Bisphosphonates' antitumor activity: An unravelled side of a multifaceted drug class

Bone

Volumn 48, Issue 1, 2011, Pages 71-79

  Clézardin, Philippe ^a  

^a UNIVERSITÉ LYON 1   (France)

Author keywords

Angiogenesis; Bisphosphonate; Breast; Gamma delta T; Metastasis

Indexed keywords

4 [5 (4 CHLOROPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOL 1 YL]BENZENESULFONAMIDE; ALENDRONIC ACID; ANTIBODY; BISPHOSPHONIC ACID DERIVATIVE; CHEMOKINE RECEPTOR CXCR4; CLODRONIC ACID; CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; GAMMA INTERFERON; GEFITINIB; IBANDRONIC ACID; IFOSFAMIDE; IMATINIB; INCADRONIC ACID; MINODRONIC ACID; PACLITAXEL; PAMIDRONIC ACID; PARATHYROID HORMONE RELATED PROTEIN ANTIBODY; RISEDRONIC ACID; TOPOTECAN; TRANSFORMING GROWTH FACTOR BETA; UFT; UNCLASSIFIED DRUG; ZOLEDRONIC ACID;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BLADDER CANCER; BONE DENSITY; BONE DESTRUCTION; BONE METASTASIS; BONE TUMOR; BREAST CANCER; BREAST CARCINOMA; CANCER INHIBITION; CELL CYCLE ARREST; CYTOTOXIC T LYMPHOCYTE; DISEASE FREE SURVIVAL; DRUG STRUCTURE; ENDOTHELIUM CELL; EWING SARCOMA; HUMAN; KIDNEY CARCINOMA; LEUKEMIA; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; MELANOMA; MESOTHELIOMA; MOLECULARLY TARGETED THERAPY; MYELOMA; NONHUMAN; OSTEOPOROSIS; OSTEOSARCOMA; OVARY CARCINOMA; OVERALL SURVIVAL; PROSTATE CARCINOMA; REVIEW; SINGLE DRUG DOSE; SOFT TISSUE TUMOR; TUMOR GROWTH; TUMOR VASCULARIZATION; UTERINE CERVIX CARCINOMA; VISCERAL METASTASIS;

ANIMALS; ANTINEOPLASTIC AGENTS; BONE RESORPTION; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; DIPHOSPHONATES; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; FORECASTING; HUMANS; MACROPHAGES; MICE; MICE, SCID; NEOPLASMS; OSTEOCLASTS; T-LYMPHOCYTES;

EID: 78650304661     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2010.07.016     Document Type: Review

References (69)

1. Fleisch H. Development of bisphosphonates. Breast Cancer Res 2002, 4:30-34.
2. Masarachia P., Weinreb M., Balena R., Rodan G.A. Comparison of the distribution of 3H-alendronate and 3H-etidronate in rat and mouse bones. Bone 1996, 3:281-290.
3. Lehenkari P.P., Kellinsalmi M., Näpänkangas J.P., Ylitalo K.V., Mönkkönen J., Rogers M.J., et al. Further insight into mechanism of action of clodronate: inhibition of mitochondrial ADP/ATP translocase by a nonhydrolyzable, adenine-containing metabolite. Mol Pharmacol 2002, 61:1255-1262.
4. Kavanagh K.L., Guo K., Dunford J.E., Wu X., Knapp S., Ebetino F.H., et al. The molecular mechanism of nitrogen-containing bisphosphonates as antiosteoporosis drugs. Proc Natl Acad Sci U S A 2006, 103:7829-7834.
5. Rondeau J.M., Bitsch F., Bourgier E., Geiser M., Hemmig R., Kroemer M., et al. Structural basis for the exceptional in vivo efficacy of bisphosphonate drugs. Chem Med Chem 2006, 1:267-273.
6. Guo R.T., Cao R., Liang P.H., Ko T.P., Chang T.H., Hudock M.P., et al. Bisphosphonates target multiple sites in both cis- and trans-prenyltransferases. Proc Natl Acad Sci U S A 2007, 104:10022-10027.
7. Mönkkönen H., Auriola S., Lehenkari P., Kellinsalmi M., Hassinen I.E., Vepsäläinen J., 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, 147:437-445.
8. Stresing V., Daubiné F., Benzaid I., Mönkkönen H., Clézardin P. Bisphosphonates in cancer therapy. Cancer Lett 2007, 257:16-35.
9. 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, 79:777-783.
10. Desai B., Rogers M.J., Chellaiah M.A. Mechanisms of osteopontin and CD44 as metastatic principles in prostate cancer cells. Mol Cancer 2007, 6:18.
11. Marra M., Santini Test D. Cyr61 downmodulation potentiates the anticancer effects of zoledronic acid in androgen-independent prostate cancer cells. Int J Cancer 2009, 125:2004-2013.
12. H.K. Brown, P.D. Ottewell, R.E. Coleman, I. Holen, The kinetochore protein Cenp-F is a potential novel target for zoledronic acid in breast cancer cells. J Cell Mol Med, in press. doi:10.1111/j.1582-4934.2009.00995.x.
13. Mitrofan L.M., Pelkonen J., Mönkkönen J. The level of ATP analog and isopentenyl pyrophosphate correlates with zoledronic acid-induced apoptosis in cancer cells in vitro. Bone 2009, 45:1153-1160.
14. Schmidt A., Rutledge S.J., Endo N., Opas E.E., Tanaka H., Wesolowski G., et al. Protein-tyrosine phosphatase activity regulates osteoclast formation and function: inhibition by alendronate. Proc Natl Acad Sci U S A 1996, 93:3068-3073.
15. Skorey K., Ly H.D., Kelly J., Hammond M., Ramachandran C., Huang Z., et al. How does alendronate inhibit protein-tyrosine phosphatases?. J Biol Chem 1997, 272:22472-22480.
16. Tang X., Zhang Q., Shi S., Yen Y., Li X., Zhang Y., et al. Bisphosphonates suppress insulin-like growth factor 1-induced angiogenesis via the HIF-1alpha/VEGF signaling pathways in human breast cancer cells. Int J Cancer 2010, 126:90-103.
17. Inoue R., Matsuki N., Jing G., Kanematsu T., Abe K., Hirata M. The inhibitory effect of alendronate, a nitrogen-containing bisphosphonate on the PI3K-Akt-NFκB pathway in osteosarcoma cells. Br J Pharmacol 2005, 146:633-641.
18. Rachner T.D., Singh S.K., Schoppet M., Benad P., Bornhäuser M., Ellenrieder V., et al. Zoledronic acid induces apoptosis and changes the TRAIL/OPG ratio in breast cancer cells. Cancer Lett 2010, 287:109-116.
19. Bivi N., Romanello M., Harrison R., Clarke I., Hoyle D.C., Moro L., et al. Identification of secondary targets of N-containing bisphosphonates in mammalian cells via parallel competition analysis of the barcoded yeast deletion collection. Genome Biol 2009, 10:R93.
20. Sonnemann J., Bumbul B., Beck J.F. Synergistic activity of the histone deacetylase inhibitor suberoylanilide hydroxamic acid and the bisphosphonate zoledronic acid against prostate cancer cells in vitro. Mol Cancer Ther 2007, 6:2976-2984.
21. Chang J.W., Hsieh J.J., Shen Y.C., Yeh K.Y., Wang C.H., Li Y.Y., et al. Bisphosphonate zoledronic acid enhances the inhibitory effects of gefitinib on EGFR-mutated non-small cell lung carcinoma cells. Cancer Lett 2009, 278:17-26.
22. Neville-Webbe H.L., Coleman R.E., Holen I. Combined effects of the bisphosphonate, zoledronic acid and the aromatase inhibitor letrozole on breast cancer cells in vitro: evidence of synergistic interaction. Br J Cancer 2010, 102:1010-1017.
23. Ottewell P.D., Woodward J.K., Lefley D.V., Evans C.A., Coleman R.E., Holen I. Anticancer mechanisms of doxorubicin and zoledronic acid in breast cancer tumor growth in bone. Mol Cancer Ther 2009, 8:2821-2832.
24. Biver E., Vieillard M.H., Cortet B., Salleron J., Falgayrac G., Penel G. No anti-angiogenic effect of clinical dosing regimens of a single zoledronic acid injection in an experimental bone healing site. Bone 2010, 46:643-648.
25. Kaplan R.N., Psaila B., Lyden D. Bone marrow cells in the 'pre-metastatic niche': within bone and beyond. Cancer Metastasis Rev 2006, 25:521-529.
26. Tuomela J.M., Valta M.P., Väänänen K., Härkönen P. Alendronate decreases orthotopic PC-3 prostate tumor growth and metastasis to prostate-draining lymph nodes in nude mice. BioMed Central Cancer 2008, 8:81.
27. van der Pluijm G., Que I., Sijmons B., Buijs J.T., Löwik C.W.G.M., Wetterwald A., et al. Interference with the microenvironmental support impairs the de novo formation of bone metastases in vivo. Cancer Res 2005, 65:7682-7690.
28. Korpal M., Yan J., Lu X., Xu S., Lerit D.A., Kang Y. Imaging transforming growth factor-beta signaling dynamics and therapeutic response in breast cancer bone metastasis. Nat Med 2009, 15:960-966.
29. Hirbe A.C., Roelofs A.J., Floyd D.H., Deng H., Becker S.N., Lanigan L.G., et al. The bisphosphonate zoledronic acid decreases tumor growth in bone in mice with defective osteoclasts. Bone 2009, 44:908-916.
30. Fournier P.G., Stresing V., Ebetino F.H., Clezardin P. How do bisphosphonates inhibit bone metastasis in vivo ?. Neoplasia 2010, 12:571-578.
31. Boissier S., Magnetto S., Frappart L., Cuzin B., Ebetino F.H., Delmas P.D., et al. Bisphosphonates inhibit prostate and breast carcinoma cell adhesion to unmineralized and mineralized bone extracellular matrices. Cancer Res 1997, 57:3890-3894.
32. Fournier P.G., Daubiné F., Lundy M.W., Rogers M.J., Ebetino F.H., Clezardin P. Lowering bone mineral affinity of bisphosphonates as a therapeutic strategy to optimize skeletal tumor growth inhibition in vivo. Cancer Res 2008, 68:8945-8953.
33. Daubiné F., Le Gall C., Gasser J., Green J., Clézardin P. Antitumor effects of clinical dosing regimens of bisphosphonates in experimental breast cancer bone metastasis. J Natl Cancer Inst 2007, 99:322-330.
34. Yamada T., Muguruma H., Yano S., Ikuta K., Ogino H., Kakiuchi S., et al. Intensification therapy with anti-parathyroid hormone-related protein antibody plus zoledronic acid for bone metastases of small cell lung cancer cells in severe combined immunodeficient mice. Mol Cancer Ther 2009, 8:119-126.
35. van Beek E.R., Löwik C.W.G.M., van Wijngaarden J., Ebetino F.H., Papapoulos S.E. Synergistic effect of bisphosphonate and docetaxel on the growth of bone metastasis in an animal model of established metastatic bone disease. Breast Cancer Res Treat 2009, 118:307-313.
36. Peng H., Sohara Y., Moats R.A., Nelson M.D., Groshen S.G., Ye W., et al. The activity of zoledronic acid on neuroblastoma bone metastasis involves inhibition of osteoclasts and tumor cell survival and proliferation. Cancer Res 2007, 67:9346-9355.
37. Ottewell P.D., Deux B., Mönkkönen H., Cross S., Coleman R.E., Clezardin P., et al. Differential effect of doxorubicin and zoledronic acid on intraosseous versus extraosseous breast tumor growth in vivo. Clin Cancer Res 2008, 14:4658-4666.
38. Ottewell P.D., Mönkkönen H., Jones M., Lefley D.V., Coleman R.E., Holen I. Antitumor effects of doxorubicin followed by zoledronic acid in a mouse model of breast cancer. J Natl Cancer Inst 2008, 100:1167-1178.
39. Ottewell P.D., Lefley D.V., Cross S.S., Evans C.A., Coleman R.E., Holen I. Sustained inhibition of tumor growth and prolonged survival following sequential administration of doxorubicin and zoledronic acid in a breast cancer model. Int J Cancer 2009, 126:522-532.
40. Melani C., Sangaletti S., Barazzetta F.M., Werb Z., Colombo M.P. Amino-bisphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloid-derived suppressor cell expansion and macrophage infiltration in tumor stroma. Cancer Res 2007, 67:11438-11446.
41. Coscia M., Quaglino E., Iezzi M., Curcio C., Pantaleoni F., Riganti C., Holen I., Mönkkönen H., Boccadoro M., Forni G., Musiani P., Bosia A., Cavallo F., Massaia M. Zoledronic acid repolarizes tumor-associated macrophages and inhibits mammary carcinogenesis by targeting the mevalonate pathway. J Cell Mol Med 2010, 14:2803-2815.
42. Hashimoto K., Morishige K., Sawada K., Tahara M., Shimizu S., Ogata S., et al. Alendronate suppresses tumor angiogenesis by inhibiting Rho activation of endothelial cells. Biochem Biophys Res Commun 2007, 354:478-484.
43. Li Y.Y., Chang J.W., Chou W.C., Liaw C.C., Wang H.M., Huang J.S., et al. Zoledronic acid is unable to induce apoptosis, but slows tumor growth and prolongs survival for non-small-cell lung cancers. Lung Cancer 2008, 59:180-191.
44. Chang J.W.C., Hsieh J.J., Shen Y.C., Yeh K.Y., Wang C.H., Li Y.Y., et al. Bisphosphonate zoledronic acid enhances the inhibitory effects of gefitinib on EGFR-mutated non-small cell lung carcinoma cells. Cancer Lett 2009, 278:17-26.
45. Koto K., Horie N., Kimura S., Murata H., Sakabe T., Matsui T., et al. Clinically relevant dose of zoledronic acid inhibits spontaneous lung metastasis in a murine osteosarcoma model. Cancer Lett 2009, 18:271-278.
46. Labrinidis A., Hay S., Liapis V., Ponomarev V., Findlay D.M., Evdokiou A. Zoledronic acid inhibits both the osteolytic and osteoblastic components of osteosarcoma lesions in a mouse model. Clin Cancer Res 2009, 15:3451-3461.
47. Dallas S.L., Garrett I.R., Oyajobi B.O., Dallas M.R., Boyce B.F., Bauss F., et al. Ibandronate reduces osteolytic lesions but not tumor burden in a murine model of myeloma bone disease. Blood 1999, 93:1697-1706.
48. Croucher P.I., De Raeve H., Perry M.J., Hijzen A., Shipman C.M., Lippitt J., et al. Zoledronic acid treatment of 5T2MM-bearing mice inhibits the development of myeloma bone disease: evidence for decreased osteolysis, tumor burden and angiogenesis, and increased survival. J Bone Min Res 2003, 18:482-492.
49. Guenther A., Gordon S., Tiemann M., Burger R., Bakker F., Green J.R., et al. The bisphosphonate zoledronic acid has antimyeloma activity in vivo by inhibition of protein prenylation. Int J Cancer 2010, 126:239-246.
50. Miwa S., Mizokami A., Keller E.T., Taichman R., Zhang J., Namiki M. The bisphosphonate YM529 inhibits osteolytic and osteoblastic changes and CXCR-4-induced invasion in prostate cancer. Cancer Res 2005, 65:8818-8825.
51. Morita C.T., Jin C., Sarikonda G., Wang H. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vgamma2Vdelta2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol Rev 2007, 215:59-76.
52. Vantourout P., Mookerjee-Basu J., Rolland C., Pont F., Martin H., Davrinche C., et al. Specific requirements for Vγ9Vδ2 T cell stimulation by a natural adenylated phosphoantigen. J Immunol 2009, 183:3848-3857.
53. Kunzmann V., Bauer E., Wilhelm M. Gamma/delta T-cell stimulation by pamidronate. N Engl J Med 1999, 340:737-738.
54. Fiore F., Castella B., Nuschak B., Bertieri R., Mariani S., Bruno B., et al. Enhanced ability of dendritic cells to stimulate innate and adaptive immunity on short-term incubation with zoledronic acid. Blood 2007, 110:921-927.
55. Roelofs A.J., Jauhiainen M., Mönkkönen H., Rogers M.J., Mönkkönen J., Thompson K. Peripheral blood monocytes are responsible for gammadelta T cell activation induced by zoledronic acid through accumulation of IPP/DMAPP. Br J Haematol 2009, 144:245-250.
56. Mönkkönen H., Kuokkanen J., Holen I., Evans A., Lefley D.V., Jauhiainen M., et al. Bisphosphonate-induced ATP analog formation and its effect on inhibition of cancer cell growth. Anticancer Drugs 2008, 19:391-399.
57. Li J., Herold M.J., Kimmel B., Müller I., Rincon-Orozco B., Kunzmann V., et al. Reduced expression of the mevalonate pathway enzyme farnesyl pyrophosphate synthase unveils recognition of tumor cells by Vγ9Vδ2 T cells. J Immunol 2009, 182:8118-8124.
58. Wei H., Huang D., Lai X., Chen M., Zhong W., Wang R., et al. Definition of APC presentation of phosphoantigen (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate to Vgamma2 Vdelta 2 TCR. J Immunol 2008, 181:4798-4806.
59. Bonneville M., Scotet E. Human Vgamma9Vdelta2 T cells: promising new leads for immunotherapy of infections and tumors. Curr Opin Immunol 2006, 18:539-546.
60. J. Mookerjee-Basu, P. Vautourout, L.O. Martinez, B. Perret, X. Collet, C. Perigaud, S. Peyrottes, E. Champagne, F1-adenosine triphosphatase displays properties characteristic of an antigen presentation molecule for Vgamma9Vdelta2 T cells, J Immunol 2010;184:6920-8.
61. Sato K., Kimura S., Segawa H., Yokota A., Matsumoto S., Kuroda J., et al. Cytotoxic effects of gammadelta T cells expanded ex vivo by a third generation bisphosphonate for cancer immunotherapy. Int J Cancer 2005, 116:94-99.
62. Yuasa T., Sato K., Ashihara E., Takeuchi M., Maita S., Tsuchiya N., et al. Intravesical administration of gammadelta T cells successfully prevents the growth of bladder cancer in the murine model. Cancer Immunol Immunother 2009, 58:493-502.
63. D'Asaro M., La Mendola C., Di Liberto D., Orlando V., Todaro M., Spina M., et al. V gamma 9V delta 2T lymphocytes efficiently recognize and kill zoledronate-sensitized, imatinib-sensitive, and imatinib-resistant chronic myelogenous leukemia cells. J Immunol 2010, 184:3260-3268.
64. Dieli F., Vermijlen D., Fulfaro F., Caccamo N., Meraviglia S., Cicero G., et al. Targeting human gammadelta T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res 2007, 67:7450-7457.
65. Gnant M., Mlineritsch B., Schippinger W., Luschin-Ebengreuth G., Pöstlberger S., Menzel C., et al. Endocrine therapy plus zoledronic acid in premenopausal breast cancer. N Engl J Med 2009, 360:679-691. ABCSG-12 Trial Investigators, C. Marth.
66. Aft R., Naughton M., Trinkaus K., Watson M., Ylagan L., Chavez-MacGregor M., et al. Effect of zoledronic acid on disseminated tumour cells in women with locally advanced breast cancer: an open label, randomised, phase 2 trial. Lancet Oncol 2010, 11:421-428.
67. Coleman R.E., Winter M.C., Cameron D., Bell R., Dodwell D., Keane M.M., et al. The effects of adding zoledronic acid to neoadjuvant chemotherapy on tumor response: exploratory evidence for direct anti-tumor activity in breast cancer. Br J Cancer 2010, 102:1099-1105.
68. Mattarollo S.R., Kenna T., Nieda M., Nicol A.J. Chemotherapy and zoledronate sensitize solid tumour cells to Vgamma9Vdelta2 T cell cytotoxicity. Cancer Immunol Immunother 2007, 56:1285-1297.
69. R.T. Chlebowski, Z. Chen, J.A. Cauley, G. Anderson, R.J. Rodabough, A. McTiernan, D.S. Lane, J.E. Manson, L. Snetselaar, S. Yasmeen, M.J. O'Sullivan, M. Safford, S.L. Hendrix, R.B. Wallace, Oral bisphosphonate use and breast cancer incidence in postmenopausal women, J Clin Oncol 2010;28:3582-90.