Selective silencing of euchromatic L1s revealed by genome-wide screens for L1 regulators

Nature

Volumn 553, Issue 7687, 2018, Pages 228-232

  Liu, Nian ^a   Lee, Cameron H ^a   Swigut, Tomek ^a   Grow, Edward ^a,b   Gu, Bo ^a   Bassik, Michael C ^a   Wysocka, Joanna ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; DNA; HISTONE; MORC2 PROTEIN; PROTEIN; RNA; UNCLASSIFIED DRUG; MORC2 PROTEIN, HUMAN; MPP8 PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; NUCLEAR PROTEIN; PHOSPHOPROTEIN; TASOR PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

CELL; COMPLEXITY; DISEASE; DNA; EVOLUTION; GENE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC VARIATION; GENOME; LIFE CYCLE; PROTEIN;

ARTICLE; DNA DAMAGE; DOWN REGULATION; EPIGENETICS; EUCHROMATIN; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; GENETIC CONSERVATION; GENETIC VARIABILITY; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HUMAN; INTRON; LIFE CYCLE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA PROCESSING; TRANSPOSON; ANIMAL; CRISPR CAS SYSTEM; EMBRYONIC STEM CELL; GENETIC TRANSCRIPTION; GENETICS; GENOMICS; HUMAN GENOME; K-562 CELL LINE; LONG INTERSPERSED REPEAT; MALE; METABOLISM; MOUSE; PROTEIN SUBUNIT; SILENCER ELEMENT;

ANIMALS; CRISPR-CAS SYSTEMS; EMBRYONIC STEM CELLS; EUCHROMATIN; GENE SILENCING; GENOME, HUMAN; GENOMICS; HUMANS; K562 CELLS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MICE; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTEIN SUBUNITS; SILENCER ELEMENTS, TRANSCRIPTIONAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 85040462484     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature25179     Document Type: Article

References (40)

1. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).
2. Levin, H. L. & Moran, J. V. Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12, 615-627 (2011).
3. Beck, C. R., Garcia-Perez, J. L., Badge, R. M. & Moran, J. V. LINE-1 elements in structural variation and disease. Annu. Rev. Genomics Hum. Genet. 12, 187-215 (2011).
4. Mita, P. & Boeke, J. D. How retrotransposons shape genome regulation. Curr. Opin. Genet. Dev. 37, 90-100 (2016).
5. Goodier, J. L. Restricting retrotransposons: A review. Mob. DNA 7, 16 (2016).
6. Chuong, E. B., Elde, N. C. & Feschotte, C. Regulatory activities of transposable elements: from conflicts to benefits. Nat. Rev. Genet. 18, 71-86 (2017).
7. Philippe, C. et al. Activation of individual L1 retrotransposon instances is restricted to cell-type dependent permissive loci. eLife 5, e13926 (2016).
8. Tchasovnikarova, I. A. et al. Epigenetic silencing by the HUSH complex mediates position-effect variegation in human cells. Science 348, 1481-1485 (2015).
9. Moran, J. V. et al. High frequency retrotransposition in cultured mammalian cells. Cell 87, 917-927 (1996).
10. Morgens, D. W. et al. Genome-scale measurement of off-target activity using Cas9 toxicity in high-throughput screens. Nat. Commun. 8, 15178 (2017).
11. Morgens, D. W., Deans, R. M., Li, A. & Bassik, M. C. Systematic comparison of CRISPR/Cas9 and RNAi screens for essential genes. Nat. Biotechnol. 34, 634-636 (2016).
12. Suzuki, J. et al. Genetic evidence that the non-homologous end-joining repair pathway is involved in LINE retrotransposition. PLoS Genet. 5, e1000461 (2009).
13. Chance, P. F. et al. Linkage of the gene for an autosomal dominant form of juvenile amyotrophic lateral sclerosis to chromosome 9q34. Am. J. Hum. Genet. 62, 633-640 (1998).
14. Németh, A. H. et al. Autosomal recessive cerebellar ataxia with oculomotor apraxia (ataxia-telangiectasia-like syndrome) is linked to chromosome 9q34. Am. J. Hum. Genet. 67, 1320-1326 (2000).
15. Albulym, O. M. et al. MORC2 mutations cause axonal Charcot-Marie-Tooth disease with pyramidal signs. Ann. Neurol. 79, 419-427 (2016).
16. Schottmann, G., Wagner, C., Seifert, F., Stenzel, W. & Schuelke, M. MORC2 mutation causes severe spinal muscular atrophy-phenotype, cerebellar atrophy, and diaphragmatic paralysis. Brain 139, 1-4 (2016).
17. Brégnard, C. et al. Upregulated LINE-1 activity in the Fanconi anemia cancer susceptibility syndrome leads to spontaneous pro-inflammatory cytokine production. EBioMedicine 8, 184-194 (2016).
18. Ostertag, E. M., Prak, E. T., DeBerardinis, R. J., Moran, J. V. & Kazazian, H. H. Jr. Determination of L1 retrotransposition kinetics in cultured cells. Nucleic Acids Res. 28, 1418-1423 (2000).
19. Han, J. S. & Boeke, J. D. A highly active synthetic mammalian retrotransposon. Nature 429, 314-318 (2004).
20. Wagstaff, B. J., Barnerssoi, M. & Roy-Engel, A. M. Evolutionary conservation of the functional modularity of primate and murine LINE-1 elements. PLoS ONE 6, e19672 (2011).
21. Tchasovnikarova, I. A. et al. Hyperactivation of HUSH complex function by Charcot-Marie-Tooth disease mutation in MORC2. Nat. Genet. 49, 1035-1044 (2017).
22. Moissiard, G. et al. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336, 1448-1451 (2012).
23. Pastor, W. A. et al. MORC1 represses transposable elements in the mouse male germline. Nat. Commun. 5, 5795 (2014).
24. Garcia-Perez, J. L. et al. LINE-1 retrotransposition in human embryonic stem cells. Hum. Mol. Genet. 16, 1569-1577 (2007).
25. Han, J. S., Szak, S. T. & Boeke, J. D. Transcriptional disruption by the L1 retrotransposon and implications for mammalian transcriptomes. Nature 429, 268-274 (2004).
26. Saint-André, V., Batsché, E., Rachez, C. & Muchardt, C. Histone H3 lysine 9 trimethylation and HP1 favor inclusion of alternative exons. Nat. Struct. Mol. Biol. 18, 337-344 (2011).
27. Khan, H., Smit, A. & Boissinot, S. Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. Genome Res. 16, 78-87 (2006).
28. Brouha, B. et al. Evidence consistent with human L1 retrotransposition in maternal meiosis I. Am. J. Hum. Genet. 71, 327-336 (2002).
29. Gasior, S. L., Roy-Engel, A. M. & Deininger, P. L. ERCC1/XPF limits L1 retrotransposition. DNA Repair (Amst.) 7, 983-989 (2008).
30. Deans, R. M. et al. Parallel shRNA and CRISPR-Cas9 screens enable antiviral drug target identification. Nat. Chem. Biol. 12, 361-366 (2016).
31. Bassik, M. C. et al. A systematic mammalian genetic interaction map reveals pathways underlying ricin susceptibility. Cell 152, 909-922 (2013).
32. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
33. Coufal, N. G. et al. L1 retrotransposition in human neural progenitor cells. Nature 460, 1127-1131 (2009).
34. Shukla, R. et al. Endogenous retrotransposition activates oncogenic pathways in hepatocellular carcinoma. Cell 153, 101-111 (2013).
35. Carreira, P. E. et al. Evidence for L1-associated DNA rearrangements and negligible L1 retrotransposition in glioblastoma multiforme. Mob. DNA 7, 21-34 (2016).
36. Doucet, A. J., Wilusz, J. E., Miyoshi, T., Liu, Y. & Moran, J. V. A. A 3 poly(A) tract is required for LINE-1 retrotransposition. Mol. Cell 60, 728-741 (2015).
37. Otsu, N. A threshold selection method from gray-level histograms. IEEE Trans. Syst. Man Cybern. 9, 62-66 (1979).
38. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
39. Bajpai, R. et al. CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463, 958-962 (2010).
40. Rada-Iglesias, A. et al. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470, 279-283 (2011).