V(D)J recombination of chromosomally integrated, wild-type deletional and inversional substrates occur at similar frequencies with no preference for orientation

Immunology Letters

Volumn 97, Issue 1, 2005, Pages 69-80

  Shuh, Maureen ^a   Hixson, Douglas C ^b  

^a LOYOLA UNIVERSITY   (United States)

^b RHODE ISLAND HOSPITAL   (United States)

Author keywords

Recombination; scid; V(D)J

Indexed keywords

RECOMBINASE;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CHROMOSOME ANALYSIS; CONTROLLED STUDY; EMBRYO; GENE CONSTRUCT; GENE DELETION; GENE SEQUENCE; GENETIC RECOMBINATION; MOUSE; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; BASE SEQUENCE; GENE REARRANGEMENT; IMMUNOGLOBULINS; MICE; MICE, SCID; MOLECULAR SEQUENCE DATA; MUTATION; POLYMERASE CHAIN REACTION;

EID: 11144336532     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2004.09.016     Document Type: Article

References (95)

1. S. Tonegawa Somatic generation of antibody diversity Nature 302 1983 575 581
2. Y.H. Chien, Gascoigne NRJ, J. Kavaler, N.E. Lee, and M.M. Davis Somatic recombination in a murine T-cell receptor gene Nature 309 1984 322 326
3. S.M. Lewis The mechanism of V(D)J joining: lessons from molecular, immunological, and comparative analyses Adv Immunol 56 1994 27 150
4. M.R. Lieber, C.P. Chang, M. Gallo, G. Gauss, R. Gerstein, and A. Islas The mechanism of V(D)J recombination: site-specificity, reaction fidelity and immunologic diversity Semin Immunol 6 1994 143 153
5. S.D. Fugmann, A.I. Lee, P.E. Shockett, I.J. Villey, and D.G. Schatz The RAG proteins and V(D)J recombination: complexes, ends, and transposition Annu Rev Immunol 18 2000 495 527
6. M. Gellert V(D)J recombination: RAG proteins, repair factors, and regulation Annu Rev Biochem 71 2002 101 132
7. H. Sakano, K. Huppi, G. Heinrich, and S. Tonegawa Sequences at the somatic recombination sites of immunoglobulin light-chain genes Nature 280 1979 288 294
8. E.E. Max, J.G. Seidman, and P. Leder Sequences of five potential recombination sites encoded close to an immunoglobulin kappa constant region gene Proc Natl Acad Sci U S A 76 1979 3450 3454
9. H. Sakano, R. Maki, Y. Kurosawa, W. Roeder, and S. Tonegawa Two types of somatic recombination are necessary for the generation of complete immunoglobulin heavy-chain genes Nature 286 1980 676 683
10. P. Early, H. Huang, M. Davis, K. Calame, and L. Hood An immunoglobulin heavy chain variable region gene is generated from three segments of DNA: VH, D and JH Cell 19 1980 981 992
11. G.D. Yancopoulos, and F.W. Alt Regulation of the assembly and expression of variable-region genes Annu Rev Immunol 4 1986 339 368
12. D. Jung, and F.W. Alt Unraveling V(D)J recombination; insights into gene regulation Cell 116 2004 299 311
13. C.H. Bassing, W. Swat, and F.W. Alt The mechanism and regulation of chromosomal V(D)J recombination Cell 109 Suppl. 2002 S45 S55
14. M.S. Krangel Gene segment selection in V(D)J recombination: accessibility and beyond Nat Immunol 4 2003 624 630
15. J.F. McBlane, D.C. van Gent, D.A. Ramsden, C. Romeo, C.A. Cuomo, M. Gellert, and M.A. Oettinger Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps Cell 83 1995 387 395
16. D.C. van Gent, J.F. McBlane, D.A. Ramsden, M.J. Sadofsky, J.E. Hesse, and M. Gellert Initiation of V(D)J recombination in a cell-free system Cell 81 1995 925 934
17. D.C. van Gent, D.A. Ramsden, and M. Gellert The RAG1 and RAG2 proteins establish the 12/23 rule in V(D)J recombination Cell 85 1996 107 113
18. C.A. Cuomo, C.L. Mundy, and M.A. Oettinger DNA sequence and structure requirements for cleavage of V(D)J recombination signal sequences Mol Cell Biol 16 1996 5683 5690
19. D.A. Ramsden, J.F. McBlane, D.C. van Gent, and M. Gellert Distinct DNA sequence and structure requirements for the two steps of V(D)J recombination signal cleavage Embo J 15 1996 3197 3206
20. K. Hiom, and M. Gellert A stable RAG1-RAG2-DNA complex that is active in V(D)J cleavage Cell 88 1997 65 72
21. D.J. Sawchuk, F. Weis-Garcia, S. Malik, E. Besmer, M. Bustin, M.C. Nussenzweig, and P. Cortes V(D)J recombination: modulation of RAG1 and RAG2 cleavage activity on 12/23 substrates by whole cell extract and DNA-bending proteins J Exp Med 185 1997 2025 2032
22. M.J. Difilippantonio, C.J. McMahan, Q.M. Eastman, E. Spanopoulou, and D.G. Schatz RAG1 mediates signal sequence recognition and recruitment of RAG2 in V(D)J recombination Cell 87 1996 253 262
23. E. Spanopoulou, F. Zaitseva, F.H. Wang, S. Santagata, D. Baltimore, and G. Panayotou The homeodomain region of RAG-1 reveals the parallel mechanisms of bacterial and V(D)J recombination Cell 87 1996 263 276
24. P.C. Swanson, and S. Desiderio V(D)J recombination signal recognition: distinct, overlapping DNA-protein contacts in complexes containing RAG1 with and without RAG2 Immunity 9 1998 115 125
25. F. Nagawa, K. Ishiguro, A. Tsuboi, T. Yoshida, A. Ishikawa, T. Takemori, A.J. Otsuka, and H. Sakano Footprint analysis of the RAG protein recombination signal sequence complex for V(D)J type recombination Mol Cell Biol 18 1998 655 663
26. S. Akira, K. Okazaki, and H. Sakano Two pairs of recombination signals are sufficient to cause immunoglobulin V-(D)-J joining Science 238 1987 1134 1138
27. S.M. Lewis, J.E. Hesse, K. Mizuuchi, and M. Gellert Novel strand exchanges in V(D)J recombination Cell 55 1988 1099 1107
28. J.E. Hesse, M.R. Lieber, K. Mizuuchi, and M. Gellert V(D)J recombination: a functional definition of the joining signals Genes Dev 3 1989 1053 1061
29. S.M. Lewis, and J.E. Hesse Cutting and closing without recombination in V(D)J joining Embo J 10 1991 3631 3639
30. Y. Akamatsu, N. Tsurushita, F. Nagawa, M. Matsuoka, K. Okazaki, M. Imai, and H. Sakano Essential residues in V(D)J recombination signals J Immunol 153 1994 4520 4529
31. D.A. Ramsden, K. Baetz, and G.E. Wu Conservation of sequence in recombination signal sequence spacers Nucl Acids Res 22 1994 1785 1796
32. Y. Akamatsu, and M.A. Oettinger Distinct roles of RAG1 and RAG2 in binding the V(D)J recombination signal sequences Mol Cell Biol 18 1998 4670 4678
33. M.M. Hughes, R.E. Tillman, T.D. Wehrly, J.M. White, and B.P. Sleckman The B12/23 restriction is critically dependent on recombination signal nonamer and spacer sequences J Immunol 171 2003 6604 6610
34. A.I. Lee, S.D. Fugmann, L.G. Cowell, L.M. Ptaszek, G. Kelsoe, and D.G. Schatz A functional analysis of the spacer of V(D)J recombination signal sequences PLoS Biol 1 2003 E1
35. J.G. Seidman, M.M. Nau, B. Norman, S.P. Kwan, M. Scharff, and P. Leder Immunoglobulin V/J recombination is accompanied by deletion of joining site and variable region segments Proc Natl Acad Sci U S A 77 1980 6022 6026
36. F.W. Alt, and D. Baltimore Joining of immunoglobulin heavy chain gene segments: implications from a chromosome with evidence of three D-JH fusions Proc Natl Acad Sci U S A 79 1982 4118 4122
37. J. Hochtl, and H.G. Zachau A novel type of aberrant recombination in immunoglobulin genes and its implications for V-J joining mechanism Nature 302 1983 260 263
38. K.D. Meek, C.A. Hasemann, and J.D. Capra Novel rearrangements at the immunoglobulin D locus. Inversions and fusions add to IgH somatic diversity J Exp Med 170 1989 39 57
39. J.E. Hesse, M.R. Lieber, M. Gellert, and K. Mizuuchi Extrachromosomal DNA substrates in pre-B cells undergo inversion or deletion at immunoglobulin V-(D)-J joining signals Cell 49 1987 775 783
40. G.H. Gauss, and M.R. Lieber The basis for the mechanistic bias for deletional over inversional V(D)J recombination Genes Dev 6 1992 1553 1561
41. E. Morzycka-Wroblewska, F.E. Lee, and S.V. Desiderio Unusual immunoglobulin gene rearrangement leads to replacement of recombinational signal sequences Science 242 1988 261 263
42. D. Alexandre, P. Chuchana, M.G. Roncarolo, H. Yssel, H. Spits, G. Lefranc, and M.P. Lefranc Reciprocal hybrid joints demonstrate successive V-J rearrangements on the same chromosome in the human TCR gamma locus Int Immunol 3 1991 973 982
43. A.E. Sollbach, and G.E. Wu Inversions produced during V(D)J rearrangement at IgH, the immunoglobulin heavy-chain locus Mol Cell Biol 15 1995 671 681
44. E.A. Hendrickson, V.F. Liu, and D.T. Weaver Strand breaks without DNA rearrangement in V(D)J recombination Mol Cell Biol 11 1991 3155 3162
45. A.M. Carroll, J.K. Slack, and W.T. Chang Biased T-cell receptor δ element recombination in scid thymocytes Mol Cell Biol 13 1993 3632 3640
46. R.E. Tillman, A.L. Wooley, M.M. Hughes, T.D. Wehrly, W. Swat, and B.P. Sleckman Restrictions limiting the generation of DNA double strand breaks during chromosomal V(D)J recombination J Exp Med 195 2002 309 316
47. G.D. Yancopoulos, B.A. Malynn, and F.W. Alt Developmentally regulated and strain-specific expression of murine VH gene families J Exp Med 168 1988 417 435
48. U. Storb, D. Haasch, B. Arp, P. Sanchez, P.A. Cazenave, and J. Miller Physical linkage of mouse lambda genes by pulsed-field gel electrophoresis suggests that the rearrangement process favors proximate target sequences Mol Cell Biol 9 1989 711 718
49. T. Blunt, D. Gell, M. Fox, G.E. Taccioli, A.R. Lehmann, S.P. Jackson, and P.A. Jeggo Identification of a nonsense mutation in the carboxyl-terminal region of DNA-dependent protein kinase catalytic subunit in the scid mouse Proc Natl Acad Sci U S A 93 1996 10285 10290
50. P.A. Jeggo, S.P. Jackson, and G.E. Taccioli Identification of the catalytic subunit of DNA dependent protein kinase as the product of the mouse scid gene Curr Top Microbiol Immunol 217 1996 79 89
51. R. Araki, A. Fujimori, K. Hamatani, K. Mita, T. Saito, M. Mori, R. Fukumura, M. Morimyo, M. Muto, M. Itoh, K. Tatsumi, and M. Abe Nonsense mutation at Tyr-4046 in the DNA-dependent protein kinase catalytic subunit of severe combined immune deficiency mice Proc Natl Acad Sci U S A 94 1997 2438 2443
52. M.R. Lieber, J.E. Hesse, S. Lewis, G.C. Bosma, N. Rosenberg, K. Mizuuchi, M.J. Bosma, and M. Gellert The defect in murine severe combined immune deficiency: joining of signal sequences but not coding segments in V(D)J recombination Cell 55 1988 7 16
53. M.J. Bosma, and A.M. Carroll The SCID mouse mutant: definition, characterization, and potential uses Annu Rev Immunol 9 1991 323 350
54. S. Lew, D. Franco, and Y. Chang Activation of V(D)J recombination induces the formation of interlocus joints and hybrid joints in scid pre-B-cell lines Mol Cell Biol 20 2000 7170 7177
55. A.J. Korman, J.D. Frantz, J.L. Strominger, and R.C. Mulligan Expression of human class II major histocompatibility complex antigens using retrovirus vectors Proc Natl Acad Sci U S A 84 1987 2150 2154
56. J. Sambrook, E.F. Fritsch, and T. Maniatis Molecular cloning: a laboratory manual 2nd ed 1989 Cold Spring Harbor Press Cold Spring Harbor, NY
57. M.G. Reth, P. Ammirati, S. Jackson, and F.W. Alt Regulated progression of a cultured pre-B-cell line to the B-cell stage Nature 317 1985 353 355
58. E.A. Hendrickson, D.G. Schatz, and D.T. Weaver The scid gene encodes a trans-acting factor that mediates the rejoining event of Ig gene rearrangement Genes Dev 2 1988 817 829
59. J.D. Broome, and M.W. Jeng Growth stimulation of mouse leukemia cells by thiols and disulfides in vitro J Natl Cancer Inst 49 1972 579 581
60. R. Mann, R.C. Mulligan, and D. Baltimore Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus Cell 33 1983 153 159
61. F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl Current protocols in molecular biology 1994 Wiley New York
62. S.B. Steen, L. Gomelsky, S.L. Speidel, and D.B. Roth Initiation of V(D)J recombination in vivo: role of recombination signal sequences in formation of single and paired double-strand breaks Embo J 16 1997 2656 2664
63. A. Golding, S. Chandler, E. Ballestar, A.P. Wolffe, and M.S. Schlissel Nucleosome structure completely inhibits in vitro cleavage by the V(D)J recombinase Embo J 18 1999 3712 3723
64. J. Kwon, A.N. Imbalzano, A. Matthews, and M.A. Oettinger Accessibility of nucleosomal DNA to V(D)J cleavage is modulated by RSS positioning and HMG1 Mol Cell 2 1998 829 839
65. F. McBlane, and J. Boyes Stimulation of V(D)J recombination by histone acetylation Curr Biol 10 2000 483 486
66. J. Kwon, K.B. Morshead, J.R. Guyon, R.E. Kingston, and M.A. Oettinger Histone acetylation and hSWI/SNF remodeling act in concert to stimulate V(D)J cleavage of nucleosomal DNA Mol Cell 6 2000 1037 1048
67. F. Alt, N. Rosenberg, S. Lewis, E. Thomas, and D. Baltimore Organization and reorganization of immunoglobulin genes in A-MULV-transformed cells: rearrangement of heavy but not light chain genes Cell 27 1981 381 390
68. S. Cheung, K. Arndt, and P. Lu Correlation of lac operator DNA imino proton exchange kinetics with its function Proc Natl Acad Sci U S A 81 1984 3665 3669
69. Y. Timsit, E. Vilbois, and D. Moras Base-pairing shift in the major groove of (CA)n tracts by B-DNA crystal structures Nature 354 1991 167 170
70. P.C. Swanson A RAG-1/RAG-2 tetramer supports 12/23-regulated synapsis, cleavage, and transposition of V(D)J recombination signals Mol Cell Biol 22 2002 7790 77801
71. L. Fanning, A. Connor, K. Baetz, D. Ramsden, and G.E. Wu Mouse RSS spacer sequences affect the rate of V(D)J recombination Immunogenetics 44 1996 146 150
72. D.C. van Gent, K. Hiom, T.T. Paull, and M. Gellert Stimulation of V(D)J cleavage by high mobility group proteins Embo J 16 1997 2665 2670
73. K. Hiom, and M. Gellert Assembly of a 12/23 paired signal complex: a critical control point in V(D)J recombination Mol Cell 1 1998 1011 1019
74. R.B. West, and M.R. Lieber The RAG-HMG1 complex enforces the 12/23 rule of V(D)J recombination specifically at the double-hairpin formation step Mol Cell Biol 18 1998 6408 6415
75. D.R. Kim, and M.A. Oettinger Functional analysis of coordinated cleavage in V(D)J recombination Mol Cell Biol 18 1998 4679 4688
76. T. Yoshida, A. Tsuboi, K. Ishiguro, F. Nagawa, and H. Sakano The DNA-bending protein, HMG1, is required for correct cleavage of 23 bp recombination signal sequences by recombination activating gene proteins in vitro Int Immunol 12 2000 721 729
77. D. Jung, C.H. Bassing, S.D. Fugmann, H.L. Cheng, D.G. Schatz, and F.W. Alt Extrachromosomal recombination substrates recapitulate beyond 12/23 restricted VDJ recombination in nonlymphoid cells Immunity 18 2003 65 74
78. C.H. Bassing, F.W. Alt, M.M. Hughes, M. D'Auteuil, T.D. Wehrly, B.B. Woodman, F. Gartner, J.M. White, L. Davidson, and B.P. Sleckman Recombination signal sequences restrict chromosomal V(D)J recombination beyond the 12/23 rule Nature 405 2000 583 586
79. D.J. Sawchuk, J. Mansilla-Soto, C. Alarcon, N.C. Singha, H. Langen, M.E. Bianchi, S.P. Lees-Miller, M.C. Nussenzweig, and P. Cortes Ku70/Ku80 and DNA-dependent protein kinase catalytic subunit modulate RAG-mediated cleavage: implications for the enforcement of the 12/23 rule J Biol Chem 279 2004 29821 29831
80. A.M. Carroll, J.K. Slack, and X. Mu V(D)J recombination generates a high frequency of nonstandard TCR D δ-associated rearrangements in thymocytes J Immunol 150 1993 2222 2230
81. F. Lista, V. Bertness, C.J. Guidos, J.S. Danska, and I.R. Kirsch The absolute number of trans-rearrangements between the TCRG and TCRB loci is predictive of lymphoma risk: a severe combined immune deficiency (SCID) murine model Cancer Res 57 1997 4408 4413
82. M. Serwe, and F. Sablitzky V(D)J recombination in B cells is impaired but not blocked by targeted deletion of the immunoglobulin heavy chain intron enhancer Embo J 12 1993 2321 2327
83. S. Takeda, Y.R. Zou, H. Bluethmann, D. Kitamura, U. Muller, and K. Rajewsky Deletion of the immunoglobulin kappa chain intron enhancer abolishes κ chain gene rearrangement in cis but not lambda chain gene rearrangement in trans Embo J 12 1993 2329 2336
84. H. Leung, and N. Maizels Transcriptional regulatory elements stimulate recombination in extrachromosomal substrates carrying immunoglobulin switch-region sequences Proc Natl Acad Sci U S A 89 1992 4154 4158
85. H. Leung, and N. Maizels Regulation and targeting of recombination in extrachromosomal substrates carrying immunoglobulin switch region sequences Mol Cell Biol 14 1994 1450 1458
86. F.A. Roch, R. Hobi, M.W. Berchtold, and C.C. Kuenzle V(D)J recombination frequency is affected by the sequence interposed between a pair of recombination signals: sequence comparison reveals a putative recombinational enhancer element Nucl Acids Res 25 1997 2303 2310
87. W.M. Hempel, P. Stanhope-Baker, N. Mathieu, F. Huang, M.S. Schlissel, and P. Ferrier Enhancer control of V(D)J recombination at the TCR β locus: differential effects on DNA cleavage and joining Genes Dev 12 1998 2305 2317
88. F.W. Alt, N. Rosenberg, V. Enea, E. Siden, and D. Baltimore Multiple immunoglobulin heavy-chain gene transcripts in Abelson murine leukemia virus-transformed lymphoid cell lines Mol Cell Biol 2 1982 386 400
89. T.K. Blackwell, M.W. Moore, G.D. Yancopoulos, H. Suh, S. Lutzker, E. Selsing, and F.W. Alt Recombination between immunoglobulin variable region gene segments is enhanced by transcription Nature 324 1986 585 589
90. L. Ramakrishnan, and N. Rosenberg Novel B-cell precursors blocked at the stage of DJH recombination Mol Cell Biol 8 1988 5216 5223
91. D.J. Bolland, A.L. Wood, C.M. Johnston, S.F. Bunting, G. Morgan, L. Chakalova, P.J. Fraser, and A.E. Corcoran Antisense intergenic transcription in V(D)J recombination Nat Immunol 5 2004 630 637
92. N. Biswal, and M. Benyesh-Melnick Complementary nuclear RNA's of murine sarcoma-leukemia virus complex in transformed cells Proc Natl Acad Sci U S A 64 1969 1372 1379
93. N. Biswal, and M. Benyesh-Melnick Characterization of the complementary nuclear RNA of murine sarcoma-leukemia virus Virology 42 1970 1064 1072
94. M.I. Bukrinsky, and A.F. Etkin Plus strand of the HIV provirus DNA is expressed at early stages of infection AIDS Res Hum Retroviruses 6 1990 425 426
95. M.A. Gama Sosa, D.H. Rosas, R. DeGasperi, E. Morita, M.R. Hutchison, and R.M. Ruprecht Negative regulation of the 5′ long terminal repeat (LTR) by the 3′ LTR in the murine proviral genome J Virol 68 1994 2662 2670