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Genome biology and evolution2016; 8(5); 1327-1337; doi: 10.1093/gbe/evw078

Transposable Element Targeting by piRNAs in Laurasiatherians with Distinct Transposable Element Histories.

Abstract: PIWI proteins and PIWI-interacting RNAs (piRNAs) are part of a cellular pathway that has evolved to protect genomes against the proliferation of transposable elements (TEs). PIWIs and piRNAs assemble into complexes that are involved in epigenetic and post-transcriptional repression of TEs. Most of our understanding of the mechanisms of piRNA-mediated TE silencing comes from fruit fly and mouse models. However, even in these well-studied animals it is unclear how piRNA responses relate to variable TE expression and whether the strength of the piRNA response affects TE content over time. Here, we assessed the evolutionary interactions between TE and piRNAs in a statistical framework using three nonmodel laurasiatherian mammals as a study system: dog, horse, and a vesper bat. These three species diverged ∼80 million years ago and have distinct genomic TE contents. By comparing species with distinct TE landscapes, we aimed to identify clear relationships among TE content, expression, and piRNAs. We found that the TE subfamilies that are the most transcribed appear to elicit the strongest "ping-pong" response. This was most evident among long interspersed elements, but the relationships between expression and ping-pong pilRNA (piRNA-like) expression were more complex among SINEs. SINE transcripts were equally abundant in the dog and horse yet new SINE insertions were relatively rare in the horse genome, where we identified a stronger piRNA response. Our analyses suggest that the piRNA response can have a strong impact on the TE composition of a genome. However, our results also suggest that the presence of a robust piRNA response is apparently not sufficient to stop TE mobilization and accumulation.
© The Author(s) 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
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Publication Date: 2016-05-09 PubMed ID: 27060702PubMed Central: PMC4898795DOI: 10.1093/gbe/evw078Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research explores how PIWI proteins and PIWI-interacting RNAs (piRNAs) – components of cellular pathways that protect genomes from transposable elements (TEs) – work in various mammals. By studying three different species – dog, horse, and vesper bat – the researchers aim to understand the relationship between TE content, their expression, and piRNAs. The findings suggest that a robust piRNA response doesn’t necessarily stop TE mobilization and build-up.

More on PIWI Proteins and PIWI-Interacting RNAs (piRNAs)

  • These are critical components of cellular pathways that evolved to shield genomes against the proliferation of transposable elements (TEs).
  • These PIWIs and piRNAs gather into complexes that play a role in the epigenetic and post-transcriptional repression of TEs.
  • Understanding of piRNA-mediated TE silencing is largely from fruit fly and mouse models. Even in these models, it is not quite clear how the piRNA responses are related to variable TE expression and how the strength of the piRNA response affects TE content over time.

Research Aims and Approach

  • The research sought to study the evolutionary interaction between TE and piRNAs using a statistical framework and using nonmodel laurasiatherian mammals (dog, horse, and vesper bat) as the subjects.
  • These three species were chosen because they separated approximately 80 million years ago and each has distinct genomic TE contents.
  • The goal was to identify clear relationships among TE content, TE expression, and piRNAs by comparing the species that have distinct TE landscapes.

Findings of the Study

  • The researchers found that TE subfamilies that are most transcribed tend to cause the strongest “ping-pong” response.
  • This “ping-pong” response is primarily seen among long interspersed elements, but the relationships between expression and ping-pong pilRNA (piRNA-like) expression were more complex among SINEs.
  • SINE transcripts were equally abundant in the dog and horse, but new SINE insertions were rare in the horse genome, where there was a stronger piRNA response.
  • The study suggests that piRNA response can strongly impact the TE composition of a genome. However, a robust piRNA response does not appear to be sufficient in stopping TE mobilization and accumulation.

Cite This Article

APA
Vandewege MW, Platt RN, Ray DA, Hoffmann FG. (2016). Transposable Element Targeting by piRNAs in Laurasiatherians with Distinct Transposable Element Histories. Genome Biol Evol, 8(5), 1327-1337. https://doi.org/10.1093/gbe/evw078

Publication

Genome biology and evolution
ISSN: 1759-6653
NlmUniqueID: 101509707
Country: England
Language: English
Volume: 8
Issue: 5
Pages: 1327-1337

Researcher Affiliations

Vandewege, Michael W
  • Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University.
Platt, Roy N
  • Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University.
Ray, David A
  • Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University federico.g.hoffmann@gmail.com david.4.ray@gmail.com.
Hoffmann, Federico G
  • Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University federico.g.hoffmann@gmail.com david.4.ray@gmail.com.

MeSH Terms

  • Animals
  • Chiroptera
  • DNA Transposable Elements / genetics
  • Dogs
  • Evolution, Molecular
  • Gene Silencing
  • Horses
  • Mice
  • RNA, Small Interfering / genetics
  • Selection, Genetic
  • Transcription, Genetic

References

This article includes 46 references
  1. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju J, Sheridan R, Sander C, Zavolan M, Tuschl T. A novel class of small RNAs bind to MILI protein in mouse testes.. Nature 2006 Jul 13;442(7099):203-7.
    pubmed: 16751777doi: 10.1038/nature04916google scholar: lookup
  2. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice.. Mol Cell 2008 Sep 26;31(6):785-99.
    pmc: PMC2730041pubmed: 18922463doi: 10.1016/j.molcel.2008.09.003google scholar: lookup
  3. Aravin AA, Hannon GJ, Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race.. Science 2007 Nov 2;318(5851):761-4.
    pubmed: 17975059doi: 10.1126/science.1146484google scholar: lookup
  4. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control.. Science 2007 May 4;316(5825):744-7.
    pubmed: 17446352doi: 10.1126/science.1142612google scholar: lookup
  5. Beyret E, Liu N, Lin H. piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism.. Cell Res 2012 Oct;22(10):1429-39.
    pmc: PMC3463270pubmed: 22907665doi: 10.1038/cr.2012.120google scholar: lookup
  6. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila.. Cell 2007 Mar 23;128(6):1089-103.
    pubmed: 17346786doi: 10.1016/j.cell.2007.01.043google scholar: lookup
  7. Brookfield JF, Johnson LJ. The evolution of mobile DNAs: when will transposons create phylogenies that look as if there is a master gene?. Genetics 2006 Jun;173(2):1115-23.
    pmc: PMC1526530pubmed: 16790583doi: 10.1534/genetics.104.027219google scholar: lookup
  8. Callinan PA, Wang J, Herke SW, Garber RK, Liang P, Batzer MA. Alu retrotransposition-mediated deletion.. J Mol Biol 2005 May 13;348(4):791-800.
    pubmed: 15843013doi: 10.1016/j.jmb.2005.02.043google scholar: lookup
  9. Chirn GW, Rahman R, Sytnikova YA, Matts JA, Zeng M, Gerlach D, Yu M, Berger B, Naramura M, Kile BT, Lau NC. Conserved piRNA Expression from a Distinct Set of piRNA Cluster Loci in Eutherian Mammals.. PLoS Genet 2015 Nov;11(11):e1005652.
    pmc: PMC4654475pubmed: 26588211doi: 10.1371/journal.pgen.1005652google scholar: lookup
  10. de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD. Repetitive elements may comprise over two-thirds of the human genome.. PLoS Genet 2011 Dec;7(12):e1002384.
    pmc: PMC3228813pubmed: 22144907doi: 10.1371/journal.pgen.1002384google scholar: lookup
  11. Gilbert N, Lutz-Prigge S, Moran JV. Genomic deletions created upon LINE-1 retrotransposition.. Cell 2002 Aug 9;110(3):315-25.
    pubmed: 12176319doi: 10.1016/s0092-8674(02)00828-0google scholar: lookup
  12. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins.. Nature 2006 Jul 13;442(7099):199-202.
    pubmed: 16751776doi: 10.1038/nature04917google scholar: lookup
  13. Gou LT, Dai P, Yang JH, Xue Y, Hu YP, Zhou Y, Kang JY, Wang X, Li H, Hua MM, Zhao S, Hu SD, Wu LG, Shi HJ, Li Y, Fu XD, Qu LH, Wang ED, Liu MF. Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis.. Cell Res 2014 Jun;24(6):680-700.
    pmc: PMC4042167pubmed: 24787618doi: 10.1038/cr.2014.41google scholar: lookup
  14. Ha H, Song J, Wang S, Kapusta A, Feschotte C, Chen KC, Xing J. A comprehensive analysis of piRNAs from adult human testis and their relationship with genes and mobile elements.. BMC Genomics 2014 Jul 1;15(1):545.
    pmc: PMC4094622pubmed: 24981367doi: 10.1186/1471-2164-15-545google scholar: lookup
  15. Han K, Sen SK, Wang J, Callinan PA, Lee J, Cordaux R, Liang P, Batzer MA. Genomic rearrangements by LINE-1 insertion-mediated deletion in the human and chimpanzee lineages.. Nucleic Acids Res 2005;33(13):4040-52.
    pmc: PMC1179734pubmed: 16034026doi: 10.1093/nar/gki718google scholar: lookup
  16. Hirano T, Iwasaki YW, Lin ZY, Imamura M, Seki NM, Sasaki E, Saito K, Okano H, Siomi MC, Siomi H. Small RNA profiling and characterization of piRNA clusters in the adult testes of the common marmoset, a model primate.. RNA 2014 Aug;20(8):1223-37.
    pmc: PMC4105748pubmed: 24914035doi: 10.1261/rna.045310.114google scholar: lookup
  17. Höck J, Meister G. The Argonaute protein family.. Genome Biol 2008;9(2):210.
    pmc: PMC2374724pubmed: 18304383doi: 10.1186/gb-2008-9-2-210google scholar: lookup
  18. Kapitonov VV, Jurka J. Helitrons on a roll: eukaryotic rolling-circle transposons.. Trends Genet 2007 Oct;23(10):521-9.
    pubmed: 17850916doi: 10.1016/j.tig.2007.08.004google scholar: lookup
  19. Kelleher ES, Barbash DA. Analysis of piRNA-mediated silencing of active TEs in Drosophila melanogaster suggests limits on the evolution of host genome defense.. Mol Biol Evol 2013 Aug;30(8):1816-29.
    pmc: PMC3708497pubmed: 23625890doi: 10.1093/molbev/mst081google scholar: lookup
  20. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.. J Mol Evol 1980 Dec;16(2):111-20.
    pubmed: 7463489doi: 10.1007/BF01731581google scholar: lookup
  21. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.. Genome Biol 2009;10(3):R25.
    pmc: PMC2690996pubmed: 19261174doi: 10.1186/gb-2009-10-3-r25google scholar: lookup
  22. Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, Kingston RE. Characterization of the piRNA complex from rat testes.. Science 2006 Jul 21;313(5785):363-7.
    pubmed: 16778019doi: 10.1126/science.1130164google scholar: lookup
  23. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome.. BMC Bioinformatics 2011 Aug 4;12:323.
    pmc: PMC3163565pubmed: 21816040doi: 10.1186/1471-2105-12-323google scholar: lookup
  24. Li XZ, Roy CK, Dong X, Bolcun-Filas E, Wang J, Han BW, Xu J, Moore MJ, Schimenti JC, Weng Z, Zamore PD. An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes.. Mol Cell 2013 Apr 11;50(1):67-81.
    pmc: PMC3671569pubmed: 23523368doi: 10.1016/j.molcel.2013.02.016google scholar: lookup
  25. Liu G, Zhao S, Bailey JA, Sahinalp SC, Alkan C, Tuzun E, Green ED, Eichler EE. Analysis of primate genomic variation reveals a repeat-driven expansion of the human genome.. Genome Res 2003 Mar;13(3):358-68.
    pmc: PMC430288pubmed: 12618366doi: 10.1101/gr.923303google scholar: lookup
  26. Liu G, Lei B, Li Y, Tong K, Ding Y, Luo L, Xia X, Jiang S, Deng C, Xiong Y, Li F. Discovery of potential piRNAs from next generation sequences of the sexually mature porcine testes.. PLoS One 2012;7(4):e34770.
    pmc: PMC3321025pubmed: 22493715doi: 10.1371/journal.pone.0034770google scholar: lookup
  27. Lukic S, Chen K. Human piRNAs are under selection in Africans and repress transposable elements.. Mol Biol Evol 2011 Nov;28(11):3061-7.
    pmc: PMC3199439pubmed: 21613236doi: 10.1093/molbev/msr141google scholar: lookup
  28. Malone CD, Hannon GJ. Small RNAs as guardians of the genome.. Cell 2009 Feb 20;136(4):656-68.
    pmc: PMC2792755pubmed: 19239887doi: 10.1016/j.cell.2009.01.045google scholar: lookup
  29. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification.. Science 2011 Oct 28;334(6055):521-4.
    pubmed: 21940861doi: 10.1126/science.1211028google scholar: lookup
  30. Miller-Butterworth CM, Murphy WJ, O'Brien SJ, Jacobs DS, Springer MS, Teeling EC. A family matter: conclusive resolution of the taxonomic position of the long-fingered bats, miniopterus.. Mol Biol Evol 2007 Jul;24(7):1553-61.
    pubmed: 17449895doi: 10.1093/molbev/msm076google scholar: lookup
  31. Mitra R, Li X, Kapusta A, Mayhew D, Mitra RD, Feschotte C, Craig NL. Functional characterization of piggyBat from the bat Myotis lucifugus unveils an active mammalian DNA transposon.. Proc Natl Acad Sci U S A 2013 Jan 2;110(1):234-9.
    pmc: PMC3538221pubmed: 23248290doi: 10.1073/pnas.1217548110google scholar: lookup
  32. Mourier T. Retrotransposon-centered analysis of piRNA targeting shows a shift from active to passive retrotransposon transcription in developing mouse testes.. BMC Genomics 2011 Sep 1;12:440.
    pmc: PMC3175481pubmed: 21884594doi: 10.1186/1471-2164-12-440google scholar: lookup
  33. O'Donnell KA, Boeke JD. Mighty Piwis defend the germline against genome intruders.. Cell 2007 Apr 6;129(1):37-44.
    pmc: PMC4122227pubmed: 17418784doi: 10.1016/j.cell.2007.03.028google scholar: lookup
  34. Pagán HJ, Macas J, Novák P, McCulloch ES, Stevens RD, Ray DA. Survey sequencing reveals elevated DNA transposon activity, novel elements, and variation in repetitive landscapes among vesper bats.. Genome Biol Evol 2012;4(4):575-85.
    pmc: PMC3342881pubmed: 22491057doi: 10.1093/gbe/evs038google scholar: lookup
  35. Platt RN 2nd, Vandewege MW, Kern C, Schmidt CJ, Hoffmann FG, Ray DA. Large numbers of novel miRNAs originate from DNA transposons and are coincident with a large species radiation in bats.. Mol Biol Evol 2014 Jun;31(6):1536-45.
    pubmed: 24692655doi: 10.1093/molbev/msu112google scholar: lookup
  36. Pritham EJ, Feschotte C. Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus.. Proc Natl Acad Sci U S A 2007 Feb 6;104(6):1895-900.
    pmc: PMC1794268pubmed: 17261799doi: 10.1073/pnas.0609601104google scholar: lookup
  37. Ray DA, Feschotte C, Pagan HJ, Smith JD, Pritham EJ, Arensburger P, Atkinson PW, Craig NL. Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus.. Genome Res 2008 May;18(5):717-28.
    pmc: PMC2336803pubmed: 18340040doi: 10.1101/gr.071886.107google scholar: lookup
  38. Ray DA, Pagan HJ, Thompson ML, Stevens RD. Bats with hATs: evidence for recent DNA transposon activity in genus Myotis.. Mol Biol Evol 2007 Mar;24(3):632-9.
    pubmed: 17150974doi: 10.1093/molbev/msl192google scholar: lookup
  39. Reuter M, Berninger P, Chuma S, Shah H, Hosokawa M, Funaya C, Antony C, Sachidanandam R, Pillai RS. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing.. Nature 2011 Nov 27;480(7376):264-7.
    pubmed: 22121019doi: 10.1038/nature10672google scholar: lookup
  40. Rosenkranz D, Rudloff S, Bastuck K, Ketting RF, Zischler H. Tupaia small RNAs provide insights into function and evolution of RNAi-based transposon defense in mammals.. RNA 2015 May;21(5):911-22.
    pmc: PMC4408798pubmed: 25802409doi: 10.1261/rna.048603.114google scholar: lookup
  41. Saito K, Siomi MC. Small RNA-mediated quiescence of transposable elements in animals.. Dev Cell 2010 Nov 16;19(5):687-97.
    pubmed: 21074719doi: 10.1016/j.devcel.2010.10.011google scholar: lookup
  42. Sen SK, Han K, Wang J, Lee J, Wang H, Callinan PA, Dyer M, Cordaux R, Liang P, Batzer MA. Human genomic deletions mediated by recombination between Alu elements.. Am J Hum Genet 2006 Jul;79(1):41-53.
    pmc: PMC1474114pubmed: 16773564doi: 10.1086/504600google scholar: lookup
  43. Siomi MC, Sato K, Pezic D, Aravin AA. PIWI-interacting small RNAs: the vanguard of genome defence.. Nat Rev Mol Cell Biol 2011 Apr;12(4):246-58.
    pubmed: 21427766doi: 10.1038/nrm3089google scholar: lookup
  44. Thomas J, Phillips CD, Baker RJ, Pritham EJ. Rolling-circle transposons catalyze genomic innovation in a mammalian lineage.. Genome Biol Evol 2014 Sep 14;6(10):2595-610.
    pmc: PMC4224331pubmed: 25223768doi: 10.1093/gbe/evu204google scholar: lookup
  45. Yan Z, Hu HY, Jiang X, Maierhofer V, Neb E, He L, Hu Y, Hu H, Li N, Chen W, Khaitovich P. Widespread expression of piRNA-like molecules in somatic tissues.. Nucleic Acids Res 2011 Aug;39(15):6596-607.
    pmc: PMC3159465pubmed: 21546553doi: 10.1093/nar/gkr298google scholar: lookup
  46. Yohn CT, Jiang Z, McGrath SD, Hayden KE, Khaitovich P, Johnson ME, Eichler MY, McPherson JD, Zhao S, Pääbo S, Eichler EE. Lineage-specific expansions of retroviral insertions within the genomes of African great apes but not humans and orangutans.. PLoS Biol 2005 Apr;3(4):e110.
    pmc: PMC1054887pubmed: 15737067doi: 10.1371/journal.pbio.0030110google scholar: lookup

Citations

This article has been cited 18 times.
  1. Wang J, Yuan L, Tang J, Liu J, Sun C, Itgen MW, Chen G, Sessions SK, Zhang G, Mueller RL. Transposable element and host silencing activity in gigantic genomes. Front Cell Dev Biol 2023;11:1124374.
    doi: 10.3389/fcell.2023.1124374pubmed: 36910142google scholar: lookup
  2. Soares SC, Eler ES, E Silva CEF, da Silva MNF, Araújo NP, Svartman M, Feldberg E. LINE-1 and SINE-B1 mapping and genome diversification in Proechimys species (Rodentia: Echimyidae). Life Sci Alliance 2022 Jun;5(6).
    doi: 10.26508/lsa.202101104pubmed: 35304430google scholar: lookup
  3. Suda K, Hayashi SR, Tamura K, Takamatsu N, Ito M. Activation of DNA Transposons and Evolution of piRNA Genes Through Interspecific Hybridization in Xenopus Frogs. Front Genet 2022;13:766424.
    doi: 10.3389/fgene.2022.766424pubmed: 35173768google scholar: lookup
  4. Vandewege MW, Patt RN 2nd, Merriman DK, Ray DA, Hoffmann FG. The PIWI/piRNA response is relaxed in a rodent that lacks mobilizing transposable elements. RNA 2022 Apr;28(4):609-621.
    doi: 10.1261/rna.078862.121pubmed: 35064043google scholar: lookup
  5. Ghosh B, Sarkar A, Mondal S, Bhattacharya N, Khatua S, Ghosh Z. piRNAQuest V.2: an updated resource for searching through the piRNAome of multiple species. RNA Biol 2022;19(1):12-25.
    doi: 10.1080/15476286.2021.2010960pubmed: 34965192google scholar: lookup
  6. Huang S, Yoshitake K, Asakawa S. A Review of Discovery Profiling of PIWI-Interacting RNAs and Their Diverse Functions in Metazoans. Int J Mol Sci 2021 Oct 16;22(20).
    doi: 10.3390/ijms222011166pubmed: 34681826google scholar: lookup
  7. Mastora E, Christodoulaki A, Papageorgiou K, Zikopoulos A, Georgiou I. Expression of Retroelements in Mammalian Gametes and Embryos. In Vivo 2021 Jul-Aug;35(4):1921-1927.
    doi: 10.21873/invivo.12458pubmed: 34182464google scholar: lookup
  8. Palacios-Gimenez OM, Koelman J, Palmada-Flores M, Bradford TM, Jones KK, Cooper SJB, Kawakami T, Suh A. Comparative analysis of morabine grasshopper genomes reveals highly abundant transposable elements and rapidly proliferating satellite DNA repeats. BMC Biol 2020 Dec 21;18(1):199.
    doi: 10.1186/s12915-020-00925-xpubmed: 33349252google scholar: lookup
  9. Kelleher ES, Barbash DA, Blumenstiel JP. Taming the Turmoil Within: New Insights on the Containment of Transposable Elements. Trends Genet 2020 Jul;36(7):474-489.
    doi: 10.1016/j.tig.2020.04.007pubmed: 32473745google scholar: lookup
  10. Pasquesi GIM, Perry BW, Vandewege MW, Ruggiero RP, Schield DR, Castoe TA. Vertebrate Lineages Exhibit Diverse Patterns of Transposable Element Regulation and Expression across Tissues. Genome Biol Evol 2020 May 1;12(5):506-521.
    doi: 10.1093/gbe/evaa068pubmed: 32271917google scholar: lookup
  11. Platt RN 2nd, Vandewege MW, Ray DA. Mammalian transposable elements and their impacts on genome evolution. Chromosome Res 2018 Mar;26(1-2):25-43.
    doi: 10.1007/s10577-017-9570-zpubmed: 29392473google scholar: lookup
  12. Singh G, Roy J, Rout P, Mallick B. Genome-wide profiling of the PIWI-interacting RNA-mRNA regulatory networks in epithelial ovarian cancers. PLoS One 2018;13(1):e0190485.
    doi: 10.1371/journal.pone.0190485pubmed: 29320577google scholar: lookup
  13. Gainetdinov I, Skvortsova Y, Kondratieva S, Funikov S, Azhikina T. Two modes of targeting transposable elements by piRNA pathway in human testis. RNA 2017 Nov;23(11):1614-1625.
    doi: 10.1261/rna.060939.117pubmed: 28842508google scholar: lookup
  14. Platt RN 2nd, Mangum SF, Ray DA. Pinpointing the vesper bat transposon revolution using the Miniopterus natalensis genome. Mob DNA 2016;7:12.
    doi: 10.1186/s13100-016-0071-ypubmed: 27489570google scholar: lookup
  15. Cai Y, Huang S, Dong Y, Li S, Jin X. PIWI-Interacting RNAs in brain health and disease: biogenesis, mechanisms, and therapeutic horizons. Psychopharmacology (Berl) 2025 Nov 3;.
    doi: 10.1007/s00213-025-06958-wpubmed: 41182353google scholar: lookup
  16. Huang S, Yoshitake K, Kinoshita S, Asakawa S. Transcriptional landscape of small non-coding RNAs reveals diversity of categories and functions in molluscs. RNA Biol 2024 Jan;21(1):1-13.
    doi: 10.1080/15476286.2024.2348893pubmed: 38693614google scholar: lookup
  17. Huang Y, Lee YCG. Blessing or curse: how the epigenetic resolution of host-transposable element conflicts shapes their evolutionary dynamics. Proc Biol Sci 2024 Apr 10;291(2020):20232775.
    doi: 10.1098/rspb.2023.2775pubmed: 38593848google scholar: lookup
  18. Wu Z, Yu X, Zhang S, He Y, Guo W. Novel roles of PIWI proteins and PIWI-interacting RNAs in human health and diseases. Cell Commun Signal 2023 Nov 29;21(1):343.
    doi: 10.1186/s12964-023-01368-xpubmed: 38031146google scholar: lookup
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