cross‐α structure; functional amyloids; green energy harvesting; helicity inversion; nanotechnology; peptide self‐assembly; piezoelectric biomaterials; cross-alpha structure
Abstract :
[en] Although initially identified as pathological aggregates, amyloid fibrillar assemblies formed by various proteins and peptides are now known to have crucial physiological roles, carrying out numerous biological functions in almost all organisms. Due to unique features, the common etiology of amyloids' cross-β structure is long posited as a template for designing artificial self-assembling systems. However, the recent discovery of cross-α amyloids indicates additional structural paradigms for self-assembly into ordered nanostructures, turning significant attention toward designing artificial nanostructures based on cross-α assembly. Herein, a minimalistic designer peptide which forms a hydrogen-bonded amyloid-like structure while remaining in the α region of conformation is engineered, to investigate the effect of aromatic, hydrophobic, and steric considerations on amyloidal assemblies. These results demonstrate a significant modulation of helicity and self-assembly, leading to the structure-dependent piezoelectric function of the amyloid-like cross-α fibrils. This study indicates a potential avenue for molecular engineering of functional peptide materials.
Research center :
ULHPC - University of Luxembourg: High Performance Computing
Disciplines :
Physical, chemical, mathematical & earth Sciences: Multidisciplinary, general & others
Author, co-author :
Dey, Sukantha; Department of Chemistry, Ashoka University, Sonipat, Haryana, 131029, India
Field, Emily H; Department of Biochemistry & Chemistry, La Trobe Institute for Molecular Science (LIMS), La Trobe University, Melbourne, Victoria, 3086, Australia
Wang, Yuehui; Key Laboratory of Biorheological Science and Technology, Ministry of Education, College of Bioengineering, Chongqing University, Chongqing, 400044, China
HAN, Kyunghoon ; University of Luxembourg > Faculty of Science, Technology and Medicine (FSTM) > Department of Physics and Materials Science (DPHYMS)
Kumar, Rohit; Department of Chemistry, Ashoka University, Sonipat, Haryana, 131029, India
Shimon, Linda J W; Department of Chemical Research Support, Weizmann Institute of Science, Rehovot, 76100, Israel
Liu, Shuaijie; Key Laboratory of Biorheological Science and Technology, Ministry of Education, College of Bioengineering, Chongqing University, Chongqing, 400044, China
Guerin, Sarah; Department of Chemical Sciences, Bernal Institute, University of Limerick, Limerick, V94 T9PX, Ireland ; SSPC, The Science Foundation Ireland Research Centre for Pharmaceuticals, University of Limerick, Limerick, V94 T9PX, Ireland
BERRYMAN, Josh ; University of Luxembourg > Faculty of Science, Technology and Medicine (FSTM) > Department of Physics and Materials Science (DPHYMS)
Ji, Wei; Key Laboratory of Biorheological Science and Technology, Ministry of Education, College of Bioengineering, Chongqing University, Chongqing, 400044, China
Reynolds, Nicholas P; Department of Biochemistry & Chemistry, La Trobe Institute for Molecular Science (LIMS), La Trobe University, Melbourne, Victoria, 3086, Australia ; The Biomedical and Environmental Sensor Technology (BEST) Research Centre, Biosensors Program, La Trobe Institute for Molecular Science (LIMS), La Trobe University, Melbourne, Victoria, 3086, Australia
Bera, Santu ; Department of Chemistry, Ashoka University, Sonipat, Haryana, 131029, India
External co-authors :
yes
Language :
English
Title :
Fluorination Induced Inversion of Helicity and Self-Assembly Into Cross-α Like Piezoelectric Amyloids by Minimalistic Designer Peptide.
M. G. Iadanza, M. P. Jackson, E. W. Hewitt, N. A. Ranson, S. E. Radford, Nat. Rev. Mol. Cell Biol. 2018, 19, 755.
P. C. Ke, R. Zhou, L. C. Serpell, R. Riek, T. P. J. Knowles, H. A. Lashuel, E. Gazit, I. W. Hamley, T. P. Davis, M. Fändrich, D. E. Otzen, M. R. Chapman, C. M. Dobson, D. S. Eisenberg, R. Mezzenga, Chem. Soc. Rev. 2020, 49, 5473.
M. R. Sawaya, M. P. Hughes, J. A. Rodriguez, R. Riek, D. S. Eisenberg, Cell 2021, 184, 4857.
X. Wang, S. Zhang, J. Zhang, Y. Wang, X. Jiang, Y. Tao, D. Li, C. Zhong, C. Liu, Chem. Soc. Rev. 2023, 52, 4603.
G. Wei, Z. Su, N. P. Reynolds, P. Arosio, I. W. Hamley, E. Gazit, R. Mezzenga, Chem. Soc. Rev. 2017, 46, 4661.
E. Tayeb-Fligelman, O. Tabachnikov, A. Moshe, O. Goldshmidt-Tran, M. R. Sawaya, N. Coquelle, J.-P. Colletier, M. Landau, Science 2017, 355, 831.
V. Daggett, Acc. Chem. Res. 2006, 39, 594.
S.-Q. Zhang, H. Huang, J. Yang, H. T. Kratochvil, M. Lolicato, Y. Liu, X. Shu, L. Liu, W. F. DeGrado, Nat. Chem. Biol. 2018, 14, 870.
F. Wang, O. Gnewou, C. Modlin, L. C. Beltran, C. Xu, Z. Su, P. Juneja, G. Grigoryan, E. H. Egelman, V. P. Conticello, Nat. Commun. 2021, 12, 407.
S. Bera, S. Mondal, B. Xue, L. J. W. Shimon, Y. Cao, E. Gazit, Nat. Mater. 2019, 18, 503.
S. Dey, R. Kumar, R. Mishra, S. Bera, Trends Biochem. Sci. 2024, 49, 1097.
M. Salwiczek, E. K. Nyakatura, U. I. M. Gerling, S. Ye, B. Koksch, Chem. Soc. Rev. 2012, 41, 2135.
A. A. Berger, J.-S. Völler, N. Budisa, B. Koksch, Acc. Chem. Res. 2017, 50, 2093.
B. C. Buer, J. L. Meagher, J. A. Stuckey, E. N. G. Marsh, Proc. Natl. Acad. Sci. USA 2012, 109, 4810.
S. S. Pendley, Y. B. Yu, T. E. Cheatham, Proteins 2009, 74, 612.
Y. Tang, G. Ghirlanda, N. Vaidehi, J. Kua, D. T. Mainz, W. A. Goddard, W. F. DeGrado, D. A. Tirrell, Biochemistry 2001, 40, 2790.
L. M. Gottler, H. Lee, C. E. Shelburne, A. Ramamoorthy, E. N. G. Marsh, ChemBioChem 2008, 9, 370.
A. Niemz, D. A. Tirrell, J. Am. Chem. Soc. 2001, 123, 7407.
M. A. Dominguez, K. C. Thornton, M. G. Melendez, C. M. Dupureur, Proteins 2001, 45, 55.
N. Voloshchuk, A. Y. Zhu, D. Snydacker, J. K. Montclare, Bioorg. Med. Chem. Lett. 2009, 19, 5449.
M. G. Woll, E. B. Hadley, S. Mecozzi, S. H. Gellman, J. Am. Chem. Soc. 2006, 128, 15932.
H. Zheng, J. Gao, Angew. Chem., Int. Ed. 2010, 49, 8635.
M. A. Cejas, W. A. Kinney, C. Chen, J. G. Vinter, H. R. Almond, K. M. Balss, C. A. Maryanoff, U. Schmidt, M. Breslav, A. Mahan, E. Lacy, B. E. Maryanoff, Proc. Natl. Acad. Sci. USA 2008, 105, 8513.
S. M. Butterfield, P. R. Patel, M. L. Waters, J. Am. Chem. Soc. 2002, 124, 9751.
Y. Suzuki, J. R. Brender, M. T. Soper, J. Krishnamoorthy, Y. Zhou, B. T. Ruotolo, N. A. Kotov, A. Ramamoorthy, E. N. G. Marsh, Biochemistry 2013, 52, 1903.
P. Wadhwani, E. Strandberg, N. Heidenreich, J. Bürck, S. Fanghänel, A. S. Ulrich, J. Am. Chem. Soc. 2012, 134, 6512.
F. T. Senguen, T. M. Doran, E. A. Anderson, B. L. Nilsson, Mol. BioSyst. 2011, 7, 497.
U. I. M. Gerling, M. Salwiczek, C. D. Cadicamo, H. Erdbrink, C. Czekelius, S. L. Grage, P. Wadhwani, A. S. Ulrich, M. Behrends, G. Haufe, B. Koksch, Chem. Sci. 2014, 5, 819.
A. M. Garcia, D. Iglesias, E. Parisi, K. E. Styan, L. J. Waddington, C. Deganutti, R. De Zorzi, M. Grassi, M. Melchionna, A. V. Vargiu, S. Marchesan, Chem 2018, 4, 1862.
D. Eisenberg, Proc. Natl. Acad. Sci. USA 2003, 100, 11207.
R. Parthasarathy, S. Chaturvedi, K. Go, Proc. Natl. Acad. Sci. USA 1990, 87, 871.
M. Novotny, G. J. Kleywegt, J. Mol. Biol. 2005, 347, 231.
J. Makowska, S. Rodziewicz-Motowidło, K. Bagińska, J. A. Vila, A. Liwo, L. Chmurzyński, H. A. Scheraga, Proc. Natl. Acad. Sci. USA 2006, 103, 1744.
H. Miyake, H. Kamon, I. Miyahara, H. Sugimoto, H. Tsukube, J. Am. Chem. Soc. 2008, 130, 792.
S. Zahn, J. W. Canary, Science 2000, 288, 1404.
K. Maeda, H. Mochizuki, M. Watanabe, E. Yashima, J. Am. Chem. Soc. 2006, 128, 7639.
A. L. Hofacker, J. R. Parquette, Angew. Chem. Int. Ed. 2005, 44, 1053.
H.-P. Chiu, Y. Suzuki, D. Gullickson, R. Ahmad, B. Kokona, R. Fairman, R. P. Cheng, J. Am. Chem. Soc. 2006, 128, 15556.
R. Nelson, M. R. Sawaya, M. Balbirnie, A. Ø. Madsen, C. Riekel, R. Grothe, D. Eisenberg, Nature 2005, 435, 773.
T. R. Jahn, G. A. Tennent, S. E. Radford, J. Biol. Chem. 2008, 283, 17279.
A. Bleem, R. Francisco, J. D. Bryers, V. Daggett, ngp Biofilms Microbioms 2017, 3, 16.
D.-H. Chin, R. W. Woody, C. A. Rohl, R. L. Baldwin, Proc. Natl. Acad. Sci. USA 2002, 99, 15416.
N. E. Shepherd, H. N. Hoang, G. Abbenante, D. P. Fairlie, J. Am. Chem. Soc. 2005, 127, 2974.
N. E. Shepherd, H. N. Hoang, G. Abbenante, D. P. Fairlie, J. Am. Chem. Soc. 2009, 131, 15877.
T. Yoshiya, T. Maruno, T. Uemura, S. Kubo, Y. Kiso, Y. Sohma, K. Yoshizawa-Kumagaye, Y. Kobayashi, Y. Nishiuchi, Bioorg. Med. Chem. Lett. 2014, 24, 3861.
J. Kellock, G. Hopping, B. Caughey, V. Daggett, J. Mol. Biol. 2016, 428, 2317.
N. P. Reynolds, J. Adamcik, J. T. Berryman, S. Handschin, A. A. H. Zanjani, W. Li, K. Liu, A. Zhang, R. Mezzenga, Nat. Commun. 2017, 8, 1338.
O. Sanislav, R. Tetaj, M. J. Ratcliffe, W. Phillips, A. R. Klein, A. Sethi, J. Zhou, R. Mezzenga, S. S. Saxer, M. Charnley, S. J. Annesley, N. P. Reynolds, Nanoscale 2024, 16, 19814.
R. Tycko, Curr. Opin. Struct. Biol. 2004, 14, 96.
J. Meinhardt, C. Sachse, P. Hortschansky, N. Grigorieff, M. Fändrich, J. Mol. Biol. 2009, 386, 869.
L. Bousset, L. Pieri, G. Ruiz-Arlandis, J. Gath, P. H. Jensen, B. Habenstein, K. Madiona, V. Olieric, A. Böckmann, B. H. Meier, R. Melki, Nat. Commun. 2013, 4, 2575.
C. Lara, J. Adamcik, S. Jordens, R. Mezzenga, Biomacromolecules 2011, 12, 1868.
J. Adamcik, A. Sánchez-Ferrer, N. Ait-Bouziad, N. P. Reynolds, H. A. Lashuel, R. Mezzenga, Angew. Chem. 2016, 128, 628.
S. Bera, S. Guerin, H. Yuan, J. O'Donnell, N. P. Reynolds, O. Maraba, W. Ji, L. J. W. Shimon, P.-A. Cazade, S. A. M. Tofail, D. Thompson, R. Yang, E. Gazit, Nat. Commun. 2021, 12, 2634.
T. P. J. Knowles, M. J. Buehler, Nat. Nanotechnol. 2011, 6, 469.
C. C. vandenAkker, M. F. M. Engel, K. P. Velikov, M. Bonn, G. H. Koenderink, J. Am. Chem. Soc. 2011, 133, 18030.
J. Adamcik, J.-M. Jung, J. Flakowski, P. De Los Rios, G. Dietler, R. Mezzenga, Nat. Nanotechnol. 2010, 5, 423.
J. Adamcik, F. S. Ruggeri, J. T. Berryman, A. Zhang, T. P. J. Knowles, R. Mezzenga, Adv. Sci. 2021, 8, 2002182.
I. Usov, R. Mezzenga, Macromolecules 2015, 48, 1269.
D. Dharmadana, N. P. Reynolds, C. Dekiwadia, C. E. Conn, C. Valéry, Nanoscale 2018, 10, 18195.
C. Lara, I. Usov, J. Adamcik, R. Mezzenga, Phys. Rev. Lett. 2011, 107, 238101.
M. Schleeger, C. C. vandenAkker, T. Deckert-Gaudig, V. Deckert, K. P. Velikov, G. Koenderink, M. Bonn, Polymer 2013, 54, 2473.
E. L. Guenther, P. Ge, H. Trinh, M. R. Sawaya, D. Cascio, D. R. Boyer, T. Gonen, Z. H. Zhou, D. S. Eisenberg, Nat. Struct. Mol. Biol. 2018, 25, 311.
D. A. Case, H. Metin Aktulga, K. Belfon, I. Y. Ben-Shalom, J. T. Berryman, S. R. Brozell, D. S. Cerutti, T. E. Cheatham, G. Andrés Cisneros, V. W. D. Cruzeiro, T. A. Darden, R. E. Duke, G. Giambasu, M. K. Gilson, H. Gohlke, A. W. Goetz, R. Harris, S. Izadi, S. A. Izmailov, K. Kasavajhala, M. C. Kaymak, E. King, A. Kovalenko, T. Kurtzman, T. Lee, S. LeGrand, P. Li, C. Lin, J. Liu, T. Luchko, et al., Amber, University of California, San Francisco 2022.
A. Hjorth Larsen, J. Jørgen Mortensen, J. Blomqvist, I. E. Castelli, R. Christensen, M. Dułak, J. Friis, M. N. Groves, B. Hammer, C. Hargus, E. D. Hermes, P. C. Jennings, P. Bjerre Jensen, J. Kermode, J. R. Kitchin, E. Leonhard Kolsbjerg, J. Kubal, K. Kaasbjerg, S. Lysgaard, J. Bergmann Maronsson, T. Maxson, T. Olsen, L. Pastewka, A. Peterson, C. Rostgaard, J. Schiøtz, O. Schütt, M. Strange, K. S. Thygesen, T. Vegge, et al., J. Phys.: Condens. Matter 2017, 29, 273002.
D. Svergun, C. Barberato, M. H. J. Koch, J. Appl. Crystallogr. 1995, 28, 768.
Z.-M. Zhang, S. Chen, Y.-Z. Liang, Analyst 2010, 135, 1138.
S.-J. Baek, A. Park, Y.-J. Ahn, J. Choo, Analyst 2015, 140, 250.
K. Han, A. Boziki, A. Tkatchenko, J. T. Berryman, ACS Omega 2024, 9, 49397.
J. Wang, R. M. Wolf, J. W. Caldwell, P. A. Kollman, D. A. Case, J. Comput. Chem. 2004, 25, 1157.
A. D. MacKerell, D. Bashford, M. Bellott, R. L. Dunbrack, J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, W. E. Reiher, B. Roux, M. Schlenkrich, J. C. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiórkiewicz-Kuczera, D. Yin, M. Karplus, J. Phys. Chem. B 1998, 102, 3586.
P. Mark, L. Nilsson, J. Phys. Chem. A 2001, 105, 9954.
S. Chen, X. Tong, Y. Huo, S. Liu, Y. Yin, M. L. Tan, K. Cai, W. Ji, Adv. Mater. 2024, 36, 2406192.
R. Kumar, S. Bera, Giant 2024, 17, 100214.
Y. Cheng, T. Wang, H. Zhu, X. Hu, J. Mi, L. Li, Y. Zhang, J. Yang, L. Dong, Y. Li, W. Sun, X. Lu, W. Wang, Y. Cao, B. Xue, Angew. Chem., Int. Ed. 2025, 202500334.
Y. Cheng, J. Xu, L. Li, P. Cai, Y. Li, Q. Jiang, W. Wang, Y. Cao, B. Xue, Adv. Sci. 2023, 10, 2207269.
T. Hu, J. P. Lee, P. Huang, A. J. Ong, J. Yu, S. Zhu, Y. Jiang, Z. Zhang, M. Reches, P. S. Lee, Adv. Mater. 2025, 37, 2413049.
D. Denning, J. I. Kilpatrick, E. Fukada, N. Zhang, S. Habelitz, A. Fertala, M. D. Gilchrist, Y. Zhang, S. A. M. Tofail, B. J. Rodriguez, ACS Biomater. Sci. Eng. 2017, 3, 929.
B. Y. Lee, J. Zhang, C. Zueger, W.-J. Chung, S. Y. Yoo, E. Wang, J. Meyer, R. Ramesh, S.-W. Lee, Nat. Nanotechnol. 2012, 7, 351.
D. Farrar, K. Ren, D. Cheng, S. Kim, W. Moon, W. L. Wilson, J. E. West, S. M. Yu, Adv. Mater. 2011, 23, 3954.
M. P. Nikiforov, G. L. Thompson, V. V. Reukov, S. Jesse, S. Guo, B. J. Rodriguez, K. Seal, A. A. Vertegel, S. V. Kalinin, ACS Nano 2010, 4, 689.
J. Dolai, A. Maity, B. Mukherjee, R. Ray, N. R. Jana, ACS Appl. Mater. Interfaces 2024, 16, 217.
D. A. D. Gito, A. Akbarinejad, A. Dixon, T. Loho, M. Nieuwoudt, Q. Chen, L. J. Domigan, J. Malmström, Biomacromolecules 2025, 26, 514.
P. J. Dobson, Phys. Bull. 1985, 36, 506.
S. Guerin, A. Stapleton, D. Chovan, R. Mouras, M. Gleeson, C. McKeown, M. R. Noor, C. Silien, F. M. F. Rhen, A. L. Kholkin, N. Liu, T. Soulimane, S. A. M. Tofail, D. Thompson, Nat. Mater. 2018, 17, 180.
J. Y. Fu, P. Y. Liu, J. Cheng, A. S. Bhalla, R. Guo, Appl. Phys. Lett. 2007, 90, 212907.
C. M. Lueng, H. L. W. Chan, C. Surya, C. L. Choy, J. Appl. Phys. 2000, 88, 5360.
D. A. Scrymgeour, J. W. P. Hsu, Nano Lett. 2008, 8, 2204.
A. Heredia, V. Meunier, I. K. Bdikin, J. Gracio, N. Balke, S. Jesse, A. Tselev, P. K. Agarwal, B. G. Sumpter, S. V. Kalinin, A. L. Kholkin, Adv. Funct. Mater. 2012, 22, 2996.
Z. Zhou, D. Qian, M. Minary-Jolandan, ACS Biomater. Sci. Eng. 2016, 2, 929.
A. A. Gundjian, H. L. Chen, IEEE Trans. Biomed. Eng. 1974, BME-21, 177.
S. Zhang, R. Xia, T. R. Shrout, in 2006 IEEE International Symposium on the Applications of Ferroelectrics, IEEE, Sunset Beach, NC, USA, 2006, pp. 1–7.
V. Nguyen, R. Zhu, K. Jenkins, R. Yang, Nat. Commun. 2016, 7, 13566.
Y. Wang, S. Liu, L. Li, H. Li, Y. Yin, S. Rencus-Lazar, S. Guerin, W. Ouyang, D. Thompson, R. Yang, K. Cai, E. Gazit, W. Ji, J. Am. Chem. Soc. 2023, 145, 15331.
W. Ji, B. Xue, Y. Yin, S. Guerin, Y. Wang, L. Zhang, Y. Cheng, L. J. W. Shimon, Y. Chen, D. Thompson, R. Yang, Y. Cao, W. Wang, K. Cai, E. Gazit, J. Am. Chem. Soc. 2022, 144, 18375.
W. Wu, L. Wang, Y. Li, F. Zhang, L. Lin, S. Niu, D. Chenet, X. Zhang, Y. Hao, T. F. Heinz, J. Hone, Z. L. Wang, Nature 2014, 514, 470.
S. K. Ghosh, D. Mandal, Appl. Phys. Lett. 2016, 109, 103701.
W. Kohn, A. D. Becke, R. G. Parr, J. Phys. Chem. 1996, 100, 12974.
J. Hafner, J. Comput. Chem. 2008, 29, 2044.
M. Ernzerhof, G. E. Scuseria, J. Chem. Phys. 1999, 110, 5029.
G. Kresse, D. Joubert, Phys. Rev. B 1999, 59, 1758.
E. Kiely, R. Zwane, R. Fox, A. M. Reilly, S. Guerin, CrystEngComm 2021, 23, 5697.
X. Wu, D. Vanderbilt, D. R. Hamann, Phys. Rev. B 2005, 72, 035105.
