Structural and enzymatic analysis of MshA from Corynebacterium glutamicum: substrate-assisted catalysis - PubMed (original) (raw)
Structural and enzymatic analysis of MshA from Corynebacterium glutamicum: substrate-assisted catalysis
Matthew W Vetting et al. J Biol Chem. 2008.
Abstract
The glycosyltransferase termed MshA catalyzes the transfer of N-acetylglucosamine from UDP-N-acetylglucosamine to 1-L-myo-inositol-1-phosphate in the first committed step of mycothiol biosynthesis. The structure of MshA from Corynebacterium glutamicum was determined both in the absence of substrates and in a complex with UDP and 1-L-myo-inositol-1-phosphate. MshA belongs to the GT-B structural family whose members have a two-domain structure with both domains exhibiting a Rossman-type fold. Binding of the donor sugar to the C-terminal domain produces a 97 degrees rotational reorientation of the N-terminal domain relative to the C-terminal domain, clamping down on UDP and generating the binding site for 1-L-myo-inositol-1-phosphate. The structure highlights the residues important in binding of UDP-N-acetylglucosamine and 1-L-myo-inositol-1-phosphate. Molecular models of the ternary complex suggest a mechanism in which the beta-phosphate of the substrate, UDP-N-acetylglucosamine, promotes the nucleophilic attack of the 3-hydroxyl group of 1-L-myo-inositol-1-phosphate while at the same time promoting the cleavage of the sugar nucleotide bond.
Figures
FIGURE 1.
Steps in the biosynthesis of mycothiol.
FIGURE 2.
Structure of APO CgMshA. A, ribbon diagram of an APO-CgMshA monomer (open conformation). Helices are in blue, strands are in_orange_, and coils are in gray. B, molecular dimer of CgMshA.C, illustration of the secondary structure involved in formation of the molecular dimer. In B and C, the 2-fold-related monomer is colored gray with secondary structure labeled with prime (′) designations (i.e. α1′ and β12′).
FIGURE 3.
Structure of the CgMshA UDP·1-l-Ins-1-P complex. A, final 2_Fo_ - Fc density for UDP and 1-
l
-Ins-1-P contoured at 1.0σ. B, ribbon diagram of a CgMshA monomer in complex with UDP and 1-
l
-Ins-1-P (closed conformation). UDP and 1-
l
-Ins-1-P are shown as sticks colored by atom type. C, molecular dimer of CgMshA after domain reorientation. Electron density for 1-
l
-Ins-1-P was sufficient only to fit in one subunit but was modeled in the dimer shown here for illustrative purposes. D, stereo illustration of DYNDOM rotation axis, relating the N- and C-terminal domain before and after binding of nucleoside. The APO structure is illustrated by the green trace, whereas the N- and C-terminal domains of the ternary complex are colored_blue_ and cyan, respectively. α12 is colored_maroon_ in both structures to help in orientation, whereas the hinge residues (196–197 and 386–392) are colored red.
FIGURE 4.
Interactions in the ternary complex. Illustrations of the interaction of CgMshA with the UDP-GlcNAc model and 1-
l
-Ins-1-P are shown. A, Chemdraw diagram. Interactions shown with UDP (maroon) and 1-
l
-Ins-1-P (blue) are those observed in the ternary complex, whereas those with GlcNAc (red) are those found in the molecular model. B, stereo stick diagram.1-
l
-Ins-1-P carbons are colored yellow, and UDP-GlcNAc carbons are colored green. Important hydrogen bonding interactions are shown as gray dotted lines, and the interaction of the 3-OH of 1-
l
-Ins-1-P with the UDP-GlcNAc at the site of reaction chemistry is shown as a cyan dotted line. C, proposed SNi-substrate-assisted catalysis mechanism, featuring oxocarbenium-ion like transition state, with asymmetric phosphor bond breakage, and glycosidic bond formation.
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References
- Demain, A. L. (1999) Appl. Microbiol. Biotechnol. 52 455-463 - PubMed
- Hermann, T. (2003) J. Biotechnol. 104 155-172 - PubMed
- Dye, C., Scheele, S., Dolin, P., Pathania, V., and Raviglione, M. C. (1999) J. Am. Med. Assoc. 282 677-686 - PubMed
- Britton, W. J., and Lockwood, D. N. (2004) Lancet 363 1209-1219 - PubMed
- Hand, C. E., and Honek, J. F. (2005) J. Nat. Prod. 68 293-308 - PubMed
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