A family of RS domain proteins with novel subcellular localization and trafficking

Nucleic Acids Research

Volumn 33, Issue 4, 2005, Pages 1309-1322

  Kavanagh, Steven J ^a   Schulz, T C Thomas C ^a   Davey, Philippa ^a   Claudianos, Charles ^b   Russell, Carrie ^a   Rathjen, Peter D ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c National Stem Cell Centre   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; PROTEIN PSC1; UNCLASSIFIED DRUG; COMPLEMENTARY DNA; NUCLEAR PROTEIN; PROTEIN; PSC1 PROTEIN, MOUSE; RNA BINDING PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CELL NUCLEUS; CELL ORGANELLE; CELL POPULATION; CONTROLLED STUDY; CYTOPLASM; GENE CONTROL; GENE SEQUENCE; GENETIC CONSERVATION; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TRANSPORT; RNA METABOLISM; SEQUENCE HOMOLOGY; VERTEBRATE; ACTIVE TRANSPORT; ANIMAL; BINDING SITE; CELL STRAIN COS1; CERCOPITHECUS; CHEMISTRY; ISOLATION AND PURIFICATION; METABOLISM; MICROTUBULE; MOLECULAR GENETICS; MOUSE; PROTEIN TERTIARY STRUCTURE;

VERTEBRATA;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL NUCLEUS; CELL NUCLEUS STRUCTURES; CERCOPITHECUS AETHIOPS; CONSERVED SEQUENCE; COS CELLS; CYTOPLASM; CYTOPLASMIC STRUCTURES; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; MICE; MICROTUBULES; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RNA-BINDING PROTEINS;

EID: 14844364471     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gki269     Document Type: Article

References (76)

1. Boucher,L., Ouzounis,C.A., Enright,A.J. and Blencowe,B.J. (2001) A genome-wide survey of RS domain proteins. RNA, 7, 1693-1701.
2. Graveley,B.R. (2000) Sorting out the complexity of SR protein functions. RNA, 6, 1197-1211.
3. Tacke,R. and Manley,J.L. (1999) Determinants of SR protein specificity. Curr. Opin. Cell Biol., 11, 358-362.
4. Valcarcel,J. and Green,M.R. (1996) The SR protein family: Pleiotropic functions in pre-mRNA splicing. Trends Biochem. Sci., 21, 296-301.
5. Fu,X.-D. (1995) The superfamily of arginine/serine rich splicing factors. RNA, 1, 663-680.
6. Hedley,M.L., Amrein,H. and Maniatis,T. (1995) An amino acid sequence motif sufficient for subnuclear localization of an arginine/serine-rich splicing factor. Proc. Natl Acad. Sci. USA, 92, 11524-11528.
7. Fu,X.-D. and Maniatis,T. (1990) Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature, 343, 437-441.
8. Lamond,A.I. and Spector,D.L. (2003) Nuclear speckles: A model for nuclear organelles. Nature Rev. Mol. Cell Biol., 4, 605-612.
9. Jimenez-Garcia,L.F. and Spector,D.L. (1993) In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism. Cell, 73, 47-59.
10. Misteli,T., Caceres,J.F. and Spector,D.L. (1997) The dynamics of a pre-mRNA splicing factor in living cells. Nature, 387, 523-527.
11. Bregman,D.B., Du,L., van der Zee,S. and Warren,S.L. (1995) Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol., 129 287-298.
12. Dostie,J., Lejbkowicz,F. and Sonenberg,N. (2000) Nuclear eukaryotic initiation factor 4E (eIF4E) colocalizes with splicing factors in speckles. J. Cell Biol., 148, 239-247.
13. Zhao,K., Wang,W., Rando,O.J., Xue,Y., Swiderek,K., Kuo,A. and Crabtree,G.R. (1998) Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell, 95, 625-636.
14. Manley,J.L. and Tacke,R. (1996) SR proteins and splicing control. Genes Dev., 10, 1569-1579.
15. Graveley,B.R. (2004) A protein interaction domain contacts RNA in the prespliceosome. Mol. Cell, 13, 302-30416.
16. Allemand,E., Dokudovskaya,S., Bordonne,R. and Tazi,J. (2002) A conserved Drosophila transportin-serine/arginine-rich (SR) protein permits nuclear import of Drosophila SR protein splicing factors and their antagonist repressor splicing factor 1. Mol. Biol. Cell, 13, 2436-2447.
17. Kataoka,N., Bachorik,J.L. and Dreyfuss,G.J. (1999) Transportin-SR, a nuclear import receptor for SR proteins. Cell Biol., 145, 1145-1152.
18. Lai,M.C., Lin,R.I. and Tarn,W.Y. (2001) Transportin-SR2 mediates nuclear import of phosphorylated SR proteins. Proc. Natl Acad. Sci. USA, 98, 10154-10159.
19. Li,H. and Bingham,P.M. (1991) Arginine/serine-rich domains of the su(wa) and tra RNA processing regulators target proteins to a subnuclear compartment implicated in splicing. Cell, 18, 335-342.
20. Philipps,D., Celotto,A.M., Wang,Q.Q., Tarng,R.S. and Graveley,B.R. (2003) Arginine/serine repeats are sufficient to constitute a splicing activation domain. Nucleic Acids Res., 15, 6502-6508.
21. Caceres,J.F., Misteli,T., Screaton,G.R., Spector,D.L. and Krainer,A.R. (1997) Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J. Cell Biol., 138, 225-238.
22. Caceres,J.F., Screaton,G.R. and Krainer,A.R. (1998) A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev., 12, 55-66.
23. Sanford,J.R. and Bruzik,J.P. (2001) Regulation of SR protein localization during development. Proc. Natl Acad. Sci. USA, 98 10184-10189.
24. Huang,Y., Yario,T.A. and Steitz,J.A. (2004) A molecular link between SR protein dephosphorylation and mRNA export. Proc. Natl Acad. Sci. USA 101, 9666-9670.
25. Gilbert,W. and Guthrie,C. (2004) The Glc7p nuclear phosphatase promotes mRNA export by facilitating association of Mex67p with mRNA. Mol. Cell, 13, 201-212.
26. Tacke,R., Chen,Y. and Manley,J.L. (1997) Sequence specific RNA binding by an SR protein requires RS domain phosphorylation: Creation of an SRp40 specific splicing enhancer. Proc. Natl Acad. Sci. USA, 94 1148-1153.
27. Pelton,T.A., Sharma,S., Schulz,T.C., Rathjen,J. and Rathjen,P.D. (2002) Transient pluripotent cell populations during primitive ectoderm formation: Correlation of in vivo and in vitro pluripotent cell development. J. Cell Sci., 115, 329-339.
28. Chapman,G. and Rathjen,P.D. (1995) Sequence and evolutionary conservation of the murine Gbx-2 homeobox gene. FEBS Lett., 364 289-292.
29. Stockham,C., Wang,L.S. and Warnow,T. (2002) Statistically based postprocessing of phylogenetic analysis by clustering. Bioinformatics 18(Suppl. 1), 285-293.
30. Rathjen,P.D., Toth,S., Willis,A., Heath,J.K. and Smith,A.G. (1990) Differentiation inhibiting activity is produced in matrix-associated and diffusible forms that are generated by alternate promoter usage. Cell 62, 1105-1114.
31. Rathjen,J., Lake,J.A., Bettess,M.D., Washington,J.M., Chapman,G. and Rathjen,P.D. (1999) Formation of a primitive ectoderm like cell population, EPL cells, from ES cells in response to biologically derived factors. J. Cell Sci., 112, 601-612.
32. Durand,R.E. and Olive,P.L. (1982) Cytotoxicity, mutagenicity and DNA damage by Hoechst 33342. J. Histochem. Cytochem., 30, 111-116.
33. Zuccotti,M., Ponce,R.H., Boiani,M., Guizzardi,S., Govoni,P., Scandroglio,R., Garagna,S. and Redi,C.A. (2002) The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote, 10, 73-78.
34. Krainer,A.R., Conway,G.C. and Kozak,D. (1990) Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev., 4, 1158-1171.
35. Nagase,T., Kikuno,R., Ishikawa,K.I., Hirosawa,M. and Ohara,O. (2000) Prediction of the coding sequences of unidentified human genes. XVI. The complete sequences of 150 new cDNA clones from brain which code for large proteins in vitro. DNA Res., 7, 65-73.
36. Gonzalez-Santos,J.M., Wang,A., Jones,J., Ushida,C., Liu,J. and Hu,J. (2002) Central region of the human splicing factor Hprp3p interacts with Hprp4p. J. Biol. Chem., 277, 23764-23772.
37. Screaton,G.R., Caceres,J.F., Mayeda,A., Bell,M.V., Plebanski,M., Jackson,D.G., Bell,J.I. and Krainer,A.R. (1995) Identification and characterization of three members of the human SR family of pre-mRNA splicing factors. EMBO J., 14, 4336-4349.
38. Marchler-Bauer,A., Anderson,J.B., DeWeese-Scott,C., Fedorova,N.D., Geer,L.Y., He,S., Hurwitz,D.I., Jackson,J.D., Jacobs,A.R., Lanczycki, C.J. et al. (2003) CDD: A curated Entrez database of conserved domain alignments. Nucleic Acids Res., 31, 383-387.
39. Misteli,T. and Spector,D.L. (1998) The cellular organization of gene expression. Curr. Opin. Cell Biol., 10, 323-331.
40. Carninci,P. and Hayashizaki,Y. (1999) High-efficiency full-length cDNA cloning. Meth. Enzymol., 303, 19-44.
41. Eichmüller,S., Usener,D., Dummer,R., Stein,A., Thiel,D. and Schadendorf,D. (2001) Serological detection of cutaneous T-cell lymphoma-associated antigens. Proc. Natl Acad. Sci. USA, 98, 629-634.
42. Graham,F.L. and Prevec,L. (1991) Manipulation of adenovirus vectors. Methods Mol. Biol., 7, 109-128.
43. Rodda,S., Sharma,S., Scherer,M., Chapman,G. and Rathjen,P. (2001) CRTR-1, a developmentally regulated transcriptional repressor related to the CP2 family of transcription factors. J. Biol. Chem., 276 3324-3332.
44. Igel,H., Wells,S., Perriman,R. and Ares,M.,Jr (1998) Conservation of structure and subunit interactions in yeast homologues of splicing factor 3b (SF3b) subunits. RNA, 4, 1-10.
45. Zahler,A.M., Neugebauer,K.M., Lane,W.S. and Roth,M.B. (1993) Distinct functions of SR proteins in alternative pre-mRNA splicing. Science 260, 219-222.
46. Jiang,Z.-H., Zhang,W.-J., Rao,Y. and Wu,J.Y. (1998) Regulation of Ich-1 pre mRNA alternative splicing and apoptosis by mammalian splicing factors. Proc. Natl Acad. Sci. USA, 95, 9155-9160.
47. Jumaa,H., Wei,G. and Nielson,P.J. (1999) Blastocyst formation is blocked in mouse embryos lacking the splicing factor SRp20. Curr. Biol., 9, 899-902.
48. Yang,L., Embree,L.J. and Hickstein,D.D. (2000) TLS-ERG leukemia fusion protein inhibits RNA splicing mediated by serine-arginine proteins. Mol. Cell. Biol., 20, 3345-3354.
49. Young,P.J., DiDonato,C.J., Hu,D., Kothary,R., Androphy,E.J. and Lorson,C.L. (2002) SRp30c-dependent stimulation of survival motor neuron (SMN) exon 7 inclusion is facilitated by a direct interaction with hTra2 beta 1. Hum. Mol. Genet., 11, 577-587.
50. Kataoka,N., Bachorik,J.L. and Dreyfuss,G. (1999) Transportin-SR, a nuclear import receptor for SR proteins. J. Cell Biol., 145, 1145-11452.
51. Bouvet,P., Diaz,J.J., Kindbeiter,K., Madjar,J.J. and Amalric,F. (1998) Nucleolin interacts with several ribosomal proteins through its RGG domain. J. Biol. Chem., 273, 19025-19029.
52. Miller,M.M. and Read,L.K. (2003) Trypanosoma brucei: Functions of RBP16 cold shock and RGG domains in macromolecular interactions. Exp. Parasitol., 105, 140-148.
53. Burd,C.G. and Dreyfuss,G. (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science, 265, 615-621.
54. Gendra,E., Moreno,A., Alba,M.M. and Pages,M. (2004) Interaction of the plant glycine-rich RNA-binding protein MA16 with a novel nucleolar DEAD box RNA helicase protein from Zea mays. Plant J., 38, 875-886.
55. Heine,M.A., Rankin,M.L. and DiMario,P.J. (1993) The Gly/Arg-rich (GAR) domain of Xenopus nucleolin facilitates in vitro nucleic acid binding and in vivo nucleolar localization. Mol. Biol. Cell, 4, 1189-1204.
56. Gall,J.G. (2001) A role for Cajal bodies in assembly of the nuclear transcription machinery. FEBS Lett., 498, 164-167.
57. Zhang,G., Taneja,K.L., Singer,R.H. and Green,M.R. (1994) Localization of pre-mRNA splicing in mammalian nuclei. Nature, 372, 809-812.
58. Puvion-Dutilleul,F., Bachellerie,J.P., Visa,N. and Puvion,E. (1994) Rearrangements of intranuclear structures involved in RNA processing in response to adenovirus infection. J. Cell Sci., 107, 1457-1468.
59. Cmarko,D., Verschure,P.J., Martin,T.E., Dahmus,M.E., Krause,S., Fu,X.-D., van Driel,R. and Fakan,S. (1999) Ultrastructural analysis of transcription and splicing in the cell nucleus after bromo-UTP microinjection. Mol. Biol. Cell, 10, 211-223.
60. Herrmann,C.H. and Mancini,M.A. (2001) The Cdk9 and cyclin T subunits of TAK/P-TEFb localize to splicing factor-rich nuclear speckle regions. J. Cell Sci., 114, 1491-1503.
61. Xing,Y., Johnson,C.V., Moen,P.T., McNeil,J.A. and Lawrence,J. (1995) Nonrandom gene organization: Structural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains. J. Cell Biol. 131, 1635-1647.
62. Mintz,P.J. and Spector,D.L. (2000) Compartmentalization of RNA processing factors within nuclear speckles. J. Struct. Biol., 129, 241-251.
63. Gourlay,C.W., Dewar,H., Warren,D.T., Costa,R., Satish,N. and Ayscough,K.R. (2003) An interaction between Sla1p and Sla2p plays a role in regulating actin dynamics and endocytosis in budding yeast. J. Cell Sci., 116, 2551-2564.
64. Cazalla,D., Zhu,J., Manche,L., Huber,E., Krainer,A.R. and Caceres,J.F. (2002) Nuclear export and retention signals in the RS domain of SR proteins. Mol. Cell. Biol., 22, 6871-6882.
65. Eystathioy,T., Chan,E.K., Takeuchi,K., Mahler,M., Luft,L.M., Zochodne,D.W. and Fritzler,M.J. (2003) Clinical and serological associations of autoantibodies to GW bodies and a novel cytoplasmic autoantigen GW182. J. Mol. Med., 81, 811-818.
66. Cougot,N., Babajko,S. and Seraphin,B. (2004) Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol., 165, 31-40.
67. Kedersha,N. and Anderson,P. (2002) Stress granules: Sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans., 30, 963-969.
68. Carson,J.H., Cui,H. and Barbarese,E. (2001) The balance of power in RNA trafficking. Curr. Opin. Neurobiol., 11, 558-563.
69. Barbarese,E., Koppel,D.E., Deutscher,M.P., Smith,C.L., Ainger,K., Morgan,F. and Carson,J.H. (1995) Protein translation components are colocalized in granules in oligodendrocytes. J. Cell Sci., 108 2781-2790.
70. Carson,J.H., Worboys,K., Ainger,K. and Barbarese,E. (1997) Translocation of myelin basic protein mRNA in oligodendrocytes requires microtubules and kinesin. Cell Motil. Cytoskeleton, 38, 318-328.
71. Schuman,E.M. (1999) mRNA trafficking and local protein synthesis at the synapse. Neuron, 23, 645-648.
72. Fusco,D., Accornero,N., Lavoie,B., Shenoy,S.M., Blanchard,J.M., Singer,R.H. and Bertrand,E. (2003) Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Curr. Biol., 13, 161-167.
73. Mouland,A.J., Xu,H., Cui,H., Krueger,W., Munro,T.P., Prasol,M., Mercier,J., Rekosh,D., Smith,R. and Barbarese,E. (2001) RNA trafficking signals in human immunodeficiency virus type 1. Mol. Cell. Biol., 21, 2133-2143.
74. Ligon,L.A., Tokito,M., Finklestein,J.M., Grossman,F.E. and Holzbaur,E.L. (2004) A direct interaction between cytoplasmic dynein and kinesin I may coordinate motor activity. J. Biol. Chem., 279, 19201-19208.
75. Shaw,S.L., Kamyar,R. and Ehrhardt,D.W. (2003) Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science, 300 1715-1718.
76. Swofford,D.L. (2000) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.