Zoledronate sensitizes neuroblastoma-derived tumor-initiating cells to cytolysis mediated by human γδ T cells

Journal of Immunotherapy

Volumn 35, Issue 8, 2012, Pages 598-606

  Nishio, Nobuhiro ^a,b   Fujita, Mitsugu ^a   Tanaka, Yoshimasa ^c   Maki, Hiroyuki ^a   Zhang, Rong ^a   Hirosawa, Tomoya ^a   Demachi Okamura, Ayako ^a   Uemura, Yasushi ^a   Taguchi, Osamu ^a   Takahashi, Yoshiyuki ^b   Kojima, Seiji ^b   Kuzushima, Kiyotaka ^a,b  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

T cell; cancer stem cell; immunotherapy; neuroblastoma; tumorinitiating cell

Indexed keywords

INTERLEUKIN 15; INTERLEUKIN 18; ZOLEDRONIC ACID;

ARTICLE; CANCER IMMUNOTHERAPY; CANCER STEM CELL; CELL THERAPY; CHILD; CYTOLYSIS; DRUG EFFECT; DRUG EFFICACY; FEMALE; HUMAN; HUMAN CELL; INFANT; LYMPHOCYTE CULTURE; MALE; NEUROBLASTOMA; PRESCHOOL CHILD; PRIORITY JOURNAL; T LYMPHOCYTE; TREATMENT OUTCOME; VGAMMA9VSIGMA2 T LYMPHOCYTE;

ADOLESCENT; ADULT; ANIMALS; ANTINEOPLASTIC AGENTS; BONE MARROW NEOPLASMS; CELL LINE, TUMOR; CHILD; CYTOTOXICITY, IMMUNOLOGIC; DIPHOSPHONATES; DRUG SYNERGISM; FEMALE; GROWTH INHIBITORS; HUMANS; IMIDAZOLES; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-15; INTERLEUKIN-18; MALE; MICE; MICE, SCID; NEOPLASTIC STEM CELLS; NEUROBLASTOMA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES; XENOGRAFT MODEL ANTITUMOR ASSAYS; YOUNG ADULT;

EID: 84866673004     PISSN: 15249557     EISSN: 15374513     Source Type: Journal    
DOI: 10.1097/CJI.0b013e31826a745a     Document Type: Article

References (52)

1. .Hoehner JC, Gestblom C, Hedborg F, et al. A developmental model of neuroblastoma: differentiating stroma-poor tumors' progress along an extra-Adrenal chromaffin lineage. Lab Invest. 1996;75:659-675. (Pubitemid 26392797)
2. London WB, Castleberry RP, Matthay KK, et al. Evidence for an age cutoff greater than 365 days for neuroblastoma risk group stratification in the Children's Oncology Group. J Clin Oncol. 2005;23:6459-6465 (Pubitemid 46190236)
3. Yamamoto K, Hanada R, Kikuchi A, et al. Spontaneous regression of localized neuroblastoma detected by mass screening. J Clin Oncol. 1998;16:1265-1269 (Pubitemid 28175738)
4. Park JR, Eggert A, Caron H. Neuroblastoma: biology, prognosis, and treatment. Hematol Oncol Clin North Am. 2010;24:65-86
5. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105-111 (Pubitemid 33041634)
6. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer. 2005;5:275-284 (Pubitemid 40488633)
7. Frank NY, Schatton T, Frank MH. The therapeutic promise of the cancer stem cell concept. J Clin Invest. 2010;120:41-50
8. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396-401. (Pubitemid 39551674)
9. Blair A, Hogge DE, Ailles LE, et al. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-Term proliferative ability in vitro and in vivo. Blood. 1997;89:3104-3112 (Pubitemid 27229792)
10. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730-737 (Pubitemid 27298715)
11. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100:3983-3988 (Pubitemid 36418143)
12. Collins AT, Berry PA, Hyde C, et al. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65:10946-10951 (Pubitemid 41713363)
13. Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030-1037
14. O'Brien CA, Pollett A, Gallinger S, et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106-110 (Pubitemid 46067310)
15. Eramo A, Lotti F, Sette G, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 2008;15:504-514 (Pubitemid 351267301)
16. Costello RT, Mallet F, Gaugler B, et al. Human acute myeloid leukemia CD34+/CD38-progenitor cells have decreased sensitivity to chemotherapy and Fas-induced apoptosis, reduced immunogenicity, and impaired dendritic cell transformation capacities. Cancer Res. 2000;60:4403-4411 (Pubitemid 32103618)
17. Zhou S, Schuetz JD, Bunting KD, et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med. 2001;7:1028-1034 (Pubitemid 32937383)
18. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756-760 (Pubitemid 44949604)
19. Hansford LM, McKee AE, Zhang L, et al. Neuroblastoma cells isolated from bone marrow metastases contain a naturally enriched tumor-initiating cell. Cancer Res. 2007;67:11234-11243 (Pubitemid 350248549)
20. Cotterill SJ, Pearson AD, Pritchard J, et al. Clinical prognostic factors in 1277 patients with neuroblastoma: results of The European Neuroblastoma Study Group "Survey" 1982-1992. Eur J Cancer. 2000;36:901-908 (Pubitemid 30214141)
21. Mahller YY, Williams JP, Baird WH, et al. Neuroblastoma cell lines contain pluripotent tumor initiating cells that are susceptible to a targeted oncolytic virus. PLoS ONE. 2009; 4:e4235
22. Wolfl M, Jungbluth AA, Garrido F, et al. Expression of MHC class I, MHC class II, and cancer germline antigens in neuroblastoma. Cancer Immunol Immunother. 2005;54:400-406 (Pubitemid 40238934)
23. Tanaka Y, Morita CT, Nieves E, et al. Natural and synthetic non-peptide antigens recognized by human gamma delta T cells. Nature. 1995;375:155-158
24. Tanaka Y, Kobayashi H, Terasaki T, et al. Synthesis of pyrophosphate-containing compounds that stimulate Vgamma2Vdelta2 T cells: application to cancer immunotherapy. Med Chem. 2007;3:85-99 (Pubitemid 46062346)
25. Gober HJ, Kistowska M, Angman L, et al. Human T cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med. 2003;197:163-168 (Pubitemid 36152311)
26. Tanaka Y. Human gamma delta T cells and tumor immunotherapy. J Clin Exp Hematop. 2006;46:11-23
27. Miyagawa F, Tanaka Y, Yamashita S, et al. 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 (Pubitemid 32374172)
28. Lamb LS Jr. Gammadelta T cells as immune effectors against high-grade gliomas. Immunol Res. 2009;45:85-95.
29. Wilhelm M, Kunzmann V, Eckstein S, et al. Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood. 2003;102:200-206 (Pubitemid 36759655)
30. Dieli F, Vermijlen D, Fulfaro F, et al. Targeting human gdT cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res. 2007;67: 7450-7457 (Pubitemid 47206575)
31. Kobayashi H, Tanaka Y, Shimmura H, et al. Complete remission of lung metastasis following adoptive immunotherapy using activated autologous gammadelta T-cells in a patient with renal cell carcinoma. Anticancer Res. 2010;30: 575-579.
32. Meraviglia S, Eberl M, Vermijlen D, et al. In vivo manipulation of Vgamma9Vdelta2 T cells with zoledronate and lowdose interleukin-2 for immunotherapy of advanced breast cancer patients. Clin Exp Immunol. 2010;161:290-297
33. Schilbach KE, Geiselhart A, Wessels JT, et al. Human gammadelta T lymphocytes exert natural and IL-2-induced cytotoxicity to neuroblastoma cells. J Immunother. 2000;23: 536-548
34. Chargui J, Combaret V, Scaglione V, et al. Bromohydrin pyrophosphate-stimulated Vgamma9delta2 T cells expanded ex vivo from patients with poor-prognosis neuroblastoma lyse autologous primary tumor cells. J Immunother. 2010;33:591-598
35. Yamashita S, Tanaka Y, Harazaki M, et al. Recognition mechanism of non-peptide antigens by human gammadelta T cells. Int Immunol. 2003;15:1301-1307 (Pubitemid 37369323)
36. FujitaM, Zhu X, Sasaki K, et al. Inhibition of STAT3 promotes the efficacy of adoptive transfer therapy using type-1 CTLs by modulation of the immunological microenvironment in a murine intracranial glioma. J Immunol. 2008;180:2089-2098
37. Fujita M, Zhu X, Ueda R, et al. Effective immunotherapy against murine gliomas using type 1 polarizing dendritic cells -significant roles of CXCL10. Cancer Res. 2009;69:1587-1595
38. Fisch P, Malkovsky M, Kovats S, et al. Recognition by human V gamma 9/V delta 2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science. 1990;250:1269-1273 (Pubitemid 120031842)
39. Li W, Kubo S, Okuda A, et al. Effect of IL-18 on expansion of gammadelta T cells stimulated by zoledronate and IL-2. J Immunother. 2010;33:287-296
40. Teague RM, Sather BD, Sacks JA, et al. Interleukin-15 rescues tolerant CD8+ T cells for use in adoptive immunotherapy of established tumors. Nat Med. 2006;12:335-341 (Pubitemid 43355083)
41. Gedye C, Quirk J, Browning J, et al. Cancer/testis antigens can be immunological targets in clonogenic CD133+ melanoma cells. Cancer Immunol Immunother. 2009;58:1635-1646
42. Todaro M, D'Asaro M, Caccamo N, et al. Efficient killing of human colon cancer stem cells by gammadelta T lymphocytes. J Immunol. 2009;182:7287-7296
43. Gertner-Dardenne J, Bonnafous C, Bezombes C, et al. Bromohydrin pyrophosphate enhances antibody-dependent cell-mediated cytotoxicity induced by therapeutic antibodies. Blood. 2009;113:4875-4884
44. Gomes AQ, Correia DV, Grosso AR, et al. Identification of a panel of ten cell surface protein antigens associated with immunotargeting of leukemias and lymphomas by peripheral blood gammadelta T cells. Haematologica. 2010;95:1397-1404
45. D'Asaro M, La Mendola C, Di Liberto D, et al. Vgamma9Vdelta2 T lymphocytes efficiently recognize and kill zoledronate-sensitized, imatinib-sensitive, and imatinib-resistant chronic myelogenous leukemia cells. J Immunol. 2010;184: 3260-3268
46. Rauch F, Glorieux FH. Osteogenesis imperfecta. Lancet. 2004;363:1377-1385 (Pubitemid 38529880)
47. Morimoto A, Shioda Y, Imamura T, et al. Nationwide survey of bisphosphonate therapy for children with reactivated Langerhans cell histiocytosis in Japan. Pediatr Blood Cancer. 2011;56:110-115
48. August KJ, Dalton A, Katzenstein HM, et al. The use of zoledronic acid in pediatric cancer patients. Pediatr Blood Cancer. 2011;56:610-614
49. Kato Y, Tanaka Y, Tanaka H, et al. Requirement of speciesspecific interactions for the activation of human gamma delta T cells by pamidronate. J Immunol. 2003;170:3608-3613 (Pubitemid 36359229)
50. Kato Y, Tanaka Y, Hayashi M, et al. Involvement of CD166 in the activation of human gamma delta T cells by tumor cells sensitized with nonpeptide antigens. J Immunol. 2006;177:877-884 (Pubitemid 44036588)
51. Lodolce JP, Boone DL, Chai S, et al. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity. 1998;9:669-676 (Pubitemid 28557595)
52. Caccamo N, Meraviglia S, Ferlazzo V, et al. Differential requirements for antigen or homeostatic cytokines for proliferation and differentiation of human Vgamma9Vdelta2 naive, memory and effector T cell subsets. Eur J Immunol. 2005;35:1764-1772. (Pubitemid 40862324)