The assembly of Vif ubiquitin E3 ligase for APOBEC3 degradation

Archives of Pharmacal Research

Volumn 38, Issue 4, 2015, Pages 435-445

  Kim, Dong Young ^a  

^a Yeungnam University   (South Korea)

Author keywords

APOBEC3; CBF ; CUL5; ELOC; HIV 1 Vif; Ubiquitin E3 ligase

Indexed keywords

APOBEC3 PROTEIN, HUMAN; CYTOSINE DEAMINASE; PROTEIN BINDING; UBIQUITIN PROTEIN LIGASE;

ANIMAL; CHEMISTRY; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CYTOSINE DEAMINASE; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; UBIQUITIN-PROTEIN LIGASES;

EID: 84939977932     PISSN: 02536269     EISSN: 19763786     Source Type: Journal    
DOI: 10.1007/s12272-014-0519-x     Document Type: Review

References (103)

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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
17. Cullen, B.R. 2003. Nuclear mRNA export: Insights from virology. Trends in Biochemical Sciences 28: 419-424.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
85. Strebel, K. 2013. HIV accessory proteins versus host restriction factors. Current opinion in Virology 3: 692-699.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.