Development of broad-spectrum human monoclonal antibodies for rabies post-exposure prophylaxis

EMBO Molecular Medicine

Volumn 8, Issue 4, 2016, Pages 407-421

  De Benedictis, Paola ^a   Minola, Andrea ^b   Rota Nodari, Elena ^a   Aiello, Roberta ^a   Zecchin, Barbara ^a   Salomoni, Angela ^a   Foglierini, Mathilde ^c   Agatic, Gloria ^b   Vanzetta, Fabrizia ^b   Lavenir, Rachel ^d   Lepelletier, Anthony ^d   Bentley, Emma ^e   Weiss, Robin ^f   Cattoli, Giovanni ^a   Capua, Ilaria ^a   Sallusto, Federica ^c   Wright, Edward ^e   Lanzavecchia, Antonio ^c,g   Bourhy, Hervé ^d   Corti, Davide ^b,c  

^a ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLE VENEZIE   (Italy)

^b Humabs BioMed SA ^*  (Switzerland)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^d WORLD HEALTH ORGANIZATION   (Switzerland)

^e UNIVERSITY OF WESTMINSTER   (United Kingdom)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g ETH ZURICH   (Switzerland)

Author keywords

Human monoclonal antibody; Lyssaviruses; Post exposure prophylaxis; Rabies

Indexed keywords

EPITOPE; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; RABIES IMMUNOGLOBULIN; RABIES VACCINE; RVC20 VACCINE; RVC58 VACCINE; UNCLASSIFIED DRUG; IMMUNOLOGIC FACTOR; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; CELL IMMORTALIZATION; DISEASE MODEL; DONOR; DRUG ACTIVITY; DRUG COST; DRUG DEVELOPMENT; DRUG POTENCY; DRUG SPECIFICITY; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; LYSSAVIRUS; MEMORY CELL; NONHUMAN; POST EXPOSURE PROPHYLAXIS; PRIORITY JOURNAL; RABIES; RABIES VIRUS; SYRIAN HAMSTER; VACCINATION; VIRUS NEUTRALIZATION; ANIMAL; IMMUNOLOGY; ISOLATION AND PURIFICATION; MESOCRICETUS; PASSIVE IMMUNIZATION; PROCEDURES; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; DISEASE MODELS, ANIMAL; HUMANS; IMMUNIZATION, PASSIVE; IMMUNOLOGIC FACTORS; MESOCRICETUS; POST-EXPOSURE PROPHYLAXIS; RABIES; RABIES VIRUS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84961282543     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201505986     Document Type: Article

References (62)

1. Amengual B, Whitby JE, King A, Cobo JS, Bourhy H (1997) Evolution of European bat lyssaviruses. J Gen Virol 78(Pt 9): 2319-2328
2. Archer BG, Dierks RE (1968) Effects of homologous or heterologous antiserum on neutralizing-antibody response to rabies vaccine. Bull World Health Organ 39: 407-417
3. Arechiga Ceballos N, Vazquez Moron S, Berciano JM, Nicolas O, Aznar Lopez C, Juste J, Rodriguez Nevado C, Aguilar Setien A, Echevarria JE (2013) Novel lyssavirus in bat, Spain. Emerg Infect Dis 19: 793-795
4. Atanasiu P, Bahmanyar M, Baltazard M, Fox JP, Habel K, Kaplan MM, Kissling RE, Komarov A, Koprowski H, Lepine P et al (1956) Rabies neutralizing antibody response to different schedules of serum and vaccine inoculations in non-exposed persons. Bull World Health Organ 14: 593-611
5. Atanasiu P, Cannon DA, Dean DJ, Fox JP, Habel K, Kaplan MM, Kissling RE, Koprowski H, Lepine P, Perez Gallardo F (1961) Rabies neutralizing antibody response to different schedules of serum and vaccine inoculations in non-exposed persons. 3. Bull World Health Organ 25: 103-114
6. Atanasiu P, Dean DJ, Habel K, Kaplan MM, Koprowski H, Lepine P, Serie C (1967) Rabies neutralizing antibody response to different schedules of serum and vaccine inoculations in non-exposed persons. 4. Bull World Health Organ 36: 361-365
7. Babes V, Lepp M (1889) Recherches sur la vaccination antirabique. Ann Inst Pasteur 3: 384-390
8. Badrane H, Bahloul C, Perrin P, Tordo N (2001) Evidence of two Lyssavirus phylogroups with distinct pathogenicity and immunogenicity. J Virol 75: 3268-3276
9. Bakker AB, Marissen WE, Kramer RA, Rice AB, Weldon WC, Niezgoda M, Hanlon CA, Thijsse S, Backus HH, de Kruif J et al (2005) Novel human monoclonal antibody combination effectively neutralizing natural rabies virus variants and individual invitro escape mutants. J Virol 79: 9062-9068
10. Bakker AB, Python C, Kissling CJ, Pandya P, Marissen WE, Brink MF, Lagerwerf F, Worst S, van Corven E, Kostense S et al (2008) First administration to humans of a monoclonal antibody cocktail against rabies virus: safety, tolerability, and neutralizing activity. Vaccine 26: 5922-5927
11. Baltazard M, Bahmanyar M (1955) Field trials with rabies vaccine on persons bitten by rabid wolves. Bull World Health Organ 13: 747-772
12. Both L, Banyard AC, van Dolleweerd C, Horton DL, Ma JK, Fooks AR (2012) Passive immunity in the prevention of rabies. Lancet Infect Dis 12: 397-407
13. Bourhy H, Kissi B, Lafon M, Sacramento D, Tordo N (1992) Antigenic and molecular characterization of bat rabies virus in Europe. J Clin Microbiol 30: 2419-2426
14. Bourhy H, Kissi B, Tordo N (1993) Molecular diversity of the Lyssavirus genus. Virology 194: 70-81
15. Bourhy H, Goudal M, Mailles A, Sadkowska-Todys M, Dacheux L, Zeller H (2009) Is there a need for anti-rabies vaccine and immunoglobulins rationing in Europe? Euro Surveill 14: 19166
16. Brookes SM, Parsons G, Johnson N, McElhinney LM, Fooks AR (2005) Rabies human diploid cell vaccine elicits cross-neutralising and cross-protecting immune responses against European and Australian bat lyssaviruses. Vaccine 23: 4101-4109
17. Cabasso VJ, Loofbourow JC, Roby RE, Anuskiewicz W (1971) Rabies immune globulin of human origin: preparation and dosage determination in non-exposed volunteer subjects. Bull World Health Organ 45: 303-315
18. Cabasso VJ (1974) Properties of rabies immune globulin of human origin. J Biol Stand 2: 43-50
19. Cabasso VJ, Dobkin MB, Roby RE, Hammar AH (1974) Antibody response to a human diploid cell rabies vaccine. Appl Microbiol 27: 553-561
20. Cliquet F, Aubert M, Sagne L (1998) Development of a fluorescent antibody virus neutralisation test (FAVN test) for the quantitation of rabies-neutralising antibody. J Immunol Methods 212: 79-87
21. Corti D, Lanzavecchia A (2013) Broadly neutralizing antiviral antibodies. Annu Rev Immunol 31: 705-742
22. Dietzgen R, Calisher C, Kurath G, Kuzmin I, Rodriguez L, Stone D, Tesh R, Tordo N, Walker P, Wetzel T et al (2011) Rhabdoviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds), pp 686-714. Oxford, UK: Elsevier
23. Dodet B, Africa Rabies Bureau (AfroREB) (2009) The fight against rabies in Africa: from recognition to action. Vaccine 27: 5027-5032
24. Ertl HC (2009) Novel vaccines to human rabies. PLoS Negl Trop Dis 3: e515
25. Fooks AR, Banyard AC, Horton DL, Johnson N, McElhinney LM, Jackson AC (2014) Current status of rabies and prospects for elimination. Lancet 384: 1389-1399
26. Goudsmit J, Marissen WE, Weldon WC, Niezgoda M, Hanlon CA, Rice AB, Kruif J, Dietzschold B, Bakker AB, Rupprecht CE (2006) Comparison of an anti-rabies human monoclonal antibody combination with human polyclonal anti-rabies immune globulin. J Infect Dis 193: 796-801
27. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704
28. Habel K (1954) Antiserum in the prophylaxis of rabies. Bull World Health Organ 10: 781-788
29. Habel K (1957) Rabies prophylaxis in man. Public Health Rep 72: 667-673
30. Hampson K, Coudeville L, Lembo T, Sambo M, Kieffer A, Attlan M, Barrat J, Blanton JD, Briggs DJ, Cleaveland S et al (2015) Estimating the global burden of endemic canine rabies. PLoS Negl Trop Dis 9: e0003709
31. Hanlon CA, DeMattos CA, DeMattos CC, Niezgoda M, Hooper DC, Koprowski H, Notkins A, Rupprecht CE (2001a) Experimental utility of rabies virus-neutralizing human monoclonal antibodies in post-exposure prophylaxis. Vaccine 19: 3834-3842
32. Hanlon CA, Niezgoda M, Morrill PA, Rupprecht CE (2001b) The incurable wound revisited: progress in human rabies prevention? Vaccine 19: 2273-2279
33. Hanlon CA, Kuzmin IV, Blanton JD, Weldon WC, Manangan JS, Rupprecht CE (2005) Efficacy of rabies biologics against new lyssaviruses from Eurasia. Virus Res 111: 44-54
34. Heckman KL, Pease LR (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc 2: 924-932
35. Hooper PT, Lunt RA, Gould AR, Samaratunga H, Hyatt AD, Gleeson LJ, Rodwell BJ, Rupprecht CE, Smith JS, Murray PK (1997) A new lyssavirus - The first endemic rabies-related virus recognized in Australia. Bull Inst Pasteur 95: 209-218
36. Horton DL, McElhinney LM, Marston DA, Wood JL, Russell CA, Lewis N, Kuzmin IV, Fouchier RA, Osterhaus AD, Fooks AR et al (2010) Quantifying antigenic relationships among the lyssaviruses. J Virol 84: 11841-11848
37. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772-780
38. Kelley B (2009) Industrialization of mAb production technology: the bioprocessing industry at a crossroads. MAbs 1: 443-452
39. Kitasato BU (1890) Ueber das Zustandekommender Diphterie-Immunitat und der Tetanus-Immunitat. Deutsche Medizinische Wochenschrift
40. Kohler G, Milstein C (2005) Continuous cultures of fused cells secreting antibody of predefined specificity. 1975. J Immunol 174: 2453-2455
41. Koprowski H, Van Der Scheer J, Black J (1950) Use of hyperimmune anti-rabies serum concentrates in experimental rabies. Am J Med 8: 412-420
42. de Kruif J, Bakker AB, Marissen WE, Kramer RA, Throsby M, Rupprecht CE, Goudsmit J (2007) A human monoclonal antibody cocktail as a novel component of rabies postexposure prophylaxis. Annu Rev Med 58: 359-368
43. Kuzimina NA, Kuzmin IV, Ellison JA, Rupprecht CE (2013) Conservation of binding epitopes for monoclonal antibodies on the rabies virus glycoprotein. Journal of Antiviral and Antiretrovirals 5: 37-43
44. Kuzmin IV, Mayer AE, Niezgoda M, Markotter W, Agwanda B, Breiman RF, Rupprecht CE (2010) Shimoni bat virus, a new representative of the Lyssavirus genus. Virus Res 149: 197-210
45. Mallewa M, Fooks AR, Banda D, Chikungwa P, Mankhambo L, Molyneux E, Molyneux ME, Solomon T (2007) Rabies encephalitis in malaria-endemic area, Malawi, Africa. Emerg Infect Dis 13: 136-139
46. Manning SE, Rupprecht CE, Fishbein D, Hanlon CA, Lumlertdacha B, Guerra M, Meltzer MI, Dhankhar P, Vaidya SA, Jenkins SR et al (2008) Human rabies prevention-United States, 2008: recommendations of the Advisory Committee on Immunization Practices. MMWR Recomm Rep 57: 1-28.
47. Marissen WE, Kramer RA, Rice A, Weldon WC, Niezgoda M, Faber M, Slootstra JW, Meloen RH, Clijsters-van der Horst M, Visser TJ et al (2005) Novel rabies virus-neutralizing epitope recognized by human monoclonal antibody: fine mapping and escape mutant analysis. J Virol 79: 4672-4678
48. Marston DA, Horton DL, Ngeleja C, Hampson K, McElhinney LM, Banyard AC, Haydon D, Cleaveland S, Rupprecht CE, Bigambo M et al (2012) Ikoma lyssavirus, highly divergent novel lyssavirus in an African civet. Emerg Infect Dis 18: 664-667
49. th edn. Geneva, Switzerland: World Health Organization
50. Nagarajan T, Marissen WE, Rupprecht CE (2014) Monoclonal antibodies for the prevention of rabies: theory and clinical practice. Antibody Technol J 4: 1-12
51. OIE World Organization for Animal Health (2013) Rabies. In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals
52. Sayers EW, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Edgar R, Federhen S et al (2009) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 37: D5-D15
53. Sievers F, Higgins DG (2014) Clustal omega. Curr Protoc Bioinformatics 48: 3.13.1-3.13.16
54. Sikes RK (1969) Human rabies immune globulin. Public Health Rep 84: 797-801
55. Sloan SE, Hanlon C, Weldon W, Niezgoda M, Blanton J, Self J, Rowley KJ, Mandell RB, Babcock GJ, Thomas WD Jr et al (2007) Identification and characterization of a human monoclonal antibody that potently neutralizes a broad panel of rabies virus isolates. Vaccine 25: 2800-2810
56. Tiller T, Meffre E, Yurasov S, Tsuiji M, Nussenzweig MC, Wardemann H (2008) Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 329: 112-124
57. Traggiai E, Becker S, Subbarao K, Kolesnikova L, Uematsu Y, Gismondo MR, Murphy BR, Rappuoli R, Lanzavecchia A (2004) An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat Med 10: 871-875
58. Warrell MJ, Riddell A, Yu LM, Phipps J, Diggle L, Bourhy H, Deeks JJ, Fooks AR, Audry L, Brookes SM et al (2008) A simplified 4-site economical intradermal post-exposure rabies vaccine regimen: a randomised controlled comparison with standard methods. PLoS Negl Trop Dis 2: e224
59. Wiktor TJ, Lerner RA, Koprowski H (1971) Inhibitory effect of passive antibody on active immunity induced against rabies by vaccination. Bull World Health Organ 45: 747-753
60. World Health Organization (2013) WHO Experts Consultation on Rabies. Second report World Health Organ Tech Rep Ser (982): 1-139
61. Wright E, Temperton NJ, Marston DA, McElhinney LM, Fooks AR, Weiss RA (2008) Investigating antibody neutralization of lyssaviruses using lentiviral pseudotypes: a cross-species comparison. J Gen Virol 89: 2204-2213
62. Wright E, McNabb S, Goddard T, Horton DL, Lembo T, Nel LH, Weiss RA, Cleaveland S, Fooks AR (2009) A robust lentiviral pseudotype neutralisation assay for in-field serosurveillance of rabies and lyssaviruses in Africa. Vaccine 27: 7178-7186