Deviation of the B cell pathway in senescent mice is associated with reduced surrogate light chain expression and altered immature B cell generation, phenotype, and light chain expression

Journal of Immunology

Volumn 182, Issue 1, 2009, Pages 138-147

  Alter Wolf, Sarah ^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

BREAKPOINT CLUSTER REGION PROTEIN; LEUKOSIALIN; STEM CELL FACTOR; PRE B CELL RECEPTOR; SURROGATE IMMUNOGLOBULIN LIGHT CHAIN;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; IN VIVO CULTURE; LIGHT CHAIN; LYMPHOPOIESIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; WILD TYPE; AGING; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTOPENIA; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; PRE B LYMPHOCYTE; SIGNAL TRANSDUCTION;

AGING; ANIMALS; B-LYMPHOCYTE SUBSETS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; IMMUNOGLOBULIN LIGHT CHAINS, SURROGATE; IMMUNOPHENOTYPING; LYMPHOPENIA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PRE-B CELL RECEPTORS; PRECURSOR CELLS, B-LYMPHOID; SIGNAL TRANSDUCTION;

EID: 59849105341     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.182.1.138     Document Type: Article

References (38)

1. 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: 301-313.
2. Stephan, R. P., V. M. Sanders, and P. L. Witte. 1996. Stage-specific alterations in murine B lymphopoiesis with age. Int. Immunol. 8: 509-518.
3. Sherwood, E. M., B. B. Blomberg, W. Xu, C. A. Warner, and R. L. Riley. 1998. Cutting edge: Senescent BALB/c mice exhibit decreased expression of λ5 surrogate light chains and reduced development within the pre-B cell compartment. J. Immunol. 161: 4472-4475.
4. Miller, J. P., and D. Allman. 2003. The decline in B lymphopoiesis in aged mice reflects loss of very early B-lineage precursors. J. Immunol. 171: 2326-2330.
5. Labrie, J. E., L. Borghesi, and R. Gerstein. 2005. Bone marrow microenvironmental changes in aged mice compromise VDJ recombinase activity and B cell generation in aged mice. J. Exp. Med. 200: 411-423.
6. Van der Put, E., E. M. Sherwood, 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: 1137-1147.
7. 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: 1598-1609.
8. 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: 1385-1392.
9. Szabo, P., S. Shen, W. Telford, and M. E. Weksler. 2003. Impaired rearrangement of IgH V to DJ segments in bone marrow pro-B cells from old mice. Cell. Immunol. 222: 78-87.
10. Riley, R. L., E. Van der Put, A. M. King, D. Frasca, and B. B. Blomberg. 2005. Deficient B lymphopoiesis in murine senescence: potential roles for dysregulation of E2A, Pax-5, and STAT5. Semin. Immunol. 17: 330-336.
11. 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: 45-59.
12. Frasca, D., D. Nguyyen, 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: 719-726.
13. Van der Put, E., D. Frasca, A. M. King, B. B. Blomberg, and R. L. Riley. 2004. Decreased E47 in senescent B cell precursors is stage specific and regulated posttranslationally by protein turnover. J. Immunol. 173: 818-827.
14. King, A. M., E. Van der Put, B. B. Blomberg, and R. L. Riley. 2007. Accelerated Notch-dependent degradation of E47 proteins in aged B cell precursors is associated with increased ERK MAPK activation. J. Immunol. 178: 3521-3529.
15. 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: 25-36.
16. Riley, R. L., B. B. Blomberg, and D. Frasca. 2005. B cells, E2A, and aging. Immunol. Rev. 205: 30-47.
17. Kawano, Y., S. Yoshikawa, Y. Minegishi, and H. Karasuyama. 2006. Pre-B cell receptor assesses the quality of IgH chains and tunes the pre-B cell repertoire by delivering differential signals. J. Immunol. 177: 2242-2249.
18. Kitamura, D., A. Kudo, S. Schaal, W. Muller, F. Melchers, and K. Rajewsky. 1992. A critical role of λ5 protein in B cell development. Cell 69: 823-831.
19. Karasuyama, H., A. Rolink, Y. Shinkai, F. Young, F. W. Alt, and F. Melchers. 1994. The expression of Vpre-B/λ5 surrogate light chain in early bone marrow precursor B cells of normal and B cell-deficient mutant mice. Cell 77: 133-143.
20. Rolink, A., U. Grawunder, T. H. Winkler, H. Karasuyama, and F. Melchers. 1994. IL-2 receptor α chain (CD25. TAC) expression defines a crucial stage in pre-B cell development. Int. Immunol. 6: 1257-1264.
21. Rolink, A. G., T. Winkler, F. Melchers, and J. Andersson. 2000. Precursor B cell receptor-dependent B cell proliferation and differentiation does not require the bone marrow or fetal liver environment. J. Exp. Med. 191: 23-32.
22. ten Boekel, E., F. Melchers, and A. G. Rolink. 1997. Changes in the V(H) gene repertoire of developing precursor B lymphocytes in mouse bone marrow mediated by the pre-B cell receptor. Immunity 7: 357-368.
23. Wilson, E. L., E. M. Sherwood, A. M. King, and, R. L. Riley. 2003. A phenotypically distinct subset of immature B cells exhibits partial activation, increased survival, and preferential expression of VhS107. Eur. J. Immunol. 33: 3398-3408.
24. Wilson, E. L., A. M. King, E. M. Sherwood, and R. L. Riley. 2005. Pre-B cell loss in senescence coincides with preferential development of immature B cells characterized by partial activation and altered Vh repertoire. Exp. Gerontol. 40: 67-79.
25. Shinjo, F., R. R. Hardy, and J. Jongstra. 1994. Monoclonal anti-λ5 antibody FS1 identifies a 130kDa protein associated with λ5 and VpreB on the surface of early pre-B cell lines. Int. Immunol. 6: 393-399.
26. Kawano, Y., S. Yoshikawa, Y. Minegishi, and H. Karsuyama. 2005. Selection of stereotyped VH81X-μH chains via pre-B cell receptor early in ontogeny and their conservation in adults by marginal zone B cells. Int. Immunol. 17: 857-867.
27. 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 stages in normal mouse bone marrow. J. Exp. Med. 173: 1213-1225.
28. + stage. Eur. J. Immunol. 34: 2647-2655.
29. Lindsley, R. C., M. Thomas, B. Srivastava, and D. Allman. 2007. Generation of peripheral B cells occurs via two spatially and temporally distinct pathways. Blood 109: 2521-2528.
30. Yamamoto, M., K. Hayashi, T. Nojima, Y. Matsuzaki, Y. Kawano, H. Karasuyama, R. Goitsuka, and D. Kitamura. 2006. BASH-novel PKC-Raf-1 pathway of pre-BCR signaling induces κ gene rearrangement. Blood 108: 2703-2711.
31. Riley, S. C., B. G. Froscher, P. J. Linton, D. Zharhary, K. Marcu, and N. R. Klinman. 1989. Altered VH gene segment utilization in the response to phosphorylcholine by aged mice. J. Immunol. 143: 3798-3805.
32. Kline, G. H., T. A. Hayden, and N. R. Klinman. 1999. B cell maintenance in aged mice reflects both increased B cell longevity and decreased B cell generation. J. Immunol. 162: 3342-3349.
33. Johnson, K. M., K. Owen, and P. L. Witte. 2002. Aging and developmental transitions in the B cell lineage. Int. Immunol. 14: 1313-1323.
34. Klinman, N. R., and G. H. Kline. 1997. The B-cell biology of aging. Immunol. Rev. 160: 103-114.
35. Kenny, J. J., L. J. Rezanka, A. Lustig, R. T. Fischer, J. Yoder, S. Marshall, and D. L. Longo. 2000. Autoreactive B cells escape clonal deletion by expressing multiple antigen receptors. J. Immunol. 164: 4111-4119.
36. Li, Y., H. Li, D. Ni, and M. Weigert. 2002. Anti-DNA B cells in MRL/lpr mice show altered differentiation and editing pattern. J. Exp. Med. 196: 1543-1552.
37. +) arise during the ontogeny of B cells in the bone marrow of normal nontransgenic mice. Cell. Immunol. 238: 38-48.
38. 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.