AbstractNon-thermal plasma (NTP) is an emerging technology with extensive applications in biomedicine, including treatment of abnormal pigmentation. However, very few studies have investigated how plasma induces anti-melanogenesis. Here, liquid plasma was prepared by treating an NTP jet with helium and oxygen (as carrier gases) for 15 min in serum-free culture media.

。然而，很少有研究调查血浆如何诱导抗黑素生成。在这里，通过在无血清培养基中用氦气和氧气（作为载气）处理NTP射流15分钟来制备液体等离子体。

In the zebrafish model, pigmentation ratio was observed with or without liquid plasma. The anti-melanogenic effect of liquid plasma was evaluated in human melanocytes by assessing the expression of melanogenesis-related genes using western blotting, RT-PCR, and immunohistochemistry. Liquid plasma reduced pigmentation in the zebrafish model and inhibited melanin synthesis in primary human melanocytes.

在斑马鱼模型中，观察到有或没有液体血浆的色素沉着率。通过使用蛋白质印迹，RT-PCR和免疫组织化学评估黑素生成相关基因的表达，在人黑素细胞中评估了液体血浆的抗黑素生成作用。液体血浆减少了斑马鱼模型中的色素沉着，并抑制了原代人黑素细胞中的黑色素合成。

Intracellular reactive oxygen species levels decreased and Nrf2 expression increased in liquid plasma–treated melanocytes. Liquid plasma affected microphthalmia-associated transcription factor (MITF) and tyrosinase mRNA and protein levels, tyrosinase activity, and melanin content. Considering the role of Wnt/β-catenin and PI3K/Akt pathways in melanogenesis, the effect of liquid plasma on this pathway was determined; liquid plasma decreased active β-catenin, LEF1/TCF4, MITF, and tyrosinase levels in a time-dependent manner and inhibited the nuclear translocation of β-catenin.

在液体血浆处理的黑素细胞中，细胞内活性氧水平降低，Nrf2表达增加。液体血浆影响小眼症相关转录因子（MITF）和酪氨酸酶mRNA和蛋白质水平，酪氨酸酶活性和黑色素含量。；液体血浆以时间依赖性方式降低活性β-连环蛋白，LEF1/TCF4，MITF和酪氨酸酶水平，并抑制β-连环蛋白的核转位。

This inhibition subsequently suppressed melanogenesis by downregulating MITF and tyrosinase. These results suggest that liquid plasma may be used for treating pigmentary disorders..

这种抑制随后通过下调MITF和酪氨酸酶来抑制黑素生成。这些结果表明，液体血浆可用于治疗色素性疾病。。

IntroductionOne of the most actively explored realms in applied technology utilizing plasma is a medical-related study, called ‘plasma medicine’1. Plasma, often referred to as the fourth state of matter alongside solid, liquid, and gas, is created by applying energy on a neutral gas, causing the electrical conductivity of the ionized gaseous material to improve over time2,3.

引言利用血浆的应用技术中最积极探索的领域之一是一项医学相关研究，称为“血浆医学”1。等离子体通常被称为固体、液体和气体旁边的第四种物质状态，它是通过对中性气体施加能量而产生的，导致电离气体材料的电导率随着时间的推移而提高2,3。

Plasma includes charged ions, free electrons, reactive species, and fragmented molecules, and releases electromagnetic radiation, primarily in the form of UV radiation and visible light4. This unique state of matter is not only found in naturally occurring phenomena, such as stars, lightning bolts, and auroras, but is also used for various artificial applications in our daily lives, including fluorescent lights, neon signs, and plasma TVs5.

等离子体包括带电离子，自由电子，活性物质和碎片分子，并释放电磁辐射，主要以紫外线和可见光的形式4。这种独特的物质状态不仅存在于恒星、闪电和极光等自然现象中，而且还用于我们日常生活中的各种人工应用，包括荧光灯、霓虹灯和等离子电视5。

Faure et al., developed a laser-plasma accelerator capable of generating monoenergetic electron beams, suggesting broad potential for applications in radiotherapy and radiobiology6.Non-thermal plasma (NTP) is a subtype of plasma, which is produced below 40 °C and under atmospheric pressure7. Due to its relatively low temperature, NTP does not harm tissues, and is therefore widely used in various medical fields.

Faure等人开发了一种能够产生单能电子束的激光等离子体加速器，这表明其在放射治疗和放射生物学中具有广泛的应用潜力6.非热等离子体（NTP）是一种等离子体亚型，在40°C以下和大气压下产生7。由于其相对较低的温度，NTP不会伤害组织，因此广泛用于各个医学领域。

NTP can stimulate blood clotting by activating platelets and initiating fibrin formation8. Additionally, various reactive oxygen and nitrogen species are generated, including radicals, ozone, and peroxides. These species exhibit potent antimicrobial properties and effectively damage the cell membrane, proteins, and DNA of bacteria9.

NTP可以通过激活血小板和启动纤维蛋白形成来刺激凝血8。此外，还会产生各种活性氧和氮物质，包括自由基，臭氧和过氧化物。这些物种表现出有效的抗菌特性，并有效破坏细菌的细胞膜，蛋白质和DNA 9。

Some studies reported that plasma-induced reactive oxygen species (ROS) contribute to wound healing by promoting molecular signaling pathways associated with epithelial migration, inducing the secretion of cytokines, and stimul.

一些研究报道，血浆诱导的活性氧（ROS）通过促进与上皮迁移相关的分子信号传导途径，诱导细胞因子的分泌和刺激来促进伤口愈合。

MITF sense 5′-CACATACAGCAAGCCCAA-3′.

无5′-CATAACAGCAAGCCCAA-3′的MITF。

antisense 5′-CAGTGCTCTTGCTTCAGA-3′.

反义5′-CAGTGTCTTGCTTCAGA-3′。

tyrosinase sense 5′-ATCCAGAAGCTGACAGGA-3′.

酪氨酸酶5™-ATCAGAGCTGACAGGA-3™。

antisense 5′-TTTGAGAGGCATCCGCTA-3’.

反义5′-TTTGGGCATCCGCTA-3'。

GAPDH sense 5′-GAGTACGTCGTGGAGTCCA-3′.

GAPDH有义5'-GAGTACGTCGTGGAGTCCA-3'。

antisense 5′-ATGGCATGGACTGTGGTCA-3′.

反义5±-ATGCATGACTGTGGTGTCA-3™。

PCR products were separated on a 1% agarose gel and observed using a LAS4000 (Fuji, Japan).Measurement of extracellular H2O2

PCR产物在1%琼脂糖凝胶上分离，并使用LAS4000（日本富士）进行观察。

To measure extracellular H2O2 production, the plasma-treated supernatant was used with a hydrogen peroxide assay kit (Abcam, Cambridge, UK, ab102500) according to the manufacturer’s protocol. The concentration of H2O2 in the supernatant was determined using a microplate reader (Epoch 2; BioTek Instruments, Inc., Winooski, VT, USA) with excitation at 540 nm.

为了测量细胞外H2O2的产生，根据制造商的方案，将血浆处理的上清液与过氧化氢测定试剂盒（Abcam，Cambridge，UK，ab102500）一起使用。使用酶标仪（Epoch 2；BioTek Instruments，Inc.，Winooski，VT，USA）在540 nm激发下测定上清液中H2O2的浓度。

according to the manufacturer’s protocol.Measurement of intracellular ROSTo detect intracellular ROS production, cells were treated with liquid plasma for 24 h and then hydroethidine was used as described previously41. Fluorescent cells were analyzed using flow cytometry.Statistical analysisAll data were compared using one-way analysis of variance (ANOVA) (SPSS 12.0; SPSS Inc., Chicago, IL, U.S.A.).

根据制造商的协议。细胞内ROS的测量为了检测细胞内ROS的产生，将细胞用液体血浆处理24小时，然后如前所述使用氢乙啶41。使用流式细胞术分析荧光细胞。。

The results are expressed as mean ± standard deviation (SD). All p-values were two-tailed, and p-values less than 0.05 were considered statistically significant..

。所有p值均为双尾，小于0.05的p值被认为具有统计学意义。。

Data availability

数据可用性

All data generated or analyzed during this study are included in this published article and its Supplementary Information files.

本研究期间生成或分析的所有数据均包含在本文及其补充信息文件中。

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Download referencesFundingThis research was supported by a grant from the Korea Health Technology R&D Project of the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (HR21C1003), the Basic Science Research Program of the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT, and Future Planning (RS-2023-00273483), the Ministry of Environment (MOE) of the Republic of Korea (2021003350001), and the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), Republic of Korea (RS-2024-00438448).Author informationAuthor notesThese authors contributed equally: Ju Hyun Yun and Yeon Soo Kim.These authors jointly supervised this work: Sung Un Kang and Chul-Ho Kim.Authors and AffiliationsDepartment of Otorhinolaryngology-Head and Neck Surgery, College of Medicine, Ewha Womans University, Seoul, 07985, KoreaJu Hyun YunDepartment of Otorhinolaryngology-Head and Neck Surgery, Korea University College of Medicine, Seoul, 02841, KoreaYeon Soo KimDepartment of Dermatology, School of Medicine, Ajou University, Suwon, 16499, KoreaHee Young KangDepartment of Otolaryngology, Ajou University School of Medicine, Suwon, 16499, KoreaSung Un Kang & Chul-Ho KimAuthorsJu Hyun YunView author publicationsYou can also search for this author in.

下载参考文献资助这项研究得到了韩国健康产业发展研究所（KHIDI）韩国健康技术研发项目（HR21C1003）的资助，韩国健康与福利部（HR21C1003）资助，韩国国家研究基金会（NRF）基础科学研究计划（RS-2023-00273483），韩国环境部（MOE）（2021003350001）资助，以及韩国健康产业发展研究所（KHIDI）资助的韩国健康技术研发项目（RS-2024-00438448）。作者信息作者注意到这些作者做出了同样的贡献：Ju Hyun Yun和Yeon Soo Kim。这些作者共同监督了这项工作：Sung Un Kang和Chul Ho Kim。作者和附属机构梨花女子大学医学院耳鼻咽喉头颈外科，首尔，07985，KoreaJu Hyun Yung韩国大学医学院耳鼻咽喉头颈外科，首尔，02841，KoreaYeon Soo Kim Ajou大学医学院皮肤科，水原，16499，KoreaHee Young Kang Ajou大学医学院耳鼻咽喉科，水原，16499，KoreaSung Un Kang＆Chul Ho Kimouthor作者Ju Hyun YunView作者出版物您也可以在中搜索这位作者。

PubMed Google ScholarYeon Soo KimView author publicationsYou can also search for this author in

PubMed Google ScholarYeon Soo KimView作者出版物您也可以在

PubMed Google ScholarHee Young KangView author publicationsYou can also search for this author in

PubMed Google ScholarHee Young KangView作者出版物您也可以在

PubMed Google ScholarSung Un KangView author publicationsYou can also search for this author in

PubMed Google ScholarSung Un KangView作者出版物您也可以在

PubMed Google ScholarChul-Ho KimView author publicationsYou can also search for this author in

PubMed Google ScholarChul Ho KimView作者出版物您也可以在

PubMed Google ScholarContributionsJ.H.Y. designed the study, analyzed the results, and wrote the manuscript; Y.S.K. analyzed the results and wrote the manuscript; H.Y.K. analyzed the results and wrote the manuscript; S.U.K. designed and performed all experiments and wrote the manuscript; C-H.K.

PubMed谷歌学术贡献。H、 Y.设计了研究，分析了结果，并撰写了手稿；Y、 S.K.分析了结果并撰写了手稿；H、 Y.K.分析了结果并撰写了手稿；S、 英国设计并进行了所有实验并撰写了手稿；C-H.K。

supervised experiments and wrote the manuscript.Corresponding authorsCorrespondence to.

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Reprints and permissionsAbout this articleCite this articleYun, J.H., Kim, Y.S., Kang, H.Y. et al. A novel liquid plasma derivative inhibits melanogenesis through upregulation of Nrf2.

转载和许可本文引用本文Yun，J.H.，Kim，Y.S.，Kang，H.Y.等人。一种新型液体血浆衍生物通过上调Nrf2抑制黑素生成。

Sci Rep 14, 21851 (2024). https://doi.org/10.1038/s41598-024-72750-zDownload citationReceived: 17 May 2024Accepted: 10 September 2024Published: 19 September 2024DOI: https://doi.org/10.1038/s41598-024-72750-zShare this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

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KeywordsLiquid type non-thermal plasma (liquid plasma)MelanocytesMelanin

关键词液体型低温等离子体（液体等离子体）黑素细胞黑色素

β -catenin

β-连环蛋白

MITF

MITF

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