106
Views
10
CrossRef citations to date
0
Altmetric
Original Article

Thermal stress and the disruption of redox-sensitive signalling and transcription factor activation: possible role in radiosensitization

, , , &
Pages 213-223 | Received 04 Mar 2003, Accepted 14 Aug 2003, Published online: 09 Jul 2009

References

  • Halliwell B, Gutteridge JM. Free radicals and antioxidant protection: mechanisms and significance in toxicology and disease. Hum Toxicol 1988; 7: 7–13.
  • Holbrook NK, Fornace AJ. Response to adversity: molecular control of gene activation following genotoxic stress. New Biol 1991; 3: 825–33.
  • Weichselbaum RR, Hallahan DE, Fuks Z, Kufe, D. Radiation induction of immediate early genes: effectors of the radiation-stress response. Int J Radiat Oncol Biol Phys 1994; 30: 229–34.
  • Maity A, Kao GD, Muschel RJ, McKenna, WG. Potential molecular targets for manipulating the radiation response. Int J Radiat Oncol Biol Phys 1997; 37: 639–53.
  • Alpert D, Schwenger P, Han J, Vilcek J. Cell stress and MKK6b-mediated p38 MAP kinase activation inhibit tumor necrosis factor-induced I-kB phosphorylation and NF-kB activation. J Biol Chem 1999; 274: 22176–83.
  • Karin M, Smeal T. Control of transcription factors by signal transduction pathways: the beginning of the end. Trends Biochern Sci 1992; 17: 418–22.
  • Bergelson S, Pinkus R, Daniel V. Intracellular glutathione levels regulate Fos/Jun induction and activation of glutathione S-transferase gene expression. Cancer Res 1994; 54: 36–40.
  • Hill CS, Treisman R. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell 1995; 80: 199–211.
  • Datta R, Hallahan SE, Kharbanda M, Rubin E, Sherman ML, Huberman E, Weichselbaum RR, Kufe DW. Involvement of reactive oxygen intermediates in the induc-tion of c-jun gene transcription by ionizing radiation. Biochemistry 1992; 31: 8300–6.
  • Hallahan DE, Gius D, Kuchibhotla J, Sukhatme V, Kufe DW, Weichselbaum RR. Radiation signaling mediated by Jun activation following dissociation from a cell type-specific repressor. J Biol Chem 1993; 268: 4903–7.
  • Hallahan DE, Dunphy E, Virudachalam S, Sukhatme VP, Kufe DW, Weichselbaum RR. c-jun and Egr-1 participate in DNA synthesis and cell survival in response to ionizing radiation. J Biol Chem 1995; 270: 30303–9.
  • Neta R, Oppenheim .1.1, Douches SD. Interdependence of the radioprotective effects of human recombinant IL-1a, TNF-c, G-CSF in murine recombinant G-CSF. J Immunol 1988; 140: 108–11.
  • Kasid U, Suy S, Dent P, Ray S, Whiteside TL, Sturgill TW. Activation of Raf by ionizing radiation. Nature 1996; 382: 813–16.
  • Connor WG, Gerner EW, Miller RC, Boone ML. Prospects for hyperthermia in human cancer therapy: II. Implications of biological and physical data for applications of hyperthermia to man. Radiology 1977; 123: 497.
  • Dewey WC, Freeman ML, Raaphorst GP. Cell biology of hyperthermia and radiation. In: Meyn RE, Withers HR, eds. Radiation Biology in Cancer Research, New York: Raven, 1980: 589.
  • Dewey WC. Arrhenius relationships from the molecule and cell to the clinic. Int J Hypertherrnia 1994; 10: 457–63.
  • Sinclair WK. Protection by cysteamine against lethal x-ray damage during the cell cycle of Chinese hamster cells. Radiat Res 1969; 39: 135–54.
  • Sukhatme VP, Cao XM, Chang LC, Tsai-Morris CH, Stamenkovich D, Ferreira PC, Cohen DR, Edwards SA, Shows TB, Curran T. A zinc finger-encoding gene coregu-lated with c-fos during growth and differentiation, and after cellular depolarization. Cell 1988; 53: 37–43.
  • Overgaard J. The current and potential role of hyperthermia in radiotherapy. Int J Radiat Oncol Biol Phys 1989; 16: 535–49.
  • Iliakis G, Seaner R, Okayasu R. Effects of hyperthermia on the repair of radiation-induced DNA single- and double-strand breaks in DNA double-strand break repair-deficient and repair-proficient cell lines. Int J Hypertherrnia 1990; 6: 813–33.
  • Lin P-S, Quamo S, Ho KC, Gladding J. Hyperthermia enhances the cytotoxic effect of reactive oxygen species in Chinese hamster cells and bovine endothelized cells in vitro. Radiat Res 1991; 126: 43–51.
  • Urano M, Tanaka N. The effect of preirradiated tumour bed on the response of a murine fibrosarcoma to elevated temperatures. Int J Hypertherrnia 1989; 5: 617–24.
  • Brizel DM, Scully SP, Harrelson JM, Layfield Li, Dodge RK, Charles HC, Samulski TV, Prosnitz LR, Dewhirst MW. Radiation therapy and hyperthermia improve the oxygena-tion of human soft tissue sarcomas. Cancer Res 1996; 56: 5347–50.
  • Batandier C, Fontaine E, Keriel C, Leverve XM. Determination of mitochondrial reactive oxygen species: methodological aspects. J Cell Mol Med 2002; 6: 175–87.
  • Copeland WC, Wachsman JT, Johnson FM, Penta JS. Mitochondrial DNA alterations in cancer. Cancer Invest 2002; 20: 557–69.
  • Spitz DR, Sim JE, Ridnour LA, Galoforo SS, Lee YJ: Glucose deprivation-induced oxidative stress in human tumor cells: a fundamental defect in metabolism? Ann NY Acad Sci 2000; 899: 349–62.
  • Sies, H. Oxidative stress: from basic research to clinical application. Am J Med 1991; 91(Suppl. 3C): 31S–38S.
  • Spitz DR, Li GC: Heat-induced cytotoxicity in H202-resistant Chinese hamster fibro-blasts. J Cell Physiol 1990; 142: 255–60.
  • Stevenson MA, Pollock SS, Coleman CN, Calderwood SK. X-irradiation, phorbol esters, and H202 stimulate mitogen-activated protein kinase activity in NIH-3T3 cells through the formation of reactive oxygen intermediates. Cancer Res 1994; 54: 12–15.
  • Demple B, Amabile-Cuevas CF. Redox redux: the control of oxidative stress responses. Cell 1991; 67: 837–9.
  • Ishii T, Sugita Y, Bonnai S. Regulation of glutathione levels in mouse spleen lymphocytes by transport of cysteine. J Cell Physiol 1987; 133: 330–6.
  • Hwang C, Sinskey A.1, Lodish HF. Oxidized redox state of glutothione in the endoplasmic reticulum. Science 1992; 257: 1496–502.
  • De Bleser RI, Xu G, Rombouts K, Rogiers V, Geerts A. Glutathione levels discriminate between oxidative stress and transforming growth factor-beta signaling in activated rat hepatic satellite cells. Biol Chem 1999; 274: 33881–7.
  • Yang JQ, Buettner GR, Domann FE, Li Q, Engelhardt JF, Weydert CD, Oberley LW. v-Ha-ras mitogenic signaling through superoxide and derived reactive oxygen species. Mol Carcinog 2002; 33: 206–18.
  • Nishinaka T, Yabe-Nishimura C. EGF receptor-ERK pathway is the major signaling pathway that mediates upregulation of aldose reductase expression under oxidative stress. Free Radic Biol Med 2001; 31: 205–16.
  • Nakashima I, Kato M, Akhand AA, Suzuki H, Takeda K, Hossain K, Kawamoto Y. Redox-linked signal transduction pathways for protein tyrosine kinase activation. Antioxid Redox Signal 2002; 4: 517–31.
  • Rincon M, Flavell RA, Davis RA. The JNK and p38 MAP kinase signaling pathways in T cell-mediated immune responses. Free Radic Biol Med 2000; 28: 1328–37.
  • Owuor ED, Kong AN. Antioxidants and oxidants regulated signal transduction path-ways. Biochern Pharmacol 2002; 64: 765–70.
  • Blanc A, Pandey NR, Srivastava AK. Synchronous activation of ERK 1/2, p38mapk and PKB/Akt signaling by H202 in vascular smooth muscle cells: Potential involvement in vascular disease. Int J Mol Med 2003; 11: 229–34.
  • Griendling KK, Sorescu D, Lassegue B, Ushio-Fukai M. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiol-ogy and pathophysiology. Arterioscler Thrornb Vase Biol 2000; 20: 2175–83.
  • Inoshita S, Takeda K, Hatai T, Terada Y, Sano M, Hata J, Umezawa A, Ichijo H. Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative. J Biol Chem 2002; 277: 43730–4.
  • Matsuzawa A, Nishitoh H, Tobiume K, Takeda K, Ichijo H. Physiological roles of ASK1-mediated signal transduction in oxidative stress- and endoplasmic reticulum stress-induced apoptosis: advanced findings from ASK1 knockout mice. Antioxid Redox Signal 2002; 4: 415–25.
  • Deora AA, Win T, Vanhaesebroeck B, Lander HM. A redox-triggered ras-effector interaction. Recruitment of phosphatidylinositol 3'-kinase to Ras by redox stress. J Biol Chem 1998; 273: 29923–8.
  • Gius D, Botero A, Shah S, Curry HA. Intracellular oxidation/reduction status in the regulation of transcription factors NF-kappaB and AP-1. Toxicol Lett 1999; 106: 93–106.
  • Abate C, Patel L, Rauscher FJ III, Curran T. Redox regulation of Fos and Jun DNA-binding activity in vitro. Science 1990; 249: 1157–61.
  • Xanthoudakis S, Curran T. Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity. EMBO J 1992; 11: 653–64.
  • Diamond DA, Parsian A, Hunt CR, Lofgren S, Spitz DR, Goswami PC, Gius D. J Biol Chem 1999; 274: 1659–64.
  • Kerppola TK, Curran, T. Transcription: Zen and the art of FOS and JUN. Nature 1995; 373: 199–200.
  • Guyton KZ, Spitz DR, Holbrook NJ. Expression of stress response genes GADD153, c-jun, and heme oxygenase-1 in H202- and 02-resistant fibroblasts. Free Rad Biol Med 1996; 20: 735–41.
  • Halliwell B, Gutteridge JM. Role of free radicals and catalytic metal ions in oxyen inter-mediates. Methods Enzyrnol 1990; 186: 1–85.
  • Morgan JI, Curran T. Immediate-early genes: ten years on. Trends Neurosci 1995; 18: 66–7.
  • Lindquist S, Kim G. Heat-shock protein 104 expression is sufficient for thermotolerance in yeast. Proc Natl Acad Sci USA 1996; 93: 5301–6.
  • Morimoto RI, Kroeger PE, Cotto JJ. The transcriptional regulation of heat shock genes: a plethora of heat shock factors and regulatory conditions. EXS 1996; 77: 139–63.
  • Chen C, Xie Y, Stevenson MA, Auron PE, Calderwood SK. Heat shock factor 1 represses ras-induced transcriptional activation of the c-fos gene. J Biol Chem 1997; 272: 26803–6.
  • Dubois M, Bensaude O. MAP kinase activation during heat shock in quiescent and exponentially growing mammalian cells. FEBS Lett 1993; 324: 191–5.
  • Kamada Y, Jung US, Piotrowski J, Levin DE. The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev 1995; 9: 1559–71.
  • Kozawa O, Niwa M, Matsuno H, Tokuda H, Miwa M, Ito H, Kato K, Uematsu T. Sphingosine 1-phosphate induces heat shock protein 27 via p38 mitogen-activated protein kinase activation in osteoblasts. J Bone Min Res 1999; 14: 1761–7.
  • Rouse J, Cohen P, Trigon S, Morange M, Alonso-Llamazares A, Zamanillo D, Hunt T, Nebreda A. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 1994; 78: 1027–37.
  • Jurivich DA, Sistonen L, Sarge KD, Morimoto RI. Effect of sodium salicylate on the human heat shock response. Science 1992; 265: 1243–5.
  • Jurivich DA, Pachetti C, Qiu L, Welk JF. Salicylate triggers heat shock factor differently than heat. J Biol Chem 1995; 270: 24489–95.
  • Nguyen AN, Shiozaki K. Heat-shock-induced activation of stress MAP kinase is regu-lated by threonine- and tyrosine-specific phosphatases. Genes Dev 1999; 13: 1653–63.
  • Adler V, Schaffer A, Kim J, Dolan L, Ronai Z. UV irradiation and heat shock mediate JNK activation via alternate pathways. J Biol Chem 1995; 270: 26071–7.
  • Wooten MW. Alterations in protein kinase C type III-alpha during heat shock of rat embryo fibroblasts. Exp Cell Res 1991; 193: 274–8.
  • Roulston A, Reinhard C, Amiri P, Williams LT. Early activation of c-Jun N-terminal kinase and p38 regulate cell survival in response to tumor necrosis factor-a. J Biol Chem 1998; 273: 10232–9.
  • Ohnishi T, Wang X, Ohnishi K, Matsumoto H, Takahashi A. p53-dependent induction of WAF1 by heat treatment in human glioblastoma cells. J Biol Chem 1996; 271: 14510–13.
  • Fuse T, Yamada K, Asai K, Kato T, Nakanishi M. Heat shock-mediated cell cycle arrest is accompanied by induction of p21 CKI. Biochern Biophys Res Commun 1996; 225: 759–63.
  • Yamashita N, Hoshida S, Taniguchi N, Kuzuya T, Hon i M. Whole-body hyperthermia provides biphasic cardioprotection against ischemia/reperfusion injury in the rat. Circulation 1998; 98: 1414–21.
  • Lim CP, Jain N, Cao X. Stress-induced immediate-early gene, egr-1, involves activation of p38/JNK1. Oncogene 1998; 16: 2915–26.
  • Sikora E, Grassilli E, Radziszewska E, Bellesia E, Barbieri D, Franceschi C. Transcription factors DNA-binding activity in rat thymocytes undergoing apoptosis after heat-shock or dexamethasone treatment. Biochern Biophys Res Commun 1993; 197: 709–15.
  • Ghoshal K, Jacob ST. Heat shock selectively inhibits ribosomal RNA gene transcription and down-regulates ElBF/Ku in mouse lymphosarcoma cells. Biochern J 1996; 317: 689–95.
  • Balcer-Kubiczek EK, Harrison GH, Davis CC, Haas ML, Koffman BH. Expression analysis of human HL60 cells exposed to 60 Hz square- or sine-wave magnetic fields. Radiat Res 2000; 153: 670–78.
  • Eisenman RN. Deconstructing myc. Genes Dev 2001; 15: 2023–30.
  • Bradbury CM, Markovina S, Wei SJ, Rene LM, Zoberi I, Horikoshi N, Gius D. Indomethacin-induced radiosensitization and inhibition of ionizing radiation-induced NF-KB activation in HeLa cells occur via a mechanism involving p38 MAP kinase. Cancer Res 2001; 61: 7689–96.
  • Guo G, Yan-Sanders Y, Lyn-Cook BD, Wang T, Tamae D, Ogi J, Khaletskiy A, Li Z, Weydert C, Longmate JA, Huang T-T, Spitz DR, Oberley LW, Li JJ. Manganese superoxide dismutase-mediated gene expression in radiation-induced adaptive responses. Mol Cell Biol 2003; 23: 2362–78.
  • Curry HA, Clemens RA, Botero A, Bradbury CM, Spitz DR, Goswami P, Gius D. Heat shock inhibits radiation-induced activation of NF-KB via inhibition of the I-KB kinase complex. J Biol Chem 1999; 274: 23061–7.
  • Sonna LA, Fujita J, Gaffin SL, Lilly CM. Molecular Biology of Thermoregulation: Invited Review: Effects of heat and cold stress on mammalian gene expression. J Appl Physiol 2002; 92: 1725–42.
  • Yoo CG, Lee S, Lee CT, Kim YW, Han SK, Shim YS. Anti-inflammatory effect of heat shock protein induction is related to stabilization of IB through preventing IB activation in respiratory epithelial cells. J Imrnunol 2000; 164: 5416–23.
  • Lord-Fontaine S, Averill-Bates DA. Heat shock inactivates cellular antioxidant defenses against hydrogen peroxide: protection by glucose. Free Radic Biol Med 2002; 32: 752–65.
  • Morimoto RI, Kline MP, Bimston DN, Cotto JJ. The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochern 1997; 32: 17–29.
  • Morimoto RI, Santoro MG. Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat Biotechnol 1998; 16: 833–8.
  • Pirkkala L, Nykanen P, Sistonen L. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 2001; 15: 1118–31.
  • Cotto J, Kline M, Morimoto R. J Biol Chem 1996; 271: 3355–8.
  • Vujaskovic Z, Poulson JM, Gaskin AA, Thrall DE, Page RL, Charles HC, MacFall JR, Brizel DM, Meyer RE, Prescott DM, Samulski TV, Dewhirst MW. Temperature-depen-dent changes in physiologic parameters of spontaneous canine soft tissue sarcomas after combined radiotherapy and hyperthermia treatment. Int .1 Radiat Oncol Biol Phys 2000; 46: 179–85.
  • Mitchell JB, Russo A. Thiols, thiol depletion, and thermosensitivity. Radiat Res 1983; 95: 471–85.
  • Spitz DR, Dewey WC, Li GC: Hydrogen peroxide or heat shock induces resistance to hydrogen peroxide in Chinese hamster fibroblasts. J Cell Physiol 1987; 131: 364–73.
  • Freeman M, Spitz D, Meredith M. Does heat shock enhance oxidative stress? Studies with ferrous and ferric iron. Radiat Res 1990; 124: 288–93.
  • Polla BS, Kentengwa S, Francois D, Salvioloi S, Franceschi C, Marsac C, Cossarizza A. Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc Natl Acad Sci USA 1996; 93: 6458–63.
  • Morimoto RI. Regulation of the heat shock transcriptional response: Cross-talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 1998; 12: 3788–96.
  • Sarge KD, Murphy SP, Morimoto RI. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol Cell Biol 1993; 13: 1392–407.
  • Zuo J, Rungger D, Voellmy R. Multiple layers of regulation of human heat shock transcription factor 1. Mol Cell Biol 1995; 15: 4319–30.
  • Orosz A, Wisniewski J, Wu C. Regulation of Drosophila heat shock factor trimerization: global sequence requirements and independence of nuclear localization. Mol Cell Biol 1996; 16: 7018–30.
  • Morano KA, Thiele DJ. The Sch9 protein kinase regulates Hsp90 chaperone complex signal transduction activity in vivo. EMBO J 1999; 18: 5953–62.
  • Ahn SG, Thiele DJ. Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 2003; 17: 516–28.
  • Guyton KZ, Spitz DR, Holbrook NJ. Expression of stress response genes GADD153, c-jun, and heme oxygenase-1 in H202- and 02-resistant fibroblasts. Free Rad Biol Med 1996; 20: 735–41.
  • Gius D, Cao X, Rauscher FJ III, Cohen DR, Curran T, Sukhatme VP. Transcriptional activation and repression by Fos are independent functions: the C-terminus represses immediate-early gene expression via CArG elements. Mol Cell Biol 1990; 10: 4243–55.
  • Privalle CT, Fridovich I. Induction of superoxide dismutase in Escherichia coli by heat shock. Proc Natl Acad Sci USA 1987; 84: 2723–6.
  • Hall DM, Buettner GR, Matthes RD, Gisolfi CV. Hyperthermia stimulates nitric oxide formation: electron paramagnetic resonance detection of NO-heme in blood. J Appl Physiol 1994; 77: 548–53.
  • Davidson JF, Whyte B, Bissinger PH, Schiestl RH. Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1996; 93: 5116–21.
  • Flanagan SW, Moseley PL, Buettner GR. Increased flux of free radicals in cells subjected to hyperthermia: detection by electron paramagnetic resonance spin trapping. FEBS Lett 1998; 431: 285–6.

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.