Intercellular viral spread and intracellular transposition of Drosophila gypsy
Autoři:
Richard M. Keegan aff001; Lillian R. Talbot aff002; Yung-Heng Chang aff003; Michael J. Metzger aff004; Josh Dubnau aff001
Působiště autorů:
Program in Neuroscience, Department of Neurobiology and Behavior, Stony Brook University, New York City, New York, United States of America
aff001; Medical Scientist Training Program, Department of Neurobiology and Behavior, Stony Brook University, New York City, New York, United States of America
aff002; Department of Anesthesiology, Stony Brook School of Medicine, New York City, New York, United States of America
aff003; Pacific Northwest Research Institute, Seattle, Washington, United States of America
aff004
Vyšlo v časopise:
Intercellular viral spread and intracellular transposition of Drosophila gypsy. PLoS Genet 17(4): e1009535. doi:10.1371/journal.pgen.1009535
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009535
Souhrn
It has become increasingly clear that retrotransposons (RTEs) are more widely expressed in somatic tissues than previously appreciated. RTE expression has been implicated in a myriad of biological processes ranging from normal development and aging, to age related diseases such as cancer and neurodegeneration. Long Terminal Repeat (LTR)-RTEs are evolutionary ancestors to, and share many features with, exogenous retroviruses. In fact, many organisms contain endogenous retroviruses (ERVs) derived from exogenous retroviruses that integrated into the germ line. These ERVs are inherited in Mendelian fashion like RTEs, and some retain the ability to transmit between cells like viruses, while others develop the ability to act as RTEs. The process of evolutionary transition between LTR-RTE and retroviruses is thought to involve multiple steps by which the element loses or gains the ability to transmit copies between cells versus the ability to replicate intracellularly. But, typically, these two modes of transmission are incompatible because they require assembly in different sub-cellular compartments. Like murine IAP/IAP-E elements, the gypsy family of retroelements in arthropods appear to sit along this evolutionary transition. Indeed, there is some evidence that gypsy may exhibit retroviral properties. Given that gypsy elements have been found to actively mobilize in neurons and glial cells during normal aging and in models of neurodegeneration, this raises the question of whether gypsy replication in somatic cells occurs via intracellular retrotransposition, intercellular viral spread, or some combination of the two. These modes of replication in somatic tissues would have quite different biological implications. Here, we demonstrate that Drosophila gypsy is capable of both cell-associated and cell-free viral transmission between cultured S2 cells of somatic origin. Further, we demonstrate that the ability of gypsy to move between cells is dependent upon a functional copy of its viral envelope protein. This argues that the gypsy element has transitioned from an RTE into a functional endogenous retrovirus with the acquisition of its envelope gene. On the other hand, we also find that intracellular retrotransposition of the same genomic copy of gypsy can occur in the absence of the Env protein. Thus, gypsy exhibits both intracellular retrotransposition and intercellular viral transmission as modes of replicating its genome.
Klíčová slova:
Drosophila melanogaster – Fluorescence imaging – Invertebrate genomics – Polymerase chain reaction – Retroviruses – Romani people – Transfection – Viral replication
Zdroje
1. Huang CR, Burns KH, Boeke JD. Active transposition in genomes. Annu Rev Genet. 2012;46:651–75. doi: 10.1146/annurev-genet-110711-155616 23145912
2. Kazazian HH Jr. Mobile elements: drivers of genome evolution. Science. 2004;303(5664):1626–32. doi: 10.1126/science.1089670 15016989
3. Babushok DV, Kazazian HH Jr. Progress in understanding the biology of the human mutagen LINE-1. Hum Mutat. 2007;28(6):527–39. doi: 10.1002/humu.20486 17309057
4. Dubnau J. The Retrotransposon storm and the dangers of a Collyer’s genome. Curr Opin Genet Dev. 2018;49:95–105. doi: 10.1016/j.gde.2018.04.004 29705598
5. Faulkner GJ, Billon V. L1 retrotransposition in the soma: a field jumping ahead. Mob DNA. 2018;9:22. doi: 10.1186/s13100-018-0128-1 30002735
6. Reilly MT, Faulkner GJ, Dubnau J, Ponomarev I, Gage FH. The role of transposable elements in health and diseases of the central nervous system. J Neurosci. 2013;33(45):17577–86. doi: 10.1523/JNEUROSCI.3369-13.2013 24198348
7. Richardson SR, Morell S, Faulkner GJ. L1 retrotransposons and somatic mosaicism in the brain. Annu Rev Genet. 2014;48:1–27. doi: 10.1146/annurev-genet-120213-092412 25036377
8. Baillie JK, Barnett MW, Upton KR, Gerhardt DJ, Richmond TA, De Sapio F, et al. Somatic retrotransposition alters the genetic landscape of the human brain. Nature. 2011;479(7374):534–7. doi: 10.1038/nature10531 22037309
9. Burns KH. Transposable elements in cancer. Nat Rev Cancer. 2017;17(7):415–24. doi: 10.1038/nrc.2017.35 28642606
10. Chang YH, Dubnau J. The Gypsy Endogenous Retrovirus Drives Non-Cell-Autonomous Propagation in a Drosophila TDP-43 Model of Neurodegeneration. Curr Biol. 2019;29(19):3135–52 e4. doi: 10.1016/j.cub.2019.07.071 31495585
11. Chang YH, Keegan RM, Prazak L, Dubnau J. Cellular labeling of endogenous retrovirus replication (CLEVR) reveals de novo insertions of the gypsy retrotransposable element in cell culture and in both neurons and glial cells of aging fruit flies. PLoS Biol. 2019;17(5):e3000278. doi: 10.1371/journal.pbio.3000278 31095565
12. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, et al. L1 retrotransposition in human neural progenitor cells. Nature. 2009;460(7259):1127–31. doi: 10.1038/nature08248 19657334
13. Eickbush MT, Eickbush TH. Retrotransposition of R2 elements in somatic nuclei during the early development of Drosophila. Mob DNA. 2011;2(1):11. doi: 10.1186/1759-8753-2-11 21958913
14. Kazazian HH Jr., Moran JV. Mobile DNA in Health and Disease. N Engl J Med. 2017;377(4):361–70. doi: 10.1056/NEJMra1510092 28745987
15. Kubo S, Seleme MC, Soifer HS, Perez JL, Moran JV, Kazazian HH Jr., et al. L1 retrotransposition in nondividing and primary human somatic cells. Proc Natl Acad Sci U S A. 2006;103(21):8036–41. doi: 10.1073/pnas.0601954103 16698926
16. Li W, Prazak L, Chatterjee N, Gruninger S, Krug L, Theodorou D, et al. Activation of transposable elements during aging and neuronal decline in Drosophila. Nat Neurosci. 2013;16(5):529–31. doi: 10.1038/nn.3368 23563579
17. Muotri AR, Chu VT, Marchetto MC, Deng W, Moran JV, Gage FH. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature. 2005;435(7044):903–10. doi: 10.1038/nature03663 15959507
18. Bae BI, Jayaraman D, Walsh CA. Genetic changes shaping the human brain. Dev Cell. 2015;32(4):423–34. doi: 10.1016/j.devcel.2015.01.035 25710529
19. Evrony GD, Cai X, Lee E, Hills LB, Elhosary PC, Lehmann HS, et al. Single-neuron sequencing analysis of L1 retrotransposition and somatic mutation in the human brain. Cell. 2012;151(3):483–96. doi: 10.1016/j.cell.2012.09.035 23101622
20. Poduri A, Evrony GD, Cai X, Walsh CA. Somatic mutation, genomic variation, and neurological disease. Science. 2013;341(6141):1237758. doi: 10.1126/science.1237758 23828942
21. Cai X, Evrony GD, Lehmann HS, Elhosary PC, Mehta BK, Poduri A, et al. Single-cell, genome-wide sequencing identifies clonal somatic copy-number variation in the human brain. Cell Rep. 2014;8(5):1280–9. doi: 10.1016/j.celrep.2014.07.043 25159146
22. Bedrosian TA, Linker S, Gage FH. Environment-driven somatic mosaicism in brain disorders. Genome Med. 2016;8(1):58. doi: 10.1186/s13073-016-0317-9 27215330
23. Muotri AR, Marchetto MC, Coufal NG, Oefner R, Yeo G, Nakashima K, et al. L1 retrotransposition in neurons is modulated by MeCP2. Nature. 2010;468(7322):443–6. doi: 10.1038/nature09544 21085180
24. Muotri AR, Zhao C, Marchetto MC, Gage FH. Environmental influence on L1 retrotransposons in the adult hippocampus. Hippocampus. 2009;19(10):1002–7. doi: 10.1002/hipo.20564 19771587
25. Faulkner GJ. Retrotransposons: mobile and mutagenic from conception to death. FEBS Lett. 2011;585(11):1589–94. doi: 10.1016/j.febslet.2011.03.061 21477589
26. De Cecco M, Criscione SW, Peckham EJ, Hillenmeyer S, Hamm EA, Manivannan J, et al. Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements. Aging Cell. 2013;12(2):247–56. doi: 10.1111/acel.12047 23360310
27. De Cecco M, Criscione SW, Peterson AL, Neretti N, Sedivy JM, Kreiling JA. Transposable elements become active and mobile in the genomes of aging mammalian somatic tissues. Aging (Albany NY). 2013;5(12):867–83. doi: 10.18632/aging.100621 24323947
28. De Cecco M, Ito T, Petrashen AP, Elias AE, Skvir NJ, Criscione SW, et al. L1 drives IFN in senescent cells and promotes age-associated inflammation. Nature. 2019;566(7742):73–8. doi: 10.1038/s41586-018-0784-9 30728521
29. Driver CJ, McKechnie SW. Transposable elements as a factor in the aging of Drosophila melanogaster. Ann N Y Acad Sci. 1992;673:83–91. doi: 10.1111/j.1749-6632.1992.tb27439.x 1336649
30. Elsner D, Meusemann K, Korb J. Longevity and transposon defense, the case of termite reproductives. Proc Natl Acad Sci U S A. 2018;115(21):5504–9. doi: 10.1073/pnas.1804046115 29735660
31. St Laurent G 3rd, Hammell N, McCaffrey TA. A LINE-1 component to human aging: do LINE elements exact a longevity cost for evolutionary advantage? Mech Ageing Dev. 2010;131(5):299–305. doi: 10.1016/j.mad.2010.03.008 20346965
32. Wood JG, Helfand SL. Chromatin structure and transposable elements in organismal aging. Front Genet. 2013;4:274. doi: 10.3389/fgene.2013.00274 24363663
33. Wood JG, Jones BC, Jiang N, Chang C, Hosier S, Wickremesinghe P, et al. Chromatin-modifying genetic interventions suppress age-associated transposable element activation and extend life span in Drosophila. Proc Natl Acad Sci U S A. 2016;113(40):11277–82. doi: 10.1073/pnas.1604621113 27621458
34. Maxwell PH, Burhans WC, Curcio MJ. Retrotransposition is associated with genome instability during chronological aging. Proc Natl Acad Sci U S A. 2011;108(51):20376–81. doi: 10.1073/pnas.1100271108 22021441
35. Maxwell PH, Curcio MJ. Incorporation of Y’-Ty1 cDNA destabilizes telomeres in Saccharomyces cerevisiae telomerase-negative mutants. Genetics. 2008;179(4):2313–7. doi: 10.1534/genetics.108.089052 18660531
36. Maxwell PH, Curcio MJ. Host factors that control long terminal repeat retrotransposons in Saccharomyces cerevisiae: implications for regulation of mammalian retroviruses. Eukaryot Cell. 2007;6(7):1069–80. doi: 10.1128/EC.00092-07 17496126
37. Sankowski R, Strohl JJ, Huerta TS, Nasiri E, Mazzarello AN, D’Abramo C, et al. Endogenous retroviruses are associated with hippocampus-based memory impairment. Proc Natl Acad Sci U S A. 2019;116(51):25982–90. doi: 10.1073/pnas.1822164116 31792184
38. Criscione SW, Zhang Y, Thompson W, Sedivy JM, Neretti N. Transcriptional landscape of repetitive elements in normal and cancer human cells. BMC Genomics. 2014;15:583. doi: 10.1186/1471-2164-15-583 25012247
39. Lee E, Iskow R, Yang L, Gokcumen O, Haseley P, Luquette LJ, 3rd, et al. Landscape of somatic retrotransposition in human cancers. Science. 2012;337(6097):967–71. doi: 10.1126/science.1222077 22745252
40. Lock FE, Rebollo R, Miceli-Royer K, Gagnier L, Kuah S, Babaian A, et al. Distinct isoform of FABP7 revealed by screening for retroelement-activated genes in diffuse large B-cell lymphoma. Proc Natl Acad Sci U S A. 2014;111(34):E3534–43. doi: 10.1073/pnas.1405507111 25114248
41. Miki Y, Nishisho I, Horii A, Miyoshi Y, Utsunomiya J, Kinzler KW, et al. Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer. Cancer Res. 1992;52(3):643–5. 1310068
42. Rodriguez-Martin C, Cidre F, Fernandez-Teijeiro A, Gomez-Mariano G, de la Vega L, Ramos P, et al. Familial retinoblastoma due to intronic LINE-1 insertion causes aberrant and noncanonical mRNA splicing of the RB1 gene. J Hum Genet. 2016;61(5):463–6. doi: 10.1038/jhg.2015.173 26763876
43. Scarfo I, Pellegrino E, Mereu E, Kwee I, Agnelli L, Bergaggio E, et al. Identification of a new subclass of ALK-negative ALCL expressing aberrant levels of ERBB4 transcripts. Blood. 2016;127(2):221–32. doi: 10.1182/blood-2014-12-614503 26463425
44. Scott EC, Gardner EJ, Masood A, Chuang NT, Vertino PM, Devine SE. A hot L1 retrotransposon evades somatic repression and initiates human colorectal cancer. Genome Res. 2016;26(6):745–55. doi: 10.1101/gr.201814.115 27197217
45. Teugels E, De Brakeleer S, Goelen G, Lissens W, Sermijn E, De Greve J. De novo Alu element insertions targeted to a sequence common to the BRCA1 and BRCA2 genes. Hum Mutat. 2005;26(3):284. doi: 10.1002/humu.9366 16088935
46. Wiesner T, Lee W, Obenauf AC, Ran L, Murali R, Zhang QF, et al. Alternative transcription initiation leads to expression of a novel ALK isoform in cancer. Nature. 2015;526(7573):453–7. doi: 10.1038/nature15258 26444240
47. Wolff EM, Byun HM, Han HF, Sharma S, Nichols PW, Siegmund KD, et al. Hypomethylation of a LINE-1 promoter activates an alternate transcript of the MET oncogene in bladders with cancer. PLoS Genet. 2010;6(4):e1000917. doi: 10.1371/journal.pgen.1000917 20421991
48. Nguyen THM, Carreira PE, Sanchez-Luque FJ, Schauer SN, Fagg AC, Richardson SR, et al. L1 Retrotransposon Heterogeneity in Ovarian Tumor Cell Evolution. Cell Rep. 2018;23(13):3730–40. doi: 10.1016/j.celrep.2018.05.090 29949758
49. Schauer SN, Carreira PE, Shukla R, Gerhardt DJ, Gerdes P, Sanchez-Luque FJ, et al. L1 retrotransposition is a common feature of mammalian hepatocarcinogenesis. Genome Res. 2018;28(5):639–53. doi: 10.1101/gr.226993.117 29643204
50. Shukla R, Upton KR, Munoz-Lopez M, Gerhardt DJ, Fisher ME, Nguyen T, et al. Endogenous retrotransposition activates oncogenic pathways in hepatocellular carcinoma. Cell. 2013;153(1):101–11. doi: 10.1016/j.cell.2013.02.032 23540693
51. Rodic N, Sharma R, Sharma R, Zampella J, Dai L, Taylor MS, et al. Long interspersed element-1 protein expression is a hallmark of many human cancers. Am J Pathol. 2014;184(5):1280–6. doi: 10.1016/j.ajpath.2014.01.007 24607009
52. Rodic N, Steranka JP, Makohon-Moore A, Moyer A, Shen P, Sharma R, et al. Retrotransposon insertions in the clonal evolution of pancreatic ductal adenocarcinoma. Nat Med. 2015;21(9):1060–4. doi: 10.1038/nm.3919 26259033
53. Treger RS, Pope SD, Kong Y, Tokuyama M, Taura M, Iwasaki A. The Lupus Susceptibility Locus Sgp3 Encodes the Suppressor of Endogenous Retrovirus Expression SNERV. Immunity. 2019;50(2):334–47 e9. doi: 10.1016/j.immuni.2018.12.022 30709743
54. Wu Z, Mei X, Zhao D, Sun Y, Song J, Pan W, et al. DNA methylation modulates HERV-E expression in CD4+ T cells from systemic lupus erythematosus patients. J Dermatol Sci. 2015;77(2):110–6. doi: 10.1016/j.jdermsci.2014.12.004 25595738
55. Neidhart M, Rethage J, Kuchen S, Kunzler P, Crowl RM, Billingham ME, et al. Retrotransposable L1 elements expressed in rheumatoid arthritis synovial tissue: association with genomic DNA hypomethylation and influence on gene expression. Arthritis Rheum. 2000;43(12):2634–47. doi: 10.1002/1529-0131(200012)43:12<2634::AID-ANR3>3.0.CO;2-1 11145021
56. Arru G, Mameli G, Deiana GA, Rassu AL, Piredda R, Sechi E, et al. Humoral immunity response to human endogenous retroviruses K/W differentiates between amyotrophic lateral sclerosis and other neurological diseases. Eur J Neurol. 2018;25(8):1076–e84. doi: 10.1111/ene.13648 29603839
57. Douville R, Liu J, Rothstein J, Nath A. Identification of active loci of a human endogenous retrovirus in neurons of patients with amyotrophic lateral sclerosis. Ann Neurol. 2011;69(1):141–51. doi: 10.1002/ana.22149 21280084
58. Krug L, Chatterjee N, Borges-Monroy R, Hearn S, Liao WW, Morrill K, et al. Retrotransposon activation contributes to neurodegeneration in a Drosophila TDP-43 model of ALS. PLoS Genet. 2017;13(3):e1006635. doi: 10.1371/journal.pgen.1006635 28301478
59. Li W, Jin Y, Prazak L, Hammell M, Dubnau J. Transposable elements in TDP-43-mediated neurodegenerative disorders. PLoS One. 2012;7(9):e44099. doi: 10.1371/journal.pone.0044099 22957047
60. Li W, Lee MH, Henderson L, Tyagi R, Bachani M, Steiner J, et al. Human endogenous retrovirus-K contributes to motor neuron disease. Sci Transl Med. 2015;7(307):307ra153. doi: 10.1126/scitranslmed.aac8201 26424568
61. Tam OH, Rozhkov NV, Shaw R, Kim D, Hubbard I, Fennessey S, et al. Postmortem Cortex Samples Identify Distinct Molecular Subtypes of ALS: Retrotransposon Activation, Oxidative Stress, and Activated Glia. Cell Rep. 2019;29(5):1164–77 e5. doi: 10.1016/j.celrep.2019.09.066 31665631
62. Crow YJ, Rehwinkel J. Aicardi-Goutieres syndrome and related phenotypes: linking nucleic acid metabolism with autoimmunity. Hum Mol Genet. 2009;18(R2):R130–6. doi: 10.1093/hmg/ddp293 19808788
63. Thomas CA, Tejwani L, Trujillo CA, Negraes PD, Herai RH, Mesci P, et al. Modeling of TREX1-Dependent Autoimmune Disease using Human Stem Cells Highlights L1 Accumulation as a Source of Neuroinflammation. Cell Stem Cell. 2017;21(3):319–31 e8. doi: 10.1016/j.stem.2017.07.009 28803918
64. Bollati V, Galimberti D, Pergoli L, Dalla Valle E, Barretta F, Cortini F, et al. DNA methylation in repetitive elements and Alzheimer disease. Brain Behav Immun. 2011;25(6):1078–83. doi: 10.1016/j.bbi.2011.01.017 21296655
65. Guo C, Jeong HH, Hsieh YC, Klein HU, Bennett DA, De Jager PL, et al. Tau Activates Transposable Elements in Alzheimer’s Disease. Cell Rep. 2018;23(10):2874–80. doi: 10.1016/j.celrep.2018.05.004 29874575
66. Protasova MS, Gusev FE, Grigorenko AP, Kuznetsova IL, Rogaev EI, Andreeva TV. Quantitative Analysis of L1-Retrotransposons in Alzheimer’s Disease and Aging. Biochemistry (Mosc). 2017;82(8):962–71. doi: 10.1134/S0006297917080120 28941465
67. Sun W, Samimi H, Gamez M, Zare H, Frost B. Pathogenic tau-induced piRNA depletion promotes neuronal death through transposable element dysregulation in neurodegenerative tauopathies. Nat Neurosci. 2018;21(8):1038–48. doi: 10.1038/s41593-018-0194-1 30038280
68. Yan Z, Zhou Z, Wu Q, Chen ZB, Koo EH, Zhong S. Presymptomatic Increase of an Extracellular RNA in Blood Plasma Associates with the Development of Alzheimer’s Disease. Curr Biol. 2020;30(10):1771–82 e3. doi: 10.1016/j.cub.2020.02.084 32220323
69. Perron H, Bernard C, Bertrand JB, Lang AB, Popa I, Sanhadji K, et al. Endogenous retroviral genes, Herpesviruses and gender in Multiple Sclerosis. J Neurol Sci. 2009;286(1–2):65–72. doi: 10.1016/j.jns.2009.04.034 19447411
70. Perron H, Garson JA, Bedin F, Beseme F, Paranhos-Baccala G, Komurian-Pradel F, et al. Molecular identification of a novel retrovirus repeatedly isolated from patients with multiple sclerosis. The Collaborative Research Group on Multiple Sclerosis. Proc Natl Acad Sci U S A. 1997;94(14):7583–8. doi: 10.1073/pnas.94.14.7583 9207135
71. Perron H, Suh M, Lalande B, Gratacap B, Laurent A, Stoebner P, et al. Herpes simplex virus ICP0 and ICP4 immediate early proteins strongly enhance expression of a retrovirus harboured by a leptomeningeal cell line from a patient with multiple sclerosis. J Gen Virol. 1993;74 (Pt 1):65–72. doi: 10.1099/0022-1317-74-1-65 7678635
72. Tan H, Qurashi A, Poidevin M, Nelson DL, Li H, Jin P. Retrotransposon activation contributes to fragile X premutation rCGG-mediated neurodegeneration. Hum Mol Genet. 2012;21(1):57–65. doi: 10.1093/hmg/ddr437 21940752
73. Gemenetzi M, Lotery AJ. The role of epigenetics in age-related macular degeneration. Eye (Lond). 2014;28(12):1407–17. doi: 10.1038/eye.2014.225 25233816
74. Zhao B, Wu Q, Ye AY, Guo J, Zheng X, Yang X, et al. Somatic LINE-1 retrotransposition in cortical neurons and non-brain tissues of Rett patients and healthy individuals. PLoS Genet. 2019;15(4):e1008043. doi: 10.1371/journal.pgen.1008043 30973874
75. Bourque G, Burns KH, Gehring M, Gorbunova V, Seluanov A, Hammell M, et al. Ten things you should know about transposable elements. Genome Biol. 2018;19(1):199. doi: 10.1186/s13059-018-1577-z 30454069
76. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8(12):973–82. doi: 10.1038/nrg2165 17984973
77. Boeke JD, Garfinkel DJ, Styles CA, Fink GR. Ty elements transpose through an RNA intermediate. Cell. 1985;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7 2982495
78. Ashley J, Cordy B, Lucia D, Fradkin LG, Budnik V, Thomson T. Retrovirus-like Gag Protein Arc1 Binds RNA and Traffics across Synaptic Boutons. Cell. 2018;172(1–2):262–74 e11. doi: 10.1016/j.cell.2017.12.022 29328915
79. Kawamura Y, Sanchez Calle A, Yamamoto Y, Sato TA, Ochiya T. Extracellular vesicles mediate the horizontal transfer of an active LINE-1 retrotransposon. J Extracell Vesicles. 2019;8(1):1643214. doi: 10.1080/20013078.2019.1643214 31448067
80. Pastuzyn ED, Day CE, Kearns RB, Kyrke-Smith M, Taibi AV, McCormick J, et al. The Neuronal Gene Arc Encodes a Repurposed Retrotransposon Gag Protein that Mediates Intercellular RNA Transfer. Cell. 2018;173(1):275. doi: 10.1016/j.cell.2018.03.024 29570995
81. Ribet D, Harper F, Dupressoir A, Dewannieux M, Pierron G, Heidmann T. An infectious progenitor for the murine IAP retrotransposon: emergence of an intracellular genetic parasite from an ancient retrovirus. Genome Res. 2008;18(4):597–609. doi: 10.1101/gr.073486.107 18256233
82. Burke WD, Malik HS, Rich SM, Eickbush TH. Ancient lineages of non-LTR retrotransposons in the primitive eukaryote, Giardia lamblia. Mol Biol Evol. 2002;19(5):619–30. doi: 10.1093/oxfordjournals.molbev.a004121 11961096
83. Eickbush DG, Eickbush TH. Vertical transmission of the retrotransposable elements R1 and R2 during the evolution of the Drosophila melanogaster species subgroup. Genetics. 1995;139(2):671–84. 7713424
84. Malik HS, Burke WD, Eickbush TH. The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol. 1999;16(6):793–805. doi: 10.1093/oxfordjournals.molbev.a026164 10368957
85. Malik HS, Henikoff S, Eickbush TH. Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res. 2000;10(9):1307–18. doi: 10.1101/gr.145000 10984449
86. Jones BC, Wood JG, Chang C, Tam AD, Franklin MJ, Siegel ER, et al. A somatic piRNA pathway in the Drosophila fat body ensures metabolic homeostasis and normal lifespan. Nat Commun. 2016;7:13856. doi: 10.1038/ncomms13856 28000665
87. Sousa-Victor P, Ayyaz A, Hayashi R, Qi Y, Madden DT, Lunyak VV, et al. Piwi Is Required to Limit Exhaustion of Aging Somatic Stem Cells. Cell Rep. 2017;20(11):2527–37. doi: 10.1016/j.celrep.2017.08.059 28903034
88. Zhou F, Li M, Wei Y, Lin K, Lu Y, Shen J, et al. Activation of HERV-K Env protein is essential for tumorigenesis and metastasis of breast cancer cells. Oncotarget. 2016;7(51):84093–117. doi: 10.18632/oncotarget.11455 27557521
89. Chan SM, Sapir T, Park SS, Rual JF, Contreras-Galindo R, Reiner O, et al. The HERV-K accessory protein Np9 controls viability and migration of teratocarcinoma cells. PLoS One. 2019;14(2):e0212970. doi: 10.1371/journal.pone.0212970 30818388
90. Gonzalez-Cao M, Iduma P, Karachaliou N, Santarpia M, Blanco J, Rosell R. Human endogenous retroviruses and cancer. Cancer Biol Med. 2016;13(4):483–8. doi: 10.20892/j.issn.2095-3941.2016.0080 28154780
91. Kim A, Terzian C, Santamaria P, Pelisson A, Purd’homme N, Bucheton A. Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1994;91(4):1285–9. doi: 10.1073/pnas.91.4.1285 8108403
92. Marlor RL, Parkhurst SM, Corces VG. The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol. 1986;6(4):1129–34. doi: 10.1128/mcb.6.4.1129 3023871
93. Pelisson A, Song SU, Prud’homme N, Smith PA, Bucheton A, Corces VG. Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J. 1994;13(18):4401–11. 7925283
94. Song SU, Gerasimova T, Kurkulos M, Boeke JD, Corces VG. An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev. 1994;8(17):2046–57. doi: 10.1101/gad.8.17.2046 7958877
95. Ribet D, Harper F, Esnault C, Pierron G, Heidmann T. The GLN family of murine endogenous retroviruses contains an element competent for infectious viral particle formation. J Virol. 2008;82(9):4413–9. doi: 10.1128/JVI.02141-07 18287236
96. Dewannieux M, Harper F, Richaud A, Letzelter C, Ribet D, Pierron G, et al. Identification of an infectious progenitor for the multiple-copy HERV-K human endogenous retroelements. Genome Res. 2006;16(12):1548–56. doi: 10.1101/gr.5565706 17077319
97. Robinson-McCarthy LR, McCarthy KR, Raaben M, Piccinotti S, Nieuwenhuis J, Stubbs SH, et al. Reconstruction of the cell entry pathway of an extinct virus. PLoS Pathog. 2018;14(8):e1007123. doi: 10.1371/journal.ppat.1007123 30080900
98. Szymczak AL, Workman CJ, Wang Y, Vignali KM, Dilioglou S, Vanin EF, et al. Correction of multi-gene deficiency in vivo using a single ’self-cleaving’ 2A peptide-based retroviral vector. Nat Biotechnol. 2004;22(5):589–94. doi: 10.1038/nbt957 15064769
99. Capy P, Langin T, Higuet D, Maurer P, Bazin C. Do the integrases of LTR-retrotransposons and class II element transposases have a common ancestor? Genetica. 1997;100(1–3):63–72. 9440259
100. Chalvet F, Teysset L, Terzian C, Prud’homme N, Santamaria P, Bucheton A, et al. Proviral amplification of the Gypsy endogenous retrovirus of Drosophila melanogaster involves env-independent invasion of the female germline. EMBO J. 1999;18(9):2659–69. doi: 10.1093/emboj/18.9.2659 10228177
101. Syomin BV, Fedorova LI, Surkov SA, Ilyin YV. The endogenous Drosophila melanogaster retrovirus gypsy can propagate in Drosophila hydei cells. Mol Gen Genet. 2001;264(5):588–94. doi: 10.1007/s004380000344 11212913
102. Brasset E, Taddei AR, Arnaud F, Faye B, Fausto AM, Mazzini M, et al. Viral particles of the endogenous retrovirus ZAM from Drosophila melanogaster use a pre-existing endosome/exosome pathway for transfer to the oocyte. Retrovirology. 2006;3:25. doi: 10.1186/1742-4690-3-25 16684341
103. Teysset L, Burns JC, Shike H, Sullivan BL, Bucheton A, Terzian C. A Moloney murine leukemia virus-based retroviral vector pseudotyped by the insect retroviral gypsy envelope can infect Drosophila cells. J Virol. 1998;72(1):853–6. doi: 10.1128/JVI.72.1.853-856.1998 9420299
104. Lecher P, Bucheton A, Pelisson A. Expression of the Drosophila retrovirus gypsy as ultrastructurally detectable particles in the ovaries of flies carrying a permissive flamenco allele. J Gen Virol. 1997;78 (Pt 9):2379–88. doi: 10.1099/0022-1317-78-9-2379 9292028
105. Bodea GO, McKelvey EGZ, Faulkner GJ. Retrotransposon-induced mosaicism in the neural genome. Open Biol. 2018;8(7). doi: 10.1098/rsob.180074 30021882
106. Upton KR, Gerhardt DJ, Jesuadian JS, Richardson SR, Sanchez-Luque FJ, Bodea GO, et al. Ubiquitous L1 mosaicism in hippocampal neurons. Cell. 2015;161(2):228–39. doi: 10.1016/j.cell.2015.03.026 25860606
107. Maxwell PH. What might retrotransposons teach us about aging? Curr Genet. 2016;62(2):277–82. doi: 10.1007/s00294-015-0538-2 26581630
108. Savva YA, Jepson JE, Chang YJ, Whitaker R, Jones BC, St Laurent G, et al. RNA editing regulates transposon-mediated heterochromatic gene silencing. Nat Commun. 2013;4:2745. doi: 10.1038/ncomms3745 24201902
109. Simon M, Van Meter M, Ablaeva J, Ke Z, Gonzalez RS, Taguchi T, et al. LINE1 Derepression in Aged Wild-Type and SIRT6-Deficient Mice Drives Inflammation. Cell Metab. 2019;29(4):871–85 e5. doi: 10.1016/j.cmet.2019.02.014 30853213
110. Blaudin de The FX, Rekaik H, Peze-Heidsieck E, Massiani-Beaudoin O, Joshi RL, Fuchs J, et al. Engrailed homeoprotein blocks degeneration in adult dopaminergic neurons through LINE-1 repression. EMBO J. 2018;37(15). doi: 10.15252/embj.201797374 29941661
111. Kaneko H, Dridi S, Tarallo V, Gelfand BD, Fowler BJ, Cho WG, et al. DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature. 2011;471(7338):325–30. doi: 10.1038/nature09830 21297615
112. Tarallo V, Hirano Y, Gelfand BD, Dridi S, Kerur N, Kim Y, et al. DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88. Cell. 2012;149(4):847–59. doi: 10.1016/j.cell.2012.03.036 22541070
113. Carreira PE, Ewing AD, Li G, Schauer SN, Upton KR, Fagg AC, et al. Evidence for L1-associated DNA rearrangements and negligible L1 retrotransposition in glioblastoma multiforme. Mob DNA. 2016;7:21. doi: 10.1186/s13100-016-0076-6 27843499
114. Doucet-O’Hare TT, Rodic N, Sharma R, Darbari I, Abril G, Choi JA, et al. LINE-1 expression and retrotransposition in Barrett’s esophagus and esophageal carcinoma. Proc Natl Acad Sci U S A. 2015;112(35):E4894–900. doi: 10.1073/pnas.1502474112 26283398
115. Doucet-O’Hare TT, Sharma R, Rodic N, Anders RA, Burns KH, Kazazian HH Jr. Somatically Acquired LINE-1 Insertions in Normal Esophagus Undergo Clonal Expansion in Esophageal Squamous Cell Carcinoma. Hum Mutat. 2016;37(9):942–54. doi: 10.1002/humu.23027 27319353
116. Solyom S, Ewing AD, Rahrmann EP, Doucet T, Nelson HH, Burns MB, et al. Extensive somatic L1 retrotransposition in colorectal tumors. Genome Res. 2012;22(12):2328–38. doi: 10.1101/gr.145235.112 22968929
117. Tang Z, Steranka JP, Ma S, Grivainis M, Rodic N, Huang CR, et al. Human transposon insertion profiling: Analysis, visualization and identification of somatic LINE-1 insertions in ovarian cancer. Proc Natl Acad Sci U S A. 2017;114(5):E733–E40. doi: 10.1073/pnas.1619797114 28096347
118. Wylie A, Jones AE, D’Brot A, Lu WJ, Kurtz P, Moran JV, et al. p53 genes function to restrain mobile elements. Genes Dev. 2016;30(1):64–77. doi: 10.1101/gad.266098.115 26701264
119. Yang N, Kazazian HH Jr. L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol. 2006;13(9):763–71. doi: 10.1038/nsmb1141 16936727
120. Carreira PE, Richardson SR, Faulkner GJ. L1 retrotransposons, cancer stem cells and oncogenesis. FEBS J. 2014;281(1):63–73. doi: 10.1111/febs.12601 24286172
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