Protein universe containing a PUA RNA‐binding domain

Here, we review current knowledge about pseudouridine synthase and archaeosine transglycosylase (PUA)‐domain‐containing proteins to illustrate progress in this field. A methodological analysis of the literature about the topic was carried out, together with a ‘qualitative comparative analysis’ to give a more comprehensive review. Bioinformatics methods for whole‐protein or protein‐domain identification are commonly based on pairwise protein sequence comparisons; we added comparison of structures to detect the whole universe of proteins containing the PUA domain. We present an update of proteins having this domain, focusing on the specific proteins present in Homo sapiens (dyskerin, MCT1, Nip7, eIF2D and Nsun6), and explore the existence of these in other species. We also analyze the phylogenetic distribution of the PUA domain in different species and proteins. Finally, we performed a structural comparison of the PUA domain through data mining of structural databases, determining a conserved structural motif, despite the differences in the sequence, even among eukaryotes, archaea and bacteria. All data discussed in this review, both bibliographic and analytical, corroborate the functional importance of the PUA domain in RNA‐binding proteins.

[1]  K. Mazan-Mamczarz,et al.  MCT-1 protein interacts with the cap complex and modulates messenger RNA translational profiles. , 2006, Cancer research.

[2]  Michelle S. Scott,et al.  Characterization and prediction of protein nucleolar localization sequences , 2010, Nucleic acids research.

[3]  S. Aymerich,et al.  Crystal structure of a new RNA‐binding domain from the antiterminator protein SacY of Bacillus subtilis , 1997, The EMBO journal.

[4]  Gabriele Varani,et al.  The Cbf5–Nop10 complex is a molecular bracket that organizes box H/ACA RNPs , 2005, Nature Structural &Molecular Biology.

[5]  U. Meier,et al.  The many facets of H/ACA ribonucleoproteins , 2005, Chromosoma.

[6]  A. Ferré-D’Amaré,et al.  Cocrystal Structure of a tRNA Ψ55 Pseudouridine Synthase Nucleotide Flipping by an RNA-Modifying Enzyme , 2001, Cell.

[7]  E. Koonin,et al.  THUMP--a predicted RNA-binding domain shared by 4-thiouridine, pseudouridine synthases and RNA methylases. , 2001, Trends in biochemical sciences.

[8]  G. Montoya,et al.  Crystal structure of phosphoadenylyl sulphate (PAPS) reductase: a new family of adenine nucleotide alpha hydrolases. , 1997, Structure.

[9]  Mahavir Singh,et al.  Structure and Functional Studies of the CS Domain of the Essential H/ACA Ribonucleoparticle Assembly Protein SHQ1* , 2009, Journal of Biological Chemistry.

[10]  A. Komar,et al.  Activities of Ligatin and MCT-1/DENR in eukaryotic translation initiation and ribosomal recycling. , 2010, Genes & development.

[11]  Liisa Holm,et al.  Dali server: conservation mapping in 3D , 2010, Nucleic Acids Res..

[12]  A. Noor,et al.  Mutation in NSUN2, which encodes an RNA methyltransferase, causes autosomal-recessive intellectual disability. , 2012, American journal of human genetics.

[13]  H. Takagi,et al.  Functional Analysis of the C-Terminal Region of γ-Glutamyl Kinase of Saccharomyces cerevisiae , 2012, Bioscience, biotechnology, and biochemistry.

[14]  D. Barford,et al.  Structural insights into mRNA recognition from a PIWI domain–siRNA guide complex , 2005, Nature.

[15]  P. Strippoli,et al.  The human TruB family of pseudouridine synthase genes, including the Dyskeratosis Congenita 1 gene and the novel member TRUB1. , 2003, International journal of molecular medicine.

[16]  Hui Liu,et al.  Dyskerin Overexpression in Human Hepatocellular Carcinoma Is Associated with Advanced Clinical Stage and Poor Patient Prognosis , 2012, PloS one.

[17]  D. Xie,et al.  Structural evolution and functional diversification analyses of argonaute protein , 2012, Journal of cellular biochemistry.

[18]  K. Miyazono,et al.  Crystal structure of hypothetical protein PH0734.1 from hyperthermophilic archaea Pyrococcus horikoshii OT3 , 2008, Proteins.

[19]  R. Lehmann,et al.  The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. , 1997, RNA.

[20]  D. Baker,et al.  Crystal structure of a Cbf5-Nop10-Gar1 complex and implications in RNA-guided pseudouridylation and dyskeratosis congenita. , 2006, Molecular cell.

[21]  Andrei N. Lupas,et al.  CLANS: a Java application for visualizing protein families based on pairwise similarity , 2004, Bioinform..

[22]  O. Nureki,et al.  Crystal structure of archaeosine tRNA-guanine transglycosylase. , 2002, Journal of molecular biology.

[23]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[24]  E. C. Teixeira,et al.  Structural insights into the interaction of the Nip7 PUA domain with polyuridine RNA. , 2007, Biochemistry.

[25]  Robert M. Stroud,et al.  The structural basis for tRNA recognition and pseudouridine formation by pseudouridine synthase I , 2000, Nature Structural Biology.

[26]  Gabriele Varani,et al.  Protein families and RNA recognition , 2005, The FEBS journal.

[27]  I. Pérez-Arellano,et al.  The PUA domain − a structural and functional overview , 2007, The FEBS journal.

[28]  chen wang,et al.  Architecture and assembly of mammalian H/ACA small nucleolar and telomerase ribonucleoproteins , 2004, The EMBO journal.

[29]  A. Ferré-D’Amaré,et al.  Pseudouridine synthases. , 2006, Chemistry & biology.

[30]  H. Dyson,et al.  Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d , 2004, Nature Structural &Molecular Biology.

[31]  Shuang Li,et al.  Structure of the Shq1–Cbf5–Nop10–Gar1 complex and implications for H/ACA RNP biogenesis and dyskeratosis congenita , 2011, The EMBO journal.

[32]  D. Gomez,et al.  Telomere structure and telomerase in health and disease , 2012, International journal of oncology.

[33]  C. Bellodi,et al.  Deregulation of oncogene‐induced senescence and p53 translational control in X‐linked dyskeratosis congenita , 2010, The EMBO journal.

[34]  M. Furia,et al.  A new human dyskerin isoform with cytoplasmic localization. , 2011, Biochimica et biophysica acta.

[35]  T. Boulikas,et al.  Nuclear localization signals (NLS). , 1993, Critical reviews in eukaryotic gene expression.

[36]  Shuang Li,et al.  Reconstitution and structural analysis of the yeast box H/ACA RNA-guided pseudouridine synthase. , 2011, Genes & development.

[37]  W. Merrick,et al.  GTP-independent tRNA Delivery to the Ribosomal P-site by a Novel Eukaryotic Translation Factor* , 2010, The Journal of Biological Chemistry.

[38]  Hailing Jin,et al.  Role of small RNAs in host-microbe interactions. , 2010, Annual review of phytopathology.

[39]  E. Birney,et al.  Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. , 1993, Nucleic acids research.

[40]  Narmada Thanki,et al.  CDD: conserved domains and protein three-dimensional structure , 2012, Nucleic Acids Res..

[41]  J. L. Jennings,et al.  Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. , 2006, Genes & development.

[42]  E. Skordalakes,et al.  Structure of the RNA-binding domain of telomerase: implications for RNA recognition and binding. , 2007, Structure.

[43]  K. Kurvinen,et al.  Molecular Markers Implicating Early Malignant Events in Cervical Carcinogenesis , 2010, Cancer Epidemiology, Biomarkers & Prevention.

[44]  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.

[45]  Mingli Yang,et al.  JAZ Requires the Double-stranded RNA-binding Zinc Finger Motifs for Nuclear Localization* , 1999, The Journal of Biological Chemistry.

[46]  Alan Bridge,et al.  New and continuing developments at PROSITE , 2012, Nucleic Acids Res..

[47]  Laurie Smith,et al.  The RNA World of the Nucleolus: Two Major Families of Small RNAs Defined by Different Box Elements with Related Functions , 1996, Cell.

[48]  L. Regan,et al.  Structure and function of KH domains , 2008, The FEBS journal.

[49]  T. Vulliamy,et al.  Mutations in dyskeratosis congenita: their impact on telomere length and the diversity of clinical presentation. , 2006, Blood.

[50]  Yang Wang,et al.  Specific and Modular Binding Code for Cytosine Recognition in Pumilio/FBF (PUF) RNA-binding Domains*♦ , 2011, The Journal of Biological Chemistry.

[51]  Xinquan Wang,et al.  Crystal structure of KD93, a novel protein expressed in human hematopoietic stem/progenitor cells. , 2004, Journal of structural biology.

[52]  E. Birney,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..

[53]  Mensur Dlakic,et al.  DUF283 domain of Dicer proteins has a double-stranded RNA-binding fold , 2006, Bioinform..

[54]  A. Murzin.  OB(oligonucleotide/oligosaccharide binding)‐fold: common structural and functional solution for non‐homologous sequences. , 1993, The EMBO journal.

[55]  Ian Lee,et al.  RAP--a putative RNA-binding domain. , 2004, Trends in biochemical sciences.

[56]  Y. Tong,et al.  Crystal structure of human multiple copies in T‐cell lymphoma‐1 oncoprotein , 2013, Proteins.

[57]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[58]  S. Aymerich,et al.  Solution structure of the LicT–RNA antitermination complex: CAT clamping RAT , 2002, The EMBO journal.

[59]  Dagmar Wieczorek,et al.  Mutations in NSUN2 cause autosomal-recessive intellectual disability. , 2012, American journal of human genetics.

[60]  T. Kiss,et al.  Box H/ACA small ribonucleoproteins. , 2010, Molecular cell.

[61]  E. Koonin,et al.  Crystal structure of Bacillus anthracis ThiI, a tRNA-modifying enzyme containing the predicted RNA-binding THUMP domain. , 2005, Journal of molecular biology.

[62]  D. Draper,et al.  The crystal structure of ribosomal protein S4 reveals a two‐domain molecule with an extensive RNA‐binding surface: one domain shows structural homology to the ETS DNA‐binding motif , 1998, The EMBO journal.

[63]  E. Tacconelli.  Systematic reviews: CRD's guidance for undertaking reviews in health care , 2010 .

[64]  S. Yokoyama,et al.  Structures of a putative RNA 5-methyluridine methyltransferase, Thermus thermophilus TTHA1280, and its complex with S-adenosyl-L-homocysteine. , 2005, Acta crystallographica. Section F, Structural biology and crystallization communications.

[65]  V. Rubio,et al.  Dissection of Escherichia coli glutamate 5‐kinase: Functional impact of the deletion of the PUA domain , 2005, FEBS letters.

[66]  Sean R. Eddy,et al.  Profile hidden Markov models , 1998, Bioinform..

[67]  R. Terns,et al.  Formation of the conserved pseudouridine at position 55 in archaeal tRNA , 2006, Nucleic acids research.

[68]  Bernd Hinzmann,et al.  Insights into the evolution of the nucleolus by an analysis of its protein domain repertoire. , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[69]  Allen F. Brooks,et al.  Evolution of eukaryal tRNA-guanine transglycosylase: insight gained from the heterocyclic substrate recognition by the wild-type and mutant human and Escherichia coli tRNA-guanine transglycosylases , 2010, Nucleic acids research.

[70]  L. Aravind,et al.  Novel Predicted RNA-Binding Domains Associated with the Translation Machinery , 1999, Journal of Molecular Evolution.

[71]  P. Forterre,et al.  Mining archaeal proteomes for eukaryotic proteins with novel functions: the PACE case. , 2000, Trends in genetics : TIG.

[72]  F. Alawi,et al.  Loss of dyskerin reduces the accumulation of a subset of H/ACA snoRNA-derived miRNA , 2010, Cell cycle.