The Salmonella enterica serovar Typhi ltrR-ompR-ompC-ompF genes are involved in resistance to the bile salt sodium deoxycholate and in bacterial transformation

Molecular Microbiology

Volumn 92, Issue 5, 2014, Pages 1005-1024

  Villarreal, J M ^a   Becerra Lobato, N ^a   Rebollar Flores, J E ^a   Medina Aparicio, L ^a   Carbajal Gomez E ^a   Zavala Garcia M L ^a   Vazquez A ^a   Gutierrez Rios R M ^a   Olvera, L ^a   Encarnacion S ^b   Martinez Batallar A G ^b   Calva, E ^a   Hernandez Lucas I ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^b INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DEOXYCHOLATE SODIUM; LYSR TYPE TRANSCRIPTIONAL REGULATOR; OUTER MEMBRANE PROTEIN C; OUTER MEMBRANE PROTEIN F; OUTER MEMBRANE PROTEIN REGULATOR; PORIN; UNCLASSIFIED DRUG; BILE ACID; DEOXYCHOLIC ACID; OUTER MEMBRANE PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIUM TRANSFORMATION; CONTROLLED STUDY; ENVZ GENE; GENE EXPRESSION PROFILING; GENE MUTATION; GENE REGULATORY NETWORK; LTRR GENE; NONHUMAN; OMPC GENE; OMPF GENE; OMPR GENE; PHYSICAL RESISTANCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; SALMONELLA TYPHI; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI; SALMONELLA TYPHI;

BACTERIAL OUTER MEMBRANE PROTEINS; BILE ACIDS AND SALTS; DEOXYCHOLIC ACID; GENE EXPRESSION REGULATION, BACTERIAL; SALMONELLA TYPHI; TRANSFORMATION, BACTERIAL;

EID: 84901636378     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12610     Document Type: Article

References (94)

1. Achouak, W., Heulin, T., and Pages, J.M. (2001) Multiple facets of bacterial porins. FEMS Microbiol Lett 199: 1-7.
2. - mutants and stabilization of mating aggregates. Mol Gen Genet 164: 171-183.
3. Alphen, W.V., and Lugtenberg, B. (1977) Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J Bacteriol 131: 623-630.
4. Bang, I.S., Kim, B.H., Foster, J.W., and Park, Y.K. (2000) OmpR regulates the stationary-phase acid tolerance response of Salmonella enterica serovar Typhimurium. J Bacteriol 182: 2245-2252.
5. Bang, I.S., Audia, J.P., Park, Y.K., and Foster, J.W. (2002) Autoinduction of the ompR response regulator by acid shock and control of the Salmonella enterica acid tolerance response. Mol Microbiol 44: 1235-1250.
6. Baños, R.C., Martínez, J., Polo, C., Madrid, C., Prenafeta, A., and Juárez, A. (2011) The yfeR gene of Salmonella enterica serovar Typhimurium encodes an osmoregulated LysR-type transcriptional regulator. FEMS Microbiol Lett 315: 63-71.
7. Borum, P.R., and Monty, K.J. (1976) Regulatory mutants and control of cysteine biosynthetic enzymes in Salmonella typhimurium. J Bacteriol 125: 94-101.
8. Brzostek, K., Brzóstkowska, M., Bukowska, I., Karwicka, E., and Raczkowska, A. (2007) OmpR negatively regulates expression of invasin in Yersinia enterocolitica. Microbiology 153: 2416-2425.
9. Cameron, A.D., and Dorman, C.J. (2012) A fundamental regulatory mechanism operating through OmpR and DNA topology controls expression of Salmonella pathogenicity islands SPI-1 and SPI-2. PLoS Genet 8: e1002615.
10. Christman, M.F., Storz, G., and Ames, B.N. (1989) OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc Natl Acad Sci USA 86: 3484-3488.
11. Condemine, G., and Ghazi, A. (2007) Differential regulation of two oligogalacturonate outer membrane channels, KdgN and KdgM, of Dickeya dadantii (Erwinia chrysanthemi). J Bacteriol 189: 5955-5962.
12. Condemine, G., Berrier, C., Plumbridge, J., and Ghazi, A. (2005) Function and expression of an N-acetylneuraminic acid-inducible outer membrane channel in Escherichia coli. J Bacteriol 187: 1959-1965.
13. Coynault, C., Robbe-Saule, V., Popoff, M.Y., and Norel, F. (1992) Growth phase and SpvR regulation of transcription of Salmonella typhimurium spvABC virulence genes. Microb Pathog 13: 133-143.
14. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
15. De la Cruz, M.A., Fernández-Mora, M., Guadarrama, C., Flores-Valdez, M.A., Bustamante, V.H., Vázquez, A., and Calva, E. (2007) LeuO antagonizes H-NS and StpA-dependent repression in Salmonella enterica ompS1. Mol Microbiol 66: 727-743.
16. Deiwick, J., Nikolaus, T., Erdogan, S., and Hensel, M. (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31: 1759-1773.
17. Dillon, S.C., Espinosa, E., Hokamp, K., Ussery, D.W., Casadesús, J., and Dorman, C.J. (2012) LeuO is a global regulator of gene expression in Salmonella enterica serovar Typhimurium. Mol Microbiol 85: 1072-1089.
18. Encarnación, S., Guzmán, Y., Dunn, M.F., Hernández, M., del Carmen Vargas, M., and Mora, J. (2003) Proteome analysis of aerobic and fermentative metabolism in Rhizobium etli CE3. Proteomics 3: 1077-1085.
19. Encarnación, S., Hernández, M., Martínez-Batallar, G., Contreras, S., Vargas Mdel, C., and Mora, J. (2005) Comparative proteomics using 2-D gel electrophoresis and mass spectrometry as tools to dissect stimulons and regulons in bacteria with sequenced or partially sequenced genomes. Biol Proced Online 7: 117-135.
20. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M., and Hinton, J.C. (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103-118.
21. Fang, M., Majumder, A., Tsai, K.J., and Wu, H.Y. (2000) ppGpp-dependent leuO expression in bacteria under stress. Biochem Biophys Res Commun 276: 64-70.
22. Fernández-Mora, M., Puente, J.L., and Calva, E. (2004) OmpR and LeuO positively regulate the Salmonella enterica serovar Typhi ompS2 porin gene. J Bacteriol 186: 2909-2920.
23. Flamez, C., Ricard, I., Arafah, S., Simonet, M., and Marceau, M. (2008) Phenotypic analysis of Yersinia pseudotuberculosis 32777 response regulator mutants: new insights into two-component system regulon plasticity in bacteria. Int J Med Microbiol 298: 193-207.
24. Galdiero, S., Falanga, A., Cantisani, M., Tarallo, R., Della Pepa, M.E., D'Oriano, V., and Galdiero, M. (2012) Microbe-host interactions: structure and role of Gram-negative bacterial porins. Curr Protein Pept Sci 13: 843-854.
25. Gallego-Hernández, A.L., Hernández-Lucas, I., De la Cruz, M.A., Olvera, L., Morett, E., Medina-Aparicio, L., etal. (2012) Transcriptional regulation of the assT-dsbL-dsbI gene cluster in Salmonella enterica serovar Typhi IMSS-1 depends on LeuO, H-NS, and specific growth conditions. J Bacteriol 194: 2254-2264.
26. Gao, H., Zhang, Y., Yang, L., Liu, X., Guo, Z., Tan, Y., etal. (2011) Regulatory effects of cAMP receptor protein (CRP) on porin genes and its own gene in Yersinia pestis. BMC Microbiol 11: 40.
27. Hall, M.N., and Silhavy, T.J. (1981) Genetic analysis of the ompB locus in Escherichia coli K-12. J Mol Biol 151: 1-15.
28. Hansen, M.R., Tranekjaer Jørgensen, J., and Dandanell, G. (2006) Xanthosine utilization in Salmonella enterica serovar Typhimurium is recovered by a single aspartate-to-glycine substitution in xanthosine phosphorylase. J Bacteriol 188: 4153-4157.
29. Hernández, S.B., Cota, I., Ducret, A., Aussel, L., and Casadesús, J. (2012) Adaptation and preadaptation of Salmonella enterica to Bile. PLoS Genet 8: e1002459.
30. Hernández-Lucas, I., Gallego-Hernández, A.L., Encarnación, S., Fernández-Mora, M., Martínez-Batallar, A.G., Salgado, H., etal. (2008) The LysR-type transcriptional regulator LeuO controls expression of several genes in Salmonella enterica serovar Typhi. J Bacteriol 190: 1658-1670.
31. Hirakawa, H., Nishino, K., Hirata, T., and Yamaguchi, A. (2003) Comprehensive studies of drug resistance mediated by overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J Bacteriol 185: 1851-1856.
32. Huang, L., Tsui, P., and Freundlich, M. (1992) Positive and negative control of ompB transcription in Escherichia coli by cyclic AMP and the cyclic AMP receptor protein. J Bacteriol 174: 664-670.
33. Hurkman, W.J., and Tanaka, C.K. (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81: 802-806.
34. Isibasi, A., Ortíz-Navarrete, V., Paniagua, J., Pelayo, R., González, C.R., García, J.A., and Kumate, J. (1992) Active protection of mice against Salmonella typhi by immunization with strain-specific porins. Vaccine 10: 811-813.
35. Jakomin, M., Chessa, D., Baumler, A.J., and Casadesús, J. (2008) Regulation of the Salmonella enterica std fimbrial operon by DNA adenine methylation, SeqA, and HdfR. J Bacteriol 190: 7406-7413.
36. Jennings, M.E., Quick, L.N., Soni, A., Davis, R.R., Crosby, K., Ott, C.M., etal. (2011) Characterization of the Salmonella enterica serovar Typhimurium ydcI gene, which encodes a conserved DNA binding protein required for full acid stress resistance. J Bacteriol 193: 2208-2217.
37. Kawaji, H., Mizuno, T., and Mizushima, S. (1979) Influence of molecular size and osmolarity of sugars and dextrans on the synthesis of outer membrane proteins O-8 and O-9 of Escherichia coli K-12. J Bacteriol 140: 843-847.
38. Kenney, L.J., Bauer, M.D., and Silhavy, T.J. (1995) Phosphorylation-dependent conformational changes in OmpR, an osmoregulatory DNA-binding protein of Escherichia coli. Proc Natl Acad Sci USA 92: 8866-8870.
39. Kim, M.J., Lim, S., and Ryu, S. (2008) Molecular analysis of the Salmonella Typhimurium tdc operon regulation. J Microbiol Biotechnol 18: 1024-1032.
40. Klimke, W.A., and Frost, L.S. (1998) Genetic analysis of the role of the transfer gene, traN, of the F and R100-1 plasmids in mating pair stabilization during conjugation. J Bacteriol 180: 4036-4043.
41. Klimke, W.A., Rypien, C.D., Klinger, B., Kennedy, R.A., Rodríguez-Maillard, J.M., and Frost, L.S. (2005) The mating pair stabilization protein, TraN, of the F plasmid is an outer-membrane protein with two regions that are important for its function in conjugation. Microbiology 151: 3527-3540.
42. Kovacikova, G., and Skorupski, K. (2001) Overlapping binding sites for the virulence gene regulators AphA, AphB and cAMP-CRP at the Vibrio cholerae tcpPH promoter. Mol Microbiol 41: 393-407.
43. Kumar, A., Gart, E., Nagaraja, T.G., and Narayanan, S. (2013) Adhesion of Fusobacterium necrophorum to bovine endothelial cells is mediated by outer membrane proteins. Vet Microbiol 162: 813-818.
44. Kumar, S., Kumar, S., and Kumar, S. (2006) Infection as a risk factor for gallbladder cancer. J Surg Oncol 93: 633-639.
45. Lacroix, F.J., Cloeckaert, A., Grepinet, O., Pinault, C., Popoff, M.Y., Waxin, H., and Pardon, P. (1996) Salmonella typhimurium acrB-like gene: identification and role in resistance to biliary salts and detergents and in murine infection. FEMS Microbiol Lett 135: 161-167.
46. Lahiri, A., Das, P., and Chakravortty, D. (2008) The LysR-type transcriptional regulator Hrg counteracts phagocyte oxidative burst and imparts survival advantage to Salmonella enterica serovar Typhimurium. Microbiology 154: 2837-2846.
47. Lahiri, A., Ananthalakshmi, T.K., Nagarajan, A.G., Ray, S., and Chakravortty, D. (2011) TolA mediates the differential detergent resistance pattern between the Salmonella enterica subsp. enterica serovars Typhi and Typhimurium. Microbiology 157: 1402-1415.
48. Langridge, G.C., Phan, M.D., Turner, D.J., Perkins, T.T., Parts, L., Haase, J., etal. (2009) Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res 19: 2308-2316.
49. Lawley, T.D., Chan, K., Thompson, L.J., Kim, C.C., Govoni, G.R., and Monack, D.M. (2006) Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2: e11.
50. Lee, A.K., Detweiler, C.S., and Falkow, S. (2000) OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J Bacteriol 182: 771-781.
51. Lewis, J.A., Stamper, L.W., and Escalante-Semerena, J.C. (2009) Regulation of expression of the tricarballylate utilization operon (tcuABC) of Salmonella enterica. Res Microbiol 160: 179-186.
52. López-Garrido, J., Cheng, N., García-Quintanilla, F., García-del Portillo, F., and Casadesús, J. (2010) Identification of the Salmonella enterica damX gene product, an inner membrane protein involved in bile resistance. J Bacteriol 192: 893-895.
53. Maddocks, S.E., and Oyston, P.C. (2008) Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154: 3609-3623.
54. Martínez-Flores, I., Cano, R., Bustamante, V.H., Calva, E., and Puente, J.L. (1999) The ompB operon partially determines differential expression of OmpC in Salmonella typhi and Escherichia coli. J Bacteriol 181: 556-562.
55. Martínez-Laguna, Y., Calva, E., and Puente, J.L. (1999) Autoactivation and environmental regulation of bfpT expression, the gene coding for the transcriptional activator of bfpA in enteropathogenic Escherichia coli. Mol Microbiol 33: 153-166.
56. Mayer, M.P. (1995) A new set of useful cloning and expression vectors derived from pBlueScript. Gene 163: 41-46.
57. Medeiros, A.A., O'Brien, T.F., Rosenberg, E.Y., and Nikaido, H. (1987) Loss of OmpC porin in a strain of Salmonella typhimurium causes increased resistance to cephalosporins during therapy. J Infect Dis 156: 751-757.
58. Medina-Aparicio, L., Rebollar-Flores, J.E., Gallego-Hernández, A.L., Vázquez, A., Olvera, L., Gutiérrez-Ríos, R.M., etal. (2011) The CRISPR/Cas immune system is an operon regulated by LeuO, H-NS, and leucine-responsive regulatory protein in Salmonella enterica serovar Typhi. J Bacteriol 193: 2396-2407.
59. Mendoza-Vargas, A., Olvera, L., Olvera, M., Grande, R., Vega-Alvarado, L., Taboada, B., etal. (2009) Genome-wide identification of transcription start sites, promoters and transcription factor binding sites in E. coli. PLoS ONE 4: e7526.
60. Miller, V.L., and Mekalanos, J.J. (1988) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170: 2575-2583.
61. Moreno-Eutimio, M.A., Tenorio-Calvo, A., Pastelin-Palacios, R., Pérez-Shibayama, C., Gil-Cruz, C., López-Santiago, R., etal. (2013) Salmonella Typhi OmpS1 and OmpS2 porins are potent protective immunogens with adjuvant properties. Immunology 139: 459-471.
62. Murata, T., Tseng, W., Guina, T., Miller, S.I., and Nikaido, H. (2007) PhoPQ-mediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar Typhimurium. J Bacteriol 189: 7213-7222.
63. Nikaido, H. (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67: 593-656.
64. Nishino, K., Latifi, T., and Groisman, E.A. (2006) Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol Microbiol 59: 126-141.
65. Oropeza, R., and Calva, E. (2009) The cysteine 354 and 277 residues of Salmonella enterica serovar Typhi EnvZ are determinants of autophosphorylation and OmpR phosphorylation. FEMS Microbiol Lett 292: 282-290.
66. Oropeza, R., Sampieri, C.L., Puente, J.L., and Calva, E. (1999) Negative and positive regulation of the non-osmoregulated ompS1 porin gene in Salmonella typhi: a novel regulatory mechanism that involves OmpR. Mol Microbiol 32: 243-252.
67. Pareja, E., Pareja-Tobes, P., Manrique, M., Pareja-Tobes, E., Bonal, J., and Tobes, R. (2006) ExtraTrain: a database of extragenic regions and transcriptional information in prokaryotic organisms. BMC Microbiol 6: 29.
68. Prieto, A.I., Ramos-Morales, F., and Casadesús, J. (2004) Bile-induced DNA damage in Salmonella enterica. Genetics 168: 1787-1794.
69. Prieto, A.I., Ramos-Morales, F., and Casadesús, J. (2006) Repair of DNA damage induced by bile salts in Salmonella enterica. Genetics 174: 575-584.
70. Prieto, A.I., Jakomin, M., Segura, I., Pucciarelli, M.G., Ramos-Morales, F., García-Del Portillo, F., and Casadesús, J. (2007) The GATC-binding protein SeqA is required for bile resistance and virulence in Salmonella enterica serovar Typhimurium. J Bacteriol 189: 8496-8502.
71. Prieto, A.I., Hernández, S.B., Cota, I., Pucciarelli, M.G., Orlov, Y., Ramos-Morales, F., etal. (2009) Roles of the outer membrane protein AsmA of Salmonella enterica in the control of marRAB expression and invasion of epithelial cells. J Bacteriol 191: 3615-3622.
72. Prouty, A.M., Van Velkinburgh, J.C., and Gunn, J.S. (2002) Salmonella enterica serovar Typhimurium resistance to bile: identification and characterization of the tolQRA cluster. J Bacteriol 184: 1270-1276.
73. Prouty, A.M., Brodsky, I.E., Falkow, S., and Gunn, J.S. (2004) Bile-salt-mediated induction of antimicrobial and bile resistance in Salmonella typhimurium. Microbiology 150: 775-783.
74. Puente, J.L., Flores, V., Fernández, M., Fuchs, Y., and Calva, E. (1987) Isolation of an ompC-like outer membrane protein gene from Salmonella typhi. Gene 61: 75-83.
75. Puente, J.L., Verdugo-Rodríguez, A., and Calva, E. (1991) Expression of Salmonella typhi and Escherichia coli OmpC is influenced differently by medium osmolarity; dependence on Escherichia coli OmpR. Mol Microbiol 5: 1205-1210.
76. Puente, J.L., Juárez, D., Bobadilla, M., Arias, C.F., and Calva, E. (1995) The Salmonella ompC gene: structure and use as a carrier for heterologous sequences. Gene 156: 1-9.
77. Ramos-Morales, F., Prieto, A.I., Beuzón, C.R., Holden, D.W., and Casadesús, J. (2003) Role for Salmonella enterica enterobacterial common antigen in bile resistance and virulence. J Bacteriol 185: 5328-5332.
78. Rodríguez-Morales, O., Fernández-Mora, M., Hernández-Lucas, I., Vázquez, A., Puente, J.L., and Calva, E. (2006) Salmonella enterica serovar Typhimurium ompS1 and ompS2 mutants are attenuated for virulence in mice. Infect Immun 74: 1398-1402.
79. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
80. Sato, M., Machida, K., Arikado, E., Saito, H., Kakegawa, T., and Kobayashi, H. (2000) Expression of outer membrane proteins in Escherichia coli growing at acid pH. Appl Environ Microbiol 66: 943-947.
81. Schell, M.A. (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47: 597-626.
82. Secundino, I., López-Macías, C., Cervantes-Barragán, L., Gil-Cruz, C., Ríos-Sarabia, N., Pastelin-Palacios, R., etal. (2006) Salmonella porins induce a sustained, lifelong specific bactericidal antibody memory response. Immunology 117: 59-70.
83. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
84. Shin, S., and Park, C. (1995) Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol 177: 4696-4702.
85. Tartera, C., and Metcalf, E.S. (1993) Osmolarity and growth phase overlap in regulation of Salmonella typhi adherence to and invasion of human intestinal cells. Infect Immun 61: 3084-3089.
86. Tenor, J.L., McCormick, B.A., Ausubel, F.M., and Aballay, A. (2004) Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr Biol 14: 1018-1024.
87. Tewari, M., Mishra, R.R., and Shukla, H.S. (2010) Salmonella typhi and gallbladder cancer: report from an endemic region. Hepatobiliary Pancreat Dis Int 9: 524-530.
88. Thanassi, D.G., Cheng, L.W., and Nikaido, H. (1997) Active efflux of bile salts by Escherichia coli. J Bacteriol 179: 2512-2518.
89. Turnbull, A.L., Kim, W., and Surette, M.G. (2012) Transcriptional regulation of sdiA by cAMP-receptor protein, LeuO, and environmental signals in Salmonella enterica serovar Typhimurium. Can J Microbiol 58: 10-22.
90. van Velkinburgh, J.C., and Gunn, J.S. (1999) PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect Immun 67: 1614-1622.
91. Vidal, O., Longin, R., Prigent-Combaret, C., Dorel, C., Hooreman, M., and Lejeune, P. (1998) Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J Bacteriol 180: 2442-2449.
92. Wang, R.F., and Kushner, S.R. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.
93. Washburn, M.P., Wolters, D., and Yates, J.R. (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19: 242-247.
94. Yuan, J., Wei, B., Shi, M., and Gao, H. (2011) Functional assessment of EnvZ/OmpR two-component system in Shewanella oneidensis. PLoS ONE 6: e23701.