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Published online before print December 22, 2006, 10.1110/ps.062590807
Protein Science (2007), 16:323-328. Published by Cold Spring Harbor Laboratory Press. Copyright © 2007 The Protein Society
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PROTEIN STRUCTURE REPORT

Self-assembly of coiled-coil tetramers in the 1.40 Å structure of a leucine-zipper mutant

Yiqun Deng1, Qi Zheng1, Jie Liu1, Chao-Sheng Cheng1, Neville R. Kallenbach2, and Min Lu1

1 Department of Biochemistry, Weill Medical College of Cornell University, New York, New York 10021, USA
2 Department of Chemistry, New York University, New York, New York 10003, USA

(RECEIVED September 28, 2006; FINAL REVISION November 8, 2006; ACCEPTED November 8, 2006)


   Abstract
TOP
 Abstract
Introduction
 Results and Discussion
 Materials and methods
 Acknowledgments
 References
 
The hydrophobic core of the GCN4 leucine-zipper dimerization domain is formed by a parallel helical association between nonpolar side chains at the a and d positions of the heptad repeat. Here we report a self-assembling coiled-coil array formed by the GCN4-pAe peptide that differs from the wild-type GCN4 leucine zipper by alanine substitutions at three charged e positions. GCN4-pAe is incompletely folded in normal solution conditions yet self-assembles into an antiparallel tetraplex in crystals by formation of unanticipated hydrophobic seams linking the last two heptads of two parallel double-stranded coiled coils. The GCN4-pAe tetramers in the lattice associate laterally through the identical interactions to those in the intramolecular dimer–dimer interface. The van der Waals packing interaction in the solid state controls extended supramolecular assembly of the protein, providing an unusual atomic scale view of a mesostructure.

Keywords: protein engineering; coiled-coil assembly; supramolecular structure


   Introduction
TOP
 Abstract
 Introduction
Results and Discussion
 Materials and methods
 Acknowledgments
 References
 
Coiled-coil motifs have provided a fundamental model system for investigating the interplay between amino acid sequence and structure of {alpha}-helical protomers (Bryson et al. 1995; Kohn et al. 1997; Lupas and Gruber 2005; Woolfson 2005). Coiled-coil proteins commonly share a seven-residue sequence repeat, (a-b-c-d-e-f-g) n , with hydrophobic amino acids at positions a and d and polar residues generally elsewhere (McLachlan and Stewart 1975). The nonpolar a and d side chains associate via knobs-into-holes packing to create the interacting surface between supercoiled {alpha}-helical ribbons (Crick 1953; Harbury et al. 1993). Residues at the flanking e and g positions are frequently charged and have been shown to influence helix orientation preference and partner specificity through interhelical ionic interactions (Betz et al. 1995). Despite the constraints of sequence regularity and symmetry, coiled coils exhibit remarkable diversity in the number, heptad register, and orientation of the associating helices (Bryson et al. 1995; Kohn et al. 1997; Lupas and Gruber 2005; Woolfson 2005). While peptide models such as GCN4 leucine-zipper variants have led to considerable progress in defining principles of coiled-coil formation (Harbury et al. 1993; Bryson et al. 1995; Woolfson 2005), the rules and mechanisms that govern supramolecular coiled-coil assemblies in biological systems such as cytoskeleton and extracellular matrix remain incompletely understood. Here we report the 1.40 Å resolution crystal structure of a self-assembling coiled-coil peptide that reveals the side-to-side aggregation of tetramers through specific van der Waals packing interactions.


   Results and Discussion
TOP
 Abstract
 Introduction
 Results and Discussion
Materials and methods
 Acknowledgments
 References
 
Design of the GCN4-pAe peptide
We have recently shown that introducing apolar side chains such as alanine at the normally charged g positions in the dimeric GCN4 leucine zipper can specify formation of an antiparallel four-helix structure (Deng et al. 2006). In the hydrophobic core of this tetramer, buried a, d, g side chains interlock in a nonclassical knobs-against-knobs packing pattern in addition to the traditional knobs-into-holes pattern. This variation in helix–helix interactions suggests that distinct van der Waals interactions beyond the a and d side chains offer routes to control the global architecture of coiled coils. To explore the structural determinants of heptad repeats containing three hydrophobic positions and evaluate the relative roles of the e and g positions, we engineered a leucine-zipper mutant called GCN4-pAe by the complete substitution of each charged amino acid at the e positions in the classical GCN4-pR dimer sequence with alanine (see Fig. 1A legend). The GCN4-pAe peptide was expressed in Escherichia coli and purified by reverse-phase HPLC.


Figure 1
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  		Figure 1. Crystal structure of the GCN4-pAe tetramer. (A) Lateral view of the tetramer. The sequence of the GCN4-pAe peptide is MK VKQLADK VEELLSK NYHLANE VARLAKL VGER, with e heptad positions underlined. Residues at the a positions are shown as red van der Waals surfaces, and the d positions are green. Blue van der Waals surfaces identify Ala21(e) and Ala28(e), and pink surfaces identify Glu23(g) and Leu30(g). The N termini of the A–B (cyan) and C–D (light pink) dimers are indicated. (B) Cross-section of the A–B dimer in the Leu13(d) layer. The 1.40 Å 2F obs – F calc electron density map (contoured at 1.5{sigma}) is shown with the refined molecular model. (C) Cross-section of the A–B dimer in the Asn17(a) layer. Water molecules are shown as red spheres. Hydrogen bonds are denoted by pink dotted lines, and hydrogen-bond distances are given in Å. (D) Superposition of the backbone conformations of the GCN4-pAe tetramer and two wild-type leucine-zipper dimers (green).

 
Formation of the GCN4-pAe dimer in solution
The circular dichroism (CD) spectrum of GCN4-pAe exhibits an ellipticity of –21,500 deg cm2 dmol–1 at 222 nm and a ratio of ~1.03 for the ellipticity at 222 nm to the ellipticity at 208 nm (data not shown), consistent with ~65% helical structure at 4°C in TBS (pH 8.0). GCN4-pAe undergoes a cooperative and reversible thermal unfolding transition with a midpoint (T m value) of 54°C at 200 µM peptide, compared with a T m of 63°C for the parent molecule GCN4-pR under the same conditions (data not shown). Equilibrium analytical ultracentrifugation indicates that GCN4-pAe sediments as a dimeric species with no systematic dependence of apparent molecular mass on protein concentration from 50–800 µM (data not shown). Nonetheless, analysis of residual differences from the dimeric model reveals a systematic error (data not shown), indicating that the partially folded GCN4-pAe molecule is prone to associate in solution. Thus replacement of the three charged e residues by nonpolar alanine side chains affects both the secondary structure and dimer association of the parent GCN4-pR peptide. Conserved, charged residues at the e and g positions of the GCN4 leucine zipper clearly play an important role in regulating structural features of interhelical interaction specificity (Kohn et al. 1995, 1998; Deng et al. 2006; Liu et al. 2006a,b; Yadav et al. 2006).

Crystal structure of the GCN4-pAe tetramer
The X-ray crystal structure of the GCN4-pAe peptide was determined at 1.40 Å resolution by molecular replacement. The final experimental electron density map is of excellent quality and reveals the positions of 128 amino acid residues of the tetramer in the asymmetric unit (eight residues at the chain termini are disordered). (Note that this extent of structural order is well above the ~65% {alpha}-helical content of the peptide in solution.) The refined model has a conventional R-factor of 18.3% and a free R-factor of 21.9%. Data collection and refinement statistics are summarized in Table 1. Unexpectedly, GCN4-pAe forms an unusual dimer of two interacting coiled-coil dimers (A–B and C–D) in crystals (Fig. 1A). The last four helical turns from each peptide chain entwine obliquely to form an antiparallel four-helix bundle so that the first five helical turns are extended into two parallel coiled-coil dimer arms.


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  		Table 1. Data collection and refinement statistics

 
The A–B and C–D dimers each adopt an identical parallel two-stranded coiled-coil conformation with a root mean square deviation (RMSD) between equivalent C{alpha} atom positions of 0.20 Å; the heptad repeat is maintained in register through the entire 30-residue region (Lys2–Val31). The superhelix pitch, supercoil radius, and residues per supercoil turn in these dimeric coiled coils are about the same as those in the wild-type GCN4-p1 leucine zipper (O'Shea et al. 1991). In effect, the wild-type, A–B, and C–D dimers can be superimposed on each other with an RMSD for the C{alpha} atoms of 0.50 Å (Fig. 1D). Moreover, the knobs-into-holes side chain packing in A–B and C–D dimer interfaces closely matches that in GCN4-p1 (Fig. 1B,C). All core side chains at the a and d positions (excluding Asn17 in the A and C chains) in the GCN4-pAe structure adopt their most preferred rotamer conformations in {alpha}-helices. The Asn17 residues of the A and C chains assume dihedral angles {chi} 1 and {chi} 2 near –177°, 30°, thereby satisfying their interhelix hydrogen-bonding potential (Fig. 1C). The same buried polar interaction directs formation of the parallel leucine-zipper dimer (Harbury et al. 1993).

Lateral association of GCN4-pAe tetramers
What interactions might then explain the precise native-like supramolecular assembly of GCN4-pAe helical tetramers in the crystalline state? The crystal structure displays a distinctive packing arrangement in which continuous strips of GCN4-pAe tetraplexes are situated closely perpendicular to the helical axis (Fig. 2A). Because an approximate dyad is perpendicular to the superhelical axis in the tetramer, distinct interdimer van der Waals packing appears to anchor the last four helical turns of successive tetraplexes in the crystal (see below). Conversely, because GCN4-pAe lacks interdimer association and has a substantially reduced helical structure under native folding conditions in solution, the crystal lattice presumably provides hydrophobic interactions that lock a labile dimer solution structure into a defined antiparallel tetramer in the solid state.


Figure 2
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  		Figure 2. Interfacial interactions between GCN4-pAe dimers. (A) Side view showing side-to-side aggregation of dimers. The side chains of residues 19–32 that form the dimer–dimer interface are displayed. (B) Helix-to-helix packing in the Leu-A20(d)–Leu-C30(g)–Val-D31(a) layer. The 1.40 Å 2F obs – F calc electron density map contoured at 1.5{sigma} is shown with the refined molecular model. (C) Helix to helix packing in the Val-B24(a)–Leu-C27(d)–Ala-D28(e) layer. (D) Helical wheel projection of residues 19–32 of the GCN4-pAe tetramer, depicting interdimer packing interactions (dotted lines).

 
Interacting surface of GCN4-pAe dimers
The antiparallel A–B and C–D helices are offset by ~0.25 heptad with respect to each other (note that the helical offset is zero in the parallel dimer structures). As a result, the apolar interface between GCN4-pAe dimers (residues 19–32) shows a unique interdigitation between side chains at the a, d, e, and g positions (rather than forming discrete layers of side chain interactions in classical coiled-coil structures). The side chains of Leu20(d) and Leu27(d) of helix A intercalate into grooves formed between Val31(a) and Val24(a) of helix D and Leu30(g) and Glu23(g) of helix C (Fig. 2B); those at the d positions of helix C associate with the a and g residues of the B and A helices. Similarly, the side chains of Val24(a) and Val31(a) of helix B fit into grooves formed by Leu27(d) and Leu20(d) of helix C and Ala28(e) and Ala21(e) of helix D (Fig. 2C); those at the a positions of helix D pack against the d and e residues of the A and B helices. Moreover, the g side chains of helix A point into triangular spaces between the c, d, and g residues of the neighboring C helix and vice versa; those at the e positions of helix B pack into triangular spaces between the a, b, and e residues of helix D and vice versa. Thus, the a, d, e, and g residues of the last two heptads form an extended hydrophobic core in the intermolecular tetramer (Fig. 2D); the dimer–dimer interface buries ~1880 Å2 of surface area. In summary, the high-resolution crystal structure of the GCN4-pAe tetramer shows specific tertiary packing among helices, notwithstanding that GCN4-pAe is incompletely folded in solution.

Structure of the intermolecular array
The interactions that stabilize the dimer-dimer interface in the GCN4-pAe tetrameric domain propagate outward to create a two-dimensional coiled-coil array. The reason appears to be the almost perfect symmetry of the antiparallel tetramers, which allows a "tongue-into-groove" extension of the dimer–dimer interface. In other words, the interactions between intra- and intermolecular dimers are identical. This gives rise to an extended layer of interlocked tetramers in the crystal. These results demonstrate that engineering van der Waals packing at the e and g positions of the heptad repeat can stabilize a lateral association of GCN4-pAe coiled-coil dimers during crystallization. The precision of this process is reflected by the high resolution of the crystal structure (1.40 Å) with low temperature factors (24.6 and 33.9 Å2 for protein and solvent atoms, respectively).

It is noteworthy that many designed coiled-coil peptides tend to show a lateral form of association (Pandya et al. 2000; Ogihara et al. 2001; Potekhin et al. 2001; Ryadnov and Woolfson 2003a,b; Zimenkov et al. 2004; Wagner et al. 2005), leading to fibril formation rather than discrete assemblies. Understanding the molecular basis of the formation of this kind of interaction might allow one to engineer phased-hydrophobic interactions capable of assembly to create more precise supramolecular aggregates that can be exploited for elaboration of novel biomaterials. The diversity of internal van der Waals packing interactions revealed in GCN4-pAe and in previous designs (Potekhin et al. 2001; Ryadnov and Woolfson 2003a; Zimenkov et al. 2004; Wagner et al. 2005; Deng et al. 2006; Liu et al. 2006a,b) might circumvent problems of uncontrolled self-assembly that have beset efforts to use electrostatics alone to control self-assembly. Determining rules for these higher-order coiled-coil interactions should also provide insights into biologically important natural assemblies. The full range and complexity of coiled-coil interfaces needs to be deciphered at a fundamental level to fully understand the variety of natural as well as unnatural structures.


   Materials and methods
TOP
 Abstract
 Introduction
 Results and Discussion
 Materials and methods
Acknowledgments
 References
 
Protein expression and purification
The GCN4-pAe peptide was expressed in Escherichia coli strain BL21(DE3)/pLysS (Novagen) using a modified pET3a vector (Lu et al. 1999). Cells were grown at 37°C in LB media to an optical density of 0.6 at 600 nm and induced with isopropylthio-beta-D-galactoside for 3 h at 37°C. Bacterial cells were lysed at 0°C by glacial acetic acid and centrifuged (35,000g for 30 min) to separate the soluble fraction from inclusion bodies. Peptides from the soluble fraction were purified to homogeneity by reverse-phase HPLC on a C18 preparative column using a water-acetonitrile gradient in the presence of 0.1% trifluoroacetic acid and lyophilized. Peptide identities were confirmed by electrospray mass spectrometry. Protein concentrations were determined using the method of Edelhoch (Edelhoch 1967).

Biophysical experiments
Circular dichroism spectra were acquired on an Aviv 62DS spectropolarimeter at 0°C in TBS (pH 8.0). A [{theta}]222 value of –33,000 deg cm2 dmol–1 was taken to correspond to 100% helix. Thermal melts were performed on in the same buffer by measuring [{theta}]222 in 2°C steps with a 2-min equilibration time and a 30-sec integration time. Values of midpoint unfolding transitions (T m) were estimated by evaluating the maximum of the first derivative of [{theta}]222 versus temperature data. Analytical ultracentrifugation measurements were performed on a Beckman XL-A analytical ultracentrifuge as described (Shu et al. 1999). Peptide solutions were dialyzed overnight against TBS (pH 8.0), loaded at initial concentrations of 50, 200, and 800 µM, and analyzed at rotor speeds of 31,000 and 34,000 rpm using an An-60 Ti rotor. Data were acquired at two wavelengths per rotor speed setting and processed simultaneously with a nonlinear least-squares fitting routine (Johnson et al. 1981). Solvent density and protein partial specific volume were calculated according to solvent and protein composition, respectively (Laue et al. 1992).

Crystallization and structure determination
GCN4-pAe was crystallized at room temperature using the hanging drop vapor diffusion method by equilibrating against reservoir buffer (0.1 M sodium citrate at pH 5.4, 1 M NH4H2PO4), a solution containing 1 µL of 15 mg/mL peptide in water and 1 µL of reservoir buffer. Crystals belong to space group P21 (a = 20.1 Å, b = 87.9 Å, c = 35.5 Å, beta = 103.8°) and contain four monomers in the asymmetric unit. The crystals were harvested in 0.1 M sodium citrate (pH 5.4), 0.6 M NH4H2PO4, and 25% glycerol and frozen in liquid nitrogen. Diffraction data were recorded at 100 K on a MAR345 image plate at the beamline X4C of the National Synchrotron Light Source at Brookhaven National Laboratory. Reflection intensities were integrated and scaled with the programs DENZO and SCALEPACK (Table 1) (Otwinowski and Minor 1997). Initial phases were determined by molecular replacement with Phaser (Storoni et al. 2004) using the structure of the GCN4-pVe monomer (Protein Data Bank [PDB] accession code 2IPZ) as a search model. Crystallographic refinement of the GCN4-pAe structure was carried out with Refmac (Murshudov et al. 1997). Density interpretation and manual model building were done with the program O (Jones et al. 1991). Refinement was concluded with overall anisotropic thermal factors by using TLS groups for each monomer (Schomaker and Trueblood 1998). The final model (R cryst = 18.3% and R free = 21.9% for the resolution range 43.9–1.40 Å) consists of residues 2–31 (monomer A), 2–34 (monomer B), 2–32 (monomer C), 1–34 (monomer D) in the asymmetric unit, four phosphate ions, and 129 water molecules. All protein residues are in the most favored regions of the Ramachandran plot. The structural coordinates have been deposited in the Protein Data Bank (accession code 2NRN).

Structure analysis
Coiled-coil parameters were calculated with the program TWISTER (Strelkov and Burkhard 2002). The RMSDs were calculated with LSQKAB in CCP4i program suite (Potterton et al. 2003). Residues 3–31 of GCN4-pAe and residues 2–30 of GCN4-p1 were used in the calculations. Buried surface areas were calculated from the difference of the accessible side chain surface areas of the tetramer structure and of the individual helical monomers using CNS 1.0 (Brunger et al. 1998). Figures were generated using MOLSCRIPT (Kraulis 1991), Raster 3D (Merritt and Bacon 1997), and SETOR (Evans 1993).


   Footnotes
 
Reprint requests to: Min Lu, Department of Biochemistry, Weill Medical College of Cornell University, 1300 York Avenue, New York, NY 10021, USA; e-mail: mlu{at}med.cornell.edu; fax: (212) 746-8875.

Abbreviations: TBS, Tris-buffered saline; CD, circular dichroism; [{theta}]222, molar ellipticity at 222 nm; T m, midpoint of the thermal unfolding transition; RMS, root mean square; LB, Luria-Bertani; IPTG, isopropylthio-beta-D-galactoside; HPLC, high-performance liquid chromatography.

Article published online ahead of print. Article and publication date are at http://www.proteinscience.org/cgi/doi/10.1110/ps.062590807.


   Acknowledgments
TOP
 Abstract
 Introduction
 Results and Discussion
 Materials and methods
 Acknowledgments
References
 
We thank John Schwanof at the National Synchrotron Light Source for support at beamline X4A. This work was supported by NIH grant AI042382 and by the Irma T. Hirschl Trust.


   References
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 Abstract
 Introduction
 Results and Discussion
 Materials and methods
 Acknowledgments
 References
 
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