Excreted cytoplasmic proteins contribute to pathogenicity in Staphylococcus aureus

Infection and Immunity

Volumn 84, Issue 6, 2016, Pages 1672-1681

  Ebner, Patrick ^a   Rinker, Janina ^a   Nguyen, Minh Thu ^a   Popella, Peter ^a   Nega, Mulugeta ^a   Luqman, Arif ^a   Schittek, Birgit ^a   Di Marco, Moreno ^a   Stevanovic, Stefan ^a   Götza, Friedrich ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOLYSIN; CYTOPLASM PROTEIN; FBAA ENZYME; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; UNCLASSIFIED DRUG; ADHESIN; FIBRONECTIN-BINDING PROTEINS, BACTERIAL; N ACETYLMURAMOYLALANINE AMIDASE; PROTEIN BINDING; SCLEROPROTEIN;

ARTICLE; BACTERIAL CELL; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL INVASION; CELL SURFACE; CONTROLLED STUDY; CYTOTOXICITY; GALLERIA MELLONELLA; HOST CELL; HUMAN; HUMAN CELL; INFECTION; INTERNALIZATION; MONOCYTE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; ANIMAL; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; KERATINOCYTE; LARVA; LEUKOCYTE; METABOLISM; MICROBIOLOGY; MOTH; SECRETION (PROCESS); SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TUMOR CELL LINE; VIRULENCE;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (PHOSPHORYLATING); HOST-PATHOGEN INTERACTIONS; HUMANS; KERATINOCYTES; LARVA; LEUKOCYTES; MOTHS; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; PROTEIN BINDING; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; SURVIVAL ANALYSIS; VIRULENCE;

EID: 84971504912     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00138-16     Document Type: Article

References (61)

1. Nickel W. 2003. The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem 270: 2109-2119.
2. Wang G, Chen H, Xia Y, Cui J, Gu Z, Song Y, Chen YQ, Zhang H, Chen W. 2013. How are the non-classically secreted bacterial proteins released into the extracellular milieu? Curr Microbiol 67:688-695. http://dx.doi.org/10.1007/s00284-013-0422-6.
3. Pancholi V, Fischetti VA. 1992. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J Exp Med 176: 415-426. http://dx.doi.org/10.1084/jem.176.2.415.
4. Pancholi V, Chhatwal GS. 2003. Housekeeping enzymes as virulence factors for pathogens. Int J Med Microbiol 293: 391-401. http://dx.doi.org/10.1078/1438-4221-00283.
5. D'Costa SS, Boyle MD. 2000. Interaction of group A streptococci with human plasmin(ogen) under physiological conditions. Methods 21: 165-177. http://dx.doi.org/10.1006/meth.2000.0988.
6. Lottenberg R, Broder CC, Boyle MD, Kain SJ, Schroeder BL, Curtiss R, III. 1992. Cloning, sequence analysis, and expression in Escherichia coli of a streptococcal plasmin receptor. J Bacteriol 174: 5204-5210.
7. Winram SB, Lottenberg R. 1996. The plasmin-binding protein Plr of group A streptococci is identified as glyceraldehyde-3-phosphate de-hydrogenase. Microbiology 142: 2311-2320. http://dx.doi.org/10.1099/13500872-142-8-2311.
8. Jin H, Song YP, Boel G, Kochar J, Pancholi V. 2005. Group A strepto-coccal surface GAPDH, SDH, recognizes uPAR/CD87 as its receptor on the human pharyngeal cell and mediates bacterial adherence to host cells. J Mol Biol 350: 27-41. http://dx.doi.org/10.1016/j.jmb.2005.04.063.
9. Madureira P, Baptista M, Vieira M, Magalhaes V, Camelo A, Oliveira L, Ribeiro A, Tavares D, Trieu-Cuot P, Vilanova M, Ferreira P. 2007. Streptococcus agalactiae GAPDH is a virulence-associated immunomodulatory protein. J Immunol 178: 1379-1387. http://dx.doi.org/10.4049/jimmunol.178.3.1379.
10. Oliveira L, Madureira P, Andrade EB, Bouaboud A, Morello E, Ferreira P, Poyart C, Trieu-Cuot P, Dramsi S. 2012. Group B streptococcus GAPDH is released upon cell lysis, associates with bacterial surface, and induces apoptosis in murine macrophages. PLoS One 7: e29963. http://dx.doi.org/10.1371/journal.pone.0029963.
11. Egea L, Aguilera L, Gimenez R, Sorolla MA, Aguilar J, Badia J, Baldoma L. 2007. Role of secreted glyceraldehyde-3-phosphate dehydrogenase in the infection mechanism of enterohemorrhagic and enteropathogenic Escherichia coli: interaction of the extracellular enzyme with human plasminogen and fibrinogen. Int J Biochem Cell Biol 39: 1190-1203. http://dx.doi.org/10.1016/j.biocel.2007.03.008.
12. Jeffery CJ. 1999. Moonlighting proteins. Trends Biochem Sci 24: 8-11. http://dx.doi.org/10.1016/S0968-0004(98)01335-8.
13. Henderson B, Martin A. 2013. Bacterial moonlighting proteins and bacterial virulence. Curr Top Microbiol Immunol 358: 155-213. http://dx.doi.org/10.1007/82_2011_188.
14. Sibbald MJ, Winter T, van der Kooi-Pol MM, Buist G, Tsompanidou E, Bosma T, Schafer T, Ohlsen K, Hecker M, Antelmann H, Engelmann S, van Dijl JM. 2010. Synthetic effects of secG and secY2 mutations on exoproteome biogenesis in Staphylococcus aureus. J Bacteriol 192: 3788-3800. http://dx.doi.org/10.1128/JB.01452-09.
15. Tjalsma H, Antelmann H, Jongbloed JD, Braun PG, Darmon E, Dorenbos R, Dubois JY, Westers H, Zanen G, Quax WJ, Kuipers OP, Bron S, Hecker M, van Dijl JM. 2004. Proteomics of protein secretion by Bacillus subtilis: separating the "secrets" of the secretome. Microbiol Mol Biol Rev 68: 207-233. http://dx.doi.org/10.1128/MMBR.68.2.207-233.2004.
16. Ziebandt AK, Becher D, Ohlsen K, Hacker J, Hecker M, Engelmann S. 2004. The influence of agr and crB in growth phase dependent regulation of virulence factors in Staphylococcus aureus. Proteomics 4: 3034-3047. http://dx.doi.org/10.1002/pmic.200400937.
17. Nega M, Dube L, Kull M, Ziebandt AK, Ebner P, Albrecht D, Krismer B, Rosenstein R, Hecker M, Götz F. 2015. Secretome analysis revealed adaptive and non-adaptive responses of the Staphylococcus carnosus femB mutant. Proteomics 15: 1268-1279. http://dx.doi.org/10.1002/pmic.201400343.
18. Pasztor L, Ziebandt AK, Nega M, Schlag M, Haase S, Franz-Wachtel M, Madlung J, Nordheim A, Heinrichs DE, Götz F. 2010. Staphylococcal major autolysin (Atl) is involved in excretion of cytoplasmic proteins. J Biol Chem 285: 36794-36803. http://dx.doi.org/10.1074/jbc.M110.167312.
19. Ebner P, Prax M, Nega M, Koch I, Dube L, Yu W, Rinker J, Popella P, Flötenmeyer M, Götz F. 2015. Excretion of cytoplasmic proteins (ECP) in Staphylococcus aureus. Mol Microbiol 97: 775-789. http://dx.doi.org/10.1111/mmi.13065.
20. Ling E, Feldman G, Portnoi M, Dagan R, Overweg K, Mulholland F, Chalifa-Caspi V, Wells J, Mizrachi-Nebenzahl Y. 2004. 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 138: 290-298. http://dx.doi.org/10.1111/j.1365-2249.2004.02628.x.
21. Tunio SA, Oldfield NJ, Berry A, Ala'Aldeen DA, Wooldridge KG, Turner DP. 2010. The moonlighting protein fructose-1, 6-bisphosphate aldolase of Neisseria meningitidis: surface localization and role in host cell adhesion. Mol Microbiol 76: 605-615. http://dx.doi.org/10.1111/j.1365-2958.2010.07098.x.
22. Fey PD, Endres JL, Yajjala VK, Widhelm TJ, Boissy RJ, Bose JL, Bayles KW. 2013. A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. mBio 4: e00537-12. http://dx.doi.org/10.1128/mBio.00537-12.
23. Cheng AG, DeDent AC, Schneewind O, Missiakas D. 2011. A play in four acts: Staphylococcus aureus abscess formation. Trends Microbiol 19: 225-232. http://dx.doi.org/10.1016/j.tim.2011.01.007.
24. Bae T, Schneewind O. 2006. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63. http://dx.doi.org/10.1016/j.plasmid.2005.05.005.
25. Geiger T, Francois P, Liebeke M, Fraunholz M, Goerke C, Krismer B, Schrenzel J, Lalk M, Wolz C. 2012. The stringent response of Staphylococcus aureus and its impact on survival after phagocytosis through the induction of intracellular PSMs expression. PLoS Pathog 8: e1003016. http://dx.doi.org/10.1371/journal.ppat.1003016.
26. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA, III, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6: 343-345. http://dx.doi.org/10.1038/nmeth.1318.
27. Monk IR, Shah IM, Xu M, Tan MW, Foster TJ. 2012. Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. mBio 3: e00277-11. http://dx.doi.org/10.1128/mBio.00277-11.
28. Biswas R, Voggu L, Simon UK, Hentschel P, Thumm G, Götz F. 2006. Activity of the major staphylococcal autolysin Atl. FEMS Microbiol Lett 259: 260-268. http://dx.doi.org/10.1111/j.1574-6968.2006.00281.x.
29. Heilmann C, Hussain M, Peters G, Götz F. 1997. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24: 1013-1024. http://dx.doi.org/10.1046/j.1365-2958.1997.4101774.x.
30. de Jonge BL, Chang YS, Gage D, Tomasz A. 1992. Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. The role of penicillin binding protein 2A. J Biol Chem 267:11248-11254.
31. Terrasse R, Amoroso A, Vernet T, Di Guilmi AM. 2015. Streptococcus pneumoniae GAPDH Is released by cell lysis and interacts with peptidoglycan. PLoS One 10: e0125377. http://dx.doi.org/10.1371/journal.pone.0125377.
32. Wu Y, Li Q, Chen XZ. 2007. Detecting protein-protein interactions by Far Western blotting. Nat Protoc 2: 3278-3284. http://dx.doi.org/10.1038/nprot.2007.459.
33. Kall L, Canterbury JD, Weston J, Noble WS, MacCoss MJ. 2007. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat Methods 4: 923-925. http://dx.doi.org/10.1038/nmeth1113.
34. Nguyen MT, Kraft B, Yu W, Demicrioglu DD, Hertlein T, Burian M, Schmaler M, Boller K, Bekeredjian-Ding I, Ohlsen K, Schittek B, Götz F. 2015. The vSaQ specific lipoprotein like cluster (lpl) of Staphylococcu saureus USA300 contributes to immune stimulation and invasion in human cells. PLoS Pathog 11: e1004984. http://dx.doi.org/10.1371/journal.ppat.1004984.
35. Yu W, Götz F. 2012. Cell wall antibiotics provoke accumulation of anchored mCherry in the cross wall of Staphylococcus aureus. PLoS One 7: e30076. http://dx.doi.org/10.1371/journal.pone.0030076.
36. Barlow M. 2009. What antimicrobial resistance has taught us about horizontal gene transfer. Methods Mol Biol 532: 397-411. http://dx.doi.org/10.1007/978-1-60327-853-9_23.
37. Mechler L, Herbig A, Paprotka K, Fraunholz M, Nieselt K, Bertram R. 2015. A novel point mutation promotes growth phase-dependent daptomycin tolerance in Staphylococcus aureus. Antimicrob Agents Chemother 59: 5366-5376. http://dx.doi.org/10.1128/AAC.00643-15.
38. Peleg AY, Jara S, Monga D, Eliopoulos GM, Moellering RC, Jr, Mylonakis E. 2009. Galleria mellonella as a model system to study Acineto-bacter baumannii pathogenesis and therapeutics. Antimicrob Agents Chemother 53: 2605-2609. http://dx.doi.org/10.1128/AAC.01533-08.
39. Olaru F, Jensen LE. 2010. Chemokine expression by human keratinocyte cell lines after activation of Toll-like receptors. Exp Dermatol 19: e314-e316. http://dx.doi.org/10.1111/j.1600-0625.2009.01026.x.
40. Weidenmaier C, McLoughlin RM, Lee JC. 2010. The zwitterionic cell wall teichoic acid of Staphylococcus aureus provokes skin abscesses in mice by a novel CD4+ T-cell-dependent mechanism. PLoS One 5: e13227. http://dx.doi.org/10.1371/journal.pone.0013227.
41. Blau K, Portnoi M, Shagan M, Kaganovich A, Rom S, Kafka D, Chalifa Caspi V, Porgador A, Givon-Lavi N, Gershoni JM, Dagan R, Mizrachi Nebenzahl Y. 2007. Flamingo cadherin: a putative host receptor for Strep-tococcus pneumoniae. J Infect Dis 195: 1828-1837. http://dx.doi.org/10.1086/518038.
42. Hirschhausen N, Schlesier T, Schmidt MA, Götz F, Peters G, Heilmann C. 2010. A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell Microbiol 12: 1746-1764. http://dx.doi.org/10.1111/j.1462-5822.2010.01506.x.
43. Götz F, Yu W, Dube L, Prax M, Ebner P. 2015. Excretion of cytosolic proteins (ECP) in bacteria. Int J Med Microbiol 305: 230-237. http://dx.doi.org/10.1016/j.ijmm.2014.12.021.
44. Jeffery CJ. 2003. Moonlighting proteins: old proteins learning new tricks. Trends Genet 19: 415-417. http://dx.doi.org/10.1016/S0168-9525(03)00167-7.
45. Sibbald MJ, Ziebandt AK, Engelmann S, Hecker M, de Jong A, Harmsen HJ, Raangs GC, Stokroos I, Arends JP, Dubois JY, van Dijl JM. 2006. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol Mol Biol Rev 70: 755-788. http://dx.doi.org/10.1128/MMBR.00008-06.
46. Trost M, Wehmhoner D, Karst U, Dieterich G, Wehland J, Jansch L. 2005. Comparative proteome analysis of secretory proteins from pathogenic and nonpathogenic Listeria species. Proteomics 5: 1544-1557. http://dx.doi.org/10.1002/pmic.200401024.
47. Xia XX, Han MJ, Lee SY, Yoo JS. 2008. Comparison of the extracellular proteomes of Escherichia coli B and K-12 strains during high cell density cultivation. Proteomics 8: 2089-2103. http://dx.doi.org/10.1002/pmic.200700826.
48. Li M, Rosenshine I, Tung SL, Wang XH, Friedberg D, Hew CL, Leung KY. 2004. Comparative proteomic analysis of extracellular proteins of enterohemorrhagic and enteropathogenic Escherichia coli strains and their ihf and ler mutants. Appl Environ Microbiol 70: 5274-5282. http://dx.doi.org/10.1128/AEM.70.9.5274-5282.2004.
49. Herbert S, Ziebandt AK, Ohlsen K, Schäfer T, Hecker M, Albrecht D, Novick R, Götz F. 2010. Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect Immun 78: 2877-2889. http://dx.doi.org/10.1128/IAI.00088-10.
50. Rosenstein R, Götz F. 2013. What distinguishes highly pathogenic staphylococci from mediumand non-pathogenic? Curr Top Microbiol Immunol 358:33-89. http://dx.doi.org/10.1007/82_2012_286.
51. Crowe JD, Sievwright IK, Auld GC, Moore NR, Gow NA, Booth NA. 2003. Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol Microbiol 47: 1637-1651. http://dx.doi.org/10.1046/j.1365-2958.2003.03390.x.
52. Puckett S, Trujillo C, Eoh H, Marrero J, Spencer J, Jackson M, Schnappinger D, Rhee K, Ehrt S. 2014. Inactivation of fructose-1,6-bisphosphate aldolase prevents optimal co-catabolism of glycolytic and gluconeogenic carbon substrates in Mycobacterium tuberculosis. PLoS Pathog 10: e1004144. http://dx.doi.org/10.1371/journal.ppat.1004144.
53. Rosenstein R, Nerz C, Biswas L, Resch A, Raddatz G, Schuster SC, Götz F. 2009. Genome analysis of the meat starter culture bacterium Staphyloicoccus carnosus TM300. Appl Environ Microbiol 75: 811-822. http://dx.doi.org/10.1128/AEM.01982-08.
54. Albrecht T, Raue S, Rosenstein R, Nieselt K, Götz F. 2012. Phylogeny of the staphylococcal major autolysin and its use in genus and species typing. J Bacteriol 194: 2630-2636. http://dx.doi.org/10.1128/JB.06609-11.
55. Götz F, Heilmann C, Stehle T. 2014. Functional and structural analysis of the major amidase (Atl) in Staphylococcus. Int J Med Microbiol 304: 156-163. http://dx.doi.org/10.1016/j.ijmm.2013.11.006.
56. Komatsuzawa H, Sugai M, Nakashima S, Yamada S, Matsumoto A, Oshida T, Suginaka H. 1997. Subcellular localization of the major autolysin, ATL and its processed proteins in Staphylococcus aureus. Microbiol Immunol 41: 469-479. http://dx.doi.org/10.1111/j.1348-0421.1997.tb01880.x.
57. Yamada S, Sugai M, Komatsuzawa H, Nakashima S, Oshida T, Matsumoto A, Suginaka H. 1996. An autolysin ring associated with cell separation of Staphylococcus aureus. J Bacteriol 178: 1565-1571.
58. Schlag M, Biswas R, Krismer B, Köhler T, Zoll S, Yu W, Schwarz H, Peschel A, Götz F. 2010. Role of staphylococcal wall teichoic acid in targeting the major autolysin Atl. Mol Microbiol 75: 864-873. http://dx.doi.org/10.1111/j.1365-2958.2009.07007.x.
59. Zoll S, Schlag M, Shkumatov AV, Rautenberg M, Svergun DI, Götz F, Stehle T. 2012. Ligand-binding properties and conformational dynamics of autolysin repeat domains in staphylococcal cell wall recognition. J Bacteriol 194: 3789-3802. http://dx.doi.org/10.1128/JB.00331-12.
60. Attia AS, Cassat JE, Aranmolate SO, Zimmerman LJ, Boyd KL, Skaar EP. 2013. Analysis of the Staphylococcus aureus abscess proteome identifies antimicrobial host proteins and bacterial stress responses at the hostpathogen interface. Pathog Dis 69: 36-48. http://dx.doi.org/10.1111/2049-632X.12063.
61. Kobayashi SD, Malachowa N, DeLeo FR. 2015. Pathogenesis of Staph-ylococcus aureus abscesses. Am J Pathol 185: 1518-1527. http://dx.doi.org/10.1016/j.ajpath.2014.11.030.