The Nucleolus of Caenorhabditis elegans

Nucleolar size and appearance correlate with ribosome biogenesis and cellular activity. The mechanisms underlying changes in nucleolar appearance and regulation of nucleolar size that occur during differentiation and cell cycle progression are not well understood. Caenorhabditis elegans provides a good model for studying these processes because of its small size and transparent body, well-characterized cell types and lineages, and because its cells display various sizes of nucleoli. This paper details the advantages of using C. elegans to investigate features of the nucleolus during the organism's development by following dynamic changes in fibrillarin (FIB-1) in the cells of early embryos and aged worms. This paper also illustrates the involvement of the ncl-1 gene and other possible candidate genes in nucleolar-size control. Lastly, we summarize the ribosomal proteins involved in life span and innate immunity, and those homologous genes that correspond to human disorders of ribosomopathy.

[1]  Sui Huang,et al.  The perinucleolar compartment. , 2010, Cold Spring Harbor perspectives in biology.

[2]  K. Wilson,et al.  The expression, lamin-dependent localization and RNAi depletion phenotype for emerin in C. elegans. , 2002, Journal of cell science.

[3]  Daniele Zink,et al.  Nuclear structure in cancer cells , 2004, Nature Reviews Cancer.

[4]  J. Wasmuth,et al.  Positional cloning of a gene involved in the pathogenesis of Treacher Collins syndrome , 1996, Nature Genetics.

[5]  D. Killian,et al.  C. elegans pro-1 activity is required for soma/germline interactions that influence proliferation and differentiation in the germ line , 2004, Development.

[6]  A. Coulson,et al.  The rDNA of C. elegans: sequence and structure. , 1986, Nucleic acids research.

[7]  M. Lovett,et al.  TCOF1 gene encodes a putative nucleolar phosphoprotein that exhibits mutations in Treacher Collins Syndrome throughout its coding region. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[8]  H. Pi,et al.  New insights into polycistronic transcripts in eukaryotes. , 2009, Chang Gung medical journal.

[9]  S. Lo,et al.  The nucleolus: reviewing oldies to have new understandings , 2006, Cell Research.

[10]  L. Romanova,et al.  Critical Role of Nucleostemin in Pre-rRNA Processing* , 2009, Journal of Biological Chemistry.

[11]  Two highly conserved transcribed regions in the 5S DNA repeats of the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. , 1989, Nucleic acids research.

[12]  J. Berg Genome sequence of the nematode C. elegans: a platform for investigating biology. , 1998, Science.

[13]  Peter Gregor,et al.  NOPdb: Nucleolar Proteome Database—2008 update , 2008, Nucleic Acids Res..

[14]  S. White,et al.  RNAi-mediated chromatin silencing in fission yeast. , 2008, Current topics in microbiology and immunology.

[15]  Johanna M. Rommens,et al.  Mutations in SBDS are associated with Shwachman–Diamond syndrome , 2003, Nature Genetics.

[16]  E. Hedgecock,et al.  The ncl-1 gene and genetic mosaics of Caenorhabditis elegans. , 1995, Genetics.

[17]  Christopher Y. Park,et al.  Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects , 2008, Nature Genetics.

[18]  D. Birnbaum,et al.  Intracellular trafficking of LET-756, a fibroblast growth factor of C. elegans, is controlled by a balance of export and nuclear signals. , 2006, Experimental cell research.

[19]  Li-Wei Lee,et al.  Vectors for co-expression of two genes in Caenorhabditis elegans. , 2010, Gene.

[20]  Michelle M. Kudron,et al.  C. elegans Nucleostemin Is Required for Larval Growth and Germline Stem Cell Division , 2008, PLoS genetics.

[21]  M. Lesley The Relation between Satellite Size and Nucleolus Size in Three Races of Solanum Lycopersicum. , 1938, Genetics.

[22]  Paul W Sternberg,et al.  Genetic dissection of developmental pathways. , 2006, WormBook : the online review of C. elegans biology.

[23]  M. Hall,et al.  TOR Signaling in Growth and Metabolism , 2006, Cell.

[24]  R. Kamath,et al.  Genome-wide RNAi screening in Caenorhabditis elegans. , 2003, Methods.

[25]  C. Ushida,et al.  Isolation and Characterization of Small RNAs in Caenorhabditis elegans , 2009 .

[26]  Yosef Gruenbaum,et al.  Age-related changes of nuclear architecture in Caenorhabditis elegans. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[27]  T. Pederson,et al.  In search of nonribosomal nucleolar protein function and regulation , 2009, The Journal of cell biology.

[28]  S. Lo,et al.  Ser-123 of the large antigen of hepatitis delta virus modulates its cellular localization to the nucleolus, SC-35 speckles or the cytoplasm. , 2004, The Journal of general virology.

[29]  Marc S. Williams,et al.  Analysis of RPS19 in patients with cartilage‐hair hypoplasia and severe anemia: Preliminary results , 2005, American journal of medical genetics. Part A.

[30]  H. Wu,et al.  Post-translational modification of delta antigen of hepatitis D virus. , 2006, Current topics in microbiology and immunology.

[31]  Lesilee S. Rose,et al.  Asymmetric cell division and axis formation in the embryo. , 2005, WormBook : the online review of C. elegans biology.

[32]  M. Lai The molecular biology of hepatitis delta virus. , 1990, Annual review of biochemistry.

[33]  M. Thiry,et al.  Ultrastructural changes of the carp (Cyprinus carpio) hepatocyte nucleolus during seasonal acclimatization , 2006, Biology of the cell.

[34]  S. Ellis,et al.  Diamond Blackfan anemia 2008–2009: broadening the scope of ribosome biogenesis disorders , 2010, Current opinion in pediatrics.

[35]  G. Ruvkun,et al.  Lifespan Regulation by Evolutionarily Conserved Genes Essential for Viability , 2007, PLoS genetics.

[36]  Sean R Eddy,et al.  C. elegans noncoding RNA genes. , 2005, WormBook : the online review of C. elegans biology.

[37]  I. Ruvinsky,et al.  Computational prediction of Caenorhabditis box H/ACA snoRNAs using genomic properties of their host genes. , 2010, RNA.

[38]  D. Albertson Localization of the ribosomal genes in Caenorhabditis elegans chromosomes by in situ hybridization using biotin‐labeled probes. , 1984, The EMBO journal.

[39]  N. Munakata [Genetics of Caenorhabditis elegans]. , 1989, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[40]  D. Frank,et al.  ncl-1 Is Required for the Regulation of Cell Size and Ribosomal RNA Synthesis in Caenorhabditis elegans , 1998, The Journal of cell biology.

[41]  G. Morris,et al.  The Cajal body. , 2008, Biochimica et biophysica acta.

[42]  Kunio Inoue,et al.  RBD-1, a nucleolar RNA-binding protein, is essential for Caenorhabditis elegans early development through 18S ribosomal RNA processing. , 2004, Nucleic acids research.

[43]  S. Lockery,et al.  Developmental control of lateralized neuron size in the nematode Caenorhabditis elegans , 2010, Neural Development.

[44]  J. Apfeld,et al.  The Caenorhabditis elegans Germ Line Regulates Distinct Signaling Pathways to Control Lifespan and Innate Immunity* , 2009, The Journal of Biological Chemistry.

[45]  M. Lai RNA Replication without RNA-Dependent RNA Polymerase: Surprises from Hepatitis Delta Virus , 2005, Journal of Virology.

[46]  Chia-Yi Hsu,et al.  Chromatin tethering effects of hNopp140 are involved in the spatial organization of nucleolus and the rRNA gene transcription , 2008, Journal of biomedical science.

[47]  T. Powers,et al.  Regulation of ribosome biogenesis: where is TOR? , 2006, Cell metabolism.

[48]  Roumen Voutev,et al.  Alterations in ribosome biogenesis cause specific defects in C. elegans hermaphrodite gonadogenesis. , 2006, Developmental biology.

[49]  K. Zeller,et al.  Alterations in nucleolar structure and gene expression programs in prostatic neoplasia are driven by the MYC oncogene. , 2011, The American journal of pathology.

[50]  M. Thiry,et al.  Nucleolar Changes and Fibrillarin Redistribution Following Apatone Treatment of Human Bladder Carcinoma Cells , 2010, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[51]  F. Boisvert,et al.  The Nucleolus under Stress , 2010, Molecular Cell.

[52]  J. Gall,et al.  Cajal bodies: the first 100 years. , 2000, Annual review of cell and developmental biology.

[53]  Jean Thierry-Mieg,et al.  A global analysis of Caenorhabditis elegans operons , 2002, Nature.

[54]  K. Shianna,et al.  Nucleolar Proteins Suppress Caenorhabditis elegans Innate Immunity by Inhibiting p53/CEP-1 , 2009, PLoS genetics.

[55]  Thomas Blumenthal,et al.  Caenorhabditis elegans operons: form and function , 2003, Nature Reviews Genetics.

[56]  S. Mango,et al.  The Target of Rapamycin Pathway Antagonizes pha-4/FoxA to Control Development and Aging , 2008, Current Biology.

[57]  K. Entian,et al.  Mutation of a gene essential for ribosome biogenesis, EMG1, causes Bowen-Conradi syndrome. , 2009, American journal of human genetics.

[58]  A. Shearn,et al.  Mutations in the β-propeller domain of the Drosophila brain tumor (brat) protein induce neoplasm in the larval brain , 2000, Oncogene.

[59]  J. Yochem Nomarski images for learning the anatomy, with tips for mosaic analysis. , 2006, WormBook : the online review of C. elegans biology.

[60]  B. Edgar,et al.  The Drosophila melanogaster gene brain tumor negatively regulates cell growth and ribosomal RNA synthesis. , 2002, Development.

[61]  D. Treré,et al.  Nucleolar size indicates the rapidity of cell proliferation in cancer tissues , 2000, The Journal of pathology.

[62]  M. Blaxter Nematodes: The Worm and Its Relatives , 2011, PLoS biology.

[63]  H. Handa,et al.  Hepatitis Delta Virus , 2006 .

[64]  C. Hong,et al.  Multi-Step Usage of in Vivo Models During Rational Drug Design and Discovery , 2011, International journal of molecular sciences.

[65]  Seung-Jae V. Lee,et al.  Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans , 2007, Aging cell.

[66]  D. Tollervey,et al.  Box C/D small nucleolar RNA trafficking involves small nucleolar RNP proteins, nucleolar factors and a novel nuclear domain , 2001, The EMBO journal.

[67]  J. Sulston,et al.  The DNA of Caenorhabditis elegans. , 1974, Genetics.

[68]  B. Ebert,et al.  Ribosomopathies: human disorders of ribosome dysfunction. , 2010, Blood.

[69]  L. Montanaro,et al.  Nucleolar Size and Activity Are Related to pRb and p53 Status in Human Breast Cancer , 2004, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[70]  P. Jiang,et al.  Altered subcellular distribution of nucleolar protein fibrillarin by actinomycin D in HEp-2 cells. , 2004, Acta pharmacologica Sinica.

[71]  D. Jackson,et al.  Lamin B1 maintains the functional plasticity of nucleoli , 2009, Journal of Cell Science.

[72]  D. Fay Genetic mapping and manipulation: chapter 1--Introduction and basics. , 2006, WormBook : the online review of C. elegans biology.

[73]  A. Gregory Matera,et al.  Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product , 2001, The Journal of cell biology.

[74]  S. Lo,et al.  The HDV large-delta antigen fused with GFP remains functional and provides for studying its dynamic distribution. , 2001, Virology.

[75]  A. Fire,et al.  Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. , 2001, Gene.

[76]  Iva Greenwald,et al.  OrthoList: A Compendium of C. elegans Genes with Human Orthologs , 2011, PloS one.

[77]  W. Sewell,et al.  Do ribosomopathies explain some cases of common variable immunodeficiency? , 2011, Clinical and experimental immunology.

[78]  F. Boisvert,et al.  The multifunctional nucleolus , 2007, Nature Reviews Molecular Cell Biology.