Nanomedicine strategies for sustained, controlled and targeted treatment of cancer stem cells

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1 Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 414(6859), 105–111 (2001). • An excellent review paper that clarifies the idea of cancer stem cells (CSCs).
  Medline CASGoogle Scholar
• 2 Clarke MF, Dick JE, Dirks PB et al. Cancer stem cells-perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res. 66(19), 9339–9344 (2006).
  Medline CASGoogle Scholar
• 3 Zhou B-BS, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat. Rev. Drug Discov. 8(10), 806–823 (2009). •• An good review paper about how CSC target drugs could be discovered.
  Medline CASGoogle Scholar
• 4 Takebe N, Harris PJ, Warren RQ, Ivy SP. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat. Rev. Clin. Oncol. 8(2), 97–106 (2011).
  Medline CASGoogle Scholar
• 5 Fang DD, Wen D, Xu Y. Identification of cancer stem cells provides novel tumor models for drug discovery. Front. Med. 6(2), 112–121 (2012).
  MedlineGoogle Scholar
• 6 James AM, Linda SS, Stephen LA et al. Targeting the cancer initiating cell: the ultimate target for cancer therapy. Curr. Pharm. Des. 18(13), 1784–1795 (2012).
  MedlineGoogle Scholar
• 7 Shigdar S, Lin J, Li Y et al. Cancer stem cell targeting: the next generation of cancer therapy and molecular imaging. Ther. Deliv. 3(2), 227–244 (2012).
  Medline CASGoogle Scholar
• 8 Feng SS. Chemotherapeutic Engineering – Collected Papers of Si-Shen Feng – A Tribute to Shu Chien on His 82nd Birthday. CRC Press, FL, USA (2014).
  Google Scholar
• 9 Mei L, Zhang Z, Zhao L et al. Pharmaceutical nanotechnology for oral delivery of anticancer drugs. Adv. Drug Deliv. Rev. 65(6), 880–890 (2013).
  Medline CASGoogle Scholar
• 10 Zhang Z, Mei L, Feng SS. Paclitaxel drug delivery systems. Expert Opin. Drug Deliv. 10(3), 325–340 (2013).
  Medline CASGoogle Scholar
• 11 Zhang Z, Tan S, Feng SS. Vitamin E TPGS as a molecular biomaterial for drug delivery. Biomaterials 33(19), 4889–4906 (2012).
  Medline CASGoogle Scholar
• 12 Feng SS. New-concept chemotherapy by nanoparticles of biodegradable polymers: where are we now? Nanomedicine (Lond.) 1(3), 297–309 (2006).
  CASGoogle Scholar
• 13 Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2(12), 751–760 (2007).
  Medline CASGoogle Scholar
• 14 Moghimi SM, Hunter AC, Murray JC. Nanomedicine: current status and future prospects. FASEB J. 19(3), 311–330 (2005).
  Medline CASGoogle Scholar
• 15 Zhang X, Dong Y, Zeng X et al. The effect of autophagy inhibitors on drug delivery using biodegradable polymer nanoparticles in cancer treatment. Biomaterials 35(6), 1932–1943 (2014).
  Medline CASGoogle Scholar
• 16 Mei L, Zhang X, Feng SS. Autophagy inhibition strategy for advanced nanomedicine. Nanomedicine (Lond.) 9(3), 377–380 (2014).
  CASGoogle Scholar
• 17 Zhao Y, Alakhova DY, Kabanov AV. Can nanomedicines kill cancer stem cells? Adv. Drug Deliv. Rev. 65(13–4), 1763–1783 (2013).
  Medline CASGoogle Scholar
• 18 Wang K, Wu X, Wang J, Huang J. Cancer stem cell theory: therapeutic implications for nanomedicine. Int. J Nanomedicine 8, 899–908 (2013).
  MedlineGoogle Scholar
• 19 Win YK, Feng SS. Effects of particle size and surface coating on cellular uptake of polymeric nanoparticles for oral delivery of anticancer drugs. Biomaterials 26(15), 2713–2722 (2005).
  Medline CASGoogle Scholar
• 20 Feng SS. Chemotherapeutic engineering: concept, feasibility, safety and prospect – a tribute to Shu Chien’s 80th birthday. Cell. Mol. Bioeng. 4(4), 708–716 (2011).
  CASGoogle Scholar
• 21 Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat. Rev. Cancer 5(4), 275–284 (2005).
  Medline CASGoogle Scholar
• 22 He S, Nakada D, Morrison SJ. Mechanisms of stem cell self-renewal. Annu. Rev. Cell Dev. Biol. 25, 377–406 (2009).
  Medline CASGoogle Scholar
• 23 Wray J, Kalkan T, Smith Austin G. The ground state of pluripotency. Biochem. Soc. Trans. 38(4), 1027–1032 (2010).
  Medline CASGoogle Scholar
• 24 Vermeulen L, de Sousa e Melo F, Richel DJ, Medema JP. The developing cancer stem-cell model: clinical challenges and opportunities. Lancet Oncol. 13(2), e83–e89 (2012).
  MedlineGoogle Scholar
• 25 Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell 10(6), 717–728 (2012).
  Medline CASGoogle Scholar
• 26 Tang DG. Understanding cancer stem cell heterogeneity and plasticity. Cell Res. 22(3), 457–472 (2012).
  Medline CASGoogle Scholar
• 27 Stewart JM, Shaw PA, Gedye C, Bernardini MQ, Neel BG, Ailles LE. Phenotypic heterogeneity and instability of human ovarian tumor-initiating cells. Proc. Natl Acad. Sci. USA 108(16), 6468–6473 (2011).
  Medline CASGoogle Scholar
• 28 Gibbs KD, Jager A, Crespo O et al. Decoupling of tumor-initiating activity from stable immunophenotype in HoxA9-Meis1-driven AML. Cell Stem Cell 10(2), 210–217 (2012).
  Medline CASGoogle Scholar
• 29 Gottesman MM. Mechanisms of cancer drug resistance. Annu. Rev. Med. 53(1), 615–627 (2002).
  Medline CASGoogle Scholar
• 30 Ito K, Hirao A, Arai F et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431(7011), 997–1002 (2004).
  Medline CASGoogle Scholar
• 31 Kim J, Wong PKY. Loss of ATM impairs proliferation of neural stem cells through oxidative stress-mediated p38 MAPK signaling. Stem Cells 27(8), 1987–1998 (2009).
  Medline CASGoogle Scholar
• 32 Bao S, Wu Q, McLendon RE et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444(7120), 756–760 (2006).
  Medline CASGoogle Scholar
• 33 Diehn M, Cho RW, Lobo NA et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458(7239), 780–783 (2009).
  Medline CASGoogle Scholar
• 34 Lagadinou ED, Sach A, Callahan K et al. BCL-2 inhibition targets oxidative phosphorylation and selectively eradicates quiescent human leukemia stem cells. Cell Stem Cell 12(3), 329–341 (2013).
  Medline CASGoogle Scholar
• 35 Ye XQ, Wang GH, Huang GJ, Bian XW, Qian GS, Yu SC. Heterogeneity of mitochondrial membrane potential: a novel tool to isolate and identify cancer stem cells from a tumor mass? Stem Cell Rev. 7(1), 153–160 (2011).
  Medline CASGoogle Scholar
• 36 Yi SY, Hao YB, Nan KJ, Fan TL. Cancer stem cells niche: a target for novel cancer therapeutics. Cancer Treat. Rev. 39(3), 290–296 (2013).
  Medline CASGoogle Scholar
• 37 Ma S, Tang KH, Chan YP et al. miR-130b promotes CD133+ liver tumor-initiating cell growth and self-renewal via tumor protein 53-induced nuclear protein 1. Cell Stem Cell 7(6), 694–707 (2010).
  Medline CASGoogle Scholar
• 38 Zeppernick F, Ahmadi R, Campos B et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin. Cancer Res. 14(1), 123 (2008).
  Medline CASGoogle Scholar
• 39 Ginestier C, Hur MH, Charafe-Jauffret E et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1(5), 555–567 (2007).
  Medline CASGoogle Scholar
• 40 Lepourcelet M, Chen Y-NP, France DS et al. Small-molecule antagonists of the oncogenic Tcf/β-catenin protein complex. Cancer Cell 5(1), 91–102 (2004).
  Medline CASGoogle Scholar
• 41 Emami KH, Nguyen C, Ma H et al. A small molecule inhibitor of β-catenin/cyclic AMP response element-binding protein transcription. Proc. Natl Acad. Sci. USA 101(34), 12682–12687 (2004).
  Medline CASGoogle Scholar
• 42 LoRusso PM, Rudin CM, Reddy JC et al. Phase I trial of hedgehog pathway inhibitor vismodegib (GDC-0449) in patients with refractory, locally advanced or metastatic solid tumors. Clin. Cancer Res. 17(8), 2502 (2011).
  Medline CASGoogle Scholar
• 43 Wicha MS, Liu S, Dontu G. Cancer stem cells: an old idea – a paradigm shift. Cancer Res. 66(4), 1883 (2006). • An excellent review paper about how the idea of CSCs was generated.
  Medline CASGoogle Scholar
• 44 Weijzen S, Rizzo P, Braid M et al. Activation of Notch-1 signalling maintains the neoplastic phenotype in human Ras-transformed cells. Nat. Med. 8(9), 979–986 (2002).
  Medline CASGoogle Scholar
• 45 Weng AP, Ferrando AA, Lee W et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306(5694), 269–271 (2004).
  Medline CASGoogle Scholar
• 46 Fan X, Matsui W, Khaki L et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 66(15), 7445 (2006).
  Medline CASGoogle Scholar
• 47 Deangelo DJ, Stone RM, Silverman LB et al. A Phase I clinical trial of the notch inhibitor MK-0752 in patients with T-cell acute lymphoblastic leukemia/lymphoma (T-ALL) and other leukemias. J. Clin. Oncol. 24(18S), 6585 (2006).
  Google Scholar
• 48 Bednar F, Simeone DM. Metformin and cancer stem cells: old drug, new targets. Cancer Prev. Res. 5(3), 351–354 (2012).
  Medline CASGoogle Scholar
• 49 Del Barco S, Vazquez-Martin A, Cufí S et al. Metformin: multi-faceted protection against cancer. Oncotarget 2(12), 896–917 (2011).
  MedlineGoogle Scholar
• 50 Naujokat C, Steinhart R. Salinomycin as a drug for targeting human cancer stem cells. J. Biomed. Biotechnol. 2012, 950658 (2012).
  MedlineGoogle Scholar
• 51 Chong CR, Sullivan DJ. New uses for old drugs. Nature 448(7154), 645–646 (2007).
  Medline CASGoogle Scholar
• 52 de Fougerolles A, Vornlocher H-P, Maraganore J, Lieberman J. Interfering with disease: a progress report on siRNA-based therapeutics. Nat. Rev. Drug Discov. 6(6), 443–453 (2007).
  Medline CASGoogle Scholar
• 53 Yin C, Lin Y, Zhang X et al. Differentiation therapy of hepatocellular carcinoma in mice with recombinant adenovirus carrying hepatocyte nuclear factor-4alpha gene. Hepatology 48(5), 1528–1539 (2008).
  Medline CASGoogle Scholar
• 54 Yin C, Xie WF. Differentiation therapy with transcription factors might present as an ideal strategy for the treatment of cancer. Hepatology 50(6), 2046–2047 (2009). • A good paper about the idea of targeting CSCs by differentiation therapy.
  MedlineGoogle Scholar
• 55 Yin C, Xie WF. Hepatocellular carcinoma: basic and transitional research. Gastroint. Tumors 1(2), 76–83 (2014).
  Medline CASGoogle Scholar
• 56 Ning BF, Ding J, Yin C et al. Hepatocyte nuclear factor 4α suppresses the development of hepatocellular carcinoma. Cancer Res. 70(19), 7640 (2010).
  Medline CASGoogle Scholar
• 57 Jiang CF, Wen LZ, Yin C et al. Apoptosis signal-regulating kinase 1 mediates the inhibitory effect of hepatocyte nuclear factor-4α on hepatocellular carcinoma. Oncotarget 7(19), 27408–27421 (2016).
  MedlineGoogle Scholar
• 58 Ning BF, Ding J, Liu J et al. Hepatocyte nuclear factor 4α-nuclear factor-κB feedback circuit modulates liver cancer progression. Hepatology 60(5), 1607–1619 (2014).
  Medline CASGoogle Scholar
• 59 Zeng X, Lin Y, Yin C et al. Recombinant adenovirus carrying the hepatocyte nuclear factor-1alpha gene inhibits hepatocellular carcinoma xenograft growth in mice. Hepatology 54(6), 2036–2047 (2011).
  Medline CASGoogle Scholar
• 60 Shi YC, Zhao H, Yin C et al. C/EBPα inhibits hepatocellular carcinoma by reducing Notch3/Hes1/p27 cascades. Dig. Liver Dis. 45(10), 844–851 (2013).
  Medline CASGoogle Scholar
• 61 You L, He B, Xu Z et al. An anti-Wnt-2 monoclonal antibody induces apoptosis in malignant melanoma cells and inhibits tumor growth. Cancer Res. 64(15), 5385–5389 (2004).
  Medline CASGoogle Scholar
• 62 You L, He B, Xu Z et al. Inhibition of Wnt-2-mediated signaling induces programmed cell death in non-small-cell lung cancer cells. Oncogene 23(36), 6170–6174 (2004).
  Medline CASGoogle Scholar
• 63 Sanchez P, Hernández AM, Stecca B et al. Inhibition of prostate cancer proliferation by interference with SONIC HEDGEHOG-GLI1 signaling. Proc. Natl Acad. Sci. USA 101(34), 12561–12566 (2004).
  Medline CASGoogle Scholar
• 64 Jiang J, Zhang Y, Chuai S et al. Trastuzumab (herceptin) targets gastric cancer stem cells characterized by CD90 phenotype. Oncogene 31(6), 671–682 (2012).
  Medline CASGoogle Scholar
• 65 Magnifico A, Albano L, Campaner S et al. Tumor-initiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clin. Cancer Res. 15(6), 2010 (2009).
  Medline CASGoogle Scholar
• 66 Schatton T, Murphy GF, Frank NY et al. Identification of cells initiating human melanomas. Nature 451(7176), 345–349 (2008).
  Medline CASGoogle Scholar
• 67 Burges A, Wimberger P, Kümper C et al. Effective relief of malignant ascites in patients with advanced ovarian cancer by a trifunctional anti-EpCAM × anti-CD3 antibody: a Phase I/II study. Clin. Cancer Res. 13(13), 3899–3905 (2007).
  Medline CASGoogle Scholar
• 68 Wu AM, Senter PD. Arming antibodies: prospects and challenges for immunoconjugates. Nat. Biotech. 23(9), 1137–1146 (2005).
  Medline CASGoogle Scholar
• 69 Clayton S, Mousa SA. Therapeutics formulated to target cancer stem cells: Is it in our future? Cancer Cell Int. 11, 7 (2011).
  MedlineGoogle Scholar
• 70 Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat. Med. 12(10), 1167–1174 (2006).
  MedlineGoogle Scholar
• 71 Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB. Bioavailability of curcumin: problems and promises. Mol. Pharm. 4(6), 807–818 (2007).
  Medline CASGoogle Scholar
• 72 Capaccione KM, Pine SR. The Notch signaling pathway as a mediator of tumor survival. Carcinogenesis 34(7), 1420–1430 (2013).
  Medline CASGoogle Scholar
• 73 Chaffer CL, Brueckmann I, Scheel C et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc. Natl Acad. Sci. USA 108(19), 7950–7955 (2011).
  Medline CASGoogle Scholar
• 74 Dubrovska A, Elliott J, Salamone RJ et al. Combination therapy targeting both tumor-initiating and differentiated cell populations in prostate carcinoma. Clin. Cancer Res. 16(23), 5692 (2010).
  Medline CASGoogle Scholar
• 75 Mueller MT, Hermann PC, Witthauer J et al. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 137(3), 1102–1113 (2009).
  Medline CASGoogle Scholar
• 76 Zucker D, Barenholz Y. Optimization of vincristine-topotecan combination – Paving the way for improved chemotherapy regimens by nanoliposomes. J. Control. Release 146(3), 326–333 (2010).
  Medline CASGoogle Scholar
• 77 Parhi P, Mohanty C, Sahoo SK. Nanotechnology-based combinational drug delivery: an emerging approach for cancer therapy. Drug Discov. Today 17(17–18), 1044–1052 (2012).
  Medline CASGoogle Scholar
• 78 Zhang Z, Yang X, Feng SS. Copolymer technology for advanced nanomedicine. Nanomedicine (Lond.) 6(4), 583–587 (2011).
  CASGoogle Scholar
• 79 Gan CW, Chien S, Feng SS. Nanomedicine: enhancement of chemotherapeutical efficacy of docetaxel by using a biodegradable nanoparticle formulation. Curr. Pharm. Des. 16(21), 2308–2320 (2010).
  Medline CASGoogle Scholar
• 80 Gao J, Yu Y, Zhang Y et al. EGFR-specific PEGylated immunoliposomes for active siRNA delivery in hepatocellular carcinoma. Biomaterials 33(1), 270–282 (2012).
  Medline CASGoogle Scholar
• 81 Gao J, Liu W, Xia Y et al. The promotion of siRNA delivery to breast cancer overexpressing epidermal growth factor receptor through anti-EGFR antibody conjugation by immunoliposomes. Biomaterials 32(13), 3459–3470 (2011).
  Medline CASGoogle Scholar
• 82 Gao J, Sun J, Li H et al. Lyophilized HER2-specific PEGylated immunoliposomes for active siRNA gene silencing. Biomaterials 31(9), 2655–2664 (2010).
  Medline CASGoogle Scholar
• 83 Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science 303(5665), 1818 (2004).
  Medline CASGoogle Scholar
• 84 Gao J, Feng SS, Guo Y. Antibody engineering promotes nanomedicine for cancer treatment. Nanomedicine (Lond.) 5(8), 1141–1145 (2010).
  CASGoogle Scholar
• 85 Gao J, Chen H, Song H et al. Antibody-targeted immunoliposomes for cancer treatment. Mini. Rev. Med. Chem. 13(14), 2026–2035 (2013).
  Medline CASGoogle Scholar
• 86 Vinogradov S, Wei X. Cancer stem cells and drug resistance: the potential of nanomedicine. Nanomedicine (Lond.) 7(4), 597–615 (2012).
  CASGoogle Scholar
• 87 van Rhenen A, van Dongen GAMS, Kelder A et al. The novel AML stem cell-associated antigen CLL-1 aids in discrimination between normal and leukemic stem cells. Blood 110(7), 2659 (2007).
  Medline CASGoogle Scholar
• 88 Zhang H, Luo J, Li Y et al. Characterization of high-affinity peptides and their feasibility for use in nanotherapeutics targeting leukemia stem cells. Nanomedicine 8(7), 1116–1124 (2012).
  Medline CASGoogle Scholar
• 89 Gao J, Feng SS, Guo Y. Nanomedicine against multidrug resistance in cancer treatment. Nanomedicine (Lond.) 7(4), 465–468 (2012).
  CASGoogle Scholar
• 90 Gao J, Feng SS, Guo Y. Nanomedicine for treatment of cancer stem cells. Nanomedicine (Lond.) 9(2), 181–184 (2014). • An excellent editorial paper about CSCs targeting nanomedicines.
  CASGoogle Scholar
• 91 Su X, Song H, Niu F et al. Co-delivery of doxorubicin and PEGylated C16-ceramide by nanoliposomes for enhanced therapy against multidrug resistance. Nanomedicine (Lond.) 10(13), 2033–2050 (2015).
  CASGoogle Scholar
• 92 Chen Y, Bathula SR, Li J, Huang L. Multifunctional nanoparticles delivering small interfering RNA and doxorubicin overcome drug resistance in cancer. J. Biol. Chem. 285(29), 22639–22650 (2010).
  Medline CASGoogle Scholar
• 93 Gao J, Chen H, Yu Y et al. Inhibition of hepatocellular carcinoma growth using immunoliposomes for co-delivery of adriamycin and ribonucleotide reductase M2 siRNA. Biomaterials 34(38), 10084–10098 (2013).
  Medline CASGoogle Scholar
• 94 Milane L, Ganesh S, Shah S, Duan Z-f, Amiji M. Multi-modal strategies for overcoming tumor drug resistance: hypoxia, the Warburg effect, stem cells, and multifunctional nanotechnology. J. Control. Release 155(2), 237–247 (2011).
  Medline CASGoogle Scholar
• 95 Li W, Li J, Gao J et al. The fine-tuning of thermosensitive and degradable polymer micelles for enhancing intracellular uptake and drug release in tumors. Biomaterials 32(15), 3832–3844 (2011).
  Medline CASGoogle Scholar
• 96 Singh Y, Palombo M, Sinko PJ. Recent trends in targeted anticancer prodrug and conjugate design. Curr. Med. Chem. 15(18), 1802–1826 (2008).
  Medline CASGoogle Scholar
• 97 Li F, Maag H, Alfredson T. Prodrugs of nucleoside analogues for improved oral absorption and tissue targeting. J. Pharm. Sci. 97(3), 1109–1134 (2008).
  Medline CASGoogle Scholar
• 98 Chen JK, Taipale J, Cooper MK, Beachy PA. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16(21), 2743–2748 (2002).
  Medline CASGoogle Scholar
• 99 Zhou Y, Yang J, Kopeček J. Selective inhibitory effect of HPMA copolymer–cyclopamine conjugate on prostate cancer stem cells. Biomaterials 33(6), 1863–1872 (2012).
  Medline CASGoogle Scholar
• 100 Mimeault M, Batra SK. Potential applications of curcumin and its novel synthetic analogs and nanotechnology-based formulations in cancer prevention and therapy. Chin. Med. 6, 31–31 (2011).
  Medline CASGoogle Scholar
• 101 Lim KJ, Bisht S, Bar EE, Maitra A, Eberhart CG. A polymeric nanoparticle formulation of curcumin inhibits growth, clonogenicity and stem-like fraction in malignant brain tumors. Cancer Biol. Ther. 11(5), 464–473 (2011).
  Medline CASGoogle Scholar
• 102 Mamaeva V, Rosenholm JM, Bate-Eya LT et al. Mesoporous silica nanoparticles as drug delivery systems for targeted inhibition of Notch signaling in cancer. Mol. Ther. 19(8), 1538–1546 (2011).
  Medline CASGoogle Scholar
• 103 Aydın RST. Herceptin-decorated salinomycin-loaded nanoparticles for breast tumor targeting. J. Biomed. Mater. Res. A 101(5), 1405–1415 (2013).
  MedlineGoogle Scholar
• 104 Orza A, Soriţău O, Tomuleasa C et al. Reversing chemoresistance of malignant glioma stem cells using gold nanoparticles. Int. J. Nanomedicine 8, 689–702 (2013).
  MedlineGoogle Scholar
• 105 Lee H, Park S, Kim JB, Kim J, Kim H. Entrapped doxorubicin nanoparticles for the treatment of metastatic anoikis-resistant cancer cells. Cancer Lett. 332(1), 110–119 (2013).
  Medline CASGoogle Scholar
• 106 Sun T-M, Wang Y-C, Wang F et al. Cancer stem cell therapy using doxorubicin conjugated to gold nanoparticles via hydrazone bonds. Biomaterials 35(2), 836–845 (2014).
  Medline CASGoogle Scholar
• 107 Mizrahy S, Raz SR, Hasgaard M et al. Hyaluronan-coated nanoparticles: The influence of the molecular weight on CD44-hyaluronan interactions and on the immune response. J. Control. Release 156(2), 231–238 (2011).
  Medline CASGoogle Scholar
• 108 Ossipov DA. Nanostructured hyaluronic acid-based materials for active delivery to cancer. Expert Opin. Drug Deliv. 7(6), 681–703 (2010).
  Medline CASGoogle Scholar
• 109 Lim ST, Martin GP, Berry DJ, Brown MB. Preparation and evaluation of the in vitro drug release properties and mucoadhesion of novel microspheres of hyaluronic acid and chitosan. J. Control. Release 66(2–3), 281–292 (2000).
  Medline CASGoogle Scholar
• 110 Choi KY, Chung H, Min KH et al. Self-assembled hyaluronic acid nanoparticles for active tumor targeting. Biomaterials 31(1), 106–114 (2010).
  Medline CASGoogle Scholar
• 111 Cho H-J, Yoon I-S, Yoon HY et al. Polyethylene glycol-conjugated hyaluronic acid-ceramide self-assembled nanoparticles for targeted delivery of doxorubicin. Biomaterials 33(4), 1190–1200 (2012).
  Medline CASGoogle Scholar
• 112 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 7(1), 69–79 (2011).
  Medline CASGoogle Scholar
• 113 Shvedova AA, Kagan VE. The role of nanotoxicology in realizing the ‘helping without harm’ paradigm of nanomedicine: lessons from studies of pulmonary effects of single-walled carbon nanotubes. J. Intern. Med. 267(1), 106–118 (2010).
  Medline CASGoogle Scholar
• 114 Guibal FC, Alberich-Jorda M, Hirai H et al. Identification of a myeloid committed progenitor as the cancer-initiating cell in acute promyelocytic leukemia. Blood 114(27), 5415–5425 (2009).
  Medline CASGoogle Scholar
• 115 Barth BM, I Altinoğlu E, Shanmugavelandy SS et al. Targeted indocyanine-green-loaded calcium phosphosilicate nanoparticles for in vivo photodynamic therapy of leukemia. ACS Nano 5(7), 5325–5337 (2011).
  Medline CASGoogle Scholar
• 116 Zhou P, Hatziieremia S, Elliott MA et al. Uptake of synthetic low density lipoprotein by leukemic stem cells – a potential stem cell targeted drug delivery strategy. J. Control. Release 148(3), 380–387 (2010).
  Medline CASGoogle Scholar
• 117 Daka A, Peer D. RNAi-based nanomedicines for targeted personalized therapy. Adv. Drug Deliv. Rev. 64(13), 1508–1521 (2012).
  Medline CASGoogle Scholar
• 118 Zhao J, Mi Y, Feng SS. siRNA-based nanomedicine. Nanomedicine (Lond.) 8(6), 859–862 (2013).
  CASGoogle Scholar
• 119 Yang Y-P, Chien Y, Chiou G-Y et al. Inhibition of cancer stem cell-like properties and reduced chemoradioresistance of glioblastoma using microRNA145 with cationic polyurethane-short branch PEI. Biomaterials 33(5), 1462–1476 (2012).
  Medline CASGoogle Scholar
• 120 Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int. J. Radiat. Oncol. Biol. Phys. 10(6), 787–800 (1984).
  Medline CASGoogle Scholar
• 121 Burke AR, Singh RN, Carroll DL et al. The resistance of breast cancer stem cells to conventional hyperthermia and their sensitivity to nanoparticle-mediated photothermal therapy. Biomaterials 33(10), 2961–2970 (2012).
  Medline CASGoogle Scholar
• 122 Atkinson RL, Zhang M, Diagaradjane P et al. Thermal enhancement with optically activated gold nanoshells sensitizes breast cancer stem cells to radiation therapy. Sci. Transl. Med. 2(55), 55ra79 (2010).
  MedlineGoogle Scholar
• 123 Sadhukha T, Niu L, Wiedmann TS, Panyam J. Effective elimination of cancer stem cells by magnetic hyperthermia. Mol. Pharm. 10(4), 1432–1441 (2013).
  Medline CASGoogle Scholar
• 124 Mannix RJ, Kumar S, Cassiola F et al. Nanomagnetic actuation of receptor-mediated signal transduction. Nat Nanotechnol. 3(1), 36–40 (2008).
  Medline CASGoogle Scholar
• 125 Konan YN, Gurny R, Allémann E. State of the art in the delivery of photosensitizers for photodynamic therapy. J. Photochem. Photobiol. B. 66(2), 89–106 (2002).
  Medline CASGoogle Scholar
• 126 Hambley TW, Hait WN. Is anticancer drug development heading in the right direction? Cancer Res. 69(4), 1259–1262 (2009).
  Medline CASGoogle Scholar
• 127 Minchinton AI, Tannock IF. Drug penetration in solid tumours. Nat. Rev. Cancer 6(8), 583–592 (2006).
  Medline CASGoogle Scholar
• 128 Heddleston JM, Li Z, Lathia JD, Bao S, Hjelmeland AB, Rich JN. Hypoxia inducible factors in cancer stem cells. Br. J. Cancer 102(5), 789–795 (2010).
  Medline CASGoogle Scholar
• 129 Keith B, Simon MC. Hypoxia-inducible factors, stem cells and cancer. Cell 129(3), 465–472 (2007).
  Medline CASGoogle Scholar
• 130 Heddleston JM, Li Z, Hjelmeland AB, Rich JN. The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 8(20), 3274–3284 (2009).
  Medline CASGoogle Scholar
• 131 Li Z, Bao S, Wu Q et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 15(6), 501–513 (2009).
  Medline CASGoogle Scholar
• 132 Grainger SJ, Serna JV, Sunny S, Zhou Y, Deng CX, El-Sayed MEH. Pulsed ultrasound enhances nanoparticle penetration into breast cancer spheroids. Mol. Pharm. 7(6), 2006–2019 (2010).
  Medline CASGoogle Scholar
• 133 Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 4(2), 145–160 (2005).
  Medline CASGoogle Scholar
• 134 Guo J, Zhou J, Ying X et al. Effects of stealth liposomal daunorubicin plus tamoxifen on the breast cancer and cancer stem cells. J. Pharm. Pharm. Sci. 13(2), 136–151 (2010).
  Medline CASGoogle Scholar
• 135 Zhang L, Yao H-J, Yu Y et al. Mitochondrial targeting liposomes incorporating daunorubicin and quinacrine for treatment of relapsed breast cancer arising from cancer stem cells. Biomaterials 33(2), 565–582 (2012).
  Medline CASGoogle Scholar
• 136 Xie F, Zhang S, Liu J et al. Codelivery of salinomycin and chloroquine by liposomes enables synergistic antitumor activity in vitro. Nanomedicine (Lond.) 11(14), 1831–1846 (2016).
  CASGoogle Scholar
• 137 Liu Y, Lu W-L, Guo J et al. A potential target associated with both cancer and cancer stem cells: a combination therapy for eradication of breast cancer using vinorelbine stealthy liposomes plus parthenolide stealthy liposomes. J. Control. Release 129(1), 18–25 (2008).
  Medline CASGoogle Scholar
• 138 Li R-J, Ying X, Zhang Y et al. All-trans retinoic acid stealth liposomes prevent the relapse of breast cancer arising from the cancer stem cells. J. Control. Release 149(3), 281–291 (2011).
  Medline CASGoogle Scholar
• 139 Padhye SS, Guin S, Yao H-P, Zhou Y-Q, Zhang R, Wang MH. Sustained expression of the RON receptor tyrosine kinase by pancreatic cancer stem cells as a potential targeting moiety for antibody-directed chemotherapeutics. Mol. Pharm. 8(6), 2310–2319 (2011).
  Medline CASGoogle Scholar
• 140 Kong Y, Yoshida S, Saito Y et al. CD34+CD38+CD19+ as well as CD34+CD38-CD19+ cells are leukemia-initiating cells with self-renewal capacity in human B-precursor ALL. Leukemia 22(6), 1207–1213 (2008).
  Medline CASGoogle Scholar
• 141 Uckun FM, Jaszcz W, Ambrus JL et al. Detailed studies on expression and function of CD19 surface determinant by using B43 monoclonal antibody and the clinical potential of anti-CD19 immunotoxins. Blood 71(1), 13–29 (1988).
  Medline CASGoogle Scholar
• 142 Zhang J, Tang Y, Li S, Liao C, Guo X. Targeting of the B-lineage leukemia stem cells and their progeny with norcantharidin encapsulated liposomes modified with a novel CD19 monoclonal antibody 2E8 in vitro. J. Drug Target. 18(9), 675–687 (2010).
  MedlineGoogle Scholar
• 143 Song H, Su X, Yang K et al. CD20 antibody-conjugated immunoliposomes for targeted chemotherapy of melanoma cancer initiating cells. J. Biomed. Nanotechnol. 11(11), 1927–1946 (2015).
  Medline CASGoogle Scholar
• 144 Brandes AA, Franceschi E, Tosoni A et al. MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J. Clin. Oncol. 26(13), 2192–2197 (2008).
  MedlineGoogle Scholar
• 145 Kato T, Natsume A, Toda H et al. Efficient delivery of liposome-mediated MGMT-siRNA reinforces the cytotoxity of temozolomide in GBM-initiating cells. Gene Ther. 17(11), 1363–1371 (2010).
  Medline CASGoogle Scholar
• 146 Li SD, Chono S, Huang L. Efficient gene silencing in metastatic tumor by siRNA formulated in surface-modified nanoparticles. J. Control. Release 126(1), 77–84 (2008).
  Medline CASGoogle Scholar
• 147 Cabral H, Matsumoto Y, Mizuno K et al. Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nat. Nanotechnol. 6(12), 815–823 (2011).
  Medline CASGoogle Scholar
• 148 Huang K, Ma H, Liu J et al. Size-dependent localization and penetration of ultrasmall gold nanoparticles in cancer cells, multicellular spheroids, and tumors in vivo. ACS Nano 6(5), 4483–4493 (2012).
  Medline CASGoogle Scholar
• 149 Ong S-M, Zhao Z, Arooz T et al. Engineering a scaffold-free 3D tumor model for in vitro drug penetration studies. Biomaterials 31(6), 1180–1190 (2010).
  Medline CASGoogle Scholar
• 150 Lin RZ, Chang HY. Recent advances in three-dimensional multicellular spheroid culture for biomedical research. Biotechnol. J. 3(9–10), 1172–1184 (2008).
  Medline CASGoogle Scholar
• 151 Pickl M, Ries CH. Comparison of 3D and 2D tumor models reveals enhanced HER2 activation in 3D associated with an increased response to trastuzumab. Oncogene 28(3), 461–468 (2009).
  Medline CASGoogle Scholar
• 152 Mao X, Liu J, Gong Z et al. iRGD-conjugated DSPE-PEG2000 nanomicelles for targeted delivery of salinomycin for treatment of both liver cancer cells and cancer stem cells. Nanomedicine (Lond.) 10(17), 2677–2695 (2015).
  CASGoogle Scholar
• 153 Kim TH, Mount CW, Gombotz WR, Pun SH. The delivery of doxorubicin to 3-D multicellular spheroids and tumors in a murine xenograft model using tumor-penetrating triblock polymeric micelles. Biomaterials 31(28), 7386–7397 (2010).
  Medline CASGoogle Scholar
• 154 Zhao X, Singh S, Pardoux C et al. Targeting C-type lectin-like molecule-1 for antibody-mediated immunotherapy in acute myeloid leukemia. Haematologica 95(1), 71–78 (2010).
  Medline CASGoogle Scholar
• 155 Mu L, Feng SS. Vitamin E TPGS used as emulsifier in the solvent evaporation/extraction technique for fabrication of polymeric nanospheres for controlled release of paclitaxel (Taxol). J. Control. Release 80(1–3), 129–144 (2002).
  Medline CASGoogle Scholar
• 156 Zhang Z, Feng SS. Nanoparticles of poly(lactide)/vitamin E TPGS copolymer for cancer chemotherapy: synthesis, formulation, characterization and in vitro drug release. Biomaterials 27(2), 262–270 (2006).
  MedlineGoogle Scholar
• 157 Zhang Z, Feng SS. The drug encapsulation efficiency, in vitro drug release, cellular uptake and cytotoxicity of paclitaxel-loaded poly(lactide)-tocopheryl polyethylene glycol succinate nanoparticles. Biomaterials 27(21), 4025–4033 (2006).
  Medline CASGoogle Scholar
• 158 Zhang Z, Feng SS. In vitro investigation on poly(lactide)-Tween 80 copolymer nanoparticles fabricated by dialysis method for chemotherapy. Biomacromolecules 7(4), 1139–1146 (2006).
  Medline CASGoogle Scholar
• 159 Dong Y, Feng SS. Methoxy poly(ethylene glycol)-poly(lactide) (MPEG-PLA) nanoparticles for controlled delivery of anticancer drugs. Biomaterials 25(14), 2843–2849 (2004).
  Medline CASGoogle Scholar
• 160 Zou GM. Cancer stem cells in leukemia, recent advances. J. Cell Physiol. 213(2), 440–444 (2007).
  Medline CASGoogle Scholar
• 161 Holyoake TL, Jiang X, Drummond MW, Eaves AC, Eaves CJ. Elucidating critical mechanisms of deregulated stem cell turnover in the chronic phase of chronic myeloid leukemia. Leukemia 16(4), 549–558 (2002).
  Medline CASGoogle Scholar
• 162 Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100(7), 3983–3988 (2003).
  Medline CASGoogle Scholar
• 163 Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res. 10(2), R25 (2008).
  MedlineGoogle Scholar
• 164 Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, Varticovski L. Brca1 breast tumors contain distinct CD44⁺/CD24^- and CD133⁺ cells with cancer stem cell characteristics. Breast Cancer Res. 10(1), R10 (2008).
  MedlineGoogle Scholar
• 165 Hwang-Verslues WW, Kuo W-H, Chang P-H et al. Multiple lineages of human breast cancer stem/progenitor cells identified by profiling with stem cell markers. PLoS ONE 4(12), e8377 (2009).
  MedlineGoogle Scholar
• 166 Patrawala L, Calhoun T, Schneider-Broussard R et al. Highly purified CD44⁺ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25(12), 1696–1708 (2006).
  Medline CASGoogle Scholar
• 167 Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 65(23), 10946–10951 (2005).
  Medline CASGoogle Scholar
• 168 Mulholland DJ, Xin L, Morim A, Lawson D, Witte O, Wu H. Lin-Sca-1⁺CD49^fhigh stem/progenitors are tumor-initiating cells in the PTEN-null prostate cancer model. Cancer Res. 69(22), 8555–8562 (2009).
  Medline CASGoogle Scholar
• 169 Li T, Su Y, Mei Y et al. ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients’ outcome. Lab Invest. 90(2), 234–244 (2010).
  Medline CASGoogle Scholar
• 170 Zhang K, Waxman DJ. PC3 prostate tumor-initiating cells with molecular profile FAM65Bhigh/MFI2low/LEF1low increase tumor angiogenesis. Mol. Cancer 9, 319 (2010).
  Medline CASGoogle Scholar
• 171 Trerotola M, Rathore S, Goel HL et al. CD133, Trop-2 and α2β1 integrin surface receptors as markers of putative human prostate cancer stem cells. Am. J. Transl. Res. 2(2), 135–144 (2010).
  Medline CASGoogle Scholar
• 172 Bussolati B, Bruno S, Grange C, Ferrando U, Camussi G. Identification of a tumor-initiating stem cell population in human renal carcinomas. FASEB J. 22(10), 3696–3705 (2008).
  Medline CASGoogle Scholar
• 173 Silva IA, Bai S, McLean K et al. Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res. 71(11), 3991–4001 (2011).
  Medline CASGoogle Scholar
• 174 Zhang S, Balch C, Chan MW et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 68(11), 4311–4320 (2008).
  Medline CASGoogle Scholar
• 175 Gao MQ, Choi YP, Kang S, Youn JH, Cho NH. CD24⁺ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells. Oncogene 29(18), 2672–2680 (2010).
  Medline CASGoogle Scholar
• 176 Bertolini G, Roz L, Perego P et al. Highly tumorigenic lung cancer CD133⁺ cells display stem-like features and are spared by cisplatin treatment. Proc. Natl Acad. Sci. USA 106(38), 16281–16286 (2009).
  Medline CASGoogle Scholar
• 177 Rivera C, Rivera S, Loriot Y, Vozenin M-C, Deutsch E. Lung cancer stem cell: new insights on experimental models and preclinical data. J. Oncol. 2011, 549181 (2011).
  MedlineGoogle Scholar
• 178 Takaishi S, Okumura T, Tu S et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 27(5), 1006–1020 (2009).
  Medline CASGoogle Scholar
• 179 Sergeant G, Vankelecom H, Gremeaux L, Topal B. Role of cancer stem cells in pancreatic ductal adenocarcinoma. Nat. Rev. Clin. Oncol. 6(10), 580–586 (2009).
  MedlineGoogle Scholar
• 180 Li C, Heidt DG, Dalerba P et al. Identification of pancreatic cancer stem cells. Cancer Res. 67(3), 1030–1037 (2007).
  Medline CASGoogle Scholar
• 181 Jaiswal KR, Xin HW, Anderson A et al. Comparative testing of various pancreatic cancer stem cells results in a novel class of pancreatic-cancer-initiating cells. Stem Cell Res. 9(3), 249–260 (2012).
  Medline CASGoogle Scholar
• 182 May R, Sureban SM, Lightfoot SA et al. Identification of a novel putative pancreatic stem/progenitor cell marker DCAMKL-1 in normal mouse pancreas. Am. J. Physiol. Gastrointest. Liver Physiol. 299(2), G303–G310 (2010).
  Medline CASGoogle Scholar
• 183 Ma S, Chan KW, Hu L et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 132(7), 2542–2556 (2007).
  Medline CASGoogle Scholar
• 184 Yang ZF, Ho DW, Ng MN et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13(2), 153–166 (2008).
  Medline CASGoogle Scholar
• 185 Yamashita T, Forgues M, Wang W et al. EpCAM and alpha-fetoprotein expression defines novel prognostic subtypes of hepatocellular carcinoma. Cancer Res. 68(5), 1451–1461 (2008).
  Medline CASGoogle Scholar
• 186 Haraguchi N, Ishii H, Mimori K et al. CD13 is a therapeutic target in human liver cancer stem cells. J. Clin. Invest. 120(9), 3326–3339 (2010).
  Medline CASGoogle Scholar
• 187 Lee TKW, Castilho A, Cheung VCH, Tang KH, Ma S, Ng IOL. CD24(⁺) liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation. Cell Stem Cell 9(1), 50–63 (2011).
  Medline CASGoogle Scholar
• 188 Zhu Z, Hao X, Yan M et al. Cancer stem/progenitor cells are highly enriched in CD133⁺CD44⁺ population in hepatocellular carcinoma. Int. J. Cancer 126(9), 2067–2078 (2010).
  Medline CASGoogle Scholar
• 189 Yang W, Wang C, Lin Y et al. OV6+ tumor-initiating cells contribute to tumor progression and invasion in human hepatocellular carcinoma. J. Hepatol. 57(3), 613–620 (2012).
  Medline CASGoogle Scholar
• 190 Deng S, Yang X, Lassus H et al. Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS ONE 5(4), e10277 (2010).
  MedlineGoogle Scholar
• 191 Dalerba P, Dylla SJ, Park I-K et al. Phenotypic characterization of human colorectal cancer stem cells. Proc. Natl Acad. Sci. USA 104(24), 10158–10163 (2007).
  Medline CASGoogle Scholar
• 192 Y01eung TM, Gandhi SC, Wilding JL, Muschel R, Bodmer WF. Cancer stem cells from colorectal cancer-derived cell lines. Proc. Natl Acad. Sci. USA 107(8), 3722–3727 (2010).
  MedlineGoogle Scholar
• 193 Vermeulen L, Todaro M, de Sousa Mello F et al. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc. Natl Acad. Sci. USA 105(36), 13427–13432 (2008).
  Medline CASGoogle Scholar
• 194 Singh SK, Hawkins C, Clarke ID et al. Identification of human brain tumour initiating cells. Nature 432(7015), 396–401 (2004).
  Medline CASGoogle Scholar
• 195 Tchoghandjian A, Baeza N, Colin C et al. A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathol. 20(1), 211–221 (2010).
  MedlineGoogle Scholar
• 196 Read T-A, Fogarty MP, Markant SL et al. Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell 15(2), 135–147 (2009).
  Medline CASGoogle Scholar
• 197 Welte Y, Davies C, Schä;fer R, Regenbrecht CRA. Patient derived cell culture and isolation of CD133⁺ putative cancer stem cells from melanoma. J. Vis. Exp. 73, e50200 (2013).
  Google Scholar
• 198 Fang D, Nguyen TK, Leishear K et al. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 65(20), 9328–9337 (2005).
  Medline CASGoogle Scholar
• 199 Tirino V, Desiderio V, Paino F et al. Human primary bone sarcomas contain CD133+ cancer stem cells displaying high tumorigenicity in vivo. FASEB J. 25(6), 2022–2030 (2011).
  Medline CASGoogle Scholar
• 200 Adhikari AS, Agarwal N, Wood BM et al. CD117 and Stro-1 identify osteosarcoma tumor-initiating cells associated with metastasis and drug resistance. Cancer Res. 70(11), 4602–4612 (2010).
  Medline CASGoogle Scholar