Notch-regulated periphery B cell differentiation involves suppression of E protein function

Journal of Immunology

Volumn 191, Issue 2, 2013, Pages 726-736

  Zhang, Ping ^a   Zhao, Ying ^a   Sun, Xiao Hong ^a  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN REPEAT SOCS BOX CONTAINING PROTEIN 2; DNA; E PROTEIN; INHIBITOR OF DIFFERENTIATION 2; NOTCH RECEPTOR; NOTCH1 RECEPTOR; PROTEIN BCL 6; SUPPRESSOR OF CYTOKINE SIGNALING 2; TRANSCRIPTION FACTOR E2A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL LEVEL; CELL LINE; CELL MATURATION; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; ENZYME INHIBITION; ENZYME REPRESSION; GAIN OF FUNCTION MUTATION; HUMORAL IMMUNITY; INTRACELLULAR SIGNALING; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHENOTYPE; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SPLEEN CELL; UBIQUITINATION; UPREGULATION;

ANIMALS; ANKYRIN REPEAT; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; DNA-BINDING PROTEINS; INHIBITOR OF DIFFERENTIATION PROTEIN 2; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS C-BCL-6; RECEPTOR, NOTCH1; RECEPTORS, PROSTAGLANDIN E; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; UBIQUITINATION;

EID: 84880088455     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202134     Document Type: Article

References (51)

1. Pillai, S., and A. Cariappa. 2009. The follicular versus marginal zone B lymphocyte cell fate decision. Nat. Rev. Immunol. 9: 767-777.
2. Merrell, K. T., R. J. Benschop, S. B. Gauld, K. Aviszus, D. Decote-Ricardo, L. J. Wysocki, and J. C. Cambier. 2006. Identification of anergic B cells within a wild-type repertoire. Immunity 25: 953-962. (Pubitemid 44894955)
3. Allman, D., and S. Pillai. 2008. Peripheral B cell subsets. Curr. Opin. Immunol. 20: 149-157.
4. Martin, F., and J. F. Kearney. 2002. Marginal-zone B cells. Nat. Rev. Immunol. 2: 323-335. (Pubitemid 37328755)
5. Pillai, S., A. Cariappa, and S. T. Moran. 2004. Positive selection and lineage commitment during peripheral B-lymphocyte development. Immunol. Rev. 197: 206-218. (Pubitemid 38142178)
6. Batten, M., J. Groom, T. G. Cachero, F. Qian, P. Schneider, J. Tschopp, J. L. Browning, and F. Mackay. 2000. BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med. 192: 1453-1466.
7. Cariappa, A., H. C. Liou, B. H. Horwitz, and S. Pillai. 2000. Nuclear factor kappa B is required for the development of marginal zone B lymphocytes. J. Exp. Med. 192: 1175-1182.
8. Moran, S. T., A. Cariappa, H. Liu, B. Muir, D. Sgroi, C. Boboila, and S. Pillai. 2007. Synergism between NF-kappa B1/p50 and Notch2 during the development of marginal zone B lymphocytes. J. Immunol. 179: 195-200. (Pubitemid 46986534)
9. Schiemann, B., J. L. Gommerman, K. Vora, T. G. Cachero, S. Shulga-Morskaya, M. Dobles, E. Frew, and M. L. Scott. 2001. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293: 2111-2114. (Pubitemid 32848063)
10. Saito, T., S. Chiba, M. Ichikawa, A. Kunisato, T. Asai, K. Shimizu, T. Yamaguchi, G. Yamamoto, S. Seo, K. Kumano, et al. 2003. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 18: 675-685. (Pubitemid 36588584)
11. Witt, C. M., W. J. Won, V. Hurez, and C. A. Klug. 2003. Notch2 haploinsufficiency results in diminished B1 B cells and a severe reduction in marginal zone B cells. J. Immunol. 171: 2783-2788. (Pubitemid 37093496)
12. Tanigaki, K., H. Han, N. Yamamoto, K. Tashiro, M. Ikegawa, K. Kuroda, A. Suzuki, T. Nakano, and T. Honjo. 2002. Notch-RBP-J signaling is involved in cell fate determination of marginal zone B cells. Nat. Immunol. 3: 443-450. (Pubitemid 34520793)
13. Maillard, I., A. P. Weng, A. C. Carpenter, C. G. Rodriguez, H. Sai, L. Xu, D. Allman, J. C. Aster, and W. S. Pear. 2004. Mastermind critically regulates Notch-mediated lymphoid cell fate decisions. Blood 104: 1696-1702. (Pubitemid 39202276)
14. Hozumi, K., N. Negishi, D. Suzuki, N. Abe, Y. Sotomaru, N. Tamaoki, C. Mailhos, D. Ish-Horowicz, S. Habu, and M. J. Owen. 2004. Delta-like 1 is necessary for the generation of marginal zone B cells but not T cells in vivo. Nat. Immunol. 5: 638-644. (Pubitemid 38811889)
15. Hampel, F., S. Ehrenberg, C. Hojer, A. Draeseke, G. Marschall- Schröter, R. Kühn, B. Mack, O. Gires, C. J. Vahl, M. Schmidt-Supprian, et al. 2011. CD19-independent instruction of murine marginal zone B-cell development by constitutive Notch2 signaling. Blood 118: 6321-6331.
16. Murre, C. 2005. Helix-loop-helix proteins and lymphocyte development. Nat. Immunol. 6: 1079-1086. (Pubitemid 41541785)
17. Kee, B. L. 2009. E and ID proteins branch out. Nat. Rev. Immunol. 9: 175-184.
18. Sun, X. H. 2004. Multitasking of helix-loop-helix proteins in lymphopoiesis. Adv. Immunol. 84: 43-77.
19. Quong, M. W., A. Martensson, A. W. Langerak, R. R. Rivera, D. Nemazee, and C. Murre. 2004. Receptor editing and marginal zone B cell development are regulated by the helix-loop-helix protein, E2A. J. Exp. Med. 199: 1101-1112. (Pubitemid 38619906)
20. Beck, K., M. M. Peak, T. Ota, D. Nemazee, and C. Murre. 2009. Distinct roles for E12 and E47 in B cell specification and the sequential rearrangement of immunoglobulin light chain loci. J. Exp. Med. 206: 2271-2284.
21. Becker-Herman, S., F. Lantner, and I. Shachar. 2002. Id2 negatively regulates B cell differentiation in the spleen. J. Immunol. 168: 5507-5513. (Pubitemid 34556129)
22. Nie, L., M. Xu, A. Vladimirova, and X. H. Sun. 2003. Notch-induced E2A ubiquitination and degradation are controlled by MAP kinase activities. EMBO J. 22: 5780-5792. (Pubitemid 37408817)
23. Huang, Z., L. Nie, M. Xu, and X. H. Sun. 2004. Notch-induced E2A degradation requires CHIP and Hsc70 as novel facilitators of ubiquitination. Mol. Cell. Biol. 24: 8951-8962. (Pubitemid 39313900)
24. Nie, L., S. S. Perry, Y. Zhao, J. Huang, P. W. Kincade, M. A. Farrar, and X. H. Sun. 2008. Regulation of lymphocyte development by cell-type-specific interpretation of Notch signals. Mol. Cell. Biol. 28: 2078-2090. (Pubitemid 351342637)
25. Nie, L., Y. Zhao, W. Wu, Y. Z. Yang, H. C. Wang, and X. H. Sun. 2011. Notch-induced Asb2 expression promotes protein ubiquitination by forming noncanonical E3 ligase complexes. Cell Res. 21: 754-769.
26. Cochrane, S. W., Y. Zhao, R. S. Welner, and X. H. Sun. 2009. Balance between Id and E proteins regulates myeloid-versus-lymphoid lineage decisions. Blood 113: 1016-1026.
27. Wang, H. C., V. Peng, Y. Zhao, and X. H. Sun. 2012. Enhanced Notch activation is advantageous but not essential for T cell lymphomagenesis in Id1 transgenic mice. PLoS ONE 7: e32944.
28. Schmitt, T. M., and J. C. Zúñiga-Pflücker. 2002. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17: 749-756. (Pubitemid 35477794)
29. Soriano, P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21: 70-71. (Pubitemid 29036285)
30. Srinivas, S., T. Watanabe, C. S. Lin, C. M. William, Y. Tanabe, T. M. Jessell, and F. Costantini. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1: 4.
31. Rickert, R. C., J. Roes, and K. Rajewsky. 1997. B lymphocyte-specific, Cremediated mutagenesis in mice. Nucleic Acids Res. 25: 1317-1318.
32. Ruzinova, M. B., and R. Benezra. 2003. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13: 410-418. (Pubitemid 36897645)
33. Kin, N.W., D. M. Crawford, J. Liu, T.W. Behrens, and J. F. Kearney. 2008. DNA microarray gene expression profile of marginal zone versus follicular B cells and idiotype positive marginal zone B cells before and after immunization with Streptococcus pneumoniae. J. Immunol. 180: 6663-6674.
34. Zambrowicz, B. P., A. Imamoto, S. Fiering, L. A. Herzenberg, W. G. Kerr, and P. Soriano. 1997. Disruption of overlapping transcripts in the ROSA beta geo 26 gene trap strain leads to widespread expression of beta-galactosidase in mouse embryos and hematopoietic cells. Proc. Natl. Acad. Sci. USA 94: 3789-3794. (Pubitemid 27180451)
35. Park, S. T., and X. H. Sun. 1998. The Tal1 oncoprotein inhibits E47-mediated transcription. Mechanism of inhibition. J. Biol. Chem. 273: 7030-7037. (Pubitemid 28160370)
36. Sun, X.-H., N. G. Copeland, N. A. Jenkins, and D. Baltimore. 1991. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol. Cell. Biol. 11: 5603-5611. (Pubitemid 21895327)
37. Nie, L., H. Wu, and X. H. Sun. 2008. Ubiquitination and degradation of Tal1/ SCL are induced by notch signaling and depend on Skp2 and CHIP. J. Biol. Chem. 283: 684-692.
38. Cariappa, A., C. Boboila, S. T. Moran, H. Liu, H. N. Shi, and S. Pillai. 2007. The recirculating B cell pool contains two functionally distinct, long-lived, posttransitional, follicular B cell populations. J. Immunol. 179: 2270-2281.
39. Srivastava, B., W. J. Quinn, III, K. Hazard, J. Erikson, and D. Allman. 2005. Characterization of marginal zone B cell precursors. J. Exp. Med. 202: 1225-1234. (Pubitemid 41586953)
40. Lin, Y. C., S. Jhunjhunwala, C. Benner, S. Heinz, E. Welinder, R. Mansson, M. Sigvardsson, J. Hagman, C. A. Espinoza, J. Dutkowski, et al. 2010. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat. Immunol. 11: 635-643.
41. Artavanis-Tsakonas, S., M. D. Rand, and R. J. Lake. 1999. Notch signaling: cell fate control and signal integration in development. Science 284: 770-776. (Pubitemid 29291335)
42. Radtke, F., A. Wilson, and H. R. MacDonald. 2005. Notch signaling in hematopoiesis and lymphopoiesis: lessons from Drosophila. Bioessays 27: 1117-1128. (Pubitemid 43076138)
43. Tan, J. B., K. Xu, K. Cretegny, I. Visan, J. S. Yuan, S. E. Egan, and C. J. Guidos. 2009. Lunatic and manic fringe cooperatively enhance marginal zone B cell precursor competition for delta-like 1 in splenic endothelial niches. Immunity 30: 254-263.
44. Radtke, F., N. Fasnacht, and H. R. Macdonald. 2010. Notch signaling in the immune system. Immunity 32: 14-27.
45. Allman, D., J. A. Punt, D. J. Izon, J. C. Aster, and W. S. Pear. 2002. An invitation to T and more: notch signaling in lymphopoiesis. Cell 109(Suppl): S1-S11. (Pubitemid 34457847)
46. 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: 1367-1376. (Pubitemid 21906045)
47. Murre, C., P. S. McCaw, and D. Baltimore. 1989. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56: 777-783. (Pubitemid 19082513)
48. Kadesch, T. 1992. Helix-loop-helix proteins in the regulation of immunoglobulin gene transcription. Immunol. Today 13: 31-36.
49. Pasqualucci, L., O. Bereschenko, H. Niu, U. Klein, K. Basso, R. Guglielmino, G. Cattoretti, and R. Dalla-Favera. 2003. Molecular pathogenesis of non- Hodgkin's lymphoma: the role of Bcl-6. Leuk. Lymphoma 44(Suppl. 3): S5-S12. (Pubitemid 38196057)
50. Basso, K., and R. Dalla-Favera. 2010. BCL6: master regulator of the germinal center reaction and key oncogene in B cell lymphomagenesis. Adv. Immunol. 105: 193-210.
51. Barish, G. D., R. T. Yu, M. Karunasiri, C. B. Ocampo, J. Dixon, C. Benner, A. L. Dent, R. K. Tangirala, and R. M. Evans. 2010. Bcl-6 and NF-kappaB cistromes mediate opposing regulation of the innate immune response. Genes Dev. 24: 2760-2765.