Neurotransmitter vesicle release from human model neurons (NT2) is sensitive to botulinum toxin A

Cellular and Molecular Neurobiology

Volumn 32, Issue 6, 2012, Pages 1021-1029

  Tegenge, Million Adane ^a,b,c   Böhnel, Helge ^d   Gessler, Frank ^d   Bicker, Gerd ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Cell culture assay; FM1 43 imaging; Synaptic vesicle exocytosis; Synaptotagmin

Indexed keywords

BETA TUBULIN; BETA3 TUBULIN; BOTULINUM TOXIN A; MICROTUBULE ASSOCIATED PROTEIN 2; NEUROTRANSMITTER; NEUTRALIZING ANTIBODY; SYNAPSIN; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ARTICLE; CANCER STEM CELL; CELL STRAIN NT2; CONTROLLED STUDY; DEPOLARIZATION; DRUG ACTIVITY; DRUG POTENCY; ENDOCYTOSIS; EXOCYTOSIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; IN VITRO STUDY; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURITE; NEUROTRANSMITTER RELEASE; PRIORITY JOURNAL; SYNAPSE VESICLE;

ANTIBODIES, NEUTRALIZING; BOTULINUM TOXINS, TYPE A; CELL DIFFERENTIATION; ENDOCYTOSIS; HUMANS; MODELS, BIOLOGICAL; NEURONS; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; SYNAPTIC VESICLES; TERATOCARCINOMA;

EID: 84864713532     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-012-9818-2     Document Type: Article

References (42)

1. Adler S, Bicker G, Bigalke H, Bishop C, Blümel J, Dressler D et al (2010) The current scientific and legal status of alternative methods to the LD50 test for botulinum neurotoxin potency testing. The report and recommendations of a ZEBET expert meeting. Altern Lab Anim 38:315-330
2. Andrews PW (1984) Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol 103:285-293
3. Arnon SS, Schechter R, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS et al (2001) Botulinum toxin as a biological weapon: medical and public health management. JAMA 285:1059-1070 (Pubitemid 32176420)
4. Baldwin MR, Barbieri JT (2007) Association of botulinum neurotoxin serotypes A and B with synaptic vesicle protein complexes. Biochemistry 46:3200-3210 (Pubitemid 46449141)
5. Bergsman JB, Krueger SR, Fitzsimonds RM (2006) Automated criteria-based selection and analysis of fluorescent synaptic puncta. J Neurosci Methods 152(1-2):32-39 (Pubitemid 43343472)
6. Dressler D (1997) Botulinum toxin therapy failure: causes, evaluation procedures and management strategies. Eur J Neurol 4:S67-S70 (Pubitemid 28000095)
7. Franco I (2007) Pediatric overactive bladder syndrome: pathophysiology and management. Paediatr Drugs 9:379-390 (Pubitemid 350208912)
8. Gaffield MA, Betz WJ (2006) Imaging synaptic vesicle exocytosis and endocytosis with FM dyes. Nat Protoc 1:2916-2921
9. Gessler F, Pagel-Wieder S, Avondet M-A, Böhnel H (2007) Evaluation of lateral flow assays for the detection of botulinum neurotoxin type A and their application in laboratory diagnosis of botulism. Diagn Microbiol Infect Dis 57:243-249 (Pubitemid 46330657)
10. Guillemain I, Alonso G, Patey G, Privat A, Chaudieu I (2000) Human NT2 neurons express a large variety of neurotransmission phenotypes in vitro. J Comp Neurol 422:380-395 (Pubitemid 30387669)
11. Hall YHJ, Chaddock JA, Moulsdale HJ, Kirby ER, Alexander FCG, Marks JD et al (2004) Novel application of an in vitro technique to the detection and quantification of botulinum neurotoxin antibodies. J Immunol Methods 288:55-60 (Pubitemid 38739252)
12. Hartley RS, Margulis M, Fishman PS, Lee VM, Tang CM (1999) Functional synapses are formed between human NTera2 (NT2N, hNT) neurons grown on astrocytes. J Comp Neurol 407:1-10 (Pubitemid 29161989)
13. Houldsworth J, Heath SC, Bosl GJ, Studer L, Chaganti RSK (2002) Expression profiling of lineage differentiation in pluripotential human embryonal carcinoma cells. Cell Growth Differ 13: 257-264 (Pubitemid 34755378)
14. Keller JE, Neale EA, Oyler G, Adler M (1999) Persistence of botulinum neurotoxin action in cultured spinal cord cells. FEBS Lett 456:137-142 (Pubitemid 29339056)
15. Kostrzewa RM, Segura-Aguilar J (2007) Botulinum neurotoxin: evolution from poison, to research tool - onto medicinal therapeutic and future pharmaceutical panacea. Neurotox Res 12:275-290
16. Kraszewski K, Mundigl O, Daniell L, Verderio C, Matteoli M, De Camilli P (1995) Synaptic vesicle dynamics in living cultured hippocampal neurons visualized with CY3-conjugated antibodies directed against the lumenal domain of synaptotagmin. J Neurosci 15:4328-4342
17. Li L, Singh BR (1998) Isolation of synaptotagmin as a receptor for types A and E botulinum neurotoxin and analysis of their comparative binding using a new microtiter plate assay. J Nat Toxins 7:215-226 (Pubitemid 28456458)
18. Lindström M, Korkeala H (2006) Laboratory diagnostics of botulism. Clin Microbiol Rev 19:298-314
19. Matteoli M, Takei K, Perin MS, Südhof TC, De Camilli P (1992) Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J Cell Biol 117: 849-861
20. McNutt P, Celver J, Hamilton T, Mesngon M (2011) Embryonic stem cell-derived neurons are a novel, highly sensitive tissue culture platform for botulinum research. Biochem Biophys Res Commun 405:85-90
21. Neale EA, Bowers LM, Jia M, Bateman KE, Williamson LC (1999) Botulinum neurotoxin A blocks synaptic vesicle exocytosis but not endocytosis at the nerve terminal. J Cell Biol 147:1249-1260 (Pubitemid 30012810)
22. Nelson PT, Kondziolka D, Wechsler L, Goldstein S, Gebel J, DeCesare S et al (2002) Clonal human (hNT) neuron grafts for stroke therapy: neuropathology in a patient 27 months after implantation. Am J Pathol 160:1201-1206 (Pubitemid 34411623)
23. Nuss JE, Ruthel G, Tressler LE, Wanner LM, Torres-Melendez E, Hale ML et al (2010) Development of cell-based assays to measure botulinum neurotoxin serotype A activity using cleavage-sensitive antibodies. J Biomol Screen 15:42-51
24. Paquet-Durand F, Bicker G (2007) Human model neurons in studies of brain cell damage and neural repair. Curr Mol Med 7:541-554 (Pubitemid 47618051)
25. Paquet-Durand F, Tan S, Bicker G (2003) Turning teratocarcinoma cells into neurons: rapid differentiation of NT-2 cells in floating spheres. Brain Res Dev Brain Res 142:161-167 (Pubitemid 36593159)
26. 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 (Pubitemid 47531746)
27. Pleasure SJ, Page C, Lee VM (1992) Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J Neurosci 12:1802-1815
28. Podrygajlo G, Tegenge MA, Gierse A, Paquet-Durand F, Tan S, Bicker G et al (2009) Cellular phenotypes of human model neurons (NT2) after differentiation in aggregate culture. Cell Tissue Res 336:439-452
29. Podrygajlo G, Song Y, Schlesinger F, Krampfl K, Bicker G (2010a) Synaptic currents and transmitter responses in human NT2 neurons differentiated in aggregate culture. Neurosci Lett 4683:207-210
30. Podrygajlo G, Wiegreffe C, Scaal M, Bicker G (2010b) Integration of human model neurons (NT2) into embryonic chick nervous system. Dev Dyn 239:496-504
31. Polo M (2008) Botulinum toxin type A (Botox) for the neuromuscular correction of excessive gingival display on smiling (gummy smile). Am J Orthod Dentofacial Orthop 133:195-203
32. Przyborski SA, Morton IE, Wood A, Andrews PW (2000) Developmental regulation of neurogenesis in the pluripotent human embryonal carcinoma cell line NTERA-2. Eur J Neurosci 12: 3521-3528
33. Przyborski SA, Smith S, Wood A (2003) Transcriptional profiling of neuronal differentiation by human embryonal carcinoma stem cells in vitro. Stem Cells 21:459-471 (Pubitemid 36793488)
34. Schantz EJ, Kautter DA (1978) Standardized assay for Clostridium botulinum toxins. J Assoc Off Anal Chem 6:96-99
35. Schiavo G, Matteoli M, Montecucco C (2000) Neurotoxins affecting neuroexocytosis. Physiol Rev 80:717-766 (Pubitemid 30164948)
36. Scholtes VA, Dallmeijer AJ, Becher JG (2008) Can we identify predictors of multilevel botulinum toxin A injections in children with cerebral palsy who walk with a flexed knee pattern? J Child Neurol 23:628-634 (Pubitemid 351715908)
37. Schwartz CM, Spivak CE, Baker SC, McDaniel TK, Loring JF, Nguyen C et al (2005) NTera2: a model system to study dopaminergic differentiation of human embryonic stem cells. Stem Cells Dev 14:517-534 (Pubitemid 41780804)
38. Shukla HD, Sharma SK (2005) Clostridium botulinum: a bug with beauty and weapon. Crit Rev Microbiol 31:11-18 (Pubitemid 40461594)
39. Tegenge MA, Bicker G (2009) Nitric oxide and cGMP signal transduction positively regulates the motility of human neuronal precursor (NT2) cells. J Neurochem 110:1828-1841
40. Tegenge MA, Stern M, Bicker G (2009) Nitric oxide and cyclic nucleotide signal transduction modulates synaptic vesicle turnover in human model neurons. J Neurochem 111:1434-1446
41. Verderio C, Grumelli C, Raiteri L, Coco S, Paluzzi S, Caccin P et al (2007) Traffic of botulinum toxins A and E in excitatory and inhibitory neurons. Traffic 8:142-153 (Pubitemid 46100001)
42. Welch MJ, Purkiss JR, Foster KA (2000) Sensitivity of embryonic rat dorsal root ganglia neurons to Clostridium botulinum neurotoxins. Toxicon 38:245-258 (Pubitemid 29512196)