Expression profiling reveals developmentally regulated lncRNA repertoire in the mouse male germline

Biology of Reproduction

Volumn 89, Issue 5, 2013, Pages

  Bao, Jianqiang ^b   Wu, Jingwen ^b,c   Schuster, Andrew S ^b   Hennig, Grant W ^b   Yan, Wei ^a  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

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

^c Shanghai Key Laboratory for Reproductive Medicine   (China)

Author keywords

Epigenetics; Fertility; Germ cell; Reproduction; Spermatogenesis

Indexed keywords

LARGE NONCODING RNA; LONG UNTRANSLATED RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; FEMALE; FETUS; GENE CLUSTER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LOCATION; GERM CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TESTIS DEVELOPMENT; UPREGULATION;

EPIGENETICS; FERTILITY; GERM CELL; REPRODUCTION; SPERMATOGENESIS;

ANIMALS; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; MALE; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; RNA, LONG NONCODING; SPERMATOGENESIS; SPERMATOZOA;

EID: 84899084041     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.113308     Document Type: Article

References (58)

1. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007; 447:799-816.
2. Pennisi E. ENCODE project writes eulogy for junk DNA. Science 2012; 337:1159-1161.
3. The ENCODE Project Consortium. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 2004; 306:636-640.
4. Kaikkonen MU, Lam MT, Glass CK. Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc Res 2011; 90:430-440.
5. Ng K, Pullirsch D, Leeb M, Wutz A. Xist and the order of silencing. EMBO Rep 2007; 8:34-39.
6. Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell 2009; 136:629-641.
7. Gabory A, Jammes H, Dandolo L. The H19 locus: role of an imprinted non-coding RNA in growth and development. Bioessays 2010; 32: 473-480.
8. Kwong WY, Miller DJ, Ursell E, Wild AE, Wilkins AP, Osmond C, Anthony FW, Fleming TP. Imprinted gene expression in the rat embryofetal axis is altered in response to periconceptional maternal low protein diet. Reproduction 2006; 132:265-277.
9. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010; 464:1071-1076.
10. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY. Long noncoding RNA as modular scaffold of histone modification complexes. Science 2010; 329:689-693.
11. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007; 129:1311-1323.
12. An S, Song JJ. The coded functions of noncoding RNAs for gene regulation. Mol Cells 2011; 31:491-496.
13. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011; 12: 861-874.
14. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 2009; 106:11667-11672.
15. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 2008; 9: 129-140.
16. Lees-Murdock DJ, Walsh CP. DNA methylation reprogramming in the germ line. Epigenetics 2008; 3:5-13.
17. Koh FM, Sachs M, Guzman-Ayala M, Ramalho-Santos M. Parallel gateways to pluripotency: open chromatin in stem cells and development. Curr Opin Genet Dev 2010; 20:492-499.
18. Hermo L, Pelletier RM, Cyr DG, Smith CE. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes. Microsc Res Tech 2010; 73:241-278.
19. Turner JM. Meiotic sex chromosome inactivation. Development 2007; 134:1823-1831.
20. Yan W, McCarrey JR. Sex chromosome inactivation in the male. Epigenetics 2009; 4:452-456.
21. Yan W. Male infertility caused by spermiogenic defects: lessons from gene knockouts. Mol Cell Endocrinol 2009; 306:24-32.
22. Carrell DT, Hammoud SS. The human sperm epigenome and its potential role in embryonic development. Mol Hum Reprod 2010; 16:37-47.
23. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, Roloff TC, Beisel C, Schubeler D, Stadler MB, Peters AH. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 2010; 17:679-687.
24. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. Distinctive chromatin in human sperm packages genes for embryo development. Nature 2009; 460:473-478.
25. Batista PJ, Chang HY. Long noncoding RNAs: cellular address codes in development and disease. Cell 2013; 152:1298-1307.
26. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell 2011; 43:904-914.
27. Song R, Ro S, Michaels JD, Park C, McCarrey JR, Yan W. Many Xlinked microRNAs escape meiotic sex chromosome inactivation. Nat Genet 2009; 41:488-493.
28. Wu Q, Song R, Ortogero N, Zheng H, Evanoff R, Small CL, Griswold MD, Namekawa SH, Royo H, Turner JM, Yan W. The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis. J Biol Chem 2012; 287:25173-25190.
29. Song R, Hennig GW, Wu Q, Jose C, Zheng H, Yan W. Male germ cells express abundant endogenous siRNAs. Proc Natl Acad Sci U S A 2011; 108:13159-13164.
30. Papaioannou MD, Pitetti JL, Ro S, Park C, Aubry F, Schaad O, Vejnar CE, Kuhne F, Descombes P, Zdobnov EM, McManus MT, Guillou F, et al. Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 2009; 326:250-259.
31. Wang F, Flanagan J, Su N, Wang LC, Bui S, Nielson A, Wu X, Vo HT, Ma XJ, Luo Y. RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues. J Mol Diagn 2012; 14:22-29.
32. Guil S, Soler M, Portela A, Carrere J, Fonalleras E, Gomez A, Villanueva A, Esteller M. Intronic RNAs mediate EZH2 regulation of epigenetic targets. Nat Struct Mol Biol 2012; 19:664-670.
33. Anguera MC, Ma W, Clift D, Namekawa S, Kelleher RJ III, Lee JT. Tsx produces a long noncoding RNA and has general functions in the germline, stem cells, and brain. PLoS Genet 2011; 7:e1002248.
34. Mulligan P, Yang F, Di Stefano L, Ji JY, Ouyang J, Nishikawa JL, Toiber D, Kulkarni M, Wang Q, Najafi-Shoushtari SH, Mostoslavsky R, Gygi SP, et al. A SIRT1-LSD1 corepressor complex regulates Notch target gene expression and development. Mol Cell 2011; 42:689-699.
35. Sparmann A, van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 2006; 6:846-856.
36. Di Stefano L, Ji JY, Moon NS, Herr A, Dyson N. Mutation of Drosophila Lsd1 disrupts H3-K4 methylation, resulting in tissue-specific defects during development. Curr Biol 2007; 17:808-812.
37. Huarte M. LncRNAs have a say in protein translation. Cell Res 2013; 23: 449-451.
38. Flynn RA, Chang HY. Active chromatin and noncoding RNAs: an intimate relationship. Curr Opin Genet Dev 2012; 22:172-178.
39. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem 2012; 81:145-166.
40. MacLean JA II, Wilkinson MF. The Rhox genes. Reproduction 2010; 140: 195-213.
41. Hogeveen KN, Sassone-Corsi P. Homeobox galore: when reproduction goes RHOX and roll. Cell 2005; 120:287-288.
42. da Rocha ST, Edwards CA, Ito M, Ogata T, Ferguson-Smith AC. Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet 2008; 24:306-316.
43. Lin SP, Coan P, da Rocha ST, Seitz H, Cavaille J, Teng PW, Takada S, Ferguson-Smith AC. Differential regulation of imprinting in the murine embryo and placenta by the Dlk1-Dio3 imprinting control region. Development 2007; 134:417-426.
44. Seitz H, Royo H, Bortolin ML, Lin SP, Ferguson-Smith AC, Cavaille J. A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res 2004; 14:1741-1748.
45. Lin SP, Youngson N, Takada S, Seitz H, Reik W, Paulsen M, Cavaille J, Ferguson-Smith AC. Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12. Nat Genet 2003; 35:97-102.
46. Beyret E, Lin H. Pinpointing the expression of piRNAs and function of the PIWI protein subfamily during spermatogenesis in the mouse. Dev Biol 2011; 355:215-226.
47. Deng W, Lin H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis.Dev Cell 2002; 2:819-830.
48. Thomson T, Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 2009; 25: 355-376.
49. Lin H. piRNAs in the germ line. Science 2007; 316:397.
50. Siomi MC, Sato K, Pezic D, Aravin AA. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 2011; 12: 246-258.
51. 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; 31:785-799.
52. Aravin AA, Bourc'his D. Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes Dev 2008; 22:970-975.
53. Lee C, Kikyo N. Strategies to identify long noncoding RNAs involved in gene regulation. Cell Biosci 2012; 2:37.
54. Guenzl PM, Barlow DP. Macro lncRNAs: a new layer of cis-regulatory information in the mammalian genome. RNA Biol 2012; 9:731-741.
55. Tay Y, Kats L, Salmena L, Weiss D, Tan SM, Ala U, Karreth F, Poliseno L, Provero P, Di Cunto F, Lieberman J, Rigoutsos I, et al. Codingindependent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 2011; 147:344-357.
56. Yoon JH, Abdelmohsen K, Srikantan S, Yang X, Martindale JL, De S, Huarte M, Zhan M, Becker KG, Gorospe M. LincRNA-p21 suppresses target mRNA translation. Mol Cell 2012; 47:648-655.
57. Liu X, Li D, Zhang W, Guo M, Zhan Q. Long non-coding RNA gadd7 interacts with TDP-43 and regulates Cdk6 mRNA decay. EMBO J 2012; 31:4415-4427.
58. Shamovsky I, Nudler E. Gene control by large noncoding RNAs. Sci STKE Oct 3; 2006:pe40.