Antimicrobial peptides: New recognition molecules for detecting botulinum toxins

Sensors

Volumn 7, Issue 11, 2007, Pages 2808-2824

  Kulagina, Nadezhda V ^a   Anderson, George P ^a   Ligler, Frances S ^a   Shaffer, Kara M ^a   Taitt, Chris Rowe ^a  

^a NAVAL RESEARCH LABORATORY   (United States)

Author keywords

Antimicrobial peptide; Array; Biosensor; Botulinum toxin; Detection

Indexed keywords

ANTIBODIES; BIOSENSORS; CHEMICAL DETECTION; ERROR DETECTION; METABOLITES; MICROORGANISMS; PEPTIDES; POLYPEPTIDES;

ACTIVE TOXINS; ANTIMICROBIAL PEPTIDE; ARRAY; ARRAY BIOSENSORS; BINDING PATTERN; BOTULINUM TOXINS; DETECTION SENSITIVITY; RECOGNITION ELEMENT;

TOXIC MATERIALS;

EID: 36849045621     PISSN: 14243210     EISSN: 14248220     Source Type: Journal    
DOI: 10.3390/s7112808     Document Type: Article

References (81)

1. Wein, L.M.; Liu, Y. Analyzing a bioterror attack on the food supply: The case of botulinum toxin in milk. Proc. Natl. Acad. Sci. USA 2005, 102, 9984-9989.
2. CDC. Botulism in the United States 1899-1996: Handbook for Epidemiologists, Clinicians, and Laboratory Workers; Centers for Disease Control and Prevention: Atlanta, GA, 1998.
3. Tacket, O.; Shandera, W.X.; Mann, J.M.; Hargrett, N.T.; Blake, P.A. Equine antitoxin use and other factors that predict outcome in type A foodborne botulism. Am. J. Med. 1984, 76, 794-798.
4. Falkenrath, R.A.; Newman, R.D.; Thayer, B.A. Americas's Achilles Heel. Nuclear, Biological and Chemical Terrorism and Covert Attack; MIT Press: Cambridge, MA, 1998.
5. Gill, M.D. Bacterial toxins: a table of lethal amounts. Microbiol Rev. 1982, 46, 86-94.
6. National Institute of Occupational Safety and Health. Registry of Toxic Effects of Chemical Substances (R-TECS). National Institute of Occupational Safety and Health: Cincinnati, Ohio, 1996.
7. Schantz, E.J.; Johnson, E.A. Properties and use of botulinum toxin and other microbial neurotoxins in medicine. Microbiol Rev. 1992, 56, 80-99.
8. Centers for Disease Control and Prevention. Botulism in the United States 1899-1996: Handbook for Epidemiologists, Clinicians, and Laboratory Workers. Centers for Disease Control and Prevention: Atlanta, Ga, 1998. http://www.cdc.gov/ncidod/dbmd/diseaseinfo/botulism.pdf.
9. Salomon, H.M.; Lilly, T. Jr. In Bacteriological Analytical Manual Online, http://www.cfsan.fda.gov/3bam/bam-17.htm#authors. Accessed 17 Oct. 2007.
10. Doellgast, G.J.; Triscott, M.X.; Beard, G.A.; Bottoms, J.D.; Cheng, T.; Roh, B.H.; Roman, M.G.; Hall, P.A.; Brown, J.E. Sensitive enzyme-linked immunosorbent assay for detection of Clostridium botulinum neurotoxins A, B, and E using signal amplification via enzyme-linked coagulation assay. J. Clin. Microbiol. 1993, 31, 2402-2409.
11. Wictome, M.; Newton, K.; Jameson, K.; Hallis, B.; Dunnigan, P.; MacKay, E.; Clarke, S.; Taylor, R.; Gaze, J.; Foster, K.; Shone, C. Development of an in vitro bioassay for Clostridium botulinum type B neurotoxin in foods that is more sensitive than the mouse bioassay. Appl. Environ. Microbiol. 1999, 65, 3787-3792.
12. Chao, H.-Y.; Wang, Y.-C.; Tang, S.-S.; Liu, H.-W. A highly sensitive immuno-polymerase chain reaction assay for Clostridium botulinum neurotoxin type A. Toxicon 2004, 43, 27-34.
13. Boyer, A.E.; Moura, H.; Woolfitt, A.R.; Kalb, S.R.; McWilliams, L.G.; Pavlopoulos, A.; Schmidt, J.G.; Ashley, D.L.; Barr, J. R. From the mouse to the mass spectrometer: Detection and differentiation of the endoproteinase activities of botulinum neurotoxins A-G by mass spectrometry. Anal. Chem. 2005, 77, 3916-3924.
14. Liu, W.; Montana, V.; Chapman, E.R.; Mohideen, U.; Parpura, V. Botulinum toxin type B micromechanosensor. Proc. Natl. Acad. Sci. USA 2003, 100, 13621-13625.
15. Rivera, V.R.; Gamez, F.J.; Keener, W.K.; White, J.A.; Poli, M.A. Rapid detection of Clostridium botulinum toxins A, B, E, and F in clinical samples, selected food matrices, and buffer using paramagnetic bead-based electrochemiluminescence detection. Anal. Biochem. 2006, 353, 248-256.
16. Kulagina, N.V.; Lassman, M.E.; Ligler, F.S.; Taitt, C.R. Antimicrobial peptides for detection of bacteria in biosensor assays. Anal. Chem. 2005, 77, 6504-6408.
17. Kulagina, N.V.; Shaffer, K.S.; Anderson G.W.; Ligler, F.S.; Taitt, C.R. Antimicrobial peptide-based array for Escherichia coli and Salmonella screening. Anal. Chim. Acta 2006, 575, 9-15.
18. Kulagina, N. K.; Shaffer, K. M.; Ligler, F. S.; Taitt, C. R. Antimicrobial peptides, new recognition molecules for challenging targets. Sens. Actuators B 2007, 121, 150-157.
19. Hancock, R.E.W.; Chapple, D.S. Peptide antibiotics. Antimicrob. Agents Chemother. 1999, 43, 1317-1323.
20. Matsuzaki, K. Why and how are peptide-lipid interactions utilized for self defence? Biochem. Soc. Trans. 2001, 29, 598-601.
21. Papo, N.; Shai, Y. Exploring peptide membrane interaction using surface plasmon resonance: differentiation between pore formation versus membrane disruption by lytic peptides. Biochemistry 2003, 42, 458-466.
22. Andreu, D.; Rivas, L. 1999. Animal antimicrobial peptides: an overview. Biopolymers 1999, 47, 415-433.
23. Cleveland, J.; Montville, T. J.; Nes, I. F., Chikindas, M. L. Bacteriocins: safe natural antimicrobials for food preservation. J. Food Microbiol. 2001, 71, 1-20.
24. Garcia, G.E.; Moorad, D.R.; Gordon, R.K. Buforin I, a natural peptide, inhibits botulinum neurotoxin B activity in vitro. J. Appl. Toxicol. 1999, 19, S19-S22.
25. Garcia, G.E.; Gordon, R.K.; Moorad, D.R.; Doctor, B.P. Buforin I as a specific inhibitor and therpeutic agent for botulinum toxin B and tetanus neurotoxins. US Patent No. 6,713,444. 2004.
26. Gordon, R.K.; Moorad, D.R.; Doctor, B.P.; Garcia, G.E. Previns as specific inhibitors and therapeutic agents for botulinum toxin B and tetanus neurotoxins. US Patent No. 7,235,521. 2007.
27. Rowe-Taitt, C.R.; Golden, J.P.; Feldstein, M.J.; Gras, J.J.; Hoffman, K.E.; Ligler, F.S. Array biosensor for detection of biohazards. Biosens. Bioelectron. 2000, 14, 785-794.
28. Sapsford, K.E.; Taitt, C.R; Loo, N.; Ligler, F.S. Biosensor detection of botulinum toxoid A and staphylococcal enterotoxin B in food. Appl. Environ. Microb. 2005, 71, 5590-5592.
29. Cruciani, R.A.; Barker, J.L.; Zasloff, M.; Chen, H.-C.; Colamonici, O. Antibiotic magainins exert cytolytic activity against transformed cell lines through channel formation. Proc. Natl. Acad. Sci. USA 1991, 88, 3792-3796.
30. Bechinger, B.; Zasloff, M.; Opella, S.J. Structure and orientation of the antibiotic peptide magainin in membranes by solid-state nuclear magnetic resonance spectroscopy Prot. Sci. 1993, 2, 2077-2084.
31. Matsuzaki, K.; Mitani, Y.; Akada, K.; Murase, O.; Yaneyama, S.; Zasloff, M.; Miyajima, K. Mechanism of synergism between antimicrobial peptides magainin 2 and PGLa. Biochemistry 1998, 37, 15144-15153.
32. Matsuzaki, K. Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1999, 1462, 1-10
33. Franciosa, G.; Fenicia, L.; Pourshaban, M.; Aureli, P. Recovery of a strain of Clostridium botulinum producing both neurotoxin A and neurotoxin B from canned macrobiotic food. Appl. Environ. Microbiol. 1997, 63, 1148-1150.
34. Kirma, N.; Ferreira, J.L.; Baumstark, B.R. Characterization of six type A strains of Clostridium botulinum that contain type B toxin gene sequences. FEMS Microbiol. Lett. 2004, 231, 159-164.
35. Lindström, M.; Korkeala, H. Laboratory diagnostics of botulism. Clin. Microbiol. Rev. 2006, 19, 298-314.
36. Schmidt, J. J.; Stafford, R. G.; Bostian, K. A. Type A botulinum neurotoxin proteolytic activity: development of competitive inhibitors and implications for substrate specificity at the S1' binding subsite. FEBS Lett. 1998, 435, 61-64.
37. Schmidt, J. J.; Stafford, R. G. A high-affinity competitive inhibitor of type A botulinum neurotoxin protease activity. FEBS Lett. 2002, 532, 423-426.
38. Oost, T.; Sukonpan, C.; Brewer, M.; Goodnough, M.; Tepp, W.; Johnson, E. A.; Rich, D. H. Design and synthesis of substrate-based inhibitors of botulinum neurotoxin type B metalloprotease. Biopolymers 2003, 71, 602-619.
39. Anne, C.; Turcaud, S; Quancard, J.; Teffo, F.; Meudal, H.; Fournie-Zaluski, M. C; Roques, B. P. Development of potent inhibitors of botulinum neurotoxin type B. J. Med. Chem. 2003, 46, 4648-4656.
40. Sukonpan, C.; Oost, T.; Goodnough, M.; Tepp, W.; Johnson, E. A.; Rich, D. H. Synthesis of substrates and inhibitors of botulinum neurotoxin type A metalloprotease. J. Peptide Res. 2004, 63, 181-193.
41. Schmidt, J.J.; Stafford, R.G. Botulinum neurotoxin serotype F: identification of substrate recognition requirements and development of inhibitors with low nanomolar affinity. Biochemistry 2005, 44, 4067-4073.
42. Schaivo, G.; Benfenati, F.; Poulain, B.; Rossetto, O.; Polverino de Laureto, P.; DasGupta, B. R.; Montecucco, C Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 1992, 359, 832-835
43. Schaivo, G.; Rossetto, O.; Catsicas, S.; Delaureto, P. P.; DasGeupta, B. R.; Benefenati, F.; Montecucco, C Identification of the nerve terminal targets of botulinum neurotoxin serotypes A, D, and E. J. Biol. Chem. 1993, 268, 23784-23787.
44. Schaivo, G.; Santucci, A.; DasGupta, B. R.; Mehta, P. P.; Jones, J.; Benefenati, F.; Wilson, M. C.; Montecucco, C Botulinum neurotoxins serotypes A and E cleave SNAP-25 at distinct COOH-terminal peptide bonds. FEBS Lett. 1993, 335, 99-103.
45. Moore, G.J.; Moore, D.M.; Roy, S.S.; Hayden, L.J.; Hamilton, M.G.; Chan, N.W.C.; Lee, W.E. Hinge peptide combinatorial libraries for inhibitors of botulinum neurotoxins and saxitoxin: Deconvolution strategy. Mol. Divers. 2006, 10, 9-16.
46. Clark, G.C; Basak, A.K.; Titball, R.W. The rational design of bacterial toxin inhibitors. Curr. Computer-Aided Drug Des. 2007, 3, 1-12.
47. Hanson, M. A.; Stevens, R. C Cocrystal structure of synaptobrevin-II bound to botulinum neurotoxin type B at 2.0 A resolution. Nat. Struct. Biol. 2000, 7, 687-692.
48. Segelke, B.; Knapp, M.; Kankhodayan, S.; Balhorn, R.; Rupp, B. Crystal structure of Clostridium botulinum neurotoxin protease in a productbound state: Evidence for noncanonical zinc protease activity. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 6888-6893.
49. Arndt, J. W.; Chai, Q.; Christian, T.; Stevens, R. C Structure of botulinum neurotoxin type D light chain at 1.65 Åresolution - Repercussions into VAMP-2 substrate specificity. Biochemistry 2006, 45, 3255-3262.
50. Montecucco, C.; Schaivo, G. Structure and function of tetanus and botulinum neurotoxins. Quart. Rev. Biophys. 1995, 4, 423-472.
51. Breidenbach, M. A.; Brunger, A. T. Substrate recognition strategy for botulinum neurotoxin serotype A. Nature 2004, 432, 925-929.
52. Breidenbach, M. A.; Brunger, A. T. New insights into clostridial neurotoxin-SNARE interactions. Trends Mol. Med. 2005, 11, 377-381.
53. Washbourne, P.; Pellizari R.; Baldini, G.; Wilson, M. C.; Montecucco, C. Botulinum neurotoxin types A and E require the SNARE motif in SNAP-25 for proteolysis. FEBS Lett. 1997, 418, 1-5.
54. Eswaramoorthy, S.; Kumaran, D.; Swaminathan, S. Crystallographic evidence for doxorubicin binding to the receptor-binding site in Clostridium botulinum neurotoxin B. Acta Cryst. 2001, D57, 1743-1746.
55. Kitamura, M.; Sakaguchi, S.; Sakaguchi, G. Significance of 12S toxin of Clostridium botulinum Type E. J Bacteriol. 1969, 98, 1173-1178.
56. Sugii, S.; Ohishi, I.; Sakaguchi, G. Correlation between oral toxicity and in vitro stability of Clostridium botulinum type A and B toxins of different molecular sizes. Infect. Immunol. 1977, 16, 910-914.
57. Sakaguchi, G. Clostridium botulinum toxins. Pharmac. Ther. 1983, 19, 165-194.
58. Ogert, R. A.; Brown, J. E.; Singh, B. R.; Shriver-Lake, L. C., Ligler, F. S. Detection of Clostridium botulinum toxin A using a fiber optic-based biosensor. Anal. Biochem. 1992, 205, 306-312.
59. Kumar, P.; Colston, J. T.; Chambers, J. P.; Rael, E. D.; Valdes, J. J. Detection of botulinum toxin using an evanescent wave immunosensor. Biosens. Bioelectron. 1991, 9, 57-63.
60. Singh, B. R.; Silva, M. Detection of botulinum neurotoxins using optical fiber-based biosensor. Adv. Exp. Med. Biol. 1996, 391, 499-508.
61. O'Brien, T.; Johnson, L. H. III; Aldrich, J. L.; Allen, S. G.; Liang, L.-T.; Plummer, A. L.; Krak, S. J.; Boiarski, A. A. The development of immunoassays to four biological threat agents in a bidiffractive grating biosensor. Biosens. Bioelectron. 2000, 14, 815-828.
62. Peruski, A. H.; Johnson, L. H. III; Peruski, L. F., Jr. Rapid and sensitive detection of biological warfare agents using time-resolved fluorescence assays. J. Immunol. Methods 2002, 263, 35-41.
63. Sharma, S. K.; Eblen, B. S.; Bull, R. L.; Burr, D. H.; Whiting, R. C Evaluation of lateral-flow Clostridium botulinum neurotoxin detection kits for food analysis. Appl. Environ. Microbiol. 2005, 71, 3935-3941.
64. Urbanowicz, R. Reassessment of a ganglioside-liposome biosensor; M. Eng. Thesis, Cornell Univ.: Ithaca, NY, 2005.
65. Barr, J. R.; Moura, H.; Boyer, A. E.; Woolfitt, A. R.; Kalb, S. R.; Pavlopoulos, A.; McWilliams, L. G.; Schmidt, J. G.; Martinez, R. A.; Ashley D. L. Botulinum neurotoxin detection and differentiation by mass spectrometry. Emerg. Infect. Dis. 2005, 11, 1578-1583.
66. Schmidt, J.J.; Stafford, R.G.; Millard, C.B. High-throughput assays for botulinum neurotoxin proteolytic activity: serotypes A, B, D, and F. Anal. Biochem. 2001, 296, 130-137
67. Hancock, R.E.W.; Sahn, H.-G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nature Biotechnol. 2006, 24, 1551-1557.
68. Sharma, S. K.; Ferreira, J. L.; Eblen, B. S.; Whiting, R. C. 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. 2006, 72, 1231-1238.
69. Fach, P.; Perelle, S.; Dilassar, F.; Grout, J.; Dargaignaratz, C.; Botella, L.; Gorreau, J.M.; Carlin, F.; Popoff, M.R.; Brousalle, V. Detection by PCR-enzyme-linked immunosorbent assay of Clostridium botulinum in fish and environmental samples from a coastal area in northern France. Appl. Environ. Microbiol. 2002, 68, 5870-5876.
70. Poli, M.A.; Rivera, V.R.; Neal, D. Development of sensitive colorimetric capture ELISAs for Clostridium botulinum neurotoxin serotypes E and F. Toxicon 2002, 40, 797-802.
71. Ferreira, J.L.; Maslanka, S.; Johnson, E.; Goodnough, M. Detection of preformed type A botulinal toxin in hash brown potatoes by using the mouse bioasssay and a modified ELISA test. J. AOAC 2003, 84, 1460-1464.
72. Ma, H.; Zhou, B.; Kim, Y.S.; Jana, K.D. A cyclic peptide-polymer probe for the detection of Clostridium botulinum neurotoxin serotype A. Toxicon 2006, 47, 901-908.
73. Shone, C.; Wilton-Smith, P.; Appleton, N.; Hambleton, P.; Modi, N.; Gatley, S.; Melling, J. Monoclonal antibody-based immunoassay for type A Clostridium botulinum toxin is comparable to the mouse bioassay. Appl. Environ. Microbiol. 1985, 50, 63-67.
74. Ekong, T. A. N.; McLellan, K.; Sesardic, D. Immunological detection of Clostridium botulinum toxin type A in therapeutic preparations. J. Immunol. Methods 1995, 180, 181-191.
75. Singh, A.K.; Harrison, S.H.; Schoninger, J.S. Gangliosides as receptors for biological toxins: Development of sensitive fluoroimmunoassays using ganglioside-bearing liposomes. Anal. Chem. 2000, 72, 6019-6024.
76. Ahn-Yoon, S.; DeCrory, T.R.; Durst, R.A. Ganglioside-lipsosome immunoassay for the detection of botulinum toxin. Anal. Bioanal. Chem. 2004, 378, 68-75.
77. Wu, H.C; Huang, Y.L.; Lai, S.C.; Huang, Y.Y.; Shaio, M.F. Detection of Clostridium botulinum neurotoxin type A using immuno-PCR. Lett. Appl. Microbiol. 2001, 32, 321-325.
78. Chao, H.-Y.; Wang, Y.-C.; Tang, S.-S.; Liu, H.W. A highly sensitive immuno-polymerase chain reaction assay for Clostridium botulinum neurotoxin type A. Toxicon 2004, 43, 27-34.
79. Mason, J.T.; Xu, L.; Sheng, Z.-M.; O'Leary, T.J. A liposome-PCR assay for the ultrasensitive detection of biological toxins. Nature Biotechnol. 2006, 24, 555-557.
80. Edwards, K. A.; Baeumner, A.J. Analysis of liposomes. Talanta 2006, 68, 1432-1441.
81. Ngundi, M. M.; Taitt, C. R.; Ligler, F. S. Simultaneous determination of kinetic parameters for the binding of cholera toxin to immobilized sialic acid and monoclonal antibody using an array biosensor. Biosens. Bioelectron. 2006, 22, 124-130.