867
Views
49
CrossRef citations to date
0
Altmetric
Review Article

Botulinum neurotoxin: Where are we with detection technologies?

, &
Pages 43-56 | Received 19 Jan 2012, Accepted 03 May 2012, Published online: 08 Jun 2012

References

  • Adler M, Scovill J, Parker G, Lebeda FJ, Piotrowski J, Deshpande SS. (1995). Antagonism of botulinum toxin-induced muscle weakness by 3,4-diaminopyridine in rat phrenic nerve-hemidiaphragm preparations. Toxicon, 33, 527–537.
  • Aoki KR. (2001). A comparison of the safety margins of botulinum neurotoxin serotypes A, B, and F in mice. Toxicon, 39, 1815–1820.
  • Arnon SS, Schechter R, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Hauer J, Layton M, Lillibridge S, Osterholm MT, O’Toole T, Parker G, Perl TM, Russell PK, Swerdlow DL, Tonat K. (2001). Botulinum toxin as a biological weapon: medical and public health management. JAMA, 285, 1059–1070.
  • Atlas RM. (2002). Bioterriorism: from threat to reality. Annu Rev Microbiol, 56, 167–185.
  • Attrée O, Guglielmo-Viret V, Gros V, Thullier P. (2007). Development and comparison of two immunoassay formats for rapid detection of botulinum neurotoxin type A. J Immunol Methods, 325, 78–87.
  • Bagramyan K, Barash JR, Arnon SS, Kalkum M. (2008). Attomolar detection of botulinum toxin type A in complex biological matrices. PLoS ONE, 3, e2041.
  • Barr JR, Moura H, Boyer AE, Woolfitt AR, Kalb SR, Pavlopoulos A, McWilliams LG, Schmidt JG, Martinez RA, Ashley DL. (2005). Botulinum neurotoxin detection and differentiation by mass spectrometry. Emerging Infect Dis, 11, 1578–1583.
  • Basavanna U, Muruvanda T, Brown EW, Sharma SK. Development of a cell based functional assay for the detection of botulinum neurotoxin type A and E. (Unpublished data)
  • Benatar MG, Willison HJ, Vincent A. (1997). Lack of effect of Miller Fisher sera/plasmas on transmitter release from PC12 cells. J Neuroimmunol, 80, 1–5.
  • Brunt J, Webb MD, Peck MW. (2010). Rapid affinity immunochromatography column-based tests for sensitive detection of Clostridium botulinum neurotoxins and Escherichia coli O157. Appl Environ Microbiol, 76, 4143–4150.
  • Burbulis I, Yamaguchi K, Gordon A, Carlson R, Brent R. (2005). Using protein-DNA chimeras to detect and count small numbers of molecules. Nat Methods, 2, 31–37.
  • Burbulis I, Yamaguchi K, Yu R, Resnekov O, Brent R. (2007). Quantifying small numbers of antibodies with a ‘near-universal’ protein-DNA chimera. Nat Methods, 4, 1011–1013.
  • Cai S, Singh BR, Sharma S. (2007). Botulism diagnostics: from clinical symptoms to in vitro assays. Crit Rev Microbiol, 33, 109–125.
  • Capek P, Dickerson TJ. (2010). Sensing the deadliest toxin: technologies for botulinum neurotoxin detection. Toxins (Basel), 2, 24–53.
  • Chao HY, Wang YC, Tang SS, Liu HW. (2004). A highly sensitive immuno-polymerase chain reaction assay for Clostridium botulinum neurotoxin type A. Toxicon, 43, 27–34.
  • Chiao DJ, Shyu RH, Hu CS, Chiang HY, Tang SS. (2004). Colloidal gold-based immunochromatographic assay for detection of botulinum neurotoxin type B. J Chromatogr B Analyt Technol Biomed Life Sci, 809, 37–41.
  • Chiao DJ, Wey JJ, Shyu RH, Tang SS. (2008). Monoclonal antibody-based lateral flow assay for detection of botulinum neurotoxin type A. Hybridoma (Larchmt), 27, 31–35.
  • Ching KH, Lin A, McGarvey JA, Stanker LH, Hnasko R. (2012). Rapid and selective detection of botulinum neurotoxin serotype-A and -B with a single immunochromatographic test strip. J Immunological Methods, 380, 23–29.
  • De Medici D, Anniballi F, Wyatt GM, Lindström M, Messelhäusser U, Aldus CF, Delibato E, Korkeala H, Peck MW, Fenicia L. (2009). Multiplex PCR for detection of botulinum neurotoxin-producing clostridia in clinical, food, and environmental samples. Appl Environ Microbiol, 75, 6457–6461.
  • Dembek ZF, Smith LA, Rusnak JM. (2007). Botulism: cause, effects, diagnosis, clinical and laboratory identification, and treatment modalities. Disaster Med Public Health Prep, 1, 122–134.
  • Deshpande SS, Sheridan RE, Adler M. (1995). A study of zinc-dependent metalloendopeptidase inhibitors as pharmacological antagonists in botulinum neurotoxin poisoning. Toxicon, 33, 551–557.
  • Dong M, Tepp WH, Johnson EA, Chapman ER. (2004). Using fluorescent sensors to detect botulinum neurotoxin activity in vitro and in living cells. Proc Natl Acad Sci USA, 101, 14701–14706.
  • Dressler D. (2008). Botulinum toxin drugs: future developments. J Neural Transm, 115, 575–577.
  • Fach P, Micheau P, Mazuet C, Perelle S, Popoff M. (2009). Development of real-time PCR tests for detecting botulinum neurotoxins A, B, E, F producing Clostridium botulinum, Clostridium baratii and Clostridium butyricum. J Appl Microbiol, 107, 465–473.
  • Feldstein MJ, Golden JP, Rowe CA, Maccraith BD, Ligler FS. (1999). Array biosensor: optical and fluidics systems. Biomed Microdevices, 1, 139–153.
  • Fenicia L, Fach P, van Rotterdam BJ, Anniballi F, Segerman B, Auricchio B, Delibato E, Hamidjaja RA, Wielinga PR, Woudstra C, Agren J, De Medici D, Knutsson R. (2011). Towards an international standard for detection and typing botulinum neurotoxin-producing Clostridia types A, B, E and F in food, feed and environmental samples: a European ring trial study to evaluate a real-time PCR assay. Int J Food Microbiol, 145 Suppl 1, S152–S157.
  • Ferracci G, Marconi S, Mazuet C, Jover E, Blanchard MP, Seagar M, Popoff M, Lévêque C. (2011). A label-free biosensor assay for botulinum neurotoxin B in food and human serum. Anal Biochem, 410, 281–288.
  • Ferreira JL. (2001). Comparison of amplified ELISA and mouse bioassay procedures for determination of botulinal toxins A, B, E, and F. J AOAC Int, 84, 85–88.
  • Ferreira JL, Eliasberg SJ, Edmonds P, Harrison MA. (2004). Comparison of the mouse bioassay and enzyme-linked immunosorbent assay procedures for the detection of type A botulinal toxin in food. J Food Prot, 67, 203–206.
  • Frisk ML, Tepp WH, Johnson EA, Beebe DJ. (2009). Self-assembled peptide monolayers as a toxin sensing mechanism within arrayed microchannels. Anal Chem, 81, 2760–2767.
  • Gessler F, Pagel-Wieder S, Avondet MA, 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.
  • Goldman ER, Anderson GP, Conway J, Sherwood LJ, Fech M, Vo B, Liu JL, Hayhurst A. (2008). Thermostable llama single domain antibodies for detection of botulinum A neurotoxin complex. Anal Chem, 80, 8583–8591.
  • Goldman ER, Anderson GP, Bernstein RD, Swain MD. (2010). Amplification of immunoassays using phage-displayed single domain antibodies. J Immunol Methods, 352, 182–185.
  • Grate JW, Warner MG, Ozanich RM Jr, Miller KD, Colburn HA, Dockendorff B, Antolick KC, Anheier NC Jr, Lind MA, Lou J, Marks JD, Bruckner-Lea CJ. (2009). Renewable surface fluorescence sandwich immunoassay biosensor for rapid sensitive botulinum toxin detection in an automated fluidic format. Analyst, 134, 987–996.
  • Hakami RM, Ruthel G, Stahl AM, Bavari S. (2010). Gaining ground: assays for therapeutics against botulinum neurotoxin. Trends Microbiol, 18, 164–172.
  • Hall YH, Chaddock JA, Moulsdale HJ, Kirby ER, Alexander FC, Marks JD, Foster KA. (2004). Novel application of an in vitro technique to the detection and quantification of botulinum neurotoxin antibodies. J Immunol Methods, 288, 55–60.
  • Han SM, Cho JH, Cho IH, Paek EH, Oh HB, Kim BS, Ryu C, Lee K, Kim YK, Paek SH. (2007). Plastic enzyme-linked immunosorbent assays (ELISA)-on-a-chip biosensor for botulinum neurotoxin A. Anal Chim Acta, 587, 1–8.
  • Hill BJ, Skerry JC, Smith TJ, Arnon SS, Douek DC. (2010). Universal and specific quantitative detection of botulinum neurotoxin genes. BMC Microbiol, 10, 267.
  • Kalb SR, Goodnough MC, Malizio CJ, Pirkle JL, Barr JR. (2005). Detection of botulinum neurotoxin A in a spiked milk sample with subtype identification through toxin proteomics. Anal Chem, 77, 6140–6146.
  • Kalb SR, Lou J, Garcia-Rodriguez C, Geren IN, Smith TJ, Moura H, Marks JD, Smith LA, Pirkle JL, Barr JR. (2009). 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, e5355.
  • Kalb SR, Garcia-Rodriguez C, Lou J, Baudys J, Smith TJ, Marks JD, Smith LA, Pirkle JL, Barr JR. (2010). Extraction of BoNT/A, /B, /E, and /F with a single, high affinity monoclonal antibody for detection of botulinum neurotoxin by Endopep-MS. PLoS ONE, 5, e12237.
  • Keller JE, Cai F, Neale EA. (2004). Uptake of botulinum neurotoxin into cultured neurons. Biochemistry, 43, 526–532.
  • Keller JE. (2006). Recovery from botulinum neurotoxin poisoning in vivo. Neuroscience, 139, 629–637.
  • Keller JE, Neale EA, Oyler G, Adler M. (1999). Persistence of botulinum neurotoxin action in cultured spinal cord cells. FEBS Lett, 456, 137–142.
  • Kirchner S, Krämer KM, Schulze M, Pauly D, Jacob D, Gessler F, Nitsche A, Dorner BG, Dorner MB. (2010). Pentaplexed quantitative real-time PCR assay for the simultaneous detection and quantification of botulinum neurotoxin-producing clostridia in food and clinical samples. Appl Environ Microbiol, 76, 4387–4395.
  • 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.
  • Lalli G, Herreros J, Osborne SL, Montecucco C, Rossetto O, Schiavo G. (1999). Functional characterisation of tetanus and botulinum neurotoxins binding domains. J Cell Sci, 112 (Pt 16), 2715–2724.
  • Ligler FS, Taitt CR, Shriver-Lake LC, Sapsford KE, Shubin Y, Golden JP. (2003). Array biosensor for detection of toxins. Anal Bioanal Chem, 377, 469–477.
  • Lillehoj PB, Wei F, Ho CM. (2010). A self-pumping lab-on-a-chip for rapid detection of botulinum toxin. Lab Chip, 10, 2265–2270.
  • Lindström M, Korkeala H. (2006). Laboratory diagnostics of botulism. Clin Microbiol Rev, 19, 298–314.
  • Lindström M, Hinderink K, Somervuo P, Kiviniemi K, Nevas M, Chen Y, Auvinen P, Carter AT, Mason DR, Peck MW, Korkeala H. (2009). Comparative genomic hybridization analysis of two predominant Nordic group I (proteolytic) Clostridium botulinum type B clusters. Appl Environ Microbiol, 75, 2643–2651.
  • Maksymowych AB, Simpson LL. (2004). Structural features of the botulinum neurotoxin molecule that govern binding and transcytosis across polarized human intestinal epithelial cells. J Pharmacol Exp Ther, 310, 633–641.
  • Marconi S, Ferracci G, Berthomieu M, Kozaki S, Miquelis R, Boucraut J, Seagar M, Lévêque C. (2008). A protein chip membrane-capture assay for botulinum neurotoxin activity. Toxicol Appl Pharmacol, 233, 439–446.
  • Mason JT, Xu L, Sheng ZM, O’Leary TJ. (2006). A liposome-PCR assay for the ultrasensitive detection of biological toxins. Nat Biotechnol, 24, 555–557.
  • Mayorov AV, Willis B, Di Mola A, Adler D, Borgia J, Jackson O, Wang J, Luo Y, Tang L, Knapp RJ, Natarajan C, Goodnough MC, Zilberberg N, Simpson LL, Janda KD. (2010). Symptomatic relief of botulinum neurotoxin/a intoxication with aminopyridines: a new twist on an old molecule. ACS Chem Biol, 5, 1183–1191.
  • Min D, Tepp WH, Johnson EA, Chapman ER. (2004). Using fluorescent sensors to detect botulinum neurotoxin activity in vitro and in living cells. Proc Natl Acad Sci USA, 101, 14701–14706.
  • 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.
  • O’Brien T, Johnson LH 3rd, Aldrich JL, Allen SG, Liang LT, Plummer AL, Krak SJ, Boiarski AA. (2000). The development of immunoassays to four biological threat agents in a bidiffractive grating biosensor. Biosens Bioelectron, 14, 815–828.
  • Ozanich RM Jr, Bruckner-Lea CJ, Warner MG, Miller K, Antolick KC, Marks JD, Lou J, Grate JW. (2009). Rapid multiplexed flow cytometric assay for botulinum neurotoxin detection using an automated fluidic microbead-trapping flow cell for enhanced sensitivity. Anal Chem, 81, 5783–5793.
  • Parpura V, Chapman ER. (2005). Detection of botulinum toxins: micromechanical and fluorescence-based sensors. Croat Med J, 46, 491–497.
  • Pauly D, Kirchner S, Stoermann B, Schreiber T, Kaulfuss S, Schade R, Zbinden R, Avondet MA, Dorner MB, Dorner BG. (2009). Simultaneous quantification of five bacterial and plant toxins from complex matrices using a multiplexed fluorescent magnetic suspension assay. Analyst, 134, 2028–2039.
  • Pellett S, Tepp WH, Toth SI, Johnson EA. (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.
  • Pickett A, Perrow K. (2011). Towards new uses of botulinum toxin as a novel therapeutic tool. Toxins (Basel), 3, 63–81.
  • Pires-Alves M, Ho M, Aberle KK, Janda KD, Wilson BA. (2009). Tandem fluorescent proteins as enhanced FRET-based substrates for botulinum neurotoxin activity. Toxicon, 53, 392–399.
  • Raphael BH, Andreadis JD. (2007). Real-time PCR detection of the nontoxic nonhemagglutinin gene as a rapid screening method for bacterial isolates harboring the botulinum neurotoxin (A–G) gene complex. J Microbiol Methods, 71, 343–346.
  • Raphael BH, Joseph LA, McCroskey LM, Lúquez C, Maslanka SE. (2010). Detection and differentiation of Clostridium botulinum type A strains using a focused DNA microarray. Mol Cell Probes, 24, 146–153.
  • Rasetti-Escargueil C, Jones RG, Liu Y, Sesardic D. (2009). Measurement of botulinum types A, B and E neurotoxicity using the phrenic nerve-hemidiaphragm: improved precision with in-bred mice. Toxicon, 53, 503–511.
  • Rasetti-Escargueil C, Liu Y, Rigsby P, Jones RG, Sesardic D. (2011). Phrenic nerve-hemidiaphragm as a highly sensitive replacement assay for determination of functional botulinum toxin antibodies. Toxicon, 57, 1008–1016.
  • Schantz EJ, Johnson EA. (1992). Properties and use of botulinum toxin and other microbial neurotoxins in medicine. Microbiol Rev, 56, 80–99.
  • Sapsford KE, Taitt CR, Loo N, Ligler FS. (2005). Biosensor detection of botulinum toxoid A and staphylococcal enterotoxin B in food. Appl Environ Microbiol, 71, 5590–5592.
  • Satterfield BA, Stewart AF, Lew CS, Pickett DO, Cohen MN, Moore EA, Luedtke PF, O’Neill KL, Robison RA. (2010). A quadruplex real-time PCR assay for rapid detection and differentiation of the Clostridium botulinum toxin genes A, B, E and F. J Med Microbiol, 59, 55–64.
  • Scarlatos A, Cadotte AJ, DeMarse TB, Welt BA. (2008). Cortical networks grown on microelectrode arrays as a biosensor for botulinum toxin. J Food Sci, 73, E129–E136.
  • Schiavo G, Shone CC, Rossetto O, Alexander FC, Montecucco C. (1993). Botulinum neurotoxin serotype F is a zinc endopeptidase specific for VAMP/synaptobrevin. J Biol Chem, 268, 11516–11519.
  • Schmidt JJ, Stafford RG, Millard CB. (2001). High-throughput assays for botulinum neurotoxin proteolytic activity: serotypes A, B, D, and F. Anal Biochem, 296, 130–137.
  • Scotcher MC, Cheng LW, Stanker LH. (2010). Detection of botulinum neurotoxin serotype B at sub mouse LD(50) levels by a sandwich immunoassay and its application to toxin detection in milk. PLoS ONE, 5, e11047.
  • Sharma SK, Eblen BS, Bull RL, Burr DH, Whiting RC. (2005). Evaluation of lateral-flow Clostridium botulinum neurotoxin detection kits for food analysis. Appl Environ Microbiol, 71, 3935–3941.
  • Sharma SK, Ferreira JL, Eblen BS, Whiting RC. (2006). Detection of type A, B, E, and F Clostridium botulinum neurotoxins in foods by using an amplified enzyme-linked immunosorbent assay with digoxigenin-labeled antibodies. Appl Environ Microbiol, 72, 1231–1238.
  • Sharma SK, Whiting RC. (2005). Methods for detection of Clostridium botulinum toxin in foods. J Food Prot, 68, 1256–1263.
  • Sheridan RE, Deshpande SS, Smith T. (1999). Comparison of in vivo and in vitro mouse bioassays for botulinum toxin antagonists. J Appl Toxicol, 19 Suppl 1, S29–S33.
  • Simpson LL. (2004). Identification of the major steps in botulinum toxin action. Annu Rev Pharmacol Toxicol, 44, 167–193.
  • Solomon HM, Lilly TJ. (2001). Clostridium botulinum. In: Bacteriological analytical manual, 8th Ed. Silver Spring, MD, USA: US Food and Drug Administration.
  • Song L, Ahn S, Walt DR. (2006). Fiber-optic microsphere-based arrays for multiplexed biological warfare agent detection. Anal Chem, 78, 1023–1033.
  • Stahl AM, Ruthel G, Torres-Melendez E, Kenny TA, Panchal RG, Bavari S. (2007). Primary cultures of embryonic chicken neurons for sensitive cell-based assay of botulinum neurotoxin: implications for therapeutic discovery. J Biomol Screen, 12, 370–377.
  • Stanker LH, Merrill P, Scotcher MC, Cheng LW. (2008). Development and partial characterization of high-affinity monoclonal antibodies for botulinum toxin type A and their use in analysis of milk by sandwich ELISA. J Immunol Methods, 336, 1–8.
  • Stenmark P, Dupuy J, Imamura A, Kiso M, Stevens RC. (2008). Crystal structure of botulinum neurotoxin type A in complex with the cell surface co-receptor GT1b-insight into the toxin-neuron interaction. PLoS Pathog, 4, e1000129.
  • Swain MD, Anderson GP, Zabetakis D, Bernstein RD, Liu JL, Sherwood LJ, Hayhurst A, Goldman ER. (2010). Llama-derived single-domain antibodies for the detection of botulinum A neurotoxin. Anal Bioanal Chem, 398, 339–348.
  • Volland H, Lamourette P, Nevers MC, Mazuet C, Ezan E, Neuburger LM, Popoff M, Créminon C. (2008). A sensitive sandwich enzyme immunoassay for free or complexed Clostridium botulinum neurotoxin type A. J Immunol Methods, 330, 120–129.
  • Warner MG, Grate JW, Tyler A, Ozanich RM, Miller KD, Lou J, Marks JD, Bruckner-Lea CJ. (2009). Quantum dot immunoassays in renewable surface column and 96-well plate formats for the fluorescence detection of botulinum neurotoxin using high-affinity antibodies. Biosens Bioelectron, 25, 179–184.
  • Wei F, Ho CM. (2009). Aptamer-based electrochemical biosensor for Botulinum neurotoxin. Anal Bioanal Chem, 393, 1943–1948.
  • Welch MJ, Purkiss JR, Foster KA. (2000). Sensitivity of embryonic rat dorsal root ganglia neurons to Clostridium botulinum neurotoxins. Toxicon, 38, 245–258.
  • Wu HC, Huang YL, Lai SC, Huang YY, Shaio MF. (2001). Detection of Clostridium botulinum neurotoxin type A using immuno-PCR. Lett Appl Microbiol, 32, 321–325.
  • Yowler BC, Kensinger RD, Schengrund CL. (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.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.