Response regulator ArcA of Salmonella enterica serovar Typhimurium downregulates expression of OmpD, a porin facilitating uptake of hydrogen peroxide

Research in Microbiology

Volumn 162, Issue 2, 2011, Pages 214-222

  Calderón, Iván L ^a   Morales, Eduardo ^a   Caro, Nelson J ^a   Chahúan, Catalina A ^a   Collao, Bernardo ^a   Gil, Fernando ^a   Villarreal, José M ^a   Ipinza, Francisco ^a   Mora, Guido C ^a   Saavedra, Claudia P ^a  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

Author keywords

ArcA; Hydrogen peroxide; OmpD porin

Indexed keywords

AEROBIC RESPIRATION CONTROL PROTEIN A; HYDROGEN PEROXIDE; PORIN; PROTEIN OMPD; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BINDING SITE; DOWN REGULATION; ELECTROPHORETIC MOBILITY; IN VITRO STUDY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEOLIPOSOME; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; WESTERN BLOTTING;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; HYDROGEN PEROXIDE; OXIDATIVE STRESS; PORINS; REPRESSOR PROTEINS; SALMONELLA TYPHIMURIUM;

ARCA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 79952103360     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2010.11.001     Document Type: Article

References (52)

1. Benz R., Ishii J., Nakae T. Determination of ion permeability through the channels made of porins from the outer membrane of Salmonella typhimurium in lipid bilayer membranes. J. Membr. Biol. 1980, 56:19-29.
2. Bienert G.P., Schjoerring J.K., Jahn T.P. Membrane transport of hydrogen peroxide. Biochim. Biophys. Acta. 2006, 1758:994-1003.
3. Bienert G.P., Møller A.L., Kristiansen K.A., Schulz A., Møller I.M., Schjoerring J.K., Jahn T.P. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 2007, 282:1183-1192.
4. Boveris A. Determination of the production of superoxide radicals and hydrogen peroxide in mitochondria. Meth. Enzymol. 1984, 105:429-435.
5. Chopra I., Eccles S.J. Diffusion of tetracycline across the outer membrane of Escherichia coli K-12: involvement of protein Ia. Biochem. Biophys. Res. Commun. 1978, 83:550-557.
6. Christman M.F., Morgan R.W., Jacobson F.S., Ames B.N. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cellule 1985, 41:753-762.
7. Cubillos M.A., Lissi E.A., Abuin E.B. Kinetics of peroxidation of linoleic acid incorporated into DPPC vesicles initiated by the thermal decomposition of 2,2'-azobis(2-amidinopropane) dihydrochloride. Chem. Phys. Lipids. 2001, 112:41-46.
8. Datsenko K.A., Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A 2000, 97:6640-6645.
9. Dé E., Baslé A., Jaquinod M., Saint N., Malléa M., Molle G., Pagès J.M. A new mechanism of antibiotic resistance in Enterobacteriaceae induced by a structural modification of the major porin. Mol. Microbiol. 2001, 41:189-198.
10. De la Cruz M.A., Calva E. The complexities of porin genetic regulation. J. Mol. Microbiol. Biotechnol. 2010, 18:24-36.
11. Doménech-Sánchez A., Martínez-Martínez L., Hernández-Allés S., del Carmen Conejo M., Pascual A., Tomás J.M., Albertí S., Benedí V.J. Role of Klebsiella pneumoniae OmpK35 porin in antimicrobial resistance. Antimicrobial. Agents. Chemother. 2003, 47:3332-3335.
12. Eriksson S., Lucchini S., Thompson A., Rhen M., Hinton J.C. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 2003, 47:103-118.
13. Fridovich I. The biology of oxygen radicals. Science 1978, 201:875-880.
14. Gehring K.B., Nikaido H. Existence and purification of porin heterotrimers of Escherichia coli K12 OmpC, OmpF, and PhoE proteins. J. Biol. Chem. 1989, 264:2810-2815.
15. Georgellis D., Kwon O., De Wulf P., Lin E.C. Signal decay through a reverse phosphorelay in the Arc two-component signal transduction system. J. Biol. Chem. 1998, 273:32864-32869.
16. Georgellis D., Lynch A.S., Lin E.C. In vitro phosphorylation study of the arc two-component signal transduction system of Escherichia coli. J. Bacteriol. 1997, 179:5429-5435.
17. Gil F., Ipinza F., Fuentes J., Fumeron R., Villarreal J.M., Aspée A., Mora G.C., Vásquez C.C., Saavedra C. The ompW (porin) gene mediates methyl viologen (paraquat) efflux in Salmonella enterica serovar Typhimurium. Res. Microbiol. 2007, 158:529-536.
18. Greenberg J.T., Monach P., Chou J.H., Josephy P.D., Demple B. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A 1990, 87:6181-6185.
19. Gutmann L., Williamson R., Moreau N., Kitzis M.D., Collatz E., Acar J.F., Goldstein F.W. Cross-resistance to nalidixic acid, trimethoprim, and chloramphenicol associated with alterations in outer membrane proteins of Klebsiella, Enterobacter, and Serratia. J. Infect. Dis. 1985, 151:501-507.
20. Hu W.S., Lin J.F., Lin Y.H., Chang H.Y. Outer membrane protein STM3031 (Ail/OmpX-like protein) plays a key role in the ceftriaxone resistance of Salmonella enterica serovar Typhimurium. Antimicrobial. Agents. Chemother. 2009, 53:248-255.
21. Ishige K., Nagasawa S., Tokishita S., Mizuno T. A novel device of bacterial signal transducers. EMBO. J. 1994, 13:5195-5202.
22. Iuchi S., Lin E.C. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc. Natl. Acad. Sci. U.S.A 1988, 85:1888-1892.
23. Iuchi S., Matsuda Z., Fujiwara T., Lin E.C. The arcB gene of Escherichia coli encodes a sensor-regulator protein for anaerobic repression of the arc modulon. Mol. Microbiol. 1990, 4:715-727.
24. Jaffe A., Chabbert Y.A., Semonin O. Role of porin proteins OmpF and OmpC in the permeation of beta-lactams. Antimicrobial. Agents. Chemother. 1982, 22:942-948.
25. Jeon Y., Lee Y.S., Han J.S., Kim J.B., Hwang D.S. Multimerization of phosphorylated and non-phosphorylated ArcA is necessary for the response regulator function of the Arc two-component signal transduction system. J. Biol. Chem. 2001, 276:40873-40879.
26. Koebnik R. Proposal for a peptidoglycan-associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins. Mol. Microbiol. 1995, 16:1269-1270.
27. Loui C., Chang A.C., Lu S. Role of the ArcAB two-component system in the resistance of Escherichia coli to reactive oxygen stress. BMC Microbiol 2009, 9:183.
28. Lu S., Killoran P.B., Fang F.C., Riley L.W. The global regulator ArcA controls resistance to reactive nitrogen and oxygen intermediates in Salmonella enterica serovar Enteritidis. Infect. Immun. 2002, 70:451-461.
29. Luchi S., Weiner L. Cellular and molecular physiology of Escherichia coli in the adaptation to aerobic environments. J. Biochem. 1996, 120:1055-1063.
30. Lugtenberg B., van Alphen L. Molecular architecture and functioning of the outer membrane of Escherichia coli and other gram-negative bacteria. Biochim. Biophys. Acta. 1983, 737:51-115.
31. Lynch A.S., Lin E.C. Transcriptional control mediated by the ArcA two-component response regulator protein of Escherichia coli: characterization of DNA binding at target promoters. J. Bacteriol. 1996, 178:6238-6249.
32. Mallea M., Chevalier J., Bornet C., Eyraud A., Davin-Regli A., Bollet C., Pagès J.M. Porin alteration and active efflux: two in vivo drug resistance strategies used by Enterobacter aerogenes. Microbiology 1998, 144:3003-3009.
33. Matsushika A., Mizuno T. A dual-signaling mechanism mediated by the ArcB hybrid sensor kinase containing the histidine-containing phosphotransfer domain in Escherichia coli. J. Bacteriol. 1998, 180:3973-3977.
34. Medeiros A.A., O'Brien T.F., Rosenberg E.Y., Nikaido H. Loss of OmpC porin in a strain of Salmonella typhimurium causes increased resistance to cephalosporins during therapy. J. Infect. Dis. 1987, 156:751-757.
35. Mika F., Hengge R. A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of sigmaS (RpoS) in E. coli. Genes. Dev. 2005, 19:2770-2781.
36. Münch R., Hiller K., Grote A., Scheer M., Klein J., Schobert M., Jahn D. Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 2005, 15:4187-4189.
37. Nikaido H., Rosenberg E.Y. Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins. J. Bacteriol. 1983, 153:241-252.
38. Nikaido H. Transport through the outer membrane of bacteria. Meth. Enzymol. 1986, 125:265-278.
39. Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 2003, 67:593-656.
40. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic. Acids. Res. 2001, 29:e45.
41. Santiviago C.A., Fuentes J.A., Bueno S.M., Trombert A.N., Hildago A.A., Socías L.T., Youderian P., Mora G. The Salmonella enterica sv. Typhimurium smvA, yddG and ompD (porin) genes are required for the efficient efflux of methyl viologen. Mol. Microbiol. 2002, 46:687-698.
42. Santiviago C.A., Toro C.S., Hidalgo A.A., Youderian P., Mora G.C. Global regulation of the Salmonella enterica serovar Typhimurium major porin, OmpD. J. Bacteriol. 2003, 185:5901-5905.
43. Sawai T., Hiruma R., Kawana N., Kaneko M., Taniyasu F., Inami A. Outer membrane permeation of beta-lactam antibiotics in Escherichia coli, Proteus mirabilis, and Enterobacter cloacae. Antimicrobial. Agents. Chemother. 1982, 22:585-592.
44. Sawers G. The aerobic/anaerobic interface. Curr. Opin. Microbiol. 1999, 2:181-187.
45. Seaver L.C., Imlay J.A. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J. Bacteriol. 2001, 183:7182-7189.
46. 2 protects Saccharomyces cerevisiae cells in stationary phase against oxidative stress. FEBS. Lett. 2004, 578:152-156.
47. Sugawara E., Nikaido H. Pore-forming activity of OmpA protein of Escherichia coli. J. Biol. Chem. 1992, 267:2507-2511.
48. Surrey T., Jahnig F. Refolding and oriented insertion of a membrane protein into a lipid bilayer. Proc. Natl. Acad. Sci. U.S.A 1992, 89:7457-7461.
49. Szabó D., Silveira F., Hujer A.M., Bonomo R.A., Hujer K.M., Marsh J.W., Bethel C.R., Doi Y., Deeley K., Paterson D.L. Outer membrane protein changes and efflux pump expression together may confer resistance to ertapenem in Enterobacter cloacae. Antimicrobial. Agents. Chemother. 2006, 50:2833-2835.
50. Toro C.S., Lobos S.R., Calderón I., Rodríguez M., Mora G.C. Clinical isolate of a porinless Salmonella typhi resistant to high levels of chloramphenicol. Antimicrobial. Agents. Chemother. 1990, 34:1715-1719.
51. Uzzau S., Figueroa-Bossi N., Rubino S., Bossi L. Epitope tagging of chromosomal genes in Salmonella. Proc. Natl. Acad. Sci. U.S.A 2001, 98:15264-15269.
52. Wong S.M., Alugupalli K.R., Ram S., Akerley B.J. The ArcA regulon and oxidative stress resistance in Haemophilus influenzae. Mol. Microbiol. 2007, 64:1375-1390.