Angiopep-2-conjugated liposomes encapsulating γ-secretase inhibitor for targeting glioblastoma stem cells

Journal of Pharmaceutical Investigation

Volumn 44, Issue 7, 2014, Pages 473-483

  Xuan, Shuhua ^a   Shin, Dae Hwan ^a   Kim, Jin Seok ^a  

^a Sookmyung Women's University   (South Korea)

Author keywords

Angiopep 2; CD133; Glioblastoma multiforme; Liposome; Secretase inhibitor

Indexed keywords

ANGIOPEPTIN; CD133 ANTIGEN; CYSTEINE; DIBENZAZEPINE DERIVATIVE; GAMMA SECRETASE INHIBITOR; LIPOSOME; PHYCOERYTHRIN; PLASMA PROTEIN;

AMINO ACID ANALYSIS; ARTICLE; CELL PROLIFERATION ASSAY; CHEMOLUMINESCENCE; DRUG RETENTION; ENCAPSULATION; GENE EXPRESSION; GENE SEQUENCE; GLIOBLASTOMA CELL LINE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN TISSUE; IC50; MTT ASSAY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ZETA POTENTIAL;

EID: 84919442893     PISSN: 20935552     EISSN: 20936214     Source Type: Journal    
DOI: 10.1007/s40005-014-0151-2     Document Type: Article

References (68)

1. Akbarzadeh A, Rezaei-Sadabady R, Davaran S, Joo SW, Zarghami N, Hanifehpour Y, Samiei M, Kouhi M, Nejati-Koshki K (2013) Liposome: classification, preparation, and applications. Nanoscale Res Lett 8:102
2. Bartlett GR (1959) Phosphorus assay in column chromatography. J Biol Chem 234:466–468
3. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
4. Chow TH, Lin YY, Hwang JJ, Wang HE, Tseng YL, Wang SJ, Liu RS, Lin WJ, Yang CS, Ting G (2009) Improvement of biodistribution and therapeutic index via increase of polyethylene glycol on drug-carrying liposomes in an HT-29/luc xenografted mouse model. Anticancer Res 29:2111–2120
5. Cullis PR, Chonn A, Semple SC (1998) Interactions of liposomes and lipid-based carrier systems with blood proteins: relation to clearance behaviour in vivo. Adv Drug Deliv Rev 32:3–17
6. Demeule M, Currie JC, Bertrand Y, Che C, Nguyen T, Regina A, Gabathuler R, Castaigne JP, Beliveau R (2008) Involvement of the low-density lipoprotein receptor-related protein in the transcytosis of the brain delivery vector angiopep-2. J Neurochem 106:1534–1544
7. Ehebauer M, Hayward P, Martinez-Arias A (2006) Notch signaling pathway. Sci STKE 364(2006):7
8. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM, Eberhart CG (2006) Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 66:7445–7452
9. Fan X, Khaki L, Zhu TS, Soules ME, Talsma CE, Gul N, Koh C, Zhang J, Li YM, Maciaczyk J, Nikkhah G, Dimeco F, Piccirillo S, Vescovi AL, Eberhart CG (2010) NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 28:5–16
10. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64:7011–7021
11. Garner JM, Fan M, Yang CH, Du Z, Sims M, Davidoff AM, Pfeffer LM (2013) Constitutive activation of signal transducer and activator of transcription 3 (STAT3) and nuclear factor kappaB signaling in glioblastoma cancer stem cells regulates the Notch pathway. J Biol Chem 288:26167–26176
12. Gref R, Luck M, Quellec P, Marchand M, Dellacherie E, Harnisch S, Blunk T, Muller RH (2000) ‘Stealth’ corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption. Colloids Surf B Biointerfaces 18:301–313
13. Guichet PO, Guelfi S, Teigell M, Hoppe L, Bakalara N, Bauchet L, Duffau H, Lamszus K, Rothhut B, Hugnot JP (2014). Notch1 stimulation induces a vascularization switch with pericyte-like cell differentiation of glioblastoma stem cells. Stem Cells [in press]
14. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100:15178–15183
15. Hovinga KE, Shimizu F, Wang R, Panagiotakos G, Van Der Heijden M, Moayedpardazi H, Correia AS, Soulet D, Major T, Menon J, Tabar V (2010) Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate. Stem Cells 28:1019–1029
16. Hu YY, Zheng MH, Cheng G, Li L, Liang L, Gao F, Wei YN, Fu LA, Han H (2011) Notch signaling contributes to the maintenance of both normal neural stem cells and patient-derived glioma stem cells. BMC Cancer 11:82
17. Hu YY, Fu LA, Li SZ, Chen Y, Li JC, Han J, Liang L, Li L, Ji CC, Zheng MH, Han H (2014) Hif-1alpha and Hif-2alpha differentially regulate Notch signaling through competitive interaction with the intracellular domain of Notch receptors in glioma stem cells. Cancer Lett 349:67–76
18. Huang S, Li J, Han L, Liu S, Ma H, Huang R, Jiang C (2011) Dual targeting effect of Angiopep-2-modified, DNA-loaded nanoparticles for glioma. Biomaterials 32:6832–6838
19. Iso T, Kedes L, Hamamori Y (2003) HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 194:237–255
20. Israelachvili JN, Mitchell DJ (1975) A model for the packing of lipids in bilayer membranes. Biochim Biophys Acta 389:13–19
21. Kirpotin D, Park JW, Hong K, Zalipsky S, Li WL, Carter P, Benz CC, Papahadjopoulos D (1997) Sterically stabilized anti-HER2 immunoliposomes: design and targeting to human breast cancer cells in vitro. Biochemistry 36:66–75
22. Li JL, Sainson RC, Shi W, Leek R, Harrington LS, Preusser M, Biswas S, Turley H, Heikamp E, Hainfellner JA, Harris AL (2007) Delta-like 4 Notch ligand regulates tumor angiogenesis, improves tumor vascular function, and promotes tumor growth in vivo. Cancer Res 67:11244–11253
23. Lian T, Ho RJ (2001) Trends and developments in liposome drug delivery systems. J Pharm Sci 90:667–680
24. Lopes MB, Bogaev CA, Gonias SL, VandenBerg SR (1994) Expression of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein is increased in reactive and neoplastic glial cells. FEBS Lett 338:301–305
25. Louvi A, Artavanis-Tsakonas S (2006) Notch signalling in vertebrate neural development. Nat Rev Neurosci 7:93–102
26. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K (2000) Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release 65:271–284
27. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavenee WK, DePinho RA (2001) Malignant glioma: genetics and biology of a grave matter. Genes Dev 15:1311–1333
28. Mamaeva V, Rosenholm JM, Bate-Eya LT, Bergman L, Peuhu E, Duchanoy A, Fortelius LE, Landor S, Toivola DM, Linden M, Sahlgren C (2011) Mesoporous silica nanoparticles as drug delivery systems for targeted inhibition of Notch signaling in cancer. Mol Ther 19:1538–1546
29. Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT, Bray RA, Waller EK, Buck DW (1997) A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 90:5013–5021
30. Moellering RE, Cornejo M, Davis TN, Del Bianco C, Aster JC, Blacklow SC, Kung AL, Gilliland DG, Verdine GL, Bradner JE (2009) Direct inhibition of the NOTCH transcription factor complex. Nature 462:182–188
31. Ohgaki H, Kleihues P (2005) Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol 64:479–489
32. Pardridge WM (1999) Blood-brain barrier biology and methodology. J Neurovirol 5:556–569
33. Pardridge WM (2005) The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2:3–14
34. Pardridge WM (2007) Drug targeting to the brain. Pharm Res 24:1733–1744
35. Park DM, Rich JN (2009) Biology of glioma cancer stem cells. Mol Cells 28:7–12
36. Purow B (2012) Notch inhibition as a promising new approach to cancer therapy. Adv Exp Med Biol 727:305–319
37. Radtke F, Raj K (2003) The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat Rev Cancer 3:756–767
38. Ren J, Shen S, Wang D, Xi Z, Guo L, Pang Z, Qian Y, Sun X, Jiang X (2012) The targeted delivery of anticancer drugs to brain glioma by PEGylated oxidized multi-walled carbon nanotubes modified with angiopep-2. Biomaterials 33:3324–3333
39. Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105–111
40. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, Kowalski J, Watts RJ, Callahan C, Kasman I, Singh M, Chien M, Tan C, Hongo JA, de Sauvage F, Plowman G, Yan M (2006) Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444:1083–1087
41. Rizzo P, Osipo C, Foreman K, Golde T, Osborne B, Miele L (2008) Rational targeting of Notch signaling in cancer. Oncogene 27:5124–5131
42. Sahebjam S, Bedard PL, Castonguay V, Chen Z, Reedijk M, Liu G, Cohen B, Zhang WJ, Clarke B, Zhang T, Kamel-Reid S, Chen H, Ivy SP, Razak AR, Oza AM, Chen EX, Hirte HW, McGarrity A, Wang L, Siu LL, Hotte SJ (2013) A phase I study of the combination of ro4929097 and cediranib in patients with advanced solid tumours (PJC-004/NCI 8503). Br J Cancer 109:943–949
43. Saito N, Fu J, Zheng S, Yao J, Wang S, Liu DD, Yuan Y, Sulman EP, Lang FF, Colman H, Verhaak RG, Yung WK, Koul D (2014) A high Notch pathway activation predicts response to gamma secretase inhibitors in proneural subtype of glioma tumor-initiating cells. Stem Cells 32:301–312
44. Sanai N, Alvarez-Buylla A, Berger MS (2005) Neural stem cells and the origin of gliomas. N Engl J Med 353:811–822
45. Schott AF, Landis MD, Dontu G, Griffith KA, Layman RM, Krop I, Paskett LA, Wong H, Dobrolecki LE, Lewis MT, Froehlich AM, Paranilam J, Hayes DF, Wicha MS, Chang JC (2013) Preclinical and clinical studies of gamma secretase inhibitors with docetaxel on human breast tumors. Clin Cancer Res 19:1512–1524
46. Shao K, Wu J, Chen Z, Huang S, Li J, Ye L, Lou J, Zhu L, Jiang C (2012) A brain-vectored angiopep-2 based polymeric micelles for the treatment of intracranial fungal infection. Biomaterials 33:6898–6907
47. Shi S, Han L, Gong T, Zhang Z, Sun X (2013) Systemic delivery of microRNA-34a for cancer stem cell therapy. Angew Chem Int Ed Engl 52:3901–3905
48. Shih AH, Holland EC (2006) Notch signaling enhances nestin expression in gliomas. Neoplasia 8:1072–1082
49. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821–5828
50. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432:396–401
51. Sun X, Pang Z, Ye H, Qiu B, Guo L, Li J, Ren J, Qian Y, Zhang Q, Chen J, Jiang X (2012) Co-delivery of pEGFP-hTRAIL and paclitaxel to brain glioma mediated by an angiopep-conjugated liposome. Biomaterials 33:916–924
52. Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R, Gordon SA, Shimada Y, Wang TC (2009) Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 27:1006–1020
53. Telerman A, Amson R (2009) The molecular programme of tumour reversion: the steps beyond malignant transformation. Nat Rev Cancer 9:206–216
54. van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, Clevers H (2005) Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435:959–963
55. Wang L, Rahn JJ, Lun X, Sun B, Kelly JJ, Weiss S, Robbins SM, Forsyth PA, Senger DL (2008) Gamma-secretase represents a therapeutic target for the treatment of invasive glioma mediated by the p75 neurotrophin receptor. PLoS Biol 6:e289
56. Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN, Sullenger BA (2010) Notch promotes radioresistance of glioma stem cells. Stem Cells 28:17–28
57. Wen PY, Kesari S (2008) Malignant gliomas in adults. N Engl J Med 359:492–507
58. Wong GT, Manfra D, Poulet FM, Zhang Q, Josien H, Bara T, Engstrom L, Pinzon-Ortiz M, Fine JS, Lee HJ, Zhang L, Higgins GA, Parker EM (2004) Chronic treatment with the gamma-secretase inhibitor LY-411,575 inhibits beta-amyloid peptide production and alters lymphopoiesis and intestinal cell differentiation. J Biol Chem 279:12876–12882
59. Wu Y, Cain-Hom C, Choy L, Hagenbeek TJ, de Leon GP, Chen Y, Finkle D, Venook R, Wu X, Ridgway J, Schahin-Reed D, Dow GJ, Shelton A, Stawicki S, Watts RJ, Zhang J, Choy R, Howard P, Kadyk L, Yan M, Zha J, Callahan CA, Hymowitz SG, Siebel CW (2010) Therapeutic antibody targeting of individual Notch receptors. Nature 464:1052–1057
60. Xin H, Jiang X, Gu J, Sha X, Chen L, Law K, Chen Y, Wang X, Jiang Y, Fang X (2011) Angiopep-conjugated poly(ethylene glycol)-co-poly(epsilon-caprolactone) nanoparticles as dual-targeting drug delivery system for brain glioma. Biomaterials 32:4293–4305
61. Xin H, Sha X, Jiang X, Chen L, Law K, Gu J, Chen Y, Wang X, Fang X (2012a) The brain targeting mechanism of Angiopep-conjugated poly(ethylene glycol)-co-poly(epsilon-caprolactone) nanoparticles. Biomaterials 33:1673–1681
62. Xin H, Sha X, Jiang X, Zhang W, Chen L, Fang X (2012b) Anti-glioblastoma efficacy and safety of paclitaxel-loading Angiopep-conjugated dual targeting PEG-PCL nanoparticles. Biomaterials 33:8167–8176
63. Yan M, Callahan CA, Beyer JC, Allamneni KP, Zhang G, Ridgway JB, Niessen K, Plowman GD (2010) Chronic DLL4 blockade induces vascular neoplasms. Nature 463:E6–E7
64. Yu Y, Flint A, Dvorin EL, Bischoff J (2002) AC133-2, a novel isoform of human AC133 stem cell antigen. J Biol Chem 277:20711–20716
65. Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS (2004) Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 23:9392–9400
66. Zhang XP, Zheng G, Zou L, Liu HL, Hou LH, Zhou P, Yin DD, Zheng QJ, Liang L, Zhang SZ, Feng L, Yao LB, Yang AG, Han H, Chen JY (2008) Notch activation promotes cell proliferation and the formation of neural stem cell-like colonies in human glioma cells. Mol Cell Biochem 307:101–108
67. Zhang GS, Tian Y, Huang JY, Tao RR, Liao MH, Lu YM, Ye WF, Wang R, Fukunaga K, Lou YJ, Han F (2013) The gamma-secretase blocker DAPT reduces the permeability of the blood-brain barrier by decreasing the ubiquitination and degradation of occludin during permanent brain ischemia. CNS Neurosci Ther 19:53–60
68. Zhu X, Bidlingmaier S, Hashizume R, James CD, Berger MS, Liu B (2010) Identification of internalizing human single-chain antibodies targeting brain tumor sphere cells. Mol Cancer Ther 9:2131–2141