Active nuclear import and cytoplasmic retention of activation-induced deaminase

Nature Structural and Molecular Biology

Volumn 16, Issue 5, 2009, Pages 517-527

  Patenaude, Anne Marie ^a   Orthwein, Alexandre ^a,b   Hu, Yi ^a,c   Campo, Vanina A ^a   Kavli, Bodil ^c   Buschiazzo, Alejandro ^d,e   Di Noia, Javier M ^a,b  

^a Rehabilitation Institute of Montreal   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; AICDA (ACTIVATION INDUCED CYTIDINE DEAMINASE); AICDA (ACTIVATION-INDUCED CYTIDINE DEAMINASE); CYTIDINE DEAMINASE; KARYOPHERIN ALPHA;

ARTICLE; B LYMPHOCYTE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; DEAMINATION; GENE MUTATION; IMMUNOGLOBULIN GENE; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; ACTIVE TRANSPORT; CELL FRACTIONATION; CELL NUCLEUS; CHEMICAL STRUCTURE; CHEMISTRY; DIFFUSION; ENZYMOLOGY; HELA CELL; HUMAN; METABOLISM; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; CELL NUCLEUS; CYTIDINE DEAMINASE; DIFFUSION; HELA CELLS; HUMANS; MODELS, MOLECULAR; NUCLEAR LOCALIZATION SIGNALS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SUBCELLULAR FRACTIONS;

EID: 66149126655     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1598     Document Type: Article

References (59)

1. Muramatsu, M. et al. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553-563 (2000).
2. Revy, P. et al. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 102, 565-575 (2000).
3. Peled, J.U. et al. The biochemistry of somatic hypermutation. Annu. Rev. Immunol. 26, 481-511 (2007).
4. Di Noia, J.M. & Neuberger, M.S. Molecular mechanisms of antibody somatic hyper-mutation. Annu. Rev. Biochem. 76, 1-22 (2007).
5. Chaudhuri, J. et al. Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv. Immunol. 94, 157-214 (2007).
6. Martin, A. & Scharff, M.D. Somatic hypermutation of the AID transgene in B and non-B cells. Proc. Natl. Acad. Sci. USA 99, 12304-12308 (2002).
7. Okazaki, I.M. et al. Constitutive expression of AID leads to tumorigenesis. J. Exp. Med. 197, 1173-1181 (2003).
8. Liu, M. et al. Two levels of protection for the B cell genome during somatic hypermutation. Nature 451, 841-845 (2008).
9. Pasqualucci, L. et al. BCL-6 mutations in normal germinal center B cells: evidence of somatic hypermutation acting outside Ig loci. Proc. Natl. Acad. Sci. USA 95, 11816-11821 (1998).
10. Shen, H.M., Peters, A., Baron, B., Zhu, X. & Storb, U. Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes. Science 280, 1750-1752 (1998).
11. Dorsett, Y. et al. A role for AID in chromosome translocations between c-myc and the IgH variable region. J. Exp. Med. 204, 2225-2232 (2007).
12. Ramiro, A.R. et al. AID is required for c-myc/IgH chromosome translocations in vivo. Cell 118, 431-438 (2004).
13. Crouch, E.E. et al. Regulation of AID expression in the immune response. J. Exp. Med. 204, 1145-1156 (2007).
14. de Yébenes, V.G. et al. miR-181b negatively regulates activation-induced cytidine deaminase in B cells. J. Exp. Med. 205, 2199-2206 (2008).
15. Dorsett, Y. et al. MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity 28, 630-638 (2008).
16. Teng, G. et al. MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 28, 621-629 (2008).
17. Ito, S. et al. Activation-induced cytidine deaminase shuttles between nucleus and cytoplasm like apolipoprotein B mRNA editing catalytic polypeptide 1. Proc. Natl. Acad. Sci. USA 101, 1975-1980 (2004).
18. McBride, K.M., Barreto, V.M., Ramiro, A.R., Stavropoulos, P. & Nussenzweig, M.C. Somatic hypermutation is limited by CRM1-dependent nuclear export of activation-induced deaminase. J. Exp. Med. 199, 1235-1244 (2004).
19. Aoufouchi, S. et al. Proteasomal degradation restricts the nuclear lifespan of AID. J. Exp. Med. 205, 1357-1368 (2008).
20. Basu, U. et al. The AID antibody diversification enzyme is regulated by protein kinase A phosphorylation. Nature 438, 508-511 (2005).
21. McBride, K.M. et al. Regulation of hypermutation by activation-induced cytidine deaminase phosphorylation. Proc. Natl. Acad. Sci. USA 103, 8798-8803 (2006).
22. Pasqualucci, L., Kitaura, Y., Gu, H. & Dalla-Favera, R. PKA-mediated phosphorylation regulates the function of activation-induced deaminase (AID) in B cells. Proc. Natl. Acad. Sci. USA 103, 395-400 (2006).
23. Rada, C., Jarvis, J.M. & Milstein, C. AID-GFP chimeric protein increases hypermutation of Ig genes with no evidence of nuclear localization. Proc. Natl. Acad. Sci. USA 99, 7003-7008 (2002).
24. Brar, S.S., Watson, M. & Diaz, M. Activation-induced cytosine deaminase (AID) is actively exported out of the nucleus but retained by the induction of DNA breaks. J. Biol. Chem. 279, 26395-26401 (2004).
25. Richardson, W.D., Mills, A.D., Dilworth, S.M., Laskey, R.A. & Dingwall, C. Nuclear protein migration involves two steps: rapid binding at the nuclear envelope followed by slower translocation through nuclear pores. Cell 52, 655-664 (1988).
26. Newmeyer, D.D. & Forbes, D.J. Nuclear import can be separated into distinct steps in vitro: nuclear pore binding and translocation. Cell 52, 641-653 (1988).
27. Guiochon-Mantel, A. et al. Nucleocytoplasmic shuttling of the progesterone receptor. EMBO J. 10, 3851-3859 (1991).
28. Larijani, M. et al. AID associates with single-stranded DNA with high affinity and a long complex half-life in a sequence-independent manner. Mol. Cell. Biol. 27, 20-30 (2007).
29. Macara, I.G. Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev. 65, 570-594 (2001).
30. Görlich, D. & Kutay, U. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15, 607-660 (1999).
31. Chen, K.M. et al. Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452, 116-119 (2008).
32. Holden, L.G. et al. Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456, 121-124 (2008).
33. Prochnow, C. et al. The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 445, 447-451 (2007).
34. Nilsen, H. et al. Analysis of uracil-DNA glycosylases from the murine Ung gene reveals differential expression in tissues and in embryonic development and a subcellular sorting pattern that differs from the human homologues. Nucleic Acids Res. 28, 2277-2285 (2000).
35. Conticello, S.G. et al. Interaction between antibody- diversification enzyme AID and spliceosome-associated factor CTNNBL1. Mol. Cell 31, 474-484 (2008).
36. Lange, A. et al. Classical nuclear localization signals: definition, function, and interaction with importinα. J. Biol. Chem. 282, 5101-5105 (2007).
37. Miyamoto, Y. et al. Cellular stresses induce the nuclear accumulation of importin a and cause a conventional nuclear import block. J. Cell Biol. 165, 617-623 (2004).
38. Kodiha, M., Chu, A., Matusiewicz, N. & Stochaj, U. Multiple mechanisms promote the inhibition of classical nuclear import upon exposure to severe oxidative stress. Cell Death Differ. 11, 862-874 (2004).
39. Shivarov, V., Shinkura, R. & Honjo, T. Dissociation of in vitro DNA deamination activity and physiological functions of AID mutants. Proc. Natl. Acad. Sci. USA 105, 15866-15871 (2008).
40. Doi, T. et al. The C-terminal region of activation-induced cytidine deaminase is responsible for a recombination function other than DNA cleavage in class switch recombination. Proc. Natl. Acad. Sci. USA 106, 2758-2763 (2009).
41. Barreto, V., Reina-San-Martin, B., Ramiro, A.R., McBride, K.M. & Nussenzweig, M.C. C-terminal deletion of AID uncouples class switch recombination from somatic hypermutation and gene conversion. Mol. Cell 12, 501-508 (2003).
42. Ta, V. et al. AID mutant analyses indicate requirement for class-switch-specific cofactors. Nat. Immunol. 4, 843-848 (2003).
43. Shinkura, R. et al. Separate domains of AID are required for somatic hypermutation and class-switch recombination. Nat. Immunol. 5, 707-712 (2004).
44. LaCasse, E.C. & Lefebvre, Y.A. Nuclear localization signals overlap DNA- or RNA-binding domains in nucleic acid-binding proteins. Nucleic Acids Res. 23, 1647-1656 (1995).
45. Chester, A. et al. The apolipoprotein B mRNA editing complex performs a multifunctional cycle and suppresses nonsense-mediated decay. EMBO J. 22, 3971-3982 (2003).
46. Yang, Y. & Smith, H.C. Multiple protein domains determine the cell type-specific nuclear distribution of the catalytic subunit required for apolipoprotein B mRNA editing. Proc. Natl. Acad. Sci. USA 94, 13075-13080 (1997).
47. Dickerson, S.K., Market, E., Besmer, E. & Papavasiliou, F.N. AID mediates hypermuta-tion by deaminating single stranded DNA. J. Exp. Med. 197, 1291-1296 (2003).
48. Yang, G. et al. Activation-induced deaminase cloning, localization, and protein extraction from young VH-mutant rabbit appendix. Proc. Natl. Acad. Sci. USA 102, 17083-17088 (2005).
49. Bennett, R.P., Presnyak, V., Wedekind, J.E. & Smith, H.C. Nuclear exclusion of the HIV-1 host defense factor APOBEC3G requires a novel cytoplasmic retention signal and is not dependent on RNA binding. J. Biol. Chem. 283, 7320-7327 (2008).
50. Lau, P.P., Zhu, H.J., Baldini, A., Charnsangavej, C. & Chan, L. Dimeric structure of a human apolipoprotein B mRNA editing protein and cloning and chromosomal localization of its gene. Proc. Natl. Acad. Sci. USA 91, 8522-8526 (1994).
51. Stenglein, M.D., Matsuo, H. & Harris, R.S. Two regions within the amino-terminal half of APOBEC3G cooperate to determine cytoplasmic localization. J. Virol. 82, 9591-9599 (2008).
52. Wu, X., Geraldes, P., Platt, J.L. & Cascalho, M. The double-edged sword of activation-induced cytidine deaminase. J. Immunol. 174, 934-941 (2005).
53. Cattoretti, G. et al. Nuclear and cytoplasmic AID in extrafollicular and germinal center B cells. Blood 107, 3967-3975 (2006).
54. Greiner, A. et al. Differential expression of activation-induced cytidine deaminase (AID) in nodular lymphocyte-predominant and classical Hodgkin lymphoma. J. Pathol. 205, 541-547 (2005).
55. Pasqualucci, L. et al. Expression of the AID protein in normal and neoplastic B cells. Blood 104, 3318-3325 (2004).
56. Petersen-Mahrt, S.K., Harris, R.S. & Neuberger, M.S. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418, 99-104 (2002).
57. Di Noia, J.M. et al. Dependence of antibody gene diversification on uracil excision. J. Exp. Med. 204, 3209-3219 (2007).
58. Kitamura, T. et al. Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp. Hematol. 31, 1007-1014 (2003).
59. Zhang, W. et al. Clonal instability of V region hypermutation in the Ramos Burkitt's lymphoma cell line. Int. Immunol. 13, 1175-1184 (2001).