Water Ordering Controls the Dynamic Equilibrium of Micelle-Fiber Formation in Self-Assembly of Peptide Amphiphiles

Deshmukh, Sanket; Solomon, Lee A.; Kamath, Ganesh; Fry, H. Christopher; Sankaranarayanan, Subramanian K. R. S.

doi:10.1038/ncomms12367

Title: Water Ordering Controls the Dynamic Equilibrium of Micelle-Fiber Formation in Self-Assembly of Peptide Amphiphiles

Journal Article · Wed Aug 24 00:00:00 EDT 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms12367· OSTI ID:1339526

Deshmukh, Sanket ^[1]; Solomon, Lee A. ^[1]; Kamath, Ganesh ^[2]; Fry, H. Christopher ^[1]; Sankaranarayanan, Subramanian K. R. S. ^[1]

Argonne National Lab. (ANL), Lemont, IL (United States)
Univ. of Missouri, Columbia, MO (United States)

Understanding the role of water in governing the kinetics of the self-assembly processes of amphiphilic peptides has still remained elusive. Here, using a multi-stage atomistic-coarse-grained approach, complemented by circular dichroism/infra-red spectroscopy and dynamic light scattering experiments, we highlight the dual nature of water in dictating the mechanism and dynamics of self-assembly of peptide amphiphiles (PAs). Our computational study shows that (i) Water cage formation and breakage near the hydrophobic groups controls the fusion dynamics and aggregation of PAs in the micellar stage, and (ii) Enhanced structural ordering of vicinal water near the hydrophilic amino acids shifts the equilibrium towards the fiber phase and stimulates structure and order in the PAs when they assemble into a hexagonal nanofiber architecture. Finally, spectroscopy and microscopy studies authenticate our computational observation that water ordering near the PAs increases with increase in time. The measured infra-red O-H bond stretch frequency reminiscent of ice-like suggests that the solvated water becomes increasingly solid-like with increased structural order in the assembled peptide network – thus shedding light on the role of water in a self-assembly process.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1339526

Journal Information:: Nature Communications, Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 44 works

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References (58)

Peptide-amphiphile nanofibers: A versatile scaffold for the preparation of self-assembling materials Hartgerink, J. D.; Beniash, E.; Stupp, S. I. Proceedings of the National Academy of Sciences, Vol. 99, Issue 8, p. 5133-5138 https://doi.org/10.1073/pnas.072699999	journal	April 2002
Nanofibers and their applications in tissue engineering Vasita, Rajesh; Katti, Dhirendra S. International Journal of Nanomedicine, Vol. 1, Issue 1 https://doi.org/10.2147/nano.2006.1.1.15	journal	January 2006
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
Enhanced angiogenesis through controlled release of basic fibroblast growth factor from peptide amphiphile for tissue regeneration Hosseinkhani, Hossein; Hosseinkhani, Mohsen; Khademhosseini, Ali Biomaterials, Vol. 27, Issue 34 https://doi.org/10.1016/j.biomaterials.2006.08.003	journal	December 2006
Self-Assembly of Highly Ordered Peptide Amphiphile Metalloporphyrin Arrays Fry, H. Christopher; Garcia, Jamie M.; Medina, Matthew J. Journal of the American Chemical Society, Vol. 134, Issue 36 https://doi.org/10.1021/ja304674d	journal	August 2012
On the Mechanism of Light Harvesting in Photosynthetic Purple Bacteria: B800 to B850 Energy Transfer Scholes, Gregory D.; Fleming, Graham R. The Journal of Physical Chemistry B, Vol. 104, Issue 8 https://doi.org/10.1021/jp993435l	journal	March 2000
Self-assembly of peptide amphiphiles: From molecules to nanostructures to biomaterials Cui, Honggang; Webber, Matthew J.; Stupp, Samuel I. Biopolymers, Vol. 94, Issue 1, p. 1-18 https://doi.org/10.1002/bip.21328	journal	January 2010
Toward a Mechanistic Understanding of Ionic Self-Complementary Peptide Self-Assembly: Role of Water Molecules and Ions Kabiri, Maryam; Bushnak, Ibraheem; McDermot, Mark T. Biomacromolecules, Vol. 14, Issue 11 https://doi.org/10.1021/bm401077b	journal	October 2013
Self-assembly of diphenylalanine peptides into microtubes with “turn on” fluorescence using an aggregation-induced emission molecule Na, Na; Mu, Xiaoyan; Liu, Qiuling Chemical Communications, Vol. 49, Issue 86 https://doi.org/10.1039/c3cc45320k	journal	January 2013
Peptide self-assembly at the nanoscale: a challenging target for computational and experimental biotechnology Colombo, Giorgio; Soto, Patricia; Gazit, Ehud Trends in Biotechnology, Vol. 25, Issue 5 https://doi.org/10.1016/j.tibtech.2007.03.004	journal	May 2007
Exploring the Early Steps of Amyloid Peptide Aggregation by Computers Mousseau, Normand; Derreumaux, Philippe Accounts of Chemical Research, Vol. 38, Issue 11 https://doi.org/10.1021/ar050045a	journal	November 2005
Atomistic Molecular Dynamics Simulations of Peptide Amphiphile Self-Assembly into Cylindrical Nanofibers Lee, One-Sun; Stupp, Samuel I.; Schatz, George C. Journal of the American Chemical Society, Vol. 133, Issue 10 https://doi.org/10.1021/ja110966y	journal	March 2011
Modeling the Self-Assembly of Peptide Amphiphiles into Fibers Using Coarse-Grained Molecular Dynamics Lee, One-Sun; Cho, Vince; Schatz, George C. Nano Letters, Vol. 12, Issue 9 https://doi.org/10.1021/nl302487m	journal	January 2012
Probing the Interior of Peptide Amphiphile Supramolecular Aggregates Tovar, John D.; Claussen, Randal C.; Stupp, Samuel I. Journal of the American Chemical Society, Vol. 127, Issue 20 https://doi.org/10.1021/ja043764d	journal	May 2005
Modeling Self-Assembly Processes Driven by Nonbonded Interactions in Soft Materials ^† McCullagh, Martin; Prytkova, Tatiana; Tonzani, Stefano The Journal of Physical Chemistry B, Vol. 112, Issue 34 https://doi.org/10.1021/jp803192u	journal	August 2008
Self-Assembly Combining Two Bioactive Peptide-Amphiphile Molecules into Nanofibers by Electrostatic Attraction Niece, Krista L.; Hartgerink, Jeffrey D.; Donners, Jack J. J. M. Journal of the American Chemical Society, Vol. 125, Issue 24 https://doi.org/10.1021/ja028215r	journal	June 2003
Design of nanostructures based on aromatic peptide amphiphiles Fleming, Scott; Ulijn, Rein V. Chem. Soc. Rev., Vol. 43, Issue 23 https://doi.org/10.1039/C4CS00247D	journal	January 2014
Assembly and structure of α-helical peptide films on hydrophobic fluorocarbon surfaces Weidner, Tobias; Samuel, Newton T.; McCrea, Keith Biointerphases, Vol. 5, Issue 1 https://doi.org/10.1116/1.3317116	journal	March 2010
Going Backward: A Flexible Geometric Approach to Reverse Transformation from Coarse Grained to Atomistic Models Wassenaar, Tsjerk A.; Pluhackova, Kristyna; Böckmann, Rainer A. Journal of Chemical Theory and Computation, Vol. 10, Issue 2 https://doi.org/10.1021/ct400617g	journal	January 2014
Multiscale modeling of biomolecular systems: in serial and in parallel Ayton, Gary S.; Noid, Will G.; Voth, Gregory A. Current Opinion in Structural Biology, Vol. 17, Issue 2 https://doi.org/10.1016/j.sbi.2007.03.004	journal	April 2007
Multiscale molecular dynamics simulations of micelles: coarse-grain for self-assembly and atomic resolution for finer details Brocos, Pilar; Mendoza-Espinosa, Paola; Castillo, Rolando Soft Matter, Vol. 8, Issue 34 https://doi.org/10.1039/c2sm25877c	journal	January 2012
Surfactant Hydrophobic Effect on the Phase Behavior of Oppositely Charged Protein and Surfactant Mixtures: Lysozyme and Sodium Alkyl Sulfates Morén, Anna Karin; Khan, Ali Langmuir, Vol. 14, Issue 24 https://doi.org/10.1021/la980368y	journal	November 1998
Thermodynamics of the hydrophobic effect in surfactant solutions: Micellization and adsorption Kronberg, Bengt; Costas, M.; Silveston, R. Pure and Applied Chemistry, Vol. 67, Issue 6 https://doi.org/10.1351/pac199567060897	journal	January 1995
Hydrophobic effect in protein folding and other noncovalent processes involving proteins. Spolar, R. S.; Ha, J. H.; Record, M. T. Proceedings of the National Academy of Sciences, Vol. 86, Issue 21 https://doi.org/10.1073/pnas.86.21.8382	journal	November 1989
Modeling the Influence of Salt on the Hydrophobic Effect and Protein Fold Stability Date, Mihir S.; Dominy, Brian N. Communications in Computational Physics, Vol. 13, Issue 1 https://doi.org/10.4208/cicp.290711.121011s	journal	January 2013
Effect of Ions on the Hydrophobic Interaction between Two Plates Zangi, Ronen; Hagen, Morten; Berne, B. J. Journal of the American Chemical Society, Vol. 129, Issue 15 https://doi.org/10.1021/ja068305m	journal	April 2007
Ion binding and the hydrophobic effect Evans, D. Fennell; Ninham, B. W. The Journal of Physical Chemistry, Vol. 87, Issue 24 https://doi.org/10.1021/j150642a050	journal	November 1983
Role of Solvation Dynamics and Local Ordering of Water in Inducing Conformational Transitions in Poly( N -isopropylacrylamide) Oligomers through the LCST Deshmukh, Sanket A.; Sankaranarayanan, Subramanian K. R. S.; Suthar, Kamlesh The Journal of Physical Chemistry B, Vol. 116, Issue 9 https://doi.org/10.1021/jp210788u	journal	February 2012
Thermodynamic considerations for solubility and conformational transitions of poly-N-isopropyl-acrylamide Kamath, Ganesh; Deshmukh, Sanket A.; Baker, Gary A. Physical Chemistry Chemical Physics, Vol. 15, Issue 30 https://doi.org/10.1039/c3cp44076a	journal	January 2013
Molecular dynamics simulations of the interactions and dispersion of carbon nanotubes in polyethylene oxide/water systems Uddin, Nasir M.; Capaldi, Franco M.; Farouk, Bakhtier Polymer, Vol. 52, Issue 2 https://doi.org/10.1016/j.polymer.2010.11.056	journal	January 2011
Enthalpy−Entropy Contributions to the Potential of Mean Force of Nanoscopic Hydrophobic Solutes Choudhury, Niharendu; Pettitt, B. Montgomery The Journal of Physical Chemistry B, Vol. 110, Issue 16 https://doi.org/10.1021/jp056909r	journal	April 2006
Free Energy Profile and Mechanism of Self-Assembly of Peptide Amphiphiles Based on a Collective Assembly Coordinate Yu, Tao; Schatz, George C. The Journal of Physical Chemistry B, Vol. 117, Issue 30 https://doi.org/10.1021/jp404835q	journal	July 2013
A fresh look at the Ramachandran plot and the occurrence of standard structures in proteins Hollingsworth, Scott A.; Karplus, P. Andrew BioMolecular Concepts, Vol. 1, Issue 3-4 https://doi.org/10.1515/bmc.2010.022	journal	January 2010
Are proteins made from a limited parts list? Fitzkee, Nicholas C.; Fleming, Patrick J.; Gong, Haipeng Trends in Biochemical Sciences, Vol. 30, Issue 2 https://doi.org/10.1016/j.tibs.2004.12.005	journal	February 2005
Theory of self-assembly of hydrocarbon amphiphiles into micelles and bilayers Israelachvili, Jacob N.; Mitchell, D. John; Ninham, Barry W. Journal of the Chemical Society, Faraday Transactions 2, Vol. 72 https://doi.org/10.1039/f29767201525	journal	January 1976
Chemistry and Technology of Surfactants Farn, Richard J. https://doi.org/10.1002/9780470988596	book	March 2006
The Role of Electrostatics and Temperature on Morphological Transitions of Hydrogel Nanostructures Self-Assembled by Peptide Amphiphiles Via Molecular Dynamics Simulations Fu, Iris W.; Markegard, Cade B.; Chu, Brian K. Advanced Healthcare Materials, Vol. 2, Issue 10 https://doi.org/10.1002/adhm.201200400	journal	April 2013
Wormlike Micelle Formation in Peptide-Lipid Conjugates Driven by Secondary Structure Transformation of the Headgroups ^† Shimada, Tomoko; Lee, Sangwoo; Bates, Frank S. The Journal of Physical Chemistry B, Vol. 113, Issue 42 https://doi.org/10.1021/jp901727q	journal	October 2009
Self-Assembly Process of Peptide Amphiphile Worm-Like Micelles Shimada, Tomoko; Sakamoto, Naoki; Motokawa, Ryuhei The Journal of Physical Chemistry B, Vol. 116, Issue 1 https://doi.org/10.1021/jp209105z	journal	December 2011
Free-Energy Landscape for Peptide Amphiphile Self-Assembly: Stepwise versus Continuous Assembly Mechanisms Yu, Tao; Schatz, George C. The Journal of Physical Chemistry B, Vol. 117, Issue 45 https://doi.org/10.1021/jp409305e	journal	October 2013
Coarse Grained Protein−Lipid Model with Application to Lipoprotein Particles ^† Shih, Amy Y.; Arkhipov, Anton; Freddolino, Peter L. The Journal of Physical Chemistry B, Vol. 110, Issue 8 https://doi.org/10.1021/jp0550816	journal	March 2006
Is the first hydration shell of lysozyme of higher density than bulk water? Merzel, F.; Smith, J. C. Proceedings of the National Academy of Sciences, Vol. 99, Issue 8 https://doi.org/10.1073/pnas.082335099	journal	April 2002
Molecular Simulation Study of Peptide Amphiphile Self-Assembly Velichko, Yuri S.; Stupp, Samuel I.; de la Cruz, Monica Olvera The Journal of Physical Chemistry B, Vol. 112, Issue 8 https://doi.org/10.1021/jp074420n	journal	February 2008
The role of water in structural changes of poly(N-isopropylacrylamide) and poly(N-isopropylmethacrylamide) studied by FTIR, Raman spectroscopy and quantum chemical calculations Dybal, Jiří; Trchová, Miroslava; Schmidt, Pavel Vibrational Spectroscopy, Vol. 51, Issue 1 https://doi.org/10.1016/j.vibspec.2008.10.003	journal	September 2009
Vibrational Spectra of Proximal Water in a Thermo-Sensitive Polymer Undergoing Conformational Transition Across the Lower Critical Solution Temperature Deshmukh, Sanket A.; Sankaranarayanan, Subramanian K. R. S.; Mancini, Derrick C. The Journal of Physical Chemistry B, Vol. 116, Issue 18 https://doi.org/10.1021/jp211831x	journal	April 2012
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
Pathway Selection in Peptide Amphiphile Assembly Korevaar, Peter A.; Newcomb, Christina J.; Meijer, E. W. Journal of the American Chemical Society, Vol. 136, Issue 24 https://doi.org/10.1021/ja503882s	journal	June 2014
The infrared spectra of amorphous solid water and ice Ic between 10 and 140 K Hagen, W.; Tielens, A. G. G. M.; Greenberg, J. M. Chemical Physics, Vol. 56, Issue 3 https://doi.org/10.1016/0301-0104(81)80158-9	journal	April 1981
Infrared spectra of , and D2O in the liquid phase by single-pass attenuated total internal reflection spectroscopy Lappi, Simon E.; Smith, Brandye; Franzen, Stefan Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 60, Issue 11 https://doi.org/10.1016/j.saa.2003.12.042	journal	September 2004
Interpretation of IR and Raman Line Shapes for H ₂ O and D ₂ O Ice Ih Shi, L.; Gruenbaum, S. M.; Skinner, J. L. The Journal of Physical Chemistry B, Vol. 116, Issue 47 https://doi.org/10.1021/jp3059239	journal	October 2012
Fourier Transform Infrared Spectroscopic Analysis of Protein Secondary Structures Kong, Jilie; Yu, Shaoning Acta Biochimica et Biophysica Sinica, Vol. 39, Issue 8 https://doi.org/10.1111/j.1745-7270.2007.00320.x	journal	August 2007
The MARTINI Force Field: Coarse Grained Model for Biomolecular Simulations Marrink, Siewert J.; Risselada, H. Jelger; Yefimov, Serge The Journal of Physical Chemistry B, Vol. 111, Issue 27 https://doi.org/10.1021/jp071097f	journal	July 2007
Assembly of lipoprotein particles revealed by coarse-grained molecular dynamics simulations Shih, Amy Y.; Freddolino, Peter L.; Arkhipov, Anton Journal of Structural Biology, Vol. 157, Issue 3 https://doi.org/10.1016/j.jsb.2006.08.006	journal	March 2007
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
Constant pressure molecular dynamics algorithms Martyna, Glenn J.; Tobias, Douglas J.; Klein, Michael L. The Journal of Chemical Physics, Vol. 101, Issue 5 https://doi.org/10.1063/1.467468	journal	September 1994
Constant pressure molecular dynamics simulation: The Langevin piston method Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W. The Journal of Chemical Physics, Vol. 103, Issue 11 https://doi.org/10.1063/1.470648	journal	September 1995
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
Reconstruction of atomistic details from coarse-grained structures Rzepiela, Andrzej J.; Schäfer, Lars V.; Goga, Nicolae Journal of Computational Chemistry https://doi.org/10.1002/jcc.21415	journal	January 2010

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