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Cited by 38Nanoparticle-Based Drug DeliveryBarrier Structure and Function StudiesGlioma Diagnosis and Treatment

A nanostructure of functional targeting epirubicin liposomes dually modified with aminophenyl glucose and cyclic pentapeptide used for brain glioblastoma treatment

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Zhang, Cheng-Xiang, Zhao, Wei-Yu, Liu, Lei, Ju, Rui-Jun, Mu, Li-Min, Zhao, Yao, Zeng, Fan, Xie, Hong-Jun +2 more·2015·Oncotarget
DOI 10.18632/oncotarget.5354PMC PMC4741722
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Abstract

// Cheng-Xiang Zhang 1 , Wei-Yu Zhao 1 , Lei Liu 1 , Rui-Jun Ju 1 , Li-Min Mu 1 , Yao Zhao 1 , Fan Zeng 1 , Hong-Jun Xie 1 , Yan Yan 1 , Wan-Liang Lu 1 1 Beijing Key Laboratory of Molecular Pharmaceutics and New Drug System, State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing 100191, China Correspondence to: Wan-Liang Lu, e-mail: luwl@bjmu.edu.cn Keywords: Functional targeting epirubicin liposomes, BBB, brain glioblastoma, neovasculatures, mechanism and efficacy Received: April 14, 2015 Accepted: September 14, 2015 Published: September 25, 2015 ABSTRACT The objectives of the present study were to develop functional targeting epirubicin liposomes for transferring drugs across the blood-brain barrier (BBB), treating glioblastoma, and disabling neovascularization. The studies were performed on glioblastoma cells in vitro and on glioblastoma-bearing mice. The results showed that the constructed liposomes had a high encapsulation efficiency for drugs (>95%), suitable particle size (109 nm), and less leakage in the blood component-containing system; were significantly able to be transported across the BBB; and exhibited efficacies in killing glioblastoma cells and in destroying glioblastoma neovasculature in vitro and in glioblastoma-bearing mice. The action mechanisms of functional targeting epirubicin liposomes correlated with the following features: the long circulation in the blood system, the ability to be transported across the BBB via glucose transporter-1, and the targeting effects on glioblastoma cells and on the endothelial cells of the glioblastoma neovasculature via the integrin β3 receptor. In conclusion, functional targeting epirubicin liposomes could be used as a potential therapy for treating brain glioblastoma and disabling neovascularization in brain glioblastomas.

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  • Bifunctional liposomal delivery carriers increase BBB targeting efficiency, most likely by overcoming receptor or transporter saturation limitation of monofunctional liposomes.

    “These bifunctional liposomal delivery carriers increase BBB targeting efficiency, most likely by overcoming the receptor or transporter saturation limitation of monofunctional liposomes [221].”

    From Alzheimer's Disease: Treatment Strategies and Their Limitations. (2022) · cites this paper as [221]

    The Results (‘Transport across the BBB and treatment of glioblastoma cells’; page unavailable) report a higher transport ratio in the in-vitro BBB model for dual-targeting liposomes (15.00 ± 6.24%) than for Glu-targeting liposomes (11.00 ± 7.00%). The Discussion attributes BBB transport to Glut-1 binding and describes the second target, integrin β3, in relation to glioblastoma cells. The paper does not attribute the transport difference to overcoming receptor or transporter saturation in monofunctional liposomes. (LLM, conf=0.87)

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Research works printed but not linked: 39

  1. [1]McNamara MG Mason WP Antiangiogenic therapies in glioblastoma multiforme Expert Review of Anticancer Therapy 2012 12 643 654 22594899
  2. [2]Lebelt A Dzieciol J Guzinska-Ustymowicz K Lemancewicz D Zimnoch L Czykier E Angiogenesis in gliomas Folia Histochemica et Cytobiologica 2008 46 69 72 18296266
  3. [3]Hardee ME Zagzag D Mechanisms of glioma-associated neovascularization The American Journal of Pathology 2012 181 1126 1141 22858156 PMC3463636
  4. [4]Jo J Schiff D Purow B Angiogenic inhibition in high-grade gliomas: past, present and future Expert Review of Neurotherapeutics 2012 12 733 747 22650175
  5. [5]Pardridge WM Blood-brain barrier delivery Drug Discovery Today 2007 12 54 61 17198973
  6. [6]Bicker J Alves G Fortuna A Falcao A Blood-brain barrier models and their relevance for a successful development of CNS drug delivery systems: a review European Journal of Pharmaceutics and Biopharmaceutics 2014 87 409 432 24686194
  7. [7]Chen Y Liu L Modern methods for delivery of drugs across the blood-brain barrier Advanced Drug Delivery Reviews 2012 64 640 665 22154620
  8. [8]Brodbelt A Greenberg D Winters T Williams M Vernon S Collins VP Glioblastoma in England: 2007–2011 European Journal of Cancer 2015 51 533 542 25661102
  9. [9]Omuro A DeAngelis LM Glioblastoma and other malignant gliomas: a clinical review Jama 2013 310 1842 1850 24193082
  10. [10]Wait SD Prabhu RS Burri SH Atkins TG Asher AL Polymeric drug delivery for the treatment of glioblastoma Neuro-Oncology 2015 17 ii9 ii23 25746091 PMC4483039
  11. [11]Abbott NJ Ronnback L Hansson E Astrocyte-endothelial interactions at the blood-brain barrier Nature Reviews. Neuroscience 2006 7 41 53 16371949
  12. [12]Okonogi N Shirai K Oike T Murata K Noda SE Suzuki Y Nakano T Topics in chemotherapy, molecular-targeted therapy, and immunotherapy for newly-diagnosed glioblastoma multiforme Anticancer Research 2015 35 1229 1135 25750269
  13. [13]Cornford EM Hyman S Swartz BE The human brain GLUT1 glucose transporter: ultrastructural localization to the blood-brain barrier endothelia Journal of Cerebral Blood Flow and Metabolism 1994 14 106 112 8263045
  14. [14]Adekola K Rosen ST Shanmugam M Glucose transporters in cancer metabolism Current Opinion in Oncology 2012 24 650 654 22913968 PMC6392426
  15. [15]Weis SM Cheresh DA Tumor angiogenesis: molecular pathways and therapeutic targets Nature Medicine 2011 17 1359 1370 22064426
  16. [16]Brooks PC Clark RA Cheresh DA Requirement of vascular integrin alpha v beta 3 for angiogenesis Science 1994 264 569 571 7512751
  17. [17]Brooks PC Montgomery AM Rosenfeld M Reisfeld RA Hu T Klier G Cheresh DA Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels Cell 1994 79 1157 1164 7528107
  18. [18]Walbert T Mikkelsen T Recurrent high-grade glioma: a diagnostic and therapeutic challenge Expert Review of Neurotherapeutics 2011 11 509 518 21469924
  19. [19]Alsibai W Hahnenkamp A Eisenblatter M Riemann B Schafers M Bremer C Haufe G Holtke C Fluorescent non-peptidic RGD mimetics with high selectivity for alphaVbeta3 vs alphaIIbbeta3 integrin receptor: novel probes for in vivo optical imaging Journal of Medicinal Chemistry 2014 57 9971 9982 25384028
  20. [20]Wang K Zhang X Liu Y Liu C Jiang B Jiang Y Tumor penetrability and anti-angiogenesis using iRGD-mediated delivery of doxorubicin-polymer conjugates Biomaterials 2014 35 8735 8747 25023394
  21. [21]Khatri N Baradia D Vhora I Rathi M Misra A cRGD grafted liposomes containing inorganic nano-precipitate complexed siRNA for intracellular delivery in cancer cells Journal of Controlled Release 2014 182 45 57 24631861
  22. [22]Sakurai Y Hatakeyama H Sato Y Hyodo M Akita H Ohga N Hida K Harashima H RNAi-mediated gene knockdown and anti-angiogenic therapy of RCCs using a cyclic RGD-modified liposomal-siRNA system Journal of Controlled Release 2014 173 110 118 24120854
  23. [23]Murphy EA Majeti BK Barnes LA Makale M Weis SM Lutu-Fuga K Wrasidlo W Cheresh DA Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis Proceedings of the National Academy of Sciences of the United States of America 2008 105 9343 9348 18607000 PMC2453735
  24. [24]Yamada T Egashira N Bando A Nishime Y Tonogai Y Imuta M Yano T Oishi R Activation of p38 MAPK by oxidative stress underlying epirubicin-induced vascular endothelial cell injury Free Radical Biology & Medicine 2012 52 1285 1293 22330067
  25. [25]Bar-Joseph H Ben-Aharon I Tzabari M Tsarfaty G Stemmer SM Shalgi R In vivo bioimaging as a novel strategy to detect doxorubicin-induced damage to gonadal blood vessels PLoS One 2011 6 e23492 21931602 PMC3170286
  26. [26]Srinivasan B Kolli AR Esch MB Abaci HE Shuler ML Hickman JJ TEER measurement techniques for in vitro barrier model systems Journal of Laboratory Automation 2015 20 107 126 25586998 PMC4652793
  27. [27]Torchilin V Tumor delivery of macromolecular drugs based on the EPR effect Advanced Drug Delivery Reviews 2011 63 131 135 20304019
  28. [28]Wang XX Li YB Yao HJ Ju RJ Zhang Y Li RJ Yu Y Zhang L Lu WL The use of mitochondrial targeting resveratrol liposomes modified with a dequalinium polyethylene glycol-distearoylphosphatidyl ethanolamine conjugate to induce apoptosis in resistant lung cancer cells Biomaterials 2011 32 5673 5687 21550109
  29. [29]Igarashi Y Utsumi H Chiba H Yamada-Sasamori Y Tobioka H Kamimura Y Furuuchi K Kokai Y Nakagawa T Mori M Sawada N Glial cell line-derived neurotrophic factor induces barrier function of endothelial cells forming the blood-brain barrier Biochemical and Biophysical Research Communications 1999 261 108 112 10405331
  30. [30]Lin LF Doherty DH Lile JD Bektesh S Collins F GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons Science 1993 260 1130 1132 8493557
  31. [31]Lee SW Kim WJ Choi YK Song HS Son MJ Gelman IH Kim YJ Kim KW SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier Nature Medicine 2003 9 900 906 12808449
  32. [32]Wilhelm I Fazakas C Krizbai IA In vitro models of the blood-brain barrier Acta Neurobiologiae Experimentalis 2011 71 113 128 21499332
  33. [33]Rautio J Laine K Gynther M Savolainen J Prodrug approaches for CNS delivery The AAPS Journal 2008 10 92 102 18446509 PMC2751454
  34. [34]Dhanikula RS Argaw A Bouchard JF Hildgen P Methotrexate loaded polyether-copolyester dendrimers for the treatment of gliomas: enhanced efficacy and intratumoral transport capability Molecular Pharmaceutics 2008 5 105 116 18171013
  35. [35]Yuhas JM Li AP Martinez AO Ladman AJ A simplified method for production and growth of multicellular tumor spheroids Cancer Research 1977 37 3639 3643 908012
  36. [36]Szablewski L Expression of glucose transporters in cancers Biochimica et Biophysica Acta 2013 1835 164 169 23266512
  37. [37]Haubner R Gratias R Diefenbach B Goodman SL Jonczyk A Kessler H Structural and functional aspects of RGD-containing cyclic pentapeptides as highly potent and selective integrin αVβ3 antagonists Journal of the American Chemical Society 1996 118 7461 7472
  38. [38]Gao H Xiong Y Zhang S Yang Z Cao S Jiang X RGD and interleukin-13 peptide functionalized nanoparticles for enhanced glioblastoma cells and neovasculature dual targeting delivery and elevated tumor penetration Molecular Pharmaceutics 2014 11 1042 1052 24521297
  39. [39]Wuest DM Lee KH Optimization of endothelial cell growth in a murine in vitro blood-brain barrier model Biotechnology Journal 2012 7 409 417 22095877 PMC3488296

Cited by

Sorted by citations

Authors
Zhang, C.-X., Zhao, W.-Y., Liu, L., Ju, R.-J., Mu, L.-M., Zhao, Y., Zeng, F., Xie, H.-J., Yan, Y., & Lu, W.-L.
Affiliations
  • Peking University (CN)
  • Beijing Key Laboratory of Molecular Pharmaceutics and New Drug System, State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking University, Beijing 100191, China
ORCID
Venue
Oncotarget
Publisher
Impact Journals, LLC
Published
2015-09-25
Volume
6
Issue
32
Pages
32681-32700
ISSN
1949-2553 (ISSN-L)
DOI
10.18632/oncotarget.5354
PMC
PMC4741722
OpenAlex
W2200083991
Cited by
38
References
0
Citations by year
2026: 1 · 2025: 1 · 2023: 5 · 2022: 3 · 2021: 5 · 2020: 6 · 2019: 3 · 2018: 5 · 2017: 9
FWCI
1.69
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Oncotarget (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Natural Science Foundation of China (81373343)
  • National Key Research and Development Program of China (2013CB932501)
Topics
  • Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
  • Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
  • Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
Keywords
glioblastoma, blood-brain barrier, cyclic pentapeptide, glucose transporter 1, tumor angiogenesis, targeted drug delivery, liposomal drug delivery, encapsulation efficiency
MeSH terms
Animals, Antibiotics, Antineoplastic, Blood-Brain Barrier, Brain Neoplasms, Capillary Permeability, Chemistry, Pharmaceutical, Dose-Response Relationship, Drug, Glioblastoma, Glucosides, Humans, Liposomes, Male, Mice, Inbred BALB C, Mice, Nude, Neovascularization, Pathologic, Peptides, Cyclic, Time Factors, Tissue Distribution, Epirubicin, Spheroids, Cellular, Angiogenesis Inhibitors, Xenograft Model Antitumor Assays, Endothelial Cells, Cell Line, Tumor, Nanoparticles

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