HEAT SHOCK PROTEIN 90C is a bona fide Hsp90 that interacts with plastidic HSP70B in Chlamydomonas reinhardtii

Plant Physiology

Volumn 138, Issue 4, 2005, Pages 2310-2322

  Willmund, Felix ^a   Schroda, Michael ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINETRIPHOSPHATE; MICROORGANISMS; MONOMERS;

CHAPERONES; CHLAMYDOMONAS REINHARDTII; ENDOPLASMIC RETICULUM; HEAT SHOCK; PLASTIDIC PROTEIN;

PROTEINS;

MICROORGANISMS; MONOMERS; PROTEINS;

CHLAMYDOMONAS REINHARDTII;

HEAT SHOCK PROTEIN; ISOPROTEIN; LACTONE; MACROLIDE; RADICICOL;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; HEAT; LIGHT; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PLASTID; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; HEAT; HEAT-SHOCK PROTEINS; LACTONES; LIGHT; MACROLIDES; MOLECULAR SEQUENCE DATA; PLASTIDS; PROTEIN ISOFORMS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 33644666048     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.063578     Document Type: Article

References (71)

1. Ali A, Bharadwaj S, O'Carrol R, Ovsenek N (1998) Hsp90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes. Mol Cell Biol 18: 4949-4960
2. 2 adapted cells of Chlamydomonas reinhardtii. DNA Res 7: 305-307
3. Asamizu E, Nakamura Y, Sato S, Fukuzawa H, Tabata S (1999) A large scale structural analysis of cDNAs in a unicellular green alga, Chlamydomonas reinhardtii. Generation of 3433 non-redundant expressed sequence tags. DNA Res 6: 369-373
4. Buhen SP, Yamamoto KR. (1993) Isolation of Hsp90 mutants by screening for decreased steroid receptor function. Proc Natl Acad Sci USA 90: 11424-11428
5. Brychzy A, Rein T, Winklhofer KF, Hartl FU, Young JC, Obermann WMJ (2003) Cofactor Tpr2 combines two TPR domains and a J domain to regulate the Hsp70/Hsp90 chaperone system. EMBO J 22: 3613-3623
6. Buchner J (1999) HSP90 & Co.-a holding for folding. Trends Biochem Sci 24: 136-141
7. Cao D, Froehlich JE, Zhang H, Cheng C-L (2003) The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90. Plant J 33: 107-118
8. Cao D, Lin Y, Cheng C-L (2000) Genetic interactions between the chlorate-resistant mutant cr88 and the photomorphogenic mutants cop1 and hy5. Plant Cell 12: 199-210
9. Chadli A, Bouhouche I, Sullivan W, Stensgard B, McMahon N, Catelli MG, Toft DO (2000) Dimerization and N-terminal domain proximity underlie the function of the molecular chaperone heat shock protein 90. Proc Natl Acad Sci USA 97: 12524-12529
10. Csermely P, Schnaider T, Söti C, Prohászka Z, Nardai G (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 79: 129-168
11. Drzymalla C, Schroda M, Beck CF (1996) Light inducible gene HSP70B encodes a chloroplast-localized heat shock protein in Chlamydomonas reinhardtii. Plant Mol Biol 31: 1185-1194
12. Eisenthal R, Cornish-Bowden A (1974) The direct linear plot. Biochem J 139: 715-720
13. Emanuelsson O, Nilsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016
14. Emelyanov VV (2002) Phylogenetic relationship of organellar Hsp90 homologs reveal fundamental differences to organellar Hsp70 and Hsp60 evolution. Gene 299: 125-133
15. Eriksson M, Gardeström P, Samuelsson G (1995) Isolation, purification, and characterization of mitochondria from Chlamydomonas reinhardtii. Plant Physiol 107: 479-483
16. 2-induced polypeptide in Chlamydomonas reinhardtii. Proc Nati Acad Sci USA 93: 12031-12034
17. Feinberg AP, Vogelstein B (1983) A technique for radiolabelling DNA restriction endonuclease fragments to high activity. Anal Biochem 132: 6-13
18. Felts SJ, Owen BAL, Nguyen P, Trepel J, Donner DB, Toft DO (2000) The hsp90-related protein TEAP1 is a mitochondrial protein with distinct functional properties. J Biol Chem 275: 3305-3312
19. Freitag DG, Ouimet PM, Girvitz TL, Kapoor M (1997) Heat shock protein 80 of Neurospora crassa, a cytosolic molecular chaperone of the eukaryotic stress 90 family, interacts directly with heat shock protein 70. Biochemistry 36: 10221-10229
20. Harris EH (1989) The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego
21. Hutchison KA, Brott BK, De Leon JH, Perdew GH, Jove R, Pratt WB (1992) Reconstitution of the multiprotein complex of pp60src, hsp90, and p50 in a cell-free system. J Biol Chem 267: 2902-2908
22. Jakob U, Lilie H, Meyer I, Buchner J (1995) Transient interactions of Hsp90 with early unfolding intermediates of citrate synthase. Implications for heat shock in vivo. J Biol Chem 270: 7288-7294
23. Kamal A, Thao L, Sensintaffar J, Zhang L, Boehm MF, Fritz LC, Burrows FJ (2003) A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425: 407-410
24. Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6: 238-246
25. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685
26. Lin B-L, Wang J-S, Lin H-C, Chen R-W, Meyer Y, Barakat A, Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 6: 201-208
27. Lin Y, Cheng CL (1997) A chlorate-resistant mutant defective in the regulation of nitrate reductase gene expression in Arabidopsis defines a new HY locus. Plant Cell 9: 21-35
28. Liu C, Willmund F, Whitelegge JP, Hawat S, Knapp B, Lodha M, Schroda M (2005) J-domain protein CDJ2 and HSP70B are a plastidic chaperone pair that interacts with vesicle inducing protein in plastids 1 (VIPP1). Mol Biol Cell 16: 1165-1177
29. Mason CA, Dunner J, Indra P, Colangelo T (1999) Heat-induced expression and chemically induced expression of the Escherichia coli stress protein HtpG are affected by the growth environment. Appl Environ Microbiol 65: 3433-3440
30. Mazzarella RA, Green M (1987) ERp99, an abundant conserved glycoprotein of the endoplasmic reticulum, is homologous to the 90-kDa heat shock protein (hsp90) and the 94-kDa glucose regulated protein (GRP94). J Biol Chem 262: 8875-8883
31. Melnick J, Aviel S, Argon Y (1992) The endoplasmic reticulum stress protein GRP94, in addition to BiP, associates with unassembled immunoglobulin chains. J Biol Chem 267: 21303-21306
32. Meunier L, Usherwood YK, Chung KT, Hendershot LM (2002) A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol Biol Cell 13: 4456-4469
33. Meyer P, Prodromou C, Hu B, Vaughan C, Roe SM, Panaretou B, Piper PW, Pearl LH (2003) Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions. Mol Cell 11: 647-658
34. Minami Y, Kimura Y, Kawasaki H, Suzuki K, Yahara I (1994) The carboxy-terminal region of mammalian HSP90 is required for its dimerization and function in vivo. Mol Cell Biol 14: 1459-1464
35. Morishima Y, Kanelakis KC, Silverstein AM, Dittmar KD, Estrada L, Pratt WB (2000) The Hsp organizer protein hop enhances the rate of but is not essential for glucocorticoid receptor folding by the multiprotein Hsp90-based chaperone system. J Biol Chem 275: 6894-6900
36. Morita T, Yamaguchi H, Amagai A, Maeda Y (2005) Involvement of the TPNAP-1 homologue, Dd-TEAP1, in spore differentiation during Dictyostelium development. Exp Cell Res 303: 425-431
37. Nathan DF, Lindquist S (1995) Mutational analysis of Hsp90 function: interactions with a steroid receptor and a protein kinase. Mol Cell Biol 15: 3917-3925
38. Panaretou B, Prodromou C, Roe SM, O'Brien R, Ladbury JE, Piper PW, Pearl LH (1998) ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J 17: 4829-4836
39. Panaretou B, Siligardi G, Meyer P, Maloney A, Sullivan JK, Singh S, Millson SH, Clarke PA, Naaby-Hansen S, Stein R, et al (2002) Activation of the ATPase activity of Hsp90 by the stress-regulated cochaperone Aha1. Mol Cell 10: 1307-1318
40. 6f complex from Chlamydomonas reinhardtii. C R Acad Sci Ser III Sci Vie 316: 1404-1409
41. Popov N, Schmitt S, Matthies H (1975) Eine störungsfreie Mikromethode zur Bestimmung des Proteingehalts in Gewebshomogenaten. Acta Biol Germ 34: 1441-1446
42. Pratt WB, Toft DO (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med 228: 111-133
43. Prodromou C, Panaretou B, Chohan S, Siligardi G, O'Brian R, Ladburry JE, Roe SM, Piper PW, Pearl LH (2000) The ATPase cycle of Hsp90 drives a molecular "clamp(Graph Presented) via transient dimerisation of the N-terminal domains. EMBO J 19: 4333-4392
44. Prodromou C, Roe SM, O'Brien O, Ladbury JE, Piper PW, Pearl LH (1997) Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90: 65-75
45. Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417: 618-624
46. Richter K, Buchner J (2001) Hsp90: chaperoning signal transduction. J Cell Physiol 188: 281-290
47. Roe SM, Prodromou C, O'Brien R, Ladbury JE, Piper PW, Pearl LH (1999) Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. J Med Chem 42: 260-266
48. Rowley N, Prip-Buus C, Westermann B, Brown C, Schwarz E, Barrell B, Neupert W (1994) Mdj1p, a novel chaperone of the DnaJ family, is involved in mitochondrial biogenesis and protein folding. Cell 77: 249-259
49. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342
50. Ryan MT, Voos W, Pfanner N (2001) Assaying protein import into mitochondria. Methods Cell Biol 65: 189-215
51. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
52. Schägger H, Cramer WA, von Jagow G (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal Biochem 217: 220-230
53. Schlicher T, Soll J (1997) Chloroplastic isoforms of DnaJ and GrpE in pea. Plant Mol Biol 33: 181-185
54. Schmitz G, Schmidt M, Feierabend J (1996) Characterization of a plastid-specific HSP90 homologue: identification of a cDNA sequence, phylogenetic descendence and analysis of its mRNA and protein expression. Plant Mol Biol 30: 479-492
55. Schroda M (2004) The Chlamydomonas genome reveals its secrets: chaperone genes and the potential roles of their gene products in the chloroplast. Photosynth Res 82: 221-240
56. Schroda M, Vallon O, Whitelegge JP, Beck CF, Wollman F-A (2001) The chloroplastic GrpE homolog of Chlamydomonas: two isoforms generated by differential splicing. Plant Cell 13: 2823-2839
57. Schroda M, Vallon O, Wollman F-A, Beck CF (1999) Achloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell 11: 1165-1178
58. Schulte TW, Akinaga S, Soga S, Sullivan W, Stensgard B, Toft D, Neckers LM (1998) Antibiotic radicicol binds to the N-terminal domain of Hsp90 and shares important biologic activities with geldanamycin. Cell Stress Chaperones 3: 100-108
59. Sharma SV, Agatsuma T, Nakano H (1998) Targeting of the protein chaperone, HSP90, by the transformation suppressing agent, radicicol. Oncogene 16: 2639-2645
60. Shrager J, Hauser C, Chang CW, Harris EH, Davies J, McDermott J, Tamse R, Zhang Z, Grossman AR (2003) The Chlamydomonas reinhardtii genome project. A guide to the generation and use of the cDNA information. Plant Physiol 131: 401-408
61. Smith DF, Sullivan WP, Marion TN, Zaitsu K, Madden B, McCormick DJ, Toft DO (1993) Identification of a 60-kilodalton stress-related protein, p60, which interacts with hsp90 and hsp70. Mol Cell Biol 13: 869-876
62. Stancato LF, Chow YH, Hutchison KA, Perdew GH, Jove R, Pratt WB (1993) Raf exists in a native heterocomplex with hsp90 and p50 that can be reconstituted in a cell-free system. J Biol Chem 268: 21711-21716
63. Stancato LF, Hutchison KA, Krishna P, Pratt WB (1996) Animal and plant cell lysates share a conserved chaperone system that assembles the glucocorticoid receptor into a functional heterocomplex with hsp90. Biochemistry 35: 554-561
64. Stechmann A, Cavalier-Smith T (2004) Evolutionary origins of Hsp90 chaperones and a deep paralogy in their bacterial ancestors. J Eukaryot Microbiol 51: 364-373
65. Stewart S, Sundaram M, Zhang Y, Lee J, Han M, Guan KL (1999) Kinase suppressor of Ras forms a multiprotein signaling complex and modulates MEK localization. Mol Cell Biol 19: 5523-5534
66. Von Kampen J, Nieländer U, von Wettern M (1994) Stress-dependent transcription of a gene encoding a Gb-like polypeptide from Chlamydomonas reinhnrdtii. J Plant Physiol 143: 756-758
67. Wearsch PA, Nicchitta CV (1996) Purification and partial molecular characterization of GEP94, an ER resident chaperone. Protein Expr Purif 7: 114-121
68. Wegele H, Müller L, Buchner J (2004) Hsp70 and Hsp90-a relay team for protein folding. Rev Physiol Biochem Pharmacol 151: 1-44
69. Welch WJ, Feramisco JR (1982) Purification of the major mammalian heat shock proteins. J Biol Chem 257: 14949-14959
70. Young JC, Moarefi I, Hartl FU (2001) Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154: 267-273
71. Zerges W, Rochaix J-D (1998) Low density membranes are associated with RNA-binding proteins and thylakoids in the chloroplast of Chlamydomonas reinhardtii. J Cell Biol 140: 101-110