Glycine insertion at protease cleavage site of SNAP25 resists cleavage but enhances affinity for botulinum neurotoxin serotype A

Protein Science

Volumn 21, Issue 3, 2012, Pages 318-326

  Ho, Mengfei ^a   Goh, Cheong Hian ^a   Brothers, Michael C ^b   Wang, Shihua ^a,c   Young, Ryan L ^a   Ou, Yuxiang ^a   Lui, Juliana Nga Man ^a   Kalafatis, Marinos ^a   Lan, Xiuwan ^a,d   Wolf, Abigail E ^a   Rienstra, Chad M ^b   Wilson, Brenda A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^d GUANGXI MEDICAL UNIVERSITY   (China)

Author keywords

BoNT; Induced fit; Pseudosubstrate; YsCsY; Zn protease

Indexed keywords

BOTULINUM TOXIN A; E 5531; GLYCINE; HISTIDINE; PROTEIN SNAP25; PROTEINASE; SNARE PROTEIN; UNCLASSIFIED DRUG; ZINC;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; SINGLE POINT MUTATION;

BINDING SITES; BOTULINUM TOXINS, TYPE A; CATALYTIC DOMAIN; GLYCINE; MODELS, MOLECULAR; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

EID: 84863167974     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2017     Document Type: Article

References (33)

1. Arnon SS, Schechter R, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Hauer J, Layton M, Lillibridge S, Osterholm MT, O'Toole T, Parker G, Perl TM, Russell PK, Swerdlow DL, Tonat K (2001) Botulinum toxin as a biological weapon: medical and public health management. JAMA 285: 1059-1070. (Pubitemid 32176420)
2. Schiavo G, Matteoli M, Montecucco C (2000) Neurotoxins affecting neuroexocytosis. Physiol Rev 80: 717-766. (Pubitemid 30164948)
3. Lacy DB, Stevens RC (1998) Unraveling the structures and modes of action of bacterial toxins. Curr Opin Struct Biol 8: 778-784. (Pubitemid 29004676)
4. Lacy DB, Tepp W, Cohen AC, DasGupta BR, Stevens RC (1998) Crystal structure of botulinum neurotoxin type A and implications for toxicity. Nat Struct Biol 5: 898-902. (Pubitemid 28467413)
5. Montecucco C, Molgo J (2005) Botulinal neurotoxins: revival of an old killer. Curr Opin Pharmacol 5: 274-279. (Pubitemid 40674251)
6. Montal M (2010) Botulinum neurotoxin: a marvel of protein design. Ann Rev Biochem 79: 591-617.
7. Foran PG, Davletov B, Meunier FA (2003) Getting muscles moving again after botulinum toxin: novel therapeutic challenges. Trends Mol Med 9: 291-299. (Pubitemid 37039963)
8. Chertow DS, Tan ET, Maslanka SE, Schulte J, Bresnitz EA, Weisman RS, Bernstein J, Marcus SM, Kumar S, Malecki J, Sobel J, Braden CR (2006) Botulism in 4 adults following cosmetic injections with an unlicensed, highly concentrated botulinum preparation. JAMA 296: 2476-2479. (Pubitemid 44791204)
9. Hakami RM, Ruthel G, Stahl AM, Bavari S (2010) Gaining ground: assays for therapeutics against botulinum neurotoxin. Trends Microbiol 18: 164-172.
10. Goodnough MC, Oyler G, Fishman PS, Johnson EA, Neale EA, Keller JE, Tepp WH, Clark M, Hartz S, Adler M (2002) Development of a delivery vehicle for intracellular transport of botulinum neurotoxin antagonists. FEBS Lett 513: 163-168. (Pubitemid 34251257)
11. Ho M, Chang LH, Pires-Alves M, Thyagarajan B, Bloom JE, Gu Z, Aberle KK, Teymorian SA, Bannai Y, Johnson SC, McArdle JJ, Wilson BA (2011) Recombinant botulinum neurotoxin A heavy chain-based delivery vehicles for neuronal cell targeting. Protein Eng Des Sel 24: 247-253.
12. Tsai YC, Maditz R, Kuo CL, Fishman PS, Shoemaker CB, Oyler GA, Weissman AM (2010) Targeting botulinum neurotoxin persistence by the ubiquitin-proteasome system. Proc Natl Acad Sci USA 107: 16554-16559.
13. Kuo CL, Oyler GA, Shoemaker CB (2011) Accelerated neuronal cell recovery from botulinum neurotoxin intoxication by targeted ubiquitination. PLoS One 6: e20352.
14. Rubinsztein DC (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443: 780-786.
15. Chen S, Barbieri JT (2011) Association of botulinum neurotoxin serotype A light chain with plasma membrane-bound SNAP-25. J Biol Chem 286: 15067-15072.
16. Washbourne P, Pellizzari R, Baldini G, Wilson MC, Montecucco C (1997) Botulinum neurotoxin types A and E require the SNARE motif in SNAP-25 for proteolysis. FEBS Lett 4189(1-2):1-5. (Pubitemid 27514402)
17. Breidenbach MA, Brunger AT (2004) Substrate recognition strategy for botulinum neurotoxin serotype A. Nature 432: 925-929. (Pubitemid 40037157)
18. Brunger AT, Breidenbach MA, Jin R, Fischer A, Santos JS, Montal M (2007) Botulinum neurotoxin heavy chain belt as an intramolecular chaperone for the light chain. PLoS Pathog 3: 1191-1194. (Pubitemid 47510272)
19. Silvaggi NR, Wilson D, Tzipori S, Allen KN (2008) Catalytic features of the botulinum neurotoxin A light chain revealed by high resolution structure of an inhibitory peptide complex. Biochemistry 47: 5736-5745. (Pubitemid 351747052)
20. Schmidt JJ, Stafford RG, Bostian KA (1998) Type A botulinum neurotoxin proteolytic activity: development of competitive inhibitors and implications for substrate specificity at the S1' binding subsite. FEBS Lett 435: 61-64. (Pubitemid 28432015)
21. Hale M, Oyler G, Swaminathan S, Ahmed SA (2011) Basic tetrapeptides as potent intracellular inhibitors of type A botulinum neurotoxin protease activity. J Biol Chem 286: 1802-1811.
22. Zuniga JE, Schmidt JJ, Fenn T, Burnett JC, Arac D, Gussio R, Stafford RG, Badie SS, Bavari S, Brunger AT (2008) A potent peptidomimetic inhibitor of botulinum neurotoxin serotype A has a very different conformation than SNAP-25 substrate. Structure 16: 1588-1597.
23. Pires-Alves M, Ho M, Aberle KK, Janda KD, Wilson BA (2009) Tandem fluorescent proteins as enhanced FRET-based substrates for botulinum neurotoxin activity. Toxicon 53: 392-399.
24. O'Sullivan GA, Mohammed N, Foran PG, Lawrence GW, Oliver Dolly J (1999) Rescue of exocytosis in botulinum toxin A-poisoned chromaffin cells by expression of cleavage-resistant SNAP-25. Identification of the minimal essential C-terminal residues. J Biol Chem 274: 36897-36904.
25. Chen S, Barbieri JT (2006) Unique substrate recognition by botulinum neurotoxins serotypes A and E. J Biol Chem 281: 10906-10911. (Pubitemid 43855514)
26. Raghunath A, Perez-Branguli F, Smith L, Dolly JO (2008) Adeno-associated virus transfer of a gene encoding SNAP-25 resistant to botulinum toxin A attenuates neuromuscular paralysis associated with botulism. J Neurosci 28: 3683-3688.
27. Kumaran D, Rawat R, Ahmed SA, Swaminathan S (2008) Substrate binding mode and its implication on drug design for botulinum neurotoxin A. PLoS Pathog 4: e1000165.
28. Kumaran D, Rawat R, Ludivico ML, Ahmed SA, Swaminathan S (2008) Structure- and substrate-based inhibitor design for Clostridium botulinum neurotoxin serotype A. J Biol Chem 283: 18883-18891.
29. Chen S, Kim JJ, Barbieri JT (2007) Mechanism of substrate recognition by botulinum neurotoxin serotype A. J Biol Chem 282: 9621-9627. (Pubitemid 47104595)
30. Silvaggi NR, Boldt GE, Hixon MS, Kennedy JP, Tzipori S, Janda KD, Allen KN (2007) Structures of Clostridium botulinum neurotoxin serotype A light chain complexed with small-molecule inhibitors highlight activesite flexibility. Chem Biol 14: 533-542. (Pubitemid 46765150)
31. Sali A, Blundell TL (1993) Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234: 779-815. (Pubitemid 24007801)
32. Marti-Renom MA, Stuart A, Fiser A, Sanchez R, Melo F, Sali A (2000) Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29: 291-325. (Pubitemid 30599596)
33. Shen MY, Sali A (2006) Statistical potential for assessment and prediction of protein structures. Prot Sci 15: 2507-2524.