Depletion of glycolytic intermediates plays a key role in glucose-phosphate stress in escherichia coli

Journal of Bacteriology

Volumn 195, Issue 21, 2013, Pages 4816-4825

  Richards, Gregory R ^a,b   Patel, Maulik V ^a   Lloyd, Chelsea R ^a   Vanderpool, Carin K ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF WISCONSIN PARKSIDE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRUCTOSE 6 PHOSPHATE; GLUCOSE 6 PHOSPHATE; GLUCOSE PHOSPHATE; GLYCOLYTIC ENZYME; PHOSPHOENOLPYRUVATE; PYRUVIC ACID; RNA;

ARTICLE; BACTERIAL GROWTH; CELL GROWTH; CYTOLYSIS; ESCHERICHIA COLI; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; STRESS;

BIOLOGICAL TRANSPORT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE-6-PHOSPHATE; GLYCOLYSIS; METHYLGLUCOSIDES; MUTATION;

EID: 84886013496     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00705-13     Document Type: Article

References (42)

1. Englesberg E, Anderson RL, Weinberg R, Lee N, Hoffee P, Huttenhauer G, Boyer H. 1962. L-Arabinose-sensitive, L-ribulose 5-phosphate 4-epimerase- deficient mutants of Escherichia coli. J. Bacteriol. 84:137-146.
2. Irani MH, Maitra PK. 1977. Properties of Escherichia coli mutants deficient in enzymes of glycolysis. J. Bacteriol. 132:398-410.
3. Yarmolinsky MB, Wiesmeyer H, Kalckar HM, Jordan E. 1959. Hereditary defects in galactose metabolism in Escherichia coli mutants. II. Galactose- induced sensitivity. Proc. Natl. Acad. Sci. U. S. A. 45:1786-1791.
4. Elliott J, Arber W. 1978. E. coli K-12 pel mutants, which block phage lambda DNA injection, coincide with ptsM, which determines a component of a sugar transport system. Mol. Gen. Genet. 161:1-8.
5. Meadow ND, Fox DK, Roseman S. 1990. The bacterial phosphoenolpyruvate: glycose phosphotransferase system. Annu. Rev. Biochem. 59:497- 542.
6. Erni B, Zanolari B, Kocher HP. 1987. The mannose permease of Escherichia coli consists of three different proteins. Amino acid sequence and function in sugar transport, sugar phosphorylation, and penetration of phage lambda DNA. J. Biol. Chem. 262:5238-5247.
7. Henderson PJ, Giddens RA, Jones-Mortimer MC. 1977. Transport of galactose, glucose and their molecular analogues by Escherichia coli K12. Biochem. J. 162:309-320.
8. 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.
9. 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.
10. Morita T, El-Kazzaz W, Tanaka Y, Inada T, Aiba H. 2003. Accumulation of glucose 6-phosphate or fructose 6-phosphate is responsible for destabilization of glucose transporter mRNA in Escherichia coli. J. Biol. Chem. 278:15608-15614.
11. Vanderpool CK. 2007. Physiological consequences of small RNAmediated regulation of glucose-phosphate stress. Curr. Opin. Microbiol. 10:146-151.
12. Vanderpool CK, Gottesman S. 2007. The novel transcription factor SgrR coordinates the response to glucose-phosphate stress. J. Bacteriol. 189: 2238-2248.
13. Morita T, Mochizuki Y, Aiba H. 2006. Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proc. Natl. Acad. Sci. U. S. A. 103:4858-4863.
14. Rice JB, Vanderpool CK. 2011. The small RNA SgrS controls sugarphosphate accumulation by regulating multiple PTS genes. Nucleic Acids Res. 39:3806-3819.
15. Kawamoto H, Koide Y, Morita T, Aiba H. 2006. Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol. Microbiol. 61:1013-1022.
16. Morita T, Maki K, Aiba H. 2005. RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev. 19:2176-2186.
17. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S. 2003. Global analysis of small RNA and mRNA targets of Hfq. Mol. Microbiol. 50:1111-1124.
18. Vanderpool CK, Balasubramanian D, Lloyd CR. 2011. Dual-function RNA regulators in bacteria. Biochimie 93:1943-1949.
19. Wadler CS, Vanderpool CK. 2007. A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc. Natl. Acad. Sci. U. S. A. 104:20454-20459.
20. Richards GR, Vanderpool CK. 2011. Molecular call and response: the physiology of bacterial small RNAs. Biochim. Biophys. Acta 1809:525- 531.
21. Kadner RJ, Murphy GP, Stephens CM. 1992. Two mechanisms for growth inhibition by elevated transport of sugar phosphates in Escherichia coli. J. Gen. Microbiol. 138:2007-2014.
22. Hopper DJ, Cooper RA. 1971. The regulation of Escherichia coli methylglyoxal synthase; a new control site in glycolysis? FEBS Lett. 13:213-216.
23. Wadler CS, Vanderpool CK. 2009. Characterization of homologs of the small RNA SgrS reveals diversity in function. Nucleic Acids Res. 37:5477- 5485.
24. 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. doi:10.1038/msb4100050.
25. Sun Y, Vanderpool CK. 2011. Regulation and function of Escherichia coli sugar efflux transporter A (SetA) during glucose-phosphate stress. J. Bacteriol. 193:143-153.
26. Richards GR, Vanderpool CK. 2012. Induction of the Pho regulon suppresses the growth defect of an Escherichia coli sgrS mutant, connecting phosphate metabolism to the glucose-phosphate stress response. J. Bacteriol. 194:2520-2530.
27. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H. 2005. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12:291-299.
28. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
29. Garcia-Alles LF, Zahn A, Erni B. 2002. Sugar recognition by the glucose and mannose permeases of Escherichia coli. Steady-state kinetics and inhibition studies. Biochemistry 41:10077-10086.
30. Sonna LA, Ambudkar SV, Maloney PC. 1988. The mechanism of glucose 6-phosphate transport by Escherichia coli. J. Biol. Chem. 263:6625-6630.
31. Maloney PC, Ambudkar SV, Anatharam V, Sonna LA, Varadhachary A. 1990. Anion-exchange mechanisms in bacteria. Microbiol. Rev. 54:1-17.
32. Winkler HH. 1966. A hexose-phosphate transport system in Escherichia coli. Biochim. Biophys. Acta 117:231-240.
33. Chao YP, Patnaik R, Roof WD, Young RF, Liao JC. 1993. Control of gluconeogenic growth by pps and pck in Escherichia coli. J. Bacteriol. 175: 6939-6944.
34. Ogawa T, Mori H, Tomita M, Yoshino M. 2007. Inhibitory effect of phosphoenolpyruvate on glycolytic enzymes in Escherichia coli. Res. Microbiol. 158:159-163.
35. Hogema BM. Arents JC, Bader R, Eijkemans K, Yoshida H, Takahashi H, Aiba H, Postma PW. 1998. Inducer exclusion in Escherichia coli by non-PTS substrates: the role of the PEP to pyruvate ratio in determining the phosphorylation state of enzyme IIAGlc. Mol. Microbiol. 30:487-498.
36. Barabote RD, Saier MH, Jr. 2005. Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol. Mol. Biol. Rev. 69:608- 634.
37. Tchieu JH, Norris V, Edwards JS, Saier MH, Jr. 2001. The complete phosphotranferase system in Escherichia coli. J. Mol. Microbiol. Biotechnol. 3:329-346.
38. Kornberg H, Lambourne LT. 1994. The role of phosphoenolpyruvate in the simultaneous uptake of fructose and 2-deoxyglucose by Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 91:11080-11083.
39. Roehl RA, Vinopal RT. 1976. Lack of glucose phosphotransferase function in phosphofructokinase mutants of Escherichia coli. J. Bacteriol. 126: 852-860.
40. Vinopal RT, Fraenkel DG. 1974. Phenotypic suppression of phosphofructokinase mutations in Escherichia coli by constitutive expression of the glyoxylate shunt. J. Bacteriol. 118:1090-1100.
41. Lee SJ, Trostel A, Le P, Harinarayanan R, Fitzgerald PC, Adhya S. 2009. Cellular stress created by intermediary metabolite imbalances. Proc. Natl. Acad. Sci. U. S. A. 106:19515-19520.
42. Sun Y, Vanderpool CK. 2013. Physiological consequences of multipletarget regulation by the small RNA SgrS in Escherichia coli. J. Bacteriol. 195:4804-4815.