Expression of Tra2 β in cancer cells as a potential contributory factor to neoplasia and metastasis

International Journal of Cell Biology

Volumn , Issue , 2013, Pages

  Best, Andrew ^a   Dagliesh, Caroline ^a   Ehrmann, Ingrid ^a   Kheirollahi Kouhestani, Mahsa ^a   Tyson Capper, Alison ^a   Elliott, David J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; REACTIVE OXYGEN METABOLITE; RNA BINDING PROTEIN; SERINE ARGININE RICH PROTEIN; TRA2 BETA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETS 1; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; CANCER CELL; CARCINOGENESIS; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION; GENE FUNCTION; HUMAN; LIVER CANCER; METASTASIS; NONHUMAN; ONCOGENE MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTO ONCOGENE; REVIEW; SPLICEOSOME; UPREGULATION;

EID: 84880904913     PISSN: 16878876     EISSN: 16878884     Source Type: Journal    
DOI: 10.1155/2013/843781     Document Type: Review

References (65)

1. Hanahan D., Weinberg R. A., Hallmarks of cancer: the next generation. Cell 2011 144 5 646 674 2-s2.0-79952284127 10.1016/j.cell.2011.02.013
2. Rajan P., Elliott D. J., Robson C. N., Leung H. Y., Alternative splicing and biological heterogeneity in prostate cancer. Nature Reviews Urology 2009 6 8 454 460 2-s2.0-76649088636 10.1038/nrurol.2009.125
3. Venables J. P., Aberrant and alternative splicing in cancer. Cancer Research 2004 64 21 7647 7654 2-s2.0-7444220147 10.1158/0008-5472.CAN-04-1910 (Pubitemid 39446889)
4. Venables J. P., Unbalanced alternative splicing and its significance in cancer. BioEssays 2006 28 4 378 386 2-s2.0-33645833000 10.1002/bies.20390
5. 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
6. Grosso A. R., Martins S., Carmo-Fonseca M., The emerging role of splicing factors in cancer. EMBO Reports 2008 9 11 1087 1093 2-s2.0-55549143293 10.1038/embor.2008.189
7. Bonnal S., Vigevani L., Valcarcel J., The spliceosome as a target of novel antitumour drugs. Nature Reviews Drug Discovery 2012 11 847 859
8. Long J. C., Caceres J. F., The SR protein family of splicing factors: master regulators of gene expression. Biochemical Journal 2009 417 1 15 27 2-s2.0-58249093940 10.1042/BJ20081501
9. Shepard P. J., Hertel K. J., The SR protein family. Genome Biology 2009 10 10 242 2-s2.0-75349085408
10. Zhou Z., Fu X. D., Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 2013 122 3 191 207 10.1007/s00412-013-0407- z
11. Tacke R., Tohyama M., Ogawa S., Manley J. L., Human Tra2 proteins are sequence-specific activators of pre-mRNA splicing. Cell 1998 93 1 139 148 2-s2.0-0032478506 10.1016/S0092-8674(00)81153-8 (Pubitemid 28173559)
12. Krainer A. R., Maniatis T., Multiple factors including the small nuclear ribonucleoproteins U1 and U2 are necessary for Pre-mRNA splicing in vitro. Cell 1985 42 3 725 736 2-s2.0-0022135603
13. Zahler A. M., Neugebauer K. M., Lane W. S., Roth M. B., Distinct functions of SR proteins in alternative pre-mRNA splicing. Science 1993 260 5105 219 222 2-s2.0-0027160003 (Pubitemid 23140888)
14. Elliott D. J., Best A., Dalgliesh C., Ehrmann I., Grellscheid S., How does Tra2beta protein regulate tissue-specific RNA splicing? Biochemical Society Transactions 2012 40 784 788
15. Grellscheid S., Dalgliesh C., Storbeck M., Best A., Liu Y., Jakubik M., Mende Y., Ehrmann I., Curk T., Rossbach K., Bourgeois C. F., Stévenin J., Grellscheid D., Jackson M. S., Wirth B., Elliott D. J., Identification of evolutionarily conserved exons as regulated targets for the splicing activator Tra2 β in development. PLoS Genetics 2011 7 12 2-s2.0-84855281890 10.1371/journal.pgen.1002390 e1002390
16. Cléry A., Jayne S., Benderska N., Dominguez C., Stamm S., Allain F. H.-T., Molecular basis of purine-rich RNA recognition by the human SR-like protein Tra2- β 1. Nature Structural and Molecular Biology 2011 18 4 443 451 2-s2.0-79953805056 10.1038/nsmb.2001
17. Tsuda K., Someya T., Kuwasako K., Takahashi M., He F., Unzai S., Inoue M., Harada T., Watanabe S., Terada T., Kobayashi N., Shirouzu M., Kigawa T., Tanaka A., Sugano S., Güntert P., Yokoyama S., Muto Y., Structural basis for the dual RNA-recognition modes of human Tra2- β RRM. Nucleic Acids Research 2011 39 4 1538 1553 2-s2.0-79952324952 10.1093/nar/gkq854
18. Novoyatleva T., Heinrich B., Tang Y., Benderska N., Butchbach M. E. R., Lorson C. L., Lorson M. A., Ben-Dov C., Fehlbaum P., Bracco L., Burghes A. H. M., Bollen M., Stamm S., Protein phosphatase 1 binds to the RNA recognition motif of several splicing factors and regulates alternative pre-mRNA processing. Human Molecular Genetics 2008 17 1 52 70 2-s2.0-37549002103 10.1093/hmg/ddm284
19. Mende Y., Jakubik M., Riessland M., Schoenen F., Roßbach K., Kleinridders A., Köhler C., Buch T., Wirth B., Deficiency of the splicing factor Sfrs10 results in early embryonic lethality in mice and has no impact on full-length SMN /Smn splicing. Human Molecular Genetics 2010 19 11 2154 2167 2-s2.0-77953519937 10.1093/hmg/ddq094 ddq094
20. Meyer L. R., Zweig A. S., Hinrichs A. S., The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Research 2013 41 D64 D69 10.1093/nar/gks1048
21. 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)
22. Cerami E., Gao J., Dogrusoz U., The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discovery 2012 2 401 404
23. Gao J., Aksoy B. A., Dogrusoz U., Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Science Signaling 2013 6 269 pl1 10.1126/scisignal.2004088
24. Das S., Anczukow O., Akerman M., Krainer A. R., Oncogenic splicing factor SRSF1 is a critical transcriptional target of MYC. Cell Reports 2012 1 110 117
25. Anczuków O., Rosenberg A. Z., Akerman M., Das S., Zhan L., Karni R., Muthuswamy S. K., Krainer A. R., The splicing factor SRSF1 regulates apoptosis and proliferation to promote mammary epithelial cell transformation. Nature Structural and Molecular Biology 2012 19 2 220 228 2-s2.0-84856759933 10.1038/nsmb.2207
26. Jia R., Li C., McCoy J. P., Deng C.-X., Zheng Z.-M., SRp20 is a proto-oncogene critical for cell proliferation and tumor induction and maintenance. International Journal of Biological Sciences 2010 6 7 806 826 2-s2.0-78650553169
27. He X., Arslan A. D., Pool M. D., Ho T.-T., Darcy K. M., Coon J. S., Beck W. T., Knockdown of splicing factor SRp20 causes apoptosis in ovarian cancer cells and its expression is associated with malignancy of epithelial ovarian cancer. Oncogene 2011 30 3 356 365 2-s2.0-78751647679 10.1038/onc.2010.426
28. Kurokawa K., Akaike Y., Masuda K., Downregulation of serine/arginine-rich splicing factor 3 induces G1 cell cycle arrest and apoptosis in colon cancer cells. Oncogene 2013 10.1038/onc.2013.86
29. Gabriel B., Hausen A. Z., Bouda J., Boudova L., Koprivova M., Hirschfeld M., Jäger M., Stickeler E., Significance of nuclear hTra2-beta1 expression in cervical cancer. Acta Obstetricia et Gynecologica Scandinavica 2009 88 2 216 221 2-s2.0-59649122661 10.1080/00016340802503021
30. Watermann D. O., Tang Y., Hausen A. Z., Jäger M., Stamm S., Stickeler E., Splicing factor Tra2- β 1 is specifically induced in breast cancer and regulates alternative splicing of the CD44 gene. Cancer Research 2006 66 9 4774 4780 2-s2.0-33646426385 10.1158/0008-5472.CAN-04-3294
31. Fischer D.-C., Noack K., Runnebaum I. B., Watermann D. O., Kieback D. G., Stamm S., Stickeler E., Expression of splicing factors in human ovarian cancer. Oncology Reports 2004 11 5 1085 1090 2-s2.0-13944276467
32. Kajita K., Kuwano Y., Kitamura N., Ets1 and heat shock factor 1 regulate transcription of the Transformer 2 β gene in human colon cancer cells. Journal of Gastroenterology 2013 10.1007/s00535-012-0745-2
33. Takeo K., Kawai T., Nishida K., Masuda K., Teshima-Kondo S., Tanahashi T., Rokutan K., Oxidative stress-induced alternative splicing of transformer 2 β (SFRS10) and CD44 pre-mRNAs in gastric epithelial cells. American Journal of Physiology 2009 297 2 C330 C338 2-s2.0-68849110620 10.1152/ajpcell.00009. 2009
34. Lincoln D. W. II, Bove K., The transcription factor Ets-1 in breast cancer. Frontiers in Bioscience 2005 10 506 511 2-s2.0-27544508293
35. Lincoln D. W. II, Phillips P. G., Bove K., Estrogen-induced Ets-1 promotes capillary formation in an in vitro tumor angiogenesis model. Breast Cancer Research and Treatment 2003 78 2 167 178 2-s2.0-0037358574 10.1023/A:1022904624054 (Pubitemid 36433910)
36. Dittmer J., The biology of the Ets1 proto-oncogene. Molecular Cancer 2003 2, article 29 2-s2.0-2942529276 10.1186/1476-4598-2-29 (Pubitemid 38751468)
37. Zhang X., Moor A. N., Merkler K. A., Liu Q., McLean M. P., Regulation of alternative splicing of liver scavenger receptor class B gene by estrogen and the involved regulatory splicing factors. Endocrinology 2007 148 11 5295 5304 2-s2.0-35548938260 10.1210/en.2007-0376 (Pubitemid 350012650)
38. Tsukamoto Y., Matsuo N., Ozawa K., Hori O., Higashi T., Nishizaki J., Tohnai N., Nagata I., Kawano K., Yutani C., Hirota S., Kitamura Y., Stern D. M., Ogawa S., Expression of a novel RNA-splicing factor, RA301/Tra2 β in vascular lesions and its role in smooth muscle cell proliferation. American Journal of Pathology 2001 158 5 1685 1694 2-s2.0-0035003275 (Pubitemid 32422933)
39. Matsuo N., Ogawa S., Imai Y., Takagi T., Tohyama M., Stern D., Wanaka A., Cloning of a novel RNA binding polypeptide (RA301) induced by hypoxia/reoxygenation. Journal of Biological Chemistry 1995 270 47 28216 28222 2-s2.0-0028807463 10.1074/jbc.270.47.28216
40. Daoud R., Mies G., Smialowska A., Oláh L., Hossmann K.-A., Stamm S., Ischemia induces a translocation of the splicing factor tra2- β 1 and changes alternative splicing patterns in the brain. Journal of Neuroscience 2002 22 14 5889 5899 2-s2.0-0037101633 (Pubitemid 35387633)
41. McGlincy N. J., Smith C. W. J., Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense? Trends in Biochemical Sciences 2008 33 8 385 393 2-s2.0-48149095822 10.1016/j.tibs.2008. 06.001
42. Stoilov P., Dauod R., Nayler O., Stamm S., Human tra2-beta1 autoregulates its protein concentration by infuencing alternative splicing of its pre-mRNA. Human Molecular Genetics 2004 13 5 509 524 2-s2.0-1542359466 10.1093/hmg/ddh051 (Pubitemid 38313210)
43. Lareau L. F., Inada M., Green R. E., Wengrod J. C., Brenner S. E., Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 2007 446 7138 926 929 2-s2.0-34247330971 10.1038/nature05676 (Pubitemid 46633161)
44. Finn R. M., Ellard K., Eirin-Lopez J. M., Ausio J., Vertebrate nucleoplasmin and NASP: egg histone storage proteins with multiple chaperone activities. The FASEB Journal 2012 26 4788 4804 10.1096/fj.12-216663
45. Cook A. J. L., Gurard-Levin Z. A., Vassias I., Almouzni G., A specific function for the histone chaperone NASP to fine-tune a reservoir of soluble H3-H4 in the histone supply chain. Molecular Cell 2011 44 6 918 927 2-s2.0-84255198348 10.1016/j.molcel.2011.11.021
46. UniProt Consortium, Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Research 2012 40 D71 D75 10.1093/nar/gkr981
47. Alekseev O. M., Richardson R. T., Tsuruta J. K., O'Rand M. G., Depletion of the histone chaperone tNASP inhibits proliferation and induces apoptosis in prostate cancer PC-3 cells. Reproductive Biology and Endocrinology 2011 9 50 2-s2.0-79955092713 10.1186/1477-7827-9-50
48. Ma W., Xie S., Ni M., Huang X., Hu S., Liu Q., Liu A., Zhang J., Zhang Y., MicroRNA-29a inhibited epididymal epithelial cell proliferation by targeting nuclear autoantigenic sperm protein (NASP). Journal of Biological Chemistry 2012 287 13 10189 10199 2-s2.0-84858972149 10.1074/jbc.M111.303636
49. Richardson R. T., Batova I. N., Widgren E. E., Zheng L.-X., Whitfield M., Marzluff W. F., O'Rand M. G., Characterization of the histone H1-binding protein, NASP, as a cell cycle-regulated somatic protein. Journal of Biological Chemistry 2000 275 39 30378 30386 2-s2.0-0034730502
50. Richardson R. T., Alekseev O. M., Grossman G., Widgren E. E., Thresher R., Wagner E. J., Sullivan K. D., Marzluff W. F., O'Rand M. G., Nuclear autoantigenic sperm protein (NASP), a linker histone chaperone that is required for cell proliferation. Journal of Biological Chemistry 2006 281 30 21526 21534 2-s2.0-33746342798 10.1074/jbc.M603816200 (Pubitemid 44115489)
51. Alekseev O. M., Richardson R. T., Alekseev O., O'Rand M. G., Analysis of gene expression profiles in HeLa cells in response to overexpression or siRNA-mediated depletion of NASP. Reproductive Biology and Endocrinology 2009 7, article 45 2-s2.0-66749110375 10.1186/1477-7827-7-45
52. Ali-Fehmi R., Chatterjee M., Ionan A., Levin N. K., Arabi H., Bandyopadhyay S., Shah J. P., Bryant C. S., Hewitt S. M., O'Rand M. G., Alekseev O. M., Morris R., Munkarah A., Abrams J., Tainsky M. A., Analysis of the expression of human tumor antigens in ovarian cancer tissues. Cancer Biomarkers 2009 6 1 33 48 2-s2.0-77249166533 10.3233/CBM-2009-0117
53. 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)
54. Ponta H., Sherman L., Herrlich P. A., CD44: from adhesion molecules to signalling regulators. Nature Reviews Molecular Cell Biology 2003 4 1 33 45 2-s2.0-0037227965 10.1038/nrm1004 (Pubitemid 36077255)
55. Screaton G. R., Bell M. V., Jackson D. G., Cornelis F. B., Gerth U., Bell J. I., Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proceedings of the National Academy of Sciences of the United States of America 1992 89 24 12160 12164 2-s2.0-0027065573 10.1073/pnas.89.24.12160 (Pubitemid 23004805)
56. Brown R. L., Reinke L. M., Damerow M. S., Perez D., Chodosh L. A., Yang J., Cheng C., CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. Journal of Clinical Investigation 2011 121 3 1064 1074 2-s2.0-79952227361 10.1172/JCI44540
57. Venables J. P., Bourgeois C. F., Dalgliesh C., Kister L., Stevenin J., Elliott D. J., Up-regulation of the ubiquitous alternative splicing factor Tra2 β causes inclusion of a germ cell-specific exon. Human Molecular Genetics 2005 14 16 2289 2303 2-s2.0-26444575502 10.1093/hmg/ddi233 (Pubitemid 41417993)
58. Liu Y., Bourgeois C. F., Pang S., Kudla M., Dreumont N., Kister L., Sun Y.-H., Stevenin J., Elliott D. J., The germ cell nuclear proteins hnRNP G-T and RBMY activate a testis-specific exon. PLoS Genetics 2009 5 11 2-s2.0-73649137474 10.1371/journal.pgen.1000707 e1000707
59. Nasim M. T., Chernova T. K., Chowdhury H. M., Yue B.-G., Eperon I. C., HnRNP G and Tra2 β: opposite effects on splicing matched by antagonism in RNA binding. Human Molecular Genetics 2003 12 11 1337 1348 2-s2.0-0037669004 10.1093/hmg/ddg136 (Pubitemid 36722614)
60. Hofmann Y., Lorson C. L., Stamm S., Androphy E. J., Wirth B., Htra2- β 1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proceedings of the National Academy of Sciences of the United States of America 2000 97 17 9618 9623 2-s2.0-0034662922 (Pubitemid 30650825)
61. Tsuei D.-J., Lee P.-H., Peng H.-Y., Lu S.-L., Su D.-S., Jeng Y.-M., Hsu H.-C., Hsu S.-H., Wu J.-F., Ni Y.-H., Chang M.-H., Male germ cell-specific RNA binding protein RBMY: a new oncogene explaining male predominance in liver cancer. PLoS ONE 2011 6 11 2-s2.0-80455150228 10.1371/journal.pone.0026948 e26948
62. Elliott D. J., Bourgeois C. F., Klink A., Stévenin J., Cooke H. J., A mammalian germ cell-specific RNA-binding protein interacts with ubiquitously expressed proteins involved in splice site selection. Proceedings of the National Academy of Sciences of the United States of America 2000 97 11 5717 5722 2-s2.0-0034705231 10.1073/pnas.97.11.5717 (Pubitemid 30367464)
63. Moore M. J., Wang Q., Kennedy C. J., Silver P. A., An alternative splicing network links cell-cycle control to apoptosis. Cell 2010 142 4 625 636 2-s2.0-77955662560 10.1016/j.cell.2010.07.019
64. Paronetto M. P., Achsel T., Massiello A., Chalfant C. E., Sette C., The RNA-binding protein Sam68 modulates the alternative splicing of Bcl-x. Journal of Cell Biology 2007 176 7 929 939 2-s2.0-33947712084 10.1083/jcb.200701005 (Pubitemid 46506967)
65. Gautrey H. L., Tyson-Capper A. J., Regulation of Mcl-1 by SRSF1 and SRSF5 in cancer cells. PLoS ONE 2012 7 10.1371/journal.pone.0051497 e51497