Structural and Mechanical Properties of Amyloid Beta Fibrils: A Combined Experimental and Theoretical Approach

Overview

Journal J Phys Chem Lett

Publisher American Chemical Society

Specialty Chemistry

Date 2016 Jul 9

PMID 27387853

Citations 11

Authors

Thomas J Paul

Zachary Hoffmann

Congzhou Wang

Maruda Shanmugasundaram

Jason DeJoannis

Alexander Shekhtman

Igor K Lednev

Vamsi K Yadavalli

Rajeev Prabhakar

Affiliations

Soon will be listed here.

Abstract

In this combined experimental (deep ultraviolet resonance Raman (DUVRR) spectroscopy and atomic force microscopy (AFM)) and theoretical (molecular dynamics (MD) simulations and stress-strain (SS)) study, the structural and mechanical properties of amyloid beta (Aβ40) fibrils have been investigated. The DUVRR spectroscopy and AFM experiments confirmed the formation of linear, unbranched and β-sheet rich fibrils. The fibrils (Aβ40)n, formed using n monomers, were equilibrated using all-atom MD simulations. The structural properties such as β-sheet character, twist, interstrand distance, and periodicity of these fibrils were found to be in agreement with experimental measurements. Furthermore, Young's modulus (Y) = 4.2 GPa computed using SS calculations was supported by measured values of 1.79 ± 0.41 and 3.2 ± 0.8 GPa provided by two separate AFM experiments. These results revealed size dependence of structural and material properties of amyloid fibrils and show the utility of such combined experimental and theoretical studies in the design of precisely engineered biomaterials.

Citing Articles

From Research to Diagnostic Application of Raman Spectroscopy in Neurosciences: Past and Perspectives.

Klamminger G, Frauenknecht K, Mittelbronn M, Kleine Borgmann F Free Neuropathol. 2023; 3.

PMID: 37284145 PMC: 10209863. DOI: 10.17879/freeneuropathology-2022-4210.

Structure of Anabaena flos-aquae gas vesicles revealed by cryo-ET.

Dutka P, Metskas L, Hurt R, Salahshoor H, Wang T, Malounda D Structure. 2023; 31(5):518-528.e6.

PMID: 37040766 PMC: 10185304. DOI: 10.1016/j.str.2023.03.011.

The physical basis of fabrication of amyloid-based hydrogels by lysozyme.

Kumari A, Ahmad B RSC Adv. 2022; 9(64):37424-37435.

PMID: 35542254 PMC: 9075597. DOI: 10.1039/c9ra07179b.

A central role for amyloid fibrin microclots in long COVID/PASC: origins and therapeutic implications.

Kell D, Laubscher G, Pretorius E Biochem J. 2022; 479(4):537-559.

PMID: 35195253 PMC: 8883497. DOI: 10.1042/BCJ20220016.

Label-Free Infrared Spectroscopic Imaging Reveals Heterogeneity of β-Sheet Aggregates in Alzheimer's Disease.

Confer M, Holcombe B, Foes A, Holmquist J, Walker S, Deb S J Phys Chem Lett. 2021; 12(39):9662-9671.

PMID: 34590866 PMC: 8933041. DOI: 10.1021/acs.jpclett.1c02306.

References

Xu Z, Paparcone R, Buehler M . Alzheimer's abeta(1-40) amyloid fibrils feature size-dependent mechanical properties. Biophys J. 2010; 98(10):2053-62. PMC: 2872369. DOI: 10.1016/j.bpj.2009.12.4317. View

Nielsen L, Frokjaer S, Carpenter J, Brange J . Studies of the structure of insulin fibrils by Fourier transform infrared (FTIR) spectroscopy and electron microscopy. J Pharm Sci. 2000; 90(1):29-37. DOI: 10.1002/1520-6017(200101)90:1<29::aid-jps4>3.0.co;2-4. View

Serpell L, Sunde M, Benson M, Tennent G, Pepys M, Fraser P . The protofilament substructure of amyloid fibrils. J Mol Biol. 2000; 300(5):1033-9. DOI: 10.1006/jmbi.2000.3908. View

Hamada D, Yanagihara I, Tsumoto K . Engineering amyloidogenicity towards the development of nanofibrillar materials. Trends Biotechnol. 2004; 22(2):93-7. DOI: 10.1016/j.tibtech.2003.12.003. View

Hamley I . The amyloid beta peptide: a chemist's perspective. Role in Alzheimer's and fibrillization. Chem Rev. 2012; 112(10):5147-92. DOI: 10.1021/cr3000994. View

Hussein K, Park K, Kang K, Woo H . Biocompatibility evaluation of tissue-engineered decellularized scaffolds for biomedical application. Mater Sci Eng C Mater Biol Appl. 2016; 67:766-778. DOI: 10.1016/j.msec.2016.05.068. View

Teo A, Mishra A, Park I, Kim Y, Park W, Yoon Y . Polymeric Biomaterials for Medical Implants and Devices. ACS Biomater Sci Eng. 2021; 2(4):454-472. DOI: 10.1021/acsbiomaterials.5b00429. View

Petkova A, Ishii Y, Balbach J, Antzutkin O, Leapman R, Delaglio F . A structural model for Alzheimer's beta -amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci U S A. 2002; 99(26):16742-7. PMC: 139214. DOI: 10.1073/pnas.262663499. View

Choi B, Yoon G, Lee S, Eom K . Mechanical deformation mechanisms and properties of amyloid fibrils. Phys Chem Chem Phys. 2014; 17(2):1379-89. DOI: 10.1039/c4cp03804e. View

10.

Khurana R, Ionescu-Zanetti C, Pope M, Li J, Nielson L, Ramirez-Alvarado M . A general model for amyloid fibril assembly based on morphological studies using atomic force microscopy. Biophys J. 2003; 85(2):1135-44. PMC: 1303232. DOI: 10.1016/S0006-3495(03)74550-0. View

11.

Hauser C, Maurer-Stroh S, Martins I . Amyloid-based nanosensors and nanodevices. Chem Soc Rev. 2014; 43(15):5326-45. DOI: 10.1039/c4cs00082j. View

12.

Wang X, Li Y, Zhong C . Amyloid-directed assembly of nanostructures and functional devices for bionanoelectronics. J Mater Chem B. 2020; 3(25):4953-4958. DOI: 10.1039/c5tb00374a. View

13.

Adamcik J, Jung J, Flakowski J, De Los Rios P, Dietler G, Mezzenga R . Understanding amyloid aggregation by statistical analysis of atomic force microscopy images. Nat Nanotechnol. 2010; 5(6):423-8. DOI: 10.1038/nnano.2010.59. View

14.

Irimia-Vladu M . "Green" electronics: biodegradable and biocompatible materials and devices for sustainable future. Chem Soc Rev. 2013; 43(2):588-610. DOI: 10.1039/c3cs60235d. View

15.

Wang J, Zhao X, Li J, Kuang X, Fan Y, Wei G . Electrostatic Assembly of Peptide Nanofiber-Biomimetic Silver Nanowires onto Graphene for Electrochemical Sensors. ACS Macro Lett. 2022; 3(6):529-533. DOI: 10.1021/mz500213w. View

16.

Mankar S, Anoop A, Sen S, Maji S . Nanomaterials: amyloids reflect their brighter side. Nano Rev. 2011; 2. PMC: 3215191. DOI: 10.3402/nano.v2i0.6032. View

17.

Assenza S, Adamcik J, Mezzenga R, De Los Rios P . Universal behavior in the mesoscale properties of amyloid fibrils. Phys Rev Lett. 2015; 113(26):268103. DOI: 10.1103/PhysRevLett.113.268103. View

18.

Lu K, Jacob J, Thiyagarajan P, Conticello V, Lynn D . Exploiting amyloid fibril lamination for nanotube self-assembly. J Am Chem Soc. 2003; 125(21):6391-3. DOI: 10.1021/ja0341642. View

19.

Shashilov V, Sikirzhytski V, Popova L, Lednev I . Quantitative methods for structural characterization of proteins based on deep UV resonance Raman spectroscopy. Methods. 2010; 52(1):23-37. DOI: 10.1016/j.ymeth.2010.05.004. View

20.

Li C, Adamcik J, Mezzenga R . Biodegradable nanocomposites of amyloid fibrils and graphene with shape-memory and enzyme-sensing properties. Nat Nanotechnol. 2012; 7(7):421-7. DOI: 10.1038/nnano.2012.62. View