APOBEC3 proteins in viral immunity

Journal of Immunology

Volumn 195, Issue 10, 2015, Pages 4565-4570

  Stavrou, Spyridon ^a   Ross, Susan R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; APOBEC3 PROTEIN, HUMAN; CYTOSINE DEAMINASE; VIRUS DNA;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; APOBEC3 GENE; ARTICLE; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CYTOKINE PRODUCTION; GENE FREQUENCY; GENETIC POLYMORPHISM; GENOMICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IMMUNOGENICITY; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SOMATIC HYPERMUTATION; STOP CODON; UBIQUITINATION; VIRUS IMMUNITY; VIRUS INFECTIVITY; VIRUS REPLICATION; ANIMAL; CD8+ T LYMPHOCYTE; GENETICS; HEPATITIS B; HERPES VIRUS INFECTION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; PAPILLOMAVIRUS INFECTION; PARVOVIRUS INFECTION; VIROLOGY; VIRUS INFECTION;

ADAPTIVE IMMUNITY; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOSINE DEAMINASE; DNA, VIRAL; HEPATITIS B; HERPESVIRIDAE INFECTIONS; HIV INFECTIONS; HIV-1; HUMANS; PAPILLOMAVIRUS INFECTIONS; PARVOVIRIDAE INFECTIONS; VIRUS DISEASES;

EID: 84958601685     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501504     Document Type: Article

References (108)

1. 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.
2. Sobieszczyk, M. E., J. R. Lingappa, and M. J. McElrath. 2011. Host genetic polymorphisms associated with innate immune factors and HIV-1. Curr. Opin. HIV AIDS 6: 427-434.
3. Ross, S. R. 2009. Are viruses inhibited by APOBEC3 molecules from their host species? PLoS Pathog. 5: e1000347.
4. Emerman, M., and H. S. Malik. 2010. Paleovirology-modern consequences of ancient viruses. PLoS Biol. 8: e1000301.
5. Daugherty, M. D., and H. S. Malik. 2012. Rules of engagement: molecular insights from host-virus arms races. Annu. Rev. Genet. 46: 677-700.
6. Sawyer, S. L., M. Emerman, and H. S. Malik. 2004. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol. 2: E275.
7. OhAinle, M., J. A. Kerns, H. S. Malik, and M. Emerman. 2006. Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H. J. Virol. 80: 3853-3862.
8. Compton, A. A., V. M. Hirsch, and M. Emerman. 2012. The host restriction factor APOBEC3G and retroviral Vif protein coevolve due to ongoing genetic conflict. Cell Host Microbe 11: 91-98.
9. Sanville, B., M. A. Dolan, K. Wollenberg, Y. Yan, C. Martin, M. L. Yeung, K. Strebel, A. Buckler-White, and C. A. Kozak. 2010. Adaptive evolution of Mus Apobec3 includes retroviral insertion and positive selection at two clusters of residues flanking the substrate groove. PLoS Pathog. 6: e1000974.
10. LaRue, R. S., V. Andrésdóttir, Y. Blanchard, S. G. Conticello, D. Derse,M. Emerman, W. C. Greene, S. R. Jónsson, N. R. Landau, M. Löchelt, et al. 2009. Guidelines for naming nonprimate APOBEC3 genes and proteins. J. Virol. 83: 494-497.
11. Miyazawa, M., S. Tsuji-Kawahara, and Y. Kanari. 2008. Host genetic factors that control immune responses to retrovirus infections. Vaccine 26: 2981-2996.
12. Okeoma, C. M., J. Petersen, and S. R. Ross. 2009. Expression of murine APOBEC3 alleles in different mouse strains and their effect on mouse mammary tumor virus infection. J. Virol. 83: 3029-3038.
13. Santiago, M. L., M. Montano, R. Benitez, R. J. Messer, W. Yonemoto, B. Chesebro, K. J. Hasenkrug, and W. C. Greene. 2008. Apobec3 encodes Rfv3, a gene influencing neutralizing antibody control of retrovirus infection. Science 321: 1343-1346.
14. Ooms, M., B. Brayton, M. Letko, S. M. Maio, C. D. Pilcher, F. M. Hecht, J. D. Barbour, and V. Simon. 2013. HIV-1 Vif adaptation to human APOBEC3H haplotypes. Cell Host Microbe 14: 411-421.
15. An, P., G. Bleiber, P. Duggal, G. Nelson, M. May, B. Mangeat, I. Alobwede, D. Trono, D. Vlahov, S. Donfield, et al. 2004. APOBEC3G genetic variants and their influence on the progression to AIDS. J. Virol. 78: 11070-11076.
16. An, P., R. Johnson, J. Phair, G. D. Kirk, X. F. Yu, S. Donfield, S. Buchbinder, J. J. Goedert, and C. A. Winkler. 2009. APOBEC3B deletion and risk of HIV-1 acquisition. J. Infect. Dis. 200: 1054-1058.
17. Reddy, K., C. A. Winkler, L. Werner, K. Mlisana, S. S. Abdool Karim, and T. Ndung'u, CAPRISA Acute Infection Study Team. 2010. APOBEC3G expression is dysregulated in primary HIV-1 infection and polymorphic variants influence CD4+ T-cell counts and plasma viral load. AIDS 24: 195-204.
18. Kanari, Y., M. Clerici, H. Abe, H. Kawabata, D. Trabattoni, S. L. Caputo, F. Mazzotta, H. Fujisawa, A. Niwa, C. Ishihara, et al. 2005. Genotypes at chromosome 22q12-13 are associated with HIV-1-exposed but uninfected status in Italians. AIDS 19: 1015-1024.
19. Duggal, N. K., W. Fu, J. M. Akey, and M. Emerman. 2013. Identification and antiviral activity of common polymorphisms in the APOBEC3 locus in human populations. Virology 443: 329-337.
20. 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. Curr. Biol. 14: 1392-1396.
21. 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. EMBO J. 23: 2451-2458.
22. Liddament, M. T., W. L. Brown, A. J. Schumacher, and R. S. Harris. 2004. APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr. Biol. 14: 1385-1391.
23. Zheng, Y. H., D. Irwin, T. Kurosu, K. Tokunaga, T. Sata, and B. M. Peterlin. 2004. Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication. J. Virol. 78: 6073-6076.
24. Mehle, A., B. Strack, P. Ancuta, C. Zhang, M. McPike, and D. Gabuzda. 2004. Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J. Biol. Chem. 279: 7792-7798.
25. 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.
26. 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.
27. Marin, M.,K.M. Rose, S. L. Kozak, andD.Kabat. 2003.HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 9: 1398-1403.
28. Münk, C., B. E. Jensen, J. Zielonka, D. Häussinger, and C. Kamp. 2012. Running loose or getting lost: how HIV-1 counters and capitalizes on APOBEC3-induced mutagenesis through its Vif protein. Viruses 4: 3132-3161.
29. Jäger, S., D. Y. Kim, J. F. Hultquist, K. Shindo, R. S. LaRue, E. Kwon, M. Li, B. D. Anderson, L. Yen, D. Stanley, et al. 2012. Vif hijacks CBF-b to degrade APOBEC3G and promote HIV-1 infection. Nature 481: 371-375.
30. Zhang, W., J. Du, S. L. Evans, Y. Yu, and X. F. Yu. 2012. T-cell differentiation factor CBF-b regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481: 376-379.
31. Huthoff, H., F. Autore, S. Gallois-Montbrun, F. Fraternali, and M. H. Malim. 2009. RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog. 5: e1000330.
32. Apolonia, L., R. Schulz, T. Curk, P. Rocha, C. M. Swanson, T. Schaller, J. Ule, and M. H. Malim. 2015. Promiscuous RNA binding ensures effective encapsidation of APOBEC3 proteins by HIV-1. PLoS Pathog. 11: e1004609.
33. Burnett, A., and P. Spearman. 2007. APOBEC3G multimers are recruited to the plasma membrane for packaging into human immunodeficiency virus type 1 viruslike particles in an RNA-dependent process requiring the NC basic linker. J. Virol. 81: 5000-5013.
34. Svarovskaia, E. S., H. Xu, J. L. Mbisa, R. Barr, R. J. Gorelick, A. Ono, E. O. Freed, W. S. Hu, and V. K. Pathak. 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.
35. Okeoma, C. M., N. Lovsin, B. M. Peterlin, and S. R. Ross. 2007. APOBEC3 inhibits mouse mammary tumour virus replication in vivo. Nature 445: 927-930.
36. Cullen, B. R. 2006. Role and mechanism of action of the APOBEC3 family of antiretroviral resistance factors. J. Virol. 80: 1067-1076.
37. 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. J. Mol. Biol. 337: 585-596.
38. Langlois, M. A., R. C. Beale, S. G. Conticello, and M. S. Neuberger. 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.
39. Armitage, A. E., K. Deforche, J. J. Welch, K. Van Laethem, R. Camacho, A. Rambaut, and A. K. Iversen. 2014. Possible footprints of APOBEC3F and/or other APOBEC3 deaminases, but not APOBEC3G, on HIV-1 from patients with acute/early and chronic infections. J. Virol. 88: 12882-12894.
40. Kim, E. Y., R. Lorenzo-Redondo, S. J. Little, Y. S. Chung, P. K. Phalora, I. Maljkovic Berry, J. Archer, S. Penugonda, W. Fischer, D. D. Richman, et al. 2014. Human APOBEC3 induced mutation of human immunodeficiency virus type-1 contributes to adaptation and evolution in natural infection. PLoS Pathog. 10: e1004281.
41. Jern, P., R. A. Russell, V. K. Pathak, and J. M. Coffin. 2009. Likely role of APOBEC3G-mediated G-to-A mutations in HIV-1 evolution and drug resistance. PLoS Pathog. 5: e1000367.
42. 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. Curr. Biol. 15: 166-170.
43. Holmes, R. K., F. A. Koning, K. N. Bishop, and M. H. Malim. 2007. APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G. J. Biol. Chem. 282: 2587-2595.
44. MacMillan, A. L., R. M. Kohli, and S. R. Ross. 2013. APOBEC3 inhibition of mouse mammary tumor virus infection: the role of cytidine deamination versus inhibition of reverse transcription. J. Virol. 87: 4808-4817.
45. Stavrou, S., T. Nitta, S. Kotla, D. Ha, K. Nagashima, A. R. Rein, H. Fan, and S. R. Ross. 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.
46. Sanchez-Martinez, S., A. L. Aloia, D. Harvin, J. Mirro, R. J. Gorelick, P. Jern, J. M. Coffin, and A. Rein. 2012. Studies on the restriction of murine leukemia viruses by mouse APOBEC3. PLoS One 7: e38190.
47. Jónsson, S. R., R. S. LaRue, M. D. Stenglein, S. C. Fahrenkrug, V. Andrésdóttir, and R. S. Harris. 2007. The restriction of zoonotic PERV transmission by human APOBEC3G. PLoS One 2: e893.
48. Narvaiza, I., D. C. Linfesty, B. N. Greener, Y. Hakata, D. J. Pintel, E. Logue, N. R. Landau, and M. D. Weitzman. 2009. Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog. 5: e1000439.
49. Muckenfuss, H., M. Hamdorf, U. Held, M. Perkovic, J. Löwer, K. Cichutek, E. Flory, G. G. Schumann, and C. Münk. 2006. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J. Biol. Chem. 281: 22161-22172.
50. Stenglein, M. D., and R. S. Harris. 2006. APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J. Biol. Chem. 281: 16837-16841.
51. Chen, H., C. E. Lilley, Q. Yu, D. V. Lee, J. Chou, I. Narvaiza, N. R. Landau, and M. D. Weitzman. 2006. APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr. Biol. 16: 480-485.
52. Okeoma, C. M., A. Low, W. Bailis, H. Y. Fan, B. M. Peterlin, and S. R. Ross. 2009. Induction of APOBEC3 in vivo causes increased restriction of retrovirus infection. J. Virol. 83: 3486-3495.
53. Low, A., C. M. Okeoma, N. Lovsin, M. de las Heras, T. H. Taylor, B. M. Peterlin, S. R. Ross, and H. Fan. 2009. Enhanced replication and pathogenesis of Moloney murine leukemia virus in mice defective in the murine APOBEC3 gene. Virology 385: 455-463.
54. Stavrou, S., D. Crawford, K. Blouch, E. P. Browne, R. M. Kohli, and S. R. Ross. 2014. Different modes of retrovirus restriction by human APOBEC3A and APOBEC3G in vivo. PLoS Pathog. 10: e1004145.
55. Koning, F. A., C. Goujon, H. Bauby, and M. H. Malim. 2011. Target cellmediated editing of HIV-1 cDNA by APOBEC3 proteins in human macrophages. J. Virol. 85: 13448-13452.
56. Vetter, M. L., and R. T. D'Aquila. 2009. Cytoplasmic APOBEC3G restricts incoming Vif-positive human immunodeficiency virus type 1 and increases two-long terminal repeat circle formation in activated T-helper-subtype cells. J. Virol. 83: 8646-8654.
57. Langlois, M. A., K. Kemmerich, C. Rada, and M. S. Neuberger. 2009. The AKV murine leukemia virus is restricted and hypermutated by mouse APOBEC3. J. Virol. 83: 11550-11559.
58. Suspène, R., M. M. Aynaud, S. Koch, D. Pasdeloup, M. Labetoulle, B. Gaertner, J. P. Vartanian, A. Meyerhans, and S. Wain-Hobson. 2011. Genetic editing of herpes simplex virus 1 and Epstein-Barr herpesvirus genomes by human APOBEC3 cytidine deaminases in culture and in vivo. J. Virol. 85: 7594-7602.
59. Vartanian, J. P., D. Guétard, M. Henry, and S. Wain-Hobson. 2008. Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions. Science 320: 230-233.
60. Vartanian, J. P., M. Henry, A. Marchio, R. Suspène, M. M. Aynaud, D. Guétard, M. Cervantes-Gonzalez, C. Battiston, V. Mazzaferro, P. Pineau, et al. 2010. Massive APOBEC3 editing of hepatitis B viral DNA in cirrhosis. PLoS Pathog. 6: e1000928.
61. Refsland, E. W., M. D. Stenglein, K. Shindo, J. S. Albin, W. L. Brown, and R. S. Harris. 2010. Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues: implications for HIV-1 restriction. Nucleic Acids Res. 38: 4274-4284.
62. 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. J. Virol. 83: 9474-9485.
63. Gillick, K., D. Pollpeter, P. Phalora, E. Y. Kim, S. M. Wolinsky, and M. H. Malim. 2013. Suppression of HIV-1 infection by APOBEC3 proteins in primary human CD4(+) T cells is associated with inhibition of processive reverse transcription as well as excessive cytidine deamination. J. Virol. 87: 1508-1517.
64. Land, A. M., T. B. Ball, M. Luo, R. Pilon, P. Sandstrom, J. E. Embree, C. Wachihi, J. Kimani, and F. A. Plummer. 2008. Human immunodeficiency virus (HIV) type 1 proviral hypermutation correlates with CD4 count in HIVinfected women from Kenya. J. Virol. 82: 8172-8182.
65. Jin, X., A. Brooks, H. Chen, R. Bennett, R. Reichman, and H. Smith. 2005. APOBEC3G/CEM15 (hA3G) mRNA levels associate inversely with human immunodeficiency virus viremia. J. Virol. 79: 11513-11516.
66. Pace, C., J. Keller, D. Nolan, I. James, S. Gaudieri, C. Moore, and S. Mallal. 2006. Population level analysis of human immunodeficiency virus type 1 hypermutation and its relationship with APOBEC3G and vif genetic variation. J. Virol. 80: 9259-9269.
67. Kieffer, T. L., P. Kwon, R. E. Nettles, Y. Han, S. C. Ray, and R. F. Siliciano. 2005. G→A hypermutation in protease and reverse transcriptase regions of human immunodeficiency virus type 1 residing in resting CD4+ T cells in vivo. J. Virol. 79: 1975-1980.
68. Koppensteiner, H., R. Brack-Werner, and M. Schindler. 2012. Macrophages and their relevance in Human Immunodeficiency Virus Type I infection. Retrovirology 9: 82.
69. Berger, G., S. Durand, G. Fargier, X. N. Nguyen, S. Cordeil, S. Bouaziz, D. Muriaux, J. L. Darlix, and A. Cimarelli. 2011. APOBEC3A is a specific inhibitor of the early phases of HIV-1 infection in myeloid cells. PLoS Pathog. 7: e1002221.
70. Laguette, N., N. Rahm, B. Sobhian, C. Chable-Bessia, J. Münch, J. Snoeck, D. Sauter, W. M. Switzer, W. Heneine, F. Kirchhoff, et al. 2012. Evolutionary and functional analyses of the interaction between the myeloid restriction factor SAMHD1 and the lentiviral Vpx protein. Cell Host Microbe 11: 205-217.
71. Cassetta, L., A. Kajaste-Rudnitski, T. Coradin, E. Saba, G. Della Chiara, M. Barbagallo, F. Graziano, M. Alfano, E. Cassol, E. Vicenzi, and G. Poli. 2013. M1 polarization of human monocyte-derived macrophages restricts pre and postintegration steps of HIV-1 replication. AIDS 27: 1847-1856.
72. Lahouassa, H., W. Daddacha, H. Hofmann, D. Ayinde, E. C. Logue, L. Dragin, N. Bloch, C. Maudet, M. Bertrand, T. Gramberg, et al. 2012. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat. Immunol. 13: 223-228.
73. 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. J. Virol. 87: 444-453.
74. Peng, G., T. Greenwell-Wild, S. Nares, W. Jin, K. J. Lei, Z. G. Rangel, P. J. Munson, and S. M. Wahl. 2007. Myeloid differentiation and susceptibility to HIV-1 are linked to APOBEC3 expression. Blood 110: 393-400.
75. Biasin, M., L. Piacentini, S. Lo Caputo, Y. Kanari, G. Magri, D. Trabattoni, V. Naddeo, L. Lopalco, A. Clivio, E. Cesana, et al. 2007. Apolipoprotein B mRNAediting enzyme, catalytic polypeptide-like 3G: a possible role in the resistance to HIV of HIV-exposed seronegative individuals. J. Infect. Dis. 195: 960-964.
76. Cavrois, M., J. Neidleman, J. F. Kreisberg, D. Fenard, C. Callebaut, and W. C. Greene. 2006. Human immunodeficiency virus fusion to dendritic cells declines as cells mature. J. Virol. 80: 1992-1999.
77. Coleman, C. M., and L. Wu. 2009. HIV interactions with monocytes and dendritic cells: viral latency and reservoirs. Retrovirology 6: 51.
78. Chen, B. K. 2012. T cell virological synapses and HIV-1 pathogenesis. Immunol. Res. 54: 133-139.
79. Yamamoto, T., Y. Tsunetsugu-Yokota, Y. Y. Mitsuki, F. Mizukoshi, T. Tsuchiya, K. Terahara, Y. Inagaki, N. Yamamoto, K. Kobayashi, and J. Inoue. 2009. Selective transmission of R5 HIV-1 over X4 HIV-1 at the dendritic cell-T cell infectious synapse is determined by the T cell activation state. PLoS Pathog. 5: e1000279.
80. Mohanram, V., A. E. Sköld, S. M. Bächle, S. K. Pathak, and A. L. Spetz. 2013. IFN-a induces APOBEC3G, F, and A in immature dendritic cells and limits HIV-1 spread to CD4+ T cells. J. Immunol. 190: 3346-3353.
81. Peng, G., K. J. Lei, W. Jin, T. Greenwell-Wild, and S. M. Wahl. 2006. Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J. Exp. Med. 203: 41-46.
82. McLellan, A. D. 2009. Exosome release by primary B cells. Crit. Rev. Immunol. 29: 203-217.
83. Khatua, A. K., H. E. Taylor, J. E. Hildreth, and W. Popik. 2009. Exosomes packaging APOBEC3G confer human immunodeficiency virus resistance to recipient cells. J. Virol. 83: 512-521.
84. Seidl, T., T. Whittall, K. Babaahmady, and T. Lehner. 2012. B-cell agonists upregulate AID and APOBEC3G deaminases, which induce IgA and IgG class antibodies and anti-viral function. Immunology 135: 207-215.
85. Wang, X., W. Chao, M. Saini, and M. J. Potash. 2011. A common path to innate immunity to HIV-1 induced by Toll-like receptor ligands in primary human macrophages. PLoS One 6: e24193.
86. Mehta, H. V., P. H. Jones, J. P. Weiss, and C. M. Okeoma. 2012. IFN-a and lipopolysaccharide upregulate APOBEC3 mRNA through different signaling pathways. J. Immunol. 189: 4088-4103.
87. Chen, K., J. Huang, C. Zhang, S. Huang, G. Nunnari, F. X. Wang, X. Tong, L. Gao, K. Nikisher, and H. Zhang. 2006. Alpha interferon potently enhances the anti-human immunodeficiency virus type 1 activity of APOBEC3G in resting primary CD4 T cells. J. Virol. 80: 7645-7657.
88. Sarkis, P. T., S. Ying, R. Xu, and X. F. Yu. 2006. STAT1-independent cell typespecific regulation of antiviral APOBEC3G by IFN-alpha. J. Immunol. 177: 4530-4540.
89. Stopak, K. S., Y. L. Chiu, J. Kropp, R. M. Grant, and W. C. Greene. 2007. Distinct patterns of cytokine regulation of APOBEC3G expression and activity in primary lymphocytes, macrophages, and dendritic cells. J. Biol. Chem. 282: 3539-3546.
90. Goubau, D., S. Deddouche, and C. Reis e Sousa. 2013. Cytosolic sensing of viruses. Immunity 38: 855-869.
91. Lahaye, X., T. Satoh, M. Gentili, S. Cerboni, C. Conrad, I. Hurbain, A. El Marjou, C. Lacabaratz, J. D. Lelièvre, and N. Manel. 2013. The capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity 39: 1132-1142.
92. Gao, D., J. Wu, Y. T. Wu, F. Du, C. Aroh, N. Yan, L. Sun, and Z. J. Chen. 2013. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341: 903-906.
93. Stavrou, S., K. Blouch, S. Kotla, A. Bass, and S. R. Ross. 2015. Nucleic acid recognition orchestrates the anti-viral response to retroviruses. Cell Host Microbe 17: 478-488.
94. Norman, J. M., M. Mashiba, L. A. McNamara, A. Onafuwa-Nuga, E. Chiari-Fort, W. Shen, and K. L. Collins. 2011. The antiviral factor APOBEC3G enhances the recognition of HIV-infected primary T cells by natural killer cells. Nat. Immunol. 12: 975-983.
95. Pillai, S. K., J. K. Wong, and J. D. Barbour. 2008. Turning up the volume on mutational pressure: is more of a good thing always better? (A case study of HIV-1 Vif and APOBEC3). Retrovirology 5: 26.
96. Addo, M. M., X. G. Yu, E. S. Rosenberg, B. D. Walker, and M. Altfeld. 2002. Cytotoxic T-lymphocyte (CTL) responses directed against regulatory and accessory proteins in HIV-1 infection. DNA Cell Biol. 21: 671-678.
97. Kiepiela, P., K. Ngumbela, C. Thobakgale, D. Ramduth, I. Honeyborne, E. Moodley, S. Reddy, C. de Pierres, Z. Mncube, N. Mkhwanazi, et al. 2007. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13: 46-53.
98. Monajemi, M., C. F. Woodworth, K. Zipperlen, M. Gallant, M. D. Grant, and M. Larijani. 2014. Positioning of APOBEC3G/F mutational hotspots in the human immunodeficiency virus genome favors reduced recognition by CD8+ T cells. PLoS One 9: e93428.
99. Casartelli, N., F. Guivel-Benhassine, R. Bouziat, S. Brandler, O. Schwartz, and A. Moris. 2010. The antiviral factor APOBEC3G improves CTL recognition of cultured HIV-infected T cells. J. Exp. Med. 207: 39-49.
100. Shankar, P., M. Russo, B. Harnisch, M. Patterson, P. Skolnik, and J. Lieberman. 2000. Impaired function of circulating HIV-specific CD8(+) T cells in chronic human immunodeficiency virus infection. Blood 96: 3094-3101.
101. Ogg, G. S., X. Jin, S. Bonhoeffer, P. R. Dunbar, M. A. Nowak, S. Monard, J. P. Segal, Y. Cao, S. L. Rowland-Jones, V. Cerundolo, et al. 1998. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279: 2103-2106.
102. Tsuji-Kawahara, S., T. Chikaishi, E. Takeda, M. Kato, S. Kinoshita, E. Kajiwara, S. Takamura, and M. Miyazawa. 2010. Persistence of viremia and production of neutralizing antibodies differentially regulated by polymorphic APOBEC3 and BAFF-R loci in friend virus-infected mice. J. Virol. 84: 6082-6095.
103. Takeda, E., S. Tsuji-Kawahara, M. Sakamoto, M. A. Langlois, M. S. Neuberger, C. Rada, and M. Miyazawa. 2008. Mouse APOBEC3 restricts friend leukemia virus infection and pathogenesis in vivo. J. Virol. 82: 10998-11008.
104. Peled, J. U., F. L. Kuang, M. D. Iglesias-Ussel, S. Roa, S. L. Kalis, M. F. Goodman, and M. D. Scharff. 2008. The biochemistry of somatic hypermutation. Annu. Rev. Immunol. 26: 481-511.
105. Halemano, K., K. Guo, K. J. Heilman, B. S. Barrett, D. S. Smith, K. J. Hasenkrug, and M. L. Santiago. 2014. Immunoglobulin somatic hypermutation by APOBEC3/Rfv3 during retroviral infection. Proc. Natl. Acad. Sci. USA 111: 7759-7764.
106. Kato, M., S. Tsuji-Kawahara, Y. Kawasaki, S. Kinoshita, T. Chikaishi, S. Takamura, M. Fujisawa, A. Kawada, and M. Miyazawa. 2015. Class switch recombination and somatic hypermutation of virus-neutralizing antibodies are not essential for control of friend retrovirus infection. J. Virol. 89: 1468-1473.
107. Landry, S., I. Narvaiza, D. C. Linfesty, and M. D. Weitzman. 2011. APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep. 12: 444-450.
108. Burns, M. B., N. A. Temiz, and R. S. Harris. 2013. Evidence for APOBEC3B mutagenesis in multiple human cancers. Nat. Genet. 45: 977-983.