Bubble liposomes and ultrasound enhance the antitumor effects of AG73 liposomes encapsulating antitumor agents

Molecular Pharmaceutics

Volumn 10, Issue 2, 2013, Pages 774-779

  Hamano, Nobuhito ^a   Negishi, Yoichi ^a   Omata, Daiki ^a   Takahashi, Yoko ^a   Manandhar, Maya ^a   Suzuki, Ryo ^b   Maruyama, Kazuo ^b   Nomizu, Motoyoshi ^a   Aramaki, Yukihiko ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b TEIKYO UNIVERSITY   (Japan)

Author keywords

AG73 peptide; Bubble liposomes; drug delivery; liposomes; ultrasound

Indexed keywords

AG73 LIPOSOME; BUBBLE LIPOSOME; DOXORUBICIN; LIPOSOME; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER THERAPY; CELL VIABILITY; CELLULAR DISTRIBUTION; CYTOPLASM; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG RELEASE; DRUG UPTAKE; ENDOSOME; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LOW TEMPERATURE; NANOENCAPSULATION; PRIORITY JOURNAL; ULTRASOUND;

ANTINEOPLASTIC AGENTS; CELL LINE; FLOW CYTOMETRY; HUMANS; LIPOSOMES; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; ULTRASONICS;

EID: 84873387911     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300463h     Document Type: Article

References (45)

1. Perez, A. T.; Domenech, G. H.; Frankel, C.; Vogel, C. L. Pegylated liposomal doxorubicin (Doxil) for metastatic breast cancer: the Cancer Research Network, Inc., experience Cancer Invest. 2002, 20 (Suppl. 2) 22-29 (Pubitemid 35303440)
2. Allen, T. M.; Cullis, P. R. Drug delivery systems: entering the mainstream Science 2004, 303 (5665) 1818-1822 (Pubitemid 38374867)
3. Lukyanov, A. N.; Elbayoumi, T. A.; Chakilam, A. R.; Torchilin, V. P. Tumor-targeted liposomes: doxorubicin-loaded long-circulating liposomes modified with anti-cancer antibody J. Controlled Release 2004, 100 (1) 135-144 (Pubitemid 39445991)
4. Pan, X. G.; Wu, G.; Yang, W. L.; Barth, R. F.; Tjarks, W.; Lee, R. J. Synthesis of cetuximab-immunoliposomes via a cholesterol-based membrane anchor for targeting of EGFR Bioconjugate Chem. 2007, 18 (1) 101-108 (Pubitemid 46145999)
5. Hatakeyama, H.; Akita, H.; Ishida, E.; Hashimoto, K.; Kobayashi, H.; Aoki, T.; Yasuda, J.; Obata, K.; Kikuchi, H.; Ishida, T.; Kiwada, H.; Harashima, H. Tumor targeting of doxorubicin by anti-MT1-MMP antibody-modified PEG liposomes Int. J. Pharm. 2007, 342 (1-2) 194-200 (Pubitemid 47259319)
6. Li, S. D.; Huang, L. Pharmacokinetics and biodistribution of nanoparticles Mol. Pharmaceutics 2008, 5 (4) 496-504
7. Tagami, T.; Ernsting, J. M.; Li, S. D. Efficient tumor regression by a single and low dose treatment with a novel and enhanced formulation of thermosensitive liposomal doxorubicin J. Controlled Release 2011, 152 (2) 303-309
8. Zheng, Y.; Liu, X.; Samoshina, N. M.; Chertkov, V. A.; Franz, A. H.; Guo, X.; Samoshin, V. V. Fliposomes: pH-controlled release from liposomes containing new trans-2-morpholinocyclohexanol-based amphiphiles that perform a conformational flip and trigger an instant cargo release upon acidification Nat. Prod. Commun. 2012, 7 (3) 353-358
9. Negishi, Y.; Hamano, N.; Omata, D.; Fujisawa, A.; Manandhar, M.; Nomizu, M.; Aramaki, Y. Effect of doxorubicin-encupsulating AG73 peptide-modified liposomes on tumor selectively and cytotoxity Results Pharma Sci. 2011, 1 (1) 68-75
10. Carey, D. J. Syndecans: multifunctional cell-surface co-receptors Biochem. J. 1997, 327 (Part 1) 1-16 (Pubitemid 27455453)
11. Hoffman, M, P.; Nomizu, M.; Roque, E.; Lee, S.; Jung, D. W.; Yamada, Y.; Kleinman, H, K. Laminin-1 and laminin-2 G-domain synthetic peptides bind syndecan-1 and are involved in acinar formation of a human submandibular gland cell line J. Biol. Chem. 1998, 273 (44) 28633-28641 (Pubitemid 28507547)
12. Suzuki, N.; Ichikawa, N.; Kasai, S.; Yamada, M.; Nishi, N.; Morioka, H.; Yamashita, H.; Kitagawa, Y.; Utani, A.; Hoffman, M, P.; Nomizu, M. Syndecan binding sites in the laminin alpha1chain G domain Biochemistry 2003, 42 (43) 12625-12633 (Pubitemid 37337553)
13. Han, I.; Park, H.; Oh, E. S. New insights into syndecan-2 expression and tumourigenic activity in colon carcinoma cells J. Mol. Histol. 2004, 35 (3) 319-326 (Pubitemid 40585317)
14. Tkachenko, E.; Rhodes, J, M.; Simons, M. Syndecans: new kids on the signaling block Circ. Res. 2005, 96 (5) 488-500 (Pubitemid 40463457)
15. Essner, J. J.; Chen, E.; Ekker, S. C. Syndecan-2 Int. J. Biochem. Cell Biol. 2006, 38 (2) 152-156 (Pubitemid 41619444)
16. Liu, J.; Lewis, T. N.; Prausnitz, M. R. Non-invasive assessment and control of ultrasound-mediated membrane permeabilization Pharm. Res. 1998, 15 (6) 918-924 (Pubitemid 28307835)
17. Shohet, R. V.; Chen, S.; Zhou, Y. T.; Wang, Z.; Meidell, R. S.; Unger, R. H.; Grayburn, P. A. Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium Circulation 2000, 101 (22) 2554-2556 (Pubitemid 30350631)
18. Cochran, S. A.; Prausnitz, M. R. Sonoluminescence as an indicator of cell membrane disruption by acoustic cavitation Ultrasound Med. Biol. 2001, 27 (6) 841-850 (Pubitemid 32552037)
19. Unger, E. C.; McCreery, T. P.; Sweitzer, R. H.; Caldwell, V. E.; Wu, Y. Acoustically active lipospheres containing paclitaxel: a new therapeutic ultrasound contrast agent Invest. Radiol. 1998, 33 (12) 886-892 (Pubitemid 30247061)
20. Unger, E. C.; Hersh, E.; Vannan, M.; Matsunaga, T. O.; McCreery, T. Local drug and gene delivery through microbubbles Prog. Cardiovasc. Dis. 2001, 44 (1) 45-54 (Pubitemid 32807854)
21. Tachibana, K.; Feril, L. B., Jr.; Ikeda-Dantsuji, Y. Sonodynamic therapy Ultrasonics 2008, 48 (4) 253-259
22. Feril, L. B., Jr.; Tachibana, K. Use of ultrasound in drug delivery systems: emphasis on experimental methodology and mechanisms Int. J. Hyperthermia 2012, 28 (4) 282-289
23. Matsuo, M.; Yamaguchi, K.; Feril, L. B., Jr.; Endo, H.; Ogawa, K.; Tachibana, K.; Nakayama, J. Synergistic inhibition of malignant melanoma proliferation by melphalan combined with ultrasound and microbubbles Ultrason. Sonochem. 2011, 18 (5) 1218-1224
24. O'Reilly, M. A.; Hynynen, K. Ultrasound enhanced drug delivery to the brain and central nervous system Int. J. Hyperthermia 2012, 28 (4) 386-396
25. Suzuki, R.; Takizawa, T.; Negishi, Y.; Hagisawa, K.; Tanaka, K.; Sawamura, K.; Utoguchi, N.; Nishioka, T.; Maruyama, K. Gene delivery by combination of novel liposomal bubbles with perfluoropropane and ultrasound J. Controlled Release 2007, 117 (1) 130-136 (Pubitemid 46161862)
26. Suzuki, R.; Takizawa, T.; Negishi, Y.; Utoguchi, N.; Maruyama, K. Effective gene delivery with novel liposomal bubbles and ultrasonic destruction technology Int. J. Pharm. 2008, 354 (1-2) 49-55
27. Suzuki, R.; Takizawa, T.; Negishi, Y.; Utoguchi, N.; Sawamura, K.; Tanaka, K.; Namai, E.; Oda, Y.; Matsumura, Y.; Maruyama, K. Tumor specific ultrasound enhanced gene transfer in vivo with novel liposomal bubbles J. Controlled Release 2008, 125 (2) 137-144 (Pubitemid 350299602)
28. Negishi, Y.; Matsuo, K.; Endo-Takahashi, Y.; Suzuki, K.; Matsuki, Y.; Takagi, N.; Suzuki, R.; Maruyama, K.; Aramaki, Y. Delivery of an angiogenic gene into ischemic muscle by novel bubble liposomes followed by ultrasound exposure Pharm. Res. 2011, 28 (4) 712-719
29. Negishi, Y.; Tsunoda, Y.; Endo-Takahashi, Y.; Oda, Y.; Suzuki, R.; Maruyama, K.; Yamamoto, M.; Aramaki, Y. Local gene delivery system by bubble liposomes and ultrasound exposure into joint synovium J. Drug Delivery 2011, 2011, 203986
30. Endo-Takahashi, Y.; Negishi, Y.; Kato, Y.; Suzuki, R.; Maruyama, K.; Aramaki, Y. Efficient siRNA delivery using novel siRNA-loaded Bubble liposomes and ultrasound Int. J. Pharm. 2012, 422 (1-2) 504-509
31. Negishi, Y.; Endo-Takahashi, Y.; Matsuki, Y.; Kato, Y.; Takagi, N.; Suzuki, R.; Maruyama, K.; Aramaki, Y. Systemic delivery systems of angiogenic gene by novel bubble liposomes containing cationic lipid and ultrasound exposure Mol. Pharmaceutics 2012, 9 (6) 1834-1840
32. Omata, D.; Negishi, Y.; Hagiwara, S.; Yamamura, S.; Endo-Takahashi, Y.; Suzuki, R.; Maruyama, K.; Nomizu, M.; Aramaki, Y. Bubble liposomes and ultrasound promoted endosomal escape of TAT-PEG liposomes as gene delivery carriers Mol. Pharmaceutics 2011, 8 (6) 2416-2423
33. Omata, D.; Negishi, Y.; Hagiwara, S.; Yamamura, S.; Endo-Takahashi, Y.; Suzuki, R.; Maruyama, K.; Aramaki, Y. Enhanced gene delivery using Bubble liposomes and ultrasound for folate-PEG liposomes J. Drug Targeting 2012, 20 (4) 355-363
34. 2+ and ATP in enhanced gene delivery by bubble liposomes and ultrasound exposure Mol. Pharmaceutics 2012, 9 (4) 1017-1023
35. Dos Santos, N.; Cox, K. A.; McKenzie, C. A.; van Baarda, F.; Gallagher, R. C.; Karlsson, G.; Edwards, K.; Mayer, L. D.; Allen, C.; Bally, M. B. pH gradient loading of anthracyclines into cholesterol-free liposomes: enhancing drug loading rates through use of ethanol Biochim. Biophys. Acta 2004, 1661 (1) 47-60 (Pubitemid 38201570)
36. Negussie, A. H.; Miller, J. L.; Reddy, G.; Drake, S. K.; Wood, B. J.; Dreher, M. R. Synthesis and in vitro evaluation of cyclic NGR peptide targeted thermally sensitive liposome J. Controlled Release 2010, 143 (2) 265-273
37. Negishi, Y.; Omata, D.; Iijima, H.; Takabayashi, Y.; Suzuki, K.; Endo, Y.; Suzuki, R.; Maruyama, K.; Nomizu, M.; Aramaki, Y. Enhanced laminin-derived peptide AG73-mediated liposomal gene transfer by bubble liposomesand ultrasound Mol. Pharmaceutics 2010, 7 (1) 217-226
38. Gabizon, A.; Shmeeda, H.; Horowitz, A. T.; Zalipsky, S. Tumor cell targeting of liposome-entrapped drugs with phospholipid-anchored folic acid-PEG conjugates Adv. Drug Delivery Rev. 2004, 56 (8) 1177-1192 (Pubitemid 38496514)
39. Xiong, X. B.; Huang, Y.; Lu, W. L.; Zhang, X.; Zhang, H.; Nagai, T.; Zhang, Q. Enhanced intracellular delivery and improved antitumor efficacy of doxorubicin by sterically stabilized liposomes modified with a synthetic RGD mimetic J. Controlled Release 2005, 107 (2) 262-275 (Pubitemid 41316289)
40. Suzuki, R.; Takizawa, T.; Kuwata, Y.; Mutoh, M.; Ishiguro, N.; Utoguchi, N.; Shinohara, A.; Eriguchi, M.; Yanagie, H.; Maruyama, K. Effective anti-tumor activity of oxaliplatin encapsulated intransferrin-PEG-liposome Int. J. Pharm. 2008, 346 (1-2) 143-150 (Pubitemid 350101994)
41. Li, C.; Zhang, W.; Fan, W.; Huang, J.; Zhang, F.; Wu, P. Noninvasive treatment of malignant bone tumors using high-intensity focused ultrasound Cancer 2010, 116 (16) 3934-3942
42. Chen, W.; Zhu, H.; Zhang, L.; Li, K.; Su, H.; Jin, C.; Zhou, K.; Bai, J.; Wu, F.; Wang, Z. Primary bone malignancy: effective treatment with high-intensity focused ultrasound ablation Radiology 2010, 255 (3) 967-978
43. Li, Q.; Du, J.; Yu, M.; He, G.; Luo, W.; Li, H.; Zhou, X. Transmission electron microscopy of VX2 liver tumors after high-intensity focused ultrasound ablation enhanced withSonoVue Adv. Ther. 2009, 26 (1) 117-125
44. Luo, W.; Zhou, X.; Yu, M.; He, G.; Zheng, X.; Li, Q.; Liu, Q.; Han, Z.; Zhang, J.; Qian, Y. Ablation of high-intensity focused ultrasound assisted with SonoVue on Rabbit VX2 liver tumors: sequential findings with histopathology, immunohistochemistry, and enzyme histochemistry Ann. Surg. Oncol. 2009, 16 (8) 2359-2368
45. Chung, D. J.; Cho, S. H.; Lee, J. M.; Hahn, S. T. Effect of microbubble contrast agent during high intensity focused ultrasound ablation on rabbit liver in vivo Eur. J. Radiol. 2012, 81 (4) e519-523