Development of novel chimeric toxins for targeted therapy by genetic engineering


 

Principal Investigator :    Janendra K Batra

PhD Students
Shveta
Divya Vijayan
Paroma Ghosh
Deepak Gaur

Collaborators
Raj K Puri, CBER, FDA, USA

Design and development of recombinant protein toxins for targeted therapy is the main theme of research of this project. Fungal ribotoxins, plant ribosome inactivating proteins (RIP), and human ribonucleases 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 protein toxins

The objective of the study is to investigate structure-function relationship of Aspergillus ribotoxin restrictocin, human pancreatic ribonuclease (HPR), ribosome inactivating protein saporin, eosinophil cationic protein (ECP), and eosinophil-derived neurotoxin (EDN) to understand their mechanism of action.

The structural and functional characterization of saporin mutants was continued to understand its mechanism of cytotoxicity. From the earlier year’s study no direct correlation was found in the catalytic activity and cytotoxic activity of a few saporin mutants. The mutant Y16A showed a 20-fold reduced protein synthesis inhibitory activity whereas the mutant W208A had a similar protein synthesis inhibitory activity as that of the native toxin. Mutants Y16A and W208A showed similar cytotoxic activities on all the cell lines studied despite the two mutants showing very different protein synthesis inhibitory activity. The activity of native saporin was investigated on the genomic DNA of cell lines treated with the toxin for different periods of time. It was seen that in the presence of toxin the DNA of these cells was fragmented and the appearance of DNA was similar to that of apoptotic cells. The DNA fragmentation did not appear to be a consequence of protein synthesis inhibition by saporin as the laddering was seen at doses of toxin where protein synthesis was only partially inhibited. Among various mutants of saporin only Y16A and R24A showed genomic DNA fragmentation activity. W208A failed to affect DNA inspite of having full N-glycosidase activity. Individually Y16A and W208A were found to be six-fold less active on U937 cells compared to saporin. Interestingly, an equimolar mixture of the two proteins resulted in cytotoxic activity very similar to that of saporin. The study now clearly establishes that the cytotoxic activity of saporin is a cumulative effect of its N-glycosidase and DNA fragmentation activity. The intracellular trafficking and processing of saporin was also investigated in J774A.1 cells using iodinated saporin and/or various metabolic and protease inhibitors. The results demonstrate that i) an acidic endosomal pH is required as 10 mM ammonium chloride protected cells from saporin cytotoxicity, ii) intracellular routing of saporin is not through Golgi as BFA did not affect its activity, iii) upon internalization no proteolytic processing of saporin takes place as none of the protease inhibitors used affected the cytotoxic activity, and iv) saporin remains intact in the cell upto 24 hrs and translocates to nucelus and cytosol.

The characterization of EDN mutants was extended by investigating their activity on substrates, cCMP, UpA and CpA, and also in the in vitro protein synthesis assay. Except for the mutants H82A and D112A all other mutants of EDN namely W7A, Q14A, R36A, N39A, and Q40A had reduced activity on cCMP compared to the native EDN. On UpA all mutants had reduced activity, whereas on CpA, W7A, N39A, H82A and D112A had an increased catalytic activity. In the in vitro cell-free translation mutants W7A, N39A, Q40A, H82A and D112A had an increased inhibitory activity whereas mutants Q14A and R36A had a reduced activity. The study indicates crucial involvement of the studied residues in the catalytic activity and specificity of EDN. Further characterization is required to assign specific roles to these residues in the EDN activity. We have also initiated studies to investigate the role of unique loops and insertions in the EDN protein in its function. Specific mutations have been made to study the role of residues R117, P120 and Q122. Mutants have been generated in which amino acids 1-3, 68-69, and 91-92 have been separately deleted. Characterization of these mutants is currently being carried out.

B.        Construction and evaluation of ribonuclease-based chimeric toxins

The objectives of this study are (i) development of chimeric toxins with restrictocin and human pancreatic ribonuclease, and characterization of their in vitro and in vivo cytotoxic activity and (ii) to design and engineer the chimeric toxins based on the knowledge from the structure-function analysis to improve their biological activity.

IL13 receptors are overexpressed on a variety of human tumors including renal cell carcinoma, AIDS-associated Kaposi’s sarcoma, ovarian carcinoma, prostate cancer and malignant glioma. IL13 has been shown to be a good target for immunotoxin therapy in these carcinomas. We developed four restrictocin-based immunotoxins namely IL13-restrictocin, IL13-spacer-restrictocin, restrictocin-IL13 and restrictocin-spacer-IL13, 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 restrictocin. The fusion proteins were expressed in E. coli and purified to homogeneity. The cytotoxicity of the immunotoxins was checked on target cell lines U373, T98G, A172, and U251, and non-target Colo205 and A431 cell lines. U251 and A172 were found to be the most sensitive cell lines. Restrictocin-spacer-IL13 was found to be the most active immunotoxin indicating that the intracellular proteolytic processing is crucial for the activity and blocking the carboxyl terminus of IL13 hampers its receptor binding activity.

The cytotoxic activity of recombinant dimeric HPR was studied on a variety of cell lines including IMR32, SJRH30, SKNAS, U373MG, J774A.1, K562, A431 and A549. Human neuroblastoma, IMR32 and SKNAS, human rhabdomysarcoma, SJRH30 and human glioblastoma U373MG were found be sensitive to HPR dimer toxicity compared to monomeric native HPR. We are currently investigating the mechanism of HPR dimer cytotoxicity.

Publications

Original peer-reviewed articles

1.    Gaur D, Swaminathan S and Batra JK (2001) Interaction of human pancreatic ribonuclease with human ribonuclease inhibitor: Generation of inhibitor-resistant cytotoxic variants. J Biol Chem  276:24978-24984.

2.     Nayak SK, Bagga S, Gaur D, Nair DT, Salunke DM and Batra JK (2001) Mechanism of specific target recognition and RNA hydrolysis by ribonucleolytic toxin restrictocin. Biochemistry 40:9115-9124.