Pseudomonas aeruginosa is one of the pathogenic bacteria which utilize binding of the host plasminogen (Plg) to promote their invasion throughout the host tissues. In the present study, we confirmed that P. aeruginosa exhibits binding affinity for human plasminogen. Furthermore, we showed that the protein detected on the cell wall of P. aeruginosa and binding human plasminogen is an enolase-like protein. The hypothesis that alpha-enolase, a cytoplasmatic glycolytic enzyme, resides also on the cell surface of the bacterium was supported by electron microscopy analysis. The plasminogen-binding activity of bacterial cell wall outer membrane enolase-like protein was examined by immunoblotting assay.

Department of Medical Biochemistry Wroclaw Medical University Chalubinskiego 10 50 368 Wroclaw Poland

Zobrazit více v PubMed

Agarwal S, Kulshreshtha P, Bambah Mukku D, Bhatnagar R. α-Enolase binds to human plasminogen on the surface of Bacillus anthracis. Biochim Biophys Acta. 2008;1784:986–994. doi: 10.1016/j.bbapap.2008.03.017. PubMed DOI

Bergmann S, Rohde M, Chhatwal GS, Hammerschmidt S. α-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol Microbiol. 2001;40:1273–1287. doi: 10.1046/j.1365-2958.2001.02448.x. PubMed DOI

Campbell WN, Hendrix E, Cryz S, Jr, Cross AS. Immunogenicity of a 24-valent Klebsiella capsular polysaccharide vaccine and an eight-valent Pseudomonas O-polysaccharide conjugate vaccine administered to victims of acute trauma. Clin Infect Dis. 1996;23:179–181. doi: 10.1093/clinids/23.1.179. PubMed DOI

Diaz-Ramos A, Roig-Borrellas A, Garcia-Melero A, Lopez-Alemany R. α-Enolase, amultifunctional protein: its role onpathophysiological situations. J Biomed Biotechnol. 2012;2012:156795. doi: 10.1155/2012/156795. PubMed DOI PMC

Doring G, Pier GB. Vaccines and immunotherapy against Pseudomonas aeruginosa. Vaccine. 2008;26:1011–1024. doi: 10.1016/j.vaccine.2007.12.007. PubMed DOI

Ge J, Catt DM, Gregory RL. Streptococcus mutans surface alpha-enolase binds salivary mucin MG2 and human plasminogen. Infect Immun. 2004;72:6748–6752. doi: 10.1128/IAI.72.11.6748-6752.2004. PubMed DOI PMC

Govan JR, Deretic V. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev. 1996;60:539–574. PubMed PMC

Hancock RE, Speert DP. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist Updat. 2000;3:247–255. doi: 10.1054/drup.2000.0152. PubMed DOI

Jo JT, Brinkman FS, Hancock RE. Aminoglycoside efflux in Pseudomonas aeruginosa: involvement of novel outer membrane proteins. Antimicrob Agents Chemother. 2003;47:1101–1111. doi: 10.1128/AAC.47.3.1101-1111.2003. PubMed DOI PMC

Kim DK, Kim JJ, Kim JH, Woo YM, Kim S, Yoon DW, Choi CS, Kim I, Park WJ, Lee N, Jung SB, Ahn BY, Nam SW, Yoon SM, Choi WJ. Comparison of two immunization schedules for a Pseudomonas aeruginosa outer membrane proteins vaccine in burn patients. Vaccine. 2000;19:1274–1283. doi: 10.1016/S0264-410X(00)00235-8. PubMed DOI

Kinloch A, Tatzer V, Wait R, Peston D, Lundberg K, Donatien P, Moyes D, Taylor PC, Venables PJ. Identification of citrullinated alpha-enolase as a candidate autoantigen in rheumatoid arthritis. Arthritis Res Ther. 2005;7:R1421–R1429. doi: 10.1186/ar1845. PubMed DOI PMC

Lang H. Outer membrane proteins as surface display systems. Int J Med Microbiol. 2000;290:579–585. doi: 10.1016/S1438-4221(00)80004-1. PubMed DOI

Larbig M, Mansouri E, Freihorst J, Tummler B, Kohler G, Domdey H, Knapp B, Hungerer KD, Hundt E, Gabelsberger J, von Specht BU. Safety and immunogenicity of an intranasal Pseudomonas aeruginosa hybrid outer membrane protein F-I vaccine in human volunteers. Vaccine. 2001;19:2291–2297. doi: 10.1016/S0264-410X(00)00550-8. PubMed DOI

Lin J, Huang S, Zhang Q. Outer membrane proteins: key players for bacterial adaptation in host niches. Microbes Infect. 2002;4:325–331. doi: 10.1016/S1286-4579(02)01545-9. PubMed DOI

Liu KJ, Shih NY. The role of enolase in tissue invasion and metastasis of pathogens and tumor cells. J Cancer Mol. 2007;3:45–48.

Lomholt JA, Poulsen K, Kilian M. Epidemic population structure of Pseudomonas aeruginosa: evidence for a clone that is pathogenic to the eye and that has a distinct combination of virulence factors. Infect Immun. 2001;69:6284–6295. doi: 10.1128/IAI.69.10.6284-6295.2001. PubMed DOI PMC

Lopez-Alemany R, Longstaff C, Hawley S, Mirshahi M, Fabregas P, Jardi M, Merton E, Miles LA, Felez J. Inhibition of cell surface mediated plasminogen activation by a monoclonal antibody against alpha-enolase. Am J Hematol. 2003;72:234–242. doi: 10.1002/ajh.10299. PubMed DOI

Mundodi V, Kucknoor AS, Alderete JF. Immunogenic and plasminogen-binding surface-associated alpha-enolase of Trichomonas vaginalis. Infect Immun. 2008;76:523–531. doi: 10.1128/IAI.01352-07. PubMed DOI PMC

Pancholi V. Multifunctional alpha-enolase: its role in diseases. Cell Mol Life Sci. 2001;58:902–920. doi: 10.1007/PL00000910. PubMed DOI PMC

Pancholi V, Fischetti VA. Alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J Biol Chem. 1998;273:14503–14515. doi: 10.1074/jbc.273.23.14503. PubMed DOI

Piast M, Kustrzeba-Wojcicka I, Matusiewicz M, Banas T. Molecular evolution of enolase. Acta Biochim Pol. 2005;52:507–513. PubMed

Seweryn E, Pietkiewicz J, Szamborska A, Gamian A. Enolase on the surface of prockaryotic and eukaryotic cells is a receptor for human plasminogen. Postepy Hig Med Dosw (Online) 2007;61:672–682. PubMed

Seweryn E, Pietkiewicz J, Bednarz-Misa IS, Ceremuga I, Saczko J, Kulbacka J, Gamian A. Localization of enolase in the subfractions of a breast cancer cell line. Z Naturforsch C. 2009;64:754–758. PubMed

Terrier B, Degand N, Guilpain P, Servettaz A, Guillevin L, Mouthon L. Alpha-enolase: a target of antibodies in infectious and autoimmune diseases. Autoimmun Rev. 2007;6:176–182. doi: 10.1016/j.autrev.2006.10.004. PubMed DOI

Whiting GC, Evans JT, Patel S, Gillespie SH. Purification of native alpha-enolase from Streptococcus pneumoniae that binds plasminogen and is immunogenic. J Med Microbiol. 2002;51:837–843. PubMed

Witkowska D, Pietkiewicz J, Szostko B, Danielewicz R, Maslowski L, Gamian A. Antibodies against human muscle enolase recognize a 45-kDa bacterial cell wall outer membrane enolase-like protein. FEMS Immunol Med Microbiol. 2005;45:53–62. doi: 10.1016/j.femsim.2005.01.005. PubMed DOI

Yavlovich A, Rechnitzer H, Rottem S. Alpha-enolase resides on the cell surface of Mycoplasma fermentans and binds plasminogen. Infect Immun. 2007;75:5716–5719. doi: 10.1128/IAI.01049-07. PubMed DOI PMC