Annals of Clinical Cytology and Pathology

Synthesis, Molecular Docking and Antiamoebic Studies of Nitroimidazole-Indole Conjugate

Research Article | Open Access

  • 1. Department of Chemistry, Jamia Millia Islamia, Jamia Nagar, 110 025, New Delhi, India
  • 2. Medicinal Chemistry Laboratory, Department of Biosciences, Jamia Millia Islamia, 110025, New Delhi, India
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Corresponding Authors
Amir Azam, Department of Chemistry, Jamia Millia Islamia, Jamia Nagar, 110 025, New Delhi, India, Tel: 91-11-26981717/3254; Fax: 91-11-26980229

In an imperative search for efficacious antiamoebic agents nitroimidazoles-indole conjugates were synthesized, characterised and biologically tested for HM1: IMSS strain of E. histolytica. Designing of conjugates by linking two scaffolds with different intrinsic properties can give remarkable results. Molecular docking studies showed the key interacting active residues in the binding site of E. histolytica O-acetyl-serine Sulfohydroylase protein (EhOASS) recommended that the addition of a hydrophobic group better fit within enzyme active site leading to enhanced inhibitory activity. All the compounds were less toxic against HeLA cervical cancer cell line. The compounds RC6, RC8, RC9 and RC10 exhibited strong inhibitory activities, with IC50 values of 3.61, 2.08, 1.75, and 1.22mM E. histolytica O-acetyl-serine Sulfohydroylase protein (EhOASS) in vitro respectively. The promising antiamoebic activity and enzymatic assay of RC6, RC8, RC9 and RC10 make them promising molecules for further lead optimization in the development of novel antiamoebic agents


Inam A, Uddin A, Akhtar A, Abid M, Azam A (2021) Synthesis, Molecular Docking and Antiamoebic Studies of Nitroimidazole-Indole Conjugate. Ann Clin Cytol Pathol 7(1): 1141.


•    Nitroimidazole; Amoebiasis; Entamoeba histolytica; 


Amoebiasis is the most aggressive infection of the human gastrointestinal tract caused by the anaerobic protozoan parasite Entamoeba histolytica. The parasite invades the intestinal mucosa causing amoebic dysentery. At times, they migrate towards the liver, causing an amoebic liver abscess [1]. Infection of this parasite is common and occurs in several developing countries with poor sanitation facilities, resulting in 50 million cases of invasive disease and up to 100,000 fatalities per year [2,3], being the fourth leading cause of death after malaria, Chagas disease, and leishmaniasis [4]. Amoebic liver abscess is mainly observed in young adults, adults in the productive stage of life (20-50 years) and is more prone to be developed in males than females [5-9]. It has been an active area of research for decades [10]. The first-line drugs in the treatment of amoebiasis and other parasitic disease such as leishmaniasis, trichomoniasis and giardiasis are metronidazole or nitroimidazole derivatives (tinidazole, secnidazole, ornidazole [11] and nitazoxanide [12]).These compounds involve the transfer of an electron to the nitro group of the drug which leads to the generation of a short-lived nitroso free radical by intracellular reduction besides the capacity to bind DNA inducing single and double-strand breaks [13,14]. Several side effects in addition to clinical resistance and carcinogenicity to this class of compounds especially metronidazole have been reported [15,16] such as nausea, diarrhea, headache, dizziness, vomiting, metallic taste in the mouth, stomatitis, glossitis, dark urine, paresthesia, and central nervous system toxicity [17]. Therefore, to cope with this derelict protozoan disease it has become essential to discover new leads for the development of less toxic novel drugs against E. histolytica.

The heterocycles bearing nitrogen such as imidazole and indole have attracted considerable attention owing to their extensive biological spectrum such as antifungal, antimicrobial, anticancer, antiviral, anti-inflammatory, analgesic [18-23]. Previously, thiosemicarbazones, thiosalicylate conjugates, triazoles, and hydrazones of 5-nitroimidazole endowed antiamoebic activity have been reported [10,24]. Due to the high therapeutic index and clinical benefits of nitroimidazoles, its hydrazone conjugates are a promising scaffold for the synthesis of a potential bioactive agent. The class of acyl hydrazones is classically employed as the warheads during drug design and shows reactivity as Michael-acceptors [25]. Due to its reactivity as Michael acceptor, the acyl hydrazone, the linker is recognized as a good functional group in drug discovery.

Prompted by the extensive chemotherapeutic importance of these core groups, a series of compounds bearing hydrazones, 5-nitroimidazole, and indole scaffolds have been designed synthesized, and screened against E. histolytica (Figure 1).


The nitroimidazole acetohydrazide derivatives were synthesized by reported methods [26]. Target compounds (RC1- RC15) were obtained by the steps as outlined in scheme 1. The synthesis of N-substituted-2-(3-formyl-1H-indol-1-yl) acetamide (C1-C15) was carried out by reacting indole-3-carbaldehyde with different substituted 2-chloroacetamides as reported in the literature [27]. On condensation of 2-(2-methyl-5-nitro1H-imidazol-1-yl) acetohydrazide (2) with different aldehydes (C1-C15) yielded the final products N-substituted-2-oxoethyl)- 1H-indol-3-yl) methylene)-2-(2-methyl-5-nitro-1H-imidazol-1- yl) acetohydrazide (RC1-RC15). The purity of the compounds was confirmed by CHNS analysis. All the compounds were characterized by IR, 1 H NMR, 13C NMR and mass spectral studies (Scheme 1).


In the IR spectra, the formation of nitroimidazole acetohydrazide derivatives (RC1-RC15) showed two characteristic bands at 3149- 3345 cm -1 and 1665-1677 cm -1 were assigned to N-H and C=O stretching respectively. The band at 1537-1550 cm -1 due to C=N suggested the condensation of different substituted indole-3-carbaldehyde with 2-(2-methyl-5- nitro-1H-imidazol-1-yl) acetohydrazide (2). The 1 H NMR spectra of all the compounds favour the proposed structure. In all the compounds the -NH peaks of hydrazone appeared at δ11.45-11.56 ppm and for the aromatic and aliphatic substituted amide NH appeared at δ10.13-10.70ppm and δ8.30-7.45ppm respectively which was also observed in the spectra of the aldehydes (C1- C15). The peak for aldehydic group in (C1-C15) was observed at δ9.90-9.98ppm whose absence in final compounds showed the formation of the final products. The peaks for the carbonyl carbon were present in the range δ168-165ppm. The signals for the aromatic regions appeared in their respective range. The values are given in the supplementary data.

All the synthesized compounds were screened in vitro for antiamoebic activity by micro-dilution method using HM1: IMSS strain of E. histolytica and their IC50 values are reported in Table1. Metronidazole (Mtz) is used as a reference drug having IC50 value 1.80µM in our experiment. The results were estimated as % of growth inhibition, compared with the untreated controls, and plotted as probit values as a function of drug concentration. The activity results can be elucidated as a comparison between the activity of the aldehydes and their corresponding hydrazones. The N-substituted-2-(3-formyl-1H-indol-1-yl) acetamide (C1- C15)were found IC50 values in the range 0.5 to 23.7 µM. Out of the fifteen derivatives of indole-3-carboxaldehyde (C1-C15) only two (C4 and C8) showed IC50 values less than Mtz. However, the hydrazone formation enhanced the antiamoebic activity. Though no trend has been followed, the IC50 values for C4 (IC50 0.83µM ±0.012) was lower than its hydrazone RC4 (IC50 1.60µM ±0.031) whereas for C8 (IC50 0.76µM ±0.008) was higher than RC8 (IC50 0.44µM ±0.028). The IC50 values for the hydrazones (RC1-RC15) lies in the range 0.2 to 11.6 µM. Among all the fifteen compounds eight compounds (RC2, RC3, RC4, RC6, RC8, RC9, RC10, RC11) showed promising results while three compounds exhibited considerable activity (RC1, IC50 4.20µM ±0.010, RC7, IC50 3.48µM ±0.032, RC14 IC50 2.30µM ±0.010). None of the alicyclic compound (C13-15, RC13-15) was found with significant activity. The compounds containing acetophenone group on the phenyl ring (RC2, IC50 0.60µM ±0.006 & RC9, IC50 0.73µM ±0.023) were found to be better growth inhibitor of E. histolytica. O-tolyl (RC8) was found to be more imperative with IC50 value lower than Mtz as compared to p-tolyl (RC7) and m- tolyl (RC1) substituted compounds. Both the disubstituted compounds (RC6, IC50 0.26µM ±0.022, RC10, IC50 0.68µM ±0.020) were found to be more persuasive amoebicidal agents (Figure 2). The compound RC6 was best among the series which can be accredited to the presence of two halogens. The presence of aliphatic isopropyl group RC3 also enhanced the activity to two folds than Mtz.

The considerable increase in the antiamoebic activity can be attributed to the presence of the hydrazone linkage [-NH-N=CH-] thereby reducing the IC50 values to three to four times as compared to their corresponding aldehydes.

Among all, the best antiamoebic compounds were further validated by Invitro enzymatic inhibition on E.histolytica O-acetyle-l-serine sulfohydrolase (EhOASS) (Figure 3), and their IC50 values were listed in (Table 1). Inhibitory kinetics analysis was carried out for EhOASS with varied concentration of Metronidazole derived compounds to measure the decrease in enzymatic activity. The rate of a reaction was found to significantly decrease with increasing concentration of inhibitor. To explore the inhibition of Metronidazolederived compounds, IC50 values were calculated by measuring normalized inhibition with increasing log inhibition concentration (Figure 4). The Metronidazole derived compounds RC6, RC8, RC9 and RC10 significantly inhibiting EhOASS with IC50 of 3.61, 2.08, 1.75, and 1.22 mM respectively.

The compounds (C4, C8, RC2, RC3, RC4, RC6, RC8, RC9, RC10 and RC11) having less IC50 than metronidazole were screened for their cytotoxicity profile against the HeLa, cervical cancer cell line. HeLa, cells (4000cells/well) were plated in 96 well plates in triplicate. The cells were treated with compounds (C4, C8, RC2, RC3, RC4, RC6, RC8, RC9, RC10, RC11) as indicated in the Figure 2, the concentration values correspond to the IC50 value observed for these compounds for E. histolytica. The cell viability values were notified after 48 hours and 72 hours. Both the aldehydes showed a slight diminution in IC50 value after 72 hrs [{C4: IC50=100.00µM ± 1.3 (48hrs), 82.50µM ± 4.5 (72 hrs)}, {C8: IC50=98.60µM ± 1.8 (48hrs), 86.3µM ± 2.9 (72 hrs)} while no regular trend was observed for the hydrazones. The best IC50 value was assessed for hydrazones RC10 (IC50: 99.10 ± 17.0) after 48 hrs and for RC3 (IC50: 99.30 ± 5.3) after 72 hrs. Overall all the compounds are proposed to be less toxic with good cell viability results (Table 2).

E.histolytica o-acetyl-L-Serine Sulfohydrolase (EhOASS) is an attractive target for the treatment of amoebiasis,as it catalyzes the last step of cysteine biosynthetic pathway which is responsible for the survival and growth of E.histolytica. 3D dimensional coordinates of the target protein O-acetyl-serine sulfohydrolase (EhOASS) from E. histolytica were directly taken from Protein Data Bank (PDB ID: 3BM5) for molecular docking studies with the selected compounds. The structures of the compounds were drawn using ChemBioDraw Ultra 12.0 and converted into PDB format using online free web server of National Cancer Institute (NCI) named SMILES translator tool (http://cactus.nci.nih. gov/translate/) [28]. Molecular docking study was performed using InstaDock [29], a single click molecular docking tool that automizes the entire process of molecular docking-based virtual screening. The binding affinities between the ligand and protein were calculated using the QuickVina-W (Modified AutoDock Vina) program which uses a hybrid scoring function (empirical + knowledge-based) in docking calculations and a blind search space for the ligand.

To establish the nature of interaction with E. histolytica O-acetyl-serine sulfohydrolaseprotein (EhOASS), all the four compounds were subjected to molecular docking analysis. The binding affinity of the compounds with EhOASS was found in the range of -9.2 kcal/mol to -9.3 kcal/mol. The highest binding affinity was observed with RC-6 and RC-10 as -9.3 kcal/mol. Interestingly, RC-6 and RC-10 bind at the same position where co-crystalized cysteine (with EhOASS in PDB: 3BM5) interacts [30]. Moreover, both RC-6 and RC-10 interacted with the active site residues, to which co-crystalized cysteine was interacting which may be presumably responsible for inhibiting the protein-substrate interaction (Figure 1). The EhOASS-RC6 complex is stabilized by six hydrogen bonds and EhOASS-RC10 complex is stabilized by three hydrogen bonds and other close interactions within the active site of the protein. Interaction analysis of all the possible docked conformers of all the four compounds was carried out to investigate their binding pattern and possible interactions towards the EhOASS binding pocket (Table 1).The binding interactions of compound RC6 with EhOASS include H-bond with LYS-58, SER-86, GLY-87, GLN-159, HIS-232, ALA-239. H-bond for compound RC8 was found with ASN-88, THR-89, GLN-159. Compound RC 9 was observed to form H-bonds with SER-86, GLY-87, GLN-159. H-bond for compound RC 10 was observed to be SER-86, GLY-87GLN-159 (Figure 2).

Ligplot analysis shows the residues that interact with compound RC6 and contribute to the hydrophobic interactions are Val 158, Gly 159, Gly 160, Gly 161, Asp 162, Ala 163, Leu 181, Arg 183, Arg 188, Ile 246, Gly 247, Pro 250, Asp 264 and Tyr 266 while the ND1 atom of His 182 of the active site of the receptor forms hydrogen bond with O2 of compound RC6 (Figure 2A).

Table 2: Effect on cell viability of HeLa cells in response to compounds (C4, C8, RC2, RC3, RC4, RC6, RC8, RC9, RC10, RC11) as assessed by MTT assay.

Compound. Conc. in nM % Cell viability±s.d. (48h) % Cell viability±s.d. (72h)
C4 830 100.00±1.3 82.50±4.5
C8 760 98.60±1.8 86.3±2.9
RC2 600 85.00±11.6 71.90±2.5
RC3 520 91.60±21.0 99.30±5.3
RC4 1600 89.30±12.0 97.66±5.7
RC6 260 83.87±14.4 90.80±3.6
RC8 440 83.00±14.0 97.30±6.0
RC9 730 92.80±7.7 85.60±4.3
RC10 680 99.10±17.0 77.10±4.4
RC11 1550 87.10±20.0 97.66±6.6
Mtz 1800 96.50±15.2 100.00±1.1



An analysis of the antiamoebic properties for the N-acylhydrazones (RC1-RC15) showed an incredible potency enhancement when compared to the aldehydes N-substituted 2-(3-formyl-1H-indol-1-yl)acetamide (C1-C15). The in vitro antiamoebic results and cytotoxicity profile revealed that the compounds (RC6 and RC8) can further be explored and can turn out to be better future drugs. Further validation by enzyme inhibition kinetics showed the RC6, RC8, RC9 and RC10 could be optimized to be better inhibitors. These studies showed that modifying the nitroimidazoles conjugates into N-acylhydrazone derivatives is an appealing synthetic tool for the antiparasitic drug discovery.

Table 3: Binding affinity of compounds with EhOASS generated from molecular docking.

Compound Protein-ligand Interactions
Affinity (kcal/mol) pKi Liand Efficiency (kcal/mol/non -H atom) Hydrogen Bonds Other Interacting Residues
Amino Acid Residues Distance (Å)
RC-6 -9.3 6.75 0.184 LYS-58, SER-86, GLY-87,
GLN-159, HIS-232, ALA-239
2.27, 2.38, 2.16 2.75, 2.25, 2.62 THR-85, ASN-88, THR-89, AR-116, PRO-137, MET-136, ILE-140, PHE-160, LYS-229, GLY-230, PRO-231, GLN-235, GLY-236, GLY-238, GLY-240, PHE-2
RC-8 -9.2 6.60 0.174 ASN-88, THR-89, GLN-15 2.13, 2.16, 2.33 PRO-137, MET-136, ILE-140, SER-86, ALA-239, THR-85, GLY-192, GLY-236, THR-193, GLY-87, LYS-58, PHE-160, ASP-244, PHE-24
RC-9 -9.2 6.60 0.173 SER-86, GLY-87, GLN-159 2.05, 2.72, 2.96 SER-84, ILE-237, ALA-239, GLY-236, THR-85, LYS-58, GLY-240, LYS-229, PHE-241, ILE-140, ASN-158, MET-136, GLU-83, PHE-160
RC-10 -9.3 6.75 0.180 SER-86, GLY-87, GLN- 2.33, 2.39, 2.48 PRO-137, MET-136, GLY-233, HIS-232, GLN-235, PHE-160, ILE-237, GLY-236, ASN-88, THR-89, THR-85, LYS-58, ALA-239, LYS-229, PHE-241

* pKi (the negative decimal logarithm of inhibition constant)


This work was supported by University Grants Commission (UGC) (grant # 41-275/2012(SR), New Delhi, India. A. Inam is also thankful to UGC, for the SRF BSR meritorious fellowship.


Supplementary data (synthetic procedures, spectral data, antiamoebic assay, MTT assay and molecular docking) associated with this article can be found, in the online version, at


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Received : 19 Jul 2021
Accepted : 13 Oct 2021
Published : 15 Oct 2021
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ISSN : 2641-7731
Launched : 2016
Journal of Behavior
ISSN : 2576-0076
Launched : 2016
Annals of Clinical and Experimental Metabolism
ISSN : 2572-2492
Launched : 2016
Clinical Research in Infectious Diseases
ISSN : 2379-0636
Launched : 2013
JSM Microbiology
ISSN : 2333-6455
Launched : 2013
Journal of Urology and Research
ISSN : 2379-951X
Launched : 2014
Journal of Family Medicine and Community Health
ISSN : 2379-0547
Launched : 2013
Annals of Pregnancy and Care
ISSN : 2578-336X
Launched : 2017
JSM Cell and Developmental Biology
ISSN : 2379-061X
Launched : 2013
Annals of Aquaculture and Research
ISSN : 2379-0881
Launched : 2014
Clinical Research in Pulmonology
ISSN : 2333-6625
Launched : 2013
Journal of Immunology and Clinical Research
ISSN : 2333-6714
Launched : 2013
Annals of Forensic Research and Analysis
ISSN : 2378-9476
Launched : 2014
JSM Biochemistry and Molecular Biology
ISSN : 2333-7109
Launched : 2013
Annals of Breast Cancer Research
ISSN : 2641-7685
Launched : 2016
Annals of Gerontology and Geriatric Research
ISSN : 2378-9409
Launched : 2014
Journal of Sleep Medicine and Disorders
ISSN : 2379-0822
Launched : 2014
JSM Burns and Trauma
ISSN : 2475-9406
Launched : 2016
Chemical Engineering and Process Techniques
ISSN : 2333-6633
Launched : 2013
JSM Allergy and Asthma
ISSN : 2573-1254
Launched : 2016
Journal of Neurological Disorders and Stroke
ISSN : 2334-2307
Launched : 2013
Annals of Sports Medicine and Research
ISSN : 2379-0571
Launched : 2014
JSM Sexual Medicine
ISSN : 2578-3718
Launched : 2016
Annals of Vascular Medicine and Research
ISSN : 2378-9344
Launched : 2014
JSM Biotechnology and Biomedical Engineering
ISSN : 2333-7117
Launched : 2013
Journal of Hematology and Transfusion
ISSN : 2333-6684
Launched : 2013
JSM Environmental Science and Ecology
ISSN : 2333-7141
Launched : 2013
Journal of Cardiology and Clinical Research
ISSN : 2333-6676
Launched : 2013
JSM Nanotechnology and Nanomedicine
ISSN : 2334-1815
Launched : 2013
Journal of Ear, Nose and Throat Disorders
ISSN : 2475-9473
Launched : 2016
JSM Ophthalmology
ISSN : 2333-6447
Launched : 2013
Journal of Pharmacology and Clinical Toxicology
ISSN : 2333-7079
Launched : 2013
Annals of Psychiatry and Mental Health
ISSN : 2374-0124
Launched : 2013
Medical Journal of Obstetrics and Gynecology
ISSN : 2333-6439
Launched : 2013
Annals of Pediatrics and Child Health
ISSN : 2373-9312
Launched : 2013
JSM Clinical Pharmaceutics
ISSN : 2379-9498
Launched : 2014
JSM Foot and Ankle
ISSN : 2475-9112
Launched : 2016
JSM Alzheimer's Disease and Related Dementia
ISSN : 2378-9565
Launched : 2014
Journal of Addiction Medicine and Therapy
ISSN : 2333-665X
Launched : 2013
Journal of Veterinary Medicine and Research
ISSN : 2378-931X
Launched : 2013
Annals of Public Health and Research
ISSN : 2378-9328
Launched : 2014
Annals of Orthopedics and Rheumatology
ISSN : 2373-9290
Launched : 2013
Journal of Clinical Nephrology and Research
ISSN : 2379-0652
Launched : 2014
Annals of Community Medicine and Practice
ISSN : 2475-9465
Launched : 2014
Annals of Biometrics and Biostatistics
ISSN : 2374-0116
Launched : 2013
JSM Clinical Case Reports
ISSN : 2373-9819
Launched : 2013
Journal of Cancer Biology and Research
ISSN : 2373-9436
Launched : 2013
Journal of Surgery and Transplantation Science
ISSN : 2379-0911
Launched : 2013
Journal of Dermatology and Clinical Research
ISSN : 2373-9371
Launched : 2013
JSM Gastroenterology and Hepatology
ISSN : 2373-9487
Launched : 2013
Annals of Nursing and Practice
ISSN : 2379-9501
Launched : 2014
JSM Dentistry
ISSN : 2333-7133
Launched : 2013
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