Home LiteratureArticle Details
PMID: 1628625 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box.

The EMBO journal ·Vol. 11 ·No. 7 ·1992-07-00 ·Pages 2655-64

Kiledjian M, Dreyfuss G

Abstract

Heterogeneous nuclear ribonucleoproteins (hnRNPs) are thought to influence the structure of hnRNA and participate in the processing of hnRNA to mRNA. The hnRNP U protein is an abundant nucleoplasmic phosphoprotein that is the largest of the major hnRNP proteins (120 kDa by SDS-PAGE). HnRNP U binds pre-mRNA in vivo and binds both RNA and ssDNA in vitro. Here we describe the cloning and sequencing of a cDNA encoding the hnRNP U protein, the determination of its amino acid sequence and the delineation of a region in this protein that confers RNA binding. The predicted amino acid sequence of hnRNP U contains 806 amino acids (88,939 Daltons), and shows no extensive homology to any known proteins. The N-terminus is rich in acidic residues and the C-terminus is glycine-rich. In addition, a glutamine-rich stretch, a putative NTP binding site and a putative nuclear localization signal are present. It could not be defined from the sequence what segment of the protein confers its RNA binding activity. We identified an RNA binding activity within the C-terminal glycine-rich 112 amino acids. This region, designated U protein glycine-rich RNA binding region (U-gly), can by itself bind RNA. Furthermore, fusion of U-gly to a heterologous bacterial protein (maltose binding protein) converts this fusion protein into an RNA binding protein. A 26 amino acid peptide within U-gly is necessary for the RNA binding activity of the U protein. Interestingly, this peptide contains a cluster of RGG repeats with characteristic spacing and this motif is found also in several other RNA binding proteins. We have termed this region the RGG box and propose that it is an RNA binding motif and a predictor of RNA binding activity.

MeSH Terms
Amino Acid Sequence Base Sequence Blotting, Western DNA Electrophoresis, Polyacrylamide Gel HeLa Cells Heterogeneous-Nuclear Ribonucleoprotein U Heterogeneous-Nuclear Ribonucleoproteins Humans Molecular Sequence Data Peptide Mapping Plasmids Precipitin Tests Protein Binding Protein Biosynthesis RNA, Heterogeneous Nuclear/metabolism RNA-Binding Proteins/genetics,metabolism Ribonucleoproteins/genetics,metabolism Transcription, Genetic
Chemicals
Heterogeneous-Nuclear Ribonucleoprotein U Heterogeneous-Nuclear Ribonucleoproteins RNA, Heterogeneous Nuclear RNA-Binding Proteins Ribonucleoproteins DNA
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Kiledjian M
Howard Hughes Medical Institute, Philadelphia, PA.
Dreyfuss G
References (59)
59 references, click to expand
  1. Chemical and biological evolution of nucleotide-binding protein.
    Nature. 1974 Jul 19;250(463):194-9 PMID: 4368490
  2. Characterization of the major hnRNP proteins from Drosophila melanogaster.
    J Cell Biol. 1992 Jan;116(2):257-69 PMID: 1730754
  3. Prediction of the secondary structure of proteins from their amino acid sequence.
    Adv Enzymol Relat Areas Mol Biol. 1978;47:45-148 PMID: 364941
  4. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles.
    Microbiol Rev. 1983 Mar;47(1):1-45 PMID: 6343825
  5. Physical change in cytoplasmic messenger ribonucleoproteins in cells treated with inhibitors of mRNA transcription.
    Mol Cell Biol. 1984 Mar;4(3):415-23 PMID: 6717428
  6. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold.
    EMBO J. 1982;1(8):945-51 PMID: 6329717
  7. Characterization of heterogeneous nuclear RNA-protein complexes in vivo with monoclonal antibodies.
    Mol Cell Biol. 1984 Jun;4(6):1104-14 PMID: 6204191
  8. Monoclonal antibody characterization of the C proteins of heterogeneous nuclear ribonucleoprotein complexes in vertebrate cells.
    J Cell Biol. 1984 Dec;99(6):1997-204 PMID: 6209285
  9. Isolation of the heterogeneous nuclear RNA-ribonucleoprotein complex (hnRNP): a unique supramolecular assembly.
    Proc Natl Acad Sci U S A. 1984 Dec;81(23):7471-5 PMID: 6594697
  10. Rapid and sensitive protein similarity searches.
    Science. 1985 Mar 22;227(4693):1435-41 PMID: 2983426
  11. Structure of rodent helix-destabilizing protein revealed by cDNA cloning.
    J Biol Chem. 1986 Mar 15;261(8):3536-43 PMID: 3005291
  12. Molecular cloning of cDNA for the nuclear ribonucleoprotein particle C proteins: a conserved gene family.
    Proc Natl Acad Sci U S A. 1986 Apr;83(7):2007-11 PMID: 3457372
  13. Functional dissection of a eukaryotic transcriptional activator protein, GCN4 of yeast.
    Cell. 1986 Sep 12;46(6):885-94 PMID: 3530496
  14. mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence.
    Mol Cell Biol. 1986 Aug;6(8):2932-43 PMID: 3537727
  15. Structure and function of nuclear and cytoplasmic ribonucleoprotein particles.
    Annu Rev Cell Biol. 1986;2:459-98 PMID: 3548774
  16. Nucleolin, the major nucleolar protein of growing eukaryotic cells: an unusual protein structure revealed by the nucleotide sequence.
    Proc Natl Acad Sci U S A. 1987 Mar;84(6):1472-6 PMID: 3470736
  17. Primary structure of human nuclear ribonucleoprotein particle C proteins: conservation of sequence and domain structures in heterogeneous nuclear RNA, mRNA, and pre-rRNA-binding proteins.
    Mol Cell Biol. 1987 May;7(5):1731-9 PMID: 3110598
  18. Saccharomyces cerevisiae SSB1 protein and its relationship to nucleolar RNA-binding proteins.
    Mol Cell Biol. 1987 Aug;7(8):2947-55 PMID: 2823109
  19. Mammalian heterogeneous nuclear ribonucleoprotein complex protein A1. Large-scale overproduction in Escherichia coli and cooperative binding to single-stranded nucleic acids.
    J Biol Chem. 1988 Jan 15;263(2):1063-71 PMID: 2447078
  20. Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins.
    Genes Dev. 1988 Feb;2(2):215-27 PMID: 3129338
  21. Preparative elution of proteins blotted to Immobilon membranes.
    Anal Biochem. 1988 Jan;168(1):48-53 PMID: 3364716
  22. cDNA cloning of human hnRNP protein A1 reveals the existence of multiple mRNA isoforms.
    Nucleic Acids Res. 1988 May 11;16(9):3751-70 PMID: 2836799
  23. Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities.
    Mol Cell Biol. 1988 May;8(5):2237-41 PMID: 3386636
  24. Structure of the mouse nucleolin gene. The complete sequence reveals that each RNA binding domain is encoded by two independent exons.
    J Mol Biol. 1988 Apr 20;200(4):627-38 PMID: 3137346
  25. The nucleolar protein, B-36, contains a glycine and dimethylarginine-rich sequence conserved in several other nuclear RNA-binding proteins.
    Biochem Biophys Res Commun. 1988 Sep 30;155(3):1278-83 PMID: 3140806
  26. Sequence of the latency-related gene of herpes simplex virus type 1.
    Virology. 1989 Jan;168(1):168-72 PMID: 2535901
  27. Heterogeneous nuclear ribonucleoprotein particles and the pathway of mRNA formation.
    Trends Biochem Sci. 1988 Mar;13(3):86-91 PMID: 3072706
  28. Nucleolin from Xenopus laevis: cDNA cloning and expression during development.
    Genes Dev. 1989 Mar;3(3):324-33 PMID: 2656405
  29. RNA-binding proteins as developmental regulators.
    Genes Dev. 1989 Apr;3(4):431-7 PMID: 2470643
  30. Cloning and sequencing of the human nucleolin cDNA.
    FEBS Lett. 1989 Jun 19;250(1):99-105 PMID: 2737305
  31. Sequence-specific recognition of RNA hairpins by bacteriophage antiterminators requires a conserved arginine-rich motif.
    Cell. 1989 Oct 6;59(1):207-18 PMID: 2477156
  32. Scissors-grip model for DNA recognition by a family of leucine zipper proteins.
    Science. 1989 Nov 17;246(4932):911-6 PMID: 2683088
  33. Identification of the RNA binding segment of human U1 A protein and definition of its binding site on U1 snRNA.
    EMBO J. 1989 Dec 20;8(13):4163-70 PMID: 2531658
  34. Primary structures of the heterogeneous nuclear ribonucleoprotein A2, B1, and C2 proteins: a diversity of RNA binding proteins is generated by small peptide inserts.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):9788-92 PMID: 2557628
  35. Isolation and sequencing of NOP1. A yeast gene encoding a nucleolar protein homologous to a human autoimmune antigen.
    J Biol Chem. 1990 Feb 5;265(4):2209-15 PMID: 2298745
  36. Potential for two isoforms of the A1 ribonucleoprotein in Xenopus laevis.
    Proc Natl Acad Sci U S A. 1990 Feb;87(4):1367-71 PMID: 2137612
  37. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation.
    Cell. 1990 Mar 9;60(5):733-46 PMID: 2155707
  38. Structure and developmental expression of chicken nucleolin and NO38: coordinate expression of two abundant non-ribosomal nucleolar proteins.
    Biochim Biophys Acta. 1990 Jun 21;1049(2):126-33 PMID: 2114180
  39. Quantitative determination that one of two potential RNA-binding domains of the A protein component of the U1 small nuclear ribonucleoprotein complex binds with high affinity to stem-loop II of U1 RNA.
    Proc Natl Acad Sci U S A. 1990 Aug;87(16):6393-7 PMID: 1696729
  40. Structural studies of protein-nucleic acid interaction: the sources of sequence-specific binding.
    Q Rev Biophys. 1990 Aug;23(3):205-80 PMID: 2204954
  41. A novel RNA helicase gene tightly linked to the Triplo-lethal locus of Drosophila.
    Nucleic Acids Res. 1990 Sep 25;18(18):5489-94 PMID: 2170937
  42. Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A.
    Nature. 1990 Dec 6;348(6301):515-20 PMID: 2147232
  43. cDNA cloning and sequencing of human fibrillarin, a conserved nucleolar protein recognized by autoimmune antisera.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):931-5 PMID: 1846968
  44. Analysis of arginine-rich peptides from the HIV Tat protein reveals unusual features of RNA-protein recognition.
    Genes Dev. 1991 Feb;5(2):201-10 PMID: 1899841
  45. p68 RNA helicase: identification of a nucleolar form and cloning of related genes containing a conserved intron in yeasts.
    Mol Cell Biol. 1991 Mar;11(3):1326-33 PMID: 1996094
  46. Nuclear protein localization.
    Biochim Biophys Acta. 1991 Mar 7;1071(1):83-101 PMID: 2004116
  47. RNA-binding domain of the A protein component of the U1 small nuclear ribonucleoprotein analyzed by NMR spectroscopy is structurally similar to ribosomal proteins.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2495-9 PMID: 1826055
  48. Interactions of the A1 heterogeneous nuclear ribonucleoprotein and its proteolytic derivative, UP1, with RNA and DNA: evidence for multiple RNA binding domains and salt-dependent binding mode transitions.
    Biochemistry. 1991 Mar 19;30(11):2968-76 PMID: 1848781
  49. The NSR1 gene encodes a protein that specifically binds nuclear localization sequences and has two RNA recognition motifs.
    J Cell Biol. 1991 Apr;113(1):1-12 PMID: 1706724
  50. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A.
    Science. 1991 May 10;252(5007):809-17 PMID: 2028256
  51. The multiple RNA-binding domains of the mRNA poly(A)-binding protein have different RNA-binding activities.
    Mol Cell Biol. 1991 Jul;11(7):3419-24 PMID: 1675426
  52. RNA recognition: towards identifying determinants of specificity.
    Trends Biochem Sci. 1991 Jun;16(6):214-20 PMID: 1716386
  53. Mutations in an RNP1 consensus sequence of Rho protein reduce RNA binding affinity but facilitate helicase turnover.
    J Biol Chem. 1991 Sep 15;266(26):17296-305 PMID: 1716628
  54. Identification of molecular contacts between the U1 A small nuclear ribonucleoprotein and U1 RNA.
    EMBO J. 1991 Nov;10(11):3447-56 PMID: 1833186
  55. Crystal structure of a MAT alpha 2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions.
    Cell. 1991 Nov 1;67(3):517-28 PMID: 1682054
  56. Primary structure of rat ribosomal protein S2. A ribosomal protein with arginine-glycine tandem repeats and RGGF motifs that are associated with nucleolar localization and binding to ribonucleic acids.
    J Biol Chem. 1991 Oct 25;266(30):20007-10 PMID: 1939063
  57. Characterization and primary structure of the poly(C)-binding heterogeneous nuclear ribonucleoprotein complex K protein.
    Mol Cell Biol. 1992 Jan;12(1):164-71 PMID: 1729596
  58. Modification of the single tryptophan residue of staphylococcal nuclease by a new mild oxidizing agent.
    J Biol Chem. 1970 Apr 25;245(8):1895-902 PMID: 4985905
  59. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1992-07-00
Pages
2655-64
Language
English
Region
England
NLM ID
8208664
PMCID
PMC556741
Subset
IM
Databases
GENBANK
X65488, X66291, X66292, X66293, X66294, X67725, X67726, X68880, X68881, X68882
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]