Reviews
Jiwei Cui, Yuanxin Xu, Haiyan Tu, Huacong Zhao, Honglan Wang, Liuqing Di, Ruoning Wang. Gather wisdom to overcome barriers: Well-designed nano-drug delivery systems for treating gliomas[J]. Acta Pharmaceutica Sinica B, 2022, 12(3): 1100-1125

Gather wisdom to overcome barriers: Well-designed nano-drug delivery systems for treating gliomas
Jiwei Cuia,b, Yuanxin Xua,b, Haiyan Tua,b, Huacong Zhaoa,b, Honglan Wanga,b, Liuqing Dia,b, Ruoning Wanga,b
a. College of Pharmacy, Nanjing University of Chinese Medicine, Nanjing 210023, China;
b. Jiangsu Provincial TCM Engineering Technology, Research Center of High Efficient Drug Delivery System, Nanjing 210023, China
Abstract:
Due to the special physiological and pathological characteristics of gliomas, most therapeutic drugs are prevented from entering the brain. To improve the poor prognosis of existing therapies, researchers have been continuously developing non-invasive methods to overcome barriers to gliomas therapy. Although these strategies can be used clinically to overcome the blood-brain barrier (BBB), the accurate delivery of drugs to the glioma lesions cannot be ensured. Nano-drug delivery systems (NDDS) have been widely used for precise drug delivery. In recent years, researchers have gathered their wisdom to overcome barriers, so many well-designed NDDS have performed prominently in preclinical studies. These meticulous designs mainly include cascade passing through BBB and targeting to glioma lesions, drug release in response to the glioma microenvironment, biomimetic delivery systems based on endogenous cells/extracellular vesicles/protein, and carriers created according to the active ingredients of traditional Chinese medicines. We reviewed these well-designed NDDS in detail. Furthermore, we discussed the current ongoing and completed clinical trials of NDDS for gliomas therapy, and analyzed the challenges and trends faced by clinical translation of these well-designed NDDS.
Key words:    Glioma    Blood-brain barrier    Non-invasive strategies    Nano-drug delivery systems    Cascade targeting    Responsive delivery and release    Biomimetic designs    Active ingredients    Traditional Chinese medicine   
Received: 2021-06-03     Revised: 2021-07-07
DOI: 10.1016/j.apsb.2021.08.013
Funds: The authors acknowledge financial support from National Natural Science Foundation of China (Nos. 81903557 and 82074024), Natural Science Foundation of Jiangsu Province (No. BK20190802, China), Natural Science Foundation Youth Project of Nanjing University of Chinese Medicine (No. NZY81903557, China), the Open Project of Chinese Materia Medica First-Class Discipline of Nanjing University of Chinese Medicine (No. 2020YLXK019, China), the Natural Science Foundation of the Jiangsu Higher Education Institutions of China (No. 19KJB350003, China), and College Students' Innovative Entrepreneurial Training Plan Program of Nanjing University of Chinese Medicine (No. 202010315XJ040, China).
Corresponding author: Ruoning Wang,E-mai:ruoningw@njucm.edu.cn     Email:ruoningw@njucm.edu.cn
Author description:
Service
PDF(KB) Free
Print
0
Authors
Jiwei Cui
Yuanxin Xu
Haiyan Tu
Huacong Zhao
Honglan Wang
Liuqing Di
Ruoning Wang

References:
[1] Chen J, McKay RM, Parada LF. Malignant glioma:lessons from genomics, mouse models, and stem cells. Cell 2012;149:36-47
[2] Xue S, Hu M, Iyer V, Yu JM. Blocking the PD-1/PD-L1 pathway in glioma:a potential new treatment strategy. J Hematol Oncol 2017;10:81
[3] Juratli TA, Cahill DP, McCutcheon IE. Determining optimal treatment strategy for diffuse glioma:the emerging role of IDH mutations. Expert Rev Anticancer Ther 2015;15:603-606
[4] Mahmoud BS, AlAmri AH, McConville C. Polymeric nanoparticles for the treatment of malignant gliomas. Cancers 2020;12:175
[5] Zhao Z, Nelson AR, Betsholtz C, Zlokovic BV. Establishment and dysfunction of the blood-brain barrier. Cell 2015;163:1064-1078
[6] Loscher W, Potschka H. Drug resistance in brain diseases and the role of drug efflux transporters. Nat Rev Neurosci 2005;6:591-602
[7] Pulgar VM. Transcytosis to cross the blood brabin barrier, new advancements and challenges. Front Neurosci 2018;12:1019
[8] Buahin KG, Brem H. Interstitial chemotherapy of experimental brain tumors:comparison of intratumoral injection versus polymeric controlled release. J Neurooncol 1995;26:103-110
[9] Foley CP, Rubin DG, Santillan A, Sondhi D, Dyke JP, Gobin YP, et al. Intra-arterial delivery of AAV vectors to the mouse brain after mannitol mediated blood brain barrier disruption. J Control Release 2014;196:71-78
[10] Inamura T, Black KL. Bradykinin selectively opens blood-tumor barrier in experimental brain tumors. J Cereb Blood Flow Metab 1994;14:862-870
[11] Deng ZT, Sheng ZH, Yan F. Ultrasound-Induced blood-brain-barrier opening enhances anticancer efficacy in the treatment of glioblastoma:current status and future prospects. J Oncol 2019;2019:2345203
[12] Illum L. Transport of drugs from the nasal cavity to the central nervous system. Eur J Pharm Sci 2000;11:1-18
[13] Crowe TP, Greenlee MHW, Kanthasamy AG, Hsu WH. Mechanism of intranasal drug delivery directly to the brain. Life Sci 2018;195:44-52
[14] Khan AR, Yang XY, Fu MF, Zhai GX. Recent progress of drug nanoformulations targeting to brain. J Control Release 2018;291:37-64
[15] Gao HL. Perspectives on dual targeting delivery systems for brain tumors. J Neuroimmune Pharm 2017;12:6-16
[16] Meng FH, Cheng R, Deng C, Zhong ZY. Intracellular drug release nanosystems. Mater Today 2012;15:436-442
[17] Ayer M, Klok HA. Cell-mediated delivery of synthetic nano- and microparticles. J Control Release 2017;259:92-104
[18] Iqbal H, Yang T, Li T, Zhang MY, Ke HT, Ding DW, et al. Serum protein-based nanoparticles for cancer diagnosis and treatment. J Control Release 2021;329:997-1022
[19] Bottcher S, Drusch S. Saponins-self-assembly and behavior at aqueous interfaces. Adv Colloid Interface Sci 2017;243:105-113
[20] Daneman R, Prat A. The blood-brain barrier. Cold Spring Harbor Perspect Biol 2015;7:a020412
[21] Wei XL, Chen XS, Ying M, Lu WY. Brain tumor-targeted drug delivery strategies. Acta Pharm Sin B 2014;4:193-201
[22] Pandit R, Chen LY, Gotz J. The blood-brain barrier:physiology and strategies for drug delivery. Adv Drug Deliv Rev 2020;165-166:1-14
[23] Pardridge WM. Drug transport across the blood-brain barrier. J Cereb Blood Flow Metab 2012;32:1959-1972
[24] Hashimoto Y, Campbell M. Tight junction modulation at the blood-brain barrier:current and future perspectives. Biochim Biophys Acta-Biomembr 2020;1862:183298
[25] Luo HL, Shusta EV. Blood-brain barrier modulation to improve glioma drug delivery. Pharmaceutics 2020;12:1085
[26] Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis 2010;37:13-25
[27] Lee SW, Kim WJ, Choi YK, Song HS, Son MJ, Gelman IH, et al. SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier. Nat Med 2003;9:900-906
[28] Baeten KM, Akassoglou K. Extracellular matrix and matrix receptors in blood-brain barrier formation and stroke. Dev Neurobiol 2011;71:1018-1039
[29] Schneider SW, Ludwig T, Tatenhorst L, Braune S, Oberleithner H, Senner V, et al. Glioblastoma cells release factors that disrupt blood-brain barrier features. Acta Neuropathol 2004;107:272-276
[30] Plate KH, Scholz A, Dumont DJ. Tumor angiogenesis and anti-angiogenic therapy in malignant gliomas revisited. Acta Neuropathol 2012;124:763-775
[31] Wang D, Wang C, Wang L, Chen Y. A comprehensive review in improving delivery of small-molecule chemotherapeutic agents overcoming the blood-brain/brain tumor barriers for glioblastoma treatment. Drug Deliv 2019;26:551-565
[32] Sarkaria JN, Hu LS, Parney IF, Pafundi DH, Brinkmann DH, Laack NN, et al. Is the blood-brain barrier really disrupted in all glioblastomas? A critical assessment of existing clinical data. Neuro Oncol 2018;20:184-191
[33] Belykh E, Shaffer KV, Lin CQ, Byvaltsev VA, Preul MC, Chen LK. Blood-brain barrier, blood-brain tumor barrier, and fluorescence-guided neurosurgical oncology:delivering optical labels to brain tumors. Front Oncol 2020;10:739
[34] Tate MC, Aghi MK. Biology of angiogenesis and invasion in glioma. Neurotherapeutics 2009;6:447-457
[35] Oberoi RK, Parrish KE, Sio TT, Mittapalli RK, Elmquist WF, Sarkaria JN. Strategies to improve delivery of anticancer drugs across the blood-brain barrier to treat glioblastoma. Neuro Oncol 2016;18:27-36
[36] Haumann R, Videira JC, Kaspers GJL, van Vuurden DG, Hulleman E. Overview of current drug delivery methods across the blood-brain barrier for the treatment of primary brain tumors. CNS Drugs 2020;34:1121-1131
[37] Arvanitis CD, Ferraro GB, Jain RK. The blood-brain barrier and blood-tumour barrier in brain tumours and metastases. Nat Rev Cancer 2020;20:26-41
[38] Robey RW, Pluchino KM, Hall MD, Fojo AT, Bates SE, Gottesman MM. Revisiting the role of ABC transporters in multidrug-resistant cancer. Nat Rev Cancer 2018;18:452-464
[39] Chaves C, Shawahna R, Jacob A, Scherrmann JM, Decleves X. Human ABC transporters at blood-CNS interfaces as determinants of CNS drug penetration. Curr Pharm Design 2014;20:1450-1462
[40] Bart J, Groen HJ, Hendrikse NH, van der Graaf WT, Vaalburg W, de Vries EG. The blood-brain barrier and oncology:new insights into function and modulation. Cancer Treat Rev 2000;26:449-462
[41] Kemper EM, van Zandbergen AE, Cleypool C, Mos HA, Boogerd W, Beijnen JH, et al. Increased penetration of paclitaxel into the brain by inhibition of P-glycoprotein. Clin Cancer Res 2003;9:2849-2855
[42] Neuwelt EA, Bauer B, Fahlke C, Fricker G, Iadecola C, Janigro D, et al. Engaging neuroscience to advance translational research in brain barrier biology. Nat Rev Neurosci 2011;12:169-182
[43] Binkhathlan Z, Lavasanifar A. P-glycoprotein inhibition as a therapeutic approach for overcoming multidrug resistance in cancer:current status and future perspectives. Curr Cancer Drug Targets 2013;13:326-346
[44] Tournier N, Goutal S, Auvity S, Traxl A, Mairinger S, Wanek T, et al. Strategies to inhibit ABCB1- and ABCG2-mediated efflux transport of erlotinib at the blood-brain barrier:a PET study on nonhuman primates. J Nucl Med 2017;58:117-122
[45] Lazarova N, Zoghbi SS, Hong J, Seneca N, Tuan E, Gladding RL, et al. Synthesis and evaluation of[N-methyl-11C]N-desmethyl-loperamide as a new and improved PET radiotracer for imaging P-gp function. J Med Chem 2008;51:6034-6043
[46] Sweeney MD, Zhao Z, Montagne A, Nelson AR, Zlokovic BV. Blood-brain barrier:from physiology to disease and back. Physiol Rev 2019;99:21-78
[47] Ruan SB, Zhou Y, Jiang XG, Gao HL. Rethinking CRITID procedure of brain targeting drug delivery:circulation, blood brain barrier recognition, intracellular transport, diseased cell targeting, internalization, and drug release. Adv Sci 2021;8:2004025
[48] Ayloo S, Gu CH. Transcytosis at the blood-brain barrier. Curr Opin Neurobiol 2019;57:32-38
[49] Cullen PJ, Steinberg F. To degrade or not to degrade:mechanisms and significance of endocytic recycling. Nat Rev Mol Cell Biol 2018;19:679-696
[50] Bathori G, Cervenak L, Karadi I. Caveolae-an alternative endocytotic pathway for targeted drug delivery. Crit Rev Ther Drug Carr Syst 2004;21:67-95
[51] Moura RP, Martins C, Pinto S, Sousa F, Sarmento B. Blood-brain barrier receptors and transporters:an insight on their function and how to exploit them through nanotechnology. Expert Opin Drug Deliv 2019;16:271-285
[52] Sabel M, Giese A. Safety profile of carmustine wafers in malignant glioma:a review of controlled trials and a decade of clinical experience. Curr Med Res Opin 2008;24:3239-3257
[53] Jahangiri A, Chin AT, Flanigan PM, Chen R, Bankiewicz K, Aghi MK. Convection-enhanced delivery in glioblastoma:a review of preclinical and clinical studies. J Neurosurg 2017;126:191-200
[54] Blakeley J. Drug delivery to brain tumors. Curr Neurol Neurosci Rep 2008;8:235-241
[55] Hersh DS, Wadajkar AS, Roberts NB, Perez JG, Connolly NP, Frenkel V, et al. Evolving drug delivery strategies to overcome the blood brain barrier. Curr Pharm Design 2016;22:1177-1193
[56] Kroll RA, Neuwelt EA. Outwitting the blood-brain barrier for therapeutic purposes:osmotic opening and other means. Neurosurgery 1998;42:1083-1099
[57] Boockvar JA, Tsiouris AJ, Hofstetter CP, Kovanlikaya I, Fralin S, Kesavabhotla K, et al. Safety and maximum tolerated dose of superselective intraarterial cerebral infusion of bevacizumab after osmotic blood-brain barrier disruption for recurrent malignant glioma. Clinical article. J Neurosurg 2011;114:624-632
[58] Kozler P, Riljak V, Pokorny J. Both water intoxication and osmotic BBB disruption increase brain water content in rats. Physiol Res 2013;62:S75-S80
[59] Liu LB, Xue YX, Liu YH, Wang YB. Bradykinin increases blood-tumor barrier permeability by down-regulating the expression levels of ZO-1, occludin, and claudin-5 and rearranging actin cytoskeleton. J Neurosci Res 2008;86:1153-1168
[60] Zhang H, Gu YT, Xue YX. Bradykinin-induced blood-brain tumor barrier permeability increase is mediated by adenosine 5'-triphosphate-sensitive potassium channel. Brain Res 2007;1144:33-41
[61] Xie ZX, Shen Q, Xie C, Lu WY, Peng CM, Wei XL, et al. Retro-inverso bradykinin opens the door of blood-brain tumor barrier for nanocarriers in glioma treatment. Cancer Lett 2015;369:144-151
[62] Emerich DF, Dean RL, Osborn C, Bartus RT. The development of the bradykinin agonist labradimil as a means to increase the permeability of the blood-brain barrier:from concept to clinical evaluation. Clin Pharmacokinet 2001;40:105-123
[63] Zhao YS, Xue YX, Liu YH, Fu W, Jiang NJ, An P, et al. Study of correlation between expression of bradykinin B2 receptor and pathological grade in human gliomas. Br J Neurosurg 2005;19:322-326
[64] Bates E. Ion channels in development and cancer. Annu Rev Cell Dev Biol 2015;31:231-247
[65] Gu YT, Xue YX, Wang YF, Wang JH, Chen X, ShangGuan QR, et al. Minoxidil sulfate induced the increase in blood-brain tumor barrier permeability through ROS/RhoA/PI3K/PKB signaling pathway. Neuropharmacology 2013;75:407-415
[66] Liang JM, Gao CF, Zhu Y, Ling CL, Wang Q, Huang YZ, et al. Natural brain penetration enhancer-modified albumin nanoparticles for glioma targeting delivery. ACS Appl Mater Interfaces 2018;10:30201-30213
[67] Zhang QL, Fu BMM, Zhang ZJ. Borneol, a novel agent that improves central nervous system drug delivery by enhancing blood-brain barrier permeability. Drug Deliv 2017;24:1037-1044
[68] Duan MM, Xing YM, Guo JQ, Chen H, Zhang R. Borneol increases blood-tumour barrier permeability by regulating the expression levels of tight junction-associated proteins. Pharm Biol 2016;54:3009-3018
[69] Wu T, Zhang AQ, Lu HY, Cheng QY. The role and mechanism of borneol to open the blood-brain barrier. Integr Cancer Ther 2018;17:806-812
[70] Yu B, Ruan M, Dong XP, Yu Y, Cheng HB. The mechanism of the opening of the blood-brain barrier by borneol:a pharmacodynamics and pharmacokinetics combination study. J Ethnopharmacol 2013;150:1096-1108
[71] Liu WJ, Yin YB, Sun JY, Feng S, Ma JK, Fu XY, et al. Natural borneol is a novel chemosensitizer that enhances temozolomide-induced anticancer efficiency against human glioma by triggering mitochondrial dysfunction and reactive oxide species-mediated oxidative damage. Onco Targets Ther 2018;11:5429-5439
[72] Elias WJ, Huss D, Voss T, Loomba J, Khaled M, Zadicario E, et al. A pilot study of focused ultrasound thalamotomy for essential tremor. N Engl J Med 2013;369:640-648
[73] Liu HL, Fan CH, Ting CY, Yeh CK. Combining microbubbles and ultrasound for drug delivery to brain tumors:current progress and overview. Theranostics 2014;4:432-444
[74] Park J, Aryal M, Vykhodtseva N, Zhang YZ, McDannold N. Evaluation of permeability, doxorubicin delivery, and drug retention in a rat brain tumor model after ultrasound-induced blood-tumor barrier disruption. J Control Release 2017;250:77-85
[75] Ting CY, Fan CH, Liu HL, Huang CY, Hsieh HY, Yen TC, et al. Concurrent blood-brain barrier opening and local drug delivery using drug-carrying microbubbles and focused ultrasound for brain glioma treatment. Biomaterials 2012;33:704-712
[76] Barth RF, Coderre JA, Vicente MGH, Blue TE. Boron neutron capture therapy of cancer:current status and future prospects. Clin Cancer Res 2005;11:3987-4002
[77] Fan CH, Wang TW, Hsieh YK, Wang CF, Gao ZY, Kim A, et al. Enhancing boron uptake in brain glioma by a boron-polymer/microbubble complex with focused ultrasound. ACS Appl Mater Interfaces 2019;11:11144-11156
[78] Mainprize T, Lipsman N, Huang YX, Meng Y, Bethune A, Ironside S, et al. Blood-brain barrier opening in primary brain tumors with non-invasive MR-guided focused ultrasound:a clinical safety and feasibility study. Sci Rep 2019;9:321
[79] Huang YX, Alkins R, Schwartz ML, Hynynen K. Opening the blood-brain barrier with MR imaging-guided focused ultrasound:preclinical testing on a trans-human skull porcine model. Radiology 2017;282:123-130
[80] Quintana DS, Guastella AJ, Westlye LT, Andreassen OA. The promise and pitfalls of intranasally administering psychopharmacological agents for the treatment of psychiatric disorders. Mol Psychiatr 2016;21:29-38
[81] Chen TC, da Fonseca CO, Schonthal AH. Intranasal perillyl alcohol for glioma therapy:molecular mechanisms and clinical development. Int J Mol Sci 2018;19:3905
[82] Mistry A, Stolnik S, Illum L. Nose-to-brain delivery:investigation of the transport of nanoparticles with different surface characteristics and sizes in excised porcine olfactory epithelium. Mol Pharm 2015;12:2755-2766
[83] da Fonseca CO, Schwartsmann G, Fischer J, Nagel J, Futuro D, Quirico-Santos T, et al. Preliminary results from a phase I/II study of perillyl alcohol intranasal administration in adults with recurrent malignant gliomas. Surg Neurol 2008;70:259-267
[84] da Fonseca CO, Simao M, Lins IR, Caetano RO, Futuro D, Quirico-Santos T. Efficacy of monoterpene perillyl alcohol upon survival rate of patients with recurrent glioblastoma. J Cancer Res Clin Oncol 2011;137:287-293
[85] Comfort C, Garrastazu G, Pozzoli M, Sonvico F. Opportunities and challenges for the nasal administration of nanoemulsions. Curr Top Med Chem 2015;15:356-368
[86] Sekerdag E, Lule S, Pehlivan SB, Ozturk N, Kara A, Kaffashi A, et al. A potential non-invasive glioblastoma treatment:nose-to-brain delivery of farnesylthiosalicylic acid incorporated hybrid nanoparticles. J Control Release 2017;261:187-198
[87] Colombo M, Figueiro F, Dias AD, Teixeira HF, Battastini AMO, Koester LS. Kaempferol-loaded mucoadhesive nanoemulsion for intranasal administration reduces glioma growth in vitro. Int J Pharm 2018;543:214-223
[88] Chen YS, Chiu YH, Li YS, Lin EY, Hsieh DK, Lee CH, et al. Integration of PEG 400 into a self-nanoemulsifying drug delivery system improves drug loading capacity and nasal mucosa permeability and prolongs the survival of rats with malignant brain tumors. Int J Nanomed 2019;14:3601-3613
[89] de Oliveira ER, Santos LCR, Salomao MA, Nascimento TL, Oliveira GDR, Liao LM, et al. Nose-to-brain drug delivery mediated by polymeric nanoparticles:influence of PEG surface coating. Drug Deliv Transl Res 2020;10:1688-1699
[90] Sukumar UK, Bose RJC, Malhotra M, Babikir HA, Afjei R, Robinson E, et al. Intranasal delivery of targeted polyfunctional gold-iron oxide nanoparticles loaded with therapeutic microRNAs for combined theranostic multimodality imaging and presensitization of glioblastoma to temozolomide. Biomaterials 2019;218:119342
[91] Chen Y, Liu LH. Modern methods for delivery of drugs across the blood-brain barrier. Adv Drug Deliv Rev 2012;64:640-665
[92] Lam FC, Morton SW, Wyckoff J, Han TLV, Hwang MK, Maffa A, et al. Enhanced efficacy of combined temozolomide and bromodomain inhibitor therapy for gliomas using targeted nanoparticles. Nat Commun 2018;9:1991
[93] Jiang Y, Zhang J, Meng FH, Zhong ZY. Apolipoprotein E peptide-directed chimeric polymersomes mediate an ultrahigh-efficiency targeted protein therapy for glioblastoma. ACS Nano 2018;12:11070-11079
[94] Lu F, Pang ZY, Zhao JJ, Jin K, Li HC, Pang Q, et al. Angiopep-2-conjugated poly(ethylene glycol)-co-poly(epsilon-caprolactone) polymersomes for dual-targeting drug delivery to glioma in rats. Int J Nanomed 2017;12:2117-2127
[95] Niu JX, Wang AD, Ke ZC, Zheng ZB. Glucose transporter and folic acid receptor-mediated pluronic P105 polymeric micelles loaded with doxorubicin for brain tumor treating. J Drug Target 2014;22:712-723
[96] Luo MH, Lewik G, Ratcliffe JC, Choi CHJ, Makila E, Tong WY, et al. Systematic evaluation of transferrin-modified porous silicon nanoparticles for targeted delivery of doxorubicin to glioblastoma. ACS Appl Mater Interfaces 2019;11:33637-33649
[97] Jhaveri A, Deshpande P, Pattni B, Torchilin V. Transferrin-targeted, resveratrol-loaded liposomes for the treatment of glioblastoma. J Control Release 2018;277:89-101
[98] Bi YK, Liu LS, Lu YF, Sun T, Shen C, Chen XL, et al. T7 peptide-functionalized PEG-PLGA micelles loaded with carmustine for targeting therapy of glioma. ACS Appl Mater Interfaces 2016;8:27465-27473
[99] Wei L, Guo XY, Yang T, Yu MZ, Chen DW, Wang JC. Brain tumor-targeted therapy by systemic delivery of siRNA with transferrin receptor-mediated core-shell nanoparticles. Int J Pharm 2016;510:394-405
[100] Yu MA, Su DY, Yang YY, Qin L, Hu C, Liu R, et al. D-T7 peptide-modified PEGylated bilirubin nanoparticles loaded with cediranib and paclitaxel for antiangiogenesis and chemotherapy of glioma. ACS Appl Mater Interfaces 2019;11:176-186
[101] Sun P, Xiao Y, Di QQ, Ma WJ, Ma XY, Wang QQ, et al. Transferrin receptor-targeted PEG-PLA polymeric micelles for chemotherapy against glioblastoma multiforme. Int J Nanomed 2020;15:6673-6688
[102] Ramalho MJ, Sevin E, Gosselet F, Lima J, Coelho MAN, Loureiro JA, et al. Receptor-mediated PLGA nanoparticles for glioblastoma multiforme treatment. Int J Pharm 2018;545:84-92
[103] Kang SM, Duan WJ, Zhang SQ, Chen DW, Feng JF, Qi N. Muscone/RI7217 co-modified upward messenger DTX liposomes enhanced permeability of blood-brain barrier and targeting glioma. Theranostics 2020;10:4308-4322
[104] Kim SS, Rait A, Kim E, DeMarco J, Pirollo KF, Chang EH. Encapsulation of temozolomide in a tumor-targeting nanocomplex enhances anti-cancer efficacy and reduces toxicity in a mouse model of glioblastoma. Cancer Lett 2015;369:250-258
[105] Jiang Y, Yang WJ, Zhang J, Meng FH, Zhong ZY. Protein toxin chaperoned by LRP-1-targeted virus-mimicking vesicles induces high-efficiency glioblastoma therapy in vivo. Adv Mater 2018;30:e1800316
[106] Zou Y, Sun XH, Wang YB, Yan CN, Liu YJ, Li J, et al. Single siRNA nanocapsules for effective siRNA brain delivery and glioblastoma treatment. Adv Mater 2020;32:e2000416
[107] Qin HZ, Jiang Y, Zhang J, Deng C, Zhong ZY. Oncoprotein inhibitor rigosertib loaded in ApoE-targeted smart polymersomes reveals high safety and potency against human glioblastoma in mice. Mol Pharm 2019;16:3711-3719
[108] Qian WB, Qian M, Wang Y, Huang JF, Chen J, Ni LC, et al. Combination glioma therapy mediated by a dual-targeted delivery system constructed using OMCN-PEG-Pep22/DOX. Small 2018;14:e1801905
[109] Ruan HT, Chai ZL, Shen Q, Chen XS, Su BX, Xie C, et al. A novel peptide ligand RAP12 of LRP1 for glioma targeted drug delivery. J Control Release 2018;279:306-315
[110] Zhao LZ, Zhu JY, Gong JL, Song NN, Wu S, Qiao WL, et al. Polyethylenimine-based theranostic nanoplatform for glioma-targeting single-photon emission computed tomography imaging and anticancer drug delivery. J Nanobiotechnol 2020;18:143
[111] Mao JN, Ran DN, Xie C, Shen Q, Wang SL, Lu WY. EGFR/EGFRvIII dual-targeting peptide-mediated drug delivery for enhanced glioma therapy. ACS Appl Mater Interfaces 2017;9:24462-24475
[112] Wang SS, Reinhard S, Li CY, Qian M, Jiang HL, Du YL, et al. Antitumoral cascade-targeting ligand for IL-6 receptor-mediated gene delivery to glioma. Mol Ther 2017;25:1556-1566
[113] Kang YJ, Holley CK, Abidian MR, Madhankumar AB, Connor J, Majd S. Tumor targeted delivery of an anti-cancer therapeutic:an in vitro and in vivo evaluation. Adv Healthc Mater 2021;10:e2001261
[114] Hua HC, Zhang XM, Mu HJ, Meng QQ, Jiang Y, Wang YY, et al. RVG29-modified docetaxel-loaded nanoparticles for brain-targeted glioma therapy. Int J Pharm 2018;543:179-189
[115] Ying M, Wang SL, Zhang MF, Wang RF, Zhu HC, Ruan HT, et al. Myristic acid-modified DA7R peptide for whole-process glioma-targeted drug delivery. ACS Appl Mater Interfaces 2018;10:19473-19482
[116] Zhang MF, Chen XS, Ying M, Gao J, Zhan CY, Lu WY. Glioma-targeted drug delivery enabled by a multifunctional peptide. Bioconjugate Chem 2017;28:775-781
[117] Shi KR, Long Y, Xu CQ, Wang Y, Qiu Y, Yu QW, et al. Liposomes combined an integrin alpha(v)beta(3)-specific vector with pH-responsible cell-penetrating property for highly effective antiglioma therapy through the blood-brain barrier. ACS Appl Mater Interfaces 2015;7:21442-21454
[118] Ruan HT, Chen XS, Xie C, Li BB, Ying M, Liu Y, et al. Stapled RGD peptide enables glioma-targeted drug delivery by overcoming multiple barriers. ACS Appl Mater Interfaces 2017;9:17745-17756
[119] Liu AP, Aguet F, Danuser G, Schmid SL. Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J Cell Biol 2010;191:1381-1393
[120] van Rooy I, Mastrobattista E, Storm G, Hennink WE, Schiffelers RM. Comparison of five different targeting ligands to enhance accumulation of liposomes into the brain. J Control Release 2011;150:30-36
[121] Wang SS, Meng Y, Li CY, Qian M, Huang RQ. Receptor-mediated drug delivery systems targeting to glioma. Nanomaterials 2015;6:3
[122] Huang JL, Jiang G, Song QX, Gu X, Hu M, Wang XL, et al. Lipoprotein-biomimetic nanostructure enables efficient targeting delivery of siRNA to Ras-activated glioblastoma cells via macropinocytosis. Nat Commun 2017;8:15144
[123] Liu YY, Ran R, Chen JT, Kuang QF, Tang J, Mei L, et al. Paclitaxel loaded liposomes decorated with a multifunctional tandem peptide for glioma targeting. Biomaterials 2014;35:4835-4847
[124] Liu YY, Mei L, Xu CQ, Yu QW, Shi KR, Zhang L, et al. Dual receptor recognizing cell penetrating peptide for selective targeting, efficient intratumoral diffusion and synthesized anti-glioma therapy. Theranostics 2016;6:177-191
[125] Saalik P, Niinep A, Pae J, Hansen M, Lubenets D, Langel U, et al. Penetration without cells:membrane translocation of cell-penetrating peptides in the model giant plasma membrane vesicles. J Control Release 2011;153:117-125
[126] Jiang XY, Xin HL, Gu JJ, Xu XM, Xia WY, Chen S, et al. Solid tumor penetration by integrin-mediated pegylated poly(trimethylene carbonate) nanoparticles loaded with paclitaxel. Biomaterials. 2013;34:1739-1746
[127] Patching SG. Glucose transporters at the blood-brain barrier:function, regulation and gateways for drug delivery. Mol Neurobiol 2017;54:1046-1077
[128] Jiang XY, Xin HL, Ren QY, Gu JJ, Zhu LJ, Du FY, et al. Nanoparticles of 2-deoxy-D-glucose functionalized poly(ethylene glycol)-co-poly(trimethylene carbonate) for dual-targeted drug delivery in glioma treatment. Biomaterials 2014;35:518-529
[129] Li XY, Zhao Y, Sun MG, Shi JF, Ju RJ, Zhang CX, et al. Multifunctional liposomes loaded with paclitaxel and artemether for treatment of invasive brain glioma. Biomaterials 2014;35:5591-5604
[130] Ju RJ, Mu LM, Li XT, Li CQ, Cheng ZJ, Lu WL. Development of functional docetaxel nanomicelles for treatment of brain glioma. Artif Cells Nanomed Biotechnol 2018;46:S1180-S1190
[131] Li L, Di XS, Zhang SW, Kan QM, Liu H, Lu TS, et al. Large amino acid transporter 1 mediated glutamate modified docetaxel-loaded liposomes for glioma targeting. Colloid Surf B-Biointerfaces 2016;141:260-267
[132] Kou LF, Hou YX, Yao Q, Guo WL, Wang G, Wang ML, et al. L-Carnitine-conjugated nanoparticles to promote permeation across blood-brain barrier and to target glioma cells for drug delivery via the novel organic cation/carnitine transporter OCTN2. Artif Cells Nanomed Biotechnol 2018;46:1605-1616
[133] Kucheryavykh YV, Davila J, Ortiz-Rivera J, Inyushin M, Almodovar L, Mayol M, et al. Targeted delivery of nanoparticulate cytochrome C into glioma cells through the proton-coupled folate transporter. Biomolecules 2019;9:154
[134] Wei XL, Zhan CY, Shen Q, Fu W, Xie C, Gao J, et al. A D-peptide ligand of nicotine acetylcholine receptors for brain-targeted drug delivery. Angew Chem Int Edit. 2015;54:3023-3027
[135] Zheng ZN, Zhang JX, Jiang JZ, He Y, Zhang WY, Mo XP, et al. Remodeling tumor immune microenvironment (TIME) for glioma therapy using multi-targeting liposomal codelivery. J Immunother Cancer 2020;8:e000207
[136] Gao HL, Qian J, Cao SJ, Yang Z, Pang ZQ, Pan SQ, et al. Precise glioma targeting of and penetration by aptamer and peptide dual-functioned nanoparticles. Biomaterials 2012;33:5115-5123
[137] Shen ZY, Liu T, Li Y, Lau J, Yang Z, Fan WP, et al. Fenton-reaction-acceleratable magnetic nanoparticles for ferroptosis therapy of orthotopic brain tumors. ACS Nano 2018;12:11355-11365
[138] Cui YX, Sun JJ, Hao WY, Chen MY, Wang YZ, Xu FH, et al. Dual-target peptide-modified erythrocyte membrane-enveloped PLGA nanoparticles for the treatment of glioma. Front Oncol 2020;10:563938
[139] Zhang M, Asghar S, Tian CH, Hu ZY, Ping QN, Chen ZP, et al. Lactoferrin/phenylboronic acid-functionalized hyaluronic acid nanogels loading doxorubicin hydrochloride for targeting glioma. Carbohydr Polym 2021;253:117194
[140] Ruan SB, Qin L, Xiao W, Hu C, Zhou Y, Wang RR, et al. Acid-responsive transferrin dissociation and GLUT mediated exocytosis for increased blood-brain barrier transcytosis and programmed glioma targeting delivery. Adv Funct Mater 2018;28:1802227
[141] Wu H, Lu HW, Xiao WW, Yang JF, Du HX, Shen YB, et al. Sequential targeting in crosslinking nanotheranostics for tackling the multibarriers of brain tumors. Adv Mater 2020;32:1903759
[142] Hu QY, Kang T, Feng JX, Zhu QQ, Jiang TZ, Yao JH, et al. Tumor microenvironment and angiogenic blood vessels dual-targeting for enhanced anti-glioma therapy. ACS Appl Mater Interfaces 2016;8:23568-23579
[143] Gao JQ, Lv Q, Li LM, Tang XJ, Li FZ, Hu YL, et al. Glioma targeting and blood-brain barrier penetration by dual-targeting doxorubincin liposomes. Biomaterials 2013;34:5628-5639
[144] Zhang Y, Zhai MF, Chen ZJ, Han XY, Yu FL, Li ZP, et al. Dual-modified liposome codelivery of doxorubicin and vincristine improve targeting and therapeutic efficacy of glioma. Drug Deliv 2017;24:1045-1055
[145] Chen CT, Duan ZQ, Yuan Y, Li RX, Pang L, Liang JM, et al. Peptide-22 and cyclic RGD functionalized liposomes for glioma targeting drug delivery overcoming BBB and BBTB. ACS Appl Mater Interfaces 2017;9:5864-5873
[146] Kim JS, Shin DH, Kim JS. Dual-targeting immunoliposomes using angiopep-2 and CD133 antibody for glioblastoma stem cells. J Control Release 2018;269:245-257
[147] Wei XL, Gao J, Zhan CY, Xie C, Chai ZL, Ran D, et al. Liposome-based glioma targeted drug delivery enabled by stable peptide ligands. J Control Release 2015;218:13-21
[148] Ying X, Wen H, Lu WL, Du J, Guo J, Tian W, et al. Dual-targeting daunorubicin liposomes improve the therapeutic efficacy of brain glioma in animals. J Control Release 2010;141:183-192
[149] Lu L, Chen HY, Wang LK, Zhao L, Cheng YN, Wang AJ, et al. A dual receptor targeting- and BBB penetrating-peptide functionalized polyethyleneimine nanocomplex for secretory endostatin gene delivery to malignant glioma. Int J Nanomed 2020;15:8875-8892
[150] Zhao PF, Wang YH, Kang XJ, Wu AH, Yin WM, Tang YS, et al. Dual-targeting biomimetic delivery for anti-glioma activity via remodeling the tumor microenvironment and directing macrophage-mediated immunotherapy. Chem Sci 2018;9:2674-2689
[151] Ye J, Yang YF, Jin J, Ji M, Gao Y, Feng Y, et al. Targeted delivery of chlorogenic acid by mannosylated liposomes to effectively promote the polarization of TAMs for the treatment of glioblastoma. Bioact Mater 2020;5:694-708
[152] Mura S, Nicolas J, Couvreur P. Stimuli-responsive nanocarriers for drug delivery. Nat Mater 2013;12:991-1003
[153] Qiao YT, Wan JQ, Zhou LQ, Ma W, Yang YY, Luo WX, et al. Stimuli-responsive nanotherapeutics for precision drug delivery and cancer therapy. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2019;11:e1527
[154] Da Ros M, De Gregorio V, Iorio AL, Giunti L, Guidi M, de Martino M, et al. Glioblastoma chemoresistance:the double play by microenvironment and blood-brain barrier. Int J Mol Sci 2018;19:2879
[155] Wojtkowiak JW, Verduzco D, Schramm KJ, Gillies RJ. Drug resistance and cellular adaptation to tumor acidic pH microenvironment. Mol Pharm 2011;8:2032-2038
[156] Xu HL, Fan ZL, ZhuGe DL, Tong MQ, Shen BX, Lin MT, et al. Ratiometric delivery of two therapeutic candidates with inherently dissimilar physicochemical property through pH-sensitive core-shell nanoparticles targeting the heterogeneous tumor cells of glioma. Drug Deliv 2018;25:1302-1318
[157] Muniswamy VJ, Raval N, Gondaliya P, Tambe V, Kalia K, Tekade RK. 'Dendrimer-cationized-albumin' encrusted polymeric nanoparticle improves BBB penetration and anticancer activity of doxorubicin. Int J Pharm 2019;555:77-99
[158] Tian Y, Mi GJ, Chen Q, Chaurasiya B, Li YN, Shi D, et al. Acid-induced activated cell-penetrating peptide-modified cholesterol-conjugated polyoxyethylene sorbitol oleate mixed micelles for pH-triggered drug release and efficient brain tumor targeting based on charge reversal mechanism. ACS Appl Mater Interfaces 2018;10:43411-43428
[159] Ma QQ, Long WY, Xing CS, Chu JJ, Luo M, Wang HY, et al. Cancer stem cells and immunosuppressive microenvironment in glioma. Front Immunol 2018;9:2924
[160] Aldea M, Florian IA, Kacso G, Craciun L, Boca S, Soritau O, et al. Nanoparticles for targeting intratumoral hypoxia:exploiting a potential weakness of glioblastoma. Pharm Res 2016;33:2059-2077
[161] Liu HM, Zhang YF, Xie YD, Cai YF, Li BY, Li W, et al. Hypoxia-responsive ionizable liposome delivery siRNA for glioma therapy. Int J Nanomed 2017;12:1065-1083
[162] Liu HM, Xie YD, Zhang YF, Cai YF, Li BY, Mao HL, et al. Development of a hypoxia-triggered and hypoxic radiosensitized liposome as a doxorubicin carrier to promote synergetic chemo-/radio-therapy for glioma. Biomaterials 2017;121:130-143
[163] Hua L, Wang Z, Zhao L, Mao HL, Wang GH, Zhang KR, et al. Hypoxia-responsive lipid-poly-(hypoxic radiosensitized polyprodrug) nanoparticles for glioma chemo- and radiotherapy. Theranostics 2018;8:5088-5105
[164] Andresen TL, Thompson DH, Kaasgaard T. Enzyme-triggered nanomedicine:drug release strategies in cancer therapy. Mol Membr Biol 2010;27:353-363
[165] Chen GH, Yue Y, Qin J, Xiao XP, Ren Q, Xiao B. Plumbagin suppresses the migration and invasion of glioma cells via downregulation of MMP-2/9 expression and inaction of PI3K/Akt signaling pathway in vitro. J Pharmacol Sci 2017;134:59-67
[166] Bruun J, Larsen TB, Jolck RI, Eliasen R, Holm R, Gjetting T, et al. Investigation of enzyme-sensitive lipid nanoparticles for delivery of siRNA to blood-brain barrier and glioma cells. Int J Nanomed 2015;10:5995-6008
[167] Chen YZ, Zhang M, Jin HY, Li DD, Xu F, Wu AH, et al. Glioma dual-targeting nanohybrid protein toxin constructed by intein-mediated site-specific ligation for multistage booster delivery. Theranostics 2017;7:3489-3503
[168] Liu J, Huang YR, Kumar A, Tan A, Jin SB, Mozhi A, et al. pH-sensitive nano-systems for drug delivery in cancer therapy. Biotechnol Adv 2014;32:693-710
[169] Liu YJ, Zou Y, Feng C, Lee A, Yin JL, Chung R, et al. Charge conversional biomimetic nanocomplexes as a multifunctional platform for boosting orthotopic glioblastoma RNA
Similar articles:
1.Caifang Gao, Jianming Liang, Ying Zhu, Chengli Ling, Zhekang Cheng, Ruixiang Li, Jing Qin, Weigen Lu, Jianxin Wang.Menthol-modified casein nanoparticles loading 10-hydroxycamptothecin for glioma targeting therapy[J]. Acta Pharmaceutica Sinica B, 2019,9(4): 843-857
2.Chunhui Ruan, Lisha Liu, Yifei Lu, Yu Zhang, Xi He, Xinli Chen, Yujie Zhang, Qinjun Chen, Qin Guo, Tao Sunn, Chen Jiang.Substance P-modified human serum albumin nanoparticles loaded with paclitaxel for targeted therapy of glioma[J]. Acta Pharmaceutica Sinica B, 2018,8(1): 85-96
3.Xiao Zhao, Rujing Chen, Mei Liu, Jianfang Feng, Jun Chen, Kaili Hu.Remodeling the blood-brain barrier microenvironment by natural products for brain tumor therapy[J]. Acta Pharmaceutica Sinica B, 2017,7(5): 541-553
Similar articles: