Direct reduction of antigen receptor expression in polyclonal B cell populations developing in vivo results in light chain receptor editing

Journal of Immunology

Volumn 188, Issue 1, 2012, Pages 47-56

  Shen, Shixue ^a   Manser, Tim ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR; SHORT HAIRPIN RNA;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; GENE; GENE EXPRESSION; GENE REARRANGEMENT; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; RAG GENE; TRANSLATION REGULATION;

ANIMALS; CELL LINE; GENE EXPRESSION REGULATION; IMMUNOGLOBULIN KAPPA-CHAINS; IMMUNOGLOBULIN LAMBDA-CHAINS; MICE; RECEPTORS, ANTIGEN, B-CELL; RNA EDITING; RNA, MESSENGER;

EID: 84855398937     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102109     Document Type: Article

References (45)

1. Rolink, A. G., E. ten Boekel, T. Yamagami, R. Ceredig, J. Andersson, and F. Melchers. 1999. B cell development in the mouse from early progenitors to mature B cells. Immunol. Lett. 68: 89-93. (Pubitemid 29265657)
2. von Boehmer, H. 2004. Selection of the T-cell repertoire: receptor-controlled checkpoints in T-cell development. Adv. Immunol. 84: 201-238.
3. Löffert, D., S. Schaal, A. Ehlich, R. R. Hardy, Y. R. Zou, W. Müller, and K. Rajewsky. 1994. Early B-cell development in the mouse: insights from mutations introduced by gene targeting. Immunol. Rev. 137: 135-153. (Pubitemid 24117121)
4. Melchers, F., E. ten Boekel, T. Yamagami, J. Andersson, and A. Rolink. 1999. The roles of preB and B cell receptors in the stepwise allelic exclusion of mouse IgH and L chain gene loci. Semin. Immunol. 11: 307-317. (Pubitemid 29452868)
5. Burrows, P. D., R. P. Stephan, Y. H. Wang, K. Lassoued, Z. Zhang, and M. D. Cooper. 2002. The transient expression of pre-B cell receptors governs B cell development. Semin. Immunol. 14: 343-349. (Pubitemid 35015080)
6. Stoddart, A., H. E. Fleming, and C. J. Paige. 2000. The role of the preBCR, the interleukin-7 receptor, and homotypic interactions during B-cell development. Immunol. Rev. 175: 47-58. (Pubitemid 30427155)
7. Papavasiliou, F., Z. Misulovin, H. Suh, and M. C. Nussenzweig. 1995. The role of Ig beta in precursor B cell transition and allelic exclusion. Science 268: 408-411.
8. Nemazee, D. 2000. Receptor selection in B and T lymphocytes. Annu. Rev. Immunol. 18: 19-51. (Pubitemid 30365373)
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. (Pubitemid 23097389)
10. Tiegs, S. L., D. M. Russell, and D. Nemazee. 1993. Receptor editing in selfreactive bone marrow B cells. J. Exp. Med. 177: 1009-1020. (Pubitemid 23097390)
11. Nemazee, D., and M. Weigert. 2000. Revising B cell receptors. J. Exp. Med. 191: 1813-1817. (Pubitemid 30390345)
12. Jankovic, M., R. Casellas, N. Yannoutsos, H. Wardemann, and M. C. Nussenzweig. 2004. RAGs and regulation of autoantibodies. Annu. Rev. Immunol. 22: 485-501. (Pubitemid 38680431)
13. Melchers, F. 2005. The pre-B-cell receptor: selector of fitting immunoglobulin heavy chains for the B-cell repertoire. Nat. Rev. Immunol. 5: 578-584. (Pubitemid 40961335)
14. Monroe, J. G. 2006. ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat. Rev. Immunol. 6: 283-294.
15. Kouskoff, V., G. Lacaud, K. Pape, M. Retter, and D. Nemazee. 2000. B cell receptor expression level determines the fate of developing B lymphocytes: receptor editing versus selection. Proc. Natl. Acad. Sci. USA 97: 7435-7439. (Pubitemid 30431481)
16. Braun, U., K. Rajewsky, and R. Pelanda. 2000. Different sensitivity to receptor editing of B cells from mice hemizygous or homozygous for targeted Ig transgenes. Proc. Natl. Acad. Sci. USA 97: 7429-7434. (Pubitemid 30431480)
17. Keren, Z., E. Diamant, O. Ostrovsky, E. Bengal, and D. Melamed. 2004. Modification of ligand-independent B cell receptor tonic signals activates receptor editing in immature B lymphocytes. J. Biol. Chem. 279: 13418-13424. (Pubitemid 38468865)
18. Shivtiel, S., N. Leider, O. Sadeh, Z. Kraiem, and D. Melamed. 2002. Impaired light chain allelic exclusion and lack of positive selection in immature B cells expressing incompetent receptor deficient of CD19. J. Immunol. 168: 5596-5604. (Pubitemid 34556140)
19. Amin, R. H., and M. S. Schlissel. 2008. Foxo1 directly regulates the transcription of recombination-activating genes during B cell development. Nat. Immunol. 9: 613-622. (Pubitemid 351712632)
20. Herzog, S., E. Hug, S. Meixlsperger, J. H. Paik, R. A. DePinho, M. Reth, and H. Jumaa. 2008. SLP-65 regulates immunoglobulin light chain gene recombination through the PI(3)K-PKB-Foxo pathway. Nat. Immunol. 9: 623-631. (Pubitemid 351712633)
21. Schram, B. R., L. E. Tze, L. B. Ramsey, J. Liu, L. Najera, A. L. Vegoe, R. R. Hardy, K. L. Hippen, M. A. Farrar, and T. W. Behrens. 2008. B cell receptor basal signaling regulates antigen-induced Ig light chain rearrangements. J. Immunol. 180: 4728-4741.
22. Tze, L. E., B. R. Schram, K. P. Lam, K. A. Hogquist, K. L. Hippen, J. Liu, S. A. Shinton, K. L. Otipoby, P. R. Rodine, A. L. Vegoe, et al. 2005. Basal immunoglobulin signaling actively maintains developmental stage in immature B cells. PLoS Biol. 3: e82.
23. Aït-Azzouzene, D., P. Skog, M. Retter, V. Kouskoff, M. Hertz, J. Lang, J. Kench, M. Chumley, D. Melamed, J. Sudaria, et al. 2004. Tolerance-induced receptor selection: scope, sensitivity, locus specificity, and relationship to lymphocytepositive selection. Immunol. Rev. 197: 219-230. (Pubitemid 38142179)
24. Takeda, S., Y. R. Zou, H. Bluethmann, D. Kitamura, U. Muller, and K. Rajewsky. 1993. Deletion of the immunoglobulin kappa chain intron enhancer abolishes kappa chain gene rearrangement in cis but not lambda chain gene rearrangement in trans. EMBO J. 12: 2329-2336. (Pubitemid 23194183)
25. Zou, Y. R., S. Takeda, and K. Rajewsky. 1993. Gene targeting in the Ig kappa locus: efficient generation of lambda chain-expressing B cells, independent of gene rearrangements in Ig kappa. EMBO J. 12: 811-820. (Pubitemid 23095829)
26. Nakajima, P. B., J. P. Menetski, D. B. Roth, M. Gellert, and M. J. Bosma. 1995. V-D-J rearrangements at the T cell receptor delta locus in mouse thymocytes of the alpha beta lineage. Immunity 3: 609-621.
27. Kiefer, K., P. B. Nakajima, J. Oshinsky, S. H. Seeholzer, M. Radic, G. C. Bosma, and M. J. Bosma. 2008. Antigen receptor editing in anti-DNA transitional B cells deficient for surface IgM. J. Immunol. 180: 6094-6106.
28. Cadera, E. J., F. Wan, R. H. Amin, H. Nolla, M. J. Lenardo, and M. S. Schlissel. 2009. NF-kappaB activity marks cells engaged in receptor editing. J. Exp. Med. 206: 1803-1816.
29. Liu, X., S. Shen, and T. Manser. 2009. Influence of B cell antigen receptor expression level on pathways of B cell tolerance induction. J. Immunol. 182: 398-407.
30. Dickins, R. A., M. T. Hemann, J. T. Zilfou, D. R. Simpson, I. Ibarra, G. J. Hannon, and S. W. Lowe. 2005. Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat. Genet. 37: 1289-1295. (Pubitemid 41568715)
31. Pui, J. C., D. Allman, L. Xu, S. DeRocco, F. G. Karnell, S. Bakkour, J. Y. Lee, T. Kadesch, R. R. Hardy, J. C. Aster, and W. S. Pear. 1999. Notch1 expression inearly lymphopoiesis influences B versus T lineage determination. Immunity 11: 299-308. (Pubitemid 29463238)
32. Rao, S. P., K. A. Vora, and T. Manser. 2002. Differential expression of the inhibitory IgG Fc receptor FcgammaRIIB on germinal center cells: implications for selection of high-affinity B cells. J. Immunol. 169: 1859-1868. (Pubitemid 34857648)
33. Kusser, K. L., and T. D. Randall. 2003. Simultaneous detection of EGFP and cell surface markers by fluorescence microscopy in lymphoid tissues. J. Histochem. Cytochem. 51: 5-14. (Pubitemid 36133482)
34. 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.
35. Allman, D., R. C. Lindsley, W. DeMuth, K. Rudd, S. A. Shinton, and R. R. Hardy. 2001. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167: 6834-6840. (Pubitemid 33144175)
36. Hayakawa, K., R. R. Hardy, and L. A. Herzenberg. 1986. Peritoneal Ly-1 B cells: genetic control, autoantibody production, increased lambda light chain expression. Eur. J. Immunol. 16: 450-456. (Pubitemid 16104530)
37. Hayakawa, K., R. R. Hardy, L. A. Herzenberg, and L. A. Herzenberg. 1985. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 161: 1554-1568. (Pubitemid 15046047)
38. Imanishi-Kari, T., E. Rajnavölgyi, T. Takemori, R. S. Jack, and K. Rajewsky. 1979. The effect of light chain gene expression on the inheritance of an idiotype associated with primary anti-(4-hydroxy-3-nitrophenyl)acetyl(NP) antibodies. Eur. J. Immunol. 9: 324-331. (Pubitemid 9205198)
39. Rowland, S. L., C. L. DePersis, R. M. Torres, and R. Pelanda. 2010. Ras activation of Erk restores impaired tonic BCR signaling and rescues immature B cell differentiation. J. Exp. Med. 207: 607-621.
40. Notidis, E., L. Heltemes, and T. Manser. 2002. Dominant, hierarchical induction of peripheral tolerance during foreign antigen-driven B cell development. Immunity 17: 317-327. (Pubitemid 35279552)
41. Heltemes-Harris, L., X. Liu, and T. Manser. 2004. Progressive surface B cell antigen receptor down-regulation accompanies efficient development of antinuclear antigen B cells to mature, follicular phenotype. J. Immunol. 172: 823-833. (Pubitemid 38113738)
42. 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. (Pubitemid 29313091)
43. Chen, J., M. Trounstine, C. Kurahara, F. Young, C. C. Kuo, Y. Xu, J. F. Loring, F. W. Alt, and D. Huszar. 1993. B cell development in mice that lack one or both immunoglobulin kappa light chain genes. EMBO J. 12: 821-830. (Pubitemid 23095830)
44. Sanchez, P., B. Nadel, and P. A. Cazenave. 1991. V lambda-J lambda rearrangements are restricted within a V-J-C recombination unit in the mouse. Eur. J. Immunol. 21: 907-911.
45. 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: 1213-1225.