Physicochemical Study of the Influenza a Virus M2 Protein and Aluminum Salt Adjuvant Interaction As a Vaccine Candidate Model

References

• Lindblad EB . Aluminium compounds for use in vaccines. Immunol. Cell. Biol., 82, 497–505 (2004).
   PubMed Web of Science ®Google Scholar
• Otto RBD , BurkinK, AmirSE, CraneDT, BolgianoB. Patterns of binding of aluminum-containing adjuvants to Haemophilus influenzae type B and meningococcal group C conjugate vaccines and components. Biologicals, 43(5), 355–362 (2015).
   PubMed Web of Science ®Google Scholar
• Art JF , Vander StraetenA, Dupont-GillainCC. Immobilization of aluminum hydroxide particles on quartz crystal microbalance sensors to elucidate antigen-adjuvant interaction mechanisms in vaccines. Anal. Chem., 90(2), 1168–1176 (2018).
   PubMed Web of Science ®Google Scholar
• Di Pasquale A , PreissS, TavaresDSF, GarçonN. Vaccine adjuvants: from 1920 to 2015 and beyond. Vaccine, 33, 20–43 (2015).
   Google Scholar
• Rappuoli R , MandlCW, BlackS, DeGregorio E. Vaccines for the twenty-first century society. Nat. Rev. Immuno., 11, 865–872 (2011).
   PubMed Web of Science ®Google Scholar
• Régnier M , MetzB, TilstraWet al. Structural perturbation of diphtheria toxoid upon adsorption to aluminium hydroxide adjuvant. Vaccine, 30, 6783–6788 (2012).
   PubMed Web of Science ®Google Scholar
• Jones LS , PeekLJ, PowerJet al. Effects of adsorption to aluminum salt adjuvants on the structure and stability of model protein antigens. J. Biol. Chem., 280, 13406–13414 (2005).
   PubMed Web of Science ®Google Scholar
• Ausar SF , ChanJ, HoqueWet al. Application of extrinsic fluorescence spectroscopy for the high throughput formulation screening of aluminum-adjuvanted vaccines. J. Pharm. Sci., 100(2), 431–440 (2011).
   PubMed Web of Science ®Google Scholar
• Soliakov A , KellyIF, LakeyJH, WatkinsonA. Anthrax sub-unit vaccine: the structural consequences of binding rPA83 to Alhydrogel®. Eur. J. Pharm. Biopharm., 80, 25–32 (2012).
   PubMed Web of Science ®Google Scholar
• Peek LJ , MartinTT, ElkNation C, PegramSA, MiddaughCR. Effects of stabilizers on the destabilization of proteins upon adsorption to aluminum salt adjuvants. J. Pharm. Sci., 96, 547–557 (2007).
   PubMed Web of Science ®Google Scholar
• Johnston CT , WangSL, HemSL. Measuring the surface area of aluminum hydroxide adjuvant. J. Pharm. Sci., 91(7), 1702–1706 (2002).
   PubMed Web of Science ®Google Scholar
• Coffman RL , SherA, SederRA. Vaccine adjuvants: putting innate immunity to work. Immunity, 33(4), 492–503 (2010).
   PubMed Web of Science ®Google Scholar
• Marrack P , McKeeAS, MunksMW. Towards an understanding of the adjuvant action of aluminium. Nat. Rev. Immunol., 9(4), 287–293 (2009).
   PubMed Web of Science ®Google Scholar
• Huang M , WangW. Factors affecting alum-protein interactions. Int. J. Pharm., 466, 139–146 (2014).
   PubMedGoogle Scholar
• Feng L , ShayDK, JiangYet al. Influenza-associated mortality in temperate and subtropical Chinese cities, 2003–2008. Bull. World Health Organ., 90, 279–288B (2012).
   PubMed Web of Science ®Google Scholar
• Kilbourne ED . Influenza pandemics of the 20th century. Emerg. Infect. Dis., 12(1), 9–14 (2006).
   PubMed Web of Science ®Google Scholar
• Johnson NP , MuellerJ. Updating the accounts: global mortality of the 1918–1920 “Spanish” influenza pandemic. Bull. Hist. Med., 76, 105–115 (2002).
   PubMed Web of Science ®Google Scholar
• Shrestha SS , SwerdlowDL, BorseRet al. Estimating the burden of 2009 pandemic influenza A (H1N1) in the United States (April 2009–April 2010). Cllin. Infect. Dis., 52, S75–S82 (2011).
   PubMed Web of Science ®Google Scholar
• Barr IG , DengYM, GrauMLet al. Intense interseasonal influenza outbreaks, Australia, 2018/19 (2019). www.eurosurveillance.org
   Google Scholar
• Wong S-S , WebbyRJ. Traditional and new influenza vaccines. Clin. Microbiol. Rev., 26(3), 476–492 (2013).
   PubMed Web of Science ®Google Scholar
• Schnell JR , ChouJJ. Structure and mechanism of the M2 proton channel of influenza A virus. Nature, 451(7178), 591–595 (2008).
   PubMed Web of Science ®Google Scholar
• Acharya R , CarnevaleV, FiorinGet al. Structure and mechanism of proton transport through the transmembrane tetrameric M2 protein bundle of the influenza A virus. Proc. Natl Acad. Sci. USA, 107(34), 15075–15080 (2010).
   PubMed Web of Science ®Google Scholar
• Zhou H-X . A theory for the proton transport of the influenza virus M2 protein: extensive test against conductance data. Biophys. J., 100(4), 912–921 (2011).
   PubMed Web of Science ®Google Scholar
• Pielak RM , ChouJJ. Influenza M2 proton channels. Biochim. Biophys. Acta, 1808(2), 522–529 (2011).
   PubMed Web of Science ®Google Scholar
• Shao Q , HallCK. Protein adsorption on nanoparticles: model development using computer simulation. J. Phys. Condens. Matter., 28(41), 414019 (2016).
   PubMed Web of Science ®Google Scholar
• Alavi Esfahani M , FotouhiF, GhaemiAet al. Over expression of influenza virus M2 protein in prokaryotic system. Iran. J. Virol., 6, 13–19 (2012).
   Google Scholar
• Fotouhi F , FarahmandB, HeidarchiBet al. In vitro evaluation of influenza M2 and Leishmania major HSP70 (221-604) chimer protein. Jundishapur J. Microbiol., 7(9), e11812–e11812 (2014).
   PubMed Web of Science ®Google Scholar
• Hamborg M , JorgensenL, BojsenAR, ChristensenD, FogedC. Protein antigen adsorption to the DDA/TDB liposomal adjuvant: effect on protein structure, stability, and liposome physicochemical characteristics. Pharm. Res., 30, 140–155 (2012).
   PubMed Web of Science ®Google Scholar
• O’Sullivan J , BeeversJ, ParkM, GreenwoodR, NortonI. Comparative assessment of the effect of ultrasound treatment on protein functionality pre- and post-emulsification. Colloids Surf. A Physicochem. Eng. Asp., 484, 89–98 (2015).
   Web of Science ®Google Scholar
• Dong A , JonesLS, KerwinBA, KrishnanS, CarpenterJF. Secondary structures of proteins adsorbed onto aluminum hydroxide: infrared spectroscopic analysis of proteins from low solution concentrations. Anal. Biochem., 351, 282–289 (2006).
   PubMed Web of Science ®Google Scholar
• Bolden JS , WarburtonRE, PhelanRet al. Endotoxin recovery using limulus amebocyte lysate (LAL) assay. Biologicals, 44(5), 434–440 (2016).
   PubMed Web of Science ®Google Scholar
• Schwarz H , GornicecJ, NeuperTet al. Biological activity of masked endotoxin. Sci. Rep., 7, 44750 (2017).
   PubMed Web of Science ®Google Scholar
• Akbar John B , JalalKCA, KamaruzzamanYB, ZalehaK. Mechanism in the clot formation of horseshoe crab blood during bacterial endotoxin invasion. J. Appl. Sci., 10(17), 1930–1936 (2010).
   Google Scholar
• Vanhaecke E , PijckJ, VuyeA. Endotoxin testing. J. Clin. Pharm. Ther., 12(4), 223–235 (1987).
   PubMed Web of Science ®Google Scholar
• Baars EW , Adriaansen-TennekesR, EikmansKJL. Safety of homeopathic injectables for subcutaneous administration: a documentation of the experience of prescribing practitioners. J. Altern. Complement. Med., 11(4), 609–616 (2005).
   PubMed Web of Science ®Google Scholar
• Mehmood Y . What is limulus amebocyte lysate (LAL) and its applicability in endotoxin quantification of pharma products (2019).Faculty of Pharmaceutical SciencesGovernment College University Faisalabad: Pakistan. www.intechopen.com
   Google Scholar
• British Pharmacopoeia Commission . Test for Bacterial Endotoxins (LAL Test) (2012).
   Google Scholar
• Azmi F , AhmadFuaad AAH, SkwarczynskiM, TothI. Recent progress in adjuvant discovery for peptide-based subunit vaccines. Hum. Vaccin. Immunother., 10(3), 778–796 (2014).
   PubMed Web of Science ®Google Scholar
• Betakova T , VareckovaE, KostolanskyF, MuchaV, DanielsRS. Monoclonal anti-idiotypic antibodies mimicking the immunodominant epitope of influenza virus haemagglutinin elicit biologically significant immune responses. J. Gen. Virol., 79(Pt 3), 461–470 (1998).
   PubMedGoogle Scholar
• Lee YT , KimKH, KoEJet al. New vaccines against influenza virus. Clin. Exp. Vaccine Res., 3(1), 12–28 (2014).
   PubMedGoogle Scholar
• Ngo VKT , NguyenHPU, HuynhTPet al. Preparation of gold nanoparticles by microwave heating and application of spectroscopy to study conjugate of gold nanoparticles with antibody E. coli O157:H7. Adv. Nat. Sci: Nanosci. Nanotechnol., 6, 61–66 (2015).
   Google Scholar
• Jully V , MathotF, MoniotteN, PréatV, LemoineD. Mechanisms of antigen adsorption onto an aluminum-hydroxide adjuvant evaluated by high-throughput screening. J. Pharm. Sci., 105(6), 1829–1836 (2016).
   PubMed Web of Science ®Google Scholar
• Zhou Y , FangX, GongYet al. The interactions between ZnO nanoparticles (NPs) and α-linolenic acid (LNA) complexed to BSA did not influence the toxicity of ZnO NPs on HepG2 cells. Nanomaterials, 7(4), 91 (2017).
   Web of Science ®Google Scholar
• Sun J , XuR, YangY. Conformational changes and bioactivity of lysozyme on binding to and desorption from magnetite nanoparticles. J. Chromatogr. B, 879(28), 3053–3058 (2011).
   PubMed Web of Science ®Google Scholar
• Fox CB , KramerRM, BarnesVL, DowlingQM, VedvickTS. Working together: interactions between vaccine antigens and adjuvants. Ther. Adv. Vaccines., 1(1), 7–20 (2013).
   PubMedGoogle Scholar
• Hamborg M , RoseF, JorgensenLet al. Elucidating the mechanisms of protein antigen adsorption to the CAF/NAF liposomal vaccine adjuvant systems: effect of charge, fluidity and antigen-to-lipid ratio. Biochim. Biophys. Acta Biomembr., 1838, 2001–2010 (2014).
   Web of Science ®Google Scholar
• Kosmulski M . Isoelectric points and points of zero charge of metal (hydr)oxides: 50 years after Parks’ review. Adv. Colloid Interface Sci., 238, 1–61 (2016).
   PubMed Web of Science ®Google Scholar
• Wagner L , VermaA, MeadeBDet al. Structural and immunological analysis of anthrax recombinant protective antigen adsorbed to aluminum hydroxide adjuvant. Clin. Vaccine Immunol., 19, 1465–1473 (2012).
   PubMed Web of Science ®Google Scholar
• Bai S , DongA. Effects of immobilization onto aluminum hydroxide particles on the thermally induced conformational behavior of three model proteins. Int. J. Biol. Macromol., 45(1), 80–85 (2009).
   PubMed Web of Science ®Google Scholar
• White J , HemS. Characterization of aluminium-containing adjuvants. Dev. Biol., 103, 217–228 (2000).
   Google Scholar
• Watkinson A , SoliakovA, GanesanAet al. Increasing the potency of an alhydrogel-formulated anthrax vaccine by minimizing antigen-adjuvant interactions. Clin. Vaccine Immunol., 20(11), 1659–1668 (2013).
   PubMedGoogle Scholar
• Goudarzi M , GhanbariD, Salavati-NiasariM. Room temperature preparation of aluminum hydroxide nanoparticles and flame retardant poly vinyl alcohol nanocomposite. J. Nanostruct., 5(2), 110–115 (2015).
   Google Scholar
• Eisenberg D , SchwarzE, KomaromyM, WallR. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol., 179(1), 125–142 (1984).
   PubMed Web of Science ®Google Scholar
• Eisenberg D , WeissRM, TerwilligerTC. The hydrophobic moment detects periodicity in protein hydrophobicity. Proc. Natl Acad. Sci. USA, 81(1), 140–144 (1984).
   PubMed Web of Science ®Google Scholar
• Kyte J , DoolittleRF. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol., 157(1), 105–132 (1982).
   PubMed Web of Science ®Google Scholar
• Chaudhuri D , NarayanM, BerlinerLJ. Conformation-dependent interaction of alpha-lactalbumin with model and biological membranes: a spin-label ESR study. Protein J., 23, 95–101 (2004).
   PubMed Web of Science ®Google Scholar
• Barth A . Infrared spectroscopy of proteins. Biochim. Biophys. Acta Bioenerg., 1767(9), 1073–1101 (2007).
   PubMed Web of Science ®Google Scholar
• Wu X , NarsimhanG. Effect of surface concentration on secondary and tertiary conformational changes of lysozyme adsorbed on silica nanoparticles. Biochim. Biophys. Acta Proteins Proteomics, 1784(11), 1694–1701 (2008).
   Web of Science ®Google Scholar
• Mobarak-Qamsari E , Kasra-KermanshahiR, ErfanMet al. Characteristics of surface layer proteins from two new and native strains of Lactobacillus brevis. Int. J. Biol. Macromol., 95, 1004–1010 (2017).
   PubMed Web of Science ®Google Scholar
• Kong J , YuS. Fourier transform infrared spectroscopic analysis of protein secondary structures. Acta Biochim. Biophys. Sin. (Shanghai), 39, 549–559 (2007).
   PubMed Web of Science ®Google Scholar
• Shaffifar M , TabarraeiA, SajadianA, FotouhiF, GhaemiA. Immunologic evaluation of DNA vaccine encoding influenza virus M2 gene in type A- influenza mice model. mljgoums, 9(1), 9–16 (2015).
   Google Scholar
• Hanly W , ArtwohlJ, BennettB. Review of polyclonal antibody production procedures in mammals and poultry. ILAR J., 37(3), 93–118 (1995).
   PubMedGoogle Scholar
• Weber J , PengH, RaderC. From rabbit antibody repertoires to rabbit monoclonal antibodies. Exp. Mol. Med., 49, e305 (2017).
   PubMed Web of Science ®Google Scholar
• Majidi J , BaradaranB, HassanZ, MostafaieA. Production and characterization of monoclonal antibodies against human IgG in Balb/c mouse. Hum. Antibodies, 14(1-2), 1–5 (2005).
   PubMedGoogle Scholar
• Ghimire TR . The mechanisms of action of vaccines containing aluminum adjuvants: an in vitro vs in vivo paradigm. SpringerPlus, 4(181), 1–18 (2015).
   PubMedGoogle Scholar
• Lee YN , KimMC, LeeYT, KimYJ, KangSM. Mechanisms of cross-protection by influenza virus M2-based vaccines. Immune Netw., 15(5), 213–221 (2015).
   PubMed Web of Science ®Google Scholar