Highly penetrative, drug-loaded nanocarriers improve treatment of glioblastoma

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 29, 2013, Pages 11751-11756

  Zhou, Jiangbing ^a,b   Patel, Toral R ^b   Sirianni, Rachael W ^c   Strohbehn, Garth ^a   Zheng, Ming Qiang ^c   Duong, Nha ^a   Schafbauer, Thomas ^c   Huttner, Anita J ^d   Huang, Yiyun ^c   Carson, Richard E ^a,c   Zhang, Ying ^e   Sullivan, David J ^e   Piepmeier, Joseph M ^b   Saltzman, W Mark ^a  

^a Biomedical Engineering   (United States)

^b Departments of Neurosurgery Anatomical Pathology   (United States)

^c Departments of Diagnostic Radiology   (United States)

^d YALE UNIVERSITY   (United States)

^e JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DITHIAZANINE IODIDE; NANOCARRIER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN SIZE; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; EMISSION TOMOGRAPHY; FLUORESCENCE IMAGING; FOOD AND DRUG ADMINISTRATION; GLIOBLASTOMA; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RAT; SURVIVAL; SWINE;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOOD-BRAIN BARRIER; DITHIAZANINE; DRUG DELIVERY SYSTEMS; FLUORESCENCE; GLIOBLASTOMA; KAPLAN-MEIER ESTIMATE; NANOPARTICLES; POSITRON-EMISSION TOMOGRAPHY; RATS; SWINE;

EID: 84880347703     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1304504110     Document Type: Article

References (64)

1. Mrugala MM, Chamberlain MC (2008) Mechanisms of disease: Temozolomide and glioblastoma - look to the future. Nat Clin Pract Oncol 5(8):476-486.
2. Stupp R, et al.; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987-996.
3. Stupp R, et al.; European Organisation for Research and Treatment of Cancer Brain Tumour and Radiation Oncology Groups; National Cancer Institute of Canada Clinical Trials Group (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10(5):459-466.
4. Hochberg FH, Pruitt A (1980) Assumptions in the radiotherapy of glioblastoma. Neurology 30(9):907-911.
5. Kreuter J (2001) Nanoparticulate systems for brain delivery of drugs. Adv Drug Deliv Rev 47(1):65-81.
6. Pardridge WM (2005) The blood-brain barrier and neurotherapeutics. NeuroRx: The journal of the American Society for Experimental NeuroTherapeutics 2(1)-1-2.
7. Schneider T, et al. (2008) Brain tumor therapy by combined vaccination and antisense oligonucleotide delivery with nanoparticles. J Neuroimmunol 195(1-2):21-27.
8. Wohlfart S, et al. (2011) Treatment of glioblastoma with poly(isohexyl cyanoacrylate) nanoparticles. Int J Pharm 415(1-2):244-251.
9. Brem H, et al. (1991) Interstitial chemotherapy with drug polymer implants for the treatment of recurrent gliomas. J Neurosurg 74(3):441-446.
10. Brem H, et al.; The Polymer-brain Tumor Treatment Group (1995) Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. Lancet 345(8956)-1008-1012.
11. Fung LK, Shin M, Tyler B, Brem H, Saltzman WM (1996) Chemotherapeutic drugs released from polymers: distribution of 1,3-bis(2-chloroethyl)-1- nitrosourea in the rat brain. Pharm Res 13(5):671-682.
12. Fung LK, et al. (1998) Pharmacokinetics of interstitial delivery of carmustine, 4-hydroperoxycyclophosphamide, and paclitaxel from a biodegradable polymer implant in the monkey brain. Cancer Res 58(4):672-684.
13. Bobo RH, et al. (1994) Convection-enhanced delivery of macromolecules in the brain. Proc Natl Acad Sci USA 91(6):2076-2080.
14. Kunwar S, et al.; PRECISE Study Group (2010) Phase III randomized trial of CED of IL13- PE38QQR vs Gliadel wafers for recurrent glioblastoma. Neuro-oncol 12(8):871-881.
15. Sampson JH, et al. (2008) Intracerebral infusion of an EGFR-targeted toxin in recurrent malignant brain tumors. Neuro-oncol 10(3):320-329.
16. Jacobs A, et al. (2001) Positron-emission tomography of vector-mediated gene expression in gene therapy for gliomas. Lancet 358(9283):727-729.
17. Sampson JH, et al.; PRECISE Trial Investigators (2010) Poor drug distribution as a possible explanation for the results of the PRECISE trial. J Neurosurg 113(2):301-309.
18. Allard E, Passirani C, Benoit JP (2009) Convection-enhanced delivery of nanocarriers for the treatment of brain tumors. Biomaterials 30(12):2302-2318.
19. Krauze MT, et al. (2007) Convection-enhanced delivery of nanoliposomal CPT-11 (irinotecan) and PEGylated liposomal doxorubicin (Doxil) in rodent intracranial brain tumor xenografts. Neuro-oncol 9(4):393-403.
20. Sawyer AJ, Piepmeier JM, Saltzman WM (2006) New methods for direct delivery of chemotherapy for treating brain tumors. Yale J Biol Med 79(3-4)-141-152.
21. Sawyer AJ, et al. (2011) Convection-enhanced delivery of camptothecin-loaded polymer nanoparticles for treatment of intracranial tumors. Drug Deliv Transl Res 1(1):34-42.
22. Neeves KB, Sawyer AJ, Foley CP, Saltzman WM, Olbricht WL (2007) Dilation and degradation of the brain extracellular matrix enhances penetration of infused polymer nanoparticles. Brain Res 1180-121-132.
23. Chen MY, et al. (2005) Surface properties, more than size, limiting convective distribution of virus-sized particles and viruses in the central nervous system. J Neurosurg 103(2):311-319.
24. Thorne RG, Nicholson C (2006) In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc Natl Acad Sci USA 103(14): 5567-5572.
25. Hobbs SK, et al. (1998) Regulation of transport pathways in tumor vessels: Role of tumor type and microenvironment. Proc Natl Acad Sci USA 95(8):4607-4612.
26. Snuderl M, et al. (2011) Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 20(6):810-817.
27. Fan X, Salford LG, Widegren B (2007) Glioma stem cells: Evidence and limitation. Semin Cancer Biol 17(3):214-218.
28. Clarke MF (2004) Neurobiology: At the root of brain cancer. Nature 432(7015):281-282.
29. Bao S, et al. (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444(7120):756-760.
30. Calabrese C, et al. (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11(1):69-82.
31. Singh SK, et al. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63(18):5821-5828.
32. Galli R, et al. (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64(19):7011-7021.
33. Singh SK, et al. (2004) Identification of human brain tumour initiating cells. Nature 432(7015):396-401.
34. Yuan X, et al. (2004) Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 23(58):9392-9400.
35. Bao S, et al. (2006) Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66(16):7843-7848.
36. BeierD, et al. (2007) CD133(+) andCD133(-) glioblastoma-derived cancer stemcells show differential growth characteristics and molecular profiles. Cancer Res 67(9):4010-4015.
37. Gunther HS, et al. (2008) Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene 27(20): 2897-2909.
38. Jones RJ, Matsui WH, Smith BD (2004) Cancer stem cells: Are we missing the target? J Natl Cancer Inst 96(8):583-585.
39. Tang C, Chua CL, Ang BT (2007) Insights into the cancer stem cell model of glioma tumorigenesis. Ann Acad Med Singapore 36(5):352-357.
40. Liu G, et al. (2006) Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67.
41. Eramo A, et al. (2006) Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ 13(7)-1238-1241.
42. Hirschmann-Jax C, et al. (2004) A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 101(39)-14228-14233.
43. Abbott A (2006) Cancer: The root of the problem. Nature 442(7104):742-743.
44. Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414(6859)-105-111.
45. Kocbek P, Baumgartner S, Kristl J (2006) Preparation and evaluation of nanosuspensions for enhancing the dissolution of poorly soluble drugs. Int J Pharm 312(1-2)-179-186.
46. Anhorn MG, Mahler HC, Langer K (2008) Freeze drying of human serum albumin (HSA) nanoparticles with different excipients. Int J Pharm 363(1-2)-162-169.
47. Konan YN, Gurny R, Allémann E (2002) Preparation and characterization of sterile and freeze-dried sub-200 nm nanoparticles. Int J Pharm 233(1-2):239-252.
48. Corrigan OI, Li X (2009) Quantifying drug release from PLGA nanoparticulates. Eur J Pharm Sci 37(3-4):477-485.
49. Levin VA, Fenstermacher JD, Patlak CS (1970) Sucrose and inulin space measurements of cerebral cortex in four mammalian species. Am J Physiol 219(5)-1528-1533.
50. Nicholson C, Syková E (1998) Extracellular space structure revealed by diffusion analysis. Trends Neurosci 21(5):207-215.
51. Syková E, Nicholson C (2008) Diffusion in brain extracellular space. Physiol Rev 88(4): 1277-1340.
52. Sirianni RW, Zheng MQ, Huang Y, Saltzman WM, Carson RE (2010) Development of dPET, a non-invasive imaging technique to measure the distribution of drugs after direct delivery to the brain. J Nucl Med 51(Suppl 1):829.
53. Fahmy TM, Samstein RM, Harness CC, Mark Saltzman W (2005) Surface modification of biodegradable polyesters with fatty acid conjugates for improved drug targeting. Biomaterials 26(28):5727-5736.
54. Zheng MQ, et al. (2011) PEG-Biotin labeled nanoparticles for tracking drug delivery and tumor therapy. J Nucl Med 52(Suppl 1):417.
55. Wong K, et al. (2011) Characterization of a human tumorsphere glioma orthotopic model using magnetic resonance imaging. J Neurooncol 104(2):473-481.
56. Lee J, et al. (2006) 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 9(5):391-403.
57. Wolpert F, et al. (2012) HLA-E contributes to an immune-inhibitory phenotype of glioblastoma stem-like cells. J Neuroimmunol 250(1-2):27-34.
58. Chong CR, Chen X, Shi L, Liu JO, Sullivan DJ, Jr. (2006) A clinical drug library screen identifies astemizole as an antimalarial agent. Nat Chem Biol 2(8):415-416.
59. Zhou J, et al. (2009) Cancer stem/progenitor cell active compound 8-quinolinol in combination with paclitaxel achieves an improved cure of breast cancer in the mouse model. Breast Cancer Res Treat 115(2):269-277.
60. Visnyei K, et al. (2011) A molecular screening approach to identify and characterize inhibitors of glioblastoma stem cells. Mol Cancer Ther 10(10)-1818-1828.
61. Saito R, et al. (2006) Tissue affinity of the infusate affects the distribution volume during convection-enhanced delivery into rodent brains: Implications for local drug delivery. J Neurosci Methods 154(1-2):225-232.
62. Verhaak RG, et al.; Cancer Genome Atlas Research Network (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17(1):98-110.
63. Zhou J, Patel TR, Fu M, Bertram JP, Saltzman WM (2012) Octa-functional PLGA nanoparticles for targeted and efficient siRNA delivery to tumors. Biomaterials 33(2): 583-591.
64. Nance EA, et al. (2012) A dense poly(ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue. Sci Transl Med 4(149)-149ra119.