PAX5 activates the transcription of the human telomerase reverse transcriptase gene in B cells

Journal of Pathology

Volumn 220, Issue 1, 2010, Pages 87-96

  Bougel, St́ephanie ^a   Renaud, St́ephanie ^b   Braunschweig, Richard ^a   Loukinov, Dmitri ^b   Morse III, Herbert C ^b   Bosman, Fred T ^a   Lobanenkov, Victor ^b   Benhattar, Jean ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

B cells; Chromatin immunoprecipitation; CTCF; DNA methylation; hTERT; PAX5; Telomerase

Indexed keywords

SMALL INTERFERING RNA; TELOMERASE REVERSE TRANSCRIPTASE; THYMOCYTE ANTIBODY; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR PAX5;

ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; BINDING SITE; CELL LINE; CELL SPECIFICITY; CONTROLLED STUDY; DNA FLANKING REGION; FIBROBLAST; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPH NODE; LYMPHOID CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN METHYLATION; T CELL LYMPHOMA; TRANSCRIPTION INITIATION;

B-CELL-SPECIFIC ACTIVATOR PROTEIN; B-LYMPHOCYTES; BASE SEQUENCE; BINDING SITES; BINDING, COMPETITIVE; CPG ISLANDS; DNA METHYLATION; DNA, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHOMA; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, NEOPLASM; RNA, SMALL INTERFERING; TELOMERASE; TRANSCRIPTIONAL ACTIVATION; TUMOR CELLS, CULTURED;

EID: 73649094144     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2620     Document Type: Article

References (47)

1. Meeker AK, Coffey DS. Telomerase: a promising marker of biological immortality of germ, stem, and cancer cells. A review. Biochemistry (Mosc) 1997;62:1323-1331.
2. Meyerson M, Counter CM, Eaton EN, Ellisen LW, Steiner P, Caddle SD, et al. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 1997;90:785-795.
3. Nakamura TM, Morin GB, Chapman KB, Weinrich SL, Andrews WH, Lingner J, et al. Telomerase catalytic subunit homologs from fission yeast and human. Science 1997;277:955-959.
4. Goueli BS, Janknecht R. Regulation of telomerase reverse transcriptase gene activity by upstream stimulatory factor. Oncogene 2003;22:8042-8047.
5. Poole JC, Andrews LG, Tollefsbol TO. Activity, function, and gene regulation of the catalytic subunit of telomerase (hTERT). Gene 2001;269:1-12.
6. Renaud S, Loukinov D, Bosman FT, Lobanenkov V, Benhattar J. CTCF binds the proximal exonic region of hTERT and inhibits its transcription. Nucleic Acids Res 2005;33:6850-6860.
7. Dessain SK, Yu HY, Reddel RR, Beijersbergen RL, Weinberg RA. Methylation of the human telomerase gene CpG island. Cancer Res 2000;60:537- 541.
8. Devereux TR, Horikawa I, Anna CH, Annab LA, Afshari CA, Barrett JC. DNA methylation analysis of the promoter region of the human telomerase reverse transcriptase (hTERT) gene. Cancer Res 1999;59:6087-6090.
9. Guilleret I, Yan P, Grange F, Braunschweig R, Bosman FT, Benhattar J. Hypermethylation of the human telomerase catalytic subunit (hTERT) gene correlates with telomerase activity. Int J Cancer 2002;101:335- 341.
10. Nomoto K, Maekawa M, Sugano K, Ushiama M, Fukayama N, Fujita S, et al. Methylation status and expression of human telomerase reverse transcriptase mRNA in relation to hypermethylation of the p16 gene in colorectal cancers as analyzed by bisulfite PCR-SSCP. Jpn J Clin Oncol 2002;32:3-8.
11. Renaud S, Loukinov D, Abdullaev Z, Guilleret I, Bosman FT, Lobanenkov V, et al. Dual role of DNA methylation inside and outside of CTCF-binding regions in the transcriptional regulation of the telomerase hTERT gene. Nucleic Acids Res 2007;35:1245-1256.
12. Zinn RL, Pruitt K, Eguchi S, Baylin SB, Herman JG. hTERT is expressed in cancer cell lines despite promoter DNA methylation by preservation of unmethylated DNA and active chromatin around the transcription start site. Cancer Res 2007;67:194-201.
13. Widschwendter A, Muller HM, Hubalek MM, Wiedemair A, Fiegl H, Goebel G, et al. Methylation status and expression of human telomerase reverse transcriptase in ovarian and cervical cancer. Gynecol Oncol 2004;93:407-416.
14. Bechter OE, Eisterer W, Dlaska M, Kuhr T, Thaler J. CpG island methylation of the hTERT promoter is associated with lower telomerase activity in B-cell lymphocytic leukemia. Exp Hematol 2002;30:26-33.
15. Martens UM, Brass V, Sedlacek L, Pantic M, Exner C, Guo Y, et al. Telomere maintenance in human B lymphocytes. Br J Haematol 2002;119:810-818.
16. Weng NP, Granger L, Hodes RJ. Telomere lengthening and telomerase activation during human B cell differentiation. Proc Natl Acad Sci USA 1997;94:10827-10832.
17. Hu BT, Lee SC, Marin E, Ryan DH, Insel RA. Telomerase is upregulated in human germinal center B cells in vivo and can be re-expressed in memory B cells activated in vitro. J Immunol 1997;159:1068-1071.
18. Underhill DA. Genetic and biochemical diversity in the Pax gene family. Biochem Cell Biol 2000;78:629-638.
19. Busslinger M, Klix N, Pfeffer P, Graninger PG, Kozmik Z. Deregulation of PAX-5 by translocation of the Emu enhancer of the IgH locus adjacent to two alternative PAX-5 promoters in a diffuse large-cell lymphoma. Proc Natl Acad Sci USA 1996;93:6129-6134.
20. Dorfler P, Busslinger M. C-terminal activating and inhibitory domains determine the transactivation potential of BSAP (Pax-5 ), Pax-2 and Pax-8 . EMBO J 1996;15:1971-1982.
21. Nutt SL, Morrison AM, Dorfler P, Rolink A, Busslinger M. Identification of BSAP (Pax-5 ) target genes in early B-cell development by loss- and gain-of-function experiments. EMBO J 1998;17:2319-2333.
22. Muratovska A, Zhou C, He S, Goodyer P, Eccles MR. Paired-box genes are frequently expressed in cancer and often required for cancer cell survival. Oncogene 2003;22:7989-7997.
23. Robson EJ, He SJ, Eccles MR. A PANorama of PAX genes in cancer and development. Nat Rev Cancer 2006;6:52-62.
24. Chen YJ, Campbell HG, Wiles AK, Eccles MR, Reddel RR, Braithwaite AW, et al. PAX8 regulates telomerase reverse transcriptase and telomerase RNA component in glioma. Cancer Res 2008;68:5724-5732.
25. Barberis A, Widenhorn K, Vitelli L, Busslinger M. A novel B-cell lineage-specific transcription factor present at early but not late stages of differentiation. Genes Dev 1990;4:849-859.
26. Nutt SL, Urbanek P, Rolink A, Busslinger M. Essential functions of Pax5 (BSAP) in pro-B cell development: difference between fetal and adult B lymphopoiesis and reduced V-to-DJ recombination at the IgH locus. Genes Dev 1997;11:476-491.
27. Mhawech-Fauceglia P, Saxena R, Zhang SZ, Terracciano L, Sauter G, Chadhuri A, et al. Pax-5 immunoexpression in various types of benign and malignant tumours: a high-throughput tissue microarray analysis. J Clin Pathol 2007;60:709-714.
28. Torlakovic E, Torlakovic G, Nguyen PL, Brunning RD, Delabie J. The value of anti-pax-5 immunostaining in routinely fixed and paraffin-embedded sections: a novel pan pre-B and B-cell marker. Am J Surg Pathol 2002;26:1343-1350.
29. Fitzsimmons D, Hodsdon W, Wheat W, Maira SM, Wasylyk B, Hagman J. Pax-5 (BSAP) recruits Ets proto-oncogene family proteins to form functional ternary complexes on a B-cell-specific promoter. Genes Dev 1996;10:2198- 2211.
30. Nutt SL, Urbanek P, Rolink A, Busslinger M. Essential functions of Pax5 (BSAP) in pro-B cell development: difference between fetal and adult B lymphopoiesis and reduced V-to-DJ recombination at the IgH locus. Genes Dev 1997;11:476-491.
31. Kozmik Z, Wang S, Dorfler P, Adams B, Busslinger M. The promoter of the Cd19 gene is a target for the B-cell-specific transcription factor BSAP. Mol Cell Biol 1992;12:2662-2672.
32. Schebesta M, Pfeffer PL, Busslinger M. Control of pre-BCR signaling by Pax5-dependent activation of the BLNK gene. Immunity 2002;17:473-485.
33. Fuxa M, Skok J, Souabni A, Salvagiotto G, Roldan E, Busslinger M. Pax5 induces V-to-DJ rearrangements and locus contraction of the immunoglobulin heavy-chain gene. Genes Dev 2004;18:411-422.
34. Guillou L, Coindre JM, Gallagher G, Terrier P, Gebhard S, Somerhausen ND, et al. Detection of the synovial sarcoma translocation t(X; 18) (SYT; SSX) in paraffin-embedded tissues using reverse transcriptase-polymerase chain reaction. A reliable and powerful diagnostic tool for pathologists - a molecular analysis of 221 mesenchymal tumors fixed in different fixatives. Hum Pathol 2001;32:105-112.
35. Clement G, Benhattar J. A methylation sensitive dot blot assay (MS-DBA) for the quantitative analysis of DNA methylation in clinical samples. J Clin Pathol 2005;58:155-158.
36. Bian YS, Yan P, Osterheld MC, Fontolliet C, Benhattar J. Promoter methylation analysis on micro-dissected paraffin-embedded tissues using bisulfite treatment and PCR-SSCP. Biotechniques 2001;30:66-72.
37. Bianco T, Hussey D, Dobrovic A. Methylation-sensitive, singlestrand conformation analysis (MS-SSCA): a rapid method to screen for and analyze methylation. Hum Mutat 1999;14:289-293.
38. Pugacheva EM, Tiwari VK, Abdullaev Z, Vostrov AA, Flanagan PT, Quitschke WW, et al. Familial cases of point mutations in the XIST promoter reveal a correlation between CTCF binding and pre-emptive choices of X chromosome inactivation. Hum Mol Genet 2005;14:953-965.
39. Renaud S, Pugacheva EM, Delgado MD, Braunschweig R, Abdullaev Z, Loukinov D, et al. Expression of the CTCF-paralogous cancer-testis gene, brother of the regulator of imprinted sites (BORIS), is regulated by three alternative promoters modulated by CpG methylation and by CTCF and p53 transcription factors. Nucleic Acids Res 2007;35:7372-7388.
40. Nutt SL, Morrison AM, Dorfler P, Rolink A, Busslinger M. Identification of BSAP (Pax-5 ) target genes in early B-cell development by loss- and gain-of-function experiments. EMBO J 1998;17:2319-2333.
41. Wheat W, Fitzsimmons D, Lennox H, Krautkramer SR, Gentile LN, McIntosh LP, et al. The highly conserved β-hairpin of the paired DNA-binding domain is required for assembly of Pax-Ets ternary complexes. Mol Cell Biol 1999;19:2231-2241.
42. Jensen KC, Higgins JPT, Montgomery K, Kaygusuz G, van de Rijn M, Natkunam Y. The utility of PAX5 immunohistochemistry in the diagnosis of undifferentiated malignant neoplasms. Mod Pathol 2007;20:871-877.
43. Cozma D, Yu D, Hodawadekar S, Azvolinsky A, Grande S, Tobias JW, et al. B cell activator PAX5 promotes lymphomagenesis through stimulation of B cell receptor signaling. J Clin Invest 2007;117:2602-2610.
44. Schebesta A, McManus S, Salvagiotto G, Delogu A, Busslinger GA, Busslinger M. Transcription factor Pax5 activates the chromatin of key genes involved in B cell signaling, adhesion, migration, and immune function. Immunity 2007;27:49-63.
45. Gregory PD, Wagner K, Horz W. Histone acetylation and chromatin remodeling. Exp Cell Res 2001;265:195-202.
46. Lutz M, Burke LJ, Barreto G, Goeman F, Greb H, Arnold R, et al. Transcriptional repression by the insulator protein CTCF involves histone deacetylases. Nucleic Acids Res 2000;28: 1707-1713.
47. Czerny T, Busslinger M. DNA-binding and transactivation properties of Pax-6: three amino acids in the paired domain are responsible for the different sequence recognition of Pax-6 and BSAP (Pax-5). Mol Cell Biol 1995;15:2858-2871.