Research Article | Open Access
B. Franzetti, G. Schoehn, D. Garcia, R. W. H. Ruigrok, G. Zaccai, "Characterization of the proteasome from the extremely halophilic archaeon Haloarcula marismortui", Archaea, vol. 1, Article ID 601719, 9 pages, 2002. https://doi.org/10.1155/2002/601719
Characterization of the proteasome from the extremely halophilic archaeon Haloarcula marismortui
A 20S proteasome, comprising two subunits α and β, was purified from the extreme halophilic archaeon Haloarcula marismortui, which grows only in saturated salt conditions. The three-dimensional reconstruction of the H. marismortui proteasome (Hm proteasome), obtained from negatively stained electron micrographs, is virtually identical to the structure of a thermophilic proteasome filtered to the same resolution. The stability of the Hm proteasome was found to be less salt-dependent than that of other halophilic enzymes previously described. The proteolytic activity of the Hm proteasome was investigated using the malate dehydrogenase from H. marismortui (HmMalDH) as a model substrate. The HmMalDH denatures when the salt concentration is decreased below 2 M. Under these conditions, the proteasome efficiently cleaves HmMalDH during its denaturation process, but the fully denatured HmMalDH is poorly degraded. These in vitro experiments show that, at low salt concentrations, the 20S proteasome from halophilic archaea eliminates a misfolded protein.
- C. Allison and G.T. Macfarlane, “Regulation of protease production in Clostridium sporogenes,” Appl. Environ. Microbiol., vol. 56, pp. 3485–3490, 1990.
- F. Arsene, T. Tomoyasu, and B. Bukau, “The heat shock response of Escherichia coli,” Int. J. Food Microbiol., vol. 55, pp. 3–9, 2000.
- R.D. Barber and J.G. Ferry, “Archaeal proteasomes,” Methods Enzymol., vol. 330, pp. 413–424, 2001.
- M.W. Bauer, S.B. Halio, and R.M. Kelly, “Proteases and glycosyl hydrolases from hyperthermophilic microorganisms,” Adv. Protein Chem., vol. 48, pp. 271–310, 1996.
- I.I. Blumentals, A.S. Robinson, and R.M. Kelly, “Characterization of sodium dodecyl sulfate-resistant proteolytic activity in the hyperthermophilic archaebacterium Pyrococcus furiosus,” Appl. Environ. Microbiol., vol. 56, pp. 1992–1998, 1990.
- M. Bochtler, L. Ditzel, M. Groll, and R. Huber, “Crystal structure of heat shock locus V (HslV) from Escherichia coli,” Proc. Natl. Acad. Sci. USA, vol. 94, pp. 6070–6074, 1997.
- M. Bochtler, L. Ditzel, M. Groll, C. Hartmann, and R. Huber, “The proteasome,” Annu. Rev. Biophys. Biomol. Struct., vol. 28, pp. 295–317, 1999.
- T.D. Brock, K.M. Brock, R.T. Belly, and R.L. Weiss, “Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature,” Arch. Microbiol., vol. 84, pp. 54–68, 1972.
- B. Bukau, “Regulation of the Escherichia coli heat-shock response,” Mol. Microbiol., vol. 9, pp. 671–680, 1993.
- N. Burlini, P. Magnani, A. Villa, F. Macchi, P. Tortora, and A. Guerritore, “A heat-stable serine proteinase from the extreme thermophilic archaebacterium Sulfolobus solfataricus,” Biochim. Biophys. Acta, vol. 1122, pp. 283–292, 1992.
- L.S. Chang, P.M. Hicks, and R.M. Kelly, “Protease I from Pyrococcus furiosus,” Methods Enzymol., vol. 330, pp. 403–413, 2001.
- I.G. Choi, W.G. Bang, S.H. Kim, and Y.G. Yu, “Extremely thermostable serine-type protease from Aquifex pyrophilus. Molecular cloning, expression, and characterization.,” J. Biol. Chem., vol. 274, pp. 881–888, 1999.
- H. Connaris, D. Cowan, and R. Sharp, “Heterogeneity of proteinases from the hyperthermophilic archeobacterium Pyrococcus furiosus,” J. Gen. Microbiol., vol. 137, pp. 1193–1199, 1991.
- H. Dargatz, T. Diefenthal, V. Witte, G. Reipen, and D. von Wettstein, “The heterodimeric protease clostripain from Clostridium histolyticum is encoded by a single gene,” Mol. Gen. Genet., vol. 240, pp. 140–145, 1993.
- W.M. de Vos, W.G. Voorhorst, M. Dijkgraaf, L.D. Kluskens, J. van der Oost, and R.J. Siezen, “Purification, characterization, and molecular modeling of pyrolysin and other extracellular thermostable serine proteases from hyperthermophilic microorganisms,” Methods Enzymol., vol. 330, pp. 383–393, 2001.
- G. Deckert, P.V. Warren, T. Gaasterland et al., “The complete genome of the hyperthermophilic bacterium Aquifex aeolicus,” Nature, vol. 392, pp. 353–358, 1998.
- G.N. DeMartino and C.A. Slaughter, “The proteasome, a novel protease regulated by multiple mechanisms,” J. Biol. Chem., vol. 274, pp. 22123–22126, 1999.
- R. Dib, J.M. Chobert, M. Dalgalarrondo, G. Barbier, and T. Haertle, “Purification, molecular properties and specificity of a thermoactive and thermostable proteinase from Pyrococcus abyssi, strain st 549, hyperthermophilic archaea from deep-sea hydrothermal ecosystem,” FEBS Lett., vol. 431, pp. 279–284, 1998.
- X.L. Du, I.G. Choi, R. Kim, W.R. Wang, J. Jancarik, H. Yokota, and S.H. Kim, “Crystal structure of an intracellular protease from Pyrococcus horikoshii at 2-Å resolution,” Proc. Natl. Acad. Sci. USA, vol. 97, pp. 14079–14084, 2000.
- R.I. Eggen, A.C. Geerling, J. Watts, and W.M. de Vos, “Characterization of pyrolysin, a hyperthermoactive serine protease from the archaebacterium Pyrococcus furiosus,” FEMS Microbiol. Lett., vol. 71, pp. 17–20, 1990.
- G. Erauso, A.-L. Reysenbach, A. Godfroy et al., “Pyrococcus abyssi sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent,” Arch. Microbiol., vol. 160, pp. 338–349, 1993.
- G. Fiala and K.O. Stetter, “Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100 °C,” Arch. Microbiol., vol. 161, pp. 168–175, 1986.
- M. Fusek, X.L. Lin, and J. Tang, “Enzymic properties of thermopsin,” J. Biol. Chem., vol. 265, pp. 1496–1501, 1990.
- A.L. Goldberg, “Probing the proteasome pathway,” Nat. Biotechnol., vol. 18, pp. 494–496, 2000.
- J.M. Gonzalez, Y. Masuchi, F.T. Robb, J.W. Ammerman, M. Yanagibayashi, J. Tamaoka, and C. Kato, “Pyrococcus horikoshii sp. nov., a hyperthermophilic archaeon isolated from a hydrothermal vent at the Okinawa Trough,” Extremophiles, vol. 2, pp. 123–130, 1998.
- S. Gottesman, “Proteases and their targets in Escherichia coli,” Annu. Rev. Genet., vol. 30, pp. 465–506, 1996.
- S. Gottesman, “Regulation by proteolysis: developmental switches,” Curr. Opin. Microbiol., vol. 2, pp. 142–147, 1999.
- E. Guedon, P. Renault, S.D. Ehrlich, and C. Delorme, “Transcriptional pattern of genes coding for the proteolytic system of Lactococcus lactis and evidence for coordinated regulation of key enzymes by peptide supply,” J. Bacteriol., vol. 183, pp. 3614–3622, 2001.
- S.B. Halio, I.I. Blumentals, S.A. Short, B.M. Merrill, and R.M. Kelly, “Sequence, expression in Escherichia coli, and analysis of the gene encoding a novel intracellular protease (PfpI) from the hyperthermophilic archaeon Pyrococcus furiosus,” J. Bacteriol., vol. 178, pp. 2605–2612, 1996.
- S.B. Halio, M.W. Bauer, S. Mukund, M.W.W. Adams, and R.M. Kelly, “Purification and characterization of intracellular protease PfpI from the hyperthermophilic archaeon Pyrococcus furiosus,” Appl. Environ. Microbiol., vol. 63, pp. 289–295, 1997.
- M. Hecker, W. Schumann, and U. Volker, “Heat-shock and general stress response in Bacillus subtilis,” Mol. Microbiol., vol. 19, pp. 417–428, 1996.
- P.M. Hicks, K.D. Rinker, J.R. Baker, and R.M. Kelly, “Homomultimeric protease in the hyperthermophilic bacterium Thermotoga maritima has structural and amino acid sequence homology to bacteriocins in mesophilic bacteria,” FEBS Lett., vol. 440, pp. 393–398, 1998.
- P.M. Hicks, L.S. Chang, and R.M. Kelly, “Homomultimeric protease and putative bacteriocin homolog from Thermotoga maritima,” Methods Enzymol., vol. 330, pp. 455–460, 2001.
- R. Huber, T.A. Langworthy, H. König, M. Thomm, C.R. Woese, U.B. Sleytr, and K.O. Stetter, “Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90 °C,” Arch. Microbiol., vol. 144, pp. 324–333, 1986.
- Y. Kannan, Y. Koga, and Y. Koga, “Active subtilisin-like protease from a hyperthermophilic archaeon in a form with a putative prosequence,” Appl. Environ. Microbiol., vol. 67, pp. 2445–2452, 2001.
- Y. Kawarabayasi, M. Sawada, H. Horikawa et al., “Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3,” DNA Res., vol. 5, pp. 55–76, 1998.
- A.R. Khan, S. Nirasawa, S. Kaneko, T. Shimonishi, and K. Hayashi, “Characterization of a solvent resistant and thermostable aminopeptidase from the hyperthermophillic bacterium, Aquifex aeolicus,” Enzyme Microb. Technol., vol. 27, pp. 83–88, 2000.
- A.F. Kisselev, T.N. Akopian, and A.L. Goldberg, “Range of sizes of peptide products generated during degradation of different proteins by archaeal proteasomes,” J. Biol. Chem., vol. 273, pp. 1982–1989, 1998.
- M. Klingeberg, B. Galunsky, C. Sjoholm, V. Kasche, and G. Antranikian, “Purification and properties of a highly thermostable, sodium dodecyl sulfate-resistant and stereospecific proteinase from the extremely thermophilic archaeon Thermococcus stetteri,” Appl. Environ. Microbiol., vol. 61, pp. 3098–3104, 1995.
- E.V. Koonin, Y.I. Wolf, and L. Aravind, “Prediction of the archaeal exosome and its connections with the proteasome and the translation and transcription machineries by a comparative-genomic approach,” Genome Res., vol. 11, pp. 240–252, 2001.
- T. Langer, “AAA proteases: cellular machines for degrading membrane proteins,” TIBS., vol. 25, pp. 247–251, 2000.
- X. Lin, M. Fusek, and J. Tang, “Thermopsin, a thermostable acid protease from Sulfolobus acidocaldarius,” Adv. Exp. Med. Biol., vol. 306, pp. 255–257, 1991.
- J. Lowe, D. Stock, B. Jap, P. Zwickl, W. Baumeister, and R. Huber, “Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution.,” Science, vol. 268, pp. 533–539, 1995.
- A. Lupas, J.M. Flanagan, T. Tamura, and W. Baumeister, “Self-compartmentalizing proteases,” Trends Biochem. Sci., vol. 22, pp. 399–404, 1997.
- J.A. Maupin-Furlow and J.G. Ferry, “A proteasome from the methanogenic archaeon Methanosarcina thermophila,” J. Biol. Chem., vol. 270, pp. 28617–28622, 1995.
- J.A. Maupin-Furlow, H.L. Wilson, S.J. Kaczowka, and M.S. Ou, “Proteasomes in the Archaea: from structure to function,” Front. Biosci., vol. 5, pp. 837–865, 2000.
- M.R. Maurizi, “Proteases and protein degradation in Escherichia coli,” Experientia, vol. 48, pp. 178–201, 1992.
- J. Mayr, A. Lupas, J. Kellermann, C. Eckerskorn, W. Baumeister, and J. Peters, “A hyperthermostable protease of the subtilisin family bound to the surface layer of the archaeon Staphylothermus marinus,” Curr. Biol., vol. 6, pp. 739–749, 1996.
- M. Morikawa, Y. Izawa, N. Rashid, T. Hoaki, and T. Imanaka, “Purification and characterization of a thermostable thiol protease from a newly isolated hyperthermophilic Pyrococcus sp,” Appl. Environ. Microbiol., vol. 60, pp. 4559–4566, 1994.
- K.E. Nelson, R.A. Clayton, S.R. Gill et al., “Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima,” Nature, vol. 399, pp. 323–329, 1999.
- J. Porankiewicz, J. Wang, and A.K. Clarke, “New insights into the ATP-dependent Clp protease: Escherichia coli and beyond,” Mol. Microbiol., vol. 32, pp. 449–458, 1999.
- M. Rechsteiner, L. Hoffman, and W. Dubiel, “The multicatalytic and 26 S proteases,” J. Biol. Chem., vol. 268, pp. 6065–6068, 1993.
- A. Ruepp, C. Eckerskorn, M. Bogyo, and W. Baumeister, “Proteasome function is dispensable under normal but not under heat shock conditions in Thermoplasma acidophilum,” FEBS Lett., vol. 425, pp. 87–90, 1998.
- Y. Sako, P.C. Croocker, and Y. Ishida, “An extremely heat-stable extracellular proteinase (aeropyrolysin) from the hyperthermophilic archaeon Aeropyrum pernix K1,” FEBS Lett., vol. 415, pp. 329–334, 1997.
- M. Schmidt, A.N. Lupas, and D. Finley, “Structure and mechanism of ATP-dependent proteases,” Curr. Opin. Chem. Biol., vol. 3, pp. 584–591, 1999.
- W. Schumann, “FtsH—a single-chain charonin?” FEMS Microbiol. Rev., vol. 23, pp. 1–11, 1999.
- T. Schäfer, M. Selig, and P. Schönheit, “Acetyl-CoA synthetase (ADP forming) in archaea, a novel enzyme involved in acetate formation and ATP synthesis,” Arch. Microbiol., vol. 159, pp. 72–83, 1993.
- P. Schönheit and T. Schäfer, “Metabolism of hyperthermophiles,” World J. Microbiol. Biotechnol., vol. 11, pp. 26–57, 1995.
- Q. She, R.K. Singh, F. Confalonieri et al., “The complete genome of the crenarchaeon Sulfolobus solfataricus P2,” Proc. Natl. Acad. Sci. USA, vol. 98, pp. 7835–7840, 2001.
- B. Snel, G. Lehmann, P. Bork, and M.A. Huynen, “STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene,” Nucleic Acids Res., vol. 28, pp. 3442–3444, 2000.
- N. Tamura, F. Lottspeich, W. Baumeister, and T. Tamura, “The role of tricorn protease and its aminopeptidase-interacting factors in cellular protein degradation,” Cell, vol. 95, pp. 637–648, 1998.
- T. Tomoyasu, A. Mogk, H. Langen, P. Goloubinoff, and B. Bukau, “Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Eschirichia coli cytosol,” Mol. Microbiol., vol. 40, pp. 397–413, 2001.
- N. Valdes-Stauber and S. Scherer, “Nucleotide sequence and taxonomical distribution of the bacteriocin gene lin cloned from Brevibacterium linens M18,” Appl. Environ. Microbiol., vol. 62, pp. 1283–1286, 1996.
- W.G. Voorhorst, R.I. Eggen, A.C. Geerling, C. Platteeuw, R.J. Siezen, and W.M. de Vos, “Isolation and characterization of the hyperthermostable serine protease, pyrolysin, and its gene from the hyperthermophilic archaeon Pyrococcus furiosus,” J. Biol. Chem., vol. 271, pp. 20426–20431, 1996.
- W.G. Voorhorst, A. Warner, W.M. de Vos, and R.J. Siezen, “Homology modelling of two subtilisin-like proteases from the hyperthermophilic archaea Pyrococcus furiosus and Thermococcus stetteri,” Protein Eng., vol. 10, pp. 905–914, 1997.
- H.L. Wilson, H.C. Aldrich, and J. Maupin-Furlow, “Halophilic 20S proteasomes of the archaeon Haloferax volcanii: purification, characterization, and gene sequence analysis,” J. Bacteriol., vol. 181, pp. 5814–5824, 1999.
- H.L. Wilson, M.S. Ou, H.C. Aldrich, and J. Maupin-Furlow, “Biochemical and physical properties of the Methanococcus jannaschii 20S proteasome and PAN, a homolog of the ATPase (Rpt) subunits of the eucaryal 26S proteasome,” J. Bacteriol., vol. 182, pp. 1680–1692, 2000.
- W. Zillig, K.O. Stetter, S. Wunderl, W. Schulz, H. Priess, and I. Scholz, “The Sulfolobus “Caldariella” group: taxonomy on the basis of the structure of DNA-dependent RNA polymerases,” Arch. Microbiol., vol. 125, pp. 259–269, 1980.
Copyright © 2002 Hindawi Publishing Corporation. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.