Mechanism of ADP-ribosylation removal revealed by the structure and ligand complexes of the dimanganese mono-ADP-ribosylhydrolase DraG

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 34, 2009, Pages 14247-14252

  Berthold, Catrine L ^a   Wang, He ^b   Nordlund, Stefan ^b   Högbom, Martin ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Binuclear dinuclear; Bioinorganic chemistry; Covalent modification; Nitrogen fixation; Posttranslational modifications

Indexed keywords

MAGNESIUM; MANGANESE; RIBOSE;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CATALYSIS; CHEMICAL REACTION; CHEMICAL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; MOLECULAR MECHANICS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; RING OPENING;

ADENOSINE DIPHOSPHATE RIBOSE; BACTERIAL PROTEINS; BLOTTING, WESTERN; CATALYSIS; CRYSTALLIZATION; LIGANDS; MANGANESE; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MUTATION; N-GLYCOSYL HYDROLASES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RHODOSPIRILLUM RUBRUM; RIBOSE;

BACTERIA (MICROORGANISMS); PHOTOBACTERIA; RHODOSPIRILLUM RUBRUM;

EID: 70149101122     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0905906106     Document Type: Article

References (42)

1. Moss J, Zolkiewska A, Okazaki I (1997) ADP-ribosylarginine hydrolases and ADP-ribosyltransferases. Partners in ADP-ribosylation cycles. Adv Exp Med Biol 419:25-33. (Pubitemid 27256046)
2. Koch-Nolte F, et al. (2008) Mammalian ADP-ribosyltransferases and ADP-ribosylhydolases. Front Biosci 13:6716-6729.
3. Deng Q, Barbieri JT (2008) Molecular mechanisms of the cytotoxicity of ADP-ribosylating toxins. Annu Rev Microbiol 62:271-288.
4. Vanden Broeck D, Horvath C, De Wolf MJ (2007) Vibrio cholerae: Cholera toxin. Int J Biochem Cell Biol 39:1771-1775.
5. Corda D, Di Girolamo M (2002) Mono-ADP-ribosylation: A tool for modulating immune response and cell signaling. Sci STKE 2002:PE53.
6. Hassa PO, Haenni SS, Elser M, Hottiger MO (2006) Nuclear ADP-ribosylation reactions in mammalian cells: Where are we today and where are we going? Microbiol Mol Biol Rev 70:789-829. (Pubitemid 44484693)
7. Diefenbach J, Burkle A (2005) Introduction to poly(ADP-ribose) metabolism. Cell Mol Life Sci 62:721-730.
8. Masutani M, Nakagama H, Sugimura T (2005) Poly(ADP-ribosyl)ation in relation to cancer and autoimmune disease. Cell Mol Life Sci 62:769-783. (Pubitemid 40655627)
9. Helleday T, et al. (2008) DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 8:193-204. (Pubitemid 351301852)
10. Moss J, Stanley SJ, Oppenheimer NJ (1979) Substrate specificity and partial purification of a stereospecific NAD-and guanidine-dependent ADP-ribosyltransferase from avian erythrocytes. J Biol Chem 254:8891-8894.
11. Hassa PO, Hottiger MO (2008) The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci 13:3046-3082.
12. Koch-Nolte F, Haag F (1997) Mono(ADP-ribosyl)transferases and related enzymes in animal tissues. Emerging gene families. Adv Exp Med Biol 419:1-13. (Pubitemid 27256044)
13. Moss J, Oppenheimer NJ, West RE, Jr., Stanley SJ (1986) Amino acid specific ADP-ribosylation: Substrate specificity of an ADP-ribosylarginine hydrolase from turkey erythrocytes. Biochemistry 25:5408-5414.
14. Nordlund S, Ludden PW (2004) in Genetics and regulation of nitrogen fixation in free-living bacteria, eds Klipp W, Masephol B, Gallon JR, Newton WE (Kluwer Academic Publisher, The Netherlands), pp 175-196.
15. Wang H, Franke CC, Nordlund S, Noren A (2005) Reversible membrane association of dinitrogenase reductase activating glycohydrolase in the regulation of nitrogenase activity in Rhodospirillum rubrum; dependence on GlnJ and AmtB1. FEMS Microbiol Lett 253:273-279. (Pubitemid 41674526)
16. Norén A, Nordlund S (1997) Dinitrogenase reductase-activating glycohydrolase can be released from chromatophores of Rhodospirillum rubrum by treatment with MgGDP. J Bacteriol 179:7872-7874. (Pubitemid 27525721)
17. Halbleib CM, Ludden PW (1999) Characterization of the interaction of dinitrogenase reductase-activating glycohydrolase from Rhodospirillum rubrum with bacterial membranes. Arch Microbiol 172:51-58.
18. Nordlund S, Eriksson U, Baltscheffsky H (1977) Necessity of a membrane component for nitrogenase activity in Rhodospirillum rubrum. Biochim Biophys Acta 462:187-195. (Pubitemid 8232619)
19. Pope MR, Saari LL, Ludden PW (1986) N-glycohydrolysis of adenosine diphosphoribosyl arginine linkages by dinitrogenase reductase activating glycohydrolase (activating enzyme) from. Rhodospirillum rubrum. J Biol Chem 261:10104-10111.
20. Saari LL, Pope MR, Murrell SA, Ludden PW (1986) Studies on the activating enzyme for iron protein of nitrogenase from. Rhodospirillum rubrum. J Biol Chem 261:4973-4977.
21. Antharavally BS, Poyner RR, Ludden PW (1998) EPR spectral evidence for a binuclear Mn(II) center in dinitrogenase reductase-activating glycohydrolase from. Rhodospirillum rubrum. J Am Chem Soc 120:8897-8898.
22. Glowacki G, et al. (2002) The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse. Protein Sci 11:1657-1670. (Pubitemid 34663545)
23. Moss J, et al. (1992) Molecular and immunological characterization of ADP-ribosylarginine hydrolases. J Biol Chem 267:10481-10488.
24. Oka S, Kato J, Moss J (2006) Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J Biol Chem 281:705-713.
25. Mueller-Dieckmann C, et al. (2006) The structure of human ADP-ribosylhydrolase 3 (ARH3) provides insights into the reversibility of protein ADP-ribosylation. Proc Natl Acad Sci USA 103:15026-15031. (Pubitemid 44583158)
26. Mueller-Dieckmann C, et al. (2008) Structure of mouse ADP-ribosylhydrolase 3 (mARH3). Acta Crystallogr Sect F Struct Biol Cryst Commun 64:156-162.
27. Nordlund S, Norén A (1984) Dependence on divalent cations of the activation of inactive Fe-protein of nitrogenase from Rhodospirillum rubrum. Biochim Biophys Acta 791:21-27.
28. Li XD, et al. (2009) Crystal structure of dinitrogenase reductase activating glycohydrolase (DraG) reveals conservation in the ADP-ribosylhydrolase fold and specific features in the ADP-ribose binding pocket. J Mol Biol 390:737-746.
29. Ljungstrom E, Yates MG, Nordlund S (1989) Purification of the Activating Enzyme for the Fe-Protein of Nitrogenase from Azospirillum Brasilense. Biochim Biophys Acta 994:210-214.
30. Andersson CS, Högbom M (2009) A Mycobacterium tuberculosis ligand-binding Mn/Fe protein reveals a new cofactor in a remodeled R2-protein scaffold. Proc Natl Acad Sci USA 106:5633-5638.
31. Andersson ME, et al. (1999) The crystal structure of an azide complex of the diferrous R2 subunit of ribonucleotide reductase displays a novel carboxylate shift with important mechanistic implications for diiron-catalyzedoxygenactivation. J Am Chem Soc 121:2346-2352.
32. Högbom M, Andersson ME, Nordlund P (2001) Crystal structures of oxidized dinuclear manganese centres in Mn-substituted class I ribonucleotide reductase from Escherichia coli: Carboxylate shifts with implications for O2 activation and radical generation. J Biol Inorg Chem 6:315-323. (Pubitemid 32823963)
33. Cervantes-Laurean D, Minter DE, Jacobson EL, Jacobson MK (1993) Protein glycation by ADP-ribose: Studies of model conjugates. Biochemistry 32:1528-1534. (Pubitemid 23077560)
34. Håkansson K, Carlsson M, Svensson LA, Liljas A (1992) Structure of native and apo carbonic anhydrase II and structure of some of its anion-ligand complexes. J Mol Biol 227:1192-1204.
35. Kanyo ZF, Scolnick LR, Ash DE, Christianson DW (1996) Structure of a unique binuclear manganese cluster in arginase. Nature 383:554-557.
36. Christianson DW, Cox JD (1999) Catalysis by metal-activated hydroxide in zinc and manganese metalloenzymes. Annu Rev Biochem 68:33-57.
37. Dismukes GC (1996) Manganese Enzymes with Binuclear Active Sites. Chem Rev 96:2909-2926.
38. Krebs JF, Ippolito JA, Christianson DW, Fierke CA (1993) Structural and functional importance of a conserved hydrogen bond network inhumancarbonic anhydrase II. J Biol Chem 268:27458-27466. (Pubitemid 24006470)
39. Jonsson A, Nordlund S (2007) In vitro studies of the uridylylation of the three PII protein paralogs from Rhodospirillum rubrum: The transferase activity of R. rubrum GlnD is regulated by alpha-ketoglutarate and divalent cations but not by glutamine. J Bacteriol 189:3471-3478. (Pubitemid 46668811)
40. Saari LL, Triplett EW, Ludden PW (1984) Purification and properties of the activating enzyme for iron protein of nitrogenase from the photosynthetic bacterium. Rhodospirillum rubrum. J Biol Chem 259:15502-15508.
41. Nielsen GM, Bao Y, Roberts GP, Ludden PW (1994) Purification and characterization of an oxygen-stable form of dinitrogenase reductase-activating glycohydrolase from Rhodospirillum rubrum. Biochem J 302(Pt 3):801-806. (Pubitemid 24289317)
42. Kanemoto RH, Ludden PW (1984) Effect of ammonia, darkness, and phenazine methosulfate on whole-cell nitrogenase activity and Fe protein modification in Rhodospirillum rubrum. J Bacteriol 158:713-720.