Received date: 02 Nov 2010
Accepted date: 08 Dec 2010
Published date: 01 Aug 2011
Copyright
Heat shock proteins (Hsps) or molecular chaperones, are highly conserved protein families present in all studied organisms. Following cellular stress, the intracellular concentration of Hsps generally increases several folds. Hsps undergo ATP-driven conformational changes to stabilize unfolded proteins or unfold them for translocation across membranes or mark them for degradation. They are broadly classified in several families according to their molecular weights and functional properties. Extensive studies during the past few decades suggest that Hsps play a vital role in both normal cellular homeostasis and stress response. Hsps have been reported to interact with numerous substrates and are involved in many biological functions such as cellular communication, immune response, protein transport, apoptosis, cell cycle regulation, gametogenesis and aging. The present review attempts to provide a brief overview of various Hsps and summarizes their involvement in diverse biological activities.
Key words： heat shock protein; chaperone; chaperonin; Hsp100; Hsp90; Hsp70; Hsp60; sHsps; fertility; apoptosis; cytoskeleton
Surajit SARKAR , M. Dhruba SINGH , Renu YADAV , K. P. ARUNKUMAR , Geoffrey W. PITTMAN . Heat shock proteins: Molecules with assorted functions[J]. Frontiers in Biology, 2011 , 6(4) : 312 -327 . DOI: 10.1007/s11515-011-1080-3
| 1 |
Adams M D, Celniker S E, Holt R A, Evans C A, Gocayne J D, Amanatides P G, Scherer S E, Li P W, Hoskins R A, Galle R F, George R A, Lewis S E, Richards S, Ashburner M, Henderson S N, Sutton G G, Wortman J R, Yandell M D, Zhang Q, Chen L X, Brandon R C, Rogers Y H, Blazej R G, Champe M, Pfeiffer B D, Wan K H, Doyle C, Baxter E G, Helt G, Nelson C R, Gabor G L, Abril J F, Agbayani A, An H J, Andrews-Pfannkoch C, Baldwin D, Ballew R M, Basu A, Baxendale J, Bayraktaroglu L, Beasley E M, Beeson K Y, Benos P V, Berman B P, Bhandari D, Bolshakov S, Borkova D, Botchan M R, Bouck J, Brokstein P, Brottier P, Burtis K C, Busam D A, Butler H, Cadieu E, Center A, Chandra I, Cherry J M, Cawley S, Dahlke C, Davenport L B, Davies P, de Pablos B, Delcher A, Deng Z, Mays A D, Dew I, Dietz S M, Dodson K, Doup L E, Downes M, Dugan-Rocha S, Dunkov B C, Dunn P, Durbin K J, Evangelista C C, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian A E, Garg N S, Gelbart W M, Glasser K, Glodek A, Gong F, Gorrell J H, Gu Z, Guan P, Harris M, Harris N L, Harvey D, Heiman T J, Hernandez J R, Houck J, Hostin D, Houston K A, Howland T J, Wei M H, Ibegwam C, Jalali M, Kalush F, Karpen G H, Ke Z, Kennison J A, Ketchum K A, Kimmel B E, Kodira C D, Kraft C, Kravitz S, Kulp D, Lai Z, Lasko P, Lei Y, Levitsky A A, Li J, Li Z, Liang Y, Lin X, Liu X, Mattei B, McIntosh T C, McLeod M P, McPherson D, Merkulov G, Milshina N V, Mobarry C, Morris J, Moshrefi A, Mount S M, Moy M, Murphy B, Murphy L, Muzny D M, Nelson D L, Nelson D R, Nelson K A, Nixon K, Nusskern D R, Pacleb J M, Palazzolo M, Pittman G S, Pan S, Pollard J, Puri V, Reese M G, Reinert K, Remington K, Saunders R D, Scheeler F, Shen H, Shue B C, Sidén-Kiamos I, Simpson M, Skupski M P, Smith T, Spier E, Spradling A C, Stapleton M, Strong R, Sun E, Svirskas R, Tector C, Turner R, Venter E, Wang A H, Wang X, Wang Z Y, Wassarman D A, Weinstock G M, Weissenbach J, Williams S M, WoodageT K C, Worley D, Wu S, Yang Q A, Yao J, Ye R F, Yeh J S, Zaveri M, Zhan G, Zhang Q, Zhao L, Zheng X H, Zheng F N, Zhong W, Zhong X, Zhou S, Zhu X, Smith H O, Gibbs R A, Myers E W, Rubin G M, Venter J C, (2000). The genome sequence of Drosophila melanogaster. Science, 287(5461): 2185–2195
|
| 2 |
Ambrosio L, Schedl P (1984). Gene expression during Drosophila melanogaster oogenesis: analysis by in situ hybridization to tissue sections. Dev Biol, 105(1): 80–92
|
| 3 |
Arrigo A P, Tanguay R M (1991). Expression of heat shock proteins during development in Drosophila. Results Probl Cell Differ, 17: 106–119
|
| 4 |
Arya R, Lakhotia S C (2008). Hsp60D is essential for caspase-mediated induced apoptosis in Drosophila melanogaster. Cell Stress Chaperones, 13(4): 509–526
|
| 5 |
Arya R, Mallik M, Lakhotia S C (2007). Heat shock genes-integrating cell survival and death. J Biosci, 32(3): 595–610
|
| 6 |
Asquith K L, Baleato R M, McLaughlin E A, Nixon B, Aitken R J (2004). Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci, 117(Pt 16): 3645–3657
|
| 7 |
Baena-López L A, Alonso J, Rodriguez J, Santarén J F (2008). The expression of heat shock protein HSP60A reveals a dynamic mitochondrial pattern in Drosophila melanogaster embryos. J Proteome Res, 7(7): 2780–2788
|
| 8 |
Betrán E, Thornton K, Long M (2002). Retroposed new genes out of the X in Drosophila. Genome Res, 12(12): 1854–1859
|
| 9 |
Boilard M, Reyes-Moreno C, Lachance C, Massicotte L, Bailey J L, Sirard M A, Leclerc P (2004). Localization of the chaperone proteins GRP78 and HSP60 on the luminal surface of bovine oviduct epithelial cells and their association with spermatozoa. Biol Reprod, 71(6): 1879–1889
|
| 10 |
Bond U, Schlesinger M J (1985). Ubiquitin is a heat shock protein in chicken embryo fibroblasts. Mol Cell Biol, 5(5): 949–956
|
| 11 |
Bösl B, Grimminger V, Walter S (2005). Substrate binding to the molecular chaperone Hsp104 and its regulation by nucleotides. J Biol Chem, 280(46): 38170–38176
|
| 12 |
Bukau B, Horwich A L (1998). The Hsp70 and Hsp60 chaperone machines. Cell, 92(3): 351–366
|
| 13 |
Burmester T, Mink M, Pál M, Lászlóffy Z, Lepesant J, Maróy P (2000). Genetic and molecular analysis in the 70CD region of the third chromosome of Drosophila melanogaster. Gene, 246(1–2): 157–167
|
| 14 |
Burns R G, Surridge C D (1994). Functional role of a consensus peptide which is common to alpha-, beta-, and gamma-tubulin, to actin and centractin, to phytochrome A, and to the TCP1 alpha chaperonin protein. FEBS Lett, 347(2–3): 105–111
|
| 15 |
Candido E P (2002). The small heat shock proteins of the nematode Caenorhabditis elegans: structure, regulation and biology. Prog Mol Subcell Biol, 28: 61–78
|
| 16 |
Caplan A J (2003). What is a co-chaperone? Cell Stress Chaperones, 8(2): 105–107
|
| 18 |
Carbajal M E, Valet J P, Charest P M, Tanguay R M (1990). Purification of Drosophila hsp 83 and immunoelectron microscopic localization. Eur J Cell Biol, 52(1): 147–156
|
| 19 |
Cavanagh A C (1996). Identification of early pregnancy factor as chaperonin 10: implications for understanding its role. Rev Reprod, 1(1): 28–32
|
| 20 |
Chan H Y, Warrick J M, Andriola I, Merry D, Bonini N M (2002). Genetic modulation of polyglutamine toxicity by protein conjugation pathways in Drosophila. Hum Mol Genet, 11(23): 2895–2904
|
| 21 |
Chandrasekhar G N, Tilly K, Woolford C, Hendrix R, Georgopoulos C (1986). Purification and properties of the groES morphogenetic protein of Escherichia coli. J Biol Chem, 261(26): 12414–12419
|
| 22 |
Chen X, Sullivan D S, Huffaker T C (1994). Two yeast genes with similarity to TCP-1 are required for microtubule and actin function in vivo. Proc Natl Acad Sci USA, 91(19): 9111–9115
|
| 23 |
Chun J N, Choi B, Lee K W, Lee D J, Kang D H, Lee J Y, Song I S, Kim H I, Lee S H, Kim H S, Lee N K, Lee S Y, Lee K J, Kim J, Kang S W, Linden R (2010). Cytosolic Hsp60 is involved in the NF-kappaB-dependent survival of cancer cells via IKK regulation. PLoS ONE, 5(3): e9422
|
| 24 |
Clarke A K (1996). Variation on a theme: Combined molecular chaperone and proteolysis functions in Clp/Hsp100 proteins. J Biosci, 21(2): 161–177
|
| 25 |
Creutz C E, Liou A, Snyder S L, Brownawell A, Willison K (1994). Identification of the major chromaffin granule-binding protein, chromobindin A, as the cytosolic chaperonin CCT (chaperonin containing TCP-1). J Biol Chem, 269(51): 32035–32038
|
| 26 |
Csermely P (1997). Proteins, RNAs and chaperones in enzyme evolution: a folding perspective. Trends Biochem Sci, 22(5): 147–149
|
| 27 |
Csermely P, Kahn C R (1991). The 90-kDa heat shock protein (hsp-90) possesses an ATP binding site and autophosphorylating activity. J Biol Chem, 266(8): 4943–4950
|
| 28 |
Csermely P, Kajtár J, Hollósi M, Oikarinen J, Somogyi J (1994). The 90 kDa heat shock protein (hsp90) induces the condensation of the chromatin structure. Biochem Biophys Res Commun, 202(3): 1657–1663
|
| 29 |
Csermely P, Schnaider T, Soti C, Prohaszka Z, Nadai G (1998). The 90 kDa molecular chaperone family: Structure, function and clinical applications. A comprehensive review. J Phar Ther, 79(2): 129–168
|
| 30 |
Cutforth T, Rubin G M (1994). Mutations in Hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell, 77(7): 1027–1036
|
| 31 |
Czar M J, Owens-Grillo J K, Dittmar K D, Hutchison K A, Zacharek A M, Leach K L, Deibel M R Jr, Pratt W B (1994). Characterization of the protein-protein interactions determining the heat shock protein (hsp90.hsp70.hsp56) heterocomplex. J Biol Chem, 269(15): 11155–11161
|
| 32 |
de Graeff-Meeder E R, Voorhorst M, van Eden W, Schuurman H J, Huber J, Barkley D, Maini R N, Kuis W, Rijkers G T, Zegers B J (1990). Antibodies to the mycobacterial 65-kD heat-shock protein are reactive with synovial tissue of adjuvant arthritic rats and patients with rheumatoid arthritis and osteoarthritis. Am J Pathol, 137(5): 1013–1017
|
| 33 |
Dix D J (1997). Hsp70 expression and function during gametogenesis. Cell Stress Chaperones, 2(2): 73–77
|
| 34 |
Eddy E M (1998). HSP70-2 heat-shock protein of mouse spermatogenic cells. J Exp Zool, 282(1–2): 261–271
|
| 35 |
Ellis J (1987). Proteins as molecular chaperones. Nature, 328(6129): 378–379
|
| 36 |
Ellis R J (2005). Chaperomics: in vivo GroEL function defined. Curr Biol, 15(17): 661–663
|
| 37 |
Eskes R, Desagher S, Antonsson B, Martinou J C (2000). Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol, 20(3): 929–935
|
| 38 |
Feder M E, Hofmann G E (1999). Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol, 61(1): 243–282
|
| 39 |
Feldman D E, Frydman J (2000). Protein folding in vivo: the importance of molecular chaperones. Curr Opin Struct Biol, 10(1): 26–33
|
| 40 |
Feltham J L, Gierasch L M (2000). GroEL-substrate interactions: molding the fold, or folding the mold? Cell, 100(2): 193–196
|
| 41 |
Frees D, Chastanet A, Qazi S, Sørensen K, Hill P, Msadek T, Ingmer H (2004). Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol Microbiol, 54(5): 1445–1462
|
| 42 |
Galdiero M, de l’Ero G C, Marcatili A (1997). Cytokine and adhesion molecule expression in human monocytes and endothelial cells stimulated with bacterial heat shock proteins. Infect Immun, 65(2): 699–707
|
| 43 |
Gao Y, Thomas J O, Chow R L, Lee G H, Cowan N J (1992). A cytoplasmic chaperonin that catalyzes beta-actin folding. Cell, 69(6): 1043–1050
|
| 44 |
Garrido C, Gurbuxani S, Ravagnan L, Kroemer G (2001). Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun, 286(3): 433–442
|
| 45 |
Gerthoffer W T, Gunst S J (2001). Invited review: focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol, 91(2): 963–972
|
| 46 |
Gething M J, Sambrook J (1992). Protein folding in the cell. Nature, 355(6355): 33–45
|
| 47 |
Glass J I, Lefkowitz E J, Glass J S, Heiner C R, Chen E Y, Cassell G H (2000). The complete sequence of the mucosal pathogen Ureaplasma urealyticum. Nature, 407(6805): 757–762
|
| 48 |
Gong W J, Golic K G (2006). Loss of Hsp70 in Drosophila is pleiotropic, with effects on thermotolerance, recovery from heat shock and neurodegeneration. Genetics, 172(1): 275–286
|
| 49 |
Gozes I, Brenneman D E (1996). Activity-dependent neurotrophic factor (ADNF). An extracellular neuroprotective chaperonin? J Mol Neurosci, 7(4): 235–244
|
| 50 |
Grantham J, Ruddock L W, Roobol A, Carden M J (2002). Eukaryotic chaperonin containing T-complex polypeptide 1 interacts with filamentous actin and reduces the initial rate of actin polymerization in vitro. Cell Stress Chaperones, 7(3): 235–242
|
| 51 |
Günther E, Walter L (1994). Genetic aspects of the hsp70 multigene family in vertebrates. Experientia, 50(11–12): 987–1001
|
| 52 |
Gupta R S (1995). Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells. Mol Microbiol, 15(1): 1–11
|
| 53 |
Gupta R S, Ramachandra N B, Bowes T, Singh B (2008). Unusual cellular disposition of the mitochondrial molecular chaperones Hsp60, Hsp70 and Hsp10. Novartis Found Symp, 291: 59–68, discussion 69–73, 137–140
|
| 54 |
Gupta S, Knowlton A A (2002). Cytosolic heat shock protein 60, hypoxia, and apoptosis. Circulation, 106(21): 2727–2733
|
| 55 |
Hackett R W, Lis J T (1983). Localization of the hsp83 transcript within a 3292 nucleotide sequence from the 63B heat shock locus of D. melanogaster. Nucleic Acids Res, 11(20): 7011–7030
|
| 56 |
Hartl F U, Martin J, Neupert W (1992). Protein folding in the cell: the role of molecular chaperones Hsp70 and Hsp60. Annu Rev Biophys Biomol Struct, 21(1): 293–322
|
| 57 |
Heikkila J J (2010). Heat shock protein gene expression and function in amphibian model systems. Comp Biochem Physiol A Mol Integr Physiol, 156(1): 19–33
|
| 58 |
Hemmingsen S M (1992). What is a chaperonin? Nature, 357(6380): 650–650
|
| 59 |
Heufelder A E, Wenzel B E, Bahn R S (1992). Cell surface localization of a 72 kilodalton heat shock protein in retroocular fibroblasts from patients with Graves’ ophthalmopathy. J Clin Endocrinol Metab, 74(4): 732–736
|
| 60 |
Hightower L E, Seth S E (1994). Interactions of vertebrate Hsc70 and HSP70 with unfolded proteins and peptides. In “The Biology of Heat Shock Proteins and Molecular Chaperones”, Morimoto RI (ed), Cold Spring Harbour Lab Press, NY, 179–207
|
| 61 |
Hill J E, Penny S L, Crowell K G, Goh S H, Hemmingsen S M (2004). cpnDB: a chaperonin sequence database. Genome Res, 14(8): 1669–1675
|
| 62 |
Hixon W G, Searcy D G (1993). Cytoskeleton in the archaebacterium Thermoplasma acidophilum? Viscosity increase in soluble extracts. Biosystems, 29(2–3): 151–160
|
| 63 |
Hochstrasser M (1992). Ubiquitin and intracellular protein degradation. Curr Opin Cell Biol, 4(6): 1024–1031
|
| 64 |
Houlihan J L, Metzler J J, Blum J S (2009). HSP90alpha and HSP90beta isoforms selectively modulate MHC class II antigen presentation in B cells. J Immunol, 182(12): 7451–7458
|
| 65 |
Houry W A, Frishman D, Eckerskorn C, Lottspeich F, Hartl F U (1999). Identification of in vivo substrates of the chaperonin GroEL. Nature, 402(6758): 147–154
|
| 66 |
Hwang M, Moretti L, Lu B (2009). HSP90 inhibitors: multi-targeted antitumor effects and novel combinatorial therapeutic approaches in cancer therapy. Curr Med Chem, 16(24): 3081–3092
|
| 67 |
Inano K, Curtis S W, Korach K S, Omata S, Horigome T (1994). Heat shock protein 90 strongly stimulates the binding of purified estrogen receptor to its responsive element. J Biochem, 116(4): 759–766
|
| 68 |
Ireland R C, Berger E M (1982). Synthesis of low molecular weight heat shock peptides stimulated by ecdysterone in a cultured Drosophila cell line. Proc Natl Acad Sci USA, 79(3): 855–859
|
| 69 |
Ito H, Kamei K, Iwamoto I, Inaguma Y, Tsuzuki M, Kishikawa M, Shimada A, Hosokawa M, Kato K (2003). Hsp27 suppresses the formation of inclusion bodies induced by expression of R120G alpha B-crystallin, a cause of desmin-related myopathy. Cell Mol Life Sci, 60(6): 1217–1223
|
| 70 |
Iwasaki S, Kobayashi M, Yoda M, Sakaguchi Y, Katsuma S, Suzuki T, Tomari Y (2010). Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol Cell, 39(2): 292–299
|
| 71 |
Jakus S, Neuer A, Dieterle S, Bongiovanni A M, Witkin S S (2008). Antibody to the Chlamydia trachomatis 60 kDa heat shock protein in follicular fluid and in vitro fertilization outcome. Am J Reprod Immunol, 59(2): 85–89
|
| 72 |
Jinn T L, Chen Y M, Lin C Y (1995). Characterization and physiological function of Class I low-molecular-mass, heat-shock protein complex in soybean. Plant Physiol, 108(2): 693–701
|
| 73 |
Johnston M, Geoffroy M C, Sobala A, Hay R, Hutvagner G (2010). HSP90 protein stabilizes unloaded argonaute complexes and microscopic P-bodies in human cells. Mol Biol Cell, 21(9): 1462–1469
|
| 74 |
Jost M, Kari C, Rodeck U (2000). The EGF receptor- an essential regulator of multiple epidermal functions. Eur J Dermatol, 10(7): 505–510
|
| 75 |
Kagawa H K, Osipiuk J, Maltsev N, Overbeek R, Quaite-Randall E, Joachimiak A, Trent J D (1995). The 60 kDa heat shock proteins in the hyperthermophilic archaeon Sulfolobus shibatae. J Mol Biol, 253(5): 712–725
|
| 76 |
Kampinga H H, Craig E A (2010). The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol, 11(8): 579–592
|
| 77 |
Kappé G, Franck E, Verschuure P, Boelens W C, Leunissen J A, de Jong W W (2003). The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10. Cell Stress Chaperones, 8(1): 53–61
|
| 78 |
Katinka M D, Duprat S, Cornillot E, Méténier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, Delbac F, El Alaoui H, Peyret P, Saurin W, Gouy M, Weissenbach J, Vivarès C P (2001). Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature, 414(6862): 450–453
|
| 79 |
Kellermayer M S, Csermely P (1995). ATP induces dissociation of the 90 kDa heat shock protein (hsp90) from F-actin: interference with the binding of heavy meromyosin. Biochem Biophys Res Commun, 211(1): 166–174
|
| 80 |
Kikis E A, Gidalevitz T, Morimoto R I (2010). Protein homeostasis in models of aging and age-related conformational disease. Adv Exp Med Biol, 694: 138–159
|
| 81 |
Kitagawa M, Wada C, Yoshioka S, Yura T (1991). Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32). J Bacteriol, 173(14): 4247–4253
|
| 82 |
Kol A, Lichtman A H, Finberg R W, Libby P, Kurt-Jones E A (2000). Cutting edge: heat shock protein (HSP) 60 activates the innate immune response: CD14 is an essential receptor for HSP60 activation of mononuclear cells. J Immunol, 164(1): 13–17
|
| 83 |
Kozlova T, Perezgasga L, Reynaud E, Zurita M (1997). The Drosophila melanogaster homologue of the hsp60 gene is encoded by the essential locus l(1)10AC and is differentially expressed during fly development. Dev Genes Evol, 207(4): 253–263
|
| 84 |
Kurtz S, Rossi J, Petko L, Lindquist S (1986). An ancient developmental induction: heat-shock proteins induced in sporulation and oogensis. Science, 231(4742): 1154–1157
|
| 85 |
Lakhotia S C (2001). Heat Shock Response- Regulation and Functions of Coding and non-coding genes in Drosophila. Proc Ind Natl Acad Sci, B5:247–264.
|
| 86 |
Lakhotia S C, Singh A K (1989). A novel heat shock polypeptide in Malpighian tubule of Drosophila melanogaster. J Genet, 68(3): 129–268
|
| 87 |
Laplante A F, Moulin V, Auger F A, Landry J, Li H, Morrow G, Tanguay R M, Germain L (1998). Expression of heat shock proteins in mouse skin during wound healing. J Histochem Cytochem, 46(11): 1291–1301
|
| 88 |
Larsen J K, Yamboliev I A, Weber L A, Gerthoffer W T (1997). Phosphorylation of the 27-kDa heat shock protein via p38 MAP kinase and MAPKAP kinase in smooth muscle. Am J Physiol, 273(5 Pt 1): L930–L940
|
| 89 |
Leicht B G, Biessmann H, Palter K B, Bonner J J (1986). Small heat shock proteins of Drosophila associate with the cytoskeleton. Proc Natl Acad Sci USA, 83(1): 90–94
|
| 90 |
Leonhardt S A, Fearson K, Danese P N, Mason T L (1993). HSP78 encodes a yeast mitochondrial heat shock protein in the Clp family of ATP-dependent proteases. Mol Cell Biol, 13(10): 6304–6313
|
| 91 |
Leroux M R, Candido E P M (1997). Subunit characterization of the Caenorhabditis elegans chaperonin containing TCP-1 and expression pattern of the gene encoding CCT-1. Biochem Biophys Res Commun, 241(3): 687–692
|
| 92 |
Lewis J, Devin A, Miller A, Lin Y, Rodriguez Y, Neckers L, Liu Z G (2000). Disruption of hsp90 function results in degradation of the death domain kinase, receptor-interacting protein (RIP), and blockage of tumor necrosis factor-induced nuclear factor-kappaB activation. J Biol Chem, 275(14): 10519–10526
|
| 93 |
Lilie H, Lang K, Rudolph R, Buchner J (1993). Prolyl isomerases catalyze antibody folding in vitro. Protein Sci, 2(9): 1490–1496
|
| 94 |
Lindquist S (1980). Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev Biol, 77(2): 463–479
|
| 95 |
Lindquist S (1986). The heat-shock response. Annu Rev Biochem, 55(1): 1151–1191
|
| 96 |
Lopatin D E, Combs A, Sweier D G, Fenno J C, Dhamija S (2000). Characterization of heat-inducible expression and cloning of HtpG (Hsp90 homologue) of Porphyromonas gingivalis. Infect Immun, 68(4): 1980–1987
|
| 97 |
Matzinger P (2002). The danger model: a renewed sense of self. Science, 296(5566): 301–305
|
| 98 |
Mayer M P (2010). Gymnastics of molecular chaperones. Mol Cell, 39(3): 321–331
|
| 99 |
McDonough H, Patterson C (2003). CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones, 8(4): 303–308
|
| 100 |
McKay D B (1991). Structure of the 70-kilodalton heat-shock-related proteins. Springer Semin Immunopathol, 13(1): 1–9
|
| 101 |
Meinhardt A, Parvinen M, Bacher M, Aumüller G, Hakovirta H, Yagi A, Seitz J (1995). Expression of mitochondrial heat shock protein 60 in distinct cell types and defined stages of rat seminiferous epithelium. Biol Reprod, 52(4): 798–807
|
| 102 |
Melki R, Cowan N J (1994). Facilitated folding of actins and tubulins occurs via a nucleotide-dependent interaction between cytoplasmic chaperonin and distinctive folding intermediates. Mol Cell Biol, 14(5): 2895–2904
|
| 103 |
Michaud S, Morrow G, Marchand J, Tanguay R M (2002). Drosophila small heat shock proteins: cell and organelle-specific chaperones? Prog Mol Subcell Biol, 28: 79–101
|
| 104 |
Mikhaylova L M, Nguyen K, Nurminsky D I (2008). Analysis of the Drosophila melanogaster testes transcriptome reveals coordinate regulation of paralogous genes. Genetics, 179(1): 305–315
|
| 105 |
Miklos D, Caplan S, Mertens D, Hynes G, Pitluk Z, Kashi Y, Harrison-Lavoie K, Stevenson S, Brown C, Barrell B,
|
| 106 |
Miller S G, Leclerc R F, Erdos G W (1990). Identification and characterization of a testis-specific isoform of a chaperonin in a moth, Heliothis virescens. J Mol Biol, 214(2): 407–422
|
| 107 |
Morange M (2006). HSFs in development. Handb Exp Pharmacol, 172(172): 153–169
|
| 108 |
Morcillo G, Diez J L, Carbajal M E, Tanguay R M (1993). HSP90 associates with specific heat shock puffs (hsr omega) in polytene chromosomes of Drosophila and Chironomus. Chromosoma, 102(9): 648–659
|
| 109 |
Morrow G, Heikkila J J, Tanguay R M (2006). Differences in the chaperone-like activities of the four main small heat shock proteins of Drosophila melanogaster. Cell Stress Chaperones, 11(1): 51–60
|
| 110 |
Morrow G, Tanguay R M (2003). Heat shock proteins and aging in Drosophila melanogaster. Semin Cell Dev Biol, 14(5): 291–299
|
| 111 |
Murata S, Minami Y, Minami M, Chiba T, Tanaka K (2001). CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep, 2(12): 1133–1138
|
| 112 |
Naaby-Hansen S, Herr J C (2010). Heat shock proteins on the human sperm surface. J Reprod Immunol, 84(1): 32–40
|
| 113 |
Nakahara K, Kim K, Sciulli C, Dowd S R, Minden J S, Carthew R W (2005). Targets of microRNA regulation in the Drosophila oocyte proteome. Proc Natl Acad Sci USA, 102(34): 12023–12028
|
| 114 |
Neuer A, Lam K N, Tiller F W, Kiesel L, Witkin S S (1997). Humoral immune response to membrane components of Chlamydia trachomatis and expression of human 60 kDa heat shock protein in follicular fluid of in-vitro fertilization patients. Hum Reprod, 12(5): 925–929
|
| 115 |
Neuer A, Spandorfer S D, Giraldo P, Dieterle S, Rosenwaks Z, Witkin S (2000). The role of heat shock protein in reproduction. Hum Repro Updt, 6(2): 149–159
|
| 116 |
Nollen E A, Morimoto R I (2002). Chaperoning signaling pathways: molecular chaperones as stress-sensing ‘heat shock’ proteins. J Cell Sci, 115(Pt 14): 2809–2816
|
| 117 |
Nover L, ed. (1984). Heat Shock Response in eukaryotic cells. Springer-Verlag, Berlin, pp-1–78.
|
| 118 |
Novoselova T V, Margulis B A, Novoselov S S, Sapozhnikov A M, van der Spuy J, Cheetham M E, Guzhova I V (2005). Treatment with extracellular HSP70/HSC70 protein can reduce polyglutamine toxicity and aggregation. J Neurochem, 94(3): 597–606
|
| 119 |
Pandey P, Saleh A, Nakazawa A, Kumar S, Srinivasula S M, Kumar V, Weichselbaum R, Nalin C, Alnemri E S, Kufe D, Kharbanda S (2000). Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90. EMBO J, 19(16): 4310–4322
|
| 120 |
Paranko J, Seitz J, Meinhardt A (1996). Developmental expression of heat shock protein 60 (HSP60) in the rat testis and ovary. Differentiation, 60(3): 159–167
|
| 121 |
Parsell D A, Lindquist S (1994). Heat shock proteins and stress tolerance. In “The Biology of Heat Shock proteins and Molecular Chaperones”, Morimoto RI. (ed), Cold Spring Harbor Lab Press, NY, 457–493
|
| 122 |
Parsell D A, Sanchez Y, Stitzel J D, Lindquist S (1991). Hsp104 is a highly conserved protein with two essential nucleotide-binding sites. Nature, 353(6341): 270–273
|
| 123 |
Pauli D, Arrigo A P, Tissières A (1992). Heat shock response in Drosophila. Experientia, 48(7): 623–629
|
| 124 |
Pelham H R (1986). Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell, 46(7): 959–961
|
| 125 |
Pfister G, Stroh C M, Perschinka H, Kind M, Knoflach M, Hinterdorfer P, Wick G (2005). Detection of HSP60 on the membrane surface of stressed human endothelial cells by atomic force and confocal microscopy. J Cell Sci, 118(Pt 8): 1587–1594
|
| 126 |
Pockley A G (2002). Heat shock proteins, inflammation, and cardiovascular disease. Circulation, 105(8): 1012–1017
|
| 127 |
Pratt W B, Czar M J, Stancato L F, Owens J K (1993). The hsp56 immunophilin component of steroid receptor heterocomplexes: could this be the elusive nuclear localization signal-binding protein? J Steroid Biochem Mol Biol, 46(3): 269–279
|
| 128 |
Pratt W B, Toft D O (2003). Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood), 228(2): 111–133
|
| 129 |
Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan R C, Melton D A (2002). “Stemness”: transcriptional profiling of embryonic and adult stem cells. Science, 298(5593): 597–600
|
| 130 |
Ranford J C, Coates A R, Henderson B (2000). Chaperonins are cell-signalling proteins: the unfolding biology of molecular chaperones. Expert Rev Mol Med, 2(8): 1–17
|
| 131 |
Ranson N A, White H E, Saibil H R (1998). Chaperonins. Biochem J, 333(Pt 2): 233–242
|
| 132 |
Rassow J, Ahsen O V, Bomer U, Pfanner N (1997). Molecular chaperones: Towards a characterization of the heat-shock protein 70 family. Trends Genet, 7: 129–133
|
| 133 |
Retzlaff C, Yamamoto Y, Hoffman P S, Friedman H, Klein T W (1994). Bacterial heat shock proteins directly induce cytokine mRNA and interleukin-1 secretion in macrophage cultures. Infect Immun, 62(12): 5689–5693
|
| 134 |
Richter K, Haslbeck M, Buchner J (2010). The heat shock response: life on the verge of death. Mol Cell, 40(2): 253–266
|
| 135 |
Ritossa F A (1962). A new puffing pattern induced by a temperature shock and DNP in Drosophila. Experientia, 18(12): 571–573
|
| 136 |
Roobol A, Carden M J (1999). Subunits of the eukaryotic cytosolic chaperonin CCT do not always behave as components of a uniform hetero-oligomeric particle. Eur J Cell Biol, 78(1): 21–32
|
| 137 |
Roobol A, Holmes F E, Hayes N V L, Baines A J, Carden M J (1995). Cytoplasmic chaperonin complexes enter neurites developing in vitro and differ in subunit composition within single cells. J Cell Sci, 108(Pt 4): 1477–1488
|
| 138 |
Rubin G M, Yandell M D, Wortman J R, Gabor Miklos G L, Nelson C R, Hariharan I K, Fortini M E, Li P W, Apweiler R, Fleischmann W, Cherry J M, Henikoff S, Skupski M P, Misra S, Ashburner M, Birney E, Boguski M S, Brody T, Brokstein P, Celniker S E, Chervitz S A, Coates D, Cravchik A, Gabrielian A, Galle R F, Gelbart W M, George R A, Goldstein L S, Gong F, Guan P, Harris N L, Hay B A, Hoskins R A, Li J, Li Z, Hynes R O, Jones S J, Kuehl P M, Lemaitre B, Littleton J T, Morrison D K, Mungall C, O’Farrell P H, Pickeral O K, Shue C, Vosshall L B, Zhang J, Zhao Q, Zheng X H, Lewis S (2000). Comparative genomics of the eukaryotes. Science, 287(5461): 2204–2215
|
| 139 |
Rutherford S, Knapp J R, Csermely P (2007). Hsp90 and developmental networks. Adv Exp Med Biol, 594: 190–197
|
| 140 |
Rutherford S L (2003). Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet, 4(4): 263–274
|
| 141 |
Rutherford S L, Lindquist S (1998). Hsp90 as a capacitor for morphological evolution. Nature, 396(6709): 336–342
|
| 142 |
Saibil H (1996). The lid that shapes the pot: structure and function of the chaperonin GroES. Structure, 4(1): 1–4
|
| 143 |
Samali A, Cai J, Zhivotovsky B, Jones D P, Orrenius S (1999). Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of jurkat cells. EMBO J, 18(8): 2040–2048
|
| 144 |
Sanchez Y, Lindquist S L (1990). HSP104 required for induced thermotolerance. Science, 248(4959): 1112–1115
|
| 145 |
Sarge K D, Cullen K E (1997). Regulation of hsp expression during rodent spermatogenesis. Cell Mol Life Sci, 53(2): 191–197
|
| 146 |
Sarkar S, Arya S, Lakhotia S C (2006) Chaperonins in life and death. In: Stress response: a molecular biology approach (A.S. Sreedhar ed): Signpost Publication: Trivandrum, India (p 43–60).
|
| 147 |
Sarkar S, Lakhotia S C (2005). The Hsp60C gene in the 25F cytogenetic region in Drosophila melanogaster is essential for tracheal development and fertility. J Genet, 84(3): 265–281
|
| 148 |
Sarkar S, Lakhotia S C (2008). Hsp60C is required in follicle as well as germline cells during oogenesis in Drosophila melanogaster. Dev Dyn, 237(5): 1334–1347
|
| 149 |
Schirmer E C, Glover J R, Singer M A, Lindquist S (1996). HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci, 21(8): 289–296
|
| 150 |
Shinoda H, Huang C C (1996). Heat shock proteins in middle ear cholesteatoma. Otolaryngol Head Neck Surg, 114(1): 77–83
|
| 151 |
Singh B N, Lakhotia S C (1995). The non-induction of heat shocked Malpighian tubules of Drosophila larvae is not due to constitutive presence of hsp70 or hsc70. Curr Sci, 69: 178–182
|
| 152 |
Sjögren L L, MacDonald T M, Sutinen S, Clarke A K (2004). Inactivation of the clpC1 gene encoding a chloroplast Hsp100 molecular chaperone causes growth retardation, leaf chlorosis, lower photosynthetic activity, and a specific reduction in photosystem content. Plant Physiol, 136(4): 4114–4126
|
| 153 |
Slavotinek A M, Biesecker L G (2001). Unfolding the role of chaperones and chaperonins in human disease. Trends Genet, 17(9): 528–535
|
| 154 |
Soares H, Penque D, Mouta C, Rodrigues-Pousada C (1994). A Tetrahymena orthologue of the mouse chaperonin subunit CCT gamma and its coexpression with tubulin during cilia recovery. J Biol Chem, 269(46): 29299–29307
|
| 155 |
Sollars V, Lu X, Xiao L, Wang X, Garfinkel M D, Ruden D M (2003). Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nat Genet, 33(1): 70–74
|
| 156 |
Soltys B J, Gupta R S (1996). Immunoelectron microscopic localization of the 60-kDa heat shock chaperonin protein (Hsp60) in mammalian cells. Exp Cell Res, 222(1): 16–27
|
| 157 |
Soltys B J, Gupta R S (1999). Mitochondrial-matrix proteins at unexpected locations: are they exported? Trends Biochem Sci, 24(5): 174–177
|
| 158 |
Song H Y, Dunbar J D, Zhang Y X, Guo D, Donner D B (1995). Identification of a protein with homology to hsp90 that binds the type 1 tumor necrosis factor receptor. J Biol Chem, 270(8): 3574–3581
|
| 159 |
Soti C, Csermely P (2002). Chaperones come of age. Cell Stress Chaperones, 7(2): 186–190
|
| 160 |
Sõti C, Nagy E, Giricz Z, Vígh L, Csermely P, Ferdinandy P (2005). Heat shock proteins as emerging therapeutic targets. Br J Pharmacol, 146(6): 769–780
|
| 161 |
Southgate R, Ayme A, Voellmy R (1983). Nucleotide sequence analysis of the Drosophila small heat shock gene cluster at locus 67B. J Mol Biol, 165(1): 35–57
|
| 162 |
Spiess C, Meyer A S, Reissmann S, Frydman J (2004). Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets. Trends Cell Biol, 14(11): 598–604
|
| 163 |
Squires C L, Pedersen S, Ross B M, Squires C (1991). ClpB is the Escherichia coli heat shock protein F84.1. J Bacteriol, 173(14): 4254–4262
|
| 164 |
Srinivas U K, Revathi C J, Das M R (1987). Heat-induced expression of albumin during early stages of rat embryo development. Mol Cell Biol, 7(12): 4599–4602
|
| 165 |
Sternlicht H, Farr G W, Sternlicht M L, Driscoll J K, Willison K, Yaffe M B (1993). The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc Natl Acad Sci USA, 90(20): 9422–9426
|
| 166 |
Sun Y, MacRae T H (2005). Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci, 62(21): 2460–2476
|
| 167 |
Tabibzadeh S, Kong Q F, Satyaswaroop P G, Babaknia A (1996). Heat shock proteins in human endometrium throughout the menstrual cycle. Hum Reprod, 11(3): 633–640
|
| 168 |
Tai P K, Albers M W, Chang H, Faber L E, Schreiber S L (1992). Association of a 59-kilodalton immunophilin with the glucocorticoid receptor complex. Science, 256(5061): 1315–1318
|
| 169 |
Tai P K, Faber L E (1985). Isolation of dissimilar components of the 8.5S nonactivated uterine progestin receptor. Can J Biochem Cell Biol, 63(1): 41–49
|
| 170 |
Taipale M, Jarosz D F, Lindquist S (2010). HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol, 11(7): 515–528
|
| 171 |
Thirumalai D, Lorimer G H (2001). Chaperonin-mediated protein folding. Annu Rev Biophys Biomol Struct, 30(1): 245–269
|
| 172 |
Thornberry N A, Lazebnik Y (1998). Caspases: enemies within. Science, 281(5381): 1312–1316
|
| 173 |
Timakov B, Zhang P (2001). The hsp60B gene of Drosophila melanogaster is essential for the spermatid individualization process. Cell Stress Chaperones, 6(1): 71–77
|
| 174 |
Tissières A, Mitchell H K, Tracy U M (1974). Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J Mol Biol, 84(3): 389–398
|
| 175 |
Togo T, Dickson D W (2002). Ballooned neurons in progressive supranuclear palsy are usually due to concurrent argyrophilic grain disease. Acta Neuropathol, 104(1): 53–56
|
| 176 |
Török Z, Horváth I, Goloubinoff P, Kovács E, Glatz A, Balogh G, Vígh L (1997). Evidence for a lipochaperonin: association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. Proc Natl Acad Sci USA, 94(6): 2192–2197
|
| 177 |
Trent J D, Kagawa H K, Yaoi T, Olle E, Zaluzec N J (1997). Chaperonin filaments: the archaeal cytoskeleton? Proc Natl Acad Sci USA, 94(10): 5383–5388
|
| 178 |
Trent J D, Nimmesgern E, Wall J S, Hartl F U, Horwich A L (1991). A molecular chaperone from a thermophilic archaebacterium is related to the eukaryotic protein t-complex polypeptide-1. Nature, 354(6353): 490–493
|
| 179 |
Trepel J, Mollapour M, Giaccone G, Neckers L (2010). Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer, 10(8): 537–549
|
| 180 |
Ursic D, Culbertson M R (1991). The yeast homolog to mouse Tcp-1 affects microtubule-mediated processes. Mol Cell Biol, 11(5): 2629–2640
|
| 181 |
Ursic D, Sedbrook J C, Himmel K L, Culbertson M R (1994). The essential yeast Tcp1 protein affects actin and microtubules. Mol Biol Cell, 5(10): 1065–1080
|
| 182 |
van der Straten A, Rommel C, Dickson B, Hafen E (1997). The heat shock protein 83 (Hsp83) is required for Raf-mediated signalling in Drosophila. EMBO J, 16(8): 1961–1969
|
| 183 |
van Eden W (2006). Immunoregulation of autoimmune diseases. Hum Immunol, 67(6): 446–453
|
| 184 |
Verdegaal M E, Zegveld S T, van Furth R (1996). Heat shock protein 65 induces CD62e, CD106, and CD54 on cultured human endothelial cells and increases their adhesiveness for monocytes and granulocytes. J Immunol, 157(1): 369–376
|
| 185 |
Vinh D B, Drubin D G (1994). A yeast TCP-1-like protein is required for actin function in vivo. Proc Natl Acad Sci USA, 91(19): 9116–9120
|
| 186 |
Voellmy R, Bromley P, Kocher H P (1983). Structural similarities between corresponding heat-shock proteins from different eucaryotic cells. J Biol Chem, 258(6): 3516–3522
|
| 187 |
Vos M J, Zijlstra M P, Kanon B, van Waarde-Verhagen M A, Brunt E R, Oosterveld-Hut H M, Carra S, Sibon O C, Kampinga H H (2010). HSPB7 is the most potent polyQ aggregation suppressor within the HSPB family of molecular chaperones. Hum Mol Genet, 19(23): 4677–4693
|
| 188 |
Werner A, Meinhardt A, Seitz J, Bergmann M (1997). Distribution of heat-shock protein 60 immunoreactivity in testes of infertile men. Cell Tissue Res, 288(3): 539–544
|
| 189 |
Werner A, Seitz J, Meinhardt A, Bergmann M (1996). Distribution pattern of HSP60 immunoreactivity in the testicular tissue of infertile men. Ann Anat, 178(1): 81–82
|
| 190 |
Whitley D, Goldberg S P, Jordan W D (1999). Heat shock proteins: a review of the molecular chaperones. J Vasc Surg, 29(4): 748–751
|
| 190 |
Wolf B B, Green D R (1999). Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem, 274(29): 20049–20052
|
| 191 |
Xanthoudakis S, Roy S, Rasper D, Hennessey T, Aubin Y, Cassady R, Tawa P, Ruel R, Rosen A, Nicholson D W (1999). Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J, 18(8): 2049–2056
|
| 192 |
Xu Q, Wick G (1996). The role of heat shock proteins in protection and pathophysiology of the arterial wall. Mol Med Today, 2(9): 372–379
|
| 193 |
Yaffe M B, Farr G W, Miklos D, Horwich A L, Sternlicht M L, Sternlicht H (1992). TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature, 358(6383): 245–248
|
| 194 |
Yahara I (1999). The role of HSP90 in evolution. Genes Cells, 4(7): 375–379
|
| 195 |
Yamamoto M, Takahashi Y, Inano K, Horigome T, Sugano H (1991). Characterization of the hydrophobic region of heat shock protein 90. J Biochem, 110(1): 141–145
|
| 196 |
Zhang L, Koivisto L, Heino J, Uitto V J (2004). Bacterial heat shock protein 60 may increase epithelial cell migration through activation of MAP kinases and inhibition of α6β4 integrin expression. Biochem Biophys Res Commun, 319(4): 1088–1095
|
| 197 |
Zhang L, Pelech S L, Mayrand D, Grenier D, Heino J, Uitto V J (2001). Bacterial heat shock protein-60 increases epithelial cell proliferation through the ERK1/2 MAP kinases. Exp Cell Res, 266(1): 11–20
|
| 198 |
Zhao R, Davey M, Hsu Y C, Kaplanek P, Tong A, Parsons A B, Krogan N, Cagney G, Mai D, Greenblatt J, Boone C, Emili A, Houry W A (2005). Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell, 120(5): 715–727
|
| 199 |
Zimmerman J L, Petri W, Meselson M (1983). Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell, 32(4): 1161–1170
|
| 200 |
Zügel U, Kaufmann S H (1999). Immune response against heat shock proteins in infectious diseases. Immunobiology, 201(1): 22–35
|
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