1,559
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Epitope-specific anti-PrP antibody toxicity: a comparative in-silico study of human and mouse prion proteins

ORCID Icon & ORCID Icon
Pages 155-176 | Received 02 Jun 2021, Accepted 30 Jul 2021, Published online: 10 Oct 2021

References

  • Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science. 1982;216(4542):136–144.
  • Baskakov IV, Breydo L, Converting the prion protein: what makes the protein infectious. Biochim Biophys Acta - Mol Basis Dis. 2007; 1772(6):692–703.
  • Liao YC, Lebo RV, Clawson GA, et al., Human prion protein cDNA: molecular cloning, chromosomal mapping, and biological implications. Science. 1986; 233(4761):364–367.
  • Sparkes RS, Simon M, Cohn VH, et al., Assignment of the human and mouse prion protein genes to homologous chromosomes. Proc Natl Acad Sci. 1986; 83(19):7358–7362.
  • Walmsley AR, Zeng F, Hooper NM, Membrane topology influences N-glycosylation of the prion protein. EMBO J. 2001; 20(4):703–712.
  • Puig B, Altmeppen HC, Linsenmeier L, et al. GPI-anchor signal sequence influences PrPC sorting, shedding and signalling, and impacts on different pathomechanistic aspects of prion disease in mice. PLoS Pathog. 2019;15(1):e1007520.
  • Turnbaugh JA, Unterberger U, Saá P, et al. The N-terminal, polybasic region of PrP(C) dictates the efficiency of prion propagation by binding to PrP(Sc). J Neurosci. 2012;32(26):8817–8830.
  • Shyng S-L, Moulder KL, Lesko A, et al., The N-terminal domain of a glycolipid-anchored prion protein is essential for its endocytosis via clathrin-coated pits. J Biol Chem. 1995; 270(24):14793–14800.
  • Sunyach C, Jen A, Deng J, et al. The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein. EMBO J. 2003;22(14):3591–3601.
  • Davies P, Brown DR. The chemistry of copper binding to PrP: is there sufficient evidence to elucidate a role for copper in protein function? Biochem J. 2008;410:237–44.
  • Sakudo A, Lee D, Nishimura T, et al. Octapeptide repeat region and N-terminal half of hydrophobic region of prion protein (PrP) mediate PrP-dependent activation of superoxide dismutase. Biochem Biophys Res Commun. 2005;326(3):600–606. .
  • Kupfer L, Hinrichs W, Groschup MH, Prion protein misfolding. Curr Mol Med. 2009; 9(7):826–835.
  • Watts JC, Bourkas MEC, Arshad H. The function of the cellular prion protein in health and disease. Acta Neuropathol. 2018;135(2):159–178.
  • Legname G. Elucidating the function of the prion protein. PLOS Pathog. 2017;13(8):1–6.
  • Heppner FL, Musahl C, Arrighi I, et al., Prevention of scrapie pathogenesis by transgenic expression of anti-prion protein antibodies. Science. 2001; 294(5540):178–182.
  • Schwarz A, Krätke O, Burwinkel M, et al., Immunisation with a synthetic prion protein-derived peptide prolongs survival times of mice orally exposed to the scrapie agent. Neurosci Lett. 2003; 350(3):187–189.
  • Frontzek K, Aguzzi A. Recent developments in antibody therapeutics against prion disease. Emerg Top Life Sci. 2020;4(2):169–173.
  • Sigurdsson EM, Brown DR, Daniels M, et al., Immunization delays the onset of prion disease in mice. Am J Pathol. 2002; 161(1):13–17.
  • White AR, Enever P, Tayebi M, et al. Monoclonal antibodies inhibit prion replication and delay the development of prion disease. Nature. 2003;422(6927):80–83.
  • Aguzzi A, Nuvolone M, Zhu C. The immunobiology of prion diseases. Nat Rev Immunol. 2013;13(12):888.
  • Ma Y, Ma J. Immunotherapy against PRION DIsease. Pathog (Basel, Switzerland). 2020;9(3):216.
  • Burchell JT, Panegyres PK. Prion diseases: immunotargets and therapy. ImmunoTargets Ther. 2016;5:57–68.
  • Aguzzi A, Lakkaraju AKK, Frontzek K. Toward therapy of human prion diseases. Annu Rev Pharmacol Toxicol. 2018;58(1):331–351.
  • Roettger Y, Du Y, Bacher M, et al. Immunotherapy in prion disease. Nat Rev Neurol. 2013;9(2):98–105.
  • Trevitt CR, Collinge J. A systematic review of prion therapeutics in experimental models. Brain. 2006;129(9):2241–2265.
  • Enari M, Flechsig E, Weissmann C. Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody. Proc Natl Acad Sci U S A. 2001;98(16):9295–9299.
  • Beringue V, Mallinson G, Kaisar M, et al. Regional heterogeneity of cellular prion protein isoforms in the mouse brain. Brain. 2003;126(9):2065–2073.
  • Polymenidou M, Moos R, Scott M, et al. The POM monoclonals: a comprehensive set of antibodies to non-overlapping prion protein epitopes. PLoS One. 2008;3(12):e3872. .
  • Williamson RA, Peretz D, Pinilla C, et al. Mapping the prion protein using recombinant antibodies. J Virol. 1998;72(11):9413–9418.
  • Peretz D, Williamson RA, Kaneko K, et al. Antibodies inhibit prion propagation and clear cell cultures of prion infectivity. Nature. 2001;412(6848):739–743.
  • Féraudet C, Morel N, Simon S, et al. Screening of 145 anti-PrP monoclonal antibodies for their capacity to inhibit PrPSc replication in infected cells. J Biol Chem. 2005;280(12):11247–11258.
  • Demart S, Fournier J-G, Creminon C, et al., New insight into abnormal prion protein using monoclonal antibodies. Biochem Biophys Res Commun. 1999; 265(3):652–657.
  • Reimann RR, Sonati T, Hornemann S, et al., differential toxicity of antibodies to the prion protein. PLoS Pathog. 2016; 12(1):e1005401.
  • Solforosi L, Criado JR, McGavern DB, et al. Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science. 2004;303(5663):1514–1516.
  • P-c K, Farmer M, Linehan JM, et al. PrP antibodies do not trigger mouse hippocampal neuron apoptosis. Science. 2012;335(6064):52.
  • Sonati T, Rr R, Falsig J, et al. The toxicity of antiprion antibodies is mediated by the flexible tail of the prion protein. Nature. 2013;501(7465):102.
  • Herrmann US, Sonati T, Falsig J, et al. Prion infections and anti-PrP antibodies trigger converging neurotoxic pathways. PLoS Pathog. 2015;11(2):e1004662. .
  • Frontzek K, Pfammatter M, Sorce S, et al., Neurotoxic antibodies against the prion protein do not trigger prion replication. PLoS One. 2016; 11(9):e0163601.
  • Lefebvre-Roque M, Kremmer E, Gilch S, et al. Toxic effects of intracerebral PrP antibody administration during the course of BSE infection in mice. Prion. 2007;1(3):198–206. .
  • Klyubin I, Nicoll AJ, Khalili-Shirazi A, et al. Peripheral administration of a humanized anti-PrP antibody blocks Alzheimer’s disease Aβ synaptotoxicity. J Neurosci. 2014; 34(18)::6140–6145.
  • Khalili-Shirazi A, Quaratino S, Londei M, et al. Protein conformation significantly influences immune responses to prion protein. J Immunol. 2005;174(6):3256–3263.
  • Brown DR, Iordanova IK, Wong BS, et al. Functional and structural differences between the prion protein from two alleles prnp(a) and prnp(b) of mouse. Eur J Biochem. 2000;267(8):2452–2459. .
  • Sanchez-Trincado JL, Gomez-Perosanz M, Reche PA. Fundamentals and methods for t- and b-cell epitope prediction. J Immunol Res. 2017;2017:2680160.
  • Roy A, Kucukural A, Zhang Y, I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc. 2010; 5(4):725–738.
  • Krieger E, Darden T, Nabuurs SB, et al. Making optimal use of empirical energy functions: force-field parameterization in crystal space. Proteins. 2004;57(4):678–683.
  • Krieger E, Vriend G. New ways to boost molecular dynamics simulations. J Comput Chem. 2015;36(13):996–1007.
  • Zahn R, Liu A, Lührs T, et al., NMR solution structure of the human prion protein. Proc Natl Acad Sci U S A. 2000; 97(1):145–150.
  • Knaus KJ, Morillas M, Swietnicki W, et al. Crystal structure of the human prion protein reveals a mechanism for oligomerization. Nat Struct Biol. 2001;8(9):770–774.
  • Riek R, Hornemann S, Wider G, et al. NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Lett. 1997;413(2):282–288.
  • Kumar CV, Swetha RG, Anbarasu A, et al. Computational analysis reveals the association of threonine 118 methionine mutation in PMP22 resulting in CMT-1A. Adv Bioinformatics. 2014;2014:502618.
  • Ponomarenko J, Bui -H-H, Li W, et al. ElliPro: a new structure-based tool for the prediction of antibody epitopes. BMC Bioinformatics. 2008;9(1):514.
  • Jespersen MC, Peters B, Nielsen M, et al. BepiPred-2.0: improving sequence-based B-cell epitope prediction using conformational epitopes. Nucleic Acids Res. 2017;45(W1):W24–W29.
  • Gupta S, Kapoor P, Chaudhary K, et al., Open source drug discovery consortium, raghava gps. in silico approach for predicting toxicity of peptides and proteins. PLoS One. 2013; 8(9):e73957.
  • Garnier J, Osguthorpe DJ, Robson B, Prediction of the secondary structure of proteins from their amino-acid sequence. J Mol Biol. 1978; 120(1):97–120.
  • Adhikari UK, Tayebi M, Mizanur RM. Immunoinformatics approach for epitope-based peptide vaccine design and active site prediction against polyprotein of emerging oropouche virus. J Immunol Res. 2018;2018:1–22.
  • Adhikari UK, Rahman MM. Overlapping {CD8} + and {CD4} + T-cell epitopes identification for the progression of epitope-based peptide vaccine from nucleocapsid and glycoprotein of emerging Rift Valley fever virus using immunoinformatics approach. Infect Genet Evol 2017; 56:75–91.
  • Nain Z, Karim MM, Sen MK, et al. Structural basis and designing of peptide vaccine using PE-PGRS family protein of mycobacterium ulcerans—An integrated vaccinomics approach. Mol Immunol. 2020; 120:146–163.
  • Abdulla F, Nain Z, Hossain MM, et al. A comprehensive screening of the whole proteome of hantavirus and designing a multi-epitope subunit vaccine for cross-protection against hantavirus: structural vaccinology and immunoinformatics study. Microb Pathog. 2021; 150:104705.
  • Khan MSA, Nain Z, Bin SS, et al. Computational formulation and immune dynamics of a multi-peptide vaccine candidate against Crimean-Congo hemorrhagic fever virus. Mol Cell Probes. 2021; 55:101693.
  • Bin SS, Nain Z, Khan MSA, et al. Exploring Lassa Virus Proteome to Design a Multi-epitope Vaccine Through Immunoinformatics and Immune Simulation Analyses. Int J Pept Res Ther. 2020;26(4):2089–2107.
  • DeLuca DS, Blasczyk R, The immunoinformatics of cancer immunotherapy. Tissue Antigens. 2007; 70(4):265–271.
  • Büeler H, Aguzzi A, Sailer A, et al. Mice devoid of PrP are resistant to scrapie. Cell. 1993;73(7):1339–1347.
  • Brandner S, Raeber A, Sailer A, et al. Normal host prion protein (PrPC) is required for scrapie spread within the central nervous system. Proc Natl Acad Sci U S A. 1996;93(23):13148–13151.
  • Brandner S, Isenmann S, Raeber A, et al. Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature. 1996;379(6563):339–343.
  • David MA, Jones DR, Tayebi M, Potential candidate camelid antibodies for the treatment of protein-misfolding diseases. J Neuroimmunol. 2014; 272(1–2):76–85.
  • Aguzzi A, Baumann F, Bremer J. The prion’s elusive reason for being. Annu Rev Neurosci. 2008;31(1):439–477.
  • Liemann S, Glockshuber R. Influence of amino acid substitutions related to inherited human prion diseases on the thermodynamic stability of the cellular prion protein †. Biochemistry. 1999;38(11):3258–3267.
  • Calzolai L, Zahn R. Influence of pH on NMR structure and stability of the human prion protein globular domain. J Biol Chem. 2003;278(37):35592–35596.
  • Antonyuk SV, Trevitt CR, Strange RW, et al. Crystal structure of human prion protein bound to a therapeutic antibody. Proc Natl Acad Sci U S A. 2009;106(8):2554–2558. .
  • Riek R, Hornemann S, Wider G, et al. NMR structure of the mouse prion protein domain PrP(121–231). Nature. 1996;382(6587):180–182.
  • Hollingsworth SA, Dror RO, Molecular dynamics simulation for all. Neuron. 2018; 99(6):1129–1143.
  • Karplus M, McCammon JA. Molecular dynamics simulations of biomolecules. Nat Struct Biol. 2002;9(9):646–652.
  • Spagnolli G, Rigoli M, Orioli S, et al. Full atomistic model of prion structure and conversion. PLOS Pathog. 2019;15(7):1–18.
  • Buchete N-V, Tycko R, Hummer G. Molecular dynamics simulations of Alzheimer’s beta-amyloid protofilaments. J Mol Biol. 2005;353(4):804–821.
  • Lemkul JA, Bevan DR. The role of molecular simulations in the development of inhibitors of amyloid β-peptide aggregation for the treatment of Alzheimer’s disease. ACS Chem Neurosci. 2012;3(11):845–856.
  • Hassan M, Shahzadi S, Seo SY, et al. Molecular docking and dynamic simulation of AZD3293 and Solanezumab effects against BACE1 to treat alzheimer’s disease. Front Comput Neurosci. 2018; 12:34.
  • Mohankumar T, Chandramohan V, Lalithamba HS, et al. Design and molecular dynamic investigations of 7,8-dihydroxyflavone derivatives as potential neuroprotective agents against alpha-synuclein. Sci Rep. 2020;10(1):599.
  • Barducci A, Chelli R, Procacci P, et al., Misfolding Pathways of the prion protein probed by molecular dynamics simulations. Biophys J. 2005; 88(2):1334–1343.
  • Cheng CJ, Daggett V. Molecular dynamics simulations capture the misfolding of the bovine prion protein at acidic pH. Biomolecules. 2014;4(1):181–201.
  • Lee J, Chang I, Yu W. Atomic insights into the effects of pathological mutants through the disruption of hydrophobic core in the prion protein. Sci Rep. 2019;9(1):19144.
  • DeMarco ML, Daggett V. Molecular Mechanism for low ph triggered misfolding of the human prion protein†. Biochemistry. 2007;46(11):3045–3054.
  • Zuegg J, Gready JE. Molecular dynamics simulation of human prion protein including both N-linked oligosaccharides and the GPI anchor. Glycobiology. 2000;10(10):959–974.
  • Zheng Z, Zhang M, Wang Y, et al. Structural basis for the complete resistance of the human prion protein mutant G127V to prion disease. Sci Rep. 2018;8(1):13211.
  • Jobling MF, Stewart LR, White AR, et al. The hydrophobic core sequence modulates the neurotoxic and secondary structure properties of the prion peptide 106-126. J Neurochem. 1999;73(4):1557-65.
  • Baumann F, Tolnay M, Brabeck C, et al. Lethal recessive myelin toxicity of prion protein lacking its central domain. EMBO J. 2007;26(2):538–547.
  • Zhang B, Shen P, Yin X, et al., Expression and functions of cellular prion proteins in immunocytes. Scand J Immunol. 2020; 91(3):e12854.
  • Isaacs JD, Jackson GS, Altmann DM. The role of the cellular prion protein in the immune system. Clin Exp Immunol. 2006;146(1):1–8.
  • Bakkebø MK, Mouillet-Richard S, Espenes A, et al. The cellular prion protein: a player in immunological quiescence. Front Immunol. 2015;6:450.
  • Senatore A, Frontzek K, Emmenegger M, et al. Protective anti-prion antibodies in human immunoglobulin repertoires. EMBO Mol Med. 2020; 12(9):e12739.
  • Bairoch A, The AR, SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res. 2000; 28(1):45–48.
  • Cheng J, Randall AZ, Sweredoski MJ, et al. SCRATCH: a protein structure and structural feature prediction server. Nucleic Acids Res. 2005;33:W72–6.
  • Chenna R, Sugawara H, Koike T, et al., Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003; 31(13):3497–3500.
  • Laskowski RA, Jabłońska J, Pravda L, et al., PDBsum: structural summaries of PDB entries. Protein Sci. 2018; 27:129–134.
  • Wiederstein M, Sippl MJ. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007;35:W407–10.
  • Castrignanò T, De Meo PD, Cozzetto D, et al. The PMDB protein model database. Nucleic Acids Res. 2006; 34:D306.
  • Dickson CJ, Madej BD, Skjevik AA, et al. Lipid14: the Amber Lipid Force Field. J Chem Theory Comput. 2014;10(2):865–879.
  • Emini EA, Hughes JV, Perlow DS, et al. Induction of hepatitis A virus-neutralizing antibody by a virus-specific synthetic peptide. J Virol. 1985;55(3):836–839.
  • Karplus PA, Schulz GE. Prediction of chain flexibility in proteins. Naturwissenschaften. 1985;72(4):212–213.
  • Kolaskar AS, Tongaonkar PC. A semi-empirical method for prediction of antigenic determinants on protein antigens. FEBS Lett. 1990;276(1–2):172–174.
  • Vita R, Overton JA, Greenbaum JA, et al. The immune epitope database (IEDB) 3.0. Nucleic Acids Res] 2015; 43:D405–12.
  • Adhikari UK, Sakiz E, Zheng Y-F, et al. Cross-linking cellular prion protein induces neuronal type 2-like hypersensitivity. Front Immunol. 2021;12:639008.