|
Plant Physiol, January 2000, Vol. 122, pp. 189-198
A Small Heat Shock Protein Cooperates with Heat Shock Protein 70 Systems to Reactivate a Heat-Denatured Protein1
Garrett J.
Lee2 and
Elizabeth
Vierling*
Department of Biochemistry (G.J.L., E.V.) and Department of
Molecular and Cellular Biology (E.V.), The University of Arizona,
1007 E. Lowell Street, Tucson, Arizona 85721-0106.
Small heat shock proteins (sHsps) are
a diverse group of heat-induced proteins that are conserved in
prokaryotes and eukaryotes and are especially abundant in plants.
Recent in vitro data indicate that sHsps act as molecular chaperones to
prevent thermal aggregation of proteins by binding non-native
intermediates, which can then be refolded in an ATP-dependent fashion
by other chaperones. We used heat-denatured firefly luciferase (Luc)
bound to pea (Pisum sativum) Hsp18.1 as a model to
define the minimum chaperone system required for refolding of a
sHsp-bound substrate. Heat-denatured Luc bound to Hsp18.1 was
effectively refolded either with Hsc/Hsp70 from diverse eukaryotes plus
the DnaJ homologs Hdj1 and Ydj1 (maximum = 97% Luc reactivation
with kob = 1.0 × 10 2/min), or with prokaryotic Escherichia
coli DnaK plus DnaJ and GrpE (100% Luc reactivation,
kob = 11.3 × 10 2/min). Furthermore, we show that Hsp18.1 is more
effective in preventing Luc thermal aggregation than the Hsc70 or DnaK
systems, and that Hsp18.1 enhances the yields of refolded Luc even when other chaperones are present during heat inactivation. These findings integrate the aggregation-preventive activity of sHsps with the protein-folding activity of the Hsp70 system and define an in vitro
system for further investigation of the mechanism of sHsp action.
1
This work was supported by the National
Institutes of Health (grant no. RO1 GM42762 to E.V. and postdoctoral
fellowship no. 5F32-GM16748 to G.J.L.) and by the American Cancer
Society Faculty Research Award (no. FRA-420 to E.V.).
2
Present address: Monsanto Company, 800 N. Lindbergh Boulevard, St. Louis, MO 63167.
*
Corresponding author; e-mail vierling{at}u.arizona.edu; fax
520-621-3709.
© 2000 American Society of Plant Physiologists
This article has been cited by other articles:

|
 |

|
 |
 
P.-C. Liao, T.-P. Lin, W.-C. Lan, J.-D. Chung, and S.-Y. Hwang
Duplication of the class I cytosolic small heat shock protein gene and potential functional divergence revealed by sequence variations flanking the {alpha}-crystallin domain in the genus Rhododendron (Ericaceae)
Ann. Bot.,
November 3, 2009;
(2009)
mcp272v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. E. Perez, J. S. Hoyer, A. I. Johnson, Z. R. Moody, J. Lopez, and N. J. Kaplinsky
BOBBER1 Is a Noncanonical Arabidopsis Small Heat Shock Protein Required for Both Development and Thermotolerance
Plant Physiology,
September 1, 2009;
151(1):
241 - 252.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Cheng, E. Basha, V. H. Wysocki, and E. Vierling
Insights into Small Heat Shock Protein and Substrate Structure during Chaperone Action Derived from Hydrogen/Deuterium Exchange and Mass Spectrometry
J. Biol. Chem.,
September 26, 2008;
283(39):
26634 - 26642.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Balogi, O. Cheregi, K. C. Giese, K. Juhasz, E. Vierling, I. Vass, L. Vigh, and I. Horvath
A Mutant Small Heat Shock Protein with Increased Thylakoid Association Provides an Elevated Resistance Against UV-B Damage in Synechocystis 6803
J. Biol. Chem.,
August 22, 2008;
283(34):
22983 - 22991.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Vasquez-Robinet, S. P. Mane, A. V. Ulanov, J. I. Watkinson, V. K. Stromberg, D. De Koeyer, R. Schafleitner, D. B. Willmot, M. Bonierbale, H. J. Bohnert, et al.
Physiological and molecular adaptations to drought in Andean potato genotypes
J. Exp. Bot.,
May 1, 2008;
59(8):
2109 - 2123.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Carra, S. J. Seguin, H. Lambert, and J. Landry
HspB8 Chaperone Activity toward Poly(Q)-containing Proteins Depends on Its Association with Bag3, a Stimulator of Macroautophagy
J. Biol. Chem.,
January 18, 2008;
283(3):
1437 - 1444.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Stahl, J. Beck, and M. Nassal
Chaperones Activate Hepadnavirus Reverse Transcriptase by Transiently Exposing a C-Proximal Region in the Terminal Protein Domain That Contributes to {varepsilon} RNA Binding
J. Virol.,
December 15, 2007;
81(24):
13354 - 13364.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-C. Chang, P.-S. Huang, H.-R. Lin, and C.-H. Lu
Transactivation of Protein Expression by Rice HSP101 in Planta and Using Hsp101 as a Selection Marker for Transformation
Plant Cell Physiol.,
August 1, 2007;
48(8):
1098 - 1107.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Y. Yoo, K. Miura, J. B. Jin, J. Lee, H. C. Park, D. E. Salt, D.-J. Yun, R. A. Bressan, and P. M. Hasegawa
SIZ1 Small Ubiquitin-Like Modifier E3 Ligase Facilitates Basal Thermotolerance in Arabidopsis Independent of Salicylic Acid
Plant Physiology,
December 1, 2006;
142(4):
1548 - 1558.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Ma, M. Haslbeck, L. Babujee, O. Jahn, and S. Reumann
Identification and Characterization of a Stress-Inducible and a Constitutive Small Heat-Shock Protein Targeted to the Matrix of Plant Peroxisomes
Plant Physiology,
May 1, 2006;
141(1):
47 - 60.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. J. Gong and K. G. Golic
Loss of Hsp70 in Drosophila Is Pleiotropic, With Effects on Thermotolerance, Recovery From Heat Shock and Neurodegeneration
Genetics,
January 1, 2006;
172(1):
275 - 286.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. C. Giese, E. Basha, B. Y. Catague, and E. Vierling
Evidence for an essential function of the N terminus of a small heat shock protein in vivo, independent of in vitro chaperone activity
PNAS,
December 27, 2005;
102(52):
18896 - 18901.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Hirose, H. Tohda, Y. Giga-Hama, R. Tsushima, T. Zako, R. Iizuka, C. Pack, M. Kinjo, N. Ishii, and M. Yohda
Interaction of a Small Heat Shock Protein of the Fission Yeast, Schizosaccharomyces pombe, with a Denatured Protein at Elevated Temperature
J. Biol. Chem.,
September 23, 2005;
280(38):
32586 - 32593.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Haslbeck, A. Miess, T. Stromer, S. Walter, and J. Buchner
Disassembling Protein Aggregates in the Yeast Cytosol: THE COOPERATION OF HSP26 WITH SSA1 AND HSP104
J. Biol. Chem.,
June 24, 2005;
280(25):
23861 - 23868.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. G. Cashikar, M. Duennwald, and S. L. Lindquist
A Chaperone Pathway in Protein Disaggregation: HSP26 ALTERS THE NATURE OF PROTEIN AGGREGATES TO FACILITATE REACTIVATION BY HSP104
J. Biol. Chem.,
June 24, 2005;
280(25):
23869 - 23875.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Neta-Sharir, T. Isaacson, S. Lurie, and D. Weiss
Dual Role for Tomato Heat Shock Protein 21: Protecting Photosystem II from Oxidative Stress and Promoting Color Changes during Fruit Maturation
PLANT CELL,
June 1, 2005;
17(6):
1829 - 1838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. P. Place and G. E. Hofmann
Comparison of Hsc70 orthologs from polar and temperate notothenioid fishes: differences in prevention of aggregation and refolding of denatured proteins
Am J Physiol Regulatory Integrative Comp Physiol,
May 1, 2005;
288(5):
R1195 - R1202.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-P. Liu, S. Perrett, and J.-M. Zhou
Dimeric Trigger Factor Stably Binds Folding-competent Intermediates and Cooperates with the DnaK-DnaJ-GrpE Chaperone System to Allow Refolding
J. Biol. Chem.,
April 8, 2005;
280(14):
13315 - 13320.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Matuszewska, D. Kuczynska-Wisnik, E. Laskowska, and K. Liberek
The Small Heat Shock Protein IbpA of Escherichia coli Cooperates with IbpB in Stabilization of Thermally Aggregated Proteins in a Disaggregation Competent State
J. Biol. Chem.,
April 1, 2005;
280(13):
12292 - 12298.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T.-L. Jinn, C.-C. Chiu, W.-W. Song, Y.-M. Chen, and C.-Y. Lin
Azetidine-induced Accumulation of Class I Small Heat Shock Proteins in the Soluble Fraction Provides Thermotolerance in Soybean Seedlings
Plant Cell Physiol.,
December 15, 2004;
45(12):
1759 - 1767.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. C. Giese and E. Vierling
Mutants in a Small Heat Shock Protein That Affect the Oligomeric State: ANALYSIS AND ALLELE-SPECIFIC SUPPRESSION
J. Biol. Chem.,
July 30, 2004;
279(31):
32674 - 32683.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Basha, G. J. Lee, L. A. Breci, A. C. Hausrath, N. R. Buan, K. C. Giese, and E. Vierling
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.,
February 27, 2004;
279(9):
7566 - 7575.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. L. Friedrich, K. C. Giese, N. R. Buan, and E. Vierling
Interactions between Small Heat Shock Protein Subunits and Substrate in Small Heat Shock Protein-Substrate Complexes
J. Biol. Chem.,
January 9, 2004;
279(2):
1080 - 1089.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. I. Watkinson, A. A. Sioson, C. Vasquez-Robinet, M. Shukla, D. Kumar, M. Ellis, L. S. Heath, N. Ramakrishnan, B. Chevone, L. T. Watson, et al.
Photosynthetic Acclimation Is Reflected in Specific Patterns of Gene Expression in Drought-Stressed Loblolly Pine
Plant Physiology,
December 1, 2003;
133(4):
1702 - 1716.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
A. Mogk, C. Schlieker, K. L. Friedrich, H.-J. Schonfeld, E. Vierling, and B. Bukau
Refolding of Substrates Bound to Small Hsps Relies on a Disaggregation Reaction Mediated Most Efficiently by ClpB/DnaK
J. Biol. Chem.,
August 15, 2003;
278(33):
31033 - 31042.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S.-W. Hong, U. Lee, and E. Vierling
Arabidopsis hot Mutants Define Multiple Functions Required for Acclimation to High Temperatures
Plant Physiology,
June 1, 2003;
132(2):
757 - 767.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Stromer, M. Ehrnsperger, M. Gaestel, and J. Buchner
Analysis of the Interaction of Small Heat Shock Proteins with Unfolding Proteins
J. Biol. Chem.,
May 9, 2003;
278(20):
18015 - 18021.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. C. Giese and E. Vierling
Changes in Oligomerization Are Essential for the Chaperone Activity of a Small Heat Shock Protein in Vivo and in Vitro
J. Biol. Chem.,
November 22, 2002;
277(48):
46310 - 46318.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Sobott, J. L. P. Benesch, E. Vierling, and C. V. Robinson
Subunit Exchange of Multimeric Protein Complexes. REAL-TIME MONITORING OF SUBUNIT EXCHANGE BETWEEN SMALL HEAT SHOCK PROTEINS BY USING ELECTROSPRAY MASS SPECTROMETRY
J. Biol. Chem.,
October 4, 2002;
277(41):
38921 - 38929.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. K. Mishra, J. Tripp, S. Winkelhaus, B. Tschiersch, K. Theres, L. Nover, and K.-D. Scharf
In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato
Genes & Dev.,
June 15, 2002;
16(12):
1555 - 1567.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Kuczynska-Wisnik, S. Kcdzierska, E. Matuszewska, P. Lund, A. Taylor, B. Lipinska, and E. Laskowska
The Escherichia coli small heat-shock proteins IbpA and IbpB prevent the aggregation of endogenous proteins denatured in vivo during extreme heat shock
Microbiology,
June 1, 2002;
148(6):
1757 - 1765.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Puigderrajols, A. Jofre, G. Mir, M. Pla, D. Verdaguer, G. Huguet, and M. Molinas
Developmentally and stress-induced small heat shock proteins in cork oak somatic embryos
J. Exp. Bot.,
June 1, 2002;
53(373):
1445 - 1452.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. H. Cheong, H.-S. Chang, R. Gupta, X. Wang, T. Zhu, and S. Luan
Transcriptional Profiling Reveals Novel Interactions between Wounding, Pathogen, Abiotic Stress, and Hormonal Responses in Arabidopsis
Plant Physiology,
June 1, 2002;
129(2):
661 - 677.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Almoguera, A. Rojas, and J. Jordano
Reversible Heat-Induced Inactivation of Chimeric beta -Glucuronidase in Transgenic Plants
Plant Physiology,
May 1, 2002;
129(1):
333 - 341.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Narberhaus
{alpha}-Crystallin-Type Heat Shock Proteins: Socializing Minichaperones in the Context of a Multichaperone Network
Microbiol. Mol. Biol. Rev.,
March 1, 2002;
66(1):
64 - 93.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-H. Yeh, Y.-M. Chen, and C.-Y. Lin
Functional Regions of Rice Heat Shock Protein, Oshsp16.9, Required for Conferring Thermotolerance in Escherichia coli
Plant Physiology,
February 1, 2002;
128(2):
661 - 668.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Török, P. Goloubinoff, I. Horváth, N. M. Tsvetkova, A. Glatz, G. Balogh, V. Varvasovszki, D. A. Los, E. Vierling, J. H. Crowe, et al.
Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding
PNAS,
February 22, 2001;
(2001)
51619498.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
T. M. NOSEK, M. A. P. BROTTO, D. A. ESSIG, R. MESTRIL, R. C. CONOVER, W. H. DILLMANN, and R. C. KOLBECK
Functional properties of skeletal muscle from transgenic animals with upregulated heat shock protein 70
Physiol Genomics,
November 9, 2000;
4(1):
25 - 33.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. B. Gurley
HSP101: A Key Component for the Acquisition of Thermotolerance in Plants
PLANT CELL,
April 1, 2000;
12(4):
457 - 460.
[Full Text]
|
 |
|

|
 |

|
 |
 
Z. Torok, P. Goloubinoff, I. Horvath, N. M. Tsvetkova, A. Glatz, G. Balogh, V. Varvasovszki, D. A. Los, E. Vierling, J. H. Crowe, et al.
Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding
PNAS,
March 13, 2001;
98(6):
3098 - 3103.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|