Artículo

Muñoz, M.J.; Nieto Moreno, N.; Giono, L.E.; Cambindo Botto, A.E.; Dujardin, G.; Bastianello, G.; Lavore, S.; Torres-Méndez, A.; Menck, C.F.M.; Blencowe, B.J.; Irimia, M.; Foiani, M.; Kornblihtt, A.R. "Major Roles for Pyrimidine Dimers, Nucleotide Excision Repair, and ATR in the Alternative Splicing Response to UV Irradiation" (2017) Cell Reports. 18(12):2868-2879
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

We have previously found that UV irradiation promotes RNA polymerase II (RNAPII) hyperphosphorylation and subsequent changes in alternative splicing (AS). We show now that UV-induced DNA damage is not only necessary but sufficient to trigger the AS response and that photolyase-mediated removal of the most abundant class of pyrimidine dimers (PDs) abrogates the global response to UV. We demonstrate that, in keratinocytes, RNAPII is the target, but not a sensor, of the signaling cascade initiated by PDs. The UV effect is enhanced by inhibition of gap-filling DNA synthesis, the last step in the nucleotide excision repair pathway (NER), and reduced by the absence of XPE, the main NER sensor of PDs. The mechanism involves activation of the protein kinase ATR that mediates the UV-induced RNAPII hyperphosphorylation. Our results define the sequence UV-PDs-NER-ATR-RNAPII-AS as a pathway linking DNA damage repair to the control of both RNAPII phosphorylation and AS regulation. © 2017 The Author(s)

Registro:

Documento: Artículo
Título:Major Roles for Pyrimidine Dimers, Nucleotide Excision Repair, and ATR in the Alternative Splicing Response to UV Irradiation
Autor:Muñoz, M.J.; Nieto Moreno, N.; Giono, L.E.; Cambindo Botto, A.E.; Dujardin, G.; Bastianello, G.; Lavore, S.; Torres-Méndez, A.; Menck, C.F.M.; Blencowe, B.J.; Irimia, M.; Foiani, M.; Kornblihtt, A.R.
Filiación:Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE-UBA-CONICET) and Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Argentina
Fondazione Istituto FIRC di Oncologia Molecolare (IFOM), Via Adamello 16, Milan, 20139, Italy
Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), Dr. Aiguader 88, Barcelona, 08003, Spain
Universitat Pompeu Fabra (UPF), Barcelona, 08003, Spain
Departamento de Microbiologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, 05508-900, Brazil
Donnelly Centre and Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 3E1, Canada
Palabras clave:alternative splicing; ATR; cyclobutane pyrimidine dimers; DNA damage; global genome repair; nucleotide excision repair; Potorous photolyase; UV irradiation; ATR protein; cyclobutane; deoxyribodipyrimidine photolyase; pyrimidine dimer; RNA polymerase II; ATM protein; ATR protein, human; DNA; pyrimidine dimer; RNA polymerase II; alternative RNA splicing; Article; controlled study; DNA damage; DNA repair; DNA synthesis; enzyme phosphorylation; excision repair; gene expression; human; human cell; inhibition kinetics; keratinocyte; signal transduction; transcription initiation; ultraviolet irradiation; alternative RNA splicing; cytology; DNA repair; genetic transcription; genetics; metabolism; phosphorylation; radiation response; skin; ultraviolet radiation; Alternative Splicing; Ataxia Telangiectasia Mutated Proteins; DNA; DNA Repair; Humans; Keratinocytes; Phosphorylation; Pyrimidine Dimers; RNA Polymerase II; Skin; Transcription, Genetic; Ultraviolet Rays
Año:2017
Volumen:18
Número:12
Página de inicio:2868
Página de fin:2879
DOI: http://dx.doi.org/10.1016/j.celrep.2017.02.066
Título revista:Cell Reports
Título revista abreviado:Cell Rep.
ISSN:22111247
CAS:cyclobutane, 287-23-0; deoxyribodipyrimidine photolyase, 37290-70-3; pyrimidine dimer, 25247-63-6; DNA, 9007-49-2; Ataxia Telangiectasia Mutated Proteins; ATR protein, human; DNA; Pyrimidine Dimers; RNA Polymerase II
Registro:http://digital.bl.fcen.uba.ar/collection/paper/document/paper_22111247_v18_n12_p2868_Munoz

Referencias:

  • Anindya, R., Mari, P.-O., Kristensen, U., Kool, H., Giglia-Mari, G., Mullenders, L.H., Fousteri, M., Svejstrup, J.Q., A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair (2010) Mol. Cell, 38, pp. 637-648
  • Barash, Y., Calarco, J.A., Gao, W., Pan, Q., Wang, X., Shai, O., Blencowe, B.J., Frey, B.J., Deciphering the splicing code (2010) Nature, 465, pp. 53-59
  • Bartkowiak, B., Liu, P., Phatnani, H.P., Fuda, N.J., Cooper, J.J., Price, D.H., Adelman, K., Greenleaf, A.L., CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1 (2010) Genes Dev., 24, pp. 2303-2316
  • Bernard, J.J., Cowing-Zitron, C., Nakatsuji, T., Muehleisen, B., Muto, J., Borkowski, A.W., Martinez, L., Gallo, R.L., Ultraviolet radiation damages self noncoding RNA and is detected by TLR3 (2012) Nat. Med., 18, pp. 1286-1290
  • Besaratinia, A., Yoon, J.-I., Schroeder, C., Bradforth, S.E., Cockburn, M., Pfeifer, G.P., Wavelength dependence of ultraviolet radiation-induced DNA damage as determined by laser irradiation suggests that cyclobutane pyrimidine dimers are the principal DNA lesions produced by terrestrial sunlight (2011) FASEB J., 25, pp. 3079-3091
  • Boros, G., Miko, E., Muramatsu, H., Weissman, D., Emri, E., van der Horst, G.T., Szegedi, A., Remenyik, É., Identification of cyclobutane pyrimidine dimer-responsive genes using UVB-irradiated human keratinocytes transfected with in vitro-synthesized photolyase mRNA (2015) PLoS ONE, 10, p. e0131141
  • D'Errico, M., Teson, M., Calcagnile, A., Nardo, T., De Luca, N., Lazzari, C., Soddu, S., Dogliotti, E., Differential role of transcription-coupled repair in UVB-induced response of human fibroblasts and keratinocytes (2005) Cancer Res., 65, pp. 432-438
  • D'Errico, M., Lemma, T., Calcagnile, A., Proietti De Santis, L., Dogliotti, E., Cell type and DNA damage specific response of human skin cells to environmental agents (2007) Mutat. Res., 614, pp. 37-47
  • de la Mata, M., Kornblihtt, A.R., RNA polymerase II C-terminal domain mediates regulation of alternative splicing by SRp20 (2006) Nat. Struct. Mol. Biol., 13, pp. 973-980
  • de la Mata, M., Alonso, C.R., Kadener, S., Fededa, J.P., Blaustein, M., Pelisch, F., Cramer, P., Kornblihtt, A.R., A slow RNA polymerase II affects alternative splicing in vivo (2003) Mol. Cell, 12, pp. 525-532
  • de Lima-Bessa, K.M., Armelini, M.G., Chiganças, V., Jacysyn, J.F., Amarante-Mendes, G.P., Sarasin, A., Menck, C.F., CPDs and 6-4PPs play different roles in UV-induced cell death in normal and NER-deficient human cells (2008) DNA Repair (Amst.), 7, pp. 303-312
  • Dujardin, G., Lafaille, C., de la Mata, M., Marasco, L.E., Muñoz, M.J., Le Jossic-Corcos, C., Corcos, L., Kornblihtt, A.R., How slow RNA polymerase II elongation favors alternative exon skipping (2014) Mol. Cell, 54, pp. 683-690
  • Ellis, J.D., Barrios-Rodiles, M., Colak, R., Irimia, M., Kim, T., Calarco, J.A., Wang, X., Kim, P.M., Tissue-specific alternative splicing remodels protein-protein interaction networks (2012) Mol. Cell, 46, pp. 884-892
  • Fong, N., Kim, H., Zhou, Y., Ji, X., Qiu, J., Saldi, T., Diener, K., Bentley, D.L., Pre-mRNA splicing is facilitated by an optimal RNA polymerase II elongation rate (2014) Genes Dev., 28, pp. 2663-2676
  • Garcin, G., Douki, T., Stoebner, P.E., Guesnet, J., Guezennec, A., Martinez, J., Cadet, J., Meunier, L., Cell surface expression of melanocortin-1 receptor on HaCaT keratinocytes and alpha-melanocortin stimulation do not affect the formation and repair of UVB-induced DNA photoproducts (2007) Photochem. Photobiol. Sci., 6, pp. 585-593
  • Gracheva, E.O., Cordero-Morales, J.F., González-Carcacía, J.A., Ingolia, N.T., Manno, C., Aranguren, C.I., Weissman, J.S., Julius, D., Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats (2011) Nature, 476, pp. 88-91
  • Hanasoge, S., Ljungman, M., H2AX phosphorylation after UV irradiation is triggered by DNA repair intermediates and is mediated by the ATR kinase (2007) Carcinogenesis, 28, pp. 2298-2304
  • Hua, Y., Sahashi, K., Rigo, F., Hung, G., Horev, G., Bennett, C.F., Krainer, A.R., Peripheral SMN restoration is essential for long-term rescue of a severe spinal muscular atrophy mouse model (2011) Nature, 478, pp. 123-126
  • Ip, J.Y., Schmidt, D., Pan, Q., Ramani, A.K., Fraser, A.G., Odom, D.T., Blencowe, B.J., Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation (2011) Genome Res., 21, pp. 390-401
  • Kemp, M.G., Sancar, A., ATR kinase inhibition protects non-cycling cells from the lethal effects of DNA damage and transcription stress (2016) J. Biol. Chem., 291, pp. 9330-9342
  • Kornblihtt, A.R., Schor, I.E., Alló, M., Dujardin, G., Petrillo, E., Muñoz, M.J., Alternative splicing: a pivotal step between eukaryotic transcription and translation (2013) Nat. Rev. Mol. Cell Biol., 14, pp. 153-165
  • Kulaksiz, G., Reardon, J.T., Sancar, A., Xeroderma pigmentosum complementation group E protein (XPE/DDB2): purification of various complexes of XPE and analyses of their damaged DNA binding and putative DNA repair properties (2005) Mol. Cell. Biol., 25, pp. 9784-9792
  • Marteijn, J.A., Bekker-Jensen, S., Mailand, N., Lans, H., Schwertman, P., Gourdin, A.M., Dantuma, N.P., Vermeulen, W., Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response (2009) J. Cell Biol., 186, pp. 835-847
  • Marteijn, J.A., Lans, H., Vermeulen, W., Hoeijmakers, J.H., Understanding nucleotide excision repair and its roles in cancer and ageing (2014) Nat. Rev. Mol. Cell Biol., 15, pp. 465-481
  • Matsumoto, M., Yaginuma, K., Igarashi, A., Imura, M., Hasegawa, M., Iwabuchi, K., Date, T., Yamashita, K., Perturbed gap-filling synthesis in nucleotide excision repair causes histone H2AX phosphorylation in human quiescent cells (2007) J. Cell Sci., 120, pp. 1104-1112
  • Matsuoka, S., Ballif, B.A., Smogorzewska, A., McDonald, E.R., 3rd, Hurov, K.E., Luo, J., Bakalarski, C.E., Lerenthal, Y., ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage (2007) Science, 316, pp. 1160-1166
  • Melnikova, V.O., Ananthaswamy, H.N., Cellular and molecular events leading to the development of skin cancer (2005) Mutat. Res., 571, pp. 91-106
  • Mouret, S., Charveron, M., Favier, A., Cadet, J., Douki, T., Differential repair of UVB-induced cyclobutane pyrimidine dimers in cultured human skin cells and whole human skin (2008) DNA Repair (Amst.), 7, pp. 704-712
  • Muñoz, M.J., Pérez Santangelo, M.S., Paronetto, M.P., de la Mata, M., Pelisch, F., Boireau, S., Glover-Cutter, K., Lozano, J.J., DNA damage regulates alternative splicing through inhibition of RNA polymerase II elongation (2009) Cell, 137, pp. 708-720
  • Muñoz, M.J., de la Mata, M., Kornblihtt, A.R., The carboxy terminal domain of RNA polymerase II and alternative splicing (2010) Trends Biochem. Sci., 35, pp. 497-504
  • Perdiz, D., Grof, P., Mezzina, M., Nikaido, O., Moustacchi, E., Sage, E., Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. Possible role of Dewar photoproducts in solar mutagenesis (2000) J. Biol. Chem., 275, pp. 26732-26742
  • Sancar, A., Lindsey-Boltz, L.A., Unsal-Kaçmaz, K., Linn, S., Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints (2004) Annu. Rev. Biochem., 73, pp. 39-85
  • Shell, S.M., Hawkins, E.K., Tsai, M.S., Hlaing, A.S., Rizzo, C.J., Chazin, W.J., Xeroderma pigmentosum complementation group C protein (XPC) serves as a general sensor of damaged DNA (2013) DNA Repair (Amst.), 12, pp. 947-953
  • Srebrow, A., Kornblihtt, A.R., The connection between splicing and cancer (2006) J. Cell Sci., 119, pp. 2635-2641
  • Stiff, T., Cerosaletti, K., Concannon, P., O'Driscoll, M., Jeggo, P.A., Replication independent ATR signalling leads to G2/M arrest requiring Nbs1, 53BP1 and MDC1 (2008) Hum. Mol. Genet., 17, pp. 3247-3253
  • Stiff, T., Walker, S.A., Cerosaletti, K., Goodarzi, A.A., Petermann, E., Concannon, P., O'Driscoll, M., Jeggo, P.A., ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling (2006) EMBO J., 25, pp. 5775-5782
  • Tresini, M., Warmerdam, D.O., Kolovos, P., Snijder, L., Vrouwe, M.G., Demmers, J.A., van IJcken, W.F., Hoeijmakers, J.H., The core spliceosome as target and effector of non-canonical ATM signalling (2015) Nature, 523, pp. 53-58
  • Vrouwe, M.G., Pines, A., Overmeer, R.M., Hanada, K., Mullenders, L.H., UV-induced photolesions elicit ATR-kinase-dependent signaling in non-cycling cells through nucleotide excision repair-dependent and -independent pathways (2011) J. Cell Sci., 124, pp. 435-446

Citas:

---------- APA ----------
Muñoz, M.J., Nieto Moreno, N., Giono, L.E., Cambindo Botto, A.E., Dujardin, G., Bastianello, G., Lavore, S.,..., Kornblihtt, A.R. (2017) . Major Roles for Pyrimidine Dimers, Nucleotide Excision Repair, and ATR in the Alternative Splicing Response to UV Irradiation. Cell Reports, 18(12), 2868-2879.
http://dx.doi.org/10.1016/j.celrep.2017.02.066
---------- CHICAGO ----------
Muñoz, M.J., Nieto Moreno, N., Giono, L.E., Cambindo Botto, A.E., Dujardin, G., Bastianello, G., et al. "Major Roles for Pyrimidine Dimers, Nucleotide Excision Repair, and ATR in the Alternative Splicing Response to UV Irradiation" . Cell Reports 18, no. 12 (2017) : 2868-2879.
http://dx.doi.org/10.1016/j.celrep.2017.02.066
---------- MLA ----------
Muñoz, M.J., Nieto Moreno, N., Giono, L.E., Cambindo Botto, A.E., Dujardin, G., Bastianello, G., et al. "Major Roles for Pyrimidine Dimers, Nucleotide Excision Repair, and ATR in the Alternative Splicing Response to UV Irradiation" . Cell Reports, vol. 18, no. 12, 2017, pp. 2868-2879.
http://dx.doi.org/10.1016/j.celrep.2017.02.066
---------- VANCOUVER ----------
Muñoz, M.J., Nieto Moreno, N., Giono, L.E., Cambindo Botto, A.E., Dujardin, G., Bastianello, G., et al. Major Roles for Pyrimidine Dimers, Nucleotide Excision Repair, and ATR in the Alternative Splicing Response to UV Irradiation. Cell Rep. 2017;18(12):2868-2879.
http://dx.doi.org/10.1016/j.celrep.2017.02.066