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New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds

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A special issue of Molecules (ISSN 1420-3049). This special issue belongs to the section "Medicinal Chemistry".

Deadline for manuscript submissions: closed (31 May 2025) | Viewed by 20435

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Prof. Dr. Constantinos Athanassopoulos

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Guest Editor

Department of Chemistry, University of Patras, GR-26504 Patras, Greece
Interests: small organic molecules; natural products; anticancer and antibacterial agents; multitarget inhibitors; hybrids; bioconjugates
Special Issues, Collections and Topics in MDPI journals

Dr. Antonia Antoniou

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Department of Chemistry, University of Milan, I-20122 Milan, Italy
Interests: anticancer and anti-neurodegenerative agents; self-assembled nanoparticles; liposomal nanovectors; imaging-friendly liposomes

Special Issue Information

Dear Colleagues,

Multidrug resistance (MDR) is one of the major obstacles to clinical treatment, resulting from different defensive mechanisms in cancer. To circumvent MDR many reversal agents have been developed, from a broad collaboration between synthetic/ medicinal chemists and biologists. At present, a plethora of synthetic strategies helps researchers in building molecular libraries, often having templates directly inspired by nature. As a consequence, the development of new methods that can be applied in preparing new and powerful bioactive compounds is a fundamental need for the treatment of MDR tumors.

In this Special Issue, we wish to focus on the most recent research efforts, toward the discovery of lead compounds and the development of drug candidates for successful therapies against MDR tumors. Special attention will be given to interdisciplinary studies on novel therapeutic agents targeting specific receptors, enzymes, or cellular pathways related to MDR.

Original research articles, reviews, and focus papers will be welcome, with the aim of collecting the most recent insights and results on new and straightforward synthetic approaches to bioactive organic compounds, the preparation of molecular templates for combinatorial chemistry, as well as the application of computational methods for the rational design and synthesis of novel lead drug candidates, focusing on fighting MDR tumors.

Prof. Dr. Constantinos Athanassopoulos
Dr. Antonia Antoniou
Guest Editors

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Keywords

cancer chemotherapy
multi-drug resistance (MDR)
design and synthesis of MDR reversing agents
structure-activity relationship studies
MDR active targeting
hybrids and conjugates
drug repurposing
modulators/ inhibitors of MDR transporters

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Published Papers (10 papers)

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Research

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12 pages, 2911 KiB

Open AccessArticle

A pH-Sensitive Glutathione Responsive Small-Molecule Probe TZ2 Sensitizes Lung Cancer Cells to Chemotherapy by Targeting Tumor Microenvironment

by Changle Zhong, Minghan Lu, Guanhao Pan, Xintong You, Yan Peng, Shulan Zeng and Guohai Zhang

Molecules 2025, 30(15), 3081; https://doi.org/10.3390/molecules30153081 - 23 Jul 2025

Viewed by 303

Abstract

The tumor microenvironment plays an important role in tumor incidence, metastasis, and chemotherapy resistance. Novel therapeutic strategies targeting the tumor microenvironment have become a research focus in the field of biomedicine. In this study, we developed a smart small-molecule probe, TZ2, featuring pH/GSH dual-responsive characteristics. TZ2 exhibits a unique pH-dependent reaction mechanism: GSH is preferentially covalently modified with maleimide groups in acidic microenvironments (pH < 7), while specifically activating nucleophilic substitutions under alkaline conditions (pH > 7). It is worth noting that TZ2 effectively eliminates intracellular glutathione (GSH) in a time and concentration-dependent manner, demonstrating significant GSH depletion ability in various tumor cell lines. Pharmacodynamic studies have shown that TZ2 not only inhibits the cell cycle by regulating the expression of cell cycle-related proteins, but also effectively suppresses the cloning ability of cancer cells. Furthermore, TZ2 significantly increases the sensitivity of drug-resistant cancer cells to cisplatin. By integrating microenvironment modulation, real-time monitoring, and synergistic therapy, TZ2 provides a novel molecular tool and theoretical basis for tumor theranostics integration. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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14 pages, 2434 KiB

Open AccessArticle

Drug-Resistant Cholangiocarcinoma Cell Lines for Therapeutic Evaluation of Novel Drugs

by Kevin Delgado-Calvo, Elisa Lozano, Oscar Briz, Candela Cives-Losada, Jose J. G. Marin and Rocio I. R. Macias

Molecules 2025, 30(14), 3053; https://doi.org/10.3390/molecules30143053 - 21 Jul 2025

Viewed by 614

Abstract

The pharmacological treatment of cholangiocarcinoma (CCA) is often hampered by tumor resistance. Improving our understanding of this issue is crucial for developing strategies that can overcome drug refractoriness. We have established and characterized two novel human cell sublines derived from extrahepatic CCA EGI-1 cells that are resistant to cisplatin and 5-fluorouracil (5-FU). Migration and proliferation were analyzed using holographic microscopy. The expression of genes involved in drug uptake and efflux was determined by RT-qPCR. Cross-resistance to commonly used antitumor drugs was assayed using the MTT test. EGI-1 sublines resistant to cisplatin (CR) or 5-FU (FR) exhibited more than a three-fold increase in resistance to cisplatin and 5-FU, respectively, and showed reduced proliferation, migration, and colony-formation rates, along with an altered cell cycle compared to wild-type cells, while retaining tumorigenic capacity. The analysis of the transportome showed downregulation of uptake transporters and upregulation of the export pumps MRP3/4. EGI-1 cells with acquired resistance to 5-FU demonstrated cross-resistance to irinotecan and gemcitabine, while cisplatin-resistant cells showed decreased sensitivity to 5-FU and platinum derivatives. These resistant cell lines offer valuable models for investigating the molecular basis of chemoresistance in CCA, providing a robust platform for the development and evaluation of novel therapeutic strategies. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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21 pages, 2231 KiB

Open AccessArticle

A Quantitative Model of Chemotherapeutic Drug Sensitivity as a Function of P-Glycoprotein Expression

by Cara M. Robertus, Nisha Kannan and David Putnam

Molecules 2025, 30(14), 3014; https://doi.org/10.3390/molecules30143014 - 18 Jul 2025

Viewed by 328

Abstract

(1) Background: Overexpression of P-glycoprotein (P-gp) is one mediator of multidrug resistance in cancer. While many studies demonstrate the efficacy of modulating P-glycoprotein expression to increase drug response in cancer cells, the nature of the mathematical relationship between drug sensitivity and P-glycoprotein surface density is not yet characterized. (2) Methods: In this study, we employ siRNA to modulate P-gp expression in two model cell lines and evaluate their steady-state response to three common chemotherapeutics in vitro. Additionally, we model the kinetics of calcein-AM, a P-gp substrate, as a function of P-gp expression. (3) Results: For both cell lines, a robust linear relationship governs chemotherapeutic sensitivity as a function of P-gp expression, demonstrating that characterization of P-gp surface density is a strong indicator of drug response in drug-resistant cells. Furthermore, calcein accumulation and initial influx rate exhibit first-order kinetics with respect to P-gp density, further elucidating the nature of substrate interactions with P-gp-overexpressing cells. When transport kinetics are evaluated using a Michaelis–Menten model, V_max varies with P-gp density according to a first-order relationship. (4) Conclusions: These results establish the mathematical relationships between chemotherapeutic response and substrate influx as a function of P-gp expression and suggest that rational changes in P-gp expression could be used as a predictive measure of drug sensitivity in model cell lines. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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15 pages, 7465 KiB

Open AccessArticle

Soloxolone N-3-(Dimethylamino)propylamide Restores Drug Sensitivity of Tumor Cells with Multidrug-Resistant Phenotype via Inhibition of P-Glycoprotein Efflux Function

by Arseny D. Moralev, Oksana V. Salomatina, Nariman F. Salakhutdinov, Marina A. Zenkova and Andrey V. Markov

Molecules 2024, 29(20), 4939; https://doi.org/10.3390/molecules29204939 - 18 Oct 2024

Cited by 1 | Viewed by 1316

Abstract

Multidrug resistance (MDR) remains a significant challenge in cancer therapy, primarily due to the overexpression of transmembrane drug transporters, with P-glycoprotein (P-gp) being a central focus. Consequently, the development of P-gp inhibitors has emerged as a promising strategy to combat MDR. Given the P-gp targeting potential of soloxolone amides previously predicted by us by an absorption, distribution, metabolism, excretion, and toxicity (ADMET) analysis, the aim of the current study was to experimentally verify their P-gp inhibitory and MDR reversing activities in vitro. Screening of soloxolone amides as modulators of P-gp using molecular docking and cellular P-gp substrate efflux assays revealed the ability of compound 4 bearing a N-3-(dimethylamino)propylamide group to interact with the active site of P-gp and inhibit its transport function. Blind and site-specific molecular docking accompanied by a kinetic assay showed that 4 directly binds to the P-gp transmembrane domain with a binding energy similar to that of zosuquidar, a third-generation P-gp inhibitor (ΔG = −10.3 kcal/mol). In vitro assays confirmed that compound 4 enhanced the uptake of Rhodamine 123 (Rho123) and doxorubicin (DOX) by the P-gp-overexpressing human cervical carcinoma KB-8-5 (by 10.2- and 1.5-fold, respectively (p < 0.05, unpaired t-test)) and murine lymphosarcoma RLS40 (by 15.6- and 1.75-fold, respectively (p < 0.05, unpaired t-test)) cells at non-toxic concentrations. In these cell models, 4 showed comparable or slightly higher activity than the reference inhibitor verapamil (VPM), with the most pronounced effect of the hit compound in Rho123-loaded RLS40 cells, where 4 was 2-fold more effective than VPM. Moreover, 4 synergistically restored the sensitivity of KB-8-5 cells to the cytotoxic effect of DOX, demonstrating MDR reversal activity. Based on the data obtained, 4 can be considered as a drug candidate to combat the P-gp-mediated MDR of tumor cells and semisynthetic triterpenoids, with amide moieties in general representing a promising scaffold for the development of novel therapeutics for tumors with low susceptibility to antineoplastic agents. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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20 pages, 5343 KiB

Open AccessArticle

Novel Pyrimidine Derivatives as Antioxidant and Anticancer Agents: Design, Synthesis and Molecular Modeling Studies

by Malama Myriagkou, Evangelia Papakonstantinou, Georgia-Eirini Deligiannidou, Alexandros Patsilinakos, Christos Kontogiorgis and Eleni Pontiki

Molecules 2023, 28(9), 3913; https://doi.org/10.3390/molecules28093913 - 5 May 2023

Cited by 30 | Viewed by 4786

Abstract

The heterocyclic ring system of pyrido [2,3-d]pyrimidines is a privileged scaffold in medicinal chemistry, possessing several biological activities. The synthesis of the pyrimidine derivatives was performed via the condensation of a suitable α,β-unsaturated ketone with 4-amino-6-hydroxy-2-mercaptopyrimidine monohydrate in glacial acetic acid. Chalcones were synthesized, as starting materials, via the Claisen–Schmidt condensation of an appropriately substituted ketone and an appropriately substituted aldehyde in the presence of aqueous KOH 40% w/v in ethanol. All the synthesized compounds were characterized using IR, ¹H-NMR, ¹³C-NMR, LC-MS and elemental analysis. The synthesized compounds were evaluated for their antioxidant (DPPH assay), anti-lipid peroxidation (AAPH), anti-LOX activities and ability to interact with glutathione. The compounds do not interact significantly with DPPH but strongly inhibit lipid peroxidation. Pyrimidine derivatives 2a (IC₅₀ = 42 μΜ), 2f (IC₅₀ = 47.5 μΜ) and chalcone 1g (IC₅₀ = 17 μM) were the most potent lipoxygenase inhibitors. All the tested compounds were found to interact with glutathione, apart from 1h. Cell viability and cytotoxicity assays were performed with the HaCaT and A549 cell lines, respectively. In the MTT assay towards the HaCaT cell line, none of the compounds presented viability at 100 μM. On the contrary, in the MTT assay towards the A549 cell line, the tested compounds showed strong cytotoxicity at 100 μM, with derivative 2d presenting the strongest cytotoxic effects at the concentration of 50 μΜ. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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14 pages, 2633 KiB

Open AccessArticle

Alvespimycin Inhibits Heat Shock Protein 90 and Overcomes Imatinib Resistance in Chronic Myeloid Leukemia Cell Lines

by Raquel Alves, Diogo Santos, Joana Jorge, Ana Cristina Gonçalves, Steve Catarino, Henrique Girão, Joana Barbosa Melo and Ana Bela Sarmento-Ribeiro

Molecules 2023, 28(3), 1210; https://doi.org/10.3390/molecules28031210 - 26 Jan 2023

Cited by 6 | Viewed by 3105

Abstract

Heat shock protein 90 (HSP90) facilitates folding and stability and prevents the degradation of multiple client proteins. One of these HSP90 clients is BCR-ABL, the oncoprotein characteristic of chronic myeloid leukemia (CML) and the target of tyrosine kinase inhibitors, such as imatinib. Alvespimycin is an HSP90 inhibitor with better pharmacokinetic properties and fewer side effects than other similar drugs, but its role in overcoming imatinib resistance is not yet clarified. This work studied the therapeutic potential of alvespimycin in imatinib-sensitive (K562) and imatinib-resistant (K562-RC and K562-RD) CML cell lines. Metabolic activity was determined by the resazurin assay. Cell death, caspase activity, mitochondrial membrane potential, and cell cycle were evaluated by means of flow cytometry. Cell death was also analyzed by optical microscopy. HSPs expression levels were assessed by western blotting. Alvespimycin reduced metabolic activity in a time-, dose-, and cell line-dependent manner. Resistant cells were more sensitive to alvespimycin with an IC₅₀ of 31 nM for K562-RC and 44 nM for K562-RD, compared to 50 nM for K562. This drug induced apoptosis via the mitochondrial pathway. In K562 cells, alvespimycin induced cell cycle arrest in G₀/G₁. As a marker of HSP90 inhibition, a significant increase in HSP70 expression was observed. Our results suggest that alvespimycin might be a new therapeutic approach to CML treatment, even in cases of resistance to imatinib. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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14 pages, 2404 KiB

Open AccessArticle

Development of Polymersomes Co-Delivering Doxorubicin and Melittin to Overcome Multidrug Resistance

by Eunkyung Han, Doyeon Kim, Youngheun Cho, Seonock Lee, Jungho Kim and Hyuncheol Kim

Molecules 2023, 28(3), 1087; https://doi.org/10.3390/molecules28031087 - 21 Jan 2023

Cited by 14 | Viewed by 2822

Abstract

Multidrug resistance (MDR) is one of the major barriers in chemotherapy. It is often related to the overexpression of efflux receptors such as P-glycoprotein (P-gp). Overexpressed efflux receptors inhibit chemotherapeutic efficacy by pumping out intracellularly delivered anticancer drugs. In P-gp-mediated MDR-related pathways, PI3K/Akt and NF-kB pathways are commonly activated signaling pathways, but these pathways are downregulated by melittin, a main component of bee venom. In this study, a polymersome based on a poly (lactic acid) (PLA)-hyaluronic acid (HA) (20k-10k) di-block copolymer and encapsulating melittin and doxorubicin was developed to overcome anticancer resistance and enhance chemotherapeutic efficacy. Through the simultaneous delivery of doxorubicin and melittin, PI3K/Akt and NF-κB pathways could be effectively inhibited, thereby downregulating P-gp and successfully enhancing chemotherapeutic efficacy. In conclusion, a polymersome carrying an anticancer drug and melittin could overcome MDR by regulating P-gp overexpression pathways. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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13 pages, 2647 KiB

Open AccessArticle

Highly Efficient and Mild Gold (I) Catalyzed Synthesis of 3,8-Diarylidene-2,7-dioxaspiro[4.4]nonane-1,6-diones

by Antonia Iazzetti, Dario Allevi, Andrea Calcaterra, Giancarlo Fabrizi, Antonella Goggiamani, Giulia Mazzoccanti, Alessio Sferrazza, Rosanna Verdiglione and Valeria Vergine

Molecules 2023, 28(1), 300; https://doi.org/10.3390/molecules28010300 - 30 Dec 2022

Cited by 1 | Viewed by 2434

Abstract

The gold-catalyzed cyclization of 2,2-bis(3-arylprop-2-yn1-yl)malonic acid has been proposed as an efficient approach to substituted 3,8-dibenzyl-2,7-dioxaspiro[4.4]nonane-1,6-diones. The reaction proceeds smoothly in mild reaction conditions to give the desired products in quantitative yields in the presence of variously substituted starting materials. In addition, the synthesis of γ-arylidene spirobislactone bearing different substituents on the two aromatic rings has been achieved. This kind of compound could be of great interest in pharmaceutical science given the widespread presence of this scaffold in bioactive natural and synthetic products. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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12 pages, 3145 KiB

Open AccessArticle

Carnosine Potentiates Doxorubicin-Induced Cytotoxicity in Resistant NCI/ADR-RES Cells by Inhibiting P-Glycoprotein—In Silico and In Vitro Evidence

by Mohamed A. Morsy, Mahmoud Kandeel, Ahmed R. N. Ibrahim, Seham A. Abdel-Gaber, Shery Jacob, Katharigatta N. Venugopala, Pottathil Shinu and Mahmoud El-Daly

Molecules 2022, 27(21), 7383; https://doi.org/10.3390/molecules27217383 - 30 Oct 2022

Cited by 3 | Viewed by 2090

Abstract

The activity of the P-glycoprotein (P-gp) transporter encoded by the ABCB1 gene confers resistance to anticancer drugs and contributes to cancer-related mortality and morbidity. Recent studies revealed the cytotoxic effects of the endogenous dipeptide carnosine. The current study aimed to investigate the role of carnosine as a potential inhibitor of P-gp activity. We used molecular docking and molecular dynamic simulations to study the possible binding and stability of carnosine-P-gp interactions compared with verapamil. In vitro assays using doxorubicin-resistant NCI/ADR-RES cells were established to test the effects of carnosine (10–300 µM) on P-gp activity by the rhodamine-123 efflux assay and its effect on cell viability and doxorubicin-induced cytotoxicity. Verapamil (10 µM) was used as a positive control. The results showed that carnosine binding depends mainly on hydrogen bonding with GLU875, GLN946, and ALA871, with a higher average Hbond than verapamil. Carnosine showed significant but weaker than verapamil-induced rhodamine-123 accumulation. Carnosine and verapamil similarly inhibited cell viability. However, verapamil showed a more significant potentiating effect on doxorubicin-induced cytotoxicity than a weaker effect of carnosine at 300 µM. These results suggest that carnosine inhibits P-gp activity and potentiates doxorubicin-induced cytotoxicity at higher concentrations. Carnosine might be a helpful lead compound in the fight against multidrug-resistant cancers. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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Review

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24 pages, 3327 KiB

Open AccessReview

CD44 Variant Expression in Follicular Cell-Derived Thyroid Cancers: Implications for Overcoming Multidrug Resistance

by Benny Mosoane, Michelle McCabe, Brandon S. Jackson and Zodwa Dlamini

Molecules 2025, 30(9), 1899; https://doi.org/10.3390/molecules30091899 - 24 Apr 2025

Cited by 1 | Viewed by 902

Abstract

Thyroid cancer (TC) is a significant global health issue that exhibits notable heterogeneity in incidence and outcomes. In low-resource settings such as Africa, delayed diagnosis and limited healthcare access exacerbate mortality rates. Among follicular cell-derived thyroid cancers—including papillary (PTC), follicular (FTC), anaplastic (ATC), and poorly differentiated (PDTC) subtypes—the role of CD44 variants has emerged as a critical factor influencing tumor progression and multidrug resistance (MDR). CD44, a transmembrane glycoprotein, and its splice variants (CD44v) mediate cell adhesion, migration, and survival, contributing to cancer stem cell (CSC) maintenance and therapy resistance. Differential expression patterns of CD44 isoforms across TC subtypes have shown diagnostic, prognostic, and therapeutic implications. Specifically, CD44v6 expression in PTC has been correlated with metastasis and aggressive tumor behavior, while in FTC, its expression aids in distinguishing malignant from benign lesions. Furthermore, CD44 contributes to MDR through enhanced drug efflux via ABC transporters, apoptosis evasion, and CSC maintenance via the Wnt/β-catenin and PI3K/Akt pathways. Targeted therapies against CD44 such as monoclonal antibodies, hyaluronic acid-based nanocarriers, and gene-editing technologies hold promise in overcoming MDR. However, despite the mounting evidence supporting CD44-targeted strategies in various cancers, research on this therapeutic potential in TC remains limited. This review synthesizes existing knowledge on CD44 variant expression in follicular cell-derived thyroid cancers and highlights potential therapeutic strategies to mitigate MDR, particularly in high-burden regions, thereby improving patient outcomes and survival. Full article

(This article belongs to the Special Issue New Therapeutic Tools against MDR Tumors: Discovery, Synthesis and Evaluation of Bioactive Compounds)

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