Global characterization of the oocyte-to-embryo transition in Caenorhabditis elegans uncovers a novel mRNA clearance mechanism

EMBO Journal

Volumn 33, Issue 16, 2014, Pages 1751-1766

  Stoeckius, Marlon ^a   Grün, Dominic ^a   Kirchner, Marieluise ^a   Ayoub, Salah ^a   Torti, Francesca ^a   Piano, Fabio ^b,c   Herzog, Margareta ^a   Selbach, Matthias ^a   Rajewsky, Nikolaus ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b NEW YORK UNIVERSITY   (United States)

^c NEW YORK UNIVERSITY ABU DHABI   (United Arab Emirates)

Author keywords

Caenorhabditis elegans; embryogenesis; maternal mRNA; oocyte to embryo transition; posttranscriptional gene regulation

Indexed keywords

CAENORHABDITIS ELEGANS; EMBRYOGENESIS; MATERNAL MRNA; OOCYTE-TO-EMBRYO TRANSITION; POSTTRANSCRIPTIONAL GENE REGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; FERTILIZATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICRORNAS; OOCYTES; POLY C; PROTEOME; RNA STABILITY; RNA, MESSENGER, STORED; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

EID: 84905732318     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201488769     Document Type: Article

References (73)

1. Aanes H, Winata C, Mathavan S, (2011) Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. Genome Res 21: 1328-1338
2. Aroian RV, Field C, Pruliere G, Kenyon C, Alberts BM, (1997) Isolation of actin-associated proteins from Caenorhabditis elegans oocytes and their localization in the early embryo. EMBO J 16: 1541-1549
3. Bailey TL, Elkan C, (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 8-36
4. Bailey TL, Bodén M, Whitington T, Machanick P, (2010) The value of position-specific priors in motif discovery using MEME. BMC Bioinformatics 11: 179
5. Baugh LR, Hill AA, Slonim DK, Brown EL, Hunter CP, (2003) Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome. Development 130: 889-900
6. Bazzini AA, Lee MT, Giraldez AJ, (2012) Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science (80-.). 336: 233-237
7. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94
8. Bushati N, Stark A, Brennecke J, Cohen SM, (2008) Temporal reciprocity of miRNAs and their targets during the maternal-to-zygotic transition in Drosophila. Curr Biol 18: 501-506
9. Claycomb JM, Batista PJ, Pang K, Gu W, Vasale J, van Wolfswinkel J, Chaves DA, Shirayama M, Mitani S, Ketting RF, Conte D, Mello CC, (2009) The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 139: 123-134
10. Cox J, Mann M, (2007) Is proteomics the new genomics? Cell 130: 395-398
11. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, Olsen JV, Mann M, (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc 4: 698-705
12. Cuenca AA, Schetter A, Aceto D, Kemphues K, Seydoux G, (2003) Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130: 1255-1265
13. Cutter AD, (2008) Divergence times in Caenorhabditis and Drosophila inferred from direct estimates of the neutral mutation rate. Mol Biol Evol 25: 778-786
14. rd edn. New York, NY: Academic Press.
15. Dieckmann-Schuppert A, Schnittler HJ, (1997) A simple assay for quantification of protein in tissue sections, cell cultures, and cell homogenates, and of protein immobilized on solid surfaces. Cell Tissue Res 288: 119-126
16. Dobson AT, Raja R, Abeyta MJ, Taylor T, Shen S, Haqq C, Pera RAR, (2004) The unique transcriptome through day 3 of human preimplantation development. Hum Mol Genet 13: 1461-1470
17. Dreszer TR, Karolchik D, Zweig AS, Hinrichs AS, Raney BJ, Kuhn RM, Meyer LR, Wong M, Sloan CA, Rosenbloom KR, Roe G, Rhead B, Pohl A, Malladi VS, Li CH, Learned K, Kirkup V, Hsu F, Harte RA, Guruvadoo L, et al, (2012) The UCSC Genome Browser database: extensions and updates 2011. Nucleic Acids Res 40: D918-D923
18. Elias JE, Gygi SP, (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214
19. Evsikov AV, Graber JH, Brockman JM, Hampl A, Holbrook AE, Singh P, Eppig JJ, Solter D, Knowles BB, (2006) Cracking the egg: molecular dynamics and evolutionary aspects of the transition from the fully grown oocyte to embryo. Genes Dev 20: 2713-2727
20. Evsikov AV, Evsikova CM, (2009) Gene expression during the oocyte-to-embryo transition in mammals. Mol Reprod Dev 76: 805-818
21. Fredens J, Engholm-Keller K, Giessing A, Pultz D, Larsen MR, Højrup P, Møller-Jensen J, Færgeman NJ, (2011) Quantitative proteomics by amino acid labeling in C. elegans. Nat Methods 8: 845-847
22. Frøkjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, Olesen S-P, Grunnet M, Jorgensen EM, (2008a) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40: 1375-1383
23. Frøkjær-Jensen C, Davis WM, Hopkins CE, Jorgensen EM, (2008b) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40: 1375-1383
24. Gamberi C, Gottlieb E, (2002) Internally controlled poly(A) tail assay to study gene regulation. Biotechniques 33: 476, 478, 480
25. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, Yip KY, Robilotto R, Rechtsteiner A, Ikegami K, Alves P, Chateigner A, Perry M, Morris M, Auerbach RK, Feng X, Leng J, Vielle A, Niu W, Rhrissorrakrai K, et al, (2010) Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science (80-.). 330: 1775-1787
26. Gilbert I, Scantland S, Sylvestre E-L, Gravel C, Laflamme I, Sirard M-A, Robert C, (2009) The dynamics of gene products fluctuation during bovine pre-hatching development. Mol Reprod Dev 76: 762-772
27. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van DS, Inoue K, Enright AJ, Schier AF, (2006) Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science (80-.). 312: 75-79
28. Giraldez AJ, (2010) microRNAs, the cell's Nepenthe: clearing the past during the maternal-to-zygotic transition and cellular reprogramming. Curr Opin Genet Dev 20: 369-375
29. Grün D, Kirchner M, Thierfelder N, Stoeckius M, Selbach M, Rajewsky N, (2014) Conservation of mRNA and Protein Expression during Development of C. elegans. Cell Rep 6: 565-577
30. Guven-Ozkan T, Nishi Y, Robertson SM, Lin R, (2008) Global transcriptional repression in C. elegans germline precursors by regulated sequestration of TAF-4. Cell 135: 149-160
31. Hamatani T, Carter MG, Sharov AA, Ko MSH, (2004) Dynamics of Global Gene Expression Changes during Mouse Preimplantation Development. Dev Cell 6: 117-131
32. Hubner NC, Bird AW, Cox J, Splettstoesser B, Bandilla P, Poser I, Hyman A, Mann M, (2010) Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J Cell Biol 189: 739-754
33. Ji X, Wan J, Vishnu M, Xing Y, Liebhaber S, a, (2013) αCP Poly(C) binding proteins act as global regulators of alternative polyadenylation. Mol Cell Biol 33: 2560-2573
34. Krawetz SA, (2005) Paternal contribution: new insights and future challenges. Nat Rev Genet 6: 633-642
35. Lall S, Grün D, Krek A, Chen K, Wang Y-L, Dewey CN, Sood P, Colombo T, Bray N, Macmenamin P, Kao H-L, Gunsalus KC, Pachter L, Piano F, Rajewsky N, (2006) A genome-wide map of conserved microRNA targets in C. elegans. Curr Biol 16: 460-471
36. Larance M, Bailly AP, Pourkarimi E, Hay RT, Buchanan G, Coulthurst S, Xirodimas DP, Gartner A, Lamond AI, (2011) Stable-isotope labeling with amino acids in nematodes. Nat Methods 8: 849-851
37. Lee MH, Schedl T, (2001) Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev 15: 2408-2420
38. Li H, Durbin R, (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595
39. Lin R, (2003) A gain-of-function mutation in oma-1, a C. elegans gene required for oocyte maturation, results in delayed degradation of maternal proteins and embryonic lethality. Dev Biol 258: 226-239
40. Makeyev AV, Liebhaber SA, (2002) The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms. RNA 8: 265-278
41. Mangone M, Manoharan AP, Thierry-Mieg D, Thierry-Mieg J, Han T, Mackowiak SD, Mis E, Zegar C, Gutwein MR, Khivansara V, Attie O, Chen K, Salehi-Ashtiani K, Vidal M, Harkins TT, Bouffard P, Suzuki Y, Sugano S, Kohara Y, Rajewsky N, et al, (2010) The landscape of C. elegans 3′UTRs. Science (80-.). 329: 432-435
42. McCarter J, Bartlett B, Dang T, Schedl T, (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205: 111-128
43. Merritt C, Rasoloson D, Ko D, Seydoux G, (2008) 3′ UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol 18: 1476-1482
44. Miska EA, Alvarez-Saavedra E, Abbott AL, Lau NC, Hellman AB, McGonagle SM, Bartel DP, Ambros VR, Horvitz HR, (2007) Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet 3: e215
45. Peaston AE, Graber JH, Knowles BB, de Vries WN, (2010) Interrogating the transcriptome of oocytes and preimplantation embryos. Methods Enzymol 477: 481-510
46. Pepke S, Wold B, Mortazavi A, (2009) Computation for ChIP-seq and RNA-seq studies. Nat Methods 6: S22-S32
47. Piko L, Clegg KB, (1982) Quantitative changes in total RNA, total poly(A), and ribosomes in early mouse embryos. Dev Biol 89: 362-378
48. Radford HE, Meijer HA, de Moor CH, (2008) Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim Biophys Acta 1779: 217-229
49. Rappsilber J, Ishihama Y, Mann M, (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 75: 663-670
50. Reinke V, Gil IS, Ward S, Kazmer K, (2004) Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131: 311-323
51. Robertson S, Lin R, (2013) The oocyte-to-embryo transition. Adv Exp Med Biol 757: 351-372
52. Rouget C, Boureux A, Franco B, Papin C, Simonelig M, (2010) Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 467: 1128-1132
53. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N, (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63
54. Seydoux G, Fire A, (1994) Soma-germline asymmetry in the distributions of embryonic RNAs in Caenorhabditis elegans. Development 120: 2823-2834
55. Seydoux G, Dunn MA, (1997) Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. Development 124: 2191-2201
56. Shevchenko A, Loboda A, Ens W, Standing KG, (2000) MALDI quadrupole time-of-flight mass spectrometry: a powerful tool for proteomic research. Anal Chem 72: 2132-2141
57. Srayko M, Buster DW, Bazirgan OA, McNally FJ, Mains PE, (2000) MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes Dev 14: 1072-1084
58. Stadler M, Artiles K, Pak J, Fire A, (2012) Contributions of mRNA abundance, ribosome loading, and post- or peri-translational effects to temporal repression of C. elegans heterochronic miRNA targets. Genome Res 22: 2418-2426
59. Stiernagle T, (2006) Maintenance of C. elegans. WormBook: 1-11
60. Stitzel ML, Seydoux G, (2007) Regulation of the oocyte-to-zygote transition. Science (80-.). 316: 407-408
61. Stoeckius M, Maaskola J, Colombo T, Rahn H-P, Friedländer MR, Li N, Chen W, Piano F, Rajewsky N, (2009) Large-scale sorting of C. elegans embryos reveals the dynamics of small RNA expression. Nat Methods 6: 745-751
62. Stoeckius M, Grün D, Rajewsky N, (2014) Paternal RNA contributions in the Caenorhabditis elegans zygote. EMBO J 33: 1740-1750
63. Suh N, Baehner L, Moltzahn F, Melton C, Shenoy A, Chen J, Blelloch R, (2010) MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr Biol 20: 271-277
64. Svoboda P, Flemr M, (2010) The role of miRNAs and endogenous siRNAs in maternal-to-zygotic reprogramming and the establishment of pluripotency. EMBO Rep 11: 590-597
65. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L, Orr-Weaver T, Hughes TR, Westwood JT, Smibert CA, Lipshitz HD, (2007) SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev Cell 12: 143-155
66. Tadros W, Lipshitz HD, (2009) The maternal-to-zygotic transition: a play in two acts. Development 136: 3033-3042
67. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, Hannon GJ, (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453: 534-538
68. Van Wolfswinkel J, Claycomb JM, Batista PJ, Mello CC, Berezikov E, Ketting RF, (2009) CDE-1 affects chromosome segregation through uridylation of CSR-1-bound siRNAs. Cell 139: 135-148
69. Vasale JJ, Gu W, Thivierge C, Batista PJ, Claycomb JM, Youngman EM, Duchaine TF, Mello CC, Conte D, (2010) Sequential rounds of RNA-dependent RNA transcription drive endogenous small-RNA biogenesis in the ERGO-1/Argonaute pathway. Proc Natl Acad Sci USA 107: 3582-3587
70. Vasudevan S, Seli E, Steitz JA, (2006) Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades. Genes Dev 20: 138-146
71. Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP, Davis RW, Zernicka-Goetz M, (2004) A Genome-Wide Study of Gene Activity Reveals Developmental Signaling Pathways in the Preimplantation Mouse Embryo. Dev Cell 6: 133-144
72. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, Chiba H, Kohara Y, Kono T, Nakano T, Surani MA, Sakaki Y, Sasaki H, (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453: 539-543
73. Zhang P, Zucchelli M, Bruce S, Hambiliki F, Stavreus-Evers A, Levkov L, Skottman H, Kerkelä E, Kere J, Hovatta O, (2009) Transcriptome profiling of human pre-implantation development. PLoS ONE 4: e7844