Functionalised nanomaterials for eradication of CSCs, a promising approach for overcoming tumour heterogeneity

References

• Burrell RA, Swanton C. Tumour heterogeneity and the evolution of polyclonal drug resistance. Mol Oncol. 2014;8:1095–1111.
   PubMed Web of Science ®Google Scholar
• Marusyk A, Polyak K. Tumor heterogeneity: causes and consequences. Biochim Biophys Acta. 2010;1805:105–117.
   PubMed Web of Science ®Google Scholar
• Burrell RA, McGranahan N, Bartek J, et al. The causes and consequences of genetic heterogeneity in cancer evolution. Nature. 2013;501:338.
   PubMed Web of Science ®Google Scholar
• Gerdes MJ, Sood A, Sevinsky C, et al. Emerging understanding of multiscale tumor heterogeneity. Front Oncol. 2014;4:366. doi: 10.3389/fonc.2014.00366
   PubMedGoogle Scholar
• Michor F, Polyak K. The origins and implications of intratumor heterogeneity. Cancer Prev Res (Phila). 2010;3:1361–1364.
   PubMed Web of Science ®Google Scholar
• Bruce WR, Van Der Gaag H. A quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo. Nature. 1963;199:79–80.
   PubMed Web of Science ®Google Scholar
• Hewitt H. Studies of the dissemination and quantitative transplantation of a lymphocytic leukaemia of CBA mice. Br J Cancer. 1958;12:378.
   PubMed Web of Science ®Google Scholar
• Fidler IJ, Kripke ML. Metastasis results from preexisting variant cells within a malignant tumor. Science. 1977;197:893–895.
   PubMed Web of Science ®Google Scholar
• Sottoriva A, Spiteri I, Piccirillo SGM, et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci. 2013;110:4009–4014.
   PubMed Web of Science ®Google Scholar
• Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366:883–892.
   PubMed Web of Science ®Google Scholar
• Anderson ARA, Weaver AM, Cummings PT, et al. Tumor morphology and phenotypic evolution driven by selective pressure from the microenvironment. Cell. 2006;127:905–915.
   PubMed Web of Science ®Google Scholar
• Sottoriva A, Verhoeff JJC, Borovski T, et al. Cancer stem cell tumor model reveals invasive morphology and increased phenotypical heterogeneity. Cancer Res. 2010;70:46–56.
   PubMed Web of Science ®Google Scholar
• Waclaw B, Bozic I, Pittman ME, et al. A spatial model predicts that dispersal and cell turnover limit intratumour heterogeneity. Nature. 2015;525:261–264.
   PubMed Web of Science ®Google Scholar
• Gupta PB, Onder TT, Jiang G, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009;138:645–659.
   PubMed Web of Science ®Google Scholar
• Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730–737.
   PubMed Web of Science ®Google Scholar
• Clevers H. The cancer stem cell: premises, promises and challenges. Nature Med. 2011;17:313–319.
   PubMed Web of Science ®Google Scholar
• Medema JP. Cancer stem cells: the challenges ahead. Nat Cell Biol. 2013;15:338–344.
   PubMed Web of Science ®Google Scholar
• Meacham CE, Morrison SJ. Tumour heterogeneity and cancer cell plasticity. Nature. 2013;501:328.
   PubMed Web of Science ®Google Scholar
• Melo FDSE, Vermeulen L, Fessler E, et al. Cancer heterogeneity—a multifaceted view. EMBO Rep. 2013;14:686–695.
   PubMed Web of Science ®Google Scholar
• Campbell LL, Polyak K. Breast tumor heterogeneity: cancer stem cells or clonal evolution? Cell Cycle. 2007;6:2332–2338.
   PubMed Web of Science ®Google Scholar
• Nowell PC. Mechanisms of tumor progression. Cancer Res. 1986;46:2203–2207.
   PubMed Web of Science ®Google Scholar
• Baylin SB, Jones PA. A decade of exploring the cancer epigenome—biological and translational implications. Nat Rev Cancer. 2011;11:726–734.
   PubMed Web of Science ®Google Scholar
• Polyak K, Haviv I, Campbell IG. Co-evolution of tumor cells and their microenvironment. Trends Genet. 2009;25:30–38.
   PubMed Web of Science ®Google Scholar
• Bissell MJ, Hines WC. Why don’t we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med. 2011;17:320–329.
   PubMed Web of Science ®Google Scholar
• Dick JE. Stem cell concepts renew cancer research. Blood. 2008;112:4793–4807.
   PubMed Web of Science ®Google Scholar
• Shackleton M, Quintana E, Fearon ER, et al. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell. 2009;138:822–829.
   PubMed Web of Science ®Google Scholar
• Chang JC. Cancer stem cells: role in tumor growth, recurrence, metastasis, and treatment resistance. Medicine. 2016;95:S20–S25.
   PubMed Web of Science ®Google Scholar
• Cojoc M, Mäbert K, Muders MH, et al. A role for cancer stem cells in therapy resistance: cellular and molecular mechanisms. Semin Cancer Biol. 2015;31:16–27.
   Google Scholar
• Wang A, Chen L, Li C, et al. Heterogeneity in cancer stem cells. Cancer Lett. 2015;357:63–68.
   PubMed Web of Science ®Google Scholar
• Albini A, Bruno A, Gallo C, et al. Cancer stem cells and the tumor microenvironment: interplay in tumor heterogeneity. Connect Tissue Res. 2015;56:414–425.
   PubMed Web of Science ®Google Scholar
• Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell. 2012;10:717–728.
   PubMed Web of Science ®Google Scholar
• Suvà ML, Riggi N, Bernstein BE. Epigenetic reprogramming in cancer. Science. 2013;339:1567–1570.
   PubMed Web of Science ®Google Scholar
• Korkaya H, Liu S, Wicha MS. Breast cancer stem cells, cytokine networks, and the tumor microenvironment. J Clin Invest. 2011;121:3804–3809.
   PubMed Web of Science ®Google Scholar
• Tang DG. Understanding cancer stem cell heterogeneity and plasticity. Cell Res. 2012;22:457–472.
   PubMed Web of Science ®Google Scholar
• Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci. 2003;100:3983–3988.
   PubMed Web of Science ®Google Scholar
• Cabrera MC, Hollingsworth RE, Hurt EM. Cancer stem cell plasticity and tumor hierarchy. World J Stem Cells. 2015;7:27–36.
   PubMed Web of Science ®Google Scholar
• Brodsky AS, Fischer A, Miller DH, et al. Expression profiling of primary and metastatic ovarian tumors reveals differences indicative of aggressive disease. PLoS One. 2014;9:e94476.
   PubMed Web of Science ®Google Scholar
• Mullighan CG, Phillips LA, Su X, et al. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science. 2008;322:1377–1380.
   PubMed Web of Science ®Google Scholar
• Zuna J. TEL deletion analysis supports a novel view of relapse in childhood acute lymphoblastic leukemia. Clin Cancer Res. 2004;10:5355–5360.
   PubMed Web of Science ®Google Scholar
• Ma XJ, Salunga R, Tuggle JT, et al. Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci USA. 2003;100:5974–5979.
   PubMed Web of Science ®Google Scholar
• Weigelt B, Glas AM, Wessels LFA, et al. Gene expression profiles of primary breast tumors maintained in distant metastases. Proc Natl Acad Sci. 2003;100:15901–15905.
   PubMed Web of Science ®Google Scholar
• Muñoz P, Iliou MS, Esteller M. Epigenetic alterations involved in cancer stem cell reprogramming. Mol Oncol. 2012;6:620–636.
   PubMed Web of Science ®Google Scholar
• Barabé F, Kennedy JA, Hope KJ, et al. Modeling the initiation and progression of human acute leukemia in mice. Science. 2007;316:600–604.
   PubMed Web of Science ®Google Scholar
• Fearon ER, Burke PJ, Schiffer CA, et al. Differentiation of leukemia cells to polymorphonuclear leukocytes in patients with acute nonlymphocytic leukemia. N Engl J Med. 1986;315:15–24.
   PubMed Web of Science ®Google Scholar
• Illmensee K, Mintz B. Totipotency and normal differentiation of single teratocarcinoma cells cloned by injection into blastocysts. Proc Natl Acad Sci. 1976;73:549–553.
   PubMed Web of Science ®Google Scholar
• Yamazaki J, Estecio MR, Lu Y, et al. The epigenome of AML stem and progenitor cells. Epigenetics. 2013;8:92–104.
   PubMed Web of Science ®Google Scholar
• Rheinbay E, Suvà ML, Gillespie SM, et al. An aberrant transcription factor network essential for Wnt signaling and stem cell maintenance in glioblastoma. Cell Rep. 2013;3:1567–1579.
   PubMed Web of Science ®Google Scholar
• Easwaran H, Tsai HC, Baylin SB. Cancer epigenetics: tumor heterogeneity, plasticity of stem-like states, and drug resistance. Mol Cell. 2014;54:716–727.
   PubMed Web of Science ®Google Scholar
• Sun T, Zhang YS, Pang B, et al. Engineered nanoparticles for drug delivery in cancer therapy. Angew Chem Int Edn. 2014;53:12320–12364.
   PubMed Web of Science ®Google Scholar
• Maeda H, Nakamura H, Fang J. The EPR effect for macromolecular drug delivery to solid tumors: Improvement of tumor uptake, lowering of systemic toxicity, and distinct tumor imaging in vivo. Adv Drug Deliv Rev. 2013;65:71–79.
   PubMed Web of Science ®Google Scholar
• Gao Z, Zhang L, Sun Y. Nanotechnology applied to overcome tumor drug resistance. J Control Release. 2012;162:45–55.
   PubMed Web of Science ®Google Scholar
• Xia P. Surface markers of cancer stem cells in solid tumors. Curr Stem Cell Res Ther. 2014;9:102–111.
   PubMed Web of Science ®Google Scholar
• Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell. 2010;7:150–161.
   PubMed Web of Science ®Google Scholar
• Markman JL, Rekechenetskiy A, Holler E, et al. Nanomedicine therapeutic approaches to overcome cancer drug resistance. Adv Drug Deliv Rev. 2013;65:1866–1879.
   PubMed Web of Science ®Google Scholar
• Livney YD, Assaraf YG. Rationally designed nanovehicles to overcome cancer chemoresistance. Adv Drug Deliv Rev. 2013;65:1716–1730.
   PubMed Web of Science ®Google Scholar
• Hu Y, Fu L. Targeting cancer stem cells: a new therapy to cure cancer patients. Am J Cancer Res. 2012;2:340.
   PubMed Web of Science ®Google Scholar
• Davis ME, Chen Z(G), Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov. 2008;7:771.
   PubMed Web of Science ®Google Scholar
• Toole BP. Hyaluronan-CD44 interactions in cancer: paradoxes and possibilities. Clin Cancer Res. 2009;15:7462–7468.
   PubMed Web of Science ®Google Scholar
• Wei X, Senanayake TH, Warren G, et al. Hyaluronic acid-based nanogel–drug conjugates with enhanced anticancer activity designed for the targeting of CD44-positive and drug-resistant tumors. Bioconjugate Chem. 2013;24:658–668.
   PubMed Web of Science ®Google Scholar
• Wang K, Zhang T, Liu L, et al. Novel micelle formulation of curcumin for enhancing antitumor activity and inhibiting colorectal cancer stem cells. Int J Nanomed. 2012;7:4487.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Yang J, Kopeček J. Selective inhibitory effect of HPMA copolymer-cyclopamine conjugate on prostate cancer stem cells. Biomaterials. 2012;33:1863–1872.
   PubMed Web of Science ®Google Scholar
• Vinogradov S, Wei X. Cancer stem cells and drug resistance: the potential of nanomedicine. Nanomedicine (Lond). 2012;7:597–615.
   PubMed Web of Science ®Google Scholar
• Yang C, Xiong F, Wang J, et al. Anti-ABCG2 monoclonal antibody in combination with paclitaxel nanoparticles against cancer stem-like cell activity in multiple myeloma. Nanomedicine. 2014;9:45–60.
   PubMed Web of Science ®Google Scholar
• Sun TM, Wang YC, Wang F, et al. Cancer stem cell therapy using doxorubicin conjugated to gold nanoparticles via hydrazone bonds. Biomaterials. 2014;35:836–845.
   PubMed Web of Science ®Google Scholar
• Sun X, Jiao X, Pestell TG, et al. MicroRNAs and cancer stem cells: the sword and the shield. Oncogene. 2014;33:4967–4977.
   PubMed Web of Science ®Google Scholar
• Ji Q, Hao X, Zhang M, et al. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One. 2009;4:e6816.
   PubMed Web of Science ®Google Scholar
• Liu C, Kelnar K, Liu B, et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 2011;17:211–215.
   PubMed Web of Science ®Google Scholar
• Li Y, Guessous F, Zhang Y, et al. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res. 2009;69:7569–7576.
   PubMed Web of Science ®Google Scholar
• Shi S, Han L, Gong T, et al. Systemic delivery of microRNA-34a for cancer stem cell therapy. Angew Chem Int Ed Engl. 2013;52:3901–3905.
   PubMed Web of Science ®Google Scholar
• Yang YP, Chien Y, Chiou GY, et al. Inhibition of cancer stem cell-like properties and reduced chemoradioresistance of glioblastoma using microRNA145 with cationic polyurethane-short branch PEI. Biomaterials. 2012;33:1462–1476.
   PubMed Web of Science ®Google Scholar
• Piao L, Zhang M, Datta J, et al. Lipid-based nanoparticle delivery of Pre-miR-107 inhibits the tumorigenicity of head and neck squamous cell carcinoma. Mol Ther. 2012;20:1261–1269.
   PubMed Web of Science ®Google Scholar
• Williford JM, Wu J, Ren Y, et al. Recent advances in nanoparticle-mediated siRNA delivery. Annu Rev Biomed Eng. 2014;16:347–370.
   PubMed Web of Science ®Google Scholar
• Andey T, Marepally S, Patel A, et al. Cationic lipid guided short-hairpin RNA interference of annexin A2 attenuates tumor growth and metastasis in a mouse lung cancer stem cell model. J Controlled Release. 2014;184:67–78.
   PubMed Web of Science ®Google Scholar
• Xu C-F, Liu Y, Shen S, et al. Targeting glucose uptake with siRNA-based nanomedicine for cancer therapy. Biomaterials. 2015;51:1–11.
   PubMed Web of Science ®Google Scholar
• Liu C, Zhao G, Liu J, et al. Novel biodegradable lipid nano complex for siRNA delivery significantly improving the chemosensitivity of human colon cancer stem cells to paclitaxel. J Controlled Release. 2009;140:277–283.
   PubMed Web of Science ®Google Scholar
• Kobayashi CI, Suda T. Regulation of reactive oxygen species in stem cells and cancer stem cells. J Cell Physiol. 2012;227:421–430.
   PubMed Web of Science ®Google Scholar
• Ishimoto T, Nagano O, Yae T, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc − and thereby promotes tumor growth. Cancer Cell. 2011;19:387–400.
   PubMed Web of Science ®Google Scholar
• Moon EJ, Sonveaux P, Porporato PE, et al. NADPH oxidase-mediated reactive oxygen species production activates hypoxia-inducible factor-1 (HIF-1) via the ERK pathway after hyperthermia treatment. Proc Natl Acad Sci. 2010;107:20477–20482.
   PubMed Web of Science ®Google Scholar
• Vujaskovic Z, Rosen EL, Blackwell KL, et al. Ultrasound guided pO2 measurement of breast cancer reoxygenation after neoadjuvant chemotherapy and hyperthermia treatment. Int J Hyperthermia. 2003;19:498–506.
   PubMed Web of Science ®Google Scholar
• Vujaskovic Z, Song C. Physiological mechanisms underlying heat-induced radiosensitization. Int J Hyperthermia. 2004;20:163–174.
   PubMed Web of Science ®Google Scholar
• Zhang L, Yao HJ, Yu Y, et al. Mitochondrial targeting liposomes incorporating daunorubicin and quinacrine for treatment of relapsed breast cancer arising from cancer stem cells. Biomaterials. 2012;33:565–582.
   PubMed Web of Science ®Google Scholar
• Sadhukha T, Niu L, Wiedmann TS, et al. Effective elimination of cancer stem cells by magnetic hyperthermia. Mol Pharmaceutics. 2013;10:1432–1441.
   PubMed Web of Science ®Google Scholar
• Domenech M, Marrero-Berrios I, Torres-Lugo M, et al. Lysosomal membrane permeabilization by targeted magnetic nanoparticles in alternating magnetic fields. ACS Nano. 2013;7:5091–5101.
   PubMed Web of Science ®Google Scholar
• 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. 2012;33:2961–2970.
   PubMed Web of Science ®Google Scholar
• Li SY, Sun R, Wang HX, et al. Combination therapy with epigenetic-targeted and chemotherapeutic drugs delivered by nanoparticles to enhance the chemotherapy response and overcome resistance by breast cancer stem cells. J Controlled Release. 2015;205:7–14.
   PubMed Web of Science ®Google Scholar
• Hong IS, Jang GB, Lee HY, et al. Targeting cancer stem cells by using the nanoparticles. Int J Nanomedicine. 2015;10:251.
   PubMed Web of Science ®Google Scholar
• Jain A, Jain SK. In vitro and cell uptake studies for targeting of ligand anchored nanoparticles for colon tumors. Eur J Pharm Sci. 2008;35:404–416.
   PubMed Web of Science ®Google Scholar
• 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. 2011;19:1538–1546.
   PubMed Web of Science ®Google Scholar
• Liu P, Wang Z, Brown S, et al. Liposome encapsulated Disulfiram inhibits NFκB pathway and targets breast cancer stem cells in vitro and in vivo. Oncotarget. 2014;5:7471.
   PubMed Web of Science ®Google Scholar
• Wang J, Sefah K, Altman MB, et al. Aptamer‐conjugated nanorods for targeted photothermal therapy of prostate cancer stem cells. Chem Asian J. 2013;8:2417–2422.
   PubMed Web of Science ®Google Scholar
• Yao HJ, Zhang YG, Sun L, et al. The effect of hyaluronic acid functionalized carbon nanotubes loaded with salinomycin on gastric cancer stem cells. Biomaterials. 2014;35:9208–9223.
   PubMed Web of Science ®Google Scholar
• Liu J, Meng T, Yuan M, et al. MicroRNA-200c delivered by solid lipid nanoparticles enhances the effect of paclitaxel on breast cancer stem cell. Int J Nanomedicine. 2016;11:6713.
   PubMed Web of Science ®Google Scholar
• Chiou GY, Cherng JY, Hsu HS, et al. Cationic polyurethanes-short branch PEI-mediated delivery of Mir145 inhibited epithelial–mesenchymal transdifferentiation and cancer stem-like properties and in lung adenocarcinoma. J Controlled Release. 2012;159:240–250.
   PubMed Web of Science ®Google Scholar
• Gul-Uludağ H, Valencia-Serna J, Kucharski C, et al. Polymeric nanoparticle-mediated silencing of CD44 receptor in CD34+ acute myeloid leukemia cells. Leukemia Res. 2014;38:1299–1308.
   PubMed Web of Science ®Google Scholar
• Lo WL, Chien Y, Chiou GY, et al. Nuclear localization signal-enhanced RNA interference of EZH2 and Oct4 in the eradication of head and neck squamous cell carcinoma-derived cancer stem cells. Biomaterials. 2012;33:3693–3709.
   PubMed Web of Science ®Google Scholar