Autocrine VEGF-A/KDR loop protects epithelial ovarian carcinoma cells from anoikis

International Journal of Cancer

Volumn 124, Issue 3, 2009, Pages 553-561

  Sher, Ifat ^a   Adham, Sirin A ^a   Petrik, James ^a   Coomber, Brenda L ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Anoikis; epithelial ovarian cancer; KDR; VEGF

Indexed keywords

VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; ENZYME INHIBITOR; MESSENGER RNA;

ANOIKIS; APOPTOSIS; ARTICLE; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; OVARY CARCINOMA; OVARY METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; AUTOCRINE EFFECT; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOPRECIPITATION; METABOLISM; NEOPLASM; NICK END LABELING; OVARY TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; WESTERN BLOTTING;

ANOIKIS; AUTOCRINE COMMUNICATION; BLOTTING, WESTERN; CELL LINE, TUMOR; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOPRECIPITATION; IN SITU NICK-END LABELING; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 58149314571     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23963     Document Type: Article

References (79)

1. Cannistra SA. Cancer of the ovary. NEngl J Med 1993;329:1550-9.
2. Perez RP, Godwin AK, Hamilton TC, Ozols RF. Ovarian cancer biology. Semin Oncol 1991;18:186-204.
3. Burleson KM, Casey RC, Skubitz KM, Pambuccian SE, Oegema TR, Jr, Skubitz AP. Ovarian carcinoma ascites spheroids adhere to extracellular matrix components and mesothelial cell monolayers. Gynecol Oncol 2004;93:170-81.
4. Abu-Jawdeh GM, Faix JD, Niloff J, Tognazzi K, Manseau E, Dvorak HF, Brown LF. Strong expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in ovarian borderline and malignant neoplasms. Lab Invest 1996;74:1105-15.
5. Fujimoto J, Sakaguchi H, Hirose R, Ichigo S, Tamaya T. Biologic implications of the expression of vascular endothelial growth factor subtypes in ovarian carcinoma. Cancer 1998;83:2528-33.
6. Yokoyama Y, Charnock-Jones DS, Licence D, Yanaihara A, Hastings JM, Holland CM, Emoto M, Umemoto M, Sakamoto T, Sato S, Mizunuma H, Smith SK. Vascular endothelial growth factor-D is an independent prognostic factor in epithelial ovarian carcinoma. Br J Cancer 2003;88:237-44.
7. Nishida N, Yano H, Komai K, Nishida T, Kamura T, 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 2004;101:1364-74.
8. Robinson CJ, Stringer SE. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci 2001;114:853-65.
9. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 2006;7:359-71.
10. Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 1997;18:4-25.
11. Su JL, Yen CJ, Chen PS, Chuang SE, Hong CC, Kuo IH, Chen HY, Hung MC, Kuo ML. The role of the VEGF-C/VEGFR-3 axis in cancer progression. Br J Cancer 2007;96:541-5.
12. McClure N, Healy DL, Rogers PA, Sullivan J, Beaton L, Haning RV, Jr, Connolly DT, Robertson DM. Vascular endothelial growth factor as capillary permeability agent in ovarian hyperstimulation syndrome. Lancet 1994;344:235-6.
13. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983;219:983-5.
14. Nagy JA, Masse EM, Herzberg KT, Meyers MS, Yeo KT, Yeo TK, Sioussat TM, Dvorak HF. Pathogenesis of ascites tumor growth: vascular permeability factor, vascular hyperpermeability, and ascites fluid accumulation. Cancer Res 1995;55:360-8.
15. Nagy JA, Morgan ES, Herzberg KT, Manseau EJ, Dvorak AM, Dvorak HF. Pathogenesis of ascites tumor growth: angiogenesis, vascular remodeling, and stroma formation in the peritoneal lining. Cancer Res 1995;55:376-85.
16. Zebrowski BK, Liu W, Ramirez K, Akagi Y, Mills GB, Ellis LM. Markedly elevated levels of vascular endothelial growth factor in malignant ascites. Ann Surg Oncol 1999;6:373-8.
17. Rudlowski C, Pickart AK, Fuhljahn C, Friepoertner T, Schlehe B, Biesterfeld S, Schroeder W. Prognostic significance of vascular endothelial growth factor expression in ovarian cancer patients: a long-term follow-up. Int J Gynecol Cancer 2006;16 (Suppl 1):183-9.
18. Mesiano S, Ferrara N, Jaffe RB. Role of vascular endothelial growth factor in ovarian cancer: inhibition of ascites formation by immuno-neutralization. Am J Pathol 1998;153:1249-56.
19. Xu L, Yoneda J, Herrera C, Wood J, Killion JJ, Fidler IJ. Inhibition of malignant ascites and growth of human ovarian carcinoma by oral administration of a potent inhibitor of the vascular endothelial growth factor receptor tyrosine kinases. Int J Oncol 2000;16:445-54.
20. Yukita A, Asano M, Okamoto T, Mizutani S, Suzuki H. Suppression of ascites formation and re-accumulation associated with human ovarian cancer by an anti-VPF monoclonal antibody in vivo. Anticancer Res 2000;20:155-60.
21. Hasumi Y, Mizukami H, Urabe M, Kohno T, Takeuchi K, Kume A, Momoeda M, Yoshikawa H, Tsuruo T, Shibuya M, Taketani Y, Ozawa K. Soluble FLT-1 expression suppresses carcinomatous ascites in nude mice bearing ovarian cancer. Cancer Res 2002;62:2019-23.
22. Hu L, Hofmann J, Zaloudek C, Ferrara N, Hamilton T, Jaffe RB. Vascular endothelial growth factor immunoneutralization plus paclitaxel markedly reduces tumor burden and ascites in athymic mouse model of ovarian cancer. Am J Pathol 2002;161:1917-24.
23. Byrne AT, Ross L, Holash J, Nakanishi M, Hu L, Hofmann JI, Yancopoulos GD, Jaffe RB. Vascular endothelial growth factor-trap decreases tumor burden, inhibits ascites, and causes dramatic vascular remodeling in an ovarian cancer model. Clin Cancer Res 2003;9:5721-8.
24. Hu L, Hofmann J, Holash J, Yancopoulos GD, Sood AK, Jaffe RB. Vascular endothelial growth factor trap combined with paclitaxel strikingly inhibits tumor and ascites, prolonging survival in a human ovarian cancer model. Clin Cancer Res 2005;11:6966-71.
25. Pourgholami MH, Yan Cai Z, Lu Y, Wang L, Morris DL. Albendazole: a potent inhibitor of vascular endothelial growth factor and malignant ascites formation in OVCAR-3 tumor-bearing nude mice. Clin Cancer Res 2006;12:1928-35.
26. Burger RA, Sill MW, Monk BJ, Greer BE, Sorosky JL. Phase II trial of bevacizumab in persistent or recurrent epithelial ovarian cancer or primary peritoneal cancer: a gynecologic oncology group study. J Clin Oncol 2007;25:5165-71.
27. Cannistra SA, Matulonis UA, Penson RT, Hambleton J, Dupont J, Mackey H, Douglas J, Burger RA, Armstrong D, Wenham R, McGuire W. Phase II study of bevacizumab in patients with platinum-resistant ovarian cancer or peritoneal serous cancer. J Clin Oncol 2007;25:5180-6.
28. Garcia AA, Hirte H, Fleming G, Yang D, Tsao-Wei DD, Roman L, Groshen S, Swenson S, Markland F, Gandara D, Scudder S, Morgan R. Phase II clinical trial of bevacizumab and low-dose metronomic oral cyclophosphamide in recurrent ovarian cancer: a trial of the California, Chicago and Princess Margaret Hospital phase II consortia. J Clin Oncol 2008;26:76-82.
29. Frisch SM, Ruoslahti E. Integrins and anoikis. Curr Opin Cell Biol 1997;9:701-6.
30. Meredith JE, Jr, Schwartz MA. Integrins, adhesion and apoptosis. Trends Cell Biol 1997;7:146-50.
31. Valentinis B, Morrione A, Peruzzi F, Prisco M, Reiss K, Baserga R. Anti-apoptotic signaling of the IGF-I receptor in fibroblasts following loss of matrix adhesion. Oncogene 1999;18:1827-36.
32. Bates RC, Buret A, van Helden DF, Horton MA, Burns GF. Apoptosis induced by inhibition of intercellular contact. J Cell Biol 1994;125:403-15.
33. McGill G, Shimamura A, Bates RC, Savage RE, Fisher DE. Loss of matrix adhesion triggers rapid transformation-selective apoptosis in fibroblasts. J Cell Biol 1997;138:901-11.
34. Boocock CA, Charnock-Jones DS, Sharkey AM, McLaren J, Barker PJ, Wright KA, Twentyman PR, Smith SK. Expression of vascular endothelial growth factor and its receptors flt and KDR in ovarian carcinoma. J Natl Cancer Inst 1995;87:506-16.
35. Inan S, Vatansever S, Celik-Ozenci C, Sanci M, Dicle N, Demir R. Immunolocalizations of VEGF, its receptors flt-1, KDR and TGF-β's in epithelial ovarian tumors. Histol Histopathol 2006;21:1055-64.
36. Greenaway J, Connor K, Pedersen HG, Coomber BL, LaMarre J, Petrik J. Vascular endothelial growth factor and its receptor. Flk-1/KDR, are cytoprotective in the extravascular compartment of the ovarian follicle. Endocrinology 2004;145:2896-905.
37. St Croix B, Sheehan C, Rak JW, Flørenes VA, Slingerland JM, Kerbel RS. E-cadherin-dependent growth suppression is mediated by the cyclin-dependent kinase inhibitor p27(KIP1). J Cell Biol 1998;142:557-71.
38. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 1992;68:869-77.
39. Tsujimura T, Kanakura Y, Kitamura Y. Mechanisms of constitutive activation of c-kit receptor tyrosine kinase. Leukemia 1997;11:396-8.
40. Yamamoto Y, Kiyoi H, Nakano Y, Suzuki R, Kodera Y, Miyawaki S, Asou N, Kuriyama K, Yagasaki F, Shimazaki C, Akiyama H, Saito K, et al. Activating mutation of D835 within the activation loop of FLT3 in human hematologic malignancies. Blood 2001;97:2434-9.
41. Meshinchi S, Stirewalt DL, Alonzo TA, Zhang Q, Sweetser DA, Woods WG, Bernstein ID, Arceci RJ, Radich JP. Activating mutations of RTK/ras signal transduction pathway in pediatric acute myeloid leukemia. Blood 2003;102:1474-9.
42. Walter JW, North PE, Waner M, Mizeracki A, Blei F, Walker JW, Reinisch JF, Marchuk DA. Somatic mutation of vascular endothelial growth factor receptors in juvenile hemangioma. Genes Chromosomes Cancer 2002;33:295-303.
43. Burns PA, Wilson DJ. Angiogenesis mediated by metabolites is dependent on vascular endothelial growth factor (VEGF). Angiogenesis 2003;6:73-7.
44. Sun L, Tran N, Tang F, App H, Hirth P, McMahon G, Tang C. Synthesis and biological evaluations of 3-substituted indolin-2-ones: a novel class of tyrosine kinase inhibitors that exhibit selectivity toward particular receptor tyrosine kinases. J Med Chem 1998;41:2588-603.
45. Santos SC, Dias S. Internal and external autocrine VEGF/KDR loops regulate survival of subsets of acute leukemia through distinct signaling pathways. Blood 2004;103:3883-9.
46. Coppola S, Narciso L, Feccia T, Bonci D, Calabrò L, Morsilli O, Gabbianelli M, De Maria R, Testa U, Peschle C. Enforced expression of KDR receptor promotes proliferation, survival and megakaryocytic differentiation of TF1 progenitor cell line. Cell Death Differ 2006;13:61-74.
47. Whittles CE, Pocock TM, Wedge SR, Kendrew J, Hennequin LF, Harper SJ, Bates DO. ZM323881, a novel inhibitor of vascular endothelial growth factor-receptor-2 tyrosine kinase activity. Microcirculation 2002;9:513-22.
48. Endo A, Fukuhara S, Masuda M, Ohmori T, Mochizuki N. Selective inhibition of vascular endothelial growth factor receptor-2 (VEGFR- 2) identifies a central role for VEGFR-2 in human aortic endothelial cell responses to VEGF. J Recept Signal Transduct Res 2003;23:239-54.
49. Xiao Z, Kong Y, Yang S, Li M, Wen J, Li L. Upregulation of Flk-1 by bFGF via the ERK pathway is essential for VEGF-mediated promotion of neural stem cell proliferation. Cell Res 2007;17:73-9.
50. Nakayama GR, Caton MC, Nova MP, Parandoosh Z. Assessment of the alamar blue assay for cellular growth and viability in vitro. J Immunol Methods 1997;204:205-8.
51. Voytik-Harbin SL, Brightman AO, Waisner B, Lamar CH, Badylak SF. Application and evaluation of the alamarblue assay for cell growth and survival of fibroblasts. In Vitro Cell Dev Biol Anim 1998;34:239-46.
52. Gloeckner H, Jonuleit T, Lemke HD. Monitoring of cell viability and cell growth in a hollow-fiber bioreactor by use of the dye alamar blue. J Immunol Methods 2001;252:131-8.
53. Solovey A, Gui L, Ramakrishnan S, Steinberg MH, Hebbel RP. Sickle cell anemia as a possible state of enhanced anti-apoptotic tone: survival effect of vascular endothelial growth factor on circulating and unanchored endothelial cells. Blood 1999;93:3824-30.
54. Wu Y, Li ZY, Zhao X, Kan B, Wei YQ. Inhibition of ovarian tumor growth by gene therapy with recombinant soluble vascular endothelial growth factor receptor 2. Hum Gene Ther 2006;17:941-8.
55. So J, Wang FQ, Navari J, Schreher J, Fishman DA. LPA-induced epithelial ovarian cancer (EOC) in vitro invasion and migration are mediated by VEGF receptor-2 (VEGF-R2). Gynecol Oncol 2005;97:870-8.
56. Wang FQ, So J, Reierstad S, Fishman DA. Vascular endothelial growth factor-regulated ovarian cancer invasion and migration involves expression and activation of matrix metalloproteinases. Int J Cancer 2006;118:879-88.
57. Zhang A, Meng L, Wang Q, Xi L, Chen G, Wang S, Zhou J, Lu Y, Ma D. Enhanced in vitro invasiveness of ovarian cancer cells through up-regulation of VEGF and induction of MMP-2. Oncol Rep 2006;15:831-6.
58. Frankel A, Rosen K, Filmus J, Kerbel RS. Induction of anoikis and suppression of human ovarian tumor growth in vivo by down-regulation of Bcl-X(L). Cancer Res 2001;61:4837-41.
59. Dodier P, Piché A. Bcl-X(L) is functionally non-equivalent for the regulation of growth and survival in human ovarian cancer cells. Gynecol Oncol 2006;100:254-63.
60. Cheng KW, Lahad JP, Kuo WL, Lapuk A, Yamada K, Auersperg N, Liu J, Smith-McCune K, Lu KH, Fishman D, Gray JW, Mills GB. The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers. Nat Med 2004;10:1251-6.
61. Yu X, Liu L, Cai B, He Y, Wan X. Suppression of anoikis by the neurotrophic receptor TrkB in human ovarian cancer. Cancer Sci 2008;99:543-52.
62. Furui T, LaPushin R, Mao M, Khan H, Watt SR, Watt MA, Lu Y, Fang X, Tsutsui S, Siddik ZH, Bast RC, Mills GB. Overexpression of edg-2/vzg-1 induces apoptosis and anoikis in ovarian cancer cells in a lysophosphatidic acid-independent manner. Clin Cancer Res 1999;5:4308-18.
63. Fang X, Gaudette D, Furui T, Mao M, Estrella V, Eder A, Pustilnik T, Sasagawa T, Lapushin R, Yu S, Jaffe RB, Wiener JR, et al. Lysophospholipid growth factors in the initiation, progression, metastases, and management of ovarian cancer. Ann NY Acad Sci 2000;905:188-208.
64. Hu YL, Tee MK, Goetzl EJ, Auersperg N, Mills GB, Ferrara N, Jaffe RB. Lysophosphatidic acid induction of vascular endothelial growth factor expression in human ovarian cancer cells. J Natl Cancer Inst 2001;93:762-8.
65. Blazquez C, Cook N, Micklem K, Harris AL, Gatter KC, Pezzella F. Phosphorylated KDR can be located in the nucleus of neoplastic cells. Cell Res 2006;16:93-8.
66. Gerber HP, Malik AK, Solar GP, Sherman D, Liang XH, Meng G, Hong K, Marsters JC, Ferrara N. VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 2002;417:954-8.
67. Shayesteh L, Lu Y, Kuo WL, Baldocchi R, Godfrey T, Collins C, Pinkel D, Powell B, Mills GB, Gray JW. PIK3CA is implicated as an oncogene in ovarian cancer. Nat Genet 1999;21:99-102.
68. Yuan ZQ, Sun M, Feldman RI, Wang G, Ma X, Jiang C, Coppola D, Nicosia SV, Cheng JQ. Frequent activation of AKT2 and induction of apoptosis by inhibition of phosphoinositide-3-OH kinase/Akt pathway in human ovarian cancer. Oncogene 2000;19:2324-30.
69. Philp AJ, Campbell IG, Leet C, Vincan E, Rockman SP, Whitehead RH, Thomas RJ, Phillips WA. The phosphatidylinositol 3′-kinase p85α gene is an oncogene in human ovarian and colon tumors. Cancer Res 2001;61:7426-9.
70. Altomare DA, Wang HQ, Skele KL, De Rienzo A, Klein-Szanto AJ, Godwin AK, Testa JR. AKT and mTOR phosphorylation is frequently detected in ovarian cancer and can be targeted to disrupt ovarian tumor cell growth. Oncogene 2004;23:5853-7.
71. Hu L, Zaloudek C, Mills GB, Gray J, Jaffe RB. In vivo and in vitro ovarian carcinoma growth inhibition by a phosphatidylinositol 3-kinase inhibitor (LY294002). Clin Cancer Res 2000;6:880-6.
72. Fujio Y, Walsh K. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem 1999;274:16349-54.
73. Dayanir V, Meyer RD, Lashkari K, Rahimi N. Identification of tyrosine residues in vascular endothelial growth factor receptor-2/FLK-1 involved in activation of phosphatidylinositol 3-kinase and cell proliferation. J Biol Chem 2001;276:17686-92.
74. Chen H, Ye D, Xie X, Chen B, Lu W. VEGF, VEGFRs expressions and activated. STATs in ovarian epithelial carcinoma. Gynecol Oncol 2004;94:630-5.
75. Osada R, Horiuchi A, Kikuchi N, Ohira S, Ota M, Katsuyama Y, Konishi I. Expression of semaphorins, vascular endothelial growth factor, and their common receptor neuropilins and alleic loss of semaphorin locus in epithelial ovarian neoplasms: increased ratio of vascular endothelial growth factor to semaphorin is a poor prognostic factor in ovarian carcinomas. Hum Pathol 2006;37:1414-25.
76. Wu Y, Hooper AT, Zhong Z, Witte L, Bohlen P, Rafii S, Hicklin DJ. The vascular endothelial growth factor receptor (VEGFR-1) supports growth and survival of human breast carcinoma. Int J Cancer 2006;119:1519-29.
77. Barr MP, Byrne AM, Duffy AM, Condron CM, Devocelle M, Harriott P, Bouchier-Hayes DJ, Harmey JH. A peptide corresponding to the neuropilin-1-binding site on VEGF(165) induces apoptosis of neuropilin-1- expressing breast tumour cells. Br J Cancer 2005;92:328-33.
78. Frumovitz M, Sood AK. Vascular endothelial growth factor (VEGF) pathway as a therapeutic target in gynecologic malignancies. Gynecol Oncol 2007;104:768-78.
79. Rosanò L, Spinella F, Salani D, Di Castro V, Venuti A, Nicotra MR, Natali PG, Bagnato A. Therapeutic targeting of the endothelin a receptor in human ovarian carcinoma. Cancer Res 2003;63:2447-53.