HtpG, the prokaryotic homologue of Hsp90, stabilizes a phycobilisome protein in the cyanobacterium Synechococcus elongatus PCC 7942

Molecular Microbiology

Volumn 76, Issue 3, 2010, Pages 576-589

  Sato, Takeshi ^a   Minagawa, Shun ^a   Kojima, Erika ^a   Okamoto, Naoki ^a   Nakamoto, Hitoshi ^a  

^a SAITAMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CELL PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN 90; PEPTIDE DERIVATIVE; POLYPEPTIDE; PROTEIN HTPG; UNCLASSIFIED DRUG; HTPG PROTEIN, BACTERIA; PHYCOBILISOME; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; NONHUMAN; PHYCOBILISOME; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SYNECHOCOCCUS ELONGATUS; CHEMISTRY; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; SYNECHOCOCCUS;

CYANOBACTERIA; PROKARYOTA; SYNECHOCOCCUS ELONGATUS PCC 6301; SYNECHOCOCCUS ELONGATUS PCC 7942;

BACTERIAL PROTEINS; DIMERIZATION; HSP90 HEAT-SHOCK PROTEINS; PHYCOBILISOMES; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SYNECHOCOCCUS;

EID: 77951610740     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07139.x     Document Type: Article

References (45)

1. Adir, N. (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85 : 15 32. (Pubitemid 40678757)
2. Ali, M.M., Roe, S.M., Vaughan, C.K., Meyer, P., Panaretou, B., Piper, P.W., et al 2006) Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440 : 1013 1017.
3. Arnon, D.I., McSwain, B.D., Tsujimoto, H.Y. Wada, K. (1974) Photochemical activity and components of membrane preparations from blue-green algae. I. Coexistence of two photosystems in relation to chlorophyll a and removal of phycocyanin. Biochim Biophys Acta 357 : 231 245.
4. Bardwell, J.C. Craig, E.A. (1988) Ancient heat shock gene is dispensable. J Bacteriol 170 : 2977 2983.
5. Borkovich, K.A., Farrelly, F.W., Finkelstein, D.B., Taulien, J. Lindquist, S. (1989) hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 9 : 3919 3930. (Pubitemid 19216285)
6. Dollins, D.E., Warren, J.J., Immormino, R.M. Gewirth, D.T. (2007) Structures of GRP94-nucleotide complexes reveal mechanistic differences between the hsp90 chaperones. Mol Cell 28 : 41 56.
7. Falsone, S.F., Kungl, A.J., Rek, A., Cappai, R. Zangger, K. (2009) The molecular chaperone Hsp90 modulates intermediate steps of amyloid assembly of the Parkinson-related protein alpha-synuclein. J Biol Chem 284 : 31190 31199.
8. Glazer, A.N. (1989) Light guides. Directional energy transfer in a photosynthetic antenna. J Biol Chem 264 : 1 4.
9. Golden, S.S., Nalty, M.S. Cho, D.S. (1989) Genetic relationship of two highly studied Synechococcus strains designated Anacystis nidulans. J Bacteriol 171 : 24 29.
10. Grossman, A.R., Schaefer, M.R., Chiang, G.G. Collier, J.L. (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57 : 725 749. (Pubitemid 23262516)
11. Harris, S.F., Shiau, A.K. Agard, D.A. (2004) The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site. Structure 12 : 1087 1097.
12. Hessling, M., Richter, K. Buchner, J. (2009) Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90. Nat Struct Mol Biol 16 : 287 293.
13. Jakob, U., Lilie, H., Meyer, I. Buchner, J. (1995) Transient interaction of Hsp90 with early unfolding intermediates of citrate synthase. Implications for heat shock in vivo. J Biol Chem 270 : 7288 7294.
14. Krukenberg, K.A., Southworth, D.R., Street, T.O. Agard, D.A. (2009) pH-dependent conformational changes in bacterial Hsp90 reveal a Grp94-like conformation at pH 6 that is highly active in suppression of citrate synthase aggregation. J Mol Biol 390 : 278 291.
15. Liu, L.N., Chen, X.L., Zhang, Y.Z. Zhou, B.C. (2005) Characterization, structure and function of linker polypeptides in phycobilisomes of cyanobacteria and red algae: an overview. Biochim Biophys Acta 1708 : 133 142.
16. Lundell, D.J., Williams, R.C. Glazer, A.N. (1981) Molecular architecture of a light-harvesting antenna. In vitro assembly of the rod substructures of Synechococcus 6301 phycobilisomes. J Biol Chem 256 : 3580 3592.
17. MacColl, R. (1998) Cyanobacterial phycobilisomes. J Struct Biol 124 : 311 334. (Pubitemid 29143068)
18. McLaughlin, S.H., Ventouras, L.A., Lobbezoo, B. Jackson, S.E. (2004) Independent ATPase activity of Hsp90 subunits creates a flexible assembly platform. J Mol Biol 344 : 813 826. (Pubitemid 39469222)
19. Mickler, M., Hessling, M., Ratzke, C., Buchner, J. Hugel, T. (2009) The large conformational changes of Hsp90 are only weakly coupled to ATP hydrolysis. Nat Struct Mol Biol 16 : 281 286.
20. Nakamoto, H. Honma, D. (2006) Interaction of a small heat shock protein with light-harvesting cyanobacterial phycocyanins under stress conditions. FEBS Lett 580 : 3029 3034. (Pubitemid 43729678)
21. Neckers, L. (2002) Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol Med 8 : S55 S61. (Pubitemid 34297080)
22. Nemoto, T., Ohara-Nemoto, Y., Ota, M., Takagi, T. Yokoyama, K. (1995) Mechanism of dimer formation of the 90-kDa heat-shock protein. Eur J Biochem 233 : 1 8.
23. Parbel, A. Scheer, H. (2000) Model for the phycobilisome rod with interlocking disks based on domain-weighted linker-polypeptide sequence homologies of Mastigocladus laminosus. Int J Photoenergy 2 : 31 40.
24. Pearl, L.H. Prodromou, C. (2006) Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75 : 271 294. (Pubitemid 44118034)
25. Picard, D. (2006) Chaperoning steroid hormone action. Trends Endocrinol Metab 17 : 229 235. (Pubitemid 44164280)
26. Pratt, W.B. Toft, D.O. (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood) 228 : 111 133. (Pubitemid 36187918)
27. Prodromou, C., Roe, S.M., O'Brien, R., Ladbury, J.E., Piper, P.W. Pearl, L.H. (1997) Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90 : 65 75. (Pubitemid 28009419)
28. Richter, K., Muschler, P., Hainzl, O. Buchner, J. (2001) Coordinated ATP hydrolysis by the Hsp90 dimer. J Biol Chem 276 : 33689 33696. (Pubitemid 37384586)
29. Roy, S.K., Hiyama, T. Nakamoto, H. (1999) Purification and characterization of the 16-kDa heat-shock-responsive protein from the thermophilic cyanobacterium Synechococcus vulcanus, which is an alpha-crystallin-related, small heat shock protein. Eur J Biochem 262 : 406 416. (Pubitemid 29266052)
30. Saito, M., Watanabe, S., Yoshikawa, H. Nakamoto, H. (2008) Interaction of the molecular chaperone HtpG with uroporphyrinogen decarboxylase in the cyanobacterium Synechococcus elongatus PCC 7942. Biosci Biotechnol Biochem 72 : 1394 1397. (Pubitemid 351872510)
31. Scheibel, T., Weikl, T. Buchner, J. (1998) Two chaperone sites in Hsp90 differing in substrate specificity and ATP dependence. Proc Natl Acad Sci USA 95 : 1495 1499. (Pubitemid 28103420)
32. Shiau, A.K., Harris, S.F., Southworth, D.R. Agard, D.A. (2006) Structural Analysis of E. coli hsp90 reveals dramatic nucleotide-dependent conformational rearrangements. Cell 127 : 329 340.
33. Southworth, D.R. Agard, D.A. (2008) Species-dependent ensembles of conserved conformational states define the Hsp90 chaperone ATPase cycle. Mol Cell 32 : 631 640.
34. Spence, J. Georgopoulos, C. (1989) Purification and properties of the Escherichia coli heat shock protein, HtpG. J Biol Chem 264 : 4398 4403. (Pubitemid 19081339)
35. Tanaka, N. Nakamoto, H. (1999) HtpG is essential for the thermal stress management in cyanobacteria. FEBS Lett 458 : 117 123. (Pubitemid 29428166)
36. Ughy, B. Ajlani, G. (2004) Phycobilisome rod mutants in Synechocystis sp. strain PCC6803. Microbiology 150 : 4147 4156. (Pubitemid 40045343)
37. Vaughan, C.K., Gohlke, U., Sobott, F., Good, V.M., Ali, M.M., Prodromou, C., et al 2006) Structure of an Hsp90-Cdc37-Cdk4 complex. Mol Cell 23 : 697 707. (Pubitemid 44292559)
38. Versteeg, S., Mogk, A. Schumann, W. (1999) The Bacillus subtilis htpG gene is not involved in thermal stress management. Mol Gen Genet 261 : 582 588. (Pubitemid 29185051)
39. Wandinger, S.K., Richter, K. Buchner, J. (2008) The Hsp90 chaperone machinery. J Biol Chem 283 : 18473 18477.
40. Watanabe, S., Kobayashi, T., Saito, M., Sato, M., Nimura-Matsune, K., Chibazakura, T., et al 2007) Studies on the role of HtpG in the tetrapyrrole biosynthesis pathway of the cyanobacterium Synechococcus elongatus PCC 7942. Biochem Biophys Res Commun 352 : 36 41. (Pubitemid 44821090)
41. Wiech, H., Buchner, J., Zimmermann, R. Jakob, U. (1992) Hsp90 chaperones protein folding in vitro. Nature 358 : 169 170.
42. Winston, J.L., Toth, S.I., Roe, B.A. Dyer, D.W. (1996) Cloning and characterization of the Actinobacillus actinomycetemcomitans gene encoding a heat-shock protein 90 homologue. Gene 179 : 199 204. (Pubitemid 26397692)
43. Yamanaka, G., Glazer, A.N. Williams, R.C. (1978) Cyanobacterial phycobilisomes. Characterization of the phycobilisomes of Synechococcus sp. 6301. J Biol Chem 253 : 8303 8310. (Pubitemid 9073733)
44. Young, J.C., Schneider, C. Hartl, F.U. (1997) In vitro evidence that hsp90 contains two independent chaperone sites. FEBS Lett 418 : 139 143. (Pubitemid 27514433)
45. Young, J.C., Moarefi, I. Hartl, F.U. (2001) Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154 : 267 273. (Pubitemid 34286138)