Dysregulated TCL1 requires the germinal center and genome instability for mature B-cell transformation

Blood

Volumn 108, Issue 6, 2006, Pages 1991-1998

  Shen, Rhine R ^b   Ferguson, David O ^b   Renard, Mathilde ^b   Hoyer, Katrina K ^b   Kim, Unkyu ^b   Hao, Xingpei ^b   Alt, Frederick W ^b   Roeder, Robert G ^b   Morse III, Herbert C ^b   Teitell, Michael A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD40 ANTIGEN; FAS ANTIGEN; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR; ONCOPROTEIN; PROTEIN; PROTEIN AICDA; PROTO ONCOGENE PROTEIN TCL1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CARCINOGENESIS; CELL MATURATION; CELL STIMULATION; CELL SURVIVAL; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; GENOMIC INSTABILITY; GERMINAL CENTER; LYMPHOCYTE TRANSFORMATION; MALE; MALIGNANT TRANSFORMATION; MITOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTO ONCOGENE; REGULATORY MECHANISM; SPECTRAL KARYOTYPING; TRANSGENE; TRISOMY; TRISOMY 15; WILD TYPE;

EID: 33748696775     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-02-001354     Document Type: Article

References (66)

1. Jaffe ES, Harris NL, Stein H, Vardiman JW. Pathology and genetics of tumours of haematopoietic and lymphoid tissues. In: Kleihues P and Sobin LH, eds. World Health Organization Classification of Tumours. Lyon, France: IARC Press; 2001:119-185.
2. Dalla-Favera R, Bregni M, Erikson J, Patterson D, Gallo RC, Croce CM. Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci U S A. 1982;79:7824-7827.
3. Bakhshi A, Jensen JP, Goldman P, et al. Cloning the chromosomal breakpoint of t(14;18) human lymphomas: clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell. 1985;41:899-906.
4. Chen W, Iida S, Louie DC, Dalla-Favera R, Chaganti RS. Heterologous promoters fused to BCL6 by chromosomal translocations affecting band 3q27 cause its deregulated expression during B-cell differentiation. Blood. 1998;91:603-607.
5. Rabbitts TH, Forster A, Hamlyn P, Baer R. Effect of somatic mutation within translocated c-myc genes in Burkitt's lymphoma. Nature. 1984;309:592-597.
6. Cesarman E, Dalla-Favera R, Bentley D, Groudine M. Mutations in the first exon are associated with altered transcription of c-myc in Burkitt lymphoma. Science. 1987;238:1272-1275.
7. Teitell MA. The TCL1 family of oncoproteins: coactivators of transformation. Nat Rev Cancer. 2005;5:640-648.
8. Laine J, Kunstle G, Obata T, Sha M, Noguchi M. The protooncogene TCL1 is an Akt kinase coactivator. Mol Cell. 2000;6:395-407.
9. Pekarsky Y, Koval A, Hallas C, et al. Tcl1 enhances Akt kinase activity and mediates its nuclear translocation. Proc Natl Acad Sci U S A. 2000;97:3028-3033.
10. French SW, Shen RR, Koh PJ, Malone CS, Mallick P, Teitell MA. A modeled hydrophobic domain on the TCL1 oncoprotein mediates association with AKT at the cytoplasmic membrane. Biochemistry. 2002;41:6376-6382.
11. Auguin D, Barthe P, Royer C, et al. Structural basis for the co-activation of protein kinase B by T-cell leukemia-1 (TCL1) family proto-oncoproteins. J Biol Chem. 2004;279:35890-35902.
12. Hoyer KK, French SW, Turner DE, et al. Dysregulated TCL1 promotes multiple classes of mature B cell lymphoma. Proc Natl Acad Sci U S A. 2002; 99:14392-14397.
13. Hoyer KK, Herling M, Bagrintseva K, et al. T cell leukemia-1 modulates TCR signal strength and IFN-{gamma} levels through phosphatidylinositol 3-kinase and protein kinase C pathway activation. J Immunol. 2005;175:864-873.
14. Virgilio L, Narducci MG, Isobe M, et al. Identification of the TCL1 gene involved in T-cell malignancies. Proc Natl Acad Sci U S A. 1994;91:12530-12534.
15. Pekarsky Y, Hallas C, Croce CM. The role of TCL1 in human T-cell leukemia. Oncogene. 2001;20:5638-5643.
16. Virgilio L, Lazzeri C, Bichi R, et al. Deregulated expression of TCL1 causes T cell leukemia in mice. Proc Natl Acad Sci U S A. 1998;95:3885-3889.
17. Said JW, Hoyer KK, French SW, et al. TCL1 oncogene expression in B cell subsets from lymphoid hyperplasia and distinct classes of B cell lymphoma. Lab Invest. 2001;81:555-564.
18. Teitell M, Damore MA, Sulur GG, et al. TCL1 oncogene expression in AIDS-related lymphomas and lymphoid tissues. Proc Natl Acad Sci U S A. 1999;96:9809-9814.
19. Narducci MG, Pescarmona E, Lazzeri C, et al. Regulation of TCL1 expression in B- and T-cell lymphomas and reactive lymphoid tissues. Cancer Res. 2000;60:2095-2100.
20. Maljaei SH, Brito-Babapulle V, Hiorns LR, Catovsky D. Abnormalities of chromosomes 8, 11, 14, and X in T-prolymphocytic leukemia studied by fluorescence in situ hybridization. Cancer Genet Cytogenet. 1998;103:110-116.
21. Soulier J, Pierron G, Vecchione D, et al. A complex pattern of recurrent chromosomal losses and gains in T-cell prolymphocytic leukemia. Genes Chromosomes Cancer. 2001;31:248-254.
22. Teitell MA, Lones MA, Perkins SL, Sanger WG, Cairo MS, Said JW. TCL1 expression and Epstein-Barr virus status in pediatric Burkitt lymphoma. Am J Clin Pathol. 2005;124:569-575.
23. Kim U, Qin XF, Gong S, et al. The B-cell-specific transcription coactivator OCA-B/OBF-1/Bob-1 is essential for normal production of immunoglobulin isotypes. Nature. 1996;383:542-547.
24. Muramatsu M, Sankaranand VS, Anant S, et al. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J Biol Chem. 1999;274:18470-18476.
25. Morse HC 3rd, Anver MR, Fredrickson TN, et al. Bethesda proposals for classification of lymphoid neoplasms in mice. Blood. 2002;100:246-258.
26. Lahvis GP, Cerny J. Induction of germinal center B cell markers in vitro by activated CD4+ T lymphocytes: the role of CD40 ligand, soluble factors, and B cell antigen receptor cross-linking. J Immunol. 1997;159:1783-1793.
27. Mizuno T, Zhong X, Rothstein TL. Fas-induced apoptosis in B cells. Apoptosis. 2003;8:451-460.
28. Rothstein TL. Inducible resistance to Fas-mediated apoptosis in B cells. Cell Res. 2000;10:245-266.
29. Zhang X, Li L, Choe J, et al. Up-regulation of Bcl-xL expression protects CD40-activated human B cells from Fas-mediated apoptosis. Cell Immunol. 1996;173:149-154.
30. Schneider TJ, Grillot D, Foote LC, Nunez GE, Rothstein TL. Bcl-x protects primary B cells against Fas-mediated apoptosis. J Immunol. 1997;159:4834-4839.
31. Wang J, Lobito AA, Shen F, Hornung F, Winoto A, Lenardo MJ. Inhibition of Fas-mediated apoptosis by the B cell antigen receptor through c-FLIP. Eur J Immunol. 2000;30:155-163.
32. Van Parijs L, Refaeli Y, Abbas AK, Baltimore D. Autoimmunity as a consequence of retrovirus-mediated expression of C-FLIP in lymphocytes. Immunity. 1999;11:763-770.
33. Rothstein TL, Wang JK, Panka DJ, et al. Protection against Fas-dependent Th1-mediated apoptosis by antigen receptor engagement in B cells. Nature. 1995;374:163-165.
34. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 2000;102:553-563.
35. Pasqualucci L, Guglielmino R, Houldsworth J, et al. Expression of the AID protein in normal and neoplastic B cells. Blood. 2004;104:3318-3325.
36. Greeve J, Philipsen A, Krause K, et al. Expression of activation-induced cytidine deaminase in human B-cell non-Hodgkin lymphomas. Blood. 2003;101:3574-3580.
37. Smit LA, Bende RJ, Aten J, Guikema JE, Aarts WM, van Noesel CJ. Expression of activation-induced cytidine deaminase is confined to B-cell non-Hodgkin's lymphomas of germinal-center phenotype. Cancer Res. 2003;63:3894-3898.
38. Hardianti MS, Tatsumi E, Syampurnawati M, et al. Activation-induced cytidine deaminase expression in follicular lymphoma: association between AID expression and ongoing mutation in FL. Leukemia. 2004;18:826-831.
39. Pasqualucci L, Neumeister P, Goossens T, et al. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature. 2001;412:341-346.
40. Okazaki IM, Hiai H, Kakazu N, et al. Constitutive expression of AID leads to tumorigenesis. J Exp Med. 2003;197:1173-1181.
41. Rush JS, Liu M, Odegard VH, Unniraman S, Schatz DG. Expression of activation-induced cytidine deaminase is regulated by cell division, providing a mechanistic basis for division-linked class switch recombination. Proc Natl Acad Sci U S A. 2005;102:13242-13247.
42. Dedeoglu F, Horwitz B, Chaudhuri J, Alt FW, Geha RS. Induction of activation-induced cytidine deaminase gene expression by IL-4 and CD40 ligation is dependent on STAT6 and NFkappaB. Int Immunol. 2004;16:395-404.
43. Ramiro AR, Jankovic M, Eisenreich T, et al. AID is required for c-myc/IgH chromosome translocations in vivo. Cell. 2004;118:431-438.
44. Unniraman S, Zhou S, Schatz DG. Identification of an AID-independent pathway for chromosomal translocations between the Igh switch region and Myc. Nat Immunol. 2004;5:1117-1123.
45. Teitell MA. OCA-B regulation of B-cell development and function. Trends Immunol. 2003;24:546-553.
46. Corcoran LM, Hasbold J, Dietrich W, et al. Differential requirement for OBF-1 during antibody-secreting cell differentiation. J Exp Med. 2005;201:1385-1396.
47. Malone CS, Wall R. Bob1 (OCA-B/OBF-1) differential transactivation of the B cell-specific B29 (Ig beta) and mb-1 (Ig alpha) promoters. J Immunol. 2002;168:3369-3375.
48. Hess J, Nielsen PJ, Fischer KD, Bujard H, Wirth T. The B lymphocyte-specific coactivator BOB.1/OBF.1 is required at multiple stages of B-cell development. Mol Cell Biol. 2001;21:1531-1539.
49. Rose ML, Birbeck MS, Wallis VJ, Forrester JA, Davies AJ. Peanut lectin binding properties of germinal centres of mouse lymphoid tissue. Nature. 1980;284:364-366.
50. Bain G, Engel I, Robanus Maandag EC, et al. E2A deficiency leads to abnormalities in alpha-beta T-cell development and to rapid development of T-cell lymphomas. Mol Cell Biol. 1997;17:4782-4791.
51. Gaudet F, Hodgson JG, Eden A, et al. Induction of tumors in mice by genomic hypomethylation. Science. 2003;300:489-492.
52. Klein U, Tu Y, Stolovitzky GA, et al. Transcriptional analysis of the B cell germinal center reaction. Proc Natl Acad Sci U S A. 2003;100:2639-2644.
53. Phan RT, Dalla-Favera R. The BCL6 proto-oncogene suppresses p53 expression in germinal-centre B cells. Nature. 2004;432:635-639.
54. Suzuki A, Kaisho T, Ohishi M, et al. Critical roles of Pten in B cell homeostasis and immunoglobulin class switch recombination. J Exp Med. 2003;197:657-667.
55. Miyauchi H, Minamino T, Tateno K, Kunieda T, Toko H, Komuro I. Akt negatively regulates the in vitro lifespan of human endothelial cells via a p53/p21-dependent pathway. EMBO J. 2004;23:212-220.
56. Mayo LD, Donner DB. The PTEN, Mdm2, p53 tumor suppressor-oncoprotein network. Trends Biochem Sci. 2002;27:462-467.
57. Chen Z, Trotman LC, Shaffer D, et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature. 2005;436:725-730.
58. Yadav A, Olaru A, Saltis M, Setren A, Cerny J, Livak F. Identification of a ubiquitously active promoter of the murine activation-induced cytidine deaminase (AICDA) gene. Mol Immunol. 2006;43:529-541.
59. Egle A, Harris AW, Bath ML, O'Reilly L, Cory S. VavP-Bcl2 transgenic mice develop follicular lymphoma preceded by germinal center hyperplasia. Blood. 2004;103:2276-2283.
60. Samardzic T, Marinkovic D, Nielsen PJ, Nitschke L, Wirth T. BOB.1/OBF.1 deficiency affects marginal-zone B-cell compartment. Mol Cell Biol. 2002;22:8320-8331.
61. Monti S, Savage KJ, Kutok JL, et al. Molecular profiling of diffuse large B-cell lymphoma identifies robust subtypes including one characterized by host inflammatory response. Blood. 2005;105:1851-1861.
62. Chiang YC, Teng SC, Su YN, Hsieh FJ, Wu KJ. c-Myc directly regulates the transcription of the NBS1 gene involved in DNA double-strand break repair. J Biol Chem. 2003;278:19286-19291.
63. Karlsson A, Deb-Basu D, Cherry A, Turner S, Ford J, Felsher DW. Defective double-strand DNA break repair and chromosomal translocations by MYC overexpression. Proc Natl Acad Sci U S A. 2003;100:9974-9979.
64. Neil JC, Cameron ER. Retroviral insertion sites and cancer: fountain of all knowledge? Cancer Cell. 2002;2:253-255.
65. Maljaie SH, Brito-Babapulle V, Matutes E, Hiorns LR, De Schouwer PJ, Catovsky D. Expression of c-myc oncoprotein in chronic T cell leukemias. Leukemia. 1995;9:1694-1699.
66. Ramiro AR, Jankovic M, Callen E, et al. Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature. 2006;440:105-109.