Assessment of bishosphonate activity In Vitro

Current Pharmaceutical Design

Volumn 16, Issue 27, 2010, Pages 2970-2980

  Mitrofan, L M ^a   Auriola, S ^b   Monkkonen H ^b   Monkkonen J ^b  

^a INSERM   (France)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Atp analogs; Bps; Cell death; Cell growth; Flow cytometry; Immunomodulation; Mass spectrometry; Uptake

Indexed keywords

ALENDRONIC ACID; BISPHOSPHONIC ACID DERIVATIVE; CLODRONIC ACID; ETIDRONIC ACID; EVEROLIMUS; IBANDRONIC ACID; INCADRONIC ACID; MINODRONIC ACID; PAMIDRONIC ACID; RISEDRONIC ACID; ZOLEDRONIC ACID; ADENOSINE TRIPHOSPHATE; BONE DENSITY CONSERVATION AGENT; DRUG DERIVATIVE; IMMUNOLOGIC FACTOR; ORGANOPHOSPHORUS COMPOUND;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CELLULAR DISTRIBUTION; CYTOTOXICITY; DRUG MECHANISM; GROWTH INHIBITION; HUMAN; IMMUNOMODULATION; IN VITRO STUDY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; CELL LINE; CELL SURVIVAL; CHEMISTRY; DRUG DESIGN; DRUG EFFECT; DRUG SCREENING; ENDOTHELIUM CELL; MACROPHAGE; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); TUMOR CELL LINE;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; BONE DENSITY CONSERVATION AGENTS; CELL LINE; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DIPHOSPHONATES; DRUG DESIGN; DRUG SCREENING ASSAYS, ANTITUMOR; ENDOTHELIAL CELLS; HUMANS; IMMUNOLOGIC FACTORS; MACROPHAGES; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; ORGANOPHOSPHORUS COMPOUNDS;

EID: 78649819207     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161210793563644     Document Type: Review

References (136)

1. van Beek E, Pieterman E, Cohen L, Löwik C, Papapoulos S. Farnesyl pyrophosphate synthase is the molecular target of nitrogen-containing bisphosphonates. Biochem Biophys Res Commun 1999; 264(1): 108-111.
2. Luckman SP, Hughes DE, Coxon FP, Graham R, Russell G, Rogers MJ. Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras. J Bone Miner Res 1998; 13(4): 581-9.
3. Hughes DE, Wright KR, Uy HL, et al. Bisphosphonates promote apoptosis in murine osteoclasts in vitro and in vivo. J Bone Miner Res 1995; 10(10): 1478-87.
4. Mönkkönen H, Auriola S, Lehenkari P, et al. A new endogenous ATP analog (ApppI) inhibits the mitochondrial adenine nucleotide translocase (ANT) and is responsible for the apoptosis induced by nitrogen-containing bisphosphonates. Br J Pharmacol 2006; 147(4): 437-45.
5. Ory B, Blanchard F, Battaglia S, Gouin F, Rédini F, Heymann D. Zoledronic acid activates the DNA S-phase checkpoint and induces osteosarcoma cell death characterized by apoptosis-inducing factor and endonuclease-G translocation independently of p53 and retinoblastoma status. Mol Pharmacol 2007; 71(1): 333-43.
6. Sewing L, Steinberg F, Schmidt H, Göke R. The bisphosphonate zoledronic acid inhibits the growth of HCT-116 colon carcinoma cells and induces tumor cell apoptosis. Apoptosis 2008; 13(6): 782-9.
7. Russell RGG, Watts NB, Ebetino FH, Rogers MJ. Mechanisms of action of bisphosphonates: similarities and differences and their potential influence on clinical efficacy. Osteoporos Int 2008; 19(6): 733-59.
8. Jauhiainen M, Mönkkönen H, Räikkönen J, Mönkkönen J, Auriola S. Analysis of endogenous ATP analogs and mevalonate pathway metabolites in cancer cell cultures using liquid chromatographyelectrospray ionization mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2009; 877(27): 2967-75.
9. Mönkkönen H, Kuokkanen J, Holen I, et al. Bisphosphonateinduced ATP analog formation and its effect on inhibition of cancer cell growth. Anticancer Drugs 2008; 19(4): 391-9.
10. Mitrofan LM, Castells FB, Pelkonen J, Mönkkönen J. Lysosomalmitochondrial axis in zoledronic acid-induced apoptosis in human follicular lymphoma cells. J Biol Chem 2010; 285(3): 1967-79.
11. Räikkönen J, Crockett JC, Rogers MJ, Mönkkönen H, Auriola S, Mönkkönen J. Zoledronic acid induces formation of a proapoptotic ATP analog and isopentenyl pyrophosphate in osteoclasts in vivo and in MCF-7 cells in vitro. Br J Pharmacol 2009; 157(3): 427-35.
12. Rogers MJ, Russell RG, Blackburn GM, Williamson MP, Watts DJ. Metabolism of halogenated bisphosphonates by the cellular slime mould Dictyostelium discoideum. Biochem Biophys Res Commun 1992; 189(1): 414-23.
13. Lehenkari PP, Kellinsalmi M, Näpänkangas JN, et al. Further insight into the mechanism of action of clodronate: inhibition of the mitochondrial ADP/ATP translocase by a non-hydrolysable, adenine-containing metabolite. Mol Pharmacol 2002; 62:1255-62.
14. Rogers MJ, Xiong X, Ji X, et al. Inhibition of growth of Dictyostelium discoideum amoebae by bisphosphonate drugs is dependent on cellular uptake. Pharm Res 1997; 14(5): 625-30.
15. Auriola S, Frith J, Rogers MJ, Koivuniemi A, Mönkkönen J. Identification of adenine nucleotide-containing metabolites of bisphosphonate drugs using ion-pair liquid chromatographyelectrospray mass spectrometry. J Chromatogr (B) Biomed Appl 1997; 704: 187-95.
16. Mönkkönen H, Moilanen P, Mönkkönen J, Frith JC, Rogers MJ, Auriola S. Analysis of an adenine nucleotide-containing metabolite of clodronate using ion pair high-performance liquid chromatography- electrospray ionisation mass spectrometry. J Chromatogr B Biomed Sci Appl 2000; 738(2): 395-403.
17. Rogers MJ, Russell RG, Blackburn GM, Williamson MP, Watts DJ. Metabolism of halogenated bisphosphonates by the cellular slime mould Dictyostelium discoideum. Biochem Biophys Res Commun 1992; 189(1): 414-23.
18. Keller RK, Fliesler SJ. Mechanism of Aminobisphosphonate Action: Characterization of Alendronate Inhibition of the Isoprenoid Pathway. Biochem Biophys Res Commun 1999; 266(2): 560-3.
19. Coscia M, Quaglino E, Iezzi M, et al. Zoledronic acid repolarizes tumor-associated macrophages and inhibits mammary carcinogenesis by targeting the mevalonate pathway. J. Cell. Mol. Med [Internet]. 2009 Oct 10 [cité 2010 Mar 31]; Available from: http://www.ncbi.nlm.nih.gov.gate2.inist.fr/pubmed/19818098.
20. Mitrofan LM, Pelkonen J, Mönkkönen J. The level of ATP analog and isopentenyl pyrophosphate correlates with zoledronic acidinduced apoptosis in cancer cells in vitro. Bone 2009; 45(6): 1153-60.
21. Michailidou M, Neville-Webbe HL, Woodward JKL, et al. The effects of combined treatment using paclitaxel and zoledronic acid on tumor cells and endothelial cells in vitro. Haematol Rep 2006; 2: 36-7.
22. Caron E. Cellular functions of the Rap1 GTP-binding protein: a pattern emerges. J Cell Sci 2003; 116(3): 435-40.
23. Räikkönen J, Mönkkönen H, Auriola S, Mönkkönen J. Mevalonate pathway intermediates downregulate zoledronic acid-induced isopentenyl pyrophosphate and ATP analog formation in human breast cancer cells. Biochem Pharmacol 2010; 79(5): 777-83.
24. Martin TJ, Moseley JM. Mechanisms in the skeletal complications of breast cancer. Endocr Relat Cancer 2000; 7: 271-84.
25. Coleman RE. The role of bisphosphonates in breast cancer. Breast 2004; 13(1): 19-28.
26. Green JR. Antitumor effects of bisphosphonates. Cancer 2003; 97(3): 840-7.
27. Winter MC, Holen I, Coleman RE. Exploring the anti-tumor activity of bisphosphonates in early breast cancer. Cancer Treat Rev 2008; 34(5): 453-75.
28. Rogers MJ, Chilton KM, Coxon FP, et al. Bisphosphonates induce apoptosis in mouse macrophage-like cells in vitro by a nitric oxideindependent mechanism. J Bone Miner Res 1996; 11(10): 1482-91.
29. Coxon FP, Benford HL, Russell RGG, Rogers MJ. Protein synthesis is required for caspase activation and induction of apoptosis by bisphosphonate drugs. Mol Pharmacol 1998; 54(4): 631-38.
30. Reszka AA, Halasy-Nagy JM, Masarachia PJ, Rodan GA. Bisphosphonates act directly on the osteoclast to induce caspase cleavage of mst1 kinase during apoptosis. A link between inhibition of the mevalonate pathway and regulation of an apoptosispromoting kinase. J Biol Chem 1999; 274(49): 34967-73.
31. Benford HL, McGowan NW, Helfrich MH, Nuttall ME, Rogers MJ. Visualization of bisphosphonate-induced caspase-3 activity in apoptotic osteoclasts in vitro. Bone 2001; 28(5): 465-73.
32. Dunford JE, Rogers MJ, Ebetino FH, Phipps RJ, Coxon FP. Inhibition of protein prenylation by bisphosphonates causes sustained activation of Rac, Cdc42, and Rho GTPases. J Bone Miner Res 2006; 21(5): 684-94.
33. Hasmim M, Bieler G, Rüegg C. Zoledronate inhibits endothelial cell adhesion, migration and survival through the suppression of multiple, prenylation-dependent signaling pathways. J Thromb Haemost 2007; 5: 166-73.
34. Shipman CM, Rogers MJ, Apperley JF, Russell RG, Croucher PI. Bisphosphonates induce apoptosis in human myeloma cell lines: a novel anti-tumor activity. Br J Haematol 1997; 98(3): 665-72.
35. Aparicio A, Gardner A, Tu Y, Savage A, Berenson J, Lichtenstein A. In vitro cytoreductive effects on multiple myeloma cells induced by bisphosphonates. Leukemia 1998; 12(2): 220-9.
36. Senaratne SG, Pirianov G, Mansi JL, Arnett TR, Colston KW. Bisphosphonates induce apoptosis in human breast cancer cell lines. Br J Cancer 2000; 82(8): 1459-68.
37. Fromigue O, Lagneaux L, Body JJ. Bisphosphonates induces breast cancer cell death in vitro. J Bone Miner Res 2000; 15(11): 2211-21.
38. Jagdev SP, Coleman RE, Shipman CM, Rostami AH, Croucher PI. The bisphosphonate, zoledronic acid, induces apoptosis of breast cancer cells: evidence for synergy with paclitaxel. Br J Cancer 2001; 84(8): 1126-34.
39. Senaratne SG, Mansi JL, Colston KW. The bisphosphonate zoledronic acid impairs Ras membrane [correction of impairs membrane] localisation and induces cytochrome c release in breast cancer cells. Br J Cancer 2002; 86(9): 1479-86.
40. Evdokiou A, Labrinidis A, Bouralexis S, Hay S, Findlay DM. Induction of cell death of human osteogenic sarcoma cells by zoledronic acid resembles anoikis. Bone 2003; 33(2): 216-28.
41. Salomo M, Jurlander J, Nielsen LB, Gimsing P. How myeloma cells escape bisphosphonate-mediated killing: development of specific resistance with preserved sensitivity to conventional chemotherapeutics. Br J Haematol 2003; 122: 202-10.
42. Denoyelle C, Hong L, Vannier JP, Soria J, Soria C. New insights into the actions of bisphosphonate zoledronic acid in breast cancer cells by dual RhoA-dependent and -independent effects. Br J Cancer 2003; 88(10): 1631-40.
43. Nishida S, Fujii Y, Yoshioka S, Kikuichi S, Tsubaki M, Irimajiri K. A new bisphosphonate, YM529 induces apoptosis in HL60 cells by decreasing phosphorylation of single survival signal ERK. Life Sci 2003; 73:2655-64.
44. Tassone P, Tagliaferri P, Viscomi C, et al. Zoledronic acid induces antiproliferative and apoptotic effects in human pancreatic cancer cells in vitro. Br J Cancer 2003; 88(12): 1971-8.
45. Kuroda J, Kimura S, Segawa H, et al. p53-independent anti-tumor effects of the nitrogen-containing bisphosphonate zoledronic acid. Cancer Sci 2004; 95(2): 186-92.
46. Kubista B, Trieb K, Sevelda F, et al. Anticancer effects of zoledronic acid against human osteosarcoma cells. J Orthop Res 2006; 24(6): 1145-52.
47. Merrell MA, Wakchoure S, Lehenkari PP, Harris KW, Selander KS. Inhibition of the mevalonate pathway and activation of p38 MAP kinase are independently regulated by nitrogen-containing bisphosphonates in breast cancer cells. Eur J Pharmacol 2007; 570(1-3): 27-37.
48. Caraglia M, Santini D, Marra M, Vincenzi B, Tonini G, Budillon A. Emerging anti-cancer molecular mechanisms of aminobisphosphonates. Endocr Relat Cancer 2006; 13(1): 7-26.
49. Clézardin P, Fournier P, Boissier S, Peyruchaud O. In vitro and in vivo antitumor effects of bisphosphonates. Curr Med Chem 2003; 10(2): 173-80.
50. Clézardin P. Anti-tumor activity of zoledronic acid. Cancer Treat Rev 2005; 31(3): 1-8.
51. Stresing V, Daubiné F, Benzaid I, Mönkkönen H, Clézardin P. Bisphosphonates in cancer therapy. Cancer Lett 2007; 257(1): 16-35.
52. Zhang FL, Casey PJ. Protein prenylation: molecular mechanisms and functional consequences. Annu Rev Biochem 1996; 65: 241-69.
53. Caraglia M, Budillon A, Tagliaferri P, Marra M, Abbruzzese A, Caponigro F. Isoprenylation of intracellular proteins as a new target for the therapy of human neoplasms: preclinical and clinical implications. Curr Drug Targets 2005; 6: 301-23.
54. Tee A.R., Blenis J. mTOR, translational control and human disease. Semin Cell Develop Biol 2005; (16): 29-37.
55. Tang X, Zhang Q, Shi S, et al. Bisphosphonates suppress insulinlike growth factor 1-induced angiogenesis via the HIF-1alpha/VEGF signaling pathways in human breast cancer cells. Int J Cancer 2010; 126(1): 90-103.
56. Morgan TM, Pitts TE, Gross TS, Poliachik SL, Vessella RL, Corey E. RAD001 (Everolimus) inhibits growth of prostate cancer in the bone and the inhibitory effects are increased by combination with docetaxel and zoledronic acid. Prostate 2008; 68(8): 861-71.
57. Ory B, Moriceau G, Redini F, Heymann D. mTOR inhibitors (rapamycin and its derivatives) and nitrogen containing bisphosphonates: bi-functional compounds for the treatment of bone tumors. Curr Med Chem 2007; 14(13): 1381-7.
58. Riss TL, Moravec RA. Use of multiple assay endpoints to investigate the effects of incubation time, dose of toxin, and plating density in cell-based cytotoxicity assays. Assay Drug Dev Technol 2004; 2(1): 51-62.
59. Wlodkowic D, Skommer J, McGuinness D, et al. Chip-based dynamic real-time quantification of drug-induced cytotoxicity in human tumor cells. Anal Chem 2009 15; 81(16): 6952-9.
60. Decker T, Lohmann-Matthes ML. A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J Immunol Methods 1988; 115(1): 61-9.
61. Mosman T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55-63.
62. Meshulam T, Levitz SM, Christin L, Diamond RD. A simplified new assay for assessment of fungal cell damage with the tetrazolium dye, (2,3)-bis-(2-methoxy-4-nitro-5-sulphenyl)-(2H)- tetrazolium-5-carboxanilide (XTT). J Infect Dis 1995; 172(4): 1153-6.
63. Nargi FE, Yang TJ. Optimization of the L-M cell bioassay for quantitating tumor necrosis factor alpha in serum and plasma. J Immunol Methods 1993; 159(1-2): 81-91.
64. Niles AL, Moravec RA, Eric Hesselberth P, Scurria MA, Daily WJ, Riss TL. A homogeneous assay to measure live and dead cells in the same sample by detecting different protease markers. Anal Biochem 2007; 366 (2): 197-206.
65. Wosikowski K, Küng W, Hasmann M, Löser R, Eppenberger U. Inhibition of growth-factor-activated proliferation by antiestrogens and effects on early gene expression of MCF-7 cells. Int J Cancer 1993; 53(2): 290-297.
66. Leist M and Jäättelä M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2001; 2: 589-98.
67. Jäättelä M. Multiple cell death pathways as regulators of tumor initiation and progression. Oncogene 2004; 23(16): 2746-56.
68. Kroemer G. Cell death and cancer: an introduction. Oncogene 2004;23: 2744-45.
69. Meijer AJ and Codogno P. Regulation and role of autophagy in mammalian cells. Int J Biochem Cell Biol 2004; 36(12): 2445-62.
70. Debatin KM, Krammer PH. Death receptors in chemotherapy and cancer. Oncogene 2004; 23(16): 2950-66.
71. Blagosklonny MV. Prospective strategies to enforce selectively cell death in cancer cells. Oncogene 2004; 23: 2967-75.
72. Hengartner MO. The biochemistry of apoptosis. Nature 2000; 407(6805): 770-6.
73. Fulda S, Meyer E, Friesen C, Susin SA, Kroemer G, Debatin KM. Cell type specific involvement of death receptor and mitochondrial pathways in drug-induced apoptosis. Oncogene 2001; 20(9): 1063-75.
74. Adrain C, Martin SJ. The mitochondrial apoptosome: a killer unleashed by the cytochrome seas. Trends Biochem Sci 2001; 26(6): 390-7.
75. Darzynkiewicz Z, Roederer M, Tanke HJ. Cytometry: New Developments. Fourth Edition. London: Elsevier Inc. All Rights Reserved 2004.
76. Galluzzi L, Aaronson SA, Abrams J, et al. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 2009; 16(8): 1093-107.
77. Klionsky DJ, Abeliovich H, Agostinis P, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4(2): 151-75.
78. Green DR and Kroemer G. The central executioner of apoptosis: mitochondria or caspases?. Trends Cell Biol 1998; (8): 267-71.
79. Green DR and Reed JC. Mitochondria and apoptosis. Science 1998; 281: 1309-12.
80. Kroemer G, Petit PX, Zamzami N, Vayssière JL, Mignotte B. The biochemistry of apoptosis. FASEB J 1995; (9):1277-87.
81. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med 2000; 6:513-9.
82. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997; (275):1132-6.
83. Patterson S, Spahr CS, Daugas E, et al. Mass spectrometric identification of proteins released from mitochondria undergoing permeability transition. Cell Death Differ 2000;7: 137-44.
84. Cossarizza A, Cooper EL, Quaglino D, Salvioli S, Kalachnikova G, Franceschi C. Mitochondrial mass and membrane potential in coelomocytes from the earthworm Eisenia foetida: studies with fluorescent probes in single intact cells. Biochem Biophys Res Commun 1995; 214: 503-10.
85. Marchetti P, Castedo M, Susin SA, et al. Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 1996; 184(3): 1155-60.
86. Petit PX, LeCoeur H, Zorn E, Dauguet C, Mignotte B, Gougeon ML. Alterations of mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J Cell Biol 1995; 130: 157-67.
87. Zamzami N, Marchetti P, Castedo M, et al. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 1995; 182: 367-77.
88. Belzacq AS, Vieira HL, Kroemer G, Brenner C. The adenine nucleotide translocator in apoptosis. Biochimie 2002; 84: 167-176.
89. Tsujimoto Y. Bcl-2 family of proteins: life-or-death switch in mitochondria. Biosci Rep 2002; 22 (1): 47-58.
90. Roy SS, Hajnóczky G. Fluorometric methods for detection of mitochondrial membrane permeabilization in apoptosis. Methods Mol Biol 2009; 559: 173-90.
91. Castedo M, Ferri K, Roumier T, Métivier D, Zamzami N, Kroemer G. Quantitation of mitochondrial alterations associated with apoptosis. J Immunol Methods 2002; 265: 39-47.
92. Ferri KF, Kroemer G. Organelle-specific initiation of cell death pathways. Nat Cell Biol 2001; 3(11): 255-63.
93. Boya P, Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene 2008; 27(50): 6434-51.
94. Wlodkowic D, Skommer J, McGuinness D, Hillier C, Darzynkiewicz Z. ER-Golgi network-A future target for anticancer therapy. Leuk Res 2009; 33(11): 1440-47.
95. Zdolsek JM, Olsson GM, Brunk UT. Photooxidative damage to lysosomes of cultured macrophages by acridine orange. Photochem Photobiol 1990; 51(1): 67-76.
96. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 1991; 139:271-9.
97. Duke RC, Cohen JJ. Morphological, biochemical, and flow cytometric assays of apoptosis. In: Coligan JE, Kruisbeek AM, Margulies DH, Shevach EM, Strober W, Eds. Current protocols in immunology. USA, New York: Green/Wiley 1992; pp. 3.17.1-3.17.16.
98. Martin SJ, Finucane DM, Amarante-Mendes GP, O'Brien GA, Green DR. Phosphatidylserine externalization during CD95- induced apoptosis of cells and cytoplasts requires ICE/CED-3 protease activity. J Biol Chem 1996; 271(46): 28753-56.
99. Ferraro-Peyret C, Quemeneur L, Flacher M, Revillard JP, Genestier L. Caspase-independent phosphatidylserine exposure during apoptosis of primary T lymphocytes. J Immunol 2002; 169(9): 4805-10.
100. Martin SJ, Reutelingsperger CP, McGahon AJ, et al. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 1995; 182: 1545-56.
101. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995; 17(184): 39-51.
102. Moreau MF, Guillet C, Massin P, et al. Comparative effects of five bisphosphonates on apoptosis of macrophage cells in vitro. Biochem Pharmacol 2007; 73(5): 718-23.
103. Wlodkowic D, Skommer J, Darzynkiewicz Z. Flow cytometrybased apoptosis detection. Methods Mol Biol (Clifton, N.J.) 2009; 559: 19-32.
104. van Engeland M, Ramaekers FC, Schutte B, Reutelingsperger CP. A novel assay to measure loss of plasma membrane asymmetry during apoptosis of adherent cells in culture. Cytometry 1996; 24(2):131-139.
105. Ribble D, Goldstein NB, Norris DA, Shellman YG. A simple technique for quantifying apoptosis in 96-well plates. BMC Biotechnol 2005; 5:12.
106. Luther E, Darzynkiewicz Z, Lee M, Holden E. Detection of differential effects of camptothecin on the cell cycle in adherent cell lines. AACR Cellcycle Cancer Ft, USA: Ft. Lauderdale 2004.
107. Kunzmann V, Bauer E, Feurle J, Weißinger F, Tony HP, Wilhelm M. Stimulation of γδ T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma. Blood 2000; 96: 384-92.
108. Miyagawa F, Tanaka Y, Yamashita S, Minato N. Essential requirement of antigen presentation by monocyte lineage cells for the activation of primary human γδ T cells by aminobisphosphonate antigen. J Immunol 2001; 166: 5508-14.
109. Dieli F, Gebbia N, Poccia F, et al. Induction of gammadelta Tlymphocyte effector functions by bisphosphonate zoledronic acid in cancer patients in vivo. Blood 2003; 102: 2310-11.
110. Wilhelm M, Kunzmann V, Eckstein S, et al. Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood 2003; 102: 200-06.
111. Kabelitz D, Marischen L, Oberg HH, Holtmeier W, Wesch D. Epithelial defence by gamma delta T cells. Int Arch Allergy Immunol 2005; 137: 73-81.
112. Roelofs AJ, Jauhiainen M, Mönkkönen H, et al. Peripheral blood monocytes are responsible for gammadelta T cell activation induced by zoledronic acid through accumulation of IPP/DMAPP. Br J Haematol 2009; 144: 245-50.
113. Tanaka Y, Morita CT, Tanaka Y, Nieves E, Brenner MB, Bloom BR. Natural and synthetic non-peptide antigens recognized by human gamma delta T cells. Nature 1995; 375: 155-8.
114. Vantourout P, Mookerjee-Basu J, Rolland C, et al. Specific requirements for Vγ9Vδ2 T cell stimulation by a natural adenylated phosphoantigen. J Immunol 2009; 183: 3848-57.
115. Mattarollo SR, Kenna T, Nieda M, Nicol AJ. Chemotherapy and zoledronate sensitize solid tumor cells to Vgamma9Vdelta2 T cell cytotoxicity. Cancer Immunol Immunother 2007; 56: 1285-97.
116. Gertner J, Wiedemann A, Poupot M, Fournié JJ. Human gammadelta T lymphocytes strip and kill tumor cells simultaneously. Immunol Lett 2007; 110: 42-53.
117. Watanabe N, Narita M, Yokoyama A, et al. Type I IFN-mediated enhancement of anti-leukemic cytotoxicity of gammadelta T cells expanded from peripheral blood cells by stimulation with zoledronate. Cytotherapy 2006; 8: 118-29.
118. Märten A, Lilienfeld-Toal M, Büchler MW, Schmidt J. Zoledronic acid has direct antiproliferative and antimetastatic effect on pancreatic carcinoma cells and acts as an antigen for delta2 gamma/delta T cells. J Immunother 2007; 30: 370-77.
119. Muraro M, Mereuta OM, Carraro F, et al. Osteosarcoma cell line growth inhibition by zoledronate-stimulated effector cells. Cell Immunol 2007; 249: 63-72.
120. Kabelitz D, Wesch D, Pitters E, Zöller M. Characterization of tumor reactivity of human V gamma 9V delta 2 gamma delta T cells in vitro and in SCID mice in vivo. J Immunol 2004; 173: 6767-776.
121. Sato K, Kimura S, Segawa H, et al. Cytotoxic effects of gammadelta T cells expanded ex vivo by a third generation bisphosphonate for cancer immunotherapy. Int J Cancer 2005; 116: 94-9.
122. Sato M, Grasser W, Endo N, et al. Bisphosphonate action. Alendronate localization in rat bone and effects on osteoclast ultrastructure. J Clin Invest 1991; 88: 2095-105.
123. Thompson K, Rogers MJ, Coxon FP, Crockett JC. Cytosolic entry of bisphosphonate drugs requires acidification of vesicles after fluid-phase endocytosis. Mol Pharmacol 2006; 69:1624-32.
124. Mönkkönen J, Taskinen M, Auriola SOK, Urtti A. Growth inhibition of macrophage-like and other cell types by liposomeencapsulated, calcium-bound and free bisphopshonates in vitro. J Drug Targeting 1994; 2:299-308.
125. Mönkkönen J, Urtti A, Paronen P, Elo HA, Ylitalo P. The uptake of clodronate (dichloromethylene bisphosphonate) by macrophages in vivo and in vitro. Drug Metab Dispos 1989; 17: 690-693.
126. Journe F, Kheddoumi N, Chaboteaux D, Duvillier H, Lauren G, Body JJ. Extracellular calcium increases bisphopshonate induced growth inhibition of breast canpcer cells. Breast Cancer Res 2008; 10: R4.
127. Frith JC, Rogers MJ. Antagonistic effects of different classes of bisphosphonates in osteoclasts and macrophages in vitro. J Bone Miner Res 2003; 18: 204-212.
128. Coxon FP, Thompson K, Roelofs AJ, Ebetini FH, Rogers MJ. Visualizing mineral binding and uptake of bisphopshonate by osteoclasts and non-resorbing cells. Bone 2008; 42: 846-60.
129. Roelofs AJ, Coxon FP, Ebetino FH, et al. Fluorescent risedronate analoques reveal bisphosphonate uptake by bone marrow monocytes and localization around osteocytes in vivo. J Bone Miner Res 2010: in press, DOI: 10.1359/jbmr.09 1009.
130. Zaheer A, Lenkinsky RE, Mahmood A, Jones AG, Cantley LC, Frangioni JV. In vivo nearinfrared fluorescence imaging of osteoblastic activity. Nat Biotech 2001; 19: 1148-54.
131. Kozloff KM, Weissleder R, MAhmood U. Noninvasive optical detection of bone mineral. J Bone Miner Res. 2007; 22: 1208-16.
132. Kashemirov BA, Bala JLF, Chen X, et al. Fluorecently labeled risedronate and related analoques. "Magic linker" synthesis. Bioconjug Chem 2008; 19: 2308-10.
133. Maalouf MA, Wiemer AJ, Kuder CH, Hohl RJ, Wiemer DF. Synthesis of fluorescently tagged isoprenoid bisphosphonates that inhibit protein geranylgeranylation. Bioconjug Chem 2007; 15: 1959-66.
134. Holen I, Coleman RE. Bisphosphonates as Treatment of Bone Metastases. Curr Pharm Des 2010; 15(11): 1262-71.
135. Rogers MJ. New insights into the molecular mechanisms of action of bisphosphonates. Curr Pharm Des 2003; 9(32): 2643-58.
136. Uludag H. Bisphosphonates as a foundation of drug delivery to bone. Curr Pharm Des 2002; 8(21): 1929-44.