Effect of phosphatidylcholine regioisomerism on lateral segregation of milk sphingomyelin in bilayer membranes

IF 3.4 3区生物学 Q2 BIOCHEMISTRY & MOLECULAR BIOLOGY

Chemistry and Physics of Lipids Pub Date : 2024-09-24 DOI:10.1016/j.chemphyslip.2024.105445

Md Abdullah Al Sazzad , Max Lönnfors , Baoru Yang

{"title":"Effect of phosphatidylcholine regioisomerism on lateral segregation of milk sphingomyelin in bilayer membranes","authors":"Md Abdullah Al Sazzad , Max Lönnfors , Baoru Yang","doi":"10.1016/j.chemphyslip.2024.105445","DOIUrl":null,"url":null,"abstract":"<div><div>Milk fat globule membrane (MFGM) promotes the lateral phase separation of milk lipids and stabilizes the fat globules in milk. The composition and structures of lipids have a significant impact on physicochemical properties of MFGM, which in turn influences the digestion and absorption of milk lipids. Phospholipids (PL), sphingolipids, and cholesterol are the major lipid constituents of MFGM. While the effects of the head-group and structure of the fatty acids (FAs) on membrane properties are commonly studied, little is known on the impact of PL regioisomerism. The present study investigated the impact of phosphatidylcholine (PC) regioisomerism on lateral segregation of milk-sphingomyelin (milk-SM) as well as the influence on the interaction of milk-SM with ceramide and cholesterol in simulated membrane systems. The regioisomer pairs of four molecular species PC 16:0/18:1n-9, PC 16:0/18:2n-6, PC 16:0/18:3n-3, and PC 16:0/20:4n-6 were included in this study. The lateral segregation was determined using lifetime analysis of <em>trans-</em>parinaric acid (<em>tPA</em>) fluorescence. Thermostability of the domains was detected using steady-state anisotropy of <em>tPA.</em> Our results demonstrated a clear impact of PC regioisomerism on membrane properties. PC regioisomers having the unsaturated FAs at the <em>sn</em>-2 position enhanced the lateral segregation of milk-SM with and without the presence of ceramide and cholesterol compared to the regioiosmers having 16:0 at the <em>sn</em>-2 position. Furthermore, the characteristics i. e. the acyl chain length and degree of unsaturation of <em>sn</em>-2 FA of the PCs had a major impact on the milk-SM gel phase and the intermolecular forces between milk-SM and ceramide/cholesterol. This work is the first investigation showing the effect of PL regioisomerism on milk-SM domains, which might have significant influence on functional properties of MFGM.</div></div>","PeriodicalId":275,"journal":{"name":"Chemistry and Physics of Lipids","volume":"265 ","pages":"Article 105445"},"PeriodicalIF":3.4000,"publicationDate":"2024-09-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Chemistry and Physics of Lipids","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0009308424000707","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}

引用次数: 0

Abstract

Milk fat globule membrane (MFGM) promotes the lateral phase separation of milk lipids and stabilizes the fat globules in milk. The composition and structures of lipids have a significant impact on physicochemical properties of MFGM, which in turn influences the digestion and absorption of milk lipids. Phospholipids (PL), sphingolipids, and cholesterol are the major lipid constituents of MFGM. While the effects of the head-group and structure of the fatty acids (FAs) on membrane properties are commonly studied, little is known on the impact of PL regioisomerism. The present study investigated the impact of phosphatidylcholine (PC) regioisomerism on lateral segregation of milk-sphingomyelin (milk-SM) as well as the influence on the interaction of milk-SM with ceramide and cholesterol in simulated membrane systems. The regioisomer pairs of four molecular species PC 16:0/18:1n-9, PC 16:0/18:2n-6, PC 16:0/18:3n-3, and PC 16:0/20:4n-6 were included in this study. The lateral segregation was determined using lifetime analysis of trans-parinaric acid (tPA) fluorescence. Thermostability of the domains was detected using steady-state anisotropy of tPA. Our results demonstrated a clear impact of PC regioisomerism on membrane properties. PC regioisomers having the unsaturated FAs at the sn-2 position enhanced the lateral segregation of milk-SM with and without the presence of ceramide and cholesterol compared to the regioiosmers having 16:0 at the sn-2 position. Furthermore, the characteristics i. e. the acyl chain length and degree of unsaturation of sn-2 FA of the PCs had a major impact on the milk-SM gel phase and the intermolecular forces between milk-SM and ceramide/cholesterol. This work is the first investigation showing the effect of PL regioisomerism on milk-SM domains, which might have significant influence on functional properties of MFGM.

查看原文本刊更多论文

磷脂酰胆碱区域异构性对双层膜中牛奶鞘磷脂横向分离的影响

牛奶脂肪球膜（MFGM）可促进牛奶脂质的横向相分离，并稳定牛奶中的脂肪球。脂质的组成和结构对牛奶脂肪球膜的理化性质有重要影响，进而影响牛奶脂质的消化和吸收。磷脂（PL）、鞘脂和胆固醇是乳脂微球的主要脂质成分。虽然人们通常研究脂肪酸（FAs）的头基和结构对膜特性的影响，但对磷脂的再生异构体的影响却知之甚少。本研究调查了磷脂酰胆碱（PC）的 Regioisomerism 对牛奶-鞘磷脂（牛奶-SM）横向分离的影响，以及在模拟膜系统中牛奶-SM 与神经酰胺和胆固醇相互作用的影响。这项研究包括了四种分子物种的区域异构体对：PC 16:0/18:1n-9、PC 16:0/18:2n-6、PC 16:0/18:3n-3和PC 16:0/20:4n-6。横向分离是通过反式天冬氨酸（tPA）荧光的寿命分析确定的。利用 tPA 的稳态各向异性检测了结构域的热稳定性。我们的研究结果表明，PC 重组异构体对膜特性有明显的影响。与sn-2位为16:0的重组聚糖相比，sn-2位为不饱和脂肪酸的PC重组异构体在存在或不存在神经酰胺和胆固醇的情况下都能增强牛奶-SM的横向分离。此外，多氯化萘的特征（即酰基链长度和 sn-2 FA 的不饱和程度）对牛奶-SM 的凝胶相以及牛奶-SM 与神经酰胺/胆固醇之间的分子间作用力有重大影响。这项研究首次显示了聚乳酸的区域异构性对牛奶-SM 结构域的影响，这可能会对 MFGM 的功能特性产生重大影响。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Chemistry and Physics of Lipids 生物-生化与分子生物学

CiteScore

7.60

自引率

2.90%

发文量

审稿时长

40 days

期刊介绍： Chemistry and Physics of Lipids publishes research papers and review articles on chemical and physical aspects of lipids with primary emphasis on the relationship of these properties to biological functions and to biomedical applications. Accordingly, the journal covers: advances in synthetic and analytical lipid methodology; mass-spectrometry of lipids; chemical and physical characterisation of isolated structures; thermodynamics, phase behaviour, topology and dynamics of lipid assemblies; physicochemical studies into lipid-lipid and lipid-protein interactions in lipoproteins and in natural and model membranes; movement of lipids within, across and between membranes; intracellular lipid transfer; structure-function relationships and the nature of lipid-derived second messengers; chemical, physical and functional alterations of lipids induced by free radicals; enzymatic and non-enzymatic mechanisms of lipid peroxidation in cells, tissues, biofluids; oxidative lipidomics; and the role of lipids in the regulation of membrane-dependent biological processes.