Engineered LINE-1 retrotransposition in nondividing human neurons

Genome Research

Volumn 27, Issue 3, 2017, Pages 335-348

  MacIa, Angela ^a,f   Widmann, Thomas J ^a   Heras, Sara R ^a   Ayllon, Veronica ^b   Sanchez, Laura ^a   Benkaddour Boumzaouad, Meriem ^a   Muñoz Lopez, Martin ^a   Rubio, Alejandro ^a   Amador Cubero, Suyapa ^a   Blanco Jimenez, Eva ^a   Garcia Castro, Javier ^c   Menendez, Pablo ^b,d   Ng, Philip ^e   Muotri, Alysson R ^f   Goodier, John L ^g   Garcia Perez, Jose L ^a,h  

^a UNIVERSITY OF GRANADA   (Spain)

^b PTS Granada   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d JOSEP CARRERAS LEUKAEMIA RESEARCH INSTITUTE IJC   (Spain)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENETIC ENGINEERING; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LINE 1 GENE; MESENCHYMAL STEM CELL; MOSAICISM; NEURAL STEM CELL; PRIORITY JOURNAL; RETROPOSON; SOMATIC CELL; STEM CELL MOBILIZATION; CELL CULTURE; CELL DIVISION; CYTOLOGY; HELA CELL LINE; LONG INTERSPERSED REPEAT; MESENCHYMAL STROMA CELL; METABOLISM; TRANSPOSON;

CELL DIVISION; CELLS, CULTURED; DNA TRANSPOSABLE ELEMENTS; HELA CELLS; HEMATOPOIETIC STEM CELLS; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MESENCHYMAL STROMAL CELLS; MOSAICISM; NEURAL STEM CELLS;

EID: 85016477787     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.206805.116     Document Type: Article

References (79)

1. Aasen T, Raya A, Barrero MJ, Garreta E, Consiglio A, Gonzalez F, Vassena R, Bilić J, Pekarik V, Tiscornia G, et al. 2008. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 26: 1276-1284.
2. Alisch RS, Garcia-Perez JL, Muotri AR, Gage FH, Moran JV. 2006. Unconventional translation of mammalian LINE-1 retrotransposons. Genes Dev 20: 210-224.
3. Baillie JK, Barnett MW, Upton KR, Gerhardt DJ, Richmond TA, De Sapio F, Brennan PM, Rizzu P, Smith S, Fell M, et al. 2011. Somatic retrotransposition alters the genetic landscape of the human brain. Nature 479: 534-537.
4. Beck CR, Collier P, Macfarlane C, Malig M, Kidd JM, Eichler EE, Badge RM, Moran JV. 2010. LINE-1 retrotransposition activity in human genomes. Cell 141: 1159-1170.
5. 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.
6. 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.
7. Bestor TH. 2003. Cytosine methylation mediates sexual conflict. Trends Genet 19: 185-190.
8. Brouha B, Meischl C, Ostertag E, de Boer M, Zhang Y, Neijens H, Roos D, Kazazian HH Jr. 2002. Evidence consistent with human L1 retrotransposition in maternal meiosis I. Am J Hum Genet 71: 327-336.
9. Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV, Kazazian HH Jr. 2003. Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci 100: 5280-5285.
10. Carreira PE, Richardson SR, Faulkner GJ. 2013. L1 retrotransposons, cancer stem cells and oncogenesis. FEBS J 281: 63-73.
11. Chadwick K, Wang L, Li L, Menendez P, Murdoch B, Rouleau A, Bhatia M. 2003. Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102: 906-915.
12. Choi KD, Vodyanik M, Slukvin II. 2011. Hematopoietic differentiation and production of mature myeloid cells from human pluripotent stem cells. Nat Protoc 6: 296-313.
13. 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.
14. Coufal NG, Garcia-Perez JL, Peng GE, Marchetto MC, Muotri AR, Mu Y, Carson CT, Macia A, Moran JV, Gage FH. 2011. Ataxia telangiectasia mutated (ATM) modulates long interspersed element-1 (L1) retrotransposition in human neural stem cells. Nat Protoc 108: 20382-20387.
15. 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.
16. Del Re B, Marcantonio P, Capri M, Giorgi G. 2010. Evaluation of LINE-1 mobility in neuroblastoma cells by in vitro retrotransposition reporter assay: FACS analysis can detect only the tip of the iceberg of the inserted L1 elements. Exp Cell Res 316: 3358-3367.
17. Dmitriev SE, Andreev DE, Terenin IM, Olovnikov IA, Prassolov VS, Merrick WC, Shatsky IN. 2007. Efficient translation initiation directed by the 900-nucleotide-long and GC-rich 5' untranslated region of the human retrotransposon LINE-1 mRNA is strictly cap dependent rather than internal ribosome entry site mediated. Mol Cell Biol 27: 4685-4697.
18. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. 2006. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317.
19. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
20. Erwin JA, Paquola AC, Singer T, Gallina I, Novotny M, Quayle C, Bedrosian TA, Alves FI, Butcher CR, Herdy JR, et al. 2016. L1-associated genomic regions are deleted in somatic cells of the healthy human brain. Nat Neurosci 19: 1583-1591.
21. Evrony GD, Cai X, Lee E, Hills LB, Elhosary PC, Lehmann HS, Parker JJ, Atabay KD, Gilmore EC, Poduri A, et al. 2012. Single-neuron sequencing analysis of L1 retrotransposition and somatic mutation in the human brain. Cell 151: 483-496.
22. Ewing AD, Gacita A, Wood LD, Ma F, Xing D, Kim MS, Manda SS, Abril G, Pereira G, Makohon-Moore A, et al. 2015. Widespread somatic L1 retrotransposition occurs early during gastrointestinal cancer evolution. Genome Res 25: 1536-1545.
23. Faulkner GJ, Kimura Y, Daub CO, Wani S, Plessy C, Irvine KM, Schroder K, Cloonan N, Steptoe AL, Lassmann T, et al. 2009. The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41: 563-571.
24. Feng Q, Moran JV, Kazazian HH Jr, Boeke JD. 1996. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87: 905-916.
25. Fritschy JM, Brandner S, Aguzzi A, Koedood M, Luscher B, Mitchell PJ. 1996. Brain cell type specificity and gliosis-induced activation of the human cytomegalovirus immediate-early promoter in transgenic mice. J Neurosci 16: 2275-2282.
26. Fuchs E. 2007. Scratching the surface of skin development. Nature 445: 834-842.
27. Garcia-Perez JL, Marchetto MC, Muotri AR, Coufal NG, Gage FH, O'Shea KS, Moran JV. 2007. LINE-1 retrotransposition in human embryonic stem cells. Hum Mol Genet 16: 1569-1577.
28. Garcia-Perez JL, Morell M, Scheys JO, Kulpa DA, Morell S, Carter CC, Hammer GD, Collins KL, O'Shea KS, Menendez P, et al. 2010. Epigenetic silencing of engineered L1 retrotransposition events in human embryonic carcinoma cells. Nature 466: 769-773.
29. Giorgi G, Marcantonio P, Del Re B. 2011. LINE-1 retrotransposition in human neuroblastoma cells is affected by oxidative stress. Cell Tissue Res 346: 383-391.
30. Goodier JL. 2016. Restricting retrotransposons: a review. Mobile DNA 7: 16.
31. 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.
32. Griesi-Oliveira K, Acab A, Gupta AR, Sunaga DY, Chailangkarn T, Nicol X, Nunez Y, Walker MF, Murdoch JD, Sanders SJ, et al. 2015. Modeling non-syndromic autism and the impact of TRPC6 disruption in human neurons. Mol Psychiatry 20: 1350-1365.
33. Hancks DC, Kazazian HH Jr. 2012. Active human retrotransposons: variation and disease. Curr Opin Genet Dev 22: 191-203.
34. Hohjoh H, Singer MF. 1996. Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J 15: 630-639.
35. Hohjoh H, Singer MF. 1997. Sequence-specific single-strand RNA binding protein encoded by the human LINE-1 retrotransposon. EMBO J 16: 6034-6043.
36. International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.
37. Isern J, Martín-Antonio B, Ghazanfari R, Martín AM, López JA, del Toro R, Sánchez-Aguilera A, Arranz L, Martín-Pérez D, Suárez-Lledó M, et al. 2013. Self-renewing human bone marrow mesenspheres promote hematopoietic stem cell expansion. Cell Rep 3: 1714-1724.
38. Ji J, Vijayaragavan K, Bosse M, Menendez P, Weisel K, Bhatia M. 2008. OP9 stroma augments survival of hematopoietic precursors and progenitors during hematopoietic differentiation from human embryonic stem cells. Stem Cells 26: 2485-2495.
39. Kano H, Godoy I, Courtney C, Vetter MR, Gerton GL, Ostertag EM, Kazazian HH Jr. 2009. L1 retrotransposition occurs mainly in embryogenesis and creates somatic mosaicism. Genes Dev 23: 1303-1312.
40. Khazina E, Weichenrieder O. 2009. Non-LTR retrotransposons encode noncanonical RRM domains in their first open reading frame. Proc Natl Acad Sci 106: 731-736.
41. Kimberland ML, Divoky V, Prchal J, Schwahn U, BergerW, Kazazian HH Jr. 1999. Full-length human L1 insertions retain the capacity for high frequency retrotransposition in cultured cells. Hum Mol Genet 8: 1557-1560.
42. Klawitter S, Fuchs NV, Upton KR, Muñoz-Lopez M, Shukla R, Wang J, Garcia-Cañadas M, Lopez-Ruiz C, Gerhardt DJ, Sebe A, et al. 2016. Reprogramming triggers endogenous L1 and Alu retrotransposition in human induced pluripotent stem cells. Nat Commun 7: 10286.
43. Kubo S, Seleme MC, Soifer HS, Perez JL, Moran JV, Kazazian HH Jr, Kasahara N. 2006. L1 retrotransposition in nondividing and primary human somatic cells. Proc Natl Acad Sci 103: 8036-8041.
44. 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.
45. 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.
46. Mathias SL, Scott AF, Kazazian HH Jr, Boeke JD, Gabriel A. 1991. Reverse transcriptase encoded by a human transposable element. Science 254: 1808-1810.
47. Mills RE, Bennett EA, Iskow RC, Devine SE. 2007. Which transposable elements are active in the human genome? Trends Genet 23: 183-191.
48. Moldovan JB, Moran JV. 2015. The zinc-finger antiviral protein ZAP inhibits LINE and alu retrotransposition. PLoS Genet 11: e1005121.
49. Montes R, Ayllón V, Gutierrez-Aranda I, Prat I, Hernández-Lamas MC, Ponce L, Bresolin S, Te Kronnie G, Greaves M, Bueno C, et al. 2011. Enforced expression of MLL-AF4 fusion in cord blood CD34+ cells enhances the hematopoietic repopulating cell function and clonogenic potential but is not sufficient to initiate leukemia. Blood 117: 4746-4758.
50. Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian HH Jr. 1996. High frequency retrotransposition in cultured mammalian cells. Cell 87: 917-927.
51. Muñoz-Lopez M, Garcia-Cañadas M, Macia A, Morell S, Garcia-Perez JL. 2012. Analysis of LINE-1 expression in human pluripotent cells. Methods Mol Biol 873: 113-125.
52. Muotri AR, Chu VT, Marchetto MC, Deng W, Moran JV, Gage FH. 2005. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435: 903-910.
53. Muotri AR, Marchetto MC, Coufal NG, Oefner R, Yeo G, Nakashima K, Gage FH. 2010. L1 retrotransposition in neurons is modulated by MeCP2. Nature 468: 443-446.
54. 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.
55. Palmer DJ, Ng P. 2008. Methods for the production of helper-dependent adenoviral vectors. Methods Mol Biol 433: 33-53.
56. Rapaport F, Khanin R, Liang Y, Pirun M, Krek A, Zumbo P, Mason CE, Socci ND, Betel D. 2013. Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data. Genome Biol 14: R95.
57. Raya A, Rodríguez-Pizà I, Guenechea G, Vassena R, Navarro S, Barrero MJ, Consiglio A, Castellà M, Río P, Sleep E, et al. 2009. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 460: 53-59.
58. Richardson SR, Morell S, Faulkner GJ. 2014a. L1 retrotransposons and somatic mosaicism in the brain. Annu Rev Genet 48: 1-27.
59. Richardson SR, Narvaiza I, Planegger RA, Weitzman MD, Moran JV. 2014b. APOBEC3A deaminates transiently exposed single-strand DNA during LINE-1 retrotransposition. eLife 3: e02008.
60. 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: MDNA3-0061-2014.
61. Sánchez L, Gutierrez-Aranda I, Ligero G, Rubio R, Muñoz-López M, García-Pérez JL, Ramos V, Real PJ, Bueno C, Rodríguez R, et al. 2011. Enrichment of human ESC-derived multipotent mesenchymal stem cells with immunosuppressive and anti-inflammatory properties capable to protect against experimental inflammatory bowel disease. Stem Cells 29: 251-262.
62. Sassaman DM, Dombroski BA, Moran JV, Kimberland ML, Naas TP, DeBerardinis RJ,Gabriel A, SwergoldGD,KazazianHHJr.1997.Manyhuman L1 elements are capable of retrotransposition. Nat Genet 16: 37-43.
63. Singer T, McConnell MJ, Marchetto MC, Coufal NG, Gage FH. 2010. LINE-1 retrotransposons: mediators of somatic variation in neuronal genomes? Trends Neurosci 33: 345-354.
64. Soifer H, Higo C, Kazazian HH Jr, Moran JV, Mitani K, Kasahara N. 2001. Stable integration of transgenes delivered by a retrotransposon-adenovirus hybrid vector. Hum Gene Ther 12: 1417-1428.
65. Swergold GD. 1990. Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol Cell Biol 10: 6718-6729.
66. Tang Y, Nyengaard JR, De Groot DM, Gundersen HJ. 2001. Total regional and global number of synapses in the human brain neocortex. Synapse 41: 258-273.
67. Taylor MS, Lacava J, Mita P, Molloy KR, Huang CR, Li D, Adney EM, Jiang H, Burns KH, Chait BT, et al. 2013. Affinity proteomics reveals human host factors implicated in discrete stages of LINE-1 retrotransposition. Cell 155: 1034-1048.
68. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
69. Upton KR, Gerhardt DJ, Jesuadian JS, Richardson SR, Sánchez-Luque FJ, Bodea GO, Ewing AD, Salvador-Palomeque C, van der Knaap MS, Brennan PM, et al. 2015. Ubiquitous L1 mosaicism in hippocampal neurons. Cell 161: 228-239.
70. van den Hurk JA, Meij IC, Seleme MC, Kano H, Nikopoulos K, Hoefsloot LH, Sistermans EA, de Wijs IJ, Mukhopadhyay A, Plomp AS, et al. 2007. L1 retrotransposition can occur early in human embryonic development. Hum Mol Genet 16: 1587-1592.
71. van den Pol AN, Ghosh PK. 1998. Selective neuronal expression of green fluorescent protein with cytomegalovirus promoter reveals entire neuronal arbor in transgenic mice. J Neurosci 18: 10640-10651.
72. Villa-Diaz LG, Garcia-Perez JL, Krebsbach PH. 2010. Enhanced transfection efficiency of human embryonic stem cells by the incorporation of DNA liposomes in extracellular matrix. Stem Cells Dev 19: 1949-1957.
73. Vodyanik MA, Slukvin II. 2007. Hematoendothelial differentiation of human embryonic stem cells. Curr Protoc Cell Biol Chapter 23: Unit 23 26.
74. Wang L. 2006. Endothelial and hematopoietic cell fate of human embryonic stem cells. Trends Cardiovasc Med 16: 89-94.
75. Wang L, Cerdan C, Menendez P, Bhatia M. 2006. Derivation and characterization of hematopoietic cells from human embryonic stem cells. Methods Mol Biol 331: 179-200.
76. WeiW, Morrish TA, Alisch RS, Moran JV. 2000. A transient assay reveals that cultured human cells can accommodate multiple LINE-1 retrotransposition events. Anal Biochem 284: 435-438.
77. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, Kazazian HH, Boeke JD, Moran JV. 2001. Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol 21: 1429-1439.
78. 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.
79. Wissing S, Muñoz-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.