Persistence of HIV-1 Env-Specific Plasmablast Lineages in Plasma Cells after Vaccination in Humans
Madhubanti Basu, Michael S Piepenbrink, Czestochowa Francois, Fritzlaine Roche, Bo Zheng, David A Spencer, Ann J Hessell, Christopher F Fucile, Alexander F Rosenberg, Catherine A Bunce, Jane Liesveld, Michael C Keefer, James J Kobie, Madhubanti Basu, Michael S Piepenbrink, Czestochowa Francois, Fritzlaine Roche, Bo Zheng, David A Spencer, Ann J Hessell, Christopher F Fucile, Alexander F Rosenberg, Catherine A Bunce, Jane Liesveld, Michael C Keefer, James J Kobie
Abstract
Induction of persistent HIV-1 Envelope (Env) specific antibody (Ab) is a primary goal of HIV vaccine strategies; however, it is unclear whether HIV Env immunization in humans induces bone marrow plasma cells, the presumed source of long-lived systemic Ab. To define the features of Env-specific plasma cells after vaccination, samples were obtained from HVTN 105, a phase I trial testing the same gp120 protein immunogen, AIDSVAX B/E, used in RV144, along with a DNA immunogen in various prime and boost strategies. Boosting regimens that included AIDSVAX B/E induced robust peripheral blood plasmablast responses. The Env-specific immunoglobulin repertoire of the plasmablasts is dominated by VH1 gene usage and targeting of the V3 region. Numerous plasmablast-derived immunoglobulin lineages persisted in the bone marrow >8 months after immunization, including in the CD138+ long-lived plasma cell compartment. These findings identify a cellular linkage for the development of sustained Env-specific Abs following vaccination in humans.
Trial registration: ClinicalTrials.gov NCT02207920.
Conflict of interest statement
DECLARATION OF INTERESTS The authors declare no competing interests.
Figures
References
- WHO . 2017. HIV/AIDS Data and Statistics.
- Excler J.L., Michael N.L. Lessons from HIV-1 vaccine efficacy trials. Curr. Opin. HIV AIDS. 2016;11:607–613.
- Rerks-Ngarm S., Pitisuttithum P., Nitayaphan S., Kaewkungwal J., Chiu J., Paris R., Premsri N., Namwat C., de Souza M., Adams E., MOPH-TAVEG Investigators Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 2009;361:2209–2220.
- Robb M.L., Rerks-Ngarm S., Nitayaphan S., Pitisuttithum P., Kaewkungwal J., Kunasol P., Khamboonruang C., Thongcharoen P., Morgan P., Benenson M. Risk behaviour and time as covariates for efficacy of the HIV vaccine regimen ALVAC-HIV (vCP1521) and AIDSVAX B/E: a post-hoc analysis of the Thai phase 3 efficacy trial RV 144. Lancet Infect. Dis. 2012;12:531–537.
- Haynes B.F., Gilbert P.B., McElrath M.J., Zolla-Pazner S., Tomaras G.D., Alam S.M., Evans D.T., Montefiori D.C., Karnasuta C., Sutthent R. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 2012;366:1275–1286.
- Karasavvas N., Billings E., Rao M., Williams C., Zolla-Pazner S., Bailer R.T., Koup R.A., Madnote S., Arworn D., Shen X., MOPH TAVEG Collaboration The Thai Phase III HIV Type 1 Vaccine trial (RV144) regimen induces antibodies that target conserved regions within the V2 loop of gp120. AIDS Res. Hum. Retroviruses. 2012;28:1444–1457.
- Zolla-Pazner S., deCamp A., Gilbert P.B., Williams C., Yates N.L., Williams W.T., Howington R., Fong Y., Morris D.E., Soderberg K.A. Vaccine-induced IgG antibodies to V1V2 regions of multiple HIV-1 subtypes correlate with decreased risk of HIV-1 infection. PLoS One. 2014;9:e87572.
- Zolla-Pazner S., deCamp A.C., Cardozo T., Karasavvas N., Gottardo R., Williams C., Morris D.E., Tomaras G., Rao M., Billings E. Analysis of V2 antibody responses induced in vaccinees in the ALVAC/AIDSVAX HIV-1 vaccine efficacy trial. PLoS One. 2013;8:e53629.
- Yates N.L., Liao H.X., Fong Y., deCamp A., Vandergrift N.A., Williams W.T., Alam S.M., Ferrari G., Yang Z.Y., Seaton K.E. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci. Transl. Med. 2014;6:228ra39.
- Chung A.W., Kumar M.P., Arnold K.B., Yu W.H., Schoen M.K., Dunphy L.J., Suscovich T.J., Frahm N., Linde C., Mahan A.E. Dissecting Polyclonal Vaccine-Induced Humoral Immunity against HIV Using Systems Serology. Cell. 2015;163:988–998.
- Tomaras G.D., Ferrari G., Shen X., Alam S.M., Liao H.X., Pollara J., Bonsignori M., Moody M.A., Fong Y., Chen X. Vaccine-induced plasma IgA specific for the C1 region of the HIV-1 envelope blocks binding and effector function of IgG. Proc. Natl. Acad. Sci. USA. 2013;110:9019–9024.
- Bonsignori M., Pollara J., Moody M.A., Alpert M.D., Chen X., Hwang K.K., Gilbert P.B., Huang Y., Gurley T.C., Kozink D.M. Antibody-dependent cellular cytotoxicity-mediating antibodies from an HIV-1 vaccine efficacy trial target multiple epitopes and preferentially use the VH1 gene family. J. Virol. 2012;86:11521–11532.
- Chung A.W., Ghebremichael M., Robinson H., Brown E., Choi I., Lane S., Dugast A.S., Schoen M.K., Rolland M., Suscovich T.J. Polyfunctional Fc-effector profiles mediated by IgG subclass selection distinguish RV144 and VAX003 vaccines. Sci. Transl. Med. 2014;6:228ra38.
- Barouch D.H., Stephenson K.E., Borducchi E.N., Smith K., Stanley K., McNally A.G., Liu J., Abbink P., Maxfield L.F., Seaman M.S. Protective efficacy of a global HIV-1 mosaic vaccine against heterologous SHIV challenges in rhesus monkeys. Cell. 2013;155:531–539.
- Barouch D.H., Alter G., Broge T., Linde C., Ackerman M.E., Brown E.P., Borducchi E.N., Smith K.M., Nkolola J.P., Liu J. Protective efficacy of adenovirus/protein vaccines against SIV challenges in rhesus monkeys. Science. 2015;349:320–324.
- Bradley T., Pollara J., Santra S., Vandergrift N., Pittala S., Bailey-Kellogg C., Shen X., Parks R., Goodman D., Eaton A. Pentavalent HIV-1 vaccine protects against simian-human immunodeficiency virus challenge. Nat. Commun. 2017;8:15711.
- Wrammert J., Smith K., Miller J., Langley W.A., Kokko K., Larsen C., Zheng N.Y., Mays I., Garman L., Helms C. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature. 2008;453:667–671.
- Halliley J.L., Kyu S., Kobie J.J., Walsh E.E., Falsey A.R., Randall T.D., Treanor J., Feng C., Sanz I., Lee F.E. Peak frequencies of circulating human influenza-specific antibody secreting cells correlate with serum antibody response after immunization. Vaccine. 2010;28:3582–3587.
- Kyu S.Y., Kobie J., Yang H., Zand M.S., Topham D.J., Quataert S.A., Sanz I., Lee F.E. Frequencies of human influenza-specific antibody secreting cells or plasmablasts post vaccination from fresh and frozen peripheral blood mononuclear cells. J. Immunol. Methods. 2009;340:42–47.
- Chu V.T., Berek C. The establishment of the plasma cell survival niche in the bone marrow. Immunol. Rev. 2013;251:177–188.
- Kometani K., Kurosaki T. Differentiation and maintenance of long-lived plasma cells. Curr. Opin. Immunol. 2015;33:64–69.
- McMillan R., Longmire R.L., Yelenosky R., Lang J.E., Heath V., Craddock C.G. Immunoglobulin synthesis by human lymphoid tissues: normal bone marrow as a major site of IgG production. J. Immunol. 1972;109:1386–1394.
- Weisel F.J., Zuccarino-Catania G.V., Chikina M., Shlomchik M.J. A Temporal Switch in the Germinal Center Determines Differential Output of Memory B and Plasma Cells. Immunity. 2016;44:116–130.
- Donius L.R., Cheng Y., Choi J., Sun Z.Y., Hanson M., Zhang M., Gierahn T.M., Marquez S., Uduman M., Kleinstein S.H. Generation of Long-Lived Bone Marrow Plasma Cells Secreting Antibodies Specific for the HIV-1 gp41 Membrane-Proximal External Region in the Absence of Polyreactivity. J. Virol. 2016;90:8875–8890.
- Halliley J.L., Tipton C.M., Liesveld J., Rosenberg A.F., Darce J., Gregoretti I.V., Popova L., Kaminiski D., Fucile C.F., Albizua I. Long-Lived Plasma Cells Are Contained within the CD19(-)CD38(hi)CD138(+) Subset in Human Bone Marrow. Immunity. 2015;43:132–145.
- Amanna I.J., Carlson N.E., Slifka M.K. Duration of humoral immunity to common viral and vaccine antigens. N. Engl. J. Med. 2007;357:1903–1915.
- Amanna I.J., Slifka M.K. Mechanisms that determine plasma cell lifespan and the duration of humoral immunity. Immunol. Rev. 2010;236:125–138.
- Montezuma-Rusca J.M., Moir S., Kardava L., Buckner C.M., Louie A., Kim L.J., Santich B.H., Wang W., Fankuchen O.R., Diaz G. Bone marrow plasma cells are a primary source of serum HIV-1-specific antibodies in chronically infected individuals. J. Immunol. 2015;194:2561–2568.
- Huang K.H., Bonsall D., Katzourakis A., Thomson E.C., Fidler S.J., Main J., Muir D., Weber J.N., Frater A.J., Phillips R.E. B-cell depletion reveals a role for antibodies in the control of chronic HIV-1 infection. Nat. Commun. 2010;1:102.
- Sundling C., Martinez P., Soldemo M., Spångberg M., Bengtsson K.L., Stertman L., Forsell M.N., Karlsson Hedestam G.B. Immunization of macaques with soluble HIV type 1 and influenza virus envelope glycoproteins results in a similarly rapid contraction of peripheral B-cell responses after boosting. J. Infect. Dis. 2013;207:426–431.
- Rouphael N.G., Morgan C., Li S.S., Jensen R., Sanchez B., Karuna S., Swann E., Sobieszczyk M.E., Frank I., Wilson G.J., HVTN 105 Protocol Team and the NIAID HIV Vaccine Trials Network DNA priming and gp120 boosting induces HIV-specific antibodies in a randomized clinical trial. J. Clin. Invest. 2019;129:4769–4785.
- González-García I., Ocaña E., Jiménez-Gómez G., Campos-Caro A., Brieva J.A. Immunization-induced perturbation of human blood plasma cell pool: progressive maturation, IL-6 responsiveness, and high PRDI-BF1/BLIMP1 expression are critical distinctions between antigen-specific and nonspecific plasma cells. J. Immunol. 2006;176:4042–4050.
- Gorny M.K., Wang X.H., Williams C., Volsky B., Revesz K., Witover B., Burda S., Urbanski M., Nyambi P., Krachmarov C. Preferential use of the VH5-51 gene segment by the human immune response to code for antibodies against the V3 domain of HIV-1. Mol. Immunol. 2009;46:917–926.
- Gorny M.K., Sampson J., Li H., Jiang X., Totrov M., Wang X.H., Williams C., O’Neal T., Volsky B., Li L. Human anti-V3 HIV-1 monoclonal antibodies encoded by the VH5-51/VL lambda genes define a conserved antigenic structure. PLoS One. 2011;6:e27780.
- Zhou T., Georgiev I., Wu X., Yang Z.Y., Dai K., Finzi A., Kwon Y.D., Scheid J.F., Shi W., Xu L. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science. 2010;329:811–817.
- West A.P., Jr., Diskin R., Nussenzweig M.C., Bjorkman P.J. Structural basis for germ-line gene usage of a potent class of antibodies targeting the CD4-binding site of HIV-1 gp120. Proc. Natl. Acad. Sci. USA. 2012;109:E2083–E2090.
- Easterhoff D., Moody M.A., Fera D., Cheng H., Ackerman M., Wiehe K., Saunders K.O., Pollara J., Vandergrift N., Parks R. Boosting of HIV envelope CD4 binding site antibodies with long variable heavy third complementarity determining region in the randomized double blind RV305 HIV-1 vaccine trial. PLoS Pathog. 2017;13:e1006182.
- Walker L.M., Phogat S.K., Chan-Hui P.Y., Wagner D., Phung P., Goss J.L., Wrin T., Simek M.D., Fling S., Mitcham J.L., Protocol G Principal Investigators Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science. 2009;326:285–289.
- Bonsignori M., Hwang K.K., Chen X., Tsao C.Y., Morris L., Gray E., Marshall D.J., Crump J.A., Kapiga S.H., Sam N.E. Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J. Virol. 2011;85:9998–10009.
- Zhou T., Lynch R.M., Chen L., Acharya P., Wu X., Doria-Rose N.A., Joyce M.G., Lingwood D., Soto C., Bailer R.T., NISC Comparative Sequencing Program Structural Repertoire of HIV-1-Neutralizing Antibodies Targeting the CD4 Supersite in 14 Donors. Cell. 2015;161:1280–1292.
- Walker L.M., Huber M., Doores K.J., Falkowska E., Pejchal R., Julien J.P., Wang S.K., Ramos A., Chan-Hui P.Y., Moyle M., Protocol G Principal Investigators Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature. 2011;477:466–470.
- Doria-Rose N.A., Schramm C.A., Gorman J., Moore P.L., Bhiman J.N., DeKosky B.J., Ernandes M.J., Georgiev I.S., Kim H.J., Pancera M., NISC Comparative Sequencing Program Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature. 2014;509:55–62.
- Vidarsson G., Dekkers G., Rispens T. IgG subclasses and allotypes: from structure to effector functions. Front. Immunol. 2014;5:520.
- Scherpenisse M., Mollers M., Schepp R.M., Meijer C.J., de Melker H.E., Berbers G.A., van der Klis F.R. Detection of systemic and mucosal HPV-specific IgG and IgA antibodies in adolescent girls one and two years after HPV vaccination. Hum. Vaccin. Immunother. 2013;9:314–321.
- Petäjä T., Pedersen C., Poder A., Strauss G., Catteau G., Thomas F., Lehtinen M., Descamps D. Long-term persistence of systemic and mucosal immune response to HPV-16/18 AS04-adjuvanted vaccine in preteen/adolescent girls and young women. Int. J. Cancer. 2011;129:2147–2157.
- Wagner D.K., Clements M.L., Reimer C.B., Snyder M., Nelson D.L., Murphy B.R. Analysis of immunoglobulin G antibody responses after administration of live and inactivated influenza A vaccine indicates that nasal wash immunoglobulin G is a transudate from serum. J. Clin. Microbiol. 1987;25:559–562.
- Liao H.X., Bonsignori M., Alam S.M., McLellan J.S., Tomaras G.D., Moody M.A., Kozink D.M., Hwang K.K., Chen X., Tsao C.Y. Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity. 2013;38:176–186.
- Montefiori D.C., Karnasuta C., Huang Y., Ahmed H., Gilbert P., de Souza M.S., McLinden R., Tovanabutra S., Laurence-Chenine A., Sanders-Buell E. Magnitude and breadth of the neutralizing antibody response in the RV144 and Vax003 HIV-1 vaccine efficacy trials. J. Infect. Dis. 2012;206:431–441.
- Balasubramanian P., Williams C., Shapiro M.B., Sinangil F., Higgins K., Nádas A., Totrov M., Kong X.P., Fiore-Gartland A.J., Haigwood N.L. Functional Antibody Response Against V1V2 and V3 of HIV gp120 in the VAX003 and VAX004 Vaccine Trials. Sci. Rep. 2018;8:542.
- Jiang X., Burke V., Totrov M., Williams C., Cardozo T., Gorny M.K., Zolla-Pazner S., Kong X.P. Conserved structural elements in the V3 crown of HIV-1 gp120. Nat. Struct. Mol. Biol. 2010;17:955–961.
- Gottardo R., Bailer R.T., Korber B.T., Gnanakaran S., Phillips J., Shen X., Tomaras G.D., Turk E., Imholte G., Eckler L. Plasma IgG to linear epitopes in the V2 and V3 regions of HIV-1 gp120 correlate with a reduced risk of infection in the RV144 vaccine efficacy trial. PLoS One. 2013;8:e75665.
- Zolla-Pazner S., Edlefsen P.T., Rolland M., Kong X.P., deCamp A., Gottardo R., Williams C., Tovanabutra S., Sharpe-Cohen S., Mullins J.I. Vaccine-induced Human Antibodies Specific for the Third Variable Region of HIV-1 gp120 Impose Immune Pressure on Infecting Viruses. EBioMedicine. 2014;1:37–45.
- Yu L., Guan Y. Immunologic Basis for Long HCDR3s in Broadly Neutralizing Antibodies Against HIV-1. Front. Immunol. 2014;5:250.
- Briney B.S., Willis J.R., Crowe J.E., Jr. Human peripheral blood antibodies with long HCDR3s are established primarily at original recombination using a limited subset of germline genes. PLoS One. 2012;7:e36750.
- Costa M.R., Pollara J., Edwards R.W., Seaman M.S., Gorny M.K., Montefiori D.C., Liao H.X., Ferrari G., Lu S., Wang S. Fc Receptor-Mediated Activities of Env-Specific Human Monoclonal Antibodies Generated from Volunteers Receiving the DNA Prime-Protein Boost HIV Vaccine DP6-001. J. Virol. 2016;90:10362–10378.
- Michaeli M., Tabibian-Keissar H., Schiby G., Shahaf G., Pickman Y., Hazanov L., Rosenblatt K., Dunn-Walters D.K., Barshack I., Mehr R. Immunoglobulin gene repertoire diversification and selection in the stomach - from gastritis to gastric lymphomas. Front. Immunol. 2014;5:264.
- Julakyan U.L., Biderman B.V., Gemdzhian E.G., Sudarikov A.B., Savchenko V.G. [Molecular analysis of immunoglobulin genes in the tumor B cells in splenic marginal zone lymphoma] Ter. Arkh. 2015;87:58–63.
- Bikos V., Darzentas N., Hadzidimitriou A., Davis Z., Hockley S., Traverse-Glehen A., Algara P., Santoro A., Gonzalez D., Mollejo M. Over 30% of patients with splenic marginal zone lymphoma express the same immunoglobulin heavy variable gene: ontogenetic implications. Leukemia. 2012;26:1638–1646.
- Pujanauski L.M., Janoff E.N., McCarter M.D., Pelanda R., Torres R.M. Mouse marginal zone B cells harbor specificities similar to human broadly neutralizing HIV antibodies. Proc. Natl. Acad. Sci. USA. 2013;110:1422–1427.
- Williams W.B., Han Q., Haynes B.F. Cross-reactivity of HIV vaccine responses and the microbiome. Curr. Opin. HIV AIDS. 2018;13:9–14.
- Williams W.B., Liao H.X., Moody M.A., Kepler T.B., Alam S.M., Gao F., Wiehe K., Trama A.M., Jones K., Zhang R. HIV-1 VACCINES. Diversion of HIV-1 vaccine-induced immunity by gp41-microbiota cross-reactive antibodies. Science. 2015;349:aab1253.
- Howell D.N., Andreotti P.E., Dawson J.R., Cresswell P. Natural killing target antigens as inducers of interferon: studies with an immunoselected, natural killing-resistant human T lymphoblastoid cell line. J. Immunol. 1985;134:971–976.
- Trkola A., Matthews J., Gordon C., Ketas T., Moore J.P. A cell line-based neutralization assay for primary human immunodeficiency virus type 1 isolates that use either the CCR5 or the CXCR4 coreceptor. J. Virol. 1999;73:8966–8974.
- Yagita M., Huang C.L., Umehara H., Matsuo Y., Tabata R., Miyake M., Konaka Y., Takatsuki K. A novel natural killer cell line (KHYG-1) from a patient with aggressive natural killer cell leukemia carrying a p53 point mutation. Leukemia. 2000;14:922–930.
- Kobie J.J., Alcena D.C., Zheng B., Bryk P., Mattiacio J.L., Brewer M., Labranche C., Young F.M., Dewhurst S., Montefiori D.C. 9G4 autoreactivity is increased in HIV-infected patients and correlates with HIV broadly neutralizing serum activity. PLoS One. 2012;7:e35356.
- Kobie J.J., Zheng B., Bryk P., Barnes M., Ritchlin C.T., Tabechian D.A., Anandarajah A.P., Looney R.J., Thiele R.G., Anolik J.H. Decreased influenza-specific B cell responses in rheumatoid arthritis patients treated with anti-tumor necrosis factor. Arthritis Res. Ther. 2011;13:R209.
- Nogales A., Piepenbrink M.S., Wang J., Ortega S., Basu M., Fucile C.F., Treanor J.J., Rosenberg A.F., Zand M.S., Keefer M.C. A Highly Potent and Broadly Neutralizing H1 Influenza-Specific Human Monoclonal Antibody. Sci. Rep. 2018;8:4374.
- Liao H.X., Levesque M.C., Nagel A., Dixon A., Zhang R., Walter E., Parks R., Whitesides J., Marshall D.J., Hwang K.K. High-throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J. Virol. Methods. 2009;158:171–179.
- Tiller T., Meffre E., Yurasov S., Tsuiji M., Nussenzweig M.C., Wardemann H. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods. 2008;329:112–124.
- Kobie J.J., Zheng B., Piepenbrink M.S., Hessell A.J., Haigwood N.L., Keefer M.C., Sanz I. Functional and Molecular Characteristics of Novel and Conserved Cross-Clade HIV Envelope Specific Human Monoclonal Antibodies. Monoclon. Antib. Immunodiagn. Immunother. 2015;34:65–72.
- Ackerman M.E., Moldt B., Wyatt R.T., Dugast A.S., McAndrew E., Tsoukas S., Jost S., Berger C.T., Sciaranghella G., Liu Q. A robust, high-throughput assay to determine the phagocytic activity of clinical antibody samples. J. Immunol. Methods. 2011;366:8–19.
- Alpert M.D., Heyer L.N., Williams D.E., Harvey J.D., Greenough T., Allhorn M., Evans D.T. A novel assay for antibody-dependent cell-mediated cytotoxicity against HIV-1- or SIV-infected cells reveals incomplete overlap with antibodies measured by neutralization and binding assays. J. Virol. 2012;86:12039–12052.
- Blay W.M., Kasprzyk T., Misher L., Richardson B.A., Haigwood N.L. Mutations in envelope gp120 can impact proteolytic processing of the gp160 precursor and thereby affect neutralization sensitivity of human immunodeficiency virus type 1 pseudoviruses. J. Virol. 2007;81:13037–13049.
- Wei X., Decker J.M., Wang S., Hui H., Kappes J.C., Wu X., Salazar-Gonzalez J.F., Salazar M.G., Kilby J.M., Saag M.S. Antibody neutralization and escape by HIV-1. Nature. 2003;422:307–312.
- Montefiori D.C. Measuring HIV neutralization in a luciferase reporter gene assay. Methods Mol. Biol. 2009;485:395–405.
- Khan S., Nakajima R., Jain A., de Assis R.R., Jasinskas A., Obiero J.M., Adenaiye O., Tai S., Hong F., Milton D.K. Analysis of Serologic Cross-Reactivity Between Common Human Coronaviruses and SARS-CoV-2 Using Coronavirus Antigen Microarray. bioRxiv. 2020 doi: 10.1101/2020.03.24.006544.
- Piepenbrink M.S., Nogales A., Basu M., Fucile F.F., Liesveld J.L., Keefer M.C., Rosenberg A.F., Martinez-Sobrido L., Kobie J.J. Broad and Protective Influenza B Virus Neuraminidase Antibodies in Humans after Vaccination and their Clonal Persistence as Plasma Cells. mBio. 2019 doi: 10.1128/mBio.00066-19. Published online March 12, 2019.
- Tipton C.M., Fucile C.F., Darce J., Chida A., Ichikawa T., Gregoretti I., Schieferl S., Hom J., Jenks S., Feldman R.J. Diversity, cellular origin and autoreactivity of antibody-secreting cell population expansions in acute systemic lupus erythematosus. Nat. Immunol. 2015;16:755–765.
- Aouinti S., Giudicelli V., Duroux P., Malouche D., Kossida S., Lefranc M.P. IMGT/StatClonotype for Pairwise Evaluation and Visualization of NGS IG and TR IMGT Clonotype (AA) Diversity or Expression from IMGT/HighV-QUEST. Front. Immunol. 2016;7:339.
- Felsenstein J. Department of Genome Sciences, University of Washington; 2005. PHYLIP (Phylogeny Inference Package) version 3.6.
- Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–2504.
Source: PubMed