Human regulator of telomere elongation helicase 1 (RTEL1) is required for the nuclear and cytoplasmic trafficking of pre-U2 RNA

Nucleic Acids Research

Volumn 43, Issue 3, 2015, Pages 1834-1847

  Schertzer, Michael ^a,b,c   Jouravleva, Karina ^a,b,c   Perderiset, Mylene ^a,b,c   Dingli, Florent ^a   Loew, Damarys ^a   Le Guen, Tangui ^d,e   Bardoni, Barbara ^f,g   De Villartay, Jean Pierre ^d,e   Revy, Patrick ^d,e   Londoño Vallejo, Arturo ^a,b,c  

^a INSTITUT CURIE   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d INSERM   (France)

^e Laboratoire d'Excellence GR Ex   (France)

^f INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^g UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; HELICASE; REGULATOR OF TELOMERE ELONGATION HELICASE 1; RIBONUCLEOTIDE; SMALL INTERFERING RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; DNA HELICASE; PRIMER DNA; RNA PRECURSOR; RTEL1 PROTEIN, HUMAN; SMALL NUCLEAR RNA; U2 SMALL NUCLEAR RNA;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; DYSKERATOSIS CONGENITA; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC TRANSFECTION; HELA CELL LINE; HOYERAAL HREIDARSSON SYNDROME; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR CLONING; NORTHERN BLOTTING; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ANALYSIS; WESTERN BLOTTING; WILD TYPE; CELL NUCLEUS; GENETICS; HEK293 CELL LINE; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; TRANSPORT AT THE CELLULAR LEVEL;

MUS MUSCULUS;

BASE SEQUENCE; BIOLOGICAL TRANSPORT; BLOTTING, NORTHERN; CELL NUCLEUS; CHROMATOGRAPHY, LIQUID; CYTOPLASM; DNA HELICASES; DNA PRIMERS; HEK293 CELLS; HELA CELLS; HUMANS; POLYMERASE CHAIN REACTION; RNA PRECURSORS; RNA, SMALL INTERFERING; RNA, SMALL NUCLEAR; TANDEM MASS SPECTROMETRY;

EID: 84936064211     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1402     Document Type: Article

References (41)

1. Ding,H., Schertzer,M., Wu,X., Gertsenstein,M., Selig,S., Kammori,M., Pourvali,R., Poon,S., Vulto,I., Chavez,E. et al. (2004) Regulation of murine telomere length by Rtel: an essential gene encoding a helicase-like protein. Cell, 117, 873-886.
2. Vannier,J.B., Pavicic-Kaltenbrunner,V., Petalcorin,M.I., Ding,H. and Boulton,S.J. (2012) RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell, 149, 795-806.
3. Vannier,J.B., Sandhu,S., Petalcorin,M.I., Wu,X., Nabi,Z., Ding,H. and Boulton,S.J. (2013) RTEL1 is a replisome-associated helicase that promotes telomere and genome-wide replication. Science, 342, 239-242.
4. Uringa,E.J., Lisaingo,K., Pickett,H.A., Brind'Amour,J., Rohde,J.H., Zelensky,A., Essers,J. and Lansdorp,P.M. (2012) RTEL1 contributes to DNA replication and repair and telomere maintenance. Mol. Biol. Cell, 23, 2782-2792.
5. Youds,J.L., Mets,D.G., McIlwraith,M.J., Martin,J.S., Ward,J.D., ONeil,N.J., Rose,A.M., West,S.C., Meyer,B.J. and Boulton,S.J. (2010) RTEL-1 enforces meiotic crossover interference and homeostasis. Science, 327, 1254-1258.
6. Barber,L.J., Youds,J.L., Ward,J.D., McIlwraith,M.J., O'Neil,N.J., Petalcorin,M.I., Martin,J.S., Collis,S.J., Cantor,S.B., Auclair,M. et al. (2008) RTEL1 maintains genomic stability by suppressing homologous recombination. Cell, 135, 261-271.
7. Ballew,B.J., Yeager,M., Jacobs,K., Giri,N., Boland,J., Burdett,L., Alter,B.P. and Savage,S.A. (2013) Germline mutations of regulator of telomere elongation helicase 1, RTEL1, in Dyskeratosis congenita. Hum. Genet., 132, 473-480.
8. Ballew,B.J., Joseph,V., De,S., Sarek,G., Vannier,J.B., Stracker,T., Schrader,K.A., Small,T.N., O'Reilly,R., Manschreck,C. et al. (2013) A recessive founder mutation in regulator of telomere elongation helicase 1, RTEL1, underlies severe immunodeficiency and features of Hoyeraal Hreidarsson syndrome. PLoS Genet., 9, e1003695.
9. Deng,Z., Glousker,G., Molczan,A., Fox,A.J., Lamm,N., Dheekollu,J., Weizman,O.E., Schertzer,M., Wang,Z., Vladimirova,O. et al. (2013) Inherited mutations in the helicase RTEL1 cause telomere dysfunction and Hoyeraal-Hreidarsson syndrome. Proc. Natl. Acad. Sci. U.S.A., 110, E3408-E3416.
10. Le Guen,T., Jullien,L., Touzot,F., Schertzer,M., Gaillard,L., Perderiset,M., Carpentier,W., Nitschke,P., Picard,C., Couillault,G. et al. (2013) Human RTEL1 deficiency causes Hoyeraal-Hreidarsson syndrome with short telomeres and genome instability. Hum. Mol. Genet. 22, 3239-3249.
11. Walne,A.J., Vulliamy,T., Kirwan,M., Plagnol,V. and Dokal,I. (2013) Constitutional mutations in RTEL1 cause severe dyskeratosis congenita. Am. J. Hum. Genet., 92, 448-453.
12. Nagai,K., Muto,Y., Pomeranz Krummel,D.A., Kambach,C., Ignjatovic,T., Walke,S. and Kuglstatter,A. (2001) Structure and assembly of the spliceosomal snRNPs. Novartis Medal Lecture. Biochem. Soc. Trans., 29, 15-26.
13. Chandrasekharappa,S.C., Smith,J.H. and Eliceiri,G.L. (1983) Biosynthesis of small nuclear RNAs in human cells. J. Cell. Physiol., 117, 169-174.
14. Izaurralde,E., Lewis,J., Gamberi,C., Jarmolowski,A., McGuigan,C. and Mattaj,I.W. (1995) A cap-binding protein complex mediating U snRNA export. Nature, 376, 709-712.
15. Ohno,M., Segref,A., Bachi,A., Wilm,M. and Mattaj,I.W. (2000) PHAX, a mediator of U snRNA nuclear export whose activity is regulated by phosphorylation. Cell, 101, 187-198.
16. Yong,J., Kasim,M., Bachorik,J.L., Wan,L. and Dreyfuss,G. (2010) Gemin5 delivers snRNA precursors to the SMN complex for snRNP biogenesis. Mol. Cell, 38, 551-562.
17. Battle,D.J., Kasim,M., Yong,J., Lotti,F., Lau,C.K., Mouaikel,J., Zhang,Z., Han,K., Wan,L. and Dreyfuss,G. (2006) The SMN complex: an assembly machine for RNPs. Cold Spring Harb. Symp. Quant. Biol., 71, 313-320.
18. Kiss,T. (2004) Biogenesis of small nuclear RNPs. J. Cell. Sci., 117, 5949-5951.
19. Buck,D., Malivert,L., de Chasseval,R., Barraud,A., Fondaneche,M.C., Sanal,O., Plebani,A., Stephan,J.L., Hufnagel,M., le Deist,F. et al. (2006) Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell, 124, 287-299.
20. Poullet,P., Carpentier,S. and Barillot,E. (2007) myProMS, a web server for management and validation of mass spectrometry-based proteomic data. Proteomics, 7, 2553-2556.
21. Smith,K.P. and Lawrence,J.B. (2000) Interactions of U2 gene loci and their nuclear transcripts with Cajal (coiled) bodies: evidence for PreU2 within Cajal bodies. Mol. Biol. Cell, 11, 2987-2998.
22. Keene,J.D., Komisarow,J.M. and Friedersdorf,M.B. (2006) RIP-Chip: the isolation and identification of mRNAs, microRNAs and protein components of ribonucleoprotein complexes from cell extracts. Nat. Protoc., 1, 302-307.
23. Bensaid,M., Melko,M., Bechara,E.G., Davidovic,L., Berretta,A., Catania,M.V., Gecz,J., Lalli,E. and Bardoni,B. (2009) FRAXE-associated mental retardation protein (FMR2) is an RNA-binding protein with high affinity for G-quartet RNA forming structure. Nucleic Acids Res., 37, 1269-1279.
24. Andersen,J.S., Lyon,C.E., Fox,A.H., Leung,A.K., Lam,Y.W., Steen,H., Mann,M. and Lamond,A.I. (2002) Directed proteomic analysis of the human nucleolus. Curr. Biol., 12, 1-11.
25. Kudo,N., Matsumori,N., Taoka,H., Fujiwara,D., Schreiner,E.P., Wolff,B., Yoshida,M. and Horinouchi,S. (1999) Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. U.S.A., 96, 9112-9117.
26. Ishikawa,H., Nobe,Y., Izumikawa,K., Yoshikawa,H., Miyazawa,N., Terukina,G., Kurokawa,N., Taoka,M., Yamauchi,Y., Nakayama,H. et al. (2014) Identification of truncated forms of U1 snRNA reveals a novel RNA degradation pathway during snRNP biogenesis. Nucleic Acids Res., 42, 2708-2724.
27. Ossareh-Nazari,B., Maison,C., Black,B.E., Levesque,L., Paschal,B.M. and Dargemont,C. (2000) RanGTP-binding protein NXT1 facilitates nuclear export of different classes of RNA in vitro. Mol. Cell. Biol., 20, 4562-4571.
28. Kohler,A. and Hurt,E. (2007) Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell. Biol., 8, 761-773.
29. Massenet,S. and Branlant,C. (1999) A limited number of pseudouridine residues in the human atac spliceosomal UsnRNAs as compared to human major spliceosomal UsnRNAs. RNA, 5, 1495-1503.
30. Tarn,W.Y., Yario,T.A. and Steitz,J.A. (1995) U12 snRNA in vertebrates: evolutionary conservation of 5′ sequences implicated in splicing of pre-mRNAs containing a minor class of introns. RNA, 1, 644-656.
31. Visa,N., Izaurralde,E., Ferreira,J., Daneholt,B. and Mattaj,I.W. (1996) A nuclear cap-binding complex binds Balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export. J. Cell Biol., 133, 5-14.
32. Broome,H.J. and Hebert,M.D. (2012) In vitro RNase and nucleic acid binding activities implicate coilin in U snRNA processing. PLoS One, 7, e36300.
33. Bradrick,S.S. and Gromeier,M. (2009) Identification of gemin5 as a novel 7-methylguanosine cap-binding protein. PLoS One, 4, e7030.
34. Massenet,S., Pellizzoni,L., Paushkin,S., Mattaj,I.W. and Dreyfuss,G. (2002) The SMN complex is associated with snRNPs throughout their cytoplasmic assembly pathway. Mol. Cell. Biol., 22, 6533-6541.
35. Faure,G., Revy,P., Schertzer,M., Londono-Vallejo,A. and Callebaut,I. (2013) The C-terminal extension of human RTEL1, mutated in Hoyeraal-Hreidarsson syndrome, contains Harmonin-N-like domains. Proteins, 29, 1138-1144.
36. Ohno,M. (2012) Size matters in RNA export. RNA Biol., 9, 1413-1417.
37. Buchwald,G., van der Stoop,P., Weichenrieder,O., Perrakis,A., van Lohuizen,M. and Sixma,T.K. (2006) Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J., 25, 2465-2474.
38. Mitra,S.A., Mitra,A.P. and Triche,T.J. (2012) A central role for long non-coding RNA in cancer. Front. Genet., 3, 17.
39. Qureshi,I.A. and Mehler,M.F. (2011) Non-coding RNA networks underlying cognitive disorders across the lifespan. Trends Mol. Med., 17, 337-346.
40. Blasco,M.A., Lee,H.W., Hande,M.P., Samper,E., Lansdorp,P.M., DePinho,R.A. and Greider,C.W. (1997) Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell, 91, 25-34.
41. Oka,M., Asally,M., Yasuda,Y., Ogawa,Y., Tachibana,T. and Yoneda,Y. (2010) The mobile FG nucleoporin Nup98 is a cofactor for Crm1-dependent protein export. Mol. Biol. Cell, 21, 1885-1896.