Accessible Unlicensed Requires Authentication Published by De Gruyter January 27, 2014

Human dyskerin: beyond telomeres

Alberto Angrisani, Rosario Vicidomini, Mimmo Turano and Maria Furia
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.

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Alter, B.P., Giri, N., Savage, S.A., and Rosenberg, P.S. (2009). Cancer in dyskeratosis congenita. Blood 113, 6549–6557. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Davis, D.R. (1995). Stabilization of RNA stacking by pseudouridine. Nucleic Acids Res. 23, 5020–5026. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Dokal, I. (2011). Dyskeratosis congenita. Hematology Am. Soc. Hematol. Educ. Program. 2011, 480–486. Search in Google Scholar

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. Search 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. Search in Google Scholar

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. Search in Google Scholar

Fatica, A., Dlakic, M., and Tollervey, D. (2002). Naf1p is a box H/ACA snoRNP assembly factor. RNA 8, 1502–1514. Search 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. Search in Google Scholar

Ge, J. and Yu, Y.T. (2013). RNA pseudouridylation: new insights into an old modification. Trends Biochem. Sci. 38, 210–218. Search in Google Scholar

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. Search in Google Scholar

Giordano, E., Peluso, I., Senger, S., and Furia M. (1999). Minifly, a Drosophila gene required for ribosome biogenesis. J. Cell. Biol. 144, 1123–1133. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Khanna, A. and Stamm, S. (2010). Regulation of alternative splicing by short non-coding nuclear RNAs. RNA Biol. 7, 480–485. Search in Google Scholar

Kirwan, M. and Dokal, I. (2008). Dyskeratosis congenita: a genetic disorder of many faces. Clin. Genet. 73, 103–112. Search 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. Search 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. Search 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. Search 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. Search 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. Search in Google Scholar

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. Search in Google Scholar

Li, L. and Ye, K. (2006). Crystal structure of an H/ACA box ribonucleoprotein particle. Nature 443, 302–307. Search in Google Scholar

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. Search in Google Scholar

Lin, X. and Momany, M. (2003). The Aspergillus nidulans swoC1 mutant shows defects in growth and development. Genetics 165, 543–554. Search in Google Scholar

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. Search in Google Scholar

Luzzatto, L. and Karadimitris, A. (1998). Dyskeratosis and ribosomal rebellion. Nat. Genet. 19, 6–7. Search 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. Search in Google Scholar

Maden, B.E. (1990). The numerous modified nucleotides in eukaryotic ribosomal RNA. Prog. Nucleic Acid. Res. Mol. Biol. 39, 241–303. Search 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. Search in Google Scholar

Mason, P.J. and Bessler, M. (2011). The genetics of dyskeratosis congenita. Cancer Genet. 204, 635–645. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Mitchell, J.R., Wood, E., and Collins, K. (1999). A telomerase component is defective in the human disease dyskeratosis congenital. Nature 402, 551–555. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search 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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search 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. Search 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. Search in Google Scholar

Sali, A. and Blundell, T.L. (1993). Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779–815. Search 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. Search in Google Scholar

Saraiya, A.A. and Wang, C.C. (2008). snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog. 4, e1000224. Search in Google Scholar

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. Search in Google Scholar

Savage, S.A. and Bertuch, A.A. (2010). The genetics and clinical manifestations of telomere biology disorders. Genet. Med. 12, 753–764. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Taulli, R. and Pandolfi, P.P. (2012). ‘Snorkeling’ for missing players in cancer. J. Clin. Invest. 122, 2765–2768. Search in Google Scholar

Tortoriello, G., de Celis, J.F., and Furia, M. (2010). Linking pseudouridine synthases to growth, development and cell competition. FEBS J. 277, 3249–3263. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search 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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Yu, A.T., Ge, J., and Yu, Y.T. (2011). Pseudouridines in spliceosomal snRNAs. Protein Cell 2, 712–725. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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