TGF-β induces apoptosis in human B cells by transcriptional regulation of BIK and BCL-XL

Cell Death and Differentiation

Volumn 16, Issue 4, 2009, Pages 593-602

  Spender, L C ^a   O'Brien, D I ^a   Simpson, D ^b   Dutt, D ^a   Gregory, C D ^c   Allday, M J ^d   Clark, L J ^e   Inman, G J ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b STOBHILL HOSPITAL   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e SOUTHERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BCL 2 INTERACTING KILLER PROTEIN; BINDING PROTEIN; PROTEIN BCL XL; SHORT HAIRPIN RNA; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; B LYMPHOCYTE; CONSENSUS SEQUENCE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; B-LYMPHOCYTES; BCL-X PROTEIN; CELL LINE, TUMOR; CELLS, CULTURED; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 62849101540     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2008.183     Document Type: Article

References (40)

1. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003; 113: 685-700.
2. Schuster N, Krieglstein K. Mechanisms of TGF-beta-mediated apoptosis. Cell Tissue Res 2002; 307: 1-14.
3. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA. Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 2006; 24: 99-146.
4. Dong M, Blobe GC. Role of transforming growth factor-beta in hematologic malignancies. Blood 2006; 107: 4589-4596.
5. Inman GJ, Allday MJ. Resistance to TGF-beta1 correlates with a reduction of TGF-beta type II receptor expression in Burkitt's lymphoma and Epstein-Barr virus-transformed B lymphoblastoid cell lines. J Gen Virol 2000; 81: 1567-1578.
6. Allen CD, Okada T, Cyster JG. Germinal-center organization and cellular dynamics. Immunity 2007; 27: 190-202.
7. Takahashi Y, Ohta H, Takemori T. Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 2001; 14: 181-192.
8. van Eijk M, Defrance T, Hennino A, de Groot C. Death-receptor contribution to the germinal-center reaction. Trends Immunol 2001; 22: 677-682.
9. Mizuno T, Zhong X, Rothstein TL. Fas-induced apoptosis in B cells. Apoptosis 2003; 8: 451-460.
10. Opferman JT. Apoptosis in the development of the immune system. Cell Death Differ 2008; 15: 234-242.
11. Adams JM, Cory S. Bcl-2-regulated apoptosis: Mechanism and therapeutic potential. Curr Opin Immunol 2007; 19: 488-496.
12. George NM, Evans JJ, Luo X. A three-helix homo-oligomerization domain containing BH3 and BH1 is responsible for the apoptotic activity of Bax. Genes Dev 2007; 21: 1937-1948.
13. Inman GJ, Allday MJ. Apoptosis induced by TGF-beta 1 in Burkitt's lymphoma cells is caspase 8 dependent but is death receptor independent. J Immunol 2000; 165: 2500-2510.
14. Schrantz N, Bourgeade MF, Mouhamad S, Leca G, Sharma S, Vazquez A. p38-mediated regulation of an Fas-associated death domain protein-independent pathway leading to caspase-8 activation during TGFbeta-induced apoptosis in human Burkitt lymphoma B cells BL41. Mol Biol Cell 2001; 12: 3139-3151.
15. Doucet JP, Hussain A, Al-Rasheed M, Gaidano G, Gutierrez MI, Magrath I et al. Differences in the expression of apoptotic proteins in Burkitt's lymphoma cell lines: Potential models for screening apoptosis-inducing agents. Leuk Lymphoma 2004; 45: 357-362.
16. Wildey GM, Patil S, Howe PH. Smad3 potentiates transforming growth factor beta (TGFbeta)-induced apoptosis and expression of the BH3-only protein Bim in WEHI 231 B lymphocytes. J Biol Chem 2003; 278 18069-18077.
17. Ramjaun AR, Tomlinson S, Eddaoudi A, Downward J. Upregulation of two BH3-only proteins, Bmf and Bim, during TGF beta-induced apoptosis. Oncogene 2007; 26: 970-981.
18. Gordon J, Challa A, Levens JM, Gregory CD, Williams JM, Armitage RJ et al. CD40 ligand, Bcl-2, and Bcl-xL spare group I Burkitt lymphoma cells from CD77-directed killing via Verotoxin-1 B chain but fail to protect against the holotoxin. Cell Death Differ 2000; 7: 785-794.
19. Degterev A, Lugovskoy A, Cardone M, Mulley B, Wagner G, Mitchison T et al. Identification of small-molecule inhibitors of interaction between the BH3 domain and Bcl-xL. Nat Cell Biol 2001; 3: 173-182.
20. Habens F, Lapham AS, Dallman CL, Pickering BM, Michels J, Marcusson EG et al. Distinct promoters mediate constitutive and inducible Bcl-XL expression in malignant lymphocytes. Oncogene 2007; 26 1910-1919.
21. Kang JS, Alliston T, Delston R, Derynck R. Repression of Runx2 function by TGF-beta through recruitment of class II histone deacetylases by Smad3. EMBO J 2005; 24: 2543-2555.
22. Yang YC, Piek E, Zavadil J, Liang D, Xie D, Heyer J et al. Hierarchicalmodel of gene regulation by transforming growth factor beta. Proc Natl Acad Sci USA 2003; 100: 10269-10274.
23. Holder MJ, Knox K, Gordon J. Factors modifying survival pathways of germinal center B cells. Glucocorticoids and transforming growth factor-beta, but not cyclosporin A or anti-CD19, block surface immunoglobulin-mediated rescue from apoptosis. Eur J Immunol 1992; 22: 2725-2728.
24. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, Reith AD et al. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 2002; 62: 65-74.
25. Klein U, Tu Y, Stolovitzky GA, Keller JL, Haddad Jr J, Miljkovic V et al. Transcriptional analysis of the B cell germinal center reaction. Proc Natl Acad Sci USA 2003; 100: 2639-2644.
26. Jiang A, Clark EA. Involvement of Bik, a proapoptotic member of the Bcl-2 family, in surface IgM-mediated B cell apoptosis. J Immunol 2001; 166: 6025-6033.
27. Gillissen B, Essmann F, Graupner V, Starck L, Radetzki S, Dorken B et al. Induction of cell death by the BH3-only Bcl-2 homolog Nbk/Bik is mediated by an entirely Bax-dependent mitochondrial pathway. EMBO J 2003; 22: 3580-3590.
28. Shimazu T, Degenhardt K, Nur EKA, Zhang J, Yoshida T, Zhang Y et al NBK/BIK antagonizes MCL-1 and BCL-XL and activates BAK-mediated apoptosis in response to protein synthesis inhibition. Genes Dev 2007; 21: 929-941.
29. Takahashi Y, Cerasoli DM, Dal Porto JM, Shimoda M, Freund R, Fang W et al. Relaxed negative selection in germinal centers and impaired affinity maturation in bcl-xL transgenic mice. J Exp Med 1999; 190: 399-410.
30. Mathai JP, Germain M, Marcellus RC, Shore GC. Induction and endoplasmic reticulum location of BIK/NBK in response to apoptotic signaling by E1A and p53. Oncogene 2002; 21: 2534-2544.
31. Subramanian T, Vijayalingam S, Lomonosova E, Zhao LJ, Chinnadurai G. Evidence for involvement of BH3-only proapoptotic members in adenovirus-induced apoptosis. J Virol 2007; 81: 10486-10495.
32. Real PJ, Sanz C, Gutierrez O, Pipaon C, Zubiaga AM, Fernandez-Luna JL. Transcriptional activation of the proapoptotic bik gene by E2F proteins in cancer cells. FEBS Lett 2006; 580: 5905-5909.
33. Amanna IJ, Dingwall JP, Hayes CE. Enforced bcl-xL gene expression restored splenic B lymphocyte development in BAFF-R mutant mice. J Immunol 2003; 170: 4593-4600.
34. Coultas L, Bouillet P, Stanley EG, Brodnicki TC, Adams JM, Strasser A. Proapoptotic BH3-only Bcl-2 family member Bik/Blk/Nbk is expressed in hemopoietic and endothelial cells but is redundant for their programmed death. Mol Cell Biol 2004; 24: 1570-1581.
35. Wang Z, Spittau B, Behrendt M, Peters B, Krieglstein K. Human TIEG2/ KLF11 induces oligodendroglial cell death by downregulation of Bcl-X(L) expression. J Neural Transm 2007; 114: 867-875.
36. Hennino A, Berard M, Krammer PH, Defrance T. FLICE-inhibitory protein is a key regulator of germinal center B cell apoptosis. J Exp Med 2001; 193: 447-458.
37. Arena V, Martini M, Luongo M, Capelli A, Larocca LM. Mutations of the BIK gene in human peripheral B-cell lymphomas. Genes Chromosomes Cancer 2003; 38: 91-96.
38. Spender LC, Whiteman HJ, Karstegl CE, Farrell PJ. Transcriptional cross-regulation of RUNX1 by RUNX3 in human B cells. Oncogene 2005; 24: 1873-1881.
39. Dickins RA, Hemann MT, Zilfou JT, Simpson DR, Ibarra I, Hannon GJ et al. Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat Genet 2005; 37: 1289-1295.
40. Inman GJ, Nicolás FJ, Hill CS. Nucleocytoplasmic shuttling of Smads 2, 3 and 4 permits sensing of TGF-b receptor activity. Mol Cell 2002; 10: 283-294.