Chiral Recognition of Lipid Bilayer Membranes by Supramolecular Assemblies of Peptide Amphiphiles

Sato, Kohei; Ji, Wei; Álvarez, Zaida; Palmer, Liam C.; Stupp, Samuel I.

doi:10.1021/acsbiomaterials.9b00553

Chiral Recognition of Lipid Bilayer Membranes by Supramolecular Assemblies of Peptide Amphiphiles

Journal Article · Wed May 29 00:00:00 EDT 2019 · ACS Biomaterials Science & Engineering

DOI:https://doi.org/10.1021/acsbiomaterials.9b00553· OSTI ID:1544845

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Northwestern Univ., Evanston, IL (United States); Northwestern Univ., Chicago, IL (United States)
Northwestern Univ., Chicago, IL (United States); Katholieke Univ. Leuven (Belgium)
Northwestern Univ., Chicago, IL (United States)

On the basis of the exclusive existence of homochirality in biomolecules and the well-known phenomenon of chiral recognition, it is obvious that chirality is a crucial factor in biological events. We report here that supramolecular assemblies of peptide amphiphiles interact with lipid bilayer membranes in a stereospecific manner. When negatively charged chiral phospholipid bilayer vesicles were subjected to the assemblies, we found that peptide amphiphiles with l-amino acids show stronger affinity for the liposomes compared to the ones with d-amino acids. To examine their biological functions, we tested the cytotoxicity of nanofibers against mammalian primary cells using human bone marrow mesenchymal stem cells and murine astroglial cells. In this work, we demonstrated that cell viability increased when d-amino acids were incorporated in the structure of peptide amphiphiles, which is consistent with our finding of their weaker interactions with lipid bilayer membranes.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); Energy Frontier Research Centers (EFRC) (United States). Center for Bio-Inspired Energy Sciences (CBES)

Sponsoring Organization:: National Science Foundation (NSF); International Institute for Nanotechnology (IIN); Keck Foundation; State of Illinois; US Army Research Office (ARO); US Army Medical Research and Materiel Command (USAMRDC); Northwestern University; E.I. DuPont de Nemours & Co.; The Dow Chemical Company; USDOE Office of Science (SC), Basic Energy Sciences (BES); Japan Society for the Promotion of Science (JSPS); Research Foundation Flanders; Paralyzed Veterans of America Research Foundation

Grant/Contract Number:: AC02-06CH11357; SC0000989

OSTI ID:: 1544845

Alternate ID(s):: OSTI ID: 1822218
OSTI ID: 1846654

Journal Information:: ACS Biomaterials Science & Engineering, Journal Name: ACS Biomaterials Science & Engineering Journal Issue: 6 Vol. 5; ISSN 2373-9878

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (50)

Asymmetric Catalysis: Science and Opportunities (Nobel Lecture) Copyright© The Nobel Foundation 2002. We thank the Nobel Foundation, Stockholm, for permission to print this lecture. Noyori, Ryoji Angewandte Chemie International Edition, Vol. 41, Issue 12 https://doi.org/10.1002/1521-3773(20020617)41:12<2008::AID-ANIE2008>3.0.CO;2-4	journal	June 2002
Chiral Design for Polymeric Biointerface: The Influence of Surface Chirality on Protein Adsorption Wang, Xing; Gan, Hui; Sun, Taolei Advanced Functional Materials, Vol. 21, Issue 17 https://doi.org/10.1002/adfm.201101032	journal	June 2011
Gel Scaffolds of BMP-2-Binding Peptide Amphiphile Nanofibers for Spinal Arthrodesis Lee, Sungsoo S.; Hsu, Erin L.; Mendoza, Marco Advanced Healthcare Materials, Vol. 4, Issue 1 https://doi.org/10.1002/adhm.201400129	journal	April 2014
Chiral Biomaterials: From Molecular Design to Regenerative Medicine Green, David W.; Lee, Jong-Min; Kim, Eun-Jung Advanced Materials Interfaces, Vol. 3, Issue 6 https://doi.org/10.1002/admi.201500411	journal	January 2016
A Torsional Strain Mechanism To Tune Pitch in Supramolecular Helices Li, Liang-shi; Jiang, Hongzhou; Messmore, Benjamin W. Angewandte Chemie International Edition, Vol. 46, Issue 31 https://doi.org/10.1002/anie.200701328	journal	August 2007
Control of Three-Dimensional Cell Adhesion by the Chirality of Nanofibers in Hydrogels Liu, Guo-Feng; Zhang, Di; Feng, Chuan-Liang Angewandte Chemie International Edition, Vol. 53, Issue 30 https://doi.org/10.1002/anie.201403249	journal	June 2014
Chirality-Assisted Ring-Like Aggregation of Aβ(1 - 40) at Liquid-Solid Interfaces: A Stereoselective Two-Step Assembly Process Gao, Guanbin; Zhang, Mingxi; Lu, Pei Angewandte Chemie International Edition, Vol. 54, Issue 7 https://doi.org/10.1002/anie.201410768	journal	December 2014
Equilibrium constants for association of guanidinium and ammonium ions with oxyanions Springs, Bleecker; Haake, Paul Bioorganic Chemistry, Vol. 6, Issue 2 https://doi.org/10.1016/0045-2068(77)90019-0	journal	June 1977
Progress towards understanding β-sheet structure Nesloney, Carey L.; Kelly, Jeffery W. Bioorganic & Medicinal Chemistry, Vol. 4, Issue 6 https://doi.org/10.1016/0968-0896(96)00051-X	journal	June 1996
Membrane lipid composition and cellular function. Spector, A. A.; Yorek, M. A. Journal of Lipid Research, Vol. 26, Issue 9 https://doi.org/10.1016/S0022-2275(20)34276-0	journal	September 1985
Structure, dynamics, and hydration of POPC/POPS bilayers suspended in NaCl, KCl, and CsCl solutions Jurkiewicz, Piotr; Cwiklik, Lukasz; Vojtíšková, Alžběta Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1818, Issue 3 https://doi.org/10.1016/j.bbamem.2011.11.033	journal	March 2012
Fabrication of self-assembling d-form peptide nanofiber scaffold d-EAK16 for rapid hemostasis Luo, Zhongli; Wang, Shunkang; Zhang, Shuguang Biomaterials, Vol. 32, Issue 8 https://doi.org/10.1016/j.biomaterials.2010.11.049	journal	March 2011
Effects of surface molecular chirality on adhesion and differentiation of stem cells Yao, Xiang; Hu, Yiwen; Cao, Bin Biomaterials, Vol. 34, Issue 36 https://doi.org/10.1016/j.biomaterials.2013.08.013	journal	December 2013
Cell-Penetrating Peptides: From Basic Research to Clinics Guidotti, Giulia; Brambilla, Liliana; Rossi, Daniela Trends in Pharmacological Sciences, Vol. 38, Issue 4 https://doi.org/10.1016/j.tips.2017.01.003	journal	April 2017
Supramolecular Assembly of Peptide Amphiphiles Hendricks, Mark P.; Sato, Kohei; Palmer, Liam C. Accounts of Chemical Research, Vol. 50, Issue 10 https://doi.org/10.1021/acs.accounts.7b00297	journal	September 2017
Supramolecular Helical Systems: Helical Assemblies of Small Molecules, Foldamers, and Polymers with Chiral Amplification and Their Functions Yashima, Eiji; Ousaka, Naoki; Taura, Daisuke Chemical Reviews, Vol. 116, Issue 22 https://doi.org/10.1021/acs.chemrev.6b00354	journal	October 2016
Chiral Recognition of l -Amino Acids on Liposomes Prepared with l -Phospholipid Ishigami, Takaaki; Suga, Keishi; Umakoshi, Hiroshi ACS Applied Materials & Interfaces, Vol. 7, Issue 38 https://doi.org/10.1021/acsami.5b07198	journal	September 2015
Enhancing the Magnitude of Antibody Responses through Biomaterial Stereochemistry Appavu, Rajagopal; Chesson, Charles B.; Koyfman, Alexey Y. ACS Biomaterials Science & Engineering, Vol. 1, Issue 7 https://doi.org/10.1021/acsbiomaterials.5b00139	journal	June 2015
Control of Supramolecular Chirality of Nanofibers and Its Effect on Protein Adhesion Lv, Kai; Zhang, Li; Lu, Wensheng ACS Applied Materials & Interfaces, Vol. 6, Issue 21 https://doi.org/10.1021/am504702p	journal	October 2014
Neuronal Growth on l - and d -Cysteine Self-Assembled Monolayers Reveals Neuronal Chiral Sensitivity Baranes, Koby; Moshe, Hagay; Alon, Noa ACS Chemical Neuroscience, Vol. 5, Issue 5 https://doi.org/10.1021/cn500015s	journal	March 2014
Chirality-Sensing Supramolecular Systems Hembury, Guy A.; Borovkov, Victor V.; Inoue, Yoshihisa Chemical Reviews, Vol. 108, Issue 1 https://doi.org/10.1021/cr050005k	journal	January 2008
Chiral recognition of odorants (+)- and (-)-carvone by phospholipid monolayers Pathirana, Suram; Neely, William C.; Myers, Lawrence J. Journal of the American Chemical Society, Vol. 114, Issue 4 https://doi.org/10.1021/ja00030a041	journal	February 1992
Chiral Recognition of Dipeptides in a Biomembrane Model Bombelli, Cecilia; Borocci, Stefano; Lupi, Federica Journal of the American Chemical Society, Vol. 126, Issue 41 https://doi.org/10.1021/ja0470057	journal	October 2004
Stereospecific Interaction between Immune Cells and Chiral Surfaces Sun, Taolei; Han, Dong; Rhemann, Kristina Journal of the American Chemical Society, Vol. 129, Issue 6 https://doi.org/10.1021/ja0686155	journal	February 2007
Multivalent Nanofibers of a Controlled Length: Regulation of Bacterial Cell Agglutination Lee, Dong-Woo; Kim, Taehoon; Park, Il-Soo Journal of the American Chemical Society, Vol. 134, Issue 36 https://doi.org/10.1021/ja306802m	journal	August 2012
Nucleation and Growth of Ordered Arrays of Silver Nanoparticles on Peptide Nanofibers: Hybrid Nanostructures with Antimicrobial Properties Pazos, Elena; Sleep, Eduard; Rubert Pérez, Charles M. Journal of the American Chemical Society, Vol. 138, Issue 17 https://doi.org/10.1021/jacs.6b01570	journal	April 2016
Water Dynamics from the Surface to the Interior of a Supramolecular Nanostructure Ortony, Julia H.; Qiao, Baofu; Newcomb, Christina J. Journal of the American Chemical Society, Vol. 139, Issue 26 https://doi.org/10.1021/jacs.7b02969	journal	June 2017
Programmable Assembly of Peptide Amphiphile via Noncovalent-to-Covalent Bond Conversion Sato, Kohei; Ji, Wei; Palmer, Liam C. Journal of the American Chemical Society, Vol. 139, Issue 26 https://doi.org/10.1021/jacs.7b03878	journal	June 2017
Modulating Cell Behaviors on Chiral Polymer Brush Films with Different Hydrophobic Side Groups Wang, Xing; Gan, Hui; Zhang, Mingxi Langmuir, Vol. 28, Issue 5 https://doi.org/10.1021/la204143g	journal	January 2012
Presentation and Recognition of Biotin on Nanofibers Formed by Branched Peptide Amphiphiles Guler, Mustafa O.; Soukasene, Stephen; Hulvat, James F. Nano Letters, Vol. 5, Issue 2 https://doi.org/10.1021/nl048238z	journal	February 2005
Super-resolution microscopy reveals structural diversity in molecular exchange among peptide amphiphile nanofibres da Silva, Ricardo M. P.; van der Zwaag, Daan; Albertazzi, Lorenzo Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11561	journal	May 2016
Cell death versus cell survival instructed by supramolecular cohesion of nanostructures Newcomb, Christina J.; Sur, Shantanu; Ortony, Julia H. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4321	journal	February 2014
Internal dynamics of a supramolecular nanofibre Ortony, Julia H.; Newcomb, Christina J.; Matson, John B. Nature Materials, Vol. 13, Issue 8 https://doi.org/10.1038/nmat3979	journal	May 2014
Energy landscapes and functions of supramolecular systems Tantakitti, Faifan; Boekhoven, Job; Wang, Xin Nature Materials, Vol. 15, Issue 4 https://doi.org/10.1038/nmat4538	journal	January 2016
Putting chirality to work: the strategy of chiral switches Agranat, Israel; Caner, Hava; Caldwell, John Nature Reviews Drug Discovery, Vol. 1, Issue 10 https://doi.org/10.1038/nrd915	journal	October 2002
Tuning the interactions between chiral plasmonic films and living cells Zhao, Xueli; Xu, Liguang; Sun, Maozhong Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02268-8	journal	December 2017
The Handedness of the Universe Hegstrom, Roger A.; Kondepudi, Dilip K. Scientific American, Vol. 262, Issue 1 https://doi.org/10.1038/scientificamerican0190-108	journal	January 1990
Chiral biointerface materials Zhang, Mingxi; Qing, Guangyan; Sun, Taolei Chem. Soc. Rev., Vol. 41, Issue 5 https://doi.org/10.1039/C1CS15209B	journal	January 2012
Emerging chirality in nanoscience Wang, Yong; Xu, Jun; Wang, Yawen Chem. Soc. Rev., Vol. 42, Issue 7 https://doi.org/10.1039/C2CS35332F	journal	January 2013
Peptide supramolecular materials for therapeutics Sato, Kohei; Hendricks, Mark P.; Palmer, Liam C. Chemical Society Reviews, Vol. 47, Issue 20 https://doi.org/10.1039/C7CS00735C	journal	January 2018
Stereochemistry triggered differential cell behaviours on chiral polymer surfaces Wang, Xing; Gan, Hui; Sun, Taolei Soft Matter, Vol. 6, Issue 16 https://doi.org/10.1039/c0sm00151a	journal	January 2010
Induced dye leakage by PAMAM G6 does not imply dendrimer entry into vesicle lumen Åkesson, Anna; Lundgaard, Christian Veje; Ehrlich, Nicky Soft Matter, Vol. 8, Issue 34 https://doi.org/10.1039/c2sm25864a	journal	January 2012
Loss, Restoration, and Maintenance of Plasma Membrane Integrity McNeil, Paul L.; Steinhardt, Richard A. Journal of Cell Biology, Vol. 137, Issue 1 https://doi.org/10.1083/jcb.137.1.1	journal	April 1997
Attachment and Culture of Dissociated Cells from rat Embryo Cerebral Hemispheres on Polylysine-Coated Surface Yavin, Ephraim; Yavin, Ziva Journal of Cell Biology, Vol. 62, Issue 2 https://doi.org/10.1083/jcb.62.2.540	journal	August 1974
The Origin of Biological Homochirality Blackmond, D. G. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 5 https://doi.org/10.1101/cshperspect.a002147	journal	March 2010
Self-Assembly and Mineralization of Peptide-Amphiphile Nanofibers Hartgerink, Jeffrey D.; Beniash, Elia; Stupp, Samuel I. Science, Vol. 294, Issue 5547, p. 1684-1688 https://doi.org/10.1126/science.1063187	journal	November 2001
Selective Differentiation of Neural Progenitor Cells by High-Epitope Density Nanofibers Silva, Gabriel A.; Czeisler, Catherine; Niece, Krista L. Science, Vol. 303, Issue 5662, p. 1352-1355 https://doi.org/10.1126/science.1093783	journal	February 2004
Expanding Roles for Diverse Physical Phenomena During the Origin of Life Budin, Itay; Szostak, Jack W. Annual Review of Biophysics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.biophys.050708.133753	journal	April 2010
The Distribution and Function of Phosphatidylserine in Cellular Membranes Leventis, Peter A.; Grinstein, Sergio Annual Review of Biophysics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.biophys.093008.131234	journal	April 2010
Self-Assembling Nanofibers Inhibit Glial Scar Formation and Promote Axon Elongation after Spinal Cord Injury Tysseling-Mattiace, V. M.; Sahni, V.; Niece, K. L. Journal of Neuroscience, Vol. 28, Issue 14 https://doi.org/10.1523/JNEUROSCI.0143-08.2008	journal	April 2008

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