NMR analysis of a stress response metabolic signaling network

Journal of Proteome Research

Volumn 10, Issue 8, 2011, Pages 3743-3754

  Zhang, Bo ^a   Halouska, Steven ^a   Schiaffo, Charles E ^a   Sadykov, Marat R ^a   Somerville, Greg A ^a   Powers, Robert ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

bioinformatics; central metabolism; metabolomics; NMR; stress response

Indexed keywords

ALCOHOL; AUTOINDUCER 2; GLUCOSE; HYDROLASE; IRON; SODIUM CHLORIDE; TETRACYCLINE; TRICARBOXYLIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL METABOLISM; BIOFILM; CITRIC ACID CYCLE; METABOLOME; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; STAPHYLOCOCCUS EPIDERMIDIS; STRESS;

BIOFILMS; CITRIC ACID CYCLE; METABOLOME; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PRINCIPAL COMPONENT ANALYSIS; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS EPIDERMIDIS;

STAPHYLOCOCCUS EPIDERMIDIS;

EID: 79961235661     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200360w     Document Type: Article

References (74)

1. Brent, R. Cell signaling: What is the signal and what information does it carry? FEBS Lett. 2009, 583 (24) 4019-4024
2. Jorgensen, C.; Linding, R. Simplistic pathways or complex networks? Curr. Opin. Genet. Dev. 2010, 20 (1) 15-22
3. Kholodenko, B. N. Spatially distributed cell signaling FEBS Lett. 2009, 583 (24) 4006-4012
4. Scott, J. D.; Pawson, T. Cell signaling in space and time: Where proteins come together and when they're apart Science 2009, 326 (5957) 1220-1224
5. Mascher, T.; Helmann, J. D.; Unden, G. Stimulus perception in bacterial signal-transducing histidine kinases Microbiol. Mol. Biol. Rev. 2006, 70 (4) 910-938 (Pubitemid 44958261)
6. Gill, S. R.; Fouts, D. E.; Archer, G. L.; Mongodin, E. F.; DeBoy, R. T.; Ravel, J.; Paulsen, I. T.; Kolonay, J. F.; Brinkac, L.; Beanan, M.; Dodson, R. J.; Daugherty, S. C.; Madupu, R.; Angiuoli, S. V.; Durkin, A. S.; Haft, D. H.; Vamathevan, J.; Khouri, H.; Utterback, T.; Lee, C.; Dimitrov, G.; Jiang, L.; Qin, H.; Weidman, J.; Tran, K.; Kang, K.; Hance, I. R.; Nelson, K. E.; Fraser, C. M. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Streptococcus epidermidis strain J. Bacteriol. 2005, 187 (7) 2426-2438 (Pubitemid 40389140)
7. Novick, R. P.; Geisinger, E. Quorum sensing in staphylococci Annu. Rev. Genet. 2008, 42 (1) 541-564
8. Reznikoff, W. S.; Siegele, D. A.; Cowing, D. W.; Gross, C. A. The regulation of transcription initiation in bacteria Annu. Rev. Genet. 1985, 19, 355-87
9. Wu, S.; de, L. H.; Tomasz, A. Sigma-B, a putative operon encoding alternate sigma factor of Staphylococcus aureus RNA polymerase: molecular cloning and DNA sequencing J. Bacteriol. 1996, 178 (20) 6036-6042 (Pubitemid 26337791)
10. B operon in Staphylococcus aureus J. Bacteriol. 2005, 187 (23) 8006-8019 (Pubitemid 41691694)
11. Somerville, G. A.; Proctor, R. A. At the crossroads of bacterial metabolism and virulence factor synthesis in Staphylococci Microbiol. Mol. Biol. Rev. 2009, 73 (2) 233-248
12. Lloyd, D. The tricarboxylic acid cycle Process. Biochem. 1966, 1 (9) 465-469
13. Bae, T.; Banger, A. K.; Wallace, A.; Glass, E. M.; Aslund, F.; Schneewind, O.; Missiakas, D. M. Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (33) 12312-12317 (Pubitemid 39145440)
14. Begun, J.; Sifri, C. D.; Goldman, S.; Calderwood, S. B.; Ausubel, F. M. Staphylococcus aureus virulence factors identified by using a high-throughput Caenorhabditis elegans -killing model Infect. Immun. 2005, 73 (2) 872-7 (Pubitemid 40165745)
15. Coulter, S. N.; Schwan, W. R.; Ng, E. Y.; Langhorne, M. H.; Ritchie, H. D.; Westbrock-Wadman, S.; Hufnagle, W. O.; Folger, K. R.; Bayer, A. S.; Stover, C. K. Staphylococcus aureus genetic loci impacting growth and survival in multiple infection environments Mol. Microbiol. 1998, 30 (2) 393-404 (Pubitemid 28480189)
16. Sadykov, M. R.; Olson, M. E.; Halouska, S.; Zhu, Y.; Fey, P. D.; Powers, R.; Somerville, G. A. Tricarboxylic acid cycle-dependent regulation of Staphylococcus epidermidis polysaccharide intercellular adhesin synthesis J. Bacteriol. 2008, 190 (23) 7621-7632
17. Cramton, S. E.; Gerke, C.; Schnell, N. F.; Nichols, W. W.; Gotz, F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation Infect. Immun. 1999, 67 (10) 5427-5433 (Pubitemid 29455321)
18. Maira-Litran, T.; Kropec, A.; Abeygunawardana, C.; Joyce, J.; Mark, G., 3rd; Goldmann, D. A.; Pier, G. B. Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide Infect. Immun. 2002, 70 (8) 4433-40 (Pubitemid 34790954)
19. Rupp, M. E.; Ulphani, J. S.; Fey, P. D.; Bartscht, K.; Mack, D. Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model Infect. Immun. 1999, 67 (5) 2627-2632 (Pubitemid 29200530)
20. Rupp, M. E.; Ulphani, J. S.; Fey, P. D.; Mack, D. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model Infect. Immun. 1999, 67 (5) 2656-2659 (Pubitemid 29200536)
21. Fitzpatrick, F.; Humphreys, H.; O'Gara, J. P. The genetics of staphylococcal biofilm formation - will a greater understanding of pathogenesis lead to better management of device-related infection? Clin. Microbiol. Infect. 2005, 11 (12) 967-973 (Pubitemid 41748930)
22. Vuong, C.; Kidder, J. B.; Jacobson, E. R.; Otto, M.; Proctor, R. A.; Somerville, G. A. Staphylococcus epidermidis polysaccharide intercellular adhesin production significantly increases during tricarboxylic acid cycle stress J. Bacteriol. 2005, 187 (9) 2967-2973 (Pubitemid 40571588)
23. Sadykov, M. R.; Zhang, B.; Halouska, S.; Nelson, J. L.; Kreimer, L. W.; Zhu, Y.; Powers, R.; Somerville, G. A. Using NMR metabolomics to investigate tricarboxylic acid cycle dependent signal transduction in Staphylococcus epidermidis J. Biol. Chem. 2010, 285 (47) 36616-36624
24. Knobloch, J. K. M.; Bartscht, K.; Sabottke, A.; Rohde, H.; Feucht, H.-H.; Mack, D. Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: Differential activation mechanisms due to ethanol and salt stress J. Bacteriol. 2001, 183 (8) 2624-2633 (Pubitemid 32249772)
25. Campbell, I. M.; Crozier, D. N.; Pawagi, A. B.; Buivids, I. A. In vitro response of Staphylococcus aureus from cystic fibrosis patients to combinations of linoleic and oleic acids added to nutrient medium J. Clin. Microbiol. 1983, 18 (2) 408-415 (Pubitemid 13075289)
26. Mack, D.; Siemssen, N.; Laufs, R. Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion Infect. Immun. 1992, 60 (5) 2048-2057
27. Gerke, C.; Kraft, A.; Sussmuth, R.; Schweitzer, O.; Gotz, F. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin J. Biol. Chem. 1998, 273 (29) 18586-18593 (Pubitemid 28334789)
28. Rachid, S.; Ohlsen, K.; Witte, W.; Hacker, J.; Ziebuhr, W. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis Antimicrob. Agents Chemother. 2000, 44 (12) 3357-3363 (Pubitemid 33009495)
29. Cramton, S. E.; Ulrich, M.; Gotz, F.; Doring, G. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis Infect. Immun. 2001, 69 (6) 4079-4085 (Pubitemid 32493332)
30. Deighton, M.; Borland, R. Regulation of slime production in Staphylococcus epidermidis by iron limitation Infect. Immun. 1993, 61 (10) 4473-4479 (Pubitemid 23298612)
31. Elci, S.; Atmaca, S.; Gul, K. Effect of iron limitation on the amount of slime produced by strains of Staphylococcus epidermidis Cytobios 1995, 84 (338-339) 141-146
32. Evans, E.; Brown, M. R. W.; Gilbert, P. Iron chelator, exopolysaccharide and protease production in Staphylococcus epidermidis: a comparative study of the effects of specific growth rate in biofilm and planktonic culture Microbiology 1994, 140 (1) 153-157 (Pubitemid 24067321)
33. B is involved in regulation of biofilm expression in a Staphylococcus aureus mucosal isolate J. Bacteriol. 2000, 182 (23) 6824-6826 (Pubitemid 32249268)
34. Zhao, L.; Xue, T.; Shang, F.; Sun, H.; Sun, B. Staphylococcus aureus AI-2 quorum sensing associates with the KdpDE two-component system to regulate capsular polysaccharide synthesis and virulence Infect. Immun. 2010, 78 (8) 3506-3515
35. Forgue, P.; Halouska, S.; Werth, M.; Xu, K.; Harris, S.; Powers, R. NMR metabolic profiling of aspergillus nidulans to monitor drug and protein activity J. Proteome Res. 2006, 5 (8) 1916-1923 (Pubitemid 44232704)
36. Halouska, S.; Chacon, O.; Fenton, R. J.; Zinniel, D. K.; Barletta, R. G.; Powers, R. Use of NMR metabolomics to analyze the targets of D-cycloserine in mycobacteria: role of D-alanine racemase J. Proteome Res. 2007, 6 (12) 4608-4614
37. Werth, M. T.; Halouska, S.; Shortridge, M. D.; Zhang, B.; Powers, R. Analysis of metabolomic pca data using tree diagrams Anal. Biochem. 2010, 399 (1) 56-63
38. Lindon, J. C.; Holmes, E.; Nicholson, J. K. Pattern recognition methods and applications in biomedical magnetic resonance Prog. Nucl. Magn. Reson. Spectrosc. 2001, 39 (1) 40
39. Stoyanova, R.; Brown, T. R. NMR spectral quantitation by principal component analysis NMR Biomed 2001, 14 (4) 271-277 (Pubitemid 32611439)
40. Killcoyne, S.; Carter, G. W.; Smith, J.; Boyle, J. Cytoscape: a community-based framework for network modeling Methods Mol. Biol. 2009, 563, 219-239
41. Cao, J. G.; Meighen, E. A. Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi J. Biol. Chem. 1989, 264 (36) 21670-21676 (Pubitemid 20028734)
42. Semmelhack, M. F.; Campagna, S. R.; Federle, M. J.; Bassler, B. L. An Expeditious Synthesis of DPD and Boron Binding Studies Org. Lett. 2005, 7 (4) 569-572 (Pubitemid 40353443)
43. Nguyen, B. D.; Meng, X.; Donovan, K. J.; Shaka, A. J. SOGGY: solvent-optimized double gradient spectroscopy for water suppression. A comparison with some existing techniques J. Magn. Reson. 2007, 184 (2) 263-274 (Pubitemid 46177673)
44. Palmer, A. G., III; Cavanagh, J.; Wright, P. E.; Rance, M. J. Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy J. Magn. Reson. 1991, 93 (1) 20
45. Kay, L. E.; Keifer, P.; Saarinen, T. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J. Am. Chem. Soc. 1992, 114 (26) 3
46. Bax, A; Davis, D. G. MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy J. Magn. Reson. 1985, 65, 6
47. Piotto, M.; Saudek, V.; Sklenar, V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions J. Biomol. NMR 1992, 2 (6) 661-665
48. Halouska, S.; Powers, R. Negative impact of noise on the principal component analysis of NMR data J. Magn. Reson. 2006, 178 (1) 88-95 (Pubitemid 41774015)
49. Johnson, B. A. Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol. Biol. 2004, 278, 313-352
50. Xia, J.; Bjorndahl, T. C.; Tang, P.; Wishart, D. S. Metabominer-semi- automated identification of metabolites from 2D NMR spectra of complex biofluids BMC Bioinform. 2008, 9, 507
51. Cui, Q.; Lewis, I. A.; Hegeman, A. D.; Anderson, M. E.; Li, J.; Schulte, C. F.; Westler, W. M.; Eghbalnia, H. R.; Sussman, M. R.; Markley, J. L. Metabolite identification via the Madison Metabolomics Consortium Database Nat. Biotechnol. 2008, 26 (2) 162-4 (Pubitemid 351225941)
52. Ulrich, E. L.; Akutsu, H.; Doreleijers, J. F.; Harano, Y.; Ioannidis, Y. E.; Lin, J.; Livny, M.; Mading, S.; Maziuk, D.; Miller, Z.; Nakatani, E.; Schulte, C. F.; Tolmie, D. E.; Kent, W. R.; Yao, H.; Markley, J. L. BioMagResBank Nucleic Acids Res. 2008, 36 (Database Iss) D402-D408
53. Wishart, D. S.; Knox, C.; Guo, A. C.; Eisner, R.; Young, N.; Gautam, B.; Hau, D. D.; Psychogios, N.; Dong, E.; Bouatra, S.; Mandal, R.; Sinelnikov, I.; Xia, J.; Jia, L.; Cruz, J. A.; Lim, E.; Sobsey, C. A.; Shrivastava, S.; Huang, P.; Liu, P.; Fang, L.; Peng, J.; Fradette, R.; Cheng, D.; Tzur, D.; Clements, M.; Lewis, A.; De, S. A.; Zuniga, A.; Dawe, M.; Xiong, Y.; Clive, D.; Greiner, R.; Nazyrova, A.; Shaykhutdinov, R.; Li, L.; Vogel, H. J.; Forsythe, I. HMDB: a knowledge-base for the human metabolome Nucleic Acids Res. 2009, 37 (Database Iss) D603-D610
54. Kanehisa, M.; Araki, M.; Goto, S.; Hattori, M.; Hirakawa, M.; Itoh, M.; Katayama, T.; Kawashima, S.; Okuda, S.; Tokimatsu, T.; Yamanishi, Y. KEGG for linking genomes to life and the environment Nucleic Acids Res. 2008, 36 (Database Iss) D480-D484
55. Caspi, R.; Altman, T.; Dale, J. M.; Dreher, K.; Fulcher, C. A.; Gilham, F.; Kaipa, P.; Karthikeyan, A. S.; Kothari, A.; Krummenacker, M.; Latendresse, M.; Mueller, L. A.; Paley, S.; Popescu, L.; Pujar, A.; Shearer, A. G.; Zhang, P.; Karp, P. D. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases Nucleic Acids Res. 2010, 38 (Database Iss) D473-D479
56. van den Berg, R. A.; Hoefsloot, H. C.; Westerhuis, J. A.; Smilde, A. K.; van der Werf, M. J. Centering, scaling, and transformations: improving the biological information content of metabolomics data BMC Genomics 2006, 7, 142
57. Somerville, G. A.; Chaussee, M. S.; Morgan, C. I.; Fitzgerald, J. R.; Dorward, D. W.; Reitzer, L. J.; Musser, J. M. Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival Infect. Immun. 2002, 70 (11) 6373-6382 (Pubitemid 35192730)
58. Mack, D.; Becker, P.; Chatterjee, I.; Dobinsky, S.; Knobloch, J. K. M.; Peters, G.; Rohde, H.; Herrmann, M. Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: Functional molecules, regulatory circuits, and adaptive responses Int. J. Med. Microbiol. 2004, 294 (2-3) 203-212 (Pubitemid 39281051)
59. Collins, F. M.; Lascelles, J. The effect of growth conditions on oxidative and dehydrogenase activity in Staphylococcus aureus J. Gen. Microbiol. 1962, 29, 531-535
60. Costerton, J. W.; Stewart, P. S.; Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections Science 1999, 284 (5418) 1318-1322 (Pubitemid 29289651)
61. Kornmann, H.; Duboc, P.; Niederberger, P.; Marison, I.; von Stockar, U. Influence of residual ethanol concentration on the growth of Gluconacetobacter xylinus I 2281 Appl. Microbiol. Biotechnol. 2003, 62 (2-3) 168-173 (Pubitemid 36995168)
62. Throup, J. P.; Zappacosta, F.; Lunsford, R. D.; Annan, R. S.; Carr, S. A.; Lonsdale, J. T.; Bryant, A. P.; McDevitt, D.; Rosenberg, M.; Burnham, M. K. The srhSR gene pair from Staphylococcus aureus: genomic and proteomic approaches to the identification and characterization of gene function Biochemistry 2001, 40 (34) 10392-10401 (Pubitemid 32800146)
63. Tomlins, R. I.; Pierson, M. D.; Ordal, Z. J. Effect of thermal injury on the TCA cycle enzymes of Staphylococcus aureus MF 31 and Salmonella typhimurium 7136 Can. J. Microbiol. 1971, 17 (6) 759-765
64. Miller, M. B.; Bassler, B. L. Quorum sensing in bacteria Annu. Rev. Microbiol. 2001, 55, 165-199 (Pubitemid 32978104)
65. Lim, Y.; Jana, M.; Luong, T. T.; Lee, C. Y. Control of glucose- and NaCl-induced biofilm formation by rbf in Staphylococcus aureus J. Bacteriol. 2004, 186 (3) 722-729 (Pubitemid 38129650)
66. Cue, D.; Lei, M. G.; Luong, T. T.; Kuechenmeister, L.; Dunman, P. M.; O'Donnell, S.; Rowe, S.; O'Gara, J. P.; Lee, C. Y. Rbf promotes biofilm formation by Staphylococcus aureus via repression of icaR, a negative regulator of icaADBC J. Bacteriol. 2009, 191 (20) 6363-6373
67. Heilmann, C.; Schweitzer, O.; Gerke, C.; Vanittanakom, N.; Mack, D.; Goetz, F. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis Mol. Microbiol. 1996, 20 (5) 1083-1091 (Pubitemid 26198280)
68. Hoffman, L. R.; D'Argenio, D. A.; MacCoss, M. J.; Zhang, Z.; Jones, R. A.; Miller, S. I. Aminoglycoside antibiotics induce bacterial biofilm formation Nature 2005, 436 (7054) 1171-1175 (Pubitemid 41232296)
69. Chang, Y.-M.; Jeng, W.-Y.; Ko, T.-P.; Yeh, Y.-J.; Chen, C. K. M.; Wang, A. H. J. Structural study of TcaR and its complexes with multiple antibiotics from Staphylococcus epidermidis Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (19) 8617-8622, S8617/1-S8617/13
70. Sousa, C.; Henriques, M.; Azeredo, J.; Teixeira, P.; Oliveira, R. Staphylococcus epidermidis glucose uptake in biofilm versus planktonic cells World J. Microbiol. Biotechnol. 2008, 24 (3) 423-426 (Pubitemid 351286964)
71. Croes, S.; Deurenberg, R. H.; Boumans, M.-L. L.; Beisser, P. S.; Neef, C.; Stobberingh, E. E. Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage BMC Microbiol. 2009, 9, 229
72. Somerville, G. A.; Said-Salim, B.; Wickman, J. M.; Raffel, S. J.; Kreiswirth, B. N.; Musser, J. M. Correlation of acetate catabolism and growth yield in Staphylococcus aureus: implications for host-pathogen interactions Infect. Immun. 2003, 71 (8) 4724-4732 (Pubitemid 36919941)
73. Cline, M. S.; Smoot, M.; Cerami, E.; Kuchinsky, A.; Landys, N.; Workman, C.; Christmas, R.; Avila-Campilo, I.; Creech, M.; Gross, B.; Hanspers, K.; Isserlin, R.; Kelley, R.; Killcoyne, S.; Lotia, S.; Maere, S.; Morris, J.; Ono, K.; Pavlovic, V.; Pico, A. R.; Vailaya, A.; Wang, P. L.; Adler, A.; Conklin, B. R.; Hood, L.; Kuiper, M.; Sander, C.; Schmulevich, I.; Schwikowski, B.; Warner, G. J.; Ideker, T.; Bader, G. D. Integration of biological networks and gene expression data using Cytoscape Nat. Protoc. 2007, 2 (10) 2366-2382
74. Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N. S.; Wang, J. T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: a software environment for integrated models of biomolecular interaction networks Genome Res. 2003, 13 (11) 2498-2504 (Pubitemid 37428274)