The GlcN6P cofactor plays multiple catalytic roles in the glms ribozyme
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1 SUPPLEMENTARY INFORMATION The GlcN6P cofctor plys multiple ctlytic roles in the glms ribozyme Jmie L. Bingmn 1, Sixue Zhng 2, Dvid R. Stevens 2, Neel H. Yennwr 3, Shron Hmmes-Schiffer 2,* Philip C. Bevilcqu 1,4,* 1 Deprtment of Chemistry nd Center for RNA Moleculr Biology, Pennsylvni Stte University, 104 Chemistry Building, University Prk, Pennsylvni 16802, USA 2 Deprtment of Chemistry, University of Illinois t Urbn-Chmpign, 600 South Mthews Avenue, Urbn, Illinois 61801, USA 3 X-ry Crystllogrphy Fcility, Huck Institutes of the Life Sciences, Pennsylvni Stte University, 8 Althouse Lbortory, University Prk, Pennsylvni 16802, USA 4 Deprtment of Biochemistry nd Moleculr Biology, Pennsylvni Stte University, University Prk, Pennsylvni 16802, USA *Emil: shs3@illinois.edu; pcb5@psu.edu S1
2 Supplementry Results Supplementry Tble 1. SAXS-determined R g, moleculr weight (MW), D mx, RMSD, nd verge excluded volume vlues for vrious po nd holoribozyme constructs Conditions Aporibozyme oxo substrte Aporibozyme deoxy substrte R g (Guinier) R g (GNOM) MW (Guinier) (kd) D mx RMSD b Excluded volume (Å 3 ) ± , ± ,000 Holoribozyme deoxy substrte ± ,000 The vlues of Rg, MW, nd Dmx were clculted for the Coot-corrected crystl structure (PDB ID 2NZ4) to be 30.3 Å, 47.7 kd, nd 120 Å. b Generted by SUPCOMB using the DAMFILT models nd Coot-corrected crystl structure (PDB ID 2NZ4). S2
3 Supplementry Tble 2. Thio effects nd metl ion rescue for the glms holoribozyme in 10 mm Mg 2+. Ionic conditions Substrte k obs (min -1 ) b Amplitude (%) c k O/k d S Metl ion rescue e 10 mm Mg 2+ oxo 80 ± ± oxo 50 ± 3 82 ± R P 0.40 ± ± ± 50 - R P 0.33 ± ± ± 20 - S P 5 ± 1 53 ± 4 15 ± 5 - dithio ± ± ± mm Mg 2+ oxo 60 ± ± with 0.01 µm Cd 2+ oxo 48 ± ± R P 0.33 ± ± ± ± 0.1 S P 7.6 ± ± 2 8 ± ± 0.7 dithio ± ± ± ± mm Mg 2+ with 0.1 µm Cd mm Mg 2+ with 1 µm Cd mm Mg 2+ with 10 µm Cd 2+ oxo 70 ± ± oxo 49 ± 2 83 ± R P 0.36 ± ± ± ± 0.3 S P 8 ± 1 49 ± 2 8 ± ± 0.8 dithio ± ± ± ± 0.5 oxo 59 ± 2 87 ± oxo 47 ± 4 79 ± R P 0.34 ± ± ± ± 0.2 S P 3 ± 1 54 ± 3 17 ± ± 0.4 dithio ± ± ± ± 0.3 oxo 56 ± 3 90 ± oxo 50 ± 4 80 ± R P 0.30 ± ± ± ± 0.2 S P 4.0 ± ± 2 14 ± ± 0.4 dithio ± ± ± ± 0.5 S3
4 10 mm Mg 2+ with 100 µm Cd mm Mg 2+ with 1 mm Cd mm Mg 2+ with 2 mm Cd 2+ oxo 52 ± 8 90 ± oxo 38.8 ± ± R P 0.20 ± ± ± ± 0.1 S P 3.5 ± ± 5 15 ± ± 0.4 oxo 40 ± ± oxo 33 ± 6 72 ± R P 0.13 ± ± ± ± 0.1 S P 2.3 ± ± ± ± 0.4 oxo 33 ± 4 84 ± oxo 27.9 ± ± R P 0.16 ± ± ± ± 0.4 S P 1.8 ± ± ± ± M K + oxo (1.71 ± 0.06) x ± R P (5 ± 1) x ± ± 90 - S P (6.3 ± 0.3) x ± ± 20 - dithio (4.1 ± 0.4) x ± ± 40 - Renturtion consisting of heting t 95 o C for 3 min nd snp cooling on ice for 10 min. The dditionl step of heting t 55 o C for 3 min nd cooling t room temperture for 10 min ws omitted to void extensive clevge of the RP thio substrte before initition with GlcN6P. b kobs is mesured with the specified concentrtion of Cd 2+ in bckground of 10 mm Mg 2+. Error represents stndrd devition of three or more mesurements. c Amplitude is mesured s the size of the phse of clevge rther thn the finl percent cleved. d The thio effect is clculted s the rtio of ko/ks for the corresponding condition s described in eqution (3). e Metl ion rescue is clculted s described in eqution (4). S4
5 Supplementry Tble 3. RMSD between different glms crystl structures. Structures Active site RMSD Whole ribozyme RMSD b c 2NZ4 d nd 3G8S e NZ4 d nd 2Z75 f 0.51 N/A 3G8S e nd 2GCS g 0.63 N/A Experiments were conducted on the glms ribozyme from Bcillus nthrcis while clcultions were on the glms ribozyme from Thermonerobcter tengcongensis. The structures re virtully identicl t the ctive site s supported by the tble bove. Nucleotide numbering used in the text is from B. nthrcis. b The ctive site for the po glms includes A 1, G1, nd the puttive bse gunine residue G33/G40. The ctive site for the holo glms includes the bove three residues plus the cofctor. The highly flexible unpired A 1 nucleotide bse is excluded in the ctive site RMSD clcultions. c The glms ribozymes from different species hve different sequences except for some conservtive regions nd thus re not compred. d The holoribozyme glms from Bcillus nthrcis 1 used in the experiments for the present pper. e The poribozyme glms from Bcillus nthrcis 2 used in the experiments for the present pper. f The holoribozyme glms from Thermonerobcter tengcongensis 3 used in the clcultions for the present pper. g The poribozyme glms from Thermonerobcter tengcongensis 4 used in the clcultions for the present pper. S5
6 Supplementry Tble 4. Distnces nd ngles from QM/MM geometry optimiztions for glms holoribozyme. Substrte A 1 (O2 ):RP A 1(O2 ) H RP ( o ) GlcN6P(O1) :RP GlcN6P(O1) H RP ( o ) G32(N1): SP G32(N1) H SP ( o ) G32(N2): SP G32(N2) H SP ( o ) G57(N1): RP H-RP ( o ) G57(N2): RP G57(N1)- G57(N2)- H-RP ( o ) oxo RP SP oxo b RP b SP b oxo c RP c SP c Initil structure hs hydrogen bond between G57(N2) nd RP nd between GlcN6P(O1) nd RP. b Initil structure hs hydrogen bond between A 1(O2 ) nd RP nd between GlcN6P(O1) nd RP. c Initil structure hs hydrogen bond between G57(N1) nd RP nd between G57(N2) nd RP. S6
7 Supplementry Tble 5. Thio effects nd metl ion rescue for the glms poribozyme in 10 mm Mg 2+. Ionic conditions Substrte k obs (min -1 ) Amplitude (%) b k O/k S c k S/k O d Metl ion rescue e,f 10 mm Mg 2+ oxo (9 ± 3) x ± R P (2.7 ± 0.1) x ± 1 (3 ± 1) x ± 9 - f S P (8 ± 1) x ± 0.5 (1.2 ± 0.4) x ± 3 - dithio f (1.3 ± 0.1) x ± 1 (7 ± 2) x ± 5-10 mm Mg 2+ with 0.01 µm Cd 2+ oxo (4.6 ± 0.8) x ± R P (2.6 ± 0.1) x ± 2 (1.8 ± 0.3) x ± ± 0.7 dithio (2 ± 1) x ± 1 (2 ± 1) x ± 30 3 ± 2 10 mm Mg 2+ with 0.1 µm Cd 2+ oxo (5.2 ± 0.7) x ± R P (2.7 ± 0.3) x ± 2 (1.9 ± 0.3) x ± ± 0.6 dithio (4 ± 2) x ± 1 (1.4 ± 0.8) x ± 40 5 ± 3 10 mm Mg 2+ with 1 µm Cd 2+ oxo (4.8 ± 0.1) x ± R P (2.8 ± 0.4) x ± 4 (1.8 ± 0.3) x ± ± 0.7 dithio (3 ± 1) x ± 2 (2 ± 1) x ± 30 4 ± 2 10 mm Mg 2+ with 10 µm Cd 2+ oxo (4.4 ± 0.5) x ± R P (3.9 ± 0.3) x ± 3 (1.1 ± 0.2) x ± 10 3 ± 1 dithio (3.0 ± 0.6) x ± 0.9 (1.5 ± 0.4) x ± 20 5 ± 2 10 mm Mg 2+ with 100 µm Cd 2+ oxo (9 ± 9) x ± R P (1.35 ± 0.08) x ± 1 (6 ± 6) x ± ± 6 dithio (1 ± 2) x ± 8 (6 ± 9) x ± 30 1 ± 2 10 mm Mg 2+ with 1 mm Cd 2+ oxo (8.5 ± 0.5) x ± R P (6.7 ± 0.9) x ± 2 (1.3 ± 0.2) x ± ± 9 dithio (1.2 ± 0.6) x ± 4 (7 ± 3) x ± ± 6 10 mm Mg 2+ with 2 mm Cd 2+ oxo (1.2 ± 0.1) x ± R P (1.0 ± 0.1) x ± 5 (1.2 ± 0.2) x ± ± 10 dithio (2.0 ± 0.6) x ± 1 (6 ± 2) x ± ± 6 S7
8 1 mm Mg 2+ oxo (2.9 ± 0.2) x ± R P (1.4 ± 0.4) x ± 2 (2.0 ± 0.6) x ± 10-5 mm Mg 2+ oxo (7.0 ± 0.2) x ± R P (2.1 ± 0.3) x ± 2 (3.4 ± 0.5) x ± 4-50 mm Mg 2+ oxo (1.68 ± 0.06) x ± R P (2.8 ± 0.3) x ± 0.7 (5.9 ± 0.6) x ± 2 - Renturtion consists of heting t 95 o C for 3 min nd snp cooling on ice for 10 min. kobs is mesured with the specified concentrtion of Cd 2+ in bckground of 10 mm Mg 2+. Error represents stndrd devition of three or more mesurements. b Amplitude is mesured s the size of the phse of clevge rther thn the finl percent cleved. c The thio effect is clculted s the rtio of ko/ks for the corresponding condition (eqution (3)). d The inverse thio effect is clculted s the rtio of ks/ko. e Metl ion rescue is clculted s described. f In the bsence of Cd 2+, extents of rection for the SP nd dithio substrtes were similr to the oxo substrte, which led to uncertinty in the rtes. The metl ion rescue for the dithio substrte should be tken s lower limit. S8
9 Supplementry Tble 6. Distnces nd ngles from QM/MM geometry optimiztions for glms poribozyme. Conformtion Mg 2+ :R P Mg 2+ :S P A 1(O2 ):R P A 1(O2 ) H R P ( ) Mg 2+ closer to pro-r P (see Fig. 5) oxo R P S P Mg 2+ closer to pro-s P (see Supplementry Fig. 7) oxo R P b 160 S P When the Mg 2+ is closer to the pro-rp position, the RP thio substitution breks the wek A 1(O2 ):RP hydrogen bond, s indicted by the hydrogen-bonding ngle. b When the Mg 2+ is closer to the pro-sp position, the RP thio substitution wekens the A 1(O2 ):RP hydrogen bond, s indicted by the lrger hydrogen-bonding distnce. S9
10 b c Supplementry Figure 1: Optimiztion of RNA purifiction nd renturtion gives wellbehved ribozyme system. () 8% ntive nd denturing PAGE of vrious rentured enzyme species: ntive gel-purified monomer (lne 1; NM) nd dimer (lne 3; ND), nd denturing gel-purified enzyme (lne 4; DM). The second lne in both gels is smple where NM nd ND species were mixed (lne 2; NM+ND). The ntive gel suggests tht DM, in ddition to being homogenous, is the most compct of ll enzyme species. Purifiction of the enzyme strnd by denturing gel electrophoresis ws thus dopted s the stndrd purifiction technique. The ntive gel running buffer consists of 1X THE nd 10 mm MgCl 2. Bnds were visulized with SYBR Gold stining. The denturing gel confirms tht ll enzyme species re the sme length. (b) Denturing PAGE (18% crylmide) of time points from rection with 0.25 nm oxo substrte nd 100 nm denturing gel-purified enzyme t 37 o C nd ph 7 with 10 mm MgCl 2 nd 10 mm GlcN6P performed by rpid-mixing. The RNA ws rentured ccording to the stndrd renturtion protocol described in the min text. (c) Plot of frction of substrte cleved versus time for the gel shown in Pnel b. Experiments were performed in triplicte nd gve n verge rte constnt of 80 ± 20 min -1 (t 1/2 ~ 0.5 s) nd n mplitude of 90 ± 4%. Thus, the rection kinetics of clevge re fst, monophsic, nd complete, consistent with single, well-folded ribozyme species. S10
11 b c d Supplementry Figure 2: Enzyme, GlcN6P cofctor, nd MgCl 2 sturtion ssys demonstrte tht stndrd rection conditions re under sturting conditions. () Kinetic ssys show tht incresing the concentrtion of enzyme five-fold does not ffect the observed rte constnt under stndrd rection conditions, provided t the bottom of this cption. Dt shown re from one tril t ech concentrtion of enzyme. (b) Gel shift ssys show tht 100 nm enzyme, indicted with n rrow, is sturting. Fitting where the Hill coefficient ws kept t 1 gve K d of 1.5 ± 0.2 nm. The 200 nm enzyme dt point ws omitted from the fit. Though the ssy ws performed in duplicte, dt shown re from one tril t ech concentrtion of enzyme. (c) Kinetic ssys show tht incresing the concentrtion of GlcN6P cofctor two-fold does not ffect the observed rte constnt under stndrd rection conditions. Dt shown re the verge of t lest three independent trils, where stndrd devition is indicted with error brs. (d) Kinetic ssys demonstrte tht incresing the concentrtion of MgCl 2 two-fold does not significntly ffect the observed rte constnt under stndrd rection conditions. Stndrd rection conditions re ~0.25 nm substrte, 100 nm enzyme, 50 mm HEPES (ph 7.0), 50 mm N +, nd 10 mm Mg 2+. Dt shown re the verge of t lest three independent trils, where stndrd devition is indicted with error brs. S11
12 90 rottion b 90 rottion S12
13 c 90 rottion Supplementry Figure 3: Smll-ngle X-ry scttering (SAXS) nlysis of construct used for kinetics experiments supports well-folded, monomeric species. Experimentl scttering dt (red points) overlid with clculted scttering dt for the Coot-corrected crystl structure (blck curve; I(q) vs. q), dimensionless Krtky plots (I(q)q 2 vs. q), p(r) plots, SEC trces (blck) overlid with moleculr weight (blue), SEC trces (blck) overlid with R g (blue), nd DAMMIF reconstructions (ten independent runs verged together) overlid with the modified 2NZ4 crystl structure for the () oxo poribozyme, (b) deoxy poribozyme, nd (c) deoxy holoribozyme. These dt suggest the experimentl construct is well folded nd monomeric, with t most smll percentge exhibiting dimeric or ggregte chrcteristics. The finl item in pnel is the sme s pnel c of Fig. 1 in the min text. Dt presented come from one SAXS experiment for ech ribozyme. S13
14 b c d Supplementry Figure 4: Mss spectrometry performed on R P, S P, oxo, nd dithio substrtes confirms identity of the vrious substrtes. Actul (nd expected) msses for ech substrte re () R P substrte: mu ( mu), (b) S P substrte: mu ( mu), (c) oxo substrte: mu ( mu), nd (d) dithio substrte: mu ( mu). Ech substrte ws run once on the mss spectrometer. S14
15 Supplementry Figure 5. Degrdtion control with the S P thio substrte in the poribozyme in 10 mm Mg 2+ nd 2 mm Cd 2+. Plot of frction of S P thio substrte cleved versus time for the fully-folded ribozyme with both substrte nd enzyme (blck), the substrte nd its complementry strnd (blue), nd the substrte only (red). All experiments were preceded by the typicl poribozyme renturtion. This experiment reveled tht the S P thio substrte shows higher bckground rection rte constnt (both with nd without complementry RNA strnd) thn ribozyme rection rte for the poribozyme under conditions of 10 mm Mg 2+ nd 2 mm Cd 2+. Thus, metl ion rescue in the poribozyme for the S P substrte could not be ssessed. S15
16 Supplementry Figure 6. Clssicl free energy simultions support metl ion interctions. () Definition of rection coordintes. (b) 2D free energy projection. Blck line indictes the minimum free energy pth (MFEP). Color br indictes free energy vlue nd hs unit of kcl/mol. (c) Free energy profile long the MFEP. Following the procedure given in Ref. 5, sttisticl nlysis ws performed to estimte the sttisticl error to be pproximtely 1 kcl/mol. However, this error nlysis does not ccount for systemtic error due to limittions in the level of theory or the dependence on the initil string. The initil string ws generted by liner interpoltion between two optimized geometries corresponding to the Mg 2+ ion t either the pro-r P or the pro-s P site, thereby voiding bis towrd either site, lthough limited smpling prevents explortion of the full conformtionl spce. Thermodynmiclly stble configurtions were found t both the pro-r P nd the pro-s P sites, s well s n intermedite region. According to the minimum free energy pth in prt b, the free energy of the minimum corresponding to Mg 2+ closer to pro-r P (~1.8 Å from pro-r P nd ~3.8 Å from pro-s P) is ~14 kcl/mol lower in free energy thn the minimum corresponding to Mg 2+ closer to pro S P (~3.5 Å from pro-r P nd ~1.8 Å from pro-s P). A shllow minimum is found with the Mg 2+ midwy between the pro R P nd pro S P oxygen toms, which is even higher in free energy thn either of the two other positions. During these free energy simultions, when the Mg 2+ ion is coordinted to pro R P, the A-1(O2 ):pro R P hydrogen bond is disrupted, wheres it is formed consistently when the Mg 2+ ion is coordinted to pro S P. S16
17 Supplementry Figure 7. Active site structures from QM/MM optimiztions for glms poribozyme with Mg 2+ closer to the S P position. The Mg 2+ ion is represented by the cyn sphere nd is closer to the S P position in these conformtions. Only key residues re shown. Sulfur substitution is indicted by yellow, nd hydrogen bonds re indicted by blck dshed lines. The optimized geometries re for the () oxo substrte, (b) R P thio substrte, nd (c) S P thio substrte. Note tht the R P thio substitution hs lengthened nd thus wekened A 1(O2 ):R P hydrogen bond (denoted with grey dshed line in pnel b), wheres the S P thio substitution hs not significntly ltered this hydrogen bond (pnel c). The A 1(O2 ):R P distnces re lbeled in the figure. See Supplementry Tble 6 for dditionl distnces nd ngles ssocited with these three conformtions. For the oxo substrte, the A 1(O2 ):pro-r P hydrogen bond is quite stble, with distnce of 2.68 Å between the two oxygen toms nd hydrogen bond ngle of 161 (pnel ). In clssicl MD simultions of the oxo substrte, the A 1(O2 ):pro R P hydrogen bond ws observed consistently, with n verge A 1(O2 ):pro R P distnce of 2.65 Å nd n verge hydrogen bond ngle of Thio substitution t the pro-r P tom in the Mg 2+ :pro-s P bckground wekens but does not brek this hydrogen bond, s indicted by hydrogen bond distnce of 3.41 Å nd n ngle of 160 (pnel b), while thio substitution t the pro-s P tom does not significntly impct this hydrogen bond (pnel c). S17
18 References 1. Cochrne, J.C., Lipchock, S.V. & Strobel, S.A. Structurl investigtion of the glms ribozyme bound to its ctlytic cofctor. Chem. Biol. 14, (2007). 2. Cochrne, J.C., Lipchock, S.V., Smith, K.D. & Strobel, S.A. Structurl nd chemicl bsis for glucosmine 6-phosphte binding nd ctivtion of the glms ribozyme. Biochemistry 48, (2009). 3. Klein, D.J., Wilkinson, S.R., Been, M.D. & Ferré-D'Amré, A.R. Requirement of helix P2.2 nd nucleotide G1 for positioning the clevge site nd cofctor of the glms ribozyme. J. Mol. Biol. 373, (2007). 4. Klein, D.J. & Ferré-D'Amré, A.R. Structurl bsis of glms ribozyme ctivtion by glucosmine-6-phosphte. Science 313, (2006). 5. Zhng, S. et l. Role of the ctive site gunine in the glms ribozyme self-clevge mechnism: quntum mechnicl/moleculr mechnicl free energy simultions. J. Am. Chem. Soc. 137, (2015). S18
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