Contrasting effects of VEGF gene disruption in embryonic stem cell-derived versus oncogene-induced tumors

EMBO Journal

Volumn 22, Issue 16, 2003, Pages 4091-4102

  Viloria Petit, Alicia ^a   Miquerol, Lucile ^b   Yu, Joanne L ^c   Gertsenstein, Marina ^b   Sheehan, Capucine ^a   May, Linda ^c   Henkin, Jack ^d   Lobe, Corrinne ^a   Nagy, Andras ^b   Kerbel, Robert S ^a   Rak, Janusz ^c  

^a SUNNYBROOK RESEARCH INSTITUTE   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d ABBOTT LABORATORIES   (United States)

Author keywords

Neu; PEDF; Ras; TSP 1; VEGF

Indexed keywords

ABT 526; PEPTIDE DERIVATIVE; PIGMENT EPITHELIUM DERIVED FACTOR; THROMBOSPONDIN 1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; DOWN REGULATION; EMBRYONIC STRUCTURES; FIBROBLAST; FIBROSARCOMA; GENE DISRUPTION; GENE TARGETING; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE NEU; ONCOGENE RAS; PERICYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; STEM CELL;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; CHIMERA; EYE PROTEINS; FIBROBLASTS; FIBROSARCOMA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TARGETING; GENES, ERBB-2; GENES, RAS; MICE; MICE, KNOCKOUT; MICE, SCID; MODELS, BIOLOGICAL; MUTATION; NEOVASCULARIZATION, PATHOLOGIC; NERVE GROWTH FACTORS; PEPTIDE FRAGMENTS; PROTEINS; SERPINS; STEM CELLS; TERATOMA; THROMBOSPONDIN 1; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA;

EID: 0042967959     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg408     Document Type: Article

References (41)

1. Bouck, N., Stellmach, V. and Hsu, S.C. (1996) How tumors become angiogenic. Adv. Cancer Res., 69, 135-174.
2. Carmeliet, P. (2000) Mechanisms of angiogenesis and arteriogenesis. Nat. Med., 6, 389-395.
3. Carmeliet, P. et al. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature, 380, 435-439.
4. Claffey, K.P., Brown, L.F., del Aguila, L.F., Tognazzi, K., Yeo, K.-T., Manseau, E.J. and Dvorak, H.F. (1996) Expression of vascular permeability factor/vascular endothelial growth factor melanoma cells increases tumor growth, angiogenesis, and experimental metastasis. Cancer Res., 56, 172-181.
5. Coussens, L.M., Raymond, W.W., Bergers, G., Laig-Webster, M., Behrendtsen, O., Werb, Z., Caughey, G.H. and Hanahan, D. (1999) Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev., 13, 1382-1397.
6. Dameron, K.M., Volpert, O.V., Tainsky, M.A. and Bouck, N. (1994) Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science, 265, 1582-1584.
7. Dawson, D.W. and Bouck, N.P. (1999) Thrombospondin as an inhibitor of angiogenesis. In Teicher, B.A. (ed.), Antiangiogenic Agents in Cancer Therapy. Humana Press, Totowa, NJ, pp. 185-203.
8. Dawson, D.W., Volpert, O.V., Gillis, P., Crawford, S.E., Xu, H., Benedict, W. and Bouck, N.P. (1999) Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science, 285, 245-248.
9. Dvorak, H.F., Brown, L.F., Detmar, M. and Dvorak, A.M. (1995) Review: Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol., 146, 1029-1039.
10. Ferrara, N. and Gerber, H.P. (2001) The role of vascular endothelial growth factor in angiogenesis. Acta Haematol., 106, 148-156.
11. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K.S., Powell-Braxton, L., Hillan, K.J. and Moore, M.W. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature, 380, 439-442.
12. Fukumura, D. et al. (1998) Tumor induction of VEGF promoter activity in stromal cells. Cell, 94, 715-725.
13. Garber, K. (2002) Angiogenesis inhibitors suffer new setback. Nat. Biotechnol., 20, 1067-1068.
14. Grunstein, J., Roberts, W.G., Mathieu-Costello, O., Hanahan, D. and Johnson, R.S. (1999) Tumor-derived expression of vascular endothelial growth factor is a critical factor in tumor expansion and vascular function. Cancer Res., 59, 1592-1598.
15. Grunstein, J., Masbad, J.J., Hickey, R., Giordano, F. and Johnson, R.S. (2000) Isoforms of vascular endothelial growth factor act in a coordinate fashion to recruit and expand tumor vasculature. Mol. Cell. Biol., 20, 7282-7291.
16. Hadjantonakis, A.K., Gertsenstein, M., Ikawa, M., Okabe, M. and Nagy, A. (1998) Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech. Dev., 76, 79-90.
17. Hanahan, D. and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353-364.
18. Hlatky, L., Tsionou, C., Hahnfeldt, P. and Coleman, C.N. (1994) Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res., 54, 6083-6086.
19. Inoue, M., Hager, J.H., Ferrara, N., Gerber, H.P. and Hanahan, D. (2002) VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic beta cell carcinogenesis. Cancer Cell, 1, 193-202.
20. Izumi, Y., Xu, L., diTomaso, E., Fukumura, D. and Jain, R.K. (2002) Herceptin acts as an anti-angiogenic cocktail. Nature, 416, 279-280.
21. Kim, K.J., Li, B., Houck, K., Winer, J. and Ferrara, N. (1992) The vascular endothelial growth factor proteins: identification of biologically relevant regions by neutralizing monoclonal antibodies. Growth Factors, 7, 53-64.
22. Kishimoto, J., Ehama, R., Ge, Y., Kobayashi, T., Nishiyama, T., Detmar, M. and Burgeson, R.E. (2000) In vivo detection of human vascular endothelial growth factor promoter activity in transgenic mouse skin. Am. J. Pathol., 157, 103-110.
23. Lawler, J. (2002) Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J. Cell. Mol. Med., 6, 1-12.
24. Lyden, D. et al. (2001) Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat. Med., 7, 1194-1201.
25. Minchenko, A., Salceda, S., Bauer, T. and Caro, J. (1994) Hypoxia regulatory elements of the human vascular endothelial growth factor gene. Cell. Mol. Biol. Res., 40, 35-39.
26. Miquerol, L., Gertsenstein, M., Harpal, K., Rossant, J. and Nagy, A. (1999) Multiple developmental roles of VEGF suggested by a LacZ-tagged allele. Dev. Biol., 212, 307-322.
27. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. and Roder, J.C. (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl Acad. Sci. USA, 90, 8424-8428.
28. Rak, J. and Kerbel, R.S. (2003) Oncogenes and tumor angiogenesis. In Rak, J. (ed.), Oncogene-Directed Therapies. Humana Press, Totowa, NJ, pp. 171-218.
29. Rak, J., Mitsuhashi, Y., Sheehan, C., Tamir, A., Viloria-Petit, A., Filmus, J., Mansour, S.J., Ahn, N.G. and Kerbel, R.S. (2000) Oncogenes and tumor angiogenesis: differential modes of vascular endothelial growth factor up-regulation in ras-transformed epithelial cells and fibroblasts. Cancer Res., 60, 490-498.
30. Rak, J.W., Yu, J.L., Kerbel, R.S. and Coomber, B.L. (2002) What do oncogenic mutations have to do with angiogenesis/vascular dependence of tumors. Cancer Res., 62, 1931-1934.
31. Reiher, F.K., Volpert, O.V., Jimenez, B., Crawford, S.E., Dinney, C.P., Henkin, J., Haviv, F., Bouck, N.P. and Campbell, S.C. (2002) Inhibition of tumor growth by systemic treatment with thrombospondin-1 peptide mimetics. Int. J. Cancer, 98, 682-689.
32. Relf, M. et al. (1997) Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res., 57, 963-969.
33. Shi, Y.P. and Ferrara, N. (1999) Oncogenic ras fails to restore an in vivo tumorigenic phenotype in embryonic stem cells lacking vascular endothelial growth factor (VEGF). Biochem. Biophys. Res. Commun., 254, 480-483.
34. Soloway, P.D., Alexander, C.M., Werb, Z. and Jaenisch, R. (1996) Targeted mutagenesis of Timp-1 reveals that lung tumor invasion is influenced by Timp-1 genotype of the tumor but not by that of the host. Oncogene, 13, 2307-2314.
35. Tanaka, M., Gertsenstein, M., Rossant, J. and Nagy, A. (1997) Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev. Biol., 190, 55-65.
36. Tsuzuki, Y., Fukumura, D., Oosthuyse, B., Koike, C., Carmeliet, P. and Jain, R.K. (2000) Vascular endothelial growth factor (VEGF) modulation by targeting hypoxia-inducible factor-1alpha→hypoxia response element→VEGF cascade differentially regulates vascular response and growth rate in tumors. Cancer Res., 60, 6248-6252.
37. Watnick, R.S., Cheng, Y.-N., Rangarajan, A., Ince, T.A. and Weinberg, R.A. (2003) Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis. Cancer Cell, 3, 219-231.
38. Yoshiji, H., Harris, S.R. and Thorgeirsson, U.P. (1997) Vascular endothelial growth factor is essential for initial but not continued in vivo growth of human breast carcinoma cells. Cancer Res., 57, 3924-3928.
39. Yu, J.L., Rak, J.W., Carmeliet, P., Nagy, A., Kerbel, R.S. and Coomber, B.L. (2001) Heterogeneous vascular dependence of tumor cell populations. Am. J. Pathol., 158, 1325-1334.
40. Zabrenetzky, V., Harris, C.C., Steeg, P.S. and Roberts, D.D. (1994) Expression of the extracellular matrix molecule thrombospondin inversely correlates with malignant progression in melanoma, lung and breast carcinoma cell lines. Int. J. Cancer, 59, 191-195.
41. Zuber, J., Tchernitsa, O.I, Hinzmann, B., Schmitz, A.C., Grips, M., Hellriegel, M., Sers, C., Rosenthal, A. and Schafer, R. (2000) A genome-wide survey of RAS transformation targets. Nat. Genet., 24, 144-152.