Alpha-latrotoxin rescues SNAP-25 from BoNT/A-mediated proteolysis in embryonic stem cell-derived neurons

Toxins

Volumn 3, Issue 5, 2011, Pages 489-503

  Mesngon, Mariano ^a   Mcnutt, Patrick ^a  

^a US ARMY MEDICAL RESEARCH INSTITUTE OF CHEMICAL DEFENSE   (United States)

Author keywords

Alpha latrotoxin; Botulinum neurotoxin; Embryonic stem cell derived neurons

Indexed keywords

ALPHA LATROTOXIN; BOTULINUM TOXIN A; SYNAPTOSOMAL ASSOCIATED PROTEIN 25;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EXPOSURE; DRUG MECHANISM; EMBRYONIC STEM CELL DERIVED NEURON; EXCITOTOXICITY; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PROTEIN DEGRADATION; TIME LAPSE IMAGING;

ANIMALS; BOTULINUM TOXINS, TYPE A; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; IMMUNOBLOTTING; MICE; MICROSCOPY, CONFOCAL; NEURONS; PROTEOLYSIS; SPIDER VENOMS; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; TIME-LAPSE IMAGING;

ARANEAE; LATRODECTUS;

EID: 79958069102     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins3050489     Document Type: Article

References (46)

1. Simpson, L.L. Identification of the major steps in botulinum toxin action. Annu. Rev. Pharmacol. Toxicol. 2004, 44, 167-193.
2. Johnson, E.A.; Montecucco, C. Chapter 11 botulism. Handb. Clin. Neurol. 2008, 91, 333-368.
3. Bakry, N.; Kamata, Y.; Simpson, L.L. Lectins from Triticum vulgaris and Limax flavus are universal antagonists of botulinum neurotoxin and tetanus toxin. J. Pharmacol. Exp. Ther. 1991, 258, 830-836.
4. Adler, M.; Nicholson, J.D. Evaluation of toosendanin as a botulinum neurotoxin antagonist. Botulinum J. 2008, 1, 208-218.
5. Larsen, J.C. U.S. Army Botulinum Neurotoxin (BoNT) Medical therapeutics research program: Past accomplishments and future directions. Drug Develop. Res. 2009, 70, 266-278.
6. Foran, P.G.; Mohammed, N.; Lisk, G.O.; Nagwaney, S.; Lawrence, G.W.; Johnson, E.; Smith, L.; Aoki, K.R.; Dolly, J.O. 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. 2003, 278, 1363-1371.
7. Rogozhin, A.A.; Pang, K.K.; Bukharaeva, E.; Young, C.; Slater, C.R. Recovery of mouse neuromuscular junctions from single and repeated injections of botulinum neurotoxin A. J. Physiol. 2008, 586, 3163-3182.
8. Morbiato, L.; Carli, L.; Johnson, E.A.; Montecucco, C.; Molgo, J.; Rossetto, O. Neuromuscular paralysis and recovery in mice injected with botulinum neurotoxins A and C. Eur. J. Neurosci. 2007, 25, 2697-2704.
9. Juzans, P.; Comella, J.X.; Molgo, J.; Faille, L.; Angaut-Petit, D. Nerve terminal sprouting in botulinum type-A treated mouse levator auris longus muscle. Neuromuscul. Disord. 1996, 6, 177-185.
10. Silva, J.P.; Suckling, J.; Ushkaryov, Y. Penelope's web: Using alpha-latrotoxin to untangle the mysteries of exocytosis. J. Neurochem. 2009, 111, 275-290.
11. Li, G.; Lee, D.; Wang, L.; Khvotchev, M.; Chiew, S.K.; Arunachalam, L.; Collins, T.; Feng, Z.P.; Sugita, S. N-terminal insertion and C-terminal ankyrin-like repeats of alpha-latrotoxin are critical for Ca2+-dependent exocytosis. J. Neurosci. 2005, 25, 10188-10197.
12. Capogna, M.; Volynski, K.E.; Emptage, N.J.; Ushkaryov, Y.A. The alpha-latrotoxin mutant LTXN4C enhances spontaneous and evoked transmitter release in CA3 pyramidal neurons. J. Neurosci. 2003, 23, 4044-4053.
13. Van Renterghem, C.; Iborra, C.; Martin-Moutot, N.; Lelianova, V.; Ushkaryov, Y.; Seagar, M. alpha-latrotoxin forms calcium-permeable membrane pores via interactions with latrophilin or neurexin. Eur. J. Neurosci. 2000, 12, 3953-3962.
14. Ushkaryov, Y.A.; Rohou, A.; Sugita, S. alpha-Latrotoxin and its receptors. Handb. Exp. Pharmacol. 2008, 184, 171-206.
15. Orlova, E.V.; Rahman, M.A.; Gowen, B.; Volynski, K.E.; Ashton, A.C.; Manser, C.; van Heel, M.; Ushkaryov, Y.A. Structure of alpha-latrotoxin oligomers reveals that divalent cation-dependent tetramers form membrane pores. Nat. Struct. Biol. 2000, 7, 48-53.
16. Deak, F.; Liu, X.; Khvotchev, M.; Li, G.; Kavalali, E.T.; Sugita, S.; Südhof, T.C. Alpha-latrotoxin stimulates a novel pathway of Ca2+-dependent synaptic exocytosis independent of the classical synaptic fusion machinery. J. Neurosci. 2009, 29, 8639-8648.
17. Bronk, P.; Deak, F.; Wilson, M.C.; Liu, X.; Sudhof, T.C.; Kavalali, E.T. Differential effects of SNAP-25 deletion on Ca2+ -dependent and Ca2+ -independent neurotransmission. J. Neurophysiol. 2007, 98, 794-806.
18. Deak, F.; Schoch, S.; Liu, X.; Sudhof, T.C.; Kavalali, E.T. Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nat. Cell. Biol. 2004, 6, 1102-1108.
19. Washbourne, P.; Thompson, P.M.; Carta, M.; Costa, E.T.; Mathews, J.R.; Lopez-Benditó, G.; Molnár, Z.; Becher, M.W.; Valenzuela, C.F.; Partridge, L.D. et al. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 2002, 5, 19-26.
20. Clark, A.W.; Hurlbut, W.P.; Mauro, A. Changes in the fine structure of the neuromuscular junction of the frog caused by black widow spider venom. J. Cell Biol. 1972, 52, 1-14.
21. Ceccarelli, B.; Grohovaz, F.; Hurlbut, W.P. Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. II. Effects of electrical stimulation and high potassium. J. Cell. Biol. 1979, 81, 178-192.
22. Ceccarelli, B.; Grohovaz, F.; Hurlbut, W.P. Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. I. Effects of black widow spider venom and Ca2+-free solutions on the structure of the active zone. J. Cell. Biol. 1979, 81, 163-177.
23. Duchen, L.W.; Gomez, S.; Queiroz, L.S. The neuromuscular junction of the mouse after black widow spider venom. J. Physiol. 1981, 316, 279-291.
24. Henkel, A.W.; Betz, W.J. Monitoring of black widow spider venom (BWSV) induced exo- and endocytosis in living frog motor nerve terminals with FM1-43. Neuropharmacology 1995, 34, 1397-1406.
25. Gomez, S.; Queiroz, L.S. The effects of black widow spider venom on the innervation of muscles paralysed by botulinum toxin. Q. J. Exp. Physiol. 1982, 67, 495-506.
26. Thesleff, S.; Zelena, J.; Hofmann, W.W. Restoration of Function in Botulinum Paralysis by Experimental Nerve Regeneration. Proc. Soc. Exp. Biol. Med. 1964, 116, 19-20.
27. Duchen, L.W. The effects in the mouse of nerve crush and regneration on the innervation of skeletal muscles paralysed by Clostridium botulinum toxin. J. Pathol. 1970, 102, 9-14.
28. McNutt, P.; Celver, J.; Hamilton, T.; Mesngon, M. Embryonic stem cell-derived neurons are a novel, highly sensitive tissue culture platform for botulinum research. Biochem. Biophys. Res. Commun. 2011, 405, 85-90.
29. Keller, J.E.; Neale, E.A.; Oyler, G.; Adler, M. Persistence of botulinum neurotoxin action in cultured spinal cord cells. FEBS Lett. 1999, 456, 137-142.
30. Sanders, J.D.; Yang, Y.; Liu, Y. Differential turnover of syntaxin and SNAP-25 during synaptogenesis in cultured cerebellar granule neurons. J. Neurosci. Res. 1998, 53, 670-676.
31. Tedesco, E.; Rigoni, M.; Caccin, P.; Grishin, E.; Rossetto, O.; Montecucco, C. Calcium overload in nerve terminals of cultured neurons intoxicated by alpha-latrotoxin and snake PLA2 neurotoxins. Toxicon 2009, 54, 138-144.
32. Boldt, G.E.; Eubanks, L.M.; Janda, K.D. Identification of a botulinum neurotoxin A protease inhibitor displaying efficacy in a cellular model. Chem. Commun. (Camb.), 2006, 7, 3063-3065.
33. Dong, M.; Tepp, W.H.; Johnson, E.A.; Chapman, E.R. Using fluorescent sensors to detect botulinum neurotoxin activity in vitro and in living cells. Proc. Natl. Acad. Sci. USA 2004, 101, 14701-14706.
34. Puffer, E.B.; Lomneth, R.B.; Sarkar, H.K.; Singh, B.R. Differential roles of developmentally distinct SNAP-25 isoforms in the neurotransmitter release process. Biochemistry 2001, 40, 9374-9378.
35. Purkiss, J.R.; Friis, L.M.; Doward, S.; Quinn, C.P. Clostridium botulinum neurotoxins act with a wide range of potencies on SH-SY5Y human neuroblastoma cells. Neurotoxicology 2001, 22, 447-453.
36. Tarasenko, A.S.; Storchak, L.G.; Himmelreich, N.H. alpha-Latrotoxin affects mitochondrial potential and synaptic vesicle proton gradient of nerve terminals. Neurochem. Int. 2008, 52, 392-400.
37. Ahmed, S.A.; Ludivico, M.L.; Smith, L.A. Factors affecting autocatalysis of botulinum A neurotoxin light chain. Protein J. 2004, 23, 445-451.
38. de Paiva, A.; Meunier, F.A.; Molgo, J.; Aoki, K.R.; Dolly, J.O. 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. USA 1999, 96, 3200-3205.
39. 2+-independent excitotoxic neurodegeneration in isolated retina, an intact neural net, a role for Cl- and inhibitory transmitters. Mol. Pharmacol. 1998, 53, 564-572.
40. Hoffmann, E.K.; Dunham, P.B. Membrane mechanisms and intracellular signalling in cell volume regulation. Int. Rev.Cytol. 1995, 161, 173-262.
41. Hasbani, M.J.; Hyrc, K.L.; Faddis, B.T.; Romano, C.; Goldberg, M.P. Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp. Neurol. 1998, 154, 241-258.
42. Ashton, A.C.; Volynski, K.E.; Lelianova, V.G.; Orlova, E.V.; van Renterghem, C.; Canepari, M.; Seagar, M.; Ushkaryov, Y.A. alpha-Latrotoxin, acting via two Ca2+-dependent pathways, triggers exocytosis of two pools of synaptic vesicles. J. Biol. Chem. 2001, 276, 44695-44703.
43. Lajus, S.; Vacher, P.; Huber, D.; Dubois, M.; Benassy, M.N.; Ushkaryov, Y.; Lang, J. Alpha-latrotoxin induces exocytosis by inhibition of voltage-dependent K+ channels and by stimulation of L-type Ca2+ channels via latrophilin in beta-cells. J. Biol. Chem. 2006, 281, 5522-5531.
44. Madl, J.E.; Burgesser, K. Adenosine triphosphate depletion reverses sodium-dependent, neuronal uptake of glutamate in rat hippocampal slices. J. Neurosci. 1993, 13, 4429-4444.
45. +]: Involvement of transporter reversal and mitochondrial calcium. J. Neurochem. 2002, 80, 706-714.
46. Kubo, T.; Randolph, M.A.; Groger, A.; Winograd, J.M. Embryonic stem cell-derived motor neurons form neuromuscular junctions in vitro and enhance motor functional recovery in vivo. Plast. Reconstr. Surg. 2009, 123, 139S-148S.