Fluorescence Imaging of Calcium Loading and Mitochondrial Depolarization in Cancer Cells Exposed to Heat Stress

  • Olaf Minet
  • Cathrin Dressler
  • Jürgen Beuthan
  • Urszula Zabaryło
  • Rasa Zukiene
  • Vida Midaziene
Part of the Reviews in Fluorescence 2008 book series (RFLU, volume 2008)


One main issue of thermotherapy is the stress response of mitochondria to heat. Thermotherapies function by inducing lethal heat inside target tissues. Actually spatial and temporal instabilities of temperature distributions inside target volumes require optimized treatment protocols and reliable temperature-control methods during thermotherapies. Since solid tumors present predominant targets to thermotherapy, on the one hand, the hyperthermic stress-induced effects on mitochondrial transmembrane potentials in breast cancer cells (MX1) were analyzed. On the other hand, the intracellular Ca2+ fluctuations in different cell types responding to heat stress were investigated.

Heat sensitivities and stress reactions might be extremely different among different tissue species and tissue dignities; therefore, it is very important to investigate tissue-specific stress responses systematically. Even though this chapter contributes little information, only, to the enlightenment of systemic cellular heat stress mechanisms, it may support the fortification of basic knowledge about systemic stress responses. Using cytoplasmic and intramitochondrial fluorescent Ca2+ probes it was possible to compare hyperthermia-induced changes in the Ca2+ distribution between the cytoplasm and the mitochondria of normal and tumor cells and to examine the relationship between mitochondrial Ca2+ concentration and changes in the viability of these cell types upon hyperthermic treatment. We compared Ca2+ concentrations in cytoplasm and mitochondria in cancerous CX1 and MX1 cells with normal CHO cells after transfer from room temperature (25°C) to 37°C or 43°C. Sudden increase in the incubation temperature (from room temperature to 37°C) induced very different cytoplasmic and mitochondrial Ca2+ fluctuation patterns in normal CHO and CX1 and MX1 tumor cells. Estimating the CX1, MX1, and CHO cell viabilities upon hyperthermic treatment, we found that thermosensitivities increase in the sequence CX1<CHO<MX1. CHO cells were not less sensitive to hyperthermia than were MX1 tumor cells, but results show that the lowest amount of calcium is in the CHO cells, whereas the highest mitochondrial Ca2+ is in the most thermosensitive MX1 cells. The preliminary results are consistent with the conclusion that the sensitivities of cancer cells to hyperthermic treatments depend on the initial mitochondrial Ca2+ concentrations. However, more experiments are needed to confirm these suggestions. Further on, the data presented here might support an optimization of the treatment protocols applied during thermotherapy, particularly LITT and hyperthermia.


Heat Stress Chinese Hamster Ovary Cell Chinese Hamster Ovary Mitochondrial Permeability Transition Mitochondrial Depolarization 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    B. Gewiese, J. Beuthan, F. Fobbe, D. Stiller, G. Müller, J. Böse-Landgraf, K.J. Wolf, and M. Deimling, Magnetic resonance imaging-controlled laser-induced interstitial thermotherapy, Invest. Radiol. 29(3), 345–351 (1994).Google Scholar
  2. 2.
    A. Roggan, J.P. Ritz, V. Knappe, C.T. Germer, C. Isbert, D. Schädel, and G. Müller, Radiation planning of thermal laser treatment, Med. Laser Appl. 16(2), 65–72 (2001).CrossRefGoogle Scholar
  3. 3.
    M. Nikfarjam, and C. Christophi, Interstitial laser thermotherapy for liver tumors. Brit. J. Surg. 90(9), 1033–1047 (2003).CrossRefPubMedGoogle Scholar
  4. 4.
    J. van der Zee, Heating the patient: a promising approach? Ann. Oncol. 13(8), 1173–1184 (2002).CrossRefPubMedGoogle Scholar
  5. 5.
    A. Debes, R. Willers, U. Göbel, and R. Wessalowski, Role of heat treatment in childhood cancers: distinct resistance profiles of solid tumor cell lines towards combined thermotherapy. Pediatr. Blood Cancer 45(5), 663–669 (2004).CrossRefGoogle Scholar
  6. 6.
    T. Hehr, P. Wust, M. Bamberg, and W. Budach, Current and potential role of thermoradiotherapy for solid tumors, Onkologie 26(3), 295–302 (2003).CrossRefPubMedGoogle Scholar
  7. 7.
    R. Colombo, A. Salonia, L.F. Da Pozzo, R. Naspro, M. Freschi, R. Paroni, M. Pavone-Malasco, and P. Rigatti, Combination of intravesical chemotherapy and hyperthermia for the treatment of superficial bladder cancers: preliminary and clinical experience. Crit. Rev. Oncol. Hematol. 47(2), 127–139 (2003).CrossRefPubMedGoogle Scholar
  8. 8.
    R.B. Campbell, Battling tumors with magnetic nanotherapeutics and hyperthermia: turning up the heat, Nanomedicine 2(5), 649–652 (2007).CrossRefPubMedGoogle Scholar
  9. 9.
    M. Johannsen, U. Gneveckow, B. Thiesen, K. Taymoorian, C.H. Cho, N. Waldöfner, R. Scholz, A. Jordan, S. Loening, and P. Wust, Thermotherapy of prostate cancer using magnetic nanoparticles: feasibility, imaging, and three-dimensional temperature distribution. Eur. Urol. 52(6), 1653–1662 (2007).CrossRefPubMedGoogle Scholar
  10. 10.
    A. Jordan, R. Scholz, K. Maier-Hauff, F. Landeghem, N. Waldöfner, U. Teichgraeber, J. Pinkernelle, H. Bruhn, F. Neumann, B. Thiesen, A. Deimling, and R. Felix, The effect of thermotherapy using magnetic nanoparticles on rat malignant glioma, J. Neuro-Oncol. 78(1), 7–14 (2006).CrossRefGoogle Scholar
  11. 11.
    J. Gellermann, W. Wlodarczyk, B. Hildebrandt, H. Ganter, A. Nicolau, B. Rau, W. Tilly, H. Fähling, J. Nadobny, R. Felix, and P. Wust, Noninvasive magnetic resonance thermography of recurrent rectal carcinoma in a 1.5 Tesla hybrid system, Cancer Res. 65(13), 5872–5880 (2005).CrossRefPubMedGoogle Scholar
  12. 12.
    M. Mack, R. Straub, K. Eichler, O. Söllner, T. Lehnert, and T. Vogl, Breast cancer metastases in liver: laser-induced interstitial thermotherapy-local tumor control rate and survival data. Radiology 233(2), 400–409 (2004).CrossRefPubMedGoogle Scholar
  13. 13.
    M.W. Dewhirst, B.L. Viglianti, M. Lora-Michiels, M. Hanson, and P.J. Hoopes, Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia, Int. J. Hyperthermia 19(3), 267–294 (2003).CrossRefPubMedGoogle Scholar
  14. 14.
    H.G. Park, S.L. Han, S.Y. Oh, and H.S. Kang, Cellular responses to mild heat stress. Cell. Mol. Life Sci. 62(1), 10–23 (2005).CrossRefPubMedGoogle Scholar
  15. 15.
    D.L. Vaux, Apoptosis and toxicology―what relevance? Toxicology 181–182, 3–7 (2002).Google Scholar
  16. 16.
    S.Y. Proskuryakov, A.G. Konoplyannikov, and V.L. Gabai, Necrosis: a specific form of programmed cell death? Exp. Cell Res. 283(1), 1–16 (2003).CrossRefPubMedGoogle Scholar
  17. 17.
    W.F. Yuuen, K.P. Fung, C.Y. Lee, Y.M. Choy, S.K. Kong, S. Ko, and T.T. Kwok, Hyperthermia and tumor necrosis factor-induced apoptosis via mitochondrial damage, Life Sci. 67(6), 725–732 (2000).CrossRefGoogle Scholar
  18. 18.
    W.F. Ko, K.P. Yuen, C.Y. Fung, Y.M. Lee, H.K. Choy, T.T. Cheng, and S.K. Kwok, Reversal of TNF-a resistance by hyperthermia: role of mitochondria, Life Sci. 67(25), 3113–3121 (2000).CrossRefPubMedGoogle Scholar
  19. 19.
    S. Lindquist, The heat-shock response, Annu. Rev. Biochem. 55, 1151–1191 (1986).CrossRefPubMedGoogle Scholar
  20. 20.
    L.A. Sonna, J. Fujita, S.L. Gaffin, and C.M. Lilly, Effects of heat and cold stress on mammalian gene expression, J. Appl. Physiol. 92(4), 1725–1742 (2002).PubMedGoogle Scholar
  21. 21.
    S. Takayama, J.C. Reed, and S. Homma, Heat-shock proteins as regulators of apoptosis. Oncogene 22(56), 9041–9047 (2003).CrossRefPubMedGoogle Scholar
  22. 22.
    K.C. Kregel, Molecular biology of thermoregulation: invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermo tolerance, J. Appl. Physiol. 92(5), 2177–2186 (2002).PubMedGoogle Scholar
  23. 23.
    K.R.H.W. Funk, F. Nagel, F. Wanka, H.E. Krinke, F. Gölfert, and A. Hofer, Effects of heat shock on the functional morphology of cell organelles observed by video-enhanced microscopy, Anat. Rec. 255(4), 458–64 (1999).CrossRefPubMedGoogle Scholar
  24. 24.
    A. Huckriede, A. Heikema, K. Sjollema, P. Briones, and E. Agsteribbe, Morphology of the mitochondria in heat shock protein 60 deficient fibroblasts from mitochondrial myopathy patients. Effects of stress conditions, Virchows Arch. 427(2), 159–65 (1995).CrossRefPubMedGoogle Scholar
  25. 25.
    Y.K. Lai, W.C. Lee, C.H. Hu, and G.L. Hammond, The mitochondria are recognition organelles of cell stress, J. Surg. Res. 62(1), 90–94 (1996).CrossRefPubMedGoogle Scholar
  26. 26.
    F. Macouillard-Poulletier de Gannes, M. Merle, P. Canioni, and P.J. Voison, Metabolic and cellular characterization of immortalized human microglial cells under heat stress, Neurochem. Int. 33(1), 61–73 (1998).CrossRefGoogle Scholar
  27. 27.
    F. Macouillard-Poulletier de Gannes, N. Leducq, P. Diolez, F. Belloc, M. Merle, P. Canioni, and P.J. Voison, Mitochondrial impairment and recovery after heat shock treatment in a human microglial cell line, Neurochem. Int. 36(3), 233–241 (2000).CrossRefGoogle Scholar
  28. 28.
    S. Jakobs, High resolution imaging of live mitochondria, Biochim. Biophys. Acta 1763(5–6), 561–575 (2006).PubMedGoogle Scholar
  29. 29.
    E. Carafoli, L. Santella, D. Branca, and M. Brini, Generation, control, and processing of cellular calcium signals, Biochem. Mol. Biol. 36(2), 107–260 (2001).CrossRefGoogle Scholar
  30. 30.
    R. Rafoli, Calcium signaling: a tail for all seasons, Proc. Natl. Acad. Sci. U S A 99, 1115–1122 (2004).Google Scholar
  31. 31.
    M.J. Erridge, Inositol trisphosphate and calcium signaling, Nature 361, 315–325 (1993).CrossRefGoogle Scholar
  32. 32.
    E.M. Brown, S.M. Quinn, and P.M. Vasseliev, The plasma membrane calcium sensor. In: E. Carafoli and C. Klee (eds.), Calcium as a Cellular Regulator, Oxford University Press, New York, 1999, pp. 295–310.Google Scholar
  33. 33.
    E. Carafoli, Calcium-mediated cellular signals: a story of failures, Trends Biochem. Sci. 29(7), 371–379 (2004).CrossRefPubMedGoogle Scholar
  34. 34.
    L. Santella, and E. Carafoli, Calcium signaling in the cell nucleus, FASEB J. 11(13), 1091–1109 (1997).PubMedGoogle Scholar
  35. 35.
    N.P. Kinnear, C.N. Wyatt, J.H. Clark, P.J. Calcraft, S. Fleischer, L.H. Jeyakumar, G.F. Nixon, and A.M. Evans, Lysosomes co-localize with ryanodine receptor subtype 3 to form a trigger zone for calcium signalling by NAADP in rat pulmonary arterial smooth muscle, Cell Calcium 44(2), 190–201 (2008).CrossRefPubMedGoogle Scholar
  36. 36.
    F. Zhang and P.L. Li, Reconstitution and characterization of a nicotinic acid adenine dinucleotide phosphate (NAADP)-sensitive Ca2+ release channel from liver lysosomes of rats, J. Biol. Chem. 282(35), 25259–25269 (2007).CrossRefPubMedGoogle Scholar
  37. 37.
    F. Zhang, G. Zhang, A.Y. Zhang, M.J. Koeberl, E. Wallander, and P.L. Li, Production of NAADP and its role in Ca2+ mobilization associated with lysosomes in coronary arterial myocytes, Am. J. Physiol. Heart Circ. Physiol. 291(1), H274–H282 (2006).CrossRefPubMedGoogle Scholar
  38. 38.
    B. Dale, L.J. De Felice, K. Kyozuka, L. Santella, and E. Tosti, Voltage clamp of the nuclear envelope, Proc. R. Soc. Lond. 255, 119–124 (1994).CrossRefGoogle Scholar
  39. 39.
    L. Lanini, O. Bachs, and E. Carafoli, The calcium pump of the liver nuclear membrane is identical to that of endoplasmic reticulum, J. Biol. Chem. 267, 11548–11552 (1992).PubMedGoogle Scholar
  40. 40.
    L. Antella and K. Kyozuka, Calcium release into the nucleus by 1,4,5-triphosphate and cyclic ADP-ribose gated channels induces the resumption of meiosis in starfish oocytes. Cell Calcium 22, 1–10 (1997).CrossRefGoogle Scholar
  41. 41.
    J.V. Erasimenko, Y. Maruyama, K. Yano, N.J. Dolman, A.V. Tepikin, O.H. Petersen, and O.V. Gerasimenko, NAADP mobilizes Ca2+ from a thapsigargin-sensitive store in the nuclear envelope by activating ryanodine receptors, J. Cell Biol. 163(2), 271–282 (2003).CrossRefGoogle Scholar
  42. 42.
    F. Shibasaki, E.R. Price, and D. Milan, Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4, Nature 382, 370–373 (1996).CrossRefPubMedGoogle Scholar
  43. 43.
    R. Rizzuto, M. Brini, M. Murgia, and T. Pozzan, Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighbouring mitochondria, Science 262, 744–747 (1993).CrossRefPubMedGoogle Scholar
  44. 44.
    E. Carafoli, The calcium cycle of mitochondria, FEBS Lett. 104, 1–5 (1979).CrossRefPubMedGoogle Scholar
  45. 45.
    R. Baniene, Z. Nauciene, S. Maslauskaite, G. Baliutyte, and V. Mildaziene, Contribution of ATP synthase to stimulation of respiration by Ca2+ in heart mitochondria, Syst. Biol. 153(5), 350–3 (2006).Google Scholar
  46. 46.
    P. Bernardi, Mitochondrial transport of cations: channels, exchangers, and permeability transition, Physiol. Rev. 79, 1127–1155 (1999).PubMedGoogle Scholar
  47. 47.
    B.A. Bornstein, P.S. Zouranjian, J.L. Hansen, S.M. Fraser, L.A. Gelwan, B.B.A. Teichler, and G.K. Svensson, Local hyperthermia, radiation therapy, and chemotherapy in patients with local-regional recurrence of breast carcinoma, Int. J. Radiat. Oncol. Biol. Phys. 25, 79–85 (1992).Google Scholar
  48. 48.
    S. Ringer, A further contribution regarding the influence of different constituents of the blood on the contraction of the heart, J. Physiol. 4, 29–43 (1883).PubMedGoogle Scholar
  49. 49.
    P.M. Hopkins, Malignant hyperthermia: advances in clinical management and diagnosis. Br. J. Anaesth. 85, 118–28 (2002).CrossRefGoogle Scholar
  50. 50.
    N. Sambuughin, Y. Sei, K.L. Gallagher, H.W. Wyre, D. Madsen, T.E. Nelson, J.E. Fletcher, H. Rosenberg, and S.M. Muldoon, North American malignant hyperthermia population: screening of the ryanodine receptor gene and identification of novel mutations, Anasthesiologie 95, 594–599 (2001).CrossRefGoogle Scholar
  51. 51.
    F.K. Storm, Background, principles and practice. In: F.K. Storm (ed.), Hyperthermia in Cancer Therapy, GK Hall Medical Publishers, Boston, 1986, pp. 1–8.Google Scholar
  52. 52.
    N.R. Datta, A.K. Bose, H.K. Kapoor, and S. Gupta, Head and neck cancers: results of thermoradiotherapy versus radiotherapy. Int. J. Hyperthermia 6(3), 479–486 (1990).CrossRefPubMedGoogle Scholar
  53. 53.
    W.F. Yuen, K.P. Fung, C.Y. Lee, Y.M. Choy, S.K. Kong, S. Ko, and T.T. Kwok, Hyperthermia and tumor necrosis factor-induced apoptosis via mitochondrial damage, Life Sci. 67(6), 725–732 (2000).CrossRefPubMedGoogle Scholar
  54. 54.
    S. Ko, W.F. Yuen, K.P. Fung, C.Y. Lee, Y.M. Choy, H.K. Cheng, T.T. Kwok, and S.K. Kong, Reversal of TNF-resistance by hyperthermia role of mitochondria, Life Sci. 67(25), 3113–3121 (2000).CrossRefPubMedGoogle Scholar
  55. 55.
    L. Qian, X. Song, H. Ren, J. Gong, and S. Cheng, Mitochondrial mechanism of heat stress-induced injury in rat cardiomyocyte, Cell Stress Chaperones 9(3), 281–293 (2004).CrossRefPubMedGoogle Scholar
  56. 56.
    S.H.P. Chan, and R.L. Barbour, Adenine nucleotide transport in hepatoma mitochondria. Characterisation of factors influencing the kinetics of ATP/ADP uptake, Biochim. Biophys. Acta 723, 104–113 (1983).CrossRefPubMedGoogle Scholar
  57. 57.
    S.K. Calderwood, M.A. Stevenson, and G.M. Hahn, Effects of heat on cell calcium and inositol lipid metabolism, Radiat. Res. 113(3), 414–425 (1988).CrossRefPubMedGoogle Scholar
  58. 58.
    Y. Itagaki, K. Akagi, M. Uda, and Y. Tanaka, Role of intracellular calcium concentration on tumor cell death from hyperthermia, Oncol. Rep. 5(1), 139–141 (1998).PubMedGoogle Scholar
  59. 59.
    K. Kameda, T. Kondo, K. Tanabe, Q.L. Zhao, and H. Seto, The role of intracellular Ca(2+) in apoptosis induced by hyperthermia and its enhancement by verapamil in U937 cells, Int. J. Radiat. Oncol. Biol. Phys. 49(5), 1369–1379 (2001).CrossRefPubMedGoogle Scholar
  60. 60.
    C.A. Vidair, and W.C. Dewey, Evaluation of a role for intracellular Na+, K+, Ca2+, and Mg2+ in hyperthermic cell killing, Radiat. Res. 105(2), 187–200 (1986).CrossRefPubMedGoogle Scholar
  61. 61.
    J.R. Dynlacht, W.C. Hyun, and W.C. Dewey, Changes in intracellular free calcium during hyperthermia: effects of local anesthetics and induction of thermotolerance, cytometry 14(2), 223–229 (1993).Google Scholar
  62. 62.
    P.K. Wierenga, G.J. Stege, H.H. Kampinga, and A.W. Konings, Intracellular free calcium concentrations in cell suspensions during hyperthermia, Eur. J. Cell. Biol. 63(1), 68–76 (1994).PubMedGoogle Scholar
  63. 63.
    E.D. Wieder, and M.H. Fox, The role of intracellular free calcium in the cellular response to hyperthermia, Int. J. Hyperthermia 11(5), 733–742 (1995).CrossRefPubMedGoogle Scholar
  64. 64.
  65. 65.
  66. 66.
  67. 67.
  68. 68.
  69. 69.
  70. 70.
  71. 71.
    S.L. Keeling, Total variation based convex filters for medical imaging, Appl. Math. Comput. 139(1), 101–109 (2003).CrossRefGoogle Scholar
  72. 72.
    J.L. Wang, D.S. Ke, and M.T. Lin, Heat shock pretreatment may protect against heatstroke-induced circulatory shock and cerebral ischemia by reducing oxidative stress and energy depletion, Shock 23(2), 161–167 (2005).CrossRefPubMedGoogle Scholar
  73. 73.
    C. Dressler, O. Minet, V. Novkov, G. Müller, and J. Beuthan, Microscopical heat stress investigations under application of quantum dots, J. Biomed. Opt. 10(4), 1–9 (2005).CrossRefGoogle Scholar
  74. 74.
    J. Beuthan, C. Dressler, and O. Minet, Laser induced fluorescence detection of quantum dots redistributed in thermally stressed tumor cells, Laser Phys. 14(2), 213–219 (2004).Google Scholar
  75. 75.
    P. Keshavan, S.J. Schwemberger, D.L.H. Smith, G.F. Babcock, and S.D. Zucker, Unconjugated bilirubin induces apoptosis in colon cancer cells by triggering mitochondrial depolarization, Int. J. Cancer 112(3), 433–445 (2004).CrossRefPubMedGoogle Scholar
  76. 76.
    M. Crompton, The mitochondrial permeability transition pore and its role in cell death, Biochem. J. 341(2), 233–249 (1999).CrossRefPubMedGoogle Scholar
  77. 77.
    J.S. Kim, L. He, and J.L. Lemasters, Mitochondrial permeability transition: a common pathway to necrosis and apoptosis, Biochem. Biophys. Res. Commun. 304(3), 463–470 (2003).CrossRefPubMedGoogle Scholar
  78. 78.
    A. Cossarizza, M. Baccarani-Contri, G. Kalashnikova, and C. Francheschi, A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5ʹ,6,6ʹ-tetrachloro-1,1ʹ,3,3ʹ-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem. Biophys. Res. Commun. 197(1), 40–45 (1993).CrossRefPubMedGoogle Scholar
  79. 79.
    S.J. Zunino, and D.H. Storms, Resveratrol-induced apoptosis is enhanced in acute lymphoblastic leukemia cells by modulation of the mitochondrial permeability transition pore. Cancer Lett. 240(1), 123–134 (2006).CrossRefPubMedGoogle Scholar
  80. 80.
    C.J. Lieven, J.P. Vrabec, and L.A. Levin, The effects of oxidative stress on mitochondrial transmembrane potential in retinal ganglion cells. Antioxid. Redox Signal. 5(5), 641–646 (2003).CrossRefPubMedGoogle Scholar
  81. 81.
    M.R. Duchen, A. Leyssens, and M. Crompton, Transient mitochondrial depolarizations reflect focal sarcoplasmic reticular calcium release in single cardiomyocytes. J. Cell Biol. 142(4), 975–988 (1998).CrossRefPubMedGoogle Scholar
  82. 82.
    D.E. Clapham, Calcium Signal. Cell 131, 1047–1058 (2007).CrossRefPubMedGoogle Scholar
  83. 83.
    C. Dressler, J. Beuthan, G. Müller, U. Zabarylo, and O. Minet, Fluorescence imaging of heat-stress induced mitochondrial long-term depolarization in breast cancer cells, J. Fluor. 16(5), 689–695 (2006).CrossRefGoogle Scholar
  84. 84.
    C.M. O´Reilly, K.E. Fogarty, R.M. Drummond, R.A. Tuft, and J.V. Walsh Jr., Quantitative analysis of spontaneous mitochondrial depolarizations, Biophys. J. 85(5), 3350–3357 (2003).CrossRefGoogle Scholar
  85. 85.
    P. Bernardi, L. Scorrano, R. Colonna, V. Petronelli, and F. Di Lisa, Mitochondria and cell death, Eur. J. Biochem. 264(3), 687–701 (1999).CrossRefPubMedGoogle Scholar
  86. 86.
    J.C. Bischof, J. Padanilam, W.H. Holmes, R.M. Ezzell, and R.C. Lee, Dynamics of cell membrane permeability changes at supraphysiological temperatures, Biophys. J. 68(6), 2608–2614 (1995).CrossRefPubMedGoogle Scholar
  87. 87.
    M.A. Stevenson, S.K. Calderwood, and G.M. Hahn, Effect of hyperthermia (45°C) on calcium flux in Chinese hamster ovary HA-1 fibroblasts and its potential role in cytotoxicity and heat resistance, Cancer Res. 47(14), 3712–7 (1987).PubMedGoogle Scholar
  88. 88.
    J.D. Schertzer, H.J. Green, and A.R. Tupling, Thermal instability of rat muscle sarcoplasmic reticulum Ca2+-ATPase function. Am. J. Physiol. Endocrinol. Metab. 283(4), 722–728 (2002).Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Olaf Minet
    • 1
  • Cathrin Dressler
    • 2
  • Jürgen Beuthan
    • 3
  • Urszula Zabaryło
    • 3
  • Rasa Zukiene
    • 4
  • Vida Midaziene
    • 4
  1. 1.Jürgen Beuthan, Urszula Zabaryło: Charité – Universitätsmedizin Berlin, CC6 AG Medizinische Physik / Optische DiagnostikBerlinGermany
  2. 2.LMTB GmbHBerlinGermany
  3. 3.Charité – Universitätsmedizin Berlin, CC6 AG Medizinische Physik/Optische DiagnostikBerlinGermany
  4. 4.Vytautas Magnus UniversityKaunasLithuania

Personalised recommendations