Secondary structure of rat and human amylin across force fields

Hoffmann, Kyle Quynn; McGovern, Michael; Chiu, Chi -Cheng; de Pablo, Juan J.

doi:10.1371/journal.pone.0134091

Title: Secondary structure of rat and human amylin across force fields

Journal Article · Wed Jul 29 00:00:00 EDT 2015 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0134091· OSTI ID:1249116

Hoffmann, Kyle Quynn ^[1]; McGovern, Michael ^[1]; Chiu, Chi -Cheng ^[2]; de Pablo, Juan J. ^[3]

Univ. of Chicago, Chicago, IL (United States)
National Cheng Kung Univ., Tainan (Taiwan)
Univ. of Chicago, Chicago, IL (United States); Argonne National Lab. (ANL), Argonne, IL (United States)

The aggregation of human amylin has been strongly implicated in the progression of Type II diabetes. This 37-residue peptide forms a variety of secondary structures, including random coils, α-helices, and β- hairpins. The balance between these structures depends on the chemical environment, making amylin an ideal candidate to examine inherent biases in force fields. Rat amylin differs from human amylin by only 6 residues; however, it does not form fibrils. Therefore it provides a useful complement to human amylin in studies of the key events along the aggregation pathway. In this work, the free energy of rat and human amylin was determined as a function of α-helix and β-hairpin content for the Gromos96 53a6, OPLS-AA/L, CHARMM22/CMAP, CHARMM22*, Amberff99sb*-ILDN, and Amberff03w force fields using advanced sampling techniques, specifically bias exchange metadynamics. This work represents a first systematic attempt to evaluate the conformations and the corresponding free energy of a large, clinically relevant disordered peptide in solution across force fields. The NMR chemical shifts of rIAPP were calculated for each of the force fields using their respective free energy maps, allowing us to quantitatively assess their predictions. We show that the predicted distribution of secondary structures is sensitive to the choice of force-field: Gromos53a6 is biased towards β-hairpins, while CHARMM22/CMAP predicts structures that are overly α-helical. OPLS-AA/L favors disordered structures. Amberff99sb*-ILDN, AmberFF03w and CHARMM22* provide the balance between secondary structures that is most consistent with available experimental data. In contrast to previous reports, our findings suggest that the equilibrium conformations of human and rat amylin are remarkably similar, but that subtle differences arise in transient alpha-helical and beta-strand containing structures that the human peptide can more readily adopt. We hypothesize that these transient states enable dynamic pathways that facilitate the formation of aggregates and, eventually, amyloid fibrils.

View Accepted Manuscript (DOE)

Cite

Export

Save

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:: 1249116

Alternate ID(s):: OSTI ID: 1212376; OSTI ID: 1395962

Journal Information:: PLoS ONE, Vol. 10, Issue 7; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 54 works

Citation information provided by
Web of Science

References (117)

Constant pressure molecular dynamics for molecular systems Nosé, Shuichi; Klein, M. L. Molecular Physics, Vol. 50, Issue 5 https://doi.org/10.1080/00268978300102851	journal	December 1983
Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling Torrie, G. M.; Valleau, J. P. Journal of Computational Physics, Vol. 23, Issue 2 https://doi.org/10.1016/0021-9991(77)90121-8	journal	February 1977
Comparative Molecular Dynamics Study of Human Islet Amyloid Polypeptide (IAPP) and Rat IAPP Oligomers Liang, Guizhao; Zhao, Jun; Yu, Xiang Biochemistry, Vol. 52, Issue 6 https://doi.org/10.1021/bi301525e	journal	January 2013
SHIFTX2: significantly improved protein chemical shift prediction Han, Beomsoo; Liu, Yifeng; Ginzinger, Simon W. Journal of Biomolecular NMR, Vol. 50, Issue 1 https://doi.org/10.1007/s10858-011-9478-4	journal	March 2011
Quantitative Studies of Amyloid in the Islets of Langerhans Westermark, Per Upsala Journal of Medical Sciences, Vol. 77, Issue 2 https://doi.org/10.1517/03009734000000014	journal	July 1972
GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation Hess, Berk; Kutzner, Carsten; van der Spoel, David Journal of Chemical Theory and Computation, Vol. 4, Issue 3 https://doi.org/10.1021/ct700301q	journal	February 2008
Exploring the Folding Free Energy Landscape of Insulin Using Bias Exchange Metadynamics Todorova, Nevena; Marinelli, Fabrizio; Piana, Stefano The Journal of Physical Chemistry B, Vol. 113, Issue 11 https://doi.org/10.1021/jp809776v	journal	March 2009
Structure and Dynamics of an Unfolded Protein Examined by Molecular Dynamics Simulation Lindorff-Larsen, Kresten; Trbovic, Nikola; Maragakis, Paul Journal of the American Chemical Society, Vol. 134, Issue 8 https://doi.org/10.1021/ja209931w	journal	February 2012
Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides ^† Kaminski, George A.; Friesner, Richard A.; Tirado-Rives, Julian The Journal of Physical Chemistry B, Vol. 105, Issue 28 https://doi.org/10.1021/jp003919d	journal	July 2001
Metadynamics convergence law in a multidimensional system Crespo, Yanier; Marinelli, Fabrizio; Pietrucci, Fabio Physical Review E, Vol. 81, Issue 5 https://doi.org/10.1103/PhysRevE.81.055701	journal	May 2010
Optimized Molecular Dynamics Force Fields Applied to the Helix−Coil Transition of Polypeptides Best, Robert B.; Hummer, Gerhard The Journal of Physical Chemistry B, Vol. 113, Issue 26 https://doi.org/10.1021/jp901540t	journal	July 2009
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation. Westermark, P.; Engstrom, U.; Johnson, K. H. Proceedings of the National Academy of Sciences, Vol. 87, Issue 13 https://doi.org/10.1073/pnas.87.13.5036	journal	July 1990
Amyloidogenic Propensities and Conformational Properties of ProIAPP and IAPP in the Presence of Lipid Bilayer Membranes Jha, Suman; Sellin, Daniel; Seidel, Ralf Journal of Molecular Biology, Vol. 389, Issue 5 https://doi.org/10.1016/j.jmb.2009.04.077	journal	June 2009
How Type II Diabetes-Related Islet Amyloid Polypeptide Damages Lipid Bilayers Lee, Chang-Chun; Sun, Yen; Huang, Huey W. Biophysical Journal, Vol. 102, Issue 5 https://doi.org/10.1016/j.bpj.2012.01.039	journal	March 2012
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Amylin Proprotein Processing Generates Progressively More Amyloidogenic Peptides that Initially Sample the Helical State ^† Yonemoto, Isaac T.; Kroon, Gerard J. A.; Dyson, H. Jane Biochemistry, Vol. 47, Issue 37 https://doi.org/10.1021/bi800828u	journal	September 2008
Two-dimensional infrared spectroscopy reveals the complex behaviour of an amyloid fibril inhibitor Middleton, Chris T.; Marek, Peter; Cao, Ping Nature Chemistry, Vol. 4, Issue 5 https://doi.org/10.1038/nchem.1293	journal	March 2012
How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? Wang, Junmei; Cieplak, Piotr; Kollman, Peter A. Journal of Computational Chemistry, Vol. 21, Issue 12 https://doi.org/10.1002/1096-987X(200009)21:12<1049::AID-JCC3>3.0.CO;2-F	journal	January 2000
Molecular Simulations Indicate Marked Differences in the Structure of Amylin Mutants, Correlated with Known Aggregation Propensity Miller, Cayla; Zerze, Gül H.; Mittal, Jeetain The Journal of Physical Chemistry B, Vol. 117, Issue 50 https://doi.org/10.1021/jp409755y	journal	November 2013
SPARTA+: a modest improvement in empirical NMR chemical shift prediction by means of an artificial neural network Shen, Yang; Bax, Ad Journal of Biomolecular NMR, Vol. 48, Issue 1 https://doi.org/10.1007/s10858-010-9433-9	journal	July 2010
Lipid Membranes Modulate the Structure of Islet Amyloid Polypeptide ^† Jayasinghe, Sajith A.; Langen, Ralf Biochemistry, Vol. 44, Issue 36 https://doi.org/10.1021/bi050840w	journal	September 2005
-Helical stabilization by side chain shielding of backbone hydrogen bonds Garcia, A. E.; Sanbonmatsu, K. Y. Proceedings of the National Academy of Sciences, Vol. 99, Issue 5 https://doi.org/10.1073/pnas.042496899	journal	February 2002
Two-dimensional IR spectroscopy and isotope labeling defines the pathway of amyloid formation with residue-specific resolution Shim, S. -H.; Gupta, R.; Ling, Y. L. Proceedings of the National Academy of Sciences, Vol. 106, Issue 16 https://doi.org/10.1073/pnas.0805957106	journal	April 2009
Comparing the structural properties of human and rat islet amyloid polypeptide by MD computer simulations Andrews, Maximilian N.; Winter, Roland Biophysical Chemistry, Vol. 156, Issue 1 https://doi.org/10.1016/j.bpc.2010.12.007	journal	June 2011
Phospholipid Catalysis of Diabetic Amyloid Assembly Knight, Jefferson D.; Miranker, Andrew D. Journal of Molecular Biology, Vol. 341, Issue 5 https://doi.org/10.1016/j.jmb.2004.06.086	journal	August 2004
Comparisons of force fields for proteins by generalized-ensemble simulations Yoda, Takao; Sugita, Yuji; Okamoto, Yuko Chemical Physics Letters, Vol. 386, Issue 4-6 https://doi.org/10.1016/j.cplett.2004.01.078	journal	March 2004
α-helix to β-hairpin transition of human amylin monomer Singh, Sadanand; Chiu, Chi-cheng; Reddy, Allam S. The Journal of Chemical Physics, Vol. 138, Issue 15 https://doi.org/10.1063/1.4798460	journal	April 2013
Using PC clusters to evaluate the transferability of molecular mechanics force fields for proteins Okur, Asim; Strockbine, Bentley; Hornak, Viktor Journal of Computational Chemistry, Vol. 24, Issue 1 https://doi.org/10.1002/jcc.10184	journal	December 2002
Force Field Bias in Protein Folding Simulations Freddolino, Peter L.; Park, Sanghyun; Roux, Benoît Biophysical Journal, Vol. 96, Issue 9 https://doi.org/10.1016/j.bpj.2009.02.033	journal	May 2009
Conformational dynamics of human IAPP monomers Murphy, Ronan D.; Conlon, Jennifer; Mansoor, Tayyaub Biophysical Chemistry, Vol. 167 https://doi.org/10.1016/j.bpc.2012.03.010	journal	June 2012
How Robust Are Protein Folding Simulations with Respect to Force Field Parameterization? Piana, Stefano; Lindorff-Larsen, Kresten; Shaw, David E. Biophysical Journal, Vol. 100, Issue 9 https://doi.org/10.1016/j.bpj.2011.03.051	journal	May 2011
Syntheses, structures and anorectic effects of human and rat amylin Balasubramaniam, A.; Renugopalakrishnan, V.; Stein, M. Peptides, Vol. 12, Issue 5 https://doi.org/10.1016/0196-9781(91)90038-Q	journal	September 1991
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
Flux Tempered Metadynamics Singh, Sadanand; Chiu, Chi-cheng; de Pablo, Juan J. Journal of Statistical Physics, Vol. 145, Issue 4 https://doi.org/10.1007/s10955-011-0301-0	journal	September 2011
Scrutinizing Molecular Mechanics Force Fields on the Submicrosecond Timescale with NMR Data Lange, Oliver F.; van der Spoel, David; de Groot, Bert L. Biophysical Journal, Vol. 99, Issue 2 https://doi.org/10.1016/j.bpj.2010.04.062	journal	July 2010
Amyloid Fibril Formation from Full-Length and Fragments of Amylin Goldsbury, C.; Goldie, K.; Pellaud, J. Journal of Structural Biology, Vol. 130, Issue 2-3 https://doi.org/10.1006/jsbi.2000.4268	journal	June 2000
Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features Kabsch, Wolfgang; Sander, Christian Biopolymers, Vol. 22, Issue 12 https://doi.org/10.1002/bip.360221211	journal	December 1983
Diabetes Due to a Progressive Defect in -Cell Mass in Rats Transgenic for Human Islet Amyloid Polypeptide (HIP Rat): A New Model for Type 2 Diabetes Butler, A. E.; Jang, J.; Gurlo, T. Diabetes, Vol. 53, Issue 6 https://doi.org/10.2337/diabetes.53.6.1509	journal	May 2004
Polymorphic transitions in single crystals: A new molecular dynamics method Parrinello, M.; Rahman, A. Journal of Applied Physics, Vol. 52, Issue 12 https://doi.org/10.1063/1.328693	journal	December 1981
Constrained reaction coordinate dynamics for the simulation of rare events Carter, E. A.; Ciccotti, Giovanni; Hynes, James T. Chemical Physics Letters, Vol. 156, Issue 5 https://doi.org/10.1016/S0009-2614(89)87314-2	journal	April 1989
Systematic Validation of Protein Force Fields against Experimental Data Lindorff-Larsen, Kresten; Maragakis, Paul; Piana, Stefano PLoS ONE, Vol. 7, Issue 2 https://doi.org/10.1371/journal.pone.0032131	journal	February 2012
Peptide Conformation and Supramolecular Organization in Amylin Fibrils: Constraints from Solid-State NMR ^† Luca, Sorin; Yau, Wai-Ming; Leapman, Richard Biochemistry, Vol. 46, Issue 47 https://doi.org/10.1021/bi701427q	journal	November 2007
A general purpose model for the condensed phases of water: TIP4P/2005 Abascal, J. L. F.; Vega, C. The Journal of Chemical Physics, Vol. 123, Issue 23 https://doi.org/10.1063/1.2121687	journal	December 2005
Conformational Distribution and α-Helix to β-Sheet Transition of Human Amylin Fragment Dimer Qi, Ruxi; Luo, Yin; Ma, Buyong Biomacromolecules, Vol. 15, Issue 1 https://doi.org/10.1021/bm401406e	journal	December 2013
Human Islet Amyloid Polypeptide Monomers Form Ordered β-hairpins: A Possible Direct Amyloidogenic Precursor Dupuis, Nicholas F.; Wu, Chun; Shea, Joan-Emma Journal of the American Chemical Society, Vol. 131, Issue 51 https://doi.org/10.1021/ja903814q	journal	December 2009
A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations Duan, Yong; Wu, Chun; Chowdhury, Shibasish Journal of Computational Chemistry, Vol. 24, Issue 16 https://doi.org/10.1002/jcc.10349	journal	October 2003
Solution Structures of Rat Amylin Peptide: Simulation, Theory, and Experiment Reddy, Allam S.; Wang, Lu; Lin, Yu-Shan Biophysical Journal, Vol. 98, Issue 3 https://doi.org/10.1016/j.bpj.2009.10.029	journal	February 2010
Missense Mutation of Amylin Gene (S20G) in Japanese NIDDM Patients Sakagashira, S.; Sanke, T.; Hanabusa, T. Diabetes, Vol. 45, Issue 9 https://doi.org/10.2337/diab.45.9.1279	journal	September 1996
A role for helical intermediates in amyloid formation by natively unfolded polypeptides? Abedini, Andisheh; Raleigh, Daniel P. Physical Biology, Vol. 6, Issue 1 https://doi.org/10.1088/1478-3975/6/1/015005	journal	February 2009
Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Cooper, G. J.; Willis, A. C.; Clark, A. Proceedings of the National Academy of Sciences, Vol. 84, Issue 23 https://doi.org/10.1073/pnas.84.23.8628	journal	December 1987
Are Protein Force Fields Getting Better? A Systematic Benchmark on 524 Diverse NMR Measurements Beauchamp, Kyle A.; Lin, Yu-Shan; Das, Rhiju Journal of Chemical Theory and Computation, Vol. 8, Issue 4 https://doi.org/10.1021/ct2007814	journal	March 2012
Tackling Force-Field Bias in Protein Folding Simulations: Folding of Villin HP35 and Pin WW Domains in Explicit Water Mittal, Jeetain; Best, Robert B. Biophysical Journal, Vol. 99, Issue 3 https://doi.org/10.1016/j.bpj.2010.05.005	journal	August 2010
Self-Assembling Pathway of HiApp Fibrils within Lipid Bilayers Scalisi, Silvia; Sciacca, Michele F. M.; Zhavnerko, Genady ChemBioChem, Vol. 11, Issue 13 https://doi.org/10.1002/cbic.201000090	journal	July 2010
Stable and Metastable States of Human Amylin in Solution Reddy, Allam S.; Wang, Lu; Singh, Sadanand Biophysical Journal, Vol. 99, Issue 7 https://doi.org/10.1016/j.bpj.2010.07.014	journal	October 2010
Direct detection of transient α-helical states in islet amyloid polypeptide Williamson, Jessica A.; Miranker, Andrew D. Protein Science, Vol. 16, Issue 1 https://doi.org/10.1110/ps.062486907	journal	January 2007
Are Current Molecular Dynamics Force Fields too Helical? Best, Robert B.; Buchete, Nicolae-Viorel; Hummer, Gerhard Biophysical Journal, Vol. 95, Issue 1 https://doi.org/10.1529/biophysj.108.132696	journal	July 2008
Islet Amyloid Polypeptide Inserts into Phospholipid Monolayers as Monomer Engel, Maarten F. M.; Yigittop, HaciAli; Elgersma, Ronald C. Journal of Molecular Biology, Vol. 356, Issue 3 https://doi.org/10.1016/j.jmb.2005.12.020	journal	February 2006
A series of PDB related databases for everyday needs Joosten, R. P.; te Beek, T. A. H.; Krieger, E. Nucleic Acids Research, Vol. 39, Issue Database https://doi.org/10.1093/nar/gkq1105	journal	November 2010
Spontaneous diabetes mellitus in transgenic mice expressing human islet amyloid polypeptide. Janson, J.; Soeller, W. C.; Roche, P. C. Proceedings of the National Academy of Sciences, Vol. 93, Issue 14 https://doi.org/10.1073/pnas.93.14.7283	journal	July 1996
Islet Amyloid Polypeptide (IAPP) Transgenic Rodents as Models for Type 2 Diabetes Matveyenko, A. V.; Butler, P. C. ILAR Journal, Vol. 47, Issue 3 https://doi.org/10.1093/ilar.47.3.225	journal	January 2006
Structural Similarities and Differences between Amyloidogenic and Non-Amyloidogenic Islet Amyloid Polypeptide (IAPP) Sequences and Implications for the Dual Physiological and Pathological Activities of These Peptides Wu, Chun; Shea, Joan-Emma PLoS Computational Biology, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pcbi.1003211	journal	August 2013
Interaction Models for Water in Relation to Protein Hydration Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F. The Jerusalem Symposia on Quantum Chemistry and Biochemistry https://doi.org/10.1007/978-94-015-7658-1_21	book	January 1981
Conserved and Cooperative Assembly of Membrane-Bound α-Helical States of Islet Amyloid Polypeptide ^† Knight, Jefferson D.; Hebda, James A.; Miranker, Andrew D. Biochemistry, Vol. 45, Issue 31 https://doi.org/10.1021/bi060579z	journal	August 2006
Comparison of multiple Amber force fields and development of improved protein backbone parameters Hornak, Viktor; Abel, Robert; Okur, Asim Proteins: Structure, Function, and Bioinformatics, Vol. 65, Issue 3 https://doi.org/10.1002/prot.21123	journal	November 2006
Effect of Proline Mutations on the Monomer Conformations of Amylin Chiu, Chi-cheng; Singh, Sadanand; de Pablo, Juan J. Biophysical Journal, Vol. 105, Issue 5 https://doi.org/10.1016/j.bpj.2013.07.029	journal	September 2013
The Role of the Peripheral Anionic Site and Cation−π Interactions in the Ligand Penetration of the Human AChE Gorge Branduardi, Davide; Gervasio, Francesco Luigi; Cavalli, Andrea Journal of the American Chemical Society, Vol. 127, Issue 25 https://doi.org/10.1021/ja0512780	journal	June 2005
The Relation oe Diabetes Mellitus to Lesions of the Pancreas. Hyaline Degeneration of the Islands oe Langerhans Opie, E. L. Journal of Experimental Medicine, Vol. 5, Issue 5 https://doi.org/10.1084/jem.5.5.527	journal	March 1901
Mechanism of IAPP amyloid fibril formation involves an intermediate with a transient -sheet Buchanan, L. E.; Dunkelberger, E. B.; Tran, H. Q. Proceedings of the National Academy of Sciences, Vol. 110, Issue 48 https://doi.org/10.1073/pnas.1314481110	journal	November 2013
Systematic Comparison of Empirical Forcefields for Molecular Dynamic Simulation of Insulin Todorova, Nevena; Legge, F. Sue; Treutlein, Herbert The Journal of Physical Chemistry B, Vol. 112, Issue 35 https://doi.org/10.1021/jp076825d	journal	September 2008
Certification of Molecular Dynamics Trajectories with NMR Chemical Shifts Li, Da-Wei; Brüschweiler, Rafael The Journal of Physical Chemistry Letters, Vol. 1, Issue 1 https://doi.org/10.1021/jz9001345	journal	November 2009
Common structure and toxic function of amyloid oligomers implies a common mechanism of pathogenesis Glabe, C. G.; Kayed, R. Neurology, Vol. 66, Issue Issue 1, Supplement 1 https://doi.org/10.1212/01.wnl.0000192103.24796.42	journal	December 2005
Parallel tempering: Theory, applications, and new perspectives Earl, David J.; Deem, Michael W. Physical Chemistry Chemical Physics, Vol. 7, Issue 23 https://doi.org/10.1039/b509983h	journal	January 2005
PLUMED: A portable plugin for free-energy calculations with molecular dynamics Bonomi, Massimiliano; Branduardi, Davide; Bussi, Giovanni Computer Physics Communications, Vol. 180, Issue 10 https://doi.org/10.1016/j.cpc.2009.05.011	journal	October 2009
Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in a membrane environment Nanga, Ravi Prakash Reddy; Brender, Jeffrey R.; Vivekanandan, Subramanian Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1808, Issue 10 https://doi.org/10.1016/j.bbamem.2011.06.012	journal	October 2011
Identification of a novel human islet amyloid polypeptide β-sheet domain and factors influencing fibrillogenesis Jaikaran, Emma T. A. S.; Higham, Claire E.; Serpell, Louise C. Journal of Molecular Biology, Vol. 308, Issue 3 https://doi.org/10.1006/jmbi.2001.4593	journal	May 2001
Density of States–Based Molecular Simulations Singh, Sadanand; Chopra, Manan; de Pablo, Juan J. Annual Review of Chemical and Biomolecular Engineering, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-chembioeng-062011-081032	journal	July 2012
A molecular dynamics method for simulations in the canonical ensemble Nosé, Shūichi Molecular Physics, Vol. 52, Issue 2 https://doi.org/10.1080/00268978400101201	journal	June 1984
Comparison of Secondary Structure Formation Using 10 Different Force Fields in Microsecond Molecular Dynamics Simulations Cino, Elio A.; Choy, Wing-Yiu; Karttunen, Mikko Journal of Chemical Theory and Computation, Vol. 8, Issue 8 https://doi.org/10.1021/ct300323g	journal	July 2012
Protein Simulations with an Optimized Water Model: Cooperative Helix Formation and Temperature-Induced Unfolded State Collapse Best, Robert B.; Mittal, Jeetain The Journal of Physical Chemistry B, Vol. 114, Issue 46 https://doi.org/10.1021/jp108618d	journal	November 2010
Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations Mackerell, Alexander D.; Feig, Michael; Brooks, Charles L. Journal of Computational Chemistry, Vol. 25, Issue 11 https://doi.org/10.1002/jcc.20065	journal	August 2004
LINCS: A linear constraint solver for molecular simulations Hess, Berk; Bekker, Henk; Berendsen, Herman J. C. Journal of Computational Chemistry, Vol. 18, Issue 12 https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H	journal	September 1997
Well-Tempered Metadynamics: A Smoothly Converging and Tunable Free-Energy Method Barducci, Alessandro; Bussi, Giovanni; Parrinello, Michele Physical Review Letters, Vol. 100, Issue 2 https://doi.org/10.1103/PhysRevLett.100.020603	journal	January 2008
The Amyloid Formation Mechanism in Human IAPP: Dimers Have β-Strand Monomer−Monomer Interfaces Dupuis, Nicholas F.; Wu, Chun; Shea, Joan-Emma Journal of the American Chemical Society, Vol. 133, Issue 19 https://doi.org/10.1021/ja1081537	journal	May 2011
Islet Amyloid Formed from Diabetes-Associated Peptide may be Pathogenic in Type-2 Diabetes Clark, A.; Lewis, C. E.; Willis, A. C. The Lancet, Vol. 330, Issue 8553 https://doi.org/10.1016/S0140-6736(87)90825-7	journal	August 1987
Pore Formation by the Cytotoxic Islet Amyloid Peptide Amylin Mirzabekov, Tajib A.; Lin, Meng-chin; Kagan, Bruce L. Journal of Biological Chemistry, Vol. 271, Issue 4 https://doi.org/10.1074/jbc.271.4.1988	journal	January 1996
Induction of endoplasmic reticulum stress-induced β-cell apoptosis and accumulation of polyubiquitinated proteins by human islet amyloid polypeptide Huang, Chang-jiang; Haataja, Leena; Gurlo, Tatyana American Journal of Physiology-Endocrinology and Metabolism, Vol. 293, Issue 6 https://doi.org/10.1152/ajpendo.00318.2007	journal	December 2007
Three Force Fields' Views of the 310 Helix Patapati, Kalliopi K.; Glykos, Nicholas M. Biophysical Journal, Vol. 101, Issue 7 https://doi.org/10.1016/j.bpj.2011.08.044	journal	October 2011
Canonical dynamics: Equilibrium phase-space distributions Hoover, William G. Physical Review A, Vol. 31, Issue 3 https://doi.org/10.1103/PhysRevA.31.1695	journal	March 1985
Multidimensional View of Amyloid Fibril Nucleation in Atomistic Detail Baftizadeh, Fahimeh; Biarnes, Xevi; Pietrucci, Fabio Journal of the American Chemical Society, Vol. 134, Issue 8 https://doi.org/10.1021/ja210826a	journal	February 2012
Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in Vitro Kayed, Rakez; Bernhagen, Jürgen; Greenfield, Norma Journal of Molecular Biology, Vol. 287, Issue 4 https://doi.org/10.1006/jmbi.1999.2646	journal	April 1999
A Collective Variable for the Efficient Exploration of Protein Beta-Sheet Structures: Application to SH3 and GB1 Pietrucci, Fabio; Laio, Alessandro Journal of Chemical Theory and Computation, Vol. 5, Issue 9 https://doi.org/10.1021/ct900202f	journal	August 2009
Three-Dimensional Structure and Orientation of Rat Islet Amyloid Polypeptide Protein in a Membrane Environment by Solution NMR Spectroscopy Nanga, Ravi Prakash Reddy; Brender, Jeffrey R.; Xu, Jiadi Journal of the American Chemical Society, Vol. 131, Issue 23 https://doi.org/10.1021/ja9010095	journal	June 2009
Association of Highly Compact Type II Diabetes Related Islet Amyloid Polypeptide Intermediate Species at Physiological Temperature Revealed by Diffusion NMR Spectroscopy Soong, Ronald; Brender, Jeffrey R.; Macdonald, Peter M. Journal of the American Chemical Society, Vol. 131, Issue 20 https://doi.org/10.1021/ja900285z	journal	May 2009
Structural Characterisation of Islet Amyloid Polypeptide Fibrils Sumner Makin, O.; Serpell, Louise C. Journal of Molecular Biology, Vol. 335, Issue 5 https://doi.org/10.1016/j.jmb.2003.11.048	journal	January 2004
A smooth particle mesh Ewald method Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L. The Journal of Chemical Physics, Vol. 103, Issue 19 https://doi.org/10.1063/1.470117	journal	November 1995
Escaping free-energy minima Laio, A.; Parrinello, M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 20 https://doi.org/10.1073/pnas.202427399	journal	September 2002
A boundary correction algorithm for metadynamics in multiple dimensions McGovern, Michael; de Pablo, Juan The Journal of Chemical Physics, Vol. 139, Issue 8 https://doi.org/10.1063/1.4818153	journal	August 2013
A Bias-Exchange Approach to Protein Folding Piana, Stefano; Laio, Alessandro The Journal of Physical Chemistry B, Vol. 111, Issue 17 https://doi.org/10.1021/jp067873l	journal	May 2007
Implementation of the CHARMM Force Field in GROMACS: Analysis of Protein Stability Effects from Correction Maps, Virtual Interaction Sites, and Water Models Bjelkmar, Pär; Larsson, Per; Cuendet, Michel A. Journal of Chemical Theory and Computation, Vol. 6, Issue 2 https://doi.org/10.1021/ct900549r	journal	January 2010
Empirical Predictions of Protein Conformation Chou, P. Y.; Fasman, G. D. Annual Review of Biochemistry, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.bi.47.070178.001343	journal	June 1978
The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles Janson, J.; Ashley, R. H.; Harrison, D. Diabetes, Vol. 48, Issue 3 https://doi.org/10.2337/diabetes.48.3.491	journal	March 1999
Improved side-chain torsion potentials for the Amber ff99SB protein force field Lindorff-Larsen, Kresten; Piana, Stefano; Palmo, Kim Proteins: Structure, Function, and Bioinformatics https://doi.org/10.1002/prot.22711	journal	January 2010
Islet Amyloid: A Critical Entity in the Pathogenesis of Type 2 Diabetes Hull, Rebecca L.; Westermark, Gunilla T.; Westermark, Per The Journal of Clinical Endocrinology & Metabolism, Vol. 89, Issue 8 https://doi.org/10.1210/jc.2004-0405	journal	August 2004
A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6 Oostenbrink, Chris; Villa, Alessandra; Mark, Alan E. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20090	journal	January 2004
Islet amyloid polypeptide in diabetic and non-diabetic Pima Indians Clark, A.; Saad, M. F.; Nezzer, T. Diabetologia, Vol. 33, Issue 5 https://doi.org/10.1007/bf00403322	journal	May 1990
The influence of amyloid deposits on the islet volume in maturity onset diabetes mellitus Westermark, P.; Wilander, E. Diabetologia, Vol. 15, Issue 5 https://doi.org/10.1007/bf01219652	journal	November 1978
S20G Mutant Amylin Exhibits Increased in Vitro Amyloidogenicity and Increased Intracellular Cytotoxicity Compared to Wild-Type Amylin Sakagashira, Setsuya; Hiddinga, Henry J.; Tateishi, Kayoko The American Journal of Pathology, Vol. 157, Issue 6 https://doi.org/10.1016/s0002-9440(10)64848-1	journal	December 2000
Preparation of synthetic human islet amyloid polypeptide (IAPP) in a stable conformation to enable study of conversion to amyloid-like fibrils Higham, Claire E.; Jaikaran, Emma T. A. S.; Fraser, Paul E. FEBS Letters, Vol. 470, Issue 1 https://doi.org/10.1016/s0014-5793(00)01287-4	journal	March 2000
Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus Lorenzo, Alfredo; Razzaboni, Bronwyn; Weir, Gordon C. Nature, Vol. 368, Issue 6473 https://doi.org/10.1038/368756a0	journal	April 1994
Syndecan-4 tunes cell mechanics by activating the kindlin-integrin-RhoA pathway Chronopoulos, Antonios; Thorpe, Stephen D.; Cortes, Ernesto Nature Materials, Vol. 19, Issue 6 https://doi.org/10.1038/s41563-019-0567-1	journal	January 2020
Islet Amyloid and Type 2 Diabetes Mellitus Höppener, Jo W. M.; Ahrén, Bo; Lips, Cornelis J. M. New England Journal of Medicine, Vol. 343, Issue 6 https://doi.org/10.1056/nejm200008103430607	journal	August 2000
Structure of α-Helical Membrane-bound Human Islet Amyloid Polypeptide and Its Implications for Membrane-mediated Misfolding Apostolidou, Melania; Jayasinghe, Sajith A.; Langen, Ralf Journal of Biological Chemistry, Vol. 283, Issue 25 https://doi.org/10.1074/jbc.m801383200	journal	April 2008
Dynamic α-Helix Structure of Micelle-bound Human Amylin Patil, Sharadrao M.; Xu, Shihao; Sheftic, Sarah R. Journal of Biological Chemistry, Vol. 284, Issue 18 https://doi.org/10.1074/jbc.m809085200	journal	February 2009
Macroscopic conductivity of aqueous electrolyte solutions scales with ultrafast microscopic ion motions Balos, Vasileios; Imoto, Sho; Netz, Roland R. Freie Universität Berlin https://doi.org/10.17169/refubium-28486	text	January 2020
Phosphorylated peptide of G protein-coupled receptor induces dimerization in activated arrestin Stadler, Andreas M.; Granzin, Joachim; Cousin, Anneliese RWTH Aachen University https://doi.org/10.18154/rwth-2020-08655	text	January 2020
Parallel Tempering: Theory, Applications, and New Perspectives Earl, David J.; Deem, Michael W. arXiv https://doi.org/10.48550/arxiv.physics/0508111	text	January 2005

Cited By (12)

Revisiting the earliest signatures of amyloidogenesis: Roadmaps emerging from computational modeling and experiment Bhattacharya, Shayon; Xu, Liang; Thompson, Damien Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 8, Issue 4 https://doi.org/10.1002/wcms.1359	journal	February 2018
Revealing a Dual Role of Ganglioside Lipids in the Aggregation of Membrane-Associated Islet Amyloid Polypeptide Christensen, Mikkel; Schiøtt, Birgit The Journal of Membrane Biology, Vol. 252, Issue 4-5 https://doi.org/10.1007/s00232-019-00074-5	journal	June 2019
Synergistic long-range effects of mutations underlie aggregation propensities of amylin analogues Alves, Nelson A.; Dias, Luis G.; Frigori, Rafael B. Journal of Molecular Modeling, Vol. 25, Issue 9 https://doi.org/10.1007/s00894-019-4137-x	journal	August 2019
Influence of fullerenol on hIAPP aggregation: amyloid inhibition and mechanistic aspects Bai, Cuiqin; Lin, Dongdong; Mo, Yuxiang Physical Chemistry Chemical Physics, Vol. 21, Issue 7 https://doi.org/10.1039/c8cp07501h	journal	January 2019
Extensive tests and evaluation of the CHARMM36IDPSFF force field for intrinsically disordered proteins and folded proteins Liu, Hao; Song, Dong; Zhang, Yangpeng Physical Chemistry Chemical Physics, Vol. 21, Issue 39 https://doi.org/10.1039/c9cp03434j	journal	January 2019
Early-stage human islet amyloid polypeptide aggregation: Mechanisms behind dimer formation Guo, Ashley Z.; Fluitt, Aaron M.; de Pablo, Juan J. The Journal of Chemical Physics, Vol. 149, Issue 2 https://doi.org/10.1063/1.5033458	journal	July 2018
Phase space and collective variable based simulation methods for studies of rare events Paul, Sanjib; Nair, Nisanth N.; Vashisth, Harish Molecular Simulation, Vol. 45, Issue 14-15 https://doi.org/10.1080/08927022.2019.1634268	journal	June 2019
Secondary structures transition of tau protein with intrinsically disordered proteins specific force field Dan, Aohuan; Chen, Hai-Feng Chemical Biology & Drug Design, Vol. 93, Issue 3 https://doi.org/10.1111/cbdd.13407	journal	October 2018
Seed-Induced Heterogeneous Cross-Seeding Self-Assembly of Human and Rat Islet Polypeptides Hu, Rundong; Ren, Baiping; Zhang, Mingzhen ACS Omega, Vol. 2, Issue 3 https://doi.org/10.1021/acsomega.6b00559	journal	March 2017
Site-specific detection of protein secondary structure using 2D IR dihedral indexing: a proposed assembly mechanism of oligomeric hIAPP Maj, Michał; Lomont, Justin P.; Rich, Kacie L. Chemical Science, Vol. 9, Issue 2 https://doi.org/10.1039/c7sc03789a	journal	January 2018
Effects of forcefield and sampling method in all-atom simulations of inherently disordered proteins: Application to conformational preferences of human amylin Peng, Enxi; Todorova, Nevena; Yarovsky, Irene PLOS ONE, Vol. 12, Issue 10 https://doi.org/10.1371/journal.pone.0186219	journal	October 2017
Characterisation of the Structure and Oligomerisation of Islet Amyloid Polypeptides (IAPP): A Review of Molecular Dynamics Simulation Studies Moore, Sandra; Sonar, Krushna; Bharadwaj, Prashant Molecules, Vol. 23, Issue 9 https://doi.org/10.3390/molecules23092142	journal	August 2018

Similar Records

Characterization of Aβ Monomers through the Convergence of Ensemble Properties among Simulations with Multiple Force Fields

Journal Article · Tue Jan 12 00:00:00 EST 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1249116

Rosenman, David J.; Wang, Chunyu; García, Angel E.

Rapid assessment of human amylin aggregation and its inhibition by copper(II) ions by laser ablation electrospray ionization mass spectrometry with ion mobility separation

Journal Article · Wed Sep 09 00:00:00 EDT 2015 · Analytical Chemistry · OSTI ID:1249116

Li, Hang; Ha, Emmeline; Donaldson, Robert P.; +2 more

The structure and IR signatures of the arginine-glutamate salt bridge. Insights from the classical MD simulations

Journal Article · Sun Jun 07 00:00:00 EDT 2015 · Journal of Chemical Physics · OSTI ID:1249116

Odinokov, A. V.; Wehmeyer, C.; Sebastiani, D.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
free energy
biochemical simulations
molecular dynamics
proline
amyloid proteins
intermolecular forces
protein structure prediction
diabetes mellitus
oligomers
molecular structure

Title: Secondary structure of rat and human amylin across force fields

Citation Formats

References (117)

Cited By (12)

Similar Records

Related Subjects