Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T19:33:43.121Z Has data issue: false hasContentIssue false
  • English
  • Français

A Comparative Study on the Self-Assembly of Peptide TGV-9 by In Situ Atomic Force Microscopy

Published online by Cambridge University Press:  13 February 2020

Yaping Li ,
Na Li ,
Lei Wang ,
Qinhua Lu ,
Xiang Ji  and
Feng Zhang Open the ORCID record for Feng Zhang [Opens in a new window]
Yaping Li
Affiliation:
School of Life Science and Technology, Inner Mongolia University of Science and Technology, Baotou014010, P. R. China
Na Li
Affiliation:
Terahertz Technology Innovation Research Institute, Shanghai Key Laboratory of Modern Optical System, Terahertz Science Cooperative Innovation Center, University of Shanghai for Science and Technology, 516 Jungong Road, Shanghai200093, P. R. China Biomedical Nanocenter, School of Life Science, Inner Mongolia Agricultural University, Hohhot010018, P. R. China
Lei Wang
Affiliation:
School of Life Science and Technology, Inner Mongolia University of Science and Technology, Baotou014010, P. R. China
Qinhua Lu
Affiliation:
School of Life Science and Technology, Inner Mongolia University of Science and Technology, Baotou014010, P. R. China
Xiang Ji*
Affiliation:
School of Life Science and Technology, Inner Mongolia University of Science and Technology, Baotou014010, P. R. China
Feng Zhang*
Affiliation:
School of Life Science and Technology, Inner Mongolia University of Science and Technology, Baotou014010, P. R. China Biomedical Nanocenter, School of Life Science, Inner Mongolia Agricultural University, Hohhot010018, P. R. China Key Laboratory of Oral Medicine, Department of Biomedical Engineering, School of Basic Medical Sciences, Guangzhou Institute of Oral Disease, Stomatology Hospital, Guangzhou Medical University, Guangzhou511436, P. R. China
*
*Authors for correspondence: Xiang Ji, E-mail: [email protected]; Feng Zhang, E-mail: [email protected]
*Authors for correspondence: Xiang Ji, E-mail: [email protected]; Feng Zhang, E-mail: [email protected]
Get access

Abstract

Previous studies of amyloid diseases reported that the aggregating proteins share a similar conserved peptide sequence which can form the cross-β-sheet-containing nanostructures like nanofilaments. The template-assisted self-assembly (TASA) of peptides on inorganic substrates with different hydrophilicity could be an alternative approach to shed light on the fibrillization mechanism of proteins/peptides in vivo. To figure out the effect of interfaces on amyloid aggregation, we herein employed in situ atomic force microscopy (AFM) to investigate the self-assembling of a Parkinson disease-related core peptide sequence (TGV-9) on a hydrophobic liquid–solid interface via real-time observation of the dynamic fibrillization process. The results show that TGV-9 forms one-dimensional nanostructures on the surface of highly ordered pyrolytic graphite (HOPG) with three preferred growth orientations, which are consistent with the atomic lattice of HOPG, indicating an epitaxial growth or TASA. Conversely, the nanostructures formed in bulk solution can be free-standing nanofilaments, and the fibrillization mechanism is different from that on HOPG. These results could not only deepen the understanding of the protein/peptide aggregation mechanism but also benefit for the early diagnosis and clinic treatment of related diseases.

Keywords

in situ atomic force microscopynanofilamenttemplate-assisted self-assemblyTGV-9α-synuclein
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 26 , Issue 2 , April 2020 , pp. 319 - 325
Copyright
Copyright © Microscopy Society of America 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agnati, LF, Leo, G, Genedani, S, Piron, L, Rivera, A, Guidolin, D & Fuxe, K (2009). Common key-signals in learning and neurodegeneration: Focus on excito-amino acids, β-amyloid peptides and α-synuclein. J Neural Transm 116(8), 953–974.CrossRefGoogle ScholarPubMed
Aguzzi, A & O'Connor, T (2010). Protein aggregation diseases: Pathogenicity and therapeutic perspectives. Nat Rev Drug Discov 9(3), 237–248.CrossRefGoogle ScholarPubMed
Arce, FT, Jang, H, Ramachandran, S, Landon, PB, Nussinov, R & Lal, R (2011). Polymorphism of amyloid β peptide in different environments: Implications for membrane insertion and pore formation. Soft Matter 7(11), 5267.CrossRefGoogle ScholarPubMed
Biancalana, M & Koide, S (2010). Molecular mechanism of Thioflavin-T binding to amyloid fibrils. BBA-Proteins Proteom 1804(7), 1405–1412.CrossRefGoogle ScholarPubMed
Chaves, RS, Melo, TQ, Martins, SA & Ferrari, MF (2010). Protein aggregation containing beta-amyloid, alpha-synuclein and hyperphosphorylated tau in cultured cells of hippocampus, substantia nigra and locus coeruleus after rotenone exposure. BMC Neurosci 11(1), 144–144.CrossRefGoogle ScholarPubMed
Chitnumsub, P, Fiori, WR, Lashuel, HA, Diaz, H & Kelly, JW (1999). The nucleation of monomeric parallel β-sheet-like structures and their self-assembly in aqueous solution. Bioorg Med Chem 7(1), 39.CrossRefGoogle ScholarPubMed
Choi, J-S, Braymer, JJ, Nanga, RPR, Ramamoorthy, A & Lim, MH (2010). Design of small molecules that target metal-Aβ species and regulate metal-induced Aβ aggregation and neurotoxicity. Proc Natl Acad Sci USA 107(51), 21990–21995.CrossRefGoogle ScholarPubMed
Du, Q, Dai, B, Hou, J, Hu, J, Zhang, F & Zhang, Y (2015). A comparative study on the self-assembly of an amyloid-like peptide at water-solid interfaces and in bulk solutions. Microsc Res Tech 78(5), 375–381.CrossRefGoogle ScholarPubMed
Du, HN, Li, H-T, Zhang, F, Lin, X-J, Shi, J-H, Shi, Y-H, Ji, L-N, Hu, J, Lin, D-H & Hu, H-Y (2006). Acceleration of α-synuclein aggregation by homologous peptides. FEBS Lett 580(15), 3657–3664.CrossRefGoogle ScholarPubMed
Du, HN, Tang, L, Luo, XY, Li, HT, Hu, J, Zhou, JW & Hu, HY (2003). A peptide motif consisting of glycine, alanine, and valine is required for the fibrillization and cytotoxicity of human α-synuclein. Biochemistry 42, 8870–8878.CrossRefGoogle ScholarPubMed
Eisenberg, DS & Sawaya, MR (2017). Structural studies of amyloid proteins at the molecular level. Annu Rev Biochem 61(Suppl), 8.Google Scholar
Evangelia, E, Dimitris, E, Themis, P, Georgios, S, Kyriaki, G, Ioannou, CP & Vekrellis, K (2011). Assessment of α-synuclein secretion in mouse and human brain parenchyma. PLoS ONE 6(7), e22225.Google Scholar
Fowler, DM, Koulov, AV, Alory-Jost, C, Marks, MS, Balch, WE & Kelly, JW (2005). Functional amyloid formation within mammalian tissue. PLoS Biol 4(1), e6.CrossRefGoogle Scholar
Hansma, P, Elings, V, Marti, O & Bracker, C (1988). Scanning tunneling microscopy and atomic force microscopy: Application to biology and technology. Science 242(4876), 209–216.CrossRefGoogle ScholarPubMed
Hillner, PE, Manne, S, Hansma, PK & Gratz, AJ (1993). Atomic force microscope: A new tool for imaging crystal growth processes. Faraday Discuss 95(95), 191–197.CrossRefGoogle Scholar
Hou, JH, Du, QQG, Zhong, RB, Zhang, P & Zhang, F (2014). Temperature manipulating peptide self-assembly in water nanofilm. Nucl Sci Tech 25(6), 060502.Google Scholar
Hoyer, W, Cherny, DV & Jovin, TM (2004). Rapid self-assembly of alpha-synuclein observed by in situ atomic force microscopy. J Mol Biol 340(1), 127–139.CrossRefGoogle ScholarPubMed
Kad, NM, Myers, SL, Smith, DP, Smith, DA, Radford, SE & Thomson, NH (2003). Hierarchical assembly of beta(2)-microglobulin amyloid in vitro revealed by atomic force microscopy. J Mol Biol 330(4), 785–797.CrossRefGoogle ScholarPubMed
Kang, SG, Huynh, T, Xia, Z, Zhang, Y, Fang, H, Wei, G & Zhou, R (2013). Hydrophobic interaction drives surface-assisted epitaxial assembly of amyloid-like peptides. J Am Chem Soc 135(8), 3150–3157.CrossRefGoogle ScholarPubMed
Kellermayer, MSZ, Karsai, A, Benke, M, Soos, K & Penke, B (2008). Stepwise dynamics of epitaxially growing single amyloid fibrils. Proc Natl Acad Sci USA 105(1), 141–144.CrossRefGoogle ScholarPubMed
Khurana, R, Coleman, C, Ionescu-Zanetti, C, Carter, SA, Krishna, V, Grover, RK, Roy, R & Singh, S (2005). Mechanism of thioflavin T binding to amyloid fibrils. J Struct Biol 151(3), 229–238.CrossRefGoogle ScholarPubMed
Kowalewski, T & Holtzman, DM (1999). In situ atomic force microscopy study of Alzheimer's beta-amyloid peptide on different substrates: New insights into mechanism of beta-sheet formation. Proc Natl Acad Sci USA 96(7), 3688–3693.CrossRefGoogle ScholarPubMed
Kuroda, Y, Maeda, Y, Hanaoka, H, Miyamoto, K & Nakagawa, T (2004). Oligopeptide-mediated acceleration of amyloid fibril formation of amyloidβ(Aβ) and α-synuclein fragment peptide (NAC). J Pept Sci 10(1), 8–17.CrossRefGoogle Scholar
Li, N, Jang, H, Yuan, M, Li, W, Yun, X, Lee, J, Du, Q, Nussinov, R, Hou, J & Lal, R (2017). Graphite-templated amyloid nanostructures formed by a potential pentapeptide inhibitor for Alzheimer's disease: A combined study of real-time atomic force microscopy and molecular dynamics simulations. Langmuir 33, 27.Google ScholarPubMed
Lou, S, Wang, X, Yu, Z & Shi, L (2019). Peptide tectonics: Encoded structural complementarity dictates programmable self-assembly. Adv Sci 6(13), 1802043.CrossRefGoogle ScholarPubMed
Murphy, DD, Rueter, SM, Trojanowski, JQ & Lee, VM-Y (2000). Synucleins are developmentally expressed, and α-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J Neurosci 20(9), 3214–3220.CrossRefGoogle ScholarPubMed
Nievergelt, AP, Banterle, N, Andany, SH, Gonczy, P & Fantner, GE (2018). High-speed photothermal off-resonance atomic force microscopy reveals assembly routes of centriolar scaffold protein SAS-6. Nat Nanotechnol 13(8), 696–701.CrossRefGoogle ScholarPubMed
Pantoja-Uceda, D, Santiveri, CM & Jiménez, MA (2006). De novo design of monomeric β-hairpin and β-sheet peptides. Methods Mol Biol 340, 27–51.Google ScholarPubMed
Shahmoradian, SH, Lewis, AJ, Genoud, C, Hench, J, Moors, TE, Navarro, PP, Castaño-Díez D, Schweighauser, G, Graff-Meyer, A, Goldie, KN, Sütterlin, R, Huisman, E, Ingrassia, A, Gier, Y, Rozemuller, AJM, Wang, J, Paepe, AD, Erny, J, Staempfli, A, Hoernschemeyer, J, Großerüschkamp, F, Niedieker, D, El-Mashtoly, SF, Quadri, M, Van Ijcken, WFJ, Bonifati, V, Gerwert, K, Bohrmann, B, Frank, S, Britschgi, M, Stahlberg, H, Van de Berg, WDJ & Lauer, ME (2019). Lewy pathology in Parkinson's disease consists of crowded organelles and lipid membranes. Nat Neurosci 22(7), 1099–1109.CrossRefGoogle ScholarPubMed
Takeuchi, A, Ohtsuki, C, Kamitakahara, M, Ogata, S-i, Miyazaki, T & Tanihara, M (2008). Biomimetic deposition of hydroxyapatite on a synthetic polypeptide with β sheet structure in a solution mimicking body fluid. J Mater Sci Mater Med 19(1), 387–393.CrossRefGoogle Scholar
Whitehouse, C, Fang, J, Aggeli, A, Bell, M & Boden, N (2010). Adsorption and self-assembly of peptides on mica substrates. Angew Chem Int Ed Engl 44(13), 1965–1968.CrossRefGoogle Scholar
Yang, GC, Woodhouse, KA & Yip, CM (2002). Substrate-facilitated assembly of elastin-like peptides: Studies by variable-temperature in situ atomic force microscopy. J Am Chem Soc 124(36), 10648–10649.CrossRefGoogle ScholarPubMed
Yin, Y, Lu, Y, Gates, B & Xia, Y (2001). Template-assisted self-assembly: A practical route to complex aggregates of monodispersed colloids with well-defined sizes, shapes, and structures. J Am Chem Soc 123(36), 8718–8729.CrossRefGoogle ScholarPubMed
Yoo, SI, Yang, M, Subramanian, V, Brender, JR, Sun, K, Joo, NE, Jeong, SH, Ramamoorthy, A & Kotov, NA (2011). Mechanism of fibrillation inhibition of amyloid peptides by inorganic nanoparticles reveal functional similarities with proteins. Angew Chem Int Ed 50(22), 5110.CrossRefGoogle Scholar
You, SK, Lim, D, Kim, JY, Kang, SJ, Kim, Y-H & Im, H (2009). β-Sheet-breaking peptides inhibit the fibrillation of human α-synuclein. Biochem Biophys Res Commun 387(4), 682–687.Google Scholar
Yun, X, Tang, M, Yang, Z, Wilksch, JJ, Xiu, P, Gao, H, Zhang, F & Wang, H (2017). Interrogation of drug effects on HeLa cells by exploiting new AFM mechanical biomarkers. RSC Adv 7(69), 43764–43771.CrossRefGoogle Scholar
Zhang, F, Du, HN, Zhang, ZX, Ji, LN, Li, HT, Tang, L, Wang, HB, Fan, CH, Xu, HJ, Zhang, Y, Hu, J, Hu, HY & He, JH (2006). Epitaxial growth of peptide nanofilaments on inorganic surfaces: Effects of interfacial hydrophobicity/hydrophilicity. Angew Chem Int Ed 45(22), 3611–3613.CrossRefGoogle ScholarPubMed
Zhang, F, Zhang, P, Hou, J, Yun, X, Li, W, Du, Q & Chen, Y (2015). Large scale anomalous patterns of muscovite mica discovered by atomic force microscopy. ACS Appl Mater Interfaces 7(16), 8699–8705.CrossRefGoogle ScholarPubMed