263
Views
22
CrossRef citations to date
0
Altmetric
Original Article

The effect of transferrin-targeted, resveratrol-loaded liposomes on neurosphere cultures of glioblastoma: implications for targeting tumour-initiating cells

, &
Pages 601-613 | Received 15 Sep 2018, Accepted 16 Nov 2018, Published online: 04 Dec 2018

References

  • Ostrom QT, Gittleman H, Liao P, et al. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007–2011. Neuro Oncol. 2014;16:iv1–i63.
  • Huse JT, Holland EC. Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer. 2010;10:319–331.
  • Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821–5828.
  • Hemmati HD, Nakano I, Lazareff JA, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA. 2003;100:15178–15183.
  • Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401.
  • Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004;64:7011–7021.
  • Ignatova TN, Kukekov VG, Laywell ED, et al. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia. 2002;39:193–206.
  • Venere M, Fine HA, Dirks PB, et al. Cancer stem cells in gliomas: identifying and understanding the apex cell in cancer’s hierarchy. Glia. 2011;59:1148–1154.
  • Ahmed AU, Auffinger B, Lesniak MS. Understanding glioma stem cells: rationale, clinical relevance and therapeutic strategies. Expert Rev Neurother. 2013;13:545–555.
  • Dirks PB. Brain tumor stem cells: bringing order to the chaos of brain cancer. J Clin Oncol. 2008;26:2916–2924.
  • Bao S, Wu Q, Li Z, et al. Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Res. 2008;68:6043–6048.
  • Lathia JD, Gallagher J, Heddleston JM, et al. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell. 2010;6 421–432.
  • Ogden AT, Waziri AE, Lochhead RA, et al. Identification of A2B5 + CD133-tumor-initiating cells in adult human gliomas. Neurosurgery. 2008;62:505–514; discussion 514–515.
  • Iacopino F, Angelucci C, Piacentini R, et al. Isolation of cancer stem cells from three human glioblastoma cell lines: characterization of two selected clones. PLoS One. 2014;9:e105166.
  • Kang SK, Park JB, Cha SH. Multipotent, dedifferentiated cancer stem-like cells from brain gliomas. Stem Cells Dev. 2006;15:423–435.
  • Kondo T, Setoguchi T, Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA. 2004;101:781–786.
  • Qiang L, Yang Y, Ma YJ, et al. Isolation and characterization of cancer stem like cells in human glioblastoma cell lines. Cancer Lett. 2009;279:13–21.
  • Yu SC, Ping YF, Yi L, et al. Isolation and characterization of cancer stem cells from a human glioblastoma cell line U87. Cancer Lett. 2008;265:124–134.
  • Rich JN, Bao S. Chemotherapy and cancer stem cells. Cell Stem Cell. 2007;1:353–355.
  • Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–760.
  • Kitange GJ, Carlson BL, Schroeder MA, et al. Induction of MGMT expression is associated with temozolomide resistance in glioblastoma xenografts. Neuro Oncol. 2009;11:281–291.
  • Neves AR, Lucio M, Lima JL, et al. Resveratrol in medicinal chemistry: a critical review of its pharmacokinetics, drug-delivery, and membrane interactions. CMC. 2012;19:1663–1681.
  • Jang M, Cai L, Udeani GO, et al. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science. 1997;275:218–220.
  • Yang Y-P, Chang Y-L, Huang P-I, et al. Resveratrol suppresses tumorigenicity and enhances radiosensitivity in primary glioblastoma tumor initiating cells by inhibiting the STAT3 axis. J Cell Physiol. 2012;227:976–993.
  • Castino R, Pucer A, Veneroni R, et al. Resveratrol reduces the invasive growth and promotes the acquisition of a long-lasting differentiated phenotype in human glioblastoma cells. J Agric Food Chem. 2011;59:4264–4272.
  • Sato A, Okada M, Shibuya K, et al. Resveratrol promotes proteasome-dependent degradation of Nanog via p53 activation and induces differentiation of glioma stem cells. Stem Cell Res. 2013;11:601–610.
  • Filippi-Chiela EC, Villodre ES, Zamin LL, et al. Autophagy interplay with apoptosis and cell cycle regulation in the growth inhibiting effect of resveratrol in glioma cells. PLoS One. 2011;6:e20849.
  • Cilibrasi C, Riva G, Romano G, et al. Resveratrol impairs glioma stem cells proliferation and motility by modulating the Wnt signaling pathway. PLoS One. 2017;12:e0169854.
  • Clark PA, Bhattacharya S, Elmayan A, et al. Resveratrol targeting of AKT and p53 in glioblastoma and glioblastoma stem-like cells to suppress growth and infiltration. J Neurosurg. 2016;126:1448–1460.
  • Jiao Y, Li H, Liu Y, et al. Resveratrol inhibits the invasion of glioblastoma-initiating cells via down-regulation of the PI3K/Akt/NF-kappaB signaling pathway. Nutrients. 2015;7:4383–4402.
  • Walle T, Hsieh F, DeLegge MH, et al. High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab Dispos. 2004;32:1377–1382.
  • Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov. 2006;5:493–506.
  • Singh M. Transferrin as a targeting ligand for liposomes and anticancer drugs. Curr Pharm Des. 1999;5:443–451.
  • Daniels TR, Delgado T, Rodriguez JA, et al. The transferrin receptor part I: biology and targeting with cytotoxic antibodies for the treatment of cancer. Clin Immunol. 2006;121:144–158.
  • Calzolari A, Larocca LM, Deaglio S, et al. Transferrin receptor 2 is frequently and highly expressed in glioblastomas. Transl Oncol. 2010;3:123–134.
  • Kim SS, Rait A, Rubab F, et al. The clinical potential of targeted nanomedicine: delivering to cancer stem-like cells. Mol Ther. 2014;22:278–291.
  • Schonberg DL, Miller TE, Wu Q, et al. Preferential iron trafficking characterizes glioblastoma stem-like cells. Cancer Cell. 2015;28:441–455.
  • Vijayakumar MR, Vajanthri KY, Balavigneswaran CK, et al. Pharmacokinetics, biodistribution, in vitro cytotoxicity and biocompatibility of vitamin E TPGS coated trans resveratrol liposomes. Colloids Surf B Biointerfaces. 2016;145:479–491.
  • Guo W, Li A, Jia Z, et al. Transferrin modified PEG–PLA-resveratrol conjugates: in vitro and in vivo studies for glioma. Eur J Pharmacol. 2013;718:41–47.
  • Jhaveri A, Deshpande P, Pattni B, et al. Transferrin-targeted, resveratrol-loaded liposomes for the treatment of glioblastoma. J Control Release. 2018;277:89–101.
  • Torchilin VP, Levchenko TS, Lukyanov AN, et al. p-Nitrophenylcarbonyl-PEG-PE-liposomes: fast and simple attachment of specific ligands, including monoclonal antibodies, to distal ends of PEG chains via p-nitrophenylcarbonyl groups. Biochim Biophys Acta. 2001;1511:397–411.
  • Allen TM, Sapra P, Moase E. Use of the post-insertion method for the formation of ligand-coupled liposomes. Cell Mol Biol Lett. 2002;7:217–219.
  • Lee J, Kotliarova S, Kotliarov Y, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006;9:391–403.
  • Bez A, Corsini E, Curti D, et al. Neurosphere and neurosphere-forming cells: morphological and ultrastructural characterization. Brain Res. 2003;993:18–29.
  • McKay R. Stem cells in the central nervous system. Science. 1997;276:66–71.
  • Nakano I, Kornblum HI. Methods for analysis of brain tumor stem cell and neural stem cell self-renewal. In: Yu JS, editor. Cancer stem cells. Methods in molecular biology (Methods and protocols). Vol. 568. New York, NY: Humana Press; 2009. p. 37–56.
  • Jiang H, Zhang L, Kuo J, et al. Resveratrol-induced apoptotic death in human U251 glioma cells. Mol Cancer Ther. 2005;4:554–561.
  • Pozo-Guisado E, Merino JM, Mulero-Navarro S, et al. Resveratrol-induced apoptosis in MCF-7 human breast cancer cells involves a caspase-independent mechanism with downregulation of Bcl-2 and NF-kappaB. Int J Cancer. 2005;115:74–84.
  • Liu B, Zhou Z, Zhou W, et al. Resveratrol inhibits proliferation in human colorectal carcinoma cells by inducing G1/S phase cell cycle arrest and apoptosis through caspase/cyclin CDK pathways. Mol Med Rep. 2014;10:1697–1702.
  • Kumar S, Eroglu E, Stokes JA, 3rd, et al. Resveratrol induces mitochondria-mediated, caspase-independent apoptosis in murine prostate cancer cells. Oncotarget. 2017;8:20895–20908.
  • Lang F, Qin Z, Li F, et al. Apoptotic cell death induced by resveratrol is partially mediated by the autophagy pathway in human ovarian cancer cells. PLoS One. 2015;10:e0129196.
  • Hsu KF, Wu CL, Huang SC, et al. Cathepsin L mediates resveratrol-induced autophagy and apoptotic cell death in cervical cancer cells. Autophagy. 2009;5:451–460.
  • Delmas D, Rebe C, Lacour S, et al. Resveratrol-induced apoptosis is associated with Fas redistribution in the rafts and the formation of a death-inducing signaling complex in colon cancer cells. J Biol Chem. 2003;278:41482–41490.
  • Chen J, Li Y, Yu TS, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 2012;488:522–526.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.