ACS Publications. Most Trusted. Most Cited. Most Read

OR SEARCH CITATIONS

My Activity
Publications
CONTENT TYPES

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Am. Chem. Soc. 2007, 129, 47, 14746-14751
RETURN TO ISSUEPREVArticleNEXT

Biophysical and Structural Characterization of a Robust Octameric β-Peptide Bundle

View Author Information
Contribution from the Departments of Molecular Biochemistry and Biophysics, Chemistry and Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520-8107
Cite this: J. Am. Chem. Soc. 2007, 129, 47, 14746–14751
Publication Date (Web):November 7, 2007
https://doi.org/10.1021/ja0754002
Copyright © 2007 American Chemical Society
Request reuse permissions

    Article Views

    792

    Altmetric

    -

    Citations

    59
    LEARN ABOUT THESE METRICS
    Read OnlinePDF (343 KB)
    Get e-Alerts
    Supporting Info (1)»
    SUBJECTS:

    Abstract

    Abstract Image

    Proteins composed of α-amino acids are essential components of the machinery required for life. Stanley Miller's renowned electric discharge experiment provided evidence that an environment of methane, ammonia, water, and hydrogen was sufficient to produce α-amino acids. This reaction also generated other potential protein building blocks such as the β-amino acid β-glycine (also known as β-alanine); however, the potential of these species to form complex ordered structures that support functional roles has not been widely investigated. In this report we apply a variety of biophysical techniques, including circular dichroism, differential scanning calorimetry, analytical ultracentrifugation, NMR and X-ray crystallography, to characterize the oligomerization of two 12-mer β3-peptides, Acid-1Y and Acid-1Y*. Like the previously reported β3-peptide Zwit-1F, Acid-1Y and Acid-1Y* fold spontaneously into discrete, octameric quaternary structures that we refer to as β-peptide bundles. Surprisingly, the Acid-1Y octamer is more stable than the analogous Zwit-1F octamer, in terms of both its thermodynamics and kinetics of unfolding. The structure of Acid-1Y, reported here to 2.3 Å resolution, provides intriguing hypotheses for the increase in stability. To summarize, in this work we provide additional evidence that nonnatural β-peptide oligomers can assemble into cooperatively folded structures with potential application in enzyme design, and as medical tools and nanomaterials. Furthermore, these studies suggest that nature's selection of α-amino acid precursors was not based solely on their ability to assemble into stable oligomeric structures.

    †

     Department of Molecular Biochemistry and Biophysics.

    ‡

     Department of Chemistry.

    §

     Current Address:  University of Pennsylvania, School of Medicine.

    *

    In papers with more than one author, the asterisk indicates the name of the author to whom inquiries about the paper should be addressed.

    #

     Department of Molecular, Cellular and Developmental Biology.

    Supporting Information Available

    ARTICLE SECTIONS
    Jump To

    Experimental details. This material is available free of charge via the Internet at http://pubs.acs.org. CCDC 662300 contains the supplementary crystallographic data for this paper. These data can be obtained free of charge from The Cambridge Crystallographic Data Centre via www.ccdc.cam.ac.uk/data_request/cif.

    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 59 publications.

    1. Gavin W. Collie, Remy Bailly, Karolina Pulka-Ziach, Caterina M. Lombardo, Laura Mauran, Nada Taib-Maamar, Jean Dessolin, Cameron D. Mackereth, and Gilles Guichard . Molecular Recognition within the Cavity of a Foldamer Helix Bundle: Encapsulation of Primary Alcohols in Aqueous Conditions. Journal of the American Chemical Society 2017, 139 (17) , 6128-6137. https://doi.org/10.1021/jacs.7b00181
    2. Caterina M. Lombardo, Gavin W. Collie, Karolina Pulka-Ziach, Frederic Rosu, Valerie Gabelica, Cameron D. Mackereth, and Gilles Guichard . Anatomy of an Oligourea Six-Helix Bundle. Journal of the American Chemical Society 2016, 138 (33) , 10522-10530. https://doi.org/10.1021/jacs.6b05063
    3. Xuesong Li, Ting Qi, Kolupula Srinivas, Stéphane Massip, Victor Maurizot, and Ivan Huc . Synthesis and Multibromination of Nanosized Helical Aromatic Amide Foldamers via Segment-Doubling Condensation. Organic Letters 2016, 18 (5) , 1044-1047. https://doi.org/10.1021/acs.orglett.6b00165
    4. Jonathan P. Miller, Michael S. Melicher, and Alanna Schepartz . Positive Allostery in Metal Ion Binding by a Cooperatively Folded β-Peptide Bundle. Journal of the American Chemical Society 2014, 136 (42) , 14726-14729. https://doi.org/10.1021/ja508872q
    5. Pam S. P. Wang, Jennifer B. Nguyen, and Alanna Schepartz . Design and High-Resolution Structure of a β3-Peptide Bundle Catalyst. Journal of the American Chemical Society 2014, 136 (19) , 6810-6813. https://doi.org/10.1021/ja5013849
    6. Geronda L. Montalvo, Feng Gai, Heinrich Roder, and William F. DeGrado . Slow Folding–Unfolding Kinetics of an Octameric β-Peptide Bundle. ACS Chemical Biology 2014, 9 (1) , 276-281. https://doi.org/10.1021/cb400621y
    7. Michael S. Melicher, John Chu, Allison S. Walker, Scott J. Miller, Richard H. G. Baxter, and Alanna Schepartz . A β-Boronopeptide Bundle of Known Structure As a Vehicle for Polyol Recognition. Organic Letters 2013, 15 (19) , 5048-5051. https://doi.org/10.1021/ol402381n
    8. William C. Pomerantz, Virany M. Yuwono, Ryan Drake, Jeffrey D. Hartgerink, Nicholas L. Abbott, and Samuel H. Gellman . Lyotropic Liquid Crystals Formed from ACHC-Rich β-Peptides. Journal of the American Chemical Society 2011, 133 (34) , 13604-13613. https://doi.org/10.1021/ja204874h
    9. Nicolas Delsuc, Stéphane Massip, Jean-Michel Léger, Brice Kauffmann, and Ivan Huc . Relative Helix−Helix Conformations in Branched Aromatic Oligoamide Foldamers. Journal of the American Chemical Society 2011, 133 (9) , 3165-3172. https://doi.org/10.1021/ja110677a
    10. Prema. G. Vasudev, Sunanda Chatterjee, Narayanaswamy Shamala, and Padmanabhan Balaram . Structural Chemistry of Peptides Containing Backbone Expanded Amino Acid Residues: Conformational Features of β, γ, and Hybrid Peptides. Chemical Reviews 2011, 111 (2) , 657-687. https://doi.org/10.1021/cr100100x
    11. Ivan V. Korendovych, Yong Ho Kim, Andrew H. Ryan, James D. Lear, William F. DeGrado, and Scott J. Shandler . Computational Design of a Self-Assembling β-Peptide Oligomer. Organic Letters 2010, 12 (22) , 5142-5145. https://doi.org/10.1021/ol102092r
    12. Emilie Pouget, Nicolas Fay, Erik Dujardin, Nadège Jamin, Patrick Berthault, Lionel Perrin, Anjali Pandit, Thierry Rose, Céline Valéry, Daniel Thomas, Maïté Paternostre and Franck Artzner . Elucidation of the Self-Assembly Pathway of Lanreotide Octapeptide into β-Sheet Nanotubes: Role of Two Stable Intermediates. Journal of the American Chemical Society 2010, 132 (12) , 4230-4241. https://doi.org/10.1021/ja9088023
    13. Matthew A. Molski, Jessica L. Goodman, Cody J. Craig, He Meng, Krishna Kumar and Alanna Schepartz . β-Peptide Bundles with Fluorous Cores. Journal of the American Chemical Society 2010, 132 (11) , 3658-3659. https://doi.org/10.1021/ja910903c
    14. Arjel D. Bautista, Jacob S. Appelbaum, Cody J. Craig, Julien Michel and Alanna Schepartz . Bridged β3-Peptide Inhibitors of p53-hDM2 Complexation: Correlation between Affinity and Cell Permeability. Journal of the American Chemical Society 2010, 132 (9) , 2904-2906. https://doi.org/10.1021/ja910715u
    15. Fredy Sussman, M. Carmen Villaverde, Juan Carlos Estévez and Ramón J. Estévez. Searching the Conformational Space of Cyclic β-Amino Acid Peptides. The Journal of Physical Chemistry B 2009, 113 (29) , 9669-9680. https://doi.org/10.1021/jp811321n
    16. Jonel P. Saludes, James B. Ames and Jacquelyn Gervay-Hague. Synthesis and Structural Characterization of Sialic Acid−Glutamic Acid Hybrid Foldamers as Conformational Surrogates of α-2,8-Linked Polysialic Acid. Journal of the American Chemical Society 2009, 131 (15) , 5495-5505. https://doi.org/10.1021/ja808286x
    17. Ralf David, Robert Günther, Lars Baumann, Tessa Lühmann, Dieter Seebach, Hans-Jörg Hofmann and Annette G. Beck-Sickinger . Artificial Chemokines: Combining Chemistry and Molecular Biology for the Elucidation of Interleukin-8 Functionality. Journal of the American Chemical Society 2008, 130 (46) , 15311-15317. https://doi.org/10.1021/ja802453x
    18. Byoung-Chul Lee, Tammy K. Chu, Ken A. Dill and Ronald N. Zuckermann . Biomimetic Nanostructures: Creating a High-Affinity Zinc-Binding Site in a Folded Nonbiological Polymer. Journal of the American Chemical Society 2008, 130 (27) , 8847-8855. https://doi.org/10.1021/ja802125x
    19. Anna S. Norgren and Per I. Arvidsson . Design and Synthesis of Glycosylated β3-Peptides Capable of Folding into the 314-Helical Conformation in Water. The Journal of Organic Chemistry 2008, 73 (14) , 5272-5278. https://doi.org/10.1021/jo8003265
    20. William C. Pomerantz, Tami L. R. Grygiel, Jonathan R. Lai and Samuel H. Gellman. Distinctive Circular Dichroism Signature for 14-Helix-Bundle Formation by β-Peptides. Organic Letters 2008, 10 (9) , 1799-1802. https://doi.org/10.1021/ol800622e
    21. Jihye Park, Hee-Seung Lee, Hyungjun Kim, Jeong-Mo Choi. Conformational landscapes of artificial peptides predicted by various force fields: are we ready to simulate β-amino acids?. Physical Chemistry Chemical Physics 2023, 25 (10) , 7466-7476. https://doi.org/10.1039/D2CP05998C
    22. Gavin W. Collie, Caterina M. Lombardo, Sung Hyun Yoo, Karolina Pułka-Ziach, Valérie Gabelica, Cameron D. Mackereth, Frédéric Rosu, Gilles Guichard. Crystal structures capture multiple stoichiometric states of an aqueous self-assembling oligourea foldamer. Chemical Communications 2021, 57 (75) , 9514-9517. https://doi.org/10.1039/D1CC03604A
    23. Rajkumar Misra, Safra Rudnick‐Glick, Lihi Adler‐Abramovich. From Folding to Assembly: Functional Supramolecular Architectures of Peptides Comprised of Non‐Canonical Amino Acids. Macromolecular Bioscience 2021, 21 (8) https://doi.org/10.1002/mabi.202100090
    24. Imola Cs. Szigyártó, Judith Mihály, András Wacha, Dóra Bogdán, Tünde Juhász, Gergely Kohut, Gitta Schlosser, Ferenc Zsila, Vlada Urlacher, Zoltán Varga, Ferenc Fülöp, Attila Bóta, István Mándity, Tamás Beke-Somfai. Membrane active Janus-oligomers of β 3 -peptides. Chemical Science 2020, 11 (26) , 6868-6881. https://doi.org/10.1039/D0SC01344G
    25. Samuele Rinaldi. The Diverse World of Foldamers: Endless Possibilities of Self-Assembly. Molecules 2020, 25 (14) , 3276. https://doi.org/10.3390/molecules25143276
    26. Claire Buchanan, Christopher J Garvey, Ljiljana Puskar, Patrick Perlmutter, Adam Mechler. Coordination crosslinking of helical substituted oligoamide nanorods with Cu(II). Supramolecular Chemistry 2020, 32 (3) , 222-232. https://doi.org/10.1080/10610278.2020.1730839
    27. Ketav Kulkarni, Nathan Habila, Mark P. Del Borgo, Marie-Isabel Aguilar. Novel Materials From the Supramolecular Self-Assembly of Short Helical β3-Peptide Foldamers. Frontiers in Chemistry 2019, 7 https://doi.org/10.3389/fchem.2019.00070
    28. Monika Szefczyk, Ewelina Węglarz-Tomczak, Paulina Fortuna, Agnieszka Krzysztoń, Ewa Rudzińska-Szostak, Łukasz Berlicki. Controlling the Helix Handedness of ααβ-Peptide Foldamers through Sequence Shifting. Angewandte Chemie 2017, 129 (8) , 2119-2123. https://doi.org/10.1002/ange.201610154
    29. Monika Szefczyk, Ewelina Węglarz-Tomczak, Paulina Fortuna, Agnieszka Krzysztoń, Ewa Rudzińska-Szostak, Łukasz Berlicki. Controlling the Helix Handedness of ααβ-Peptide Foldamers through Sequence Shifting. Angewandte Chemie International Edition 2017, 56 (8) , 2087-2091. https://doi.org/10.1002/anie.201610154
    30. Tushar Satav, Peter Korevaar, Tom F. A. de Greef, Jurriaan Huskens, Pascal Jonkheijm. Modulating the Nucleated Self‐Assembly of Tri‐β 3 ‐Peptides Using Cucurbit[ n ]urils. Chemistry – A European Journal 2016, 22 (36) , 12675-12679. https://doi.org/10.1002/chem.201602896
    31. Gavin William Collie, Karolina Pulka-Ziach, Gilles Guichard. In situ iodination and X-ray crystal structure of a foldamer helix bundle. Chemical Communications 2016, 52 (6) , 1202-1205. https://doi.org/10.1039/C5CC07916K
    32. Pam S. P. Wang, Alanna Schepartz. β-Peptide bundles: Design. Build. Analyze. Biosynthesize.. Chemical Communications 2016, 52 (47) , 7420-7432. https://doi.org/10.1039/C6CC01546H
    33. Romila D. Gopalan, Mark P. Del Borgo, Adam I. Mechler, Patrick Perlmutter, Marie-Isabel Aguilar. Geometrically Precise Building Blocks: the Self-Assembly of β-Peptides. Chemistry & Biology 2015, 22 (11) , 1417-1423. https://doi.org/10.1016/j.chembiol.2015.10.005
    34. Andrea Bonetti, Francesca Clerici, Francesca Foschi, Donatella Nava, Sara Pellegrino, Michele Penso, Raffaella Soave, Maria Luisa Gelmi. syn / anti Switching by Specific Heteroatom-Titanium Coordination in the Mannich-Like Synthesis of 2,3-Diaryl-β-amino Acid Derivatives. European Journal of Organic Chemistry 2014, 2014 (15) , 3203-3209. https://doi.org/10.1002/ejoc.201400142
    35. Junjian Miao, Shuhua Li. Structural preferences of two unnatural hybrid octapeptides with and without the crystal environment: a computational study. Theoretical Chemistry Accounts 2014, 133 (3) https://doi.org/10.1007/s00214-013-1444-7
    36. Éva Szolnoki, Anasztázia Hetényi, István M. Mándity, Ferenc Fülöp, Tamás A. Martinek. Foldameric β‐H18/20 P Mixed Helix Stabilized by Head‐to‐Tail Contacts: A Way to Higher‐Order Structures. European Journal of Organic Chemistry 2013, 2013 (17) , 3555-3559. https://doi.org/10.1002/ejoc.201201633
    37. Sergey Lyskov, Fang-Chieh Chou, Shane Ó. Conchúir, Bryan S. Der, Kevin Drew, Daisuke Kuroda, Jianqing Xu, Brian D. Weitzner, P. Douglas Renfrew, Parin Sripakdeevong, Benjamin Borgo, James J. Havranek, Brian Kuhlman, Tanja Kortemme, Richard Bonneau, Jeffrey J. Gray, Rhiju Das, . Serverification of Molecular Modeling Applications: The Rosetta Online Server That Includes Everyone (ROSIE). PLoS ONE 2013, 8 (5) , e63906. https://doi.org/10.1371/journal.pone.0063906
    38. Colleen M. Doyle, Jessica A. Rumfeldt, Helen R. Broom, Aron Broom, Peter B. Stathopulos, Kenrick A. Vassall, Johnathan J. Almey, Elizabeth M. Meiering. Energetics of oligomeric protein folding and association. Archives of Biochemistry and Biophysics 2013, 531 (1-2) , 44-64. https://doi.org/10.1016/j.abb.2012.12.005
    39. Claudia Tomasini, Nicola Castellucci. Introduction to Unnatural Foldamers. 2013, 51-89. https://doi.org/10.1002/9781118517413.ch2
    40. Sandip V. Jadhav, Anupam Bandyopadhyay, Hosahudya N. Gopi. Protein secondary structure mimetics: crystal conformations of α/γ 4 -hybrid peptide12-helices with proteinogenic side chains and their analogy with α- and β-peptide helices. Org. Biomol. Chem. 2013, 11 (3) , 509-514. https://doi.org/10.1039/C2OB26805A
    41. Matthew A. Molski, Jessica L. Goodman, Fang-Chieh Chou, David Baker, Rhiju Das, Alanna Schepartz. Remodeling a β-peptide bundle. Chem. Sci. 2013, 4 (1) , 319-324. https://doi.org/10.1039/C2SC21117C
    42. Shohei Tashiro, Koji Matsuoka, Ai Minoda, Mitsuhiko Shionoya. Metallo-Foldamers with Backbone-Coordinative Oxime Peptides: Control of Secondary Structures. Angewandte Chemie 2012, 124 (52) , 13300-13304. https://doi.org/10.1002/ange.201206968
    43. Shohei Tashiro, Koji Matsuoka, Ai Minoda, Mitsuhiko Shionoya. Metallo-Foldamers with Backbone-Coordinative Oxime Peptides: Control of Secondary Structures. Angewandte Chemie International Edition 2012, 51 (52) , 13123-13127. https://doi.org/10.1002/anie.201206968
    44. Ying-Ling Chiang, Justin A. Russak, Nancy Carrillo, Jeffrey W. Bode. Synthesis of Enantiomerically Pure Isoxazolidine Monomers for the Preparation of β 3 -Oligopeptides by Iterative α -Keto AcidHydroxylamine (KAHA) Ligations. Helvetica Chimica Acta 2012, 95 (12) , 2481-2501. https://doi.org/10.1002/hlca.201200484
    45. Pam Shou-Ping Wang, Cody J. Craig, Alanna Schepartz. Relationship between side-chain branching and stoichiometry in β3-peptide bundles. Tetrahedron 2012, 68 (23) , 4342-4345. https://doi.org/10.1016/j.tet.2012.03.079
    46. Sunbum Kwon, Kyungtae Kang, Aram Jeon, Ji Hun Park, Insung S. Choi, Hee-Seung Lee. Evaporation-induced self-assembly of trans-2-aminocyclopentanecarboxylic acid hexamers. Tetrahedron 2012, 68 (23) , 4368-4373. https://doi.org/10.1016/j.tet.2012.02.061
    47. Tamás A. Martinek, Ferenc Fülöp. Peptidic foldamers: ramping up diversity. Chem. Soc. Rev. 2012, 41 (2) , 687-702. https://doi.org/10.1039/C1CS15097A
    48. Éva Szolnoki, Anasztázia Hetényi, Tamás A. Martinek, Zsolt Szakonyi, Ferenc Fülöp. Self-association-driven transition of the β-peptidic H12 helix to the H18 helix. Org. Biomol. Chem. 2012, 10 (2) , 255-259. https://doi.org/10.1039/C1OB06627G
    49. Mark S. Taylor. A stereochemical sojourn. Nature Chemistry 2011, 3 (9) , 660-662. https://doi.org/10.1038/nchem.1133
    50. Ludwig K. A. Pilsl, Oliver Reiser. α/β-Peptide foldamers: state of the art. Amino Acids 2011, 41 (3) , 709-718. https://doi.org/10.1007/s00726-011-0894-2
    51. Cody J. Craig, Jessica L. Goodman, Alanna Schepartz. Enhancing β3-Peptide Bundle Stability by Design. ChemBioChem 2011, 12 (7) , 1035-1038. https://doi.org/10.1002/cbic.201000753
    52. Sunbum Kwon, Aram Jeon, Sung Hyun Yoo, Im Sik Chung, Hee-Seung Lee. Unprecedented Molecular Architectures by the Controlled Self-Assembly of a β-Peptide Foldamer. Angewandte Chemie 2010, 122 (44) , 8408-8412. https://doi.org/10.1002/ange.201003302
    53. Sunbum Kwon, Aram Jeon, Sung Hyun Yoo, Im Sik Chung, Hee-Seung Lee. Unprecedented Molecular Architectures by the Controlled Self-Assembly of a β-Peptide Foldamer. Angewandte Chemie International Edition 2010, 49 (44) , 8232-8236. https://doi.org/10.1002/anie.201003302
    54. Nathan T. Ross, William P. Katt, Andrew D. Hamilton. Synthetic mimetics of protein secondary structure domains. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 2010, 368 (1914) , 989-1008. https://doi.org/10.1098/rsta.2009.0210
    55. Knud J. Jensen. De Novo Design of Proteins. 2009, 207-248. https://doi.org/10.1002/9780470749708.ch6
    56. Sara J. Buhrlage, Bin Chen, Anna K. Mapp. A flexible synthetic route to isoxazolidine β-proline analogs. Tetrahedron 2009, 65 (16) , 3305-3313. https://doi.org/10.1016/j.tet.2008.12.062
    57. Jessica L. Goodman, Matthew A. Molski, Jade Qiu, Alanna Schepartz. Tetrameric β 3 ‐Peptide Bundles. ChemBioChem 2008, 9 (10) , 1576-1578. https://doi.org/10.1002/cbic.200800039
    58. Robert J. Mart, Simon J. Webb. Bioinspired organic chemistry. Annual Reports Section "B" (Organic Chemistry) 2008, 104 , 370. https://doi.org/10.1039/b716609p
    59. Arjel D Bautista, Cody J Craig, Elizabeth A Harker, Alanna Schepartz. Sophistication of foldamer form and function in vitro and in vivo. Current Opinion in Chemical Biology 2007, 11 (6) , 685-692. https://doi.org/10.1016/j.cbpa.2007.09.009
    Download PDF

    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