A measure of the broad substrate specificity of enzymes based on 'duplicate' catalytic residues - PubMed (original) (raw)
Comparative Study
A measure of the broad substrate specificity of enzymes based on 'duplicate' catalytic residues
Sandeep Chakraborty et al. PLoS One. 2012.
Abstract
The ability of an enzyme to select and act upon a specific class of compounds with unerring precision and efficiency is an essential feature of life. Simultaneously, these enzymes often catalyze the reaction of a range of similar substrates of the same class, and also have promiscuous activities on unrelated substrates. Previously, we have established a methodology to quantify promiscuous activities in a wide range of proteins. In the current work, we quantitatively characterize the active site for the ability to catalyze distinct, yet related, substrates (BRASS). A protein with known structure and active site residues provides the framework for computing 'duplicate' residues, each of which results in slightly modified replicas of the active site scaffold. Such spatial congruence is supplemented by Finite difference Poisson Boltzmann analysis which filters out electrostatically unfavorable configurations. The congruent configurations are used to compute an index (BrassIndex), which reflects the broad substrate profile of the active site. We identify an acetylhydrolase and a methyltransferase as having the lowest and highest BrassIndex, respectively, from a set of non-homologous proteins extracted from the Catalytic Site Atlas. The acetylhydrolase, a regulatory enzyme, is known to be highly specific for platelet-activating factor. In the methyltransferase (PDB: 1QAM), various combinations of glycine (Gly38/40/42), asparagine (Asn101/11) and glutamic acid (Glu59/36) residues having similar spatial and electrostatic profiles with the specified scaffold (Gly38, Asn101 and Glu59) exemplifies the broad substrate profile such an active site may provide. 'Duplicate' residues identified by relaxing the spatial and/or electrostatic constraints can be the target of directed evolution methodologies, like saturation mutagenesis, for modulating the substrate specificity of proteins.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
Figures
Figure 1. Active sites of proteins with the highest and lowest BrassIndex.
(a) rRNA Methyltransferase (PDBid:1QAM): This protein has the highest BrassIndex, as can be seen by the presence of various similar residues in close proximity, that results in electrostatically similar scaffolds as well (Table 2). (b) Palmitoyl protein thioesterase 1 (PPT1) (PDBid:1EH5): Protein with the next highest BrassIndex. We hypothesize that a ‘replica’ catalytic triad consisting of Asp288 exists and is congruent to the known catalytic triad (His289, Asp233, Ser115) (Table 3). (c) Palmitoyl protein thioesterase 2 (PPT2) (PDBid:1PJA): PPT2 has a 26% similarity with PPT1, but has a non-redundant role in the cell. The absence of supporting residues could be a possible reason why PPT2 is unable to act upon all compounds (particularly those with have bulky head groups) which PPT1 catalyzes. (d) Platelet-activating acetylhydrolase (PDBid:1BWP): This protein has the lowest BrassIndex, which is due to the absence of ‘duplicate’ residues in the proximity of the core active site residues (Table 5). This implies that this protein has high specificity, a fact that has been noted in .
Figure 2. Statistics of BrassIndex on the population: (a) Frequency distribution of BrassIndex.
It can be seen that most proteins are highly specific (low BrassIndex), and the number of proteins with high specificity drops exponentially. (b) Lack of correlation between promiscuity and substrate specificity (Brass) indices: As expected, there is no correlation between promiscuity (defined as the ability to catalyze reactions distinct from the one the protein has evolved to perform, but using the same active site scaffold) and the ability of enzymes to catalyze the reaction of different, but related, compounds using the same catalytic mechanism (broad substrate specificity). The promiscuity indices are computed as described in .
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This work was funded by the Tata Institute of Fundamental Research (Department of Atomic Energy), and the Department of Science and Technology (JC Bose Award Grant). BA extends gratitude to the Icelandic National Research Council (RANNIS) and the University of Iceland Research Found for supporting the project financially. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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