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Proteomic profile of dormancy within Staphylococcus epidermidis biofilms using iTRAQ and label-free strategies
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  • 作者:Virginia Carvalhais (1) (2)
    Nuno Cerca (1)
    Manuel Vilanova (3) (4)
    Rui Vitorino (2) (5)

    1. Centre of Biological Engineering (CEB)
    ; Laboratory of Research in Biofilms Ros谩rio Oliveira (LIBRO) ; University of Minho ; Campus de Gualtar ; 4710-057 ; Braga ; Portugal
    2. QOPNA
    ; Mass Spectrometry Center ; Department of Chemistry ; University of Aveiro ; 3810-193 ; Aveiro ; Portugal
    3. Instituto de Biologia Molecular e Celular (IBMC)
    ; Rua do Campo Alegre 83 ; Porto ; Portugal
    4. Instituto de Ci锚ncias Biom茅dicas Abel Salazar (ICBAS)
    ; University of Porto ; Rua de Rua de Jorge Viterbo Ferreira 228 ; 4050-313 ; Porto ; Portugal
    5. University of Aveiro
    ; Aveiro ; Portugal
  • 关键词:Carbonylation ; Dormancy ; emPAI ; iTRAQ ; Quantitative proteomics ; Staphylococcus epidermidis biofilm
  • 刊名:Applied Microbiology and Biotechnology
  • 出版年:2015
  • 出版时间:March 2015
  • 年:2015
  • 卷:99
  • 期:6
  • 页码:2751-2762
  • 全文大小:846 KB
  • 参考文献:1. Abdallah, C, Dumas-Gaudot, E, Renaut, J, Sergeant, K (2012) Gel-based and gel-free quantitative proteomics approaches at a glance. Int J Plant Genomics 2012: pp. 494-572 CrossRef
    2. Alves, RM, Vitorino, R, Padrao, AI, Moreira-Goncalves, D, Duarte, JA, Ferreira, RM, Amado, F (2013) iTRAQ-based quantitative proteomic analysis of submandibular glands from rats with STZ-induced hyperglycemia. J Biochem 153: pp. 209-220 CrossRef
    3. Asakura, H, Panutdaporn, N, Kawamoto, K, Igimi, S, Yamamoto, S, Makino, S (2007) Proteomic characterization of enterohemorrhagic Escherichia coli O157:H7 in the oxidation-induced viable but non-culturable state. Microbiol Immunol 51: pp. 875-881 CrossRef
    4. Ashburner, M, Ball, CA, Blake, JA, Botstein, D, Butler, H, Cherry, JM, Davis, AP, Dolinski, K, Dwight, SS, Eppig, JT, Harris, MA, Hill, DP, Issel-Tarver, L, Kasarskis, A, Lewis, S, Matese, JC, Richardson, JE, Ringwald, M, Rubin, GM, Sherlock, G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: pp. 25-29 CrossRef
    5. Balaban, NQ, Gerdes, K, Lewis, K, McKinney, JD (2013) A problem of persistence: still more questions than answers?. Nat Rev Microbiol 11: pp. 587-591 CrossRef
    6. Berghoff, BA, Konzer, A, Mank, NN, Looso, M, Rische, T, Forstner, KU, Kruger, M, Klug, G (2013) Integrative 鈥渙mics鈥?approach discovers dynamic and regulatory features of bacterial stress responses. PLoS Genet 9: CrossRef
    7. Bhatt, AN, Shukla, N, Aliverti, A, Zanetti, G, Bhakuni, V (2005) Modulation of cooperativity in Mycobacterium tuberculosis NADPH-ferredoxin reductase: cation-and pH-induced alterations in native conformation and destabilization of the NADP+-binding domain. Protein Sci 14: pp. 980-992 CrossRef
    8. Cain, JA, Solis, N, Cordwell, SJ (2013) Beyond gene expression: the impact of protein post-translational modifications in bacteria. J Proteomics 97: pp. 265-286 CrossRef
    9. Carvalhais, V, Franca, A, Cerca, F, Vitorino, R, Pier, GB, Vilanova, M, Cerca, N (2014) Dormancy within Staphylococcus epidermidis biofilms: a transcriptomic analysis by RNA-seq. Appl Microbiol Biotechnol 98: pp. 2585-2596 CrossRef
    10. Carvalhais, V, Franca, A, Pier, GB, Vilanova, M, Cerca, N, Vitorino, R (2015) Comparative proteomic and transcriptomic profile of Staphylococcus epidermidis biofilms grown in glucose-enriched medium. Talanta 132: pp. 705-712 CrossRef
    11. Cashel M, Gentry D, Hernandez V, Vinella D (1996) The stringent response. In: Neidhardt FC, Curtiss IIIR, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed) / Escherichia coli and / Salmonella: Cellular and Molecular Biology, 2nd edn. AMS Press, Washington DC, pp 1458鈥?496
    12. Cerca, N, Martins, S, Cerca, F, Jefferson, KK, Pier, GB, Oliveira, R, Azeredo, J (2005) Comparative assessment of antibiotic susceptibility of coagulase-negative staphylococci in biofilm versus planktonic culture as assessed by bacterial enumeration or rapid XTT colorimetry. J Antimicrob Chemother 56: pp. 331-336 CrossRef
    13. Cerca, N, Jefferson, KK, Oliveira, R, Pier, GB, Azeredo, J (2006) Comparative antibody-mediated phagocytosis of Staphylococcus epidermidis cells grown in a biofilm or in the planktonic state. Infect Immun 74: pp. 4849-4855 CrossRef
    14. Cerca, F, Andrade, F, Franca, A, Andrade, EB, Ribeiro, A, Almeida, AA, Cerca, N, Pier, G, Azeredo, J, Vilanova, M (2011) Staphylococcus epidermidis biofilms with higher proportions of dormant bacteria induce a lower activation of murine macrophages. J Med Microbiol 60: pp. 1717-1724 CrossRef
    15. Cerca, F, Franca, A, Perez-Cabezas, B, Carvalhais, V, Ribeiro, A, Azeredo, J, Pier, GB, Cerca, N, Vilanova, M (2014) Dormant bacteria within Staphylococcus epidermidis biofilms have low inflammatory properties and maintain tolerance to vancomycin and penicillin after entering planktonic growth. J Med Microbiol 63: pp. 1274-1283 CrossRef
    16. Conrad, CC, Choi, J, Malakowsky, CA, Talent, JM, Dai, R, Marshall, P, Gracy, RW (2001) Identification of protein carbonyls after two-dimensional electrophoresis. Proteomics 1: pp. 829-834 CrossRef
    17. Cucarella, C, Solano, C, Valle, J, Amorena, B, Lasa, I, Penades, JR (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183: pp. 2888-2896 CrossRef
    18. Cutinelli, C, Galdiero, F (1967) Ion-binding properties of the cell wall of Staphylococcus aureus. J Bacteriol 93: pp. 2022-2023
    19. Dalle-Donne, I, Carini, M, Orioli, M, Vistoli, G, Regazzoni, L, Colombo, G, Rossi, R, Milzani, A, Aldini, G (2009) Protein carbonylation: 2,4-dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids. Free Radic Biol Med 46: pp. 1411-1419 CrossRef
    20. Sousa, AR, Penalva, LO, Marcotte, EM, Vogel, C (2009) Global signatures of protein and mRNA expression levels. Mol BioSyst 5: pp. 1512-1526
    21. Dean, RT, Fu, S, Stocker, R, Davies, MJ (1997) Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 324: pp. 1-18
    22. Deng, X, Weerapana, E, Ulanovskaya, O, Sun, F, Liang, H, Ji, Q, Ye, Y, Fu, Y, Zhou, L, Li, J, Zhang, H, Wang, C, Alvarez, S, Hicks, LM, Lan, L, Wu, M, Cravatt, BF, He, C (2013) Proteome-wide quantification and characterization of oxidation-sensitive cysteines in pathogenic bacteria. Cell Host Microbe 13: pp. 358-370 CrossRef
    23. Donlan, RM (2001) Biofilms and device-associated infections. Emerg Infect Dis 7: pp. 277-281 CrossRef
    24. Dorr, T, Vulic, M, Lewis, K (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8: CrossRef
    25. Doyle, RJ, Matthews, TH, Streips, UN (1980) Chemical basis for selectivity of metal ions by the Bacillus subtilis cell wall. J Bacteriol 143: pp. 471-480
    26. Dunne, v, Burd, EM (1992) The effects of magnesium, calcium, EDTA, and pH on the in vitro adhesion of Staphylococcus epidermidis to plastic. Microbiol Immunol 36: pp. 1019-1027 CrossRef
    27. Fey, PD (2010) Modality of bacterial growth presents unique targets: how do we treat biofilm-mediated infections?. Curr Opin Microbiol 13: pp. 610-615 CrossRef
    28. Fey, PD, Olson, ME (2010) Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol 5: pp. 917-933 CrossRef
    29. Fozo, EM, Makarova, KS, Shabalina, SA, Yutin, N, Koonin, EV, Storz, G (2010) Abundance of type I toxin-antitoxin systems in bacteria: searches for new candidates and discovery of novel families. Nucleic Acids Res 38: pp. 3743-3759 CrossRef
    30. Franceschini, A, Szklarczyk, D, Frankild, S, Kuhn, M, Simonovic, M, Roth, A, Lin, J, Minguez, P, Bork, P, Mering, C, Jensen, LJ (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41: pp. D808-D815 CrossRef
    31. Gaupp, R, Ledala, N, Somerville, GA (2012) Staphylococcal response to oxidative stress. Front Cell Infect Microbiol 2: pp. 33 CrossRef
    32. Goeders, N, Melderen, L (2014) Toxin-antitoxin systems as multilevel interaction systems. Toxins (Basel) 6: pp. 304-324 CrossRef
    33. Groisman, EA, Hollands, K, Kriner, MA, Lee, EJ, Park, SY, Pontes, MH (2013) Bacterial Mg2+ homeostasis, transport, and virulence. Annu Rev Genet 47: pp. 625-646 CrossRef
    34. Guell, M, Yus, E, Lluch-Senar, M, Serrano, L (2011) Bacterial transcriptomics: what is beyond the RNA horiz-ome?. Nat Rev Microbiol 9: pp. 658-669 CrossRef
    35. Hall-Stoodley, L, Costerton, JW, Stoodley, P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2: pp. 95-108 CrossRef
    36. Heilmann, C, Hussain, M, Peters, G, Gotz, F (1997) Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 5: pp. 1013-1024 CrossRef
    37. Heim, S, Lleo, M, Bonato, B, Guzman, CA, Canepari, P (2002) The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J Bacteriol 184: pp. 6739-6745 CrossRef
    38. Hong, SH, Wang, X, O鈥機onnor, HF, Benedik, MJ, Wood, TK (2012) Bacterial persistence increases as environmental fitness decreases. Microb Biotechnol 5: pp. 509-522 CrossRef
    39. Ishihama, Y, Oda, Y, Tabata, T, Sato, T, Nagasu, T, Rappsilber, J, Mann, M (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: pp. 1265-1272 CrossRef
    40. Kanehisa, M, Goto, S, Kawashima, S, Okuno, Y, Hattori, M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32: pp. D277-D280 CrossRef
    41. Kaprelyants, AS, Gottschal, JC, Kell, DB (1993) Dormancy in non-sporulating bacteria. FEMS Microbiol Rev 10: pp. 271-285 CrossRef
    42. Keren, I, Shah, D, Spoering, A, Kaldalu, N, Lewis, K (2004) Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 186: pp. 8172-8180 CrossRef
    43. Kuhn, M, Szklarczyk, D, Pletscher-Frankild, S, Blicher, TH, Mering, C, Jensen, LJ, Bork, P (2014) STITCH 4: integration of protein-chemical interactions with user data. Nucleic Acids Res 42: pp. D401-D407 CrossRef
    44. Lasa, I, Penades, JR (2006) Bap: a family of surface proteins involved in biofilm formation. Res Microbiol 157: pp. 99-107 CrossRef
    45. Lellouche, J, Friedman, A, Lahmi, R, Gedanken, A, Banin, E (2012) Antibiofilm surface functionalization of catheters by magnesium fluoride nanoparticles. Int J Nanomedicine 7: pp. 1175-1188
    46. Leszczynska, D, Matuszewska, E, Kuczynska-Wisnik, D, Furmanek-Blaszk, B, Laskowska, E (2013) The formation of persister cells in stationary-phase cultures of Escherichia coli is associated with the aggregation of endogenous proteins. PLoS One 8: CrossRef
    47. Lewis, K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5: pp. 48-56 CrossRef
    48. Liebler, DC (2008) Protein damage by reactive electrophiles: targets and consequences. Chem Res Toxicol 21: pp. 117-128 CrossRef
    49. Mack, D, Siemssen, N, Laufs, R (1992) Parallel induction by glucose of ahderence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion. Infect Immun 60: pp. 2048-2057
    50. Maisonneuve, E, Castro-Camargo, M, Gerdes, K (2013) (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154: pp. 1140-1150 CrossRef
    51. Oliveros JC (2007) VENNY. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/
    52. Orman, MA, Brynildsen, MP (2013) Dormancy is not necessary or sufficient for bacterial persistence. Antimicrob Agents Chemother 57: pp. 3230-3239 CrossRef
    53. Otto, M (2012) Molecular basis of Staphylococcus epidermidis infections. Semin Immunopathol 34: pp. 201-214 CrossRef
    54. Otto, M (2013) Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu Rev Med 64: pp. 175-188 CrossRef
    55. Otto, M (2014) Staphylococcus epidermidis pathogenesis. Methods Mol Biol 1106: pp. 17-31 CrossRef
    56. Park, PW, Rosenbloom, J, Abrams, WR, Rosenbloom, J, Mecham, RP (1996) Molecular cloning and expression of the gene for elastin-binding protein (ebpS) in Staphylococcus aureus. J Biol Chem 271: pp. 15803-15809 CrossRef
    57. Piddington, DL, Kashkouli, A, Buchmeier, NA (2000) Growth of Mycobacterium tuberculosis in a defined medium is very restricted by acid pH and Mg2+ levels. Infect Immun 68: pp. 4518-4522 CrossRef
    58. Pinto D, Santos MA, Chambel L (2013) Thirty years of viable but nonculturable state research: Unsolved molecular mechanisms. Crit Rev Microbiol聽41:61鈥?6
    59. Potrykus, K, Cashel, M (2008) (p)ppGpp: still magical?. Annu Rev Microbiol 62: pp. 35-51 CrossRef
    60. Qin, Z, Ou, Y, Yang, L, Zhu, Y, Tolker-Nielsen, T, Molin, S, Qu, D (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153: pp. 2083-2092 CrossRef
    61. Robinson, CE, Keshavarzian, A, Pasco, DS, Frommel, TO, Winship, DH, Holmes, EW (1999) Determination of protein carbonyl groups by immunoblotting. Anal Biochem 266: pp. 48-57 CrossRef
    62. 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: pp. 1883-1895 CrossRef
    63. Ross, PL, Huang, YN, Marchese, JN, Williamson, B, Parker, K, Hattan, S, Khainovski, N, Pillai, S, Dey, S, Daniels, S, Purkayastha, S, Juhasz, P, Martin, S, Bartlet-Jones, M, He, F, Jacobson, A, Pappin, DJ (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3: pp. 1154-1169 CrossRef
    64. Sadovskaya, I, Vinogradov, E, Li, J, Jabbouri, S (2004) Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus epidermidis RP62A, a reference biofilm-positive strain. Carbohydr Res 339: pp. 1467-1473 CrossRef
    65. Sadovskaya, I, Vinogradov, E, Flahaut, S, Kogan, G, Jabbouri, S (2005) Extracellular carbohydrate-containing polymers of a model biofilm-producing strain, Staphylococcus epidermidis RP62A. Infect Immun 73: pp. 3007-3017 CrossRef
    66. Sanchez, R, Riddle, M, Woo, J, Momand, J (2008) Prediction of reversibly oxidized protein cysteine thiols using protein structure properties. Protein Sci 17: pp. 473-481 CrossRef
    67. Sayed, N, Nonin-Lecomte, S, Rety, S, Felden, B (2012) Functional and structural insights of a Staphylococcus aureus apoptotic-like membrane peptide from a toxin-antitoxin module. J Biol Chem 287: pp. 43454-43463 CrossRef
    68. Sonenshein, AL (2005) CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol 8: pp. 203-207 CrossRef
    69. Song, B, Leff, LG (2006) Influence of magnesium ions on biofilm formation by Pseudomonas fluorescens. Microbiol Res 161: pp. 355-361 CrossRef
    70. Stewart, PS, Franklin, MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6: pp. 199-210 CrossRef
    71. Straub, L (2011) Beyond the transcripts: what controls protein variation?. PLoS Biol 9: CrossRef
    72. Thompson, A, Schafer, J, Kuhn, K, Kienle, S, Schwarz, J, Schmidt, G, Neumann, T, Johnstone, R, Mohammed, AK, Hamon, C (2003) Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 75: pp. 1895-1904 CrossRef
    73. Unterholzner, SJ, Poppenberger, B, Rozhon, W (2013) Toxin-antitoxin systems: Biology, identification, and application. Mob Genet Elements 3: CrossRef
    74. Verstraeten, N, Fauvart, M, Versees, W, Michiels, J (2011) The universally conserved prokaryotic GTPases. Microbiol Mol Biol Rev 75: pp. 507-542 CrossRef
    75. Vitorino, R, Guedes, S, Manadas, B, Ferreira, R, Amado, F (2012) Toward a standardized saliva proteome analysis methodology. J Proteomics 75: pp. 5140-5165 CrossRef
    76. Vuong, C, Kocianova, S, Voyich, JM, Yao, Y, Fischer, ER, DeLeo, FR, Otto, M (2004) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279: pp. 54881-54886 CrossRef
    77. Wakamoto, Y, Dhar, N, Chait, R, Schneider, K, Signorino-Gelo, F, Leibler, S, McKinney, JD (2013) Dynamic persistence of antibiotic-stressed mycobacteria. Science 339: pp. 91-95 CrossRef
    78. Wang, R, Khan, BA, Cheung, GY, Bach, TH, Jameson-Lee, M, Kong, KF, Queck, SY, Otto, M (2011) Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. J Clin Invest 121: pp. 238-248 CrossRef
    79. Williamson, KS, Richards, LA, Perez-Osorio, AC, Pitts, B, McInnerney, K, Stewart, PS, Franklin, MJ (2012) Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. J Bacteriol 194: pp. 2062-2073 CrossRef
    80. Zhang, W, Li, F, Nie, L (2010) Integrating multiple 鈥榦mics鈥?analysis for microbial biology: application and methodologies. Microbiology 156: pp. 287-301 CrossRef
  • 刊物类别:Chemistry and Materials Science
  • 刊物主题:Chemistry
    Biotechnology
    Microbiology
    Microbial Genetics and Genomics
  • 出版者:Springer Berlin / Heidelberg
  • ISSN:1432-0614
文摘
Staphylococcus epidermidis is an important nosocomial bacterium among carriers of indwelling medical devices, since it has a strong ability to form biofilms. The presence of dormant bacteria within a biofilm is one of the factors that contribute to biofilm antibiotic tolerance and immune evasion. Here, we provide a detailed characterization of the quantitative proteomic profile of S. epidermidis biofilms with different proportions of dormant bacteria. A total of 427 and 409 proteins were identified by label-free and label-based quantitative methodologies, respectively. From these, 29 proteins were found to be differentially expressed between S. epidermidis biofilms with prevented and induced dormancy. Proteins overexpressed in S. epidermidis with prevented dormancy were associated with ribosome synthesis pathway, which reflects the metabolic state of dormant bacteria. In the opposite, underexpressed proteins were related to catalytic activity and ion binding, with involvement in purine, arginine, and proline metabolism. Additionally, GTPase activity seems to be enhanced in S. epidermidis biofilm with induced dormancy. The role of magnesium in dormancy modulation was further investigated with bioinformatics tool based in predicted interactions. The main molecular function of proteins, which strongly interact with magnesium, was nucleic acid binding. Different proteomic strategies allowed to obtain similar results and evidenced that prevented dormancy led to an expression of a markedly different repertoire of proteins in comparison to the one of dormant biofilms.

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