Mycobacterium tuberculosis RsdA provides a conformational rationale for selective regulation of σ-factor activity by proteolysis

Nucleic Acids Research

Volumn 41, Issue 5, 2013, Pages 3414-3423

  Jaiswal, Ravi K ^a   Prabha, Tangirala Surya ^a   Manjeera, Gowravaram ^a   Gopal, Balasubramanian ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN RSDA; RECOMBINANT PROTEIN; SIGMA FACTOR; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTALLIZATION; MOLECULAR DYNAMICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA, BACTERIAL; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; SIGMA FACTOR;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 84876404291     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1468     Document Type: Article

References (47)

1. Rodrigue, S., Provvedi, R., Jacques, P.E., Gaudreau, L. and Manganelli, R. (2006) The sigma factors of Mycobacterium tuberculosis. FEMS Microbiol. Rev., 30, 926-941.
2. Sachdeva, P., Misra, R., Tyagi, A.K. and Singh, Y. (2009) The sigma factors of Mycobacterium tuberculosis: regulation of the regulators. FEBS J., 277, 605-626.
3. Baker, T.A. and Sauer, R.T. (2011) ClpXP, an ATP-powered unfolding and protein-degradation machine. Biochim. Biophys. Acta, 1823, 15-28.
4. Hanson, P.I. and Whiteheart, S.W. (2005) AAA+proteins: have engine, will work. Nat. Rev. Mol. Cell. Biol., 6, 519-529.
5. Wojtkowiak, D., Georgopoulos, C. and Zylicz, M. (1993) Isolation and characterization of ClpX, a new ATP-dependent specificity component of the Clp protease of Escherichia coli. J. Biol. Chem., 268, 22609-22617.
6. Wang, J., Hartling, J.A. and Flanagan, J.M. (1997) The structure of ClpP at 2.3 A resolution suggests a model for ATP-dependent proteolysis. Cell, 91, 447-456.
7. Kessel, M., Maurizi, M.R., Kim, B., Kocsis, E., Trus, B.L., Singh, S.K. and Steven, A.C. (1995) Homology in structural organization between E. coli ClpAP protease and the eukaryotic 26 S proteasome. J. Mol. Biol., 250, 587-594.
8. Chaba, R., Grigorova, I.L., Flynn, J.M., Baker, T.A. and Gross, C.A. (2007) Design principles of the proteolytic cascade governing the sigmaE-mediated envelope stress response in Escherichia coli: keys to graded, buffered, and rapid signal transduction. Genes Dev., 21, 124-136.
9. Flynn, J.M., Neher, S.B., Kim, Y.I., Sauer, R.T. and Baker, T.A. (2003) Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell, 11, 671-683.
10. Heinrich, J. and Wiegert, T. (2009) Regulated intramembrane proteolysis in the control of extracytoplasmic function sigma factors. Res. Microbiol., 160, 696-703.
11. Qiu, D., Eisinger, V.M., Head, N.E., Pier, G.B. and Yu, H.D. (2008) ClpXP proteases positively regulate alginate overexpression and mucoid conversion in Pseudomonas aeruginosa. Microbiology, 154, 2119-2130.
12. Zellmeier, S., Schumann, W. and Wiegert, T. (2006) Involvement of Clp protease activity in modulating the Bacillus subtilis sigmaW stress response. Mol. Microbiol., 61, 1569-1582.
13. Raju, R.M., Unnikrishnan, M., Rubin, D.H., Krishnamoorthy, V., Kandror, O., Akopian, T.N., Goldberg, A.L. and Rubin, E.J. (2012) Mycobacterium tuberculosis ClpP1 and ClpP2 function together in protein degradation and are required for viability in vitro and during infection. PLoS Pathog., 8, e1002511.
14. Akopian, T., Kandror, O., Raju, R.M., Unnikrishnan, M., Rubin, E.J. and Goldberg, A.L. (2012) The active ClpP protease from M. tuberculosis is a complex composed of a heptameric ClpP1 and a ClpP2 ring. EMBO J., 31, 1529-1541.
15. Sklar, J.G., Makinoshima, H., Schneider, J.S. and Glickman, M.S. (2010) M. tuberculosis intramembrane protease Rip1 controls transcription through three anti-sigma factor substrates. Mol. Microbiol., 77, 605-617.
16. Thakur, K.G., Praveena, T. and Gopal, B. (2010) Structural and biochemical bases for the redox sensitivity of Mycobacterium tuberculosis RslA. J. Mol. Biol., 397, 1199-1208.
17. Calamita, H., Ko, C., Tyagi, S., Yoshimatsu, T., Morrison, N.E. and Bishai, W.R. (2005) The Mycobacterium tuberculosis SigD sigma factor controls the expression of ribosome-associated gene products in stationary phase and is required for full virulence. Cell. Microbiol., 7, 233-244.
18. Raman, S., Hazra, R., Dascher, C.C. and Husson, R.N. (2004) Transcription regulation by the Mycobacterium tuberculosis alternative sigma factor SigD and its role in virulence. J. Bacteriol., 186, 6605-6616.
19. Shenoy, A.R. and Visweswariah, S.S. (2003) Site-directed mutagenesis using a single mutagenic oligonucleotide and DpnI digestion of template DNA. Anal. Biochem., 319, 335-336.
20. Battye, T.G., Kontogiannis, L., Johnson, O., Powell, H.R. and Leslie, A.G. (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr., 67, 271-281.
21. 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. et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr., 67, 235-242.
22. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
23. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
24. Painter, J. and Merritt, E.A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. J. Appl. Cryst., 39, 109-111.
25. Jorgensen, W., Maxwell, D. and Tirado-Rives, J. (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc., 118, 11225-11236.
26. Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A.E. and Berendsen, H.J. (2005) GROMACS: fast, flexible, and free. J. Comput. Chem., 26, 1701-1718.
27. Berk Hess, H.B., Berendsen, H.J.C. and Fraaije, J.G. (1997) LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem., 18, 1463-1472.
28. Kabsch, W. and Sander, C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
29. Smoot, M.E., Ono, K., Ruscheinski, J., Wang, P.L. and Ideker, T. (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics, 27, 431-432.
30. Thakur, K.G., Jaiswal, R.K., Shukla, J.K., Praveena, T. and Gopal, B. (2010) Over-expression and purification strategies for recombinant multi-protein oligomers: a case study of Mycobacterium tuberculosis sigma/anti-sigma factor protein complexes. Protein Expr Purif, 74, 223-230.
31. Campbell, E.A., Greenwell, R., Anthony, J.R., Wang, S., Lim, L., Das, K., Sofia, H.J., Donohue, T.J. and Darst, S.A. (2007) A conserved structural module regulates transcriptional responses to diverse stress signals in bacteria. Mol. Cell, 27, 793-805.
32. Campbell, E.A., Tupy, J.L., Gruber, T.M., Wang, S., Sharp, M.M., Gross, C.A. and Darst, S.A. (2003) Crystal structure of Escherichia coli sigmaE with the cytoplasmic domain of its anti-sigma RseA. Mol. Cell, 11, 1067-1078.
33. Lambert, L.J., Wei, Y., Schirf, V., Demeler, B. and Werner, M.H. (2004) T4 AsiA blocks DNA recognition by remodeling sigma70 region 4. EMBO J., 23, 2952-2962.
34. Vassylyev, D.G., Sekine, S., Laptenko, O., Lee, J., Vassylyeva, M.N., Borukhov, S. and Yokoyama, S. (2002) Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 A resolution. Nature, 417, 712-719.
35. Lane, W.J. and Darst, S.A. (2006) The structural basis for promoter -35 element recognition by the group IV sigma factors. PLoS Biol., 4, e269.
36. Patikoglou, G.A., Westblade, L.F., Campbell, E.A., Lamour, V., Lane, W.J. and Darst, S.A. (2007) Crystal structure of the Escherichia coli regulator of sigma70, Rsd, in complex with sigma70 domain 4. J. Mol. Biol., 372, 649-659.
37. Buchan, D.W., Ward, S.M., Lobley, A.E., Nugent, T.C., Bryson, K. and Jones, D.T. (2010) Protein annotation and modelling servers at University College London. Nucleic Acids Res., 38, W563-W568.
38. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
39. Sharma, A., Sekar, K. and Vijayan, M. (2009) Structure, dynamics, and interactions of jacalin. Insights from molecular dynamics simulations examined in conjunction with results of X-ray studies. Proteins, 77, 760-777.
40. Luo, P. and Baldwin, R.L. (1997) Mechanism of helix induction by trifluoroethanol: a framework for extrapolating the helix-forming properties of peptides from trifluoroethanol/water mixtures back to water. Biochemistry, 36, 8413-8421.
41. Flynn, J.M., Levchenko, I., Sauer, R.T. and Baker, T.A. (2004) Modulating substrate choice: the SspB adaptor delivers a regulator of the extracytoplasmic-stress response to the AAA+ protease ClpXP for degradation. Genes Dev., 18, 2292-2301.
42. Kim, J.H., Wei, J.R., Wallach, J.B., Robbins, R.S., Rubin, E.J. and Schnappinger, D. (2010) Protein inactivation in mycobacteria by controlled proteolysis and its application to deplete the beta subunit of RNA polymerase. Nucleic Acids Res., 39, 2210-2220.
43. Barik, S., Sureka, K., Mukherjee, P., Basu, J. and Kundu, M. (2010) RseA, the SigE specific anti-sigma factor of Mycobacterium tuberculosis, is inactivated by phosphorylation-dependent ClpC1P2 proteolysis. Mol. Microbiol., 75, 592-606.
44. Ingvarsson, H., Mate, M.J., Hogbom, M., Portnoi, D., Benaroudj, N., Alzari, P.M., Ortiz-Lombardia, M. and Unge, T. (2007) Insights into the inter-ring plasticity of caseinolytic proteases from the X-ray structure of Mycobacterium tuberculosis ClpP1. Acta Crystallogr. D Biol. Crystallogr., 63, 249-259.
45. Benaroudj, N., Raynal, B., Miot, M. and Ortiz-Lombardia, M. (2011) Assembly and proteolytic processing of mycobacterial ClpP1 and ClpP2. BMC Biochem., 12, 61.
46. Kim, Y.I., Burton, R.E., Burton, B.M., Sauer, R.T. and Baker, T.A. (2000) Dynamics of substrate denaturation and translocation by the ClpXP degradation machine. Mol. Cell, 5, 639-648.
47. Kirstein, J., Moliere, N., Dougan, D.A. and Turgay, K. (2009) Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+proteases. Nat. Rev. Microbiol., 7, 589-599.