Receptor Editing and Marginal Zone B Cell Development Are Regulated by the Helix-Loop-Helix Protein, E2A

Journal of Experimental Medicine

Volumn 199, Issue 8, 2004, Pages 1101-1112

  Quong, Melanie W ^a   Martensson, Annica ^b   Langerak, Anton W ^c   Rivera, Richard R ^a   Nemazee, David ^b   Murre, Cornelis ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

Author keywords

Checkpoint; E proteins; Follicular B cells; Id3; RAG

Indexed keywords

B LYMPHOCYTE RECEPTOR; DNA; GENE PRODUCT; HELIX LOOP HELIX PROTEIN; IMMUNOGLOBULIN LIGHT CHAIN; PROTEIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL MATURATION; FLOW CYTOMETRY; GENE EXPRESSION; GENE REARRANGEMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; B-LYMPHOCYTES; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; DNA PRIMERS; DNA-BINDING PROTEINS; GENE EXPRESSION; GENE REARRANGEMENT, B-LYMPHOCYTE, LIGHT CHAIN; GENES, RAG-1; HELIX-LOOP-HELIX MOTIFS; HETEROZYGOTE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, B-CELL; RNA EDITING; TCF TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 2442587261     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20031180     Document Type: Article

References (48)

1. Alt, F.W., G.D. Yancopoulos, T.K. Blackwell, C. Wood, E. Thomas, M. Boss, R. Coffman, N. Kosenberg, S. Tonegawa, and D. Baltimore. 1984. Ordered rearrangement of immunoglobulin heavy chain variable region segments. EMBO J. 3:1209-1219.
2. Rajewsky, K. 1996. Clonal selection and learning in the antibody system. Nature. 381:751-758.
3. Cedar, H., and Y. Bergman. Developmental regulation of immune system gene rearrangement. 1999. Curr. Opin. Immunol. 11:64-69.
4. Nussenzweig, M.C., A.C. Shaw, E. Sinn, D.B. Danner, H.C. Hohnes, C. Morse III, and P. Leder. 1988. Allelic exclusion in transgenic mice that express the membrane form of immunoglobulin μ. Science. 236:816-819.
5. Manz, J., K. Denis, O. Witte, R. Brinster, and U. Storb. 1988. Feedback inhibition of immunoglobulin gene rearrangement by membrane but not by secreted μ heavy chains. J. Exp. Med. 168:1363-1381.
6. Sleckman, B.P., J.R. Gorman, and F.W. Alt. 1996. Accessibility control of antigen-receptor variable-region gene assembly: role of cis-acting element. Annu. Rev. Immunol. 14:459-481.
7. Goodnow, C.C., J. Crosbie, S. Adelstein, T.B. Lavoie, S.J. Smith-Gill, R.A. Brink, H. Pritchard-Briscoe, J.S. Wotherspoon, R.H. Loblay, and K. Raphale. 1988. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature. 334:676-682.
8. Nemazee, D.A., and K. Burki. 1989. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature. 337:562-566.
9. Gay, D., T. Saunders, S. Camper, and M. Weigert. 1993. Receptor editing: an approach by autoreactive B cells to escape tolerance. J. Exp. Med. 177:999-1008.
10. Tiegs, S.L., D.M. Russell, and D. Nemazee. 1993. Receptor editing in self-reactive bone marrow B cells. J. Exp. Med. 177:1009-1020.
11. Radic, M.Z., J. Erikson, S. Litwin, and M. Weigert. 1993. B lymphocytes may escape tolerance by revising their antigen receptors. J. Exp. Med. 177:1165-1173.
12. Casellas, R., T. Shih, M. Kleinewietfeld, J. Rakonjac, D. Nemazee, K. Rajewsky, and M.C. Nussenzweig. 2001. Contribution of receptor editing to the antibody repertoire. Science. 291:1541-1544.
13. Melamed, D., R.J. Benschop, J.C. Cambier, and D. Nemazee. 1998. Developmental regulation of B lymphocyte immune tolerance compartmentalizes clonal selection from receptor selection. Cell. 92:173-182.
14. Zhuang, Y., P. Soriano, and H. Weintraub. 1994. The helix-loop-helix gene E2A is required for B cell formation. Cell. 79:875-884.
15. Bain, G., E. Robanus Maandag, D. Izon, D. Armsen, A. Kruisbeek, B.C. Weintraub, I. Krop, M.S. Schlissel, A. Feeney, M. van Roon, M. van der Valk, H.P.J. te Riele, A. Berns, and C. Murre. 1994. E2A proteins are required for proper B cell development and initiation of immunoglobuhn gene rearrangements. Cell. 79:885-892.
16. Urbanek, P., Z. Wang, I. Fetka, E.F. Wagner, and M. Busslinger. 1994. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell. 79:901-912.
17. Lin, H., and R. Grosschedl. 1995. Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature. 376:263-267.
18. Engel, I., and C. Murre. 2001. The function of E- and Id proteins in lymphocyte development. Nat. Rev. Immunol. 1:193-200.
19. O'Riordan, M., and R. Grosschedl. 1999. Coordinate regulation of B cell differentiation by the transcription factors EBF and E2A. Immunity. 11:21-31.
20. Kee, B.L., and C. Murre. 1998. Induction of early B cell factor (EBF) and multiple B lineage genes by the basic helix-loop-helix transcription factor E12. J. Exp. Med. 188:699-713.
21. Kee, B.L., R.R. Rivera, and C. Murre. 2001. Id3 inhibits B lymphocyte progenitor growth and survival in response to TGF-β. Nat. Immun. 2:242-247.
22. Schlissel, M., A. Voronova, and D. Baltimore. 1991. Helix-loop-helix transcription factor E47 activates germ-line immunoglobulin heavy-chain gene transcription and rearrangement in a pre-T-cell line. Genes Dev. 5:1367-1371.
23. Romanow, W., A.W. Langerak, P. Goebel, I.L.M. Wovers-Tettero, J.J.M. van Dongen, A.J. Feeney, and C. Murre. 2000. E2A and EBF act in synergy with the V(D)J recombinase to generate a diverse immunoglobuhn repertoire in nonlymphoid cells. Mol. Cell. 5:343-553.
24. Rivera, R.R., C.P. Johns, J. Quan, R.S. Johnson, and Murre, C. 2000. Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3. Immunity. 12:17-26.
25. Engel, I., C. Johns, G. Bain, R.R. Rivera, and C. Murre. 2001. Early thymocyte development is regulated by modulation of E2A protein activity. J. Exp. Med. 194:733-745.
26. Schlissel, M.S., and D. Baltimore. 1989. Activation of immunolobulin kappa gene rearrangement correlates with induction of germline kappa gene transcription. Cell. 58:1001-1007.
27. Engel, H., A. Rolink, and S. Weiss. 1999. B cells are programmed to activate kappa and lambda for rearrangement at consecutive developmental stages. Eur. J. Immunol. 29:2167-2176.
28. Pongers-Willemse, M.J., O.J. Verhagen, G.J. Tibbe, A.J. Wijkhuis, V. de Haas, E. Roovers, C.E. van der Schoot, and J.J. van Dongen. 1998. Real-time quantitative PCR for the detection of minimal residual disease in acute lymphoblastic leukemia using junctional region specific TaqMan probes. Leukemia. 12:2006-2014.
29. Herblot, S., P.D. Aplan, and T. Hoang. 2002. Gradient of E2A activity in B cell development. Mol. Cell. Biol. 22:886-900.
30. Bain, G., S. Gruenwald, and C. Murre. 1993. E2A and E2-2 are subunits of B-cell-specific E2-box DNA-binding proteins. Mol. Cell. Biol. 13:3522-3529.
31. Shen, C.P., and T. Kadesch. 1995. B-cell-specific DNA binding by an E47 homodimer. Mol. Cell. Biol. 15:4518-4524.
32. Greenbaum, S., and Y. Zhuang. 2002. Identification of E2A target genes in B lymphocyte development by using a gene tagging-based chromatin immunoprecipitation system. Proc. Natl. Acad. Sci. USA. 99:15030-15035.
33. Goebel, P., N. Janney, J.R. Valenzuela, W.J. Romanow, C. Murre, and A. Feeney. 2001. Localized gene-specific induction of accessibility to V(D)J recombination induced by E2A and EBF in nonlymphoid cells. J. Exp. Med. 194:645-656.
34. Yu, W., H. Nagaoka, M. Jankovic, Z. Misulovin, H. Suh, A. Rolink, F. Melchers, E. Meffre, and M.C. Nussenzweig. 1999. Continued RAG expression in late stages of B cell development and no apparent re-induction after immunization. Nature. 400:682-687.
35. Xu, Y., L. Davidson, F.W. Alt, and D. Baltimore. 1996. Deletion of the IgK light chain intronic enhancer/matrix attachment region impairs but does not abolish VκJκ rearrangement. Immunity. 4:377-385.
36. Siminovitch, K.A., A. Bakhshi, P. Goldman, and S.J. Korsmeyer. 1985. A uniform deleting element mediates the loss of kappa genes in human B cells. Nature. 316:260-262.
37. Hau, L. J. Lauring, H. Liang, S. Greenbaum, D. Cado, Y. Zhuang, and M.S. Schlissel. 2003. A conserved transcriptional enhancer regulates RAG gene expression in developing B cells. Immunity. 19:105-117.
38. Bain, G., C.B. Cravatt, C. Loomans, J. Alberola-Ila, S.M. Hedrick, and C. Murre. 2001. Regulation of the helix-loop-helix proteins, E2A and Id3, by the Ras-ERK MAPK cascade. Nat. Immun. 2:165-171.
39. Schebesta, M., P.L. Pfeffer, and M. Busslinger. 2002. Control of pre-BCR signaling by Pax-5 dependent activation of the BLNK gene. Immunity. 17:473-485.
40. Barndt, R.J., M. Dai, and Y. Zhuang. 2000. Functions of E2A/HEB heterodimers in T-cell development revealed by a dominant negative mutation of HEB. Mol. Cell. Biol. 20: 6677-6685.
41. Murre, C., P.S. McCaw, and D. Baltimore. 1989. A new DNA binding and dimerization motif in immunoglobulin enhancer, daughterless, MyoD and myc proteins. Cell. 56: 777-783.
42. Bain, G., M.W. Quong, R.S. Soloff, S.M. Hedrick, and C. Murre. 1999. Thymocyte maturation is regulated by the activity of the helix-loop-helix protein, E47. J. Exp. Med. 190: 1605-616.
43. Martin, F., and J.F. Kearney. 2002. Marginal zone B cells. Nat. Rev. Immunol. 2:323-335.
44. Wang, J.H., N. Avitahl, A. Cariappa, C. Friedrich, T. Ikeda, A. Renold, K. Andrikopoulos, L. Liang, S. Pillai, B.A. Morgan, and K. Georgopoulos. 1998. Aiolos regulates B cell activation and maturation to effector state. Immunity. 9:543-553.
45. Tanigaki, K., H. Han, N. Yamamoto, K. Tashiro, M. Ikegawa, K. Kuroda, A. Susuki, T. Nakano, and T. Honjo. 2002. Notch-RBP-J signaling is involved in cell fate determination of marginal zone B cells. Nat. Immun. 3:443-450.
46. Ordentlich, P., A. Lin, C.P. Shen, C. Blaumueller, K. Matsuno, S. Artavanis-Tsakonas, and T. Kadesch. 1998. Notch inhibition of E47 supports the existence of a novel signaling pathway. Mol. Cell. Biol. 18:2230-2239.
47. Nie, L., M. Xu, A. Vladimirova, and X.H. Sun. 2003. Notch-induced E2A ubiquitination and activities. EMBO J. 3:5780-5792.
48. Guinamard, R., M. Okigaki, J. Schlessinger, and J.V. Ravetch. 2000. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat. Immun. 1:31-36.