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“Molecular understanding of the possible mechanisms of oligosaccharide oxidation by cold plasma”. Yusupov M, Dewaele D, Attri P, Khalilov U, Sobott F, Bogaerts A, Plasma processes and polymers (2022). http://doi.org/10.1002/ppap.202200137
Abstract: Cold atmospheric plasma (CAP) is a promising technology for several medical applications, including the removal of biofilms from surfaces. However, the molecular mechanisms of CAP treatment are still poorly understood. Here we unravel the possible mechanisms of CAP‐induced oxidation of oligosaccharides, employing reactive molecular dynamics simulations based on the density functional‐tight binding potential. Specifically, we find that the interaction of oxygen atoms (used as CAP‐generated reactive species) with cellotriose (a model system for the oligosaccharides) can break structurally important glycosidic bonds, which subsequently leads to the disruption of the oligosaccharide molecule. The overall results help to shed light on our experimental evidence for cellotriose CAP. This oxidation by study provides atomic‐level insight into the onset of plasma‐induced removal of biofilms, as oligosaccharides are one of the main components of biofilm.
Keywords: A1 Journal article; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 3.5
DOI: 10.1002/ppap.202200137
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“Effect of plasma-induced oxidative stress on the glycolysis pathway of Escherichia coli”. Ranjbar S, Shahmansouri M, Attri P, Bogaerts A, Computers In Biology And Medicine 127, 104064 (2020). http://doi.org/10.1016/j.compbiomed.2020.104064
Abstract: Antibiotic resistance is one of the world’s most urgent public health problems. Due to its antibacterial properties, cold atmospheric plasma (CAP) may serve as an alternative method to antibiotics. It is claimed that oxidative stress caused by CAP is the main reason of bacteria inactivation. In this work, we computationally investigated the effect of plasma-induced oxidation on various glycolysis metabolites, by monitoring the production of the biomass. We observed that in addition to the significant reduction in biomass production, the rate of some reactions has increased. These reactions produce anti-oxidant products, showing the bacterial defense mechanism to escape the oxidative damage. Nevertheless, the simulations show that the plasma-induced oxidation effect is much stronger than the defense mechanism, causing killing of the bacteria.
Keywords: A1 Journal article; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 7.7
DOI: 10.1016/j.compbiomed.2020.104064
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“Influence of osmolytes and ionic liquids on the Bacteriorhodopsin structure in the absence and presence of oxidative stress: A combined experimental and computational study”. Attri P, Razzokov J, Yusupov M, Koga K, Shiratani M, Bogaerts A, International Journal Of Biological Macromolecules 148, 657 (2020). http://doi.org/10.1016/j.ijbiomac.2020.01.179
Abstract: Understanding the folding and stability of membrane proteins is of great importance in protein science. Recently, osmolytes and ionic liquids (ILs) are increasingly being used as drug delivery systems in the biopharmaceutical industry. However, the stability of membrane proteins in the presence of osmolytes and ILs is not yet fully understood. Besides, the effect of oxidative stress on membrane proteins with osmolytes or ILs has not been investigated. Therefore, we studied the influence of osmolytes and ILs as co-solvents on the stability of a model membrane protein (i.e., Bacteriorhodopsin in purple membrane of Halobacterium salinarum), using UV–Vis spectroscopy and molecular dynamics (MD) simulations. The MD simulations allowed us to determine the flexibility and solvent accessible surface area (SASA) of Bacteriorhodopsin protein in the presence and/or absence of cosolvents, as well as to carry out principal component analysis (PCA) to identify the most important movements in this protein. In addition, by means of UV–Vis spectroscopy we studied the effect of oxidative stress generated by cold atmospheric plasma on the stability of Bacteriorhodopsin in the presence and/or absence of co-solvents. This study is important for a better understanding of the stability of proteins in the presence of oxidative stress.
Keywords: A1 Journal article; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 8.2
DOI: 10.1016/j.ijbiomac.2020.01.179
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“Structural modification of NADPH oxidase activator (Noxa 1) by oxidative stress: An experimental and computational study”. Attri P, Park J-H, De Backer J, Kim M, Yun J-H, Heo Y, Dewilde S, Shiratani M, Choi EH, Lee W, Bogaerts A, International Journal Of Biological Macromolecules 163, 2405 (2020). http://doi.org/10.1016/j.ijbiomac.2020.09.120
Abstract: NADPH oxidases 1 (NOX1) derived reactive oxygen species (ROS) play an important role in the progression of cancer through signaling pathways. Therefore, in this paper, we demonstrate the effect of cold atmospheric plasma (CAP) on the structural changes of Noxa1 SH3 protein, one of the regulatory subunits of NOX1. For this purpose, firstly we purified the Noxa1 SH3 protein and analyzed the structure using X-ray crystallography, and subsequently, we treated the protein with two types of CAP reactors such as pulsed dielectric barrier discharge (DBD) and Soft Jet for different time intervals. The structural deformation of Noxa1 SH3 protein was analyzed by various experimental methods (circular dichroism, fluorescence, and NMR spectroscopy) and by MD simulations. Additionally, we demonstrate the effect of CAP (DBD and Soft Jet) on the viability and expression of NOX1 in A375 cancer cells. Our results are useful to understand the structural modification/oxidation occur in protein due to reactive oxygen and nitrogen (RONS) species generated by CAP.
Keywords: A1 Journal article; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 8.2
DOI: 10.1016/j.ijbiomac.2020.09.120
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“Plasma treatment causes structural modifications in lysozyme, and increases cytotoxicity towards cancer cells”. Attri P, Kaushik NK, Kaushik N, Hammerschmid D, Privat-Maldonado A, De Backer J, Shiratani M, Choi EH, Bogaerts A, International Journal Of Biological Macromolecules 182, 1724 (2021). http://doi.org/10.1016/j.ijbiomac.2021.05.146
Abstract: Bacterial and mammalian proteins, such as lysozyme, are gaining increasing interest as anticancer drugs. This study aims to modify the lysozyme structure using cold atmospheric plasma to boost its cancer cell killing effect. We investigated the structure at acidic and neutral pH using various experimental techniques (circular dichroism, fluorescence, and mass spectrometry) and molecular dynamics simulations. The controlled structural modification of lysozyme at neutral pH enhances its activity, while the activity was lost at acidic pH at the same treatment conditions. Indeed, a larger number of amino acids were oxidized at acidic pH after plasma treatment, which results in a greater distortion of the lysozyme structure, whereas only limited structural changes were observed in lysozyme after plasma treatment at neutral pH. We found that the plasma-treated lysozyme significantly induced apoptosis to the cancer cells. Our results reveal that plasma-treated lysozyme could have potential as a new cancer cell killing drug.
Keywords: A1 Journal Article; Lysozyme; Cold atmospheric plasma; Cancer cell death; Plasma, laser ablation and surface modeling Antwerp (PLASMANT) ;
Impact Factor: 3.671
DOI: 10.1016/j.ijbiomac.2021.05.146
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“CAP modifies the structure of a model protein from thermophilic bacteria: mechanisms of CAP-mediated inactivation”. Attri P, Han J, Choi S, Choi EH, Bogaerts A, Lee W, Scientific reports 8, 10218 (2018). http://doi.org/10.1038/s41598-018-28600-w
Abstract: Cold atmospheric plasma (CAP) has great potential for sterilization in the food industry, by deactivation of thermophilic bacteria, but the underlying mechanisms are largely unknown. Therefore, we investigate here whether CAP is able to denature/modify protein from thermophilic bacteria. We focus on MTH1880 (MTH) from Methanobacterium thermoautotrophicum as model protein, which we treated with dielectric barrier discharge (DBD) plasma operating in air for 10, 15 and 20 mins. We analysed the structural changes of MTH using circular dichroism, fluorescence and NMR spectroscopy, as well as the thermal and chemical denaturation, upon CAP treatment. Additionally, we performed molecular dynamics (MD) simulations to determine the stability, flexibility and solvent accessible surface area (SASA) of both the native and oxidised protein.
Keywords: A1 Journal article; Engineering sciences. Technology; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 4.259
Times cited: 6
DOI: 10.1038/s41598-018-28600-w
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“Bacterial inactivation by plasma treated water enhanced by reactive nitrogen species”. Shaw P, Kumar N, Kwak HS, Park JH, Uhm HS, Bogaerts A, Choi EH, Attri P, Scientific reports 8, 11268 (2018). http://doi.org/10.1038/s41598-018-29549-6
Abstract: There is a growing body of literature that recognizes the importance of plasma treated water (PTW)for inactivation of microorganism. However, very little attention has been paid to the role of reactive nitrogen species (RNS) in deactivation of bacteria. The aim of this study is to explore the role of RNS in bacterial killing, and to develop a plasma system with increased sterilization efficiency. To increase the concentration of reactive oxygen and nitrogen species (RONS) in solution, we have used vapor systems (DI water/HNO3 at different wt%) combined with plasma using N2 as working gas. The results show that the addition of the vapor system yields higher RONS contents. Furthermore, PTW produced by N2 + 0.5 wt% HNO3 vapor comprises a large amount of both RNS and ROS, while PTW created by N2 + H2O vapor consists of a large amount of ROS, but much less RNS. Interestingly, we observed more deactivation of E. Coli with PTW created by N2 + 0.5 wt% HNO3 vapor plasma as compared to PTW generated by the other plasma systems. This work provides new insight into the role of RNS along with ROS for deactivation of bacteria.
Keywords: A1 Journal article; Engineering sciences. Technology; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 4.259
Times cited: 17
DOI: 10.1038/s41598-018-29549-6
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“A comparative study for the inactivation of multidrug resistance bacteria using dielectric barrier discharge and nano-second pulsed plasma”. Hoon Park J, Kumar N, Hoon Park D, Yusupov M, Neyts EC, Verlackt CCW, Bogaerts A, Ho Kang M, Sup Uhm H, Ha Choi E, Attri P;, Scientific reports 5, 13849 (2015). http://doi.org/10.1038/srep13849
Abstract: Bacteria can be inactivated through various physical and chemical means, and these have always been the focus of extensive research. To further improve the methodology for these ends, two types of plasma systems were investigated: nano-second pulsed plasma (NPP) as liquid discharge plasma and an Argon gas-feeding dielectric barrier discharge (Ar-DBD) as a form of surface plasma. To understand the sterilizing action of these two different plasma sources, we performed experiments with Staphylococcus aureus (S. aureus) bacteria (wild type) and multidrug resistant bacteria (Penicillum-resistant, Methicillin-resistant and Gentamicin-resistant). We observed that both plasma sources can inactivate both the wild type and multidrug-resistant bacteria to a good extent. Moreover, we observed a change in the surface morphology, gene expression and β-lactamase activity. Furthermore, we used X-ray photoelectron spectroscopy to investigate the variation in functional groups (C-H/C-C, C-OH and C=O) of the peptidoglycan (PG) resulting from exposure to plasma species. To obtain atomic scale insight in the plasma-cell interactions and support our experimental observations, we have performed molecular dynamics simulations to study the effects of plasma species, such as OH, H2O2, O, O3, as well as O2 and H2O, on the dissociation/formation of above mentioned functional groups in PG.
Keywords: A1 Journal article; Engineering sciences. Technology; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 4.259
Times cited: 32
DOI: 10.1038/srep13849
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“Mechanism and comparison of needle-type non-thermal direct and indirect atmospheric pressure plasma jets on the degradation of dyes”. Attri P, Yusupov M, Park JH, Lingamdinne LP, Koduru JR, Shiratani M, Choi EH, Bogaerts A, Scientific reports 6, 34419 (2016). http://doi.org/10.1038/srep34419
Abstract: Purified water supply for human use, agriculture and industry is the major global priority nowadays. The advanced oxidation process based on atmospheric pressure non-thermal plasma (NTP) has been used for purification of wastewater, although the underlying mechanisms of degradation of organic pollutants are still unknown. In this study we employ two needle-type atmospheric pressure non-thermal plasma jets, i.e., indirect (ID-APPJ) and direct (D-APPJ) jets operating at Ar feed gas, for the treatment of methylene blue, methyl orange and congo red dyes, for two different times (i.e., 20 min and 30 min). Specifically, we study the decolorization/degradation of all three dyes using the above mentioned plasma sources, by means of UV-Vis spectroscopy, HPLC and a density meter. We also employ mass spectroscopy to verify whether only decolorization or also degradation takes place after treatment of the dyes by the NTP jets. Additionally, we analyze the interaction of OH radicals with all three dyes using reactive molecular dynamics simulations, based on the density functional-tight binding method. This investigation represents the first report on the degradation of these three different dyes by two types of NTP setups, analyzed by various methods, and based on both experimental and computational studies.
Keywords: A1 Journal article; Engineering sciences. Technology; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 4.259
Times cited: 23
DOI: 10.1038/srep34419
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“Enhancement of cellular glucose uptake by reactive species: a promising approach for diabetes therapy”. Kumar N, Shaw P, Razzokov J, Yusupov M, Attri P, Uhm HS, Choi EH, Bogaerts A, RSC advances 8, 9887 (2018). http://doi.org/10.1039/C7RA13389H
Abstract: It is generally known that antidiabetic activity is associated with an increased level of glucose uptake in adipocytes and skeletal muscle cells. However, the role of exogenous reactive oxygen and nitrogen species (RONS) in muscle development and more importantly in glucose uptake is largely unknown. We investigate the effect of RONS generated by cold atmospheric plasma (CAP) in glucose uptake. We show that the glucose uptake is significantly enhanced in differentiated L6 skeletal muscle cells after CAP treatment. We also observe a significant increase of the intracellular Ca++ and ROS level, without causing toxicity. One of the possible reasons for an elevated level of glucose uptake as well as intracellular ROS and Ca++ ions is probably the increased oxidative stress leading to glucose transport.
Keywords: A1 Journal article; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 3.108
Times cited: 1
DOI: 10.1039/C7RA13389H
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“The role of UV photolysis and molecular transport in the generation of reactive species in a tissue model with a cold atmospheric pressure plasma jet”. Ghimire B, Szili EJ, Lamichhane P, Short RD, Lim JS, Attri P, Masur K, Weltmann K-D, Hong S-H, Choi EH, Applied physics letters 114, 093701 (2019). http://doi.org/10.1063/1.5086522
Abstract: Cold atmospheric pressure plasma jets (plasma) operated in ambient air provide a rich source of reactive oxygen and nitrogen species (RONS), which are known to influence biological processes important in disease. In the plasma treatment of diseased tissue such as subcutaneous cancer tumors, plasma RONS need to first traverse an interface between the plasma-skin surface and second be transported to millimeter depths in order to reach deep-seated diseased cells. However, the mechanisms in the plasma generation of RONS within soft tissues are not understood. In this study, we track the plasma jet delivery of RONS into a tissue model target and we delineate two processes: through target delivery of RONS generated (primarily) in the plasma jet and in situ RONS generation by UV photolysis within the target. We demonstrate that UV photolysis promotes the rapid generation of RONS in the tissue model target’s surface after which the RONS are transported to millimeter depths via a slower molecular process. Our results imply that the flux of UV photons from plasma jets is important for delivering RONS through seemingly impenetrable barriers such as skin. The findings have implications not only in treatments of living tissues but also in the functionalization of soft hydrated biomaterials such as hydrogels and extracellular matrix derived tissue scaffolds.
Keywords: A1 Journal article; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 3.411
Times cited: 12
DOI: 10.1063/1.5086522
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“Inactivation of human pancreatic ductal adenocarcinoma with atmospheric plasma treated media and water: a comparative study”. Kumar N, Attri P, Dewilde S, Bogaerts A, Journal of physics: D: applied physics 51, 255401 (2018). http://doi.org/10.1088/1361-6463/aac571
Abstract: In recent years, the interest in treating cancer cells with plasma treated media (PTM) and plasma treated water (PTW) has increased tremendously. However, the actions of PTM and PTW are still not entirely understood. For instance, it is not clear whether the action of PTM is due to a modification in proteins/amino acids after plasma treatment of the media, or due to reactive oxygen and nitrogen species (RONS) generated from the plasma, or a combination of both effects. To differentiate between the actions of RONS and modified proteins/amino acids on the treatment of cancer cells, we compared the effects of PTM and PTW on two different pancreatic ductal adenocarcinomas (MiaPaca-2, BxPc3) and pancreatic stellate cells
(PSCs) (hPSC128-SV). PSCs closely interact with cancer cells to create a tumor-promoting environment that stimulates local tumor progression and metastasis. We treated culture media and deionized water with a cold atmospheric plasma (CAP) jet, and subsequently applied this PTM/PTW at various ratios to the pancreatic cancer and PSC cell lines. We evaluated cell death, intracellular ROS concentrations and the mRNA expression profiles of four oxidative stress-related genes, i.e. Mitogen-activated protein kinase 7 (MAPK7), B-cell lymphoma 2 (BCL2), Checkpoint kinase 1 (CHEK1) and DNA damage-inducible transcript 3, also known as C/EBP homologous protein (CHOP). Our findings demonstrate that PTM and PTW have a similar efficacy to kill pancreatic cancer cells, while PTW is slightly more effective in killing PSCs, as compared to PTM. Furthermore, we observed an enhancement of the intracellular ROS concentrations in both pancreatic cancer cells and PSCs. Thus, it is likely that under our experimental conditions, the anti-cancer activity of PTM can be attributed more to the RONS present in the treated liquid, than to the modification of proteins/amino acids in the media. Furthermore, the fact that the chemo-resistant PSCs were killed by PTM/PTW may offer possibilities for new anti-cancer therapies for pancreatic cancer cells, including PSCs.
Keywords: A1 Journal article; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 2.588
Times cited: 6
DOI: 10.1088/1361-6463/aac571
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“Cocktail of reactive species generated by cold atmospheric plasma: oral administration induces non-small cell lung cancer cell death”. Song C-H, Attri P, Ku S-K, Han I, Bogaerts A, Choi EH, Journal Of Physics D-Applied Physics 54, 185202 (2021). http://doi.org/10.1088/1361-6463/abdff2
Abstract: Non-small cell lung cancer (NSCLC) is the most common type of lung cancer, with 85% of all lung cancer reported as NSCLC. Moreover, there are no effective treatments in advanced NSCLC. This study shows for the first time that oral administration of plasma-treated water (PTW) can cure advanced NSCLC. The cold plasma in water generates a cocktail of reactive species, and oral administration of this cocktail to mice showed no toxicities even at the highest dose of PTW, after a single dose and repeated doses for 28 d in mice. In vivo studies reveal that PTW showed favorable anticancer effects on chemo-resistant lung cancer, similarly to gefitinib treatment as a reference drug in a chemo-resistant NSCLC model. The anticancer activities of PTW seem to be involved in inhibiting proliferation and angiogenesis and enhancing apoptosis in the cancer cells. Interestingly, the PTW contributes to enhanced immune response and improved cachexia in the model.
Keywords: A1 Journal article; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 2.588
DOI: 10.1088/1361-6463/abdff2
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“Perspectives of Plasma-treated Solutions as Anticancer Drugs”. Attri P, Bogaerts A, Anti-cancer agents in medicinal chemistry 19, 436 (2019). http://doi.org/10.2174/187152061904190521102345
Keywords: A1 Journal article; Pharmacology. Therapy; Plasma Lab for Applications in Sustainability and Medicine – Antwerp (PLASMANT)
Impact Factor: 2.598
Times cited: 2
DOI: 10.2174/187152061904190521102345
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“Unraveling the Transport Properties of RONS across Nitro-Oxidized Membranes”. Abduvokhidov D, Yusupov M, Shahzad A, Attri P, Shiratani M, Oliveira MC, Razzokov J, Biomolecules 13, 1043 (2023). http://doi.org/10.3390/biom13071043
Abstract: The potential of cold atmospheric plasma (CAP) in biomedical applications has received significant interest, due to its ability to generate reactive oxygen and nitrogen species (RONS). Upon exposure to living cells, CAP triggers alterations in various cellular components, such as the cell membrane. However, the permeation of RONS across nitrated and oxidized membranes remains understudied. To address this gap, we conducted molecular dynamics simulations, to investigate the permeation capabilities of RONS across modified cell membranes. This computational study investigated the translocation processes of less hydrophilic and hydrophilic RONS across the phospholipid bilayer (PLB), with various degrees of oxidation and nitration, and elucidated the impact of RONS on PLB permeability. The simulation results showed that less hydrophilic species, i.e., NO, NO2, N2O4, and O3, have a higher penetration ability through nitro-oxidized PLB compared to hydrophilic RONS, i.e., HNO3, s-cis-HONO, s-trans-HONO, H2O2, HO2, and OH. In particular, nitro-oxidation of PLB, induced by, e.g., cold atmospheric plasma, has minimal impact on the penetration of free energy barriers of less hydrophilic species, while it lowers these barriers for hydrophilic RONS, thereby enhancing their translocation across nitro-oxidized PLB. This research contributes to a better understanding of the translocation abilities of RONS in the field of plasma biomedical applications and highlights the need for further analysis of their role in intracellular signaling pathways.
Keywords: A1 Journal Article; Plasma, laser ablation and surface modeling Antwerp (PLASMANT) ;
DOI: 10.3390/biom13071043
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