Home LiteratureArticle Details
PMID: 14993249 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Mapping of a functional recombination motif that defines isotype specificity for mu-->gamma3 switch recombination implicates NF-kappaB p50 as the isotype-specific switching factor.

The Journal of experimental medicine ·Vol. 199 ·No. 5 ·2004-03-01 ·Pages 617-27

Kenter AL, Wuerffel R, Dominguez C, Shanmugam A, Zhang H

Abstract

Ig class switch recombination (CSR) requires expression of activation-induced deaminase (AID) and production of germline transcripts to target S regions for recombination. However, the mechanism of CSR remains unclear. Here we show that an extrachromosomal S plasmid assay is AID dependent and that a single consensus repeat is both necessary and sufficient for isotype-specific CSR. Transfected switch substrates specific for mu-->gamma3 and mu-->gamma1 are stimulated to switch with lipopolysaccharide (LPS) alone or LPS and interleukin-4, respectively. An Sgamma3/Sgamma1 substrate containing only three Sgamma3-associated nucleotides reconstituted LPS responsiveness and permitted mapping of a functional recombination motif specific for mu-->gamma3 CSR. This functional recombination motif colocalized with a binding site for NF-kappaB p50, and p50 binding to this site was previously established. We show a p50 requirement for plasmid-based mu-->gamma3 CSR using p50-deficient B cells. Switch junctions from p50-deficient B cells showed decreased lengths of microhomology between Smu and Sgamma3 relative to wild-type cells, indicating a function for p50 in the mechanics of CSR. We note a striking parallel between the affects of p50 and Msh2 deficiency on Smu/Sgamma3 junctions. The data suggest that p50 may be the isotype-specific factor in mu-->gamma3 CSR and epistatic with Msh2.

MeSH Terms
Animals Base Sequence Chromosome Mapping Cytidine Deaminase/genetics,metabolism DNA/genetics Gene Expression Immunoglobulin Class Switching Immunoglobulin Isotypes/genetics Immunoglobulin gamma-Chains/genetics Immunoglobulin mu-Chains/genetics In Vitro Techniques Mice Mice, Inbred C57BL Mice, Knockout Molecular Sequence Data NF-kappa B/metabolism NF-kappa B p50 Subunit Plasmids/genetics Recombination, Genetic Tandem Repeat Sequences
Chemicals
Immunoglobulin Isotypes Immunoglobulin gamma-Chains Immunoglobulin mu-Chains NF-kappa B NF-kappa B p50 Subunit DNA AICDA (activation-induced cytidine deaminase) Cytidine Deaminase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Kenter Amy L
Department of Microbiology and Immunology, University of Illinois College of Medicine, Chicago 60612-7344, USA. star1@uic.edu
Wuerffel Robert
Dominguez Carmen
Shanmugam Ananth
Zhang Hongmei
References (67)
67 references, click to expand
  1. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination.
    Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9214-9 PMID: 9256462
  2. DHFR/MSH3 amplification in methotrexate-resistant cells alters the hMutSalpha/hMutSbeta ratio and reduces the efficiency of base-base mismatch repair.
    Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10144-9 PMID: 9294177
  3. B cells genetically deficient in the c-Rel transactivation domain have selective defects in germline CH transcription and Ig class switching.
    J Immunol. 1997 Oct 1;159(7):3133-9 PMID: 9317110
  4. Genomic instability in mice lacking histone H2AX.
    Science. 2002 May 3;296(5569):922-7 PMID: 11934988
  5. AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts.
    Science. 2002 Jun 14;296(5575):2033-6 PMID: 12065838
  6. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification.
    Nature. 2002 Jul 4;418(6893):99-103 PMID: 12097915
  7. Internal IgH class switch region deletions are position-independent and enhanced by AID expression.
    Proc Natl Acad Sci U S A. 2002 Jul 23;99(15):9984-9 PMID: 12114543
  8. Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase.
    Nature. 2002 Sep 5;419(6902):43-8 PMID: 12214226
  9. Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice.
    Curr Biol. 2002 Oct 15;12(20):1748-55 PMID: 12401169
  10. DNA-dependent protein kinase activity is not required for immunoglobulin class switching.
    J Exp Med. 2002 Dec 2;196(11):1483-95 PMID: 12461083
  11. Class-switch recombination: after the dawn of AID.
    Curr Opin Immunol. 2003 Apr;15(2):190-8 PMID: 12633669
  12. Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4102-7 PMID: 12651944
  13. Transcription-targeted DNA deamination by the AID antibody diversification enzyme.
    Nature. 2003 Apr 17;422(6933):726-30 PMID: 12692563
  14. The influence of transcriptional orientation on endogenous switch region function.
    Nat Immunol. 2003 May;4(5):435-41 PMID: 12679811
  15. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells.
    Nat Immunol. 2003 May;4(5):442-51 PMID: 12679812
  16. Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand.
    Nat Immunol. 2003 May;4(5):452-6 PMID: 12692548
  17. Constitutive expression of AID leads to tumorigenesis.
    J Exp Med. 2003 May 5;197(9):1173-81 PMID: 12732658
  18. Mlh1 can function in antibody class switch recombination independently of Msh2.
    J Exp Med. 2003 May 19;197(10):1377-83 PMID: 12743174
  19. AID mediates hypermutation by deaminating single stranded DNA.
    J Exp Med. 2003 May 19;197(10):1291-6 PMID: 12756266
  20. H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation.
    J Exp Med. 2003 Jun 16;197(12):1767-78 PMID: 12810694
  21. Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation.
    Nature. 2003 Jul 3;424(6944):103-7 PMID: 12819663
  22. The block in immunoglobulin class switch recombination caused by activation-induced cytidine deaminase deficiency occurs prior to the generation of DNA double strand breaks in switch mu region.
    J Immunol. 2003 Sep 1;171(5):2504-9 PMID: 12928399
  23. Human uracil-DNA glycosylase deficiency associated with profoundly impaired immunoglobulin class-switch recombination.
    Nat Immunol. 2003 Oct;4(10):1023-8 PMID: 12958596
  24. The Smu tandem repeat region is critical for Ig isotype switching in the absence of Msh2.
    Immunity. 2003 Oct;19(4):515-24 PMID: 14563316
  25. Mutations occur in the Ig Smu region but rarely in Sgamma regions prior to class switch recombination.
    EMBO J. 2003 Nov 3;22(21):5893-903 PMID: 14592986
  26. Mutations, duplication, and deletion of recombined switch regions suggest a role for DNA replication in the immunoglobulin heavy-chain switch.
    Mol Cell Biol. 1989 May;9(5):1850-6 PMID: 2747637
  27. Molecular aspects of heavy-chain class switching.
    Crit Rev Immunol. 1989;9(3):173-200 PMID: 2505810
  28. Copy choice mechanism of immunoglobulin heavy-chain switch recombination.
    Mol Cell Biol. 1990 Jan;10(1):397-400 PMID: 2104661
  29. Induction of RNA-stabilized DNA conformers by transcription of an immunoglobulin switch region.
    Nature. 1990 Nov 22;348(6299):342-4 PMID: 1701219
  30. Switch recombination breakpoints are strictly correlated with DNA recognition motifs for immunoglobulin S gamma 3 DNA-binding proteins.
    J Exp Med. 1992 Aug 1;176(2):339-49 PMID: 1500850
  31. DNA sequences at immunoglobulin switch region recombination sites.
    Nucleic Acids Res. 1993 Feb 11;21(3):365-72 PMID: 8441648
  32. Switch recombination breakpoints occur at nonrandom positions in the S gamma tandem repeat.
    J Immunol. 1993 Nov 1;151(9):4718-31 PMID: 8409431
  33. Transcription induces the formation of a stable RNA.DNA hybrid in the immunoglobulin alpha switch region.
    J Biol Chem. 1994 Aug 26;269(34):21850-7 PMID: 8063829
  34. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses.
    Cell. 1995 Jan 27;80(2):321-30 PMID: 7834752
  35. Ku70 is required for late B cell development and immunoglobulin heavy chain class switching.
    J Exp Med. 1998 Jun 15;187(12):2081-9 PMID: 9625768
  36. Mismatch repair deficiency associated with overexpression of the MSH3 gene.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8568-73 PMID: 9671718
  37. Deficiency in Msh2 affects the efficiency and local sequence specificity of immunoglobulin class-switch recombination: parallels with somatic hypermutation.
    EMBO J. 1999 Jun 15;18(12):3484-90 PMID: 10369687
  38. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells.
    J Biol Chem. 1999 Jun 25;274(26):18470-6 PMID: 10373455
  39. Reduced isotype switching in splenic B cells from mice deficient in mismatch repair enzymes.
    J Exp Med. 1999 Aug 2;190(3):323-30 PMID: 10430621
  40. Switch recombination in a transfected plasmid occurs preferentially in a B cell line that undergoes switch recombination of its chromosomal Ig heavy chain genes.
    J Immunol. 1999 Aug 15;163(4):2028-40 PMID: 10438941
  41. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching.
    Nature. 2001 Dec 6;414(6864):660-5 PMID: 11740565
  42. Novel in vitro model for high-rate IgA class switching.
    J Immunol. 1995 Apr 1;154(7):3156-61 PMID: 7897205
  43. B cells from p50/NF-kappa B knockout mice have selective defects in proliferation, differentiation, germ-line CH transcription, and Ig class switching.
    J Immunol. 1996 Jan 1;156(1):183-91 PMID: 8598461
  44. RNA:DNA complex formation upon transcription of immunoglobulin switch regions: implications for the mechanism and regulation of class switch recombination.
    Nucleic Acids Res. 1995 Dec 25;23(24):5006-11 PMID: 8559658
  45. Two pathways for removal of nonhomologous DNA ends during double-strand break repair in Saccharomyces cerevisiae.
    Mol Cell Biol. 1997 Nov;17(11):6765-71 PMID: 9343441
  46. Ig Sgamma3 DNA-specifc double strand breaks are induced in mitogen-activated B cells and are implicated in switch recombination.
    J Immunol. 1997 Nov 1;159(9):4139-44 PMID: 9379005
  47. Ku80 is required for immunoglobulin isotype switching.
    EMBO J. 1998 Apr 15;17(8):2404-11 PMID: 9545251
  48. Molecular processes that regulate class switching.
    Curr Top Microbiol Immunol. 2000;245(2):127-68 PMID: 10533321
  49. Multiple functions of MutS- and MutL-related heterocomplexes.
    Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14186-8 PMID: 10588673
  50. Suppression of spontaneous mutagenesis in human cells by DNA base excision-repair.
    Mutat Res. 2000 Apr;462(2-3):129-35 PMID: 10767624
  51. Evidence for class-specific factors in immunoglobulin isotype switching.
    J Exp Med. 2000 Apr 17;191(8):1365-80 PMID: 10770803
  52. Steady-state regulation of the human DNA mismatch repair system.
    J Biol Chem. 2000 Jun 16;275(24):18424-31 PMID: 10747992
  53. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme.
    Cell. 2000 Sep 1;102(5):553-63 PMID: 11007474
  54. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2).
    Cell. 2000 Sep 1;102(5):565-75 PMID: 11007475
  55. Roles for mismatch repair factors in regulating genetic recombination.
    Mol Cell Biol. 2000 Nov;20(21):7839-44 PMID: 11027255
  56. The mu switch region tandem repeats are important, but not required, for antibody class switch recombination.
    J Exp Med. 2001 Jan 15;193(2):159-68 PMID: 11148220
  57. NF-kappa B p50-dependent in vivo footprints at Ig S gamma 3 DNA are correlated with mu-->gamma 3 switch recombination.
    J Immunol. 2001 Apr 1;166(7):4552-9 PMID: 11254712
  58. Variable deletion and duplication at recombination junction ends: implication for staggered double-strand cleavage in class-switch recombination.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13860-5 PMID: 11717442
  59. Switch junction sequences in PMS2-deficient mice reveal a microhomology-mediated mechanism of Ig class switch recombination.
    Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14553-8 PMID: 11717399
  60. Mechanism and control of class-switch recombination.
    Trends Immunol. 2002 Jan;23(1):31-9 PMID: 11801452
  61. Role for mismatch repair proteins Msh2, Mlh1, and Pms2 in immunoglobulin class switching shown by sequence analysis of recombination junctions.
    J Exp Med. 2002 Feb 4;195(3):367-73 PMID: 11828012
  62. Activation-induced cytidine deaminase turns on somatic hypermutation in hybridomas.
    Nature. 2002 Feb 14;415(6873):802-6 PMID: 11823785
  63. Activation-induced deaminase (AID)-directed hypermutation in the immunoglobulin Smu region: implication of AID involvement in a common step of class switch recombination and somatic hypermutation.
    J Exp Med. 2002 Feb 18;195(4):529-34 PMID: 11854365
  64. Two new isotype-specific switching activities detected for Ig class switching.
    J Immunol. 2002 Mar 15;168(6):2835-46 PMID: 11884453
  65. The AID enzyme induces class switch recombination in fibroblasts.
    Nature. 2002 Mar 21;416(6878):340-5 PMID: 11875397
  66. IgH class switch recombination to IgG1 in DNA-PKcs-deficient B cells.
    Immunity. 2002 Apr;16(4):607-17 PMID: 11970883
  67. Analysis of immunoglobulin Sgamma3 recombination breakpoints by PCR: implications for the mechanism of isotype switching.
    Nucleic Acids Res. 1997 Aug 1;25(15):3066-73 PMID: 9224606
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
2004-03-01
Pages
617-27
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2213297
Subset
IM
Grants
NIAID NIH HHS · R21 AI106328 · United States
NIAID NIH HHS · R01 AI052400 · United States
NIAID NIH HHS · AI45045 · United States
NIAID NIH HHS · R01 AI045045 · United States
NIAID NIH HHS · R01 AI052400-03 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com