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Article

Modeling Study of OH Radical-Dominated H-Abstraction Reaction for Understanding Nucleotides Oxidation Induced by Cold Atmospheric Plasmas

by
Yu-Xuan Jiang
1,
Yang Chen
2 and
Yuan-Tao Zhang
2,*
1
Department of Electrical and Electronic Engineering, University of Nottingham Ningbo China, Ningbo 315100, China
2
School of Electrical Engineering, Shandong University, Jinan 250061, China
*
Author to whom correspondence should be addressed.
Plasma 2024, 7(2), 498-509; https://doi.org/10.3390/plasma7020026
Submission received: 30 April 2024 / Revised: 10 June 2024 / Accepted: 12 June 2024 / Published: 19 June 2024
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Abstract

:
In recent years, plasma medicine, as an innovative and rapidly growing field, has garnered increasing attention. Nonetheless, the fundamental mechanisms of the interaction processes of cold atmospheric plasma (CAP) and biomolecules remain under investigation. In this paper, a reactive molecular dynamic (MD) simulation with ReaxFF potential was performed to explore the interactions of reactive oxygen species (ROS) produced in CAP, exemplified by OH radicals, and four distinct oligonucleotides. The breakage of single-stranded oligonucleotides induced by OH is observed in the simulation, which could seriously influence the biological activity of cellular DNA. The base release induced by OH radicals means the loss of base sequence information, and the H-abstraction at nucleobases affects the gene strand complementarity, gene transcription, and replication. In addition, the dose effects of OH radicals on bond formation and breaking of oligonucleotides are also discussed by adjusting the number of ROS in the simulation box. This study can enhance the comprehension of interactions between CAP and DNA, thereby indicating possible improvements in plasma device optimization and operation for medical applications.

1. Introduction

Plasma medicine is a rapidly growing and new, largely unexplored multi-disciplinary scientific field of medical treatment [1], such as antimicrobial and surface sterilization, wound healing, cancer treatment, and dentistry, which has been the focus of attention in recent decades. CAP therapy has emerged as a novel technique for cancer treatment, offering numerous advantages over conventional therapies [2,3]. Numerous in vitro and in vivo studies have reported the selectivity of CAP towards tumor cells, highlighting its potential as both an adjunct therapy and a successful approach for tumor cell elimination [3]. The FDA’s approval of the first clinical trial utilizing CAP for cancer therapy in 2019 further underscores its significance in this field. Some medical plasma devices have been used for clinical applications. For instance, the driven HF plasma jet k I N P e n ® MED has received CE certification as a medical device class IIa for the treatment of skin diseases as well as chronic wounds [4,5].
However, a fundamental and detailed understanding of the interaction mechanisms of CAP and biological structures remains crucial for the advancement of plasma medicine [6,7,8]. According to numerous results from experimental observations in vitro, the biological effects of plasma are mainly based on ROS and RNS [9]. ROS (such as OH radical als, H 2 O 2 , O, and O 3 ) could interact with organic molecules in the cell, and RNS (such as NO, N O 2 , and O N O O − )are usually second messengers [10]. Many experiments have been carried out to explore the multiple relationships between ROS and the therapeutic effect treated by CAP [11,12,13,14], which enables the explanation of specific biological effects of CAP by considering redox biology. When RONS particles exceed physiological levels within organisms, oxidative stress ensues, potentially leading to severe outcomes. ROS have been shown to interact with various macromolecules, exerting profound effects on cells, including the oxidation of cell membranes, proteins, and DNA during the sterilization process of CAP [15,16,17]. Furthermore, ROS function as pivotal intracellular signal regulators, modulating numerous cellular signaling pathways through diverse mechanisms instrumental in cell transformation, inflammatory responses, tumor proliferation, and metastasis [18,19]. However, it remains elusive the exact interaction mechanism among reactive species and biomolecules. Computer simulation may deliver a robust solution for this problem by providing fundamental and elaborate information. It may be difficult or impossible to obtain by experimental methods [20,21,22,23]. At present, many modeling techniques have been developed for the study of plasma medicine, such as quantum mechanical (QM) calculations, density functional tight binding (DFTB) method, molecular dynamic (MD) simulation, and reactive MD simulation [24,25,26,27,28]. Reactive MD simulation is the most commonly used method in plasma medicine and has the advantage of describing the breaking and formation of chemical bonds, and recently, the machine learning technology is also introduced to the reactive MD simulation for efficiently understanding the bond reactions [29]. Compared to QM calculations, it can handle much larger systems and much longer time scales [17,30,31,32,33].
From the foregoing discussion, we try to study the interaction of plasma species with nucleotides utilizing the reactive MD simulation method. The results of this analysis summarize the reactions of particles to four distinct types of nucleotides and delve into the mechanisms that underlie the DNA strand damage induced by reactive particles at varying concentrations. On the one hand, the influence could effectively avoid caused by other factors (such as hydrogen bond, and the interaction of different nucleotides). On the other hand, the reaction mechanism discussed in this paper could lay a solid foundation for the interaction between OH radicals and DNA macromolecules. According to previous research, as the chosen reactive particles in our work, OH radicals are the most reactive toward nucleotides [34]. In Section 2, the constituent structure of nucleotides, the computational setup, and the preparatory work are detailed. Section 3 delves into the interaction mechanisms between the particles and strand nucleotides, as well as the dose effects revealed through simulations. Finally, Section 4 summarizes the conclusion of this study.

2. Simulation Setup

2.1. Molecular Structure of the Nucleotide

It is crucial for understanding specific reaction processes to have a basic appreciation of the individual components of a nucleotide. As shown in Figure 1, the nucleotide comprises heterocyclic aromatic nucleobases, sugar moiety (also called 2-deoxyribose), and phosphate groups. There are four kinds of nucleobases in nucleotides: pyrimidines thymine (Thy) and cytosine (Cyt); and the purines guanine (Gua) and adenine (Ade). Ade has an amino group ( − N H 2 ) on the C 6 position; guanine has the C 2 amino group position and C 6 carbonyl group; thymine contains a methyl group at the C 5 site, a key site for H-abstraction reaction, with carbonyl groups at the C 4 and C 2 positions; cytosine contains C 2 carbonyl groupand C 4 the amino group. 2-Deoxyribose is a five-carbon sugar, where carbon atoms are numbered with primes (such as C2′) to avoid confusion. C1′ and C4′ are joined into a five-member ring through an ether bond. The sugar moiety and phosphate groups, joined by a 3′-5′ phosphodiester bond, are on the outside of the helix and form a “backbone” for the helix. In this simulation, an oligonucleotide composed of the same three nucleosides is constructed to investigate the individual interaction mechanism of OH radicals with each kind of nucleotide.

2.2. Generation of CAP and Reactive Species

The origin of plasma technology can be traced back to early 1879, when William Crookes applied high voltage to an ionized gas known as radiant gas. Then, to describe a fluid that is electrified and includes ions and electrons, Irvin Langmuir introduced the term “plasma” in 1927 [35,36]. As living organisms are commonly situated in atmospheric pressure environments and exhibit significant sensitivity to temperature variations, cold atmospheric plasma (CAP) is the foundation for most plasma applications in medicine, with plenty of ROS and RNS and very frequent collisions at atmospheric pressure [37]. CAP demonstrates the capability to interact directly with biological tissues, while its generated thermal effects neither inflict damage upon human or other biological tissues nor contaminate the proximate environment. These advantageous characteristics have facilitated the increasing application of CAP in the biomedical field. The plasma configurations in plasma medicine commonly use atmospheric air as working gas [38]. In this context, the non-equilibrium atmospheric plasmas can provide high densities of ROS, mainly including ground state atomic oxygen, excited atomic oxygen, ozone, and single delta oxygen (SDO), due to multiple collisions. They are very essential for many biomedical applications, such as dermatology, cancer treatment, and wound healing. Extensive research suggests that the concentrations of desired active particles are influenced by factors such as the power supply, electrode structure, discharge mode, and modulation frequency [39]. For instance, in radio frequency discharge, an optimal oxygen admixture of approximately 0.6% leads to the achievement of the highest density of ground-state atomic oxygen [37]. Furthermore, according to [40], the densities of ROS can be effectively increased by augmenting the input power density and broadening the oxygen admixture range in atmospheric radio frequency helium-oxygen discharges operating at a relatively higher frequency.

2.3. Simulation Details

At first, a specific selected oligonucleotide undergoes geometry and dynamic optimization to ensure the stability of the molecular system. This optimization process is performed within the COMPASS II field at room temperature (i.e., 300 K). Subsequently, the optimized oligonucleotide structure and OH radicals are randomly positioned in a box measuring 20 Å × 20 Å × 20 Å, and the periodic boundary conditions are applied. Figure 2 depicts an example of 15 OH radicals and a single-stranded oligonucleotide enclosed within an amorphous cell. Variations in OH radical concentration are achieved by adjusting the number (5, 10, 15, 20) of OH radicals in the fixed-size box. Following a 50 ps equilibration period, reactive MD simulations using ReaxFF potential at 310 K within an NVT (constant number of atoms, volume, and temperature) ensemble. Every simulation lasts for 200 ps with a time step length of 0.1 fs. Typically, ten runs are performed for each type of single-stranded oligonucleotide in the specific OH radicals concentration to investigate all potential reaction pathways and obtain statistically valid results. Thus, the ReaxFF potential allows for the dynamic and computationally efficient investigation of relatively large systems [34,41].

3. Results and Discussion

3.1. The Impact of OH Radicals on Nucleosides

Generally speaking, the interaction between OH radicals and organic molecules are three types of reactions: radical adduct formation (RAF), H-abstraction (HA), and single electron transfer (SET). From previous research, OH radicals mainly react with nucleobases by H-abstraction or through addition to C—C and C—N double bonds. The type and extent of reactions vary depending on the molecular structure and reactivity of different nucleobases. According to previous studies, RAF, with higher rate constants, is the general interaction route preferred interaction between OH radicals and nucleobases [42,43,44]. OH radicals can regioselectively add to the C 4 and C 8 atom of purine and to the C 5 - C 6 double bond of pyrimidine [45,46,47,48].
However, the role of H-abstraction at nucleobases should not be ignored in the work of numerous studies. For one thing, nucleobases may convert to highly reactive radical species after the HA, which constitutes the initiation step in radical chain reactions [49]. For another, the HA results in the rearrangement and opening of the ring structure, which affects base-pairing abilities. Previous experiments conducted by various groups have demonstrated that the typical site of HA occurrence is at the C 5 methyl group of thymine and the C 2 amino group of guanine [50,51], which is the focal point of this section. Furthermore, numerous studies have characterized the oxidation products resulting from OH-mediated HA in terms of 2-deoxyribose. Significant efforts focus on the addition processes of carbon-centered radicals, triggered by the HA from 2-deoxyribose, with other molecules [52,53]. Furthermore, this section will elaborate on the oxidant of 2-deoxyribose completely caused by HA reaction and its related consequences (such as strand breaks and abasic sites).

3.1.1. Oxidation of C 5 Methyl Group at Thymine

Compared with unsaturated hydrocarbons of the six-member ring, the exocyclic methyl group shows more active reactivity because of less steric hindrance and more accessibility. There is reasonable agreement between computation and experiment. The OH free radical abstracts the hydrogen atom from the C 5 methyl of thymine by employing density functional theory (DFT) in ref. [54]. It is also verified via presenting a detailed Car-Parrinello molecular dynamics study of nucleobases in explicit water interacting with an OH radical [55]. In addition, the statement is also supported in the work of many experiments by varied experimental methods [56,57,58,59]. Figure 3 illustrates the reaction mechanism between OH radicals and the methyl group of thymine in detail. At first, the hydrogen atom of the methyl group at the C 5 position is abstracted by nearby OH radicals (seen in the red circle of Figure 3a), leading to two products: water and the 5-methyl-2′ -deoxyuridine radical (seen in Figure 3b). The product was detected by high-performance liquid chromatography (HPLC) analysis in [59]. By this time, the C 5 , C 6 , and C M atoms(the C atom ofthemethyl group at the C 5 site) share the unpaired electron. In the presence of OH radicals, the 5-methyl-2′ -deoxyuridine radical tends to attract OH free radicals (red dash in Figure 3b), resulting in the formation of a hydroxymethyl group (seen in the blue circle of Figure 3c). The product was identified using gas chromatography/mass spectrometry (GC/MS) in ref. [60]. Then, the C-H bond and O-H bond of the hydroxymethyl group (red circle in Figure 3c) continued to be rupturedby surrounding OH free radicals, leading to the formation of an aldehyde group (namely, 5-formyl-2′ -deoxyuridine (5ForU), seen in Figure 3d. 5ForU, as a common oxidation product of thymine, has been detected in many research studies [51,61,62,63,64].

3.1.2. H-Abstraction from C 2 Amino Group at Guanine

According to previous experimental investigations, four kinds of nucleobases are attacked by OH radicals decrease in the order of Gua > Ade > Cyt > Thy [56,65]. The guanine is preferentially targeted for oxidation by the oxidant for its lowest redox potential. From the foregoing discussion, the H-abstraction from C 2 amino group at guanine is one of the typical types of OH-mediated reactions. A broad band was detected in the visible region (around 610 nm) in ref. [66], which characterizes the hydrogen abstraction from the NH moiety to give a guanyl radical. This point also was confirmed in ref. [67] via a novel isotope labeling strategy. As shown in Figure 4, the H atom of C 2 the amino group at guanine is abstracted by nearby OH radicals, resulting in the formation of a molecule of water and a C 2 -centered radicals (seen in Figure 4a). Subsequently, the H atom at N 1 positions is prone to be abstracted by other OH radicals, as seen in Figure 4b. Therefore, N 1 , N a , and N 3 atoms share the unpaired electron forming C 2 -centered product in the form of resonant (seen in Figure 4c).

3.1.3. Strand Breakage Arising from H-Abstraction at C2′ Site of 2-deoxyribose

As depicted in Figure 5, the breakage of a single-stranded oligonucleotide is typically a consequence of the rupture of a phosphodiester bond. In the simulation, the process mechanism commences with HA originating from various carbon atoms of the sugar moiety. For instance, the HA from 4′ carbon may result in the formation of the C4′=C5′ bond and the breaking of the 5′-phosphodiester bond or the formation of the C4′=C3′ bond and the breaking of 3′-phosphodiester bond; the HA from the 2′ carbon may lead to the formation of the C2′=C3′ bond and the breaking of 3′-phosphodiester bond. Following the research presented in reference [68], the mechanism involving the C4′ radical has remained the most extensively studied process for strand breakage. For concision, the interaction processes of H-abstraction at the C2′ site will be described in detail in this section. As shown in Figure 5a, a first OH radical uptakes one of the H atoms from the C2′ position, leading to two products: a molecule of water and a C2′-centered radical. Then, the 2′ carbon tends to form a double bond with adjacent carbons (such as C2′=C3′, C2′=C1′). The formation of C2′=C3 results in the detachment of phosphate groups from the C3′ position (seen in Figure 5b), which means single-stranded oligonucleotide breaking.

3.1.4. Base Release Resulting from H-Abstraction at C5′ Site of 2-deoxyribose

The base release is a general phenomenon in the free-radical-induced reactions on DNA [44,69,70]. In the simulation, the base release mechanism is also initiated by the HA from different carbons of the sugar moiety. For example, the HA from 5′ or 3′ carbon may lead to base release by forming a double bond with 4′ carbon. It also results from the HA at the 2′ carbon, forming the C2′=C1′ bond. In concision, this section outlines the reaction mechanism between the OH radical and the C5′ of sugar moiety. As illustrated in Figure 6a, the OH radical abstracts an H atom from the C5′, resulting in the formation of a water molecule. Hence, the 5′ carbon transforms into a 5′ carbon radical. To keep stable, the 5′ carbon radical tends to form the C5′=C4′ bond (seen in Figure 6b). It results in the breaking of the C4′-O bond and the transformation from the C1′-O bond into the C1′=O bond. At this time, the 1′ carbon is oversaturated and unstable, which yields the detachment of the intact base from sugar moiety, leaving the backbone intact (seen in Figure 6c).

3.2. Dose Effects of OH Radical on Nucleobases and Sugar Moiety

Figure 7 shows the statistics for the broken N-H bonds in the reaction of OH radicals and nucleobases. It is clear that the breaking ratio of N-H bonds decreases in the order of Thy > Cyt > Ade ≈ Gua. As shown in Figure 7, thymine contains a methyl group at the C 5 position with carbonyl groups at the C 4 and C 2 positions. So, no other chemical bonds compete with amino in attracting OH radicals at the same level. The breaking probability of the N-H bond in thymine is up to 90%. However, cytosine contains two N-H bonds, which reduces the probability of a single N-H being attacked. Therefore, the curve of cytosine is well below that of thymine at low radical concentrations and roughly equal at high concentrations. Consequently, guanine, containing three N-H bonds, has the lowest breaking-ration of N-H bonds. As for adenine, the HA from the exocyclic amino group increases reactivity on the C 2 site. It induces the competition between the C 2 position and the exocyclic amino in attracting OH.
Figure 8 reveals the probability of broken C-H bonds in the reaction of OH radicals and nucleobases. In the simulation, the breaking ratio of C-H bonds is highly lower than N-H in four nucleobases, which is in line with previous studies [21]. The unsaturated bond of aromatic ring structures is responsible for the stability of C-H bonds on bases. It is obvious that the breaking ratio of C-H bonds decreases in the order of Ade > Thy > Cyt ≈ Gua in Figure 8. Influenced by the HA reaction from the exocyclic amino group, the H atom at the C 2 site is more inclined to be abstracted by near OH radicals. It leads to the highest breaking ratio of C-H bonds of adenine. In the case of thymine, the probability of broken C-H bonds is second-highest. This is because the C-H bond on the exocyclic group is more attacked than that of the ring structure. Furthermore, as depicted in Figure 8, curves representing cytosine and guanine remain close to zero. The increase in OH radical concentration does not alter these statistical outcomes, aligning with the simulation results reported in reference [71].
In the simulation, the destructive impact of sugar moiety can be divided into four types: strand breakage, ring-opening, ethylenic bond, and release base. The probability of occurrence decreases with the mentioned order and increases with the rising of OH radicals, as shown in Figure 9. It should be noted that each type of damage is accompanied by at least one HA reaction, indicating that the C-H bonds of the sugar moiety are more susceptible than those of the base ring. In addition, despite the overall rupture ratio of 2-deoxyribose being below 15%, the impact of OH radicals remains significant. On the one hand, the presence of multiple destructive factors can induce single-strand break (SSB), double-strand break (DSB), tandem lesions, and various clustered lesions could be induced under the case of multiple destructive factors. On the other hand, further lesions (such as DNA/DNA and DNA/protein cross-links) could be triggered by injured 2-deoxyribose.

4. Conclusions

In recent years, plasma medicine has attracted increasing attention, and a detailed understanding of CAP on biological issues is very essential for plasma medicine. To elucidate the interaction mechanism between OH radicals with a single nucleotide, a reactive MD simulation is performed to discuss the interaction processes of four types of nucleotides and OH radicals for various concentrations at the atomic level. The computational data describe the typical H-abstraction reaction processes at the C 5 methyl group of thymine, the C 2 amino group at guanine, and 2-deoxyribose. In the simulation, the breakage of single-stranded oligonucleotides is observed, which seriously influences the biological activity of cellular DNA. The base release induced by OH radicals means the loss of base sequence information, and the H-abstraction at nucleobases affects the gene strand complementarity, gene transcription, and replication. The impact of OH radical dosage on bond formation and breakage is also discussed based on computational data. Additionally, this study compares the distinct breakage ratios of chemical bonds among four types of nucleobases, taking into account their unique molecular structures. The simulation results enhance our understanding of the interactions between oligonucleotide and OH radicals by unveiling detailed insights into typical H-abstraction reactions, which could potentially aid in the optimization of plasma sources and operations in the field of plasma medicine.

Author Contributions

Methodology, Y.-T.Z.; Software, Y.C.; Validation, Y.C.; Data curation, Y.-X.J.; Writing—original draft, Y.-X.J.; Writing—eview and editing, Y.-T.Z.; Visualization, Y.C.; Project administration, Y.-T.Z.; Funding acquisition, Y.-T.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research has received funding from National Natural Science Foundation of China, grant number 11975142 and 12375201.

Data Availability Statement

The data that support the findings of this corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Schematic representation of a basic nucleotide molecule structure.
Figure 1. Schematic representation of a basic nucleotide molecule structure.
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Figure 2. A reactive MD simulation box with a single-stranded oligonucleotide and 15 OH radicals.
Figure 2. A reactive MD simulation box with a single-stranded oligonucleotide and 15 OH radicals.
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Figure 3. Snapshots from MD simulations showing the reaction processes of OH radicals with C 5 methyl group at thymine. The OH radical captures an H atom from the methyl group, as illustrated in (a), forming an unsaturated site. Subsequently, the liberated OH is adsorbed onto this site (b), forming hydroxymethyl groups (c). The surrounding OH radicals continue to break the C-H and O-H bonds of the hydroxymethyl group (indicated by red circles in (c)), ultimately forming the aldehyde group (d).
Figure 3. Snapshots from MD simulations showing the reaction processes of OH radicals with C 5 methyl group at thymine. The OH radical captures an H atom from the methyl group, as illustrated in (a), forming an unsaturated site. Subsequently, the liberated OH is adsorbed onto this site (b), forming hydroxymethyl groups (c). The surrounding OH radicals continue to break the C-H and O-H bonds of the hydroxymethyl group (indicated by red circles in (c)), ultimately forming the aldehyde group (d).
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Figure 4. Snapshots from MD simulations, showing the reaction processes of OH radicals with C 2 amino group at guanine. One of the H atoms at C2 is abstracted by OH radicals, forming a water molecule (a). Following this, an H-atom at the N1 position is abstracted by an OH radical (b). Consequently, the N1, N2, and N3 atoms share unpaired electrons, forming the C2-centered product in its resonance form (c).
Figure 4. Snapshots from MD simulations, showing the reaction processes of OH radicals with C 2 amino group at guanine. One of the H atoms at C2 is abstracted by OH radicals, forming a water molecule (a). Following this, an H-atom at the N1 position is abstracted by an OH radical (b). Consequently, the N1, N2, and N3 atoms share unpaired electrons, forming the C2-centered product in its resonance form (c).
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Figure 5. Snapshots from MD simulations, showing the reaction processes of strand breakage upon the impact of OH radicals. The OH radical abstracts an H atom from the C2′ position, forming two products: a water molecule and a C2′ centered radical (a). Subsequently, C2 tends to establish a double bond with an adjacent carbon, such as C2′=C3′ (b).
Figure 5. Snapshots from MD simulations, showing the reaction processes of strand breakage upon the impact of OH radicals. The OH radical abstracts an H atom from the C2′ position, forming two products: a water molecule and a C2′ centered radical (a). Subsequently, C2 tends to establish a double bond with an adjacent carbon, such as C2′=C3′ (b).
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Figure 6. Snapshots from MD simulations, showing the reaction processes of base release upon the impact of OH radicals. The OH radical abstracts an H atom from C5′, forming a water molecule (a). To maintain stability, the resulting C5′ radical forms a C5′=C4′ double bond (b). This process leads to the cleavage of the C4′-O bond (b) and the conversion of the C1′-O bond into a C1′=O double bond (c). Subsequently, C1′ enters a supersaturated and unstable state, facilitating the detachment of the intact base from the sugar molecule while preserving the integrity of the backbone (c).
Figure 6. Snapshots from MD simulations, showing the reaction processes of base release upon the impact of OH radicals. The OH radical abstracts an H atom from C5′, forming a water molecule (a). To maintain stability, the resulting C5′ radical forms a C5′=C4′ double bond (b). This process leads to the cleavage of the C4′-O bond (b) and the conversion of the C1′-O bond into a C1′=O double bond (c). Subsequently, C1′ enters a supersaturated and unstable state, facilitating the detachment of the intact base from the sugar molecule while preserving the integrity of the backbone (c).
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Figure 7. The breaking-ratio of N-H bods upon impact of OH radicals.
Figure 7. The breaking-ratio of N-H bods upon impact of OH radicals.
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Figure 8. The breaking-ratio of C-H bods upon impact of OH radicals.
Figure 8. The breaking-ratio of C-H bods upon impact of OH radicals.
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Figure 9. The rupture ratio of 2-deoxyribose bonds upon impact of OH radicals.
Figure 9. The rupture ratio of 2-deoxyribose bonds upon impact of OH radicals.
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Jiang, Y.-X.; Chen, Y.; Zhang, Y.-T. Modeling Study of OH Radical-Dominated H-Abstraction Reaction for Understanding Nucleotides Oxidation Induced by Cold Atmospheric Plasmas. Plasma 2024, 7, 498-509. https://doi.org/10.3390/plasma7020026

AMA Style

Jiang Y-X, Chen Y, Zhang Y-T. Modeling Study of OH Radical-Dominated H-Abstraction Reaction for Understanding Nucleotides Oxidation Induced by Cold Atmospheric Plasmas. Plasma. 2024; 7(2):498-509. https://doi.org/10.3390/plasma7020026

Chicago/Turabian Style

Jiang, Yu-Xuan, Yang Chen, and Yuan-Tao Zhang. 2024. "Modeling Study of OH Radical-Dominated H-Abstraction Reaction for Understanding Nucleotides Oxidation Induced by Cold Atmospheric Plasmas" Plasma 7, no. 2: 498-509. https://doi.org/10.3390/plasma7020026

APA Style

Jiang, Y. -X., Chen, Y., & Zhang, Y. -T. (2024). Modeling Study of OH Radical-Dominated H-Abstraction Reaction for Understanding Nucleotides Oxidation Induced by Cold Atmospheric Plasmas. Plasma, 7(2), 498-509. https://doi.org/10.3390/plasma7020026

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