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European Journal of Applied Sciences – Vol. 10, No. 3

Publication Date: June 25, 2022

DOI:10.14738/aivp.103.12352. Atse, A. J., Diomande, S., Kone, S., & Bamba, E. S. (2022). Lipophilicity and Interactions Properties of a Group of Thirteen

Manzamenones in Comparison with Artemisinin and Quinine Using Quantum Chemical Methods: ONIOM and DFT (B3LYP).

European Journal of Applied Sciences, 10(3). 258-274.

Services for Science and Education – United Kingdom

Lipophilicity and Interactions Properties of a Group of Thirteen

Manzamenones in Comparison with Artemisinin and Quinine

Using Quantum Chemical Methods: ONIOM and DFT (B3LYP)

ATSE Adepo Jacques

Laboratoire de Constitution et de Réaction de la matière de L’UFR

SSMT Université Félix Houphouët Boigny 22 BP 582 Abidjan 22

DIOMANDE Sékou

UFR Agriculture, Ressources Halieutiques et Agro-industrie

Université de San Pedro

KONE Soleymane

Laboratoire de Constitution et de Réaction de la matière de L’UFR

SSMT Université Félix Houphouët Boigny 22 BP 582 Abidjan 22

BAMBA El-Hadji Sawaliho

Laboratoire de Constitution et de Réaction de la matière de L’UFR

SSMT Université Félix Houphouët Boigny 22 BP 582 Abidjan 22

ABSTRACT

This work was undertaken to determine and compare the lipophilic properties of a

group of Manzamenones with those of two antimalarials (Quinine and Artemisinin).

Manzamenones are atypical fatty acid derivatives, belonging to the large family of

lipids. They are extracted from a marine sponge, of the genus Plakortis kenyensis,

used in the treatment of malaria. Three approaches were used to estimate the

lipophilicity values of the molecules. Secondly, we analyzed the intermolecular

interactions between these molecules and each of the two probes: the water

molecule and the 3-aminopropanoic acid molecule (alanine: a protein residue of the

polymerase). Manzamenones are studied with a mixed method: ONIOM 2. The

intermolecular interactions between Manzamenones and water are described at

the B3LYP/6-31++G(d,p) level. The ones between Manzamenones and 3-

aminopropanoic acid are described at B3LYP/6-31+G(d,p). The last part of the

study was the determination of energetic parameters and the estimation of the

relative stabilities of the complexes formed with the two probes. This part allowed

making comparisons with Quinine or Artemisinin.

Keywords: Manzamenone, Artemisinin, Quinine, lipophilicity, hydrogen bond, level of

theory

INTRODUCTION

Malaria is a parasitic disease caused by the infection of erythrocytes by a hematophagous

protozoan of the species Plasmodium. It is transmitted to humans through the bite of an

infected female Anopheles mosquito [1]. Malaria is one of the principal causes of death of

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Atse, A. J., Diomande, S., Kone, S., & Bamba, E. S. (2022). Lipophilicity and Interactions Properties of a Group of Thirteen Manzamenones in

Comparison with Artemisinin and Quinine Using Quantum Chemical Methods: ONIOM and DFT (B3LYP). European Journal of Applied Sciences,

10(3). 258-274.

URL: http://dx.doi.org/10.14738/aivp.103.12352

children in the world . Despite more than a century of control efforts, it remains one of the major

diseases in tropical areas. In Africa, malaria infection is one of the main causes of death [3].

Regardless of WHO's efforts, the African region still accounts for approximately 92% of malaria

cases and deaths worldwide. This disease is caused by five parasites of the genus Plasmodium.

However, the majority of deaths are caused by Plasmodium falciparum and Plasmodium vivax

[4,5-7]. Quinine, Quinoline, Mefloquine and Artemisinin used to be effective treatments for

malaria.

Since about 25 years, the parasite has been developing resistance to the main classes of drugs.

Quinine, usually used in severe cases, has shown resistance [8, 9, 10]. Manzamenones from

marine sources derived from sponges are becoming increasingly extracted and used in drug

diversification for the treatment of malaria [11]. They are atypical fatty acid derivatives,

belonging to the large family of lipids. These molecules have antifungal, anticancer,

antimicrobial, enzymatic and antibacterial activities [12, 13]. Some work has shown that

Manzamenone A is a potent inhibitor of β DNA polymerase and only weakly active against the

α form of the enzyme [11, 14, 15, 16]. A previous study allowed us to compare some molecular

parameters including the interaction sites of Manzamenones with those of Quinine and

Artemisinin [17]. The present study first compares the lipophilic properties of thirteen

Manzamenones with two antimalarials. These results will allow knowing the ability of these

molecules to migrate to the blood lipoproteins. The lipophilic properties are estimated with

three different software. In a second part, a more elaborate analysis of intermolecular

interactions was performed. The aim of this part is to specify the binding mode(s) in biological

sites. The interactions are calculated between the studied molecules and a water molecule

(complexes) and then the 3-aminopropanoic acid (Alanine) a protein residue of the

polymerase. The calculations also allow examining the relative stability of the complexes. Some

similarities between the Manzamenones and the selected antimalarial drugs are investigated.

All calculations are performed in the gas phase. A mixed method of quantum chemistry is used

for the calculations of Manzamenones; ONIOM 2. Quinine and Artemisinin are described with

the DFT method (B3LYP).

STUDIED MOLECULES AND CALCULATION METHODS

Studied molecules

The studied molecules in this work are the two antimalarials Quinine and Artemisinin used as

references figure 1 and the fourteen (14) Manzamenones listed in the literature figure 2.

Artemisinin

Figure 1 : Structures of Quinine and Artemisinin

N

O

HO

N

H

Quinine

H3C H

O

O

CH3

H

H CH3

O

H3C O

O

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European Journal of Applied Sciences (EJAS) Vol. 10, Issue 3, June-2022

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A B C D

E F

H

L M N

G J K O

Figure 2: 2D structures and refcodes of the fourteen Manzamenones listed in the literature.

Calculation methods

Partition coefficient or molecular lipophilicity

The logarithm of the partition coefficient (logP) is a parameter combining several effects such

as non-covalent interactions, solvation and an entropic component. For a studied substance, it

is expressed by the logarithm of the ratio of the concentrations in octanol and in water.

���� = ��� %

!!"#$%!&

!'$(

&

This value allows understanding the hydrophilic or hydrophobic (lipophilic) character of a

molecule. Indeed, if logP is positive (logP > 0) and very high then the considered molecule is

much more soluble in octanol than in water. The various theoretical methods used to determine

theoretically lipophilicity are briefly described.

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Atse, A. J., Diomande, S., Kone, S., & Bamba, E. S. (2022). Lipophilicity and Interactions Properties of a Group of Thirteen Manzamenones in

Comparison with Artemisinin and Quinine Using Quantum Chemical Methods: ONIOM and DFT (B3LYP). European Journal of Applied Sciences,

10(3). 258-274.

URL: http://dx.doi.org/10.14738/aivp.103.12352

Three freeware programs were used to perform these calculations. They are

MOLINSPIRATION, ACD/ChemSketch(Freeware)2016.2.2 and EPIWEB [18, 19, 20]. These

programs are known respectively under the names: MI/logP, ACD/logP and KowWIN/logP. The

mi/logP software is available from vcclab.org. This calculation approach is based on functional

groups. It takes into account intramolecular H-bonds and charge interactions. The ACD/logP

approach is based on the contributions of the atoms and structural fragments taken separately.

It takes into account the intramolecular interactions between the different fragments.

KowWIN/logP is a method that takes into account steric interactions between atoms, the H

bond and polar substructure effects.

With the ACD/logP approach, if fragmentary and interaction contributions are not in the

internal database, a special secondary algorithm is used to calculate them. The values from the

ACD/logP calculations are provided with an error equal to 0.6 [19]. Any greater error reflects

that the compound studied is not the database of the ACD/logP program. It is a new compound.

ONIOM method

The ONIOM method consists in dividing the studied system into several layers, each of them

being treated at a different level of calculation. In our case, the system is two-layered (ONIOM2)

as shown in Figure 3. The interactions between the water molecule or the alanine molecule and

the model system are studied at two different ONIOM levels (B3LYP / Base). In both types of

complexes, the real system is studied with the AM1 method. In a previous work [17], we have

shown the compatibility of the two levels of theory chosen to study these two layers in

Manzamenones.

Figure 3: Splitting model of a Manzamenone A complex with the ONIOM 2 method

.

Software and levels of quantum computation theory

The calculations are performed with the Gaussian 09 software [21]. The method used is the

density functional theory (DFT) [22]. Previous theoretical work on molecular properties

calculations has shown that hybrid functionals such as B3LYP and others, combined with an

extended base of functions lead to values in good agreement with experimental results [23]. An

optimization calculation of the molecular geometry is followed by the vibration frequencies for

each structure.

The calculations of the complexes with the water molecule are performed using the ONIOM

method (B3LYP / 6-31 ++ G (d, p): AM1). Those of the complexes formed with the alanine

External

layer (real

system)

Internal layer

(model

system)

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European Journal of Applied Sciences (EJAS) Vol. 10, Issue 3, June-2022

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molecule are carried out using ONIOM (B3LYP / 6-31+G (d, p): AM1). The choice of the ONIOM

method, developed by Morokuma et al [24-26], is justified by the fact that it has been

successfully used to study big size molecules [27-30].

Description of the hydrogen bond

Hydrogen bond (HB) results from an attractive interaction between a hydrogen atom

covalently bonded to a strongly electronegative donor atom such as nitrogen, oxygen, fluorine

or carbon and a similar acceptor atom, which may or may not be part of the same molecule as

the donor. The geometric analysis of this bond is performed according to the recommendations

of Desiraju and Steiner [31], which suggest the characteristic parameters α, θ, d and D defined

in Figure 4.

Figure 4: Geometric parameters α, θ, d and D to describe hydrogen bond.

Energy parameters of interactions

The formation of a hydrogen bond between a donor molecule H ̶X and an acceptor molecule Y ̶

A results in the reaction 1. The hydrogen bond complex Y ̶A--- H ̶X is the product. The variation

of the energy, at 298.15 K is given by equation (2).

Y ̶A + H ̶X → Y ̶A···H ̶X (1)

Δ� = �(Y ̶A···H ̶X) − [E(Y ̶A) + E(H ̶Y)] (2)

The internal energy, at 298.15 K, corresponds to the sum of the electronic, rotational,

translational and vibrational contributions, so that its variation can be written according to

equation (3):

Δ�"#$ = Δ�%&%'+ Δ�()*+ Δ�+,- (3)

The optimization of the reactant and product geometry gives access to all contributions. The

translational contributions are given by equation (4):

Δ�*(./0= Δ�()* = ̶ 1

"

RT (4)

ΔE_vib includes the Zero Point Vibrational Energy (ZPVE), which is the energy of the lowest

vibrational level at 0 K. Taking into account the additional energy due to the vibrational levels

of the population, the increase in temperature from 0 to 298.15 K thus leads to equation (5),

from which the term E can be derived:

�+,-,*3%(4.&= R ∑ 3+)/6

%*+)⁄,-./78

197:

,;8 (5)

Therefore, the internal energy variation at 298.15 K is given by equation (6):

Δ�"#$ = Δ�%&%' + ΔZPVE + Δ�+,-,*3%(4.& ̶ 3RT (6)

atome

donneur

(C,N, O,...)

H

atome

accepteur

(N, O, F,...)

D

d

X Y

a

q

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Atse, A. J., Diomande, S., Kone, S., & Bamba, E. S. (2022). Lipophilicity and Interactions Properties of a Group of Thirteen Manzamenones in

Comparison with Artemisinin and Quinine Using Quantum Chemical Methods: ONIOM and DFT (B3LYP). European Journal of Applied Sciences,

10(3). 258-274.

URL: http://dx.doi.org/10.14738/aivp.103.12352

The variations, at 298.15 K, of enthalpy and free enthalpy are respectively given by equations

(7) and (8), and the variation of entropy, by equation (9)

Δ�"#$<

= = Δ�"#$< ̶ RT (7)

Δ�"#$<

= = Δ�"#$<

= ̶ TΔ�"#$<

= (8)

Where

Δ�"#$<

= = Δ�*(./0

= + Δ�()*

= + Δ�+,-

= (10)

Results and discussion

The molecular lipophilicity

The calculated lipophilic values of the two antimalarials (Artemisinin and Quinine) and the

Manzamenones are reported in Table 1.

Table 1: Lipophilic values of Artemisinin, Quinine and Manzamenones calculated with the three

software

softwares ACD/logP KOWWIN/logP Mi/logP logP (average)

Artemisinin 2.27±0.68 2.85 3.32 2.81

Quinine 3.44±0.43 3.29 3.06 3.26

A(B) 17.17±0.39 15.93 10.25 14.45

C 17.59±0.39 16.71 10.35 14.88

D 15.69±0.40 14.68 10.20 13.52

E 16.82±0.38 16.55 10.15 14.51

F 18.66±0.39 17.69 10.45 15.60

G 17.70±0.41 16.71 10.34 14.92

H 16.32±0.45 17.75 10.25 14.77

J 16.25±0.41 14.81 10.18 13.75

K 15.46±0.51 13.57 10.00 13.01

L 17.35±0.43 14.71 10.22 14.09

M 16.39±0.42 14.43 10.15 13.66

N 17.66±0.40 16.34 10.30 14.77

O 22.33±0.57 20.48 10.73 17.85

The errors are less than 0.6 except for Artemisinin where the uncertainty is equal to 0.68. Only

this molecule is not in the ACD/Labs software database. All calculated lipophilicity values are

positive. These molecules (Manzamenones and antimalarials) are therefore naturally lipophilic.

They are then potentially biologically active.

For each molecule, the ACD/LogP method predicts a higher value of lipophilicity. The MI/LogP

approach suggests the smallest value. The ACD/LogP and KOWWIN/logP calculations give

closer values. The average values of the three calculation approaches are between 13 and 17.

They are therefore high. The comparison with the two antimalarials shows very clearly that

Manzamenones are much more lipophilic than Artemisinin and Quinine. According to the

theoretical values obtained, Manzamenones are 3 to 6 times more lipophilic. All three

calculation approaches classify Manzamenone O as more lipophilic.

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Lipophilicity is an important molecular property in predicting the pharmacological activity of a

molecule. Its division between a lipidic phase and an aqueous phase [32, 33] can condition its

transport, its transit through the membranes. Biological membranes being lipophilic, the

greater the degree of lipophilicity, the better the molecule crosses them and migrates to the

lipoproteins of the blood. The role of blood lipoproteins is to supply cells with lipid substances.

According to our calculations, the model systems of Manzamenones are excellent "candidates"

to ensure this function.

Geometric characteristics of hydrogen bonds

The numbers assigned to the heteroatoms and hydrogen-carrying carbon atoms of Artemisinin,

Quinine and the Manzamenone model system are specified on the optimized (3D) structures

shown in Figure 5.

Artemisinin Quinine A(B), C, D, E, F et H

L, M et N G J

K O

Figure 5: 3D structures showing the numbers of the heteroatoms of the hydrogen-carrying

carbons

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determined [17]. The results in Table 2 confirm the implication of these sites of the two

reference molecules. Especially with Quinine, the oxygen O39 as acceptor and the hydrogen of

the group O22H as donor interact with the water molecule. We obtain for this complex a

multicentric interaction. For most of the Manzamenones (10/13), the interaction takes place

on the oxygen O11 as acceptor. However, this oxygen is not always identified as a preferred

acceptor site from electrostatic interaction potential calculations [17]. The oxygen O11 and the

acceptor oxygens O13 and O25 of the Manzamenones G and K respectively are carbonyl functions.

In these Manzamenones, this function is always conjugated with a double bond of a ring with

five members (cyclopentenone) except Manzamenone G for which the ring is with six members

(cyclohexenone). The interaction study reveals that the bond always involves the carbonyl of

each of the Manzamenones. The preferred acceptor site for Artemisinin is also a carbonyl

oxygen. This oxygen is also responsible for the interaction with the water molecule. Figure 6

gives an illustration of these interactions between the studied molecules and the water

molecule.

Quinine---H2O Artemisinin---H2O

A(B)---H2O M---H2O

K---H2O G---H2O

Figure 6: Optimized structures of the complexes of Quinine, Artemisinin, Manzamenones A(B),

M, K and G with the water molecule