PSF and p54nrb bind a conserved stem in U5 snRNA (original) (raw)

Abstract

PTB-associated splicing factor (PSF) has been implicated in both early and late steps of pre-mRNA splicing, but its exact role in this process remains unclear. Here we show that PSF interacts with p54nrb, a highly related protein first identified based on cross-reactivity to antibodies against the yeast second-step splicing factor Prpl8. We performed RNA-binding experiments to determine the preferred RNA-binding sequences for PSF and p54nrb, both individually and in combination. In all cases, iterative selection assays identified a purine-rich sequence located on the 3' side of U5 snRNA stem 1b. Filter-binding assays and RNA affinity selection experiments demonstrated that PSF and p54nrb bind U5 snRNA with both the sequence and structure of stem 1b contributing to binding specificity. Sedimentation analyses show that both proteins associate with spliceosomes and with U4/U6.U5 tri-snPNP.

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Selected References

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  1. Abmayr S. M., Workman J. L., Roeder R. G. The pseudorabies immediate early protein stimulates in vitro transcription by facilitating TFIID: promoter interactions. Genes Dev. 1988 May;2(5):542–553. doi: 10.1101/gad.2.5.542. [DOI] [PubMed] [Google Scholar]
  2. Achsel T., Ahrens K., Brahms H., Teigelkamp S., Lührmann R. The human U5-220kD protein (hPrp8) forms a stable RNA-free complex with several U5-specific proteins, including an RNA unwindase, a homologue of ribosomal elongation factor EF-2, and a novel WD-40 protein. Mol Cell Biol. 1998 Nov;18(11):6756–6766. doi: 10.1128/mcb.18.11.6756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Akhmedov A. T., Lopez B. S. Human 100-kDa homologous DNA-pairing protein is the splicing factor PSF and promotes DNA strand invasion. Nucleic Acids Res. 2000 Aug 15;28(16):3022–3030. doi: 10.1093/nar/28.16.3022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Alvi R. K., Lund M., Okeefe R. T. ATP-dependent interaction of yeast U5 snRNA loop 1 with the 5' splice site. RNA. 2001 Jul;7(7):1013–1023. doi: 10.1017/s135583820101041x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Andersen Jens S., Lyon Carol E., Fox Archa H., Leung Anthony K. L., Lam Yun Wah, Steen Hanno, Mann Matthias, Lamond Angus I. Directed proteomic analysis of the human nucleolus. Curr Biol. 2002 Jan 8;12(1):1–11. doi: 10.1016/s0960-9822(01)00650-9. [DOI] [PubMed] [Google Scholar]
  6. Barnard D. C., Patton J. G. Identification and characterization of a novel serine-arginine-rich splicing regulatory protein. Mol Cell Biol. 2000 May;20(9):3049–3057. doi: 10.1128/mcb.20.9.3049-3057.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Basu A., Dong B., Krainer A. R., Howe C. C. The intracisternal A-particle proximal enhancer-binding protein activates transcription and is identical to the RNA- and DNA-binding protein p54nrb/NonO. Mol Cell Biol. 1997 Feb;17(2):677–686. doi: 10.1128/mcb.17.2.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bennett M., Michaud S., Kingston J., Reed R. Protein components specifically associated with prespliceosome and spliceosome complexes. Genes Dev. 1992 Oct;6(10):1986–2000. doi: 10.1101/gad.6.10.1986. [DOI] [PubMed] [Google Scholar]
  9. Branlant C., Krol A., Lazar E., Haendler B., Jacob M., Galego-Dias L., Pousada C. High evolutionary conservation of the secondary structure and of certain nucleotide sequences of U5 RNA. Nucleic Acids Res. 1983 Dec 10;11(23):8359–8367. doi: 10.1093/nar/11.23.8359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Burd C. G., Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science. 1994 Jul 29;265(5172):615–621. doi: 10.1126/science.8036511. [DOI] [PubMed] [Google Scholar]
  11. Chiara M. D., Palandjian L., Feld Kramer R., Reed R. Evidence that U5 snRNP recognizes the 3' splice site for catalytic step II in mammals. EMBO J. 1997 Aug 1;16(15):4746–4759. doi: 10.1093/emboj/16.15.4746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chua K., Reed R. Human step II splicing factor hSlu7 functions in restructuring the spliceosome between the catalytic steps of splicing. Genes Dev. 1999 Apr 1;13(7):841–850. doi: 10.1101/gad.13.7.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Coolidge C. J., Patton J. G. Run-around PCR: a novel way to create duplications using polymerase chain reaction. Biotechniques. 1995 May;18(5):762–764. [PubMed] [Google Scholar]
  14. Dong B., Horowitz D. S., Kobayashi R., Krainer A. R. Purification and cDNA cloning of HeLa cell p54nrb, a nuclear protein with two RNA recognition motifs and extensive homology to human splicing factor PSF and Drosophila NONA/BJ6. Nucleic Acids Res. 1993 Aug 25;21(17):4085–4092. doi: 10.1093/nar/21.17.4085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dye B. T., Buvoli M., Mayer S. A., Lin C. H., Patton J. G. Enhancer elements activate the weak 3' splice site of alpha-tropomyosin exon 2. RNA. 1998 Dec;4(12):1523–1536. doi: 10.1017/s1355838298980360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dye B. T., Patton J. G. An RNA recognition motif (RRM) is required for the localization of PTB-associated splicing factor (PSF) to subnuclear speckles. Exp Cell Res. 2001 Feb 1;263(1):131–144. doi: 10.1006/excr.2000.5097. [DOI] [PubMed] [Google Scholar]
  17. Fabrizio P., Laggerbauer B., Lauber J., Lane W. S., Lührmann R. An evolutionarily conserved U5 snRNP-specific protein is a GTP-binding factor closely related to the ribosomal translocase EF-2. EMBO J. 1997 Jul 1;16(13):4092–4106. doi: 10.1093/emboj/16.13.4092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fields S., Song O. A novel genetic system to detect protein-protein interactions. Nature. 1989 Jul 20;340(6230):245–246. doi: 10.1038/340245a0. [DOI] [PubMed] [Google Scholar]
  19. Fong N., Bentley D. L. Capping, splicing, and 3' processing are independently stimulated by RNA polymerase II: different functions for different segments of the CTD. Genes Dev. 2001 Jul 15;15(14):1783–1795. doi: 10.1101/gad.889101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fong Y. W., Zhou Q. Stimulatory effect of splicing factors on transcriptional elongation. Nature. 2001 Dec 20;414(6866):929–933. doi: 10.1038/414929a. [DOI] [PubMed] [Google Scholar]
  21. Fox Archa H., Lam Yun Wah, Leung Anthony K. L., Lyon Carol E., Andersen Jens, Mann Matthias, Lamond Angus I. Paraspeckles: a novel nuclear domain. Curr Biol. 2002 Jan 8;12(1):13–25. doi: 10.1016/s0960-9822(01)00632-7. [DOI] [PubMed] [Google Scholar]
  22. Fu X. D. The superfamily of arginine/serine-rich splicing factors. RNA. 1995 Sep;1(7):663–680. [PMC free article] [PubMed] [Google Scholar]
  23. Ghetti A., Company M., Abelson J. Specificity of Prp24 binding to RNA: a role for Prp24 in the dynamic interaction of U4 and U6 snRNAs. RNA. 1995 Apr;1(2):132–145. [PMC free article] [PubMed] [Google Scholar]
  24. Gozani O., Patton J. G., Reed R. A novel set of spliceosome-associated proteins and the essential splicing factor PSF bind stably to pre-mRNA prior to catalytic step II of the splicing reaction. EMBO J. 1994 Jul 15;13(14):3356–3367. doi: 10.1002/j.1460-2075.1994.tb06638.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Guthrie C., Patterson B. Spliceosomal snRNAs. Annu Rev Genet. 1988;22:387–419. doi: 10.1146/annurev.ge.22.120188.002131. [DOI] [PubMed] [Google Scholar]
  26. Hallier M., Tavitian A., Moreau-Gachelin F. The transcription factor Spi-1/PU.1 binds RNA and interferes with the RNA-binding protein p54nrb. J Biol Chem. 1996 May 10;271(19):11177–11181. doi: 10.1074/jbc.271.19.11177. [DOI] [PubMed] [Google Scholar]
  27. Hastings M. L., Krainer A. R. Pre-mRNA splicing in the new millennium. Curr Opin Cell Biol. 2001 Jun;13(3):302–309. doi: 10.1016/s0955-0674(00)00212-x. [DOI] [PubMed] [Google Scholar]
  28. Hinz M., Moore M. J., Bindereif A. Domain analysis of human U5 RNA. Cap trimethylation, protein binding, and spliceosome assembly. J Biol Chem. 1996 Aug 2;271(31):19001–19007. doi: 10.1074/jbc.271.31.19001. [DOI] [PubMed] [Google Scholar]
  29. Horowitz D. S., Abelson J. A U5 small nuclear ribonucleoprotein particle protein involved only in the second step of pre-mRNA splicing in Saccharomyces cerevisiae. Mol Cell Biol. 1993 May;13(5):2959–2970. doi: 10.1128/mcb.13.5.2959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Horowitz D. S., Krainer A. R. A human protein required for the second step of pre-mRNA splicing is functionally related to a yeast splicing factor. Genes Dev. 1997 Jan 1;11(1):139–151. doi: 10.1101/gad.11.1.139. [DOI] [PubMed] [Google Scholar]
  31. Imai Y., Matsushima Y., Sugimura T., Terada M. A simple and rapid method for generating a deletion by PCR. Nucleic Acids Res. 1991 May 25;19(10):2785–2785. doi: 10.1093/nar/19.10.2785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Jones K. R., Rubin G. M. Molecular analysis of no-on-transient A, a gene required for normal vision in Drosophila. Neuron. 1990 May;4(5):711–723. doi: 10.1016/0896-6273(90)90197-n. [DOI] [PubMed] [Google Scholar]
  33. Jurica Melissa S., Licklider Lawrence J., Gygi Steven R., Grigorieff Nikolaus, Moore Melissa J. Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA. 2002 Apr;8(4):426–439. doi: 10.1017/s1355838202021088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Konarska M. M., Sharp P. A. Interactions between small nuclear ribonucleoprotein particles in formation of spliceosomes. Cell. 1987 Jun 19;49(6):763–774. doi: 10.1016/0092-8674(87)90614-3. [DOI] [PubMed] [Google Scholar]
  35. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  36. Laggerbauer B., Achsel T., Lührmann R. The human U5-200kD DEXH-box protein unwinds U4/U6 RNA duplices in vitro. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4188–4192. doi: 10.1073/pnas.95.8.4188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Lauber J., Fabrizio P., Teigelkamp S., Lane W. S., Hartmann E., Luhrmann R. The HeLa 200 kDa U5 snRNP-specific protein and its homologue in Saccharomyces cerevisiae are members of the DEXH-box protein family of putative RNA helicases. EMBO J. 1996 Aug 1;15(15):4001–4015. [PMC free article] [PubMed] [Google Scholar]
  38. Lindsey L. A., Garcia-Blanco M. A. Functional conservation of the human homolog of the yeast pre-mRNA splicing factor Prp17p. J Biol Chem. 1998 Dec 4;273(49):32771–32775. doi: 10.1074/jbc.273.49.32771. [DOI] [PubMed] [Google Scholar]
  39. Lynch K. W., Maniatis T. Synergistic interactions between two distinct elements of a regulated splicing enhancer. Genes Dev. 1995 Feb 1;9(3):284–293. doi: 10.1101/gad.9.3.284. [DOI] [PubMed] [Google Scholar]
  40. MacMillan A. M., Query C. C., Allerson C. R., Chen S., Verdine G. L., Sharp P. A. Dynamic association of proteins with the pre-mRNA branch region. Genes Dev. 1994 Dec 15;8(24):3008–3020. doi: 10.1101/gad.8.24.3008. [DOI] [PubMed] [Google Scholar]
  41. Maniatis Tom, Reed Robin. An extensive network of coupling among gene expression machines. Nature. 2002 Apr 4;416(6880):499–506. doi: 10.1038/416499a. [DOI] [PubMed] [Google Scholar]
  42. Maroney P. A., Romfo C. M., Nilsen T. W. Functional recognition of 5' splice site by U4/U6.U5 tri-snRNP defines a novel ATP-dependent step in early spliceosome assembly. Mol Cell. 2000 Aug;6(2):317–328. doi: 10.1016/s1097-2765(00)00032-0. [DOI] [PubMed] [Google Scholar]
  43. Mathews D. H., Sabina J., Zuker M., Turner D. H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol. 1999 May 21;288(5):911–940. doi: 10.1006/jmbi.1999.2700. [DOI] [PubMed] [Google Scholar]
  44. Mathur M., Tucker P. W., Samuels H. H. PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors. Mol Cell Biol. 2001 Apr;21(7):2298–2311. doi: 10.1128/MCB.21.7.2298-2311.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. McConnell T. S., Steitz J. A. Proximity of the invariant loop of U5 snRNA to the second intron residue during pre-mRNA splicing. EMBO J. 2001 Jul 2;20(13):3577–3586. doi: 10.1093/emboj/20.13.3577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Meissner M., Dechat T., Gerner C., Grimm R., Foisner R., Sauermann G. Differential nuclear localization and nuclear matrix association of the splicing factors PSF and PTB. J Cell Biochem. 2000 Jan;76(4):559–566. [PubMed] [Google Scholar]
  47. Miralles F., Ofverstedt L. G., Sabri N., Aissouni Y., Hellman U., Skoglund U., Visa N. Electron tomography reveals posttranscriptional binding of pre-mRNPs to specific fibers in the nucleoplasm. J Cell Biol. 2000 Jan 24;148(2):271–282. doi: 10.1083/jcb.148.2.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Monsalve M., Wu Z., Adelmant G., Puigserver P., Fan M., Spiegelman B. M. Direct coupling of transcription and mRNA processing through the thermogenic coactivator PGC-1. Mol Cell. 2000 Aug;6(2):307–316. doi: 10.1016/s1097-2765(00)00031-9. [DOI] [PubMed] [Google Scholar]
  49. Newman A. J. The role of U5 snRNP in pre-mRNA splicing. EMBO J. 1997 Oct 1;16(19):5797–5800. doi: 10.1093/emboj/16.19.5797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. O'Keefe R. T., Newman A. J. Functional analysis of the U5 snRNA loop 1 in the second catalytic step of yeast pre-mRNA splicing. EMBO J. 1998 Jan 15;17(2):565–574. doi: 10.1093/emboj/17.2.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Patton J. G., Mayer S. A., Tempst P., Nadal-Ginard B. Characterization and molecular cloning of polypyrimidine tract-binding protein: a component of a complex necessary for pre-mRNA splicing. Genes Dev. 1991 Jul;5(7):1237–1251. doi: 10.1101/gad.5.7.1237. [DOI] [PubMed] [Google Scholar]
  52. Patton J. G., Porro E. B., Galceran J., Tempst P., Nadal-Ginard B. Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev. 1993 Mar;7(3):393–406. doi: 10.1101/gad.7.3.393. [DOI] [PubMed] [Google Scholar]
  53. Patton J. R. Pseudouridine modification of U5 RNA in ribonucleoprotein particles assembled in vitro. Mol Cell Biol. 1991 Dec;11(12):5998–6006. doi: 10.1128/mcb.11.12.5998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Pérez I., Lin C. H., McAfee J. G., Patton J. G. Mutation of PTB binding sites causes misregulation of alternative 3' splice site selection in vivo. RNA. 1997 Jul;3(7):764–778. [PMC free article] [PubMed] [Google Scholar]
  55. Reed R. Mechanisms of fidelity in pre-mRNA splicing. Curr Opin Cell Biol. 2000 Jun;12(3):340–345. doi: 10.1016/s0955-0674(00)00097-1. [DOI] [PubMed] [Google Scholar]
  56. Reyes J. L., Kois P., Konforti B. B., Konarska M. M. The canonical GU dinucleotide at the 5' splice site is recognized by p220 of the U5 snRNP within the spliceosome. RNA. 1996 Mar;2(3):213–225. [PMC free article] [PubMed] [Google Scholar]
  57. Sewer Marion B., Nguyen Viet Q., Huang Ching-Jung, Tucker Philip W., Kagawa Norio, Waterman Michael R. Transcriptional activation of human CYP17 in H295R adrenocortical cells depends on complex formation among p54(nrb)/NonO, protein-associated splicing factor, and SF-1, a complex that also participates in repression of transcription. Endocrinology. 2002 Apr;143(4):1280–1290. doi: 10.1210/endo.143.4.8748. [DOI] [PubMed] [Google Scholar]
  58. Staley J. P., Guthrie C. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell. 1998 Feb 6;92(3):315–326. doi: 10.1016/s0092-8674(00)80925-3. [DOI] [PubMed] [Google Scholar]
  59. Straub T., Grue P., Uhse A., Lisby M., Knudsen B. R., Tange T. O., Westergaard O., Boege F. The RNA-splicing factor PSF/p54 controls DNA-topoisomerase I activity by a direct interaction. J Biol Chem. 1998 Oct 9;273(41):26261–26264. doi: 10.1074/jbc.273.41.26261. [DOI] [PubMed] [Google Scholar]
  60. Straub T., Knudsen B. R., Boege F. PSF/p54(nrb) stimulates "jumping" of DNA topoisomerase I between separate DNA helices. Biochemistry. 2000 Jun 27;39(25):7552–7558. doi: 10.1021/bi992898e. [DOI] [PubMed] [Google Scholar]
  61. Ségault V., Will C. L., Polycarpou-Schwarz M., Mattaj I. W., Branlant C., Lührmann R. Conserved loop I of U5 small nuclear RNA is dispensable for both catalytic steps of pre-mRNA splicing in HeLa nuclear extracts. Mol Cell Biol. 1999 Apr;19(4):2782–2790. doi: 10.1128/mcb.19.4.2782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Teigelkamp S., Mundt C., Achsel T., Will C. L., Lührmann R. The human U5 snRNP-specific 100-kD protein is an RS domain-containing, putative RNA helicase with significant homology to the yeast splicing factor Prp28p. RNA. 1997 Nov;3(11):1313–1326. [PMC free article] [PubMed] [Google Scholar]
  63. Traish A. M., Huang Y. H., Ashba J., Pronovost M., Pavao M., McAneny D. B., Moreland R. B. Loss of expression of a 55 kDa nuclear protein (nmt55) in estrogen receptor-negative human breast cancer. Diagn Mol Pathol. 1997 Aug;6(4):209–221. doi: 10.1097/00019606-199708000-00005. [DOI] [PubMed] [Google Scholar]
  64. Tuerk C., Gold L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science. 1990 Aug 3;249(4968):505–510. doi: 10.1126/science.2200121. [DOI] [PubMed] [Google Scholar]
  65. Urban R. J., Bodenburg Y., Kurosky A., Wood T. G., Gasic S. Polypyrimidine tract-binding protein-associated splicing factor is a negative regulator of transcriptional activity of the porcine p450scc insulin-like growth factor response element. Mol Endocrinol. 2000 Jun;14(6):774–782. doi: 10.1210/mend.14.6.0485. [DOI] [PubMed] [Google Scholar]
  66. Valcárcel J., Gaur R. K., Singh R., Green M. R. Interaction of U2AF65 RS region with pre-mRNA branch point and promotion of base pairing with U2 snRNA [corrected]. Science. 1996 Sep 20;273(5282):1706–1709. doi: 10.1126/science.273.5282.1706. [DOI] [PubMed] [Google Scholar]
  67. Vijayraghavan U., Abelson J. PRP18, a protein required for the second reaction in pre-mRNA splicing. Mol Cell Biol. 1990 Jan;10(1):324–332. doi: 10.1128/mcb.10.1.324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wurtz-T, Kiseleva E., Nacheva G., Alzhanova-Ericcson A., Rosén A., Daneholt B. Identification of two RNA-binding proteins in Balbiani ring premessenger ribonucleoprotein granules and presence of these proteins in specific subsets of heterogeneous nuclear ribonucleoprotein particles. Mol Cell Biol. 1996 Apr;16(4):1425–1435. doi: 10.1128/mcb.16.4.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Yang Y. S., Hanke J. H., Carayannopoulos L., Craft C. M., Capra J. D., Tucker P. W. NonO, a non-POU-domain-containing, octamer-binding protein, is the mammalian homolog of Drosophila nonAdiss. Mol Cell Biol. 1993 Sep;13(9):5593–5603. doi: 10.1128/mcb.13.9.5593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Zamore P. D., Patton J. G., Green M. R. Cloning and domain structure of the mammalian splicing factor U2AF. Nature. 1992 Feb 13;355(6361):609–614. doi: 10.1038/355609a0. [DOI] [PubMed] [Google Scholar]
  71. Zhang W. W., Zhang L. X., Busch R. K., Farrés J., Busch H. Purification and characterization of a DNA-binding heterodimer of 52 and 100 kDa from HeLa cells. Biochem J. 1993 Feb 15;290(Pt 1):267–272. doi: 10.1042/bj2900267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Zhang Z., Carmichael G. G. The fate of dsRNA in the nucleus: a p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell. 2001 Aug 24;106(4):465–475. doi: 10.1016/s0092-8674(01)00466-4. [DOI] [PubMed] [Google Scholar]
  73. Zhou Z., Reed R. Human homologs of yeast prp16 and prp17 reveal conservation of the mechanism for catalytic step II of pre-mRNA splicing. EMBO J. 1998 Apr 1;17(7):2095–2106. doi: 10.1093/emboj/17.7.2095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. von Besser H., Schnabel P., Wieland C., Fritz E., Stanewsky R., Saumweber H. The puff-specific Drosophila protein Bj6, encoded by the gene no-on transient A, shows homology to RNA-binding proteins. Chromosoma. 1990 Dec;100(1):37–47. doi: 10.1007/BF00337601. [DOI] [PubMed] [Google Scholar]