Heterogeneous nuclear ribonucleoproteins (hnRNPs) in cellular processes: Focus on hnRNP E1's multifunctional regulatory roles.

Heterogeneous nuclear ribonucleoproteins (hnRNPs) comprise a family of RNA-binding proteins. The complexity and diversity associated with the hnRNPs render them multifunctional, involved not only in processing heterogeneous nuclear RNAs (hnRNAs) into mature mRNAs, but also acting as trans-factors in regulating gene expression. Heterogeneous nuclear ribonucleoprotein E1 (hnRNP E1), a subgroup of hnRNPs, is a KH-triple repeat containing RNA-binding protein. It is encoded by an intronless gene arising from hnRNP E2 through a retrotransposition event. hnRNP E1 is ubiquitously expressed and functions in regulating major steps of gene expression, including pre-mRNA processing, mRNA stability, and translation. Given its wide-ranging functions in the nucleus and cytoplasm and interaction with multiple proteins, we propose a post-transcriptional regulon model that explains hnRNP E1's widespread functional diversity.

[1]  G. Meister,et al.  MicroRNAs: From Decay to Decoy , 2010, Cell.

[2]  M. Caligiuri,et al.  miR-328 Functions as an RNA Decoy to Modulate hnRNP E2 Regulation of mRNA Translation in Leukemic Blasts , 2010, Cell.

[3]  G. Hussey,et al.  Transforming Growth Factor-β (TGFβ)-mediated Phosphorylation of hnRNP E1 Induces EMT via Transcript Selective Translational Induction of Dab2 and ILEI , 2010, Nature cell biology.

[4]  P. Anderson Post-transcriptional regulons coordinate the initiation and resolution of inflammation , 2010, Nature Reviews Immunology.

[5]  Feimeng Zheng,et al.  Pluripotency-associated genes in human nasopharyngeal carcinoma CNE-2 cells are reactivated by a unique epigenetic sub-microenvironment , 2010, BMC Cancer.

[6]  R. Mukhopadhyay,et al.  The GAIT system: a gatekeeper of inflammatory gene expression. , 2009, Trends in biochemical sciences.

[7]  A. Hartmann,et al.  Heterogeneous Nuclear Ribonucleoprotein G Regulates Splice Site Selection by Binding to CC(A/C)-rich Regions in Pre-mRNA* , 2009, Journal of Biological Chemistry.

[8]  M. Hatzoglou,et al.  A stress-responsive RNA switch regulates VEGF expression , 2008, Nature.

[9]  Wei Mo,et al.  Arginine methylation of hnRNP K enhances p53 transcriptional activity , 2008, FEBS letters.

[10]  B. Szaro,et al.  Dynamic endogenous association of neurofilament mRNAs with K-homology domain ribonucleoproteins in developing cerebral cortex , 2008, Brain Research.

[11]  H. Baharvand,et al.  Identification of mouse embryonic stem cell-associated proteins. , 2008, Journal of proteome research.

[12]  R. Carstens,et al.  Heterogeneous Ribonucleoprotein M Is a Splicing Regulatory Protein That Can Enhance or Silence Splicing of Alternatively Spliced Exons* , 2007, Journal of Biological Chemistry.

[13]  S. Chew,et al.  Pre-spliceosomal binding of U1 small nuclear ribonucleoprotein (RNP) and heterogenous nuclear RNP E1 is associated with suppression of a growth hormone receptor pseudoexon. , 2007, Molecular endocrinology.

[14]  Anupama E. Gururaj,et al.  Signaling-dependent and coordinated regulation of transcription, splicing, and translation resides in a single coregulator, PCBP1 , 2007, Proceedings of the National Academy of Sciences.

[15]  H. Beug,et al.  ILEI: a cytokine essential for EMT, tumor formation, and late events in metastasis in epithelial cells. , 2006, Cancer cell.

[16]  Jian Kong,et al.  Shared Stabilization Functions of Pyrimidine-Rich Determinants in the Erythroid 15-lipoxygenase and α-globin mRNAs , 2006, Molecular and Cellular Biology.

[17]  G. Korza,et al.  Heterogeneous nuclear ribonucleoprotein (hnRNP) E1 binds to hnRNP A2 and inhibits translation of A2 response element mRNAs. , 2006, Molecular biology of the cell.

[18]  H. Loh,et al.  Poly(C) Binding Protein Family Is a Transcription Factor in μ-Opioid Receptor Gene Expression , 2005, Molecular Pharmacology.

[19]  Juan Valcárcel,et al.  Building specificity with nonspecific RNA-binding proteins , 2005, Nature Structural &Molecular Biology.

[20]  E. Schmidt,et al.  hnRNP K Binds a Core Polypyrimidine Element in the Eukaryotic Translation Initiation Factor 4E (eIF4E) Promoter, and Its Regulation of eIF4E Contributes to Neoplastic Transformation , 2005, Molecular and Cellular Biology.

[21]  J. Helmann,et al.  Genetic and physiological responses of Bacillus subtilis to metal ion stress , 2005, Molecular microbiology.

[22]  P. Howe,et al.  Disabled-2 (Dab2) Is Required for Transforming Growth Factor β-induced Epithelial to Mesenchymal Transition (EMT)* , 2005, Journal of Biological Chemistry.

[23]  J. Wilce,et al.  Structure and RNA binding of the third KH domain of poly(C)-binding protein 1 , 2005, Nucleic acids research.

[24]  Doree Sitkoff,et al.  models homology modeling : From sequence alignments to structural A comparative study of available software for high-accuracy , 2005 .

[25]  B. Szaro,et al.  Phylogenetically Conserved Binding of Specific K Homology Domain Proteins to the 3′-Untranslated Region of the Vertebrate Middle Neurofilament mRNA* , 2004, Journal of Biological Chemistry.

[26]  Roland Hetzer,et al.  RNA-Binding Proteins Heterogeneous Nuclear Ribonucleoprotein A1, E1, and K Are Involved in Post-Transcriptional Control of Collagen I and III Synthesis , 2004, Circulation research.

[27]  A. Ostareck-Lederer,et al.  Control of mRNA translation and stability in haematopoietic cells: The function of hnRNPs K and E1/E2 , 2004, Biology of the cell.

[28]  Tao Wang,et al.  Sumoylation of heterogeneous nuclear ribonucleoproteins, zinc finger proteins, and nuclear pore complex proteins: a proteomic analysis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Jerzy Ostrowski,et al.  hnRNP K: One protein multiple processes , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[30]  M. Mann,et al.  RNA and RNA Binding Proteins Participate in Early Stages of Cell Spreading through Spreading Initiation Centers , 2004, Cell.

[31]  U. Scheer,et al.  Structural organization of nascent transcripts and hnRNA molecules in amphibian oocytes , 1981, Molecular Biology Reports.

[32]  A. Chkheidze,et al.  A Novel Set of Nuclear Localization Signals Determine Distributions of the αCP RNA-Binding Proteins , 2003, Molecular and Cellular Biology.

[33]  A. Antony,et al.  Expression of folate receptors and heterogeneous nuclear ribonucleoprotein E1 in women with human papillomavirus mediated transformation of cervical tissue to cancer , 2003, Journal of clinical pathology.

[34]  S. Guil,et al.  Roles of hnRNP A1, SR Proteins, and p68 Helicase in c-H-ras Alternative Splicing Regulation , 2003, Molecular and Cellular Biology.

[35]  S. Liebhaber,et al.  Regulation of α-Globin mRNA Stability , 2003 .

[36]  P. Persson,et al.  Posttranscriptional Control of Renin Synthesis: Identification of Proteins Interacting With Renin mRNA 3′-Untranslated Region , 2003, Circulation research.

[37]  A. Willis,et al.  Polypyrimidine tract binding protein and poly r(C) binding protein 1 interact with the BAG-1 IRES and stimulate its activity in vitro and in vivo. , 2003, Nucleic acids research.

[38]  A. Thomson,et al.  Novel Binding of HuR and Poly(C)-binding Protein to a Conserved UC-rich Motif within the 3′-Untranslated Region of the Androgen Receptor Messenger RNA* , 2002, The Journal of Biological Chemistry.

[39]  M. Hentze,et al.  c-Src-Mediated Phosphorylation of hnRNP K Drives Translational Activation of Specifically Silenced mRNAs , 2002, Molecular and Cellular Biology.

[40]  S. Tenenbaum,et al.  Eukaryotic mRNPs may represent posttranscriptional operons. , 2002, Molecular cell.

[41]  A. Bergamaschi,et al.  hnRNP A1 Nucleocytoplasmic Shuttling Activity Is Required for Normal Myelopoiesis and BCR/ABL Leukemogenesis , 2002, Molecular and Cellular Biology.

[42]  G. Dreyfuss,et al.  Messenger-RNA-binding proteins and the messages they carry , 2002, Nature Reviews Molecular Cell Biology.

[43]  S. Liebhaber,et al.  The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms. , 2002, RNA.

[44]  J. Steitz,et al.  Delineation of mRNA Export Pathways by the Use of Cell-Permeable Peptides , 2001, Science.

[45]  J. Yong,et al.  SMN interacts with a novel family of hnRNP and spliceosomal proteins , 2001, The EMBO journal.

[46]  Jia Yu,et al.  Structural and Functional Analysis of an mRNP Complex That Mediates the High Stability of Human β-Globin mRNA , 2001, Molecular and Cellular Biology.

[47]  C. Geczy,et al.  IL-10 Up-Regulates Macrophage Expression of the S100 Protein S100A81 , 2001, The Journal of Immunology.

[48]  M. Mandal,et al.  Growth Factors Regulate Heterogeneous Nuclear Ribonucleoprotein K Expression and Function* , 2001, The Journal of Biological Chemistry.

[49]  Kavita Shah,et al.  ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation , 2001, Nature Cell Biology.

[50]  N. Grishin,et al.  KH domain: one motif, two folds. , 2001, Nucleic acids research.

[51]  M. Hentze,et al.  Lipoxygenase mRNA Silencing in Erythroid Differentiation The 3′UTR Regulatory Complex Controls 60S Ribosomal Subunit Joining , 2001, Cell.

[52]  J. E. Russell,et al.  Structural and Functional Analysis of an mRNP Complex That Mediates the High Stability of Human b -Globin mRNA , 2001 .

[53]  J H Carson,et al.  RNA trafficking in oligodendrocytes. , 2001, Results and problems in cell differentiation.

[54]  T. Henics Differentiation-dependent cytoplasmic distribution and in vivo RNA association of proteins recognized by the 3'-UTR stability element of alpha-globin mRNA in erythroleukemic cells. , 2000, Biochemical and biophysical research communications.

[55]  M. Kiledjian,et al.  The Poly(A)-Binding Protein and an mRNA Stability Protein Jointly Regulate an Endoribonuclease Activity , 2000, Molecular and Cellular Biology.

[56]  B. Calabretta,et al.  BCR-ABL Prevents c-Jun-Mediated and Proteasome-Dependent FUS (TLS) Proteolysis through a Protein Kinase CβII-Dependent Pathway , 2000, Molecular and Cellular Biology.

[57]  S K Burley,et al.  The tetranucleotide UCAY directs the specific recognition of RNA by the Nova K-homology 3 domain. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[58]  R. Darnell,et al.  Sequence-Specific RNA Binding by a Nova KH Domain Implications for Paraneoplastic Disease and the Fragile X Syndrome , 2000, Cell.

[59]  M. Kiledjian,et al.  Identification of an erythroid‐enriched endoribonuclease activity involved in specific mRNA cleavage , 2000, The EMBO journal.

[60]  A. Chkheidze,et al.  A Set of Highly Conserved RNA-binding Proteins, αCP-1 and αCP-2, Implicated in mRNA Stabilization, Are Coexpressed from an Intronless Gene and Its Intron-containing Paralog* , 1999, The Journal of Biological Chemistry.

[61]  A. F. Neuwald,et al.  Purification and biochemical characterization of interchromatin granule clusters , 1999, The EMBO journal.

[62]  J. Morales,et al.  Assembly of the α-Globin mRNA Stability Complex Reflects Binary Interaction between the Pyrimidine-Rich 3′ Untranslated Region Determinant and Poly(C) Binding Protein αCP , 1999, Molecular and Cellular Biology.

[63]  M. Kiledjian,et al.  An mRNA Stability Complex Functions with Poly(A)-Binding Protein To Stabilize mRNA In Vitro , 1999, Molecular and Cellular Biology.

[64]  M. Swanson,et al.  hnRNP complexes: composition, structure, and function. , 1999, Current opinion in cell biology.

[65]  R. Kelley,et al.  Specific isoforms of squid, a Drosophila hnRNP, perform distinct roles in Gurken localization during oogenesis. , 1999, Genes & development.

[66]  M. Czyzyk-Krzeska,et al.  Identification of the poly(C) binding protein in the complex associated with the 3' untranslated region of erythropoietin messenger RNA. , 1999, Blood.

[67]  S K Burley,et al.  Crystal structures of Nova-1 and Nova-2 K-homology RNA-binding domains. , 1999, Structure.

[68]  N. Maizels,et al.  G4 DNA Binding by LR1 and Its Subunits, Nucleolin and hnRNP D, A Role for G-G pairing in Immunoglobulin Switch Recombination* , 1999, The Journal of Biological Chemistry.

[69]  Douglas L. Black,et al.  hnRNP H Is a Component of a Splicing Enhancer Complex That Activates a c-src Alternative Exon in Neuronal Cells , 1999, Molecular and Cellular Biology.

[70]  M. Hentze,et al.  Cytoplasmic regulatory functions of the KH-domain proteins hnRNPs K and E1/E2. , 1998, Trends in biochemical sciences.

[71]  S. Schwartz,et al.  Translational Inhibition in Vitro of Human Papillomavirus Type 16 L2 mRNA Mediated through Interaction with Heterogenous Ribonucleoprotein K and Poly(rC)-binding Proteins 1 and 2* , 1998, The Journal of Biological Chemistry.

[72]  S. Dupuis,et al.  Telomere elongation by hnRNP A1 and a derivative that interacts with telomeric repeats and telomerase , 1998, Nature Genetics.

[73]  K. Hoek,et al.  hnRNP A2 selectively binds the cytoplasmic transport sequence of myelin basic protein mRNA. , 1998, Biochemistry.

[74]  Sheng‐Chung Lee,et al.  Identification of Heterogeneous Nuclear Ribonucleoprotein K (hnRNP K) as a Repressor of C/EBPβ-mediated Gene Activation* , 1998, The Journal of Biological Chemistry.

[75]  G. Dreyfuss,et al.  Molecular definition of heterogeneous nuclear ribonucleoprotein R (hnRNP R) using autoimmune antibody: immunological relationship with hnRNP P. , 1998, Nucleic acids research.

[76]  K. Artzt,et al.  STAR, a gene family involved in signal transduction and activation of RNA. , 1997, Trends in genetics : TIG.

[77]  Marco M. Kessler,et al.  Hrp1, a sequence-specific RNA-binding protein that shuttles between the nucleus and the cytoplasm, is required for mRNA 3'-end formation in yeast. , 1997, Genes & development.

[78]  T. Gibson,et al.  The solution structure of the first KH domain of FMR1, the protein responsible for the fragile X syndrome , 1997, Nature Structural Biology.

[79]  R. Andino,et al.  Two functional complexes formed by KH domain containing proteins with the 5' noncoding region of poliovirus RNA. , 1997, RNA.

[80]  C. Demaria,et al.  Identification of AUF1 (heterogeneous nuclear ribonucleoprotein D) as a component of the alpha-globin mRNA stability complex , 1997, Molecular and cellular biology.

[81]  G. Dreyfuss,et al.  The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein , 1997, The EMBO journal.

[82]  R. Darnell,et al.  The neuronal RNA binding protein Nova-1 recognizes specific RNA targets in vitro and in vivo , 1997, Molecular and cellular biology.

[83]  M. Hentze,et al.  mRNA Silencing in Erythroid Differentiation: hnRNP K and hnRNP E1 Regulate 15-Lipoxygenase Translation from the 3′ End , 1997, Cell.

[84]  K. Williams,et al.  Identification of N(G)-methylarginine residues in human heterogeneous RNP protein A1: Phe/Gly-Gly-Gly-Arg-Gly-Gly-Gly/Phe is a preferred recognition motif. , 1997, Biochemistry.

[85]  S. Liebhaber,et al.  Four highly stable eukaryotic mRNAs assemble 3' untranslated region RNA-protein complexes sharing cis and trans components. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[86]  T. Steitz,et al.  Crystal structure of the two RNA binding domains of human hnRNP A1 at 1.75 Å resolution , 1997, Nature Structural Biology.

[87]  J. Ostrowski,et al.  Diverse molecular interactions of the hnRNP K protein , 1997, FEBS letters.

[88]  H. Leffers,et al.  Characterisation of the nucleic-acid-binding activity of KH domains. Different properties of different domains. , 1996, European journal of biochemistry.

[89]  S. Riva,et al.  The roles of heterogeneous nuclear ribonucleoproteins (hnRNP) in RNA metabolism , 1996, BioEssays : news and reviews in molecular, cellular and developmental biology.

[90]  T. Gibson,et al.  Three-Dimensional Structure and Stability of the KH Domain: Molecular Insights into the Fragile X Syndrome , 1996, Cell.

[91]  H. Leffers,et al.  Assignment of human KH-box-containing genes by in situ hybridization: HNRNPK maps to 9q21.32-q21.33, PCBP1 to 2p12-p13, and PCBP2 to 12q13.12-q13.13, distal to FRA12A. , 1996, Genomics.

[92]  M. Czyzyk-Krzeska,et al.  Characterization of the Hypoxia-inducible Protein Binding Site within the Pyrimidine-rich Tract in the 3′-Untranslated Region of the Tyrosine Hydroxylase mRNA (*) , 1996, The Journal of Biological Chemistry.

[93]  G. Dreyfuss,et al.  A nuclear export signal in hnRNP A1: A signal-mediated, temperature-dependent nuclear protein export pathway , 1995, Cell.

[94]  Douglas S. Portman,et al.  Cell type-specific expression of hnRNP proteins. , 1995, Experimental cell research.

[95]  H. Urlaub,et al.  Protein‐rRNA binding features and their structural and functional implications in ribosomes as determined by cross‐linking studies. , 1995, The EMBO journal.

[96]  S. Liebhaber,et al.  Identification of two KH domain proteins in the alpha‐globin mRNP stability complex. , 1995, The EMBO journal.

[97]  H. Leffers,et al.  Characterisation of two major cellular poly(rC)-binding human proteins, each containing three K-homologous (KH) domains. , 1995, European journal of biochemistry.

[98]  K. Liu,et al.  NusA interferes with interactions between the nascent RNA and the C-terminal domain of the alpha subunit of RNA polymerase in Escherichia coli transcription complexes. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[99]  G. Dreyfuss,et al.  A nuclear localization domain in the hnRNP A1 protein , 1995, The Journal of cell biology.

[100]  D. Rio,et al.  Soma-specific expression and cloning of PSI, a negative regulator of P element pre-mRNA splicing. , 1995, Genes & development.

[101]  S. Liebhaber,et al.  Erythroid cell-specific determinants of alpha-globin mRNA stability , 1994, Molecular and cellular biology.

[102]  S. Fumagalli,et al.  A mitotic function for Src? , 1994, Trends in cell biology.

[103]  A. Krainer,et al.  Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. , 1994, Science.

[104]  C. Burd,et al.  Conserved structures and diversity of functions of RNA-binding proteins. , 1994, Science.

[105]  E. Smeland,et al.  Tissue specific expression and cDNA structure of a human transcript encoding a nucleic acid binding [oligo(dC)] protein related to the pre-mRNA binding protein K. , 1994, Nucleic Acids Research.

[106]  N. Standart,et al.  Translation of 15‐lipoxygenase mRNA is inhibited by a protein that binds to a repeated sequence in the 3′ untranslated region. , 1994, The EMBO journal.

[107]  R. Darnell,et al.  Nova, the paraneoplastic Ri antigen, is homologous to an RNA-binding protein and is specifically expressed in the developing motor system , 1993, Neuron.

[108]  R. Nussbaum,et al.  The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein , 1993, Cell.

[109]  G. Dreyfuss,et al.  Nuclear proteins that bind the pre-mRNA 3' splice site sequence r(UUAG/G) and the human telomeric DNA sequence d(TTAGGG)n , 1993, Molecular and cellular biology.

[110]  T. Gibson,et al.  The KH domain occurs in a diverse set of RNA‐binding proteins that include the antiterminator NusA and is probably involved in binding to nucleic acid , 1993, FEBS letters.

[111]  K. Nandabalan,et al.  Mutations in U1 snRNA bypass the requirement for a cell type-specific RNA splicing factor , 1993, Cell.

[112]  G. Dreyfuss,et al.  Association of individual hnRNP proteins and snRNPs with nascent transcripts , 1993, The Journal of cell biology.

[113]  G. Dreyfuss,et al.  The pre-mRNA binding K protein contains a novel evolutionarily conserved motif. , 1993, Nucleic acids research.

[114]  C. Burd,et al.  hnRNP proteins and the biogenesis of mRNA. , 1993, Annual review of biochemistry.

[115]  A. L. Beyer,et al.  Independent deposition of heterogeneous nuclear ribonucleoproteins and small nuclear ribonucleoprotein particles at sites of transcription. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[116]  M. Wittekind,et al.  Interaction of the RNA‐binding domain of the hnRNP C proteins with RNA. , 1992, The EMBO journal.

[117]  G. Dreyfuss,et al.  Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. , 1992, The EMBO journal.

[118]  W. Purschke,et al.  Complete cDNA sequence of chicken vigilin, a novel protein with amplified and evolutionary conserved domains. , 1992, European journal of biochemistry.

[119]  Adrian R. Krainer,et al.  Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2 , 1992, Cell.

[120]  G. Dreyfuss,et al.  Characterization and primary structure of the poly(C)-binding heterogeneous nuclear ribonucleoprotein complex K protein , 1992, Molecular and cellular biology.

[121]  J. Keene,et al.  A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein , 1989, Cell.

[122]  G. Dreyfuss,et al.  RNA-binding proteins as developmental regulators. , 1989, Genes & development.

[123]  J. Adamson,et al.  Evidence for clonal development and stem cell origin of M7 megakaryocytic leukemia. , 1988, Leukemia.

[124]  G. Dreyfuss,et al.  Ribonucleoprotein particles in cellular processes , 1988, The Journal of cell biology.

[125]  R. Conaway,et al.  ATP activates transcription initiation from promoters by RNA polymerase II in a reversible step prior to RNA synthesis. , 1988, The Journal of biological chemistry.

[126]  G. Dreyfuss,et al.  Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins. , 1988, Genes & development.

[127]  M. Grunberg‐Manago,et al.  Nucleotide sequence of the pnp gene of Escherichia coli encoding polynucleotide phosphorylase. Homology of the primary structure of the protein with the RNA-binding domain of ribosomal protein S1. , 1987, The Journal of biological chemistry.

[128]  P. Keohavong,et al.  Mild nuclease treatment as a probe for a non-random distribution of adenovirus-specific RNA sequences and of cellular RNA in nuclear ribonucleoprotein fibrils. , 1982, Journal of molecular biology.

[129]  O. Samarina,et al.  Structural investigation of nuclear RNP particles containing pre-mRNA by different fluorescence techniques. , 1981, Nucleic acids research.

[130]  A. Beyer,et al.  Identification and characterization of the packaging proteins of core 40S hnRNP particles , 1977, Cell.

[131]  A. Bakken,et al.  Morphological studies of transcription. , 1972, Acta endocrinologica. Supplementum.

[132]  J. Molnár,et al.  Structural organization of nuclear complexes containing DNA-like RNA. , 1968, Journal of molecular biology.

[133]  G. Georgiev,et al.  Nuclear Ribonucleoprotein Particles Containing Messenger Ribonucleic Acid , 1966, Nature.

[134]  J. Gall SMALL GRANULES IN THE AMPHIBIAN OOCYTE NUCLEUS AND THEIR RELATIONSHIP TO RNA , 1956, The Journal of biophysical and biochemical cytology.