Zoledronic acid induces apoptosis and changes the TRAIL/OPG ratio in breast cancer cells

Cancer Letters

Volumn 287, Issue 1, 2010, Pages 109-116

  Rachner, Tilman D ^a,b   Singh, Shiv K ^a   Schoppet, Michael ^a   Benad, Peggy ^b   Bornhäuser, Martin ^b,c   Ellenrieder, Volker ^a   Ebert, Regina ^d   Jakob, Franz ^d   Hofbauer, Lorenz C ^a,c  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Breast cancer; OPG; TRAIL; Zoledronic acid

Indexed keywords

CASPASE 3; CASPASE 7; ESTROGEN RECEPTOR; OSTEOPROTEGERIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; ZOLEDRONIC ACID;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CELL STRAIN MCF 7; DRUG RESPONSE; DRUG TARGETING; ENZYME ACTIVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

APOPTOSIS; BONE DENSITY CONSERVATION AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DIPHOSPHONATES; FEMALE; HUMANS; IMIDAZOLES; OSTEOPROTEGERIN; RNA, MESSENGER; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 72049100087     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2009.06.003     Document Type: Article

References (35)

1. Martin T.J., and Moseley J.M. Mechanisms in the skeletal complications of breast cancer. Endocr. Relat. Cancer 7 (2000) 271-284
2. Costa L. Bisphosphonates: reducing the risk of skeletal complications from bone metastasis. Breast 16 (2007) 16-20
3. Body J.J., Diel I.J., Lichinitser M.R., Kreuser E.D., Dornoff W., Gorbunova V.A., Budde M., Bergström B., and MF 4265 Study Group. Intravenous Ibandronate reduces the incidence of skeletal complications in patients with breast cancer and bone metastases. Ann. Oncol. 14 (2003) 1399-1405
4. Hughes D.E., Wright K.R., Uy H.L., Sasaki A., Yoneda T., Roodman G.D., Mundy G.R., and Boyce B.F. Bisphosphonates promote apoptosis in murine osteoclasts in vitro and in vivo. J. Bone Miner. Res. 10 (1995) 1478-1487
5. Boissier S., Ferreras M., Peyruchaud O., Magnetto S., Ebetino F.H., Colombel M., Delmas P., Delaissé J.M., and Clézardin P. Bisphosphonates inhibit breast and prostate carcinoma cell invasion, an early event in the formation of bone metastases. Cancer Res. 60 (2000) 2949-2954
6. van der Pluijm G., Vloedgraven H., van Beek E., van der Wee-Pals L., Löwik C., and Papapoulos S. Bisphosphonates inhibit the adhesion of breast cancer cells to bone matrices in vitro. J. Clin. Invest. 98 (1996) 698-705
7. Santini D., Vincenzi B., Dicuonzo G., Avvisati G., Massacesi C., Battistoni F., Gavasci M., Rocci L., Tirindelli M.C., Altomare V., Tocchini M., Bonsignori M., and Tonini G. Zoledronic acid induces significant and long-lasting modifications of circulating angiogenic factors in cancer patients. Clin. Cancer Res. 9 (2003) 2893-2897
8. Fromigue O., Lagneaux L., and Body J.J. Bisphosphonates induce breast cancer cell death in vitro. J. Bone Miner. Res. 15 (2000) 2211-2221
9. Lowe L.C., Senaratne S.G., and Colston K.W. Induction of apoptosis in breast cancer cells by apomine is mediated by caspase and p38 mitogen activated protein kinase activation. Biochem. Biophys. Res. Commun. 329 (2005) 772-779
10. Verdidk R., Franke H.R., Wolbers F., and Vermes I. Differential effects of bisphosphonates on breast cancer cell lines. Cancer Lett. 246 (2007) 308-312
11. Gnant M., Mlineritsch B., Schippinger W., Luschin-Ebengreuth G., Pöstlberger S., Menzel C., Jakesz R., Seifert M., Hubalek M., Bjelic-Radisic V., Samonigg H., Tausch C., Eidtmann H., Steger G., Kwasny W., Dubsky P., Fridrik M., Fitzal F., Stierer M., Rücklinger E., Greil R., ABCSG-12 Trial Investigators, and Marth C. Endocrine therapy plus zoledronic acid in premenopausal breast cancer. New Engl. J. Med. 360 (2009) 679-691
12. Morony S., Capparelli C., Sarosi I., Lacey D.L., Dunstan C.R., and Kostenuik P.J. Osteoprotegerin inhibits osteolysis and decreases skeletal tumor burden in syngeneic and nude mouse models of experimental bone metastasis. Cancer Res. 61 (2001) 4432-4436
13. Kearns A.E., Khosla S., and Kostenuik P.J. Receptor activator of nuclear factor kappaB ligand and osteoprotegerin regulation of bone remodeling in health and disease. Endocr. Rev. 29 (2008) 155-192
14. Holen I., Cross S.S., Neville-Webbe H.L., Cross N.A., Balasubramanian S.P., Croucher P.I., Evans C.A., Lippitt J.M., Coleman R., and Ebetino F.H. Osteoprotegerin (OPG) expression by breast cancer cells in vitro and breast tumours in vivo - a role in tumour cell survival?. Breast Cancer Res. Treat. 92 (2005) 207-215
15. Viereck V., Emons G., Lauck V., Frosch K.H., Blaschke S., Gründker C., and Hofbauer L.C. Bisphosphonates pamidronate and zoledronic acid stimulate osteoprotegerin production by primary human osteoblasts. Biochem. Biophys. Res. Commun. 291 (2002) 680-686
16. Lipton A., Cook R.J., Major P., Smith M.R., and Coleman R. Zoledronic acid and survival in breast cancer patients with bone metastases and elevated markers of osteoclast activity. Oncologist 12 (2007) 1035-1043
17. Oura S., Hirai I., Yoshimasu T., Kokawa Y., and Sasaki R. Clinical efficacy of bisphosphonate therapy for bone metastasis from breast cancer. Breast Cancer 10 (2003) 28-32
18. Rachner T.D., Schoppet M., Niebergall U., and Hofbauer L.C. 17β-Estradiol inhibits osteoprotegerin production by the estrogen receptor-α-positive human breast cancer cell line MCF-7. Biochem. Biophys. Res. Commun. 368 (2008) 736-741
19. Van Poznak C., Cross S.S., Saggese M., Hudis C., Panageas K.S., Norton L., Colemann R.E., and Holen I. Expression of osteoprotegerin (OPG), TNF related apoptosis inducing ligand (TRAIL), and receptor activator of nuclear factor kappaB ligand (RANKL) in human breast tumours. J. Clin. Pathol. 59 (2006) 56-63
20. Kohno N., Aogi K., Minami H., Nakamura S., Asaga T., Iino Y., Watanabe T., Goessl C., Ohashi Y., and Takashima S. Zoledronic acid significantly reduces skeletal complications compared with placebo in Japanese women with bone metastases from breast cancer: a randomized, placebo-controlled trial. J. Clin. Oncol. 23 (2005) 3314-3321
21. Luckman S.P., Hughes D.E., Coxon F.P., Russell R.G., and Rogers M.J. Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTPbinding proteins, including Ras. J. Bone Miner. Res. 13 (1998) 581-589
22. van Beek E., Pieterman E., Cohen L., Lowik C., and Papoulos C. Nitrogen-containing bisphosphonates inhibit isopentyl pyrophosphate isomerase/farnesyl pyrophosphate synthase activity with relative potencies corresponding to their antiresorptive potencies in vitro and in vivo. Biochem. Biophys. Res. Commun. 255 (1999) 491-494
23. Shipman C.M., Rogers M.J., Apperley J.F., Russell R.G., and Croucher P.I. Bisphosphonates induce apoptosis in human myeloma cell lines: a novel anti-tumour activity. Br. J. Haematol. 98 (1997) 665-672
24. Tassone P., Tagliaferri P., Viscomi C., Palmieri C., Caraglia M., D'Alessandro A., Galea E., Goel A., Abbruzzese A., Boland C.R., and Venuta S. Zoledronic acid induces antiproliferative and apoptotic effects in human pancreatic cancer cells in vitro. Br. J. Cancer 88 (2003) 1971-1978
25. Lee M.V., Fong E.M., Singer F.R., and Guenette R.S. Bisphosphonate treatment inhibits the growth of prostrate cancer cells. Cancer Res. 61 (2001) 2602-2608
26. Senaratne S.G., Pirianov G., Mansi J.L., Arnett T.R., and Colston K.W. Bisphosphonates induce apoptosis in human breast cancer cell lines. Br. J. Cancer 82 (2000) 1459-1468
27. Chen T., Berenson J., Vescio R., Swift R., Gilchick A., Goodin S., LoRusso P., Ma P., Ravera C., Deckert F., Schran H., Seaman J., and Skerjanec A. Pharmacokinetics and pharmacodynamics of zoledronic acid in cancer patients with bone metastases. J. Clin. Pharmacol. 42 (2002) 1228-1236
28. Sato M., Grasser W., Endo N., Akins R., Simmons H., Thompson D.D., Golb E., and Rodan G.A. Bisphosphonate action. Alendronate localization in rat bone and effects on osteoclast ultrastructure. J. Clin. Invest. 88 (1991) 2095-2105
29. Li Y.Y., Chang J.W., Chou W.C., Liaw C.C., Wang H.M., Huang J.S., Wang C.H., and Yeh K.Y. Zoledronic acid is unable to induce apoptosis, but slows tumor growth and prolongs survival for non-small-cell lung cancers. Lung Cancer 59 (2008) 180-191
30. Busch M., Rave-Fränk M., Hille A., and Dühmke E. Influence of clodronate on breast cancer cells in vitro. Eur. J. Med. Res. 3 (1998) 427-431
31. Coxon F.P., Benford H.L., Russell R.G., and Rogers M.J. Protein synthesis is required for caspase activation and induction of apoptosis by bisphosphonate drugs. Mol. Pharmacol. 54 (1998) 631-638
32. Jänicke R.U., Sprengart M.L., Wati M.R., and Porter A.G. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273 (1998) 9357-9360
33. Rahman M., Davis S.R., Pumphrey J.G., Bao J., Nau M.M., Meltzer P.S., and Lipkowitz S. TRAIL induces apoptosis in triple-negative breast cancer cells with a mesenchymal phenotype. Breast Cancer Res. Treat. 113 (2008) 217-230
34. Coleman R. Potential use of bisphosphonates in the prevention of metastases in early-stage breast cancer. Clin. Breast Cancer Suppl. 1 (2007) 29-35
35. Jones D.H., Nakashima T., Sanchez O.H., Kozieradzki I., Komarova S.V., Sarosi I., Morony S., Rubin E., Sarao R., Hojilla C.V., Komnenovic V., Kong Y.Y., Schreiber M., Dixon S.J., Sims S.M., Khokha R., Wada T., and Penninger J.M. Regulation of cancer cell migration and bone metastasis by RANKL. Nature 440 (2006) 692-696