Regulation of heme biosynthesis in Salmonella typhimurium: Activity of glutamyl-tRNA reductase (HemA) is greatly elevated during heme limitation by a mechanism which increases abundance of the protein

Journal of Bacteriology

Volumn 179, Issue 9, 1997, Pages 2907-2914

  Wang, Li Ying ^a   Brown, Larissa ^a   Elliott, Meenal ^a   Elliott, Thomas ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOLEVULINIC ACID; GLUTAMINE TRANSFER RNA; HEME; OXIDOREDUCTASE;

ARTICLE; ENZYME INDUCTION; HEME SYNTHESIS; IMMUNOBLOTTING; METABOLIC REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SALMONELLA TYPHIMURIUM;

EID: 0344361618     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.9.2907-2914.1997     Document Type: Article

References (56)

1. Ailion, M., T. A. Bobik, and J. R. Roth. 1993. Two global regulatory systems (Crp and Arc) control the cobalamin/propanediol regulon of Salmonella typhimurium. J. Bacteriol. 175:7200-7208.
2. Anraku, Y., and R. B. Gennis. 1987. The aerobic respiratory chain of Escherichia coli. Trends Biochem. Sci. 12:262-266.
3. Archer, C. D., X. Wang, and T. Elliott. 1993. Mutants defective in the energy-conserving NADH dehydrogenase of Salmonella typhimurium identified by a decrease in energy-dependent proteolysis after carbon starvation. Proc. Natl. Acad. Sci. USA 90:9877-9881.
4. Avissar, Y. J., and S. I. Beale. 1989. Identification of the enzymatic basis for δ-aminolevulinic acid auxotrophy in a hemA mutant of Escherichia coli. J. Bacteriol. 171:2919-2924.
5. Avissar, Y. J., and S, I. Beale. 1990. Cloning and expression of a structural gene from Chlorobium vibrioforme that complements the hemA mutation in Escherichia coli. J. Bacteriol. 172:1656-1659.
6. Avissar, Y. J., J. G. Ormerod, and S. I. Beale. 1989. Distribution of δ-aminolevulinic acid biosynthetic pathways among phototrophic bacterial groups. Arch. Microbiol. 151:513-519.
7. Beale, S. I. 1996. Biosynthesis of hemes, p. 731-748. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. American Society for Microbiology, Washington, D.C.
8. Berkowitz, D., J. M. Hushon, H. J. Whitfield, J. Roth, and B. N. Ames. 1968. Procedure for identifying nonsense mutations. J. Bacteriol. 96:215-220.
9. Bochner, B. R., and B. N. Ames. 1982. Complete analysis of cellular nucleotides by two-dimensional thin layer chromatography. J. Biol. Chem. 257: 9759-9769.
10. Breton, R., H. Sanfacon, I. Papayannopoulos, K. Biemann, and J. Lapointe. 1986. Glutamyl-tRNA synthetase of Escherichia coli. Isolation and primary structure of the gltX gene and homology with other aminoacyl-tRNA synthatases. J. Biol. Chem. 261:10610-10717.
11. Brown, L., and T. Elliott. 1996. Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J. Bacteriol. 178:3763-3770.
12. Chen, W., C. S. Russell, Y. Murooka, and S. D. Cosloy. 1994. 5-Aminolevulinic acid synthesis in Escherichia coli requires expression of hemA. J. Bacteriol. 176:2743-2746.
13. Chiu, J. T., P. C. Loewen, J. Switala, R. B. Gennis, and R. Timkovich. 1989. Proposed structure for the prosthetic group of the catalase HPII from Escherichia coli. J. Am. Chcm. Soc. 111:7046-7050.
14. Choi, P., and T. Elliott. Unpublished results.
15. Choi, P., L. Wang, C. D. Archer, and T. Elliott. 1996. Transcription of the glutamyl-tRNA reductase (hemA) gene in Salmonella typhimurium and Escherichia coli: role of the hemA P1 promoter and the arcA gene product. J. Bacteriol. 178:638-646.
16. Dailey, H. A. 1990. Conversion of coproporphyrinogen to protoheme in higher eukaryotes and bacteria: terminal three enzymes, p. 123-161. In H. A. Dailey (ed.). Biosynthesis of heme and chlorophylls. McGraw Hill Book Co., New York, N.Y.
17. Darie, S., and R. P. Gunsalus. 1994. Effect of heme and oxygen availability on hemA gene expression in Escherichia coli: role of the fnr, arcA. and himA gene products. J. Bacteriol. 176:5270-5276.
18. 17a.Desrochers, M., L. Peloquin, and A. Sasarman. 1978. Mapping of the hemE locus in Salmonella typhimurium. J. Bacteriol. 135:1151-1153.
19. Elliott, T. 1989. Cloning, genetic characterization, and nucleotide sequence of the hemA-prfA operon of Salmonella typhimurium. J. Bacteriol. 171:3948-3960.
20. Elliott, T. 1992. A method for constructing single-copy lac fusions in Salmonella typhimurium and its application to the hemA-prfA operon. J. Bacteriol. 174:245-253.
21. 19a.Elliott, T. 1993. Transport of 5-aminolevulinic acid by the dipeptide permease in Salmonella typhimurium. J. Bacteriol. 175:325-331.
22. Elliott, T., Y. J. Avissar, G.-E. Rhie, and S. I. Beale. 1990. Cloning and sequence of the Salmonella typhimurium hemL gene and identification of the missing enzyme in hemL mutants as glutamate-1-semialdehyde aminotransferase. J. Bacteriol. 172:7071-7084.
23. Elliott, T., and J. R. Roth. 1989. Heme-deficient mutants of Salmonella typhimurium: two genes required for ALA synthesis. Mol. Gen. Genet. 216: 303-314.
24. Elliott, T., and X. Wang. 1991. Salmonella typhimurium mutants defective in release factor 1. J. Bacteriol. 173:4144-4154.
25. Hart, R. A., P. T. Kallio, and J. E. Bailey. 1994. Effect of biosynthetic manipulation of heme on insolubility of Vitreoscilla hemoglobin in Escherichia coli. Appl. Environ. Microbiol. 60:2431-2437.
26. Hino, S., and A. Ishida. 1973. Effect of oxygen on heme and cytochrome content in some facultative bacteria. Enzyme 16:42-49.
27. Hoober, J. K., A. Kahn, D. E. Ash, S. Gough, and C. G. Kannangara. 1988. Biosynthesis of Δ-aminolevulinate in greening barley leaves. IX. Structure of the substrate, mode of gabaculine inhibition, and the catalytic mechanism of glutamate-1-semialdehyde aminotransferase. Carlsberg Res. Commun. 53: 11-25.
28. Jahn, D., U. Michelsen, and D. Soll. 1991. Two glutamyl-tRNA reductase activities in Escherichia coli. J. Biol. Chem. 266:2542-2548.
29. Jahn, D., E. Verkamp, and D. Soll. 1992. Glutamyl-transfer RNA: a precursor of heme and chlorophyll biosynthesis. Trends Biochem. Sci. 17:215-218.
30. Javor, G. T., and E. F. Febre. 1992. Enzymatic basis of thiol-stimulated secretion of porphyrins by Escherichia coli. J. Bacteriol. 174:1072-1075.
31. Jordan, P. M. 1990. Biosynthesis of 5-aminolevulinic acid and its transformation into coproporphyrinogen in animals and bacteria, p. 55-121. In H. A. Dailey (ed.). Biosynthesis of heme and chlorophylls. McGraw-Hill Book Co., New York, N.Y.
32. 29a.Kaderbhai, M. A., S. G. Sligar, T. Barnfield, T. Reames, J. Gallagher, M. He, E. I. Mercer, and N. Kaderbhai. 1990. A novel series of pEX-PINK expression vectors for screening high-level production of (un)fused foreign proteins by rapid visual detection of PINK Escherichia coli clones. Nucleic Acids Res. 18:4629-4630.
33. Kearney, J. F., A. Radbruch, B. Liesegang, and K. Rajewsky. 1979. A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines. J. Immunol. 123:1548-1550.
34. Kredich, N. M. 1996. Biosynthesis of cysteine, p. 514-527. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. American Society for Microbiology, Washington, D.C.
35. 31a.Lascelles, J. 1978. Regulation of pyrrole synthesis, p. 795-808. In R. K. Clayton and W. R. Systrom, (ed.), The photosynthetic bacteria. Plenum Press, New York, N.Y.
36. Li, J.-M., O. Brathwaite, S. D. Cosloy, and C. S. Russell. 1989. 5-Aminolevulinic acid synthesis in Escherichia coli. J. Bacteriol. 171:2547-2552.
37. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor. N.Y.
38. Mogi, T., K. Saiki, and Y. Anraku. 1994. Biosynthesis and functional role of haem O and haem A. Mol. Microbiol. 14:391-398.
39. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
40. O'Neill, G. P., M.-W. Chen, and D. Soll. 1989. δ-Aminolevulinic acid biosynthesis in Escherichia coli and Bacillus subtilis involves formation of glutamyl-tRNA. FEMS Microbiol. Lett. 60:255-260.
41. O'Toole, G. A., M. R. Rondon, J. R. Trzebiatowski, S.-J. Suh, and J. C. Escalante-Semerena. 1996. Biosynthesis and utilization of adenosyl-cobalamin (coenzyme B12), p. 710-720. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.). Escherichia coli and Salmonella: cellular and molecular biology. 2nd ed. American Society for Microbiology, Washington, D.C.
42. Richmond, M. H., and O. Maaloe. 1962. The rate of growth of Salmonella typhimurium with individual carbon sources related to glucose metabolism or to the Krebs cycle. J. Gen. Microbiol. 27:285-297.
43. Ron, D., and H. Dressier. 1992. pGSTag - a versatile bacterial expression plasmid for enzymatic labeling of recombinant proteins. BioTechniques 13: 866-869.
44. Schmieger, H. 1972. Phage P22 mutants with increased or decreased transductional abilities. Mol. Gen. Genet. 119:75-88.
45. Schneegurt, M. A., S. Rieble, and S. I. Beale. 1988. The tRNA required for in vitro δ-aminolevulinic acid formation from glutamate in Synechocystis extracts. Determination of activity in a Synechocystis in vitro protein synthesizing system. Plant Physiol. 88:1358-1366.
46. Schroder, I., L. Hederstedt, C. G. Kannangara, and S. P. Gough. 1992. Glutamyl-tRNA reductase activity in Bacillus subtilis is dependent on the hemA gene product. Biochem. J. 281:843-850.
47. Silhavy, T. J., M. L. Berman, and L. W. Enquist. 1984. Experiments with gene fusions. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
48. Studier, F. W., A. H. Rosenberg, J. J. Dunn, and J. W. Dubendorff. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:60-89.
49. Verkamp, E., M. Jahn, D. Jahn, A. M. Kumar, and D. Soll. 1992. Glutamyl-tRNA reductase from Escherichia coli and Synechocystis 6803. J. Biol. Chem. 267:8275-8280.
50. Verkamp, E., V. M. Backman, J. M. Bjornsson, D. Soll, and G. Eggertsson. 1993. The periplasmic dipeptide permease system transports 5-aminolevulinic acid in Escherichia coli. J. Bacteriol. 175:1452-1456.
51. 46a.Wang, L.-Y., and T. Elliott. Unpublished results.
52. Warren, M. J., E. L. Bolt, C. A. Roessner, A. I. Scott, J. B. Spencer, and S. C. Woodcock. 1994. Gene dissection demonstrates that the Escherichia coli cysG gene encodes a multifunctional protein. Biochem. J. 302:837-844.
53. Woodard, S. I., and H. A. Dailey. 1995. Regulation of heme biosynthesis in Escherichia coli. Arch. Biochem. Biophys. 316:110-115.
54. Xu, K., J. Delling, and T. Elliott. 1992. The genes required for heme synthesis in Salmonella typhimurium include those encoding alternative functions for aerobic and anaerobic coproporphyrinogen oxidation. J. Bacteriol. 174:3953-3963.
55. Xu, K., and T. Elliott. Unpublished observations.
56. Zeilstra-Ryalls, J. H., and S. Kaplan. 1996. Control of hemA expression in Rhodobacter sphaeroides 2.4.1: regulation through alterations in the cellular redox state. J. Bacteriol. 178:985-993.