Loading mitomycin C inside long circulating hyaluronan targeted nano-liposomes increases its antitumor activity in three mice tumor models

International Journal of Cancer

Volumn 108, Issue 5, 2004, Pages 780-789

  Peer, Dan ^a   Margalit, Rimona ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Bioadhesive liposomes; Drug delivery; Hyaluronan; Mitomycin C; Targeting

Indexed keywords

HYALURONIC ACID; LIPOSOME; MITOMYCIN C; NANOLIPOSOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER SURVIVAL; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG DIFFUSION; DRUG DISTRIBUTION; ENCAPSULATION; HUMAN; HUMAN CELL; LUNG METASTASIS; LUNG TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLID TUMOR; TUMOR; TUMOR GROWTH;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTIGENS, CD44; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HYALURONIC ACID; LIPOSOMES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; TUMOR CELLS, CULTURED;

EID: 0347285397     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.11615     Document Type: Article

References (65)

1. O'Regan M, Martini I, Crescenzi F, De Luca C, Lansing M. Molecular mechanisms and genetics of hyaluronan biosynthesis. Int J Biol Macromol 1994;16:283-6.
2. Baker JR, Caterson B. Radioimmunoassay of the link proteins associated with bovine nasal cartilage proteoglycan. J Biol Cheml 1979;254:9369-72.
3. LeBaron RG, Zimmermann DR, Ruoslahti E. Hyaluronate binding properties of versican J Biol Chem 1992;267:10003-10.
4. Rauch U, Karthikeyan, L, Maurel P, Margolis RU, Margolis RK. Cloning and primary structure of neurocan, a developmentally regulated, aggregating chondroitin sulfate proteoglycan of brain. J Biol Chem 1992;267:19536-47.
5. Zöller M. CD44: physiological expression of distinct isoforms as evidence for organ-specific metastasis formation. J Mol Med 1995;73:425-38.
6. Smadja-Joffe F, Legras S, Girard N, Li Y, Delpech B, Bloget F, Morimoto K, Le Bousse-Kerdiles C, Clay D, Jasmin C, Levesque JP. CD44 and hyaluronan binding by human myeloid cells. Leuk Lymphoma 1996;21:407-20.
7. Rudzki Z., Jothy S. CD44 and the adhesion of neoplastic cells. Mol Pathol 1997;50:57-71.
8. Sneath RJ, Mangham DC. The normal structure and function of CD44 and its role in neoplasia. Mol Pathol 1998;51:191-200.
9. Borland G, Ross JA, Guy K. Forms and functions of CD44. Immunology 1998;93:139-48.
10. Herrera-Gayol A, Jothy S. Adhesion proteins in the biology of breast cancer: contribution of CD44. Exp Mol Pathol 1999;66:149-56.
11. Tran TA, Kallakury BV, Sheehan CE, Ross JS. Expression of CD44 standard form and variant isoforms in non-small cell lung carcinomas. Hum Pathol 1997;28:809-14.
12. Fasano M, Sabatini MT, Wieczorek R, Sidhu G, Goswami S., Jagirdar J. CD44 and its v6 spliced variant in lung tumors: a role in histogenesis? Cancer 1997;80:34-41.
13. Gallatin M, St. John TP, Siegelman M, Reichert R, Butcher EC, Weissman IL. Lymphocyte homing receptors. Cell 1986;44:673-80.
14. Li H, Guo L, Li JW, Liu N, Qi R, Liu J. Expression of Hyaluronan receptors CD44 and RHAMM in stomach cancers: relevance with tumor progression. Int J Oncol 2000;17:927-32.
15. Abetamann V, Kern HF, Elsasser HP. Differential expression of the hyaluronan receptors CD44 and RHAMM in human pancreatic cancer cells. Clin Cancer Res 1996;2:1607-18.
16. Ahrens T, Assmann V, Fieber C, Termeer C, Herrlich P, Hofmann M, Simon JC. CD44 is the principal mediator of hyaluronic-acid-induced melanoma cell proliferation. J Invest Dermatol 2001;116:93-101.
17. Ohene-Abuakwa Y, Pignatelli M. Adhesion molecules in cancer biology. Adv Exp Med Biol 2000;465:115-26.
18. Penno MB, August JT, Baylin SB, Mabry M, Linnoila RI, Lee VS, Croteau D, Yang XL, Rosada C. Expression of CD44 in human lung tumors. Cancer Res 1994;54:1381-7.
19. Birch M, Mitchell S, Hart IR. Isolation and characterization of human melanoma cell variants expressing high and low levels of CD44. Cancer Res 1991;51:6660-7.
20. Bartolazzi A, Peach R, Aruffo A, Stamenkovic I. Interaction between CD44 and hyaluronate is directly implicated in the regulation of tumor development. J Exp Med 1994;180:53-66.
21. Lesley J, Hyman R. CD-44 structure and function. Frontiers in Bioscience, 1998;3:D616-30.
22. Zeng C, Toole BP, Kinney SD, Kuo JW, Stamenkovic I. Inhibition of tumor growth in vivo by hyaluronan oligomers. Int J Cancer 1998;77:396-401.
23. Zawadzki V, Perschl A, Rösel M, Hekele A, Zöller M. Blockade of metastasis formation by CD44-receptor globulin. Int J Cancer 1998;75:919-24.
24. Sy MS, Guo YJ, Stamenkovic I. Inhibition of tumor growth in vivo with a soluble CD44-immunoglobulin fusion protein. J Exp Med 1992;176:623-7.
25. Gabizon AA. Pegylated liposomal doxorubicin: metamorphosis of an old drug into a new form of chemotherapy. Cancer Invest 2001;19:424-36.
26. Moghimi SM, Hunter AC, Murray JC. Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol Rev 2001;53:283-318.
27. Forssen AE, Coulter DM, Proffit RC. Selective localization of daunorubicin small unilamellar vesicles in solid tumors. Cancer Res 1992;52:3255-61.
28. Allen TM. Long-circulating (sterically stabilized) liposomes for targeted drug delivery Trends Pharmacol Sci 1994;15:215-20.
29. Oku N, Namba Y. Long-circulating liposomes. Crit Rev Ther Drug Carrier Syst 1994;11:231-70.
30. Tardi P, Choice E, Masin D, Redelmeier T, Bally M, Madden TD. Liposomal encapsulation of topotecan enhances anticancer efficacy in murine and human xenograft models. Cancer Res 2000;60:3389-93.
31. Tseng YL, Hong RL, Tao MH, Chang FH. Sterically stabilized anti-idiotype immunoliposomes improve the therapeutic efficacy of doxorubicin in a murine B-cell lymphoma mode. Int J Cancer 1999;80:723-30.
32. Koning GA, Morselt HW, Gorter A, Allen TM, Zalipsky S, Kamps JA, Scherphof GL. Pharmacokinetics of differently designed immunoliposome formulations in rats with or without hepatic colon cancer metastases. Pharm Res 2001;18:1291-8.
33. Yerushalmi N, Margalit R. Bioadhesive, collagen-modified liposomes: molecular and cellular level studies on the kinetics of drug release and on binding to cell monolayers. Biochim Biophys Acta 1994;1189:13-20.
34. Yerushalmi N, Margalit R. Hyaluronic acid-modified bioadhesive liposomes as local drug depots: effects of cellular and fluid dynamics on liposome retention at target sites. Arch Biochem Biophys 1998;349:21-6.
35. Yerushalmi N, Arad A, Margalit R. Molecular and cellular studies of hyaluronic acid-modified liposomes as bioadhesive carriers for topical drug delivery in wound healing. Arch Biochem Biophys 1994;313:267-73.
36. Margalit R. Liposome-mediated drug targeting in topical and regional therapies. Crit Rev Ther Drug Carrier Syst 1995;12:233-61.
37. Margalit R, Okon M, Yerushalmi N, Avidor E. Bioadhesive liposomes for topical drug delivery: molecular and cellular studies. J Cont Rel 1992;19:275-88.
38. Margalit, R. Bioadhesive liposomes in topical treatment of wounds. In: Cohen S, Berenstein H, eds. Microparticulates: preparation, characterization and application in medicine. New York: Marcel Dekker Inc., 1996, 425-61.
39. Carter SK, Crooke ST. Mitomycin C: current status and new developments. New York: Academic Press, 1979.
40. Hinoshita E, Uchiumi T, Taguchi K, Kinukawa N, Tsuneyoshi M, Sugimachi K, Kuwano M. Increased expression of an ATP-binding cassette superfamily transporter, multidrug resistance Protein 2, in human colorectal carcinomas. Clin Cancer Res 2000;6:2401-7.
41. Dalton JT, Wientjes MG, Badalament RA, Drago JR, Au JL. Pharmacokinetics of intravesical mitomycin C in superficial bladder cancer patients. Cancer Res 1991;51:5144-52.
42. Chang MR, Cheng QI, Lee DA. Basic science and clinical aspects of wound healing in Glaucoma filtering surgery. J Ocul Pharmacol Ther 1998;14:75-95.
43. Tahery MM, Lee DA. Pharmacologic control of wound healing in Glaucoma filtration surgery. J Ocul Pharmacol 1989;5:155-179.
44. Yoshimoto M, Saito M, Tada T, Kasumi KT. Unexpected increase in the bone marrow toxicity of mitomycin C (MMC). Br J Cancer 2001;84:736-7.
45. Tokunaga Y, Kagayama A. Liposomal sustained release delivery systems for intravenous injection. I, Physicochemical and biological properties of newly synthesized lipophilic derivatives of Mitomycin C. Chem Pharmacol Bull 1988;36:3060-9.
46. Sasaki H, Hashida M, Sezaki H. Characterization of liposomes and emulation containing Mitomycin C or lipophilic prodrugs. J Pharm Sci 1986;75:1166-70.
47. Sasaki H, Hashida M, Sezaki H. Absorption characteristics of lipophilic prodrug of Mitomycin C from injected liposomes or an emulsion. J Pharm Sci 1985;37:461-5.
48. Tsai DC, Howard SA, Hogan TF, Malanga CJ, Kandzari SJ, Ma JKH. Preparation and in vitro evaluation of polylactic acid-mitomycin C microcapsules. J Microencapsul 1986;3:181-93.
49. Whateley TL, Eley JG, Kerr DJ, McArdle CS, Anderson J, Vert M, Davis SS. Incorporation of mitomycin C into microspheres of biodegradable poly (lactide-glycolide) co-polymers. Abstr Pap Am Chem Soc 1992;203:59.
50. Cummings J, Allan L, Smyth JF. Encapsulation of mitomycin C in albumin microspheres markedly alters pharmacokinetics. Biochem Pharmacol 1994;47:1345-56.
51. Peer D, Margalit R. Physicochemical evaluation of a stability-driven approach to drug entrapment in regular and in surface-modified liposomes. Arch Biochem Biophys 2000;383:185-90.
52. Peer D, Florentin A, Margalit R. Hyaluronan is a key component of cryoprotection and formulation of targeted unilamellar liposomes. Biochim Biophys Acta 2003;1612:76-82.
53. Hong RL, Huang CJ, Tseng YL, Pang V, Chen ST, Liu JJ, Chang FH. Direct comparison of liposomal doxorubicin with or without polyethylene glycol coating in C-26 tumor-bearing mice: is surface coating with polyethylene glycol beneficial? Clin Cancer Res 1999;5:3645-52.
54. Lin P, Buxton JA, Acheson A, Radziejewski C, Maisonpierre PC, Yancopoulos GD, Channon KM, Hale LP, Dewhirst MW, George SE, Peters KG. Antiangiogenic gene therapy targeting the endothelium-specific receptor tyrosine kinase Tie2. Proc Natl Acad Sci USA 1998;21:8829-34.
55. Goldman Y, Peled A, Shinitzky M. Effective elimination of lung metastases induced by tumor cells treated with hydrostatic pressure and N-acetyl-L-cysteine. Cancer Res 2000;60:350-8.
56. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immun Methods 1983;65:55-63.
57. Samuelsson C, Gustafson S. Studies on the interaction between hyaluronan and a mouse colon cancer cell line. Glycoconj J 1998;15:169-75.
58. Lokeshwar VB, Iida N, Bourguignon LYW. The cell adhesion molecule, GP116, is a new CD44 variant (ex14/v10) involved in hyaluronic acid binding and endothelial cell proliferation. J Biol Chem 1996;271:23853-64.
59. Hofmann M, Fieber C, Assmann V, Gottlicher M, Sleeman J, Plug R, Howells N, von Stein O, Ponta H, Herrlich P. Identification of IHABP, a 95 kDa intracellular hyaluronate binding protein. J Cell Sci 1998;111:1673-84.
60. Eliaz RE, Szoka FC Jr. Liposome-encapsulated doxorubicin targeted to CD44: a strategy to kill CD44-overexpressing tumor cells. Cancer Res 2001;61:2592-601.
61. Karvinen S, Kosma VM, Tammi MI, Tammi R. Hyaluronan, CD44 and versican in epidermal keratinocyte tumours. Br J Dermatol 2003;148:86-94.
62. Emanuel N, Kedar E, Bolotin EM, Smorodinsky NI, Barenholz Y. Targeted delivery of doxorubicin via sterically stabilized immunoliposomes: pharmacokinetics and biodistribution in tumor-bearing mice. Pharm Res 1996;13:861-8.
63. Newman MS, Colbern GT, Working PK, Engbers C, Amantea MA. Comparative pharmacokinetics, tissue distribution, and therapeutic effectiveness of cisplatin encapsulated in long-circulating, pegylated liposomes (SPI-077) in tumor-bearing mice. Cancer Chemother Pharmacol 1999;43:1-7.
64. Charrois JRG, Allen TM. Rate of biodistribution of STEALTH® liposomes to tumor and skin: influence of liposome diameter and implications for toxicity and therapeutic activity. Biochim Biophys Acta 2003;1609:102-8.
65. Junping W, Maitani Y, Takayama K, Nagai T. In vivo evaluation of doxorubicin carried with long circulating and remote loading proliposome. Int J Pharm 2000;203:61-9.