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Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria

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A special issue of Biomedicines (ISSN 2227-9059). This special issue belongs to the section "Drug Discovery, Development and Delivery".

Deadline for manuscript submissions: closed (31 August 2023) | Viewed by 19320

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Dr. Maria A. Bonifacio

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Department of Precision and Regenerative Medicine and Ionian Area, University of Bari Aldo Moro Medical School, 70124 Bari, Italy
Interests: tissue engineering; regenerative medicine; spectroscopy; biological characterization; composite materials; hydrogels; coatings; phytochemicals
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Antonio Mazzocca

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Interdisciplinary Department of Medicine, University of Bari School of Medicine, I-70124 Bari, Italy
Interests: cancer theories; endosymbiosis; evolution; complex systems; emerging properties; metabolism; liver cancer; transcriptome; microenvironment; pathobiology

Prof. Dr. Anna Volpe

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Clinic of Infectious Diseases, Department of Biomedical Sciences and Human Oncology, University of Bari Aldo Moro, Bari, Italy
Interests: infectious diseases; HIV; HCV; TBC; sequencing; NGS; resistance-associated mutations; antivirals; ART therapy; inflammaging

Special Issue Information

Dear Colleagues,

Salvador Luria studied the development of bacterial resistance to phages, clarifying that mutations arise randomly and are selected by the presence of phages. The development of the Luria–Delbrück fluctuation test represents a brilliant moment in science, which opened up new landscapes in molecular genetics and led to Luria, Delbrück, and Hershey being awarded a Nobel Prize for their work. Indeed, it has been more than half a century since their study, but it is still relevant today, and Luria’s pioneering work has provided elegant theoretical tools to face the drug resistance phenomenon, which continues to be a contemporary and challenging issue in microbiology and oncohematology.

Is it useful to target cancer, as well as an infectious agent, with the most effective drugs at the first line? What strategies are more promising to hinder the selection and spread of resistant pathogens? When healing is not a concrete option, how can we ensure that the disease becomes chronic rather than terminal and achieve a better quality of life for patients?

All manuscripts providing answers to the above questions are welcome in this Special Issue, which is aimed at celebrating the work of Salvador Luria, on what would have been the year of his 110th birthday. Original research articles and reviews describing innovative approaches to deal with drug resistance will be considered for publication.

Dr. Maria A. Bonifacio
Prof. Dr. Antonio Mazzocca
Prof. Dr. Anna Volpe
Guest Editors

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Keywords

drug resistance
cancer
mutations
anticancer drugs
infectious diseases
drug-resistant pathogens
antiviral
antibiotics
innovative treatments
drug development

Published Papers (10 papers)

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Research

21 pages, 8998 KiB

Open AccessArticle

Expression of Claudin-9 (CLDN9) in Breast Cancer, the Clinical Significance in Connection with Its Subcoat Anchorage Proteins ZO-1 and ZO-3 and Impact on Drug Resistance

by Xinguo Zhuang, Tracey A. Martin, Fiona Ruge, Jianyuan (Jimmy) Zeng, Xinyu (Amber) Li, Elyas Khan, Qingping Dou, Eleri Davies and Wen G. Jiang

Biomedicines 2023, 11(12), 3136; https://doi.org/10.3390/biomedicines11123136 - 24 Nov 2023

Viewed by 1148

Abstract

(1) Introduction: Claudin-9 (CLDN9) is a member of the claudin protein family, a critical transmembrane protein family for tight junctions that are implemented in the progression of numerous cancer types. The present study investigated the role that CLDN9, along with the subcoat proteins, Zonula Occludens (ZOs), plays in clinical breast cancer and subsequent impact on drug response of patients. (2) Methods: CLDN9 protein and CLDN9 transcript were determined and correlated with clinical and pathological indicators, together with the status of hormonal receptors. The levels of CLDN9 transcript were also assessed against the therapeutic responses of the patients to chemotherapies by using a dataset from the TCGA database. Breast cancer cell models, representing different molecular subtypes of breast cancer, with differential expression of CLDN9 were created and used to assess the biological impact and response to chemotherapeutic drugs. (3) Results: Breast cancer tissues expressed significantly higher levels of the CLDN9, with the high levels being associated with shorter survival. CLDN9 was significantly correlated with its anchorage proteins ZO-1 and ZO-3. Integrated expression of CLDN9, ZO-1 and ZO-3 formed a signature that was significantly linked to overall survival (OS) (p = 0.013) and relapse-free survival (RFS) (p = 0.024) in an independent matter. CLDN9 transcript was significantly higher in patients who were resistant to chemotherapies (p < 0.000001). CLDN9 connection to chemoresistance was particularly prominent in patients of ER-positive (ER(+)), Her-2-negative((Her-2(−)), ER(+)/Her-2(−) and triple-negative breast cancers (TNBCs), but not in patients with HER-2-positive tumors. In Her-2-negative MCF7 and MDA-MB-231 cancer cells, loss of CLDN9 significantly increased sensitivity to several chemotherapeutic drugs including paclitaxel, gemcitabine and methotrexate, which was not seen in Her-2(+) SKBR3 cells. However, suppressing Her-2 using neratinib, a permanent Her-2 inhibitor, sensitized cellular response to these chemodrugs in cells with CLDN9 knockdown. (4) Conclusions: CLDN9 is an important prognostic indicator for patients with breast cancer and also a pivotal factor in assessing patient responses to chemotherapies. Her-2 is a negating factor for the treatment response prediction value by CLDN9 and negating Her-2 and CLDN9 may enhance breast cancer cellular response to chemotherapeutic drugs. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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13 pages, 5501 KiB

Open AccessArticle

Resistance Modulation of Individual and Polymicrobial Culture of S. aureus and E. coli through Nanoparticle-Coupled Antibiotics

by Sana Zia, Song Peng, Arslan Bashir, Tasleem Kausar, Shanza Rauf Khan, Afshan Muneer, Attia Nawaz, Lina I. Alnajjar, Mohd Saeed, Nawaf Alshammari, Amjad Islam Aqib and Kun Li

Biomedicines 2023, 11(11), 2988; https://doi.org/10.3390/biomedicines11112988 - 07 Nov 2023

Viewed by 1034

Abstract

Polymicrobial mastitis is now becoming very common in dairy animals, resulting in exaggerated resistance to multiple antibiotics. The current study was executed to find drug responses in individual and mixed Culture of Staphylococcus aureus and Escherichia coli isolated from milk samples, as well as to evaluate the antibacterial potential of tungsten oxide nanoparticles. These isolates (alone and in mixed culture) were further processed for their responses to antibiotics using the disc diffusion method. On the other hand, tungsten oxide WO₃ (W) nanoparticles coupled with antibiotics (ampicillin, A, and oxytetracycline, O) were prepared through the chemical method and characterized by X-ray diffraction, scanning electron microscopy (SEM), and UV-visible techniques. The preparations consisting of nanoparticles alone (W) and coupled with ampicillin (WA) and oxytetracycline (WO) were tested against individual and mixed Culture through the well diffusion and broth microdilution methods. The findings of the current study showed the highest resistance in E. coli was against penicillin (60%) and ampicillin (50%), while amikacin, erythromycin, ciprofloxacin, and oxytetracycline were the most effective antibiotics. S. aureus showed the highest resistance against penicillin (50%), oxytetracycline (40%), and ciprofloxacin (40%), while, except for ampicillin, the sensitive strains of S. aureus were in the range of 40–60% against the rest of antibiotics. The highest zones of inhibition (ZOI) against mixed Culture were shown by imipenem and ampicillin, whereas the highest percentage decrease in ZOI was noted in cases of ciprofloxacin (−240%) and gentamicin (−119.4%) in comparison to individual Culture of S. aureus and E. coli. It was noteworthy that the increase in ZOI was not more than 38% against mixed Culture as compared to the individual Culture. On the other hand, there was a significant reduction in the minimum inhibitory concentration (MIC) of nanoparticle-coupled antibiotics compared to nanoparticles alone for individual and mixed-culture bacteria, while MICs in the case of mixed Culture remained consistently high throughout the trial. This study therefore concluded that diverse drug resistance was present in both individual and mixed-culture bacteria, whereas the application of tungsten oxide nanoparticle-coupled antibiotics proved to be an effective candidate in reversing the drug resistance in bacterial strains. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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27 pages, 6199 KiB

Open AccessArticle

Synergy Assessment of Four Antimicrobial Bioactive Compounds for the Combinational Treatment of Bacterial Pathogens

by Kevin Masterson, Ian Major, Mark Lynch and Neil Rowan

Biomedicines 2023, 11(8), 2216; https://doi.org/10.3390/biomedicines11082216 - 07 Aug 2023

Viewed by 1060

Abstract

Antimicrobial resistance (AMR) has become a topic of great concern in recent years, with much effort being committed to developing alternative treatments for resistant bacterial pathogens. Drug combinational therapies have been a major area of research for several years, with modern iterations using combining well-established antibiotics and other antimicrobials with the aim of discovering complementary mechanisms. Previously, we characterised four GRAS antimicrobials that can withstand thermal polymer extrusion processes for novel medical device-based and therapeutic applications. In the present study, four antimicrobial bioactive—silver nitrate, nisin, chitosan and zinc oxide—were assessed for their potential combined use as an alternative synergistic treatment for AMR bacteria via a broth microdilution assay based on a checkerboard format. The bioactives were tested in arrangements of two-, three- and four-drug combinations, and their interactions were determined and expressed in terms of a synergy score. Results have revealed interesting interactions based on treatments against recognised test bacterial strains that cause human and animal infections, namely E. coli, S. aureus and S. epidermidis. Silver nitrate was seen to greatly enhance the efficacy of its paired treatment. Combinations with nisin, which is a lantibiotic, exhibited the most interesting results, as nisin has no effect against Gram-negative bacteria when used alone; however, it demonstrated antimicrobial effects when combined with silver nitrate or chitosan. This study constitutes the first study to both report on practical three- and four-drug combinational assays and utilise these methods for the assessment of established and emerging antimicrobials. The novel methods and results presented in this study show the potential to explore previously unknown drug combination compatibility measures in an ease-of-use- and high-throughput-based format, which can greatly help future research that aims to identify appropriate alternative treatments for AMR, including the screening of potential new bioactives biorefined from various sources. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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14 pages, 642 KiB

Open AccessArticle

Computational Guided Drug Targets Identification against Extended-Spectrum Beta-Lactamase-Producing Multi-Drug Resistant Uropathogenic Escherichia coli

by Harpreet Kaur, Vinay Modgil, Naveen Chaudhary, Balvinder Mohan and Neelam Taneja

Biomedicines 2023, 11(7), 2028; https://doi.org/10.3390/biomedicines11072028 - 19 Jul 2023

Cited by 2 | Viewed by 1483

Abstract

Urinary tract infections (UTIs) are one of the most frequent bacterial infections in the world, both in the hospital and community settings. Uropathogenic Escherichia coli (UPEC) are the predominant etiological agents causing UTIs. Extended-spectrum beta-lactamase (ESBL) production is a prominent mechanism of resistance that hinders the antimicrobial treatment of UTIs caused by UPEC and poses a substantial danger to the arsenal of antibiotics now in use. As bacteria have several methods to counteract the effects of antibiotics, identifying new potential drug targets may help in the design of new antimicrobial agents, and in the control of the rising trend of antimicrobial resistance (AMR). The public availability of the entire genome sequences of humans and many disease-causing organisms has accelerated the hunt for viable therapeutic targets. Using a unique, hierarchical, in silico technique using computational tools, we discovered and described potential therapeutic drug targets against the ESBL-producing UPEC strain NA114. Three different sets of proteins (chokepoint, virulence, and resistance genes) were explored in phase 1. In phase 2, proteins shortlisted from phase 1 were analyzed for their essentiality, non-homology to the human genome, and gut flora. In phase 3, the further shortlisted putative drug targets were qualitatively characterized, including their subcellular location, broad-spectrum potential, and druggability evaluations. We found seven distinct targets for the pathogen that showed no similarity to the human proteome. Thus, possibilities for cross-reactivity between a target-specific antibacterial and human proteins were minimized. The subcellular locations of two targets, ECNA114_0085 and ECNA114_1060, were predicted as cytoplasmic and periplasmic, respectively. These proteins play an important role in bacterial peptidoglycan biosynthesis and inositol phosphate metabolism, and can be used in the design of drugs against these bacteria. Inhibition of these proteins will be helpful to combat infections caused by MDR UPEC. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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18 pages, 15207 KiB

Open AccessArticle

A CAF-Based Two-Cell Hybrid Co-Culture Model to Test Drug Resistance in Endometrial Cancers

by Raed Sulaiman, Pradip De, Jennifer C. Aske, Xiaoqian Lin, Adam Dale, Kris Gaster, Luis Rojas Espaillat, David Starks and Nandini Dey

Biomedicines 2023, 11(5), 1326; https://doi.org/10.3390/biomedicines11051326 - 29 Apr 2023

Viewed by 1716

Abstract

The management of advanced or recurrent endometrial cancers presents a challenge due to the development of resistance to treatments. The knowledge regarding the role of the tumor microenvironment (TME) in determining the disease’s progression and treatment outcome has evolved in recent years. As a TME component, cancer-associated fibroblasts (CAFs) are essential in developing drug-induced resistance in various solid tumors, including endometrial cancers. Hence, an unmet need exists to test the role of endometrial CAF in overcoming the roadblock of resistance in endometrial cancers. We present a novel tumor–TME two-cell ex vivo model to test CAF’s role in resisting the anti-tumor drug, paclitaxel. Endometrial CAFs, both NCAFs (tumor-adjacent normal-tissue-derived CAFs) and TCAFs (tumor-tissue-derived CAFs) were validated by their expression markers. Both TCAFs and NCAFs expressed positive markers of CAF, including SMA, FAP, and S100A4, in varying degrees depending on the patients, while they consistently lacked the negative marker of CAF, EpCAM, as tested via flow cytometry and ICC. CAFs expressed TE-7 and immune marker, PD-L1, via ICC. CAFs better resisted the growth inhibitory effect of paclitaxel on endometrial tumor cells in 2D and 3D formats compared to the resistance of the tumoricidal effect of paclitaxel in the absence of CAFs. TCAF resisted the growth inhibitory effect of paclitaxel on endometrial AN3CA and RL-95-2 cells in an HyCC 3D format. Since NCAF similarly resisted the growth inhibitor action of paclitaxel, we tested NCAF and TCAF from the same patient to demonstrate the protective action of NCAF and TCAF in resisting the tumoricidal effect of paclitaxel in AN3CA in both 2D and 3D matrigel formats. Using this hybrid co-culture CAF and tumor cells, we established a patient-specific, laboratory-friendly, cost-effective, and time-sensitive model system to test drug resistance. The model will help test the role of CAFs in developing drug resistance and contribute to understanding tumor cell-CAF dialogue in gynecological cancers and beyond. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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18 pages, 3099 KiB

Open AccessArticle

Identification and Elimination of Antifungal Tolerance in Candida auris

by Samira Rasouli Koohi, Shamanth A. Shankarnarayan, Clare Maristela Galon and Daniel A. Charlebois

Biomedicines 2023, 11(3), 898; https://doi.org/10.3390/biomedicines11030898 - 14 Mar 2023

Cited by 1 | Viewed by 2363

Abstract

Antimicrobial resistance is a global health crisis to which pathogenic fungi make a substantial contribution. The human fungal pathogen C. auris is of particular concern due to its rapid spread across the world and its evolution of multidrug resistance. Fluconazole failure in C. auris has been recently attributed to antifungal “tolerance”. Tolerance is a phenomenon whereby a slow-growing subpopulation of tolerant cells, which are genetically identical to susceptible cells, emerges during drug treatment. We use microbroth dilution and disk diffusion assays, together with image analysis, to investigate antifungal tolerance in C. auris to all three classes of antifungal drugs used to treat invasive candidiasis. We find that (1) C. auris is tolerant to several common fungistatic and fungicidal drugs, which in some cases can be detected after 24 h, as well as after 48 h, of antifungal drug exposure; (2) the tolerant phenotype reverts to the susceptible phenotype in C. auris; and (3) combining azole, polyene, and echinocandin antifungal drugs with the adjuvant chloroquine in some cases reduces or eliminates tolerance and resistance in patient-derived C. auris isolates. These results suggest that tolerance contributes to treatment failure in C. auris infections for a broad range of antifungal drugs, and that antifungal adjuvants may improve treatment outcomes for patients infected with antifungal-tolerant or antifungal-resistant fungal pathogens. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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10 pages, 1975 KiB

Open AccessArticle

Intravenous Infusion of High Dose Selenite in End-Stage Cancer Patients: Analysis of Systemic Exposure to Selenite and Seleno-Metabolites

by Olof Breuer, Ola Brodin, Ali Razaghi, David Brodin, Bente Gammelgaard and Mikael Björnstedt

Biomedicines 2023, 11(2), 295; https://doi.org/10.3390/biomedicines11020295 - 20 Jan 2023

Cited by 1 | Viewed by 1423

Abstract

Cancer is one of the main causes of human death globally and novel chemotherapeutics are desperately required. As a simple selenium oxide, selenite is a very promising chemotherapeutic because of pronounced its dose-dependent tumor-specific cytotoxicity. We previously published a first-in-man systematic phase I clinical trial in patients with cancer (from IV to end-stage) (the SECAR trial) showing that selenite is safe and tolerable with an unexpectable high maximum tolerated dose (MTD) and short half-life. In the present study, we analyzed the selenium species in plasma samples, from the patients participating in the SECAR trial and from various time points and dose cohorts using LC-ICP-MS. In conclusion, selenite, selenosugars, and 1–2 unidentified peaks that did not correspond to any standard, herein denoted ui-selenium, were detected in the plasma. However, trimethylated selenium (trimethylselenonoium) was not detected. The unidentified ui-selenium was eluting close to the selenium-containing amino acids (selenomethionine and selenocysteine) but was not part of a protein fraction. Our data demonstrate that the major metabolite detected was selenosugar. Furthermore, the identification of selenite even long after the administration is remarkable and unexpected. The kinetic analysis did not support that dosing per the body surface area would reduce interindividual variability of the systemic exposure in terms of trough concentrations. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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13 pages, 3548 KiB

Open AccessArticle

Coupling CRISPR/Cas9 and Lambda Red Recombineering System for Genome Editing of Salmonella Gallinarum and the Effect of ssaU Knock-Out Mutant on the Virulence of Bacteria

by Hamza Tahir, Abdul Basit, Hafsa Tariq, Zulquernain Haider, Asim Ullah, Zafar Hayat and Shafiq Ur Rehman

Biomedicines 2022, 10(12), 3028; https://doi.org/10.3390/biomedicines10123028 - 24 Nov 2022

Cited by 1 | Viewed by 2903

Abstract

The poultry industry in developing countries still faces a significant threat from fowl typhoid, a disease caused by Salmonella Gallinarum that has been well contained in more economically developed countries. In addition to the virulence exhibited by large virulence plasmid (85 kb), Salmonella Pathogenicity Island 2 in S. Gallinarum plays a key role in mediating disease through its type III secretion systems (TTSS). The TTSS secrete effector protein across the Salmonella containing vacuoles and mediate the internalization of bacteria by modulating vesicular passage. In this study, candidate virulent ssaU gene (~1 kb) encoding type III secretion system was successfully deleted from indigenously isolated S. Gallinarum genome through homology-directed repair using CRISPR/Cas9 and lambda recombination systems. CRISPR/Cas9-based genome editing of poultry-derived Salmonella Gallinarum has not been previously reported, which might be linked to a lack of efficiency in its genetic tools. This is the first study which demonstrates a complete CRISPR/Cas9-based gene deletion from this bacterial genome. More importantly, a poultry experimental model was employed to assess the virulence potential of this mutant strain (ΔssaU_SG18) which was unable to produce any mortality in the experimentally challenged birds as compared to the wild type strain. No effect on weight gain was observed whereas bacteria were unable to colonize the intestine and liver in our challenge model. This in vivo loss of virulence in mutant strain provides an excellent functionality of this system to be useful in live vaccine development against this resistant and patho genic bacteria. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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12 pages, 860 KiB

Open AccessArticle

Protein-Functionalized Microgel for Multiple Myeloma Cells’ 3D Culture

by Juan Carlos Marín-Payá, Sandra Clara-Trujillo, Lourdes Cordón, Gloria Gallego Ferrer, Amparo Sempere and José Luis Gómez Ribelles

Biomedicines 2022, 10(11), 2797; https://doi.org/10.3390/biomedicines10112797 - 03 Nov 2022

Viewed by 1464

Abstract

Multiple myeloma is a hematologic neoplasm caused by an uncontrolled clonal proliferation of neoplastic plasma cells (nPCs) in the bone marrow. The development and survival of this disease is tightly related to the bone marrow environment. Proliferation and viability of nPCs depend on their interaction with the stromal cells and the extracellular matrix components, which also influences the appearance of drug resistance. Recapitulating these interactions in an in vitro culture requires 3D environments that incorporate the biomolecules of interest. In this work, we studied the proliferation and viability of three multiple myeloma cell lines in a microgel consisting of biostable microspheres with fibronectin (FN) on their surfaces. We also showed that the interaction of the RPMI8226 cell line with FN induced cell arrest in the G0/G1 cell cycle phase. RPMI8226 cells developed a significant resistance to dexamethasone, which was reduced when they were treated with dexamethasone and bortezomib in combination. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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14 pages, 2910 KiB

Open AccessArticle

The Antifungal and Antibiofilm Activities of Caffeine against Candida albicans on Polymethyl Methacrylate Denture Base Material

by Doaa M. AlEraky, Hatem M. Abuohashish, Mohammed M. Gad, Muneer H. Alshuyukh, Amr S. Bugshan, Khalid S. Almulhim and Maha M. Mahmoud

Biomedicines 2022, 10(9), 2078; https://doi.org/10.3390/biomedicines10092078 - 25 Aug 2022

Cited by 6 | Viewed by 2881

Abstract

Background: In this study, the effect of pure caffeine was established against Candida albicans (C. albicans) using different microbiological techniques. Methods: Broth microdilution and colony forming units (CFUs) assays were used to detect the minimum inhibitory concentration (MIC) and minimum fungicidal concentration (MFC). The Live/Dead fluorescent dyes were implemented to determine the yeast viability. Polymethyl methacrylate acrylic resin (PMMA) discs were prepared to evaluate caffeine’s effects against adherent C. albicans using microplate reader, CFUs, and scanning electron microscope (SEM). Results: caffeine’s MIC was detected around 30 mg/mL, while the MFC was considered at 60 mg/mL. In an agar-well diffusion test, the inhibition zones were wider in caffeine groups. The Live/Dead viability test verified caffeine’s antifungal effects. The optical density of the adherent C. albicans on PMMA discs were lower at 620 nm or 410 nm in caffeine groups. CFU count was also reduced by caffeine treatments. SEM revealed the lower adherent C. albicans count in caffeine groups. The effect of caffeine was dose-dependent at which the 60 mg/mL dose demonstrated the most prominent effect. Conclusion: The study reinforced caffeine’s antifungal and antibiofilm properties and suggested it as an additive, or even an alternative, disinfectant solution for fungal biofilms on denture surfaces. Full article

(This article belongs to the Special Issue Innovations in Drug Resistance: A Commemorative Issue in Honor of Prof. Salvador Luria)

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