Therapeutic targeting of the BCL6 oncogene for diffuse large B-cell lymphomas

References

• Melnick A, Licht J D. Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood 1999; 93: 3167–3215
   PubMed Web of Science ®Google Scholar
• Dent A L, Shaffer A L, Yu X, Allman D, Staudt L M. Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 1997; 276: 589–592
   PubMed Web of Science ®Google Scholar
• Ye B H, Cattoretti G, Shen Q, Zhang J, Hawe N, de Waard R, et al. The BCL-6 proto-oncogene controls germinal-centre formation and Th2-type inflammation. Nat Genet 1997; 16: 161–170
   PubMed Web of Science ®Google Scholar
• Tunyaplin C, Shaffer A L, Angelin-Duclos C D, Yu X, Staudt L M, Calame K L. Direct repression of prdm1 by Bcl-6 inhibits plasmacytic differentiation. J Immunol 2004; 173: 1158–1165
   PubMed Web of Science ®Google Scholar
• Kuo T C, Shaffer A L, Haddad J, Choi Y S, Jr, Staudt L M, Calame K. Repression of BCL-6 is required for the formation of human memory B cells in vitro. J Exp Med 2007; 204: 819–830
   PubMed Web of Science ®Google Scholar
• Shaffer A L, Yu X, He Y, Boldrick J, Chan E P, Staudt L M. BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity 2000; 13: 199–212
   PubMed Web of Science ®Google Scholar
• Reljic R, Wagner S D, Peakman L J, Fearon D T. Suppression of signal transducer and activator of transcription 3-dependent B lymphocyte terminal differentiation by BCL-6. J Exp Med 2000; 192: 1841–1848
   PubMed Web of Science ®Google Scholar
• Allen C D, Okada T, Cyster J G. Germinal-center organization and cellular dynamics. Immunity 2007; 27: 190–202
   PubMed Web of Science ®Google Scholar
• Okazaki I M, Kotani A, Honjo T. Role of AID in tumourigenesis. Adv Immunol 2007; 94: 245–273
   PubMedGoogle Scholar
• Pasqualucci L, Neumeister P, Goossens T, Nanjangud G, Chaganti R S, Kuppers R, et al. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 2001; 412: 341–346
   PubMed Web of Science ®Google Scholar
• Spencer J O, Dunn-Walters D K. Somatic hypermutation and B-cell malignancies. J Pathol 1999; 187: 158–163
   PubMed Web of Science ®Google Scholar
• Pasqualucci L, Bereschenko O, Niu H, Klein U, Basso K, Guglielmino R, et al. Molecular pathogenesis of non-Hodgkin's lymphoma: the role of Bcl-6. Leuk Lymphoma 2003; 44(Suppl 3)S5–S12
   PubMed Web of Science ®Google Scholar
• Cattoretti G, Pasqualucci L, Ballon G, Tam W, Nandula S V, Shen Q, et al. Deregulated BCL6 expression recapitulates the pathogenesis of human diffuse large B cell lymphomas in mice. Cancer Cell 2005; 7: 445–455
   PubMed Web of Science ®Google Scholar
• Baron B W, Anastasi J, Montag A, Huo D, Baron R M, Karrison T, et al. The human BCL6 transgene promotes the development of lymphomas in the mouse. Proc Natl Acad Sci USA 2004; 101: 14198–14203
   PubMed Web of Science ®Google Scholar
• Polo J M, Juszczynski P, Monti S, Cerchietti L, Ye K, Greally J M, et al. Transcriptional signature with differential expression of BCL6 target genes accurately identifies BCL6-dependent diffuse large B cell lymphomas. Proc Natl Acad Sci USA 2007; 104: 3207–3212
   PubMed Web of Science ®Google Scholar
• Ranuncolo S M, Polo J M, Dierov J, Singer M, Kuo T, Greally J, et al. Bcl-6 mediates the germinal center B cell phenotype and lymphomagenesis through transcriptional repression of the DNA-damage sensor ATR. Nat Immunol 2007; 8: 705–714
   PubMedGoogle Scholar
• Phan R T, Dalla-Favera R. The BCL6 proto-oncogene suppresses p53 expression in germinal-centre B cells. Nature 2004; 432: 635–639
   PubMed Web of Science ®Google Scholar
• Phan R T, Saito M, Basso K, Niu H, Dalla-Favera R. BCL6 interacts with the transcription factor Miz-1 to suppress the cyclin-dependent kinase inhibitor p21 and cell cycle arrest in germinal center B cells. Nat Immunol 2005; 6: 1054–1060
   PubMed Web of Science ®Google Scholar
• Wright J A, Keegan K S, Herendeen D R, Bentley N J, Carr A M, Hoekstra M F, et al. Protein kinase mutants of human ATR increase sensitivity to UV and ionizing radiation and abrogate cell cycle checkpoint control. Proc Natl Acad Sci USA 1998; 95: 7445–7450
   PubMed Web of Science ®Google Scholar
• Cuadrado M, Martinez-Pastor B, Murga M, Toledo L I, Gutierrez-Martinez P, Lopez E, et al. ATM regulates ATR chromatin loading in response to DNA double-strand breaks. J Exp Med 2006; 203: 297–303
   PubMed Web of Science ®Google Scholar
• Petermann E, Caldecott K W. Evidence that the ATR/Chk1 pathway maintains normal replication fork progression during unperturbed S phase. Cell Cycle 2006; 5: 2203–2209
   PubMed Web of Science ®Google Scholar
• Ward I M, Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 2001; 276: 47759–47762
   PubMed Web of Science ®Google Scholar
• Liu Q, Guntuku S, Cui X S, Matsuoka S, Cortez D, Tamai K, et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev 2000; 14: 1448–1459
   PubMed Web of Science ®Google Scholar
• Mailand N, Falck J, Lukas C, Syljuasen R G, Welcker M, Bartek J, et al. Rapid destruction of human Cdc25A in response to DNA damage. Science 2000; 288: 1425–1429
   PubMed Web of Science ®Google Scholar
• Shieh S Y, Ahn J, Tamai K, Taya Y, Prives C. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev 2000; 14: 289–300
   PubMed Web of Science ®Google Scholar
• Sanchez Y, Wong C, Thoma R S, Richman R, Wu Z, Piwnica-Worms H, et al. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 1997; 277: 1497–1501
   PubMed Web of Science ®Google Scholar
• Tibbetts R S, Brumbaugh K M, Williams J M, Sarkaria J N, Cliby W A, Shieh S Y, et al. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev 1999; 13: 152–157
   PubMed Web of Science ®Google Scholar
• Phan R T, Saito M, Kitagawa Y, Means A R, Dalla-Favera R. Genotoxic stress regulates expression of the proto-oncogene Bcl6 in germinal center B cells. Nat Immunol 2007; 8: 1132–1139
   PubMedGoogle Scholar
• Parekh S, Polo J M, Shaknovich R, Juszczynski P, Lev P, Ranuncolo S M, et al. BCL6 programs lymphoma cells for survival and differentiation through distinct biochemical mechanisms. Blood 2007; 110: 2067–2074
   PubMed Web of Science ®Google Scholar
• Vasanwala F H, Kusam S, Toney L M, Dent A L. Repression of AP-1 function: a mechanism for the regulation of Blimp-1 expression and B lymphocyte differentiation by the B cell lymphoma-6 protooncogene. J Immunol 2002; 169: 1922–1929
   PubMed Web of Science ®Google Scholar
• Shaffer A L, Lin K I, Kuo T C, Yu X, Hurt E M, Rosenwald A, et al. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 2002; 17: 51–62
   PubMed Web of Science ®Google Scholar
• Allen C D, Okada T, Tang H L, Cyster J G. Imaging of germinal center selection events during affinity maturation. Science 2007; 315: 528–531
   PubMed Web of Science ®Google Scholar
• Saito M, Gao J, Basso K, Kitagawa Y, Smith P M, Bhagat G, et al. A signalling pathway mediating downregulation of BCL6 in germinal center B cells is blocked by BCL6 gene alterations in B cell lymphoma. Cancer Cell 2007; 12: 280–292
   PubMed Web of Science ®Google Scholar
• Walker S R, Nelson E A, Frank D A. STAT5 represses BCL6 expression by binding to a regulatory region frequently mutated in lymphomas. Oncogene 2007; 26: 224–233
   PubMed Web of Science ®Google Scholar
• Chang C C, Ye B H, Chaganti R S, Dalla-Favera R. BCL-6, a POZ/zinc-finger protein, is a sequence-specific transcriptional repressor. Proc Natl Acad Sci USA 1996; 93: 6947–6952
   PubMed Web of Science ®Google Scholar
• Ahmad K F, Melnick A, Lax S, Bouchard D, Liu J, Kiang C L, et al. Mechanism of SMRT corepressor recruitment by the BCL6 BTB domain. Mol Cell 2003; 12: 1551–1564
   PubMed Web of Science ®Google Scholar
• Huynh K D, Bardwell V J. The BCL-6 POZ domain and other POZ domains interact with the co-repressors N-CoR and SMRT. Oncogene 1998; 17: 2473–2484
   PubMed Web of Science ®Google Scholar
• Huynh K D, Fischle W, Verdin E, Bardwell V J. BCoR, a novel corepressor involved in BCL-6 repression. Genes Dev 2000; 14: 1810–1823
   PubMed Web of Science ®Google Scholar
• Stogios P J, Chen L, Prive G G. Crystal structure of the BTB domain from the LRF/ZBTB7 transcriptional regulator. Protein Sci 2007; 16: 336–342
   PubMed Web of Science ®Google Scholar
• Prive G G, Melnick A. Specific peptides for the therapeutic targeting of oncogenes. Curr Opin Genet Dev 2006; 16: 71–77
   PubMed Web of Science ®Google Scholar
• Polo J M, Dell'Oso T, Ranuncolo S M, Cerchietti L, Beck D, Da Silva G F, et al. Specific peptide interference reveals BCL6 transcriptional and oncogenic mechanisms in B-cell lymphoma cells. Nat Med 2004; 10: 1329–1335
   PubMed Web of Science ®Google Scholar
• Cerchietti L, Polo J, DaSilva G, Dowdy S, Cattoretti G, Shaknovich R, et al. BCL6, p53 and Molecular Targeted Therapy in B-Cell Lymphomas. Blood 2005; 106(427a)
   Google Scholar
• Stogios P J, Downs G S, Jauhal J J, Nandra S K, Prive G G. Sequence and structural analysis of BTB domain proteins. Genome Biol 2005; 6: R82
   PubMed Web of Science ®Google Scholar
• Ahmad K F, Engel C K, Prive G G. Crystal structure of the BTB domain from PLZF. Proc Natl Acad Sci USA 1998; 95: 12123–12128
   PubMed Web of Science ®Google Scholar
• Melnick A, Carlile G, Ahmad K F, Kiang C L, Corcoran C, Bardwell V, et al. Critical residues within the BTB domain of PLZF and Bcl-6 modulate interaction with corepressors. Mol Cell Biol 2002; 22: 1804–1818
   PubMed Web of Science ®Google Scholar
• Chattopadhyay A, Tate S A, Beswick R W, Wagner S D, Ko Ferrigno P. A peptide aptamer to antagonize BCL-6 function. Oncogene 2006; 25: 2223–2233
   PubMed Web of Science ®Google Scholar
• Fujita N, Jaye D L, Geigerman C, Akyildiz A, Mooney M R, Boss J M, et al. MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 2004; 119: 75–86
   PubMedGoogle Scholar
• Chevallier N, Corcoran C M, Lennon C, Hyjek E, Chadburn A, Bardwell V J, et al. ETO protein of t(8;21) AML is a corepressor for Bcl-6 B-cell lymphoma oncoprotein. Blood 2004; 103: 1454–1463
   PubMed Web of Science ®Google Scholar
• Miles R R, Crockett D K, Lim M S, Elenitoba-Johnson K S. Analysis of BCL6-interacting proteins by tandem mass spectrometry. Mol Cell Proteomics 2005; 4: 1898–1909
   PubMed Web of Science ®Google Scholar
• Bereshchenko O R, Gu W, Dalla-Favera R. Acetylation inactivates the transcriptional repressor BCL6. Nat Genet 2002; 32: 606–613
   PubMed Web of Science ®Google Scholar
• Li J, Wang J, Nawaz Z, Liu J M, Qin J, Wong J. Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3. Embo J 2000; 19: 4342–4350
   PubMed Web of Science ®Google Scholar
• Sakajiri S, Kumagai T, Kawamata N, Saitoh T, Said J W, Koeffler H P. Histone deacetylase inhibitors profoundly decrease proliferation of human lymphoid cancer cell lines. Exp Hematol 2005; 33: 53–61
   PubMed Web of Science ®Google Scholar
• Heltweg B, Gatbonton T, Schuler A D, Posakony J, Li H, Goehle S, et al. Antitumour activity of a small-molecule inhibitor of human silent information regulator 2 enzymes. Cancer Res 2006; 66: 4368–4377
   PubMed Web of Science ®Google Scholar
• Kalota A, Opalinska J B. Design of antisense oligonucleotides and short interfering RNA duplexes (siRNA) targeted to BCL6 mRNA: towards rational drug development for specific lymphoma subsets. Blood Cells Mol Dis 2007; 38: 199–203
   PubMed Web of Science ®Google Scholar
• Saito Y, Liang G, Egger G, Friedman J M, Chuang J C, Coetzee G A, et al. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 2006; 9: 435–443
   PubMed Web of Science ®Google Scholar
• Alizadeh A A, Eisen M B, Davis R E, Ma C, Lossos I S, Rosenwald A, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000; 403: 503–511
   PubMed Web of Science ®Google Scholar
• Monti S, Savage K J, Kutok J L, Feuerhake F, Kurtin P, Mihm M, 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
   PubMed Web of Science ®Google Scholar
• Faber A C, Chiles T C. Resveratrol induces apoptosis in transformed follicular lymphoma OCI-LY8 cells: evidence for a novel mechanism involving inhibition of BCL6 signalling. Int J Oncol 2006; 29: 1561–1566
   PubMed Web of Science ®Google Scholar
• Jazirehi A R, Bonavida B. Resveratrol modifies the expression of apoptotic regulatory proteins and sensitizes non-Hodgkin's lymphoma and multiple myeloma cell lines to paclitaxel-induced apoptosis. Mol Cancer Ther 2004; 3: 71–84
   PubMed Web of Science ®Google Scholar