CcpA Regulates Arginine Biosynthesis in Staphylococcus aureus through Repression of Proline Catabolism

PLoS Pathogens

Volumn 8, Issue 11, 2012, Pages

  Nuxoll, Austin S ^a   Halouska, Steven M ^b   Sadykov, Marat R ^a   Hanke, Mark L ^a   Bayles, Kenneth W ^a   Kielian, Tammy ^a   Powers, Robert ^b   Fey, Paul D ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; ARGININE; CATABOLITE CONTROL PROTEIN A; COLLAGEN TYPE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; PROLINE;

AMINO ACID ANALYSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUXOTROPHY; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CARBON SOURCE; CATABOLITE REPRESSION; DEFENSE MECHANISM; GENE MUTATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; IMMUNOFLUORESCENCE TEST; MOUSE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; STAPHYLOCOCCUS AUREUS;

ABSCESS; ANIMALS; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; GENOME, BACTERIAL; KIDNEY DISEASES; MICE; MUTATION; PROLINE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION FACTORS;

STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 84870772944     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003033     Document Type: Article

References (68)

1. Deleo FR, Otto M, Kreiswirth BN, (2010) Chambers HF, (2010) Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557-1568.
2. Seidl K, Stucki M, Ruegg M, Goerke C, Wolz C, et al. (2006) Staphylococcus aureus CcpA affects virulence determinant production and antibiotic resistance. Antimicrob Agents Chemother 50: 1183-1194.
3. Majerczyk CD, Sadykov MR, Luong TT, Lee C, Somerville GA, et al. (2008) Staphylococcus aureus CodY negatively regulates virulence gene expression. J Bacteriol 190: 2257-2265.
4. Pohl K, Francois P, Stenz L, Schlink F, Geiger T, et al. (2009) CodY in Staphylococcus aureus: a regulatory link between metabolism and virulence gene expression. J Bacteriol 191: 2953-2963.
5. Somerville GA, Proctor RA, (2009) At the crossroads of bacterial metabolism and virulence factor synthesis in Staphylococci. Microbiol Mol Biol Rev 73: 233-248.
6. Zhu Y, Nandakumar R, Sadykov MR, Madayiputhiya N, Luong TT, et al. (2011) RpiR Homologues May Link Staphylococcus aureus RNAIII Synthesis and Pentose Phosphate Pathway Regulation. J Bacteriol 193: 6187-6196.
7. Zhu Y, Weiss EC, Otto M, Fey PD, Smeltzer MS, et al. (2009) Tricarboxylic acid cycle-dependent attenuation of Staphylococcus aureus in vivo virulence by selective inhibition of amino acid transport. Infect Immun 77: 4256-4264.
8. Emmett M, Kloos WE, (1975) Amino acid requirements of staphylococci isolated from human skin. Can J Microbiol 21: 729-733.
9. Gladstone GP, (1937) The nutrition of Staphylococcus aureus; nitrogen requirements. Br J Exp Pathol 18: 322-333.
10. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa, et al. (2001) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357: 1225-1240.
11. Cunin R, Glansdorff N, Pierard A, Stalon V, (1986) Biosynthesis and metabolism of arginine in bacteria. Microbiological reviews 50: 314-352.
12. Vogel RH, Vogel HJ, (1963) Acetylated intermediates of arginine synthesis in Bacillus subtilis. Biochim Biophysica ACTA 69: 174-176.
13. Prozesky OW, (1967) Arginine synthesis in Proteus mirabilis. J Gen Microbiol 49: 325-334.
14. Rodriguez-Garcia A, de la Fuente A, Perez-Redondo R, Martin JF, Liras P, (2000) Characterization and expression of the arginine biosynthesis gene cluster of Streptomyces clavuligerus. J Mol Microbiol Biotechnol 2: 543-550.
15. Leisinger T (1987) Proline Biosynthesis. In: Neidhardt F, Ingraham JL, Low K, Magasanik B, Schaechter M, & Umbarger H, editors. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. Washington DC: ASM Press. pp. 345-357.
16. Abdelal AT, (1979) Arginine catabolism by microorganisms. Annu Rev Microbiol 33: 139-168.
17. Townsend DE, Kaenjak A, Jayaswal RK, Wilkinson BJ, (1996) Proline is biosynthesized from arginine in Staphylococcus aureus. Microbiology 142: 1491-1497.
18. Li C, Sun F, Cho H, Yelavarthi V, Sohn C, et al. (2010) CcpA mediates proline auxotrophy and is required for Staphylococcus aureus pathogenesis. J Bacteriol 192: 3883-3892.
19. Stulke J, Hillen W, (1999) Carbon catabolite repression in bacteria. Curr Opin Microbiol 2: 195-201.
20. Deutscher J, Kuster E, Bergstedt U, Charrier V, Hillen W, (1995) Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol Microbiol 15: 1049-1053.
21. Henkin TM, (1996) The role of CcpA transcriptional regulator in carbon metabolism in Bacillus subtilis. FEMS Microbiol Lett 135: 9-15.
22. Hueck CJ, Hillen W, (1995) Catabolite repression in Bacillus subtilis: a global regulatory mechanism for the gram-positive bacteria? Mol Microbiol 15: 395-401.
23. Schumacher MA, Allen GS, Diel M, Seidel G, Hillen W, et al. (2004) Structural basis for allosteric control of the transcription regulator CcpA by the phosphoprotein HPr-Ser46-P. Cell 118: 731-741.
24. Deutscher J, Saier MH Jr, (1983) ATP-dependent protein kinase-catalyzed phosphorylation of a seryl residue in HPr, a phosphate carrier protein of the phosphotransferase system in Streptococcus pyogenes. Proc Natl Acad Sci U S A 80: 6790-6794.
25. Mijakovic I, Poncet S, Galinier A, Monedero V, Fieulaine S, et al. (2002) Pyrophosphate-producing protein dephosphorylation by HPr kinase/phosphorylase: a relic of early life? Proc Natl Acad Sci U S A 99: 13442-13447.
26. Sonenshein AL, (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5: 917-927.
27. Lu CD, (2006) Pathways and regulation of bacterial arginine metabolism and perspectives for obtaining arginine overproducing strains. Appl Microbiol Biotechnol 70: 261-272.
28. Maas WK, (1964) Studies on the Mechanism of Repression of Arginine Biosynthesis in Escherichia coli. Ii. Dominance of Repressibility in Diploids. J Mol Biol 8: 365-370.
29. Xu Y, Labedan B, Glansdorff N, (2007) Surprising arginine biosynthesis: a reappraisal of the enzymology and evolution of the pathway in microorganisms. Microbiol Mol Biol Rev 71: 36-47.
30. Somerville GA, Proctor RA (2009) The Biology of Staphylococci. In: Crossley KB, Jefferson KK, Archer GL, & Fowler VG, editors. Staphylococci in Human Disease. Oxford: Blackwell Publishing Ltd. pp. 3-18.
31. Sadykov MR, Hartmann T, Mattes TA, Hiatt M, Jann NJ, et al. (2011) CcpA coordinates central metabolism and biofilm formation in Staphylococcus epidermidis. Microbiology 157: 3458-3468.
32. Seidl K, Bischoff M, Berger-Bachi B, (2008) CcpA mediates the catabolite repression of tst in Staphylococcus aureus. Infect Immun 76: 5093-5099.
33. Seidl K, Goerke C, Wolz C, Mack D, Berger-Bachi B, et al. (2008) Staphylococcus aureus CcpA affects biofilm formation. Infect Immun 76: 2044-2050.
34. Seidl K, Muller S, Francois P, Kriebitzsch C, Schrenzel J, et al. (2009) Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol 9: 95.
35. Becker SA, Palsson BO, (2005) Genome-scale reconstruction of the metabolic network in Staphylococcus aureus N315: an initial draft to the two-dimensional annotation. BMC Microbiol 5: 8.
36. Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, et al. (2008) The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197: 1523-1530.
37. Davis JS, Anstey NM, (2011) Is plasma arginine concentration decreased in patients with sepsis? A systematic review and meta-analysis. Crit Care Med 39: 380-385.
38. Fang FC, (1997) Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 99: 2818-2825.
39. Ochoa JB, Strange J, Kearney P, Gellin G, Endean E, et al. (2001) Effects of L-arginine on the proliferation of T lymphocyte subpopulations. JPEN J Parenter Enteral Nutr 25: 23-29.
40. Luiking YC, Poeze M, Ramsay G, Deutz NE, (2005) The role of arginine in infection and sepsis. JPEN J Parenter Enteral Nutr 29: S70-74.
41. Shi HP, Most D, Efron DT, Witte MB, Barbul A, (2003) Supplemental L-arginine enhances wound healing in diabetic rats. Wound Repair Regen 11: 198-203.
42. Witte MB, (2003) Barbul A, (2003) Arginine physiology and its implication for wound healing. Wound Repair Regen 11: 419-423.
43. Thurlow LR, Hanke ML, Fritz T, Angle A, Aldrich A, et al. (2011) Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J Immunol 186: 6585-6596.
44. Kalil AC, (2011) Is it time to replace L-arginine in severe sepsis? Crit Care Med 39: 417-418.
45. Shoulders MD, Raines RT, (2009) Collagen structure and stability. Annu Rev Biochem 78: 929-958.
46. Kantyka T, Shaw LN, Potempa J, (2011) Papain-like proteases of Staphylococcus aureus. Adv Exp Med Biol 712: 1-14.
47. Ohbayashi T, Irie A, Murakami Y, Nowak M, Potempa J, et al. (2011) Degradation of fibrinogen and collagen by staphopains, cysteine proteases released from Staphylococcus aureus. Microbiology 157: 786-792.
48. Rice K, Peralta R, Bast D, de Azavedo J, McGavin MJ, (2001) Description of staphylococcus serine protease (ssp) operon in Staphylococcus aureus and nonpolar inactivation of sspA-encoded serine protease. Infect Immun 69: 159-169.
49. Bayer AS, Coulter SN, Stover CK, Schwan WR, (1999) Impact of the high-affinity proline permease gene (putP) on the virulence of Staphylococcus aureus in experimental endocarditis. Infect Immun 67: 740-744.
50. Coulter SN, Schwan WR, Ng EY, Langhorne MH, Ritchie HD, et al. (1998) Staphylococcus aureus genetic loci impacting growth and survival in multiple infection environments. Mol Microbiol 30(2): 393-404.
51. Cheng AG, Cheng AG, Kim HK, Burts ML, Krausz T, Schneewind O, et al. (2009) Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J 23: 3393-3404.
52. Pitz AM, Yu F, Hermsen ED, Rupp ME, Fey PD, et al. (2010) Vancomycin Susceptibility Trends and Prevalence of Heterogeneous Vancomycin-Intermediate Staphylococcus aureus (hVISA) in Clinical Methicillin-Resistant S. aureus (MRSA) Isolates. J Clin Microbiol 49: 269-274.
53. Hussain M, Hastings JG, White PJ, (1991) A chemically defined medium for slime production by coagulase-negative staphylococci. J Med Microbiol 34: 143-147.
54. Bae T, Banger AK, Wallace A, Glass EM, Aslund F, et al. (2004) Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc Natl Acad Sci U S A 101: 12312-12317.
55. Climo MW, Sharma VK, Archer GL, (1996) Identification and characterization of the origin of conjugative transfer (oriT) and a gene (nes) encoding a single-stranded endonuclease on the staphylococcal plasmid pGO1. J Bacteriol 178: 4975-4983.
56. Horton RM, Cai ZL, Ho SN, Pease LR, (1990) Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8: 528-535.
57. Bruckner R, (1997) Gene replacement in Staphylococcus carnosus and Staphylococcus xylosus. FEMS Microbiol Lett 151: 1-8.
58. Sadykov MR, Olson ME, Halouska S, Zhu Y, Fey PD, et al. (2008) Tricarboxylic acid cycle-dependent regulation of Staphylococcus epidermidis polysaccharide intercellular adhesin synthesis. J Bacteriol 190: 7621-7632.
59. Foster TJ (1998) Molecular Genetic Analysis of Staphylococcal Virulence. In: Williams P, Ketley J, & Salmond GPC, editors. Methods in Microbiology, Bacterial Pathogenesis. San Diego: Academic Press. pp. 433-454.
60. Charpentier E, Anton AI, Barry P, Alfonso B, Fang Y, et al. (2004) Novel cassette-based shuttle vector system for gram-positive bacteria. Appl Environ Microbiol 70: 6076-6085.
61. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
62. Johnson BA, (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods in molecular biology 278: 313-352.
63. Wishart DS, Knox C, Guo AC, Eisner R, Young N, et al. (2009) HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res 37: D603-610.
64. Cui Q, Lewis IA, Hegeman AD, Anderson ME, Li J, et al. (2008) Metabolite identification via the Madison Metabolomics Consortium Database. Nat Biotechnol 26(2): 162-164.
65. Akiyama K, Chikayama E, Yuasa H, Shimada Y, Tohge T, et al. (2008) PRIMe: a Web site that assembles tools for metabolomics and transcriptomics. In Silico Biol 8: 339-345.
66. Okuda S, Yamada T, Hamajima M, Itoh M, Katayama T, et al. (2008) KEGG Atlas mapping for global analysis of metabolic pathways. Nucleic Acids Res 36: W423-426.
67. Caspi R, Altman T, Dale JM, Dreher K, Fulcher CA, et al. (2010) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 38: D473-479.
68. Zhang B, Halouska S, Schiafo CE, Sadykov MR, Somerville GA, et al. (2011) NMR analysis of a stress response metabolic signaling network. J prot Res 10: 3743-3754.