Model for studying Clostridium botulinum neurotoxin using differentiated motor neuron-like NG108-15 cells

Biochemical and Biophysical Research Communications

Volumn 427, Issue 2, 2012, Pages 426-430

  Whitemarsh, Regina C M ^a   Pier, Christina L ^a   Tepp, William H ^a   Pellett, Sabine ^a   Johnson, Eric A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

BoNT A; Cell based assay; Clostridium botulinum; Neurotoxins; NG108 15

Indexed keywords

BOTULINUM TOXIN; GANGLIOSIDE GT 1B; PURINE DERIVATIVE; PURMORPHAMINE; RETINOIC ACID; TRIASIALOGANGLIOSIDE GT1B; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL POPULATION; CLOSTRIDIUM BOTULINUM; HYBRID CELL; MOTONEURON; MOUSE; MYOTUBE; NEUROBLASTOMA CELL; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; APOPTOSIS; BOTULINUM TOXINS, TYPE A; CELL DIFFERENTIATION; CHOLINERGIC NEURONS; CLOSTRIDIUM BOTULINUM; COCULTURE TECHNIQUES; GANGLIOSIDES; MICE; MODELS, NEUROLOGICAL; MORPHOLINES; MOTOR NEURONS; NEUROTOXINS; PURINES; RATS; TRETINOIN;

CLOSTRIDIUM BOTULINUM;

EID: 84867857479     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.09.082     Document Type: Article

References (48)

1. Arnon S.S., Schechter R., Inglesby T.V., Henderson D.A., Bartlett J.G., Ascher M.S., Eitzen E., Fine A.D., Hauer J., Layton M., Lillibridge S., Osterholm M.T., O'Toole T., Parker G., Perl T.M., Russell P.K., Swerdlow D.L., Tonat K. Working group on civilian biodefense botulinum toxin as a biological weapon: medical and public health management. JAMA 2001, 285:1059-1070.
2. Chaddock J.A., Acharya K.R. Engineering toxins for 21st century therapies. FEBS J. 2011, 278:899-904.
3. Gimenez D.F., Gimenez J.A. The typing of botulinal neurotoxins. Int. J. Food Microbiol. 1995, 27:1-9.
4. Smith T.J., Lou J., Geren I.N., Forsyth C.M., Tsai R., Laporte S.L., Tepp W.H., Bradshaw M., Johnson E.A., Smith L.A., Marks J.D. Sequence variation within botulinum neurotoxin serotypes impacts antibody binding and neutralization. Infect. Immun. 2005, 73:5450-5457.
5. Fischer A., Nakai Y., Eubanks L.M., Clancy C.M., Tepp W.H., Pellett S., Dickerson T.J., Johnson E.A., Janda K.D., Montal M. Bimodal modulation of the botulinum neurotoxin protein-conducting channel. Proc. Nat. Acad. Sci. USA 2009, 106:1330-1335.
6. Fischer A., Montal M. Crucial role of the disulfide bridge between botulinum neurotoxin light and heavy chains in protease translocation across membranes. J. Biol. Chem. 2007, 282:29604-29611.
7. Montecucco C., Rossetto O., Schiavo G. Presynaptic receptor arrays for clostridial neurotoxins. Trends Microbiol. 2004, 12:442-446.
8. Montecucco C., Schiavo G. Mechanism of action of tetanus and botulinum neurotoxins. Mol. Microbiol. 1994, 13:1-8.
9. Johnson E.A., Montecucco C. Botulism. Handbook of Clinical Neurology 2008, 333-368. Elsevier, (Chapter 11). A.G. Engel (Ed.).
10. Schiavo G., Matteoli M., Montecucco C. Neurotoxins affecting neuroexocytosis. Physiol. Rev. 2000, 80:717-766.
11. 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.
12. Pellett S., Du Z.W., Pier C.L., Tepp W.H., Zhang S.C., Johnson E.A. Sensitive and quantitative detection of botulinum neurotoxin in neurons derived from mouse embryonic stem cells. Biochem. Biophys. Res. Commun. 2011, 404:388-392.
13. Neale E.A., Bowers L.M., Jia M., Bateman K.E., Williamson L.C. Botulinum neurotoxin A blocks synaptic vesicle exocytosis but not endocytosis at the nerve terminal. J. Cell Biol. 1999, 147:1249-1260.
14. Stahl A.M., Ruthel G., Torres-Melendez E., Kenny T.A., Panchal R.G., Bavari S. Primary cultures of embryonic chicken neurons for sensitive cell-based assay of botulinum neurotoxin: implications for therapeutic discovery. J. Biomol. Screening 2007, 12:370-377.
15. Pier C.L., Chen C., Tepp W.H., Lin G., Janda K.D., Barbieri J.T., Pellett S., Johnson E.A. Botulinum neurotoxin subtype A2 enters neuronal cells faster than subtype A1. FEBS Lett. 2011, 585:199-206.
16. Yowler B.C., Kensinger R.D., Schengrund C.L. Botulinum neurotoxin A activity is dependent upon the presence of specific gangliosides in neuroblastoma cells expressing synaptotagmin I. J. Biol. Chem. 2002, 277:32815-32819.
17. Shone C.C., Melling J. Inhibition of calcium-dependent release of noradrenaline from PC12 cells by botulinum type-A neurotoxin Long-term effects of the neurotoxin on intact cells. Eur. J. Biochem. 1992, 207:1009-1016.
18. Ray P. Botulinum toxin A inhibits acetylcholine release from cultured neurons in vitro. In Vitro Cell Dev. Biol. Anim. 1993, 29A:456-460.
19. 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. 2003, 162:1293-1303.
20. 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.
21. Rasetti-Escargueil C., Machado C.B., Preneta-Blanc R., Fleck R.A., Sesardic D. Enhanced sensitivity to Botulinum type A neurotoxin of human neuroblastoma SH-SY5Y cells after differentiation into mature neuronal cells. Botulinum J. 2011, 2:30.
22. Lee S.K., Jurata L.W., Funahashi J., Ruiz E.C., Pfaff S.L. Analysis of embryonic motoneuron gene regulation: derepression of general activators function in concert with enhancer factors. Development 2004, 131:3295-3306.
23. Tegenge M.A., Bohnel H., Gessler F., Bicker G. Neurotransmitter vesicle release from human model neurons (NT2) is sensitive to botulinum toxin A. Cell Mol. Neurobiol. 2012, 32:1021-1029.
24. H. Zhu, J. Wang, B.P.S. Jacky, et al., Cells useful for immuno-based botulinum toxin serotype A activity assays, 2010, Patent.
25. Schantz E.J., Kautter D.A. Standardized assay for Clostridium botulinum toxins. J. Assoc. Off. Anal. Chem. 1978, 61:96-99.
26. Hatheway C.L. Botulism. Laboratory diagnosis of infectious diseases: principles and practice 1988, 111-133. Springer-Verlag, New York. A. Balows, W.H. Hausler, M. Ohashi, M.A. Turano (Eds.).
27. Jiang J.X., Choi R.C., Siow N.L., Lee H.H., Wan D.C., Tsim K.W. Muscle induces neuronal expression of acetylcholinesterase in neuron-muscle co-culture: transcriptional regulation mediated by cAMP-dependent signaling. J. Biol. Chem. 2003, 278:45435-45444.
28. Choi R.C., Pun S., Dong T.T., Wan D.C., Tsim K.W. NG108-15 cells induce the expression of muscular acetylcholinesterase when co-cultured with myotubes. Neurosci. Lett. 1997, 236:167-170.
29. Busis N.A., Daniels M.P., Bauer H.C., Pudimat P.A., Sonderegger P., Schaffner A.E., Nirenberg M. Three cholinergic neuroblastoma hybrid cell lines that form few synapses on myotubes are deficient in acetylcholine receptor aggregation molecules and large dense core vesicles. Brain Res. 1984, 324:201-210.
30. Pun S., Tsim K.W. Antisense agrin cDNA transfection blocks neuroblastoma cell-induced acetylcholine receptor aggregation when co-cultured with myotubes. Mol. Cell Neurosci. 1997, 10:87-99.
31. Malizio C.J., Goodnough M.C., Johnson E.A. Purification of Clostridium botulinum type A neurotoxin. Methods Mol. Biol. 2000, 145:27-39.
32. Schantz E.J., Kautter D.A. Standardized assay for Clostridium botulinum toxins. J. Assoc. Off. Anal. Chem. 1978, 61:96-99.
33. Pellett S., Tepp W.H., Clancy C.M., Borodic G.E., Johnson E.A. A neuronal cell-based botulinum neurotoxin assay for highly sensitive and specific detection of neutralizing serum antibodies. FEBS Lett. 2007, 581:4803-4808.
34. Pellett S., Tepp W.H., Toth S.I., Johnson E.A. 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 2010, 61:304-310.
35. Rummel A., Mahrhold S., Bigalke H., Binz T. The HCC-domain of botulinum neurotoxins A and B exhibits a singular ganglioside binding site displaying serotype specific carbohydrate interaction. Mol. Microbiol. 2004, 51:631-643.
36. Johnson J.E., Zimmerman K., Saito T., Anderson D.J. Induction and repression of mammalian achaete-scute homologue (MASH) gene expression during neuronal differentiation of P19 embryonal carcinoma cells. Development 1992, 114:75-87.
37. Okamoto K., Okazawa H., Okuda A., Sakai M., Muramatsu M., Hamada H. A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells. Cell 1990, 60:461-472.
38. Shimazaki T., Okazawa H., Fujii H., Ikeda M., Tamai K., McKay R.D., Muramatsu M., Hamada H. Hybrid cell extinction and re-expression of Oct-3 function correlates with differentiation potential. EMBO J. 1993, 12:4489-4498.
39. Fujii H., Hamada H., factor A CNS-specific POU transcription Brn-2 is required for establishing mammalian neural cell lineages. Neuron 1993, 11:1197-1206.
40. Turner E.E., Jenne K.J., Rosenfeld M.G. Brn-3.2: a Brn-3-related transcription factor with distinctive central nervous system expression and regulation by retinoic acid. Neuron 1994, 12:205-218.
41. Takahashi J., Palmer T.D., Gage F.H. Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J. Neurobiol. 1999, 38:65-81.
42. Li X.J., Hu B.Y., Jones S.A., Zhang Y.S., Lavaute T., Du Z.W., Zhang S.C. Directed differentiation of ventral spinal progenitors and motor neurons from human embryonic stem cells by small molecules. Stem Cells 2008, 26:886-893.
43. Dahms N.M., Schnaar R.L. Ganglioside composition is regulated during differentiation in the neuroblastoma X glioma hybrid cell line NG108-15. J. Neurosci. 1983, 3:806-817.
44. Wilson S., Higashida H., Minna J., Nirenberg M. Defects in synapse formation and acetylcholine release by neuroblastoma and hybrid cell lines. Federal Proc. 1978, 37:1784.
45. McGee R., Simpson P., Christian C., Mata M., Nelson P., Nirenberg M. Regulation of acetylcholine release from neuroblastoma X glioma hybrid cells. Proc. Nat. Acad. Sci. USA 1978, 75:1314-1318.
46. Nelson P., Christian C., Nirenberg M. Synapse formation between clonal neuroblastoma X glioma hybrid cells and striated muscle cells. Proc. Nat. Acad. Sci. USA 1976, 73:123-127.
47. Higashida H. Acetylcholine release by bradykinin, inositol 1,4,5-trisphosphate and phorbol dibutyrate in rodent neuroblastoma cells. J. Physiol. 1988, 397:209-222.
48. Whitemarsh R.C., Strathman M.J., Chase L.G., Stankewicz C., Tepp W.H., Johnson E.A., Pellett S. Novel application of human neurons derived from induced pluripotent stem cells for highly sensitive botulinum neurotoxin detection. Toxicol. Sci. 2012, 126:426-435.