Knowledge-based homology modelling and experimental determination of amino acid side chain accessiblity by the laser photo CIDNP(chemically induced dynamic nuclear polarization) approach in solution: lessons from the small sialidase of Clostridium perfringens

Hans-Christian Siebert1,2, Emadeddin Tajkhorshid3,4, Claus-Wilhelm von der Lieth4, Reinhard G. Kleineidam5, Sussane Kruse6, Roland Schauer6, Robert Kaptein2, Hans Joachim Gabius1 and Johannes F. G. Vliegenthart2*

  1. Institut für Physiologische Chemie, Tierärztliche Fakultät, Ludwig-Maximilians-Universität, Veterinärstr. 13, D-80539 München, Germany
  2. Bijvoet Center for Biomolecular Research, University of Utrecht, P. O. Box 80075, NL-3508 TB Utrecht, The Netherland
  3. Zentrale Spektroskopie, Deutsches Krebsforschungszentrum, Im Neuenheimer Feld 280, D-69120 Heidelberg, Germany
  4. Department of Medicinal Chemistry, School of Pharmacy, Tehran University of Medical Sciences, P. O. Box 14155/6451, Tehran, Iran
  5. Biochemisch Laboratorium, University of Groningen, Nijenborgh 4, NL-9747 AG Groningen, The Netherland
  6. Biochemisches Institut, Christian-Albrechts Universität, Olshausenstr. 40, D-24098 Kiel, Germany

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Abstract

Sialidases (N-acylneuraminosyl-glycohydrolases, EC 3.2.1.18) hydrolytically cleave alpha-glycosidically bound sialic acids, derivatives of the amino sugar neuraminic acid. Sialic acids are mostly found as terminal constituents of oligosaccharides, glycoproteins and glycolipids in higher animals. The sialidases, however, are widely distributed not only throughout the metazoan animals of the deuterostomate lineage, but also among protozoa, viruses, fungi and bacteria, most of which are unable to produce sialic acid by themselves. Remarkably, the enzyme is often produced by microorganisms, which live in close contact with an animal host, whereby the enzyme may serve as a pathogenicity factor, or as an important tool for nutrition.

X-ray structure of sialidase of Salmonella typhimurium was used as the template for homology modeling of Clostridium perfringens sialidase (CPS). Both FastA and BLAST algorithm indicate high similarity between these two enzymes. The amino acids located in the four "Asp boxes" and those of the active site of the enzyme are highly conserved. Construction of the starting framework, fitting of the CPS backbone, addition of loop regions and missing side chains, and preliminary refinement of model were carried out using the Swiss-Model Automated Protein Modelling service. The generation of hydrogen atoms and automatic assignment of partial charges of each atom were accomplished using the INSIGHTII. The structures were then submitted to an MD simulation using the CVFF force field at a temperature of 300 K with an equilibration time of 20 ps and production period of 100 ps. The ten lowest potential energy conformers were selected for further minimization and surface accessibility calculation of aromatic residues.


The function of sialidases can be studied with help of mutants constructed by site-directed mutagenesis. Based on the known three- dimensional structure of the Salmonella typhimurium sialidase, amino acids analogous to those that seem to be important for substrate binding or catalysis, were selected for mutation in CPS. The activity of some of the mutant sialidases was strongly decreased but the Km-values were hardly changed.

The side chains of tyrosine, tryptophan and histidine are able to produce CIDNP (Chemically Induced Dynamic Nuclear Polarization) signals after laser irradiation in the presence of a suitable radical pair-generating dye. The CIDNP technique has previously been used for comparative studies of non-specific and specific interaction between the lac-repressor headpiece and DNA denatured states of lysozyme as well as of glycoproteins in glycosylated and deglycosylated form or in sialylated and desialylated form in solution.


The results from CIDNP experiments with CPS and its mutant forms indicated significant changes in the pattern of surface accessibility of aromatic residues of CPS in all of the mutants, which is in complete agreement with the measured Connolly surfaces of amino acids in the modeled structures.



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