Combined treatment with modulated electro-hyperthermia and an autophagy inhibitor effectively inhibit ovarian and cervical cancer growth

Reference

• McGuire S. World Cancer Report 2014. Geneva, Switzerland: World Health Organization, International Agency for Research on Cancer, WHO Press, 2015. Adv Nutr. 2016;7:418–419.
   PubMed Web of Science ®Google Scholar
• Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2017. CA Cancer J Clin. 2017;67:7.
   PubMed Web of Science ®Google Scholar
• Hisamatsu T, Mabuchi S, Yoshino K, et al. Prediction of progression-free survival and response to paclitaxel plus carboplatin in patients with recurrent or advanced cervical cancer. Int J Gynecol Cancer. 2012;22:623–629.
   PubMed Web of Science ®Google Scholar
• Dixon SC, Nagle CM, Wentzensen N, et al. Use of common analgesic medications and ovarian cancer survival: results from a pooled analysis in the Ovarian Cancer Association Consortium. Br J Cancer. 2017;116:1223–1228. doi: 10.1038/bjc.2017.68.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature. 2011;474:609–615.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research Network, Albert Einstein College of Medicine, Analytical Biological Services et. al. Integrated genomic and molecular characterization of cervical cancer. Nature. 2017;543:378–384.
   PubMed Web of Science ®Google Scholar
• Fong PC, Boss DS, Yap TA, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med. 2009;361:123–134.
   PubMed Web of Science ®Google Scholar
• Ledermann J, Harter P, Gourley C, et al. Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol. 2014;15:852–861.
   PubMed Web of Science ®Google Scholar
• Oza AM, Cibula D, Benzaquen AO, et al. Olaparib combined with chemotherapy for recurrent platinum-sensitive ovarian cancer: a randomised phase 2 trial. Lancet Oncol. 2015;16:87–97.
   PubMed Web of Science ®Google Scholar
• Ledermann JA, Harter P, Gourley C, et al. Overall survival in patients with platinum-sensitive recurrent serous ovarian cancer receiving olaparib maintenance monotherapy: an updated analysis from a randomised, placebo-controlled, double-blind, phase 2 trial. Lancet Oncol. 2016;17:1579–1589.
   PubMed Web of Science ®Google Scholar
• Chicheł A, Skowronek J, Kubaszewska M, et al. Hyperthermia – description of a method and a review of clinical applications. Rep Pract Oncol Radiother. 2007;12:267–275.
   Google Scholar
• Hildebrandt B, Wust P, Ahlers O, et al. The cellular and molecular basis of hyperthermia. Crit Rev Oncol Hematol. 2002;43:33–56.
   PubMed Web of Science ®Google Scholar
• Wust P, Hildebrandt B, Sreenivasa G, et al. Hyperthermia in combined treatment of cancer. Lancet Oncol. 2002;3:487–497.
   PubMed Web of Science ®Google Scholar
• Fotopoulou C, Cho CH, Kraetschell R, et al. Regional abdominal hyperthermia combined with systemic chemotherapy for the treatment of patients with ovarian cancer relapse: results of a pilot study. Int J Hyperthermia. 2010;26:118–126.
   PubMed Web of Science ®Google Scholar
• Andocs G, Rehman MU, Zhao QL, et al. Comparison of biological effects of modulated electro-hyperthermia and conventional heat treatment in human lymphoma U937 cells. Cell Death Dis. 2016;2:16039.
   PubMed Web of Science ®Google Scholar
• Andocs G, Szasz O, Szasz A. Oncothermia treatment of cancer: from the laboratory to clinic. Electromagn Biol Med. 2009;28:148–165.
   PubMed Web of Science ®Google Scholar
• Yang KL, Huang CC, Chi MS, et al. In vitro comparison of conventional hyperthermia and modulated electro-hyperthermia. Oncotarget. 2016;7:84082–84092.
   PubMedGoogle Scholar
• Meggyeshazi N, Andocs G, Balogh L, et al. DNA fragmentation and caspase-independent programmed cell death by modulated electrohyperthermia. Strahlenther Onkol. 2014;190:815–822.
   PubMed Web of Science ®Google Scholar
• Tsang YW, Huang CC, Yang KL, et al. Improving immunological tumor microenvironment using electro-hyperthermia followed by dendritic cell immunotherapy. BMC Cancer. 2015;15:708. doi: 10.1186/s12885-015-1690-2.
   PubMed Web of Science ®Google Scholar
• Cha J, Jeon TW, Lee CG, et al. Electro-hyperthermia inhibits glioma tumorigenicity through the induction of E2F1-mediated apoptosis. Int J Hyperthermia. 2015;31:784–792.
   PubMed Web of Science ®Google Scholar
• Wilde L, Tanson K, Curry J, et al. Autophagy in cancer: a complex relationship. Biochem J. 2018;475:1939–1954.
   PubMed Web of Science ®Google Scholar
• Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221:3–12.
   PubMed Web of Science ®Google Scholar
• Friant S, Meier KD, Riezman H. Increased ubiquitin-dependent degradation can replace the essential requirement for heat shock protein induction. EMBO J. 2003;22:3783–3791.
   PubMed Web of Science ®Google Scholar
• Maiuri MC, Zalckvar E, Kimchi A, et al. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol. 2007;8:741–752.
   PubMed Web of Science ®Google Scholar
• Salomons FA, Menendez-Benito V, Bottcher C, et al. Selective accumulation of aggregation-prone proteasome substrates in response to proteotoxic stress. Mol Cell Biol. 2009;29:1774–1785.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Calderwood SK. Autophagy, protein aggregation and hyperthermia: a mini-review. Int J Hyperthermia. 2011;27:409–414.
   PubMed Web of Science ®Google Scholar
• Lavandero S, Chiong M, Rothermel BA, et al. Autophagy in cardiovascular biology. J Clin Invest. 2015;125:55–64.
   PubMed Web of Science ®Google Scholar
• White E. The role for autophagy in cancer. J Clin Invest. 2015;125:42–46.
   PubMed Web of Science ®Google Scholar
• Yang Z, Goronzy JJ, Weyand CM. Autophagy in autoimmune disease. J Mol Med. 2015;93:707–717.
   PubMed Web of Science ®Google Scholar
• Bellmann K, Charette SJ, Nadeau PJ, et al. The mechanism whereby heat shock induces apoptosis depends on the innate sensitivity of cells to stress. Cell Stress Chaperones. 2010;15:101–113.
   PubMed Web of Science ®Google Scholar
• Monastyrska I, Klionsky DJ. Autophagy in organelle homeostasis: peroxisome turnover. Mol Asp Med. 2006;27:483–494.
   PubMedGoogle Scholar
• Rubinsztein DC, Gestwicki JE, Murphy LO, et al. Potential therapeutic applications of autophagy. Nat Rev Drug Discov. 2007;6:304–312.
   PubMed Web of Science ®Google Scholar
• Kameda K, Kondo T, Tanabe K, et al. 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. 2001;49:1369–1379.
   PubMed Web of Science ®Google Scholar
• Hirano H, Tabuchi Y, Kondo T, et al. Analysis of gene expression in apoptosis of human lymphoma U937 cells induced by heat shock and the effects of alpha-phenyl N-tert-butylnitrone (PBN) and its derivatives. Apoptosis. 2005;10:331–340.
   PubMed Web of Science ®Google Scholar
• Wada S, Tabuchi Y, Kondo T, et al. Gene expression in enhanced apoptosis of human lymphoma U937 cells treated with the combination of different free radical generators and hyperthermia. Free Radic Res. 2007;41:73–81.
   PubMed Web of Science ®Google Scholar
• Haynes MK, Strouse JJ, Waller A, et al. Detection of intracellular granularity induction in prostate cancer cell lines by small molecules using the HyperCyt high-throughput flow cytometry system. J Biomol Screen. 2009;14:596–609.
   PubMed Web of Science ®Google Scholar
• Sherwood SW, Rush D, Ellsworth JL, et al. Defining cellular senescence in IMR-90 cells: a flow cytometric analysis. Proc Natl Acad Sci USA. 1988;85:9086–9090.
   PubMed Web of Science ®Google Scholar
• Barranco WT, Eckhert CD. Cellular changes in boric acid-treated DU-145 prostate cancer cells. Br J Cancer. 2006;94:884–890.
   PubMed Web of Science ®Google Scholar
• Dive C, Gregory CD, Phipps DJ, et al. Analysis and discrimination of necrosis and apoptosis (programmed cell death) by multiparameter flow cytometry. Biochim Biophys Acta. 1992;1133:275–285.
   PubMed Web of Science ®Google Scholar
• Pal S, Salunke-Gawalib S, Konkimallaa VB. Induction of autophagic cell death in apoptosis-resistant pancreatic cancer cells using benzo[alpha]phenoxazines derivatives, 10-methyl-benzo[alpha]phenoxazine-5-one and benzo[alpha]phenoxazine-5-one. Anticancer Agents Med Chem. 2017;17:115–125.
   PubMed Web of Science ®Google Scholar
• Kaluđerović MR, Mojić M, Schreckenbach JP, et al. A key role of autophagy in osteoblast differentiation on titanium-based dental implants. Cells Tissues Organs. 2014;200:265–277.
   PubMed Web of Science ®Google Scholar