Genome-wide analysis of the maternal-to-zygotic transition in Drosophila primordial germ cells

Genome Biology

Volumn 13, Issue 2, 2012, Pages

  Siddiqui, Najeeb U ^a,b   Li, Xiao ^a   Luo, Hua ^a   Karaiskakis, Angelo ^a   Hou, Huayun ^a,c   Kislinger, Thomas ^d   Westwood, J Timothy ^e   Morris, Quaid ^a   Lipshitz, Howard D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c PEKING UNIVERSITY   (China)

^d UNIVERSITY HEALTH NETWORK   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; MESSENGER RNA; PROTEOME; RNA; RNA BINDING PROTEIN; TRANSCRIPTOME;

ARTICLE; CELL TYPE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE ACTIVATION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC CODE; GENETIC TRANSCRIPTION; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PRIMORDIAL GERM CELL; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; ZYGOTE; ANIMAL; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GERM CELL; METABOLISM; PRENATAL DEVELOPMENT;

ANIMALS; DROSOPHILA MELANOGASTER; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; PROTEOME; RNA, MESSENGER, STORED; TRANSCRIPTOME; ZYGOTE;

EID: 84862777100     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2012-13-2-r11     Document Type: Article

References (90)

1. Tadros W, Lipshitz HD. The maternal-to-zygotic transition: a play in two acts. Development 2009, 136:3033-3042. 10.1242/dev.033183, 19700615.
2. Walser CB, Lipshitz HD. Transcript clearance during the maternal-to-zygotic transition. Curr Opin Genet Dev 2011, 21:431-443. 10.1016/j.gde.2011.03.003, 21497081.
3. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L, Orr-Weaver T, Hughes TR, Westwood JT, Smibert CA, Lipshitz HD. SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev Cell 2007, 12:143-155. 10.1016/j.devcel.2006.10.005, 17199047.
4. Aviv T, Lin Z, Ben-Ari G, Smibert CA, Sicheri F. Sequence-specific recognition of RNA hairpins by the SAM domain of Vts1p. Nat Struct Mol Biol 2006, 13:168-176. 10.1038/nsmb1053, 16429151.
5. Aviv T, Lin Z, Lau S, Rendl LM, Sicheri F, Smibert CA. The RNA-binding SAM domain of Smaug defines a new family of post-transcriptional regulators. Nat Struct Biol 2003, 10:614-621. 10.1038/nsb956, 12858164.
6. Dahanukar A, Wharton RP. The Nanos gradient in Drosophila embryos is generated by translational regulation. Genes Dev 1996, 10:2610-2620. 10.1101/gad.10.20.2610, 8895662.
7. Semotok JL, Cooperstock RL, Pinder BD, Vari HK, Lipshitz HD, Smibert CA. Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr Biol 2005, 15:284-294. 10.1016/j.cub.2005.01.048, 15723788.
8. Semotok JL, Luo H, Cooperstock RL, Karaiskakis A, Vari HK, Smibert CA, Lipshitz HD. Drosophila maternal Hsp83 mRNA destabilization is directed by multiple SMAUG recognition elements in the open reading frame. Mol Cell Biol 2008, 28:6757-6772. 10.1128/MCB.00037-08, 2573300, 18794360.
9. Smibert CA, Wilson JE, Kerr K, Macdonald PM. Smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev 1996, 10:2600-2609. 10.1101/gad.10.20.2600, 8895661.
10. Baez MV, Boccaccio GL. Mammalian Smaug is a translational repressor that forms cytoplasmic foci similar to stress granules. J Biol Chem 2005, 280:43131-43140. 10.1074/jbc.M508374200, 16221671.
11. Baez MV, Luchelli L, Maschi D, Habif M, Pascual M, Thomas MG, Boccaccio GL. Smaug1 mRNA-silencing foci respond to NMDA and modulate synapse formation. J Cell Biol 2011, 195:1141-1157. 10.1083/jcb.201108159, 22201125.
12. Benoit B, He CH, Zhang F, Votruba SM, Tadros W, Westwood JT, Smibert CA, Lipshitz HD, Theurkauf WE. An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition. Development 2009, 136:923-932. 10.1242/dev.031815, 2727558, 19234062.
13. Bushati N, Stark A, Brennecke J, Cohen SM. Temporal reciprocity of miRNAs and their targets during the maternal-to-zygotic transition in Drosophila. Curr Biol 2008, 18:501-506. 10.1016/j.cub.2008.02.081, 18394895.
14. Graindorge A, Le Tonqueze O, Thuret R, Pollet N, Osborne HB, Audic Y. Identification of CUG-BP1/EDEN-BP target mRNAs in Xenopus tropicalis. Nucleic Acids Res 2008, 36:1861-1870. 10.1093/nar/gkn031, 2330240, 18267972.
15. Paillard L, Omilli F, Legagneux V, Bassez T, Maniey D, Osborne HB. EDEN and EDEN-BP, a cis element and an associated factor that mediate sequence-specific mRNA deadenylation in Xenopus embryos. EMBO J 1998, 17:278-287. 10.1093/emboj/17.1.278, 1170378, 9427761.
16. Schubert CM, Lin R, de Vries CJ, Plasterk RH, Priess JR. MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos. Mol Cell 2000, 5:671-682. 10.1016/S1097-2765(00)80246-4, 10882103.
17. Voeltz GK, Steitz JA. AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development. Mol Cell Biol 1998, 18:7537-7545. 109334, 9819439.
18. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF. Zebrafish miR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312:75-79. 10.1126/science.1122689, 16484454.
19. Lund E, Liu M, Hartley RS, Sheets MD, Dahlberg JE. Deadenylation of maternal mRNAs mediated by miR-427 in Xenopus laevis embryos. RNA 2009, 15:2351-2363. 10.1261/rna.1882009, 2779678, 19854872.
20. Strome S, Lehmann R. Germ versus soma decisions: lessons from flies and worms. Science 2007, 316:392-393. 10.1126/science.1140846, 17446385.
21. Nakamura A, Shirae-Kurabayashi M, Hanyu-Nakamura K. Repression of early zygotic transcription in the germline. Curr Opin Cell Biol 2010, 22:709-714. 10.1016/j.ceb.2010.08.012, 20817425.
22. Shigenobu S, Arita K, Kitadate Y, Noda C, Kobayashi S. Isolation of germline cells from Drosophila embryos by flow cytometry. Dev Growth Differ 2006, 48:49-57. 10.1111/j.1440-169X.2006.00845.x, 16466393.
23. Yatsu J, Hayashi M, Mukai M, Arita K, Shigenobu S, Kobayashi S. Maternal RNAs encoding transcription factors for germline-specific gene expression in Drosophila embryos. Int J Dev Biol 2008, 52:913-923. 10.1387/ijdb.082576jy, 18956321.
24. Kislinger T, Cox B, Kannan A, Chung C, Hu P, Ignatchenko A, Scott MS, Gramolini AO, Morris Q, Hallett MT, Rossant J, Hughes TR, Frey B, Emili A. Global survey of organ and organelle protein expression in mouse: combined proteomic and transcriptomic profiling. Cell 2006, 125:173-186. 10.1016/j.cell.2006.01.044, 16615898.
25. Taylor P, Nielsen PA, Trelle MB, Horning OB, Andersen MB, Vorm O, Moran MF, Kislinger T. Automated 2D peptide separation on a 1D nano-LC-MS system. J Proteome Res 2009, 8:1610-1616. 10.1021/pr800986c, 19178303.
26. Washburn MP, Wolters D, Yates JR. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 2001, 19:242-247. 10.1038/85686, 11231557.
27. Gouw JW, Pinkse MW, Vos HR, Moshkin Y, Verrijzer CP, Heck AJ, Krijgsveld J. In vivo stable isotope labeling of fruit flies reveals post-transcriptional regulation in the maternal-to-zygotic transition. Mol Cell Proteomics 2009, 8:1566-1578. 10.1074/mcp.M900114-MCP200, 2709187, 19321433.
28. Bardsley A, McDonald K, Boswell RE. Distribution of tudor protein in the Drosophila embryo suggests separation of functions based on site of localization. Development 1993, 119:207-219.
29. Breitwieser W, Markussen FH, Horstmann H, Ephrussi A. Oskar protein interaction with Vasa represents an essential step in polar granule assembly. Genes Dev 1996, 10:2179-2188. 10.1101/gad.10.17.2179, 8804312.
30. Harris AN, Macdonald PM. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 2001, 128:2823-2832.
31. Hay B, Jan LY, Jan YN. A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 1988, 55:577-587. 10.1016/0092-8674(88)90216-4, 3052853.
32. Megosh HB, Cox DN, Campbell C, Lin H. The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr Biol 2006, 16:1884-1894. 10.1016/j.cub.2006.08.051, 16949822.
33. Theurkauf WE. Behavior of structurally divergent alpha-tubulin isotypes during Drosophila embryogenesis: evidence for post-translational regulation of isotype abundance. Dev Biol 1992, 154:205-217. 10.1016/0012-1606(92)90060-T, 1426627.
34. Reveal B, Yan N, Snee MJ, Pai CI, Gim Y, Macdonald PM. BREs mediate both repression and activation of oskar mRNA translation and act in trans. Dev Cell 2010, 18:496-502. 10.1016/j.devcel.2009.12.021, 2841435, 20230756.
35. St Johnston D, Beuchle D, Nusslein-Volhard C. Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 1991, 66:51-63. 10.1016/0092-8674(91)90138-O, 1712672.
36. BDGP in situ homepage. , http://insitu.fruitfly.org/cgi-bin/ex/insitu.pl
37. FlyFISH database. , http://www.utoronto.ca/krause/
38. Ohlstein B, Lavoie CA, Vef O, Gateff E, McKearin DM. The Drosophila cystoblast differentiation factor, benign gonial cell neoplasm, is related to DExH-box proteins and interacts genetically with bag-of-marbles. Genetics 2000, 155:1809-1819. 1461197, 10924476.
39. Gonczy P, Matunis E, DiNardo S. Bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Development 1997, 124:4361-4371.
40. McKearin DM, Spradling AC. Bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev 1990, 4:2242-2251. 10.1101/gad.4.12b.2242, 2279698.
41. Neumuller RA, Betschinger J, Fischer A, Bushati N, Poernbacher I, Mechtler K, Cohen SM, Knoblich JA. Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature 2008, 454:241-245. 10.1038/nature07014, 2988194, 18528333.
42. Ding D, Whittaker KL, Lipshitz HD. Mitochondrially encoded 16S large ribosomal RNA is concentrated in the posterior polar plasm of early Drosophila embryos but is not required for pole cell formation. Dev Biol 1994, 163:503-515. 10.1006/dbio.1994.1166, 7515364.
43. Dalby B, Glover DM. Discrete sequence elements control posterior pole accumulation and translational repression of maternal cyclin B RNA in Drosophila. EMBO J 1993, 12:1219-1227. 413325, 8458334.
44. Zhang N, Zhang J, Purcell KJ, Cheng Y, Howard K. The Drosophila protein Wunen repels migrating germ cells. Nature 1997, 385:64-67. 10.1038/385064a0, 8985246.
45. Sano H, Renault AD, Lehmann R. Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatases Wunen and Wunen 2. J Cell Biol 2005, 171:675-683. 10.1083/jcb.200506038, 2171572, 16301333.
46. Renault AD, Kunwar PS, Lehmann R. Lipid phosphate phosphatase activity regulates dispersal and bilateral sorting of embryonic germ cells in Drosophila. Development 2010, 137:1815-1823. 10.1242/dev.046110, 2867317, 20431117.
47. Starz-Gaiano M, Cho NK, Forbes A, Lehmann R. Spatially restricted activity of a Drosophila lipid phosphatase guides migrating germ cells. Development 2001, 128:983-991.
48. Uemura T, Shepherd S, Ackerman L, Jan LY, Jan YN. numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 1989, 58:349-360. 10.1016/0092-8674(89)90849-0, 2752427.
49. Qin H, Percival-Smith A, Li C, Jia CY, Gloor G, Li SS. A novel transmembrane protein recruits numb to the plasma membrane during asymmetric cell division. J Biol Chem 2004, 279:11304-11312. 10.1074/jbc.M311733200, 14670962.
50. Moreira S, Stramer B, Evans I, Wood W, Martin P. Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo. Curr Biol 2010, 20:464-470. 10.1016/j.cub.2010.01.047, 20188558.
51. Paululat A, Goubeaud A, Damm C, Knirr S, Burchard S, Renkawitz-Pohl R. The mesodermal expression of rolling stone (rost) is essential for myoblast fusion in Drosophila and encodes a potential transmembrane protein. J Cell Biol 1997, 138:337-348. 10.1083/jcb.138.2.337, 2138187, 9230076.
52. Sun Q, Schindelholz B, Knirr M, Schmid A, Zinn K. Complex genetic interactions among four receptor tyrosine phosphatases regulate axon guidance in Drosophila. Mol Cell Neurosci 2001, 17:274-291. 10.1006/mcne.2000.0939, 11178866.
53. Lee YS, Pressman S, Andress AP, Kim K, White JL, Cassidy JJ, Li X, Lubell K, Lim do H, Cho IS, Nakahara K, Preall JB, Bellare P, Sontheimer EJ, Carthew RW. Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 2009, 11:1150-1156. 10.1038/ncb1930, 2737091, 19684574.
54. Hanyu-Nakamura K, Sonobe-Nojima H, Tanigawa A, Lasko P, Nakamura A. Drosophila Pgc protein inhibits P-TEFb recruitment to chromatin in primordial germ cells. Nature 2008, 451:730-733. 10.1038/nature06498, 2719856, 18200011.
55. Hoffman BE, Lis JT. Pre-mRNA splicing by the essential Drosophila protein B52: tissue and target specificity. Mol Cell Biol 2000, 20:181-186. 10.1128/MCB.20.1.181-186.2000, 85073, 10594020.
56. Herold N, Will CL, Wolf E, Kastner B, Urlaub H, Luhrmann R. Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol Cell Biol 2009, 29:281-301. 10.1128/MCB.01415-08, 2612486, 18981222.
57. Mount SM, Salz HK. Pre-messenger RNA processing factors in the Drosophila genome. J Cell Biol 2000, 150:F37-44. 10.1083/jcb.150.2.F37, 2180228, 10908584.
58. Aravin AA, Naumova NM, Tulin AV, Vagin VV, Rozovsky YM, Gvozdev VA. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol 2001, 11:1017-1027. 10.1016/S0960-9822(01)00299-8, 11470406.
59. Lecuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T, Cerovina T, Hughes TR, Tomancak P, Krause HM. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 2007, 131:174-187. 10.1016/j.cell.2007.08.003, 17923096.
60. Dahanukar A, Walker JA, Wharton RP. Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol Cell 1999, 4:209-218. 10.1016/S1097-2765(00)80368-8, 10488336.
61. Smibert CA, Lie YS, Shillinglaw W, Henzel WJ, Macdonald PM. Smaug, a novel and conserved protein, contributes to repression of nanos mRNA translation in vitro. RNA 1999, 5:1535-1547. 10.1017/S1355838299991392, 1369876, 10606265.
62. Neumuller RA, Richter C, Fischer A, Novatchkova M, Neumuller KG, Knoblich JA. Genome-wide analysis of self-renewal in Drosophila neural stem cells by transgenic RNAi. Cell Stem Cell 2011, 8:580-593. 10.1016/j.stem.2011.02.022, 3093620, 21549331.
63. Weyers JJ, Milutinovich AB, Takeda Y, Jemc JC, Van Doren M. A genetic screen for mutations affecting gonad formation in Drosophila reveals a role for the slit/robo pathway. Dev Biol 2011, 353:217-228. 10.1016/j.ydbio.2011.02.023, 21377458.
64. Junger MA, Rintelen F, Stocker H, Wasserman JD, Vegh M, Radimerski T, Greenberg ME, Hafen E. The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2003, 2:20. 10.1186/1475-4924-2-20, 333403, 12908874.
65. Puig O, Marr MT, Ruhf ML, Tjian R. Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev 2003, 17:2006-2020. 10.1101/gad.1098703, 196255, 12893776.
66. Rhyu MS, Jan LY, Jan YN. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 1994, 76:477-491. 10.1016/0092-8674(94)90112-0, 8313469.
67. Li X, Quon G, Lipshitz HD, Morris Q. Predicting in vivo binding sites of RNA-binding proteins using mRNA secondary structure. RNA 2010, 16:1096-1107. 10.1261/rna.2017210, 2874161, 20418358.
68. Murata Y, Wharton RP. Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 1995, 80:747-756. 10.1016/0092-8674(95)90353-4, 7889568.
69. De Renzis S, Elemento O, Tavazoie S, Wieschaus EF. Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 2007, 5:e117. 10.1371/journal.pbio.0050117, 1854917, 17456005.
70. Nelson MR, Luo H, Vari HK, Cox BJ, Simmonds AJ, Krause HM, Lipshitz HD, Smibert CA. A multiprotein complex that mediates translational enhancement in Drosophila. J Biol Chem 2007, 282:34031-34038. 10.1074/jbc.M706363200, 17890223.
71. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N. Combinatorial microRNA target predictions. Nat Genet 2005, 37:495-500. 10.1038/ng1536, 15806104.
72. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20. 10.1016/j.cell.2004.12.035, 15652477.
73. Aboobaker AA, Tomancak P, Patel N, Rubin GM, Lai EC. Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc Natl Acad Sci USA 2005, 102:18017-18022. 10.1073/pnas.0508823102, 1306796, 16330759.
74. Thomsen S, Anders S, Janga SC, Huber W, Alonso CR. Genome-wide analysis of mRNA decay patterns during early Drosophila development. Genome Biol 2010, 11:R93. 10.1186/gb-2010-11-9-r93, 2965385, 20858238.
75. Santon JB, Pellegrini M. Expression of ribosomal proteins during Drosophila early development. Proc Natl Acad Sci USA 1980, 77:5649-5653. 10.1073/pnas.77.10.5649, 350126, 6777772.
76. Santon JB, Pellegrini M. Rates of ribosomal protein and total protein synthesis during Drosophila early embryogenesis. Dev Biol 1981, 85:252-257. 10.1016/0012-1606(81)90255-4, 7250514.
77. Gilbert WV. Functional specialization of ribosomes?. Trends Biochem Sci 2011, 36:127-132. 10.1016/j.tibs.2010.12.002, 3056915, 21242088.
78. Kai T, Williams D, Spradling AC. The expression profile of purified Drosophila germline stem cells. Dev Biol 2005, 283:486-502. 10.1016/j.ydbio.2005.04.018, 15927177.
79. Bashirullah A, Cooperstock RL, Lipshitz HD. Spatial and temporal control of RNA stability. Proc Natl Acad Sci USA 2001, 98:7025-7028. 10.1073/pnas.111145698, 34617, 11416182.
80. Bashirullah A, Halsell SR, Cooperstock RL, Kloc M, Karaiskakis A, Fisher WW, Fu W, Hamilton JK, Etkin LD, Lipshitz HD. Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J 1999, 18:2610-2620. 10.1093/emboj/18.9.2610, 1171340, 10228172.
81. Tadros W, Houston SA, Bashirullah A, Cooperstock RL, Semotok JL, Reed BH, Lipshitz HD. Regulation of maternal transcript destabilization during egg activation in Drosophila. Genetics 2003, 164:989-1001. 1462612, 12871909.
82. Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP. Gene expression during the life cycle of Drosophila melanogaster. Science 2002, 297:2270-2275. 10.1126/science.1072152, 12351791.
83. Martinho RG, Kunwar PS, Casanova J, Lehmann R. A noncoding RNA is required for the repression of RNApolII-dependent transcription in primordial germ cells. Curr Biol 2004, 14:159-165. 10.1016/j.cub.2003.12.036, 14738740.
84. Bergsten SE, Gavis ER. Role for mRNA localization in translational activation but not spatial restriction of nanos RNA. Development 1999, 126:659-669.
85. Zaessinger S, Busseau I, Simonelig M. Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4. Development 2006, 133:4573-4583. 10.1242/dev.02649, 17050620.
86. Pritchard DK, Schubiger G. Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio. Genes Dev 1996, 10:1131-1142. 10.1101/gad.10.9.1131, 8654928.
87. Johnstone O, Lasko P. Interaction with eIF5B is essential for Vasa function during development. Development 2004, 131:4167-4178. 10.1242/dev.01286, 15280213.
88. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002, 74:5383-5392. 10.1021/ac025747h, 12403597.
89. DAVID Functional Annotation Tool. , http://david.abcc.ncifcrf.gov/summary.jsp
90. GeneMANIA. , http://www.GeneMANIA.org/