Home LiteratureArticle Details
PMID: 12853611 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Transient recruitment of the hnRNP K protein to inducibly transcribed gene loci.

Nucleic acids research ·Vol. 31 ·No. 14 ·2003-07-15 ·Pages 3954-62

Ostrowski J, Kawata Y, Schullery DS, Denisenko ON, Bomsztyk K

Abstract

The heterogeneous nuclear ribonucleoprotein K protein is an RNA- and DNA-binding protein implicated in the regulation of multiple processes that comprise gene expression. We used chromatin immunoprecipitation (ChIP) assays to explore K protein interactions with serum-inducible, constitutively expressed and untranscribed gene loci in vivo. In the rat HTC-IR hepatoma cell line, serum treatment induced transient increases in the mRNA levels of two immediate-early genes, egr-1 and c-myc. ChIP analysis showed that the induction of egr-1 and c-myc genes was associated with a transient recruitment of K protein to multiple sites within each of these loci, including the promoter and transcribed regions. In contrast, recruitment of K protein to the constitutively transcribed beta-actin locus and to randomly chosen non-transcribed loci was far weaker. In rat mesangial cells, c-myc was constitutively expressed while egr-1 remained serum responsive. In these cells, ChIP analysis showed serum-induced recruitment to the inducible egr-1 but not to the c-myc locus. Pre-treatment with the transcription inhibitor actinomycin D blocked the inducible but not the constitutive binding of K protein to these loci. Taken together, the results of this study suggest that the transient recruitment of K protein to serum-responsive loci depends on the inducible transcription of these immediate-early genes.

MeSH Terms
Animals Culture Media, Serum-Free/pharmacology DNA/metabolism DNA-Binding Proteins/genetics Early Growth Response Protein 1 Gene Expression Heterogeneous-Nuclear Ribonucleoprotein K/metabolism Immediate-Early Proteins/genetics Precipitin Tests/methods Protein Binding Proto-Oncogene Proteins c-myc/genetics RNA, Messenger/genetics,metabolism Reverse Transcriptase Polymerase Chain Reaction Transcription Factors/genetics Transcription, Genetic/drug effects,genetics Tumor Cells, Cultured
Chemicals
Culture Media, Serum-Free DNA-Binding Proteins Early Growth Response Protein 1 Egr1 protein, rat Heterogeneous-Nuclear Ribonucleoprotein K Immediate-Early Proteins Proto-Oncogene Proteins c-myc RNA, Messenger Transcription Factors DNA
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Ostrowski Jerzy
Department of Medicine, University of Washington, Seattle, WA 98195, USA.
Kawata Yasunobu
Schullery Daniel S
Denisenko Oleg N
Bomsztyk Karol
References (48)
48 references, click to expand
  1. The hnRNP F protein: unique primary structure, nucleic acid-binding properties, and subcellular localization.
    Nucleic Acids Res. 1994 Mar 25;22(6):1059-67 PMID: 7512260
  2. Cloning and characterization of a single-stranded DNA binding protein that specifically recognizes deoxycytidine stretch.
    Nucleic Acids Res. 1994 Jan 11;22(1):53-8 PMID: 8127654
  3. Novel signaling pathway suggested by SH3 domain-mediated p95vav/heterogeneous ribonucleoprotein K interaction.
    J Biol Chem. 1994 Aug 12;269(32):20225-8 PMID: 8051112
  4. In vivo cross-linking and immunoprecipitation for studying dynamic Protein:DNA associations in a chromatin environment.
    Methods. 1999 Nov;19(3):425-33 PMID: 10579938
  5. Role of tyrosine phosphorylation in the regulation of the interaction of heterogenous nuclear ribonucleoprotein K protein with its protein and RNA partners.
    J Biol Chem. 2000 Feb 4;275(5):3619-28 PMID: 10652358
  6. Interaction of two multifunctional proteins. Heterogeneous nuclear ribonucleoprotein K and Y-box-binding protein.
    J Biol Chem. 2000 May 19;275(20):15498-503 PMID: 10809782
  7. ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation.
    Nat Cell Biol. 2001 Mar;3(3):325-30 PMID: 11231586
  8. Growth factors regulate heterogeneous nuclear ribonucleoprotein K expression and function.
    J Biol Chem. 2001 Mar 30;276(13):9699-704 PMID: 11121407
  9. Identification of new JNK substrate using ATP pocket mutant JNK and a corresponding ATP analogue.
    J Biol Chem. 2001 May 25;276(21):18090-5 PMID: 11259409
  10. Insulin alters heterogeneous nuclear ribonucleoprotein K protein binding to DNA and RNA.
    Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9044-9 PMID: 11470915
  11. Distinct RNP complexes of shuttling hnRNP proteins with pre-mRNA and mRNA: candidate intermediates in formation and export of mRNA.
    Mol Cell Biol. 2001 Nov;21(21):7307-19 PMID: 11585913
  12. Yeast hnRNP K-like genes are involved in regulation of the telomeric position effect and telomere length.
    Mol Cell Biol. 2002 Jan;22(1):286-97 PMID: 11739741
  13. Association of the vav proto-oncogene product with poly(rC)-specific RNA-binding proteins.
    Mol Cell Biol. 1995 Mar;15(3):1324-32 PMID: 7862126
  14. Cellular nucleic acid binding protein regulates the CT element of the human c-myc protooncogene.
    J Biol Chem. 1995 Apr 21;270(16):9494-9 PMID: 7721877
  15. Description of an IL-1-responsive kinase that phosphorylates the K protein. Enhancement of phosphorylation by selective DNA and RNA motifs.
    Biochemistry. 1995 Apr 25;34(16):5644-50 PMID: 7727425
  16. Signal transduction pathways leading to insulin-induced early gene induction.
    Biochemistry. 1995 Jun 27;34(25):7996-8004 PMID: 7540866
  17. The K protein domain that recruits the interleukin 1-responsive K protein kinase lies adjacent to a cluster of c-Src and Vav SH3-binding sites. Implications that K protein acts as a docking platform.
    J Biol Chem. 1995 Nov 10;270(45):26976-85 PMID: 7592945
  18. Heterogeneous nuclear ribonucleoprotein K is a transcription factor.
    Mol Cell Biol. 1996 May;16(5):2350-60 PMID: 8628302
  19. trans-Activation by the hnRNP K protein involves an increase in RNA synthesis from the reporter genes.
    J Biol Chem. 1996 Feb 16;271(7):3420-7 PMID: 8631943
  20. Activation of a nuclear DNA-binding protein recognized by a transcriptional element, bcn-1, from the laminin B2 chain gene promoter.
    J Biol Chem. 1996 Aug 2;271(31):18981-8 PMID: 8702563
  21. Zik1, a transcriptional repressor that interacts with the heterogeneous nuclear ribonucleoprotein particle K protein.
    J Biol Chem. 1996 Nov 1;271(44):27701-6 PMID: 8910362
  22. Diverse molecular interactions of the hnRNP K protein.
    FEBS Lett. 1997 Feb 17;403(2):113-5 PMID: 9042948
  23. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3' end.
    Cell. 1997 May 16;89(4):597-606 PMID: 9160751
  24. The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein.
    EMBO J. 1997 Jun 16;16(12):3587-98 PMID: 9218800
  25. The product of the murine homolog of the Drosophila extra sex combs gene displays transcriptional repressor activity.
    Mol Cell Biol. 1997 Aug;17(8):4707-17 PMID: 9234727
  26. STAR, a gene family involved in signal transduction and activation of RNA.
    Trends Genet. 1997 Dec;13(12):479-84 PMID: 9433137
  27. In situ cross-linking by cisplatin of nuclear matrix-bound transcription factors to nuclear DNA of human breast cancer cells.
    Cancer Res. 1998 Jul 15;58(14):3004-8 PMID: 9679963
  28. Differential effects of heterogeneous nuclear ribonucleoprotein K on Sp1- and Sp3-mediated transcriptional activation of a neuronal nicotinic acetylcholine receptor promoter.
    J Biol Chem. 1998 Jul 31;273(31):19877-83 PMID: 9677424
  29. Cytoplasmic regulatory functions of the KH-domain proteins hnRNPs K and E1/E2.
    Trends Biochem Sci. 1998 Nov;23(11):409-11 PMID: 9852755
  30. The transcriptional program in the response of human fibroblasts to serum.
    Science. 1999 Jan 1;283(5398):83-7 PMID: 9872747
  31. Spatial organization of four hnRNP proteins in relation to sites of transcription, to nuclear speckles, and to each other in interphase nuclei and nuclear matrices of HeLa cells.
    Exp Cell Res. 1999 Feb 1;246(2):461-70 PMID: 9925762
  32. Regulated interaction of protein kinase Cdelta with the heterogeneous nuclear ribonucleoprotein K protein.
    J Biol Chem. 1999 May 21;274(21):15101-9 PMID: 10329716
  33. The multifunctional herpes simplex virus IE63 protein interacts with heterogeneous ribonucleoprotein K and with casein kinase 2.
    J Biol Chem. 1999 Oct 8;274(41):28991-8 PMID: 10506147
  34. The levels of the bancal product, a Drosophila homologue of vertebrate hnRNP K protein, affect cell proliferation and apoptosis in imaginal disc cells.
    Mol Cell Biol. 1999 Nov;19(11):7846-56 PMID: 10523673
  35. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation.
    Genes Dev. 2000 May 15;14(10):1236-48 PMID: 10817758
  36. Heterogeneous nuclear ribonucleoprotein K protein associates with multiple mitochondrial transcripts within the organelle.
    J Biol Chem. 2002 Feb 22;277(8):6303-10 PMID: 11741984
  37. Heterogeneous nuclear ribonucleoprotein (hnRNP) K is a component of an intronic splicing enhancer complex that activates the splicing of the alternative exon 6A from chicken beta-tropomyosin pre-mRNA.
    J Biol Chem. 2002 May 10;277(19):16614-23 PMID: 11867641
  38. The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms.
    RNA. 2002 Mar;8(3):265-78 PMID: 12003487
  39. c-Src-mediated phosphorylation of hnRNP K drives translational activation of specifically silenced mRNAs.
    Mol Cell Biol. 2002 Jul;22(13):4535-43 PMID: 12052863
  40. Signal-dependent regulation of splicing via phosphorylation of Sam68.
    Nature. 2002 Dec 12;420(6916):691-5 PMID: 12478298
  41. Protein synthesis and the temporal control of genetic transcription during slime mold development.
    Proc Natl Acad Sci U S A. 1966 Apr;55(4):813-8 PMID: 5219688
  42. 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
  43. Chromatin architecture and nuclear RNA.
    Proc Natl Acad Sci U S A. 1989 Jan;86(1):177-81 PMID: 2911567
  44. Transcription elongation and eukaryotic gene regulation.
    Oncogene. 1990 Jun;5(6):777-85 PMID: 2193290
  45. A serine/threonine kinase activity is closely associated with a 65-kDa phosphoprotein specifically recognized by the kappa B enhancer element.
    J Biol Chem. 1991 Jul 5;266(19):12722-33 PMID: 1829460
  46. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm.
    Nature. 1992 Feb 20;355(6362):730-2 PMID: 1371331
  47. Specific binding of heterogeneous ribonucleoprotein particle protein K to the human c-myc promoter, in vitro.
    J Biol Chem. 1993 Aug 25;268(24):18249-58 PMID: 8349701
  48. Purification, cloning, and expression of a murine phosphoprotein that binds the kappa B motif in vitro identifies it as the homolog of the human heterogeneous nuclear ribonucleoprotein K protein. Description of a novel DNA-dependent phosphorylation process.
    J Biol Chem. 1994 Jul 1;269(26):17626-34 PMID: 8021272
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2003-07-15
Pages
3954-62
Language
English
Region
England
NLM ID
0411011
PMCID
PMC165967
Subset
IM
Grants
NIDDK NIH HHS · R01 DK045978 · United States
NIDDK NIH HHS · DK45978 · United States
FIC NIH HHS · TW05685 · United States
NIGMS NIH HHS · GM45134 · United States
NIDDK NIH HHS · R37 DK045978 · United States
NIGMS NIH HHS · R01 GM045134 · United States
FIC NIH HHS · R03 TW005685 · United States
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: product@genelibs.com