IsdC from Staphylococcus lugdunensis induces biofilm formation under low-iron growth conditions

Infection and Immunity

Volumn 82, Issue 6, 2014, Pages 2448-2459

  Missineo, Antonino ^a,d   Poto, Antonella Di ^a   Geoghegan, Joan A ^b   Rindi, Simonetta ^a   Heilbronner, Simon ^b   Gianotti, Valentina ^a   Arciola, Carla Renata ^c   Foster, Timothy J ^b   Speziale, Pietro ^a   Pietrocola, Giampiero ^a  

^a Section of Biochemistry   (Italy)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d IRBM   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IRON; ISDC PROTEIN; MEMBRANE PROTEIN; PERIODATE; PROTEINASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; CULTURE MEDIUM; RECOMBINANT PROTEIN;

ADHERENT CELL; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIUM ISOLATE; BACTERIUM MUTANT; BIOACCUMULATION; BIOFILM; CELL AGGREGATION; COAGULASE NEGATIVE STAPHYLOCOCCUS; CONTROLLED STUDY; ENZYME DEGRADATION; GENE LOCUS; GENE MUTATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAPHYLOCOCCUS LUGDUNENSIS; WESTERN BLOTTING; WILD TYPE; ANALYSIS OF VARIANCE; BACTERIUM ADHERENCE; CHEMISTRY; CULTURE MEDIUM; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; STAPHYLOCOCCUS INFECTION;

ANALYSIS OF VARIANCE; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; BLOTTING, WESTERN; CARRIER PROTEINS; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; IRON; RECOMBINANT PROTEINS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS LUGDUNENSIS;

EID: 84900460587     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01542-14     Document Type: Article

References (47)

1. Götz F. 2002. Staphylococcus and biofilms. Mol. Microbiol. 43:1367-1378. http://dx.doi.org/10.1046/j.1365-2958.2002.02827.x.
2. Stewart PS, Costerton JW. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358:135-138. http://dx.doi.org/10.1016/S0140-6736(01)05321-1.
3. Vuong C, Voyich JM, Fischer ER, Braughton KR, Whitney AR, DeLeo FR, Otto M. 2004. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell. Microbiol. 6:269-275. http://dx.doi.org/10.1046/j.1462-5822.2004.00367.x.
4. Bose JL, Lehman MK, Fey PD, Bayles KW. 2012. Contribution of the Staphylococcus aureus Atl AM and GL murein hydrolase activities in cell division, autolysis, and biofilm formation. PLoS One 7:e42244. http://dx.doi.org/10.1371/journal.pone.0042244.
5. Houston P, Rowe SE, Pozzi C, Waters EM, O'Gara JP. 2011. Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect. Immun. 79:1153-1165. http://dx.doi.org/10.1128/IAI.00364-10.
6. Vaudaux PE, François P, Proctor RA, McDevitt D, Foster TJ, Albrecht RM, Lew DP, Wabers H, Cooper SL. 1995. Use of adhesion-defective mutants of Staphylococcus aureus to define the role of specific plasma proteins in promoting bacterial adhesion to canine arteriovenous shunts. Infect. Immun. 63:585-590.
7. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Götz F. 1996. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol. 20:1083-1091. http://dx.doi.org/10.1111/j.1365-2958.1996.tb02548.x.
8. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penadés JR. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183:2888-2896. http://dx.doi.org/10.1128/JB.183.9.2888-2896.2001.
9. Geoghegan JA, Corrigan RM, Gruszka DT, Speziale P, O'Gara JP, Potts JR, Foster TJ. 2010. Role of surface protein SasG in biofilm formation by Staphylococcus aureus. J. Bacteriol. 192:5663-5673. http://dx.doi.org/10.1128/JB.00628-10.
10. Schroeder K, Jularic M, Horsburgh SM, Hirschhausen N, Neumann C, Bertling A, Schulte A, Foster S, Kehrel BE, Peters G, Heilmann C. 2009. Molecular characterization of a novel Staphylococcus aureus surface protein (SasC) involved in cell aggregation and biofilm accumulation. PLoS One 4:e7567. http://dx.doi.org/10.1371/journal.pone.0007567.
11. Merino N, Toledo-Arana A, Vergara-Irigaray M, Valle J, Solano C, Calvo E, Lopez JA, Foster TJ, Penadés JR, Lasa I. 2009. Protein A-mediated multicellular behavior in Staphylococcus aureus. J. Bacteriol. 191: 832-843. http://dx.doi.org/10.1128/JB.01222-08.
12. O'Neill E, Pozzi C, Houston P, Humphreys H, Robinson DA, Loughman A, Foster TJ, O'Gara JP. 2008. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and Fn-BPB. J. Bacteriol. 190:3835-3850. http://dx.doi.org/10.1128/JB.00167-08.
13. Geoghegan JA, Monk IR, O'Gara JP, Foster TJ. 2013. Subdomains N2N3 of fibronectin binding protein A mediate Staphylococcus aureus biofilm formation and adherence to fibrinogen using distinct mechanisms. J. Bacteriol. 195:2675-2683. http://dx.doi.org/10.1128/JB.02128-12.
14. Rohde H, Burdelski C, Bartscht K, Hussain M, Buck F, Horstkotte MA, Knobloch JK, Heilmann C, Herrmann M, Mack D. 2005. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol. Microbiol. 55:1883-1895. http://dx.doi.org/10.1111/j.1365-2958.2005.04515.x.
15. Banner MA, Cunniffe JG, Macintosh RL, Foster TJ, Rohde H, Mack D, Hoyes E, Derrick J, Upton M, Handley PS. 2007. Localized tufts of fibrils on Staphylococcus epidermidis NCTC 11047 are comprised of the accumulation-associated protein. J. Bacteriol. 189:2793-2804. http://dx.doi.org/10.1128/JB.00952-06.
16. Shahrooei M, Hira V, Stijlemans B, Merckx R, Hermans PW, Van Eldere J. 2009. Inhibition of Staphylococcus epidermidis biofilm formation by rabbit polyclonal antibodies against the SesC protein. Infect. Immun. 77:3670-3678. http://dx.doi.org/10.1128/IAI.01464-08.
17. Freney J, Brun Y, Bes M, Meugnier H, Grimont F, Grimont PAD, Nervi C, Fleurette J. 1988. Staphylococcus lugdunensis sp. nov. and Staphylococcus schleiferi sp. nov., two species from human clinical specimens. Int. J. Syst. Bacteriol. 38:168-172. http://dx.doi.org/10.1099/00207713-38-2-168.
18. Vandenesch F, Etienne J, Reverdy ME, Eykyn SJ. 1993. Endocarditis due to Staphylococcus lugdunensis: report of 11 cases and review. Clin. Infect. Dis. 17:871-876.
19. Patel R, Piper KE, Rouse MS, Uhl JR, Cockerill FR, III, Steckelberg JM. 2000. Frequency of isolation of Staphylococcus lugdunensis among staphylococcal isolates causing endocarditis: a 20-year experience. J. Clin. Microbiol. 38:4262-4263.
20. Anguera I, Del Río A, Miró JM, Matínez-Lacasa X, Marco F, Gumá JR, Quaglio G, Claramonte X, Moreno A, Mestres CA, Mauri E, Azqueta M, Benito N, García-de la María C, Almela M, Jiménez-Expósito, Sued MJO, De Lazzari E, Gatell JM. 2005. Staphylococcus lugdunensis infective endocarditis: description of 10 cases and analysis of native valve, prosthetic valve, and pacemaker lead endocarditis clinical profiles. Heart 91: e10. http://dx.doi.org/10.1136/hrt.2004.040659.
21. Ebright JR, Penugonda N, Brown W. 2004. Clinical experience with Staphylococcus lugdunensis bacteremia: a retrospective analysis. Diagn. Microbiol. Infect. Dis. 48:17-21. http://dx.doi.org/10.1016/j.diagmicrobio.2003.08.008.
22. Sampathkumar P, Osmon DR, Cockerill FR. 2000. Prosthetic joint infection due to Staphylococcus lugdunensis. Mayo Clin. Proc. 75:511-512. http://dx.doi.org/10.1016/S0025-6196(11)64220-1.
23. Sandoe JA, Longshaw CM. 2001. Ventriculoperitoneal shunt infection caused by Staphylococcus lugdunensis. Clin. Microbiol. Infect. 7:385-387. http://dx.doi.org/10.1046/j.1198-743x.2001.00268.x.
24. Frank KL, Patel R. 2007. Poly-N-acetylglucosamine is not a major component of the extracellular matrix in biofilms formed by icaADBCpositive Staphylococcus lugdunensis isolates. Infect. Immun. 75:4728-4742. http://dx.doi.org/10.1128/IAI.00640-07.
25. Geoghegan JA, Ganesh VK, Smeds E, Liang X, Höök M, Foster TJ. 2010. Molecular characterization of the interaction of staphylococcal microbial surface components recognizing adhesive matrix molecules (MSCRAMM) ClfA and Fbl with fibrinogen. J. Biol. Chem. 285:6208-6216. http://dx.doi.org/10.1074/jbc.M109.062208.
26. Szabados F, Marlinghaus L, Korte M, Neumann S, Kaase M, Gatermann SG. 2011. Fbl is not involved in the invasion of eukaryotic epithelial and endothelial cells by Staphylococcus lugdunensis. FEMS Microbiol. Lett. 324:48-55. http://dx.doi.org/10.1111/j.1574-6968.2011.02382.x.
27. Nilsson M, Bjerketorp J, Wiebensjö A, Ljungh A, Frykberg L, Guss B. 2004. A von Willebrand factor-binding protein from Staphylococcus lugdunensis. FEMS Microbiol. Lett. 234:155-161. http://dx.doi.org/10.1111/j.1574-6968.2004.tb09527.x.
28. Heilbronner S, Holden MT, van Tonder A, Geoghegan JA, Foster TJ, Parkhill J, Bentley SD. 2011. Genome sequence of Staphylococcus lugdunensis N920143 allows identification of putative colonization and virulence factors. FEMS Microbiol. Lett. 322:60-67. http://dx.doi.org/10.1111/j.1574-6968.2011.02339.x.
29. Zapotoczna M, Heilbronner S, Speziale P, Foster TJ. 2012. Ironregulated surface determinant (Isd) proteins of Staphylococcus lugdunensis. J. Bacteriol. 194:6453-6467. http://dx.doi.org/10.1128/JB.01195-12.
30. Haley KP, Janson EM, Heilbronner S, Foster TJ, Skaar EP. 2011. Staphylococcus lugdunensis IsdG liberates iron from host heme. J. Bacteriol. 193:4749-4757. http://dx.doi.org/10.1128/JB.00436-11.
31. Clarke SR, Mohamed R, Bian L, Routh AF, Kokai-Kun JF, Mond JJ, Tarkowski A, Foster SJ. 2007. The Staphylococcus aureus surface protein IsdA mediates resistance to innate defenses of human skin. Cell Host Microbe 1:199-212. http://dx.doi.org/10.1016/j.chom.2007.04.005.
32. Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67:5427-5433.
33. Muller E, Takeda S, Shiro H, Goldmann D, Pier GB. 1993. Occurrence of capsular polysaccharide/adhesin among clinical isolates of coagulasenegative staphylococci. J. Infect. Dis. 168:1211-1218. http://dx.doi.org/10.1093/infdis/168.5.1211.
34. Heilbronner S, Hanses F, Monk IR, Speziale P, Foster TJ. 2013. Sortase A promotes virulence in experimental Staphylococcus lugdunensis endocarditis. Microbiology 159:2141-2152.
35. Corrigan RM, Foster TJ. 2009. An improved tetracycline-inducible expression vector for Staphylococcus aureus. Plasmid 61:126-129. http://dx.doi.org/10.1016/j.plasmid.2008.10.001.
36. Li MZ, Elledge SJ. 2007. Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat. Methods 4:251-256. http://dx.doi.org/10.1038/nmeth1010.
37. Li MZ, Elledge SJ. 2012. SLIC: a method for sequence-and ligationindependent cloning. Methods Mol. Biol. 852:51-59. http://dx.doi.org/10.1007/978-1-61779-564-0_5.
38. Bahey-El-Din M, Griffin BT, Gahan CG. 2008. Nisin inducible production of listeriolysin O in Lactococcus lactis NZ9000. Microb. Cell Fact 7:24. http://dx.doi.org/10.1186/1475-2859-7-24.
39. Monk IR, Casey PG, Hill C, Gahan CG. 2010. Directed evolution and targeted mutagenesis to murinize Listeria monocytogenes internalin A for enhanced infectivity in the murine oral infection model. BMC Microbiol. 10:318. http://dx.doi.org/10.1186/1471-2180-10-318.
40. Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF, Melton DM, Beachey EH. 1985. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J. Clin. Microbiol. 22:996-1006.
41. Chaignon P, Sadovskaya I, Ragunah Ch Ramasubbu N, Kaplan JB, Jabbouri S. 2007. Susceptibility of staphylococcal biofilms to enzymatic treatments depends on their chemical composition. Appl. Microbiol. Biotechnol. 75:125-132. http://dx.doi.org/10.1007/s00253-006-0790-y.
42. Izano EA, Amarante MA, Kher WB, Kaplan JB. 2008. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl. Environ. Microbiol. 74:470-476. http://dx.doi.org/10.1128/AEM.02073-07.
43. Schwartz K, Syed AK, Stephenson RE, Rickard AH, Boles BR. 2012. Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms. PLoS Pathog. 8:e1002744. http://dx.doi.org/10.1371/journal.ppat.1002744.
44. Shahrooei M, Hira V, Khodaparast L, Khodaparast L, Stijlemans B, Kucharíková S, Burghout P, Hermans PW, Van Eldere J. 2012. Vaccination with SesC decreases Staphylococcus epidermidis biofilm formation. Infect. Immun. 80:3660-3668. http://dx.doi.org/10.1128/IAI.00104-12.
45. Vergara-Irigaray M, Valle J, Merino N, Latasa C, García B, Ruiz de Los Mozos I, Solano C, Toledo-Arana A, Penadés JR, Lasa I. 2009. Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilmassociated foreign-body infections. Infect. Immun. 77:3978-3991. http://dx.doi.org/10.1128/IAI.00616-09.
46. Conrady DG, Wilson JJ, Herr AB. 2013. Structural basis for Zn2+-dependent intercellular adhesion in staphylococcal biofilms. Proc. Natl. Acad. Sci. U. S. A. 110:E202-E211. http://dx.doi.org/10.1073/pnas.1208134110.
47. Gruszka DT, Wojdyla JA, Bingham RJ, Turkenburg JP, Manfield IW, Steward A, Leech AP, Geoghegan JA, Foster TJ, Clarke J, Potts JR. 2012. Staphylococcal biofilm-forming protein has a contiguous rod-like structure. Proc. Natl. Acad. Sci. U. S. A. 109:E1011-E1018. http://dx.doi.org/10.1073/pnas.1119456109.