Adult T-cell leukemia cells are characterized by abnormalities of helios expression that promote T cell growth

Cancer Science

Volumn 104, Issue 8, 2013, Pages 1097-1106

  Asanuma, Satomi ^a   Yamagishi, Makoto ^a   Kawanami, Katsuaki ^a   Nakano, Kazumi ^a   Sato Otsubo, Aiko ^b   Muto, Satsuki ^b   Sanada, Masashi ^b   Yamochi, Tadanori ^a   Kobayashi, Seiichiro ^a   Utsunomiya, Atae ^c   Iwanaga, Masako ^d   Yamaguchi, Kazunari ^e   Uchimaru, Kaoru ^a   Ogawa, Seishi ^b   Watanabe, Toshiki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c IMAMURA BUN IN HOSPITAL   (Japan)

^d TEIKYO UNIVERSITY   (Japan)

^e NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AIOLOS PROTEIN; HELIOS PROTEIN; IKAROS TRANSCRIPTION FACTOR; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CANCER PATIENT; CANCER TISSUE; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCUS; GENE LOSS; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; HUMAN TISSUE; LEUKEMIA CELL; LEUKEMOGENESIS; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; RNA SPLICING; T CELL LEUKEMIA; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VIRUS CARRIER;

EID: 84881118695     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12181     Document Type: Article

References (45)

1. Yamaguchi K, Watanabe T. Human T lymphotropic virus type-I and adult T-cell leukemia in Japan. Int J Hematol 2002; 76: 240-45.
2. Iwanaga M, Watanabe T, Utsunomiya A et al. Human T-cell leukemia virus type I (HTLV-1) proviral load and disease progression in asymptomatic HTLV-1 carriers: a nationwide prospective study in Japan. Blood 2010; 116: 1211-19.
3. Yamagishi M, Nakano K, Miyake A et al. Polycomb-mediated loss of miR-31 activates NIK-dependent NF-κB pathway in adult T cell leukemia and other cancers. Cancer Cell 2012; 21: 121-35.
4. Yamagishi M, Watanabe T. Molecular hallmarks of adult T cell leukemia. Front Microbiol 2012; 3: 334.
5. Lo K, Landau NR, Smale ST. LyF-1, a transcriptional regulator that interacts with a novel class of promoters for lymphocyte-specific genes. Mol Cell Biol 1991; 11: 5229-43.
6. Georgopoulos K, Moore DD, Derfler B. Ikaros, an early lymphoid-specifictranscription factor and a putative mediator for T cell commitment. Science 1992; 258: 808-12.
7. Hahm K, Ernst P, Lo K, Kim GS, Turck C, Smale ST. The lymphoid transcription factor LyF-1 is encoded by specific, alternatively spliced mRNAs derived from the Ikaros gene. Mol Cell Biol 1994; 14: 7111-23.
8. Sun L, Liu A. Zinc finger-mediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development. EMBO J 1996; 15: 5358-69.
9. Morgan B, Sun L, Avitahl N et al. Aiolos, a lymphoid restricted transcription factor that interacts with Ikaros to regulate lymphocyte differentiation. EMBO J 1997; 16: 2004-13.
10. Kelley CM, Ikeda T, Koipally J et al. Helios, a novel dimerization partner of Ikaros expressed in the earliest hematopoietic progenitors. Curr Biol 1998; 8: 508-15.
11. Cobb BS, McCarty AS, Brown KE et al. Helios, a T cell-restricted Ikaros family member that quantitatively associates with Ikaros at centromeric heterochromatin. Genes Dev 1998; 12: 782-96.
12. Winandy S, Wu P, Georgopoulos K. A dominant mutation in the Ikaros gene leads to rapid development of leukemia and lymphoma. Cell 1995; 83: 289-99.
13. Wang JH, Nichogiannopoulou A, Wu L et al. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity 1996; 5: 537-49.
14. Wang JH, Avitahl N, Cariappa A et al. Aiolos regulates B cell activation and maturation to effector state. Immunity 1998; 9: 543-53.
15. Zhang Z, Swindle CS, Bates JT, Ko R, Cotta CV, Klug CA. Expression of a non-DNA-binding isoform of Helios induces T-cell lymphoma in mice. Blood 2007; 109: 2190-7.
16. Sun L, Crotty ML, Sensel M et al. Expression of dominant-negative Ikaros isoforms in T-cell acute lymphoblastic leukemia. Clin Cancer Res 1999; 5: 2112-20.
17. Nakase K, Ishimaru F, Avitahl N et al. Dominant negative isoform of the Ikaros gene in patients with adult B-cell acute lymphoblastic leukemia. Cancer Res 2000; 60: 062-4065.
18. Takanashi M, Yagi T, Imamura T et al. Expression of the Ikaros gene family in childhood acute lymphoblastic leukaemia. Br J Haematol 2002; 117: 525-30.
19. Nishii K, Katayama N, Miwa H. Non-DNA-binding Ikaros isoform gene expressed in adult B-precursor acute lymphoblastic leukemia. Leukemia 2002; 16: 1285-92.
20. Tonnelle C, Imbert M-C, Sainty D, Granjeaud S, N'Guyen C, Chabannon C. Overexpression of dominant-negative Ikaros 6 protein is restricted to a subset of B common adult acute lymphoblastic leukemias that express high levels of the CD34 antigen. Hematol J 2003; 4: 104-9.
21. Klein F, Feldhahn N, Herzog S et al. BCR-ABL1 induces aberrant splicing of IKAROS and lineage infidelity in pre-B lymphoblastic leukemia cells. Oncogene 2006; 25: 1118-24.
22. Zhou F, Mei H, Jin R, Li X, Chen X. Expression of ikaros isoform 6 in chinese children with acute lymphoblastic leukemia. J Pediatr Hematol Oncol 2011; 33: 429-32.
23. Mullighan CG, Miller CB, Radtke I et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature 2008; 453: 110-14.
24. Kano G, Morimoto A, Takanashi M et al. Ikaros dominant negative isoform (Ik6) induces IL-3-independent survival of murine pro-B lymphocytes by activating JAK-STAT and up-regulating Bcl-xl levels. Leuk Lymphoma 2008; 49: 965-73.
25. Iacobucci I, Lonetti A, Messa F et al. Expression of spliced oncogenic Ikaros isoforms in Philadelphia-positive acute lymphoblastic leukemia patients treated with tyrosine kinase inhibitors: implications for a new mechanism of resistance. Blood 2008; 112: 3847-55.
26. Mullighan CG, Su X, Zhang J et al. Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N Engl J Med 2009; 360: 470-80.
27. Kuiper RP, Waanders E, van der Velden VHJ et al. IKZF1 deletions predict relapse in uniformly treated pediatric precursor B-ALL. Leukemia 2010; 24: 1258-64.
28. Nakase K, Ishimaru F, Fujii K et al. Overexpression of novel short isoforms of Helios in a patient with T-cell acute lymphoblastic leukemia. Exp Hematol 2002; 30: 313-17.
29. Fujii K, Ishimaru F, Tabayashi T et al. Over-expression of short isoforms of Helios in patients with adult T-cell leukaemia/lymphoma. Br J Haematol 2003; 120: 986-9.
30. Fujiwara SI, Yamashita Y, Nakamura N et al. High-resolution analysis of chromosome copy number alterations in angioimmunoblastic T-cell lymphoma and peripheral T-cell lymphoma, unspecified, with single nucleotide polymorphism-typing microarrays. Leukemia 2008; 22: 1891-8.
31. Fujimoto R, Ozawa T, Itoyama T, Sadamori N, Kurosawa N, Isobe M. HELIOS-BCL11B fusion gene involvement in a t(2;14)(q34;q32) in an adult T-cell leukemia patient. Cancer Genet 2012; 205: 356-64.
32. Shimoyama M. Diagnostic criteria and classification of clinical subtypes of adult T-cell leukaemia-lymphoma. A report from the Lymphoma Study Group (1984-87). Br J Haematol 1991; 79: 428-37.
33. Tabayashi T, Ishimaru F, Takata M et al. Characterization of the short isoform of Helios overexpressed in patients with T-cell malignancies. Cancer Sci 2007; 98: 182-8.
34. Kathrein KL, Chari S, Winandy S. Ikaros directly represses the notch target gene Hes1 in a leukemia T cell line: implications for CD4 regulation. J Biol Chem 2008; 283: 10476-84.
35. Kleinmann E, Geimer Le Lay AS, Sellars M, Kastner P, Chan S. Ikaros represses the transcriptional response to Notch signaling in T-cell development. Mol Cell Biol 2008; 28: 7465-75.
36. Molnár A, Georgopoulos K. The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol Cell Biol 1994; 14: 8292-303.
37. Schaefer CF, Anthony K, Krupa S et al. PID: the pathway interaction database. Nucleic Acids Res 2009; 37: D674-9.
38. Pancewicz J, Taylor JM, Datta A. Notch signaling contributes to proliferation and tumor formation of human T-cell leukemia virus type 1-associated adult T-cell leukemia. Proc Natl Acad Sci USA 2010; 107: 16619-24.
39. Murata K, Hattori M, Hirai N et al. Hes1 directly controls cell proliferation through the transcriptional repression of p27Kip1. Mol Cell Biol 2005; 25: 4262-71.
40. Maeda Y, Seki N, Sato N, Sugahara K, Chiba K. Sphingosine 1-phosphate receptor type 1 regulates egress of mature T cells from mouse bone marrow. Int Immunol 2010; 22: 515-25.
41. Spiegel S, Milstien S. The outs and the ins of sphingosine-1-phosphate in immunity. Nat Rev Immunol 2011; 11: 403-15.
42. Maceyka M, Harikumar KB, Milstien S, Spiegel S. Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol 2012; 22: 50-60.
43. Ghigna C, Valacca C, Biamonti G. Alternative splicing and tumor progression. Curr Genomics 2008; 9: 556-70.
44. David CJ, Manley JL. Alternative pre-mRNA splicing regulation in cancer: pathways and programs unhinged. Genes Dev 2010; 24: 2343-64.
45. Blair CA, Zi X. Potential molecular targeting of splice variants for cancer treatment. Indian J Exp Biol 2011; 49: 836-9.