Quantitative Structure-Activity Relationship Study on Phthalimide Derivatives as HIV-1 Reverse Transcriptase Inhibitors
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1 SieneAsia 27 (2001) : Quantitative Struture-Ativity Relationship Study on Phthalimide Derivatives as HIV-1 Reverse Transriptase Inhibitors Jiraporn Ungwitayatorn a, *, Chutima Matayatsuk a, Pathanakarn Sothipatharasai b a Department of Pharmaeutial Chemistry, Faulty of Pharmay, Mahidol University, 447 Sri-Ayudhya, Bangkok 10400, Thailand b Department of Pharmaeutial Chemistry, Shool of Pharmay, Rangsit University, 52/347 Muang-Ake, Lakhok, Phaholyothin Rd. Patumtani, 12000, Thailand * Corresponding author, pyjuw@mahidol.a.th Reeived 21 Aug 2000 Aepted 25 Jun 2001 ABSTRACT Quantitative struture-ativity relationships (QSAR) was performed to orrelate the physiohemial properties, ie, eletroni, hydrophobi, and steri properties with the HIV-1 reverse transriptase inhibitory ativity of phthalimide derivatives. Multiple linear regression (MLR) analysis was used for the study. The best QSAR model was obtained with orrelation oeffiient (r) of and rossvalidated r 2 (q 2 ) of This model indiates that the inhibitory ativity orrelated to the eletroni properties, ie, partial atomi harge at arbon 2, the highest oupied moleular orbital (HM), and the dipole moment. This ativity also orrelated to the steri property, ie, moleular volume (MV) and the hydrophobi property, log P. KEYWRDS: QSAR, HIV-1 reverse transriptase, phthalimide derivatives, non-nuleoside reverse transriptase inhibitors. ITRDUCTI The virus-enoded reverse transriptase (RT) plays an important role in the life yle of the human immunodefiieny virus type 1 (HIV-1), the ausative agent of AIDS. RT is a multifuntional enzyme having RA-direted DA polymerase and DAdireted DA polymerase ativities as well as Rase H ativity. 1 This enzyme is an attrative target for developing anti-hiv drugs for the treatment of AIDS. Several ompounds targeted against HIV-RTI have been shown to be ative in linial trials. 2-5 So far, nine drugs from two lasses have been approved by the US FDA, ie, AZT, ddi, ddc, d4t, 3TC, abaavir, nevirapine, delavirdine, and efavirenz. The first six drugs are members of the nuleoside lass and the others belong to the non-nuleoside lass. Treatment by these drugs usually leads to the development of resistant HIV-1 mutants. The emergene of resistant strains has neessitated the ontinuation of researh to find new inhibitors. Reently, non-nuleoside HIV-1 RT inhibitors (RTIs) 4,5 have played an important role in the treatment of HIV infetions, and several of them have been investigated for use in alternative or ombination therapy. These ompounds are highly ative against HIV-1, but inative against HIV-2 or any other retrovirus. This unique speifiity of the RTIs for HIV-1 RT is due to the presene in HIV-1 RT, but not in other reverse transriptases, of a flexible, highly hydrophobi poket. 6,7 The studies of amino aids responsible for drug-resistane of HIV-1 RT suggested that this poket determines the binding of the RTIs with their target site. These amino aid residues are Leu 100, Val 106, Val 108, Val 179, Tyr 181, Tyr 188, Gly 190, Met 230, and Pro 236. The binding of the RTIs to the hydrophobi poket of the HIV-1 RT does not interfere with the binding of the dtps (deoxynuleotide triphosphates) but slows down the rate of inorporation of the dtps into the DA produt. 8 Previous investigations in our researh group have identified the phthalimide derivatives as a new lass of non-nuleoside HIV-1 RT inhibitors. 9 The synthesized ompounds were tested in vitro for their HIV-1 reverse transriptase inhibitory ativity at onentration of 200 µg/ml by radiometri assay using polyadenyli aid (poly A) as template, oligodeoxythymidyli aid (oligo dt) as primer, and radiolabeled thymidine triphosphate ([ 3 H]dTTP) as substrate. The ativity was measured orresponding to the degree of inhibition of inorporation of
2 246 SieneAsia 27 (2001) [ 3 H]dTTP into a polymer fration by the synthesized ompounds. The inhibitory ativity was reported as % inhibition as shown in Table 1. The most potent ativity, IC 50, µg/ml, was obtained with ompound 5, whereas ompounds 11 and 2 were less potent with IC µg/ml and µg/ ml respetively. 9 These three ompounds exhibited IC 50 value lower than that of delavirdine (IC 50 = µg/ml) and AZT in HIV-1 strain M48, ddiresistant strain (IC 50 = µg/ml, using poly ri as template, oligo dc -primer and [ 3 H]dCTP as substrate) Quantitative struture-ativity relationships (QSAR) was investigated based on the fat that the biologial ativity of a ompound is a funtion of its physiohemial properties Physiohemial parameters whih are representatives of strutural features of ompounds are, for examples, eletroni effets, hydrophobiity (lipophiliity) and steri properties. In this study, the QSAR analysis of the ompounds in this phthalimide series was performed based on the assumption of linear additive ontributions of the different physiohemial properties mentioned above to the HIV-1 RT inhibitory ativity. The most ommonly used statistial and mathematial method, multiple linear regression (MLR) analysis, was applied to reate QSAR models and to obtain statistial data values, ie, orrelation oeffiient (r), standard deviation (s), F-test, rossvalidated orrelation oeffiient (q 2 ), and sum of square standard error (S PRESS ). These statistial data were used to evaluate the obtained QSAR models. The best-derived QSAR model was used to predit ativity of the untested ompounds and to suggest strutural feature(s) whih should be modified in order to improve ativity. MATERIALS AD METHDS Biologial Data The previously synthesized phthalimide ompounds (Table 1) were tested for their HIV-1 reverse transriptase inhibitory ativity by a radiometri assay. 9, The results of the inhibitory ativity were reported as present inhibition and were used as dependent variables in this QSAR study. Generating the moleular strutures and onformational analysis The moleular strutures of phthalimide derivatives were modeled with SYBYL 6.5 moleular modeling program (Tripos Assoiates, Saint Louis, M) on an Indigo Elan workstation (Silion Graphis In, Mountain View, CA) using the sketh approah. The fragment libraries in the SYBYL database ontaining small moleules were also used as building bloks for the onstrution of larger ones. Eah struture was first energy minimized using the standard Tripos fore field (Powell method and 0.05 kal/mol*å energy gradient onvergene riteria) and eletrostati harge was assigned by the Gasteiger-Hükel method. Sine ompounds in the training set possess a high degree of onformational flexibility, geometry optimization was performed by using a systemati onformational searh. In the systemati onformational searh proess, the rotatable bonds of ompounds (Figure 1) were rotated by 2 degree inrements for all possible ombinations to ahieve the global minimum energy onformations. These onformations were used as starting geometries for the following optimization using the MPAC 6.0 (PM3) interfae. Finally, these moleules were further minimized by the standard Tripos fore field (Powell method and 0.01 kal/mol*å energy gradient onvergene, the same riteria used in the initial step of energy minimization). The onformations obtained for all moleules in the training set were used in the following QSAR study. Table 1. In vitro RT inhibitory ativity of phthalimide derivatives at onentration 200 µg/ml. Ar Cpd Ar % Cpd Ar % inhibition a inhibition a 1 2 CH ± ± H 2 11 ± ± 3.7 CH3 21 ± ± 1.5 CH ± ± H H 76 ± ± 7.9 H H 3 ± 4.3 a The values represent the mean ± standard deviation of three separate determinations. (a) (b) CH 3 Fig 1. The rotatable bonds of moleules used in the systemati onformational searh proedure: (a) three rotatable bonds and (b) two rotatable bonds.
3 SieneAsia 27 (2001) 247 QSAR STUDY Calulation of physiohemial properties The physiohemial properties used in this study were eletroni, hydrophobi and steri properties. The representatives of eletroni properties were partial atomi harges, eletrostati energy (ES), dipole moment, frontier orbital, ie, the highest oupied moleular orbital (HM) and the lowest unoupied moleular orbital (LUM), and ionization potentials. The partial atomi harges of arbon 1 (C1), arbon 2 (C2) and nitrogen 1 (1) (as shown in Figure 2) were used for eletroni desriptors. Partition oeffiient (log P) and lipophili potential (LP) desriptors were used as representatives of hydrophobi properties. Molar refrativity (MR), moleular weight (MW), moleular surfae area (MS), and moleular volume (MV) were used for steri properties. Log P, MR, MW, MS, and MV were alulated by Hyper Chem Release 3.0 for Windows. LP was alulated by the MLCAD option in SYBYL 6.5 on the Silion Graphi Workstation. Partial atomi harges were alulated by the Gasteiger-Hükel method and MPAC 6.0-PM3 method in SYBYL 6.5. ES was alulated by using SYBYL 6.5 (Gasteiger- Hükel method). HM, LUM energies, ionization potential, and dipole moment were alulated by MPAC 6.0-PM3 option in SYBYL 6.5. Multiple linear regression analysis Multiple linear regression (MLR) analysis was used to investigate the orrelation between biologial ativity and physiohemial properties. The MLR was performed by using the SPSS for Windows Release 7.0 pakage by the stepwise method. The highest orrelation of independent variables with dependent variable was hosen for deriving the QSAR model. The statistial values, multiple orrelation oeffiient (r), standard errors (s), rossvalidation r 2 (q 2 ) and standard error of predition (S PRESS ) were used to evaluate the obtained QSAR models. Several ombinations of independent 1 C1 C2 1 C1 C2 variables were firstly attempted using three variables (one representative from eah property) for individual models, and then, more variables were added in order to optimize the statistial values but not more than five independent variables were used. The best model derived from the MLR analysis was used to predit the inhibitory ativity of the phthalimide ompounds (struture as shown in Figure 3) whih were not inluded in the training set. RESULTS AD DISCUSSI The QSAR models were generated from the perent inhibition of phthalimide ompounds (Table 1) as dependent variable. The alulated eletroni, hydrophobi, and steri desriptors as shown in Table 2 were used as independent variables. All possible ombinations of the physiohemial desriptors were investigated in order to obtain the best QSAR model. It should be mentioned that more models were obtained from the analysis, but they were ruled out by the MLR stepwise proedure. The stepwise MLR was used to selet eah independent variable for deriving a QSAR model by onsidering the orrelation between eah variable with the dependent variables. The MLR equation used for the QSAR model developed is as follows: y = a 1 x 1 + a 2 x 2 + a 3 x 3 a n x n + b y = dependent variable (% inhibition) a 1, a 2, a 3, a n = the regression oeffiients of independent variables x 1, x 2, x 3, x n = independent variables b = the regression onstant obtained from the fit To avoid self orrelation between the variables used for the derivation of the QSAR model, the orrelation matrix was alulated and the result shown in Table 3. The best QSAR model obtained from the MLR analysis is shown as the following equation: % inhibition = (± 0.700) MV (± ) logp (± ) HM (± ) C2 GH (± ) Dipole (± 1.716) (n = 11, r = 0.974, s = 9.683, F = , q 2 = 0.785, S PRESS = ) (a) Fig 2. Struture of phthalimide ompounds showing atoms used for atomi harge alulation: (a) phthalimide derivatives with two arbon atoms between the phthalimide and heteroyli moieties and (b) one arbon atom between the two moieties. (b) Fig 3. The phthalimide ompounds not inluded in the training set.
4 248 SieneAsia 27 (2001) Table 2. The alulated physiohemial desriptors values of phthalimide ompounds used in QSAR models. Moleular desriptors Cpd % inhi Hydrophobi Steri Eletroni -bition logp a LP b MR a MW a MS a MV a 1 GH C1 GH C2 GH 1 PM3 d C1 PM3 d C2 PM3d Dipole d ES Ioniz d HM d LUM d a b d Calulated by HyperChem 3.0 program Calulated by MLCAD program Calulated by SYBYL 6.5 program using Gasteiger Hükel method Calulated by MPAC 6.0-PM3 program Table 3. The orrelation matrix of all variables used in QSAR studies. % IR* Hydrophobi Steri Eletroni logp LP MR MW MS MV 1 GH C1 GH C2 GH 1 PM3 C1 PM3 C2 PM3 Dipole ES Ioniz HM LUM %IR* logp LP MR MW MS MV GH C1 GH C2 GH PM C1 PM C2 PM Dipole Es Ioniz HM LUM * % IR = % inhibition This model indiates the ontribution of eletroni desriptors (ie, C2 GH, dipole and HM energy), hydrophobi desriptor (logp), and steri desriptor (MV) to the enzyme inhibitory ativity of these phthalimide ompounds. The negative value of the oeffiient for the C2 GH variable suggests that high eletron density around C2 position (Figure 2) will inrease biologial ativity. Therefore, the presene of a strong eletron donating substituent at this position will be preferred. The negative value of the oeffiient for the HM, implies that a low energy of HM within the moleule orrelates with inreased ativity. Dipole moment, another eletroni desriptor, is a good indiator of the overall polarity within the moleule. The addition of this parameter to the MLR analysis obtained the higher q 2 in every
5 SieneAsia 27 (2001) 249 model studied. This indiates that the dipole moment ould be essential for inreasing the quality of the QSAR model. The positive oeffiient of the logp desriptor whih relates to the hydrophobiity of the moleule suggested that inreasing the lipophiliity might inrease the ativity. This orresponds to the presene of the hydrophobi binding site in HIV-1 RT (Pro 95, Leu 100, Val 106, Tyr 181, Tyr 188, Gly 190, Trp 229, Leu 234, and PR 236). The negative oeffiient of the moleular volume desriptor, one of the steri properties, means that a moleule ould be too large in size, and then it would not fit into suh a hydrophobi poket in the enzyme non-substrate binding site. The experimental and alulated (predited) perent inhibition of ompounds in the training set based on the equation above are shown in Table 4 and the residual plot of both values is given in Figure 4. The results indiate a good linear regression of orrelation between experimental and alulated perent inhibition. Three phthalimide ompounds, ie, ompound 12, 13 and 14 whih were not inluded in the training set, were used to test the preditive power of the derived QSAR equation. As seen from the result in Table 5, this QSAR equation gave good preditive ability with the predited ativity orresponding well to the experimental ativity. Moreover, a three-dimensional QSAR tehnique, omparative moleular field analysis (CoMFA) was also applied to the same training set. The CoMFA model was obtained with ross-validated r 2 (q 2 ) = (S PRESS = and number of the optimum omponents = 3) inluding the lowest unoupied moleular orbital (LUM) energies in addition to CoMFA fields (manusript in preparation). Table 6 summarizes Table 4. The experimental and alulated perent inhibition of phthalimide derivatives. Cpd % inhibition Residual Experimental Calulated Pred. 10 r = q 2 = n = At. Fig 4. Plot of experimental (atual) versus predited (alulated based on QSAR equation) perent inhibition of phthalimide ompounds in the training set. Table 5. The predited ativity of ompounds not inluded in training set using the QSAR model. Cpd 12 Strutures Experiment a % inhibition Predited Residual 52 ± ± ± * ompound was omitted from QSAR table in CoMFA study. Table 6. The experimental and predited perent inhibitions alulated from the lassial QSAR equation and CoMFA model. % Inhibition Cpd Classial QSAR CoMFA * Training set Test set * ompound 4 was omitted from QSAR table in CoMFA study
6 250 SieneAsia 27 (2001) the alulated ativity of ompounds in the training set and test set using QSAR equation and CoMFA model. Both lassial and CoMFA models gave omparable orrelation between experimental and alulated values. CCLUSI This QSAR study suggested the strutural features of ompounds in the phthalimide series whih possess promising high HIV-1 reverse transriptase inhibitory ativity. This study also provided preditive utility for untested ompounds, and also, it was able to predit ativity of new ompounds prior to synthesis. ACKWLEDGEMETS The authors would like to thank the ational Eletronis and Computer Tehnology Center (ECTEC) for providing SYBYL version 6.5 failities, Assistant Professor Dr Supa Hannongbua, Department of Chemistry, Kasetsart University, for advising this study. metaboli stability of novel substituted pyridine analogues. J Med Chem 39, Shinazi, RF, Mmillan, A, Cannon, D, Mathis, R, et al (1992) Seletive inhibition of human immunodefiieny viruses by raemates and enantiomers of is-fluoro-1-[2-(hydroxymethyl)-1,3-oxathiolan-5-yl] ytosine. Antimirob Agent and Chemothr 36(11), Hansh C and Fujita T (1964) A method for the orrelation of biologial ativity and hemial struture. J Am Chem So 86, Free JSM and Wilson JW (1964) A mathematial ontribution to struture ativity studies. J Med Chem 7, Kubinyi H (1993) QSAR: Hansh analysis and related approahes, vol 1 (Edited by Mannhold R, Krogsgaard-Larsen P and Timmerman H), pp VCH Publishers, ewyork. 15.Tan GT, Pezzuto JM and Kinghorn AD (1991) Evaluation of natural produts as inhibitors of human immunodefiieny virus type 1 (HIV-1) reverse transriptase. J at Prod 54(1), Hoffman AD, Banapour B and Levy JA (1985) Charaterization of the AIDS-assoiated retrovirus reverse transriptase and optimal onditions for its detetion in virions. Virology 147, Kusumoto IT, Shimada I, Kakiuhi, Hattori M and amba T (1992) Inhibitory effets of Indonesian plant extrats on reverse transriptase of an RA tumour virus (I). Phytother Res 6, REFERECES 1. Tan CK, Zhang J, Li ZY, Tarpley WG, Downey KM, and So AG (1991) Funtional haraterization of RA-dependent DA polymerase and Rase H ativities of a reombinant HIV-1 reverse transriptase. Biohemistry 30, De Clerq E (1995) Antiviral therapy for human immunodefiieny virus infetions. Clin Mirobiol Rev 8, Mansour TS, and Storer R (1997) Antiviral nuleosides. Curr Pharm Des 3, De Clerq E (1999) Perspetives of non-nuleoside reverse transriptase inhibitors (RTIs) in the therapy of HIV-1 infetion. IL Farmao 54, De Clerq E (1999) The role of non-nuleoside reverse transriptase inhibitors (RTIs) in the therapy of HIV-1 infetion. Antiviral Res 38, Kohlstaedt LA, Wang J, Friedman JM, Rie PA and Steitz TA (1992) Crystal struture at 3.5 Å resolution of HIV-1 reverse transriptase omplexed with an inhibitor. Siene 256, anni RG, Ding J, Jaobo MA, Hughes SH and Arnold E (1993) Review of HIV-1 reverse transriptase three-dimensional struture: impliations for drug design. Perspet Drug Disovery Des 1, Spene RA, Kati WM Anderson KS and Johnson KA (1995) Mehanism of inhibition of HIV-1 reverse transriptase by nonnuleoside inhibitors. Siene 267, Ungwitayatorn J, Wiwat C, Matayatsuk C, Sripha K and Kamalanonth P (2001) Synthesis and evaluation of phthalimide and benzofuran derivatives as potential HIV-1 reverse transriptase inhibitors. Songklanakarin J Si Tehnol 23(2), Genin, MJ, Poel, TJ, Yagi, et al (1996) Synthesis and bioativity of novel bis (heteroaryl) piperazine (BHAP) reverse transriptase inhibitors: Struture-ativity relationships and inreased
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