RNA splicing: A new player in the DNA damage response

International Journal of Cell Biology

Volumn , Issue , 2013, Pages

  Lenzken, Silvia C ^a   Loffreda, Alessia ^a   Barabino, Silvia M L ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; BRCA1 PROTEIN; BRCA2 PROTEIN; CAMPTOTHECIN; CARBOPLATIN; CHECKPOINT KINASE 2; CISPLATIN; MRE11 PROTEIN; PROTEIN MLH1; PROTEIN MSH2; SERINE ARGININE RICH PROTEIN; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

ACETYLATION; DEPHOSPHORYLATION; DNA ADDUCT; DNA DAMAGE; GENE EXPRESSION; GENE MUTATION; GENOMIC INSTABILITY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; RNA PROCESSING; RNA SPLICING; SUMOYLATION; UBIQUITINATION;

EID: 84885337449     PISSN: 16878876     EISSN: 16878884     Source Type: Journal    
DOI: 10.1155/2013/153634     Document Type: Review

References (138)

1. Ciccia A., Elledge S. J., The DNA damage response: making it safe to play with knives. Molecular Cell 2010 40 2 179 204 2-s2.0-78649336706 10.1016/j.molcel.2010.09.019
2. Longhese M. P., Bonetti D., Manfrini N., Clerici M., Mechanisms and regulation of DNA end resection. EMBO Journal 2010 29 17 2864 2874 2-s2.0-77956395354 10.1038/emboj.2010.165
3. Bouwman P., Jonkers J., The effects of deregulated DNA damage signalling on cancer chemotherapy response and resistance. Nature Reviews Cancer 2012 12 9 587 598
4. Lord C. J., Ashworth A., The DNA damage response and cancer therapy. Nature 2012 481 7381 287 294 2-s2.0-84856019858 10.1038/nature10760
5. Polo S. E., Jackson S. P., Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes and Development 2011 25 5 409 433 2-s2.0-79952235291 10.1101/gad.2021311
6. Rockx D. A. P., Mason R., Van Hoffen A., Barton M. C., Citterio E., Bregman D. B., Van Zeeland A. A., Vrieling H., Mullenders L. H. F., UV-induced inhibition of transcription involves repression of transcription initiation and phosphorylation of RNA polymerase II. Proceedings of the National Academy of Sciences of the United States of America 2000 97 19 10503 10508 2-s2.0-0034641753
7. Shanbhag N. M., Rafalska-Metcalf I. U., Balane-Bolivar C., Janicki S. M., Greenberg R. A., ATM-Dependent chromatin changes silence transcription in cis to dna double-strand breaks. Cell 2010 141 6 970 981 2-s2.0-77953720192 10.1016/j.cell.2010.04.038
8. Dutertre M., Sanchez G., Barbier J., Corcos L., Auboeuf D., The emerging role of pre-messenger RNA splicing in stress responses: sending alternative messages and silent messengers. RNA Biology 2011 8 5 2-s2.0-80052801997
9. Montecucco A., Biamonti G., Pre-mRNA processing factors meet the DNA damage response. Frontiers in Genetics 2013 4 102
10. Katzenberger R. J., Marengo M. S., Wassarman D. A., ATM and ATR pathways signal alternative splicing of Drosophila TAF1 pre-mRNA in response to DNA damage. Molecular and Cellular Biology 2006 26 24 9256 9267 2-s2.0-33845468254 10.1128/MCB.01125-06 (Pubitemid 44904421)
11. Katzenberger R. J., Marengo M. S., Wassarman D. A., Control of alternative splicing by signal-dependent degradation of splicing-regulatory proteins. Journal of Biological Chemistry 2009 284 16 10737 10746 2-s2.0-67449098155 10.1074/jbc.M809506200
12. Chandler D. S., Singh R. K., Caldwell L. C., Bitler J. L., Lozano G., Genotoxic stress induces coordinately regulated alternative splicing of the p53 modulators MDM2 and MDM4. Cancer Research 2006 66 19 9502 9508 2-s2.0-33750378188 10.1158/0008-5472.CAN-05-4271 (Pubitemid 44623648)
13. Kornblihtt A. R., De La Mata M., Fededa J. P., Muñoz M. J., Nogués G., Multiple links between transcription and splicing. RNA 2004 10 10 1489 1498 2-s2.0-4644334742 10.1261/rna.7100104 (Pubitemid 39288183)
14. Kornblihtt A. R., Coupling transcription and alternative splicing. Advances in Experimental Medicine and Biology 2007 623 175 189 2-s2.0-42449089029
15. Zhou Z., Fu X. D., Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 2013 122 3 191 207
16. Martinez-Contreras R., Cloutier P., Shkreta L., Fisette J., Revil T., Chabot B., hnRNP proteins and splicing control. Advances in Experimental Medicine and Biology 2007 623 123 147 2-s2.0-42449152457
17. Haley B., Paunesku T., Protic M., Woloschak G. E., Response of heterogeneous ribonuclear proteins (hnRNP) to ionising radiation and their involvement in DNA damage repair. International Journal of Radiation Biology 2009 85 8 643 655 2-s2.0-68649126316 10.1080/09553000903009548
18. Filippov V., Filippova M., Duerksen-Hughes P. J., The early response to DNA damage can lead to activation of alternative splicing activity resulting in CD44 splice pattern changes. Cancer Research 2007 67 16 7621 7630 2-s2.0-34548045983 10.1158/0008-5472.CAN-07-0145 (Pubitemid 47281354)
19. Merdzhanova G., Edmond V., De Seranno S., Van den Broeck A., Corcos L., Brambilla C., Brambilla E., Gazzeri S., Eymin B., E2F1 controls alternative splicing pattern of genes involved in apoptosis through upregulation of the splicing factor SC35. Cell Death and Differentiation 2008 15 12 1815 1823 2-s2.0-56349095800 10.1038/cdd.2008.135
20. Auclair Y., Richard S., The role of arginine methylation in the DNA damage response. DNA Repair 2013 12 7 459 465
21. Shi L., Oberdoerffer P., Chromatin dynamics in DNA double-strand break repair. Biochimica et Biophysica Acta 2012 1819 7 811 819 2-s2.0-84856446186 10.1016/j.bbagrm.2012.01.002
22. Vivarelli S., Lenzken S. C., Ruepp MD M. D., Paraquat modulates alternative pre-mRNA splicing by modifying the intracellular distribution of SRPK2. PLoS One 2013 8 4 e61980 10.1371/journal.pone.0061980
23. Edmond V., Moysan E., Khochbin S., Matthias P., Brambilla C., Brambilla E., Gazzeri S., Eymin B., Acetylation and phosphorylation of SRSF2 control cell fate decision in response to cisplatin. EMBO Journal 2011 30 3 510 523 2-s2.0-79551602983 10.1038/emboj.2010.333
24. Leva V., Giuliano S., Bardoni A., Camerini S., Crescenzi M., Lisa A., Biamonti G., Montecucco A., Phosphorylation of SRSF1 is modulated by replicational stress. Nucleic Acids Research 2012 40 3 1106 1117 2-s2.0-84856944343 10.1093/nar/gkr837
25. Mermoud J. E., Cohen P., Lamond A. I., Ser/Thr-specific protein phosphatases are required for both catalytic steps of pre-mRNA splicing. Nucleic Acids Research 1992 20 20 5263 5269 2-s2.0-0026731973
26. Murray M. V., Kobayashi R., Krainer A. R., The type 2C Ser/Thr phosphatase PP2C γ is a pre-mRNA splicing factor. Genes and Development 1999 13 1 87 97 2-s2.0-0032901297 (Pubitemid 29045118)
27. Allemand E., Hastings M. L., Murray M. V., Myers M. P., Krainer A. R., Alternative splicing regulation by interaction of phosphatase PP2Cgamma with nucleic acid-binding protein YB-1. Nature Structural & Molecular Biology 2007 14 7 630 638 (Pubitemid 47037064)
28. Beli P., Lukashchuk N., Wagner S. A., Weinert B. T., Olsen J. V., Baskcomb L., Mann M., Jackson S. P., Choudhary C., Proteomic investigations reveal a role for RNA processing factor THRAP3 in the DNA damage response. Molecular Cell 2012 46 2 212 225 2-s2.0-84860325854 10.1016/j.molcel.2012.01.026
29. Ikura T., Ogryzko V. V., Grigoriev M., Groisman R., Wang J., Horikoshi M., Scully R., Qin J., Nakatani Y., Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000 102 4 463 473 2-s2.0-0034682736
30. Sun Y., Jiang X., Price B. D., Tip60: connecting chromatin to DNA damage signaling. Cell Cycle 2010 9 5 930 936 2-s2.0-77953495958
31. Choudhary C., Kumar C., Gnad F., Nielsen M. L., Rehman M., Walther T. C., Olsen J. V., Mann M., Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009 325 5942 834 840 2-s2.0-68949212379 10.1126/science.1175371
32. Buchwald G., Van Der Stoop P., Weichenrieder O., Perrakis A., Van Lohuizen M., Sixma T. K., Structure and E3-ligase activity of the Ring-Ring complex of Polycomb proteins Bmi1 and Ring1b. EMBO Journal 2006 25 11 2465 2474 2-s2.0-33745753378 10.1038/sj.emboj.7601144 (Pubitemid 44012229)
33. Cao R., Tsukada Y., Zhang Y., Role of Bmi-1 and Ring1A in H2A ubiquitylation and hox gene silencing. Molecular Cell 2005 20 6 845 854 2-s2.0-29144487990 10.1016/j.molcel.2005.12.002 (Pubitemid 41814874)
34. Guzzo C. M., Berndsen C. E., Zhu J., RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Science Signaling 2012 5 253 ra88 10.1126/scisignal.2003485
35. Vyas R., Kumar R., Clermont F., RNF4 is required for DNA double-strand break repair in vivo. Cell Death & Differentiation 2013 20 3 490 502
36. Yin Z., Menendez D., Resnick M. A., French J. E., Janardhan K. S., Jetten A. M., RAP80 is critical in maintaining genomic stability and suppressing tumor development. Cancer Research 2012 72 19 5080 5090
37. Bellare P., Small E. C., Huang X., Wohlschlegel J. A., Staley J. P., Sontheimer E. J., A role for ubiquitin in the spliceosome assembly pathway. Nature Structural & Molecular Biology 2008 15 5 444 451 (Pubitemid 351653580)
38. Ohi M. D., Vander Kooi C. W., Rosenberg J. A., Chazin W. J., Gould K. L., Structural insights into the U-box, a domain associated with multi-ubiquitination. Nature Structural Biology 2003 10 4 250 255 2-s2.0-0037389970 10.1038/nsb906 (Pubitemid 36418748)
39. Mahajan K. N., Mitchell B. S., Role of human Pso4 in mammalian DNA repair and association with terminal deoxynucleotidyl transferase. Proceedings of the National Academy of Sciences of the United States of America 2003 100 19 10746 10751 2-s2.0-0141703274 10.1073/pnas.1631060100 (Pubitemid 37140099)
40. Wahl M. C., Will C. L., Lührmann R., The spliceosome: design principles of a dynamic RNP machine. Cell 2009 136 4 701 718 2-s2.0-60349104299 10.1016/j.cell.2009.02.009
41. Lu X., Legerski R. J., The Prp19/Pso4 core complex undergoes ubiquitylation and structural alterations in response to DNA damage. Biochemical and Biophysical Research Communications 2007 354 4 968 974 2-s2.0-33846829798 10.1016/j.bbrc.2007.01.097 (Pubitemid 46216227)
42. Jackson S. P., Durocher D., Regulation of DNA damage responses by ubiquitin and SUMO. Molecular Cell 2013 49 5 795 807
43. Pelisch F., Gerez J., Druker J., Schor I. E., Muñoz M. J., Risso G., Petrillo E., Westman B. J., Lamond A. I., Arzt E., Srebrow A., The serine/arginine-rich protein SF2/ASF regulates protein sumoylation. Proceedings of the National Academy of Sciences of the United States of America 2010 107 37 16119 16124 2-s2.0-77957986445 10.1073/pnas.1004653107
44. Vassileva M. T., Matunis M. J., SUMO modification of heterogeneous nuclear ribonucleoproteins. Molecular and Cellular Biology 2004 24 9 3623 3632 2-s2.0-1942422565 10.1128/MCB.24.9.3623-3632.2004 (Pubitemid 38496143)
45. Bomsztyk K., Denisenko O., Ostrowski J., hnRNP K: one protein multiple processes. BioEssays 2004 26 6 629 638 2-s2.0-2942623743 10.1002/bies.20048 (Pubitemid 38758340)
46. Pelisch F., Pozzi B., Risso G., Munoz M. J., Srebrow A., DNA damage-induced heterogeneous nuclear ribonucleoprotein K sumoylation regulates p53 transcriptional activation. Journal of Biological Chemistry 2012 287 36 30789 30799
47. Moumen A., Masterson P., O'Connor M. J., Jackson S. P., hnRNP K: an HDM2 target and transcriptional coactivator of p53 in response to DNA damage. Cell 2005 123 6 1065 1078 2-s2.0-28944446040 10.1016/j.cell.2005.09.032 (Pubitemid 41785421)
48. Wang D., Lippard S. J., Cellular processing of platinum anticancer drugs. Nature Reviews Drug Discovery 2005 4 4 307 320 2-s2.0-18244379333 10.1038/nrd1691 (Pubitemid 41130944)
49. Collins I., Weber A., Levens D., Transcriptional consequences of topoisomerase inhibition. Molecular and Cellular Biology 2001 21 24 8437 8451 2-s2.0-0035200324 10.1128/MCB.21.24.8437-8451.2001 (Pubitemid 33108603)
50. Luco R. F., Allo M., Schor I. E., Kornblihtt A. R., Misteli T., Epigenetics in alternative pre-mRNA splicing. Cell 2011 144 1 16 26 2-s2.0-78650961149 10.1016/j.cell.2010.11.056
51. Allemand E., Batsché E., Muchardt C., Splicing, transcription, and chromatin: a menage a trois. Current Opinion in Genetics and Development 2008 18 2 145 151 2-s2.0-44449158814 10.1016/j.gde.2008.01.006 (Pubitemid 351756536)
52. de la Mata M., Kornblihtt A. R., RNA polymerase II C-terminal domain mediates regulation of alternative splicing by SRp20. Nature Structural and Molecular Biology 2006 13 11 973 980 2-s2.0-33750596100 10.1038/nsmb1155 (Pubitemid 44684848)
53. Muñoz M. J., Santangelo M. S. P., Paronetto M. P., de la Mata M., Pelisch F., Boireau S., Glover-Cutter K., Ben-Dov C., Blaustein M., Lozano J. J., Bird G., Bentley D., Bertrand E., Kornblihtt A. R., DNA damage regulates alternative splicing through inhibition of RNA polymerase II elongation. Cell 2009 137 4 708 720 2-s2.0-65549147264 10.1016/j.cell.2009.03.010
54. 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. Genome Research 2011 21 3 390 401 2-s2.0-79952266577 10.1101/gr.111070.110
55. Solier S., Barb J., Zeeberg B. R., Varma S., Ryan M. C., Kohn K. W., Weinstein J. N., Munson P. J., Pommier Y., Genome-wide analysis of novel splice variants induced by topoisomerase I poisoning shows preferential occurrence in genes encoding splicing factors. Cancer Research 2010 70 20 8055 8065 2-s2.0-78049239924 10.1158/0008-5472.CAN-10-2491
56. Dutertre M., Sanchez G., De Cian M. C., Cotranscriptional exon skipping in the genotoxic stress response. Nature Structural & Molecular Biology 2010 17 11 1358 1366
57. alt1 in tumor and nontumorigenic cell lines correlating with p53 stability. Cancer Research 2006 66 19 9467 9473 2-s2.0-33750343019 10.1158/0008-5472.CAN-05-3013 (Pubitemid 44623644)
58. Chansky H. A., Hu M., Hickstein D. D., Yang L., Oncogenic TLS/ERG and EWS/Fli-1 fusion proteins inhibit RNA splicing mediated by YB-1 protein. Cancer Research 2001 61 9 3586 3590 2-s2.0-0035328667 (Pubitemid 32694966)
59. Sprung C. N., Li J., Hovan D., McKay M. J., Forrester H. B., Alternative transcript initiation and splicing as a response to DNA damage. PloS One 2011 6 10 e25758 10.1371/journal.pone.0025758
60. Wang Z., Burge C. B., Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 2008 14 5 802 813 2-s2.0-42449098125 10.1261/rna.876308 (Pubitemid 351574901)
61. Pan Q., Shai O., Lee L. J., Frey B. J., Blencowe B. J., Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nature Genetics 2008 40 12 1413 1415 2-s2.0-56749098074 10.1038/ng.259
62. Mazoyer S., Puget N., Perrin-Vidoz L., Lynch H. T., Serova-Sinilnikova O. M., Lenoir G. M., A BRCA1 nonsense mutation causes exon skipping. American Journal of Human Genetics 1998 62 3 713 715 2-s2.0-0031981818 10.1086/301768 (Pubitemid 28164630)
63. Cartegni L., Chew S. L., Krainer A. R., Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nature Reviews Genetics 2002 3 4 285 298 2-s2.0-0036207384 10.1038/nrg775 (Pubitemid 34279797)
64. Sanz D. J., Acedo A., Infante M., Durán M., Pérez-Cabornero L., Esteban-Cardeñosa E., Lastra E., Pagani F., Miner C., Velasco E. A., A high proportion of DNA variants of BRCA1 and BRCA2 is associated with aberrant splicing in breast/ovarian cancer patients. Clinical Cancer Research 2010 16 6 1957 1967 2-s2.0-77949762254 10.1158/1078-0432.CCR-09-2564
65. Rouleau E., Lefol C., Moncoutier V., Castera L., Houdayer C., Caputo S., Bièche I., Buisson M., Mazoyer S., Stoppa-Lyonnet D., Noguès C., Lidereau R., A missense variant within BRCA1 exon 23 causing exon skipping. Cancer Genetics and Cytogenetics 2010 202 2 144 146 2-s2.0-77957084466 10.1016/j.cancergencyto.2010.07.122
66. Raponi M., Kralovicova J., Copson E., Divina P., Eccles D., Johnson P., Baralle D., Vorechovsky I., Prediction of single-nucleotide substitutions that result in exon skipping: identification of a splicing silencer in BRCA1 exon 6. Human Mutation 2011 32 4 436 444 2-s2.0-79952755720 10.1002/humu.21458
67. Théry J. C., Krieger S., Gaildrat P., Révillion F., Buisine M., Killian A., Duponchel C., Rousselin A., Vaur D., Peyrat J., Berthet P., Frébourg T., Martins A., Hardouin A., Tosi M., Contribution of bioinformatics predictions and functional splicing assays to the interpretation of unclassified variants of the BRCA genes. European Journal of Human Genetics 2011 19 10 1052 1058 2-s2.0-80053052971 10.1038/ejhg.2011.100
68. Fackenthal J. D., Cartegni L., Krainer A. R., Olopade O. I., BRCA2 T2722R is a deleterious allele that causes exon skipping. American Journal of Human Genetics 2002 71 3 625 631 2-s2.0-0036724459 10.1086/342192 (Pubitemid 34970133)
69. Gaildrat P., Krieger S., Di Giacomo D., Multiple sequence variants of BRCA2 exon 7 alter splicing regulation. Journal of Medical Genetics 2012 49 10 609 617
70. Murphy K. M., Brune K. A., Griffin C., Sollenberger J. E., Petersen G. M., Bansal R., Hruban R. H., Kern S. E., Evaluation of candidate genes MAP2K4, MADH4, ACVR1B, and BRCA2 in familial pancreatic cancer: deleterious BRCA2 mutations in 17%. Cancer Research 2002 62 13 3789 3793 2-s2.0-0036644884 (Pubitemid 34728862)
71. Fang N. Y., Greiner T. C., Weisenburger D. D., Chan W. C., Vose J. M., Smith L. M., Armitage J. O., Mayer R. A., Pike B. L., Collins F. S., Hacia J. G., Oligonucleotide microarrays demonstrate the highest frequency of ATM mutations in the mantle cell subtype of lymphoma. Proceedings of the National Academy of Sciences of the United States of America 2003 100 9 5372 5377 2-s2.0-0037627448 10.1073/pnas.0831102100 (Pubitemid 36542712)
72. Ejima Y., Yang L., Sasaki M. S., Aberrant splicing of the ATM gene associated with shortening of the intronic mononucleotide tract in human colon tumor cell lines: a novel mutation target of microsatellite instability. International Journal of Cancer 2000 86 2 262 268 (Pubitemid 30180823)
73. Ham M. F., Takakuwa T., Luo W., Liu A., Horii A., Aozasa K., Impairment of double-strand breaks repair and aberrant splicing of ATM and MRE11 in leukemia-lymphoma cell lines with microsatellite instability. Cancer Science 2006 97 3 226 234 2-s2.0-33646009986 10.1111/j.1349-7006.2006.00165.x
74. Thorstenson Y. R., Roxas A., Kroiss R., Jenkins M. A., Yu K. M., Bachrich T., Muhr D., Wayne T. L., Chu G., Davis R. W., Wagner T. M. U., Oefner P. J., Contributions of ATM mutations to familial breast and ovarian cancer. Cancer Research 2003 63 12 3325 3333 2-s2.0-0038745419 (Pubitemid 36735890)
75. Giannini G., Ristori E., Cerignoli F., Rinaldi C., Zani M., Viel A., Ottini L., Crescenzi M., Martinotti S., Bignami M., Frati L., Screpanti I., Gulino A., Human MRE11 is inactivated in mismatch repair-deficient cancers. EMBO Reports 2002 3 3 248 254 2-s2.0-18344395671 10.1093/embo-reports/kvf044 (Pubitemid 34269518)
76. Durocher F., Labrie Y., Soucy P., Sinilnikova O., Labuda D., Bessette P., Chiquette J., Laframboise R., Lépine J., Lespérance B., Ouellette G., Pichette R., Plante M., Tavtigian S. V., Simard J., Mutation analysis and characterization of ATR sequence variants in breast cancer cases from high-risk French Canadian breast/ovarian cancer families. BMC Cancer 2006 6 230 2-s2.0-33749998118 10.1186/1471-2407-6-230 (Pubitemid 44566741)
77. Liu A., Takakuwa T., Fujita S., Luo W., Tresnasari K., Van Den Berg A., Poppema S., Aozasa K., ATR alterations in Hodgkin's lymphoma. Oncology Reports 2008 19 4 999 1005 2-s2.0-43849098414 (Pubitemid 351802672)
78. Mokrani-Benhelli H., Gaillard L., Biasutto P., Primary microcephaly, impaired DNA replication, and genomic instability caused by compound heterozygous ATR mutations. Human Mutation 2013 34 2 374 384
79. O'Driscoll M., Ruiz-Perez V. L., Woods C. G., Jeggo P. A., Goodship J. A., A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nature Genetics 2003 33 4 497 501 2-s2.0-0345073699 10.1038/ng1129 (Pubitemid 36390012)
80. Cleaver J. E., Thompson L. H., Richardson A. S., States J. C., A summary of mutations in the UV-sensitive disorders: xeroderma pigmentosum, Cockayne syndrome, and trichothiodystrophy. Human Mutation 1999 14 1 9 22 (Pubitemid 29309939)
81. Abbaszadeh F., Clingen P. H., Arlett C. F., Plowman P. N., Bourton E. C., Themis M., Makarov E. M., Newbold R. F., Green M. H. L., Parris C. N., A novel splice variant of the DNA-PKcs gene is associated with clinical and cellular radiosensitivity in a patient with xeroderma pigmentosum. Journal of Medical Genetics 2010 47 3 176 181 2-s2.0-77949724541 10.1136/jmg.2009.068866
82. Betz B., Theiss S., Aktas M., Konermann C., Goecke T. O., Möslein G., Schaal H., Royer-Pokora B., Comparative in silico analyses and experimental validation of novel splice site and missense mutations in the genes MLH1 and MSH2. Journal of Cancer Research and Clinical Oncology 2010 136 1 123 134 2-s2.0-71449113660 10.1007/s00432-009-0643-z
83. Pagenstecher C., Wehner M., Friedl W., Rahner N., Aretz S., Friedrichs N., Sengteller M., Henn W., Buettner R., Propping P., Mangold E., Aberrant splicing in MLH1 and MSH2 due to exonic and intronic variants. Human Genetics 2006 119 1-2 9 22 2-s2.0-33644546026 10.1007/s00439-005-0107-8
84. Renkonen E., Lohi H., Järvinen H. J., Mecklin J., Peltomäki P., Novel splicing associations of hereditary colon cancer related DNA mismatch repair gene mutations. Journal of Medical Genetics 2004 41 7 e95 2-s2.0-16544371552
85. Staalesen V., Falck J., Geisler S., Bartkova J., Børresen-Dale A., Lukas J., Lillehaug J. R., Bartek J., Lønning P. E., Alternative splicing and mutation status of CHEK2 in stage III breast cancer. Oncogene 2004 23 52 8535 8544 2-s2.0-9144232488 10.1038/sj.onc.1207928 (Pubitemid 39540804)
86. Bellare P., Kutach A. K., Rines A. K., Guthrie C., Sontheimer E. J., Ubiquitin binding by a variant Jab1/MPN domain in the essential pre-mRNA splicing factor Prp8p. RNA 2006 12 2 292 302 2-s2.0-31044444461 10.1261/rna.2152306 (Pubitemid 43121934)
87. Stratton M. R., Rahman N., The emerging landscape of breast cancer susceptibility. Nature Genetics 2008 40 1 17 22 2-s2.0-37549056200 10.1038/ng.2007.53
88. Liu H. X., Cartegni L., Zhang M. Q., Krainer A. R., A mechanism for exon skipping caused by nonsense or missense mutations in BRCA1 and other genes. Nature Genetics 2001 27 1 55 58 2-s2.0-0035158730 10.1038/83762 (Pubitemid 32044518)
89. Concannon P., Gatti R. A., Diversity of ATM gene mutations detected in patients with ataxia-telangiectasia. Human Mutation 1997 10 2 100 107 (Pubitemid 27327484)
90. Teraoka S. N., Telatar M., Becker-Catania S., Liang T., Önengüt S., Tolun A., Chessa L., Sanal Ö., Bernatowska E., Gatti R. A., Concannon P., Splicing defects the ataxia-telangiectasia gene, ATM: underlying mutations and consequences. American Journal of Human Genetics 1999 64 6 1617 1631 2-s2.0-0039108539 10.1086/302418 (Pubitemid 30481513)
91. Eng L., Coutinho G., Nahas S., Yeo G., Tanouye R., Babaei M., Dörk T., Burge C., Gatti R. A., Nonclassical splicing mutations in the coding and noncoding regions of the ATM gene: maximum entropy estimates of splice junction strengths. Human Mutation 2004 23 1 67 76 2-s2.0-0347988093 10.1002/humu.10295 (Pubitemid 38056103)
92. Paganil F., Burattil E., Stuani C., Bendix R., Dörk T., Baralle F. E., A new type of mutation causes a splicing defect in ATM. Nature Genetics 2002 30 4 426 429 2-s2.0-0036544858 10.1038/ng858
93. Pastor T., Talotti G., Lewandowska M. A., Pagani F., An Alu-derived intronic splicing enhancer facilitates intronic processing and modulates aberrant splicing in ATM. Nucleic Acids Research 2009 37 21 7258 7267 2-s2.0-75349097325 10.1093/nar/gkp778 gkp778
94. Dhir A., Buratti E., Van Santen M. A., Lührmann R., Baralle F. E., The intronic splicing code: multiple factors involved in ATM pseudoexon definition. EMBO Journal 2010 29 4 749 760 2-s2.0-77149153689 10.1038/emboj.2009.397
95. Lewandowska M. A., Stuani C., Parvizpur A., Baralle F. E., Pagani F., Functional studies on the ATM intronic splicing processing element. Nucleic Acids Research 2005 33 13 4007 4015 2-s2.0-22244491011 10.1093/nar/gki710 (Pubitemid 41487261)
96. Knudsen K. E., Alan Diehl J., Haiman C. A., Knudsen E. S., Cyclin D1: polymorphism, aberrant splicing and cancer risk. Oncogene 2006 25 11 1620 1628 2-s2.0-33645118564 10.1038/sj.onc.1209371
97. Betticher D. C., Thatcher N., Altermatt H. J., Hoban P., Ryder W. D. J., Heighway J., Alternate splicing produces a novel cyclin D1 transcript. Oncogene 1995 11 5 1005 1011 2-s2.0-0029083790
98. Lu F., Gladden A. B., Diehl J. A., An Alternatively Spliced Cyclin D1 Isoform, Cyclin D1b, Is a Nuclear Oncogene. Cancer Research 2003 63 21 7056 7061 2-s2.0-0242526150 (Pubitemid 37413439)
99. Wang Y., Dean J. L., Millar E. K. A., Thai H. T., McNeil C. M., Burd C. J., Henshall S. M., Utama F. E., Witkiewicz A., Rui H., Sutherland R. L., Knudsen K. E., Knudsen E. S., Cyclin D1b is aberrantly regulated in response to therapeutic challenge and promotes resistance to estrogen antagonists. Cancer Research 2008 68 14 5628 5638 2-s2.0-48649103464 10.1158/0008-5472.CAN-07-3170
100. Burd C. J., Petre C. E., Morey L. M., Wang Y., Revelo M. P., Haiman C. A., Lu S., Fenoglio-Preiser C. M., Li J., Knudsen E. S., Wong J., Knudsen K. E., Cyclin D1b variant influences prostate cancer growth through aberrant androgen receptor regulation. Proceedings of the National Academy of Sciences of the United States of America 2006 103 7 2190 2195 2-s2.0-33144474074 10.1073/pnas.0506281103 (Pubitemid 43271645)
101. Solomon D. A., Wang Y., Fox S. R., Lambeck T. C., Giesting S., Lan Z., Senderowicz A. M., Knudsen E. S., Cyclin D1 splice variants: differential effects on localization, RB phosphorylation, and cellular transformation. Journal of Biological Chemistry 2003 278 32 30339 30347 2-s2.0-0041528506 10.1074/jbc.M303969200 (Pubitemid 36962428)
102. Li Z., Jiao X., Wang C., Shirley L. A., Elsaleh H., Dahl O., Wang M., Soutoglou E., Knudsen E. S., Pestell R. G., Alternative cyclin D1 splice forms differentially regulate the DNA damage response. Cancer Research 2010 70 21 8802 8811 2-s2.0-78449273892 10.1158/0008-5472.CAN-10-0312
103. Myklebust M. P., Li Z., Tran T. H., Expression of cyclin D1a and D1b as predictive factors for treatment response in colorectal cancer. British Journal of Cancer 2012 107 10 1684 1691
104. Olshavsky N. A., Comstock C. E. S., Schiewer M. J., Augello M. A., Hyslop T., Sette C., Zhang J., Parysek L. M., Knudsen K. E., Identification of ASF/SF2 as a critical, allele-specific effector of the cyclin D1b oncogene. Cancer Research 2010 70 10 3975 3984 2-s2.0-77952796886 10.1158/0008-5472.CAN-09-3468
105. Paronetto M. P., Cappellari M., Busà R., Alternative splicing of the cyclin D1 proto-oncogene is regulated by the RNA-binding protein Sam68. Cancer Research 2010 70 1 229 239 2-s2.0-76749118934 10.1158/0008-5472.CAN-10- 0036
106. Sanchez G., Bittencourt D., Laud K., Barbier J., Delattre O., Auboeuf D., Dutertre M., Alteration of cyclin D1 transcript elongation by a mutated transcription factor up-regulates the oncogenic D1b splice isoform in cancer. Proceedings of the National Academy of Sciences of the United States of America 2008 105 16 6004 6009 2-s2.0-43149105398 10.1073/pnas.0710748105 (Pubitemid 351758389)
107. Pabla N., Bhatt K., Dong Z., Checkpoint kinase 1 (Chk1)-short is a splice variant and endogenous inhibitor of Chk1 that regulates cell cycle and DNA damage checkpoints. Proceedings of the National Academy of Sciences of the United States of America 2012 109 1 197 202 2-s2.0-84856015337 10.1073/pnas.1104767109
108. Li X., Manley J. L., Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 2005 122 3 365 378 2-s2.0-23744455164 10.1016/j.cell.2005.06.008 (Pubitemid 41127139)
109. Aguilera A., Gómez-González B., Genome instability: a mechanistic view of its causes and consequences. Nature Reviews Genetics 2008 9 3 204 217 2-s2.0-39449096135 10.1038/nrg2268 (Pubitemid 351271797)
110. Li X., Manley J. L., Cotranscriptional processes and their influence on genome stability. Genes and Development 2006 20 14 1838 1847 2-s2.0-33746093492 10.1101/gad.1438306 (Pubitemid 44079322)
111. Xiao R., Sun Y., Ding J., Lin S., Rose D. W., Rosenfeld M. G., Fu X., Li X., Splicing regulator SC35 is essential for genomic stability and cell proliferation during mammalian organogenesis. Molecular and Cellular Biology 2007 27 15 5393 5402 2-s2.0-34547190674 10.1128/MCB.00288-07 (Pubitemid 47124393)
112. Paulsen R. D., Soni D. V., Wollman R., Hahn A. T., Yee M., Guan A., Hesley J. A., Miller S. C., Cromwell E. F., Solow-Cordero D. E., Meyer T., Cimprich K. A., A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Molecular Cell 2009 35 2 228 239 2-s2.0-67651119997 10.1016/j.molcel.2009.06.021
113. Gan W., Guan Z., Liu J., Gui T., Shen K., Manley J. L., Li X., R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes and Development 2011 25 19 2041 2056 2-s2.0-80053645721 10.1101/gad.17010011
114. Je E. M., Yoo N. J., Kim Y. J., Kim M. S., Lee S. H., Mutational analysis of splicing machinery genes SF3B1, U2AF1 and SRSF2 in myelodysplasia and other common tumors. International Journal of Cancer 2013 133 1 260 265
115. Harbour J. W., Roberson E. D., Anbunathan H., Onken M. D., Worley L. A., Bowcock A. M., Recurrent mutations at codon 625 of the splicing factor SF3B1 in uveal melanoma. Nature Genetics 2013 45 2 133 135
116. Abdel-Wahab O., Manshouri T., Patel J., Harris K., Yao J., Hedvat C., Heguy A., Bueso-Ramos C., Kantarjian H., Levine R. L., Verstovsek S., Genetic analysis of transforming events that convert chronic myeloproliferative neoplasms to leukemias. Cancer Research 2010 70 2 447 452 2-s2.0-76549109434 10.1158/0008-5472.CAN-09-3783
117. Quesada V., Conde L., Villamor N., Ordóñez G. R., Jares P., Bassaganyas L., Ramsay A. J., Beà S., Pinyol M., Martínez-Trillos A., López-Guerra M., Colomer D., Navarro A., Baumann T., Aymerich M., Rozman M., Delgado J., Giné E., Hernández J. M., González-Díaz M., Puente D. A., Velasco G., Freije J. M. P., Tubío J. M. C., Royo R., Gelpí J. L., Orozco M., Pisano D. G., Zamora J., Vázquez M., Valencia A., Himmelbauer H., Bayés M., Heath S., Gut M., Gut I., Estivill X., López-Guillermo A., Puente X. S., Campo E., López-Otín C., Exome sequencing identifies recurrent mutations of the splicing factor SF3B1 gene in chronic lymphocytic leukemia. Nature Genetics 2012 44 1 47 52 2-s2.0-84555171449 10.1038/ng.1032
118. Yoshida K., Sanada M., Shiraishi Y., Nowak D., Nagata Y., Yamamoto R., Sato Y., Sato-Otsubo A., Kon A., Nagasaki M., Chalkidis G., Suzuki Y., Shiosaka M., Kawahata R., Yamaguchi T., Otsu M., Obara N., Sakata-Yanagimoto M., Ishiyama K., Mori H., Nolte F., Hofmann W., Miyawaki S., Sugano S., Haferlach C., Koeffler H. P., Shih L., Haferlach T., Chiba S., Nakauchi H., Miyano S., Ogawa S., Frequent pathway mutations of splicing machinery in myelodysplasia. Nature 2011 478 7367 64 69 2-s2.0-80053900941 10.1038/nature10496
119. Papaemmanuil E., Cazzola M., Boultwood J., Malcovati L., Vyas P., Bowen D., Pellagatti A., Wainscoat J. S., Hellstrom-Lindberg E., Gambacorti-Passerini C., Godfrey A. L., Rapado I., Cvejic A., Rance R., McGee C., Ellis P., Mudie L. J., Stephens P. J., McLaren S., Massie C. E., Tarpey P. S., Varela I., Nik-Zainal S., Davies H. R., Shlien A., Jones D., Raine K., Hinton J., Butler A. P., Teague J. W., Baxter E. J., Score J., Galli A., Della Porta M. G., Travaglino E., Groves M., Tauro S., Munshi N. C., Anderson K. C., El-Naggar A., Fischer A., Mustonen V., Warren A. J., Cross N. C. P., Green A. R., Futreal P. A., Stratton M. R., Campbell P. J., Somatic SF3B1 mutation in myelodysplasia with ring sideroblasts. New England Journal of Medicine 2011 365 15 1384 1395 2-s2.0-80054010617 10.1056/NEJMoa1103283
120. Matsuoka S., Ballif B. A., Smogorzewska A., McDonald E. R. III, Hurov K. E., Luo J., Bakalarski C. E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S. P., Elledge S. J., ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007 316 5828 1160 1166 2-s2.0-34249947699 10.1126/science.1140321 (Pubitemid 46877472)
121. Hurov K. E., Cotta-Ramusino C., Elledge S. J., A genetic screen identifies the Triple T complex required for DNA damage signaling and ATM and ATR stability. Genes and Development 2010 24 17 1939 1950 2-s2.0-77956283656 10.1101/gad.1934210
122. O'Connell B. C., Adamson B., Lydeard J. R., Sowa M. E., Ciccia A., Bredemeyer A. L., Schlabach M., Gygi S. P., Elledge S. J., Harper J. Wade J. W., A genome-wide camptothecin sensitivity screen identifies a mammalian MMS22L-NFKBIL2 complex required for genomic stability. Molecular Cell 2010 40 4 645 657 2-s2.0-78649316608 10.1016/j.molcel.2010.10.022
123. Li H., Watford W., Li C., Parmelee A., Bryant M. A., Deng C., O'Shea J., Sean B. L., Ewing sarcoma gene EWS is essential for meiosis and B lymphocyte development. Journal of Clinical Investigation 2007 117 5 1314 1323 2-s2.0-34248203558 10.1172/JCI31222 (Pubitemid 46718419)
124. Paronetto M. P., Miñana B., Valcárcel J., The ewing sarcoma protein regulates DNA damage-induced alternative splicing. Molecular Cell 2011 43 3 353 368 2-s2.0-79960925229 10.1016/j.molcel.2011.05.035
125. Lackner D. H., Durocher D., Karlseder J., A siRNA-based screen for genes involved in chromosome end protection. PLoS ONE 2011 6 6 2-s2.0-79959534357 10.1371/journal.pone.0021407 e21407
126. Heinrich B., Zhang Z., Raitskin O., Hiller M., Benderska N., Hartmann A. M., Bracco L., Elliott D., Ben-Ari S., Soreq H., Sperling J., Sperling R., Stamm S., Heterogeneous nuclear ribonucleoprotein G regulates splice site selection by binding to CC(A/C)-rich regionsin pre-mRNA. Journal of Biological Chemistry 2009 284 21 14303 14315 2-s2.0-67649831277 10.1074/jbc.M901026200
127. Adamson B., Smogorzewska A., Sigoillot F. D., King R. W., Elledge S. J., A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nature Cell Biology 2012 14 3 318 328 2-s2.0-84857781943 10.1038/ncb2426
128. Lee K. M., Hsu I. W., Tarn W. Y., TRAP150 activates pre-mRNA splicing and promotes nuclear mRNA degradation. Nucleic Acids Research 2010 38 10 3340 3350 2-s2.0-77953722272 10.1093/nar/gkq017 gkq017
129. Bracken C. P., Wall S. J., Barré B., Panov K. I., Ajuh P. M., Perkins N. D., Regulation of cyclin D1 RNA stability by SNIP1. Cancer Research 2008 68 18 7621 7628 2-s2.0-54749132279 10.1158/0008-5472.CAN-08-1217
130. Li C., Lin R., Lai M., Ouyang P., Tarn W., Nuclear Pnn/DRS protein binds to spliced mRNPs and participates in mRNA processing and export via interaction with RNPS1. Molecular and Cellular Biology 2003 23 20 7363 7376 2-s2.0-0141752774 10.1128/MCB.23.20.7363-7376.2003 (Pubitemid 37211015)
131. Venables J. P., Klinck R., Koh C., Gervais-Bird J., Bramard A., Inkel L., Durand M., Couture S., Froehlich U., Lapointe E., Lucier J., Thibault P., Rancourt C., Tremblay K., Prinos P., Chabot B., Elela S. A., Cancer-associated regulation of alternative splicing. Nature Structural and Molecular Biology 2009 16 6 670 676 2-s2.0-67349097457 10.1038/nsmb.1608
132. Karni R., De Stanchina E., Lowe S. W., Sinha R., Mu D., Krainer A. R., The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nature Structural and Molecular Biology 2007 14 3 185 193 2-s2.0-33847630730 10.1038/nsmb1209 (Pubitemid 46355578)
133. Adamson B., Smogorzewska A., Sigoillot F. D., King R. W., Elledge S. J., A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nature Cell Biology 2012 14 3 318 328 2-s2.0-84857781943 10.1038/ncb2426
134. Busà R., Geremia R., Sette C., Genotoxic stress causes the accumulation of the splicing regulator Sam68 in nuclear foci of transcriptionally active chromatin. Nucleic Acids Research 2010 38 9 3005 3018 2-s2.0-77953252238 10.1093/nar/gkq004 gkq004
135. Du L., Gatti R. A., Progress toward therapy with antisense-mediated splicing modulation. Current Opinion in Molecular Therapeutics 2009 11 2 116 123 2-s2.0-63849152847
136. Zammarchi F., De Stanchina E., Bournazou E., Supakorndej T., Martires K., Riedel E., Corben A. D., Bromberg J. F., Cartegni L., Antitumorigenic potential of STAT3 alternative splicing modulation. Proceedings of the National Academy of Sciences of the United States of America 2011 108 43 17779 17784 2-s2.0-80055072546 10.1073/pnas.1108482108
137. Bauman J. A., Kole R., Modulation of RNA splicing as a potential treatment for cancer. Bioengineered Bugs 2011 2 3 125 128 2-s2.0-79960282729 10.4161/bbug.2.3.15165
138. Bonnal S., Vigevani L., Valcarcel J., The spliceosome as a target of novel antitumour drugs. Nature Reviews Drug Discovery 2012 11 11 847 859