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Microbiol Rev. 1993 June; 57(2): 402–414.
PMCID: PMC372916

Heat shock proteins: molecular chaperones of protein biogenesis.

Abstract

Heat shock proteins (Hsps) were first identified as proteins whose synthesis was enhanced by stresses such as an increase in temperature. Recently, several of the major Hsps have been shown to be intimately involved in protein biogenesis through a direct interaction with a wide variety of proteins. As a reflection of this role, these Hsps have been referred to as molecular chaperones. Hsp70s interact with incompletely folded proteins, such as nascent chains on ribosomes and proteins in the process of translocation from the cytosol into mitochondria and the endoplasmic reticulum. Hsp60 also binds to unfolded proteins, preventing aggregation and facilitating protein folding. Although less well defined, other Hsps such as Hsp90 also play important roles in modulating the activity of a number of proteins. The function of the proteolytic system is intertwined with that of molecular chaperones. Several components of this system, encoded by heat-inducible genes, are responsible for the degradation of abnormal or misfolded proteins. The budding yeast Saccharomyces cerevisiae has proven very useful in the analysis of the role of molecular chaperones in protein maturation, translocation, and degradation. In this review, results of experiments are discussed within the context of experiments with other organisms in an attempt to describe the current state of understanding of these ubiquitous and important proteins.

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  • Atencio DP, Yaffe MP. MAS5, a yeast homolog of DnaJ involved in mitochondrial protein import. Mol Cell Biol. 1992 Jan;12(1):283–291. [PMC free article] [PubMed]
  • Beckmann RP, Mizzen LE, Welch WJ. Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science. 1990 May 18;248(4957):850–854. [PubMed]
  • Blobel G, Sabatini DD. Controlled proteolysis of nascent polypeptides in rat liver cell fractions. I. Location of the polypeptides within ribosomes. J Cell Biol. 1970 Apr;45(1):130–145. [PMC free article] [PubMed]
  • Blumberg H, Silver PA. A homologue of the bacterial heat-shock gene DnaJ that alters protein sorting in yeast. Nature. 1991 Feb 14;349(6310):627–630. [PubMed]
  • Bole DG, Hendershot LM, Kearney JF. Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J Cell Biol. 1986 May;102(5):1558–1566. [PMC free article] [PubMed]
  • Boorstein WR, Craig EA. Transcriptional regulation of SSA3, an HSP70 gene from Saccharomyces cerevisiae. Mol Cell Biol. 1990 Jun;10(6):3262–3267. [PMC free article] [PubMed]
  • Boorstein WR, Craig EA. Structure and regulation of the SSA4 HSP70 gene of Saccharomyces cerevisiae. J Biol Chem. 1990 Nov 5;265(31):18912–18921. [PubMed]
  • Borkovich KA, Farrelly FW, Finkelstein DB, Taulien J, Lindquist S. hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol. 1989 Sep;9(9):3919–3930. [PMC free article] [PubMed]
  • Bresnick EH, Dalman FC, Sanchez ER, Pratt WB. Evidence that the 90-kDa heat shock protein is necessary for the steroid binding conformation of the L cell glucocorticoid receptor. J Biol Chem. 1989 Mar 25;264(9):4992–4997. [PubMed]
  • Brizuela L, Chrebet G, Bostian KA, Parent SA. Antifungal properties of the immunosuppressant FK-506: identification of an FK-506-responsive yeast gene distinct from FKB1. Mol Cell Biol. 1991 Sep;11(9):4616–4626. [PMC free article] [PubMed]
  • Caplan AJ, Cyr DM, Douglas MG. YDJ1p facilitates polypeptide translocation across different intracellular membranes by a conserved mechanism. Cell. 1992 Dec 24;71(7):1143–1155. [PubMed]
  • Caplan AJ, Douglas MG. Characterization of YDJ1: a yeast homologue of the bacterial dnaJ protein. J Cell Biol. 1991 Aug;114(4):609–621. [PMC free article] [PubMed]
  • Caplan AJ, Tsai J, Casey PJ, Douglas MG. Farnesylation of YDJ1p is required for function at elevated growth temperatures in Saccharomyces cerevisiae. J Biol Chem. 1992 Sep 15;267(26):18890–18895. [PubMed]
  • Chappell TG, Konforti BB, Schmid SL, Rothman JE. The ATPase core of a clathrin uncoating protein. J Biol Chem. 1987 Jan 15;262(2):746–751. [PubMed]
  • Cheng MY, Hartl FU, Horwich AL. The mitochondrial chaperonin hsp60 is required for its own assembly. Nature. 1990 Nov 29;348(6300):455–458. [PubMed]
  • Chirico WJ, Waters MG, Blobel G. 70K heat shock related proteins stimulate protein translocation into microsomes. Nature. 1988 Apr 28;332(6167):805–810. [PubMed]
  • Ciechanover A, Schwartz AL. How are substrates recognized by the ubiquitin-mediated proteolytic system? Trends Biochem Sci. 1989 Dec;14(12):483–488. [PubMed]
  • Colley NJ, Baker EK, Stamnes MA, Zuker CS. The cyclophilin homolog ninaA is required in the secretory pathway. Cell. 1991 Oct 18;67(2):255–263. [PubMed]
  • Conde J, Fink GR. A mutant of Saccharomyces cerevisiae defective for nuclear fusion. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3651–3655. [PubMed]
  • Craig EA. The heat shock response. CRC Crit Rev Biochem. 1985;18(3):239–280. [PubMed]
  • Craig EA. Essential roles of 70kDa heat inducible proteins. Bioessays. 1989 Aug-Sep;11(2-3):48–52. [PubMed]
  • Craig EA, Jacobsen K. Mutations of the heat inducible 70 kilodalton genes of yeast confer temperature sensitive growth. Cell. 1984 Oct;38(3):841–849. [PubMed]
  • Craig EA, Jacobsen K. Mutations in cognate genes of Saccharomyces cerevisiae hsp70 result in reduced growth rates at low temperatures. Mol Cell Biol. 1985 Dec;5(12):3517–3524. [PMC free article] [PubMed]
  • Craig EA, Kramer J, Kosic-Smithers J. SSC1, a member of the 70-kDa heat shock protein multigene family of Saccharomyces cerevisiae, is essential for growth. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4156–4160. [PubMed]
  • Craig EA, Kramer J, Shilling J, Werner-Washburne M, Holmes S, Kosic-Smithers J, Nicolet CM. SSC1, an essential member of the yeast HSP70 multigene family, encodes a mitochondrial protein. Mol Cell Biol. 1989 Jul;9(7):3000–3008. [PMC free article] [PubMed]
  • Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677. [PubMed]
  • Cyr DM, Lu X, Douglas MG. Regulation of Hsp70 function by a eukaryotic DnaJ homolog. J Biol Chem. 1992 Oct 15;267(29):20927–20931. [PubMed]
  • Deshaies RJ, Koch BD, Werner-Washburne M, Craig EA, Schekman R. A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature. 1988 Apr 28;332(6167):800–805. [PubMed]
  • Deshaies RJ, Sanders SL, Feldheim DA, Schekman R. Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex. Nature. 1991 Feb 28;349(6312):806–808. [PubMed]
  • Eilers M, Schatz G. Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature. 1986 Jul 17;322(6076):228–232. [PubMed]
  • Ellis RJ. Molecular chaperones: the plant connection. Science. 1990 Nov 16;250(4983):954–959. [PubMed]
  • Ellis RJ, van der Vies SM. Molecular chaperones. Annu Rev Biochem. 1991;60:321–347. [PubMed]
  • Ellwood MS, Craig EA. Differential regulation of the 70K heat shock gene and related genes in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Aug;4(8):1454–1459. [PMC free article] [PubMed]
  • Engman DM, Kirchhoff LV, Donelson JE. Molecular cloning of mtp70, a mitochondrial member of the hsp70 family. Mol Cell Biol. 1989 Nov;9(11):5163–5168. [PMC free article] [PubMed]
  • Farquhar R, Honey N, Murant SJ, Bossier P, Schultz L, Montgomery D, Ellis RW, Freedman RB, Tuite MF. Protein disulfide isomerase is essential for viability in Saccharomyces cerevisiae. Gene. 1991 Dec 1;108(1):81–89. [PubMed]
  • Farrelly FW, Finkelstein DB. Complete sequence of the heat shock-inducible HSP90 gene of Saccharomyces cerevisiae. J Biol Chem. 1984 May 10;259(9):5745–5751. [PubMed]
  • Feldheim D, Rothblatt J, Schekman R. Topology and functional domains of Sec63p, an endoplasmic reticulum membrane protein required for secretory protein translocation. Mol Cell Biol. 1992 Jul;12(7):3288–3296. [PMC free article] [PubMed]
  • Felici F, Cesareni G, Hughes JM. The most abundant small cytoplasmic RNA of Saccharomyces cerevisiae has an important function required for normal cell growth. Mol Cell Biol. 1989 Aug;9(8):3260–3268. [PMC free article] [PubMed]
  • Finley D, Bartel B, Varshavsky A. The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature. 1989 Mar 30;338(6214):394–401. [PubMed]
  • Finley D, Chau V. Ubiquitination. Annu Rev Cell Biol. 1991;7:25–69. [PubMed]
  • Finley D, Ozkaynak E, Varshavsky A. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell. 1987 Mar 27;48(6):1035–1046. [PubMed]
  • Flaherty KM, DeLuca-Flaherty C, McKay DB. Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature. 1990 Aug 16;346(6285):623–628. [PubMed]
  • Flaherty KM, McKay DB, Kabsch W, Holmes KC. Similarity of the three-dimensional structures of actin and the ATPase fragment of a 70-kDa heat shock cognate protein. Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):5041–5045. [PubMed]
  • Flajnik MF, Canel C, Kramer J, Kasahara M. Which came first, MHC class I or class II? Immunogenetics. 1991;33(5-6):295–300. [PubMed]
  • Flynn GC, Pohl J, Flocco MT, Rothman JE. Peptide-binding specificity of the molecular chaperone BiP. Nature. 1991 Oct 24;353(6346):726–730. [PubMed]
  • Flynn GC, Chappell TG, Rothman JE. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science. 1989 Jul 28;245(4916):385–390. [PubMed]
  • Fremont DH, Matsumura M, Stura EA, Peterson PA, Wilson IA. Crystal structures of two viral peptides in complex with murine MHC class I H-2Kb. Science. 1992 Aug 14;257(5072):919–927. [PubMed]
  • Frydman J, Nimmesgern E, Erdjument-Bromage H, Wall JS, Tempst P, Hartl FU. Function in protein folding of TRiC, a cytosolic ring complex containing TCP-1 and structurally related subunits. EMBO J. 1992 Dec;11(13):4767–4778. [PubMed]
  • Gao BC, Biosca J, Craig EA, Greene LE, Eisenberg E. Uncoating of coated vesicles by yeast hsp70 proteins. J Biol Chem. 1991 Oct 15;266(29):19565–19571. [PubMed]
  • Gao Y, Thomas JO, Chow RL, Lee GH, Cowan NJ. A cytoplasmic chaperonin that catalyzes beta-actin folding. Cell. 1992 Jun 12;69(6):1043–1050. [PubMed]
  • Georgopoulos C. The emergence of the chaperone machines. Trends Biochem Sci. 1992 Aug;17(8):295–299. [PubMed]
  • Gething MJ, McCammon K, Sambrook J. Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell. 1986 Sep 12;46(6):939–950. [PubMed]
  • Gething MJ, Sambrook J. Protein folding in the cell. Nature. 1992 Jan 2;355(6355):33–45. [PubMed]
  • Glick BS, Brandt A, Cunningham K, Müller S, Hallberg RL, Schatz G. Cytochromes c1 and b2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell. 1992 May 29;69(5):809–822. [PubMed]
  • Goebl MG, Yochem J, Jentsch S, McGrath JP, Varshavsky A, Byers B. The yeast cell cycle gene CDC34 encodes a ubiquitin-conjugating enzyme. Science. 1988 Sep 9;241(4871):1331–1335. [PubMed]
  • Goldberg AL. The mechanism and functions of ATP-dependent proteases in bacterial and animal cells. Eur J Biochem. 1992 Jan 15;203(1-2):9–23. [PubMed]
  • Goloubinoff P, Gatenby AA, Lorimer GH. GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli. Nature. 1989 Jan 5;337(6202):44–47. [PubMed]
  • Gottesman S, Squires C, Pichersky E, Carrington M, Hobbs M, Mattick JS, Dalrymple B, Kuramitsu H, Shiroza T, Foster T, et al. Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes. Proc Natl Acad Sci U S A. 1990 May;87(9):3513–3517. [PubMed]
  • Gupta RS. Sequence and structural homology between a mouse T-complex protein TCP-1 and the 'chaperonin' family of bacterial (GroEL, 60-65 kDa heat shock antigen) and eukaryotic proteins. Biochem Int. 1990;20(4):833–841. [PubMed]
  • Haas IG, Wabl M. Immunoglobulin heavy chain binding protein. Nature. 1983 Nov 24;306(5941):387–389. [PubMed]
  • Haendler B, Keller R, Hiestand PC, Kocher HP, Wegmann G, Movva NR. Yeast cyclophilin: isolation and characterization of the protein, cDNA and gene. Gene. 1989 Nov 15;83(1):39–46. [PubMed]
  • Hann BC, Walter P. The signal recognition particle in S. cerevisiae. Cell. 1991 Oct 4;67(1):131–144. [PubMed]
  • Hartl FU, Ostermann J, Guiard B, Neupert W. Successive translocation into and out of the mitochondrial matrix: targeting of proteins to the intermembrane space by a bipartite signal peptide. Cell. 1987 Dec 24;51(6):1027–1037. [PubMed]
  • Heinemeyer W, Kleinschmidt JA, Saidowsky J, Escher C, Wolf DH. Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J. 1991 Mar;10(3):555–562. [PubMed]
  • Heitman J, Movva NR, Hall MN. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science. 1991 Aug 23;253(5022):905–909. [PubMed]
  • Heitman J, Movva NR, Hall MN. Proline isomerases at the crossroads of protein folding, signal transduction, and immunosuppression. New Biol. 1992 May;4(5):448–460. [PubMed]
  • Heitman J, Movva NR, Hiestand PC, Hall MN. FK 506-binding protein proline rotamase is a target for the immunosuppressive agent FK 506 in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1948–1952. [PubMed]
  • Hershko A. The ubiquitin pathway for protein degradation. Trends Biochem Sci. 1991 Jul;16(7):265–268. [PubMed]
  • Hutchison KA, Czar MJ, Scherrer LC, Pratt WB. Monovalent cation selectivity for ATP-dependent association of the glucocorticoid receptor with hsp70 and hsp90. J Biol Chem. 1992 Jul 15;267(20):14047–14053. [PubMed]
  • Jentsch S. The ubiquitin-conjugation system. Annu Rev Genet. 1992;26:179–207. [PubMed]
  • Jentsch S. Ubiquitin-dependent protein degradation: a cellular perspective. Trends Cell Biol. 1992 Apr;2(4):98–103. [PubMed]
  • Jentsch S, McGrath JP, Varshavsky A. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature. 1987 Sep 10;329(6135):131–134. [PubMed]
  • Kang PJ, Ostermann J, Shilling J, Neupert W, Craig EA, Pfanner N. Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature. 1990 Nov 8;348(6297):137–143. [PubMed]
  • Koll H, Guiard B, Rassow J, Ostermann J, Horwich AL, Neupert W, Hartl FU. Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space. Cell. 1992 Mar 20;68(6):1163–1175. [PubMed]
  • Koser PL, Bergsma DJ, Cafferkey R, Eng WK, McLaughlin MM, Ferrara A, Silverman C, Kasyan K, Bossard MJ, Johnson RK, et al. The CYP2 gene of Saccharomyces cerevisiae encodes a cyclosporin A-sensitive peptidyl-prolyl cis-trans isomerase with an N-terminal signal sequence. Gene. 1991 Dec 1;108(1):73–80. [PubMed]
  • Langer T, Lu C, Echols H, Flanagan J, Hayer MK, Hartl FU. Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature. 1992 Apr 23;356(6371):683–689. [PubMed]
  • Leustek T, Dalie B, Amir-Shapira D, Brot N, Weissbach H. A member of the Hsp70 family is localized in mitochondria and resembles Escherichia coli DnaK. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7805–7808. [PubMed]
  • Lewis VA, Hynes GM, Zheng D, Saibil H, Willison K. T-complex polypeptide-1 is a subunit of a heteromeric particle in the eukaryotic cytosol. Nature. 1992 Jul 16;358(6383):249–252. [PubMed]
  • Liberek K, Marszalek J, Ang D, Georgopoulos C, Zylicz M. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2874–2878. [PubMed]
  • Liberek K, Skowyra D, Zylicz M, Johnson C, Georgopoulos C. The Escherichia coli DnaK chaperone, the 70-kDa heat shock protein eukaryotic equivalent, changes conformation upon ATP hydrolysis, thus triggering its dissociation from a bound target protein. J Biol Chem. 1991 Aug 5;266(22):14491–14496. [PubMed]
  • Lubben TH, Gatenby AA, Donaldson GK, Lorimer GH, Viitanen PV. Identification of a groES-like chaperonin in mitochondria that facilitates protein folding. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7683–7687. [PubMed]
  • Luke MM, Sutton A, Arndt KT. Characterization of SIS1, a Saccharomyces cerevisiae homologue of bacterial dnaJ proteins. J Cell Biol. 1991 Aug;114(4):623–638. [PMC free article] [PubMed]
  • Malkin LI, Rich A. Partial resistance of nascent polypeptide chains to proteolytic digestion due to ribosomal shielding. J Mol Biol. 1967 Jun 14;26(2):329–346. [PubMed]
  • Manning-Krieg UC, Scherer PE, Schatz G. Sequential action of mitochondrial chaperones in protein import into the matrix. EMBO J. 1991 Nov;10(11):3273–3280. [PubMed]
  • Martin J, Langer T, Boteva R, Schramel A, Horwich AL, Hartl FU. Chaperonin-mediated protein folding at the surface of groEL through a 'molten globule'-like intermediate. Nature. 1991 Jul 4;352(6330):36–42. [PubMed]
  • Matsumura M, Fremont DH, Peterson PA, Wilson IA. Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science. 1992 Aug 14;257(5072):927–934. [PubMed]
  • McGrath JP, Jentsch S, Varshavsky A. UBA 1: an essential yeast gene encoding ubiquitin-activating enzyme. EMBO J. 1991 Jan;10(1):227–236. [PubMed]
  • McLaughlin MM, Bossard MJ, Koser PL, Cafferkey R, Morris RA, Miles LM, Strickler J, Bergsma DJ, Levy MA, Livi GP. The yeast cyclophilin multigene family: purification, cloning and characterization of a new isoform. Gene. 1992 Feb 1;111(1):85–92. [PubMed]
  • McMullin TW, Hallberg RL. A highly evolutionarily conserved mitochondrial protein is structurally related to the protein encoded by the Escherichia coli groEL gene. Mol Cell Biol. 1988 Jan;8(1):371–380. [PMC free article] [PubMed]
  • Milligan RA, Unwin PN. Location of exit channel for nascent protein in 80S ribosome. Nature. 1986 Feb 20;319(6055):693–695. [PubMed]
  • Mizzen LA, Chang C, Garrels JI, Welch WJ. Identification, characterization, and purification of two mammalian stress proteins present in mitochondria, grp 75, a member of the hsp 70 family and hsp 58, a homolog of the bacterial groEL protein. J Biol Chem. 1989 Dec 5;264(34):20664–20675. [PubMed]
  • Morishima N, Nakagawa K, Yamamoto E, Shibata T. A subunit of yeast site-specific endonuclease SceI is a mitochondrial version of the 70-kDa heat shock protein. J Biol Chem. 1990 Sep 5;265(25):15189–15197. [PubMed]
  • Munro S, Pelham HR. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell. 1986 Jul 18;46(2):291–300. [PubMed]
  • Murakami H, Pain D, Blobel G. 70-kD heat shock-related protein is one of at least two distinct cytosolic factors stimulating protein import into mitochondria. J Cell Biol. 1988 Dec;107(6 Pt 1):2051–2057. [PMC free article] [PubMed]
  • Müsch A, Wiedmann M, Rapoport TA. Yeast Sec proteins interact with polypeptides traversing the endoplasmic reticulum membrane. Cell. 1992 Apr 17;69(2):343–352. [PubMed]
  • Nakagawa K, Morishima N, Shibata T. An endonuclease with multiple cutting sites, Endo.SceI, initiates genetic recombination at its cutting site in yeast mitochondria. EMBO J. 1992 Jul;11(7):2707–2715. [PubMed]
  • Nelson RJ, Heschl MF, Craig EA. Isolation and characterization of extragenic suppressors of mutations in the SSA hsp70 genes of Saccharomyces cerevisiae. Genetics. 1992 Jun;131(2):277–285. [PubMed]
  • Nelson RJ, Ziegelhoffer T, Nicolet C, Werner-Washburne M, Craig EA. The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell. 1992 Oct 2;71(1):97–105. [PubMed]
  • Noiva R, Lennarz WJ. Protein disulfide isomerase. A multifunctional protein resident in the lumen of the endoplasmic reticulum. J Biol Chem. 1992 Feb 25;267(6):3553–3556. [PubMed]
  • Normington K, Kohno K, Kozutsumi Y, Gething MJ, Sambrook J. S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell. 1989 Jun 30;57(7):1223–1236. [PubMed]
  • Ostermann J, Voos W, Kang PJ, Craig EA, Neupert W, Pfanner N. Precursor proteins in transit through mitochondrial contact sites interact with hsp70 in the matrix. FEBS Lett. 1990 Dec 17;277(1-2):281–284. [PubMed]
  • Ostermann J, Horwich AL, Neupert W, Hartl FU. Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature. 1989 Sep 14;341(6238):125–130. [PubMed]
  • Ozkaynak E, Finley D, Varshavsky A. The yeast ubiquitin gene: head-to-tail repeats encoding a polyubiquitin precursor protein. Nature. 1984 Dec 13;312(5995):663–666. [PubMed]
  • Parsell DA, Sanchez Y, Stitzel JD, Lindquist S. Hsp104 is a highly conserved protein with two essential nucleotide-binding sites. Nature. 1991 Sep 19;353(6341):270–273. [PubMed]
  • Pelham HR, Hardwick KG, Lewis MJ. Sorting of soluble ER proteins in yeast. EMBO J. 1988 Jun;7(6):1757–1762. [PubMed]
  • Pelham HR. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 1986 Sep 26;46(7):959–961. [PubMed]
  • Pfanner N, Neupert W. The mitochondrial protein import apparatus. Annu Rev Biochem. 1990;59:331–353. [PubMed]
  • Picard D, Khursheed B, Garabedian MJ, Fortin MG, Lindquist S, Yamamoto KR. Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature. 1990 Nov 8;348(6297):166–168. [PubMed]
  • Pratt WB. Transformation of glucocorticoid and progesterone receptors to the DNA-binding state. J Cell Biochem. 1987 Sep;35(1):51–68. [PubMed]
  • Pratt WB, Scherrer LC, Hutchison KA, Dalman FC. A model of glucocorticoid receptor unfolding and stabilization by a heat shock protein complex. J Steroid Biochem Mol Biol. 1992 Mar;41(3-8):223–229. [PubMed]
  • Reading DS, Hallberg RL, Myers AM. Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor. Nature. 1989 Feb 16;337(6208):655–659. [PubMed]
  • Rechsteiner M. Natural substrates of the ubiquitin proteolytic pathway. Cell. 1991 Aug 23;66(4):615–618. [PubMed]
  • Rippmann F, Taylor WR, Rothbard JB, Green NM. A hypothetical model for the peptide binding domain of hsp70 based on the peptide binding domain of HLA. EMBO J. 1991 May;10(5):1053–1059. [PubMed]
  • Rose MD, Misra LM, Vogel JP. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell. 1989 Jun 30;57(7):1211–1221. [PubMed]
  • Rothblatt JA, Deshaies RJ, Sanders SL, Daum G, Schekman R. Multiple genes are required for proper insertion of secretory proteins into the endoplasmic reticulum in yeast. J Cell Biol. 1989 Dec;109(6 Pt 1):2641–2652. [PMC free article] [PubMed]
  • Rothman JE. Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell. 1989 Nov 17;59(4):591–601. [PubMed]
  • Richter-Ruoff B, Heinemeyer W, Wolf DH. The proteasome/multicatalytic-multifunctional proteinase. In vivo function in the ubiquitin-dependent N-end rule pathway of protein degradation in eukaryotes. FEBS Lett. 1992 May 11;302(2):192–196. [PubMed]
  • Sadler I, Chiang A, Kurihara T, Rothblatt J, Way J, Silver P. A yeast gene important for protein assembly into the endoplasmic reticulum and the nucleus has homology to DnaJ, an Escherichia coli heat shock protein. J Cell Biol. 1989 Dec;109(6 Pt 1):2665–2675. [PMC free article] [PubMed]
  • Sanchez Y, Lindquist SL. HSP104 required for induced thermotolerance. Science. 1990 Jun 1;248(4959):1112–1115. [PubMed]
  • Sanders SL, Whitfield KM, Vogel JP, Rose MD, Schekman RW. Sec61p and BiP directly facilitate polypeptide translocation into the ER. Cell. 1992 Apr 17;69(2):353–365. [PubMed]
  • Scherer PE, Krieg UC, Hwang ST, Vestweber D, Schatz G. A precursor protein partly translocated into yeast mitochondria is bound to a 70 kd mitochondrial stress protein. EMBO J. 1990 Dec;9(13):4315–4322. [PubMed]
  • Schleyer M, Neupert W. Transport of proteins into mitochondria: translocational intermediates spanning contact sites between outer and inner membranes. Cell. 1985 Nov;43(1):339–350. [PubMed]
  • Schreiber SL. Chemistry and biology of the immunophilins and their immunosuppressive ligands. Science. 1991 Jan 18;251(4991):283–287. [PubMed]
  • Seufert W, Jentsch S. Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins. EMBO J. 1990 Feb;9(2):543–550. [PubMed]
  • Seufert W, McGrath JP, Jentsch S. UBC1 encodes a novel member of an essential subfamily of yeast ubiquitin-conjugating enzymes involved in protein degradation. EMBO J. 1990 Dec;9(13):4535–4541. [PubMed]
  • Sheffield WP, Shore GC, Randall SK. Mitochondrial precursor protein. Effects of 70-kilodalton heat shock protein on polypeptide folding, aggregation, and import competence. J Biol Chem. 1990 Jul 5;265(19):11069–11076. [PubMed]
  • Silver LM, Artzt K, Bennett D. A major testicular cell protein specified by a mouse T/t complex gene. Cell. 1979 Jun;17(2):275–284. [PubMed]
  • Skowyra D, Georgopoulos C, Zylicz M. The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell. 1990 Sep 7;62(5):939–944. [PubMed]
  • Slater MR, Craig EA. Transcriptional regulation of an hsp70 heat shock gene in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1987 May;7(5):1906–1916. [PMC free article] [PubMed]
  • Slater MR, Craig EA. The SSA1 and SSA2 genes of the yeast Saccharomyces cerevisiae. Nucleic Acids Res. 1989 Jan 25;17(2):805–806. [PMC free article] [PubMed]
  • Khorana HG. Rhodopsin, photoreceptor of the rod cell. An emerging pattern for structure and function. J Biol Chem. 1992 Jan 5;267(1):1–4. [PubMed]
  • Squires CL, Pedersen S, Ross BM, Squires C. ClpB is the Escherichia coli heat shock protein F84.1. J Bacteriol. 1991 Jul;173(14):4254–4262. [PMC free article] [PubMed]
  • Stamnes MA, Zuker CS. Peptidyl-prolyl cis-trans isomerases, cyclophilin, FK506-binding protein, and ninaA: four of a kind. Curr Opin Cell Biol. 1990 Dec;2(6):1104–1107. [PubMed]
  • Straus D, Walter W, Gross CA. DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32. Genes Dev. 1990 Dec;4(12A):2202–2209. [PubMed]
  • Tachikawa H, Miura T, Katakura Y, Mizunaga T. Molecular structure of a yeast gene, PDI1, encoding protein disulfide isomerase that is essential for cell growth. J Biochem. 1991 Aug;110(2):306–313. [PubMed]
  • Ursic D, Culbertson MR. The yeast homolog to mouse Tcp-1 affects microtubule-mediated processes. Mol Cell Biol. 1991 May;11(5):2629–2640. [PMC free article] [PubMed]
  • Ursic D, Ganetzky B. A Drosophila melanogaster gene encodes a protein homologous to the mouse t complex polypeptide 1. Gene. 1988 Sep 7;68(2):267–274. [PubMed]
  • Vogel JP, Misra LM, Rose MD. Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast. J Cell Biol. 1990 Jun;110(6):1885–1895. [PMC free article] [PubMed]
  • Walter P, Lingappa VR. Mechanism of protein translocation across the endoplasmic reticulum membrane. Annu Rev Cell Biol. 1986;2:499–516. [PubMed]
  • Werner-Washburne M, Becker J, Kosic-Smithers J, Craig EA. Yeast Hsp70 RNA levels vary in response to the physiological status of the cell. J Bacteriol. 1989 May;171(5):2680–2688. [PMC free article] [PubMed]
  • Werner-Washburne M, Stone DE, Craig EA. Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae. Mol Cell Biol. 1987 Jul;7(7):2568–2577. [PMC free article] [PubMed]
  • Wiech H, Buchner J, Zimmermann R, Jakob U. Hsp90 chaperones protein folding in vitro. Nature. 1992 Jul 9;358(6382):169–170. [PubMed]
  • Willison K, Kelly A, Dudley K, Goodfellow P, Spurr N, Groves V, Gorman P, Sheer D, Trowsdale J. The human homologue of the mouse t-complex gene, TCP1, is located on chromosome 6 but is not near the HLA region. EMBO J. 1987 Jul;6(7):1967–1974. [PubMed]
  • Willison KR, Dudley K, Potter J. Molecular cloning and sequence analysis of a haploid expressed gene encoding t complex polypeptide 1. Cell. 1986 Mar 14;44(5):727–738. [PubMed]
  • Yaffe MB, Farr GW, Miklos D, Horwich AL, Sternlicht ML, Sternlicht H. TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature. 1992 Jul 16;358(6383):245–248. [PubMed]
  • Zimmermann R, Sagstetter M, Lewis MJ, Pelham HR. Seventy-kilodalton heat shock proteins and an additional component from reticulocyte lysate stimulate import of M13 procoat protein into microsomes. EMBO J. 1988 Sep;7(9):2875–2880. [PubMed]

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