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Molecular Aspects of Photodynamic Therapy

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Pathology, Diagnostics, and Therapeutics".

Deadline for manuscript submissions: closed (20 February 2025) | Viewed by 21639

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Special Issue Editors

Dr. Marina G. Strakhovskaya

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Guest Editor

Faculty of Biology, Lomonosov Moscow State University, 119234 Moscow, Russia
Interests: molecular targets for photosensitization; reactive oxygen species; photodynamic inactivation of bacteria and viruses

Dr. Gennady A. Meerovich

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Co-Guest Editor

Prokhorov General Physics Institute of the Russian Academy of Sciences, National Research Nuclear University Moscow Engineering Physics Institute, 115409 Moscow, Russia
Interests: photodynamic therapy

Special Issue Information

Dear Colleagues,

Intensive research on photodynamic therapy (PDT), originally based on empirical phototherapy, in which photoactive plant metabolites were used to enhance the action of sunlight, led to the discovery of the scientific foundations of photodynamic reactions, the creation of artificial light sources and several generations of photosensitizers, and their practical application. The basic PDT process includes the photosensitized generation of reactive oxygen species (ROS) aimed at combating life-threatening neoplasms and pathogens. The main advantages of PDT are its non-invasiveness, selectivity of action and efficiency in relation to objects resistant to traditional chemotherapy. This becomes possible due to local lesion irradiation, the selective accumulation of a photosensitizer in or near the ROS-sensitive structures and the extremely short ROS lifetimes. This Special Issue is focused on studies of ROS-sensitive targets in eukaryotic cells, bacteria and viruses, photosensitizer delivery carriers, studies on the interactions of photosensitizers with cytoplasmic membranes and intracellular structures of cancer and cancer stem cells, endotheliocytes of cancer vessels, bacterial cells and matrices of biofilms, structures of virus envelopes and genetic apparatus. Along with experimental research, studies on the use of molecular modeling and information technologies are welcome.

Dr. Marina G. Strakhovskaya
Dr. Gennady A. Meerovich
Guest Editors

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Keywords

photosensitizer
reactive oxygen species
sensitive targets
anticancer photodynamic therapy (PDT)
antimicrobial PDT
delivery carriers
molecular modeling

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Published Papers (11 papers)

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24 pages, 4201 KiB

Open AccessArticle

Can α-Mangostin and Photodynamic Therapy Support Ciprofloxacin in the Inactivation of Uropathogenic Escherichia coli and Staphylococcus aureus Strains?

by Dorota Wojnicz, Kamila Korzekwa, Mateusz Guźniczak, Maciej Wernecki, Agnieszka Ulatowska-Jarża, Igor Buzalewicz and Dorota Tichaczek-Goska

Int. J. Mol. Sci. 2025, 26(1), 76; https://doi.org/10.3390/ijms26010076 - 25 Dec 2024

Viewed by 887

Abstract

Multidrug-resistant bacteria represent a significant challenge in the treatment of bacterial infections, often leading to therapeutic failures. This issue underlines the need to develop strategies that improve the efficacy of conventional antibiotic therapies. In this study, we aimed to assess whether a plant-derived compound, α-mangostin, and photodynamic therapy (PDT) could enhance the antibacterial activity of ciprofloxacin against uropathogenic strains of Escherichia coli and Staphylococcus aureus. Using nanopore sequencing technology, we confirmed that the clinical strains tested were classified as multidrug-resistant. Digital holotomography (DHT) was used to examine α-mangostin-induced changes in the bacterial cells’ penetration by a photosensitizer. A scanning confocal fluorescence microscope was used to visualize photosensitizer penetration into bacterial cells and validate DHT results. A synergistic effect between α-mangostin and ciprofloxacin was observed exclusively in S. aureus strains, while no enhancement of ciprofloxacin’s antibacterial activity was detected in E. coli strains when combined with α-mangostin. Notably, photodynamic therapy significantly potentiated the antibacterial effects of ciprofloxacin and its combination with α-mangostin compared to untreated controls. In addition, morphological changes were observed in bacterial cells exposed to these antimicrobials. In conclusion, our findings suggest that α-mangostin and PDT may serve as valuable adjuncts to ciprofloxacin, improving the eradication of uropathogens. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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24 pages, 6303 KiB

Open AccessArticle

Optimization of the Treatment of Squamous Cell Carcinoma Cells by Combining Photodynamic Therapy with Cold Atmospheric Plasma

by Sigrid Karrer, Petra Unger, Nina Spindler, Rolf-Markus Szeimies, Anja Katrin Bosserhoff, Mark Berneburg and Stephanie Arndt

Int. J. Mol. Sci. 2024, 25(19), 10808; https://doi.org/10.3390/ijms251910808 - 8 Oct 2024

Viewed by 1506

Abstract

Actinic keratosis (AK) is characterized by a reddish or occasionally skin-toned rough patch on sun-damaged skin, and it is regarded as a precursor to squamous cell carcinoma (SCC). Photodynamic therapy (PDT), utilizing 5-aminolevulinic acid (ALA) along with red light, is a recognized treatment option for AK that is limited by the penetration depth of light and the distribution of the photosensitizer into the skin. Cold atmospheric plasma (CAP) is a partially ionized gas with permeability-enhancing and anti-cancer properties. This study analyzed, in vitro, whether a combined treatment of CAP and ALA-PDT may improve the efficacy of the treatment. In addition, the effect of the application sequence of ALA and CAP was investigated using in vitro assays and the molecular characterization of human oral SCC cell lines (SCC-9, SCC-15, SCC-111), human cutaneous SCC cell lines (SCL-1, SCL-2, A431), and normal human epidermal keratinocytes (HEKn). The anti-tumor effect was determined by migration, invasion, and apoptosis assays and supported the improved efficacy of ALA-PDT in combination with CAP. However, the application sequence ALA-CAP–red light seems to be more efficacious than CAP-ALA–red light, which is probably due to increased intracellular ROS levels when ALA is applied first, followed by CAP and red light treatment. Furthermore, the expression of apoptosis- and senescence-related molecules (caspase-3, -6, -9, p16^INK4a, p21^CIP1) was increased, and different genes of the junctional network (ZO-1, CX31, CLDN1, CTNNB1) were induced after the combined treatment of CAP plus ALA-PDT. HEKn, however, were much less affected than SCC cells. Overall, the results show that CAP may improve the anti-tumor effects of conventional ALA-PDT on SCC cells. Whether this combined application is successful in treating AK in vivo has to be carefully examined in follow-up studies. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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11 pages, 4267 KiB

Open AccessArticle

Enhancing Lung Recellularization with Mesenchymal Stem Cells via Photobiomodulation Therapy: Insights into Cytokine Modulation and Sterilization

by Leticia L. Guimarães, Auriléia A. Brito, Andressa D. Cereta, Ana Paula L. Oliveira, João Pedro R. Afonso, Diego A. C. P. G. Mello, Iransé Oliveira-Silva, Carlos H. M. Silva, Rodrigo F. Oliveira, Deise A. A. P. Oliveira, Rodolfo de Paula Vieira, Dante Brasil Santos, Giuseppe Insalaco, Luís V. F. Oliveira and Renata Kelly da Palma

Int. J. Mol. Sci. 2024, 25(18), 10131; https://doi.org/10.3390/ijms251810131 - 20 Sep 2024

Viewed by 1408

Abstract

Several lung diseases can cause structural damage, making lung transplantation the only therapeutic option for advanced disease stages. However, the transplantation success rate remains limited. Lung bioengineering using the natural extracellular matrix (ECM) of decellularized lungs is a potential alternative. The use of undifferentiated cells to seed the ECM is practical; however, sterilizing the organ for recellularization is challenging. Photobiomodulation therapy (PBMT) may offer a solution, in which the wavelength is crucial for tissue penetration. This study aimed to explore the potential of optimizing lung recellularization with mesenchymal stem cells using PBMT (660 nm) after sterilization with PBMT (880 nm). The lungs from C57BL/6 mice were decellularized using 1% SDS and sterilized using PBMT (880 nm, 100 mW, 30 s). Recellularization was performed in two groups: (1) recellularized lung and (2) recellularized lung + 660 nm PBMT (660 nm, 100 mW, 30 s). Both were seeded with mesenchymal stem cells from human tooth pulp (DPSc) and incubated for 24 h at 37 °C and 5% CO₂ in bioreactor-like conditions with continuous positive airway pressure (CPAP) at 20 cmH₂O and 90% O₂. The culture medium was analyzed after 24 h. H&E, immunostaining, SEM, and ELISA assays were performed. Viable biological scaffolds were produced, which were free of cell DNA and preserved the glycosaminoglycans; collagens I, III, and IV; fibronectin; laminin; elastin; and the lung structure (SEM). The IL-6 and IL-8 levels were stable during the 24 h culture, but the IFN-γ levels showed significant differences in the recellularized lung and recellularized lung + 660 nm PBMT groups. Greater immunological modulation was observed in the recellularized groups regarding pro-inflammatory cytokines (IL-6, IFN-γ, and IL-8). These findings suggest that PBMT plays a role in cytokine regulation and antimicrobial activity, thus offering promise for enhanced therapeutic strategies in lung bioengineering. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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15 pages, 3316 KiB

Open AccessArticle

In Vitro Effect of Epigallocatechin Gallate on Heme Synthesis Pathway and Protoporphyrin IX Production

by Daniela León, María Elena Reyes, Helga Weber, Álvaro Gutiérrez, Claudio Tapia, Ramón Silva, Tamara Viscarra, Kurt Buchegger, Carmen Ili and Priscilla Brebi

Int. J. Mol. Sci. 2024, 25(16), 8683; https://doi.org/10.3390/ijms25168683 - 9 Aug 2024

Cited by 1 | Viewed by 1418

Abstract

Photodynamic therapy (PDT) treats nonmelanoma skin cancer. PDT kills cells through reactive oxygen species (ROS), generated by interaction among cellular O_2, photosensitizer and specific light. Protoporphyrin IX (PpIX) is a photosensitizer produced from methyl aminolevulinate (MAL) by heme group synthesis (HGS) pathway. In PDT-resistant cells, PDT efficacy has been improved by addition of epigallocatechin gallate (EGCG). Therefore, the aim of this work is to evaluate the effect of EGCG properties over MAL-TFD and PpIX production on A-431 cell line. EGCG’s role over cell proliferation (flow cytometry and wound healing assay) and clonogenic capability (clonogenic assay) was evaluated in A-431 cell line, while the effect of EGCG over MAL-PDT was determined by cell viability assay (MTT), PpIX and ROS detection (flow cytometry), intracellular iron quantification and gene expression of HGS enzymes (RT-qPCR). Low concentrations of EGCG (<50 µM) did not have an antiproliferative effect over A-431 cells; however, EGCG inhibited clonogenic cell capability. Furthermore, EGCG (<50 µM) improved MAL-PDT cytotoxicity, increasing PpIX and ROS levels, exerting a positive influence on PpIX synthesis, decreasing intracellular iron concentration and modifying HGS enzyme gene expression such as PGB (upregulated) and FECH (downregulated). EGCG inhibits clonogenic capability and modulates PpIX synthesis, enhancing PDT efficacy in resistant cells. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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15 pages, 3281 KiB

Open AccessArticle

The Multifaceted Actions of PVP–Curcumin for Treating Infections

by Magdalena Metzger, Stefan Manhartseder, Leonie Krausgruber, Lea Scholze, David Fuchs, Carina Wagner, Michaela Stainer, Johannes Grillari, Andreas Kubin, Lionel Wightman and Peter Dungel

Int. J. Mol. Sci. 2024, 25(11), 6140; https://doi.org/10.3390/ijms25116140 - 2 Jun 2024

Viewed by 1090

Abstract

Curcumin is a natural compound that is considered safe and may have potential health benefits; however, its poor stability and water insolubility limit its therapeutic applications. Different strategies aim to increase its water solubility. Here, we tested the compound PVP–curcumin as a photosensitizer for antimicrobial photodynamic therapy (aPDT) as well as its potential to act as an adjuvant in antibiotic drug therapy. Gram-negative E. coli K12 and Gram-positive S. capitis were subjected to aPDT using various PVP–curcumin concentrations (1–200 µg/mL) and 475 nm blue light (7.5–45 J/cm²). Additionally, results were compared to aPDT using 415 nm blue light. Gene expression of recA and umuC were analyzed via RT-qPCR to assess effects on the bacterial SOS response. Further, the potentiation of Ciprofloxacin by PVP–curcumin was investigated, as well as its potential to prevent the emergence of antibiotic resistance. Both bacterial strains were efficiently reduced when irradiated with 415 nm blue light (2.2 J/cm²) and 10 µg/mL curcumin. Using 475 nm blue light, bacterial reduction followed a biphasic effect with higher efficacy in S. capitis compared to E. coli K12. PVP–curcumin decreased recA expression but had limited effect regarding enhancing antibiotic treatment or impeding resistance development. PVP–curcumin demonstrated effectiveness as a photosensitizer against both Gram-positive and Gram-negative bacteria but did not modulate the bacterial SOS response. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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12 pages, 4474 KiB

Open AccessArticle

Tumor-Targeted Squaraine Dye for Near-Infrared Fluorescence-Guided Photodynamic Therapy

by Yoonbin Park, Min Ho Park and Hoon Hyun

Int. J. Mol. Sci. 2024, 25(6), 3428; https://doi.org/10.3390/ijms25063428 - 18 Mar 2024

Viewed by 1897

Abstract

Many efforts have been made to develop near-infrared (NIR) fluorescent dyes with high efficiency for the NIR laser-induced phototherapy of cancer. However, the low tumor targetability and high nonspecific tissue uptake of NIR dyes in vivo limit their applications in preclinical cancer imaging and therapy. Among the various NIR dyes, squaraine (SQ) dyes are widely used due to their high molar extinction coefficient, intense fluorescence, and excellent photostability. Previously, benzoindole-derived SQ (BSQ) was prepared by incorporating carboxypentyl benzoindolium end groups into a classical SQ backbone, followed by conjugating with cyclic RGD peptides for tumor-targeted imaging. In this study, we demonstrate that the structure-inherent tumor-targeting BSQ not only shows a high fluorescence quantum yield in serum but also exhibits superior reactive oxygen species (ROS) generation capability under the 671 nm laser irradiation for effective photodynamic therapy (PDT) in vitro and in vivo. Without targeting ligands, the BSQ was preferentially accumulated in tumor tissue 24 h post-injection, which was the optimal timing of the laser irradiation to induce increments of ROS production. Therefore, this work provides a promising strategy for the development of photodynamic therapeutic SQ dyes for targeted cancer therapy. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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18 pages, 2909 KiB

Open AccessArticle

Thiophene Stability in Photodynamic Therapy: A Mathematical Model Approach

by Jackson J. Alcázar

Int. J. Mol. Sci. 2024, 25(5), 2528; https://doi.org/10.3390/ijms25052528 - 21 Feb 2024

Viewed by 2200

Abstract

Thiophene-containing photosensitizers are gaining recognition for their role in photodynamic therapy (PDT). However, the inherent reactivity of the thiophene moiety toward singlet oxygen threatens the stability and efficiency of these photosensitizers. This study presents a novel mathematical model capable of predicting the reactivity of thiophene toward singlet oxygen in PDT, using Conceptual Density Functional Theory (CDFT) and genetic programming. The research combines advanced computational methods, including various DFT techniques and symbolic regression, and is validated with experimental data. The findings underscore the capacity of the model to classify photosensitizers based on their photodynamic efficiency and safety, particularly noting that photosensitizers with a constant rate 1000 times lower than that of unmodified thiophene retain their photodynamic performance without substantial singlet oxygen quenching. Additionally, the research offers insights into the impact of electronic effects on thiophene reactivity. Finally, this study significantly advances thiophene-based photosensitizer design, paving the way for therapeutic agents that achieve a desirable balance between efficiency and safety in PDT. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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12 pages, 2264 KiB

Open AccessArticle

Interaction of Methylene Blue with Severe Acute Respiratory Syndrome Coronavirus 2 Envelope Revealed by Molecular Modeling

by Ilya Kovalenko, Ekaterina Kholina, Vladimir Fedorov, Sergei Khruschev, Ekaterina Vasyuchenko, Gennady Meerovich and Marina Strakhovskaya

Int. J. Mol. Sci. 2023, 24(21), 15909; https://doi.org/10.3390/ijms242115909 - 2 Nov 2023

Viewed by 2977

Abstract

Methylene blue has multiple antiviral properties against Severe Acute Respiratory Syndrome-related Coronavirus 2 (SARS-CoV-2). The ability of methylene blue to inhibit different stages of the virus life cycle, both in light-independent and photodynamic processes, is used in clinical practice. At the same time, the molecular aspects of the interactions of methylene blue with molecular components of coronaviruses are not fully understood. Here, we use Brownian dynamics to identify methylene blue binding sites on the SARS-CoV-2 envelope. The local lipid and protein composition of the coronavirus envelope plays a crucial role in the binding of this cationic dye. Viral structures targeted by methylene blue include the S and E proteins and negatively charged lipids. We compare the obtained results with known experimental data on the antiviral effects of methylene blue to elucidate the molecular basis of its activity against coronaviruses. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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16 pages, 4008 KiB

Open AccessArticle

Optical Differentiation of Brain Tumors Based on Raman Spectroscopy and Cluster Analysis Methods

by Anuar Ospanov, Igor Romanishkin, Tatiana Savelieva, Alexandra Kosyrkova, Svetlana Shugai, Sergey Goryaynov, Galina Pavlova, Igor Pronin and Victor Loschenov

Int. J. Mol. Sci. 2023, 24(19), 14432; https://doi.org/10.3390/ijms241914432 - 22 Sep 2023

Cited by 8 | Viewed by 1739

Abstract

In the present study, various combinations of dimensionality reduction methods with data clustering methods for the analysis of biopsy samples of intracranial tumors were investigated. Fresh biopsies of intracranial tumors were studied in the Laboratory of Neurosurgical Anatomy and Preservation of Biological Materials of N.N. Burdenko Neurosurgery Medical Center no later than 4 h after surgery. The spectra of Protoporphyrin IX (Pp IX) fluorescence, diffuse reflectance (DR) and Raman scattering (RS) of biopsy samples were recorded. Diffuse reflectance studies were carried out using a white light source in the visible region. Raman scattering spectra were obtained using a 785 nm laser. Patients diagnosed with meningioma, glioblastoma, oligodendroglioma, and astrocytoma were studied. We used the cluster analysis method to detect natural clusters in the data sample presented in the feature space formed based on the spectrum analysis. For data analysis, four clustering algorithms with eight dimensionality reduction algorithms were considered. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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21 pages, 8372 KiB

Open AccessArticle

The Effect of Antimicrobial Photodynamic Inactivation on the Protein Profile of Dormant Mycolicibacterium smegmatis Containing Endogenous Porphyrins

by Denis M. Shashin, Galina R. Demina, Irina A. Linge, Galina N. Vostroknutova, Arseny S. Kaprelyants, Alexander P. Savitsky and Margarita O. Shleeva

Int. J. Mol. Sci. 2023, 24(18), 13968; https://doi.org/10.3390/ijms241813968 - 12 Sep 2023

Cited by 3 | Viewed by 1758

Abstract

During transition into a dormant state, Mycolicibacterium (Mycobacterium) smegmatis cells are able to accumulate free porphyrins that makes them sensitive to photodynamic inactivation (PDI). The formation of dormant cells in a liquid medium with an increased concentration of magnesium (up to 25 mM) and zinc (up to 62 µM) resulted in an increase in the total amount of endogenous porphyrins in dormant M. smegmatis cells and their photosensitivity, especially for bacteria phagocytosed by macrophages. To gain insight into possible targets for PDI in bacterial dormant mycobacterial cells, a proteomic profiling with SDS gel electrophoresis and mass spectrometry analysis were conducted. Illumination of dormant forms of M. smegmatis resulted in the disappearance of proteins in the separating SDS gel. Dormant cells obtained under an elevated concentration of metal ions were more sensitive to PDI. Differential analysis of proteins with their identification with MALDI-TOF revealed that 45.2% and 63.9% of individual proteins disappeared from the separating gel after illumination for 5 and 15 min, respectively. Light-sensitive proteins include enzymes belonging to the glycolytic pathway, TCA cycle, pentose phosphate pathway, oxidative phosphorylation and energy production. Several proteins involved in protecting against oxygen stress and protein aggregation were found to be sensitive to light. This makes dormant cells highly vulnerable to harmful factors during a long stay in a non-replicative state. PDI caused inhibition of the respiratory chain activity and destroyed enzymes involved in the synthesis of proteins and nucleic acids, the processes which are necessary for dormant cell reactivation and their transition to multiplying bacteria. Because of such multiple targeting, PDI action via endogenous porphyrins could be considered as an effective approach for killing dormant bacteria and a perspective to inactivate dormant mycobacteria and combat the latent form of mycobacteriosis, first of all, with surface localization. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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Review

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21 pages, 7228 KiB

Open AccessReview

Efficacy of Green Synthesized Nanoparticles in Photodynamic Therapy: A Therapeutic Approach

by Mehak Zahra, Alexander Chota, Heidi Abrahamse and Blassan P. George

Int. J. Mol. Sci. 2023, 24(13), 10931; https://doi.org/10.3390/ijms241310931 - 30 Jun 2023

Cited by 20 | Viewed by 3348

Abstract

Cancer is a complex and diverse disease characterized by the uncontrolled growth of abnormal cells in the body. It poses a significant global public health challenge and remains a leading cause of death. The rise in cancer cases and deaths is a significant worry, emphasizing the immediate need for increased awareness, prevention, and treatment measures. Photodynamic therapy (PDT) has emerged as a potential treatment for various types of cancer, including skin, lung, bladder, and oesophageal cancer. A key advantage of PDT is its ability to selectively target cancer cells while sparing normal cells. This is achieved by preferentially accumulating photosensitizing agents (PS) in cancer cells and precisely directing light activation to the tumour site. Consequently, PDT reduces the risk of harming surrounding healthy cells, which is a common drawback of conventional therapies such as chemotherapy and radiation therapy. The use of medicinal plants for therapeutic purposes has a long history dating back thousands of years and continues to be an integral part of healthcare in many cultures worldwide. Plant extracts and phytochemicals have demonstrated the ability to enhance the effectiveness of PDT by increasing the production of reactive oxygen species (ROS) and promoting apoptosis (cell death) in cancer cells. This natural approach capitalizes on the eco-friendly nature of plant-based photoactive compounds, offering valuable insights for future research. Nanotechnology has also played a pivotal role in medical advancements, particularly in the development of targeted drug delivery systems. Therefore, this review explores the potential of utilizing photosensitizing phytochemicals derived from medicinal plants as a viable source for PDT in the treatment of cancer. The integration of green photodynamic therapy with plant-based compounds holds promise for novel treatment alternatives for various chronic illnesses. By harnessing the scientific potential of plant-based compounds for PDT, we can pave the way for innovative and sustainable treatment strategies. Full article

(This article belongs to the Special Issue Molecular Aspects of Photodynamic Therapy)

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