Unexpected rearrangement and expression of the immunoglobulin λ1 locus in scid mice

Journal of Experimental Medicine

Volumn 191, Issue 11, 2000, Pages 1933-1943

  Ruetsch, Norman R ^a   Bosma, Gayle C ^a   Bosma, Melvin J ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

B cell differentiation; P additions; Premature Ig recombination; Pro B cells; VJ junctional diversity

Indexed keywords

IMMUNOGLOBULIN; PALINDROMIC DNA;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; B-LYMPHOCYTES; BONE MARROW CELLS; FEMALE; GENE EXPRESSION; GENE REARRANGEMENT, B-LYMPHOCYTE, LIGHT CHAIN; HEMATOPOIETIC STEM CELLS; IMMUNOGLOBULIN JOINING REGION; IMMUNOGLOBULIN LAMBDA-CHAINS; IMMUNOGLOBULIN VARIABLE REGION; MALE; MICE; MICE, KNOCKOUT; MICE, SCID; PROTO-ONCOGENE PROTEINS C-BCL-2; SEQUENCE DELETION; SPLEEN;

EID: 0034608714     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.11.1933     Document Type: Article

References (70)

1. Yancopoulos, G.D., and F.W. Alt. 1986. Regulation of the assembly and expression of variable-region genes. Annu. Rev. Immunol. 4:339-368.
2. Gorman, J.R., and F.W. Alt. 1998. Regulation of immunoglobulin light chain isotype expression. Adv. Immunol. 69: 113-181.
3. Alt, F.W., G.D. Yancopoulos, T.K. Blackwell, C. Wood, E. Thomas, M. Boss, R. Coffman, N. Rosenberg, S. Tonegawa, and D. Baltimore. 1984. Ordered rearrangement of immunoglobulin heavy chain variable region segments. EMBO (Eur. Mol. Biol. Organ.) J. 3:1209-1219.
4. Hardy, R.R., C.E. Carmack, S.A. Shinton, J.D. Kemp, and K. Hayakawa. 1991. Resolution and characterization of proB and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173:1213-1225.
5. Ehlich, A., S. Schaal, H. Gu, D. Kitamura, W. Muller, and K. Rajewsky. 1993. Immunoglobulin heavy and light chain genes rearrange independently at early stages of B cell development. Cell. 72:695-704.
6. Li, Y.-S., K. Hayakawa, and R.R. Hardy. 1993. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J. Exp. Med. 178:951-960.
7. Alt, F.W., V. Enea, A.L.M. Bothwell, and D. Baltimore. 1980. Activity of multiple light chain genes in murine myeloma cells producing a single functional light chain. Cell. 21: 1-12.
8. Hieter, P., S. Korsmeyer, T. Waldman, and P. Leder. 1981. Human immunoglobulin κ light-chain genes are deleted or rearranged in λ-producing cells. Nature. 290:368-372.
9. Korsmeyer, S.I., P.A. Hieter, S.O. Sharrow, C.K. Goldman, P. Leder, and T.A. Waldman. 1982. Normal human B cells display ordered light chain gene rearrangement and deletions. J. Exp. Med. 156:975-985.
10. Engel, H., A. Rolink, and S. Weiss. 1999. B cells are programmed to activate κ and λ for rearrangement at consecutive developmental stages. Eur. J. Immunol. 29:2167-2176.
11. Coleclough, C., R.P. Perry, K. Karjalainen, and M. Weigert. 1981. Aberrant rearrangements contribute significantly to the allelic exclusion of immunoglobulin gene expression. Nature. 290:372-378.
12. Ramsden, D.A., and G.E. Wu. 1991. Mouse κ light-chain recombination signal sequences mediate recombination more frequently than do those of λ light chain. Proc. Natl. Acad. Sci. USA. 88:10721-10725.
13. Liu, D., J. Jenab, and N. Rosenberg. 1997. κ and λ rearrangement occur simultaneously in transformed pre-B cells. J. Immunol. 159:6061-6069.
14. Kubagawa, H., M.D. Cooper, A.J. Carroll, and P.D. Burrows. 1989. Light-chain gene expression before heavy-chain gene rearrangement in pre-B cells transformed by Epstein-Barr virus. Proc. Natl. Acad. Sci. USA. 86:2356-2360.
15. Schlissel, M.S., and D. Baltimore. 1989. Activation of immunoglobulin kappa gene rearrangement correlates with induction of germline kappa gene transcription. Cell. 58:1001-1007.
16. Felsher, D.W., D.T. Ando, and J. Braun. 1991. Independent rearrangement of Igλ genes in tissue culture-derived murine B cell lines. Int. Immunol. 3:711-718.
17. 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 κ light chain genes. EMBO (Eur. Mol. Biol. Organ.) J. 12: 821-830.
18. Zou, Y.-R., S. Takeda, and K. Rajewsky. 1993. Gene targeting in the Igκ locus: efficient generation of chain-expressing B cells, independent of gene rearrangements in Igκ. EMBO (Eur. Mol. Biol. Organ.) J. 12:811-820.
19. Hardy, R.R., J.L. Dangl, K. Hayakawa, G. Jager, L. Herzenberg, and L.A. Herzenberg. 1986. Frequent lambda light chain gene rearrangement and expression in a Ly-1 B lymphoma with a productive kappa chain allele. Proc. Natl. Acad. Sci. USA. 83:1438-1442.
20. Berg, J., M. McDowell, H.-M. Jack, and M. Wabl. 1990. Immunoglobulin λ gene rearrangement can precede κ gene rearrangement. Dev. Immunol. 1:53-57.
21. Tang, J.-Q., M.C. Bene, and G.C. Faure. 1991. Alternative rearrangements of immunoglobulin light chain genes in human leukemia. Leukemia. 5:651-656.
22. Gollahon, K.A., J. Hagman, R.L. Brinster, and U. Storb. 1988. Ig λ-producing B cells do not show feedback inhibition of gene rearrangement. J. Immunol. 141:2771-2780.
23. Coleclough, C. 1983. Chance, necessity and antibody gene dynamics. Nature. 303:23-26.
24. Chen, J., M. Trounstine, F.W. Alt, F. Young, C. Kurahara, J.F. Loring, and D. Huszar. 1993. Immunoglobulin gene rearrangement in B cell deficient mice generated by targeted deletion of the JH locus. Int. Immunol. 5:647-656.
25. Fulop, G.M., and R.A. Phillips. 1990. The scid mutation in mice causes a general defect in DNA repair. Nature. 347:479-482.
26. Hendrickson, E.A., X.-Q. Qin, E.A. Bump, D.G. Schatz, M. Oettinger, and D.T. Weaver. 1991. A link between double-strand break-related and V(D)J recombination: the scid mutation. Proc. Natl. Acad. Sci. USA. 88:4061-4065.
27. Biedermann, K.A., J. Sun, A.J. Giaccia, L.M. Tosto, and M. Brown. 1991. Scid mutation in mice confers hypersensitivity to ionizing radiation and a deficiency in DNA double-strand break repair. Proc. Natl. Acad. Sci. USA. 88:1394-1397.
28. Kirchgessner, C.U., C.K. Patil, J.W. Evans, C.A. Cuomo, L.M. Fried, T. Carter, M. Oettinger, and M.J. Brown. 1995. DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science. 267:1178-1182.
29. Blunt, T., D. Gell, M. Fox, G.E. Taccioli, A.R. Lehmann, S.P. Jackson, and P.A. Jeggo. 1996. Identification of a nonsense mutation in the carboxyl-terminal region of DNA-dependent protein kinase catalytic subunit in the seid mouse. Proc. Natl. Acad. Sci. USA. 93:10285-10290.
30. Danska, J., D.P. Holland, S. Mariathasan, K.M. Williams, and C.J. Guidos. 1996. Biochemical and genetic defects in the DNA-dependent protein kinase in murine scid lymphocytes. Mol. Cell. Biol. 16:5507-5517.
31. Schuler, W., I.J. Weiler, A. Schuler, R.A. Phillips, N. Rosenberg, T.W. Mak, J.F. Kearney, R.P. Perry, and M.J. Bosma. 1986. Rearrangement of antigen receptor genes is defective in mice with severe combined immune deficiency. Cell. 46:963-972.
32. Lieber, M.R., J.E. Hesse, S. Lewis, G.C. Bosnia, M.J. Bosma, and M. Gellert. 1988. The defect in murine severe combined immune deficiency: joining of signal segments but not coding segments in V(D)J recombination. Cell. 55:7-16.
33. Malynn, B.A., T.K. Blackwell, G.M. Fulop, G.A. Rathburn, A.J.W. Furley, P. Ferrier, L.B. Heinke, R.A. Phillips, G.D. Yancopoulos, and F.W. Alt. 1988. The scid defect affects the final step of the immunoglobulin VDJ recombinase mechanism. Cell. 54:453-460.
34. Blackwell, T.K., B.A. Malynn, R.R. Pollock, P. Ferrier, L.R. Covey, G.M. Fulop, R.A. Phillips, G.D. Yancopoulos, and F.W. Alt. 1989. Isolation of scid pre-B cells that rearrange kappa light chain genes: formation of normal signal and abnormal coding joins. EMBO (Eur. Mol. Biol. Organ.) J. 8:735-742.
35. McCormack, W.T., L.W. Tjoelker, L.M. Carlson, B. Petryniak, C.F. Barth, E.H. Humphries, and C.B. Thompson. 1989. Chicken IgL gene rearrangement involves deletion of a circular episome and addition of single nonrandom nucleotides to both coding segments. Cell. 56:785-791.
36. Lafaille, J.J., A. De Cloux, M. Bonneville, Y. Takagaki, and S. Tonegawa. 1989. Junctional sequences of T cell receptor γδ genes: implications for γδ T cell lineages and for a novel intermediate of V-D-J joining. Cell. 59:859-870.
37. Lieber, M.R. 1991. Site-specific recombination in the immune system. FASEB J. 5:2934-2944.
38. Roth, D.B., J.P. Menetski, P.B. Nakajima, M.J. Bosma, and M. Gellert. 1992. V(D)J recombination: broken DNA molecules with covalently sealed (hairpin) coding ends in scid mouse thymocytes. Cell. 70:983-991.
39. van Gent, D.C., J.F. McBlane, D.A. Ramsden, M.J. Sadofsky, J.E. Hesse, and M. Gellert. 1995. Initiation of V(D)J recombination in a cell-free system. Cell 81:925-934.
40. Ramsden, D.A., and M. Gellert. 1995. Formation and resolution of double-strand break intermediates in V(D)J rearrangement. Genes Dev. 9:2409-2420.
41. Bosma, G.C., R.P. Custer, and M.J. Bosma. 1983. A severe combined immunodeficiency mutation in the mouse. Nature. 30:527-530.
42. Strasser, A., A.W. Harris, L.M. Corcoran, and S. Cory. 1994. Bcl-2 expression promotes B-but not T-lymphoid development in scid mice. Nature. 368:457-460.
43. Drews, R., W.N. Drohan, and H. Lubon. 1994. Transgene detection in mouse tail digests. Biotechniques. 17:866-867.
44. Strasser, A., A.W. Harris, D.C.S. Huang, P.H. Krammer, and S. Cory. 1995. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO (Eur. Mol. Biol. Organ.) J. 14:6136-6147.
45. Mombaerts, P., J. Iacomini, R.S. Johnson, K. Herrup, S. Tonegawa, and V.E. Papaioannou. 1992. RAG-1 deficient mice have no mature B and T lymphocytes. Cell. 68:869-877.
46. Chang, Y., G.C. Bosma, and M.J. Bosma. 1995. Development of B cells in scid mice with immunoglobulin transgenes: implications for the control of V(D)J recombination. Immunity. 2:607-616.
47. Sakano, H., Y. Kurosawa, M. Weigert, and S. Tonegawa. 1981. Identification and nucleotide sequence of a diversity DNA segment (D) of immunoglobulin heavy chain genes. Nature. 290:562-565.
48. Marcu, K.B., J. Banerji, N.A. Penncavage, R. Lang, and N. Arnheim. 1980. 5′ flanking region of immunoglobulin heavy chain constant region genes displays length heterogeneity in germlines of inbred mouse strains. Cell. 22:187-196.
49. Pennycook, J.L., Y. Chang, J. Celler, R.A. Phillips, and G.E. Wu. 1993. High frequency of normal DJH joints in B cell progenitors in severe combined immunodeficiency mice. J. Exp. Med. 178:1007-1016.
50. Araki, R., M. Itoh, K. Hamatani, and M. Abe. 1996. Normal D-JH rearranged products of the Ig H gene in SCID mouse bone marrow. Int. Immunol. 8:1045-1053.
51. Chang, Y., C.J. Paige, and G.E. Wu. 1992. Enumeration and characterization of DJH structures in mouse fetal liver. EMBO (Eur. Mol. Biol. Organ.) J. 11:1891-1899.
52. Schlissel, M.S., and T. Morrow. 1994. Ig heavy chain protein controls B cell development by regulating gem-line transcription and retargeting V(D)J recombination. J. Immunol. 153:1645-1657.
53. Bosma, G.C., Y. Chang, H. Karasuyama, and M.J. Bosma. 1999. Differential effect of an Ig μ transgene on development of pre-B cells in fetal and adult scid mice. Proc. Natl. Acad. Sci. USA. 96:11952-11957.
54. Gilfillan, S., A. Dierich, M. Lemeur, C. Benoist, and D. Mathis. 1993. Mice lacking TdT: mature animals with an immature lymphocyte repertoire. Science. 261:1175-1178.
55. Komori, T., A. Okada, V. Stewart, and F.W. Alt. 1993. Lack of N regions in antigen receptor variable region genes of TdT-deficient lymphocytes. Science. 261:1171-1175.
56. Wasserman, R., Y.-S. Li, and R.R. Hardy. 1997. Down-regulation of terminal deoxynucleotidyl transferase by Ig heavy chain in B lineage cells. J. Immunol. 158:1133-1138.
57. Boudinot, P., A.M. Drapier, P.A. Cazenave, and P. Sanchez. 1994. Mechanistic and selective constraints act on the establishment of V lambda J lambda junctions in the B cell repertoire. J. Immunol. 152:2248-2255.
58. Boudinot, P., D. Rueff-Juy, A.M. Drapier, P.A. Cazenave, and P. Sanchez. 1995. Various V-J rearrangement efficiencies shape the mouse lambda B cell repertoire. Eur. J. Immunol. 25:2499-2505.
59. Young, F., E. Mizoguchi, A.K. Bhan, and F.W. Alt. 1997. Constitutive bcl-2 expression during immunoglobulin heavy chain-promoted B cell differentiation expands novel precursor B cells. Immunity. 6:23-33.
60. Chang, Y., and M.J. Bosma. 1997. Effect of different Ig transgenes on B cell differentiation in scid mice. Int. Immunol. 9:373-380.
61. Meier, J.T., and S.M. Lewis. 1993. P nucleotides in V(D)J recombination: a fine-structure analysis. Mol. Cell. Biol. 13: 1078-1092.
62. Schuler, W., N.R. Ruetsch, M. Amsler, and M.J. Bosma. 1991. Coding joint formation of endogenous T cell receptor genes in lymphoid cells from scid mice: unusual P-nucleotide additions in VJ-coding joints. Eur. J. Immunol. 21:589-596.
63. Kienker, L.J., W.A. Kuziel, and P.W. Tucker. 1991. T cell receptor γ and δ gene junctional sequences in SCID mice: excessive P nucleotide insertion. J. Exp. Med. 174:769-773.
64. Lewis, S.M., and J.E. Hesse. 1991. Cutting and closing without recombination in V(D)J joining. EMBO (Eur. Mol. Biol. Organ.) J. 10:3631-3639.
65. Reth, M. 1992. Antigen receptors on B lymphocytes. Annu. Rev. Immunol. 10:97-121.
66. Cambier, J.C., C.M. Pleiman, and M.R. Clark. 1994. Signal transduction by the B cell antigen receptor and its coreceptors. Annu. Rev. Immunol. 12:457-186.
67. Horne, M.C., P.E. Roth, and A.L. DeFranco. 1996. Assembly of truncated immunoglobulin heavy chain Dμ into antigen receptor-like complexes in pre-B cells but not in B cells. Immunity. 4:145-158.
68. Tsubata, T., R. Tsubata, and M. Reth. 1991. Cell surface expression of the short immunoglobulin μ chain (Dμ protein) in murine pre-B cells is differently regulated from that of the intact μ chain. Eur. J. Immunol. 21:1359-1363.
69. Karasuyama, H., A. Rolink, and F. Melchers. 1993. A complex of glycoproteins is associated with VpreB/λ5 surrogate light chain on the surface of μ heavy chain-negative early precursor B cell lines. J. Exp. Med. 178:469-478.
70. Melchers, F., H. Karasuyama, D. Haasner, S. Bauer, A. Kudo, N. Sakaguchi, B. Jameson, and A. Rolink. 1993. The surrogate light chain in B-cell development. Immunol. Today. 14:60-68.