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Biological Chemistry

Editor-in-Chief: Brüne, Bernhard

Editorial Board: Buchner, Johannes / Lei, Ming / Ludwig, Stephan / Thomas, Douglas D. / Turk, Boris / Wittinghofer, Alfred


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Volume 394, Issue 11

Issues

Structural features of antiviral DNA cytidine deaminases

Ananda Ayyappan Jaguva Vasudevan
  • Clinic for Gastroenterology, Hepatology, and Infectiology, Medical Faculty, Heinrich-Heine-University, D-40225 Düsseldorf, Germany
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Sander H.J. Smits / Astrid Höppner / Dieter Häussinger
  • Clinic for Gastroenterology, Hepatology, and Infectiology, Medical Faculty, Heinrich-Heine-University, D-40225 Düsseldorf, Germany
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Bernd W. Koenig
  • Institute of Structural Biochemistry (ICS-6), Research Centre Jülich, D-52425 Jülich, Germany
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  • De Gruyter OnlineGoogle Scholar
/ Carsten Münk
  • Corresponding author
  • Clinic for Gastroenterology, Hepatology, and Infectiology, Medical Faculty, Heinrich-Heine-University, D-40225 Düsseldorf, Germany
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2013-06-20 | DOI: https://doi.org/10.1515/hsz-2013-0165

Abstract

The APOBEC3 (A3) family of cytidine deaminases plays a vital role for innate defense against retroviruses. Lentiviruses such as HIV-1 evolved the Vif protein that triggers A3 protein degradation. There are seven A3 proteins, A3A-A3H, found in humans. All A3 proteins can deaminate cytidines to uridines in single-stranded DNA (ssDNA), generated during viral reverse transcription. A3 proteins have either one or two cytidine deaminase domains (CD). The CDs coordinate a zinc ion, and their amino acid specificity classifies the A3s into A3Z1, A3Z2, and A3Z3. A3 proteins occur as monomers, dimers, and large oligomeric complexes. Studies on the nature of A3 oligomerization, as well as the mode of interaction of A3s with RNA and ssDNA are partially controversial. High-resolution structures of the catalytic CD2 of A3G and A3F as well as of the single CD proteins A3A and A3C have been published recently. The NMR and X-ray crystal structures show globular proteins with six α-helices and five β sheets arranged in a characteristic motif (α1-β1-β2/2′-α2-β3-α3-β4-α4-β5-α5-α6). However, the detailed arrangement and extension of individual structure elements and their relevance for A3 complex formation and activity remains a matter of debate and will be highlighted in this review.

Keywords: APOBEC3G; HIV-1; homology modeling; NMR; Vif; X-ray

References

  • Albin, J.S. and Harris, R.S. (2010). Interactions of host APOBEC3 restriction factors with HIV-1 in vivo: implications for therapeutics. Expert. Rev. Mol. Med 12, e4.Google Scholar

  • Albin, J.S., LaRue, R.S., Weaver, J.A., Brown, W.L., Shindo, K., Harjes, E., Matsuo, H., and Harris, R.S. (2010). A single amino acid in human APOBEC3F alters susceptibility to HIV-1 Vif. J. Biol. Chem. 285, 40785–40792.Google Scholar

  • Arias, J.F., Koyama, T., Kinomoto, M., and Tokunaga, K. (2012). Retroelements versus APOBEC3 family members: no great escape from the magnificent seven. Front. Microbiol. 3, 275.Google Scholar

  • Autore, F., Bergeron, J.R., Malim, M.H., Fraternali, F., and Huthoff, H. (2010). Rationalisation of the differences between APOBEC3G structures from crystallography and NMR studies by molecular dynamics simulations. PLoS One. 5, e11515.Google Scholar

  • Bennett, R.P., Salter, J.D., Liu, X., Wedekind, J.E., and Smith, H.C. (2008). APOBEC3G subunits self-associate via the C-terminal deaminase domain. J. Biol. Chem. 283, 33329–33336.Google Scholar

  • Bergeron, J.R., Huthoff, H., Veselkov, D.A., Beavil, R.L., Simpson, P.J., Matthews, S.J., Malim, M.H., and Sanderson, M.R. (2010). The SOCS-box of HIV-1 Vif interacts with ElonginBC by induced-folding to recruit its Cul5-containing ubiquitin ligase complex. PLoS Pathog. 6, e1000925.Google Scholar

  • Bohn, M.F., Shandilya, S.M., Albin, J.S., Kouno, T., Anderson, B.D., McDougle, R.M., Carpenter, M.A., Rathore, A., Evans, L., Davis, A.N., et al. (2013). Crystal structure of the DNA cytosine deaminase APOBEC3F: the catalytically active and HIV-1 Vif-binding domain. Structure 21, 1042–1050.Google Scholar

  • Bulliard, Y., Turelli, P., Rohrig, U.F., Zoete, V., Mangeat, B., Michielin, O., and Trono, D. (2009). Functional analysis and structural modeling of human APOBEC3G reveal the role of evolutionarily conserved elements in the inhibition of human immunodeficiency virus type 1 infection and Alu transposition. J. Virol. 83, 12611–12621.Google Scholar

  • Burnett, A. and Spearman, P. (2007). APOBEC3G multimers are recruited to the plasma membrane for packaging into human immunodeficiency virus type 1 virus-like particles in an RNA-dependent process requiring the NC basic linker. J. Virol. 81, 5000–5013.Google Scholar

  • Burns, M.B., Lackey, L., Carpenter, M.A., Rathore, A., Land, A.M., Leonard, B., Refsland, E.W., Kotandeniya, D., Tretyakova, N., Nikas, J.B., et al. (2013). APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494, 366–370.Google Scholar

  • Byeon, I.J., Ahn, J., Mitra, M., Byeon, C.H., Hercik, K., Hritz, J., Charlton, L.M., Levin, J.G., and Gronenborn, A.M. (2013). NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat. Commun. 4, 1890.Google Scholar

  • Chareza, S., Slavkovic, L.D., Liu, Y., Rathe, A.M., Münk, C., Zabogli, E., Pistello, M., and Löchelt, M. (2012). Molecular and functional interactions of cat APOBEC3 and feline foamy and immunodeficiency virus proteins: different ways to counteract host-encoded restriction. Virology 424, 138–146.Google Scholar

  • Chelico, L., Pham, P., Calabrese, P., and Goodman, M.F. (2006). APOBEC3G DNA deaminase acts processively 3′→5′ on single-stranded DNA. Nat. Struct. Mol. Biol 13, 392–399.Google Scholar

  • Chelico, L., Sacho, E.J., Erie, D.A., and Goodman, M.F. (2008). A model for oligomeric regulation of APOBEC3G cytosine deaminase-dependent restriction of HIV. J. Biol. Chem. 283, 13780–13791.Google Scholar

  • Chelico, L., Prochnow, C., Erie, D.A., Chen, X.S., and Goodman, M.F. (2010). Structural model for deoxycytidine deamination mechanisms of the HIV-1 inactivation enzyme APOBEC3G. J. Biol. Chem. 285, 16195–16205.Google Scholar

  • Chen, K.M., Harjes, E., Gross, P.J., Fahmy, A., Lu, Y., Shindo, K., Harris, R.S., and Matsuo, H. (2008). Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452, 116–119.Google Scholar

  • Chiu, Y.L., Witkowska, H.E., Hall, S.C., Santiago, M., Soros, V.B., Esnault, C., Heidmann, T., and Greene, W.C. (2006). High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition. Proc. Natl. Acad. Sci. USA 103, 15588–15593.Google Scholar

  • Conticello, S.G. (2008). The AID/APOBEC family of nucleic acid mutators. Genome Biol. 9, 229.PubMedGoogle Scholar

  • Derse, D., Hill, S.A., Princler, G., Lloyd, P., and Heidecker, G. (2007). Resistance of human T cell leukemia virus type 1 to APOBEC3G restriction is mediated by elements in nucleocapsid. Proc. Natl. Acad. Sci. USA 104, 2915–2920.Google Scholar

  • Feng, Y. and Chelico, L. (2011). Intensity of deoxycytidine deamination of HIV-1 proviral DNA by the retroviral restriction factor APOBEC3G is mediated by the noncatalytic domain. J. Biol. Chem. 286, 11415–11426.Google Scholar

  • Friew, Y.N., Boyko, V., Hu, W.S., and Pathak, V.K. (2009). Intracellular interactions between APOBEC3G, RNA, and HIV-1 Gag: APOBEC3G multimerization is dependent on its association with RNA. Retrovirology 6, 56.Google Scholar

  • Furukawa, A., Nagata, T., Matsugami, A., Habu, Y., Sugiyama, R., Hayashi, F., Kobayashi, N., Yokoyama, S., Takaku, H., and Katahira, M. (2009). Structure, interaction and real-time monitoring of the enzymatic reaction of wild-type APOBEC3G. EMBO J. 28, 440–451.Google Scholar

  • Gallois-Montbrun, S., Kramer, B., Swanson, C.M., Byers, H., Lynham, S., Ward, M., and Malim, M.H. (2007). Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J. Virol. 81, 2165–2178.Google Scholar

  • Gallois-Montbrun, S., Holmes, R.K., Swanson, C.M., Fernandez-Ocana, M., Byers, H.L., Ward, M.A., and Malim, M.H. (2008). Comparison of cellular ribonucleoprotein complexes associated with the APOBEC3F and APOBEC3G antiviral proteins. J. Virol. 82, 5636–5642.Google Scholar

  • Hache, G., Liddament, M.T., and Harris, R.S. (2005). The retroviral hypermutation specificity of APOBEC3F and APOBEC3G is governed by the C-terminal DNA cytosine deaminase domain. J. Biol. Chem. 280, 10920–10924.Google Scholar

  • Harjes, E., Gross, P.J., Chen, K.M., Lu, Y., Shindo, K., Nowarski, R., Gross, J.D., Kotler, M., Harris, R.S., and Matsuo, H. (2009). An extended structure of the APOBEC3G catalytic domain suggests a unique holoenzyme model. J. Mol. Biol 389, 819–832.Google Scholar

  • Harris, R.S., Petersen-Mahrt, S.K., and Neuberger, M.S. (2002). RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol. Cell 10, 1247–1253.Google Scholar

  • Holden, L.G., Prochnow, C., Chang, Y.P., Bransteitter, R., Chelico, L., Sen, U., Stevens, R.C., Goodman, M.F., and Chen, X.S. (2008). Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456, 121–124.Google Scholar

  • Huthoff, H., Autore, F., Gallois-Montbrun, S., Fraternali, F., and Malim, M.H. (2009). RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog. 5, e1000330.Google Scholar

  • Iwatani, Y., Takeuchi, H., Strebel, K., and Levin, J.G. (2006). Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect. J. Virol. 80, 5992–6002.Google Scholar

  • Jager, S., Kim, D.Y., Hultquist, J.F., Shindo, K., LaRue, R.S., Kwon, E., Li, M., Anderson, B.D., Yen, L., Stanley, D., et al. (2012). Vif hijacks CBF-β to degrade APOBEC3G and promote HIV-1 infection. Nature 481, 371–375.Google Scholar

  • Jaguva Vasudevan, A.A., Perkovic, M., Bulliard, Y., Cichutek, K., Trono, D., Haussinger, D., and Munk, C. (2013). Prototype foamy virus bet impairs the dimerization and cytosolic solubility of human APOBEC3G. J. Virol. 2013 Jun 12. [Epub ahead of print].CrossrefGoogle Scholar

  • Jarmuz, A., Chester, A., Bayliss, J., Gisbourne, J., Dunham, I., Scott, J., and Navaratnam, N. (2002). An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 79, 285–296.Google Scholar

  • Kitamura, S., Ode, H., Nakashima, M., Imahashi, M., Naganawa, Y., Kurosawa, T., Yokomaku, Y., Yamane, T., Watanabe, N., Suzuki, A., et al. (2012). The APOBEC3C crystal structure and the interface for HIV-1 Vif binding. Nat. Struct. Mol. Biol 19, 1005–1010.Google Scholar

  • Kolokithas, A., Rosenke, K., Malik, F., Hendrick, D., Swanson, L., Santiago, M.L., Portis, J.L., Hasenkrug, K.J., and Evans, L.H. (2010). The glycosylated Gag protein of a murine leukemia virus inhibits the antiretroviral function of APOBEC3. J. Virol. 84, 10933–10936.Google Scholar

  • Kozak, S.L., Marin, M., Rose, K.M., Bystrom, C., and Kabat, D. (2006). The anti-HIV-1 editing enzyme APOBEC3G binds HIV-1 RNA and messenger RNAs that shuttle between polysomes and stress granules. J. Biol. Chem. 281, 29105–29119.Google Scholar

  • Kreisberg, J.F., Yonemoto, W., and Greene, W.C. (2006). Endogenous factors enhance HIV infection of tissue naive CD4 T cells by stimulating high molecular mass APOBEC3G complex formation. J. Exp. Med. 203, 865–870.Google Scholar

  • Krissinel, E. and Henrick, K. (2007). Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774–797.Google Scholar

  • LaRue, R.S., Jonsson, S.R., Silverstein, K.A., Lajoie, M., Bertrand, D., El-Mabrouk, N., Hotzel, I., Andresdottir, V., Smith, T.P., and Harris, R.S. (2008). The artiodactyl APOBEC3 innate immune repertoire shows evidence for a multi-functional domain organization that existed in the ancestor of placental mammals. Mol. Biol. 9, 104.Google Scholar

  • LaRue, R.S., Andresdottir, V., Blanchard, Y., Conticello, S.G., Derse, D., Emerman, M., Greene, W.C., Jonsson, S.R., Landau, N.R., Löchelt, M., et al. (2009). Guidelines for naming nonprimate APOBEC3 genes and proteins. J. Virol. 83, 494–497.Google Scholar

  • Li, M., Shandilya, S.M., Carpenter, M.A., Rathore, A., Brown, W.L., Perkins, A.L., Harki, D.A., Solberg, J., Hook, D.J., Pandey, K.K., et al. (2012). First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G. ACS Chem. Biol. 7, 506–517.Google Scholar

  • Löchelt, M., Romen, F., Bastone, P., Muckenfuss, H., Kirchner, N., Kim, Y.B., Truyen, U., Rosler, U., Battenberg, M., Saib, A., et al. (2005). The antiretroviral activity of APOBEC3 is inhibited by the foamy virus accessory Bet protein. Proc. Natl. Acad. Sci. USA 102, 7982–7987.Google Scholar

  • Mariani, R., Chen, D., Schröfelbauer, B., Navarro, F., König, R., Bollman, B., Münk, C., Nymark-McMahon, H., and Landau, N.R. (2003). Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114, 21–31.Google Scholar

  • Marin, M., Rose, K.M., Kozak, S.L., and Kabat, D. (2003). HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 9, 1398–1403.PubMedGoogle Scholar

  • Mehle, A., Goncalves, J., Santa-Marta, M., McPike, M., and Gabuzda, D. (2004). Phosphorylation of a novel SOCS-box regulates assembly of the HIV-1 Vif-Cul5 complex that promotes APOBEC3G degradation. Genes Dev. 18, 2861–2866.Google Scholar

  • Münk, C., Beck, T., Zielonka, J., Hotz-Wagenblatt, A., Chareza, S., Battenberg, M., Thielebein, J., Cichutek, K., Bravo, I.G., O’Brien, S.J., et al. (2008). Functions, structure, and read-through alternative splicing of feline APOBEC3 genes. Genome Biol. 9, R48.Google Scholar

  • Münk, C., Jensen, B.E., Zielonka, J., Häussinger, D., and Kamp, C. (2012a). Running loose or getting lost: how HIV-1 counters and capitalizes on APOBEC3-induced mutagenesis through its Vif protein. Viruses 4, 3132–3161.CrossrefGoogle Scholar

  • Münk, C., Willemsen, A., and Bravo, I.G. (2012b). An ancient history of gene duplications, fusions and losses in the evolution of APOBEC3 mutators in mammals. BMC. Evol. Biol 12, 71.Google Scholar

  • Navarro, F., Bollman, B., Chen, H., König, R., Yu, Q., Chiles, K., and Landau, N.R. (2005). Complementary function of the two catalytic domains of APOBEC3G. Virology 333, 374–386.Google Scholar

  • Niewiadomska, A.M., Tian, C., Tan, L., Wang, T., Sarkis, P.T., and Yu, X.F. (2007). Differential inhibition of long interspersed element 1 by APOBEC3 does not correlate with high-molecular-mass-complex formation or P-body association. J. Virol. 81, 9577–9583.Google Scholar

  • Nik-Zainal, S., Alexandrov, L.B., Wedge, D.C., Van, L.P., Greenman, C.D., Raine, K., Jones, D., Hinton, J., Marshall, J., Stebbings, L.A., et al. (2012). Mutational processes molding the genomes of 21 breast cancers. Cell 149, 979–993.Google Scholar

  • Nowarski, R. and Kotler, M. (2013). APOBEC3 cytidine deaminases in double-strand DNA break repair and cancer promotion. Cancer Res. 73, 3494–3498.PubMedGoogle Scholar

  • Nowarski, R., Britan-Rosich, E., Shiloach, T., and Kotler, M. (2008). Hypermutation by intersegmental transfer of APOBEC3G cytidine deaminase. Nat. Struct. Mol. Biol. 15, 1059–1066.PubMedGoogle Scholar

  • Ooms, M., Krikoni, A., Kress, A.K., Simon, V., and Münk, C. (2012). APOBEC3A, APOBEC3B, and APOBEC3H haplotype 2 restrict human T-lymphotropic virus type 1. J. Virol. 86, 6097–6108.Google Scholar

  • Perkovic, M., Schmidt, S., Marino, D., Russell, R.A., Stauch, B., Hofmann, H., Kopietz, F., Kloke, B.P., Zielonka, J., Strover, H., et al. (2009). Species-specific inhibition of APOBEC3C by the prototype foamy virus protein bet. J. Biol. Chem. 284, 5819–5826.Google Scholar

  • Prochnow, C., Bransteitter, R., Klein, M.G., Goodman, M.F., and Chen, X.S. (2007). The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 445, 447–451.Google Scholar

  • Rausch, J.W., Chelico, L., Goodman, M.F., and Le Grice, S.F. (2009). Dissecting APOBEC3G substrate specificity by nucleoside analog interference. J. Biol. Chem. 284, 7047–7058.Google Scholar

  • Roberts, S.A., Sterling, J., Thompson, C., Harris, S., Mav, D., Shah, R., Klimczak, L.J., Kryukov, G.V., Malc, E., Mieczkowski, P.A., et al. (2012). Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol. Cell 46, 424–435.Google Scholar

  • Russell, R.A., Wiegand, H.L., Moore, M.D., Schafer, A., McClure, M.O., and Cullen, B.R. (2005). Foamy virus Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors. J. Virol. 79, 8724–8731.Google Scholar

  • Salter, J.D., Krucinska, J., Raina, J., Smith, H.C., and Wedekind, J.E. (2009). A hydrodynamic analysis of APOBEC3G reveals a monomer-dimer-tetramer self-association that has implications for anti-HIV function. Biochemistry 48, 10685–10687.Google Scholar

  • Schumacher, A.J., Hache, G., MacDuff, D.A., Brown, W.L., and Harris, R.S. (2008). The DNA deaminase activity of human APOBEC3G is required for Ty1, MusD, and human immunodeficiency virus type 1 restriction. J. Virol. 82, 2652–2660.Google Scholar

  • Shandilya, S.M., Nalam, M.N., Nalivaika, E.A., Gross, P.J., Valesano, J.C., Shindo, K., Li, M., Munson, M., Royer, W.E., Harjes, E., et al. (2010). Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18, 28–38.Google Scholar

  • Sheehy, A.M., Gaddis, N.C., Choi, J.D., and Malim, M.H. (2002). Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418, 646–650.Google Scholar

  • Sheehy, A.M., Gaddis, N.C., and Malim, M.H. (2003). The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat. Med. 9, 1404–1407.Google Scholar

  • Shlyakhtenko, L.S., Lushnikov, A.Y., Li, M., Lackey, L., Harris, R.S., and Lyubchenko, Y.L. (2011). Atomic force microscopy studies provide direct evidence for dimerization of the HIV restriction factor APOBEC3G. J. Biol. Chem. 286, 3387–3395.Google Scholar

  • Shlyakhtenko, L.S., Lushnikov, A.Y., Miyagi, A., Li, M., Harris, R.S., and Lyubchenko, Y.L. (2012). Nanoscale structure and dynamics of ABOBEC3G complexes with single-stranded DNA. Biochemistry 51, 6432–6440.Google Scholar

  • Smith, J.L. and Pathak, V.K. (2010). Identification of specific determinants of human APOBEC3F, APOBEC3C, and APOBEC3DE and African green monkey APOBEC3F that interact with HIV-1 Vif. J. Virol. 84, 12599–12608.Google Scholar

  • Song, C., Sutton, L., Johnson, M.E., D’Aquila, R.T., and Donahue, J.P. (2012). Signals in APOBEC3F N-terminal and C-terminal deaminase domains each contribute to encapsidation in HIV-1 virions and are both required for HIV-1 restriction. J. Biol. Chem. 287, 16965–16974.Google Scholar

  • Soros, V.B., Yonemoto, W., and Greene, W.C. (2007). Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA, and subsequently activated by RNase H. PLoS. Pathog. 3, e15.Google Scholar

  • Stauch, B., Hofmann, H., Perkovic, M., Weisel, M., Kopietz, F., Cichutek, K., Münk, C., and Schneider, G. (2009). Model structure of APOBEC3C reveals a binding pocket modulating ribonucleic acid interaction required for encapsidation. Proc. Natl. Acad. Sci. USA 106, 12079–12084.Google Scholar

  • Stavrou, S., Nitta, T., Kotla, S., Ha, D., Nagashima, K., Rein, A.R., Fan, H., and Ross, S.R. (2013). Murine leukemia virus glycosylated Gag blocks apolipoprotein B editing complex 3 and cytosolic sensor access to the reverse transcription complex. Proc. Natl. Acad. Sci. USA 110, 9078–9083. doi: 10.1073/pnas.1217399110. [Epub 2013 May 13].CrossrefGoogle Scholar

  • Strebel, K. and Khan, M.A. (2008). APOBEC3G encapsidation into HIV-1 virions: which RNA is it? Retrovirology 5, 55.Google Scholar

  • Taylor, B.J., Nik-Zainal, S., Wu, Y.L., Stebbings, L.A., Raine, K., Campbell, P.J., Rada, C., Stratton, M.R., and Neuberger, M.S. (2013). DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis. Elife 2, e00534.Google Scholar

  • Teh, A.H., Kimura, M., Yamamoto, M., Tanaka, N., Yamaguchi, I., and Kumasaka, T. (2006). The 1.48 A resolution crystal structure of the homotetrameric cytidine deaminase from mouse. Biochemistry 45, 7825–7833.Google Scholar

  • Wang, T., Zhang, W., Tian, C., Liu, B., Yu, Y., Ding, L., Spearman, P., and Yu, X.F. (2008). Distinct viral determinants for the packaging of human cytidine deaminases APOBEC3G and APOBEC3C. Virology 377, 71–79.Google Scholar

  • Wedekind, J.E., Gillilan, R., Janda, A., Krucinska, J., Salter, J.D., Bennett, R.P., Raina, J., and Smith, H.C. (2006). Nanostructures of APOBEC3G support a hierarchical assembly model of high molecular mass ribonucleoprotein particles from dimeric subunits. J. Biol. Chem. 281, 38122–38126.Google Scholar

  • Wissing, S., Galloway, N.L., and Greene, W.C. (2010). HIV-1 Vif versus the APOBEC3 cytidine deaminases: an intracellular duel between pathogen and host restriction factors. Mol. Aspects Med. 31, 383–397.Google Scholar

  • Xiang, S., Short, S.A., Wolfenden, R., and Carter, C.W., Jr. (1997). The structure of the cytidine deaminase-product complex provides evidence for efficient proton transfer and ground-state destabilization. Biochemistry 36, 4768–4774.Google Scholar

  • Yu, X., Yu, Y., Liu, B., Luo, K., Kong, W., Mao, P., and Yu, X.F. (2003). Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302, 1056–1060.Google Scholar

  • Yu, Y., Xiao, Z., Ehrlich, E.S., Yu, X., and Yu, X.F. (2004). Selective assembly of HIV-1 Vif-Cul5-ElonginB-ElonginC E3 ubiquitin ligase complex through a novel SOCS box and upstream cysteines. Genes Dev. 18, 2867–2872.Google Scholar

  • Zhang, K.L., Mangeat, B., Ortiz, M., Zoete, V., Trono, D., Telenti, A., and Michielin, O. (2007). Model structure of human APOBEC3G. PLoS One. 2, e378.Google Scholar

  • Zhang, W., Du, J., Evans, S.L., Yu, Y., and Yu, X.F. (2012). T-cell differentiation factor CBF-β regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481, 376–379.Google Scholar

About the article

Corresponding author: Carsten Münk, Clinic for Gastroenterology, Hepatology, and Infectiology, Medical Faculty, Heinrich-Heine-University, D-40225 Düsseldorf, Germany, e-mail:


Received: 2013-04-30

Accepted: 2013-06-17

Published Online: 2013-06-20

Published in Print: 2013-11-01


Citation Information: Biological Chemistry, Volume 394, Issue 11, Pages 1357–1370, ISSN (Online) 1437-4315, ISSN (Print) 1431-6730, DOI: https://doi.org/10.1515/hsz-2013-0165.

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[1]
Ananda Ayyappan Jaguva Vasudevan, Ulrike Kreimer, Wolfgang A. Schulz, Aikaterini Krikoni, Gerald G. Schumann, Dieter Häussinger, Carsten Münk, and Wolfgang Goering
Frontiers in Microbiology, 2018, Volume 9
[2]
Tatsuya Matsuoka, Takayuki Nagae, Hirotaka Ode, Hiroaki Awazu, Teppei Kurosawa, Akiko Hamano, Kazuhiro Matsuoka, Atsuko Hachiya, Mayumi Imahashi, Yoshiyuki Yokomaku, Nobuhisa Watanabe, and Yasumasa Iwatani
Nucleic Acids Research, 2018
[3]
Axel V. Horn, Sabine Klawitter, Ulrike Held, André Berger, Ananda Ayyappan Jaguva Vasudevan, Anja Bock, Henning Hofmann, Kay-Martin O. Hanschmann, Jan-Hendrik Trösemeier, Egbert Flory, Robert A. Jabulowsky, Jeffrey S. Han, Johannes Löwer, Roswitha Löwer, Carsten Münk, and Gerald G. Schumann
Nucleic Acids Research, 2014, Volume 42, Number 1, Page 396
[4]
D. V. Sosin and N. A. Tchurikov
Molecular Biology, 2017, Volume 51, Number 4, Page 483
[6]
Ananda Ayyappan Jaguva Vasudevan, Henning Hofmann, Dieter Willbold, Dieter Häussinger, Bernd W. Koenig, and Carsten Münk
Journal of Molecular Biology, 2017, Volume 429, Number 8, Page 1171
[7]
Daniela Marino, Mario Perković, Anika Hain, Ananda A. Jaguva Vasudevan, Henning Hofmann, Kay-Martin Hanschmann, Michael D. Mühlebach, Gerald G. Schumann, Renate König, Klaus Cichutek, Dieter Häussinger, Carsten Münk, and Javier Marcelo Di Noia
PLOS ONE, 2016, Volume 11, Number 6, Page e0155422
[8]
Tao Sun, Stephane Bentolila, and Maureen R. Hanson
Trends in Plant Science, 2016, Volume 21, Number 11, Page 962
[9]
Zeli Zhang, Qinyong Gu, Ananda Ayyappan Jaguva Vasudevan, Anika Hain, Björn-Philipp Kloke, Sascha Hasheminasab, Daniel Mulnaes, Kei Sato, Klaus Cichutek, Dieter Häussinger, Ignacio G. Bravo, Sander H. J. Smits, Holger Gohlke, and Carsten Münk
Retrovirology, 2016, Volume 13, Number 1
[10]
Fengchao Xu, Hongxiao Song, Na Li, and Guangyun Tan
Biochemical and Biophysical Research Communications, 2016, Volume 473, Number 1, Page 219
[11]
[12]
Andranik Ivanov, Sebastian Memczak, Emanuel Wyler, Francesca Torti, Hagit T. Porath, Marta R. Orejuela, Michael Piechotta, Erez Y. Levanon, Markus Landthaler, Christoph Dieterich, and Nikolaus Rajewsky
Cell Reports, 2015, Volume 10, Number 2, Page 170
[13]
Marek Widera, Frank Hillebrand, Steffen Erkelenz, Ananda Ayyappan Jaguva Vasudevan, Carsten Münk, and Heiner Schaal
Retrovirology, 2014, Volume 11, Number 1
[14]
Smita Nair and Alan Rein
Virus Research, 2014, Volume 193, Page 130
[15]
Bharat Vaidyanathan, Wei-Feng Yen, Joseph N. Pucella, and Jayanta Chaudhuri
Frontiers in Immunology, 2014, Volume 5

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