High-resolution profiling of novel transcribed regions during rat spermatogenesis

Biology of Reproduction

Volumn 91, Issue 1, 2014, Pages

  Chalmel, Frédéric ^a   Lardenois, Aurélie ^a,d,e   Evrard, Bertrand ^a   Rolland, Antoine D ^a   Sallou, Olivier ^b   Dumargne, Marie Charlotte ^a,f   Coiffec, Isabelle ^a   Collin, Olivier ^b   Primig, Michael ^a   Jégou, Bernard ^a,c  

^a UNIVERSITÉ DE RENNES 1   (France)

^b CAMPUS DE BEAULIEU   (France)

^c EHESP SCHOOL OF PUBLIC HEALTH   (France)

^d INRA UMR 703   (France)

^e LUNAM UNIVERSITÉ   (France)

^f INSTITUT PASTEUR   (France)

Author keywords

intergenic transcripts; intronic transcripts; lncRNAs; mammalian spermatogenesis; novel transcribed regions; RNA profiling; Sertoli cells

Indexed keywords

LONG UNTRANSLATED RNA;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL POPULATION; CHROMOSOME INACTIVATION; CONTROLLED STUDY; EXON; GENE; GENE EXPRESSION PROFILING; GENE LOCUS; GENE SILENCING; GENETIC PROCEDURES; MALE; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEOTIDE SEQUENCE; PACHYTENE; PRIORITY JOURNAL; RAT; SERTOLI CELL; SEX CHROMOSOME; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS; TESTIS EXPRESSED UNANNOTATED TRANSCRIPT; ANIMAL; CYTOLOGY; DNA MICROARRAY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROCEDURES; SPERMATOZOON; SPRAGUE DAWLEY RAT;

ANIMALS; GENE EXPRESSION PROFILING; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, SPRAGUE-DAWLEY; SPERMATOGENESIS; SPERMATOZOA; TESTIS; TRANSCRIPTION, GENETIC;

EID: 84904440021     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.118166     Document Type: Article

References (86)

1. Chalmel F, Lardenois A, Evrard B, Mathieu R, Feig C, Demougin P, Gattiker A, Schulze W, Jegou B, Kirchhoff C, Primig M. Global human tissue profiling and protein network analysis reveals distinct levels of transcriptional germline-specificity and identifies target genes for male infertility. Hum Reprod 2012; 27:3233-3248.
2. Chalmel F, Rolland AD, Niederhauser-Wiederkehr C, Chung SS, Demougin P, Gattiker A, Moore J, Patard JJ, Wolgemuth DJ, Jegou B, Primig M. The conserved transcriptome in human and rodent male gametogenesis. Proc Natl Acad Sci U S A 2007; 104:8346-8351.
3. Son CG, Bilke S, Davis S, Greer BT, Wei JS, Whiteford CC, Chen QR, Cenacchi N, Khan J. Database of mRNA gene expression profiles of multiple human organs. Genome Res 2005; 15:443-450.
4. Wrobel G, Primig M. Mammalian male germ cells are fertile ground for expression profiling of sexual reproduction. Reproduction 2005; 129:1-7.
5. Eddy EM. Male germ cell gene expression. Recent Prog Horm Res 2002; 57:103-128.
6. Schlecht U, Demougin P, Koch R, Hermida L, Wiederkehr C, Descombes P, Pineau C, Jegou B, Primig M. Expression profiling of mammalian male meiosis and gametogenesis identifies novel candidate genes for roles in the regulation of fertility. Mol Biol Cell 2004; 15:1031-1043.
7. Schultz N, Hamra FK, Garbers DL. A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc Natl Acad Sci U S A 2003; 100:12201-12206.
8. Shima JE, McLean DJ, McCarrey JR, Griswold MD. The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 2004; 71:319-330.
9. Laiho A, Kotaja N, Gyenesei A, Sironen A. Transcriptome profiling of the murine testis during the first wave of spermatogenesis. PLoS One 2013; 8: e61558.
10. Soumillon M, Necsulea A, Weier M, Brawand D, Zhang X, Gu H, Barthes P, Kokkinaki M, Nef S, Gnirke A, Dym M, de Massy B, et al. Cellular source and mechanisms of high transcriptome complexity in the mammalian testis. Cell Rep 2013; 3:2179-2190.
11. Gan H, Wen L, Liao S, Lin X, Ma T, Liu J, Song CX, Wang M, He C, Han C, Tang F. Dynamics of 5-hydroxymethylcytosine during mouse spermatogenesis. Nat Commun 2013; 4:1995.
12. Margolin G, Khil PP, Kim J, Bellani MA, Camerini-Otero RD. Integrated transcriptome analysis of mouse spermatogenesis. BMC Genomics 2014; 15:39.
13. Encode Project Consortium. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 2004; 306:636-640.
14. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 2012; 22: 1775-1789.
15. Banfai B, Jia H, Khatun J, Wood E, Risk B, Gundling WE Jr, Kundaje A, Gunawardena HP, Yu Y, Xie L, Krajewski K, Strahl BD, et al. Long noncoding RNAs are rarely translated in two human cell lines. Genome Res 2012; 22:1646-1657.
16. Lander ES. Initial impact of the sequencing of the human genome. Nature 2011; 470:187-197.
17. Roberts A, Pimentel H, Trapnell C, Pachter L. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics 2011; 27:2325-2329.
18. Severin AJ, Peiffer GA, Xu WW, Hyten DL, Bucciarelli B, O'Rourke JA, Bolon YT, Grant D, Farmer AD, May GD, Vance CP, Shoemaker RC, et al. An integrative approach to genomic introgression mapping. Plant Physiol 2010; 154:3-12.
19. Hung T, Chang HY. Long noncoding RNA in genome regulation: prospects and mechanisms. RNA Biol 2010; 7:582-585.
20. Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet 2009; 10:155-159.
21. Janga SC, Vallabhaneni S. MicroRNAs as post-transcriptional machines and their interplay with cellular networks. Adv Exp Med Biol 2011; 722: 59-74.
22. Zhao Y, He S, Liu C, Ru S, Zhao H, Yang Z, Yang P, Yuan X, Sun S, Bu D, Huang J, Skogerbo G, et al. MicroRNA regulation of messenger-like noncoding RNAs: a network of mutual microRNA control. Trends Genet 2008; 24:323-327.
23. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 2011; 25: 1915-1927.
24. Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, Askarian-Amiri ME, Ru K, Solda G, Simons C, Sunkin SM, Crowe ML, et al. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 2008; 18:1433-1445.
25. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009; 458:223-227.
26. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, et al. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011; 477:295-300.
27. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL, Lander ES, et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 2010; 28:503-510.
28. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci U S A 2008; 105:716-721.
29. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, Schier AF. Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 2012; 22:577-591.
30. Ponjavic J, Oliver PL, Lunter G, Ponting CP. Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet 2009; 5:e1000617.
31. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, et al. The transcriptional landscape of the mammalian genome. Science 2005; 309:1559-1563.
32. Niazi F, Valadkhan S. Computational analysis of functional long noncoding RNAs reveals lack of peptide-coding capacity and parallels with 30 UTRs. RNA 2012; 18:825-843.
33. Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell 2009; 136:629-641.
34. Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 2009; 23:1494-1504.
35. Prensner JR, Chinnaiyan AM. The emergence of lncRNAs in cancer biology. Cancer Discov 2011; 1:391-407.
36. Iglesias-Platas I, Martin-Trujillo A, Cirillo D, Court F, Guillaumet-Adkins A, Camprubi C, Bourc'his D, Hata K, Feil R, Tartaglia G, Arnaud P, Monk D. Characterization of novel paternal ncRNAs at the Plagl1 locus, including Hymai, predicted to interact with regulators of active chromatin. PLoS One 2012; 7:e38907.
37. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, Guigo R, Shiekhattar R. Long noncoding RNAs with enhancer-like function in human cells. Cell 2010; 143:46-58.
38. Liao Q, Liu C, Yuan X, Kang S, Miao R, Xiao H, Zhao G, Luo H, Bu D, Zhao H, Skogerbo G, Wu Z, et al. Large-scale prediction of long noncoding RNA functions in a coding-non-coding gene co-expression network. Nucleic Acids Res 2011; 39:3864-3878.
39. 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.
40. Wan Y, Chang HY. HOTAIR: flight of noncoding RNAs in cancer metastasis. Cell Cycle 2010; 9:3391-3392.
41. Pontier DB, Gribnau J. Xist regulation and function explored. Hum Genet 2011; 130:223-236.
42. Xu C, Yang M, Tian J, Wang X, Li Z. MALAT-1: a long non-coding RNA and its important 30 end functional motif in colorectal cancer metastasis. Int J Oncol 2011; 39:169-175.
43. Prensner JR, Iyer MK, Balbin OA, Dhanasekaran SM, Cao Q, Brenner JC, Laxman B, Asangani IA, Grasso CS, Kominsky HD, Cao X, Jing X, et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat Biotechnol 2011; 29:742-749.
44. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M, Attardi LD, Regev A, et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 2010; 142:409-419.
45. Hung T, Wang Y, Lin MF, Koegel AK, Kotake Y, Grant GD, Horlings HM, Shah N, Umbricht C, Wang P, Kong B, Langerod A, et al. Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat Genet 2011; 43:621-629.
46. Tian D, Sun S, Lee JT. The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 2010; 143:390-403.
47. Hannon GJ, Rivas FV, Murchison EP, Steitz JA. The expanding universe of noncoding RNAs. Cold Spring Harb Symp Quant Biol 2006; 71: 551-564.
48. Chen LL, Carmichael GG. Long noncoding RNAs in mammalian cells: what, where, and why? Wiley Interdiscip Rev RNA 2010; 1:2-21.
49. Koziol MJ, Rinn JL. RNA traffic control of chromatin complexes. Curr Opin Genet Dev 2010; 20:142-148.
50. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell 2011; 43:904-914.
51. Valadkhan S, Nilsen TW. Reprogramming of the non-coding transcriptome during brain development. J Biol 2010; 9:5.
52. Pauli A, Rinn JL, Schier AF. Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet 2011; 12:136-149.
53. Bhartiya D, Kapoor S, Jalali S, Sati S, Kaushik K, Sachidanandan C, Sivasubbu S, Scaria V. Conceptual approaches for lncRNA drug discovery and future strategies. Expert Opin Drug Discov 2012; 7:503-513.
54. The Reprogenomics Viewer. http://rgv.genouest.org. Accessed 15 June 2012.
55. Dorval-Coiffec I, Delcros JG, Hakovirta H, Toppari J, Jegou B, Piquet-Pellorce C. Identification of the leukemia inhibitory factor cell targets within the rat testis. Biol Reprod 2005; 72:602-611.
56. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, et al. Ensembl 2013. Nucleic Acids Res 2013; 41:D48-55.
57. Pruitt KD, Tatusova T, Brown GR, Maglott DRNCBI. Reference sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 2012; 40:D130-135.
58. Thierry-Mieg D, Thierry-Mieg J. AceView: a comprehensive cDNAsupported gene and transcripts annotation. Genome Biol 2006; 7(suppl 1): S12 11-14.
59. Meyer LR, Zweig AS, Hinrichs AS, Karolchik D, Kuhn RM, Wong M, Sloan CA, Rosenbloom KR, Roe G, Rhead B, Raney BJ, Pohl A, et al. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res 2013; 41:D64-69.
60. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010; 28:511-515.
61. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012; 7:562-578.
62. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009; 25:1105-1111.
63. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4:249-264.
64. Chalmel F, Primig M. The annotation, mapping, expression and network (AMEN) suite of tools for molecular systems biology. BMC Bioinformatics 2008; 9:86.
65. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; Article3.
66. Blanchette M, Kent WJ, Riemer C, Elnitski L, Smit AF, Roskin KM, Baertsch R, Rosenbloom K, Clawson H, Green ED, Haussler D, Miller W. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res 2004; 14, 708-715.
67. Kuhn RM, Haussler D, Kent WJ. The UCSC genome browser and associated tools. Brief Bioinform 2013; 14:144-161.
68. Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G. CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 2007; 35:W345-349.
69. Lin MF, Jungreis I, Kellis M. PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics 2011; 27:i275-282.
70. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011; 39:W29-37.
71. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000; 25:25-29.
72. Ponjavic J, Ponting CP, Lunter G. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res 2007; 17:556-565.
73. Lee CS, Ungewickell A, Bhaduri A, Qu K, Webster DE, Armstrong R, Weng WK, Aros CJ, Mah A, Chen RO, Lin M, Sundram U, et al. Transcriptome sequencing in Sezary syndrome identifies Sezary cell and mycosis fungoides-associated lncRNAs and novel transcripts. Blood 2012; 120:3288-3297.
74. Schug J, Schuller WP, Kappen C, Salbaum JM, Bucan M, Stoeckert CJ Jr. Promoter features related to tissue specificity as measured by Shannon entropy. Genome Biol 2005; 6:R33.
75. Graves JA. Sex chromosome specialization and degeneration in mammals. Cell 2006; 124:901-914.
76. Khil PP, Smirnova NA, Romanienko PJ, Camerini-Otero RD. The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 2004; 36:642-646.
77. Mueller JL, Mahadevaiah SK, Park PJ, Warburton PE, Page DC, Turner JM. The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 2008; 40:794-799.
78. Wang PJ, McCarrey JR, Yang F, Page DC. An abundance of X-linked genes expressed in spermatogonia. Nat Genet 2001; 27:422-426.
79. Meikar O, Da Ros M, Korhonen H, Kotaja N. Chromatoid body and small RNAs in male germ cells. Reproduction 2011; 142:195-209.
80. Sendler E, Johnson GD, Mao S, Goodrich RJ, Diamond MP, Hauser R, Krawetz SA. Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Res 2013; 41:4104-4117.
81. Lardenois A, Liu Y, Walther T, Chalmel F, Evrard B, Granovskaia M, Chu A, Davis RW, Steinmetz LM, Primig M. Execution of the meiotic noncoding RNA expression program and the onset of gametogenesis in yeast require the conserved exosome subunit Rrp6. Proc Natl Acad Sci U S A 2011; 108:1058-1063.
82. Lalancette C, Miller D, Li Y, Krawetz SA. Paternal contributions: new functional insights for spermatozoal RNA. J Cell Biochem 2008; 104: 1570-1579.
83. Neme R, Tautz D. Phylogenetic patterns of emergence of new genes support a model of frequent de novo evolution. BMC Genomics 2013; 14: 117.
84. Ding DQ, Okamasa K, Yamane M, Tsutsumi C, Haraguchi T, Yamamoto M, Hiraoka Y. Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis. Science 2012; 336:732-736.
85. Johnstone O, Lasko P. Translational regulation and RNA localization in Drosophila oocytes and embryos. Annu Rev Genet 2001; 35:365-406.
86. Long RM, Singer RH, Meng X, Gonzalez I, Nasmyth K, Jansen RP. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 1997; 277:383-387.