Surrogate light chain is required for central and peripheral B-cell tolerance and inhibits anti-DNA antibody production by marginal zone B cells

European Journal of Immunology

Volumn 45, Issue 4, 2015, Pages 1228-1237

  Ren, Weicheng ^a   Grimsholm, Ola ^a   Bernardi, Angelina I ^a   Höök, Nina ^a   Stern, Anna ^a   Cavallini, Nicola ^a   Mårtensson, Inga Lill ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Autoantibodies; Autoimmunity; Light chain recombination; Marginal zone B cells; Pre BCR

Indexed keywords

B CELL ACTIVATING FACTOR; DNA ANTIBODY; INTERLEUKIN 7 RECEPTOR; MESSENGER RNA; SURROGATE IMMUNOGLOBULIN LIGHT CHAIN; ANTINUCLEAR ANTIBODY; AUTOANTIBODY; B CELL ACTIVATING FACTOR RECEPTOR; HOMEODOMAIN PROTEIN; IMMUNOGLOBULIN M; IMMUNOGLOBULIN MU CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR; RAG-1 PROTEIN; TNFRSF13C PROTEIN, MOUSE; TNFSF13B PROTEIN, MOUSE;

ALLELE; ANIMAL CELL; ANTIBODY PRODUCTION; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE DEPLETION; MARGINAL ZONE B CELL; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; ANIMAL; BIOSYNTHESIS; BLOOD; C57BL MOUSE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; ANTIBODIES, ANTINUCLEAR; ANTIBODY FORMATION; APOPTOSIS; AUTOANTIBODIES; B-CELL ACTIVATING FACTOR; B-CELL ACTIVATION FACTOR RECEPTOR; B-LYMPHOCYTES; HOMEODOMAIN PROTEINS; IMMUNE TOLERANCE; IMMUNOGLOBULIN LIGHT CHAINS, SURROGATE; IMMUNOGLOBULIN M; IMMUNOGLOBULIN MU-CHAINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, B-CELL;

EID: 84927013252     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444917     Document Type: Article

References (47)

1. Goodnow, C. C., Sprent, J., Fazekas de St Groth, B. and Vinuesa, C. G., Cellular and genetic mechanisms of self tolerance and autoimmunity. Nature 2005. 435: 590-597.
2. Rajewsky, K., Clonal selection and learning in the antibody system. Nature 1996. 381: 751-758.
3. Nemazee, D., Receptor editing in lymphocyte development and central tolerance. Nat. Rev. Immunol. 2006. 6: 728-740.
4. Chen, C., Radic, M. Z., Erikson, J., Camper, S. A., Litwin, S., Hardy, R. R. and Weigert, M., Deletion and editing of B cells that express antibodies to DNA. J. Immunol. 1994. 152: 1970-1982.
5. Wardemann, H., Yurasov, S., Schaefer, A., Young, J. W., Meffre, E. and Nussenzweig, M. C., Predominant autoantibody production by early human B cell precursors. Science 2003. 301: 1374-1377.
6. Lindsley, R. C., Thomas, M., Srivastava, B. and Allman, D., Generation of peripheral B cells occurs via two spatially and temporally distinct pathways. Blood 2007. 109: 2521-2528.
7. Mackay, F. and Schneider, P., Cracking the BAFF code. Nat. Rev. Immunol. 2009. 9: 491-502.
8. Yurasov, S. and Nussenzweig, M. C., Regulation of autoreactive antibodies. Curr. Opin. Rheumatol. 2007. 19: 421-426.
9. Meffre, E. and Wardemann, H., B-cell tolerance checkpoints in health and autoimmunity. Curr. Opin. Immunol. 2008. 20: 632-638.
10. Panigrahi, A. K., Goodman, N. G., Eisenberg, R. A., Rickels, M. R., Naji, A. and Luning Prak, E. T., RS rearrangement frequency as a marker of receptor editing in lupus and type 1 diabetes. J. Exp. Med. 2008. 205: 2985-2994.
11. Hardy, R. R. and Hayakawa, K., B cell development pathways. Annu. Rev. Immunol. 2001. 19: 595-621.
12. Osmond, D. G., Rolink, A. and Melchers, F., Murine B lymphopoiesis: towards a unified model. Immunol. Today 1998. 19: 65-68.
13. Parker, M. J., Licence, S., Erlandsson, L., Galler, G. R., Chakalova, L., Osborne, C. S., Morgan, G. et al., The pre-B-cell receptor induces silencing of VpreB and lambda5 transcription. EMBO J. 2005. 24: 3895-3905.
14. Conley, M. E. and Burrows, P. D., Plugging the leaky pre-B cell receptor. J. Immunol. 2010. 184: 1127-1129.
15. Almqvist, N. and Martensson, I. L., The pre-B cell receptor selecting for or against autoreactivity. Scand. J. Immunol. 2012. 76: 256-262.
16. Vettermann, C. and Jack, H. M., The pre-B cell receptor: turning autoreactivity into self-defense. Trends Immunol. 2010. 31: 176-183.
17. von Boehmer, H. and Melchers, F., Checkpoints in lymphocyte development and autoimmune disease. Nat. Immunol. 2010. 11: 14-20.
18. Herzog, S. and Jumaa, H., Self-recognition and clonal selection: autoreactivity drives the generation of B cells. Curr. Opin. Immunol. 2012. 24: 166-172.
19. Tussiwand, R., Bosco, N., Ceredig, R. and Rolink, A. G., Tolerance checkpoints in B-cell development: Johnny B good. Eur. J. Immunol. 2009. 39: 2317-2324.
20. Melchers, F., The pre-B-cell receptor: selector of fitting immunoglobulin heavy chains for the B-cell repertoire. Nat. Rev. Immunol. 2005. 5: 578-584.
21. Minegishi, Y. and Conley, M. E., Negative selection at the pre-BCR checkpoint elicited by human mu heavy chains with unusual CDR3 regions. Immunity 2001. 14: 631-641.
22. Keenan, R. A., De Riva, A., Corleis, B., Hepburn, L., Licence, S., Winkler, T. H. and Martensson, I. L., Censoring of autoreactive B cell development by the pre-B cell receptor. Science 2008. 321: 696-699.
23. Xu, J. L. and Davis, M. M., Diversity in the CDR3 region of V(H) is sufficient for most antibody specificities. Immunity 2000. 13: 37-45.
24. Vale, A. M., Kapoor, P., Skibinski, G. A., Elgavish, A., Mahmoud, T. I., Zemlin, C., Zemlin, M. et al., The link between antibodies to OxLDL and natural protection against pneumococci depends on DH gene conservation. J. Exp. Med. 2013. 210: 875-890.
25. Almqvist, N., Winkler, T. H. and Martensson, I. L., Autoantibodies: focus on anti-DNA antibodies. Self Nonself 2011. 2: 11-18.
26. Galler, G. R., Mundt, C., Parker, M., Pelanda, R., Martensson, I. L. and Winkler, T. H., Surface mu heavy chain signals down-regulation of the V(D)J-recombinase machinery in the absence of surrogate light chain components. J. Exp. Med. 2004. 199: 1523-1532.
27. Shimizu, T., Mundt, C., Licence, S., Melchers, F. and Martensson, I. L., VpreB1/VpreB2/lambda 5 triple-deficient mice show impaired B cell development but functional allelic exclusion of the IgH locus. J. Immunol. 2002. 168: 6286-6293.
28. Vela, J. L., Ait-Azzouzene, D., Duong, B. H., Ota, T. and Nemazee, D., Rearrangement of mouse immunoglobulin kappa deleting element recombining sequence promotes immune tolerance and lambda B cell production. Immunity 2008. 28: 161-170.
29. Herzog, S., Reth, M. and Jumaa, H., Regulation of B-cell proliferation and differentiation by pre-B-cell receptor signalling. Nat. Rev. Immunol. 2009. 9: 195-205.
30. Clark, M. R., Mandal, M., Ochiai, K. and Singh, H., Orchestrating B cell lymphopoiesis through interplay of IL-7 receptor and pre-B cell receptor signalling. Nat. Rev. Immunol. 2014. 14: 69-80.
31. Engel, H., Rolink, A. and Weiss, S., B cells are programmed to activate kappa and lambda for rearrangement at consecutive developmental stages. Eur. J. Immunol. 1999. 29: 2167-2176.
32. Patton, D. T., Plumb, A. W. and Abraham, N., The survival and differentiation of pro-B and pre-B cells in the bone marrow is dependent on IL-7Ralpha Tyr449. J. Immunol. 2014. 193: 3446-3455.
33. Thien, M., Phan, T. G., Gardam, S., Amesbury, M., Basten, A., Mackay, F. and Brink, R., Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 2004. 20: 785-798.
34. Cancro, M. P., Signalling crosstalk in B cells: managing worth and need. Nat. Rev. Immunol. 2009. 9: 657-661.
35. Martin, F. and Kearney, J. F., Marginal-zone B cells. Nat. Rev. Immunol. 2002. 2: 323-335.
36. Lu, T. T. and Cyster, J. G., Integrin-mediated long-term B cell retention in the splenic marginal zone. Science 2002. 297: 409-412.
37. Derudder, E., Cadera, E. J., Vahl, J. C., Wang, J., Fox, C. J., Zha, S., van Loo, G. et al., Development of immunoglobulin lambda-chain-positive B cells, but not editing of immunoglobulin kappa-chain, depends on NF-kappaB signals. Nat. Immunol. 2009. 10: 647-654.
38. Monroe, R. J., Seidl, K. J., Gaertner, F., Han, S., Chen, F., Sekiguchi, J., Wang, J. et al., RAG2:GFP knockin mice reveal novel aspects of RAG2 expression in primary and peripheral lymphoid tissues. Immunity 1999. 11: 201-212.
39. Toda, T., Kitabatake, M., Igarashi, H. and Sakaguchi, N., The immature B-cell subpopulation with low RAG1 expression is increased in the autoimmune New Zealand Black mouse. Eur. J. Immunol. 2009. 39: 600-611.
40. Wang, J. H., Avitahl, N., Cariappa, A., Friedrich, C., Ikeda, T., Renold, A., Andrikopoulos, K. et al., Aiolos regulates B cell activation and maturation to effector state. Immunity 1998. 9: 543-553.
41. Jovelin, F., Mostoslavsky, G., Amoura, Z., Chabre, H., Gilbert, D., Eilat, D., Bach, J. F. et al., Early anti-nucleosome autoantibodies from a single MRL+/ +mouse: fine specificity, V gene structure and pathogenicity. Eur. J. Immunol. 1998. 28: 3411-3422.
42. Minegishi, Y., Coustan-Smith, E., Wang, Y. H., Cooper, M. D., Campana, D. and Conley, M. E., Mutations in the human lambda5/14.1 gene result in B cell deficiency and agammaglobulinemia. J. Exp. Med. 1998. 187: 71-77.
43. Yim, S. H., Chung, Y. J., Jin, E. H., Shim, S. C., Kim, J. Y., Kim, Y. S., Hu, H. J. et al., The potential role of VPREB1 gene copy number variation in susceptibility to rheumatoid arthritis. Mol. Immunol. 2011. 48: 1338-1343.
44. Specht, C. G. and Schoepfer, R., Deletion of the alpha-synuclein locus in a subpopulation of C57BL/6J inbred mice. BMC Neurosci. 2001. 2: 11.
45. Amu, S., Gjertsson, I. and Brisslert, M., Functional characterization of murine CD25 expressing B cells. Scand. J. Immunol. 2010. 71: 275-282.
46. Erlandsson, L., Licence, S., Gaspal, F., Lane, P., Corcoran, A. E. and Martensson, I. L., Both the pre-BCR and the IL-7Ralpha are essential for expansion at the pre-BII cell stage in vivo. Eur. J. Immunol. 2005. 35: 1969-1976.
47. Ren, W., Lagerstedt, K., Grimsholm, O., Stern, A., Sun, J. B., Fang, Y., Xiang, Z. et al., Uncoupling of natural IgE production and CD23 surface expression levels. PLoS One 2013. 8: e62851.