Reductive methylation and mutation of an anthrax toxin fusion protein modulates its stability and cytotoxicity

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Bachran, Christopher ^a   Gupta, Pradeep K ^a   Bachran, Silke ^a   Leysath, Clinton E ^a   Hoover, Benjamin ^a   Fattah, Rasem J ^a   Leppla, Stephen H ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; ANTINEOPLASTIC AGENT; BACTERIAL ANTIGEN; BACTERIAL TOXIN; EPITOPE; EXOTOXIN; HYBRID PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BINDING; TOXA PROTEIN, PSEUDOMONAS AERUGINOSA; VIRULENCE FACTOR;

ANIMAL; CELL LINE; CHEMISTRY; CYTOSOL; GENETICS; HAMSTER; HUMAN; IMMUNOLOGY; KINETICS; MASS SPECTROMETRY; METABOLISM; METHYLATION; MUTATION; PROTEIN DOMAIN; PROTEIN STABILITY; UBIQUITINATION;

ADP RIBOSE TRANSFERASES; ANIMALS; ANTIGENS, BACTERIAL; ANTINEOPLASTIC AGENTS; BACTERIAL TOXINS; CELL LINE; CRICETINAE; CYTOSOL; EPITOPES; EXOTOXINS; HUMANS; KINETICS; MASS SPECTROMETRY; METHYLATION; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; RECOMBINANT FUSION PROTEINS; UBIQUITINATION; VIRULENCE FACTORS;

EID: 84899121610     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep04754     Document Type: Article

References (34)

1. Fuchs, H. & Bachran, C. Targeted tumor therapies at a glance. Curr Drug Targets 10, 89-93 (2009).
2. Liu, S., Netzel-Arnett, S., Birkedal-Hansen, H.&Leppla, S. H. Tumor cell-selective cytotoxicity of matrix metalloproteinase-activated anthrax toxin. Cancer Res 60, 6061-6067 (2000).
3. Liu, S. et al. Matrix metalloproteinase-activated anthrax lethal toxin demonstrates high potency in targeting tumor vasculature. J Biol Chem 283, 529-540, doi:10.1074/jbc.M707419200 (2008).
4. Park, S. & Leppla, S. H. Optimized production and purification of Bacillus anthracis lethal factor. Protein Expr Purif 18, 293-302, doi:10.1006/prep.2000.1208 (2000). (Pubitemid 30213446)
5. Abi-Habib, R. J., Liu, S., Bugge, T. H., Leppla, S. H. & Frankel, A. E. A urokinaseactivated recombinant diphtheria toxin targeting the granulocyte-macrophage colony-stimulating factor receptor is selectively cytotoxic to human acute myeloid leukemia blasts. Blood 104, 2143-2148, doi:10.1182/blood-2004-01-0339 (2004). (Pubitemid 39297869)
6. Thrower, J. S., Hoffman, L., Rechsteiner, M. & Pickart, C. M. Recognition of the polyubiquitin proteolytic signal. EMBO J 19, 94-102, doi:10.1093/emboj/19.1.94 (2000). (Pubitemid 30009229)
7. Bachmair, A., Finley, D.&Varshavsky, A. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234, 179-186 (1986). (Pubitemid 17186094)
8. Varshavsky, A. The N-end rule pathway and regulation by proteolysis. Protein Sci doi:10.1002/pro.666 (2011).
9. Gupta, P. K., Moayeri, M., Crown, D., Fattah, R. J. & Leppla, S. H. Role of Nterminal amino acids in the potency of anthrax lethal factor. PLoS One 3, e3130, doi:10.1371/journal.pone.0003130 (2008).
10. Rayment, I. Reductive alkylation of lysine residues to alter crystallization properties of proteins. Methods Enzymol 276, 171-179 (1997). (Pubitemid 27085603)
11. Leysath, C. E. et al. Anthrax edema factor toxicity is strongly mediated by the Nend rule. PLoS One 8, e74474, doi:10.1371/journal.pone.0074474 (2013).
12. Hetzel, C., Bachran, C., Tur, M. K., Fuchs, H. & Stocker, M. Improved immunotoxins with novel functional elements. Curr Pharm Des 15, 2700-2711 (2009).
13. Bachran, C. et al. The saponin-mediated enhanced uptake of targeted saporinbased drugs is strongly dependent on the saponin structure. Exp Biol Med (Maywood) 231, 412-420 (2006).
14. Bachran, C., Heisler, I., Fuchs, H. & Sutherland, M. Influence of protein transduction domains on target-specific chimeric proteins. Biochem Biophys Res Commun 337, 602-609, doi:10.1016/j.bbrc.2005.09.095 (2005). (Pubitemid 41429327)
15. Weldon, J. E. et al. A protease-resistant immunotoxin against CD22 with greatly increased activity against CLL and diminished animal toxicity. Blood 113, 3792-3800, doi:10.1182/blood-2008-08-173195 (2009).
16. London, E. & Luongo, C. L. Domain-specific bias in arginine/lysine usage by protein toxins. Biochem Biophys Res Commun 160, 333-339 (1989). (Pubitemid 19116501)
17. Falnes, P. O., Ariansen, S., Sandvig, K. & Olsnes, S. Requirement for prolonged action in the cytosol for optimal protein synthesis inhibition by diphtheria toxin. J Biol Chem 275, 4363-4368 (2000). (Pubitemid 30094678)
18. Su, Y. et al. Systematic urokinase-activated anthrax toxin therapy produces regressions of subcutaneous human non-small cell lung tumor in athymic nude mice. Cancer Res 67, 3329-3336, doi:10.1158/0008-5472.CAN-06-4642 (2007). (Pubitemid 46724872)
19. Abi-Habib, R. J. et al. A urokinase-activated recombinant anthrax toxin is selectively cytotoxic to many human tumor cell types. Mol Cancer Ther 5, 2556-2562, doi:10.1158/1535-7163.MCT-06-0315 (2006). (Pubitemid 44650920)
20. Fan, Y. & Joachimiak, A. Enhanced crystal packing due to solvent reorganization through reductive methylation of lysine residues in oxidoreductase from Streptococcus pneumoniae. J Struct Funct Genomics 11, 101-111, doi:10.1007/s10969-010-9079-6 (2010).
21. Abraham, S. J., Kobayashi, T., Solaro, R. J. & Gaponenko, V. Differences in lysine pKa values may be used to improve NMR signal dispersion in reductively methylated proteins. J Biomol NMR 43, 239-246, doi:10.1007/s10858- 009-9306-2 (2009).
22. Taylor, I. A., Webb, M. & Kneale, G. G. Surface labelling of the type I methyltransferase M.EcoR124I reveals lysine residues critical for DNA binding. J Mol Biol 258, 62-73, doi:10.1006/jmbi.1996.0234 (1996).
23. Weng, A. et al. Enhancement of saporin cytotoxicity by Gypsophila saponins-more than stimulation of endocytosis. Chem Biol Interact 181, 424-429, doi:10.1016/j.cbi.2009.07.007 (2009).
24. Liu, W. et al. Recombinant immunotoxin engineered for low immunogenicity and antigenicity by identifying and silencing human B-cell epitopes. Proc Natl Acad Sci U S A 109, 11782-11787, doi:10.1073/pnas.1209292109 (2012).
25. Smallshaw, J. E. et al. Genetic engineering of an immunotoxin to eliminate pulmonary vascular leak in mice. Nat Biotechnol 21, 387-391, doi:10.1038/nbt800 (2003). (Pubitemid 36397658)
26. Thoren, K. L. & Krantz, B. A. The unfolding story of anthrax toxin translocation. Mol Microbiol 80, 588-595, doi:10.1111/j.1365-2958.2011.07614.x (2011).
27. Pentelute, B. L., Sharma, O. & Collier, R. J. Chemical dissection of protein translocation through the anthrax toxin pore. Angew Chem Int Ed Engl 50, 2294-2296, doi:10.1002/anie.201006460 (2011).
28. Milne, J. C., Blanke, S. R., Hanna, P. C. & Collier, R. J. Protective antigen-binding domain of anthrax lethal factor mediates translocation of a heterologous protein fused to its amino-or carboxy-terminus. Mol Microbiol 15, 661-666 (1995).
29. Arora, N. & Leppla, S. H. Fusions of anthrax toxin lethal factor with shiga toxin and diphtheria toxin enzymatic domains are toxic to mammalian cells. Infect Immun 62, 4955-4961 (1994). (Pubitemid 24332801)
30. Wesche, J., Elliott, J. L., Falnes, P. O., Olsnes, S. & Collier, R. J. Characterization of membrane translocation by anthrax protective antigen. Biochemistry 37, 15737-15746, doi:10.1021/bi981436i (1998). (Pubitemid 28524745)
31. Singh, Y., Klimpel, K. R., Arora, N., Sharma, M.&Leppla, S. H. The chymotrypsin sensitive site, FFD315, in anthrax toxin protective antigen is required for translocation of lethal factor. J Biol Chem 269, 29039-29046 (1994).
32. Liu, S., Leung, H. J. & Leppla, S. H. Characterization of the interaction between anthrax toxin and its cellular receptors. Cell Microbiol 9, 977-987, doi:10.1111/j.1462-5822.2006.00845.x (2007). (Pubitemid 46394908)
33. Bachran, C., Sutherland, M., Bachran, D. &Fuchs, H. Quantification of diphtheria toxin mediated ADP-ribosylation in a solid-phase assay. Clin Chem 53, 1676-1683, doi:10.1373/clinchem.2007.085365 (2007). (Pubitemid 47340065)
34. Newman, Z. L., Leppla, S. H.&Moayeri, M. CA-074Me protection against anthrax lethal toxin. Infect Immun 77, 4327-4336, doi:10.1128/IAI.00730-09 (2009).