Differential inhibition of LINE1 and LINE2 retrotransposition by vertebrate AID/APOBEC proteins

Retrovirology

Nika Lovšin²  Erez Y Levanon³  Binyamin A Knisbacher³  Toni Petan¹  Maruška Budič²  Nataša Lindič² 

[1] Department of Molecular and Biomedical Sciences, Jožef Stefan Institute, SI-1000, Ljubljana, Slovenia;Department of Chemistry and Biochemistry, Chair of Biochemistry, Faculty of Chemistry and Chemical Technology, University of Ljubljana, SI-1000, Ljubljana, Slovenia;The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan 52900, Israel

关键词: Retrotransposon;    Cytidine deaminase;    Zebrafish APOBEC2;    LINE1;    Zebrafish LINE2;    Lizard APOBEC1;    ORF1p;    APOBEC3;    AID;    G to A hypermutation;   

Others  :  805691
DOI  :  10.1186/1742-4690-10-156

 received in 2013-08-04, accepted in 2013-12-02,  发布年份 2013

【 摘 要 】

Background

The role of AID/APOBEC proteins in the mammalian immune response against retroviruses and retrotransposons is well established. G to A hypermutations, the hallmark of their cytidine deaminase activity, are present in several mammalian retrotransposons. However, the role of AID/APOBEC proteins in non-mammalian retroelement restriction is not completely understood.

Results

Here we provide the first evidence of anti-retroelement activity of a reptilian APOBEC protein. The green anole lizard A1 protein displayed potent DNA mutator activity and inhibited ex vivo retrotransposition of LINE1 and LINE2 ORF1 protein encoding elements, displaying a mechanism of action similar to that of the human A1 protein. In contrast, the human A3 proteins did not require ORF1 protein to inhibit LINE retrotransposition, suggesting a differential mechanism of anti-LINE action of A1 proteins, which emerged in amniotes, and A3 proteins, exclusive to placental mammals. In accordance, genomic analyses demonstrate differential G to A DNA editing of LINE retrotransposons in the lizard genome, which is also the first evidence for G to A DNA editing in non-mammalian genomes.

Conclusion

Our data suggest that vertebrate APOBEC proteins differentially inhibit the retrotransposition of LINE elements and that the anti-retroelement activity of APOBEC proteins predates mammals.

【 授权许可】

   
2013 Lindič et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Kazazian HH Jr: Mobile elements: drivers of genome evolution. Science 2004, 303:1626-1632.
• [2]Goodier JL, Kazazian HH Jr: Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 2008, 135:23-35.
• [3]Khazina E, Truffault V, Buttner R, Schmidt S, Coles M, Weichenrieder O: Trimeric structure and flexibility of the L1ORF1 protein in human L1 retrotransposition. Nat Struct Mol Biol 2011, 18:1006-1014.
• [4]Khazina E, Weichenrieder O: Non-LTR retrotransposons encode noncanonical RRM domains in their first open reading frame. Proc Natl Acad Sci U S A 2009, 106:731-736.
• [5]Holmes SE, Singer MF, Swergold GD: Studies on p40, the leucine zipper motif-containing protein encoded by the first open reading frame of an active human LINE-1 transposable element. J Biol Chem 1992, 267:19765-19768.
• [6]Hohjoh H, Singer MF: Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J 1996, 15:630-639.
• [7]Kolosha VO, Martin SL: High-affinity, non-sequence-specific RNA binding by the open reading frame 1 (ORF1) protein from long interspersed nuclear element 1 (LINE-1). J Biol Chem 2003, 278:8112-8117.
• [8]Doucet AJ, Hulme AE, Sahinovic E, Kulpa DA, Moldovan JB, Kopera HC, Athanikar JN, Hasnaoui M, Bucheton A, Moran JV, Gilbert N: Characterization of LINE-1 ribonucleoprotein particles. PLoS Genet 2010., 6
• [9]Feng Q, Moran JV, Kazazian HH Jr, Boeke JD: Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 1996, 87:905-916.
• [10]Mathias SL, Scott AF, Kazazian HH Jr, Boeke JD, Gabriel A: Reverse transcriptase encoded by a human transposable element. Science 1991, 254:1808-1810.
• [11]Sugano T, Kajikawa M, Okada N: Isolation and characterization of retrotransposition-competent LINEs from zebrafish. Gene 2006, 365:74-82.
• [12]Kajikawa M, Okada N: LINEs mobilize SINEs in the eel through a shared 3′ sequence. Cell 2002, 111:433-444.
• [13]Kajikawa M, Sugano T, Sakurai R, Okada N: Low dependency of retrotransposition on the ORF1 protein of the zebrafish LINE, ZfL2-1. Gene 2012, 499:41-47.
• [14]Esnault C, Maestre J, Heidmann T: Human LINE retrotransposons generate processed pseudogenes. Nat Genet 2000, 24:363-367.
• [15]Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, Kazazian HH, Boeke JD, Moran JV: Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol 2001, 21:1429-1439.
• [16]Dewannieux M, Esnault C, Heidmann T: LINE-mediated retrotransposition of marked Alu sequences. Nat Genet 2003, 35:41-48.
• [17]Okada N, Hamada M, Ogiwara I, Ohshima K: SINEs and LINEs share common 3′ sequences: a review. Gene 1997, 205:229-243.
• [18]Lovšin N, Gubenšek F, Kordiš D: Evolutionary dynamics in a novel L2 clade of non-LTR retrotransposons in Deuterostomia. Mol Biol Evol 2001, 18:2213-2224.
• [19]Kordiš D, Lovšin N, Gubenšek F: Phylogenomic analysis of the L1 retrotransposons in Deuterostomia. Syst Biol 2006, 55:886-901.
• [20]Piskurek O, Nishihara H, Okada N: The evolution of two partner LINE/SINE families and a full-length chromodomain-containing Ty3/Gypsy LTR element in the first reptilian genome of Anolis carolinensis. Gene 2009, 441:111-118.
• [21]Furano AV, Duvernell DD, Boissinot S: L1 (LINE-1) retrotransposon diversity differs dramatically between mammals and fish. Trends Genet 2004, 20:9-14.
• [22]Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al.: Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
• [23]Conticello SG: The AID/APOBEC family of nucleic acid mutators. Genome Biol 2008, 9:229.
• [24]Severi F, Chicca A, Conticello SG: Analysis of reptilian APOBEC1 suggests that RNA editing may not be its ancestral function. Mol Biol Evol 2011, 28:1125-1129.
• [25]Novick PA, Basta H, Floumanhaft M, McClure MA, Boissinot S: The evolutionary dynamics of autonomous non-LTR retrotransposons in the lizard Anolis carolinensis shows more similarity to fish than mammals. Mol Biol Evol 2009, 26:1811-1822.
• [26]Rogozin IB, Basu MK, Jordan IK, Pavlov YI, Koonin EV: APOBEC4, a new member of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases predicted by computational analysis. Cell Cycle 2005, 4:1281-1285.
• [27]Kordiš D: Transposable elements in reptilian and avian (sauropsida) genomes. Cytogenet Genome Research 2009, 127:94-111.
• [28]Bohne A, Brunet F, Galiana-Arnoux D, Schultheis C, Volff JN: Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res 2008, 16:203-215.
• [29]Sawyer SL, Emerman M, Malik HS: Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2004, 2:E275.
• [30]OhAinle M, Kerns JA, Li MM, Malik HS, Emerman M: Antiretroelement activity of APOBEC3H was lost twice in recent human evolution. Cell Host Microbe 2008, 4:249-259.
• [31]OhAinle M, Kerns JA, Malik HS, Emerman M: Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H. J Virol 2006, 80:3853-3862.
• [32]Volff JN, Bouneau L, Ozouf-Costaz C, Fischer C: Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet 2003, 19:674-678.
• [33]Malik HS, Burke WD, Eickbush TH: The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol 1999, 16:793-805.
• [34]Malik HS, Eickbush TH: The RTE class of non-LTR retrotransposons is widely distributed in animals and is the origin of many SINEs. Mol Biol Evol 1998, 15:1123-1134.
• [35]Conticello SG, Thomas CJ, Petersen-Mahrt SK, Neuberger MS: Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol Biol Evol 2005, 22:367-377.
• [36]Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, Cairns BR: DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 2008, 135:1201-1212.
• [37]Etard C, Roostalu U, Strahle U: Lack of Apobec2-related proteins causes a dystrophic muscle phenotype in zebrafish embryos. J Cell Biol 2010, 189:527-539.
• [38]Sato Y, Probst HC, Tatsumi R, Ikeuchi Y, Neuberger MS, Rada C: Deficiency in APOBEC2 leads to a shift in muscle fiber type, diminished body mass, and myopathy. J Biol Chem 2010, 285:7111-7118.
• [39]Navaratnam N, Morrison JR, Bhattacharya S, Patel D, Funahashi T, Giannoni F, Teng BB, Davidson NO, Scott J: The p27 catalytic subunit of the apolipoprotein B mRNA editing enzyme is a cytidine deaminase. J Biol Chem 1993, 268:20709-20712.
• [40]Teng B, Burant CF, Davidson NO: Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 1993, 260:1816-1819.
• [41]Blanc V, Davidson NO: APOBEC-1-mediated RNA editing. Wiley Interdiscip Rev Syst Biol Med 2010, 2:594-602.
• [42]Jarmuz A, Chester A, Bayliss J, Gisbourne J, Dunham I, Scott J, Navaratnam N: An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 2002, 79:285-296.
• [43]Li MM, Emerman M: Polymorphism in human APOBEC3H affects a phenotype dominant for subcellular localization and antiviral activity. J Virol 2011, 85:8197-8207.
• [44]Arias JF, Koyama T, Kinomoto M, Tokunaga K: Retroelements versus APOBEC3 family members: No great escape from the magnificent seven. Front Microbiol 2012, 3:275.
• [45]Newman EN, Holmes RK, Craig HM, Klein KC, Lingappa JR, Malim MH, Sheehy AM: Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol 2005, 15:166-170.
• [46]Bishop KN, Holmes RK, Malim MH: Antiviral potency of APOBEC proteins does not correlate with cytidine deamination. J Virol 2006, 80:8450-8458.
• [47]Iwatani Y, Chan DS, Wang F, Maynard KS, Sugiura W, Gronenborn AM, Rouzina I, Williams MC, Musier-Forsyth K, Levin JG: Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res 2007, 35:7096-7108.
• [48]Horn AV, Klawitter S, Held U, Berger A, Jaguva Vasudevan AA, Bock A, Hofmann H, Hanschmann KM, Trosemeier JH, Flory E, et al.: Human LINE-1 restriction by APOBEC3C is deaminase independent and mediated by an ORF1p interaction that affects LINE reverse transcriptase activity. Nucleic Acids Res 2013. in press
• [49]Chen H, Lilley CE, Yu Q, Lee DV, Chou J, Narvaiza I, Landau NR, Weitzman MD: APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr Biol 2006, 16:480-485.
• [50]Esnault C, Heidmann O, Delebecque F, Dewannieux M, Ribet D, Hance AJ, Heidmann T, Schwartz O: APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 2005, 433:430-433.
• [51]Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O’Shea KS, Moran JV, Cullen BR: Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci U S A 2006, 103:8780-8785.
• [52]Schumacher AJ, Nissley DV, Harris RS: APOBEC3G hypermutates genomic DNA and inhibits Ty1 retrotransposition in yeast. Proc Natl Acad Sci U S A 2005, 102:9854-9859.
• [53]Muckenfuss H, Hamdorf M, Held U, Perkovic M, Lower J, Cichutek K, Flory E, Schumann GG, Munk C: APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 2006, 281:22161-22172.
• [54]Kinomoto M, Kanno T, Shimura M, Ishizaka Y, Kojima A, Kurata T, Sata T, Tokunaga K: All APOBEC3 family proteins differentially inhibit LINE-1 retrotransposition. Nucleic Acids Res 2007, 35:2955-2964.
• [55]Ikeda T, Abd El Galil KH, Tokunaga K, Maeda K, Sata T, Sakaguchi N, Heidmann T, Koito A: Intrinsic restriction activity by apolipoprotein B mRNA editing enzyme APOBEC1 against the mobility of autonomous retrotransposons. Nucleic Acids Res 2011, 39:5538-5554.
• [56]MacDuff DA, Demorest ZL, Harris RS: AID can restrict L1 retrotransposition suggesting a dual role in innate and adaptive immunity. Nucleic Acids Res 2009, 37:1854-1867.
• [57]Zaranek AW, Levanon EY, Zecharia T, Clegg T, Church GM: A survey of genomic traces reveals a common sequencing error, RNA editing, and DNA editing. PLoS Genet 2010, 6:e1000954.
• [58]Carmi S, Church GM, Levanon EY: Large-scale DNA editing of retrotransposons accelerates mammalian genome evolution. Nat Commun 2011, 2:519.
• [59]Macduff DA, Harris RS: Directed DNA deamination by AID/APOBEC3 in immunity. Curr Biol 2006, 16:R186-189.
• [60]Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian HH Jr: High frequency retrotransposition in cultured mammalian cells. Cell 1996, 87:917-927.
• [61]Bogerd HP, Wiegand HL, Doehle BP, Lueders KK, Cullen BR: APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res 2006, 34:89-95.
• [62]Harris RS, Petersen-Mahrt SK, Neuberger MS: RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol Cell 2002, 10:1247-1253.
• [63]Petersen-Mahrt SK, Harris RS, Neuberger MS: AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 2002, 418:99-103.
• [64]Wang M, Rada C, Neuberger MS: A high-throughput assay for DNA deaminases. Methods Mol Biol 2011, 718:171-184.
• [65]Stenglein MD, Harris RS: APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J Biol Chem 2006, 281:16837-16841.
• [66]Niewiadomska AM, Tian C, Tan L, Wang T, Sarkis PT, Yu XF: Differential inhibition of long interspersed element 1 by APOBEC3 does not correlate with high-molecular-mass-complex formation or P-body association. J Virol 2007, 81:9577-9583.
• [67]Stenglein MD, Burns MB, Li M, Lengyel J, Harris RS: APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat Struct Mol Biol 2010, 17:222-229.
• [68]Narvaiza I, Linfesty DC, Greener BN, Hakata Y, Pintel DJ, Logue E, Landau NR, Weitzman MD: Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog 2009, 5:e1000439.
• [69]Bulliard Y, Narvaiza I, Bertero A, Peddi S, Rohrig UF, Ortiz M, Zoete V, Castro-Diaz N, Turelli P, Telenti A, et al.: Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities. J Virol 2011, 85:1765-1776.
• [70]Mitra M, Hercik K, Byeon IJ, Ahn J, Hill S, Hinchee-Rodriguez K, Singer D, Byeon CH, Charlton LM, Nam G, et al.: Structural determinants of human APOBEC3A enzymatic and nucleic acid binding properties. Nucleic Acids Res 2013. in press
• [71]Bogerd HP, Wiegand HL, Doehle BP, Cullen BR: The intrinsic antiretroviral factor APOBEC3B contains two enzymatically active cytidine deaminase domains. Virology 2007, 364:486-493.
• [72]Lee YN, Malim MH, Bieniasz PD: Hypermutation of an ancient human retrovirus by APOBEC3G. J Virol 2008, 82:8762-8770.
• [73]Esnault C, Priet S, Ribet D, Heidmann O, Heidmann T: 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 2008, 5:75. BioMed Central Full Text
• [74]Armitage AE, Katzourakis A, de Oliveira T, Welch JJ, Belshaw R, Bishop KN, Kramer B, McMichael AJ, Rambaut A, Iversen AK: Conserved footprints of APOBEC3G on Hypermutated human immunodeficiency virus type 1 and human endogenous retrovirus HERV-K(HML2) sequences. J Virol 2008, 82:8743-8761.
• [75]Kolosha VO, Martin SL: In vitro properties of the first ORF protein from mouse LINE-1 support its role in ribonucleoprotein particle formation during retrotransposition. Proc Natl Acad Sci U S A 1997, 94:10155-10160.
• [76]Nakamura M, Okada N, Kajikawa M: Self-interaction, nucleic acid binding, and nucleic acid chaperone activities are unexpectedly retained in the unique ORF1p of zebrafish LINE. Mol Cell Biol 2012, 32:458-469.
• [77]Liddament MT, Brown WL, Schumacher AJ, Harris RS: APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr Biol 2004, 14:1385-1391.
• [78]Dang Y, Wang X, Esselman WJ, Zheng YH: Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. J Virol 2006, 80:10522-10533.
• [79]Okeoma CM, Lovsin N, Peterlin BM, Ross SR: APOBEC3 inhibits mouse mammary tumour virus replication in vivo. Nature 2007, 445:927-930.
• [80]Zheng YH, Irwin D, Kurosu T, Tokunaga K, Sata T, Peterlin BM: Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication. J Virol 2004, 78:6073-6076.
• [81]Dang Y, Siew LM, Wang X, Han Y, Lampen R, Zheng YH: Human cytidine deaminase APOBEC3H restricts HIV-1 replication. J Biol Chem 2008, 283:11606-11614.
• [82]Rose PP, Korber BT: Detecting hypermutations in viral sequences with an emphasis on G – A hypermutation. Bioinformatics 2000, 16:400-401.
• [83]Kersting C, Tidow N, Schmidt H, Liedtke C, Neumann J, Boecker W, van Diest PJ, Brandt B, Buerger H: Gene dosage PCR and fluorescence in situ hybridization reveal low frequency of egfr amplifications despite protein overexpression in invasive breast carcinoma. Lab Invest 2004, 84:582-587.
• [84]Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F: Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002., 3RESEARCH0034
• [85]Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, Kent WJ: The UCSC Table Browser data retrieval tool. Nucleic Acids Res 2004, 32:D493-496.
• [86]Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J, et al.: Galaxy: a platform for interactive large-scale genome analysis. Genome Res 2005, 15:1451-1455.
• [87]Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J: Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol 2010, 11-21. Chapter 19:Unit 19 10
• [88]Goecks J, Nekrutenko A, Taylor J: Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010, 11:R86. BioMed Central Full Text
• [89]Karolchik D, Baertsch R, Diekhans M, Furey TS, Hinrichs A, Lu YT, Roskin KM, Schwartz M, Sugnet CW, Thomas DJ, et al.: The UCSC Genome Browser Database. Nucleic Acids Res 2003, 31:51-54.
• [90]Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J: Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 2005, 110:462-467.
• [91]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.