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Cooperative systems constructed using crystalline metal complexes of short flexible peptides

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Abstract

Biological systems display a range of sophisticated functions that cannot be performed by artificial systems, through intricate cooperative structural changes involving multiple functional units. The designability and structural flexibility of peptides are demonstrated by biological systems that display cooperative structural changes; these properties also make them well-suited for the formation of artificial systems that display such changes. The problem with the use of peptide frameworks is that long peptide residues, which are not suitable for gram-scale use, are required for the formation of stable ordered structures. However, if ordered structures containing peptides could be constructed by coordinating them to metal ions, peptides could be widely used to develop sophisticated functional materials. Crystal packing can be used for the design of functional materials made from simple molecules because it provides a way to place the components relative to each other. Although crystalline systems have been reported in which the small size of the cavities has been attributed to the flexibility of the peptide, recently, large systems with giant cavities have been developed with flexible peptides. In this review, we summarize the formation of cooperative multicomponent systems in the crystalline state using metal complexes of simple peptides, along with recent advances in the construction of giant artificial systems using short peptides.

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References

  1. de la Rica, R., Matsui, H.: Applications of peptide and protein-based materials in bionanotechnology. Chem. Soc. Rev. 39, 3499–3509 (2010)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Okesola, B.O., Mata, A.: Multicomponent self-assembly as a tool to harness new properties from peptides and proteins in material design. Chem. Soc. Rev. 47, 3721–3736 (2018)

    Article  PubMed  CAS  Google Scholar 

  3. Li, D., Kaneko, K.: Hydrogen bond-regulated microporous nature of copper complex-assembled microcrystals. Chem. Phys. Lett. 335, 50–56 (2001)

    Article  CAS  Google Scholar 

  4. Barthelet, K., Marrot, J., Riou, D., Férey, G.: A breathing hybrid organic-inorganic solid with very large pores and high magnetic characteristics. Angew Chem. Int. Ed. 41, 281–284 (2002)

    Article  CAS  Google Scholar 

  5. Uemura, K., Kitagawa, S., Kondo, M., Fukui, K., Kitaura, R., Chang, H.-C., Mizutani, T.: Novel flexible frameworks od porous cobalt(II) coordination polymers that show selective guest adsorption based on the switching of hydrogen-bond pairs of amide groups. Chem. Eur. J. 88, 3587–3600 (2002)

    Google Scholar 

  6. Biradha, K., Fujita, M.: A springlike 3D-coordination network that shrinks or swells in a crystal-to-crystal manner upon guest removal or readsorption. Angwe Chem. Int. Ed. 41, 3392–3395 (2002)

    Article  CAS  Google Scholar 

  7. Atwood, J.L., Barbour, L.J., Jerga, A., Schottel, B.L.: Guest transport in a nonporous organic solid via dynamic van der Waals cooperativity. Science 298, 1000–1002 (2002)

    Article  PubMed  CAS  Google Scholar 

  8. Takamizawa, S., Nakata, E., Yokoyama, H., Mochizuki, K., Mori, W.: Carbon dioxide inclusion phases of a transformable 1D coordination polymer host [Rh2(O2CPh)4(pyz)]n, Angew. Chem. Int. Ed. 42, 4331–4334 (2003)

    Article  CAS  Google Scholar 

  9. Krause, S., Hosono, N., Kitagawa, S.: Chemistry of soft porous crystals: structural dynamics and gas adsorption properties. Angew Chem. Int. Ed. 59, 15325–15341 (2020)

    Article  CAS  Google Scholar 

  10. Kremer, C., Lützen, A.: Artificial allosteric receptors. Chem. Eur. J. 19, 6162–6192 (2013)

    Article  PubMed  CAS  Google Scholar 

  11. Lifschitz, A.M., Rosen, M.S., McGuirk, C.M., Mirkin, C.A.: Allosteric supramolecular coordination constructs. J. Am. Chem. Soc. 137, 7252–7261 (2015)

    Article  PubMed  CAS  Google Scholar 

  12. Von Krbek, L.K.S., Schally, C.A., Thordarson, P.: Assessing cooperativity in supramolecular systems. Chem. Soc. Rev. 46, 2622–2637 (2017)

    Article  Google Scholar 

  13. Akine, S.: Novel ion recognition systems based on cyclic and acyclic oligo(salen)-type ligands. J. Incl. Phenom. Macrocycl. Chem. 75, 25–54 (2012)

    Article  CAS  Google Scholar 

  14. Görbitz, C.H.: Nanotube formation by hydrophobic dipeptides. Chem. Eur. J. 7, 5153–5159 (2001)

    Article  PubMed  Google Scholar 

  15. Görbitz, C.H.: Microporous organic materials form hydrophobic dipeptides. Chem. Eur. J. 13, 1022–1031 (2007)

    Article  PubMed  CAS  Google Scholar 

  16. Adler-Abramovich, L., Gazit, E.: The physical properties of supramolecular peptide assemblies: from building block association to technological applications. Chem. Soc. Rev. 43, 6881–6893 (2014)

    Article  PubMed  CAS  Google Scholar 

  17. Soldatov, D.V., Moudrakovski, I.L., Ripmeester, J.A.: Dipeptides as microporous materials. Angew Chem. Int. Ed. 43, 6308–6311 (2004)

    Article  CAS  Google Scholar 

  18. Soldatov, D.V., Moudrakovski, I.L., Grachev, E.V., Ripmeester, J.A.: Micropores in crystalline dipeptides as seen from the crystal structure, He pycnometry, and 129Xe NMR spectroscopy. J. Am. Chem. Soc. 128, 6737–6744 (2006)

    Article  PubMed  CAS  Google Scholar 

  19. Comotti, A., Bracco, S., Distefano, G., Sozzani, P.: Methane, carbon dioxide and hydrogen storage in nanoporous dipeptide-based materials, Chem. Commun. 284–286 (2009)

  20. Afonso, R.V., Durão, Mendes, A., Damas, A.M., Gales, L.: Dipeptide crystals as excellent permselective materials: sequential exclusion of argon, nitrogen, and oxygen. Angwe Chem. Int. Ed. 49, 3034–3036 (2010)

    Article  CAS  Google Scholar 

  21. Yadav, V.N., Comotti, A., Sozzani, P., Bracco, S., Bonge-Hansen, T., Hennum, M., Görbitz, C.H.: Microporous molecular materials from dipeptides containing non-proteinogenic residues. Angew Chem. Int. Ed. 54, 15684–15688 (2015)

    Article  CAS  Google Scholar 

  22. Mantion, A., Massüger, L., Rabu, P., Palivan, C., McCusker, L.B., Tauberrt, A.: Metal-Peptide Frameworks (MPFs): “Bioinspired” metal organic frameworks. J. Am. Chem. Soc. 130, 2517–2526 (2008)

    Article  PubMed  CAS  Google Scholar 

  23. Fujita, M., Yazaki, J., Ogura, K.: Preparation of a macrocyclic polynuclear complex, [(en)Pd(4,4’-bpy)]4(NO3)8, which recognizes an organic molecule in aqueous media. J. Am. Chem. Soc. 112, 5645–5647 (1990)

    Article  CAS  Google Scholar 

  24. Fujita, M.: Metal-directed sekf-assembly of two- and three-dimensional synthetic receptors. Chem. Soc. Rev. 27, 417–425 (1998)

    Article  CAS  Google Scholar 

  25. Cook, T.R., Stang, P.J.: Recent developments in the preparation and chemistry of metallocyclces and metallacages via coordination. Chem. Rev. 115, 7001–7045 (2015)

    Article  PubMed  CAS  Google Scholar 

  26. Precástegui, E.G., Ronson, T.K., Nitschke, J.R.: Design and application of water-soluble coordination cages. Chem. Rev. 120, 13480–13544 (2020)

    Article  CAS  Google Scholar 

  27. Kitagawa, S., Kitaura, R., Noro, S.-I.: Functional porous coordination polymers. Angew Chem. Int. Ed. 43, 2334–2375 (2004)

    Article  CAS  Google Scholar 

  28. Furukawa, H., Cordova, K.E., O’Keeffe, M., Yaghi, O.M.: The chemistry and applicaitonns of metal-organic frameworks. Science 341, 1230444 (2013)

    Article  PubMed  CAS  Google Scholar 

  29. Miyake, R., Tashiro, S., Shiro, M., Tanaka, K., Shionoya, M.: Ni(II)-mediated self-assembly of artificial b-dipeptides forming a macrocyclic tetranuclear complex with interior spaces for in-line molecular arrangement. J. Am. Chem. Soc. 130, 5646–5647 (2008)

    Article  PubMed  CAS  Google Scholar 

  30. Dong, J., Liu, Y., Cui, Y.: Artificial metal-peptide assemblies: bioinspired assembly of peptides and metals through Space and across length scales. J. Am. Chem. Soc. 143, 17316–11736 (2021)

    Article  PubMed  CAS  Google Scholar 

  31. Ueda, E., Yoshikawa, Y., Kishimoto, N., Tadokoro, M., Sakurai, H., Kajiwara, N., Kojima, Y.: New bioactive zinc (II) complexes with peptides and their derivatives: synthesis, structure, and In Vitro insulinomimetic activity. Bull. Chem. Soc. Jpn 77, 981–986 (2004)

    Article  CAS  Google Scholar 

  32. Tiliakos, M., Katsoulakou, E., Terzis, A., Raptopoulou, C., Cordopatis, P., Manessi-Zoupa, E.: The dipeptide H-Aib-L-Ala-OH ligand in copper(II) chemistry: variation of product identity as a function of pH. Inorg. Chem. Commun. 8, 1085–1089 (2005)

    Article  CAS  Google Scholar 

  33. Rabone, J., Yue, Y.-F., Chong, S.Y., Stylianou, K.C., Bacsa, J., Bradshaw, D., Darling, G.R., Berry, N.G., Khimyak, Y.Z., Ganin, A., Wiper, Y., Claridge, P., Rosseinsky, J.B.: M. J.: An adaptable peptide-based porous material. Science 329, 1053–1057 (2010)

    Article  PubMed  CAS  Google Scholar 

  34. Martí-Gastaldo, C., Antypov, D., Warren, J.E., Briuggs, M.E., Chater, P.A., Wiper, P.V., Miller, G.J., Khimyak, Y.Z., Darrling, G.R., Berry, N.G., Rosseinsky, M.J.: Side-chain control of porosity closure in single-and multiple-peptide-based porous materials by cooperative folding. Nat. Chem. 6, 343–351 (2014)

    Article  PubMed  CAS  Google Scholar 

  35. Martí-Gastaldo, C., Warren, J.E., Briggs, M.E., Armstrong, J.A., Thomas, K.M., Rosseinsky, M.J.: Sponge-like behaviour in isoreticular Cu(Gly-His-X) peptide-based porous materials. Chem. Eur. J. 21, 16027–16034 (2015)

    Article  PubMed  CAS  Google Scholar 

  36. Martí-Gastaldo, C., Stylianou, W.J.E., Flack, K.C., Rosseinsky, N.L.O.: M. J.: Enhanced stability in rigid peptide-based porous materials. Angew Chem. Int. Ed. 51, 11044–11048 (2012)

    Article  CAS  Google Scholar 

  37. Katsoulidis, A.P., Park, K.S., Antypov, D., Martí-Gastaldo, C., Miller, G.J., Warren, J.E., Robertson, C.M., Blanc, F., Darling, G.R., Berry, N.G., Purton, J.A., Adams, D.J., Rosseinsky, M.j.: Guest-adaptable and water-stable peptide-based porous materials by imidazolate side chain control. Angew Chem. Int. Ed. 53, 193–198 (2014)

    Article  CAS  Google Scholar 

  38. Katsoulidis, A.P., Antypov, D., Whitehead, G.F.S., Carrington, E.J., Adams, D.J., Berry, N.G., Darling, G.R., Byer, M.S., Rossesinsky, M.J.: Chemical control of structure and guest uptake by a conformationally mobile porous material. Nature 565, 213 (2019)

    Article  PubMed  CAS  Google Scholar 

  39. Navarro-Sánchez, J., Mullor-Ruíz, I., Popescu, C., Santamaría-Pérez, D., Segura, A., Errandonea, D., González-Platas, Martí-Gastaldo, C.: Peptide metal-oragnic frameworks under pressure: flexible linkers for cooperative compression. Dalton Trans. 47, 10654–10659 (2018)

    Article  PubMed  Google Scholar 

  40. Misra, R., Saseendran, A., Dey, S., Gopi, H.N.: Metal-helix framework from short hybrid peptide flodamers. Angew Chem. Int. Ed. 58, 2251–2255 (2019)

    Article  CAS  Google Scholar 

  41. Dey, S., Misra, R., Saseendran, A., Pahan, S., Gopi, H.N.: Metal-coordinated supramoleculea polymers from the minimalistic hybrid peptide foldamers. Angew Chem. Int. Ed. 60, 9863–9868 (2021)

    Article  CAS  Google Scholar 

  42. Navarro-Sánchez, J., Argente-Garxcia, A.I., Moliner-Marrtinez, Y., Roca-Sanjuan, D., Antypov, D., Campins-Falco, P., Rosseinsky, M.J., Martí-Gastaldo, C.: Peptide metal-organic frameworks for enantioselective separation of chiral drug. J. Am. Chem. Soc. 139, 4294–4297 (2017)

    Article  PubMed  CAS  Google Scholar 

  43. Corella-Ochoa, M.N., Tapia, J.B., Rubin, H.N., Lillo, V., González-Cobos, J., Núñez-Rico, J., Balestra, S.R.G., Almora-Barrios, N., Lledós, M., Güell-Bara, A., Cabezas-Giménez, J., Escudero-Adán, E.C., Videl-Ferran, A., Calero, S., Reynolds, M., Martí-Gastaldo, C., Galán-Mascarós, J.R.: Homochiral metal-organic frameworks for enantioselective separations in liguid chromatography. J. Am. Chem. Soc. 141, 14306–14316 (2019)

    Article  PubMed  CAS  Google Scholar 

  44. Saito, A., Sawada, T., Fujita, M.: X-ray Crystallographic observation of chiral transformations within a metal-peptide pore. Angew Chem. Int. Ed. 59, 20367–20370 (2020)

    Article  CAS  Google Scholar 

  45. Miyake, R., Shionoya, M.: Reversible structural switch in the nano-caivity of crystalline metallo-macrocycle with smooth ligand exchange by non-coordinating guest stimuli. Chem. Commun. 48, 7553–7555 (2012)

    Article  CAS  Google Scholar 

  46. Miyake, R., Shionoya, M.: Concerted ligand exchange and the roles of counter anions in the reversible structural switching of crystalline peptide metallo-macorcycles. Inorg. Chem. 53, 5717–5723 (2014)

    Article  PubMed  CAS  Google Scholar 

  47. Unpublished data. We will report elsewhere in near future

  48. Miyake, R., Kuwata, C., Masumoto, Y.: Selective CO2 gas adsorption in the narrow crystalline cavities of flexible peptide metallo-macrocycles. Dalton Trans. 44, 2993–2996 (2015)

    Article  PubMed  CAS  Google Scholar 

  49. Miyake, R., Kuwata, C., Ueno, M., Yamada, T.: Humidity-responsive ON/OFF switching of gas inclusion by using cooperative opening/closing of heterogeneous crystalline cavities in a peptide NiII macrocycle, Chem. Eur. J. 24, 793–797 (2018)

    Article  CAS  Google Scholar 

  50. Sawada, T., Matsumoto, A., Fujita, M.: Coordination-driven folding and assembly of a short peptide into a protein-like two-nanometer-sized channel. Angew Chem. Int. Ed. 53, 7228–7232 (2014)

    Article  CAS  Google Scholar 

  51. Sawada, T., Yamagami, M., Akinaga, S., Miyaji, T., Fujita, M.: Porous peptide complexes by a folding-and-assembly strategy. Chem. Asian J. 12, 1715–1718 (2017)

    Article  PubMed  CAS  Google Scholar 

  52. Yamagami, M., Sawada, T., Fujita, M.: Synthetic β-barrel by metal-induced folding and assembly. J. Am. Chem. Soc. 140, 8644–8647 (2018)

    Article  PubMed  CAS  Google Scholar 

  53. Miyake, R., Ando, A., Ueno, M., Muraoka, T.: Formation of giant and small cyclic complexes from a flexible tripeptide ligand controlled by metal coordination and hydrogen bonds. J. Am. Chem. Soc. 141, 8675–8679 (2019)

    Article  PubMed  CAS  Google Scholar 

  54. Forgan, R.S., Sauvage, J.-P., Stoddart, J.F.: Chemical topology: complex molecular knots, links, and entaglements. Chem. Rev. 111, 5434–5464 (2011)

    Article  PubMed  CAS  Google Scholar 

  55. Huang, S.-L., Hor, T.S.A., Jinn, G.-X.: Metallacyclic assembly of interlocked superstructures. Coord. Chem. Rev. 333, 1–26 (2017)

    Article  CAS  Google Scholar 

  56. Gil-Ramírez, G., Leigh, D.A., Stephens, A.J.: Catenanes: fifty years of molecular links. Angew Chem. Int. Ed. 54, 6110–6150 (2015)

    Article  CAS  Google Scholar 

  57. Miyake, R.: Constructing multicomponent cooperative functional systems using metal complexes of short flexible peptides. Chem. Commun. 57, 7987–7996 (2021)

    Article  CAS  Google Scholar 

  58. Sawada, T., Yamagami, M., Ohara, K., Yamaguchi, K., Fujita, M.: Peptide [4] catenane by folding and assembly. Angew Chem. Int. Ed. 55, 4519–4522 (2016)

    Article  CAS  Google Scholar 

  59. Sawada, T., Saito, A., Tamiya, K., Shimokawa, K., Hisada, Y., Fujita, M.: Metal-peptide rings form highly entagled topologically inequivalent frameworks with the same ring- and crossing-numbers. Nat. Commun. 10, 921 (2019)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Inomata, Y., Sawada, T., Fujita, M.: Metal-peptide torus knots from flexible short peptides. Chem. 6, 294–303 (2020)

    Article  CAS  Google Scholar 

  61. Sawada, T., Inomata, Y., Shimokawa, K., Fujita, M.: A metal-peptide capsule by multiple ring threading. Nat. Commun. 10, 5687 (2019)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Inomata, Y., Sawada, T., Fujita, M.: Metal-peptide nonafoil knots and decafoil supercoils. J. Am. Chem. Soc. 143, 16734–16739 (2021)

    Article  PubMed  CAS  Google Scholar 

  63. Schnitzer, T., Paenurk, E., Trapp, N., Gershoni-Poranne, R., Wennemers, J.: Peptide-metal frameworks with meal strings guided by dipersion interactions. J. Am. Chem. Soc. 143, 644–648 (2021)

    Article  PubMed  CAS  Google Scholar 

  64. Jeong, S., Zhang, L., Kim, J., Gong, J., Choi, J., Ok, K.M., Lee, Y., Kwon, S., Lee, H.-S.: Conformational adapation of b-peptide foldamers for the formation of metal-peptide frameworks. Angew. Chem. Int. Ed. 61, e202108364 (2022)

    Google Scholar 

  65. Okada, T., Tanaka, K., Shiro, M., Shionoya, M.: Heterogeneous assembly of silver (I) and calcium(II) ions accompanying a dimer formation of cyclo(L-Ala-L-Met)3, Chem. Commun. 1483 (2005)

  66. Vairaprakash, P., Ueki, H., Tashiro, K., Yaghi, O.M.: Synthesis of metal-organic complex arrays. J. Am. Chem. Soc. 133, 759–761 (2011)

    Article  PubMed  CAS  Google Scholar 

  67. Yamada, Y., Kubota, T., Nishio, M., Tanaka, K.: Sequential and spatial organization of metal complexes inside a peptide duplex. J. Am. Chem. Soc. 136, 6505–6509 (2014)

    Article  PubMed  CAS  Google Scholar 

  68. Isozaki, K., Haga, Y., Ogata, K., Naota, T., Takaya, H.: Metal array fabrication based on ultrasound-induced self assembly of metalated dipeptides. Dalton Trans. 42, 15953–15966 (2013)

    Article  PubMed  CAS  Google Scholar 

  69. Dutta, A., Hamilton, G.A., Hartnett, H.E., Jones, A.K.: Construction of heterometallic clusters in a small peptide scaffold as [NiFe]-Hydrogenase models: development of a synthetic methodology. Inorg. Chem. 51, 9580–9588 (2012)

    Article  PubMed  CAS  Google Scholar 

  70. Miyake, R., Suganuma, E., Kimura, S., Mori, H., Okabayashi, J., Kusamoto, T.: Cyclic heterometallic interactions formed from a flexible tripeptide complex showing effective antiferromagnetic spin coupling. Angew Chem. Int. Ed. 60, 5179–5183 (2021)

    Article  CAS  Google Scholar 

  71. Miyake, R., Nakagawa, Y., Hase, M.: Selective thermal elongation of metal-meatal distances in the two-dimensional assembly of Ag(I) ions templated by assembled peptide ligands. Cryst. Growth&Des 14, 4882–4885 (2014)

    Article  CAS  Google Scholar 

  72. Miyake, R., Nitanai, Y., Nakagawa, Y., Xing, J., Harano, K., Nakamura, E., Okabayashi, J., Minamikawa, T., Urma, K., Kanaizuka, K., Kurihara, M.: Preparation of hierarchically assembled silver nanostructures based on the morphologies of crystalline peptide-silver(I) complexes, ChemPlusChem 84, 295–301: (2019)

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Acknowledgements

The author thanks the organizing committee of Host-Guest and Supramolecular Chemistry Society, Japan for giving him the SHGCS Japan Award of Excellence 2021 and the opportunity to write this review. This work was financially supported by a JSPS KAKENHI Grant-in-Aid for Scientific Research (C) (20K05539), a JSPS KAKENHI Grant-in-Aid for Young Scientists (B) (25810037), and JST PRESTO (JPMJPR151A). The author would also like to thank all the collaborators who contributed to the work described in this review. This is a paper selected for the “SHGCS Japan Award of Excellence 2021”.

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Miyake, R. Cooperative systems constructed using crystalline metal complexes of short flexible peptides. J Incl Phenom Macrocycl Chem 102, 711–722 (2022). https://doi.org/10.1007/s10847-022-01145-2

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