It's Getting Hot in Here: Targeting Cancer Stem-like Cells with Hyperthermia

Haidong Huang, Kevin Yu, Alireza Mohammadi, Efstathios Karanthanasis, Andrew Godley, Jennifer S Yu, Haidong Huang, Kevin Yu, Alireza Mohammadi, Efstathios Karanthanasis, Andrew Godley, Jennifer S Yu

Abstract

Cancer stem-like cells (CSCs) are a subset of cancer cells that are resistant to conventional radiotherapy and chemotherapy. As such, CSCs have been recognized as playing a large role in tumor initiation and recurrence. Although hyperthermia is broadly used in cancer treatment either alone or in combination with radio- or chemo-therapy, its potential to target CSCs is not well understood. In this review, we discuss different types of hyperthermia and potential mechanisms of action in cancer treatment, particularly in regards to killing CSCs.

Keywords: Ablation; Cancer stem-like cells; Chemotherapy; Cytotoxic treatment; Hyperthermia; LITT; Nanoparticle; Radiation.

Conflict of interest statement

Conflict of Interest Authors declare no conflict of interest.

References

    1. Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annu Rev Med. 2007;58:267–84.
    1. Batlle E, Clevers H. Cancer stem cells revisited. Nat Med. 2017;23(10):1124–1134. doi: 10.1038/nm.4409.
    1. Beck B, Blanpain C. Unravelling cancer stem cell potential. Nat Rev Cancer. 2013;13(10):727–38. doi: 10.1038/nrc3597.
    1. Nassar D, Blanpain C. Cancer Stem Cells: Basic Concepts and Therapeutic Implications. Annu Rev Pathol. 2016;11:47–76. doi: 10.1146/annurev-pathol-012615-044438.
    1. Mallory M, Gogineni E, Jones GC, Greer L, Simone CB. Therapeutic hyperthermia: The old, the new, and the upcoming. Crit Rev Oncol Hematol. 2016;97:56–64. doi: 10.1016/j.critrevonc.2015.08.003.
    1. Wust P, Hildebrandt B, Sreenivasa G, Rau B, Gellermann J, Riess H, et al. Hyperthermia in combined treatment of cancer. Lancet Oncol. 2002;3(8):487–97.
    1. Van Valenberg H, Colombo R, Witjes F. Intravesical radiofrequency-induced hyperthermia combined with chemotherapy for non-muscle-invasive bladder cancer. Int J Hyperthermia. 2016;32(4):351–62. doi: 10.3109/02656736.2016.1140232.
    1. Hu Y, Li Z, Mi DH, Cao N, Zu SW, Wen ZZ, et al. Chemoradiation combined with regional hyperthermia for advanced oesophageal cancer: a systematic review and meta-analysis. J Clin Pharm Ther. 2017;42(2):155–164. doi: 10.1111/jcpt.12498.
    1. Jones EL, Oleson JR, Prosnitz LR, Samulski TV, Vujaskovic Z, Yu D, et al. Randomized trial of hyperthermia and radiation for superficial tumors. J Clin Oncol. 2005;23(13):3079–3085.
    1. Zagar TM, Higgins KA, Miles EF, Vujaskovic Z, Dewhirst MW, Clough RW, et al. Durable palliation of breast cancer chest wall recurrence with radiation therapy, hyperthermia, and chemotherapy. Radiotherapy and Oncology. 2010;97(3):535–540. doi: 10.1016/j.radonc.2010.10.020.
    1. Datta NR, Puric E, Klingbiel D, Gomez S, Bodis S. Hyperthermia and Radiation Therapy in Locoregional Recurrent Breast Cancers: A Systematic Review and Meta-analysis. Int J Radiat Oncol Biol Phys. 2016;94(5):1073–1087.
    1. Overgaard J, Gonzalez Gonzalez D, Hulshof MC, Arcangeli G, Dahl O, Mella O, et al. Hyperthermia as an adjuvant to radiation therapy of recurrent or metastatic malignant melanoma. A multicentre randomized trial by the European Society for Hyperthermic Oncology. Int J Hyperthermia. 1996;12(1):3–20.
    1. Overgaard J, Gonzalez Gonzalez D, Hulshof MC, Arcangeli G, Dahl O, Mella O, et al. Randomized Trial of Hyperthermia as Adjuvant to Radiotherapy for Recurrent or Metastatic Malignant-Melanoma. Lancet. 1995;345(8949):540–543.
    1. Eckert F, Braun LH, Traub F, Kopp HG, Sipos В, Lamprecht U, et al. Radiotherapy and hyperthermia with curative intent in recurrent high risk soft tissue sarcomas. Int J Hyperthermia. 2017:1–8. doi: 10.1080/02656736.2017.1369174.
    1. Issels RD, Lindner LH, Verweij J, Wust P, Reichardt P, Schem BC, et al. Neo-adjuvant chemotherapy alone or with regional hyperthermia for localised high-risk soft-tissue sarcoma: a randomised phase 3 multicentre study. Lancet Oncol. 2010;11(6):561–70. doi: 10.1016/S1470-2045(10)70071-1.
    1. Lutgens LC, Koper PC, Jobsen JJ, van der Steen-Banasik EM, Creutzberg CL, van den Berg HA, et al. Radiation therapy combined with hyperthermia versus cisplatin for locally advanced cervical cancer: Results of the randomized RADCHOC trial. Radiother Oncol. 2016;120(3):378–382. doi: 10.1016/j.radonc.2016.02.010.
    1. Datta NR, Rogers S, Klingbiel D, Gómez S, Puric E, Bodis S. Hyperthermia and radiotherapy with or without chemotherapy in locally advanced cervical cancer: a systematic review with conventional and network meta-analyses. International Journal of Hyperthermia. 2016;32(7):809–821. doi: 10.1080/02656736.2016.1195924.
    1. Harima Y, Ohguri T, Imada H, Sakurai H, Ohno T, Hiraki Y. A multicentre randomised clinical trial of chemoradiotherapy plus hyperthermia versus chemoradiotherapy alone in patients with locally advanced cervical cancer. Int J Hyperthermia. 2016;32(7):801–808. doi: 10.1080/02656736.2016.1213430.
    1. Diederich CJ, Wootton J, Prakash P, Salgaonkar V, Juang T, Scott S, et al. Catheter-based ultrasound hyperthermia with HDR brachytherapy for treatment of locally advanced cancer of the prostate and cervix. Proc SPIE Int Soc Opt Eng. 2011;7901:79010O.
    1. Hurwitz MD, Hansen JL, Prokopios-Davos S, Manola J, Wang Q, Bornstein BA, et al. Hyperthermia Combined With Radiation for the Treatment of Locally Advanced Prostate Cancer Long-Term Results From Dana-Farber Cancer Institute Study 94–153. Cancer. 2011;117(3):510–516. doi: 10.1002/cncr.25619.
    1. Hurwitz MD, Kaplan ID, Hansen JL, Prokopios-Davos S, Topulos GP, Wishnow K, et al. Hyperthermia combined with radiation in treatment of locally advanced prostate cancer is associated with a favourable toxicity profile. Int J Hyperthermia. 2005;21(7):649–56.
    1. Zwirner K, Bonomo P, Lamprecht U, Zips D, Gani C. External validation of a rectal cancer outcome prediction model with a cohort of patients treated with preoperative radiochemotherapy and deep regional hyperthermia. Int J Hyperthermia. 2017:1–6. doi: 10.1080/02656736.2017.1338364.
    1. Gani C, Schroeder C, Heinrich V, Spillner P, Lamprecht U, Berger B. Longterm local control and survival after preoperative radiochemotherapy in combination with deep regional hyperthermia in locally advanced rectal cancer. Int J Hyperthermia. 2016;32(2):187–92. doi: 10.3109/02656736.2015.1117661.
    1. Rasulov AO, Gordeyev SS, Barsukov YA, Tkachev SI, Malikhov AG, Balyasnikova SS, et al. Short-course preoperative radiotherapy combined with chemotherapy, delayed surgery and local hyperthermia for rectal cancer: a phase II study. Int J Hyperthermia. 2017;2:1–9. doi: 10.1080/02656736.2016.1272138.
    1. Chi MS, Yang KL, Chang YC, Ko HL, Lin YH, Huang SC. Comparing the Effectiveness of Combined External Beam Radiation and Hyperthermia Versus External Beam Radiation Alone in Treating Patients With Painful Bony Metastases: A Phase 3 Prospective, Randomized, Controlled Trial. Int J Radiat Oncol Biol Phys. 2017 doi: 10.1016/j.ijrobp.2017.09.030.
    1. Dewhirst MW, Vujaskovic Z, Jones E, Thrall D. Re-setting the biologic rationale for thermal therapy. Int J Hyperthermia. 2005;21(8):779–90.
    1. Diederich CJ. Thermal ablation and high-temperature thermal therapy: overview of technology and clinical implementation. Int J Hyperthermia. 2005;21(8):745–53.
    1. Chu KF, Dupuy DE. Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer. 2014;14(3):199–208. doi: 10.1038/nrc3672.
    1. Friedman M, Mikityansky I, Kam A, Libutti SK, Walther MM, Neeman Z, et al. Radiofrequency ablation of cancer. Cardiovasc Intervent Radiol. 2004;27(5):427–34.
    1. Curley SA. Radiofrequency ablation of malignant liver tumors. Oncologist. 2001;6(1):14–23.
    1. Brace CL. Radiofrequency and microwave ablation of the liver, lung, kidney, and bone: what are the differences? Curr Probl Diagn Radiol. 2009;38(3):135–43. doi: 10.1067/j.cpradiol.2007.10.001.
    1. Lencioni R, Crocetti L, Cioni D, Della Pina C, Bartolozzi C. Percutaneous radiofrequency ablation of hepatic colorectal metastases: technique, indications, results, and new promises. Invest Radiol. 2004;39(11):689–97.
    1. Zorbas G, Samaras T. A study of the sink effect by blood vessels in radiofrequency ablation. Comput Biol Med. 2015;57:182–6. doi: 10.1016/j.compbiomed.2014.12.014.
    1. Lubner MG, Brace CL, Hinshaw JL, Lee FT., Jr Microwave Tumor Ablation: Mechanism of Action, Clinical Results, and Devices. J Vasc Interv Radiol. 2010;21(8 Suppl):S192–203. doi: 10.1016/j.jvir.2010.04.007.
    1. Lee I, Kalkanis S, Hadjipanayis CG. Stereotactic Laser Interstitial Thermal Therapy for Recurrent High-Grade Gliomas. Neurosurgery. 2016;79(6):S24–S34.
    1. Missios S, Bekelis K, Barnett GH. Renaissance of laser interstitial thermal ablation. Neurosurg Focus. 2015;38(3):E13. doi: 10.3171/2014.12.FOCUS14762.
    1. Zhou YF. High intensity focused ultrasound in clinical tumor ablation. World J Clin Oncol. 2011;2(1):8–27. doi: 10.5306/wjco.v2.i1.8.
    1. Zhang L, Wang ZB. High-intensity focused ultrasound tumor ablation: review of ten years of clinical experience. Front Med China. 2010;4(3):294–302.
    1. Maloney E, Hwang JH. Emerging HIFU applications in cancer therapy. Int J Hyperthermia. 2015;31(3):302–9.
    1. Chatterjee DK, Diagaradjane P, Krishnan S. Nanoparticle-mediated hyperthermia in cancer therapy. Ther Deliv. 2011;02(8):1001–14.
    1. Cherukuri P, Glazer ES, Curley SA. Targeted hyperthermia using metal nanoparticles. Adv Drug Deliv Rev. 2010;62(3):339–45. doi: 10.1016/j.addr.2009.11.006.
    1. Singh R, Torti SV. Carbon nanotubes in hyperthermia therapy. Adv Drug Deliv Rev. 2013;65(15):2045–60. doi: 10.1016/j.addr.2013.08.001.
    1. Hervault A, Thanh NT. Magnetic nanoparticle-based therapeutic agents for thermo-chemotherapy treatment of cancer. Nanoscale. 2014;6(20):11553–73. doi: 10.1039/c4nr03482a.
    1. Peiris PM, Bauer L, Toy R, Tran E, Pansky J, Doolittle E, et al. Enhanced Delivery of Chemotherapy to tumors Using a Multicomponent Nanochain with Radio-Frequency-Tunable Drug Release. Acs Nano. 2012;6(5):4157–4168. doi: 10.1021/nn300652p.
    1. Toy R, Bauer L, Hoimes C, Ghaghada KB, Karathanasis E. Targeted nanotechnology for cancer imaging. Adv Drug Deliv Rev. 2014;76:79–97. doi: 10.1016/j.addr.2014.08.002.
    1. Baumann BC, Kao GD, Mahmud A, Harada T, Swift J, Chapman C, et al. Enhancing the efficacy of drug-loaded nanocarriers against brain tumors by targeted radiation therapy. Oncotarget. 2013;4(1):64–79.
    1. Maier-Hauff K, Ulrich F, Nestler D, Niehoff H, Wust P, Thiesen B, et al. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J Neurooncol. 2011;103(2):317–324. doi: 10.1007/s11060-010-0389-0.
    1. Johannsen M, Gneveckow U, Eckelt L, Feussner A, Waldöfner N, Scholz R, et al. Clinical hyperthermia of prostate cancer using magnetic nanoparticles: Presentation of a new interstitial technique. Int J Hyperthermia. 2005;21(7):637–47.
    1. Bañobre-López M, Teijeiro A, Rivasa J. Magnetic nanoparticle-based hyperthermia for cancer treatment. Rep Pract Oncol Radiother. 2013;18(6):397–400. doi: 10.1016/j.rpor.2013.09.011.
    1. Nikfarjam M, Muralidharan V, Christophi C. Mechanisms of focal heat destruction of liver tumors. J Surg Res. 2005;127(2):208–23.
    1. Fajardo LF, Egbert B, Marmor J, Hahn GM. Effects of Hyperthermia in a Malignant-Tumor. Cancer. 1980;45(3):613–623.
    1. Nishida T, Akagi K, Tanaka Y. Correlation between cell killing effect and cell membrane potential after heat treatment: Analysis using fluorescent dye and flow cytometry. International Journal of Hyperthermia. 1997;13(2):227–234.
    1. Ruifrok AC, Kanon B, Konings AW. Correlation between Cellular- Survival and Potassium-Loss in Mouse Fibroblasts after Hyperthermia Alone and after a Combined Treatment with X-Rays. Radiation Research. 1985;101(2):326–331.
    1. Vidair CA, Dewey WC. Evaluation of a role for intracellular Na+, K+, Ca2+, and Mg2+ in hyperthermic cell killing. Radiat Res. 1986;105(2):187–200.
    1. Willis WT, Jackman MR, Bizeau ME, Pagliassotti MJ, Hazel JR. Hyperthermia impairs liver mitochondrial function in vitro. Am J Physiol Regul Integr Comp Physiol. 2000;278(5):R1240–6.
    1. Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell. 2014;14(3):275–91. doi: 10.1016/j.stem.2014.02.006.
    1. Warters RL, Roti Roti JL. Hyperthermia and the cell nucleus. Radiat Res. 1982;92(3):458–62.
    1. Krawczyk PM, Eppink B, Essers J, Stap J, Rodermond H, Odijk H, et al. Mild hyperthermia inhibits homologous recombination, induces BRCA2 degradation, and sensitizes cancer cells to poly (ADP-ribose) polymerase-1 inhibition. Proc Natl Acad Sci U S A. 2011;108(24):9851–6. doi: 10.1073/pnas.1101053108.
    1. Oei AL, Vriend LEM, Crezee J, Franken NAP, Krawczyk PM. Effects of hyperthermia on DNA repair pathways: one treatment to inhibit them all. Radiat Oncol. 2015;10:165. doi: 10.1186/s13014-015-0462-0.
    1. Milleron RS, Bratton SB. Heat shock induces apoptosis independently of any known initiator caspase-activating complex. J Biol Chem. 2006;281(25):16991–7000.
    1. Morlé A, Garrido C, Micheau O. Hyperthermia restores apoptosis induced by death receptors through aggregation-induced c-FLIP cytosolic depletion. Cell Death Dis. 2015;6:e1633. doi: 10.1038/cddis.2015.12.
    1. Vertrees RA, Das GC, Coscio AM, Xie J, Zwischenberger JB, Boor PJ. A mechanism of hyperthermia-induced apoptosis in ras-transformed lung cells. Molecular Carcinogenesis. 2005;44(2):111–121.
    1. Skibba JL, Quebbeman EJ, Kalbfleisch JH. Nitrogen-Metabolism and Lipid-Peroxidation during Hyperthermic Perfusion of Human Livers with Cancer. Cancer Research. 1986;46(11):6000–6003.
    1. Wang Z, Cai F, Chen X, Luo M, Hu L, Lu Y. The Role of Mitochondria-Derived Reactive Oxygen Species in Hyperthermia-Induced Platelet Apoptosis. Plos One. 2013;8(9) doi: 10.1371/journal.pone.0075044.
    1. El-Orabi NF, Rogers CB, Edwards HG. Schwartz DD. Heat-induced inhibition of superoxide dismutase and accumulation of reactive oxygen species leads to HT-22 neuronal cell death. Journal of Thermal Biology. 2011;36(1):49–56.
    1. Dörthe M. Katschinski, Kristina Boos, Susann G. Schindler, Joachim Fandrey. Pivotal role of reactive oxygen species as intracellular mediators of hyperthermia-induced apoptosis. Journal of Biological Chemistry. 2000;275(28):21094–21098.
    1. Matés JM, Sánchez-Jiménez FM. Role of reactive oxygen species in apoptosis: implications for cancer therapy. Int J Biochem Cell Biol. 2000;32(2):157–170.
    1. Song CW. Effect of local hyperthermia on blood flow and microenvironment: a review. Cancer Res. 1984;44:4721s–4730s.
    1. Sun X, Xing L, Ling CC, Li GC. The effect of mild temperature hyperthermia on tumour hypoxia and blood perfusion: relevance for radiotherapy, vascular targeting and imaging. Int J Hyperthermia. 2010;26(3):224–31. doi: 10.3109/02656730903479855.
    1. Song CW, Park HJ, Lee CK, Griffin R. Implications of increased tumor blood flow and oxygenation caused by mild temperature hyperthermia in tumor treatment. Int J Hyperthermia. 2005;21(8):761–767.
    1. Song CW, Kang MS, Rhee JG, Levitt SH. The effect of hyperthermia on vascular function, pH, and cell survival. Radiology. 1980;137(3):795–803.
    1. Sun X, Li XF, Russell J, Xing L, Urano M, Li GC, et al. Changes in tumor hypoxia induced by mild temperature hyperthermia as assessed by dual-tracer immunohistochemistry. Radiother Oncol. 2008;88(2):269–276. doi: 10.1016/j.radonc.2008.05.015.
    1. Evans SS, Wang WC, Bain MD, Burd R, Ostberg JR, Repasky EA. Fever-range hyperthermia dynamically regulates lymphocyte delivery to high endothelial venules. Blood. 2001;97(9):2727–2733.
    1. Muthana M, Multhoff G, Pockley AG. Tumour infiltrating host cells and their significance for hyperthermia. Int J Hyperthermia. 2010;26(3):247–255. doi: 10.3109/02656730903413375.
    1. den Brok MH, Sutmuller RP, van der Voort R, Bennink EJ, Figdor CG, Ruers TJ, et al. In situ tumor ablation creates an antigen source for the generation of antitumor immunity. Cancer Research. 2004;64(11):4024–4029.
    1. Mikucki ME, Fisher DT, Ku AW, Appenheimer MM, Muhitch JB, Evans SS. Preconditioning thermal therapy: Flipping the switch on IL-6 for antitumour immunity. Int J Hyperthermia. 2013;29(5):464–473.
    1. Ali MY, Grimm CF, Ritter M, Mohr F, Allgaier HP, Weth R, et al. Activation of dendritic cells by local ablation of hepatocellular carcinoma. J Hepatol. 2005;43(5):817–22.
    1. Hausner PF. Image-guided thermal ablation of tumors increases the plasma level of interleukin-6 and interleukin-10. J Vasc Interv Radiol. 2013;24(8):1105–12. doi: 10.1016/j.jvir.2013.05.059.
    1. Milani V, Noessner E, Ghose S, Kuppner M, Ahrens B, Scharner A, et al. Heat shock protein 70: role in antigen presentation and immune stimulation. Int J Hyperthermia. 2002;18(6):563–75.
    1. Multhoff G, Hightower LE. Hightower Cell surface expression of heat shock proteins and the immune response. Cell Stress Chaperones. 1996;1(3):167–76.
    1. Frey B, Weiss EM, Rubner Y, Wunderlich R, Ott OJ, Sauer R, et al. Old and new facts about hyperthermia-induced modulations of the immune system. Int J Hyperthermia. 2012;28(6):528–42. doi: 10.3109/02656736.2012.677933.
    1. Srivastava PK, Udono H, Blachere NE, Li Z. Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics. 1994;39(2):93–8.
    1. Carper SW, Duffy JJ, Gerner EW. Heat shock proteins in thermotolerance and other cellular processes. Cancer Res. 1987;47(20):5249–55.
    1. Landry J, Chrétien P, Bernier D, Nicole LM, Marceau N, Tanguay RM. Thermotolerance and heat shock proteins induced by hyperthermia in rat liver cells. Int J Radiat Oncol Biol Phys. 1982;8(1):59–62.
    1. Fanneau D, Brunet M, Frisan E, Solary E, Fontenay M, Garrido C. Heat shock proteins: essential proteins for apoptosis regulation. J Cell Mol Med. 2008;12(3):743–761.
    1. Sreedhar AS, Csermely P. Heat shock proteins in the regulation of apoptosis: new strategies in tumor therapy: a comprehensive review. Pharmacol Ther. 2004;101(3):227–57.
    1. Beere HM. The stress of dying”: the role of heat shock proteins in the regulation of apoptosis. J Cell Sci. 2004;117:2641–51.
    1. van der Zee J. Heating the patient: a promising approach? Ann Oncol. 2002;13(8):1173–84.
    1. Sharma S, Sandhu AP, Patel FD, Ghoshal S, Gupta BD, Yadav NS. Side- Effects of Local Hyperthermia - Results of a Prospectively Randomized Clinical-Study. Int J Hyperthermia. 1990;6(2):279–285.
    1. Izukura R, Imada H, Hashiguchi N, Sawatari H, Ohguri T, Miyazono M, et al. Cardiac and respiratory effects of deep regional hyperthermia using an 8MHz radiofrequency-capacitive device on patients with cancer. International Journal of Hyperthermia. 2017;33(4):428–434. doi: 10.1080/02656736.2017.1283064.
    1. Borovski T, De Sousa E, Melo F, Vermeulen F, Medema JP. Cancer stem cell niche: the place to be. Cancer Res. 2011;71(3):634–9. doi: 10.1158/0008-5472.CAN-10-3220.
    1. Plaks V, Kong N, Werb Z. The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Cell Stem Cell. 2015;16(3):225–38. doi: 10.1016/j.stem.2015.02.015.
    1. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444(7120):756–760.
    1. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature. 2009;458(7239):780–3. doi: 10.1038/nature07733.
    1. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med. 2001;7(9):1028–34.
    1. Golebiewska A, Brons NH, Bjerkvig R, Niclou SP. Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell. 2011;8(2):136–47. doi: 10.1016/j.stem.2011.01.007.
    1. Zhao J. Cancer stem cells and chemoresistance: The smartest survives the raid. Pharmacol Ther. 2016;160:145–58. doi: 10.1016/j.pharmthera.2016.02.008.
    1. Konopleva M, Zhao S, Hu W, Jiang S, Snell V, Weidner D, et al. The anti-apoptotic genes Bcl-X(L) and Bcl-2 are over-expressed and contribute to chemoresistance of non-proliferating leukaemic CD34+ cells. Br J Haematol. 2002;118(2):521–34.
    1. Wang J, Wakeman TP, Fathia JD, Hjelmeland AB, Wang XF, White RR, et al. Notch promotes radioresistance of glioma stem cells. Stem Cells. 2010;28(1):17–28. doi: 10.1002/stem.261.
    1. Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen F, Iovino F, et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell. 2007;1(4):389–402. doi: 10.1016/j.stem.2007.08.001.
    1. Zhao C, Blum J, Chen A, Kwon HY, Jung SH, Cook JM, et al. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell. 2007;12(6):528–41.
    1. Chen J, Li Y, Yu T, McKay RM, Burns DK, Kernie SG, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 2012;488(7412):522–6. doi: 10.1038/nature11287.
    1. Saito Y, Uchida N, Tanaka S, Suzuki N, Tomizawa-Murasawa M, Sone A, et al. Induction of cell cycle entry eliminates human leukemia stem cells in a mouse model of AML. Nat Biotechnol. 2010;28(3):275–80. doi: 10.1038/nbt.1607.
    1. Liu L, Wise DR, Diehl JA, Simon MC. Hypoxic reactive oxygen species regulate the integrated stress response and cell survival. J Biol Chem. 2008;283(45):31153–62. doi: 10.1074/jbc.M805056200.
    1. Harrison H, Rogerson L, Gregson HJ, Brennan KR, Clarke RB, Landberg G. Contrasting hypoxic effects on breast cancer stem cell hierarchy is dependent on ER-alpha status. Cancer Res. 2013;73(4):1420–33. doi: 10.1158/0008-5472.CAN-12-2505.
    1. Malanchi I, Santamaria-Martínez A, Susanto E, Peng H, Lehr HA, Delaloye JF, et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2011;481(7379):85–9. doi: 10.1038/nature10694.
    1. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton F, Chan E, et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature. 2012;487(7408):505–9. doi: 10.1038/nature11249.
    1. Wierenga PK, Setroikromo R, Kamps G, Kampinga HH, Vellenga E. Differences in heat sensitivity between normal and acute myeloid leukemic stem cells: Feasibility of hyperthermic purging of leukemic cells from autologous stem cell grafts. Experimental Hematology. 2003;31(5):421–427.
    1. Burke AR, Singh RN, Carroll DL, Wood JC, DAgostino RB, Jr, Ajayan PM, et al. The resistance of breast cancer stem cells to conventional hyperthermia and their sensitivity to nanoparticle-mediated photothermal therapy. Biomaterials. 2012;33(10):2961–70. doi: 10.1016/j.biomaterials.2011.12.052.
    1. Sadhukha T, Niu L, Wiedmann TS, Panyam J. Effective elimination of cancer stem cells by magnetic hyperthermia. Mol Pharm. 2013;10(4):1432–41.
    1. Atkinson RL, Zhang M, Diagaradjane P, Sirisha P, Contreras A, Hilsenbeck SG, et al. Thermal enhancement with optically activated gold nanoshells sensitizes breast cancer stem cells to radiation therapy. Sci Transl Med. 2010;2(55):55ra79. doi: 10.1126/scitranslmed.3001447.
    1. Man J, Shoemake JD, Ma T, Rizzo AE, Godley AR, Wu Q, et al. Hyperthermia Sensitizes Glioma Stem-like Cells to Radiation by Inhibiting AKT Signaling. Cancer Res. 2015;75(8):1760–9. doi: 10.1158/0008-5472.CAN-14-3621.
    1. Lee H, Park HJ, Park CS, Oh ET, Choi BH, Williams B, et al. Response of breast cancer cells and cancer stem cells to metformin and hyperthermia alone or combined. PLoS One. 2014;9(2):e87979. doi: 10.1371/journal.pone.0087979.
    1. Wang CH, Chiou SH, Chou CP, Chen YC, Huang YJ, Peng CA. Photothermolysis of glioblastoma stem-like cells targeted by carbon nanotubes conjugated with CD133 monoclonal antibody. Nanomedicine. 2011;7(1):69–79. doi: 10.1016/j.nano.2010.06.010.

Source: PubMed

3
Iratkozz fel