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PMID: 18368500 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Complexity of Hsp90 in organelle targeting.

Plant molecular biology ·Vol. 67 ·No. 4 ·2008-07-00 ·Pages 323-34

Prassinos C, Haralampidis K, Milioni D, Samakovli D, Krambis K, Hatzopoulos P

Abstract

Heat shock protein 90 (Hsp90) is an abundant and highly conserved molecular chaperone. In Arabidopsis, the Hsp90 gene family consists of seven members. Here, we report that the AtHsp90-6 gene gives rise to two mRNA populations, termed AtHsp90-6L and AtHsp90-6S due to alternative initiation of transcription. The AtHsp90-6L and AtHsp90-6S transcription start sites are located 228 nucleotides upstream and 124 nucleotides downstream of the annotated translation start site, respectively. Both transcripts are detected under normal or heat-shock conditions. The inducibility of AtHsp90-6 mRNAs by heat shock implies a potential role of both isoforms in stress management. Stable transformation experiments with fusion constructs between the N-terminal part of each AtHsp90-6 isoform and green fluorescent protein indicated import of both fusion proteins into mitochondria. In planta investigation confirmed that fusion of the AtHsp90-5 N-terminus to green fluorescent protein (GFP) did result in specific chloroplastic localization. The mechanisms of regulation for mitochondria- and plastid-localized chaperone-encoding genes are not well understood. Future work is needed to address the possible roles of harsh environmental conditions and developmental processes on fine-tuning and compartmentalization of the AtHsp90-6L, AtHsp90-6S, and AtHsp90-5 proteins in Arabidopsis.

MeSH Terms
Alternative Splicing Amino Acid Sequence Arabidopsis/metabolism Base Sequence DNA Primers HSP90 Heat-Shock Proteins/chemistry,genetics,metabolism,physiology Microscopy, Fluorescence Molecular Sequence Data Organelles/metabolism RNA, Messenger/genetics Reverse Transcriptase Polymerase Chain Reaction Sequence Homology, Amino Acid Transcription, Genetic
Chemicals
DNA Primers HSP90 Heat-Shock Proteins RNA, Messenger
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Prassinos Constantinos
Laboratory of Molecular Biology, Agricultural Biotechnology Department, Agricultural University of Athens, Athens, Greece.
Haralampidis Kosmas
Milioni Dimitra
Samakovli Despina
Krambis Konstantinos
Hatzopoulos Polydefkis
References (54)
54 references, click to expand
  1. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  2. Hsp70 and Hsp90--a relay team for protein folding.
    Rev Physiol Biochem Pharmacol. 2004;151:1-44 PMID: 14740253
  3. Transient expression in Arabidopsis thaliana protoplasts derived from rapidly established cell suspension cultures.
    Plant Cell Rep. 1993 Mar;12(5):241-4 PMID: 24197149
  4. The specific DNA binding activity of the dioxin receptor is modulated by the 90 kd heat shock protein.
    EMBO J. 1990 Jan;9(1):69-76 PMID: 2153080
  5. The Arabidopsis PPDK gene is transcribed from two promoters to produce differentially expressed transcripts responsible for cytosolic and plastidic proteins.
    Plant Mol Biol. 2006 Oct;62(3):339-49 PMID: 16915520
  6. The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity.
    Curr Opin Plant Biol. 2005 Feb;8(1):86-92 PMID: 15653405
  7. HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11777-82 PMID: 14504384
  8. Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms.
    BMC Genomics. 2006 Jun 17;7:156 PMID: 16780600
  9. The Hsp90 family of proteins in Arabidopsis thaliana.
    Cell Stress Chaperones. 2001 Jul;6(3):238-46 PMID: 11599565
  10. The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90.
    Plant J. 2003 Jan;33(1):107-18 PMID: 12943545
  11. Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity.
    Plant Cell. 2007 Nov;19(11):3791-804 PMID: 18032631
  12. Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins.
    Plant Cell. 2004 Jan;16(1):241-56 PMID: 14671022
  13. Evolutionary origins of Hsp90 chaperones and a deep paralogy in their bacterial ancestors.
    J Eukaryot Microbiol. 2004 May-Jun;51(3):364-73 PMID: 15218707
  14. Combinatorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1 gene.
    Plant Physiol. 2002 Jul;129(3):1138-49 PMID: 12114568
  15. Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on full-length cDNA sequences.
    Nucleic Acids Res. 2004 Sep 27;32(17):5096-103 PMID: 15452276
  16. Hsp90 canalizes developmental perturbation.
    J Exp Bot. 2007;58(13):3513-24 PMID: 18057034
  17. In vivo modifications of the maize mitochondrial small heat stress protein, HSP22.
    J Biol Chem. 2001 Aug 10;276(32):29924-9 PMID: 11397800
  18. SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins.
    EMBO J. 2002 Mar 1;21(5):898-908 PMID: 11867518
  19. The J-related segment of tim44 is essential for cell viability: a mutant Tim44 remains in the mitochondrial import site, but inefficiently recruits mtHsp70 and impairs protein translocation.
    J Cell Biol. 1999 May 31;145(5):961-72 PMID: 10352014
  20. Genomic organization of hsp90 gene family in Arabidopsis.
    Plant Mol Biol. 1997 Dec;35(6):955-61 PMID: 9426614
  21. The hsp90-related protein TRAP1 is a mitochondrial protein with distinct functional properties.
    J Biol Chem. 2000 Feb 4;275(5):3305-12 PMID: 10652318
  22. Phylogenetic relationships of organellar Hsp90 homologs reveal fundamental differences to organellar Hsp70 and Hsp60 evolution.
    Gene. 2002 Oct 16;299(1-2):125-33 PMID: 12459260
  23. Heat shock protein 84 forms a complex with mutant p53 protein predominantly within a cytoplasmic compartment of the cell.
    J Biol Chem. 1996 Jun 21;271(25):15084-90 PMID: 8663025
  24. Changes in spatial and temporal localization of Dictyostelium homologues of TRAP1 and GRP94 revealed by immunoelectron microscopy.
    Exp Cell Res. 2005 Feb 15;303(2):415-24 PMID: 15652353
  25. Genomewide comparative analysis of alternative splicing in plants.
    Proc Natl Acad Sci U S A. 2006 May 2;103(18):7175-80 PMID: 16632598
  26. Tight regulation of expression of two Arabidopsis cytosolic Hsp90 genes during embryo development.
    J Exp Bot. 2005 Feb;56(412):633-44 PMID: 15582930
  27. Hsp90 as a capacitor for morphological evolution.
    Nature. 1998 Nov 26;396(6709):336-42 PMID: 9845070
  28. Common principles of protein translocation across membranes.
    Science. 1996 Mar 15;271(5255):1519-26 PMID: 8599107
  29. Differential impact of environmental stresses on the pea mitochondrial proteome.
    Mol Cell Proteomics. 2005 Aug;4(8):1122-33 PMID: 15914488
  30. Role of mitochondrial glucocorticoid receptor in glucocorticoid-induced apoptosis.
    J Exp Med. 2006 Jan 23;203(1):189-201 PMID: 16390935
  31. Hsp90: a specialized but essential protein-folding tool.
    J Cell Biol. 2001 Jul 23;154(2):267-73 PMID: 11470816
  32. Structure, function, and mechanism of the Hsp90 molecular chaperone.
    Adv Protein Chem. 2001;59:157-86 PMID: 11868271
  33. Identification of a protein with homology to hsp90 that binds the type 1 tumor necrosis factor receptor.
    J Biol Chem. 1995 Feb 24;270(8):3574-81 PMID: 7876093
  34. Immunoelectron microscopy provides evidence that tumor necrosis factor receptor-associated protein 1 (TRAP-1) is a mitochondrial protein which also localizes at specific extramitochondrial sites.
    Exp Cell Res. 2000 Oct 10;260(1):30-9 PMID: 11010808
  35. Structure and function in GroEL-mediated protein folding.
    Annu Rev Biochem. 1998;67:581-608 PMID: 9759498
  36. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes.
    Cell. 1986 Jan 31;44(2):283-92 PMID: 3943125
  37. Iron chelation study in a normal human hepatocyte cell line suggests that tumor necrosis factor receptor-associated protein 1 (TRAP1) regulates production of reactive oxygen species.
    J Cell Biochem. 2007 Feb 1;100(2):474-86 PMID: 16927372
  38. One ticket for multiple destinations: dual targeting of proteins to distinct subcellular locations.
    Curr Opin Plant Biol. 2003 Dec;6(6):589-95 PMID: 14611958
  39. Involvement of tumor necrosis factor receptor-associated protein 1 (TRAP1) in apoptosis induced by beta-hydroxyisovalerylshikonin.
    J Biol Chem. 2004 Oct 8;279(41):42503-15 PMID: 15292218
  40. Hsp90 as a capacitor of phenotypic variation.
    Nature. 2002 Jun 6;417(6889):618-24 PMID: 12050657
  41. Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae.
    Plant J. 2005 Jan;41(1):15-30 PMID: 15610346
  42. Small heat shock proteins and stress tolerance in plants.
    Biochim Biophys Acta. 2002 Aug 19;1577(1):1-9 PMID: 12151089
  43. The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts.
    Plant Cell Physiol. 2002 Jul;43(7):697-705 PMID: 12154132
  44. Molecular mechanisms of glucocorticoid action and resistance.
    J Steroid Biochem Mol Biol. 2002 Dec;83(1-5):37-48 PMID: 12650700
  45. Changes in the 5'-untranslated region of the rbcL gene accelerate transcript degradation more than 50-fold in the chloroplast of Chlamydomonas reinhardtii.
    Curr Genet. 2004 Mar;45(3):176-82 PMID: 14628153
  46. Synergistic effect of upstream sequences, CCAAT box elements, and HSE sequences for enhanced expression of chimaeric heat shock genes in transgenic tobacco.
    Mol Gen Genet. 1992 Jan;231(2):226-32 PMID: 1736093
  47. Common non-hormone binding component in non-transformed chick oviduct receptors of four steroid hormones.
    Nature. 1984 Apr 26-May 2;308(5962):850-3 PMID: 6201744
  48. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone.
    Cell. 2005 Mar 11;120(5):715-27 PMID: 15766533
  49. A mitochondrial specific stress response in mammalian cells.
    EMBO J. 2002 Sep 2;21(17):4411-9 PMID: 12198143
  50. A microarray analysis of the rice transcriptome and its comparison to Arabidopsis.
    Genome Res. 2005 Sep;15(9):1274-83 PMID: 16140994
  51. Expression of RPS4 in tobacco induces an AvrRps4-independent HR that requires EDS1, SGT1 and HSP90.
    Plant J. 2004 Oct;40(2):213-24 PMID: 15447648
  52. An additional exon of stress-inducible heat shock protein 70 gene (HSP70-1).
    Biochem Biophys Res Commun. 1999 Apr 2;257(1):193-8 PMID: 10092532
  53. The plant mitochondrial proteome.
    Trends Plant Sci. 2005 Jan;10(1):36-43 PMID: 15642522
  54. Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted three-dimensional structures, and functional implications.
    J Biol Chem. 2004 Feb 6;279(6):4768-81 PMID: 14593120
Article Info
Journal
Plant molecular biology
Abbr.
Plant Mol Biol
ISSN
0167-4412
Published
2008-07-00
Epub
2008-00-27
Pages
323-34
Language
English
Region
Netherlands
NLM ID
9106343
Subset
IM
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