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Review

B cell targeting by molecular adjuvants for enhanced immunogenicity

, & ORCID Icon
Pages 1023-1039 | Received 27 Jul 2020, Accepted 25 Nov 2020, Published online: 24 Dec 2020

References

  • Plotkin SA. Correlates of protection induced by vaccination. Clin Vaccine Immunol. 2010;17(7):1055–1065.
  • Liljeqvist S, Ståhl S. Production of recombinant subunit vaccines: protein immunogens, live delivery systems and nucleic acid vaccines. J Biotechnol. 1999;73(1):1–33.
  • Palumbo E, Fiaschi L, Brunelli B, et al. Antigen identification starting from the genome: a “reverse vaccinology” approach applied to MenB. Methods Mol Biol. 2012;799:361–403.
  • Serruto D, Bottomley MJ, Ram S, et al. The new multicomponent vaccine against meningococcal serogroup B, 4CMenB: immunological, functional and structural characterization of the antigens. Vaccine. 2012;30:B87–B97.
  • O’Ryan M, Stoddard J, Toneatto D, et al. A multi-component meningococcal serogroup B vaccine (4CMenB): the clinical development program. Drugs. 2014;74(1):15–30.
  • Plotkin SA. Vaccines: correlates of vaccine‐induced immunity. Clin Infect Dis. 2008;47(3):401–409.
  • Amanna IJ, Carlson NE, Slifka MK. Duration of humoral immunity to common viral and vaccine antigens. N Engl J Med. 2007;357(19):1903–1915.
  • McLeod B, Miura K, Scally SW, et al. Potent antibody lineage against malaria transmission elicited by human vaccination with Pfs25. Nat Commun. 2019;10(1):4328.
  • Scally SW, McLeod B, Bosch A, et al. Molecular definition of multiple sites of antibody inhibition of malaria transmission-blocking vaccine antigen Pfs25. Nat Commun. 2017;8(1):1568.
  • Oyen D, Torres JL, Wille-Reece U, et al. Structural basis for antibody recognition of the NANP repeats in plasmodium falciparum circumsporozoite protein. Proc Natl Acad Sci. 2017;114(48):E10438–E10445.
  • Murugan R, Scally SW, Costa G, et al. Evolution of protective human antibodies against Plasmodium falciparum circumsporozoite protein repeat motifs. Nat Med. 2020;26(7):1135–1145.
  • Kisalu NK, Idris AH, Weidle C, et al. A human monoclonal antibody prevents malaria infection by targeting a new site of vulnerability on the parasite. Nat Med. 2018;24(4):408–416.
  • Tan J, Sack BK, Oyen D, et al. A public antibody lineage that potently inhibits malaria infection through dual binding to the circumsporozoite protein. Nat Med. 2018;24(4):401–407.
  • Scally SW, Murugan R, Bosch A, et al. Rare PfCSP C-terminal antibodies induced by live sporozoite vaccination are ineffective against malaria infection. J Exp Med. 2018;215(1):63–75.
  • Thai E, Costa G, Weyrich A, et al. A high-affinity antibody against the CSP N-terminal domain lacks plasmodium falciparum inhibitory activity. J Exp Med. 2020;217(11):e20200061.
  • McLellan JS, Chen M, Joyce MG, et al. Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science. 2013;342(6158):592–598.
  • McLellan JS, Chen M, Leung S, et al. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science. 2013;340(6136):1113–1117.
  • Cai Y, Zhang J, Xiao T, et al. Distinct conformational states of SARS-CoV-2 spike protein. Science. 2020; eabd4251. 10.1126/science.abd4251.
  • de Taeye SW, Ozorowski G, Torrents de la Peña A, et al. Immunogenicity of stabilized HIV-1 envelope trimers with reduced exposure of non-neutralizing epitopes. Cell. 2015;163(7):1702–1715.
  • Do Kwon Y, Pancera M, Acharya P, et al. Crystal structure, conformational fixation and entry-related interactions of mature ligand-free HIV-1 Env. Nat Struct Mol Biol. 2015;22(7):522–531.
  • Rutten L, Lai Y-T, Blokland S, et al. A universal approach to optimize the folding and stability of prefusion-closed HIV-1 Envelope trimers. Cell Rep. 2018;23(2):584–595.
  • Torrents de la Peña A, Sanders RW. Stabilizing HIV-1 envelope glycoprotein trimers to induce neutralizing antibodies. Retrovirology. 2018;15(1):63.
  • Sanders RW, Derking R, Cupo A, et al. A next-generation cleaved, soluble HIV-1 Env trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies. PLoS Pathog. 2013;9(9):e1003618.
  • Wrapp D, Wang N, Corbett KS, et al. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science. 2020;367(6483):1260–1263.
  • Walls AC, Park Y-J, Tortorici MA, et al. Structure, function, and antigenicity of the SARS-CoV-2 Spike glycoprotein. Cell. 2020;181(2):e6.
  • Shang J, Ye G, Shi K, et al. Structural basis of receptor recognition by SARS-CoV-2. Nature. 2020;581(7807):221–224.
  • Joyce MG, Georgiev IS, Yang Y, et al. Soluble prefusion closed DS-SOSIP664-Env trimers of diverse HIV-1 strains. Cell Rep. 2017;21(10):2992–3002.
  • Steel J, Lowen AC, Wang TT, et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio. 2010;1(1):e00018–10.
  • Impagliazzo A, Milder F, Kuipers H, et al. A stable trimeric influenza hemagglutinin stem as a broadly protective immunogen. Science. 2015;349(6254):1301–1306.
  • Yassine HM, Boyington JC, McTamney PM, et al. Hemagglutinin-stem nanoparticles generate heterosubtypic influenza protection. Nat Med. 2015;21(9):1065–1070.
  • Jardine JG, Kulp DW, Havenar-Daughton C, et al. HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogen. Science. 2016;351(6280):1458–1463.
  • Havenar-Daughton C, Sarkar A, Kulp DW, et al. The human naive B cell repertoire contains distinct subclasses for a germline-targeting HIV-1 vaccine immunogen. Sci Transl Med. 2018;10(448):eaat0381.
  • Jardine J, Julien J-P, Menis S, et al. Rational HIV immunogen design to target specific germline B cell receptors. Science. 2013;340(6133):711–716.
  • Dietrich J, Andreasen LV, Andersen P, et al. Inducing dose sparing with inactivated polio virus formulated in adjuvant CAF01. PLoS One. 2014;9(6):e100879. Rodrigues MM, editor.
  • Lindenstrøm T, Agger EM, Korsholm KS, et al. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J Immunol. 2009;182(12):8047–8055.
  • Kasturi SP, Rasheed MAU, Havenar-Daughton C, et al. 3M-052, a synthetic TLR-7/8 agonist, induces durable HIV-1 envelope–specific plasma cells and humoral immunity in nonhuman primates. Sci Immunol. 2020;5(48):eabb1025.
  • Khurana S, Chearwae W, Castellino F, et al. Vaccines with MF59 adjuvant expand the antibody repertoire to target protective sites of pandemic avian H5N1 influenza virus. Sci Transl Med. 2010;2:15ra5-15ra5.
  • McKee AS, Munks MW, Marrack P. How do adjuvants work? Important considerations for new generation adjuvants. Immunity. 2007;27(5):687–690.
  • Coffman RL, Sher A, Seder RA. Vaccine adjuvants: putting innate immunity to work. Immunity. 2010;33(4):492–503.
  • Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science. 2010;327(5963):291–295.
  • Mosca F, Tritto E, Muzzi A, et al. Molecular and cellular signatures of human vaccine adjuvants. Proc Natl Acad Sci. 2008;105(30):10501–10506.
  • Mbow ML, De Gregorio E, Valiante NM, et al. New adjuvants for human vaccines. Curr Opin Immunol. 2010;22(3):411–416.
  • Gavin AL, Hoebe K, Duong B, et al. Adjuvant-enhanced antibody responses in the absence of Toll-like receptor signaling. Science. 2006;314(5807):1936–1938.
  • Knudsen NPH, Olsen A, Buonsanti C, et al. Different human vaccine adjuvants promote distinct antigen-independent immunological signatures tailored to different pathogens. Sci Rep. 2016;6(1):1–13.
  • Stoute JA, Slaoui M, Heppner DG, et al. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against plasmodium falciparum malaria. N Engl J Med. 1997;336(2):86–91.
  • Kester KE, Cummings JF, Ofori‐Anyinam O, et al. Randomized, double‐blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria‐naive adults: safety, efficacy, and immunologic associates of protection. J Infect Dis. 2009;200(3):337–346.
  • JDS A, Lunardelli VAS, Coirada FC, et al. Adjuvants: classification, modus operandi, and licensing. J Immunol Res. 2016;2016:1–16.
  • Petrovsky N. Comparative safety of vaccine adjuvants: a summary of current evidence and future needs. Drug Saf. 2015;38(11):1059–1074.
  • Del Giudice G, Rappuoli R, Didierlaurent AM. Correlates of adjuvanticity: A review on adjuvants in licensed vaccines. Semin Immunol. 2018;39:14–21.
  • Dolmetsch RE, Lewis RS, Goodnow CC, et al. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature. 1997;386(6627):855–858.
  • Hashimoto A, Okada H, Jiang A, et al. Involvement of guanosine triphosphatases and phospholipase C-γ2 in extracellular signal–regulated kinase, c-Jun NH2-terminal kinase, and p38 mitogen-activated protein kinase activation by the B cell antigen receptor. J Exp Med. 1998;188(7):1287–1295.
  • Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol. 1997;15(1):707–747.
  • Kouskoff V, Famiglietti S, Lacaud G, et al. Antigens varying in affinity for the B cell receptor induce differential B lymphocyte responses. J Exp Med. 1998;188(8):1453–1464.
  • Liu W, Meckel T, Tolar P, et al. Antigen affinity discrimination is an intrinsic function of the B cell receptor. J Exp Med. 2010;207(5):1095–1111.
  • Carter R, Fearon D. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science. 1992;256(5053):105–107.
  • Gasparrini F, Feest C, Bruckbauer A, et al. Nanoscale organization and dynamics of the siglec CD22 cooperate with the cytoskeleton in restraining BCR signalling. Embo J. 2016;35(3):258–280.
  • Nitschke L, Carsetti R, Ocker B, et al. CD22 is a negative regulator of B-cell receptor signalling. Curr Biol. 1997;7(2):133–143.
  • Giovannone N, Smith LK, Treanor B, et al. Galectin-glycan interactions as regulators of B cell immunity. Front Immunol. 2018;9:2839.
  • Wang TT, Maamary J, Tan GS, et al. Anti-HA glycoforms drive B cell affinity selection and determine influenza vaccine efficacy. Cell. 2015;162(1):160–169.
  • Petersone L, Edner NM, Ovcinnikovs V, et al. T cell/B cell collaboration and autoimmunity: an intimate relationship. Front Immunol. 2018;9:1941.
  • Kwak K, Akkaya M, Pierce SK. B cell signaling in context. Nat Immunol. 2019;20(8):963–969.
  • Benson MJ, Elgueta R, Noelle RJ. B cell survival: an unexpected mechanism of lymphocyte vitality. Immunol Cell Biol. 2008;86(6):485–486.
  • Mackay F, Schneider P, Rennert P, et al. BAFF AND APRIL: A Tutorial on B Cell Survival. Annu Rev Immunol. 2003;21(1):231–264.
  • Smulski CR, Eibel H. BAFF and BAFF-receptor in B cell selection and survival. Front Immunol. 2018;9:2285.
  • Wurster AL, Rodgers VL, White MF, et al. Interleukin-4-mediated protection of primary B cells from apoptosis through Stat6-dependent up-regulation of Bcl-xL. J Biol Chem. 2002;277(30):27169–27175.
  • Pulendran B, Ahmed R. Immunological mechanisms of vaccination. Nat Immunol. 2011;12(6):509–517.
  • Brynjolfsson SF, Persson Berg L, Olsen Ekerhult T, et al. Long-lived plasma cells in mice and men. Front Immunol. 2018;9:2673.
  • Slifka MK, Antia R, Whitmire JK, et al. Humoral immunity due to long-lived plasma cells. Immunity. 1998;8(3):363–372.
  • McHeyzer-Williams MG, Ahmed R. B cell memory and the long-lived plasma cell. Curr Opin Immunol. 1999;11(2):172–179.
  • Kurosaki T, Kometani K. Ise W. memory B cells. Nat Rev Immunol. 2015;15(3):149–159.
  • Ricklin D, Reis ES, Mastellos DC, et al. Complement component C3 - the “swiss army knife” of innate immunity and host defense. Immunol Rev. 2016;274:33–58.
  • Bergmann-Leitner ES, Leitner WW, Tsokos GC. Complement 3d: from molecular adjuvant to target of immune escape mechanisms. Clin Immunol. 2006;121(2):177–185.
  • Walport MJ. Complement: second of two parts. N Engl J Med. 2001;344:1140–1144.
  • Matsumoto AK, Kopicky-Burd J, Carter RH, et al. Intersection of the complement and immune systems: A signal transduction complex of the B lymphocyte-containing complement receptor type 2 and CD19. J Exp Med. 1991. 10.1084/jem.173.1.55
  • Bradbury LE, Kansas GS, Levy S, et al. The CD19/CD21 signal transducing complex of human B lymphocytes includes the target of antiproliferative antibody-1 and Leu-13 molecules. J Immunol. 1992;149:2841 LP– 2850.
  • Cooper NR, Moore MD, Nemerow GR. Immunobiology of CR2, the B lymphocyte receptor for Epstein-Barr virus and the C3d complement fragment. Annu Rev Immunol. 1988;6(1):85–113.
  • Ahearn JM, Fearon DT. Structure and function of the complement receptors, CR1 (CD35) and CR2 (CD21). Adv Immunol. 1989;46:183–219.
  • Hasegawa M, Fujimoto M, Poe JC, et al. CD19 can regulate B lymphocyte signal transduction independent of complement activation. J Immunol. 2001;167(6):3190–3200.
  • Fearon DT, Carter RH. The CD19/CR2/TAPA-1 complex of B lymphocytes: linking natural to acquired immunity. Annu Rev Immunol. 1995;13(1):127–149.
  • Cambier JC, Pleiman CM, Clark MR. Signal transduction by the B cell antigen receptor and its coreceptors. Annu Rev Immunol. 1994;12(1):457–486.
  • Dempsey PW, Allison MED, Akkaraju S, et al., C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science. 1996; 271(5247): 348–350.
  • Toapanta FR, Ross TM. Complement-mediated activation of the adaptive immune responses: role of C3d in linking the innate and adaptive Immunity. Immunol Res. 2006;36(1–3):197–210.
  • Bergmann-Leitner ES, Duncan EH, Leitner WW, et al. C3d-defined complement receptor-binding peptide p28 conjugated to circumsporozoite protein provides protection against plasmodium berghei. Vaccine. 2007;25(45):7732–7736.
  • Pompa-Mera EN, Arroyo-Matus P, Ocaña-Mondragón A, et al. Protective immunity against enteral stages of trichinella spiralis elicited in mice by live attenuated salmonella vaccine that secretes a 30-mer parasite epitope fused to the molecular adjuvant C3d-P28. Res Vet Sci. 2014;97(3):533–545.
  • Movsesyan N, Mkrtichyan M, Petrushina I, et al. DNA epitope vaccine containing complement component C3d enhances anti-amyloid-β antibody production and polarizes the immune response towards a Th2 phenotype. J Neuroimmunol. 2008;205(1–2):57–63.
  • Wang XL, Zhao XR, Yu M, et al. Gene conjugation of molecular adjuvant C3d3 to hCGβ increased the anti-hCGβ Th2 and humoral immune response in DNA immunization. J Gene Med. 2006;8(4):498–505.
  • Toapanta FR, Ross TM. Mouse strain-dependent differences in enhancement of immune responses by C3d. Vaccine. 2004;22:1773–1781.
  • Mitchell J. Induction of heterosubtypic immunity to influenza A virus using a DNA vaccine expressing hemagglutinin-C3d fusion proteins. Vaccine. 2003;21:902–914.
  • Green TD, Newton BR, Rota PA, et al. C3d enhancement of neutralizing antibodies to measles hemagglutinin. Vaccine. 2001;20(1–2):242–248.
  • Green TD, Montefiori DC, Ross TM. Enhancement of antibodies to the human immunodeficiency virus type 1 envelope by using the molecular adjuvant C3d. J Virol. 2003;77:2046–2055.
  • Suradhat S, Braun RP, Lewis PJ, et al. Fusion of C3d molecule with bovine rotavirus VP7 or bovine herpesvirus type 1 glycoprotein D inhibits immune responses following DNA immunization. Vet Immunol Immunopathol. 2001;83(1–2):79–92.
  • Bergmann-Leitner ES. C3d binding to the circumsporozoite protein carboxy-terminus deviates immunity against malaria. Int Immunol. 2005;17(3):245–255.
  • Gor D, Ding X, Li Q, et al. Genetic fusion of three tandem copies of murine C3d sequences to diphtheria toxin fragment B elicits a decreased fragment B-specific antibody response. Immunol Lett. 2006;102(1):38–49.
  • Bower JF, Ross TM. A minimum CR2 binding domain of C3d enhances immunity following vaccination. curr. top. complement. Boston, MA: Springer US; 2006. p. 249–264.
  • Dunn MD, Rossi SL, Carter DM, et al. Enhancement of anti-DIII antibodies by the C3d derivative P28 results in lower viral titers and augments protection in mice. Virol J. 2010;7:95.
  • Galvez-Romero G, Salas-Rojas M, Pompa-Mera EN, et al. Addition of C3d-P28 adjuvant to a rabies DNA vaccine encoding the G5 linear epitope enhances the humoral immune response and confers protection. Vaccine. 2018;36(2):292–298.
  • Zhang D, Xia Q, Wu J, et al. Construction and immunogenicity of DNA vaccines encoding fusion protein of murine complement C3d-p28 and GP5 gene of porcine reproductive and respiratory syndrome virus. Vaccine. 2011;29(4):629–635.
  • Weiss R, Gabler M, Jacobs T, et al. Differential effects of C3d on the immunogenicity of gene gun vaccines encoding Plasmodium falciparum and Plasmodium berghei MSP142. Vaccine. 2010;28(28):4515–4522.
  • Haas KM, Toapanta FR, Oliver JA, et al., Cutting edge: C3d functions as a molecular adjuvant in the absence of CD21/35 expression. J Immunol. 2004; 172(10): 5833–5837.
  • ÉS V, Faustman DL. Structural principles of tumor necrosis factor superfamily signaling. Sci Signal. 2018;11(511):eaao4910.
  • Aggarwal BB. Signalling pathways of the TNF superfamily: a double-edged sword. Nat Rev Immunol. 2003;3:745–756.
  • Gupta S, Termini JM, Kanagavelu S, et al. Design of vaccine adjuvants incorporating TNF superfamily ligands and TNF superfamily molecular mimics. Immunol Res. 2013;57:303–310.
  • Schneider P, MacKay F, Steiner V, et al. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J Exp Med. 1999;189(11):1747–1756.
  • Varfolomeev E, Kischkel F, Martin F, et al. APRIL-deficient mice have normal immune system development. Mol Cell Biol. 2004;24(3):997–1006.
  • Bossen C, Tardivel A, Willen L, et al. Mutation of the BAFF furin cleavage site impairs B-cell homeostasis and antibody responses. Eur J Immunol. 2011;41(3):787–797.
  • López‐Fraga M, Fernández R, Albar JP, et al. Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase. EMBO Rep. 2001;2(10):945–951.
  • Bossen C, Cachero TG, Tardivel A, et al. TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts. Blood. 2008;111(3):1004–1012.
  • Cachero TG, Schwartz IM, Qian F, et al. Formation of virus-like clusters is an intrinsic property of the tumor necrosis factor family member BAFF (B cell activating factor). Biochemistry. 2006;45(7):2006–2013.
  • Ingold K, Zumsteg A, Tardivel A, et al. Identification of proteoglycans as the APRIL-specific binding partners. J Exp Med. 2005;201(9):1375–1383.
  • Vincent FB, Saulep-Easton D, Figgett WA, et al. The BAFF/APRIL system: emerging functions beyond B cell biology and autoimmunity. Cytokine Growth Factor Rev. 2013;24(3):203–215.
  • Zhang L, Zheng S, Wu H, et al. Identification of BLyS (B lymphocyte stimulator), a non-myelin-associated protein, as a functional ligand for Nogo-66 receptor. J Neurosci. 2009;29(19):6348–6352.
  • Yan M, Brady JR, Chan B, et al. Identification of a novel receptor for B lymphocyte stimulator that is mutated in a mouse strain with severe B cell deficiency. Curr Biol. 2001;11(19):1547–1552.
  • Sasaki Y, Casola S, Kutok JL, et al. TNF family member B cell-activating factor (BAFF) receptor-dependent and -independent roles for BAFF in B cell physiology. J Immunol. 2004;173(4):2245–2252.
  • Sakurai D, Kanno Y, Hase H, et al. TACI attenuates antibody production costimulated by BAFF-R and CD40. Eur J Immunol. 2007;37(1):110–118.
  • Seshasayee D, Valdez P, Yan M, et al. Loss of TACI causes fatal lymphoproliferation and autoimmunity, establishing TACI as an inhibitory BLyS receptor. Immunity. 2003;18(2):279–288.
  • Tsuji S, Cortesão C, Bram RJ, et al. TACI deficiency impairs sustained Blimp-1 expression in B cells decreasing long-lived plasma cells in the bone marrow. Blood. 2011;118:5832–5839.
  • Tsuji S, Stein L, Kamada N, et al. TACI deficiency enhances antibody avidity and clearance of an intestinal pathogen. J Clin Invest. 2014;124(11):4857–4866.
  • Day ES, Cachero TG, Qian F, et al. Selectivity of BAFF/BLyS and APRIL for binding to the TNF family receptors BAFFR/BR3 and BCMA. Biochemistry. 2005;44(6):1919–1931.
  • Locksley RM, Killeen N, Lenardo MJ. The TNF and TNF receptor superfamilies. Cell. 2001;104(4):487–501.
  • Pietravalle F, Lecoanet-Henchoz S, Aubry J-P, et al. Cleavage of membrane-bound CD40 ligand is not required for inducing B cell proliferation and differentiation. Eur J Immunol. 1996;26:725–728.
  • Ma DY, Clark EA. The role of CD40 and CD154/CD40L in dendritic cells. Semin Immunol. 2009;21(5):265–272.
  • Plummer JR, McGettigan JP. Incorporating B cell activating factor (BAFF) into the membrane of rabies virus (RABV) particles improves the speed and magnitude of vaccine-induced antibody responses. PLoS Negl Trop Dis. 2019;13:e0007800.
  • Haley SL, Tzvetkov EP, Lytle AG, et al. APRIL:TACI axis is dispensable for the immune response to rabies vaccination. Antiviral Res. 2017;144:130–137.
  • Hong J-Y, Chen T-H, Chen Y-J, et al. Highly immunogenic influenza virus-like particles containing B-cell-activating factor (BAFF) for multi-subtype vaccine development. Antiviral Res. 2019;164:12–22.
  • Melchers M, Bontjer I, Tong T, et al. Targeting HIV-1 envelope glycoprotein trimers to B cells using APRIL improves antibody responses. Retrovirology. 2012;9:P300.
  • Gupta S, Clark ES, Termini JM, et al. DNA vaccine molecular adjuvants SP-D-BAFF and SP-D-APRIL enhance anti-gp120 immune response and increase HIV-1 neutralizing antibody titers. J Virol. 2015;89:4158–4169.
  • Valentine MA, Clark EA, Shu GL, et al. Antibody to a novel 95-kDa surface glycoprotein on human B cells induces calcium mobilization and B cell activation. J Immunol. 1988;140(12):4071–8.
  • Miyake K, Yamashita Y, Hitoshi Y, et al. Murine B cell proliferation and protection from apoptosis with an antibody against a 105-kD molecule: unresponsiveness of X-linked immunodeficient B cells. J Exp Med. 1994;180(4):1217–1224.
  • Chaplin JW, Chappell CP, Clark EA. Targeting antigens to CD180 rapidly induces antigen-specific IgG, affinity maturation, and immunological memory. J Exp Med. 2013;210:2135–2146.
  • Miyake K, Yamashita Y, Ogata M, et al. RP105, a novel B cell surface molecule implicated in B cell activation, is a member of the leucine-rich repeat protein family. J Immunol. 1995;154:3333–3340.
  • Roe K, Shu GL, Draves KE, et al., Targeting antigens to CD180 but not CD40 programs immature and mature B cell subsets to become efficient APCs. J Immunol. 2019; 203(7): 1715–1729.
  • Copeman SM. Experiences with the Schick test and active immunization against Diphtheria. Proc R Soc Med. 1922;15:41–43.
  • Olitzki, L. The antigenic properties of bacteria combined with antibodies. J Immunol. 1935; 29(6):453–465.
  • Wen Y, Mu L, Shi Y. Immunoregulatory functions of immune complexes in vaccine and therapy. EMBO Mol Med. 2016;8(10):1120–1133.
  • Terres G, Wolins W. Enhanced immunological sensitization of mice by the simultaneous injection of antigen and specific antiserum. J Immunol. 1961;86:361–8.
  • Regnault A, Lankar D, Lacabanne V, et al. Fcγ receptor–mediated induction of dendritic cell maturation and major histocompatibility complex class I–restricted antigen presentation after immune complex internalization. J Exp Med. 1999;189(2):371–380.
  • van Montfoort N, ’T Hoen P, Mangsbo S, et al. Fcγ receptor IIb strongly regulates Fcγ receptor-facilitated T cell activation by dendritic cells. J Immunol. 2012;189:92–101.
  • Schuurhuis DH, Ioan-Facsinay A, Nagelkerken B, et al. Antigen-antibody immune complexes empower dendritic cells to efficiently prime specific CD8 CTL responses in vivo. J Immunol. 2002;168(5):2240–2246.
  • Maamary J, Wang TT, Tan GS, et al. Increasing the breadth and potency of response to the seasonal influenza virus vaccine by immune complex immunization. Proc Natl Acad Sci. 2017;114:10172–10177.
  • Temming AR, Dekkers G, van de Bovenkamp FS, et al. Human DC-SIGN and CD23 do not interact with human IgG. Sci Rep. 2019;9(1):9995.
  • Kanagavelu S, Termini JM, Gupta S, et al. HIV-1 adenoviral vector vaccines expressing multi-trimeric BAFF and 4-1BBL enhance T cell mediated anti-viral immunity. PLoS One. 2014;9:e90100.
  • Darrah PA, Zeppa JJ, Maiello P, et al. Prevention of tuberculosis in macaques after intravenous BCG immunization. Nature. 2020;577:95–102.
  • Roques E, Girard A, Gagnon CA, et al. Antibody responses induced in mice immunized with recombinant adenovectors expressing chimeric proteins of various porcine pathogens. Vaccine. 2013;31(24):2698–2704.
  • Ross TM, Xu Y, Bright RA, et al. C3d enhancement of antibodies to hemagglutinin accelerates protection against influenza virus challenge. Nat Immunol. 2000;1(2):127–131.
  • Ross TM, Xu Y, Green TD, et al. Enhanced avidity maturation of antibody to human immunodeficiency virus Envelope: DNA vaccination with gp120–C3d fusion proteins. AIDS Res Hum Retroviruses. 2001;17(9):829–835.
  • Musa HH, Zhang WJ, Lv J, et al. The molecular adjuvant mC3d enhances the immunogenicity of FimA from type I fimbriae of Salmonella enterica serovar Enteritidis. J Microbiol Immunol Infect. 2014;47(1):57–62.
  • Al-Halifa S, Gauthier L, Arpin D, et al. Nanoparticle-based vaccines against respiratory viruses. Front Immunol. 2019;10:22.
  • Sliepen K, Ozorowski G, Burger JA, et al. Presenting native-like HIV-1 envelope trimers on ferritin nanoparticles improves their immunogenicity. Retrovirology. 2015;12:82.
  • He L, de Val N, Morris CD, et al. Presenting native-like trimeric HIV-1 antigens with self-assembling nanoparticles. Nat Commun. 2016;7(1):12041.
  • Bale JB, Gonen S, Liu Y, et al. Accurate design of megadalton-scale two-component icosahedral protein complexes. Science. 2016;353(6297):389–394.