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PMID: 19684020 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Biochemical basis of immunological and retroviral responses to DNA-targeted cytosine deamination by activation-induced cytidine deaminase and APOBEC3G.

The Journal of biological chemistry ·Vol. 284 ·No. 41 ·2009-10-09 ·Pages 27761-27765

Chelico L, Pham P, Petruska J, Goodman MF

Abstract

Activation-induced cytidine deaminase (AID) and APOBEC3G catalyze deamination of cytosine to uracil on single-stranded DNA, thereby setting in motion a regulated hypermutagenic process essential for human well-being. However, if regulation fails, havoc ensues. AID plays a central role in the synthesis of high affinity antibodies, and APOBEC3G inactivates human immunodeficiency virus-1. This minireview highlights biochemical and structural properties of AID and APOBEC3G, showing how studies using the purified enzymes provide valuable insight into the considerably more complex biology governing antibody generation and human immunodeficiency virus inactivation.

MeSH Terms
APOBEC-3G Deaminase Animals Base Pair Mismatch Cytidine Deaminase/chemistry,genetics,immunology Cytosine/chemistry,metabolism DNA, Single-Stranded/genetics,metabolism HIV-1/immunology Humans Immunoglobulins/chemistry,genetics,immunology Models, Molecular Protein Structure, Quaternary Protein Structure, Tertiary Protein Subunits/chemistry,genetics,metabolism Retroviridae/genetics,metabolism Somatic Hypermutation, Immunoglobulin/genetics,immunology Uracil/chemistry,metabolism
Chemicals
DNA, Single-Stranded Immunoglobulins Protein Subunits Uracil Cytosine AICDA (activation-induced cytidine deaminase) APOBEC-3G Deaminase APOBEC3G protein, human Cytidine Deaminase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Chelico Linda
Department of Biological Sciences, Molecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089-2910.
Pham Phuong
Department of Biological Sciences, Molecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089-2910.
Petruska John
Department of Biological Sciences, Molecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089-2910.
Goodman Myron F
Department of Biological Sciences, Molecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089-2910. Electronic address: mgoodman@usc.edu.
References (50)
50 references, click to expand
  1. Hypermutation by intersegmental transfer of APOBEC3G cytidine deaminase.
    Nat Struct Mol Biol. 2008 Oct;15(10):1059-66 PMID: 18820687
  2. The concerted action of Msh2 and UNG stimulates somatic hypermutation at A . T base pairs.
    Mol Cell Biol. 2009 Sep;29(18):5148-57 PMID: 19596785
  3. The APOBEC-2 crystal structure and functional implications for the deaminase AID.
    Nature. 2007 Jan 25;445(7126):447-51 PMID: 17187054
  4. A model for oligomeric regulation of APOBEC3G cytosine deaminase-dependent restriction of HIV.
    J Biol Chem. 2008 May 16;283(20):13780-91 PMID: 18362149
  5. Comparison of cellular ribonucleoprotein complexes associated with the APOBEC3F and APOBEC3G antiviral proteins.
    J Virol. 2008 Jun;82(11):5636-42 PMID: 18367521
  6. Structure, interaction and real-time monitoring of the enzymatic reaction of wild-type APOBEC3G.
    EMBO J. 2009 Feb 18;28(4):440-51 PMID: 19153609
  7. Mutational comparison of the single-domained APOBEC3C and double-domained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities.
    Nucleic Acids Res. 2005 Apr 04;33(6):1913-23 PMID: 15809227
  8. The current structural and functional understanding of APOBEC deaminases.
    Cell Mol Life Sci. 2009 Oct;66(19):3137-47 PMID: 19547914
  9. 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
  10. 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
  11. Strand-biased spreading of mutations during somatic hypermutation.
    Science. 2007 Aug 31;317(5842):1227-30 PMID: 17761884
  12. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45.
    Cell. 2008 Dec 26;135(7):1201-12 PMID: 19109892
  13. Identification of amino acid residues in APOBEC3G required for regulation by human immunodeficiency virus type 1 Vif and Virion encapsidation.
    J Virol. 2007 Apr;81(8):3807-15 PMID: 17267497
  14. An extended structure of the APOBEC3G catalytic domain suggests a unique holoenzyme model.
    J Mol Biol. 2009 Jun 26;389(5):819-32 PMID: 19389408
  15. Interference of mismatch and base excision repair during the processing of adjacent U/G mispairs may play a key role in somatic hypermutation.
    Proc Natl Acad Sci U S A. 2009 Apr 7;106(14):5593-8 PMID: 19307563
  16. Extensive mutagenesis experiments corroborate a structural model for the DNA deaminase domain of APOBEC3G.
    FEBS Lett. 2007 Oct 2;581(24):4761-6 PMID: 17869248
  17. 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
  18. The activation-induced cytidine deaminase (AID) efficiently targets DNA in nucleosomes but only during transcription.
    J Exp Med. 2009 May 11;206(5):1057-71 PMID: 19380635
  19. Model structure of human APOBEC3G.
    PLoS One. 2007 Apr 18;2(4):e378 PMID: 17440614
  20. Estrogen directly activates AID transcription and function.
    J Exp Med. 2009 Jan 16;206(1):99-111 PMID: 19139166
  21. 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
  22. A portable hot spot recognition loop transfers sequence preferences from APOBEC family members to activation-induced cytidine deaminase.
    J Biol Chem. 2009 Aug 21;284(34):22898-904 PMID: 19561087
  23. Nanostructures of APOBEC3G support a hierarchical assembly model of high molecular mass ribonucleoprotein particles from dimeric subunits.
    J Biol Chem. 2006 Dec 15;281(50):38122-6 PMID: 17079235
  24. Role of AID in tumorigenesis.
    Adv Immunol. 2007;94:245-73 PMID: 17560277
  25. RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1.
    PLoS Pathog. 2009 Mar;5(3):e1000330 PMID: 19266078
  26. AID upmutants isolated using a high-throughput screen highlight the immunity/cancer balance limiting DNA deaminase activity.
    Nat Struct Mol Biol. 2009 Jul;16(7):769-76 PMID: 19543289
  27. AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations.
    Cell. 2008 Dec 12;135(6):1028-38 PMID: 19070574
  28. 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
  29. Replication protein A interacts with AID to promote deamination of somatic hypermutation targets.
    Nature. 2004 Aug 26;430(7003):992-8 PMID: 15273694
  30. The biochemistry of somatic hypermutation.
    Annu Rev Immunol. 2008;26:481-511 PMID: 18304001
  31. Competitive repair pathways in immunoglobulin gene hypermutation.
    Philos Trans R Soc Lond B Biol Sci. 2009 Mar 12;364(1517):613-9 PMID: 19010770
  32. Restriction of HIV-1 by APOBEC3G is cytidine deaminase-dependent.
    Virology. 2009 May 10;387(2):313-21 PMID: 19304304
  33. APOBEC3G DNA deaminase acts processively 3' --> 5' on single-stranded DNA.
    Nat Struct Mol Biol. 2006 May;13(5):392-9 PMID: 16622407
  34. The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements.
    Annu Rev Immunol. 2008;26:317-53 PMID: 18304004
  35. APOBEC3G subunits self-associate via the C-terminal deaminase domain.
    J Biol Chem. 2008 Nov 28;283(48):33329-36 PMID: 18842592
  36. Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation.
    Nature. 2003 Jul 3;424(6944):103-7 PMID: 12819663
  37. Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications.
    Nature. 2008 Nov 6;456(7218):121-4 PMID: 18849968
  38. 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
  39. Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming.
    J Biol Chem. 2004 Dec 10;279(50):52353-60 PMID: 15448152
  40. Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions.
    Science. 2008 Apr 11;320(5873):230-3 PMID: 18403710
  41. AID constrains germinal center size by rendering B cells susceptible to apoptosis.
    Blood. 2009 Jul 16;114(3):547-54 PMID: 19478044
  42. Hypermutation at A/T sites during G.U mismatch repair in vitro by human B-cell lysates.
    J Biol Chem. 2008 Nov 14;283(46):31754-62 PMID: 18786917
  43. Interaction between antibody-diversification enzyme AID and spliceosome-associated factor CTNNBL1.
    Mol Cell. 2008 Aug 22;31(4):474-484 PMID: 18722174
  44. A cis-acting diversification activator both necessary and sufficient for AID-mediated hypermutation.
    PLoS Genet. 2009 Jan;5(1):e1000332 PMID: 19132090
  45. Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells.
    Nature. 2005 May 5;435(7038):108-14 PMID: 15829920
  46. Twin gradients in APOBEC3 edited HIV-1 DNA reflect the dynamics of lentiviral replication.
    Nucleic Acids Res. 2006;34(17):4677-84 PMID: 16963778
  47. Dissecting APOBEC3G substrate specificity by nucleoside analog interference.
    J Biol Chem. 2009 Mar 13;284(11):7047-58 PMID: 19136562
  48. V-region mutation in vitro, in vivo, and in silico reveal the importance of the enzymatic properties of AID and the sequence environment.
    Proc Natl Acad Sci U S A. 2009 May 26;106(21):8629-34 PMID: 19443686
  49. Two levels of protection for the B cell genome during somatic hypermutation.
    Nature. 2008 Feb 14;451(7180):841-5 PMID: 18273020
  50. Mechanism and regulation of class switch recombination.
    Annu Rev Immunol. 2008;26:261-92 PMID: 18370922
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2009-10-09
Epub
2009-00-13
Pages
27761-27765
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2788826
Subset
IM
Grants
NIEHS NIH HHS · R01 ES013192 · United States
NIGMS NIH HHS · R37GM21422 · United States
NIEHS NIH HHS · ES013192 · United States
NIEHS NIH HHS · R56 ES013192 · United States
NIGMS NIH HHS · R37 GM021422 · United States
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