The catabolite control protein E (CcpE) affects virulence determinant production and pathogenesis of Staphylococcus aureus

Journal of Biological Chemistry

Volumn 289, Issue 43, 2014, Pages 29701-29711

  Hartmann, Torsten ^a   Baronian, Grégory ^b   Nippe, Nadine ^c   Voss, Meike ^a   Schulthess, Bettina ^d   Wolz, Christiane ^e   Eisenbeis, Janina ^a   Schmidt Hohagen, Kerstin ^f   Gaupp, Rosmarie ^a   Sunderkötter, Cord ^c   Beisswenger, Christoph ^a   Bals, Robert ^a   Somerville, Greg A ^g   Herrmann, Mathias ^a   Molle, Virginie ^b   Bischoff, Markus ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b UNIVERSITÉ DE MONTPELLIER   (France)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^f TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^g UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; ELECTROPHORETIC MOBILITY; ENCODING (SYMBOLS); GENE ENCODING; PROTEINS; TRANSCRIPTION;

CATABOLITE CONTROL PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; NEGATIVE REGULATORS; PATHOGENIC BACTERIUM; REGULATORY ELEMENTS; STAPHYLOCOCCUS AUREUS; TRICARBOXYLIC ACID CYCLE; VIRULENCE FACTORS;

BACTERIA;

BACTERIAL PROTEIN; CATABOLITE CONTROL PROTEIN E; PIGMENT; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL RNA; RNAIII, STAPHYLOCOCCUS AUREUS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CAPSULE; BACTERIAL GENE; BACTERIAL SKIN DISEASE; BACTERIAL VIRULENCE; BIOSYNTHESIS; CAPA GENE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GEL MOBILITY SHIFT ASSAY; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HLA GENE; LUNG INFECTION; MOUSE; NONHUMAN; NUTRITIONAL STATUS; PATHOGENESIS; PIGMENTATION; PROMOTER REGION; PROTEIN BINDING; PSM ALPHA GENE; RNA TRANSCRIPTION; STAPHYLOCOCCUS AUREUS; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; DISEASE MODEL; GENETICS; LUNG; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; PATHOGENICITY; PATHOLOGY; STAPHYLOCOCCUS INFECTION; VIRULENCE;

ANIMALS; BACTERIAL CAPSULES; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; FEMALE; GENE DELETION; LUNG; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MULTIGENE FAMILY; PIGMENTS, BIOLOGICAL; RNA, BACTERIAL; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION, GENETIC; VIRULENCE; VIRULENCE FACTORS;

EID: 84908191985     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.584979     Document Type: Article

References (83)

1. Görke, B., and Stülke, J. (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat. Rev. Microbiol. 6, 613-624
2. Poncet, S., Milohanic, E., Mazé, A., Nait Abdallah, J., Aké, F., Larribe, M., Deghmane, A. E., Taha, M. K., Dozot, M., De Bolle, X., Letesson, J. J., and Deutscher, J. (2009) Correlations between carbon metabolism and virulence in bacteria. Contrib. Microbiol. 16, 88-102
3. Seidl, K., Stucki, M., Ruegg, M., Goerke, C., Wolz, C., Harris, L., Berger-Bächi, B., and Bischoff, M. (2006) Staphylococcus aureus CcpA affects virulence determinant production and antibiotic resistance. Antimicrob. Agents Chemother. 50, 1183-1194
4. Majerczyk, C. D., Sadykov, M. R., Luong, T. T., Lee, C., Somerville, G. A., and Sonenshein, A. L. (2008) Staphylococcus aureus CodY negatively regulates virulence gene expression. J. Bacteriol. 190, 2257-2265
5. Zhu, Y., Nandakumar, R., Sadykov, M. R., Madayiputhiya, N., Luong, T. T., Gaupp, R., Lee, C. Y., and Somerville, G. A. (2011) RpiR homologues may link Staphylococcus aureus RNAIII synthesis and pentose phosphate pathway regulation. J. Bacteriol. 193, 6187-6196
6. Hartmann, T., Zhang, B., Baronian, G., Schulthess, B., Homerova, D., Grubmüller, S., Kutzner, E., Gaupp, R., Bertram, R., Powers, R., Eisenreich, W., Kormanec, J., Herrmann, M., Molle, V., Somerville, G. A., and Bischoff, M. (2013) Catabolite control protein E (CcpE) is a LysR-type transcriptional regulator of tricarboxylic acid cycle activity in Staphylococcus aureus. J. Biol. Chem. 288, 36116-36128
7. Seidl, K., Bischoff, M., and Berger-Bächi, B. (2008) CcpA mediates the catabolite repression of tst in Staphylococcus aureus. Infect. Immun. 76, 5093-5099
8. Seidl, K., Müller, S., Franc¸ois, P., Kriebitzsch, C., Schrenzel, J., Engelmann, S., Bischoff, M., and Berger-Bächi, B. (2009) Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol. 9, 95
9. Seidl, K., Goerke, C., Wolz, C., Mack, D., Berger-Bächi, B., and Bischoff, M. (2008) Staphylococcus aureus CcpA affects biofilm formation. Infect. Immun. 76, 2044-2050
10. Li, C., Sun, F., Cho, H., Yelavarthi, V., Sohn, C., He, C., Schneewind, O., and Bae, T. (2010) CcpA mediates proline auxotrophy and is required for Staphylococcus aureus pathogenesis. J. Bacteriol. 192, 3883-3892
11. Nuxoll, A. S., Halouska, S. M., Sadykov, M. R., Hanke, M. L., Bayles, K. W., Kielian, T., Powers, R., and Fey, P. D. (2012) CcpA regulates arginine biosynthesis in Staphylococcus aureus through repression of proline catabolism. PLoS Pathog. 8, e1003033
12. Majerczyk, C. D., Dunman, P. M., Luong, T. T., Lee, C. Y., Sadykov, M. R., Somerville, G. A., Bodi, K., and Sonenshein, A. L. (2010) Direct targets of CodY in Staphylococcus aureus. J. Bacteriol. 192, 2861-2877
13. Pohl, K., Francois, P., Stenz, L., Schlink, F., Geiger, T., Herbert, S., Goerke, C., Schrenzel, J., and Wolz, C. (2009) CodY in Staphylococcus aureus: a regulatory link between metabolism and virulence gene expression. J. Bacteriol. 191, 2953-2963
14. Geiger, T., Goerke, C., Fritz, M., Schäfer, T., Ohlsen, K., Liebeke, M., Lalk, M., and Wolz, C. (2010) Role of the (p)ppGpp synthase RSH, a RelA/SpoT homolog, in stringent response and virulence of Staphylococcus aureus. Infect. Immun. 78, 1873-1883
15. Montgomery, C. P., Boyle-Vavra, S., Roux, A., Ebine, K., Sonenshein, A. L., and Daum, R. S. (2012) CodY deletion enhances in vivo virulence of community-associated methicillin-resistant Staphylococcus aureus clone USA300. Infect. Immun. 80, 2382-2389
16. Lan, L., Cheng, A., Dunman, P. M., Missiakas, D., and He, C. (2010) Golden pigment production and virulence gene expression are affected by metabolisms in Staphylococcus aureus. J. Bacteriol. 192, 3068-3077
17. Chatterjee, I., Herrmann, M., Proctor, R. A., Peters, G., and Kahl, B. C. (2007) Enhanced post-stationary-phase survival of a clinical thymidine-dependent small-colony variant of Staphylococcus aureus results from lack of a functional tricarboxylic acid cycle. J. Bacteriol. 189, 2936-2940
18. Gaupp, R., Schlag, S., Liebeke, M., Lalk, M., and Götz, F. (2010) Advantage of upregulation of succinate dehydrogenase in Staphylococcus aureus biofilms. J. Bacteriol. 192, 2385-2394
19. Massilamany, C., Gangaplara, A., Gardner, D. J., Musser, J. M., Steffen, D., Somerville, G. A., and Reddy, J. (2011) TCA cycle inactivation in Staphylococcus aureus alters nitric oxide production in RAW 264.7 cells. Mol. Cell. Biochem. 355, 75-82
20. Sadykov, M. R., Mattes, T. A., Luong, T. T., Zhu, Y., Day, S. R., Sifri, C. D., Lee, C. Y., and Somerville, G. A. (2010) Tricarboxylic acid cycle-dependent synthesis of Staphylococcus aureus Type 5 and 8 capsular polysaccharides. J. Bacteriol. 192, 1459-1462
21. Sheldon, J. R., Marolda, C. L., and Heinrichs, D. E. (2014) TCA cycle activity in Staphylococcus aureus is essential for iron-regulated synthesis of staphyloferrin A, but not staphyloferrin B: the benefit of a second citrate synthase. Mol. Microbiol. 92, 824-839
22. Zhu, Y., Xiong, Y. Q., Sadykov, M. R., Fey, P. D., Lei, M. G., Lee, C. Y., Bayer, A. S., and Somerville, G. A. (2009) Tricarboxylic acid cycle-dependent attenuation of Staphylococcus aureus in vivo virulence by selective inhibition of amino acid transport. Infect. Immun. 77, 4256-4264
23. Liu, C. I., Liu, G. Y., Song, Y., Yin, F., Hensler, M. E., Jeng, W. Y., Nizet, V., Wang, A. H., and Oldfield, E. (2008) A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence. Science 319, 1391-1394
24. Liu, G. Y., Essex, A., Buchanan, J. T., Datta, V., Hoffman, H. M., Bastian, J. F., Fierer, J., and Nizet, V. (2005) Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J. Exp. Med. 202, 209-215
25. Duthie, E. S. (1952) Variation in the antigenic composition of staphylococcal coagulase. J. Gen. Microbiol. 7, 320-326
26. Boyle-Vavra, S., Yin, S., and Daum, R. S. (2006) The VraS/VraR two-component regulatory system required for oxacillin resistance in community-acquired methicillin-resistant Staphylococcus aureus. FEMS Microbiol. Lett. 262, 163-171
27. Somerville, G. A., Chaussee, M. S., Morgan, C. I., Fitzgerald, J. R., Dorward, D. W., Reitzer, L. J., and Musser, J. M. (2002) Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival. Infect. Immun. 70, 6373-6382
28. Cheung, A. L., Eberhardt, K. J., and Fischetti, V. A. (1994) A method to isolate RNA from Gram-positive bacteria and mycobacteria. Anal. Biochem. 222, 511-514
29. McCallum, N., Karauzum, H., Getzmann, R., Bischoff, M., Majcherczyk, P., Berger-Bächi, B., and Landmann, R. (2006) In vivo survival of teicoplanin-resistant Staphylococcus aureus and fitness cost of teicoplanin resistance. Antimicrob. Agents Chemother. 50, 2352-2360
30. Chatterjee, I., Becker, P., Grundmeier, M., Bischoff, M., Somerville, G. A., Peters, G., Sinha, B., Harraghy, N., Proctor, R. A., and Herrmann, M. (2005) Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J. Bacteriol. 187, 4488-4496
31. Valihrach, L., and Demnerova, K. (2012) Impact of normalization method on experimental outcome using RT-qPCR in Staphylococcus aureus. J. Microbiol. Methods 90, 214-216
32. Qazi, S. N., Counil, E., Morrissey, J., Rees, C. E., Cockayne, A., Winzer, K., Chan, W. C., Williams, P., and Hill, P. J. (2001) agr expression precedes escape of internalized Staphylococcus aureus from the host endosome. Infect. Immun. 69, 7074-7082
33. Schmitt, J., Joost, I., Skaar, E. P., Herrmann, M., and Bischoff, M. (2012) Haemin represses the haemolytic activity of Staphylococcus aureus in an Sae-dependent manner. Microbiology 158, 2619-2631
34. Hoeger, P. H., Lenz, W., Boutonnier, A., and Fournier, J. M. (1992) Staphylococcal skin colonization in children with atopic dermatitis: prevalence, persistence, and transmission of toxigenic and nontoxigenic strains. J. Infect. Dis. 165, 1064-1068
35. Selinummi, J., Seppälä, J., Yli-Harja, O., and Puhakka, J. A. (2005) Software for quantification of labeled bacteria from digital microscope images by automated image analysis. BioTechniques 39, 859-863
36. Morikawa, K., Maruyama, A., Inose, Y., Higashide, M., Hayashi, H., and Ohta, T. (2001) Overexpression of sigma factor, σ(B), urges Staphylococcus aureus to thicken the cell wall and to resist β-lactams. Biochem. Biophys. Res. Commun. 288, 385-389
37. Seiler, F., Hellberg, J., Lepper, P. M., Kamyschnikow, A., Herr, C., Bischoff, M., Langer, F., Schäfers, H. J., Lammert, F., Menger, M. D., Bals, R., and Beisswenger, C. (2013) FOXO transcription factors regulate innate immune mechanisms in respiratory epithelial cells. J. Immunol. 190, 1603-1613
38. Nippe, N., Varga, G., Holzinger, D., Löffler, B., Medina, E., Becker, K., Roth, J., Ehrchen, J. M., and Sunderkötter, C. (2011) Subcutaneous infection with S. aureus in mice reveals association of resistance with influx of neutrophils and Th2 response. J. Investig. Dermatol. 131, 125-132
39. Pragman, A. A., and Schlievert, P. M. (2004) Virulence regulation in Staphylococcus aureus: the need for in vivo analysis of virulence factor regulation. FEMS Immunol. Med. Microbiol. 42, 147-154
40. Queck, S. Y., Jameson-Lee, M., Villaruz, A. E., Bach, T. H., Khan, B. A., Sturdevant, D. E., Ricklefs, S. M., Li, M., and Otto, M. (2008) RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol. Cell 32, 150-158
41. Cheung, A. L., and Ying, P. (1994) Regulation of α- and β-hemolysins by the sar locus of Staphylococcus aureus. J. Bacteriol. 176, 580-585
42. Ingavale, S., van Wamel, W., Luong, T. T., Lee, C. Y., and Cheung, A. L. (2005) Rat/MgrA, a regulator of autolysis, is a regulator of virulence genes in Staphylococcus aureus. Infect. Immun. 73, 1423-1431
43. Morfeldt, E., Taylor, D., von Gabain, A., and Arvidson, S. (1995) Activation of α-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J. 14, 4569-4577
44. Oscarsson, J., Kanth, A., Tegmark-Wisell, K., and Arvidson, S. (2006) SarA is a repressor of hla (α-hemolysin) transcription in Staphylococcus aureus: its apparent role as an activator of hla in the prototype strain NCTC 8325 depends on reduced expression of sarS. J. Bacteriol. 188, 8526-8533
45. Leiba, J., Hartmann, T., Cluzel, M. E., Cohen-Gonsaud, M., Delolme, F., Bischoff, M., and Molle, V. (2012) A novel mode of regulation of the Staphylococcus aureus catabolite control protein A (CcpA) mediated by Stk1 protein phosphorylation. J. Biol. Chem. 287, 43607-43619
46. Peschel, A., and Otto, M. (2013) Phenol-soluble modulins and staphylococcal infection. Nat. Rev. Microbiol. 11, 667-673
47. Zielinska, A. K., Beenken, K. E., Joo, H. S., Mrak, L. N., Griffin, L. M., Luong, T. T., Lee, C. Y., Otto, M., Shaw, L. N., and Smeltzer, M. S. (2011) Defining the strain-dependent impact of the Staphylococcal accessory regulator (sarA) on the α-toxin phenotype of Staphylococcus aureus. J. Bacteriol. 193, 2948-2958
48. Pelz, A., Wieland, K. P., Putzbach, K., Hentschel, P., Albert, K., and Götz, F. (2005) Structure and biosynthesis of staphyloxanthin from Staphylococcus aureus. J. Biol. Chem. 280, 32493-32498
49. Suzuki, S., Kobayashi, M., Chiba, K., Horiuchi, I., Wang, J., Kondoh, T., Hashino, S., Tanaka, J., Hosokawa, M., and Asaka, M. (2002) Autocrine production of epithelial cell-derived neutrophil attractant-78 induced by granulocyte colony-stimulating factor in neutrophils. Blood 99, 1863-1865
50. Somerville, G. A., Cockayne, A., Dürr, M., Peschel, A., Otto, M., and Musser, J. M. (2003) Synthesis and deformylation of Staphylococcus aureus δ-toxin are linked to tricarboxylic acid cycle activity. J. Bacteriol. 185, 6686-6694
51. Bubeck Wardenburg, J., Bae, T., Otto, M., Deleo, F. R., and Schneewind, O. (2007) Poring over pores: α-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat. Med. 13, 1405-1406
52. Bubeck Wardenburg, J., Patel, R. J., and Schneewind, O. (2007) Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect. Immun. 75, 1040-1044
53. Bubeck Wardenburg, J., and Schneewind, O. (2008) Vaccine protection against Staphylococcus aureus pneumonia. J. Exp. Med. 205, 287-294
54. Bartlett, A. H., Foster, T. J., Hayashida, A., and Park, P. W. (2008) α-Toxin facilitates the generation of CXC chemokine gradients and stimulates neutrophil homing in Staphylococcus aureus pneumonia. J. Infect. Dis. 198, 1529-1535
55. Kebaier, C., Chamberland, R. R., Allen, I. C., Gao, X., Broglie, P. M., Hall, J. D., Jania, C., Doerschuk, C. M., Tilley, S. L., and Duncan, J. A. (2012) Staphylococcus aureus alpha-hemolysin mediates virulence in a murine model of severe pneumonia through activation of the NLRP3 inflammasome. J. Infect. Dis. 205, 807-817
56. Geisinger, E., Chen, J., and Novick, R. P. (2012) Allele-dependent differences in quorum-sensing dynamics result in variant expression of virulence genes in Staphylococcus aureus. J. Bacteriol. 194, 2854-2864
57. Novick, R. P. (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48, 1429-1449
58. Boisset, S., Geissmann, T., Huntzinger, E., Fechter, P., Bendridi, N., Possedko, M., Chevalier, C., Helfer, A. C., Benito, Y., Jacquier, A., Gaspin, C., Vandenesch, F., and Romby, P. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev. 21, 1353-1366
59. Kobayashi, S. D., Malachowa, N., Whitney, A. R., Braughton, K. R., Gardner, D. J., Long, D., Bubeck Wardenburg, J., Schneewind, O., Otto, M., and Deleo, F. R. (2011) Comparative analysis of USA300 virulence determinants in a rabbit model of skin and soft tissue infection. J. Infect. Dis. 204, 937-941
60. Abdelnour, A., Arvidson, S., Bremell, T., Rydén, C., and Tarkowski, A. (1993) The accessory gene regulator (agr) controls Staphylococcus aureus virulence in a murine arthritis model. Infect. Immun. 61, 3879-3885
61. Gillaspy, A. F., Hickmon, S. G., Skinner, R. A., Thomas, J. R., Nelson, C. L., and Smeltzer, M. S. (1995) Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect. Immun. 63, 3373-3380
62. Cheung, G. Y., Wang, R., Khan, B. A., Sturdevant, D. E., and Otto, M. (2011) Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infect. Immun. 79, 1927-1935
63. Cheung, A. L., Eberhardt, K. J., Chung, E., Yeaman, M. R., Sullam, P. M., Ramos, M., and Bayer, A. S. (1994) Diminished virulence of a sar-/agr-mutant of Staphylococcus aureus in the rabbit model of endocarditis. J. Clin. Investig. 94, 1815-1822
64. Montgomery, C. P., Boyle-Vavra, S., and Daum, R. S. (2010) Importance of the global regulators Agr and SaeRS in the pathogenesis of CA-MRSA USA300 infection. PloS One 5, e15177
65. Chua, K. Y., Monk, I. R., Lin, Y. H., Seemann, T., Tuck, K. L., Porter, J. L., Stepnell, J., Coombs, G. W., Davies, J. K., Stinear, T. P., and Howden, B. P. (2014) Hyperexpression of α-hemolysin explains enhanced virulence of sequence type 93 community-associated methicillin-resistant Staphylococcus aureus. BMC Microbiol. 14, 31
66. Mayville, P., Ji, G., Beavis, R., Yang, H., Goger, M., Novick, R. P., and Muir, T. W. (1999) Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc. Natl. Acad. Sci. U.S.A. 96, 1218-1223
67. Wright, J. S., 3rd, Jin, R., and Novick, R. P. (2005) Transient interference with staphylococcal quorum sensing blocks abscess formation. Proc. Natl. Acad. Sci. U.S.A. 102, 1691-1696
68. Zhang, P., Bagby, G. J., Kolls, J. K., Welsh, D. A., Summer, W. R., Andresen, J., and Nelson, S. (2001) The effects of granulocyte colony-stimulating factor and neutrophil recruitment on the pulmonary chemokine response to intratracheal endotoxin. J. Immunol. 166, 458-465
69. Koyama, S., Sato, E., Masubuchi, T., Takamizawa, A., Kubo, K., Nagai, S., and Izumi, T. (1998) Alveolar type II-like cells release G-CSF as neutrophil chemotactic activity. Am. J. Physiol. Lung Cell. Mol. Physiol. 275, L687-L693
70. Koyama, S., Sato, E., Nomura, H., Kubo, K., Miura, M., Yamashita, T., Nagai, S., and Izumi, T. (2000) The potential of various lipopolysaccharides to release IL-8 and G-CSF. Am. J. Physiol. Lung Cell. Mol. Physiol. 278, L658-L666
71. Saba, S., Soong, G., Greenberg, S., and Prince, A. (2002) Bacterial stimulation of epithelial G-CSF and GM-CSF expression promotes PMN survival in CF airways. Am. J. Respir. Cell Mol. Biol. 27, 561-567
72. Balamayooran, G., Batra, S., Theivanthiran, B., Cai, S., Pacher, P., and Jeyaseelan, S. (2012) Intrapulmonary G-CSF rescues neutrophil recruitment to the lung and neutrophil release to blood in Gram-negative bacterial infection in MCP-1-/- mice. J. Immunol. 189, 5849-5859
73. Hua, L., Hilliard, J. J., Shi, Y., Tkaczyk, C., Cheng, L. I., Yu, X., Datta, V., Ren, S., Feng, H., Zinsou, R., Keller, A., O'Day, T., Du, Q., Cheng, L., Damschroder, M., Robbie, G., Suzich, J., Stover, C. K., and Sellman, B. R. (2014) Assessment of an anti-α-toxin monoclonal antibody for prevention and treatment of Staphylococcus aureus-induced pneumonia. Antimicrob. Agents Chemother. 58, 1108-1117
74. Reyes, D., Andrey, D. O., Monod, A., Kelley, W. L., Zhang, G., and Cheung, A. L. (2011) Coordinated regulation by AgrA, SarA, and SarR to control agr expression in Staphylococcus aureus. J. Bacteriol. 193, 6020-6031
75. Gupta, R. K., Alba, J., Xiong, Y. Q., Bayer, A. S., and Lee, C. Y. (2013) MgrA activates expression of capsule genes, but not the α-toxin gene in experimental Staphylococcus aureus endocarditis. J. Infect. Dis. 208, 1841-1848
76. van Wamel, W., Xiong, Y. Q., Bayer, A. S., Yeaman, M. R., Nast, C. C., and Cheung, A. L. (2002) Regulation of Staphylococcus aureus type 5 capsular polysaccharides by agr and sarA in vitro and in an experimental endocarditis model. Microb. Pathogen. 33, 73-79
77. Luong, T., Sau, S., Gomez, M., Lee, J. C., and Lee, C. Y. (2002) Regulation of Staphylococcus aureus capsular polysaccharide expression by agr and sarA. Infect. Immun. 70, 444-450
78. Alén, C., and Sonenshein, A. L. (1999) Bacillus subtilis aconitase is an RNA-binding protein. Proc. Natl. Acad. Sci. U.S.A. 96, 10412-10417
79. Serio, A. W., Pechter, K. B., and Sonenshein, A. L. (2006) Bacillus subtilis aconitase is required for efficient late-sporulation gene expression. J. Bacteriol. 188, 6396-6405
80. Pechter, K. B., Meyer, F. M., Serio, A. W., Stülke, J., and Sonenshein, A. L. (2013) Two roles for aconitase in the regulation of tricarboxylic acid branch gene expression in Bacillus subtilis. J. Bacteriol. 195, 1525-1537
81. Regassa, L. B., and Betley, M. J. (1992) Alkaline pH decreases expression of the accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol. 174, 5095-5100
82. Anderson, K. L., Roux, C. M., Olson, M. W., Luong, T. T., Lee, C. Y., Olson, R., and Dunman, P. M. (2010) Characterizing the effects of inorganic acid and alkaline shock on the Staphylococcus aureus transcriptome and messenger RNA turnover. FEMS Immunol. Med. Microbiol. 60, 208-250
83. Pané-Farré, J., Jonas, B., Förstner, K., Engelmann, S., and Hecker, M. (2006) The σB regulon in Staphylococcus aureus and its regulation. Int. J. Med. Microbiol. 296, 237-258