Measurement of Three-Bond 13C−13C J Couplings between Carbonyl and Carbonyl/Carboxyl Carbons in Isotopically Enriched Proteins

Three-bond13C-13C J couplings have long been recognized as a valuable source of structural information in the study of organic, organometallic, and biological compounds. 1-3 For13Cenriched proteins, two different approaches have been proposed for measurement of these couplings: ECOSY 4 and quantitative J correlation. 5,6 Both approaches benefit from the exceptionally narrow line widths of methyl 13C resonances, and in proteins these measurements therefore have largely been restricted to JCC couplings involvingCH3. Here we demonstrate that the quantitative J correlation approach can also be used for measurement ofJCC couplings between carbonyl (C ′) and carbonyl/carboxyl carbons. JC′C′ provides direct information on theφ backbone angle, and JC′Cγ in Asn and Asp residues relates toø1. Previously, a Karplus curve appropriate for peptides has been proposed on the basis of FPT-INDO calculations. 1 Here we present the first empirical Karplus relation for this coupling based onJC′C′ couplings measured in ubiquitin (76 residues) and φ angles from its X-ray structure. Application to apocalmodulin (apo-CaM, 148 residues) confirms the backbone geometry of the first Ca 2+-binding site7 and adds new information on the orientations of its three Asp side chains which ligate Ca2+ in the bound state. The experiment (Figure 1) for measuring JC′C′ starts with transfer of magnetization from the amide proton (H N) through the 15N to the preceding13C′ and is followed by a13C′-13C′ dephasing period prior to magnetization transfer to its longrange coupled13C′ which subsequently evolves during t2 and is finally transferred back along the reverse pathway for 1HN detection. The pulse scheme is very similar to that of the longrange carbon -carbon correlation experiment 5,8 and details regarding the magnetization transfer in this class of experiments have been discussed elsewhere. 8-10 In the present case, after magnetization has been transferred from 15N to its adjacent 13C′ (referred to as source-C ′, or sC′), it dephases during the time 2ú with respect to carbonylsJ coupled to sC′. Exactly analogous to the homonuclear HAHB experiment, 10 a fraction sin(2πJsC′dC′ú) Πk cos(2πJsC′kC′ú) of the source-C′ magnetization is transferred to the destination C ′, dC′, where the product extends over all C′ nuclei, other than dC ′, that areJ coupled to sC′. A fraction cos(2πJsC′dC′ú) Πk cos(2πJsC′dC′ú) remains as in-phase sC′ magnetization at the start of t2. The same fractions apply to the reverse transfer of C ′ magnetization between the end oft2 and the end of the second 2 ú period, and the diagonalto-cross-peak ratio therefore equals -tan(2πJsC′dC′ú). As ú is known, JsC′dC′ follows directly from the intensity ratio. Strictly speaking, this ratio applies to the volume integrals of the sC’ and dC’ resonances, but as the line widths of the two resonances in the 3D spectrum are identical in the 15N (t1) and 1HN (t3) dimensions, and the same to within the digital resolution in the C′ (t2) dimension, peak heights are used instead for deriving JsC′dC′. Experiments were carried out for samples containing 3.5 mg of 13C/15N-enriched ubiquitin (pH 4.7; 30°C) in a 220μL Shigemi microcell (1.8 mM) at 600 MHz and 10 mg of apoCaM (pH 6.3; 23°C) in 450 μL (1.3 mM) at 500 MHz. Experiments on ubiquitin were carried out twice, once with 4 scans (Figure 2A) and once with 16 scans per FID (12 h and 2 d measuring time, respectively). Each strip shows the negative9,10 “diagonal” peak, corresponding to the 13C′ of the preceding residue, and positive cross peaks to its long-range coupled13C. For most backbone carbonyls, the value of JC′C′ coupling was measured twice, once with sC ′ ) C′i-1 and dC′ ) C′i, and once vice versa. The pairwise root-mean-square (rms) difference between these measurements was smaller than 0.1 Hz, and the rms pairwise difference between measured J values in the 4-scan and 16-scan experiments was also less than 0.1 Hz (supporting information). Figure 3 shows the averages of these two measurements as a function of the intervening φ angles, taken from the ubiquitin X-ray structure. 11 The data were fit to a Karplus curve, yielding