolin– (H2O)3 respectively. We have discovered the interaction energies of 1:2 and 1:3 complexes are 1.5 and 1.7 times of 1:1 complexes respectively, which show that the bonding of water on different hydroxyl function of luteolin has the additive property. From vibration frequencies analysis, we can know the OAH vibrational frequencies had moved to the low wave number direction and the corresponding stretching vibration intensity is increased after the formation of OAH. . .O hydrogen bond. This shows OAH. . .O bonds are typically red- shifted, the change tendency of red-shifted and interaction energies are in the same order. References [1] [2] [3] [4] [5] [6] [7] [8] [9]

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