Targeting human clonogenic acute myelogenous leukemia cells via folate conjugated liposomes combined with receptor modulation by all-trans retinoic acid

International Journal of Pharmaceutics

Volumn 402, Issue 1-2, 2010, Pages 57-63

  Li, Hong ^a   Lu, Yanhui ^a   Piao, Longzhu ^a   Wu, Jun ^a   Liu, Shujun ^a   Marcucci, Guido ^a,b   Ratnam, Manohar ^c   Lee, Robert J ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF TOLEDO MEDICAL CENTER   (United States)

Author keywords

Acute myeloid leukemia; All trans retinoic acid; Clonogenic cell; Doxorubicin; Folate receptor; Liposomes; Targeted drug delivery

Indexed keywords

CALCEIN; DOXORUBICIN; FOLATE RECEPTOR; FOLATE RECEPTOR BETA; FOLIC ACID; LIPOSOME; RETINOIC ACID; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; BLAST CELL; CELL PROLIFERATION; CLONOGENESIS; CONJUGATION; CONTROLLED STUDY; DISTRIBUTION VOLUME; DRUG CLEARANCE; DRUG CYTOTOXICITY; DRUG DISTRIBUTION; DRUG HALF LIFE; DRUG POTENTIATION; DRUG RECEPTOR BINDING; DRUG TARGETING; FEMALE; HUMAN; HUMAN CELL; LEUKEMIA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; AREA UNDER CURVE; COLONY-FORMING UNITS ASSAY; DOXORUBICIN; DRUG DELIVERY SYSTEMS; FEMALE; FLUORESCEINS; FOLATE RECEPTOR 2; HUMANS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED ICR; TISSUE DISTRIBUTION; TRETINOIN; UP-REGULATION;

EID: 78349310359     PISSN: 03785173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2010.09.019     Document Type: Article

References (36)

1. Bishop J.F. Adult acute myeloid leukemia: update on treatment. Med. J. Aust. 1999, 170:39-43.
2. Blaser B., Gonit M., Qi H., Shatnawi A., Guimond M., Lee R.J., Ratnam M. Induction of folate receptor type β in a bone marrow engraftment model of acute myelogenous leukemia. Leukemia 2007, 21:2233-2235.
3. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3:730-737.
4. Booser D.J., Hortobagyi G.N. Anthracycline antibiotics in cancer therapy Focus on drug resistance. Drugs 1994, 47:223-258.
5. Duncan R. Polymer conjugates as anticancer nanomedicines. Nat. Rev. Cancer 2006, 6:688-701.
6. Gabizon A., Horowitz A.T., Goren D., Tzemach D., Shmeeda H., Zalipsky S. In vivo fate of folate-targeted polyethylene-glycol liposomes in tumor-bearing mice. Clin. Cancer Res. 2003, 9:6551-6559.
7. Gabizon A., Shmeeda H., Horowitz A.T., Zalipsky S. Tumor cell targeting of liposome-entrapped drugs with phospholipidsanchored folic-PEG conjugates. Adv. Drug Deliv. Rev. 2004, 56:1177-1192.
8. Hong K., Kirpotin D.B., Park J.W., Shao Y., Shalaby R., Colbern G., Benz C.C., Papahadjopoulos D. Anti-HER2 immunoliposomes for targeted drug delivery. Ann. N. Y. Acad. Sci. 1999, 886:293-296.
9. Hortoagyi G.N. Anthracyclines in the treatment of cancer: an overview. Drugs 1997, 54:1-7.
10. Jackman A.L., Theti D.S., Gibbs D.D. Antifolates targeted specifically to the drug and gene delivery. Adv. Drug Deliv. Rev. 2004, 56:1111-1125.
11. Jordan C.T., Guzman M.L. Mechanisms controlling pathogenesis and survival of leukemic stem cells. Oncogene 2004, 23:7178-7187.
12. Kamen B.A., Smith A.K. A review of folate receptor α cycling and 5-methyltetrahydrofolate accumulation with an emphasis on cell models in vitro. Adv. Drug Deliv. Rev. 2004, 54:1085-1097.
13. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., Minden M., Paterson B., Caligiuri M.A., Dick J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
14. Lee R.J., Low P.S. Folate-mediated tumor cell targeting of liposome-entrapped doxorubicin in vitro. Biochim. Biophys. Acta 1995, 1233:134-144.
15. List A.F. Role of multidrug resistance and its pharmacological modulation in acute myeloid leukemia. Leukemia 1997, 10:937-942.
16. Lu Y., Wu J., Wu J., Gonit M., Yang X., Lee A., Xiang G., Li H., Liu S., Marcucci G., Ratnam M., Lee R.J. Role of formulation composition in folate receptor-targeted liposomal doxorubicin delivery to acute myelogenous leukemia cells. Mol. Pharm. 2007, 4:707-712.
17. Mayer L.D., Tai L.C., Bally M.B., Mitilenes G.N., Ginsberg R.S., Cullis P.R. Characterization of liposomal systems containing doxorubicin entrapped in response to pH gradients. Biochim. Biophys. Acta 1990, 1025:143-151.
18. Michieli M., Damiani D., Ermacora A., Masolini P., Michelutti A., Michelutti T., Russo D., Pea F., Baccarani M. Liposome-encapsulated daunorubicin for PGP-related multidrug resistance. Br. J. Haematol. 1999, 106:92-99.
19. Michieli M., Damiani D., Ermacora A., Masolini P., Michelutti A., Baccarani M. Liposome encapsulated daunorubicin doubles anthracycline toxicity in cell lines showing a non-PGP related multidrug resistance. Haematologica 1999, 84:1151-1152.
20. Nakamura M., Nagayoshi R., Ijiri K., Nakashima-Matsushita N., Takeuchi T., Matsuyama T. Nitration and chlorination of folic acid by peroxynitrite and hypochlorous acid, and the selective binding of 10-nitro-folate to folate receptor β. Biochem. Biophys. Res. Commun. 2002, 297:1238-1244.
21. Nakashima-Matsushita N., Homma T., Yu S. Selective expression of folate receptor β and its possible role in methotrexate transport in synovial macrophages form patients with rheumatoid arthritis. Arthritis Rheum. 1999, 42:1609-1616.
22. Pan X., Lee R.J. Tumour-selective drug delivery via folate receptor-targeted liposomes. Expert. Opin. Drug Deliv. 2004, 1:7-17.
23. Pan X.Q., Zheng X., Shi G., Wang H., Ratnam M., Lee R.J. Strategy for the treatment of acute myelogenous leukemia based on folate receptor beta-targeted liposomal doxorubicin combined with receptor induction using all-trans retinoic acid. Blood 2002, 100:594-602.
24. Pan X.Q., Wang H., Lee R.J. Antitumor activity of folate receptor-targeted liposomal doxorubicin in a KB oral carcinoma murine xenograft model. Pharm. Res. 2003, 20:417-422.
25. Passegué E., Jamieson C.H., Ailles L.E., Weissman I.L. Normal and leukemic hematopoiesis: are leukemias a stem cell disorder or a reacquisition of stem cell characteristics?. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11842-11849.
26. Qi H., Ratnam M. Synergistic induction of folate receptor beta by all-trans retinoic acid and histone deacetylase inhibitors in acute myelogenous leukemia cells: mechanism and utility in enhancing selective growth inhibition by antifolates. Cancer Res. 2006, 66:5875-5882.
27. Ross J.F., Wang H., Behm F.G. Folate receptor type β is neutrophilic lineage marker and is differentially expressed in myeloid leukemia. Cancer 1999, 85:348-357.
28. Salazar M.D., Ratnam M. The folate receptor: what does it promise in tissue-targeted therapeutics?. Cancer Metastasis Rev. 2007, 26:141-152.
29. Sperr W.R., Hauswirth A.W., Florian S., Ohler L., Geissler K., Valent P. Human leukaemic stem cells: a novel target of therapy. Eur. J. Clin. Invest. 2004, 34:31-40.
30. Taussig D.C., Pearce D.J., Simpson C., Rohatiner A.Z., Lister T.A., Kelly G., Luongo J.L., Danet-Desnoyers G.A., Bonnet D. Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood 2005, 106:4086-4092.
31. van Etten E.W., Snijders S.V., van Vianen W., Bakker-Woudenberg I.A. Superior efficacy of liposomal amphotericin B with prolonged circulation in blood in the treatment of severe candidiasis in leukopenic mice. Antimicrob. Agents. Chemother. 1998, 42:2431-2433.
32. Wang H., Zheng X., Behm F.G., Ratnam M. Differentiation-independent retinoid induction of folate receptor type beta, a potential tumor target in myeloid leukemia. Blood 2000, 96:3529-3536.
33. Xiang G., Wu J., Lu Y., Liu Z., Lee R.J. Synthesis and evaluation of a novel ligand for folate-mediated targeting liposomes. Int. J. Pharm. 2008, 356:29-36.
34. Yan W., Ratnam M. Preferred sites of glycosylphos phatidylino sitol modification in folate receptors and constraints in the hydrophobic portion of the signal. Biochemistry 1995, 34:14594-14600.
35. Yarali N., Tavil B., Kara A., Ozkasap S., Tunç B. Acute renal failure during ATRA treatment. Pediatr. Hematol. Oncol. 2008, 25:115-118.
36. Zhao X.B., Muthusamy N., Byrd J.C., Lee R.J. Cholesterol as a bilayer anchor for PEGylation and targeting ligand in folate-receptor-targeted liposomes. J. Pharm. Sci. 2007, 96:2424-2435.