A quantitative RNA code for mRNA target selection by the germline fate determinant GLD-1

EMBO Journal

Volumn 30, Issue 3, 2011, Pages 533-545

  Wright, Jane E ^a   Gaidatzis, Dimos ^a   Senften, Mathias ^a   Farley, Brian M ^b   Westhof, Eric ^c   Ryder, Sean P ^b   Ciosk, Rafal ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

GLD 1; Quaking; RBP; ribonomics; STAR

Indexed keywords

GLD 1 PROTEIN; MESSENGER RNA; PROTOZOAL PROTEIN; RNA; RNA BINDING PROTEIN; SIGNAL TRANSDUCTION AND ACTIVATION OF RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CAENORHABDITIS ELEGANS; CELL FATE; CONTROLLED STUDY; EMBRYO; GENE ACTIVATION; GENE REGULATORY NETWORK; GENE REPRESSION; GENE TARGETING; GENETIC SELECTION; GERM CELL; GLD 1 BINDING MOTIF; IMMUNOPRECIPITATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PROCESSING; QUANTITATIVE ANALYSIS; RNA ANALYSIS; RNA TRANSLATION; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; UNTRANSLATED REGION;

ANIMALS; BINDING, COMPETITIVE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; COMPUTATIONAL BIOLOGY; GENE REGULATORY NETWORKS; IMMUNOPRECIPITATION; MICROARRAY ANALYSIS; MODELS, BIOLOGICAL; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA, MESSENGER; RNA-BINDING PROTEINS;

CAENORHABDITIS ELEGANS;

EID: 79551607008     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.334     Document Type: Article

References (49)

1. 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: 28-36
2. Berger MF, Philippakis AA, Qureshi AM, He FS, Estep III PW, Bulyk ML (2006) Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat Biotechnol 24: 1429-1435
3. Biedermann B, Hotz HR, Ciosk R (2010) The quaking family of RNA-binding proteins: coordinators of the cell cycle and differentiation. Cell Cycle 9: 1929-1933
4. Biedermann B, Wright J, Senften M, Kalchhauser I, Sarathy G, Lee MH, Ciosk R (2009) Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis. Dev Cell 17: 355-364
5. Ciosk R, DePalma M, Priess JR (2006) Translational regulators maintain totipotency in the Caenorhabditis elegans germline. Science (New York, NY) 311 : 851-853
6. Cooper TA, Wan L, Dreyfuss G (2009) RNA and disease. Cell 136: 777-793
7. Emmerth S, Schober H, Gaidatzis D, Roloff T, Jacobeit K, Buhler M (2010) Nuclear retention of fission yeast dicer is a prerequisite for RNAi-mediated heterochromatin assembly. Dev Cell 18: 102-113
8. Francis R, Barton MK, Kimble J, Schedl T (1995a) gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139: 579-606
9. Francis R, Maine E, Schedl T (1995b) Analysis of the multiple roles of gld-1 in germline development: interactions with the sex determination cascade and the glp-1 signaling pathway. Genetics 139: 607-630
10. Frokjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, Olesen SP, Grunnet M, Jorgensen EM (2008) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40: 1375-1383
11. Galarneau A, Richard S (2005) Target RNA motif and target mRNAs of the Quaking STAR protein. Nat Struct Mol Biol 12: 691-698
12. Galarneau A, Richard S (2009) The STAR RNA binding proteins GLD-1, QKI, SAM68 and SLM-2 bind bipartite RNA motifs. BMC Mol Biol 10: 47
13. Gentleman R, Ihaka R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5: 299-314
14. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
15. Gerber AP, Herschlag D, Brown PO (2004) Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol 2: E79
16. Grant B, Hirsh D (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10: 4311-4326
17. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano Jr M, Jungkamp AC, Munschauer M, Ulrich A, Wardle GS, Dewell S, Zavolan M, Tuschl T (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141
18. Halbeisen RE, Galgano A, Scherrer T, Gerber AP (2008) Post-transcriptional gene regulation: from genome-wide studies to principles. Cell Mol Life Sci 65: 798-813
19. Israeli D, Nir R, Volk T (2007) Dissection of the target specificity of the RNA-binding protein HOW reveals dpp mRNA as a novel HOW target. Development 134: 2107-2114
20. Jan E, Motzny CK, Graves LE, Goodwin EB (1999) The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J 18: 258-269
21. Jones AR, Francis R, Schedl T (1996) GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev Biol 180: 165-183
22. Jones AR, Schedl T (1995) Mutations in gld-1, a female germ cell-specific tumor suppressor gene in Caenorhabditis elegans, affect a conserved domain also found in Src-associated protein Sam68. Genes Dev 9: 1491-1504
23. Keene JD (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8: 533-543
24. Kim MY, Hur J, Jeong S (2009) Emerging roles of RNA and RNA-binding protein network in cancer cells. BMB Rep 42: 125-130
25. 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
26. Lee MH, Schedl T (2004) Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans. Genes Dev 18: 1047-1059
27. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X, Darnell JC, Darnell RB (2008) HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456: 464-469
28. Liu Z, Luyten I, Bottomley MJ, Messias AC, Houngninou-Molango S, Sprangers R, Zanier K, Kramer A, Sattler M (2001) Structural basis for recognition of the intron branch site RNA by splicing factor 1. Science (New York, NY) 294: 1098-1102
29. Lukong KE, Chang KW, Khandjian EW, Richard S (2008) RNA-binding proteins in human genetic disease. Trends Genet 24: 416-425
30. Lunde BM, Moore C, Varani G (2007) RNA-binding proteins: modular design for efficient function. Nat Rev 8: 479-490
31. Ma J, Flemr M, Stein P, Berninger P, Malik R, Zavolan M, Svoboda P, Schultz RM (2010) MicroRNA activity is suppressed in mouse oocytes. Curr Biol 20: 265-270
32. Marin VA, Evans TC (2003) Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1. Development 130: 2623-2632
33. 0 UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol 18: 1476-1482
34. Mootz D, Ho DM, Hunter CP (2004) The STAR/Maxi-KH domain protein GLD-1 mediates a developmental switch in the translational control of C. elegans PAL-1. Development 131: 3263-3272
35. Praitis V, Casey E, Collar D, Austin J (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157: 1217-1226
36. Ray D, Kazan H, Chan ET, Pena Castillo L, Chaudhry S, Talukder S, Blencowe BJ, Morris Q, Hughes TR (2009) Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat Biotechnol 27: 667-670
37. Ryder SP, Frater LA, Abramovitz DL, Goodwin EB, Williamson JR (2004) RNA target specificity of the STAR/GSG domain post-transcriptional regulatory protein GLD-1. Nat Struct Mol Biol 11 : 20-28
38. Schumacher B, Hanazawa M, Lee MH, Nayak S, Volkmann K, Hofmann R, Hengartner M, Schedl T, Gartner A (2005) Translational repression of C. elegans p53 by GLD-1 regulates DNA damage-induced apoptosis. Cell 120: 357-368
39. Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745
40. 0UTR evolution. Cell 123: 1133-1146
41. 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
42. Tenenbaum SA, Carson CC, Lager PJ, Keene JD (2000) Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc Natl Acad Sci USA 97: 14085-14090
43. Ule J (2008) Ribonucleoprotein complexes in neurologic diseases. Curr Opin Neurobiol 18: 516-523
44. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, Darnell RB (2003) CLIP identifies Nova-regulated RNA networks in the brain. Science (New York, NY) 302: 1212-1215
45. Vernet C, Artzt K (1997) STAR, a gene family involved in signal transduction and activation of RNA. Trends Genet 13: 479-484
46. Volk T, Israeli D, Nir R, Toledano-Katchalski H (2008) Tissue development and RNA control: 'HOW' is it coordinated? Trends Genet 24: 94-101
47. Wang X, Zhao Y, Wong K, Ehlers P, Kohara Y, Jones SJ, Marra MA, Holt RA, Moerman DG, Hansen D (2009) Identification of genes expressed in the hermaphrodite germ line of C. elegans using SAGE. BMC Genomics 10 : 21 3
48. Wu Z, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleo-tide expression arrays. J Am Stat Assoc 99: 909
49. Xu L, Paulsen J, Yoo Y, Goodwin EB, Strome S (2001) Caenorhabditis elegans MES-3 is a target of GLD-1 and functions epigenetically in germline development. Genetics 159: 1007-1017