The active ClpP protease from M. tuberculosis is a complex composed of a heptameric ClpP1 and a ClpP2 ring

EMBO Journal

Volumn 31, Issue 6, 2012, Pages 1529-1541

  Akopian, Tatos ^a   Kandror, Olga ^a   Raju, Ravikiran M ^b   Unnikrishnan, Meera ^b   Rubin, Eric J ^b   Goldberg, Alfred L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

cleavage preferences; dipeptide activator; protease ClpP1P2

Indexed keywords

BACTERIAL PROTEIN; CASPASE; CHYMOTRYPSIN; PROTEIN CLPP 1; PROTEIN CLPP 2; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVATION; ENZYME ACTIVITY; MOLECULAR LIBRARY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN PURIFICATION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; BINDING SITES; CASPASES; CHYMOTRYPSIN; HYDROLYSIS; MYCOBACTERIUM TUBERCULOSIS; PEPTIDE HYDROLASES; PEPTIDES; PROTEIN CONFORMATION; SERINE ENDOPEPTIDASES;

MYCOBACTERIUM TUBERCULOSIS;

EID: 84858794930     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.5     Document Type: Article

References (65)

1. Akopian TN, Kisselev AF, Goldberg AL (1997) Processive degradation of proteins and other catalytic properties of the proteasome from Thermoplasma acidophilum. J Biol Chem 272: 1791-1798 (Pubitemid 27043269)
2. Andersson FI, Tryggvesson A, Sharon M, Diemand AV, Classen M, Best C, Schmidt R, Schelin J, Stanne TM, Bukau B, Robinson CV, Witt S, Mogk A, Clarke AK (2009) Structure and function of a novel type of ATP-dependent Clp protease. J Biol Chem 284: 13519-13532
3. Barik S, Sureka K, Mukherjee P, Basu J, 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
4. Baumeister W, Walz J, Zühl F, Seemü ller E (1998) The proteasome: paradigm of a self-compartmentalizing protease. Cell 92: 367-380 (Pubitemid 28093014)
5. Baykov AA, Evtushenko OA, Avaeva SM (1988) A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal Biochem 171: 266-270
6. Benaroudj N, Raynal B, Miot M, Ortiz-Lombardia M (2011) Assembly and proteolytic processing of mycobacterial ClpP1 and ClpP2. BMC Biochem 12: 61
7. Bewley MC, Graziano V, Griffin K, Flanagan JM (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)
8. Brotz-Oesterhelt H, Beyer D, Kroll HP, Endermann R, Ladel C, Schroeder W, Hinzen B, Raddatz S, Paulsen H, Henninger K, Bandow JE, Sahl HG, Labischinski H (2005) Dysregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat Med 11: 1082-1087 (Pubitemid 41486830)
9. Butler SM, Festa RA, Pearce MJ, Darwin KH (2006) Self-compartmentalized bacterial proteases and pathogenesis. Mol Microbiol 60: 553-562
10. Flanagan JM, Wall JS, Capel MS, Schneider DK, Shanklin J (1995) Scanning transmission electron microscopy and small-angle scattering provide evidence that native Escherichia coli ClpP is a tetradecamer with an axial pore. Biochemistry 34: 10910-10917
11. Grimaud R, Kessel M, Beuron F, Steven AC, Maurizi MR (1998) Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP. J Biol Chem 273: 12476-12481 (Pubitemid 28240621)
12. Groll M, Bajorek M, Kohler A, Moroder L, Rubin DM, Huber R, Glickman MH, Finley D (2000) A gated channel into the proteasome core particle. Nat Struct Biol 7: 1062-1067
13. Hoskins JR, Pak M, Maurizi MR, Wickner S (1998) The role of the ClpA chaperone in proteolysis by ClpAP. Proc Natl Acad Sci USA 95: 12135-12140 (Pubitemid 28483731)
14. Huang H, Goldberg AL (1997) Proteolytic activity of the ATPdependent protease HslVU can be uncoupled from ATP hydrolysis. J Biol Chem 272: 21364-21372 (Pubitemid 27374005)
15. Hwang BJ, Park WJ, Chung CH, Goldberg AL (1987) Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La. Proc Natl Acad Sci USA 84: 5550-5554
16. Hwang BJ, Woo KM, Goldberg AL, Chung CH (1988) Protease Ti, a new ATP-dependent protease in Escherichia coli, contains protein-activated ATPase and proteolytic functions in distinct subunits. J Biol Chem 263: 8727-8734
17. Ingvarsson H, Mate MJ, Hogbom M, Portnoi D, Benaroudj N, Alzari PM, Ortiz-Lombardia M, 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)
18. Ishikawa T, Beuron F, Kessel M, Wickner S, Maurizi MR, Steven AC (2001) Translocation pathway of protein substrates in ClpAP protease. Proc Natl Acad Sci USA 98: 4328-4333 (Pubitemid 32294976)
19. Kang SG, Dimitrova MN, Ortega J, Ginsburg A, Maurizi MR (2005) Human mitochondrial ClpP is a stable heptamer that assembles into a tetradecamer in the presence of ClpX. J Biol Chem 280: 35424-35432 (Pubitemid 41532732)
20. Katayama-Fujimura Y, Gottesman S, Maurizi MR (1987) A multiplecomponent, ATP-dependent protease from Escherichia coli. J Biol Chem 262: 4477-4485 (Pubitemid 17102807)
21. Kim YI, Levchenko I, Fraczkowska K, Woodruff RV, Sauer RT, Baker TA (2001) Molecular determinants of complex formation between Clp/Hsp100 ATPases and the ClpP peptidase. Nat Struct Biol 8: 230-233 (Pubitemid 32180048)
22. Kirstein J, Hoffmann A, Lilie H, Schmidt R, Rubsamen-Waigmann H, Brotz-Oesterhelt H, Mogk A, Turgay K (2009) The antibiotic ADEP reprogrammes ClpP, switching it from a regulated to an uncontrolled protease. EMBO Mol Med 1: 37-49
23. Kisselev AF, Callard A, Goldberg AL (2006) Importance of the different proteolytic sites of the proteasome and the efficacy of inhibitors varies with the protein substrate. J Biol Chem 281: 8582-8590 (Pubitemid 43847961)
24. Kisselev AF, Garcia-Calvo M, Overkleeft HS, Peterson E, Pennington MW, Ploegh HL, Thornberry NA, Goldberg AL (2003) The QJ;caspase-like sites of proteasomes, their substrate specificity, new inhibitors and substrates, and allosteric interactions with the trypsin-like sites. J Biol Chem 278: 35869-35877 (Pubitemid 37139904)
25. Kress W, Maglica Z, Weber-Ban E (2009) Clp chaperone-proteases: structure and function. Res Microbiol 160: 618-628
26. Lee BG, Park EY, Lee KE, Jeon H, Sung KH, Paulsen H, Rubsamen-Schaeff H, Brotz-Oesterhelt H, Song HK (2010a) Structures of ClpP in complex with acyldepsipeptide antibiotics reveal its activation mechanism. Nat Struct Mol Biol 17: 471-478
27. Lee JW, Park E, Jeong MS, Jeon YJ, Eom SH, Seol JH, Chung CH (2009) HslVU ATP-dependent protease utilizes maximally six among twelve threonine active sites during proteolysis. J Biol Chem 284: 33475-33484
28. Lee ME, Baker TA, Sauer RT (2010b) Control of substrate gating and translocation into ClpP by channel residues and ClpX binding. J Mol Biol 399: 707-718
29. Leung E, Datti A, Cossette M, Goodreid J, McCaw SE, Mah M, Nakhamchik A, Ogata K, El Bakkouri M, Cheng YQ, Wodak SJ, Eger BT, Pai EF, Liu J, Gray-Owen S, Batey RA, Houry WA (2011) Activators of cylindrical proteases as antimicrobials: identification and development of small molecule activators of ClpP protease. Chem Biol 18: 1167-1178
30. Liu Y, Patricelli MP, Cravatt BF (1999) Activity-based protein profiling: the serine hydrolases. Proc Natl Acad Sci USA 96: 14694-14699 (Pubitemid 30019702)
31. Maurizi MR (1991) ATP-promoted interaction between Clp A and Clp P in activation of Clp protease from Escherichia coli. Biochem Soc Trans 19: 719-723
32. Maurizi MR, Clark WP, Katayama Y, Rudikoff S, Pumphrey J, Bowers B, Gottesman S (1990a) Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J Biol Chem 265: 12536-12545
33. Maurizi MR, Clark WP, Kim SH, Gottesman S (1990b) Clp P represents a unique family of serine proteases. J Biol Chem 265: 12546-12552
34. Maurizi MR, Singh SK, Thompson MW, Kessel M, Ginsburg A (1998) Molecular properties of ClpAP protease of Escherichia coli: ATP-dependent association of ClpA and clpP. Biochemistry 37: 7778-7786 (Pubitemid 28248637)
35. Maurizi MR, Thompson MW, Singh SK, Kim SH (1994) Endopeptidase Clp: ATP-dependent Clp protease from Escherichia coli. Methods Enzymol 244: 314-331
36. Ollinger J, O'Malley T, Kesicki EA, Odingo J, Parish T (2012) Validation of the essential ClpP protease in Mycobacterium tuberculosis as a novel drug target. J Bacteriol 194: 663-668
37. Ortega J, Singh SK, Ishikawa T, Maurizi MR, Steven AC (2000) Visualization of substrate binding and translocation by the ATPdependent protease, ClpXP. Mol Cell 6: 1515-1521 (Pubitemid 32045943)
38. Peltier JB, Ripoll DR, Friso G, Rudella A, Cai Y, Ytterberg J, Giacomelli L, Pillardy J, van Wijk KJ (2004) Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted three-dimensional structures, and functional implications. J Biol Chem 279: 4768-4781 (Pubitemid 38199072)
39. Peltier JB, Ytterberg J, Liberles DA, Roepstorff P, van Wijk KJ (2001) Identification of a 350-kDa ClpP protease complex with 10 different Clp isoforms in chloroplasts of Arabidopsis thaliana. J Biol Chem 276: 16318-16327
40. Porankiewicz J, Wang J, Clarke AK (1999) New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol Microbiol 32: 449-458 (Pubitemid 29233891)
41. Powers JC, Kam CM (1994) Isocoumarin inhibitors of serine peptidases. Methods Enzymol 244: 442-457
42. Rabl J, Smith DM, Yu Y, Chang SC, Goldberg AL, Cheng Y (2008) Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol Cell 30: 360-368 (Pubitemid 351615314)
43. Raju R, Unnikrishnan M, Rubin D, Krishnamoorthy V, Kandror O, Akopian T, Goldberg AL, Rubin EJ (2011) Mycobacterium tuberculosis encodes a heteromeric ClpP protease required for normal growth and virulence. PLoS Pathog (in press)
44. Reid BG, Fenton WA, Horwich AL, Weber-Ban EU (2001) ClpA mediates directional translocation of substrate proteins into the ClpP protease. Proc Natl Acad Sci USA 98: 3768-3772 (Pubitemid 32249846)
45. Sassetti CM, Boyd DH, Rubin EJ (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48: 77-84 (Pubitemid 36411469)
46. Schelin J, Lindmark F, Clarke AK (2002) The clpP multigene family for the ATP-dependent Clp protease in the cyanobacterium Synechococcus. Microbiology 148: 2255-2265 (Pubitemid 34785308)
47. Schmitt EK, Riwanto M, Sambandamurthy V, Roggo S, Miault C, Zwingelstein C, Krastel P, Noble C, Beer D, Rao SP, Au M, Niyomrattanakit P, Lim V, Zheng J, Jeffery D, Pethe K, Camacho LR (2011) The natural product cyclomarin kills Mycobacterium tuberculosis by targeting the ClpC1 subunit of the caseinolytic protease. Angew Chem Int Ed Engl 50: 5889-5891
48. Seol JH, Yoo SJ, Shin DH, Shim YK, Kang MS, Goldberg AL, Chung CH (1997) The heat-shock protein HslVU from Escherichia coli is a protein-activated ATPase as well as an ATP-dependent proteinase. Eur J Biochem 247: 1143-1150 (Pubitemid 27337071)
49. Sherrid AM, Rustad TR, Cangelosi GA, Sherman DR (2010) Characterization of a Clp protease gene regulator and the reaeration response in Mycobacterium tuberculosis. PLoS One 5: e11622
50. Shin DH, Lee CS, Chung CH, Suh SW (1996) Molecular symmetry of the ClpP component of the ATP-dependent Clp protease, an Escherichia coli homolog of 20 S proteasome. J Mol Biol 262: 71-76 (Pubitemid 26326963)
51. Sjogren LL, Stanne TM, Zheng B, Sutinen S, Clarke AK (2006) Structural and functional insights into the chloroplast ATPdependent Clp protease in Arabidopsis. Plant Cell 18: 2635-2649 (Pubitemid 44749894)
52. Smith DM, Chang SC, Park S, Finley D, Cheng Y, Goldberg AL (2007) Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol Cell 27: 731-744 (Pubitemid 47333222)
53. Smith N, Naude RJ, Oelofsen W, Lazure C, Patthy A (1992) The isolation and partial characterization of trypsinogen, pancreatic secretory trypsin inhibitor and multiple forms of chymotrypsinogen and trypsin from the pancreas of the ostrich (Struthio camelus). Int J Biochem 24: 877-885
54. Sousa MC, Kessler BM, Overkleeft HS, McKay DB (2002) Crystal structure of HslUV complexed with a vinyl sulfone inhibitor: corroboration of a proposed mechanism of allosteric activation of HslV by HslU. J Mol Biol 318: 779-785 (Pubitemid 34729368)
55. Stanne TM, Pojidaeva E, Andersson FI, Clarke AK (2007) Distinctive types of ATP-dependent Clp proteases in cyanobacteria. J Biol Chem 282: 14394-14402 (Pubitemid 47100425)
56. Striebel F, Kress W, Weber-Ban E (2009) Controlled destruction: AAA+ ATPases in protein degradation from bacteria to eukaryotes. Curr Opin Struct Biol 19: 209-217
57. 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: 165-174 (Pubitemid 44486061)
58. Thompson MW, Maurizi MR (1994) Activity and specificity of Escherichia coli ClpAP protease in cleaving model peptide substrates. J Biol Chem 269: 18201-18208 (Pubitemid 24206221)
59. Viala J, Mazodier P (2002) ClpP-dependent degradation of PopR allows tightly regulated expression of the clpP3 clpP4 operon in Streptomyces lividans. Mol Microbiol 44: 633-643 (Pubitemid 34526576)
60. Viala J, Rapoport G, Mazodier P (2000) The clpP multigenic family in Streptomyces lividans: conditional expression of the clpP3 clpP4 operon is controlled by PopR, a novel transcriptional activator. Mol Microbiol 38: 602-612
61. 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: 447-456 (Pubitemid 27508234)
62. Waxman L, Goldberg AL (1982) Protease La from Escherichia coli hydrolyzes ATP and proteins in a linked fashion. Proc Natl Acad Sci USA 79: 4883-4887 (Pubitemid 12004136)
63. Whitby FG, Masters EI, Kramer L, Knowlton JR, Yao Y, Wang CC, Hill CP (2000) Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 408: 115-120
64. Yoo SJ, Seol JH, Shin DH, Rohrwild M, Kang MS, Tanaka K, Goldberg AL, Chung CH (1996) Purification and characterization of the heat shock proteins HslV and HslU that form a new ATP-dependent protease in Escherichia coli. J Biol Chem 271: 14035-14040 (Pubitemid 26190295)
65. Yu AY, Houry WA (2007) ClpP: a distinctive family of cylindrical energy-dependent serine proteases. FEBS Lett 581: 3749-3757 (Pubitemid 47082517)