Development of novel chimeric toxins for targeted therapy by genetic engineering

 
Principal Investigator :  Janendra K Batra

Ph D Students
Punyatirtha Dey
Paroma Ghosh
Deepa Sikriwal

Divya Seth (till Jun 2003)

Collaborator
Raj K Puri, CBER, FDA, USA

The theme of research is the design and development of recombinant protein toxins for targeted therapy. Members of fungal ribotoxin, plant ribosome-inactivating proteins, and ribonuclease-A families are being analysed for structure-function relationships to understand their molecular mechanism of action with an aim to design knowledge-based chimeric toxins.

A.    Studies on the molecular mechanism of action of ribonucleolytic and ribosome-inactivating protein toxins

The objective of the study is to investigate structure-function relationship of Aspergillus ribotoxin, restrictocin; ribosome inactivating protein, saporin; human pancreatic ribonuclease, and eosinophil-derived neurotoxin to understand their mechanism of catalysis and cytotoxicity.

We had earlier demonstrated that for the catalytic activity of EDN the putative substrate binding residue Gln14 is indispensable; Arg36 and Gln40 could be partially dispensed with, and Trp7, Asn39, His82 and Asp112 individually are completely dispensable. EDN and its several mutants were assayed for their ability to inhibit the infectivity of extracellular virions of the paramyxovirus, RSV-B. The mutants Q14A, R36A, H82A and D112A were taken with the aim of studying the correlation between RNase activity and antiviral activity. While Q14A showed an almost complete loss of activity on yeast tRNA, R36A, H82A and D112A had enzymatic activity comparable to that of EDN. RNase A was used as a control as it is not known to have antiviral activity on RSV-B inspite of being a much more active ribonuclease. EDN inhibited the infectivity of RSV-B by 50% at a concentration of 0.2 mM. While mutant R36A had antiviral activity very similar to that of EDN, the mutant Q14A did not have any antiviral activity and did not cause any loss of infectivity of RSV-B virions. The mutant H82A had slightly higher activity than EDN, and D112A had about 65% of the activity shown by EDN. The three mutants in loop L7, R117A, P120A and Q122A showed a loss of activity and their ID50 values were 2.5-3.5-fold higher than EDN. The maximum loss of activity was observed in R117A mutant. RNase A was inactive even at concentrations as high as 10 mM. The current study shows that although the antiviral activity of EDN is dependent on its ribonucleolytic activity, loop L7 is crucial for the antiviral activity. While Pro120 and Gln122 are required structurally for full antiviral activity, Arg117 is critical for EDN’s interaction of with RSV-B.

The saporin isoforms show a very high sequence similarity, with all catalytically crucial residues conserved. We have earlier shown saporin-6 to have higher N-glycosidase and DNA-fragmentation activities than saporin-5 that reflect in a similar difference in their cytotoxic activities. The difference in the activity of the two isoforms could be attributed to amino acid differences, which lie outside the proposed active site of the toxin. Of the twelve differences between saporin-5 and saporin-6, substitutions at positions 134(Q/K), 147(S/L), 149(S/F), 162(D/N), 188(I/T) and 196(N/D) result in change in polarity or charge of amino acid residue. To understand the mechanism of saporin toxicity and specific contribution of these residues in the activity of toxin, we substituted theses residues singly in saporin-6 to those in saporin-5. The preliminary results show that individually these residues are not critical for the catalytic as well as cytotoxic activity of saporin.

We earlier analyzed a model of restrictocin-29-mer RNA substrate complex to understand the mechanism of restrictocin catalysis, particularly to identify residues involved in stabilizing the substrate onto the enzyme. The base G10, analogous to G4319 of 28S rRNA, considered to be an identity element for ribotoxin recognition, forms a large number of contacts, both van der Waal and hydrogen bonding most of which are with Lys42, Ser46, Lys110 and Lys111 residues of restrictocin. In addition Pro48 was also predicated to be important for restrictocin catalysis. We made four single amino acid mutants, K42A, S46A, P48A and K111A, to investigate the roles of Lys42, Ser46, Pro48, and Lys111 respectively in the ribonucleolytic activity of restrictocin. While Lys111 appears to be absolutely essential for the catalytic activity of restrictocin, mutation of Lys42, Ser46 and Pro48 rendered the toxin partially inactive.

B.     Construction and evaluation of ribonuclease and ribosome-inactivating protein-based chimeric toxins

The objective of the study is to develop chimeric toxins with ribosome-inactivating and ribonucleolytic toxins, and to characterize their in vitro and in vivo cytotoxic activity and also, to rationally design and engineer the chimeric toxins based on the knowledge from the structure-function analysis to improve their biological activity.

The cytotoxic activity of IL13-restrictocin-KDEL and IL13-spacer-restrictocin-KDEL, in which the carboxyl terminus of restrictocin was extended by incorporating the KDEL tetrapeptide, was assayed on IL13 expressing cell lines U251 and A172. Though both the chimeric toxins displayed cytotoxicity there was no improvement in the activity compared to that of IL13-restrictocin and IL13-spacer-restrictocin respectively.

We have developed saporin, and human pancreatic ribonuclease (HPR)-based immunotoxins targeted at the human IL13 receptor. The fusion proteins contain IL13 fused either directly or through a proteolytically cleavable spacer at the amino or carboxyl terminus of saporin, and a cytotoxic variant of HPR. The fusion proteins were expressed in E.coli and purified to homogeneity. The cytotoxicity of the immunotoxins was checked on target cell lines A172 and U251. However, these chimeric toxins were not found to be as potent as restrictocin-containing chimeric toxins directed at the IL-13 receptor.

Publications

Original peer-reviewed articles

1.     Bagga S, Hosur MV and Batra JK (2003) Cytotoxicity of ribosome-inactivating protein saporin is not mediated through a2-macroglobulin receptor. FEBS Lett 541:16-20.

Review/Proceedings

1.     Batra JK (2003) The Aspergillus ribotoxins. Appl Genomics Proteomics 2:145-159.

2.     Basu SK, Batra JK and Salunke DM (2004) (Editors) Deep roots, open skies: New biolgy in India. Narosa Publishing House, New Delhi, 200p.