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Proteome analysis of Streptomyces coelicolor mutants affected in the proteasome system reveals changes in stress-responsive proteins

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Abstract

Prokaryotic 20S proteasomes are confined to archaebacteria and actinomycetes. Bacterial targets of this compartmentalized multi-subunit protease have not yet been identified and its physiological function in prokaryotes remains unknown. In this study, intracellular and extracellular proteomes of Streptomyces coelicolor A3(2) mutants affected in the structural genes of the 20S proteasome, in the gene encoding the presumed proteasome-accessory AAA ATPase ARC, or in two putative proteasome-associated actinomycete-specific genes (sco1646, sco1647) were analysed, revealing modified patterns of stress-responsive proteins. In addition, the extracellular protease profile of the sco1647 mutant was significantly altered. The most prominent change, common to the four mutants, was a strongly increased level of the non-heme chloroperoxidase SCO0465, coinciding with an increased resistance to cumene hydroperoxide.

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Abbreviations

DTT:

Dithiothreitol

HPPD:

4-Hydroxyphenylpyruvate dioxygenase

MALDI TOF MS:

Matrix-assisted laser desorption/ionization time of flight mass spectrometry

NO:

Nitric oxide

PEP:

Phosphoenolpyruvate

SAM:

S-adenosylmethionine

TCA:

Tricarboxylic acid

TSB:

Tryptic soy broth

References

  • Aitken SM, Kirsch JF (2005) The enzymology of cystathionine biosynthesis: strategies for the control of substrate and reaction specificity. Arch Biochem Biophys 433:166–175

    Article  PubMed  CAS  Google Scholar 

  • Anantharaman V, Aravind L (2002) The PRC-barrel: a widespread, conserved domain shared by photosynthetic reaction center subunits and proteins of RNA metabolism. Genome Biol 3(11)

  • Artymiuk PJ, Green J (2006) The double life of aconitase. Structure 14:2–4

    Article  PubMed  CAS  Google Scholar 

  • Bantleon R, Altenbuchner J, van Pée K-H (1994) Chloroperoxidase from Streptomyces lividans: isolation and characterization of the enzyme and the corresponding gene. J Bacteriol 176:2339–2347

    PubMed  CAS  Google Scholar 

  • Baumeister W, Walz J, Zühl F, Seemüller E (1998) The proteasome: paradigm of a self-compartmentalizing protease. Cell 92:367–380

    Article  PubMed  CAS  Google Scholar 

  • Bertram R, Schlicht M, Mahr K, Nothaft H, Saier MH Jr, Titgemeyer F (2004) In silico and transcriptional analysis of carbohydrate uptake systems of Streptomyces coelicolor A3(2). J Bacteriol 186:1362–1373

    Article  PubMed  CAS  Google Scholar 

  • Boes N, Schreiber K, Hartig E, Jaensch L, Schobert M (2006) The Pseudomonas aeruginosa universal stress protein PA4352 is essential for surviving anaerobic energy stress. J Bacteriol 188:6529–6538

    Article  PubMed  CAS  Google Scholar 

  • Bordo D, Bork P (2002) The rhodanese/Cdc25 phosphatase superfamily. Sequence-structure-function relations. EMBO Rep 3:741–746

    Article  PubMed  CAS  Google Scholar 

  • Butler MJ, Davey CC, Krygsman P, Walczyk E, Malek LT (1992) Cloning of genetic loci involved in endoprotease activity in Streptomyces lividans 66: a novel neutral protease gene with an adjacent divergent putative regulatory gene. Can J Microbiol 38:912–920

    Article  PubMed  CAS  Google Scholar 

  • Butler SM, Festa RA, Pearce MJ, Darwin KH (2006) Self-compartmentalized bacterial proteases and pathogenesis. Mol Microbiol 60:553–562

    Article  PubMed  CAS  Google Scholar 

  • Cho YH, Kim EJ, Chung HJ, Choi JH, Chater KF, Ahn BE, Shin JH, Roe JH (2003) The pqrAB operon is responsible for paraquat resistance in Streptomyces coelicolor. J Bacteriol 185:6756–6763

    Article  PubMed  CAS  Google Scholar 

  • Chung HJ, Kim EJ, Suh B, Choi JH, Roe JH (1999) Duplicate genes for Fe-containing superoxide dismutase in Streptomyces coelicolor A3(2). Gene 231:87–93

    Article  PubMed  CAS  Google Scholar 

  • Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF (2003) The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302:1963–1966

    Article  PubMed  CAS  Google Scholar 

  • Darwin KH, Lin G, Chen Z, Li H, Nathan CF (2005) Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue. Mol Microbiol 55:561–571

    Article  PubMed  CAS  Google Scholar 

  • De Mot R, De Schrijver A, Schoofs G, Parret AHA (2003) The thiocarbamate-inducible Rhodococcus enzyme ThcF as a member of the family of α/β hydrolases with haloperoxidative side activity. FEMS Microbiol Lett 224:197–203

    Article  PubMed  CAS  Google Scholar 

  • De Mot R, Nagy I, Walz J, Baumeister W (1999) Proteasomes and other self-compartmentalizing proteases in prokaryotes. Trends Microbiol 7:88–92

    Article  PubMed  Google Scholar 

  • De Mot R, Vanderleyden J (1989) Application of two-dimensional protein analysis for strain fingerprinting and mutant analysis of Azospirillum brasilense. Can J Microbiol 35:960–967

    Article  Google Scholar 

  • Denis F, Brzezinski R (1992) A versatile shuttle cosmid vector for use in Escherichia coli and actinomycetes. Gene 111:115–118

    Article  PubMed  CAS  Google Scholar 

  • Denoya CD, Skinner DD, Morgenstern MR (1994) A Streptomyces avermitilis gene encoding a 4-hydroxyphenylpyruvic acid dioxygenase-like protein that directs the production of homogentisic acid and an ochronotic pigment in Escherichia coli. J Bacteriol 176:5312–5319

    PubMed  CAS  Google Scholar 

  • Dupuy J, Volbeda A, Carpentier P, Darnault C, Moulis JM, Fontecilla-Camps JC (2006) Crystal structure of human iron regulatory protein 1 as cytosolic aconitase. Structure 14:129–139

    Article  PubMed  CAS  Google Scholar 

  • Ehling-Schulz M, Schulz S, Wait R, Gorg A, Scherer S (2002) The UV-B stimulon of the terrestrial cyanobacterium Nostoc commune comprises early shock proteins and late acclimation proteins. Mol Microbiol 46:827–843

    Article  PubMed  CAS  Google Scholar 

  • Ehrensberger AH, Wilson DK (2004) Structural and catalytic diversity in the two family 11 aldo-keto reductases. J Mol Biol 337:661–673

    Article  PubMed  CAS  Google Scholar 

  • Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R

    Article  PubMed  CAS  Google Scholar 

  • Festa RA, Pearce MJ, Darwin KH (2007) Characterization of the proteasome accessory factor (paf) operon in Mycobacterium tuberculosis. J Bacteriol 189:3044–3050

    Article  PubMed  CAS  Google Scholar 

  • Green J, Paget MS (2004) Bacterial redox sensors. Nat Rev Microbiol 2:954–966

    Article  PubMed  CAS  Google Scholar 

  • Hahn JS, Oh SY, Roe JH (2002) Role of OxyR as a peroxide-sensing positive regulator in Streptomyces coelicolor A3(2). J Bacteriol 184:5214–5222

    Article  PubMed  CAS  Google Scholar 

  • Hammad Y, Maréchal J, Cournoyer B, Normand P, Domenach A-M (2001) Modification of the protein expression pattern induced in the nitrogen-fixing actinomycete Frankia sp. strain ACN14a-tsr by root exudates of its symbiotic host Alnus glutinosa and cloning of the sodF gene. Can J Microbiol 47:541–547

    Article  PubMed  CAS  Google Scholar 

  • Hecker M, W. Schumann W, Voelker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19:417–428

    Article  PubMed  CAS  Google Scholar 

  • Hesketh AR, Chandra G, Shaw AD, Rowland JJ, Kell DB, Bibb MJ, Chater KF (2002) Primary and secondary metabolism, and post-translational protein modifications, as portrayed by proteomic analysis of Streptomyces coelicolor. Mol Microbiol 46:917–932

    Article  PubMed  CAS  Google Scholar 

  • Hofmann B, Tolzer S, Pelletier I, Altenbuchner J, van Pée K-H, Hecht HJ (1998) Structural investigation of the cofactor-free chloroperoxidases. J Mol Biol 279:889–900

    Article  PubMed  CAS  Google Scholar 

  • Hong B, Wang L, Lammertyn E, Geukens N, Van Mellaert L, Li Y, Anné J (2005) Inactivation of the 20S proteasome in Streptomyces lividans and its influence on the production of heterologous proteins. Microbiology 151:3137–3145

    Article  PubMed  CAS  Google Scholar 

  • Hu G, Lin G, Wang M, Dick L, Xu RM, Nathan C, Li H (2006) Structure of the Mycobacterium tuberculosis proteasome and mechanism of inhibition by a peptidyl boronate. Mol Microbiol 59:1417–1428

    Article  PubMed  CAS  Google Scholar 

  • Johnson-Winters K, Purpero VM, Kavana M, Moran GR (2005) Accumulation of multiple intermediates in the catalytic cycle of (4-hydroxyphenyl)pyruvate dioxygenase from Streptomyces avermitilis. Biochemistry 44:7189–7199

    Article  PubMed  CAS  Google Scholar 

  • Kang SK, Chung TW, Lee JH, Kim CH (2006) Cloning and expression of superoxide dismutase from Mycobacterium bovis BCG. Protein Exp Purif 47:52–59

    Article  CAS  Google Scholar 

  • Kato JY, Hirano S, Ohnishi Y, Horinouchi S (2005) The Streptomyces subtilisin inhibitor (SSI) gene in Streptomyces coelicolor A3(2). Biosci Biotechnol Biochem 69:1624–1629

    Article  PubMed  CAS  Google Scholar 

  • Kim DW, Chater K, Lee KJ, Hesketh A (2005) Changes in the extracellular proteome caused by the absence of the bldA gene product, a developmentally significant tRNA, reveal a new target for the pleiotropic regulator AdpA in Streptomyces coelicolor. J Bacteriol 187:2957–2966

    Article  PubMed  CAS  Google Scholar 

  • Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. The John Innes Foundation, Norwich

    Google Scholar 

  • Knipfer N, Shrader TE (1997) Inactivation of the 20S proteasome in Mycobacterium smegmatis. Mol Microbiol 25:375–383

    Article  PubMed  CAS  Google Scholar 

  • Kvint K, Nachin L, Diez A, Nystrom T (2003) The bacterial universal stress protein: function and regulation. Curr Opin Microbiol 6:140–145

    Article  PubMed  CAS  Google Scholar 

  • Kwon YD, Nagy I, Adams PD, Baumeister W, Jap BK (2004) Crystal structures of the Rhodococcus proteasome with and without its pro-peptides: implications for the role of the pro-peptide in proteasome assembly. J Mol Biol 335:233–245

    Article  PubMed  CAS  Google Scholar 

  • Lamichhane G, Raghunand TR, Morrison NE, Woolwine SC, Tyagi S, Kandavelou K, Bishai WR (2006) Deletion of a Mycobacterium tuberculosis proteasomal ATPase homologue gene produces a slow-growing strain that persists in host tissues. J Infect Dis 194:1233–1240

    Article  PubMed  CAS  Google Scholar 

  • Langlois P, Bourassa S, Poirier GG, Beaulieu C (2003) Identification of Streptomyces coelicolor proteins that are differentially expressed in the presence of plant material. Appl Environ Microbiol 69:1884–1889

    Article  PubMed  CAS  Google Scholar 

  • Lee EJ, Karoonuthaisiri N, Kim HS, Park JH, Cha CJ, Kao CM, Roe J-H (2005) A master regulator σB governs osmotic and oxidative response as well as differentiation via a network of sigma factors in Streptomyces coelicolor. Mol Microbiol 57:1252–1264

    Article  PubMed  CAS  Google Scholar 

  • Lichenstein HS, Busse LA, Smith GA, Narhi LO, McGinley MO, Rohde MF, Katzowitz JL, Zukowski MM (1992) Cloning and characterization of a gene encoding extracellular metalloprotease from Streptomyces lividans. Gene 111:125–130

    Article  PubMed  CAS  Google Scholar 

  • Lin G, Hu G, Tsu C, Kunes YZ, Li H, Dick L, Parsons T, Li P, Chen Z, Zwickl P, Weich N, Nathan C (2006) Mycobacterium tuberculosis prcBA genes encode a gated proteasome with broad oligopeptide specificity. Mol Microbiol 59:1405–1416

    Article  PubMed  CAS  Google Scholar 

  • Maupin-Furlow JA, Humbard MA, Kirkland PA, Li W, Reuter CJ, Wright AJ (2005) Archaeal proteasomes and other regulatory proteases. Curr Opin Microbiol 8:720–728

    PubMed  CAS  Google Scholar 

  • McMillan DJ, Davies MR, Good MF, Sriprakash KS (2004) Immune response to superoxide dismutase in group A streptococcal infection. FEMS Immunol Med Microbiol 40:249–256

    Article  PubMed  CAS  Google Scholar 

  • Medalia N, Sharon M, Martinez-Arias R, Mihalache O, Robinson CV, Medalia O, Zwickl P (2006) Functional and structural characterization of the Methanosarcina mazei proteasome and PAN complexes. J Struct Biol 156:84–92

    PubMed  CAS  Google Scholar 

  • Muschko K, Kienzlen G, Fiedler HP, Wohlleben W, Schwartz D (2002) Tricarboxylic acid cycle aconitase activity during the life cycle of Streptomyces viridochromogenes Tu494. Arch Microbiol 178:499–505

    Article  PubMed  CAS  Google Scholar 

  • Nagy I, Banerjee T, Tamura T, Schoofs G, Gils A, Proost P, Tamura N, Baumeister W, De Mot R (2003) Characterization of a novel intracellular endopeptidase of the α/β hydrolase family from Streptomyces coelicolor A3(2). J Bacteriol 185:496–503

    Article  PubMed  CAS  Google Scholar 

  • Nagy I, Tamura T, Vanderleyden J, Baumeister W (1998) The 20S proteasome of Streptomyces coelicolor. J Bacteriol 180:5448–5453

    PubMed  CAS  Google Scholar 

  • Nothaft H, Parche S, Kamionka A, Titgemeyer F (2003) In vivo analysis of HPr reveals a fructose-specific phosphotransferase system that confers high-affinity uptake in Streptomyces coelicolor. J Bacteriol 185:929–937

    Article  PubMed  CAS  Google Scholar 

  • Novotna J, Vohradsky J, Berndt P, Gramajo H, Langen H, Li XM, Minas W, Orsaria L, Roeder D, Thompson CJ (2003) Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol Microbiol 48:1289–1303

    Article  PubMed  CAS  Google Scholar 

  • Oh SH, Chater KF (1997) Denaturation of circular or linear DNA facilitates targeted integrative transformation of Streptomyces coelicolor A3(2): possible relevance to other organisms. J Bacteriol 179:122–127

    PubMed  CAS  Google Scholar 

  • O’Toole R, Smeulders MJ, Blokpoel MC, Kay EJ, Lougheed K, Williams HD (2003) A two-component regulator of universal stress protein expression and adaptation to oxygen starvation in Mycobacterium smegmatis. J Bacteriol 185:1543–1554

    Article  PubMed  CAS  Google Scholar 

  • Paget MS, Kang JG, Roe JH, Buttner MJ (1998) σR, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J 17:5776–5782

    Article  PubMed  CAS  Google Scholar 

  • Park W, Pena-Llopis S, Lee Y, Demple B (2006) Regulation of superoxide stress in Pseudomonas putida KT2440 is different from the SoxR paradigm in Escherichia coli. Biochem Biophys Res Commun 341:51–56

    Article  PubMed  CAS  Google Scholar 

  • Parret AHA, Schoofs G, Proost P, De Mot R (2003) Plant lectin-like bacteriocin from a rhizosphere-colonizing Pseudomonas isolate. J Bacteriol 185:897–908

    Article  PubMed  CAS  Google Scholar 

  • Pearce MJ, Arora P, Festa RA, Butler-Wu SM, Gokhale RS, Darwin KH (2006) Identification of substrates of the Mycobacterium tuberculosis proteasome. EMBO J 25:5423–5432

    Article  PubMed  CAS  Google Scholar 

  • Pessolani MC, Brennan PJ (1996) Molecular definition and identification of new proteins of Mycobacterium leprae. Infect Immun 64:5425–5427

    PubMed  CAS  Google Scholar 

  • Petersohn A, Antelmann H, Gerth U, Hecker M (1999) Identification and transcriptional analysis of new members of the σB regulon in Bacillus subtilis. Microbiology 145:869–880

    Article  PubMed  CAS  Google Scholar 

  • Poole LB (2005) Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch Biochem Biophys 433:240–254

    Article  PubMed  CAS  Google Scholar 

  • Pouch M-N, Cournoyer B, Baumeister W (2000) Characterization of the 20S proteasome from the actinomycete Frankia. Mol Microbiol 35:368–377

    Article  PubMed  CAS  Google Scholar 

  • Prabhu J, Schauwecker F, Grammel N, Keller U, Bernhard M (2004) Functional expression of the ectoine hydroxylase gene (thpD) from Streptomyces chrysomallus in Halomonas elongata. Appl Environ Microbiol 70:3130–3132

    Article  PubMed  CAS  Google Scholar 

  • Rhee KY, Erdjument-Bromage H, Tempst P, Nathan CF (2005) S-nitroso proteome of Mycobacterium tuberculosis: enzymes of intermediary metabolism and antioxidant defense. Proc Natl Acad Sci USA 102:467–472

    Article  PubMed  CAS  Google Scholar 

  • Rosenkrands I, Slayden RA, Crawford J, Aagaard C, Barry CE III, Andersen P (2002) Hypoxic response of Mycobacterium tuberculosis studied by metabolic labeling and proteome analysis of cellular and extracellular proteins. J Bacteriol 184:3485–3491

    Article  PubMed  CAS  Google Scholar 

  • Schilling O, Overall CM (2007) Proteomic discovery of protease substrates. Curr Opin Chem Biol 11:36–45

    Article  PubMed  CAS  Google Scholar 

  • Sevo M, Buratti E, Venturi V (2004) Ribosomal protein S1 specifically binds to the 5′ untranslated region of the Pseudomonas aeruginosa stationary-phase sigma factor rpoS mRNA in the logarithmic phase of growth. J Bacteriol 186:4903–4909

    Article  PubMed  CAS  Google Scholar 

  • Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, Schoolnik GK (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding α-crystallin. Proc Natl Acad Sci USA 98:7534–7539

    Article  PubMed  CAS  Google Scholar 

  • Smeulders MJ, Keer J, Gray KM, Williams HD (2004) S-Nitrosoglutathione cytotoxicity to Mycobacterium smegmatis and its use to isolate stationary phase survival mutants. FEMS Microbiol Lett 239:221–228

    Article  PubMed  CAS  Google Scholar 

  • Smith DM, Kafri G, Cheng Y, Ng D, Walz T, Goldberg AL (2005) ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins. Mol Cell 20:687–698

    Article  PubMed  CAS  Google Scholar 

  • Smith JL (2004) The physiological role of ferritin-like compounds in bacteria. Crit Rev Microbiol 30:173–185

    Article  PubMed  CAS  Google Scholar 

  • Springer B, Master S, Sander P, Zahrt T, McFalone M, Song J, Papavinasasundaram KG, Colston MJ, Boettger E, Deretic V (2001) Silencing of oxidative stress response in Mycobacterium tuberculosis: expression patterns of ahpC in virulent and avirulent strains and effect of ahpC inactivation. Infect Immun 69:5967–5973

    Article  PubMed  CAS  Google Scholar 

  • Steinert M, Flugel M, Schuppler M, Helbig JH, Supriyono A, Proksch P, Luck PC (2001) The Lly protein is essential for p-hydroxyphenylpyruvate dioxygenase activity in Legionella pneumophila. FEMS Microbiol Lett 203:41–47

    Article  PubMed  CAS  Google Scholar 

  • Tamura T, Nagy I, Lupas A, Lottspeich F, Cejka Z, Schoofs G, Tanaka K, De Mot R, Baumeister W (1995) The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr Biol 5:766–774

    Article  PubMed  CAS  Google Scholar 

  • Tebbe A, Klein C, Bisle B, Siedler F, Scheffer B, Garcia-Rizo C, Wolfertz J, Hickmann V, Pfeiffer F, Oesterhelt D (2005) Analysis of the cytosolic proteome of Halobacterium salinarum and its implication for genome annotation. Proteomics 5:168–179

    Article  PubMed  CAS  Google Scholar 

  • Teixeira-Gomes AP, Cloeckaert A, Zygmunt MS (2000) Characterization of heat, oxidative, and acid stress responses in Brucella melitensis. Infect Immun 68:2954–2961

    Article  PubMed  CAS  Google Scholar 

  • Thompson CJ (2001) Pleiotropic functions of a Streptomyces pristinaespiralis autoregulator receptor in development, antibiotic biosynthesis, and expression of a superoxide dismutase. J Biol Chem 276:44297–44306

    Article  PubMed  Google Scholar 

  • van Keulen G, Alderson J, White J, Sawers RG (2005) Nitrate respiration in the actinomycete Streptomyces coelicolor. Biochem Soc Trans 33:210–212

    Article  PubMed  Google Scholar 

  • van Pée KH, Unversucht S (2003) Biological dehalogenation and halogenation reactions. Chemosphere 52:299–312

    Article  PubMed  CAS  Google Scholar 

  • Varshney U, Ramesh V, Madabushi A, Gaur R, Subramanya HS, RajBhandary UL (2004) Mycobacterium tuberculosis Rv2118c codes for a single-component homotetrameric m1A58 tRNA methyltransferase. Nucleic Acids Res 32:1018–1027

    Article  PubMed  CAS  Google Scholar 

  • Viollier PH, Nguyen KT, Minas W, Folcher M, Dale GE, Thompson CJ (2001) Roles of aconitase in growth, metabolism, and morphological differentiation of Streptomyces coelicolor. J Bacteriol 183:3193–3203

    Article  PubMed  CAS  Google Scholar 

  • von der Haar B, Schrempf H (1995) Purification and characterization of a novel extracellular Streptomyces lividans 66 enzyme inactivating fusidic acid. J Bacteriol 177:152–155

    PubMed  Google Scholar 

  • von der Haar B, Walter S, Schwapenheuer S, Schrempf H (1997) A novel fusidic acid resistance gene from Streptomyces lividans 66 encodes a highly specific esterase. Microbiology 143:867–874

    PubMed  Google Scholar 

  • Wallace MA, Bailey S, Fukuto JM, Valentine JS, Gralla EB (2005) Induction of phenotypes resembling CuZn-superoxide dismutase deletion in wild-type yeast cells: an in vivo assay for the role of superoxide in the toxicity of redox-cycling compounds. Chem Res Toxicol 18:1279–1286

    Article  PubMed  CAS  Google Scholar 

  • Watt SA, Tellstrom V, Patschkowski T, Niehaus K (2006) Identification of the bacterial superoxide dismutase (SodM) as plant-inducible elicitor of an oxidative burst reaction in tobacco cell suspension cultures. J Biotechnol 126:78–86

    Article  PubMed  CAS  Google Scholar 

  • Witt S, Kwon YD, Sharon M, Felderer K, Beuttler M, Robinson CV, Baumeister W, Jap BK (2006) Proteasome assembly triggers a switch required for active-site maturation. Structure 14:1179–1188

    Article  PubMed  CAS  Google Scholar 

  • Wolf S, Nagy I, Lupas A, Pfeifer G, Cejka Z, Muller SA, Engel A, De Mot R, Baumeister W (1998) Characterization of ARC, a divergent member of the AAA ATPase family from Rhodococcus erythropolis. J Mol Biol 277:13–25

    Article  PubMed  CAS  Google Scholar 

  • Yamada SI, Niwa JI, Ishigaki S, Takahashi M, Ito T, Sone J, Doyu M, Sobue G (2006) Archaeal proteasomes effectively degrade aggregation-prone proteins and reduce cellular toxicities in mammalian cells. J Biol Chem 281:23842–23851

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Stoffels K, Wurzbacher S, Schoofs G, Pfeifer G, Banerjee T, Parret AHA, Baumeister W, De Mot R, Zwickl P (2004) The N-terminal coiled coil of the Rhodococcus erythropolis ARC AAA ATPase is neither necessary for oligomerization nor nucleotide hydrolysis. J Struct Biol 146:155–165

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

This work was supported by a grant (Onderzoeksproject G.0192.02N) from the Fund for Scientific Research (FWO-Vlaanderen) to R.D.M. The authors thank Paul Proost (Rega Institute, K.U. Leuven) for N-terminal sequencing of several proteins, and Sigrid Bauer, Beate Scheffer (Mass Spectrometry Service, Max-Planck-Institute of Biochemistry, Martinsried) and Na Sun (Department of Molecular Structural Biology, Max-Planck-Institute of Biochemistry, Martinsried) for the MALDI TOF MS identification of protein samples.

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Authors and Affiliations

  1. Centre of Microbial and Plant Genetics, Department of Microbial and Molecular Systems, Faculty of Bioscience Engineering, Katholieke Universiteit Leuven, Kasteelpark Arenberg 20, 3001, Leuven, Belgium

    René De Mot & Geert Schoofs

  2. Department of Molecular Structural Biology, Max-Planck-Institute of Biochemistry, Am Klopferspitz 18, 82152, Martinsried, Germany

    István Nagy

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  1. René De Mot
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  2. Geert Schoofs
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  3. István Nagy
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Correspondence to René De Mot.

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Communicated by Jean-Luc Pernodet.

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203_2007_243_MOESM1_ESM.ppt

Images of analytical (black frame) and corresponding preparative ‘picking’ 2D-gels (red frame) used to identify and isolate differential spots in the cellular and extracellular fractions for the respective S. coelicolor A3(2) mutants (ARC, SCO1647, SCO1646, 20S proteasome (PRC)). The spots listed in Tables 1–4 are marked. The positions of landmark spots (labelled with ‘m’) are indicated (PPT 834 kb)

203_2007_243_MOESM2_ESM.xls

Data supporting identification of S. coelicolor A3(2) gene products with altered abundance in the intracellular and extracellular proteome of mutants lacking ARC, SCO1647, SCO1646, or the 20S proteasome (PRC), as listed in Tables 1–4. For each ORF, data on matched peptides (amino acid sequence, position in the polypeptide, experimental and calculated Mr values) and the corresponding MOWSE score are shown. Dots are used to indicate the flanking amino acids for the MS-identified peptides (sites of cleavage by trypsin). Asterisk-labeled sequences were determined by N-terminal sequence analysis. Spot coordinates estimated from 2D gels are listed together with the theoretical pI and Mr values. For extracellular proteins with a probable signal peptide predicted by SignalP (http://www.cbs.dtu.dk/services/SignalP/), the pI and Mr values calculated for the putative processed form are shown in square brackets. These values were obtained using the ExPASy Compute pI/Mw tool (http://www.expasy.org/tools/pi_tool.html) (XLS 176 kb)

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De Mot, R., Schoofs, G. & Nagy, I. Proteome analysis of Streptomyces coelicolor mutants affected in the proteasome system reveals changes in stress-responsive proteins. Arch Microbiol 188, 257–271 (2007). https://doi.org/10.1007/s00203-007-0243-8

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