Effective antigen delivery via dual entrapment in erythrocytes and autologous plasma beads

References

• Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol Cell Biol. 2004;82:488–496.
   PubMed Web of Science ®Google Scholar
• Caputo A, Sparnacci K, Ensoli B, et al. Functional polymeric nano/microparticles for surface adsorption and delivery of protein and DNA vaccines. CDD. 2008;5:230–242.
   PubMedGoogle Scholar
• García A, De Sanctis JB. An overview of adjuvant formulations and delivery systems. APMIS. 2014;122:257–267.
   PubMed Web of Science ®Google Scholar
• Reed SG, Bertholet S, Coler RN, et al. New horizons in adjuvants for vaccine development. Trends Immunol. 2009;30:23–32.
   PubMed Web of Science ®Google Scholar
• Oyewumi MO, Kumar A, Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert Rev Vaccines. 2010;9:1095–1107.
   PubMed Web of Science ®Google Scholar
• Schijns VE. Immunological concepts of vaccine adjuvant activity. Curr Opin Immunol. 2000;12:456–463.
   PubMed Web of Science ®Google Scholar
• Bungener L, Geeraedts F, ter Veer W, et al. Alum boosts TH2-type antibody responses to whole-inactivated virus influenza vaccine in mice but does not confer superior protection. Vaccine. 2008;26:2350–2359.
   PubMed Web of Science ®Google Scholar
• Men Y, Gander B, Merkle HP, et al. Induction of sustained and elevated immune responses to weakly immunogenic synthetic malarial peptides by encapsulation in biodegradable polymer microspheres. Vaccine. 1996;14:1442–1450.
   PubMed Web of Science ®Google Scholar
• Bolhassani A, Safaiyan S, Rafati S. Improvement of different vaccine delivery systems for cancer therapy. Mol Cancer. 2011;10:3.
   PubMed Web of Science ®Google Scholar
• Ihler GM, Glew RH, Schnure FW. Enzyme loading of erythrocytes. Proc Natl Acad Sci USA. 1973;70:2663–2666.
   PubMed Web of Science ®Google Scholar
• DeLoach JR, Harris RL, Ihler GM. An erythrocyte encapsulator dialyzer used in preparing large quantities of erythrocyte ghosts and encapsulation of a pesticide in erythrocyte ghosts. Anal Biochem. 1980;102:220–227.
   PubMed Web of Science ®Google Scholar
• Sprandel U, Lanz DJ, von HW. Magnetically responsive erythrocyte ghosts. Meth Enzymol. 1987;149:301–312.
   PubMed Web of Science ®Google Scholar
• Murray AM, Pearson IFS, Fairbanks LD, et al. The mouse immune response to carrier erythrocyte entrapped antigens. Vaccine. 2006;24:6129–6139.
   PubMed Web of Science ®Google Scholar
• Hamidi M, Zarei N, Zarrin AH, et al. Preparation and in vitro characterization of carrier erythrocytes for vaccine delivery. Int J Pharm. 2007;338:70–78.
   PubMed Web of Science ®Google Scholar
• Godfrin Y, Horand F, Franco R, et al. International seminar on the red blood cells as vehicles for drugs. Expert Opin Biol Ther. 2012;12:127–133.
   PubMed Web of Science ®Google Scholar
• Cremel M, Guérin N, Horand F, et al. Red blood cells as innovative antigen carrier to induce specific immune tolerance. Int J Pharm. 2013;443:39–49.
   PubMed Web of Science ®Google Scholar
• Magnani M, Chiarantini L, Vittoria E, et al. Red blood cells as an antigen-delivery system. Biotechnol Appl Biochem. 1992;16:188–194.
   PubMed Web of Science ®Google Scholar
• Wang HJ, Di L, Ren QS, et al. Applications and degradation of proteins used as tissue engineering materials. Materials. 2009;2:613–635.
   Web of Science ®Google Scholar
• Malafaya PB, Silva GA, Reis RL. Natural-origin polymers as carriers and scaffolds for biomolecules and cell delivery in tissue engineering applications. Adv Drug Deliv Rev. 2007;59:207–233.
   PubMed Web of Science ®Google Scholar
• Breen A, O’Brien T, Pandit A. Fibrin as a delivery system for therapeutic drugs and biomolecules. Tissue Eng Part B Rev. 2009;15:201–214.
   PubMed Web of Science ®Google Scholar
• Praveen G, Sreerekha PR, Menon D, et al. Fibrin nanoconstructs: a novel processing method and their use as controlled delivery agents. Nanotechnology. 2012;23:95102.
   PubMed Web of Science ®Google Scholar
• Ahmad E, Zia Q, Fatima MT, et al. Vaccine potential of plasma bead-based dual antigen delivery system against experimental murine candidiasis. Int J Biol Macromol. 2015;81:100–111.
   PubMed Web of Science ®Google Scholar
• Ahmad E, Fatima MT, Hoque M, et al. Fibrin matrices: the versatile therapeutic delivery systems. Int J Biol Macromol. 2015;81:121–136.
   PubMed Web of Science ®Google Scholar
• Saldanha J, Minor P. Detection of human parvovirus B19 DNA in plasma pools and blood products derived from these pools: implications for efficiency and consistency of removal of B19 DNA during manufacture. Br J Haematol. 1996;93:714–9.
   PubMed Web of Science ®Google Scholar
• Jackson MR. Fibrin sealants in surgical practice: an overview. Am J Surg. 2001;182:1S–7S.
   PubMed Web of Science ®Google Scholar
• Ho HO, Hsiao CC, Sokoloski TD, et al. Fibrin-based drug delivery systems III: the evaluation of the release of macromolecules from microbeads. J Control Release. 1995;34:65–70.
   Web of Science ®Google Scholar
• Chung TW, Yang MC, Tsai WJ. A fibrin encapsulated liposomes-in-chitosan matrix (FLCM) for delivering water-soluble drugs: influences of the surface properties of liposomes and the crosslinked fibrin network. Int J Pharm. 2006;311:122–129.
   PubMed Web of Science ®Google Scholar
• Dare EV, Griffith M, Poitras P, et al. Genipin cross-linked fibrin hydrogels for in vitro human articular cartilage tissue-engineered regeneration. Cells Tissues Organs (Print). 2009;190:313–325.
   PubMed Web of Science ®Google Scholar
• Meyenburg S, Lilie H, Panzner S, et al. Fibrin encapsulated liposomes as protein delivery system Studies on the in vitro release behavior. J Control Release. 2000;69:159–168.
   PubMed Web of Science ®Google Scholar
• Ahmad E, Fatima MT, Owais MSM. Beaded plasma clot: a potent sustained-release, drug-delivery system. Ther Deliv. 2011;2:573–583.
   PubMedGoogle Scholar
• Ahmad E, Fatima MT, Saleemuddin M, et al. Plasma beads loaded with Candida albicans cytosolic proteins impart protection against the fungal infection in BALB/c mice. Vaccine. 2012;30:6851–6858.
   PubMed Web of Science ®Google Scholar
• Deloach J, Ihler G. A dialysis procedure for loading erythrocytes with enzymes and lipids. Biochim Biophys Acta. 1977;496:136–145.
   PubMed Web of Science ®Google Scholar
• Reddy VA, Johnson RS, Biemann K, et al. Characterization of the glycosylation sites in yeast external invertase. I. N-linked oligosaccharide content of the individual sequons. J Biol Chem. 1988;263:6978–6985.
   PubMed Web of Science ®Google Scholar
• Bernfeld P. Amylases, α and β. Methods Enzymol. 1955;1:149–158.
   Web of Science ®Google Scholar
• Whelan D, Caplice NM, Clover AJP. Fibrin as a delivery system in wound healing tissue engineering applications. J Control Release. 2014;196:1–8.
   PubMed Web of Science ®Google Scholar
• Kim BS, Shkembi FLJ. In vitro and in vivo evaluation of commercially available fibrin gel as a carrier of alendronate for bone tissue engineering. Biomed Res Int. 2017;2017:6434169.
   Web of Science ®Google Scholar
• Pierigè F, Bigini N, Rossi LMM. Reengineering red blood cells for cellular therapeutics and diagnostics. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2017; doi: 10.1002/wnan.1454. [Epub ahead of print].
   Google Scholar
• Fatima MT, Ahmad ESM. Entrapment in plasma microparticles: a promising strategy for antigen delivery. J Biomed Mater Res. 2014;102:1244–1254.
   Web of Science ®Google Scholar
• Polvani C, Gasparini A, Benatti U, et al. Murine red blood cells as efficient carriers of three bacterial antigens for the production of specific and neutralizing antibodies. Biotechnol Appl Biochem. 1991;14:347–356.
   PubMed Web of Science ®Google Scholar
• Chiarantini L, Argnani R, Zucchini S, et al. Red blood cells as delivery system for recombinant HSV-1 glycoprotein B: immunogenicity and protection in mice. Vaccine. 1997;15:276–280.
   PubMed Web of Science ®Google Scholar
• Dominici S, Laguardia ME, Serafini G, et al. Red blood cell-mediated delivery of recombinant HIV-1 Tat protein in mice induces anti-Tat neutralizing antibodies and CTL. Vaccine. 2003;21:2082–2090.
   PubMed Web of Science ®Google Scholar
• Banz A, Cremel M, Mouvant A, et al. Tumor growth control using red blood cells as the antigen delivery system and poly(I:C). J Immunother. 2012;35:409–417.
   PubMed Web of Science ®Google Scholar
• Gautam S, Barna B, Chiang T, et al. Use of resealed erythrocytes as delivery system for C-reactive protein (CRP) to generate macrophage-mediated tumoricidal activity. J Biol Response Mod. 1987;6:346–354.
   PubMedGoogle Scholar
• Banz A, Cremel M, Rembert A, et al. In situ targeting of dendritic cells by antigen-loaded red blood cells: a novel approach to cancer immunotherapy. Vaccine. 2010;28:2965–2972.
   PubMed Web of Science ®Google Scholar
• Melnick LM, Turner BG, Puma P, et al. Characterization of a nonglycosylated single chain urinary plasminogen activator secreted from yeast. J Biol Chem. 1990;265:801–807.
   PubMed Web of Science ®Google Scholar
• Romanos M. Advances in the use of Pichia pastoris for high-level gene expression. Curr Opin Biotechnol. 1995;6:527–533.
   Web of Science ®Google Scholar
• De Flora a, Benatti U, Guida L, et al. Encapsulation of adriamycin in human erythrocytes. Proc Natl Acad Sci USA. 1986;83:7029–7033.
   PubMed Web of Science ®Google Scholar
• Hamidi M, Zarrin AH, Foroozesh M, et al. Preparation and in vitro evaluation of carrier erythrocytes for RES-targeted delivery of interferon-alpha 2b. Int J Pharm. 2007;341:125–133.
   PubMed Web of Science ®Google Scholar
• Bax BE, Bain MD, Fairbanks LD, et al. In vitro and in vivo studies with human carrier erythrocytes loaded with polyethylene glycol-conjugated and native adenosine deaminase. Br J Haematol. 2000;109:549–554.
   PubMed Web of Science ®Google Scholar
• Hamidi M, Tajerzadeh H, Dehpour a. R, et al. In vitro characterization of human intact erythrocytes loaded by enalaprilat. Drug Deliv. 2001;8:223–230.
   PubMed Web of Science ®Google Scholar
• Hamidi M, Tajerzadeh H. Carrier erythrocytes: an overview. Drug Deliv. 2003;10:9–20.
   PubMed Web of Science ®Google Scholar
• Talwar N, Jain NK. Erythrocyte based delivery system of primaquine: in vitro characterization. J Microencapsul. 1992;9:357–364.
   PubMed Web of Science ®Google Scholar
• Chiarantini L, Matteucci D, Pistello M, et al. AIDS vaccination studies using an ex vivo feline immunodeficiency virus model: homologous erythrocytes as a delivery system for preferential immunisation with putative protective antigens. Clin Diagn Lab Immunol. 1998;5:235–241.
   PubMedGoogle Scholar
• Kovacsovics-Bankowski M, Clark K, Benacerraf B, et al. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc Natl Acad Sci USA. 1993;90:4942–4946.
   PubMed Web of Science ®Google Scholar
• Magnani M, Rossi L, Fraternale A, et al. Erythrocyte-mediated delivery of drugs, peptides and modified oligonucleotides. Gene Ther. 2002;9:749–751.
   PubMed Web of Science ®Google Scholar
• Cohen SS, Li C, Ding L, et al. Pronounced acute immunosuppression in vivo mediated by HIV Tat challenge. Proc Natl Acad Sci USA. 1999;96:10842–10847.
   PubMed Web of Science ®Google Scholar
• Moingeon P. Strategies for designing vaccines eliciting Th1 responses in humans. J Biotechnol. 2002;98:189–198.
   PubMed Web of Science ®Google Scholar
• Broere F, Apasov SG, Sitkovsky MV, et al. T cell subsets and T cell-mediated immunity. In: Nijkamp FP, Parnham JM, editors. Principles of immunopharmacology. Basel (Switzerland): Birkha ¨user Basel; 2011. p. 15–27. Available from: http://link.springer.com/10.1007/978-3-0346-0136-8%5Cn http://www.ncbi.nlm.nih.gov/pubmed/8717522%5Cn http://link.springer.com/10.1007/978-3-0346-0136-8_2
   Google Scholar
• Constant SL, Bottomly K. Induction of Th1 and Th2 CD4+ T cell responses: the alternative approaches. Annu Rev Immunol. 1997;15:297–322.
   PubMed Web of Science ®Google Scholar
• Rothoeft T, Gonschorek A, Bartz H, et al. Antigen dose, type of antigen-presenting cell and time of differentiation contribute to the T helper 1/T helper 2 polarization of naive T cells. Immunology. 2003;110:430–439.
   PubMed Web of Science ®Google Scholar
• Bancroft AJ, Else KJ, Grencis RK. Low-level infection with Trichuris muris significantly affects the polarization of the CD4 response. Eur J Immunol. 1994;24:3113–3118.
   PubMed Web of Science ®Google Scholar
• Sarzotti M, Robbins DS, Hoffman PM, et al. Induction of protective CTL responses in newborn mice by a murine retrovirus. Science. 1996;271:1726–1728.
   PubMed Web of Science ®Google Scholar
• Wang LF, Lin JY, Hsieh KH, et al. Epicutaneous exposure of protein antigen induces a predominant Th2-like response with high IgE production in mice. J Immunol. 1996;156:4077–4082.
   PubMed Web of Science ®Google Scholar
• Hayglass KT, Naides SJ, Scott CF, et al. T cell development in B cell-deficient mice. IV. The role of B cells as antigen-presenting cells in vivo. J Immunol. 1986;136:823–829.
   PubMed Web of Science ®Google Scholar