Silencing of LINE-1 retrotransposons contributes to variation in small noncoding RNA expression in human cancer cells

Oncotarget

Volumn 5, Issue 12, 2014, Pages 4103-4117

  Ohms, Stephen ^a   Rangasamy, Danny ^a  

^a Australian National University   (Australia)

Author keywords

Breast cancer cells; Genome defense; MicroRNAs; PIWI interacting RNAs; Retrotransposons; Small RNAs

Indexed keywords

SMALL UNTRANSLATED RNA; MICRORNA; RETROPOSON;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC VARIABILITY; HUMAN; HUMAN CELL; LINE 1 GENE; LONG INTERSPERSED REPEAT; LONG TERMINAL REPEAT; MOLECULAR LIBRARY; OPEN READING FRAME; RETROPOSON; RNA ANALYSIS; SEQUENCE ALIGNMENT; SHORT INTERSPERSED REPEAT; TUMOR GENE; UPREGULATION; GENE EXPRESSION; GENETICS; METABOLISM;

GENE EXPRESSION; GENE SILENCING; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MICRORNAS; RETROELEMENTS; RNA, SMALL UNTRANSLATED;

EID: 84905096226     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1822     Document Type: Article

References (49)

1. Ambros V and Chen X. The regulation of genes and genomes by small RNAs. Development (Cambridge, England). 2007; 134 (9):1635-1641.
2. Ghildiyal M and Zamore PD. Small silencing RNAs: an expanding universe. Nat Rev Genet. 2009; 10 (2):94-108.
3. Peng JC and Lin H. Beyond transposons: the epigenetic and somatic functions of the Piwi-piRNA mechanism. Curr Opin Cell Biol. 2013; 25 (2):190-194.
4. Kim VN, Han J and Siomi MC. Biogenesis of small RNAs in animals. Nature reviews. 2009; 10 (2):126-139.
5. Wu L, Fan J and Belasco JG. MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci U S A. 2006; 103 (11):4034-4039.
6. Ghildiyal M, Seitz H, Horwich MD, Li C, Du T, Lee S, Xu J, Kittler EL, Zapp ML, Weng Z and Zamore PD. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science (New York, NY. 2008; 320 (5879):1077-1081.
7. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, CheloufiS, Hodges E, Anger M, Sachidanandam R, Schultz RM and Hannon GJ. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature. 2008; 453 (7194):534-538.
8. Okamura K, Balla S, Martin R, Liu N and Lai EC. Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nature structural & molecular biology. 2008; 15(9):998.
9. Girard A, Sachidanandam R, Hannon GJ and Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 2006; 442 (7099):199-202.
10. Aravin AA, Hannon GJ and Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science (New York, NY. 2007; 318 (5851):761-764.
11. Fagegaltier D, Bouge AL, Berry B, Poisot E, Sismeiro O, Coppee JY, Theodore L, Voinnet O and Antoniewski C. The endogenous siRNA pathway is involved in heterochromatin formation in Drosophila. Proc Natl Acad Sci U S A. 2009; 106 (50):21258-21263.
12. Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV and Kazazian HH, Jr. Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci U S A. 2003; 100 (9):5280-5285.
13. Gasior SL, Wakeman TP, Xu B and Deininger PL. The human LINE-1 retrotransposon creates DNA double-strand breaks. Journal of molecular biology. 2006; 357 (5):1383-1393.
14. Iskow RC, McCabe MT, Mills RE, Torene S, Pittard WS, Neuwald AF, Van Meir EG, Vertino PM and Devine SE. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell. 2010; 141 (7):1253-1261.
15. Chen L, Dahlstrom JE, Chandra A, Board P and Rangasamy D. Prognostic value of LINE-1 retrotransposon expression and its subcellular localization in breast cancer. Breast Cancer Res Treat. 2012; 136 (1):129-142.
16. Esnault C, Maestre J and Heidmann T. Human LINE retrotransposons generate processed pseudogenes. Nature genetics. 2000; 24 (4):363-367.
17. Gualtieri A, Andreola F, Sciamanna I, Sinibaldi-Vallebona P, Serafino A and Spadafora C. Increased expression and copy number amplification of LINE-1 and SINE B1 retrotransposable elements in murine mammary carcinoma progression. Oncotarget. 2013; 4 (11):1882-1893.
18. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N and Imai H. Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev. 2006; 20 (13):1732-1743.
19. Huang G, Hu H, Xue X, Shen S, Gao E, Guo G, Shen X and Zhang X. Altered expression of piRNAs and their relation with clinicopathologic features of breast cancer. Clin Transl Oncol. 2013; 15 (7):563-568.
20. Chen L, Dahlstrom JE, Lee SH and Rangasamy D. Naturally occurring endo-siRNA silences LINE-1 retrotransposons in human cells through DNA methylation. Epigenetics. 2012; 7 (7):758-771.
21. Patnala R, Lee SH, Dahlstrom JE, Ohms S, Chen L, Dheen ST and Rangasamy D. Inhibition of LINE-1 retrotransposon-encoded reverse transcriptase modulates the expression of cell differentiation genes in breast cancer cells. Breast Cancer Res Treat 2014; 143(2):239-253.
22. Jordan IK, Rogozin IB, Glazko GV and Koonin EV. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 2003; 19 (2):68-72.
23. Piriyapongsa J, Marino-Ramirez L and Jordan IK. Origin and evolution of human microRNAs from transposable elements. Genetics. 2007; 176 (2):1323-1337.
24. Levy A, Sela N and Ast G. TranspoGene and microTranspoGene: transposed elements influence on the transcriptome of seven vertebrates and invertebrates. Nucleic Acids Res. 2008; 36(Database issue):D47-52.
25. Weber MJ. Mammalian small nucleolar RNAs are mobile genetic elements. PLoS genetics. 2006; 2(12):e205.
26. Luo Y and Li S. Genome-wide analyses of retrogenes derived from the human box H/ACA snoRNAs. Nucleic Acids Res. 2007; 35 (2):559-571.
27. Scott MS, Avolio F, Ono M, Lamond AI and Barton GJ. Human miRNA precursors with box H/ACA snoRNA features. PLoS Comput Biol. 2009; 5(9):e1000507.
28. Hackenberg M, Rodriguez-Ezpeleta N and Aransay AM. miRanalyzer: an update on the detection and analysis of microRNAs in high-throughput sequencing experiments. Nucleic Acids Research. 2011; 39:W132-W138.
29. Friedlander MR, Chen W, Adamidi C, Maaskola J, Einspanier R, Knespel S and Rajewsky N. Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol. 2008; 26 (4):407-415.
30. Sai Lakshmi S and Agrawal S. piRNABank: a web resource on classified and clustered Piwi-interacting RNAs. Nucleic Acids Res. 2008; 36(Database issue):D173-177.
31. Yang JH, Shao P, Zhou H, Chen YQ and Qu LH. deepBase: a database for deeply annotating and mining deep sequencing data. Nucleic Acids Res. 2010; 38(Database issue):D123-130.
32. Anders S and Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010; 11(10).
33. Marie-Agnès Dillies*, Andrea Rau*, Julie Aubert*, Christelle Hennequet-Antier*, Marine Jeanmougin*, Nicolas Servant*, Céline Keime*, Guillemette Marot, David Castel, Jordi Estelle, Gregory Guernec, Bernd Jagla, Luc Jouneau, Denis Laloë, Caroline Le Gall, Brigitte Schaëffer, et al. A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. BRIEFINGS IN BIOINFORMATICS. 2012.
34. Feng J, Meyer CA, Wang Q, Liu JS, Shirley Liu X and Zhang Y. GFOLD: a generalized fold change for ranking differentially expressed genes from RNA-seq data. Bioinformatics. 2012; 28 (21):2782-2788.
35. Mayr C, Hemann MT and Bartel DP. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science (New York, NY. 2007; 315 (5818):1576-1579.
36. Kuchenbauer F, Mah SM, Heuser M, McPherson A, Ruschmann J, Rouhi A, Berg T, Bullinger L, Argiropoulos B, Morin RD, Lai D, Starczynowski DT, Karsan A, Eaves CJ, Watahiki A, Wang Y, et al. Comprehensive analysis of mammalian miRNA* species and their role in myeloid cells. Blood. 2011; 118 (12):3350-3358.
37. Ruby JG, Jan CH and Bartel DP. Intronic microRNA precursors that bypass Drosha processing. Nature. 2007; 448 (7149):83-86.
38. Mei Y, Clark D and Mao L. Novel dimensions of piRNAs in cancer. Cancer Lett. 2013; 336 (1):46-52.
39. Cheng J, Deng H, Xiao B, Zhou H, Zhou F, Shen Z and Guo J. piR-823, a novel non- coding small RNA, demonstrates in vitro and in vivo tumor suppressive activity in human gastric cancer cells. Cancer Lett. 2012; 315 (1):12-17.
40. Rozenberg P, Kocsis J, Saar M, Prohaszka Z, Fust G and Fishelson Z. Elevated levels of mitochondrial mortalin and cytosolic HSP70 in blood as risk factors in patients with colorectal cancer. Int J Cancer. 2013; 133 (2):514-518.
41. Blackwell BJ, Lopez MF, Wang J, Krastins B, Sarracino D, Tollervey JR, Dobke M, Jordan IK and Lunyak VV. Protein interactions with piALU RNA indicates putative participation of retroRNA in the cell cycle, DNA repair and chromatin assembly. Mob Genet Elements. 2012; 2 (1):26-35.
42. Smit A, Green P. RepeatMasker. Available: http://www.repeatmasker.org.
43. Golden DE, Gerbasi VR and Sontheimer EJ. An inside job for siRNAs. Mol Cell. 2008; 31 (3):309-312.
44. Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T and Hammond SM. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 2006; 20 (16):2202-2207.
45. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR and Golub TR. MicroRNA expression profiles classify human cancers. Nature. 2005; 435 (7043):834-838.
46. Sciamanna I, Gualtieri A, Cossetti C, Osimo EF, Ferracin M, Macchia G, Arico E, Prosseda G, Vitullo P, Misteli T and Spadafora C. A tumor-promoting mechanism mediated by retrotransposon-encoded reverse transcriptase is active in human transformed cell lines. Oncotarget. 2013; 4 (12):2271-2287.
47. Lujambio A, Portela A, Liz J, Melo SA, Rossi S, Spizzo R, Croce CM, Calin GA and Esteller M. CpG island hypermethylation-associated silencing of non-coding RNAs transcribed from ultraconserved regions in human cancer. Oncogene. 2010:1-12.
48. Han L, Witmer PD, Casey E, Valle D and Sukumar S. DNA methylation regulates MicroRNA expression. Cancer biology & therapy. 2007; 6 (8):1284-1288.
49. Oricchio E, Sciamanna I, Beraldi R, Tolstonog GV, Schumann GG and Spadafora C. Distinct roles for LINE-1 and HERV-K retroelements in cell proliferation, differentiation and tumor progression. Oncogene. 2007; 26 (29):4226-4233.