Structure, interaction and design studies involving regulatory peptides and proteins


 

Principal Investigator : Dinakar M Salunke

Co-Investigator
Kanwal J Kaur

Project Associates/Assistants
Kavita Singh
Deepti Jain
Sushma Nagpal
Pampi Sarkar (till Dec 2000)

CSIR Associate
Gargi Mitra

CSIR Sr Research Fellow
Pratibha Srivastava

Ph D Students
Deepak Nair
Usha Nair
Manisha Goel
Gaurav Sahani
Dhruv K Sethi

Collaborators
Satyajit Rath
KVS Rao, ICGEB, New Delhi
A Karande, IISc, Bangalore
J Nagaraju, CDFD, Hyderabad

The structural aspects of molecular recognition and its applications in analyzing the mechanisms associated with specific regulatory events and in rational molecular design is the theme of research. The main objectives include i) understanding the protein architecture, ii) analysis of the structural principles of molecular recognition and mimicry, iii) Structural biology of various regulatory events and iv) rational molecular design studies based on the above.

Conacanavalin A (ConA) is an extensively studied model lectin. It has provided vital insights regarding protein-carbohydrate recognition. It has also been shown to bind to a variety of other ligands including certain peptides and porphyrin derivatives. Different porphyrins bind to ConA with affinities comparable to that of Mea-D-mannopyranoside. The crystal structure of meso-tetrasulphanatophenylporphyrin complexed with ConA was analyzed in order to define the binding site and mode of interactions of porphyrins with ConA and correlate them with the corresponding interactions involving other ligands. A pair of stacked porphyrin molecules stabilizes the crystal structure by end-to-end cross-linking of ConA resulting in a three-dimensional network similar to that observed on agglutination of cells. The porphyrin binds to ConA predominantly through hydrogen bonds and water-mediated interactions involving the sulphanatophenyl side group at the site overlapping with the Mea-D-mannopyranoside binding site. Although the sulphanatophenyl side group of the porphyrin does not show any topological resemblance with the monosaccharide, it mimics hydrogen bonding interactions of ConA-sugar binding, implying molecular mimicry between sugar and porphyrin.

In order to define the invariant structural properties associated with molecular recognition, a set of genetically distinct monoclonal antibodies are being subjected to crystallographic analyses. The model system used here constitutes the IgG antibodies PC283, PC282 and PC287 which have been raised against the peptide antigen PS1 (HQLDPAFGANSTNPD). The peptide is derived from the large surface antigen of the Hepatitis B virus. The immune response against this peptide antigen has been studied extensively. It has been shown that the three antibodies bind to an epitope defined by the same continuous stretch of amino acids-DPAF. The antibodies PC283, PC282 and PC287 bind the DPAF epitope with comparable affinities. A detailed structural analysis of the bound and unbound states of these antibodies was completed.

 The comparison of the variable region sequences of both heavy and light chains of the three antibodies shows that the three antibodies are genetically heterogeneous. For CDR sequences, there are a total of 14 differences between PC283 and PC282, 8 differences between PC282 and PC287 and 11 differences between PC287 and PC283. The crystals of the Fab of PC283, PC282 and PC287 in complex with the antigen PS1 were obtained and they diffracted up to 2.9, 2.5 and 2.5 Å, respectively. The crystals of the Fab of PC282 and PC287 were obtained in their native state also and they diffracted up to 1.8 and 2.3 Å, respectively. The three complex and the two native structures have been refined using all data to their maximum resolutions. The crystallographic R factors for all the structures were within 20% and the free R factors were within 26%. The structures of the three complexes were compared in all aspects. There were significant differences in the elbow angle and the VH:VL interface area in the three antibodies. It has been postulated that differences in elbow angle and VH:VL interface area reflect the differences in relative orientation of the VH and VL domains. Changes in the relative orientation of the variable domains can lead to changes in the topology of the antigen-binding site. When the variable domains of the three antibodies were structurally aligned it was observed that the CDR L3 shows a significant change in conformation in case of PC287 and PC282 as compared to PC283. This is due to the insertion present in CDR L3 of PC287 and PC282. A comparison of the rmsd values in the position of Ca atoms shows that there is only slight variation in the main chain conformation of the other five CDRs.

 The conformation of the peptide in the three complexes was compared. For PC282 density was seen for the stretch QLDPAFG and for PC287 the stretch HQLDPAFGA could be fitted to the observed density, unlike in case of PC283 where electron density could be seen for all fifteen residues. The residues Asp4P, Pro5P, Ala6P and Phe7P form a b-turn in all the three complexes. It is appropriate to mention here that the peptide shows a random conformation as shown by CD and NMR studies. Thus the main chain conformation is very similar in case of these four residues. In addition, the side chain of the residues Pro5P, Ala6P and Phe7P is also very similar. However, the side chain conformation of Asp4P in case of PC283 is very different from that in case of PC287 and PC282. The conformation of the residues before Asp4P is different in case of PC283 than in case of PC282 and PC287. A comparison of the interactions between the peptide and antibody highlights the similarities and differences in the recognition of the peptide by the three antibodies. There is a great deal of degeneracy in the location and nature of the antibody residues, which interact with the three residues Pro5P, Ala6P and Phe7P. This is true even for residues from CDR L3 which has a different main chain conformation in PC283 than that seen in PC282 and PC287. The interactions shown by Leu3P and Asp4P are very different in case of PC283 as compared to that in PC282 and PC287. In case of PC283 Asp4P is oriented towards the surface of the groove due to the formation of a salt bridge with the side chain of Arg53H. In case of PC287 and PC282 this interaction is absent as there is a Ser residue at the 53H position the side chain of, which is too short for any such interactions to occur. As a result the Asp4P side chain turns downwards into the groove and forms hydrogen bonding interactions with the side chain of Ser91L (which is Thr in PC283). Consequently the Leu3P also has to change its conformation in case of PC282 and PC287 because Asp4P occupies the position it occupied in PC283. The changes in conformation of Leu3P and Asp4P show that the flexible nature of the peptide allows it compensate for changes in the paratope by changing its conformation in such a way that the interactions with the CDR residues are optimized.

When the bound and native structures of PC287 were compared it was seen that the main chain conformation of all the CDRs were similar. The side chain conformation of the residues from CDRs L1, L2, H1, H2 and H3 were also similar. In case of CDR L3, the comparison showed that the residue Tyr94 flips outwards to facilitate peptide binding. In case of PC282 it was seen that the main chain as well as side chain conformation of the residues from CDRs H1, H2 and L2 were similar. The CDR H3 undergoes a significant outward movement on peptide binding. The CDRs L1 and L3 show a slight inward movement on peptide binding. Thus, it appears that the two antibodies PC282 and PC287 follow two different mechanisms to arrive at a common conformation of peptide and CDRs in the bound state. In spite of repeated attempts, PC283 Fab was not crystallized in its native state. It is inferred that the PC283 CDRs are flexible and the peptide binding is required for their stabilization. This flexibility would lead to a repertoire of conformations for the CDRs in the unliganded state compared to the bound form.

The ability of the peptide to move from a disordered conformation to an ordered b-turn conformation in different antigen binding sites could be one of the reasons for its well characterized immunodominant properties. The similarities observed between the three complexes point that the immune response appears to have evolved a common conformation of CDRs in genetically distinct antibodies to bind to a flexible epitope in a similar conformation with similar affinities. The differences observed in the native structure lead to the conclusion that different mechanisms are followed in the antibodies to converge to the same bound conformations.

The crystal structure of an antibacterial protein of immune origin, which was purified from tasar silkworm (Antheraea mylitta) larvae after induction by E.coli infection, has been determined and refined. The core structure of this protein is similar to c-type lysozymes and a-lactalbumins. The catalytic residues are conserved with respect to the chicken lysozyme. While the A.mylitta protein is functionally similar to chicken lysozyme unlike human a-lactalbumin, it is significantly different in certain structural features with respect to the other two proteins. Although physiological origins of the tasar silkworm protein and chicken lysozyme are different, the catalytic mechanism employed by them would probably be similar with subtle differences in the specificity and level of activity. On the basis of the structural comparisons between tasar silkworm protein, chicken lysozyme and human a-lactalbumin it can be suggested that the conformational changes in a protein are minimal during rapid evolution as compared to those in the normal course of evolution.

Publications

Original peer-reviewed articles

1.   Nair DT, Singh K, Sahu N, Rao KVS and Salunke DM (2000) Crystal structure of an antibody bound to an immunodominant peptide epitope: Novel features in peptide-antibody recognition. J Immunol 165:6949-6955.

2.   Manivel V, Sahoo NC, Salunke DM and Rao KVS (2000) Maturation of an antibody response is governed by modulations in flexibility of the antigen-combining site. Immunity 13:611-620.

3.   *Jain D, Kaur KJ, Sundaravadivel B and Salunke DM (2000) Structural and functional consequences of peptide-carbohydrate mimicry: crystal structure of a carbohydrate-mimicking peptide bound to concanavalin A. J Biol Chem 275:16098-16102 (*in press last year, since published).

4.   Jain D, Kaur KJ, Goel M and Salunke DM (2000) Structural basis of functional mimicry between carbohydrate and peptide ligands of ConA. Biochem Biophys Res Commun 272:843-849.

5.    Kaur KJ, Jain D, Goel M and Salunke DM (2001) Immunological implications of structural mimicry between a dodecapeptide and a carbohydrate moiety. Vaccine (in press).

6.   Chavali GB, Vijayalakshmi C and Salunke DM (2001) Analysis of sequence signature defining functional specificity and structural stability in helix-loop-helix proteins. Proteins: Struct Func Genet 42:471-480.

7.   Jain D, Kaur KJ and Salunke DM (2001) Plasticity in protein-peptide recognition: crystal structures of two different peptides bound to concanavalin A. Biophys J (in press).