Frontiers in Biology

, 6:312 | Cite as

Heat shock proteins: Molecules with assorted functions

  • Surajit Sarkar
  • M. Dhruba Singh
  • Renu Yadav
  • K. P. Arunkumar
  • Geoffrey W. Pittman
Review
  • 180 Downloads

Abstract

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.

Keywords

heat shock protein chaperone chaperonin Hsp100 Hsp90 Hsp70 Hsp60 sHsps fertility apoptosis cytoskeleton 

References

  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 WM, 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 MH, 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): 2185–2195PubMedGoogle Scholar
  2. Ambrosio L, Schedl P (1984). Gene expression during Drosophila melanogaster oogenesis: analysis by in situ hybridization to tissue sections. Dev Biol, 105(1): 80–92PubMedGoogle Scholar
  3. Arrigo A P, Tanguay R M (1991). Expression of heat shock proteins during development in Drosophila. Results Probl Cell Differ, 17: 106–119PubMedGoogle Scholar
  4. Arya R, Lakhotia S C (2008). Hsp60D is essential for caspase-mediated induced apoptosis in Drosophila melanogaster. Cell Stress Chaperones, 13(4): 509–526PubMedGoogle Scholar
  5. Arya R, Mallik M, Lakhotia S C (2007). Heat shock genes-integrating cell survival and death. J Biosci, 32(3): 595–610PubMedGoogle Scholar
  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): 3645–3657PubMedGoogle Scholar
  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): 2780–2788PubMedGoogle Scholar
  8. Betrán E, Thornton K, Long M (2002). Retroposed new genes out of the X in Drosophila. Genome Res, 12(12): 1854–1859PubMedGoogle Scholar
  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): 1879–1889PubMedGoogle Scholar
  10. Bond U, Schlesinger M J (1985). Ubiquitin is a heat shock protein in chicken embryo fibroblasts. Mol Cell Biol, 5(5): 949–956PubMedGoogle Scholar
  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): 38170–38176PubMedGoogle Scholar
  12. Bukau B, Horwich A L (1998). The Hsp70 and Hsp60 chaperone machines. Cell, 92(3): 351–366PubMedGoogle Scholar
  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): 157–167PubMedGoogle Scholar
  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): 105–111PubMedGoogle Scholar
  15. Candido E P (2002). The small heat shock proteins of the nematode Caenorhabditis elegans: structure, regulation and biology. Prog Mol Subcell Biol, 28: 61–78PubMedGoogle Scholar
  16. Caplan A J (2003). What is a co-chaperone? Cell Stress Chaperones, 8(2): 105–107PubMedGoogle Scholar
  17. 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): 147–156PubMedGoogle Scholar
  18. Cavanagh A C (1996). Identification of early pregnancy factor as chaperonin 10: implications for understanding its role. Rev Reprod, 1(1): 28–32PubMedGoogle Scholar
  19. 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): 2895–2904PubMedGoogle Scholar
  20. 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): 12414–12419PubMedGoogle Scholar
  21. 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): 9111–9115PubMedGoogle Scholar
  22. 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 SW, Linden R (2010). Cytosolic Hsp60 is involved in the NF-kappaBdependent survival of cancer cells via IKK regulation. PLoS ONE, 5(3): e9422PubMedGoogle Scholar
  23. Clarke A K (1996). Variation on a theme: Combined molecular chaperone and proteolysis functions in Clp/Hsp100 proteins. J Biosci, 21(2): 161–177Google Scholar
  24. 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): 32035–32038PubMedGoogle Scholar
  25. Csermely P (1997). Proteins, RNAs and chaperones in enzyme evolution: a folding perspective. Trends Biochem Sci, 22(5): 147–149PubMedGoogle Scholar
  26. 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): 4943–4950PubMedGoogle Scholar
  27. 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): 1657–1663PubMedGoogle Scholar
  28. 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): 129–168Google Scholar
  29. Cutforth T, Rubin G M (1994). Mutations in Hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell, 77(7): 1027–1036PubMedGoogle Scholar
  30. 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): 11155–11161Google Scholar
  31. 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): 1013–1017PubMedGoogle Scholar
  32. Dix D J (1997). Hsp70 expression and function during gametogenesis. Cell Stress Chaperones, 2(2): 73–77PubMedGoogle Scholar
  33. Eddy E M (1998). HSP70-2 heat-shock protein of mouse spermatogenic cells. J Exp Zool, 282(1–2): 261–271PubMedGoogle Scholar
  34. Ellis J (1987). Proteins as molecular chaperones. Nature, 328(6129): 378–379PubMedGoogle Scholar
  35. Ellis R J (2005). Chaperomics: in vivo GroEL function defined. Curr Biol, 15(17): 661–663Google Scholar
  36. 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): 929–935PubMedGoogle Scholar
  37. 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): 243–282PubMedGoogle Scholar
  38. Feldman D E, Frydman J (2000). Protein folding in vivo: the importance of molecular chaperones. Curr Opin Struct Biol, 10(1): 26–33PubMedGoogle Scholar
  39. Feltham J L, Gierasch L M (2000). GroEL-substrate interactions: molding the fold, or folding the mold? Cell, 100(2): 193–196PubMedGoogle Scholar
  40. 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): 1445–1462PubMedGoogle Scholar
  41. 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): 699–707PubMedGoogle Scholar
  42. 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): 1043–1050PubMedGoogle Scholar
  43. Garrido C, Gurbuxani S, Ravagnan L, Kroemer G (2001). Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun, 286(3): 433–442PubMedGoogle Scholar
  44. 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): 963–972PubMedGoogle Scholar
  45. Gething M J, Sambrook J (1992). Protein folding in the cell. Nature, 355(6355): 33–45PubMedGoogle Scholar
  46. 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): 757–762PubMedGoogle Scholar
  47. 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): 275–286PubMedGoogle Scholar
  48. Gozes I, Brenneman D E (1996). Activity-dependent neurotrophic factor (ADNF). An extracellular neuroprotective chaperonin? J Mol Neurosci, 7(4): 235–244PubMedGoogle Scholar
  49. 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): 235–242PubMedGoogle Scholar
  50. Günther E, Walter L (1994). Genetic aspects of the hsp70 multigene family in vertebrates. Experientia, 50(11–12): 987–1001PubMedGoogle Scholar
  51. 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): 1–11PubMedGoogle Scholar
  52. 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, 137–140PubMedGoogle Scholar
  53. Gupta S, Knowlton A A (2002). Cytosolic heat shock protein 60, hypoxia, and apoptosis. Circulation, 106(21): 2727–2733PubMedGoogle Scholar
  54. 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): 7011–7030Google Scholar
  55. 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): 293–322PubMedGoogle Scholar
  56. Heikkila J J (2010). Heat shock protein gene expression and function in amphibian model systems. Comp Biochem Physiol A Mol Integr Physiol, 156(1): 19–33PubMedGoogle Scholar
  57. Hemmingsen S M (1992). What is a chaperonin? Nature, 357(6380): 650–650PubMedGoogle Scholar
  58. 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): 732–736PubMedGoogle Scholar
  59. 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, 179–207Google Scholar
  60. 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): 1669–1675PubMedGoogle Scholar
  61. Hixon W G, Searcy D G (1993). Cytoskeleton in the archaebacterium Thermoplasma acidophilum? Viscosity increase in soluble extracts. Biosystems, 29(2–3): 151–160PubMedGoogle Scholar
  62. Hochstrasser M (1992). Ubiquitin and intracellular protein degradation. Curr Opin Cell Biol, 4(6): 1024–1031PubMedGoogle Scholar
  63. 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): 7451–7458PubMedGoogle Scholar
  64. 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): 147–154PubMedGoogle Scholar
  65. 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): 3081–3092PubMedGoogle Scholar
  66. 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): 759–766PubMedGoogle Scholar
  67. 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): 855–859PubMedGoogle Scholar
  68. 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): 1217–1223PubMedGoogle Scholar
  69. Iwasaki S, Kobayashi M, Yoda M, Sakaguchi Y, Katsuma S, Suzuki T, Tomari Y (2010). Hsc70/Hsp90 chaperone machinery mediates ATPdependent RISC loading of small RNA duplexes. Mol Cell, 39(2): 292–299PubMedGoogle Scholar
  70. 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): 85–89PubMedGoogle Scholar
  71. Jinn T L, Chen YM, Lin C Y (1995). Characterization and physiological function of Class I low-molecular-mass, heat-shock protein complex in soybean. Plant Physiol, 108(2): 693–701PubMedGoogle Scholar
  72. 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): 1462–1469PubMedGoogle Scholar
  73. Jost M, Kari C, Rodeck U (2000). The EGF receptor — an essential regulator of multiple epidermal functions. Eur J Dermatol, 10(7): 505–510PubMedGoogle Scholar
  74. 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): 712–725PubMedGoogle Scholar
  75. 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): 579–592PubMedGoogle Scholar
  76. Kappé G, Franck E, Verschuure P, Boelens WC, Leunissen J A, de Jong WW (2003). The human genome encodes 10 alpha-crystallin-related small heat shock proteins: HspB1-10. Cell Stress Chaperones, 8(1):53–61PubMedGoogle Scholar
  77. 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): 450–453PubMedGoogle Scholar
  78. 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): 166–174PubMedGoogle Scholar
  79. 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: 138–159PubMedGoogle Scholar
  80. 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): 4247–4253PubMedGoogle Scholar
  81. 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): 13–17PubMedGoogle Scholar
  82. 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): 253–263Google Scholar
  83. Kurtz S, Rossi J, Petko L, Lindquist S (1986). An ancient developmental induction: heat-shock proteins induced in sporulation and oogensis. Science, 231(4742): 1154–1157PubMedGoogle Scholar
  84. Lakhotia S C (2001). Heat Shock Response-Regulation and Functions of Coding and non-coding genes in Drosophila. Proc Ind Natl Acad Sci, B 5:247–264.Google Scholar
  85. Lakhotia S C, Singh A K (1989). A novel heat shock polypeptide in Malpighian tubule of Drosophila melanogaster. J Genet, 68(3): 129–268Google Scholar
  86. 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):1291–1301PubMedGoogle Scholar
  87. 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–L940PubMedGoogle Scholar
  88. 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): 90–94PubMedGoogle Scholar
  89. 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): 6304–6313PubMedGoogle Scholar
  90. 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): 687–692PubMedGoogle Scholar
  91. 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): 10519–10526PubMedGoogle Scholar
  92. Lilie H, Lang K, Rudolph R, Buchner J (1993). Prolyl isomerases catalyze antibody folding in vitro. Protein Sci, 2(9): 1490–1496PubMedGoogle Scholar
  93. Lindquist S (1980). Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev Biol, 77(2): 463–479PubMedGoogle Scholar
  94. Lindquist S (1986). The heat-shock response. Annu Rev Biochem, 55(1): 1151–1191PubMedGoogle Scholar
  95. 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): 1980–1987PubMedGoogle Scholar
  96. Matzinger P (2002). The danger model: a renewed sense of self. Science, 296(5566): 301–305PubMedGoogle Scholar
  97. Mayer M P (2010). Gymnastics of molecular chaperones. Mol Cell, 39(3): 321–331PubMedGoogle Scholar
  98. McDonough H, Patterson C (2003). CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones, 8(4): 303–308PubMedGoogle Scholar
  99. McKay D B (1991). Structure of the 70-kilodalton heat-shock-related proteins. Springer Semin Immunopathol, 13(1): 1–9PubMedGoogle Scholar
  100. 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): 798–807PubMedGoogle Scholar
  101. 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): 2895–2904PubMedGoogle Scholar
  102. 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: 79–101PubMedGoogle Scholar
  103. 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): 305–315PubMedGoogle Scholar
  104. Miklos D, Caplan S, Mertens D, Hynes G, Pitluk Z, Kashi Y, Harrison-Lavoie K, Stevenson S, Brown C, Barrell B, et al (1994). Primary structure and function of a second essential member of the heterooligomeric TCP1 chaperonin complex of yeast, TCP1 beta. Proc Natl Acad Sci USA, 91(7): 2743–2747PubMedGoogle Scholar
  105. 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): 407–422PubMedGoogle Scholar
  106. Morange M (2006). HSFs in development. Handb Exp Pharmacol, 172(172): 153–169PubMedGoogle Scholar
  107. 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):648–659PubMedGoogle Scholar
  108. 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): 51–60PubMedGoogle Scholar
  109. Morrow G, Tanguay R M (2003). Heat shock proteins and aging in Drosophila melanogaster. Semin Cell Dev Biol, 14(5): 291–299PubMedGoogle Scholar
  110. 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): 1133–1138PubMedGoogle Scholar
  111. Naaby-Hansen S, Herr J C (2010). Heat shock proteins on the human sperm surface. J Reprod Immunol, 84(1): 32–40PubMedGoogle Scholar
  112. 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): 12023–12028PubMedGoogle Scholar
  113. 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):925–929PubMedGoogle Scholar
  114. 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): 149–159Google Scholar
  115. Nollen E A, Morimoto R I (2002). Chaperoning signaling pathways: molecular chaperones as stress-sensing ‘heat shock’ proteins. J Cell Sci, 115(Pt 14): 2809–2816PubMedGoogle Scholar
  116. Nover L, ed. (1984). Heat Shock Response in eukaryotic cells. Springer-Verlag, Berlin, pp-1–78.Google Scholar
  117. 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): 597–606PubMedGoogle Scholar
  118. 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): 4310–4322PubMedGoogle Scholar
  119. Paranko J, Seitz J, Meinhardt A (1996). Developmental expression of heat shock protein 60 (HSP60) in the rat testis and ovary. Differentiation, 60(3): 159–167PubMedGoogle Scholar
  120. 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, 457–493Google Scholar
  121. 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): 270–273PubMedGoogle Scholar
  122. Pauli D, Arrigo A P, Tissières A (1992). Heat shock response in Drosophila. Experientia, 48(7): 623–629PubMedGoogle Scholar
  123. Pelham H R (1986). Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell, 46(7): 959–961PubMedGoogle Scholar
  124. 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): 1587–1594PubMedGoogle Scholar
  125. Pockley A G (2002). Heat shock proteins, inflammation, and cardiovascular disease. Circulation, 105(8): 1012–1017PubMedGoogle Scholar
  126. 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): 269–279PubMedGoogle Scholar
  127. Pratt WB, Toft D O (2003). Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood), 228(2): 111–133Google Scholar
  128. 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): 597–600PubMedGoogle Scholar
  129. Ranford J C, Coates A R, Henderson B (2000). Chaperonins are cellsignalling proteins: the unfolding biology of molecular chaperones. Expert Rev Mol Med, 2(8): 1–17PubMedGoogle Scholar
  130. Ranson N A, White H E, Saibil H R (1998). Chaperonins. Biochem J, 333(Pt 2): 233–242PubMedGoogle Scholar
  131. 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: 129–133Google Scholar
  132. 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): 5689–5693PubMedGoogle Scholar
  133. Richter K, Haslbeck M, Buchner J (2010). The heat shock response: life on the verge of death. Mol Cell, 40(2): 253–266PubMedGoogle Scholar
  134. Ritossa F A (1962). A new puffing pattern induced by a temperature shock and DNP in Drosophila. Experientia, 18(12): 571–573Google Scholar
  135. 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): 21–32PubMedGoogle Scholar
  136. 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): 1477–1488PubMedGoogle Scholar
  137. Rubin GM, Yandell MD, 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): 2204–2215PubMedGoogle Scholar
  138. Rutherford S, Knapp J R, Csermely P (2007). Hsp90 and developmental networks. Adv Exp Med Biol, 594: 190–197PubMedGoogle Scholar
  139. Rutherford S L (2003). Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet, 4(4): 263–274PubMedGoogle Scholar
  140. Rutherford S L, Lindquist S (1998). Hsp90 as a capacitor for morphological evolution. Nature, 396(6709): 336–342PubMedGoogle Scholar
  141. Saibil H (1996). The lid that shapes the pot: structure and function of the chaperonin GroES. Structure, 4(1): 1–4PubMedGoogle Scholar
  142. 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): 2040–2048PubMedGoogle Scholar
  143. Sanchez Y, Lindquist S L (1990). HSP104 required for induced thermotolerance. Science, 248(4959): 1112–1115PubMedGoogle Scholar
  144. Sarge K D, Cullen K E (1997). Regulation of hsp expression during rodent spermatogenesis. Cell Mol Life Sci, 53(2): 191–197PubMedGoogle Scholar
  145. 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).Google Scholar
  146. 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): 265–281PubMedGoogle Scholar
  147. 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): 1334–1347PubMedGoogle Scholar
  148. 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): 289–296PubMedGoogle Scholar
  149. Shinoda H, Huang C C (1996). Heat shock proteins in middle ear cholesteatoma. Otolaryngol Head Neck Surg, 114(1): 77–83PubMedGoogle Scholar
  150. 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: 178–182Google Scholar
  151. 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): 4114–4126PubMedGoogle Scholar
  152. Slavotinek AM, Biesecker L G (2001). Unfolding the role of chaperones and chaperonins in human disease. Trends Genet, 17(9): 528–535PubMedGoogle Scholar
  153. 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): 29299–29307PubMedGoogle Scholar
  154. 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): 70–74PubMedGoogle Scholar
  155. 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): 16–27PubMedGoogle Scholar
  156. Soltys B J, Gupta R S (1999). Mitochondrial-matrix proteins at unexpected locations: are they exported? Trends Biochem Sci, 24(5): 174–177PubMedGoogle Scholar
  157. 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): 3574–3581PubMedGoogle Scholar
  158. Soti C, Csermely P (2002). Chaperones come of age. Cell Stress Chaperones, 7(2): 186–190PubMedGoogle Scholar
  159. 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): 769–780PubMedGoogle Scholar
  160. 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): 35–57PubMedGoogle Scholar
  161. 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): 598–604PubMedGoogle Scholar
  162. 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): 4254–4262PubMedGoogle Scholar
  163. 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): 4599–4602PubMedGoogle Scholar
  164. Sternlicht H, Farr GW, Sternlicht ML, Driscoll J K, Willison K, YaffeM B (1993). The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc Natl Acad Sci USA, 90(20): 9422–9426PubMedGoogle Scholar
  165. Sun Y, MacRae T H (2005). Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci, 62(21): 2460–2476PubMedGoogle Scholar
  166. 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): 633–640PubMedGoogle Scholar
  167. 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): 1315–1318PubMedGoogle Scholar
  168. 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): 41–49Google Scholar
  169. 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): 515–528PubMedGoogle Scholar
  170. Thirumalai D, Lorimer G H (2001). Chaperonin-mediated protein folding. Annu Rev Biophys Biomol Struct, 30(1): 245–269PubMedGoogle Scholar
  171. Thornberry N A, Lazebnik Y (1998). Caspases: enemies within. Science, 281(5381): 1312–1316PubMedGoogle Scholar
  172. Timakov B, Zhang P (2001). The hsp60B gene of Drosophila melanogaster is essential for the spermatid individualization process. Cell Stress Chaperones, 6(1): 71–77PubMedGoogle Scholar
  173. 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): 389–398PubMedGoogle Scholar
  174. Togo T, Dickson D W (2002). Ballooned neurons in progressive supranuclear palsy are usually due to concurrent argyrophilic grain disease. Acta Neuropathol, 104(1): 53–56PubMedGoogle Scholar
  175. 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): 2192–2197PubMedGoogle Scholar
  176. 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): 5383–5388PubMedGoogle Scholar
  177. 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): 490–493PubMedGoogle Scholar
  178. Trepel J, Mollapour M, Giaccone G, Neckers L (2010). Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer, 10(8): 537–549PubMedGoogle Scholar
  179. Ursic D, Culbertson M R (1991). The yeast homolog to mouse Tcp-1 affects microtubule-mediated processes. Mol Cell Biol, 11(5): 2629–2640PubMedGoogle Scholar
  180. 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): 1065–1080PubMedGoogle Scholar
  181. 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): 1961–1969PubMedGoogle Scholar
  182. van Eden W (2006). Immunoregulation of autoimmune diseases. Hum Immunol, 67(6): 446–453PubMedGoogle Scholar
  183. 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): 369–376PubMedGoogle Scholar
  184. 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): 9116–9120PubMedGoogle Scholar
  185. Voellmy R, Bromley P, Kocher H P (1983). Structural similarities between corresponding heat-shock proteins from different eukaryotic cells. J Biol Chem, 258(6): 3516–3522PubMedGoogle Scholar
  186. 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): 4677–4693PubMedGoogle Scholar
  187. 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): 539–544PubMedGoogle Scholar
  188. 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): 81–82PubMedGoogle Scholar
  189. Whitley D, Goldberg S P, Jordan W D (1999). Heat shock proteins: a review of the molecular chaperones. J Vasc Surg, 29(4): 748–751PubMedGoogle Scholar
  190. Wolf B B, Green D R (1999). Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem, 274(29): 20049–20052PubMedGoogle Scholar
  191. Xanthoudakis S, Roy S, Rasper D, Hennessey T, Aubin Y, Cassady R, Tawa P, Ruel R, Rosen A, Nicholson DW(1999). Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J, 18(8): 2049–2056PubMedGoogle Scholar
  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): 372–379PubMedGoogle Scholar
  193. Yaffe MB, Farr GW, Miklos D, Horwich A L, Sternlicht ML, Sternlicht H (1992). TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature, 358(6383): 245–248PubMedGoogle Scholar
  194. Yahara I (1999). The role of HSP90 in evolution. Genes Cells, 4(7): 375–379PubMedGoogle Scholar
  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): 141–145PubMedGoogle Scholar
  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): 1088–1095PubMedGoogle Scholar
  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): 11–20PubMedGoogle Scholar
  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): 715–727PubMedGoogle Scholar
  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): 1161–1170PubMedGoogle Scholar
  200. Zügel U, Kaufmann S H (1999). Immune response against heat shock proteins in infectious diseases. Immunobiology, 201(1): 22–35PubMedGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Surajit Sarkar
    • 1
    • 2
  • M. Dhruba Singh
    • 1
  • Renu Yadav
    • 1
  • K. P. Arunkumar
    • 2
  • Geoffrey W. Pittman
    • 2
  1. 1.Department of GeneticsUniversity of DelhiNew DelhiIndia
  2. 2.Division of Biology, MC156-29California Institute of TechnologyPasadenaUSA

Personalised recommendations