Login Register Cart 0
Generic placeholder image

Current Proteomics

Editor-in-Chief

ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Heat Shock Factor (HSF): The Promoter of Chaperone Genes. A Mini Review

Author(s): Natália Galdi Quel and Carlos H.I. Ramos*

Volume 16, Issue 1, 2019

Page: [22 - 30] Pages: 9

DOI: 10.2174/1570164615666180713095309

Price: $65

Abstract

Protein homeostasis, or proteostasis, is required for proper cell function and thus must be under tight maintenance in all circumstances. In crowded cell conditions, protein folding is sometimes unfavorable, and this condition is worsened during stress situations. Cells cope with such stress through the use of a Protein Quality Control system, which uses molecular chaperones and heat shock proteins as its major players. This system aids with folding, avoiding misfolding and/or reversing aggregation. A pivotal regulator of the response to heat stress is Heat Shock Factor, which is recruited to the promoters of the chaperone genes, inducting their expression. This mini review aims to cover our general knowledge on the structure and function of this factor.

Keywords: Heat shock protein, homeostasis, catalysis, molecular chaperones, protein folding and misfolding, heat shock factor.

« Previous Next »
Graphical Abstract

[1]
Dodson, G. Protein folding: Deciphering the second half of the genetic code. Trends Biochem. Sci., 1991, 16, 76-77.
[2]
Ramos, C.H.I.; Ferreira, S.T. Protein folding, misfolding and aggregation: Evolving concepts and conformational diseases. Protein Pept. Lett., 2005, 12, 213-222.
[3]
Dill, K.A.; MacCallum, J.L. The protein-folding problem, 50 years on. Science, 2012, 338(6110), 1042-1046.
[4]
Baldwin, R.L.; Rose, G.D. Molten globules, entropy-driven conformational change and protein folding. Curr. Opin. Struct. Biol., 2013, 23(1), 4-10.
[5]
Huang, P.S.; Boyken, S.E.; Baker, D. The coming of age of de novo protein design. Nature, 2016, 537(7620), 320-327.
[6]
Uversky, V.N.; Fink, A.L. Conformational constraints for amyloid fibrillation: The importance of being unfolded. Biochim. Biophys. Acta, 2004, 1698(2), 131-153.
[7]
Ferreira, S.T.; Vieira, M.N.; Felice, F.G. Soluble protein oligomers as emerging toxins in Alzheimer’s and other amyloid diseases. IUBMB Life, 2007, 59(4-5), 332-345.
[8]
Eisenberg, D.; Jucker, M. The amyloid state of proteins in human diseases. Cell, 2012, 148(6), 1188-1203.
[9]
Knowles, T.P.; Vendruscolo, M.; Dobson, C.M. The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol., 2014, 15(6), 384-396.
[10]
de Oliveira, G.A.P.; Rangel, L.P.; Costa, D.C.F.; Silva, J.L. Misfolding, aggregation, and disordered segments in c-Abl and p53 in human cancer. Front. Oncol., 2015, 5, 97.
[11]
Douglas, P.M.; Summers, D.W.; Cyr, D.M. Molecular chaperones antagonize proteotoxicity by differentially modulating protein aggregation pathways. Prion, 2009, 3(2), 51-58.
[12]
Morimoto, I.R. The heat shock response: Systems biology of proteotoxic stress in aging and disease. Cold Spring Harb. Symp. Quant. Biol., 2011, 76, 91-99.
[13]
Tiroli-Cepeda, A.; Ramos, C.H.I. An overview of the role of molecular chaperones in protein homeostasis. Protein Pept. Lett., 2011, 18, 101-109.
[14]
Kim, Y.E.; Hipp, M.S.; Bracher, A.; Hayer-Hartl, M.; Hartl, F.U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem., 2013, 82, 323-355.
[15]
Dubnikov, T.; Ben-Gedalya, T.; Cohen, E. Protein quality control in health and disease. Cold Spring Harb. Perspect. Biol., 2017, 9(3), a023523.
[16]
Fink, A.L. Chaperone-mediated protein folding. Physiol. Rev., 1999, 79, 425-449.
[17]
Hartl, F.U.; Bracher, A.; Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature, 2011, 475, 324-332.
[18]
Doyle, S.M.; Genest, O.; Wickner, S. Protein rescue from aggregates by powerful molecular chaperone machines. Nat. Rev. Mol. Cell Biol., 2013, 14(10), 617-629.
[19]
Priya, S.; Sharma, S.K.; Goloubinoff, P. Molecular chaperones as enzymes that catalytically unfold misfolded polypeptides. FEBS Lett., 2013, 587, 1981-1987.
[20]
Saibil, H. Chaperone machines for protein folding, unfolding and disaggregation. Nat. Rev. Mol. Cell Biol., 2013, 14(10), 630-642.
[21]
Mokry, D.Z.; Abrahao, J.; Ramos, C.H.I. Disaggregases, molecular chaperones that resolubilize protein aggregates. Natl. Acad. Bras. Ciênc., 2015, 87(2), 1273-1292.
[22]
Lindquist, S.; Craig, E.A. The heat-shock proteins. Annu. Rev. Genet., 1988, 22, 631-677.
[23]
Bukau, B.; Horwich, A.L. The Hsp70 and Hsp60 chaperone machines. Cell, 1998, 92, 351-366.
[24]
Hartl, F.U.; Hayer-Hartl, M. Molecular chaperones in the cytosol: From nascent chain to folded protein. Science, 2002, 295, 1852-1858.
[25]
Lee, S.; Tsai, F.T.F. Molecular chaperones in protein quality control. J. Biochem. Mol. Biol., 2005, 38, 259-265.
[26]
Ramos, C.H.I. In: Protein Misfolding; O’Doherty, C.B.; Byrne, A.C., Eds.; Nova Science Publishers: New York, 2008.
[27]
Mayer, M.P. Gymnastics of molecular chaperones. Mol. Cell, 2010, 39, 321-331.
[28]
Parsell, A.D.; Kowal, A.S.; Singer, A.M.; Lindquist, S. Protein disaggregation mediated by heat-shock protein Hsp104. Nature, 1994, 372, 475-478.
[29]
Zietkiewicz, S.; Krzewska, J.; Liberek, K. Successive and synergistic action of the Hsp70 and Hsp100 chaperones in protein disaggregation. J. Biol. Chem., 2004, 279, 44376-44383.
[30]
Shorter, J. The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLoS One, 2011, 6, e26319.
[31]
Rampelt, H.; Kirstein-Miles, J.; Nillegoda, N.B.; Chi, K.; Scholz, S.R.; Morimoto, R.I.; Bukau, B. Metazoan Hsp70 machines use Hsp110 to power protein disaggregation. EMBO J., 2012, 31, 4221-4235.
[32]
Mattoo, R.U.; Sharma, S.K.; Priya, S.; Finka, A.; Goloubinoff, P. Hsp110 is a bona fide chaperone using ATP to unfold stable misfolded polypeptides and reciprocally collaborate with Hsp70 to solubilize protein aggregates. J. Biol. Chem., 2013, 288, 21399-21411.
[33]
Wegele, H.; Müller, L.; Buchner, J. Hsp70 and Hsp90-a relay team for protein folding. Rev. Physiol. Biochem. Pharmacol., 2004, 151, 1-44.
[34]
Gava, L.; Ramos, C.H.I. Human 90 kDa heat shock protein Hsp90 as a target for cancer therapeutics. Curr. Chem. Biol., 2009, 3, 330-341.
[35]
da Silva, K.P.; Borges, J.C. The molecular chaperone Hsp70 family members function by a bidirectional heterotrophic allosteric mechanism. Protein Pept. Lett., 2011, 18(2), 132-142.
[36]
da Silva, V.C.; Ramos, C.H.I. The network interaction of human 90 kDa heat shock protein Hsp90: A target for cancer therapeutics. J. Proteomics, 2012, 75, 2790-2802.
[37]
Batista, F.A.; Gava, L.M.; Pinheiro, G.M.; Ramos, C.H.; Borges, J.C. From conformation to interaction: Techniques to explore the Hsp70/Hsp90 network. Curr. Protein Pept. Sci., 2015, 16(8), 735-753.
[38]
Garrido, C.; Paul, C.; Seigneuric, R.; Kampinga, H.H. The small heat shock proteins family: The long forgotten chaperones. Int. J. Biochem. Cell Biol., 2012, 44(10), 1588-1592.
[39]
Haslbeck, M.; Vierling, E. A first line of stress defense: Small heat shock proteins and their function in protein homeostasis. J. Mol. Biol., 2015, 427(7), 1537-1548.
[40]
Morimoto, R.I. Regulation of the heat shock transcriptional response: Cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev., 1998, 12, 3788-3796.
[41]
Fujimoto, M.; Nakai, A. The heat shock factor family and adaptation to proteotoxic stress. FEBS J., 2010, 277, 4112-4125.
[42]
Anckar, J.; Sistonen, L. Regulation of HSF1 function in the heat stress response: Implications in aging and disease. Annu. Rev. Biochem., 2011, 80, 1089-1115.
[43]
Miozzo, F.; Sabéran-Djoneidi, D.; Mezger, V. HSFs, stress sensors and sculptors of transcription compartments and epigenetic landscapes. J. Mol. Biol., 2015, 427(24), 3793-3781.
[44]
Akerfelt, M.; Morimoto, R.I.; Sistonen, L. Heat shock factors: Integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell Biol., 2010, 11(8), 545-555.
[45]
Tower, J. Heat shock proteins and Drosophila aging. Exp. Geront., 2011, 46(5), 355-562.
[46]
Zuo, J.; Baler, R.; Dahl, G.; Voellmy, R. Activation of the DNA-binding ability of human heat shock transcription factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure. Mol. Cell. Biol., 1994, 14(11), 7557-7568.
[47]
Zuo, J.; Rungger, D.; Voellmy, R. Multiple layers of regulation of human heat shock transcription factor 1. Mol. Cell. Biol., 1995, 15(8), 4319-4330.
[48]
Littlefield, O.; Nelson, H.C. A new use for the “wing” of the “winged” helix-turn-helix motif in the HSF-DNA cocrystal. Nat. Struct. Mol. Biol., 1999, 6(5), 464-470.
[49]
Vuister, G.W.; Kim, S.J.; Orosz, A.; Marquardt, J.; Wu, C.; Bax, A. Solution structure of the DNA-binding domain of Drosophila heat shock transcription factor. Nat. Struct. Mol. Biol., 1994, 1(9), 605-614.
[50]
Perisic, O.; Xiao, H.; Lis, J.T. Stable binding of Drosophila heat shock factor to head-to-head and tail-to-tail repeats of a conserved 5 bp recognition unit. Cell, 1989, 59(5), 797-806.
[51]
Kroeger, P.E.; Morimoto, R.I. Selection of new HSF1 and HSF2 DNA-binding sites reveals difference in trimer cooperativity. Mol. Cell. Biol., 1994, 14(11), 7592-7603.
[52]
Xiao, H.; Perisic, O.; Lis, J.T. Cooperative binding of Drosophila heat shock factor to arrays of a conserved 5 bp unit. Cell, 1991, 64(3), 585-593.
[53]
Peteranderl, R.; Nelson, H.C.M. Trimerization of the heat shock transcription factor by a triple-stranded alpha-helical coiled-coil. Biochemistry, 1992, 31(48), 12272-12276.
[54]
Peteranderl, R.; Rabenstein, M.; Shin, Y.K.; Liu, C.W.; Wemmer, D.E.; King, D.S.; Nelson, H.C. Biochemical and biophysical characterization of the trimerization domain from the heat shock transcription factor. Biochem., 1999, 38(12), 3559-3569.
[55]
Vihervaara, A.; Sistonen, L. HSF1 at a glance. J. Cell Sci., 2014, 127(2), 261-266.
[56]
Rabindran, S.K.; Haroun, R.I.; Clos, J.; Wisniewski, J.; Wu, C. Regulation of heat shock factor trimer formation: Role of a conserved leucine zipper. Science, 1993, 259(5092), 230-234.
[57]
Green, M.; Schuetz, T.J.; Sullivan, E.K.; Kingston, R.E. A heat shock-responsive domain of human HSF1 that regulates transcription activation domain function. Mol. Cell. Biol., 1995, 15(6), 3354-3362.
[58]
Abravaya, K.; Myers, M.P.; Murphy, S.P.; Morimoto, R.I. The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev., 1992, 6(7), 1153-1164.
[59]
Shi, Y.; Mosser, D.D.; Morimoto, R.I. Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev., 1998, 12(5), 654-666.
[60]
Morimoto, R.I. Dynamic remodeling of transcription complexes by molecular chaperones. Cell, 2002, 110(3), 281-284.
[61]
Zou, J.; Guo, Y.; Guettouche, T.; Smith, D.F.; Voellmy, R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell, 1998, 94(4), 471-480.
[62]
Denegri, M.; Moralli, D.; Rocch, M.; Biggiogera, M.; Raimondi, E.; Cobianchi, F.; De Carli, L.; Riva, S.; Biamonti, G. Human chromosomes 9, 12, and 15 contain the nucleation sites of stress-induced nuclear bodies. Mol. Biol. Cell, 2002, 13(6), 2069-2079.
[63]
Jolly, C.; Konecny, L.; Grady, D.L.; Kutskova, Y.; Cotto, J.J.; Morimoto, R.I.; Vourc’h, C. In vivo binding of active heat shock transcription factor 1 to human chromosome 9 heterochromatin during stress. J. Cell Biol., 2002, 156(5), 775-781.
[64]
Baler, R. Heat shock gene regulation by nascent polypeptides and denatured proteins: Hsp70 as a potential autoregulatory factor. J. Cell Biol., 1992, 117(6), 1151-1159.
[65]
Mosser, D.D.; Duchaine, J.; Massie, B. The DNA-binding activity of the human heat shock transcription factor is regulated in vivo by hsp70. Mol. Cell. Biol., 1993, 13(9), 5427-5438.
[66]
Raychaudhuri, S.; Loew, C.; Körner, R.; Pinkert, S.; Theis, M.; Hayer-Hartl, M.; Buchholz, F.; Hartl, F.U. Interplay of acetyltransferase EP300 and the proteasome system in regulating heat shock transcription factor 1. Cell, 2014, 156, 975-985.
[67]
Mendillo, M.L.; Santagata, S.; Koeva, M. Bel,l G.W.; Hu, R.; Tamimi, R.M.; Fraenkel, E.; Ince, T.A.; Whitesell, L.; Lindquist, S. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell, 2012, 150, 549-562.
[68]
Akerfelt, M.; Trouillet, D.; Mezger, V.; Sistonen, L. Heat shock factors at a crossroad between stress and development. Ann. N. Y. Acad. Sci., 2007, 1113(1), 15-27.
[69]
Birch-Machin, I.; Gao, S.; Huen, D.; McGirr, R.; White, R.A.H.; Russell, S. Genomic analysis of heat-shock factor targets in Drosophila. Genome Biol. Evol., 2005, 6(7), R63.
[70]
Hahn, J.; Hu, Z.; Thiele, D.J.; Iyer, V.R. Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Society, 2004, 24(12), 5249-5256.
[71]
Nakai, A. Heat shock transcription factors and sensory placode development. BMB Rep., 2009, 42(10), 631-635.
[72]
Trinklein, N.D.; Murray, J.I.; Hartman, S.J.; Botstein, D.; Myers, R.M. The role of heat shock transcription factor 1 in the genome-wide regulation of the mammalian heat shock response. Mol. Biol. Cell, 2004, 15(3), 1254-1261.
[73]
Vihervaara, A.; Sergelius, C.; Vasara, J.; Blom, M.A.H.; Elsing, A.N.; Roos-Mattjus, P.; Sistonen, L. Transcriptional response to stress in the dynamic chromatin environment of cycling and mitotic cells. Proc. Nat. Acad. Sci. USA, 2013, 110(36), e3388-e3397.
[74]
Carnemolla, A.; Labbadia, J.P.; Lazell, H.; Neueder, A.; Moussaoui, S.; Bates, G.P. Contesting the dogma of an age-related heat shock response impairment: Implications for cardiac-specific age-related disorders. Hum. Mol. Gen., 2014, 23(14), 3641-3656.
[75]
Demirovic, D.; de Toda, I.M.; Nizard, C.; Rattan, S.I.S. Differential translocation of heat shock factor-1 after mild and severe stress to human skin fibroblasts undergoing aging in vitro. J. Cell Commun. Signal., 2014, 8(4), 333-339.
[76]
Gelmedin, V.; Delaney, A.; Jennelle, L.; Hawdon, J.M. Expression profile of heat shock response factors during hookworm larval activation and parasitic development. Mol. Biochem. Parasitol., 2015, 202(1), 1-14.
[77]
Hsu, A.L.; Murphy, C.T.; Kenyon, C. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science, 2003, 300(5622), 1142-1145.
[78]
Kern, A.; Ackermann, B.; Clement, A.M.; Duerk, H.; Behl, C. HSF1-controlled and age-associated chaperone capacity in neurons and muscle cells of C. elegans. PLoS One, 2010, 5(1), e8568.
[79]
Maheshwari, M.; Bhutani, S.; Das, A.; Mukherjee, R.; Sharma, A.; Kino, Y.; Nukina, N.; Jana, N.R. Dexamethasone induces heat shock response and slows down disease progression in mouse and fly models of Huntington’s disease. Hum. Mol. Gen., 2013, 23(10), 2737-2751.
[80]
Morley, J.F.; Morimoto, R.I. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol. Biol. Cell, 2004, 15(2), 657-664.
[81]
Walker, G.A.; Thompson, F.J.; Brawley, A.; Scanlon, T.; Devaney, E. Heat shock factor functions at the convergence of the stress response and developmental pathways in Caenorhabditis elegans. FASEB J., 2003, 17(13), 1960-1962.
[82]
Sorger, P.K.; Pelham, H.R. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell, 1998, 54(6), 855-864.
[83]
Hietakangas, V.; Ahlskog, J.K.; Jakobsson, A.M.; Hellesuo, M.; Sahlberg, N.M.; Holmberg, C.I.; Mikhailov, A.; Palvimo, J.J.; Pirkkala, L.; Sistonen, L. Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol., 2003, 23(8), 2953-2968.
[84]
Westerheide, S.D.; Anckar, J.; Stevens, S.M.J.; Sistonen, L.; Morimoto, R.I. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science, 2009, 323(5917), 1063-1066.
[85]
Kim, E.; Wang, B.; Sastry, N.; Nelson, P.T.; Cai, H.; Liao, F.F. NEDD4-mediated HSF1 degradation underlies α-synucleinopathy. Hum. Mol. Gen., 2016, 25(2), 211-222.
[86]
Kline, M.P.; Morimoto, R.I. Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation. Mol. Cel. Biol., 1997, 17(4), 2107-2115.
[87]
Knauf, U.; Newton, E.M.; Kyriakis, J.; Kingston, R.E. Repression of human heat shock factor 1 activity at control temperature by phosphorylation. Genes Dev., 1996, 10(21), 2782-2793.
[88]
Budzyński, M.A.; Puustinen, M.C.; Joutsen, J.; Sistonen, L. Uncoupling stress-inducible phosphorylation of heat shock factor 1 from its activation. Mol. Cell. Biol., 2015, 35(14), 2530-2540.
[89]
Geiss-Friedlander, R.; Melchior, F. Concepts in sumoylation: A decade on. Nat. Rev. Mol. Cell Biol., 2007, 8(12), 947-956.
[90]
Hietakangas, V.; Anckar, J.; Blomster, H.A.; Fujimoto, M.; Palvimo, J.J.; Nakai, A.; Sistonen, L. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc. Nat. Acad. Sci. USA, 2006, 103(1), 45-50.
[91]
Zelin, E.; Freeman, B.C. Lysine deacetylases regulate the heat shock response including the age-associated impairment of HSF1. J. Mol. Biol., 2015, 427(7), 1644-1654.
[92]
Zelin, E.; Zhang, Y.; Toogun, O.A.; Zhong, S.; Freeman, B.C. The p23 molecular chaperone and GCN5 acetylase jointly modulate protein-DNA dynamics and open chromatin status. Mol. Cell, 2012, 48(3), 459-470.
[93]
Calderwood, S.K. HSF1, a versatile factor in tumorogenesis. Curr. Mol. Med., 2012, 12(9), 1102-1107.
[94]
Ciocca, D.R.; Arrigo, A.P.; Calderwood, S.K. Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: An update. Arch. Toxicol., 2013, 87(1), 19-48.
[95]
Dai, C.; Santagata, S.; Tang, Z.; Shi, J.; Cao, J.; Kwon, H.; Bronson, R.T.; Whitesell, L.; Lindquist, S. Loss of tumor suppressor NF1 activates HSF1 to promote carcinogenesis. J. Clin. Invest., 2012, 122(10), 3742-3754.
[96]
Dai, C.; Whitesell, L.; Rogers, A.B.; Lindquist, S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell, 2007, 130(6), 1005-1018.
[97]
Santagata, S.; Mendillo, M.L.; Tang, Y.; Subramanian, A.; Perley, C.C.; Roche, S.P.; Wong, B.; Narayan, R.; Kwon, H.; Amon, A.; Golub, T.R.; Porco, J.A.J.; Whitesell, L.; Lindquist, S. Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state. Science, 2013, 341(6143), 1238303.
[98]
Vydra, N.; Toma, A.; Widlak, W. Pleiotropic role of HSF1 in neoplastic transformation. Curr. Cancer Drug Targets, 2014, 14(2), 144-155.
[99]
Kenyon, C.J. The genetics of ageing. Nature, 2010, 464(7288), 504-512.
[100]
López-Otín, C.; Blasco, M.A.; Partridge, L.; Serrano, M.; Kroemer, G. The hallmarks of aging. Cell, 2013, 153(6), 1194-1217.
[101]
Sóti, C.; Csermely, P. Molecular chaperones and the aging process. Biogerontology, 2000, 1(3), 225-233.
[102]
Labbadia, J.; Morimoto, R.I. The biology of proteostasis in aging and disease. Annu. Rev. Biochem., 2015, 84(1), 435-464.
[103]
Liang, V.; Ullrich, M.; Lam, H.; Chew, Y.L.; Banister, S.; Song, X.; Zaw, T.; Kassiou, M.; Gotz, J.; Nicholas, H.R. Altered proteostasis in aging and heat shock response in C. elegans revealed by analysis of the global and de novo synthesized proteome. Cell. Mol. Life Sci., 2014, 71(17), 3339-3361.
[104]
Ben-Zvi, A.; Miller, E.A.; Morimoto, R.I. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc. Nat. Acad. Sci. USA, 2009, 106(35), 14914-14919.
[105]
Taylor, R.C.; Dillin, A. Aging as an event of proteostasis collapse. Cold Spring Harb. Perspect. Bio., 2011, 3, a00444.
[106]
Koga, H.; Kaushik, S.; Cuervo, A.M. Protein Homeostasis and Aging: The importance of exquisite quality control. Ageing Res. Rev., 2011, 10(2), 205-215.
[107]
Chai, Y.; Koppenhafer, S.L.; Shoesmith, S.J.; Perez, M.K.; Paulson, H.L. Evidence for proteasome involvement in polyglutamine disease: Localization to nuclear inclusions in SCA3/MJD and suppression of polyglutamine aggregation in vitro. Hum. Mol. Gen., 1999, 8(4), 673-682.
[108]
Cummings, C.J.; Mancini, M.A.; Antalffy, B.; DeFranco, D.B.; Orr, H.T.; Zoghbi, H.Y. Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat. Genet., 1998, 19(2), 148-154.
[109]
Jana, N.R.; Tanaka, M.; Wang, G.H.; Nukina, N. Polyglutamine length-dependent interaction of Hsp40 and Hsp70 family chaperones with truncated N-terminal huntingtin: Their role in suppression of aggregation and cellular toxicity. Hum. Mol. Gen., 2000, 9(13), 2009-2018.
[110]
Steele, A.D.; Hutter, G.; Jackson, W.S.; Heppner, F.L.; Borkowski, A.W.; King, O.D.; Raymond, G.J.; Aguzzi, A.; Lindquist, S. Heat shock factor 1 regulates lifespan as distinct from disease onset in prion disease. Proc. Nat. Acad. Sci. USA, 2008, 105(36), 13626-13631.
[111]
Tomita, T.; Hamazaki, J.; Hirayama, S.; McBurney, M.W.; Yashiroda, H.; Murata, S. Sirt1-deficiency causes defective protein quality control. Sci. Rep., 2015, 5, 12613.

Rights & Permissions Print Cite
Article Metrics
41
2
© 2024 Bentham Science Publishers | Privacy Policy