Ribosomal protein L2 associates with E. coli HtpG and activates its ATPase activity

Biochemical and Biophysical Research Communications

Volumn 400, Issue 2, 2010, Pages 241-245

  Motojima Miyazaki, Yuko ^a   Yoshida, Masasuke ^b   Motojima, Fumihiro ^b  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b KYOTO SANGYO UNIVERSITY   (Japan)

Author keywords

ATPase activation; Hsp90; HtpG; L2; Ribosomal protein

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; CHAPERONIN; ESCHERICHIA COLI PROTEIN; PROTEIN DNAJ; PROTEIN DNAK; PROTEIN HTPG; RIBOSOME PROTEIN; RIBOSOME PROTEIN L2; SODIUM CHLORIDE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; HEAT SHOCK PROTEIN 90; HTPG PROTEIN, E COLI; POTASSIUM CHLORIDE; RIBOSOMAL PROTEIN L2;

ARTICLE; BACTERIUM CULTURE; CARBOXY TERMINAL SEQUENCE; CONCENTRATION (PARAMETERS); ENZYME ACTIVATION; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYDROLYSIS; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ENZYME ACTIVATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HYDROLYSIS; POTASSIUM CHLORIDE; PROTEIN STRUCTURE, TERTIARY; RIBOSOMAL PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

EID: 77956766997     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2010.08.047     Document Type: Article

References (43)

1. Richter K., Buchner J. Hsp90: chaperoning signal transduction. J. Cell. Physiol. 2001, 188:281-290.
2. Pratt W.B., Morishima Y., Osawa Y. The Hsp90 chaperone machinery regulates signaling by modulating ligand binding clefts. J. Biol. Chem. 2008, 283:22885-22889.
3. Gupta R.S. Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol. Biol. Evol. 1995, 12:1063-1073.
4. Lindquist S., Craig E.A. The heat-shock proteins. Annu. Rev. Genet. 1988, 22:631-677.
5. Borkovich K.A., Farrelly F.W., Finkelstein D.B., Taulien J., Lindquist S. Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell. Biol. 1989, 9:3919-3930.
6. Bardwell J.C., Craig E.A. Ancient heat shock gene is dispensable. J. Bacteriol. 1988, 170:2977-2983.
7. Thomas J.G., Baneyx F. Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG In vivo. J. Bacteriol. 1998, 180:5165-5172.
8. Shiau A.K., Harris S.F., Southworth D.R., Agard D.A. Structural analysis of E. coli hsp90 reveals dramatic nucleotide-dependent conformational rearrangements. Cell 2006, 127:329-340.
9. Southworth D.R., Agard D.A. Species-dependent ensembles of conserved conformational states define the Hsp90 chaperone ATPase cycle. Mol. Cell 2008, 32:631-640.
10. Nadeau K., Das A., Walsh C.T. Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J. Biol. Chem. 1993, 268:1479-1487.
11. Guisbert E., Herman C., Lu C.Z., Gross C.A. A chaperone network controls the heat shock response in E. coli. Genes Dev. 2004, 18:2812-2821.
12. Thomas J.G., Baneyx F. ClpB and HtpG facilitate de novo protein folding in stressed Escherichia coli cells. Mol. Microbiol. 2000, 36:1360-1370.
13. Shirai Y., Akiyama Y., Ito K. Suppression of ftsH mutant phenotypes by overproduction of molecular chaperones. J. Bacteriol. 1996, 178:1141-1145.
14. Ueguchi C., Ito K. Multicopy suppression: an approach to understanding intracellular functioning of the protein export system. J. Bacteriol. 1992, 174:1454-1461.
15. Vivien E., Megessier S., Pieretti I., Cociancich S., Frutos R., Gabriel D.W., Rott P.C., Royer M. Xanthomonas albilineans HtpG is required for biosynthesis of the antibiotic and phytotoxin albicidin. FEMS Microbiol. Lett. 2005, 251:81-89.
16. Watanabe S., Kobayashi T., Saito M., Sato M., Nimura-Matsune K., Chibazakura T., Taketani S., Nakamoto H., Yoshikawa H. Studies on the role of HtpG in the tetrapyrrole biosynthesis pathway of the cyanobacterium Synechococcus elongatus PCC 7942. Biochem. Biophys. Res. Commun. 2007, 352:36-41.
17. Saito M., Watanabe S., Yoshikawa H., Nakamoto H. Interaction of the molecular chaperone HtpG with uroporphyrinogen decarboxylase in the cyanobacterium Synechococcus elongatus PCC 7942. Biosci. Biotechnol. Biochem. 2008, 72:1394-1397.
18. Sato T., Minagawa S., Kojima E., Okamoto N., Nakamoto H. HtpG, the prokaryotic homologue of Hsp90, stabilizes a phycobilisome protein in the cyanobacterium Synechococcus elongatus PCC 7942. Mol. Microbiol. 2010, 76:576-589.
19. Jakob U., Lilie H., Meyer I., Buchner J. Transient interaction of Hsp90 with early unfolding intermediates of citrate synthase, implications for heat shock in vivo. J. Biol. Chem. 1995, 270:7288-7294.
20. McLaughlin S.H., Smith H.W., Jackson S.E. Stimulation of the weak ATPase activity of human hsp90 by a client protein. J. Mol. Biol. 2002, 315:787-798.
21. Datsenko K.A., Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 2000, 97:6640-6645.
22. Randall L.L., Hardy S.J. Correlation of competence for export with lack of tertiary structure of the mature species: a study in vivo of maltose-binding protein in E. coli. Cell 1986, 46:921-928.
23. Taniguchi K., Nomura K., Hata Y., Nishimura T., Asami Y., Kuroda A. The Si-tag for immobilizing proteins on a silica surface. Biotechnol. Bioeng. 2007, 96:1023-1029.
24. Chang H.C., Lindquist S. Conservation of Hsp90 macromolecular complexes in Saccharomyces cerevisiae. J. Biol. Chem. 1994, 269:24983-24988.
25. Panaretou B., Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., Pearl L.H. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J. 1998, 17:4829-4836.
26. Young J.C., Hartl F.U. Polypeptide release by Hsp90 involves ATP hydrolysis and is enhanced by the co-chaperone p23. EMBO J. 2000, 19:5930-5940.
27. Diedrich G., Spahn C.M., Stelzl U., Schafer M.A., Wooten T., Bochkariov D.E., Cooperman B.S., Traut R.R., Nierhaus K.H. Ribosomal protein L2 is involved in the association of the ribosomal subunits, tRNA binding to A and P sites and peptidyl transfer. EMBO J. 2000, 19:5241-5250.
28. Bolanos-Garcia V.M., Davies O.R. Structural analysis and classification of native proteins from E. coli commonly co-purified by immobilised metal affinity chromatography. Biochim. Biophys. Acta 2006, 1760:1304-1313.
29. Uhlein M., Weglohner W., Urlaub H., Wittmann-Liebold B. Functional implications of ribosomal protein L2 in protein biosynthesis as shown by in vivo replacement studies. Biochem. J. 1998, 331(Pt 2):423-430.
30. Hayashi T., Tahara M., Iwasaki K., Kouzuma Y., Kimura M. Requirement for C-terminal extension to the RNA binding domain for efficient RNA binding by ribosomal protein L2. Biosci. Biotechnol. Biochem. 2002, 66:682-684.
31. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., Cate J.H. Structures of the bacterial ribosome at 3.5 A resolution. Science 2005, 310:827-834.
32. Muller L., Schaupp A., Walerych D., Wegele H., Buchner J. Hsp90 regulates the activity of wild type p53 under physiological and elevated temperatures. J. Biol. Chem. 2004, 279:48846-48854.
33. Howard K.J., Holley S.J., Yamamoto K.R., Distelhorst C.W. Mapping the HSP90 binding region of the glucocorticoid receptor. J. Biol. Chem. 1990, 265:11928-11935.
34. Cadepond F., Binart N., Chambraud B., Jibard N., Schweizer-Groyer G., Segard-Maurel I., Baulieu E.E. Interaction of glucocorticosteroid receptor and wild-type or mutated 90-kDa heat shock protein coexpressed in baculovirus-infected Sf9 cells. Proc. Natl. Acad. Sci. USA 1993, 90:10434-10438.
35. Sato S., Fujita N., Tsuruo T. Modulation of Akt kinase activity by binding to Hsp90. Proc. Natl. Acad. Sci. USA 2000, 97:10832-10837.
36. Sullivan W.P., Toft D.O. Mutational analysis of hsp90 binding to the progesterone receptor. J. Biol. Chem. 1993, 268:20373-20379.
37. Flynn G.C., Chappell T.G., Rothman J.E. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 1989, 245:385-390.
38. Uversky V.N., Gillespie J.R., Fink A.L. Why are natively unfolded, proteins unstructured under physiologic conditions?. Proteins 2000, 41:415-427.
39. Murzin A.G., Brenner S.E., Hubbard T., Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 1995, 247:536-540.
40. Butland G., Peregrin-Alvarez J.M., Li J., Yang W., Yang X., Canadien V., Starostine A., Richards D., Beattie B., Krogan N., Davey M., Parkinson J., Greenblatt J., Emili A. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 2005, 433:531-537.
41. Kim T.S., Jang C.Y., Kim H.D., Lee J.Y., Ahn B.Y., Kim J. Interaction of Hsp90 with ribosomal proteins protects from ubiquitination and proteasome-dependent degradation. Mol. Biol. Cell 2006, 17:824-833.
42. Zhao R., Kakihara Y., Gribun A., Huen J., Yang G., Khanna M., Costanzo M., Brost R.L., Boone C., Hughes T.R., Yip C.M., Houry W.A. Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J. Cell Biol. 2008, 180:563-578.
43. Boulon S., Marmier-Gourrier N., Pradet-Balade B., Wurth L., Verheggen C., Jady B.E., Rothe B., Pescia C., Robert M.C., Kiss T., Bardoni B., Krol A., Branlant C., Allmang C., Bertrand E., Charpentier B. The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J. Cell Biol. 2008, 180:579-595.