Heat-induced BRCA2 degradation in human tumours provides rationale for hyperthermia-PARP-inhibitor combination therapies

References

• Horsman MR, Overgaard J. (2007). Hyperthermia: a potent enhancer of radiotherapy. Clin Oncol (R Coll Radiol) 19:418–26.
   PubMed Web of Science ®Google Scholar
• Issels RD. (2008). Hyperthermia adds to chemotherapy. Eur J Cancer 44:2546–54.
   PubMed Web of Science ®Google Scholar
• Van Der Zee J, De Bruijne M, Mens JWM, et al. (2010). Reirradiation combined with hyperthermia in breast cancer recurrences: overview of experience in Erasmus MC. Int J Hyperth 26:638–48.
   PubMed Web of Science ®Google Scholar
• Linthorst M, Baaijens M, Wiggenraad R, et al. (2015). Local control rate after the combination of re-irradiation and hyperthermia for irresectable recurrent breast cancer: results in 248 patients. Radiother Oncol 117:217–22.
   PubMed Web of Science ®Google Scholar
• van der Zee J, van Rhoon GC. (2006). Cervical cancer: radiotherapy and hyperthermia. Int J Hyperthermia 22:229–34.
   PubMed Web of Science ®Google Scholar
• Franckena M. (2012). Review of radiotherapy and hyperthermia in primary cervical cancer. Int J Hyperthermia 28:543–8.
   PubMed Web of Science ®Google Scholar
• Paulides MM, Verduijn GM, Van Holthe N. (2016). Status quo and directions in deep head and neck hyperthermia. Radiat Oncol 11:21.
   PubMed Web of Science ®Google Scholar
• Datta NR, Rogers S, Ordonez SG, et al. (2016). Hyperthermia and radiotherapy in the management of head and neck cancers: a systematic review and meta-analysis. Int J Hyperthermia 32:31–40.
   PubMed Web of Science ®Google Scholar
• Rampersaud EN, Vujaskovic Z, Inman BA. (2010). Hyperthermia as a treatment for bladder cancer. Oncology (Williston Park, N.Y.) 24:1149–55.
   PubMed Web of Science ®Google Scholar
• Longo TA, Gopalakrishna A, Tsivian M, et al. (2016). A systematic review of regional hyperthermia therapy in bladder cancer. Int J Hyperthermia 32:381–9.
   PubMed Web of Science ®Google Scholar
• Crezee H, Inman BA. (2016). The use of hyperthermia in the treatment of bladder cancer. Int J Hyperthermia 32:349–50.
   PubMed Web of Science ®Google Scholar
• Wust P, Hildebrandt B, Sreenivasa G, et al. (2002). Hyperthermia in combined treatment of cancer. Lancet Oncol 3:487–97.
   PubMed Web of Science ®Google Scholar
• Dewhirst MW, Lee C-T, Ashcraft KA. (2016). The future of biology in driving the field of hyperthermia. Int J Hyperthermia 32:4–13.
   PubMed Web of Science ®Google Scholar
• van den Tempel N, Horsman MR, Kanaar R. (2016). Improving efficacy of hyperthermia in oncology by exploiting biological mechanisms. Int J Hyperthermia 32:446–54.
   PubMed Web of Science ®Google Scholar
• Vujaskovic Z, Song CW. (2004). Physiological mechanisms underlying heat-induced radiosensitization. Int J Hyperthermia 20:163–74.
   PubMed Web of Science ®Google Scholar
• Evans SS, Repasky EA, Fisher DT. (2015). Fever and the thermal regulation of immunity: the immune system feels the heat. Nat Rev Immunol 15:335–49.
   PubMed Web of Science ®Google Scholar
• Datta NR, Ordóñez SG, Gaipl US, et al. (2015). Local hyperthermia combined with radiotherapy and-/or chemotherapy: recent advances and promises for the future. Cancer Treat Rev 41:742–53.
   PubMed Web of Science ®Google Scholar
• Roti Roti JL. (2008). Cellular responses to hyperthermia (40–46 degrees C): cell killing and molecular events. Int J Hyperthermia 24:3–15.
   PubMed Web of Science ®Google Scholar
• Krawczyk PM, Eppink B, Essers J, et al. (2011). Mild hyperthermia inhibits homologous recombination, induces BRCA2 degradation, and sensitizes cancer cells to poly (ADP-ribose) polymerase-1 inhibition. Proc Natl Acad Sci USA 108:9851–6.
   PubMed Web of Science ®Google Scholar
• Jasin M, Rothstein R. (2013). Repair of strand breaks by homologous recombination. Cold Spring Harb Perspect Biol 5:a012740.
   PubMed Web of Science ®Google Scholar
• Moynahan ME, Pierce AJ, Jasin M. (2001). BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell 7:263–72.
   PubMed Web of Science ®Google Scholar
• Tarsounas M, Davies D, West SC. (2003). BRCA2-dependent and independent formation of RAD51 nuclear foci. Oncogene 22:1115–23.
   PubMed Web of Science ®Google Scholar
• Thorslund T, West SC. (2007). BRCA2: a universal recombinase regulator. Oncogene 26:7720–30.
   PubMed Web of Science ®Google Scholar
• Bryant HE, Schultz N, Thomas HD, et al. (2005). Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434:913–7.
   PubMed Web of Science ®Google Scholar
• Farmer H, McCabe N, Lord CJ, et al. (2005). Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434:917–21.
   PubMed Web of Science ®Google Scholar
• Saleh-Gohari N, Bryant HE, Schultz N, et al. (2005). Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol Cell Biol 25:7158–69.
   PubMed Web of Science ®Google Scholar
• Brown JS, Kaye SB, Yap TA. (2016). PARP inhibitors: the race is on. Br J Cancer 114:713–5.
   PubMed Web of Science ®Google Scholar
• Alexandrov LB, Nik-Zainal S, Wedge DC, et al. (2013). Signatures of mutational processes in human cancer. Nature 500:415–21.
   PubMed Web of Science ®Google Scholar
• van Rhoon GC, Rietveld PJ, van der Zee J. (1998). A 433 MHz Lucite cone waveguide applicator for superficial hyperthermia. Int J Hyperthermia 14:13–27.
   PubMed Web of Science ®Google Scholar
• Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. (1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–75.
   PubMed Web of Science ®Google Scholar
• Schindelin J, Arganda-Carreras I, Frise E, et al. (2012). Fiji: an open source platform for biological image analysis. Nat Methods 9:676–82.
   PubMed Web of Science ®Google Scholar
• Franckena M, Fatehi D, De Bruijne M, et al. (2009). Hyperthermia dose-effect relationship in 420 patients with cervical cancer treated with combined radiotherapy and hyperthermia. Eur J Cancer 45:1969–78.
   PubMed Web of Science ®Google Scholar
• Oldenborg S, Griesdoorn V, van Os R, et al. (2015). Reirradiation and hyperthermia for irresectable locoregional recurrent breast cancer in previously irradiated area: Size matters. Radiother Oncol 117:223–8.
   PubMed Web of Science ®Google Scholar
• Franckena M, De Wit R, Ansink AC, et al. (2007). Weekly systemic cisplatin plus locoregional hyperthermia: an effective treatment for patients with recurrent cervical carcinoma in a previously irradiated area. Int J Hyperthermia 23:443–50.
   PubMed Web of Science ®Google Scholar
• Heijkoop ST, van Doorn HC, Stalpers LJA, et al. (2014). Results of concurrent chemotherapy and hyperthermia in patients with recurrent cervical cancer after previous chemoradiation. Int J Hyperthermia 30:6–10.
   PubMed Web of Science ®Google Scholar
• Harnicek D, Kampmann E, Lauber K, et al. (2016). Hyperthermia adds to trabectedin effectiveness and thermal enhancement is associated with BRCA2 degradation and impairment of DNA homologous recombination repair. Int J Cancer 139:467–79.
   PubMed Web of Science ®Google Scholar
• Oei AL, Vriend LEM, van Leeuwen CM, et al. (2017). Sensitizing thermochemotherapy with a PARP1-inhibitor. Oncotarget 8:16303–12.
   PubMed Web of Science ®Google Scholar
• Oei AL, van Leeuwen CM, Ahire VR, et al. (2017). Enhancing synthetic lethality of PARP-inhibitor and cisplatin in BRCA-proficient tumour cells with hyperthermia. Oncotarget 8:28116–24.
   PubMed Web of Science ®Google Scholar
• Oei AL, Ahire VR, van Leeuwen CM, et al. (2017). Enhancing radiosensitisation of BRCA2-proficient and BRCA2-deficient cell lines with hyperthermia and PARP1-i. Int J Hyperthermia. [Epub ahead of print]. doi: 10.1080/02656736.2017.1324642
   Web of Science ®Google Scholar
• Eppink B, Krawczyk PM, Stap J, Kanaar R. (2012). Hyperthermia-induced DNA repair deficiency suggests novel therapeutic anti-cancer strategies. Int J Hyperthermia 28:509–17.
   PubMed Web of Science ®Google Scholar
• Guo Z, Pontén F, Wilander E, Pontén J. (2000). Clonality of precursors of cervical cancer and their genetical links to invasive cancer. Mod Pathol 13:606–13.
   PubMed Web of Science ®Google Scholar
• Kidd EA, Grigsby PW. (2008). Intratumoral metabolic heterogeneity of cervical cancer. Clin Cancer Res 14:5236–41.
   PubMed Web of Science ®Google Scholar
• Vaupel PW, Kelleher DK. (2012). Blood flow and associated pathophysiology of uterine cervix cancers: characterisation and relevance for localised hyperthermia. Int J Hyperthermia 28:518–27.
   PubMed Web of Science ®Google Scholar
• Vaughn JP, Cirisano FD, Huper G, et al. (1996). Cell cycle control of BRCA2. Cancer Res 56:4590–4.
   PubMed Web of Science ®Google Scholar
• Evans SS, Wang WC, Bain MD, et al. (2001). Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood 97:2727–33.
   PubMed Web of Science ®Google Scholar