1887

Abstract

Proteasomes play key roles in a variety of eukaryotic cell functions, including translation, transcription, metabolism, DNA repair and cell-cycle control. The biological functions of these multicatalytic proteases in archaea, however, are poorly understood. In this study, was used as a model to determine the influence the proteasome-specific inhibitor -lactacystin--lactone (LL) has on archaeal proteome composition. Addition of 20–30 μM LL had a widespread effect on the proteome, with a 38–42 % increase in the number of 2-D gel electrophoresis (2-DE) protein spots, from an average of 627 to 1036 spots. Protein identities for 17 of the spots that were easily separated by 2-DE and unique and/or increased 2- to 14-fold in the LL-treated cells were determined by tandem mass spectrometry (MS/MS). These included protein homologues of the DJ-1/ThiJ family, mobilization of sulfur system, translation elongation factor EF-1 A, ribosomal proteins, tubulin-like FtsZ, divalent metal ABC transporter, dihydroxyacetone kinase DhaL, aldehyde dehydrogenase and 2-oxoacid decarboxylase E1. Based on these results, inhibition of proteasomes had a global influence on proteome composition, including proteins involved in central functions of the cell.

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2007-07-01
2020-07-16
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References

  1. Arora S., Yang J. M., Hait W. N.. 2005; Identification of the ubiquitin-proteasome pathway in the regulation of the stability of eukaryotic elongation factor-2 kinase. Cancer Res65:3806–3810[CrossRef]
    [Google Scholar]
  2. Asher G., Reuven N., Shaul Y.. 2006; 20S proteasomes and protein degradation ‘by default’. Bioessays28:844–849[CrossRef]
    [Google Scholar]
  3. Bachler C., Schneider P., Bahler P., Lustig A., Erni B.. 2005; Escherichia coli dihydroxyacetone kinase controls gene expression by binding to transcription factor DhaR. EMBO J24:283–293[CrossRef]
    [Google Scholar]
  4. Bandyopadhyay S., Cookson M. R.. 2004; Evolutionary and functional relationships within the DJ1 superfamily. BMC Evol Biol4:6[CrossRef]
    [Google Scholar]
  5. Baugh J. M., Pilipenko E. V.. 2004; 20S proteasome differentially alters translation of different mRNAs via the cleavage of eIF4F and eIF3. Mol Cell16:575–586[CrossRef]
    [Google Scholar]
  6. Caldas T., Laalami S., Richarme G.. 2000; Chaperone properties of bacterial elongation factor EF-G and initiation factor IF2. J Biol Chem275:855–860[CrossRef]
    [Google Scholar]
  7. Casal J. J., Yanovsky M. J.. 2005; Regulation of gene expression by light. Int J Dev Biol49:501–511[CrossRef]
    [Google Scholar]
  8. Chuang S. M., Chen L., Lambertson D., Anand M., Kinzy T. G., Madura K.. 2005; Proteasome-mediated degradation of cotranslationally damaged proteins involves translation elongation factor 1A. Mol Cell Biol25:403–413[CrossRef]
    [Google Scholar]
  9. Claverys J. P.. 2001; A new family of high-affinity ABC manganese and zinc permeases. Res Microbiol152:231–243[CrossRef]
    [Google Scholar]
  10. Coux O.. 2003; An interaction map of proteasome subunits. Biochem Soc Trans31:465–469[CrossRef]
    [Google Scholar]
  11. Danson M. J., Eisenthal R., Hall S., Kessell S. R., Williams D. L.. 1984; Dihydrolipoamide dehydrogenase from halophilic archaebacteria. Biochem J218:811–818
    [Google Scholar]
  12. Del Sol R., Mullins J. G., Grantcharova N., Flardh K., Dyson P.. 2006; Influence of CrgA on assembly of the cell division protein FtsZ during development of Streptomyces coelicolor. J Bacteriol188:1540–1550[CrossRef]
    [Google Scholar]
  13. Devoy A., Soane T., Welchman R., Mayer R. J.. 2005; The ubiquitin-proteasome system and cancer. Essays Biochem41:187–203[CrossRef]
    [Google Scholar]
  14. Dopson M., Baker-Austin C., Bond P. L.. 2005; Analysis of differential protein expression during growth states of Ferroplasma strains and insights into electron transport for iron oxidation. Microbiology151:4127–4137[CrossRef]
    [Google Scholar]
  15. Erni B., Siebold C., Christen S., Srinivas A., Oberholzer A., Baumann U.. 2006; Small substrate, big surprise: fold, function and phylogeny of dihydroxyacetone kinases. Cell Mol Life Sci63:890–900[CrossRef]
    [Google Scholar]
  16. Falb M., Aivaliotis M., Garcia-Rizo C., Bisle B., Tebbe A., Klein C., Konstantinidis K., Siedler F., Pfeiffer F., Oesterhelt D.. 2006; Archaeal N-terminal protein maturation commonly involves N-terminal acetylation: a large-scale proteomics survey. J Mol Biol362:915–924[CrossRef]
    [Google Scholar]
  17. Fenteany G., Schreiber S. L.. 1998; Lactacystin, proteasome function, and cell fate. J Biol Chem273:8545–8548[CrossRef]
    [Google Scholar]
  18. Flynn J. M., Neher S. B., Kim Y. I., Sauer R. T., Baker T. A.. 2003; Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol Cell11:671–683[CrossRef]
    [Google Scholar]
  19. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M. R., Appel R. D., Bairoch A.. 2005; Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook pp571–607 Edited by Walker J. M.. Totawa, NJ: Humana Press;
    [Google Scholar]
  20. Giometti C. S., Reich C., Tollaksen S., Babnigg G., Lim H., Zhu W., Yates J., Olsen G.. 2002; Global analysis of a ‘simple’ proteome: Methanococcus jannaschii. J Chromatogr B Analyt Technol Biomed Life Sci782:227–243[CrossRef]
    [Google Scholar]
  21. Gonen H., Smith C. E., Siegel N. R., Kahana C., Merrick W. C., Chakraburity K., Schwartz A. L., Ciechanover A.. 1994; Protein synthesis elongation factor EF-1 α is essential for ubiquitin-dependent degradation of certain N α -acetylated proteins and may be substituted for by the bacterial elongation factor EF-Tu. Proc Natl Acad Sci U S A91:7648–7652[CrossRef]
    [Google Scholar]
  22. Gonen H., Dickman D., Schwartz A. L., Ciechanover A.. 1996; Protein synthesis elongation factor EF-1 α is an isopeptidase essential for ubiquitin-dependent degradation of certain proteolytic substrates. Adv Exp Med Biol389:209–219
    [Google Scholar]
  23. Goodchild A., Saunders N. F., Ertan H., Raftery M., Guilhaus M., Curmi P. M., Cavicchioli R.. 2004; A proteomic determination of cold adaptation in the Antarctic archaeon, Methanococcoides burtonii. Mol Microbiol53:309–321[CrossRef]
    [Google Scholar]
  24. Grant A. G., Flomen R. M., Tizard M. L., Grant D. A.. 1992; Differential screening of a human pancreatic adenocarcinoma λ gt11 expression library has identified increased transcription of elongation factor EF-1 α in tumour cells. Int J Cancer50:740–745[CrossRef]
    [Google Scholar]
  25. Hantke K.. 2005; Bacterial zinc uptake and regulators. Curr Opin Microbiol8:196–202[CrossRef]
    [Google Scholar]
  26. Heath C., Jeffries A. C., Hough D. W., Danson M. J.. 2004; Discovery of the catalytic function of a putative 2-oxoacid dehydrogenase multienzyme complex in the thermophilic archaeon Thermoplasma acidophilum. FEBS Lett577:523–527[CrossRef]
    [Google Scholar]
  27. Hotokezaka Y., Tobben U., Hotokezaka H., Van Leyen K., Beatrix B., Smith D. H., Nakamura T., Wiedmann M.. 2002; Interaction of the eukaryotic elongation factor 1A with newly synthesized polypeptides. J Biol Chem277:18545–18551[CrossRef]
    [Google Scholar]
  28. Humbard M. A., Maupin-Furlow J. A., Stevens S. M. Jr. 2006; Post-translational modification of the 20S proteasomal proteins of the archaeon Haloferax volcanii. J Bacteriol188:7521–7530[CrossRef]
    [Google Scholar]
  29. Jiang H. Y., Wek R. C.. 2005; Phosphorylation of the α -subunit of the eukaryotic initiation factor-2 (eIF2 α ) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem280:14189–14202[CrossRef]
    [Google Scholar]
  30. Johnston J. W., Myers L. E., Ochs M. M., Briles D. E., Hollingshead S. K., Benjamin W. H. Jr. 2004; Lipoprotein PsaA in virulence of Streptococcus pneumoniae : surface accessibility and role in protection from superoxide. Infect Immun72:5858–5867[CrossRef]
    [Google Scholar]
  31. Jolley K. A., Maddocks D. G., Gyles S. L., Mullan Z., Tang S. L., Dyall-Smith M. L., Hough D. W., Danson M. J.. 2000; 2-Oxoacid dehydrogenase multienzyme complexes in the halophilic Archaea? Gene sequences and protein structural predictions. Microbiology146:1061–1069
    [Google Scholar]
  32. Kanemori M., Yanagi H., Yura T.. 1999; The ATP-dependent HslVU/ClpQY protease participates in turnover of cell division inhibitor SulA in Escherichia coli. J Bacteriol181:3674–3680
    [Google Scholar]
  33. Karadzic I. M., Maupin-Furlow J. A.. 2005; Improvement of two-dimensional gel electrophoresis proteome maps of the haloarchaeon Haloferax volcanii. Proteomics5:354–359[CrossRef]
    [Google Scholar]
  34. Kim H. J., Joo W. A., Cho C. W., Kim C. W.. 2006a; Halophile aldehyde dehydrogenase from Halobacterium salinarum. J Proteome Res5:192–195[CrossRef]
    [Google Scholar]
  35. Kim T. S., Jang C. Y., Kim H. D., Lee J. Y., Ahn B. Y., Kim J.. 2006b; Interaction of Hsp90 with ribosomal proteins protects from ubiquitination and proteasome-dependent degradation. Mol Biol Cell17:824–833
    [Google Scholar]
  36. Kirkland P. A., Busby J., Maupin-Furlow J. A., Stevens S. Jr. 2006; Trizol-based method for sample preparation and isoelectric focusing of halophilic proteins. Anal Biochem351:254–259[CrossRef]
    [Google Scholar]
  37. Kloetzel P. M., Ossendorp F.. 2004; Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr Opin Immunol16:76–81[CrossRef]
    [Google Scholar]
  38. Krieg P. A., Varnum S. M., Wormington W. M., Melton D. A.. 1989; The mRNA encoding elongation factor 1- α (EF-1 α ) is a major transcript at the midblastula transition in Xenopus. Dev Biol133:93–100[CrossRef]
    [Google Scholar]
  39. Kruse T., Blagoev B., Lobner-Olesen A., Wachi M., Sasaki K., Iwai N., Mann M., Gerdes K.. 2006; Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. Genes Dev20:113–124[CrossRef]
    [Google Scholar]
  40. Lee J. H., Yeo W. S., Roe J. H.. 2004; Induction of the sufA operon encoding Fe-S assembly proteins by superoxide generators and hydrogen peroxide: involvement of OxyR, IHF and an unidentified oxidant-responsive factor. Mol Microbiol51:1745–1755[CrossRef]
    [Google Scholar]
  41. Lill R., Muhlenhoff U.. 2005; Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci30:133–141[CrossRef]
    [Google Scholar]
  42. Lipford J. R., Smith G. T., Chi Y., Deshaies R. J.. 2005; A putative stimulatory role for activator turnover in gene expression. Nature438:113–116[CrossRef]
    [Google Scholar]
  43. Lopez-Valenzuela J. A., Gibbon B. C., Hughes P. A., Dreher T. W., Larkins B. A.. 2003; eEF1A isoforms change in abundance and actin-binding activity during maize endosperm development. Plant Physiol133:1285–1295[CrossRef]
    [Google Scholar]
  44. Lupas A.. 1996; Prediction and analysis of coiled-coil structures. Methods Enzymol266:513–525
    [Google Scholar]
  45. Malki A., Caldas T., Abdallah J., Kern R., Eckey V., Kim S. J., Cha S. S., Mori H., Richarme G.. 2005; Peptidase activity of the Escherichia coli Hsp31 chaperone. J Biol Chem280:14420–14426[CrossRef]
    [Google Scholar]
  46. Margolin W.. 2005; FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol6:862–871[CrossRef]
    [Google Scholar]
  47. Mascarenhas J., Volkov A. V., Rinn C., Schiener J., Guckenberger R., Graumann P. L.. 2005; Dynamic assembly, localization and proteolysis of the Bacillus subtilis SMC complex. BMC Cell Biol6:28[CrossRef]
    [Google Scholar]
  48. Maupin-Furlow J. A., Gil M. A., Karadzic I. M., Kirkland P. A., Reuter C. J.. 2004; Proteasomes: perspectives from the archaea. Front Biosci9:1743–1758 update 2004[CrossRef]
    [Google Scholar]
  49. Maupin-Furlow J. A., Gil M. A., Humbard M. A., Kirkland P. A., Li W., Reuter C. J., Wright A. J.. 2006; Proteasomes and other nanocompartmentalized proteases in archaea. In Complex Intracellular Structures in Prokaryotes pp23–46 Edited by Shively J. M.. Berlin: Springer-Verlag;
    [Google Scholar]
  50. Mizusawa S., Gottesman S.. 1983; Protein degradation in Escherichia coli : the lon gene controls the stability of sulA protein. Proc Natl Acad Sci U S A80:358–362[CrossRef]
    [Google Scholar]
  51. Nasmyth K., Haering C. H.. 2005; The structure and function of SMC and kleisin complexes. Annu Rev Biochem74:595–648[CrossRef]
    [Google Scholar]
  52. Outten F. W., Djaman O., Storz G.. 2004; A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol Microbiol52:861–872[CrossRef]
    [Google Scholar]
  53. Ransom-Hodgkins W. D., Brglez I., Wang X., Boss W. F.. 2000; Calcium-regulated proteolysis of eEF1A. Plant Physiol122:957–965[CrossRef]
    [Google Scholar]
  54. Reuter C. J., Maupin-Furlow J. A.. 2004; Analysis of proteasome-dependent proteolysis in Haloferax volcanii cells, using short-lived green fluorescent proteins. Appl Environ Microbiol70:7530–7538[CrossRef]
    [Google Scholar]
  55. Sastry M. S. R., Korotkov K., Brodsky Y., Baneyx F.. 2002; Hsp31, the Escherichia coli yedU gene product, is a molecular chaperone whose activity is inhibited by ATP at high temperatures. J Biol Chem277:46026–46034[CrossRef]
    [Google Scholar]
  56. Shukla H. D.. 2006; Proteomic analysis of acidic chaperones, and stress proteins in extreme halophile Halobacterium NRC-1: a comparative proteomic approach to study heat shock response. Proteome Sci4:6[CrossRef]
    [Google Scholar]
  57. Smith D. M., Benaroudj N., Goldberg A.. 2006; Proteasomes and their associated ATPases: a destructive combination. J Struct Biol156:72–83[CrossRef]
    [Google Scholar]
  58. Snowden L. J., Blumentals I. I., Kelly R. M.. 1992; Regulation of proteolytic activity in the hyperthermophile Pyrococcus furiosus. Appl Environ Microbiol58:1134–1141
    [Google Scholar]
  59. Verma R., Chen S., Feldman R., Schieltz D., Yates J., Dohmen J., Deshaies R. J.. 2000; Proteasomal proteomics: identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes. Mol Biol Cell11:3425–3439[CrossRef]
    [Google Scholar]
  60. Wang W., Poovaiah B. W.. 1999; Interaction of plant chimeric calcium/calmodulin-dependent protein kinase with a homolog of eukaryotic elongation factor-1 α. J Biol Chem274:12001–12008[CrossRef]
    [Google Scholar]
  61. Wanner C., Soppa J.. 2002; Functional role for a 2-oxo acid dehydrogenase in the halophilic archaeon Haloferax volcanii. J Bacteriol184:3114–3121[CrossRef]
    [Google Scholar]
  62. Weart R. B., Nakano S., Lane B. E., Zuber P., Levin P. A.. 2005; The ClpX chaperone modulates assembly of the tubulin-like protein FtsZ. Mol Microbiol57:238–249[CrossRef]
    [Google Scholar]
  63. Whiteheart S. W., Shenbagamurthi P., Chen L., Cotter R. J., Hart G. W.. 1989; Murine elongation factor 1 α (EF-1 α ) is posttranslationally modified by novel amide-linked ethanolamine-phosphoglycerol moieties. Addition of ethanolamine-phosphoglycerol to specific glutamic acid residues on EF-1 α. J Biol Chem264:14334–14341
    [Google Scholar]
  64. Wilson H. L., Aldrich H. C., Maupin-Furlow J. A.. 1999; Halophilic 20S proteasomes of the archaeon Haloferax volcanii : purification, characterization, and gene sequence analysis. J Bacteriol181:5814–5824
    [Google Scholar]
  65. Zobel-Thropp P., Yang M. C., Machado L., Clarke S.. 2000; A novel post-translational modification of yeast elongation factor 1A. Methylesterification at the C terminus. J Biol Chem275:37150–37158[CrossRef]
    [Google Scholar]
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