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Title: Protein-Containing Lipid Bilayers Intercalated with Size-Matched Mesoporous Silica Thin Films

Abstract

Here, proteins are key components in a multitude of biological processes, of which the functions carried out by transmembrane (membrane-spanning) proteins are especially demanding for investigations. This is because this class of protein needs to be incorporated into a lipid bilayer representing its native environment, and in addition, many experimental conditions also require a solid support for stabilization and analytical purposes. The solid support substrate may, however, limit the protein functionality due to protein–material interactions and a lack of physical space. We have in this work tailored the pore size and pore ordering of a mesoporous silica thin film to match the native cell-membrane arrangement of the transmembrane protein human aquaporin 4 (hAQP4). Using neutron reflectivity (NR), we provide evidence of how substrate pores host the bulky water-soluble domain of hAQP4, which is shown to extend 7.2 nm into the pores of the substrate. Complementary surface analytical tools, including quartz crystal microbalance with dissipation monitoring (QCM-D) and fluorescence microscopy, revealed successful protein-containing supported lipid bilayer (pSLB) formation on mesoporous silica substrates, whereas pSLB formation was hampered on nonporous silica. Additionally, electron microscopy (TEM and SEM), light scattering (DLS and stopped-flow), and small-angle X-ray scattering (SAXS) were employed to provide amore » comprehensive characterization of this novel hybrid organic–inorganic interface, the tailoring of which is likely to be generally applicable to improve the function and stability of a broad range of membrane proteins containing water-soluble domains.« less

Authors:
 [1]; ORCiD logo [2];  [3];  [4];  [4];  [5];  [6]; ORCiD logo [1]
  1. Chambers Univ. of Technology, Gothenburg (Sweden)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  3. Uppsala Univ., Uppsala (Sweden)
  4. Malmo Univ., Malmo (Sweden)
  5. Univ. of Gothenburg, Gothenburg (Sweden)
  6. Chalmers Univ. of Technology, Gothenburg (Sweden)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
Universities/Institutions; USDOE
OSTI Identifier:
1418770
Report Number(s):
LA-UR-17-28188
Journal ID: ISSN 1530-6984; TRN: US1801299
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
Nano Letters
Additional Journal Information:
Journal Volume: 17; Journal Issue: 1; Journal ID: ISSN 1530-6984
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; lipids aquaporin silica; Aquaporin; Lipid bilayer; Liposome; Membrane protein; Neutron reflectivity; Silica

Citation Formats

Isaksson, Simon, Watkins, Erik Benjamin, Browning, Kathryn L., Lind, Tania Kjellerup, Cardenas, Marite, Hedfalk, Kristina, Hook, Fredrik, and Andersson, Martin. Protein-Containing Lipid Bilayers Intercalated with Size-Matched Mesoporous Silica Thin Films. United States: N. p., 2016. Web. doi:10.1021/acs.nanolett.6b04493.
Isaksson, Simon, Watkins, Erik Benjamin, Browning, Kathryn L., Lind, Tania Kjellerup, Cardenas, Marite, Hedfalk, Kristina, Hook, Fredrik, & Andersson, Martin. Protein-Containing Lipid Bilayers Intercalated with Size-Matched Mesoporous Silica Thin Films. United States. https://doi.org/10.1021/acs.nanolett.6b04493
Isaksson, Simon, Watkins, Erik Benjamin, Browning, Kathryn L., Lind, Tania Kjellerup, Cardenas, Marite, Hedfalk, Kristina, Hook, Fredrik, and Andersson, Martin. Wed . "Protein-Containing Lipid Bilayers Intercalated with Size-Matched Mesoporous Silica Thin Films". United States. https://doi.org/10.1021/acs.nanolett.6b04493. https://www.osti.gov/servlets/purl/1418770.
@article{osti_1418770,
title = {Protein-Containing Lipid Bilayers Intercalated with Size-Matched Mesoporous Silica Thin Films},
author = {Isaksson, Simon and Watkins, Erik Benjamin and Browning, Kathryn L. and Lind, Tania Kjellerup and Cardenas, Marite and Hedfalk, Kristina and Hook, Fredrik and Andersson, Martin},
abstractNote = {Here, proteins are key components in a multitude of biological processes, of which the functions carried out by transmembrane (membrane-spanning) proteins are especially demanding for investigations. This is because this class of protein needs to be incorporated into a lipid bilayer representing its native environment, and in addition, many experimental conditions also require a solid support for stabilization and analytical purposes. The solid support substrate may, however, limit the protein functionality due to protein–material interactions and a lack of physical space. We have in this work tailored the pore size and pore ordering of a mesoporous silica thin film to match the native cell-membrane arrangement of the transmembrane protein human aquaporin 4 (hAQP4). Using neutron reflectivity (NR), we provide evidence of how substrate pores host the bulky water-soluble domain of hAQP4, which is shown to extend 7.2 nm into the pores of the substrate. Complementary surface analytical tools, including quartz crystal microbalance with dissipation monitoring (QCM-D) and fluorescence microscopy, revealed successful protein-containing supported lipid bilayer (pSLB) formation on mesoporous silica substrates, whereas pSLB formation was hampered on nonporous silica. Additionally, electron microscopy (TEM and SEM), light scattering (DLS and stopped-flow), and small-angle X-ray scattering (SAXS) were employed to provide a comprehensive characterization of this novel hybrid organic–inorganic interface, the tailoring of which is likely to be generally applicable to improve the function and stability of a broad range of membrane proteins containing water-soluble domains.},
doi = {10.1021/acs.nanolett.6b04493},
journal = {Nano Letters},
number = 1,
volume = 17,
place = {United States},
year = {Wed Nov 23 00:00:00 EST 2016},
month = {Wed Nov 23 00:00:00 EST 2016}
}

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Works referenced in this record:

Pore Spanning Lipid Bilayers on Mesoporous Silica Having Varying Pore Size
journal, July 2011

  • Claesson, Maria; Frost, Rickard; Svedhem, Sofia
  • Langmuir, Vol. 27, Issue 14
  • DOI: 10.1021/la201411b

Preserved Transmembrane Protein Mobility in Polymer-Supported Lipid Bilayers Derived from Cell Membranes
journal, August 2015


Formation of supported planar bilayers by fusion of vesicles to supported phospholipid monolayers
journal, January 1992

  • Kalb, Edwin; Frey, Sammy; Tamm, Lukas K.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1103, Issue 2
  • DOI: 10.1016/0005-2736(92)90101-Q

Composition and structure of mixed phospholipid supported bilayers formed by POPC and DPPC
journal, January 2012

  • Åkesson, Anna; Lind, Tania; Ehrlich, Nicky
  • Soft Matter, Vol. 8, Issue 20
  • DOI: 10.1039/c2sm00013j

Supported Membranes: Scientific and Practical Applications
journal, January 1996


The druggable genome
journal, September 2002

  • Hopkins, Andrew L.; Groom, Colin R.
  • Nature Reviews Drug Discovery, Vol. 1, Issue 9
  • DOI: 10.1038/nrd892

Aquaporin-4 square array assembly: Opposing actions of M1 and M23 isoforms
journal, November 2003

  • Furman, C. S.; Gorelick-Feldman, D. A.; Davidson, K. G. V.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 23
  • DOI: 10.1073/pnas.2235843100

Evaporation-Induced Self-Assembly: Nanostructures Made Easy
journal, May 1999


Co-refinement of multiple-contrast neutron/X-ray reflectivity data using MOTOFIT
journal, March 2006


Contour Length and Refolding Rate of a Small Protein Controlled by Engineered Disulfide Bonds
journal, January 2007


Improved QCM-D signal-to-noise ratio using mesoporous silica and titania
journal, May 2012

  • Claesson, Maria; Ahmadi, Akbar; Fathali, Hoda M.
  • Sensors and Actuators B: Chemical, Vol. 166-167
  • DOI: 10.1016/j.snb.2012.03.002

Bacteriorhodopsin Conjugates as Anchors for Supported Membranes
journal, July 2004

  • Sharma, Manoj K.; Jattani, Harsha; Gilchrist, M. Lane
  • Bioconjugate Chemistry, Vol. 15, Issue 4
  • DOI: 10.1021/bc034231h

General Predictive Syntheses of Cubic, Hexagonal, and Lamellar Silica and Titania Mesostructured Thin Films §
journal, August 2002

  • Alberius, Peter C. A.; Frindell, Karen L.; Hayward, Ryan C.
  • Chemistry of Materials, Vol. 14, Issue 8
  • DOI: 10.1021/cm011209u

Specific and Stable Fluorescence Labeling of Histidine-Tagged Proteins for Dissecting Multi-Protein Complex Formation
journal, February 2006

  • Lata, Suman; Gavutis, Martynas; Tampé, Robert
  • Journal of the American Chemical Society, Vol. 128, Issue 7
  • DOI: 10.1021/ja0563105

Osmotic water permeabilities of brush border and basolateral membrane vesicles from rat renal cortex and small intestine
journal, June 1986

  • van Heeswijk, M. P. E.; van Os, C. H.
  • The Journal of Membrane Biology, Vol. 92, Issue 2
  • DOI: 10.1007/BF01870707

The yellow mini-hutch for SAXS experiments at MAX IV Laboratory
journal, March 2013


Formation of Streptavidin-Supported Lipid Bilayers on Porous Anodic Alumina:  Electrochemical Monitoring of Triggered Vesicle Fusion
journal, September 2001

  • Proux-Delrouyre, Vanessa; Laval, Jean-Marc; Bourdillon, Christian
  • Journal of the American Chemical Society, Vol. 123, Issue 37
  • DOI: 10.1021/ja010361u

Improving recombinant eukaryotic membrane protein yields in Pichia pastoris : The importance of codon optimization and clone selection
journal, July 2011


Discrete Conductance Fluctuations in Lipid Bilayer Protein Membranes
journal, June 1969

  • Bean, R. C.; Shepherd, W. C.; Chan, H.
  • Journal of General Physiology, Vol. 53, Issue 6
  • DOI: 10.1085/jgp.53.6.741

A new family of mesoporous molecular sieves prepared with liquid crystal templates
journal, December 1992

  • Beck, J. S.; Vartuli, J. C.; Roth, W. J.
  • Journal of the American Chemical Society, Vol. 114, Issue 27, p. 10834-10843
  • DOI: 10.1021/ja00053a020

The trials and tribulations of membrane protein folding in vitro
journal, February 2003


Implications of the Aquaporin-4 Structure on Array Formation and Cell Adhesion
journal, January 2006

  • Hiroaki, Yoko; Tani, Kazutoshi; Kamegawa, Akiko
  • Journal of Molecular Biology, Vol. 355, Issue 4
  • DOI: 10.1016/j.jmb.2005.10.081

Allogeneic stimulation of cytotoxic T cells by supported planar membranes.
journal, October 1984

  • Brian, A. A.; McConnell, H. M.
  • Proceedings of the National Academy of Sciences, Vol. 81, Issue 19
  • DOI: 10.1073/pnas.81.19.6159

The human AQP4 gene: definition of the locus encoding two water channel polypeptides in brain.
journal, October 1996

  • Lu, M.; Lee, M. D.; Smith, B. L.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 20
  • DOI: 10.1073/pnas.93.20.10908

Oriented Attachment and Membrane Reconstitution of His-Tagged Cytochrome c Oxidase to a Gold Electrode:  In Situ Monitoring by Surface-Enhanced Infrared Absorption Spectroscopy
journal, December 2004

  • Ataka, Kenichi; Giess, Frank; Knoll, Wolfgang
  • Journal of the American Chemical Society, Vol. 126, Issue 49
  • DOI: 10.1021/ja045951h

Polymer-Tethered Bimolecular Lipid Membranes
book, January 2009

  • Knoll, Wolfgang; Bender, Katja; Förch, Renate
  • Advances in Polymer Science
  • DOI: 10.1007/12_2009_27

Formation of Supported Lipid Bilayers by Vesicle Fusion: Effect of Deposition Temperature
journal, June 2014

  • Lind, Tania Kjellerup; Cárdenas, Marité; Wacklin, Hanna Pauliina
  • Langmuir, Vol. 30, Issue 25
  • DOI: 10.1021/la500897x

Characterization of individual polynucleotide molecules using a membrane channel
journal, November 1996

  • Kasianowicz, J. J.; Brandin, E.; Branton, D.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 24
  • DOI: 10.1073/pnas.93.24.13770

Determinants of aquaporin-4 assembly in orthogonal arrays revealed by live-cell single-molecule fluorescence imaging
journal, March 2009

  • Crane, Jonathan M.; Verkman, Alan S.
  • Journal of Cell Science, Vol. 122, Issue 6
  • DOI: 10.1242/jcs.042341

Triblock Copolymer Syntheses of Mesoporous Silica with Periodic 50 to 300 Angstrom Pores
journal, January 1998


Crystal structure of human aquaporin 4 at 1.8 A and its mechanism of conductance
journal, April 2009

  • Ho, J. D.; Yeh, R.; Sandstrom, A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 18
  • DOI: 10.1073/pnas.0902725106

Molecular cloning of a mercurial-insensitive water channel expressed in selected water-transporting tissues.
journal, February 1994


Works referencing / citing this record:

An Assessment of the Use of Mesoporous Silica Materials to Improve Pulsed Dipolar Spectroscopy
journal, July 2018