The Phe-Phe motif for peptide self-assembly in nanomedicine

Molecules

Volumn 20, Issue 11, 2015, Pages 19775-19788

  Marchesan, Silvia ^a   Vargiu, Attilio V ^b   Styan, Katie E ^c  

^a UNIVERSITY OF TRIESTE   (Italy)

^b UNIVERSITY OF CAGLIARI   (Italy)

^c CSIRO   (Australia)

Author keywords

Diphenylalanine; Hydrogels; Nanostructures; Peptides; Self assembly

Indexed keywords

DIPEPTIDE; DRUG CARRIER; HYDROGEL; NANOMATERIAL; PEPTIDE; PHENYLALANYLPHENYLALANINE;

CHEMISTRY; DRUG DELIVERY SYSTEM; HYDROGEL; NANOMEDICINE; NANOTECHNOLOGY; PROTEIN MOTIF;

AMINO ACID MOTIFS; DIPEPTIDES; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HYDROGELS; NANOMEDICINE; NANOSTRUCTURES; NANOTECHNOLOGY; PEPTIDES;

EID: 84949973055     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules201119658     Document Type: Review

References (83)

1. Min, Y.; Caster, J.M.; Eblan, M.J.; Wang, A.Z. Clinical Translation of Nanomedicine. Chem. Rev. 2015, 115, 11147-11190.
2. Marchesan, S.; Prato, M. Nanomaterials for (Nano)medicine. ACS Med. Chem. Lett. 2013, 4, 147-149.
3. Yu, C.Y.; Huang, W.; Li, Z.P.; Lei, X.Y.; He, D.X.; Sun, L. Progress in Self-assembling Peptide-based Nanomaterials for Biomedical Applications. Curr. Top. Med. Chem. 2016, 16, 281-290.
4. Collier, J.H.; Segura, T. Evolving the use of peptides as components of biomaterials. Biomaterials 2011, 32, 4198-4204.
5. Adams, D.J. Dipeptide and tripeptide conjugates as low-molecular-weight hydrogelators. Macromol. Biosci. 2011, 11, 160-173.
6. Fleming, S.; Ulijn, R.V. Design of nanostructures based on aromatic peptide amphiphiles. Chem. Soc. Rev. 2014, 43, 8150-8177.
7. Mba, M.; Mazzier, D.; Silvestrini, S.; Toniolo, C.; Fatás, P.; Jiménez, A.I.; Cativiela, C.; Moretto, A. Photocontrolled Self-Assembly of a Bis-Azobenzene-Containing α-Amino Acid. Chem. Eur. J. 2013, 19, 15841-15846.
8. Reches, M.; Gazit, E. Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 2003, 300, 625-627.
9. Adler-Abramovich, L.; Vaks, L.; Carny, O.; Trudler, D.; Magno, A.; Caflisch, A.; Frenkel, D.; Gazit, E. Phenylalanine assembly into toxic fibrils suggests amyloid etiology in phenylketonuria. Nat. Chem. Biol. 2012, 8, 701-706.
10. Yan, X.; Zhu, P.; Li, J. Self-assembly and application of diphenylalanine-based nanostructures. Chem. Soc. Rev. 2010, 39, 1877-1890.
11. Dudukovic, N.A.; Zukoski, C.F. Gelation of Fmoc-diphenylalanine is a first order phase transition. Soft Matter 2015, 11, 7663-7673.
12. Yan, X.; He, Q.; Wang, K.; Duan, L.; Cui, Y.; Li, J. Transition of Cationic Dipeptide Nanotubes into Vesicles and Oligonucleotide Delivery. Angew. Chem. Int. Ed. 2007, 46, 2431-2434.
13. Reches, M.; Gazit, E. Formation of Closed-Cage Nanostructures by Self-Assembly of Aromatic Dipeptides. Nano Lett. 2004, 4, 581-585.
14. Adler-Abramovich, L.; Gazit, E. Controlled patterning of peptide nanotubes and nanospheres using inkjet printing technology. J. Pept. Sci. 2008, 14, 217-223.
15. Marchesan, S.; Easton, C.D.; Kushkaki, F.; Waddington, L.; Hartley, P.G. Tripeptide self-assembled hydrogels: Unexpected twists of chirality. Chem. Commun. 2012, 48, 2195-2197.
16. Maity, S.; Nir, S.; Zada, T.; Reches, M. Self-assembly of a tripeptide into a functional coating that resists fouling. Chem. Commun. 2014, 50, 11154-11157.
17. Fu, Y.; Li, B.; Huang, Z.; Li, Y.; Yang, Y. Terminal Is Important for the Helicity of the Self-Assemblies of Dipeptides Derived from Alanine. Langmuir 2013, 29, 6013-6017.
18. Das, A.K.; Collins, R.; Ulijn, R.V. Exploiting enzymatic (reversed) hydrolysis in directed self-assembly of peptide nanostructures. Small 2008, 4, 279-287.
19. Chronopoulou, L.; Sennato, S.; Bordi, F.; Giannella, D.; di Nitto, A.; Barbetta, A.; Dentini, M.; Togna, A.R.; Togna, G.I.; Moschini, S.; et al. Designing unconventional Fmoc-peptide-based biomaterials: Structure and related properties. Soft Matter 2014, 10, 1944-1952.
20. Ostrov, N.; Gazit, E. Genetic engineering of biomolecular scaffolds for the fabrication of organic and metallic nanowires. Angew. Chem. Int. Ed. 2010, 49, 3018-3021.
21. Conlon, J.M. Purification of naturally occurring peptides by reversed-phase HPLC. Nat. Protoc. 2007, 2, 191-197.
22. Mant, C.T.; Chen, Y.; Yan, Z.; Popa, T.V.; Kovacs, J.M.; Mills, J.B.; Tripet, B.P.; Hodges, R.S. HPLC analysis and purification of peptides. Methods Mol. Biol. 2007, 386, 3-55.
23. Arai, T.; Kino, K. New L-amino acid ligases catalyzing oligopeptide synthesis from various microorganisms. Biosci. Biotechnol. Biochem. 2010, 74, 1572-1577.
24. Toledano, S.; Williams, R.J.; Jayawarna, V.; Ulijn, R.V. Enzyme-Triggered Self-Assembly of Peptide Hydrogels via Reversed Hydrolysis. J. Am. Chem. Soc. 2006, 128, 1070-1071.
25. Taylor Paul, P.; Grinter Nigel, J.; McCarthy Shelly, L.; Pantaleone David, P.; Ton Jennifer, L.; Yoshida Roberta, K.; Fotheringham Ian, G. D-Phenylalanine Biosynthesis Using Escherichia coli: Creation of a New Metabolic Pathway. In Applied Biocatalysis in Specialty Chemicals and Pharmaceuticals; American Chemical Society: Washington, DC, USA, 2001; Volume 776, pp. 65-75.
26. Ollivaux, C.; Soyez, D.; Toullec, J.-Y. Biogenesis of D-amino acid containing peptides/proteins: Where, when and how? J. Pept. Sci. 2014, 20, 595-612.
27. Fusetani, N. Antifungal peptides in marine invertebrates. ISJ 2010, 7, 53-66.
28. Yuran, S.; Reches, M. Formation of ordered biomolecular structures by the self-assembly of short peptides. J. Vis. Exp. 2013, 21, e50946.
29. Adamcik, J.; Mezzenga, R. Study of amyloid fibrils via atomic force microscopy. Curr. Opin. Coll. Interface Sci. 2012, 17, 369-376.
30. Gras, S.L.; Waddington, L.J.; Goldie, K.N. Transmission electron microscopy of amyloid fibrils. Methods Mol. Biol. 2011, 752, 197-214.
31. Wang, Z.; Zhou, C.; Wang, C.; Wan, L.; Fang, X.; Bai, C. AFM and STM study of β-amyloid aggregation on graphite. Ultramicroscopy 2003, 97, 73-79.
32. Takai, E.; Ohashi, G.; Ueki, R.; Yamada, Y.; Fujita, J.-I.; Shiraki, K. Scanning Electron Microscope Imaging of Amyloid Fibrils. Am. J. Biochem. Biotechnol. 2014, 10, 31-39.
33. Schermelleh, L.; Heintzmann, R.; Leonhardt, H. A guide to super-resolution fluorescence microscopy. J. Cell Biol. 2010, 190, 165-175.
34. Biancalana, M.; Koide, S. Molecular Mechanism of Thioflavin-T Binding to Amyloid Fibrils. Biochim. Biophys. Acta 2010, 1804, 1405-1412.
35. Howie, A.J.; Brewer, D.B. Optical properties of amyloid stained by Congo red: History and mechanisms. Micron 2009, 40, 285-301.
36. Marchesan, S.; Styan, K.; Easton, C.D.; Waddington, L.; Vargiu, A.V. Higher and lower supramolecular order for the design of self-assembled heterochiral tripeptide hydrogel biomaterials. J. Mater. Chem. B 2015, 3, 8123-8132.
37. Ryu, J.; Kim, S.-W.; Kang, K.; Park, C.B. Mineralization of Self-assembled Peptide Nanofibers for Rechargeable Lithium Ion Batteries. Adv. Mater. 2010, 22, 5537-5541.
38. Van den Hout, K.P.; Martin-Rapun, R.; Vekemans, J.A.; Meijer, E.W. Tuning the stacking properties of C3-symmetrical molecules by modifying a dipeptide motif. Chem. Eur. J. 2007, 13, 8111-8123.
39. Ryu, J.; Park, C.B. High-Temperature Self-Assembly of Peptides into Vertically Well-Aligned Nanowires by Aniline Vapor. Adv. Mater. 2008, 20, 3754-3758.
40. Görbitz, C.H. Microporous Organic Materials from Hydrophobic Dipeptides. Chem. Eur. J. 2007, 13, 1022-1031.
41. Krysmann, M.J.; Castelletto, V.; Hamley, I.W. Fibrillisation of hydrophobically modified amyloid peptide fragments in an organic solvent. Soft Matter 2007, 3, 1401-1406.
42. Pudakalakatti, S.M.; Chandra, K.; Thirupathi, R.; Atreya, H.S. Rapid Characterization of Molecular Diffusion by NMR Spectroscopy. Chem. Eur. J. 2014, 20, 15719-15722.
43. Tamamis, P.; Adler-Abramovich, L.; Reches, M.; Marshall, K.; Sikorski, P.; Serpell, L.; Gazit, E.; Archontis, G. Self-assembly of phenylalanine oligopeptides: Insights from experiments and simulations. Biophys. J. 2009, 96, 5020-5029.
44. Tuttle, T. Computational Approaches to Understanding the Self-assembly of Peptide-based Nanostructures. Isr. J. Chem. 2015, 55, 724-734.
45. Colombo, G.; Soto, P.; Gazit, E. Peptide self-assembly at the nanoscale: A challenging target for computational and experimental biotechnology. Trends Biotechnol. 2007, 25, 211-218.
46. Tamamis, P.; Kasotakis, E.; Mitraki, A.; Archontis, G. Amyloid-Like Self-Assembly of Peptide Sequences from the Adenovirus Fiber Shaft: Insights from Molecular Dynamics Simulations. J. Phys. Chem. B 2009, 113, 15639-15647.
47. Azuri, I.; Adler-Abramovich, L.; Gazit, E.; Hod, O.; Kronik, L. Why Are Diphenylalanine-Based Peptide Nanostructures so Rigid? Insights from First Principles Calculations. J. Am. Chem. Soc. 2014, 136, 963-969.
48. Guo, C.; Luo, Y.; Zhou, R.; Wei, G. Probing the Self-Assembly Mechanism of Diphenylalanine-Based Peptide Nanovesicles and Nanotubes. ACS Nano 2012, 6, 3907-3918.
49. Guo, C.; Luo, Y.; Zhou, R.; Wei, G. Triphenylalanine peptides self-assemble into nanospheres and nanorods that are different from the nanovesicles and nanotubes formed by diphenylalanine peptides. Nanoscale 2014, 6, 2800-2811.
50. Kelly, C.M.; Northey, T.; Ryan, K.; Brooks, B.R.; Kholkin, A.L.; Rodriguez, B.J.; Buchete, N.V. Conformational dynamics and aggregation behavior of piezoelectric diphenylalanine peptides in an external electric field. Biophys. Chem. 2015, 196, 16-24.
51. Jeon, J.; Mills, C.E.; Shell, M.S. Molecular Insights into Diphenylalanine Nanotube Assembly: All-Atom Simulations of Oligomerization. J. Phys. Chem. B 2013, 117, 3935-3943.
52. Frederix, P.W.J.M.; Ulijn, R.V.; Hunt, N.T.; Tuttle, T. Virtual Screening for Dipeptide Aggregation: Toward Predictive Tools for Peptide Self-Assembly. J. Phys. Chem. Lett. 2011, 2, 2380-2384.
53. Frederix, P.W.J.M.; Scott, G.G.; Abul-Haija, Y.M.; Kalafatovic, D.; Pappas, C.G.; Javid, N.; Hunt, N.T.; Ulijn, R.V.; Tuttle, T. Exploring the sequence space for (tri-)peptide self-assembly to design and discover new hydrogels. Nat. Chem. 2015, 7, 30-37.
54. Marchesan, S.; Waddington, L.; Easton, C.D.; Winkler, D.A.; Goodall, L.; Forsythe, J.; Hartley, P.G. Unzipping the role of chirality in nanoscale self-assembly of tripeptide hydrogels. Nanoscale 2012, 4, 6752-6760.
55. Yuran, S.; Razvag, Y.; Reches, M. Coassembly of aromatic dipeptides into biomolecular necklaces. ACS Nano 2012, 6, 9559-9566.
56. Marchesan, S.; Easton, C.D.; Styan, K.E.; Waddington, L.J.; Kushkaki, F.; Goodall, L.; McLean, K.M.; Forsythe, J.S.; Hartley, P.G. Chirality effects at each amino acid position on tripeptide self-assembly into hydrogel biomaterials. Nanoscale 2014, 6, 5172-5180.
57. Reches, M.; Gazit, E. Controlled patterning of aligned self-assembled peptide nanotubes. Nat. Nanotechnol. 2006, 1, 195-200.
58. Song, Y.; Challa, S.R.; Medforth, C.J.; Qiu, Y.; Watt, R.K.; Pena, D.; Miller, J.E.; Swol, F.V.; Shelnutt, J.A. Synthesis of peptide-nanotube platinum-nanoparticle composites. Chem. Commun. 2004, 1044-1045.
59. Yuran, S.; Razvag, Y.; Das, P.; Reches, M. Self-assembly of azide containing dipeptides. J. Pept. Sci. 2014, 20, 479-486.
60. Pappas, C.G.; Frederix, P.W.J.M.; Mutasa, T.; Fleming, S.; Abul-Haija, Y.M.; Kelly, S.M.; Gachagan, A.; Kalafatovic, D.; Trevino, J.; Ulijn, R.V.; et al. Alignment of nanostructured tripeptide gels by directional ultrasonication. Chem. Commun. 2015, 51, 8465-8468.
61. Bonetti, A.; Pellegrino, S.; Das, P.; Yuran, S.; Bucci, R.; Ferri, N.; Meneghetti, F.; Castellano, C.; Reches, M.; Gelmi, M.L. Dipeptide Nanotubes Containing Unnatural Fluorine-Substituted β-Diarylamino Acid and L-Alanine as Candidates for Biomedical Applications. Org. Lett. 2015, 17, 4468-4471.
62. Liu, J.; Liu, J.; Chu, L.; Zhang, Y.; Xu, H.; Kong, D.; Yang, Z.; Yang, C.; Ding, D. Self-Assembling Peptide of D-Amino Acids Boosts Selectivity and Antitumor Efficacy of 10-Hydroxycamptothecin. ACS Appl. Mater. Interfaces 2014, 6, 5558-5565.
63. Li, J.; Gao, Y.; Kuang, Y.; Shi, J.; Du, X.; Zhou, J.; Wang, H.; Yang, Z.; Xu, B. Dephosphorylation of D-Peptide Derivatives to Form Biofunctional, Supramolecular Nanofibers/Hydrogels and Their Potential Applications for Intracellular Imaging and Intratumoral Chemotherapy. J. Am. Chem. Soc. 2013, 135, 9907-9914.
64. Mao, L.N.; Wang, H.M.; Tan, M.; Ou, L.L.; Kong, D.L.; Yang, Z.M. Conjugation of two complementary anti-cancer drugs confers molecular hydrogels as a co-delivery system. Chem. Commun. 2012, 48, 395-397.
65. Li, J.; Kuang, Y.; Gao, Y.; Du, X.; Shi, J.; Xu, B. D-amino acids boost the selectivity and confer supramolecular hydrogels of a nonsteroidal anti-inflammatory drug (NSAID). J. Am. Chem. Soc. 2013, 135, 542-545.
66. Liang, G.; Yang, Z.; Zhang, R.; Li, L.; Fan, Y.; Kuang, Y.; Gao, Y.; Wang, T.; Lu, W.W.; Xu, B. Supramolecular Hydrogel of a D-Amino Acid Dipeptide for Controlled Drug Release in Vivo. Langmuir 2009, 25, 8419-8422.
67. Marchesan, S.; Qu, Y.; Waddington, L.J.; Easton, C.D.; Glattauer, V.; Lithgow, T.J.; McLean, K.M.; Forsythe, J.S.; Hartley, P.G. Self-assembly of ciprofloxacin and a tripeptide into an antimicrobial nanostructured hydrogel. Biomaterials 2013, 34, 3678-3687.
68. Marchesan, S.; Waddington, L.; Easton, C.D.; Kushkaki, F.; McLean, K.M.; Forsythe, J.S.; Hartley, P.G. Tripeptide Self-Assembled Hydrogels: Soft Nanomaterials for Biological Applications. Bio Nano Science 2013, 3, 21-29.
69. Johnson, E.K.; Adams, D.J.; Cameron, P.J. Peptide based low molecular weight gelators. J. Mater. Chem. 2011, 21, 2024-2027.
70. Dasgupta, A.; Mondal, J.H.; Das, D. Peptide hydrogels. RSC Adv. 2013, 3, 9117-9149.
71. Martin, A.D.; Robinson, A.B.; Mason, A.F.; Wojciechowski, J.P.; Thordarson, P. Exceptionally strong hydrogels through self-assembly of an indole-capped dipeptide. Chem. Commun. 2014, 50, 15541-15544.
72. Raeburn, J.; Zamith Cardoso, A.; Adams, D.J. The importance of the self-assembly process to control mechanical properties of low molecular weight hydrogels. Chem. Soc. Rev. 2013, 42, 5143-5156.
73. Jayawarna, V.; Ali, M.; Jowitt, T.A.; Miller, A.F.; Saiani, A.; Gough, J.E.; Ulijn, R.V. Nanostructured Hydrogels for Three-Dimensional Cell Culture Through Self-Assembly of Fluorenylmethoxycarbonyl-Dipeptides. Adv. Mater. 2006, 18, 611-614.
74. Zhou, M.; Smith, A.M.; Das, A.K.; Hodson, N.W.; Collins, R.F.; Ulijn, R.V.; Gough, J.E. Self-assembled peptide-based hydrogels as scaffolds for anchorage-dependent cells. Biomaterials 2009, 30, 2523-2530.
75. Kuang, Y.; Shi, J.; Li, J.; Yuan, D.; Alberti, K.A.; Xu, Q.; Xu, B. Pericellular hydrogel/nanonets inhibit cancer cells. Angew. Chem. Int. Ed. 2014, 53, 8104-8107.
76. Das, P.; Yuran, S.; Yan, J.; Lee, P.S.; Reches, M. Sticky tubes and magnetic hydrogels co-assembled by a short peptide and melanin-like nanoparticles. Chem. Commun. 2015, 51, 5432-5435.
77. Adler-Abramovich, L.; Reches, M.; Sedman, V.L.; Allen, S.; Tendler, S.J.; Gazit, E. Thermal and chemical stability of diphenylalanine peptide nanotubes: Implications for nanotechnological applications. Langmuir 2006, 22, 1313-1320.
78. Yemini, M.; Reches, M.; Gazit, E.; Rishpon, J. Peptide nanotube-modified electrodes for enzyme-biosensor applications. Anal. Chem. 2005, 77, 5155-5159.
79. Ikezoe, Y.; Washino, G.; Uemura, T.; Kitagawa, S.; Matsui, H. New Autonomous Motors of Metal-Organic Framework (MOF) Powered by Reorganization of Self-Assembled Peptides at interfaces. Nat. Mater. 2012, 11, 1081-1085.
80. Gan, Z.; Wu, X.; Zhu, X.; Shen, J. Light-Induced Ferroelectricity in Bioinspired Self-Assembled Diphenylalanine Nanotubes/Microtubes. Angew. Chem. Int. Ed. 2013, 52, 2055-2059.
81. Ryan, K.; Beirne, J.; Redmond, G.; Kilpatrick, J.I.; Guyonnet, J.; Buchete, N.V.; Kholkin, A.L.; Rodriguez, B.J. Nanoscale Piezoelectric Properties of Self-Assembled Fmoc-FF Peptide Fibrous Networks. ACS Appl. Mater. Interfaces 2015, 7, 12702-12707.
82. Handelman, A.; Lavrov, S.; Kudryavtsev, A.; Khatchatouriants, A.; Rosenberg, Y.; Mishina, E.; Rosenman, G. Nonlinear Optical Bioinspired Peptide Nanostructures. Adv. Opt. Mater. 2013, 1, 875-884.
83. Ryu, J.; Lim, S.Y.; Park, C.B. Photoluminescent Peptide Nanotubes. Adv. Mater. 2009, 21, 1577-1581.