Generic placeholder image

Infectious Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5265
ISSN (Online): 2212-3989

Review Article

Recent Progress on Neutralizing Antibodies against Hepatitis B Virus and its Implications

Author(s): Binbin Hong, Yumei Wen* and Tianlei Ying*

Volume 19, Issue 3, 2019

Page: [213 - 223] Pages: 11

DOI: 10.2174/1871526518666180628122400

Price: $65

Abstract

Background: Hepatitis B virus (HBV) infection remains a global health problem. As “cure” for chronic hepatitis B is of current priority, hepatitis B immunoglobulin (HBIG) has been utilized for several decades to provide post-exposure prophylaxis.

In recent years, a number of monoclonal antibodies (mAbs) targeting HBV have been developed and demonstrated with high affinity, specificity, and neutralizing potency.

Objective: HBV neutralizing antibodies may play a potentially significant role in the search for an HBV cure. In this review, we will summarize the recent progress in developing HBV-neutralizing antibodies, describing their characteristics and potential clinical applications.

Results and Conclusion: HBV neutralizing antibodies could be a promising alternative in the prevention and treatment of HBV infection. More importantly, global collaboration and coordinated approaches are thus needed to facilitate the development of novel therapies for HBV infection.

Keywords: Hepatitis B virus, neutralizing antibody, HbsAg, infection, HBV cure, antibodies.

Graphical Abstract
[1]
Pan, C.Q.; Zhang, J.X. Natural History and Clinical Consequences of Hepatitis B Virus Infection. Int. J. Med. Sci., 2005, 2(1), 36-40.
[http://dx.doi.org/10.7150/ijms.2.36] [PMID: 15968338]
[2]
Gish, R.; Jia, J.D.; Locarnini, S.; Zoulim, F. Selection of chronic hepatitis B therapy with high barrier to resistance. Lancet Infect. Dis., 2012, 12(4), 341-353.
[http://dx.doi.org/10.1016/S1473-3099(11)70314-0] [PMID: 22326017]
[3]
Revill, P.; Testoni, B.; Locarnini, S.; Zoulim, F. Global strategies are required to cure and eliminate HBV infection. Nat. Rev. Gastroenterol. Hepatol., 2016, 13(4), 239-248.
[http://dx.doi.org/10.1038/nrgastro.2016.7] [PMID: 26907881]
[4]
Michel, M.L.; Deng, Q.; Mancini-Bourgine, M. Therapeutic vaccines and immune-based therapies for the treatment of chronic hepatitis B: perspectives and challenges. J. Hepatol., 2011, 54(6), 1286-1296.
[http://dx.doi.org/10.1016/j.jhep.2010.12.031] [PMID: 21238516]
[5]
Menne, S.; Roneker, C.A.; Korba, B.E.; Gerin, J.L.; Tennant, B.C.; Cote, P.J. Immunization with surface antigen vaccine alone and after treatment with 1-(2-fluoro-5-methyl-β-L-arabinofuranosyl)-uracil (L-FMAU) breaks humoral and cell-mediated immune tolerance in chronic woodchuck hepatitis virus infection. J. Virol., 2002, 76(11), 5305-5314.
[http://dx.doi.org/10.1128/JVI.76.11.5305-5314.2002] [PMID: 11991959]
[6]
Rollier, C.; Sunyach, C.; Barraud, L.; Madani, N.; Jamard, C.; Trepo, C.; Cova, L. Protective and therapeutic effect of DNA-based immunization against hepadnavirus large envelope protein. Gastroenterology, 1999, 116(3), 658-665.
[http://dx.doi.org/10.1016/S0016-5085(99)70188-5] [PMID: 10029625]
[7]
Eren, R.; Lubin, I.; Terkieltaub, D.; Ben-Moshe, O.; Zauberman, A.; Uhlmann, R.; Tzahor, T.; Moss, S.; Ilan, E.; Shouval, D.; Galun, E.; Daudi, N.; Marcus, H.; Reisner, Y.; Dagan, S. Human monoclonal antibodies specific to hepatitis B virus generated in a human/mouse radiation chimera: the Trimera system. Immunology, 1998, 93(2), 154-161.
[http://dx.doi.org/10.1046/j.1365-2567.1998.00426.x] [PMID: 9616363]
[8]
Shin, Y.W.; Ryoo, K.H.; Hong, K.W.; Chang, K.H.; Choi, J.S.; So, M.; Kim, P.K.; Park, J.Y.; Bong, K.T.; Kim, S.H. Human monoclonal antibody against Hepatitis B virus surface antigen (HBsAg). Antiviral Res., 2007, 75(2), 113-120.
[http://dx.doi.org/10.1016/j.antiviral.2007.01.005] [PMID: 17343928]
[9]
Ecker, D.M.; Jones, S.D.; Levine, H.L. The therapeutic monoclonal antibody market. MAbs, 2015, 7(1), 9-14.
[http://dx.doi.org/10.4161/19420862.2015.989042] [PMID: 25529996]
[10]
Ledford, H. ‘Biosimilar’ drugs poised to penetrate market. Nature, 2010, 468(7320), 18-19.
[http://dx.doi.org/10.1038/468018a] [PMID: 21048737]
[11]
Heermann, K.H.; Goldmann, U.; Schwartz, W.; Seyffarth, T.; Baumgarten, H.; Gerlich, W.H. Large surface proteins of hepatitis B virus containing the pre-s sequence. J. Virol., 1984, 52(2), 396-402.
[PMID: 6492255]
[12]
Glebe, D.; Bremer, C.M. The molecular virology of hepatitis B virus. Semin. Liver Dis., 2013, 33(2), 103-112.
[http://dx.doi.org/10.1055/s-0033-1345717] [PMID: 23749666]
[13]
Stirk, H.J.; Thornton, J.M.; Howard, C.R. A topological model for hepatitis B surface antigen. Intervirology, 1992, 33(3), 148-158.
[http://dx.doi.org/10.1159/000150244] [PMID: 1500275]
[14]
Norder, H.; Couroucé, A.M.; Magnius, L.O. Molecular basis of hepatitis B virus serotype variations within the four major subtypes. J. Gen. Virol., 1992, 73(Pt 12), 3141-3145.
[http://dx.doi.org/10.1099/0022-1317-73-12-3141] [PMID: 1469353]
[15]
Lempp, F.A.; Urban, S. Inhibitors of hepatitis B virus attachment and entry. Intervirology, 2014, 57(3-4), 151-157.
[http://dx.doi.org/10.1159/000360948] [PMID: 25034482]
[16]
Yuan, Q.; Ge, S.; Xiong, J.; Yan, Q.; Li, Z.; Hao, X.; Tian, D.; Niu, J.; Su, Z.; Chen, C.; Shih, J.W.; Zhang, J.; Xia, N. A novel immunoassay for PreS1 and/or core-related antigens for detection of HBsAg variants. J. Virol. Methods, 2010, 168(1-2), 108-113.
[http://dx.doi.org/10.1016/j.jviromet.2010.04.029] [PMID: 20451558]
[17]
Chen, W.; Zhang, J.; Zhang, J.; Wang, D.; Li, Y.; Huang, A. Expression of the PreS1 peptide of hepatitis B virus and preparation of its polyclonal antibody. Hybridoma (Larchmt.), 2011, 30(6), 525-530.
[http://dx.doi.org/10.1089/hyb.2011.0065] [PMID: 22149277]
[18]
Neurath, A.R.; Kent, S.B.; Strick, N.; Parker, K. Identification and chemical synthesis of a host cell receptor binding site on hepatitis B virus. Cell, 1986, 46(3), 429-436.
[http://dx.doi.org/10.1016/0092-8674(86)90663-X] [PMID: 3015414]
[19]
Pontisso, P.; Ruvoletto, M.G.; Gerlich, W.H.; Heermann, K.H.; Bardini, R.; Alberti, A. Identification of an attachment site for human liver plasma membranes on hepatitis B virus particles. Virology, 1989, 173(2), 522-530.
[http://dx.doi.org/10.1016/0042-6822(89)90564-3] [PMID: 2480688]
[20]
Barrera, A.; Guerra, B.; Notvall, L.; Lanford, R.E. Mapping of the hepatitis B virus pre-S1 domain involved in receptor recognition. J. Virol., 2005, 79(15), 9786-9798.
[http://dx.doi.org/10.1128/JVI.79.15.9786-9798.2005] [PMID: 16014940]
[21]
Chi, S.W.; Kim, D.H.; Lee, S.H.; Chang, I.; Han, K.H. Pre-structured motifs in the natively unstructured preS1 surface antigen of hepatitis B virus. Protein Sci., 2007, 16(10), 2108-2117.
[http://dx.doi.org/10.1110/ps.072983507] [PMID: 17766372]
[22]
Listed, N. Recommendations for protection against viral hepatitis. Recommendation of the Immunization Practices Advisory Committee. Centers for Disease Control, Department of Health and Human Services. Ann. Intern. Med., 1985, 103(3), 391-402.
[http://dx.doi.org/10.7326/0003-4819-103-3-391] [PMID: 3161440]
[23]
Gaggar, A.; Coeshott, C.; Apelian, D.; Rodell, T.; Armstrong, B.R.; Shen, G.; Subramanian, G.M.; McHutchison, J.G. Safety, tolerability and immunogenicity of GS-4774, a hepatitis B virus-specific therapeutic vaccine, in healthy subjects: a randomized study. Vaccine, 2014, 32(39), 4925-4931.
[http://dx.doi.org/10.1016/j.vaccine.2014.07.027] [PMID: 25045824]
[24]
Beasley, R.P.; Hwang, L.Y.; Stevens, C.E.; Lin, C.C.; Hsieh, F.J.; Wang, K.Y.; Sun, T.S.; Szmuness, W. Efficacy of hepatitis B immune globulin for prevention of perinatal transmission of the hepatitis B virus carrier state: final report of a randomized double-blind, placebo-controlled trial. Hepatology, 1983, 3(2), 135-141.
[http://dx.doi.org/10.1002/hep.1840030201] [PMID: 6339349]
[25]
Lo, K.J.; Tsai, Y.T.; Lee, S.D.; Yeh, C.L.; Wang, J.Y.; Chiang, B.N.; Wu, T.C.; Yeh, P.S.; Goudeau, A.; Coursaget, P. Combined passive and active immunization for interruption of perinatal transmission of hepatitis B virus in Taiwan. Hepatogastroenterology, 1985, 32(2), 65-68.
[PMID: 3159639]
[26]
Johnson, P.J.; Wansbrough-Jones, M.H.; Portmann, B.; Eddleston, A.L.; Williams, R.; Maycook, W.D.; Calne, R.Y. Familial HBsAg-positive hepatoma: treatment with orthotopic liver transplantation and specific immunoglobulin. BMJ, 1978, 1(6107), 216.
[http://dx.doi.org/10.1136/bmj.1.6107.216] [PMID: 202371]
[27]
Ehrlich, P.H.; Moustafa, Z.A.; Justice, J.C.; Harfeldt, K.E.; Kelley, R.L.; Ostberg, L. Characterization of human monoclonal antibodies directed against hepatitis B surface antigen. Hum. Antibodies Hybridomas, 1992, 3(1), 2-7.
[http://dx.doi.org/10.3233/HAB-1992-3101] [PMID: 1374272]
[28]
Witherell, G. XTL-001. XTL Pharmaceuticals. Curr. Opin. Investig. Drugs, 2002, 3(5), 684-692.
[PMID: 12090540]
[29]
Grazi, D.G.L.; Mazziotti, A.; Sama, C.; Jovine, E.; Stefanini, F.; Paladini, R.; Rossi, R.; Cavallari, A. Liver transplantation in HBsAg‐positive HBV‐DNA—negative cirrhotics: Immunoprophylaxis and long‐term outcome. Liver transplantation and surgery: official publication of the American Association for the study of liver diseases and the international liver transplantation society, 1996, 2, 418-25.
[30]
Manne, V.; Allen, R.M.; Saab, S. Strategies for the prevention of recurrent hepatitis B virus infection after liver transplantation. Gastroenterol. Hepatol. (N. Y.), 2014, 10(3), 175-179.
[PMID: 24829544]
[31]
Müller, R.; Gubernatis, G.; Farle, M.; Niehoff, G.; Klein, H.; Wittekind, C.; Tusch, G.; Lautz, H.U.; Böker, K.; Stangel, W. Liver transplantation in HBs antigen (HBsAg) carriers. Prevention of hepatitis B virus (HBV) recurrence by passive immunization. J. Hepatol., 1991, 13(1), 90-96.
[http://dx.doi.org/10.1016/0168-8278(91)90869-D] [PMID: 1918881]
[32]
Samuel, D.; Bismuth, A.; Serres, C.; Arulnaden, J.L.; Reynes, M.; Benhamou, J.P.; Brechot, C.; Bismuth, H. HBV infection after liver transplantation in HBsAg positive patients: experience with long-term immunoprophylaxis. Transplant. Proc., 1991, 23(1 Pt 2), 1492-1494.
[PMID: 1989275]
[33]
Terrault, N.A.; Zhou, S.; Combs, C.; Hahn, J.A.; Lake, J.R.; Roberts, J.P.; Ascher, N.L.; Wright, T.L. Prophylaxis in liver transplant recipients using a fixed dosing schedule of hepatitis B immunoglobulin. Hepatology, 1996, 24(6), 1327-1333.
[http://dx.doi.org/10.1002/hep.510240601] [PMID: 8938155]
[34]
Wen, Y.M.; Wu, X.H.; Hu, D.C.; Zhang, Q.P.; Guo, S.Q. Hepatitis B vaccine and anti-HBs complex as approach for vaccine therapy. Lancet, 1995, 345(8964), 1575-1576.
[http://dx.doi.org/10.1016/S0140-6736(95)91126-X] [PMID: 7791465]
[35]
Wen, Y.M.; Xiong, S.D.; Zhang, W. Solid matrix-antibody-antigen complex can clear viraemia and antigenaemia in persistent duck hepatitis B virus infection. J. Gen. Virol., 1994, 75(Pt 2), 335-339.
[http://dx.doi.org/10.1099/0022-1317-75-2-335] [PMID: 8113755]
[36]
Wang, X.Y.; Zhang, X.X.; Yao, X.; Jiang, J.H.; Xie, Y.H.; Yuan, Z.H.; Wen, Y.M. Serum HBeAg sero-conversion correlated with decrease of HBsAg and HBV DNA in chronic hepatitis B patients treated with a therapeutic vaccine. Vaccine, 2010, 28(51), 8169-8174.
[http://dx.doi.org/10.1016/j.vaccine.2010.09.093] [PMID: 20937312]
[37]
Xu, D.Z.; Huang, K.L.; Zhao, K.; Xu, L.F.; Shi, N.; Yuan, Z.H.; Wen, Y.M. Vaccination with recombinant HBsAg-HBIG complex in healthy adults. Vaccine, 2005, 23(20), 2658-2664.
[http://dx.doi.org/10.1016/j.vaccine.2004.10.040] [PMID: 15780449]
[38]
Yao, X.; Zheng, B.; Zhou, J.; Xu, D.Z.; Zhao, K.; Sun, S.H.; Yuan, Z.H.; Wen, Y.M. Therapeutic effect of hepatitis B surface antigen-antibody complex is associated with cytolytic and non-cytolytic immune responses in hepatitis B patients. Vaccine, 2007, 25(10), 1771-1779.
[http://dx.doi.org/10.1016/j.vaccine.2006.11.019] [PMID: 17224217]
[39]
Glebe, D.; Aliakbari, M.; Krass, P.; Knoop, E.V.; Valerius, K.P.; Gerlich, W.H. Pre-s1 antigen-dependent infection of Tupaia hepatocyte cultures with human hepatitis B virus. J. Virol., 2003, 77(17), 9511-9521.
[http://dx.doi.org/10.1128/JVI.77.17.9511-9521.2003] [PMID: 12915565]
[40]
Kucinskaite-Kodze, I.; Pleckaityte, M.; Bremer, C.M.; Seiz, P.L.; Zilnyte, M.; Bulavaite, A.; Mickiene, G.; Zvirblis, G.; Sasnauskas, K.; Glebe, D.; Zvirbliene, A. New broadly reactive neutralizing antibodies against hepatitis B virus surface antigen. Virus Res., 2016, 211, 209-221.
[http://dx.doi.org/10.1016/j.virusres.2015.10.024] [PMID: 26541316]
[41]
Kunpeng, Z.; Yugang, W.; Jugao, C.; Yan, L.; Beifen, S.; Yuanfang, M. The construction and expression of a novel chimeric anti-DR5 antibody. Hybridoma (Larchmt.), 2009, 28(2), 101-105.
[http://dx.doi.org/10.1089/hyb.2008.0080] [PMID: 19249994]
[42]
Tiwari, A.; Dutta, D.; Khanna, N.; Acharya, S.K.; Sinha, S. Generation and characterization of high affinity humanized fab against hepatitis B surface antigen. Mol. Biotechnol., 2009, 43(1), 29-40.
[http://dx.doi.org/10.1007/s12033-009-9165-9] [PMID: 19326261]
[43]
Kim, K.S.; Kim, H.J.; Han, B.W.; Myung, P.K.; Hong, H.J. Construction of a humanized antibody to hepatitis B surface antigen by specificity-determining residues (SDR)-grafting and de-immunization. Biochem. Biophys. Res. Commun., 2010, 396(2), 231-237.
[http://dx.doi.org/10.1016/j.bbrc.2010.04.071] [PMID: 20399745]
[44]
Hong, H.J.; Ryu, C.J.; Hur, H.; Kim, S.; Oh, H.K.; Oh, M.S.; Park, S.Y. In vivo neutralization of hepatitis B virus infection by an anti-preS1 humanized antibody in chimpanzees. Virology, 2004, 318(1), 134-141.
[http://dx.doi.org/10.1016/j.virol.2003.09.014] [PMID: 14972542]
[45]
Ryu, C.J.; Padlan, E.A.; Jin, B.R.; Yoo, O.J.; Hong, H.J. A humanized antibody with specificity for hepatitis B surface antigen. Hum. Antibodies Hybridomas, 1996, 7(3), 113-122.
[http://dx.doi.org/10.3233/HAB-1996-7304] [PMID: 9057059]
[46]
Tiwari, A.; Khanna, N.; Acharya, S.K.; Sinha, S. Humanization of high affinity anti-HBs antibody by using human consensus sequence and modification of selected minimal positional template and packing residues. Vaccine, 2009, 27(17), 2356-2366.
[http://dx.doi.org/10.1016/j.vaccine.2009.02.019] [PMID: 19428851]
[47]
Kim, J.H.; Gripon, P.; Bouezzedine, F.; Jeong, M.S.; Chi, S.W.; Ryu, S.E.; Hong, H.J. Enhanced humanization and affinity maturation of neutralizing anti-hepatitis B virus preS1 antibody based on antigen-antibody complex structure. FEBS Lett., 2015, 589(2), 193-200.
[http://dx.doi.org/10.1016/j.febslet.2014.11.046] [PMID: 25481411]
[48]
Zhang, T.Y.; Yuan, Q.; Zhao, J.H.; Zhang, Y.L.; Yuan, L.Z.; Lan, Y.; Lo, Y.C.; Sun, C.P.; Wu, C.R.; Zhang, J.F.; Zhang, Y.; Cao, J.L.; Guo, X.R.; Liu, X.; Mo, X.B.; Luo, W.X.; Cheng, T.; Chen, Y.X.; Tao, M.H.; Shih, J.W.; Zhao, Q.J.; Zhang, J.; Chen, P.J.; Yuan, Y.A.; Xia, N.S. Prolonged suppression of HBV in mice by a novel antibody that targets a unique epitope on hepatitis B surface antigen. Gut, 2016, 65(4), 658-671.
[http://dx.doi.org/10.1136/gutjnl-2014-308964] [PMID: 26423112]
[49]
Bose, B.; Chugh, D.A.; Kala, M.; Acharya, S.K.; Khanna, N.; Sinha, S. Characterization and molecular modeling of a highly stable anti-Hepatitis B surface antigen scFv. Mol. Immunol., 2003, 40(9), 617-631.
[http://dx.doi.org/10.1016/j.molimm.2003.07.002] [PMID: 14597165]
[50]
Ryu, C.J.; Cho, D.Y.; Gripon, P.; Kim, H.S.; Guguen-Guillouzo, C.; Hong, H.J. An 80-kilodalton protein that binds to the pre-S1 domain of hepatitis B virus. J. Virol., 2000, 74(1), 110-116.
[http://dx.doi.org/10.1128/JVI.74.1.110-116.2000] [PMID: 10590097]
[51]
Ryu, C.J.; Kim, Y.K.; Hur, H.; Kim, H.S.; Oh, J.M.; Kang, Y.J.; Hong, H.J. Mouse monoclonal antibodies to hepatitis B virus preS1 produced after immunization with recombinant preS1 peptide. Hybridoma, 2000, 19(2), 185-189.
[http://dx.doi.org/10.1089/02724570050031248] [PMID: 10868800]
[52]
Chi, S.W.; Maeng, C.Y.; Kim, S.J.; Oh, M.S.; Ryu, C.J.; Kim, S.J.; Han, K.H.; Hong, H.J.; Ryu, S.E. Broadly neutralizing anti-hepatitis B virus antibody reveals a complementarity determining region H3 lid-opening mechanism. Proc. Natl. Acad. Sci. USA, 2007, 104(22), 9230-9235.
[http://dx.doi.org/10.1073/pnas.0701279104] [PMID: 17517649]
[53]
Kim, S.H.; Kim, S.H.; Oh, H.K.; Ryu, C.J.; Park, S.Y.; Hong, H.J. In vivo hepatitis B virus-neutralizing activity of an anti-HBsAg humanized antibody in chimpanzees. Exp. Mol. Med., 2008, 40(1), 145-149.
[http://dx.doi.org/10.3858/emm.2008.40.1.145] [PMID: 18305407]
[54]
Baca, M.; Presta, L.G.; O’Connor, S.J.; Wells, J.A. Antibody humanization using monovalent phage display. J. Biol. Chem., 1997, 272(16), 10678-10684.
[http://dx.doi.org/10.1074/jbc.272.16.10678] [PMID: 9099717]
[55]
Nakamura, K.; Tanaka, Y.; Shitara, K.; Hanai, N. Construction of humanized anti-ganglioside monoclonal antibodies with potent immune effector functions. Cancer Immunol. Immunother., 2001, 50(5), 275-284.
[http://dx.doi.org/10.1007/PL00006689] [PMID: 11499811]
[56]
McMahon, G.; Ehrlich, P.H.; Moustafa, Z.A.; McCarthy, L.A.; Dottavio, D.; Tolpin, M.D.; Nadler, P.I.; Ostberg, L. Genetic alterations in the gene encoding the major HBsAg: DNA and immunological analysis of recurrent HBsAg derived from monoclonal antibody-treated liver transplant patients. Hepatology, 1992, 15(5), 757-766.
[http://dx.doi.org/10.1002/hep.1840150503] [PMID: 1568715]
[57]
Ogata, N.; Ostberg, L.; Ehrlich, P.H.; Wong, D.C.; Miller, R.H.; Purcell, R.H. Markedly prolonged incubation period of hepatitis B in a chimpanzee passively immunized with a human monoclonal antibody to the a determinant of hepatitis B surface antigen. Proc. Natl. Acad. Sci. USA, 1993, 90(7), 3014-3018.
[http://dx.doi.org/10.1073/pnas.90.7.3014] [PMID: 8464917]
[58]
Kim, S.H.; Shin, Y.W.; Hong, K.W.; Chang, K.H.; Ryoo, K.H.; Paik, S.H.; Kim, J.M.; Brotman, B.; Pfahler, W.; Prince, A.M. Neutralization of hepatitis B virus (HBV) by human monoclonal antibody against HBV surface antigen (HBsAg) in chimpanzees. Antiviral Res., 2008, 79(3), 188-191.
[http://dx.doi.org/10.1016/j.antiviral.2008.03.006] [PMID: 18479762]
[59]
Cerino, A.; Bremer, C.M.; Glebe, D.; Mondelli, M.U. A Human Monoclonal Antibody against Hepatitis B Surface Antigen with Potent Neutralizing Activity. PLoS One, 2015, 10(4)e0125704
[http://dx.doi.org/10.1371/journal.pone.0125704] [PMID: 25923526]
[60]
Wang, W.; Sun, L.; Li, T.; Ma, Y.; Li, J.; Liu, Y.; Li, M.; Wang, L.; Li, C.; Xie, Y.; Wen, Y.; Liang, M.; Chen, L.; Tong, S. A human monoclonal antibody against small envelope protein of hepatitis B virus with potent neutralization effect. MAbs, 2016, 8(3), 468-477.
[http://dx.doi.org/10.1080/19420862.2015.1134409] [PMID: 26713590]
[61]
Li, D.; He, W.; Liu, X.; Zheng, S.; Qi, Y.; Li, H.; Mao, F.; Liu, J.; Sun, Y.; Pan, L.; Du, K.; Ye, K.; Li, W.; Sui, J. A potent human neutralizing antibody Fc-dependently reduces established HBV infections. eLife, 2017, 6, 6.
[http://dx.doi.org/10.7554/eLife.26738] [PMID: 28949917]
[62]
Regales, L.; Gong, Y.; Shen, R.; de Stanchina, E.; Vivanco, I.; Goel, A.; Koutcher, J.A.; Spassova, M.; Ouerfelli, O.; Mellinghoff, I.K.; Zakowski, M.F.; Politi, K.A.; Pao, W. Dual targeting of EGFR can overcome a major drug resistance mutation in mouse models of EGFR mutant lung cancer. J. Clin. Invest., 2009, 119(10), 3000-3010.
[http://dx.doi.org/10.1172/JCI38746] [PMID: 19759520]
[63]
Eren, R.; Ilan, E.; Nussbaum, O.; Lubin, I.; Terkieltaub, D.; Arazi, Y.; Ben-Moshe, O.; Kitchinzky, A.; Berr, S.; Gopher, J.; Zauberman, A.; Galun, E.; Shouval, D.; Daudi, N.; Eid, A.; Jurim, O.; Magnius, L.O.; Hammas, B.; Reisner, Y.; Dagan, S. Preclinical evaluation of two human anti-hepatitis B virus (HBV) monoclonal antibodies in the HBV-trimera mouse model and in HBV chronic carrier chimpanzees. Hepatology, 2000, 32(3), 588-596.
[http://dx.doi.org/10.1053/jhep.2000.9632] [PMID: 10960454]
[64]
Galun, E.; Eren, R.; Safadi, R.; Ashour, Y.; Terrault, N.; Keeffe, E.B.; Matot, E.; Mizrachi, S.; Terkieltaub, D.; Zohar, M.; Lubin, I.; Gopher, J.; Shouval, D.; Dagan, S. Clinical evaluation (phase I) of a combination of two human monoclonal antibodies to HBV: safety and antiviral properties. Hepatology, 2002, 35(3), 673-679.
[http://dx.doi.org/10.1053/jhep.2002.31867] [PMID: 11870383]
[65]
Heijtink, R.; Paulij, W.; van Bergen, P.; van Roosmalen, M.; Rohm, D.; Eichentopf, B.; Muchmore, E.; de Man, R.; Osterhaus, A. In vivo activity of a mixture of two human monoclonal antibodies (anti-HBs) in a chronic hepatitis B virus carrier chimpanzee. J. Gen. Virol., 1999, 80(Pt 6), 1529-1535.
[http://dx.doi.org/10.1099/0022-1317-80-6-1529] [PMID: 10374972]
[66]
Heijtink, R.A.; Kruining, J.; Weber, Y.A.; de Man, R.A.; Schalm, S.W. Anti-hepatitis B virus activity of a mixture of two monoclonal antibodies in an “inhibition in solution” assay. Hepatology, 1995, 22(4 Pt 1), 1078-1083.
[http://dx.doi.org/10.1002/hep.1840220410] [PMID: 7557854]
[67]
Sankhyan, A.; Sharma, C.; Dutta, D.; Sharma, T.; Chosdol, K.; Wakita, T.; Watashi, K.; Awasthi, A.; Acharya, S.K.; Khanna, N.; Tiwari, A.; Sinha, S. Inhibition of preS1-hepatocyte interaction by an array of recombinant human antibodies from naturally recovered individuals. Sci. Rep., 2016, 6, 21240.
[http://dx.doi.org/10.1038/srep21240] [PMID: 26888694]
[68]
Tajiri, K.; Ozawa, T.; Jin, A.; Tokimitsu, Y.; Minemura, M.; Kishi, H.; Sugiyama, T.; Muraguchi, A. Analysis of the epitope and neutralizing capacity of human monoclonal antibodies induced by hepatitis B vaccine. Antiviral Res., 2010, 87(1), 40-49.
[http://dx.doi.org/10.1016/j.antiviral.2010.04.006] [PMID: 20412816]
[69]
Neumann, A.U.; Phillips, S.; Levine, I.; Ijaz, S.; Dahari, H.; Eren, R.; Dagan, S.; Naoumov, N.V. Novel mechanism of antibodies to hepatitis B virus in blocking viral particle release from cells. Hepatology, 2010, 52(3), 875-885.
[http://dx.doi.org/10.1002/hep.23778] [PMID: 20593455]
[70]
Park, S.S.; Ryu, C.J.; Kang, Y.J.; Kashmiri, S.V.S.; Hong, H.J. Generation and characterization of a novel tetravalent bispecific antibody that binds to hepatitis B virus surface antigens. Mol. Immunol., 2000, 37(18), 1123-1130.
[http://dx.doi.org/10.1016/S0161-5890(01)00027-X] [PMID: 11451417]
[71]
Tan, W.; Meng, Y.; Li, H.; Chen, Y.; Han, S.; Zeng, J.; Huang, A.; Li, B.; Zhang, Y.; Guo, Y. A bispecific antibody against two different epitopes on hepatitis B surface antigen has potent hepatitis B virus neutralizing activity. MAbs, 2013, 5(6), 946-955.
[http://dx.doi.org/10.4161/mabs.26390] [PMID: 24492346]

Rights & Permissions Print Export Cite as
© 2024 Bentham Science Publishers | Privacy Policy