Do Small RNAs Interfere With LINE-1?

Soifer, Harris S.

doi:https://doi.org/10.1155/JBB/2006/29049

BioMed Research International

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LINE-1 Retrotransposition: Impact on Genome Stability and Diversity and Human Disease

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Review Article | Open Access

Volume 2006 | Article ID 029049 | https://doi.org/10.1155/JBB/2006/29049

Do Small RNAs Interfere With LINE-1?

Harris S. Soifer¹

Received02 Aug 2005

Revised07 Oct 2005

Accepted12 Oct 2005

Published02 Feb 2006

Abstract

Long interspersed elements (LINE-1 or L1) are the most active transposable elements in the human genome. Due to their high copy number and ability to sponsor retrotransposition of nonautonomous RNA sequences, unchecked L1 activity can negatively impact the genome by a number of means. Substantial evidence in lower eukaryotes demonstrates that the RNA interference (RNAi) machinery plays a major role in containing transposon activity. Despite extensive analysis in other eukaryotes, no experimental evidence has been presented that L1-derived siRNAs exist, or that the RNAi plays a significant role in restricting L1 activity in the human genome. This review will present evidence showing a direct role for RNAi in suppressing the movement of transposable elements in other eukaryotes, as well as speculate on the role RNAi might play in protecting the human genome from LINE-1 activity.

References

E M Ostertag and H H Jr Kazazian, “Biology of mammalian L1 retrotransposons,” Annual Review of Genetics, vol. 35, pp. 501–538, 2001.
View at: Google Scholar
B Brouha, J Schustak, R M Badge et al., “Hot L1s account for the bulk of retrotransposition in the human population,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 9, pp. 5280–5285, 2003.
View at: Google Scholar
D A Kulpa and J V Moran, “Ribonucleoprotein particle formation is necessary but not sufficient for LINE-1 retrotransposition,” Human Molecular Genetics, vol. 14, no. 21, pp. 3237–3248, 2005.
View at: Google Scholar
M L Kimberland, V Divoky, J Prchal, U Schwahn, W Berger, and H H Jr Kazazian, “Full-length human L1 insertions retain the capacity for high frequency retrotransposition in cultured cells,” Human Molecular Genetics, vol. 8, no. 8, pp. 1557–1560, 1999.
View at: Google Scholar
N Gilbert, S Lutz-Prigge, and J V Moran, “Genomic deletions created upon LINE-1 retrotransposition,” Cell, vol. 110, no. 3, pp. 315–325, 2002.
View at: Google Scholar
D E Symer, C Connelly, S T Szak et al., “Human l1 retrotransposition is associated with genetic instability in vivo,” Cell, vol. 110, no. 3, pp. 327–338, 2002.
View at: Google Scholar
B Burwinkel and M W Kilimann, “Unequal homologous recombination between LINE-1 elements as a mutational mechanism in human genetic disease,” Journal of Molecular Biology, vol. 277, no. 3, pp. 513–517, 1998.
View at: Google Scholar
A Kumatori, N N Faizunnessa, S Suzuki, T Moriuchi, H Kurozumi, and M Nakamura, “Nonhomologous recombination between the cytochrome ${\mathrm {b}}_{558}$ heavy chain gene (CYBB) and LINE-1 causes an X-linked chronic granulomatous disease,” Genomics, vol. 53, no. 2, pp. 123–128, 1998.
View at: Google Scholar
R Suminaga, Y Takeshima, K Yasuda, N Shiga, H Nakamura, and M Matsuo, “Non-homologous recombination between Alu and LINE-1 repeats caused a 430-kb deletion in the dystrophin gene: a novel source of genomic instability,” Journal of Human Genetics, vol. 45, no. 6, pp. 331–336, 2000.
View at: Google Scholar
H H Jr Kazazian and J V Moran, “The impact of L1 retrotransposons on the human genome,” Nature Genetics, vol. 19, no. 1, pp. 19–24, 1998.
View at: Google Scholar
C Esnault, J Maestre, and T Heidmann, “Human LINE retrotransposons generate processed pseudogenes,” Nature Genetics, vol. 24, no. 4, pp. 363–367, 2000.
View at: Google Scholar
W Wei, N Gilbert, S L Ooi et al., “Human L1 retrotransposition: cis preference versus trans complementation,” Molecular and Cellular Biology, vol. 21, no. 4, pp. 1429–1439, 2001.
View at: Google Scholar
G Meister and T Tuschl, “Mechanisms of gene silencing by double-stranded RNA,” Nature, vol. 431, no. 7006, pp. 343–349, 2004.
View at: Google Scholar
E Bernstein, A A Caudy, S M Hammond, and G J Hannon, “Role for a bidentate ribonuclease in the initiation step of RNA interference,” Nature, vol. 409, no. 6818, pp. 363–366, 2001.
View at: Google Scholar
Y Lee, K Jeon, J-T Lee, S Kim, and V N Kim, “MicroRNA maturation: stepwise processing and subcellular localization,” The EMBO Journal, vol. 21, no. 17, pp. 4663–4670, 2002.
View at: Google Scholar
S M Hammond, S Boettcher, A A Caudy, R Kobayashi, and G J Hannon, “Argonaute2, a link between genetic and biochemical analyses of RNAi,” Science, vol. 293, no. 5532, pp. 1146–1150, 2001.
View at: Google Scholar
D S Schwarz, Y Tomari, and P D Zamore, “The RNA-induced silencing complex is a ${\text{Mg}}^{2 + }$ -dependent endonuclease,” Current Biology, vol. 14, no. 9, pp. 787–791, 2004.
View at: Google Scholar
Z Mourelatos, J Dostie, S Paushkin et al., “miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs,” Genes & Development, vol. 16, no. 6, pp. 720–728, 2002.
View at: Google Scholar
H Tabara, M Sarkissian, W G Kelly et al., “The rde-1 gene, RNA interference, and transposon silencing in C elegans,” Cell, vol. 99, no. 2, pp. 123–132, 1999.
View at: Google Scholar
R F Ketting, T HA Haverkamp, H GAM van Luenen, and R HA Plasterk, “Mut-7 of C elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD,” Cell, vol. 99, no. 2, pp. 133–141, 1999.
View at: Google Scholar
N L Vastenhouw, S EJ Fischer, V JP Robert et al., “A genome-wide screen identifies 27 genes involved in transposon silencing in C elegans,” Current Biology, vol. 13, no. 15, pp. 1311–1316, 2003.
View at: Google Scholar
H Zhang, F A Kolb, L Jaskiewicz, E Westhof, and W Filipowicz, “Single processing center models for human Dicer and bacterial RNase III,” Cell, vol. 118, no. 1, pp. 57–68, 2004.
View at: Google Scholar
E Bernstein, S Y Kim, M A Carmell et al., “Dicer is essential for mouse development,” Nature Genetics, vol. 35, no. 3, pp. 215–217, 2003.
View at: Google Scholar
C Kanellopoulou, S A Muljo, A L Kung et al., “Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing,” Genes & Development, vol. 19, no. 4, pp. 489–501, 2005.
View at: Google Scholar
P Svoboda, P Stein, M Anger, E Bernstein, G J Hannon, and R M Schultz, “RNAi and expression of retrotransposons MuERV-L and IAP in preimplantation mouse embryos,” Developmental Biology, vol. 269, no. 1, pp. 276–285, 2004.
View at: Google Scholar
G Meister, M Landthaler, A Patkaniowska, Y Dorsett, G Teng, and T Tuschl, “Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs,” Molecular Cell, vol. 15, no. 2, pp. 185–197, 2004.
View at: Google Scholar
J Liu, M A Carmell, F V Rivas et al., “Argonaute2 is the catalytic engine of mammalian RNAi,” Science, vol. 305, no. 5689, pp. 1437–1441, 2004.
View at: Google Scholar
T Nolan, L Braccini, G Azzalin, A De Toni, G Macino, and C Cogoni, “The post-transcriptional gene silencing machinery functions independently of DNA methylation to repress a LINE1-like retrotransposon in Neurospora crassa,” Nucleic Acids Research, vol. 33, no. 5, pp. 1564–1573, 2005.
View at: Google Scholar
H Shi, A Djikeng, C Tschudi, and E Ullu, “Argonaute protein in the early divergent eukaryote Trypanosoma brucei: control of small interfering RNA accumulation and retroposon transcript abundance,” Molecular and Cellular Biology, vol. 24, no. 1, pp. 420–427, 2004.
View at: Google Scholar
A Djikeng, H Shi, C Tschudi, and E Ullu, “RNA interference in Trypanosoma brucei: cloning of small interfering RNAs provides evidence for retroposon-derived 24-26-nucleotide RNAs,” RNA, vol. 7, no. 11, pp. 1522–1530, 2001.
View at: Google Scholar
D Zilberman, X Cao, and S E Jacobsen, “ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation,” Science, vol. 299, no. 5607, pp. 716–719, 2003.
View at: Google Scholar
E Sarot, G Payen-Groschêne, A Bucheton, and A Pélisson, “Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene,” Genetics, vol. 166, no. 3, pp. 1313–1321, 2004.
View at: Google Scholar
A I Kalmykova, M S Klenov, and V A Gvozdev, “Argonaute protein PIWI controls mobilization of retrotransposons in the Drosophila male germline,” Nucleic Acids Research, vol. 33, no. 6, pp. 2052–2059, 2005.
View at: Google Scholar
N L Vastenhouw and R HA Plasterk, “RNAi protects the Caenorhabditis elegans germline against transposition,” Trends in Genetics, vol. 20, no. 7, pp. 314–319, 2004.
View at: Google Scholar
T Sijen and R HA Plasterk, “Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi,” Nature, vol. 426, no. 6964, pp. 310–314, 2003.
View at: Google Scholar
D F Hudson, C Morrison, S Ruchaud, and W C Earnshaw, “Reverse genetics of essential genes in tissue-culture cells: ‘dead cells talking’,” Trends in Cell Biology, vol. 12, no. 6, pp. 281–287, 2002.
View at: Google Scholar
P J Paddison, J M Silva, D S Conklin et al., “A resource for large-scale RNA-interference-based screens in mammals,” Nature, vol. 428, no. 6981, pp. 427–431, 2004.
View at: Google Scholar
K Berns, E M Hijmans, J Mullenders et al., “A large-scale RNAi screen in human cells identifies new components of the p53 pathway,” Nature, vol. 428, no. 6981, pp. 431–437, 2004.
View at: Google Scholar
G Hutvágner, J McLachlan, A E Pasquinelli, E Bálint, T Tuschl, and P D Zamore, “A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA,” Science, vol. 293, no. 5531, pp. 834–838, 2001.
View at: Google Scholar
K Ye, L Malinina, and D J Patel, “Recognition of small interfering RNA by a viral suppressor of RNA silencing,” Nature, vol. 426, no. 6968, pp. 874–878, 2003.
View at: Google Scholar
S Lu and B R Cullen, “Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and MicroRNA biogenesis,” Journal of Virology, vol. 78, no. 23, pp. 12868–12876, 2004.
View at: Google Scholar
E Bucher, H Hemmes, P de Haan, R Goldbach, and M Prins, “The influenza A virus NS1 protein binds small interfering RNAs and suppresses RNA silencing in plants,” Journal of General Virology, vol. 85, no. pt 4, pp. 983–991, 2004.
View at: Google Scholar
H Kawasaki and K Taira, “Short hairpin type of dsRNAs that are controlled by ${\text{tRNA}}^{{\text{Val}}}$ promoter significantly induce RNAi-mediated gene silencing in the cytoplasm of human cells,” Nucleic Acids Research, vol. 31, no. 2, pp. 700–707, 2003.
View at: Google Scholar
M Lagos-Quintana, R Rauhut, W Lendeckel, and T Tuschl, “Identification of novel genes coding for small expressed RNAs,” Science, vol. 294, no. 5543, pp. 853–858, 2001.
View at: Google Scholar
T Fukagawa, M Nogami, M Yoshikawa et al., “Dicer is essential for formation of the heterochromatin structure in vertebrate cells,” Nature Cell Biology, vol. 6, no. 8, pp. 784–791, 2004.
View at: Google Scholar
D Branciforte and S L Martin, “Developmental and cell type specificity of LINE-1 expression in mouse testis: implications for transposition,” Molecular and Cellular Biology, vol. 14, no. 4, pp. 2584–2592, 1994.
View at: Google Scholar
S Ergün, C Buschmann, J Heukeshoven et al., “Cell type-specific expression of LINE-1 open reading frames 1 and 2 in fetal and adult human tissues,” The Journal of Biological Chemistry, vol. 279, no. 26, pp. 27753–27763, 2004.
View at: Google Scholar
Y Miki, I Nishisho, A Horii et al., “Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer,” Cancer Research, vol. 52, no. 3, pp. 643–645, 1992.
View at: Google Scholar
J Skowronski and M F Singer, “Expression of a cytoplasmic LINE-1 transcript is regulated in a human teratocarcinoma cell line,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 18, pp. 6050–6054, 1985.
View at: Google Scholar
G D Swergold, “Identification, characterization, and cell specificity of a human LINE-1 promoter,” Molecular and Cellular Biology, vol. 10, no. 12, pp. 6718–6729, 1990.
View at: Google Scholar
H S Soifer, A Zaragoza, M Peyvan, M A Behlke, and J J Rossi, “A potential role for RNA interference in controlling the activity of the human LINE-1 retrotransposon,” Nucleic Acids Research, vol. 33, no. 3, pp. 846–856, 2005.
View at: Google Scholar
M Speek, “Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes,” Molecular and Cellular Biology, vol. 21, no. 6, pp. 1973–1985, 2001.
View at: Google Scholar
P Nigumann, K Redik, K Mätlik, and M Speek, “Many human genes are transcribed from the antisense promoter of L1 retrotransposon,” Genomics, vol. 79, no. 5, pp. 628–634, 2002.
View at: Google Scholar
N Yang, L Zhang, Y Zhang, and H H Jr Kazazian, “An important role for RUNX3 in human L1 transcription and retrotransposition,” Nucleic Acids Research, vol. 31, no. 16, pp. 4929–4940, 2003.
View at: Google Scholar
D S Schwarz, G Hutvágner, T Du, Z Xu, N Aronin, and P D Zamore, “Asymmetry in the assembly of the RNAi enzyme complex,” Cell, vol. 115, no. 2, pp. 199–208, 2003.
View at: Google Scholar
A Khvorova, A Reynolds, and S D Jayasena, “Functional siRNAs and miRNAs exhibit strand bias,” Cell, vol. 115, no. 2, pp. 209–216, 2003.
View at: Google Scholar
S Boissinot, P Chevret, and A V Furano, “L1 (LINE-1) retrotransposon evolution and amplification in recent human history,” Molecular Biology and Evolution, vol. 17, no. 6, pp. 915–928, 2000.
View at: Google Scholar
S A Muljo, K M Ansel, C Kanellopoulou, D M Livingston, A Rao, and K Rajewsky, “Aberrant T cell differentiation in the absence of Dicer,” The Journal of Experimental Medicine, vol. 202, no. 2, pp. 261–269, 2005.
View at: Google Scholar

Copyright

Copyright © 2006 Harris S. Soifer. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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