Design, synthesis and antimycobacterial evaluation of novel adamantane and adamantanol analogues effective against drug-resistant tuberculosis

The treacherous nature of tuberculosis (TB) combined with the ubiquitous presence of the drug-resistant (DR) forms pose this disease as a growing public health menace. Therefore, it is imperative to develop new chemotherapeutic agents with a novel mechanism of action to circumvent the cross-resistan...

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Main Authors: Alsayed, S.S.R., Lun, S., Payne, Alan, Bishai, W.R., Gunosewoyo, Hendra
Format: Journal Article
Language:English
Published: ACADEMIC PRESS INC ELSEVIER SCIENCE 2021
Subjects:
Online Access:http://purl.org/au-research/grants/arc/DE160100482
http://hdl.handle.net/20.500.11937/90998
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author Alsayed, S.S.R.
Lun, S.
Payne, Alan
Bishai, W.R.
Gunosewoyo, Hendra
author_facet Alsayed, S.S.R.
Lun, S.
Payne, Alan
Bishai, W.R.
Gunosewoyo, Hendra
author_sort Alsayed, S.S.R.
building Curtin Institutional Repository
collection Online Access
description The treacherous nature of tuberculosis (TB) combined with the ubiquitous presence of the drug-resistant (DR) forms pose this disease as a growing public health menace. Therefore, it is imperative to develop new chemotherapeutic agents with a novel mechanism of action to circumvent the cross-resistance problems. The unique architecture of the Mycobacterium tuberculosis (M. tb) outer envelope plays a predominant role in its pathogenesis, contributing to its intrinsic resistance against available therapeutic agents. The mycobacterial membrane protein large 3 (MmpL3), which is a key player in forging the M. tb rigid cell wall, represents an emerging target for TB drug development. Several indole-2-carboxamides were previously identified in our group as potent anti-TB agents that act as inhibitor of MmpL3 transporter protein. Despite their highly potent in vitro activities, the lingering Achilles heel of these indoleamides can be ascribed to their high lipophilicity as well as low water solubility. In this study, we report our attempt to improve the aqueous solubility of these indole-2-carboxamides while maintaining an adequate lipophilicity to allow effective M. tb cell wall penetration. A more polar adamantanol moiety was incorporated into the framework of several indole-2-carboxamides, whereupon the corresponding analogues were tested for their anti-TB activity against drug-sensitive (DS) M. tb H37Rv strain. Three adamantanol derivatives 8i, 8j and 8l showed nearly 2- and 4-fold higher activity (MIC = 1.32 – 2.89 µM) than ethambutol (MIC = 4.89 µM). Remarkably, the most potent adamantanol analogue 8j demonstrated high selectivity towards DS and DR M. tb strains over mammalian cells [IC50 (Vero cells) ≥ 169 µM], evincing its lack of cytotoxicity. The top eight active compounds 8b, 8d, 8f, 8i, 8j, 8k, 8l and 10a retained their in vitro potency against DR M. tb strains and were docked into the MmpL3 active site. The most potent adamantanol/adamantane-based indoleamides 8j/8k displayed a two-fold surge in potency against extensively DR (XDR) M. tb strains with MIC values of 0.66 and 0.012 µM, respectively. The adamantanol-containing indole-2-carboxamides exhibited improved water solubility both in silico and experimentally, relative to the adamantane counterparts. Overall, the observed antimycobacterial and physicochemical profiles support the notion that adamantanol moiety is a suitable replacement to the adamantane scaffold within the series of indole-2-carboxamide-based MmpL3 inhibitors.
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spelling curtin-20.500.11937-909982023-05-24T01:03:33Z Design, synthesis and antimycobacterial evaluation of novel adamantane and adamantanol analogues effective against drug-resistant tuberculosis Alsayed, S.S.R. Lun, S. Payne, Alan Bishai, W.R. Gunosewoyo, Hendra Science & Technology Life Sciences & Biomedicine Physical Sciences Biochemistry & Molecular Biology Chemistry, Organic Chemistry Tuberculosis MmpL3 Indoleamides Adamantane Adamantanol MDR-TB XDR-TB Cytotoxicity Water solubility MYCOLIC ACID TRANSPORT MYCOBACTERIUM-TUBERCULOSIS MULTIDRUG-RESISTANT BIOLOGICAL EVALUATION MEMBRANE TRANSPORTER CELL-WALL MMPL3 DISCOVERY TARGETS DERIVATIVES Adamantane Adamantanol Cytotoxicity Indoleamides MDR-TB MmpL3 Tuberculosis Water solubility XDR-TB Adamantane Antitubercular Agents Dose-Response Relationship, Drug Drug Design Microbial Sensitivity Tests Models, Molecular Molecular Structure Mycobacterium tuberculosis Structure-Activity Relationship Tuberculosis, Multidrug-Resistant Mycobacterium tuberculosis Tuberculosis, Multidrug-Resistant Adamantane Antitubercular Agents Microbial Sensitivity Tests Molecular Structure Structure-Activity Relationship Dose-Response Relationship, Drug Drug Design Models, Molecular The treacherous nature of tuberculosis (TB) combined with the ubiquitous presence of the drug-resistant (DR) forms pose this disease as a growing public health menace. Therefore, it is imperative to develop new chemotherapeutic agents with a novel mechanism of action to circumvent the cross-resistance problems. The unique architecture of the Mycobacterium tuberculosis (M. tb) outer envelope plays a predominant role in its pathogenesis, contributing to its intrinsic resistance against available therapeutic agents. The mycobacterial membrane protein large 3 (MmpL3), which is a key player in forging the M. tb rigid cell wall, represents an emerging target for TB drug development. Several indole-2-carboxamides were previously identified in our group as potent anti-TB agents that act as inhibitor of MmpL3 transporter protein. Despite their highly potent in vitro activities, the lingering Achilles heel of these indoleamides can be ascribed to their high lipophilicity as well as low water solubility. In this study, we report our attempt to improve the aqueous solubility of these indole-2-carboxamides while maintaining an adequate lipophilicity to allow effective M. tb cell wall penetration. A more polar adamantanol moiety was incorporated into the framework of several indole-2-carboxamides, whereupon the corresponding analogues were tested for their anti-TB activity against drug-sensitive (DS) M. tb H37Rv strain. Three adamantanol derivatives 8i, 8j and 8l showed nearly 2- and 4-fold higher activity (MIC = 1.32 – 2.89 µM) than ethambutol (MIC = 4.89 µM). Remarkably, the most potent adamantanol analogue 8j demonstrated high selectivity towards DS and DR M. tb strains over mammalian cells [IC50 (Vero cells) ≥ 169 µM], evincing its lack of cytotoxicity. The top eight active compounds 8b, 8d, 8f, 8i, 8j, 8k, 8l and 10a retained their in vitro potency against DR M. tb strains and were docked into the MmpL3 active site. The most potent adamantanol/adamantane-based indoleamides 8j/8k displayed a two-fold surge in potency against extensively DR (XDR) M. tb strains with MIC values of 0.66 and 0.012 µM, respectively. The adamantanol-containing indole-2-carboxamides exhibited improved water solubility both in silico and experimentally, relative to the adamantane counterparts. Overall, the observed antimycobacterial and physicochemical profiles support the notion that adamantanol moiety is a suitable replacement to the adamantane scaffold within the series of indole-2-carboxamide-based MmpL3 inhibitors. 2021 Journal Article http://hdl.handle.net/20.500.11937/90998 10.1016/j.bioorg.2020.104486 English http://purl.org/au-research/grants/arc/DE160100482 http://creativecommons.org/licenses/by-nc-nd/4.0/ ACADEMIC PRESS INC ELSEVIER SCIENCE fulltext
spellingShingle Science & Technology
Life Sciences & Biomedicine
Physical Sciences
Biochemistry & Molecular Biology
Chemistry, Organic
Chemistry
Tuberculosis
MmpL3
Indoleamides
Adamantane
Adamantanol
MDR-TB
XDR-TB
Cytotoxicity
Water solubility
MYCOLIC ACID TRANSPORT
MYCOBACTERIUM-TUBERCULOSIS
MULTIDRUG-RESISTANT
BIOLOGICAL EVALUATION
MEMBRANE TRANSPORTER
CELL-WALL
MMPL3
DISCOVERY
TARGETS
DERIVATIVES
Adamantane
Adamantanol
Cytotoxicity
Indoleamides
MDR-TB
MmpL3
Tuberculosis
Water solubility
XDR-TB
Adamantane
Antitubercular Agents
Dose-Response Relationship, Drug
Drug Design
Microbial Sensitivity Tests
Models, Molecular
Molecular Structure
Mycobacterium tuberculosis
Structure-Activity Relationship
Tuberculosis, Multidrug-Resistant
Mycobacterium tuberculosis
Tuberculosis, Multidrug-Resistant
Adamantane
Antitubercular Agents
Microbial Sensitivity Tests
Molecular Structure
Structure-Activity Relationship
Dose-Response Relationship, Drug
Drug Design
Models, Molecular
Alsayed, S.S.R.
Lun, S.
Payne, Alan
Bishai, W.R.
Gunosewoyo, Hendra
Design, synthesis and antimycobacterial evaluation of novel adamantane and adamantanol analogues effective against drug-resistant tuberculosis
title Design, synthesis and antimycobacterial evaluation of novel adamantane and adamantanol analogues effective against drug-resistant tuberculosis
title_full Design, synthesis and antimycobacterial evaluation of novel adamantane and adamantanol analogues effective against drug-resistant tuberculosis
title_fullStr Design, synthesis and antimycobacterial evaluation of novel adamantane and adamantanol analogues effective against drug-resistant tuberculosis
title_full_unstemmed Design, synthesis and antimycobacterial evaluation of novel adamantane and adamantanol analogues effective against drug-resistant tuberculosis
title_short Design, synthesis and antimycobacterial evaluation of novel adamantane and adamantanol analogues effective against drug-resistant tuberculosis
title_sort design, synthesis and antimycobacterial evaluation of novel adamantane and adamantanol analogues effective against drug-resistant tuberculosis
topic Science & Technology
Life Sciences & Biomedicine
Physical Sciences
Biochemistry & Molecular Biology
Chemistry, Organic
Chemistry
Tuberculosis
MmpL3
Indoleamides
Adamantane
Adamantanol
MDR-TB
XDR-TB
Cytotoxicity
Water solubility
MYCOLIC ACID TRANSPORT
MYCOBACTERIUM-TUBERCULOSIS
MULTIDRUG-RESISTANT
BIOLOGICAL EVALUATION
MEMBRANE TRANSPORTER
CELL-WALL
MMPL3
DISCOVERY
TARGETS
DERIVATIVES
Adamantane
Adamantanol
Cytotoxicity
Indoleamides
MDR-TB
MmpL3
Tuberculosis
Water solubility
XDR-TB
Adamantane
Antitubercular Agents
Dose-Response Relationship, Drug
Drug Design
Microbial Sensitivity Tests
Models, Molecular
Molecular Structure
Mycobacterium tuberculosis
Structure-Activity Relationship
Tuberculosis, Multidrug-Resistant
Mycobacterium tuberculosis
Tuberculosis, Multidrug-Resistant
Adamantane
Antitubercular Agents
Microbial Sensitivity Tests
Molecular Structure
Structure-Activity Relationship
Dose-Response Relationship, Drug
Drug Design
Models, Molecular
url http://purl.org/au-research/grants/arc/DE160100482
http://hdl.handle.net/20.500.11937/90998