Transcriptomic Analysis Reveals Sixteen Potential Genes Associated with the Successful Differentiation of Antibody-Secreting Cells through the Utilization of Unfolded Protein Response Mechanisms in Robust Responders to the Influenza Vaccine
Life sciences: Multidisciplinary, general & others
Author, co-author :
Tawfik, Ahmed
Kawaguchi, Takahisa
Takahashi, Meiko
Setoh, Kazuya
Yamaguchi, Izumi
Tabara, Yasuharu
Van Steen, Kristel ; Université de Liège - ULiège > Département d'électricité, électronique et informatique (Institut Montefiore) > Bioinformatique
Sakuntabhai, Anavaj
Matsuda, Fumihiko
Language :
English
Title :
Transcriptomic Analysis Reveals Sixteen Potential Genes Associated with the Successful Differentiation of Antibody-Secreting Cells through the Utilization of Unfolded Protein Response Mechanisms in Robust Responders to the Influenza Vaccine
Rothberg M.B. Haessler S.D. Brown R.B. Complications of viral influenza Am. J. Med. 2008 121 258 264 10.1016/j.amjmed.2007.10.040
Buchy P. Selim B. Who and when to vaccinate against influenza Int. J. Infect. Dis. 2020 93 375 387 10.1016/j.ijid.2020.02.040
Manzoli L. Schioppa F. Boccia A. Villari P. The efficacy of influenza vaccine for healthy children. A meta-analysis evaluating potential sources of variation in efficacy estimates including study quality Pediatr. Infect. Dis. J. 2007 26 97 106 10.1097/01.inf.0000253053.01151.bd
Jefferson T. Rivetti A. Harnden A. Di Pietrantonj C. Demicheli V. Vaccines for preventing influenza in health children Cochrane Database Syst. Rev. 2008 2 CD004879
Negri E. Colombo C. Giordano L. Groth L. Apolone G. Vecchia C.L. Influenza vaccine in health children: A meta-analysis Vaccine 2005 23 2851 2861 10.1016/j.vaccine.2004.11.053
Villari P. Manzoli L. Boccia A. Methodological quality of studies and patient age as major sources of variation in efficacy estimates of influenza vaccination in healthy adults: A meta-analysis Vaccine 2004 22 3475 3486 10.1016/j.vaccine.2004.01.068
Beyer W.E.P. Heterogeneity of case definitions used in vaccine effectiveness studies—And its impact on meta-analysis Vaccine 2006 24 6602 6604 10.1016/j.vaccine.2006.05.038
Jefferson T.O. Rivetti D. Di Pietrantonj C. Rivetti A. Demicheli V. Vaccines for preventing influenza in healthy adults Cochrane Database Syst. Rev. 2007 2 CD001269
Govaert T.M. Thijs C.T. Masurel N. Sprenger M.J. Dinant G.J. Knottnerus J.A. The efficacy of influenza vaccination in elderly individuals. A randomized doubleblind placebo-controlled trial JAMA 1994 272 1661 1665 10.1001/jama.1994.03520210045030
Chen J. Wang J. Zhang J. Ly H. Advances in development and application of influenza vaccines Front. Immunol. 2021 12 711997 10.3389/fimmu.2021.711997 34326849
Soema P.C. Kompier R. Amorij J.P. Kersten G.F. Current and next generation influenza vaccines: Formulation and production strategies Eur. J. Pharm. Biopharm. 2015 94 251 263 10.1016/j.ejpb.2015.05.023
Krammer F. Fouchier R.A. Eichelberger M.C. Webby R.J. Shaw-Saliba K. Wan H. Wilson P.C. Compans R.W. Skountzou I. Monto A.S. NAction! How can neuraminidase-based immunity contribute to better influenza virus vaccines? mBio 2018 9 e02332-17 10.1128/mBio.02332-17
Sangster M.Y. Nguyen P.Q. Topham D.J. Role of memory B cells in hemagglutinin-specific antibody production following human influenza A virus infection Pathogens 2019 8 167 10.3390/pathogens8040167 31569328
Hannoun C. Megas F. Piercy J. Immunogenicity and protective efficacy of influenza vaccination Virus Res. 2004 103 133 138 10.1016/j.virusres.2004.02.025
Ritchie M.E. Phipson B. Wu D.I. Hu Y. Law C.W. Shi W. Smyth G.K. limma powers differential expression analyses for RNA-sequencing and microarray studies Nucleic Acids Res. 2015 43 e47 10.1093/nar/gkv007
Chambers J.M. Freeny A.E. Heiberger R.M. Analysis of variance; designed experiments Statistical Models in S Routledge London, UK 2017 145 193
Wu T. Hu E. Xu S. Chen M. Guo P. Dai Z. Feng T. Zhou L. Tang W. Zhan L. et al. ClusterProfiler 4.0: A universal enrichment tool for interpreting omics data Innovation 2021 2 100141 10.1016/j.xinn.2021.100141
Szklarczyk D. Franceschini A. Wyder S. Forslund K. Heller D. Huerta-Cepas J. Simonovic S.M. Roth A. Santos A. Von Mering C. et al. STRING v10: Protein–protein interaction networks, integrated over the tree of life Nucleic Acids Res. 2015 43 D447 D452 10.1093/nar/gku1003
Cyster J.G. Allen C.D. B cell responses: Cell interaction dynamics and decisions Cell 2019 177 524 540 10.1016/j.cell.2019.03.016
Batista F.D. Harwood N.E. The who, how and where of antigen presentation to B cells Nat. Rev. Immunol. 2009 9 15 27 10.1038/nri2454
Cyster J.G. B cell follicles and antigen encounters of the third kind Nat. Immunol. 2010 11 989 996 10.1038/ni.1946
Leu C.M. Davis R.S. Gartland L.A. Fine W.D. Cooper M.D. FcRH1: An activation coreceptor on human B cells Blood 2005 105 1121 1126 10.1182/blood-2004-06-2344
Schwartz M.A. Kolhatkar N.S. Thouvenel C. Khim S. Rawlings D.J. CD4+ T cells and CD40 participate in selection and homeostasis of peripheral B cells J. Immunol. 2014 193 3492 3502 10.4049/jimmunol.1400798
Crotty S. T follicular helper cell biology: A decade of discovery and diseases Immunity 2019 50 1132 1148 10.1016/j.immuni.2019.04.011
Kerfoot S.M. Yaari G. Patel J.R. Johnson K.L. Gonzalez D.G. Kleinstein S.H. Haberman A.M. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone Immunity 2011 34 947 960 10.1016/j.immuni.2011.03.024 21636295
Mesin L. Ersching J. Victora G.D. Germinal center B cell dynamics Immunity 2016 45 471 482 10.1016/j.immuni.2016.09.001 27653600
Eisen H.N. Affinity enhancement of antibodies: How low-affinity antibodies produced early in immune responses are followed by high-affinity antibodies later and in memory B-cell responses Cancer Immunol. Res. 2014 2 381 392 10.1158/2326-6066.CIR-14-0029
Elsner R.A. Shlomchik M.J. Germinal center and extrafollicular B cell responses in vaccination, immunity, and autoimmunity Immunity 2020 53 1136 1150 10.1016/j.immuni.2020.11.006 33326765
Gitlin A.D. Shulman Z. Nussenzweig M.C. Clonal selection in the germinal centre by regulated proliferation and hypermutation Nature 2014 509 637 640 10.1038/nature13300 24805232
Tas J.M.J. Mesin L. Pasqual G. Targ S. Jacobsen J.T. Mano Y.M. Chen C.S. Weill J.-C. Reynaud C.-A. Browne E.P. et al. Visualizing antibody affinity maturation in germinal centers Science 2016 351 1048 1054 10.1126/science.aad3439
Lindhout E. Mevissen M.L.C.M. Kwekkeboom J. Tager J.M. De Groot C. Direct evidence that human follicular dendritic cells (FDC) rescue germinal centre B cells from death by apoptosis Clin. Exp. Immunol. 1993 91 330 336 10.1111/j.1365-2249.1993.tb05904.x
Chevrier S. Kratina T. Emslie D. Tarlinton D.M. Corcoran L.M. IL4 and IL21 cooperate to induce the high Bcl6 protein level required for germinal center formation Immunol. Cell Biol. 2017 95 925 932 10.1038/icb.2017.71
Shlomchik M.J. Luo W. Weisel F. Linking signaling and selection in the germinal center Immunol. Rev. 2019 288 49 63 10.1111/imr.12744
Shlomchik M.J. Weisel F. Germinal center selection and the development of memory B and plasma cells Immunol. Rev. 2012 247 52 63 10.1111/j.1600-065X.2012.01124.x
Radbruch A. Muehlinghaus G. Luger E.O. Inamine A. Smith K.G. Dörner T. Hiepe F. Competence and competition: The challenge of becoming a long-lived plasma cell Nat. Rev. Immunol. 2006 6 741 750 10.1038/nri1886
Slifka M.K. Matloubian M. Ahmed R. Bone marrow is a major site of long-term antibody production after acute viral infection J. Virol. 1995 69 1895 1902 10.1128/jvi.69.3.1895-1902.1995
Slifka M.K. Antia R. Whitmire J.K. Ahmed R. Humoral immunity due to long-lived plasma cells Immunity 1998 8 363 372 10.1016/S1074-7613(00)80541-5 9529153
Bonaud A. Lemos J.P. Espéli M. Balabanian K. Hematopoietic multipotent progenitors and plasma cells: Neighbors or roommates in the mouse bone marrow ecosystem? Front. Immunol. 2021 12 658535 10.3389/fimmu.2021.658535 33936091
Taillardet M. Haffar G. Mondière P. Asensio M.-J. Gheit H. Burdin N. Defrance T. Genestier L. The thymus-independent immunity conferred by a pneumococcal polysaccharide is mediated by long-lived plasma cells Blood J. Am. Soc. Hematol. 2009 114 4432 4440 10.1182/blood-2009-01-200014
Kometani K. Nakagawa R. Shinnakasu R. Kaji T. Rybouchkin A. Moriyama S. Furukawa K. Koseki H. Takemori T. Kurosaki T. Repression of the transcription factor Bach2 contributes to predisposition of IgG1 memory B cells toward plasma cell differentiation Immunity 2013 39 136 147 10.1016/j.immuni.2013.06.011 23850379
Inoue T. Kurosaki T. Memory B cells Nat. Rev. Immunol. 2015 15 149 159 10.1038/s41577-023-00897-3
Liu Q. Kriksunov I.A. Jiang H. Graeff R. Lin H. Lee H.C. Hao Q. Covalent and noncovalent intermediates of an NAD utilizing enzyme, human CD38 Chem. Biol. 2008 15 1068 1078 10.1016/j.chembiol.2008.08.007 18940667
Camponeschi A. Kläsener K. Sundell T. Lundqvist C. Manna P.T. Ayoubzadeh N. Sundqvist M. Thorarinsdottir K. Gatto M. Visentini M. et al. Human CD38 regulates B cell antigen receptor dynamic organization in normal and malignant B cells J. Exp. Med. 2022 219 e20220201 10.1084/jem.20220201 35819358
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. et al. Long-lived plasma cells are contained within the CD19− CD38hiCD138+ subset in human bone marrow Immunity 2015 43 132 145 10.1016/j.immuni.2015.06.016
Garimilla S. Nguyen D.C. Halliley J.L. Tipton C. Rosenberg A.F. Fucile C.F. Saney C.L. Kyu S. Kaminski D. Lee F.E.H. et al. Differential transcriptome and development of human peripheral plasma cell subsets JCI Insight 2019 4 e126732 10.1172/jci.insight.126732
McCarron M.J. Park P.W. Fooksman D.R. CD138 mediates selection of mature plasma cells by regulating their survival Blood J. Am. Soc. Hematol. 2017 129 2749 2759 10.1182/blood-2017-01-761643
Sowa S.T. Moilanen A. Biterova E. Saaranen M.J. Lehtiö L. Ruddock L.W. High-resolution Crystal Structure of Human pERp1, A Saposin-like Protein Involved in IgA, IgM and Integrin Maturation in the Endoplasmic Reticulum J. Mol. Biol. 2021 433 166826 10.1016/j.jmb.2021.166826
Shimizu Y. Meunier L. Hendershot L.M. pERp1 is significantly up-regulated during plasma cell differentiation and contributes to the oxidative folding of immunoglobulin Proc. Natl. Acad. Sci. USA 2009 106 17013 17018 10.1073/pnas.0811591106
Rosenbaum M. Andreani V. Kapoor T. Herp S. Flach H. Duchniewicz M. Grosschedl R. MZB1 is a GRP94 cochaperone that enables proper immunoglobulin heavy chain biosynthesis upon ER stress Genes Dev. 2014 28 1165 1178 10.1101/gad.240762.114
Andreani V. Ramamoorthy S. Pandey A. Lupar E. Nutt S.L. Lämmermann T. Grosschedl R. Cochaperone Mzb1 is a key effector of Blimp1 in plasma cell differentiation and β1-integrin function Proc. Natl. Acad. Sci. USA 2018 115 E9630 E9639 10.1073/pnas.1809739115 30257949
Hatzoglou A. Roussel J. Bourgeade M.-F. Rogier E. Madry C. Inoue J. Devergne O. Tsapis A. TNF receptor family member BCMA (B cell maturation) associates with TNF receptor-associated factor (TRAF) 1, TRAF2, and TRAF3 and activates NF-κB, elk-1, c-Jun N-terminal kinase, and p38 mitogen-activated protein kinase J. Immunol. 2000 165 1322 1330 10.4049/jimmunol.165.3.1322 10903733
Thompson J.S. Schneider P. Kalled S.L. Wang L. Lefevre E.A. Cachero T.G. MacKay F. Bixler S.A. Zafari M. Liu Z.-Y. et al. BAFF binds to the tumor necrosis factor receptor–like molecule B cell maturation antigen and is important for maintaining the peripheral B cell population J. Exp. Med. 2000 192 129 136 10.1084/jem.192.1.129 10880534
Salzer U. Jennings S. Grimbacher B. To switch or not to switch–the opposing roles of TACI in terminal B cell differentiation Eur. J. Immunol. 2007 37 17 20 10.1002/eji.200636914
O’Connor B.P. Raman V.S. Erickson L.D. Cook W.J. Weaver L.K. Ahonen C. Lin L.-L. Mantchev G.T. Bram R.J. Noelle R.J. BCMA is essential for the survival of long-lived bone marrow plasma cells J. Exp. Med. 2004 199 91 98 10.1084/jem.20031330
Hymowitz S.G. Patel D.R. Wallweber H.J. Runyon S. Yan M. Yin J. Shriver S.K. Gordon N.C. Pan B. Starovasnik M.A. et al. Structures of APRIL-receptor complexes: Like BCMA, TACI employs only a single cysteine-rich domain for high affinity ligand binding J. Biol. Chem. 2005 280 7218 7227 10.1074/jbc.M411714200
Bossen C. Schneider P. BAFF, APRIL and their receptors: Structure, function and signaling Seminars in Immunology Academic Press Cambridge, MA, USA 2006 Volume 18 263 275
Yu G. Boone T. Delaney J. Hawkins N. Kelley M. Ramakrishnan M. McCabe S. Qiu W.-R. Kornuc M. Xia X.-Z. et al. APRIL and TALL-1 and receptors BCMA and TACI: System for regulating humoral immunity Nat. Immunol. 2000 1 252 256 10.1038/79802
Wu Y. Bressette D. Carrell J.A. Kaufman T. Feng P. Taylor K. Gan Y. Cho Y.H. Garcia A.D. Gollatz E. et al. Tumor necrosis factor (TNF) receptor superfamily member TACI is a high affinity receptor for TNF family members APRIL and BLyS J. Biol. Chem. 2000 275 35478 35485 10.1074/jbc.M005224200
He B. Santamaria R. Xu W. Cols M. Chen K. Puga I. Shan M. Xiong H. Bussel J.B. Cerutti A. et al. The transmembrane activator TACI triggers immunoglobulin class switching by activating B cells through the adaptor MyD88 Nat. Immunol. 2010 11 836 845 10.1038/ni.1914 20676093
Strubin M. Newell J.W. Matthias P. OBF-1, a novel B cell-specific coactivator that stimulates immunoglobulin promoter activity through association with octamer-binding proteins Cell 1995 80 497 506 10.1016/0092-8674(95)90500-6 7859290
Luo Y. Roeder R.G. Cloning, functional characterization, and mechanism of action of the B-cell-specific transcriptional coactivator OCA-B Mol. Cell. Biol. 1995 15 4115 4124 10.1128/MCB.15.8.4115 7623806
Ren X. Siegel R. Kim U. Roeder R.G. Direct interactions of OCA-B and TFII-I regulate immunoglobulin heavy-chain gene transcription by facilitating enhancer-promoter communication Mol. Cell 2011 42 342 355 10.1016/j.molcel.2011.04.011
Karnowski A. Chevrier S. Belz G.T. Mount A. Emslie D. D’costa K. Tarlinton D.M. Kallies A. Corcoran L.M. B and T cells collaborate in antiviral responses via IL-6, IL-21, and transcriptional activator and coactivator, Oct2 and OBF-1 J. Exp. Med. 2012 209 2049 2064 10.1084/jem.20111504
Schubart D.B. Rolink A. Kosco-Vilbois M.H. Botteri F. Matthias P. B-cell-specif ic coactivator OBF-1/OCA-B/Bob1 required for immune response and germinal centre formation Nature 1996 383 538 542 10.1038/383538a0
Corcoran L.M. Hasbold J. Dietrich W. Hawkins E. Kallies A. Nutt S.L. Tarlinton D.M. Matthias P. Hodgkin P.D. Differential requirement for OBF-1 during antibody-secreting cell differentiation J. Exp. Med. 2005 201 1385 1396 10.1084/jem.20042325
Nutt S.L. Heavey B. Rolink A.G. Busslinger M. Commitment to the B-lymphoid lineage depends on the transcription factor Pax5 Nature 1999 401 556 562 10.1038/44076
Revilla-I-Domingo R. Bilic I. Vilagos B. Tagoh H. Ebert A. Tamir I.M. Smeenk L. Trupke J. Sommer A. Jaritz M. et al. The B-cell identity factor Pax5 regulates distinct transcriptional programmes in early and late B lymphopoiesis EMBO J. 2012 31 3130 3146 10.1038/emboj.2012.155
Schebesta A. McManus S. Salvagiotto G. Delogu A. Busslinger G.A. Busslinger M. Transcription factor Pax5 activates the chromatin of key genes involved in B cell signaling, adhesion, migration, and immune function Immunity 2007 27 49 63 10.1016/j.immuni.2007.05.019
Delogu A. Schebesta A. Sun Q. Aschenbrenner K. Perlot T. Busslinger M. Gene repression by Pax5 in B cells is essential for blood cell homeostasis and is reversed in plasma cells Immunity 2006 24 269 281 10.1016/j.immuni.2006.01.012 16546096
Hill L. Ebert A. Jaritz M. Wutz G. Nagasaka K. Tagoh H. Kostanova-Poliakova D. Schindler K. Sun Q. Bönelt P. et al. Wapl repression by Pax5 promotes V gene recombination by Igh loop extrusion Nature 2020 584 142 147 10.1038/s41586-020-2454-y
Max E.E. Wakatsuki Y. Neurath M.F. Strober W. The role of BSAP in immunoglobulin isotype switching and B-cell proliferation Mechanisms in B-Cell Neoplasia 1994 Springer Berlin/Heidelberg, Germany 1995 449 458
Falini B. Fizzotti M. Pucciarini A. Bigerna B. Marafioti T. Gambacorta M. Pacini R. Alunni C. Natali–Tanci L. Stein H. et al. A monoclonal antibody (MUM1p) detects expression of the MUM1/IRF4 protein in a subset of germinal center B cells, plasma cells, and activated T cells Blood J. Am. Soc. Hematol. 2000 95 2084 2092 10.1182/blood.V95.6.2084
Ochiai K. Maienschein-Cline M. Simonetti G. Chen J. Rosenthal R. Brink R. Chong A.S. Klein U. Dinner A.R. Sciammas R. et al. Transcriptional regulation of germinal center B and plasma cell fates by dynamical control of IRF4 Immunity 2013 38 918 929 10.1016/j.immuni.2013.04.009
Klein U. Casola S. Cattoretti G. Shen Q. Lia M. Mo T. Ludwig T. Rajewsky K. Dalla-Favera R. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination Nat. Immunol. 2006 7 773 782 10.1038/ni1357
Wang X. Li H. Chang X. The role and mechanism of TXNDC5 in diseases Eur. J. Med. Res. 2022 27 145 10.1186/s40001-022-00770-4
Pace P.E. Peskin A.V. Han M.H. Hampton M.B. Winterbourn C.C. Hyperoxidized peroxiredoxin 2 interacts with the protein disulfide-isomerase ERp46 Biochem. J. 2013 453 475 485 10.1042/BJ20130030 23713588
Murase R. Yamamoto A. Hirata Y. Oh-Hashi K. Expression analysis and functional characterization of thioredoxin domain-containing protein 11 Mol. Biol. Rep. 2022 49 10541 10556 10.1007/s11033-022-07932-x
Liu B. Li Z. Endoplasmic reticulum HSP90b1 (gp96, grp94) optimizes B-cell function via chaperoning integrin and TLR but not immunoglobulin Blood J. Am. Soc. Hematol. 2008 112 1223 1230 10.1182/blood-2008-03-143107
Preisendörfer S. Ishikawa Y. Hennen E. Winklmeier S. Schupp J.C. Knüppel L. Fernandez I.E. Binzenhöfer L. Flatley A. Juan-Guardela B.M. et al. FK506-binding protein 11 is a novel plasma cell-specific antibody folding catalyst with increased expression in idiopathic pulmonary fibrosis Cells 2022 11 1341 10.3390/cells11081341
Vinaik R. Kozlov G. Gehring K. Structure of the non-catalytic domain of the protein disulfide isomerase-related protein (PDIR) reveals function in protein binding PLoS ONE 2013 8 e62021 10.1371/journal.pone.0062021
Bortnov V. Annis D.S. Fogerty F.J. Barretto K.T. Turton K.B. Mosher D.F. Myeloid-derived growth factor is a resident endoplasmic reticulum protein J. Biol. Chem. 2018 293 13166 13175 10.1074/jbc.AC118.002052 29954947
Gaffen S.L. Structure and signalling in the IL-17 receptor family Nat. Rev. Immunol. 2009 9 556 567 10.1038/nri2586 19575028
Ferretti E. Ponzoni M. Doglioni C. Pistoia V. IL-17 superfamily cytokines modulate normal germinal center B cell migration J. Leucoc. Biol. 2016 100 913 918 10.1189/jlb.1VMR0216-096RR 27566830
Tavender T.J. Sheppard A.M. Bulleid N.J. Peroxiredoxin IV is an endoplasmic reticulum-localized enzyme forming oligomeric complexes in human cells Biochem. J. 2008 411 191 199 10.1042/BJ20071428 18052930
Zhu L. Yang K. Wang X.E. Wang X. Wang C.C. A novel reaction of peroxiredoxin 4 towards substrates in oxidative protein folding PLoS ONE 2014 9 e105529 10.1371/journal.pone.0105529
Jin D.Y. Chae H.Z. Rhee S.G. Jeang K.T. Regulatory role for a novel human thioredoxin peroxidase in NF-κB activation J. Biol. Chem. 1997 272 30952 30961 10.1074/jbc.272.49.30952
Acosta-Alvear D. Zhou Y. Blais A. Tsikitis M. Lents N.H. Arias C. Lennon C.J. Kluger Y. Dynlacht B.D. XBP1 controls diverse cell type-and condition-specific transcriptional regulatory networks Mol. Cell 2007 27 53 66 10.1016/j.molcel.2007.06.011
Liu Y. Adachi M. Zhao S. Hareyama M. Koong A.C. Luo D. A Rando T. Imai K. Shinomura Y. Preventing oxidative stress: A new role for XBP1 Cell Death Differ. 2009 16 847 857 10.1038/cdd.2009.14
Reimold A.M. Iwakoshi N.N. Manis J. Vallabhajosyula P. Szomolanyi-Tsuda E. Gravallese E.M. Friend D. Grusby M.J. Alt F. Glimcher L.H. Plasma cell differentiation requires the transcription factor XBP-1 Nature 2001 412 300 307 10.1038/35085509
Iwakoshi N.N. Lee A.H. Glimcher L.H. The X-box binding protein-1 transcription factor is required for plasma cell differentiation and the unfolded protein response Immunol. Rev. 2003 194 29 38 10.1034/j.1600-065X.2003.00057.x
Taubenheim N. Tarlinton D.M. Crawford S. Corcoran L.M. Hodgkin P.D. Nutt S.L. High rate of antibody secretion is not integral to plasma cell differentiation as revealed by XBP-1 deficiency J. Immunol. 2012 189 3328 3338 10.4049/jimmunol.1201042
Kaufman R.J. Scheuner D. Schröder M. Shen X. Lee K. Liu C.Y. Arnold S.M. The unfolded protein response in nutrient sensing and differentiation Nat. Rev. Mol. Cell Biol. 2002 3 411 421 10.1038/nrm829 12042763
Lu Y. Welsh J.P. Swartz J.R. Production and stabilization of the trimeric influenza hemagglutinin stem domain for potentially broadly protective influenza vaccines Proc. Natl. Acad. Sci. USA 2014 111 125 130 10.1073/pnas.1308701110
Eichelberger M.C. Monto A.S. Neuraminidase, the forgotten surface antigen, emerges as an influenza vaccine target for broadened protection J. Infect. Dis. 2019 219 (Suppl. S1) S75 S80 10.1093/infdis/jiz017 30715357
Mezhenskaya D. Isakova-Sivak I. Rudenko L. M2e-based universal influenza vaccines: A historical overview and new approaches to development J. Biomed. Sci. 2019 26 1 15 10.1186/s12929-019-0572-3
Pengo N. Scolari M. Oliva L. Milan E. Mainoldi F. Raimondi A. Fagioli C. Merlini A. Mariani E. Pasqualetto E. et al. Plasma cells require autophagy for sustainable immunoglobulin production Nat. Immunol. 2013 14 298 305 10.1038/ni.2524
Cassese G. Arce S. Hauser A.E. Lehnert K. Moewes B. Mostarac M. Muehlinghaus G. Szyska M. Radbruch A. Manz R.A. Plasma cell survival is mediated by synergistic effects of cytokines and adhesion-dependent signals J. Immunol. 2003 171 1684 1690 10.4049/jimmunol.171.4.1684
Kawano M.M. Mihara K. Huang N. Tsujimoto T. Kuramoto A. Differentiation of early plasma cells on bone marrow stromal cells requires interleukin-6 for escaping from apoptosis Blood 1995 85 487 494 10.1182/blood.V85.2.487.487
Belnoue E. Pihlgren M. McGaha T.L. Tougne C. Rochat A.-F. Bossen C. Schneider P. Huard B. Lambert P.-H. Siegrist C.-A. APRIL is critical for plasmablast survival in the bone marrow and poorly expressed by early-life bone marrow stromal cells Blood J. Am. Soc. Hematol. 2008 111 2755 2764 10.1182/blood-2007-09-110858
Hargreaves D.C. Hyman P.L. Lu T.T. Ngo V.N. Bidgol A. Suzuki G. Zou Y.-R. Littman D.R. Cyster J.G. A coordinated change in chemokine responsiveness guides plasma cell movements J. Exp. Med. 2001 194 45 56 10.1084/jem.194.1.45 11435471
Wols H.A.M. Underhill G.H. Kansas G.S. Witte P.L. The role of bone marrow-derived stromal cells in the maintenance of plasma cell longevity J. Immunol. 2002 169 4213 4221 10.4049/jimmunol.169.8.4213 12370351
Rozanski C.H. Utley A. Carlson L.M. Farren M.R. Murray M. Russell L.M. Nair J.R. Yang Z. Brady W. Garrett-Sinha L.A. et al. CD28 promotes plasma cell survival, sustained antibody responses, and BLIMP-1 upregulation through its distal PYAP proline motif J. Immunol. 2015 194 4717 4728 10.4049/jimmunol.1402260 25833397
Chevrier S. Genton C. Kallies A. Karnowski A. Otten L.A. Malissen B. Malissen M. Botto M. Corcoran L.M. Nutt S.L. et al. CD93 is required for maintenance of antibody secretion and persistence of plasma cells in the bone marrow niche Proc. Natl. Acad. Sci. USA 2009 106 3895 3900 10.1073/pnas.0809736106 19228948
Liu G.J. Jaritz M. Wöhner M. Agerer B. Bergthaler A. Malin S.G. Busslinger M. Repression of the B cell identity factor Pax5 is not required for plasma cell development J. Exp. Med. 2020 217 e20200147 10.1084/jem.20200147
Nakaya H.I. Wrammert J. Lee E.K. Racioppi L. Marie-Kunze S. Haining W.N. Means A.R. Kasturi S.P. Khan N. Li G.-M. et al. Systems biology of vaccination for seasonal influenza in humans Nat. Immunol. 2011 12 786 795 10.1038/ni.2067
