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Research Progress of the Screening Technique for HIV- 1 Broad-spectrum Neutralizing Antibodies |
JIANG Wen-ling1,DENG Ting-ting2,LI Shao-wei1,2,GU Ying1,2,**() |
1 National Institute of Diagnostics and Vaccine Development in Infectious Diseases, School of Public Health, Xiamen University, Xiamen 361102, China 2 State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, School of Life Sciences, Xiamen University, Xiamen 361102, China |
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Abstract HIV-1 broadly neutralizing antibodies (HIV-1 bNAbs) are a class of antibodies that can neutralize most of the circulating strains. The study of HIV-1 bNAbs can provide candidates for anti-AIDS drugs and guide vaccine design, and meanwhile HIV-1 bNAbs is an important indicator for evaluating the efficacy of HIV-1 vaccines. HIV-1 bNAbs can be obtained through traditional screening techniques, such as hybridoma technology, Epstein-Barr virus transformation, and the display library technology. In recent years, with the development of single-cell cloning and sorting technologies, the screening efficiency and antibody specificity of HIV-1 bNAbs have significantly improved. Combined screening methods and novel screening technologies, such as LIBRA-seq and bioinformatics-assisted screening techniques, can unify antibody sequences and functional information, providing technical support for HIV-1 bNAb screening and vaccine design. In addition, these screening techniques and methods for HIV-1 can also be used for the screening of bNAbs against other viruses, providing useful insights into vaccine design and antiviral drug development. This article reviews the widely used screening techniques and latest advances in HIV-1 bNAbs, providing a reference for the screening of HIV-1 or other viruses’ bNAbs in the future.
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Received: 13 March 2023
Published: 08 October 2023
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|
[1] |
Lee J H, Crotty S. HIV vaccinology: 2021 update. Seminars in Immunology, 2021, 51: 101470.
doi: 10.1016/j.smim.2021.101470
|
|
|
[2] |
UNAIDS 2021 Epidemiological Estimates. Global HIV & AIDS statistics. [2022-02-24]. https://www.unaids.org/en/resources/fact-sheet.
|
|
|
[3] |
Li G D, Wang Y L, De Clercq E. Approved HIV reverse transcriptase inhibitors in the past decade. Acta Pharmaceutica Sinica B, 2022, 12(4): 1567-1590.
doi: 10.1016/j.apsb.2021.11.009
pmid: 35847492
|
|
|
[4] |
Markham A. Ibalizumab: first global approval. Drugs, 2018, 78(7): 781-785.
doi: 10.1007/s40265-018-0907-5
pmid: 29675744
|
|
|
[5] |
Mullard A. FDA approves 100th monoclonal antibody product. Nature Reviews Drug Discovery, 2021, 20(7): 491-495.
doi: 10.1038/d41573-021-00079-7
pmid: 33953368
|
|
|
[6] |
Corey L, Gilbert P B, Juraska M, et al. Two randomized trials of neutralizing antibodies to prevent HIV-1 acquisition. The New England Journal of Medicine, 2021, 384(11): 1003-1014.
doi: 10.1056/NEJMoa2031738
pmid: 33730454
|
|
|
[7] |
Gaebler C, Nogueira L, Stoffel E, et al. Prolonged viral suppression with anti-HIV-1 antibody therapy. Nature, 2022, 606(7913): 368-374.
doi: 10.1038/s41586-022-04597-1
|
|
|
[8] |
Gruell H, Gunst J D, Cohen Y Z, et al. Effect of 3BNC117 and romidepsin on the HIV-1 reservoir in people taking suppressive antiretroviral therapy (ROADMAP): a randomised, open-label, phase 2A trial. The Lancet Microbe, 2022, 3(3): e203-e214.
doi: 10.1016/S2666-5247(21)00239-1
|
|
|
[9] |
Haynes B F, Burton D R, Mascola J R. Multiple roles for HIV broadly neutralizing antibodies. Science Translational Medicine, 2019, 11(516): eaaz2686.
doi: 10.1126/scitranslmed.aaz2686
|
|
|
[10] |
Julg B, Barouch D. Broadly neutralizing antibodies for HIV-1 prevention and therapy. Seminars in Immunology, 2021, 51: 101475.
doi: 10.1016/j.smim.2021.101475
|
|
|
[11] |
Prashar P, Swain S, Adhikari N, et al. A novel high-throughput single B-cell cloning platform for isolation and characterization of high-affinity and potent SARS-CoV-2 neutralizing antibodies. Antiviral Research, 2022, 203: 105349.
doi: 10.1016/j.antiviral.2022.105349
|
|
|
[12] |
Smith S A, Crowe J E Jr. Use of human hybridoma technology to isolate human monoclonal antibodies. Microbiology Spectrum, 2015, 3(1): AID-0027-2014.
|
|
|
[13] |
Köhler G, Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature, 1975, 256(5517): 495-497.
doi: 10.1038/256495a0
|
|
|
[14] |
Parray H A, Shukla S, Samal S, et al. Hybridoma technology a versatile method for isolation of monoclonal antibodies, its applicability across species, limitations, advancement and future perspectives. International Immunopharmacology, 2020, 85: 106639.
doi: 10.1016/j.intimp.2020.106639
|
|
|
[15] |
Stephenson K E, Wagh K, Korber B, et al. Vaccines and broadly neutralizing antibodies for HIV-1 prevention. Annual Review of Immunology, 2020, 38: 673-703.
doi: 10.1146/annurev-immunol-080219-023629
pmid: 32340576
|
|
|
[16] |
Moraes J Z, Hamaguchi B, Braggion C, et al. Hybridoma technology: is it still useful? Current Research in Immunology, 2021, 2: 32-40.
|
|
|
[17] |
Mitra S, Tomar P C. Hybridoma technology; advancements, clinical significance, and future aspects. Journal, Genetic Engineering & Biotechnology, 2021, 19(1): 159.
|
|
|
[18] |
Lonberg N, Taylor L D, Harding F A, et al. Antigen-specific human antibodies from mice comprising four distinct genetic modifications. Nature, 1994, 368(6474): 856-859.
doi: 10.1038/368856a0
|
|
|
[19] |
Markham A. Correction to: Ibalizumab: first global approval. Drugs, 2018, 78(8): 859.
doi: 10.1007/s40265-018-0926-2
pmid: 29846911
|
|
|
[20] |
Wang L W, Shen H Y, Nobre L, et al. Epstein-Barr-virus-induced one-carbon metabolism drives B cell transformation. Cell Metabolism, 2019, 30(3): 539-555.e11.
doi: S1550-4131(19)30306-7
pmid: 31257153
|
|
|
[21] |
Damania B, Kenney S C, Raab-Traub N. Epstein-Barr virus: biology and clinical disease. Cell, 2022, 185(20): 3652-3670.
doi: 10.1016/j.cell.2022.08.026
pmid: 36113467
|
|
|
[22] |
Valgardsdottir R, Cattaneo I, Napolitano G, et al. Identification of human SARS-CoV-2 monoclonal antibodies from convalescent patients using EBV immortalization. Antibodies, 2021, 10(3): 26.
doi: 10.3390/antib10030026
|
|
|
[23] |
Sun Z H, Lu S Q, Yang Z, et al. Isolation and characterization of an HIV-1 envelope glycoprotein-specific B-cell from an immortalized human naïve B-cell library. Journal of General Virology, 2017, 98(4): 791-798.
doi: 10.1099/jgv.0.000706
pmid: 28073404
|
|
|
[24] |
Miller N L, Clark T, Raman R, et al. Glycans in virus-host interactions: a structural perspective. Frontiers in Molecular Biosciences, 2021, 8: 666756.
doi: 10.3389/fmolb.2021.666756
|
|
|
[25] |
Krebs S J, Kwon Y D, Schramm C A, et al. Longitudinal analysis reveals early development of three MPER-directed neutralizing antibody lineages from an HIV-1-infected individual. Immunity, 2019, 50(3): 677-691.e13.
doi: S1074-7613(19)30074-3
pmid: 30876875
|
|
|
[26] |
Mahdavi S Z B, Oroojalian F, Eyvazi S, et al. An overview on display systems (phage, bacterial, and yeast display) for production of anticancer antibodies; advantages and disadvantages. International Journal of Biological Macromolecules, 2022, 208: 421-442.
doi: 10.1016/j.ijbiomac.2022.03.113
|
|
|
[27] |
Wang Y, Shan Y M, Gao X Y, et al. Screening and expressing HIV-1 specific antibody fragments in Saccharomyces cerevisiae. Molecular Immunology, 2018, 103: 279-285.
doi: 10.1016/j.molimm.2018.10.013
|
|
|
[28] |
Mathew E, Zhu H, Connelly S M, et al. Display of the HIV envelope protein at the yeast cell surface for immunogen development. PLoS One, 2018, 13(10): e0205756.
doi: 10.1371/journal.pone.0205756
|
|
|
[29] |
Ledsgaard L, Ljungars A, Rimbault C, et al. Advances in antibody phage display technology. Drug Discovery Today, 2022, 27(8): 2151-2169.
doi: 10.1016/j.drudis.2022.05.002
|
|
|
[30] |
Jaroszewicz W, Morcinek-Orłowska J, Pierzynowska K, et al. Phage display and other peptide display technologies. FEMS Microbiology Reviews, 2022, 46(2): fuab052.
doi: 10.1093/femsre/fuab052
|
|
|
[31] |
Muyldermans S. Applications of nanobodies. Annual Review of Animal Biosciences, 2021, 9: 401-421.
doi: 10.1146/annurev-animal-021419-083831
pmid: 33233943
|
|
|
[32] |
Weiss R A, Verrips C T. Nanobodies that neutralize HIV. Vaccines, 2019, 7(3): 77.
doi: 10.3390/vaccines7030077
|
|
|
[33] |
Omidfar K, Daneshpour M. Advances in phage display technology for drug discovery. Expert Opinion on Drug Discovery, 2015, 10(6): 651-669.
doi: 10.1517/17460441.2015.1037738
pmid: 25910798
|
|
|
[34] |
Doores K J, Fulton Z, Huber M, et al. Antibody 2G 12 recognizes di-mannose equivalently in domain- and nondomain-exchanged forms but only binds the HIV-1 glycan shield if domain exchanged. Journal of Virology, 2010, 84(20): 10690-10699.
doi: 10.1128/JVI.01110-10
pmid: 20702629
|
|
|
[35] |
Burton D R, Pyati J, Koduri R, et al. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science, 1994, 266(5187): 1024-1027.
pmid: 7973652
|
|
|
[36] |
Yang G, Holl T M, Liu Y, et al. Identification of autoantigens recognized by the 2F5 and 4E 10 broadly neutralizing HIV-1 antibodies. The Journal of Experimental Medicine, 2013, 210(2): 241-256.
doi: 10.1084/jem.20121977
|
|
|
[37] |
McCoy L E, Burton D R. Identification and specificity of broadly neutralizing antibodies against HIV. Immunological Reviews, 2017, 275(1): 11-20.
doi: 10.1111/imr.12484
pmid: 28133814
|
|
|
[38] |
Walker L M, Huber M, Doores K J, et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature, 2011, 477(7365): 466-470.
doi: 10.1038/nature10373
|
|
|
[39] |
Walker L M, Phogat S K, Chan-Hui P Y, et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science, 2009, 326(5950): 285-289.
doi: 10.1126/science.1178746
pmid: 19729618
|
|
|
[40] |
Doria-Rose N A, Bhiman J N, Roark R S, et al. New member of the V1V2-directed CAP256-VRC 26 lineage that shows increased breadth and exceptional potency. Journal of Virology, 2015, 90(1): 76-91.
doi: 10.1128/JVI.01791-15
|
|
|
[41] |
Bonsignori M, Hwang K K, Chen X, et al. Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. Journal of Virology, 2011, 85(19): 9998-10009.
doi: 10.1128/JVI.05045-11
pmid: 21795340
|
|
|
[42] |
Bonsignori M, Zhou T Q, Sheng Z Z, et al. Maturation pathway from germline to broad HIV-1 neutralizer of a CD4-mimic antibody. Cell, 2016, 165(2): 449-463.
doi: 10.1016/j.cell.2016.02.022
pmid: 26949186
|
|
|
[43] |
Huang J H, Ofek G, Laub L, et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature, 2012, 491(7424): 406-412.
doi: 10.1038/nature11544
|
|
|
[44] |
Falkowska E, Le K, Ramos A, et al. Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp 41 on cleaved envelope trimers. Immunity, 2014, 40(5): 657-668.
doi: 10.1016/j.immuni.2014.04.009
pmid: 24768347
|
|
|
[45] |
Huang J H, Kang B H, Pancera M, et al. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-gp120 interface. Nature, 2014, 515(7525): 138-142.
doi: 10.1038/nature13601
|
|
|
[46] |
Perry S T, Keogh E, Morton M, et al. Single-cell screening method for the selection and recovery of antibodies with desired specificities from enriched human memory B cell populations. Journal of Visualized Experiments, 2019(150). DOI: 10.3791/59809.
doi: 10.3791/59809
|
|
|
[47] |
Starkie D O, Compson J E, Rapecki S, et al. Generation of recombinant monoclonal antibodies from immunised mice and rabbits via flow cytometry and sorting of antigen-specific IgG+ memory B cells. PLoS One, 2016, 11(3): e0152282.
doi: 10.1371/journal.pone.0152282
|
|
|
[48] |
Sok D, Pauthner M, Briney B, et al. A prominent site of antibody vulnerability on HIV envelope incorporates a motif associated with CCR5 binding and its camouflaging glycans. Immunity, 2016, 45(1): 31-45.
doi: 10.1016/j.immuni.2016.06.026
pmid: 27438765
|
|
|
[49] |
Mouquet H, Scharf L, Euler Z, et al. Complex-type N-glycan recognition by potent broadly neutralizing HIV antibodies. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(47): E3268-E3277.
|
|
|
[50] |
Liao H X, Lynch R, Zhou T Q, et al. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature, 2013, 496(7446): 469-476.
doi: 10.1038/nature12053
|
|
|
[51] |
Zhou T Q, Georgiev I, Wu X L, et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science, 2010, 329(5993): 811-817.
doi: 10.1126/science.1192819
pmid: 20616231
|
|
|
[52] |
van Gils M J, van den Kerkhof T L G M, Ozorowski G, et al. An HIV-1 antibody from an elite neutralizer implicates the fusion peptide as a site of vulnerability. Nature Microbiology, 2017, 2(2): 1-10.
|
|
|
[53] |
Wu X L, Zhou T Q, Zhu J, et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science, 2011, 333(6049): 1593-1602.
doi: 10.1126/science.1207532
pmid: 21835983
|
|
|
[54] |
Scheid J F, Mouquet H, Ueberheide B, et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science, 2011, 333(6049): 1633-1637.
doi: 10.1126/science.1207227
pmid: 21764753
|
|
|
[55] |
Carbonetti S, Oliver B G, Vigdorovich V, et al. A method for the isolation and characterization of functional murine monoclonal antibodies by single B cell cloning. Journal of Immunological Methods, 2017, 448: 66-73.
doi: S0022-1759(17)30067-4
pmid: 28554543
|
|
|
[56] |
Kreer C, Döring M, Lehnen N, et al. openPrimeR for multiplex amplification of highly diverse templates. Journal of Immunological Methods, 2020, 480: 112752.
doi: 10.1016/j.jim.2020.112752
|
|
|
[57] |
Gieselmann L, Kreer C, Ercanoglu M S, et al. Effective high-throughput isolation of fully human antibodies targeting infectious pathogens. Nature Protocols, 2021, 16(7): 3639-3671.
doi: 10.1038/s41596-021-00554-w
pmid: 34035500
|
|
|
[58] |
Akagi S, Nakajima C, Tanaka Y, et al. Flow cytometry-based method for rapid and high-throughput screening of hybridoma cells secreting monoclonal antibody. Journal of Bioscience and Bioengineering, 2018, 125(4): 464-469.
doi: S1389-1723(17)30577-7
pmid: 29174537
|
|
|
[59] |
Xu Z Y, Walker S, Wise M C, et al. Induction of tier-2 neutralizing antibodies in mice with a DNA-encoded HIV envelope native like trimer. Nature Communications, 2022, 13(1): 1-18.
doi: 10.1038/s41467-021-27699-2
|
|
|
[60] |
Setliff I, Shiakolas A R, Pilewski K A, et al. High-throughput mapping of B cell receptor sequences to antigen specificity. Cell, 2019, 179(7): 1636-1646.e15.
doi: S0092-8674(19)31224-3
pmid: 31787378
|
|
|
[61] |
Shiakolas A R, Kramer K J, Wrapp D, et al. Cross-reactive coronavirus antibodies with diverse epitope specificities and Fc effector functions. Cell Reports Medicine, 2021, 2(6): 100313.
doi: 10.1016/j.xcrm.2021.100313
|
|
|
[62] |
Kramer K J, Johnson N V, Shiakolas A R, et al. Potent neutralization of SARS-CoV-2 variants of concern by an antibody with an uncommon genetic signature and structural mode of spike recognition. Cell Reports, 2021, 37(1): 109784.
doi: 10.1016/j.celrep.2021.109784
|
|
|
[63] |
Walker L M, Shiakolas A R, Venkat R, et al. High-throughput B cell epitope determination by next-generation sequencing. Frontiers in Immunology, 2022, 13: 855772.
doi: 10.3389/fimmu.2022.855772
|
|
|
[64] |
Hu T S, Chitnis N, Monos D, et al. Next-generation sequencing technologies: an overview. Human Immunology, 2021, 82(11): 801-811.
doi: 10.1016/j.humimm.2021.02.012
pmid: 33745759
|
|
|
[65] |
Sun C J, Zuo T, Wen Z Y. First clinical study of germline-targeting strategy: one step closer to a successful bnAb-based HIV vaccine. The Innovation, 2023, 4(1): 100374.
doi: 10.1016/j.xinn.2023.100374
|
|
|
[66] |
Burton D R. Advancing an HIV vaccine; advancing vaccinology. Nature Reviews Immunology, 2019, 19(2): 77-78.
doi: 10.1038/s41577-018-0103-6
pmid: 30560910
|
|
|
[67] |
Yan Q H, He P, Huang X H, et al. Germline IGHV3-53-encoded RBD-targeting neutralizing antibodies are commonly present in the antibody repertoires of COVID-19 patients. Emerging Microbes & Infections, 2021, 10(1): 1097-1111.
|
|
|
[68] |
Tan T J C, Yuan M, Kuzelka K, et al. Sequence signatures of two public antibody clonotypes that bind SARS-CoV-2 receptor binding domain. Nature Communications, 2021, 12(1): 1-10.
doi: 10.1038/s41467-020-20314-w
|
|
|
[69] |
Setliff I, McDonnell W J, Raju N, et al. Multi-donor longitudinal antibody repertoire sequencing reveals the existence of public antibody clonotypes in HIV-1 infection. Cell Host & Microbe, 2018, 23(6): 845-854.e6.
|
|
|
[70] |
Parola C, Neumeier D, Reddy S T. Integrating high-throughput screening and sequencing for monoclonal antibody discovery and engineering. Immunology, 2018, 153(1): 31-41.
doi: 10.1111/imm.12838
pmid: 28898398
|
|
|
[71] |
Sun Z H, Yan L X, Tang J S, et al. Brief introduction of current technologies in isolation of broadly neutralizing HIV-1 antibodies. Virus Research, 2018, 243: 75-82.
doi: S0168-1702(17)30572-5
pmid: 29051051
|
|
|
[72] |
Huang J H, Kang B, Ishida E, et al. Identification of a CD4-binding-site antibody to HIV that evolved near-pan neutralization breadth. Immunity, 2016, 45(5): 1108-1121.
doi: S1074-7613(16)30438-1
pmid: 27851912
|
|
|
[73] |
Sajadi M M, Dashti A, Rikhtegaran Tehrani Z, et al. Identification of near-pan-neutralizing antibodies against HIV-1 by deconvolution of plasma humoral responses. Cell, 2018, 173(7): 1783-1795.e14.
doi: S0092-8674(18)30393-3
pmid: 29731169
|
|
|
[74] |
Rudicell R S, Do Kwon Y, Ko S Y, et al. Enhanced potency of a broadly neutralizing HIV-1 antibody in vitro improves protection against lentiviral infection in vivo. Journal of Virology, 2014, 88(21): 12669-12682.
doi: 10.1128/JVI.02213-14
pmid: 25142607
|
|
|
[75] |
Zhou T Q, Lynch R, Chen L, et al. Structural repertoire of HIV-1-neutralizing antibodies targeting the CD 4 supersite in 14 donors. Cell, 2015, 161(6): 1280-1292.
doi: 10.1016/j.cell.2015.05.007
|
|
|
[76] |
Williams L D, Ofek G, Schätzle S, et al. Potent and broad HIV-neutralizing antibodies in memory B cells and plasma. Science Immunology, 2017, 2(7): eaal2200.
|
|
|
[77] |
Schoofs T, Barnes C O, Suh-Toma N, et al. Broad and potent neutralizing antibodies recognize the silent face of the HIV envelope. Immunity, 2019, 50(6): 1513-1529.e9.
doi: S1074-7613(19)30194-3
pmid: 31126879
|
|
|
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