Scabin, a novel DNA-acting ADP-ribosyltransferase from Streptomyces scabies

Journal of Biological Chemistry

Volumn 291, Issue 21, 2016, Pages 11198-11215

  Lyons, Bronwyn ^a   Ravulapalli, Ravikiran ^a   Lanoue, Jason ^a   Lugo, Miguel R ^a   Dutta, Debajyoti ^b   Carlin, Stephanie ^a   Merrill, A Rod ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOINFORMATICS; BIOMOLECULES; DNA; ENZYME KINETICS; ENZYMES; MASS SPECTROMETRY;

ADP-RIBOSYLTRANSFERASE; DOUBLE STRANDED DNA; HIGH-RESOLUTION STRUCTURES; MASS SPECTROMETRY ANALYSIS; POTENT COMPOUNDS; SEQUENCE IDENTITY; SMALL MOLECULE INHIBITOR; STREPTOMYCES SCABIES;

ENZYME ACTIVITY;

DEOXYGUANOSINE; DOUBLE STRANDED DNA; GENOMIC DNA; GUANINE; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE NUCLEOSIDASE; PIERISIN; SCABIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; BACTERIAL TOXIN; ENZYME INHIBITOR;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME KINETICS; ENZYME PURIFICATION; ENZYME SUBSTRATE; GENE EXPRESSION; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; STREPTOMYCES SCABIEI; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MOLECULAR DYNAMICS; PATHOGENICITY; SEQUENCE HOMOLOGY; STREPTOMYCES; X RAY CRYSTALLOGRAPHY;

ADP RIBOSE TRANSFERASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL TOXINS; CRYSTALLOGRAPHY, X-RAY; DNA, BACTERIAL; ENZYME INHIBITORS; KINETICS; MOLECULAR DYNAMICS SIMULATION; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOMYCES; SUBSTRATE SPECIFICITY;

EID: 84971434951     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.707653     Document Type: Article

References (45)

1. Yates, S. P., Jørgensen, R., Andersen, G. R., and Merrill, A. R. (2006) Stealth and mimicry by deadly bacterial toxins. Trends Biochem. Sci. 31, 123-133
2. Holbourn, K. P., Shone, C. C., and Acharya, K. R. (2006) A family of killer toxins: exploring the mechanism of ADP-ribosylating toxins. FEBS J. 273, 4579-4593
3. Simon, N. C., Aktories, K., and Barbieri, J. T. (2014) Novel bacterial ADP-ribosylating toxins: structure and function. Nat. Rev. Microbiol. 12, 599-611
4. Watanabe, M., Kono, T., Matsushima-Hibiya, Y., Kanazawa, T., Nishisaka, N., Kishimoto, T., Koyama, K., Sugimura, T., and Wakabayashi, K. (1999) Molecular cloning of an apoptosis-inducing protein, pierisin, from cabbage butterfly: possible involvement of ADP-ribosylation in its activity. Proc. Natl. Acad. Sci. U.S.A. 96, 10608-10613
5. Krska, D., Ravulapalli, R., Fieldhouse, R. J., Lugo, M. R., and Merrill, A. R. (2015) C3larvin toxin, an ADP-ribosyltransferase from Paenibacillus larvae. J. Biol. Chem. 290, 1639-1653
6. Fieldhouse, R. J., and Merrill, A. R. (2008) Needle in the haystack: structure-based toxin discovery. Trends Biochem. Sci. 33, 546-556
7. Takamura-Enya, T., Watanabe, M., Totsuka, Y., Kanazawa, T., Matsushima-Hibiya, Y., Koyama, K., Sugimura, T., and Wakabayashi, K. (2001) Mono(ADP-ribosyl)ation of 2'-deoxyguanosine residue in DNA by an apoptosis-inducing protein, pierisin-1, from cabbage butterfly. Proc. Natl. Acad. Sci. U.S.A. 98, 12414-12419
8. Nakano, T., Takahashi-Nakaguchi, A., Yamamoto, M., and Watanabe, M. (2015) Pierisins and CARP-1: ADP-ribosylation of DNA by ARTCs in butterflies and shellfish. Curr. Top. Microbiol. Immunol. 384, 127-149
9. Lerat, S., Simao-Beaunoir, A. M., and Beaulieu, C. (2009) Genetic and physiological determinants of Streptomyces scabies pathogenicity. Mol. Plant. Pathol. 10, 579-585
10. Goyer, C., and Beaulieu, C. (1997) Host range of streptomycete strains causing common scab. Plant Dis. 81, 901-904
11. Kabsch, W. (2010) XDS. Acta Crystallogr. D. Biol. Crystallogr. 66, 125-132
12. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025
13. Reinert, D. J., Carpusca, I., Aktories, K., and Schulz, G. E. (2006) Structure of the mosquitocidal toxin from Bacillus sphaericus. J. Mol. Biol. 357, 1226-1236
14. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815
15. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
16. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
17. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
18. Healey, A., Furtado, A., Cooper, T., and Henry, R. J. (2014) Protocol: a simple method for extracting next-generation sequencing quality genomic DNA from recalcitrant plant species. Plant Methods 10, 21
19. Cheng, Y., and Prusoff, W. H. (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition ( I50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108
20. Labute, P. (2010) LowModeMD: implicit low-mode velocity filtering applied to conformational search of macrocycles and protein loops. J. Chem. Inf. Model. 50, 792-800
21. Masignani, V., Balducci, E., Serruto, D., Veggi, D., Aricò, B., Comanducci, M., Pizza, M., and Rappuoli, R. (2004) In silico identification of novel bacterial ADP-ribosyltransferases. Int. J. Med. Microbiol. 293, 471-478
22. Armstrong, S., and Merrill, A. R. (2001) Application of a fluorometric assay for characterization of the catalytic competency of a domain III fragment of Pseudomonas aeruginosa exotoxin A. Anal. Biochem. 292, 26-33
23. Visschedyk, D., Rochon, A., Tempel, W., Dimov, S., Park, H. W., and Merrill, A. R. (2012) Certhrax toxin, an anthrax-related ADP-ribosyltransferase from Bacillus cereus. J. Biol. Chem. 287, 41089-41102
24. Visschedyk, D. D., Perieteanu, A. A., Turgeon, Z. J., Fieldhouse, R. J., Dawson, J. F., and Merrill, A. R. (2010) Photox, a novel actin-targeting mono-ADP-ribosyltransferase from Photorhabdus luminescens. J. Biol. Chem. 285, 13525-13534
25. Turgeon, Z., Jørgensen, R., Visschedyk, D., Edwards, P. R., Legree, S., McGregor, C., Fieldhouse, R. J., Mangroo, D., Schapira, M., and Merrill, A. R. (2011) Newly discovered and characterized antivirulence compounds inhibit bacterial mono-ADP-ribosyltransferase toxins. Antimicrob. Agents Chemother. 55, 983-991
26. Niesen, F. H., Berglund, H., and Vedadi, M. (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2, 2212-2221
27. Sakurai, J., Nagahama, M., Hisatsune, J., Katunuma, N., and Tsuge, H. (2003) Clostridium perfringens ι-toxin, ADP-ribosyltransferase: structure and mechanism of action. Adv. Enzyme Regul. 43, 361-377
28. Han, S., Arvai, A. S., Clancy, S. B., and Tainer, J. A. (2001) Crystal structure and novel recognition motif of rho ADP-ribosylating C3 exoenzyme from Clostridium botulinum: structural insights for recognition specificity and catalysis. J. Mol. Biol. 305, 95-107
29. Ravulapalli, R., Lugo, M. R., Pfoh, R., Visschedyk, D., Poole, A., Fieldhouse, R. J., Pai, E. F., and Merrill, A. R. (2015) Characterization of vis toxin, a novel ADP-ribosyltransferase from Vibrio splendidus. Biochemistry 54, 5920-5936
30. Lesnick, M. L., Reiner, N. E., Fierer, J., and Guiney, D. G. (2001) The Salmonella spvB virulence gene encodes an enzyme that ADP-ribosylates actin and destabilizes the cytoskeleton of eukaryotic cells. Mol. Microbiol. 39, 1464-1470
31. Vogelsgesang, M., Pautsch, A., and Aktories, K. (2007) C3 exoenzymes, novel insights into structure and action of Rho-ADP-ribosylating toxins. Naunyn Schmiedebergs Arch. Pharmacol. 374, 347-360
32. Aktories, K., Rösener, S., Blaschke, U., and Chhatwal, G. S. (1988) Botulinum ADP-ribosyltransferase C3: purification of the enzyme and characterization of the ADP-ribosylation reaction in platelet membranes. Eur. J. Biochem. 172, 445-450
33. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948
34. Barbieri, J. T., Mende-Mueller, L. M., Rappuoli, R., and Collier, R. J. (1989) Photolabeling of Glu-129 of the S-1 subunit of pertussis toxin with NAD. Infect. Immun. 57, 3549-3554
35. Yates, S. P., Taylor, P. L., Jørgensen, R., Ferraris, D., Zhang, J., Andersen, G. R., and Merrill, A. R. (2005) Structure-function analysis of water-soluble inhibitors of the catalytic domain of exotoxin A from Pseudomonas aeruginosa. Biochem. J. 385, 667-675
36. Jørgensen, R., Purdy, A. E., Fieldhouse, R. J., Kimber, M. S., Bartlett, D. H., and Merrill, A. R. (2008) Cholix toxin, a novel ADP-ribosylating factor from Vibrio cholerae. J. Biol. Chem. 283, 10671-10678
37. Jørgensen, R., Merrill, A. R., Yates, S. P., Marquez, V. E., Schwan, A. L., Boesen, T., and Andersen, G. R. (2005) Exotoxin A-eEF2 complex structure indicates ADP ribosylation by ribosome mimicry. Nature 436, 979-984
38. Tsurumura, T., Tsumori, Y., Qiu, H., Oda, M., Sakurai, J., Nagahama, M., and Tsuge, H. (2013) Arginine ADP-ribosylation mechanism based on structural snapshots of ι-toxin and actin complex. Proc. Natl. Acad. Sci. U.S.A. 110, 4267-4272
39. Parikh, S. L., and Schramm, V. L. (2004) Transition state structure for ADP-ribosylation of eukaryotic elongation factor 2 catalyzed by diphtheria toxin. Biochemistry 43, 1204-1212
40. Lugo, M. R., and Merrill, A. R. (2015) A comparative structure-function analysis of active-site inhibitors of Vibrio cholerae cholix toxin. J. Mol. Recognit. 28, 539-552
41. Lugo, M. R., and Merrill, A. R. (2015) Pocket analysis of the full-length cholix toxin: an assessment of the structure-dynamics of the apo catalytic domain. J. Biomol. Struct. Dyn. 33, 2452-2468
42. Joshi, M. V., Mann, S. G., Antelmann, H., Widdick, D. A., Fyans, J. K., Chandra, G., Hutchings, M. I., Toth, I., Hecker, M., Loria, R., and Palmer, T. (2010) The twin arginine protein transport pathway exports multiple virulence proteins in the plant pathogen Streptomyces scabies. Mol. Microbiol. 77, 252-271
43. Fieldhouse, R. J., Turgeon, Z., White, D., and Merrill, A. R. (2010) Choleraand anthrax-like toxins are among several new ADP-ribosyltransferases. PLoS Comput. Biol. 6, e1001029
44. Lugo, M. R., Ravulapalli, R., Dutta, D., and Merrill, A. R. (2016) Structural variability of C3larvin toxin: intrinsic dynamics of the α/β fold of the C3-like group of mono-ADP-ribosyltransferase toxins. J. Biomol. Struct. Dyn. 26, 1-62
45. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308