The HSP90 complex of plants

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 3, 2012, Pages 689-697

  Kadota, Yasuhiro ^a   Shirasu, Ken ^a  

^a RIKEN Center for Sustainable Resource Science   (Japan)

Author keywords

Disease resistance; HSP90; Innate immunity; Molecular chaperone; NLR protein; Protein structure

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; AHA1 PROTEIN; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CELL CYCLE PROTEIN 37; CHITIN ELICITOR RECEPTOR KINASE1; CHLORATE; CRYOPYRIN; CYCLOPHILIN; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; MELUSIN; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PROTEIN P23; RAR1 PROTEIN; SACCHAROMYCES CEREVISIAE CYCLOPHILIN 6; SGT1 PROTEIN; SUPPRESSOR OF KINETOCHORE PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARABIDOPSIS; CHLOROPLAST; CONFORMATION; ENZYME ACTIVITY; EUKARYOTE; HEAT STRESS; HYDROGEN BOND; HYDROLYSIS; ISOTHERMAL TITRATION CALORIMETRY; MITOCHONDRION; NONHUMAN; PLANT; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; RNA CONFORMATION; SIGNAL TRANSDUCTION; STOICHIOMETRY;

HSP90 HEAT-SHOCK PROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PLANT PROTEINS; PLANTS; STRUCTURE-ACTIVITY RELATIONSHIP;

EUKARYOTA;

EID: 84857063270     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.09.016     Document Type: Review

References (85)

1. Pearl L.H., Prodromou C. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 2006, 75:271-294.
2. Krishna P., Gloor G. The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 2001, 6:238-246.
3. Hubert D.A., He Y., McNulty B.C., Tornero P., Dangl J.L. Specific Arabidopsis HSP90.2 alleles recapitulate RAR1 cochaperone function in plant NB-LRR disease resistance protein regulation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9556-9563.
4. Ali M.M., Roe S.M., Vaughan C.K., Meyer P., Panaretou B., Piper P.W., Prodromou C., Pearl L.H. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 2006, 440:1013-1017.
5. Prodromou C., Siligardi G., O'Brien R., Woolfson D.N., Regan L., Panaretou B., Ladbury J.E., Piper P.W., Pearl L.H. Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO J. 1999, 18:754-762.
6. 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.
7. Siligardi G., Panaretou B., Meyer P., Singh S., Woolfson D.N., Piper P.W., Pearl L.H., Prodromou C. Regulation of Hsp90 ATPase activity by the co-chaperone Cdc37p/p50cdc37. J. Biol. Chem. 2002, 277:20151-20159.
8. Johnson J.L., Toft D.O. A novel chaperone complex for steroid receptors involving heat shock proteins, immunophilins, and p23. J. Biol. Chem. 1994, 269:24989-24993.
9. Panaretou B., Siligardi G., Meyer P., Maloney A., Sullivan J.K., Singh S., Millson S.H., Clarke P.A., Naaby-Hansen S., Stein R., Cramer R., Mollapour M., Workman P., Piper P.W., Pearl L.H., Prodromou C. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol. Cell. 2002, 10:1307-1318.
10. Zhang Z., Sullivan W., Felts S.J., Prasad B.D., Toft D.O., Krishna P. Characterization of plant p23-like proteins for their co-chaperone activities. Cell Stress Chaperones 2010, 15:703-715.
11. Kadota Y., Amigues B., Ducassou L., Madaoui H., Ochsenbein F., Guerois R., Shirasu K. Structural and functional analysis of SGT1-HSP90 core complex required for innate immunity in plants. EMBO Rep. 2008, 9:1209-1215.
12. Kurek I., Harvey A.J., Lonsdale D.M., Breiman A. Isolation and characterization of the wheat prolyl isomerase FK506-binding protein (FKBP) 73 promoter. Plant Mol. Biol. 2000, 42:489-497.
13. Aviezer-Hagai K., Skovorodnikova J., Galigniana M., Farchi-Pisanty O., Maayan E., Bocovza S., Efrat Y., von Koskull-Doring P., Ohad N., Breiman A. Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol. Biol. 2007, 63:237-255.
14. Meiri D., Breiman A. Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J. 2009, 59:387-399.
15. de la Fuente van Bentem S., Vossen J.H., de Vries K.J., van Wees S., Tameling W.I., Dekker H.L., de Koster C.G., Haring M.A., Takken F.L., Cornelissen B.J. Heat shock protein 90 and its co-chaperone protein phosphatase 5 interact with distinct regions of the tomato I-2 disease resistance protein. Plant J. 2005, 43:284-298.
16. Chen L., Hamada S., Fujiwara M., Zhu T., Thao N.P., Wong H.L., Krishna P., Ueda T., Kaku H., Shibuya N., Kawasaki T., Shimamoto K. The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host Microbe 2010, 7:185-196.
17. Cao D., Froehlich J.E., Zhang H., Cheng C.L. The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90. Plant J. 2003, 33:107-118.
18. Ishiguro S., Watanabe Y., Ito N., Nonaka H., Takeda N., Sakai T., Kanaya H., Okada K. SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins. EMBO J. 2002, 21:898-908.
19. Queitsch C., Sangster T.A., Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature 2002, 417:618-624.
20. Sangster T.A., Salathia N., Lee H.N., Watanabe E., Schellenberg K., Morneau K., Wang H., Undurraga S., Queitsch C., Lindquist S. HSP90-buffered genetic variation is common in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:2969-2974.
21. Sangster T.A., Salathia N., Undurraga S., Milo R., Schellenberg K., Lindquist S., Queitsch C. HSP90 affects the expression of genetic variation and developmental stability in quantitative traits. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:2963-2968.
22. Sangster T.A., Bahrami A., Wilczek A., Watanabe E., Schellenberg K., McLellan C., Kelley A., Kong S.W., Queitsch C., Lindquist S. Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS One 2007, 2:e648.
23. Hahn A., Bublak D., Schleiff E., Scharf K.D. Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 2011, 23:741-755.
24. Baniwal S.K., Bharti K., Chan K.Y., Fauth M., Ganguli A., Kotak S., Mishra S.K., Nover L., Port M., Scharf K.-D., Tripp J., Weber C., Zielinski D., von Koskull-Doring P. Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J. Biosci. 2004, 29:471-487.
25. Scharf K.D., Heider H., Hohfeld I., Lyck R., Schmidt E., Nover L. The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol. Cell. Biol. 1998, 18:2240-2251.
26. Heerklotz D., Doring P., Bonzelius F., Winkelhaus S., Nover L. The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HsfA2. Mol. Cell. Biol. 2001, 21:1759-1768.
27. Hahn A., Bublak D., Schleiff E., Scharf K.-D. Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 2011, 23:741-755.
28. Ishii K.J., Koyama S., Nakagawa A., Coban C., Akira S. Host innate immune receptors and beyond: making sense of microbial infections. Cell Host Microbe 2008, 3:352-363.
29. Shirasu K. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu. Rev. Plant Biol. 2009, 60:139-164.
30. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
31. Block A., Li G., Fu Z.Q., Alfano J.R. Phytopathogen type III effector weaponry and their plant targets. Curr. Opin. Plant Biol. 2008, 11:396-403.
32. Azevedo C., Sadanandom A., Kitagawa K., Freialdenhoven A., Shirasu K., Schulze-Lefert P. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 2002, 295:2073-2076.
33. Shirasu K., Lahaye T., Tan M.W., Zhou F., Azevedo C., Schulze-Lefert P. A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 1999, 99:355-366.
34. Takahashi A., Casais C., Ichimura K., Shirasu K. HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:11777-11782.
35. Austin M.J., Muskett P., Kahn K., Feys B.J., Jones J.D., Parker J.E. Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 2002, 295:2077-2080.
36. Hubert D.A., Tornero P., Belkhadir Y., Krishna P., Takahashi A., Shirasu K., Dangl J.L. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J. 2003, 22:5679-5689.
37. Boter M., Amigues B., Peart J., Breuer C., Kadota Y., Casais C., Moore G., Kleanthous C., Ochsenbein F., Shirasu K., Guerois R. 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, 19:3791-3804.
38. Zhang M., Kadota Y., Prodromou C., Shirasu K., Pearl L.H. Structural basis for assembly of Hsp90-Sgt1-CHORD protein complexes: implications for chaperoning of NLR innate immunity receptors. Mol. Cell. 2010, 39:269-281.
39. Franchi L., Warner N., Viani K., Nunez G. Function of Nod-like receptors in microbial recognition and host defense. Immunol. Rev. 2009, 227:106-128.
40. Martinon F., Mayor A., Tschopp J. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 2009, 27:229-265.
41. Liu Y., Burch-Smith T., Schiff M., Feng S., Dinesh-Kumar S.P. Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J. Biol. Chem. 2004, 279:2101-2108.
42. Bieri S., Mauch S., Shen Q.H., Peart J., Devoto A., Casais C., Ceron F., Schulze S., Steinbiss H.H., Shirasu K., Schulze-Lefert P. RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance. Plant Cell 2004, 16:3480-3495.
43. Leister R.T., Dahlbeck D., Day B., Li Y., Chesnokova O., Staskawicz B.J. Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in Nicotiana benthamiana. Plant Cell 2005, 17:1268-1278.
44. Hein I., Barciszewska-Pacak M., Hrubikova K., Williamson S., Dinesen M., Soenderby I.E., Sundar S., Jarmolowski A., Shirasu K., Lacomme C. Virus-induced gene silencing-based functional characterization of genes associated with powdery mildew resistance in barley. Plant Physiol. 2005, 138:2155-2164.
45. Lu R., Malcuit I., Moffett P., Ruiz M.T., Peart J., Wu A.J., Rathjen J.P., Bendahmane A., Day L., Baulcombe D.C. High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J. 2003, 22:5690-5699.
46. Bhattarai K.K., Li Q., Liu Y., Dinesh-Kumar S.P., Kaloshian I. The MI-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol. 2007, 144:312-323.
47. Kanzaki H., Saitoh H., Ito A., Fujisawa S., Kamoun S., Katou S., Yoshioka H., Terauchi R. Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol. Plant Pathol. 2003, 4:383-391.
48. Liu Y., Schiff M., Marathe R., Dinesh-Kumar S.P. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 2002, 30:415-429.
49. Azevedo C., Betsuyaku S., Peart J., Takahashi A., Noel L., Sadanandom A., Casais C., Parker J., Shirasu K. Role of SGT1 in resistance protein accumulation in plant immunity. EMBO J. 2006, 25:2007-2016.
50. Holt B.F., Belkhadir Y., Dangl J.L. Antagonistic control of disease resistance protein stability in the plant immune system. Science 2005, 309:929-932.
51. Kadota Y., Shirasu K., Guerois R. NLR sensors meet at the SGT1-HSP90 crossroad. Trends Biochem. Sci. 2010, 35:199-207.
52. Peart J.R., Lu R., Sadanandom A., Malcuit I., Moffett P., Brice D.C., Schauser L., Jaggard D.A., Xiao S., Coleman M.J., Dow M., Jones J.D., Shirasu K., Baulcombe D.C. Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10865-10869.
53. Kitagawa K., Skowyra D., Elledge S.J., Harper J.W., Hieter P. SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol. Cell. 1999, 4:21-33.
54. Dubacq C., Guerois R., Courbeyrette R., Kitagawa K., Mann C. Sgt1p contributes to cyclic AMP pathway activity and physically interacts with the adenylyl cyclase Cyr1p/Cdc35p in budding yeast. Eukaryot. Cell 2002, 1:568-582.
55. Steensgaard P., Garre M., Muradore I., Transidico P., Nigg E.A., Kitagawa K., Earnshaw W.C., Faretta M., Musacchio A. Sgt1 is required for human kinetochore assembly. EMBO Rep. 2004, 5:626-631.
56. Martins T., Maia A.F., Steffensen S., Sunkel C.E. Sgt1, a co-chaperone of Hsp90 stabilizes Polo and is required for centrosome organization. EMBO J. 2009, 28:234-247.
57. Chen S., Sullivan W.P., Toft D.O., Smith D.F. Differential interactions of p23 and the TPR-containing proteins Hop, Cyp40, FKBP52 and FKBP51 with Hsp90 mutants. Cell Stress Chaperones 1998, 3:118-129.
58. Lee Y.T., Jacob J., Michowski W., Nowotny M., Kuznicki J., Chazin W.J. Human Sgt1 binds HSP90 through the CHORD-Sgt1 domain and not the tetratricopeptide repeat domain. J. Biol. Chem. 2004, 279:16511-16517.
59. Bansal P.K., Nourse A., Abdulle R., Kitagawa K. Sgt1 dimerization is required for yeast kinetochore assembly. J. Biol. Chem. 2009, 284:3586-3592.
60. Nyarko A., Mosbahi K., Rowe A.J., Leech A., Boter M., Shirasu K., Kleanthous C. TPR-mediated self-association of plant SGT1. Biochemistry 2007, 46:11331-11341.
61. da Silva Correia J., Miranda Y., Leonard N., Ulevitch R. SGT1 is essential for Nod1 activation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6764-6769.
62. Mayor A., Martinon F., De Smedt T., Petrilli V., Tschopp J. A crucial function of SGT1 and HSP90 in inflammasome activity links mammalian and plant innate immune responses. Nat. Immunol. 2007, 8:497-503.
63. Liu Y., Schiff M., Serino G., Deng X.W., Dinesh-Kumar S.P. Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to Tobacco mosaic virus. Plant Cell 2002, 14:1483-1496.
64. Hahn J.S. Regulation of Nod1 by Hsp90 chaperone complex. FEBS Lett. 2005, 579:4513-4519.
65. Sbroggio M., Ferretti R., Percivalle E., Gutkowska M., Zylicz A., Michowski W., Kuznicki J., Accornero F., Pacchioni B., Lanfranchi G., Hamm J., Turco E., Silengo L., Tarone G., Brancaccio M. The mammalian CHORD-containing protein melusin is a stress response protein interacting with Hsp90 and Sgt1. FEBS Lett. 2008, 582:1788-1794.
66. Brancaccio M., Fratta L., Notte A., Hirsch E., Poulet R., Guazzone S., De Acetis M., Vecchione C., Marino G., Altruda F., Silengo L., Tarone G., Lembo G. Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat. Med. 2003, 9:68-75.
67. Zhang M., Boter M., Li K., Kadota Y., Panaretou B., Prodromou C., Shirasu K., Pearl L.H. Structural and functional coupling of Hsp90- and Sgt1-centred multi-protein complexes. EMBO J. 2008, 27:2789-2798.
68. Karagoz G.E., Duarte A.M., Ippel H., Uetrecht C., Sinnige T., van Rosmalen M., Hausmann J., Heck A.J., Boelens R., Rudiger S.G. N-terminal domain of human Hsp90 triggers binding to the cochaperone p23. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:580-585.
69. Siligardi G., Hu B., Panaretou B., Piper P.W., Pearl L.H., Prodromou C. Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle. J. Biol. Chem. 2004, 279:51989-51998.
70. Sullivan W., Stensgard B., Caucutt G., Bartha B., McMahon N., Alnemri E.S., Litwack G., Toft D. Nucleotides and two functional states of hsp90. J. Biol. Chem. 1997, 272:8007-8012.
71. Catlett M.G., Kaplan K.B. Sgt1p is a unique co-chaperone that acts as a client adaptor to link Hsp90 to Skp1p. J. Biol. Chem. 2006, 281:33739-33748.
72. Prodromou C., Roe S.M., Piper P.W., Pearl L.H. A molecular clamp in the crystal structure of the N-terminal domain of the yeast Hsp90 chaperone. Nat. Struct. Biol. 1997, 4:477-482.
73. Noel L.D., Cagna G., Stuttmann J., Wirthmuller L., Betsuyaku S., Witte C.P., Bhat R., Pochon N., Colby T., Parker J.E. Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 2007, 19:4061-4076.
74. Spiechowicz M., Zylicz A., Bieganowski P., Kuznicki J., Filipek A. Hsp70 is a new target of Sgt1-an interaction modulated by S100A6. Biochem. Biophys. Res. Commun. 2007, 357:1148-1153.
75. Van Ooijen G., Lukasik E., Van Den Burg H.A., Vossen J.H., Cornelissen B.J., Takken F.L. The small heat shock protein 20 RSI2 interacts with and is required for stability and function of tomato resistance protein I-2. Plant J. 2010, 63:563-572.
76. Mickler M., Hessling M., Ratzke C., Buchner J., Hugel T. The large conformational changes of Hsp90 are only weakly coupled to ATP hydrolysis. Nat. Struct. Mol. Biol. 2009, 16:281-286.
77. Hessling M., Richter K., Buchner J. Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90. Nat. Struct. Mol. Biol. 2009, 16:287-293.
78. Moffett P., Farnham G., Peart J., Baulcombe D.C. Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J. 2002, 21:4511-4519.
79. Rairdan G.J., Collier S.M., Sacco M.A., Baldwin T.T., Boettrich T., Moffett P. The coiled-coil and nucleotide binding domains of the Potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell 2008, 20:739-751.
80. Tanabe T., Chamaillard M., Ogura Y., Zhu L., Qiu S., Masumoto J., Ghosh P., Moran A., Predergast M.M., Tromp G., Williams C.J., Inohara N., Nunez G. Regulatory regions and critical residues of NOD2 involved in muramyl dipeptide recognition. EMBO J. 2004, 23:1587-1597.
81. 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.
82. van Ooijen G., van den Burg H.A., Cornelissen B.J., Takken F.L. Structure and function of resistance proteins in solanaceous plants. Annu. Rev. Phytopathol. 2007, 45:43-72.
83. Y.T. Cheng, Y. Li, S. Huang, Y. Huang, X. Dong, Y. Zhang, X. Li, Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proc. Natl. Acad. Sci. U. S. A. 108 (2011) 14694-14699.
84. Li Y., Li S., Bi D., Cheng Y.T., Li X., Zhang Y. SRFR1 negatively regulates plant NB-LRR resistance protein accumulation to prevent autoimmunity. PLoS Pathog. 2010, 6:e1001111.
85. Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., Pearl L.H. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 1997, 90:65-75.