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Archives of Pharmacal Research

, Volume 38, Issue 4, pp 435–445 | Cite as

The assembly of Vif ubiquitin E3 ligase for APOBEC3 degradation

  • Dong Young KimEmail author
Review

Abstract

APOBEC3G is a cellular antiviral protein that restricts retroviral infection. In non-permissive cells infected by Vif-deficient HIV-1, the protein mediates the hypermutation of viral DNA through the enzymatic activity of cytidine deaminase. To counteract the antiviral activity of APOBEC3G, an accessory protein of HIV-1, Vif, forms ubiquitin E3 ligase through assembly with CUL5-RBX2, ELOB-ELOC and CBFβ. Subsequently, Vif recruits APOBEC3G to the complex as a substrate adaptor of ubiquitin E3 ligase and induces poly-ubiquitination of APOBEC3G for its proteasomal degradation (Fig. 1). This review briefly summarizes current understanding of protein–protein interaction between Vif and host factors required for APOBEC3 degradation, based on high resolution structures of APOBEC3 proteins and Vif-CUL5NTD-ELOBC-CBFβ complex.
Fig. 1

A schematic model of assembly of Vif ubiquitin E3 ligase and subsequent APOBEC3 degradation. HIV-1 Vif hijacks cellular E3 ligase components containing CUL5, RBX2, ELOB, ELOC and CBFβ, to poly-ubiquitinate antiviral cellular factors, APOBEC3 proteins. Poly-ubiquitinated APOBEC3 proteins are targeted for proteasomal degradation. Ubiquitin is labeled as Ub

Keywords

HIV-1 Vif APOBEC3 CUL5 ELOC CBFβ Ubiquitin E3 ligase 

Notes

Acknowledgments

This work was supported by the 2013 Yeungnam University Research Grant, Korea Basic Science Institute Grant (T34415, H.S.Jung) and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (NRF-2014R1A1A1002064).

References

  1. Aguiar, R.S., N. Lovsin, A. Tanuri, and B.M. Peterlin. 2008. Vpr. A3A chimera inhibits HIV replication. The Journal of Biological Chemistry 283: 2518–2525.PubMedCrossRefGoogle Scholar
  2. Beale, R.C., S.K. Petersen-Mahrt, I.N. Watt, R.S. Harris, C. Rada, and M.S. Neuberger. 2004. Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. Journal of Molecular Biology 337: 585–596.PubMedCrossRefGoogle Scholar
  3. Belanger, K., M. Savoie, M.C. Rosales Gerpe, J.F. Couture, and M.A. Langlois. 2013. Binding of RNA by APOBEC3G controls deamination-independent restriction of retroviruses. Nucleic Acids Research 41: 7438–7452.PubMedCentralPubMedCrossRefGoogle Scholar
  4. Bishop, K.N., R.K. Holmes, A.M. Sheehy, N.O. Davidson, S.J. Cho, and M.H. Malim. 2004. Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Current Biology 14: 1392–1396.PubMedCrossRefGoogle Scholar
  5. Bishop, K.N., M. Verma, E.Y. Kim, S.M. Wolinsky, and M.H. Malim. 2008. APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathogens 4: e1000231.PubMedCentralPubMedCrossRefGoogle Scholar
  6. Bogerd, H.P., B.P. Doehle, H.L. Wiegand, and B.R. Cullen. 2004. A single amino acid difference in the host APOBEC3G protein controls the primate species specificity of HIV type 1 virion infectivity factor. Proceedings of the National Academy of Sciences of the United States of America 101: 3770–3774.PubMedCentralPubMedCrossRefGoogle Scholar
  7. Bohn, M.F., S.M. Shandilya, J.S. Albin, T. Kouno, B.D. Anderson, R.M. Mcdougle, M.A. Carpenter, A. Rathore, L. Evans, A.N. Davis, J. Zhang, Y. Lu, M. Somasundaran, H. Matsuo, R.S. Harris, and C.A. Schiffer. 2013. Crystal structure of the DNA cytosine deaminase APOBEC3F: the catalytically active and HIV-1 Vif-binding domain. Structure 21: 1042–1050.PubMedCentralPubMedCrossRefGoogle Scholar
  8. Bouyac, M., F. Rey, M. Nascimbeni, M. Courcoul, J. Sire, D. Blanc, F. Clavel, R. Vigne, and B. Spire. 1997. Phenotypically Vif- human immunodeficiency virus type 1 is produced by chronically infected restrictive cells. Journal of Virology 71: 2473–2477.PubMedCentralPubMedGoogle Scholar
  9. Bullock, A.N., J.E. Debreczeni, A.M. Edwards, M. Sundstrom, and S. Knapp. 2006. Crystal structure of the SOCS2-elongin C-elongin B complex defines a prototypical SOCS box ubiquitin ligase. Proceedings of the National Academy of Sciences of the United States of America 103: 7637–7642.PubMedCentralPubMedCrossRefGoogle Scholar
  10. Bullock, A.N., M.C. Rodriguez, J.E. Debreczeni, Z. Songyang, and S. Knapp. 2007. Structure of the SOCS4-ElonginB/C complex reveals a distinct SOCS box interface and the molecular basis for SOCS-dependent EGFR degradation. Structure 15: 1493–1504.PubMedCentralPubMedCrossRefGoogle Scholar
  11. Byeon, I.J., J. Ahn, M. Mitra, C.H. Byeon, K. Hercik, J. Hritz, L.M. Charlton, J.G. Levin, and A.M. Gronenborn. 2013. NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nature Communications 4: 1890.PubMedCentralPubMedCrossRefGoogle Scholar
  12. Chaipan, C., J.L. Smith, W.S. Hu, and V.K. Pathak. 2013. APOBEC3G restricts HIV-1 to a greater extent than APOBEC3F and APOBEC3DE in human primary CD4+ T cells and macrophages. Journal of Virology 87: 444–453.PubMedCentralPubMedCrossRefGoogle Scholar
  13. Chelico, L., P. Pham, P. Calabrese, and M.F. Goodman. 2006. APOBEC3G DNA deaminase acts processively 3′ → 5′ on single-stranded DNA. Nature Structural & Molecular Biology 13: 392–399.CrossRefGoogle Scholar
  14. Chen, G., Z. He, T. Wang, R. Xu, and X.F. Yu. 2009. A patch of positively charged amino acids surrounding the human immunodeficiency virus type 1 Vif SLVx4Yx9Y motif influences its interaction with APOBEC3G. Journal of Virology 83: 8674–8682.PubMedCentralPubMedCrossRefGoogle Scholar
  15. Chen, K.M., E. Harjes, P.J. Gross, A. Fahmy, Y. Lu, K. Shindo, R.S. Harris, and H. Matsuo. 2008. Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452: 116–119.PubMedCrossRefGoogle Scholar
  16. Conticello, S.G., R.S. Harris, and M.S. Neuberger. 2003. The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Current Biology 13: 2009–2013.PubMedCrossRefGoogle Scholar
  17. Cullen, B.R. 2003. Nuclear mRNA export: Insights from virology. Trends in Biochemical Sciences 28: 419–424.PubMedCrossRefGoogle Scholar
  18. Dang, Y., R.W. Davis, I.A. York, and Y.H. Zheng. 2010. Identification of 81LGxGxxIxW89 and 171EDRW174 domains from human immunodeficiency virus type 1 Vif that regulate APOBEC3G and APOBEC3F neutralizing activity. Journal of Virology 84: 5741–5750.PubMedCentralPubMedCrossRefGoogle Scholar
  19. Dang, Y., X. Wang, W.J. Esselman, and Y.H. Zheng. 2006. Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. Journal of Virology 80: 10522–10533.PubMedCentralPubMedCrossRefGoogle Scholar
  20. Dang, Y., X. Wang, T. Zhou, I.A. York, and Y.H. Zheng. 2009. Identification of a novel WxSLVK motif in the N terminus of human immunodeficiency virus and simian immunodeficiency virus Vif that is critical for APOBEC3G and APOBEC3F neutralization. Journal of Virology 83: 8544–8552.PubMedCentralPubMedCrossRefGoogle Scholar
  21. Desimmie, B.A., K.A. Delviks-Frankenberrry, R.C. Burdick, D. Qi, T. Izumi, and V.K. Pathak. 2014. Multiple APOBEC3 restriction factors for HIV-1 and one Vif to rule them all. Journal of Molecular Biology 426: 1220–1245.PubMedCentralPubMedCrossRefGoogle Scholar
  22. Doehle, B.P., A. Schafer, and B.R. Cullen. 2005. Human APOBEC3B is a potent inhibitor of HIV-1 infectivity and is resistant to HIV-1 Vif. Virology 339: 281–288.PubMedCrossRefGoogle Scholar
  23. Fisher, A.G., B. Ensoli, L. Ivanoff, M. Chamberlain, S. Petteway, L. Ratner, R.C. Gallo, and F. Wong-Staal. 1987. The sor gene of HIV-1 is required for efficient virus transmission in vitro. Science 237: 888–893.PubMedCrossRefGoogle Scholar
  24. Furukawa, A., T. Nagata, A. Matsugami, Y. Habu, R. Sugiyama, F. Hayashi, N. Kobayashi, S. Yokoyama, H. Takaku, and M. Katahira. 2009. Structure, interaction and real-time monitoring of the enzymatic reaction of wild-type APOBEC3G. The EMBO Journal 28: 440–451.PubMedCentralPubMedCrossRefGoogle Scholar
  25. Gabuzda, D.H., K. Lawrence, E. Langhoff, E. Terwilliger, T. Dorfman, W.A. Haseltine, and J. Sodroski. 1992. Role of vif in replication of human immunodeficiency virus type 1 in CD4+ T lymphocytes. Journal of Virology 66: 6489–6495.PubMedCentralPubMedGoogle Scholar
  26. Guo, F., S. Cen, M. Niu, J. Saadatmand, and L. Kleiman. 2006. Inhibition of formula-primed reverse transcription by human APOBEC3G during human immunodeficiency virus type 1 replication. Journal of Virology 80: 11710–11722.PubMedCentralPubMedCrossRefGoogle Scholar
  27. Guo, F., S. Cen, M. Niu, Y. Yang, R.J. Gorelick, and L. Kleiman. 2007. The interaction of APOBEC3G with human immunodeficiency virus type 1 nucleocapsid inhibits tRNA3Lys annealing to viral RNA. Journal of Virology 81: 11322–11331.PubMedCentralPubMedCrossRefGoogle Scholar
  28. Guo, Y., L. Dong, X. Qiu, Y. Wang, B. Zhang, H. Liu, Y. Yu, Y. Zang, M. Yang, and Z. Huang. 2014. Structural basis for hijacking CBF-beta and CUL5 E3 ligase complex by HIV-1 Vif. Nature 505: 229–233.PubMedCrossRefGoogle Scholar
  29. Harjes, E., P.J. Gross, K.M. Chen, Y. Lu, K. Shindo, R. Nowarski, J.D. Gross, M. Kotler, R.S. Harris, and H. Matsuo. 2009. An extended structure of the APOBEC3G catalytic domain suggests a unique holoenzyme model. Journal of Molecular Biology 389: 819–832.PubMedCentralPubMedCrossRefGoogle Scholar
  30. Harris, R.S., K.N. Bishop, A.M. Sheehy, H.M. Craig, S.K. Petersen-Mahrt, I.N. Watt, M.S. Neuberger, and M.H. Malim. 2003. DNA deamination mediates innate immunity to retroviral infection. Cell 113: 803–809.PubMedCrossRefGoogle Scholar
  31. He, Z., W. Zhang, G. Chen, R. Xu, and X.F. Yu. 2008. Characterization of conserved motifs in HIV-1 Vif required for APOBEC3G and APOBEC3F interaction. Journal of Molecular Biology 381: 1000–1011.PubMedCrossRefGoogle Scholar
  32. Holden, L.G., C. Prochnow, Y.P. Chang, R. Bransteitter, L. Chelico, U. Sen, R.C. Stevens, M.F. Goodman, and X.S. Chen. 2008. Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456: 121–124.PubMedCentralPubMedCrossRefGoogle Scholar
  33. Huthoff, H., and M.H. Malim. 2007. Identification of amino acid residues in APOBEC3G required for regulation by human immunodeficiency virus type 1 Vif and Virion encapsidation. Journal of Virology 81: 3807–3815.PubMedCentralPubMedCrossRefGoogle Scholar
  34. Inoue, K., S. Ozaki, T. Shiga, K. Ito, T. Masuda, N. Okado, T. Iseda, S. Kawaguchi, M. Ogawa, S.C. Bae, N. Yamashita, S. Itohara, N. Kudo, and Y. Ito. 2002. Runx3 controls the axonal projection of proprioceptive dorsal root ganglion neurons. Nature Neuroscience 5: 946–954.PubMedCrossRefGoogle Scholar
  35. Iwatani, Y., D.S. Chan, F. Wang, K.S. Maynard, W. Sugiura, A.M. Gronenborn, I. Rouzina, M.C. Williams, K. Musier-Forsyth, and J.G. Levin. 2007. Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Research 35: 7096–7108.PubMedCentralPubMedCrossRefGoogle Scholar
  36. Jager, S., D.Y. Kim, J.F. Hultquist, K. Shindo, R.S. Larue, E. Kwon, M. Li, B.D. Anderson, L. Yen, D. Stanley, C. Mahon, J. Kane, K. Franks-Skiba, P. Cimermancic, A. Burlingame, A. Sali, C.S. Craik, R.S. Harris, J.D. Gross, and N.J. Krogan. 2012. Vif hijacks CBF-beta to degrade APOBEC3G and promote HIV-1 infection. Nature 481: 371–375.Google Scholar
  37. Jarmuz, A., A. Chester, J. Bayliss, J. Gisbourne, I. Dunham, J. Scott, and N. Navaratnam. 2002. An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 79: 285–296.PubMedCrossRefGoogle Scholar
  38. Kagoshima, H., K. Shigesada, M. Satake, Y. Ito, H. Miyoshi, M. Ohki, M. Pepling, and P. Gergen. 1993. The Runt domain identifies a new family of heteromeric transcriptional regulators. Trends in Genetics 9: 338–341.PubMedCrossRefGoogle Scholar
  39. Kamura, T., K. Maenaka, S. Kotoshiba, M. Matsumoto, D. Kohda, R.C. Conaway, J.W. Conaway, and K.I. Nakayama. 2004. VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes & Development 18: 3055–3065.CrossRefGoogle Scholar
  40. Kim, D.Y., E. Kwon, P.D. Hartley, D.C. Crosby, S. Mann, N.J. Krogan, and J.D. Gross. 2013. CBFbeta stabilizes HIV Vif to counteract APOBEC3 at the expense of RUNX1 target gene expression. Molecular Cell 49: 632–644.PubMedCentralPubMedCrossRefGoogle Scholar
  41. Kitamura, S., H. Ode, M. Nakashima, M. Imahashi, Y. Naganawa, T. Kurosawa, Y. Yokomaku, T. Yamane, N. Watanabe, A. Suzuki, W. Sugiura, and Y. Iwatani. 2012. The APOBEC3C crystal structure and the interface for HIV-1 Vif binding. Nature Structural & Molecular Biology 19: 1005–1010.CrossRefGoogle Scholar
  42. Komori, T., H. Yagi, S. Nomura, A. Yamaguchi, K. Sasaki, K. Deguchi, Y. Shimizu, R.T. Bronson, Y.H. Gao, M. Inada, M. Sato, R. Okamoto, Y. Kitamura, S. Yoshiki, and T. Kishimoto. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89: 755–764.PubMedCrossRefGoogle Scholar
  43. Koning, F.A., E.N. Newman, E.Y. Kim, K.J. Kunstman, S.M. Wolinsky, and M.H. Malim. 2009. Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. Journal of Virology 83: 9474–9485.PubMedCentralPubMedCrossRefGoogle Scholar
  44. Langlois, M.A., R.C. Beale, S.G. Conticello, and M.S. Neuberger. 2005. 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 Research 33: 1913–1923.PubMedCentralPubMedCrossRefGoogle Scholar
  45. Larue, R.S., V. Andresdottir, Y. Blanchard, S.G. Conticello, D. Derse, M. Emerman, W.C. Greene, S.R. Jonsson, N.R. Landau, M. Lochelt, H.S. Malik, M.H. Malim, C. Munk, S.J. O’brien, V.K. Pathak, K. Strebel, S. Wain-Hobson, X.F. Yu, N. Yuhki, and R.S. Harris. 2009. Guidelines for naming nonprimate APOBEC3 genes and proteins. Journal of Virology 83: 494–497.PubMedCentralPubMedCrossRefGoogle Scholar
  46. Lecossier, D., F. Bouchonnet, F. Clavel, and A.J. Hance. 2003. Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300: 1112.PubMedCrossRefGoogle Scholar
  47. Levanon, D., D. Bettoun, C. Harris-Cerruti, E. Woolf, V. Negreanu, R. Eilam, Y. Bernstein, D. Goldenberg, C. Xiao, M. Fliegauf, E. Kremer, F. Otto, O. Brenner, A. Lev-Tov, and Y. Groner. 2002. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. The EMBO Journal 21: 3454–3463.PubMedCentralPubMedCrossRefGoogle Scholar
  48. Li, X.Y., F. Guo, L. Zhang, L. Kleiman, and S. Cen. 2007. APOBEC3G inhibits DNA strand transfer during HIV-1 reverse transcription. The Journal of Biological Chemistry 282: 32065–32074.PubMedCrossRefGoogle Scholar
  49. Luo, K., T. Wang, B. Liu, C. Tian, Z. Xiao, J. Kappes, and X.F. Yu. 2007. Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. Journal of Virology 81: 7238–7248.PubMedCentralPubMedCrossRefGoogle Scholar
  50. Luo, K., Z. Xiao, E. Ehrlich, Y. Yu, B. Liu, S. Zheng, and X.F. Yu. 2005. Primate lentiviral virion infectivity factors are substrate receptors that assemble with cullin 5-E3 ligase through a HCCH motif to suppress APOBEC3G. Proceedings of the National Academy of Sciences of the United States of America 102: 11444–11449.PubMedCentralPubMedCrossRefGoogle Scholar
  51. Mangeat, B., P. Turelli, G. Caron, M. Friedli, L. Perrin, and D. Trono. 2003. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424: 99–103.PubMedCrossRefGoogle Scholar
  52. Mangeat, B., P. Turelli, S. Liao, and D. Trono. 2004. A single amino acid determinant governs the species-specific sensitivity of APOBEC3G to Vif action. The Journal of Biological Chemistry 279: 14481–14483.PubMedCrossRefGoogle Scholar
  53. Marcsisin, S.R., P.S. Narute, L.A. Emert-Sedlak, M. Kloczewiak, T.E. Smithgall, and J.R. Engen. 2011. On the solution conformation and dynamics of the HIV-1 viral infectivity factor. Journal of Molecular Biology 410: 1008–1022.PubMedCentralPubMedCrossRefGoogle Scholar
  54. Mariani, R., D. Chen, B. Schrofelbauer, F. Navarro, R. Konig, B. Bollman, C. Munk, H. Nymark-Mcmahon, and N.R. Landau. 2003. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114: 21–31.PubMedCrossRefGoogle Scholar
  55. Marin, M., K.M. Rose, S.L. Kozak, and D. Kabat. 2003. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nature Medicine 9: 1398–1403.PubMedCrossRefGoogle Scholar
  56. Mbisa, J.L., R. Barr, J.A. Thomas, N. Vandegraaff, I.J. Dorweiler, E.S. Svarovskaia, W.L. Brown, L.M. Mansky, R.J. Gorelick, R.S. Harris, A. Engelman, and V.K. Pathak. 2007. Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plus-strand DNA transfer and integration. Journal of Virology 81: 7099–7110.PubMedCentralPubMedCrossRefGoogle Scholar
  57. Mehle, A., J. Goncalves, M. Santa-Marta, M. Mcpike, and D. Gabuzda. 2004. Phosphorylation of a novel SOCS-box regulates assembly of the HIV-1 Vif-Cul5 complex that promotes APOBEC3G degradation. Genes & Development 18: 2861–2866.CrossRefGoogle Scholar
  58. Mehle, A., E.R. Thomas, K.S. Rajendran, and D. Gabuzda. 2006. A zinc-binding region in Vif binds Cul5 and determines cullin selection. The Journal of Biological Chemistry 281: 17259–17265.PubMedCrossRefGoogle Scholar
  59. Miyagi, E., C.R. Brown, S. Opi, M. Khan, R. Goila-Gaur, S. Kao, R.C. Walker Jr, V. Hirsch, and K. Strebel. 2010. Stably expressed APOBEC3F has negligible antiviral activity. Journal of Virology 84: 11067–11075.PubMedCentralPubMedCrossRefGoogle Scholar
  60. Mulder, L.C., M. Ooms, S. Majdak, J. Smedresman, C. Linscheid, A. Harari, A. Kunz, and V. Simon. 2010. Moderate influence of human APOBEC3F on HIV-1 replication in primary lymphocytes. Journal of Virology 84: 9613–9617.PubMedCentralPubMedCrossRefGoogle Scholar
  61. Neil, S.J., T. Zang, and P.D. Bieniasz. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451: 425–430.PubMedCrossRefGoogle Scholar
  62. Newman, E.N., R.K. Holmes, H.M. Craig, K.C. Klein, J.R. Lingappa, M.H. Malim, and A.M. Sheehy. 2005. Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Current Biology 15: 166–170.PubMedCrossRefGoogle Scholar
  63. Ogawa, E., M. Inuzuka, M. Maruyama, M. Satake, M. Naito-Fujimoto, Y. Ito, and K. Shigesada. 1993. Molecular cloning and characterization of PEBP2 beta, the heterodimeric partner of a novel Drosophila runt-related DNA binding protein PEBP2 alpha. Virology 194: 314–331.PubMedCrossRefGoogle Scholar
  64. Okuda, T., J. Van Deursen, S.W. Hiebert, G. Grosveld, and J.R. Downing. 1996. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84: 321–330.PubMedCrossRefGoogle Scholar
  65. Ott, M., M. Geyer, and Q. Zhou. 2011. The control of HIV transcription: keeping RNA polymerase II on track. Cell Host & Microbe 10: 426–435.CrossRefGoogle Scholar
  66. Otto, F., A.P. Thornell, T. Crompton, A. Denzel, K.C. Gilmour, I.R. Rosewell, G.W. Stamp, R.S. Beddington, S. Mundlos, B.R. Olsen, P.B. Selby, and M.J. Owen. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89: 765–771.PubMedCrossRefGoogle Scholar
  67. Paul, I., J. Cui, and E.L. Maynard. 2006. Zinc binding to the HCCH motif of HIV-1 virion infectivity factor induces a conformational change that mediates protein-protein interactions. Proceedings of the National Academy of Sciences of the United States of America 103: 18475–18480.Google Scholar
  68. Perez-Caballero, D., T. Zang, A. Ebrahimi, M.W. Mcnatt, D.A. Gregory, M.C. Johnson, and P.D. Bieniasz. 2009. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139: 499–511.PubMedCentralPubMedCrossRefGoogle Scholar
  69. Pery, E., K.S. Rajendran, A.J. Brazier, and D. Gabuzda. 2009. Regulation of APOBEC3 proteins by a novel YXXL motif in human immunodeficiency virus type 1 Vif and simian immunodeficiency virus SIVagm Vif. Journal of Virology 83: 2374–2381.PubMedCentralPubMedCrossRefGoogle Scholar
  70. Petroski, M.D., and R.J. Deshaies. 2005. Function and regulation of cullin-RING ubiquitin ligases. Nature Reviews Molecular Cell Biology 6: 9–20.PubMedCrossRefGoogle Scholar
  71. Russell, R.A., and V.K. Pathak. 2007. Identification of two distinct human immunodeficiency virus type 1 Vif determinants critical for interactions with human APOBEC3G and APOBEC3F. Journal of Virology 81: 8201–8210.PubMedCentralPubMedCrossRefGoogle Scholar
  72. Russell, R.A., J. Smith, R. Barr, D. Bhattacharyya, and V.K. Pathak. 2009. Distinct domains within APOBEC3G and APOBEC3F interact with separate regions of human immunodeficiency virus type 1 Vif. Journal of Virology 83: 1992–2003.PubMedCentralPubMedCrossRefGoogle Scholar
  73. Sakai, H., R. Shibata, J. Sakuragi, S. Sakuragi, M. Kawamura, and A. Adachi. 1993. Cell-dependent requirement of human immunodeficiency virus type 1 Vif protein for maturation of virus particles. Journal of Virology 67: 1663–1666.PubMedCentralPubMedGoogle Scholar
  74. Santa-Marta, M., F.A. Da Silva, A.M. Fonseca, and J. Goncalves. 2005. HIV-1 Vif can directly inhibit apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3G-mediated cytidine deamination by using a single amino acid interaction and without protein degradation. The Journal of Biological Chemistry 280: 8765–8775.PubMedCrossRefGoogle Scholar
  75. Schrofelbauer, B., D. Chen, and N.R. Landau. 2004. A single amino acid of APOBEC3G controls its species-specific interaction with virion infectivity factor (Vif). Proceedings of the National Academy of Sciences of the United States of America 101: 3927–3932.PubMedCentralPubMedCrossRefGoogle Scholar
  76. Sheehy, A.M., N.C. Gaddis, J.D. Choi, and M.H. Malim. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418: 646–650.PubMedCrossRefGoogle Scholar
  77. Sheehy, A.M., N.C. Gaddis, and M.H. Malim. 2003. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nature Medicine 9: 1404–1407.PubMedCrossRefGoogle Scholar
  78. Simon, J.H., N.C. Gaddis, R.A. Fouchier, and M.H. Malim. 1998. Evidence for a newly discovered cellular anti-HIV-1 phenotype. Nature Medicine 4: 1397–1400.PubMedCrossRefGoogle Scholar
  79. Siu, K.K., A. Sultana, F.C. Azimi, and J.E. Lee. 2013. Structural determinants of HIV-1 Vif susceptibility and DNA binding in APOBEC3F. Nature Communications 4: 2593.PubMedCrossRefGoogle Scholar
  80. Smith, J.L., and V.K. Pathak. 2010. Identification of specific determinants of human APOBEC3F, APOBEC3C, and APOBEC3DE and African green monkey APOBEC3F that interact with HIV-1 Vif. Journal of Virology 84: 12599–12608.PubMedCentralPubMedCrossRefGoogle Scholar
  81. Sova, P., and D.J. Volsky. 1993. Efficiency of viral DNA synthesis during infection of permissive and nonpermissive cells with vif-negative human immunodeficiency virus type 1. Journal of Virology 67: 6322–6326.PubMedCentralPubMedGoogle Scholar
  82. Stanley, B.J., E.S. Ehrlich, L. Short, Y. Yu, Z. Xiao, X.F. Yu, and Y. Xiong. 2008. Structural insight into the human immunodeficiency virus Vif SOCS box and its role in human E3 ubiquitin ligase assembly. Journal of Virology 82: 8656–8663.PubMedCentralPubMedCrossRefGoogle Scholar
  83. Stanley, D.J., K. Bartholomeeusen, D.C. Crosby, D.Y. Kim, E. Kwon, L. Yen, N.C. Cartozo, M. Li, S. Jager, J. Mason-Herr, F. Hayashi, S. Yokoyama, N.J. Krogan, R.S. Harris, B.M. Peterlin, and J.D. Gross. 2012. Inhibition of a NEDD8 cascade restores restriction of HIV by APOBEC3G. PLoS Pathogens 8: e1003085.PubMedCentralPubMedCrossRefGoogle Scholar
  84. Stopak, K., C. De Noronha, W. Yonemoto, and W.C. Greene. 2003. HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Molecular Cell 12: 591–601.PubMedCrossRefGoogle Scholar
  85. Strebel, K. 2013. HIV accessory proteins versus host restriction factors. Current opinion in Virology 3: 692–699.PubMedCrossRefGoogle Scholar
  86. Tahirov, T.H., T. Inoue-Bungo, H. Morii, A. Fujikawa, M. Sasaki, K. Kimura, M. Shiina, K. Sato, T. Kumasaka, M. Yamamoto, S. Ishii, and K. Ogata. 2001. Structural analyses of DNA recognition by the AML1/Runx-1 Runt domain and its allosteric control by CBFbeta. Cell 104: 755–767.PubMedCrossRefGoogle Scholar
  87. Taniuchi, I., M. Osato, T. Egawa, M.J. Sunshine, S.C. Bae, T. Komori, Y. Ito, and D.R. Littman. 2002. Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell 111: 621–633.PubMedCrossRefGoogle Scholar
  88. Van Damme, N., D. Goff, C. Katsura, R.L. Jorgenson, R. Mitchell, M.C. Johnson, E.B. Stephens, and J. Guatelli. 2008. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host & Microbe 3: 245–252.CrossRefGoogle Scholar
  89. Von Schwedler, U., J. Song, C. Aiken, and D. Trono. 1993. Vif is crucial for human immunodeficiency virus type 1 proviral DNA synthesis in infected cells. Journal of Virology 67: 4945–4955.Google Scholar
  90. Wang, X., Z. Ao, L. Chen, G. Kobinger, J. Peng, and X. Yao. 2012. The cellular antiviral protein APOBEC3G interacts with HIV-1 reverse transcriptase and inhibits its function during viral replication. Journal of Virology 86: 3777–3786.PubMedCentralPubMedCrossRefGoogle Scholar
  91. Wiegand, H.L., B.P. Doehle, H.P. Bogerd, and B.R. Cullen. 2004. A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. The EMBO Journal 23: 2451–2458.PubMedCentralPubMedCrossRefGoogle Scholar
  92. Xiao, Z., E. Ehrlich, K. Luo, Y. Xiong, and X.F. Yu. 2007a. Zinc chelation inhibits HIV Vif activity and liberates antiviral function of the cytidine deaminase APOBEC3G. FASEB Journal 21: 217–222.PubMedCrossRefGoogle Scholar
  93. Xiao, Z., E. Ehrlich, Y. Yu, K. Luo, T. Wang, C. Tian, and X.F. Yu. 2006. Assembly of HIV-1 Vif-Cul5 E3 ubiquitin ligase through a novel zinc-binding domain-stabilized hydrophobic interface in Vif. Virology 349: 290–299.PubMedCrossRefGoogle Scholar
  94. Xiao, Z., Y. Xiong, W. Zhang, L. Tan, E. Ehrlich, D. Guo, and X.F. Yu. 2007b. Characterization of a novel Cullin5 binding domain in HIV-1 Vif. Journal of Molecular Biology 373: 541–550.PubMedCrossRefGoogle Scholar
  95. Yamashita, T., K. Kamada, K. Hatcho, A. Adachi, and M. Nomaguchi. 2008. Identification of amino acid residues in HIV-1 Vif critical for binding and exclusion of APOBEC3G/F. Microbes and infection/Institut Pasteur 10: 1142–1149.PubMedCrossRefGoogle Scholar
  96. Yu, X., Y. Yu, B. Liu, K. Luo, W. Kong, P. Mao, and X.F. Yu. 2003. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302: 1056–1060.Google Scholar
  97. Yu, Q., R. Konig, S. Pillai, K. Chiles, M. Kearney, S. Palmer, D. Richman, J.M. Coffin, and N.R. Landau. 2004a. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nature Structural & Molecular Biology 11: 435–442.CrossRefGoogle Scholar
  98. Yu, Y., Z. Xiao, E.S. Ehrlich, X. Yu, and X.F. Yu. 2004b. Selective assembly of HIV-1 Vif-Cul5-ElonginB-ElonginC E3 ubiquitin ligase complex through a novel SOCS box and upstream cysteines. Genes & Development 18: 2867–2872.CrossRefGoogle Scholar
  99. Zhang, H., B. Yang, R.J. Pomerantz, C. Zhang, S.C. Arunachalam, and L. Gao. 2003. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424: 94–98.PubMedCentralPubMedCrossRefGoogle Scholar
  100. Zhang, W., G. Chen, A.M. Niewiadomska, R. Xu, and X.F. Yu. 2008. Distinct determinants in HIV-1 Vif and human APOBEC3 proteins are required for the suppression of diverse host anti-viral proteins. PLoS One 3: e3963.PubMedCentralPubMedCrossRefGoogle Scholar
  101. Zhang, W., J. Du, S.L. Evans, Y. Yu, and X.F. Yu. 2012. T-cell differentiation factor CBF-beta regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481: 376–379.Google Scholar
  102. Zhen, A., T. Wang, K. Zhao, Y. Xiong, and X.F. Yu. 2010. A single amino acid difference in human APOBEC3H variants determines HIV-1 Vif sensitivity. Journal of Virology 84: 1902–1911.PubMedCentralPubMedCrossRefGoogle Scholar
  103. Zheng, N., B.A. Schulman, L. Song, J.J. Miller, P.D. Jeffrey, P. Wang, C. Chu, D.M. Koepp, S.J. Elledge, M. Pagano, R.C. Conaway, J.W. Conaway, J.W. Harper, and N.P. Pavletich. 2002. Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416: 703–709.PubMedCrossRefGoogle Scholar

Copyright information

© The Pharmaceutical Society of Korea 2014

Authors and Affiliations

  1. 1.College of PharmacyYeungnam UniversityGyeongsanSouth Korea

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