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Xia Lab-Radical Mass Spectrometry

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Our research program aims broadly at developing new mass spectrometry (MS) methods for bio-analysis. Research efforts are currently focused on utilizing radical reactions as a unique approach to providing the high level of structural information of proteins and lipids, such as disulfide linkage pattern and carbon-carbon double bond location. We are also developing new MS instrumentation to investigate the radical attack on biomolecules in the gas phase and characterizing a series of peptide or protein radicals which are of biological importance. 

光催化Paternò-Büchi反应与离子淌度-质谱联用对皮脂进行鸟枪法分析

清华大学化学系瑕瑜教授课题组于近期在Analytical Chemistry杂志上发表了题为“Shotgun Lipidomic Profiling of Sebum Lipids via Photocatalyzed Paternò-Büchi Reaction and Ion Mobility-Mass Spectrometry” 的论文,第一作者是博士生施恒学。此研究中,该团队开发了一种基于离子淌度-质谱、Paternò-Büchi反应-MS/MS (PB-MS/MS)的鸟枪法分析流程,实现了对皮脂组超过900种脂质C=C异构体的快速及灵敏分析。

皮脂是皮脂腺的分泌物,构成皮肤的保护层和保湿层。皮脂的无创获取方法及其反映远端器官病理变化的潜力,使其成为理想的生物样本。皮脂由非极性脂质组成,主要包含蜡酯(WE)、脂肪酸(FA)、甘油三酯(TG)、甘油二酯(DG)、胆固醇酯(CE)及角鲨烯(SQ)。非极性脂质的电离效率低,且其同分异构体和同重素的多样性为皮脂组的分析带来了挑战。本研究旨在通过发展高效率电荷标签PB衍生反应,结合电喷雾电离-离子淌度-串联质谱实现对皮脂组在精细结构层级上的定性定量。

首先,研究者们使用电荷标签PB试剂ethyl 2-oxo-2-(pyridine-3-yl)acetate (EP)和光催化剂米氏酮对脂质C=C的PB反应进行评估(图1)。以单不饱和蜡酯WE 18:0/18:1(Δ9)(见图2)为例,其经电荷标签PB反应后,离子化效率可提升约1000倍。PB产物的MS2 CID产生了指向n-端C=C位置的诊断离子,进一步的pseudo-MS3 CID分析能够识别Δ-端位置,从而实现WE中FA链上C=C位置的特异性鉴定。研究者们还对WE 18:1(Δ9)/18:0进行了PB-MS/MS分析。无论C=C双键是位于FA链还是FOH链,PB-MS/MS均能实现链特异性的C=C位置鉴定。此外,研究者还对SQ的C=C进行了PB-MS1和PB-MS2 CID分析,成功鉴定了SQ中各个C=C双键的位置。

图1 皮脂的PB-MS/MS分析流程和碎裂模式

图2 蜡酯WE 18:0/18:1(Δ9)的PB-MS/MS分析

在鸟枪法分析皮脂时,研究者们采用高分辨率环形离子淌度谱(cyclic IMS)对来自含多一个不饱和度脂质的同位素峰( [M+2 Da])进行分离。研究表明,经过10圈cyclic IMS分离(分辨率约260),WE 36:2/WE 36:1 (5:1)的PB产物中,[M+2 Da]干扰由60 %显著降至4 %。此方法相较于反相色谱法(干扰6 %),干扰更少,分离速度也更快(< 250 ms vs. 30 min)。

基于以上,研究者开发了皮脂的分析工作流程(见图3)。首先,他们通过RPLC-APCI-MS定性定量蜡酯的总组成,随后采用结合离子淌度-质谱、PB-MS/MS的鸟枪法分析流程对皮脂进行C=C结构层次的分析。cyclic IMS实现了PB反应后的皮脂中不同脂质亚类、脂质链长不同和不饱和度差异以及同重素干扰的分离。此外,cyclic IMS还可以提升PB-MS/MS对脂质C=C异构体的鉴定能力。以皮脂中的WE 36:1为例,PB-MS/MS产生的C=C诊断离子经过一圈的cyclic IMS分离,其淌度到达时间与C=C位置(m/z)呈现线性关系。研究者们沿着该线性关系的趋势,可发现2个相对丰度低于0.3%的诊断离子。这一发现表明,在即便缺少脂质C=C位置异构体标准品的情况下,基于PB-MS/MS诊断离子的IMS到达时间的线性关系,可以提高对低丰度C=C位置异构体的鉴定能力。

图3 皮脂的分析工作流程

PB-MS/MS显著拓展了对皮脂样本中脂质的丰富性的认知。以WE 36:1为例,研究者们实现了对其含有的31种C=C异构体的定性和定量分析(图4a)。进而,针对WE总碳数为C28至C42,研究者们实现了链特异性C=C位置异构体的定量分析(图4b),共计600个的C=C异构体。

图4 皮脂中WE链特异性C=C异构体定性定量分析

综上,研究者们结合PB-MS/MS和离子淌度-质谱法,开发了对皮脂组WE、TG、DG和CE的C=C位置异构体的鸟枪法快速分析流程,实现了共计超过900个C=C异构体的定性定量分析。

 

本文编辑:施恒学 

本文审核:瑕瑜

原文链接:https://doi.org/10.1021/acs.analchem.4c00141

 

鞘氨醇-1-磷酸转运蛋白(SPNS2)转运机制研究

哈工大生命科学中心何元政课题组在鞘氨醇-1-磷酸(S1P)通过人鞘氨醇-1-磷酸转运蛋白(SPNS2)转运的结构基础方面取得新进展,揭示了SPNS2独特的S1P转运机制。12月20日,研究成果以《鞘氨醇-1-磷酸通过人鞘氨醇-1-磷酸转运蛋白(SPNS2)转运的结构基础》(Structural basis of Sphingosine-1-phosphate transport via human SPNS2)为题发表在《细胞研究》(Cell Research)上。该研究阐明了SPNS2介导的S1P转运,并有助于开发新型SPNS2抑制剂,为治疗自身免疫疾病提供新的靶点。

鞘氨醇-1-磷酸是细胞膜鞘脂的代谢物,作为脂质信号分子在免疫反应、血管发育和神经系统稳态等多种生理过程中发挥重要作用。S1P的适当空间梯度是S1P信号转导的关键,S1P空间梯度的建立是由S1P转运蛋白(包括SPNS2和MFSD2B)将S1P从细胞内侧运输到细胞外侧来实现的。尽管在建立S1P的空间梯度中起着关键作用,但目前对S1P的转运机制知之甚少。

基于在S1P转运中发挥的重要作用和靶向SPNS2降低自身免疫性疾病方面的可能性,何元政课题组运用冷冻电镜技术解析了SPNS2的无配体结合状态、S1P结合状态、FTY720-P结合状态和抑制剂16d结合的多种状态结构(图1)。该研究开发出抗SPNS2的纳米抗体,以克服小尺寸膜蛋白在冷冻电镜结构解析中的困难,并开发出S1P转运检测方法来评估SPNS2的转运活性。该研究揭示了SPNS2门控区域中由Y246和G333形成的氢键是控制底物转运的关键因素(图2)。该研究还提出了用“阶梯”模型来阐述SPNS2的底物转运机制,底物的磷酸头基是运用SPNS2细胞内腔中一系列极性残基形成的“梯子”爬升到达了门控区域,进而进行脂质转运(图2)。此外,该研究还解析了最新研发的SPNS2抑制剂16d结合SPNS2的结构,并对其抑制机理进行了阐释。综上所述,通过解析SPNS2及其与小分子复合物的结构,该研究为理解S1P的转运机制提供了框架,并为设计靶向SPNS2的抑制剂提供了结构基础。

图1. SPNS2及其与小分子复合物的冷冻电镜结构

图2. SPNS2的底物转运机制

何元政课题组博士研究生段亚宁、新加坡国立大学医学院生物化学系阮龙(Long N.Nguyen)课题组博士研究生梁南希(Nancy C.P.Leong)、清华大学化学系瑕瑜课题组博士研究生赵婧为并列第一作者。何元政研究员、阮龙教授为共同通讯作者。何元政课题组硕士研究生张羽,博士研究生王娜,博士后徐珍媚,博士研究生夏瑞雪、马正雄、钱雨、尹晗、祝鑫焱,阮龙课题组博士研究生阮达特(Dat T.Nguyen)、哈和(Hoa T.T.Ha),瑕瑜教授参与该课题相关研究工作。

该研究获国家自然科学基金和哈工大生命科学中心启动基金等资助。

 

本文编辑:梁英爽,段亚宁

本文审核:赵   婧

原文链接:https://doi.org/10.1038/s41422-023-00913-0

TLR天然免疫信号传递中PI4P介导的细胞外囊泡生成新机制

细胞外囊泡(Extracellular Vesicles,EVs)是细胞分泌的磷脂双分子层膜包裹而成的小泡(图1)。1996年首次在抗原呈递过程中发现,它不仅是细胞排出垃圾的方式,更在细胞间信号传递中发挥重要功能。Toll样受体(Toll-like receptor, TLR)是天然免疫与适应性免疫之间最重要的桥梁之一,严格的信号传导和时空调控为免疫系统的有序运行提供保障,可有效避免脓毒症等天然免疫疾病的发生。然而,EVs作为重要的细胞间通讯介质,在TLRs信号传递过程中的功能报道尚少,同时TLRs激活是否会调控EVs的生成与释放尚无充分证据。

2023年4月,来自清华大学的尹航研究组在Journal of Extracellular Vesicles上发表题为“Exosomal lipid PI4P regulates small extracellular vesicle secretion by modulating intraluminal vesicle formation”的文章,报道了一项新的PI4P在调控EV生成的分子机制,并且为EVs调控天然免疫TLR4信号调控提供新证据,为新的EV调控与TLR4天然免疫信号调控提供潜在靶点(图1)。

图1 LPS-TLR4 信号通路调节 EVs 释放的分子机制模式图

该研究发现,在TLR4激活条件下,巨噬细胞内EVs释放速率随TLR4的配体革兰氏阴性细菌外部细胞壁的一种主要糖脂组分——脂多糖(Lipopolysaccharide,LPS)刺激时间先升高后降低,表现出明显的时间规律。通过与清华大学化学系瑕瑜课题组合作,成功实现对EVs中微量磷脂——磷脂酰肌醇的定量检测,发现介导囊泡生成的磷脂酰肌醇-4-磷酸(Phosphatidylinositol-4-phosphate,PI4P)与EVs的释放速率呈显著正相关关系(图2)。

图2 LPS刺激调控EV释放速率变化及EV中PIP含量

探究分子机制发现,LPS刺激短时间内,TLR4激活产生的I型干扰素可调控PI4P激酶表达增加多囊泡体(MVB)上PI4P含量,从而招募下游蛋白促进胞内囊泡(ILV)生成,从而增加EV释放速率;LPS刺激时间增长后,PI4P从MVB减少,从而EVs生成与释放减少。TLR4受体持续性激活所致的过度免疫反应是脓毒血症的主要诱因,EVs所参与的严格时序调控将有效避免信号的持续性激活。

进一步探究EVs释放与LPS刺激信号的关系,发现TLR4天然免疫信号激活后,巨噬细胞内LPS-TLR4下游的TRIF信号通路激活所产生 IFN-β,对PI(4,5)P2激酶PIP5K1C的表达调控实现,通过改变PI4P的定位调控EV的生成(图3)。该结论在巨噬细胞RAW264.7细胞系和C57BL/6J小鼠原代BMDMs生理模型中均表现出一致的调控作用。

图3  LPS-IFN-β信号通路调控PIP变化及EV前体的生成

近年来,由于EV可以实现液体活检以及载药透过血脑屏障等优势,该领域的研究持续升温。天然免疫中EV调控的新机制的发现为疾病的发病机理提供新解释,同时EV生成机制的解析也为其标准化生产提供潜在参考途径。

 

本文编辑:夏天

本文审核:靳学

原文链接:https://doi.org/10.1002/jev2.12319

1. Gas-phase radical ion chemistry

Radical ions, which consist of unpaired electrons, offer distinct gas-phase ion chemistry as compared to the even-electron species. Radical chemistry can be utilized to tackle challenging problems, such as differentiating isomeric structures, which would otherwise not be solved by traditional MS analysis of even-electron ions of the biomolecules. We are developing MS instrumentation and methods to facilitate radical reactions for either in the vacuum or in ambient air.

1. Radical reactions at the interface of ESI-MS.

Radicals or excited neutrals are generated via air discharge or UV photolysis and subsequently reacted with ions entrained in the ESI plume.  Radical reactions are subsequently monitored and characterized in situ by MS analysis. Reactions of peptides and lipids with various radical species have been investigated, including •OH, •CH2OH, excited state of (CH3)2CO.  Novel analytical applications based on these reactions have been developed.

AC; 2010, 82, 2856JASMS., 2011, 22, 922Analyst, 2013, 138, 2840;JASMS, 2014, 25, 1192.

 

2. Ion/radical reactions in a linear ion trap mass spectrometer.

A first linear ion trap mass spectrometer capable of studying reactions between the mass-selected ions and radicals has been recently developed and tested in collaboration with Prof. Zheng Ouyang from Biomedical Engineering at Purdue. This instrument uses a rectilinear ion trap as the mass analyzer and gas-phase reactor, an ESI as the source of the bimolecular ions, a pulsed pyrolysis valve for the generating an intense radical beam, and a glow discharge electron impact (GDEI) source for radical characterization. This MS platform can facilitate mechanistic studies on the radical attack to biomolecules that are of biological significance

 

3. Chemistry of bio-radical ions.

Through radical relations at ESI-MS interface, our group has synthesized and studied cysteine sulfinyl radical in the gas phase (Cys-SO•), which has a wide relevance to radical-induced oxidation of proteins, however, has been poorly characterized due to its transient nature in the condensed phases. Different from carbon-centered radicals, we have discovered that sulfinyl radical has a dual property of being acting as a base or a radical via combined experimental and theoretical approaches. The base property allows the formation of proton bridging between the radical site and the neighboring amino acid residues and thus contributes to the overall structural and chemical property of a polypeptide.

Love et al. J. Am. Chem. Soc., 2013, 135, 6226

Tan et al. J Phys. Chem. A, 2014, 118 ,11828

 

We also systematically investigated the inter- and intra-molecular reactivity of the sulfinyl radicals. They showed that the cysteine sulfinyl radical can react with a disulfide bond or a thiol group within a peptide, which has implications to radical-induced disulfide bond scrambling.

Using functionalized sulfinyl radical as a precursor of glycyl-type radical, we have also developed an experimental approach based on tandem mass spectrometry to correlate the electronic property of the connecting groups to the stability of glycyl-type radical species (Angew. Chem., Int. Ed., 2014, 53, 1887-1890, featured as the front cover and the “hot article”).

Tan et al. Angew. Chem. Int. Ed. 2014, 53, 1887

4. Application of radical chemistry for bio-analysis Analysis of unsaturated lipids:

Facile determination of C=C bond locations of lipids is a long-standing challenge for lipid analysis using MS. Intact lipid analysis via conventional low energy collisional activation tandem mass spectrometry does not provide information for the C=C location because much higher energies are required for cleaving C-C or C=C bonds and thus no fragments specific to the C=C locations can be produced. Utilizing the high reactivity of C=C with radicals or electrophilic excited state molecules, our group has recently developed coupling Paternò–Büchi (PB) reaction with MS/MS for highly confident C=C bond location determination in lipids (Angew. Chem., Int. Ed, 2014, 53, 2592-2596). This PB-MS/MS strategy is currently being developed for unsaturated lipid C=C location isomer characterization and quantitation of biological samples (tissue, cell lines, plasma), application to shotgun and separation based lipidomics, biomarker discovery, and bio-imaging.

Ma and Xia, Angew. Chem. Int. Ed. 2014, 53, 2592

 

2. PB-MS/MS developed by our group

42. Tian Xia, Xue Jin, Donghui Zhang, Jitong Wang, Ruijun Jian, Hang Yin, Yu Xia*, "Alternative fatty acid desaturation pathways revealed by deep profiling of total fatty acids in RAW 264.7 cell line", J. Lipid. Res. 2023.

https://doi.org/10.1016/j.jlr.2023.100410

41.  Qiaohong Lin, Ruijun Jian, Shengzhuo Wang, Yu Xia*, "Characterization of Oxidized Glycerophosphoethanolamines via Radical-Directed Dissociation Tandem Mass Spectrometry and the Paternò–Büchi Derivatization", Anal. Chem. 2023, 95, 25, 9422–9427.

https://doi.org/10.1021/acs.analchem.3c00792

40.  Tian Xia, Feng Zhou, Donghui Zhang, Xue Jin, Hengxue Shi, Hang Yin, Yanqing Gong, Yu Xia*, "Deep-profiling of phospholipidome via rapid orthogonal separations and isomer-resolved mass spectrometry", Nat. Commun., 202314, 4263.

https://doi.org/10.1038/s41467-023-40046-x

39.  Hengxue Shi, Zhenshu Tan, Xiangyu Guo, Hanlin Ren, Shengzhuo Wang, Yu Xia*, "Visible-Light Paternò–Büchi Reaction for Lipidomic Profiling at Detailed Structure Levels", Anal. Chem. 2023, 95, 11, 5117–5125.

https://doi.org/10.1021/acs.analchem.3c00085

38.  Wenpeng Zhang, Ruijun Jian, Jing Zhao, Yikun Liu, Yu Xia*, "Deep-lipidotyping by mass spectrometry: recent technical advances and applications", Journal of Lipid Research, 2022.

https://doi.org/10.1016/j.jlr.2022.100219

37.  Donghui Zhang, Qiaohong Lin, Tian Xia, Jing Zhao, Wenpeng Zhang, Zheng Ouyang* and Yu Xia*, "LipidOA: A Machine-Learning and Prior-Knowledge-Based Tool for Structural Annotation of Glycerophospholipids", Anal. Chem. 2022, 94, 48, 16759–16767.

https://doi.org/10.1021/acs.analchem.2c03505

36. Hai-Fang Li, Jing Zhao, Wenbo Cao, Wenpeng Zhang, Yu Xia*, and Zheng Ouyang*, “Site-Specific Photochemical Reaction for Improved C=C Location Analysis of Unsaturated Lipids by Ultraviolet Photodissociation” Research, 2022, Article ID 9783602, Published: 12 Feb 2022

https://doi.org/10.34133/2022/9783602

35. Xiaoxiao Ma, Wenpeng Zhang, Zishuai Li, Yu Xia* and Zheng Ouyang*, Enabling High Structural Specificity to Lipidomics by Coupling Photochemical Derivatization with Tandem Mass Spectrometry. Acc. Chem. Res. 2021, 54, 20, 3873–3882.

https://doi.org/10.1021/acs.accounts.1c00419

34. Zishuai Li, Simin Cheng, Qiaohong Lin, Wenbo Cao, Jing Yang, Minmin Zhang, Aijun Shen, Wenpeng Zhang, Yu Xia, Xiaoxiao Ma* and Zheng Ouyang*, "Single-cell lipidomics with high structural specificity by mass spectrometry" Nature Communications, 2021, 12, 2869.

https://doi.org/10.1038/s41467-021-23161-5

33. Qiaohong Lin, Pengyun Li, Mengxuan Fang, Donghui Zhang, and Yu Xia*, “Deep Profiling of Aminophospholipids Reveals a Dysregulated Desaturation Pattern in Breast Cancer Cell Lines” Anal. Chem. 2021, Publication Date:December 21

https://doi.org/10.1021/acs.analchem.1c03494

32. Jing Zhao, Mengxuan Fang, Yu Xia*, “A Liquid Chromatography-Mass Spectrometry Workflow for In-Depth Quantitation of Fatty Acid Double Bond Location Isomers”J. Lipid. Res. 2021, Available online 24 August .

https://doi.org/10.1016/j.jlr.2021.100110

31. Qingyuan Hu, Yu Xia*, Xiaoxiao Ma*, “Comprehensive Structural Characterization of Lipids by Coupling Paternò–Büchi Reaction and Tandem Mass Spectrometry”, In: Hsu FF. (eds) Mass Spectrometry-Based Lipidomics. Methods in Molecular Biology, vol 2306. Humana, New York, NY.

https://doi.org/10.1007/978-1-0716-1410-5_4

30. Tian Xia, Ming Yuan, Yongwei Xu, Feng Zhou, Kate Yu*, and Yu Xia*, “Deep Structural Annotation of Glycerolipids by the Charge-Tagging Paterno–Büchi Reaction and Supercritical Fluid Chromatography–Ion Mobility Mass Spectrometry", Anal. Chem. 2021, 93, 23, 8345–8353

https://pubs.acs.org/doi/10.1021/acs.analchem.1c01379

29. Hanlin Ren, Alexander Triebl, Sneha Muralidharan, Markus R. Wenk*, Yu Xia* and Federico Torta*, "Mapping the Distribution of Double Bond Location Isomers in Lipids across Mouse Tissues", Analyst, 2021,146, 3899-3907

https://doi.org/10.1039/D1AN00449B

28. X. Ma, Y. Xia, "Unsaturated Lipid Analysis via Coupling the Paternò–Büchi Reaction with ESI-MS/MS", Lipidomics. 2020: 148-174.

27. Xue Zhao, Gang Wu, Wenpeng Zhang, Mengqiu Dong, and Yu Xia*, "Resolving Modifications on Sphingoid Base and N-Acyl Chain of Sphingomyelin Lipids in Complex Lipid Extracts", Anal. Chem. 2020, 92, 21, 14775–14782

https://doi.org/10.1021/acs.analchem.0c03502

26. Jing Zhao, Xiaobo Xie, Qiaohong Lin, Xiaoxiao Ma, Pei Su, Yu Xia*, "Next-Generation Paternò–Büchi Reagents for Lipid Analysis by Mass Spectrometry", Anal. Chem. 2020, 92, 19, 13470–13477

https://pubs.acs.org/doi/10.1021/acs.analchem.0c02896

25. Elissia T. Franklin, Yu Xia*, "Structural elucidation of triacylglycerol using online acetone Paternò–Büchi reaction coupled with reversed-phase liquid chromatography mass spectrometry" , Analyst. 2020, 145, 6532-6540.

https://doi.org/10.1039/D0AN01353F

24. Elissia Franklin, Samuel Shields, Jeffrey Manthorpe, Jeffrey C. Smith, Yu Xia, Scott A. Mcluckey*, "Coupling Headgroup and Alkene Specific Solution Modifications with Gas-Phase Ion/Ion Reactions for Sensitive Glycerophospholipid Identification and Characterization", J. Am. Soc. Mass Spectrom. 2020, 31, 4, 938–945.

https://doi.org/10.1021/jasms.0c00001

23. Wenpeng Zhang*, Bing Shang, Zheng Ouyang, Yu Xia*, "Enhanced Phospholipid Isomer Analysis by Online Photochemical Derivatization and RPLC-MS", Anal. Chem. 2020, 92, 9, 6719–6726.

https://doi.org/10.1021/acs.analchem.0c00690

22. Tian Xia, Hanlin Ren, Wenpeng Zhang, Yu Xia*, "Lipidome-Wide Characterization of Phosphatidylinositols and Phosphatidylglycerols on C=C Location Level", Analytica Chimica Acta, 2020, 1128, 107-115.

http://dx.doi.org/10.1016/j.aca.2020.06.017

21. Wenbo Cao, Simin Cheng, Jing Yang, Wenpeng Zhang, Zishuai Li, Qinhua Chen, Yu Xia, Zheng Ouyang*, Xiaoxiao Ma*, "Large-scale lipid analysis with C=C location and sn-position isomer resolving power", Nat Commun, 2020, 11, 375.

https://www.nature.com/articles/s41467-019-14180-4

20. 马潇潇,胡清源,瑕瑜*, "Paternò-Büchi(PB)反应与串联质谱结合实现不饱和脂质精确结构解析", 分析测试学报, 2020, 39(1), 19-27.

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19. Xiaobo Xie, Jing Zhao, Miao Lin, Jinlan Zhang, Yu Xia*, "Profiling of Cholesteryl Esters by Coupling Charge Tagging Paternò-Büchi Reaction and Liquid Chromatography-Mass Spectrometry", Anal. Chem. 2020, 92, 12, 8487–8496.

https://doi.org/10.1021/acs.analchem.0c01241

18. Haifang Li, Wenbo Cao, Xiaoxiao Ma, Xiaobo Xie, Yu Xia, Zheng Ouyang*, "Visible-Light-Driven [2 + 2] Photocycloadditions between Benzophenone and C=C Bonds in Unsaturated Lipids", J. Am. Chem. Soc. 2020, 142, 7, 3499–3505.

https://doi.org/10.1021/jacs.9b12120

17. Wenpeng Zhang, Bing Shang, Yu Xia, "Comprehensive Characterization of Phospholipid Isomers in Human Platelets", J. Anal. Test., 2020, 4, 210–216.

https://link.springer.com/article/10.1007/s41664-020-00137-w

16. Q. Lin, D. Zhang, Y. Xia*, "Analysis of Ether Glycerophosphocholines at the Level of C=C Locations from Human Plasma", Analyst, 2020, 145, 513-522.

https://doi.org/10.1039/C9AN01515A

15. X. Zhao, W. Zhang, D. Zhang, X. Liu, W. Cao, Q. Chen, Z. Ouyang, Y. Xia*, "A Lipidomic Workflow Capable of Resolving sn- and C=C Location Isomers of Phosphatidylcholines", Chem. Science, 2019, 10, 10740-10748.

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14. Y. Su, J. Page, X. Ma, R. Shi, Y. Xia*, Zheng Ouyang*, "Mapping Lipid C=C Location Isomers in Organ Tissues by Coupling Photochemical Derivatization and Rapid Extractive Mass Spectrometry", Int. J. Mass Spectrom. 2019, 445, 116206

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13. Elissia T. Franklin, Stella K. Betancourt, Caitlin E. Randolph, Scott A. McLuckey* , and Yu Xia* ,"In-depth structural characterization of phospholipids by pairing solution photochemical reaction with charge inversion ion/ion chemistry",  Anal Bioanal Chem. 2019, 411, 4739–4749.

https://doi.org/10.1007/s00216-018-1537-1

12. R. Zou, W. Cao, L. Chong, W. Hua, H. Xu, Y. Mao, J. Page, R. Shi, Y. Xia, Tony Y. Hu, W. Zhang*, and Z. Ouyang*, "Point-of-Care Tissue Analysis Using Miniature Mass Spectrometer", Anal. Chem. 2019, 91, 1, 1157–1163

https://doi.org/10.1021/acs.analchem.8b04935

11. X. Xie, Y. Xia*, "Analysis of Conjugated Fatty Acid Isomers by the Paternò-Büchi Reaction and Trapped Ion Mobility Mass Spectrometry", Anal. Chem. 2019, 91, 7173-7180.

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10. W. Zhang, S. Chiang, Z. Li, Q. Chen, Y. Xia, Z. Ouyang*, "A Polymer Coating Transfer Enrichment for Direct Mass Spectrometry Analysis of Lipids in Biofluid Samples", Angew. Chem., Int. Ed., 2019, 58, 6064-6069.

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9. W. Zhang, D. Zhang, Q. Chen, J. Wu, Z. Ouyang*, Y. Xia*, "Online photochemical derivatization enables comprehensive mass spectrometric analysis of unsaturated phospholipid isomers", Nat. Commun., 2019, 10, 79.

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8. L. Chong, R. Tian, R. Shi, Z. Ouyang*, and Y. Xia*, "Coupling the Paternò-Büchi (PB) Reaction With Mass Spectrometry to Study Unsaturated Fatty Acids in Mouse Model of Multiple Sclerosis", Front. Chem. 2019, 7:807.

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7. F. Tang*, C. Guo, X. Ma, J. Zhang, Y. Su, R. Tian, R. Shi, Y. Xia, X. Wang, Z. Ouyang*, "Rapid in situ Profiling of Lipid C=C Location Isomers in Tissue Using Ambient Mass Spectrometry with Photochemical Reactions", Anal. Chem. 2018, 90, 5612-5619

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6. J. Li, S. Condello, J. T. Pepin, X. Ma, Y. Xia, T. D. Hurley, D. Matei*, and J. Cheng*, “Lipid Desaturation Is a Metabolic Marker and Therapeutic Target of Ovarian Cancer Stem Cells”, Cell Stem Cell, 2017, 20, 3, 301-314

https://doi.org/10.1016/j.stem.2016.11.004

5. J. Ren, E.T. Franklin, Y. Xia*, "Uncovering Structural Diversity of Unsaturated Fatty Acyls in Cholesteryl Esters via Photochemical Reaction and Tandem Mass Spectrometry", J. Am. Soc. Mass Spectrom. 2017, 28, 1432-1441

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4. X. Ma, X. Zhao, J. Li, W. Zhang, J.-X. Cheng, Z. Ouyang*, Y. Xia*, "Photochemical Tagging for Quantitation of Unsaturated Fatty Acids by Mass Spectrometry", Anal. Chem. 2016, 88, 8931–8935

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3. C. A. Stinson, Y. Xia*, "A Method of coupling Paternò-Büchi reaction with direct infusion ESI-MS/MS for locating C=C bond in glycerophospholipids", Analyst, 2016, 141, 3696-3704

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2. X. Ma, L. Chong, R. Tian, R. Shi, T. Y. Hu, Z. Ouyang*, Y. Xia*, "Identification and quantitation of lipid C=C location isomers: a shotgun lipidomics approach enabled by photochemical reaction", Proc. Natl. Acad. Sci. USA, 2016, 113, 2573-2578. Featured by C&E News and Nature Methods

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1. X. Ma and Y. Xia*, "Pinpointing Double Bonds in Lipids by Paternò–Büchi Reactions and Mass Spectrometry", Angew. Chem., Int. Ed, 2014, 53, 2592-2596.

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3. Advances of PB-MS/MS by other research groups around the world.(2017-2023)

53. Wang Z.; Garza S.; Li X.; Rahman M. S.; Brenna J. T.*; Wang D. H.^; Paternò–Büchi Reaction Mass Spectrometry Enables Positional Assignment of Polymethylene-Interrupted Double Bonds in Food-Derived Lipids. J. Agric. Food Chem. 2024.

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52. Chen M.; Wang R.; Ren Q. X.; Li B.; Li P.*; Yang H.*; Gao W.*; Analysis of unsaturated fatty acids by supercritical fluid chromatography tandem mass spectrometry coupled with online Paternò-Büchi reaction. Microchemical Journal. 2023, 109551.

https://doi.org/10.1016/j.microc.2023.109551

51. Guo X. Y.; Cao W. B.; Fan X. M.; Guo Z. Y.; Zhang D. H.; Zhang H. Y.; Ma X. X.; Dong J. H.; Wang Y. F. *; Zhang W. P. *; Ouyang Z.*; Tandem Mass Spectrometry Imaging Enables High Definition for Mapping Lipids in Tissues. Angew Chem Int Ed Engl. 2023, 62, 9, e202214804

https://doi.org/10.1002/anie.202214804

50. Cheng S. M.; Xie Z. N.; Hu Q. Y.; Qian Y.; Ma X. X.*; Familiarizing Undergraduate Students with Advanced Mass Spectrometry Techniques: An Example of Detailed Lipid Structure Characterization. J. Chem. Educ. 2023, 100, 3, 1270–1276.

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49. Cheng S. M.; Zhang D. H.; Feng J. X.; Hu Q. Y.; Tan A.; Xie Z. N.; Chen Q. H.; Huang H. M.; Wei Y.; Ouyang Z.*; Ma X. X.*; Metabolic Pathway of Monounsaturated Lipids Revealed by In-Depth Structural Lipidomics by Mass Spectrometry. Research, 2023, 6, 0087.

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48. Hu W. Y.; Han Y. H.*; Selective Characterization of Olefins by Paternò–Büchi Reaction with Ultrahigh Resolution Mass Spectrometry. Anal. Chem. 2023.

https://doi.org/10.1021/acs.analchem.3c02966

47. Freitas D. P.; Yan X.*; In situ droplet-based on-tissue chemical derivatization for lipid isomer characterization using LESA. Analytical and Bioanalytical Chemistry 2023, 415, 4197–4208.

https://doi.org/10.1007/s00216-023-04653-3

46. Lu H. Y.; Zhang H.; Li L. J.*; Chemical tagging mass spectrometry: an approach for single‑cell Omics. Analytical and Bioanalytical Chemistry. 2023.

https://doi.org/10.1007/s00216-023-04850-0

45. Kanter J. P.; Honold P. J.; Luh D.; Heiles S., Spengler B.; Fraatz M. A.; Zorn H.; Hammer A. K.*; Biocatalytic Production of Odor-Active Fatty Aldehydes from Fungal Lipids. J. Agric. Food Chem. 2023, 71, 21, 8112–8120

https://doi.org/10.1021/acs.jafc.3c01972

44. Wang D. H.; Brenna J. T.*, and Shchepinov M. S.*; Quantitative High-Field NMR- and Mass Spectrometry-Based Fatty Acid Sequencing Reveals Internal Structure in Ru-Catalyzed Deuteration of Docosahexaenoic Acid. Anal. Chem. 2022, 94, 38, 12971–12980.

https://doi.org/10.1021/acs.analchem.2c00923

43. Kanter J.P.; Honold P. J.; Lüke D.; Heiles S.; Spengler B.; Fraatz M. A.; Harms C.; Ley J. P.; Zorn H.; Hammer A. K.*; An enzymatic tandem reaction to produce odor-active fatty aldehydes. Appl. Microbiol. Biotechnol. 2022, 106, 6095–6107

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42. Bednařík A.*; Prysiazhnyi V.; Bezdeková D.; Soltwisch J.; Dreisewerd K.; Preisler J.*; Mass Spectrometry Imaging Techniques Enabling Visualization of Lipid Isomers in Biological Tissues. Anal. Chem. 2022, 94, 12, 4889–4900.

https://doi.org/10.1021/acs.analchem.1c05108

41. Bechtella L.; Walrant A.*; Structural Bases for the Involvement of Phosphatidylinositol-4,5-bisphosphate in the Internalization of the Cell-Penetrating Peptide Penetratin. ACS Chem. Biol. 2022, 17, 6, 1427–1439.

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40. Cerrato A.; Capriotti A. L.*; Novel Aza-Paternò-Büchi Reaction Allows Pinpointing Carbon–Carbon Double Bonds in Unsaturated Lipids by Higher Collisional Dissociation. Anal. Chem. 2022, 94, 38, 13117–13125.

https://doi.org/10.1021/acs.analchem.3c02966

39. Christiana M.;Kokotou M. G.*; Liquid Chromatography-Mass Spectrometry (LC-MS) Derivatization-Based Methods for the Determination of Fatty Acids in Biological Samples. Molecules 202227(17), 5717

https://doi.org/10.3390/molecules27175717

38. Sun C. L.*; Wan X.*; A novel on-tissue cycloaddition reagent for mass spectrometry imaging of lipid C=C position isomers in biological tissues. Chinese Chemical Letters 2022, 33, 2073-2076.

https://doi.org/10.1016/j.cclet.2021.08.034

37. Hynds H. M.;Hines K. M.*; Ion Mobility Shift Reagents for Lipid Double Bonds Based on Paternò–Büchi Photoderivatization with Halogenated Acetophenones. J. Am. Soc. Mass Spectrom. 2022, 33, 10, 1982–1989

https://doi.org/10.1021/jasms.2c00211

36. Chen Y. Y.; Xie C. Y.; Wang X. X.; Cao G. D.; Ru. Y.; Song Y. Y.; Iyaswamy A.; Li M.; Wang J. N.*; Cai Z. W.*; 3Acetylpyridine On-Tissue Paterno−Buchi Derivatization Enabling High Coverage Lipid C=C Location-Resolved MS Imaging in Biological Tissues. Analytical Chemistry, 2022.

https://doi.org/10.1021/acs.analchem.2c03089

35. Feng, G. F.; Gao, M.; Wang L.W.; Chen J. Y.; Hou M. L.; Wan Q. Q.; Lin Y.; Xu G. Y.; Qi X. T.; Chen S. M.*; Dual-resolving of positional and geometric isomers of C=C bonds via bifunctional photocycloaddition-photoisomerization reaction system. Nature Communications, 2022, 13, 2652

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34. Mao, R.; Li, W.; Ji, P.; Ding, H.; Teka, T.; Zhang, L.; Fu, Z.; Fu, X.; Kaushal, S.; Dou, Z.*; Han, L.*; An efficient and sensitive method on the identification of unsaturated fatty acids in biosamples: Total lipid extract from bovine liver as a case study. Journal of Chromatography A, 2022, 1675, 463176

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33. Sun, J.; Liu, R. X.; Li, S.; Li, W. *; M. L. Gross*; Nanoparticles and photochemistry for native-like transmembrane protein footprinting. Nature Communications, 2021, 12, 7270

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32. Han, Y.; Chen, P.; Li, Z.; Wang, X.; Sun, C. *; Multi-wavelength visible-light induced [2+2] cycloaddition for identification of lipid isomers in biological samples. Journal of Chromatography A, 2022, 1662, 462742

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31. Liu, Z.; S. Rochfort*; Regio-distribution and double bond locations of unsaturated fatty acids in phospholipids of bovine milk. Food Chemistry, 2021, Available online 2 November.

https://doi.org/10.1016/j.foodchem.2021.131515

30. Deng, J.; Yang, Y.*; Zeng, Z.; Xiao, X.; Li, J.; Luan, T.*; Discovery of Potential Lipid Biomarkers for Human Colorectal Cancer by In-Capillary Extraction Nanoelectrospray Ionization Mass Spectrometry. Analytical Chemistry, 2021, 93, 38, 13089–13098

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29. Zhang, J.; Guo, C.; Huo, X.; Ma, X.; Li, X.; Zeper, A.; Chu, Y.; Wang, X.; Tang, F.; Unsaturated lipid isomeric imaging based on the Paternò–Büchi reaction in the solid phase in ambient conditions. Talanta, 2021, 235, 122816.

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28. Sun, C; Ma, C; Li, L; Han, Y; Wang, D; Wan,X; "A novel on-tissue cycloaddition reagent for mass spectrometry imaging of lipid C=C position isomers in biological tissues", Chinese Chemical Letters, 2021, Available online 12 August.

https://doi.org/10.1016/j.cclet.2021.08.034

27. Huang, W.; Zhou. H.; Yuan, M.; Lan, L.; Hou, A.; Ji, S. Comprehensive Characterization of the Chemical Constituents in Platycodon Grandiflorum by an Integrated Liquid Chromatography-Mass Spectrometry Strategy. Journal of Chromatography A, 2021, 1654, 462-477.

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26. Yang Y. Coupling Paternò-Büchi Reaction with Ambient NanoESI-MS for Identification of Unsaturated Triacylglycerols in Peanut Oils. Journal of Chinese Mass Spectrometry Society, 2021, 42(4): 455-461.

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25. Wang, D.; Park, H.; Wang, Z.; Lacombe, R.S.; Shmanai, V.V.; Bekish, A.V.; Schmidt, K.; Shchepinov, M.S.; Brenna, J.T.“Toward Quantitative Sequencing of Deuteration of Unsaturated Hydrocarbon Chains in Fatty Acids" Analytical Chemistry, 2021, 93, 8238–8247

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24. Xu, S.; Lv, X.; Wu, B.; Xie, Y.; Wu, Z.; Tu, X.; Chen, H.; Wei, F. Pseudotargeted Lipidomics Strategy Enabling Comprehensive Profiling and Precise Lipid Structural Elucidation of Polyunsaturated Lipid-Rich Echium Oil. Journal of Agricultural and Food Chemistry, 2021

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23. Wäldchen, F.; Mohr, F.; Wagner, A.H.; Heiles, S. "Multifunctional reactive MALDI matrix enabling high-lateral resolution dual polarity MS imaging and lipid C= C position-resolved MS2 imaging." Analytical Chemistry. 2020, 92, 14130–14138

https://doi.org/10.1021/acs.analchem.0c03150

22. Jeck, V.; Froning, M.; Tiso, T.; Blank, L. M.; Hayen, H. "Double bond localization in unsaturated rhamnolipid precursors 3-(3-hydroxyalkanoyloxy) alkanoic acids by liquid chromatography–mass spectrometry applying online Paternò–Büchi reaction." Analytical and bioanalytical chemistry, 2020, 412, 5601-5613.

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21.Maddox, S. W., Olsen, S. S., Velosa, D. C., Burkus-Matesevac, A., Peverati, R., & Chouinard, C. D. Improved Identification of Isomeric Steroids using the Paternò-Büchi Reaction with Ion Mobility-Mass Spectrometry. Journal of the American Society for Mass Spectrometry, 2020, 31, 2086–2092

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20. Xu, S.; Wei, F.; Xie, Y.; Wu, B.; Lv, X.; Qin, Z.; Chen, H. Localisation of C=C Bond and Absolute Quantification of Unsaturated Fatty Acids in Vegetable Oils based on Photochemical Derivatisation Reaction Coupled with Mass Spectrometry. International Journal of Food Science & Technology, 2020, 55,  2883-2892

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19. Li, P.; Deng, J.; Xiao, N.; Cai, X.; Wu, Q.; Lu, Z.; Du, B. "Identification of polyunsaturated triacylglycerols and CC location isomers in sacha inchi oil by photochemical reaction mass spectrometry combined with nuclear magnetic resonance spectroscopy." Food chemistry, 2020, 307, 125568.

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18. Zhu, Y.; Wang, W.; Yang, Z. "Combining Mass Spectrometry with Paternò-Büchi Reaction to Determine Double-bond Positions in Lipids at the Single-cell Level." Analytical Chemistry, 2020, 92, 11380–11387

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17. Xu, S.; Wu, B.; Oresic, M.; Xie, Y.; Yao, P.; Wu, Z.; Wei, F. "Double Derivatization Strategy for High-Sensitivity and High-Coverage Localization of Double Bonds in Free Fatty Acids by Mass Spectrometry." Analytical Chemistry, 2020, 92, 6446-6455.

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16. Feng, G.; Hao, Y.; Wu, L.; Chen, S. "A visible-light activated [2+ 2] cycloaddition reaction enables pinpointing carbon–carbon double bonds in lipids." Chemical Science, 2020, 11, 7244-7251.

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15. Esch, P.; Heiles, S. "Investigating C=C Positions and Hydroxylation Sites in Lipids Using Paternò–Büchi Functionalization Mass Spectrometry." Analyst, 2020, 145, 2256-2266.

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14. Wäldchen, F.; Spengler, B.; Heiles, S. "Reactive Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry Imaging Using an Intrinsically Photoreactive Paternò–Büchi Matrix for Double-Bond Localization in Isomeric Phospholipids." Journal of the American Chemical Society, 2019, 141, 11816-11820.

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13. Deng, J.; Yang, Y.; Liu, Y.; Fang, L.; Lin, L.; Luan, T. "Coupling Paternò-Büchi Reaction with Surface-Coated Probe Nanoelectrospray Ionization Mass Spectrometry for In Vivo and Microscale Profiling of Lipid C═ C Location Isomers in Complex Biological Tissues." Analytical chemistry, 2019, 91, 4592-4599.

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12. Esch, P.; Fischer, M.; Heiles, S.; Schäfer, M. "Olefinic Reagents Tested for Peptide Derivatization with Switchable Properties: Stable upon Collision Induced Dissociation and Cleavable by In-Source Paternò-Büchi Reactions." Journal of Mass Spectrometry, 2019, 54, 976-986.

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11. Birk, F.; Fraatz, M. A.; Esch, P.; Heiles, S.; Pelzer, R.; Zorn, H. "Industrial Riboflavin Fermentation Broths Represent a Diverse Source of Natural Saturated and Unsaturated Lactones." Journal of Agricultural and Food Chemistry, 2019, 67, 13460-13469.

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10. Zhao, X.; Chen, J.; Zhang, W.; Yang, C.; Ma, X.; Zhang, S.; Zhang, X. "Lipid Alterations during Zebrafish Embryogenesis Revealed by Dynamic Mass Spectrometry Profiling with C=C Specificity." Journal of The American Society for Mass Spectrometry, 2019, 30, 2646-2654.

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9. Bednařík, A.; Bölsker, S.; Soltwisch, J.; Dreisewerd, K., "An On-Tissue Paternò–Büchi Reaction for Localization of Carbon–Carbon Double Bonds in Phospholipids and Glycolipids by Matrix-Assisted Laser-Desorption–Ionization Mass-Spectrometry Imaging." Angewandte Chemie International Edition, 2018, 57, 12092-12096.

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8. Jeck, V.; Korf, A.; Vosse, C.; Hayen, H. "Localization of Double-Bond Positions in Lipids by Tandem Mass Spectrometry Succeeding High-Performance Liquid Chromatography with Post-Column Derivatization." Rapid Communications in Mass Spectrometry, 2019, 33, 86-94.

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2. Murphy, R. C.; Okuno, T.; Johnson, C. A.; Barkley, R. M. "Determination of double bond positions in polyunsaturated fatty acids using the photochemical Paterno-Buchi reaction with acetone and tandem mass spectrometry." Analytical Chemistry, 2017, 89, 8545-8553.

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