Comparison of γδ T cell responses and farnesyl diphosphate synthase inhibition in tumor cells pretreated with zoledronic acid

Cancer Science

Volumn 104, Issue 5, 2013, Pages 536-542

  Idrees, Atif S M ^a   Sugie, Tomoharu ^a   Inoue, Chiyomi ^a   Murata Hirai, Kaoru ^a   Okamura, Haruki ^b   Morita, Craig T ^c   Minato, Nagahiro ^a   Toi, Masakazu ^a   Tanaka, Yoshimasa ^a,d  

^a KYOTO UNIVERSITY   (Japan)

^b HYOGO COLLEGE OF MEDICINE   (Japan)

^c UNIVERSITY OF IOWA   (United States)

^d NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GERANYLTRANSFERASE; ISOPENTENYL DIPHOSPHATE; TUMOR NECROSIS FACTOR ALPHA; ZOLEDRONIC ACID;

ARTICLE; BIOACCUMULATION; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; CELL KILLING; COCULTURE; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; CYTOPATHOGENIC EFFECT; DOSE RESPONSE; DRUG MECHANISM; DRUG SENSITIVITY; ENZYME INHIBITION; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; IC 50; LYMPHOMA; MYELOID LEUKEMIA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TUMOR CELL;

CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; DIPHOSPHONATES; GERANYLTRANSTRANSFERASE; HEMITERPENES; HL-60 CELLS; HUMANS; IMIDAZOLES; K562 CELLS; LEUKEMIA, MYELOID; LYMPHOMA; MCF-7 CELLS; ORGANOPHOSPHORUS COMPOUNDS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA; U937 CELLS;

EID: 84876416861     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12124     Document Type: Article

References (40)

1. Morita CT, Jin C, Sarikonda G, Wang H. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vγ2Vδ2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol Rev 2007; 215: 59-76.
2. Hayday AC. γδ T cells and the lymphoid stress-surveillance response. Immunity 2009; 31: 184-96.
3. Bonneville M, O'Brien RL, Born WK. γδ T cell effector functions: a blend of innate programming and acquired plasticity. Nat Rev Immunol 2010; 10: 467-78.
4. Kabelitz D, Wesch D, He W. Perspectives of γδ T cells in tumor immunology. Cancer Res 2007; 67: 5-8.
5. Kato Y, Tanaka Y, Miyagawa F, Yamashita S, Minato N. Targeting of tumor cells for human γδ T cells by nonpeptide antigens. J Immunol 2001; 167: 5092-8.
6. Aft R. Bisphosphonates in breast cancer: antitumor effects. Clin Adv Hematol Oncol 2011; 9: 292-9.
7. Bukowski JF, Morita CT, Tanaka Y, Bloom BR, Brenner MB, Band H. Vγ2Vδ2 TCR-dependent recognition of non-peptide antigens and Daudi cells analyzed by TCR gene transfer. J Immunol 1995; 154: 998-1006.
8. Yamashita S, Tanaka Y, Harazaki M, Mikami B, Minato N. Recognition mechanism of non-peptide antigens by human γδ T cells. Int Immunol 2003; 15: 1301-7.
9. Angelini DF, Zambello R, Galandrini R et al. NKG2A inhibits NKG2C effector functions of γδ T cells: implications in health and disease. J Leukoc Biol 2011; 89: 75-84.
10. Toutirais O, Cabillic F, Le Friec G et al. DNAX accessory molecule-1 (CD226) promotes human hepatocellular carcinoma cell lysis by Vγ9Vδ2 T cells. Eur J Immunol 2009; 39: 1361-8.
11. von Lilienfeld-Toal M, Nattermann J, Feldmann G et al. Activated γδ T cells express the natural cytotoxicity receptor natural killer p44 and show cytotoxic activity against myeloma cells. Clin Exp Immunol 2006; 144: 528-33.
12. Wrobel P, Shojaei H, Schittek B et al. Lysis of a broad range of epithelial tumour cells by human γδ T cells: involvement of NKG2D ligands and T-cell receptor- versus NKG2D-dependent recognition. Scand J Immunol 2007; 66: 320-8.
13. Gnant M, Mlineritsch B, Schippinger W et al. Endocrine therapy plus zoledronic acid in premenopausal breast cancer. N Engl J Med 2009; 360: 679-91.
14. Gnant M, Mlineritsch B, Stoeger H et al. Adjuvant endocrine therapy plus zoledronic acid in premenopausal women with early-stage breast cancer: 62-month follow-up from the ABCSG-12 randomised trial. Lancet Oncol 2011; 12: 631-41.
15. Coleman RE, Marshall H, Cameron D et al. Breast-cancer adjuvant therapy with zoledronic acid. N Engl J Med 2011; 365: 1396-405.
16. Coleman R, de Boer R, Eidtmann H et al. Zoledronic acid (zoledronate) for postmenopausal women with early breast cancer receiving adjuvant letrozole (ZO-FAST study): final 60-month results. Ann Oncol 2013; 24: 398-405.
17. Morgan GJ, Davies FE, Gregory WM et al. First-line treatment with zoledronic acid as compared with clodronic acid in multiple myeloma (MRC Myeloma IX): a randomised controlled trial. Lancet 2010; 376: 1989-99.
18. Wang H, Sarikonda G, Puan K-J et al. Indirect stimulation of human Vγ2Vδ2 T cells through alterations in isoprenoid metabolism. J Immunol 2011; 187: 5099-113.
19. Gober H-J, Kistowska M, Angman L, Jenö P, Mori L, De Libero G. Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 2003; 197: 163-8.
20. Thompson K, Rogers MJ. Statins prevent bisphosphonate-induced γ, δ-T-cell proliferation and activation in vitro. J Bone Miner Res 2004; 19: 278-88.
21. Kunzmann V, Wilhelm M. Adjuvant zoledronic acid for breast cancer: mechanism of action? Lancet Oncol 2011; 12: 991-2.
22. + T cells, regulatory T cells, and dendritic cells. J Immunol 2011; 187: 1578-90.
23. Moser B, Eberl M. γδ T cells: novel initiators of adaptive immunity. Immunol Rev 2007; 215: 89-102.
24. Lang JM, Kaikobad MR, Wallace M et al. Pilot trial of interleukin-2 and zoledronic acid to augment γδ T cells as treatment for patients with refractory renal cell carcinoma. Cancer Immunol Immunother 2011; 60: 1447-60.
25. Dieli F, Gebbia N, Poccia F et al. Induction of γδ T-lymphocyte effector functions by bisphosphonate zoledronic acid in cancer patients in vivo. Blood 2003; 102: 2310-1.
26. Dieli F, Vermijlen D, Fulfaro F et al. Targeting human γδ T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res 2007; 67: 7450-7.
27. Meraviglia S, Eberl M, Vermijlen D et al. In vivo manipulation of Vγ9Vδ2 T cells with zoledronate and low-dose interleukin-2 for immunotherapy of advanced breast cancer patients. Clin Exp Immunol 2010; 161: 290-7.
28. Coscia M, Vitale C, Peola S et al. Dysfunctional Vγ9Vδ2 T cells are negative prognosticators and markers of dysregulated mevalonate pathway activity in chronic lymphocytic leukemia cells. Blood 2012; 120: 3271-9.
29. Bryant NL, Gillespie GY, Lopez RD et al. Preclinical evaluation of ex vivo expanded/activated γδ T cells for immunotherapy of glioblastoma multiforme. J Neurooncol 2011; 101: 179-88.
30. 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.
31. Katagiri K, Hattori M, Minato N, Kinashi T. Rap1 functions as a key regulator of T-cell and antigen-presenting cell interactions and modulates T-cell responses. Mol Cell Biol 2002; 22: 1001-15.
32. Riganti C, Massaia M, Davey MS, Eberl M. Human γδ T-cell responses in infection and immunotherapy: common mechanisms, common mediators? Eur J Immunol 2012; 42: 1668-76.
33. Benzaid I, Mönkkönen H, Stresing V et al. High phosphoantigen levels in bisphosphonate-treated human breast tumors promote Vγ9Vδ2 T-cell chemotaxis and cytotoxicity in vivo. Cancer Res 2011; 71: 4562-72.
34. 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.
35. Zhang Y, Cao R, Yin F et al. Lipophilic pyridinium bisphosphonates: potent γδ T cell stimulators. Angew Chem Int Ed Engl 2010; 49: 1136-8.
36. Zhang Y, Cao R, Yin F et al. Lipophilic bisphosphonates as dual farnesyl/geranylgeranyl diphosphate synthase inhibitors: an X-ray and NMR investigation. J Am Chem Soc 2009; 131: 5153-62.
37. Sugie T, Murata-Hirai K, Iwasaki M et al. Zoledronic acid-induced expansion of γδ T cells from early-stage breast cancer patients: effect of IL-18 on helper NK cells. Cancer Immunol Immunother 2012. doi:10.1007/s00262-012-1368-4.
38. Kobayashi H, Tanaka Y, Yagi J, Minato N, Tanabe K. Phase I/II study of adoptive transfer of γδ T cells in combination with zoledronic acid and IL-2 to patients with advanced renal cell carcinoma. Cancer Immunol Immunother 2011; 60: 1075-84.
39. Kobayashi H, Tanaka Y, Shimmura H, Minato N, Tanabe K. Complete remission of lung metastasis following adoptive immunotherapy using activated autologous γδ T-cells in a patient with renal cell carcinoma. Anticancer Res 2010; 30: 575-9.
40. Nicol AJ, Tokuyama H, Mattarollo SR et al. Clinical evaluation of autologous gamma delta T cell-based immunotherapy for metastatic solid tumours. Br J Cancer 2011; 105: 778-86.