Mechanistic and structural insights into the proteolytic activation of Vibrio cholerae MARTX toxin

Nature Chemical Biology

Volumn 5, Issue 7, 2009, Pages 469-478

  Shen, Aimee ^a   Lupardus, Patrick J ^a   Albrow, Victoria E ^a   Guzzetta, Andrew ^a   Powers, James C ^b   Garcia, K Christopher ^a   Bogyo, Matthew ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLERA TOXIN; CYSTEINE PROTEINASE INHIBITOR; MARTX TOXIN; PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME SPECIFICITY; MUTATIONAL ANALYSIS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; VIBRIO; VIBRIO CHOLERAE;

EID: 67650290548     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.178     Document Type: Article

References (36)

1. Satchel l, K.J. MARTX, multifunctional autoprocessing repeats-in-toxin toxins. Infect. Immun. 75, 5079-5084 (2007).
2. Li, L, Rock, J.L. & Nelson, D.R. Identification and characterization of a repeat-in-toxin gene cluster in Vibrio anguillarum. Infect. Immun. 76, 2620-2632 (2008).
3. Lee, B.C. et al. Vibrio vulnificus rtxE is important for virulence, and its expression is induced by exposure to host cells. Infect. Immun. 76, 1509-1517 (2008).
4. Lee, J.H. et al. Identification and characterization of the Vibrio vulnificus rtxA essential for cytotoxicity in vitro and virulence in mice. J. Microbiol. 45, 146-152 (2007).
5. Liu, M., Alice, A.F., Naka, H. & Crosa, J.H. The HlyU protein is a positive regulator of rtxA1, a gene responsible for cytotoxicity and virulence in the human pathogen Vibrio vulnificus. Infect. Immun. 75, 3282-3289 (2007).
6. Olivier, V., Haines III, G.K., Tan, Y. & Satchel l, K.J. Hemolysin and the multifunctional autoprocessing RTX toxin are virulence factors during intestinal infection of mice with Vibrio cholerae El Tor O1 strains. Infect. Immun. 75, 5035-5042 (2007).
7. Olivier, V., Salzman, N.H. & Satchell, K.J. Prolonged colonization of mice by Vibrio cholerae El Tor O1 depends on accessory toxins. Infect. Immun. 75, 5043-5051 (2007).
8. Cordero, C.L., Sozhamannan, S. & Satchel l, K.J. RTX toxin actin cross-linking activity in clinical and environmental isolates of Vibrio cholerae. J. Clin. Microbiol. 45, 2289-2292 (2007).
9. Rahman, M.H. et al. Distribution of genes for virulence and ecological fitness among diverse Vibrio cholerae population in a cholera endemic area: tracking the evolution of pathogenic strains. DNA Cell Biol. 27, 347-355 (2008).
10. Sheahan, K.L., Cordero, C.L. & Satchel l, K.J. Identification of a domain within the multifunctional Vibrio cholerae RTX toxin that covalently cross-links actin. Proc. Natl. Acad. Sci. USA 101, 9798-9803 (2004).
11. Sheahan, K.L. & Satchel l, K.J. Inactivation of small Rho GTPases by the multifunctional RTX toxin from Vibrio cholerae. Cell. Microbiol. 9, 1324-1335 (2007).
12. Sheahan, K.L., Cordero, C.L. & Satchel l, K.J. Autoprocessing of the Vibrio cholerae RTX toxin by the cysteine protease domain. EMBO J. 26, 2552-2561 (2007).
13. Lupardus, P.J., Shen, A., Bogyo, M. & Garcia, K.C. Small molecule-induced allosteric activation of the Vibrio cholerae RTX cysteine protease domain. Science 322, 265-268 (2008).
14. Egerer, M., Giesemann, T., Jank, T., Satchell, K.J. & Aktories, K. Auto-catalytic cleavage of Clostridium difficile toxins A and B depends on cysteine protease activity. J. Biol. Chem. 282, 25314-25321 (2007).
15. Giesemann, T., Egerer, M., Jank, T. & Aktories, K. Processing of Clostridium difficile toxins. J. Med. Microbiol. 57, 690-696 (2008).
16. Reineke, J. et al. Autocatalytic cleavage of Clostridium difficile toxin B. Nature 446, 415-419 (2007).
17. Gordon, V.M. & Leppla, S.H. Proteolytic activation of bacterial toxins: role of bacterial and host cell proteases. Infect. Immun. 62, 333-340 (1994).
18. Arastu-Kapur, S. et al. Identification of proteases that regulate erythrocyte rupture by the malaria parasite Plasmodium falciparum. Nat. Chem. Biol. 4, 203-213 (2008).
19. Powers, J.C., Asgian, J.L., Ekici, O.D. & James, K.E. Irreversible inhibitors of serine, cysteine, and threonine proteases. Chem. Rev. 102, 4639-4750 (2002).
20. Prochazkova, K. & Satchel l, K.J. Structure-function analysis of inositol hexakispho-sphate-induced autoprocessing of the Vibrio cholerae multifunctional autoprocessing RTX toxin. J. Biol. Chem. 283, 23656-23664 (2008).
21. Asgian, J.L. et al. Aza-peptide epoxides: a new class of inhibitors selective for clan CD cysteine proteases. J. Med. Chem. 45, 4958-4960 (2002).
22. Ganesan, R. et al. Exploring the S4 and S1 prime subsite specificities in caspase-3 with aza-peptide epoxide inhibitors. Biochemistry 45, 9059-9067 (2006).
23. Barrett, A.J. & Rawlings, N.D. Evolutionary lines of cysteine peptidases. Biol. Chem. 382, 727-733 (2001).
24. Bedard, K.M. & Semler, B.L. Regulation of picornavirus gene expression. Microbes Infect. 6, 702-713 (2004).
25. Reed, K.E. & Rice, CM. Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr. Top. Microbiol. Immunol. 242, 55-84 (2000).
26. Schilling, O. & Overall, CM. Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites. Nat. Biotechnol. 26, 685-694 (2008).
27. Stennicke, H.R., Renatus, M., Meldal, M. & Salvesen, G.S. Internally quenched fluorescent peptide substrates disclose the subsite preferences of human caspases 1, 3, 6, 7 and 8. Biochem. J. 350, 563-568 (2000).
28. Eichinger, A. et al. Crystal structure of gingipain R: an Arg-specific bacterial cysteine proteinase with a caspase-like fold. EMBO J. 18, 5453-5462 (1999).
29. Kato, D. et al. Activity-based probes that target diverse cysteine protease families. Nat. Chem. Biol. 1, 33-38 (2005).
30. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
31. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
32. Brunger, A.T. et al. Crystallography & NMR system: a new software suite for macro-molecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
33. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
34. Davis, I.W. et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383 (2007).
35. Potterton, E., Briggs, P., Turkenburg, M. & Dodson, E. A graphical user interface to the CCP4 program suite. Acta Crystallogr. D Biol. Crystallogr. 59, 1131-1137 (2003).
36. DeLano, W.L. The PyMOL Molecular Graphics System (DeLano Scientific, San Carlos, California, USA, 2002).