Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1988 May;170(5):2344–2351. doi: 10.1128/jb.170.5.2344-2351.1988

Near-UV stress in Salmonella typhimurium: 4-thiouridine in tRNA, ppGpp, and ApppGpp as components of an adaptive response.

G F Kramer 1, J C Baker 1, B N Ames 1
PMCID: PMC211128  PMID: 3283108

Abstract

We have examined the role of 4-thiouridine in the responses of Salmonella typhimurium to near-UV irradiation. Mutants lacking 4-thiouridine (nuv) and mutants defective in the synthesis of ppGpp (guanosine 5'-diphosphate-3'-diphosphate) (relA) were found to be sensitive to killing by near-UV. Near-UV induced the synthesis of a set of proteins that were not induced in the nuv mutant. Some of these proteins were identified as oxidative defense proteins, and others were identified as ppGpp-inducible proteins. Over 100-fold increases in ApppGpp (adenosine 5', 5"'-triphosphoguanosine-3"'-diphosphate, the adenylylated form of ppGpp) were observed in wild-type cells after near-UV irradiation but not in the 4-thiouridine-deficient mutant. These data support a model in which ppGpp and ApppGpp, a dinucleotide proposed to be synthesized by tRNA-aminoacyl synthetases as a response to the cross-linking of 4-thiouridine in tRNA by near-UV, induce the synthesis of proteins necessary for resistance to near-UV irradiation.

Full text

PDF
2344

Images in this article

2348Image
on p.2348

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baker J. C., Jacobson M. K. Determination of diadenosine 5',5''',-P1,P4-tetraphosphate levels in cultured mammalian cells. Anal Biochem. 1984 Sep;141(2):451–460. doi: 10.1016/0003-2697(84)90070-8. [DOI] [PubMed] [Google Scholar]
  2. Blanchetot A., Hajnsdorf E., Favre A. Metabolism of tRNA in near-ultraviolet-illuminated Escherichia coli. The tRNA repair hypothesis. Eur J Biochem. 1984 Mar 15;139(3):547–552. doi: 10.1111/j.1432-1033.1984.tb08040.x. [DOI] [PubMed] [Google Scholar]
  3. Bochner B. R., Lee P. C., Wilson S. W., Cutler C. W., Ames B. N. AppppA and related adenylylated nucleotides are synthesized as a consequence of oxidation stress. Cell. 1984 May;37(1):225–232. doi: 10.1016/0092-8674(84)90318-0. [DOI] [PubMed] [Google Scholar]
  4. Bochner B. R., Zylicz M., Georgopoulos C. Escherichia coli DnaK protein possesses a 5'-nucleotidase activity that is inhibited by AppppA. J Bacteriol. 1986 Nov;168(2):931–935. doi: 10.1128/jb.168.2.931-935.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boehm D. E., Vincent K., Brown O. R. Oxygen and toxicity inhibition of amino acid biosynthesis. Nature. 1976 Jul 29;262(5567):418–420. doi: 10.1038/262418a0. [DOI] [PubMed] [Google Scholar]
  6. Brown O. R., Seither R. L. Oxygen and redox-active drugs: shared toxicity sites. Fundam Appl Toxicol. 1983 Jul-Aug;3(4):209–214. doi: 10.1016/s0272-0590(83)80127-4. [DOI] [PubMed] [Google Scholar]
  7. Cashel M. The control of ribonucleic acid synthesis in Escherichia coli. IV. Relevance of unusual phosphorylated compounds from amino acid-starved stringent strains. J Biol Chem. 1969 Jun 25;244(12):3133–3141. [PubMed] [Google Scholar]
  8. 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. Cell. 1985 Jul;41(3):753–762. doi: 10.1016/s0092-8674(85)80056-8. [DOI] [PubMed] [Google Scholar]
  9. Demple B., Halbrook J. Inducible repair of oxidative DNA damage in Escherichia coli. Nature. 1983 Aug 4;304(5925):466–468. doi: 10.1038/304466a0. [DOI] [PubMed] [Google Scholar]
  10. Favre A., Hajnsdorf E., Thiam K., Caldeira de Araujo A. Mutagenesis and growth delay induced in Escherichia coli by near-ultraviolet radiations. Biochimie. 1985 Mar-Apr;67(3-4):335–342. doi: 10.1016/s0300-9084(85)80076-6. [DOI] [PubMed] [Google Scholar]
  11. Favre A., Michelson A. M., Yaniv M. Photochemistry of 4-thiouridine in Escherichia coli transfer RNA1Val. J Mol Biol. 1971 May 28;58(1):367–379. doi: 10.1016/0022-2836(71)90252-x. [DOI] [PubMed] [Google Scholar]
  12. Gallant J. A. Stringent control in E. coli. Annu Rev Genet. 1979;13:393–415. doi: 10.1146/annurev.ge.13.120179.002141. [DOI] [PubMed] [Google Scholar]
  13. Goerlich O., Foeckler R., Holler E. Mechanism of synthesis of adenosine(5')tetraphospho(5')adenosine (AppppA) by aminoacyl-tRNA synthetases. Eur J Biochem. 1982 Aug;126(1):135–142. doi: 10.1111/j.1432-1033.1982.tb06757.x. [DOI] [PubMed] [Google Scholar]
  14. Hajnsdorf E., Favre A. Metabolism of tRNAs in growing cells of Escherichia coli illuminated with near-ultraviolet light. Photochem Photobiol. 1986 Feb;43(2):157–164. doi: 10.1111/j.1751-1097.1986.tb09508.x. [DOI] [PubMed] [Google Scholar]
  15. Hilderman R. H., Ortwerth B. J. A preferential role for lysyl-tRNA4 in the synthesis of diadenosine 5',5'''-P1,P4-tetraphosphate by an arginyl-tRNA synthetase-lysyl-tRNA synthetase complex from rat liver. Biochemistry. 1987 Mar 24;26(6):1586–1591. doi: 10.1021/bi00380a015. [DOI] [PubMed] [Google Scholar]
  16. Lang H., Riesenberg D., Zimmer C., Bergter F. Fluence-rate dependence of monophotonic reactions of nucleic acids in vitro and in vivo. Photochem Photobiol. 1986 Nov;44(5):565–570. doi: 10.1111/j.1751-1097.1986.tb04710.x. [DOI] [PubMed] [Google Scholar]
  17. Lee P. C., Bochner B. R., Ames B. N. AppppA, heat-shock stress, and cell oxidation. Proc Natl Acad Sci U S A. 1983 Dec;80(24):7496–7500. doi: 10.1073/pnas.80.24.7496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lee P. C., Bochner B. R., Ames B. N. Diadenosine 5',5"'-P1,P4-tetraphosphate and related adenylylated nucleotides in Salmonella typhimurium. J Biol Chem. 1983 Jun 10;258(11):6827–6834. [PubMed] [Google Scholar]
  19. Lipsett M. N. Enzymes producing 4-thiouridine in Escherichia coli tRNA: approximate chromosomal locations of the genes and enzyme activities in a 4-thiouridine-deficient mutant. J Bacteriol. 1978 Sep;135(3):993–997. doi: 10.1128/jb.135.3.993-997.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Morgan R. W., Christman M. F., Jacobson F. S., Storz G., Ames B. N. Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8059–8063. doi: 10.1073/pnas.83.21.8059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  22. O'Farrell P. H. The suppression of defective translation by ppGpp and its role in the stringent response. Cell. 1978 Jul;14(3):545–557. doi: 10.1016/0092-8674(78)90241-6. [DOI] [PubMed] [Google Scholar]
  23. Peak J. G., Peak M. J. Lethality in repair-proficient Escherichia coli after 365 nm ultraviolet light irradiation is dependent on fluence rate. Photochem Photobiol. 1982 Jul;36(1):103–105. doi: 10.1111/j.1751-1097.1982.tb04348.x. [DOI] [PubMed] [Google Scholar]
  24. Peak M. J., Peak J. G., Nerad L. The role of 4-thiouridine in lethal effects and in DNA backbone breakage caused by 334 nm ultraviolet light in Escherichia coli. Photochem Photobiol. 1983 Feb;37(2):169–172. doi: 10.1111/j.1751-1097.1983.tb04453.x. [DOI] [PubMed] [Google Scholar]
  25. Pedersen S., Bloch P. L., Reeh S., Neidhardt F. C. Patterns of protein synthesis in E. coli: a catalog of the amount of 140 individual proteins at different growth rates. Cell. 1978 May;14(1):179–190. doi: 10.1016/0092-8674(78)90312-4. [DOI] [PubMed] [Google Scholar]
  26. Peters J., Jagger J. Inducible repair of near-UV radiation lethal damage in E. coli. Nature. 1981 Jan 15;289(5794):194–195. doi: 10.1038/289194a0. [DOI] [PubMed] [Google Scholar]
  27. Plateau P., Fromant M., Blanquet S. Heat shock and hydrogen peroxide responses of Escherichia coli are not changed by dinucleoside tetraphosphate hydrolase overproduction. J Bacteriol. 1987 Aug;169(8):3817–3820. doi: 10.1128/jb.169.8.3817-3820.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ramabhadran T. V., Fossum T., Jagger J. Escherichia coli mutant lacking 4-thiouridine in its transfer ribonucleic acid. J Bacteriol. 1976 Nov;128(2):671–672. doi: 10.1128/jb.128.2.671-672.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ramabhadran T. V., Jagger J. Mechanism of growth delay induced in Escherichia coli by near ultraviolet radiation. Proc Natl Acad Sci U S A. 1976 Jan;73(1):59–63. doi: 10.1073/pnas.73.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ramabhadran T. V. Method for the isolation of Escherichia coli relaxed mutants, utilizing near-ultraviolet irradiation. J Bacteriol. 1976 Sep;127(3):1587–1589. doi: 10.1128/jb.127.3.1587-1589.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ryals J., Hsu R. Y., Lipsett M. N., Bremer H. Isolation of single-site Escherichia coli mutants deficient in thiamine and 4-thiouridine syntheses: identification of a nuvC mutant. J Bacteriol. 1982 Aug;151(2):899–904. doi: 10.1128/jb.151.2.899-904.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schweizer M. P., Olsen J. I., De N., Messner A., Walkiw I., Grant D. M. 13C NMR studies of dynamics and synthetase interaction of [4-13C]uracil-labeled Escherichia coli tRNAs. Fed Proc. 1984 Dec;43(15):2984–2986. [PubMed] [Google Scholar]
  33. Stephens J. C., Artz S. W., Ames B. N. Guanosine 5'-diphosphate 3'-diphosphate (ppGpp): positive effector for histidine operon transcription and general signal for amino-acid deficiency. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4389–4393. doi: 10.1073/pnas.72.11.4389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Thiam K., Favre A. Role of the stringent response in the expression and mechanism of near-ultraviolet induced growth delay. Eur J Biochem. 1984 Nov 15;145(1):137–142. doi: 10.1111/j.1432-1033.1984.tb08532.x. [DOI] [PubMed] [Google Scholar]
  35. Thomas G., Favre A. 4-Thiouridine triggers both growth delay induced by near-ultraviolet light and photoprotection. Eur J Biochem. 1980 Dec;113(1):67–74. doi: 10.1111/j.1432-1033.1980.tb06140.x. [DOI] [PubMed] [Google Scholar]
  36. Tosa T., Pizer L. I. Biochemical bases for the antimetabolite action of L-serine hydroxamate. J Bacteriol. 1971 Jun;106(3):972–982. doi: 10.1128/jb.106.3.972-982.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tsai S. C., Jagger J. The roles of the rel+ gene and of 4-thiouridine in killing and photoprotection of Escherichia coli by near-ultraviolet radiation. Photochem Photobiol. 1981 Jun;33(6):825–834. doi: 10.1111/j.1751-1097.1981.tb05499.x. [DOI] [PubMed] [Google Scholar]
  38. Tuveson R. W., Sammartano L. J. Sensitivity of hemA mutant Escherichia coli cells to inactivation by near-UV light depends on the level of supplementation with delta-aminolevulinic acid. Photochem Photobiol. 1986 Jun;43(6):621–626. doi: 10.1111/j.1751-1097.1986.tb05637.x. [DOI] [PubMed] [Google Scholar]
  39. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  40. VanBogelen R. A., Kelley P. M., Neidhardt F. C. Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J Bacteriol. 1987 Jan;169(1):26–32. doi: 10.1128/jb.169.1.26-32.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yaniv M., Chestier A., Gros F., Favre A. Biological activity of irradiated tRNA Val containing a 4-thiouridine-cytosine dimer. J Mol Biol. 1971 May 28;58(1):381–388. doi: 10.1016/0022-2836(71)90253-1. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES