The 3′ IgH locus control region is sufficient to deregulate a c-myc transgene and promote mature B cell malignancies with a predominant burkitt-like phenotype

Journal of Immunology

Volumn 179, Issue 9, 2007, Pages 6033-6042

  Truffinet, Véronique ^a   Pinaud, Eric ^a   Cogné, Nadine ^a   Petit, Barbara ^a,b   Guglielmi, Laurence ^a,c   Cogné, Michel ^a   Denizot, Yves ^a,d  

^a UNIVERSITY OF LIMOGES   (France)

^b LIMOGES UNIVERSITY HOSPITAL   (France)

^c INSERM   (France)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD45 ANTIGEN; IMMUNOGLOBULIN D; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN M; PROTEIN P21; RAS PROTEIN; MYC PROTEIN;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN PRODUCTION; IN VITRO STUDY; IN VIVO STUDY; INCIDENCE; LYMPHOBLASTOMA; MALE; MOUSE; NONHUMAN; ONCOGENE C MYC; PHENOTYPE; PLASMACYTOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; SPLEEN CELL; TRANSGENE; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; BURKITT LYMPHOMA; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; PATHOLOGY; SECRETION; SURVIVAL RATE;

ANIMALS; B-LYMPHOCYTES; BURKITT LYMPHOMA; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; IMMUNOGLOBULIN HEAVY CHAINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-MYC; SURVIVAL RATE; TRANSCRIPTION, GENETIC; TRANSGENES;

EID: 38449097468     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.9.6033     Document Type: Article

References (36)

1. Pelengaris, S., M. Khan, and G. Evan. 2002. c-Myc: more than just a matter of life and death. Nat. Rev. Cancer 2: 764-776.
2. Blum, K. A., G. Lozanski, and J. C. Byrd. 2004. Adult Burkitt leukemia and lymphoma. Blood 104: 3009-3020.
3. Henderson, A., and K. Calame. 1998. Transcriptional regulation during B cell development. Annu. Rev. Immunol. 16: 163-200.
4. Perlot, T., F. W. Alt, C. H. Bassing, H. Suh, and E. Pinaud. 2005. Elucidation of IgH intronic enhancer functions via germ-line deletion. Proc. Natl. Acad. Sci. USA 102: 14362-14367.
5. Adams, J. M., A. W. Harris, C. A. Pinkert, L. M. Corcoran, W. S. Alexander, S. Cory, R. D. Palmiter, and R. L. Brinster. 1985. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533-538.
6. Butzler, C., X. Zou, A. V. Popov, and M. Bruggemann. 1997. Rapid induction of B-cell lymphomas in mice carrying a human IgH/c-mycYAC. Oncogene 14: 1383-1388.
7. Palomo, C., X. Zou, I. C. Nicholson, C. Butzler, and M. Bruggemann. 1999. B-cell tumorigenesis in mice carrying a yeast artificial chromosome-based immunoglobulin heavy/c-myc translocus is independent of the heavy chain intron enhancer (Emu). Cancer Res. 59: 5625-5628.
8. Chauveau, C., and M. Cogne. 1996. Palindromic structure of the IgH 3′locus control region. Nat. Genet. 14: 15-16.
9. Madisen, L., and M. Groudine. 1994. Identification of a locus control region in the immunoglobulin heavy-chain locus that deregulates c-myc expression in plasmacytoma and Burkitt's lymphoma cells. Genes Dev. 8: 2212-2226.
10. Laurencikiene, J., V. Tamosiunas, and E. Severinson. 2007. Regulation of ε germline transcription and switch region mutations by IgH locus 3′ enhancers in transgenic mice. Blood 109: 159-167.
11. Morvan, C. L., E. Pinaud, C. Decourt, A. Cuvillier, and M. Cogne. 2003. The immunoglobulin heavy-chain locus hs3b and hs4 3′ enhancers are dispensable for VDJ assembly and somatic hypermutation. Blood 102: 1421-1427.
12. Pinaud, E., A. A. Khamlichi, C. Le Morvan, M. Drouet, V. Nalesso, M. Le Bert, and M. Cogne. 2001. Localization of the 3′ IgH locus elements that effect long-distance regulation of class switch recombination. Immunity 15: 187-199.
13. Guglielmi, L., M. Le Bert, V. Truffinet, M. Cogne, and Y. Denizot. 2003. Insulators to improve expression of a 3′ IgH LCR-driven reporter gene in transgenic mouse models. Biochem. Biophys. Res. Commun. 307: 466-471.
14. Kovalchuk, A. L., C. F. Qi, T. A. Torrey, L. Taddesse-Heath, L. Feigenbaum, S. S. Park, A. Gerbitz, G. Klobeck, K. Hoertnagel, A. Polack, et al. 2000. Burkitt lymphoma in the mouse. J. Exp. Med. 192: 1183-1190.
15. Park, S. S., J. S. Kim, L. Tessarollo, J. D. Owens, L. Peng, S. S. Han, S. Tae Chung, T. A. Torrey, W. C. Cheung, R. D. Polakiewicz, et al. 2005. Insertion of c-Myc into Igh induces B-cell and plasma-cell neoplasms in mice. Cancer Res. 65: 1306-1315.
16. Park, S. S., A. L. Shaffer, J. S. Kim, W. duBois, M. Potter, L. M. Staudt, and S. Janz. 2005. Insertion of Myc into Igh accelerates peritoneal plasmacytomas in mice. Cancer Res. 65: 7644-7652.
17. Wang, J., and L. M. Boxer. 2005. Regulatory elements in the immunoglobulin heavy chain gene 3′-enhancers induce c-myc deregulation and lymphomagenesis in murine B cells. J. Biol. Chem. 280: 12766-12773.
18. Mautner, J., S. Joos, T. Werner, D. Eick, G. W. Bornkamm, and A. Polack. 1995. Identification of two enhancer elements downstream of the human c-myc gene. Nucleic Acids Res. 23: 72-80.
19. Remmers, E. F., J. Q. Yang, and K. B. Marcu. 1986. A negative transcriptional control element located upstream of the murine c-myc gene. EMBO J. 5: 899-904.
20. Pettersson, S., G. P. Cook, M. Bruggemann, G. T. Williams, and M. S. Neuberger. 1990. A second B cell-specific enhancer 3′ of the immunoglobulin heavy-chain locus. Nature 344: 165-168.
21. Matthias, P., and D. Baltimore. 1993. The immunoglobulin heavy chain locus contains another B-cell-specific 3′ enhancer close to the constant region. Mol. Cell. Biol. 13: 1547-1553.
22. Michaelson, J. S., S. L. Giannini, and B. K. Birshtein. 1995. Identification of 3′ α-hs4, a novel Ig heavy chain enhancer element regulated at multiple stages of B cell differentiation. Nucleic Acids Res. 23: 975-981.
23. Morse, H. C., 3rd, M. R. Anver, T. N. Fredrickson, D. C. Haines, A. W. Harris, N. L. Harris, E. S. Jaffe, S. C. Kogan, I. C. MacLennan, P. K. Pattengale, and J. M. Ward. 2002. Bethesda proposals for classification of lymphoid neoplasms in mice. Blood 100: 246-258.
24. Desagher, S., D. Severac, A. Lipkin, C. Bernis, W. Ritchie, A. Le Digarcher, and L. Journot. 2005. Genes regulated in neurons undergoing transcription-dependent apoptosis belong to signaling pathways rather than the apoptotic machinery. J. Biol. Chem. 280: 5693-5702.
25. Guglielmi, L., V. Truffinet, C. Carrion, M. Le Bert, N. Cogne, M. Cogne, and Y. Denizot. 2005. The 5′HS4 insulator element is an efficient tool to analyse the transient expression of an Em mu-GFP vector in a transgenic mouse model. Transgenic Res. 14: 361-364.
26. Guglielmi, L., V. Truffinet, M. Cogne, and Y. Denizot. 2003. The β-globin HS4 insulator confers copy-number dependent expression of IgH regulatory elements in stable B cell transfectants. Immunol. Lett. 89: 119-123.
27. Chauveau, C., E. Pinaud, and M. Cogne. 1998. Synergies between regulatory elements of the immunoglobulin heavy chain locus and its palindromic 3′ locus control region. Eur. J. Immunol. 28: 3048-3056.
28. Pelengaris, S., and M. Khan. 2003. The many faces of c-Myc. Arch. Biochem. Biophys. 416: 129-136.
29. Lin, Y., K. Wong, and K. Calame. 1997. Repression of c-myc transcription by Blimp-1, an inducer of terminal B cell differentiation. Science 276: 596-599.
30. Zhu, D., C. F. Qi, H. C. Morse, 3rd, S. Janz, and F. K. Stevenson. 2005. Deregulated expression of the Myc cellular oncogene drives development of mouse "Burkitt-like" lymphomas from naive B cells. Blood 105: 2135-2137.
31. Guglielmi, L., M. Le Bert, I. Comte, M. L. Dessain, M. Drouet, C. Ayer-Le Lievre, M. Cogne, and Y. Denizot. 2003. Combination of 3′ and 5′ IgH regulatory elements mimics the B-specific endogenous expression pattern of IgH genes from pro-B cells to mature B cells in a transgenic mouse model. Biochim. Biophys. Acta 1642: 181-190.
32. Weisinger, G., E. F. Remmers, P. Hearing, and K. B. Marcu. 1988. Multiple negative elements upstream of the murine c-myc gene share nuclear factor binding sites with SV40 and polyoma enhancers. Oncogene 3: 635-646.
33. Lindstrom, M. S., and K. G. Wiman. 2002. Role of genetic and epigenetic changes in Burkitt lymphoma. Semin. Cancer Biol. 12: 381-387.
34. Sanchez-Beato, M., A. Sanchez-Aguilera, and M. A. Piris. 2003. Cell cycle deregulation in B-cell lymphomas. Blood 101: 1220-1235.
35. L or Bcl-2 is bypassed during lymphomagenesis. Mol. Cell. Biol. 21: 5063-5070.
36. Gartel, A. L., and A. L. Tyner. 2002. The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol. Cancer Ther. 1: 639-649.