SAMHD1 Inhibits LINE-1 Retrotransposition by Promoting Stress Granule Formation

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Long interspersed element 1 (LINE-1 or L1) comprises 17% of human genome, and has played a major role in shaping the evolution of human genome. Approximately 100 copies of LINE-1 are still active in an average individual genome. Movement of these LINE-1 sequences to new loci in the genome has the potential of causing sporadic cases of disease. Among the multi-layered mechanisms by which the host controls LINE-1 activity is a group of host restriction factors including APOBEC3 proteins. SAMHD1 was known for the association of its mutations with the Aicardi-Goutieres syndrome (AGS), a congenital autoimmune disease. SAMHD1 was recently reported as a host restriction factor that inhibits a number of retroviruses and DNA viruses including human immunodeficiency virus type 1 (HIV-1) and herpes simplex virus 1 (HSV-1). Here, we demonstrate that SAMHD1 inhibits LINE-1 retrotransposition through promoting the sequestration of LINE-1 RNP within the cytoplasmic stress granules. SAMHD1 promotes the formation of large stress granules by inducing phosphorylation of eIF2α and disrupting eIF4A/eIF4G interaction. This is the first report describing the role of SAMHD1 in modulating the formation of stress granules. We envision that this function of SAMHD1 not only contributes to the inhibition of LINE-1, but also the restriction of various viruses.

Vyšlo v časopise: SAMHD1 Inhibits LINE-1 Retrotransposition by Promoting Stress Granule Formation. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005367
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005367

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1. Li N, Zhang W, Cao X (2000) Identification of human homologue of mouse IFN-gamma induced protein from human dendritic cells. Immunology letters 74: 221–224. 11064105

2. Rice GI, Bond J, Asipu A, Brunette RL, Manfield IW, et al. (2009) Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat Genet 41: 829–832. doi: 10.1038/ng.373 19525956

3. Fazzi E, Cattalini M, Orcesi S, Tincani A, Andreoli L, et al. (2012) Aicardi-Goutieres syndrome, a rare neurological disease in children: a new autoimmune disorder? Autoimmun Rev 12: 506–509. doi: 10.1016/j.autrev.2012.08.012 22940555

4. Goldstone DC, Ennis-Adeniran V, Hedden JJ, Groom HC, Rice GI, et al. (2011) HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480: 379–382. doi: 10.1038/nature10623 22056990

5. Powell RD, Holland PJ, Hollis T, Perrino FW (2011) Aicardi-Goutieres syndrome gene and HIV-1 restriction factor SAMHD1 is a dGTP-regulated deoxynucleotide triphosphohydrolase. J Biol Chem 286: 43596–43600. doi: 10.1074/jbc.C111.317628 22069334

6. Gramberg T, Kahle T, Bloch N, Wittmann S, Mullers E, et al. (2013) Restriction of diverse retroviruses by SAMHD1. Retrovirology 10: 26. doi: 10.1186/1742-4690-10-26 23497255

7. Kim ET, White TE, Brandariz-Nunez A, Diaz-Griffero F, Weitzman MD (2013) SAMHD1 restricts herpes simplex virus 1 in macrophages by limiting DNA replication. J Virol 87: 12949–12956. doi: 10.1128/JVI.02291-13 24067963

8. Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, 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. doi: 10.1038/ni.2236 22327569

9. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, et al. (2011) Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474: 658–661. doi: 10.1038/nature10195 21720370

10. Brandariz-Nunez A, Valle-Casuso JC, White TE, Laguette N, Benkirane M, et al. (2012) Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac. Retrovirology 9: 49. doi: 10.1186/1742-4690-9-49 22691373

11. Hofmann H, Logue EC, Bloch N, Daddacha W, Polsky SB, et al. (2012) The Vpx lentiviral accessory protein targets SAMHD1 for degradation in the nucleus. J Virol 86: 12552–12560. doi: 10.1128/JVI.01657-12 22973040

12. Goujon C, Arfi V, Pertel T, Luban J, Lienard J, et al. (2008) Characterization of simian immunodeficiency virus SIVSM/human immunodeficiency virus type 2 Vpx function in human myeloid cells. J Virol 82: 12335–12345. doi: 10.1128/JVI.01181-08 18829761

13. Goujon C, Riviere L, Jarrosson-Wuilleme L, Bernaud J, Rigal D, et al. (2007) SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells. Retrovirology 4: 2. 17212817

14. Kaushik R, Zhu X, Stranska R, Wu Y, Stevenson M (2009) A cellular restriction dictates the permissivity of nondividing monocytes/macrophages to lentivirus and gammaretrovirus infection. Cell Host Microbe 6: 68–80. doi: 10.1016/j.chom.2009.05.022 19616766

15. Laguette N, Rahm N, Sobhian B, Chable-Bessia C, Munch J, 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. doi: 10.1016/j.chom.2012.01.007 22305291

16. Sharova N, Wu Y, Zhu X, Stranska R, Kaushik R, et al. (2008) Primate lentiviral Vpx commandeers DDB1 to counteract a macrophage restriction. PLoS Pathog 4: e1000057. doi: 10.1371/journal.ppat.1000057 18451984

17. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, et al. (2011) SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474: 654–657. doi: 10.1038/nature10117 21613998

18. Baldauf HM, Pan X, Erikson E, Schmidt S, Daddacha W, et al. (2012) SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat Med 18: 1682–1687. doi: 10.1038/nm.2964 22972397

19. Descours B, Cribier A, Chable-Bessia C, Ayinde D, Rice G, et al. (2012) SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells. Retrovirology 9: 87. doi: 10.1186/1742-4690-9-87 23092122

20. White TE, Brandariz-Nunez A, Valle-Casuso JC, Amie S, Nguyen LA, et al. (2013) The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe 13: 441–451. doi: 10.1016/j.chom.2013.03.005 23601106

21. Cribier A, Descours B, Valadao AL, Laguette N, Benkirane M (2013) Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep 3: 1036–1043. doi: 10.1016/j.celrep.2013.03.017 23602554

22. Koseoglu MM, Dong J, Marzluff WF (2010) Coordinate regulation of histone mRNA metabolism and DNA replication: cyclin A/cdk1 is involved in inactivation of histone mRNA metabolism and DNA replication at the end of S phase. Cell Cycle 9: 3857–3863. 20935461

23. Hass R, Gunji H, Datta R, Kharbanda S, Hartmann A, et al. (1992) Differentiation and retrodifferentiation of human myeloid leukemia cells is associated with reversible induction of cell cycle-regulatory genes. Cancer Res 52: 1445–1450. 1531783

24. Kim MO, Moon DO, Choi YH, Lee JD, Kim ND, et al. (2008) Platycodin D induces mitotic arrest in vitro, leading to endoreduplication, inhibition of proliferation and apoptosis in leukemia cells. Int J Cancer 122: 2674–2681. doi: 10.1002/ijc.23442 18351645

25. Traore K, Trush MA, George M Jr., Spannhake EW, Anderson W, et al. (2005) Signal transduction of phorbol 12-myristate 13-acetate (PMA)-induced growth inhibition of human monocytic leukemia THP-1 cells is reactive oxygen dependent. Leuk Res 29: 863–879. 15978937

26. Welbourn S, Dutta SM, Semmes OJ, Strebel K (2013) Restriction of virus infection but not catalytic dNTPase activity is regulated by phosphorylation of SAMHD1. J Virol 87: 11516–11524. doi: 10.1128/JVI.01642-13 23966382

27. Zhao K, Du J, Han X, Goodier JL, Li P, et al. (2013) Modulation of LINE-1 and Alu/SVA retrotransposition by Aicardi-Goutieres syndrome-related SAMHD1. Cell Rep 4: 1108–1115. doi: 10.1016/j.celrep.2013.08.019 24035396

28. 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. doi: 10.1146/annurev-genom-082509-141802 21801021

29. Martin SL (1991) Ribonucleoprotein particles with LINE-1 RNA in mouse embryonal carcinoma cells. Mol Cell Biol 11: 4804–4807. 1715025

30. Holmes SE, Singer MF, Swergold GD (1992) 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 267: 19765–19768. 1328181

31. Martin SL, Branciforte D, Keller D, Bain DL (2003) Trimeric structure for an essential protein in L1 retrotransposition. Proc Natl Acad Sci U S A 100: 13815–13820. 14615577

32. Hohjoh H, Singer MF (1996) Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J 15: 630–639. 8599946

33. Mathias SL, Scott AF, Kazazian HH Jr., Boeke JD, Gabriel A (1991) Reverse transcriptase encoded by a human transposable element. Science 254: 1808–1810. 1722352

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. 8945517

35. Kulpa DA, Moran JV (2006) Cis-preferential LINE-1 reverse transcriptase activity in ribonucleoprotein particles. Nat Struct Mol Biol 13: 655–660. 16783376

36. Doucet AJ, Hulme AE, Sahinovic E, Kulpa DA, Moldovan JB, et al. (2010) Characterization of LINE-1 ribonucleoprotein particles. PLoS Genet 6.

37. Goodier JL, Mandal PK, Zhang L, Kazazian HH Jr. (2010) Discrete subcellular partitioning of human retrotransposon RNAs despite a common mechanism of genome insertion. Hum Mol Genet 19: 1712–1725. doi: 10.1093/hmg/ddq048 20147320

38. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, et al. (2001) Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol 21: 1429–1439. 11158327

39. Kulpa DA, Moran JV (2005) Ribonucleoprotein particle formation is necessary but not sufficient for LINE-1 retrotransposition. Hum Mol Genet 14: 3237–3248. 16183655

40. Cost GJ, Feng Q, Jacquier A, Boeke JD (2002) Human L1 element target-primed reverse transcription in vitro. EMBO J 21: 5899–5910. 12411507

41. Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72: 595–605. 7679954

42. Matsuki H, Takahashi M, Higuchi M, Makokha GN, Oie M, et al. (2012) Both G3BP1 and G3BP2 contribute to stress granule formation. Genes Cells 18: 135–146. doi: 10.1111/gtc.12023 23279204

43. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, et al. (2004) Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15: 5383–5398. 15371533

44. Esnault C, Maestre J, Heidmann T (2000) Human LINE retrotransposons generate processed pseudogenes. Nat Genet 24: 363–367. 10742098

45. Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, et al. (1996) High frequency retrotransposition in cultured mammalian cells. Cell 87: 917–927. 8945518

46. Esnault C, Millet J, Schwartz O, Heidmann T (2006) Dual inhibitory effects of APOBEC family proteins on retrotransposition of mammalian endogenous retroviruses. Nucleic Acids Res 34: 1522–1531. 16537839

47. Martin SL, Branciforte D (1993) Synchronous expression of LINE-1 RNA and protein in mouse embryonal carcinoma cells. Mol Cell Biol 13: 5383–5392. 8395003

48. Ortyn WE, Hall BE, George TC, Frost K, Basiji DA, et al. (2006) Sensitivity measurement and compensation in spectral imaging. Cytometry A 69: 852–862. 16969805

49. Goodier JL, Zhang L, Vetter MR, Kazazian HH Jr. (2007) LINE-1 ORF1 protein localizes in stress granules with other RNA-binding proteins, including components of RNA interference RNA-induced silencing complex. Mol Cell Biol 27: 6469–6483. 17562864

50. Belancio VP, Roy-Engel AM, Pochampally RR, Deininger P (2010) Somatic expression of LINE-1 elements in human tissues. Nucleic Acids Res 38: 3909–3922. doi: 10.1093/nar/gkq132 20215437

51. Belancio VP, Hedges DJ, Deininger P (2006) LINE-1 RNA splicing and influences on mammalian gene expression. Nucleic Acids Res 34: 1512–1521. 16554555

52. Goodier JL, Cheung LE, Kazazian HH Jr. (2013) Mapping the LINE1 ORF1 protein interactome reveals associated inhibitors of human retrotransposition. Nucleic Acids Res 41: 7401–7419. doi: 10.1093/nar/gkt512 23749060

53. Tourriere H, Chebli K, Zekri L, Courselaud B, Blanchard JM, et al. (2003) The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160: 823–831. 12642610

54. Kedersha NL, Gupta M, Li W, Miller I, Anderson P (1999) RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol 147: 1431–1442. 10613902

55. McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, et al. (2005) Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J Biol Chem 280: 16925–16933. 15684421

56. Reineke LC, Dougherty JD, Pierre P, Lloyd RE Large G3BP-induced granules trigger eIF2alpha phosphorylation. Mol Biol Cell 23: 3499–3510. doi: 10.1091/mbc.E12-05-0385 22833567

57. Gingras AC, Raught B, Sonenberg N (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913–963. 10872469

58. Zhu Y, Wang X, Goff SP, Gao G (2012) Translational repression precedes and is required for ZAP-mediated mRNA decay. EMBO J 31: 4236–4246. doi: 10.1038/emboj.2012.271 23023399

59. Kato Y, Kaneda M, Hata K, Kumaki K, Hisano M, et al. (2007) Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum Mol Genet 16: 2272–2280. 17616512

60. Bourc'his D, Bestor TH (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431: 96–99. 15318244

61. Walsh CP, Chaillet JR, Bestor TH (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 20: 116–117. 9771701

62. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, et al. (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12: 503–514. 17395546

63. Aravin AA, Hannon GJ, Brennecke J (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761–764. 17975059

64. Niewiadomska AM, Tian C, Tan L, Wang T, Sarkis PT, et al. (2007) Differential inhibition of long interspersed element 1 by APOBEC3 does not correlate with high-molecular-mass-complex formation or P-body association. J Virol 81: 9577–9583. 17582006

65. Wissing S, Montano M, Garcia-Perez JL, Moran JV, Greene WC (2011) Endogenous APOBEC3B restricts LINE-1 retrotransposition in transformed cells and human embryonic stem cells. J Biol Chem 286: 36427–36437. doi: 10.1074/jbc.M111.251058 21878639

66. 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. doi: 10.7554/eLife.02008 24843014

67. Chen H, Lilley CE, Yu Q, Lee DV, Chou J, et al. (2006) APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr Biol 16: 480–485. 16527742

68. Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, et al. (2006) Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci U S A 103: 8780–8785. 16728505

69. Arjan-Odedra S, Swanson CM, Sherer NM, Wolinsky SM, Malim MH (2012) Endogenous MOV10 inhibits the retrotransposition of endogenous retroelements but not the replication of exogenous retroviruses. Retrovirology 9: 53. doi: 10.1186/1742-4690-9-53 22727223

70. Goodier JL, Cheung LE, Kazazian HH Jr. (2012) MOV10 RNA helicase is a potent inhibitor of retrotransposition in cells. PLoS Genet 8: e1002941. doi: 10.1371/journal.pgen.1002941 23093941

71. Li X, Zhang J, Jia R, Cheng V, Xu X, et al. (2013) The MOV10 helicase inhibits LINE-1 mobility. J Biol Chem 288: 21148–21160. doi: 10.1074/jbc.M113.465856 23754279

72. Goodier JL, Pereira GC, Cheung LE, Rose RJ, Kazazian HH Jr. (2015) The Broad-Spectrum Antiviral Protein ZAP Restricts Human Retrotransposition. PLoS Genet 11: e1005252. doi: 10.1371/journal.pgen.1005252 26001115

73. Moldovan JB, Moran JV (2015) The Zinc-Finger Antiviral Protein ZAP Inhibits LINE and Alu Retrotransposition. PLoS Genet 11: e1005121. doi: 10.1371/journal.pgen.1005121 25951186

74. 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. 10684937

75. Reineke LC, Lloyd RE (2013) Diversion of stress granules and P-bodies during viral infection. Virology 436: 255–267. doi: 10.1016/j.virol.2012.11.017 23290869

76. Valiente-Echeverria F, Melnychuk L, Vyboh K, Ajamian L, Gallouzi IE, et al. (2014) eEF2 and Ras-GAP SH3 domain-binding protein (G3BP1) modulate stress granule assembly during HIV-1 infection. Nat Commun 5: 4819. doi: 10.1038/ncomms5819 25229650

77. Ng CS, Jogi M, Yoo JS, Onomoto K, Koike S, et al. (2013) Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. J Virol 87: 9511–9522. doi: 10.1128/JVI.03248-12 23785203

78. Dombroski BA, Mathias SL, Nanthakumar E, Scott AF, Kazazian HH Jr. (1991) Isolation of an active human transposable element. Science 254: 1805–1808. 1662412

79. Dewannieux M, Dupressoir A, Harper F, Pierron G, Heidmann T (2004) Identification of autonomous IAP LTR retrotransposons mobile in mammalian cells. Nat Genet 36: 534–539. 15107856

80. Graf Einsiedel H, Taube T, Hartmann R, Wellmann S, Seifert G, et al. (2002) Deletion analysis of p16(INKa) and p15(INKb) in relapsed childhood acute lymphoblastic leukemia. Blood 99: 4629–4631. 12036898

81. Piao X, Cai P, Liu S, Hou N, Hao L, et al. (2011) Global expression analysis revealed novel gender-specific gene expression features in the blood fluke parasite Schistosoma japonicum. PLoS One 6: e18267. doi: 10.1371/journal.pone.0018267 21494327

82. Nobile C, Rudnicka D, Hasan M, Aulner N, Porrot F, et al. (2010) HIV-1 Nef inhibits ruffles, induces filopodia, and modulates migration of infected lymphocytes. J Virol 84: 2282–2293. doi: 10.1128/JVI.02230-09 20015995