New perspectives on zoledronic acid in breast cancer: Potential augmentation of anticancer immune response

Cancer Investigation

Volumn 29, Issue 8, 2011, Pages 533-541

  Hamilton, Erika ^a   Clay, Timothy M ^a   Blackwell, Kimberly L ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Anticancer; Bisphosphonate; Breast cancer; T cells; Zoledronic acid

Indexed keywords

CLODRONIC ACID; CYCLOPHOSPHAMIDE; DOCETAXEL; EPIRUBICIN; ESTROGEN RECEPTOR; ETIDRONIC ACID; FLUOROURACIL; IBANDRONIC ACID; INTERLEUKIN 2; METHOTREXATE; NERIDRONIC ACID; OLPADRONIC ACID; PACLITAXEL; PAMIDRONIC ACID; RISEDRONIC ACID; UFT; ZOLEDRONIC ACID;

ANTINEOPLASTIC ACTIVITY; BREAST CANCER; CELL EXPANSION; CELL PROLIFERATION; GAMMA DELTA T LYMPHOCYTE; HUMAN; IMMUNE RESPONSE; LOW DRUG DOSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW;

BONE DENSITY CONSERVATION AGENTS; BREAST NEOPLASMS; DIPHOSPHONATES; FEMALE; HUMANS; IMIDAZOLES; LYMPHOCYTE ACTIVATION; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES;

EID: 80052734955     PISSN: 07357907     EISSN: 15324192     Source Type: Journal    
DOI: 10.3109/07357907.2011.605413     Document Type: Review

References (78)

1. Casetti R, Martino, A. Te plasticity of gamma delta T cells: innate immunity, antigen presentation and new immunotherapy. Cell Mol Immunol 2008;5:161-170.
2. Dieli F, Poccia F, Lipp M, Sireci G, Caccamo N, Di Sano C, Salerno A. Diferentiation of efector/memory Vdelta2 T cells and migratory routes in lymph nodes or infammatory sites. J Exp Med 2003;198:391-397. (Pubitemid 36980610)
3. 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 aminobispho-sphonate antigen. J Immunol 2001;166:5508-5514. (Pubitemid 32374172)
4. Kabelitz D, Wesch D, He W. Perspectives of gammadelta T cells in tumor immunology. Cancer Res 2007;67:5-8. (Pubitemid 46142752)
5. Vantourout P, Mookerjee-Basu J, Rolland C, Pont F, Martin H, Davrinche C, Martinez LO, Perret B, Collet X, Peri-gaud C, Peyrottes S, Champagne E. Specifc requirements for Vgamma9Vdelta2 T cell stimulation by a natural adenylated phos-phoantigen. J Immunol 2009;183:3848-3857.
6. 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.
7. 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. (Pubitemid 26349174)
8. 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. (Pubitemid 27427670)
9. Boissier, S Ferreras M, Peyruchaud O, Magnetto S, Ebetino FH, Colombel M, Delmas P, Delaisse JM, Clezardin P. Bisphospho-nates inhibit breast and prostate carcinoma cell invasion, an early event in the formation of bone metastases. Cancer Res 2000;60:2949-2954. (Pubitemid 30395820)
10. 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 efects. Br J Cancer 2003;88:1631-1640. (Pubitemid 36713793)
11. Fromigue O, Lagneaux L, Body JJ. Bisphosphonates induce breast cancer cell death in vitro. J Bone Miner Res 2000;15:2211-2221.
12. Senaratne SG, Pirianov G, Mansi JL, Arnett TR, Colston KW. Bis-phosphonates induce apoptosis in human breast cancer cell lines. Br J Cancer 2000;82:1459-1468. (Pubitemid 30175914)
13. Jagdev SP, Coleman RE, Shipman CM, Rostami HA, Croucher PI. Te bisphosphonate, zoledronic acid, induces apoptosis of breast cancer cells: evidence for synergy with paclitaxel. Br J Cancer 2001;84:1126-1134. (Pubitemid 32448513)
14. Senaratne SG, Mansi JL, Colston KW. Te bisphosphonate zole-dronic 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. (Pubitemid 34548073)
15. Verdijk R, Franke HR, Wolbers F, Vermes I. Diferential effects of bisphosphonates on breast cancer cell lines. Cancer Lett 2007;246:308-312. (Pubitemid 44959401)
16. Dhar S, Chiplunkar SV. Lysis of aminobisphosphonate-sensitized MCF-7 breast tumor cells by Vgamma9Vdelta2Tcells.Cancer Im-mun 2010;10:10.
17. 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. (Pubitemid 35364119)
18. Wood J, Bonjean K, Ruetz S, Bellahcene A, Devy L, Foidart JM, Castronovo V, Green JR. Novel antiangiogenic efects of the bis-phosphonate compound zoledronic acid. J Pharmacol Exp Ter 2002;302:1055-1061. (Pubitemid 34920226)
19. 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. (Pubitemid 37345986)
20. 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.
21. Witters LM, Crispino J, Fraterrigo T, Green J, Lipton A. Efect 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. (Pubitemid 36961148)
22. Hiraga T, Ueda A, Tamura D, Hata K, Ikeda F, Williams PJ, Yoneda T. Efects of oral UFT combined with or without zole-dronic acid on bone metastasis in the 4T1/luc mouse breast cancer. Int J Cancer 2003;106:973-979. (Pubitemid 37071680)
23. Vogt U, Bielawski KP, Bosse U, Schlotter CM. Breast tumour growth inhibition in vitro through the combination of cyclophosphamide/metotrexate/5- fuorouracil, epiru-bicin/cyclophosphamide, epirubicin/paclitaxel, and epiru-bicin/docetaxel with the bisphosphonates ibandronate and zoledronic acid. Oncol Rep 2004;12:1109-1114.
24. 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. (Pubitemid 40038702)
25. Woodward JK, Neville-Webbe HL, Coleman RE, Holen I. Combined efects of zoledronic acid and doxorubicin on breast cancer cell invasion in vitro. Anticancer Drugs 2005;16:845-854. (Pubitemid 41215749)
26. 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 geftinib in inhibiting breast and prostate cancer. Endocr Relat Cancer 2005;12:1051-1058. (Pubitemid 41815796)
27. Neville-Webbe HL, Evans CA, Coleman RE, Holen I. Mechanisms of the synergistic interaction between the bisphosphonate zole-dronic acid and the chemotherapy agent paclitaxel in breast cancer cells in vitro. Tumour Biol 2006;27:92-103.
28. Ural AU, Avcu F, Candir M, Guden M, Ozcan MA. In vitro syn-ergistic cytoreductive efects of zoledronic acid and radiation on breast cancer cells. Breast Cancer Res 2006;8:R52.
29. Ottewell PD, Jones M, Coleman RE, Holen I. Combined efects 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.
30. Duivenvoorden WC, Vukmirovic-Popovic S, Kalina M, Seidlitz E, Singh G. Efect 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. (Pubitemid 46762946)
31. Ottewell PD, Deux B, Monkkonen H, Cross S, Coleman RE, Clezardin P, Holen I. Diferential efect of doxorubicin and zole-dronic acid on intraosseous versus extraosseous breast tumor growth in vivo. Clin Cancer Res 2008;14:4658-4666.
32. Winter MC, Holen I, Coleman RE. Exploring the anti-tumour activity of bisphosphonates in early breast cancer. Cancer Treat Rev 2008;34:453-475.
33. 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.
34. Cabillic F, Toutirais O, Lavoue V, de La Pintiere CT, Daniel P, Rioux-Leclerc N, Turlin B, Monkkonen H, Monkkonen J, Boud-jema K, Catros V, Bouet-Toussaint F. Aminobisphosphonate-pretreated dendritic cells trigger successful Vgamma9Vdelta2 T cell amplifcation for immunotherapy in advanced cancer patients. Cancer Immunol Immunother 2010;59:1611-1619.
35. Naoe M, Ogawa Y, Takeshita K, Morita J, Shichijo T, Fuji K, Fuk-agai T, Iwamoto S, Terao S. Zoledronate stimulates gamma delta T cells in prostate cancer patients. Oncol Res 2010;18:493-501.
36. Roelofs AJ, Jauhiainen M, Monkkonen H, Rogers MJ, Monkkonen J, Tompson 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.
37. Santini D, Martini F, Fratto ME, Galluzzo S, Vincenzi B, Agrati C, Turchi F, Piacentini P, Rocci L, Manavalan JS, Tonini G, Poc-cia F. In vivo efects of zoledronic acid on peripheral gammadelta T lymphocytes in early breast cancer patients. Cancer Immunol Immunother 2009;58:31-38.
38. Tompson K, Roelofs AJ, Jauhiainen M, Monkkonen H, Monkko-nen J, Rogers MJ. Activation of gammadelta T cells by bisphospho-nates. Adv Exp Med Biol 2010;658:11-20.
39. 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.
40. Yu P, Fu YX. Tumor-infltrating T lymphocytes: friends or foes? Lab Invest 2006;86:231-245.
41. Michalek J, Buchler T, Hajek R. T lymphocyte therapy of cancer. Physiol Res 2004;53:463-469. (Pubitemid 39486702)
42. Tanaka, Y. Human gamma delta T cells and tumor immunother-apy. J Clin Exp Hematop 2006;46:11-23.
43. Fritz, G. Targeting the mevalonate pathway for improved anti-cancer therapy. Curr Cancer Drug Targets 2009;9:626-638.
44. Suzuki T, Terao S, Acharya B, Naoe M, Yamamoto S, Okamura H, Gotoh A. Te antitumour efect of {gamma}{delta} T-cells is enhanced by valproic acid-induced up-regulation of NKG2D lig-ands. Anticancer Res 2010;30:4509-4513.
45. Monkkonen H, Kuokkanen J, Holen I, Evans A, Lefey DV, Jauhi-ainen M, Auriola S, Monkkonen J. Bisphosphonate-induced ATP analog formation and its efect on inhibition of cancer cell growth. Anticancer Drugs 2008;19:391-399.
46. 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.
47. Nakajima J, Murakawa T, Fukami T, Goto S, Kaneko T, Yoshida Y, Takamoto S, Kakimi K. A phase I study of adoptive im-munotherapy for recurrent non-small-cell lung cancer patients with autologous gammadelta T cells. Eur J Cardiothorac Surg 2010;37:1191-1197.
48. Coleman RE, Winter MC, Cameron D, Bell R, Dodwell D, Keane MM, Gil M, Ritchie D, Passos-Coelho JL, Wheatley D, Burkin-shaw R, Marshall SJ, Torpe H. Te efects of adding zole-dronic acid to neoadjuvant chemotherapy on tumour response: exploratory evidence for direct anti-tumour activity in breast cancer. Br J Cancer 2010;102:1099-1105.
49. Powles T, Paterson A, McCloskey E, Schein P, Schefer 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.
50. Diel IJ, Solomayer EF, Costa SD, Gollan C, Goerner R, Wall-wiener D, Kaufmann M, Bastert G. Reduction in new metastases in breast cancer with adjuvant clodronate treatment. N Engl J Med 1998;339:357-363. (Pubitemid 28363797)
51. 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 micrometas-tases to the bone marrow: a long-term follow-up. Ann Oncol 2008;19:2007-2011.
52. Saarto T, Blomqvist C, Virkkunen P, Elomaa I. Adjuvant clo-dronate 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. (Pubitemid 32063474)
53. 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. (Pubitemid 39563937)
54. 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.
55. Solomayer EF, Gebauer G, Hirnle P, Jannit W, Luck HJ, Becker S, Huober J, Kramer B, Wackwitz B, Fehm T. Infuence 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.
56. Af 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, Weil-baecher K. Efect 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.
57. Rack B, Juckstock J, Genss EM, Schoberth A, Schindlbeck C, Strobl B, Heinrigs M, Rammel G, Zwingers T, Sommer H, Friese K, Janni W. Efect of zoledronate on persisting isolated tumour cells in patients with early breast cancer. Anticancer Res 2010;30:1807-1813.
58. Eidtmann H, de Boer R, Bundred N, Llombart-Cussac A, Davidson N, Neven P, von Minckwitz G, Miller J, Schenk N, Coleman R. Efcacy 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.
59. Coleman R, Bundred N, de Boer R, Llombart A, Campbell I, Neven P, Barrios C, Miller J, Dias R, Brufsky A. Impact of zole-dronic 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.
60. 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.
61. 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.
62. Coleman RE, Torpe 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. Te AZURE trial (BIG 01/04) [oral presentation]. Presented at 33rd Annual San Antonio Breast Cancer Symposium; San Antonio, TX; December 8-12, 2010.
63. Mystakidou K, Katsouda E, Parpa E, Kelekis A, Galanos A, Vlahos L. Randomized, open label, prospective study on the efect of zole-dronic 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. (Pubitemid 41003454)
64. 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.
65. Zarogoulidis K, Boutsikou E, Zarogoulidis P, Elefheriadou E, Kontakiotis T, Lithoxopoulou H, Tzanakakis G, Kanakis I, Kara-manos NK. Te impact of zoledronic acid therapy in survival of lung cancer patients with bone metastasis. Int J Cancer 2009;125:1705-1709.
66. Aviles A, Nambo MJ, Neri N, Castaneda C, Cleto S, Huerta-Guzman J. Antitumor efect of zoledronic acid in previously untreated patients with multiple myeloma. Med Oncol 2007;24:227-230. (Pubitemid 350135975)
67. Morgan GJ, Davies FE, Gregory WM, Cocks K, Bell SE, Szubert AJ, Navarro-Coy N, Drayson MT, Owen RG, Feyler S, Ashcrof 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.
68. Gnant M. Bisphosphonates in the prevention of disease recurrence: current results and ongoing trials. Curr Cancer Drug Targets 2009;9:824-833.
69. Mundy GR. Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Cancer 2002;2:584-593. (Pubitemid 37328925)
70. Norton L, Massague J. Is cancer a disease of self-seeding? Nat Med. 2006; 12: 875-878. (Pubitemid 44175132)
71. Greenberg S, Park JW, Melisko ME, Goga A, Moasser MM, Anderson JH, Scott L, Petrillo A, Moore DH, Rugo HS. Efect 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.
72. Green JR. Bisphosphonates: preclinical review. Oncologist 2004;9(Suppl 4):3-13. (Pubitemid 39363164)
73. Kimmel DB. Mechanism of action, pharmacokinetic and phar-macodynamic profle, and clinical applications of nitrogen-containing bisphosphonates. J Dent Res 2007;86:1022-1033.
74. Tanvetyanon T, Stif PJ. Management of the adverse effects associated with intravenous bisphosphonates. Ann Oncol 2006;17:897-907. (Pubitemid 43785797)
75. 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.
76. 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. (Pubitemid 351161269)
77. Fouque-Aubert A, Chapurlat R. Infuence of RANKL inhibition on immune system in the treatment of bone diseases. Joint Bone Spine 2008;75:5-10.
78. 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.