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Molecular structure of monomorphic peptide fibrils within a kinetically trapped hydrogel network.

Nagy-Smith K, Moore E, Schneider J, Tycko R
Proc Natl Acad Sci U S A 112 9816-21 (2015)
Cited: 64 times
EuropePMC logo PMID: 26216960

Abstract

Most, if not all, peptide- and protein-based hydrogels formed by self-assembly can be characterized as kinetically trapped 3D networks of fibrils. The propensity of disease-associated amyloid-forming peptides and proteins to assemble into polymorphic fibrils suggests that cross-β fibrils comprising hydrogels may also be polymorphic. We use solid-state NMR to determine the molecular and supramolecular structure of MAX1, a de novo designed gel-forming peptide, in its fibrillar state. We find that MAX1 adopts a β-hairpin conformation and self-assembles with high fidelity into a double-layered cross-β structure. Hairpins assemble with an in-register Syn orientation within each β-sheet layer and with an Anti orientation between layers. Surprisingly, although the MAX1 fibril network is kinetically trapped, solid-state NMR data show that fibrils within this network are monomorphic and most likely represent the thermodynamic ground state. Intermolecular interactions not available in alternative structural arrangements apparently dictate this monomorphic behavior.

Reviews - 2n1e mentioned but not cited (3)

  1. De novo protein design, a retrospective. Korendovych IV, DeGrado WF. Q Rev Biophys 53 e3 (2020)
  2. Protein Design: From the Aspect of Water Solubility and Stability. Qing R, Hao S, Smorodina E, Jin D, Zalevsky A, Zhang S. Chem Rev 122 14085-14179 (2022)
  3. Catalytic Amyloids as Novel Synthetic Hydrolases. Duran-Meza E, Diaz-Espinoza R. Int J Mol Sci 22 9166 (2021)

Articles - 2n1e mentioned but not cited (3)

  1. Molecular structure of monomorphic peptide fibrils within a kinetically trapped hydrogel network. Nagy-Smith K, Moore E, Schneider J, Tycko R. Proc Natl Acad Sci U S A 112 9816-9821 (2015)
  2. Molecular, Local, and Network-Level Basis for the Enhanced Stiffness of Hydrogel Networks Formed from Coassembled Racemic Peptides: Predictions from Pauling and Corey. Nagy-Smith K, Beltramo PJ, Moore E, Tycko R, Furst EM, Schneider JP. ACS Cent Sci 3 586-597 (2017)
  3. Direct observation of peptide hydrogel self-assembly. Adams ZC, Olson EJ, Lopez-Silva TL, Lian Z, Kim AY, Holcomb M, Zimmermann J, Adhikary R, Dawson PE. Chem Sci 13 10020-10028 (2022)


Reviews citing this publication (16)

  1. Application of NMR to studies of intrinsically disordered proteins. Gibbs EB, Cook EC, Showalter SA. Arch Biochem Biophys 628 57-70 (2017)
  2. Structure-mechanical property correlations of hydrogel forming β-sheet peptides. De Leon Rodriguez LM, Hemar Y, Cornish J, Brimble MA. Chem Soc Rev 45 4797-4824 (2016)
  3. Designer Self-Assembling Peptide Hydrogels to Engineer 3D Cell Microenvironments for Cell Constructs Formation and Precise Oncology Remodeling in Ovarian Cancer. Yang Z, Xu H, Zhao X. Adv Sci (Weinh) 7 1903718 (2020)
  4. Polymeric Biomaterials for In Vitro Cancer Tissue Engineering and Drug Testing Applications. Pradhan S, Hassani I, Clary JM, Lipke EA. Tissue Eng Part B Rev 22 470-484 (2016)
  5. Biomolecular Assemblies: Moving from Observation to Predictive Design. Wilson CJ, Bommarius AS, Champion JA, Chernoff YO, Lynn DG, Paravastu AK, Liang C, Hsieh MC, Heemstra JM. Chem Rev 118 11519-11574 (2018)
  6. Insights into protein misfolding and aggregation enabled by solid-state NMR spectroscopy. van der Wel PCA. Solid State Nucl Magn Reson 88 1-14 (2017)
  7. Peptide Tectonics: Encoded Structural Complementarity Dictates Programmable Self-Assembly. Lou S, Wang X, Yu Z, Shi L. Adv Sci (Weinh) 6 1802043 (2019)
  8. Amyloid-Like Aggregation in Diseases and Biomaterials: Osmosis of Structural Information. Balasco N, Diaferia C, Morelli G, Vitagliano L, Accardo A. Front Bioeng Biotechnol 9 641372 (2021)
  9. Supramolecular Peptide Assemblies as Antimicrobial Scaffolds. Simonson AW, Aronson MR, Medina SH. Molecules 25 E2751 (2020)
  10. Defining the Landscape of the Pauling-Corey Rippled Sheet: An Orphaned Motif Finding New Homes. Raskatov JA, Schneider JP, Nilsson BL. Acc Chem Res 54 2488-2501 (2021)
  11. Supramolecular assembly of protein building blocks: from folding to function. Kim NH, Choi H, Shahzad ZM, Ki H, Lee J, Chae H, Kim YH. Nano Converg 9 4 (2022)
  12. Supramolecular assembly of functional peptide-polymer conjugates. Otter R, Besenius P. Org Biomol Chem 17 6719-6734 (2019)
  13. From structure to application: Progress and opportunities in peptide materials development. Lopez-Silva TL, Schneider JP. Curr Opin Chem Biol 64 131-144 (2021)
  14. Peptide hydrogels for affinity-controlled release of therapeutic cargo: Current and potential strategies. Nambiar M, Schneider JP. J Pept Sci 28 e3377 (2022)
  15. Fmoc-Diphenylalanine Hydrogels: Optimization of Preparation Methods and Structural Insights. Diaferia C, Rosa E, Morelli G, Accardo A. Pharmaceuticals (Basel) 15 1048 (2022)
  16. Solid-State NMR Structural Characterization of Self-Assembled Peptides with Selective 13C and 15N Isotopic Labels. Huang D, Hudson BC, Gao Y, Roberts EK, Paravastu AK. Methods Mol Biol 1777 23-68 (2018)

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  1. Zinc-binding structure of a catalytic amyloid from solid-state NMR. Lee M, Wang T, Makhlynets OV, Wu Y, Polizzi NF, Wu H, Gosavi PM, Stöhr J, Korendovych IV, DeGrado WF, Hong M. Proc Natl Acad Sci U S A 114 6191-6196 (2017)
  2. Molecular structure of a prevalent amyloid-β fibril polymorph from Alzheimer's disease brain tissue. Ghosh U, Thurber KR, Yau WM, Tycko R. Proc Natl Acad Sci U S A 118 e2023089118 (2021)
  3. Switchable Hydrolase Based on Reversible Formation of Supramolecular Catalytic Site Using a Self-Assembling Peptide. Zhang C, Shafi R, Lampel A, MacPherson D, Pappas CG, Narang V, Wang T, Maldarelli C, Ulijn RV. Angew Chem Int Ed Engl 56 14511-14515 (2017)
  4. Enzymatic Control of the Conformational Landscape of Self-Assembling Peptides. Shi J, Fichman G, Schneider JP. Angew Chem Int Ed Engl 57 11188-11192 (2018)
  5. Enzymatic Self-Assembly Confers Exceptionally Strong Synergism with NF-κB Targeting for Selective Necroptosis of Cancer Cells. Zhou J, Du X, Chen X, Wang J, Zhou N, Wu D, Xu B. J Am Chem Soc 140 2301-2308 (2018)
  6. Atomic-level insight into mRNA processing bodies by combining solid and solution-state NMR spectroscopy. Damman R, Schütz S, Luo Y, Weingarth M, Sprangers R, Baldus M. Nat Commun 10 4536 (2019)
  7. Chiral recognition in amyloid fiber growth. Torbeev V, Grogg M, Ruiz J, Boehringer R, Schirer A, Hellwig P, Jeschke G, Hilvert D. J Pept Sci 22 290-304 (2016)
  8. Protofilament Structure and Supramolecular Polymorphism of Aggregated Mutant Huntingtin Exon 1. Boatz JC, Piretra T, Lasorsa A, Matlahov I, Conway JF, van der Wel PCA. J Mol Biol 432 4722-4744 (2020)
  9. Structural analysis of cross α-helical nanotubes provides insight into the designability of filamentous peptide nanomaterials. Wang F, Gnewou O, Modlin C, Beltran LC, Xu C, Su Z, Juneja P, Grigoryan G, Egelman EH, Conticello VP. Nat Commun 12 407 (2021)
  10. Beta-hairpin hydrogels as scaffolds for high-throughput drug discovery in three-dimensional cell culture. Worthington P, Drake KM, Li Z, Napper AD, Pochan DJ, Langhans SA. Anal Biochem 535 25-34 (2017)
  11. Design of a Peptide-Based Electronegative Hydrogel for the Direct Encapsulation, 3D Culturing, in Vivo Syringe-Based Delivery, and Long-Term Tissue Engraftment of Cells. Yamada Y, Patel NL, Kalen JD, Schneider JP. ACS Appl Mater Interfaces 11 34688-34697 (2019)
  12. Electrostatically Driven Guanidinium Interaction Domains that Control Hydrogel-Mediated Protein Delivery In Vivo. Miller SE, Yamada Y, Patel N, Suárez E, Andrews C, Tau S, Luke BT, Cachau RE, Schneider JP. ACS Cent Sci 5 1750-1759 (2019)
  13. Ambidextrous helical nanotubes from self-assembly of designed helical hairpin motifs. Hughes SA, Wang F, Wang S, Kreutzberger MAB, Osinski T, Orlova A, Wall JS, Zuo X, Egelman EH, Conticello VP. Proc Natl Acad Sci U S A 116 14456-14464 (2019)
  14. Design Parameters of Tissue-Engineering Scaffolds at the Atomic Scale. Jekhmane S, Prachar M, Pugliese R, Fontana F, Fontana F, Medeiros-Silva J, Gelain F, Weingarth M. Angew Chem Int Ed Engl 58 16943-16951 (2019)
  15. Protein release from highly charged peptide hydrogel networks. Nagy-Smith K, Yamada Y, Schneider JP. J Mater Chem B 4 1999-2007 (2016)
  16. Serum Protein Adsorption Modulates the Toxicity of Highly Positively Charged Hydrogel Surfaces. Yamada Y, Fichman G, Schneider JP. ACS Appl Mater Interfaces 13 8006-8014 (2021)
  17. Supramolecular Nanofibers of Drug-Peptide Amphiphile and Affibody Suppress HER2+ Tumor Growth. Liang C, Zhang L, Zhao W, Xu L, Chen Y, Long J, Wang F, Wang L, Yang Z. Adv Healthc Mater 7 e1800899 (2018)
  18. Macromolecule-Network Electrostatics Controlling Delivery of the Biotherapeutic Cell Modulator TIMP-2. Yamada Y, Chowdhury A, Schneider JP, Stetler-Stevenson WG. Biomacromolecules 19 1285-1293 (2018)
  19. Multiphase Assembly of Small Molecule Microcrystalline Peptide Hydrogel Allows Immunomodulatory Combination Therapy for Long-Term Heart Transplant Survival. Majumder P, Zhang Y, Iglesias M, Fan L, Kelley JA, Andrews C, Patel N, Stagno JR, Oh BC, Furtmüller GJ, Lai CC, Wang YX, Brandacher G, Raimondi G, Schneider JP. Small 16 e2002791 (2020)
  20. Deterministic chaos in the self-assembly of β sheet nanotubes from an amphipathic oligopeptide. Wang F, Gnewou O, Wang S, Osinski T, Zuo X, Egelman EH, Conticello VP. Matter 4 3217-3231 (2021)
  21. Implementation of a High-Throughput Pilot Screen in Peptide Hydrogel-Based Three-Dimensional Cell Cultures. Worthington P, Drake KM, Li Z, Napper AD, Pochan DJ, Langhans SA. SLAS Discov 24 714-723 (2019)
  22. Amyloid Peptide Mixtures: Self-Assembly, Hydrogelation, Nematic Ordering, and Catalysts in Aldol Reactions. Pelin JNBD, Gerbelli BB, Edwards-Gayle CJC, Aguilar AM, Castelletto V, Hamley IW, Alves WA. Langmuir 36 2767-2774 (2020)
  23. Dopamine Self-Polymerization as a Simple and Powerful Tool to Modulate the Viscoelastic Mechanical Properties of Peptide-Based Gels. Fichman G, Schneider JP. Molecules 26 1363 (2021)
  24. Post-Translational Backbone Engineering through Selenomethionine-Mediated Incorporation of Freidinger Lactams. Flood DT, Yan NL, Dawson PE. Angew Chem Int Ed Engl 57 8697-8701 (2018)
  25. Surface-fill hydrogel attenuates the oncogenic signature of complex anatomical surface cancer in a single application. Majumder P, Singh A, Wang Z, Dutta K, Pahwa R, Liang C, Andrews C, Patel NL, Shi J, de Val N, Walsh STR, Jeon AB, Karim B, Hoang CD, Schneider JP. Nat Nanotechnol 16 1251-1259 (2021)
  26. A Two-Tailed Phosphopeptide Crystallizes to Form a Lamellar Structure. Pellach M, Mondal S, Harlos K, Mance D, Baldus M, Gazit E, Shimon LJ. Angew Chem Int Ed Engl 56 3252-3255 (2017)
  27. Antibacterial Gel Coatings Inspired by the Cryptic Function of a Mussel Byssal Peptide. Fichman G, Andrews C, Patel NL, Schneider JP. Adv Mater 33 e2103677 (2021)
  28. Multifunctional thermoresponsive designer peptide hydrogels. De Leon-Rodriguez LM, Hemar Y, Mo G, Mitra AK, Cornish J, Brimble MA. Acta Biomater 47 40-49 (2017)
  29. Peptide hydrogel with self-healing and redox-responsive properties. D'Souza A, Marshall LR, Yoon J, Kulesha A, Edirisinghe DIU, Chandrasekaran S, Rathee P, Prabhakar R, Makhlynets OV. Nano Converg 9 18 (2022)
  30. Enzymatic activatable self-assembled peptide nanowire for targeted therapy and fluorescence imaging of tumors. Tang Y, Wu Z, Zhang CH, Zhang XL, Jiang JH. Chem Commun (Camb) 52 3631-3634 (2016)
  31. Utilizing Frémy's Salt to Increase the Mechanical Rigidity of Supramolecular Peptide-Based Gel Networks. Fichman G, Schneider JP. Front Bioeng Biotechnol 8 594258 (2020)
  32. Intracellular artificial supramolecules based on de novo designed Y15 peptides. Miki T, Nakai T, Hashimoto M, Kajiwara K, Tsutsumi H, Mihara H. Nat Commun 12 3412 (2021)
  33. Understanding the metal mediated assembly and hydrogel formation of a β-hairpin peptide. De Leon-Rodriguez LM, Hemar Y, Mitra AK, Brimble MA. Biomater Sci 5 1993-1997 (2017)
  34. Dynamic protein folding at the surface of stimuli-responsive peptide fibrils. Nagarkar RP, Miller SE, Zhong S, Pochan DJ, Schneider JP. Protein Sci 27 1243-1251 (2018)
  35. Accelerating the prediction and discovery of peptide hydrogels with human-in-the-loop. Xu T, Wang J, Zhao S, Chen D, Zhang H, Fang Y, Kong N, Zhou Z, Li W, Wang H. Nat Commun 14 3880 (2023)
  36. Comparative analysis of 13C chemical shifts of β-sheet amyloid proteins and outer membrane proteins. Somberg NH, Gelenter MD, Hong M. J Biomol NMR 75 151-166 (2021)
  37. Decoupling the effects of hydrophilic and hydrophobic moieties at the neuron-nanofibre interface. Martin AD, Wojciechowski JP, Du EY, Rawal A, Stefen H, Au CG, Hou L, Cranfield CG, Fath T, Ittner LM, Thordarson P. Chem Sci 11 1375-1382 (2019)
  38. EMBER multidimensional spectral microscopy enables quantitative determination of disease- and cell-specific amyloid strains. Yang H, Yuan P, Wu Y, Shi M, Caro CD, Tengeiji A, Yamanoi S, Inoue M, DeGrado WF, Condello C. Proc Natl Acad Sci U S A 120 e2300769120 (2023)
  39. Experimental Insights into Conformational Ensembles of Assembled β-Sheet Peptides. Yu L, Wang R, Li S, Kara UI, Boerner EC, Chen B, Zhang F, Jian Z, Li S, Liu M, Wang Y, Liu S, Yang Y, Wang C, Zhang W, Yao Y, Wang X, Wang C. ACS Cent Sci 9 1480-1487 (2023)
  40. Sequence patterns and signatures: Computational and experimental discovery of amyloid-forming peptides. Xiao X, Robang AS, Sarma S, Le JV, Helmicki ME, Lambert MJ, Guerrero-Ferreira R, Arboleda-Echavarria J, Paravastu AK, Hall CK. PNAS Nexus 1 pgac263 (2022)
  41. Structural Arrangement within a Peptide Fibril Derived from the Glaucoma-Associated Myocilin Olfactomedin Domain. Gao Y, Saccuzzo EG, Hill SE, Huard DJE, Robang AS, Lieberman RL, Paravastu AK. J Phys Chem B 125 2886-2897 (2021)
  42. The Effects of Charged Amino Acid Side-Chain Length on Diagonal Cross-Strand Interactions between Carboxylate- and Ammonium-Containing Residues in a β-Hairpin. Chang JY, Pan YJ, Huang PY, Sun YT, Yu CH, Ning ZJ, Huang SL, Huang SJ, Cheng RP. Molecules 27 4172 (2022)


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