Supplementary Material
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- Ξάνθος Βιλαέτης
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1 MMP-inhibitor interaction: the solution structure of the catalytic domain of Human Matrix metalloproteinase -3 with different inhibitors Luis A. Alcaraz 1,2, Lucia Banci 1,3, Ivano Bertini 1,3, Francesca Cantini 1, Antonio Donaire 4, Leonardo Gonnelli 1 Magnetic Resonance Center (CERM) University of Florence, Via L. Sacconi 6, Sesto Fiorentino, Italy (1); From Instituto de Biologia Molecular y Celular, Universidad Miguel Hernandez, Edificio Torregaitan, Elche (Alicante), Spain (2); Department of Chemistry - University of Florence, Via della Lastruccia 3, Sesto Fiorentino, Italy (3); Department of Inorganic Chemistry, Universidad de Murcia, Campus Universitario de Espinardo, Apdo. 4021, Murcia, Spain (4). Address correspondence to: Prof. Ivano Bertini Magnetic Resonance Center, University of Florence Via L. Sacconi, Sesto Fiorentino, ITALY Fax: Tel: ivanobertini@cerm.unifi.it Supplementary Material
2 Figure S1. Schematic representation of the active-site of MMPs interacting with a polipeptide substrate (A) and with the inhibitor NNGH (B). Numbering is according to MMP3 sequence. A B
3 Figure S2. RMSD values per residue to the mean structure for the backbone (filled squares) and all heavy atoms (open circles) of the REM family of 30 conformers of MMP3-NNGH. The secondary structure elements of MMP3-NNGH are also reported at the top. RMSD (Å) β1 α1 β2 β3 β4 β5 α2 α Residue Number
4 Figure S3. 15 N R 1 and R 2 relaxation data and heteronuclear NOEs of the MMP3-NNGH measured at 600 MHz and 298 K. The secondary structure elements of MMP3-NNGH are also reported at the top. The fits and their uncertainties were calculated by means of the Levenberg-Marquardt algorithm and a Monte Carlo approach, respectively. β1 α1 β2 β3 β4 β5 α2 α3 R 2 [s -1 ] NOE R 1 [s -1 ] Residue number
5 Figure S4. Parameters characterizing the overall and internal mobility of MMP3-NNGH adduct within the Lipari-Szabo model. The backbone amide order parameters (S 2 ), the effective correlation time for motions faster than the overall tumbling rate (τ e ), and the conformational exchange contribution to R 2 are shown. The secondary structure elements are reported at the top. β1 α1 β2 β3 β4 β5 α2 α3 8 6 S 2 t e (ps) K ex Residue number
6 Figure. S5. Combined chemical shift differences between: A) MMP3-NNGH and MMP3-MLC88; B) MMP3-NNGH and MMP3-InhVII. The secondary structure elements are reported at the top. 1.0 A β1 α1 β2 β3 β4 β5 α2 α3 0.8 Combined δ (ppm) Residue Number 1.0 B β1 α1 β2 β3 β4 β5 α2 α3 Combined δ (ppm) Residue Number
7 Figure. S6. Representative structures of the adducts of MMP3 with the inhibitors MLC88 (A) and InhVII (B) for the lowest energy clusters obtained from Autodock and Xplor-NIH calculations. The total Xplor-NIH energies calculated considering the energetic contributions deriving from the intra-inhibitor atoms and inter protein-inhibitor interactions together with the standard deviation within the family structures of the cluster are also shown. A Cluster 1 (-87 ± 4 kcal mol - 1 ) Cluster 2 (-83± 3 kcal mol - 1 ) B Cluster 1 (-106 ± 6 kcal mol - 1 ) Cluster 2 (-100± 7 kcal mol - 1 )
8 Supplementary Table S1. NMR experiments performed on MMP3-NNGH at 298 K for spectral assignment and structure determination. Experiments Dimension of acquired data (nucleus) Spectral width (ppm) n a t 1 t 2 t 3 F 1 F 2 F 3 [ 1 H- 1 H]-NOESY b 1024( 1 H) 2048( 1 H) H- 15 N-HSQC c 64( 15 N) 2048( 1 H) H- 13 C-HSQC c CBCA(CO)NH c 128( 13 C) 40( 15 N) 1024( 1 H) CBCANH c 128( 13 C) 40( 15 N) 1024( 1 H) (h)cch-tocsy c 230( 13 C) 64( 13 C) 1024( 1 H) C-NOESY-HSQC b 240( 13 C) 64( 1 H) 2048( 1 H) N-NOESY-HSQC b 180( 1 H) 40( 15 N) 2048( 1 H) HNHA c 256( 1 H) 40( 15 N) 1024( 1 H) N R 1 c 256( 15 N) 1676 ( 1 H) HNCA HNCOCA N R 2 c 256( 15 N) 1676( 1 H) Filtered noesy b 512( 1 H) 4096( 1 H) steady-state heteronuclear 256( 15 N) 1676( 1 H) NOEs c a Number of acquired scans. b These experiments were acquired on a 900 MHz spectrometer with mixing time of 100ms ( 15 N) or 120ms ( 13 C). c Data acquired on 500MHz or 800MHz spectrometers. All the triple resonance cryo-probes (TXI 5-mm) used were equipped with Pulsed Field Gradients along the z-axis. In R 1, R 2 and heteronuclear NOE experiments the water signal was suppressed with the water flip-back scheme. R 2 rates were measured using a refocusing time of 450 µs. All 2D and 3D spectra were then processed using the standard Bruker software (XWINNMR) and analyzed with the Sparky program
9 Supplementary Table S2. 1 H, 15 N and 13 C resonance assignment of MMP3-NNGH at 298 K. The assignment of the side chain resonances was performed through the analysis of the 3D (H)CCH-TOCSY spectrum together with the 15 N- NOESY-HSQC and 13 C- NOESY-HSQC spectra. Proton resonances were calibrated with respect to the signal of 2,2- dimethylsilapentane-5-sulfonic acid (DSS). Nitrogen chemical shifts were referenced indirectly to the 1 H standard using a conversion factor derived from the ratio of NMR frequencies. Carbon resonances were calibrated using the signal of dioxane at 69.3 ppm as secondary reference. N (HN) CA (HA) CB (HB) G88 (4.23, 4.72) I (8.54) (3.79) (1.96) QG QG P (4.08) (1.93, 2.22) CD CG HD HD QG K (7.04) (3.46) (2.16) CD CE CG QD 1.79 QE 3.42 QG 0.85 W (8.215) 53.7 (4.34) (3.20, 3.57) HD HE HZ NE R (7.912) 52.9 (3.878) (1.45) CD CG 30.2 HD HD HG HG2 1.8 K (7.473) (4.224) (2.5) CD CE CG HE HE HG HG QD 1.80 T (7.993) (4.253) (4.148) CG QG H (7.027) (4.693) (2.92, 2.88) L (8.166) (4.991) (1.05) HG 0.69 QD QD T (9.242) (5.548) (4.018) QG Y (8.563) (5.536) (2.67, 1.68) QD QE R (8.158) (4.277) (1.96, 2.09) CD CG HG1 1.5 HG QD 3.22 I (8.32) (4.71) (1.54) CD CG CG QD QG QG V (9.476) (3.292) 30 (1.941) CG CG QG QG N (7.577) (4.685) (2.82, 3.05) HD HD ND Y (8.049) (4.092) (2.91) T105 (8.42) (3.992) (1.947) HG QG P106 (4.507) D (8.827) (4.066) (2.91, 2.61) L (6.929) 48.4 (4.776) (1.47, 1.07) CD CG HG 0.44 QD QD P (4.383) (1.95, 2.34) CD CG K (8.586) (3.795) (1.25, 1.34) CD CE CG 21.6 HD HD HE HE HG HG D (8.457) 53.9 (4.222) (2.69, 2.55) A (7.263) (4.21) (1.47) V (7.472) (3.639) (1.941) CG QG QG D (8.497) (4.073) (2.58, 2.51) S (8.001) ( (3.64,3.44) A (7.637) (3.945) (1.32) V (7.948) 64.3 (3.135) (2.385) CG CG QG QG E (8.337) (3.585) (1.95, 2.07) CG HG HG K (8.235) (3.819) (2.09,1.85) CD CE CG HD HD HE HE HG HG A (8.034) (4.503) (0.75) L (7.64) (1.45, 0.64) CD CG HG QD QD K (7.786) (3.974) (2.02, 1.90) CD CE CG HG HG QD 1.63 QE 2.78 V (7.35) (3.46) (1.362) CG CG QG1 0.64QG W (6.582) (4.848) (3.09, 2.92) HD HE HZ NE E (8.43) (4.728) (1.99) QG E (7.742) (4.095) (2.04, 2.27) QG 2.55 V (7.02) (4.803) (2.58) QG QG2 0.8 T (7.3) (5.422) (4.203) CG QG P129 (5.336) (2.06) L (7.259) (4.395) (1.59, 1.50) CD CD CG HG 1.27 QD QD
10 T (8.008) (4.432) (4.027) CG QG F (8.215) (5.643) (2.75, 2.73) QD QE S (8.67) (4.744) (3.80, 3.58) R (8.546) (4.601) ( ) HE 6.11 QD 2.74 L (8.455) 50.2 (4.585) 42.7 (1.15, 1.50) CD CD CG HG QD QD Y (9.205) (4.331) (2.93, 3.15) HD HE E (7.491) (4.684) 30.1 (1.99, 1.82) CG HG HG G (8.504) (3.95, 3.66) E (8.168) (4.195) (2.02) CG 33.4 HG HG A (7.986) (4.366) (1.1) D (8.273) (4.436) I (8.436) (4.375) (1.787) CD CG CG QD QG M (7.234) (4.218) (1.97, 1.85) QE I (9.171) (5.3) (1.762) CD CG CG HG HG QD QG S (8.516) (4.963) (3.17, 3.67) F (9.43) (5.231) (2.65, 2.74) A (9.266) (4.768) (0.98) V (8.166) (4.731) (2.124) QG QG R (9.616) (4.705) (2.25, 2.10) HG HG QD E (7.552) (4.066) 27.8 (2.01, 1.94) CG 34 HG HG H (9.291) 60.4 (4.205) (2.95) HD G (8.071) (3.88) D (6.822) (4.694) (2.71, 2.91) F (7.814) (4.056) QD 6.43 Y (6.776) (4.456) QE 7.06 P156 (3.92) (2.75) F (8.505) (3.99) (2.998) QD QE D (7.869) 50.8 (4.027) (2.67) G (8.857) (3.33, 4.33) P160 (3.946) G (11.33) 40.6 (3.86) N (8.798) (3.841) (3.16, 2.56) HD HD ND V (9.962) (3.51) (2.206) CG1 18 CG QG QG L (8.447) (4.575) (1.27) HG 1.75 QD QD A (7.438) (3.14) (1.68) H (9.072) (4.457) (2.92) HD A (8.013) (4.568) (2.09) Y (7.979) (4.391) (2.77, 2.62) QD 6.68 QE A (7.442) (4.7) (-0.268) P (4.138) (1.85) CD CG QD QG G (6.209) (4.67, 3.11) P (4.716) (1.94) CD CG HD HD QG 1.77 G (8.756) (3.76) I (8.904) (4.031) (1.731) CD CG CG HG HG QD QG N (14.09) (4.392) (2.27, 2.065) HD HD ND G (8.098) (4.66) D (7.76) (4.41) (2.59, 2.45) A (8.21) (4.938) (1.15) H (9.191) (4.857) F (8.818) (4.749) (3.06) HD HE2 6.81QD 6.43 QE D (8.115) (4.233) (2.71, 2.75) D (9.797) (5.399) (2.37, 2.62) D (9.226) (4.73) ( )
11 E (7.203) (4.831) (2.35) Q (8.38) (4.378) ( ) HE HE NE W (9.587) (4.924) (3.14) HD HE NE1 126 T (8.738) (4.754) (4.387) CG QG K (9.053) 54.1 (4.389) (1.84, 1.72) CD CE CG HD HD HE HE HG HG D (7.39) (4.742) (2.68, 3.30) T (7.77) (4.592) (3.936) CG QG T (8.176) (4.041) (4.058) CG HG G (7.266) ( ) T (8.534) 59.8 (3.54) (2.645) CG QG N (8.221) (4.704) (2.78) HD HD ND L (7.944) (4.404) 39.2 (2.62, 2.63) HG QD QD F (8.332) (3.93) (3.12, 3.28) QD 7.11 QE 6.54 L (8.616) (2.985) (1.60, 2.56) HG QD QD V (7.174) (3.884) (2.206) CG CG QG QG A (9.472) (3.97) (1.07) A (8.816) (3.872) (0.95) H (7.663) (4.167) (3.87) E (9.195) 56.3 (3.805) (1.69, 0.96) CG QG 2.33 I (9.016) (3.801) (1.868) CD CG CG QD QG QG G (7.474) ( ) H (7.178) (4.389) (2.77, 4.21) S (8.209) (4.647) 60.4 (3.91, 3.80) L (8.19) (3.791) (1.75) CD CD CG QD HG QD G (8.394) (5.736) L (8.804) (5.26) (1.56) HG QD QD F (8.505) (4.829) H (5.297) (3.44) S (6.821) (4.677) 64.7 (4.04, 3.07) A (8.793) (4.255) (1.64) N (8.821) (4.529) (3.15) HD T (8.029) (2.368) (3.725) CG QG E (8.581) (4.451) (2.1) A (7.833) 49.5 (4.179) (1.4) L (11.49) (4.411) (1.61, 1.35) CD CG HG QD QD M (8.016) (4.577) (2.6) QE Y (8.066) (4.853) (2.88) QD QE P (3.553) (0.78, 1.70) CG QG L (7.501) (4.443) (1.33, 1.67) CD CD CG HG QD QD Y (9.054) (4.592) 34.3 (2.21, 2.71) H (8.157) 55 (4.28) (2.87) HD S (7.832) (3.911) (3.99, 3.74) L (7.816) (4.329) (1.57, 1.42) QQD T (7.908) 58.8 (4.277) 67.1 (4.101) QG D (7.968) (4.63) (2.57, 2.48) L (8.896) (4.037) (1.49, 1.66) CD CD CG HG QD QD T (8.361) (4.065) (4.167) CG QG R (7.34) (4.672) (1.92, 1.504) CD CG HG HG QD F (7.271) (4.122) (2.79, 3.059) HE R (7.067) (3.843) (1.37, 1.58) CD CG HD HD QG L (8.331) (4.413) 40.5 CD CD CG QD QD S (8.664) (3.742) (4.71, 3.91)
12 Q (9.095) (4.412) 25.6 (2.07, 1.95) CG QG 2.34 D (8.062) (4.279) (2.55) D (8.035) (3.898) 36.5 (2.97) I (7.968) (3.592) (1.684) CD CG CG QD QG QG N (9.111) (4.361) (2.85, 2.77) HD HD ND G (8.193) (3.782) I (8.532) 60.5 (4.272) (2.09) CD CG CG QD QG QG Q (8.279) (4.655) HE HE QG S (8.029) (4.528) L (6.737) (4.093) (1.62, 1.47) CD CD CG 24.4 HG QD QD Y (7.58) (2.845) (3.15, 3.45) QD QE G (8.313) ( ) P248 QG NNGH QB HG HNA HP QM HP QP QQD
13 Supplementary Table S3. Statistical analysis of the energy minimized structures of MMP3- NNGH. MMP3-NNGH a <MMP3-NNGH> Total number of meaningful NOE upper distance 2060 constraints Intra-protein NOEs b : Intra-residue 194 Inter-residue Sequential ( i-j = 1) 584 Medium-range ( i-j < 4) 652 Long-range ( i-j > 5) 630 Total meaningful dihedral angle restraints 164 Phi 100 Psi 64 Inhibitor c -protein NOEs 17 Intra-inhibitor NOEs d 1 Hydrogen bond derived restraints 52 Intra-protein 51 Protein-inhibitor e 1 RMS violations per meaningful distance constraint (Å): Intraresidue 0.009± Sequential 0.017± Medium range 0.019± Long range 0.023± RMS violations per meaningful dihedral angle constraints ( ): Phi ± Psi ± Average number of violations per conformer: Phi ± Psi ± NOE violations between 0.1 Å and 0.3 Å 25.1 ± NOE violations larger than 0.3 Å Average RMSD to the mean (Å) Secondary structure elements (backbone atoms) 0.49 ± 0.06 Secondary structure elements (all heavy atoms) 1.12 ± 0.10 Loop regions (backbone atoms) 0.81 ± 0.10 Loop regions (all heavy atoms) 1.45 ± 0.10 NNGH atoms 1.16 ± 0.29 Target Function (Å 2 ) 1.21 ± 0.14 Structural analysis f % of residues in most favourable regions % of residues in allowed regions % of residues in generously allowed regions % of residues in disallowed regions Completeness of NOE s within 4 Å g 60% 58% Completeness of NOE s within 5 Å 41% 42% H-bond energy (kcal mol -1 ) 0.7± 0.11 WHAT IF structure Z-scores h 1st generation packing quality -2.6 ± Ramachandran plot appearance -3.0 ± χ1/χ2 rotamer normality -3.2 ±
14 Backbone conformation -2.4 ± a Structure calculations were performed with the program CYANA 2.1. A total of 400 random conformers were subjected to steps of a simulated annealing process. The 30 conformers with the lowest target function were refined through restraint energy minimization (REM) with the Amber 8.0 package. Values of 32 kcal mol -1 Ã -2 and 50 kcal mol -1 rad -2 were used as force constants for the NOE and torsion angle restraints, respectively. The data are calculated over the 30 conformers representing the NMR structure and on the energy minimized mean structure. The mean value and the standard deviation are also given b Number of meaningful constraints for each class. c These NOEs are given in Table 2 of the manuscript. The CYANA library corresponding to NNGH was obtained using the program Molmol. d Stereospecific assigned NOE between the protons HNA and HP2 of the NNGH inhibitor. e Hydrogen bond between Leu164 NH and the sulfonyl oxygen O2 of NNGH. f As it results from the Ramachandran plot analysis performed with PROCHECK. g Calculated considering amide and alpha protons g The Z-scores is reported considering the secondary structure elements h A Z-score is defined as the deviation from the average value for this indicator observed in a database of high-resolution crystal structures, expressed in units of the standard deviation of this database-derived average. Typically, Z-scores below a value of -3 are considered poor, those below - 4 are considered bad.
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