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PMID: 18786917 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Hypermutation at A/T sites during G.U mismatch repair in vitro by human B-cell lysates.

The Journal of biological chemistry ·Vol. 283 ·No. 46 ·2008-11-14 ·Pages 31754-62

Pham P, Zhang K, Goodman MF

Abstract

Somatic hypermutation in the variable regions of immunoglobulin genes is required to produce high affinity antibody molecules. Somatic hypermutation results by processing G.U mismatches generated when activation-induced cytidine deaminase (AID) deaminates C to U. Mutations at C/G sites are targeted mainly at deamination sites, whereas mutations at A/T sites entail error-prone DNA gap repair. We used B-cell lysates to analyze salient features of somatic hypermutation with in vitro mutational assays. Tonsil and hypermutating Ramos B-cells convert C-->U in accord with AID motif specificities, whereas HeLa cells do not. Using tonsil cell lysates to repair a G.U mismatch, A/T and G/C targeted mutations occur about equally, whereas Ramos cell lysates make fewer mutations at A/T sites (approximately 24%) compared with G/C sites (approximately 76%). In contrast, mutations in HeLa cell lysates occur almost exclusively at G/C sites (> 95%). By recapitulating two basic features of B-cell-specific somatic hypermutation, G/C mutations targeted to AID hot spot motifs and elevated A/T mutations dependent on error-prone processing of G.U mispairs, these cell free assays provide a practical method to reconstitute error-prone mismatch repair using purified B-cell proteins.

MeSH Terms
B-Lymphocytes/metabolism Base Sequence DNA Mismatch Repair/genetics Humans Molecular Sequence Data Mutation/genetics
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Pham Phuong
Department of Biological Sciences and Chemistry, University of Southern California, Los Angeles, California 90089-2910, USA.
Zhang Ke
Goodman Myron F
References (84)
84 references, click to expand
  1. Cloning and expression of human G/T mismatch-specific thymine-DNA glycosylase.
    J Biol Chem. 1996 May 31;271(22):12767-74 PMID: 8662714
  2. Somatic hypermutation in the heavy chain locus correlates with transcription.
    Immunity. 1998 Jul;9(1):105-14 PMID: 9697840
  3. DNA polymerase theta contributes to the generation of C/G mutations during somatic hypermutation of Ig genes.
    Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):13986-91 PMID: 16172387
  4. Somatic mutation hotspots correlate with DNA polymerase eta error spectrum.
    Nat Immunol. 2001 Jun;2(6):530-6 PMID: 11376340
  5. DNA polymerase eta is an A-T mutator in somatic hypermutation of immunoglobulin variable genes.
    Nat Immunol. 2001 Jun;2(6):537-41 PMID: 11376341
  6. APOBEC-mediated editing of viral RNA.
    Science. 2004 Jul 30;305(5684):645 PMID: 15286366
  7. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome.
    Nat Struct Mol Biol. 2004 May;11(5):435-42 PMID: 15098018
  8. A role for Msh6 but not Msh3 in somatic hypermutation and class switch recombination.
    J Exp Med. 2004 Jul 5;200(1):61-8 PMID: 15238605
  9. DNA polymerase eta is involved in hypermutation occurring during immunoglobulin class switch recombination.
    J Exp Med. 2004 Jan 19;199(2):265-70 PMID: 14734526
  10. Mechanisms in eukaryotic mismatch repair.
    J Biol Chem. 2006 Oct 13;281(41):30305-9 PMID: 16905530
  11. Base damage and single-strand break repair: mechanisms and functional significance of short- and long-patch repair subpathways.
    DNA Repair (Amst). 2007 Apr 1;6(4):398-409 PMID: 17129767
  12. Contribution of DNA polymerase eta to immunoglobulin gene hypermutation in the mouse.
    J Exp Med. 2005 Apr 18;201(8):1191-6 PMID: 15824086
  13. DNA deamination mediates innate immunity to retroviral infection.
    Cell. 2003 Jun 13;113(6):803-9 PMID: 12809610
  14. AID mediates hypermutation by deaminating single stranded DNA.
    J Exp Med. 2003 May 19;197(10):1291-6 PMID: 12756266
  15. Antisense transcripts from immunoglobulin heavy-chain locus V(D)J and switch regions.
    Proc Natl Acad Sci U S A. 2008 Mar 11;105(10):3843-8 PMID: 18292225
  16. Hot spot focusing of somatic hypermutation in MSH2-deficient mice suggests two stages of mutational targeting.
    Immunity. 1998 Jul;9(1):135-41 PMID: 9697843
  17. Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo.
    J Mol Biol. 2004 Mar 26;337(3):585-96 PMID: 15019779
  18. Transcription-targeted DNA deamination by the AID antibody diversification enzyme.
    Nature. 2003 Apr 17;422(6933):726-30 PMID: 12692563
  19. In vitro triggering of somatic mutation in human naive B cells.
    J Immunol. 1997 Oct 1;159(7):3347-53 PMID: 9317133
  20. Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation.
    Mol Cell. 2004 Oct 22;16(2):163-71 PMID: 15494304
  21. Msh2 ATPase activity is essential for somatic hypermutation at a-T basepairs and for efficient class switch recombination.
    J Exp Med. 2003 Oct 20;198(8):1171-8 PMID: 14568978
  22. DNA polymerase beta and mammalian base excision repair.
    Cold Spring Harb Symp Quant Biol. 2000;65:143-55 PMID: 12760029
  23. DNA mismatch repair.
    Annu Rev Biochem. 2005;74:681-710 PMID: 15952900
  24. DNA deaminases AID and APOBEC3G act processively on single-stranded DNA.
    DNA Repair (Amst). 2007 Jun 1;6(6):689-92; author reply 693-4 PMID: 17291835
  25. 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
  26. DNA polymerase eta is the sole contributor of A/T modifications during immunoglobulin gene hypermutation in the mouse.
    J Exp Med. 2007 Jan 22;204(1):17-23 PMID: 17190840
  27. Targeting AID to the Ig genes.
    Adv Exp Med Biol. 2007;596:93-109 PMID: 17338179
  28. AID-initiated purposeful mutations in immunoglobulin genes.
    Adv Immunol. 2007;94:127-55 PMID: 17560274
  29. AID-GFP chimeric protein increases hypermutation of Ig genes with no evidence of nuclear localization.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):7003-8 PMID: 12011459
  30. The translesion DNA polymerase zeta plays a major role in Ig and bcl-6 somatic hypermutation.
    Immunity. 2001 May;14(5):643-53 PMID: 11371365
  31. Retroviral restriction by APOBEC proteins.
    Nat Rev Immunol. 2004 Nov;4(11):868-77 PMID: 15516966
  32. A/T mutagenesis in hypermutated immunoglobulin genes strongly depends on PCNAK164 modification.
    J Exp Med. 2007 Aug 6;204(8):1989-98 PMID: 17664295
  33. Known components of the immunoglobulin A:T mutational machinery are intact in Burkitt lymphoma cell lines with G:C bias.
    Mol Immunol. 2007 Apr;44(10):2659-66 PMID: 17240451
  34. Altered somatic hypermutation and reduced class-switch recombination in exonuclease 1-mutant mice.
    Nat Immunol. 2004 Feb;5(2):224-9 PMID: 14716311
  35. Somatic hypermutation is limited by CRM1-dependent nuclear export of activation-induced deaminase.
    J Exp Med. 2004 May 3;199(9):1235-44 PMID: 15117971
  36. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases.
    Mol Biol Evol. 2005 Feb;22(2):367-77 PMID: 15496550
  37. The AID antibody diversification enzyme is regulated by protein kinase A phosphorylation.
    Nature. 2005 Nov 24;438(7067):508-11 PMID: 16251902
  38. 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
  39. Genetic analysis reveals an intrinsic property of the germinal center B cells to generate A:T mutations.
    DNA Repair (Amst). 2008 Aug 2;7(8):1392-8 PMID: 18562254
  40. An overview of cytidine deaminases.
    Int J Hematol. 2006 Apr;83(3):195-200 PMID: 16720547
  41. Replication protein A interacts with AID to promote deamination of somatic hypermutation targets.
    Nature. 2004 Aug 26;430(7003):992-8 PMID: 15273694
  42. Class-switch recombination: interplay of transcription, DNA deamination and DNA repair.
    Nat Rev Immunol. 2004 Jul;4(7):541-52 PMID: 15229473
  43. Construction and characterization of mismatch-containing circular DNA molecules competent for assessment of nick-directed human mismatch repair in vitro.
    Nucleic Acids Res. 2002 Feb 1;30(3):E14 PMID: 11809902
  44. The biochemistry of somatic hypermutation.
    Annu Rev Immunol. 2008;26:481-511 PMID: 18304001
  45. Fidelity of uracil-initiated base excision DNA repair in DNA polymerase beta-proficient and -deficient mouse embryonic fibroblast cell extracts.
    J Biol Chem. 2001 Nov 9;276(45):42588-600 PMID: 11551933
  46. The translesion DNA polymerase theta plays a dominant role in immunoglobulin gene somatic hypermutation.
    EMBO J. 2005 Nov 2;24(21):3757-69 PMID: 16222339
  47. Targeting of the activation-induced cytosine deaminase is strongly influenced by the sequence and structure of the targeted DNA.
    Mol Cell Biol. 2005 Dec;25(24):10815-21 PMID: 16314506
  48. Activation-induced cytidine deaminase shuttles between nucleus and cytoplasm like apolipoprotein B mRNA editing catalytic polypeptide 1.
    Proc Natl Acad Sci U S A. 2004 Feb 17;101(7):1975-80 PMID: 14769937
  49. APOBEC3G DNA deaminase acts processively 3' --> 5' on single-stranded DNA.
    Nat Struct Mol Biol. 2006 May;13(5):392-9 PMID: 16622407
  50. Molecular mechanisms of antibody somatic hypermutation.
    Annu Rev Biochem. 2007;76:1-22 PMID: 17328676
  51. Cytidine deamination of retroviral DNA by diverse APOBEC proteins.
    Curr Biol. 2004 Aug 10;14(15):1392-6 PMID: 15296758
  52. APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase.
    Nucleic Acids Res. 2004 Apr 30;32(8):2421-9 PMID: 15121899
  53. Type two hyper-IgM syndrome caused by mutation in activation-induced cytidine deaminase.
    J Med Dent Sci. 2003 Mar;50(1):41-6 PMID: 12715918
  54. Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors.
    Curr Biol. 1999 Feb 25;9(4):174-85 PMID: 10074426
  55. DNA polymerases and somatic hypermutation of immunoglobulin genes.
    EMBO Rep. 2005 Dec;6(12):1143-8 PMID: 16319960
  56. Gel fidelity assay measuring nucleotide misinsertion, exonucleolytic proofreading, and lesion bypass efficiencies.
    Methods Enzymol. 1995;262:232-56 PMID: 8594351
  57. Targeting and subsequent selection of somatic hypermutations in the human V kappa repertoire.
    Eur J Immunol. 1999 Oct;29(10):3122-32 PMID: 10540323
  58. Epstein-Barr virus and the somatic hypermutation of immunoglobulin genes in Burkitt's lymphoma cells.
    J Virol. 2001 Nov;75(21):10488-92 PMID: 11581418
  59. Human activation-induced cytidine deaminase causes transcription-dependent, strand-biased C to U deaminations.
    Nucleic Acids Res. 2003 Jun 15;31(12):2990-4 PMID: 12799424
  60. Activation-induced cytidine deaminase turns on somatic hypermutation in hybridomas.
    Nature. 2002 Feb 14;415(6873):802-6 PMID: 11823785
  61. Somatic hypermutation of immunoglobulin genes is linked to transcription initiation.
    Immunity. 1996 Jan;4(1):57-65 PMID: 8574852
  62. Somatic hypermutation in MutS homologue (MSH)3-, MSH6-, and MSH3/MSH6-deficient mice reveals a role for the MSH2-MSH6 heterodimer in modulating the base substitution pattern.
    J Exp Med. 2000 Feb 7;191(3):579-84 PMID: 10662804
  63. Strand-specific mismatch correction in nuclear extracts of human and Drosophila melanogaster cell lines.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5837-41 PMID: 2116007
  64. Heteroduplex repair in extracts of human HeLa cells.
    J Biol Chem. 1991 Feb 25;266(6):3744-51 PMID: 1995629
  65. Uracil-initiated base excision DNA repair synthesis fidelity in human colon adenocarcinoma LoVo and Escherichia coli cell extracts.
    Prog Nucleic Acid Res Mol Biol. 2001;68:165-88 PMID: 11554295
  66. DNA polymerases eta and theta function in the same genetic pathway to generate mutations at A/T during somatic hypermutation of Ig genes.
    J Biol Chem. 2007 Jun 15;282(24):17387-94 PMID: 17449470
  67. Correlation of somatic hypermutation specificity and A-T base pair substitution errors by DNA polymerase eta during copying of a mouse immunoglobulin kappa light chain transgene.
    Proc Natl Acad Sci U S A. 2002 Jul 23;99(15):9954-9 PMID: 12119399
  68. Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation.
    Nature. 2003 Jul 3;424(6944):103-7 PMID: 12819663
  69. Impact of phosphorylation and phosphorylation-null mutants on the activity and deamination specificity of activation-induced cytidine deaminase.
    J Biol Chem. 2008 Jun 20;283(25):17428-39 PMID: 18417471
  70. Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage.
    Mol Cell. 2004 May 21;14(4):491-500 PMID: 15149598
  71. Reward versus risk: DNA cytidine deaminases triggering immunity and disease.
    Biochemistry. 2005 Mar 1;44(8):2703-15 PMID: 15723516
  72. Evolutionary and somatic selection of the antibody repertoire in the mouse.
    Science. 1987 Nov 20;238(4830):1088-94 PMID: 3317826
  73. Regulation of hypermutation by activation-induced cytidine deaminase phosphorylation.
    Proc Natl Acad Sci U S A. 2006 Jun 6;103(23):8798-803 PMID: 16723391
  74. Increased hypermutation at G and C nucleotides in immunoglobulin variable genes from mice deficient in the MSH2 mismatch repair protein.
    J Exp Med. 1998 Jun 1;187(11):1745-51 PMID: 9607916
  75. Strand-biased defect in C/G transversions in hypermutating immunoglobulin genes in Rev1-deficient mice.
    J Exp Med. 2006 Feb 20;203(2):319-23 PMID: 16476771
  76. Mechanism and regulation of class switch recombination.
    Annu Rev Immunol. 2008;26:261-92 PMID: 18370922
  77. Somatic hypermutation and class switch recombination in Msh6(-/-)Ung(-/-) double-knockout mice.
    J Immunol. 2006 Oct 15;177(8):5386-92 PMID: 17015724
  78. CD40-mediated p38 mitogen-activated protein kinase activation is required for immunoglobulin class switch recombination to IgE.
    J Allergy Clin Immunol. 2002 Sep;110(3):421-8 PMID: 12209089
  79. 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
  80. Biochemical analysis of hypermutational targeting by wild type and mutant activation-induced cytidine deaminase.
    J Biol Chem. 2004 Dec 3;279(49):51612-21 PMID: 15371439
  81. PKA-mediated phosphorylation regulates the function of activation-induced deaminase (AID) in B cells.
    Proc Natl Acad Sci U S A. 2006 Jan 10;103(2):395-400 PMID: 16387847
  82. The majority of human tonsillar CD5+ B cells express somatically mutated V kappa 4 genes.
    Eur J Immunol. 1993 Jun;23(6):1405-8 PMID: 7684690
  83. Strand-biased spreading of mutations during somatic hypermutation.
    Science. 2007 Aug 31;317(5842):1227-30 PMID: 17761884
  84. Both DNA strands of antibody genes are hypermutation targets.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8791-4 PMID: 9671757
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2008-11-14
Epub
2008-00-11
Pages
31754-62
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2581569
Subset
IM
Grants
NIEHS NIH HHS · ES013192 · United States
NIGMS NIH HHS · R37GM21422 · United States
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