WT1 regulates angiogenesis in Ewing Sarcoma

Oncotarget

Volumn 5, Issue 9, 2014, Pages 2436-2449

  Katuri, Varalakshmi ^a   Gerber, Stephanie ^a   Qiu, Xiaofei ^b   McCarty, Gregory ^a   Goldstein, Seth D ^a   Hammers, Hans ^a   Montgomery, Elizabeth ^b   Chen, Allen R ^a   Loeb, David M ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alternative splicing; Tissue microarray; Transcriptional regulation; Tumor angiogenesis; Vascularity

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN RECEPTOR; GELATINASE B; SHORT HAIRPIN RNA; VASCULOTROPIN; WT1 PROTEIN; MESSENGER RNA; MMP9 PROTEIN, HUMAN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN; WT1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EWING SARCOMA; EWING SARCOMA CELL LINE; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR VASCULARIZATION; UPREGULATION; ANIMAL; APOPTOSIS; BONE TUMOR; CELL MOTION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; DRUG SCREENING; ENZYME IMMUNOASSAY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NONOBESE DIABETIC MOUSE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; TUMOR CELL CULTURE; VASCULARIZATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BONE NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED NOD; MICE, SCID; NEOVASCULARIZATION, PATHOLOGIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SARCOMA, EWING; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WT1 PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901227839     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1610     Document Type: Article

References (48)

1. Carpentieri DF, Nichols K, Chou PM, Matthews M, Pawel B and Huff D. The expression of WT1 in the differentiation of rhabdomyosarcoma from other pediatric small round blue cell tumors. Mod Pathol. 2002; 15(10):1080-1086.
2. Inoue K, Ogawa H, Sonoda Y, Kimura T, Sakabe H, Oka Y, Miyake S, Tamaki H, Oji Y, Yamagami T, Tatekawa T, Soma T, Kishimoto T and Sugiyama H. Aberrant overexpression of the Wilms tumor gene (WT1) in human leukemia. Blood. 1997; 89(4):1405-1412.
3. Loeb DM, Evron E, Patel CB, Sharma PM, Niranjan B, Buluwela L, Weitzman SA, Korz D and Sukumar S. Wilms' tumor suppressor gene (WT1) is expressed in primary breast tumors despite tumor-specific promoter methylation. Cancer Res. 2001; 61(3):921-925.
4. Miwa H, Beran M and Saunders GF. Expression of the Wilms' tumor gene (WT1) in human leukemias. Leukemia. 1992; 6(5):405-409.
5. Miyoshi Y, Ando A, Egawa C, Taguchi T, Tamaki Y, Tamaki H, Sugiyama H and Noguchi S. High expression of Wilms' tumor suppressor gene predicts poor prognosis in breast cancer patients. Clin Cancer Res. 2002; 8(5):1167-1171.
6. Sotobori T, Ueda T, Oji Y, Naka N, Araki N, Myoui A, Sugiyama H and Yoshikawa H. Prognostic significance of Wilms tumor gene (WT1) mRNA expression in soft tissue sarcoma. Cancer. 2006; 106(10):2233-2240.
7. Srivastava A, Fuchs B, Zhang K, Ruan M, Halder C, Mahlum E, Weber K, Bolander ME and Sarkar G. High WT1 expression is associated with very poor survival of patients with osteogenic sarcoma metastasis. Clin Cancer Res. 2006; 12(14 Pt 1):4237-4243.
8. Wagner KD, Wagner N, Bondke A, Nafz B, Flemming B, Theres H and Scholz H. The Wilms' tumor suppressor Wt1 is expressed in the coronary vasculature after myocardial infarction. Faseb J. 2002; 16(9):1117-1119.
9. Wagner N, Michiels JF, Schedl A and Wagner KD. The Wilms' tumour suppressor WT1 is involved in endothelial cell proliferation and migration: expression in tumour vessels in vivo. Oncogene. 2008; 27(26):3662-3672.
10. McCarty G, Awad O and Loeb DM. WT1 Protein Directly Regulates Expression of Vascular Endothelial Growth Factor and Is a Mediator of Tumor Response to Hypoxia. J Biol Chem. 2011; 286(51):43634-43643.
11. Haber DA, Sohn RL, Buckler AJ, Pelletier J, Call KM and Housman DE. Alternative splicing and genomic structure of the Wilms tumor gene WT1. Proc Natl Acad Sci U S A. 1991; 88(21):9618-9622.
12. Bruening W and Pelletier J. A non-AUG translational initiation event generates novel WT1 isoforms. J Biol Chem. 1996; 271(15):8646-8654.
13. Scharnhorst V, Dekker P, van der Eb AJ and Jochemsen AG. Internal translation initiation generates novel WT1 protein isoforms with distinct biological properties. J Biol Chem. 1999; 274(33):23456-23462.
14. Nakagama H, Heinrich G, Pelletier J and Housman DE. Sequence and structural requirements for high-affinity DNA binding by the WT1 gene product. Mol Cell Biol. 1995; 15(3):1489-1498.
15. Rauscher F, JF Morris, OE Tournay, DM Cook, and T Curran. Binding of the Wilms' tumor locus zinc finger protein to the EGR-1 consensus sequence. Science. 1990; 250:1259-1262.
16. Wang ZY, Qiu QQ, Enger KT and Deuel TF. A second transcriptionally active DNA-binding site for the Wilms tumor gene product, WT1. Proc Natl Acad Sci U S A. 1993; 90(19):8896-8900.
17. Drummond IA, Rupprecht HD, Rohwer-Nutter P, Lopez-Guisa JM, Madden SL, Rauscher FJ, 3rd and Sukhatme VP. DNA recognition by splicing variants of the Wilms' tumor suppressor, WT1. Mol Cell Biol. 1994; 14(6):3800-3809.
18. Reynolds PA, Smolen GA, Palmer RE, Sgroi D, Yajnik V, Gerald WL and Haber DA. Identification of a DNA-binding site and transcriptional target for the EWS-WT1(+KTS) oncoprotein. Genes Dev. 2003; 17(17):2094-2107.
19. Morrison AA, Venables JP, Dellaire G and Ladomery MR. The Wilms tumour suppressor protein WT1 (+KTS isoform) binds alpha-actinin 1 mRNA via its zinc-finger domain. Biochem Cell Biol. 2006; 84(5):789-798.
20. Amin EM, Oltean S, Hua J, Gammons MV, Hamdollah-Zadeh M, Welsh GI, Cheung MK, Ni L, Kase S, Rennel ES, Symonds KE, Nowak DG, Royer-Pokora B, Saleem MA, Hagiwara M, Schumacher VA, et al. WT1 mutants reveal SRPK1 to be a downstream angiogenesis target by altering VEGF splicing. Cancer Cell. 2011; 20(6):768-780.
21. Ruhrberg C, Gerhardt H, Golding M, Watson R, Ioannidou S, Fujisawa H, Betsholtz C and Shima DT. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 2002; 16(20):2684-2698.
22. Marcet-Palacios M, Ulanova M, Duta F, Puttagunta L, Munoz S, Gibbings D, Radomski M, Cameron L, Mayers I and Befus AD. The transcription factor Wilms tumor 1 regulates matrix metalloproteinase-9 through a nitric oxide-mediated pathway. J Immunol. 2007; 179(1):256-265.
23. Hawinkels LJ, Zuidwijk K, Verspaget HW, de Jonge-Muller ES, van Duijn W, Ferreira V, Fontijn RD, David G, Hommes DW, Lamers CB and Sier CF. VEGF release by MMP-9 mediated heparan sulphate cleavage induces colorectal cancer angiogenesis. Eur J Cancer. 2008; 44(13):1904-1913.
24. Hanson J, Gorman J, Reese J and Fraizer G. Regulation of vascular endothelial growth factor, VEGF, gene promoter by the tumor suppressor, WT1. Front Biosci. 2007; 12:2279-2290.
25. Al Dhaybi R, Powell J, McCuaig C and Kokta V. Differentiation of vascular tumors from vascular malformations by expression of Wilms tumor 1 gene: evaluation of 126 cases. J Am Acad Dermatol. 2010; 63(6):1052-1057.
26. Timar J, Meszaros L, Orosz Z, Albini A and Raso E. WT1 expression in angiogenic tumours of the skin. Histopathology. 2005; 47(1):67-73.
27. Vadasz Z, Shasha-Lavsky H, Nov Y, Bejar J, Lurie M, Tadmor T and Attias D. Wilms' tumor gene 1: a possible new proangiogenic factor in Hodgkin lymphoma. Appl Immunohistochem Mol Morphol. 2013; 21(2):177-180.
28. Koblizek TI, Weiss C, Yancopoulos GD, Deutsch U and Risau W. Angiopoietin-1 induces sprouting angiogenesis in vitro. Curr Biol. 1998; 8(9):529-532.
29. Papapetropoulos A, Garcia-Cardena G, Dengler TJ, Maisonpierre PC, Yancopoulos GD and Sessa WC. Direct actions of angiopoietin-1 on human endothelium: evidence for network stabilization, cell survival, and interaction with other angiogenic growth factors. Lab Invest. 1999; 79(2):213-223.
30. Stratmann A, Risau W and Plate KH. Cell type-specific expression of angiopoietin-1 and angiopoietin-2 suggests a role in glioblastoma angiogenesis. Am J Pathol. 1998; 153(5):1459-1466.
31. Takahama M, Tsutsumi M, Tsujiuchi T, Nezu K, Kushibe K, Taniguchi S, Kotake Y and Konishi Y. Enhanced expression of Tie2, its ligand angiopoietin-1, vascular endothelial growth factor, and CD31 in human non-small cell lung carcinomas. Clin Cancer Res. 1999; 5(9):2506-2510.
32. van der Schaft DW, Hillen F, Pauwels P, Kirschmann DA, Castermans K, Egbrink MG, Tran MG, Sciot R, Hauben E, Hogendoorn PC, Delattre O, Maxwell PH, Hendrix MJ and Griffioen AW. Tumor cell plasticity in Ewing sarcoma, an alternative circulatory system stimulated by hypoxia. Cancer Res. 2005; 65(24):11520-11528.
33. Caine GJ, Blann AD, Stonelake PS, Ryan P and Lip GY. Plasma angiopoietin-1, angiopoietin-2 and Tie-2 in breast and prostate cancer: a comparison with VEGF and Flt-1. Eur J Clin Invest. 2003; 33(10):883-890.
34. Tanaka S, Sugimachi K, Yamashita Yi Y, Ohga T, Shirabe K, Shimada M and Wands JR. Tie2 vascular endothelial receptor expression and function in hepatocellular carcinoma. Hepatology. 2002; 35(4):861-867.
35. Egeblad M and Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002; 2(3):161-174.
36. Tomanek RJ and Schatteman GC. Angiogenesis: new insights and therapeutic potential. Anat Rec. 2000; 261(3):126-135.
37. Houck KA, Ferrara N, Winer J, Cachianes G, Li B and Leung DW. The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol. 1991; 5(12):1806-1814.
38. Tischer E, Mitchell R, Hartman T, Silva M, Gospodarowicz D, Fiddes JC and Abraham JA. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J Biol Chem. 1991; 266(18):11947-11954.
39. Ruhrberg C. Growing and shaping the vascular tree: multiple roles for VEGF. Bioessays. 2003; 25(11):1052-1060.
40. Carmeliet P, Ng YS, Nuyens D, Theilmeier G, Brusselmans K, Cornelissen I, Ehler E, Kakkar VV, Stalmans I, Mattot V, Perriard JC, Dewerchin M, Flameng W, Nagy A, Lupu F, Moons L, et al. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Nat Med. 1999; 5(5):495-502.
41. Stalmans I, Ng YS, Rohan R, Fruttiger M, Bouche A, Yuce A, Fujisawa H, Hermans B, Shani M, Jansen S, Hicklin D, Anderson DJ, Gardiner T, Hammes HP, Moons L, Dewerchin M, et al. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J Clin Invest. 2002; 109(3):327-336.
42. Cunningham TJ, Palumbo I, Grosso M, Slater N and Miles CG. WT1 regulates murine hematopoiesis via maintenance of VEGF isoform ratio. Blood. 2013; 122(2):188-192.
43. Loeb DM and Sukumar S. The role of WT1 in oncogenesis: tumor suppressor or oncogene? Int J Hematol. 2002; 76(2):117-126.
44. Tilan JU, Lu C, Galli S, Izycka-Swieszewska E, Earnest JP, Shabbir A, Everhart LM, Wang S, Martin S, Horton M, Mahajan A, Christian D, O'Neill A, Wang H, Zhuang T, Czarnecka M, et al. Hypoxia shifts activity of neuropeptide Y in Ewing sarcoma from growth-inhibitory to growth-promoting effects. Oncotarget. 2013; 4(12):2487-2501.
45. Zhou Z, Yu L and Kleinerman ES. EWS-FLI-1 regulates the neuronal repressor gene REST, which controls Ewing sarcoma growth and vascular morphology. Cancer. 2014.
46. Awad O, Yustein JT, Shah P, Gul N, Katuri V, O'Neill A, Kong Y, Brown ML, Toretsky JA and Loeb DM. High ALDH activity identifies chemotherapy-resistant Ewing's sarcoma stem cells that retain sensitivity to EWS-FLI1 inhibition. PLoS One. 2010; 5(11):e13943.
47. Gum R, Lengyel E, Juarez J, Chen JH, Sato H, Seiki M and Boyd D. Stimulation of 92-kDa gelatinase B promoter activity by ras is mitogen-activated protein kinase kinase 1-independent and requires multiple transcription factor binding sites including closely spaced PEA3/ets and AP-1 sequences. J Biol Chem. 1996; 271(18):10672-10680.
48. Yan C, Wang H and Boyd DD. KiSS-1 represses 92-kDa type IV collagenase expression by down-regulating NF-kappa B binding to the promoter as a consequence of Ikappa Balpha-induced block of p65/p50 nuclear translocation. J Biol Chem. 2001; 276(2):1164-1172.