Sequence- and Structure-Based Immunoreactive Epitope Discovery for Burkholderia pseudomallei Flagellin.

Nithichanon, A; The Centre for Research and Development of Medical Diagnostic Laboratories, Faculty of Associated Medical Sciences, Khon Kaen University, Khon Kaen, Thailand.

Rinchai, D; The Centre for Research and Development of Medical Diagnostic Laboratories, Faculty of Associated Medical Sciences, Khon Kaen University, Khon Kaen, Thailand.

Gori, Alessandro; Istituto di Chimica del Riconoscimento Molecolare, Consiglio Nazionale delle Ricerche, Milan, Italy.

Lassaux, Patricia ; Université de Liège > GIGA-R : Virologie - Immunologie

Peri, Claudio; Istituto di Chimica del Riconoscimento Molecolare, Consiglio Nazionale delle Ricerche, Milan, Italy.

Conchillio-Solé, Oscar; Institute of Biotechnology and Biomedicine, Universitat Autònoma de Barcelona, Bellaterra, Spain.

Ferrer-Navarro, Mario; Department of Clinical Microbiology, Hospital Clinic, School of Medicine, University of Barcelona, Barcelona, Spain.

Gourlay, Louise; Department of Biosciences, CIMAINA and CNR Institute of Biophysics, University of Milan, Milan, Italy.

Nardini, Marco; Department of Biosciences, CIMAINA and CNR Institute of Biophysics, University of Milan, Milan, Italy.

Vila, J; Department of Clinical Microbiology, Hospital Clinic, School of Medicine, University of Barcelona, Barcelona, Spain.

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Language :

English

Title :

Sequence- and Structure-Based Immunoreactive Epitope Discovery for Burkholderia pseudomallei Flagellin.

Publication date :

2015

Journal title :

PLoS Neglected Tropical Diseases

ISSN :

1935-2727

eISSN :

1935-2735

Publisher :

Public Library of Science

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 27 January 2017

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Currie BJ, Dance DA, Cheng AC (2008) The global distribution of Burkholderia pseudomallei and melioidosis: an update. Trans R Soc Trop Med Hyg 102 Suppl 1: S1–4.
Cheng AC, Currie BJ, Dance DA, Funnell SG, Limmathurotsakul D, et al. (2013) Clinical definitions of melioidosis. Am J Trop Med Hyg 88: 411–413. doi: 10.4269/ajtmh.12-0555 PMID: 23468355
Cheng AC, Currie BJ (2005) Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18: 383–416. PMID: 15831829
Choh LC, Ong GH, Vellasamy KM, Kalaiselvam K, Kang WT, et al. (2013) Burkholderia vaccines: are we moving forward? Front Cell Infect Microbiol 3: 5. doi: 10.3389/fcimb.2013.00005 PMID: 23386999
Moyle PM, Toth I (2013) Modern subunit vaccines: development, components, and research opportunities. ChemMedChem 8: 360–376. doi: 10.1002/cmdc.201200487 PMID: 23316023
Rueckert C, Guzman CA (2012) Vaccines: from empirical development to rational design. PLoS Pathog 8: e1003001. doi: 10.1371/journal.ppat.1003001 PMID: 23144616
Sarkar-Tyson M, Titball RW (2010) Progress toward development of vaccines against melioidosis: A review. Clin Ther 32: 1437–1445. doi: 10.1016/j.clinthera.2010.07.020 PMID: 20728758
Healey GD, Elvin SJ, Morton M, Williamson ED (2005) Humoral and cell-mediated adaptive immune responses are required for protection against Burkholderia pseudomallei challenge and bacterial clearance postinfection. Infect Immun 73: 5945–5951. PMID: 16113315
Haque A, Easton A, Smith D, O'Garra A, Van Rooijen N, et al. (2006) Role of T cells in innate and adaptive immunity against murine Burkholderia pseudomallei infection. J Infect Dis 193: 370–379. PMID: 16388484
Suwannasaen D, Mahawantung J, Chaowagul W, Limmathurotsakul D, Felgner PL, et al. (2011) Human immune responses to Burkholderia pseudomallei characterized by protein microarray analysis. J Infect Dis 203: 1002–1011. doi: 10.1093/infdis/jiq142 PMID: 21300673
Chen YS, Hsiao YS, Lin HH, Liu Y, Chen YL (2006) CpG-modified plasmid DNA encoding flagellin improves immunogenicity and provides protection against Burkholderia pseudomallei infection in BALB/c mice. Infect Immun 74: 1699–1705. PMID: 16495541
Brett PJ, Mah DC, Woods DE (1994) Isolation and characterization of Pseudomonas pseudomallei flagellin proteins. Infect Immun 62: 1914–1919. PMID: 7513308
Brett PJ, Woods DE (1996) Structural and immunological characterization of Burkholderia pseudomallei O-polysaccharide-flagellin protein conjugates. Infect Immun 64: 2824–2828. PMID: 8698517
Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099–1103. PMID: 11323673
Chen YS, Hsiao YS, Lin HH, Yen CM, Chen SC, et al. (2006) Immunogenicity and anti-Burkholderia pseudomallei activity in Balb/c mice immunized with plasmid DNA encoding flagellin. Vaccine 24: 750–758. PMID: 16169637
Hespel C, Moser M (2012) Role of inflammatory dendritic cells in innate and adaptive immunity. Eur J Immunol 42: 2535–2543. doi: 10.1002/eji.201242480 PMID: 23042650
Yoon SI, Kurnasov O, Natarajan V, Hong M, Gudkov AV, et al. (2012) Structural basis of TLR5-flagellin recognition and signaling. Science 335: 859–864. doi: 10.1126/science.1215584 PMID: 22344444
Mizel SB, Bates JT (2010) Flagellin as an adjuvant: cellular mechanisms and potential. J Immunol 185: 5677–5682. doi: 10.4049/jimmunol.1002156 PMID: 21048152
Musson JA, Reynolds CJ, Rinchai D, Nithichanon A, Khaenam P, et al. (2014) CD4+ T Cell Epitopes of FliC Conserved between Strains of Burkholderia: Implications for Vaccines against Melioidosis and Cepacia Complex in Cystic Fibrosis. J Immunol 193: 6041–6049. doi: 10.4049/jimmunol.1402273 PMID: 25392525
Patronov A, Doytchinova I (2013) T-cell epitope vaccine design by immunoinformatics. Open Biol 3: 120139. doi: 10.1098/rsob.120139 PMID: 23303307
Larsen JE, Lund O, Nielsen M (2006) Improved method for predicting linear B-cell epitopes. Immunome Res 2: 2. PMID: 16635264
Saha S, Raghava GP (2006) Prediction of continuous B-cell epitopes in an antigen using recurrent neural network. Proteins 65: 40–48. PMID: 16894596
Vita R, Zarebski L, Greenbaum JA, Emami H, Hoof I, et al. (2010) The immune epitope database 2.0. Nucleic Acids Res 38: D854–862. doi: 10.1093/nar/gkp1004 PMID: 19906713
Scarabelli G, Morra G, Colombo G (2010) Predicting interaction sites from the energetics of isolated proteins: a new approach to epitope mapping. Biophys J 98: 1966–1975. doi: 10.1016/j.bpj.2010.01.014 PMID: 20441761
Fiorucci S, Zacharias M (2010) Prediction of protein-protein interaction sites using electrostatic desolvation profiles. Biophys J 98: 1921–1930. doi: 10.1016/j.bpj.2009.12.4332 PMID: 20441756
Barnes JL, Warner J, Melrose W, Durrheim D, Speare R, et al. (2004) Adaptive immunity in melioidosis: a possible role for T cells in determining outcome of infection with Burkholderia pseudomallei. Clin Immunol 113: 22–28. PMID: 15380526
Cheng AC, O'Brien M, Freeman K, Lum G, Currie BJ (2006) Indirect hemagglutination assay in patients with melioidosis in northern Australia. Am J Trop Med Hyg 74: 330–334. PMID: 16474092
Romphruk AV, Romphruk A, Kongmaroeng C, Klumkrathok K, Paupairoj C, et al. (2010) HLA class I and II alleles and haplotypes in ethnic Northeast Thais. Tissue Antigens 75: 701–711. doi: 10.1111/j.1399-0039.2010.01448.x PMID: 20230525
Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66: 125–132. doi: 10.1107/S0907444909047337 PMID: 20124692
Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235–242. doi: 10.1107/S0907444910045749 PMID: 21460441
McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658–674. PMID: 19461840
Langer G, Cohen SX, Lamzin VS, Perrakis A (2008) Automated macromolecular model building for Xray crystallography using ARP/wARP version 7. Nat Protoc 3: 1171–1179. doi: 10.1038/nprot.2008.91 PMID: 18600222
Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486–501. doi: 10.1107/S0907444910007493 PMID: 20383002
Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum- likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240–255. PMID: 15299926
Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK- NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477–486. PMID: 9008363
Berman HM, Westbrook JD, Gabanyi MJ, Tao W, Shah R, et al. (2009) The protein structure initiative structural genomics knowledgebase. Nucleic Acids Res 37: D365–368. doi: 10.1093/nar/gkn790 PMID: 19010965
Pronk S, Pall S, Schulz R, Larsson P, Bjelkmar P, et al. (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29: 845–854. doi: 10.1093/bioinformatics/btt055 PMID: 23407358
Chandrasekhar I, Kastenholz M, Lins RD, Oostenbrink C, Schuler LD, et al. (2003) A consistent potential energy parameter set for lipids: dipalmitoylphosphatidylcholine as a benchmark of the GROMOS96 45A3 force field. Eur Biophys J 32: 67–77. PMID: 12632209
Armstrong JA, Bresme F (2013) Water polarization induced by thermal gradients: the extended simple point charge model (SPC/E). J Chem Phys 139: 014504. doi: 10.1063/1.4811291 PMID: 23822311
Daura X, Jaun B, Seebach D, van Gunsteren WF, Mark AE (1998) Reversible peptide folding in solution by molecular dynamics simulation. J Mol Biol 280: 925–932. PMID: 9671560
Gourlay LJ, Peri C, Ferrer-Navarro M, Conchillo-Sole O, Gori A, et al. (2013) Exploiting the Burkholderia pseudomallei acute phase antigen BPSL2765 for structure-based epitope discovery/design in structural vaccinology. Chem Biol 20: 1147–1156. doi: 10.1016/j.chembiol.2013.07.010 PMID: 23993463
Colacino S, Tiana G, Colombo G (2006) Similar folds with different stabilization mechanisms: the cases of Prion and Doppel proteins. BMC Struct Biol 6: 17. PMID: 16857062
Colacino S, Tiana G, Broglia RA, Colombo G (2006) The determinants of stability in the human prion protein: insights into folding and misfolding from the analysis of the change in the stabilization energy distribution in different conditions. Proteins 62: 698–707. PMID: 16432880
Morra G, Colombo G (2008) Relationship between energy distribution and fold stability: Insights from molecular dynamics simulations of native and mutant proteins. Proteins 72: 660–672. doi: 10.1002/prot.21963 PMID: 18247351
Ragona L, Colombo G, Catalano M, Molinari H (2005) Determinants of protein stability and folding: comparative analysis of beta-lactoglobulins and liver basic fatty acid binding protein. Proteins 61: 366–376. PMID: 16121395
Tiana G, Simona F, De Mori GM, Broglia RA, Colombo G (2004) Understanding the determinants of stability and folding of small globular proteins from their energetics. Protein Sci 13: 113–124. PMID: 14691227
Amblard M, Fehrentz JA, Martinez J, Subra G (2006) Methods and protocols of modern solid phase Peptide synthesis. Mol Biotechnol 33: 239–254. PMID: 16946453
Zhang Q, Wang P, Kim Y, Haste-Andersen P, Beaver J, et al. (2008) Immune epitope database analysis resource (IEDB-AR). Nucleic Acids Res 36: W513–518. doi: 10.1093/nar/gkn254 PMID: 18515843
Samatey FA, Imada K, Nagashima S, Vonderviszt F, Kumasaka T, et al. (2001) Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410: 331–337. PMID: 11268201
Song WS, Yoon SI (2014) Crystal structure of FliC flagellin from Pseudomonas aeruginosa and its implication in TLR5 binding and formation of the flagellar filament. Biochem Biophys Res Commun 444: 109–115. doi: 10.1016/j.bbrc.2014.01.008 PMID: 24434155
Donnelly MA, Steiner TS (2002) Two nonadjacent regions in enteroaggregative Escherichia coli flagellin are required for activation of toll-like receptor 5. J Biol Chem 277: 40456–40461. PMID: 12185085
Eaves-Pyles TD, Wong HR, Odoms K, Pyles RB (2001) Salmonella flagellin-dependent proinflammatory responses are localized to the conserved amino and carboxyl regions of the protein. J Immunol 167: 7009–7016. PMID: 11739521
Lassaux P, Peri C, Ferrer-Navarro M, Gourlay LJ, Gori A, et al. (2013) A structure-based strategy for epitope discovery in Burkholderia pseudomallei OppA antigen. Structure 21: 167–175. doi: 10.1016/j.str.2012.10.005 PMID: 23159127
Moroni E, Scarabelli G, Colombo G (2009) Structure and sequence determinants of aggregation investigated with molecular dynamics. Front Biosci (Landmark Ed) 14: 523–539.
Koehler C, Carlier L, Veggi D, Balducci E, Di Marcello F, et al. (2011) Structural and biochemical characterization of NarE, an iron-containing ADP-ribosyltransferase from Neisseria meningitidis. J Biol Chem 286: 14842–14851. doi: 10.1074/jbc.M110.193623 PMID: 21367854
Wiersinga WJ, Currie BJ, Peacock SJ (2012) Melioidosis. N Engl J Med 367: 1035–1044. doi: 10.1056/NEJMra1204699 PMID: 22970946
Segal A (2005) How neutrophils kill microbes. Annu Rev Immunol.
Easton A, Haque A, Chu K, Lukaszewski R, Bancroft GJ (2007) A critical role for neutrophils in resistance to experimental infection with Burkholderia pseudomallei. J Infect Dis 195: 99–107. PMID: 17152013
Bobat S, Flores-Langarica A, Hitchcock J, Marshall JL, Kingsley RA, et al. (2011) Soluble flagellin, FliC, induces an Ag-specific Th2 response, yet promotes T-bet-regulated Th1 clearance of Salmonella typhimurium infection. Eur J Immunol 41: 1606–1618. doi: 10.1002/eji.201041089 PMID: 21469112
Gassmann GS, Jacobs E, Deutzmann R, Gobel UB (1991) Analysis of the Borrelia burgdorferi GeHo fla gene and antigenic characterization of its gene product. J Bacteriol 173: 1452–1459. PMID: 1704884
McSorley SJ, Cookson BT, Jenkins MK (2000) Characterization of CD4+ T cell responses during natural infection with Salmonella typhimurium. J Immunol 164: 986–993. PMID: 10623848
Bergman MA, Cummings LA, Alaniz RC, Mayeda L, Fellnerova I, et al. (2005) CD4+-T-cell responses generated during murine Salmonella enterica serovar Typhimurium infection are directed towards multiple epitopes within the natural antigen FliC. Infect Immun 73: 7226–7235. PMID: 16239517
Smith MF Jr., Mitchell A, Li G, Ding S, Fitzmaurice AM, et al. (2003) Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-kappa B activation and chemokine expression by epithelial cells. J Biol Chem 278: 32552–32560. PMID: 12807870
Samatey FA, Matsunami H, Imada K, Nagashima S, Shaikh TR, et al. (2004) Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature 431: 1062–1068. PMID: 15510139
Patel N, Conejero L, De Reynal M, Easton A, Bancroft GJ, et al. (2011) Development of vaccines against burkholderia pseudomallei. Front Microbiol 2: 198. doi: 10.3389/fmicb.2011.00198 PMID: 21991263
Yin G, Qin M, Liu X, Suo J, Tang X, et al. (2013) An Eimeria vaccine candidate based on Eimeria tenella immune mapped protein 1 and the TLR-5 agonist Salmonella typhimurium FliC flagellin. Biochem Biophys Res Commun 440: 437–442. doi: 10.1016/j.bbrc.2013.09.088 PMID: 24076159
Simon R, Wang JY, Boyd MA, Tulapurkar ME, Ramachandran G, et al. (2013) Sustained protection in mice immunized with fractional doses of Salmonella Enteritidis core and O polysaccharide-flagellin glycoconjugates. PLoS One 8: e64680. doi: 10.1371/journal.pone.0064680 PMID: 23741368
Bachar O, Fischer D, Nussinov R, Wolfson H (1993) A computer vision based technique for 3-D sequence-independent structural comparison of proteins. Protein Eng 6: 279–288. PMID: 8506262