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Vaccine potential of bacterial macrophage infectivity potentiator (MIP)-like peptidyl prolyl cis/trans isomerase (PPIase) proteins

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References

  • Reference annotations
  • * Of interest
  • ** Of considerable interest
  • Schiene-Fischer C, Aumuller T, Fischer G. Peptide bond cis/trans isomerases: a biocatalysis perspective of conformational dynamics in proteins. Top Curr Chem. 2013;328:35–67.
  • Bang H, Pecht A, Raddatz G, et al. Prolyl isomerases in a minimal cell. Catalysis of protein folding by trigger factor from Mycoplasma genitalium. Eur J Biochem. 2000;267:3270–3280.
  • Gothel SF, Marahiel MA. Peptidyl-prolyl cis–trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci. 1999;55:423–436.
  • Fanghanel J, Fischer G. Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front Biosci. 2004;9:3453–3478.
  • Holt DA, Luengo JI, Yamashita DS, et al. Design, synthesis, and kinetic evaluation of high-affinity Fkbp ligands and the X-ray crystal structures of their complexes with Fkbp12. J Am Chem Soc. 1993;115:9925–9938.
  • Luban J, Bossolt KL, Franke EK, et al. Human Immunodeficiency Virus Type-1 Gag protein binds to cyclophilin-A and cyclophilin-B. Cell. 1993;73:1067–1078.
  • Rahfeld JU, Schierhorn A, Mann K, et al. A novel peptidyl-prolyl cis/trans isomerase from Escherichia coli. FEBS Lett. 1994;343:65–69.
  • Unal CM, Steinert M. Microbial peptidyl-prolyl cis/trans isomerases (PPIases): virulence factors and potential alternative drug targets. Microbiol Mol Biol Rev. 2014;78:544–571.

* An excellent review article on PPIases.

  • Schiene-Fischer C. Multidomain peptidyl prolyl cis/trans isomerases. Biochim Biophys Acta. 2015;1850:2005–2016. doi:10.1016/j.bbagen.2014.11.012.
  • Rasch J, Unal CM, Steinert M. Peptidylprolyl cis-trans isomerases of Legionella pneumophila: virulence, moonlighting and novel therapeutic targets. Biochem Soc Trans. 2014;42:1728–1733.
  • Gioti A, Simon A, Le Pecheur P, et al. Expression profiling of Botrytis cinerea genes identifies three patterns of up-regulation in Planta and an FKBP12 protein affecting pathogenicity. J Mol Biol. 2006;358:372–386.
  • Port GC, Freitag NE. Identification of novel Listeria monocytogenes secreted virulence factors following mutational activation of the central virulence regulator, PrfA. Infect Immun. 2007;75:5886–5897.
  • Unal CM, Steinert M. FKBPs in bacterial infections. Biochim Biophys Acta. 2015;1850:2096–2102.
  • Behrens-Kneip S. The role of SurA factor in outer membrane protein transport and virulence. Int J Med Microbiol. 2010;300:421–428.
  • Hermans PWM, Adrian PV, Albert C, et al. The streptococcal lipoprotein rotamase A (SlrA) is a functional peptidyl-prolyl isomerase involved in pneumococcal colonization. J Biol Chem. 2006;281:968–976.
  • Purdy GE, Fisher CR, Payne SM. IcsA surface presentation in Shigella flexneri requires the periplasmic chaperones DegP, Skp, and SurA. J Bacteriol. 2007;189:5566–5573.
  • Alonzo F III, Freitag NE. Listeria monocytogenes PrsA2 is required for virulence factor secretion and bacterial viability within the host cell cytosol. Infect Immun. 2010;78:4944–4957.
  • Forster BM, Zemansky J, Portnoy DA, et al. Posttranslocation chaperone PrsA2 regulates the maturation and secretion of Listeria monocytogenes proprotein virulence factors. J Bacteriol. 2011;193:5961–5970.
  • Kandror O, Goldberg AL. Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Proc Natl Acad Sci USA. 1997;94:4978–4981.
  • Soderberg MA, Cianciotto NP. A Legionella pneumophila peptidyl-prolyl cis-trans isomerase present in culture supernatants is necessary for optimal growth at low temperatures. Appl Environ Microbiol. 2008;74:1634–1638.
  • Cianciotto NP, Eisenstein BI, Mody CH, et al. A mutation in the MIP gene results in an attenuation of Legionella pneumophila virulence. J Infect Dis. 1990;162:121–126.
  • Norville IH, Harmer NJ, Harding SV, et al. A Burkholderia pseudomallei Macrophage Infectivity Potentiator-Like protein has rapamycin-inhibitable peptidylprolyl isomerase activity and pleiotropic effects on virulence. Infect Immun. 2011;79:4299–4307.
  • Norville IH, Breitbach K, Eske-Pogodda K, et al. A novel FK-506-binding-like protein that lacks peptidyl-prolyl isomerase activity is involved in intracellular infection and in vivo virulence of Burkholderia pseudomallei. Microbiol-Sgm. 2011;157:2629–2638.
  • Wu T, Zhao Z, Zhang L, et al. Trigger factor of Streptococcus suis is involved in stress tolerance and virulence. Microbial Path. 2011;51:69–76.
  • Zang N, Tang DJ, Wei ML, et al. Requirement of a mip-like gene for virulence in the phytopathogenic bacterium Xanthomonas campestris pv. campestris. Molecular Plant-Microbe Interactions. 2007;20:21–30.
  • Moro A, Ruizcabello F, Fernandezcano A, et al. Secretion by Trypanosoma cruzi of a peptidyl-prolyl cis-trans isomerase involved in cell infection. EMBO J. 1995;14:2483–2490.
  • Obi IR, Nordfelth R, Francis MS. Varying dependency of periplasmic peptidylprolyl cis-trans isomerases in promoting Yersinia pseudotuberculosis stress tolerance and pathogenicity. Biochem J. 2011;439:321–332.
  • Hung MC, Salim O, Williams JN, et al. The Neisseria meningitidis Macrophage Infectivity Potentiator protein induces cross-strain serum bactericidal activity and is a potential serogroup B vaccine candidate. Infect Immun. 2011;79:3784–3791.
  • Lundemose AG, Birkelund S, Fey SJ, et al. Chlamydia trachomatis contains a protein similar to the Legionella pneumophila MIP gene-product. Mol Microbiol. 1991;5:109–115.
  • Rockey DD, Chesebro BB, Heinzen RA, et al. A 28 kDa major immunogen of Chlamydia psittaci shares identity with MIP proteins of Legionella spp and Chlamydia trachomatis - Cloning and characterization of the C-psittaci MIP-like gene. Microbiol-UK. 1996;142:945–953.
  • Horne SM, Kottom TJ, Nolan LK, et al. Decreased intracellular survival of an fkpA mutant of Salmonella typhimurium Copenhagen. Infect Immun. 1997;65:806–810.
  • Vogtherr M, Jacobs DM, Parac TN, et al. NMR solution structure and dynamics of the peptidylprolyl cis-trans isomerase domain of the trigger factor from Mycoplasma genitalium compared to FK506-binding protein. J Mol Biol. 2002;318:1097–1115.
  • Mo YY, Cianciotto NP, Mallavia LP. Molecular cloning of a Coxiella burnetii gene encoding a macrophage infectivity potentiator (Mip) analogue. Microbiol. 1995;141(Pt 11):2861–2871.
  • Cianciotto NP, Oconnell W, Dasch GA, et al. Detection of MIP-like sequences and MIP-related proteins within the Family Rickettsiaceae. Current Microbiol. 1995;30:149–153.
  • Hayano T, Takahashi N, Kato S, et al. 2 distinct forms of peptidylprolyl-cis-trans-isomerase are expressed separately in periplasmic and cytoplasmic compartments of Escherichia coli cells. Biochem. 1991;30:3041–3048.
  • Kim N, Weeks DL, Shin JM, et al. Proteins released by Helicobacter pylori in vitro. J Bacteriol. 2002;184:6155–6162.
  • Delpino MV, Comerci DJ, Ann Wagner M, et al. Differential composition of culture supernatants from wild-type Brucella abortus and its isogenic virB mutants. Arch Microbiol. 2009;191:571–581.
  • Kontinen VP, Sarvas M. The Prsa Lipoprotein is essential for protein secretion in Bacillus subtilis and sets a limit for high-level secretion. Mol Microbiol. 1993;8:727–737.
  • Dartigalongue C, Raina S. A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. Embo J. 1998;17:3968–3980.
  • Helbig JH, Luck PC, Steinert M, et al. Immunolocalization of the MIP protein of intracellularly and extracellularly grown Legionella pneumophila. Lett App Microbiol. 2001;32:83–88.
  • Tremillon N, Morello E, Llull D, et al. PpiA, a surface PPIase of the cyclophilin family in Lactococcus lactis. PLOS ONE. 2012;7:e33516.
  • Leuzzi R, Serino L, Scarselli M, et al. Ng-MIP, a surface-exposed lipoprotein of Neisseria gonorrhoeae, has a peptidyl-prolyl cis/trans isomerase (PPIase) activity and is involved in persistence in macrophages. Mol Microbiol. 2005;58:669–681.

* A paper describing the biological function of the gonococcal MIP protein, which is required for intracellular survival in human macrophages.

  • Engleberg NC, Carter C, Weber DR, et al. Dna sequence of Mip, a Legionella pneumophila gene associated with macrophage infectivity. Infect Immun. 1989;57:1263–1270.

** The first report of a Legionella gene associated with macrophage infectivity.

  • Cianciotto NP, Fields BS. Legionella pneumophila MIP gene potentiates intracellular infection of protozoa and human macrophages. Proc Natl Acad Sci USA. 1992;89:5188–5191.

* An important paper describing the requirement of MIP for Legionella virulence.

  • Wieland H, Faigle M, Lang F, et al. Regulation of the Legionella MIP promotor during infection of human monocytes. Fems Micro Letts. 2002;212:127–132.
  • Fischer G, Bang H, Ludwig B, et al. MIP protein of Legionella pneumophila exhibits peptidyl-prolyl-cis trans isomerase (PPlase) activity. Mol Microbiol. 1992;6:1375–1383.
  • Wintermeyer E, Ludwig B, Steinert M, et al. Influence of site-specifically altered Mip proteins on intracellular survival of Legionella pneumophila in eukaryotic cells. Infect Immun. 1995;63:4576–4583.
  • Bangsborg JM, Shand G, Pearlman E, et al. Cross-reactive Legionella antigens and the antibody response during infection. Apmis. 1991;99:854–865.
  • Oconnell WA, Bangsborg JM, Cianciotto NP. Characterization of a Legionella micdadei Mip mutant. Infect Immun. 1995;63:2840–2845.
  • Doyle RM, Steele TW, McLennan AM, et al. Sequence analysis of the mip gene of the soilborne pathogen Legionella longbeachae. Infect Immun. 1998;66:1492–1499.
  • Arakaki N, Higa F, Koide M, et al. Induction of apoptosis of human macrophages in vitro by Legionella longbeachae through activation of the caspase pathway. J Med Microbiol. 2002;51:159–168.
  • Neff L, Daher S, Muzzin P, et al. Molecular characterization and subcellular localization of macrophage infectivity potentiator, a Chlamydia trachomatis lipoprotein. J Bact. 2007;189:4739–4748.
  • Lundemose AG, Rouch DA, Birkelund S, et al. Chlamydia trachomatis Mip-like protein. Mol Microbiol. 1992;6:2539–2548.
  • Bas S, Neff L, Vuillet M, et al. The proinflammatory cytokine response to Chlamydia trachomatis elementary bodies in human macrophages is partly mediated by a lipoprotein, the macrophage infectivity potentiator, through TLR2/TLR1/TLR6 and CD14. J Immunol. 2008;180:1158–1168.
  • Herrmann M, Schuhmacher A, Muehldorfer I, et al. Identification and characterization of secreted effector proteins of Chlamydophila pneumoniae TW183. Res Microbiol. 2006;157:513–524.
  • Wang T, Chen JP, Li H, et al. Co-expression and immunity of Legionella pneumophila mip gene and immunoadjuvant ctxB gene. Acta Biochim et Biophys Sinica. 2005;37:199–204.
  • Seshu J, Mclvor KL, Mallavia LP. Antibodies are generated during infection to Coxiella burnetii macrophage infectivity potentiator protein (Cb-Mip). Microbiol Immun. 1997;41:371–376.
  • Xiong X, Meng Y, Wang X, et al. Mice immunized with bone marrow-derived dendritic cells stimulated with recombinant Coxiella burnetii Com1 and Mip demonstrate enhanced bacterial clearance in association with a Th1 immune response. Vaccine. 2012;30:6809–6815.
  • Xiong X, Qi Y, Jiao J, et al. Exploratory study on Th1 epitope-induced protective immunity against Coxiella burnetii infection. PLOS ONE. 2014;9:e87206.
  • Xiong X, Wang X, Wen B, et al. Potential serodiagnostic markers for Q fever identified in Coxiella burnetii by immunoproteomic and protein microarray approaches. BMC Microbiol. 2012;12:35.
  • Lu C, Peng B, Li Z, et al. Induction of protective immunity against Chlamydia muridarum intravaginal infection with the chlamydial immunodominant antigen macrophage infectivity potentiator. Microbes Infect. 2013;15:329–338.
  • Forsbach-Birk V, Foddis C, Simnacher U, et al. Profiling antibody responses to infections by Chlamydia abortus enables identification of potential virulence factors and candidates for serodiagnosis. PLOS ONE. 2013;8:e80310.
  • Marques PX, Souda P, O’Donovan J, et al. Identification of immunologically relevant proteins of Chlamydophila abortus using sera from experimentally infected pregnant ewes. Clin Vacc Immunol. 2010;17:1274–1281.
  • Sydenham M, Douce G, Bowe F, et al. Salmonella enterica serovar Typhimurium surA mutants are attenuated and effective live oral vaccines. Infect Immun. 2000;68:1109–1115.
  • Henningham A, Chiarot E, Gillen CM, et al. Conserved anchorless surface proteins as group A streptococcal vaccine candidates. J Mol Med-Jmm. 2012;90:1197–1207.
  • Starnino S, Leuzzi R, Ghisetti V, et al. Molecular analysis of two novel Neisseria gonorrhoeae virulent components: the macrophage infectivity potentiator and the outer membrane protein A. New Microbiol. 2010;33:167–170.
  • Echenique-Rivera H, Muzzi A, Del Tordello E, et al. Transcriptome analysis of Neisseria meningitidis in human whole blood and mutagenesis studies identify virulence factors involved in blood survival. PLoS Pathog. 2011;7:e10002027:18.
  • 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(Suppl 2):B87–B97.

* A paper summarizing the composition of the first-generation ‘universal’ MenB vaccine Bexsero®, a model for the development of vaccines using reverse vaccinology.

  • Bernfield L, Fletcher L, Howell A, et al. Identification of a novel vaccine candidate for group B Neisseria meningitidis. Thirteenth International Pathogenic Neisseria Conference; 2002; Oslo (Norway): National Institute of Public Health. p. 116.
  • Vogel U, Taha MK, Vazquez JA, et al. Predicted strain coverage of a meningococcal multicomponent vaccine (4CMenB) in Europe: a qualitative and quantitative assessment. Lancet Infect Dis. 2013;13:416–425.
  • Bettinger JA, Scheifele DW, Halperin SA, et al. Diversity of Canadian meningococcal serogroup B isolates and estimated coverage by an investigational meningococcal serogroup B vaccine (4CMenB). Vaccine. 2013;32:124–130.
  • Medini D, Stella M, Wassil J. MATS: Global coverage estimates for 4CMenB, a novel multicomponent meningococcal B vaccine. Vaccine. 2015;33:2629–2636.
  • Perez-Trallero E, Esnal O, Marimon JM. Progressive decrease in the potential usefulness of meningococcal serogroup B vaccine (4CMenB, Bexsero(R)) in Gipuzkoa, Northern Spain. PLOS ONE. 2014;9:e116024.
  • Mcneil LK, Zagursky RJ, Lin SL, et al. Role of Factor H binding protein in Neisseria meningitidis virulence and its potential as a vaccine candidate to broadly protect against meningococcal disease. Microbiol Mol Biol Rev. 2013;77:234–252.
  • Williams JN, Skipp PJ, Humphries HE, et al. Proteomic analysis of outer membranes and vesicles from wild-type serogroup B Neisseria meningitidis and a lipopolysaccharide-deficient mutant. Infect Immun. 2007;75:1364–1372.
  • Jolley KA, Maiden MC. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics. 2010;11:595.
  • Riboldi-Tunnicliffe A, Konig B, Jessen S, et al. Crystal structure of Mip, a prolylisomerase from Legionella pneumophila. Nat Struct Biol. 2001;8:779–783.

** A landmark paper describing the structure of Legionella pneumophila MIP; used as a template for structural modeling.

  • Ceymann A, Horstmann M, Ehses P, et al. Solution structure of the Legionella pneumophila Mip-rapamycin complex. BMC Struct Biol. 2008;8:17.
  • Bielecka MK, Devos N, Gilbert M, et al. Recombinant protein truncation strategy for inducing bactericidal antibodies to the macrophage infectivity potentiator protein of Neisseria meningitidis and circumventing potential cross-reactivity with human FK506-binding proteins. Infect Immun. 2015;83:730–742.

* An important paper that describes a protein truncation strategy that can be transferable to other MIP proteins in order to circumvent the possibility of cross-reactivity with human FKBP proteins.

  • Sampson BA, Gotschlich EC. Neisseria meningitidis encodes an Fk506-inhibitable rotamase. PNAS USA. 1992;89:1164–1168.
  • McAllister CF, Stephens DS. Analysis in Neisseria meningitidis and other Neisseria species of genes homologous to the FKBP immunophilin family. Mol Microbiol. 1993;10:13–23.
  • Dornan J, Taylor P, Walkinshaw MD. Structures of immunophilins and their ligand complexes. Curr Topics Med Chem. 2003;3:1392–1409.
  • Qin A, Scott DW, Rabideau MM, et al. Requirement of the CXXC motif of novel Francisella infectivity potentiator protein B FipB, and FipA in virulence of F. tularensis subsp. tularensis. PLOS ONE. 2011;6:e24611.
  • Myers GS, Parker D, Al-Hasani K, et al. Genome sequence and identification of candidate vaccine antigens from the animal pathogen Dichelobacter nodosus. Nat Biotechnol. 2007;25:569–575.
  • Unal C, Schwedhelm KF, Thiele A, et al. Collagen IV-derived peptide binds hydrophobic cavity of Legionella pneumophila MIP and interferes with bacterial epithelial transmigration. Cell Microbiol. 2011;13:1558–1572.
  • Biasini M, Bienert S, Waterhouse A, et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 2014;42:W252–W258.
  • Maeda T, Maeda H, Yamabe K, et al. Highly expressed genes in a rough-colony-forming phenotype of Aggregatibacter actinomycetemcomitans: implication of a mip-like gene for the invasion of host tissue. Fems Immun Med Microbiol. 2010;58:226–236.
  • Wong CYF, Heuzenroeder MW, Quinn DM, et al. Cloning and characterization of two immunophilin-like genes, ilpA and fkpA, on a single 3.9-kilobase fragment of Aeromonas hydrophila genomic DNA. J Bacteriol. 1997;179:3397–3403.
  • Humphreys S, Rowley G, Stevenson A, et al. Role of periplasmic peptidylprolyl isomerases in Salmonella enterica serovar typhimurium virulence. Infect Immun. 2003;71:5386–5388.
  • Ge X, Lyu ZX, Liu Y, et al. Identification of FkpA as a key quality control factor for the biogenesis of outer membrane proteins under heat shock conditions. J Bacteriol. 2014;196:672–680.
  • Long P, Sly L, Pham AV, et al. Characterization of Morococcus cerebrosus gen.nov.,sp.nov. and comparison with Neisseria mucosa. Int J System Bacteriol. 1981;31:294–301.
  • Wintermeyer E, Ludwig B, Steinert M, et al. Influence of site-specifically altered Mip proteins on intracellular survival of Legionella pneumophila in eukaryotic cells. Infect Immun. 1995;63:4576–4583.

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