A Novel Double-stranded RNA-binding Protein, Disco Interacting Protein 1 (DIP1), Contributes to Cell Fate Decisions during Drosophila Development

We report the identification of the Disco Interacting Protein 1 (DIP1) gene isolated in a yeast interaction trap screen using the zinc finger protein disconnected (disco) as a bait. DIP1 encodes a protein containing two double-stranded RNA binding domains (dsRBD). Consistent with the presence of dsRBD, DIP1 binds dsRNA or structured RNAs in Northwestern assays. DIP1 is found in nuclear subdomains resembling speckles known to accumulate transcription and splicing factors. In early embryos, nuclear localization of DIP1 protein coincides with the onset of zygotic gene expression. Later in development DIP1 expression is decreased in dividing cells in different tissues. Overexpression of DIP1 in the eye-antennal imaginal disc, early in embryonic and larval development, causes the formation of supernumerary structures in the head capsule. A role for DIP1 in epigenetic mechanisms that lead to the establishment and/or maintenance of cell fate specification is discussed. We report the identification of the Disco Interacting Protein 1 (DIP1) gene isolated in a yeast interaction trap screen using the zinc finger protein disconnected (disco) as a bait. DIP1 encodes a protein containing two double-stranded RNA binding domains (dsRBD). Consistent with the presence of dsRBD, DIP1 binds dsRNA or structured RNAs in Northwestern assays. DIP1 is found in nuclear subdomains resembling speckles known to accumulate transcription and splicing factors. In early embryos, nuclear localization of DIP1 protein coincides with the onset of zygotic gene expression. Later in development DIP1 expression is decreased in dividing cells in different tissues. Overexpression of DIP1 in the eye-antennal imaginal disc, early in embryonic and larval development, causes the formation of supernumerary structures in the head capsule. A role for DIP1 in epigenetic mechanisms that lead to the establishment and/or maintenance of cell fate specification is discussed. The fate and function of a large number of different RNA molecules are dependent upon their interactions with specific RNA-binding proteins. RNA-binding proteins compose a diverse group of proteins that participate in a wide range of biochemical functions (1Siomi H. Dreyfuss G. Curr. Opin. Genet. Dev. 1997; 7: 345-353Crossref PubMed Scopus (232) Google Scholar). A subset of these proteins preferentially recognizes and binds dsRNA. 1The abbreviations used are: dsRNA, double-stranded RNA; DIP1, Disco interacting protein 1; dsRBD, double-stranded RNA binding domain; DSRBP, dsRNA-binding proteins; disco, disconnected; Ubx, Ultrabithorax; ey, eyeless; hth, homothorax; salm, spalt major; dll, distalless; NLS, nuclear localization signal; UTR, untranslated region; RED1, glutamate receptor RNA editase; ADAR1, human RNA-editing enzyme; GST, glutathione S-transferase; X-gal, 5-bromo-4-chloro-3-indolyl-β-galactopyranoside. These dsRNA-binding proteins (DSRBP) feature the presence of one or more double-stranded RNA binding domains (dsRBD). These structural motifs of 65–68 amino acids in length can be divided into two groups according to their similarity to the consensus sequence and their ability to bind dsRNA. Type A dsRBDs generally bind dsRNA with high affinity and show a high degree of sequence similarity with the entire consensus sequence. Type B dsRBDs bind dsRNA less efficiently and are similar at their C termini to the consensus sequence but not at their N termini (2St. Johnston D. Brown N.H. Gall J.G. Jantsch M. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 10979-10983Crossref PubMed Scopus (486) Google Scholar). DSRBPs are involved in a variety of cellular functions that range from RNA localization to RNA editing and more recently post-transcriptional gene silencing (3Rotondo G. Frendewey D. Nucleic Acids Res. 1996; 24: 2377-2386Crossref PubMed Scopus (69) Google Scholar, 4Green S.R. Mathews M.B. Genes Dev. 1992; 6: 2478-2490Crossref PubMed Scopus (218) Google Scholar, 5Piron M. Vende P. Cohen J. Poncet D. EMBO J. 1998; 17: 5811-5821Crossref PubMed Scopus (303) Google Scholar, 6Langland J.O. Kao P.N. Jacobs B.L. Biochemistry. 1999; 38: 6361-6368Crossref PubMed Scopus (96) Google Scholar). In the Drosophila genome there are 12 dsRBD-containing proteins, and of these only 5 have been genetically characterized (7Lasko P. J. Cell Biol. 2000; 150: 51-56Crossref PubMed Scopus (115) Google Scholar, 8St. Johnston D. Beuchle D. Nusslein-Volhard C. Cell. 1991; 66: 51-63Abstract Full Text PDF PubMed Scopus (503) Google Scholar, 9Bernstein E. Caudy A.A. Hammond S.M. Hannon G.J. Nature. 2001; 409: 363-366Crossref PubMed Scopus (3819) Google Scholar, 10Palladino M.J. Keegan L.P. O'Connell M.A. Reenan R.A. RNA (New York). 2000; 6: 1004-1018Crossref PubMed Scopus (143) Google Scholar, 11Belote J.M. Lucchesi J.C. Nature. 1980; 285: 573-575Crossref PubMed Scopus (147) Google Scholar). The Staufen gene, first identified as mutations that disrupt early embryonic pattern formation, is required for RNA localization and translational control. Mutations in the maleless (mle) gene cause disruption in X chromosome dosage compensation and thus male-specific lethality. The Mle protein is part of the male-specific lethal complex that associates with the X chromosome in males and leads to a 2-fold increase in the expression of X-linked genes presumably through an increase in the level of histone acetylation (reviewed in Ref. 12Birchler J.A. Bhadra U. Bhadra M.P. Auger D.L. Dev. Biol. 2001; 234: 275-288Crossref PubMed Scopus (279) Google Scholar). Three of the Drosophila DSRBPs have been reported to function in RNA interference and editing (9Bernstein E. Caudy A.A. Hammond S.M. Hannon G.J. Nature. 2001; 409: 363-366Crossref PubMed Scopus (3819) Google Scholar, 10Palladino M.J. Keegan L.P. O'Connell M.A. Reenan R.A. RNA (New York). 2000; 6: 1004-1018Crossref PubMed Scopus (143) Google Scholar). The remaining six dsRBD-containing proteins include one protein highly similar to TAR-binding protein and five others of unknown function (7Lasko P. J. Cell Biol. 2000; 150: 51-56Crossref PubMed Scopus (115) Google Scholar). Therefore Drosophila DSRBPs compose a gene function is to the range of biochemical functions of proteins for the development and of an report the identification and of a dsRBD-containing gene, DIP1, for Disco Interacting Protein isolated in a yeast screen to of disconnected (disco) gene The gene encodes a nuclear protein with two zinc in a and a H. G. Cell. Full Text PDF PubMed Scopus Google Scholar, M. P. Dev. Biol. 1999; PubMed Scopus Google Scholar). Mutations in the gene cause a variety of that range from disruption in the of the larval to in the of the in the H. G. Cell. Full Text PDF PubMed Scopus Google Scholar, H. J. PubMed Scopus Google Scholar, C. J. 1998; PubMed Scopus Google Scholar). The DIP1 gene is in of In early embryos, nuclear localization of DIP1 coincides with the onset of zygotic gene expression. the level of DIP1 protein in dividing cells in different embryonic and DIP1 is found in nuclear subdomains resembling speckles to accumulate transcription and splicing factors. DIP1 in the eye-antennal imaginal causes cell fate and the formation of supernumerary structures in the head capsule. that DIP1 epigenetic mechanisms required for the establishment and/or maintenance of cell fate used in these include and The and used for the the into the and of the PubMed Google Scholar). The at and/or The spalt and used in E. using the and of Drosophila embryonic in the yeast expression The according to Ref. J. E. H. Cell. Full Text PDF PubMed Scopus Google The used for the interaction trap to amino or to amino of the with the sequence in the used as the yeast cell according to Ref. D. A. R.A. Nucleic Acids Res. 1992; PubMed Scopus Google A of and containing The Disco at of in of these a of DIP1 DIP1 isolated of a Cell. Full Text PDF PubMed Scopus Google and from an PubMed Scopus Google Scholar). The Drosophila the The DIP1 sequence from isolated from a J. of Disco protein in using the expression from the in the and in from the the DIP1 protein and as as from the in the the is as in Ref. M.P. A. PubMed Scopus Google DIP1 Protein at and of expression The in the used as the and the of used to the protein with a into E. Genet. 1997; PubMed Scopus Google for large protein for protein according to the with in the and The DIP1 protein from the from the for the protein in of and the protein in the at of and and and the of the with the of the The and The double-stranded RNA binding domains using of the from using containing and to for with The dsRBDs into and into E. The for are and and the for are and A with an of from with containing with the and and a using of using in The and the and into E. for are and for are and Northwestern used in Northwestern in the as the one used for The Northwestern is as (2St. Johnston D. Brown N.H. Gall J.G. Jantsch M. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 10979-10983Crossref PubMed Scopus (486) Google Scholar). dsRNA dsRNA RNA from M. with and of 5 used for the binding of DIP1 DIP1 protein to for into two the for The using DIP1 protein a or as J. A Scholar). DIP1 protein in Drosophila cells with The protein DIP1 in not the DIP1 to DIP1 protein in cells not The of the DIP1 the DIP1 the with DIP1 protein in reported not expression of the DIP1 gene the as an nuclear not DIP1 gene expression as with that RNA in not using two different DIP1 from two different an pattern of expression not the of from to as Cell. 1991; Full Text PDF PubMed Scopus Google Scholar). with at with to the number for at The in in containing of and that the with A for to in number at for 1 at for as Cell. 1991; Full Text PDF PubMed Scopus Google Scholar). The of for according to a Cell. 1991; Full Text PDF PubMed Scopus Google Scholar). DIP1 to in for 1 at of at and as J.A. The of Drosophila Google Scholar). as N.H. Cell Biol. PubMed Scopus Google Scholar). The used at a of used to or to and as for in Ref. Cell. 1991; Full Text PDF PubMed Scopus Google Scholar, for and as in Ref. N.H. Cell Biol. PubMed Scopus Google of as N.H. Cell Biol. PubMed Scopus Google that with for 1 at in and for Cell. 1991; Full Text PDF PubMed Scopus Google Scholar, N.H. Cell Biol. PubMed Scopus Google Scholar). of as J. Cell Biol. PubMed Scopus Google and with using a to at a of in a a and using of and imaginal and with for and as U. U. PubMed Scopus Google Scholar). as using and of the Disco Interacting Protein 1 to the mechanisms a yeast screen to of the gene We used an interaction trap as a of the yeast to the binding the and the of the and a to the E. J. E. H. Cell. Full Text PDF PubMed Scopus Google Scholar, Genet. 1997; PubMed Scopus Google Scholar). The a Drosophila embryonic and of the gene used as a of amino acids M. H. EMBO J. 1991; PubMed Scopus Google and a containing the two zinc to the ability of the to gene expression in the of a a of used in a is the found in the 1The abbreviations used are: dsRNA, double-stranded RNA; DIP1, Disco interacting protein 1; dsRBD, double-stranded RNA binding domain; DSRBP, dsRNA-binding proteins; disco, disconnected; Ubx, Ultrabithorax; ey, eyeless; hth, homothorax; salm, spalt major; dll, distalless; NLS, nuclear localization signal; UTR, untranslated region; RED1, glutamate receptor RNA editase; ADAR1, human RNA-editing enzyme; GST, glutathione S-transferase; X-gal, 5-bromo-4-chloro-3-indolyl-β-galactopyranoside. the to be used as in the interaction trap screen not and Ref. M. P. Dev. Biol. 1999; PubMed Scopus Google Scholar). The Disco not in two of the yeast screen The screen using the Disco of two and of these the as of from of these isolated through from interaction the Disco and DIP1 proteins in a protein to to bind to in DIP1 protein with The protein and DIP1 protein only to and not to The DIP1 a dsRNA-binding Protein DIP1 gene to the transcription that the in at the of the X chromosome A. A. A. 2001; Google Scholar). The of the DIP1 gene and the of isolated DIP1 are in A. A. A. 2001; Google Scholar). in the sequence of these at the and at the of the DIP1 can be for the of different of 1 and The of these include consensus and splicing that of these is for the sequence at the The of a in and but not in that proteins with a different N be the The of in lead to the of a protein from a in that the first is used the of the and proteins is and The DIP1 gene a nuclear localization sequence that and C. R.A. Sci. 1991; Full Text PDF PubMed Scopus Google Scholar). The number of of in in and 5 in The number of been to be A. A. A. 2001; Google Scholar). using J. Biol. PubMed Scopus Google that the DIP1 protein two with similarity to double-stranded RNA binding domains and A consensus for dsRBDs been from in binding and sequence of dsRNA-binding proteins Johnston D. Beuchle D. Nusslein-Volhard C. Cell. 1991; 66: 51-63Abstract Full Text PDF PubMed Scopus (503) Google Scholar, Nucleic Acids Res. PubMed Scopus Google Scholar). The consensus sequence is 65–68 amino acids (2St. Johnston D. Brown N.H. Gall J.G. Jantsch M. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 10979-10983Crossref PubMed Scopus (486) Google Scholar). of dsRBD, a and have been according to the degree and of similarity to the consensus sequence (2St. Johnston D. Brown N.H. Gall J.G. Jantsch M. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 10979-10983Crossref PubMed Scopus (486) Google Scholar). 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The of Drosophila Scholar). in cell fate the of DIP1 in the first DIP1 expression these the that DIP1 epigenetic mechanisms required for the establishment and/or maintenance of cell fate We report the identification and of a gene, DIP1, isolated of with the zinc gene in a yeast interaction trap the interaction in have binding of DIP1 to Disco in The not these interactions are for the function of in the function of DIP1 gene in DIP1 of with of localization in domains in the early coincides with the onset of zygotic transcription and splicing have been found in similar or speckles in with the nuclear J. Biol. 1998; PubMed Scopus Google Scholar, D. M.A. J. Cell. 1998; PubMed Scopus Google Scholar, S. S. J. Cell. 1998; PubMed Scopus Google Scholar). the that speckles of for transcription and splicing of gene expression C. E. S.M. EMBO J. 1997; PubMed Scopus Google Scholar, M.J. J. Cell Sci. 1997; Google Scholar, J. 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J. 1997; PubMed Google RNA and localization (3Rotondo G. Frendewey D. Nucleic Acids Res. 1996; 24: 2377-2386Crossref PubMed Scopus (69) Google translational S.R. Mathews M.B. Genes Dev. 1992; 6: 2478-2490Crossref PubMed Scopus (218) Google Scholar, 5Piron M. Vende P. Cohen J. Poncet D. EMBO J. 1998; 17: 5811-5821Crossref PubMed Scopus (303) Google J.O. Kao P.N. Jacobs B.L. Biochemistry. 1999; 38: 6361-6368Crossref PubMed Scopus (96) Google and recently post-transcriptional gene silencing (reviewed in Ref. M. Jantsch J. Biol. Scopus Google Scholar). In the is required to the in a of the transcription been identified that dsRBDs similar to that of DIP1 C. J.M. M.J. Cell. Biol. 1998; PubMed Scopus Google Scholar). similar to found for DIP1 in from the to the at the C. J.M. M.J. Cell. Biol. 1998; PubMed Scopus Google Scholar). The of the nuclear of a transcription required for the expression of two of the P.N. G. J. J. J. Biol. Full Text PDF PubMed Google Scholar). 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Biol. 1998; PubMed Scopus Google Scholar, C. E. S.M. EMBO J. 1997; PubMed Scopus Google Scholar, M.J. H. Proc. Natl. Acad. Sci. U. S. A. 1996; PubMed Scopus Google Scholar, S. S. G. J. M. D.L. Nature. 1997; PubMed Scopus Google Scholar, M.J. J. Biol. 1998; Full Text Full Text PDF PubMed Scopus Google of splicing and transcription with the nuclear These the of the of the nuclear as a the interaction of transcription and RNA gene expression J. Biol. 1998; PubMed Scopus Google Scholar). The of transcription and splicing with the nuclear is for and and thus for the and maintenance of D. M.A. J. Cell. 1998; PubMed Scopus Google Scholar, S. S. J. Cell. 1998; PubMed Scopus Google Scholar, C. S. S. J. S. S. Proc. Natl. Acad. Sci. U. S. A. 1998; PubMed Scopus Google Scholar). We are to and Jacobs for and and to for A. C. A. for the We and for and for their to We are to The Drosophila as as to and for Drosophila The M. We J. and for and with

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