Two-Component System Cross-Regulation Integrates Bacillus anthracis Response to Heme and Cell Envelope Stress

PLoS Pathogens

Volumn 10, Issue 3, 2014, Pages

  Mike, Laura A ^a   Choby, Jacob E ^a,b   Brinkman, Paul R ^a,b   Olive, Lorenzo Q ^a   Dutter, Brendan F ^a   Ivan, Samuel J ^b   Gibbs, Christopher M ^b   Sulikowski, Gary A ^a,c   Stauff, Devin L ^a,b   Skaar, Eric P ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GROVE CITY COLLEGE   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CHLORPROMAZINE; HEME; NORDIHYDROGUAIARETIC ACID; PROTEIN HISTIDINE KINASE; SODIUM DIHYDROGEN PHOSPHATE; TARGOCIL; UNCLASSIFIED DRUG; VANCOMYCIN;

ARTICLE; AUTOPHOSPHORYLATION; BACILLUS ANTHRACIS; BACTERIAL MEMBRANE; CELLULAR STRESS RESPONSE; MICROARRAY ANALYSIS; MUTATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION;

BACILLUS ANTHRACIS; BACTERIAL PROTEINS; CELL WALL; GENE EXPRESSION REGULATION, BACTERIAL; HEME; MEMBRANE TRANSPORT PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84897391538     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004044     Document Type: Article

References (56)

1. Stock AM, Robinson VL, Goudreau PN, (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215.
2. Skerker JM, Perchuk BS, Siryaporn A, Lubin EA, Ashenberg O, et al. (2008) Rewiring the specificity of two-component signal transduction systems. Cell 133: 1043-1054.
3. Laub MT, Goulian M, (2007) Specificity in two-component signal transduction pathways. Annu Rev Genet 41: 121-145.
4. Podgornaia AI, Laub MT, (2013) Determinants of specificity in two-component signal transduction. Curr Opin Microbiol 16: 156-162.
5. Skerker JM, Prasol MS, Perchuk BS, Biondi EG, Laub MT, (2005) Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: A system-level analysis. PLoS Biol 3: e334.
6. Groban ES, Clarke EJ, Salis HM, Miller SM, Voigt CA, (2009) Kinetic buffering of cross talk between bacterial two-component sensors. Journal of Molecular Biology 390: 380-393.
7. Cai SJ, Inouye M, (2002) EnvZ-OmpR interaction and osmoregulation in Escherichia coli. J Biol Chem 277: 24155-24161.
8. Kostakioti M, Hadjifrangiskou M, Pinkner JS, Hultgren SJ, (2009) QseC-mediated dephosphorylation of QseB is required for expression of genes associated with virulence in uropathogenic Escherichia coli. Mol Microbiol 73: 1020-1031.
9. Fisher SL, Jiang W, Wanner BL, Walsh CT, (1995) Cross-talk between the histidine protein kinase VanS and the response regulator PhoB: Characterization and identification of a VanS domain that inhibits activation of PhoB. J Biol Chem 270: 23143-23149.
10. Silva JC, Haldimann A, Prahalad MK, Walsh CT, Wanner BL, (1998) In vivo characterization of the type A and B vancomycin-resistant enterococci (VRE) VanRS two-component systems in Escherichia coli: a nonpathogenic model for studying the VRE signal transduction pathways. Proc Natl Acad Sci U S A 95: 11951-11956.
11. Siryaporn A, Goulian M, (2008) Cross-talk suppression between the CpxA-CpxR and EnvZ-OmpR two-component systems in E. coli. Mol Microbiol 70: 494-506.
12. Siryaporn A, Perchuk BS, Laub MT, Goulian M, (2010) Evolving a robust signal transduction pathway from weak cross-talk. Mol Syst Biol 6: 452.
13. Matsubara M, Kitaoka SI, Takeda SI, Mizuno T, (2000) Tuning of the porin expression under anaerobic growth conditions by His-to-Asp cross-phosphorelay through both the EnvZ-osmosensor and ArcB-anaerosensor in Escherichia coli. Genes Cells 5: 555-569.
14. Stewart V, (2003) Biochemical Society Special Lecture. Nitrate- and nitrite-responsive sensors NarX and NarQ of proteobacteria. Biochem Soc Trans 31: 1-10.
15. Howell A, Dubrac S, Noone D, Varughese KI, Devine K, (2006) Interactions between the YycFG and PhoPR two-component systems in Bacillus subtilis: the PhoR kinase phosphorylates the non-cognate YycF response regulator upon phosphate limitation. Mol Microbiol 59: 1199-1215.
16. Guckes KR, Kostakioti M, Breland EJ, Gu AP, Shaffer CL, et al. (2013) Strong cross-system interactions drive the activation of the QseB response regulator in the absence of its cognate sensor. Proc Natl Acad Sci U S A 110: 16592-16597.
17. Rietkotter E, Hoyer D, Mascher T, (2008) Bacitracin sensing in Bacillus subtilis. Mol Microbiol 68: 768-785.
18. Goodman AL, Merighi M, Hyodo M, Ventre I, Filloux A, et al. (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23: 249-259.
19. Jubelin G, Vianney A, Beloin C, Ghigo JM, Lazzaroni JC, et al. (2005) CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187: 2038-2049.
20. Batchelor E, Walthers D, Kenney LJ, Goulian M, (2005) The Escherichia coli CpxA-CpxR envelope stress response system regulates expression of the porins ompF and ompC. J Bacteriol 187: 5723-5731.
21. Delgado MA, Mouslim C, Groisman EA, (2006) The PmrA/PmrB and RcsC/YojN/RcsB systems control expression of the Salmonella O-antigen chain length determinant. Mol Microbiol 60: 39-50.
22. Mouslim C, Groisman EA, (2003) Control of the Salmonella ugd gene by three two-component regulatory systems. Mol Microbiol 47: 335-344.
23. Darwin AJ, Tyson KL, Busby SJ, Stewart V, (1997) Differential regulation by the homologous response regulators NarL and NarP of Escherichia coli K-12 depends on DNA binding site arrangement. Mol Microbiol 25: 583-595.
24. Gunn JS, Miller SI, (1996) PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J Bacteriol 178: 6857-6864.
25. Vianney A, Jubelin G, Renault S, Dorel C, Lejeune P, et al. (2005) Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis. Microbiology 151: 2487-2497.
26. Birkey SM, Liu W, Zhang X, Duggan MF, Hulett FM, (1998) Pho signal transduction network reveals direct transcriptional regulation of one two-component system by another two-component regulator: Bacillus subtilis PhoP directly regulates production of ResD. Mol Microbiol 30: 943-953.
27. Tonello F, Zornetta I, (2012) Bacillus anthracis factors for phagosomal escape. Toxins 4: 536-553.
28. Honsa ES, Maresso AW, (2011) Mechanisms of iron import in anthrax. Biometals 24: 533-545.
29. Stauff DL, Skaar EP, (2009) Bacillus anthracis HssRS signalling to HrtAB regulates haem resistance during infection. Molecular Microbiology 72: 763-778.
30. Lechardeur D, Cesselin B, Liebl U, Vos MH, Fernandez A, et al. (2012) Discovery of intracellular heme-binding protein HrtR, which controls heme efflux by the conserved HrtB-HrtA transporter in Lactococcus lactis. J Biol Chem 287: 4752-4758.
31. Torres VJ, Stauff DL, Pishchany G, Bezbradica JS, Gordy LE, et al. (2007) A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host & Microbe 1: 109-119.
32. Mike LA, Dutter BF, Stauff DL, Moore JL, Vitko NP, et al. (2013) Activation of heme biosynthesis by a small molecule that is toxic to fermenting Staphylococcus aureus. Proc Natl Acad Sci U S A 110: 8206-8211.
33. de Been M, Bart MJ, Abee T, Siezen RJ, Francke C, (2008) The identification of response regulator-specific binding sites reveals new roles of two-component systems in Bacillus cereus and closely related low-GC Gram-positives. Environ Microbiol 10: 2796-2809.
34. Lu JM, Nurko J, Weakley SM, Jiang J, Kougias P, et al. (2010) Molecular mechanisms and clinical applications of nordihydroguaiaretic acid (NDGA) and its derivatives: an update. Med Sci Monit 16: RA93-100.
35. Drucker AM, Rosen CF, (2011) Drug-induced photosensitivity. Drug Safety 34: 821-837.
36. Klubes P, Fay PJ, Cerna I, (1971) Effects of chlorpromazine on cell wall biosynthesis and incorporation of orotic acid into nucleic acids in Bacillus megaterium. Biochemical Pharmacology 20: 265-277.
37. Ordal GW, (1976) Recognition sites for chemotactic repellents of Bacillus subtilis. J Bacteriol 126: 72-79.
38. Watanakunakorn C (1984) Mode of action and in-vitro activity of vancomycin. J Antimicrob Chemother 14 Suppl D: 7-18.
39. Swoboda JG, Meredith TC, Campbell J, Brown S, Suzuki T, et al. (2009) Discovery of a small molecule that blocks wall teichoic acid biosynthesis in Staphylococcus aureus. ACS Chem Biol 4: 875-883.
40. Campbell J, Singh AK, Swoboda JG, Gilmore MS, Wilkinson BJ, et al. (2012) An antibiotic that inhibits a late step in wall teichoic acid biosynthesis induces the cell wall stress stimulon in Staphylococcus aureus. Antimicrob Agents Chemother 56: 1810-1820.
41. Schirner K, Stone LK, Walker S, (2011) ABC transporters required for export of wall teichoic acids do not discriminate between different main chain polymers. ACS Chem Biol 6: 407-412.
42. Skaar EP, Humayun M, Bae T, DeBord KL, Schneewind O, (2004) Iron-source preference of Staphylococcus aureus infections. Science 305: 1626-1628.
43. Anzaldi LL, Skaar EP, (2010) Overcoming the heme paradox: Heme toxicity and tolerance in bacterial pathogens. Infect Immun 78: 4977-4989.
44. Kirschner-Zilber I, Rabizadeh E, Shaklai N, (1982) The interaction of hemin and bilirubin with the human red cell membrane. Biochim Biophys Acta 690: 10.
45. Schmitt TH, Frezzatti WA, Schreier S, (1993) Hemin-induced lipid membrane disorder and increased permeability: a molecular model for the mechanism of cell lysis. Archives of Biochemistry and Biophysics 307: 96-103.
46. Chou A, Fitch C, (1981) Mechanism of hemolysis induced by ferriprotoporphyrin IX. Journal of Clinical Investigation 68: 6.
47. Heyningen V, (1948) Inhibition of aerobic sporing Bacilli by Haematin. Nature 162: 114.
48. Jiang M, Shao W, Perego M, Hoch JA, (2000) Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol Microbiol 38: 535-542.
49. Fujita M, Losick R, (2005) Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev 19: 2236-2244.
50. Sterne M, (1937) Avirulent anthrax vaccine. Onderstepoort J Vet Sci Animal Ind 21: 41-43.
51. Kim HS, Sherman D, Johnson F, Aronson AI, (2004) Characterization of a major Bacillus anthracis spore coat protein and its role in spore inactivation. J Bacteriol 186: 2413-2417.
52. Kern JW, Schneewind O, (2008) BslA, a pXO1-encoded adhesin of Bacillus anthracis. Mol Microbiol 68: 504-515.
53. Schneewind O, Model P, Fischetti VA, (1992) Sorting of protein A to the staphylococcal cell wall. Cell 70: 267-281.
54. 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.
55. Stauff DL, Bagaley D, Torres VJ, Joyce R, Anderson KL, et al. (2008) Staphylococcus aureus HrtA is an ATPase required for protection against heme toxicity and prevention of a transcriptional heme stress response. J Bacteriol 190: 3588-3596.
56. Stauff DL, Torres VJ, Skaar EP, (2007) Signaling and DNA-binding activities of the Staphylococcus aureus HssR-HssS two-component system required for heme sensing. J Biol Chem 282: 26111-26121.