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Published in: Molecular Cancer 1/2015

Open Access 01-12-2015 | Research

Profiling of the small RNA populations in human testicular germ cell tumors shows global loss of piRNAs

Authors: TB Rounge, K Furu, RI Skotheim, TB Haugen, T Grotmol, E Enerly

Published in: Molecular Cancer | Issue 1/2015

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Abstract

Background

Small non-coding RNAs play essential roles in gene regulation, however, the interplay between RNA groups, their expression levels and deregulations in tumorigenesis requires additional exploration. In particular, a comprehensive analysis of microRNA (miRNA), PIWI-interacting RNAs (piRNAs), and tRNA-derived small RNAs in human testis and testicular germ cell tumor (TGCT) is lacking.

Results

We performed small RNA sequencing on 22 human TGCT samples from 5 histological subtypes, 3 carcinoma in situ, and 12 normal testis samples. miRNA was the most common group among the sequences 18–24 nt in length and showed histology-specific expression. In normal samples, most sequences 25–31 nucleotides in length displayed piRNA characteristics, whereas a large proportion of the sequences 32–36 nt length was derived from tRNAs. Expression analyses of the piRNA population demonstrated global loss in all TGCT subtypes compared to normal testis. In addition, three 5′ small tRNA fragments and 23 miRNAs showed significant (p < 10−6) differential expression in cancer vs normal samples.

Conclusions

We have documented significant changes in the small RNA populations in normal adult testicular tissue and TGCT samples. Although components of the same pathways might be involved in miRNA, piRNA and tRNA-derived small RNA biogenesis, our results showed that the response to the carcinogenic process differs between these pathways, suggesting independent regulation of their biogenesis. Overall, the small RNA deregulation in TGCT provides new insight into the small RNA interplay.
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Literature
1.
go back to reference Bertone P, Stolc V, Royce TE, Rozowsky JS, Urban AE, Zhu X, et al. Global identification of human transcribed sequences with genome tiling arrays. Science. 2004;306(5705):2242–6.PubMedCrossRef Bertone P, Stolc V, Royce TE, Rozowsky JS, Urban AE, Zhu X, et al. Global identification of human transcribed sequences with genome tiling arrays. Science. 2004;306(5705):2242–6.PubMedCrossRef
3.
go back to reference Farazi TA, Juranek SA, Tuschl T. The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development. 2008;135(7):1201–14.PubMedCrossRef Farazi TA, Juranek SA, Tuschl T. The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development. 2008;135(7):1201–14.PubMedCrossRef
4.
go back to reference Peters L, Meister G. Argonaute proteins: mediators of RNA silencing. Mol Cell. 2007;26(5):611–23.PubMedCrossRef Peters L, Meister G. Argonaute proteins: mediators of RNA silencing. Mol Cell. 2007;26(5):611–23.PubMedCrossRef
5.
go back to reference Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 2006;442(7099):199–202.PubMed Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 2006;442(7099):199–202.PubMed
6.
go back to reference Deng W, Lin HF. Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell. 2002;2(6):819–30.PubMedCrossRef Deng W, Lin HF. Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell. 2002;2(6):819–30.PubMedCrossRef
7.
go back to reference Hutvagner G, Simard MJ. Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol. 2008;9(1):22–32.PubMedCrossRef Hutvagner G, Simard MJ. Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol. 2008;9(1):22–32.PubMedCrossRef
8.
go back to reference Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353(17):1793–801.PubMedCrossRef Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353(17):1793–801.PubMedCrossRef
9.
go back to reference Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834–8.PubMedCrossRef Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834–8.PubMedCrossRef
10.
go back to reference Wu Q, Song R, Ortogero N, Zheng H, Evanoff R, Small CL, et al. The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis. J Biol Chem. 2012;287(30):25173–90.PubMedCentralPubMedCrossRef Wu Q, Song R, Ortogero N, Zheng H, Evanoff R, Small CL, et al. The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis. J Biol Chem. 2012;287(30):25173–90.PubMedCentralPubMedCrossRef
11.
go back to reference Smorag L, Zheng Y, Nolte J, Zechner U, Engel W, Pantakani DV. MicroRNA signature in various cell types of mouse spermatogenesis: evidence for stage-specifically expressed miRNA-221, −203 and -34b-5p mediated spermatogenesis regulation. Biol Cell. 2012;104(11):677–92.PubMedCrossRef Smorag L, Zheng Y, Nolte J, Zechner U, Engel W, Pantakani DV. MicroRNA signature in various cell types of mouse spermatogenesis: evidence for stage-specifically expressed miRNA-221, −203 and -34b-5p mediated spermatogenesis regulation. Biol Cell. 2012;104(11):677–92.PubMedCrossRef
12.
go back to reference Gillis AJM, Stoop HJ, Hersmus R, Oosterhuis JW, Sun Y, Chen C, et al. High-throughput microRNAome analysis in human germ cell tumours. J Pathol. 2007;213(3):319–28.PubMedCrossRef Gillis AJM, Stoop HJ, Hersmus R, Oosterhuis JW, Sun Y, Chen C, et al. High-throughput microRNAome analysis in human germ cell tumours. J Pathol. 2007;213(3):319–28.PubMedCrossRef
13.
go back to reference Voorhoeve PM, le Sage C, Schrier M, Gillis AJM, Stoop H, Nagel R, et al. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell. 2006;124(6):1169–81.PubMedCrossRef Voorhoeve PM, le Sage C, Schrier M, Gillis AJM, Stoop H, Nagel R, et al. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell. 2006;124(6):1169–81.PubMedCrossRef
15.
go back to reference Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature. 2006;442(7099):203–7.PubMed Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature. 2006;442(7099):203–7.PubMed
16.
go back to reference Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, et al. Characterization of the piRNA complex from rat testes. Science. 2006;313(5785):363–7.PubMedCrossRef Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, et al. Characterization of the piRNA complex from rat testes. Science. 2006;313(5785):363–7.PubMedCrossRef
18.
go back to reference Cheng J, Guo JM, Xiao BX, Miao Y, Jiang Z, Zhou H, et al. piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clin Chim Acta. 2011;412(17–18):1621–5.PubMedCrossRef Cheng J, Guo JM, Xiao BX, Miao Y, Jiang Z, Zhou H, et al. piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clin Chim Acta. 2011;412(17–18):1621–5.PubMedCrossRef
19.
go back to reference Lu Y, Li C, Zhang K, Sun H, Tao D, Liu Y, et al. Identification of piRNAs in Hela cells by massive parallel sequencing. BMB Rep. 2010;43(9):635–41.PubMedCrossRef Lu Y, Li C, Zhang K, Sun H, Tao D, Liu Y, et al. Identification of piRNAs in Hela cells by massive parallel sequencing. BMB Rep. 2010;43(9):635–41.PubMedCrossRef
20.
go back to reference Keam SP, Young PE, McCorkindale AL, Dang TH, Clancy JL, Humphreys DT, et al. The human Piwi protein Hiwi2 associates with tRNA-derived piRNAs in somatic cells. Nucleic Acids Res. 2014;42(14):8984–95.PubMedCentralPubMedCrossRef Keam SP, Young PE, McCorkindale AL, Dang TH, Clancy JL, Humphreys DT, et al. The human Piwi protein Hiwi2 associates with tRNA-derived piRNAs in somatic cells. Nucleic Acids Res. 2014;42(14):8984–95.PubMedCentralPubMedCrossRef
21.
go back to reference Yan Z, Hu HY, Jiang X, Maierhofer V, Neb E, He L, et al. Widespread expression of piRNA-like molecules in somatic tissues. Nucleic Acids Res. 2011;39(15):6596–607.PubMedCentralPubMedCrossRef Yan Z, Hu HY, Jiang X, Maierhofer V, Neb E, He L, et al. Widespread expression of piRNA-like molecules in somatic tissues. Nucleic Acids Res. 2011;39(15):6596–607.PubMedCentralPubMedCrossRef
22.
go back to reference Ishizu H, Siomi H, Siomi MC. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012;26(21):2361–73.PubMedCentralPubMedCrossRef Ishizu H, Siomi H, Siomi MC. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012;26(21):2361–73.PubMedCentralPubMedCrossRef
23.
go back to reference Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science. 2007;316(5825):744–7.PubMedCrossRef Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science. 2007;316(5825):744–7.PubMedCrossRef
24.
go back to reference Carmell MA, Girard A, van de Kant HJG, Bourc'his D, Bestor TH, de Rooij DG, et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell. 2007;12(4):503–14.PubMedCrossRef Carmell MA, Girard A, van de Kant HJG, Bourc'his D, Bestor TH, de Rooij DG, et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell. 2007;12(4):503–14.PubMedCrossRef
25.
go back to reference Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128(6):1089–103.PubMedCrossRef Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128(6):1089–103.PubMedCrossRef
26.
go back to reference Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 1998;12(23):3715–27.PubMedCentralPubMedCrossRef Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 1998;12(23):3715–27.PubMedCentralPubMedCrossRef
27.
go back to reference Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008;31(6):785–99.PubMedCentralPubMedCrossRef Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008;31(6):785–99.PubMedCentralPubMedCrossRef
28.
go back to reference Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development. 2004;131(4):839–49.PubMedCrossRef Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development. 2004;131(4):839–49.PubMedCrossRef
29.
go back to reference Thomson T, Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Review Cell Dev Biol. 2009;25:355–76.CrossRef Thomson T, Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Review Cell Dev Biol. 2009;25:355–76.CrossRef
31.
go back to reference Sobala A, Hutvagner G. Transfer RNA-derived fragments: origins, processing, and functions. Wiley Interdis Rev RNA. 2011;2(6):853–62.CrossRef Sobala A, Hutvagner G. Transfer RNA-derived fragments: origins, processing, and functions. Wiley Interdis Rev RNA. 2011;2(6):853–62.CrossRef
32.
33.
go back to reference Yamasaki S, Ivanov P, Hu GF, Anderson P. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol. 2009;185(1):35–42.PubMedCentralPubMedCrossRef Yamasaki S, Ivanov P, Hu GF, Anderson P. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol. 2009;185(1):35–42.PubMedCentralPubMedCrossRef
34.
35.
go back to reference Peng H, Shi J, Zhang Y, Zhang H, Liao S, Li W, et al. A novel class of tRNA-derived small RNAs extremely enriched in mature mouse sperm. Cell Res. 2012;22(11):1609–12.PubMedCentralPubMedCrossRef Peng H, Shi J, Zhang Y, Zhang H, Liao S, Li W, et al. A novel class of tRNA-derived small RNAs extremely enriched in mature mouse sperm. Cell Res. 2012;22(11):1609–12.PubMedCentralPubMedCrossRef
36.
go back to reference Skakkebaek NE, Berthelsen JG, Giwercman A, Muller J. Carcinoma-in-situ of the testis: possible origin from gonocytes and precursor of all types of germ cell tumours except spermatocytoma. Int J Androl. 1987;10(1):19–28.PubMedCrossRef Skakkebaek NE, Berthelsen JG, Giwercman A, Muller J. Carcinoma-in-situ of the testis: possible origin from gonocytes and precursor of all types of germ cell tumours except spermatocytoma. Int J Androl. 1987;10(1):19–28.PubMedCrossRef
37.
go back to reference Chia VM, Quraishi SM, Devesa SS, Purdue MP, Cook MB, McGlynn KA. International Trends in the Incidence of Testicular Cancer, 1973–2002. Cancer Epidem Biomar. 2010;19(5):1151–9.CrossRef Chia VM, Quraishi SM, Devesa SS, Purdue MP, Cook MB, McGlynn KA. International Trends in the Incidence of Testicular Cancer, 1973–2002. Cancer Epidem Biomar. 2010;19(5):1151–9.CrossRef
38.
go back to reference McGlynn KA, Devesa SS, Sigurdson AJ, Brown LM, Tsao L, Tarone RE. Trends in the incidence of testicular germ cell tumors in the United States. Cancer. 2003;97(1):63–70.PubMedCrossRef McGlynn KA, Devesa SS, Sigurdson AJ, Brown LM, Tsao L, Tarone RE. Trends in the incidence of testicular germ cell tumors in the United States. Cancer. 2003;97(1):63–70.PubMedCrossRef
39.
go back to reference Sonke GS, Chang S, Strom SS, Sweeney AM, Annegers JF, Sigurdson AJ. Prenatal and perinatal risk factors and testicular cancer: a hospital-based case–control study. Oncology Res. 2007;16(8):383–7. Sonke GS, Chang S, Strom SS, Sweeney AM, Annegers JF, Sigurdson AJ. Prenatal and perinatal risk factors and testicular cancer: a hospital-based case–control study. Oncology Res. 2007;16(8):383–7.
40.
go back to reference Bernstein L, Depue RH, Ross RK, Judd HL, Pike MC, Henderson BE. Higher maternal levels of free estradiol in first compared to second pregnancy: early gestational differences. J Natl Cancer Inst. 1986;76(6):1035–9.PubMed Bernstein L, Depue RH, Ross RK, Judd HL, Pike MC, Henderson BE. Higher maternal levels of free estradiol in first compared to second pregnancy: early gestational differences. J Natl Cancer Inst. 1986;76(6):1035–9.PubMed
41.
go back to reference Aschim EL, Grotmol T, Tretli S, Haugen TB. Is there an association between maternal weight and the risk of testicular cancer? An epidemiologic study of Norwegian data with emphasis on World War II. Int J Cancer. 2005;116(2):327–30.PubMedCrossRef Aschim EL, Grotmol T, Tretli S, Haugen TB. Is there an association between maternal weight and the risk of testicular cancer? An epidemiologic study of Norwegian data with emphasis on World War II. Int J Cancer. 2005;116(2):327–30.PubMedCrossRef
42.
go back to reference Kristensen DG, Nielsen JE, Jorgensen A, Skakkebaek NE, Rajpert-De Meyts E, Almstrup K. Evidence that active demethylation mechanisms maintain the genome of carcinoma in situ cells hypomethylated in the adult testis. Br J Cancer. 2013;110(3):668–78.PubMedCentralPubMedCrossRef Kristensen DG, Nielsen JE, Jorgensen A, Skakkebaek NE, Rajpert-De Meyts E, Almstrup K. Evidence that active demethylation mechanisms maintain the genome of carcinoma in situ cells hypomethylated in the adult testis. Br J Cancer. 2013;110(3):668–78.PubMedCentralPubMedCrossRef
43.
go back to reference Ferreira HJ, Heyn H, GarciaDel Muro X, Vidal A, Larriba S, Munoz C, et al. Epigenetic loss of the PIWI/piRNA machinery in human testicular tumorigenesis. Epigenetics. 2014;9(1):113–8.PubMedCentralPubMedCrossRef Ferreira HJ, Heyn H, GarciaDel Muro X, Vidal A, Larriba S, Munoz C, et al. Epigenetic loss of the PIWI/piRNA machinery in human testicular tumorigenesis. Epigenetics. 2014;9(1):113–8.PubMedCentralPubMedCrossRef
44.
go back to reference Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature. 2003;425(6956):415–9.PubMedCrossRef Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature. 2003;425(6956):415–9.PubMedCrossRef
45.
go back to reference Luteijn MJ, Ketting RF. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nature Rev Gen. 2013;14(8):523–34.CrossRef Luteijn MJ, Ketting RF. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nature Rev Gen. 2013;14(8):523–34.CrossRef
46.
47.
go back to reference Martens-Uzunova ES, Olvedy M, Jenster G. Beyond microRNA--novel RNAs derived from small non-coding RNA and their implication in cancer. Cancer Lett. 2013;340(2):201–11.PubMedCrossRef Martens-Uzunova ES, Olvedy M, Jenster G. Beyond microRNA--novel RNAs derived from small non-coding RNA and their implication in cancer. Cancer Lett. 2013;340(2):201–11.PubMedCrossRef
48.
49.
go back to reference Beyret E, Liu N, Lin H. piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism. Cell Res. 2012;22(10):1429–39.PubMedCentralPubMedCrossRef Beyret E, Liu N, Lin H. piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism. Cell Res. 2012;22(10):1429–39.PubMedCentralPubMedCrossRef
50.
go back to reference Ha H, Song J, Wang S, Kapusta A, Feschotte C, Chen KC, et al. A comprehensive analysis of piRNAs from adult human testis and their relationship with genes and mobile elements. BMC Genomics. 2014;15:545.PubMedCentralPubMedCrossRef Ha H, Song J, Wang S, Kapusta A, Feschotte C, Chen KC, et al. A comprehensive analysis of piRNAs from adult human testis and their relationship with genes and mobile elements. BMC Genomics. 2014;15:545.PubMedCentralPubMedCrossRef
51.
go back to reference Almstrup K, Leffers H, Lothe RA, Skakkebaek NE, Sonne SB, Nielsen JE, et al. Improved gene expression signature of testicular carcinoma in situ. Int J Androl. 2007;30(4):292–302. discussion 303.PubMedCrossRef Almstrup K, Leffers H, Lothe RA, Skakkebaek NE, Sonne SB, Nielsen JE, et al. Improved gene expression signature of testicular carcinoma in situ. Int J Androl. 2007;30(4):292–302. discussion 303.PubMedCrossRef
52.
go back to reference Cole C, Sobala A, Lu C, Thatcher SR, Bowman A, Brown JW, et al. Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA. 2009;15(12):2147–60.PubMedCentralPubMedCrossRef Cole C, Sobala A, Lu C, Thatcher SR, Bowman A, Brown JW, et al. Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA. 2009;15(12):2147–60.PubMedCentralPubMedCrossRef
53.
go back to reference Burroughs AM, Ando Y, de Hoon MJ, Tomaru Y, Suzuki H, Hayashizaki Y, et al. Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol. 2011;8(1):158–77.PubMedCentralPubMedCrossRef Burroughs AM, Ando Y, de Hoon MJ, Tomaru Y, Suzuki H, Hayashizaki Y, et al. Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol. 2011;8(1):158–77.PubMedCentralPubMedCrossRef
54.
55.
go back to reference Pavon-Eternod M, Gomes S, Geslain R, Dai Q, Rosner MR, Pan T. tRNA over-expression in breast cancer and functional consequences. Nucleic Acids Res. 2009;37(21):7268–80.PubMedCentralPubMedCrossRef Pavon-Eternod M, Gomes S, Geslain R, Dai Q, Rosner MR, Pan T. tRNA over-expression in breast cancer and functional consequences. Nucleic Acids Res. 2009;37(21):7268–80.PubMedCentralPubMedCrossRef
56.
go back to reference Ushida H, Kawakami T, Minami K, Chano T, Okabe H, Okada Y, et al. Methylation profile of DNA repetitive elements in human testicular germ cell tumor. Molecular Carcinog. 2012;51(9):711–22.CrossRef Ushida H, Kawakami T, Minami K, Chano T, Okabe H, Okada Y, et al. Methylation profile of DNA repetitive elements in human testicular germ cell tumor. Molecular Carcinog. 2012;51(9):711–22.CrossRef
57.
go back to reference Murray MJ, Saini HK, van Dongen S, Palmer RD, Muralidhar B, Pett MR, et al. The two most common histological subtypes of malignant germ cell tumour are distinguished by global microRNA profiles, associated with differential transcription factor expression. Mol Cancer. 2010;9:290.PubMedCentralPubMedCrossRef Murray MJ, Saini HK, van Dongen S, Palmer RD, Muralidhar B, Pett MR, et al. The two most common histological subtypes of malignant germ cell tumour are distinguished by global microRNA profiles, associated with differential transcription factor expression. Mol Cancer. 2010;9:290.PubMedCentralPubMedCrossRef
58.
go back to reference Palmer RD, Murray MJ, Saini HK, van Dongen S, Abreu-Goodger C, Muralidhar B, et al. Malignant germ cell tumors display common microRNA profiles resulting in global changes in expression of messenger RNA targets. Cancer Res. 2010;70(7):2911–23.PubMedCentralPubMedCrossRef Palmer RD, Murray MJ, Saini HK, van Dongen S, Abreu-Goodger C, Muralidhar B, et al. Malignant germ cell tumors display common microRNA profiles resulting in global changes in expression of messenger RNA targets. Cancer Res. 2010;70(7):2911–23.PubMedCentralPubMedCrossRef
59.
go back to reference Lin SL, Chang DC, Chang-Lin S, Lin CH, Wu DT, Chen DT, et al. Mir-302 reprograms human skin cancer cells into a pluripotent ES-cell-like state. RNA (New York, NY). 2008;14(10):2115–24.CrossRef Lin SL, Chang DC, Chang-Lin S, Lin CH, Wu DT, Chen DT, et al. Mir-302 reprograms human skin cancer cells into a pluripotent ES-cell-like state. RNA (New York, NY). 2008;14(10):2115–24.CrossRef
60.
go back to reference Liu L, Lian J, Zhang H, Tian H, Liang M, Yin M, et al. MicroRNA-302a sensitizes testicular embryonal carcinoma cells to cisplatin-induced cell death. J Cell Physiol. 2013;228(12):2294–304.PubMedCrossRef Liu L, Lian J, Zhang H, Tian H, Liang M, Yin M, et al. MicroRNA-302a sensitizes testicular embryonal carcinoma cells to cisplatin-induced cell death. J Cell Physiol. 2013;228(12):2294–304.PubMedCrossRef
61.
go back to reference Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10(5):593–601.PubMedCrossRef Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10(5):593–601.PubMedCrossRef
62.
go back to reference Neves R, Scheel C, Weinhold S, Honisch E, Iwaniuk KM, Trompeter HI, et al. Role of DNA methylation in miR-200c/141 cluster silencing in invasive breast cancer cells. BMC Res Notes. 2010;3:219.PubMedCentralPubMedCrossRef Neves R, Scheel C, Weinhold S, Honisch E, Iwaniuk KM, Trompeter HI, et al. Role of DNA methylation in miR-200c/141 cluster silencing in invasive breast cancer cells. BMC Res Notes. 2010;3:219.PubMedCentralPubMedCrossRef
63.
go back to reference Hu M, Xia M, Chen X, Lin Z, Xu Y, Ma Y, et al. MicroRNA-141 regulates Smad interacting protein 1 (SIP1) and inhibits migration and invasion of colorectal cancer cells. Dig Dis Sci. 2010;55(8):2365–72.PubMedCrossRef Hu M, Xia M, Chen X, Lin Z, Xu Y, Ma Y, et al. MicroRNA-141 regulates Smad interacting protein 1 (SIP1) and inhibits migration and invasion of colorectal cancer cells. Dig Dis Sci. 2010;55(8):2365–72.PubMedCrossRef
64.
65.
go back to reference Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, et al. MicroRNA signatures in human ovarian cancer. Cancer Res. 2007;67(18):8699–707.PubMedCrossRef Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, et al. MicroRNA signatures in human ovarian cancer. Cancer Res. 2007;67(18):8699–707.PubMedCrossRef
66.
go back to reference McDonald JS, Milosevic D, Reddi HV, Grebe SK, Algeciras-Schimnich A. Analysis of circulating microRNA: preanalytical and analytical challenges. Clin Chem. 2011;57(6):833–40.PubMedCrossRef McDonald JS, Milosevic D, Reddi HV, Grebe SK, Algeciras-Schimnich A. Analysis of circulating microRNA: preanalytical and analytical challenges. Clin Chem. 2011;57(6):833–40.PubMedCrossRef
67.
go back to reference Bezan A, Gerger A, Pichler M. MicroRNAs in testicular cancer: implications for pathogenesis, diagnosis, prognosis and therapy. Anticancer Res. 2014;34(6):2709–13.PubMed Bezan A, Gerger A, Pichler M. MicroRNAs in testicular cancer: implications for pathogenesis, diagnosis, prognosis and therapy. Anticancer Res. 2014;34(6):2709–13.PubMed
68.
go back to reference Dieckmann KP, Spiekermann M, Balks T, Flor I, Loning T, Bullerdiek J, et al. MicroRNAs miR-371-3 in serum as diagnostic tools in the management of testicular germ cell tumours. Br J Cancer. 2012;107(10):1754–60.PubMedCentralPubMedCrossRef Dieckmann KP, Spiekermann M, Balks T, Flor I, Loning T, Bullerdiek J, et al. MicroRNAs miR-371-3 in serum as diagnostic tools in the management of testicular germ cell tumours. Br J Cancer. 2012;107(10):1754–60.PubMedCentralPubMedCrossRef
69.
go back to reference Spiekermann M, Belge G, Winter N, Ikogho R, Balks T, Bullerdiek J, et al. MicroRNA miR-371a-3p in serum of patients with germ cell tumours: evaluations for establishing a serum biomarker. Andrology. 2015;3(2):78–84.PubMedCrossRef Spiekermann M, Belge G, Winter N, Ikogho R, Balks T, Bullerdiek J, et al. MicroRNA miR-371a-3p in serum of patients with germ cell tumours: evaluations for establishing a serum biomarker. Andrology. 2015;3(2):78–84.PubMedCrossRef
70.
go back to reference Belge G, Dieckmann KP, Spiekermann M, Balks T, Bullerdiek J. Serum levels of microRNAs miR-371-3: a novel class of serum biomarkers for testicular germ cell tumors? Eur Urol. 2012;61(5):1068–9.PubMedCrossRef Belge G, Dieckmann KP, Spiekermann M, Balks T, Bullerdiek J. Serum levels of microRNAs miR-371-3: a novel class of serum biomarkers for testicular germ cell tumors? Eur Urol. 2012;61(5):1068–9.PubMedCrossRef
71.
go back to reference Syring I, Bartels J, Holdenrieder S, Kristiansen G, Muller SC, Ellinger J. Circulating Serum miRNA (miR-367-3p, miR-371a-3p, miR-372-3p and miR-373-3p) as Biomarkers in Patients with Testicular Germ Cell Cancer. J Urol. 2015;193(1):331–7.PubMedCrossRef Syring I, Bartels J, Holdenrieder S, Kristiansen G, Muller SC, Ellinger J. Circulating Serum miRNA (miR-367-3p, miR-371a-3p, miR-372-3p and miR-373-3p) as Biomarkers in Patients with Testicular Germ Cell Cancer. J Urol. 2015;193(1):331–7.PubMedCrossRef
72.
go back to reference Skotheim RI, Lind GE, Monni O, Nesland JM, Abeler VM, Fossa SD, et al. Differentiation of human embryonal carcinomas in vitro and in vivo reveals expression profiles relevant to normal development. Cancer Res. 2005;65(13):5588–98.PubMedCrossRef Skotheim RI, Lind GE, Monni O, Nesland JM, Abeler VM, Fossa SD, et al. Differentiation of human embryonal carcinomas in vitro and in vivo reveals expression profiles relevant to normal development. Cancer Res. 2005;65(13):5588–98.PubMedCrossRef
74.
go back to reference Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 2006;34:D140–4.PubMedCentralPubMedCrossRef Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 2006;34:D140–4.PubMedCentralPubMedCrossRef
76.
go back to reference Liao Y, Smyth GK, Shi W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–30.PubMedCrossRef Liao Y, Smyth GK, Shi W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–30.PubMedCrossRef
Metadata
Title
Profiling of the small RNA populations in human testicular germ cell tumors shows global loss of piRNAs
Authors
TB Rounge
K Furu
RI Skotheim
TB Haugen
T Grotmol
E Enerly
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Molecular Cancer / Issue 1/2015
Electronic ISSN: 1476-4598
DOI
https://doi.org/10.1186/s12943-015-0411-4

Other articles of this Issue 1/2015

Molecular Cancer 1/2015 Go to the issue

Reviewer acknowledgement

Thanking our 2014 peer reviewers

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