Isolation and characterization of human neutralizing antibodies to rabies virus derived from a recombinant immune antibody library

Journal of Virological Methods

Volumn 161, Issue 2, 2009, Pages 205-215

  Houimel, Mehdi ^a   Dellagi, Koussay ^a  

^a PASTEUR INSTITUTE OF TUNIS   (Tunisia)

Author keywords

Human Fab; Neutralization; Phage display; Rabies virus

Indexed keywords

HISTIDINE; IMMUNOGLOBULIN F(AB) FRAGMENT; NEUTRALIZING ANTIBODY; RABIES VACCINE; RNA; VIRUS GLYCOPROTEIN;

AFFINITY CHROMATOGRAPHY; ANTIBODY ISOLATION; ANTIBODY LIBRARY; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; BINDING COMPETITION; BIOPANNING; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FEMALE; GENE SEQUENCE; GENETIC ANALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE; MALE; NONHUMAN; PHAGEMID; PRIORITY JOURNAL; RABIES; RABIES VIRUS; SEQUENCE HOMOLOGY; VACCINATION; VIRUS GENE; VIRUS NEUTRALIZATION; VOLUNTEER;

ANTIBODIES, VIRAL; EPITOPE MAPPING; FEMALE; GLYCOPROTEINS; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; IMMUNOGLOBULIN VARIABLE REGION; LYMPHOCYTES; MALE; NEUTRALIZATION TESTS; PEPTIDE LIBRARY; RABIES; RABIES VACCINES; RABIES VIRUS; RNA; VIRAL PROTEINS;

ESCHERICHIA COLI; RABIES VIRUS;

EID: 68949167758     PISSN: 01660934     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jviromet.2009.06.018     Document Type: Article

References (67)

1. Anders G., and Vakil H.B. ELISA assays for rabies antibodies?. Hum. Vaccin. 3 (2007) 156
2. Andris-Widhopf J., Rader C., Steinberger P., Fuller R., and Barbas III C.F. Methods for the generation of chicken monoclonal antibody fragments by phage display. J. Immunol. Methods 242 (2000) 159-181
3. Bakker A.B., Marissen W.E., Kramer R.A., Rice A.B., Weldon W.C., Niezgoda M., Hanlon C.A., Thijsse S., Backus H.H., de Kruif J., Dietzschold B., Rupprecht C.E., and Goudsmit J. Novel human monoclonal antibody combination effectively neutralizing natural rabies virus variants and individual in vitro escape mutants. J. Virol. 79 (2005) 9062-9068
4. Bakker A.B., Python C., Kissling C.J., Pandya P., Marissen W.E., Brink M.F., Lagerwerf F., Worst S., van Corven E., Kostense S., Hartmann K., Weverling G.J., Uytdehaag F., Herzog C., Briggs D.J., Rupprecht C.E., Grimaldi R., and Goudsmit J. First administration to humans of a monoclonal antibody cocktail against rabies virus: safety, tolerability, and neutralizing activity. Vaccine 26 (2008) 5922-5927 Epub 2008 September 17
5. Barbas III C.F., Kang A.S., Lerner R.A., and Benkovic S.J. Assembly of combinatorial antibody libraries on phage surfaces: the gene III site. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 7978-7982
6. Bender E., Woof J.M., Atkin J.D., Barker M.D., Bebbington C.R., and Burton D.R. Recombinant human antibodies: linkage of an Fab fragment from a combinatorial library to an Fc fragment for expression in mammalian cell culture. Hum. Antibodies Hybridomas 4 (1993) 74-79
7. Brekke O.H., and Loset G.A. New technologies in therapeutic antibody development. Curr. Opin . Pharmacol. 3 (2003) 544-550
8. Brekke O.H., and Sandlie I. Therapeutic antibodies for human diseases at the dawn of the twenty-first century. Nat. Rev. Drug. Discov. 2 (2003) 52-62
9. Carrieri M.L., Peixoto Z.M., Paciencia M.L., Kotait I., and Germano P.M. Laboratory diagnosis of equine rabies and its implications for human postexposure prophylaxis. J. Virol. Methods 138 (2006) 1-9 Epub 2006 August 21
10. Casadevall A., Dadachova E., and Pirofski L.A. Passive antibody therapy for infectious diseases. Nat. Rev. Microbiol. 2 (2004) 695-703
11. Celis E., Karr R.W., Dietzschold B., Wunner W.H., and Koprowski H. Genetic restriction and fine specificity of human T cell clones reactive with rabies virus. J. Immunol. 141 (1988) 2721-2728
12. Cleaveland S., Kaare M., Tiringa P., Mlengeya T., and Barrat J. A dog rabies vaccination campaign in rural Africa: impact on the incidence of dog rabies and human dog-bite injuries. Vaccine 21 (2003) 1974-1982
13. Cook G.P., and Tomlinson I.M. The human immunoglobulin VH repertoire. Immunol. Today 16 (1995) 237-242
14. 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
15. Coulon P., Lafay F., Tuffereau C., and Flamand A. The molecular basis for altered pathogenicity of lyssavirus variants. Curr. Top. Microbiol. Immunol. 187 (1994) 69-84
16. Cox J.H., Dietzschold B., and Schneider L.G. Rabies virus glycoprotein. II. Biological and serological characterization. Infect. Immun. 16 (1977) 754-759
17. Cox J.P., Tomlinson I.M., and Winter G. A directory of human germ-line V kappa segments reveals a strong bias in their usage. Eur. J. Immunol. 24 (1994) 827-836
18. De Hoff J.B., and Ross L. Animal bites. Md. State Med. J. 30 (1981) 35-45
19. de Kruif J., Bakker A.B., Marissen W.E., Kramer R.A., Throsby M., Rupprecht C.E., and Goudsmit J. A human monoclonal antibody cocktail as a novel component of rabies postexposure prophylaxis. Annu. Rev. Med. 58 (2007) 359-368
20. Dietzschold B., Faber M., and Schnell M.J. New approaches to the prevention and eradication of rabies. Expert Rev. Vaccines 2 (2003) 399-406
21. Dietzschold B., Schnell M., and Koprowski H. Pathogenesis of rabies. Curr. Top. Microbiol. Immunol. 292 (2005) 45-56
22. Fitzgerald E.A., Cabasso V.J., Smith J.S., and Rastogi S.C. A collaborative study on the testing of rabies immune globulin (human) by the mouse neutralization test (MNT) and the rapid fluorescent focus inhibition test (RFFIT). J. Biol. Stand. 7 (1979) 67-72
23. Friguet B., Chaffotte A.L., Djavadi-Ohaniance L., and Goldberg M.E. Measurements of the true affinity constant in solution of antigen-antibody complexes by enzyme-linked immunosorbent assay. J. Immunol. Methods 77 (1985) 305-319
24. Gaudin Y., Ruigrok R.W., Tuffereau C., Knossow M., and Flamand A. Rabies virus glycoprotein is a trimer. Virology 187 (1992) 627-632
25. Gluck R., Wegmann A., Keller H., Hoskins J.M., and Germanier R. Human rabies immunoglobulin assayed by the rapid fluorescent focus inhibition test suppresses active rabies immunization. J. Biol. Stand. 15 (1987) 177-183
26. Goudsmit J., Marissen W.E., Weldon W.C., Niezgoda M., Hanlon C.A., Rice A.B., Kruif J., Dietzschold B., Bakker A.B., and Rupprecht C.E. Comparison of an anti-rabies human monoclonal antibody combination with human polyclonal anti-rabies immune globulin. J. Infect. Dis. 193 (2006) 796-801 Epub 2006 February 6
27. Griffiths A.D., Williams S.C., Hartley O., Tomlinson I.M., Waterhouse P., Crosby W.L., Kontermann R.E., Jones P.T., Low N.M., Allison T.J., et al. Isolation of high affinity human antibodies directly from large synthetic repertoires. EMBO J. 13 (1994) 3245-3260
28. Hemachudha T., Wacharapluesadee S., Mitrabhakdi E., Wilde H., Morimoto K., and Lewis R.A. Pathophysiology of human paralytic rabies. J. Neurovirol. 11 (2005) 93-100
29. Henderikx P., Coolen-van Neer N., Jacobs A., van der Linden E., Arends J.W., Mullberg J., and Hoogenboom H.R. A human immunoglobulin G1 antibody originating from an in vitro-selected Fab phage antibody binds avidly to tumor-associated MUC1 and is efficiently internalized. Am. J. Pathol. 160 (2002) 1597-1608
30. Hoogenboom H.R. Selecting and screening recombinant antibody libraries. Nat. Biotechnol. 23 (2005) 1105-1116
31. Houimel M., Mach J.P., Corthesy-Theulaz I., Corthesy B., and Fisch I. New inhibitors of Helicobacter Pylori urease holoenzyme selected from phage displayed peptide libraries. Eur. J. Biochem. 262 (1999) 774-780
32. Houimel M., Corthesy-Theulaz I., Fisch I., Wong C., Corthesy B., Mach J., and Finnern R. Selection of human single chain Fv antibody fragments binding and inhibiting Helicobacter pylori urease. Tumour Biol. 22 (2001) 36-44
33. Ikematsu H., Harindranath N., Ueki Y., Notkins A.L., and Casali P. Clonal analysis of a human antibody response. II. Sequences of the VH genes of human IgM, IgG, and IgA to rabies virus reveal preferential utilization of VHIII segments and somatic hypermutation. J. Immunol. 150 (1993) 1325-1337
34. Jackson A.C. Rabies virus infection: an update. J. Neurovirol. 9 (2003) 253-258
35. Kramer R.A., Marissen W.E., Goudsmit J., Visser T.J., Clijsters-Van der Horst M., Bakker A.Q., de Jong M., Jongeneelen M., Thijsse S., Backus H.H., Rice A.B., Weldon W.C., Rupprecht C.E., Dietzschold B., Bakker A.B., and de Kruif J. The human antibody repertoire specific for rabies virus glycoprotein as selected from immune libraries. Eur. J. Immunol. 35 (2005) 2131-2145
36. Knappik A., Ge L., Honegger A., Pack P., Fischer M., Wellnhofer G., Hoess A., Wolle J., Pluckthun A., and Virnekas B. Fully synthetic human combinatorial antibody libraries (HuCAL) based on modular consensus frameworks and CDRs randomized with trinucleotides. J. Mol. Biol. 296 (2000) 57-86
37. Kurz J., Vogel I., Gerstl F., and Dostal V. Comparative studies of two potency tests for antirabies serum: neutralization test in mice (MNT) and rapid fluorescent focus inhibition test (RFFIT). Dev. Biol. Stand. 64 (1986) 99-107
38. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
39. Langevin C., Jaaro H., Bressanelli S., Fainzilber M., and Tuffereau C. Rabies virus glycoprotein (RVG) is a trimeric ligand for the N-terminal cysteine-rich domain of the mammalian p75 neurotrophin receptor. J. Biol. Chem. 277 (2002) 37655-37662
40. Lanzavecchia A., Corti D., and Sallusto F. Human monoclonal antibodies by immortalization of memory B cells. Curr. Opin. Biotechnol. 18 (2007) 523-528 Epub 2007 December 11
41. Lefranc M.P., Pommie C., Ruiz M., Giudicelli V., Foulquier E., Truong L., Thouvenin- Contet V., and Lefranc G. IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev. Comp. Immunol. 27 (2003) 55-77
42. Lonberg N. Human antibodies from transgenic animals. Nat. Biotechnol. 23 (2005) 1117-1125
43. Macfarlan R.I., Dietzschold B., and Koprowski H. Stimulation of cytotoxic T-lymphocyte responses by rabies virus glycoprotein and identification of an immunodominant domain. Mol. Immunol. 23 (1986) 733-741
44. Marissen W.E., Kramer R.A., Rice A., MaWeldon W.C., Niezgoda M., Faber M., Slootstra J.W., Meloen R.H., Clijsters-van der Horst M., Visser T.J., Jongeneelen M., Thijsse S., Throsby M., de Kruif J., Rupprecht C.E., Dietzschold B., Goudsmit J., and Bakker A.B. Novel rabies virus-neutralizing epitope recognized by human monoclonal antibody: fine mapping and escape mutant analysis. J. Virol. 79 (2005) 4672-4678
45. Marks J.D., Hoogenboom H.R., Bonnert T.P., McCafferty J., Griffiths A.D., and Winter G. By-passing immunization. Human antibodies from V-gene libraries displayed on phage. J. Mol. Biol. 222 (1991) 581-597
46. Nadin-Davis S.A., and Fehlner-Gardiner C. Lyssaviruses: current trends. Adv. Virus Res. 71 (2008) 207-250
47. 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) 11346-11350 Epub 12002 August 12
48. Reichert J.M. Monoclonal antibodies as innovative therapeutics. Curr. Pharm. Biotechnol. 9 (2008) 423-430
49. Reichert J.M., Rosensweig C.J., Faden L.B., and Dewitz M.C. Monoclonal antibody successes in the clinic. Nat. Biotechnol. 23 (2005) 1073-1078
50. Rupprecht C.E., Barrett J., Briggs D., Cliquet F., Fooks A.R., Lumlertdacha B., Meslin F.X., Muler T., Nel L.H., Schneider C., Tordo N., and Wandeler A.I. Can rabies be eradicated?. Dev. Biol. (Basel) 131 (2008) 95-121
51. Rupprecht C.E., and Gibbons R.V. Clinical practice, Prophylaxis against rabies. N. Engl. J. Med. 351 (2004) 2626-2635
52. Rupprecht C.E., Hanlon C.A., and Hemachudha T. Rabies re-examined. Lancet Infect. Dis. 2 (2002) 327-343
53. Sakamoto S., Ide T., Tokiyoshi S., Nakao J., Hamada F., Yamamoto M., Grosby J.A., Ni Y., and Kawai A. Studies on the structures and antigenic properties of rabies virus glycoprotein analogues produced in yeast cells. Vaccine 17 (1999) 205-218
54. Sanna P.P., Samson M.E., Moon J.S., Rozenshteyn R., De Logu A., Williamson R.A., and Burton D.R. pFab-CMV, a single vector system for the rapid conversion of recombinant Fabs into whole IgG1 antibodies. Immunotechnology 4 (1999) 185-188
55. Sanz I. Multiple mechanisms participate in the generation of diversity of human H chain CDR3 regions. J. Immunol. 147 (1991) 1720-1729
56. Satpathy D.M., Sahu T., and Behera T.R. Equine rabies immunoglobulin: a study on its clinical safety. J. Indian Med. Assoc. 103 (2005) 238 241-232
57. Sawyer L.A. Antibodies for the prevention and treatment of viral diseases. Antiviral Res. 47 (2000) 57-77
58. Scaviner D., Barbie V., Ruiz M., and Lefranc M.P. Protein displays of the human immunoglobulin heavy, kappa and lambda variable and joining regions. Exp. Clin. Immunogenet. 16 (1999) 234-240
59. Simmons C.P., Bernasconi N.L., Suguitan A.L., Mills K., Ward J.M., Chau N.V., Hien T.T., Sallusto F., Ha do Q., Farrar J., de Jong M.D., Lanzavecchia A., and Subbarao K. Prophylactic and therapeutic efficacy of human monoclonal antibodies against H5N1 influenza. PLoS Med. 4 (2007) e178
60. Tavormina P.L., Rimoin D.L., Cohn D.H., Zhu Y.Z., Shiang R., and Wasmuth J.J. Another mutation that results in the substitution of an unpaired cysteine residue in the extracellular domain of FGFR3 in thanatophoric dysplasia type I. Hum. Mol. Genet. 4 (1995) 2175-2177
61. Tomlinson I.M., Cook G.P., Walter G., Carter N.P., Riethman H., Buluwela L., Rabbitts T.H., and Winter G. A complete map of the human immunoglobulin VH locus. Ann. N. Y. Acad. Sci. 764 (1995) 43-46
62. Wiktor T.J., MacFarlan R.I., Reagan K.J., Dietzschold B., Curtis P.J., Wunner W.H., Kieny M.P., Lathe R., Lecocq J.P., Mackett M., Moss B., and Koprowski H. Protection from rabies by a vaccinia virus recombinant containing the rabies virus glycoprotein gene. Biotechnology 24 (1992) 508-512
63. Wilde H., and Hemachudha T. Prophylaxis against rabies. N. Engl. J. Med. 352 (2005) 1608-1610 author reply 1608-1610
64. Wilde H., Khawplod P., Hemachudha T., and Sitprija V. Postexposure treatment of rabies infection: can it be done without immunoglobulin? Clin. Infect. Dis. 34 (2002) 477-480
65. Wu T.T., Johnson G., and Kabat E.A. Length distribution of CDRH3 in antibodies. Proteins 16 (1993) 1-7
66. Wunner W.H., Larson J.K., Dietzschold B., and Smith C.L. The molecular biology of rabies viruses. Rev. Infect. Dis. 10 (1988) S771-S784
67. Yazawa A., Fukuoka K., Honda H., Fukui T., and Muratsugu M. Biotin-protein ratios and stability of biotinylated immunoglobulins as standards for the quantitation of biotin-binding immunoglobulins. Biol. Pharm. Bull. 29 (2006) 1480-1482