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PMID: 15121844 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S.

The splicing factor U2AF small subunit is functionally conserved between fission yeast and humans.

Molecular and cellular biology ·Vol. 24 ·No. 10 ·2004-05-00 ·Pages 4229-40

Webb CJ, Wise JA

Abstract

The small subunit of U2AF, which functions in 3' splice site recognition, is more highly conserved than its heterodimeric partner yet is less thoroughly investigated. Remarkably, we find that the small subunit of Schizosaccharomyces pombe U2AF (U2AF(SM)) can be replaced in vivo by its human counterpart, demonstrating that the conservation extends to function. Precursor mRNAs accumulate in S. pombe following U2AF(SM) depletion in a time frame consistent with a role in splicing. A comprehensive mutational analysis reveals that all three conserved domains are required for viability. Notably, however, a tryptophan in the pseudo-RNA recognition motif implicated in a key contact with the large subunit by crystallographic data is dispensable whereas amino acids implicated in RNA recognition are critical. Mutagenesis of the two zinc-binding domains demonstrates that they are neither equivalent nor redundant. Finally, two- and three-hybrid analyses indicate that mutations with effects on large-subunit interactions are rare whereas virtually all alleles tested diminished RNA binding by the heterodimer. In addition to demonstrating extraordinary conservation of U2AF small-subunit function, these results provide new insights into the roles of individual domains and residues.

MeSH Terms
Amino Acid Sequence Base Sequence Conserved Sequence DNA, Complementary/genetics Dimerization Humans Models, Molecular Molecular Sequence Data Mutagenesis, Site-Directed Nuclear Proteins/chemistry,genetics,metabolism Protein Structure, Tertiary Protein Subunits RNA Splicing Ribonucleoproteins/chemistry,genetics,metabolism Schizosaccharomyces/genetics,metabolism Schizosaccharomyces pombe Proteins/chemistry,genetics,metabolism Sequence Homology, Amino Acid Species Specificity Splicing Factor U2AF Two-Hybrid System Techniques
Chemicals
DNA, Complementary Nuclear Proteins Protein Subunits Ribonucleoproteins Schizosaccharomyces pombe Proteins Splicing Factor U2AF U2AF2 protein, human
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Webb Christopher J
Department of Molecular Biology and Microbiology, School of Medicine, Case Western Reserve University, Cleveland, Ohio 44106-4960, USA.
Wise Jo Ann
References (65)
65 references, click to expand
  1. GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in C. elegans.
    Dev Cell. 2002 Nov;3(5):697-710 PMID: 12431376
  2. The KH domain of the branchpoint sequence binding protein determines specificity for the pre-mRNA branchpoint sequence.
    RNA. 1998 Aug;4(8):998-1006 PMID: 9701290
  3. Multiple forms of the U2 small nuclear ribonucleoprotein auxiliary factor U2AF subunits expressed in higher plants.
    J Biol Chem. 1998 Dec 18;273(51):34603-10 PMID: 9852132
  4. Ribosomal protein S14 of Saccharomyces cerevisiae regulates its expression by binding to RPS14B pre-mRNA and to 18S rRNA.
    Mol Cell Biol. 1999 Jan;19(1):826-34 PMID: 9858605
  5. Molecular genetic analysis of U2AF59 in Schizosaccharomyces pombe: differential sensitivity of introns to mutational inactivation.
    RNA. 1999 Jan;5(1):49-65 PMID: 9917066
  6. Genome-wide bioinformatic and molecular analysis of introns in Saccharomyces cerevisiae.
    RNA. 1999 Feb;5(2):221-34 PMID: 10024174
  7. U2AF35 is encoded by an essential gene clustered in an operon with RRM/cyclophilin in Caenorhabditis elegans.
    RNA. 1999 Apr;5(4):487-94 PMID: 10199565
  8. Phosphorylation regulates in vivo interaction and molecular targeting of serine/arginine-rich pre-mRNA splicing factors.
    J Cell Biol. 1999 May 3;145(3):447-55 PMID: 10225947
  9. Srp2, an SR protein family member of fission yeast: in vivo characterization of its modular domains.
    Nucleic Acids Res. 1999 Jul 1;27(13):2618-26 PMID: 10373577
  10. Solution structures of the first and second RNA-binding domains of human U2 small nuclear ribonucleoprotein particle auxiliary factor (U2AF(65)).
    EMBO J. 1999 Aug 16;18(16):4523-34 PMID: 10449418
  11. Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana.
    Nucleic Acids Res. 2002 Feb 1;30(3):623-35 PMID: 11809873
  12. The genome sequence of Schizosaccharomyces pombe.
    Nature. 2002 Feb 21;415(6874):871-80 PMID: 11859360
  13. Induced folding of the U2AF35 RRM upon binding to U2AF65.
    FEBS Lett. 2002 Sep 25;528(1-3):171-6 PMID: 12297299
  14. Sex-lethal splicing autoregulation in vivo: interactions between SEX-LETHAL, the U1 snRNP and U2AF underlie male exon skipping.
    Development. 2003 Feb;130(3):463-71 PMID: 12490553
  15. Evidence for substrate-specific requirement of the splicing factor U2AF(35) and for its function after polypyrimidine tract recognition by U2AF(65).
    Mol Cell Biol. 1999 Dec;19(12):8263-71 PMID: 10567551
  16. PUF60: a novel U2AF65-related splicing activity.
    RNA. 1999 Dec;5(12):1548-60 PMID: 10606266
  17. Functional recognition of the 3' splice site AG by the splicing factor U2AF35.
    Nature. 1999 Dec 16;402(6763):832-5 PMID: 10617206
  18. Both subunits of U2AF recognize the 3' splice site in Caenorhabditis elegans.
    Nature. 1999 Dec 16;402(6763):835-8 PMID: 10617207
  19. Inhibition of msl-2 splicing by Sex-lethal reveals interaction between U2AF35 and the 3' splice site AG.
    Nature. 1999 Dec 16;402(6763):838-41 PMID: 10617208
  20. Intron recognition comes of AGe.
    Nat Struct Biol. 2000 Jan;7(1):14-6 PMID: 10625417
  21. Mechanisms of fidelity in pre-mRNA splicing.
    Curr Opin Cell Biol. 2000 Jun;12(3):340-5 PMID: 10801464
  22. Pre-messenger RNA processing factors in the Drosophila genome.
    J Cell Biol. 2000 Jul 24;150(2):F37-44 PMID: 10908584
  23. Evidence for splice site pairing via intron definition in Schizosaccharomyces pombe.
    Mol Cell Biol. 2000 Nov;20(21):7955-70 PMID: 11027266
  24. Pre-mRNA splicing in the absence of an SR protein RS domain.
    Genes Dev. 2000 Dec 15;14(24):3166-78 PMID: 11124808
  25. Structural basis for recognition of AU-rich element RNA by the HuD protein.
    Nat Struct Biol. 2001 Feb;8(2):141-5 PMID: 11175903
  26. Where does fission yeast sit on the tree of life?
    Genome Biol. 2000;1(2):REVIEWS1011 PMID: 11178233
  27. Expressing the human genome.
    Nature. 2001 Feb 15;409(6822):832-3 PMID: 11237001
  28. The fission yeast ortholog of the coregulator SKIP interacts with the small subunit of U2AF.
    Biochem Biophys Res Commun. 2001 Jun 29;284(5):1148-54 PMID: 11414703
  29. The role of U2AF35 and U2AF65 in enhancer-dependent splicing.
    RNA. 2001 Jun;7(6):806-18 PMID: 11421359
  30. A novel peptide recognition mode revealed by the X-ray structure of a core U2AF35/U2AF65 heterodimer.
    Cell. 2001 Sep 7;106(5):595-605 PMID: 11551507
  31. Dual function for U2AF(35) in AG-dependent pre-mRNA splicing.
    Mol Cell Biol. 2001 Nov;21(22):7673-81 PMID: 11604503
  32. Identification and characterization of Prp45p and Prp46p, essential pre-mRNA splicing factors.
    RNA. 2003 Jan;9(1):138-50 PMID: 12554883
  33. Unique features of the Trypanosoma cruzi U2AF35 splicing factor.
    Mol Biochem Parasitol. 2003 Apr 25;128(1):77-81 PMID: 12706799
  34. Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP.
    Mol Cell. 2003 Apr;11(4):965-76 PMID: 12718882
  35. Optimization of specificity in a cellular protein interaction network by negative selection.
    Nature. 2003 Dec 11;426(6967):676-80 PMID: 14668868
  36. Sucl+ encodes a predicted 13-kilodalton protein that is essential for cell viability and is directly involved in the division cycle of Schizosaccharomyces pombe.
    Mol Cell Biol. 1987 Jan;7(1):504-11 PMID: 3031478
  37. A factor, U2AF, is required for U2 snRNP binding and splicing complex assembly.
    Cell. 1988 Jan 29;52(2):207-19 PMID: 2963698
  38. U1 small nuclear RNA from Schizosaccharomyces pombe has unique and conserved features and is encoded by an essential single-copy gene.
    Mol Cell Biol. 1990 Jun;10(6):2874-81 PMID: 2188102
  39. Biochemical characterization of U2 snRNP auxiliary factor: an essential pre-mRNA splicing factor with a novel intranuclear distribution.
    EMBO J. 1991 Jan;10(1):207-14 PMID: 1824937
  40. Cloning and domain structure of the mammalian splicing factor U2AF.
    Nature. 1992 Feb 13;355(6361):609-14 PMID: 1538748
  41. Cloning and intracellular localization of the U2 small nuclear ribonucleoprotein auxiliary factor small subunit.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8769-73 PMID: 1388271
  42. Systematic mutational analysis of the yeast ACT1 gene.
    Genetics. 1992 Oct;132(2):337-50 PMID: 1427032
  43. TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility.
    Gene. 1993 Jan 15;123(1):131-6 PMID: 8422997
  44. Comparison of Schizosaccharomyces pombe expression systems.
    Nucleic Acids Res. 1993 Jun 25;21(12):2955-6 PMID: 8332516
  45. The conserved pre-mRNA splicing factor U2AF from Drosophila: requirement for viability.
    Science. 1993 Oct 22;262(5133):569-73 PMID: 7692602
  46. U2AF homolog required for splicing in vivo.
    Science. 1993 Oct 22;262(5133):573-5 PMID: 8211184
  47. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing.
    Cell. 1993 Dec 17;75(6):1061-70 PMID: 8261509
  48. The yeast MUD2 protein: an interaction with PRP11 defines a bridge between commitment complexes and U2 snRNP addition.
    Genes Dev. 1994 Apr 1;8(7):843-54 PMID: 7926772
  49. The Srp54 GTPase is essential for protein export in the fission yeast Schizosaccharomyces pombe.
    Mol Cell Biol. 1994 Dec;14(12):7839-54 PMID: 7969124
  50. RASMOL: biomolecular graphics for all.
    Trends Biochem Sci. 1995 Sep;20(9):374 PMID: 7482707
  51. Schizosaccharomyces pombe zfs1+ encoding a zinc-finger protein functions in the mating pheromone recognition pathway.
    Mol Biol Cell. 1995 Sep;6(9):1185-95 PMID: 8534915
  52. The small subunit of the splicing factor U2AF is conserved in fission yeast.
    Nucleic Acids Res. 1996 May 15;24(10):1849-54 PMID: 8657565
  53. Mutational analysis of U1 function in Schizosaccharomyces pombe: pre-mRNAs differ in the extent and nature of their requirements for this snRNA in vivo.
    RNA. 1996 May;2(5):404-18 PMID: 8665408
  54. The splicing factor U2AF35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing.
    Genes Dev. 1996 Jun 1;10(11):1356-68 PMID: 8647433
  55. A three-hybrid system to detect RNA-protein interactions in vivo.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8496-501 PMID: 8710898
  56. Mutations in the small subunit of the Drosophila U2AF splicing factor cause lethality and developmental defects.
    Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10333-7 PMID: 8816800
  57. Metal binding properties and secondary structure of the zinc-binding domain of Nup475.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13754-9 PMID: 8943007
  58. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast.
    Genetics. 1996 Dec;144(4):1425-36 PMID: 8978031
  59. Cloning of Caenorhabditis U2AF65: an alternatively spliced RNA containing a novel exon.
    Mol Cell Biol. 1997 Feb;17(2):946-53 PMID: 9001248
  60. Identification and characterization of srp1, a gene of fission yeast encoding a RNA binding domain and a RS domain typical of SR splicing factors.
    Nucleic Acids Res. 1998 Jan 15;26(2):505-11 PMID: 9421507
  61. Interaction between subunits of heterodimeric splicing factor U2AF is essential in vivo.
    Mol Cell Biol. 1998 Apr;18(4):1765-73 PMID: 9528748
  62. Molecular genetic analysis of the heterodimeric splicing factor U2AF: the RS domain on either the large or small Drosophila subunit is dispensable in vivo.
    Genes Dev. 1998 Apr 1;12(7):1010-21 PMID: 9531538
  63. RNA binding activity of heterodimeric splicing factor U2AF: at least one RS domain is required for high-affinity binding.
    Mol Cell Biol. 1998 Jul;18(7):4004-11 PMID: 9632785
  64. A potential role for U2AF-SAP 155 interactions in recruiting U2 snRNP to the branch site.
    Mol Cell Biol. 1998 Aug;18(8):4752-60 PMID: 9671485
  65. Pre-spliceosome formation in S.pombe requires a stable complex of SF1-U2AF(59)-U2AF(23).
    EMBO J. 2002 Oct 15;21(20):5516-26 PMID: 12374752
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2004-05-00
Pages
4229-40
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC400479
Subset
IM
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