Hybridoma populations enriched for affinity-matured human IgGs yield high-affinity antibodies specific for botulinum neurotoxins

Journal of Immunological Methods

Volumn 333, Issue 1-2, 2008, Pages 156-166

  Adekar, Sharad P ^a,b   Jones, R Mark ^b   Elias, M D ^b   Al Saleem, Fetweh H ^b   Root, Michael J ^b   Simpson, Lance L ^b   Dessain, Scott K ^a,b  

^a THOMAS JEFFERSON UNIVERSITY HOSPITAL   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Biodefense; Botulinum neurotoxin; Human antibody cloning; Hybridomas

Indexed keywords

15A ANTIBODY; 1A ANTIBODY; 30A ANTIBODY; 6A ANTIBODY; BOTULINUM TOXIN A; BOTULINUM TOXIN B; CD27 ANTIGEN; CD40 LIGAND; CYCLOSPORIN; IMMUNOGLOBULIN G ANTIBODY; TOXOID; UNCLASSIFIED DRUG; VACCINIA VACCINE;

ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HYBRIDOMA; IMMUNE RESPONSE; MOLECULAR CLONING; MOUSE; MYELOMA CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; VACCINIA;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODY SPECIFICITY; ANTIGENS, CD27; B-LYMPHOCYTES; BOTULINUM TOXIN TYPE A; BOTULINUM TOXINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; HYBRIDOMAS; IMMUNOGLOBULIN G; KINETICS; LINEAR MODELS; MICE; NEUTRALIZATION TESTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, BACTERIAL; SURFACE PLASMON RESONANCE;

EID: 41149135281     PISSN: 00221759     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jim.2008.01.015     Document Type: Article

References (47)

1. Adekar S.P., Jones R.M., Elias M.D., Al-Saleem F.H., Root M.J., Simpson L.L., and Dessain S.K. A human monoclonal antibody that binds serotype A botulinum neurotoxin. Hybridoma (Larchmt) 27 (2008) 11
2. 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., and Tonat K. Botulinum toxin as a biological weapon: medical and public health management. JAMA 285 (2001) 1059
3. Banchereau J., and Rousset F. Growing human B lymphocytes in the CD40 system. Nature 353 (1991) 678
4. Brezinschek H.P., Brezinschek R.I., and Lipsky P.E. Analysis of the heavy chain repertoire of human peripheral B cells using single-cell polymerase chain reaction. J. Immunol. 155 (1995) 190
5. Campbell M.J., Zelenetz A.D., Levy S., and Levy R. Use of family specific leader region primers for PCR amplification of the human heavy chain variable region gene repertoire. Mol. Immunol. 29 (1992) 193
6. Carroll W.L., Thielemans K., Dilley J., and Levy R. Mouse × human heterohybridomas as fusion partners with human B cell tumors. J. Immunol. Methods 89 (1986) 61
7. Casadevall A., and Pirofski L.A. The potential of antibody-mediated immunity in the defence against biological weapons. Expert Opin. Biol. Ther. 5 (2005) 1359
8. Chin L.T., Malmborg A.C., Kristensson K., Hinkula J., Wahren B., and Borrebaeck C.A. Mimicking the humoral immune response in vitro results in antigen-specific isotype switching supported by specific autologous T helper cells: generation of human HIV-1-neutralizing IgG monoclonal antibodies from naive donors. Eur. J. Immunol. 25 (1995) 657
9. Coronella J.A., Telleman P., Truong T.D., Ylera F., and Junghans R.P. Amplification of IgG VH and VL (Fab) from single human plasma cells and B cells. Nucleic Acids Res. 28 (2000) E85
10. Coronella J.A., Spier C., Welch M., Trevor K.T., Stopeck A.T., Villar H., and Hersh E.M. Antigen-driven oligoclonal expansion of tumor-infiltrating B cells in infiltrating ductal carcinoma of the breast. J. Immunol. 169 (2002) 1829
11. Darveau A., Chevrier M.C., Neron S., Delage R., and Lemieux R. Efficient preparation of human monoclonal antibody-secreting heterohybridomas using peripheral B lymphocytes cultured in the CD40 system. J. Immunol. Methods 159 (1993) 139
12. de Wildt R.M., Steenbakkers P.G., Pennings A.H., van den Hoogen F.H., van Venrooij W.J., and Hoet R.M. A new method for the analysis and production of monoclonal antibody fragments originating from single human B cells. J. Immunol. Methods 207 (1997) 61
13. Dessain S.K., Adekar S.P., Stevens J.B., Carpenter K.A., Skorski M.L., Barnoski B.L., Goldsby R.A., and Weinberg R.A. High efficiency creation of human monoclonal antibody-producing hybridomas. J. Immunol. Methods 291 (2004) 109
14. Edelhoch H. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6 (1967) 1948
15. Galibert L., van Dooren J., Durand I., Rousset F., Jefferis R., Banchereau J., and Lebecque S. Anti-CD40 plus interleukin-4-activated human naive B cell lines express unmutated immunoglobulin genes with intraclonal heavy chain isotype variability. Eur. J. Immunol. 25 (1995) 733
16. Goossens T., Klein U., and Kuppers R. Frequent occurrence of deletions and duplications during somatic hypermutation: implications for oncogene translocations and heavy chain disease. Proc. Natl. Acad. Sci. U S A 95 (1998) 2463
17. Gray D., Siepmann K., and Wohlleben G. CD40 ligation in B cell activation, isotype switching and memory development. Semin. Immunol. 6 (1994) 303
18. Greene W.H. Econometric Analysis (2000), Prentice-Hall, Upper Saddle River, NJ
19. Grimaitre M., Werner-Favre C., Kindler V., and Zubler R.H. Human naive B cells cultured with EL-4 T cells mimic a germinal center-related B cell stage before generating plasma cells. Concordant changes in Bcl-2 protein and messenger RNA levels. Eur. J. Immunol. 27 (1997) 199
20. Hooper J.W., Custer D.M., and Thompson E. Four-gene-combination DNA vaccine protects mice against a lethal vaccinia virus challenge and elicits appropriate antibody responses in nonhuman primates. Virology 306 (2003) 181
21. Kiyatkin N., Maksymowych A.B., and Simpson L.L. Induction of an immune response by oral administration of recombinant botulinum toxin. Infect. Immun. 65 (1997) 4586
22. Klein U., Kuppers R., and Rajewsky K. Evidence for a large compartment of IgM-expressing memory B cells in humans. Blood 89 (1997) 1288
23. Klein U., Rajewsky K., and Kuppers R. Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J. Exp. Med. 188 (1998) 1679
24. Kuritani T., and Cooper M.D. Human B cell differentiation. II. Pokeweed mitogen-responsive B cells belong to a surface immunoglobulin D-negative subpopulation. J. Exp. Med. 155 (1982) 1561
25. Larrick J.W., Truitt K.E., Raubitschek A.A., Senyk G., and Wang J.C. Characterization of human hybridomas secreting antibody to tetanus toxoid. Proc. Natl. Acad. Sci. U S A 80 (1983) 6376
26. Lefranc M.P., Giudicelli V., Kaas Q., Duprat E., Jabado-Michaloud J., Scaviner D., Ginestoux C., Clement O., Chaume D., and Lefranc G. IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res. 33 (2005) D593
27. Lewis F.M., Chernak E., Goldman E., Li Y., Karem K., Damon I.K., Henkel R., Newbern E.C., Ross P., and Johnson C.C. Ocular vaccinia infection in laboratory worker, Philadelphia, 2004. Emerg. Infect. Dis. 12 (2006) 134
28. Luginbuhl B., Kanyo Z., Jones R.M., Fletterick R.J., Prusiner S.B., Cohen F.E., Williamson R.A., Burton D.R., and Pluckthun A. Directed evolution of an anti-prion protein scFv fragment to an affinity of 1 pM and its structural interpretation. J. Mol. Biol. 363 (2006) 75
29. Maksymowych A.B., and Simpson L.L. Structural features of the botulinum neurotoxin molecule that govern binding and transcytosis across polarized human intestinal epithelial cells. J. Pharmacol. Exp. Ther. 310 (2004) 633
30. Malisan F., Briere F., Bridon J.M., Harindranath N., Mills F.C., Max E.E., Banchereau J., and Martinez-Valdez H. Interleukin-10 induces immunoglobulin G isotype switch recombination in human CD40-activated naive B lymphocytes. J. Exp. Med. 183 (1996) 937
31. Mayr A. Smallpox vaccination and bioterrorism with pox viruses. Comp. Immunol. Microbiol. Infect. Dis. 26 (2003) 423
32. Nowakowski A., Wang C., Powers D.B., Amersdorfer P., Smith T.J., Montgomery V.A., Sheridan R., Blake R., Smith L.A., and Marks J.D. Potent neutralization of botulinum neurotoxin by recombinant oligoclonal antibody. Proc. Natl. Acad. Sci. U S A 99 (2002) 11346
33. Pearce L.B., Borodic G.E., First E.R., and MacCallum R.D. Measurement of botulinum toxin activity: evaluation of the lethality assay. Toxicol. Appl. Pharmacol. 128 (1994) 69
34. Pless D.D., Torres E.R., Reinke E.K., and Bavari S. High-affinity, protective antibodies to the binding domain of botulinum neurotoxin type A. Infect. Immun. 69 (2001) 570
35. Ravichandran E., Gong Y., Al Saleem F.H., Ancharski D.M., Joshi S.G., and Simpson L.L. An initial assessment of the systemic pharmacokinetics of botulinum toxin. J. Pharmacol. Exp. Ther. 318 (2006) 1343
36. Razai A., Garcia-Rodriguez C., Lou J., Geren I.N., Forsyth C.M., Robles Y., Tsai R., Smith T.J., Smith L.A., Siegel R.W., Feldhaus M., and Marks J.D. Molecular evolution of antibody affinity for sensitive detection of botulinum neurotoxin type A. J. Mol. Biol. 351 (2005) 158
37. Rudolphi U., Rzepka R., Batsford S., Kaufmann S.H., von der Mark K., Peter H.H., and Melchers I. The B cell repertoire of patients with rheumatoid arthritis. II. Increased frequencies of IgG+ and IgA+ B cells specific for mycobacterial heat-shock protein 60 or human type II collagen in synovial fluid and tissue. Arthritis Rheum. 40 (1997) 1409
38. Schultze J.L., Michalak S., Seamon M.J., Dranoff G., Jung K., Daley J., Delgado J.C., Gribben J.G., and Nadler L.M. CD40-activated human B cells: an alternative source of highly efficient antigen presenting cells to generate autologous antigen-specific T cells for adoptive immunotherapy. J. Clin. Invest. 100 (1997) 2757
39. Simpson L.L. Identification of the major steps in botulinum toxin action. Annu. Rev. Pharmacol. Toxicol. 44 (2004) 167
40. Simpson L.L., Lake P., and Kozaki S. Isolation and characterization of a novel human monoclonal antibody that neutralizes tetanus toxin. J. Pharmacol. Exp. Ther. 254 (1990) 98
41. Tangye S.G., Liu Y.J., Aversa G., Phillips J.H., and de Vries J.E. Identification of functional human splenic memory B cells by expression of CD148 and CD27. J. Exp. Med. 188 (1998) 1691
42. Thompson J.M., Lowe J., and McDonald D.F. Human monoclonal anti-D secreting heterohybridomas from peripheral B lymphocytes expanded in the CD40 system. J. Immunol. Methods 175 (1994) 137
43. Tian C., Luskin G.K., Dischert K.M., Higginbotham J.N., Shepherd B.E., and Crowe Jr. J.E. Evidence for preferential Ig gene usage and differential TdT and exonuclease activities in human naive and memory B cells. Mol. Immunol. 44 (2007) 2173
44. Traggiai E., Becker S., Subbarao K., Kolesnikova L., Uematsu Y., Gismondo M.R., Murphy B.R., Rappuoli R., and Lanzavecchia A. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat. Med. 10 (2004) 871
45. Weber M., Weiss E., and Engel A.M. Combining EL4-B5-based B-cell stimulation and phage display technology for the successful isolation of human anti-Scl-70 autoantibody fragments. J. Immunol. Methods 278 (2003) 249
46. Wen L., Hanvanich M., Werner-Favre C., Brouwers N., Perrin L.H., and Zubler R.H. Limiting dilution assay for human B cells based on their activation by mutant EL4 thymoma cells: total and antimalaria responder B cell frequencies. Eur. J. Immunol. 17 (1987) 887
47. Werner-Favre C., Bovia F., Schneider P., Holler N., Barnet M., Kindler V., Tschopp J., and Zubler R.H. IgG subclass switch capacity is low in switched and in IgM-only, but high in IgD+IgM+, post-germinal center (CD27+) human B cells. Eur. J. Immunol. 31 (2001) 243