Liposome encapsulation of zoledronic acid results in major changes in tissue distribution and increase in toxicity

Journal of Controlled Release

Volumn 167, Issue 3, 2013, Pages 265-275

  Shmeeda, Hilary ^a   Amitay, Yasmine ^a,b   Tzemach, Dina ^a   Gorin, Jenny ^a   Gabizon, Alberto ^a,b  

^a SHAARE ZEDEK MEDICAL CENTER   (Israel)

^b HEBREW UNIVERSITY   (Israel)

Author keywords

Bisphosphonates; Cancer; Folate receptor; Liposomes; Targeting; Toxicity

Indexed keywords

BISPHOSPHONATES; CANCER; FOLATE-RECEPTOR; LIPOSOMAL FORMULATION; MACROPHAGE/MONOCYTE; TARGETING; THERAPEUTIC ACTIVITY; TISSUE DISTRIBUTIONS;

BONE; DISEASES; PHOSPHOLIPIDS; TOXICITY; TUMORS;

LIPOSOMES;

DOXORUBICIN; LIPOSOME; MACROGOL; PHOSPHATIDYLGLYCEROL; PHOSPHOLIPID; ZOLEDRONIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG DISTRIBUTION; FEMALE; HISTOPATHOLOGY; ISOTOPE LABELING; LIPOPHILICITY; LIPOSOMAL DELIVERY; MACROPHAGE; MONOCYTE; MOUSE; NANOENCAPSULATION; NONHUMAN; PRIORITY JOURNAL; TISSUE DISTRIBUTION;

ANIMALS; BONE DENSITY CONSERVATION AGENTS; DIPHOSPHONATES; FEMALE; FOLIC ACID; IMIDAZOLES; LIPIDS; LIPOSOMES; MICE; MICE, INBRED BALB C; MICE, NUDE; POLYETHYLENE GLYCOLS; TISSUE DISTRIBUTION;

EID: 84874944531     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.02.003     Document Type: Article

References (58)

1. S.P. Luckman, D.E. Hughes, F.P. Coxon, R. Graham, G. Russell, and M.J. Rogers Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras J. Bone Miner. Res. 13 1998 581 589
2. M.J. Rogers, S. Gordon, H.L. Benford, F.P. Coxon, S.P. Luckman, J. Monkkonen, and J.C. Frith Cellular and molecular mechanisms of action of bisphosphonates Cancer 88 2000 2961 2978
3. M.S. Greenberg Intravenous bisphosphonates and osteonecrosis Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 98 2004 259 260
4. I. Benzaid, H. Monkkonen, V. Stresing, E. Bonnelye, J. Green, J. Monkkonen, J.L. Touraine, and P. Clezardin High phosphoantigen levels in bisphosphonate-treated human breast tumors promote Vgamma9Vdelta2 T-cell chemotaxis and cytotoxicity in vivo Cancer Res. 71 2011 4562 4572
5. P. Clezardin Bisphosphonates' antitumor activity: an unravelled side of a multifaceted drug class Bone 48 2011 71 79
6. P. Clezardin, and M. Massaia Nitrogen-containing bisphosphonates and cancer immunotherapy Curr. Pharm. Des. 16 2010 3007 3014
7. J.R. Green, and A. Guenther The backbone of progress-preclinical studies and innovations with zoledronic acid Crit. Rev. Oncol. Hematol. 77 Suppl. 1 2011 S3 S12
8. J.R. Green Bisphosphonates: preclinical review Oncologist 9 Suppl. 4 2004 3 13
9. M. Gnant, B. Mlineritsch, W. Schippinger, G. Luschin-Ebengreuth, S. Postlberger, C. Menzel, R. Jakesz, M. Seifert, M. Hubalek, V. Bjelic-Radisic, H. Samonigg, C. Tausch, H. Eidtmann, G. Steger, W. Kwasny, P. Dubsky, M. Fridrik, F. Fitzal, M. Stierer, E. Rucklinger, R. Greil, and C. Marth Endocrine therapy plus zoledronic acid in premenopausal breast cancer N. Engl. J. Med. 360 2009 679 691
10. F.P. Coxon, K. Thompson, A.J. Roelofs, F.H. Ebetino, and M.J. Rogers Visualizing mineral binding and uptake of bisphosphonate by osteoclasts and non-resorbing cells Bone 42 2008 848 860
11. H. Shmeeda, Y. Amitay, J. Gorin, D. Tzemach, L. Mak, J. Ogorka, S. Kumar, J.A. Zhang, and A. Gabizon Delivery of zoledronic acid encapsulated in folate-targeted liposome results in potent in vitro cytotoxic activity on tumor cells J. Control. Release 146 2010 76 83
12. N. Parker, M.J. Turk, E. Westrick, J.D. Lewis, P.S. Low, and C.P. Leamon Folate receptor expression in carcinomas and normal tissues determined by a quantitative radioligand binding assay Anal. Biochem. 338 2005 284 293
13. A. Gabizon Liposome circulation time and tumor targeting: implications for cancer chemotherapy Adv. Drug Deliv. Rev. 16 1995 285 294
14. H. Maeda The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting Adv. Enzyme Regul. 41 2001 189 207
15. S. Wang, and P.S. Low Folate-mediated targeting of antineoplastic drugs, imaging agents, and nucleic acids to cancer cells J. Control. Release 53 1998 39 48
16. J. Sudimack, and R.J. Lee Targeted drug delivery via the folate receptor Adv. Drug Deliv. Rev. 41 2000 147 162
17. C.P. Leamon, and P.S. Low Delivery of macromolecules into living cells: a method that exploits folate receptor endocytosis Proc. Natl. Acad. Sci. U. S. A. 88 1991 5572 5576
18. R.J. Lee, and P.S. Low Delivery of liposomes into cultured KB cells via folate receptor-mediated endocytosis J. Biol. Chem. 269 1994 3198 3204
19. N. van Rooijen Liposomes for targeting of antigens and drugs: immunoadjuvant activity and liposome-mediated depletion of macrophages J. Drug Target. 16 2008 529 534
20. N. van Rooijen, and E. Hendrikx Liposomes for specific depletion of macrophages from organs and tissues Methods Mol. Biol. 605 2010 189 203
21. H. Epstein-Barash, D. Gutman, E. Markovsky, G. Mishan-Eisenberg, N. Koroukhov, J. Szebeni, and G. Golomb Physicochemical parameters affecting liposomal bisphosphonates bioactivity for restenosis therapy: internalization, cell inhibition, activation of cytokines and complement, and mechanism of cell death J. Control. Release 146 2010 182 195
22. M. Marra, G. Salzano, C. Leonetti, P. Tassone, M. Scarsella, S. Zappavigna, T. Calimeri, R. Franco, G. Liguori, G. Cigliana, R. Ascani, M.I. La Rotonda, A. Abbruzzese, P. Tagliaferri, M. Caraglia, and G. De Rosa Nanotechnologies to use bisphosphonates as potent anticancer agents: the effects of zoledronic acid encapsulated into liposomes Nanomedicine 7 2011 955 964
23. M. McHugh, and Y.C. Cheng Demonstration of a high affinity folate binder in human cell membranes and its characterization in cultured human KB cells J. Biol. Chem. 254 1979 11312 11318
24. M.J. Turk, D.J. Waters, and P.S. Low Folate-conjugated liposomes preferentially target macrophages associated with ovarian carcinoma Cancer Lett. 213 2004 165 172
25. H. Shmeeda, S. Even-Chen, R. Honen, R. Cohen, C. Weintraub, and Y. Barenholz Enzymatic assays for quality control and pharmacokinetics of liposome formulations: comparison with nonenzymatic conventional methodologies Methods Enzymol. 367 2003 272 292
26. A. Gabizon, A.T. Horowitz, D. Goren, D. Tzemach, H. Shmeeda, and S. Zalipsky In vivo fate of folate-targeted polyethylene-glycol liposomes in tumor-bearing mice Clin. Cancer Res. 9 2003 6551 6559
27. J.T. Derksen, H.W. Morselt, and G.L. Scherphof Uptake and processing of immunoglobulin-coated liposomes by subpopulations of rat liver macrophages Biochim. Biophys. Acta 971 1988 127 136
28. S.M. Moghimi, and H.M. Patel Altered tissue-specific opsonic activities and opsono-recognition of liposomes in tumour-bearing rats Biochim. Biophys. Acta 1285 1996 56 64
29. R.E. Coleman, H. Marshall, D. Cameron, D. Dodwell, R. Burkinshaw, M. Keane, M. Gil, S.J. Houston, R.J. Grieve, P.J. Barrett-Lee, D. Ritchie, J. Pugh, C. Gaunt, U. Rea, J. Peterson, C. Davies, V. Hiley, W. Gregory, and R. Bell Breast-cancer adjuvant therapy with zoledronic acid N. Engl. J. Med. 365 2011 1396 1405
30. H. Eidtmann, R. de Boer, N. Bundred, A. Llombart-Cussac, N. Davidson, P. Neven, G. von Minckwitz, J. Miller, N. Schenk, and R. Coleman Efficacy of zoledronic acid in postmenopausal women with early breast cancer receiving adjuvant letrozole: 36-month results of the ZO-FAST Study Ann. Oncol. 21 2010 2188 2194
31. M. Gnant, B. Mlineritsch, H. Stoeger, G. Luschin-Ebengreuth, D. Heck, C. Menzel, R. Jakesz, M. Seifert, M. Hubalek, G. Pristauz, T. Bauernhofer, H. Eidtmann, W. Eiermann, G. Steger, W. Kwasny, P. Dubsky, G. Hochreiner, E.P. Forsthuber, C. Fesl, and R. Greil Adjuvant endocrine therapy plus zoledronic acid in premenopausal women with early-stage breast cancer: 62-month follow-up from the ABCSG-12 randomised trial Lancet Oncol. 12 2011 631 641
32. D. Santini, B. Vincenzi, S. Galluzzo, F. Battistoni, L. Rocci, O. Venditti, G. Schiavon, S. Angeletti, F. Uzzalli, M. Caraglia, G. Dicuonzo, and G. Tonini Repeated intermittent low-dose therapy with zoledronic acid induces an early, sustained, and long-lasting decrease of peripheral vascular endothelial growth factor levels in cancer patients Clin. Cancer Res. 13 2007 4482 4486
33. A. Guenther, S. Gordon, M. Tiemann, R. Burger, F. Bakker, J.R. Green, W. Baum, A.J. Roelofs, M.J. Rogers, and M. Gramatzki The bisphosphonate zoledronic acid has anti-myeloma activity in vivo by inhibition of protein prenylation Int. J. Cancer 126 2010 239 246
34. P.D. Ottewell, D.V. Lefley, S.S. Cross, C.A. Evans, R.E. Coleman, and I. Holen Sustained inhibition of tumour growth and prolonged survival following sequential administration of doxorubicin and zoledronic acid in a breast cancer model Int. J. Cancer 126 2010 522 532
35. A.C. Hirbe, A.J. Roelofs, D.H. Floyd, H. Deng, S.N. Becker, L.G. Lanigan, A.J. Apicelli, Z. Xu, J.L. Prior, M.C. Eagleton, D. Piwnica-Worms, M.J. Rogers, and K. Weilbaecher The bisphosphonate zoledronic acid decreases tumor growth in bone in mice with defective osteoclasts Bone 44 2009 908 916
36. L.M. Mitrofan, J. Pelkonen, and J. Monkkonen The level of ATP analog and isopentenyl pyrophosphate correlates with zoledronic acid-induced apoptosis in cancer cells in vitro Bone 45 2009 1153 1160
37. M.A. Perazella, and G.S. Markowitz Bisphosphonate nephrotoxicity Kidney Int. 74 2008 1385 1393
38. T. Chen, J. Berenson, R. Vescio, R. Swift, A. Gilchick, S. Goodin, P. LoRusso, P. Ma, C. Ravera, F. Deckert, H. Schran, J. Seaman, and A. Skerjanec Pharmacokinetics and pharmacodynamics of zoledronic acid in cancer patients with bone metastases J. Clin. Pharmacol. 42 2002 1228 1236
39. A. Skerjanec, J. Berenson, C. Hsu, P. Major, W.H. Miller Jr., C. Ravera, H. Schran, J. Seaman, and F. Waldmeier The pharmacokinetics and pharmacodynamics of zoledronic acid in cancer patients with varying degrees of renal function J. Clin. Pharmacol. 43 2003 154 162
40. H.M. Weiss, U. Pfaar, A. Schweitzer, H. Wiegand, A. Skerjanec, and H. Schran Biodistribution and plasma protein binding of zoledronic acid Drug Metab. Dispos. 36 2008 2043 2049
41. M. Marra, A. Abbruzzese, R. Addeo, S. Del Prete, P. Tassone, G. Tonini, P. Tagliaferri, D. Santini, and M. Caraglia Cutting the limits of aminobisphosphonates: new strategies for the potentiation of their anti-tumour effects Curr. Cancer Drug Targets 9 2009 791 800
42. A. Gabizon, H. Shmeeda, A.T. Horowitz, and S. Zalipsky Tumor cell targeting of liposome-entrapped drugs with phospholipid-anchored folic acid-PEG conjugates Adv. Drug Deliv. Rev. 56 2004 1177 1192
43. D. Goren, A.T. Horowitz, S. Zalipsky, M.C. Woodle, Y. Yarden, and A. Gabizon Targeting of stealth liposomes to erbB-2 (Her/2) receptor: in vitro and in vivo studies Br. J. Cancer 74 1996 1749 1756
44. A.A. Gabizon, H. Shmeeda, and S. Zalipsky Pros and cons of the liposome platform in cancer drug targeting J. Liposome Res. 16 2006 175 183
45. A. Gabizon, H. Shmeeda, H. Baabur, and R. Satchi-Fainaro Liposomes and polymers in folate-targeted cancer therapeutics A.L. Jackman, C.P. Leamon, Targeted Drug Strategies for Cancer and Inflammation 2011 Springer New York 217 247
46. A. Gabizon, and F. Martin Polyethylene glycol-coated (pegylated) liposomal doxorubicin. Rationale for use in solid tumours Drugs 54 Suppl. 4 1997 15 21
47. T. Minko, R.I. Pakunlu, Y. Wang, J.J. Khandare, and M. Saad New generation of liposomal drugs for cancer Anticancer Agents Med Chem. 6 2006 537 552
48. T.M. Allen, W.W. Cheng, J.I. Hare, and K.M. Laginha Pharmacokinetics and pharmacodynamics of lipidic nano-particles in cancer Anticancer Agents Med Chem. 6 2006 513 523
49. S.W. Canna, and E.M. Behrens Making sense of the cytokine storm: a conceptual framework for understanding, diagnosing, and treating hemophagocytic syndromes Pediatr. Clin. North Am. 59 2012 329 344
50. G. Dicuonzo, B. Vincenzi, D. Santini, G. Avvisati, L. Rocci, F. Battistoni, M. Gavasci, D. Borzomati, R. Coppola, and G. Tonini Fever after zoledronic acid administration is due to increase in TNF-alpha and IL-6 J. Interferon Cytokine Res. 23 2003 649 654
51. M.C. Woodle, and D.D. Lasic Sterically stabilized liposomes Biochim. Biophys. Acta 1113 1992 171 199
52. J. Senior, and G. Gregoriadis Stability of small unilamellar liposomes in serum and clearance from the circulation: the effect of the phospholipid and cholesterol components Life Sci. 30 1982 2123 2136
53. A. Gabizon, M. Chemla, D. Tzemach, A.T. Horowitz, and D. Goren Liposome longevity and stability in circulation: effects on the in vivo delivery to tumors and therapeutic efficacy of encapsulated anthracyclines J. Drug Target. 3 1996 391 398
54. D. Gutman, and G. Golomb Liposomal alendronate for the treatment of restenosis J. Control. Release 161 2012 619 627
55. D. Gutman, H. Epstein-Barash, M. Tsuriel, and G. Golomb Alendronate liposomes for antitumor therapy: activation of gammadelta T cells and inhibition of tumor growth Adv. Exp. Med. Biol. 733 2012 165 179
56. N. Caccamo, S. Meraviglia, F. Scarpa, C. La Mendola, D. Santini, C.T. Bonanno, G. Misiano, F. Dieli, and A. Salerno Aminobisphosphonate-activated gammadelta T cells in immunotherapy of cancer: doubts no more Expert Opin. Biol. Ther. 8 2008 875 883
57. V. Stresing, F. Daubine, I. Benzaid, H. Monkkonen, and P. Clezardin Bisphosphonates in cancer therapy Cancer Lett. 257 2007 16 35
58. K. Sato, S. Kimura, H. Segawa, A. Yokota, S. Matsumoto, J. Kuroda, M. Nogawa, T. Yuasa, Y. Kiyono, H. Wada, and T. Maekawa Cytotoxic effects of gammadelta T cells expanded ex vivo by a third generation bisphosphonate for cancer immunotherapy Int. J. Cancer 116 2005 94 99