Natural polymorphisms and Oligomerization of Human APOBEC3H contribute to single-stranded DNA scanning ability

Journal of Biological Chemistry

Volumn 290, Issue 45, 2015, Pages 27188-27203

  Feng, Yuqing ^a   Love, Robin P ^a   Ara, Anjuman ^a   Baig, Tayyba T ^a   Adolph, Madison B ^a   Chelico, Linda ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

HAPLOTYPES; PROCESSIVITY; SINGLE-STRANDED DNA;

DISEASES;

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3H; ASPARTIC ACID; CYTOSINE; GLUTAMIC ACID; HYDROLASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; APOBEC3H PROTEIN, HUMAN; VIF PROTEIN; VIF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; VIRUS DNA;

AMINO ACID SEQUENCE; APOBEC3H GENE; ARTICLE; BETA SHEET; CONTROLLED STUDY; DEAMINATION; DIMERIZATION; DNA DETERMINATION; ENZYME SUBSTRATE; GENETIC POLYMORPHISM; HAPLOTYPE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN TRANSPORT; REDUNDANCY ANALYSIS; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS VIRULENCE; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; IN VITRO STUDY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

AMINOHYDROLASES; BASE SEQUENCE; DNA, SINGLE-STRANDED; DNA, VIRAL; HAPLOTYPES; HIV-1; HUMANS; IN VITRO TECHNIQUES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; POLYMORPHISM, GENETIC; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY, NUCLEIC ACID; SUBSTRATE SPECIFICITY; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

EID: 84946605399     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.666065     Document Type: Article

References (88)

1. Desimmie, B. A., Delviks-Frankenberrry, K. A., Burdick, R. C., Qi, D., Izumi, T., and Pathak, V. K. (2014) Multiple APOBEC3 restriction factors for HIV-1 and one Vif to rule them all. J. Mol. Biol. 426, 1220-1245.
2. Feng, Y., Baig, T. T., Love, R. P., and Chelico, L. (2014) Suppression of APOBEC3-mediated restriction of HIV-1 by Vif. Front. Microbiol. 5, 450.
3. Hultquist, J. F., Lengyel, J. A., Refsland, E. W., LaRue, R. S., Lackey, L., Brown, W. L., and Harris, R. S. (2011) Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1. J. Virol. 85, 11220-11234.
4. Refsland, E. W., Hultquist, J. F., and Harris, R. S. (2012) Endogenous origins of HIV-1 G-to-A hypermutation and restriction in the nonpermissive T cell line CEM2n. PLoS Pathog. 8, e1002800.
5. Harris, R. S., Bishop, K. N., Sheehy, A. M., Craig, H. M., Petersen-Mahrt, S. K., Watt, I. N., Neuberger, M. S., and Malim, M. H. (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113, 803-809.
6. Mangeat, B., Turelli, P., Caron, G., Friedli, M., Perrin, L., and Trono, D. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424, 99-103.
7. Zhang, H., Yang, B., Pomerantz, R. J., Zhang, C., Arunachalam, S. C., and Gao, L. (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424, 94-98.
8. Yu, Q., König, R., Pillai, S., Chiles, K., Kearney, M., Palmer, S., Richman, D., Coffin, J. M., and Landau, N. R. (2004) Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 11, 435-442.
9. Liddament, M. T., Brown, W. L., Schumacher, A. J., and Harris, R. S. (2004) APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr. Biol. 14, 1385-1391.
10. Wiegand, H. L., Doehle, B. P., Bogerd, H. P., and Cullen, B. R. (2004) A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J. 23, 2451-2458.
11. Zheng, Y. H., Irwin, D., Kurosu, T., Tokunaga, K., Sata, T., and Peterlin, B. M. (2004) Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication. J. Virol. 78, 6073-6076.
12. Dang, Y., Wang, X., Esselman, W. J., and Zheng, Y. H. (2006) Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. J. Virol. 80, 10522-10533.
13. Harari, A., Ooms, M., Mulder, L. C., and Simon, V. (2009) Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H. J. Virol. 83, 295-303.
14. Harris, R. S., Hultquist, J. F., and Evans, D. T. (2012) The restriction factors of human immunodeficiency virus. J. Biol. Chem. 287, 40875-40883.
15. 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.
16. Conticello, S. G., Harris, R. S., and Neuberger, M. S. (2003) The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr. Biol. 13, 2009-2013.
17. Kao, S., Khan, M. A., Miyagi, E., Plishka, R., Buckler-White, A., and Strebel, K. (2003) The human immunodeficiency virus type 1 Vif protein reduces intracellular expression and inhibits packaging ofAPOBEC3G(CEM15), a cellular inhibitor of virus infectivity. J. Virol. 77, 11398-11407.
18. Mariani, R., Chen, D., Schröfelbauer, B., Navarro, F., König, R., Bollman, B., Münk, C., Nymark-McMahon, H., and Landau, N. R. (2003) Speciesspecific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114, 21-31.
19. 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.
20. 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.
21. Stopak, K., de Noronha, C., Yonemoto, W., and Greene, W. C. (2003) HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol. Cell 12, 591-601.
22. 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.
23. 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.
24. 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.
25. Ara, A., Love, R. P., and Chelico, L. (2014) Different mutagenic potential of HIV-1 restriction factors APOBEC3G and APOBEC3F is determined by distinct single-stranded DNA scanning mechanisms. PLoS Pathog. 10, e1004024.
26. 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.
27. Le Grice, S. F. (2012) Human immunodeficiency virus reverse transcriptase: 25 years of research, drug discovery, and promise. J. Biol. Chem. 287, 40850-40857.
28. Chelico, L., Pham, P., Calabrese, P., and Goodman, M. F. (2006) APOBEC3GDNAdeaminase acts processively 3'→5' on single-stranded DNA. Nat. Struct. Mol. Biol. 13, 392-399.
29. Love, R. P., Xu, H., and Chelico, L. (2012) Biochemical analysis of hypermutation by the deoxycytidine deaminase APOBEC3A. J. Biol. Chem. 287, 30812-30822.
30. 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.
31. Berg, O. G., Winter, R. B., and von Hippel, P. H. (1981) Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry 20, 6929-6948.
32. von Hippel, P. H., and Berg, O. G. (1989) Facilitated target location in biological systems. J. Biol. Chem. 264, 675-678.
33. Halford, S. E. (2009) An end to 40 years of mistakes in DNA-protein association kinetics Biochem. Soc. Trans. 37, 343-348.
34. Halford, S. E., and Marko, J. F. (2004) How do site-specific DNA-binding proteins find their targets Nucleic Acids Res. 32, 3040-3052.
35. OhAinle, M., Kerns, J. A., Li, M. M., Malik, H. S., and Emerman, M. (2008) Antiretroelement activity of APOBEC3H was lost twice in recent human evolution. Cell Host Microbe 4, 249-259.
36. Wang, X., Abudu, A., Son, S., Dang, Y., Venta, P. J., and Zheng, Y. H. (2011) Analysis of human APOBEC3H haplotypes and anti-human immunodeficiency virus type 1 activity. J. Virol. 85, 3142-3152.
37. Ooms, M., Brayton, B., Letko, M., Maio, S. M., Pilcher, C. D., Hecht, F. M., Barbour, J. D., and Simon, V. (2013) HIV-1 Vif adaptation to human APOBEC3H haplotypes. Cell Host Microbe 14, 411-421.
38. Mitra, M., Singer, D., Mano, Y., Hritz, J., Nam, G., Gorelick, R. J., Byeon, I. J., Gronenborn, A. M., Iwatani, Y., and Levin, J. G. (2015) Sequence and structural determinants of human APOBEC3H deaminase and anti- HIV-1 activities. Retrovirology 12, 3.
39. Refsland, E. W., Hultquist, J. F., Luengas, E. M., Ikeda, T., Shaban, N. M., Law, E. K., Brown, W. L., Reilly, C., Emerman, M., and Harris, R. S. (2014) Natural polymorphisms in human APOBEC3H and HIV-1 Vif combine in primary T lymphocytes to affect viral G-to-A mutation levels and infectivity. PLoS Genet. 10, e1004761.
40. Zhen, A., Wang, T., Zhao, K., Xiong, Y., and Yu, X. F. (2010) A single amino acid difference in human APOBEC3H variants determines HIV-1 Vif sensitivity. J. Virol. 84, 1902-1911.
41. Li, M. M., and Emerman, M. (2011) Polymorphism in human APOBEC3H affects a phenotype dominant for subcellular localization and antiviral activity. J. Virol. 85, 8197-8207.
42. LaRue, R. S., Jónsson, S. R., Silverstein, K. A., Lajoie, M., Bertrand, D., El-Mabrouk, N., Hötzel, 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. BMC Mol. Biol. 9, 104.
43. Baig, T. T., Feng, Y., and Chelico, L. (2014) Determinants of efficient degradation of APOBEC3 restriction factors by HIV-1 Vif. J. Virol. 88, 14380-14395.
44. Li, J., Chen, Y., Li, M., Carpenter, M. A., McDougle, R. M., Luengas, E. M., Macdonald, P. J., Harris, R. S., and Mueller, J. D. (2014) APOBEC3 multimerization correlates with HIV-1 packaging and restriction activity in living cells. J. Mol. Biol. 426, 1296-1307.
45. 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.
46. 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.
47. 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.
48. Zhang, H., Zhou, Y., Alcock, C., Kiefer, T., Monie, D., Siliciano, J., Li, Q., Pham, P., Cofrancesco, J., Persaud, D., and Siliciano, R. F. (2004) Novel single-cell-level phenotypic assay for residual drug susceptibility and reduced replication capacity of drug-resistant human immunodeficiency virus type 1. J. Virol. 78, 1718-1729.
49. Langlois, M. A., Beale, R. C., Conticello, S. G., and Neuberger, M. S. (2005) Mutational comparison of the single-domained APOBEC3C and doubledomained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities. Nucleic Acids Res. 33, 1913-1923.
50. Naldini, L., Blömer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F. H., Verma, I. M., and Trono, D. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267.
51. Creighton, S., Bloom, L. B., and Goodman, M. F. (1995) Gel fidelity assay measuring nucleotide misinsertion, exonucleolytic proofreading, and lesion bypass efficiencies. Methods Enzymol. 262, 232-256.
52. Lieberman, B. A., and Nordeen, S. K. (1997) DNA intersegment transfer, how steroid receptors search for a target site. J. Biol. Chem. 272, 1061-1068.
53. Luo, K., Liu, B., Xiao, Z., Yu, Y., Yu, X., Gorelick, R., and Yu, X. F. (2004) Amino-terminal region of the human immunodeficiency virus type 1 nucleocapsid is required for human APOBEC3G packaging. J. Virol. 78, 11841-11852.
54. Schäfer, A., Bogerd, H. P., and Cullen, B. R. (2004) Specific packaging of APOBEC3G into HIV-1 virions is mediated by the nucleocapsid domain of the gag polyprotein precursor. Virology 328, 163-168.
55. Svarovskaia, E. S., Xu, H., Mbisa, J. L., Barr, R., Gorelick, R. J., Ono, A., Freed, E. O., Hu, W. S., and Pathak, V. K. (2004) Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J. Biol. Chem. 279, 35822-35828.
56. Zennou, V., Perez-Caballero, D., Göttlinger, H., and Bieniasz, P. D. (2004) APOBEC3G incorporation into human immunodeficiency virus type 1 particles. J. Virol. 78, 12058-12061.
57. Alce, T. M., and Popik, W. (2004) APOBEC3G is incorporated into virus-like particles by a direct interaction with HIV-1 Gag nucleocapsid protein. J. Biol. Chem. 279, 34083-34086.
58. Bach, D., Peddi, S., Mangeat, B., Lakkaraju, A., Strub, K., and Trono, D. (2008) Characterization of APOBEC3G binding to 7SL RNA. Retrovirology 5, 54.
59. Wang, T., Tian, C., Zhang, W., Luo, K., Sarkis, P. T., Yu, L., Liu, B., Yu, Y., and Yu, X. F. (2007) 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J. Virol. 81, 13112-13124.
60. Strebel, K., and Khan, M. A. (2008) APOBEC3G encapsidation into HIV-1 virions: which RNA is it Retrovirology 5, 55.
61. Sakurai, D., Iwatani, Y., Ohtani, H., Naruse, T. K., Terunuma, H., Sugiura, W., and Kimura, A. (2015) APOBEC3H polymorphisms associated with the susceptibility to HIV-1 infection and AIDS progression in Japanese. Immunogenetics 67, 253-257.
62. Dang, Y., Siew, L. M., Wang, X., Han, Y., Lampen, R., and Zheng, Y. H. (2008) Human cytidine deaminase APOBEC3H restricts HIV-1 replication. J. Biol. Chem. 283, 11606-11614.
63. Tan, L., Sarkis, P. T., Wang, T., Tian, C., and Yu, X. F. (2009) Sole copy of Z2-type human cytidine deaminase APOBEC3H has inhibitory activity against retrotransposons and HIV-1. FASEB J. 23, 279-287.
64. Li, M. M., Wu, L. I., and Emerman, M. (2010) The range of human APOBEC3H sensitivity to lentiviral Vif proteins. J. Virol. 84, 88-95.
65. Ooms, M., Majdak, S., Seibert, C. W., Harari, A., and Simon, V. (2010) The localization of APOBEC3H variants in HIV-1 virions determines their antiviral activity. J. Virol. 84, 7961-7969.
66. Apolonia, L., Schulz, R., Curk, T., Rocha, P., Swanson, C. M., Schaller, T., Ule, J., and Malim, M. H. (2015) Promiscuous RNA binding ensures effective encapsidation of APOBEC3 proteins by HIV-1. PLoS Pathog. 11, e1004609.
67. Feng, Y., Love, R. P., and Chelico, L. (2013) HIV-1 viral infectivity factor (Vif) alters processive single-stranded DNA scanning of the retroviral restriction factor APOBEC3G. J. Biol. Chem. 288, 6083-6094.
68. Kitamura, S., Ode, H., Nakashima, M., Imahashi, M., Naganawa, Y., Kurosawa, T., Yokomaku, Y., Yamane, T., Watanabe, N., Suzuki, A., Sugiura, W., and Iwatani, Y. (2012) The APOBEC3C crystal structure and the interface for HIV-1 Vif binding. Nat. Struct. Mol. Biol. 19, 1005-1010.
69. Mu, Y., Prochnow, C., Pham, P., Chen, X. S., and Goodman, M. F. (2012)A structural basis for the biochemical behavior of activation-induced deoxycytidine deaminase class-switch recombination-defective hyper-IgM-2 mutants. J. Biolog. Chem. 287, 28007-28016.
70. Kohli, R. M., Abrams, S. R., Gajula, K. S., Maul, R. W., Gearhart, P. J., and Stivers, J. T. (2009) A portable hot spot recognition loop transfers sequence preferences from APOBEC family members to activation-induced cytidine deaminase. J. Biol. Chem. 284, 22898-22904.
71. Carpenter, M. A., Rajagurubandara, E., Wijesinghe, P., and Bhagwat, A. S. (2010) Determinants of sequence-specificity within human AID and APOBEC3G. DNA Repair 9, 579-587.
72. Rathore, A., Carpenter, M. A., Demir, Ö., Ikeda, T., Li, M., Shaban, N. M., Law, E. K., Anokhin, D., Brown, W. L., Amaro, R. E., and Harris, R. S. (2013) The local dinucleotide preference of APOBEC3G can be altered from 5'-CC to 5'-TC by a single amino acid substitution. J. Mol. Biol. 425, 4442-4454.
73. Binka, M., Ooms, M., Steward, M., and Simon, V. (2012) The activity spectrum of Vif from multiple HIV-1 subtypes against APOBEC3G, APOBEC3F, and APOBEC3H. J. Virol. 86, 49-59.
74. Ooms, M., Letko, M., Binka, M., and Simon, V. (2013) The resistance of human APOBEC3H to HIV-1 NL4-3 molecular clone is determined by a single amino acid in Vif. PLoS One 8, e57744.
75. Senavirathne, G., Jaszczur, M., Auerbach, P. A., Upton, T. G., Chelico, L., Goodman, M. F., and Rueda, D. (2012) Single-stranded DNA scanning and deamination by APOBEC3G cytidine deaminase at single molecule resolution. J. Biol. Chem. 287, 15826-15835.
76. Shlyakhtenko, L. S., Lushnikov, A. Y., Miyagi, A., Li, M., Harris, R. S., and Lyubchenko, Y. L. (2013) Atomic force microscopy studies of APOBEC3G oligomerization and dynamics. J. Struct. Biol. 184, 217-225.
77. Krzysiak, T. C., Jung, J., Thompson, J., Baker, D., and Gronenborn, A. M. (2012) APOBEC2 is a monomer in solution: implications for APOBEC3G models. Biochemistry 51, 2008-2017.
78. 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.
79. 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., Kono, T., Matsuo, H., Harris, R. S., Somasundaran, M., and Schiffer, C. A. (2010) Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18, 28-38.
80. 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., Zhang, J., Lu, Y., Somasundaran, M., Matsuo, H., Harris, R. S., and Schiffer, C. A. (2013) Crystal structure of the DNA cytosine deaminase APOBEC3F: The catalytically active and HIV-1 Vif-binding domain. Structure 21, 1042-1050.
81. Siu, K. K., Sultana, A., Azimi, F. C., and Lee, J. E. (2013) Structural determinants of HIV-1 Vif susceptibility andDNAbinding in APOBEC3F. Nat. Commun. 4, 2593.
82. Bohn, M. F., Shandilya, S. M., Silvas, T. V., Nalivaika, E. A., Kouno, T., Kelch, B. A., Ryder, S. P., Kurt-Yilmaz, N., Somasundaran, M., and Schiffer, C. A. (2015) The ssDNA mutator APOBEC3A is regulated by cooperative dimerization. Structure 23, 903-911.
83. King, J. J., Manuel, C. A., Barrett, C. V., Raber, S., Lucas, H., Sutter, P., and Larijani, M. (2015) Catalytic pocket inaccessibility of activation-induced cytidine deaminase is a safeguard against excessive mutagenic activity. Structure 23, 615-627.
84. 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.
85. Bogerd, H. P., Doehle, B. P., Wiegand, H. L., and Cullen, B. R. (2004) A single amino acid difference in the host APOBEC3G protein controls the primate species specificity of HIV type 1 virion infectivity factor. Proc. Natl. Acad. Sci. U.S.A. 101, 3770-3774.
86. Mangeat, B., Turelli, P., Liao, S., and Trono, D. (2004) A single amino acid determinant governs the species-specific sensitivity of APOBEC3G to Vif action. J. Biol. Chem. 279, 14481-14483.
87. Shandilya, S. M., Bohn, M. F., and Schiffer, C. A. (2014) A computational analysis of the structural determinants of APOBEC3's catalytic activity and vulnerability to HIV-1 Vif. Virology 471, 105-116.
88. Aydin, H., Taylor, M. W., and Lee, J. E. (2014) Structure-guided analysis of the human APOBEC3-HIV restrictome. Structure 22, 668-684.