The light chain defines the duration of action of botulinum toxin serotype a subtypes

mBio

Volumn 9, Issue 2, 2018, Pages

  Pellett, Sabine ^a   Bradshaw, Marite ^a   Tepp, William H ^a   Pier, Christina L ^a   Whitemarsh, Regina C M ^a   Chen, Chen ^b   Barbieri, Joseph T ^b   Johnson, Eric A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

BoNT; Botulinum neurotoxin; Duration of action; Hybrid toxin; Subtype

Indexed keywords

BOTULINUM TOXIN A; BOTULINUM TOXIN A1; BOTULINUM TOXIN A3; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; CELLULAR DISTRIBUTION; CHEMICAL BOND; CONTROLLED STUDY; DOSE RESPONSE; FEMALE; HUMAN; HUMAN CELL; LD50; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; SEROTYPE;

AMINO ACID SEQUENCE; ANIMALS; BOTULINUM TOXINS, TYPE A; FEMALE; HUMANS; MICE; MICE, INBRED ICR; SEROGROUP;

EID: 85046411664     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00089-18     Document Type: Article

References (56)

1. Peck MW, Smith TJ, Anniballi F, Austin JW, Bano L, Bradshaw M, Cuervo P, Cheng LW, Derman Y, Dorner BG, Fisher A, Hill KK, Kalb SR, Korkeala H, Lindström M, Lista F, Lúquez C, Mazuet C, Pirazzini M, Popoff MR, Rossetto O, Rummel A, Sesardic D, Singh BR, Stringer SC. 2017. Historical perspectives and guidelines for botulinum neurotoxin subtype nomenclature. Toxins 9:E38. https://doi.org/10.3390/toxins9010038.
2. Montecucco C, Rasotto MB. 2015. On botulinum neurotoxin variability. mBio 6:e02131-14. https://doi.org/10.1128/mBio.02131-14.
3. Pellett S, Tepp WH, Whitemarsh RC, Bradshaw M, Johnson EA. 2015. In vivo onset and duration of action varies for botulinum neurotoxin A subtypes 1-5. Toxicon 107:37-42. https://doi.org/10.1016/j.toxicon.2015.06.021.
4. Whitemarsh RC, Tepp WH, Johnson EA, Pellett S. 2014. Persistence of botulinum neurotoxin A subtypes 1-5 in primary rat spinal cord cells. PLoS One 9:e90252. https://doi.org/10.1371/journal.pone.0090252.
5. Pellett S, Tepp WH, Lin G, Johnson EA. 19 December 2017. Substrate cleavage and duration of action of botulinum neurotoxin type FA (“H, HA”). Toxicon https://doi.org/10.1016/j.toxicon.2017.12.048.
6. Tsai YC, Maditz R, Kuo CL, Fishman PS, Shoemaker CB, Oyler GA, Weissman AM. 2010. Targeting botulinum neurotoxin persistence by the ubiquitinproteasome system. Proc Natl Acad Sci U S A 107:16554-16559. https://doi.org/10.1073/pnas.1008302107.
7. Tsai YC, Kotiya A, Kiris E, Yang M, Bavari S, Tessarollo L, Oyler GA, Weissman AM. 2017. Deubiquitinating enzyme VCIP135 dictates the duration of botulinum neurotoxin type A intoxication. Proc Natl Acad Sci U S A 114:E5158-E5166. https://doi.org/10.1073/pnas.1621076114.
8. Fernández-Salas E, Ho H, Garay P, Steward LE, Aoki KR. 2004. Is the light chain subcellular localization an important factor in botulinum toxin duration of action? Mov Disord 19((Suppl 8)):S23-S34. https://doi.org/10.1002/mds.20006.
9. Fernández-Salas E, Steward LE, Ho H, Garay PE, Sun SW, Gilmore MA, Ordas JV, Wang J, Francis J, Aoki KR. 2004. Plasma membrane localization signals in the light chain of botulinum neurotoxin. Proc Natl Acad Sci U S A 101:3208-3213. https://doi.org/10.1073/pnas.0400229101.
10. 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. https://doi.org/10.1074/jbc.M111.224493.
11. Angaut-Petit D, Molgó J, Comella JX, Faille L, Tabti N. 1990. Terminal sprouting in mouse neuromuscular junctions poisoned with botulinum type A toxin: morphological and electrophysiological features. Neuroscience 37:799-808. https://doi.org/10.1016/0306-4522(90)90109-H.
12. Angaut-Petit D, Molgo J, Connold AL, Faille L. 1987. The levator auris longus muscle of the mouse: a convenient preparation for studies of short-and long-term presynaptic effects of drugs or toxins. Neurosci Lett 82:83-88. https://doi.org/10.1016/0304-3940(87)90175-3.
13. Comella JX, Molgo J, Faille L. 1993. Sprouting of mammalian motor nerve terminals induced by in vivo injection of botulinum type-D toxin and the functional recovery of paralysed neuromuscular junctions. Neurosci Lett 153:61-64. https://doi.org/10.1016/0304-3940(93)90077-X.
14. Juzans P, Comella JX, Molgo J, Faille L, Angaut-Petit D. 1996. Nerve terminal sprouting in botulinum type-A treated mouse levator auris longus muscle. Neuromuscul Disord 6:177-185. https://doi.org/10.1016/0960-8966(96) 00041-7.
15. de Paiva A, Meunier FA, Molgó J, Aoki KR, Dolly JO. 1999. Functional repair of motor endplates after botulinum neurotoxin type A poisoning:biphasic switch of synaptic activity between nerve sprouts and their parent terminals. Proc Natl Acad Sci U S A 96:3200-3205. https://doi.org/10.1073/pnas.96.6.3200.
16. Meunier FA, Schiavo G, Molgó J. 2002. Botulinum neurotoxins: from paralysis to recovery of functional neuromuscular transmission. J Physiol Paris 96:105-113. https://doi.org/10.1016/S0928-4257(01)00086-9.
17. Rummel A. 2013. Double receptor anchorage of botulinum neurotoxins accounts for their exquisite neurospecificity. Curr Top Microbiol Immunol 364:61-90.
18. Johnson EA, Montecucco C. 2008. Botulism, p 333-368. In Andrew GE (ed), Handbook of clinical neurology, vol 91. Elsevier BV, Amsterdam, The Netherlands.
19. Pirazzini M, Rossetto O, Eleopra R, Montecucco C. 2017. Botulinum neurotoxins: biology, pharmacology, and toxicology. Pharmacol Rev 69:200-235. https://doi.org/10.1124/pr.116.012658.
20. Fischer A, Montal M. 2007. Single molecule detection of intermediates during botulinum neurotoxin translocation across membranes. Proc Natl Acad Sci U S A 104:10447-10452. https://doi.org/10.1073/pnas.0700046104.
21. Fischer A, Nakai Y, Eubanks LM, Clancy CM, Tepp WH, Pellett S, Dickerson TJ, Johnson EA, Janda KD, Montal M. 2009. Bimodal modulation of the botulinum neurotoxin protein-conducting channel. Proc Natl Acad Sci U S A 106:1330-1335. https://doi.org/10.1073/pnas.0812839106.
22. Pirazzini M, Azarnia Tehran D, Zanetti G, Megighian A, Scorzeto M, Fillo S, Shone CC, Binz T, Rossetto O, Lista F, Montecucco C. 2014. Thioredoxin and its reductase are present on synaptic vesicles, and their inhibition prevents the paralysis induced by botulinum neurotoxins. Cell Rep 8:1870-1878. https://doi.org/10.1016/j.celrep.2014.08.017.
23. Zanetti G, Azarnia Tehran D, Pirazzini M, Binz T, Shone CC, Fillo S, Lista F, Rossetto O, Montecucco C. 2015. Inhibition of botulinum neurotoxins interchain disulfide bond reduction prevents the peripheral neuroparalysis of botulism. Biochem Pharmacol 98:522-530. https://doi.org/10.1016/j.bcp.2015.09.023.
24. Pirazzini M, Azarnia Tehran D, Zanetti G, Lista F, Binz T, Shone CC, Rossetto O, Montecucco C. 2015. The thioredoxin reductase-thioredoxin redox system cleaves the interchain disulphide bond of botulinum neurotoxins on the cytosolic surface of synaptic vesicles. Toxicon 107:32-36. https://doi.org/10.1016/j.toxicon.2015.06.019.
25. Lúquez C, Raphael BH, Joseph LA, Meno SR, Fernández RA, Maslanka SE. 2012. Genetic diversity among Clostridium botulinum strains harboring bont/A2 and bont/A3 genes. Appl Environ Microbiol 78:8712-8718. https://doi.org/10.1128/AEM.02428-12.
26. Arndt JW, Jacobson MJ, Abola EE, Forsyth CM, Tepp WH, Marks JD, Johnson EA, Stevens RC. 2006. A structural perspective of the sequence variability within botulinum neurotoxin subtypes A1-A4. J Mol Biol 362:733-742. https://doi.org/10.1016/j.jmb.2006.07.040.
27. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. https://doi.org/10.1016/ S0022-2836(05)80360-2.
28. Chen S, Kim JJ, Barbieri JT. 2007. Mechanism of substrate recognition by botulinum neurotoxin serotype A. J Biol Chem 282:9621-9627. https:// doi.org/10.1074/jbc.M611211200.
29. Whitemarsh RC, Tepp WH, Bradshaw M, Lin G, Pier CL, Scherf JM, Johnson EA, Pellett S. 2013. Characterization of botulinum neurotoxin A subtypes 1 through 5 by investigation of activities in mice, neuronal cell cultures, and in vitro. Infect Immun 81:3894-3902. https://doi.org/10.1128/IAI.00536-13.
30. Tepp WH, Lin G, Johnson EA. 2012. Purification and characterization of a novel subtype A3 botulinum neurotoxin. Appl Environ Microbiol 78:3108-3113. https://doi.org/10.1128/AEM.07967-11.
31. Henkel JS, Tepp WH, Przedpelski A, Fritz RB, Johnson EA, Barbieri JT. 2011. Subunit vaccine efficacy against botulinum neurotoxin subtypes. Vaccine 29:7688-7695. https://doi.org/10.1016/j.vaccine.2011.07.134.
32. Keller JE, Neale EA, Oyler G, Adler M. 1999. Persistence of botulinum neurotoxin action in cultured spinal cord cells. FEBS Lett 456:137-142. https://doi.org/10.1016/S0014-5793(99)00948-5.
33. Keller JE. 2006. Recovery from botulinum neurotoxin poisoning in vivo. Neuroscience 139:629-637. https://doi.org/10.1016/j.neuroscience.2005.12.029.
34. Scheps D, López de la Paz M, Jurk M, Hofmann F, Frevert J. 2017. Design of modified botulinum neurotoxin A1 variants with a shorter persistence of paralysis and duration of action. Toxicon 139:101-108. https://doi.org/ 10.1016/j.toxicon.2017.09.006.
35. Wang J, Zurawski TH, Meng J, Lawrence G, Olango WM, Finn DP, Wheeler L, Dolly JO. 2011. A dileucine in the protease of botulinum toxin A underlies its long-lived neuroparalysis: transfer of longevity to a novel potential therapeutic. J Biol Chem 286:6375-6385. https://doi.org/10.1074/jbc.M110.181784.
36. Toth S, Brueggmann EE, Oyler GA, Smith LA, Hines HB, Ahmed SA. 2012. Tyrosine phosphorylation of botulinum neurotoxin protease domains. Front Pharmacol 3:102. https://doi.org/10.3389/fphar.2012.00102.
37. Duregotti E, Zanetti G, Scorzeto M, Megighian A, Montecucco C, Pirazzini M, Rigoni M. 2015. Snake and spider toxins induce a rapid recovery of function of botulinum neurotoxin paralysed neuromuscular junction. Toxins 7:5322-5336. https://doi.org/10.3390/toxins7124887.
38. Dover N, Barash JR, Hill KK, Xie G, Arnon SS. 2014. Molecular character-ization of a novel botulinum neurotoxin type H gene. J Infect Dis 209:192-202. https://doi.org/10.1093/infdis/jit450.
39. Maslanka SE, Lúquez C, Dykes JK, Tepp WH, Pier CL, Pellett S, Raphael BH, Kalb SR, Barr JR, Rao A, Johnson EA. 2016. A novel botulinum neurotoxin, previously reported as serotype H, has a hybrid-like structure with regions of similarity to the structures of serotypes A and F and is neutralized with serotype A antitoxin. J Infect Dis 213:379-385. https:// doi.org/10.1093/infdis/jiv327.
40. Karalewitz AP, Kroken AR, Fu Z, Baldwin MR, Kim JJ, Barbieri JT. 2010. Identification of a unique ganglioside binding loop within botulinum neurotoxins C and D-SA. Biochemistry 49:8117-8126. https://doi.org/10.1021/bi100865f.
41. Hill KK, Smith TJ. 2013. Genetic diversity within Clostridium botulinum serotypes, botulinum neurotoxin gene clusters and toxin subtypes. Curr Top Microbiol Immunol 364:1-20.
42. Hill KK, Xie G, Foley BT, Smith TJ. 2015. Genetic diversity within the botulinum neurotoxin-producing bacteria and their neurotoxins. Toxicon 107:2-8. https://doi.org/10.1016/j.toxicon.2015.09.011.
43. Raphael BH, Choudoir MJ, Lúquez C, Fernández R, Maslanka SE. 2010. Sequence diversity of genes encoding botulinum neurotoxin type F. Appl Environ Microbiol 76:4805-4812. https://doi.org/10.1128/AEM.03109-09.
44. Heap JT, Pennington OJ, Cartman ST, Minton NP. 2009. A modular system for Clostridium shuttle plasmids. J Microbiol Methods 78:79-85. https://doi.org/10.1016/j.mimet.2009.05.004.
45. Bradshaw M, Tepp WH, Whitemarsh RC, Pellett S, Johnson EA. 2014. Holotoxin activity of botulinum neurotoxin subtype A4 originating from a nontoxigenic Clostridium botulinum expression system. Appl Environ Microbiol 80:7415-7422. https://doi.org/10.1128/AEM.01795-14.
46. Malizio CJ, Goodnough MC, Johnson EA. 2000. Purification of Clostridium botulinum type A neurotoxin. Methods Mol Biol 145:27-39. https://doi.org/10.1385/1-59259-052-7:27.
47. Pellett S, Tepp WH, Scherf JM, Pier CL, Johnson EA. 2015. Activity of botulinum neurotoxin type D (strain 1873) in human neurons. Toxicon 101:63-69. https://doi.org/10.1016/j.toxicon.2015.04.015.
48. Moberg LJ, Sugiyama H. 1978. Affinity chromatography purification of type A botulinum neurotoxin from crystalline toxic complex. Appl Environ Microbiol 35:878-880.
49. Whitemarsh RC, Strathman MJ, Chase LG, Stankewicz C, Tepp WH, Johnson EA, Pellett S. 2012. Novel application of human neurons derived from induced pluripotent stem cells for highly sensitive botulinum neurotoxin detection. Toxicol Sci 126:426-435. https://doi.org/10.1093/ toxsci/kfr354.
50. Pellett S, Tepp WH, Clancy CM, Borodic GE, Johnson EA. 2007. A neuronal cell-based botulinum neurotoxin assay for highly sensitive and specific detection of neutralizing serum antibodies. FEBS Lett 581:4803-4808. https://doi.org/10.1016/j.febslet.2007.08.078.
51. Pellett S, Tepp WH, Toth SI, Johnson EA. 2010. Comparison of the primary rat spinal cord cell (RSC) assay and the mouse bioassay for botulinum neurotoxin type A potency determination. J Pharmacol Toxicol Methods 61:304-310. https://doi.org/10.1016/j.vascn.2010.01.003.
52. Schantz E, Kautter DA. 1978. Standardized assay for Clostridium botulinum toxins. J Assoc Off Anal Chem 61:96-99.
53. Hatheway CL. 1988. Botulism, p 111-133. In Balows A, Hausler WH, Ohashi M, Turano MA (ed), Laboratory diagnosis of infectious diseases:principles and practice, vol 1. Springer-Verlag, New York, N.Y.
54. Blum FC, Przedpelski A, Tepp WH, Johnson EA, Barbieri JT. 2014. Entry of a recombinant, full-length, atoxic tetanus neurotoxin into Neuro-2a cells. Infect Immun 82:873-881. https://doi.org/10.1128/IAI.01539-13.
55. Simon NC, Barbieri JT. 2014. Exoenzyme S ADP-ribosylates Rab5 effector sites to uncouple intracellular trafficking. Infect Immun 82:21-28. https:// doi.org/10.1128/IAI.01059-13.
56. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M. 1992. The small GTPase Rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70:715-728. https://doi.org/10.1016/ 0092-8674(92)90306-W.