Protease-catalyzed splicing of peptide bond

 
Principal Investigator :  Rajendra P Roy

Project Associates/Assistants
M Pramod Kumar

Ph D Students
SR Balajee
Lavanya Anantharaman
Srijita Banerjee

Sharmishtha Samantaray

The theme of research is to study the underlying principles and mechanisms of reverse proteolysis, and also apply protease-mediated peptide ligation reactions for semi-synthesis of proteins. Currently, this strategy is being used to engineer new and novel hemoglobin molecules to delineate intermolecular interactions in the assembly of the sickle hemoglobin fiber.

A.    Protease-catalyzed splicing of peptide fragments

The objective of the study is to carry out model studies on protease-mediated peptide ligation and protein semisynthesis.

Although RNase A could not be formed from its complementary fragments [S-peptide (residues 1-20) and S-protein (residues 21-124)] in the crowded milieu, subtilisin-mediated splicing of 20-21 peptide bond readily occurs in the presence of organic cosolvent such as glycerol. We have used this strategy to introduce fluoroPhe residues in RNase A with the idea that studies of semisynthetic RNase A may serve as a model system and provide a general sense of the effect of fluoroPhe residues on structure and function of proteins.

The role of Phe at the 8th position towards stability and catalysis of RNase A was investigated through the introduction of isosteric fluorophenylalanine residues. The Phe8 residue is in sequence contiguity with Lys7 that together with Arg10 forms the P2 substrate subsite. His12, one of the catalytic residues in RNase A is also in close proximity (~ 4Å) to Phe8. We wished to explore if interactions due to Phe8 could be perturbed by alterations of the charge density of the aromatic ring. Two analogs of phenylalanine; 3-fluoro-L-phenylalanine and 3,4-difluoro-L-phenylalanine, were used so that a gradation in the effects of hydrophobic and electronic changes can be brought about in the region of RNase A that is sensitive to substrate binding and catalysis. The three synthetic peptides, native S-peptide, SFx (S-peptide with 3-fluoro-L-phenylalanine at the 8th position) and SFxx (S-peptide with 3,4-difluoro-L-phenylalanine at the 8th position), respectively, were ligated with S-protein to generate native RNase A and the mutant proteins (SFx-RNase A and SFxx-RNase A). The proteins were obtained in pure form.

The ability of fluoroPhe residues to impact the polypeptide conformation was assessed in the S-peptide and RNase A. S-peptide and its analogs, although, almost structure-less in aqueous solution, exhibited significant helical structure in the presence of structure-promoting organic co-solvent. The CD spectra monofluoro derivative was identical to that of S-peptide suggesting that the introduction of fluorine atom in the phenyl ring did not affect the stability of the peptide. However, a slight decrease in the helicity was noticeable in the difluoro derivative indicating that the two fluorine atoms substituted in the adjacent positions of the Phe8 may have perturbed the peptide stability by de-stabilizing Phe8-His12 interactions. Although, this is in consonance with the fact that His12+ and Phe8 interaction in the C-peptide stabilizes the a-helix, the effects observed in the mutant peptides are rather modest. Interestingly, this behavior was maintained even at the level of protein in that the thermal melting profiles of mutant proteins (SFx-RNase A and SFxx-RNase A) were almost identical to the wild type enzyme. Thus, introduction of fluoroPhe residues do not seem to affect the conformational stability of RNase A in any significant fashion. Studies on the effect of fluoroPhe residues on enzyme kinetics are currently in progress.

B.    Chemo-enzymic engineering of sickle hemoglobin

The objective of the project is to studysite-specific incorporation of natural and/or nonstandard amino acids in hemoglobin to probe the intermolecular interactions in sickle hemoglobin (HbS) fiber.

During the reporting period, studies were focused to delineate the inhibitory mechanism of Gly mutants. Although, sites 19 and 21 are not involved in any fiber contact but their replacements with Gly residues generate a sequence (residues 18-22, G-G-H-G-G) that has the propensity to enhance the conformational flexibility of the AB region. The AB region of a-chain contains several contact sites of the fiber (a16, a20 and a23) and lies in spatial proximity to a cluster of GH corner residues that are implicated in fiber interactions (residues a113 through a116). Besides, AB-GH corners of the a-chain engage in extensive inter-tetrameric interactions with AB-GH corners of the b-chain yielding physiologically important intra-double strand axial contacts of the fiber. Therefore, it is conceivable that even subtle alteration of the conformational dynamics generated through rational amino acid changes at non-contact sites at the AB or GH corners of a/b chains might influence the HbS polymerization by perturbing the inter-tetrameric interaction interface of the fiber. Toward this, we have carried out dynamics investigations of the Gly mutant chain. Additionally, we have engineered a-aminoisobutyric acid (Aib) residues at 19 and 21 positions to compare and contrast the influence of Gly residues at the same site.

MD simulations of mutant a-chains show that both, Gly and Aib mutants, perturbed the dynamics of the AB and GH region of the chain. However, distribution of Ca-Ca distances between pairs of AB-GH residues indicated that Gly mutant exhibit greater fluctuations as compared with Aib and Ala (native chain). The distribution of Ca-Ca distance between Ala13 and Glu116 is more variable in the Gly mutant and tends towards larger values. A similar trend is also apparent in the Ca-Ca distance distribution calculated for the Ala13-Leu113 pair. In the case of the Lys16-Glu116 and Lys16-Leu113 pairs, the effect is less pronounced for the Ca-Ca distances, but is clearly visible when one considers the side chain atoms NZ of Lys16 and CD of Glu116. The dynamical cross-correlation maps (DCCM) of native (Ala) and Aib substituted a-chains showed strong motional coupling of AB and GH region residues, whereas that of Gly substituted chains displayed significantly less coordinated movement. This can be interpreted to mean that AB-GH region of native or Aib mutant chains may be more rigid than the Gly mutant chain. However, Aib residue may exert similar effects as that of the Ala. Interestingly, the polymerization behavior of Aib mutant was found to be very similar to native HbS.

Previously we had reported the polymerization behavior of the aforementioned triple and double mutants and deduced that the interactions emanating from mutations of the AB and EF regions must be additive. We determined the polymer solubility (Csat) of HbS containing only the point mutation of a Gln or His for Asn at a78 to assess the individual contribution of these residues in the polymerization of HbS. The Csat of a2(Q78)b2S mutant was found to be similar to that of the native HbS suggesting that Gln residue behaves in much the same way as Asn. In contrast, the HbS mutant [a2(H78)b2S] containing His at this site yielded a Csat that was significantly lower than that of native HbS. This value of Csat was far less than that expected from an additive contribution of double [a2(G19G21)b2S] and single mutant [a2(H78)b2S] in the triple mutant. The shift in Csat of the triple mutant clearly suggested that the polymerization-enhancing effects due to the presence of His-78 at the EF corner synergistically compensated for the inhibitory effect, emanating from the Gly substitutions at the AB corner. Interestingly, His-78 shifted the Csat of double mutant [a2(Q16H78)b2S] in a similar synergistic fashion as it did in the case of the triple mutant [a2(G19G21H78)b2S]. Thus the polymer solubility measurements of the point mutant HbS (His-78) unambiguously established the cooperative linkage of AB and EF region fiber interactions.

In summary, the ability of a polymerization-enhancing mutation of an established inter-double strand contact point (aHis-78) at the EF corner of the a-chain to completely neutralize the inhibitory effect of Gly substitutions at the AB corner is an interesting result that suggest long-range and non-additive coupling of mutational effects in HbS polymerization. This view is strengthened with the observation that the coupling of aHis-78 at the EF corner to mutation of a specific intra-double strand fiber contact (a16) in the AB region occurs in a similar synergistic fashion as it happened with Gly mutants. The fact that aLys-16 makes axial contacts with the GH corner residues (a114, a115), and Gly substitutions at the AB corner exert their influence on polymerization by inducing dynamic changes in the AB-GH region of the a-chain, raises the intriguing possibility of interaction-linkage between AB, GH and EF regions of the a-chain in the HbS fiber assembly. Our previous work demonstrating that the inhibitory effect of a16 was additive with a113 (GH1) is consistent with this idea.

Publications

Original peer-reviewed articles

1.     Sudha R, Anantharaman L, Sivaram MV, Mirsamadi N, Choudhury D, Lohiya NK, Gupta RB and Roy RP (2004) Linkage of interactions in sickle hemoglobin fiber assembly: Inhibitory effect emanating from mutations in the AB region of the a-chain is annulled by a mutation at its EF corner. J Biol Chem (in press).

Reviews /Proceedings

1.     Balajee SR, Kumaran S, Datta D and Roy RP (2004) Protein splicing by reverse proteolysis. In: Deep roots, open skies: New biology in India. (Eds. Basu SK, Batra JK and Salunke DM) Narosa Publishing House, New Delhi, 141-145.