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Poly-L-lysine induced shape change of negatively charged giant vesicles

Sheng Jie Wang Kai-Yu Ma Bei-Bei Zhu Tao Jiang Zhong-Ying

Poly-L-lysine induced shape change of negatively charged giant vesicles

Sheng Jie, Wang Kai-Yu, Ma Bei-Bei, Zhu Tao, Jiang Zhong-Ying
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  • Decoration of biomembrane with polymer may improve its physical properties, biocompatibility, and stability. In this study, we employ the inverted fluorescence microscopy to characterize the polylysine (PLL) induced shape transformation of the negatively charged giant unilamellar vesicles (GUVs) in low ionic medium. It is found that PLL may be adsorbed to the 1, 2-dioleoyl-sn-glycero-3-phosphocholine (DOPC) and 1, 2-dioleoyl-sn-glycero-3-phosphatidic acid (DOPA) binary mixture vesicles, resulting in the attachment between the membranes, the formation of the ropes, and rupture of the GUVs. The response of GUVs generally is enhanced with the increase of the negatively charged DOPA in the membranes. The experimental observations are concluded as follows. Firstly, for the PLL induced attachment of GUVs, the attachment area grows gradually with time. Secondly, ropes can only be found in relatively large GUVs. However, the hollow structure is not discernable from the fluorescence imaging. Thirdly, after the rupture of GUVs, some phase-separated-like highly fluorescence lipid domains form in the adjacent intact vesicles. Through careful discussion and analysis, we show that on the one hand, the positively charged PLL adheres to the negatively charged membrane surface, bridging the neighboring GUVs and drawing the originally electrical repulsive vesicles together. The contact zone between GUVs expands with the increasing adsorption of PLL in this area. And the local high fluorescence areas in the GUVs originate from the PLL induced membrane attachment as well. Some membrane segments from ruptured vesicles are adsorbed to the particular areas of GUV, forming a few lipid patch structures above the latter membrane. On the other hand, PLL is adsorbed to the membrane area enriched in the negatively charged DOPA, reversing the surface charge of the upper leaflet and deteriorating the stability of the lipid bilayer. The original equilibrium of the system is broken by the change of the electrical interaction between the neighboring lipid domains as well as the interaction between the domain and water-dispersed PLL. The lipid packing density and inter-lipid force are affected by the PLL adsorption. Lipid membranes have to bud to release the stress built in the spontaneous curvature incompatibility in the two leaflets. The system may become stable again after buds grown into rods with a certain length. All in all, this study deepens the understanding of the interaction mechanism between lipid membrane and oppositely charged polymer. The conclusions obtained will provide valuable reference for the further studies on the polymer-GUV application areas including drug delivery, control release, cell deformation, micro-volume reaction, and gene therapy.
      Corresponding author: Zhu Tao, zhuttd@163.com;jiangzhying@163.com ; Jiang Zhong-Ying, zhuttd@163.com;jiangzhying@163.com
    • Funds: Project supported by the National Natural Science Foundation of China (Grant Nos. 11464047, 21764015, 11474155, 11774147), the Fundamental Research Funds for the Central Universities, China, the Youth Science and Technology Innovation Talents Training Project of the Autonomous Region, China (Grant No. QN2016YX0504), and the Scientific Research Project of Yili Normal University, China (Grant No. 2013YSYB19).
    [1]

    Yang K, Ma Y Q 2010 Nat. Nanotech. 5 579

    [2]

    Ding H M, Tian W D, Ma Y Q 2012 ACS Nano 6 1230

    [3]

    Tahara K, Tadokoro S, Kawashima Y, Hirashima N 2012 Langmuir 28 7114

    [4]

    Jiang Z Y, Zhang G L, Ma J, Zhu T 2013 Acta Phys. Sin. 62 018701 (in Chinese) [蒋中英, 张国梁, 马晶, 朱涛 2013 物理学报 62 018701]

    [5]

    Ge L, Mhwald H, Li J 2003 Colloid. Surf. A 221 49

    [6]

    Brown K L, Conboy J C 2011 J. Am. Chem. Soc. 133 8794

    [7]

    Zhu T, Jiang Z Y, Ma Y Q, Hu Y 2016 ACS Appl. Mater. Interfaces 8 5857

    [8]

    Lee I C, Wu Y C 2014 ACS Appl. Mater. Interfaces 6 14439

    [9]

    Ding L, Chi E Y, Chemburu S 2009 Langmuir 25 13742

    [10]

    Burke S E, Barrett C J 2003 Biomacromolecules 4 1773

    [11]

    Tabaei S R, Jonsson P, Branden M, Hook F 2009 J. Struct. Biol. 168 200

    [12]

    Luan Y, Ramos L 2007 J. Am. Chem. Soc. 129 14619

    [13]

    Fu M, Li Q, Sun B 2017 ACS Nano 11 7349

    [14]

    Li Z L, Ding H M, Ma Y Q 2016 J. Phys.: Condens. Matter 28 083001

    [15]

    Hu J M, Tian W D, Ma Y Q 2015 Macromol. Theory Simul. 24 399

    [16]

    Menger F M, Seredyuk V A, Kitaeva M V, Yaroslavov A A, Melik-Nubarov N S 2003 J. Am. Chem. Soc. 125 2846

    [17]

    Kim Y W, Sung W Y 2001 Phys. Rev. E 63 041910

    [18]

    Lee H, Larson G R 2008 J. Phys. Chem. B 112 12279

    [19]

    Le B M, Yamada A, Reck L, Chen Y, Baigl D 2008 Langmuir 24 2643

    [20]

    Bi H, Yang B, Wang L 2013 J. Mater. Chem. A 1 7125

    [21]

    Pantazatos D P, MacDonald R C 1999 J. Membrane Biol. 170 27

    [22]

    Fan J, Li J F, Zhang H D, Yang Y L 2007 Acta Phys. Sin. 56 7230 (in Chinese) [范瑾, 李剑锋, 张红东, 杨玉良 2007 物理学报 56 7230]

    [23]

    Duan H, Li J F, Zhang H D 2018 Acta Phys. Sin. 67 038701 (in Chinese) [段华, 李剑锋, 张红东 2018 物理学报 67 038701]

    [24]

    Laroche G, Carrier D, Pzolet M 1988 Biochemistry 27 6220

    [25]

    Xie L Q, Tian W D, Ma Y Q 2013 Soft Matter 9 9319

    [26]

    Hayward S L, Francis D M, Sis M J, Kidambi S 2015 Sci. Rep. 5 14683

    [27]

    Heath G R, Li M, Polignano I L, Richens J L, Catucci G, Butt J N 2016 Biomacromolecules 17 324

    [28]

    Tian W D, Ma Y Q 2013 Chem. Soc. Rev. 42 705

    [29]

    Li J, Zhang H, Qiu F, Yang Y, Chen J Z 2015 Soft Matter 11 1788

    [30]

    Khalifat N, Puff N, Bonneau S, Fournier J B, Angelova M I 2008 Biophys. J. 95 4924

  • [1]

    Yang K, Ma Y Q 2010 Nat. Nanotech. 5 579

    [2]

    Ding H M, Tian W D, Ma Y Q 2012 ACS Nano 6 1230

    [3]

    Tahara K, Tadokoro S, Kawashima Y, Hirashima N 2012 Langmuir 28 7114

    [4]

    Jiang Z Y, Zhang G L, Ma J, Zhu T 2013 Acta Phys. Sin. 62 018701 (in Chinese) [蒋中英, 张国梁, 马晶, 朱涛 2013 物理学报 62 018701]

    [5]

    Ge L, Mhwald H, Li J 2003 Colloid. Surf. A 221 49

    [6]

    Brown K L, Conboy J C 2011 J. Am. Chem. Soc. 133 8794

    [7]

    Zhu T, Jiang Z Y, Ma Y Q, Hu Y 2016 ACS Appl. Mater. Interfaces 8 5857

    [8]

    Lee I C, Wu Y C 2014 ACS Appl. Mater. Interfaces 6 14439

    [9]

    Ding L, Chi E Y, Chemburu S 2009 Langmuir 25 13742

    [10]

    Burke S E, Barrett C J 2003 Biomacromolecules 4 1773

    [11]

    Tabaei S R, Jonsson P, Branden M, Hook F 2009 J. Struct. Biol. 168 200

    [12]

    Luan Y, Ramos L 2007 J. Am. Chem. Soc. 129 14619

    [13]

    Fu M, Li Q, Sun B 2017 ACS Nano 11 7349

    [14]

    Li Z L, Ding H M, Ma Y Q 2016 J. Phys.: Condens. Matter 28 083001

    [15]

    Hu J M, Tian W D, Ma Y Q 2015 Macromol. Theory Simul. 24 399

    [16]

    Menger F M, Seredyuk V A, Kitaeva M V, Yaroslavov A A, Melik-Nubarov N S 2003 J. Am. Chem. Soc. 125 2846

    [17]

    Kim Y W, Sung W Y 2001 Phys. Rev. E 63 041910

    [18]

    Lee H, Larson G R 2008 J. Phys. Chem. B 112 12279

    [19]

    Le B M, Yamada A, Reck L, Chen Y, Baigl D 2008 Langmuir 24 2643

    [20]

    Bi H, Yang B, Wang L 2013 J. Mater. Chem. A 1 7125

    [21]

    Pantazatos D P, MacDonald R C 1999 J. Membrane Biol. 170 27

    [22]

    Fan J, Li J F, Zhang H D, Yang Y L 2007 Acta Phys. Sin. 56 7230 (in Chinese) [范瑾, 李剑锋, 张红东, 杨玉良 2007 物理学报 56 7230]

    [23]

    Duan H, Li J F, Zhang H D 2018 Acta Phys. Sin. 67 038701 (in Chinese) [段华, 李剑锋, 张红东 2018 物理学报 67 038701]

    [24]

    Laroche G, Carrier D, Pzolet M 1988 Biochemistry 27 6220

    [25]

    Xie L Q, Tian W D, Ma Y Q 2013 Soft Matter 9 9319

    [26]

    Hayward S L, Francis D M, Sis M J, Kidambi S 2015 Sci. Rep. 5 14683

    [27]

    Heath G R, Li M, Polignano I L, Richens J L, Catucci G, Butt J N 2016 Biomacromolecules 17 324

    [28]

    Tian W D, Ma Y Q 2013 Chem. Soc. Rev. 42 705

    [29]

    Li J, Zhang H, Qiu F, Yang Y, Chen J Z 2015 Soft Matter 11 1788

    [30]

    Khalifat N, Puff N, Bonneau S, Fournier J B, Angelova M I 2008 Biophys. J. 95 4924

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  • Received Date:  16 March 2018
  • Accepted Date:  15 April 2018
  • Published Online:  05 August 2018

Poly-L-lysine induced shape change of negatively charged giant vesicles

    Corresponding author: Zhu Tao, zhuttd@163.com;jiangzhying@163.com
    Corresponding author: Jiang Zhong-Ying, zhuttd@163.com;jiangzhying@163.com
  • 1. Collaborative Innovation Center of Advanced Microstructures, National Laboratory of Solid State Microstructures, School of Physics, Nanjing University, Nanjing 210093, China;
  • 2. Key Laboratory of Micro-nano Electric Sensing Technology and Bionic Devices, College of Electronic and Information Engineering, Yili Normal University, Yining 835000, China
Fund Project:  Project supported by the National Natural Science Foundation of China (Grant Nos. 11464047, 21764015, 11474155, 11774147), the Fundamental Research Funds for the Central Universities, China, the Youth Science and Technology Innovation Talents Training Project of the Autonomous Region, China (Grant No. QN2016YX0504), and the Scientific Research Project of Yili Normal University, China (Grant No. 2013YSYB19).

Abstract: Decoration of biomembrane with polymer may improve its physical properties, biocompatibility, and stability. In this study, we employ the inverted fluorescence microscopy to characterize the polylysine (PLL) induced shape transformation of the negatively charged giant unilamellar vesicles (GUVs) in low ionic medium. It is found that PLL may be adsorbed to the 1, 2-dioleoyl-sn-glycero-3-phosphocholine (DOPC) and 1, 2-dioleoyl-sn-glycero-3-phosphatidic acid (DOPA) binary mixture vesicles, resulting in the attachment between the membranes, the formation of the ropes, and rupture of the GUVs. The response of GUVs generally is enhanced with the increase of the negatively charged DOPA in the membranes. The experimental observations are concluded as follows. Firstly, for the PLL induced attachment of GUVs, the attachment area grows gradually with time. Secondly, ropes can only be found in relatively large GUVs. However, the hollow structure is not discernable from the fluorescence imaging. Thirdly, after the rupture of GUVs, some phase-separated-like highly fluorescence lipid domains form in the adjacent intact vesicles. Through careful discussion and analysis, we show that on the one hand, the positively charged PLL adheres to the negatively charged membrane surface, bridging the neighboring GUVs and drawing the originally electrical repulsive vesicles together. The contact zone between GUVs expands with the increasing adsorption of PLL in this area. And the local high fluorescence areas in the GUVs originate from the PLL induced membrane attachment as well. Some membrane segments from ruptured vesicles are adsorbed to the particular areas of GUV, forming a few lipid patch structures above the latter membrane. On the other hand, PLL is adsorbed to the membrane area enriched in the negatively charged DOPA, reversing the surface charge of the upper leaflet and deteriorating the stability of the lipid bilayer. The original equilibrium of the system is broken by the change of the electrical interaction between the neighboring lipid domains as well as the interaction between the domain and water-dispersed PLL. The lipid packing density and inter-lipid force are affected by the PLL adsorption. Lipid membranes have to bud to release the stress built in the spontaneous curvature incompatibility in the two leaflets. The system may become stable again after buds grown into rods with a certain length. All in all, this study deepens the understanding of the interaction mechanism between lipid membrane and oppositely charged polymer. The conclusions obtained will provide valuable reference for the further studies on the polymer-GUV application areas including drug delivery, control release, cell deformation, micro-volume reaction, and gene therapy.

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