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Review

Novel Therapeutics and drug-delivery Approaches in the Modulation of Glioblastoma Stem Cell Resistance

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 249-273 | Received 27 Nov 2021, Accepted 04 May 2022, Published online: 26 May 2022

References

  • Singh SK , HawkinsC , ClarkeIDet al. Identification of human brain tumour initiating cells. Nature432(7015), 396–401 (2004).
  • Vasilev A , SofiR , TongL , TeschemacherAG , KasparovS. In search of a breakthrough therapy for glioblastoma. Neuroglia1(2), 292–310 (2018).
  • Miller KD , OstromQT , KruchkoCet al. Brain and other central nervous system tumor statistics, 2021. CA Cancer J. Clin.71(5), 381–406 (2021).
  • Alphandery E . Glioblastoma treatments: an account of recent industrial developments. Front. Pharmacol.9, 879 (2018).
  • Urbańska K , SokołowskaJ , SzmidtM , SysaP. Glioblastoma multiforme - an overview. Contemp. Oncol. (Poznan, Poland)18(5), 307–312 (2014).
  • Davis ME . Glioblastoma: overview of disease and treatment. Clin. J. Oncol. Nurs.20(Suppl. 5), S2–S8 (2016).
  • The Huntington's Disease Collaborative Research Group . A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell72(6), 971–983 (1993).
  • Gimple RC , BhargavaS , DixitD , RichJN. Glioblastoma stem cells: lessons from the tumor hierarchy in a lethal cancer. Genes Dev.33(11–12), 591–609 (2019).
  • Wang Q , HuB , HuXet al. Tumor evolution of glioma-intrinsic gene expression subtypes associates with immunological changes in the microenvironment. Cancer Cell32(1), 42–56.e46 (2017).
  • Walid MS . Prognostic factors for long-term survival after glioblastoma. Permanente J.12(4), 45–48 (2008).
  • Pourgholi F , HajivaliliM , FarhadJN , KafilHS , YousefiM. Nanoparticles: novel vehicles in treatment of Glioblastoma. Biomed. Pharmacother.77, 98–107 (2016).
  • Van Den Bent MJ , WellerM , WenPY , KrosJM , AldapeK , ChangS. A clinical perspective on the 2016 WHO brain tumor classification and routine molecular diagnostics. Neuro-oncology19(5), 614–624 (2017).
  • Songtao Q , LeiY , SiGet al. IDH mutations predict longer survival and response to temozolomide in secondary glioblastoma. Cancer Sci.103(2), 269–273 (2012).
  • Chen X , ZhangM , GanHet al. A novel enhancer regulates MGMT expression and promotes temozolomide resistance in glioblastoma. Nat. Commun.9(1), 1–14 (2018).
  • Hsu JB , ChangTH , LeeGA , LeeTY , ChenCY. Identification of potential biomarkers related to glioma survival by gene expression profile analysis. BMC Med. Genom.11(Suppl. 7), 34 (2019).
  • Stupp R , MasonWP , VanDen Bent MJet al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N England J. Med.352(10), 987–996 (2005).
  • Stupp R , TaillibertS , KannerAet al. Effect of tumor-treating fields plus maintenance temozolomide vs maintenance temozolomide alone on survival in patients with glioblastoma: a randomized clinical trial. JAMA318(23), 2306–2316 (2017).
  • Gramatzki D , RothP , RushingEJet al. Bevacizumab may improve quality of life, but not overall survival in glioblastoma: an epidemiological study. Ann. Oncol.29(6), 1431–1436 (2018).
  • Roth P , WinklhoferS , MüllerAMet al. Neurological complications of cancer immunotherapy. Cancer Treat. Rev.97, 102189 (2021).
  • Chinot OL , WickW , MasonWet al. Bevacizumab plus radiotherapy–temozolomide for newly diagnosed glioblastoma. N. Engl. J. Med.370(8), 709–722 (2014).
  • Lapidot T , SirardC , VormoorJet al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature367(6464), 645–648 (1994).
  • Lathia JD , MackSC , Mulkearns-HubertEE , ValentimCL , RichJN. Cancer stem cells in glioblastoma. Genes Development29(12), 1203–1217 (2015).
  • Yang L , ShiP , ZhaoGet al. Targeting cancer stem cell pathways for cancer therapy. Signal Transduct. Target Ther.5(1), 8 (2020).
  • Cheng L , WuQ , GuryanovaOAet al. Elevated invasive potential of glioblastoma stem cells. Biochem. Biophys. Res. Commun.406(4), 643–648 (2011).
  • Auffinger B , SpencerD , PytelP , AhmedAU , LesniakMS. The role of glioma stem cells in chemotherapy resistance and glioblastoma multiforme recurrence. Expert. Rev. Neurother.15(7), 741–752 (2015).
  • Prager BC , BhargavaS , MahadevV , HubertCG , RichJN. Glioblastoma stem cells: driving resilience through chaos. Trends Cancer6(3), 223–235 (2020).
  • Carnero A , LleonartM. The hypoxic microenvironment: a determinant of cancer stem cell evolution. BioEssays38(Suppl. 1), S65–S74 (2016).
  • Lee JH , LeeJE , KahngJYet al. Human glioblastoma arises from subventricular zone cells with low-level driver mutations. Nature560(7717), 243–247 (2018).
  • Group BDW , AtkinsonAJJr , ColburnWAet al. Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin. Pharmacol. Therapeut.69(3), 89–95 (2001).
  • Mason S , McdonaldK. MGMT testing for glioma in clinical laboratories: discordance with methylation analyses prevents the implementation of routine immunohistochemistry. J. Cancer Res. Clin. Oncol.138(11), 1789–1797 (2012).
  • Batlle E , CleversH. Cancer stem cells revisited. Nat. Med.23(10), 1124–1134 (2017).
  • Alison MR , LimSM , NicholsonLJ. Cancer stem cells: problems for therapy?J. Pathol.223(2), 147–161 (2011).
  • Karsten U , GoletzS. What makes cancer stem cell markers different?Springerplus2(1), 301 (2013).
  • Si D , YinF , PengJ , ZhangG. High expression of CD44 predicts a poor prognosis in glioblastomas. Cancer Manag. Res.12, 769–775 (2020).
  • Mao XG , ZhangX , XueXYet al. Brain tumor stem-like cells identified by neural stem cell marker CD15. Transl. Oncol.2(4), 247–257 (2009).
  • Lee HJ , ChoeG , JheonS , SungSW , LeeCT , ChungJH. CD24, a novel cancer biomarker, predicting disease-free survival of non-small cell lung carcinomas: a retrospective study of prognostic factor analysis from the viewpoint of forthcoming (seventh) new TNM classification. J. Thorac. Oncol.5(5), 649–657 (2010).
  • Shaikh MV , KalaM , NivsarkarM. CD90 a potential cancer stem cell marker and a therapeutic target. Cancer Biomark.16(3), 301–307 (2016).
  • Lathia JD , GallagherJ , HeddlestonJMet al. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell6(5), 421–432 (2010).
  • Zheng X , XieQ , LiS , ZhangW. CXCR4-positive subset of glioma is enriched for cancer stem cells. Oncol. Res.19(12), 555–561 (2011).
  • Raveh S , GavertN , Ben-Ze'evA. L1 cell adhesion molecule (L1CAM) in invasive tumors. Cancer Lett.282(2), 137–145 (2009).
  • Li Y , WangZ , AjaniJA , SongS. Drug resistance and cancer stem cells. Cell Commun. Signal.19(1), 19 (2021).
  • Neradil J , VeselskaR. Nestin as a marker of cancer stem cells. Cancer Sci.106(7), 803–811 (2015).
  • Glazer RI , WangXY , YuanH , YinY. Musashi1: a stem cell marker no longer in search of a function. Cell Cycle7(17), 2635–2639 (2008).
  • Rasper M , SchaferA , PiontekGet al. Aldehyde dehydrogenase 1 positive glioblastoma cells show brain tumor stem cell capacity. Neuro. Oncol.12(10), 1024–1033 (2010).
  • Gupta MK , PolisettyRV , SharmaRet al. Altered transcriptional regulatory proteins in glioblastoma and YBX1 as a potential regulator of tumor invasion. Sci. Rep.9(1), 10986 (2019).
  • Godlewski J , NewtonH , ChioccaE , LawlerS. MicroRNAs and glioblastoma; the stem cell connection. Cell Death Different.17(2), 221–228 (2010).
  • Pottoo FH , JavedMN , RahmanJU , Abu-IzneidT , KhanFA. Targeted delivery of miRNA based therapeuticals in the clinical management of Glioblastoma Multiforme. Presented at: Seminars in Cancer Biol.69, 391–398 (2021).
  • Yeh M , WangYY , YooJYet al. MicroRNA-138 suppresses glioblastoma proliferation through downregulation of CD44. Scientific Reports11(1), 1–11 (2021).
  • Galli R , BindaE , OrfanelliUet al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res.64(19), 7011–7021 (2004).
  • Joo KM , KimSY , JinXet al. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab. Invest.88(8), 808–815 (2008).
  • Glumac PM , LebeauAM. The role of CD133 in cancer: a concise review. Clin. Transl. Med.7(1), 18 (2018).
  • Ahmed SI , JavedG , LaghariAAet al. CD133 expression in glioblastoma multiforme: a literature review. Cureus10(10), e3439 (2018).
  • Galli R , BindaE , OrfanelliUet al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res.64(19), 7011–7021 (2004).
  • Behrooz AB , SyahirA. Could we address the interplay between CD133, Wnt/beta-catenin, and TERT signaling pathways as a potential target for glioblastoma therapy?Front. Oncol.11, 642719 (2021).
  • Xi G , LiYD , GrahovacGet al. Targeting CD133 improves chemotherapeutic efficacy of recurrent pediatric pilocytic astrocytoma following prolonged chemotherapy. Mol. Cancer16(1), 21 (2017).
  • Wei Y , JiangY , ZouFet al. Activation of PI3K/Akt pathway by CD133-p85 interaction promotes tumorigenic capacity of glioma stem cells. Proc. Natl Acad. Sci. USA110(17), 6829–6834 (2013).
  • Liu G , YuanX , ZengZet al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol. Cancer5, 67 (2006).
  • Beier D , WischhusenJ , DietmaierWet al. CD133 expression and cancer stem cells predict prognosis in high-grade oligodendroglial tumors. Brain Pathol.18(3), 370–377 (2008).
  • Michalczyk K , ZimanM. Nestin structure and predicted function in cellular cytoskeletal organisation. Histol. Histopathol.20(2), 665–671 (2005).
  • Matsuda Y , HagioM , IshiwataT. Nestin: a novel angiogenesis marker and possible target for tumor angiogenesis. World J. Gastroenterol.19(1), 42–48 (2013).
  • Ehrmann J , KolarZ , MokryJ. Nestin as a diagnostic and prognostic marker: immunohistochemical analysis of its expression in different tumours. J. Clin. Pathol.58(2), 222–223 (2005).
  • Tang X , ZuoC , FangPet al. Targeting glioblastoma stem cells: a review on biomarkers, signal pathways and targeted therapy. Front. Oncol.11, 701291 (2021).
  • Zhang M , SongT , YangLet al. Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients. J. Exp. Clin. Cancer Res.27(1), 85 (2008).
  • Jin X , JinX , JungJE , BeckS , KimH. Cell surface Nestin is a biomarker for glioma stem cells. Biochem. Biophys. Res. Commun.433(4), 496–501 (2013).
  • Brown DV , MantamadiotisT. Insights into the next generation of cancer stem cell research. Front. Biosci. (Landmark Ed)19, 1015–1027 (2014).
  • Anido J , Sáez-BorderíasA , Gonzàlez-JuncàAet al. TGF-β receptor inhibitors target the CD44high/Id1high glioma-initiating cell population in human glioblastoma. Cancer Cell18(6), 655–668 (2010).
  • Vaillant B , BhatK , SulmanEet al. CD44 as a prognostic and predictive marker for GBM. J. Clin. Oncol.29, 2049–2049 (2011).
  • Mooney KL , ChoyW , SidhuSet al. The role of CD44 in glioblastoma multiforme. J. Clin. Neurosci.34, 1–5 (2016).
  • Penar PL , KhoshyomnS , BhushanA , TrittonTR. Inhibition of epidermal growth factor receptor-associated tyrosine kinase blocks glioblastoma invasion of the brain: experimental studies. Neurosurgery40(1), 141–151 (1997).
  • Sato H , KuwashimaN , SakaidaTet al. Epidermal growth factor receptor-transfected bone marrow stromal cells exhibit enhanced migratory response and therapeutic potential against murine brain tumors. Cancer Gene Ther.12(9), 757–768 (2005).
  • Gomez KE , WuF , KeysarSBet al. Cancer cell CD44 mediates macrophage/monocyte-driven regulation of head and neck cancer stem cells. Cancer Res.80(19), 4185–4198 (2020).
  • Wang HH , LiaoCC , ChowNHet al. Whether CD44 is an applicable marker for glioma stem cells. Am. J. Translational Res.9(11), 4785 (2017).
  • Wei KC , HuangCY , ChenPYet al. Evaluation of the prognostic value of CD44 in glioblastoma multiforme. Anticancer Res.30(1), 253–259 (2010).
  • Nishikawa M , InoueA , OhnishiTet al. Hypoxia-induced phenotypic transition from highly invasive to less invasive tumors in glioma stem-like cells: significance of CD44 and osteopontin as therapeutic targets in glioblastoma. Translat. Oncol.14(8), 101137 (2021).
  • Qiu GZ , JinMZ , DaiJX , SunW , FengJH , JinWL. Reprogramming of the tumor in the hypoxic niche: the emerging concept and associated therapeutic strategies. Trends Pharmacol. Sci.38(8), 669–686 (2017).
  • Shi Y , LimSK , LiangQet al. Gboxin is an oxidative phosphorylation inhibitor that targets glioblastoma. Nature567(7748), 341–346 (2019).
  • Brown DV , FilizG , DanielPMet al. Expression of CD133 and CD44 in glioblastoma stem cells correlates with cell proliferation, phenotype stability and intra-tumor heterogeneity. PLoS ONE12(2), e0172791–e0172791 (2017).
  • Wang R , ChadalavadaK , WilshireJet al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature468(7325), 829–833 (2010).
  • Calabrese C , PoppletonH , KocakMet al. A perivascular niche for brain tumor stem cells. Cancer Cell11(1), 69–82 (2007).
  • Da Ros M , DeGregorio V , IorioALet al. Glioblastoma chemoresistance: the double play by microenvironment and blood-brain barrier. Int. J. Mol. Sci.19(10), 2879 (2018).
  • Di Mauro PP , CascanteA , BrugadaP , Gómez-VallejoV , LlopJ , BorrósS. Peptide-functionalized and high drug loaded novel nanoparticles as dual-targeting drug delivery system for modulated and controlled release of paclitaxel to brain glioma. Int. J. Pharmaceutics553(1), 169–185 (2018).
  • Portnow J , BadieB , ChenM , LiuA , BlanchardS , SynoldTW. The neuropharmacokinetics of temozolomide in patients with resectable brain tumors: potential implications for the current approach to chemoradiation. Clin. Cancer Res.15(22), 7092–7098 (2009).
  • Lah TT , NovakM , BreznikB. Brain malignancies: glioblastoma and brain metastases. Semin. Cancer Biol.60, 262–273 (2020).
  • Wu W , KlockowJL , ZhangMet al. Glioblastoma multiforme (GBM): an overview of current therapies and mechanisms of resistance. Pharmacol. Res.171, 105780 (2021).
  • Xiong L , WangF , QiXie X. Advanced treatment in high-grade gliomas. J. Buon.24(2), 424–430 (2019).
  • Abadi B , Ahmadi-ZeidabadiM , DiniL , VergalloC. Stem cell-based therapy treating glioblastoma multiforme. Hematol Oncol Stem Cell Ther14(1), 1–15 (2021).
  • Lee CY , OoiIH. Preparation of temozolomide-loaded nanoparticles for glioblastoma multiforme targeting-ideal versus reality. Pharmaceuticals (Basel, Switzerland)9(3), 54 (2016).
  • Fang C , WangK , StephenZRet al. Temozolomide nanoparticles for targeted glioblastoma therapy. ACS Appli. Mater. Interf.7(12), 6674–6682 (2015).
  • Emamgholizadeh Minaei S , KhoeiS , KhoeeS , KarimiMR. Tri-block copolymer nanoparticles modified with folic acid for temozolomide delivery in glioblastoma. Int. J. Biochem. Cell Biol.108, 72–83 (2019).
  • Ramalho MJ , SevinE , GosseletFet al. Receptor-mediated PLGA nanoparticles for glioblastoma multiforme treatment. Int. J. Pharm.545(1–2), 84–92 (2018).
  • Wang JB , DongDF , WangMD , GaoK. IDH1 overexpression induced chemotherapy resistance and IDH1 mutation enhanced chemotherapy sensitivity in Glioma cells in vitro and in vivo. Asian Pacific J. Cancer Prevent.15(1), 427–432 (2014).
  • Huang J , YuJ , TuL , HuangN , LiH , LuoY. Isocitrate dehydrogenase mutations in glioma: from basic discovery to therapeutics development. Front. Oncol.9, 506 (2019).
  • Glaser T , HanI , WuL , ZengX. Targeted nanotechnology in glioblastoma multiforme. Front. Pharmacol.8, 166 (2017).
  • Hegi ME , DiserensAC , GorliaTet al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N England J. Med.352(10), 997–1003 (2005).
  • Beier D , RöhrlS , PillaiDRet al. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res.68(14), 5706–5715 (2008).
  • Wang H , CaiS , BaileyBJet al. Combination therapy in a xenograft model of glioblastoma: enhancement of the antitumor activity of temozolomide by an MDM2 antagonist. J. Neurosurg.126(2), 446–459 (2017).
  • Berberich A , KesslerT , ThomeCMet al. Targeting Resistance against the MDM2 Inhibitor RG7388 in Glioblastoma Cells by the MEK Inhibitor Trametinib. Clin. Cancer Res.25(1), 253–265 (2019).
  • Wang S , ZhaoY , AguilarA , BernardD , YangCY. Targeting the MDM2-p53 protein-protein interaction for new cancer therapy: progress and challenges. Cold Spring Harb. Perspect. Med.7(5), a026245 (2017).
  • Williams AB , SchumacherB. p53 in the DNA-damage-repair process. Cold Spring Harb. Perspect. Med.6(5), a026070 (2016).
  • Jerry DJ , TaoL , YanH. Regulation of cancer stem cells by p53. Breast Cancer Res.10(4), 304 (2008).
  • Chien CH , HsuehWT , ChuangJY , ChangKY. Dissecting the mechanism of temozolomide resistance and its association with the regulatory roles of intracellular reactive oxygen species in glioblastoma. Journal of Biomedical Science28(1), 18 (2021).
  • Zhao Y , AguilarA , BernardD , WangS. Small-molecule inhibitors of the MDM2-p53 protein-protein interaction (MDM2 Inhibitors) in clinical trials for cancer treatment. J. Med. Chem.58(3), 1038–1052 (2015).
  • Zanjirband M , EdmondsonRJ , LunecJ. Pre-clinical efficacy and synergistic potential of the MDM2-p53 antagonists, Nutlin-3 and RG7388, as single agents and in combined treatment with cisplatin in ovarian cancer. Oncotarget7(26), 40115–40134 (2016).
  • Kussie PH , GorinaS , MarechalVet al. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science274(5289), 948–953 (1996).
  • Sanchez-Vega F , MinaM , ArmeniaJet al. Oncogenic signaling pathways in the Cancer Genome Atlas. Cell173(2), 321–337.e310 (2018).
  • Skalniak L , KocikJ , PolakJet al. Prolonged Idasanutlin (RG7388) treatment leads to the generation of p53-mutated cells. Cancers (Basel)10(11), 396 (2018).
  • Chen L , RousseauRF , MiddletonSAet al. Pre-clinical evaluation of the MDM2-p53 antagonist RG7388 alone and in combination with chemotherapy in neuroblastoma. Oncotarget6(12), 10207–10221 (2015).
  • Khurana A , ShaferDA. MDM2 antagonists as a novel treatment option for acute myeloid leukemia: perspectives on the therapeutic potential of idasanutlin (RG7388). Onco Targets Ther12, 2903–2910 (2019).
  • Dadi N , StanleyM , ShahdaS , O'neilBH , SehdevA. Impact of Nab-Paclitaxel-based Second-line Chemotherapy in Metastatic Pancreatic Cancer. Anticancer Res.37(10), 5533–5539 (2017).
  • Branham MT , NadinSB , Vargas-RoigLM , CioccaDR. DNA damage induced by paclitaxel and DNA repair capability of peripheral blood lymphocytes as evaluated by the alkaline comet assay. Mutation Res.560(1), 11–17 (2004).
  • Horwitz SB . Taxol (paclitaxel): mechanisms of action. Ann. Oncol.5(Suppl. 6), S3–S6 (1994).
  • Surapaneni MS , DasSK , DasNG. Designing Paclitaxel drug delivery systems aimed at improved patient outcomes: current status and challenges. ISRN Pharmacol.2012, 623139 (2012).
  • Chi EY , ViriyapakB , KwackHSet al. Regulation of paclitaxel-induced programmed cell death by autophagic induction: a model for cervical cancer. Obstetr. Gynecol. Sci.56(2), 84–92 (2013).
  • Dong R , XinL , AixiaL , BaohuiL , FengX. Paclitaxel inhibits growth and proliferation of glioblastoma through MMP-9-meidated p38/JNK signaling pathway. Biomed. Res. (0970-938X)28(17), 7348–7353 (2017).
  • Yusuf RZ , DuanZ , LamendolaDE , PensonRT , SeidenMV. Paclitaxel resistance: molecular mechanisms and pharmacologic manipulation. Curr. Cancer Drug Targets3(1), 1–19 (2003).
  • Rice A , MichaelisML , GeorgG , LiuY , TurunenB , AudusKL. Overcoming the blood-brain barrier to taxane delivery for neurodegenerative diseases and brain tumors. J, Mol. Neurosci.20(3), 339–343 (2003).
  • Yusuf RZ , DuanZ , LamendolaDE , PensonRT , SeidenMV. Paclitaxel resistance: molecular mechanisms and pharmacologic manipulation. Curr. Cancer Drug Targets3(1), 1–19 (2003).
  • Scripture CD , FiggWD , SparreboomA. Paclitaxel chemotherapy: from empiricism to a mechanism-based formulation strategy. Ther. Clin. Risk Manag.1(2), 107–114 (2005).
  • Adams JD , FloraKP , GoldspielBR , WilsonJW , ArbuckSG , FinleyR. Taxol: a history of pharmaceutical development and current pharmaceutical concerns. J. Natl Cancer Inst. Monogr. (15), 141–147 (1993).
  • Campos FC , VictorinoVJ , Martins-PingeMC , CecchiniAL , PanisC , CecchiniR. Systemic toxicity induced by paclitaxel in vivo is associated with the solvent cremophor EL through oxidative stress-driven mechanisms. Food Chem. Toxicol.68, 78–86 (2014).
  • Lidar Z , MardorY , JonasTet al. Convection-enhanced delivery of paclitaxel for the treatment of recurrent malignant glioma: a phase I/II clinical study. J. Neurosurg.100(3), 472–479 (2004).
  • Chen L , RousseauRF , MiddletonSAet al. Pre-clinical evaluation of the MDM2-p53 antagonist RG7388 alone and in combination with chemotherapy in neuroblastoma. Oncotarget6(12), 10207 (2015).
  • Xu Y , ShenM , LiYet al. The synergic antitumor effects of paclitaxel and temozolomide co-loaded in mPEG-PLGA nanoparticles on glioblastoma cells. Oncotarget7(15), 20890–20901 (2016).
  • Sørensen MD , FosmarkS , HellwegeS , BeierD , KristensenBW , BeierCP. Chemoresistance and chemotherapy targeting stem-like cells in malignant glioma. Stem Cell Biology in Neoplasms of the Central Nervous System853, 111–138 (2015).
  • Saraswathy M , GongS. Different strategies to overcome multidrug resistance in cancer. Biotechnol. Adv.31(8), 1397–1407 (2013).
  • Daneman R , PratA. The blood–brain barrier. Cold Spring Harbor Perspect. Biol.7(1), a020412 (2015).
  • Bhowmik A , KhanR , GhoshMK. Blood brain barrier: a challenge for effectual therapy of brain tumors. BioMed Res. Int.2015, 320941 (2015).
  • Pardridge WM . Drug transport across the blood–brain barrier. J Cerebral Blood Flow Metabolism32(11), 1959–1972 (2012).
  • Barua S , MitragotriS. Challenges associated with penetration of nanoparticles across cell and tissue barriers: a review of current status and future prospects. Nano Today9(2), 223–243 (2014).
  • Haseloff RF , DithmerS , WinklerL , WolburgH , BlasigIE. Transmembrane proteins of the tight junctions at the blood–brain barrier: structural and functional aspects. Presented at: Seminars in Cell & Developmental Biology.38, 16–25 (2015).
  • Mosquera J , GarcíaI , Liz-MarzánLM. Cellular uptake of nanoparticles versus small molecules: a matter of size. Acc. Chem. Res.51(9), 2305–2313 (2018).
  • Abbott NJ , PatabendigeAA , DolmanDE , YusofSR , BegleyDJ. Structure and function of the blood–brain barrier. Neurobiol. Dis.37(1), 13–25 (2010).
  • Sindhwani S , SyedAM , NgaiJet al. The entry of nanoparticles into solid tumours. Nat. Mater.19(5), 566–575 (2020).
  • Westerhout J , PloegerB , SmeetsJ , DanhofM , DeLange EC. Physiologically based pharmacokinetic modeling to investigate regional brain distribution kinetics in rats. AAPS J.14(3), 543–553 (2012).
  • De Lange EC . The mastermind approach to CNS drug therapy: translational prediction of human brain distribution, target site kinetics, and therapeutic effects. Fluids Barriers CNS10(1), 1–16 (2013).
  • Bonferoni MC , RossiS , SandriGet al. Nanoemulsions for “Nose-to-Brain” Drug Delivery. Pharmaceutics11(2), 84 (2019).
  • Kumar A , PandeyAN , JainSK. Nasal-nanotechnology: revolution for efficient therapeutics delivery. Drug Delivery23(3), 681–693 (2016).
  • Mikitsh JL , ChackoAM. Pathways for small molecule delivery to the central nervous system across the blood-brain barrier. Perspecti. Med. Chem.6, 11–24 (2014).
  • Yang J , ShiZ , LiuR , WuY , ZhangX. Combined-therapeutic strategies synergistically potentiate glioblastoma multiforme treatment via nanotechnology. Theranostics10(7), 3223 (2020).
  • Blanco E , ShenH , FerrariM. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nature Biotechnol.33(9), 941–951 (2015).
  • Das SK , DasNG. Surface modification strategies in enhancing systemic delivery performance. In: Systemic Delivery Technologies in Anti-Aging Medicine: Methods and Applications.Springer, 365–392 (2020).
  • Veronesi MC , AlhamamiM , MiedemaSB , YunY , Ruiz-CardozoM , VannierMW. Imaging of intranasal drug delivery to the brain. Am. J. Nucl. Med. Mol. Imaging10(1), 1–31 (2020).
  • Chavda VP . Chapter 4 - Nanobased Nano Drug Delivery: A Comprehensive Review. In: Applications of Targeted Nano Drugs and Delivery Systems.MohapatraSS, RanjanS, DasguptaN, MishraRK, ThomasS ( Eds). Elsevier, 69–92 (2019).
  • Gabizon A , BradburyM , PrabhakarU , ZamboniW , LibuttiS , GrodzinskiP. Cancer nanomedicines: closing the translational gap. Lancet (London, England)384(9961), 2175 (2014).
  • Jabir NR , AnwarK , FirozCK , OvesM , KamalMA , TabrezS. An overview on the current status of cancer nanomedicines. Curr. Med. Res. Opin.34(5), 911–921 (2018).
  • Tong R , LangerR. Nanomedicines targeting the tumor microenvironment. Cancer J.21(4), 314–321 (2015).
  • Kammari R , DasNG , DasSK. Nanoparticulate systems for therapeutic and diagnostic applications. Emerging Nanotechnologies for Diagnostics, Drug Delivery and Medical Devices.105–144 (2017).
  • Prabhakar U , MaedaH , JainRKet al. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res.73(8), 2412–2417 (2013).
  • Zhang L , ChenQ , MaY , SunJ. Microfluidic Methods for Fabrication and Engineering of Nanoparticle Drug Delivery Systems. ACS Appl. Bio Materials3(1), 107–120 (2020).
  • Bhatia S . Nanoparticles types, classification, characterization, fabrication methods and drug delivery applications. In: Natural Polymer Drug Delivery Systems.33–93 (2016).
  • Mohanraj VJ , ChenY. Nanoparticles - A Review. Tropical J. Pharmaceutical Res.5(1), 561–573 (2007).
  • De Oliveira Junior ER , NascimentoTL , SalomaoMA , DaSilva ACG , ValadaresMC , LimaEM. Increased nose-to-brain delivery of melatonin mediated by polycaprolactone nanoparticles for the treatment of glioblastoma. Pharm. Res.36(9), 131 (2019).
  • D'mello SR , DasSK , DasNG. Polymeric nanoparticles for small-molecule drugs: biodegradation of polymers and fabrication of nanoparticles. In: Drug Delivery Nanoparticles Formulation and Characterization.CRC Press, 36–54 (2016).
  • Zhu J , HaywardRC. Spontaneous generation of amphiphilic block copolymer micelles with multiple morphologies through interfacial instabilities. J. Am. Chem. Soc.130(23), 7496–7502 (2008).
  • Taghipour B , YakhchaliM , HaririanI , TamaddonAM , SamaniSM. The effects of technical and compositional variables on the size and release profile of bovine serum albumin from PLGA based particulate systems. Res Pharm Sci9(6), 407–420 (2014).
  • Wang Y , LiP , Truong-DinhTran T , ZhangJ , KongL. Manufacturing techniques and surface engineering of polymer based nanoparticles for targeted drug delivery to cancer. Nanomaterials (Basel, Switzerland)6(2), 26 (2016).
  • López-Royo T , SebastiánV , Moreno-MartínezLet al. Encapsulation of large-size plasmids in PLGA nanoparticles for gene editing: comparison of three different synthesis methods. Nanomaterials (Basel, Switzerland)11(10), 2723 (2021).
  • Martínez-Muñoz O , Ospina-GiraldoL , Mora-HuertasCE. Nanoprecipitation: applications for entrapping active molecules of interest in pharmaceutics. Nano-and Microencapsulation-Techniques and Applications (2020).
  • Bilati U , AllémannE , DoelkerE. Development of a nanoprecipitation method intended for the entrapment of hydrophilic drugs into nanoparticles. European J. Pharmaceutical Sciences24(1), 67–75 (2005).
  • Barichello JM , MorishitaM , TakayamaK , NagaiT. Encapsulation of hydrophilic and lipophilic drugs in PLGA nanoparticles by the nanoprecipitation method. Drug Dev Ind Pharm25(4), 471–476 (1999).
  • Smiley SB , YunY , AyyagariPet al. Development of CD133 targeting multi-drug polymer micellar nanoparticles for glioblastoma - in vitro evaluation in glioblastoma stem cells. Pharm. Res.38(6), 1067–1079 (2021).
  • Niculescu AG , ChircovC , BîrcăAC , GrumezescuAM. Nanomaterials synthesis through microfluidic methods: an updated overview. Nanomaterials11(4), 864 (2021).
  • Khan AR , LiuM , KhanMW , ZhaiG. Progress in brain targeting drug delivery system by nasal route. J. Control. Release268, 364–389 (2017).
  • Bobo D , RobinsonKJ , IslamJ , ThurechtKJ , CorrieSR. Nanoparticle-based medicines: a review of fda-approved materials and clinical trials to date. Pharm. Res.33(10), 2373–2387 (2016).
  • Chu L , WangA , NiLet al. Nose-to-brain delivery of temozolomide-loaded PLGA nanoparticles functionalized with anti-EPHA3 for glioblastoma targeting. Drug Delivery25(1), 1634–1641 (2018).
  • Shilo M , SharonA , BaranesK , MotieiM , LelloucheJPM , PopovtzerR. The effect of nanoparticle size on the probability to cross the blood-brain barrier: an in-vitro endothelial cell model. J. Nanobiotechnol.13(1), 1–7 (2015).
  • Zhi K , RajiB , NookalaARet al. PLGA nanoparticle-based formulations to cross the blood–brain barrier for drug delivery: from R&D to cGMP. Pharmaceutics13(4), 500 (2021).
  • Husseini GA , PittWG. Micelles and nanoparticles for ultrasonic drug and gene delivery. Adv Drug Deliv Rev60(10), 1137–1152 (2008).
  • Majumder N , GDas N , DasSK. Polymeric micelles for anticancer drug delivery. Therap. Del.11(10), 613–635 (2020).
  • Nabar GM , MahajanKD , CalhounMAet al. Micelle-templated, poly(lactic-co-glycolic acid) nanoparticles for hydrophobic drug delivery. Int. J. Nanomed.13, 351–366 (2018).
  • Gao X , YuT , XuGet al. Enhancing the anti-glioma therapy of doxorubicin by honokiol with biodegradable self-assembling micelles through multiple evaluations. Sci. Rep.7, 43501 (2017).
  • Zhan C , GuB , XieC , LiJ , LiuY , LuW. Cyclic RGD conjugated poly(ethylene glycol)-co-poly(lactic acid) micelle enhances paclitaxel anti-glioblastoma effect. J. Control. Release143(1), 136–142 (2010).
  • Soo Choi H , LiuW , MisraPet al. Renal clearance of quantum dots. Nature Biotechnol.25(10), 1165–1170 (2007).
  • Tapeinos C , BattagliniM , CiofaniG. Advances in the design of solid lipid nanoparticles and nanostructured lipid carriers for targeting brain diseases. J. Control. Release264, 306–332 (2017).
  • Thi TTH , SuysEJA , LeeJS , NguyenDH , ParkKD , TruongNP. Lipid-based nanoparticles in the clinic and clinical trials: from cancer nanomedicine to COVID-19 vaccines. Vaccines (Basel)9(4), 359 (2021).
  • Grillone A , BattagliniM , MoscatoSet al. Nutlin-loaded magnetic solid lipid nanoparticles for targeted glioblastoma treatment. Nanomedicine (Lond)14(6), 727–752 (2019).
  • Scioli Montoto S , MuracaG , RuizME. Solid lipid nanoparticles for drug delivery: pharmacological and biopharmaceutical aspects. Front. Mol. Biosci.7, 587997 (2020).
  • Jnaidi R , AlmeidaAJ , GonçalvesLM. Solid lipid nanoparticles and nanostructured lipid carriers as smart drug delivery systems in the treatment of glioblastoma multiforme. Pharmaceutics12(9), 860 (2020).
  • Akbarzadeh A , Rezaei-SadabadyR , DavaranSet al. Liposome: classification, preparation, and applications. Nanoscale Res. Lett.8(1), 102 (2013).
  • Lakkadwala S , DosSantos Rodrigues B , SunC , SinghJ. Dual functionalized liposomes for efficient co-delivery of anti-cancer chemotherapeutics for the treatment of glioblastoma. J. Control. Release307, 247–260 (2019).
  • Shen Y , PiZ , YanFet al. Enhanced delivery of paclitaxel liposomes using focused ultrasound with microbubbles for treating nude mice bearing intracranial glioblastoma xenografts. Int. J. Nanomed.12, 5613–5629 (2017).
  • Werengowska-Ciećwierz K , WiśniewskiM , TerzykA , FurmaniakS. The chemistry of bioconjugation in nanoparticles-based drug delivery system. Advances Condensed Matter Physics2015, 1–27 (2015).
  • Hermanson GT . Bioconjugate techniques.Academic press (2013).
  • van de Watering FCJ , RijpkemaM , PerkL , BrinkmannU , OyenW , BoermanO. Zirconium-89 labeled antibodies: a new tool for molecular imaging in cancer patients. BioMed. Res. Int.2014, 203601 (2014).
  • Veronesi M , ZamoraM , BhuiyanM , Obrien-PenneyB , ChenC , VannierM. Use of a clinical pet/ct scanner for whole body biodistribution of intranasal nanoparticles. arXiv preprint arXiv:1704.00691 (2017).
  • Bien-Moller S , BalzE , HerzogSet al. Association of glioblastoma multiforme stem cell characteristics, differentiation, and microglia marker genes with patient survival. Stem Cells Int2018, 9628289 (2018).
  • Gui K , ZhangX , ChenFet al. Lipid-polymer nanoparticles with CD133 aptamers for targeted delivery of all-trans retinoic acid to osteosarcoma initiating cells. Biomed. Pharmacother.111, 751–764 (2019).
  • Shigdar S , QiaoL , ZhouSFet al. RNA aptamers targeting cancer stem cell marker CD133. Cancer Lett.330(1), 84–95 (2013).
  • Funkhouser J . Reinventing pharma: the theranostic revolution. Curr. Drug Discov.2, 17–19 (2002).
  • Yordanova A , EppardE , KurpigSet al. Theranostics in nuclear medicine practice. Onco Targets Ther.10, 4821–4828 (2017).
  • Agrawal A , RangarajanV , ShahS , PuranikA , PurandareN. MIBG (metaiodobenzylguanidine) theranostics in pediatric and adult malignancies. Br. J. Radiol.91(1091), 20180103 (2018).
  • Filippi L , ChiaravallotiA , SchillaciO , CianniR , BagniO. Theranostic approaches in nuclear medicine: current status and future prospects. Expert Rev. Med. Devices17(4), 331–343 (2020).
  • Kelkar SS , ReinekeTM. Theranostics: combining imaging and therapy. Bioconjug. Chem.22(10), 1879–1903 (2011).
  • Our World in Data . COVID-19 vaccine doses administered by manufacturer, USA (2022). https://ourworldindata.org/grapher/covid-vaccine-doses-by-manufacturer?country=∼USA