A microscale neuron and schwann cell coculture model for increasing detection sensitivity of botulinum neurotoxin type A

Toxicological Sciences

Volumn 134, Issue 1, 2013, Pages 64-72

  Hong, Won S ^a   Young, Edmond W K ^a,b   Tepp, William H ^c   Johnson, Eric A ^c   Beebe, David J ^a,d  

^a University of Wisconsin Health   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF WISCONSIN   (United States)

Author keywords

BoNT; Botulinum neurotoxin; Cell based assay; Coculture; Microenvironment; Microfluidic

Indexed keywords

BOTULINUM TOXIN A; NEUROTOXIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; MICROFLUIDIC ANALYSIS; NERVE CELL; NONHUMAN; RAT; SCHWANN CELL; ANIMAL; BIOASSAY; COCULTURE; CYTOLOGY; DEVICES; DRUG EFFECTS; EQUIPMENT DESIGN; MICROFLUIDICS; MOUSE; PROCEDURES; SENSITIVITY AND SPECIFICITY; TOXICITY; TUMOR CELL LINE;

ANIMALS; BIOLOGICAL ASSAY; BOTULINUM TOXINS, TYPE A; CELL LINE, TUMOR; COCULTURE TECHNIQUES; EQUIPMENT DESIGN; MICE; MICROFLUIDICS; NEURONS; NEUROTOXINS; RATS; SCHWANN CELLS; SENSITIVITY AND SPECIFICITY;

EID: 84880291402     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft082     Document Type: Article

References (41)

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., et al. (2001). Botulinum toxin as a biological weapon: Medical and public health management. JAMA 285, 1059-1070.
2. Bagramyan, K., Barash, J. R., Arnon, S. S., and Kalkum, M. (2008). Attomolar detection of botulinum toxin type A in complex biological matrices. PLoS One 3, e2041.
3. Cai, S., Singh, B. R., and Sharma, S. (2007). Botulism diagnostics: From clinical symptoms to in vitro assays. Crit. Rev. Microbiol. 33, 109-125.
4. Cao, G., and Ko, C. P. (2007). Schwann cell-derived factors modulate synaptic activities at developing neuromuscular synapses. J. Neurosci. 27, 6712-6722.
5. Chaddock, J. A., and Acharya, K. R. (2011). Engineering toxins for 21st century therapies. FEBS J. 278, 899-904.
6. Christian, C. N., Nelson, P. G., Bullock, P., Mullinax, D., and Nirenberg, M. (1978). Pharmacologic responses of cells of a neuroblastoma X glioma hybrid clone and modulation of synapses between hybrid cells and mouse myotubes. Brain Res. 147, 261-276.
7. Domenech, M., Yu, H., Warrick, J., Badders, N. M., Meyvantsson, I., Alexander, C. M., and Beebe, D. J. (2009). Cellular observations enabled by microculture: Paracrine signaling and population demographics. Integr. Biol. (Camb). 1, 267-274.
8. Dong, M., Tepp, W. H., Johnson, E. A., and Chapman, E. R. (2004). Using fluorescent sensors to detect botulinum neurotoxin activity in vitro and in living cells. Proc. Natl. Acad. Sci. U.S.A. 101, 14701-14706.
9. Duffy, D. C., McDonald, J. C., Schueller, O. J., and Whitesides, G. M. (1998). Rapid prototyping of microfluidic systems in poly(dimethylsiloxane). Anal. Chem. 70, 4974-4984.
10. Eroglu, C., and Barres, B. A. (2010). Regulation of synaptic connectivity by glia. Nature 468, 223-231.
11. Feng, Z., and Ko, C. P. (2008). Schwann cells promote synaptogenesis at the neuromuscular junction via transforming growth factor-beta1. J. Neurosci. 28, 9599-9609.
12. Fernández-Salas, E., Wang, J., Molina, Y., Nelson, J. B., Jacky, B. P., and Aoki, K. R. (2012). Botulinum neurotoxin serotype A specific cell-based potency assay to replace the mouse bioassay. PLoS One 7, e49516.
13. Frisk, M. L., Tepp, W. H., Johnson, E. A., and Beebe, D. J. (2009). Selfassembled peptide monolayers as a toxin sensing mechanism within arrayed microchannels. Anal. Chem. 81, 2760-2767.
14. Hai, M., Muja, N., DeVries, G. H., Quarles, R. H., and Patel, P. I. (2002). Comparative analysis of Schwann cell lines as model systems for myelin gene transcription studies. J. Neurosci. Res. 69, 497-508.
15. Hakami, R. M., Ruthel, G., Stahl, A. M., and Bavari, S. (2010). Gaining ground: Assays for therapeutics against botulinum neurotoxin. Trends Microbiol. 18, 164-172.
16. Kao, I., Drachman, D. B., and Price, D. L. (1976). Botulinum toxin: Mechanism of presynaptic blockade. Science 193, 1256-1258.
17. Lam, A. J., St-Pierre, F., Gong, Y., Marshall, J. D., Cranfill, P. J., Baird, M. A., McKeown, M. R., Wiedenmann, J., Davidson, M. W., Schnitzer, M. J., et al. (2012). Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005-1012.
18. McGee, R., Simpson, P., Christian, C., Mata, M., Nelson, P., and Nirenberg, M. (1978). Regulation of acetylcholine release from neuroblastoma x glioma hybrid cells. Proc. Natl. Acad. Sci. U.S.A. 75, 1314-1318.
19. Montal, M. (2010). Botulinum neurotoxin: A marvel of protein design. Annu. Rev. Biochem. 79, 591-617.
20. National Institute of Health. (2008). Report on the ICCVAM-NICEATM/ECVAM Scientific Workshop on Alternative Methods to Refine, Reduce or Replace the Mouse LD50 Assay for Botulinum Toxin Testing. National Institute of Health, Bethesda, MD.
21. Nirenberg, M., Wilson, S., Higashida, H., Rotter, A., Krueger, K., Busis, N., Ray, R., Kenimer, J. G., and Adler, M. (1983). Modulation of synapse formation by cyclic adenosine monophosphate. Science 222, 794-799.
22. Paguirigan, A. L., and Beebe, D. J. (2009). From the cellular perspective: Exploring differences in the cellular baseline in macroscale and microfluidic cultures. Integr. Biol. (Camb). 1, 182-195.
23. Pancrazio, J. J., Whelan, J. P., Borkholder, D. A., Ma, W., and Stenger, D. A. (1999). Development and application of cell-based biosensors. Ann. Biomed. Eng. 27, 697-711.
24. Pellett, S., Du, Z. W., Pier, C. L., Tepp, W. H., Zhang, S. C., and Johnson, E. A. (2011). Sensitive and quantitative detection of botulinum neurotoxin in neurons derived from mouse embryonic stem cells. Biochem. Biophys. Res. Commun. 404, 388-392.
25. Pellett, S., Tepp, W. H., Toth, S. I., and Johnson, E. A. (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.
26. Phillips, R. W., and Abbott, D. (2008). High-throughput enzyme-linked immunoabsorbant assay (ELISA) electrochemiluminescent detection of botulinum toxins in foods for food safety and defence purposes. Food Addit. Contam. Part A. Chem. Anal. Control. Expo. Risk Assess. 25, 1084-1088.
27. Purkiss, J. R., Friis, L. M., Doward, S., and Quinn, C. P. (2001). Clostridium botulinum neurotoxins act with a wide range of potencies on SH-SY5Y human neuroblastoma cells. Neurotoxicology 22, 447-453.
28. Reddy, L. V., Koirala, S., Sugiura, Y., Herrera, A. A., and Ko, C. P. (2003). Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron 40, 563-580.
29. Regehr, K. J., Domenech, M., Koepsel, J. T., Carver, K. C., Ellison-Zelski, S. J., Murphy, W. L., Schuler, L. A., Alarid, E. T., and Beebe, D. J. (2009). Biological implications of polydimethylsiloxane-based microfluidic cell culture. Lab Chip 9, 2132-2139.
30. Saharinen, J., and Keski-Oja, J. (2000). Specific sequence motif of 8-Cys repeats of TGF-beta binding proteins, LTBPs, creates a hydrophobic interaction surface for binding of small latent TGF-beta. Mol. Biol. Cell 11, 2691-2704.
31. Thomson, S. R., Wishart, T. M., Patani, R., Chandran, S., and Gillingwater, T. H. (2012). Using induced pluripotent stem cells (iPSC) to model human neuromuscular connectivity: Promise or reality? J. Anat. 220, 122-130.
32. Tojima, T., Yamane, Y., Takahashi, M., and Ito, E. (2000). Acquisition of neuronal proteins during differentiation of NG108-15 cells. Neurosci. Res. 37, 153-161.
33. Ullian, E. M., Harris, B. T., Wu, A., Chan, J. R., and Barres, B. A. (2004). Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture. Mol. Cell. Neurosci. 25, 241-251.
34. Walker, G., and Beebe, D. J. (2002). A passive pumping method for microfluidic devices. Lab Chip 2, 131-134.
35. Whitemarsh, R. C., Pier, C. L., Tepp, W. H., Pellett, S., and Johnson, E. A. (2012a). Model for studying Clostridium botulinum neurotoxin using differentiated motor neuron-like NG108-15 cells. Biochem. Biophys. Res. Commun. 427, 426-430.
36. Whitemarsh, R. C., Strathman, M. J., Chase, L. G., Stankewicz, C., Tepp, W. H., Johnson, E. A., and Pellett, S. (2012b). Novel application of human neurons derived from induced pluripotent stem cells for highly sensitive botulinum neurotoxin detection. Toxicol. Sci. 126, 426-435.
37. Xia, Y., and Whitesides, G. M. (1998). Soft lithography. Annu. Rev. Mater. Sci. 28, 153-184.
38. Young, E. W., and Beebe, D. J. (2010). Fundamentals of microfluidic cell culture in controlled microenvironments. Chem. Soc. Rev. 39, 1036-1048.
39. Young, E. W., Berthier, E., Guckenberger, D. J., Sackmann, E., Lamers, C., Meyvantsson, I., Huttenlocher, A., and Beebe, D. J. (2011). Rapid prototyping of arrayed microfluidic systems in polystyrene for cell-based assays. Anal. Chem. 83, 1408-1417.
40. Young, E. W., Pak, C., Kahl, B. S., Yang, D. T., Callander, N. S., Miyamoto, S., and Beebe, D. J. (2012). Microscale functional cytomics for studying hematologic cancers. Blood 119, e76-e85.
41. Yowler, B. C., Kensinger, R. D., and Schengrund, C. L. (2002). Botulinum neurotoxin A activity is dependent upon the presence of specific gangliosides in neuroblastoma cells expressing synaptotagmin I. J. Biol. Chem. 277, 32815-32819.