Conservation and Innovation of APOBEC3A Restriction Functions during Primate Evolution

Molecular Biology and Evolution

Volumn 33, Issue 8, 2016, Pages 1889-1901

  McLaughlin, Richard N ^a   Gable, Jacob T ^a,d   Wittkopp, Cristina J ^a,b   Emerman, Michael ^a   Malik, Harmit S ^a,c  

^a USA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

APOBEC3A; innate immunity; LINE 1; positive selection; primates; restriction factor; retroelements

Indexed keywords

APOBEC3A PROTEIN; CYTIDINE DEAMINASE; UNCLASSIFIED DRUG; APOBEC3A PROTEIN, HUMAN; PROTEIN; RETROPOSON;

AMINO ACID SUBSTITUTION; APOBEC3A GENE; ARTICLE; CERCOPITHECIDAE; CHIMERA; DIVERSIFYING SELECTION; GENE; GENE SEQUENCE; GENETIC CONSERVATION; HOST PATHOGEN INTERACTION; HUMAN GENOME; LONG INTERSPERSED REPEAT; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIMATE; RETROPOSON; ANIMAL; EVOLUTION; GENETICS; HUMAN; METABOLISM;

ANIMALS; BIOLOGICAL EVOLUTION; CERCOPITHECIDAE; CYTIDINE DEAMINASE; EVOLUTION, MOLECULAR; GENOME, HUMAN; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; PRIMATES; PROTEINS; RETROELEMENTS;

EID: 84982994774     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw070     Document Type: Article

References (94)

1. Aguiar RS, Lovsin N, Tanuri A, Peterlin BM. 2008. Vpr. A3A chimera inhibits HIV replication. J Biol Chem. 283:2518-2525.
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. AnW, Dai L, NiewiadomskaAM, Yetil A, O'DonnellKA, HanJS, Boeke JD. 2011. Characterization of a synthetic human LINE-1 retrotransposon ORFeus-Hs. Mob DNA. 2:2.
4. An W, Han JS, Wheelan SJ, Davis ES, Coombes CE, Ye P, Triplett C, Boeke JD. 2006. Active retrotransposition by a synthetic L1 element inmice. Proc Natl Acad Sci U S A. 103:18662-18667.
5. Arias JF, Koyama T, Kinomoto M, Tokunaga K. 2012. Retroelements versus APOBEC3 family members: no great escape from the magnificent seven. Front Microbiol. 3:275.
6. Ashkenazy H, Penn O, Doron-Faigenboim A, Cohen O, Cannarozzi G, Zomer O, Pupko T. 2012. FastML: a web server for probabilistic reconstruction of ancestral sequences. Nucleic Acids Res. 40:W580-W584.
7. Beck CR, Garcia-Perez JL, Badge RM, Moran JV. 2011. LINE-1 elements in structural variation and disease. Annu Rev Genomics Hum Genet. 12:187-215.
8. Bishop KN, Holmes RK, Sheehy AM, Davidson NO, Cho SJ, Malim MH. 2004. Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr Biol. 14:1392-1396.
9. Bogerd HP, Tallmadge RL, Oaks JL, Carpenter S, Cullen BR. 2008. Equine infectious anemia virus resists the antiretroviral activity of equine APOBEC3 proteins through a packaging-independent mechanism. J Virol. 82:11889-11901.
10. Bogerd HP, Wiegand HL, Doehle BP, Lueders KK, Cullen BR. 2006. APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res. 34:89-95.
11. Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, Moran JV, Cullen BR. 2006. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci U S A. 103:8780-8785.
12. Bohn MF, Shandilya SM, Silvas TV, Nalivaika EA, Kouno T, Kelch BA, Ryder SP, Kurt-Yilmaz N, Somasundaran M, Schiffer CA. 2015. The ssDNA mutator APOBEC3A is regulated by cooperative dimerization. Structure 23:903-911.
13. Boissinot S, Davis J, Entezam A, Petrov D, Furano AV. 2006. Fitness cost of LINE-1 (L1) activity in humans. Proc Natl Acad Sci U S A. 103:9590-9594.
14. Boissinot S, Entezam A, Furano AV. 2001. Selection against deleterious LINE-1-containing loci in the human lineage. Mol Biol Evol. 18:926-935.
15. Brouha B, Meischl C, Ostertag E, de Boer M, Zhang Y, Neijens H, RoosD, Kazazian HH Jr. 2002. Evidence consistent with human L1 retrotransposition in maternal meiosis I. Am J Hum Genet. 71:327-336.
16. Bulliard Y, Narvaiza I, Bertero A, Peddi S, Rohrig UF, Ortiz M, Zoete V, Castro-Diaz N, Turelli P Telenti A, et al. 2011. Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities. J Virol. 85:1765-1776.
17. Byeon IJ, Ahn J, MitraM, Byeon CH, Hercik K, Hritz J, Charlton LM, Levin JG, Gronenborn AM. 2013. NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat Commun. 4:1890.
18. Castro-Diaz N, Ecco G, Coluccio A, Kapopoulou A, Yazdanpanah B, Friedli M, Duc J, Jang SM, Turelli P, Trono D. 2014. Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev. 28:1397-1409.
19. Chen H, Lilley CE, Yu Q, Lee DV, Chou J, Narvaiza I, Landau NR, Weitzman MD. 2006. APOBEC3A is a potent inhibitor of adenoassociated virus and retrotransposons. Curr Biol. 16:480-485.
20. Compton AA, Emerman M. 2013. Convergence and divergence in the evolution of the APOBEC3G-Vif interaction reveal ancient origins of simian immunodeficiency viruses. PLoS Pathog. 9:e1003135.
21. Compton AA, Hirsch VM, Emerman M. 2012. The host restriction factor APOBEC3G and retroviral Vif protein coevolve due to ongoing genetic conflict. Cell Host Microbe. 11:91-98.
22. Compton AA, Malik HS, Emerman M. 2013. Host gene evolution traces the evolutionary history of ancient primate lentiviruses. Philos Trans R Soc Lond B Biol Sci. 368:20120496.
23. Conticello SG, Thomas CJ, Petersen-Mahrt SK, Neuberger MS. 2005. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol Biol Evol. 22:367-377.
24. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, Morell M, O'Shea KS, Moran JV, Gage FH. 2009. L1 retrotransposition in human neural progenitor cells. Nature. 460:1127-1131.
25. CrowYJ, Hayward BE, Parmar R, Robins P, Leitch A, AliM, Black DN, van Bokhoven H, Brunner HG, Hamel BC, et al. 2006. Mutations in the gene encoding the 3'-5' DNA exonuclease TREX1 cause Aicardi-Goutieres syndrome at the AGS1 locus. Nat Genet. 38:917-920.
26. Crow YJ, Rehwinkel J. 2009. Aicardi-Goutieres syndrome and related phenotypes: linking nucleic acid metabolism with autoimmunity. Hum Mol Genet. 18:R130-R136.
27. DaughertyMD, Malik HS. 2012. Rules of engagement: molecular insights from host-virus arms races. Annu Rev Genet. 46:677-700.
28. de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD. 2011. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet. 7:e1002384.
29. Dombroski BA, Mathias SL, Nanthakumar E, Scott AF, Kazazian HH Jr. 1991. Isolation of an active human transposable element. Science 254:1805-1808.
30. DuggalNK, Malik HS, Emerman M. 2011. The breadth of antiviral activity of Apobec3DE in chimpanzees has been driven by positive selection. J Virol. 85:11361-11371.
31. EldeNC, Child SJ, GeballeAP, MalikHS. 2009. Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457:485-489.
32. Elde NC, Malik HS. 2009. The evolutionary conundrum of pathogen mimicry. Nat Rev Microbiol. 7:787-797.
33. Esnault C, Priet S, Ribet D, Heidmann O, Heidmann T. 2008. Restriction by APOBEC3 proteins of endogenous retroviruses with an extracellular life cycle: ex vivo effects and in vivo traces on the murine IAPE and human HERV-K elements. Retrovirology 5:75.
34. Feng Q, Moran JV, Kazazian HH Jr, Boeke JD. 1996. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87:905-916.
35. Friedli M, Turelli P, Kapopoulou A, Rauwel B, Castro-Diaz N, Rowe HM, Ecco G, Unzu C, Planet E Lombardo A, et al. 2014. Loss of transcriptional control over endogenous retroelements during reprogramming to pluripotency. Genome Res. 24:1251-1259.
36. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6:343-345.
37. Goila-Gaur R, Khan MA, Miyagi E, Kao S, Strebel K. 2007. Targeting APOBEC3A to the viral nucleoprotein complex confers antiviral activity. Retrovirology 4:61.
38. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
39. Hancks DC, Kazazian HH Jr. 2012. Active human retrotransposons: variation and disease. Curr Opin Genet Dev. 22:191-203.
40. Henry M, Terzian C, Peeters M, Wain-Hobson S, Vartanian JP. 2012. Evolution of the primate APOBEC3A cytidine deaminase gene and identification of related coding regions. PLoS One 7:e30036.
41. Hu S, Li J, Xu F, Mei S, Le Duff Y, Yin L, Pang X, Cen S, Jin Q Liang C, et al. 2015. SAMHD1 inhibits LINE-1 retrotransposition by promoting stress granule formation. PLoS Genet. 11:e1005367.
42. Jacobs FM, Greenberg D, Nguyen N, Haeussler M, Ewing AD, Katzman S, Paten B, Salama SR, Haussler D. 2014. An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons. Nature 516:242-245.
43. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 110:462-467.
44. Katuwal M, Wang Y, Schmitt K, Guo K, Halemano K, Santiago ML, Stephens EB. 2014. Cellular HIV-1 inhibition by truncated old world primate APOBEC3A proteins lacking a complete deaminase domain. Virology 468-470:532-544.
45. Kidd JM, Newman TL, Tuzun E, Kaul R, Eichler EE. 2007. Population stratification of a common APOBEC gene deletion polymorphism. PLoS Genet. 3:e63.
46. KinomotoM, Kanno T, ShimuraM, Ishizaka Y, Kojima A, Kurata T, Sata T, Tokunaga K. 2007. All APOBEC3 family proteins differentially inhibit LINE-1 retrotransposition. Nucleic Acids Res. 35:2955-2964.
47. Kosakovsky Pond SL, Posada D, GravenorMB, Woelk CH, Frost SD. 2006. Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol. 23:1891-1901.
48. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
49. Marin M, Golem S, Rose KM, Kozak SL, Kabat D. 2008. Human immunodeficiency virus type 1 Vif functionally interacts with diverse APOBEC3 cytidine deaminases and moves with them between cytoplasmic sites of mRNA metabolism. J Virol. 82:987-998.
50. Martin SL, Bushman FD. 2001. Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol Cell Biol. 21:467-475.
51. Mathias SL, Scott AF, Kazazian HH Jr, Boeke JD, Gabriel A. 1991. Reverse transcriptase encoded by a human transposable element. Science 254:1808-1810.
52. Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, MarkelovML, Lukyanov SA. 1999. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol. 17:969-973.
53. Mikl MC, Watt IN, Lu M, Reik W, Davies SL, Neuberger MS, Rada C. 2005. Mice deficient in APOBEC2 and APOBEC3. Mol Cell Biol. 25:7270-7277.
54. Mitchell PS, Patzina C, Emerman M, Haller O, Malik HS, Kochs G. 2012. Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12:598-604.
55. Mitchell PS, Young JM, Emerman M, Malik HS. 2015. Evolutionary analyses suggest a function ofMxB immunity proteins beyond lentivirus restriction. PLoS Pathog. 11:e1005304.
56. Molaro A, Malik HS. 2016. Hide and seek: how chromatin-based pathways silence retroelements in the mammalian germline. Curr Opin Genet Dev. 37:51-58.
57. Montgomery E, Charlesworth B, Langley CH. 2007. A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res. 89:435-445.
58. Moran JV, Holmes SE, Naas TP, DeBerardinisRJ, Boeke JD, KazazianHH Jr. 1996. High frequency retrotransposition in cultured mammalian cells. Cell 87:917-927.
59. Munk C, Willemsen A, Bravo IG. 2012. An ancient history of gene duplications, fusions and losses in the evolution of APOBEC3 mutators in mammals. BMC Evol Biol. 12:71.
60. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K. 2013. FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol. 30:1196-1205.
61. Nielsen R, Yang Z. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929-936.
62. OhAinle M, Kerns JA, Malik HS, Emerman M. 2006. Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H. J Virol. 80:3853-3862.
63. Ooi SK, O'Donnell AH, Bestor TH. 2009. Mammalian cytosine methylation at a glance. J Cell Sci. 122:2787-2791.
64. Ooms M, Krikoni A, Kress AK, Simon V, Munk C. 2012. APOBEC3A, APOBEC3B, and APOBEC3H haplotype 2 restrict human T-lymphotropic virus type 1. J Virol. 86:6097-6108.
65. Ostertag EM, Prak ET, DeBerardinis RJ, Moran JV, Kazazian HH Jr. 2000. Determination of L1 retrotransposition kinetics in cultured cells. Nucleic Acids Res. 28:1418-1423.
66. Perelman P, JohnsonWE, Roos C, Seuanez HN, Horvath JE, Moreira MA, Kessing B, Pontius J, Roelke M, Rumpler Y, et al. 2011. A molecular phylogeny of living primates. PLoS Genet. 7:e1001342.
67. Richardson SR, Doucet AJ, Kopera HC, Moldovan JB, Garcia-Perez JL, Moran JV. 2015. The influence of LINE-1 and SINE retrotransposons on mammalian genomes. Microbiol Spectr. 3:MDNA3-M0061.
68. Richardson SDA, Kopera H, Moldovan J, Garcia-Perez J, Moran J. 2015. The Influence of LINE-1 and SINE Retrotransposons on Mammalian Genomes. In: Craig NCM, Gellert M, Lambowitz A, Rice P, Sandmeyer S, editors. Mobile DNA III. Washington, DC: ASM Press. p. 1165-1208.
69. Richardson SR, Narvaiza I, Planegger RA, Weitzman MD, Moran JV. 2014. APOBEC3A deaminates transiently exposed single-strand DNA during LINE-1 retrotransposition. Elife 3:e02008.
70. Rose KM, Marin M, Kozak SL, Kabat D. 2005. Regulated production and anti-HIV type 1 activities of cytidine deaminases APOBEC3B, 3F, and 3G. AIDS Res Hum Retroviruses 21:611-619.
71. Sawyer SL, Wu LI, Emerman M, Malik HS. 2005. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A. 102:2832-2837.
72. Schmitt K, Guo K, Algaier M, Ruiz A, Cheng F, Qiu J, Wissing S, Santiago ML, Stephens EB. 2011. Differential virus restriction patterns of rhesus macaque and human APOBEC3A: implications for lentivirus evolution. Virology 419:24-42.
73. Schmitt K, Guo K, Katuwal M, Wilson D, Prochnow C, Bransteitter R, Chen XS, Santiago ML, Stephens EB. 2013. Lentivirus restriction by diverse primate APOBEC3A proteins. Virology 442:82-96.
74. Scott AF, Schmeckpeper BJ, AbdelrazikM, ComeyCT, O'Hara B, Rossiter JP, Cooley T, Heath P, Smith KD, Margolet L. 1987. Origin of the human L1 elements: proposed progenitor genes deduced from a consensus DNA sequence. Genomics 1:113-125.
75. Sheehy AM, Gaddis NC, Choi JD, MalimMH. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650.
76. Sheehy AM, Gaddis NC, Malim MH. 2003. The antiretroviral enzyme APOBEC3Gis degraded by the proteasome in response toHIV-1Vif. Nat Med. 9:1404-1407.
77. Steinglein MD, Harris RS. 2006. APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independentmechanism. J Biol Chem. 281:16837-16841.
78. Song M, Boissinot S. 2007. Selection against LINE-1 retrotransposons results principally from their ability to mediate ectopic recombination. Gene 390:206-213.
79. Stavrou S, Crawford D, Blouch K, Browne EP, Kohli RM, Ross SR. 2014. Different modes of retrovirus restriction by human APOBEC3A and APOBEC3G in vivo. PLoS Pathog. 10:e1004145.
80. Stenglein MD, Burns MB, Li M, Lengyel J, Harris RS. 2010. APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat Struct Mol Biol. 17:222-229.
81. Stetson DB, Ko JS, Heidmann T, Medzhitov R. 2008. Trex1 prevents cellintrinsic initiation of autoimmunity. Cell 134:587-598.
82. Takeda E, Tsuji-Kawahara S, Sakamoto M, Langlois MA, Neuberger MS, Rada C, Miyazawa M. 2008. Mouse APOBEC3 restricts friend leukemia virus infection and pathogenesis in vivo. J Virol. 82:10998-11008.
83. Thielen BK, McNevin JP, McElrath MJ, Hunt BV, Klein KC, Lingappa JR. 2010. Innate immune signaling induces high levels of TC-specific deaminase activity in primary monocyte-derived cells through expression of APOBEC3A isoforms. J Biol Chem. 285:27753-27766.
84. Turelli P, Castro-Diaz N, Marzetta F, Kapopoulou A, Raclot C, Duc J, Tieng V, Quenneville S, Trono D. 2014. Interplay of TRIM28 and DNA methylation in controlling human endogenous retroelements. Genome Res. 24:1260-1270.
85. Volkman HE, Stetson DB. 2014. The enemy within: endogenous retroelements and autoimmune disease. Nat Immunol. 15:415-422.
86. Warren CJ, Xu T, Guo K, Griffin LM, Westrich JA, Lee D, Lambert PF, Santiago ML, Pyeon D. 2015. APOBEC3A functions as a restriction factor of human papillomavirus. J Virol. 89:688-702.
87. Wiegand HL, Doehle BP, Bogerd HP, Cullen BR. 2004. A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J. 23:2451-2458.
88. Wissing S, Munoz-Lopez M, Macia A, Yang Z, Montano M, Collins W, Garcia-Perez JL, Moran JV, Greene WC. 2012. Reprogramming somatic cells into iPS cells activates LINE-1 retroelement mobility. Hum Mol Genet 21:208-218.
89. Woelk CH, Frost SD, Richman DD, Higley PE, Kosakovsky Pond SL. 2007. Evolution of the interferon alpha gene family in eutherianmammals. Gene 397:38-50.
90. Xie Y, Rosser JM, Thompson TL, Boeke JD, AnW. 2011. Characterization of L1 retrotransposition with high-throughput dual-luciferase assays. Nucleic Acids Res. 39:e16.
91. Yamashita M, Emerman M. 2004. Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J Virol. 78:5670-5678.
92. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
93. Yoder JA, Walsh CP, Bestor TH. 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13:335-340.
94. Zhao K, Du J, Han X, Goodier JL, Li P, Zhou X, Wei W, Evans SL, Li L, ZhangW, et al. 2013. Modulation of LINE-1 and Alu/SVA retrotransposition by Aicardi-Goutieres syndrome-related SAMHD1. Cell Rep. 4:1108-1115.