Ubiquinone and menaquinone electron carriers represent the yin and yang in the redox regulation of the ArcB sensor kinase

Journal of Bacteriology

Volumn 195, Issue 13, 2013, Pages 3054-3061

  Alvarez, Adrián F ^a   Rodriguez, Claudia ^a   Georgellis, Dimitris ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ARCB SENSOR KINASE; ARCC SENSOR KINASE; CYSTEINE; MENAQUINONE; PROTEIN KINASE; UBIQUINONE; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ARTICLE; CONTROLLED STUDY; CYTOSOL; DISULFIDE BOND; ELECTRON TRANSPORT; ENZYME ACTIVATION; ENZYME ACTIVITY; IN VIVO STUDY; OPERON; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; OXIDATION-REDUCTION; PROTEIN KINASES; SIGNAL TRANSDUCTION; UBIQUINONE; VITAMIN K 2;

ARCA;

EID: 84880001463     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00406-13     Document Type: Article

References (45)

1. Georgellis D, Kwon O, Lin EC, Wong SM, Akerley BJ. 2001. Redox signal transduction by the ArcB sensor kinase of Haemophilus influenzae lacking the PAS domain. J. Bacteriol. 183:7206 -7212.
2. Jung WS, Jung YR, Oh DB, Kang HA, Lee SY, Chavez-Canales M, Georgellis D, Kwon O. 2008. Characterization of the Arc two-component signal transduction system of the capnophilic rumen bacterium Mannheimia succiniciproducens. FEMS Microbiol. Lett. 284:109 -119.
3. Malpica R, Sandoval GR, Rodriguez C, Franco B, Georgellis D. 2006. Signaling by the Arc two-component system provides a link between the redox state of the quinone pool and gene expression. Antioxid. Redox Signal. 8:781-795.
4. Lynch AS, Lin EC. 1996. Regulation of gene expression in Escherichia coli, p 1526-1538. In Neidhardt FC, Curtis R, Ingraham AL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella: cellular and molecular biology. American Society of Microbiology, Washington, DC.
5. Iuchi S, Lin EC. 1988. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc. Natl. Acad. Sci. U. S. A. 85:1888 -1892.
6. Iuchi S, Matsuda Z, Fujiwara T, Lin EC. 1990. The arcB gene of Escherichia coli encodes a sensor-regulator protein for anaerobic repression of the arc modulon. Mol. Microbiol. 4:715-727.
7. Kwon O, Georgellis D, Lynch AS, Boyd D, Lin EC. 2000. The ArcB sensor kinase of Escherichia coli: genetic exploration of the transmembrane region. J. Bacteriol. 182:2960 -2966.
8. Ishige K, Nagasawa S, Tokishita S, Mizuno T. 1994. A novel device of bacterial signal transducers. EMBO J. 13:5195-5202.
9. Nuñez Oreza LA, Alvarez AF, Arias-Olguín II, Torres Larios A, Georgellis D. 2012. The ArcB leucine zipper domain is required for proper ArcB signaling. PLoS One 7:e38187. doi:10.1371/journal.pone. 0038187.
10. Zhulin IB, Taylor BL, Dixon R. 1997. PAS domain S-boxes in Archaea, Bacteria and sensors for oxygen and redox. Trends Biochem. Sci. 22:331- 333.
11. Peña-Sandoval GR, Georgellis D. 2010. The ArcB sensor kinase of Escherichia coli autophosphorylates by an intramolecular reaction. J. Bacteriol. 192:1735-1739.
12. Georgellis D, Kwon O, Lin EC. 1999. Amplification of signaling activity of the Arc two-component system of Escherichia coli by anaerobic metabolites. An in vitro study with different protein modules. J. Biol. Chem. 274:35950 -35954.
13. Rodriguez C, Kwon O, Georgellis D. 2004. Effect of D-lactate on the physiological activity of the ArcB sensor kinase in Escherichia coli. J. Bacteriol. 186:2085-2090.
14. Kwon O, Georgellis D, Lin EC. 2000. Phosphorelay as the sole physiological route of signal transmission by the arc two-component system of Escherichia coli. J. Bacteriol. 182:3858 -3862.
15. Georgellis D, Lynch AS, Lin EC. 1997. In vitro phosphorylation study of the Arc two-component signal transduction system of Escherichia coli. J. Bacteriol. 179:5429 -5435.
16. Gunsalus RP, Park SJ. 1994. Aerobic-anaerobic gene regulation in Escherichia coli: control by the ArcAB and Fnr regulons. Res. Microbiol. 145: 437-450.
17. Liu X, De Wulf P. 2004. Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J. Biol. Chem. 279:12588 -12597.
18. Lynch AS, Lin EC. 1996. Transcriptional control mediated by the ArcA two-component response regulator protein of Escherichia coli: characterization of DNA binding at target promoters. J. Bacteriol. 178:6238-6249.
19. Alvarez AF, Malpica R, Contreras M, Escamilla E, Georgellis D. 2010. Cytochrome d but not cytochrome o rescues the toluidine blue growth sensitivity of arc mutants of Escherichia coli. J. Bacteriol. 192:391-399.
20. Georgellis D, Kwon O, De Wulf P, Lin EC. 1998. Signal decay through a reverse phosphorelay in the Arc two-component signal transduction system. J. Biol. Chem. 273:32864 -32869.
21. Peña-Sandoval GR, Kwon O, Georgellis D. 2005. Requirement of the receiver and phosphotransfer domains of ArcB for efficient dephosphorylation of phosphorylated ArcA in vivo. J. Bacteriol. 187:3267-3272.
22. Kwon O, Georgellis D, Lin EC. 2003. Rotational on-off switching of a hybrid membrane sensor kinase Tar-ArcB in Escherichia coli. J. Biol. Chem. 278:13192-13195.
23. Georgellis D, Kwon O, Lin EC. 2001. Quinones as the redox signal for the Arc two-component system of bacteria. Science 292:2314 -2316.
24. Malpica R, Franco B, Rodriguez C, Kwon O, Georgellis D. 2004. Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc. Natl. Acad. Sci. U. S. A. 101:13318 -13323.
25. Bekker M, Alexeeva S, Laan W, Sawers G, de Mattos JT, Hellingwerf K. 2010. The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool. J. Bacteriol. 192:746 -754.
26. Rolfe MD, Ter Beek A, Graham AI, Trotter EW, Asif HM, Sanguinetti G, de Mattos JT, Poole RK, Green J. 2011. Transcript profiling and inference of Escherichia coli K-12 ArcA activity across the range of physiologically relevant oxygen concentrations. J. Biol. Chem. 286:10147- 10154.
27. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
28. Iuchi S, Cameron DC, Lin EC. 1989. A second global regulator gene (arcB) mediating repression of enzymes in aerobic pathways of Escherichia coli. J. Bacteriol. 171:868-873.
29. Casadaban MJ. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and mu. J. Mol. Biol. 104:541-555.
30. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008.
31. Bolivar F, Rodriguez RL, Greene PJ, Betlach MC, Heyneker HL, Boyer HW, Crosa JH, Falkow S. 1977. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2:95-113.
32. Dykxhoorn DM, St. Pierre R, Linn T. 1996. A set of compatible tac promoter expression vectors. Gene 177:133-136.
33. Alvarez AF, Georgellis D. 2010. In vitro and in vivo analysis of the ArcB/A redox signaling pathway. Methods Enzymol. 471:205-228.
34. Inaba K, Ito K. 2002. Paradoxical redox properties of DsbB and DsbA in the protein disulfide-introducing reaction cascade. EMBO J. 21:2646- 2654.
35. Szajewski RP, Whitesides GM. 1980. Rate constants and equilibrium constants for thiol-disulfide interchange reactions involving oxidized glutathione. J. Am. Chem. Soc. 102:2011-2026.
36. Wunderlich M, Jaenicke R, Glockshuber R. 1993. The redox properties of protein disulfide isomerase (DsbA) of Escherichia coli result from a tense conformation of its oxidized form. J. Mol. Biol. 233:559-656.
37. Miller JH. 1972. Experiments in molecular genetics, p 352-355. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
38. Søballe B, Poole RK. 1998. Requirement for ubiquinone downstream of cytochrome(s) b in the oxygen-terminated respiratory chains of Escherichia coli K-12 revealed using a null mutant allele of ubiCA. Microbiology 144:361-373.
39. - double quinone mutant. Biochim. Biophys. Acta 461:84 -100.
40. Zhu J, Sánchez A, Bennett GN, San K-Y. 2011. Manipulating respiratory levels in Escherichia coli for aerobic formation of reduced chemical products. Metab. Eng. 13:704 -712.
41. Portnoy V, Scott D, Lewis NE, Tarasova Y, Osterman AL, Palsson Bø. 2010. Deletion of genes encoding cytochrome oxidases and quinol monooxygenase blocks the aerobic-anaerobic shift in Escherichia coli K-12 MG1655. Appl. Environ. Microbiol. 76:6529-6540.
42. Iuchi S, Chepuri V, Fu HA, Gennis RB, Lin EC. 1990. Requirement for terminal cytochromes in generation of the aerobic signal for the Arc regulatory system in Escherichia coli: study utilizing deletions and lac fusions of cyo and cyd. J. Bacteriol. 172:6020-6025.
43. Gonidakis S, Finkel SE, Longo VD. 2011. Lifespan extension and paraquat resistance in a ubiquinone-deficient Escherichia coli mutant depend on transcription factors ArcA and TdcA. Aging 3:291-303.
44. Gennis RB, Stewart V. 1996. Respiration, p 217-261. In Neidhardt FC, et al (ed), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. American Society for Microbiology, Washington, DC.
45. Shestopalov AI, Bogachev AV, Murtazina RA, Viryasov MB, Skulachev VP. 1997. Aeration-dependent changes in composition of the quinone pool in Escherichia coli. Evidence of post-transcriptional regulation of the quinone biosynthesis. FEBS Lett. 404:272-274.