A large-scale analysis of alternative splicing reveals a key role of QKI in lung cancer

Molecular Oncology

Volumn 10, Issue 9, 2016, Pages 1437-1449

  de Miguel, Fernando J ^a,b   Pajares, María J ^a,c,d   Martínez Terroba, Elena ^a,c   Ajona, Daniel ^a,b,d   Morales, Xabier ^a   Sharma, Ravi D ^b   Pardo, Francisco J ^e   Rouzaut, Ana ^a,b,d   Rubio, Angel ^b   Montuenga, Luis M ^a,c,d   Pio, Ruben ^a,b,d  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c UNIVERSITY OF NAVARRA   (Spain)

^d IdiSNA Navarra Institute for Health Research   (Spain)

^e UNIVERSITY CLINIC OF NAVARRA   (Spain)

Author keywords

Alternative splicing; ESYT2; Non small cell lung cancer; QKI

Indexed keywords

ACTIN; ALPHA TUBULIN; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; CD34 ANTIGEN; CLATHRIN; COLLAGEN TYPE 12; ESYT2 PROTEIN; F ACTIN; FBXO18 PROTEIN; FLI1 PROTEIN; KIF13A PROTEIN; MESSENGER RNA; POTASSIUM CHLORIDE COTRANSPORTER 1; PROTEIN KINASE WNK1; QUAKING; RAC1 PROTEIN; RNA BINDING PROTEIN; SCAFFOLD PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG; QKI PROTEIN, HUMAN; SYNAPTOTAGMIN;

ALTERNATIVE RNA SPLICING; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; DISEASE FREE SURVIVAL; DOWN REGULATION; GENE EXPRESSION; HUMAN; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; NON SMALL CELL LUNG CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; CYTOSKELETON; EXON; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; METABOLISM; PROGNOSIS;

ALTERNATIVE SPLICING; CARCINOMA, NON-SMALL-CELL LUNG; CLATHRIN; CYTOSKELETON; DOWN-REGULATION; EXONS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; PROGNOSIS; RNA-BINDING PROTEINS; SYNAPTOTAGMINS;

EID: 84995618086     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2016.08.001     Document Type: Article

References (83)

1. Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A.A., Kim, S., Wilson, C.J., Lehar, J., Kryukov, G.V., Sonkin, D., Reddy, A., Liu, M., Murray, L., Berger, M.F., Monahan, J.E., Morais, P., Meltzer, J., Korejwa, A., Jane-Valbuena, J., Mapa, F.A., Thibault, J., Bric-Furlong, E., Raman, P., Shipway, A., Engels, I.H., Cheng, J., Yu, G.K., Yu, J., Aspesi, P. Jr., de Silva, M., Jagtap, K., Jones, M.D., Wang, L., Hatton, C., Palescandolo, E., Gupta, S., Mahan, S., Sougnez, C., Onofrio, R.C., Liefeld, T., MacConaill, L., Winckler, W., Reich, M., Li, N., Mesirov, J.P., Gabriel, S.B., Getz, G., Ardlie, K., Chan, V., Myer, V.E., Weber, B.L., Porter, J., Warmuth, M., Finan, P., Harris, J.L., Meyerson, M., Golub, T.R., Morrissey, M.P., Sellers, W.R., Schlegel, R., Garraway, L.A., The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483 (2012), 603–607.
2. Bechara, E.G., Sebestyen, E., Bernardis, I., Eyras, E., Valcarcel, J., RBM5, 6, and 10 differentially regulate NUMB alternative splicing to control cancer cell proliferation. Mol. Cel. 52 (2013), 720–733.
3. Bezanilla, M., Gladfelter, A.S., Kovar, D.R., Lee, W.L., Cytoskeletal dynamics: a view from the membrane. J. Cel. Biol. 209 (2015), 329–337.
4. Biamonti, G., Catillo, M., Pignataro, D., Montecucco, A., Ghigna, C., The alternative splicing side of cancer. Semin. Cel. Dev. Biol. 32 (2014), 30–36.
5. Bian, Y., Wang, L., Lu, H., Yang, G., Zhang, Z., Fu, H., Lu, X., Wei, M., Sun, J., Zhao, Q., Dong, G., Lu, Z., Downregulation of tumor suppressor QKI in gastric cancer and its implication in cancer prognosis. Biochem. Biophys. Res. Commun. 422 (2012), 187–193.
6. Bria, E., Di Modugno, F., Sperduti, I., Iapicca, P., Visca, P., Alessandrini, G., Antoniani, B., Pilotto, S., Ludovini, V., Vannucci, J., Bellezza, G., Sidoni, A., Tortora, G., Radisky, D.C., Crino, L., Cognetti, F., Facciolo, F., Mottolese, M., Milella, M., Nistico, P., Prognostic impact of alternative splicing-derived hMENA isoforms in resected, node-negative, non-small-cell lung cancer. Oncotarget 5 (2014), 11054–11063.
7. Brooks, A.N., Choi, P.S., de Waal, L., Sharifnia, T., Imielinski, M., Saksena, G., Pedamallu, C.S., Sivachenko, A., Rosenberg, M., Chmielecki, J., Lawrence, M.S., DeLuca, D.S., Getz, G., Meyerson, M., A pan-cancer analysis of transcriptome changes associated with somatic mutations in U2AF1 reveals commonly altered splicing events. PloS One, 9, 2014, e87361.
8. Brosseau, J.P., Lucier, J.F., Nwilati, H., Thibault, P., Garneau, D., Gendron, D., Durand, M., Couture, S., Lapointe, E., Prinos, P., Klinck, R., Perreault, J.P., Chabot, B., Abou-Elela, S., Tumor microenvironment-associated modifications of alternative splicing. RNA 20 (2014), 189–201.
9. Cancer Genome Atlas Research Network, Comprehensive molecular profiling of lung adenocarcinoma. Nature 511 (2014), 543–550.
10. Conn, S.J., Pillman, K.A., Toubia, J., Conn, V.M., Salmanidis, M., Phillips, C.A., Roslan, S., Schreiber, A.W., Gregory, P.A., Goodall, G.J., The RNA binding protein quaking regulates formation of circRNAs. Cell 160 (2015), 1125–1134.
11. Chen, J., Weiss, W.A., Alternative splicing in cancer: implications for biology and therapy. Oncogene 34 (2015), 1–14.
12. Chen, L., Bush, S.J., Tovar-Corona, J.M., Castillo-Morales, A., Urrutia, A.O., Correcting for differential transcript coverage reveals a strong relationship between alternative splicing and organism complexity. Mol. Biol. Evol. 31 (2014), 1402–1413.
13. Christmas, P., Jones, J.P., Patten, C.J., Rock, D.A., Zheng, Y., Cheng, S.M., Weber, B.M., Carlesso, N., Scadden, D.T., Rettie, A.E., Soberman, R.J., Alternative splicing determines the function of CYP4F3 by switching substrate specificity. J. Biol. Chem. 276 (2001), 38166–38172.
14. Danan-Gotthold, M., Golan-Gerstl, R., Eisenberg, E., Meir, K., Karni, R., Levanon, E.Y., Identification of recurrent regulated alternative splicing events across human solid tumors. Nucleic Acids Res. 43 (2015), 5130–5144.
15. de Bruin, R.G., Shiue, L., Prins, J., de Boer, H.C., Singh, A., Fagg, W.S., van Gils, J.M., Duijs, J.M., Katzman, S., Kraaijeveld, A.O., Bohringer, S., Leung, W.Y., Kielbasa, S.M., Donahue, J.P., van der Zande, P.H., Sijbom, R., van Alem, C.M., Bot, I., van Kooten, C., Jukema, J.W., Van Esch, H., Rabelink, T.J., Kazan, H., Biessen, E.A., Ares, M. Jr., van Zonneveld, A.J., van der Veer, E.P., Quaking promotes monocyte differentiation into pro-atherogenic macrophages by controlling pre-mRNA splicing and gene expression. Nat. Commun., 7, 2016, 10846.
16. de Miguel, F.J., Sharma, R.D., Pajares, M.J., Montuenga, L.M., Rubio, A., Pio, R., Identification of alternative splicing events regulated by the oncogenic factor SRSF1 in lung cancer. Cancer Res. 74 (2014), 1105–1115.
17. Di Modugno, F., Iapicca, P., Boudreau, A., Mottolese, M., Terrenato, I., Perracchio, L., Carstens, R.P., Santoni, A., Bissell, M.J., Nistico, P., Splicing program of human MENA produces a previously undescribed isoform associated with invasive, mesenchymal-like breast tumors. Proc. Natl. Acad. Sci. United States America 109 (2012), 19280–19285.
18. Dolatshad, H., Pellagatti, A., Fernandez-Mercado, M., Yip, B.H., Malcovati, L., Attwood, M., Przychodzen, B., Sahgal, N., Kanapin, A.A., Lockstone, H., Scifo, L., Vandenberghe, P., Papaemmanuil, E., Smith, C.W., Campbell, P.J., Ogawa, S., Maciejewski, J.P., Cazzola, M., Savage, K.I., Boultwood, J., Disruption of SF3B1 results in deregulated expression and splicing of key genes and pathways in myelodysplastic syndrome hematopoietic stem and progenitor cells. Leukemia 29 (2015), 1092–1103.
19. Dooley, A.L., Winslow, M.M., Chiang, D.Y., Banerji, S., Stransky, N., Dayton, T.L., Snyder, E.L., Senna, S., Whittaker, C.A., Bronson, R.T., Crowley, D., Barretina, J., Garraway, L., Meyerson, M., Jacks, T., Nuclear factor I/B is an oncogene in small cell lung cancer. Genes Dev. 25 (2011), 1470–1475.
20. Ebersole, T.A., Chen, Q., Justice, M.J., Artzt, K., The quaking gene product necessary in embryogenesis and myelination combines features of RNA binding and signal transduction proteins. Nat. Genet. 12 (1996), 260–265.
21. Feliciano, D., Di Pietro, S.M., SLAC, a complex between Sla1 and Las17, regulates actin polymerization during clathrin-mediated endocytosis. Mol. Biol. Cel. 23 (2012), 4256–4272.
22. Fernandez-Busnadiego, R., Saheki, Y., De Camilli, P., Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites. Proc. Natl. Acad. Sci. United States America 112 (2015), E2004–E2013.
23. Fielding, A.B., Willox, A.K., Okeke, E., Royle, S.J., Clathrin-mediated endocytosis is inhibited during mitosis. Proc. Natl. Acad. Sci. United States America 109 (2012), 6572–6577.
24. Fu, X.D., Ares, M. Jr., Context-dependent control of alternative splicing by RNA-binding proteins. Nature Rev. Genetics 15 (2014), 689–701.
25. Galarneau, A., Richard, S., Target RNA motif and target mRNAs of the Quaking STAR protein. Nat. Struct. Mol. Biol. 12 (2005), 691–698.
26. Gamazon, E.R., Stranger, B.E., Genomics of alternative splicing: evolution, development and pathophysiology. Hum. Genet. 133 (2014), 679–687.
27. Giordano, F., Saheki, Y., Idevall-Hagren, O., Colombo, S.F., Pirruccello, M., Milosevic, I., Gracheva, E.O., Bagriantsev, S.N., Borgese, N., De Camilli, P., PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153 (2013), 1494–1509.
28. Gout, S., Brambilla, E., Boudria, A., Drissi, R., Lantuejoul, S., Gazzeri, S., Eymin, B., Abnormal expression of the pre-mRNA splicing regulators SRSF1, SRSF2, SRPK1 and SRPK2 in non small cell lung carcinoma. PloS One, 7, 2012, e46539.
29. Gridelli, C., Rossi, A., Carbone, D.P., Guarize, J., Karachaliou, N., Mok, T., Petrella, F., Spaggiari, L., Rosell, R., Non-small-cell lung cancer. Nat. Rev. Dis. Primers, 15009, 2015.
30. Gross, S.R., Actin binding proteins: their ups and downs in metastatic life. Cell Adhes. Migr. 7 (2013), 199–213.
31. Hall, M.P., Nagel, R.J., Fagg, W.S., Shiue, L., Cline, M.S., Perriman, R.J., Donohue, J.P., Ares, M. Jr., Quaking and PTB control overlapping splicing regulatory networks during muscle cell differentiation. RNA 19 (2013), 627–638.
32. He, B., Gao, S.Q., Huang, L.D., Huang, Y.H., Zhang, Q.Y., Zhou, M.T., Shi, H.Q., Song, Q.T., Shan, Y.F., MicroRNA-155 promotes the proliferation and invasion abilities of colon cancer cells by targeting quaking. Mol. Med. Rep. 11 (2015), 2355–2359.
33. Huang da, W., Sherman, B.T., Lempicki, R.A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4 (2009), 44–57.
34. Imielinski, M., Berger, A.H., Hammerman, P.S., Hernandez, B., Pugh, T.J., Hodis, E., Cho, J., Suh, J., Capelletti, M., Sivachenko, A., Sougnez, C., Auclair, D., Lawrence, M.S., Stojanov, P., Cibulskis, K., Choi, K., de Waal, L., Sharifnia, T., Brooks, A., Greulich, H., Banerji, S., Zander, T., Seidel, D., Leenders, F., Ansen, S., Ludwig, C., Engel-Riedel, W., Stoelben, E., Wolf, J., Goparju, C., Thompson, K., Winckler, W., Kwiatkowski, D., Johnson, B.E., Janne, P.A., Miller, V.A., Pao, W., Travis, W.D., Pass, H.I., Gabriel, S.B., Lander, E.S., Thomas, R.K., Garraway, L.A., Getz, G., Meyerson, M., Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 150 (2012), 1107–1120.
35. Jaffe, A.B., Hall, A., Rho GTPases in transformation and metastasis. Adv. Cancer Res. 84 (2002), 57–80.
36. Jean, S., Mikryukov, A., Tremblay, M.G., Baril, J., Guillou, F., Bellenfant, S., Moss, T., Extended-synaptotagmin-2 mediates FGF receptor endocytosis and ERK activation in vivo. Developmental Cel. 19 (2010), 426–439.
37. Jean, S., Tremblay, M.G., Herdman, C., Guillou, F., Moss, T., The endocytic adapter E-Syt2 recruits the p21 GTPase activated kinase PAK1 to mediate actin dynamics and FGF signalling. Biol. Open 1 (2012), 731–738.
38. Jensen, M.A., Wilkinson, J.E., Krainer, A.R., Splicing factor SRSF6 promotes hyperplasia of sensitized skin. Nat. Struct. Mol. Biol. 21 (2014), 189–197.
39. 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. Nat. Struct. Mol. Biol. 14 (2007), 185–193.
40. Labelle, M., Hynes, R.O., The initial hours of metastasis: the importance of cooperative host-tumor cell interactions during hematogenous dissemination. Cancer Discov. 2 (2012), 1091–1099.
41. Langer, W., Sohler, F., Leder, G., Beckmann, G., Seidel, H., Grone, J., Hummel, M., Sommer, A., Exon array analysis using re-defined probe sets results in reliable identification of alternatively spliced genes in non-small cell lung cancer. BMC Genom., 11, 2010, 676.
42. Larocque, D., Fragoso, G., Huang, J., Mushynski, W.E., Loignon, M., Richard, S., Almazan, G., The QKI-6 and QKI-7 RNA binding proteins block proliferation and promote Schwann cell myelination. PloS One, 4, 2009, e5867.
43. Misquitta-Ali, C.M., Cheng, E., O'Hanlon, D., Liu, N., McGlade, C.J., Tsao, M.S., Blencowe, B.J., Global profiling and molecular characterization of alternative splicing events misregulated in lung cancer. Mol. Cell. Biol. 31 (2011), 138–150.
44. Mountain, C.F., Revisions in the International system for staging lung Cancer. Chest 111 (1997), 1710–1717.
45. Nguewa, P.A., Agorreta, J., Blanco, D., Lozano, M.D., Gomez-Roman, J., Sanchez, B.A., Valles, I., Pajares, M.J., Pio, R., Rodriguez, M.J., Montuenga, L.M., Calvo, A., Identification of importin 8 (IPO8) as the most accurate reference gene for the clinicopathological analysis of lung specimens. BMC Mol. Biol., 9, 2008, 103.
46. Novikov, L., Park, J.W., Chen, H., Klerman, H., Jalloh, A.S., Gamble, M.J., QKI-mediated alternative splicing of the histone variant MacroH2A1 regulates cancer cell proliferation. Mol. Cell. Biol. 31 (2011), 4244–4255.
47. Olson, M.F., Sahai, E., The actin cytoskeleton in cancer cell motility. Clin. Exp. Metastasis 26 (2009), 273–287.
48. Oltean, S., Bates, D.O., Hallmarks of alternative splicing in cancer. Oncogene 33 (2014), 5311–5318.
49. Padgett, R.A., New connections between splicing and human disease. Trends Genetics: TIG 28 (2012), 147–154.
50. Pajares, M.J., Agorreta, J., Larrayoz, M., Vesin, A., Ezponda, T., Zudaire, I., Torre, W., Lozano, M.D., Brambilla, E., Brambilla, C., Wistuba II, Behrens, C., Timsit, J.F., Pio, R., Field, J.K., Montuenga, L.M., Expression of tumor-derived vascular endothelial growth factor and its receptors is associated with outcome in early squamous cell carcinoma of the lung. J. Clin. Oncol. 30 (2012), 1129–1136.
51. Pio, R., Blanco, D., Pajares, M.J., Aibar, E., Durany, O., Ezponda, T., Agorreta, J., Gomez-Roman, J., Anton, M.A., Rubio, A., Lozano, M.D., Lopez-Picazo, J.M., Subirada, F., Maes, T., Montuenga, L.M., Development of a novel splice array platform and its application in the identification of alternative splice variants in lung cancer. BMC Genom., 11, 2010, 352.
52. Pio, R., Montuenga, L.M., Alternative splicing in lung cancer. J. Thorac. Oncol. 4 (2009), 674–678.
53. Pio, R., Zudaire, I., Pino, I., Castano, Z., Zabalegui, N., Vicent, S., Garcia-Amigot, F., Odero, M.D., Lozano, M.D., Garcia-Foncillas, J., Calasanz, M.J., Montuenga, L.M., Alpha CP-4, encoded by a putative tumor suppressor gene at 3p21, but not its alternative splice variant alpha CP-4a, is underexpressed in lung cancer. Cancer Res. 64 (2004), 4171–4179.
54. Saccomanno, L., Loushin, C., Jan, E., Punkay, E., Artzt, K., Goodwin, E.B., The STAR protein QKI-6 is a translational repressor. Proc. Natl. Acad. Sci. United States America 96 (1999), 12605–12610.
55. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P., Cardona, A., Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
56. Sebestyen, E., Zawisza, M., Eyras, E., Detection of recurrent alternative splicing switches in tumor samples reveals novel signatures of cancer. Nucleic Acids Res. 43 (2015), 1345–1356.
57. Shirai, C.L., Ley, J.N., White, B.S., Kim, S., Tibbitts, J., Shao, J., Ndonwi, M., Wadugu, B., Duncavage, E.J., Okeyo-Owuor, T., Liu, T., Griffith, M., McGrath, S., Magrini, V., Fulton, R.S., Fronick, C., O'Laughlin, M., Graubert, T.A., Walter, M.J., Mutant U2AF1 expression alters hematopoiesis and pre-mRNA splicing in vivo. Cancer Cell 27 (2015), 631–643.
58. Spiering, D., Hodgson, L., Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adhes. Migration 5 (2011), 170–180.
59. Tanaka, N., Yoshida, H., Suzuki, Y., Harigaya, K., Relative expression of hMena11a and hMenaINV splice isoforms is a useful biomarker in development and progression of human breast carcinoma. Int. J. Oncol. 45 (2014), 1921–1928.
60. Travis, W.D., Brambilla, E., Muller-Hermelink, H.K., Harris, C.C., Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart. 2004, IARC Press, Lyon.
61. UniProt, C., UniProt: a hub for protein information. Nucleic Acids Res. 43 (2015), D204–D212.
62. Valles, I., Pajares, M.J., Segura, V., Guruceaga, E., Gomez-Roman, J., Blanco, D., Tamura, A., Montuenga, L.M., Pio, R., Identification of novel deregulated RNA metabolism-related genes in non-small cell lung cancer. PloS One, 7, 2012, e42086.
63. Vega, F.M., Ridley, A.J., Rho GTPases in cancer cell biology. FEBS Lett. 582 (2008), 2093–2101.
64. Wan, Y., Wu, C.J., SF3B1 mutations in chronic lymphocytic leukemia. Blood 121 (2013), 4627–4634.
65. Wang, Y., Chen, D., Qian, H., Tsai, Y.S., Shao, S., Liu, Q., Dominguez, D., Wang, Z., The splicing factor RBM4 controls apoptosis, proliferation, and migration to suppress tumor progression. Cancer Cell 26 (2014), 374–389.
66. Wang, Y., Dong, Q., Miao, Y., Fu, L., Lin, X., Wang, E., Clinical significance and biological roles of SPAG9 overexpression in non-small cell lung cancer. Lung Cancer 81 (2013), 266–272.
67. Wang, Y., Gogol-Doring, A., Hu, H., Frohler, S., Ma, Y., Jens, M., Maaskola, J., Murakawa, Y., Quedenau, C., Landthaler, M., Kalscheuer, V., Wieczorek, D., Wang, Y., Hu, Y., Chen, W., Integrative analysis revealed the molecular mechanism underlying RBM10-mediated splicing regulation. EMBO Mol. Med. 5 (2013), 1431–1442.
68. Wang, Y., Vogel, G., Yu, Z., Richard, S., The QKI-5 and QKI-6 RNA binding proteins regulate the expression of microRNA 7 in glial cells. Mol. Cell. Biol. 33 (2013), 1233–1243.
69. Wen, J., Toomer, K.H., Chen, Z., Cai, X., Genome-wide analysis of alternative transcripts in human breast cancer. Breast Cancer Res. Treat. 151 (2015), 295–307.
70. Wolf, K., Mazo, I., Leung, H., Engelke, K., von Andrian, U.H., Deryugina, E.I., Strongin, A.Y., Brocker, E.B., Friedl, P., Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cel. Biol. 160 (2003), 267–277.
71. Wyckoff, J.B., Pinner, S.E., Gschmeissner, S., Condeelis, J.S., Sahai, E., ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr. Biol. CB 16 (2006), 1515–1523.
72. Xi, L., Feber, A., Gupta, V., Wu, M., Bergemann, A.D., Landreneau, R.J., Litle, V.R., Pennathur, A., Luketich, J.D., Godfrey, T.E., Whole genome exon arrays identify differential expression of alternatively spliced, cancer-related genes in lung cancer. Nucleic Acids Res. 36 (2008), 6535–6547.
73. Xie, J., Differential evolution of signal-responsive RNA elements and upstream factors that control alternative splicing. Cell Mol. Life Sci.: CMLS 71 (2014), 4347–4360.
74. Yan, Q., Lou, G., Qian, Y., Qin, B., Xu, X., Wang, Y., Liu, Y., Dong, X., SPAG9 is involved in hepatocarcinoma cell migration and invasion via modulation of ELK1 expression. OncoTargets Ther. 9 (2016), 1067–1075.
75. Yang, G., Fu, H., Zhang, J., Lu, X., Yu, F., Jin, L., Bai, L., Huang, B., Shen, L., Feng, Y., Yao, L., Lu, Z., RNA-binding protein quaking, a critical regulator of colon epithelial differentiation and a suppressor of colon cancer. Gastroenterology 138 (2010), 231–240 e1-5.
76. Yang, X., Zhou, W., Liu, S., SPAG9 controls the cell motility, invasion and angiogenesis of human osteosarcoma cells. Exp. Ther. Med. 11 (2016), 637–644.
77. Yang, Y., Park, J.W., Bebee, T.W., Warzecha, C.C., Guo, Y., Shang, X., Xing, Y., Carstens, R.P., Determination of a comprehensive alternative splicing regulatory network and combinatorial regulation by key factors during the epithelial-to-mesenchymal transition. Mol. Cell. Biol. 36 (2016), 1704–1719.
78. Yao, Y., Gu, X., Liu, H., Wu, G., Yuan, D., Yang, X., Song, Y., Metadherin regulates proliferation and metastasis via actin cytoskeletal remodelling in non-small cell lung cancer. Br. J. Cancer 111 (2014), 355–364.
79. Yi, F., Ni, W., Liu, W., Pan, X., Han, X., Yang, L., Kong, X., Ma, R., Chang, R., SPAG9 is overexpressed in human astrocytoma and promotes cell proliferation and invasion. Tumour Biol. J. Int. Soc. Oncodevelopmental Biol. Med. 34 (2013), 2849–2855.
80. Zhang, C., Zhang, Z., Castle, J., Sun, S., Johnson, J., Krainer, A.R., Zhang, M.Q., Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2. Genes Dev. 22 (2008), 2550–2563.
81. Zhang, J., Lieu, Y.K., Ali, A.M., Penson, A., Reggio, K.S., Rabadan, R., Raza, A., Mukherjee, S., Manley, J.L., Disease-associated mutation in SRSF2 misregulates splicing by altering RNA-binding affinities. Proc. Natl. Acad. Sci. United States America 112 (2015), E4726–E4734.
82. Zhao, Y., Zhang, G., Wei, M., Lu, X., Fu, H., Feng, F., Wang, S., Lu, W., Wu, N., Lu, Z., Yuan, J., The tumor suppressing effects of QKI-5 in prostate cancer: a novel diagnostic and prognostic protein. Cancer Biol. Ther. 15 (2014), 108–118.
83. Zong, F.Y., Fu, X., Wei, W.J., Luo, Y.G., Heiner, M., Cao, L.J., Fang, Z., Fang, R., Lu, D., Ji, H., Hui, J., The RNA-binding protein QKI suppresses cancer-associated aberrant splicing. PLoS Genet., 10, 2014, e1004289.