Decreased E47 in senescent B cell precursors is stage specific and regulated posttranslationally by protein turnover

Journal of Immunology

Volumn 173, Issue 2, 2004, Pages 818-827

  Van Der Put, Elaine ^a   Frasca, Daniela ^a   King, Anne M ^a   Blomberg, Bonnie B ^a   Riley, Richard L ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CALPAIN I INHIBITOR; CALPAIN II INHIBITOR; CALPASTATIN; CYCLOHEXIMIDE; DACTINOMYCIN; GENE PRODUCT; IKAROS TRANSCRIPTION FACTOR; INTERLEUKIN 7; LACTACYSTIN; MESSENGER RNA; PROTEASOME; PROTEASOME INHIBITOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BOB1; TRANSCRIPTION FACTOR E2A; TRANSCRIPTION FACTOR E47; TRANSCRIPTION FACTOR PAX5; UNCLASSIFIED DRUG;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; IN VITRO STUDY; LYMPHOPOIESIS; MALE; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN STABILITY; SENESCENCE; TRANSLATION REGULATION; UBIQUITINATION;

EID: 3142721218     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.2.818     Document Type: Article

References (53)

1. Quong, M. W., W. J. Romanow, and C. Murre. 2002. E protein function in lymphocyte development. Annu. Rev. Immunol. 20:301.
2. 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.
3. Murre, C., G. Bain, M. A. van Dijk, I. Engel, B. A. Furnari, M. E. Massari, J. R. Matthews, M. W. Quong, R. R. Rivera. and M. H. Stuiver. 1994. Structure and function of helix-loop-helix proteins. Biochim. Biophys. Acta 1218:129.
4. Massari, M. E., P. A. Jennings, and C. Murre. 1996. The AD1 transactivation domain of E2A contains a highly conserved helix, which is required for its activity in both Saccharomyces cerevisiae and mammalian cells. Mol. Cell. Biol. 16:121.
5. Murre, C., A. Voronova, and D. Baltimore. 1991. B-cell- and myocyte-specific E2-box-binding factors contain E12/E47-like subunits. Mol. Cell. Biol. 11:1156.
6. Sloan, S. R., C. P. Shen, R. McCarrick-Walmsley, and T. Kadesh. 1996. Phosphorylation of-EA7 as a potential determinant of B-cell-specific activity. Mol. Cell. Biol. 16:6900.
7. 1 cyclin-dependent kinases. J. Biol. Chem. 276:8524.
8. Lassar, A. B., R. L. Davis, W. E. Wright, T. Kadesch, C. Murre, A. Voronova, D. Baltimore, and H. Weintraub. 1991. Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo. Cell 66:305.
9. Lee, J. E., S. M. Hollenberg, L. Snider, D. L. Turner, N. Lipnick, and H. Weintraub, H. 1995. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268:836.
10. Bain, G., E. C. Maandag, D. J. Izon, D. Amsen, A. M. Kruisbeek, B. C. Weintraub, I. Krop, M. S. Schlissel, A. J. Feeney, and M. van Roon. 1994. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79:885.
11. Zhuang, Y., P. Soriano, and H. Weintraub. 1994. The helix-loop-helix gene E2A is required for B cell formation. Cell 79:875.
12. Bain, G., E. C. Robanus Maandag, H. P. te Riele, A. J. Feeney, A. Sheehy, M. Schlissel, S. A. Shinton, R. R. Hardy, and C. Murre. 1997. Both E12 and E47 allow commitment to the B cell lineage. Immunity 6:145.
13. Bain, G., and C. Murre. 1998. The role of E-proteins in B- and T-lymphocyte development. Semin. Immunol. 10:143.
14. 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. 5:1376.
15. Choi, J. K., C. P. Shen, H. S. Radomska, L. A. Eckhardt, and T. Kadesch. 1996. E47 activates the Ig-heavy chain and TdT loci in non-B cells. EMBO J. 15:5014.
16. Sigvardsson, M., M. O'Riordan, and R. Grosschedl. 1997. EBF and E47 collaborate to induce expression of the endogenous immunoglobulin surrogate light chain genes. Immunity 7:25.
17. 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.
18. Romanow, W. J., A. W. Langerak, P. Goebel, I. L. Wolvers-Tettero, J. J. 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 immunoglobulin repertoire in nonlymphoid cells. Mol. Cell 5:343.
19. Goebel, P., N. Janney, J. R. Valenzuela, W. J. Romanow, C. Murre, and A. J. Feeney. 2001. Localized gene-specific induction of accessibility to V(D)J recombination induced by E2A and early B cell factor in nonlymphoid cells. J. Exp. Med. 194:645.
20. Quong, M. W., D. P. Harris, S. L. Swain and C. Murre. 1999. E2A activity is induced during B-cell activation to promote immunoglobulin class switch recombination. EMBO J. 18:6307.
21. Riley, R. L., J. Knowles and A. M. King. 2002. Levels of E2A protein expression in B cell precursors are stage-dependent and inhibited by stem cell factor (c-kit ligand). Exp. Hematol. 30:1412.
22. Xin, X. Q., C. Nelson, L. Collins and K. Dorshkind. 1993. Kinetics of E2A basic helix-loop-helix protein expression during myelopoiesis and primary B cell differentiation. J. Immunol. 151:5398.
23. Herblot, S., P. D. Aplan, and T. Hoang. 2002. Gradient of E2A activity in B-cell development. Mol. Cell. Biol. 22:886.
24. Riley, R. L., M. G. Kruger, and J. Elia. 1991. B cell precursors are decreased in senescent BALB/c mice, but retain normal mitotic activity in vivo and in vitro. Clin. Immunol. Immunopathol. 59:301.
25. Sherwood, E. M., B. B. Blomberg, W. Xu, C. A. Warner, and R. L. Riley. 1998. Senescent BALB/c mice exhibit decreased expression of λ5 surrogate light chains and reduced development within the pre-B cell compartment. J. Immunol. 161:4472.
26. Stephan, R. P., V. M. Sanders and P. L. Witte. 1996. Stage-specific alterations in murine B lymphopoiesis with age. Int. Immunol. 8:509.
27. Van der Put, E., D. Frasca, B. B. Blomberg, and R. L. Riley. 2003. Aged mice exhibit distinct B cell precursor phenotypes differing in activation, proliferation, and apoptosis. Exp. Gerontol. 38:1137.
28. Klinman, N. R., and G. H. Kline. 1997. The B-cell biology of aging. Immunol. Rev. 160:103.
29. Kirman, I., K. Zhao, Y. Wang, P. Szabo, W. Telford, and M. E. Weksler. 1998. Increased apoptosis of bone marrow pre-B cells in old mice associated with their low number. Int. Immunol. 10:1385.
30. Stephan, R. P., C. R. Reilly and P. L. Witte. 1998. Impaired ability of bone marrow stromal cells to support B-lymphopoiesis with age. Blood 91:75.
31. Sherwood, E. M., W. Xu, and R. L. Riley. 2003. B cell precursors in senescent mice exhibit decreased recruitment into proliferative compartments and altered expression of Bcl-2 family members. Mech. Ageing Dev. 124:147.
32. Melchers, F., E. ten Boekel, T. Seidl, X. C. Kong, T. Yamagami, K. Onishi, T. Shimizu, A. G. Rolink, and J. Andersson. 2000. Repertoire selection by pre-B-cell receptors and B-cell receptors, and genetic control of B-cell development from immature to mature B cells. Immunol. Rev. 175:33.
33. Sherwood, E. M., W. Xu, A. M. King, B. B. Blomberg, and R. L. Riley. 2000. The reduced expression of surrogate light chains.in B cell precursors from senescent BALB/c mice is associated with decreased E2A proteins. Mech. Ageing Dev. 118:45.
34. Frasca, D., D. Nguyen, R. L. Riley, and B. B. Blomberg. 2003. Decreased E12 and/or E47 transcription factor activity in the bone marrow as well as in the spleen of aged mice. J. Immunol. 170:719.
35. Hardy, R. R., C. E. Carmack, S. A. Shinton, J. D. Kemp, and K. Hayakawa. 1991. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173:1213.
36. Lu, L., G. Smithson, P. W. Kincade, and D. G. Osmond. 1998. Two models of murine B lymphopoiesis: a correlation. Eur. J. Immunol. 28:1755.
37. Frasca, D., D. Nguyen, E. Van der Put, R. L. Riley, and B. B. Blomberg. 2003. The age-related decrease in E47 DNA-binding does not depend on increased Id inhibitory proteins in bone marrow-derived B cell precursors. Front. Biosci. 8:110.
38. Kho, C. J., G. S. Huggins, W. O. Endege, C. Hsieh, and M. Lee. 1997. Degradation of E2A proteins through an ubiquitin-conjugating enzyme UbcE2A. J. Biol. Chem. 272:3845.
39. Huggins, G. S., M. T. Chin, N. E. Sibinga, S. L. Lee, E. Haber, and M. E. Lee. 1999. Characterization of the mUBC9-binding sites required for E2A protein degradation. J. Biol. Chem. 274:28690.
40. Fenteany, G., R. F. Standaert, W. S. Lane, S. Choi, E. J. Corey, and S. L. Schreiber. 1995. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268:726.
41. Choi, Y. H., S. J. Lee, P. Nguyen, J. S. Jang, J. Lee, M. L. Wu, E. Takano, M. Maki, P. A. Henkart, and J. B. Trepel. 1997. Regulation of cyclin D1 by calpain protease. J. Biol. Chem. 272:28479.
42. Wang, K. K., and P. W. Yuen. 1994. Calpain inhibition: an overview of its therapeutic potential. Trends Pharmacol. Sci. 15:412.
43. Nie, L., M. Xiu, A. Vladimirova, and X.-H. Sun. 2003. Notch-induced E2A ubiquitination and degradation are controlled by Map kinase activities. EMBO J. 22:5780.
44. Kee, B. L., R. R. Rivera, and C. Murre. 2001. Id3 inhibits B lymphocyte progenitor growth and survival in response to TGF-β. Nat. Immunol. 2:242.
45. Sayegh, C. E., M. W. Quong, Y. Agata, and C. Murre. 2003. E-proteins directly regulate expression of activation-induced deaminase in mature B cells. Nat. Immunol. 4:586.
46. Szabo, P., S. Shen, W. Telford, and M. E. Weksler. 2003. Impaired rearrangement of Ig V to DJ segments in bone marrow pro-B cells from old mice. Cell. Immunol. 222:78.
47. Hardy, R. R. 2003. B-cell commitment: deciding on the players. Curr. Opin. Immunol. 15:158.
48. Westman, B. J., J. P. Mackay, and D. Gell. 2002. Ikaros: a key regulator of haematopoiesis. Int. J. Biochem. Cell Biol. 34:1304.
49. Rolink, A. G., C. Schaniel, M. Busslinger, S. Nutt, and F. Melchers. 2000. Fidelity and infidelity in commitment to B-lymphocyte lineage development. Immunol. Rev. 175:104.
50. Stephan, R. P., D. A. Lill-Elghanian, and P. L. Witte. 1997. Development of B cells in aged mice: decline in the ability of pro-B cells to respond to IL-7 but not to other growth factors. J. Immunol. 158:1598.
51. Zhuang, Y., P. Cheng, and H. Weintraub. 1996. B-lymphocyte development is regulated by the combined dosage of three basic helix-loop-helix genes, E2A, E2-2, and HEB. Mol. Cell. Biol. 16:2898.
52. O'Riordan, M., and R. Grosschedl. 1999. Coordinate regulation of B cell differentiation by the transcription factors EBF and E2A. Immunity 11:21.
53. Frasca, D., E. Van Der Put, R. L. Riley, and B. B. Blomberg. 2004. Reduced Ig class switch in aged mice correlates with decreased E47 and activation-induced cytidine deaminase. J. Immunol. 172:2155.