Class I and II small heat shock proteins together with HSP101 protect protein translation factors during heat stress

Plant Physiology

Volumn 172, Issue 2, 2016, Pages 1221-1236

  McLoughlin, Fionn ^a,d   Basha, Eman ^b,c,e   Fowler, Mary E ^a   Kim, Minsoo ^a,b   Bordowitz, Juliana ^b,f   Katiyar Agarwal, Surekha ^b,g   Vierling, Elizabeth ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b University of Arizona   (United States)

^c TANTA UNIVERSITY   (Egypt)

^d WASHINGTON UNIVERSITY   (United States)

^e TAIF UNIVERSITY   (Saudi Arabia)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF DELHI   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR; HSP101 PROTEIN, PLANT; INITIATION FACTOR 4A; ISOPROTEIN; PLANT PROTEIN; PROTEIN BINDING; PROTEIN SUBUNIT; SMALL HEAT SHOCK PROTEIN; TRANSCRIPTION FACTOR;

ARABIDOPSIS; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETICS; HEAT; IMMUNOBLOTTING; METABOLISM; PHYSIOLOGICAL STRESS; PROTEIN SUBUNIT; RNA INTERFERENCE; SEEDLING; TANDEM MASS SPECTROMETRY; TRANSGENIC PLANT; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ARABIDOPSIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EUKARYOTIC INITIATION FACTOR-4A; GENE EXPRESSION REGULATION, PLANT; HEAT-SHOCK PROTEINS, SMALL; HOT TEMPERATURE; IMMUNOBLOTTING; PEPTIDE ELONGATION FACTORS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN SUBUNITS; RNA INTERFERENCE; SEEDLINGS; STRESS, PHYSIOLOGICAL; TANDEM MASS SPECTROMETRY; TRANSCRIPTION FACTORS;

EID: 84989287954     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00536     Document Type: Article

References (66)

1. Ahn YJ, Zimmerman JL (2006) Introduction of the carrot HSP17.7 into potato (Solanum tuberosum L.) enhances cellular membrane stability and tuberization in vitro. Plant Cell Environ 29: 95-104
2. Basha E, Jones C, Wysocki V, Vierling E (2010) Mechanistic differences between two conserved classes of small heat shock proteins found in the plant cytosol. J Biol Chem 285: 11489-11497
3. Basha E, Lee GJ, Breci LA, Hausrath AC, Buan NR, Giese KC, Vierling E (2004a) The identity of proteins associated with a small heat shock protein during heat stress in vivo indicates that these chaperones protect a wide range of cellular functions. J Biol Chem 279: 7566-7575
4. Basha E, Lee GJ, Demeler B, Vierling E (2004b) Chaperone activity of cytosolic small heat shock proteins from wheat. Eur J Biochem 271: 1426-1436
5. Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37: 106-117
6. Berkowitz O, Jost R, Pollmann S, Masle J (2008) Characterization of TCTP, the translationally controlled tumor protein, from Arabidopsis thaliana. Plant Cell 20: 3430-3447
7. Buchan JR, Yoon JH, Parker R (2011) Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J Cell Sci 124: 228-239
8. Cashikar AG, Duennwald M, Lindquist SL (2005) A chaperone pathway in protein disaggregation: Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J Biol Chem 280: 23869-23875
9. Chen Q, Vierling E (1991) Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock protein. Mol Gen Genet 228: 328
10. Cherkasov V, Grousl T, Theer P, Vainshtein Y, Glässer C, Mongis C, Kramer G, Stoecklin G, Knop M, Mogk A, et al (2015) Systemic control of protein synthesis through sequestration of translation and ribosome biogenesis factors during severe heat stress. FEBS Lett 589: 3654-3664
11. Cherkasov V, Hofmann S, Druffel-Augustin S, Mogk A, Tyedmers J, Stoecklin G, Bukau B (2013) Coordination of translational control and protein homeostasis during severe heat stress. Curr Biol 23: 2452-2462
12. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
13. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiol 133: 462-469
14. Dafny-Yelin M, Tzfira T, Vainstein A, Adam Z (2008) Non-redundant functions of sHSP-CIs in acquired thermotolerance and their role in early seed development in Arabidopsis. Plant Mol Biol 67: 363-373
15. de Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the alphacrystallin-small heat-shock protein superfamily. Int J Biol Macromol 22: 151-162
16. Delbecq SP, Klevit RE (2013) One size does not fit all: the oligomeric states of aB crystallin. FEBS Lett 587: 1073-1080
17. Derocher AE, Helm KW, Lauzon LM, Vierling E (1991) Expression of a conserved family of cytoplasmic low molecular weight heat shock proteins during heat stress and recovery. Plant Physiol 96: 1038-1047
18. Doyle SM, Genest O, Wickner S (2013) Protein rescue from aggregates by powerful molecular chaperone machines. Nat Rev Mol Cell Biol 14: 617-629
19. Faurobert M, Pelpoir E, Chaïb J (2007) Phenol extraction of proteins for proteomic studies of recalcitrant plant tissues. Methods Mol Biol 355: 9-14
20. Forreiter C, Kirschner M, Nover L (1997) Stable transformation of an Arabidopsis cell suspension culture with firefly luciferase providing a cellular system for analysis of chaperone activity in vivo. Plant Cell 9: 2171-2181
21. Franks TM, Lykke-Andersen J (2008) The control of mRNA decapping and P-body formation. Mol Cell 32: 605-615
22. Friedrich KL, Giese KC, Buan NR, Vierling E (2004) Interactions between small heat shock protein subunits and substrate in small heat shock protein-substrate complexes. J Biol Chem 279: 1080-1089
23. Ghosh S, Gepstein S, Heikkila JJ, Dumbroff EB (1988) Use of a scanning densitometer or an ELISA plate reader for measurement of nanogram amounts of protein in crude extracts from biological tissues. Anal Biochem 169: 227-233
24. Grousl T, Ivanov P, Malcova I, Pompach P, Frydlova I, Slaba R, Senohrabkova L, Novakova L, Hasek J (2013) Heat shock-induced accumulation of translation elongation and termination factors precedes assembly of stress granules in S. cerevisiae. PLoS ONE 8: e57083
25. Haslbeck M, Miess A, Stromer T, Walter S, Buchner J (2005) Disassembling protein aggregates in the yeast cytosol: the cooperation of Hsp26 with Ssa1 and Hsp104. J Biol Chem 280: 23861-23868
26. Haslbeck M, Vierling E (2015) A first line of stress defense: small heat shock proteins and their function in protein homeostasis. J Mol Biol 427: 1537-1548
27. Helm KW, Lee GJ, Vierling E (1997) Expression and native structure of cytosolic class II small heat-shock proteins. Plant Physiol 114: 1477-1485
28. Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97: 4392-4397
29. Hong SW, Vierling E (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J 27: 25-35
30. Jain S, Wheeler JR, Walters RW, Agrawal A, Barsic A, Parker R (2016) ATPase-modulated stress granules contain a diverse proteome and substructure. Cell 164: 487-498
31. Janssen GM, Möller W (1988) Kinetic studies on the role of elongation factors 1 beta and 1 gamma in protein synthesis. J Biol Chem 263: 1773-1778
32. Jiang C, Xu J, Zhang H, Zhang X, Shi J, Li M, Ming F (2009) A cytosolic class I small heat shock protein, RcHSP17.8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. Plant Cell Environ 32: 1046-1059
33. Kirschner M, Winkelhaus S, Thierfelder JM, Nover L (2000) Transient expression and heat-stress-induced co-aggregation of endogenous and heterologous small heat-stress proteins in tobacco protoplasts. Plant J 24: 397-411
34. Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10: 310-316
35. Lee GJ, Roseman AM, Saibil HR, Vierling E (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 16: 659-671
36. Lee GJ, Vierling E (2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol 122: 189-198
37. Lee U, Wie C, Escobar M, Williams B, Hong SW, Vierling E (2005) Genetic analysis reveals domain interactions of Arabidopsis Hsp100/ClpB and cooperation with the small heat shock protein chaperone system. Plant Cell 17: 559-571
38. Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20: 786-802
39. Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529: 84-87
40. Malik MK, Slovin JP, Hwang CH, Zimmerman JL (1999) Modified expression of a carrot small heat shock protein gene, hsp17. 7, results in increased or decreased thermotolerance. Plant J 20: 89-99
41. Mogk A, Schlieker C, Friedrich KL, Schönfeld HJ, Vierling E, Bukau B (2003) Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J Biol Chem 278: 31033-31042
42. Mu C, Zhang S, Yu G, Chen N, Li X, Liu H (2013) Overexpression of small heat shock protein LimHSP16.45 in Arabidopsis enhances tolerance to abiotic stresses. PLoS ONE 8: e82264
43. Nover L, Scharf KD (1997) Heat stress proteins and transcription factors. Cell Mol Life Sci 53: 80-103
44. Nover L, Scharf KD, Neumann D (1989) Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol Cell Biol 9: 1298-1308
45. Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12: 479-492
46. Rabilloud T, Carpentier G, Tarroux P (1988) Improvement and simplification of low-background silver staining of proteins by using sodium dithionite. Electrophoresis 9: 288-291
47. Rinnerthaler M, Lejskova R, Grousl T, Stradalova V, Heeren G, Richter K, Breitenbach-Koller L, Malinsky J, Hasek J, Breitenbach M (2013) Mmi1, the yeast homologue of mammalian TCTP, associates with stress granules in heat-shocked cells and modulates proteasome activity. PLoS ONE 8: e77791
48. Santhanagopalan I, Basha E, Ballard KN, Bopp NE, Vierling E (2015) Model chaperones: small heat shock proteins from plants. In RM Tanguay, LE Hightower, eds, The Big Book on Small Heat Shock Proteins. Springer International Publishing, Cham, Switzerland, pp 119-153
49. Scharf KD, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins). Cell Stress Chaperones 6: 225-237
50. Siddique M, Gernhard S, von Koskull-Döring P, Vierling E, Scharf KD (2008) The plant sHSP superfamily: five new members in Arabidopsis thaliana with unexpected properties. Cell Stress Chaperones 13: 183-197
51. Smykal P, Masin J, Hrdy I, Konopasek I, Zarsky V (2000) Chaperone activity of tobacco HSP18, a small heat-shock protein, is inhibited by ATP. Plant J 23: 703-713
52. Sun L, Liu Y, Kong X, Zhang D, Pan J, Zhou Y, Wang L, Li D, Yang X (2012) ZmHSP16.9, a cytosolic class I small heat shock protein in maize (Zea mays), confers heat tolerance in transgenic tobacco. Plant Cell Rep 31: 1473-1484
53. Tabb DL, McDonald WH, Yates JR III (2002) DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 1: 21-26
54. Takahashi T, Komeda Y (1989) Characterization of two genes encoding small heat-shock proteins in Arabidopsis thaliana. Mol Gen Genet 219: 365-372
55. Töpfer R, Matzeit V, Gronenborn B, Schell J, Steinbiss HH (1987) A set of plant expression vectors for transcriptional and translational fusions. Nucleic Acids Res 15: 5890
56. Tripp J, Mishra SK, Scharf KD (2009) Functional dissection of the cytosolic chaperone network in tomato mesophyll protoplasts. Plant Cell Environ 32: 123-133
57. van Leeuwen W, Vermeer JE, Gadella TW Jr, Munnik T (2007) Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant J 52: 1014-1026
58. van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8: 1025-1030
59. Wallace EW, Kear-Scott JL, Pilipenko EV, Schwartz MH, Laskowski PR, Rojek AE, Katanski CD, Riback JA, Dion MF, Franks AM, et al (2015) Reversible, specific, active aggregates of endogenous proteins assemble upon heat stress. Cell 162: 1286-1298
60. Walters RW, Muhlrad D, Garcia J, Parker R (2015) Differential effects of Ydj1 and Sis1 on Hsp70-mediated clearance of stress granules in Saccharomyces cerevisiae. RNA 21: 1660-1671
61. Wang AQ, Yu XH, Mao Y, Liu Y, Liu GQ, Liu YS, Niu XL (2015) Overexpression of a small heat-shock-protein gene enhances tolerance to abiotic stresses in rice. Plant Breed 134: 384-393
62. Waters ER (2013) The evolution, function, structure, and expression of the plant sHSPs. J Exp Bot 64: 391-403
63. Waters ER, Aevermann BD, Sanders-Reed Z (2008) Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperones 13: 127-142
64. Waters ER, Vierling E (1999) The diversification of plant cytosolic small heat shock proteins preceded the divergence of mosses. Mol Biol Evol 16: 127-139
65. Weber C, Nover L, Fauth M (2008) Plant stress granules and mRNA processing bodies are distinct from heat stress granules. Plant J 56: 517-530
66. Zhou Y, Chen H, Chu P, Li Y, Tan B, Ding Y, Tsang EW, Jiang L, Wu K, Huang S (2012) NnHSP17.5, a cytosolic class II small heat shock protein gene from Nelumbo nucifera, contributes to seed germination vigor and seedling thermotolerance in transgenic Arabidopsis. Plant Cell Rep 31: 379-389