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Research Article

Mild thermotolerance induced at 40 °C protects cells against hyperthermia-induced pro-apoptotic changes in Bcl-2 family proteins

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Pages 502-512 | Received 15 Jul 2014, Accepted 19 Sep 2014, Published online: 30 Oct 2014

References

  • Horsman MR, Overgaard J. Hyperthermia: A potent enhancer of radiotherapy. Clin Oncol (R Coll Radiol) 2007;19:418–26
  • Issels RD. Hyperthermia adds to chemotherapy. Eur J Cancer 2008;44:2546–54
  • van der Zee J. Heating the patient: A promising approach? Ann Oncol 2002;13:1173–84
  • van der Zee J, Vujaskovic Z, Kondo M, Sugahara T. The Kadota Fund International Forum 2004 – Clinical group consensus. Int J Hyperthermia. 2008;24:111–22
  • Milleron RS, Bratton SB. ‘Heated’ debates in apoptosis. Cell Mol Life Sci 2007;64:232:9–33
  • Lepock JR. How do cells respond to their thermal environment? Int J Hyperthermia 2005;21:681–7
  • Richter K, Haslbeck M, Buchner J. The heat shock response: Life on the verge of death. Mol Cell 2010;40:253–66
  • Bettaieb A, Averill-Bates DA. Thermotolerance induced at a mild temperature of 40 degrees C protects cells against heat shock-induced apoptosis. J Cell Physiol 2005;205:47–57
  • Bettaieb A, Averill-Bates DA. Thermotolerance induced at a fever temperature of 40 degrees C protects cells against hyperthermia-induced apoptosis mediated by death receptor signalling. Biochem Cell Biol 2008;86:521–38
  • Shellman YG, Howe WR, Miller LA, Goldstein NB, Pacheco TR, Mahajan RL, et al. Hyperthermia induces endoplasmic reticulum-mediated apoptosis in melanoma and non-melanoma skin cancer cells. J Invest Dermatol 2008;128:949–56
  • Subjeck JR, Sciandra JJ, Johnson RJ. Heat shock proteins and thermotolerance: A comparison of induction kinetics. Br J Radiol 1982;55:579–84
  • Landry J, Bernier D, Chretien P, Nicole LM, Tanguay RM, Marceau N. Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res 1982;42:2457–61
  • Przybytkowski E, Bates JH, Bates DA, Mackillop WJ. Thermal adaptation in CHO cells at 40 degrees C: The influence of growth conditions and the role of heat shock proteins. Radiat Res 1986;107:317–31
  • Singh IS, Hasday JD. Fever, hyperthermia and the heat shock response. Int J Hyperthermia 2013;29:423–35
  • Gill RR, Gbur CJ Jr, Fisher BJ, Hess ML, Fowler AA III, Kukreja RC, et al. Heat shock provides delayed protection against oxidative injury in cultured human umbilical vein endothelial cells. J Mol Cell Cardiol 1998;30:2739–49
  • Martindale JL, Holbrook NJ. Cellular response to oxidative stress: Signaling for suicide and survival. J Cell Physiol 2002;192:1–15
  • Brunelle JK, Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J Cell Sci 2009;122:437–41
  • Youle RJ, Strasser A. The BCL-2 protein family: Opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008;9:47–59
  • Szegezdi E, Macdonald DC, Ni Chonghaile T, Gupta S, Samali A. Bcl-2 family on guard at the ER. Am J Physiol Cell Physiol 2009;296:C941–53
  • Lessene G, Czabotar PE, Colman PM. BCL-2 family antagonists for cancer therapy. Nat Rev Drug Discov 2008;7:989–1000
  • Shortt J, Johnstone RW. Oncogenes in cell survival and cell death. Cold Spring Harb Perspect Biol 2012;4:a009829
  • Portt L, Norman G, Clapp C, Greenwood M, Greenwood MT. Anti-apoptosis and cell survival: A review. Biochim Biophys Acta 2011;1813:238–59
  • Samali A, Cai J, Zhivotovsky B, Jones DP, Orrenius S. Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of jurkat cells. EMBO J 1999;18:2040–8
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248–54
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680–5
  • Simon HU, Haj-Yehia A, Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000;5:415–18
  • Amaral JD, Xavier JM, Steer CJ, Rodrigues CM. The role of p53 in apoptosis. Discov Med 2010;9:145–52
  • Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005;435:677–81
  • Zhang LN, Li JY, Xu W. A review of the role of Puma, Noxa and Bim in the tumorigenesis, therapy and drug resistance of chronic lymphocytic leukemia. Cancer Gene Ther 2013;20:1–7
  • Komarov PG, Komarova EA, Kondratov RV, Christov-Tselkov K, Coon JS, Chernov MV, et al. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 1999;285:1733–7
  • Dotsch V, Bernassola F, Coutandin D, Candi E, Melino G. p63 and p73, the ancestors of p53. Cold Spring Harb Perspect Biol 2010;2:a004887
  • Melino G, Bernassola F, Ranalli M, Yee K, Zong WX, Corazzari M, et al. p73 induces apoptosis via PUMA transactivation and Bax mitochondrial translocation. J Biol Chem 2004;279:8076–83
  • Muller M, Schleithoff ES, Stremmel W, Melino G, Krammer PH, Schilling T. One, two, three – p53, p63, p73 and chemosensitivity. Drug Resist Updat 2006;9:288–306
  • Davidson W, Ren Q, Kari G, Kashi O, Dicker AP, Rodeck U. Inhibition of p73 function by Pifithrin-alpha as revealed by studies in zebrafish embryos. Cell Cycle 2008;7:1224–30
  • Bettaieb A WP, Averill-Bates DA. Hyperthermia: Cancer treatment and beyond. In: Rangel L, editor. Cancer Treatment – Conventional and Innovative Approaches. Book 2: InTech Open Access 2013, pp. 257–83. doi: 10.5772/45937
  • Tonino SH, van Laar J, van Oers MH, Wang JY, Eldering E, Kater AP. ROS-mediated upregulation of Noxa overcomes chemoresistance in chronic lymphocytic leukemia. Oncogene 2011;30:701–13
  • Yu J, Zhang L. PUMA, a potent killer with or without p53. Oncogene 2008;27:S71–83
  • Azad N, Iyer A, Vallyathan V, Wang L, Castranova V, Stehlik C, et al. Role of oxidative/nitrosative stress-mediated Bcl-2 regulation in apoptosis and malignant transformation. Ann N Y Acad Sci 2010;1203:1–6
  • Fulda S. Targeting apoptosis for anticancer therapy. Semin Cancer Biol 2014. doi: 10.1016/j.semcancer.2014.05.002
  • Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: An evolving paradigm. Nat Rev Cancer. 2013;13:714–26
  • Hildebrandt B, Wust P, Ahlers O, Dieing A, Sreenivasa G, Kerner T, et al. The cellular and molecular basis of hyperthermia. Crit Rev Oncol Hematol 2002;43:33–56
  • Pagliari LJ, Kuwana T, Bonzon C, Newmeyer DD, Tu S, Beere HM, et al. The multidomain proapoptotic molecules Bax and Bak are directly activated by heat. Proc Natl Acad Sci USA 2005;102:17975–80
  • Bonzon C, Bouchier-Hayes L, Pagliari LJ, Green DR, Newmeyer DD. Caspase-2-induced apoptosis requires bid cleavage: A physiological role for bid in heat shock-induced death. Mol Biol Cell 2006;17:2150–7
  • Mahajan IM, Chen MD, Muro I, Robertson JD, Wright CW, Bratton SB. BH3-only protein BIM mediates heat shock-induced apoptosis. PloS One 2014;9:e84388
  • Shelton SN, Dillard CD, Robertson JD. Activation of caspase-9, but not caspase-2 or caspase-8, is essential for heat-induced apoptosis in Jurkat cells. J Biol Chem 2010;285:40525–33
  • Stankiewicz AR, Livingstone AM, Mohseni N, Mosser DD. Regulation of heat-induced apoptosis by Mcl-1 degradation and its inhibition by Hsp70. Cell Death Differ 2009;16:638–47
  • Strasser A, Anderson RL. Bcl-2 and thermotolerance cooperate in cell survival. Cell Growth Differ 1995;6:799–805
  • Setroikromo R, Wierenga PK, van Waarde MA, Brunsting JF, Vellenga E, Kampinga HH. Heat shock proteins and Bcl-2 expression and function in relation to the differential hyperthermic sensitivity between leukemic and normal hematopoietic cells. Cell Stress Chaperon 2007;12:320–30
  • Robertson JD, Datta K, Kehrer JP. Bcl-xL overexpression restricts heat-induced apoptosis and influences Hsp70, Bcl-2, and Bax protein levels in FL5.12 cells. Biochem Biophys Res Commun 1997;241:164–8
  • Holsapple MP, Wallace KB. Dose response considerations in risk assessment – An overview of recent ILSI activities. Toxicol Lett 2008;180:85–92
  • Davies KJ. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 2000;50:279–89
  • Beere HM. Death versus survival: Functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J Clin Invest 2005;115:2633–9
  • Mosser DD, Morimoto RI. Molecular chaperones and the stress of oncogenesis. Oncogene 2004;23:2907–18
  • Steel R, Doherty JP, Buzzard K, Clemons N, Hawkins CJ, Anderson RL. Hsp72 inhibits apoptosis upstream of the mitochondria and not through interactions with Apaf-1. J Biol Chem 2004;279:51490–9
  • Stankiewicz AR, Lachapelle G, Foo CP, Radicioni SM, Mosser DD. Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J Biol Chem 2005;280:38729–39
  • Gabai VL, Mabuchi K, Mosser DD, Sherman MY. Hsp72 and stress kinase c-jun N-terminal kinase regulate the bid-dependent pathway in tumor necrosis factor-induced apoptosis. Mol Cell Biol 2002;22:3415–24
  • Paul C, Manero F, Gonin S, Kretz-Remy C, Virot S, Arrigo AP. Hsp27 as a negative regulator of cytochrome C release. Mol Cell Biol 2002;22:816–34
  • Hsu SF, Chao CM, Huang WT, Lin MT, Cheng BC. Attenuating heat-induced cellular autophagy, apoptosis and damage in H9c2 cardiomyocytes by pre-inducing Hsp70 with heat shock preconditioning. Int J Hyperthermia 2013;29:239–47
  • Rooswinkel RW, van de Kooij B, Verheij M, Borst J. Bcl-2 is a better ABT-737 target than Bcl-xL or Bcl-w and only Noxa overcomes resistance mediated by Mcl-1, Bfl-1, or Bcl-B. Cell Death Dis 2012;3:e366
  • Andreu-Fernandez V, Genoves A, Messeguer A, Orzaez M, Sancho M, Perez-Paya E. BH3-mimetics- and cisplatin-induced cell death proceeds through different pathways depending on the availability of death-related cellular components. PloS One 2013;8:e56881
  • Cragg MS, Harris C, Strasser A, Scott CL. Unleashing the power of inhibitors of oncogenic kinases through BH3 mimetics. Nat Rev Cancer 2009;9:321–6
  • Fang H, Harned TM, Kalous O, Maldonado V, DeClerck YA, Reynolds CP. Synergistic activity of fenretinide and the Bcl-2 family protein inhibitor ABT-737 against human neuroblastoma. Clin Cancer Res 2011;17:7093–104
  • Wilson WH, O’Connor OA, Czuczman MS, LaCasce AS, Gerecitano JF, Leonard JP, et al. Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: A phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. Lancet Oncol 2010;11:1149–59
  • Gandhi L, Camidge DR, Ribeiro de Oliveira M, Bonomi P, Gandara D, Khaira D, et al. Phase I study of Navitoclax (ABT-263), a novel Bcl-2 family inhibitor, in patients with small-cell lung cancer and other solid tumors. J Clin Oncol 2011;29:909–16
  • Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR. Heat shock proteins in cancer: Chaperones of tumorigenesis. Trends Biochem Sci 2006;31:164–72

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