Helix unfolding/refolding characterizes the functional dynamics of staphylococcus aureus clp protease

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17643-17653

  Ye, Fei ^a   Zhang, Jie ^a   Liu, Hongchuan ^a   Hilgenfeld, Rolf ^a,b   Zhang, Ruihan ^a   Kong, Xiangqian ^a   Li, Lianchun ^a   Lu, Junyan ^a   Zhang, Xinlei ^a,c   Li, Donghai ^d   Jiang, Hualiang ^a   Yang, Cai Guang ^a,e   Luo, Cheng ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b UNIVERSITY OF LÜBECK   (Germany)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d NANJING UNIVERSITY   (China)

^e LANZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBACTERIAL TREATMENT; BACTERIAL PATHOGENS; FUNCTIONAL CONFORMATIONS; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR INSIGHTS; STAPHYLOCOCCUS AUREUS; STRUCTURAL TRANSITIONS; SWITCHING MECHANISM;

BACTERIA; MOLECULAR DYNAMICS; MONOMERS; PROTEINS; X RAY CRYSTALLOGRAPHY;

DYNAMICS;

ALANINE; ENDOPEPTIDASE CLP; GLUTAMINE; MONOMER;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME STABILITY; HELIX E; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN REFOLDING; PROTEIN STRUCTURE; PROTEIN UNFOLDING; SEQUENCE ANALYSIS; STAPHYLOCOCCUS AUREUS; X RAY CRYSTALLOGRAPHY;

BACTERIAL PATHOGENESIS; CLP PROTEASE; COMPUTATIONAL BIOLOGY; CRYSTAL STRUCTURE; ENERGY LANDSCAPE; MOLECULAR DYNAMICS; PRINCIPLE-COMPONENT ANALYSIS; PROTEIN DYNAMICS;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; ENDOPEPTIDASE CLP; ENZYME STABILITY; HYDROGEN BONDING; MOLECULAR DYNAMICS SIMULATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN REFOLDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; STAPHYLOCOCCUS AUREUS; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 84879043308     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.452714     Document Type: Article

References (54)

1. Walsh, C., and Wright, G. (2005) Introduction. Antibiotic resistance. Chem. Rev. 105, 391-394
2. Williams, K. J., and Bax, R. P. (2009) Curr. Opin. Biotechnol. 10, 157-163
3. + proteases and disassembly machines. Cell 119, 9-18
4. Baker, T. A., and Sauer, R. T. (2006) ATP-dependent proteases of bacteria. Recognition logic and operating principles. Trends Biochem. Sci. 31, 647-653 (Pubitemid 44791948)
5. Wong, P., and Houry, W. A. (2004) Chaperone networks in bacteria. Analysis of protein homeostasis in minimal cells. J. Struct. Biol. 146, 79-89 (Pubitemid 38369020)
6. + ClpX machine mediate unassisted and adaptor-dependent recognition of ssrA-tagged substrates. Mol. Cell 29, 441-450
7. Frees, D., Chastanet, A., Qazi, S., Sørensen, K., Hill, P., Msadek, T., and Ingmer, H. (2004) Clp ATPases are required for stress tolerance, intracellular replication, and biofilm formation in Staphylococcus aureus. Mol. Microbiol. 54, 1445-1462 (Pubitemid 39578284)
8. Frees, D., Qazi, S. N., Hill, P. J., and Ingmer, H. (2003) Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence. Mol. Microbiol. 48, 1565-1578 (Pubitemid 36751062)
9. Michel, A., Agerer, F., Hauck, C. R., Herrmann, M., Ullrich, J., Hacker, J., and Ohlsen, K. (2006) Global regulatory impact of ClpP protease of Staphylococcus aureus on regulons involved in virulence, oxidative stress response, autolysis, and DNA repair. J. Bacteriol. 188, 5783-5796 (Pubitemid 44384086)
10. Donegan, N. P., Thompson, E. T., Fu, Z., and Cheung, A. L. (2010) Proteolytic regulation of toxin-antitoxin systems by ClpPC in Staphylococcus aureus. J. Bacteriol. 192, 1416-1422
11. Brötz-Oesterhelt, H., Beyer, D., Kroll, H. P., Endermann, R., Ladel, C., Schroeder, W., Hinzen, B., Raddatz, S., Paulsen, H., Henninger, K., Bandow, J. E., Sahl, H. G., and Labischinski, H. (2005) Dysregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat. Med. 11, 1082-1087 (Pubitemid 41486830)
12. Böttcher, T., and Sieber, S. A. (2008) β-Lactones as specific inhibitors of ClpP attenuate the production of extracellular virulence factors of Staphylococcus aureus. J. Am. Chem. Soc. 130, 14400-14401
13. Böttcher, T., and Sieber, S. A. (2008) Beta-lactones as privileged structures for the active-site labeling of versatile bacterial enzyme classes. Angew. Chem. Int. Ed. Engl. 47, 4600-4603
14. Porankiewicz, J., Wang, J., and Clarke, A. K. (1999) New insights into the ATP-dependent Clp protease. Escherichia coli and beyond. Mol. Microbiol. 32, 449-458 (Pubitemid 29233891)
15. Lee, B. G., Park, E. Y., Lee, K. E., Jeon, H., Sung, K. H., Paulsen, H., Rübsamen-Schaeff, H., Brötz-Oesterhelt, H., and Song, H. K. (2010) Structures of ClpP in complex with acyldepsipeptide antibiotics reveal its activation mechanism. Nat. Struct. Mol. Biol. 17, 471-478
16. Li, D. H., Chung, Y. S., Gloyd, M., Joseph, E., Ghirlando, R., Wright, G. D., Cheng, Y. Q., Maurizi, M. R., Guarné, A., and Ortega, J. (2010) Acyldepsipeptide antibiotics induce the formation of a structured axial channel in ClpP. A model for the ClpX/ClpA-bound state of ClpP. Chem. Biol. 17, 959-969
17. Wang, J., Hartling, J. A., and Flanagan, J. M. (1997) The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis. Cell 91, 447-456 (Pubitemid 27508234)
18. Bewley, M. C., Graziano, V., Griffin, K., and Flanagan, J. M. (2006) The asymmetry in the mature amino-terminus of ClpP facilitates a local symmetry match in ClpAP and ClpXP complexes. J. Struct. Biol. 153, 113-128 (Pubitemid 43139692)
19. Szyk, A., and Maurizi, M. R. (2006) Crystal structure at 1.9Åof E. coli ClpP with a peptide covalently bound at the active site. J. Struct. Biol. 156, 165-174 (Pubitemid 44486061)
20. Kim, D. Y., and Kim, K. K. (2008) The structural basis for the activation and peptide recognition of bacterial ClpP. J. Mol. Biol. 379, 760-771
21. Lee, B. G., Kim, M. K., and Song, H. K. (2011) Structural insights into the conformational diversity of ClpP from Bacillus subtilis. Mol. Cells 32, 589-595
22. Kang, S. G., Maurizi, M. R., Thompson, M., Mueser, T., and Ahvazi, B. (2004) Crystallography and mutagenesis point to an essential role for the N-terminus of human mitochondrial ClpP. J. Struct. Biol. 148, 338-352 (Pubitemid 39441371)
23. Zhang, J., Ye, F., Lan, L., Jiang, H., Luo, C., and Yang, C. G. (2011) Structural switching of Staphylococcus aureus Clp protease. A key to understanding protease dynamics. J. Biol. Chem. 286, 37590-37601
24. Geiger, S. R., Böttcher, T., Sieber, S. A., and Cramer, P. (2011) A conformational switch underlies ClpP protease function. Angew. Chem. Int. Ed. Engl. 50, 5749-5752
25. Gersch, M., List, A., Groll, M., and Sieber, S. A. (2012) Insights into structural network responsible for oligomerization and activity of bacterial virulence regulator caseinolytic protease P (ClpP) protein. J. Biol. Chem. 287, 9484-9494
26. Kimber, M. S., Yu, A. Y., Borg, M., Leung, E., Chan, H. S., and Houry, W. A. (2010) Structural and theoretical studies indicate that the cylindrical protease ClpP samples extended and compact conformations. Structure 18, 798-808
27. Gribun, A., Kimber, M. S., Ching, R., Sprangers, R., Fiebig, K. M., and Houry, W. A. (2005) The ClpP double ring tetradecameric protease exhibits plastic ring-ring interactions, and theNtermini of its subunits form flexible loops that are essential for ClpXP and ClpAP complex formation. J. Biol. Chem. 280, 16185-16196 (Pubitemid 40616745)
28. Ingvarsson, H., Maté, M. J., Högbom, M., Portnoï, D., Benaroudj, N., Alzari, P. M., Ortiz-Lombardía, 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 (Pubitemid 46197542)
29. El Bakkouri, M., Pow, A., Mulichak, A., Cheung, K. L., Artz, J. D., Amani, M., Fell, S., de Koning-Ward, T. F., Goodman, C. D., McFadden, G. I., Ortega, J., Hui, R., and Houry, W. A. (2010) The Clp chaperones and proteases of the human malaria parasite Plasmodium falciparum. J. Mol. Biol. 404, 456-477
30. 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
31. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrodinger, LLC, New York
32. Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G., Zhang, W., Yang, R., Cieplak, P., Luo, R., Lee, T., Caldwell, J., Wang, J., and Kollman, P. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24, 1999-2012
33. Jorgensen, W. J., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935
34. Hess, B., Bekker, H., Berendsen, H., and Fraaije, J. (1997) LINCS. A linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463-1472 (Pubitemid 127637344)
35. Klapper, I., Hagstrom, R., Fine, R., Sharp, K., and Honig, B. (1986) Focusing of electric fields in the active site of Cu-Zn superoxide dismutase. Effects of ionic strength and amino-acid modification. Proteins 1, 47-59 (Pubitemid 17073401)
36. Warshel, A., and Aqvist, J. (1991) Electrostatic energy and macromolecular function. Annu. Rev. Biophys. Biophys. Chem. 20, 267-298
37. Yang, A. S., and Honig, B. (1994) Structural origins of pH and ionic strength effects on protein stability. Acid denaturation of sperm whale apomyoglobin. J. Mol. Biol. 237, 602-614
38. Bushey, M. M., and Jorgenson, J. W. (1989) Capillary electrophoresis of proteins in buffers containing high concentrations of zwitterionic salts. J. Chromatogr. 480, 301-310 (Pubitemid 19269321)
39. Gabdoulline, R. R., and Wade, R. C. (1997) Simulation of the diffusional association of barnase and barstar. Biophys. J. 72, 1917-1929 (Pubitemid 27184422)
40. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald. An N.log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
41. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690
42. Fletcher, R. (1980) Practical Methods of Optimization, Vol. 1, pp. 1-40, John Wiley & Sons, Inc., New York
43. Amadei, A., Linssen, A. B., and Berendsen, H. J. (1993) Essential dynamics of proteins. Proteins 17, 412-425 (Pubitemid 23358549)
44. Papaleo, E., Mereghetti, P., Fantucci, P., Grandori, R., and De Gioia, L. (2009) Free-energy landscape, principal component analysis, and structural clustering to identify representative conformations from molecular dynamics simulations. The myoglobin case. J. Mol. Graph. Model. 27, 889-899
45. Zhou, R., Berne, B. J., and Germain, R. (2001) The free energy landscape for β hairpin folding in explicit water. Proc. Natl. Acad. Sci. U.S.A. 98, 14931-14936 (Pubitemid 34013947)
46. García, A. E., and Sanbonmatsu, K. Y. (2001) Exploring the energy landscape of a β hairpin in explicit solvent. Proteins 42, 345-354
47. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
48. Collaborative Computational Project, Number 4 (1994) The CCP4 suite. Programs for protein crystallography. Acta Crystallogr.DBiol. Crystallogr. 50, 760-763
49. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
50. Kabsch, W., and Sander, C. (1983) Dictionary of protein secondary structure. Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637
51. as and adding missing hydrogens to macromolecules. Nucleic Acids Res. 33, W368-W371
52. Maglica, Z., Kolygo, K., and Weber-Ban, E. (2009) Optimal efficiency of ClpAP and ClpXP chaperone-proteases is achieved by architectural symmetry. Structure 17, 508-516
53. Maurizi, M. R., Singh, S. K., Thompson, M. W., Kessel, M., and Ginsburg, A. (1998) Molecular properties of ClpAP protease of Escherichia coli. ATP-dependent association of ClpA and clpP. Biochemistry 37, 7778-7786 (Pubitemid 28248637)
54. Sprangers, R., Gribun, A., Hwang, P. M., Houry, W. A., and Kay, L. E. (2005) Quantitative NMR spectroscopy of supramolecular complexes. Dynamic side pores in ClpP are important for product release. Proc. Natl. Acad. Sci. U.S.A. 102, 16678-16683 (Pubitemid 41688836) of China