Skip to main content

Advertisement

SpringerLink
Log in

New physical approaches to treat cancer stem cells: a review

  • Review Article
  • Published:
Clinical and Translational Oncology Aims and scope Submit manuscript

Abstract

Cancer stem cells (CSCs) have been identified as the main center of tumor therapeutic resistance. They are highly resistant against current cancer therapy approaches particularly radiation therapy (RT). Recently, a wide spectrum of physical methods has been proposed to treat CSCs, including high energetic particles, hyperthermia (HT), nanoparticles (NPs) and combination of these approaches. In this review article, the importance and benefits of the physical CSCs therapy methods such as nanomaterial-based heat treatments and particle therapy will be highlighted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Abdollahi H, Shiri I, Atashzar M, Sarebani M, Moloudi K, Samadian H. Radiation protection and secondary cancer prevention using biological radioprotectors in radiotherapy. Int J Cancer Ther Oncol. 2015;3(33):335. https://doi.org/10.14319/ijcto.33.5

    Article  Google Scholar 

  2. Khademi S, Abdollahi H. Application of hydrogen producing microorganisms in radiotherapy: an idea. Iran J Pub Helath. 2014;43:1018–9.

    Google Scholar 

  3. Newhauser WD, Berrington de Gonzalez A, Schulte R, Lee CA. Review of radiotherapy-induced late effects research after advanced technology treatments. Front Oncol. 2016;6:13.

    PubMed  PubMed Central  Google Scholar 

  4. Kouhsari E, Ghadimi-Daresajini A, Abdollahi H, Amirmozafari N, Mahdavi SR, Abbasian S, et al. The potential roles of bacteria to improve radiation treatment outcome. Clin Transl Oncol. 2018;20:127–39.

    CAS  PubMed  Google Scholar 

  5. Dou J, Gu N. Biomarkers of cancer stem cells. Adv Cancer Stem Cell Biol: Springer; 2012. p. 45–67.

    Google Scholar 

  6. D’Andrea V, Panarese A, Tonda M, Biffoni M, Monti M. Cancer stem cells as functional biomarkers. Cancer Biomark. 2017;20:231–4.

    PubMed  Google Scholar 

  7. Klonisch T, Wiechec E, Hombach-Klonisch S, Ande SR, Wesselborg S, Schulze-Osthoff K, et al. Cancer stem cell markers in common cancers–therapeutic implications. Trends Mol Med. 2008;14:450–60.

    CAS  PubMed  Google Scholar 

  8. Huang H, Yu K, Mohammadi A, Karanthanasis E, Godley A, Yu JS. It’s getting hot in here: targeting cancer stem-like cells with hyperthermia. J Stem Trans Bio. 2017;2:113.

    Google Scholar 

  9. Oei AL, Vriend LE, Krawczyk PM, Horsman MR, Franken NA, Crezee J. Targeting therapy-resistant cancer stem cells by hyperthermia. Int J Hyperthermia. 2017;2:1–12. https://doi.org/10.1080/02656736.2017.1279757

    Article  CAS  Google Scholar 

  10. Krause M, Dubrovska A, Linge A, Baumann M. Cancer stem cells: radioresistance, prediction of radiotherapy outcome and specific targets for combined treatments. Adv Drug Deliv Rev. 2017;109:63–73.

    CAS  PubMed  Google Scholar 

  11. Pajonk F, Vlashi E, McBride WH. Radiation resistance of cancer stem cells: the 4 R’s of radiobiology revisited. Stem Cells (Dayton, Ohio). 2010;28:639–48.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Barcellos-Hoff MH, Park C, Wright EG. Radiation and the microenvironment—tumorigenesis and therapy. Nat Rev Cancer. 2005;5:867–75.

    CAS  PubMed  Google Scholar 

  13. 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;458:780–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Kim JJ, Tannock IF. Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer. 2005;5:516–25.

    CAS  PubMed  Google Scholar 

  15. Mitin T, Zietman AL. Promise and pitfalls of heavy-particle therapy. J Clin Oncol. 2014;32:2855–63.

    PubMed  PubMed Central  Google Scholar 

  16. Durante M, Loeffler JS. Charged particles in radiation oncology. Nat Rev Clin Oncol. 2010;7:37–43.

    PubMed  Google Scholar 

  17. Loeffler JS, Durante M. Charged particle therapy–optimization, challenges and future directions. Nat Rev Clin Oncol. 2013;10:411–24.

    PubMed  Google Scholar 

  18. Mendenhall NP, Malyapa RS, Su Z, Yeung D, Mendenhall WM, Li Z. Proton therapy for head and neck cancer: rationale, potential indications, practical considerations, and current clinical evidence. Acta Oncol. 2011;50:763–71.

    PubMed  Google Scholar 

  19. Schardt D, Elsässer T, Schulz-Ertner D. Heavy-ion tumor therapy: physical and radiobiological benefits. Rev Mod Phys. 2010;82:383–425.

    Google Scholar 

  20. Tobias CA, Lyman JT, Chatterjee A, Howard J, Maccabee HD, Raju MR, et al. Radiological physics characteristics of the extracted heavy ion beams of the bevatron. Science. 1971;174:1131–4.

    CAS  PubMed  Google Scholar 

  21. Suit H, DeLaney T, Goldberg S, Paganetti H, Clasie B, Gerweck L, et al. Proton vs carbon ion beams in the definitive radiation treatment of cancer patients. Radiother Oncol. 2010;95:3–22.

    CAS  PubMed  Google Scholar 

  22. Okayasu R. Repair of DNA damage induced by accelerated heavy ions–a mini review. Int J Cancer. 2012;130:991–1000.

    CAS  PubMed  Google Scholar 

  23. Blakely EA, Chang PY. Biology of charged particles. Cancer J. 2009;15:271–84.

    CAS  PubMed  Google Scholar 

  24. Durante M. New challenges in high-energy particle radiobiology. Br J Radiol. 2014;87:20130626.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Held KD, Kawamura H, Kaminuma T, Paz AE, Yoshida Y, Liu Q, et al. Effects of charged particles on human tumor cells. Front Oncol. 2016;6:23.

    PubMed  PubMed Central  Google Scholar 

  26. Liu H, Chang JY. Proton therapy in clinical practice. Chin J Cancer. 2011;30:315–26.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Tobias CA, Blakely EA, Alpen EL, Castro JR, Ainsworth EJ, Curtis SB, et al. Molecular and cellular radiobiology of heavy ions. Int J Radiat Oncol Biol Phys. 1982;8:2109–20.

    CAS  PubMed  Google Scholar 

  28. Tommasino F, Durante M. Proton radiobiology. Cancers (Basel). 2015;7:353–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Quan Y, Wang W, Fu Q, Mei T, Wu J, Li J, et al. Accumulation efficiency of cancer stem-like cells post γ-ray and proton irradiation. Nucl Instrum Methods Phys Res, Sect B. 2012;286:341–5.

    CAS  Google Scholar 

  30. Fu Q, Quan Y, Wang W, Mei T, Wu J, Li J, et al. Response of cancer stem-like cells and non-stem cancer cells to proton and γ-ray irradiation. Nucl Instrum Methods Phys Res Sect B. 2012;286:346–50.

    CAS  Google Scholar 

  31. Narang H, Kumar A, Bhat N, Pandey BN, Ghosh A. Effect of proton and gamma irradiation on human lung carcinoma cells: gene expression, cell cycle, cell death, epithelial-mesenchymal transition and cancer-stem cell trait as biological end points. Mutat Res. 2015;780:35–46.

    CAS  PubMed  Google Scholar 

  32. Alan Mitteer R, Wang Y, Shah J, Gordon S, Fager M, Butter PP, et al. Proton beam radiation induces DNA damage and cell apoptosis in glioma stem cells through reactive oxygen species. Sci Rep. 2015;5:13961.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhang X, Lin SH, Fang B, Gillin M, Mohan R, Chang JY. Therapy-resistant cancer stem cells have differing sensitivity to photon versus proton beam radiation. J Thorac Oncol. 2013;8:1484–91.

    CAS  PubMed  Google Scholar 

  34. Takahashi M, Hirakawa H, Yajima H, Izumi-Nakajima N, Okayasu R, Fujimori A. Carbon ion beam is more effective to induce cell death in sphere-type A172 human glioblastoma cells compared with X-rays. Int J Radiat Biol. 2014;90:1125–32.

    CAS  PubMed  Google Scholar 

  35. Ettl T, Viale-Bouroncle S, Hautmann MG, Gosau M, Kolbl O, Reichert TE, et al. AKT and MET signalling mediates antiapoptotic radioresistance in head neck cancer cell lines. Oral Oncol. 2015;51:158–63.

    CAS  PubMed  Google Scholar 

  36. Nakagawa Y, Takahashi A, Kajihara A, Yamakawa N, Imai Y, Ota I, et al. Depression of p53-independent Akt survival signals in human oral cancer cells bearing mutated p53 gene after exposure to high-LET radiation. Biochem Biophys Res Commun. 2012;423:654–60.

    CAS  PubMed  Google Scholar 

  37. Jin X, Li F, Zheng X, Liu Y, Hirayama R, Liu X, et al. Carbon ions induce autophagy effectively through stimulating the unfolded protein response and subsequent inhibiting Akt phosphorylation in tumor cells. Sci Rep. 2015;5:13815.

    PubMed  PubMed Central  Google Scholar 

  38. Takahashi A, Ma H, Nakagawa A, Yoshida Y, Kanai T, Ohno T, et al. Carbon-ion beams efficiently induce cell killing in x-ray resistant human squamous tongue cancer cells. Int J Med Phys Clin Eng Radiat Oncol. 2014;03:133–42.

    Google Scholar 

  39. Park SJ, Heo K, Choi C, Yang K, Adachi A, Okada H, et al. Carbon ion irradiation abrogates Lin28B-induced X-ray resistance in melanoma cells. J Radiat Res. 2017;58(6):765–71. https://doi.org/10.1093/jrr/rrx022

    Article  PubMed  PubMed Central  Google Scholar 

  40. Cui X, Oonishi K, Tsujii H, Yasuda T, Matsumoto Y, Furusawa Y, et al. Effects of carbon ion beam on putative colon cancer stem cells and its comparison with X-rays. Cancer Res. 2011;71:3676–87.

    CAS  PubMed  Google Scholar 

  41. Oonishi K, Cui X, Hirakawa H, Fujimori A, Kamijo T, Yamada S, et al. Different effects of carbon ion beams and X-rays on clonogenic survival and DNA repair in human pancreatic cancer stem-like cells. Radiother Oncol. 2012;105:258–65.

    CAS  PubMed  Google Scholar 

  42. Sun F, Zhang X, Zhou X, Hua J, Zhang Y, Wang B, et al. Comparisons between bio-radiation effects of X-rays and carbon-ion irradiation on glioma stem cells. Int J Clin Exp Med. 2017;10:4639–48.

    CAS  Google Scholar 

  43. Chiblak S, Tang Z, Campos B, Gal Z, Unterberg A, Debus J, et al. Radiosensitivity of Patient-Derived Glioma Stem Cell 3-Dimensional Cultures to Photon, Proton, and Carbon Irradiation. Int J Radiat Oncol Biol Phys. 2016;95:112–9.

    PubMed  Google Scholar 

  44. Moncharmont C, Guy JB, Wozny AS, Gilormini M, Battiston-Montagne P, Ardail D, et al. Carbon ion irradiation withstands cancer stem cells’ migration/invasion process in head and neck squamous cell carcinoma (HNSCC). Oncotarget. 2016;7:47738–49.

    PubMed  PubMed Central  Google Scholar 

  45. Bertrand G, Maalouf M, Boivin A, Battiston-Montagne P, Beuve M, Levy A, et al. Targeting head and neck cancer stem cells to overcome resistance to photon and carbon ion radiation. Stem Cell Rev. 2014;10:114–26.

    CAS  PubMed  Google Scholar 

  46. Sai S, Wakai T, Vares G, Yamada S, Kamijo T, Kamada T, et al. Combination of carbon ion beam and gemcitabine causes irreparable DNA damage and death of radioresistant pancreatic cancer stem-like cells in vitro and in vivo. Oncotarget. 2015;6:5517–35.

    PubMed  PubMed Central  Google Scholar 

  47. Sai S, Vares G, Kim EH, Karasawa K, Wang B, Nenoi M, et al. Carbon ion beam combined with cisplatin effectively disrupts triple negative breast cancer stem-like cells in vitro. Mol Cancer. 2015;14:166.

    PubMed  PubMed Central  Google Scholar 

  48. Gabel D, Foster S, Fairchild RG. The Monte Carlo simulation of the biological effect of the 10B(n, alpha)7Li reaction in cells and tissue and its implication for boron neutron capture therapy. Radiat Res. 1987;111:14–25.

    CAS  PubMed  Google Scholar 

  49. Barth RF, Coderre JA, Vicente MG, Blue TE. Boron neutron capture therapy of cancer: current status and future prospects. Clin Cancer Res. 2005;11:3987–4002.

    CAS  PubMed  Google Scholar 

  50. Yura Y, Fujita Y. Boron neutron capture therapy as a novel modality of radiotherapy for oral cancer: principle and antitumor effect. Oral Sci Int. 2013;10:9–14.

    Google Scholar 

  51. Utsumi H, Ichihashi M, Kobayashi T, Elkind MM. Sublethal and potentially lethal damage repair on thermal neutron capture therapy. Pigment Cell Res. 1989;2:337–42.

    CAS  PubMed  Google Scholar 

  52. Coderre JA, Morris GM. The radiation biology of boron neutron capture therapy. Radiat Res. 1999;151:1–18.

    CAS  PubMed  Google Scholar 

  53. Sun T, Zhang Z, Li B, Chen G, Xie X, Wei Y, et al. Boron neutron capture therapy induces cell cycle arrest and cell apoptosis of glioma stem/progenitor cells in vitro. Radiat Oncol. 2013;8:195.

    PubMed  PubMed Central  Google Scholar 

  54. Sun T, Li Y, Huang Y, Zhang Z, Yang W, Du Z, et al. Targeting glioma stem cells enhances anti-tumor effect of boron neutron capture therapy. Oncotarget. 2016;7:43095–108.

    PubMed  PubMed Central  Google Scholar 

  55. Hirota Y, Masunaga S, Kondo N, Kawabata S, Hirakawa H, Yajima H, et al. High linear-energy-transfer radiation can overcome radioresistance of glioma stem-like cells to low linear-energy-transfer radiation. J Radiat Res. 2014;55:75–83.

    CAS  PubMed  Google Scholar 

  56. Cui FB, Liu Q, Li RT, Shen J, Wu PY, Yu LX, et al. Enhancement of radiotherapy efficacy by miR-200c-loaded gelatinase-stimuli PEG-Pep-PCL nanoparticles in gastric cancer cells. Int J Nanomed. 2014;9:2345–58.

    Google Scholar 

  57. Miladi I, Aloy MT, Armandy E, Mowat P, Kryza D, Magne N, et al. Combining ultrasmall gadolinium-based nanoparticles with photon irradiation overcomes radioresistance of head and neck squamous cell carcinoma. Nanomedicine. 2015;11:247–57.

    CAS  PubMed  Google Scholar 

  58. Hu C, Niestroj M, Yuan D, Chang S, Chen J. Treating cancer stem cells and cancer metastasis using glucose-coated gold nanoparticles. Int J Nanomed. 2015;10:2065–77.

    CAS  Google Scholar 

  59. Castro Nava A, Cojoc M, Peitzsch C, Cirillo G, Kurth I, Fuessel S, et al. Development of novel radiochemotherapy approaches targeting prostate tumor progenitor cells using nanohybrids. Int J Cancer. 2015;137:2492–503.

    CAS  PubMed  Google Scholar 

  60. You J, Zhao J, Wen X, Wu C, Huang Q, Guan F, et al. Chemoradiation therapy using cyclopamine-loaded liquid-lipid nanoparticles and lutetium-177-labeled core-crosslinked polymeric micelles. J Control Releas. 2015;202:40–8.

    CAS  Google Scholar 

  61. Kawashima H. Radioimmunotherapy: a specific treatment protocol for cancer by cytotoxic radioisotopes conjugated to antibodies. SciWorldJ. 2014;2014:492061.

    Google Scholar 

  62. Pohlman B, Sweetenham J, Macklis RM. Review of clinical radioimmunotherapy. Expert Rev Anticancer Ther. 2006;6:445–61.

    CAS  PubMed  Google Scholar 

  63. Aghevlian S, Boyle AJ, Reilly RM. Radioimmunotherapy of cancer with high linear energy transfer (LET) radiation delivered by radionuclides emitting alpha-particles or Auger electrons. Adv Drug Deliv Rev. 2017;109:102–18.

    CAS  PubMed  Google Scholar 

  64. Jandl T, Revskaya E, Jiang Z, Harris M, Dorokhova O, Tsukrov D, et al. Melanoma stem cells in experimental melanoma are killed by radioimmunotherapy. Nucl Med Biol. 2013;40:177–81.

    CAS  PubMed  Google Scholar 

  65. Al-Ejeh F, Shi W, Miranda M, Simpson PT, Vargas AC, Song S, et al. Treatment of triple-negative breast cancer using anti-EGFR-directed radioimmunotherapy combined with radiosensitizing chemotherapy and PARP inhibitor. J Nucl Med. 2013;54:913–21.

    CAS  PubMed  Google Scholar 

  66. Leyton JV, Gao C, Williams B, Keating A, Minden M, Reilly RM. A radiolabeled antibody targeting CD123(+) leukemia stem cells—initial radioimmunotherapy studies in NOD/SCID mice engrafted with primary human AML. Leuk Res Rep. 2015;4:55–9.

    PubMed  PubMed Central  Google Scholar 

  67. Weng D, Jin X, Qin S, Lan X, Chen C, Sun X, et al. Radioimmunotherapy for CD133(+) colonic cancer stem cells inhibits tumor development in nude mice. Oncotarget. 2017;8:44004–14.

    PubMed  PubMed Central  Google Scholar 

  68. Ceder J, Elgqvist J. Targeting prostate cancer stem cells with alpha-particle therapy. Front Oncol. 2016;6:273.

    PubMed  Google Scholar 

  69. Sgouros G. Alpha-particles for targeted therapy. Adv Drug Deliv Rev. 2008;60:1402–6.

    CAS  PubMed  Google Scholar 

  70. Lassmann M, Nosske D, Reiners C. Therapy of ankylosing spondylitis with 224Ra-radium chloride: dosimetry and risk considerations. Radiat Environ Biophys. 2002;41:173–8.

    PubMed  Google Scholar 

  71. Mulford DA, Scheinberg DA, Jurcic JG. The promise of targeted α-particle therapy. J Nucl Med. 2005;46:199S–204S.

    PubMed  Google Scholar 

  72. Elgqvist J, Frost S, Pouget JP, Albertsson P. The potential and hurdles of targeted alpha therapy—clinical trials and beyond. Front Oncol. 2014;3:324.

    PubMed  PubMed Central  Google Scholar 

  73. Sgouros G, Song H. Cancer stem cell targeting using the alpha-particle emitter, 213Bi: mathematical modeling and feasibility analysis. Cancer Biother Radiopharm. 2008;23:74–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Dekempeneer Y, Keyaerts M, Krasniqi A, Puttemans J, Muyldermans S, Lahoutte T, et al. Targeted alpha therapy using short-lived alpha-particles and the promise of nanobodies as targeting vehicle. Expert Opin Biol Ther. 2016;16:1035–47.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Hegyi G, Szigeti GP, Szasz A. Hyperthermia versus oncothermia: cellular effects in complementary cancer therapy. Evid Based Complement Alternat Med. 2013;2013:672873.

    PubMed  PubMed Central  Google Scholar 

  76. Tran N, Webster TJ. Magnetic nanoparticles: biomedical applications and challenges. J Mater Chem. 2010;20:8760.

    CAS  Google Scholar 

  77. Cheung AY, Neyzari A. Deep local hyperthermia for cancer therapy: external electromagnetic and ultrasound techniques. Cancer Res. 1984;44:4736s–44s.

    CAS  PubMed  Google Scholar 

  78. Shetake NG, Kumar A, Gaikwad S, Ray P, Desai S, Ningthoujam RS, et al. Magnetic nanoparticle-mediated hyperthermia therapy induces tumour growth inhibition by apoptosis and Hsp90/AKT modulation. Int J Hyperthermia. 2015;31:909–19.

    CAS  PubMed  Google Scholar 

  79. Chatterjee DK, Diagaradjane P, Krishnan S. Nanoparticle-mediated hyperthermia in cancer therapy. Ther Deliv. 2011;2:1001–14.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Beik J, Abed Z, Ghoreishi FS, Hosseini-Nami S, Mehrzadi S, Shakeri-Zadeh A, et al. Nanotechnology in hyperthermia cancer therapy: from fundamental principles to advanced applications. J Control Release. 2016;235:205–21.

    CAS  PubMed  Google Scholar 

  81. Van Oorschot B, Granata G, Di Franco S, Ten Cate R, Rodermond HM, Todaro M, et al. Targeting DNA double strand break repair with hyperthermia and DNA-PKcs inhibition to enhance the effect of radiation treatment. Oncotarget. 2016;7:65504–13.

    PubMed  PubMed Central  Google Scholar 

  82. 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;75:1760–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Gorman AM, Heavey B, Creagh E, Cotter TG, Samali A. Antioxidant-mediated inhibition of the heat shock response leads to apoptosis. FEBS Lett. 1999;445:98–102.

    CAS  PubMed  Google Scholar 

  84. Takasu T, Lyons JC, Park HJ, Song CW. Apoptosis and perturbation of cell cycle progression in an acidic environment after hyperthermia. Cancer Res. 1998;58:2504–8.

    CAS  PubMed  Google Scholar 

  85. Slimen BI, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M. Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int J Hyperthermia. 2014;30:513–23.

  86. 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:e75044.

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Saldivar-Ramirez MM, Sanchez-Torres CG, Cortes-Hernandez DA, Escobedo-Bocardo JC, Almanza-Robles JM, Larson A, et al. Study on the efficiency of nanosized magnetite and mixed ferrites in magnetic hyperthermia. J Mater Sci Mater Med. 2014;25:2229–36.

    CAS  PubMed  Google Scholar 

  88. Shetake NG, Balla MM, Kumar A. PANDEY BN. Magnetic hyperthermia therapy: an emerging modality of cancer treatment in combination with radiotherapy. J Radiat Cancer Res. 2016;7:13–7.

    Google Scholar 

  89. Pankhurst QA, Connolly J, Jones SK, Dobson J. Applications of magnetic nanoparticles in biomedicine. J Phys D Appl Phys. 2003;36:R167–81.

    CAS  Google Scholar 

  90. Kelland LR. Targeting established tumor vasculature: a novel approach to cancer treatment. Curr Cancer Ther Rev. 2005;1:1–9.

    Google Scholar 

  91. Wu W, Wu Z, Yu T, Jiang C, Kim WS. Recent progress on magnetic iron oxide nanoparticles: synthesis, surface functional strategies and biomedical applications. Sci Technol Adv Mater. 2015;16:023501.

    PubMed  PubMed Central  Google Scholar 

  92. Salunkhe AB, Khot VM, Pawar SH. Magnetic hyperthermia with magnetic nanoparticles: a status review. Curr Top Med Chem. 2014;14:572–94.

    CAS  PubMed  Google Scholar 

  93. Kim JE, Shin JY, Cho MH. Magnetic nanoparticles: an update of application for drug delivery and possible toxic effects. Arch Toxicol. 2012;86:685–700.

    CAS  PubMed  Google Scholar 

  94. Shubayev VI, Pisanic TR 2nd, Jin S. Magnetic nanoparticles for theragnostics. Adv Drug Deliv Rev. 2009;61:467–77.

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Sharifi S, Behzadi S, Laurent S, Forrest ML, Stroeve P, Mahmoudi M. Toxicity of nanomaterials. Chem Soc Rev. 2012;41:2323–43.

    CAS  PubMed  Google Scholar 

  96. Liu G, Gao J, Ai H, Chen X. Applications and potential toxicity of magnetic iron oxide nanoparticles. Small. 2013;9:1533–45.

    CAS  PubMed  Google Scholar 

  97. Li L, Jiang L-L, Zeng Y, Liu G. Toxicity of superparamagnetic iron oxide nanoparticles: research strategies and implications for nanomedicine. Chin Phys B. 2013;22:127503.

    Google Scholar 

  98. Sadhukha T, Niu L, Wiedmann TS, Panyam J. Effective elimination of cancer stem cells by magnetic hyperthermia. Mol Pharm. 2013;10:1432–41.

    CAS  PubMed  Google Scholar 

  99. Kwon Y-S, Sim K, Seo T, Lee J-K, Kwon Y, Yoon T-J. Optimization of magnetic hyperthermia effect for breast cancer stem cell therapy. RSC Adv. 2016;6:107298–304.

    CAS  Google Scholar 

  100. Chen F, Cai W. Nanomedicine for targeted photothermal cancer therapy: where are we now? Nanomedicine (Lond). 2015;10:1–3.

    PubMed  PubMed Central  Google Scholar 

  101. Melamed JR, Edelstein RS, Day ES. Elucidating the fundamental mechanisms of cell death triggered by photothermal therapy. ACS Nano. 2015;9:6–11.

    CAS  PubMed  Google Scholar 

  102. Kennedy LC, Bickford LR, Lewinski NA, Coughlin AJ, Hu Y, Day ES, et al. A new era for cancer treatment: gold-nanoparticle-mediated thermal therapies. Small. 2011;7:169–83.

    CAS  PubMed  Google Scholar 

  103. Huang X, El-Sayed MA. Plasmonic photo-thermal therapy (PPTT). Alex J Med. 2011;47:1–9.

    CAS  Google Scholar 

  104. Li J, Hu Y, Yang J, Wei P, Sun W, Shen M, et al. Hyaluronic acid-modified Fe3O4@Au core/shell nanostars for multimodal imaging and photothermal therapy of tumors. Biomaterials. 2015;38:10–21.

    CAS  PubMed  Google Scholar 

  105. Melancon MP, Zhou M, Li C. Cancer theranostics with near-infrared light-activatable multimodal nanoparticles. Acc Chem Res. 2011;44:947–56.

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Mirrahimi M, Hosseini V, Kamrava SK, Attaran N, Beik J, Kooranifar S, et al. Selective heat generation in cancer cells using a combination of 808 nm laser irradiation and the folate-conjugated Fe2O3 Au nanocomplex. Artif Cells Nanomed Biotechnol; 2018. https://doi.org/10.1080/21691401.2017.1420072

    Article  PubMed  Google Scholar 

  107. Hessel CM, Pattani VP, Rasch M, Panthani MG, Koo B, Tunnell JW, et al. Copper selenide nanocrystals for photothermal therapy. Nano Lett. 2011;11:2560–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Zhou M, Zhao J, Tian M, Song S, Zhang R, Gupta S, et al. Radio-photothermal therapy mediated by a single compartment nanoplatform depletes tumor initiating cells and reduces lung metastasis in the orthotopic 4T1 breast tumor model. Nanoscale. 2015;7:19438–47.

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Yang K, Feng L, Shi X, Liu Z. Nano-graphene in biomedicine: theranostic applications. Chem Soc Rev. 2013;42:530–47.

    CAS  PubMed  Google Scholar 

  110. Liang C, Diao S, Wang C, Gong H, Liu T, Hong G, et al. Tumor metastasis inhibition by imaging-guided photothermal therapy with single-walled carbon nanotubes. Adv Mater. 2014;26:5646–52.

    CAS  PubMed  Google Scholar 

  111. 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;7:69–79.

    CAS  PubMed  Google Scholar 

  112. Burke AR, Singh RN, Carroll DL, Wood JC, D’Agostino 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;33:2961–70.

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Chen Z, Ma L, Liu Y, Chen C. Applications of functionalized fullerenes in tumor theranostics. Theranostics. 2012;2:238–50.

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Beik J, Khademi S, Attaran N, Sarkar S, Shakeri-Zadeh A, Ghaznavi H, et al. A nanotechnology-based strategy to increase the efficiency of cancer diagnosis and therapy: folate-conjugated gold nanoparticles. Curr Med Chem. 2017;24:4399–416.

    CAS  PubMed  Google Scholar 

  115. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Releas. 2000;65:271–84.

    CAS  Google Scholar 

  116. Liao HW, Hafner JH. Gold nanorod bioconjugates. Chem Mater. 2005;17:4636–41.

    CAS  Google Scholar 

  117. Riley RS, Day ES. Gold nanoparticle-mediated photothermal therapy: applications and opportunities for multimodal cancer treatment. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2017. https://doi.org/10.1002/wnan.1449

    Article  PubMed  PubMed Central  Google Scholar 

  118. Pattani VP, Shah J, Atalis A, Sharma A, Tunnell JW. Role of apoptosis and necrosis in cell death induced by nanoparticle-mediated photothermal therapy. J Nanopart Res. 2015;17(1):20–31.

    Google Scholar 

  119. Huang X, Kang B, Qian W, Mackey MA, Chen PC, Oyelere AK, et al. Comparative study of photothermolysis of cancer cells with nuclear-targeted or cytoplasm-targeted gold nanospheres: continuous wave or pulsed lasers. J Biomed Opt. 2010;15:058002.

    PubMed  Google Scholar 

  120. Brun E, Sanche L, Sicard-Roselli C. Parameters governing gold nanoparticle X-ray radiosensitization of DNA in solution. Colloids Surf B. 2009;72:128–34.

    CAS  Google Scholar 

  121. Atkinson RL, Zhang M, Diagaradjane P, Peddibhotla S, 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;2:55ra79.

    PubMed  PubMed Central  Google Scholar 

  122. Xu Y, Wang J, Li X, Liu Y, Dai L, Wu X, et al. Selective inhibition of breast cancer stem cells by gold nanorods mediated plasmonic hyperthermia. Biomaterials. 2014;35:4667–77.

    CAS  PubMed  Google Scholar 

  123. Li W, Tan G, Cheng J, Zhao L, Wang Z, Jin Y. A novel photosensitizer 3(1),13(1)-phenylhydrazine -Mppa (BPHM) and its in vitro photodynamic therapy against HeLa cells. Molecules. 2016. https://doi.org/10.3390/molecules21050558

    Article  PubMed  PubMed Central  Google Scholar 

  124. Konan YN, Gurny R, Allémann E. State of the art in the delivery of photosensitizers for photodynamic therapy. J Photochem Photobiol B. 2002;66:89–106.

    CAS  PubMed  Google Scholar 

  125. Foote CS. Definition of type I and type II photosensitized oxidation. Photochem Photobiol. 1991;54:659.

    CAS  PubMed  Google Scholar 

  126. Usacheva M, Swaminathan SK, Kirtane AR, Panyam J. Enhanced photodynamic therapy and effective elimination of cancer stem cells using surfactant-polymer nanoparticles. Mol Pharm. 2014;11:3186–95.

    CAS  PubMed  Google Scholar 

  127. Galanzha EI, Kim JW, Zharov VP. Nanotechnology-based molecular photoacoustic and photothermal flow cytometry platform for in vivo detection and killing of circulating cancer stem cells. J Biophotonics. 2009;2:725–35.

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Lee E, Hong Y, Choi J, Haam S, Suh JS, Huh YM, et al. Highly selective CD44-specific gold nanorods for photothermal ablation of tumorigenic subpopulations generated in MCF7 mammospheres. Nanotechnology. 2012;23:465101.

    PubMed  Google Scholar 

  129. Wang J, Sefah K, Altman MB, Chen T, You M, Zhao Z, et al. Aptamer-conjugated nanorods for targeted photothermal therapy of prostate cancer stem cells. Chem Asian J. 2013;8:2417–22.

    CAS  PubMed  Google Scholar 

  130. Peng CA, Wang CH. Cancer stem-like cells photothermolysed by gold nanorod-mediated near-infrared laser irradiation. Int J Nanotechnol. 2014;11:1157–65.

    CAS  Google Scholar 

  131. Sun T, Wang Y, Wang Y, Xu J, Zhao X, Vangveravong S, et al. Using SV119-gold nanocage conjugates to eradicate cancer stem cells through a combination of photothermal and chemo therapies. Adv Healthc Mater. 2014;3:1283–91.

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Thapa R, Galoforo S, Kandel SM, El-dakdouki MH, Wilson TG, Huang X, et al. Radiosensitizing and hyperthermic properties of hyaluronan conjugated, dextran-coated ferric oxide nanoparticles: implications for cancer stem cell therapy. J Nanomater. 2015;2015:1–11.

    Google Scholar 

  133. Yang R, Tang Q, Miao F, An Y, Li M, Han Y, et al. Inhibition of heat-shock protein 90 sensitizes liver cancer stem-like cells to magnetic hyperthermia and enhances anti-tumor effect on hepatocellular carcinoma-burdened nude mice. Int J Nanomedicine. 2015;10:7345–58.

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Liang S, Li C, Zhang C, Chen Y, Xu L, Bao C, et al. CD44v6 monoclonal antibody-conjugated gold nanostars for targeted photoacoustic imaging and plasmonic photothermal therapy of gastric cancer stem-like cells. Theranostics. 2015;5:970–84.

    CAS  PubMed  PubMed Central  Google Scholar 

  135. de Paula LB, Primo FL, Pinto MR, Morais PC, Tedesco AC. Combination of hyperthermia and photodynamic therapy on mesenchymal stem cell line treated with chloroaluminum phthalocyanine magnetic-nanoemulsion. J Magn Magn Mater. 2015;380:372–6.

    Google Scholar 

  136. Wang H, Agarwal P, Zhao S, Yu J, Lu X, He X. Combined cancer therapy with hyaluronan-decorated fullerene-silica multifunctional nanoparticles to target cancer stem-like cells. Biomaterials. 2016;97:62–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Paholak HJ, Stevers NO, Chen H, Burnett JP, He M, Korkaya H, et al. Elimination of epithelial-like and mesenchymal-like breast cancer stem cells to inhibit metastasis following nanoparticle-mediated photothermal therapy. Biomaterials. 2016;104:145–57.

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Kawakami Y, Matsushita M, Ueda R, Tsukamoto N, Ohta S. Immunotherapy targeting cancer stem cells. Nippon Rinsho Jpn J Clin Med. 2012;70:2142–6.

    Google Scholar 

  139. Kerns SL, Ostrer H, Rosenstein BS. Radiogenomics: using genetics to identify cancer patients at risk for development of adverse effects following radiotherapy. Cancer Discov. 2014;4:155–65.

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Kouhsari E, Ghadimi-Daresajini A, Abdollahi H, Amirmozafari N, Mahdavi S, Abbasian S, et al. The potential roles of bacteria to improve radiation treatment outcome. Clin Trans Oncol. 2018;20(2):127–39. https://doi.org/10.1007/s12094-017-1701-7

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medical Physics, School of Medicine, Iran University of Medical Sciences, Junction of Shahid Hemmat and Chamran Expressway, Tehran, Iran

    H. Ghaffari, J. Beik, A. Talebi, S. R. Mahdavi & H. Abdollahi

  2. Department of Medical Physics and Radiation Biology Research Center, Iran University of Medical Sciences, Junction of Shahid Hemmat and Chamran Expressway, Tehran, Iran

    S. R. Mahdavi

Authors
  1. H. Ghaffari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Beik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Talebi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. R. Mahdavi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. Abdollahi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to S. R. Mahdavi or H. Abdollahi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Consent is not required for this type of study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghaffari, H., Beik, J., Talebi, A. et al. New physical approaches to treat cancer stem cells: a review. Clin Transl Oncol 20, 1502–1521 (2018). https://doi.org/10.1007/s12094-018-1896-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12094-018-1896-2

Keywords

Search

Navigation