Long Non-Coding RNA Expression Profiling of Mouse Testis during Postnatal Development

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Sun, Jin ^a   Lin, Yi ^c   Wu, Ji ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b NINGXIA MEDICAL UNIVERSITY   (China)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; STEM CELL FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX3; TRANSCRIPTION FACTOR SOX9; WT1 PROTEIN; MICRORNA;

ADULT ANIMAL; ANIMAL TISSUE; ARTICLE; C KIT GENE; CONTROLLED STUDY; EPIGENETICS; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC CODE; LHX1 GENE; MALE; MICROARRAY ANALYSIS; MOLECULAR EVOLUTION; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OVOL1 GENE; OVOL2 GENE; PLZF GENE; POSTNATAL DEVELOPMENT; PRM1 GENE; PRM2 GENE; PROMOTER REGION; SOX3 GENE; SOX9 GENE; SPERMATOGENESIS; SYCP2 GENE; TESTIS DEVELOPMENT; WT1 GENE; ANIMAL; CHROMOSOME; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; TESTIS;

ADULT; AGED; CASE-CONTROL STUDIES; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LUNG NEOPLASMS; MALE; MESOTHELIOMA; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLEURAL NEOPLASMS; RNA, LONG NONCODING; ROC CURVE; SURVIVAL ANALYSIS; UP-REGULATION; ANIMALS; ANIMALS, NEWBORN; CHROMOSOMES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICRORNAS; TESTIS;

EID: 84885404224     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075750     Document Type: Article

References (97)

1. Hecht NB, (1998) Molecular mechanisms of male germ cell differentiation. Bioessays 20: 555-561.
2. Dym M, (1994) Spermatogonial stem cells of the testis. Proc Natl Acad Sci U S A 91: 11287-11289.
3. Sha J, Zhou Z, Li J, Yin L, Yang H, et al. (2002) Identification of testis development and spermatogenesis-related genes in human and mouse testes using cDNA arrays. Mol Hum Reprod 8: 511-517.
4. Pang AL, Taylor HC, Johnson W, Alexander S, Chen Y, et al. (2003) Identification of differentially expressed genes in mouse spermatogenesis. J Androl 24: 899-911.
5. Guo X, Shen J, Xia Z, Zhang R, Zhang P, et al. (2010) Proteomic analysis of proteins involved in spermiogenesis in mouse. J Proteome Res 9: 1246-1256.
6. Yan N, Lu Y, Sun H, Tao D, Zhang S, et al. (2007) A microarray for microRNA profiling in mouse testis tissues. Reproduction 134: 73-79.
7. Gan H, Lin X, Zhang Z, Zhang W, Liao S, et al. (2011) piRNA profiling during specific stages of mouse spermatogenesis. RNA 17: 1191-1203.
8. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, et al. (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316: 1484-1488.
9. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, et al. (2005) The transcriptional landscape of the mammalian genome. Science 309: 1559-1563.
10. Guttman M, Amit I, Garber M, French C, Lin MF, et al. (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458: 223-227.
11. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, et al. (2012) Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 22: 577-591.
12. Pang KC, Dinger ME, Mercer TR, Malquori L, Grimmond SM, et al. (2009) Genome-wide identification of long noncoding RNAs in CD8+ T cells. J Immunol 182: 7738-7748.
13. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS, (2008) Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci U S A 105: 716-721.
14. Pang KC, Frith MC, Mattick JS, (2006) Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genet 22: 1-5.
15. Struhl K, (2007) Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat Struct Mol Biol 14: 103-105.
16. Mattick JS, (2011) Long noncoding RNAs in cell and developmental biology. Semin Cell Dev Biol 22: 327.
17. Mattick JS, (2011) The central role of RNA in human development and cognition. FEBS Lett 585: 1600-1616.
18. Wapinski O, Chang HY, (2011) Long noncoding RNAs and human disease. Trends Cell Biol 21: 354-361.
19. Wang KC, Chang HY, (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43: 904-914.
20. Rinn JL, Chang HY, (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81: 145-166.
21. Lee T-L, Cheung A-H, Rennert O, Chan W-Y (2011) RNA Expression in Male Germ Cells During Spermatogenesis (Male Germ Cell Transcriptome). In: Zini A, Agarwal A, editors. Sperm Chromatin. New York, NY: Springer. pp. 107-121.
22. Anguera MC, Ma W, Clift D, Namekawa S, Kelleher RJ 3rd, et al. (2011) Tsx produces a long noncoding RNA and has general functions in the germline, stem cells, and brain. PLoS Genet 7: e1002248.
23. Arun G, Akhade VS, Donakonda S, Rao MR, (2012) mrhl RNA, a long noncoding RNA, negatively regulates Wnt signaling through its protein partner Ddx5/p68 in mouse spermatogonial cells. Mol Cell Biol 32: 3140-3152.
24. Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, et al. (2008) Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 18: 1433-1445.
25. Mercer TR, Qureshi IA, Gokhan S, Dinger ME, Li G, et al. (2010) Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation. BMC Neurosci 11: 14.
26. Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP, (2011) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147: 1537-1550.
27. Rackham O, Shearwood AM, Mercer TR, Davies SM, Mattick JS, et al. (2011) Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins. RNA 17: 2085-2093.
28. Spiess AN, Walther N, Muller N, Balvers M, Hansis C, et al. (2003) SPEER-a new family of testis-specific genes from the mouse. Biol Reprod 68: 2044-2054.
29. Vemuganti SA, Bell TA, Scarlett CO, Parker CE, de Villena FP, et al. (2007) Three male germline-specific aldolase A isozymes are generated by alternative splicing and retrotransposition. Dev Biol 309: 18-31.
30. Davis TL, Trasler JM, Moss SB, Yang GJ, Bartolomei MS, (1999) Acquisition of the H19 methylation imprint occurs differentially on the parental alleles during spermatogenesis. Genomics 58: 18-28.
31. Davis TL, Yang GJ, McCarrey JR, Bartolomei MS, (2000) The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet 9: 2885-2894.
32. Wang PJ, McCarrey JR, Yang F, Page DC, (2001) An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27: 422-426.
33. Kapranov P, Drenkow J, Cheng J, Long J, Helt G, et al. (2005) Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays. Genome Res 15: 987-997.
34. Engstrom PG, Suzuki H, Ninomiya N, Akalin A, Sessa L, et al. (2006) Complex Loci in human and mouse genomes. PLoS Genet 2: e47.
35. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, et al. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
36. Yu W, Gius D, Onyango P, Muldoon-Jacobs K, Karp J, et al. (2008) Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 451: 202-206.
37. Kotake Y, Nakagawa T, Kitagawa K, Suzuki S, Liu N, et al. (2011) Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 30: 1956-1962.
38. Wang X, Arai S, Song X, Reichart D, Du K, et al. (2008) Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 454: 126-130.
39. Lee J, Kanatsu-Shinohara M, Morimoto H, Kazuki Y, Takashima S, et al. (2009) Genetic reconstruction of mouse spermatogonial stem cell self-renewal in vitro by Ras-cyclin D2 activation. Cell Stem Cell 5: 76-86.
40. Rosok O, Sioud M, (2004) Systematic identification of sense-antisense transcripts in mammalian cells. Nat Biotechnol 22: 104-108.
41. Okada Y, Tashiro C, Numata K, Watanabe K, Nakaoka H, et al. (2008) Comparative expression analysis uncovers novel features of endogenous antisense transcription. Hum Mol Genet 17: 1631-1640.
42. Faghihi MA, Wahlestedt C, (2009) Regulatory roles of natural antisense transcripts. Nature Reviews Molecular Cell Biology 10: 637-643.
43. Yang F, De La Fuente R, Leu NA, Baumann C, McLaughlin KJ, et al. (2006) Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J Cell Biol 173: 497-507.
44. Reis EM, Louro R, Nakaya HI, Verjovski-Almeida S, (2005) As antisense RNA gets intronic. OMICS 9: 2-12.
45. Louro R, El-Jundi T, Nakaya HI, Reis EM, Verjovski-Almeida S, (2008) Conserved tissue expression signatures of intronic noncoding RNAs transcribed from human and mouse loci. Genomics 92: 18-25.
46. Louro R, Smirnova AS, Verjovski-Almeida S, (2009) Long intronic noncoding RNA transcription: expression noise or expression choice? Genomics 93: 291-298.
47. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, et al. (2004) Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36: 653-659.
48. Deng Y, Nie DS, Wang J, Tan XJ, Nie ZY, et al. (2005) Molecular cloning of MSRG-11 gene related to apoptosis of mouse spermatogenic cells. Acta Biochim Biophys Sin (Shanghai) 37: 159-166.
49. Nie DS, Liu Y, Juan H, Yang X, (2013) Overexpression of human SPATA17 protein induces germ cell apoptosis in transgenic male mice. Mol Biol Rep 40: 1905-1910.
50. Trinklein ND, Aldred SF, Hartman SJ, Schroeder DI, Otillar RP, et al. (2004) An abundance of bidirectional promoters in the human genome. Genome Res 14: 62-66.
51. Sigova AA, Mullen AC, Molinie B, Gupta S, Orlando DA, et al. (2013) Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. Proc Natl Acad Sci U S A 110: 2876-2881.
52. Kalitsis P, Saffery R, (2009) Inherent promoter bidirectionality facilitates maintenance of sequence integrity and transcription of parasitic DNA in mammalian genomes. BMC Genomics 10: 498.
53. Morris KV, Santoso S, Turner AM, Pastori C, Hawkins PG, (2008) Bidirectional transcription directs both transcriptional gene activation and suppression in human cells. PLoS Genet 4: e1000258.
54. Lee JY, Khan AA, Min H, Wang X, Kim MH, (2012) Identification and characterization of a noncoding RNA at the mouse Pcna locus. Mol Cells 33: 111-116.
55. Deng W, Lin H, (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2: 819-830.
56. Takeuchi A, Mishina Y, Miyaishi O, Kojima E, Hasegawa T, et al. (2003) Heterozygosity with respect to Zfp148 causes complete loss of fetal germ cells during mouse embryogenesis. Nat Genet 33: 172-176.
57. Nam JW, Bartel DP, (2012) Long noncoding RNAs in C. elegans. Genome Res 22: 2529-2540.
58. Liu J, Jung C, Xu J, Wang H, Deng S, et al. (2012) Genome-Wide Analysis Uncovers Regulation of Long Intergenic Noncoding RNAs in Arabidopsis. Plant Cell 24: 4333-4345.
59. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, et al. (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25: 1915-1927.
60. Tsai MC, Spitale RC, Chang HY, (2011) Long intergenic noncoding RNAs: new links in cancer progression. Cancer Res 71: 3-7.
61. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, et al. (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472: 120-124.
62. Schmidt JA, Avarbock MR, Tobias JW, Brinster RL, (2009) Identification of glial cell line-derived neurotrophic factor-regulated genes important for spermatogonial stem cell self-renewal in the rat. Biol Reprod 81: 56-66.
63. He S, Su H, Liu C, Skogerbo G, He H, et al. (2008) MicroRNA-encoding long non-coding RNAs. BMC Genomics 9: 236.
64. Fabian MR, Sonenberg N, Filipowicz W, (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: 351-379.
65. Hansen TB, Wiklund ED, Bramsen JB, Villadsen SB, Statham AL, et al. (2011) miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J 30: 4414-4422.
66. Cai X, Cullen BR, (2007) The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13: 313-316.
67. Ro S, Park C, Sanders KM, McCarrey JR, Yan W, (2007) Cloning and expression profiling of testis-expressed microRNAs. Dev Biol 311: 592-602.
68. Zamudio NM, Chong S, O'Bryan MK, (2008) Epigenetic regulation in male germ cells. Reproduction 136: 131-146.
69. Wu SC, Kallin EM, Zhang Y, (2010) Role of H3K27 methylation in the regulation of lncRNA expression. Cell Res 20: 1109-1116.
70. Sandoval J, Heyn H, Moran S, Serra-Musach J, Pujana MA, et al. (2011) Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics 6: 692-702.
71. Ponjavic J, Ponting CP, Lunter G, (2007) Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res 17: 556-565.
72. Bird A, (1992) The essentials of DNA methylation. Cell 70: 5-8.
73. Saxonov S, Berg P, Brutlag DL, (2006) A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci U S A 103: 1412-1417.
74. Nottke A, Colaiacovo MP, Shi Y, (2009) Developmental roles of the histone lysine demethylases. Development 136: 879-889.
75. Martin C, Zhang Y, (2005) The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 6: 838-849.
76. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
77. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
78. Marques AC, Ponting CP, (2009) Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness. Genome Biol 10: R124.
79. Chodroff RA, Goodstadt L, Sirey TM, Oliver PL, Davies KE, et al. (2010) Long noncoding RNA genes: conservation of sequence and brain expression among diverse amniotes. Genome Biol 11: R72.
80. Meola N, Pizzo M, Alfano G, Surace EM, Banfi S, (2012) The long noncoding RNA Vax2os1 controls the cell cycle progression of photoreceptor progenitors in the mouse retina. RNA 18: 111-123.
81. Askarian-Amiri ME, Crawford J, French JD, Smart CE, Smith MA, et al. (2011) SNORD-host RNA Zfas1 is a regulator of mammary development and a potential marker for breast cancer. RNA 17: 878-891.
82. Schonrock N, Harvey RP, Mattick JS, (2012) Long Noncoding RNAs in Cardiac Development and Pathophysiology. Circ Res 111: 1349-1362.
83. Klattenhoff CA, Scheuermann JC, Surface LE, Bradley RK, Fields PA, et al. (2013) Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell 152: 570-583.
84. Roberts KA, Abraira VE, Tucker AF, Goodrich LV, Andrews NC, (2012) Mutation of Rubie, a novel long non-coding RNA located upstream of Bmp4, causes vestibular malformation in mice. PLoS One 7: e29495.
85. Kutter C, Watt S, Stefflova K, Wilson MD, Goncalves A, et al. (2012) Rapid turnover of long noncoding RNAs and the evolution of gene expression. PLoS Genet 8: e1002841.
86. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, et al. (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22: 1775-1789.
87. Mercer TR, Dinger ME, Mattick JS, (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10: 155-159.
88. Girard A, Sachidanandam R, Hannon GJ, Carmell MA, (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202.
89. Ponjavic J, Oliver PL, Lunter G, Ponting CP, (2009) Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet 5: e1000617.
90. Munoz MJ, de la Mata M, Kornblihtt AR, (2010) The carboxy terminal domain of RNA polymerase II and alternative splicing. Trends Biochem Sci 35: 497-504.
91. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, et al. (2010) Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 40: 939-953.
92. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT, (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750-756.
93. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, et al. (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329: 689-693.
94. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
95. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
96. Gardiner-Garden M, Frommer M, (1987) CpG islands in vertebrate genomes. J Mol Biol 196: 261-282.
97. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.