Immune recognition of botulinum neurotoxin B: Antibody-binding regions on the heavy chain of the toxin

Molecular Immunology

Volumn 45, Issue 4, 2008, Pages 910-924

  Dolimbek, Behzod Z ^a   Steward, Lance E ^b   Aoki, K Roger ^b   Atassi, M Zouhair ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b ALLERGAN INC   (United States)

Author keywords

Antibodies; Antigenic sites; Antigens; Botulinum neurotoxin B; Epitopes; Immune recognition; Synthetic peptides

Indexed keywords

BOTULINUM TOXIN B; PEPTIDE DERIVATIVE; SYNAPTOTAGMIN II;

ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; HEAVY CHAIN; HORSE; HOST; HYDROPHILICITY; HYDROPHOBICITY; PRIORITY JOURNAL; TEMPERATURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES, ANTIBODY; BOTULINUM TOXINS; EPITOPE MAPPING; HORSES; HUMANS; IMMUNE SERA; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS;

EQUIDAE; RATTUS;

EID: 35548984968     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2007.08.007     Document Type: Article

References (80)

1. Ahnert-Hilger G., and Bigalke H. Molecular aspects of tetanus and botulinum neurotoxin poisoning. Prog. Neurobiol. 46 (1995) 83-96
2. Akbulut D., Grant K.A., and McLauchlin J. Development and application of real-time PCR assays to detect fragments of the Clostridium botulinum types A, B, and E neurotoxin genes for investigation of human foodborne and infant botulism. Foodborne Pathog. Dis. 1 (2004) 247-257
3. Atassi M.Z. Antigenic structure of myoglobin. The complete immunochemical anatomy of a protein and conclusions relating to antigenic structures of proteins. Immunochemistry 12 (1975) 423-438
4. Atassi M.Z. Antigenic structures of proteins. Their determination has revealed important aspects of immune recognition and generated strategies for synthetic mimicking of protein binding sites. Eur. J. Biochem. 145 (1984) 1-20
5. Atassi M.Z. Basic immunological aspects of botulinum toxin therapy. Mov. Disord. 19 Suppl. 8 (2004) S68-S84
6. Atassi M.Z. On the enhancement of anti-neurotoxin antibody production by subcomponents HA1 and HA3b of Clostridium botulinum type B 16S toxin-haemagglutinin. Microbiology 52 (2006) 1891-1895
7. Atassi M.Z., and Oshima M. Structure, activity and immune (T and B cell) recognition of botulinum neurotoxin. Crit. Rev. Immunol. 19 (1999) 219-260
8. Atassi M.Z., and Smith J.A. A Proposal for the nomenclature of antigen sites in peptides and proteins. Immunochemistry 15 (1978) 609-610
9. Atassi M.Z., and Dolimbek B.Z. Mapping of the antibody-binding regions on the HN-domain (residues 449-859) of botulinum neurotoxin A with antitoxin antibodies from four host species. Full profile of the continuous antigenic regions of the H-chain of botulinum neurotoxin A. Protein J. 23 (2004) 39-52
10. Atassi M.Z., Manshouri T., and Sakata S. Localization and synthesis of the hormone-binding regions of the human thyrotropin receptor. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 3613-3617
11. Atassi M.Z., Dolimbek G.S., Deitiker P.R., Aoki K.R., and Dolimbek B.Z. Submolecular recognition profiles in two mouse strains of non-protective and protective antibodies against botulinum neurotoxin A. Mol. Immunol. 42 (2005) 1509-1520
12. Atassi M.Z., Yoshioka M., Bean M., and Bixler Jr. G.S. Non-specific peptide size effects in the recognition by site-specific T-cell clones: demonstration with a T site of myoglobin. Biochem. J. 246 (1987) 307-312
13. Atassi M.Z., Dolimbek B.Z., and Manshouri T. Antibody and T-cell recognition of α-bungarotoxin and its synthetic loop peptides. Mol. Immunol. 13 (1995) 927-932
14. Atassi M.Z., Dolimbek B.Z., Hayakari M., Middlebrook J.L., Whitney B., and Oshima M. Mapping of the antibody-binding regions on botulinum neurotoxin H-chain domain 855-1296 with anti-toxin antibodies from three host species. J. Protein Chem. 15 (1996) 691-700
15. Bandyopadhyay S., Clark A.W., Das Gupta B., and Sathyamoorthy V. Role of the heavy and light chains of botulinum neurotoxin in neuromuscular paralysis. J. Biol. Chem. 262 (1987) 2660-2663
16. Becker-Wegerich P.M., Rauch L., and Ruzicka T. Botulinum toxin A: successful decollete rejuvenation. Dermatol. Surg. 28 (2002) 168-171
17. Binder W.J., Brin M.F., Blitzer A., and Pogoda J.M. Botulinum toxin type A (BOTOX) for treatment of migraine. Dis. Mon. 48 (2002) 323-335
18. Bixler Jr. G.S., Bean M., and Atassi M.Z. Site recognition by protein-primed T cells shows a non-specific peptide size requirement beyond the essential residues of the site: demonstration by defining an immunodominant T site in myoglobin. Biochem. J. 240 (1986) 139-146
19. Bixler G.S., and Atassi M.Z. T-cell recognition of myoglobin. Localization of the sites stimulating T-cell proliferative responses by synthetic overlapping peptides encompassing the entire molecule. J. Immunogen. 11 (1984) 339-353
20. Borodic G.E., Acquadro M., and Johnson E.A. Botulinum toxin therapy for pain and inflammatory disorders: mechanisms and therapeutic effects. Expert Opin. Investig. Drugs 10 (2001) 1531-1544
21. Brashear A., McAfee A.L., Kuhn E.R., and Fyffe J. Botulinum toxin type B in upper-limb poststroke spasticity: a double-blind, placebo-controlled trial. Arch. Phys. Med. Rehabil. 85 (2004) 705-709
22. Brooks V.B. An intracellular study of the action of repetitive nerve volleys and of botulinum toxin on miniature end-plate potentials. J. Physiol. 134 (1956) 264-277
23. Burgen A.S.V., Dickens F., and Zatman L.J. The action of botulinum toxin on the neuromuscular junction. J. Physiol. (Lond.) 109 (1949) 10-24
24. Byrne M.P., and Smith L.A. Development of vaccines for prevention of botulism. Biochimie 82 (2000) 955-966
25. Campbell K.D., Collins M.D., and East A.K. Gene probes for identification of the botulinal neurotoxin gene and specific identification of neurotoxin types B, E, and F. J. Clin. Microbiol. 31 (1993) 2255-2262 (Also, B3: C. botulinum (strain non-proteolytic Eklund 2B) gene for neurotoxin type B. Accession # X70819 (ref. same as B2); B4: C. botulinum (strain proteolytic B) gene for neurotoxin type B. Accession # X70817 (ref. same as B2); B5: Clostridium botulinum neurotoxin type B (botB) gene, complete cds Accession # M81186)
26. Cardoso F., and Jankovic J. Clinical use of botulinum neurotoxins. Curr. Top. Microbiol. Immunol. 195 (1995) 123-141
27. Chai Q., Arndt J.W., Dong M., Tepp W.H., Johnson E.A., Chapman E.R., and Stevens R.C. Structural basis of cell surface receptor recognition by botulinum neurotoxin B. Nature 444 (2006) 1096-1100
28. David C.S., and Atassi M.Z. Genetic control and intersite influences on the immune response to sperm whale myoglobin. Adv. Exp. Med. Biol. 150 (1982) 97-126
29. Dickson E.C., and Shevky R. Botulism studies on the manner in which the toxin of Clostridium botulinum acts upon the body. II. The effect on the voluntary nervous system. J. Exp. Med. 37 (1923) 327-346
30. Dickson E.C., and Shevky R. Botulism studies on the manner in which the toxin of Clostridium botulinum acts upon the body. I. The effect upon the autonomic nervous system. J. Exp. Med. 37 (1923) 711-731
31. Dolimbek B.Z., and Atassi M.Z. Protection against α-bungarotoxin poisoning by immunization with synthetic toxin peptides. Mol. Immunol. 33 (1996) 681-689
32. Dolimbek B.Z., Jankovic J., and Atassi M.Z. Cross reaction of tetanus and Botulinum neurotoxins A and B and the boosting effect of Botulinum neurotoxins A and B on a primary anti-tetanus antibody response. Immunol. Investig. 31 (2002) 247-262
33. Dolimbek G.S., Dolimbek B.Z., Aoki K.R., and Atassi M.Z. Mapping of the antibody and T cell recognition profiles of the HN domain (residues 449-859) of the heavy chain of botulinum neurotoxin A in two high-responder mouse strains. Immunol. Invest. 34 (2005) 119-142
34. Dolimbek B.Z., and Atassi M.Z. α-Bungarotoxin peptides afford a synthetic vaccine against toxin poisoning. J. Protein Chem. 13 (1994) 490-493
35. Dressler D., and Bigalke H. Antibody-induced failure of botulinum toxin type B therapy in de novo patients. Eur. Neurol. 52 (2004) 132-135
36. Dressler D., and Bigalke H. Botulinum toxin type B de novo therapy of cervical dystonia. Frequency of antibody induced therapy failure. J. Neurol. 252 (2005) 904-907
37. Dubow J., Kim A., Leikin J., Cumpston K., Bryant S., and Rezak M. Visual system side effects caused by parasympathetic dysfunction after botulinum toxin type B injections. Mov. Disord. 20 (2005) 877-880
38. Fu F.N., Lomneth R.B., Cai S., and Singh B.R. Role of zinc in the structure and toxic activity of botulinum neurotoxin. Biochemistry 37 (1998) 5267-5278
39. Göschel H., Wohlfarth K., Frevert J., Dengler R., and Bigalke H. Botulinum A toxin therapy: neutralizing and nonneutralizing antibodies-therapeutic consequences. Exp. Neurol. 147 (1997) 96-102
40. Gui D., Rossi S., Runfola M., and Magalini S.C. Review article: botulinum toxin in the therapy of gastrointestinal motility disorders. Aliment. Pharmacol. Ther. 18 (2003) 1-16
41. Gundersen C.B. The effects of botulinum toxin on the synthesis, storage and release of acetylcholine. Prog. Neurobiol. 14 (1980) 99-119
42. Hutson R.A., Collins M.D., East A.K., and Thompson D.E. Nucleotide sequence of the gene coding for non-proteolytic Clostridium botulinum type B neurotoxin: comparison with other clostridial neurotoxins. Curr. Microbiol. 28 (1994) 101-110
43. Jankovic J., Hunter C., Dolimbek B.Z., Dolimbek G.S., Adler C.H., Brashear A., Comella C.L., Gordon M., Riley D.E., Sethi K., Singer C., Stacy M., Tarsy D., and Atassi M.Z. Clinico-immunologic aspects of botulinum toxin type B treatment of cervical dystonia. Neurology 67 (2006) 2233-2235
44. Jankovic J., Hunter C., Atassi M.Z., Dolimbek B.Z., Dolimbek G.S., and BOS Research Group. Botulinum toxin type B observational study (BOS). Mov. Disord. 20 Suppl. 10 (2005) S31
45. Jankovic J., Vuong K.D., and Ahsan J. Comparison of efficacy and immunogenicity of original versus current botulinum toxin in cervical dystonia. Neurology 60 (2003) 1186-1188
46. Jankovic J. Botulinum toxin: clinical implications of antigenicity and immunoresistance. In: Brin M.F., Hallett M., and Jankovic J. (Eds). Scientific and Therapeutic Aspects of Botulinum Toxin (2002), Lippincott Williams & Wilkins, Philadelphia, PA 409-415
47. Jankovic J. Botulinum toxin in clinical practice. J. Neurol. Neurosurg. Psychiatry 75 (2004) 951-957
48. Jankovic J. Treatment of cervical dystonia with botulinum toxin. Mov. Disord. 19 Suppl. 8 (2004)
49. Jin R., Rummel A., Binz T., and Brunger A.T. Botulinum neurotoxin B recognizes its protein receptor with high affinity and specificity. Nature 444 (2006) 1092-1095
50. Kazim A.L., and Atassi M.Z. Prediction and confirmation by synthesis of two antigenic sites in human haemoglobin by extrapolation from the known antigenic structure of sperm whale myoglobin. Biochem. J. 167 (1977) 275-278
51. Kazim A.L., and Atassi M.Z. A novel and comprehensive synthetic approach for the elucidation of protein antigenic structures: determination of the full antigenic profile of the α-chain of human haemoglobin. Biochem. J. 191 (1980) 261-264
52. Kazim A.L., and Atassi M.Z. Structurally inherent antigenic sites: localization of the antigenic sites of the α-chain of human haemoglobin in three host species by a comprehensive synthetic approach. Biochem. J. 203 (1982) 201-208
53. Kozaki S., Miyazaki S., and Sakaguchi G. Development of anti-toxin with each of two complementary fragments of Clostridium botulinum type B derivative toxin. Infect. Immun. 18 (1977) 761-766
54. Kozaki S., Kamata Y., Nagai T., Ogasawara J., and Sakaguchi G. The use of monoclonal antibodies to analyze the structure of Clostridium botulinum type E derivative toxin. Infect. Immun. 52 (1986) 786-791
55. Kozaki S., Akira M., Yoichi K., Jun O., and Genji S. Immunological characterization of papain-induced fragments of Clostridium botulinum type A neurotoxin and interaction of the fragments with brain synaptosomes. Infect. Immun. 57 (1989) 2634-2639
56. Kubota T., Watanabe T., Yokosawa N., Tsuzuki K., Indoh T., Moriishi K., Sanda K., Maki Y., Inoue K., and Fujii N. Epitope regions in the heavy chain of Clostridium botulinum type E neurotoxin recognized by monoclonal antibodies. Appl. Environ. Microbiol. 63 (1997) 1214-1218
57. Llamana C. The most poisonous poison. Science 130 (1959) 763-772
58. Maruta T., Dolimbek B.Z., Aoki K.R., Steward L.E., and Atassi M.Z. Mapping of the synaptosome-binding regions on the heavy chain of botulinum neurotoxin A by synthetic overlapping peptides encompassing the entire chain. Protein J. 23 (2004) 539-552
59. Maruta T., Dolimbek B.Z., Aoki K.R., and Atassi M.Z. Inhibition by human sera of botulinum neurotoxin A binding to synaptosomes: a new assay for blocking and non-blocking antibodies. J. Neurosci. Methods 151 (2006) 90-96
60. Middlebrook J.L. Protection strategies against botulinum toxin. Adv. Exp. Med. Biol. 383 (1995) 93-98
61. Nishiki T., Kamata Y., Nemoto Y., Omori A., Ito T., Takahashi M., and Kozaki S. Identification of protein receptor for Clostridium botulinum type B neurotoxin in rat brain synaptosomes. J. Biol. Chem. 269 (1994) 10498-10503
62. Okuda K., Christadoss P.R., Twining S.S., Atassi M.Z., and David C.S. Genetic control of immune response to sperm whale myoglobin in mice. I. T lymphocyte proliferative response under H-2-linked Ir gene control. J. Immunol. 121 (1978) 866-868
63. Okuda K., Twining S.S., David C.S., and Atassi M.Z. Genetic control of immune response to sperm whale myoglobin in mice. II. T lymphocyte proliferative response to the synthetic antigenic sites. J. Immunol. 123 (1979) 182-188
64. C. Immunol. Lett. 60 (1998) 7-12
65. C fragment (residues 855-1296) of the toxin. Mol. Immunol. 34 (1997) 1031-1040
66. Rosenberg J.S., Middlebrook J.L., and Atassi M.Z. Localization of the regions on the C-terminal domain of the heavy chain of botulinum toxin A recognized by T-lymphocytes and by antibodies after immunization of mice with pentavalent toxoid. Immunol. Invest. 26 (1997) 491-504
67. Sakaguchi G., Ohishi I., and Kozaki S. In: Hardgree M.C., and Tu A.T. (Eds). Botulism-Structure and Chemistry of Botulinum in Handbook of Natural Toxins vol. 4 (1988), Marcel Dekker, New York 191-216
68. Schiavo G., Shone C.C., Bennett M.K., Scheller R.H., and Montecucco C. Botulinum neurotoxin type C cleaves a single Lys-Ala bond within the carboxyl-terminal region of syntaxins. J. Biol. Chem. 270 (1995) 10566-10570
69. Schwerin A., Berweck S., Fietzek U.M., and Heinen F. Botulinum toxin B treatment in children with spastic movement disorders: a pilot study. Pediatr. Neurol. 31 (2004) 109-113
70. Silberstein S.D. Review of botulinum toxin type A and its clinical applications in migraine headache. Expert Opin. Pharmacother. 10 (2001) 1649-1654
71. Simpson L.L. Molecular pharmacology of botulinum toxin and tetanus toxin. Ann. Rev. Pharmacol. Toxicol. 26 (1986) 427-453
72. Simpson L.L. The study of clostridial and related toxins. The search for unique mechanisms and common denominators. J. Physiol., Paris 84 (1990) 143-151
73. Swaminathan S., and Eswaramoorthy S. Structural analysis of the catalytic and binding sites of Clostridium botulinum neurotoxin B. Nat. Struct. Biol. 7 (2000) 693-699
74. Thakker M.M., and Rubin P.A. Pharmacology and clinical applications of botulinum toxins A and B. Int. Ophthalmol. Clin. 44 (2004) 147-163
75. Tintner R., Gross R., Winzer U.F., Smalky K.A., and Jankovic J. Autonomic function after botulinum toxin type A or B: a double-blind, randomized trial. Neurology 65 (2005) 765-767
76. Tousi B., Perumal J.S., Ahuja K., Ahmed A., and Subramanian T. Effects of botulinum toxin-B (BTX-B) injections for hemifacial spasm. Parkinsonism Relat. Disord. 10 (2004) 455-456
77. Turton K., Chaddock J.A., and Acharya K.R. Botulinum and tetanus neurotoxins: structure, function and therapeutic utility. Trends Biochem. Sci. 27 (2002) 552-558
78. Twining S.S., David C.S., and Atassi M.Z. Genetic control of the immune response to myoglobin. IV. Mouse antibodies in outbred and congenic strains against sperm whale myoglobin recognize the same antigenic sites that are recognized by antibodies raised in other species. Mol. Immunol. 18 (1981) 447-450
79. C subunits from clostridium types C and D and their evaluation as candidate vaccine antigens in mice. Infect. Immun. 71 (2003) 2941-2944
80. Yoshioka N., and Atassi M.Z. Antigenic structure of human haemoglobin: localization of the antigenic sites of the β-chain in three host species by synthetic overlapping peptides representing the entire chain. Biochem. J. 234 (1986) 441-447