Proteins represent the most sophisticated building blocks available to an organism and to the laboratory chemist. Yet, in contrast to nearly all other types of molecular building blocks, the designed self-assembly of proteins has largely been inaccessible because of the chemical and structural heterogeneity of protein surfaces. To circumvent the challenge of programming extensive non-covalent interactions to control protein self-assembly, we have previously exploited the directionality and strength of metal coordination interactions to guide the formation of closed, homoligomeric protein assemblies. Here, we extend this strategy to the generation of periodic protein arrays. We show that a monomeric protein with properly oriented coordination motifs on its surface can arrange, on metal binding, into one-dimensional nanotubes and two- or three-dimensional crystalline arrays with dimensions that collectively span nearly the entire nano- and micrometre scale. The assembly of these arrays is tuned predictably by external stimuli, such as metal concentration and pH.
At a glance
- Life as a nanoscale phenomenon. Angew. Chem. Int. Ed. 47, 5306–5320 (2008).
- Supramolecular chemistry: functional structures on the mesoscale. Proc. Natl Acad. Sci. USA 98, 11849–11850 (2001). , , &
- Emulating biology: building nanostructures from the bottom up. Proc. Natl Acad. Sci. USA 99, 6451–6455 (2002). &
- Synthesis of cadmium sulphide superlattices using self-assembled bacterial S-layers. Nature 389, 585–587 (1997). , , &
- Ordered nanoparticle arrays formed on engineered chaperonin protein templates. Nature Mater. 1, 247–252 (2002). et al.
- Fabricating genetically engineered high-power lithium-ion batteries using multiple virus genes. Science 324, 1051–1055 (2009). et al.
- Folding DNA to create nanoscale shapes and patterns. Nature 440, 297–302 (2006).
- From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal. Nature 461, 74–77 (2009). et al.
- Organization of intracellular reactions with rationally designed RNA assemblies. Science 333, 470–474 (2011). , , &
- Building programmable jigsaw puzzles with RNA. Science 306, 2068–2072 2004. et al.
- Responsive gels formed by the spontaneous self-assembly of peptides into polymeric beta-sheet tapes. Nature 386, 259–262 (1997). et al.
- Rational design and application of responsive [alpha]-helical peptide hydrogels. Nature Mater. 8, 596–600 (2009). et al.
- Computational design of protein–protein interactions. Curr. Opin. Chem. Biol. 8, 91–97 (2004). &
- Self-assembly of a tetrahedral lectin into predesigned diamond-like protein crystals. Angew. Chem. Int. Ed. 38, 2363–2366 (1999). , , &
- Self-assembly of proteins into designed networks. Science 302, 106–109 (2003). &
- In vitro self-assembly from a simple protein of tailorable nanotubes building block. Proc. Natl Acad. Sci. USA 105, 3733–3738 (2008). , , , &
- Nanohedra: using symmetry to design self assembling protein cages, layers, crystals, and filaments. Proc. Natl Acad. Sci. USA 98, 2217–2221 (2001). , &
- Generation of protein lattices by fusing proteins with matching rotational symmetry. Nature Nanotech. 6, 558–562 (2011). , , &
- Supermolecules by design. Acc. Chem. Res. 32, 975–982 (1999). &
- Self-assembly of discrete cyclic nanostructures mediated by transition metals. Chem. Rev. 100, 853–907 (2000). , &
- Strategies for the construction of supramolecular compounds through coordination chemistry. Angew. Chem. Int. Ed. 40, 2022–2043 (2001). &
- Metal-directed protein self-assembly. Acc. Chem. Res. 43, 661–672 (2010). , &
- Expanding the utility of proteins as platforms for coordination chemistry. Coord. Chem. Rev. 255, 790–803 (2011). , , &
- Controlling protein–protein interactions through metal coordination: assembly of a 16-helix bundle protein. J. Am. Chem. Soc. 129, 13374–13375 (2007). , &
- Control of protein oligomerization symmetry by metal coordination: C2 and C3 symmetrical assemblies through CuII and NiII coordination. Inorg. Chem. 48, 2726–2728 (2009). , , , &
- RosettaDesign server for protein design. Nucl. Acids Res. 34, W235–238 (2006). &
- Principles of protein–protein interactions. Proc. Natl Acad. Sci. USA 93, 13–20 (1996). &
- Three-dimensional structure of E. coli core RNA polymerase: promoter binding and elongation conformations of the enzyme. Cell 83, 365–373 (1995). , &
- Metal ion/buffer interactions. Eur. J. Biochem. 107, 455–466 (1980). et al.
- Cryo-reconstructions of P22 polyheads suggest that phage assembly is nucleated by trimeric interactions among coat proteins. Phys. Biol. 7, 045004 (2010). et al.
- Tetramethylrhodamine dimer formation as a spectroscopic probe of the conformation of Escherichia coli ribosomal protein L7/L12 dimers. J. Biol. Chem. 271, 7568–7573 (1996). et al.
- Effect of dimer formation of electronic absorption and emission-spectra of ionic dyes – rhodamines and other common dyes. J. Phys. Chem. 78, 380–387 (1974). , &
- Microtubule structure at 8 Ångstrom resolution. Structure 10, 1317–1328 (2002). , , , &
- Three-dimensional structure of a cloning vector: X-ray diffraction studies of filamentous bacteriophage M13 at 7 Å resolution. J. Mol. Biol. 226, 455–470 (1992). , &
- S-layer proteins. J. Bacteriol. 182, 859–868 (2000). &
- Hydrogen-bonding networks and RNA bases revealed by cryo electron microscopy suggest a triggering mechanism for calcium switches. Proc. Natl Acad. Sci. USA 108, 9637–9642 (2011). &
- Overview of the CCP4 suite and current developments. Acta Cryst. D 67, 235–242 (2011). et al.
- Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007). et al.
- Refinement of macromolecular structures by the maximum-likelihood method. Acta Cryst. D 53, 240–255 (1996). , &
- Coot: model-building tools for molecular graphics. Acta Cryst. D 60, 2126–2132 (2004). &
- The PYMOL molecular graphics system (DeLano Scientific, San Carlos, California (http://www.pymol.org), 2003).
- 2dx – User-friendly image processing for 2D crystals. J. Struct. Biol. 157, 64–72 (2007). , , &
- EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82–97 (1999). , &
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