VEGFR-2 silencing by small interference RNA (siRNA) suppresses LPA-induced epithelial ovarian cancer (EOC) invasion

Gynecologic Oncology

Volumn 115, Issue 3, 2009, Pages 414-423

  Wang, Feng qiang ^a   Barfield, Elaine ^a   Dutta, Sonia ^a   Pua, Tarah ^a   Fishman, David A ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Epithelial ovarian cancer (EOC); LPA; Small interference RNA (siRNA); VEGF121; VEGF165; VEGFR 2

Indexed keywords

LYSOPHOSPHATIDIC ACID; NEUROPILIN 1; NEUROPILIN 2; SMALL INTERFERING RNA; VASCULOTROPIN 121; VASCULOTROPIN 165; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ARTICLE; CANCER CELL CULTURE; CANCER GRADING; CANCER INVASION; EPITHELIAL OVARY CANCER; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; OVARY CANCER; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL LINE, TUMOR; EPITHELIAL CELLS; FEMALE; HUMANS; LYSOPHOSPHOLIPIDS; NEOPLASM INVASIVENESS; NEUROPILIN-1; NEUROPILIN-2; OVARIAN NEOPLASMS; RNA INTERFERENCE; RNA, SMALL INTERFERING; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 70350571185     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2009.08.019     Document Type: Article

References (58)

1. Robinson C.J., and Stringer S.E. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J. Cell. Sci. 114 (2001) 853-865
2. Spannuth W.A., Sood A.K., and Coleman R.L. Angiogenesis as a strategic target for ovarian cancer therapy. Nat. Clin. Pract. Oncol. 5 (2008) 194-204
3. Abu-Jawdeh G.M., Faix J.D., Niloff J., Tognazzi K., Manseau E., Dvorak H.F., et al. Strong expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in ovarian borderline and malignant neoplasms. Lab. Invest. 74 (1996) 1105-1115
4. Chen H., Ye D., Xie X., Chen B., and Lu W. VEGF, VEGFRs expressions and activated STATs in ovarian epithelial carcinoma. Gynecol. Oncol. 94 (2004) 630-635
5. Hu Y.L., Tee M.K., Goetzl E.J., Auersperg N., Mills G.B., Ferrara N., et al. Lysophosphatidic acid induction of vascular endothelial growth factor expression in human ovarian cancer cells. J. Natl. Cancer Inst. 93 (2001) 762-768
6. Orre M., and Rogers P.A. VEGF, VEGFR-1, VEGFR-2, microvessel density and endothelial cell proliferation in tumours of the ovary. Int. J. Cancer 84 (1999) 101-108
7. Ito T.K., Ishii G., Saito S., Yano K., Hoshino A., Suzuki T., et al. Degradation of soluble VEGF receptor-1 by MMP-7 allows VEGF access to endothelial cells. Blood 113 (2009) 2363-2369
8. Boocock C.A., Charnock-Jones D.S., Sharkey A.M., McLaren J., Barker P.J., Wright K.A., et al. Expression of vascular endothelial growth factor and its receptors flt and KDR in ovarian carcinoma. J. Natl. Cancer Inst. 87 (1995) 506-516
9. Wang F.Q., So J., Reierstad S., and Fishman D.A. Vascular endothelial growth factor-regulated ovarian cancer invasion and migration involves expression and activation of matrix metalloproteinases. Int. J. Cancer 118 (2006) 879-888
10. Sher I., Adham S.A., Petrik J., and Coomber B.L. Autocrine VEGF-A/KDR loop protects epithelial ovarian carcinoma cells from anoikis. Int. J. Cancer 124 (2009) 553-561
11. Soker S., Takashima S., Miao H.Q., Neufeld G., and Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92 (1998) 735-745
12. Broholm H., and Laursen H. Vascular endothelial growth factor (VEGF) receptor neuropilin-1's distribution in astrocytic tumors. APMIS 112 (2004) 257-263
13. Stephenson J.M., Banerjee S., Saxena N.K., Cherian R., and Banerjee S.K. Neuropilin-1 is differentially expressed in myoepithelial cells and vascular smooth muscle cells in preneoplastic and neoplastic human breast: a possible marker for the progression of breast cancer. Int. J. Cancer 101 (2002) 409-414
14. Fakhari M., Pullirsch D., Abraham D., Paya K., Hofbauer R., Holzfeind P., et al. Selective upregulation of vascular endothelial growth factor receptors neuropilin-1 and -2 in human neuroblastoma. Cancer 94 (2002) 258-263
15. Straume O., and Akslen L.A. Increased expression of VEGF-receptors (FLT-1, KDR, NRP-1) and thrombospondin-1 is associated with glomeruloid microvascular proliferation, an aggressive angiogenic phenotype, in malignant melanoma. Angiogenesis 6 (2003) 295-301
16. Hansel D.E., Wilentz R.E., Yeo C.J., Schulick R.D., Montgomery E., and Maitra A. Expression of neuropilin-1 in high-grade dysplasia, invasive cancer, and metastases of the human gastrointestinal tract. Am. J. Surg. Pathol. 28 (2004) 347-356
17. Lantuejoul S., Constantin B., Drabkin H., Brambilla C., Roche J., and Brambilla E. Expression of VEGF, semaphorin SEMA3F, and their common receptors neuropilins NP1 and NP2 in preinvasive bronchial lesions, lung tumours, and cell lines. J. Pathol. 200 (2003) 336-347
18. Kawakami T., Tokunaga T., Hatanaka H., Kijima H., Yamazaki H., Abe Y., et al. Neuropilin 1 and neuropilin 2 co-expression is significantly correlated with increased vascularity and poor prognosis in nonsmall cell lung carcinoma. Cancer 95 (2002) 2196-2201
19. Fukahi K., Fukasawa M., Neufeld G., Itakura J., and Korc M. Aberrant expression of neuropilin-1 and -2 in human pancreatic cancer cells. Clin. Cancer Res. 10 (2004) 581-590
20. Parikh A.A., Fan F., Liu W.B., Ahmad S.A., Stoeltzing O., Reinmuth N., et al. Neuropilin-1 in human colon cancer: expression, regulation, and role in induction of angiogenesis. Am. J. Pathol. 164 (2004) 2139-2151
21. Vanveldhuizen P.J., Zulfiqar M., Banerjee S., Cherian R., Saxena N.K., Rabe A., et al. Differential expression of neuropilin-1 in malignant and benign prostatic stromal tissue. Oncol. Rep. 10 (2003) 1067-1071
22. Latil A., Bieche I., Pesche S., Valeri A., Fournier G., Cussenot O., et al. VEGF overexpression in clinically localized prostate tumors and neuropilin-1 overexpression in metastatic forms. Int. J. Cancer 89 (2000) 167-171
23. Hall G.H., Turnbull L.W., Bedford K., Richmond I., Helboe L., and Atkin S.L. Neuropilin-1 and VEGF correlate with somatostatin expression and microvessel density in ovarian tumours. Int. J. Oncol. 27 (2005) 1283-1288
24. Baba T., Kariya M., Higuchi T., Mandai M., Matsumura N., Kondoh E., et al. Neuropilin-1 promotes unlimited growth of ovarian cancer by evading contact inhibition. Gynecol. Oncol. 105 (2007) 703-711
25. Goetzl E.J., Dolezalova H., Kong Y., Hu Y.L., Jaffe R.B., Kalli K.R., et al. Distinctive expression and functions of the type 4 endothelial differentiation gene-encoded G protein-coupled receptor for lysophosphatidic acid in ovarian cancer. Cancer Res. 59 (1999) 5370-5375
26. Huang M.C., Lee H.Y., Yeh C.C., Kong Y., Zaloudek C.J., and Goetzl E.J. Induction of protein growth factor systems in the ovaries of transgenic mice overexpressing human type 2 lysophosphatidic acid G protein-coupled receptor (LPA2). Oncogene 23 (2004) 122-129
27. So J., Wang F.Q., Navari J., Schreher J., and Fishman D.A. LPA-induced epithelial ovarian cancer (EOC) in vitro invasion and migration are mediated by VEGF receptor-2 (VEGF-R2). Gynecol. Oncol. 97 (2005) 870-878
28. Shen B.Q., Lee D.Y., and Zioncheck T.F. Vascular endothelial growth factor governs endothelial nitric-oxide synthase expression via a KDR/Flk-1 receptor and a protein kinase C signaling pathway. J. Biol. Chem. 274 (1999) 33057-33063
29. Jin K., Zhu Y., Sun Y., Mao X.O., Xie L., and Greenberg D.A. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 11946-11950
30. Germani A., Di Carlo A., Mangoni A., Straino S., Giacinti C., Turrini P., et al. Vascular endothelial growth factor modulates skeletal myoblast function. Am. J. Pathol. 163 (2003) 1417-1428
31. Wang Y., Chang J., Chen K.D., Li S., Li J.Y., Wu C., et al. Selective adapter recruitment and differential signaling networks by VEGF vs. shear stress. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 8875-8879
32. Boguslawski G., McGlynn P.W., Harvey K.A., and Kovala A.T. SU1498, an inhibitor of vascular endothelial growth factor receptor 2, causes accumulation of phosphorylated ERK kinases and inhibits their activity in vivo and in vitro. J. Biol. Chem. 279 (2004) 5716-5724
33. Wang F.Q., So J., Reierstad S., and Fishman D.A. Matrilysin (MMP-7) promotes invasion of ovarian cancer cells by activation of progelatinase. Int. J. Cancer 114 (2004) 19-31
34. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117 (2004) 927-939
35. Wang F.Q., So J., Reierstad S., and Fishman D.A. Matrilysin (MMP-7) promotes invasion of ovarian cancer cells by activation of progelatinase. Int. J. Cancer 114 (2005) 19-31
36. Park S.Y., Jeong K.J., Lee J., Yoon D.S., Choi W.S., Kim Y.K., et al. Hypoxia enhances LPA-induced HIF-1alpha and VEGF expression: their inhibition by resveratrol. Cancer Lett. 258 (2007) 63-69
37. Ptaszynska M.M., Pendrak M.L., Bandle R.W., Stracke M.L., and Roberts D.D. Positive feedback between vascular endothelial growth factor-A and autotaxin in ovarian cancer cells. Mol. Cancer Res. 6 (2008) 352-363
38. Slongo M.L., Molena B., Brunati A.M., Frasson M., Gardiman M., Carli M., et al. Functional VEGF and VEGF receptors are expressed in human medulloblastomas. Neuro. Oncol. (2007)
39. Bellamy W.T., Richter L., Frutiger Y., and Grogan T.M. Expression of vascular endothelial growth factor and its receptors in hematopoietic malignancies. Cancer Res. 59 (1999) 728-733
40. Masood R., Cai J., Zheng T., Smith D.L., Hinton D.R., and Gill P.S. Vascular endothelial growth factor (VEGF) is an autocrine growth factor for VEGF receptor-positive human tumors. Blood 98 (2001) 1904-1913
41. Wedge S.R., Ogilvie D.J., Dukes M., Kendrew J., Chester R., Jackson J.A., et al. ZD6474 inhibits vascular endothelial growth factor signaling, angiogenesis, and tumor growth following oral administration. Cancer Res. 62 (2002) 4645-4655
42. Ciardiello F., Caputo R., Damiano V., Troiani T., Vitagliano D., Carlomagno F., et al. Antitumor effects of ZD6474, a small molecule vascular endothelial growth factor receptor tyrosine kinase inhibitor, with additional activity against epidermal growth factor receptor tyrosine kinase. Clin. Cancer Res. 9 (2003) 1546-1556
43. Shen G.H., Ghazizadeh M., Kawanami O., Shimizu H., Jin E., Araki T., et al. Prognostic significance of vascular endothelial growth factor expression in human ovarian carcinoma. Br. J. Cancer 83 (2000) 196-203
44. Brustmann H., and Naude S. Vascular endothelial growth factor expression in serous ovarian carcinoma: relationship with high mitotic activity and high FIGO stage. Gynecol. Oncol. 84 (2002) 47-52
45. Cooper B.C., Ritchie J.M., Broghammer C.L., Coffin J., Sorosky J.I., Buller R.E., et al. Preoperative serum vascular endothelial growth factor levels: significance in ovarian cancer. Clin. Cancer Res. 8 (2002) 3193-3197
46. Garofalo A., Naumova E., Manenti L., Ghilardi C., Ghisleni G., Caniatti M., et al. The combination of the tyrosine kinase receptor inhibitor SU6668 with paclitaxel affects ascites formation and tumor spread in ovarian carcinoma xenografts growing orthotopically. Clin. Cancer Res. 9 (2003) 3476-3485
47. Mesiano S., Ferrara N., and Jaffe R.B. Role of vascular endothelial growth factor in ovarian cancer: inhibition of ascites formation by immunoneutralization. Am. J. Pathol. 153 (1998) 1249-1256
48. Hu L., Hofmann J., Zaloudek C., Ferrara N., Hamilton T., and Jaffe R.B. Vascular endothelial growth factor immunoneutralization plus Paclitaxel markedly reduces tumor burden and ascites in athymic mouse model of ovarian cancer. Am. J. Pathol. 161 (2002) 1917-1924
49. Inan S., Vatansever S., Celik-Ozenci C., Sanci M., Dicle N., and Demir R. Immunolocalizations of VEGF, its receptors flt-1, KDR and TGF-beta's in epithelial ovarian tumors. Histol. Histopathol. 21 (2006) 1055-1064
50. Nishida N., Yano H., Komai K., Nishida T., Kamura T., and Kojiro M. Vascular endothelial growth factor C and vascular endothelial growth factor receptor 2 are related closely to the prognosis of patients with ovarian carcinoma. Cancer 101 (2004) 1364-1374
51. Bielenberg D.R., Pettaway C.A., Takashima S., and Klagsbrun M. Neuropilins in neoplasms: expression, regulation, and function. Exp. Cell Res. 312 (2006) 584-593
52. Ellis L.M. The role of neuropilins in cancer. Mol. Cancer Ther. 5 (2006) 1099-1107
53. Xu Y., Shen Z., Wiper D.W., Wu M., Morton R.E., Elson P., et al. Lysophosphatidic acid as a potential biomarker for ovarian and other gynecologic cancers. JAMA 280 (1998) 719-723
54. Xu Y., Fang X.J., Casey G., and Mills G.B. Lysophospholipids activate ovarian and breast cancer cells. Biochem. J. 309 Pt 3 (1995) 933-940
55. Xu Y., Gaudette D.C., Boynton J.D., Frankel A., Fang X.J., Sharma A., et al. Characterization of an ovarian cancer activating factor in ascites from ovarian cancer patients. Clin. Cancer Res. 1 (1995) 1223-1232
56. Mills G.B., Eder A., Fang X., Hasegawa Y., Mao M., Lu Y., et al. Critical role of lysophospholipids in the pathophysiology, diagnosis, and management of ovarian cancer. Cancer Treat. Res. 107 (2002) 259-283
57. Lee C.W., Rivera R., Gardell S., Dubin A.E., and Chun J. GPR92 as a new G12/13- and Gq-coupled lysophosphatidic acid receptor that increases cAMP, LPA5. J. Biol. Chem. 281 (2006) 23589-23597
58. Fujita T., Miyamoto S., Onoyama I., Sonoda K., Mekada E., and Nakano H. Expression of lysophosphatidic acid receptors and vascular endothelial growth factor mediating lysophosphatidic acid in the development of human ovarian cancer. Cancer Lett. 192 (2003) 161-169