Effective activity of cytokine-induced killer cells against autologous metastatic melanoma including cells with stemness features

Clinical Cancer Research

Volumn 19, Issue 16, 2013, Pages 4347-4358

  Gammaitoni, Loretta ^a   Giraudo, Lidia ^a,e   Leuci, Valeria ^d,e   Todorovic, Maja ^a,e   Mesiano, Giulia ^a,e   Picciotto, Franco ^b   Pisacane, Alberto ^c   Zaccagna, Alessandro ^b   Volpe, Maria Giuseppa ^a   Gallo, Susanna ^a,e   Caravelli, Daniela ^a   Giacone, Elena ^b   Venesio, Tiziana ^c   Balsamo, Antonella ^c   Pignochino, Ymera ^d,e   Grignani, Giovanni ^d   Carnevale Schianca, Fabrizio ^a   Aglietta, Massimo ^a,e   Sangiolo, Dario ^a,e  

^a IRCCS   (Italy)

^b IRCCS   (Italy)

^c Unit of Pathology   (Italy)

^d IRCCS   (Italy)

^e UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; LENTIVIRUS VECTOR; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; OCTAMER TRANSCRIPTION FACTOR 4;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER MODEL; CANCER STEM CELL; CARCINOGENESIS; CELL ACTIVITY; CELL EXPANSION; CELL KILLING; CELL STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE INDUCED KILLER CELL; CYTOTOXICITY; FEMALE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE TRANSFER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPHENOTYPING; IN VIVO STUDY; MALE; METASTATIC MELANOMA; MOUSE; NONHUMAN; OCT4 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TARGET CELL; TUMOR CELL CULTURE;

AGED; AGED, 80 AND OVER; CYTOKINE-INDUCED KILLER CELLS; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HUMANS; IMMUNOPHENOTYPING; IMMUNOTHERAPY, ADOPTIVE; MALE; MELANOMA; MIDDLE AGED; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; PHENOTYPE; PRIMARY CELL CULTURE; TUMOR CELLS, CULTURED;

EID: 84883013065     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-0061     Document Type: Article

References (56)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
2. Middleton MR, Grob JJ, Aaronson N, Fierlbeck G, Tilgen W, Seiter S, et al. Randomized phase III study of temozolomide versus dacarbazine in the treatment of patients with advanced metastatic malignant melanoma. J Clin Oncol 2000;18:158-66.
3. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011;364:2507-16.
4. Hauschild A, Grob JJ, Demidov LV, Jouary T, Gutzmer R, Millward M, et al. Dabrafenib in BRAF-mutated metastatic melanoma: a multi-centre, open-label, phase 3 randomised controlled trial. Lancet 2012; 380:358-65.
5. Flaherty KT, Robert C, Hersey P, Nathan P, Garbe C, Milhem M, et al. Improved survival with MEK inhibition in BRAF-mutated melanoma. N Engl J Med 2012;367:107-14.
6. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
7. Wolchok JD, Neyns B, Linette G, Negrier S, Lutzky J, Thomas L, et al. Ipilimumab monotherapy in patients with pretreated advanced melanoma: a randomised, double-blind, multicentre, phase 2, dose-ranging study. Lancet Oncol 2010;11:155-64.
8. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDer-mott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
9. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-11.
10. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011;17:4550-7.
11. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 2011;29:917-24.
12. Rosenberg SA. Cell transfer immunotherapy for metastatic solid cancer-what clinicians need to know. Nat Rev Clin Oncol 2011;8:577-85.
13. Mesiano G, Todorovic M, Gammaitoni L, Leuci V, Giraudo Diego L, Carnevale-Schianca F, et al. Cytokine-induced killer (CIK) cells as feasible and effective adoptive immunotherapy for the treatment of solid tumors. Expert Opin Biol Ther 2012;12:673-84.
14. Hontscha C, Borck Y, Zhou H, Messmer D, Schmidt-Wolf IG. Clinical trials on CIK cells: first report of the international registry on CIK cells (IRCC). J Cancer Res Clin Oncol 2011;137:305-10.
15. Lu PH, Negrin RS. A novel population of expanded human CD3+CD56+ cells derived from T cells with potent in vivo antitumor activity in mice with severe combined immunodeficiency. J Immunol 1994;153:1687-96.
16. Schmidt-Wolf IG, Negrin RS, Kiem HP, Blume KG, Weissman IL. Use of a SCID mouse/human lymphoma model to evaluate cytokine-induced killer cells with potent antitumor cell activity. J Exp Med 1991;174: 139-49.
17. Schmidt-Wolf IG, Lefterova P, Johnston V, Huhn D, Blume KG, Negrin RS. Propagation of large numbers of T cells with natural killer cell markers. Br J Haematol 1994;87:453-8.
18. Baker J, Verneris MR, Ito M, Shizuru JA, Negrin RS. Expansion of cytolytic CD8(+) natural killer T cells with limited capacity for graft-versus-host disease induction due to interferon gamma production. Blood 2001;97:2923-31.
19. Karimi M, Cao TM, Baker JA, Verneris MR, Soares L, Negrin RS. Silencing human NKG2D, DAP10, and DAP12 reduces cytotoxicity of activated CD8+T cells and NK cells. J Immunol 2005;175:7819-28.
20. Verneris MR, Karami M, Baker J, Jayaswal A, Negrin RS. Role of NKG2D signaling in the cytotoxicity of activated and expanded CD8+ T cells. Blood 2004;103:3065-72.
21. Olioso P, Giancola R, Di Riti M, Contento A, Accorsi P, Iacone A. Immunotherapy with cytokine induced killer cells in solid and hema-topoietic tumours: a pilot clinical trial. Hematol Oncol 2009;27: 130-9.
22. Schmidt-Wolf IG, Finke S, Trojaneck B, Denkena A, Lefterova P, Schwella N, et al. Phase I clinical study applying autologous immu-nological effector cells transfected with the interleukin-2 gene in patients with metastatic renal cancer, colorectal cancer and lymphoma. Br J Cancer 1999;81:1009-16.
23. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, Johnson TM, et al. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 2010;18:510-23.
24. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature 2008;456:593-8.
25. Nagata S, Toyoda M, Yamaguchi S, Hirano K, Makino H, Nishino K, et al. Efficient reprogramming of human and mouse primary extra-embryonic cells to pluripotent stem cells. Genes Cells 2009;14: 1395-404.
26. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998;95: 379-91.
27. Cheli Y, Giuliano S, Fenouille N, Allegra M, Hofman V, Hofman P, et al. Hypoxia and MITF control metastatic behaviour in mouse and human melanoma cells. Oncogene 2012;31:2461-70.
28. Kumar SM, Liu S, Lu H, Zhang H, Zhang PJ, Gimotty PA, et al. Acquired cancer stem cell phenotypes through Oct4-mediated dedifferentiation. Oncogene 2012;31:4898-911.
29. Follenzi A, Ailles LE, Bakovic S, Geuna M, Naldini L Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat Genet 2000;25:217-22.
30. Gerrard L, Zhao D, Clark AJ, Cui W. Stably transfected human embryonic stem cell clones express OCT4-specific green fluorescent protein and maintain self-renewal and pluripotency. Stem Cells 2005;23: 124-33.
31. Orfanelli U, Wenke AK, Doglioni C, Russo V, Bosserhoff AK, Lavorgna G. Identification of novel sense and antisense transcription at the TRPM2 locus in cancer. Cell Res 2008;18:1128-40.
32. Fischer K, Andreesen R, Mackensen A. An improved flow cytometric assay for the determination of cytotoxic T lymphocyte activity. J Immunol Methods 2002;259:159-69.
33. Introna M, Borleri G, Conti E, Franceschetti M, Barbui AM, Broady R, et al. Repeated infusions of donor-derived cytokine-induced killer cells in patients relapsing after allogeneic stem cell transplantation: a phase I study. Haematologica 2007;92:952-9.
34. Laport GG, Sheehan K, Baker J, Armstrong R, Wong RM, Lowsky R, et al. Adoptive immunotherapy with cytokine-induced killer cells for patients with relapsed hematologic malignancies after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant 2011;17:1679-87.
35. Wu C, Jiang J, Shi L, Xu N. Prospective study of chemotherapy in combination with cytokine-induced killer cells in patients suffering from advanced non-small cell lung cancer. Anticancer Res 2008;28:3997-4002.
36. Jiang JT, Shen YP, Wu CP, Zhu YB, Wei WX, Chen LJ, et al. Increasing the frequency of CIK cells adoptive immunotherapy may decrease risk of death in gastric cancer patients. World J Gastroenterol 2010;16: 6155-62.
37. Liu L, Zhang W, Qi X, Li H, Yu J, Wei S, et al. Randomized study of autologous cytokine-induced killer cell immunotherapy in metastatic renal carcinoma. Clin Cancer Res 2012;18:1751-9.
38. Vetter CS, Groh V, thor Straten P, Spies T, Brocker EB, Becker JC. Expression of stress-induced MHCclassI related chain molecules on human melanoma. J Invest Dermatol 2002;118:600-5.
39. Vetter CS, Lieb W, Brocker EB, Becker JC. Loss of nonclassical MHC molecules MIC-A/B expression during progression of uveal melanoma. Br J Cancer 2004;91:1495-9.
40. Pich C, Teiti I, Rochaix P, Mariamé B, Couderc B, Favre G, et al. Statins reduce melanoma development and metastasis through MICA over-expression. Front Immunol 2013;4:62.
41. Tang H, Sampath P, Yan X, Thorne SH. Potential for enhanced therapeutic activity of biological cancer therapies with doxycycline combination. Gene Ther 2013;20:770-8.
42. Hervieu A, Rébe C, Vegran F, Chalmin F, Bruchard M, Vabres P, et al. Dacarbazine-mediated upregulation of NKG2D ligands on tumor cells activates NK and CD8 T cells and restrains melanoma growth. J Invest Dermatol 2013;133:499-508.
43. Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 2007;43:935-46.
44. La Porta C. Cancer stem cells: lessons from melanoma. Stem Cell Rev 2009;5:61-5.
45. La Porta CA, Zapperi S. Human breast and melanoma cancer stem cells biomarkers. Cancer Lett. 2012 Mar 20. [Epub ahead of print].
46. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cel biology to cancer. Nat Rev Cancer 2003;3:895-902.
47. Dick JE. Acute myeloid leukemia stem cells. Ann N Y Acad Sci 2005;1044:1-5.
48. La Porta CA, Zapperi S, Sethna JP. Senescent cells in growing tumors: population dynamics and cancer stem cells. PLoS Comput Biol 2012;8:e1002316.
49. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008;8:755-68.
50. Asadi MH, Mowla SJ, Fathi F, Aleyasin A, Asadzadeh J, Atlasi Y. OCT4B1, a novel spliced variant of OCT4, is highly expressed in gastric cancer and acts as an antiapoptotic factor. Int J Cancer 2011;128: 2645-52.
51. Chang CJ, Chien Y, Lu KH, Chang SC, Chou YC, Huang CS, et al. Oct4-related cytokine effects regulate tumorigenic properties of colorectal cancer cells. Biochem Biophys Res Commun 2011;415: 245-51.
52. Chiou SH, Wang ML, Chou YT, Chen CJ, Hong CF, Hsieh WJ, et al. Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiation. Cancer Res 2010;70: 10433-44.
53. Dong Z, Zeng Q, Luo H, Zou J, Cao C, Liang J, et al. Increased expression of OCT4 is associated with low differentiation and tumor recurrence in human hepatocellular carcinoma. Pathol Res Pract 2012;208:527-33.
54. Gu G, Yuan J, Wills M, Kasper S. Prostate cancer cells with stem cell characteristics reconstitute the original human tumor in vivo. Cancer Res 2007;67:4807-15.
55. Wen J, Park JY, Park KH, Chung HW, Bang S, Park SW, et al. Oct4 and Nanog expression is associated with early stages of pancreatic car-cinogenesis. Pancreas 2010;39:622-6.
56. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010;140:62-73.