钙离子和镁离子浓度变化对磷脂酰乙醇胺-磷脂酰甘油双分子层膜的影响

doi:10.3866/PKU.WHXB201811016

物理化学学报 >> 2019, Vol. 35 >> Issue (8): 840-849.doi: 10.3866/PKU.WHXB201811016

钙离子和镁离子浓度变化对磷脂酰乙醇胺-磷脂酰甘油双分子层膜的影响

张涛¹,仇运广^2,³,罗启超²,程曦²,赵丽芬²,严昕^2,⁴,彭浡²,蒋华良^1,^2,^3,*(),阳怀宇^2,^3,*()

¹ 华东理工大学药学院，上海 200237
² 中国科学院上海药物研究所，新药研究国家重点实验室药物发现与设计中心，上海 201203
³ 中国科学院大学，北京 100049
⁴ 上海科技大学生命科学与技术学院，上海 201210

收稿日期:2018-11-12 录用日期:2018-12-31 发布日期:2019-01-03
通讯作者: 蒋华良,阳怀宇 E-mail:hljiang@simm.ac.cn;hyyang@simm.ac.cn
基金资助:
国家自然科学基金(21422208);国家自然科学基金委-广东省政府联合基金(第三期)超级计算科学应用研究专项(U1501501)

Concentration Dependent Effects of Ca²⁺ and Mg²⁺ on the Phosphatidylethanolamine-Phosphatidylglycerol Bilayer

Tao ZHANG¹,Yunguang QIU^2,³,Qichao LUO²,Xi CHENG²,Lifen ZHAO²,Xin YAN^2,⁴,Bo PENG²,Hualiang JIANG^1,^2,^3,*(),Huaiyu YANG^2,^3,*()

¹ School of Pharmacy, East China University of Science and Technology, Shanghai 200237, P. R. China
² Drug Discovery and Design Center, State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Science, Shanghai 201203, P. R. China
³ University of Chinese Academy of Sciences, Beijing 100049, P. R. China
⁴ School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, P. R. China

Received:2018-11-12 Accepted:2018-12-31 Published:2019-01-03
Contact: Hualiang JIANG,Huaiyu YANG E-mail:hljiang@simm.ac.cn;hyyang@simm.ac.cn
Supported by:
the National Natural Science Foundation of China(21422208);the Special Program for Applied Research on Super Computation of the Applied Research on Super Computation of the NSFC-Guangdong Joint Fund(U1501501)

摘要/Abstract

摘要：

钙离子和镁离子是生物细胞中重要的二价阳离子，对生物膜结构保持和功能行使发挥重要作用。但至今，对两种阳离子在不同浓度下与大肠杆菌内膜相互作用的认识仍存在局限。本文采用动态光散射(DLS)、zeta电势实验、全原子分子动力学模拟(AA-MD)，定量研究了不同浓度的钙离子和镁离子对混合磷脂双分子层膜(1-棕榈酰基-2-油酰基-sn-丙三基-3-磷酸乙醇胺(POPE) : 1-棕榈酰基-2-油酰基-sn-丙三基-3-磷酸甘油(POPG)的摩尔比为3 : 1)模拟的大肠杆菌内膜的影响。DLS结果表明，在0和1 mmol∙L^-1钙离子或镁离子溶液中，POPE/POPG脂质体为均匀的单分散体系。当两种离子浓度分别提高到5-100 mmol∙L^-1范围时，单室脂质体间发生脂分子聚集或脂质体融合事件。Zeta电势数据表明，钙离子或镁离子对电负性的POPE/POPG脂质体均有电荷反转效果。AA-MD模拟计算结果表明，当模拟时间超过100 ns时，各浓度的钙离子稳定地吸附在磷脂双分子层膜上，而镁离子动态地吸附/解吸附于磷脂膜，这些结果与DLS和zeta电势实验基本吻合。同时，通过计算径向分布函数，分析了0、5、100 mmol∙L^-1浓度溶液中POPE和POPG的磷酸、羰基和羟基基团氧原子的第一配位壳层中的钙离子或镁离子的平均配位数目，结果表明两种离子主要结合在POPE和POPG电负性的磷酸基团上，因此可以解释DLS实验中钙离子或镁离子对POPE/POPG脂质体的电荷反转现象。另外，随着离子浓度的增高，钙离子减小了磷脂双分子层膜的单个磷脂面积，同时使膜的厚度增大，而镁离子对膜的两种参数影响较小。同时，相同浓度条件下两种离子对膜中磷脂分子的取向影响不同。这些模拟结果可在原子水平上解释DLS和zeta电势实验中钙离子和镁离子对POPE/POPG脂质体的不同影响。本文的实验和分子动力学模拟结果可以解释一些与二价阳离子调控相关的生物学过程，例如，膜融合。

关键词: 二价阳离子, 磷脂双分子层, 动态光散射, Zeta电势, 分子动力学模拟, 相互作用

Abstract:

Ca²⁺ and Mg²⁺ ions are the main divalent cations in living cells and play vital roles in the structure and function of biological membranes. To date, the differences in the effects of these two ions on the Escherichia coli (E. coli) inner membrane at various concentrations remain unknown. Here, the effects of Ca²⁺ and Mg²⁺ ions on a mixed lipid bilayer composed of 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphoethanolamine (POPE) and 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphoglycerol (POPG) in a 3 : 1 ratio (mol/mol), which mimics the E. coli inner membrane, were quantitatively differentiated at different concentrations by dynamic light scattering (DLS), zeta potential measurements and all-atom molecular dynamics (AA-MD) simulations. The DLS results demonstrated that the POPE/POPG liposomes were homogeneous and monodisperse in solutions with Ca²⁺ or Mg²⁺ ion concentrations of 0 and 1 mmol∙L^-1. As the Ca²⁺ or Mg²⁺ ion concentration was increased to 5-100 mmol∙L^-1, lipid aggregation or the fusion of unilamellar liposomes occurred in the ion solutions. The zeta potential measurements showed that both the Ca²⁺ and Mg²⁺ ions had overcharging effects on the negatively charged POPE/POPG liposomes. The AA-MD simulation results indicated that the Ca²⁺ ions irreversibly adsorbed on the membranes when the simulation time was longer than 100 ns, while the Mg²⁺ ions were observed to dynamically adsorb on and desorb from the membranes at various concentrations. These results are consistent with the DLS and zeta potential experiments. The average numbers of Ca²⁺ and Mg²⁺ ions in the first coordination shell of the oxygen atoms of the phosphate, carbonyl and hydroxyl groups of POPE and POPG (i.e., the first coordination numbers) in the pure membrane and membranes containing 5 and 100 mmol∙L^-1 ions were calculated from the radial distribution functions. The results indicated that the primary binding site of these two ions on POPE and POPG at the concentrations studied was the negatively charged phosphate group. Thus, these results might explain the overcharging effects of both the Ca²⁺ and Mg²⁺ ions on the POPE/POPG liposomes. Moreover, as the Ca²⁺ concentration increased, the area per lipid of the lipid bilayers decreased, and the membrane thickness increased, while the Mg²⁺ ions had negligible effects on these membrane parameters. In addition, these ions had different effects on the orientation of the lipid head groups. These simulation results may be used to provide the possible explanations for the differences between Ca²⁺ and Mg²⁺ ions in DLS and zeta potential measurements at the atomic level. The experimental results and MD simulations provide insight into various biological processes regulated by divalent cations, such as membrane fusion.

Key words: Divalent cation, Lipid bilayers, Dynamic light scattering, Zeta potential, Molecular dynamics simulation, Interaction

张涛,仇运广,罗启超,程曦,赵丽芬,严昕,彭浡,蒋华良,阳怀宇. 钙离子和镁离子浓度变化对磷脂酰乙醇胺-磷脂酰甘油双分子层膜的影响[J]. 物理化学学报, 2019, 35(8), 840-849. doi: 10.3866/PKU.WHXB201811016

Tao ZHANG,Yunguang QIU,Qichao LUO,Xi CHENG,Lifen ZHAO,Xin YAN,Bo PENG,Hualiang JIANG,Huaiyu YANG. Concentration Dependent Effects of Ca²⁺ and Mg²⁺ on the Phosphatidylethanolamine-Phosphatidylglycerol Bilayer[J]. Acta Physico-Chimica Sinica 2019, 35(8), 840-849. doi: 10.3866/PKU.WHXB201811016

链接本文: https://www.whxb.pku.edu.cn/CN/10.3866/PKU.WHXB201811016

https://www.whxb.pku.edu.cn/CN/Y2019/V35/I8/840

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Groups	POPE/POPG bilayers
Groups	5 mmol∙L^-1 CaCl₂	100 mmol∙L^-1 CaCl₂	5 mmol∙L^-1 MgCl₂	100 mmol∙L^-1 MgCl₂
POPE PO4	0.018	0.347	0.003	0.068
POPE Sn-2 C＝O	0	0	0	0
POPE Sn-1 C＝O	0	0.006	0	0.006
POPG PO4	0.037	0.0426	0.003	0.094
POPG Sn-2 C＝O	0	0.019	0	0.019
POPG Sn-1 C＝O	0	0.002	0	0
POPG-OH	0	0.017	0	0.037

System	Apl/nm²	h/nm
POPE/POPG	0.56 ± 0.01	4.25 ± 0.06
POPE/POPG-5 mmol∙L^-1 Ca²⁺	0.57 ± 0.01	4.21 ± 0.05
POPE/POPG-50 mmol∙L^-1 Ca²⁺	0.51 ± 0.02	4.51 ± 0.11
POPE/POPG-100 mmol∙L^-1 Ca²⁺	0.48 ± 0.01	4.69 ± 0.04
POPE/POPG-5 mmol∙L^-1 Mg²⁺	0.57 ± 0.01	4.19 ± 0.06
POPE/POPG-50 mmol∙L^-1 Mg²⁺	0.56 ± 0.01	4.26 ± 0.07
POPE/POPG-100 mmol∙L^-1 Mg²⁺	0.55 ± 0.01	4.28 ± 0.08

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钙离子和镁离子浓度变化对磷脂酰乙醇胺-磷脂酰甘油双分子层膜的影响

Concentration Dependent Effects of Ca²⁺ and Mg²⁺ on the Phosphatidylethanolamine-Phosphatidylglycerol Bilayer

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钙离子和镁离子浓度变化对磷脂酰乙醇胺-磷脂酰甘油双分子层膜的影响

Concentration Dependent Effects of Ca2+ and Mg2+ on the Phosphatidylethanolamine-Phosphatidylglycerol Bilayer

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Concentration Dependent Effects of Ca²⁺ and Mg²⁺ on the Phosphatidylethanolamine-Phosphatidylglycerol Bilayer