Increased production of pyruvic acid by Escherichia coli RNase G mutants in combination with cra mutations

Applied Microbiology and Biotechnology

Volumn 76, Issue 1, 2007, Pages 183-192

  Sakai, Taro ^a   Nakamura, Naoko ^a   Umitsuki, Genryou ^a   Nagai, Kazuo ^b   Wachi, Masaaki ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b CHUBU UNIVERSITY   (Japan)

Author keywords

Glycolysis; Pyruvic acid; RNase G; Valine

Indexed keywords

ACETOHYDROXY ACID SYNTHASE; ENDORIBONUCLEASE; PYRUVIC ACID; RNASE G; VALINE;

DERIVATIVES; ENZYME KINETICS; ESCHERICHIA COLI; GLUCOSE; MUTAGENESIS; RNA;

ORGANIC ACIDS;

ACETOLACTATE SYNTHASE; GLUCOSE; ISOLEUCINE; PYRUVIC ACID; RIBONUCLEASE; RIBONUCLEASE G; UNCLASSIFIED DRUG; VALINE;

BIODEGRADATION; CHEMICAL COMPOUND; COLIFORM BACTERIUM; ENZYME; GENETIC ANALYSIS; GLUCOSE; MUTATION; NUCLEIC ACID; ORGANIC ACID; RNA;

ARTICLE; ESCHERICHIA COLI; GENE MUTATION; GENETIC ANALYSIS; GLUCONEOGENESIS; GLYCOLYSIS; NONHUMAN; TRANSCRIPTION REGULATION;

ACETOLACTATE SYNTHASE; BACTERIAL PROTEINS; CULTURE MEDIA; ENDORIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; GLYCOLYSIS; ISOENZYMES; MUTATION; PYRUVIC ACID; REGULATORY ELEMENTS, TRANSCRIPTIONAL; REPRESSOR PROTEINS; VALINE;

ESCHERICHIA COLI;

EID: 34547563840     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-007-1006-9     Document Type: Article

References (93)

1. Apirion D (1978) Isolation, genetic mapping, and some characterization of a mutation in Escherichia coli that affects the processing of ribonucleic acids. Genetics 90:659-671
2. Arnold TE, Yu J, Belasco JG (1998) Importance of a 5′ stem-loop for longevity of papA mRNA in Escherichia coli. J Bacteriol 181:3587-3590
3. Bailey JE (1991) Toward a science of metabolic engineering. Science 252:1668-1675
4. Bailey JE, Sburlati A, Hatzimanikatis V, Lee K, Renner WA, Tsai PS (1996) Inverse metabolic engineering: a strategy for directed genetic engineering of useful phenotypes. Biotechnol Bioeng 52:109-121
5. Barak Z, Chipman DM, Gollop N (1987) Physiological implications of the specificity of acetohydroxy acid synthase isozymes of enteric bacteria. J Bacteriol 169:3750-3756
6. Bardey V, Vallet C, Robas N, Charpentier B, Thouvenot B, Mougin A, Hajnsdorf E, Régnier P, Springer M, Branlant C (2005) Characterization of the molecular mechanisms involved in the differential production of erythrose-4-phosphate dehydrogenase, 3-phosphoglycerate kinase and class II fructose-1,6-bisphosphate aldolase in Escherichia coli. Mol Microbiol 57:1265-1287
7. Beppu T (2000) Development of applied microbiology to modern biotechnology in Japan. Adv Biochem Eng Biotechnol 69:41-70
8. Blatt JM, Pledger WJ, Umbarger HE (1972) Isoleucine and valine metabolism in Escherichia coli. XX. Multiple forms of acetohydroxy acid synthetase. Biochem Biophys Res Commun 48:444-450
9. Bledig SA, Ramseier TM, Saier MH (1996) FruR mediates catabolite activation of pyruvate kinase (pykF) gene expression in Escherichia coli. J Bacteriol 178:280-283
10. Bouvet P, Belasco JG (1992) Control of RNase E-mediated RNA degradation by 5′-terminal base pairing in E. coli. Nature 360:488-491
11. Braun F, Le Derout J, Régnier P (1998) Ribosomes inhibit an RNase E cleavage which induces the decay of the rpsO mRNA of Escherichia coli. EMBO J 17:4790-4797
12. Briant DJ, Hankins JS, Cook MA, Mackie GA (2003) The quaternary structure of RNase G from Escherichia coli. Mol Microbiol 50:1381-1390
13. Callaghan AJ, Grossmann JG, Redko YU, Ilag LL, Moncrieffe MC, Symmons MF, Robinson CV, McDowall KJ, Luisi BF (2003) Quaternary structure and catalytic activity of the Escherichia coli ribonuclease E amino-terminal catalytic domain. Biochemistry 42:13848-13855
14. Carrier TA, Keasling JD (1997) Controlling messenger RNA stability in bacteria: strategies for engineering gene expression. Biotechnol Prog 13:699-708
15. Carrier TA, Keasling JD (1999) Library of synthetic 5′ secondary structures to manipulate mRNA stability in Escherichia coli. Biotechnol Prog 15:58-64
16. Casadaban MJ, Cohen SN (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol 138:179-207
17. Causey TB, Shanmugam KT, Yomano LP, Ingram LO (2004) Engineering Escherichia coli for efficient conversion of glucose to pyruvate. Proc Natl Acad Sci USA 101:2235-2240
18. 32. J Bacteriol 176:830-839
19. Charpentier B, Bardey V, Robas N, Branlant C (1998) The EIIGlc protein is involved in glucose-mediated activation of Escherichia coli gapA and gapB-pgk transcription. J Bacteriol 180:6476-6483
20. Cheng ZF, Zuo Y, Li Z, Rudd KE, Deutscher MP (1998) The vacB gene required for virulence in Shigella flexneri and Escherichia coli encodes the exoribonuclease RNase R. J Biol Chem 273:14077-14080
21. Deana A, Belasco JG (2004) The function of RNase G in Escherichia coli is constrained by its amino and carboxyl termini. Mol Microbiol 51:1205-1217
22. Deana A, Belasco JG (2005) Lost in translation: the influence of ribosomes on bacterial mRNA decay. Genes Dev 19:2526-2533
23. Deutscher MP (2006) Degradation of RNA in bacteria: comparison of mRNA and stable RNA. Nucleic Acids Res 34:659-666
24. Diwa A, Bricker AL, Jain C, Belasco JG (2000) An evolutionarily conserved RNA stem-loop functions as a sensor that directs feedback regulation of RNase E gene expression. Genes Dev 14:1249-1260
25. Donovan WP, Kushner SR (1986) Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc Natl Acad Sci USA 83:120-124
26. Emmerling M, Bailey JE, Sauer U (1999) Glucose catabolism of Escherichia coli strains with increased activity and altered regulation of key glycolytic enzymes. Metab Eng 1:117-127
27. Emmerling M, Bailey JE, Sauer U (2000) Altered regulation of pyruvate kinase or co-overexpression of phosphofructokinase increases glycolytic fluxes in resting Escherichia coli. Biotechnol Bioeng 67:623-627
28. Emory SA, Bouvet P, Belasco JG (1992) A 5′-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev 6:135-148
29. Englesberg E, Wilcox G (1974) Regulation: positive control. Annu Rev Genet 8:219-242
30. Favre R, Wiater A, Puppo S, Iaccarino M (1976) Expression of a valine-resistant acetolactate synthase activity mediated by the ilvO and ilvG genes of Escherichia coli K-12. Mol Gen Genet 143:243-252
31. Feng Y, Vickers TA, Cohen SN (2002) The catalytic domain of RNase E shows inherent 3′ to 5′ directionality in cleavage site selection. Proc Natl Acad Sci USA 99:14746-14751
32. Ghora BK, Apirion D (1978) Structural analysis and in vitro processing to p5 rRNA of a 9S RNA molecule isolated from an rne mutant of E. coli. Cell 15:1055-1066
33. Hagihira H, Wilson TH, Lin EC (1963) Studies on the glucose-transport system in Escherichia coli with alpha-methyl glucoside as substrate. Biochim Biophys Acta 78:505-515
34. Ikeda M (2003) Amino acid production processes. In: Scheper T, Faurie R, Thommel J (eds) Advances in biochemical engineering/biotechnology, vol 79. Springer, Berlin Heidelberg New York, pp 1-35
35. Jain C (2002) Degradation of mRNA in Escherichia coli. IUBMB Life 54:315-321
36. Jiang X, Belasco JG (2004) Catalytic activation of multimeric RNase E and RNase G by 5′-monophosphorylated RNA. Proc Natl Acad Sci USA 101:9211-9216
37. Jiang X, Diwa A, Belasco JG (2000) Regions of RNase E important for 5′-end-dependent RNA cleavage and autoregulated synthesis. J Bacteriol 182:2468-2475
38. Kaberdin VR, Bläsi U (2006) Translation initiation and the fate of bacterial mRNAs. FEMS Microbiol Rev 30:967-979
39. Kaga N, Umitsuki G, Clark DP, Nagai K, Wachi M (2002a) Extensive overproduction of the AdhE protein by rng mutations depends on mutations in the cra gene or in the Cra-box of the adhE promoter. Biochem Biophys Res Commun 295:92-97
40. Kaga N, Umitsuki G, Nagai K, Wachi M (2002b) RNase G-dependent degradation of the eno mRNA encoding a glycolysis enzyme enolase in Escherichia coli. Biosci Biotechnol Biochem 66:2216-2220
41. Kawamoto H, Morita T, Shimizu A, Inada T, Aiba H (2005) Implication of membrane localization of target mRNA in the action of a small RNA: mechanism of post-transcriptional regulation of glucose transporter in Escherichia coli. Genes Dev 19:328-338
42. Kimata K, Tanaka Y, Inada T, Aiba H (2001) Expression of the glucose transporter gene, ptsG, is regulated at the mRNA degradation step in response to glycolytic flux in Escherichia coli. EMBO J 20:3587-3595
43. Kushner SR (2004) mRNA decay in prokaryotes and eukaryotes: different approaches to a similar problem. IUBMB Life 56:585-594
44. Lago CT, Sannia G, Marino G, Squires CH, Calvo JM, De Felice M (1985) The ilvIH operon of Escherichia coli K-12. Identification of the gene products and recognition of the translational start by polypeptide microsequencing. Biochim Biophys Acta 824:74-79
45. Lawther RP, Calhoun DH, Adams CW, Hauser CA, Gray J, Hatfield GW (1981) Molecular basis of valine resistance in Escherichia coli K-12. Proc Natl Acad Sci USA 78:922-925
46. Leavitt RI, Umbarger HE (1962) Isoleucine and valine metabolism in Escherichia coli. XI. Valine inhibition of the growth of Escherichia coli strain K-12. J Bacteriol 83:624-630
47. Lee K, Bernstein JA, Cohen SN (2002) RNase G complementation of rne null mutation identifies functional interrelationships with RNase E in Escherichia coli. Mol Microbiol 43:1445-1456
48. Leuchtenberger W, Huthmacher K, Drauz K (2005) Biotechnological production of amino acids and derivatives: current status and prospects. Appl Microbiol Biotechnol 69:1-8
49. Li Z, Deutscher MP (2002) RNase E plays an essential role in the maturation of Escherichia coli tRNA precursors. RNA 8:97-109
50. Li Z, Pandit S, Deutscher MP (1999) RNase G (CafA protein) and RNase E are both required for the 5′ maturation of 16S ribosomal RNA. EMBO J 18:2878-2885
51. Li Y, Chen J, Lun SY (2001) Biotechnological production of pyruvic acid. Appl Microbiol Biotechnol 57:451-459
52. Lin-Chao S, Wong TT, McDowall KJ, Cohen SN (1994) Effects of nucleotide sequence on the specificity of rne-dependent and RNase E-mediated cleavages of RNA I encoded by the pBR322 plasmid. J Biol Chem 269:10797-10803
53. Liu JY, Miller PF, Gosink M, Olson ER (1999) The identification of a new family of sugar efflux pumps in Escherichia coli. Mol Microbiol 31:1845-1851
54. Lopez PJ, Marchand I, Joyce SA, Dreyfus M (1999) The C-terminal half of RNase E, which organizes the Escherichia coli degradosome, participates in mRNA degradation but not rRNA processing in vivo. Mol Microbiol 33:188-199
55. Mackie GA (1998) Ribonuclease E is a 5′-end-dependent endonuclease. Nature 395:720-723
56. Mackie GA, Genereaux JL, Masterman SK (1997) Modulation of the activity of RNase E in vitro by RNA sequences and secondary structures 5′ to cleavage sites. J Biol Chem 272:609-616
57. Majumder A, Fang M, Tsai KJ, Ueguchi C, Mizuno T, Wu HY (2001) LeuO expression in response to starvation for branched-chain amino acids. J Biol Chem 276:19046-19051
58. McDowall KJ, Lin-Chao S, Cohen SN (1994) A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J Biol Chem 269:10790-10796
59. Meyer D, Schneider-Fresenius C, Horlacher R, Peist R, Boos W (1997) Molecular characterization of glucokinase from Escherichia coli K-12. J Bacteriol 179:1298-1306
60. Naureckiene S, Uhlin BE (1996) In vitro analysis of mRNA processing by RNase E in the pap operon of Escherichia coli. Mol Microbiol 21:55-68
61. Nègre D, Bonod-Bidaud C, Geourjon C, Deleage G, Cozzone AJ, Cortay JC (1996) Definition of a consensus DNA-binding site for the Escherichia coli pleiotropic regulatory protein, FruR. Mol Microbiol 21:257-266
62. Nègre D, Oudot C, Prost JF, Murakami K, Ishihama A, Cozzone AJ, Cortay JC (1998) FruR-mediated transcriptional activation at the ppsA promoter of Escherichia coli. J Mol Biol 276:355-365
63. Nilsson P, Naureckiene S, Uhlin BE (1996) Mutations affecting mRNA processing and fimbrial biogenesis in the Escherichia coli pap operon. J Bacteriol 178:683-690
64. Oh MK, Liao JC (2000) Gene expression profiling by DNA microarrays and metabolic fluxes in Escherichia coli. Biotechnol Prog 16:278-286
65. Ono M, Kuwano M (1979) A conditional lethal mutation in an Escherichia coli strain with a longer chemical lifetime of messenger RNA. J Mol Biol 129:343-357
66. Ow MC, Kushner SR (2002) Initiation of tRNA maturation by RNase E is essential for cell viability in E. coli. Genes Dev 16:1102-1115
67. Ow MC, Perwez T, Kushner SR (2003) RNase G of Escherichia coli exhibits only limited functional overlap with its essential homologue, RNase E. Mol Microbiol 49:607-622
68. Peng L, Shimizu K (2003) Global metabolic regulation analysis for Escherichia coli K12 based on protein expression by 2-dimensional electrophoresis and enzyme activity measurement. Appl Microbiol Biotechnol 61:163-178
69. Perrenoud A, Sauer U (2005) Impact of global transcriptional regulation by ArcA, ArcB, Cra, Crp, Cya, Fnr, and Mlc on glucose catabolism in Escherichia coli. J Bacteriol 187:3171-3179
70. Pfleger BF, Pitera DJ, Smolke CD, Keasling JD (2006) Combinatorial engineering of intergenic regions in operons tunes expression of multiple genes. Nat Biotechnol 24:1027-1032
71. Ramseier TM (1996) Cra and the control of carbon flux via metabolic pathways. Res Microbiol 147:489-493
72. Ramseier TM, Nègre D, Cortay JC, Scarabel M, Cozzone AJ, Saier MH Jr (1993) In vitro binding of the pleiotropic transcriptional regulatory protein, FruR, to the fru, pps, ace, pts and icd operons of Escherichia coli and Salmonella typhimurium. J Mol Biol 234:28-44
73. Ramseier TM, Bledig S, Michotey V, Feghali R, Saier MH Jr (1995) The global regulatory protein FruR modulates the direction of carbon flow in Escherichia coli. Mol Microbiol 16:1157-1169
74. Ryu S, Ramseier TM, Michotey V, Saier MH Jr, Garges S (1995) Effect of the FruR regulator on transcription of the pts operon in Escherichia coli. J Biol Chem 270:2489-2496
75. Saier MH Jr, Ramseier TM (1996) The catabolite repressor/activator (Cra) protein of enteric bacteria. J Bacteriol 178:3411-3417
76. Shimada T, Fujita N, Maeda M, Ishihama A (2005) Systematic search for the Cra-binding promoters using genomic SELEX system. Genes Cells 10:907-918
77. Smolke CD, Keasling JD (2002) Effect of gene location, mRNA secondary structures, and RNase sites on expression of two genes in an engineered operon. Biotechnol Bioeng 80:762-776
78. Söderbom F, Svard SG, Kirsebom LA (2005) RNase E cleavage in the 5′ leader of a tRNA precursor. J Mol Biol 352:22-27
79. Somers JM, Amzallag A, Middleton RB (1973) Genetic fine structure of the leucine operon of Escherichia coli K-12. J Bacteriol 113:1268-1272
80. Stahl FW, Kobayashi I, Thaler D, Stahl MM (1986) Direction of travel of RecBC recombinase through bacteriophage lambda DNA. Genetics 113:215-227
81. Stephanopoulos G, Vallino JJ (1991) Network rigidity and metabolic engineering in metabolite overproduction. Science 252:1675-1681
82. Swartz JR (2001) Advances in Escherichia coli production of therapeutic proteins. Curr Opin Biotechnol 12:195-201
83. Tock MR, Walsh AP, Carroll G, McDowall KJ (2000) The CafA protein required for the 5′-maturation of 16 S rRNA is a 5′-end-dependent ribonuclease that has context-dependent broad sequence specificity. J Biol Chem 275:8726-8732
84. Umitsuki G, Wachi M, Takada A, Hikichi T, Nagai K (2001) Involvement of RNase G in in vivo mRNA metabolism in Escherichia coli. Genes Cells 6:403-410
85. Vanderpool CK, Gottesman S (2004) Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54:1076-1089
86. Vassinova N, Kozyrev D (2000) A method for direct cloning of fur-regulated genes: identification of seven new fur-regulated loci in Escherichia coli. Microbiology 146:3171-3182
87. Wachi M, Doi M, Okada Y, Matsuhashi M (1989) New mre genes mreC and mreD, responsible for formation of the rod shape of Escherichia coli cells. J Bacteriol 171:6511-6516
88. Wachi M, Umitsuki G, Nagai K (1997) Functional relationship between Escherichia coli RNase E and the CafA protein. Mol Gen Genet 253:515-519
89. Wachi M, Umitsuki G, Shimizu M, Takada A, Nagai K (1999) Escherichia coli cafA gene encodes a novel RNase, designated as RNase G, involved in processing of the 5′ end of 16S rRNA. Biochem Biophys Res Commun 259:483-488
90. Webb E, Claas K, Downs D (1998) thiBPQ encodes an ABC transporter required for transport of thiamine and thiamine pyrophosphate in Salmonella typhimurium. J Biol Chem 273:8946-8950
91. Wendisch VF, Bott M, Eikmanns BJ (2006) Metabolic engineering of Escherichia coli and Corynebacterium glutamicum for biotechnological production of organic acids and amino acids. Curr Opin Microbiol 9:268-274
92. Yokota A, Shimizu H, Terasawa Y, Takaoka N, Tomita F (1994a) Pyruvic acid production by a lipoic acid auxotroph of Escherichia coli W1485. Appl Microbiol Biotechnol 41:638-643
93. Yokota A, Terasawa Y, Takaoka N, Shimizu H, Tomita F (1994b) Pyruvic acid production by an F1-ATPase-defective mutant of Escherichia coli W1485lip2. Biosci Biotechnol Biochem 58:2164-2167