Protease-catalyzed splicing of peptide bond 


 

Principal Investigator : Rajendra P Roy

Ph D students
M V S Sivaram
R Sudha
S R Balajee
Lavanya Anantharaman

The two major themes of the project are i) understanding the structural and mechanistic imperatives of peptide ligation reactions catalyzed by proteases and ii) chemo-enzymic engineering of new and novel hemoglobin tetramers to delineate the intermolecular interactions in the sickle hemoglobin fiber.

A.    Protease-catalyzed splicing of native peptide fragments

Model studies of reverse proteolytic condensation reactions utilizing natural or designer peptide segments were continued. During the current year, we investigated the influence of macromolecular crowding on the protease-catalyzed peptide bond equilibrium. The rationale, that volume exclusion by an inert background macromolecule admixed with a protein would shift the equilibrium towards attaining a smallest excluded volume and favour formation of compact structures, formed the basis of the studies. We surmised that protease-mediated synthesis of coiled-coil or helix bundle type of structures from the respective constituent peptide fragments should be facilitated in the presence of crowded dextran solution as intermolecular interactions leading to association of enzymically ligated molecules into such ordered structure would result in a reduction of excluded volume.

Three 20 residues designer peptides, each containing Glu at the eleventh position to ensure specificity of V8 protease, were employed for this study; two of these peptides were shown to exhibit coiled-coil structures while the third one was a random coil control. The V8 protease-catalyzed ligation of respective complementary fragments (residues 1-11 and 12-20) of both the coiled-coil peptides proceeded smoothly, albeit with different extents, in the presence of dextran. In contrast, under similar conditions, the complementary fragments of the random coil peptide could not be ligated. These results suggest that enhanced tendency of polypeptide chains to form compact complexes in crowded media could be exploited to facilitate reversal of proteolysis.

B.    Chemo-enzymic engineering of proteins

We had constructed mutants of hemoglobin with a view to probe the intermolecular interactions in sickle hemoglobin (HbS) fiber. Detailed studies of HbS (a113His ®Leu) construct was carried out to unequivocally establish a role for a113 amino acid residue in the polymerization process. For the sake of brevity, henceforth the above mutant HbS would be referred to as HbS Twin Peaks after a natural hemoglobin variant. The global conformation of HbS Twin Peaks with respect to the environment of heme, as judged by soret region CD spectra, was found to be similar to that of the native HbS. First derivative UV spectra for liganded and unliganded forms of HbS Twin Peaks, which serve as indicators of micro-environment of aromatic residues located at the a1b2 interface (Trp37b and/or Tyr42a), were also similar to HbS indicating that HbS Twin Peaks assumes HbS-like quaternary structure. The preservation of quaternary structure and dimer-interaction in HbS Twin Peaks was further corroborated by oxygen binding measurements. Both the P50 (oxygen affinity) and Hill coefficient (extent of co-operativity) of HbS Twin Peaks were similar to HbS. The kinetics of polymerization revealed that the Twin Peaks mutation impeded the rate of gelation of HbS. This result was consistent with the polymer solubility (Csat) data; Csat of HbS Twin Peaks was found to be about 1.8 fold higher than that of native HbS. In order to further authenticate the participation of a113 site in the polymerization process as well as to evaluate its relative inhibitory strength, we constructed HbS tetramers in which a113 mutation at the GH corner was coupled individually with two established fiber contact sites (a16 and a23) located in the AB region of the a-chain; HbS (a16Lys®Gln, a113Leu®His), HbS (a23Glu®Gln, a113Leu®His). The single mutants at a16/a23 sites were also engineered as controls. The Csat values of the HbS point mutants involving sites a16 or a23 were higher than HbS but markedly lower as compared with HbS Twin Peaks. In contrast, Csat of both the double mutants were comparable to or higher than HbS Twin Peaks indicating independent or additive inhibitory effect. The demonstration of inhibitory effect of a113 mutation alone or in combination with other sites, in quantitative terms, unequivocally establishes a role for this site in HbS gelation. a113 amino acid residue is not postulated in any interactions in the crystal structure of HbS and is also excluded by the models of the HbS fiber. Further solution co-polymerization studies of HbS Twin Peaks should help delineate the stereochemistry of a113 residue in the polymer and facilitate efforts to develop an accurate model of the HbS fiber that could serve as a blueprint for therapeutic intervention.

Publications

Original peer-reviewed articles

1.    Sivaram MVS, Sudha R and Roy RP (2001) A role for a113 (GH1) amino acid residue in the polymerization of sickle hemoglobin: Evaluation of inhibitory strength and interaction-linkage with two fiber contact sites (a16/23) located in the AB region of the a-chain. J Biol Chem (in press).

2.   *Kumaran S, Datta D and Roy RP (2000) An enigmatic peptide ligation reaction: Protease-catalyzed oligomerization of a native protein segment in neat aqueous solution. Protein Science 9:734-741. (*in press last year, since published).