Research and development progress of human rabies vaccines and passive immune preparations
LAI Yong-jie1, LI Jing2
1. Department of Immunology and Pathogenic Biology, Zhuhai Campus, Zunyi Medical University, Zhuhai 519041, China; 2. The United Laboratories (Zhuhai) Co., Ltd, Zhuhai 519041, China
Abstract:Rabies is a zoonotic disease caused by rabies virus. Rabies virus infection has a near 100% case fatality rate following the onset of clinical disease.Currently, vaccines used for rabies prevention in human are originated from inactivated rabies virus. With rapid development of gene engineering technology, new generation rabies vaccines using viral G protein (Glycoprotein) as antigen are in development, including sub-unit vaccines purified from different expression systems, DNA vaccines, and vaccines using viral vectors as carrier, etc. This review also discusses the research and development progress of the passive immune preparations (monoclonal antibodies) which could be an ideal substitute for rabies immunoglobulin in the future.
赖永洁,李靖. 人用狂犬病疫苗和被动免疫制剂研发进展[J]. 中国人兽共患病学报, 2018, 34(6): 563-569.
LAI Yong-jie, LI Jing. Research and development progress of human rabies vaccines and passive immune preparations. Chinese Journal of Zoonoses, 2018, 34(6): 563-569.
[1] 刘淑清, 陶晓燕,于鹏程, 等.中国2015年狂犬病流行特征分析[J].中华实验和临床病毒学杂志,2016, 30(6): 537-540.DOI: 10.3760/cma.j.issn.1003-9279.2016.06.009 [2] Piyasirisilp S, Schmeckpeper BJ, Chandanayingyong D, et al.Association of HLA and T-cell receptor gene polymorphisms with semple rabies vaccine-induced autoimmune encephalomyelitis[J].Ann Neurol, 1999, 45(5): 595-600.DOI: 10.1128/JVI.79.8.4672-4678.2005 [3] World Health Organization.Weekly epidemiological record on rabies[EB/OL][2017-09-21].https://foxrabiesblueprint.org/IMG/pdf/HumanProphylaxis_wer8532_WHO.pdf [4] Pereira CA, Nozaki-Renard JN, Schwartz J, et al.Cytotoxicity reactions against target cells infected with rabies virus[J].J Virol Methods,1982, 5(2): 75-83.DOI: 10.1016/0166-0934(82)90084-2 [5] Craig Hooper D, Morimoto K, Bette M, et al.Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system[J].J Virol.1998, 72(5): 3711-3719. [6] Yelverton E, Norton S, Obijeski JF, et al.Rabies virus glycoprotein analogs: biosynthesis in Escherichia coli[J].Science, 1983, 219(4585): 614-620.DOI: 10.1126/science.6297004 [7] Ertl HC.Novel vaccines to human rabies[J].PLoS Negl Trop Dis, 2009, 3(9): e515.DOI: 10.1371/journal.pntd.0000515 [8] Sureau P, Perrin P.The use of immunosome technology for vaccines against rabies and other viral diseases[J].Eur J Epidemiol, 1989, 5(3): 275-278.DOI: 10.1007/BF00144826 [9] Prehaud C, Takehara K, Flamand A, et al.Immunogenic and protective properties of rabies virus glycoprotein expressed by baculovirus vectors[J].Virology, 1989, 173(2): 390-399.DOI: 10.1016/0042-6822(89)90551-5 [10] Fu ZF, Rupprecht CE, Dietzschold B, et al.Oral vaccination of racoons (Procyon lotor) with baculovirus-expressed rabies virus glycoprotein[J].Vaccine, 1993, 11(9): 925-928.DOI: 10.1016/0264-410X(93)90379-C [11] Ramya R, Mohana Subramanian B, Sivakumar V, et al.Expression and solubilization of insect cell-based rabies virus glycoprotein and assessment of its immunogenicity and protective efficacy in mice[J].Clin Vaccine Immunol, 2011, 18(10):1673-1679.DOI: 10.1128/CVI.05258-11 [12] Yokomizo AY, Jorge SA, Astray RM, et al.Rabies virus glycoprotein expression in Drosophila S2 cells.I.Functional recombinant protein in stable co-transfected cell line[J].Biotechnol J, 2007, 2(1): 102-109.DOI: 10.1002/biot.200600211 [13] Swiech K, Rossi N, Silva BG, et al.Bioreactor culture of recombinant Drosophila melanogaster S2 cells: characterization of metabolic features related to cell growth and production of the rabies virus glycoprotein[J].Cytotechnology, 2008, 57(1): 61-66.DOI: 10.1007/s10616-008-9130-7 [14] Galesi ALL, Aguiar MA, Astray RM.Growth of recombinant Drosophila melanogaster Schneider 2 cells producing rabies virus glycoprotein in bioreactor employing serum-free medium[J].Cytotechnology, 2008, 57(1): 73-81.DOI: 10.1007/s10616-008-9139-y [15] Ventini-Monteiro DC, Astray RM, Pereira CA.Production of recombinant rabies virus glycoprotein by insect cells in a single-use fixed-bed bioreactor[J].Methods Mol Biol, 2018, 1674: 87-94.DOI: 10.1007/978-1-4939-7312-5_7 [16] Sakamoto S, Ide T, Tokiyoshi S, et al.Studies on the structures and antigenic properties of rabies virus glycoprotein analogues produced in yeast cells[J].Vaccine, 1999, 17(3): 205-218.DOI: 10.1016/S0264-410X(98)00196-0 [17] Klepfer SR, Debouck C, Uffelman J, et al.Characterization of rabies glycoprotein expressed in yeast[J].Arch Virol, 1993, 128(3/4): 269-286.DOI: 10.1007/BF01309439 [18] McGarvey PB, Hammond J, Dienelt MM, et al.Expression of the rabies virus glycoprotein in transgenic tomatoes[J].Biotechnology (NY), 1995, 3(13): 1484-1487.DOI: 10.1038/nbt1295-1484 [19] Ashraf S, Singh PK, Yadav DK, et al.High level expression of surface glycoprotein of rabies virus in tobacco leaves and its immunoprotective activity in mice[J].J Biotechnol, 2005, 119(1): 1-14. DOI: 10.1016/j.jbiotec.2005.06.009 [20] Loza-Rubio E, Rojas E, Gomez L, et al.Development of an edible rabies vaccine in maize using the Vnukovo strain[J].Dev Biol (Basel), 2008, 131: 477-482. [21] Gupta PK, Sharma S, Walunj SS, et al.Immunogenic and antigenic properties of recombinant soluble glycoprotein of rabies virus[J].Vet Microbiol, 2005, 108(3/4): 207-214.DOI: 10.1016/j.vetmic.2005.04.007 [22] Wojczyk BS, Czerwinski M, Stwora-Wojczyk MM, et al.Purification of a secreted form of recombinant rabies virus glycoprotein: comparison of two affinity tags[J].Protein Expr Purif, 1996, 7(2): 183-193.DOI: 10.1006/prep.1996.0026 [23] Shakin-Eshleman SH, Remaley AT, Eshleman JR, et al.N-linked glycosylation of rabies virus glycoprotein.Individual sequons differ in their glycosylation efficiencies and influence on cell surface expression[J].J Biol Chem, 1992, 67(15): 10690-10698. [24] Burger SR, Remaley AT, Danley JM, et al.Stable expression of rabies virus glycoprotein in Chinese hamster ovary cells[J].J Gen Virol, 1991, 72 (Pt 2): 359-367.DOI: 10.1099/0022-1317-72-2-359 [25] Kasturi L, Eshleman JR, Wunner WH, et al.The hydroxy amino acid in an Asn-X-Ser/Thr sequon can influence N-linked core glycosylation efficiency and the level of expression of a cell surface glycoprotein[J].J Biol Chem, 1995, 270(24): 14756-14761.DOI: 10.1074/jbc.270.24.14756 [26] Wojczyk BS, Takahashi N, Levy MT, et al.N-glycosylation at one rabies virus glycoprotein sequon influences N-glycan processing at a distant sequon on the same molecule[J].Glycobiology, 2005, 15(6): 655-666.DOI: 10.1093/glycob/cwi046 [27] Tesoro Cruz E, Feria Romero IA, Lopez Mendoza JG, et al.Efficient post-exposure prophylaxis against rabies by applying a four-dose DNA vaccine intranasally[J].Vaccine, 2008, 26(52): 6936-6944.DOI: 10.1016/j.vaccine.2008.09.083 [28] Osorio JE, Tomlinson CC, Frank RS, et al.Immunization of dogs and cats with a DNA vaccine against rabies virus[J].Vaccine, 1999, 17(9/10): 1109-1116.DOI: 10.1016/S0264-410X(98)00328-4 [29] Lodmell DL, Parnell MJ, Bailey JR, et al.One-time gene gun or intramuscular rabies DNA vaccination of non-human primates: comparison of neutralizing antibody responses and protection against rabies virus 1 year after vaccination[J].Vaccine, 2001, 20(5/6): 838-844.DOI: 10.1016/S0264-410X(01)00392-9 [30] Lodmell DL, Parnell MJ, Bailey JR, et al.Rabies DNA vaccination of non-human primates: post-exposure studies using gene gun methodology that accelerates induction of neutralizing antibody and enhances neutralizing antibody titers[J].Vaccine, 2002, 20(17/18): 2221-2228.DOI: 10.1016/S0264-410X(02)00143-3 [31] Saxena S, Sonwane AA, Dahiya SS, et al.Induction of immune responses and protection in mice against rabies using a self-replicating RNA vaccine encoding rabies virus glycoprotein[J].Vet Microbiol, 2009, 136(1/2): 36-44.DOI: 10.1016/j.vetmic.2008.10.030 [32] Astray RM, Jorge SA, Pereira CA.Rabies vaccine development by expression of recombinant viral glycoprotein[J].Arch Virol, 2017, 162(2): 323-332.DOI: 10.1007/s00705-016-3128-9 [33] Weyer J, Rupprecht CE, Mans J, et al. Generation andevaluation of a recombinant modified vaccinia virus Ankara vaccine for rabies[J].Vaccine, 2007, 25(21): 4213-4222.DOI: 10.1016/j.vaccine.2007.02.084 [34] Artenstein AW, Opal JM, Opal SM, et al.History of U.S.military contributions to the study of vaccines against infectious diseases[J].Mil Med, 2005, 170(4 Suppl): 3-11.DOI:10.7205/MILMED.170.4S.3 [35] Choudhry A, Mathena J, Albano JD, et al.Safety evaluation of adenovirus type 4 and type 7 vaccine live, oral in military recruits[J].Vaccine, 2016, 34(38): 4558-4564.DOI: 10.1016/j.vaccine.2016.07.033 [36] Xiang ZQ, Pasquini S, Ertl HC.Induction of genital immunity by DNA priming and intranasal booster immunization with a replication-defective adenoviral recombinant[J].J Immunol, 1999, 162(11): 6716-6723. [37] Xiang ZQ, Yang Y, Wilson JM, et al.A replication-defective human adenovirus recombinant serves as a highly efficacious vaccine carrier[J].Virology, 1996, 219(1): 220-227.DOI: 10.1006/viro.1996.0239 [38] Xiang Z, Li Y, Gao G, et al.Mucosally delivered E1-deleted adenoviral vaccine carriers induce transgene product-specific antibody responses in neonatal mice[J].J Immunol, 2003, 171(8): 4287-4293.DOI: 10.4049/jimmunol.171.8.4287 [39] Zhou D, Cun A, Li Y, et al.A chimpanzee-origin adenovirus vector expressing the rabies virus glycoprotein as an oral vaccine against inhalation infection with rabies virus[J].Mol Ther, 2006, 14(5): 662-672.DOI: 10.1016/j.ymthe.2006.03.027 [40] De Santis O, Audran R, Pothin E, et al.Safety and immunogenicity of a chimpanzee adenovirus-vectored Ebola vaccine in healthy adults: a randomised, double-blind, placebo-controlled, dose-finding, phase 1/2a study[J].Lancet Infect Dis, 2016, 16(3): 311-320.DOI: 10.1016/S1473-3099(15)00486-7 [41] Ledgerwood JE, DeZure AD, Stanley DA, et al.Chimpanzee Adenovirus Vector Ebola Vaccine[J].N Engl J Med, 2017, 376(10): 928-938.DOI: 10.1056/NEJMoa1410863 [42] Hanlon CA, Kuzmin IV, Blanton JD, et al.Efficacy of rabies biologics against new lyssaviruses from Eurasia[J].Virus Res, 2005, 111(1): 44-54.DOI: 10.1016/j.virusres.2005.03.009 [43] Both L, Banyard AC, van Dolleweerd C, et al.Passive immunity in the prevention of rabies[J].Lancet Infect Dis, 2012, 12(5): 397-407.DOI: 10.1016/S1473-3099(11)70340-1 [44] Bakker AB, Python C, Kissling CJ, et al.First administration to humans of a monoclonal antibody cocktail against rabies virus: safety, tolerability, and neutralizing activity[J].Vaccine, 2008, 26(47): 5922-5927.DOI: 10.1016/j.vaccine.2008.08.050 [45] World Health Organization.WHO experts consultation on rabies.second report world health organ tech rep ser[EB/OL][2017-09-21], 2013, (982): 1-139.http://apps.who.int/iris/bitstream/10665/85346/1/9789240690943_eng.pdf [46] Sloan SE, Hanlon C, Weldon W, et al.Identification and characterization of a human monoclonal antibody that potently neutralizes a broad panel of rabies virus isolates[J].Vaccine, 2007, 25(15): 2800-2810.DOI: 10.1016/j.vaccine.2006.12.031 [47] Nagarajan T, Marissen WE, Rupprecht CE.Monoclonal antibodies for the prevention of rabies: theory and clinical practice[J].Antibody Technology Journal, 2014, 4: 1-12.DOI:10.2147/ANTI.S33533 [48] Wang Y, Rowley KJ, Booth BJ, et al.G glycoprotein amino acid residues required for human monoclonal antibody RAB1 neutralization are conserved in rabies virus street isolates[J].Antiviral Res, 2011, 91(2): 187-194.DOI: 10.1016/j.antiviral.2011.06.002 [49] Bakker AB, Marissen WE, Kramer RA, et al.Novel human monoclonal antibody combination effectively neutralizing natural rabies virus variants andindividual in vitro escape mutants[J].J Virol, 2005, 79(14): 9062-9068.DOI: 10.1128/JVI.79.14.9062-9068.2005 [50] Goudsmit J, Marissen WE, Weldon WC,et al.Comparison of an anti-rabies human monoclonal antibody combination with human polyclonal anti-rabiesimmune globulin[J].J Infect Dis, 2006, 193(6): 796-801.DOI:10.1086/500470 [51] Marissen WE, Kramer RA, Rice A, et al.Novel rabies virus-neutralizing epitope recognized by human monoclonal antibody: fine mapping and escapemutant analysis[J].J Virol, 2005, 79(8): 4672-4678.DOI: 10.1128/JVI.79.8.4672-4678.2005 [52] De Benedictis P, Minola A, Rota Nodari E, et al.Development of broad-spectrum human monoclonal antibodies for rabies post-exposure prophylaxis[J].EMBO Mol Med, 2016, 8(4): 407-421.DOI: 10.15252/emmm.201505986 [53] Chao TY,Ren S, Shen E, et al.SYN023, a novel humanized monoclonal antibody cocktail, for post-exposure prophylaxis of rabies.PLoS Negl Trop Dis, 2017,20(12): e0006133.DOI: 10.1371/journal.pntd.0006133 [54] 张夏玲, 孙见宇, 殷珏等.全人源抗狂犬病病毒单克隆抗体的制备与鉴定[J].南京医科大学学报(自然科学版), 2012, 32(6): 739-744. [55] 陈超, 张铁钢.人源抗狂犬病毒单克隆抗体载体的构建及烟草转基因研究[J].生物学通报, 2011, 46(2): 46-49.DOI: 10.3969/j.issn.0006-3193.2011.02.018 [56] 王晓虎, 靳玉珠, 丁壮, 等.治疗性狂犬病病毒单克隆抗体的研究进展[J].中国生物制品学杂志, 2009, 22(10): 1032-1035. [57] 刘晓雷, 侯禹男, 陈知航, 等.定量检测猕猴血清中重组人源化抗狂犬病毒单克隆抗体间接ELISA法的建立[J].生物技术通讯, 2008, 19(3): 407-409.DOI: 10.3969/j.issn.1009-0002.2008.03.026 [58] 贾茜, 徐葛林, 赵伟, 等.重组人抗狂犬病毒单抗SO57、SOJB对不同狂犬病毒毒株中和作用的研究[J].病毒学报, 2006, 22(4):256-262.DOI: 10.3321/j.issn:1000-8721.2006.04.003 [59] 李新颖, 吕明.抗体药物在抗感染领域的应用[J].药学学报, 2015, 50(12):1527-1533. [60] Kuzmina NA, Kuzmin IV, Ellison JA, et al.Conservation of binding epitopes for monoclonal antibodies on the rabies virus glycoprotein[J].Antivirals and Antiretrovirals.2013, 5(2): 37-43.DOI: 10.1099/0022-1317-74-8-1539 [61] 王美霞, 贾敏, 金铭, 等.不同剂量重组人源抗狂犬病毒单克隆抗体注射液人体单次给药的安全性[J].中国生物制品学杂志, 2013, 26(7): 986-990.