New Perspectives on Zoledronic Acid in Breast Cancer: Potential Augmentation of Anticancer Immune Response

REFERENCES

• Casetti R, Martino, A. The plasticity of gamma delta T cells: innate immunity, antigen presentation and new immunotherapy. Cell Mol Immunol 2008;5:161–170.
   PubMed Web of Science ®Google Scholar
• Dieli F, Poccia F, Lipp M, Sireci G, Caccamo N, Di Sano C, Salerno A. Differentiation of effector/memory Vdelta2 T cells and migratory routes in lymph nodes or inflammatory sites. J Exp Med 2003;198:391–397.
   PubMed Web of Science ®Google Scholar
• Miyagawa F, Tanaka Y, Yamashita S, Minato N. Essential requirement of antigen presentation by monocyte lineage cells for the activation of primary human gamma delta T cells by aminobisphosphonate antigen. J Immunol 2001;166:5508–5514.
   PubMed Web of Science ®Google Scholar
• Kabelitz D, Wesch D, He W. Perspectives of gammadelta T cells in tumor immunology. Cancer Res 2007;67:5–8.
   PubMed Web of Science ®Google Scholar
• Vantourout P, Mookerjee-Basu J, Rolland C, Pont F, Martin H, Davrinche C, Martinez LO, Perret B, Collet X, Perigaud C, Peyrottes S, Champagne E. Specific requirements for Vgamma9Vdelta2 T cell stimulation by a natural adenylated phosphoantigen. J Immunol 2009;183:3848–3857.
   PubMed Web of Science ®Google Scholar
• Maniar A, Zhang X, Lin W, Gastman BR, Pauza CD, Strome SE, Chapoval AI. Human gammadelta T lymphocytes induce robust NK cell-mediated antitumor cytotoxicity through CD137 engagement. Blood 2010;116:1726–1733.
   PubMed Web of Science ®Google Scholar
• van der Pluijm G, Vloedgraven H, van Beek E, van der Wee-Pals L, Lowik C, Papapoulos S. Bisphosphonates inhibit the adhesion of breast cancer cells to bone matrices in vitro. J Clin Invest 1996;98:698–705.
   PubMed Web of Science ®Google Scholar
• Boissier S, Magnetto S, Frappart L, Cuzin B, Ebetino FH, Delmas PD, Clezardin P. Bisphosphonates inhibit prostate and breast carcinoma cell adhesion to unmineralized and mineralized bone extracellular matrices. Cancer Res 1997;57:3890–3894.
   PubMed Web of Science ®Google Scholar
• Boissier, S Ferreras M, Peyruchaud O, Magnetto S, Ebetino FH, Colombel M, Delmas P, Delaisse JM, Clezardin P. Bisphosphonates inhibit breast and prostate carcinoma cell invasion, an early event in the formation of bone metastases. Cancer Res 2000;60:2949–2954.
   PubMed Web of Science ®Google Scholar
• 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;88:1631–1640.
   PubMed Web of Science ®Google Scholar
• Fromigue O, Lagneaux L, Body JJ. Bisphosphonates induce breast cancer cell death in vitro. J Bone Miner Res 2000;15:2211–2221.
   PubMed Web of Science ®Google Scholar
• Senaratne SG, Pirianov G, Mansi JL, Arnett TR, Colston KW. Bisphosphonates induce apoptosis in human breast cancer cell lines. Br J Cancer 2000;82:1459–1468.
   PubMed Web of Science ®Google Scholar
• Jagdev SP, Coleman RE, Shipman CM, Rostami HA, Croucher PI. The bisphosphonate, zoledronic acid, induces apoptosis of breast cancer cells: evidence for synergy with paclitaxel. Br J Cancer 2001;84:1126–1134.
   PubMed Web of Science ®Google Scholar
• 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;86:1479–1486.
   PubMed Web of Science ®Google Scholar
• Verdijk R, Franke HR, Wolbers F, Vermes I. Differential effects of bisphosphonates on breast cancer cell lines. Cancer Lett 2007;246:308–312.
   PubMed Web of Science ®Google Scholar
• Dhar S, Chiplunkar SV. Lysis of aminobisphosphonate-sensitized MCF-7 breast tumor cells by Vgamma9Vdelta2 T cells. Cancer Immun 2010;10:10.
   PubMedGoogle Scholar
• Fournier P, Boissier S, Filleur S, Guglielmi J, Cabon F, Colombel M, Clezardin P. Bisphosphonates inhibit angiogenesis in vitro and testosterone-stimulated vascular regrowth in the ventral prostate in castrated rats. Cancer Res 2002;62:6538–6544.
   PubMed Web of Science ®Google Scholar
• Wood J, Bonjean K, Ruetz S, Bellahcene A, Devy L, Foidart JM, Castronovo V, Green JR. Novel antiangiogenic effects of the bisphosphonate compound zoledronic acid. J Pharmacol Exp Ther 2002;302:1055–1061.
   PubMed Web of Science ®Google Scholar
• Bezzi M, Hasmim M, Bieler G, Dormond O, Ruegg C. Zoledronate sensitizes endothelial cells to tumor necrosis factor-induced programmed cell death: evidence for the suppression of sustained activation of focal adhesion kinase and protein kinase B/Akt. J Biol Chem 2003;278:43603–43614.
   PubMed Web of Science ®Google Scholar
• Stresing V, Fournier PG, Bellahcene A, Benzaid I, Monkkonen H, Colombel M, Ebetino FH, Castronovo V, Clezardin P. Nitrogen-containing bisphosphonates can inhibit angiogenesis in vivo without the involvement of farnesyl pyrophosphate synthase. Bone 2011;48:259–266.
   PubMed Web of Science ®Google Scholar
• Witters LM, Crispino J, Fraterrigo T, Green J, Lipton A. Effect of the combination of docetaxel, zoledronic acid, and a COX-2 inhibitor on the growth of human breast cancer cell lines. Am J Clin Oncol 2003;26:S92–S97.
   PubMed Web of Science ®Google Scholar
• Hiraga T, Ueda A, Tamura D, Hata K, Ikeda F, Williams PJ, Yoneda T. Effects of oral UFT combined with or without zoledronic acid on bone metastasis in the 4T1/luc mouse breast cancer. Int J Cancer 2003;106:973–979.
   PubMed Web of Science ®Google Scholar
• Vogt U, Bielawski KP, Bosse U, Schlotter CM. Breast tumour growth inhibition in vitro through the combination of cyclophosphamide/metotrexate/5-fluorouracil, epirubicin/cyclophosphamide, epirubicin/paclitaxel, and epirubicin/docetaxel with the bisphosphonates ibandronate and zoledronic acid. Oncol Rep 2004;12:1109–1114.
   PubMed Web of Science ®Google Scholar
• Neville-Webbe HL, Rostami-Hodjegan A, Evans CA, Coleman RE, Holen I. Sequence- and schedule-dependent enhancement of zoledronic acid induced apoptosis by doxorubicin in breast and prostate cancer cells. Int J Cancer 2005;113:364–371.
   PubMed Web of Science ®Google Scholar
• Woodward JK, Neville-Webbe HL, Coleman RE, Holen I. Combined effects of zoledronic acid and doxorubicin on breast cancer cell invasion in vitro. Anticancer Drugs 2005;16:845–854.
   PubMed Web of Science ®Google Scholar
• Melisi D, Caputo R, Damiano V, Bianco R, Veneziani BM, Bianco AR, De Placido S, Ciardiello F, Tortora G. Zoledronic acid cooperates with a cyclooxygenase-2 inhibitor and gefitinib in inhibiting breast and prostate cancer. Endocr Relat Cancer 2005;12:1051–1058.
   PubMed Web of Science ®Google Scholar
• Neville-Webbe HL, Evans CA, Coleman RE, Holen I. Mechanisms of the synergistic interaction between the bisphosphonate zoledronic acid and the chemotherapy agent paclitaxel in breast cancer cells in vitro. Tumour Biol 2006;27:92–103.
   PubMed Web of Science ®Google Scholar
• Ural AU, Avcu F, Candir M, Guden M, Ozcan MA. In vitro synergistic cytoreductive effects of zoledronic acid and radiation on breast cancer cells. Breast Cancer Res 2006;8:R52.
   Google Scholar
• Ottewell PD, Jones M, Coleman RE, Holen I. Combined effects of cytotoxic drugs and anti-resorptive agents in vivo [poster]. Presented at 29th Annual San Antonio Breast Cancer Symposium; San Antonio, TX; December 14–17, 2006.
   Google Scholar
• Duivenvoorden WC, Vukmirovic-Popovic S, Kalina M, Seidlitz E, Singh G. Effect of zoledronic acid on the doxycycline-induced decrease in tumour burden in a bone metastasis model of human breast cancer. Br J Cancer 2007;96:1526–1531.
   PubMed Web of Science ®Google Scholar
• Ottewell PD, Deux B, Monkkonen H, Cross S, Coleman RE, Clezardin P, Holen I. Differential effect of doxorubicin and zoledronic acid on intraosseous versus extraosseous breast tumor growth in vivo. Clin Cancer Res 2008;14:4658–4666.
   PubMed Web of Science ®Google Scholar
• Winter MC, Holen I, Coleman RE. Exploring the anti-tumour activity of bisphosphonates in early breast cancer. Cancer Treat Rev 2008;34:453–475.
   PubMed Web of Science ®Google Scholar
• Benzaid I, Monkkonen H, Stresing V, Bonnelye E, Green J, Monkkonen J, Touraine JL, Clezardin P. High phosphoantigen levels in bisphosphonate-treated human breast tumors promote V{gamma}9V{delta}2 T-cell chemotaxis and cytotoxicity in vivo. Cancer Res 2011;71:4562–4572.
   PubMed Web of Science ®Google Scholar
• Cabillic F, Toutirais O, Lavoue V, de La Pintiere CT, Daniel P, Rioux-Leclerc N, Turlin B, Monkkonen H, Monkkonen J, Boudjema K, Catros V, Bouet-Toussaint F. Aminobisphosphonate-pretreated dendritic cells trigger successful Vgamma9Vdelta2 T cell amplification for immunotherapy in advanced cancer patients. Cancer Immunol Immunother 2010;59:1611–1619.
   Google Scholar
• Naoe M, Ogawa Y, Takeshita K, Morita J, Shichijo T, Fuji K, Fukagai T, Iwamoto S, Terao S. Zoledronate stimulates gamma delta T cells in prostate cancer patients. Oncol Res 2010;18:493–501.
   PubMed Web of Science ®Google Scholar
• Roelofs AJ, Jauhiainen M, Monkkonen H, Rogers MJ, Monkkonen 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.
   PubMed Web of Science ®Google Scholar
• Santini D, Martini F, Fratto ME, Galluzzo S, Vincenzi B, Agrati C, Turchi F, Piacentini P, Rocci L, Manavalan JS, Tonini G, Poccia F. In vivo effects of zoledronic acid on peripheral gammadelta T lymphocytes in early breast cancer patients. Cancer Immunol Immunother 2009;58:31–38.
   PubMed Web of Science ®Google Scholar
• Thompson K, Roelofs AJ, Jauhiainen M, Monkkonen H, Monkkonen J, Rogers MJ. Activation of gammadelta T cells by bisphosphonates. Adv Exp Med Biol 2010;658:11–20.
   PubMed Web of Science ®Google Scholar
• Liseth K, Ersvaer E, Hervig T, Bruserud O. Combination of intensive chemotherapy and anticancer vaccines in the treatment of human malignancies: the hematological experience. J Biomed Biotechnol 2010;2010:692097.
   PubMed Web of Science ®Google Scholar
• Yu P, Fu YX. Tumor-infiltrating T lymphocytes: friends or foes? Lab Invest 2006;86:231–245.
   PubMed Web of Science ®Google Scholar
• Michalek J, Buchler T, Hajek R. T lymphocyte therapy of cancer. Physiol Res 2004;53:463–469.
   PubMed Web of Science ®Google Scholar
• Tanaka, Y. Human gamma delta T cells and tumor immunotherapy. J Clin Exp Hematop 2006;46:11–23.
   PubMedGoogle Scholar
• Fritz, G. Targeting the mevalonate pathway for improved anticancer therapy. Curr Cancer Drug Targets 2009;9:626–638.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Terao S, Acharya B, Naoe M, Yamamoto S, Okamura H, Gotoh A. The antitumour effect of {gamma}{delta} T-cells is enhanced by valproic acid-induced up-regulation of NKG2D ligands. Anticancer Res 2010;30:4509–4513.
   PubMed Web of Science ®Google Scholar
• Monkkonen H, Kuokkanen J, Holen I, Evans A, Lefley DV, Jauhiainen M, Auriola S, Monkkonen J. Bisphosphonate-induced ATP analog formation and its effect on inhibition of cancer cell growth. Anticancer Drugs 2008;19:391–399.
   PubMed Web of Science ®Google Scholar
• Meraviglia S, Eberl M, Vermijlen D, Todaro M, Buccheri S, Cicero G, La Mendola C, Guggino G, D'Asaro M, Orlando V, Scarpa F, Roberts A, Caccamo N, Stassi G, Dieli F, Hayday AC. In vivo manipulation of Vgamma9Vdelta2 T cells with zoledronate and low-dose interleukin-2 for immunotherapy of advanced breast cancer patients. Clin Exp Immunol 2010;161:290–297.
   PubMedGoogle Scholar
• Nakajima J, Murakawa T, Fukami T, Goto S, Kaneko T, Yoshida Y, Takamoto S, Kakimi K. A phase I study of adoptive immunotherapy for recurrent non-small-cell lung cancer patients with autologous gammadelta T cells. Eur J Cardiothorac Surg 2010;37:1191–1197.
   PubMed Web of Science ®Google Scholar
• Coleman RE, Winter MC, Cameron D, Bell R, Dodwell D, Keane MM, Gil M, Ritchie D, Passos-Coelho JL, Wheatley D, Burkinshaw R, Marshall SJ, Thorpe H. The effects of adding zoledronic acid to neoadjuvant chemotherapy on tumour response: exploratory evidence for direct anti-tumour activity in breast cancer. Br J Cancer 2010;102:1099–1105.
   PubMed Web of Science ®Google Scholar
• Powles T, Paterson A, McCloskey E, Schein P, Scheffler B, Tidy A, Ashley S, Smith I, Ottestad L, Kanis J. Reduction in bone relapse and improved survival with oral clodronate for adjuvant treatment of operable breast cancer [ISRCTN83688026]. Breast Cancer Res 2006;8:R13.
   PubMed Web of Science ®Google Scholar
• Diel IJ, Solomayer EF, Costa SD, Gollan C, Goerner R, Wallwiener D, Kaufmann M, Bastert G. Reduction in new metastases in breast cancer with adjuvant clodronate treatment. N Engl J Med 1998;339:357–363.
   PubMed Web of Science ®Google Scholar
• Diel IJ, Jaschke A, Solomayer EF, Gollan C, Bastert G, Sohn C, Schuetz F. Adjuvant oral clodronate improves the overall survival of primary breast cancer patients with micrometastases to the bone marrow: a long-term follow-up. Ann Oncol 2008;19:2007–2011.
   PubMed Web of Science ®Google Scholar
• Saarto T, Blomqvist C, Virkkunen P, Elomaa I. Adjuvant clodronate treatment does not reduce the frequency of skeletal metastases in node-positive breast cancer patients: 5-year results of a randomized controlled trial. J Clin Oncol 2001;19:10–17.
   PubMed Web of Science ®Google Scholar
• Saarto T, Vehmanen L, Virkkunen P, Blomqvist C. Ten-year follow-up of a randomized controlled trial of adjuvant clodronate treatment in node-positive breast cancer patients. Acta Oncol 2004;43:650–656.
   PubMed Web of Science ®Google Scholar
• Lin AY, Park JW, Scott J, Melisko M, Goga A, Moasser M, Moore DH, Rugo HS. Zoledronic acid as adjuvant therapy for women with early stage breast cancer and disseminated tumor cells in bone marrow [abstract 559]. J Clin Oncol 2008;26(Suppl):20s.
   PubMed Web of Science ®Google Scholar
• Solomayer EF, Gebauer G, Hirnle P, Jannit W, Luck HJ, Becker S, Huober J, Kramer B, Wackwitz B, Fehm T. Influence of zoledronic acid on disseminated tumor cells (DTC) in primary breast cancer patients. Presented at 31st Annual San Antonio Breast Cancer Symposium; San Antonio, TX; December 10–14, 2008.
   Google Scholar
• Aft R, Naughton M, Trinkaus K, Watson M, Ylagan L, Chavez-Macgregor M, Zhai J, Kuo S, Shannon W, Diemer K, Herrmann V, Dietz J, Ali A, Ellis M, Weiss P, Eberlein T, Ma C, Fracasso PM, Zoberi I, Taylor M, Gillanders W, Pluard T, Mortimer J, Weilbaecher K. 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.
   PubMed Web of Science ®Google Scholar
• Rack B, Juckstock J, Genss EM, Schoberth A, Schindlbeck C, Strobl B, Heinrigs M, Rammel G, Zwingers T, Sommer H, Friese K, Janni W. Effect of zoledronate on persisting isolated tumour cells in patients with early breast cancer. Anticancer Res 2010;30:1807–1813.
   PubMed Web of Science ®Google Scholar
• Eidtmann H, de Boer R, Bundred N, Llombart-Cussac A, Davidson N, Neven P, von Minckwitz G, Miller J, Schenk N, Coleman R. Efficacy of zoledronic acid in postmenopausal women with early breast cancer receiving adjuvant letrozole: 36-month results of the ZO-FAST study. Ann Oncol 2010;21:2188–2194.
   PubMed Web of Science ®Google Scholar
• Coleman R, Bundred N, de Boer R, Llombart A, Campbell I, Neven P, Barrios C, Miller J, Dias R, Brufsky A. Impact of zoledronic acid in postmenopausal women with early breast cancer receiving adjuvant letrozole: Z-FAST, ZO-FAST, and E-ZO-FAST [poster]. Presented at 32nd Annual San Antonio Breast Cancer Symposium; San Antonio, TX; December 10–13, 2009.
   Google Scholar
• Gnant M, Mlineritsch B, Schippinger W, Luschin-Ebengreuth G, Postlberger 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, Rucklinger E, Greil R, Marth C. Endocrine therapy plus zoledronic acid in premenopausal breast cancer. N Engl J Med 2009;360:679–691.
   PubMed Web of Science ®Google Scholar
• Gnant M, Mlineritsch B, Stoeger H, Luschin-Ebengrueth G, Poestlberger S, Dubsky PC, Jakesz R, Singer CF, Eidtman H, Greil R. Mature results from ABCSG-12: adjuvant ovarian suppression combined with tamoxifen or anastrozole, alone or in combination with zoledronic acid, in premenopausal women with endocrine-responsive early breast cancer [poster]. Presented at 46th Annual Meeting of the American Society of Clinical Oncology; Chicago, IL; June 4–8, 2010.
   Google Scholar
• Coleman RE, Thorpe HC, Cameron D, Dodwell D, Burkinshaw R, Keane M, Gil M, Houston SJ, Grieve RJ, Barrett-Lee PJ, Davies RD, Bell R. Adjuvant treatment with zoledronic acid in stage II/III breast cancer. The AZURE trial (BIG 01/04) [oral presentation]. Presented at 33rd Annual San Antonio Breast Cancer Symposium; San Antonio, TX; December 8–12, 2010.
   Google Scholar
• Mystakidou K, Katsouda E, Parpa E, Kelekis A, Galanos A, Vlahos L. Randomized, open label, prospective study on the effect of zoledronic acid on the prevention of bone metastases in patients with recurrent solid tumors that did not present with bone metastases at baseline. Med Oncol 2005;22:195–201.
   PubMed Web of Science ®Google Scholar
• Zaghloul MS, Boutrus R, El-Hossieny H, Kader YA, El-Attar I, Nazmy M. A prospective, randomized, placebo-controlled trial of zoledronic acid in bony metastatic bladder cancer. Int J Clin Oncol 2010;15:382–389.
   PubMed Web of Science ®Google Scholar
• Zarogoulidis K, Boutsikou E, Zarogoulidis P, Eleftheriadou E, Kontakiotis T, Lithoxopoulou H, Tzanakakis G, Kanakis I, Karamanos NK. The impact of zoledronic acid therapy in survival of lung cancer patients with bone metastasis. Int J Cancer 2009;125:1705–1709.
   PubMed Web of Science ®Google Scholar
• Aviles A, Nambo MJ, Neri N, Castaneda C, Cleto S, Huerta-Guzman J. Antitumor effect of zoledronic acid in previously untreated patients with multiple myeloma. Med Oncol 2007;24:227–230.
   PubMed Web of Science ®Google Scholar
• Morgan GJ, Davies FE, Gregory WM, Cocks K, Bell SE, Szubert AJ, Navarro-Coy N, Drayson MT, Owen RG, Feyler S, Ashcroft AJ, Ross F, Byrne J, Roddie H, Rudin C, Cook G, Jackson GH, Child JA. First-line treatment with zoledronic acid as compared with clodronic acid in multiple myeloma (MRC Myeloma IX): a randomised controlled trial. Lancet 2010;376:1989–1999.
   PubMed Web of Science ®Google Scholar
• Gnant M. Bisphosphonates in the prevention of disease recurrence: current results and ongoing trials. Curr Cancer Drug Targets 2009;9:824–833.
   PubMed Web of Science ®Google Scholar
• Mundy GR. Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Cancer 2002;2:584–593.
   PubMed Web of Science ®Google Scholar
• Norton L, Massague J. Is cancer a disease of self-seeding? Nat Med 2006;12:875–878.
   PubMed Web of Science ®Google Scholar
• Greenberg S, Park JW, Melisko ME, Goga A, Moasser MM, Anderson JH, Scott L, Petrillo A, Moore DH, Rugo HS. Effect of adjuvant zoledronic acid (ZOL) on disseminated tumor cells (DTC) in the bone marrow (BM) of women with early-stage breast cancer (ESBC): updated results [abstract 1002]. J Clin Oncol 2010;28(Suppl):114s.
   PubMedGoogle Scholar
• Green JR. Bisphosphonates: preclinical review. Oncologist 2004;9(Suppl 4):3–13.
   PubMed Web of Science ®Google Scholar
• Kimmel DB. Mechanism of action, pharmacokinetic and pharmacodynamic profile, and clinical applications of nitrogen-containing bisphosphonates. J Dent Res 2007;86:1022–1033.
   PubMed Web of Science ®Google Scholar
• Tanvetyanon T, Stiff PJ. Management of the adverse effects associated with intravenous bisphosphonates. Ann Oncol 2006;17:897–907.
   PubMed Web of Science ®Google Scholar
• Anastasilakis AD, Toulis KA, Polyzos SA, Terpos E. RANKL inhibition for the management of patients with benign metabolic bone disorders. Expert Opin Investig Drugs 2009;18:1085–1102.
   PubMed Web of Science ®Google Scholar
• Chakravarti A, Marceau AA, Flamand L, Poubelle PE. Normal human primary CD4+ T lymphocytes synthesize and release functional osteoprotegerin in vitro. Lab Invest 2008;88:171–184.
   PubMed Web of Science ®Google Scholar
• Fouque-Aubert A, Chapurlat R. Influence of RANKL inhibition on immune system in the treatment of bone diseases. Joint Bone Spine 2008;75:5–10.
   PubMed Web of Science ®Google Scholar
• Totsuka T, Kanai T, Nemoto Y, Tomita T, Okamoto R, Tsuchiya K, Nakamura T, Sakamoto N, Akiba H, Okumura K, Yagita H, Watanabe M. RANK-RANKL signaling pathway is critically involved in the function of CD4+CD25+ regulatory T cells in chronic colitis. J Immunol 2009;182:6079–6087.
   PubMed Web of Science ®Google Scholar