Liposomal alendronate for the treatment of restenosis

Journal of Controlled Release

Volumn 161, Issue 2, 2012, Pages 619-627

  Gutman, Dikla ^a   Golomb, Gershon ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Bisphosphonate; Inflammation; Liposome; Monocytes macrophages; Restenosis

Indexed keywords

ALENDRONATE; ANTI-INFLAMMATORY EFFECTS; BALLOON ANGIOPLASTY; BIODISTRIBUTIONS; BISPHOSPHONATES; CLINICAL TRIAL; CURRENT TREATMENTS; DRUG-ELUTING STENTS; FORMULATION DEVELOPMENT; IN-VITRO; INFLAMMATION; INNATE IMMUNITY; MONOCYTES/MACROPHAGES; PERCUTANEOUS CORONARY INTERVENTION; PHASE II; RESTENOSIS; SYSTEMIC APPROACH; VASCULAR INJURY; WOUND HEALING;

DRUG PRODUCTS; INTERFACES (COMPUTER); LIPOSOMES; PATHOLOGY; STENTS;

DISEASES;

ALENDRONIC ACID; CLODRONIC ACID; CYPHER; ETIDRONIC ACID; IBANDRONIC ACID; LIPOSOME; MINODRONIC ACID; NANOCARRIER; PACLITAXEL; PAMIDRONIC ACID; RAPAMYCIN; RISEDRONIC ACID; UNCLASSIFIED DRUG; ZOLEDRONIC ACID;

ANTIINFLAMMATORY ACTIVITY; BLOOD VESSEL INJURY; CELL DEATH; CELL PROLIFERATION; COMPLEMENT ACTIVATION; CORONARY ARTERY OBSTRUCTION; CYTOKINE RELEASE; DRUG CLEARANCE; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG ELUTING STENT; DRUG FORMULATION; DRUG HALF LIFE; ENCAPSULATION; HUMAN; HYPERCHOLESTEROLEMIA; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LIPOSOMAL DELIVERY; MACROPHAGE; MONOCYTE; NONHUMAN; OSTEOLYSIS; PERCUTANEOUS CORONARY INTERVENTION; PRIORITY JOURNAL; RESTENOSIS; REVIEW; SMOOTH MUSCLE FIBER;

ALENDRONATE; ANIMALS; BONE DENSITY CONSERVATION AGENTS; CORONARY RESTENOSIS; HUMANS; LIPOSOMES; MACROPHAGES; MONOCYTES;

EID: 84862688093     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2011.11.037     Document Type: Review

References (108)

1. L. Brito, M. Amiji, Nanoparticulate carriers for the treatment of coronary restenosis, Int. J. Nanomedicine 2 (2) (2007) 143-161.
2. A.M. Minino, J. Xu, K.D. Kochanek, B. Tejada-Vera, Death in the United States, 2007, NCHS Data Brief 26 (2009) 1-8.
3. G.D. Dangas, B.E. Claessen, A. Caixeta, E.A. Sanidas, G.S. Mintz, R. Mehran, Instent restenosis in the drug-eluting stent era, J. Am. Coll. Cardiol. 56 (23) (2010) 1897-1907.
4. A. Kastrati, J. Mehilli, J. Dirschinger, J. Pache, K. Ulm, H. Schuhlen, M. Seyfarth, C. Schmitt, R. Blasini, F.J. Neumann, A. Schomig, Restenosis after coronary placement of various stent types, Am. J. Cardiol. 87 (1) (2001) 34-39.
5. S. Elezi, A. Kastrati, M. Hadamitzky, J. Dirschinger, F.J. Neumann, A. Schomig, Clinical and angiographic follow-up after balloon angioplasty with provisional stenting for coronary in-stent restenosis, Catheter. Cardiovasc. Interv. 48 (2) (1999) 151-156.
6. M.A. Ferguson, M. Needleman, E.S. Mitchell, L.I. Carter, A.I. Bustamante, K.M. Love, M.J. Curran, A history of prior bare metal stent restenosis is associated with major adverse cardiac events in subsequent bare metal stenting of de novo coronary lesions, Cardiology 116 (3) (2010) 190-193.
7. T. Inoue, K. Node, Molecular basis of restenosis and novel issues of drug-eluting stents, Circ. J. 73 (4) (2009) 615-621.
8. D.P. Faxon, Systemic drug therapy for restenosis - "deja vu all over again", Circulation 106 (18) (2002) 2296-2298.
9. S.M. Garas, P. Huber, N.A. Scott, Overview of therapies for prevention of restenosis after coronary interventions, Pharmacol. Ther. 92 (2-3) (2001) 165-178.
10. S.O. Marx, T. Jayaraman, L.O. Go, A.R. Marks, Rapamycin-FKBP inhibits cell cycle regulators of proliferation in vascular smooth muscle cells, Circ. Res. 76 (3) (1995) 412-417.
11. M. Poon, S.O. Marx, R. Gallo, J.J. Badimon, M.B. Taubman, A.R. Marks, Rapamycin inhibits vascular smooth muscle cell migration, J. Clin. Invest. 98 (10) (1996) 2277-2283.
12. G.W. Stone, S.G. Ellis, D.A. Cox, J. Hermiller, C. O'Shaughnessy, J.T. Mann, M. Turco, R. Caputo, P. Bergin, J. Greenberg, J.J. Popma, M.E. Russell, A polymer-based, paclitaxel-eluting stent in patients with coronary artery disease, N. Engl. J. Med. 350 (3) (2004) 221-231.
13. S.J. Park, W.H. Shim, D.S. Ho, A.E. Raizner, S.W. Park, M.K. Hong, C.W. Lee, D. Choi, Y. Jang, R. Lam, N.J. Weissman, G.S. Mintz, A paclitaxel-eluting stent for the prevention of coronary restenosis, N. Engl. J. Med. 348 (16) (2003) 1537-1545.
14. G.W. Stone, S.G. Ellis, A. Colombo, K.D. Dawkins, E. Grube, D.E. Cutlip, M. Friedman, D.S. Baim, J. Koglin, Offsetting impact of thrombosis and restenosis on the occurrence of death and myocardial infarction after paclitaxeleluting and bare metal stent implantation, Circulation 115 (22) (2007) 2842-2847.
15. G. McDowell, M. Slevin, J. Krupinski, Nanotechnology for the treatment of coronary in stent restenosis: a clinical perspective, Vasc. Cell 3 (1) (2011) 8.
16. B. Godin, J.H. Sakamoto, R.E. Serda, A. Grattoni, A. Bouamrani, M. Ferrari, Emerging applications of nanomedicine for the diagnosis and treatment of cardiovascular diseases, Trends Pharmacol. Sci. 31 (5) (2010) 199-205.
17. D.N. Patel, S.R. Bailey, Nanotechnology in cardiovascular medicine, Catheter. Cardiovasc. Interv. 69 (5) (2007) 643-654.
18. R. Ross, Mechanisms of disease - atherosclerosis - an inflammatory disease, N. Engl. J. Med. 340 (2) (1999) 115-126.
19. K. Toutouzas, A. Colombo, C. Stefanadis, Inflammation and restenosis after percutaneous coronary interventions, Eur. Heart J. 25 (19) (2004) 1679-1687.
20. F.G. Welt, E.R. Edelman, C. Rogers, Neutrophil, not macrophage, infiltration precedes neointimal thickening after endothelial denudation, Circulation 100 (18) (1999) 541.
21. F. Welt, C. Tso, E. Edelman, M. Kjelsberg, J. Paolini, P. Seifert, C. Rogers, Leukocyte recruitment and expression of chemokines following different forms of vascular injury, Vasc. Med. 8 (2003) 1-7.
22. H. Tanaka, G.K. Sukhova, S.J. Swanson, S.K. Clinton, P. Ganz, M.I. Cybulsky, P. Libby, Sustained activation of vascular cells and leukocytes in the rabbit aorta after balloon injury, Circulation 88 (4 Pt 1) (1993) 1788-1803.
23. C. Rogers, F.G. Welt, M.J. Karnovsky, E.R. Edelman, Monocyte recruitment and neointimal hyperplasia in rabbits. Coupled inhibitory effects of heparin, Arterioscler. Thromb. Vasc. Biol. 16 (10) (1996) 1312-1318.
24. F.G.P. Welt, E.R. Edelman, D.I. Simon, C. Rogers, Neutrophil, not macrophage, infiltration precedes neointimal thickening in balloon-injured arteries, Arterioscler. Thromb. Vasc. Biol. 20 (12) (2000) 2553-2558.
25. F.J. Neumann, I. Ott, M. Gawaz, G. Puchner, A. Schomig, Neutrophil and platelet activation at balloon-injured coronary artery plaque in patients undergoing angioplasty, J. Am. Coll. Cardiol. 27 (4) (1996) 819-824.
26. J.K. Mickelson, N.M. Lakkis, G. VillarrealLevy, B.J. Hughes, C.W. Smith, Leukocyte activation with platelet adhesion after coronary angioplasty: a mechanism for recurrent disease? J. Am. Coll. Cardiol. 28 (2) (1996) 345-353.
27. T. Inoue, Y. Sakai, S. Morooka, T. Hayashi, K. Takayanagi, Y. Takabatake, Expression of polymorphonuclear leukocyte adhesion molecules and its clinical significance in patients treated with percutaneous transluminal coronary angioplasty, J. Am. Coll. Cardiol. 28 (5) (1996) 1127-1133.
28. T. Inoue, R. Sohma, T. Miyazaki, Y. Iwasaki, I. Yaguchi, S. Morooka, Comparison of activation process of platelets and neutrophils after coronary stent implantation versus balloon angioplasty for stable angina pectoris, Am. J. Cardiol. 86 (10) (2000) 1057-1062.
29. S. Hokimoto, Y. Oike, T. Saito, M. Kitaoka, S. Oshima, K. Noda, Y. Moriyama, F. Ishibashi, H. Ogawa, Increased expression of monocyte chemoattractant protein-1 in atherectomy specimens from patients with restenosis after percutaneous transluminal coronary angioplasty, Circulation 66 (1) (2002) 114-116.
30. P.R. Moreno, V.H. Bernardi, J. LopezCuellar, J.B. Newell, C. McMellon, H.K. Gold, I.F. Palacios, V. Fuster, J.T. Fallon, Macrophage infiltration predicts restenosis after coronary intervention in patients with unstable angina, Circulation 94 (12) (1996) 3098-3102.
31. P.R. Moreno, E. Falk, V. Fuster, J.T. Fallon, Increased macrophage content of restenotic coronary plaque tissue, Circulation 90 (4) (1994) 378.
32. D. Fukuda, K. Shimada, A. Tanaka, T. Kawarabayashi, M. Yoshiyama, J. Yoshikawa, Circulating monocytes and in-stent neointima after coronary stent implantation, J. Am. Coll. Cardiol. 43 (1) (2004) 18-23.
33. B. Passlick, D. Flieger, H.W.L. Zieglerheitbrock, Identification and characterization of a novel monocyte subpopulation in human peripheral-blood, Blood 74 (7) (1989) 2527-2534.
34. S. Yona, S. Jung, Monocytes: subsets, origins, fates and functions, Curr. Opin. Hematol. 17 (1) (2009) 53-59.
35. Y. Liu, T. Imanishi, H. Ikejima, H. Tsujioka, Y. Ozaki, A. Kuroi, K. Okochi, K. Ishibashi, T. Tanimoto, Y. Ino, H. Kitabata, T. Akasaka, Association between circulating monocyte subsets and in-stent restenosis after coronary stent implantation in patients with ST-elevation myocardial infarction, Circ. J. 74 (12) (2010) 2585-2591.
36. A. Schlitt, G.H. Heine, S. Blankenberg, C. Espinola-Klein, J.F. Dopheide, C. Bickel, K.J. Lackner, M. Iz, J. Meyer, H. Darius, H.J. Rupprecht, CD14+CD16+ monocytes in coronary artery disease and their relationship to serum TNF-alpha levels, Thromb. Haemost. 92 (2) (2004) 419-424.
37. G. Rothe, H. Gabriel, E. Kovacs, J. Klucken, J. Stohr, W. Kindermann, G. Schmitz, Peripheral blood mononuclear phagocyte subpopulations as cellular markers in hypercholesterolemia, Arterioscler. Thromb. Vasc. Biol. 16 (12) (1996) 1437-1447.
38. P. Libby, D. Schwartz, E. Brogi, H. Tanaka, S.K. Clinton, A cascade model for restenosis: a special case of atherosclerosis progression, Circulation 86 (6) (1992) 47-52.
39. R. Vanfurth, Z.A. Cohn, Origin and kinetics of mononuclear phagocytes, J. Exp. Med. 128 (3) (1968) 415-435.
40. R.M. Steinman, D.S. Lustig, Z.A. Cohn, Identification of a novel cell type in peripheral lymphoid organs of mice .3. Functional properties in vivo, J. Exp. Med. 139 (6) (1974) 1431-1445.
41. C. Auffray, M.H. Sieweke, F. Geissmann, Blood monocytes: development, heterogeneity, and relationship with dendritic cells, Annu. Rev. Immunol. 27 (2009) 669-692.
42. F. Geissmann, M.G. Manz, S. Jung, M.H. Sieweke, M. Merad, K. Ley, Development of monocytes, macrophages, and dendritic cells, Science 327 (5966) (2010) 656-661.
43. N.V. Serbina, E.G. Pamer, Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2, Nat. Immunol. 7 (3) (2006) 311-317.
44. C.L. Tsou, W. Peters, Y. Si, S. Slaymaker, A.M. Aslanian, S.P. Weisberg, M. Mack, I.F. Charo, Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites, J. Clin. Invest. 117 (4) (2007) 902-909.
45. S. Gordon, P.R. Taylor, Monocyte and macrophage heterogeneity, Nat. Rev. Immunol. 5 (12) (2005) 953-964.
46. C. Kelly, C. Jefferies, S.A. Cryan, Targeted liposomal drug delivery to monocytes and macrophages, J. Drug Deliv. (2011), doi:10.1155/2011/727241.
47. T.M. Carlos, J.M. Harlan, Leukocyte-endothelial adhesion molecules, Blood 84 (7) (1994) 2068-2101.
48. D.R. Pakianathan, Extracellular-matrix proteins and leukocyte function, J. Leukoc. Biol. 57 (5) (1995) 699-702.
49. G. Ricevuti, Host tissue damage by phagocytes, Ann. NY Acad. Sci. 832 (1997) 426-448.
50. H.D. Danenberg, I. Fishbein, J.C. Gao, J. Monkkonen, R. Reich, I. Gati, E. Moerman, G. Golomb, Macrophage depletion by clodronate-containing liposomes reduces neointimal formation after balloon injury in rats and rabbits, Circulation 106 (5) (2002) 599-605.
51. N. van Rooijen, R. van Nieuwmegen, Elimination of phagocytic cells in the spleen after intravenous injection of liposome-encapsulated dichloromethylene diphosphonate. An enzyme-histochemical study, Cell Tissue Res. 238 (2) (1984) 355-358.
52. N. Van Rooijen, The liposome-mediated macrophage 'suicide' technique, J. Immunol. Methods 124 (1) (1989) 1-6.
53. H. Fleisch, Development of bisphosphonates, Breast Cancer Res. 4 (1) (2002) 30-34.
54. G.A. Rodan, Control of bone formation and resorption: biological and clinical perspective, J. Cell. Biochem. Suppl. 30-31 (1998) 55-61.
55. M.J. Rogers, J.C. Crockett, F.P. Coxon, J. Monkkonen, Biochemical and molecular mechanisms of action of bisphosphonates, Bone 49 (1) (2011) 34-41.
56. J.R. Green, Bisphosphonates: preclinical review, Oncologist 9 (Suppl. 4) (2004) 3-13.
57. H. Fleisch, Bisphosphonates: mechanisms of action, Endocr. Rev. 19 (1) (1998) 80-100.
58. H.D. Danenberg, G. Golomb, A. Groothuis, J.C. Gao, H. Epstein, R.V. Swaminathan, P. Seifert, E.R. Edelman, Liposomal alendronate inhibits systemic innate immunity and reduces in-stent neointimal hyperplasia in rabbits, Circulation 108 (22) (2003) 2798-2804.
59. H.D. Danenberg, I. Fishbein, H. Epstein, J. Waltenberger, E. Moerman, J. Monkkonen, X.C. Gao, I. Gathi, R. Reichi, G. Golomb, Systemic depletion of macrophages by liposomal bisphosphonates reduces neointimal formation following balloon-injury in the rat carotid artery, J. Cardiovasc. Pharmacol. 42 (5) (2003) 671-679.
60. V.P. Torchilin, Liposomes as targetable drug carriers, Crit. Rev. Ther. Drug Carrier Syst. 2 (1) (1985) 65-115.
61. L. Zhang, F.X. Gu, J.M. Chan, A.Z. Wang, R.S. Langer, O.C. Farokhzad, Nanoparticles in medicine: therapeutic applications and developments, Clin. Pharmacol. Ther. 83 (5) (2008) 761-769.
62. V.P. Torchilin, Recent advances with liposomes as pharmaceutical carriers, Nat. Rev. Drug Discov. 4 (2) (2005) 145-160.
63. D.D. Lasic, Novel applications of liposomes, Trends Biotechnol. 16 (7) (1998) 307-321.
64. D.D. Lasic, J.J. Vallner, P.K. Working, Sterically stabilized liposomes in cancer therapy and gene delivery, Curr. Opin. Mol. Ther. 1 (2) (1999) 177-185.
65. A. Gabizon, M. Chemla, D. Tzemach, A.T. Horowitz, 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 (5) (1996) 391-398.
66. M.C. Woodle, D.D. Lasic, Sterically stabilized liposomes, Biochim. Biophys. Acta 1113 (2) (1992) 171-199.
67. D.D. Lasic, F.J. Martin, A. Gabizon, S.K. Huang, D. Papahadjopoulos, Sterically stabilized liposomes: a hypothesis on the molecular origin of the extended circulation times, Biochim. Biophys. Acta 1070 (1) (1991) 187-192.
68. A. Gabizon, D. Papahadjopoulos, Liposome formulations with prolonged circulation time in blood and enhanced uptake by tumors, Proc. Natl. Acad. Sci. U. S. A. 85 (18) (1988) 6949-6953.
69. S. Hosokawa, T. Tagawa, H. Niki, Y. Hirakawa, K. Nohga, K. Nagaike, Efficacy of immunoliposomes on cancer models in a cell-surface-antigen-density- dependent manner, Br. J. Cancer 89 (8) (2003) 1545-1551.
70. A. Huang, S.J. Kennel, L. Huang, Interactions of immunoliposomes with target cells, J. Biol. Chem. 258 (22) (1983) 14034-14040.
71. H. Epstein, D. Gutman, E. Cohen-Sela, E. Haber, O. Elmalak, N. Koroukhov, H.D. Danenberg, G. Golomb, Preparation of alendronate liposomes for enhanced stability and bioactivity: in vitro and in vivo characterization, Am. Assoc. Pharm. Soc. J. 10 (4) (2008) 505-515.
72. E. Afergan, Y. Najajreh, D. Gutman, H. Epstein, O. Elmalak, 31P-NMR and differential scanning calorimetry studies for determining vesicle's drug physical state and fraction in alendronate liposomes, J. Bioanal. Biomed. 2 (2010) 125-131.
73. R.L. Juliano, D. Stamp, Effects of particle size and charge on the clearance of liposomes and liposome encapsulated drugs, Biochem. Biophys. Res. Commun. 63 (1975) 651-658.
74. M. Poznansky, R. Juliano, Biological approaches to the controlled delivery of drugs: a critical review, Pharmacol. Rev. 36 (1984) 277-336.
75. S.M. Moghimi, A.C. Hunter, J.C. Murray, Long-circulating and target-specific nanoparticles: theory to practice, Pharmacol. Rev. 53 (2001) 283-318.
76. S.M. Moghimi, J. Szebeni, Stealth liposomes and long circulating nanoparticles: critical issues in pharmacokinetics, opsonization and protein-binding properties, Prog. Lipid Res. 42 (6) (2003) 463-478.
77. E.W. van Etten, M.T. ten Kate, S.V. Snijders, I.A. Bakker-Woudenberg, Administration of liposomal agents and blood clearance capacity of the mononuclear phagocyte system, Antimicrob. Agents Chemother. 42 (7) (1998) 1677-1681.
78. J. Monkkonen, J. Liukkonen, M. Taskinen, T.D. Heath, A. Urtti, Studies on liposome formulations for intraarticular delivery of clodronate, J. Control. Release 35 (2-3) (1995) 145-154.
79. K.D. Lee, K. Hong, D. Papahadjopoulos, Recognition of liposomes by cells - in vitro binding and endocytosis mediated by specific lipid headgroups and surface-charge density, Biochim. Biophys. Acta 1103 (2) (1992) 185-197.
80. H. Epstein-Barash, D. Gutman, E. Markovsky, G. Mishan-Eisenberg, N. Koroukhov, J. Szebeni, 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 (2) (2010) 182-195.
81. E. Haber, E. Afergan, H. Epstein, D. Gutman, N. Koroukhov, M. Ben-David, M. Schachter, G. Golomb, Route of administration-dependent anti-inflammatory effect of liposomal alendronate, J. Control. Release 148 (2) (2010) 226-233.
82. J.H. Lin, Bisphosphonates: a review of their pharmacokinetic properties, Bone 18 (2) (1996) 75-85.
83. J.H. Lin, D.E. Duggan, I.W. Chen, R.L. Ellsworth, Physiological disposition of alendronate, a potent anti-osteolytic bisphosphonate, in laboratory animals, Drug Metab. Dispos. 19 (5) (1991) 926-932.
84. A.M.J. Buiting, F. Zhou, J.A.J. Bakker, N. van Rooijen, L. Huang, Biodistribution of clodronate and liposomes used in the liposome mediated macrophage 'suicide'approach, J. Immunol. Methods 192 (1-2) (1996) 55-62.
85. T.M. Allen, C.B. Hansen, D.E.L. Demenezes, Pharmacokinetics of long-circulating liposomes, Adv. Drug Deliv. Rev. 16 (2-3) (1995) 267-284.
86. N. VanRooijen, A. Sanders, Kupffer cell depletion by liposome-delivered drugs: comparative activity of intracellular clodronate, propamidine, and ethylenedia-minetetraacetic acid, Hepatology 23 (5) (1996) 1239-1243.
87. E. Afergan, H. Epstein, N. Koroukhov, M. Klein, A. Litchi, E. Mishani, G. Golomb, Biodistribution and imaging studies of Ga-67-labeled liposomes in rabbits with a vascular injury, J. Drug Deliv. Sci. Technol. 19 (4) (2009) 263-268.
88. K.S. Selander, J. Monkkonen, E.K. Karhukorpi, P. Harkonen, R. Hannuniemi, H.K. Vaananen, Characteristics of clodronate-induced apoptosis in osteoclasts and macrophages, Mol. Pharmacol. 50 (5) (1996) 1127-1138.
89. G. Majai, Z. Sarang, K. Csomos, G. Zahuczky, L. Fesus, PPAR gamma-dependent regulation of human macrophages in phagocytosis of apoptotic cells, Eur. J. Immunol. 37 (5) (2007) 1343-1354.
90. G. Petrovski, G. Zahuczky, G. Majai, L. Fesues, Phagocytosis of cells dying through autophagy evokes a pro-inflammatory response in macrophages, Autophagy 3 (5) (2007) 509-511.
91. G.B. Ranjit, M.F. Cheng, W. Mackay, C.M. Whitacre, J.S. Berger, N.A. Berger, Poly(-adenosine diphosphoribose) polymerase in peripheral blood leukocytes from normal donors and patients with malignancies, Clin. Cancer Res. 1 (2) (1995) 223-234.
92. E. Cohen-Sela, O. Rosenzweig, J.C. Gao, H. Epstein, I. Gati, R. Reich, H.D. Danenberg, G. Golomb, Alendronate-loaded nanoparticles deplete monocytes and attenuate restenosis, J. Control. Release 113 (1) (2006) 23-30.
93. E. Afergan, H. Epstein, R. Dahan, N. Koroukhov, K. Rohekar, H.D. Danenberg, G. Golomb, Delivery of serotonin to the brain by monocytes following phagocytosis of liposomes, J. Control. Release 132 (2) (2008) 84-90.
94. N. Pennanen, S. Lapinjoki, A. Urtti, J. Monkkonen, Effect of liposomal and free bisphosphonates on the IL-1 beta, IL-6 and TNF alpha secretion from RAW 264 cells in vitro, Pharm. Res. 12 (6) (1995) 916-922.
95. A. Toyras, J. Ollikainen, M. Taskinen, J. Monkkonen, Inhibition of mevalonate pathway is involved in alendronate-induced cell growth inhibition, but not in cytokine secretion from macrophages in vitro, Eur. J. Pharm. Sci. 19 (4) (2003) 223-230.
96. N. Makkonen, A. Salminen, M.J. Rogers, J.C. Frith, A. Urtti, E. Azhayeva, J. Monkkonen, Contrasting effects of alendronate and clodronate on RAW 264 macrophages: the role of a bisphosphonate metabolite, Eur. J. Pharm. Sci. 8 (2) (1999) 109-118.
97. D. Thiebaud, A. Sauty, P. Burckhardt, P. Leuenberger, L. Sitzler, J.R. Green, A. Kandra, J. Zieschang, P.I. dePalacios, An in vitro and in vivo study of cytokines in the acute-phase response associated with bisphosphonates, Calcif. Tissue Int. 61 (5) (1997) 386-392.
98. S. Adami, A.K. Bhalla, R. Dorizzi, F. Montesanti, S. Rosini, G. Salvagno, V. Lo Cascio, The acute-phase response after bisphosphonate administration, Calcif. Tissue Int. 41 (6) (1987) 326-331.
99. A. Sauty, M. Pecherstorfer, I. Zimmer-Roth, P. Fioroni, L. Juillerat, M. Markert, H. Ludwig, P. Leuenberger, P. Burckhardt, D. Thiebaud, Interleukin-6 and tumor necrosis factor alpha levels after bisphosphonates treatment in vitro and in patients with malignancy, Bone 18 (2) (1996) 133-139.
100. J. Szebeni, L. Baranyi, S. Savay, M. Bodo, D.S. Morse, M. Basta, G.L. Stahl, R. Bunger, C.R. Alving, Liposome-induced pulmonary hypertension: properties and mechanism of a complement-mediated pseudoallergic reaction, Am. J. Physiol. Heart Circ. Physiol. 279 (3) (2000) H1319-H1328.
101. J. Szebeni, Complement activation-related pseudoallergy: a new class of drug-induced acute immune toxicity, Toxicology 216 (2-3) (2005) 106-121.
102. A.W. Clowes, M.M. Clowes, M.A. Reidy, Kinetics of cellular proliferation after arterial injury. 3. Endothelial and smooth-muscle growth in chronically denuded vessels, Lab. Invest. 54 (3) (1986) 295-303.
103. C. Rogers, E.R. Edelman, Endovascular stent design dictates experimental restenosis and thrombosis, Circulation 91 (12) (1995) 2995-3001.
104. M. Kollum, S. Kaiser, R. Kinscherf, J. Metz, W. Kubler, C. Hehrlein, Apoptosis after stent implantation compared with balloon angioplasty in rabbits. Role of macrophages, Arterioscler. Thromb. Vasc. Biol. 17 (11) (1997) 2383-2388.
105. L.J. Feldman, M. Mazighi, A. Scheuble, J.F. Deux, E. De Benedetti, C. Badier-Commander, E. Brambilla, D. Henin, P.G. Steg, M.P. Jacob, Differential expression of matrix metalloproteinases after stent implantation and balloon angioplasty in the hypercholesterolemic rabbit, Circulation 103 (25) (2001) 3117-3122.
106. http://clinicaltrials.gov/ct2/show/NCT00739466.
107. http://www.paragon-conventions.net/ici2010/images/stories/pdf/Ctuesday/ 0948%20Banai.pdf.
108. J.W. Jukema, T.A.N. Ahmed, J.J.W. Verschuren, P.H.A. Quax, Restenosis after PCI. Part 2: prevention and therapy, Nat. Rev. Cardiol. (2011).