LHD-Modified Mechanism-Based Liposome Coencapsulation of Mitoxantrone and Prednisolone Using Novel Lipid Bilayer Fusion for Tissue-Specific Colocalization and Synergistic Antitumor Effects

ACS Applied Materials and Interfaces

Volumn 8, Issue 10, 2016, Pages 6586-6601

  Hu, Tingting ^a   Cao, Hua ^a   Yang, Chengli ^b   Zhang, Lijing ^a   Jiang, Xiaohua ^a   Gao, Xiang ^a   Yang, Fan ^c   He, Gu ^a   Song, Xiangrong ^a   Tong, Aiping ^a   Guo, Gang ^a   Gong, Changyang ^a   Li, Rui ^a   Zhang, Xiaoning ^d   Wang, Xinchun ^e   Zheng, Yu ^a  

^a SICHUAN UNIVERSITY   (China)

^b ZUNYI MEDICAL UNIVERSITY   (China)

^c SICHUAN UNIVERSITY   (China)

^d Tsinghua University   (China)

^e SHIHEZI UNIVERSITY   (China)

Author keywords

coencapsulation liposome; mitoxantrone; prednisolone sodium phosphate; synergistic antitumor effect; tissue specific colocalization

Indexed keywords

CELL DEATH; LIPID BILAYERS; LIPOSOMES; SODIUM; SODIUM COMPOUNDS; TISSUE; TUMORS;

ANTITUMOR EFFECT; CO-ENCAPSULATION; COLOCALIZATION; MITOXANTRONE; SODIUM PHOSPHATE;

DRUG PRODUCTS;

ANTINEOPLASTIC AGENT; LIPID BILAYER; LIPOSOME; MITOXANTRONE; PREDNISOLONE;

ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; DRUG SCREENING; HUMAN; LIPID BILAYER; MALE; METABOLISM; MOUSE; NEOPLASMS, EXPERIMENTAL; PATHOLOGY; PHARMACOLOGY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; HUMANS; LIPID BILAYERS; LIPOSOMES; MALE; MICE; MICE, INBRED BALB C; MITOXANTRONE; NEOPLASMS, EXPERIMENTAL; PREDNISOLONE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84962254333     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b10598     Document Type: Article

References (64)

1. Feldman, E. J.; Lancet, J. E.; Kolitz, J. E.; Ritchie, E. K.; Roboz, G. J.; List, A. F.; Allen, S. L.; Asatiani, E.; Mayer, L. D.; Swenson, C.; Louie, A. C. First-in-man study of CPX-351: A Liposomal Carrier Containing Cytarabine and Daunorubicin in a Fixed 5:1 Molar Ratio for the Treatment of Relapsed and Refractory Acute Myeloid Leukemia J. Clin. Oncol. 2011, 29, 979-985 10.1200/JCO.2010.30.5961
2. Batist, G.; Gelmon, K. A.; Chi, K. N.; Miller, W. H. J.; Chia, S. K.; Mayer, L. D.; Swenson, C. E.; Janoff, A. S.; Louie, A. C. Safety, Pharmacokinetics, and Efficacy of CPX-1 Liposome Injection in Patients with Advanced Solid Tumors Clin. Cancer Res. 2009, 15, 692-700 10.1158/1078-0432.CCR-08-0515
3. Wong, M. Y.; Chiu, G. N. Liposome Formulation of Co-encapsulated Vincristine and Quercetin Enhanced Antitumor Activity in a Trastuzumab-insensitive Breast Tumor Xenograft Model Nanomedicine 2011, 7, 834-840 10.1016/j.nano.2011.02.001
4. Grull, H.; Langereis, S. Hyperthermia-triggered Drug Delivery from Temperature-sensitive Liposomes Using MRI-guided High Intensity Focused Ultrasound J. Controlled Release 2012, 161, 317-327 10.1016/j.jconrel.2012.04.041
5. Miao, L.; Guo, S.; Zhang, J.; Kim, W. Y.; Huang, L. Nanoparticles with Precise Ratiometric Co-Loading and Co-Delivery of Gemcitabine Monophosphate and Cisplatin for Treatment of Bladder Cancer Adv. Funct. Mater. 2014, 24, 6601-6611 10.1002/adfm.201401076
6. Guo, S.; Lin, C. M.; Xu, Z.; Miao, L.; Wang, Y.; Huang, L. Co-delivery of Cisplatin and Rapamycin for Enhanced Anticancer Therapy through Synergistic Effects and Microenvironment Modulation ACS Nano 2014, 8, 4996-5009 10.1021/nn5010815
7. Feng, T.; Tian, H.; Xu, C.; Lin, L.; Xie, Z.; Lam, M. H.; Liang, H.; Chen, X. Synergistic Co-delivery of Doxorubicin and Paclitaxel by Porous PLGA Microspheres for Pulmonary Inhalation Treatment Eur. J. Pharm. Biopharm. 2014, 88, 1086-1093 10.1016/j.ejpb.2014.09.012
8. Soma, C. E.; Dubernet, C.; Bentolila, D.; Benita, S.; Couvreur, P. Reversion of Multidrug Resistance by Co-encapsulation of Doxorubicin and Cyclosporin A in Polyalkylcyanoacrylate Nanoparticles Biomaterials 2000, 21, 1-7 10.1016/S0142-9612(99)00125-8
9. Fu, Q.; Lv, P.; Chen, Z.; Ni, D.; Zhang, L.; Yue, H.; Yue, Z.; Wei, W.; Ma, G. Programmed Co-delivery of Paclitaxel and Doxorubicin Boosted by Camouflaging with Erythrocyte Membrane Nanoscale 2015, 7, 4020-4030 10.1039/C4NR07027E
10. Hu, K.; Zhou, H.; Liu, Y.; Liu, Z.; Liu, J.; Tang, J.; Li, J.; Zhang, J.; Sheng, W.; Zhao, Y.; Wu, Y.; Chen, C. Hyaluronic Acid Functional Amphipathic and Redox-responsive Polymer Particles for the Co-delivery of Doxorubicin and Cyclopamine to Eradicate Breast Cancer Cells and Cancer Stem Cells Nanoscale 2015, 7, 8607-8618 10.1039/C5NR01084E
11. Ma, R.; Wang, Y.; Yan, L.; Ma, L.; Wang, Z.; Chan, H. C.; Chiu, S. K.; Chen, X.; Zhu, G. Efficient Co-delivery of a Pt(IV) Prodrug and a p53 Activator to Enhance the Anticancer Activity of Cisplatin Chem. Commun. (Cambridge, U. K.) 2015, 51, 7859-7862 10.1039/C4CC09879J
12. Tai, W.; Mo, R.; Lu, Y.; Jiang, T.; Gu, Z. Folding Graft Copolymer with Pendant Drug Segments for Co-delivery of Anticancer Drugs Biomaterials 2014, 35, 7194-7203 10.1016/j.biomaterials.2014.05.004
13. Noh, I.; Kim, H. O.; Choi, J.; Choi, Y.; Lee, D. K.; Huh, Y. M.; Haam, S. Co-delivery of Paclitaxel and Gemcitabine via CD44-targeting Nanocarriers as a Prodrug with Synergistic Antitumor Activity Against Human Biliary Cancer Biomaterials 2015, 53, 763-774 10.1016/j.biomaterials.2015.03.006
14. Lancet, J. E.; Cortes, J. E.; Hogge, D. E.; Tallman, M. S.; Kovacsovics, T. J.; Damon, L. E.; Komrokji, R.; Somolon, S. R.; Kolitz, J. E.; Cooper, M.; Yeaqer, A. M.; Louie, A. C.; Feldman, E. J. Phase 2 Trial of CPX-351, a Fixed 5:1 Molar Ratio of Cytarabine/Daunorubicin, vs Cytarabine/Daunorubicin in Older Adults with Untreated AML Blood 2014, 123, 3239-3246 10.1182/blood-2013-12-540971
15. Shaikh, I. M.; Tan, K. B.; Chaudhury, A.; Liu, Y.; Tan, B. J.; Tan, B. M.; Chiu, G. N. Liposome Co-encapsulation of Synergistic Combination of Irinotecan and Doxorubicin for the Treatment of Intraperitoneally Grown Ovarian Tumor Xenograft J. Controlled Release 2013, 172, 852-861 10.1016/j.jconrel.2013.10.025
16. Zhao, X.; Wu, J.; Muthusamy, N.; Byrd, J. C.; Lee, R. J. Liposomal Coencapsulated Fludarabine and Mitoxantrone for Lymphoproliferative Disorder Treatment J. Pharm. Sci. 2008, 97, 1508-1518 10.1002/jps.21046
17. Kumar, K.; Isa, L.; Egner, A.; Schmidt, R.; Textor, M.; Reimhult, E. Formation of Nanopore-spanning Lipid Bilayers Through Liposome Fusion Langmuir 2011, 27, 10920-10928 10.1021/la2019132
18. Dutta, D.; Pulsipher, A.; Luo, W.; Mak, H.; Yousaf, M. N. Engineering Cell Surfaces via Liposome Fusion Bioconjugate Chem. 2011, 22, 2423-2433 10.1021/bc200236m
19. Parker, C.; Waters, R.; Leighton, C.; Hancock, J.; Sutton, R.; Moorman, A. V. et al. Effect of Mitoxantrone on Outcome of Children with First Relapse of Acute Lymphoblastic Leukaemia (ALL R3): An Open-label Randomised Trial Lancet 2010, 376, 2009-2017 10.1016/S0140-6736(10)62002-8
20. Schrappe, M. Mitoxantrone in First-relapse Paediatric ALL: The ALL R3 Trial Lancet 2010, 376, 1968-1970 10.1016/S0140-6736(10)62194-0
21. De Bono, J. S.; Oudard, S.; Ozguroglu, M.; Hansen, S.; Machiels, J. P.; Kocak, I.; Gravis, G.; Bodrogi, I.; Mackenzie, M. J.; Shen, L.; Roessner, M.; Gupta, S.; Sartor, A. O. TROPIC, Investiqators. Prednisone Plus Cabazitaxel or Mitoxantrone for Metastatic Castration-resistant Prostate Cancer Progressing after Docetaxel Treatment: A Randomised Open-label trial Lancet 2010, 376, 1147-1154 10.1016/S0140-6736(10)61389-X
22. Zinzani, P. L.; Tani, M.; Pulsoni, A.; Gobbi, M.; Perotti, A.; De Luca, S.; Fabbri, A.; Zaccaria, A.; Voso, M. T.; Fatori, P.; Guardigni, L.; Ronconi, S.; Cabras, M. G.; Riqacci, L.; De Renzo, A.; Marchi, E.; Stefoni, V.; Fina, M.; Pellegrini, C.; Musuraca, G.; Derenzini, E.; Fanti, S.; Piccaluga, P. P.; Baccarani, M. Fludarabine and Mitoxantrone Followed by Yttrium-90 Ibritumomab Tiuxetan in Previously Untreated Patients with Follicular Non-Hodgkin Lymphoma Trial: A Phase II Non-Randomised Trial (FLUMIZ) Lancet Oncol. 2008, 9, 352-358 10.1016/S1470-2045(08)70039-1
23. Le Deley, M. C.; Suzan, F.; Cutuli, B.; Delaloge, S.; Shamsaldin, A.; Linassier, C.; Clisant, S.; De Vathaire, F.; Fenaux, P.; Hill, C. Anthracyclines, Mitoxantrone, Radiotherapy, and Granulocyte Colony-stimulating Factor: Risk Factors for Leukemia and Myelodysplastic Syndrome after Breast Cancer J. Clin. Oncol. 2007, 25, 292-300 10.1200/JCO.2006.05.9048
24. Link, K. H.; Sunelaitis, E.; Kornmann, M.; Schatz, M.; Gansauge, F.; Leder, G.; Formentini, A.; Staib, L.; Pillasch, J.; Beqer, H. G. Regional Chemotherapy of Nonresectable Colorectal Liver Metastases with Mitoxantrone, 5-fluorouracil, Folinic acid, and Mitomycin C may Prolong Survival Cancer 2001, 92, 2746-2753 10.1002/1097-0142(20011201)92:11<2746::AID-CNCR10098>3.0.CO;2-Q
25. Arseneau, J. C.; Schoenfeld, D. A.; Borden, E. C. A Phase II Study of Dihydroxyanthracenedione (DHAD, mitoxantrone, NSC 301739) in Advanced Malignant Melanoma Invest. New Drugs 1986, 4, 53-56 10.1007/BF00172017
26. Basch, E.; Loblaw, D. A.; Oliver, T. K.; Carducci, M.; Chen, R. C.; Frame, J. N.; Garrels, K.; Hotte, S.; Kattan, M. W.; Raghavan, D.; Saad, F.; Taplin, M. E.; Walker-Dilks, C.; Williams, J.; Winquist, E.; Bennett, C. L.; Wootton, T.; Rumble, R. B.; Dusetzina, S. B.; Virqo, K. S. Systemic Therapy in Men with Metastatic Castration-resistant Prostate Cancer:American Society of Clinical Oncology and Cancer Care Ontario Clinical Practice Guideline J. Clin. Oncol. 2014, 32, 3436-3448 10.1200/JCO.2013.54.8404
27. Herold, M.; Haas, A.; Srock, S.; Neser, S.; Al-Ali, K. H.; Neubauer, A.; Dolken, G.; Naumann, R.; Knauf, W.; Freund, M.; Rohrberg, R.; Hoffken, K.; Franke, A.; Ittel, T.; Kettner, E.; Haak, U.; Mey, U.; Klinkenstein, C.; Assmann, M.; Von Grunhaqen, U. East, German, Study, Group, Hematology, and, Oncology, Study. Rituximab Added to First-line Mitoxantrone, Chlorambucil, and Prednisolone Chemotherapy Followed by Interferon Maintenance Prolongs Survival in Patients with Advanced Follicular Lymphoma: An East German Study Group Hematology and Oncology Study J. Clin. Oncol. 2007, 25, 1986-1992 10.1200/JCO.2006.06.4618
28. Hussain, M.; Rathkopf, D.; Liu, G.; Armstrong, A.; Kelly, W. K.; Ferrari, A.; Hainsworth, J.; Joshi, A.; Hozak, R. R.; Yang, L.; Schwartz, J. D.; Hiqano, C. S. A Randomised Non-comparative Phase II Trial of Cixutumumab (IMC-A12) or Ramucirumab (IMC-1121B) Plus Mitoxantrone and Prednisone in Men with Metastatic Docetaxel-pretreated Castration-resistant Prostate cancer Eur. J. Cancer 2015, 51, 1714-1724 10.1016/j.ejca.2015.05.019
29. Doorduijn, J. K.; Spruit, P.; van Der Holt, B.; van't Veer, M.; Budel, L.; Lowenberg, B.; Sonneveld, P. Etoposide, Mitoxantrone and Prednisone: A Salvage Regimen with Low Toxicity for Refractory or Relapsed Non-Hodgkin's Lymphoma Haematologica 2000, 85, 814-819
30. Carmo-Pereira, J.; Costa, F. O.; Henriques, E. Mitoxantrone, Folinic Acid, 5-fluorouracil and Prednisone as First-line Chemotherapy for Advanced Breast Carcinoma. A phase II study Eur. J. Cancer 1993, 29, 1814-1816 10.1016/0959-8049(93)90527-M
31. Paciucci, P. A.; Keaveney, C.; Cuttner, J.; Holland, J. F. Mitoxantrone, Vincristine, and Prednisone in Adults with Relapsed or Primarily Refractory Acute Lymphocytic Leukemia and Terminal Deoxynucleotidyl Transferase Positive Blastic Phase Chronic Myelocytic Leukemia Cancer Res. 1987, 47, 5234-5237
32. Chung, S. W.; Bae, S. M.; Lee, M.; Al-Hilal, T. A.; Lee, C. K.; Kim, J. K.; Kim, I. S.; Kim, S. Y.; Byun, Y. LHT7, a Chemically Modified Heparin, Inhibits Multiple Stages of Angiogenesis by Blocking VEGF, FGF2 and PDGF-BSignaling Pathways Biomaterials 2015, 37, 271-278 10.1016/j.biomaterials.2014.10.004
33. Park, K.; Lee, G. Y.; Kim, Y. S.; Yu, M.; Park, R. W.; Kim, I. S.; Kim, S. Y.; Byun, Y. Heparin-deoxycholic Acid Chemical Conjugate as an Anticancer Drug Carrier and its Antitumor Activity J. Controlled Release 2006, 114, 300-6 10.1016/j.jconrel.2006.05.017
34. Bae, S. M.; Kim, J. H.; Chung, S. W.; Byun, Y.; Kim, S. Y.; Lee, B. H.; Kim, I. S.; Paek, R. W. An Apoptosis-homing Peptide-conjugated Low Molecular Weight Heparin-taurocholate Conjugate with Antitumor Properties Biomaterials 2013, 34, 2077-2086 10.1016/j.biomaterials.2012.11.020
35. Lee, D. Y.; Kim, S. K.; Kim, Y. S.; Son, D. H.; Nam, J. H.; Kim, I. S.; Park, R. W.; Kim, S. Y.; Byun, Y. Suppression of Angiogenesis and Tumor Growth by Orally Active Deoxycholic Acid-heparin Conjugate J. Controlled Release 2007, 118, 310-317 10.1016/j.jconrel.2006.12.031
36. Belz, K.; Schoeneberger, H.; Wehner, S.; Weigert, A.; Bonig, H.; Klingebiel, T.; Fichtner, I.; Fulda, S. Smac Mimetic and Glucocorticoids Synergize to Induce Apoptosis in Childhood ALL by Promoting Ripoptosome Assembly Blood 2014, 124, 240-250 10.1182/blood-2013-05-500918
37. Frenzel, M.; Steffen-Heins, A. Whey Protein Coating Increases Bilayer Rigidity and Stability of Liposomes in Food-like Matrices Food Chem. 2015, 173, 1090-1099 10.1016/j.foodchem.2014.10.076
38. Tan, H.; Liu, B.; Chen, Y. Lanthanide Coordination Polymer Nanoparticles for Sensing of Mercury(II) by Photoinduced Electron Transfer ACS Nano 2012, 6, 10505-10511
39. Mishra, R. K.; Rajeswari, M. R.; Singhal, G. S. Fusion of Phosphatidylcholine Liposomes Induced by Polyethylene Glycol Biochem Int. 1988, 16, 1137-1144
40. Kim, D. H.; Termsarasab, U.; Cho, H. J.; Yoon, I. S.; Lee, J. Y.; Moon, H. T.; Kim, D. D. Preparation and Characterization of Self-assembled Nanoparticles Based on Low-molecular-weight Heparin and Stearylamine Conjugates for Controlled Delivery of Docetaxel Int. J. Nanomed. 2014, 9, 5711-5727 10.2147/IJN.S74353
41. Smith, P. K.; Mallia, A. K.; Hermanson, G. T. Colorimetric Method for the Assay of Heparin Content in Immobilized Heparin Preparations Anal. Biochem. 1980, 109, 466-473 10.1016/0003-2697(80)90679-X
42. Kim, J. Y.; Shim, G.; Choi, H. W.; Park, J.; Chung, S. W.; Kim, S.; Kim, K.; Kwon, I. C.; Kim, C. W.; Kim, S. Y.; Yang, V. C.; Oh, Y. K. Tumor Vasculature Targeting Following Co-delivery of Heparin-taurocholate Conjugate and Suberoylanilide Hydroxamic Acid Using Cationic Nanolipoplex Biomaterials 2012, 33, 4424-4430 10.1016/j.biomaterials.2012.02.066
43. Bhalla, K.; Ibrado, A. M.; Tourkina, E.; Tang, C.; Grant, S.; Bullock, G.; Huang, Y.; Ponnathpur, V.; Mahoney, M. E. High-dose Mitoxantrone Induces Programmed Cell Death or Apoptosis in Human Myeloid Leukemia Cells Blood 1993, 82, 3133-3140
44. Bornhauser, B. C.; Bonapace, L.; Lindholm, D.; Martinez, R.; Cario, G.; Schrappe, M.; Niqqli, F. K.; Schafer, B. W.; Bourquin, J. P. Low-dose Arsenic Trioxide Sensitizes Glucocorticoid-resistant Acute Lymphoblastic Leukemia Cells to Dexamethasone via an Akt-dependent Pathway Blood 2007, 110, 2084-2091 10.1182/blood-2006-12-060970
45. Piovan, E.; Yu, J.; Tosello, V.; Herranz, D.; Ambesi-Impiombato, A.; Da Silva, A. C.; Scnchz-Martin, M.; Perez-Garcia, A.; Rigo, I.; Castillo, M.; Indraccolo, S.; Cross, J. R.; De Stanchina, E.; Paietta, E.; Racevskis, J.; Rowe, J. M.; Tallman, M. S.; Basso, G.; Meijierink, J. P.; Cordon-Cardo, C.; Ferrando, A. A. Direct Reversal of Glucocorticoid Resistance by AKT Inhibition in Acute Lymphoblastic Leukemia Cancer Cell 2013, 24, 766-776 10.1016/j.ccr.2013.10.022
46. Wei, G.; Twomey, D.; Lamb, J.; Schlis, K.; Agarwal, J.; Stam, R. W.; Opferman, J. T.; Sallan, S. E.; Der Boer, M. L.; Pieters, R.; Golub, T. R.; Amrmstrong, S. A. Gene Expression-based Chemical Genomics Identifies Rapamycin as a Modulator of MCL1 and Glucocorticoid Resistance Cancer Cell 2006, 10, 331-342 10.1016/j.ccr.2006.09.006
47. Beesley, A. H.; Firth, M. J.; Ford, J.; Weller, R. E.; Freitas, J. R.; Perera, K. U.; Kees, U. R. Glucocorticoid Resistance in T-lineage Acute Lymphoblastic Leukaemia is Associated with a Proliferative Metabolism Br. J. Cancer 2009, 100, 1926-1936 10.1038/sj.bjc.6605072
48. Datta, S. R.; Dudek, H.; Tao, X.; Masters, S.; Fu, H.; Gotoh, Y.; Greenberg, M. E. Akt Phosphorylation of BAD Couples Survival Signals to the Cell-intrinsic Death Machinery Cell 1997, 91, 231-241 10.1016/S0092-8674(00)80405-5
49. Pinto, A. C.; Moreira, J. N.; Simoes, S. Liposomal Imatinib-mitoxantrone Combination: Formulation Development and Therapeutic Evaluation in an Animal Model of Prostate Cancer Prostate 2011, 71, 81-90 10.1002/pros.21224
50. Park, J. W.; Jeon, O. C.; Kim, S. K.; Al-Hilal, T. A.; Lim, K. M.; Moon, H. T.; Kim, C. Y.; Byun, Y. Pharmacokinetic Evaluation of an Oral Tablet form of Low-molecular-weight Heparin and Deoxycholic Acid Conjugate as a Novel Oral Anticoagulant Thromb. Haemostasis 2011, 105, 1060-1071 10.1160/TH10-07-0484
51. Oehlers, S. H.; Cronan, M. R.; Scott, N. R.; Thomas, M. I.; Okuda, K. S.; Walton, E. M.; Beerman, R. W.; Crosier, P. S.; Tobin, D. M. Interception of Host Angiogenic Signalling Limits Mycobacterial Growth Nature 2014, 517, 612-615 10.1038/nature13967
52. Park, K.; Kim, K.; Kwon, I. C.; Kim, S. K.; Lee, S.; Lee, D. Y.; Byun, Y. Preparation and Characterization of Self-assembled Nanoparticles of Heparin-deoxycholic Acid Conjugates Langmuir 2004, 20, 11726-11731 10.1021/la048646i
53. Cho, K. J.; Moon, H. T.; Park, G. E.; Jeon, O. C.; Byun, Y.; Lee, Y. K. Preparation of Sodium Deoxycholate (DOC) Conjugated Heparin Derivatives for Inhibition of Angiogenesis and Cancer Cell Growth Bioconjugate Chem. 2008, 19, 1346-1351 10.1021/bc800173m
54. Qhattal, H. S.; Hye, T.; Alali, A.; Liu, X. Hyaluronan Polymer Length, Grafting Density, and Surface Poly(ethylene glycol) Coating Influence in vivo Circulation and Tumor Targeting of Hyaluronan-grafted Liposomes ACS Nano 2014, 8, 5423-5440 10.1021/nn405839n
55. Rathmell, J. C.; Fox, C. J.; Plas, D. R.; Hammerman, P. S.; Cinalli, R. M.; Thompson, C. B. Akt Directed Glucose Metabolism Can Prevent Bax Conformation Change and Promote Growth Factor Independent Survival Mol. Cell. Biol. 2003, 23 (20) 7315-7328 10.1128/MCB.23.20.7315-7328.2003
56. Mirjanian, D.; Dickey, A. N.; Hoh, J. H.; Woolf, T. B.; Stevens, M. J. Splaying of Aliphatic Tails Plays a Central Role in Barrier Crossing During Liposome Fusion J. Phys. Chem. B 2010, 114, 11061-11068 10.1021/jp1055182
57. Kasson, P. M.; Kelley, N. W.; Singhal, N.; Vrljic, M.; Brunger, A. T.; Pande, V. S. Ensemble Molecular Dynamics Yields Submillisecond Kinetics and Intermediates of Membrane Fusion Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 11916-11921 10.1073/pnas.0601597103
58. Tsai, H. H.; Chang, C. M.; Lee, J. B. Multi-step Formation of a Hemifusion Diaphragm for Vesicle Fusion Revealed by All-atom Molecular Dynamics Simulations Biochim. Biophys. Acta, Biomembr. 2014, 1838, 1529-1535 10.1016/j.bbamem.2014.01.018
59. Dass, C. R. Improving Anti-angiogenic Therapy via Selective Delivery of Cationic Liposomes to Ttumour Vasculature Int. J. Pharm. 2003, 267, 1-12 10.1016/j.ijpharm.2003.08.010
60. Fildes, F. J.; Oliver, J. E. Interaction of Cortisol-21-palmitate with Liposomes Examined by Differential Scanning Calorimetry J. Pharm. Pharmacol. 1978, 30, 337-342 10.1111/j.2042-7158.1978.tb13251.x
61. Ugwu, S.; Zhang, A.; Parmar, M.; Miller, B.; Sardone, T.; Peikov, V.; Ahmad, I. Preparation, Characterization, and Stability of Liposome-based Formulations of Mitoxantrone Drug Dev. Ind. Pharm. 2005, 31, 223-229 10.1081/DDC-200047850
62. Li, C.; Cui, J.; Li, Y.; Wang, C.; Li, Y.; Zhang, L.; Guo, W.; Wang, J.; Zhang, H.; Hao, Y.; Wang, Y. Copper Ion-mediated Liposomal Encapsulation of Mitoxantrone: The Role of Anions in Drug Loading, Retention and Release Eur. J. Pharm. Sci. 2008, 34, 333-344 10.1016/j.ejps.2008.05.006
63. Crielaard, B. J.; Yousefi, A.; Schillemans, J. P.; Vermehren, C.; Buyens, K.; Braeckmans, K.; Lammers, T.; Storm, G. An in Vitro Assay Based on Surface Plasmon Resonance to Predict the in Vivo Circulation Kinetics of Liposomes J. Controlled Release 2011, 156, 307-314 10.1016/j.jconrel.2011.07.023
64. Strieth, S.; Dunau, C.; Michaelis, U.; Jager, L.; Gellrich, D.; Wollenberg, B.; Dellian, M. Phase I/II Clinical Study on Safety and Antivascular Effects of Paclitaxel Encapsulated in Cationic Liposomes for Targeted Therapy in Advanced Head and Neck Cancer Head Neck Oncol. 2014, 36, 976-984 10.1002/hed.23397