Effect of Shiga Toxin on Inhomogeneous Biological Membrane Structure Determined by Small-Angle Scattering

Inhomogeneous structure occurring in biological membranes being rich in glycosphingolipids (GSL) has been proposed as an important phenomenon involved in the cellular endocytosis process. However, little is known about the correlation between the formation of microdomains and the GSL-dependent bioge...

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Main Authors: Shuyang Tu, Haijiao Zhang, Yawen Li, Yongchao Zhang, Qiang Tian, László Almásy, Xianhui Xu, Rongguang Zhang, Aihua Zou, Na Li
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:Applied Sciences
Subjects:
Online Access:https://www.mdpi.com/2076-3417/11/15/6965
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spelling doaj-08dcda56fa324d8ea3ff8a4d6645f10b2021-08-06T15:19:18ZengMDPI AGApplied Sciences2076-34172021-07-01116965696510.3390/app11156965Effect of Shiga Toxin on Inhomogeneous Biological Membrane Structure Determined by Small-Angle ScatteringShuyang Tu0Haijiao Zhang1Yawen Li2Yongchao Zhang3Qiang Tian4László Almásy5Xianhui Xu6Rongguang Zhang7Aihua Zou8Na Li9National Facility for Protein Science in Shanghai, Zhangjiang Lab, Shanghai Advanced Research Institute, CAS, No.333, Haike Road, Shanghai 201210, ChinaState Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, No.320, Yueyang Road, Shanghai 200031, ChinaDepartment of Chemistry, Qilu Normal University, Jinan 250013, ChinaCollege of Chemistry and Materials Science, Shanghai Normal University, Shanghai 200234, ChinaState Key Laboratory of Environment-Friendly Energy Materials, Southwest University of Science and Technology, Mianyang 621010, ChinaCentre for Energy Research, Institute for Energy Security and Environmental Safety, Konkoly-Thege Str. 29–33, 1121 Budapest, HungaryNational Facility for Protein Science in Shanghai, Zhangjiang Lab, Shanghai Advanced Research Institute, CAS, No.333, Haike Road, Shanghai 201210, ChinaState Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, No.320, Yueyang Road, Shanghai 200031, ChinaCollege of Chemistry and Materials Science, Shanghai Normal University, Shanghai 200234, ChinaNational Facility for Protein Science in Shanghai, Zhangjiang Lab, Shanghai Advanced Research Institute, CAS, No.333, Haike Road, Shanghai 201210, ChinaInhomogeneous structure occurring in biological membranes being rich in glycosphingolipids (GSL) has been proposed as an important phenomenon involved in the cellular endocytosis process. However, little is known about the correlation between the formation of microdomains and the GSL-dependent biogenesis for tubular endocytic pits occurred on the surface of the cellular membrane. In the present work, the interaction between the bacterial Shiga toxin from Escherichia coli (STxB) and its cellular receptor GSL globotriaosylceramide (Gb3) were studied using small unilamellar vesicle (SUV). The model membrane invagination induced by STxB was determined by the contrast variation small-angle neutron scattering (SANS) and the synchrotron radiation facility based small-angle X-ray scattering (SR-SAXS). The results revealed that Gb3 molecules provided the binding sites for STxB, inducing increased membrane fluctuation. The formation of protein–lipid complex (STxB-Gb3) apparently induced the thinning of model membrane with the thickness decreased from 3.10 nm to 2.50 nm. It is the first time to successfully characterize the mesoscopic change on membrane thickness upon GSL-dependent endocytic process using a small-angle scattering technique. Overall, this paper provided a practical method to quantify the inhomogeneous biological membrane structures, which is important to understand the cellular endocytosis process.https://www.mdpi.com/2076-3417/11/15/6965glycosphingolipidsmembrane microdomainsclathrin-independent endocytosissmall-angle scattering
collection DOAJ
language English
format Article
sources DOAJ
author Shuyang Tu
Haijiao Zhang
Yawen Li
Yongchao Zhang
Qiang Tian
László Almásy
Xianhui Xu
Rongguang Zhang
Aihua Zou
Na Li
spellingShingle Shuyang Tu
Haijiao Zhang
Yawen Li
Yongchao Zhang
Qiang Tian
László Almásy
Xianhui Xu
Rongguang Zhang
Aihua Zou
Na Li
Effect of Shiga Toxin on Inhomogeneous Biological Membrane Structure Determined by Small-Angle Scattering
Applied Sciences
glycosphingolipids
membrane microdomains
clathrin-independent endocytosis
small-angle scattering
author_facet Shuyang Tu
Haijiao Zhang
Yawen Li
Yongchao Zhang
Qiang Tian
László Almásy
Xianhui Xu
Rongguang Zhang
Aihua Zou
Na Li
author_sort Shuyang Tu
title Effect of Shiga Toxin on Inhomogeneous Biological Membrane Structure Determined by Small-Angle Scattering
title_short Effect of Shiga Toxin on Inhomogeneous Biological Membrane Structure Determined by Small-Angle Scattering
title_full Effect of Shiga Toxin on Inhomogeneous Biological Membrane Structure Determined by Small-Angle Scattering
title_fullStr Effect of Shiga Toxin on Inhomogeneous Biological Membrane Structure Determined by Small-Angle Scattering
title_full_unstemmed Effect of Shiga Toxin on Inhomogeneous Biological Membrane Structure Determined by Small-Angle Scattering
title_sort effect of shiga toxin on inhomogeneous biological membrane structure determined by small-angle scattering
publisher MDPI AG
series Applied Sciences
issn 2076-3417
publishDate 2021-07-01
description Inhomogeneous structure occurring in biological membranes being rich in glycosphingolipids (GSL) has been proposed as an important phenomenon involved in the cellular endocytosis process. However, little is known about the correlation between the formation of microdomains and the GSL-dependent biogenesis for tubular endocytic pits occurred on the surface of the cellular membrane. In the present work, the interaction between the bacterial Shiga toxin from Escherichia coli (STxB) and its cellular receptor GSL globotriaosylceramide (Gb3) were studied using small unilamellar vesicle (SUV). The model membrane invagination induced by STxB was determined by the contrast variation small-angle neutron scattering (SANS) and the synchrotron radiation facility based small-angle X-ray scattering (SR-SAXS). The results revealed that Gb3 molecules provided the binding sites for STxB, inducing increased membrane fluctuation. The formation of protein–lipid complex (STxB-Gb3) apparently induced the thinning of model membrane with the thickness decreased from 3.10 nm to 2.50 nm. It is the first time to successfully characterize the mesoscopic change on membrane thickness upon GSL-dependent endocytic process using a small-angle scattering technique. Overall, this paper provided a practical method to quantify the inhomogeneous biological membrane structures, which is important to understand the cellular endocytosis process.
topic glycosphingolipids
membrane microdomains
clathrin-independent endocytosis
small-angle scattering
url https://www.mdpi.com/2076-3417/11/15/6965
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