Structure, interaction and design studies involving regulatory peptides and proteins

 
Principal Investigator :  Dinakar M Salunke

Project Associates/Assistants
Chitra Gupta
Anupriya Aggarwal (till Feb 2004)

Technical Officer
Sushma Nagpal

Ph D Students
Manisha Goel
Gaurav Sahani
Dhruv K Sethi
Lavanya Krishnan
Veenu Arora
Suvendu Lomash (since Jan 2004)

Collaborator
Kanwal J Kaur
KVS Rao, ICGEB, New Delhi
MJ Swamy, Univ Hyderabad, Hyderabad
J Nagaraju,
CDFD, Hyderabad

The theme of the research is to study the structural aspects of molecular recognition and its applications in analyzing the mechanisms associated with specific regulatory events and in rational molecular design. The objectives of the project are (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.

As part of another on-going activity concerning structural basis of carbohydrate mimicry, we had determined the crystal structures of concanavalin A and Jacalin bound to a porphyrin analog, meso-tetrasulphanatophenylporphyrin (H2TPPS), and established the mimicry of mannopyranoside and porphyrin in terms of their interactions with the two lectins. We have now determined and refined the crystal structure of H2TPPS in complex with yet another lectin, peanut agglutinin (PNA) at 2.9Å resolution. PNA co-crystallizes with H2TPPS in the symmetry packing different from any of its complexes with the carbohydrate ligands determined earlier. The asymmetric unit in PNA-H2TPPS binary complex consists of 11 porphyrin molecules associated with a tetramer of PNA. The ternary complex of PNA with H2TPPS and lactose crystallizes in the symmetry packing similar to that observed in the binary complex. The asymmetric unit in the ternary complex consists of 2 lactose molecules in addition to 11 H2TPPS molecules observed in the case of binary complex associated with a tetramer of PNA. Only two of the four subunits of PNA therefore, show bound lactose molecules. Thus, the quaternary structure of PNA and the arrangement of porphyrin molecules in both complexes are identical.

The carbohydrate-binding sites of PNA are unoccupied in the binary complex. The two pairs of porphyrins interacting with subunits A and B interact near the lactose binding site on PNA, however the porphyrin association in the subunits C and D is farther away from the lactose binding site. In the ternary complex, lactose molecules occupy the carbohydrate binding sites of subunits C and D, whereas subunits A and B are still empty. The PNA molecules in the porphyrin bound state in the binary complex, have a conformational change involving the residues 95 to 104, as compared to the earlier determined structures of PNA. The loop encompassing these residues is one of the four loops (91 to 106, 125 to 135, 75 to 83 and 211 to 216) defining the carbohydrate-binding site of the lectin. The residues of the loop 95 to 104 interact with the porphyrin only in subunits A and B, but the same conformation of the loop is conserved in subunits C and D as well. This observation leads us to propose that the conformation of the loop in the binary complex may in fact represent the native carbohydrate-free state of the protein. This conformation of the loop would make binding of the lactose molecule sterically difficult at the carbohydrate binding sites. The PNA molecule may therefore be required to undergo conformational changes in this loop when binding to it’s carbohydrate ligand. This view is reiterated by the fact that subunits C and D in the ternary complex, when bound to lactose, attain the conformation similar to that determined from earlier carbohydrate bound structures of PNA.

The studies on peptide-carbohydrate mimicry in the immune response, addressed using monoclonal antibodies against mannopyranoside were further extended to include thermodynamic aspects as well. Anti-a-D-mannopyranoside monoclonal antibodies which were generated earlier have been extensively characterized for their ligand binding characteristics. Amongst them, mAb 1H7 recognized only the immunizing antigen, a-D-mannopyranoside, while mAb 2D10 recognized both the carbohydrate and the 12mer peptide. Comparison of the binding of the two antibodies to different carbohydrate ligands showed that 1H7 is highly specific and recognizes only the immunization antigen. On the other hand 2D10 showed indistinguishable binding to three different sugars, mannopyranoside, glucopyranoside and lactose implying degeneracy of recognition specificity. Thermodynamic analyses of binding of the two antibodies to the antigens showed that the affinity of mAb 1H7 to the carbohydrate antigen does not significantly change on increasing temperature from 10°C to 35°C. On the other hand, significant decrease in the affinity of the mAb 2D10 was observed over this temperature range. Analysis of the thermodynamic data along with the kinetics of binding suggested that 1H7 has well-defined relatively rigid antigen combining site and 2D10 may have substantial flexibility in the CDRs providing plasticity of interaction in the antigen combining site. It is attractive to propose that the plasticity in the antigen combining site of the mimicry-recognizing antibody is linked with the observed molecular mimicry. Screening of random peptide libraries displayed on bacteriophage indicated that mAb 2D10 recognized a wide range of peptides. However, the peptide repertoire that binds to mAb 1H7 was found to be restricted in the sequence, confirming that mAb 2D10 exhibited degenerate specificity while mAb 1H7 did not. Apparently, the functional mimicry between the carbohydrate and the peptide, as seen by the immune response, reflected in the recognition specificities with regard to screening of random peptide libraries. These observations also strengthen the proposed link between molecular mimicry and plasticity of antigen-antibody interaction.

In the context of the antibody flexibility and degenerate specificity, maturation of the specificity of recognition in the humoral immune response is being analysed by crystallographic studies involving germ line antibodies. Degenerate specificity in germline antibodies has been demonstrated earlier using phage displayed peptides and identifying diverse peptides which can bind to the antibody. This has been attributed to flexibility in the paratope. We set out to structurally image the correlation of the degenerate specificity with conformational flexibility by determining crystal structures involving antibody and peptide. We have determined structure of the Fab fragment of anti-arsonate antibody 36-65 at 2.7Å resolution. The crystals contain two molecules in the asymmetric unit with end to end packing providing psedio-antigen bound environment at the antigen combining sites of the two molecules. The conformational differences and the packing interactions involving paratopes of the two molecules in the asymmetric unit shed light on the correlation of the plasticity of interaction with conformational variability. The paratopes of the two molecules show differential interactions with the loops of the symmetry related Fab molecules, with corresponding variations in the conformations of the CDR’s L3, H2 and H3 providing structural evidence, relating degenerate specificity with conformational flexibility.

We are presently expanding our studies to include allegy-related functions. We had effectively exploited plant lectins for addressing structural basis of molecular mimicry. A variety of other plant seed proteins with potential allergenic activities have been identified; we are exploring the structure-activity correlation among these proteins. A tropical legume, Vigna unguiculata, has been subjected to structural proteomics as a part of these efforts. A 25kDa protein was purified by subjecting the seed extracts first to ammonium sulphate fractionation and then gel filteration as well as ion-exchange chromatography. Initial attempts at sequencing the N-terminal region of the 25KDa protein for its characterization suggested that the N-terminus was blocked. Trypsin digestion subsequently enabled sequencing of four different internal fragments which were used to identify the protein by database searches. The protein showed more than 85% homology to mung bean seed albumin. Legume albumins are known to be intrinsically allergenic. Structures of none of the protein homologous to Vigna unguiculata albumin is been determined so far. The CD profiles suggested the protein to have relatively high b sheet content. When the purified protein was subjected to crystallization attempts, rhombic shaped crystals which diffracted to 2.1Å resolution, were obtained. The crystals belong to the space group C2 with cell parameters, a=124.9Å,b= 60.1Å,c= 67.5Å and b=111.1°. Intensity data has been obtained and attempts at determining structure are in progress.  

Publications

Original peer-reviewed articles

1.    Chakrabarty P, Sethi DK, Padhan N, Kaur KJ, Salunke DM, Bhattacharya S and Bhattacharya A (2004) Identification and characterization of EhCaBP2: a second member of the calcium-binding protein family of  the protozoan parasite Entamoeba histolytica. J Biol Chem (in press).

2.    Jha BK, Mitra M, Rana R, Surolia A, Salunke DM and Datta K (2004) pH and cation induced thermodynamic stability of human hyaluronan binding protein 1 regulates its hyaluronan affinity. J Biol Chem (in press).

3.    Goel M, Anuradha P, Kaur KJ, Maiya BG, Swamy MJ and Salunke DM (2004) Porphyrin binding to jacalin is facilitated by the inherent plasticity of the carbohydrate-binding site: novel mode of lectin-ligand interaction Acta Crystallogr D Biol Crystallogr 60:281-288.

4.    Jha BK, Salunke DM and Datta K (2003) Structural flexibility of multifunctional HABP1 may be important for regulating its binding to different ligands. J Biol Chem 278:27464-27472.

Reviews/Proceedings

1.     Basu SK, Batra JK and Salunke DM (Eds) (2004) Deep roots, open skies: New biology in india. Narosa Publishing House, New Delhi, 200p.