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The Kinetics of Thermal Injury in Human Renal Carcinoma Cells

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Abstract

In this study, the thermal injury behavior of both suspended and attached SN12 human renal carcinoma cells (RCC) under thermal therapy conditions (i.e., heating cells to elevated temperature for seconds to minutes) was investigated using a non-isothermal method. This non-isothermal method entailed heating the cells using a programmable heating stage from room temperature at 130∘C min≥−1 to various peak temperatures from 45 to 70∘C, held for 0–10 min, and then cooling down to room temperature at 65∘C min−1. It was found that the suspended SN12 cells are more heat susceptible than attached ones. The non-isothermal portions (i.e., the heat-up and cool-down portions) of the thermal histories were found to be able to cause significant injury (> 10%) in both suspended and attached SN12 cells when the peak temperature is above 60∘C. Therefore, a non-isothermal method, which accounts for both the isothermal and non-isothermal portions of the thermal histories, was used to extract the kinetic parameters (i.e., the activation energy and frequency factor) in the Arrhenius injury model for SN12 cells. Furthermore, these results suggest that this non-isothermal method can be used to extract kinetic parameters from in vivo heating studies using minimally invasive surgical probes, where it is very difficult to get a thermal history in tissue with a dominant isothermal portion.

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References

  1. American Cancer Society. Cancer facts and figures 2004. American Cancer Society, Inc., Atlanta, GA, USA.

    Google Scholar 

  2. Bhowmick, P., J. E. Coad, S. Bhowmick, J. L. Pryor, T. Larson, J. De La Rosette, and J. C. Bischof. In vitro assessment of the efficacy of thermal therapy in human benign prostatic hyperplasia tissue. Int. J. Hyperthermia 20(4):421–439, 2004.

    Article  CAS  PubMed  Google Scholar 

  3. Bhowmick, S., J. E. Coad, D. J. Swanlund, and J. C. Bischof. In vitro thermal therapy of AT-1 Dunning prostate tumours. Int. J. Hyperthermia 20(1):73–92, 2004.

    Article  CAS  PubMed  Google Scholar 

  4. Bhowmick, S., N. E. Hoffmann, and J. C. Bischof. Thermal therapy of prostate tumor tissue in dorsal skin flap chamber. Microvasc. Res. 64:170–173, 2002.

    Article  PubMed  Google Scholar 

  5. Bhowmick, S., D. J. Swanlund, and J. C. Bischof. Supraphysiological thermal injury in dunning AT-1 prostate tumor cells. ASME J. Biomech. Eng. 122:51–59, 2000.

    CAS  Google Scholar 

  6. Bischof, J. C., W. F. Wolkers, N. M. Tsvetkova, A. E. Oliver, and J. H. Crowe. Lipid and protein changes due to freezing in dunning AT-1 cells. Cryobiology 45(1):22–32, 2002.

    Article  CAS  PubMed  Google Scholar 

  7. Borrelli, M. J., L. L. Thompson, A. A. Cain, and W. C. Dewey. Time-temperature analysis of cell killing of BHK cells heated at temperatures in the range of 43.5 degree C to 57 degree C. Int. J. Radiat. Oncol. Biol. Phys. 19(2):389–399, 1990.

    CAS  PubMed  Google Scholar 

  8. Cerretti, D. P., K. Dorsey, and D. W. Bolwen. Thermal behavior of Hela and KB cells in suspension and attached to glass. Biochimica et Biophysica Acta 462:748–758, 1977.

    CAS  PubMed  Google Scholar 

  9. Chen, S. S., N. T. Wright, and J. D. Humphrey. Heat-induced changes in the mechanics of a collagenous tissue: Isothermal isotonic-shrinkage. ASME J. Biomech. Eng. 120:382–388, 1998.

    CAS  Google Scholar 

  10. Chow, W. H., S. S. Devesa, J. L. Warren, and J. F. Fraumeni, Jr. Rising incidence of renal cell cancer in the United States. JAMA 281:1628–1631, 1999.

    Article  CAS  PubMed  Google Scholar 

  11. Cravalho, E. G., M. Toner, D. C. Gaylor, and R. C. Lee. Response of cells to supraphysiological temperatures: Experimental measurements and kinetic models. In Electrical Trauma: The Pathophysiology, Manifestations and Clinical Management, edited by R. C. Lee, E. G. Cravalho, and J. F. Burke. Cambridge: Cambridge University Press, 1992, pp. 281–300.

    Google Scholar 

  12. Dhir, V. K., and C. E. R. Dodd. Susceptibility of suspended and surface-attached Salmonella enteritidis to biocides and elevated temperature. Appl. Environ. Microbiol. 61(5):1731–1738, 1995.

    CAS  PubMed  Google Scholar 

  13. Diller, K. R. Modeling of bioheat transfer processes at high and low temperatures. In: Advances in Heat Transfer, Edited by Y. I. Cho. San Diego: Academic Press, Vol. 22, 1992.

    Google Scholar 

  14. Diller, K. R., and T. P. Ryan. Heat transfer in living systems: Current opportunities. ASME J. Heat Transf. 120:810–829, 1998.

    CAS  Google Scholar 

  15. Eyring, H., and A. E. Stearn. The application of the theory of absolute reaction rates to proteins. Chem. Rev. 24:253–270, 1939.

    CAS  Google Scholar 

  16. Frank, J. F., and R. A. Koffi. Surface-adherent growth of Listern monocytogenes is associated with increase resistance to sanitizer and heat. J. Food Prot. 53:550–554, 1990.

    Google Scholar 

  17. Gonda, T., D. Maouyo, S. E. Rees, and M. H. Montrose. Regulation of intracellular pH gradients by identified Na/H exchanger isoforms and a short-chain fatty acid. Am. J. Physiol. 276(1 Pt 1):G259–G270, 1999.

    CAS  PubMed  Google Scholar 

  18. Hall, E. J. Hyperthermia. In Radiobiology for the Radiobiologist (Fourth Edition). Philadelphia: J. B. Lippincott Company, 1994, pp. 257–288.

    Google Scholar 

  19. Han, J., X. P. Liu, L. B. Yao, and Q. Yu. Relationship between protein tyrosine phosphorylation level and anoikis resistance of breast tumor cell lines. Ai Zhang 23(1):15–22, 2004.

    CAS  Google Scholar 

  20. Harris, M. Criterion of viability in heat-treated cells. Exp. Cell Res. 44:658–661, 1966.

    CAS  PubMed  Google Scholar 

  21. Harris, J. L., and J. D. Humphrey. Kinetics of thermal damage to a collagenous membrane under biaxial isotonic loading. IEEE Trans. Biomed. Eng. 51(2):371–379, 2004.

    PubMed  Google Scholar 

  22. He, X., and J. C. Bischof. Quantification of temperature and injury in thermal therapy and cryosurgery. Crit. Rev. Biomed. Eng. 31(5):355–421, 2003.

    PubMed  Google Scholar 

  23. He, X., S. Mcgee, J. E. Coad, F. Schimidlin, P. Iaizzo, D. J. Swanlund, E. Rudie, S. Kluge, and J. C. Bischof. Investigation of the thermal and tissue injury behavior in microwave thermal therapy using a porcine kidney model. Int. J. Hyperthermia 20(6):567–593, 2004.

    CAS  PubMed  Google Scholar 

  24. He, X., W. F. Wolkers, J. H. Crowe, D. J. Swanlund, and J. C. Bischof. In situ thermal denaturation of proteins in dunning AT-1 prostate cancer cells: implication for hyperthermic cell injury. Ann. Biomed. Eng. 32(10):1384–1398, 2004.

    PubMed  Google Scholar 

  25. Henriques, F. C., Jr. Studies of thermal injury, v, the predictability and the significance of thermally induced rate processes leading to irreversible epidermal injury. Arch. Pathol. 43:489–502, 1947.

    Google Scholar 

  26. Himmelblau, D. M. Applied Nonlinear Programming. New York: McGraw-Hill Inc., 1972.

    Google Scholar 

  27. Ikehara, T., H. Yamaguchi, K. Hosokawa, A. Takahashi, T. Masuya, and H. Miyamoto. Different patterns of cell volume regulation in hyposmotic media between attached and suspended HeLa cells. Biochimica et Biophysica Acta 1111(2):151–158, 1992.

    CAS  PubMed  Google Scholar 

  28. Johnson, F. H., H. Eyring, and B. J. Stoner. The Theory of Rate Process in Biology and Medicine. New York: Wiley, 1974.

    Google Scholar 

  29. Johnson, D. B., and S. Y. Nakada. Cryosurgery and needle ablation of renal lesions. J. Endourol. 15(4):361–368, 2001.

    CAS  PubMed  Google Scholar 

  30. Lepock, J. R., H. E. Frey, H. Bayne, and J. Markus. Relationship of hyperthermia-induced hemolysis of human erythrocytes to the thermal denaturation of membrane proteins. Biochimica et Biophysica Acta 980:191–201, 1989.

    CAS  PubMed  Google Scholar 

  31. Lepock, J. R., H. E. Frey, and K. P. Ritchie. Protein denaturation in intact hepatocytes and isolated cellular organelles during heat shock. J. Cell Biol. 122:1267–1276, 1993.

    CAS  PubMed  Google Scholar 

  32. Lepock, J. R., H. E. Frey, A. M. Rodahl, and J. Kruuv. Thermal analysis of CHL v79 cells using differential scanning calorimetry: Implication for hyperthermic cell killing and the heat shock response. J. Cell. Physiol. 137:14–24, 1988.

    CAS  PubMed  Google Scholar 

  33. Lui, K. W., D. A. Gervais, R. A. Arellano, and P. R. Mueller. Radiofrequency ablation of renal cell carcinoma. Clin. Radiol. 58:905–913, 2003.

    PubMed  Google Scholar 

  34. Mabjeesh, N. J., Y. Avidor, and H. Matzkin. Emerging nephron sparing treatments for kidney tumors: A continuum of modalities from energy ablation to laparoscopic partial nephrectomy. J. Urol. 171:553–560, 2004.

    PubMed  Google Scholar 

  35. McCarthy, S. A., and A. L. Miller. Effect of three biocides on Latin American and Gulf Coast strains of Toxigenic Vibro Cholerae 01. J. Food Prot. 57(10):865–869, 1994.

    CAS  Google Scholar 

  36. Murphy, D. P., and I. S. Gill. Energy-based renal tumor ablation: A review. Semin. Urol. Oncol. 2:133–140, 2001.

    Google Scholar 

  37. Pearce, J., and S. Thomsen. Rate process analysis of thermal damage. In: Optical Thermal Response of Laser-Irradiated Tissue, edited by A. J. Welch and M. J. C. van Germert. New York: Plenum Press, 1995.

    Google Scholar 

  38. Pegg, D. Viability assays for preserved cells, tissues and organs. Cryobiology 26:212–231, 1989.

    CAS  PubMed  Google Scholar 

  39. Pittman, R. N., and P. B. Molinoff. Interactions of full and partial agonists with beta-adrenergic receptors on intact L6 muscle cells. Mol. Pharmacol. 24(3):398–408, 1983.

    CAS  PubMed  Google Scholar 

  40. Reddan, D. N., G. V. Ganesh, and T. J. Polscik. Management of small renal tumors: An overview. Am. J. Med. 10:558–562, 2001.

    Google Scholar 

  41. Stopforth, J. D., J. Samelis, J. N. Sofos, P. A. Kendall, and G. C. Smith. Biofilm formation by acid-adapted and nonadapted listeria monocytogenes in fresh beef decontamination washings and its subsequent inactivation with sanitizers. J. Food Prot. 65(11):1717–1727, 2002.

    CAS  PubMed  Google Scholar 

  42. Storm, F. K. Background, principles and practice. In: Hyperthermia in Cancer Therapy, edited by F. K. Storm and G. K. Hall. Boston: Medical Publisher, 1989, pp. 47–53.

    Google Scholar 

  43. Streffer, C. Biological basis of thermotherapy (with special reference to oncology). In: Biological Basis of Oncologic Thermotherapy, edited by M. Gautherie. Berlin Heidelberg: Springer-Verlag, 1990, pp. 1–71.

    Google Scholar 

  44. Tomasovic, S. P., M. Barta, and J. Klostergard. Neutral red uptake and clonogenic survival assays of the hyperthermic sensitization of tumor cells in tumor necrosis factor. Radiat. Res. 119:325–337, 1989.

    CAS  PubMed  Google Scholar 

  45. Waring, J. G., R. Ciurlionis, R. A. Jolly, M. Heindel, G. Gange, J. A. Fagerla, and R. G. Ulrich. Isolated human hepatocytes in culture display markedly different gene expression patterns depending on attachment status. Toxicol In Vitro 17(5–6):693–701, 2003.

    CAS  PubMed  Google Scholar 

  46. Wolkers, W. F., M. Alberda, M. Koornneef, and F. A. Hoekstra. Heat stability of proteins in maturation defective mutants of Arabidopsis thaliana: A FT-IR microspectroscopy study. Plant J. 16:133–143, 1998.

    CAS  PubMed  Google Scholar 

  47. Zhang, Z. Y., R. Baron, and W. C. Horne. Integrin engagement, the actin cytoskeleton, and c-Src are required for the calcitonin-induced tyrosine phosphorylation of paxillin and HEF1, but not for calcitonin-induced Erk1/2 phosphorylation. J. Biol. Chem. 275(47):37219–37223, 2000.

    CAS  PubMed  Google Scholar 

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Author notes

  1. Xiaoming He

    Present address: Center for Engineering in Medicine: Shriners Research Center, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02114

Authors and Affiliations

  1. Departments of Mechanical Engineering, University of Minnesota, Minneapolis, MN, 55455

    Xiaoming He & John C. Bischof

  2. Urologic Surgery, University of Minnesota, Minneapolis, MN, 55455

    John C. Bischof

  3. Biomedical Engineering, University of Minnesota, Minneapolis, MN, 55455

    John C. Bischof

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  1. Xiaoming He
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Correspondence to John C. Bischof.

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He, X., Bischof, J.C. The Kinetics of Thermal Injury in Human Renal Carcinoma Cells. Ann Biomed Eng 33, 502–510 (2005). https://doi.org/10.1007/s10439-005-2508-1

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  • DOI: https://doi.org/10.1007/s10439-005-2508-1

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