Interneuronal Transfer and Distal Action of Tetanus Toxin and Botulinum Neurotoxins A and D in Central Neurons

Cell Reports

Volumn 16, Issue 7, 2016, Pages 1974-1987

  Bomba Warczak, Ewa ^a   Vevea, Jason D ^a   Brittain, Joel M ^a   Figueroa Bernier, Annette ^a   Tepp, William H ^b   Johnson, Eric A ^b   Yeh, Felix L ^c   Chapman, Edwin R ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOTULINUM TOXIN; BOTULINUM TOXIN A; BOTULINUM TOXIN D; TETANUS TOXIN; UNCLASSIFIED DRUG; BOTULINUM TOXIN TYPE D; FLUORESCENT DYE;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL ORGANELLE; CONTROLLED STUDY; HIPPOCAMPUS; MICROFLUIDICS; MOUSE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSCYTOSIS; ANIMAL; CELL COMMUNICATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; LAB ON A CHIP; METABOLISM; NERVE CELL; PRIMARY CELL CULTURE; PROTEIN TRANSPORT;

ANIMALS; BOTULINUM TOXINS; BOTULINUM TOXINS, TYPE A; CELL COMMUNICATION; FLUORESCENT DYES; HIPPOCAMPUS; LAB-ON-A-CHIP DEVICES; MICE; NEURONS; PRIMARY CELL CULTURE; PROTEIN TRANSPORT; RATS; TETANUS TOXIN;

EID: 84997724606     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.06.104     Document Type: Article

References (71)

1. Abbruzzese, G., Berardelli, A., Neurophysiological effects of botulinum toxin type A. Neurotox. Res. 9 (2006), 109–114.
2. Antonucci, F., Rossi, C., Gianfranceschi, L., Rossetto, O., Caleo, M., Long-distance retrograde effects of botulinum neurotoxin A. J. Neurosci. 28 (2008), 3689–3696.
3. Aymard, C., Giboin, L.S., Lackmy-Vallée, A., Marchand-Pauvert, V., Spinal plasticity in stroke patients after botulinum neurotoxin A injection in ankle plantar flexors. Physiol. Rep., 1, 2013, e00173.
4. Bajjalieh, S.M., Frantz, G.D., Weimann, J.M., McConnell, S.K., Scheller, R.H., Differential expression of synaptic vesicle protein 2 (SV2) isoforms. J. Neurosci. 14 (1994), 5223–5235.
5. Benoit, R.M., Frey, D., Hilbert, M., Kevenaar, J.T., Wieser, M.M., Stirnimann, C.U., McMillan, D., Ceska, T., Lebon, F., Jaussi, R., et al. Structural basis for recognition of synaptic vesicle protein 2C by botulinum neurotoxin A. Nature 505 (2014), 108–111.
6. Berardelli, A., Curra, A., Effects of botulinum toxin type A on central nervous system function. Naunyn Schmiedebergs Arch. Pharmacol., 365, 2002, R50.
7. Bercsenyi, K., Schmieg, N., Bryson, J.B., Wallace, M., Caccin, P., Golding, M., Zanotti, G., Greensmith, L., Nischt, R., Schiavo, G., Tetanus toxin entry. Nidogens are therapeutic targets for the prevention of tetanus. Science 346 (2014), 1118–1123.
8. Björnstad, K., Tevell Åberg, A., Kalb, S.R., Wang, D., Barr, J.R., Bondesson, U., Hedeland, M., Validation of the Endopep-MS method for qualitative detection of active botulinum neurotoxins in human and chicken serum. Anal. Bioanal. Chem. 406 (2014), 7149–7161.
9. Boroojerdi, B., Cohen, L.G., Hallett, M., Effects of botulinum toxin on motor system excitability in patients with writer's cramp. Neurology 61 (2003), 1546–1550.
10. Caleo, M., Antonucci, F., Restani, L., Mazzocchio, R., A reappraisal of the central effects of botulinum neurotoxin type A: by what mechanism?. J. Neurochem. 109 (2009), 15–24.
11. Ceballos-Baumann, A.O., Sheean, G., Passingham, R.E., Marsden, C.D., Brooks, D.J., Botulinum toxin does not reverse the cortical dysfunction associated with writer's cramp. A PET study. Brain 120 (1997), 571–582.
12. Currà, A., Trompetto, C., Abbruzzese, G., Berardelli, A., Central effects of botulinum toxin type A: evidence and supposition. Mov. Disord. 19:Suppl 8 (2004), S60–S64.
13. Curtis, D.R., De Groat, W.C., Tetanus toxin and spinal inhibition. Brain Res. 10 (1968), 208–212.
14. David, A.T., Saied, A., Charles, A., Subramanian, R., Chouljenko, V.N., Kousoulas, K.G., A herpes simplex virus 1 (McKrae) mutant lacking the glycoprotein K gene is unable to infect via neuronal axons and egress from neuronal cell bodies. mBio, 3, 2012 e00144–e12.
15. de Maio, M., Therapeutic uses of botulinum toxin: from facial palsy to autonomic disorders. Expert Opin. Biol. Ther. 8 (2008), 791–798.
16. Deinhardt, K., Salinas, S., Verastegui, C., Watson, R., Worth, D., Hanrahan, S., Bucci, C., Schiavo, G., Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52 (2006), 293–305.
17. Deinhardt, K., Reversi, A., Berninghausen, O., Hopkins, C.R., Schiavo, G., Neurotrophins Redirect p75NTR from a clathrin-independent to a clathrin-dependent endocytic pathway coupled to axonal transport. Traffic 8 (2007), 1736–1749.
18. Dong, M., Richards, D.A., Goodnough, M.C., Tepp, W.H., Johnson, E.A., Chapman, E.R., Synaptotagmins I and II mediate entry of botulinum neurotoxin B into cells. J. Cell Biol. 162 (2003), 1293–1303.
19. Dong, M., Yeh, F., Tepp, W.H., Dean, C., Johnson, E.A., Janz, R., Chapman, E.R., SV2 is the protein receptor for botulinum neurotoxin A. Science 312 (2006), 592–596.
20. Dong, M., Liu, H., Tepp, W.H., Johnson, E.A., Janz, R., Chapman, E.R., Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin E into neurons. Mol. Biol. Cell 19 (2008), 5226–5237.
21. Erdmann, G., Hanauske, A., Wellhöner, H.H., Intraspinal distribution and reaction in the grey matter with tetanus toxin of intracisternally injected anti-tetanus toxoid F(ab’)2 fragments. Brain Res. 211 (1981), 367–377.
22. Fischer, A., Synchronized chaperone function of botulinum neurotoxin domains mediates light chain translocation into neurons. Curr. Top. Microbiol. Immunol. 364 (2013), 115–137.
23. Foster, L., Clapp, L., Erickson, M., Jabbari, B., Botulinum toxin A and chronic low back pain: a randomized, double-blind study. Neurology 56 (2001), 1290–1293.
24. Fu, F.N., Busath, D.D., Singh, B.R., Spectroscopic analysis of low pH and lipid-induced structural changes in type A botulinum neurotoxin relevant to membrane channel formation and translocation. Biophys. Chem. 99 (2002), 17–29.
25. Fu, Z., Chen, C., Barbieri, J.T., Kim, J.J.P., Baldwin, M.R., Glycosylated SV2 and gangliosides as dual receptors for botulinum neurotoxin serotype F. Biochemistry 48 (2009), 5631–5641.
26. Galloux, M., Vitrac, H., Montagner, C., Raffestin, S., Popoff, M.R., Chenal, A., Forge, V., Gillet, D., Membrane Interaction of botulinum neurotoxin A translocation (T) domain. The belt region is a regulatory loop for membrane interaction. J. Biol. Chem. 283 (2008), 27668–27676.
27. Giladi, N., The mechanism of action of botulinum toxin type A in focal dystonia is most probably through its dual effect on efferent (motor) and afferent pathways at the injected site. J. Neurol. Sci. 152 (1997), 132–135.
28. Gilio, F., Currà, A., Lorenzano, C., Modugno, N., Manfredi, M., Berardelli, A., Effects of botulinum toxin type A on intracortical inhibition in patients with dystonia. Ann. Neurol. 48 (2000), 20–26.
29. Gill, D.M., Bacterial toxins: a table of lethal amounts. Microbiol. Rev. 46 (1982), 86–94.
30. Jacky, B.P., Garay, P.E., Dupuy, J., Nelson, J.B., Cai, B., Molina, Y., Wang, J., Steward, L.E., Broide, R.S., Francis, J., et al. Identification of fibroblast growth factor receptor 3 (FGFR3) as a protein receptor for botulinum neurotoxin serotype A (BoNT/A). PLoS Pathog., 9, 2013, e1003369.
31. Jahn, R., Niemann, H., Molecular mechanisms of clostridial neurotoxins. Ann. N Y Acad. Sci. 733 (1994), 245–255.
32. Jankovic, J., Botulinum toxin in movement disorders. Curr. Opin. Neurol. 7 (1994), 358–366.
33. Janz, R., Südhof, T.C., SV2C is a synaptic vesicle protein with an unusually restricted localization: anatomy of a synaptic vesicle protein family. Neuroscience 94 (1999), 1279–1290.
34. Kalb, S.R., Lou, J., Garcia-Rodriguez, C., Geren, I.N., Smith, T.J., Moura, H., Marks, J.D., Smith, L.A., Pirkle, J.L., Barr, J.R., Extraction and inhibition of enzymatic activity of botulinum neurotoxins/A1, /A2, and /A3 by a panel of monoclonal anti-BoNT/A antibodies. PLoS ONE, 4, 2009, e5355.
35. Lalli, G., Schiavo, G., Analysis of retrograde transport in motor neurons reveals common endocytic carriers for tetanus toxin and neurotrophin receptor p75NTR. J. Cell Biol. 156 (2002), 233–239.
36. Lawrence, G.W., Ovsepian, S.V., Wang, J., Aoki, K.R., Dolly, J.O., Extravesicular intraneuronal migration of internalized botulinum neurotoxins without detectable inhibition of distal neurotransmission. Biochem. J. 441 (2012), 443–452.
37. Mahrhold, S., Rummel, A., Bigalke, H., Davletov, B., Binz, T., The synaptic vesicle protein 2C mediates the uptake of botulinum neurotoxin A into phrenic nerves. FEBS Lett. 580 (2006), 2011–2014.
38. Mahrhold, S., Strotmeier, J., Garcia-Rodriguez, C., Lou, J., Marks, J.D., Rummel, A., Binz, T., Identification of the SV2 protein receptor-binding site of botulinum neurotoxin type E. Biochem. J. 453 (2013), 37–47.
39. Marchand-Pauvert, V., Aymard, C., Giboin, L.S., Dominici, F., Rossi, A., Mazzocchio, R., Beyond muscular effects: depression of spinal recurrent inhibition after botulinum neurotoxin A. J. Physiol. 591 (2013), 1017–1029.
40. Montal, M., Botulinum neurotoxin: a marvel of protein design. Annu. Rev. Biochem. 79 (2010), 591–617.
41. Montecucco, C., Schiavo, G., Structure and function of tetanus and botulinum neurotoxins. Q. Rev. Biophys. 28 (1995), 423–472.
42. Nishiki, T., Kamata, Y., Nemoto, Y., Omori, A., Ito, T., Takahashi, M., Kozaki, S., Identification of protein receptor for Clostridium botulinum type B neurotoxin in rat brain synaptosomes. J. Biol. Chem. 269 (1994), 10498–10503.
43. Peng, L., Tepp, W.H., Johnson, E.A., Dong, M., Botulinum neurotoxin D uses synaptic vesicle protein SV2 and gangliosides as receptors. PLoS Pathog., 7, 2011, e1002008.
44. Peng, L., Berntsson, R.P., Tepp, W.H., Pitkin, R.M., Johnson, E.A., Stenmark, P., Dong, M., Botulinum neurotoxin D-C uses synaptotagmin I and II as receptors, and human synaptotagmin II is not an effective receptor for type B, D-C and G toxins. J. Cell Sci. 125 (2012), 3233–3242.
45. Pirazzini, M., Henke, T., Rossetto, O., Mahrhold, S., Krez, N., Rummel, A., Montecucco, C., Binz, T., Neutralisation of specific surface carboxylates speeds up translocation of botulinum neurotoxin type B enzymatic domain. FEBS Lett. 587 (2013), 3831–3836.
46. Popoff, M.R., Bouvet, P., Genetic characteristics of toxigenic Clostridia and toxin gene evolution. Toxicon 75 (2013), 63–89.
47. Priori, A., Berardelli, A., Mercuri, B., Manfredi, M., Physiological effects produced by botulinum toxin treatment of upper limb dystonia. Changes in reciprocal inhibition between forearm muscles. Brain 118 (1995), 801–807.
48. Puhar, A., Johnson, E.A., Rossetto, O., Montecucco, C., Comparison of the pH-induced conformational change of different clostridial neurotoxins. Biochem. Biophys. Res. Commun. 319 (2004), 66–71.
49. Restani, L., Antonucci, F., Gianfranceschi, L., Rossi, C., Rossetto, O., Caleo, M., Evidence for anterograde transport and transcytosis of botulinum neurotoxin A (BoNT/A). J. Neurosci. 31 (2011), 15650–15659.
50. Restani, L., Giribaldi, F., Manich, M., Bercsenyi, K., Menendez, G., Rossetto, O., Caleo, M., Schiavo, G., Botulinum neurotoxins A and E undergo retrograde axonal transport in primary motor neurons. PLoS Pathog., 8, 2012, e1003087.
51. Restani, L., Novelli, E., Bottari, D., Leone, P., Barone, I., Galli-Resta, L., Strettoi, E., Caleo, M., Botulinum neurotoxin A impairs neurotransmission following retrograde transynaptic transport. Traffic 13 (2012), 1083–1089.
52. Rossetto, O., Pirazzini, M., Montecucco, C., Botulinum neurotoxins: genetic, structural and mechanistic insights. Nat. Rev. Microbiol. 12 (2014), 535–549.
53. Rothman, J.E., Intracellular membrane fusion. Adv. Second Messenger Phosphoprotein Res. 29 (1994), 81–96.
54. Rummel, A., Eichner, T., Weil, T., Karnath, T., Gutcaits, A., Mahrhold, S., Sandhoff, K., Proia, R.L., Acharya, K.R., Bigalke, H., Binz, T., Identification of the protein receptor binding site of botulinum neurotoxins B and G proves the double-receptor concept. Proc. Natl. Acad. Sci. USA 104 (2007), 359–364.
55. Rummel, A., Häfner, K., Mahrhold, S., Darashchonak, N., Holt, M., Jahn, R., Beermann, S., Karnath, T., Bigalke, H., Binz, T., Botulinum neurotoxins C, E and F bind gangliosides via a conserved binding site prior to stimulation-dependent uptake with botulinum neurotoxin F utilising the three isoforms of SV2 as second receptor. J. Neurochem. 110 (2009), 1942–1954.
56. Salinas, S., Bilsland, L.G., Henaff, D., Weston, A.E., Keriel, A., Schiavo, G., Kremer, E.J., CAR-associated vesicular transport of an adenovirus in motor neuron axons. PLoS Pathog., 5, 2009, e1000442.
57. Salinas, S., Schiavo, G., Kremer, E.J., A hitchhiker's guide to the nervous system: the complex journey of viruses and toxins. Nat. Rev. Microbiol. 8 (2010), 645–655.
58. Schantz, E.J., Johnson, E.A., Properties and use of botulinum toxin and other microbial neurotoxins in medicine. Microbiol. Rev. 56 (1992), 80–99.
59. Schiavo, G., Matteoli, M., Montecucco, C., Neurotoxins affecting neuroexocytosis. Physiol. Rev. 80 (2000), 717–766.
60. Schmieg, N., Menendez, G., Schiavo, G., Terenzio, M., Signalling endosomes in axonal transport: travel updates on the molecular highway. Semin. Cell Dev. Biol. 27 (2014), 32–43.
61. Scott, A.B., Botulinum toxin injection into extraocular muscles as an alternative to strabismus surgery. J. Pediatr. Ophthalmol. Strabismus 17 (1980), 21–25.
62. Silberstein, S., Mathew, N., Saper, J., Jenkins, S., for the BOTOX Migraine Clinical Research Group. Botulinum toxin type A as a migraine preventive treatment. Headache 40 (2000), 445–450.
63. Sun, S., Suresh, S., Liu, H., Tepp, W.H., Johnson, E.A., Edwardson, J.M., Chapman, E.R., Receptor binding enables botulinum neurotoxin B to sense low pH for translocation channel assembly. Cell Host Microbe 10 (2011), 237–247.
64. Sverdlov, Y.S., Alekseeva, V.I., Effect of tetanus toxin on presynaptic inhibition in the spinal cord. Fed. Proc. Transl. Suppl. 25 (1966), 931–936.
65. Taylor, A.M., Blurton-Jones, M., Rhee, S.W., Cribbs, D.H., Cotman, C.W., Jeon, N.L., A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat. Methods 2 (2005), 599–605.
66. Turton, K., Chaddock, J.A., Acharya, K.R., Botulinum and tetanus neurotoxins: structure, function and therapeutic utility. Trends Biochem. Sci. 27 (2002), 552–558.
67. von Bartheld, C.S., Axonal transport and neuronal transcytosis of trophic factors, tracers, and pathogens. J. Neurobiol. 58 (2004), 295–314.
68. Wang, T., Martin, S., Papadopulos, A., Harper, C.B., Mavlyutov, T.A., Niranjan, D., Glass, N.R., Cooper-White, J.J., Sibarita, J.B., Choquet, D., et al. Control of autophagosome axonal retrograde flux by presynaptic activity unveiled using botulinum neurotoxin type a. J. Neurosci. 35 (2015), 6179–6194.
69. Williamson, L.C., Neale, E.A., Bafilomycin A1 inhibits the action of tetanus toxin in spinal cord neurons in cell culture. J. Neurochem. 63 (1994), 2342–2345.
70. Yao, G., Zhang, S., Mahrhold, S., Lam, K.H., Stern, D., Bagramyan, K., Perry, K., Kalkum, M., Rummel, A., Dong, M., Jin, R., N-linked glycosylation of SV2 is required for binding and uptake of botulinum neurotoxin A. Nat. Struct. Mol. Biol. 23 (2016), 656–662.
71. Yeh, F.L., Dong, M., Yao, J., Tepp, W.H., Lin, G., Johnson, E.A., Chapman, E.R., SV2 mediates entry of tetanus neurotoxin into central neurons. PLoS Pathog., 6, 2010, e1001207.