The immunoglobulin heavy chain gene 3′ enhancers induce Bcl2 deregulation and lymphomagenesis in murine B cells

Leukemia

Volumn 25, Issue 9, 2011, Pages 1484-1493

  Xiang, H ^a,b   Noonan, E J ^a,b   Wang, J ^a,b   Duan, H ^a,b   Ma, L ^a,b   Michie, S ^b   Boxer, L M ^a,b  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

18); BCL2; Igh enhancer; Lymphoma; mouse models; t(14

Indexed keywords

DEOXYRIBONUCLEASE I; MESSENGER RNA; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CARCINOGENESIS; CONTROLLED STUDY; DEREGULATION; EMBRYO; ENHANCER REGION; FOLLICULAR LYMPHOMA; GENE LOCUS; GENE TARGETING; HUMAN; HYPERSENSITIVITY; IMMUNOGLOBULIN HEAVY CHAIN GENE; IN VITRO STUDY; LYMPHOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; WILD TYPE;

3' UNTRANSLATED REGIONS; ANIMALS; B-LYMPHOCYTES; BLOTTING, SOUTHERN; BLOTTING, WESTERN; CELL CYCLE; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; ENHANCER ELEMENTS, GENETIC; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENES, IMMUNOGLOBULIN HEAVY CHAIN; HUMANS; LYMPHOMA, B-CELL; MALE; MICE; MICE, TRANSGENIC; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS;

EID: 80052436837     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2011.115     Document Type: Article

References (40)

1. Yunis JJ, Oken MM, Kaplan ME, Ensrud KM, Howe RR, Theologides A. Distinctive chromosomal abnormalities in histologic subtypes of non-Hodgkin's lymphomas. N Engl J Med 1982; 307: 1231.
2. Cleary ML, Smith SD, Sklar J. Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/imunoglobulin transcript resulting from the t(14;18) translocation. Cell 1986; 47: 19-28. (Pubitemid 17181529)
3. Graninger WB, Seto M, Boutain B, Goldman P, Korsmeyer SJ. Expression of bcl-2 and bcl-2-Ig fusion transcripts in normal and neoplastic cells. J Clin Invest 1987; 80: 1512-1515. (Pubitemid 18027800)
4. Tsujimoto Y, Croce C. Analysis of the structure, transcripts, and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc Natl Acad Sci 1986; 83: 5214-5218. (Pubitemid 16051345)
5. Seto M, Jaeger U, Hockett RD, Graninger W, Bennett S, Goldman P et al. Alternative promoters and exons, somatic mutation and deregulation of the Bcl-2-Ig fusion gene in lymphoma. EMBO J 1988; 7: 123-131.
6. Katsumata M, Siegel RM, Louie DC, Miyashita T, Tsujimoto Y, Nowell PC et al. Differential effects of Bcl-2 on T and B cells in transgenic mice. Proc Natl Acad Sci USA 1992; 89: 11376-11380.
7. McDonnell TJ, Deane N, Platt FM, Nunez G, Jaeger U, McKearn JP et al. Bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell 1989; 57: 79-88. (Pubitemid 19098870)
8. Strasser A, Whittingham S, Vaux DL, Bath ML, Adams JM, Cory S et al. Enforced bcl-2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci USA 1991; 88: 8661-8665. (Pubitemid 21915417)
9. McDonnell TJ, Korsmeyer SJ. Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14;18). Nature 1991; 349: 254-256. (Pubitemid 21912060)
10. Strasser A, Harris AW, Bath ML, Cory S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 1990; 348: 331-333. (Pubitemid 120029100)
11. Strasser A, Harris AW, Cory S. Em-bcl-2 transgene facilitates spontaneous transformation of early pre-B and immunoglobulinsecreting cells but not T cells. Oncogene 1993; 8: 1-9. (Pubitemid 23047224)
12. Egle A, Harris AW, Bath ML, Reilly L, Cory S. VavP-Bcl2 transgenic mice develop follicular lymphoma preceded by germinal center hyperplasia. Blood 2004; 103: 2276-2283. (Pubitemid 38326247)
13. Ogilvy S, Metcalf D, Print CG, Bath ML, Harris AW, Adams JM. Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc Natl Acad Sci USA 1999; 96: 14943-14948. (Pubitemid 30019744)
14. Fiancette R, Amin R, Truffinet V, Vincent-Fabert C, Cogne N, Cogne M et al. A myeloma translocation-like model associating CCND1 with the immunoglobulin heavy-chain locus 30 enhancers does not promote by itself B-cell malignancies. Leuk Res 2010; 34: 1043-1051.
15. Truffinet V, Pinaud E, Cogne N, Petit B, Guglielmi L, Cogne M et al. The 30 IgH locus control region is sufficient to deregulate a c-myc transgene and promote mature B cell malignancies with a predominant Burkitt-like phenotype. J Immunol 2007; 179: 6033-6042.
16. Wu Y, Mehew JW, Heckman CA, Arcinas M, Boxer LM. Negative regulation of bcl-2 expression by p53 in hematopoietic cells. Oncogene 2001; 20: 240-251. (Pubitemid 32150269)
17. Dariavach F, Williams GT, Campbell K, Pettersson S, Neuberger MS. The mouse IgH 30 enhancer. Eur J Immunol 1991; 21: 1499-1504.
18. Madisen L, Groudine M. Identification of a locus control region in the immunoglobulin heavy-chain locus that deregulates c-myc expression in plasmacytoma and Burkitt0s lymphoma cells. Gene Devel 1994; 8: 2212-2226.
19. Pettersson S, Cook GP, Bruggemann M, Williams GT, Neuberger MS. A second B cell-specific enhancer 30 of the immunoglobulin heavy chain locus. Nature 1990; 344: 165-168.
20. Duan H, Heckman CA, Boxer LM. The immunoglobulin heavychain gene 30 enhancers deregulate bcl-2 promoter usage in t(14;18) lymphoma cells. Oncogene 2007; 26: 2635-2641. (Pubitemid 46632009)
21. Lewandoski M, Meyers EN, Martin GR. Analysis of Fgf8 gene function in vertebrate development. Cold Spring Harbor Symp Quant Biol 1997; 62: 159-168. (Pubitemid 28198533)
22. Hoyer KK, French SW, Turner DE, Nguyen MT, Renard M, Malone CS et al. Dysregulated TCL1 promotes multiple classes of mature B cell lymphoma. Proc Natl Acad Sci USA 2002; 99: 14392-14397. (Pubitemid 35257682)
23. Kawamoto H, Ikawa T, Ohmura K, Fujimoto S, Katsura Y. T cell progenitors emerge earlier than B cell progenitors in the murine fetal liver. Immunity 2000; 12: 441-450.
24. Chang Y, Paige CJ, Wu GE. Enumeration and characterization of DJH structures in mouse fetal liver. EMBO J 1992; 11: 1891-1899.
25. Wang Z, Raifu M, Howard M, Smith L, Hansen D, Goldsby R et al. Universal PCR amplification of mouse immunoglobulin gene variable regions: the design of degenerate primers and an assessment of the effect of DNA polymerase 30 to 50 exonuclease activity. J Immunol Methods 2000; 233: 167-177. (Pubitemid 30058245)
26. Lefranc MP, Giudicelli V, Kaas Q, Duprat E, Jabado-Michaloud J, Scaviner D et al. IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res 2005; 33 (Database issue): D593-D597. (Pubitemid 40207943)
27. Dekker J, Rippe K, Dekker M, Kleckner N. Capturing chromosome conformation. Science 2002; 295: 1306-1311. (Pubitemid 34157624)
28. Hagege H, Klous P, Braem C, Splinter E, Dekker J, Cathala G et al. Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2007; 2: 1722-1733.
29. Zhou G-L, Xin L, Song W, Di L-J, Liu G, Wu X-S et al. Active chromatin hub of the mouse a-globin locus forms in a transcription factory of clustered housekeeping genes. Mol Cell Biol 2006; 26: 5096-5105. (Pubitemid 43955822)
30. Kienle D, Krober A, Katzenberger T, Ott G, Leupolt E, Barth TF et al. VH mutation status and VDJ rearrangement structure in mantle cell lymphoma: correlation with genomic aberrations, clinical characteristics, and outcome. Blood 2003; 102: 3003-3009. (Pubitemid 37248876)
31. Tracey L, Aggarwal M, Garcia-Cosio M, Villuendas R, Algara P, Sanchez-Beato M et al. Somatic hypermutation signature in B-cell low-grade lymphomas. Haematologica 2008; 93: 1186-1194.
32. Heckman CA, Cao T, Somsouk L, Duan H, Mehew JW, Zhang C et al. Critical elements of the immunoglobulin heavy chain gene enhancers for deregulated expression of bcl-2. Cancer Res 2003; 63: 6666-6673. (Pubitemid 37322945)
33. Greider C, Chattopadhyay A, Parkhurst C, Yang E. BCL-xL and BCL2 delay Myc-induced cell cycle entry through elevation of p27 and inhibition of G1 cyclin-dependent kinases. Oncogene 2002; 21: 7765-7775. (Pubitemid 35398834)
34. Janumyan YM, Sansam CG, Chattopadhyay A, Cheng N, Soucie EL, Penn LZ et al. Bcl-xL/Bcl-2 coordinately regulates apoptosis, cell cycle arrest and cell cycle entry. EMBO J 2003; 22: 5459-5470. (Pubitemid 37279955)
35. Reilly LA, Huang DCS, Strasser A. The cell death inhibitor Bcl-2 and its homologues influence control of cell cycle entry. EMBO J 1996; 15: 6979-6990. (Pubitemid 27023269)
36. Dave SS, Wright G, Tan B, Rosenwald A, Gascoyne RD, Chan WC et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Eng J Med 2004; 351: 2159-2169. (Pubitemid 39507628)
37. de Jong D, Koster A, Hagenbeek A, Raemaekers J, Veldhuizen D, Heisterkamp S et al. Impact of the tumor microenvironment on prognosis in follicular lymphoma is dependent on specific treatment protocols. Haematologica 2009; 94: 70-77.
38. Petrasch S, Kosco M, Perez-Alvarez C, Schmitz J, Brittinger G. Proliferation of non-Hodgkin-lymphoma lymphocytes in vitro is dependent upon follicular dendritic cell interactions. Br J Haematol 1992; 80: 21-26.
39. Wahlin BE, Sander B, Christensson B, Kimby E. CD8+ T-cell content in diagnostic lymph nodes measured by flow cytometry is a predictor of survival in follicular lymphoma. Clin Cancer Res 2007; 13 (2 Part 1): 388-397. (Pubitemid 46225341)
40. Duan H, Xiang H, Ma L, Boxer LM. Functional long-range interactions of the IgH 30 enhancers with the bcl-2 promoter region in t(14;18) lymphoma cells. Oncogene 2008; 27: 6720-6728.