ACS Publications. Most Trusted. Most Cited. Most Read
CONTENT TYPES

System Message

The ACS Publications site will be temporarily unavailable for planned maintenance on Friday, Oct. 15 starting at 6:00 pm ET for up to 4 hours. We apologize for this inconvenience.

Correlation between Nanomechanics and Polymorphic Conformations in Amyloid Fibrils

View Author Information
Food & Soft Materials Science, Department of Health Science & Technology, ETH Zurich, Schmelzbergstrasse 9, LFO E23, 8092 Zurich, Switzerland
*Address correspondence to [email protected]
Cite this: ACS Nano 2014, 8, 11, 11035–11041
Publication Date (Web):October 2, 2014
https://doi.org/10.1021/nn503530a
Copyright © 2014 American Chemical Society
Article Views
1617
Altmetric
-
Citations
LEARN ABOUT THESE METRICS
Read OnlinePDF (3 MB)
Supporting Info (1)»

Abstract

Abstract Image

Amyloid fibrils occur in diverse morphologies, but how polymorphism affects the resulting mechanical properties is still not fully appreciated. Using formalisms from the theory of elasticity, we propose an original way of averaging the second area moment of inertia for non-axisymmetric fibrils, which constitutes the great majority of amyloid fibrils. By following this approach, we derive theoretical expressions for the bending properties of the most common polymorphic forms of amyloid fibrils (twisted ribbons, helical ribbons, and nanotubes), and we benchmark the predictions to experimental cases. These results not only allow an accurate estimation of the amyloid fibrils’ elastic moduli but also bring insight into the structure–property relationships in the nanomechanics of amyloid systems, such as in the closure of helical ribbons into nanotubes.

Supporting Information

ARTICLE SECTIONS
Jump To

Brief commentaries for the pure bending of a transversally loaded beam; exact solution for the twisted ribbon persistence length on number of protofilament, n, dependence; area moment of inertia vs neutral axis position for a nanotube. This material is available free of charge via the Internet at http://pubs.acs.org.

Terms & Conditions

Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Cited By


This article is cited by 41 publications.

  1. Jiangtao Zhou, Leonardo Venturelli, Ludovic Keiser, Sergey K. Sekatskii, François Gallaire, Sandor Kasas, Giovanni Longo, Tuomas P. J. Knowles, Francesco S. Ruggeri, Giovanni Dietler. Environmental Control of Amyloid Polymorphism by Modulation of Hydrodynamic Stress. ACS Nano 2021, 15 (1) , 944-953. https://doi.org/10.1021/acsnano.0c07570
  2. Francesco Simone Ruggeri, Patrick Flagmeier, Janet R. Kumita, Georg Meisl, Dimitri Y. Chirgadze, Marie N. Bongiovanni, Tuomas P. J. Knowles, Christopher M. Dobson. The Influence of Pathogenic Mutations in α-Synuclein on Biophysical and Structural Characteristics of Amyloid Fibrils. ACS Nano 2020, 14 (5) , 5213-5222. https://doi.org/10.1021/acsnano.9b09676
  3. Ke Jiang, Daren Xu, Ziwen Ma, Peng Yang, Yu Song, Wenke Zhang. Quantifying the Mechanical Anisotropy in Poly(3-hexylthiophene) Nanofibers. ACS Macro Letters 2020, 9 (1) , 108-114. https://doi.org/10.1021/acsmacrolett.9b00866
  4. Simon M. Loveday, A. Patrick Gunning. Nanomechanics of Pectin-Linked β-Lactoglobulin Nanofibril Bundles. Biomacromolecules 2018, 19 (7) , 2834-2840. https://doi.org/10.1021/acs.biomac.8b00408
  5. Christian Helbing, Tanja Deckert-Gaudig, Izabela Firkowska-Boden, Gang Wei, Volker Deckert, and Klaus D. Jandt . Protein Handshake on the Nanoscale: How Albumin and Hemoglobin Self-Assemble into Nanohybrid Fibers. ACS Nano 2018, 12 (2) , 1211-1219. https://doi.org/10.1021/acsnano.7b07196
  6. Zhe Wang, Fuwu Zhang, Zhantong Wang, Yijing Liu, Xiao Fu, Albert Jin, Bryant C. Yung, Wei Chen, Jing Fan, Xiangyu Yang, Gang Niu, and Xiaoyuan Chen . Hierarchical Assembly of Bioactive Amphiphilic Molecule Pairs into Supramolecular Nanofibril Self-Supportive Scaffolds for Stem Cell Differentiation. Journal of the American Chemical Society 2016, 138 (45) , 15027-15034. https://doi.org/10.1021/jacs.6b09014
  7. Fengyun Guo, Nü Wang, Qunfeng Cheng, Lanlan Hou, Jingchong Liu, Yanlei Yu, and Yong Zhao . Low-Cost Coir Fiber Composite with Integrated Strength and Toughness. ACS Sustainable Chemistry & Engineering 2016, 4 (10) , 5450-5455. https://doi.org/10.1021/acssuschemeng.6b00830
  8. Yang Hu, Ran Lin, Pengcheng Zhang, Joshua Fern, Andrew G. Cheetham, Kunal Patel, Rebecca Schulman, Chengyou Kan, and Honggang Cui . Electrostatic-Driven Lamination and Untwisting of β-Sheet Assemblies. ACS Nano 2016, 10 (1) , 880-888. https://doi.org/10.1021/acsnano.5b06011
  9. Ivan Usov and Raffaele Mezzenga . FiberApp: An Open-Source Software for Tracking and Analyzing Polymers, Filaments, Biomacromolecules, and Fibrous Objects. Macromolecules 2015, 48 (5) , 1269-1280. https://doi.org/10.1021/ma502264c
  10. Yi-An Lin, Andrew G. Cheetham, Pengcheng Zhang, Yu-Chuan Ou, Yuguo Li, Guanshu Liu, Daniel Hermida-Merino, Ian W. Hamley, and Honggang Cui . Multiwalled Nanotubes Formed by Catanionic Mixtures of Drug Amphiphiles. ACS Nano 2014, 8 (12) , 12690-12700. https://doi.org/10.1021/nn505688b
  11. Nidhi Aggarwal, Dror Eliaz, Hagai Cohen, Irit Rosenhek-Goldian, Sidney R. Cohen, Anna Kozell, Thomas O. Mason, Ulyana Shimanovich. Protein nanofibril design via manipulation of hydrogen bonds. Communications Chemistry 2021, 4 (1) https://doi.org/10.1038/s42004-021-00494-2
  12. Yuhe Shen, Yuefei Wang, Ian W. Hamley, Wei Qi, Rongxin Su, Zhimin He. NChiral Self-Assembly of Peptides: toward the Design of Supramolecular Polymers with Enhanced Chemical and Biological Functions. Progress in Polymer Science 2021, 183 , 101469. https://doi.org/10.1016/j.progpolymsci.2021.101469
  13. Jozef Adamcik, Francesco Simone Ruggeri, Joshua T. Berryman, Afang Zhang, Tuomas P. J. Knowles, Raffaele Mezzenga. Evolution of Conformation, Nanomechanics, and Infrared Nanospectroscopy of Single Amyloid Fibrils Converting into Microcrystals. Advanced Science 2021, 8 (2) , 2002182. https://doi.org/10.1002/advs.202002182
  14. Qiying Feng, Yue Hong, Naga Pradeep Nidamanuri, Chuanxu Yang, Qiang Li, Mingdong Dong. Identification and Nanomechanical Characterization of the HIV Tat‐Amyloid β Peptide Multifibrillar Structures. Chemistry – A European Journal 2020, 26 (43) , 9449-9453. https://doi.org/10.1002/chem.201905715
  15. Jingjing Liu, Mengting Tian, Lei Shen. Surface effects on the degree of twist in amyloid fibril structures. Chemical Communications 2020, 56 (21) , 3147-3150. https://doi.org/10.1039/C9CC10079B
  16. . Nanomechanical Characterization of Apolipoprotein A-I Amyloid Fibrils. East European Journal of Physics 2020,,https://doi.org/10.26565/2312-4334-2020-2-11
  17. Francesco Simone Ruggeri, Tomas Šneideris, Michele Vendruscolo, Tuomas P.J. Knowles. Atomic force microscopy for single molecule characterisation of protein aggregation. Archives of Biochemistry and Biophysics 2019, 664 , 134-148. https://doi.org/10.1016/j.abb.2019.02.001
  18. Xinchen Ye, Christofer Lendel, Maud Langton, Richard T. Olsson, Mikael S. Hedenqvist. Protein nanofibrils: Preparation, properties, and possible applications in industrial nanomaterials. 2019,,, 29-63. https://doi.org/10.1016/B978-0-12-815749-7.00002-5
  19. Radoslaw Bomba, Witek Kwiatkowski, Antoni Sánchez-Ferrer, Roland Riek, Jason Greenwald. Cooperative Induction of Ordered Peptide and Fatty Acid Aggregates. Biophysical Journal 2018, 115 (12) , 2336-2347. https://doi.org/10.1016/j.bpj.2018.10.031
  20. Gustav Nyström, Raffaele Mezzenga. Liquid crystalline filamentous biological colloids: Analogies and differences. Current Opinion in Colloid & Interface Science 2018, 38 , 30-44. https://doi.org/10.1016/j.cocis.2018.08.004
  21. Jozef Adamcik, Raffaele Mezzenga. Amyloid‐Polymorphie in der Energielandschaft der Faltung und Aggregation von Proteinen. Angewandte Chemie 2018, 130 (28) , 8502-8515. https://doi.org/10.1002/ange.201713416
  22. Jozef Adamcik, Raffaele Mezzenga. Amyloid Polymorphism in the Protein Folding and Aggregation Energy Landscape. Angewandte Chemie International Edition 2018, 57 (28) , 8370-8382. https://doi.org/10.1002/anie.201713416
  23. V. Castelletto, I. W. Hamley. Methods to Characterize the Nanostructure and Molecular Organization of Amphiphilic Peptide Assemblies. 2018,,, 3-21. https://doi.org/10.1007/978-1-4939-7811-3_1
  24. Bumjoon Choi, Taehee Kim, Eue Soo Ahn, Sang Woo Lee, Kilho Eom. Mechanical Deformation Mechanisms and Properties of Prion Fibrils Probed by Atomistic Simulations. Nanoscale Research Letters 2017, 12 (1) https://doi.org/10.1186/s11671-017-1966-3
  25. Paola Cicatiello, Principia Dardano, Marinella Pirozzi, Alfredo M. Gravagnuolo, Luca De Stefano, Paola Giardina. Self-assembly of two hydrophobins from marine fungi affected by interaction with surfaces. Biotechnology and Bioengineering 2017, 114 (10) , 2173-2186. https://doi.org/10.1002/bit.26344
  26. Simon M. Loveday, Skelte G. Anema, Harjinder Singh. β-Lactoglobulin nanofibrils: The long and the short of it. International Dairy Journal 2017, 67 , 35-45. https://doi.org/10.1016/j.idairyj.2016.09.011
  27. Alina Hategan, Mario A Bianchet, Joseph Steiner, Elena Karnaukhova, Eliezer Masliah, Adam Fields, Myoung-Hwa Lee, Alex M Dickens, Norman Haughey, Emilios K Dimitriadis, Avindra Nath. HIV Tat protein and amyloid-β peptide form multifibrillar structures that cause neurotoxicity. Nature Structural & Molecular Biology 2017, 24 (4) , 379-386. https://doi.org/10.1038/nsmb.3379
  28. Guillaume Lamour, Roy Nassar, Patrick H.W. Chan, Gunes Bozkurt, Jixi Li, Jennifer M. Bui, Calvin K. Yip, Thibault Mayor, Hongbin Li, Hao Wu, Jörg A. Gsponer. Mapping the Broad Structural and Mechanical Properties of Amyloid Fibrils. Biophysical Journal 2017, 112 (4) , 584-594. https://doi.org/10.1016/j.bpj.2016.12.036
  29. Hyun Joon Chang, Myeongsang Lee, Jae In Kim, Gwonchan Yoon, Sungsoo Na. Mechanical and vibrational characterization of amyloid-like HET-s nanosheets based on the skewed plate theory. Physical Chemistry Chemical Physics 2017, 19 (18) , 11492-11501. https://doi.org/10.1039/C7CP01418J
  30. Ali Makky, Luc Bousset, Jérôme Polesel-Maris, Ronald Melki. Nanomechanical properties of distinct fibrillar polymorphs of the protein α-synuclein. Scientific Reports 2016, 6 (1) https://doi.org/10.1038/srep37970
  31. Yang Hu, Ran Lin, Kunal Patel, Andrew G. Cheetham, Chengyou Kan, Honggang Cui. Spatiotemporal control of the creation and immolation of peptide assemblies. Coordination Chemistry Reviews 2016, 320-321 , 2-17. https://doi.org/10.1016/j.ccr.2016.02.014
  32. A. V. Vargiu, D. Iglesias, K. E. Styan, L. J. Waddington, C. D. Easton, S. Marchesan. Design of a hydrophobic tripeptide that self-assembles into amphiphilic superstructures forming a hydrogel biomaterial. Chemical Communications 2016, 52 (35) , 5912-5915. https://doi.org/10.1039/C5CC10531E
  33. M. G. Santangelo, V. Foderà, V. Militello, V. Vetri. Back to the oligomeric state: pH-induced dissolution of concanavalin A amyloid-like fibrils into non-native oligomers. RSC Advances 2016, 6 (79) , 75082-75091. https://doi.org/10.1039/C6RA16690C
  34. Yi-Chih Lin, Hiroaki Komatsu, Jianqiang Ma, Paul H. Axelsen, Zahra Fakhraai. Quantitative analysis of amyloid polymorphism using height histograms to correct for tip convolution effects in atomic force microscopy imaging. RSC Advances 2016, 6 (115) , 114286-114295. https://doi.org/10.1039/C6RA24031C
  35. Bumjoon Choi, Taehee Kim, Sang Woo Lee, Kilho Eom. Nanomechanical Characterization of Amyloid Fibrils Using Single-Molecule Experiments and Computational Simulations. Journal of Nanomaterials 2016, 2016 , 1-16. https://doi.org/10.1155/2016/5873695
  36. Gwonchan Yoon, Myeongsang Lee, Kyungwoo Kim, Jae In Kim, Hyun Joon Chang, Inchul Baek, Kilho Eom, Sungsoo Na. Morphology and mechanical properties of multi-stranded amyloid fibrils probed by atomistic and coarse-grained simulations. Physical Biology 2015, 12 (6) , 066021. https://doi.org/10.1088/1478-3975/12/6/066021
  37. Ivan Usov, Gustav Nyström, Jozef Adamcik, Stephan Handschin, Christina Schütz, Andreas Fall, Lennart Bergström, Raffaele Mezzenga. Understanding nanocellulose chirality and structure–properties relationship at the single fibril level. Nature Communications 2015, 6 (1) https://doi.org/10.1038/ncomms8564
  38. Valeriya M. Trusova. Protein Fibrillar Nanopolymers: Molecular-Level Insights into Their Structural, Physical and Mechanical Properties. Biophysical Reviews and Letters 2015, 10 (03) , 135-156. https://doi.org/10.1142/S1793048015300029
  39. Anthony W. P. Fitzpatrick, Giovanni M. Vanacore, Ahmed H. Zewail. Nanomechanics and intermolecular forces of amyloid revealed by four-dimensional electron microscopy. Proceedings of the National Academy of Sciences 2015, 112 (11) , 3380-3385. https://doi.org/10.1073/pnas.1502214112
  40. Ying Li, Yang Sun, Meng Qin, Yi Cao, Wei Wang. Mechanics of single peptide hydrogelator fibrils. Nanoscale 2015, 7 (13) , 5638-5642. https://doi.org/10.1039/C4NR07657E
  41. Ian William Hamley, Steven Kirkham, Radoslaw M. Kowalczyk, Valeria Castelletto, Mehedi Reza, Janne Ruokolainen. Self-assembly of the anti-fungal polyene amphotericin B into giant helically-twisted nanotapes. Chemical Communications 2015, 51 (100) , 17680-17683. https://doi.org/10.1039/C5CC08224B

Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

You’ve supercharged your research process with ACS and Mendeley!

STEP 1:
Click to create an ACS ID

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

MENDELEY PAIRING EXPIRED
Your Mendeley pairing has expired. Please reconnect

This website uses cookies to improve your user experience. By continuing to use the site, you are accepting our use of cookies. Read the ACS privacy policy.

CONTINUE