Glutamyl Phosphate Is an Activated Intermediate in Actin Crosslinking by Actin Crosslinking Domain (ACD) Toxin

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Kudryashova, Elena ^a   Kalda, Caitlin ^a   Kudryashov, Dmitri S ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACYLPHOSPHATE; ADENOSINE TRIPHOSPHATE; AMIDE; BACTERIAL TOXIN; GLUTAMYLPHOSPHATE; GUANOSINE TRIPHOSPHATE; MAGNESIUM ION; PHOSPHATE; UNCLASSIFIED DRUG;

ACTIN CROSSLINKING DOMAIN; ANIMAL TISSUE; ARTICLE; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; COVALENT BOND; HOST PATHOGEN INTERACTION; HYDROLYSIS; IN VIVO STUDY; NONHUMAN; PH; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN TRANSPORT; RABBIT; SKELETAL MUSCLE; VIBRIO CHOLERAE;

ACTINS; ANIMALS; AUTORADIOGRAPHY; BACTERIAL TOXINS; BIOCATALYSIS; CROSS-LINKING REAGENTS; GLUTAMINE; HYDROGEN-ION CONCENTRATION; KINETICS; RABBITS;

EUKARYOTA; NEGIBACTERIA;

EID: 84866667082     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045721     Document Type: Article

References (38)

1. Sheahan KL, Cordero CL, Satchell KJ, (2004) Identification of a domain within the multifunctional Vibrio cholerae RTX toxin that covalently cross-links actin. Proc Natl Acad Sci U S A 101: 9798-9803.
2. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ, (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci U S A 104: 15508-15513.
3. Lee CT, Amaro C, Wu KM, Valiente E, Chang YF, et al. (2008) A common virulence plasmid in biotype 2 Vibrio vulnificus and its dissemination aided by a conjugal plasmid. J Bacteriol 190: 1638-1648.
4. Seshadri R, Joseph SW, Chopra AK, Sha J, Shaw J, et al. (2006) Genome sequence of Aeromonas hydrophila ATCC 7966T: jack of all trades. J Bacteriol 188: 8272-8282.
5. Prochazkova K, Shuvalova LA, Minasov G, Voburka Z, Anderson WF, et al. (2009) Structural and molecular mechanism for autoprocessing of MARTX toxin of Vibrio cholerae at multiple sites. J Biol Chem 284: 26557-26568.
6. Fullner KJ, Mekalanos JJ, (2000) In vivo covalent cross-linking of cellular actin by the Vibrio cholerae RTX toxin. EMBO J 19: 5315-5323.
7. Olivier V, Salzman NH, Satchell KJ, (2007) Prolonged colonization of mice by Vibrio cholerae El Tor O1 depends on accessory toxins. Infect Immun 75: 5043-5051.
8. Fullner KJ, Boucher JC, Hanes MA, Haines GK 3rd, Meehan BM, et al (2002) The contribution of accessory toxins of Vibrio cholerae O1 El Tor to the proinflammatory response in a murine pulmonary cholera model. J Exp Med 195: 1455-1462.
9. Olivier V, Queen J, Satchell KJ, (2009) Successful small intestine colonization of adult mice by Vibrio cholerae requires ketamine anesthesia and accessory toxins. PLoS One 4: e7352.
10. Ma AT, Mekalanos JJ, (2010) In vivo actin cross-linking induced by Vibrio cholerae type VI secretion system is associated with intestinal inflammation. Proc Natl Acad Sci U S A 107: 4365-4370.
11. Cordero CL, Kudryashov DS, Reisler E, Satchell KJ, (2006) The Actin cross-linking domain of the Vibrio cholerae RTX toxin directly catalyzes the covalent cross-linking of actin. J Biol Chem 281: 32366-32374.
12. Kudryashov DS, Cordero CL, Reisler E, Satchell KJ, (2008) Characterization of the enzymatic activity of the actin cross-linking domain from the Vibrio cholerae MARTX Vc toxin. J Biol Chem 283: 445-452.
13. Kudryashov DS, Durer ZA, Ytterberg AJ, Sawaya MR, Pashkov I, et al. (2008) Connecting actin monomers by iso-peptide bond is a toxicity mechanism of the Vibrio cholerae MARTX toxin. Proc Natl Acad Sci U S A 105: 18537-18542.
14. Cong Y, Topf M, Sali A, Matsudaira P, Dougherty M, et al. (2008) Crystallographic conformers of actin in a biologically active bundle of filaments. J Mol Biol 375: 331-336.
15. Holmes KC, Angert I, Kull FJ, Jahn W, Schroder RR, (2003) Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide. Nature 425: 423-427.
16. Oda T, Iwasa M, Aihara T, Maeda Y, Narita A, (2009) The nature of the globular- to fibrous-actin transition. Nature 457: 441-445.
17. Fujii T, Iwane AH, Yanagida T, Namba K, (2010) Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 467: 724-728.
18. Geissler B, Bonebrake A, Sheahan KL, Walker ME, Satchell KJ, (2009) Genetic determination of essential residues of the Vibrio cholerae actin cross-linking domain reveals functional similarity with glutamine synthetases. Mol Microbiol 73: 858-868.
19. Eisenberg D, Gill HS, Pfluegl GM, Rotstein SH, (2000) Structure-function relationships of glutamine synthetases. Biochim Biophys Acta 1477: 122-145.
20. Wedler FC, Boyer PD, (1972) Substrate binding and reaction intermediates of glutamine synthetase (Escherichia coli W) as studied by isotope exchanges. J Biol Chem 247: 984-992.
21. Spudich JA, Watt S, (1971) The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J Biol Chem 246: 4866-4871.
22. Kim E, Reisler E, (2000) Intermolecular dynamics and function in actin filaments. Biophys Chem 86: 191-201.
23. Grintsevich EE, Benchaar SA, Warshaviak D, Boontheung P, Halgand F, et al. (2008) Mapping the cofilin binding site on yeast G-actin by chemical cross-linking. J Mol Biol 377: 395-409.
24. Goldsmith SC, Guan JQ, Almo S, Chance M, (2001) Synchrotron protein footprinting: a technique to investigate protein-protein interactions. J Biomol Struct Dyn 19: 405-418.
25. De La Cruz EM, Mandinova A, Steinmetz MO, Stoffler D, Aebi U, et al. (2000) Polymerization and structure of nucleotide-free actin filaments. J Mol Biol 295: 517-526.
26. Bisswanger H (2004) Practical enzymology. Weinheim: Wiley-VCH. xv, 255 p.
27. Carlier MF, (1990) Actin polymerization and ATP hydrolysis. Adv Biophys 26: 51-73.
28. Kudryashov DS, Reisler E, (2003) Solution properties of tetramethylrhodamine-modified G-actin. Biophys J 85: 2466-2475.
29. Traut TW, (1994) Physiological concentrations of purines and pyrimidines. Mol Cell Biochem 140: 1-22.
30. Iyengar MR, Weber HH, (1964) The Relative Affinities of Nucleotides to G-Actin and Their Effects. Biochim Biophys Acta 86: 543-553.
31. Wen KK, Yao X, Rubenstein PA, (2002) GTP-yeast actin. J Biol Chem 277: 41101-41109.
32. Pollard TD, Blanchoin L, Mullins RD, (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29: 545-576.
33. Lehninger AL, Nelson DL, Cox MM (2008) Lehninger principles of biochemistry. New York: W.H. Freeman.
34. Lipmann F, Tuttle LC, (1945) The detection of activated carboxyl groups with hydroxylamine as interceptor. J Biol Chem 161: 415.
35. Tsuda Y, Stephani RA, Meister A, (1971) Direct evidence for the formation of an acyl phosphate by glutamine synthetase. Biochemistry 10: 3186-3189.
36. Weisbrod RE, Meister A, (1973) Studies on glutamine synthetase from Escherichia coli. Formation of pyrrolidone carboxylate and inhibition by methionine sulfoximine. J Biol Chem 248: 3997-4002.
37. Schomburg I, Chang A, Schomburg D, (2002) BRENDA, enzyme data and metabolic information. Nucleic Acids Res 30: 47-49.
38. Weinstock JV, Kassab JT, (1984) Angiotensin II stimulation of granuloma macrophage phagocytosis and actin polymerization in murine schistosomiasis mansoni. Cell Immunol 89: 46-54.