c-Myc is essential for vasculogenesis and angiogenesis during development and tumor progression

Genes and Development

Volumn 16, Issue 19, 2002, Pages 2530-2543

  Baudino, Troy A ^a   McKay, Catriona ^a   Pendeville Samain, Helene ^a   Nilsson, Jonas A ^a   Maclean, Kirsteen H ^a   White, Elsie L ^a   Davis, Ann C ^b   Ihle, James N ^a   Cleveland, John L ^a,c  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b BAYER CORPORATION   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Angiogenesis; c Myc; Tumorigenesis; Vasculogenesis; VEGF

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; THROMBOSPONDIN 1; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; DISEASE ASSOCIATION; EMBRYO; EMBRYONIC STRUCTURES; ERYTHROPOIESIS; IMMUNE DEFICIENCY; LETHALITY; MOUSE; NONHUMAN; ONCOGENE MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR GROWTH; TUMOR VASCULARIZATION; YOLK SAC;

ANGIOPOIETIN-1; ANGIOPOIETIN-2; ANIMALS; ANTIGENS, CD31; CELL DIFFERENTIATION; CELL LINE; ENDOTHELIAL GROWTH FACTORS; ERYTHROPOIESIS; FEMALE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOKINES; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MICE, SCID; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-MYC; STEM CELLS; THROMBOSPONDIN 1; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

ANIMALIA; MAMMALIA;

EID: 0036792667     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1024602     Document Type: Article

References (55)

1. Adelman, D.M., Maltepe, E., and Simon, M.C. 1999. Multilineage embryonic hematopoiesis requires hypoxic ARNT activity. Genes & Dev. 13: 2478-2483.
2. Askew, D.S., Ashmun, R.A., Simmons, B.C., and Cleveland, J.L. 1991. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6: 1915-1922.
3. Barr, L.F., Campbell, S.E., Diette, G.B., Gabrielson, E.W., Kim, S., Shim, and H., Dang, C.V. 2000. c-Myc suppresses the tumorigenicity of lung cancer cells and down-regulates vascular endothelial growth factor expression. Cancer Res. 60: 143-149.
4. Bello-Fernandez, C., Packham, G., and Cleveland, J.L. 1993. Ornithine decarboxylase is a transcriptional target of c-myc. Proc. Natl. Acad. Sci. 90: 7804-7808.
5. Blackwell, T.K., Huang, J., Ma, A., Kretzner, L., Alt, F.W., Eisenman, R.N., and Weintraub, H. 1993. Binding of myc proteins to canonical and noncanonical DNA sequences. Mol. Cell. Biol. 13: 5216-5224.
6. Bradley, A. 1987. Teratocarcinomas and embryonic stem cells. In Teratocarcinomas in embryonic stem cells: A practical approach (E.J. Robertson, ed.), pp. 113-157. IRL, Oxford.
7. Brandvold, K.A., Neiman, P., and Ruddell, A. 2000. Angiogenesis is an early event in the generation of myc-induced lymphomas. Oncogene 19: 2780-2785.
8. Breier, G., Albrecht, U., Sterrer, S., and Risau, W. 1992. Expression of vascular endothelial growth factor during angiogenesis and endothelial cell differentiation. Development 114: 521-532.
9. Carmeliet, P. and Collen, D. 1999. Role of vascular endothelial growth factor and vascular endothelial growth factor receptors in vascular development. Curr. Top. Microbiol. Immunol. 237: 133-158.
10. Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, M., Vandenhoeck, A., Harpal, K., Eberhardt, C., et al. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439.
11. Carmeliet, P., Dor, Y., Herbert, J.-M., Fukumura, D., Brusselmans, K., Dewerchin, M., Neeman, M., Bono, F., Abramovitch, R., Maxwell, P., et al. 1998. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394: 485-490.
12. Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J.C., and Keller, G. 1998. A common precursor for hematopoietic and endothelial cells. Development 125: 725-732.
13. Davis, A.C., Wims, M., Spotts, G.D., Hann, S.R., and Bradley, A. 1993. A null c-myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes & Dev. 7: 671-682.
14. de Alboran, I.M., O'Hagan, R.C., Gartner, F., Malynn, B., Davidson, L., Rickert, R., Rajewsky, K., DePinho, R.A., and Alt, F.W. 2001. Analysis of C-MYC function in normal cells via conditional gene-targeted mutation. Immunity 14: 45-55.
15. Downs, K.M., Martin, G.R., and Bishop, J.M. 1989. Contrasting patterns of myc and N-myc expression during gastrulation of the mouse embryo. Genes & Dev. 3: 860-869.
16. Eilers, M., Schirm, S., and Bishop, J.M. 1991. The MYC protein activates transcription of the α-prothymosin gene. EMBO J. 10: 133-141.
17. Eischen, C.M., Weber, J.D., Roussel, M.F., Sherr, C.J., and Cleveland, J.L. 1999. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes & Dev. 13: 2658-2669.
18. Evan, G.I., Wyllie, A.H., Gilbert, C.S., Littlewood, T.D., Land, H., Brooks, M., Waters, C.M., Penn, L.Z., and Hancock, D.C. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69: 119-128.
19. Felsher, D.W. and Bishop, J.M. 1999. Reversible tumorigenesis by MYC in hematopoietic lineages. Mol. Cell 4: 199-207.
20. 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.
21. Flamme, I., Frolich, T., and Risau, W. 1997. Molecular mechanisms of vasculogenesis and embryonic angiogenesis. J. Cell Physiol. 173: 206-210.
22. Fong, G.-H., Rossant, J., Gertsenstein, M., and Breitman, M.L. 1995. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376: 66-70.
23. Good, D.J., Polverini, P.J., Rastinejad, F., Le, B.M., Lemons, R.A., Frazier, W.A., and Bouck, N.P. 1990. A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc. Natl. Acad. Sci. 89: 6624-6628.
24. Hanahan, D. 1997. Signaling vascular morphogenesis and maintenance. Science 277: 48-50.
25. Hanahan, D. and Folkman, J. 1996. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86: 353-364.
26. Hawighorst, T., Skobe, M., Striet, M., Hong, Y.K., Velasco, P., Brown, L.F., Riccardi, L., Lange-Asschenfeldt, B., and Detmar, M. 2002. Activation of the tie2 receptor by angiopoietin-1 enhances tumor vessel maturation and impairs squamous cell carcinoma growth. Am. J. Pathol. 160: 1381-1392.
27. Ihle, J.N. 2000. The challenges of translating knockout phenotypes into gene function. Cell 102: 131-134.
28. Ilkuta, K., Kina, T., MacNeil, I., Uchida, N., Peailt, B., Chien, Y., and Weissman, I.L. 1990. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell 62: 863-874.
29. 2 homeostasis by hypoxia-inducible factor 1α. Genes & Dev. 12: 149-162.
30. Jain, M., Arvanitis, C., Chu, K., Dewey, W., Leonhardt, E., Trinh, M., Sundberg, C.D., Bishop, J.M., and Felsher, D.W. 2002. Sustained loss of a neoplastic phenotype by brief inactivation of MYC. Science 297: 102-104.
31. Johnston, L.A., Prober, D.A., Edgar, B.A., Eisenman, R.N., and Gallant, P. 1999. Drosophila myc regulates cellular growth during development. Cell 98: 779-790.
32. Kennedy, M., Firpo, M., Choi, K., Wall, C., Robertson, S., Kabrun, N., and Keller, G. 1997. A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature 386: 488-493.
33. Kerbel, R.S., Viloria-Petit, A., Okada, F., and Rak, J. 1998. Establishing a link between oncogenes and tumor angiogenesis. Mol. Med. 4: 286-295.
34. Kozak, K.R., Abbott, B., and Hankinson, O. 1997. ARNT-deficient mice and placental differentiation. Dev. Biol. 191: 297-305.
35. Maltepe, E., Schmidt, J.V., Baunoch, D., Bradfield, C.A., and Simon, M.C. 1997. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386: 403-407.
36. Malynn, B.A., Moreno de Alboran, I., O'Hagan, R.C., Bronson, R., Davidson, L., DePinho, R.A., and Alt, F.W. 2000. N-myc can functionally replace c-myc in murine development, cellular growth, and differentiation. Genes & Dev. 14: 1390-1399.
37. Mateyak, M.K., Obaya, A.J., Adachi, S., and Sedivy, J.M. 1997. Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination. Cell Growth Differ. 8: 1039-1048.
38. Mettouchi, A., Cabon, F., Montreau, N., Vernier, P., Mercier, G., Blangy, D., Tricoire, H., Vigier, P., and Binetruy, B. 1994. SPARC and thrombospondin genes are repressed by the c-jun oncogene in rat embryo fibroblasts. EMBO J. 13: 5668-5678.
39. Okajima, E. and Thorgeirsson, U.P. 2000. Different regulation of vascular endothelial cell growth factor expression by the ERK and p38 kinase pathways in v-ras, v-raf, and v-myc transformed cells. Biochem. Biophys. Res. Commun. 270: 108-111.
40. Oster, S.K., Ho, C.S., Soucie, E.L., and Penn, L.Z. 2002. The myc oncogene: MarvelouslY Complex. Adv. Cancer Res. 84: 81-154.
41. Palis, J., McGrath, K.E., and Kingsley, P.D. 1995. Initiation of hematopoiesis and vasculogenesis in murine yolk sac explants. Blood 86: 156-163.
42. Pelengaris, S., Littlewood, T.D., Khan, M., Elia, G., and Evan, G. 1999. Reversible activation of c-Myc in skin: Induction of a complex neoplastic phenotype by a single oncogenic lesion. Mol. Cell 3: 565-577.
43. Pelengaris, S., Khan, M., and Evan, G.I. 2002. Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell 109: 321-334.
44. Risau, W. 1997. Mechanisms of angiogenesis. Nature 386: 671-674.
45. Ryan, H.E., Lo, J., and Johnson, R.S. 1998. HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J. 17: 3005-3015.
46. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.-F., Breitman, M.L., and Schuh, A.C. 1995. Failure of blood island formation and vasculogenesis in Flk-1-deficient mice. Nature 376: 62-66.
47. Shen, B.Q., Lee, D.Y., Gerber, H.P., Keyt, B.A., Ferrara, N., and Zioncheck, T.F. 1998. Homologous up-regulation of KDR/Flk-1 receptor expression by vascular endothelial growth factor in vitro. J. Biol. Chem. 273: 29979-29985.
48. Slack, J.L. and Bornstein, P. 1994. Transformation by v-src causes a transient induction followed by repression of mouse thrombospondin-1. Cell Growth Differ. 5: 1373-1380.
49. Stein, I., Neeman, M., Shweiki, D., Itin, A., and Keshet, E. 1995. Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol. Cell. Biol. 15: 5363-5368.
50. Tikhonenko, A.T., Black, D.J., and Linial, M.L. 1996. Viral Myc oncoproteins in infected fibroblasts down-modulate thrombospondin-1, a possible tumor suppressor gene. J. Biol. Chem. 271: 30741-30747.
51. Trumpp, A., Refaeli, Y., Oskarsson, T., Gasser, S., Murphy, M., Martine, G.R., and Bishop, G.M. 2001. c-Myc regulates mammalian body size by controlling cell number but not cell size. Nature 414: 768-773.
52. Volpert, O.V., Dameron, K.M., and Bouck, N. 1997. Sequential development of an angiogenic phenotype by human fibroblasts progressing to tumorigenicity. Oncogene 14: 1495-1502.
53. Wagner, R.C. 1980. Endothelial cell embryology and growth. Adv. Microcirc. 9: 45-75.
54. White, F.C., Carroll, S.M., and Kamps, M.P. 1995. VEGF mRNA is reversibly stabilized by hypoxia and persistently stabilized in VEGF-overexpressing human tumor cell lines. Growth Factors 12: 289-301.
55. Zindy, F., Eischen, C.M., Randle, D.H., Kamijo, T., Cleveland, J.L., Sherr, C.J., and Roussel, M.F. 1998. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes & Dev. 12: 2424-2433.