Structural basis for the NAD-hydrolysis mechanism and the ARTT-loop plasticity of C3 exoenzymes

Protein Science

Volumn 17, Issue 5, 2008, Pages 878-886

  Ménétrey, Julie ^a,b,f   Flatau, Gilles ^c   Boquet, Patrice ^c   Ménez, André ^d   Stura, Enrico A ^e  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c INSERM   (France)

^d Museum d'Histoire Naturalle   (France)

^e Institute Frederic Joliot   (France)

^f INSTITUT CURIE   (France)

Author keywords

ADP ribosyltransferase; ARTT loop; C3 exoenzyme; Crystal structures; Plasticity

Indexed keywords

EXOENZYME C3; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ARTICLE; CLOSTRIDIUM BOTULINUM; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; STRUCTURE ANALYSIS; WILD TYPE;

ADP RIBOSE TRANSFERASES; AMINO ACID SUBSTITUTION; ASPARAGINE; BINDING SITES; BOTULINUM TOXINS; CRYSTALLOGRAPHY, X-RAY; GLUTAMIC ACID; HYDROLYSIS; MUTATION; NAD; PROTEIN CONFORMATION;

CLOSTRIDIUM BOTULINUM;

EID: 43049108453     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.073398508     Document Type: Article

References (34)

1. Aktories, K. and Frevert, J. 1987. ADP-ribosylation of a 21-24 kDa eukaryotic protein(s) by C3, a novel botulinum ADP-ribosyltransferase, is regulated by guanine nucleotide. Biochem. J. 247: 363-368.
2. Aktories, K., Rosener, 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.
3. Aktories, K., Jung, M., Bohmer, J., Fritz, G., Vandekerckhove, J., and Just, I. 1995. Studies on the active-site structure of C3-like exoenzymes: Involvement of glutamic acid in catalysis of ADP-ribosylation. Biochimie 77: 326-332.
4. Aktories, K., Wilde, C., and Vogelsgesang, M. 2004. Rho-modifying C3-like ADP-ribosyltransferases. Rev. Physiol. Biochem. Pharmacol. 152: 1-22.
5. Bohmer, J., Jung, M., Sehr, P., Fritz, G., Popoff, M., Just, I., and Aktories, K. 1996. Active site mutation of the C3-like ADP-ribosyltransferase from Clostridium limosum - analysis of glutamic acid 174. Biochemistry 35: 282-289.
6. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
7. Esnouf, R.M. 1999. Bobscript: Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr. D Biol. Crystallogr. 55: 938-940.
8. Etienne-Manneville, S. and Hall, A. 2002. Rho GTPases in cell biology. Nature 420: 629-635.
9. Evans, H.R., Sutton, J.M., Holloway, D.E., Ayriss, J., Shone, C.C., and Acharya, K.R. 2003. The crystal structure of C3stau2 from Staphylococcus aureus and its complex with NAD. J. Biol. Chem. 278: 45924-45930.
10. Genth, H., Gerhard, R., Maeda, A., Amano, M., Kaibuchi, K., Aktories, K., and Just, I. 2003a. Entrapment of Rho ADP-ribosylated by Clostridium botulinum C3 exoenzyme in the Rho-guanine nucleotide dissociation inhibitor-1 complex. J. Biol. Chem. 278: 28523-28527.
11. Genth, H., Schmidt, M., Gerhard, R., Aktories, K., and Just, I. 2003b. Activation of phospholipase D1 by ADP-ribosylated RhoA. Biochem. Biophys. Res. Commun. 302: 127-132.
12. Han, S. and Tainer, J.A. 2002. The ARTT motif and a unified structural understanding of substrate recognition in ADP-ribosylating bacterial toxins and eukaryotic ADP-ribosyltransferases. Int. J. Med. Microbiol. 291: 523-529.
13. 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.
14. Inoue, S., Sugai, M., Murooka, Y., Paik, S.Y., Hong, Y.M., Ohgai, H., and Suginaka, H. 1991. Molecular cloning and sequencing of the epidermal cell differentiation inhibitor gene from Staphylococcus aureus. Biochem. Biophys. Res. Commun. 174: 459-464.
15. Just, I., Mohr, C., Schallehn, G., Menard, L., Didsbury, J.R., Vandekerckhove, J., van Damme, J., and Aktories, K. 1992. Purification and characterization of an ADP-ribosyltransferase produced by Clostridium limosum. J. Biol. Chem. 267: 10274-10280.
16. Just, I., Selzer, J., Jung, M., van Damme, J., Vandekerckhove, J., and Aktories, K. 1995. Rho-ADP-ribosylating exoenzyme from Bacillus cereus. Purification, characterization, and identification of the NAD-binding site. Biochemistry 34: 334-340.
17. Kraulis, P.J. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946-950.
18. Ménétrey, J. and Ménez, A. 2006. Structural features of bacterial ADP-ribosyltransferase toxins. In Recent Research Developments in Toxins from Bacteria and Other Organisms (eds. D. Gillet and L. Johannes), pp. 241-263. Research Signpost, Kerala, India.
19. Ménétrey, J., Flatau, G., Stura, E.A., Charbonnier, J., Gas, F., Teulon, J., Le Du, M., Boquet, P., and Ménez, A. 2002. NAD binding induces conformational changes in Rho ADP-ribosylating Clostridium botulinum C3 exoenzyme. J. Biol. Chem. 277: 30950-30957.
20. Navaza, J. 1994. AMoRe: An automated package for molecular replacement. Acta Crystallogr. A 50: 157-163.
21. Nemoto, Y., Namba, T., Kozaki, S., and Narumiya, S. 1991. Clostridium botulinum C3 ADP-ribosyltransferase gene. Cloning, sequencing, and expression of a functional protein in Escherichia coli. J. Biol. Chem. 266: 19312-19319.
22. Otwinowski, Z. and Minor, W. 1997. HKL package. Methods Enzymol. 276: 307-326.
23. Perrakis, A., Morris, R.M., and Lamzin, V.S. 1999. ARP/wARP can be employed for automatic density interpretation and tracing of a protein model. Resolution around 2.0 Å is the current limit. . .but we are working on it!. Nat. Struct. Biol. 6: 458-463.
24. Roussel, A. and Cambillaud, C. 1989. Turbo. In Silicon Graphics Geometry Partner Directory (ed. Silicon Graphics), pp. 77-78. Silicon Graphics, Mountain View, CA.
25. Rubin, E.J., Gill, D.M., Boquet, P., and Popoff, M.R. 1988. Functional modification of a 21-kilodalton G protein when ADP-ribosylated by exoenzyme C3 of Clostridium botulinum. Mol. Cell. Biol. 8: 418-426.
26. Saito, Y., Nemoto, Y., Ishizaki, T., Watanabe, N., Morii, N., and Narumiya, S. 1995. Identification of Glu173 as the critical amino acid residue for the ADP- ribosyltransferase activity of Clostridium botulinum C3 exoenzyme. FEBS Lett. 371: 105-109.
27. Sehr, P., Joseph, G., Genth, H., Just, I., Pick, E., and Aktories, K. 1998. Glucosylation and ADP ribosylation of rho proteins: Effects on nucleotide binding, GTPase activity, and effector coupling. Biochemistry 37: 5296-5304.
28. Sekine, A., Fujiwara, M., and Narumiya, S. 1989. Asparagine residue in the Rho gene product is the modification site for botulinum ADP- ribosyltransferase. J. Biol. Chem. 264: 8602-8605.
29. Stura, E.A. 1998. Strategy 3: Reverse screening. In Protein crystallization: Techniques, strategies and tips. A laboratory manual (ed. T.M. Bergfors), pp. 113-124. International University Line, La Jolla, CA.
30. Wilde, C., Chhatwal, G.S., Schmalzing, G., Aktories, K., and Just, I. 2001. A novel C3-like ADP-ribosyltransferase from Staphylococcus aureus modifying RhoE and Rnd3. J. Biol. Chem. 276: 9537-9542.
31. Wilde, C., Barth, H., Sehr, P., Han, L., Schmidt, M., Just, I., and Aktories, K. 2002a. Interaction of the Rho-ADP-ribosylating C3 exoenzyme with RalA. J. Biol. Chem. 277: 14771-14776.
32. Wilde, C., Just, I., and Aktories, K. 2002b. Structure-function analysis of the Rho-ADP-ribosylating exoenzyme C3stau2 from Staphylococcus aureus. Biochemistry 41: 1539-1544.
33. Wilde, C., Vogelsgesang, M., and Aktories, K. 2003. Rho-specific Bacillus cereus ADP-ribosyltransferase C3cer cloning and characterization. Biochemistry 42: 9694-9702.
34. Yamaguchi, T., Hayashi, T., Takami, H., Ohnishi, M., Murata, T., Nakayama, K., Asakawa, K., Ohara, M., Komatsuzawa, H., and Sugai, M. 2001. Complete nucleotide sequence of a Staphylococcus aureus exfoliative toxin B plasmid and identification of a novel ADP-ribosyltransferase, EDIN-C. Infect. Immun. 69: 7760-7771.