142
Views
183
CrossRef citations to date
0
Altmetric
Original Article

Heat shock proteins, thermotolerance, and their relevance to clinical hyperthermia

, &
Pages 459-488 | Received 06 Sep 1994, Accepted 01 Dec 1994, Published online: 09 Jul 2009

References

  • Abravaya K., Myers M. P., Murphy S. P., Morimoto R. I. The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Development 1992; 6: 1153–1164
  • Anderson R. L., Kapp D. S., Woo S. S., Rice G. C., Lee K. J., Hahn G. M. Predictive assays for human response to single and multiple fractions of hyperthermia. Recent Results in Cancer Research 1988; 109: 240–249
  • Anderson R. L., Tao T. W., Betten D. A., Hahn G. M. Heat shock protein levels are not elevated in heat resistant B16 melanoma cells. Radiation Research 1986; 105: 240–246
  • Hyperthermia in Cancer Treatment, L. J. Anghileri, J. Robert. CRC Press, Boca Raton 1986; vol. 1
  • Arrigo A. P. Cellular localization of HSP23 during Drosophila development and subsequent heat shock. Developmental Biology 1987; 122: 39–48
  • Baler R., Welch W. J., Voellmy R. J. Heat shock gene regulation by nascent polypeptides and denatured proteins: hsp70 as a potential autoregulatory factor. Journal of Cell Biology 1992; 117: 1151–1159
  • Bauer K. D., Henle K. J. Arrhenius analysis of heat survival curves from normal and thermotolerant CHO cells. Radiation Research 1979; 78: 251–263
  • Baulieu E. E. Steroid hormone antagonists at the receptor level: a role for the heat shock protein MW 90,000 (hsp 90). Journal of Cellular Biochemistry 1987; 35: 161–174
  • Bienz M., Pelham H. R. B. Mechanisms of heat shock gene activation in higher eukaryotes. Advances in Genetics 1987; 24: 31–72
  • Black A. R., Subjeck J. R. Involvement of rRNA synthesis in the enhanced survival and recovery of protein synthesis seen in thermotolerance. Journal of Cellular Physiology 1989; 138: 439–449
  • Brustad T., Rofstad E. K. Effects of heat treatment in vitro and in vivo on human melanoma xenografts. Recent Results in Cancer Research 1988; 109: 183–197
  • Calderwood S. K., Stevenson M. A., Hahn G. M. Cyclic AMP and the heat shock response in Chinese hamster ovary cells. Biochemical and Biophysical Research Communications 1985; 126: 912–916
  • Calderwood S. K., Stevenson M. A., Hahn G. M. Heat stress stimulates inositol trisphosphate release and phosphorylation of phosphoinositides in CHO and Balb C 3T3 cells. Journal of Cellular Physiology 1987; 130: 369–376
  • Chappell T. G., Konforti B. B., Schmid S. L., Rothman J. E. The ATPase core of a clathrin uncoating protein. Journal of Biological Chemistry 1987; 262: 746–751
  • Chappell T. G., Welsh W. J., Schlossman D. M., Palter K. B., Schlesinger M. J., Rothman J. E. Uncoating ATPase is a member of the 70 kilodalton family of stress protein. Cell 1986; 45: 3–13
  • Cheng M. Y., Hartl F. U., Martin J., Pollock R. A., Kalousek F., Neupert W., Hallberg E. M., Hallberg R. L., Horwich A. L. Mitochondrial heat-shock protein hsp70 is essential for assembly of proteins imported into yeast mitochondria. Nature 1989; 337: 620–625
  • Chiang H. L., Terlecky S. R., Plant C. P., Dice J. F. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 1989; 246: 382–385
  • Chirico W. J., Waters M. G., Blobel G. 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 1988; 332: 805–810
  • Craig E. A., Jacobsen L. Mutations of the heat inducible 70 kilodalton genes of yeast confer temperature sensitive growth. Cell 1985; 38: 841–849
  • Deshaies R. J., Koch B. D., Werner-Washburne M., Craig E. A., Schekman R. A subfamily of stress protein facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 1988; 332: 800–805
  • Ellis R. J., Van derVies S. M. Molecular chaperones. Annual Review of Biochemistry 1991; 60: 321–347
  • Engelhardt R. Hyperthermia and drugs. Recent Results in Cancer Research 1987; 104: 133–203
  • Findly R. C., Penderson T. Regulated transcription of the genes for actin and heat shock proteins in Drosophila cells. Journal of Cell Biology 1981; 88: 323–328
  • Gautherie M. Biological Basis of Oncologic Thermotherapy. Springer, Berlin 1990
  • Georgopoulos C. The emergence of the chaperone machines. Trends in Biochemical Science 1992; 17: 295–299
  • Gerner E. W., Schneider M. J. Induced thermal resistance in HeLa cells. Nature London 1975; 256: 500–502
  • Gerweck L. E. Modification of cell lethality at elevated temperatures. The pH effect. Radiation Research 1977; 70: 224–235
  • Gething M. J., Sambrook J. Protein folding in the cell. Nature (London) 1992; 355: 33–45
  • Hahn G. M. Hyperthermia and Cancer. Plenum, New York 1982
  • Hahn G. M., Li G. C. Thermotolerance, thermoresistance and thermosensitization. Stress Proteins in Biology and Medicine, R. Morimoto, A. Tissieres, C. Georgopoulos. Cold Spring Harbor Laboratory Press, Plainview 1990; 79–100
  • Hahn G. M., Van Kersen I. Isolation and initial characterization of thermoresistant RIF tumor cell strains. Cancer Research 1988; 48: 1803–1807
  • Hahn G. M., Shiu E. C. Protein synthesis, thermotolerance and step down heating. International Journal of Radiation Oncology, Biology and Physics 1985; 11: 159–164
  • Harisiadis L., Sung D. I., Hall E. J. Thermal tolerance and repair of thermal damage by cultured cells. Radiology 1977; 123: 505–509
  • Henle K. J. Thermotolerance in the murine jejunum. Journal of the National Cancer Institute 1982; 68: 1033–1036
  • Henle K. J., Dethlefsen L. A. Heat fractionation and thermotolerance: a review. Cancer Research 1978; 38: 1843–1851
  • Henle K. J., Leeper D. B. Effects of hyperthermia (45°C) on macromolecular synthesis in Chinese hamster ovary cells. Cancer Research 1979; 39: 2655–2674
  • Henle K. J., Leeper D. B. Interaction of hyperthermia and radiation in CHO cells: recovery kinetics. Radiation Research 1976; 66: 505–518
  • Henle K. J., Leeper D. B. Modification of the heat response and thermotolerance by cycloheximide, hydroxyurea, and lucanthone in CHO cells. Radiation Research 1982; 90: 339–347
  • Hightower L. F., White F. P. Cellular response to stress: comparison of a family of 71–73 kilodalton proteins rapidly synthesized in rat tissue slices and canavanine-treated cells in culture. Journal of Cellular Physiology 1981; 108: 261–275
  • Hume S. P., Marigold J. C. L. Transient heat-induced thermal resistance in the small intestine of mouse. Radiation Research 1980; 82: 526–535
  • Hunt C., Morimoto R. I. Conserved features of eukaryotic HSP70 genes revealed by comparison with the nucleotide sequence of human HSP70. Proceedings of the National Academy of Sciences, USA 1985; 82: 6455–6459
  • Johnston R. N., Kucey B. L. Competitive inhibition of hsp70 gene expression causes thermosensitivity. Science 1988; 242: 1551–1554
  • Jorritsma J. B. M., Burgman P., Kampinga H. H., Konings A. W. T. DNA polymerase activity in heat killing and hyperthermic radiosensitization of mammalian cells as observed after fractionated heat treatments. Radiation Research 1986; 105: 307–319
  • Kampinga H. H., Turkel-Uygur N., Roti J. L., Konings A. W. T. The relationship of increased nuclear proteins content induced by hyperthermia to killing of HeLa S3 cells. Radiation Research 1989; 117: 511–522
  • Landry S., Bernier D., Chretien P., Nicole L. M., Tanguay R. M., Marceau N. Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Research 1982; 42: 2457–2461
  • Landry J., Chretien P. Relationship between hyperthermia-induced heat shock proteins and thermotolerance in Morris hepatoma cells. Canadian Journal of Biochemistry and Cell Biology 1983; 61: 428–437
  • Laszlo A., Li G. C. Heat resistant variants of Chinese hamster fibroblasts altered in expression of heat shock protein. Proceedings of the National Academy of Sciences, USA 1985; 82: 8029–8033
  • Laszlo A., Li G. C. Effect of amino acid analogs on the development of thermotolerance and on thermotolerant cells. Journal of Cellular Physiology 1993; 154: 419–432
  • Law M. P. The induction of thermal resistance in the mouse ear by heating at temperatures ranging from 41·5°C. Radiation Research 1981; 85: 126–134
  • Law M. P., Ahier R. G., Somaia S. Thermotolerance induced by fractionated hyperthermia: dependence on the interval between fractions. International Journal of Hyperthermia 1987; 3: 433–439
  • Li G. C. Elevated levels of 70,000 dalton heat shock protein in transiently thermotolerant Chinese hamster fibroblasts and in their heat stable variants. International Journal of Radiation Oncology, Biology and Physics 1985; 11: 165–177
  • Li G. C. HSP70 as an indicator of thermotolerance. Hyperthermic Oncology, T. Sugahara, M. Saito. Taylor & Francis, Philadelphia 1988; vol. 2: 256–259
  • Li G. C., Hahn G. M. Induction of thermotolerance and evidence for a well-defined, thermotropic cooperative process. Radiation Research 1982; 89: 361–368
  • Li G. C., Laszlo A. Amino acid analogs while inducing heat shock proteins sensitize CHO cells to thermal damage. Journal of Cellular Physiology 1985; 122: 91–97
  • Li G. C., Li L., Liu R. Y., Rehman M., Lee W. M. F. Heat shock protein hsp70 protects cells from thermal stress even after deletion of its ATP-binding domain. Proceedings of the National Academy of Sciences, USA 1992; 89: 2036–2040
  • Li G. C., Li L., Liu Y. K., Mak J. Y., Chen L., Lee W. F. Thermal response of rat fibroblasts stably transfected with the human 70-kDa heat shock protein-encoding gene. Proceedings of the National Academy of Sciences, USA 1991; 88: 681–1685
  • Li G. C., Mak J. Y. Induction of heat shock proteins during the development of thermotolerance in murine tumours. Cancer Research 1985; 45: 3816–3824
  • Li G. C., Mak J. Y. Re-induction of hsp70 synthesis: an assay for thermotolerance. International Journal of Hyperthermia 1989; 5: 389–403
  • Li G. C., Meyer J. L., Mak J. Y., Hahn G. M. Heat induced protection of mice against thermal death. Cancer Research 1983; 43: 5758–5760
  • Li G. C., Mivechi N. F. Thermotolerance in mammalian systems: A review. Hyperthermia in Cancer Treatment, L. J. Anghileri, J. Robert. CRC Press, Boca Raton 1986; vol. 1: 59–77
  • Li G. C., Petersen N. S., Mitchell H. K. Induced thermal tolerance and heat shock protein synthesis in Chinese hamster ovary cells. International Journal of Radiation Oncology, Biology and Physics 1982; 8: 63–67
  • Li G. C., Werb Z. Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. Proceedings of the National Academy of Sciences, USA 1982; 79: 3219–3222
  • Li D. J., Zhou S. L., Qiu S. L., Qiao S. J. Thermodamage, thermosensitivity and thermotolerance of normal swine oesophagus. International Journal of Hyperthermia 1987; 3: 143–151
  • Lindquist S. The heat shock response. Annual Review of Biochemistry 1986; 55: 1151–1191
  • Lindquist S., Craig E. A. The heat shock proteins. Annual Review of Genetics 1988; 22: 631–677
  • Liu R. Y., Li X., Li L., Li G. C. Expression of human hsp70 in rat fibroblasts enhances cell survival and facilitates recovery from translational and transcriptional inhibition following heat shock. Cancer Research 1992; 52: 3667–3673
  • Martinez A. A., Meshorer A., Meyer J. L., Hahn G. M., Fajardo L. F. Thermal sensitivity and thermotolerance in normal porcine tissues. Cancer Research 1983; 43: 2072–2075
  • Marquez C. M., Sneed P. K., Li G. C., Mak J. Y., Phillips T. L. Hsp70 synthesis in clinical hyperthermia patients: preliminary results of a new technique. International Journal of Radiation Oncology, Biology and Physics 1993; 28: 425–430
  • Milligan A. J., Metz J. A., Leeper D. B. Effect of intestinal hyperthermia in the Chinese hamster. International Journal of Radiation Oncology, Biology and Physics 1984; 10: 259–263
  • Mivechi N. F. Heat sensitivity, thermotolerance and profile of protein synthesis of human bone marrow progenitors. Cancer Research 1988; 48: 3630–3633
  • Mivechi N. F. Heat sensitivity, thermotolerance and profile of heat shock protein synthesis of human myelogenous leukemias. Cancer Research 1989; 49: 1954–1958
  • Mivechi N. F., Li G. C. Thermotolerance and profile of protein synthesis in murine bone marrow cells after heat shock. Cancer Research 1985; 45: 3843–3849
  • Mivechi N. F., Li G. C. Lack of development of thermotolerance in early progenitors of murine bone marrow cells. Cancer Research 1986; 46: 198–202
  • Mivechi N. F., Rossi J. J. Use of polymerase chain reaction to detect the expression of Mr 70,000 heat shock genes in control or heat shock leukemic cells as correlated to their heat response. Cancer Research 1990; 50: 2877–2884
  • Mizzen L. A., Welch W. J. Characterization of the thermotolerant cell I. Effects on protein synthesis activity and the regulation of heat shock protein regulation. Journal of Cell Biology 1988; 106: 1105–1116
  • Moriyama Y., Narita M., Sato K., Urushiyama M., Koyama S., Hirosawa H., Kishi K., Takahashi M., Takai K., Shibata A. Application of hyperthermia to treatment of human acute leukemia: purging human leukemia progenitor cells by heat. Blood 1986; 67: 802–804
  • Mooibroek J., Dikomey E., Zywietz F., Jung H. Thermotolerance kinetics and growth rate changes in the RIH tumor heated at 43°C. International Journal of Hyperthermia 1988; 4: 677–686
  • Morimoto R. I. Cells in stress: transcriptional activation of heat shock genes. Science 1993; 259: 1409–1410
  • Stress Proteins in Biology and MedicineMorimoto, R. I. Tissieres, A. C. Georgopoulos. Cold Spring Harbor Laboratory Press, Plainview 1990
  • The Biology of Heat Shock Proteins and Molecular Chaperones, R. I. Morimoto, A Tissieres, C. Georgopoulos. Cold Spring Harbor Laboratory Press, Plainview 1994
  • Neumann D., Scharf K. D., Nover L. Heat shock induced changes of plant cell ultra structure and autoradiographic localization of heat shock proteins. European Journal of Cell Biology 1994; 34: 254–264
  • Ohtsuka K., Laszlo A. Intracellular localization of HSP70 in normal and thermotolerance HA-1 Chinese hamster fibroblasts and in their heat resistant variantsHyperthermic Oncology. Summary Papers, T. Sugahara, M. Saito. Taylor & Francis, Tokyo 1988; 56–58
  • Palzer R. J., Heidelberger C. Studies on the quantitative biology of hyperthermic killing of HeLa cells. Cancer Research 1973; 33: 415–421
  • Pelham H. R. B. HSP70 accelerates the recovery of nuclear morphology after heat shock. EMBO Journal 1984; 3: 3095–3100
  • Pelham H. R. B. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 1986; 46: 959–961
  • Prionas S. D., Taylor M. A., Fajardo L. F., Kelly N. I., Nelsen T. S., Hahn G. M. Thermal sensitivity to single and double heat treatments in normal canine liver. Cancer Research 1985; 45: 4791–4797
  • Rhee J. G., Schuman V. C., Song C. W., Levitt S. H. Difference in the thermotolerance of mouse mammary carcinoma cells in vivo an. in vitro. Cancer Research 1987; 47: 2571–2575
  • Riabowol K. T., Mizzen L. A., Welch W. J. Heat shock is lethal to fibroblasts microinjected with antibodies against hsp70. Science 1988; 242: 433–436
  • Rice L. C., Urano M., Maher J. The kinetics of thermotolerance in the mouse foot. Radiation Research 1982a; 89: 291–297
  • Rice L. C., Urano M., Maher J., Suit H. D. Thermotolerance in a murine normal tissue system: effect of temperature of the priming dose. National Cancer Institute Monograph 1982b; 61: 279–281
  • Robins I. H., Steeves R. A., Schmitt C. L., Peterson C., Martin P. A. A hyperthermia study of differential sensitivity and thermotolerance in AKR murine leukemia and normal bone marrow cells. International Journal of Radiation Oncology, Biology and Physics 1988; 14: 979–982
  • Rofstad E. K., Brustad T. Arrhenius analysis of the heat response in vivo and in vitro of human melanoma xenografts. International Journal of Hyperthermia 1986; 2: 359–368
  • Roizin-Towle L., Pirro J. P. Thermotolerance in human cells of normal and neoplastic origin. International Journal of Hyperthermia 1988; 4: 665–675
  • Rothman J. E., Schmid S. L. Enzymatic recycling of clathrin from coated vesicles. Cell 1986; 46: 5–9
  • Sapareto S. A., Hopwood L. E., Dewey W. C., Raju M. R., Gray J. W. Effects of hyperthermia on survival and progression of Chinese hamster ovary cells. Cancer Research 1978; 38: 393–400
  • Schlesinger M., Ryan C. An ATP- and hsc70-dependent oligomerization of nascent heat-shock factor (HSF) polypeptide suggests that HSF itself could be a ‘sensor’ for the cellular stress response. Protein Science 1993; 2: 1356–1360
  • Schmid S. L., Rothman J. E. Enzymatic dissociation of clathrin cages in a two-step process. Journal of Biological Chemistry 1985; 260: 10044–10049
  • Solomon M., Rossi J. M., Golic K., McGarry T., Lindquist S. Changes in hsp70 alter thermotolerance and heat shock regulation i. Drosophila. New Biologist 1991; 3: 1106–1120
  • Song C. W., Patten M. S., Chelstrom L. M., Rhee J. G., Levitt S. H. Effect of multiple heatings on the blood flow in RIF-1 tumors, skin and muscle of C3H mice. International Journal of Hyperthermia 1987; 3: 535–545
  • Sorger P. K. Heat shock factor and the heat shock response. Cell 1991; 65: 363–366
  • Sorger P. K., Lewis M. J., Pelham H. R. B. Heat shock factor is regulated differently in yeast and HeLa cells. Nature (London) 1987; 329: 81–84
  • Sorger P. K., Pelham H. R. B. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 1988; 54: 855–864
  • Stege G. J. J., Kampinga H. H., Konings A. W. T., Li G. C. Importance of the ATP-binding domain and nucleolar localization domain of hsp72 in the protection of nuclear proteins against heat-induced aggregation. Experimental Cell Research 1994; 214: 279–284
  • Subjeck J. R., Sciandra J. J., Johnson R. J. Heat shock proteins and thermotolerance: a comparison of induction kinetics. British Journal of Radiology 1982; 55: 579–584
  • Symonds R. P., Wheldon T. E., Clarke B., Biley G. A comparison of the response to hyperthermia of murine hemopoietic stem cells (CFU-S) and L1210 leukemia cells: enhanced killing of leukemia cells in presence of normal marrow cells. British Journal of Cancer 1981; 44: 682–691
  • Tanguay R. M. Transcriptional activation of heat shock genes in eukaryotes. Biochemistry and Cell Biology 1988; 66: 584–593
  • Tomasovic S. P., Armour E. P., North S. M., Welch D. R. Rat mammary adenocarcinoma heat-stress protein in vivo. International Journal of Hyperthermia 1987a; 3: 467–473
  • Tomasovic S. P., Ramagli L. S., Simonette R. A., Wilson M. J., Rodriguez L. V. Heat stress proteins of rat lung endothelial and mammary adenocarcinoma cells. Radiation Research 1987b; 110: 45–60
  • Ungewickell E. The 70 kD mammalian heat shock proteins are structurally and functionally related to the uncoating protein that releases clathrin triskelion from coated vesicles. EMBO Journal 1985; 4: 3385–3391
  • Urano M. Kinetics of thermotolerance in normal and tumour tissues: a review. Cancer Research 1986; 46: 474–482
  • Velazquez J. M., Didomenico B. J., Lindquist S. Intracellular localization of heat shock proteins i. Drosophila. Cell 1980; 20: 679–689
  • Voellmy R., Ahmed A., Schiller P., Bromley P., Rungger D. Isolation and functional analysis of a human 70,000 dalton heat shock protein gene segment. Proceedings of the National Academy of Sciences, USA 1985; 82: 4949–4953
  • Weitzel G., Li G. C. Thermal response of yeast cells overexpressing hsp70 genes. International Journal of Hyperthermia 1993; 9: 783–797
  • Welch W. J., Feramisco J. R. Purification of the major mammalian heat shock proteins. Journal of Biological Chemistry 1984; 259: 4501–4513
  • Welch W. J., Mizzen L. A. Characterization of the thermotolerant cell. II. Effects on the intracellular distribution of heat shock protein 70 intermediate filaments and small nuclear ribonucleoprotein complexes. Journal of Cell Biology 1988; 106: 1117–1130
  • Werner-Washburne M., Stone D. E., Craig E. A. Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae. Molecular and Cellular Biology 1987; 7: 2568–2577
  • Weshler Z., Kapp D. S., Slord P. F., Mayes T. Development and decay of systemic thermotolerance in rats. Cancer Research 1984; 44: 1347–1351
  • Westra A., Dewey W. C. Variation in sensitivity to heat shock during the cell-cycle of Chinese hamster cell. in vitro. International Journal of Radiation Biology 1971; 19: 467–477
  • Wheldon T. E., Hingston E. C., Ledda J. L. Hyperthermia response and thermotolerance capacity of an experimental rat tumor with occluded blood flow. European Journal of Cancer Clinical Oncology 1982; 18: 1007–1011
  • White F. P. The introduction of ‘stress’ proteins in organ slices from brain, heart and lung as function of postnatal development. Journal of Neurosciences 1981; 1: 1312–1318
  • Wu C., Zimarino V., Tsai C., Walker B., Wilson S. Transcriptional regulation of heat shock genes. Stress Proteins in Biology and Medicine, R. I. Morimoto, A. Tissieres, C. Georgopoulos. Cold Spring Harbor Laboratory Press, Plainview 1990; 429–442
  • Zimmermann R., Sagstetter M., Lewis M. J., Pelham H. R. B. Seventy-kilodalton heat shock proteins and an additional component from reticulocyte lysate stimulate import of M13 procoat protein into microsomes. EMBO Journal 1988; 7: 2875–2880

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.