WT1 Mutants Reveal SRPK1 to Be a Downstream Angiogenesis Target by Altering VEGF Splicing

Cancer Cell

Volumn 20, Issue 6, 2011, Pages 768-780

  Amin, Elianna M ^a,b   Oltean, Sebastian ^b   Hua, Jing ^b   Gammons, Melissa V R ^b   Hamdollah Zadeh, Maryam ^b   Welsh, Gavin I ^c   Cheung, Man Kim ^a   Ni, Lan ^c   Kase, Satoru ^d   Rennel, Emma S ^b   Symonds, Kirsty E ^b   Nowak, Dawid G ^b   Royer Pokora, Brigitte ^e   Saleem, Moin A ^c   Hagiwara, Masatoshi ^f   Schumacher, Valérie A ^e,g,h   Harper, Steven J ^b   Hinton, David R ^d   Bates, David O ^b   Ladomery, Michael R ^a  

^a UNIVERSITY OF THE WEST OF ENGLAND   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e HEINRICH HEINE UNIVERSITY   (Germany)

^f KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g BOSTON CHILDREN S HOSPITAL   (United States)

^h HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENYS DRASH SYNDROME; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE MUTATION; GENE REPRESSION; GONAD DEVELOPMENT; GONAD DYSFUNCTION; HUMAN; HUMAN CELL; KIDNEY FAILURE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROCESSING; SPLICING DEFECT; SRPK 1 GENE; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; WILD TYPE;

EID: 83455263848     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2011.10.016     Document Type: Article

References (50)

1. Artac R.A., McFee R.M., Smith R.A., Baltes-Breitwisch M.M., Clopton D.T., Cupp A.S. Neutralization of vascular endothelial growth factor antiangiogenic isoforms is more effective than treatment with proangiogenic isoforms in stimulating vascular development and follicle progression in the perinatal rat ovary. Biol. Reprod. 2009, 81:978-988.
2. Ballmer-Hofer K., Andersson A.E., Ratcliffe L.E., Berger P. Neuropilin-1 promotes VEGFR-2 trafficking through Rab11 vesicles thereby specifying signal output. Blood 2011, 118:816-826.
3. Baltes-Breitwisch M.M., Artac R.A., Bott R.C., McFee R.M., Kerl J.G., Clopton D.T., Cupp A.S. Neutralization of vascular endothelial growth factor antiangiogenic isoforms or administration of proangiogenic isoforms stimulates vascular development in the rat testis. Reproduction 2010, 140:319-329.
4. Bates D.O., Cui T.G., Doughty J.M., Winkler M., Sugiono M., Shields J.D., Peat D., Gillatt D., Harper S.J. VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma. Cancer Res. 2002, 62:4123-4131.
5. Blann A.D., Li J.L., Li C., Kumar S. Increased serum VEGF in 13 children with Wilms' tumour falls after surgery but rising levels predict poor prognosis. Cancer Lett. 2001, 173:183-186.
6. Bonnal S., Martínez C., Förch P., Bachi A., Wilm M., Valcárcel J. RBM5/Luca-15/H37 regulates Fas alternative splice site pairing after exon definition. Mol. Cell 2008, 32:81-95.
7. Bor Y.C., Swartz J., Morrison A., Rekosh D., Ladomery M., Hammarskjöld M.L. The Wilms' tumor 1 (WT1) gene (+KTS isoform) functions with a CTE to enhance translation from an unspliced RNA with a retained intron. Genes Dev. 2006, 20:1597-1608.
8. Cébe Suarez S., Pieren M., Cariolato L., Arn S., Hoffmann U., Bogucki A., Manlius C., Wood J., Ballmer-Hofer K. A VEGF-A splice variant defective for heparan sulfate and neuropilin-1 binding shows attenuated signaling through VEGFR-2. Cell. Mol. Life Sci. 2006, 63:2067-2077.
9. Davies R., Moore A., Schedl A., Bratt E., Miyahawa K., Ladomery M., Miles C., Menke A., van Heyningen V., Hastie N. Multiple roles for the Wilms' tumor suppressor, WT1. Cancer Res. 1999, 59:1747s-1750s. discussion 1751s.
10. Davies R.C., Calvio C., Bratt E., Larsson S.H., Lamond A.I., Hastie N.D. WT1 interacts with the splicing factor U2AF65 in an isoform-dependent manner and can be incorporated into spliceosomes. Genes Dev. 1998, 12:3217-3225.
11. Denys P., Malvaux P., Van Den Berghe H., Tanghe W., Proesmans W. [Association of an anatomo-pathological syndrome of male pseudohermaphroditism, Wilms' tumor, parenchymatous nephropathy and XX/XY mosaicism]. Arch. Fr. Pediatr. 1967, 24:729-739.
12. Díaz R., Peña C., Silva J., Lorenzo Y., García V., García J.M., Sánchez A., Espinosa P., Yuste R., Bonilla F., Domínguez G. p73 Isoforms affect VEGF, VEGF165b and PEDF expression in human colorectal tumors: VEGF165b downregulation as a marker of poor prognosis. Int. J. Cancer 2008, 123:1060-1067.
13. Drash A., Sherman F., Hartmann W.H., Blizzard R.M. A syndrome of pseudohermaphroditism, Wilms' tumor, hypertension, and degenerative renal disease. J. Pediatr. 1970, 76:585-593.
14. Fukuhara T., Hosoya T., Shimizu S., Sumi K., Oshiro T., Yoshinaka Y., Suzuki M., Yamamoto N., Herzenberg L.A., Herzenberg L.A., Hagiwara M. Utilization of host SR protein kinases and RNA-splicing machinery during viral replication. Proc. Natl. Acad. Sci. USA 2006, 103:11329-11333.
15. Ghosh A., Stewart D., Matlashewski G. Regulation of human p53 activity and cell localization by alternative splicing. Mol. Cell. Biol. 2004, 24:7987-7997.
16. Gonçalves V., Matos P., Jordan P. Antagonistic SR proteins regulate alternative splicing of tumor-related Rac1b downstream of the PI3-kinase and Wnt pathways. Hum. Mol. Genet. 2009, 18:3696-3707.
17. Graham K., Li W., Williams B.R., Fraizer G. Vascular endothelial growth factor (VEGF) is suppressed in WT1-transfected LNCaP cells. Gene Expr. 2006, 13:1-14.
18. Haber D.A., Sohn R.L., Buckler A.J., Pelletier J., Call K.M., Housman D.E. Alternative splicing and genomic structure of the Wilms tumor gene WT1. Proc. Natl. Acad. Sci. USA 1991, 88:9618-9622.
19. Harper S.J., Bates D.O. VEGF-A splicing: the key to anti-angiogenic therapeutics?. Nat. Rev. Cancer 2008, 8:880-887.
20. Hayes G.M., Carrigan P.E., Miller L.J. Serine-arginine protein kinase 1 overexpression is associated with tumorigenic imbalance in mitogen-activated protein kinase pathways in breast, colonic, and pancreatic carcinomas. Cancer Res. 2007, 67:2072-2080.
21. Hohenstein P., Hastie N.D. The many facets of the Wilms' tumour gene, WT1. Hum. Mol. Genet. 2006, 15(Spec No 2):R196-R201.
22. Houck K.A., Ferrara N., Winer J., Cachianes G., Li B., Leung D.W. The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol. 1991, 5:1806-1814.
23. Hua J., Spee C., Kase S., Rennel E.S., Magnussen A.L., Qiu Y., Varey A., Dhayade S., Churchill A.J., Harper S.J., et al. Recombinant human VEGF165b inhibits experimental choroidal neovascularization. Invest. Ophthalmol. Vis. Sci. 2010, 51:4282-4288.
24. Hurwitz H., Fehrenbacher L., Novotny W., Cartwright T., Hainsworth J., Heim W., Berlin J., Baron A., Griffing S., Holmgren E., et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 2004, 350:2335-2342.
25. 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. 2007, 14:185-193.
26. Kawamura H., Li X., Harper S.J., Bates D.O., Claesson-Welsh L. Vascular endothelial growth factor (VEGF)-A165b is a weak in vitro agonist for VEGF receptor-2 due to lack of coreceptor binding and deficient regulation of kinase activity. Cancer Res. 2008, 68:4683-4692.
27. Koesters R., Linnebacher M., Coy J.F., Germann A., Schwitalle Y., Findeisen P., von Knebel Doeberitz M. WT1 is a tumor-associated antigen in colon cancer that can be recognized by in vitro stimulated cytotoxic T cells. Int. J. Cancer 2004, 109:385-392.
28. Konopatskaya O., Churchill A.J., Harper S.J., Bates D.O., Gardiner T.A. VEGF165b, an endogenous C-terminal splice variant of VEGF, inhibits retinal neovascularization in mice. Mol. Vis. 2006, 12:626-632.
29. Krishnakumar S., Mohan A., Kandalam M., Ramkumar H.L., Venkatesan N., Das R.R. SRPK1: a cisplatin sensitive protein expressed in retinoblastoma. Pediatr. Blood Cancer 2008, 50:402-406.
30. Manetti M., Guiducci S., Romano E., Ceccarelli C., Bellando-Randone S., Conforti M.L., Ibba-Manneschi L., Matucci-Cerinic M. Overexpression of VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, leads to insufficient angiogenesis in patients with systemic sclerosis. Circ. Res. 2011, 109:e14-e26.
31. Merdzhanova G., Gout S., Keramidas M., Edmond V., Coll J.L., Brambilla C., Brambilla E., Gazzeri S., Eymin B. The transcription factor E2F1 and the SR protein SC35 control the ratio of pro-angiogenic versus antiangiogenic isoforms of vascular endothelial growth factor-A to inhibit neovascularization in vivo. Oncogene 2010, 29:5392-5403.
32. Morrison A.A., Viney R.L., Ladomery M.R. The post-transcriptional roles of WT1, a multifunctional zinc-finger protein. Biochim. Biophys. Acta 2008, 1785:55-62.
33. Natoli T.A., Liu J., Eremina V., Hodgens K., Li C., Hamano Y., Mundel P., Kalluri R., Miner J.H., Quaggin S.E., Kreidberg J.A. A mutant form of the Wilms' tumor suppressor gene WT1 observed in Denys-Drash syndrome interferes with glomerular capillary development. J. Am. Soc. Nephrol. 2002, 13:2058-2067.
34. Nowak D.G., Woolard J., Amin E.M., Konopatskaya O., Saleem M.A., Churchill A.J., Ladomery M.R., Harper S.J., Bates D.O. Expression of pro- and anti-angiogenic isoforms of VEGF is differentially regulated by splicing and growth factors. J. Cell Sci. 2008, 121:3487-3495.
35. Nowak D.G., Amin E.M., Rennel E.S., Hoareau-Aveilla C., Gammons M., Damodoran G., Hagiwara M., Harper S.J., Woolard J., Ladomery M.R., Bates D.O. Regulation of vascular endothelial growth factor (VEGF) splicing from pro-angiogenic to anti-angiogenic isoforms: a novel therapeutic strategy for angiogenesis. J. Biol. Chem. 2010, 285:5532-5540.
36. Perrin R.M., Konopatskaya O., Qiu Y., Harper S., Bates D.O., Churchill A.J. Diabetic retinopathy is associated with a switch in splicing from anti- to pro-angiogenic isoforms of vascular endothelial growth factor. Diabetologia 2005, 48:2422-2427.
37. Qiu Y., Bevan H., Weeraperuma S., Wratting D., Murphy D., Neal C.R., Bates D.O., Harper S.J. Mammary alveolar development during lactation is inhibited by the endogenous antiangiogenic growth factor isoform, VEGF165b. FASEB J. 2008, 22:1104-1112.
38. Qiu Y., Ferguson J., Oltean S., Neal C.R., Kaura A., Bevan H., Wood E., Sage L.M., Lanati S., Nowak D.G., et al. Overexpression of VEGF165b in podocytes reduces glomerular permeability. J. Am. Soc. Nephrol. 2010, 21:1498-1509.
39. 165b inhibits human tumour growth in mice. Br. J. Cancer 2008, 98:1250-1257.
40. xxxb family of VEGF-A splice isoforms, inhibits neovascularisation and tumour growth in vivo. Br. J. Cancer 2009, 101:1183-1193.
41. Sanford J.R., Ellis J.D., Cazalla D., Cáceres J.F. Reversible phosphorylation differentially affects nuclear and cytoplasmic functions of splicing factor 2/alternative splicing factor. Proc. Natl. Acad. Sci. USA 2005, 102:15042-15047.
42. Sanford J.R., Coutinho P., Hackett J.A., Wang X., Ranahan W., Caceres J.F. Identification of nuclear and cytoplasmic mRNA targets for the shuttling protein SF2/ASF. PLoS ONE 2008, 3:e3369.
43. Schumacher V.A., Jeruschke S., Eitner F., Becker J.U., Pitschke G., Ince Y., Miner J.H., Leuschner I., Engers R., Everding A.S., et al. Impaired glomerular maturation and lack of VEGF165b in Denys-Drash syndrome. J. Am. Soc. Nephrol. 2007, 18:719-729.
44. Sköldenberg E.G., Christiansson J., Sandstedt B., Larsson A., Läckgren G., Christofferson R. Angiogenesis and angiogenic growth factors in Wilms tumor. J. Urol. 2001, 165:2274-2279.
45. 165b, an antiangiogenic VEGF-A isoform, binds and inhibits bevacizumab treatment in experimental colorectal carcinoma: balance of pro- and antiangiogenic VEGF-A isoforms has implications for therapy. Br. J. Cancer 2008, 98:1366-1379.
46. Viney R.L., Morrison A.A., van den Heuvel L.P., Ni L., Mathieson P.W., Saleem M.A., Ladomery M.R. A proteomic investigation of glomerular podocytes from a Denys-Drash syndrome patient with a mutation in the Wilms tumour suppressor gene WT1. Proteomics 2007, 7:804-815.
47. Woolard J., Wang W.Y., Bevan H.S., Qiu Y., Morbidelli L., Pritchard-Jones R.O., Cui T.G., Sugiono M., Waine E., Perrin R., et al. VEGF165b, an inhibitory vascular endothelial growth factor splice variant: mechanism of action, in vivo effect on angiogenesis and endogenous protein expression. Cancer Res. 2004, 64:7822-7835.
48. Woolard J., Bevan H.S., Harper S.J., Bates D.O. Molecular diversity of VEGF-A as a regulator of its biological activity. Microcirculation 2009, 16:572-592.
49. Yea S., Narla G., Zhao X., Garg R., Tal-Kremer S., Hod E., Villanueva A., Loke J., Tarocchi M., Akita K., et al. Ras promotes growth by alternative splicing-mediated inactivation of the KLF6 tumor suppressor in hepatocellular carcinoma. Gastroenterology 2008, 134:1521-1531.
50. Zhong X.Y., Ding J.H., Adams J.A., Ghosh G., Fu X.D. Regulation of SR protein phosphorylation and alternative splicing by modulating kinetic interactions of SRPK1 with molecular chaperones. Genes Dev. 2009, 23:482-495.