Dynamics of the ClpP serine protease: A model for self-compartmentalized proteases

Critical Reviews in Biochemistry and Molecular Biology

Volumn 49, Issue 5, 2014, Pages 400-412

  Liu, Kaiyin ^a   Ologbenla, Adedeji ^a   Houry, Walid A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Catalysis; ClpP; Degaradation; Dynamics; Protease

Indexed keywords

CHAPERONE; ENDOPEPTIDASE CLP; POLYPEPTIDE; PROTEASOME; SERINE PROTEINASE;

HUMAN; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN HOMEOSTASIS; REVIEW; SELF COMPARTMENTALIZED PROTEASES; SEQUENCE ALIGNMENT; THEORETICAL STUDY; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; ENDOPEPTIDASE CLP; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, SECONDARY; SERINE PROTEASES; SUBSTRATE SPECIFICITY;

EID: 84907500301     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.3109/10409238.2014.925421     Document Type: Review

References (48)

1. Alexopoulos J, Ahsan B, Homchaudhuri L, et al. (2013). Structural determinants stabilizing the axial channel of ClpP for substrate translocation. Mol Microbiol 90: 167-80.
2. Baker TA, Sauer RT. (2012). ClpXP, an ATP-powered unfolding and protein-degradation machine. Biochim Biophys Acta 1823: 15-28.
3. Bewley MC, Graziano V, Griffin K, et al. (2006). The asymmetry in the mature amino-terminus of ClpP facilitates a local symmetry match in ClpAP and ClpXP complexes. J Struct Biol 153: 113-28.
4. Bochtler M, Ditzel L, Groll M, et al. (1997). Crystal structure of heat shock locus V (HslV) from Escherichia coli. Proc Natl Acad Sci USA 94: 6070-4.
5. Brotz-Oesterhelt H, Beyer D, Kroll HP, et al. (2005). Dysregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat Med 11: 1082-7.
6. Chuang SE, Burland V, Plunkett III G, et al. (1993). Sequence analysis of four new heat-shock genes constituting the hslTS/ibpAB and hslVU operons in Escherichia coli. Gene 134: 1-6.
7. De Mot R, Nagy I, Walz J, et al. (1999). Proteasomes and other selfcompartmentalizing proteases in prokaryotes. Trends Microbiol 7: 88-92.
8. DeLano WL. (2002). The PyMOL molecular graphics system. Palo Alto (CA): DeLano Scientific.
9. Effantin G, Ishikawa T, De Donatis GM, et al. (2010a). Local and global mobility in the ClpA AAA+ chaperone detected by cryo-electron microscopy: functional connotations. Structure 18: 553-62.
10. Effantin G, Maurizi MR, Steven AC. (2010b). Binding of the ClpA unfoldase opens the axial gate of ClpP peptidase. J Biol Chem 285: 14834-40.
11. El Bakkouri M, Pow A, Mulichak A, et al. (2010). The Clp chaperones and proteases of the human malaria parasite Plasmodium falciparum. J Mol Biol 404: 456-77.
12. Geiger SR, Bottcher T, Sieber SA, et al. (2011). A conformational switch underlies ClpP protease function. Angew Chem Int Ed Engl 50: 5749-52.
13. Gersch M, List A, Groll M, et al. (2012). Insights into structural network responsible for oligomerization and activity of bacterial virulence regulator caseinolytic protease P (ClpP) protein. J Biol Chem 287: 9484-94.
14. Gille C, Frommel C. (2001). STRAP: editor for STRuctural Alignments of Proteins. Bioinformatics 17: 377-8.
15. Gribun A, Kimber MS, Ching R, et al. (2005). The ClpP double ring tetradecameric protease exhibits plastic ring-ring interactions, and the N termini of its subunits form flexible loops that are essential for ClpXP and ClpAP complex formation. J Biol Chem 280: 16185-96.
16. Humbard MA, Maupin-Furlow JA. (2013). Prokaryotic proteasomes: nanocompartments of degradation. J Mol Microbiol Biotechnol 23: 321-34.
17. Ingvarsson H, Mate MJ, Hogbom M, et al. (2007). Insights into the interring plasticity of caseinolytic proteases from the X-ray structure of Mycobacterium tuberculosis ClpP1. Acta Crystallogr D Biol Crystallogr 63: 249-59.
18. Inobe T, Matouschek A. (2014). Paradigms of protein degradation by the proteasome. Curr Opin Struct Biol 24C: 156-64.
19. Jennings LD, Bohon J, Chance MR, et al. (2008a). The ClpP N-terminus coordinates substrate access with protease active site reactivity. Biochemistry (Mosc) 47: 11031-40.
20. Jennings LD, Lun DS, Medard M, et al. (2008b). ClpP hydrolyzes a protein substrate processively in the absence of the ClpA ATPase: mechanistic studies of ATP-independent proteolysis. Biochemistry (Mosc) 47: 11536-46.
21. Kang SG, Maurizi MR, Thompson M, et al. (2004). Crystallography and mutagenesis point to an essential role for the N-terminus of human mitochondrial ClpP. J Struct Biol 148: 338-52.
22. Katayama-Fujimura Y, Gottesman S, Maurizi MR. (1987). A multiplecomponent, ATP-dependent protease from Escherichia coli. J Biol Chem 262: 4477-85.
23. Katayama Y, Gottesman S, Pumphrey J, et al. (1988). The twocomponent, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component. J Biol Chem 263: 15226-36.
24. Kessel M, Wu W, Gottesman S, et al. (1996). Six-fold rotational symmetry of ClpQ, the E. coli homolog of the 20S proteasome, and its ATP-dependent activator, ClpY. FEBS Lett 398: 274-8.
25. Kim DY, Kim KK. (2008). The structural basis for the activation and peptide recognition of bacterial ClpP. J Mol Biol 379: 760-71.
26. Kim YI, Levchenko I, Fraczkowska K, et al. (2001). Molecular determinants of complex formation between Clp/Hsp100 ATPases and the ClpP peptidase. Nat Struct Biol 8: 230-3.
27. Kimber MS, Yu AY, Borg M, et al. (2010). Structural and theoretical studies indicate that the cylindrical protease ClpP samples extended and compact conformations. Structure 18: 798-808.
28. Lee BG, Kim MK, Song HK. (2011). Structural insights into the conformational diversity of ClpP from Bacillus subtilis. Mol Cells 32: 589-95.
29. Lee BG, Park EY, Lee KE, et al. (2010). Structures of ClpP in complex with acyldepsipeptide antibiotics reveal its activation mechanism. Nat Struct Mol Biol 17: 471-8.
30. Leung E, Datti A, Cossette M, et al. (2011). Activators of cylindrical proteases as antimicrobials: identification and development of small molecule activators of ClpP protease. Chem Biol 18: 1167-78.
31. Li DH, Chung YS, Gloyd M, et al. (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: 959-69.
32. Martin A, Baker TA, Sauer RT. (2007). Distinct static and dynamic interactions control ATPase-peptidase communication in a AAA+ protease. Mol Cell 27: 41-52.
33. Maurizi MR, Clark WP, Katayama Y, et al. (1990). Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J Biol Chem 265: 12536-45.
34. Ortega J, Lee HS, Maurizi MR, et al. (2004). ClpA and ClpX ATPases bind simultaneously to opposite ends of ClpP peptidase to form active hybrid complexes. J Struct Biol 146: 217-26.
35. Pickart CM, Cohen RE. (2004). Proteasomes and their kin: proteases in the machine age. Nat Rev Mol Cell Biol 5: 177-87.
36. Religa TL, Sprangers R, Kay LE. (2010). Dynamic regulation of archaeal proteasome gate opening as studied by TROSY NMR. Science 328: 98-102.
37. Singh SK, Guo F, Maurizi MR. (1999). ClpA and ClpP remain associated during multiple rounds of ATP-dependent protein degradation by ClpAP protease. Biochemistry (Mosc) 38: 14906-15.
38. Sprangers R, Gribun A, Hwang PM, et al. (2005). Quantitative NMR spectroscopy of supramolecular complexes: dynamic side pores in ClpP are important for product release. Proc Natl Acad Sci USA 102: 16678-83.
39. Sprangers R, Kay LE. (2007). Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature 445: 618-22.
40. Szyk A, Maurizi MR. (2006). Crystal structure at 1.9A of E. coli ClpP with a peptide covalently bound at the active site. J Struct Biol 156: 165-74.
41. Tomko Jr RJ, Hochstrasser M. (2013). Molecular architecture and assembly of the eukaryotic proteasome. Annu Rev Biochem 82: 415-45.
42. UniProt C. (2014). Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res 42: D191-8.
43. Vedadi M, Lew J, Artz J, et al. (2007). Genome-scale protein expression and structural biology of Plasmodium falciparum and related Apicomplexan organisms. Mol Biochem Parasitol 151: 100-10.
44. Wang J, Hartling JA, Flanagan JM. (1997). The structure of ClpP at 2.3 A resolution suggests a model for ATP-dependent proteolysis. Cell 91: 447-56.
45. Wang J, Hartling JA, Flanagan JM. (1998). Crystal structure determination of Escherichia coli ClpP starting from an EM-derived mask. J Struct Biol 124: 151-63.
46. Ye F, Zhang J, Liu H, et al. (2013). Helix unfolding/refolding characterizes the functional dynamics of Staphylococcus aureus Clp protease. J Biol Chem 288: 17643-53.
47. Zeiler E, List A, Alte F, et al. (2013). Structural and functional insights into caseinolytic proteases reveal an unprecedented regulation principle of their catalytic triad. Proc Natl Acad Sci USA 110: 11302-7.
48. Zhang J, Ye F, Lan L, et al. (2011). Structural switching of Staphylococcus aureus Clp protease: a key to understanding protease dynamics. J Biol Chem 286: 37590-601.