Advances in the progress of monoclonal antibodies for rabies

References

• Baltimore D. Expression of animal virus genomes. Bacteriol Rev. 1971;35(3):235–8. doi:10.1128/br.35.3.235-241.1971.
   PubMedGoogle Scholar
• Wang MH, Zhu HW, He MH, Wen YJ, Cheng SP. Advance in biological function of rabies virus glycoprotein. China Anim Husb Vet Med. 2016;43(12):3349–55. in Chinese.
   Google Scholar
• Lv XJ, Ma XJ, Wang LH, Li H, Shen XX, Yu PC, Tang Q, Liang GD. Preparation and initial application of a monoclonal antibody specific for a newly discovered conserved linear epitope of rabies virus nucleoprotein. Biomed Environ Sci. 2012;25(1):98–103. doi:10.3967/0895-3988.2012.01.014.
   PubMed Web of Science ®Google Scholar
• Lafon M, Wiktor TJ, Macfarlan RI. Antigenic sites on the CVS rabies virus glycoprotein: analysis with monoclonal antibodies. J Gen Virol. 1983;64(Pt 4):843–51. doi:10.1099/0022-1317-64-4-843.
   PubMedGoogle Scholar
• Dietzschold B, Gore M, Casali P, Ueki Y, Rupprecht CE, Notkins AL, Koprowski H. Biological characterization of human monoclonal antibodies to rabies virus. J Virol. 1990;64(6):3087–90. doi:10.1128/jvi.64.6.3087-3090.1990.
   PubMed Web of Science ®Google Scholar
• Lafon M, Edelman L, Bouvet JP, Lafage M, Montchâtre E. Human monoclonal antibodies specific for the rabies virus glycoprotein and N protein. J Gen Virol. 1990;71(Pt 8):1689–96. doi:10.1099/0022-1317-71-8-1689.
   PubMedGoogle Scholar
• Yousaf MZ, Qasim M, Zia S, Khan M, Ashfaq UA, Khan S. Rabies molecular virology, diagnosis, prevention and treatment. Virol J. 2012;9:50. doi:10.1186/1743-422X-9-50.
   PubMed Web of Science ®Google Scholar
• Wilkerson JA. Rabies update. Wilderness Environ Med. 2000;11(1):31–39. doi:10.1580/1080-6032(2000)011[0031:RU]2.3.CO;2.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Rabies post-exposure prophylaxis. 2014 [accessed 2021 July 21]. https://apps.who.int/iris/bitstream/handle/10665/85346/9789245209829_chi.pdf;sequence=9.
   Google Scholar
• Both L, Banyard AC, van Dolleweerd C, Horton DL, Ma JK, Fooks AR. Passive immunity in the prevention of rabies. Lancet Infect Dis. 2012;12(5):397–407. doi:10.1016/S1473-3099(11)70340-1.
   PubMed Web of Science ®Google Scholar
• Hampson K, Coudeville L, Lembo T, Sambo M, Kieffer A, Attlan M, Barrat J, Blanton JD, Briggs DJ, Cleaveland S, et al. Estimating the global burden of endemic canine rabies. PLoS Negl Trop Dis. 2015;9(4):e0003709. doi:10.1371/journal.pntd.0003709.
   PubMed Web of Science ®Google Scholar
• Carrieri ML, Peixoto ZM, Paciencia ML, Kotait I, Germano PM. Laboratory diagnosis of equine rabies and its implications for human postexposure prophylaxis. J Virol Methods. 2006;138(1–2):1–9. doi:10.1016/j.jviromet.2006.07.005.
   PubMed Web of Science ®Google Scholar
• de Kruif J, Bakker AB, Marissen WE, Kramer RA, Throsby M, Rupprecht CE, Goudsmit J. A human monoclonal antibody cocktail as a novel component of rabies postexposure prophylaxis. Annu Rev Med. 2007;58:359–68. doi:10.1146/annurev.med.58.061705.145053.
   PubMed Web of Science ®Google Scholar
• Satpathy DM, Sahu T, Behera TR. Equine rabies immunoglobulin: a study on its clinical safety. J Indian Med Assoc. 2005;103:238, 241–232.
   Google Scholar
• Goudsmit J, Marissen WE, Weldon WC, Niezgoda M, Hanlon CA, Rice AB, Kruif J, Dietzschold B, Bakker AB, Rupprecht CE. Comparison of an anti-rabies human monoclonal antibody combination with human polyclonal anti-rabies immune globulin. J Infect Dis. 2006;193(6):796–801. doi:10.1086/500470.
   PubMed Web of Science ®Google Scholar
• De Benedictis P, Minola A, Rota Nodari E, Aiello R, Zecchin B, Salomoni A, Foglierini M, Agatic G, Vanzetta F, Lavenir R, et al. Development of broad-spectrum human monoclonal antibodies for rabies post-exposure prophylaxis. EMBO Mol Med. 2016;8(4):407–21. doi:10.15252/emmm.201505986.
   PubMed Web of Science ®Google Scholar
• Gogtay N, Thatte U, Kshirsagar N, Leav B, Molrine D, Cheslock P, Kapre SV, Kulkarni PS. Safety and pharmacokinetics of a human monoclonal antibody to rabies virus: a randomized, dose-escalation phase 1 study in adults. Vaccine. 2012;30(50):7315–20. doi:10.1016/j.vaccine.2012.09.027.
   PubMed Web of Science ®Google Scholar
• Gogtay NJ, Munshi R, Ashwath Narayana DH, Mahendra BJ, Kshirsagar V, Gunale B, Moore S, Cheslock P, Thaker S, Deshpande S, et al. Comparison of a novel human rabies monoclonal antibody to human rabies immunoglobulin for postexposure prophylaxis: a phase 2/3, randomized, single-blind, noninferiority, controlled study. Clin Infect Dis. 2018;66(3):387–95. doi:10.1093/cid/cix791.
   PubMed Web of Science ®Google Scholar
• The Clinical Trials Registry India (CTRI). A randomized, double-blind, placebo-controlled phase I/II study to evaluate the safety, tolerability and neutralizing activity of Rabimabs (A murine anti-rabies monoclonal antibody cocktails) against rabies virus in healthy subjects. 2016 November 16 [accessed 2021 July 22]. http://ctri.nic.in/Clinicaltrials/pmaindet2.php?trialid=11852&EncHid=&userName=Rabimabs.
   Google Scholar
• Kansagra K, Parmar D, Mendiratta SK, Patel J, Joshi S, Sharma N, Parihar A, Bhoge S, Patel H, Kalita P, et al. A phase 3, randomised, open-label, non-inferiority trial evaluating anti-rabies monoclonal antibody cocktail (TwinrabTM) against Human Rabies Immunoglobulin (HRIG). Clin Infect Dis. 2021;73(9):e2722–e2728.
   PubMedGoogle Scholar
• ClinicalTrials.gov. Safety and immunogenicity study of recombinant human rabies immunoglobin (rhRIG) in combination with rabies vaccine for human use with human rabies immune globulin (HRIG) in combination with rabies vaccine for human use in healthy adult subjects. 2015 Sept 25 [accessed 2021 Sept 17]. https://clinicaltrials.gov/ct2/show/study/NCT02559921.
   Google Scholar
• Chinese Clinical Trial Registry (ChiCTR). Preliminary assessment of the dose tolerance, safety, pharmacokinetics and neutralizing activity of rhRIG. 2019 Jun13 [accessed 2021 Sept 15] http://www.chictr.org.cn/showproj.aspx?proj=39967.
   Google Scholar
• Chinese Clinical Trial Registry (ChiCTR). Assessment of the safety, pharmacokinetics, neutralizing activity and immunogenicity of rhRIG combined with rabies vaccine. 2019 Jun 11 [accessed 2021 Sept 15]. http://www.chictr.org.cn/showproj.aspx?proj=36532.
   Google Scholar
• Chinese Clinical Trial Registry (ChiCTR). Evaluation of the efficacy and safety of rhRIG combined with rabies vaccine and the HRIG combined with rabies vaccine. 2019 May 17 [accessed 2021 Sept 15]. http://www.chictr.org.cn/showproj.aspx?proj=36372.
   Google Scholar
• Chinese Clinical Trial Registry (ChiCTR). Evaluation of the efficacy and safety of rhRIG combined with rabies vaccine and the marketed HRIG combined with rabies vaccine: a randomized, blind, positive controlled trial. 2019 Feb 23 [accessed 2021 Sept 15]. http://www.chictr.org.cn/showproj.aspx?proj=36013.
   Google Scholar
• ClinicalTrials.gov. A comparison of the safety, PD and PK of a single dose of SYN023 administered with licensed rabies vaccines. 2016 Nov 6. [accessed 2021 Sept 17]. https://clinicaltrials.gov/ct2/show/study/NCT02956746.
   Google Scholar
• McClain JB, Chuang A, Moore SM, Tsao E. Safety, pharmacokinetics, and neutralizing activity of SYN023, a mixture of two novel antirabies monoclonal antibodies intended for use in postrabies exposure prophylaxis. Clin Pharmacol Drug Dev. 2021;10(7):807–17. doi:10.1002/cpdd.917.
   PubMed Web of Science ®Google Scholar
• ClinicalTrials.gov. A phase III clinical study to evaluate SYN023ʹs efficacy and safety. 2020 Nov 25 [accessed 2021 Sept 17]. https://clinicaltrials.gov/ct2/show/study/NCT04644484.
   Google Scholar
• Bakker AB, Python C, Kissling CJ, Pandya P, Marissen WE, Brink MF, Lagerwerf F, Worst S, van Corven E, Kostense S, et al. First administration to humans of a monoclonal antibody cocktail against rabies virus: safety, tolerability, and neutralizing activity. Vaccine. 2008;26(47):5922–27. doi:10.1016/j.vaccine.2008.08.050.
   PubMed Web of Science ®Google Scholar
• ClinicalTrials.gov. Randomized phase II trial on safety and neutralizing activity of CL184 and rabies vaccine versus human rabies immune globulin (HRIG) and rabies vaccine in children and adolescents. 2008 Jul 2 [accessed 2021 Sept 18]. https://clinicaltrials.gov/ct2/show/study/NCT00708084.
   Google Scholar
• ClinicalTrials.gov. Rabies virus neutralizing activity and safety of CL184, a monoclonal antibody cocktail, in simulated rabies post exposure prophylaxis in healthy adults. 2010 Oct 26 [accessed 2021 Sept 18]. https://clinicaltrials.gov/ct2/show/study/NCT01228383.
   Google Scholar
• Rabishield rabies human monoclonal antibody. Serum Institute of India PVT.LTD. 2016 [accessed 2021 Jul 19]. https://www.seruminstitute.com/product_ind_rabishield.php.
   Google Scholar
• TwinrabTM (RabiMabs) rabies human monoclonal antibody. Zydus Cadila in India. 2019 [accessed 2021 Jul 19]. https://twinrab.com.
   Google Scholar
• Sloan SE, Hanlon C, Weldon W, Niezgoda M, Blanton J, Self J, Rowley KJ, Mandell RB, Babcock GJ, Thomas WDJ, et al. Identification and characterization of a human monoclonal antibody that potently neutralizes a broad panel of rabies virus isolates. Vaccine. 2007;25(15):2800–10. doi:10.1016/j.vaccine.2006.12.031.
   PubMed Web of Science ®Google Scholar
• McMichael JC, Fiske MJ, Fredenburg RA, Chakravarti DN, VanDerMeid KR, Barniak V, Caplan J, Bortell E, Baker S, Arumugham R, et al. Isolation and characterization of two proteins from Moraxella catarrhalis that bear a common epitope. Infect Immun. 1998;66(9):4374–81. doi:10.1128/IAI.66.9.4374-4381.1998.
   PubMed Web of Science ®Google Scholar
• Anwith HS, Ravish HS; DHJIJoCH Ashwathnarayana. Safety of new indigenous human Rabies Monoclonal Antibody (RMAb) for post exposure prophylaxis corresponding author citation article cycle. Indian J. Community Health. 2018;30(3):196–201.
   Web of Science ®Google Scholar
• Kuzmina NA, Kuzmin IV, Ellison JA, Rupprecht CE. Conservation of binding epitopes for monoclonal antibodies on the rabies virus glycoprotein. J Antivir Antiretrovir. 2013;5:037–043. doi:10.4172/jaa.1000061.
   Google Scholar
• Presentation from Zydus Cadila at the FDA workshop on rabies monoclonal antibody products as a component of rabies post-exposure prophylaxis. 2018 Jul 17 [accessed 5 Sept 2021]. https://www.fda.gov/downloads/Drugs/NewsEvents/UCM566898.pdf.
   Google Scholar
• Wiktor TJ, Koprowski H. Monoclonal antibodies against rabies virus produced by somatic cell hybridization: detection of antigenic variants. Proc Natl Acad Sci U S A. 1978;75(8):3938–42. doi:10.1073/pnas.75.8.3938.
   PubMed Web of Science ®Google Scholar
• Muhamuda K, Madhusudana SN, Ravi V. Use of neutralizing murine monoclonal antibodies to rabies glycoprotein in passive immunotherapy against rabies. Hum Vaccin. 2007;3(5):192–95. doi:10.4161/hv.3.5.4386.
   PubMed Web of Science ®Google Scholar
• Cheng W, Yu H, Niu WB, Tang GQ. Preparation and identification of monoclonal antibodies against rabies virus glycoprotein. Vet Orientation. 2019;22:217–18. (in Chinese).
   Google Scholar
• Ueki Y, Goldfarb IS, Harindranath N, Gore M, Koprowski H, Notkins AL, Casali P. Clonal analysis of a human antibody response. Quantitation of precursors of antibody-producing cells and generation and characterization of monoclonal IgM, IgG, and IgA to rabies virus. J Exp Med. 1990;171(1):19–34. doi:10.1084/jem.171.1.19.
   PubMed Web of Science ®Google Scholar
• Wang MX, Jia M, Jin M, Han J, Duan J, Wang LH, Jing RH, Li N, Yao JL, Li YF, et al. Safety of a single injection with recombinant human rabies immunoglobin at various dosages in humans. Chin J Biologicals. 2013;26(7):95–99. (in Chinese).
   Google Scholar
• 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. Novel rabies virus-neutralizing epitope recognized by human monoclonal antibody: fine mapping and escape mutant analysis. J Virol. 2005;79(8):4672–78. doi:10.1128/JVI.79.8.4672-4678.2005.
   PubMed Web of Science ®Google Scholar
• Bakker AB, Marissen WE, Kramer RA, Rice AB, Weldon WC, Niezgoda M, Hanlon CA, Thijsse S, Backus HH, de Kruif J, et al. Novel human monoclonal antibody combination effectively neutralizing natural rabies virus variants and individual in vitro escape mutants. J Virol. 2005;79(14):9062–68. doi:10.1128/JVI.79.14.9062-9068.2005.
   PubMed Web of Science ®Google Scholar
• Cheng Z, Sun LN, Liang MF. Progress of therapeutic human anti-rabies antibodies. Chin Med Biotechnol. 2010;5(3):208–10. (in Chinese).
   Google Scholar
• Vaughan TJ, Osbourn JK, Tempest PR. Human antibodies by design. Nat Biotechnol. 1998;16(6):535–39. doi:10.1038/nbt0698-535.
   PubMed Web of Science ®Google Scholar
• Kramer RA, Marissen WE, Goudsmit J, Visser TJ, Clijsters-van der Horst M, Bakker AQ, de Jong M, de Jongeneelen M, Thijsse S, Backus HH, et al. The human antibody repertoire specific for rabies virus glycoprotein as selected from immune libraries. Eur J Immunol. 2005;35(7):2131–45. doi:10.1002/eji.200526134.
   PubMed Web of Science ®Google Scholar
• Zhao XL, Yin J, Wang H, Jiang M, Hou XJ. Construction of human phage-displayed scFv library and selection of the ScFv against rabies virus. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi. 2004;20:243–47.
   PubMedGoogle Scholar
• Zhao XL, Yin J, Chen WQ, Jiang M, Yang G, Yang ZH. Generation and characterization of human monoclonal antibodies to G5, a linear neutralization epitope on glycoprotein of rabies virus, by phage display technology. Microbiol Immunol. 2008;52(2):89–93. doi:10.1111/j.1348-0421.2008.00016.x.
   PubMed Web of Science ®Google Scholar
• YU L, Sun L, Jin J, Li C, Li DX, Liang MF. Generation of recombinant human ScFv antibodies against Rabies virus. Chinese J Exp Clin Virol. 2012;26(3):189–92. (in Chinese).
   Google Scholar
• Fang SD, Zhao XR, Chen JJ, An C, Nan JJ, Mao XY. Construction and validation of humanized anti-rabies virus monoclonal antibodies. Prog Microbiol Immunol. 2019;47(4):7–13. (in Chinese).
   Google Scholar
• Houimel M, Dellagi K. Isolation and characterization of human neutralizing antibodies to rabies virus derived from a recombinant immune antibody library. J Virol Methods. 2009;161(2):205–15. doi:10.1016/j.jviromet.2009.06.018.
   PubMed Web of Science ®Google Scholar
• Sun L, Chen Z, Yu L, Wei J, Li C, Jin J, Shen X, Lv X, Tang Q, Li D, et al. Generation and characterization of neutralizing human recombinant antibodies against antigenic site II of rabies virus glycoprotein. Appl Microbiol Biotechnol. 2012;96(2):357–66. doi:10.1007/s00253-012-4171-4.
   PubMed Web of Science ®Google Scholar
• Zhao XL, Chen WQ, H F, Shen CF, Ji Y, Li JM, Zhang SJ, Yang ZH. Preparation of human antibody fragments against rabies virus based on ribosome display technology. Prog Biochem Biophys. 2011;38(10):945–52. (in Chinese). doi:10.3724/SP.J.1206.2010.00521.
   Web of Science ®Google Scholar
• Groves M, Lane S, Douthwaite J, Lowne D, Rees DG, Edwards B, Jackson RH. Affinity maturation of phage display antibody populations using ribosome display. J Immunol Methods. 2006;313(1–2):129–39. doi:10.1016/j.jim.2006.04.002.
   PubMed Web of Science ®Google Scholar
• Zhao XL, Chen WQ, Yang ZH, Li JM, Zhang SJ, Tian LF. Selection and affinity maturation of human antibodies against rabies virus from a scFv gene library using ribosome display. J Biotechnol. 2009;144(4):253–58. doi:10.1016/j.jbiotec.2009.09.022.
   PubMed Web of Science ®Google Scholar
• Hellert J, Buchrieser J, Larrous F, Minola A, de Melo GD, Soriaga L, England P, Haouz A, Telenti A, Schwartz O, et al. Structure of the prefusion-locking broadly neutralizing antibody RVC20 bound to the rabies virus glycoprotein. Nat Commun. 2020;11(1):596. doi:10.1038/s41467-020-14398-7.
   PubMed Web of Science ®Google Scholar
• Molecular Targeting Technologies. Rabies mAb product. [ accessed 2021 Sept 23]. http://www.mtarget.com/mm5/pdfs/pipeline/RabiesMonoclonalAnti.pdf.
   Google Scholar
• Chao TY, Ren S, Shen E, Moore S, Zhang SF, Chen L, Rupprecht CE, Tsao E. SYN023, a novel humanized monoclonal antibody cocktail, for post-exposure prophylaxis of rabies. PLoS Negl Trop Dis. 2017;11(12):e0006133. doi:10.1371/journal.pntd.0006133.
   PubMed Web of Science ®Google Scholar
• Chao TY, Zhang SF, Chen L, Tsao E, Rupprecht CE. In vivo efficacy of SYN023, an anti-rabies monoclonal antibody cocktail, in post-exposure prophylaxis animal models. Trop Med Infect Dis. 2020;5:31–39.
   Google Scholar
• Ding Y, Wu M, Zhang H, Zhu X, Hu Y, Li X, Liu J, Tsao E, Liu M, Li C. Safety, pharmacokinetics and pharmacodynamics of SYN023 alone or in combination with a rabies vaccine: an open, parallel, single dose, phase 1 bridging study in healthy Chinese subjects. Antiviral Res. 2020;184:104956. doi:10.1016/j.antiviral.2020.104956.
   PubMed Web of Science ®Google Scholar
• Franka R, Carson WC, Ellison JA, Taylor ST, Smith TG, Kuzmina NA, Kuzmin IV, Marissen WE, Rupprecht CE. In vivo efficacy of a cocktail of human monoclonal antibodies (CL184) against diverse North American bat rabies virus variants. Trop Med Infect Dis. 2017;2:48–59.
   Google Scholar
• Sparrow E, Torvaldsen S, Newall AT, Wood JG, Sheikh M, Kieny MP, Abela-Ridder B. Recent advances in the development of monoclonal antibodies for rabies post exposure prophylaxis: a review of the current status of the clinical development pipeline. Vaccine. 2019;37(Suppl 1):A132–a139. doi:10.1016/j.vaccine.2018.11.004.
   PubMed Web of Science ®Google Scholar
• Sun LN, Liu Y, Li C, Li DX, Liang MF. Generation of human scfv antibodies for antigenic site III of rabies virus glycoprotein from antibody-phage libraries by chain shuffling. Chin J Virol. 2016;32(4):393–98. (in Chinese).
   Google Scholar
• Sun LN, Liu Y, Li C, Li DX, Liang MF. Development of recombinant human monoclonal antibody cocktail for post-exposure rabies prophylaxis. Chin J Virol. 2016;32(4):399–403. (in Chinese).
   Google Scholar