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Reversible ADP-ribosylation as a mechanism of enzyme regulation in procaryotes

  • Part III Mono(ADP-ribosylation)
  • A. ADP-ribosylation Cycle
  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Several cases of ADP-ribosylation of endogenous proteins in procaryotes have been discovered and investigated. The most thoroughly studied example is the reversible ADP-ribosylation of the dinitrogenase reductase from the photosynthetic bacteriumRhodospirillum rubrum and related bacteria. A dinitrogenase reductase ADP-ribosyltransferase (DRAT) and a dinitrogenase reductase ADP-ribose glycohydrolase (DRAG) fromR. rubrum have been isolated and characterized. The genes for these proteins have been isolated and sequences and show little similarity to the ADP-ribosylating toxins. Other targets for endogenous ADP-ribosylation by procaryotes include glutamine synthetase inR. rubrum andRhizobium meliloti and undefined proteins inStreptomyces griseus andPseudomonas maltophila.

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References

  1. Honjo T, Nishizuka Y, Hayaishi O, and Kato I: Diptheria toxin-dependent adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis. J Biol Chem 243:3553–3555, 1968

    PubMed  Google Scholar 

  2. Gill DM, Pappenheimer AM, Brown R, and Kurnick JT: Studies on the mode of action of diptheria toxin. VII. Toxin-stimulated hydrolysis of nicotinamide adenine dinucleotide in mammalian cell extracts. J Exp Med 129: 1–21, 1969

    PubMed  Google Scholar 

  3. Moss J, and Vaughan M: Mechanism of action of choleragen—evidence for ADP-ribosyltransferase activity with arginine as an acceptor. J Biol Chem 252:2455–2457, 1977

    PubMed  Google Scholar 

  4. Goff CG: Chemical structure of a modification of the E. coli ribonucleic acid polymerase polypeptides induced by bacteriophage T4 infection. J Biol Chem 249:6181–6190, 1974

    PubMed  Google Scholar 

  5. Ludden PW, Roberts GP: Regulation of nitrogenase activity by reversible ADP-ribosylation. In B. Horecker, et al. (ed) Current Topics of Cellular Regulation, 989, Academic Press Inc.: Orlando, p. 23–55

  6. Pope MR, Murrell SA, Ludden PW: Covalent modification of the iron protein of nitrogenase fromRhodospirillum rubrum by adenosine diphosphoribosylation of a specific arginyl residue. Proc Natl Acad Sci USA 82: 3173–3177, 1985

    PubMed  Google Scholar 

  7. Woehle DL, Lueddecke BA, Ludden PW: ATP-dependent and NAD-dependent modification of glutamine synthetase fromRhodospirillum rubrum in vitro. J Biol Chem 265:13741–13749, 1990

    PubMed  Google Scholar 

  8. Shatters RG, Liu Y, Kahn ML: Isolation and characterization of a novel glutamine synthetase fromRhizobium meliloti. J Biol Chem 268:469–475, 1993

    PubMed  Google Scholar 

  9. Penyige A, Barabas G, Szabo I, Ensign JC: ADP-ribosylation of membrane proteins of Streptomyces griseus strain 52-I. FEMS Microbiol Lett 69: 293–298, 1990

    Google Scholar 

  10. Edmonds C, Griffin GE, Johnstone AP: Demonstration and partial characterization of ADP-ribosylation inPseudomonas maltophilia. Biochem J. 261:113–118, 1989

    PubMed  Google Scholar 

  11. Burris RH: Nitrogenases. J Biol Chem 266:9339–9342, 1991

    PubMed  Google Scholar 

  12. Hausinger RP, Howard J: Thiol reactivcity of the nitrogenase Fe-protein fromAzotobacter vinelandii. J Biol Chem 258:13486–13492, 1983

    PubMed  Google Scholar 

  13. Tso MYW, Burris RH: The binding of ATP and ADP by nitrogenased components fromClostridium pasteurianum. Biochim Biophys Acta 309: 263–70, 1973

    PubMed  Google Scholar 

  14. Ljones T, Burris RH: ATP hydrolysis and electron transfer in the nitrogenase reaction with different combinations of the iron protein and rhe molybdenum-iron protein. Biochim Biophys Acta 275:93–101, 1972

    PubMed  Google Scholar 

  15. Roberts GP, Brill WJ: Gene-product relationships of the nifregulon ofKlebsiella pneumoniae. J. Bact. 144:210–216, 1980

    PubMed  Google Scholar 

  16. Bolin JT, Ronco AE, Lorgan TV, Mortenson LE, Xuong N-H: The unusual metal clusters of nitrogenase: Structural features revealed by x-ray anomolous diffraction studies of the MoFe protein fromClostridium pasteurianum. Proc Natl Acad Sci USA 90:1078–1082, 1993

    PubMed  Google Scholar 

  17. Shah VK, Brill WJ: Isolation of an iron-molybdenum cofactor (FeMo-co) from nitrgenase. Proc Natl Acad Sci USA 74:3249–3253, 1977

    PubMed  Google Scholar 

  18. Stewart WPD, Fitzgerald GP, Burris RH:In situ studies on N2 fixation using the acetylene reduction technique. Proc Natl Acad Sci USA 58:2071–2078, 1967

    PubMed  Google Scholar 

  19. Simpson FB, Burris RH: A nitrogen pressue of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224:1095–1097, 1984

    PubMed  Google Scholar 

  20. Dowling TE, Preston GG, Ludden PW: Heat activation of the Fe protein of nitrogenase fromRhodospirillum rubrum. J Biol Chem 257:13987–13992, 1982

    PubMed  Google Scholar 

  21. Pope MR, Murrell SA, Ludden PW: Purification and properties of the heat released nucleotide modifying group from the inactive Fe protein of nitrogenase fromRhodospirillum rubrum. Biochemistry 24:2374–2380, 1985

    PubMed  Google Scholar 

  22. Hausinger RP, Howard JB: The amino acid sequence of the nitrogenase iron protein fromAzotobacter vinelandii. J Biol Chem 257:2483–2490, 1982

    PubMed  Google Scholar 

  23. Pretorius I-M, Rawlins DE, O'Neill EG, Jones WA, Kirby R, Woods DR: Nucleotide sequence of the gene encoding the nitrogenase ion protein ofThiobacillus ferrooxidans. J Bacteriol, 169:367–270, 1987

    PubMed  Google Scholar 

  24. Lehman LJ, Fitzmaurice WP, Roberts GP: The cloning and functional characterization of thenifH gene ofRhodospirillum rubrum. Gene 95: 143–147, 1990

    PubMed  Google Scholar 

  25. Pope MR, Saari LL, Ludden PW: N-glycohydrolysis of adenosine diphosphoribosyl argine linkages by dinitrogenase reductase activating glycohydrolase (activating enzyme) fromRhodospirillum rubrum. J Biol Chem 261:10104–10111, 1986

    PubMed  Google Scholar 

  26. Ludden PW, Burris RH: Activating factor for the iron protein of nitrogenase fromRhodospirillum rubrum. Science 194:424–426, 1976

    PubMed  Google Scholar 

  27. Nordlund S, Eriksson U, Blatscheffsky H: Necessity of a membrane component for nitrogenase activity inRhodospirillum rubrum. Biochem Biophys Acta 462:187–195, 1977

    PubMed  Google Scholar 

  28. Ludden PW, Burris RH: Removal of an adenine-loke molecule during activation of dinitrogenase reductase fromRhodospirillum rubrum. Proc Natl Acad Sci USA 76:6201–6205, 1979

    PubMed  Google Scholar 

  29. Saari LL, Triplett EW, Ludden PW: Purification and properties of the activating enzyme for iron protein of nitrogenase from the photosynthetic bacteriumRhodospirillum rubrum. J Biol Chem 259:15502–15508, 1984

    PubMed  Google Scholar 

  30. Triplett EW, Wall JD, Ludden PW: Expression of the activating enzyme and Fe protein of nitrogenase fromRhodospirillum rubrum. J Bacteriol 152:786–791, 1982

    PubMed  Google Scholar 

  31. Pope MR, Saari LL, Ludden PW: Fluorometric assay for ADP-ribosylarginine cleavage enzymes. Anal Biochem 160:68–77, 1987

    PubMed  Google Scholar 

  32. Saari LL, Pope MR, Murrell SA, Ludden PW: Studies on the activating enzyme for iron protein of nitrogenase fromRhodospirillum rebrum. J Biol Chem 261:4973–4977, 1986

    PubMed  Google Scholar 

  33. Ludden PW: Borate inhibits activation of inactive dinitrogenase reductase fromRhodospirillum rubrum. Biochem J 197:503–505, 1981

    PubMed  Google Scholar 

  34. Nordlund S, Noren A: Dependence on divalent cations of the activation for inactive Fe protein of nitrogenase fromRhodospirillum rubrum. Biochem Biophys Acta 791:21–27, 1984

    Google Scholar 

  35. Lowery RG, Saari LL, Ludden PW: Reversible regulation of the iron protein of nitrogenase fromRhodospirillum rubrum by ADP-ribosylationin vitro. J Bacteriol 166:513–518, 1986

    PubMed  Google Scholar 

  36. Lowery RG, Ludden PW: Purification and properties of the dinitrogenase reductase inactivating ADP-ribosyltransferase fromRhodospirillum rubrum. J Biol Chem 263:16714–16719, 1988

    PubMed  Google Scholar 

  37. Pierrard J, Ludden PW, Roberts GP: Posttranslational regulation of nitrogenase inRhodobacter capsulatus: Existence of two independent regulatory effects of ammonium. J Bacteriol 175:1358–1366, 1993

    PubMed  Google Scholar 

  38. Lowery RG, Ludden PW: Effect of Nucleotides on the Activity of Dinitrogenase Reductase ADP-ribosyltransferase fromRhodospirillum rubrum. Biochemistry 28:4956–4961, 1989

    PubMed  Google Scholar 

  39. Georgiardis MM, Komiya P, Chakrabarti P, Woo D, Kornuc JJ, Rees DC: Crystallographic structure of the nitrogenase iron protein fromAzotobacter vinelandii. Science 257:1653–1659, 1992

    PubMed  Google Scholar 

  40. Murrell SA, Lowery RG, Ludden PW: ADP-ribosylation of dinitrogenase reductase fromClostridium pasteurianum prevents its inhibition of nitrogenase fromAzotobacter vinelandii. Biochem J 251:609–612, 1988

    PubMed  Google Scholar 

  41. Lowery RG, Chang CL, Davis LC, McKenna MC, Stephens PJ, Ludden PW: Substitution of Histidine for Arginine-101 of Dinitrogenase reductase Disrupts Electron Transfer to Dinitrogenase. Biochemistry 28: 1206–1212, 1989

    PubMed  Google Scholar 

  42. Fitzmaurice WP, Saari LL, Lowery RG, Ludden PW, Roberts GP: Genes coding for the reversible ADP-ribosylation system of dinitrogenase reductase fromRhodospirillum rubrum. Mol Gen Gene 218:340–347, 1989

    Google Scholar 

  43. Fu H-A, Fitzmaurice WP, Roberts GP, Burris RH: Cloning and expression ofdraTG genes fromAzospirillum lipoferum. Gene 86:95–98, 1990

    PubMed  Google Scholar 

  44. Zhang Y, Burris RH, Roberts GP: Cloning, sequencing, mutagenesis, and functional characterization ofdraT anddraG genes fromAzospirillum brasilense. J Bacteriol 174:3364–3369, 1992

    PubMed  Google Scholar 

  45. Masephol B, Krey R, Klipp W: ThedraTG region ofRhodobacter capsulatus is required for posttranslational regulation of both the molybdenum and the alternative nitrogenase. J Gen Microbiol 1993 (in press)

  46. Fu H, Burris RH, Roberts GP: Reversible ADP-ribosylation is demonstrated to be a regulatory mechanism in prokaryotes by heterologous expression. Proc Natl Acad Sci USA 87:1720–1724, 1990

    PubMed  Google Scholar 

  47. Liang J, Nielsen GM, Lies DP, Burris RH, Roberts GP, Ludden PW: Mutations in thedraT anddraG genes ofRhodospirillum rubrum result in loss of regulation of nitrogenase by reversible ADP-ribosylation. J Bacteriology 173:6903–6909, 1991

    Google Scholar 

  48. Kanemoto RH, Ludden PW: Effect of ammonia, darkness, and phenazine methosultate on whole-cell nitrogenase activity and Fe protein modification inRhodospirillum rubrum. J Bacteriol 158:713–720, 1984

    PubMed  Google Scholar 

  49. Paul TD, Ludden PW: Adenine nucleotide levels inRhodospirillum rubrum during switch-off of whole-cell nitrogenase activity. Biochem J 224: 961–969, 1984

    PubMed  Google Scholar 

  50. Li J, Hu C, Yoch DC: Changes in amino acid and nucleotide pools ofRhodospirillum rubrum during switch-off of nitrogenase activity initiated by NH4+ or darkness. J Bacteriol 169:231–237, 1987

    PubMed  Google Scholar 

  51. Nordlund S, Hogland L: Studies of the adenylate and pyridine nucleotide pools during nitrogenase ‘switch-off’ inRhodospirillum rubrum. Plant Soil 90:203–209, 1986

    Google Scholar 

  52. Kanemoto RH, Ludden PW: Amino acid concentrations inRhodospirillum rubrum during expression and switch-off of nitrogenase activity. J Bacteriol 169:3035–3043, 1987

    PubMed  Google Scholar 

  53. Shapiro BM, Stadtman ER: 5′-adenylyl-)-tyrosine. The novel phosphodiester residue of adenylylated glutamine synthetase fromEscherichia coli. J Biol Chem 243:3769–3771, 1968

    PubMed  Google Scholar 

  54. Rhee SG, Chock PB, Stadtman ER: Glutamine synthetase fromEscherichia coli. Methods Enzymol 113:213–241, 1985

    PubMed  Google Scholar 

  55. Cervantes-Laurean D, Minter DE, Jacobson EL, Jacobson MK: Protein glycation by ADP-ribose: Studies of model conjugates. Biochemistry 32: 1528–1534, 1993

    PubMed  Google Scholar 

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  1. Department of Biochemistry, University of Wisconsin, 53706, Madison, WI, USA

    Paul W. Ludden

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Ludden, P.W. Reversible ADP-ribosylation as a mechanism of enzyme regulation in procaryotes. Mol Cell Biochem 138, 123–129 (1994). https://doi.org/10.1007/BF00928453

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