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Temperature Matters: Cellular Targets of Hyperthermia in Cancer Biology and Immunology

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Prokaryotic and Eukaryotic Heat Shock Proteins in Infectious Disease

Part of the book series: Heat Shock Proteins ((HESP,volume 4))

Abstract

Recognition of the potent radiosensitizing effects of hyperthermia on cancer cells has led to extensive research aimed at identifying the effects of heat on a variety of cellular targets, including the plasma membrane. The plasma membrane is a highly complex structure, the phospholipid backbone of which is loaded with proteins that facilitate the exchange of information between a cell and its environment. While most cancer research investigating the effects of hyperthermia on cellular functions has focused on “heat shock” temperatures of 42°C and above, there is increasing recognition of the fact that in actual clinical situations in which hyperthermia has proven to be beneficial, the temperatures achieved within tumors can be considerably lower. In some instances, these are within the range which is achievable during high fever or vigorous exercise (39–40°C). Thus, there is now a great need for additional research (particularly on membrane function and structure) to identify cellular mechanisms by which mild (fever-range) thermal stress could be sensitizing tumor cells to cancer therapies. Moreover, recognition of the potential for the addition of hyperthermia to improve overall survival in patients treated with radiation has led to the hypothesis that cells of the immune system (which may have evolutionarily conserved enhanced plasma membrane-dependent effector activity in response to fever-like conditions) could be among the cellular targets that are affected in the hyperthermic field of treatment. The objective of this chapter is to summarize examples of the literature on these topics, including recent publications that describe the effects of hyperthermia on immune effector and target cells, as well as research pertaining to how mild, fever-range temperatures affect the plasma membrane. The chapter will conclude by discussing current questions that remain to be answered within the field.

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References

  1. Raghunand, N., R.A. Gatenby, and R.J. Gillies, Microenvironmental and cellular consequences of altered blood flow in tumours. Br J Radiol, 2003. 76(Spec No. 1): S11–22.

    Article  PubMed  Google Scholar 

  2. Ben-Hur, E., M.M. Elkind, and B.V. Bronk, Thermally enhanced radioresponse of cultured Chinese hamster cells: inhibition of repair of sublethal damage and enhancement of lethal damage. Radiat Res, 1974. 58(1): 38–51.

    Article  PubMed  CAS  Google Scholar 

  3. Sapareto, S.A., L.E. Hopwood, and W.C. Dewey, Combined effects of X irradiation and hyperthermia on CHO cells for various temperatures and orders of application. Radiat Res, 1978. 73(2): 221–33.

    Article  PubMed  CAS  Google Scholar 

  4. Leyko, W. and G. Bartosz, Membrane effects of ionizing radiation and hyperthermia. Int J Radiat Biol Relat Stud Phys Chem Med, 1986. 49(5): 743–70.

    Article  PubMed  CAS  Google Scholar 

  5. Dikomey, E. and H. Jung, Thermal radiosensitization in CHO cells by prior heating at 41–46 degrees C. Int J Radiat Biol, 1991. 59(3): 815–25.

    Article  PubMed  CAS  Google Scholar 

  6. Kampinga, H.H. and E. Dikomey, Hyperthermic radiosensitization: mode of action and clinical relevance. Int J Radiat Biol, 2001. 77(4): 399–408.

    Article  PubMed  CAS  Google Scholar 

  7. Hildebrandt, B., et al., The cellular and molecular basis of hyperthermia. Crit Rev Oncol Hematol, 2002. 43(1): 33–56.

    Article  PubMed  Google Scholar 

  8. Dewey, W.C., et al., Cellular responses to combinations of hyperthermia and radiation. Radiology, 1977. 123(2): 463–74.

    PubMed  CAS  Google Scholar 

  9. Henle, K.J. and D.B. Leeper, Interaction of hyperthermia and radiation in CHO cells: recovery kinetics. Radiat Res, 1976. 66(3): 505–18.

    Article  PubMed  CAS  Google Scholar 

  10. Henle, K.J. and D.B. Leeper, The modification of radiation damage in CHO cells by hyperthermia at 40 and 45 degrees C1. Radiat Res, 1977. 70(2): 415–24.

    Article  PubMed  CAS  Google Scholar 

  11. Hahn, G.M. and G.C. Li, Thermotolerance and heat shock proteins in mammalian cells. Radiat Res, 1982. 92(3): 452–7.

    Article  PubMed  CAS  Google Scholar 

  12. Simons, K. and E. Ikonen, Functional rafts in cell membranes. Nature, 1997. 387(6633): 569–72.

    Article  PubMed  CAS  Google Scholar 

  13. Yatvin, M.B., et al., Sensitivity of tumour cells to heat and ways of modifying the response. Symp Soc Exp Biol, 1987. 41: 235–67.

    PubMed  CAS  Google Scholar 

  14. Dewhirst, M.W. and D.A. Sim, Estimation of therapeutic gain in clinical trials involving hyperthermia and radiotherapy. Int J Hyperthermia, 1986. 2(2): 165–78.

    Article  PubMed  CAS  Google Scholar 

  15. Shidnia, H., et al., Clinical experience with hyperthermia in conjunction with radiation therapy. Oncology, 1993. 50(5): 353–61.

    Article  PubMed  CAS  Google Scholar 

  16. Dewhirst, M.W., et al., Re-setting the biologic rationale for thermal therapy. Int J Hyperthermia, 2005. 21(8): 779–90.

    Article  PubMed  Google Scholar 

  17. Corry, P.M. and E.P. Armour, The heat shock response: role in radiation biology and cancer therapy. Int J Hyperthermia, 2005. 21(8): 769–78.

    Article  PubMed  Google Scholar 

  18. Song, C.W., et al., Implications of increased tumor blood flow and oxygenation caused by mild temperature hyperthermia in tumor treatment. Int J Hyperthermia, 2005. 21(8): 761–7.

    Article  PubMed  CAS  Google Scholar 

  19. Hahn, G.M. and G.C. Li, Interactions of hyperthermia and drugs: treatments and probes. Natl Cancer Inst Monogr, 1982. 61: 317–23.

    PubMed  CAS  Google Scholar 

  20. Gatenby, R.A., et al., Oxygen distribution in squamous cell carcinoma metastases and its relationship to outcome of radiation therapy. Int J Radiat Oncol Biol Phys, 1988. 14(5): 831–8.

    Article  PubMed  CAS  Google Scholar 

  21. Brizel, D.M., et al., Radiation therapy and hyperthermia improve the oxygenation of human soft tissue sarcomas. Cancer Res, 1996. 56(23): 5347–50.

    PubMed  CAS  Google Scholar 

  22. Steen, R.G. and M.M. Graham, 31P magnetic resonance spectroscopy is sensitive to tumor hypoxia: perfusion and oxygenation of rat 9L gliosarcoma after treatment with BCNU. NMR Biomed, 1991. 4(3): 117–24.

    Article  PubMed  CAS  Google Scholar 

  23. Waterman, F.M., et al., Response of human tumor blood flow to local hyperthermia. Int J Radiat Oncol Biol Phys, 1987. 13(1): 75–82.

    Article  PubMed  CAS  Google Scholar 

  24. Takasu, T., et al., Apoptosis and perturbation of cell cycle progression in an acidic environment after hyperthermia. Cancer Res, 1998. 58(12): 2504–8.

    PubMed  CAS  Google Scholar 

  25. Dynlacht, J.R. and M.H. Fox, The effect of 45 degrees C hyperthermia on the membrane fluidity of cells of several lines. Radiat Res, 1992. 130(1): 55–60.

    Article  PubMed  CAS  Google Scholar 

  26. Tannock, I.F. and D. Rotin, Acid pH in tumors and its potential for therapeutic exploitation. Cancer Res, 1989. 49(16): 4373–84.

    PubMed  CAS  Google Scholar 

  27. Dynlacht, J.R. and M.H. Fox, Effects of hyperthermia and membrane-active compounds or low pH on the membrane fluidity of Chinese hamster ovary cells. Int J Hyperthermia, 1992. 8(3): 351–62.

    Article  PubMed  CAS  Google Scholar 

  28. Roti Roti, J.L., Heat-induced alterations of nuclear protein associations and their effects on DNA repair and replication. Int J Hyperthermia, 2007. 23(1): 3–15.

    Article  PubMed  CAS  Google Scholar 

  29. Connor, W.G., et al., Prospects for hyperthermia in human cancer therapy. Part II: implications of biological and physical data for applications of hyperthermia to man. Radiology, 1977. 123(2): 497–503.

    PubMed  CAS  Google Scholar 

  30. Lepock, J.R., et al., Hyperthermia-induced inhibition of respiration and mitochondrial protein denaturation in CHL cells. Int J Hyperthermia, 1987. 3(2): 123–32.

    Article  PubMed  CAS  Google Scholar 

  31. Lepock, J.R., et al., Thermal analysis of CHL V79 cells using differential scanning calorimetry: implications for hyperthermic cell killing and the heat shock response. J Cell Physiol, 1988. 137(1): 14–24.

    Article  PubMed  CAS  Google Scholar 

  32. Lepock, J.R., et al., Increased thermostability of thermotolerant CHL V79 cells as determined by differential scanning calorimetry. J Cell Physiol, 1990. 142(3): 628–34.

    Article  PubMed  CAS  Google Scholar 

  33. Burgman, P.W. and A.W. Konings, Heat induced protein denaturation in the particulate fraction of HeLa S3 cells: effect of thermotolerance. J Cell Physiol, 1992. 153(1): 88–94.

    Article  PubMed  CAS  Google Scholar 

  34. Gerner, E.W. and M.J. Schneider, Induced thermal resistance in HeLa cells. Nature, 1975. 256(5517): 500–2.

    Article  PubMed  CAS  Google Scholar 

  35. Laszlo, A., W. Wright, and J.L. Roti Roti, Initial characterization of heat-induced excess nuclear proteins in HeLa cells. J Cell Physiol, 1992. 151(3): 519–32.

    Article  PubMed  CAS  Google Scholar 

  36. Cossins, A.R., J. Christiansen, and C.L. Prosser, Adaptation of biological membranes to temperature. The lack of homeoviscous adaptation in the sarcoplasmic reticulum. Biochim Biophys Acta, 1978. 511(3): 442–52.

    CAS  Google Scholar 

  37. Stevenson, M.A., S.K. Calderwood, and G.M. Hahn, Effect of hyperthermia (45 degrees C) on calcium flux in Chinese hamster ovary HA-1 fibroblasts and its potential role in cytotoxicity and heat resistance. Cancer Res, 1987. 47(14): 3712–7.

    PubMed  CAS  Google Scholar 

  38. Vigh, L., et al., The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803. Proc Natl Acad Sci USA, 1993. 90(19): 9090–4.

    Article  PubMed  CAS  Google Scholar 

  39. Nishida, T., K. Akagi, and Y. Tanaka, Correlation between cell killing effect and cell membrane potential after heat treatment: analysis using fluorescent dye and flow cytometry. Int J Hyperthermia, 1997. 13(2): 227–34.

    Article  PubMed  CAS  Google Scholar 

  40. Horvath, I., et al., Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a "fluidity gene". Proc Natl Acad Sci USA, 1998. 95(7): 3513–8.

    Article  PubMed  CAS  Google Scholar 

  41. Narita, N., et al., Inhibition of histone deacetylase 3 stimulates apoptosis induced by heat shock under acidic conditions in human maxillary cancer. Oncogene, 2005. 24(49): 7346–54.

    Article  PubMed  CAS  Google Scholar 

  42. Mejia, R., M.C. Gomez-Eichelmann, and M.S. Fernandez, Membrane fluidity of Escherichia coli during heat-shock. Biochim Biophys Acta, 1995. 1239(2): 195–200.

    Article  PubMed  Google Scholar 

  43. McDonough, V.M., J.E. Stukey, and C.E. Martin, Specificity of unsaturated fatty acid-regulated expression of the Saccharomyces cerevisiae OLE1 gene. J Biol Chem, 1992. 267(9): 5931–6.

    PubMed  CAS  Google Scholar 

  44. Lyons, J.M. and J.K. Raison, Oxidative activity of mitochondria isolated from plant tissue sensitive and resistant to chilling injury. Plant Physiol, 1970. 45(4): 386–389.

    Article  CAS  Google Scholar 

  45. Raison, J.K., J.M. Lyons, and W.W. Thomson, The influence of membranes on the temperature-induced changes in the kinetics of some respiratory enzymes of mitochondria. Arch Biochem Biophys, 1971. 142(1): 83–90.

    Article  PubMed  CAS  Google Scholar 

  46. Bates, D.A., et al., Effects of thermal adaptation at 40 degrees C on membrane viscosity and the sodium-potassium pump in Chinese hamster ovary cells. Cancer Res, 1985. 45(10): 4895–9.

    PubMed  CAS  Google Scholar 

  47. Vigh, L., B. Maresca, and J.L. Harwood, Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem Sci, 1998. 23(10): 369–74.

    Article  PubMed  CAS  Google Scholar 

  48. Dynlacht, J.R. and M.H. Fox, Heat-induced changes in the membrane fluidity of Chinese hamster ovary cells measured by flow cytometry. Radiat Res, 1992. 130(1): 48–54.

    Article  PubMed  CAS  Google Scholar 

  49. Mulcahy, R.T., et al., Hyperthermia and surface morphology of P388 ascites tumour cells: effects of membrane modifications. Int J Radiat Biol Relat Stud Phys Chem Med, 1981. 39(1): 95–106.

    Article  PubMed  CAS  Google Scholar 

  50. Welch, W.J. and J.P. Suhan, Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J Cell Biol, 1985. 101(4): 1198–211.

    Article  PubMed  CAS  Google Scholar 

  51. Bass, H., J.L. Moore, and W.T. Coakley, Lethality in mammalian cells due to hyperthermia under oxic and hypoxic conditions. Int J Radiat Biol Relat Stud Phys Chem Med, 1978. 33(1): 57–67.

    Article  PubMed  CAS  Google Scholar 

  52. Vertrees, R.A., et al., A mechanism of hyperthermia-induced apoptosis in ras-transformed lung cells. Mol Carcinog, 2005. 44(2): 111–21.

    Article  PubMed  CAS  Google Scholar 

  53. Wang, Y.L., Dynamics of the cytoskeleton in live cells. Curr Opin Cell Biol, 1991. 3(1): 27–32.

    Article  PubMed  CAS  Google Scholar 

  54. Glass, J.R., R.G. DeWitt, and A.E. Cress, Rapid loss of stress fibers in Chinese hamster ovary cells after hyperthermia. Cancer Res, 1985. 45(1): 258–62.

    PubMed  CAS  Google Scholar 

  55. Wachsberger, P.R. and R.A. Coss, Effects of hyperthermia on the cytoskeleton and cell survival in G1 and S phase Chinese hamster ovary cells. Int J Hyperthermia, 1990. 6(1): 67–85.

    Article  PubMed  CAS  Google Scholar 

  56. Wiegant, F.A., M. Tuyl, and W.A. Linnemans, Calmodulin inhibitors potentiate hyperthermic cell killing. Int J Hyperthermia, 1985. 1(2): 157–69.

    Article  PubMed  CAS  Google Scholar 

  57. Coss, R.A. and W.A. Linnemans, The effects of hyperthermia on the cytoskeleton: a review. Int J Hyperthermia, 1996. 12(2): 173–96.

    Article  PubMed  CAS  Google Scholar 

  58. Mikkelsen, R.B. and B. Koch, Thermosensitivity of the membrane potential of normal and simian virus 40-transformed hamster lymphocytes. Cancer Res, 1981. 41(1): 209–15.

    PubMed  CAS  Google Scholar 

  59. Moriyama-Gonda, N., et al., Heat-induced membrane damage combined with adriamycin on prostate carcinoma PC-3 cells: correlation of cytotoxicity, permeability and P-glycoprotein or metallothionein expression. Br J Urol, 1998. 82(4): 552–9.

    PubMed  CAS  Google Scholar 

  60. Torok, Z., et al., 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, 1997. 94(6): 2192–7.

    Article  PubMed  CAS  Google Scholar 

  61. Lindquist, S., Heat-shock proteins and stress tolerance in microorganisms. Curr Opin Genet Dev, 1992. 2(5): 748–55.

    Article  PubMed  CAS  Google Scholar 

  62. Feng, H., et al., Stressed apoptotic tumor cells express heat shock proteins and elicit tumor-specific immunity. Blood, 2001. 97(11): 3505–12.

    Article  PubMed  CAS  Google Scholar 

  63. Kim, C.H., et al., Enhancement of anti-tumor immunity specific to murine glioma by vaccination with tumor cell lysate-pulsed dendritic cells engineered to produce interleukin-12. Cancer Immunol Immunother, 2006. 55(11): 1309–19.

    Article  PubMed  CAS  Google Scholar 

  64. Laszlo, A., et al., Alterations in heat-induced radiosensitization accompanied by nuclear structure alterations in Chinese hamster cells. Int J Hyperthermia, 2006. 22(1): 43–60.

    Article  PubMed  CAS  Google Scholar 

  65. Calderwood, S.K. and G.M. Hahn, Thermal sensitivity and resistance of insulin-receptor binding in thermotolerant cells. Biochim Biophys Acta, 1983. 734(1): 76–82.

    Article  PubMed  CAS  Google Scholar 

  66. Magun, B.E. and C.W. Fennie, Effects of hyperthermia on binding, internalization, and degradation of epidermal growth factor. Radiat Res, 1981. 86(1): 133–46.

    Article  PubMed  CAS  Google Scholar 

  67. Stubbs, C.D. and S.J. Slater, The effects of non-lamellar forming lipids on membrane protein-lipid interactions. Chem Phys Lipids, 1996. 81(2): 185–95.

    Article  PubMed  CAS  Google Scholar 

  68. Eletr, S. and A.D. Keith, Spin-label studies of dynamics of lipid alkyl chains in biological membranes: role of unsaturated sites. Proc Natl Acad Sci USA, 1972. 69(6): 1353–1357.

    Article  PubMed  CAS  Google Scholar 

  69. Hidvegi, E.J., et al., Effect of altered membrane lipid composition and procaine on hyperthermic killing of ascites tumor cells. Oncology, 1980. 37(5): 360–3.

    Article  PubMed  CAS  Google Scholar 

  70. Yoshikawa, T., et al., Effect of intra-arterial chemotherapy combined with degradable starch microspheres against liver cancer – a study by experimental VX2 liver tumor model. Gan To Kagaku Ryoho, 1993. 20(12): 1803–9.

    PubMed  CAS  Google Scholar 

  71. Skibba, J.L., E.J. Quebbeman, and J.H. Kalbfleisch, Nitrogen metabolism and lipid peroxidation during hyperthermic perfusion of human livers with cancer. Cancer Res, 1986. 46(11): 6000–3.

    PubMed  CAS  Google Scholar 

  72. Viani, P., et al., Age-related differences in synaptosomal peroxidative damage and membrane properties. J Neurochem, 1991. 56(1): 253–8.

    Article  PubMed  CAS  Google Scholar 

  73. Sinensky, M., et al., Rate limitation of (Na+ + K+)-stimulated adenosinetriphosphatase by membrane acyl chain ordering. Proc Natl Acad Sci USA, 1979. 76(10): 4893–7.

    Article  PubMed  CAS  Google Scholar 

  74. Kluger, M.J., D.H. Ringler, and M.R. Anver, Fever and survival. Science, 1975. 188(4184): 166–8.

    Article  PubMed  CAS  Google Scholar 

  75. Hasday, J.D., K.D. Fairchild, and C. Shanholtz, The role of fever in the infected host. Microbes Infect, 2000. 2(15): 1891–904.

    Article  PubMed  CAS  Google Scholar 

  76. Roberts, N.J., Jr., Impact of temperature elevation on immunologic defenses. Rev Infect Dis, 1991. 13(3): 462–72.

    PubMed  Google Scholar 

  77. Pritchard, M.T., et al., Protocols for simulating the thermal component of fever: preclinical and clinical experience. Methods, 2004. 32(1): 54–62.

    Article  PubMed  CAS  Google Scholar 

  78. Bicher, H.I., et al., Effects of hyperthermia on normal and tumor microenvironment. Radiology, 1980. 137(2): 523–30.

    PubMed  CAS  Google Scholar 

  79. Song, C.W., et al., Tumour oxygenation is increased by hyperthermia at mild temperatures. Int J Hyperthermia, 1996. 12(3): 367–73.

    Article  PubMed  CAS  Google Scholar 

  80. Okajima, K., et al., Tumor oxygenation after mild-temperature hyperthermia in combination with carbogen breathing: dependence on heat dose and tumor type. Radiat Res, 1998. 149(3): 294–9.

    Article  PubMed  CAS  Google Scholar 

  81. Burd, R., et al., Tumor cell apoptosis, lymphocyte recruitment and tumor vascular changes are induced by low temperature, long duration (fever-like) whole body hyperthermia. J Cell Physiol, 1998. 177(1): 137–47.

    Article  PubMed  CAS  Google Scholar 

  82. Hermisson, M., et al., Sensitization to CD95 ligand-induced apoptosis in human glioma cells by hyperthermia involves enhanced cytochrome c release. Oncogene, 2000. 19(19): 2338–45.

    Article  PubMed  CAS  Google Scholar 

  83. Rolo, A.P., et al., Chenodeoxycholate induction of mitochondrial permeability transition pore is associated with increased membrane fluidity and cytochrome c release: protective role of carvedilol. Mitochondrion, 2003. 2(4): 305–11.

    Article  PubMed  CAS  Google Scholar 

  84. McLean-Bowen, C.A. and L.W. Parks, Corresponding changes in kynurenine hydroxylase activity, membrane fluidity, and sterol composition in Saccharomyces cerevisiae mitochondria. J Bacteriol, 1981. 145(3): 1325–33.

    PubMed  CAS  Google Scholar 

  85. Multhoff, G., et al., A stress-inducible 72-kDa heat-shock protein (HSP72) is expressed on the surface of human tumor cells, but not on normal cells. Int J Cancer, 1995. 61(2): 272–9.

    Article  PubMed  CAS  Google Scholar 

  86. Ostberg, J.R., et al., Enhancement of natural killer (NK) cell cytotoxicity by fever-range thermal stress is dependent on NKG2D function and is associated with plasma membrane NKG2D clustering and increased expression of MICA on target cells. J Leukoc Biol, 2007. 82(5): 1322–31.

    Article  PubMed  CAS  Google Scholar 

  87. Cohen, C.M., The molecular organization of the red cell membrane skeleton. Semin Hematol, 1983. 20(3): 141–58.

    PubMed  CAS  Google Scholar 

  88. Lee, J.K. and E.A. Repasky, Cytoskeletal polarity in mammalian lymphocytes in situ. Cell Tissue Res, 1987. 247(1): 195–202.

    Article  PubMed  CAS  Google Scholar 

  89. Hughes, C.S., et al., Effects of hyperthermia on spectrin expression patterns of murine lymphocytes. Radiat Res, 1987. 112(1): 116–23.

    Article  PubMed  CAS  Google Scholar 

  90. Lee, J.K., et al., Activation induces a rapid reorganization of spectrin in lymphocytes. Cell, 1988. 55(5): 807–16.

    Article  PubMed  CAS  Google Scholar 

  91. Di, Y.P., et al., Hsp70 translocates into a cytoplasmic aggregate during lymphocyte activation. J Cell Physiol, 1995. 165(2): 228–38.

    Article  PubMed  CAS  Google Scholar 

  92. Di, Y.P., E.A. Repasky, and J.R. Subjeck, Distribution of HSP70, protein kinase C, and spectrin is altered in lymphocytes during a fever-like hyperthermia exposure. J Cell Physiol, 1997. 172(1): 44–54.

    Article  PubMed  CAS  Google Scholar 

  93. Broquet, A.H., et al., Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J Biol Chem, 2003. 278(24): 21601–6.

    Article  PubMed  CAS  Google Scholar 

  94. Micheau, O., et al., The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J Biol Chem, 2002. 277(47): 45162–71.

    Article  PubMed  CAS  Google Scholar 

  95. Meinander, A., et al., Fever-like hyperthermia controls T Lymphocyte persistence by inducing degradation of cellular FLIPshort. J Immunol, 2007. 178(6): 3944–53.

    PubMed  CAS  Google Scholar 

  96. Wang, W.C., et al., Fever-range hyperthermia enhances L-selectin-dependent adhesion of lymphocytes to vascular endothelium. J Immunol, 1998. 160(2): 961–9.

    PubMed  CAS  Google Scholar 

  97. Evans, S.S., et al., Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood, 2001. 97(9): 2727–33.

    Article  PubMed  CAS  Google Scholar 

  98. Yoshioka, A., et al., Effects of local hyperthermia on natural killer activity in mice. Int J Hyperthermia, 1990. 6(2): 261–7.

    Article  PubMed  CAS  Google Scholar 

  99. Kappel, M., et al., Effects of in vivo hyperthermia on natural killer cell activity, in vitro proliferative responses and blood mononuclear cell subpopulations. Clin Exp Immunol, 1991. 84(1): 175–80.

    Article  PubMed  CAS  Google Scholar 

  100. van Bruggen, I., T.A. Robertson, and J.M. Papadimitriou, The effect of mild hyperthermia on the morphology and function of murine resident peritoneal macrophages. Exp Mol Pathol, 1991. 55(2): 119–34.

    Article  PubMed  Google Scholar 

  101. Zhao, W., et al., Hyperthermia differentially regulates TLR4 and TLR2-mediated innate immune response. Immunol Lett, 2007. 108(2): 137–42.

    Article  PubMed  CAS  Google Scholar 

  102. Ensor, J.E., et al., Differential effects of hyperthermia on macrophage interleukin-6 and tumor necrosis factor-alpha expression. Am J Physiol, 1994. 266(4 Pt 1): C967–74.

    PubMed  CAS  Google Scholar 

  103. Ostberg, J.R., R. Patel, and E.A. Repasky, Regulation of immune activity by mild (fever-range) whole body hyperthermia: effects on epidermal Langerhans cells. Cell Stress Chaperones, 2000. 5(5): 458–61.

    Article  PubMed  CAS  Google Scholar 

  104. Jiang, Q., et al., Exposure to febrile temperature upregulates expression of pyrogenic cytokines in endotoxin-challenged mice. Am J Physiol, 1999. 276(6 Pt 2): R1653–60.

    PubMed  CAS  Google Scholar 

  105. Ostberg, J.R., E. Kabingu, and E.A. Repasky, Thermal regulation of dendritic cell activation and migration from skin explants. Int J Hyperthermia, 2003. 19(5): 520–33.

    Article  PubMed  CAS  Google Scholar 

  106. Banchereau, J., et al., Immunobiology of dendritic cells. Annu Rev Immunol, 2000. 18: 767–811.

    Article  PubMed  CAS  Google Scholar 

  107. Tournier, J.N., et al., Fever-like thermal conditions regulate the activation of maturing dendritic cells. J Leukoc Biol, 2003. 73(4): 493–501.

    Article  PubMed  CAS  Google Scholar 

  108. Basu, S. and P.K. Srivastava, Fever-like temperature induces maturation of dendritic cells through induction of hsp90. Int Immunol, 2003. 15(9): 1053–61.

    Article  PubMed  CAS  Google Scholar 

  109. Zheng, H., et al., Heat shock factor 1-independent activation of dendritic cells by heat shock: implication for the uncoupling of heat-mediated immunoregulation from the heat shock response. Eur J Immunol, 2003. 33(6): 1754–62.

    Article  PubMed  CAS  Google Scholar 

  110. Matsumori, A., et al., Modulation of cytokine production and protection against lethal endotoxemia by the cardiac glycoside ouabain. Circulation, 1997. 96(5): 1501–6.

    PubMed  CAS  Google Scholar 

  111. Prpic, V., et al., Effects of bacterial lipopolysaccharide on the hydrolysis of phosphatidylinositol-4,5-bisphosphate in murine peritoneal macrophages. J Immunol, 1987. 139(2): 526–33.

    PubMed  CAS  Google Scholar 

  112. Petit, V.A.E.M., Lateral Phase separation of lipids in plasma membranes: effect of temperature on the mobility of membrane antigens. Science, 1974. 184: 1183–5.

    Article  PubMed  CAS  Google Scholar 

  113. Marsh, D., A. Watts, and P.F. Knowles, Evidence for phase boundary lipid. Permeability of Tempo-choline into dimyristoylphosphatidylcholine vesicles at the phase transition. Biochemistry, 1976. 15(16): 3570–8.

    Article  PubMed  CAS  Google Scholar 

  114. Overath, P. and H. Trauble, Phase transitions in cells, membranes, and lipids of Escherichia coli. Detection by fluorescent probes, light scattering, and dilatometry. Biochemistry, 1973. 12(14): 2625–34.

    Article  PubMed  CAS  Google Scholar 

  115. Thilo, L., H. Trauble, and P. Overath, Mechanistic interpretation of the influence of lipid phase transitions on transport functions. Biochemistry, 1977. 16(7): 1283–90.

    Article  PubMed  CAS  Google Scholar 

  116. Simons, K. and D. Toomre, Lipid rafts and signal transduction. Nat Rev Mol Cell Biol, 2000. 1(1): 31–9.

    Article  PubMed  CAS  Google Scholar 

  117. Xavier, R., et al., Membrane compartmentation is required for efficient T cell activation. Immunity, 1998. 8(6): 723–32.

    Article  PubMed  CAS  Google Scholar 

  118. Aman, M.J. and K.S. Ravichandran, A requirement for lipid rafts in B cell receptor induced Ca(2+) flux. Curr Biol, 2000. 10(7): 393–6.

    Article  PubMed  CAS  Google Scholar 

  119. Sprong, H., P. van der Sluijs, and G. van Meer, How proteins move lipids and lipids move proteins. Nat Rev Mol Cell Biol, 2001. 2(7): 504–13.

    Article  PubMed  CAS  Google Scholar 

  120. Manes, S., et al., From rafts to crafts: membrane asymmetry in moving cells. Trends Immunol, 2003. 24(6): 320–6.

    Article  PubMed  CAS  Google Scholar 

  121. Okamoto, T., et al., Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem, 1998. 273(10): 5419–22.

    Article  PubMed  CAS  Google Scholar 

  122. Munoz, P., et al., CD38 signaling in T cells is initiated within a subset of membrane rafts containing Lck and the CD3-zeta subunit of the T cell antigen receptor. J Biol Chem, 2003. 278(50): 50791–802.

    Article  PubMed  CAS  Google Scholar 

  123. Pralle, A., et al., Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol, 2000. 148(5): 997–1008.

    Article  PubMed  CAS  Google Scholar 

  124. Karacsonyi, C., et al., MHC II molecules and invariant chain reside in membranes distinct from conventional lipid rafts. J Leukoc Biol, 2005. 78(5): 1097–105.

    Article  PubMed  CAS  Google Scholar 

  125. Drevot, P., et al., TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J, 2002. 21(8): 1899–908.

    Article  PubMed  CAS  Google Scholar 

  126. Hanson, D.F., Fever and the immune response. The effects of physiological temperatures on primary murine splenic T-cell responses in vitro. J Immunol, 1993. 151(1): 436–48.

    PubMed  CAS  Google Scholar 

  127. Schade, A.E. and A.D. Levine, Lipid raft heterogeneity in human peripheral blood T lymphoblasts: a mechanism for regulating the initiation of TCR signal transduction. J Immunol, 2002. 168(5): 2233–9.

    PubMed  CAS  Google Scholar 

  128. Yuan, M., et al., Fever-range hyperthermia reduces the activation threshold of CD4+ T cells and promotes reorganization of lipid rafts. Submitted for publication.

    Google Scholar 

  129. Chen, S., et al., Association of heat shock proteins and neuronal membrane components with lipid rafts from the rat brain. J Neurosci Res, 2005. 81(4): 522–9.

    Article  PubMed  CAS  Google Scholar 

  130. Varma, R. and S. Mayor, GPI-anchored proteins are organized in submicron domains at the cell surface. Nature, 1998. 394(6695): 798–801.

    Article  PubMed  CAS  Google Scholar 

  131. Jordan, S. and W. Rodgers, T cell glycolipid-enriched membrane domains are constitutively assembled as membrane patches that translocate to immune synapses. J Immunol, 2003. 171(1): 78–87.

    PubMed  CAS  Google Scholar 

  132. Eleme, K., et al., Cell surface organization of stress-inducible proteins ULBP and MICA that stimulate human NK cells and T cells via NKG2D. J Exp Med, 2004. 199(7): 1005–10.

    Article  PubMed  CAS  Google Scholar 

  133. Endt, J., et al., Inhibitory receptor signals suppress ligation-induced recruitment of NKG2D to GM1-rich membrane domains at the human NK cell immune synapse. J Immunol, 2007. 178(9): 5606–11.

    PubMed  CAS  Google Scholar 

  134. Calder, P.C., et al., Incorporation of fatty acids by concanavalin A-stimulated lymphocytes and the effect on fatty acid composition and membrane fluidity. Biochem J, 1994. 300(Pt 2): 509–18.

    PubMed  CAS  Google Scholar 

  135. de Pablo, M.A. and G. Alvarez de Cienfuegos, Modulatory effects of dietary lipids on immune system functions. Immunol Cell Biol, 2000. 78(1): 31–9.

    Article  PubMed  Google Scholar 

  136. Larbi, A., et al., Acute in vivo elevation of intravascular triacylglycerol lipolysis impairs peripheral T cell activation in humans. Am J Clin Nutr, 2005. 82(5): 949–56.

    PubMed  CAS  Google Scholar 

  137. Marguet, D., et al., Dynamics in the plasma membrane: how to combine fluidity and order. Embo J, 2006. 25(15): 3446–57.

    Article  PubMed  CAS  Google Scholar 

  138. Hanzal-Bayer, M.F. and J.F. Hancock, Lipid rafts and membrane traffic. FEBS Lett, 2007. 581(11): 2098–104.

    Article  PubMed  CAS  Google Scholar 

  139. Meire, K.F., Lipid rafts and regulation of the cytoskeleton during T cell activation. Phil Trans R Soc B 2005. 360: 1663–1672.

    Article  CAS  Google Scholar 

  140. Nicolau, J., D.N. Souza, and F.N. Nogueira, Activity, distribution and regulation of phosphofructokinase in salivary gland of rats with streptozotocin-induced diabetes. Braz Oral Res, 2006. 20(2): 108–13.

    Article  PubMed  Google Scholar 

  141. Hancock, J.F., Lipid rafts: contentious only from simplistic standpoints. Nat Rev Mol Cell Biol, 2006. 7(6): 456–62.

    Article  PubMed  CAS  Google Scholar 

  142. Robins, H.I., et al., Cytokine induction by 41.8 degrees C whole body hyperthermia. Cancer Lett, 1995. 97(2): 195–201.

    Article  CAS  Google Scholar 

  143. Atanackovic, D., et al., 41.8 degrees C whole body hyperthermia as an adjunct to chemotherapy induces prolonged T cell activation in patients with various malignant diseases. Cancer Immunol Immunother, 2002. 51(11–12): 603–13.

    Article  PubMed  CAS  Google Scholar 

  144. Ahmed, K., et al., Enhancement of macrosphelide-induced apoptosis by mild hyperthermia. Int J Hyperthermia, 2007. 23(4): 353–61.

    Article  PubMed  CAS  Google Scholar 

  145. Hegewisch-Becker, S., et al., Whole-body hyperthermia (41.8 degrees C) combined with bimonthly oxaliplatin, high-dose leucovorin and 5-fluorouracil 48-hour continuous infusion in pretreated metastatic colorectal cancer: a phase II study. Ann Oncol, 2002. 13(8): 1197–204.

    Article  PubMed  CAS  Google Scholar 

  146. Bakhshandeh, A., et al., Ifosfamide, carboplatin and etoposide combined with 41.8 degrees C whole body hyperthermia for malignant pleural mesothelioma. Lung Cancer, 2003. 39(3): 339–45.

    Article  PubMed  CAS  Google Scholar 

  147. Abiko, T., et al., Prediction of anti-tumour effect of thermochemotherapy with in vitro thermochemosensitivity testing for non-small cell lung cancer. Int J Hyperthermia, 2007. 23(3): 267–75.

    Article  PubMed  CAS  Google Scholar 

  148. Sato, C., et al., Effects of hyperthermia on cell surface charge and cell survival in mastocytoma cells. Cancer Res, 1981. 41(10): 4107–10.

    PubMed  CAS  Google Scholar 

  149. Bates, D.A. and W.J. Mackillop, The effect of hyperthermia on the sodium-potassium pump in Chinese hamster ovary cells. Radiat Res, 1985. 103(3): 441–51.

    Article  PubMed  CAS  Google Scholar 

  150. Warters, R.L., et al., Heat shock (45 degrees C) results in an increase of nuclear matrix protein mass in HeLa cells. Int J Radiat Biol Relat Stud Phys Chem Med, 1986. 50(2): 253–68.

    Article  PubMed  CAS  Google Scholar 

  151. Bodell, W.J., J.E. Cleaver, and J.L. Roti Roti, Inhibition by hyperthermia of repair synthesis and chromatin reassembly of ultraviolet-induced damage to DNA. Radiat Res, 1984. 100(1): 87–95.

    Article  PubMed  CAS  Google Scholar 

  152. Trieb, K., et al., Reversible downregulation of telomerase activity by hyperthermia in osteosarcoma cells. Int J Hyperthermia, 2000. 16(5): 445–8.

    Article  PubMed  CAS  Google Scholar 

  153. Raaphorst, G.P. and M.M. Feeley, Hyperthermia radiosensitization in human glioma cells comparison of recovery of polymerase activity, survival, and potentially lethal damage repair. Int J Radiat Oncol Biol Phys, 1994. 29(1): 133–9.

    Article  PubMed  CAS  Google Scholar 

  154. Higashikubo, R., J.M. Holland, and J.L. Roti Roti, Comparative effects of caffeine on radiation- and heat-induced alterations in cell cycle progression. Radiat Res, 1989. 119(2): 246–60.

    Article  PubMed  CAS  Google Scholar 

  155. Seno, J.D. and J.R. Dynlacht, Intracellular redistribution and modification of proteins of the Mre11/Rad50/Nbs1 DNA repair complex following irradiation and heat-shock. J Cell Physiol, 2004. 199(2): 157–70.

    Article  PubMed  CAS  Google Scholar 

  156. Stevenson, M.A., K.W. Minton, and G.M. Hahn, Survival and concanavalin-A-induced capping in CHO fibroblasts after exposure to hyperthermia, ethanol, and X irradiation. Radiat Res, 1981. 86(3): 467–78.

    Article  PubMed  CAS  Google Scholar 

  157. Ostberg, J.R., et al., Regulatory potential of fever-range whole body hyperthermia on Langerhans cells and lymphocytes in an antigen-dependent cellular immune response. J Immunol, 2001. 167(5): 2666–70.

    PubMed  CAS  Google Scholar 

  158. Beck, K.A. and W.J. Nelson, The spectrin-based membrane skeleton as a membrane-sorting machine. Am J Physiol, 1996. 270: 1263–1270.

    Google Scholar 

  159. Lenne, P.F., et al., Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J, 2006. 25(14): 3245–3256.

    CAS  Google Scholar 

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Acknowledgements

The authors thank Dr. Bonnie Hylander and Maegan Capitano for their many helpful comments on this chapter.

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Authors and Affiliations

  1. Departments of Immunology and Cell Stress Biology, Roswell Park Cancer Institute, Buffalo, NY, USA

    Melissa J. Grimm & Evan R. Zynda

  2. Department of Immunology, Roswell Park Cancer Institute, 14263, Buffalo, NY, USA

    Elizabeth A. Repasky

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  1. Melissa J. Grimm
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  2. Evan R. Zynda
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Correspondence to Elizabeth A. Repasky .

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Editors and Affiliations

  1. School of Medicine & Biomedical Science, University of Sheffield, Beech Hill Road, Sheffield, S10 2RX, United Kingdom

    A. Graham Pockley

  2. Beth Israel Deaconess Medical Center, Harvard Medical School, Burlington Avenue 21-27, Boston, 02215, U.S.A.

    Stuart K. Calderwood

  3. Dipto. Biologia, Università di Roma, Tor Vergata, Via della Ricerca Scientifica 1, Roma, 00133, Italy

    M. Gabriella Santoro

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Grimm, M.J., Zynda, E.R., Repasky, E.A. (2009). Temperature Matters: Cellular Targets of Hyperthermia in Cancer Biology and Immunology. In: Pockley, A., Calderwood, S., Santoro, M. (eds) Prokaryotic and Eukaryotic Heat Shock Proteins in Infectious Disease. Heat Shock Proteins, vol 4. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2976-8_15

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