Stress protein systems of mammalian cells.

Living organisms are known to react to a heat stress by the selective induction in the synthesis of several polypeptides. In this review we list the major stress proteins of mammalian cells that are induced by heat shock and other environments and categorize these proteins into specific subgroups: the major heat shock proteins, the glucose-regulated proteins, and the low-molecular-weight heat shock proteins. Characteristics of the localization and expression of proteins in each of these subgroups are presented. Specifically, the nuclear/nucleolar locale of certain of the major heat shock proteins is considered with respect to their association with RNA and the recovery of cells after a heat exposure. The induction of these major heat shock proteins and the repression of the glucose-regulated proteins as a result of reoxygenation of anoxic cells or by the addition of glucose to glucose-deprived cultures is described. Changes in the expression of these protein systems during embryogenesis and differentiation in mammalian and nonmammalian systems is summarized, and the protective role that some of these proteins appear to play in protecting the animal against the lethal effects of a severe heat treatment and against teratogenesis is critically examined.

[1]  M. Kloc,et al.  Acquisition of the heat-shock response and thermotolerance during early development of Xenopus laevis. , 1985, Developmental biology.

[2]  H. Pelham.  Hsp70 accelerates the recovery of nucleolar morphology after heat shock. , 1984, The EMBO journal.

[3]  J. Spotila.  Role of Temperature and Water in the Ecology of Lungless Salamanders , 1972 .

[4]  W. Loomis,et al.  Heat shock response of Dictyostelium. , 1980, Developmental biology.

[5]  J. Subjeck,et al.  The effects of glucose on protein synthesis and thermosensitivity in Chinese hamster ovary cells. , 1983, The Journal of biological chemistry.

[6]  J. Landry,et al.  Relationship between hyperthermia-induced heat-shock proteins and thermotolerance in Morris hepatoma cells. , 1983, Canadian journal of biochemistry and cell biology = Revue canadienne de biochimie et biologie cellulaire.

[7]  R. Tanguay,et al.  Intracellular translocation of cellular and heat shock induced proteins upon heat shock in Drosophila Kc cells. , 1982, Canadian journal of biochemistry.

[8]  V. H. Hutchison.  Factors influencing thermal tolerances of individual organisms , 1976 .

[9]  K. Lanks,et al.  Antagonistic effects of insulin and dexamethasone on glucose‐regulated and heat shock protein synthesis , 1985, Journal of cellular physiology.

[10]  G. Hahn,et al.  Ethanol-induced tolerance to heat and to adriamycin , 1978, Nature.

[11]  N. J. McNally,et al.  Cytotoxicity of adriamycin to tumour cells in vivo and in vitro. , 1980, British Journal of Cancer.

[12]  J Jackson,et al.  Induction of four proteins in chick embryo cells by sodium arsenite. , 1980, The Journal of biological chemistry.

[13]  S. Fakan,et al.  Localization of the heat shock-induced proteins in Drosophila melanogaster tissue culture cells. , 1980, Developmental biology.

[14]  M. Ashburner,et al.  The induction of gene activity in drosophila by heat shock , 1979, Cell.

[15]  M. Olson,et al.  Distribution of proteins among chromatin components of nucleoli. , 1983, Biochemistry.

[16]  A. Shearn,et al.  Developmental regulation of Drosophila imaginal disc proteins: synthesis of a heat shock protein under non-heat-shock conditions. , 1983, Developmental biology.

[17]  J. Weatherbee,et al.  Purification and reconstitution of HeLa cell microtubules. , 1980, Biochemistry.

[18]  K. Lanks.  Metabolite regulation of heat shock protein levels. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[19]  J. M. Velazquez,et al.  hsp70: Nuclear concentration during environmental stress and cytoplasmic storage during recovery , 1984, Cell.

[20]  V. H. Hutchison,et al.  The critical thermal maximum as a determinant of thermal tolerance in Mus musculus , 1982 .

[21]  M. Morange,et al.  Heat shock proteins, first major products of zygotic gene activity in mouse embryo , 1983, Nature.

[22]  R. Mitchel,et al.  Heat-shock induction of ionizing radiation resistance in Saccharomyces cerevisiae, and correlation with stationary growth phase. , 1982, Radiation research.

[23]  K. Lanks,et al.  Dexamethasone can modulate glucose‐regulated and heat shock protein synthesis , 1983, Journal of cellular physiology.

[24]  K. Henle,et al.  Heat fractionation and thermotolerance: a review. , 1978, Cancer research.

[25]  E. Gerner,et al.  Polyamines: a dual role in the modulation of cellular sensitivity to heat. , 1982, Radiation research.

[26]  I. Pastan,et al.  Glucose depletion accounts for the induction of two transformation-sensitive membrane proteinsin Rous sarcoma virus-transformed chick embryo fibroblasts. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[27]  A. Konings,et al.  Role of membrane lipids and membrane fluidity in thermosensitivity and thermotolerance of mammalian cells. , 1985, Radiation research.

[28]  J. Belli,et al.  Enhanced survival of adriamycin-treated Chinese hamster cells by 2-deoxy-D-glucose and 2,4-dinitrophenol. , 1982, Cancer research.

[29]  R. Gomer,et al.  Heat shock proteins are methylated in avian and mammalian cells. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[30]  N. Marceau,et al.  Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. , 1982, Cancer research.

[31]  J. Nevins,et al.  Common control of the heat shock gene and early adenovirus genes: evidence for a cellular E1A-like activity , 1984, Molecular and cellular biology.

[32]  B. Ames,et al.  AppppA, heat-shock stress, and cell oxidation. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[33]  R. Morimoto,et al.  Cell-specific expression of heat shock proteins in chicken reticulocytes and lymphocytes , 1984, The Journal of cell biology.

[34]  W. Dewey,et al.  Variation in sensitivity to heat shock during the cell-cycle of Chinese hamster cells in vitro. , 1971, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[35]  F. Neidhardt,et al.  The genetics and regulation of heat-shock proteins. , 1984, Annual review of genetics.

[36]  I. Brown,et al.  Heat shock protein in mammalian brain and other organs after a physiologically relevant increase in body temperature induced by D-lysergic acid diethylamide. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Olson,et al.  Comparison of nucleolar proteins of normal rat liver and Novikoff hepatoma ascites cells by two-dimensional polyacrylamide gel electrophoresis. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Murnane,et al.  Effect of heat shock on the intracellular distribution of proteins. , 1985, Radiation research.

[39]  E. Craig,et al.  Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[40]  P. Morris,et al.  Putative function of Drosophila melanogaster heat shock proteins in the nucleoskeleton. , 1981, The Journal of biological chemistry.

[41]  A. Delegeane,et al.  Highly conserved glucose-regulated protein in hamster and chicken cells: preliminary characterization of its cDNA clone. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Kenneth M. Yamada,et al.  Isolation and immunological characterization of a glucose-regulated fibroblast cell surface glycoprotein and its nonglycosylated precursor , 1978, Cell.

[43]  W. W. Reynolds,et al.  Survival value of fever in fish , 1977, Nature.

[44]  J. Brugge,et al.  Association of the transforming proteins of Rous, Fujinami, and Y73 avian sarcoma viruses with the same two cellular proteins , 1982, Molecular and cellular biology.

[45]  L. Erickson,et al.  Calorimetric studies of the structural transitions of the human erythrocyte membrane. The involvement of spectrin in the A transition. , 1977, Biochemistry.

[46]  K. Smetana,et al.  Evidence from studies on segregated nucleoli that nucleolar silver staining proteins C23 and B23 are in the fibrillar component. , 1980, Experimental cell research.

[47]  W. Welch,et al.  Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells. , 1984, The Journal of biological chemistry.

[48]  R. Hallberg,et al.  Induction of acquired thermotolerance in Tetrahymena thermophila: effects of protein synthesis inhibitors , 1985, Molecular and cellular biology.

[49]  C. Markert,et al.  Diverse forms of stress lead to new patterns of gene expression through a common and essential metabolic pathway. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[50]  John Yu,et al.  Accumulation of a heat shock-like protein during differentiation of human erythroid cell line K562 , 1984, Nature.

[51]  B. Atkinson,et al.  Effect of heat shock on gene expression in human epidermoid carcinoma cells (strain KB) and in primary cultures of mammalian and avian cells. , 1982, Canadian journal of biochemistry.

[52]  M. Meselson,et al.  Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock , 1983, Cell.

[53]  M. Di Bernardo,et al.  Synthesis of heat-shock proteins in developing sea urchins. , 1981, Developmental biology.

[54]  G. Li,et al.  Elevated levels of 70,000 dalton heat shock protein in transiently thermotolerant Chinese hamster fibroblasts and in their stable heat resistant variants. , 1985, International journal of radiation oncology, biology, physics.

[55]  B. Lai,et al.  Quantitation and intracellular localization of the 85K heat shock protein by using monoclonal and polyclonal antibodies , 1984, Molecular and cellular biology.

[56]  S. P. Tomasovic,et al.  Heat transient related changes in stress-protein synthesis. , 1985, Radiation research.

[57]  W. Welch,et al.  Rapid purification of mammalian 70,000-dalton stress proteins: affinity of the proteins for nucleotides. , 1985, Molecular and cellular biology.

[58]  M. Olson,et al.  Localization of phosphoprotein C23 in nucleoli by immunological methods. , 1981, Experimental cell research.

[59]  A. Goldberg,et al.  Production of abnormal proteins in E. coli stimulates transcription of ion and other heat shock genes , 1985, Cell.

[60]  W. Welch.  Phorbol ester, calcium ionophore, or serum added to quiescent rat embryo fibroblast cells all result in the elevated phosphorylation of two 28,000-dalton mammalian stress proteins. , 1985, The Journal of biological chemistry.

[61]  K. Sirotkin,et al.  Ecdysterone induces the transcription of four heat-shock genes in Drosophila S3 cells and imaginal discs. , 1982, Developmental biology.

[62]  B. Wittig,et al.  Heat shock gene expression is regulated during teratocarcinoma cell differentiation and early embryonic development. , 1983, Developmental biology.

[63]  R. Warocquier,et al.  RNA metabolism in mammalian cells at elevated temperature. , 1969, European journal of biochemistry.

[64]  M. Czech,et al.  Reconstituted D-glucose transport from the adipocyte plasma membrane. Chromatographic resolution of transport activity from membrane glycoproteins using immobilized concanavalin A. , 1980, Biochemistry.

[65]  J. Lepock,et al.  Involvement of membranes in cellular responses to hyperthermia. , 1982, Radiation research.

[66]  Y. J. Kim,et al.  Nuclear localization and phosphorylation of three 25-kilodalton rat stress proteins , 1984, Molecular and cellular biology.

[67]  K. Henle,et al.  Effects of Hyperthermia (45°) on Macromolecular Synthesis in Chinese Hamster Ovary Cells , 1979 .

[68]  J. Zalta,et al.  Effet de la température supra-optimale sur les ribonucléoprotéines et le RNA nucléolaire: II. Etude biochimique , 1969 .

[69]  J. August,et al.  Coprecipitation of heat shock proteins with a cell surface glycoprotein. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[70]  T. Kinsella,et al.  Glutathione elevation during thermotolerance induction and thermosensitization by glutathione depletion. , 1983, Cancer research.

[71]  R. Johnson,et al.  Heat shock proteins and thermotolerance; a comparison of induction kinetics. , 1982, The British journal of radiology.

[72]  B. Babiarz,et al.  Distribution of a 100K dalton glucose-regulated cell surface protein in mammalian cell cultures and sectioned tissues. , 1982, Experimental cell research.

[73]  T. Herman,et al.  Polyhydroxy compounds and thermotolerance: a proposed concatenation. , 1982, Radiation research.

[74]  V. H. Hutchison,et al.  The Role of Behavior in Temperature Acclimation and Tolerance in Ectotherms , 1979 .

[75]  J. Brugge,et al.  Interaction between the Rous sarcoma virus transforming protein and two cellular phosphoproteins: analysis of the turnover and distribution of this complex , 1983, Molecular and cellular biology.

[76]  S. Lindquist,et al.  The heat shock response is self-regulated at both the transcriptional and posttranscriptional levels , 1982, Cell.

[77]  M. Schlesinger,et al.  Antibodies to two major chicken heat shock proteins cross-react with similar proteins in widely divergent species , 1982, Molecular and cellular biology.

[78]  I. Pastan,et al.  Induction of two transformation-sensitive membrane polypeptides in normal fibroblasts by a block in glycoprotein synthesis or glucose deprivation , 1977, Cell.

[79]  P. Braude,et al.  The transition from maternal to embryonic control in the 2‐cell mouse embryo. , 1982, The EMBO journal.

[80]  E. Berger,et al.  Small heat shock proteins in Drosophila may confer thermal tolerance. , 1983, Experimental cell research.

[81]  E. Lazarides,et al.  ADP-ribosylation of the Mr 83,000 stress-inducible and glucose-regulated protein in avian and mammalian cells: modulation by heat shock and glucose starvation. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[82]  M. Schlesinger,et al.  The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts , 1978, Cell.

[83]  C. Heidelberger,et al.  Studies on the quantitative biology of hyperthermic killing of HeLa cells. , 1973, Cancer research.

[84]  K. Scharf,et al.  Heat shock induced changes of plant cell ultrastructure and autoradiographic localization of heat shock proteins. , 1984, European journal of cell biology.

[85]  N. Marceau,et al.  Thermotolerance and heat shock proteins induced by hyperthermia in rat liver cells. , 1982, International journal of radiation oncology, biology, physics.

[86]  R. van Wijk,et al.  Thermotolerance in cultured hepatoma cells: cell viability, cell morphology, protein synthesis, and heat-shock proteins. , 1984, Radiation research.

[87]  V. H. Hutchison,et al.  Acute adjustment of thermal tolerance in vertebrate ectotherms following exposure to critical thermal maxima , 1980 .

[88]  K. Scharf,et al.  Formation of cytoplasmic heat shock granules in tomato cell cultures and leaves , 1983, Molecular and cellular biology.

[89]  J. Subjeck,et al.  Induction of glucose-regulated proteins during anaerobic exposure and of heat-shock proteins after reoxygenation. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[90]  A. Varshavsky,et al.  Heat-shock proteins of Drosophila are associated with nuclease- resistant, high-salt-resistant nuclear structures , 1981, The Journal of cell biology.

[91]  A. Ciechanover,et al.  Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutant ts85 , 1984, Cell.

[92]  H. K. Mitchell,et al.  Specific protection from phenocopy induction by heat shock , 1979 .

[93]  Y. J. Kim,et al.  Phosphorylation pattern of a 25 Kdalton stress protein from rat myoblasts. , 1983, Biochemical and Biophysical Research Communications - BBRC.

[94]  Gloria C. Li.  Induction of thermotolerance and enhanced heat shock protein synthesis in chinese hamster fibroblasts by sodium arsenite and by ethanol , 1983, Journal of cellular physiology.

[95]  H. Oppermann,et al.  Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. , 1980, Biochimica et biophysica acta.

[96]  C. Preston,et al.  Activation of cellular stress protein genes by herpes simplex virus temperature-sensitive mutants which overproduce immediate early polypeptides. , 1982, Virology.

[97]  H. K. Mitchell,et al.  Heat shock and Phenocopy induction in Drosophila , 1978, Cell.

[98]  H. Oppermann,et al.  A cellular protein that associates with the transforming protein of Rous sarcoma virus is also a heat-shock protein. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[99]  Z. Werb,et al.  Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[100]  A. Tissières,et al.  Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. , 1974, Journal of molecular biology.

[101]  H. Eichholtz-Wirth,et al.  Effect of different physiological conditions on the action of adriamycin on Chinese hamster cells in vitro. , 1981, British Journal of Cancer.

[102]  U. Bond,et al.  Ubiquitin is a heat shock protein in chicken embryo fibroblasts , 1985, Molecular and cellular biology.

[103]  G. Crile.  The effects of heat and radiation on cancers implanted on the feet of mice. , 1963, Cancer research.

[104]  M. Morange,et al.  Spontaneous high expression of heat‐shock proteins in mouse embryonal carcinoma cells and ectoderm from day 8 mouse embryo. , 1983, The EMBO journal.

[105]  C. Zala,et al.  In cultured chick embryo fibroblasts the hexose transport components are not the 75 000 and 95 000 dalton polypeptides synthesized following glucose deprivation. , 1980, Canadian journal of biochemistry.

[106]  G. Hahn,et al.  Differential effects of hyperthermia on the Na+,K+-ATPase of Chinese hamster ovary cells. , 1985, Radiation research.

[107]  D. Finkelstein,et al.  Heat shock proteins and thermal resistance in yeast. , 1980, Biochemical and biophysical research communications.

[108]  R. Milkman.  Temperature Effects on Day Old Drosophila Pupae , 1962, The Journal of general physiology.

[109]  B. Hille,et al.  ANALYSIS OF SOME TEMPERATURE EFFECTS ON DROSOPHILA PUPAE , 1966 .

[110]  J. Subjeck,et al.  Heat shock proteins and protection of proliferation and translation in mammalian cells. , 1984, Cancer research.

[111]  H. Biessmann,et al.  Two Drosophila melanogaster proteins related to intermediate filament proteins of vertebrate cells , 1981, The Journal of cell biology.

[112]  R. Tanguay,et al.  Heat-shock induced proteins present in the cell nucleus of Chironomus tentans salivary gland , 1979, Nature.

[113]  K. Minton,et al.  Nonspecific stabilization of stress-susceptible proteins by stress-resistant proteins: a model for the biological role of heat shock proteins. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[114]  M. Perry,et al.  The major heat-shock protein (hsp70) gene family: related sequences in mouse, Drosophila, and yeast. , 1983, Canadian journal of biochemistry and cell biology = Revue canadienne de biochimie et biologie cellulaire.

[115]  R. Lamb,et al.  Infection with paramyxoviruses stimulates synthesis of cellular polypeptides that are also stimulated in cells transformed by Rous sarcoma virus or deprived of glucose. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[116]  R. Morimoto,et al.  Studies of cloned sequences from four drosophila heat shock loci , 1979, Cell.

[117]  K. Henle,et al.  Modification of the heat response and thermotolerance by cycloheximide, hydroxyurea, and lucanthone in CHO cells. , 1982, Radiation research.

[118]  T. Delaney,et al.  Persistence of thermotolerance in slowly proliferating plateau-phase cells. , 1984, Radiation research.

[119]  J. Smith,et al.  Human Lymphocyte Responses Are Enhanced by Culture at 40°C , 1978, The Journal of Immunology.

[120]  M. Harris.  Growth and survival of mammalian cells under continuous thermal stress. , 1969, Experimental cell research.

[121]  LaThangue Nb.  A major heat-shock protein defined by a monoclonal antibody. , 1984 .

[122]  K. Scharf,et al.  Synthesis, modification and structural binding of heat-shock proteins in tomato cell cultures. , 1984, European journal of biochemistry.

[123]  G. Adams,et al.  Cytotoxicity of adriamycin on aerobic and hypoxic chinese hamster V79 cells in vitro. , 1980, British Journal of Cancer.

[124]  K. Smetana,et al.  Proteins C23 and B23 are the major nucleolar silver staining proteins. , 1979, Life sciences.

[125]  H. Varmus,et al.  Two cellular proteins that immunoprecipitate with the transforming protein of Rous sarcoma virus. , 1981, Virology.

[126]  N. Roberts,et al.  Hyperthermia and human leukocyte functions: effects on response of lymphocytes to mitogen and antigen and bactericidal capacity of monocytes and neutrophils , 1977, Infection and immunity.

[127]  J. Garrels,et al.  Biochemical characterization of the mammalian stress proteins and identification of two stress proteins as glucose- and Ca2+-ionophore-regulated proteins. , 1983, The Journal of biological chemistry.

[128]  M. Morange,et al.  Altered expression of heat shock proteins in embryonal carcinoma and mouse early embryonic cells , 1984, Molecular and cellular biology.

[129]  M. Pouchelet,et al.  Localization of the 70 000 dalton heat-induced protein in the nuclear matrix of BHK cells. , 1983, Experimental cell research.

[130]  J. Subjeck,et al.  Analysis of the expression of the two major proteins of the 70 kilodalton mammalian heat shock family. , 1985, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[131]  E. Berger,et al.  Synthesis of low molecular weight heat shock peptides stimulated by ecdysterone in a cultured Drosophila cell line. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[132]  E. Craig,et al.  Expression of Drosophila heat-shock cognate genes during heat shock and development. , 1983, Developmental biology.

[133]  G. Li,et al.  Amino acid analogs while inducing heat shock proteins sensitize CHO cells to thermal damage , 1985, Journal of cellular physiology.

[134]  J. Nevins.  Induction of the synthesis of a 70,000 dalton mammalian heat shock protein by the adenovirus E1A gene product , 1982, Cell.

[135]  M. Olson,et al.  Amino acid sequence and sites of phosphorylation in a highly acidic region of nucleolar nonhistone protein C23. , 1979, Biochemistry.

[136]  S. P. Tomasovic,et al.  Heat-stress proteins and thermal resistance in rat mammary tumor cells. , 1983, Radiation research.

[137]  K. Henle,et al.  Interaction of hyperthermia and radiation in CHO cells: recovery kinetics. , 1976, Radiation research.

[138]  E. Craig,et al.  Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[139]  R. Currie,et al.  Trauma-induced protein in rat tissues: a physiological role for a "heat shock" protein? , 1981, Science.