Control of immunoglobulin gene rearrangements in developing B cells

Current Opinion in Immunology

Volumn 9, Issue 2, 1997, Pages 233-238

  Papavasiliou, Fotini ^a   Jankovic, Mila ^a   Gong, Shiaoching ^a   Nussenzweig, Michel C ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE ANTIGEN; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN TYROSINE KINASE;

ALLELE; B LYMPHOCYTE; CELL MATURATION; GENE REARRANGEMENT; IMMUNOGLOBULIN GENE; LYMPHOCYTOPOIESIS; RECEPTOR GENE; REVIEW;

EID: 0030887997     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(97)80141-0     Document Type: Article

References (62)

1. Burnet FM. The Clonal Selection Theory of Acquired Immunity. 1959;The University Press, Cambridge, UK.
2. Talmage DW. Clonal selection theory. Science. 129:1959;1643-1648.
3. Tonegawa S. Somatic generation of antibody diversity. Nature. 302:1983;575-581.
4. Pemis BG, Chiappino G, Kelus AS, Gell PGH. Cellular localization of immunoglobulins with different allotype specificities in rabbit lymphoid tissue. J Exp Med. 122:1965;853-875.
5. Alt FW. Ordered rearrangement of immunoglobulin heavy chain variable region segments. EMBO J. 3:1984;1209-1219.
6. Rusconi S, Köhler G. Transmission and expression of a specific pair of rearranged immunoglobulin μ and κ genes in a transgenic mouse line. Nature. 314:1985;330-334.
7. Weaver D, Costantini F, Imanishi-Kari T, Baltimore D. A transgenic immunoglobulin mu gene prevents rearrangement of endogenous genes. Cell. 42:1985;117-127.
8. Kleinfield RR, Hardy RD, Tarligton J, Dangl A, Herzenberg L, Weigert M. Recombination between an expressed immunoglobulin heavy-chain gene and a germline variable gene segment in a Ly 1 + B-cell lymphoma. Nature. 322:1986;843-846.
9. Nussenzweig MC, Shaw AC, Sinn E, Danner DB, Holmes KL, Morse HC III, Leder P. Allelic exclusion in transgenic mice that express the membrane form of immunoglobulin μ Science. 236:1987;816-819.
10. Manz J, Denis K, Witte O, Brinster R, Storb U. Feedback inhibition of immunoglobulin gene rearrangement by membrane mu, but not by secreted mu heavy chains. J Exp Med. 168:1988;1363-1381. [Published erratum appears in J Exp Med 1989, 169:2269].
11. Costa T, Thais EF, Suh H, Nussenzweig MC. Chromosomal position of rearranging gene segments influences allelic exclusion in transgenic mice. Proc Natl Acad Sci USA. 89:1992;2205-2208.
12. Kitamura D, Roes J, Kuhn R, Rajewsky K. A B cell deficient mouse by targeted disruption of the membrane exons of the immunoglobulin μ chain gene. Nature. 350:1991;423-426.
13. Kitamura D, Rajewsky K. Targeted disruption of mu chain membrane exon causes loss of heavy-chain allelic exclusion. Nature. 356:1992;154-156.
14. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1 deficient mice have no mature B and T lymphocytes. Cell. 68:1992;869-877.
15. Shinkai Y, Rathbun G, Lam K-P, Oltz EM, Stewart V, Mendelsohn M, Charron J, Datta M, Young F, Stall AM, Alt FW. RAG-2 deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell. 68:1992;855-867.
16. Spanopoulou E, Roman CAJ, Corcoran LM, Schlissel MS, Silver DP, Nemazee D, Nussenzweig MC, Shinton SA, Hardy RR, Baltimore D. Functional immunoglobulin transgenes guide ordered B-cell differentiation in Rag-1-deficient mice. Genes Dev. 8:1992;1030-1042.
17. Young F, Ardman B, Shinkai Y, Lansford R, Blackwell TK, Mendelsohn M, Rolink A, Melchers F, Alt FW. Influence of immunoglobulin heavy- and light-chain expression on B-cell differentiation. Genes Dev. 8:1994;1043-1057.
18. Reth M. Antigen receptors on B lymphocytes. Annu Rev Immunol. 10:1992;97-121.
19. Pillai S, Baltimore D. Formation of disulfide-linked μ2ω2 tetramers in pre-B cells by the 18k ω-immunoglobulin light chain. Nature. 329:1987;172-174.
20. Karasuyama H, Kudo A, Melchers F. The proteins encoded by the VpreB and λ5 pre-B cell-specific genes can associate with each other and with mu heavy chain. J Exp Med. 172:1992;969-972.
21. Sakaguchi N, Melchers F. Lambda5, a new light-chain-related locus selectively expressed in pre-B lymphocytes. Nature. 324:1986;579-582.
22. Rolink A, Karasuyama H, Haasner D, Grawunder U, Martensson I-L, Kudo A, Melchers F. Two pathways of B-lymphocyte development in mouse bone marrow and the roles of surrogate L chain in this development. Immunol Rev. 137:1994;185-201.
23. Kitamura D, Kudo A, Schaal S, Muller W, Melchers F, Rajewsky K. A critical role of lambda 5 protein in B cell development. Cell. 69:1992;823-831.
24. Rolink A, Karasuyama H, Grawunder U, Haasner D, Kudo A, Melchers F. B cell development in mice with a defective lambda 5 gene. Eur J Immunol. 23:1993;1284-1288.
25. Ehlich A, Schaal S, Gu H, Kitamura D, Muller W, Rajewsky K. Ig heavy and light chain genes rearrange independently at early stages of B cell development. Cell. 72:1993;695-704.
26. Takeda S, Zou YR, Bluethmann H, Kitamura D, Muller W, Rajewsky K. Deletion of the immunoglobulin κ chain intron enhancer abolishes κ chain gene rearrangement in cis but not λ chain gene rearrangement in trans. EMBO J. 12:1993;2329-2336.
27. Pelanda R, Schaal S, Torres RM, Rajewsky K. Prematurely expressed Ig transgene, but not a VJ gene segment targeted into the Ig locus, can rescue B cell development in lamda 5-deficient mice. Immunity. 5:1996;229-239.
28. Papavasiliou F, Jankovic M, Nussenzweig MC. Surrogate or conventional light chains are required for membrane immunoglobulin mu to activate the precursor B cell transition. J Exp Med. 184:1996;2025-2029.
29. Löffert D, Ehlich A, Muller W, Rajewsky K. Surrogate light chain expression is required to establish immunoglobulin heavy chain allelic exclusion during early B cell development. Immunity. 4:1996;133-144.
30. Morrison S, Scharff MD. A mouse myeloma variant with a defect in light chain synthesis. Eur J Immunol. 9:1979;461-465.
31. Sonenshein GE, Siekevitz M, Siebert GR, Gefter ML. Control of immunoglobulin secretion in the murine plasmacytoma line MOPC. J Exp Med. 148:1978;301-312.
32. Corcos D, Dunda O, Butor C, Cesbron JY, Lores P, Bucchini D, Jami J. Pre-B-cell development in the absence of λ5 in transgenic mice expressing a heavy-chain disease protein. Curr Biol. 5:1995;1140-1148.
33. Hombach J, Leclercq L, Radbruch A, Rajewsky K, Reth M. A novel 34-kd protein co-isolated with the IgM molecule in surface IgM-expressing cells. EMBO J. 7:1988;3451-3456.
34. Hermanson GG, Eisenberg D, Kincade PW, Wall R. B29: a member of the immunoglobulin gene superfamily exclusively expressed on B-lineage cells. Proc Natl Acad Sci USA. 85:1988;6890-6894.
35. Sakaguchi N, Kashiwamura S, Kimoto M, Thalmann P, Melchers F. B lymphocyte lineage-restricted expression of mb-1, a gene with CD3-like structural properties. EMBO J. 7:1988;3457-3464.
36. Gold MR, Law DA, DeFranco AL. Stimulation of protein tyrosine phosphorylation by the B-lymphocyte antigen receptor. Nature. 345:1990;810-813.
37. Campbell MA, Sefton BM. Protein tyrosine phosphorylation is induced in murine B lymphocytes in response to stimulation with anti-immunoglobulin. EMBO J. 9:1990;2125-2131.
38. Sanchez M, Misulovin Z, Burkhardt AL, Mahajan S, Costa T, Franke R, Bolen JB, Nussenzweig MC. Signal transduction by Ig is mediated through Igα and Igβ J Exp Med. 178:1993;1049-1056.
39. Kim K, Alber G, Weiser P, Reth M. Differential signaling through the Igα and Igβ components of the B cell antigen receptor. Eur J Immunol. 23:1993;911-916.
40. Clark MR, Campbell KS, Kazlauskas A, Johnson SA, Hertz M, Potter TA, Pleiman C, Cambier JC. The B cell antigen receptor complex: association of Ig-alpha and Ig-beta with distinct cytoplasmic effectors. Science. 258:1992;123-126.
41. Grupp SA, Campbell K, Mitchell RN, Cambier JC, Abbas AK. Signaling-defective mutants of the B lymphocyte antigen receptor fail to associate with Ig-alpha and Ig-beta/gamma. J Biol Chem. 268:1993;25776-25779.
42. of special interest Papavasiliou F, Misulovin Z, Suh H, Nussenzweig MC. The role of Igβ in precursor B cell transition and allelic exclusion. Science. 268:1995;408-411 The association between mIgμ and Igα and Igβ is shown to be essential for inducing the pro- to pre-B cell transition as well as allelic exclusion in transgenic mice. Chimeric receptors composed of mIgμ and the Igβ cytoplasmic domain is shown to be sufficient for induction of these early events by a mechanism that requires conserved tyrosine residues in the Igβ protein.
43. Papavasiliou F, Jankovic M, Suh H, Nussenzweig MC. The cytoplasmic domains of immunoglobulin (Ig) alpha and Ig beta can independently induce the precursor B cell transition and allelic exclusion. J Exp Med. 182:1995;1389-1394.
44. Reth M. Antigen receptor tail clue [letter]. Nature. 338:1989;383-384.
45. Metzger H. Transmembrane signaling: the joy of aggregation. J Immunol. 149:1992;1477-1487.
46. of special interest Torres RM, Flaswinkel H, Reth M, Rajewsky K. Aberrant B cell development and immune response in mice with a compromised BCR complex. Science. 272:1996;1804-1808 Gene knockout experiments, in which the final 40 amino acids of the Igα cytoplasmic domain were deleted, are described. This truncated molecule allows assembly of pre-BCR and BCR that are able to signal for the pre-B cell transition and allelic exclusion with only a small decrease in efficiency as compared with wild-type mice. Surprisingly, there are very few B cells in the periphery of these mice, indicating a developmental arrest at the point where B cells exit the bone marrow.
47. of special interest Gong S, Nussenzweig MC. Regulation of an early developmental checkpoint in the B cell pathway by Ig beta. Science. 272:1996;411-414 Analysis of mice lacking Igβ revealed that B cell development depends on this signaling molecule not only in the context of pre-BCR and BCR signaling, but also at an earlier stage that controls the completion of V to (D)J heavy chain rearrangements. Thus, the results introduce a novel checkpoint in the course of B cell development.
48. Gong S, Sanchez M, Nussenzweig MC. Counterselection against Dμ is mediated through Igα-Igβ J Exp Med. 184:1996;2079-2084.
49. Ehlich A, Martin V, Muller W, Rajewsky K. Analysis of the B-cell progenitor compartment at the level of single cells. Curr Biol. 4:1994;573-583.
50. Ichihara Y, Hayashida H, Miyazawa S, Kurosawa Y. Only DFL16, DSP2, and DQ52 gene families exist in mouse immunoglobulin heavy chain diversity gene loci, of which DFL16 and DSP2 originate from the same primordial DH gene. Eur J Immunol. 19:1989;1849-1854.
51. Lyons DS, Lieberman SA, Hampl J, Boniface JJ, Chi Y-H, Berg LJ, Davis MM. A TCR binds to antagonist ligands with lower affinities and faster dissociation rates than to agonists. Immunity. 5:1996;53-61.
52. Satterwaite A, Witte O. Genetic analysis of tyrosine kinase function in B cell development. Annu Rev Immunol. 14:1996;131-154.
53. Takata M, Sabe H, Hata A, Inazu T, Homma Y, Nukada T, Yamamura H, Kurosaki T. Tyrosine kinases Lyn and Syk regulate B cell receptor-coupled Ca2+ mobilization through distinct pathways. EMBO J. 13:1994;1341-1349.
54. Kurosaki T, Takata M, Yamanashi Y, Inazu T, Taniguchi T, Yamamoto T, Yamamura H. Syk activation by the Src-family tyrosine kinase in the B cell receptor. J Exp Med. 179:1994;1725-1729.
55. Cheng AM, Rowley B, Pao W, Hayday A, Bolen JB, Pawson T. Syk tyrosine kinase required for mouse viability and B-cell development. Nature. 378:1995;303-306.
56. Turner M, Mee PJ, Costello PS, Williams O, Price AA, Duddy LP, Furlong MT, Geahlen RL, Tybulewicz VL. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature. 378:1995;298-302.
57. of outstanding interest Van Gent DC, McBlane J, Ramsden D, Sadofsky M, Hesse J, Gellert M. Initiation of VDJ recombination in a cell free system. Cell. 81:1995;925-934 This paper offers a major contribution to our understanding of the mechanism of V(D)J recombination. B cell extracts were shown to carry out specific cleavage of DNA in vitro, giving rise to the same reaction products that were previously found in vivo. Cleavage activity correlates with the presence of the RAG-2 protein, suggesting that RAG-1 and RAG-2 are components of the VDJ recombinase.
58. Van Gent DC, Mizuuchi K, Gellert M. Similarities between initiation of VDJ recombination and retroviral integration. Science. 271:1996;1592-1594.
59. Li Z, Otevrel T, Gao Y, Cheng HL, Seed B, Stamato TD, Taccioli GE, Alt FW. The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination. Cell. 83:1995;1079-1089.
60. Bogue M, Roth DB. Mechanism of V(D)J recombination. Curr Opin Immunol. 8:1996;175-180.
61. Sleckman BP, Alt FW, Gorman JR. Accessibility control of antigen-receptor variable-region gene assembly: role of cis-acting element. Annu Rev Immunol. 14:1996;459-482.
62. of special interest Stanhope-Baker P, Hudson K, Schaffer A, Constantinescu A, Schlissel M. Cell type specific chromatin structure determines the targeting of VDJ recombinase activity in vitro. Cell. 85:1996;887-897 Recombinase cleavage of Ig and TCR gene segments in nuclei was analyzed in vitro. The accessibility of the target sequences was found to regulate strict lineage specificity as well as the order of gene rearrangements.