Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter January 27, 2014

Human dyskerin: beyond telomeres

  • Alberto Angrisani

    Alberto Angrisani graduated in Molecular and Industrial Biotechology at the University of Naples “Federico II” in 2007, with a dissertation on the transcriptional activity of the human DKC1 gene. In 2011 he received his PhD in Genetics and Molecular Medicine for the identification of new human DKC1 gene transcripts. At present he works as PostDoc in Prof. Furia’s laboratory. Up to the present day his research interests have been focused on the study of the role of snoRNAs and snoRNP complexes in development and cancerogenesis.

    , Rosario Vicidomini

    Rosario Vicidomini studied at the University of Naples Federico II and received his degree in Biology in 2010, with a dissertation on the applications of the laser microdissection technique to the study of developmental transcriptome. As a PhD student in Genetics and Molecular Medicine he studied the telomerase-independent roles of H/ACA snoRNPs, mainly using Drosophila as model system, under Prof. Furia’s supervision. In 2013, he spent a six-month stage in Annette’s Preiss lab (Stuttgard), studying the regulation of Notch signalling.

    , Mimmo Turano

    Mimmo Turano achieved a degree in Biological Sciences at the Faculty of Sciences of University of Naples “Federico II” in 1995. From 1995 to 2003 he focused his research activity mainly on the functional role of the frataxin in the pathogenesis of the Fried-reich ataxia disease, at the Department of Biology and Cellular and Molecular Pathology. From 2004 to 2006 his scientific interest turned mainly to the understanding of the role of HEXIM1 protein on the inhibition of the transcription elongation factor P-TEFb. Since 2006 he is Research Fellow at the Biology Department of University of Naples and joined Prof. Maria Furia’s laboratory, working on the molecular characterization of the DKC1 human gene.

    and Maria Furia

    Maria Furia graduated in Biology at the University of Naples Federico II in 1971. After fellowships at the Zoological Station Anton Dohrn (Naples), at the Imperial College (London), and at the Indiana University (Bloogmington), she became Associate Professor of Genetics at the University of Naples in 1985; Professor of Genetics since 2000, and Head of the Department of Genetics, General and Molecular Biology from 2001 to 2004. The work of her laboratory is concentrated on developmental biology, mainly using Drosophila as model system, and is presently specifically focussed on the study of biological functions carried out by snoRNPs in both Drosophila and man.

    EMAIL logo
From the journal Biological Chemistry

Abstract

Human dyskerin is an evolutively conserved protein that participates in diverse nuclear complexes: the H/ACA snoRNPs, that control ribosome biogenesis, RNA pseudouridylation, and stability of H/ACA snoRNAs; the scaRNPs, that control pseudouridylation of snRNAs; and the telomerase active holoenzyme, which safeguards telomere integrity. The biological importance of dyskerin is further outlined by the fact that its deficiency causes the X-linked dyskeratosis congenita disease, while its over-expression characterizes several types of cancers and has been proposed as prognostic marker. The role of dyskerin in telomere maintenance has widely been discussed, while its functions as H/ACA sno/scaRNP component has been so far mostly overlooked and represent the main goal of this review. Here we summarize how increasing evidence indicates that the snoRNA/microRNA pathways can be interlaced, and that dyskerin-dependent RNA pseudouridylation represents a flexible mechanism able to modulate RNA function in different ways, including modulation of splicing, change of mRNA coding properties, and selective regulation of IRES-dependent translation. We also propose a speculative model that suggests that the dynamics of pre-assembly and nuclear import of H/ACA RNPs are crucial regulatory steps that can be finely controlled in the cytoplasm in response to developmental, differentiative and stress stimuli.


Corresponding author: Maria Furia, Dipartimento di Biologia, Università di Napoli ‘Federico II’, via Cinthia, I-80126 Naples, Italy, email:
aThese authors contributed equally to this work.

About the authors

Alberto Angrisani

Alberto Angrisani graduated in Molecular and Industrial Biotechology at the University of Naples “Federico II” in 2007, with a dissertation on the transcriptional activity of the human DKC1 gene. In 2011 he received his PhD in Genetics and Molecular Medicine for the identification of new human DKC1 gene transcripts. At present he works as PostDoc in Prof. Furia’s laboratory. Up to the present day his research interests have been focused on the study of the role of snoRNAs and snoRNP complexes in development and cancerogenesis.

Rosario Vicidomini

Rosario Vicidomini studied at the University of Naples Federico II and received his degree in Biology in 2010, with a dissertation on the applications of the laser microdissection technique to the study of developmental transcriptome. As a PhD student in Genetics and Molecular Medicine he studied the telomerase-independent roles of H/ACA snoRNPs, mainly using Drosophila as model system, under Prof. Furia’s supervision. In 2013, he spent a six-month stage in Annette’s Preiss lab (Stuttgard), studying the regulation of Notch signalling.

Mimmo Turano

Mimmo Turano achieved a degree in Biological Sciences at the Faculty of Sciences of University of Naples “Federico II” in 1995. From 1995 to 2003 he focused his research activity mainly on the functional role of the frataxin in the pathogenesis of the Fried-reich ataxia disease, at the Department of Biology and Cellular and Molecular Pathology. From 2004 to 2006 his scientific interest turned mainly to the understanding of the role of HEXIM1 protein on the inhibition of the transcription elongation factor P-TEFb. Since 2006 he is Research Fellow at the Biology Department of University of Naples and joined Prof. Maria Furia’s laboratory, working on the molecular characterization of the DKC1 human gene.

Maria Furia

Maria Furia graduated in Biology at the University of Naples Federico II in 1971. After fellowships at the Zoological Station Anton Dohrn (Naples), at the Imperial College (London), and at the Indiana University (Bloogmington), she became Associate Professor of Genetics at the University of Naples in 1985; Professor of Genetics since 2000, and Head of the Department of Genetics, General and Molecular Biology from 2001 to 2004. The work of her laboratory is concentrated on developmental biology, mainly using Drosophila as model system, and is presently specifically focussed on the study of biological functions carried out by snoRNPs in both Drosophila and man.

Acknowledgments

This work was supported by University Federico II of Naples and by P.O.R. Campania FSE 2007–2013 Project CREMe, which supported Alberto Angrisani’s postdoctoral fellowship.

References

Agarwal, S., Loh, Y.H., McLoughlin, E.M., Huang, J., Park, I.H., Miller, J.D., Huo, H., Okuka, M., Dos Reis, R.M., Loewer, S., et al. (2010). Telomere elongation in induced pluripotent stem cells from dyskeratosis congenita patients. Nature 464, 292–296.10.1038/nature08792Search in Google Scholar PubMed PubMed Central

Alawi, F. and Lin, P. (2010). Loss of dyskerin reduces the accumulation of a subset of H/ACA snoRNA-derived miRNA. Cell Cycle 9, 2467–2469.10.4161/cc.9.12.11922Search in Google Scholar PubMed PubMed Central

Alawi, F. and Lin, P. (2011). Dyskerin is required for tumor cell growth through mechanisms that are independent of its role in telomerase and only partially related to its function in precursor rRNA processing. Mol. Carcinog. 50, 334–345.10.1002/mc.20715Search in Google Scholar PubMed PubMed Central

Alawi, F. and Lin, P. (2013). Dyskerin localizes to the mitotic apparatus and is required for orderly mitosis in human cells. PLoS One 8, e80805.10.1371/journal.pone.0080805Search in Google Scholar PubMed PubMed Central

Alter, B.P., Giri, N., Savage, S.A., and Rosenberg, P.S. (2009). Cancer in dyskeratosis congenita. Blood 113, 6549–6557.10.1182/blood-2008-12-192880Search in Google Scholar PubMed PubMed Central

Angrisani, A., Turano, M., Paparo, L., Di Mauro, C., and Furia, M. (2011). A new human dyskerin isoform with cytoplasmic localization. Biochim. Biophys. Acta 1810, 1361–1368.10.1016/j.bbagen.2011.07.012Search in Google Scholar PubMed

Ballarino, M., Morlando, M., Pagano, F., Fatica, A., and Bozzoni, I. (2005). The cotranscriptional assembly of snoRNPs controls the biosynthesis of H/ACA snoRNAs in Saccharomyces cerevisiae. Mol. Cell Biol. 25, 5396–5403.10.1128/MCB.25.13.5396-5403.2005Search in Google Scholar PubMed PubMed Central

Batista, L.F., Pech, M.F., Zhong, F.L., Nguyen, H.N., Xie, K.T., Zaug, A.J., Crary, S.M., Choi, J., Sebastiano, V., Cherry, A., et al. (2011). Telomere shortening and loss of self-renewal in dyskeratosis congenita induced pluripotent stem cells. Nature 474, 399–402.10.1038/nature10084Search in Google Scholar PubMed PubMed Central

Bellodi, C., Krasnykh, O., Haynes, N., Theodoropoulou, M., Peng, G., Montanaro, L., and Ruggero, D. (2010). Loss of function of the tumor suppressor DKC1 perturbs p27 translation control and contributes to pituitary tumorigenesis. Cancer Res. 70, 6026–6035.10.1158/0008-5472.CAN-09-4730Search in Google Scholar PubMed PubMed Central

Bellodi, C., McMahon, M., Contreras, A., Juliano, D., Kopmar, N., Nakamura, T., Maltby, D., Burlingame, A., Savage, S.A., Shimamura, A., et al. (2013). H/ACA small RNA dysfunctions in disease reveal key roles for noncoding RNA modifications in hematopoietic stem cell differentiation. Cell. Rep. 3, 1493–1502.10.1016/j.celrep.2013.04.030Search in Google Scholar PubMed PubMed Central

Blomster, H.A., Hietakangas, V., Wu, J., Kouvonen, P., Hautaniemi, S., and Sistonen, L. (2009). Novel proteomics strategy brings insight into the prevalence of SUMO-2 target sites. Mol. Cell. Proteomics 8, 1382–1390.10.1074/mcp.M800551-MCP200Search in Google Scholar PubMed PubMed Central

Brault, M.E., Lauzon, C., and Autexier, C. (2013). Dyskeratosis congenita mutations in dyskerin SUMOylation consensus sites lead to impaired telomerase RNA accumulation and telomere defects. Hum. Mol. Genet. 22, 3498–3507.10.1093/hmg/ddt204Search in Google Scholar PubMed

Cadwell, C., Yoon, H.J., Zebarjadian, Y., and Carbon, J. (1997). The yeast nucleolar protein Cbf5p is involved in rRNA biosynthesis and interacts genetically with the RNA polymerase I transcription factor RRN3. Mol. Cell Biol. 17, 6175–6183.10.1128/MCB.17.10.6175Search in Google Scholar PubMed PubMed Central

Carrillo, J., Gonzalez, A., Manguan-Garcıa, C., Pintado-Berninches, L., and Perona, R. (2013). p53 pathway activation by telomere attrition in X-DC primary fibroblasts occurs in the absence of ribosome biogenesis failure and as a consequence of DNA damage. Clin. Transl. Oncol. [Epub ahead of print].Search in Google Scholar

Chen, C., Zhao, X., Kierzek, R., and Yu, Y.T. (2010). A flexible RNA backbone within the polypyrimidine tract is required for U2AF65 binding and pre-mRNA splicing in vivo. Mol. Cell. Biol. 30, 4108–4119.10.1128/MCB.00531-10Search in Google Scholar PubMed PubMed Central

Cohen, S.B., Graham, M.E., Lovrecz, G.O., Bache, N., Robinson, P.J., and Reddel, R.R. (2007). Protein composition of catalytically active human telomerase from immortal cells. Science 315, 1850–1853.10.1126/science.1138596Search in Google Scholar PubMed

Darzacq, X., Kittur, N., Roy, S., Shav-Tal, Y., Singer, R.H., and Meier, U.T. (2006). Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J. Cell. Biol. 173, 207–218.10.1083/jcb.200601105Search in Google Scholar PubMed PubMed Central

Davis, D.R. (1995). Stabilization of RNA stacking by pseudouridine. Nucleic Acids Res. 23, 5020–5026.10.1093/nar/23.24.5020Search in Google Scholar PubMed PubMed Central

Dephoure, N., Zhou, C., Villen, J., Beausoleil, S.A., Bakalarski, C.E., Elledge, S.J., and Gygi, S.P. (2008). A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105, 10762–10767.10.1073/pnas.0805139105Search in Google Scholar PubMed PubMed Central

Dez, C., Noaillac-Depeyre, J., Caizergues-Ferrer, M., and Henry, Y. (2002). Naf1p, an essential nucleoplasmic factor specifically required for accumulation of box H/ACA small nucleolar RNPs. Mol. Cell Biol. 22, 7053–7065.10.1128/MCB.22.20.7053-7065.2002Search in Google Scholar PubMed PubMed Central

Ding, Z., Wu, C.J., Jaskelioff, M., Ivanova, E., Kost-Alimova, M., Protopopov, A., Chu, G.C., Wang, G., Lu, X., Labrot, E.S., et al. (2012). Telomerase reactivation following telomere dysfunction yields murine prostate tumors with bone metastases. Cell 148, 896–907.10.1016/j.cell.2012.01.039Search in Google Scholar PubMed PubMed Central

Dokal, I. (2011). Dyskeratosis congenita. Hematology Am. Soc. Hematol. Educ. Program. 2011, 480–486.10.1182/asheducation-2011.1.480Search in Google Scholar PubMed

Dokal, I., Bungey, J., Williamson, P., Oscier, D., Hows, J., and Luzzatto, L. (1992). Dyskeratosis congenita fibroblasts are abnormal and have unbalanced chromosomal rearrangements. Blood 80, 3090–3096.10.1182/blood.V80.12.3090.3090Search in Google Scholar

Egan, E.D. and Collins, K. (2010). Specificity and stoichiometry of subunit interactions in the human telomerase holoenzyme assembled in vivo. Mol. Cell. Biol. 30, 2775–2786.10.1128/MCB.00151-10Search in Google Scholar PubMed PubMed Central

Ender, C., Krek, A., Friedländer, M.R., Beitzinger M., Weinmann, L., Chen, W., Pfeffer, S,. Rajewsky, N., and Meister, G. (2008). A human snoRNA with microRNA-like functions. Mol. Cell 32, 519–528.10.1016/j.molcel.2008.10.017Search in Google Scholar PubMed

Fatica, A., Dlakic, M., and Tollervey, D. (2002). Naf1p is a box H/ACA snoRNP assembly factor. RNA 8, 1502–1514.10.1017/S1355838202022094Search in Google Scholar

Forbes, S.A., Bindal, N., Bamford, S., Cole, C., Kok, C.Y., Beare, D., Jia, M., Shepherd, R., Leung, K., Menzies, A., et al. (2011). COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 39 (Database issue), D945–950.10.1093/nar/gkq929Search in Google Scholar PubMed PubMed Central

Ge, J. and Yu, Y.T. (2013). RNA pseudouridylation: new insights into an old modification. Trends Biochem. Sci. 38, 210–218.10.1016/j.tibs.2013.01.002Search in Google Scholar PubMed PubMed Central

Ge, J., Rudnick, D.A., He, J., Crimmins, D.L., Ladenson, J.H., Bessler, M., and Mason, P.J. (2010). Dyskerin ablation in mouse liver inhibits rRNA processing and cell division. Mol. Cell. Biol. 30, 413–422.10.1128/MCB.01128-09Search in Google Scholar PubMed PubMed Central

Giordano, E., Peluso, I., Senger, S., and Furia M. (1999). Minifly, a Drosophila gene required for ribosome biogenesis. J. Cell. Biol. 144, 1123–1133.10.1083/jcb.144.6.1123Search in Google Scholar PubMed PubMed Central

Grozdanov, P.N., Roy, S., Kittur, N., and Meier, U.T. (2009a). SHQ1 is required prior to NAF1 for assembly of H/ACA small nucleolar and telomerase RNPs. RNA 15, 1188–1197.10.1261/rna.1532109Search in Google Scholar PubMed PubMed Central

Grozdanov, P.N., Fernandez-Fuentes, N., Fiser, A., and Meier, U.T. (2009b). Pathogenic NAP57 mutations decrease ribonucleoprotein assembly in dyskeratosis congenita. Hum. Mol. Genet. 18, 4546–4551.10.1093/hmg/ddp416Search in Google Scholar PubMed PubMed Central

Gu, B.W., Fan, J.M., Bessler, M., and Mason, P.J. (2011). Accelerated hematopoietic stem cell aging in a mouse model of dyskeratosis congenita responds to antioxidant treatment. Aging Cell 10, 338–348.10.1111/j.1474-9726.2011.00674.xSearch in Google Scholar PubMed PubMed Central

Gu, B.W., Ge, J., Fan, J.M., Bessler, M., and Mason, P.J. (2013). Slow growth and unstable ribosomal RNA lacking pseudouridine in mouse embryonic fibroblast cells expressing catalytically inactive dyskerin. FEBS Lett. 58, 2112–2117.10.1016/j.febslet.2013.05.028Search in Google Scholar PubMed PubMed Central

Hamma, T., Reichow, S.L., Varani, G., and Ferré-D’Amaré, A.R. (2005). The Cbf5-Nop10 complex is a molecular bracket that organizes box H/ACA RNPs. Nat. Struct. Mol. Biol. 12, 1101–1107.10.1038/nsmb1036Search in Google Scholar PubMed

He, J., Navarrete, S., Jasinski, M., Vulliamy, T., Dokal, I., Bessler, M., and Mason, P.J. (2002). Targeted disruption of Dkc1, the gene mutated in X-linked dyskeratosis congenita, causes embryonic lethality in mice. Oncogene 21, 7740–7744.10.1038/sj.onc.1205969Search in Google Scholar PubMed

Heiss, N.S., Knight, S.W., Vulliamy, T.J., Klauck, S.M., Wiemann, S., Mason, P.J., Poustka, A., and Dokal, I. (1998). X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat. Genet. 19, 32–38.10.1038/ng0598-32Search in Google Scholar PubMed

Hoareau-Aveilla, C., Bonoli, M., Caizergues-Ferrer, M., and Henry, Y. (2006). hNaf1 is required for accumulation of human box H/ACA snoRNPs, scaRNPs, and telomerase. RNA 12, 832–840.10.1261/rna.2344106Search in Google Scholar PubMed PubMed Central

Hu, J., Hwang, S.S., Liesa, M., Gan, B., Sahin, E., Jaskelioff, M., Ding, Z., Ying, H., Boutin, A.T., Zhang, H., et al. (2012). Antitelomerase therapy provokes ALT and mitochondrial adaptive mechanisms in cancer. Cell 148, 651–663.10.1016/j.cell.2011.12.028Search in Google Scholar PubMed PubMed Central

Jack, K., Bellodi, C., Landry, D.M., Niederer, R.O., Meskauskas, A., Musalgaonkar, S., Kopmar, N., Krasnykh, O., Dean, A.M., Thompson, S.R., et al. (2011). rRNA pseudouridylation defects affect ribosomal ligand binding and translational fidelity from yeast to human cells. Mol. Cell 44, 660–666.10.1016/j.molcel.2011.09.017Search in Google Scholar PubMed PubMed Central

Jiang, W., Middleton, K., Yoon, H.J., Fouquet, C., and Carbon, J. (1993). An essential yeast protein, CBF5p, binds in vitro to centromeres and microtubules. Mol. Cell. Biol. 13, 4884–4893.Search in Google Scholar

Jung, C.H., Hansen, M.A., Makunin, I.V., Korbie, D.J., and Mattick, J.S. (2010). Identification of novel non-coding RNAs using profiles of short sequence reads from next generation sequencing data. BMC Genomics 11:77.Search in Google Scholar

Karijolich, J. and Yu, Y.T. (2011). Converting nonsense codons into sense codons by targeted pseudouridylation. Nature 474, 395–398.10.1038/nature10165Search in Google Scholar PubMed PubMed Central

Khanna, A. and Stamm, S. (2010). Regulation of alternative splicing by short non-coding nuclear RNAs. RNA Biol. 7, 480–485.10.4161/rna.7.4.12746Search in Google Scholar PubMed PubMed Central

Kirwan, M. and Dokal, I. (2008). Dyskeratosis congenita: a genetic disorder of many faces. Clin. Genet. 73, 103–112.10.1111/j.1399-0004.2007.00923.xSearch in Google Scholar

Kiss, T., Fayet, E., Jády, B.E., Richard, P. and Weber, M. (2006). Biogenesis and intranuclear trafficking of human box C/D and H/ACA RNPs. Cold Spring Harb. Symp. Quant. Biol. 71, 407–417.10.1101/sqb.2006.71.025Search in Google Scholar

Kittur, N., Darzacq, X., Roy, S., Singer, R.H., and Meier, U.T. (2006). Dynamic association and localization of human H/ACA RNP proteins. RNA 12, 2057–2062.10.1261/rna.249306Search in Google Scholar

Knight, S.W., Heiss, N.S., Vulliamy, T.J., Aalfs, C.M., McMahon, C., Richmond, P., Jones, A., Hennekam, R.C., Poustka, A., Mason, P.J., et al. (1999). Unexplained aplastic anaemia, immunodeficiency, and cerebellar hypoplasia (Hoyeraal-Hreidarsson syndrome). due to mutations in the dyskeratosis congenita gene, DKC1. Br. J. Haematol. 107, 335–339.10.1046/j.1365-2141.1999.01690.xSearch in Google Scholar

Lafontaine, D.L. and Tollervey, D. (1998). Birth of the snoRNPs: the evolution of the modification-guide snoRNAs. Trends Biochem. Sci. 23, 383–388.10.1016/S0968-0004(98)01260-2Search in Google Scholar

Lestrade, L. and Weber, M.J. (2006). snoRNA-LBME-db, a comprehensive database of human H/ACA and C/D box snoRNAs. Nucleic Acids Res. 34 (Database issue), D158–D162.10.1093/nar/gkj002Search in Google Scholar PubMed PubMed Central

Leulliot, N., Godin, K.S., Hoareau-Aveilla, C., Quevillon-Cheruel, S., Varani, G., Henry, Y., and Van Tilbeurgh, H. (2007). The box H/ACA RNP assembly factor Naf1p contains a domain homologousto Gar1p mediating its interaction with Cbf5p. J. Mol. Biol. 371, 1338–1353.10.1016/j.jmb.2007.06.031Search in Google Scholar PubMed

Li, L. and Ye, K. (2006). Crystal structure of an H/ACA box ribonucleoprotein particle. Nature 443, 302–307.10.1038/nature05151Search in Google Scholar PubMed

Li, S., Duan, J., Li, D., Yang, B., Dong, M. and Ye, K. (2011). Reconstitution and structural analysis of the yeast box H/ACA RNA-guided pseudouridine synthase. Genes Dev. 25, 2409–2421.10.1101/gad.175299.111Search in Google Scholar PubMed PubMed Central

Lin, X. and Momany, M. (2003). The Aspergillus nidulans swoC1 mutant shows defects in growth and development. Genetics 165, 543–554.10.1093/genetics/165.2.543Search in Google Scholar PubMed PubMed Central

Liu, B., Zhang, J., Huang, C., and Liu, H. (2012). Dyskerin overexpression in human hepatocellular carcinoma is associated with advanced clinical stage and poor patient prognosis. PLoS One 7, e43147.10.1371/journal.pone.0052675Search in Google Scholar

Luzzatto, L. and Karadimitris, A. (1998). Dyskeratosis and ribosomal rebellion. Nat. Genet. 19, 6–7.10.1038/ng0598-6Search in Google Scholar

Maceluch, J., Kmieciak, M., Szweykowska-Kulińska, Z., and Jarmołowski, A. (2001). Cloning and characterization of Arabidopsis thaliana AtNAP57 – a homologue of yeast pseudouridine synthase Cbf5p. Acta Biochim. Pol. 48, 699–709.10.18388/abp.2001_3904Search in Google Scholar

Maden, B.E. (1990). The numerous modified nucleotides in eukaryotic ribosomal RNA. Prog. Nucleic Acid. Res. Mol. Biol. 39, 241–303.10.1016/S0079-6603(08)60629-7Search in Google Scholar

Manza, L. L, Codreanu, S.G., Stamer, S.L., Smith, D.L., Wells, K.S., Roberts, R.L., and Liebler, D.C. (2004). Global shifts in protein sumoylation in response to electrophile and oxidative stress. Chem. Res. Toxicol. 17, 1706–1715.10.1021/tx049767lSearch in Google Scholar PubMed

Mason, P.J. and Bessler, M. (2011). The genetics of dyskeratosis congenita. Cancer Genet. 204, 635–645.10.1016/j.cancergen.2011.11.002Search in Google Scholar PubMed PubMed Central

McDonald, S.L., Edington, H.D., Kirkwood, J.M., and Becker, D. (2004). Expression analysis of genes identified by molecular profiling of VGP melanomas and MGP melanoma-positive lymph nodes. Cancer. Biol. Ther. 3, 110–120.10.4161/cbt.3.1.662Search in Google Scholar PubMed

Meier, U.T. and Blobel, G. (1994). NAP57, a mammalian nucleolar protein with a putative homolog in yeast and bacteria. J. Cell Biol. 127, 1505–1514.10.1083/jcb.127.6.1505Search in Google Scholar PubMed PubMed Central

Mitchell, J.R., Wood, E., and Collins, K. (1999). A telomerase component is defective in the human disease dyskeratosis congenital. Nature 402, 551–555.10.1038/990141Search in Google Scholar PubMed

Mochizuki, Y., He, J., Kulkarni, S., Bessler, M., and Mason, P.J. (2004). Mouse dyskerin mutations affect accumulation of telomerase RNA and small nucleolar RNA, telomerase activity, and ribosomal RNA processing. Proc. Natl. Acad. Sci. USA 101, 10756–10761.10.1073/pnas.0402560101Search in Google Scholar PubMed PubMed Central

Montanaro, L., Brigotti, M., Clohess, J., Barbieri, S., Ceccarelli, C., Santini, D., Taffurelli, M., Calienni, M., Teruya-Feldstein, J., Trerè, D., et al. (2006). Dyskerin expression influences the level of ribosomal RNA pseudo-uridylation and telomerase RNA component in human breast cancer. J. Pathol. 210, 10–18.10.1002/path.2023Search in Google Scholar PubMed

Montanaro, L., Calienni, M., Ceccarelli, C., Santini, D., Taffurelli, M., Pileri, S., Treré, D., and Derenzini, M. (2008). Relationship between dyskerin expression and telomerase activity in human breast cancer. Cell Oncol. 30, 483–490.10.1155/2008/830562Search in Google Scholar

Montanaro, L., Calienni, M., Bertoni, S., Rocchi, L., Sansone, P., Storci, G., Santini, D., Ceccarelli, C., Taffurelli, M., Carnicelli, D., et al. (2010). Novel dyskerin mediated mechanism of p53 inactivation through defective mRNA translation. Cancer Res. 70, 4767–4777.10.1158/0008-5472.CAN-09-4024Search in Google Scholar PubMed

Nallar, S.C., Lin, L., Srivastava,V., Gade, P., Hofmann, E.R., Ahmed, H., Reddy, S.P., and Kalvakolanu, D.V. (2011). GRIM-1, a novel growth suppressor, inhibits rRNA maturation by suppressing small nucleolar RNAs. PLoS One 6, e24082.10.1371/journal.pone.0024082Search in Google Scholar PubMed PubMed Central

Parry, E.M., Alder, J.K., Lee, S.S., Phillips J.A.3rd, Loyd, J.E., Duggal, P., and Armanios, M. (2011). Decreased dyskerin levels as a mechanism of telomere shortening in X-linked dyskeratosis congenita. J. Med. Genet. 48, 327–333.10.1136/jmg.2010.085100Search in Google Scholar PubMed PubMed Central

Phillips, B., Billin, A.N., Cadwell, C., Buchholz, R., Erickson, C., Merriam, J.R., Carbon, J., and Poole, S.J. (1998). The Nop60B gene of Drosophila encodes an essential nucleolar protein that functions in yeast. Mol. Gen. Genet. 260, 20–29.10.1007/s004380050866Search in Google Scholar PubMed

Piva, R., Pellegrino, E., Mattioli, M., Agnelli, L., Lombardi, L., Boccalatte, F., Costa, G., Ruggeri, B.A., Cheng, M., Chiarle, R., et al. (2006). Functional validation of the anaplastic lymphoma kinase signature identifies CEBPB and BCL2A1 as critical target genes. J. Clin. Invest. 116, 3171–3182.10.1172/JCI29401Search in Google Scholar PubMed PubMed Central

Rashid, R, Liang, B., Baker, D.L., Youssef, O.A., He, Y., Phipps, K., Terns, R.M., Terns, M.P., and Li, H. (2006). Crystal structure of a Cbf5-Nop10-Gar1 complex and implications in RNA-guided pseudouridylation and dyskeratosis congenita. Mol. Cell 21, 249–260.10.1016/j.molcel.2005.11.017Search in Google Scholar PubMed

Riccardo, S., Tortoriello, G., Giordano, E., Turano, M., and Furia, M. (2007). The coding/non-coding overlapping architecture of the gene encoding the Drosophila pseudouridine synthase. BMC Mol. Biol. 8, 1–17.10.1186/1471-2199-8-15Search in Google Scholar PubMed PubMed Central

Richard, P., Darzacq, X., Bertrand, E., Jády, B.E., Verheggen, C., and Kiss, T (2003). A common sequence motif determines the Cajal body-specific localization of box H/ACA scaRNAs. Embo. J. 22, 4283–4293.10.1093/emboj/cdg394Search in Google Scholar PubMed PubMed Central

Richard, P., Kiss, A.M., Darzacq, X., and Kiss, T. (2006). Cotranscriptional recognition of human intronic box H/ACA snoRNAs occurs in a splicing-independent manner. Mol. Cell Biol. 26, 2540–2549.10.1128/MCB.26.7.2540-2549.2006Search in Google Scholar

Rocchi, L., Pacilli, A., Sethi, R., Penzo, M., Schneider, R.J., Treré, D., Bigotti, M., and Montanaro, L. (2013). Dyskerin depletion increases VEGF mRNA internal ribosome entry site-mediated translation. Nucleic Acids Res. 41, 8308–8318.10.1093/nar/gkt587Search in Google Scholar

Ruggero, D., Grisendi, S., Piazza, F., Rego, E., Mari, F., Rao, P.H., Cordon-Cardo, C., and Pandolci, P.P. (2003). Dyskeratosis congenita and cancer in mice deficient in ribosomal RNA modification. Science 299, 259–262.10.1126/science.1079447Search in Google Scholar

Sali, A. and Blundell, T.L. (1993). Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779–815.10.1006/jmbi.1993.1626Search in Google Scholar

Salowsky, R., Heiss, N.S., Benner, A., Wittig, R., and Poustka, A. (2002). Basal transcription activity of the dyskeratosis congenita gene is mediated by Sp1 and Sp3 and a patient mutation in a Sp1 binding site is associated with decreased promoter activity. Gene 293, 9–19.10.1016/S0378-1119(02)00725-4Search in Google Scholar

Saraiya, A.A. and Wang, C.C. (2008). snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog. 4, e1000224.10.1371/journal.ppat.1000224Search in Google Scholar PubMed PubMed Central

Sauer, G., Korner, R., Hanisch, A., Ries, A., Nigg, E.A. and Sillje, H.H. (2005). Proteome analysis of the human mitotic spindle. Mol. Cell. Proteomics 4, 35–43.10.1074/mcp.M400158-MCP200Search in Google Scholar PubMed

Savage, S.A. and Bertuch, A.A. (2010). The genetics and clinical manifestations of telomere biology disorders. Genet. Med. 12, 753–764.10.1097/GIM.0b013e3181f415b5Search in Google Scholar PubMed PubMed Central

Schaner, M.E., Ross, D.T., Ciaravino, G., Soglie, T., Troyanskaya, O., Diehn, M., Wang Y.C., Duran, G.E., Sikic, T.L., Caldeira, S., et al. (2003). Gene expression patterns in ovarian carcinomas. Mol. Biol. Cell 14, 4376–4386.10.1091/mbc.e03-05-0279Search in Google Scholar PubMed PubMed Central

Sieron, P., Hader, C., Hatina, J., Engers, R., Wlazlinski, A., Müller, M., and Schulz, W.A. (2009). DKC1 overexpression associated with prostate cancer progression. Br. J. Cancer 101, 1410–1416.10.1038/sj.bjc.6605299Search in Google Scholar PubMed PubMed Central

Taft, R.J., Glazov, E.A., Lassmann, T., Hayashizaki, Y., Carninci, P., and Mattick, J.S. (2009). Small RNAs derived from snoRNAs. RNA 15, 1233–1240.10.1261/rna.1528909Search in Google Scholar PubMed PubMed Central

Taulli, R. and Pandolfi, P.P. (2012). ‘Snorkeling’ for missing players in cancer. J. Clin. Invest. 122, 2765–2768.10.1172/JCI63549Search in Google Scholar PubMed PubMed Central

Tortoriello, G., de Celis, J.F., and Furia, M. (2010). Linking pseudouridine synthases to growth, development and cell competition. FEBS J. 277, 3249–3263.10.1111/j.1742-4658.2010.07731.xSearch in Google Scholar PubMed

Turano, M., Angrisani, A., De Rosa, M., Izzo, P., and Furia, M. (2008). Real-time PCR quantification of human DKC1 expression in colorectal cancer. Acta Oncol. 47, 1598–1599.10.1080/02841860801898616Search in Google Scholar PubMed

Turano, M., Angrisani, A., Di Maio, N., and Furia, M. (2013). Intron retention: a human DKC1 gene common splicing event. Biochem. Cell Biol. 91, 506–512.10.1139/bcb-2013-0047Search in Google Scholar PubMed

Uhlen, M., Oksvold, P., Fagerberg, L., Lundberg, E., Jonasson, K., Forsberg, M., Zwahlen, M., Kampf, C., Wester, K., Hober, S., et al. (2010). Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 28, 1248–1250.10.1038/nbt1210-1248Search in Google Scholar PubMed

von Stedingk, K., Koster, J., Piqueras, M., Noguera, R., Navarro, S., Påhlman, S., Versteeg, R., Ora, I., Gisselsson, D., Lindgren, D., et al. (2013). snoRNPs regulate telomerase activity in neuroblastoma and are associated with poor prognosis. Transl. Oncol. 6, 447–457.10.1593/tlo.13112Search in Google Scholar PubMed PubMed Central

Vulliamy,T.J., Knight, S.W., Heiss, N.S., Smith, O.P., Poustka, A., Dokal, I., and Mason, P.J. (1999). Dyskeratosis congenita caused by a 3’ deletion: germline and somatic mosaicism in a female carrier. Blood 94, 1254–1260.10.1182/blood.V94.4.1254Search in Google Scholar

Walbott, H., Machado-Pinilla, R., Liger, D., Blaud, M., Réty, S., Grozdanov, P.N., Godin, K., van Tilbeurgh, H., Varani, G., Meier, U.T., et al. (2011). The H/ACA RNP assembly factor SHQ1 functions as an RNA mimic. Genes Dev. 25, 2398–2408.10.1101/gad.176834.111Search in Google Scholar PubMed PubMed Central

Watanabe, Y. and Gray, M.W. (2000). Evolutionary appearance of genes encoding proteins associated with box H/ACA snoRNAs: cbf5p in Euglena gracilis, an early diverging eukaryote, and candidate Gar1p and Nop10p homologs in archaebacteria. Nucleic Acids Res. 28, 2342–2352.10.1093/nar/28.12.2342Search in Google Scholar PubMed PubMed Central

Westermann, F., Henrich, K.O., Wei, J.S., Lutz, W., Fischer, M., König, R., Wiedemeyer, R., Ehemann, V., Brors, B., Ernestus, K., et al. (2007). High Skp2 expression characterizes high-risk neuroblastomas independent of MYCN status. Clin. Cancer Res. 13, 4695–4703.10.1158/1078-0432.CCR-06-2818Search in Google Scholar PubMed

Westman, B.J., Verheggen, C., Hutten, S., Lam, Y.W., Bertrand, E., and Lamond, A.I. (2010). A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol. Cell 39, 618–631.10.1016/j.molcel.2010.07.025Search in Google Scholar PubMed PubMed Central

Witkowska, A., Gumprecht, J., Glogowska-Ligus, J., Wystrychowski, G., Owczarek, A., Stachowicz, M., Bocianowska, A., Nowakowska-Zajdel, E., and Mazurek, U. (2010). Expression profile of significant immortalization genes in colon cancer. Int. J. Mol. Med. 25, 321–329.10.3892/ijmm_00000348Search in Google Scholar PubMed

Wong, J.M., Kyasa, M.J., Hutchins, L., and Collins, K. (2004). Telomerase RNA deficiency in peripheral blood mononuclear cells in X-linked dyskeratosis congenita. Hum. Genet. 115, 448–455.10.1007/s00439-004-1178-7Search in Google Scholar PubMed

Wu, G., Yu, A.T., Kantartzis, A., and Yu, Y.T. (2011). Functions and mechanisms of spliceosomal small nuclear RNA pseudouridylation. Wiley Interdiscip. Rev. RNA 2, 571–581.10.1002/wrna.77Search in Google Scholar PubMed PubMed Central

Yaghmai, R., Kimyai-Asadi, A., Rostamiani, K., Heiss, N.S., Poustka, A., Eyaid, W., Bodurtha, J., Nousari, H.C., Hamosh, A., and Metzenberg, A. (2000). Overlap of dyskeratosis congenita with the Hoyeraal-Hreidarsson syndrome. J. Pediatr. 136, 390–393.10.1067/mpd.2000.104295Search in Google Scholar PubMed

Yang, Y., Isaac, C., Wang, C., Dragon, F., Pogacic, V., and Meier, U.T. (2000). Conserved composition of mammalian box H/ACA and box C/D small nucleolar ribonucleoprotein particles and their interaction with the common factor Nopp140. Mol. Biol. Cell. 11, 567–577.10.1091/mbc.11.2.567Search in Google Scholar PubMed PubMed Central

Yang, P.K., Rotondo, G., Porras, T., Legrain, P., and Chanfreau, G. (2002). The Shq1pdNaf1p complex is required for box H/ACA small nucleolar ribonucleoprotein particle biogenesis. J. Biol. Chem. 277, 45235–45242.10.1074/jbc.M207669200Search in Google Scholar PubMed

Yang, P.K., Hoareau, C., Froment, C., Monsarrat, B., Henry, Y., and Chanfreau, G. (2005). Cotranscriptional recruitment of the pseudouridylsynthetase Cbf5p and of the RNA binding protein Naf1p during H/ACA snoRNP assembly. Mol. Cell. Biol. 25, 3295–3304.10.1128/MCB.25.8.3295-3304.2005Search in Google Scholar PubMed PubMed Central

Yoon, A., Peng, G., Brandenburger, Y., Zollo, O., Xu, W., Rego, E., and Ruggero, D. (2006). Impaired control of IRES-mediated translation in X-linked dyskeratosis congenital. Science 312, 902–906.10.1126/science.1123835Search in Google Scholar PubMed

Yu, A.T., Ge, J., and Yu, Y.T. (2011). Pseudouridines in spliceosomal snRNAs. Protein Cell 2, 712–725.10.1007/s13238-011-1087-1Search in Google Scholar PubMed PubMed Central

Zebarjadian, Y., King, T., Fournier, M.J., Clarke, L., and Carbon, J. (1999). Point mutations in yeast CBF5 can abolish in vivo pseudouridylation of rRNA. Mol. Cell Biol. 19, 7461–7472.10.1128/MCB.19.11.7461Search in Google Scholar PubMed PubMed Central

Zeng, X.L., Thumati, N.R., Fleisig, H.B., Hukezalie K.R., Savage, S.A., Giri, N., Alter, B.P., and Wong, J.M. (2012). The accumulation and not the specific activity of telomerase ribonucleoprotein determines telomere maintenance deficiency in X-linked dyskeratosis congenita. Hum. Mol. Genet. 21, 721–729.10.1093/hmg/ddr504Search in Google Scholar PubMed PubMed Central

Zhang, Y., Morimoto, K., Danilova, N., Zhang, B., and Lin, S. (2012). Zebrafish models for dyskeratosis congenita reveal critical roles of p53 activation contributing to hematopoietic defects through RNA processing. PLoS One 7, e30188.10.1371/journal.pone.0030188Search in Google Scholar PubMed PubMed Central

Received: 2013-11-29
Accepted: 2014-1-24
Published Online: 2014-1-27
Published in Print: 2014-6-1

©2014 by Walter de Gruyter Berlin/Boston

Downloaded on 22.2.2024 from https://www.degruyter.com/document/doi/10.1515/hsz-2013-0287/html
Scroll to top button