Tyrosine phosphorylation of botulinum neurotoxin protease domains

Frontiers in Pharmacology

Volumn 3 JUN, Issue , 2012, Pages

  Toth, Stephen ^a,d   Brueggmann, Ernst E ^a   Oyler, George A ^b   Smith, Leonard A ^c   Hines, Harry B ^a   Ahmed, S Ashraf ^a  

^a UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^b SYNAPTIC RESEARCH LLC   (United States)

^c Office of the Chief Scientist   (United States)

^d Mentor Biologics   (United States)

Author keywords

Botulinum neurotoxin; Clostridium botulinum; Protease; Protein phosphorylation; Tyrosine phosphorylation; Zinc endoporotease

Indexed keywords

BOTULINUM TOXIN; BOTULINUM TOXIN LCA; BOTULINUM TOXIN LCB; BOTULINUM TOXIN LCC1; BOTULINUM TOXIN LCD; BOTULINUM TOXIN LCE; BOTULINUM TOXIN LCG; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL SHEDDING; BINDING SITE; CATALYSIS; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME ACTIVE SITE; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; THERMOSTABILITY;

EID: 84866143737     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2012.00102     Document Type: Article

References (60)

1. Adler, M., Keller, J. E., Sheridan, R. E., and Deshpande, S. S. (2001). Persistence of botulinum neurotoxin A demonstrated by sequential administration of serotypes A and E in rat EDL muscle. Toxicon 39, 233-243.
2. Agarwal, R., Binz, T., and Swaminathan, S. (2005). Structural analysis of botulinum neurotoxin serotype F light chain: implications on substrate binding and inhibitor design. Biochemistry 44, 11758-11765.
3. Agarwal, R., Eswaramoorthy, S., Kumaran, D., Binz, T., and Swaminathan, S. (2004). Structural analysis of botulinum neurotoxin type E catalytic domain and its mutant Glu212s-Gln reveals the pivotal role of the Glu212 carboxylate in the catalytic pathway. Biochemistry 43, 6637-6644.
4. Agarwal, R., Schmidt, J. J., Stafford, R. G., and Swaminathan, S. (2009). Mode of VAMP substrate recognition and inhibition of Clostridium botulinum neurotoxin E Nat. Struct. Mol. Biol. 16, 789-794.
5. Ahmed, S. A., Byrne, M. P., Jensen, M., Hines, H. B., Brueggemann, E., and Smith, L. A. (2001). Enzymatic autocatalysis of botulinum A neurotoxin light chain. J. Protein Chem. 20, 221-231.
6. Ahmed, S. A., Ludivico, M. L., and Smith, L. A. (2004). Factors affecting autocatalysis of botulinum A neurotoxin light chain. Protein J. 23, 445-451.
7. Ahmed, S. A., McPhie, P., and Smith, L. A. (2003). Autocatalytically fragmented light chain of botulinum a neurotoxin is enzymatically active. Biochemistry 42, 12539-12549.
8. Ahmed, S. A., Olson, M. A., Ludivico, M. L., Gilsdorf, J., and Smith, L. A. (2008). Identification of residues surrounding the active site of type A botulinum neurotoxin important for substrate recognition and catalytic activity. Protein J. 27, 151-162.
9. Ahmed, S. A., and Smith, L. A. (2000). Light chain of botulinum A neurotoxin expressed as an inclusion body from a synthetic gene is catalytically and functionally active. J. Protein Chem. 19, 475-487.
10. Arndt, J. W., Chai, Q., Christian, T., and Stevens, R. C. (2006). Structure of botulinum neurotoxin type D light chain at 1.65 A resolution: repercussions for VAMP-2 substrate specificity. Biochemistry 45, 3255-3262.
11. Arndt, J. W., Yu, W., Bi, F., and Stevens, R. C. (2005). Crystal structure of botulinum neurotoxin type G light chain: serotype divergence in substrate recognition. Biochemistry 44, 9574-9580.
12. Arnon, S. S., Schechter, R., Inglesby, T. V., Henderson, D. A., Bartlett, J. G., Ascher, M. S., Eitzen, E., Fine, A. D., Hauer, J., Layton, M., Lillibridge, S., Osterholm, M. T., O'Toole, T., Parker, G., Perl, T. M., Russell, P. K., Swerdlow, D. L., and Tonat, K. (2001). Botulinum toxin as a biological weapon: medical and public health management. JAMA 285, 1059-1070.
13. Baldwin, M. R., Bradshaw, M., Johnson, E. A., and Barbieri, J. T. (2004). The C-terminus of botulinum neurotoxin type A light chain contributes to solubility, catalysis, and stability. Protein Expr. Purif. 37, 187-195.
14. Blanes-Mira, C., Ibanez, C., Fernandez-Ballester, G., Planells-Cases, R., Perez-Paya, E., and Ferrer-Montiel, A. (2001). Thermal stabilization of the catalytic domain of botulinum neurotoxin E by phosphorylation of a single tyrosine residue. Biochemistry 40, 2234-2242.
15. Burnett, J. C., Wang, C., Nuss, J. E., Nguyen, T. L., Hermone, A. R., Schmidt, J. J., Gussio, R., Wipf, P., and Bavari, S. (2009). Pharmacophore-guided lead optimization: the rational design of a non-zinc coordinating, sub-micromolar inhibitor of the botulinum neurotoxin serotype a metalloprotease. Bioorg. Med. Chem. Lett. 19, 5811-5813.
16. Capkova, K., Salzameda, N. T., and Janda, K. D. (2009). Investigations into small molecule non-peptidic inhibitors of the botulinum neurotoxins. Toxicon 54, 575-582.
17. Cochrane,R. C. (1947). "Biological warfare research in the United States," in History of the Chemical Warfare Service in World War II (01 July 1940-15 August 1945). Fort Detrick: Office of Chief, Chemical Corps.
18. Encinar, J. A., Fernandez, A., Ferragut, J. A., Gonzalez-Ros, J. M., Das-Gupta, B. R., Montal, M., and Ferrer-Montiel, A. (1998). Structural stabilization of botulinum neurotoxins by tyrosine phosphorylation. FEBS Lett. 429, 78-82.
19. Eswaramoorthy, S., Kumaran, D., and Swaminathan, S. (2002). A novel mechanism for Clostridium botulinum neurotoxin inhibition. Biochemistry 41, 9795-9802.
20. Ferrer-Montiel, A. V., Canaves, J. M., DasGupta, B. R., Wilson, M. C., and Montal, M. (1996). Tyrosine phosphorylation modulates the activity of clostridial neurotoxins. J. Biol. Chem. 271, 18322-18325.
21. Ferrer-Montiel, A. V., Gutierrez, L. M., Apland, J. P., Canaves, J. M., Gil, A., Viniegra, S., Biser, J. A., Adler, M., and Montal, M. (1998). The 26-mer peptide released from SNAP-25 cleavage by botulinum neurotoxin E inhibits vesicle docking. FEBS Lett. 435, 84-88.
22. Foran, P., Shone, C. C., and Dolly, J. O. (1994). Differences in the protease activities of tetanus and botulinum B toxins revealed by the cleavage of vesicle-associated membrane protein and various sized fragments. Biochemistry 33, 15365-15374.
23. Foran, P. G., Mohammed, N., Lisk, G. O., Nagwaney, S., Lawrence, G. W., Johnson, E., Smith, L., Aoki, K. R., and Dolly, J. O. (2003). Evaluation of the therapeutic usefulness of botulinum neurotoxin B, C1, E, and F compared with the long lasting type A. Basis for distinct durations of inhibition of exocytosis in central neurons. J. Biol. Chem. 278, 1363-1371.
24. Foster, L. J., Yeung, B., Mohtashami, M., Ross, K., Trimble, W. S., and Klip, A. (1998). Binary interactions of the SNARE proteins syntaxin-4, SNAP23, and VAMP-2 and their regulation by phosphorylation. Biochemistry 37, 11089-11096.
25. Gill, D. M. (1982). Bacterial toxins: a table of lethal amounts. Microbiol. Rev. 46, 86-94.
26. Gilsdorf, J., Gul, N., and Smith, L. A. (2006). Expression, purification, and characterization of Clostridium botulinum type B light chain. Protein Expr. Purif. 46, 256-267.
27. Hale, M., Oyler, G., Swaminathan, S., and Ahmed, S. A. (2011). Basic tetrapeptides as potent intracellular inhibitors of type A botulinum neurotoxin protease activity. J. Biol. Chem. 286, 1802-1811.
28. Hines, H. B., Kim, A. D., Stafford, R. G., Badie, S. S., Brueggeman, E. E., Newman, D. J., and Schmidt, J. J. (2008). Use of a recombinant fluorescent substrate with cleavage sites for all botulinum neurotoxins in high-throughput screening of natural product extracts for inhibitors of serotypes A, B, and E. Appl. Environ. Microbiol. 74, 653-659.
29. Ibanez, C., Blanes-Mira, C., Fernandez-Ballester, G., Planells-Cases, R., and Ferrer-Montiel, A. (2004). Modulation of botulinum neurotoxin A catalytic domain stability by tyrosine phosphorylation. FEBS Lett. 578, 121-127.
30. Jensen, M. J., Smith, T. J., Ahmed, S. A., and Smith, L. A. (2003). Expression, purification, and efficacy of the type A botulinum neurotoxin catalytic domain fused to two translocation domain variants. Toxicon 41, 691-701.
31. Jin, R., Sikorra, S., Stegmann, C. M., Pich, A., Binz, T., and Brunger, A. T. (2007). Structural and biochemical studies of botulinum neurotoxin serotype C1 light chain protease: implications for dual substrate specificity. Biochemistry 46, 10685-10693.
32. Keller, J. E., Neale, E. A., Oyler, G., and Adler, M. (1999). Persistence of botulinum neurotoxin action in cultured spinal cord cells. FEBS Lett. 456, 137-142.
33. Kumaran, D., Rawat, R., Ludivico, M. L., Ahmed, S. A., and Swaminathan, S. (2008). Structure-and substrate-based inhibitor design for Clostridium botulinum neurotoxin serotype A. J. Biol. Chem. 283,18883-18891.
34. Kumaran, D., Rawat, R., Ahmed, S. A., and Swaminathan, S. (2008). Substrate binding mode and its implication on drug design for botulinum neurotoxin A. PLoS Pathog. 4, e1000165. doi:10.1371/journal.ppat.1000165
35. Lacy, D. B., Tepp, W., Cohen, A. C., DasGupta, B. R., and Stevens, R. C. (1998). Crystal structure of botulinum neurotoxin type A and implications for toxicity. Nat. Struct. Biol. 5, 898-902.
36. Li, Y., Dowbenko, D., and Lasky, L. A. (2002). AKT/PKB phosphorylation of p21Cip/WAF1 enhances protein stability of p21Cip/WAF1 and promotes cell survival. J. Biol. Chem. 277, 11352-11361.
37. Ludivico, M., Smith, L. A., and Ahmed, S. A. (2009). Structure-based design of peptide inhibitors of botulinum neurotoxin serotypes A proteolytic activity. Botulinum J. 1, 297-308.
38. Montecucco, C., andSchiavo, G. (1995). Structure and function of tetanus and botulinum neurotoxins. Q. Rev. Biophys. 28, 423-472.
39. Munton, R. P., Tweedie-Cullen, R., Livingstone-Zatchej, M., Weinandy, F., Waidelich, M., Longo, D., Gehrig, P., Potthast, F., Rutishauser, D., Gerrits, B., Panse, C., Schlapbach, R., and Mansuy, I. M. (2007). Qualitative and quantitative analyses of protein phosphorylation in naive and stimulated mouse synaptosomal preparations. Mol. Cell Proteomics 6, 283-293.
40. Nagy, G., Reim, K., Matti, U., Brose, N., Binz, T., Rettig, J., Neher, E., and Sorensen, J. B. (2004). Regulation of releasable vesicle pool sizes by protein kinase A-dependent phosphorylation of SNAP-25. Neuron 41, 417-429.
41. Nielander, H. B., Onofri, F., Valtorta, F., Schiavo, G., Montecucco, C., Greengard, P., and Benfenati, F. (1995). Phosphorylation of VAMP/synaptobrevin in synaptic vesicles by endogenous protein kinases. J. Neurochem. 65, 1712-1720.
42. Pang, Y. P., Vummenthala, A., Mishra, R. K., Park, J. G., Wang, S., Davis, J., Millard, C. B., and Schmidt, J. J. (2009). Potent new small-molecule inhibitor of botulinum neuro toxin serotype A endopeptidase developed by synthesis-based computer-aided molecular design. PLoS ONE 4, e7730. doi:10.1371/journal.pone.0007730
43. Patwardhan, P., and Miller, W T. (2007). Processive phosphorylation: mechanism and biological importance. Cell. Signal. 19, 2218-2226.
44. Rawat, R., Ahmed, S. A., and Swaminathan, S. (2008). High level expression of the light chain of botulinum neurotoxin serotype C1 and an efficient HPLC assay to monitor its proteolytic activity. Protein Expr. Purif. 60, 165-169.
45. Rowe, B., Schmidt, J. J., Smith, L. A., and Ahmed, S. A. (2010). Rapid product analysis and increased sensitivity for quantitative determinations of botulinum neurotoxin pro-teolytic activity. Anal. Biochem. 396, 188-193.
46. Schiavo, G., Rossetto, O., Catsicas, S., Polverino de Laureto, P., Das-Gupta, B. R., Benfenati, F., and Montecucco, C. (1993). Identification of the nerve terminal targets of botulinum neurotoxin serotypes A, D, and E. J. Biol. Chem. 268, 23784-23787.
47. Schiavo, G., Rossetto, O., Santucci, A., DasGupta, B. R., and Montecucco, C. (1992). Botulinum neurotoxins are zinc proteins. J. Biol Chem. 267, 23479-23483.
48. Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., Polverino de Laureto, P., DasGupta, B. R., and Montecucco, C. (1992). Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832-835.
49. Schmidt, J. J., and Stafford, R. G. (2002). A high-affinity competitive inhibitor of type A botulinum neurotoxin protease activity. FEBS Lett. 532, 423-426.
50. Schmidt, J. J., and Stafford, R. G. (2005). Botulinum neurotoxin serotype F: identification of substrate recognition requirements and development of inhibitors with low nanomolar affinity. Biochemistry 44, 4067-4073.
51. Segelke, B., Knapp, M., Kadkhodayan, S., Balhorn, R., and Rupp, B. (2004). Crystal structure of Clostridium botulinum neurotoxin protease in a product-bound state: evidence for noncanonical zinc protease activity. Proc. Natl. Acad. Sci. U.S.A. 101, 6888-6893.
52. Silhar, P., Capkova, K., Salzameda, N. T., Barbieri, J. T., Hixon, M. S., and Janda, K. D. (2010). Botulinum neurotoxin A protease: discovery of natural product exosite inhibitors. J. Am. Chem. Soc. 132, 2868-2869.
53. Simpson, L. L. (2004). Identification of the major steps in botulinum toxin action. Annu. Rev. Pharmacol. Toxicol. 44, 167-193.
54. Simpson, L. L., Maksymowych, A. B., Park, J. B., and Bora, R. S. (2004). The role of the interchain disulfide bond in governing the pharmacological actions of botulinum toxin. J. Pharmacol. Exp. Ther. 308, 857-864.
55. Souayah, N., Karim, H., Kamin, S. S., McArdle, J., and Marcus, S. (2006). Severe botulism after focal injection of botulinum toxin. Neurology 67, 1855-1856.
56. Swaminathan, S., Eswaramoorthy, S., and Kumaran, D. (2004). Structure and enzymatic activity of botulinum neurotoxins. Mov. Disord. 19(Suppl. 8), S17-S22.
57. Toth, S. I., Smith, L. A., and Ahmed, S. A. (2009). Extreme sensitivity of botulinum neurotoxin domains towards mild agitation. J. Pharm. Sci. 98, 3302-3311.
58. Walsh, C. T. (2006). Posttranslational Modification of Proteins, 1st Edn. Englewood, CO: Roberts and Company Publishers.
59. Walsh, C. T. (2006). Posttranslational Modification of Proteins: Expanding Nature's Inventory, 1st Edn. Edge-wood, CO: Roberts and Company Publishers.
60. Zuniga, J. E., Schmidt, J. J., Fenn, T., Burnett, J. C., Arac, D., Gussio, R., Stafford, R. G., Badie, S. S., Bavari, S., and Brunger, A. T. (2008). A potent peptidomimetic inhibitor of botulinum neurotoxin serotype A has a very different conformation than SNAP-25 substrate. Structure 16, 1588-1597.