Lentiviral-mediated Foxp3 RNAi suppresses tumor growth of regulatory T cell-like leukemia in a murine tumor model

Gene Therapy

Volumn 17, Issue 8, 2010, Pages 972-979

  Tsai, B Y ^a   Suen, J L ^b   Chiang, B L ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Foxp3; lentivirus; leukemia; RL 1; RNAi

Indexed keywords

LENTIVIRUS VECTOR; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; LEUKEMIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATORY T LYMPHOCYTE; RNA INTERFERENCE; RNA SEQUENCE;

ANIMALS; CELL LINE, TUMOR; FORKHEAD TRANSCRIPTION FACTORS; GENE THERAPY; LENTIVIRUS; LEUKEMIA, EXPERIMENTAL; LEUKEMIA, T-CELL; MALE; MICE; MICE, INBRED BALB C; RNA INTERFERENCE; RNA STABILITY;

ANIMALIA; LENTIVIRUS; MURINAE; MUS;

EID: 77955665641     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2010.38     Document Type: Article

References (46)

1. Kersey JH. Fifty years of studies of the biology and therapy of childhood leukemia. Blood 1997; 90: 4243-4251.
2. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
3. Hahn WC, Weinberg RA. Rules for making human tumor cells. N Engl J Med 2002; 347: 1593-1603.
4. Smith SD, Uyeki EM, Lowman JT. Colony formation in vitro by leukemic cells in acute lymphoblastic leukemia (ALL). Blood 1978; 52: 712-718.
5. Smith SD, Shatsky M, Cohen PS, Warnke R, Link MP, Glader BE. Monoclonal antibody and enzymatic profiles of human malignant T-lymphoid cells and derived cell lines. Cancer Res 1984; 44 (12 Pt 1): 5657-5660.
6. Lange B, Valtieri M, Santoli D, Caracciolo D, Mavilio F, Gemperlein I et al. Growth factor requirements of childhood acute leukemia: establishment of GM-CSF-dependent cell lines. Blood 1987; 70: 192-199.
7. Gjerset R, Yu A, Haas M. Establishment of continuous cultures of T-cell acute lymphoblastic leukemia cells at diagnosis. Cancer Res 1990; 50: 10-14.
8. Dialynas DP, Lee MJ, Gold DP, Shao Le, Yu AL, Borowitz MJ et al. Pre-conditioning with fetal cord blood facilitates engraft-ment of primary childhood T-cell acute lymphoblastic leukemia in immuno-deficient mice. Blood 2001; 97: 3218-3225.
9. Burnet FM. The concept of immunologic surveillance. Prog Exp Tumor Res 1970; 13: 1-27.
10. Smyth MJ, Dunn GP, Schreiber RD. Cancer immuno-surveillance and immuno-editing: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv Immunol 2006; 90: 1-50.
11. Bui JD, Schreiber RD. Cancer immuno-surveillance, immuno-editing and inflammation: independent or interdependent processes? Curr Opin Immunol 2007; 19: 203-208.
12. Sakaguchi S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005; 6: 345-352.
13. Wang X, Zheng J, Liu J, Yao J, He Y, Li X et al. Increased population of CD4(+)CD25(high), regulatory T cells with their higher apoptotic and proliferating status in peripheral blood of acute myeloid leukemia patients. Eur J Haematol 2005; 75: 468-476.
14. Nelson BH. IL-2, regulatory T cells, and tolerance. J Immunol 2004; 172: 3983-3988.
15. Prevosto C, Zancolli M, Canevali P, Zocchi MR, Poggi A. Generation of CD4+ or CD8+ regulatory T cells upon mesen-chymal stem cell-lymphocyte interaction. Haematologica 2007; 92: 881-888.
16. Fontenot JD, Rudensky AY. A well-adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 2005; 6: 331-337.
17. Hill JA, Feuerer M, Tash K, Haxhinasto S, Perez J, Melamed R et al. Foxp3 transcription-factor-dependent and-independent regulation of the regulatory T cell transcriptional signature. Immunity 2007; 27: 786-800.
18. Nik Tavakoli N, Hambly BD, Sullivan DR, Bao S. Forkhead box protein 3: essential immune regulatory role. Int J Biochem Cell Biol 2008; 40: 2369-2373.
19. Liyanage UK, Moore TT, Joo HG, Tanaka Y, Herrmann V, Doherty G et al. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 2002; 169: 2756-2761.
20. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004; 10: 942-949.
21. Hiraoka N, Onozato K, Kosuge T, Hirohashi S. Prevalence of FOXP3+ regulatory T cells increases during the progression of pancreatic ductal adenocarcinoma and its pre-malignant lesions. Clin Cancer Res 2006; 12: 5423-5434.
22. Grauer OM, Nierkens S, Bennink E, Toonen LW, Boon L, Wesseling P et al. CD4+FoxP3+ regulatory T cells gradually accumulate in gliomas during tumor growth and efficiently suppress antiglioma immune responses in vivo. Int J Cancer 2007; 121: 95-105.
23. Hinz S, Pagerols-Raluy L, Oberg HH, Ammerpohl O, Grüssel S, Sipos B et al. Foxp3 expression in pancreatic carcinoma cells as a novel mechanism of immune evasion in cancer. Cancer Res 2007; 67: 8344-8350.
24. Roncador G, Garcia JF, Garcia JF, Maestre L, Lucas E, Menarguez J et al. FOXP3, a selective marker for a subset of adult T-cell leukemia/lymphoma. Leukemia 2005; 19: 2247-2253.
25. Chen S, Ishii N, Ine S, Ikeda S, Fujimura T, Ndhlovu LC et al. Regulatory T cell-like activity of Foxp3+ adult T cell leukemia cells. Int Immunol 2006; 18: 269-277.
26. Yano H, Ishida T, Inagaki A, Ishii T, Kusumoto S, Komatsu H et al. Regulatory T-cell function of adult T-cell leukemia/lymphoma cells. Int J Cancer 2007; 120: 2052-2057.
27. Ono M, Yaguchi H, Ohkura N, Kitabayashi I, Nagamura Y, Nomura T et al. Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 2007; 446: 685-689.
28. Pandiyan P, Zheng L, Ishihara S, Reed J, Lenardo MJ. CD4(+)CD25(+) Foxp3(+) regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4(+) T cells. Nat Immunol 2007; 8: 1353-1362.
29. Nair S, Boczkowski D, Fassnacht M, Pisetsky D, Gilboa E. Vaccination against the forkhead family transcription factor Foxp3 enhances tumor immunity. Cancer Res 2007; 67: 371-380.
30. Sato H, Boyse EA, Aoki T, Iritani C, Old LJ. Leukemia-associated transplantation antigens related to murine leukemia virus. The X.1 system: immune response controlled by a locus linked to H-2. J Exp Med 1973; 138: 593-606.
31. Iwakuma T, Cui Y, Chang LJ. Self-inactivating lentiviral vectors with U3 and U5 modifications. Virology 1999; 261: 120-132.
32. Roush W. Anti-sense aims for a renaissance. Science 1997; 276: 1192-1193.
33. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 2001; 27: 68-73.
34. Berger CL, Tigelaar R, Cohen J, Mariwalla K, Trinh J, Wang N et al. Cutaneous T-cell lymphoma: malignant proliferation of T-regulatory cells. Blood 2005; 105: 1640-1647.
35. Wu Y, Borde M, Heissmeyer V, Feuerer M, Lapan AD, Stroud JC et al. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 2006; 126: 375-387.
36. Zheng Y, Josefowicz SZ, Kas A, Chu TT, Gavin MA, Rudensky AY et al. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 2007; 445: 936-940.
37. Pandiyan P, Zheng L, Ishihara S, Reed J, Lenardo MJ. CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells. Nat Immunol 2007; 8: 1353-1362.
38. Alisky JM, Davidson BL. Towards therapy using RNA interference. Am J Pharmacogenomics 2004; 4: 45-51.
39. Abbas-Terki T, Blanco-Bose W, Deglon N, Pralong W, Aebischer P. Lentiviral-mediated RNA interference. Hum Gene Ther 2002; 13: 2197-2201.
40. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 2003; 33: 401-406.
41. Heller LC, Ingram SF, Lucas ML, Gilbert RA, Heller R. Effect of electrically mediated intratumor and intramuscular delivery of a plasmid encoding IFN alpha on visible B16 mouse melanomas. Technol Cancer Res Treat 2002; 1: 205-209.
42. Tomar RS, Matta H, Chaudhary PM. Use of adeno-associated viral vector for delivery of small interfering RNA. Oncogene 2003; 22: 5712-5715.
43. Maynard CL, Harrington LE, Janowski KM, Oliver JR, Zindl CL, Rudensky AY et al. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3-precursor cells in the absence of interleukin 10. Nat Immunol 2007; 8: 931-941.
44. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M et al. Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 2003; 21: 635-637.
45. Persengiev SP, Zhu X, Green MR. Non-specific, concentration-dependent stimulation and repression of mammalian gene expression by small interfering RNAs (siRNAs). RNA 2004; 10: 12-18.
46. Tomayko MM, Reynolds CP. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 1989; 24: 148-154.