958
Views
16
CrossRef citations to date
0
Altmetric
Reviews

Streptococcus pneumoniae proteomics: determinants of pathogenesis and vaccine development

&

References

  • Watson DA, Musher DM, Jacobson JW, et al. A brief history of the pneumococcus in biomedical research: a panoply of scientific discovery. Clin Infect Dis. 1993;17(5):913–924.
  • Bogaert D, van Belkum BA, Sluijter M, et al. Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet. 2004;363(9424):1871–1872.
  • Henriques-Normark B, Tuomanen EI. The pneumococcus: epidemiology, microbiology, and pathogenesis. Cold Spring Harb Perspect Med. 2013;3(7):1–15.
  • Simell B, Auranen K, Kayhty H, et al. The fundamental link between pneumococcal carriage and disease. Expert Rev Vaccines. 2012;11(7):841–855.
  • Shak JR, Vidal JE, Klugman KP. Influence of bacterial interactions on pneumococcal colonization of the nasopharynx. Trends Microbiol. 2013;21(3):129–135.
  • Murphy TF, Bakaletz LO, Smeesters PR. Microbial interactions in the respiratory tract. Pediatr Infect Dis J. 2009;28(Suppl 10):S121–S126.
  • Welte T, Torres A, Nathwani D. Clinical and economic burden of community-acquired pneumonia among adults in Europe. Thorax. 2012;67(1):71–79.
  • Mook-Kanamori BB, Geldhoff M, van der Poll T, et al. Pathogenesis and pathophysiology of pneumococcal meningitis. Clin Microbiol Rev. 2011;24(3):557–591.
  • Janssens JP. Pneumonia in the elderly (geriatric) population. Curr Opin Pulm Med. 2005;11(3):226–230.
  • Blasi F, Mantero M, Santus P, et al. Understanding the burden of pneumococcal disease in adults. Clin Microbiol Infect. 2012;18(Suppl 5):7–14.
  • Butler JC, Dowell SF, Breiman RF. Epidemiology of emerging pneumococcal drug resistance: implications for treatment and prevention. Vaccine. 1998;16(18):1693–1697.
  • Balaji V, Thomas K, Joshi HH, et al. Increasing invasive disease due to penicillin resistant S. pneumoniae in India. Indian J Med Sci. 2008;62(12):492–495.
  • Torres A, Blasi F, Peetermans WE, et al. The aetiology and antibiotic management of community-acquired pneumonia in adults in Europe: a literature review. Eur J Clin Microbiol Infect Dis. 2014;33(7):1065–1079.
  • Gay K, Baughman W, Miller Y, et al. The emergence of Streptococcus pneumoniae resistant to macrolide antimicrobial agents: a 6-year population-based assessment. J Infect Dis. 2000;182(5):1417–1424.
  • Amezaga MR, Carter PE, Cash P, et al. Molecular epidemiology of erythromycin resistance in Streptococcus pneumoniae isolates from blood and noninvasive sites. J Clin Microbiol. 2002;40(9):3313–3318.
  • Jacobs MR, Felmingham D, Appelbaum PC, et al. The Alexander Project 1998–2000: susceptibility of pathogens isolated from community-acquired respiratory tract infection to commonly used antimicrobial agents. J Antimicrob Chemother. 2003;52(2):229–246.
  • File TM Jr. Clinical implications and treatment of multiresistant Streptococcus pneumoniae pneumonia. Clin Microbiol Infect. 2006;12(Suppl 3):31–41.
  • McDaniel LS, Swiatlo E. Pneumococcal disease: pathogenesis, treatment, and prevention. Infect Dis Clin Pract. 2004;12:93–98.
  • Crum NF, Barrozo CP, Chapman FA, et al. An outbreak of conjunctivitis due to a novel unencapsulated Streptococcus pneumoniae among military trainees. Clin Infect Dis. 2004;39(8):1148–1154.
  • Hyams C, Camberlein E, Cohen JM, et al. The Streptococcus pneumoniae capsule inhibits complement activity and neutrophil phagocytosis by multiple mechanisms. Infect Immun. 2010;78(2):704–715.
  • Song JY, Nahm MH, Moseley MA. Clinical implications of pneumococcal serotypes: invasive disease potential, clinical presentations, and antibiotic resistance. J Korean Med Sci. 2013;28(1):4–15.
  • Kadioglu A, Weiser JN, Paton JC, et al. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol. 2008;6(4):288–301.
  • WHO pneumococcal vaccines: WHO position paper - 2012. Wkly Epidemiol Rec. 2012;87:129–144.
  • Tyrrell GJ, Lovgren M, Chui N, et al. Serotypes and antimicrobial susceptibilities of invasive Streptococcus pneumoniae pre- and post-seven valent pneumococcal conjugate vaccine introduction in Alberta, Canada, 2000–2006. Vaccine. 2009;27(27):3553–3560.
  • Brueggemann AB, Griffiths DT, Meats E, et al. Clonal relationships between invasive and carriage Streptococcus pneumoniae and serotype- and clone-specific differences in invasive disease potential. J Infect Dis. 2003;187(9):1424–1432.
  • Steenhoff AP, Shah SS, Ratner AJ, et al. Emergence of vaccine-related pneumococcal serotypes as a cause of bacteremia. Clin Infect Dis. 2006;42(7):907–914.
  • Munoz-Almagro C, Jordan I, Gene A, et al. Emergence of invasive pneumococcal disease caused by nonvaccine serotypes in the era of 7-valent conjugate vaccine. Clin Infect Dis. 2008;46(2):174–182.
  • Kadioglu A, Cuppone AM, Trappetti C, et al. Sex-based differences in susceptibility to respiratory and systemic pneumococcal disease in mice. J Infect Dis. 2011;204(12):1971–1979.
  • Tettelin H, Nelson KE, Paulsen IT, et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science. 2001;293(5529):498–506.
  • Bricker AL, Camilli A. Transformation of a type 4 encapsulated strain of Streptococcus pneumoniae. FEMS Microbiol Lett. 1999;172(2):131–135.
  • Hoskins J, Alborn WE Jr., Arnold J, et al. Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol. 2001;183(19):5709–5717.
  • Lanie JA, Ng WL, Kazmierczak KM, et al. Genome sequence of Avery’s virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J. Bacteriol. 2007;189(1):38–51.
  • Williams TM, Loman NJ, Ebruke C, et al. Genome analysis of a highly virulent serotype 1 strain of Streptococcus pneumoniae from West Africa. PLoS ONE. 2012;7(10):e26742.
  • Choi SC, Parker J, Richards VP, et al. Draft genome sequence of an atypical strain of Streptococcus pneumoniae isolated from a respiratory infection. Genome Announc. 2014;2(4):e00822–e00814.
  • Bruckner R, Nuhn M, Reichmann P, et al. Mosaic genes and mosaic chromosomes-genomic variation in Streptococcus pneumoniae. Int J Med Microbiol. 2004;294(2–3):157–168.
  • Hakenbeck R, Balmelle N, Weber B, et al. Mosaic genes and mosaic chromosomes: intra- and interspecies genomic variation of Streptococcus pneumoniae. Infect Immun. 2001;69(4):2477–2486.
  • Shen K, Gladitz J, Antalis P, et al. Characterization, distribution, and expression of novel genes among eight clinical isolates of Streptococcus pneumoniae. Infect Immun. 2006;74(1):321–330.
  • Croucher NJ, Harris SR, Fraser C, et al. Rapid pneumococcal evolution in response to clinical interventions. Science. 2011;331(6016):430–434.
  • Bergmann S, Hammerschmidt S. Versatility of pneumococcal surface proteins. Microbiology. 2006;152(Pt 2):295–303.
  • Perez-Dorado I, Galan-Bartual S, Hermoso JA. Pneumococcal surface proteins: when the whole is greater than the sum of its parts. Mol Oral Microbiol. 2012;27(4):221–245.
  • Cash P. Investigating pathogen biology at the level of the proteome. Proteomics. 2011;11(15):3190–3202.
  • Cash P. Proteomic analysis of uropathogenic Escherichia coli. Expert Rev Proteomics. 2014;11(1):43–58.
  • Choi CW, Lee YG, Kwon SO, et al. Analysis of Streptococcus pneumoniae secreted antigens by immuno-proteomic approach. Diagn Microbiol Infect Dis. 2012;72(4):318–327.
  • Lee KJ, Bae SM, Lee MR, et al. Proteomic analysis of growth phase-dependent proteins of Streptococcus pneumoniae. Proteomics. 2006;6(4):1274–1282.
  • Bae SM, Yeon SM, Kim TS, et al. The effect of protein expression of Streptococcus pneumoniae by blood. J Biochem Mol Biol. 2006;39(6):703–708.
  • Lee MR, Bae SM, Kim TS, et al. Proteomic analysis of protein expression in Streptococcus pneumoniae in response to temperature shift. J Microbiol. 2006;44(4):375–382.
  • Cozzone AJ. Role of protein phosphorylation on serine/threonine and tyrosine in the virulence of bacterial pathogens. J Mol Microbiol Biotechnol. 2005;9(3–4):198–213.
  • Sholz R, Imami K, Scott NE, et al. Novel host proteins and signaling pathways in Enteropathogenic E. coli pathogenesis identified by global phosphoproteome analysis. Mol Cell Proteomics. 2015;14:1927–1945.
  • Sun X, Ge F, Xiao CL, et al. Phosphoproteomic analysis reveals the multiple roles of phosphorylation in pathogenic bacterium Streptococcus pneumoniae. J Proteome Res. 2010;9(1):275–282.
  • Reich M, Bosshard PP, Stark M, et al. Species identification of bacteria and fungi from solid and liquid culture media by MALDI-TOF mass spectrometry. J Bacteriol Parasitol. 2013;S5:002.
  • Panda A, Kurapati S, Samantaray JC, et al. MALDI-TOF mass spectrometry proteomic based identification of clinical bacterial isolates. Indian J Med Res. 2014;140(6):770–777.
  • Williamson YM, Moura H, Woolfitt AR, et al. Differentiation of Streptococcus pneumoniae conjunctivitis outbreak isolates by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Appl Environ Microbiol. 2008;74(19):5891–5897.
  • Malmstrom L, Malmstrom J, Aebersold R. Quantitative proteomics of microbes: principles and applications to virulence. Proteomics. 2011;11(15):2947–2956.
  • Sun X, Jia HL, Xiao CL, et al. Bacterial proteome of Streptococcus pneumoniae through multidimensional separations coupled with LC-MS/MS. OMICS. 2011;15(7–8):477–482.
  • Tikhomirova A, Kidd SP. Haemophilus influenzae and Streptococcus pneumoniae: living together in a biofilm. Pathog Dis. 2013;69(2):114–126.
  • Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358(9276):135–138.
  • Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15(2):167–193.
  • Cope EK, Goldstein-Daruech N, Kofonow JM, et al. Regulation of virulence gene expression resulting from Streptococcus pneumoniae and nontypeable Haemophilus influenzae interactions in chronic disease. PLoS ONE. 2011;6(12):e28523.
  • Allegrucci M, Hu FZ, Shen K, et al. Phenotypic characterization of Streptococcus pneumoniae biofilm development. J Bacteriol. 2006;188(7):2325–2335.
  • Allegrucci M, Sauer K. Characterization of colony morphology variants isolated from Streptococcus pneumoniae biofilms. J Bacteriol. 2007;189(5):2030–2038.
  • Sanchez CJ, Hurtgen BJ, Lizcano A, et al. Biofilm and planktonic pneumococci demonstrate disparate immunoreactivity to human convalescent sera. BMC Microbiol. 2011;11:245.
  • Paton JC, Berry AM, Lock RA. Molecular analysis of putative pneumococcal virulence proteins. Microb Drug Resist. 1997;3(1):1–10.
  • Berry AM, Ogunniyi AD, Miller DC, et al. Comparative virulence of Streptococcus pneumoniae strains with insertion-duplication, point, and deletion mutations in the pneumolysin gene. Infect Immun. 1999;67(2):981–985.
  • Rossjohn J, Gilbert RJ, Crane D, et al. The molecular mechanism of pneumolysin, a virulence factor from Streptococcus pneumoniae. J Mol Biol. 1998;284(2):449–461.
  • Mellroth P, Daniels R, Eberhardt A, et al. LytA, major autolysin of Streptococcus pneumoniae, requires access to nascent peptidoglycan. J Biol Chem. 2012;287(14):11018–11029.
  • Hirst RA, Sikand KS, Rutman A, et al. Relative roles of pneumolysin and hydrogen peroxide from Streptococcus pneumoniae in inhibition of ependymal ciliary beat frequency. Infect Immun. 2000;68(3):1557–1562.
  • Marriott HM, Mitchell TJ, Dockrell DH. Pneumolysin: a double-edged sword during the host-pathogen interaction. Curr Mol Med. 2008;8(6):497–509.
  • Paton JC, Lock RA, Hansman DJ. Effect of immunization with pneumolysin on survival time of mice challenged with Streptococcus pneumoniae. Infect Immun. 1983;40(2):548–552.
  • Oloo EO, Yethon JA, Ochs MM, et al. Structure-guided antigen engineering yields pneumolysin mutants suitable for vaccination against pneumococcal disease. J Biol Chem. 2011;286(14):12133–12140.
  • Douce G, Ross K, Cowan G, et al. Novel mucosal vaccines generated by genetic conjugation of heterologous proteins to pneumolysin (PLY) from Streptococcus pneumoniae. Vaccine. 2010;28(18):3231–3237.
  • Dintilhac A, Alloing G, Granadel C, et al. Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol Microbiol. 1997;25(4):727–739.
  • Sampson JS, O’Connor SP, Stinson AR, et al. Cloning and nucleotide sequence analysis of psaA, the Streptococcus pneumoniae gene encoding a 37-kilodalton protein homologous to previously reported Streptococcus sp. adhesins. Infect Immun. 1994;62(1):319–324.
  • Briles DE, Ades E, Paton JC, et al. Intranasal immunization of mice with a mixture of the pneumococcal proteins PsaA and PspA is highly protective against nasopharyngeal carriage of Streptococcus pneumoniae. Infect Immun. 2000;68(2):796–800.
  • Romero-Steiner S, Pilishvili T, Sampson JS, et al. Inhibition of pneumococcal adherence to human nasopharyngeal epithelial cells by anti-PsaA antibodies. Clin Diagn Lab Immunol. 2003;10(2):246–251.
  • Lawrence MC, Pilling PA, Epa VC, et al. The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein. Structure. 1998;6(12):1553–1561.
  • Johnston JW, Myers LE, Ochs MM, et al. Lipoprotein PsaA in virulence of Streptococcus pneumoniae: surface accessibility and role in protection from superoxide. Infect Immun. 2004;72(10):5858–5867.
  • Tseng HJ, McEwan AG, Paton JC, et al. Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect Immun. 2002;70(3):1635–1639.
  • Jedrzejas MJ. Pneumococcal virulence factors: structure and function. Microbiol Mol Biol Rev. 2001;65(2):187–207.
  • Zhang JR, Mostov KE, Lamm ME, et al. The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell. 2000;102(6):827–837.
  • Meri T, Amdahl H, Lehtinen MJ, et al. Microbes bind complement inhibitor factor H via a common site. PLoS Pathog. 2013;9(4):e1003308.
  • Smith BL, Hostetter MK. C3 as substrate for adhesion of Streptococcus pneumoniae. J Infect Dis. 2000;182(2):497–508.
  • Voss S, Hallstrom T, Saleh M, et al. The choline-binding protein PspC of Streptococcus pneumoniae interacts with the C-terminal heparin-binding domain of vitronectin. J Biol Chem. 2013;288(22):15614–15627.
  • Rosenow C, Ryan P, Weiser JN, et al. Contribution of novel choline-binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Mol Microbiol. 1997;25(5):819–829.
  • Yother J, White JM. Novel surface attachment mechanism of the Streptococcus pneumoniae protein PspA. J Bacteriol. 1994;176(10):2976–2985.
  • McDaniel LS, Ralph BA, McDaniel DO, et al. Localization of protection-eliciting epitopes on PspA of Streptococcus pneumoniae between amino acid residues 192 and 260. Microb Pathog. 1994;17(5):323–337.
  • Hollingshead SK, Becker R, Briles DE. Diversity of PspA: mosaic genes and evidence for past recombination in Streptococcus pneumoniae. Infect Immun. 2000;68(10):5889–5900.
  • Briles DE, Hollingshead SK, King J, et al. Immunization of humans with recombinant pneumococcal surface protein A (rPspA) elicits antibodies that passively protect mice from fatal infection with Streptococcus pneumoniae bearing heterologous PspA. J Infect Dis. 2000;182(6):1694–1701.
  • Nabors GS, Braun PA, Herrmann DJ, et al. Immunization of healthy adults with a single recombinant pneumococcal surface protein A (PspA) variant stimulates broadly cross-reactive antibodies to heterologous PspA molecules. Vaccine. 2000;18(17):1743–1754.
  • Shaper M, Hollingshead SK, Benjamin WH Jr, et al. PspA protects Streptococcus pneumoniae from killing by apolactoferrin, and antibody to PspA enhances killing of pneumococci by apolactoferrin [corrected]. Infect Immun. 2004;72(9):5031–5040.
  • Mukerji R, Mirza S, Roche AM, et al. Pneumococcal surface protein A inhibits complement deposition on the pneumococcal surface by competing with the binding of C-reactive protein to cell-surface phosphocholine. J Immunol. 2012;189(11):5327–5335.
  • McDaniel LS, McDaniel DO, Hollingshead SK, et al. Comparison of the PspA sequence from Streptococcus pneumoniae EF5668 to the previously identified PspA sequence from strain Rx1 and ability of PspA from EF5668 to elicit protection against pneumococci of different capsular types. Infect Immun. 1998;66(10):4748–4754.
  • Brittan JL, Buckeridge TJ, Finn A, et al. Pneumococcal neuraminidase A: an essential upper airway colonization factor for Streptococcus pneumoniae. Mol Oral Microbiol. 2012;27(4):270–283.
  • Manco S, Hernon F, Yesilkaya H, et al. Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis. Infect Immun. 2006;74(7):4014–4020.
  • Berry AM, Lock RA, Paton JC. Cloning and characterization of nanB, a second Streptococcus pneumoniae neuraminidase gene, and purification of the NanB enzyme from recombinant Escherichia coli. J Bacteriol. 1996;178(16):4854–4860.
  • Tong HH, Liu X, Chen Y, et al. Effect of neuraminidase on receptor-mediated adherence of Streptococcus pneumoniae to chinchilla tracheal epithelium. Acta Otolaryngol. 2002;122(4):413–419.
  • King SJ, Hippe KR, Gould JM, et al. Phase variable desialylation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol Microbiol. 2004;54(1):159–171.
  • Adamou JE, Heinrichs JH, Erwin AL, et al. Identification and characterization of a novel family of pneumococcal proteins that are protective against sepsis. Infect Immun. 2001;69(2):949–958.
  • Hamel J, Charland N, Pineau I, et al. Prevention of pneumococcal disease in mice immunized with conserved surface-accessible proteins. Infect Immun. 2004;72(5):2659–2670.
  • Rioux S, Neyt C, Di PE, et al. Transcriptional regulation, occurrence and putative role of the Pht family of Streptococcus pneumoniae. Microbiology. 2011;157(Pt 2):336–348.
  • Kallio A, Sepponen K, Hermand P, et al. Role of Pht proteins in attachment of Streptococcus pneumoniae to respiratory epithelial cells. Infect Immun. 2014;82(4):1683–1691.
  • Godfroid F, Hermand P, Verlant V, et al. Preclinical evaluation of the Pht proteins as potential cross-protective pneumococcal vaccine antigens. Infect Immun. 2011;79(1):238–245.
  • Bergmann S, Schoenen H, Hammerschmidt S. The interaction between bacterial enolase and plasminogen promotes adherence of Streptococcus pneumoniae to epithelial and endothelial cells. Int J Med Microbiol. 2013;303(8):452–462.
  • Kadioglu A, Brewin H, Hartel T, et al. Pneumococcal protein PavA is important for nasopharyngeal carriage and development of sepsis. Mol Oral Microbiol. 2010;25(1):50–60.
  • Noske N, Kammerer U, Rohde M, et al. Pneumococcal interaction with human dendritic cells: phagocytosis, survival, and induced adaptive immune response are manipulated by PavA. J Immunol. 2009;183(3):1952–1963.
  • Holmes AR, McNab R, Millsap KW, et al. The pavA gene of Streptococcus pneumoniae encodes a fibronectin-binding protein that is essential for virulence. Mol Microbiol. 2001;41(6):1395–1408.
  • Bergmann S, Rohde M, Hammerschmidt S. Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pneumoniae is a surface-displayed plasminogen-binding protein. Infect Immun. 2004;72(4):2416–2419.
  • Bergmann S, Rohde M, Preissner KT, et al. The nine residue plasminogen-binding motif of the pneumococcal enolase is the major cofactor of plasmin-mediated degradation of extracellular matrix, dissolution of fibrin and transmigration. Thromb Haemost. 2005;94(2):304–311.
  • Agarwal V, Hammerschmidt S, Malm S, et al. Enolase of Streptococcus pneumoniae binds human complement inhibitor C4b-binding protein and contributes to complement evasion. J Immunol. 2012;189(7):3575–3584.
  • Nouwens AS, Cordwell SJ, Larsen MR, et al. Complementing genomics with proteomics: the membrane subproteome of Pseudomonas aeruginosa PAO1. Electrophoresis. 2000;21(17):3797–3809.
  • Sabarth N, Lamer S, Zimny-Arndt U, et al. Identification of surface proteins of Helicobacter pylori by selective biotinylation, affinity purification, and two-dimensional gel electrophoresis. J Biol Chem. 2002;277(31):27896–27902.
  • Wizemann TM, Heinrichs JH, Adamou JE, et al. Use of a whole genome approach to identify vaccine molecules affording protection against Streptococcus pneumoniae infection. Infect Immun. 2001;69(3):1593–1598.
  • Maione D, Margarit I, Rinaudo CD, et al. Identification of a universal Group B streptococcus vaccine by multiple genome screen. Science. 2005;309(5731):148–150.
  • Morsczeck C, Prokhorova T, Sigh J, et al. Streptococcus pneumoniae: proteomics of surface proteins for vaccine development. Clin Microbiol Infect. 2008;14(1):74–81.
  • Ling E, Feldman G, Portnoi M, et al. Glycolytic enzymes associated with the cell surface of Streptococcus pneumoniae are antigenic in humans and elicit protective immune responses in the mouse. Clin Exp Immunol. 2004;138(2):290–298.
  • Gatlin CL, Pieper R, Huang ST, et al. Proteomic profiling of cell envelope-associated proteins from Staphylococcus aureus. Proteomics. 2006;6(5):1530–1549.
  • Cole JN, Ramirez RD, Currie BJ, et al. Surface analyses and immune reactivities of major cell wall-associated proteins of Group A Streptococcus. Infect Immun. 2005;73(5):3137–3146.
  • Rodriguez-Ortega MJ, Norais N, Bensi G, et al. Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat Biotechnol. 2006;24(2):191–197.
  • Severin A, Nickbarg E, Wooters J, et al. Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. J Bacteriol. 2007;189(5):1514–1522.
  • Olaya-Abril A, Jimenez-Munguia I, Gomez-Gascon L, et al. Identification of potential new protein vaccine candidates through pan-surfomic analysis of pneumococcal clinical isolates from adults. PLoS ONE. 2013;8(7):e70365.
  • Doro F, Liberatori S, Rodriguez-Ortega MJ, et al. Surfome analysis as a fast track to vaccine discovery: identification of a novel protective antigen for group B Streptococcus hyper-virulent strain COH1. Mol Cell Proteomics. 2009;8(7):1728–1737.
  • Kuehn MJ, Kesty NC. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005;19(22):2645–2655.
  • Mashburn-Warren LM, Whiteley M. Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol. 2006;61(4):839–846.
  • Bernadac A, Gavioli M, Lazzaroni JC, et al. Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol. 1998;180(18):4872–4878.
  • Ferrari G, Garaguso I, Adu-Bobie J, et al. Outer membrane vesicles from group B Neisseria meningitidis delta gna33 mutant: proteomic and immunological comparison with detergent-derived outer membrane vesicles. Proteomics. 2006;6(6):1856–1866.
  • Giuliani MM, Adu-Bobie J, Comanducci M, et al. A universal vaccine for serogroup B meningococcus. Proc Natl Acad Sci U S A. 2006;103(29):10834–10839.
  • Berlanda Scorza F, Doro F, Rodriguez-Ortega MJ, et al. Proteomics characterization of outer membrane vesicles from the extraintestinal pathogenic Escherichia coli DeltatolR IHE3034 mutant. Mol Cell Proteomics. 2008;7(3):473–485.
  • Lee EY, Choi DY, Kim DK, et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics. 2009;9:5425–5436.
  • Olaya-Abril A, Prados-Rosales R, McConnell MJ, et al. Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae. J Proteomics. 2014;106:46–60.
  • Moffitt KL, Gierahn TM, Lu YJ, et al. T(H)17-based vaccine design for prevention of Streptococcus pneumoniae colonization. Cell Host Microbe. 2011;9(2):158–165.
  • Moffitt KL, Malley R, Lu YJ. Identification of protective pneumococcal T(H)17 antigens from the soluble fraction of a killed whole cell vaccine. PLoS One. 2012;7(8):e43445.
  • Ogunniyi AD, Grabowicz M, Briles DE, et al. Development of a vaccine against invasive pneumococcal disease based on combinations of virulence proteins of Streptococcus pneumoniae. Infect Immun. 2007;75(1):350–357.
  • Davies DH, Liang X, Hernandez JE, et al. Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc Natl Acad Sci U S A. 2005;102(3):547–552.
  • Eyles JE, Unal B, Hartley MG, et al. Immunodominant Francisella tularensis antigens identified using proteome microarray. Proteomics. 2007;7(13):2172–2183.
  • Felgner PL, Kayala MA, Vigil A, et al. A Burkholderia pseudomallei protein microarray reveals serodiagnostic and cross-reactive antigens. Proc Natl Acad Sci U S A. 2009;106(32):13499–13504.
  • Kunnath-Velayudhan S, Salamon H, Wang HY, et al. Dynamic antibody responses to the Mycobacterium tuberculosis proteome. Proc Natl Acad Sci U S A. 2010;107(33):14703–14708.
  • Kruh-Garcia NA, Wolfe LM, Chaisson LH, et al. Detection of Mycobacterium tuberculosis peptides in the exosomes of patients with active and latent M. tuberculosis infection using MRM-MS. PLoS One. 2014;9(7):e103811.
  • Karlsson C, Malmstrom L, Aebersold R, et al. Proteome-wide selected reaction monitoring assays for the human pathogen Streptococcus pyogenes. Nat Commun. 2012;3:1301.
  • Lange V, Picotti P, Domon B, et al. Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol. 2008;4:222–235.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.