The antibiotic ADEP reprogrammes CIP, switching it from a regulated to an uncontrolled protease

EMBO Molecular Medicine

Volumn 1, Issue 1, 2009, Pages 37-49

  Kirstein, Janine ^a,e   Hoffmann, Anja ^b   Lilie, Hauke ^c   Schmidt, Ronny ^b   Helga, Rubsamen Waigmann ^d   Heike, Brötz Oesterhelt ^d   Mogk, Axel ^b   Turgay, Kürşad ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^d AiCuris GmbH   (Germany)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

ADEP; Antibiotic; Clp proteins; ClpP; Hsp100; Proteolysis

Indexed keywords

ACYLDEPSIPEPTIDE DERIVATIVE; ADENOSINE TRIPHOSPHATASE; CASEINOLYTIC PROTEASE P; DEPSIPEPTIDE; HEAT SHOCK PROTEIN 100; PROTEINASE; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; ARTICLE; COMPLEX FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME REGULATION; GENE CONTROL; GENE SWITCHING; GENE TARGETING; INHIBITION KINETICS; MOLECULAR BIOLOGY; MOLECULAR RECOGNITION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

EID: 71749110235     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.200900002     Document Type: Article

References (46)

1. Bandow JE, Brotz H, Leichert LI, Labischinski H, Hecker M (2003) Proteomic approach to understanding antibiotic action. Antimicrob Agents Chemother 47: 948-955
2. 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
3. Blanco FJ,Angrand I,Serrano L(1999) Exploring the conformational properties of the sequence space between two proteins with different folds: an experimental study. J Mol Biol 285: 741-753
4. Brötz-Oesterhelt H, Beyer D, Kroll HP, Endermann R, Ladel C, Schroeder W, Hinzen B, Raddatz S, Paulsen H, Henninger K, BandowJE, Sahl HG, Labischinski H (2005) Dysregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat Med 11: 1082-1087
5. Bukau B, Weissman J, Horwich AL (2006) Molecular chaperones and protein quality control. Cell 125: 443-451
6. Davis BD, Chen LL,Tai PC (1986) Misread protein creates membrane channels: an essential step in the bactericidal action of aminoglycosides. Proc Natl Acad Sci USA 83: 6164-6168
7. Deuerling E, Patzelt H, Vorderwulbecke S, Rauch T, Kramer G, Schaffitzel E, Mogk A, Schulze-Specking A, Langen H, Bukau B (2003) Trigger factor and DnaK possess overlapping substrate pools and binding specificities. Mol Microbiol 47: 1317-1328
8. Deuerling E, Schulze-Specking A, Tomoyasu T, Mogk A, Bukau B (1999) Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400: 693-696
9. Dougan D, Mogk A, Zeth K, Turgay K, Bukau B (2002a) AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett 529: 6-10
10. Dougan DA, Reid BG, Horwich AL, Bukau B (2002b) ClpS, a substrate modulator of the ClpAP machine. Mol Cell 9: 673-683
11. Erbse A, Schmidt R, Bornemann T, Schneider-Mergener J, Mogk A, Zahn R, Dougan DA, Bukau B (2006) ClpS is an essential component of the N-end rule pathway in Escherichia coli. Nature 439: 753-756
12. Frees D, Savijoki K, Varmanen P, Ingmer H (2007) Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC, Gram-positive bacteria. Mol Microbiol 63: 1285-1295
13. Gerth U, Küger E, Derré I, MsadekT, Hecker M (1998) Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance. Mol Microbiol 28: 787-802
14. Gottesman S (2003) Proteolysis in bacterial regulatory circuits. Annu RevCell Dev Biol 19: 565-587
15. Gribun A, Kimber MS, Ching R, Sprangers R, Fiebig KM, Houry WA (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: 16185-16196
16. Hardy CD, Cozzarelli NR (2005) A. genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol Microbiol 57: 1636-1652
17. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858
18. Hinzen B, Raddatz S, Paulsen H, Lampe T, Schumacher A, Habich D, Hellwig V, Benet-Buchholz J, Endermann R, Labischinski H, Brotz-Oesterhelt H (2006) Medicinal chemistry optimization of acyldepsipeptides of the enopeptin class antibiotics. ChemMedChem 1: 689-693
19. Hoffmann A, Merz F, Rutkowska A, Zachmann-Brand B, Deuerling E, Bukau B (2006) Trigger factor forms a protective shield for nascent polypeptides at the ribosome. J Biol Chem 281: 6539-6545
20. Horwich AL, Weber-Ban EU, Finley D (1999) Chaperone rings in protein folding and degradation. Proc Natl Acad Sci USA 96: 11033-11040
21. Jenal U, Hengge-Aronis R (2003) Regulation by proteolysis in bacterial cells. Curr Opin Microbiol 6: 163-172
22. Joshi SA, Hersch GL, Baker TA, Sauer RT (2004) Communication between ClpX and ClpP during substrate processing and degradation. Nat Struct Mol Biol 11: 404-411
23. 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
24. Kirstein J, Schlothauer T, Dougan DA, Lilie H, Tischendorf G, Mogk A, Bukau B, Turgay K (2006) Adaptor protein controlled oligomerization activates the AAA+ protein ClpC. EMBO J 25: 1481-1491
25. Kirstein J, Strahl H, Moliere N, Hamoen LW, Turgay K (2008) Localization of general and regulatory proteolysis in Bacillus subtilis cells. Mol Microbiol 70(3): 682-694
26. Kock H, Gerth U, Hecker M (2004) Mur AA, catalysing the first committed step in peptidoglycan biosynthesis, is a target of Clp-dependent proteolysis in Bacillus subtilis. Mol Microbiol 51: 1087-1102
27. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797-810
28. Kohanski MA, Dwyer DJ, Wierzbowski J, Cottarel G, Collins JJ (2008) Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 135: 679-690
29. Levy SB, Marshall B (2004) Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10: S122-129
30. Lewis PJ, Marston AL (1999) GFP vectors for controlled expression and dual labelling of protein fusions in Bacillus subtilis. Gene 227: 101-109
31. Lupas A, Flanagan JM, Tamura T, Baumeister W (1997) Self- compartmentalizing proteases. Trends Biochem Sci 22: 399-404
32. Magnet S, Blanchard JS (2005) Molecular insights into aminoglycoside action and resistance. Chem Rev 105: 477-498
33. 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
34. Maurizi MR, Clark WP, Katayama Y, Rudikoff S, Pumphrey J, Bowers B, Gottesman S (1990) Sequence and structure of ClpP, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J Biol Chem 265: 12536-12545
35. Msadek T, Dartois V, Kunst F, Herbaud ML, Denizot F, Rapoport G (1998) ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol Microbiol 27: 899-914
36. Müller M, Blobel G (1986) In vitro analysis of the bacterial protein export. Curr Top Microbiol Immunol 125: 33-41
37. Nakano MM, Hajarizadeh F, Zhu Y, Zuber P (2001) Loss-of-function mutations in yjbD result in ClpX-and ClpP-independent competence development of Bacillus subtilis. Mol Microbiol 42: 383-394
38. Rutkowska A, Mayer MP, Hoffmann A, Merz F, Zachmann-Brand B, Schaffitzel C, Ban N, Deuerling E, Bukau B (2008) Dynamics of trigger factor interaction with translating ribosomes. J Biol Chem 283: 4124-4132
39. Sauer RT, Bolon DN, Burton BM, Burton RE, FlynnJM, Grant RA, Hersch GL, Joshi SA, Kenniston JA, Levchenko I, Neher SB, Oakes ES, Siddiqui SM, Wah DA, Baker TA (2004) Sculpting the proteome with AAA(+). proteases and disassembly machines. Cell 119: 9-18
40. Schlothauer T, Mogk A, Dougan DA, Bukau B,Turgay K (2003) MecA, an adaptor protein necessary for ClpC chaperone activity. Proc Natl Acad Sci USA 100: 2306
41. Singh SK, Guo F, Maurizi MR (1999) ClpA and ClpP remain associated during multiple rounds of ATP-dependent protein degradation by ClpAP protease. Biochemistry 38: 14906-14915
42. Turgay K, Hamoen LW, Venema G, Dubnau D (1997) Biochemical characterization of a molecular switch involving the heat shock protein ClpC, which controls the activity of ComK, the competence transcription factor of Bacillus subtilis. Genes Dev 11: 119-128
43. 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
44. Wickner S, Maurizi MR, Gottesman S (1999) Posttranslational quality control: folding, refolding, and degrading proteins. Science 286: 1888-1893
45. Winter J, Ilbert M, Graf PC, Ozcelik D, Jakob U (2008) Bleach activates a redox-regulated chaperone by oxidative protein unfolding. Cell 135: 691-701
46. Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5: 175-186