The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis

Genes and Development

Volumn 19, Issue 17, 2005, Pages 2054-2065

  Hamada, Koichi ^a   Sasaki, Takehiko ^a   Koni, Pandelakis A ^b   Natsui, Miyuki ^a   Kishimoto, Hiroyuki ^a   Sasaki, Junko ^a   Yajima, Nobuyuki ^a   Horie, Yasuo ^a   Hasegawa, Go ^c   Naito, Makoto ^c   Miyazaki, Jun Ichi ^d   Suda, Toshio ^e   Itoh, Hiroshi ^f   Nakao, Kazuwa ^f   Tak, Wah Mak ^g   Nakano, Toru ^h   Suzuki, Akira ^a  

^a AKITA UNIVERSITY   (Japan)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f KYOTO UNIVERSITY   (Japan)

^g UNIVERSITY OF TORONTO   (Canada)

^h OSAKA UNIVERSITY   (Japan)

Author keywords

Cardiovasculogenesis; Endothelial cells; PI3K; PTEN; Tumor angiogenesis

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN ANG 1; PROTEIN VCAM 1; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOCARDIUM; ENDOTHELIUM CELL; GENE MUTATION; GENETIC SUSCEPTIBILITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VASCULARIZATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BASE SEQUENCE; CELLS, CULTURED; FEMALE; FETAL HEART; GENES, TUMOR SUPPRESSOR; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MUTATION; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN-TYROSINE-PHOSPHATASE; PTEN PHOSPHOHYDROLASE; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEINS;

EID: 24344446438     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1308805     Document Type: Article

References (56)

1. Antonelli-Orlidge, A., Saunders, K.B., Smith, S.R., and D'Amore, P.A. 1989. An activated form of transforming growth factor β is produced by cocultures of endothelial cells and pericytes. Proc. Natl. Acad. Sci. 86: 4544-4548.
2. Benjamin, L.E., Hemo, I., and Keshet, E. 1998. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 125: 1591-1598.
3. Bi, L., Okabe, I., Bernard, D.J., and Nussbaum, R.L. 2002. Early embryonic lethality in mice deficient in the p110β catalytic subunit of PI 3-kinase. Mamm. Genome 13: 169-172.
4. Bingle, L., Brown, N.J., and Lewis, C.E. 2002. The role of tumour-associated macrophages in tumour progression: Implications for new anticancer therapies. J. Pathol. 196: 254-265.
5. Crackower, M.A., Oudit, G.Y., Kozieradzki, I., Sarao, R., Sun, H., Sasaki, T., Hirsch, E., Suzuki, A., Shioi, T., Irie-Sasaki, J., et al. 2002. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell 110: 737-749.
6. Daniel, T.O. and Abrahamson, D. 2000. Endothelial signal integration in vascular assembly. Annu. Rev. Physiol. 62: 649-671.
7. Dickson, M.C., Martin, J.S., Cousins, F.M., Kulkarni, A.B., Karlsson, S., and Akhurst, R.J. 1995. Defective haematopoiesis and vasculogenesis in transforming growth factor-β 1 knock out mice. Development 121: 1845-1854.
8. Dimmeler, S., Assmus, B., Hermann, C., Haendeler, J., and Zeiherk, A.M. 1998. Fluid shear stress stimulates phosphorylation of Akt in human endothelial cells: Involvement in suppression of apoptosis. Circ. Res. 83: 334-341.
9. Dumont, D.J., Gradwohl, G., Fong, G.H., Puri, M.C., Gertsenstein, M., Auerbach, A., and Breitman, M.L. 1994. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes & Dev. 8: 1897-1909.
10. Folkman, J. and Shing, Y. 1992. Angiogenesis. J. Biol. Chem. 267: 10931-10934.
11. Fruman, D.A., Snapper, S.B., Yballe, C.M., Davidson, L., Yu, J.Y., Alt, F.W., and Cantley, L.C. 1999. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85α. Science 283: 393-397.
12. Furuyama, T., Kitayama, K., Shimoda, Y., Ogawa, M., Sone, K., Yoshida-Araki, K., Hisatsune, H., Nishikawa, S., Nakayama, K., Ikeda, K., et al. 2004. Abnormal angiogenesis in Foxo1 (Fkhr)-deficient mice. J. Biol. Chem. 279: 34741-34749.
13. Gerber, H.P., McMurtrey, A., Kowalski, J., Yan, M., Keyt, B.A., Dixit, V., and Ferrara, N. 1998. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway: Requirement for Flk-1/KDR activation. J. Biol. Chem. 273: 30336-30343.
14. Hammes, H.P., Lin, J., Wagner, P., Feng, Y., Vom Hagen, F., Krzizok, T., Renner, O., Breier, G., Brownlee, M., and Deutsch, U. 2004. Angiopoietin-2 causes pericyte dropout in the normal retina: Evidence for involvement in diabetic retinopathy. Diabetes 53: 1104-1110.
15. Hartwell, D.W., Mayadas, T.N., Berger, G., Frenette, P.S., Rayburn, H., Hynes, R.O., and Wagner, D.D. 1998. Role of P-selectin cytoplasmic domain in granular targeting in vivo and in early inflammatory responses. J. Cell Biol. 143: 1129-1141.
16. Hellstrom, M., Gerhardt, H., Kalen, M., Li, X., Eriksson, U., Wolburg, H., and Betsholtz, C. 2001. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J. Cell Biol. 153: 543-553.
17. Huang, J. and Kontos, C.D. 2002. PTEN modulates vascular endothelial growth factor-mediated signaling and angiogenic effects. J. Biol. Chem. 277: 10760-10766.
18. Hungerford, J.E. and Little, C.D. 1999. Developmental biology of the vascular smooth muscle cell: Building a multilayered vessel wall. J. Vasc. Res. 36: 2-27.
19. Ito, Y., Oike, Y., Yasunaga, K., Hamada, K., Miyata, K., Matsumoto, S., Sugano, S., Tanihara, H., Masuho, Y., and Suda, T. 2003. Inhibition of angiogenesis and vascular leakiness by angiopoietin-related protein 4. Cancer Res. 63: 6651-6657.
20. Jain, R.K. 2003. Molecular regulation of vessel maturation. Nat. Med. 9: 685-693.
21. Jiang, B.H., Zheng, J.Z., Aoki, M., and Vogt, P.K. 2000. Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc. Natl. Acad. Sci. 97: 1749-1753.
22. Kaplan-Albuquerque, N., Garat, C., Desseva, C., Jones, P.L., and Nemenoff, R.A. 2003. Platelet-derived growth factor-BB-mediated activation of Akt suppresses smooth muscle-specific gene expression through inhibition of mitogen-activated protein kinase and redistribution of serum response factor. J. Biol. Chem. 278: 39830-39838.
23. Kawamoto, S., Niwa, H., Tashiro, F., Sano, S., Kondoh, G., Takeda, J., Tabayashi, K., and Miyazaki, J. 2000. A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett. 470: 263-268.
24. Kim, K.J., Li, B., Winer, J., Armanini, M., Gillett, N., Phillips, H.S., and Ferrara, N. 1993. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 362: 841-844.
25. Koni, P.A., Joshi, S.K., Temann, U.A., Olson, D., Burkly, L., and Flavell, R.A. 2001. Conditional vascular cell adhesion molecule 1 deletion in mice: Impaired lymphocyte migration to bone marrow. J. Exp. Med. 193: 741-754.
26. Kwee, L., Baldwin, H.S., Shen, H.M., Stewart, C.L., Buck, C., Buck, C.A., and Labow, M.A. 1995. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121: 489-503.
27. Larsson, J., Goumans, M.J., Sjostrand, L.J., van Rooijen, M.A., Ward, D., Leveen, P., Xu, X., ten Dijke, P., Mummery, C.L., and Karlsson, S. 2001. Abnormal angiogenesis but intact hematopoietic potential in TGF-β type I receptor-deficient mice. EMBO J. 20: 1663-1673.
28. Lee, M.J., Thangada, S., Claffey, K.P., Ancellin, N., Liu, C.H., Kluk, M., Volpi, M., Sha'afi, R.I., and Hla, T. 1999. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell 99: 301-312.
29. Li, D.M. and Sun, H. 1997. TEP1, encoded by a candidate tumor suppressor locus, is a novel protein tyrosine phosphatase regulated by transforming growth factor β. Cancer Res. 57: 2124-2129.
30. Li, J., Yen, C., Liaw, D., Podsypanina, K., Bose, S., Wang, S.I., Puc, J., Miliaresis, C., Rodgers, L., McCombie, R., et al. 1997. PTEN: A putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275: 1943-1947.
31. Liaw, D., Marsh, D.J., Li, J., Dahia, P.L., Wang, S.I., Zheng, Z., Bose, S., Call, K.M., Tsou, H.C., Peacocke, M., et al. 1997. Germline mutations of the PTEN gene in Cowden disease: An inherited breast and thyroid cancer syndrome. Nat. Genet. 16: 64-67.
32. Lindahl, P., Johansson, B.R., Leveen, P., and Betsholtz, C. 1997. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277: 242-245.
33. Lindblom, P., Gerhardt, H., Liebner, S., Abramsson, A., Enge, M., Hellstrom, M., Backstrom, G., Fredriksson, S., Landegren, U., Nystrom, H.C., et al. 2003. Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes & Dev. 17: 1835-1840.
34. Liu, Y., Wada, R., Yamashita, T., Mi, Y., Deng, C.X., Hobson, J.P., Rosenfeldt, H.M., Nava, V.E., Chae, S.S., Lee, M.J., et al. 2000. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J. Clin. Invest. 106: 951-961.
35. Maehama, T. and Dixon, J.E. 1998. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273: 13375-13378.
36. Maisonpierre, P.C., Suri, C., Jones, P.F., Bartunkova, S., Wiegand, S.J., Radziejewski, C., Compton, D., McClain, J., Aldrich, T.H., Papadopoulos, N., et al. 1997. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277: 55-60.
37. Miquerol, L., Langille, B.L., and Nagy, A. 2000. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 127: 3941-3946.
38. Miyagishi, M. and Taira, K. 2002. U6 promoter-driven siRNAs with four uridine 3′ overhangs efficiently suppress targeted gene expression in mammalian cells. Nat. Biotechnol. 20: 497-500.
39. Morales-Ruiz, M., Lee, M.J., Zollner, S., Gratton, J.P., Scotland, R., Shiojima, I., Walsh, K., Hla, T., and Sessa, W.C. 2001. Sphingosine 1-phosphate activates Akt, nitric oxide production, and chemotaxis through a Gi protein/phosphoinositide 3-kinase pathway in endothelial cells. J. Biol. Chem. 276: 19672-19677.
40. Okkenhaug, K., Bilancio, A., Farjot, G., Priddle, H., Sancho, S., Peskett, E., Pearce, W., Meek, S.E., Salpekar, A., Waterfield, M.D., et al. 2002. Impaired B and T cell antigen receptor signaling in p110Δ PI 3-kinase mutant mice. Science 297: 1031-1034.
41. Plate, K.H., Breier, G., and Risau, W. 1994. Molecular mechanisms of developmental and tumor angiogenesis. Brain Pathol. 4: 207-218.
42. Prewett, M., Huber, J., Li, Y., Santiago, A., O'Connor, W., King, K., Overholser, J., Hooper, A., Pytowski, B., Witte, L., et al. 1999. Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors. Cancer Res. 59: 5209-5218.
43. Remy, I., Montmarquette, A., and Michnick, S.W. 2004. PKB/Akt modulates TGF-β signalling through a direct interaction with Smad3. Nat. Cell Biol. 6: 358-365.
44. Sasaki, T., Irie-Sasaki, J., Jones, R.G., Oliveira-dos-Santos, A.J., Stanford, W.L., Bolon, B., Wakeham, A., Itie, A., Bouchard, D., Kozieradzki, I., et al. 2000. Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration. Science 287: 1040-1046.
45. Shiojima, I. and Walsh, K. 2002. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ. Res. 90: 1243-1250.
46. Stoyanov, B., Volinia, S., Hanck, T., Rubio, I., Loubtchenkov, M., Malek, D., Stoyanova, S., Vanhaesebroeck, B., Dhand, R., Nurnberg, B., et al. 1995. Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. Science 269: 690-693.
47. Su, J.D., Mayo, L.D., Donner, D.B., and Durden, D.L. 2003. PTEN and phosphatidylinositol 3′-kinase inhibitors upregulate p53 and block tumor-induced angiogenesis: Evidence for an effect on the tumor and endothelial compartment. Cancer Res. 63: 3585-3592.
48. Sun, J.F., Phung, T., Shiojima, I., Felske, T., Upalakalin, J.N., Feng, D., Kornaga, T., Dor, T., Dvorak, A.M., Walsh, K., et al. 2005. Microvascular patterning is controlled by fine-tuning the Akt signal. Proc. Natl. Acad. Sci. 102: 128-133.
49. Suri, C., Jones, P.F., Patan, S., Bartunkova, S., Maisonpierre, P.C., Davis, S., Sato, T.N., and Yancopoulos, G.D. 1996. Requisite role of angiopoietin-1: A ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87: 1171-1180.
50. Suzuki, A., Yamaguchi, M.T., Ohteki, T., Sasaki, T., Kaisho, T., Kimura, Y., Yoshida, R., Wakeham, A., Higuchi, T., Fukumoto, M., et al. 2001. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 14: 523-534.
51. Terauchi, Y., Tsuji, Y., Satoh, S., Minoura, H., Murakami, K., Okuno, A., Inukai, K., Asano, T., Kaburagi, Y., Ueki, K., et al. 1999. Increased insulin sensitivity and hypoglycaemia in mice lacking the p85 α subunit of phosphoinositide 3-kinase. Nat. Genet. 21: 230-235.
52. Ueki, K., Yballe, C.M., Brachmann, S.M., Vicent, D., Watt, J.M., Kahn, C.R., and Cantley, L.C. 2002. Increased insulin sensitivity in mice lacking p85β subunit of phosphoinositide 3-kinase. Proc. Natl. Acad. Sci. 99: 419-424.
53. Wang, H.U., Chen, Z.F., and Anderson, D.J. 1998. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93: 741-753.
54. Yamaguchi, T.P., Dumont, D.J., Conlon, R.A., Breitman, M.L., and Rossant, J. 1993. flk-1, an flt-related receptor tyrosine kinase, is an early marker for endothelial cell precursors. Development 118: 489-498.
55. Zeng, X., Wert, S.E., Federici, R., Peters, K.G., and Whitsett, J.A. 1998. VEGF enhances pulmonary vasculogenesis and disrupts lung morphogenesis in vivo. Dev. Dyn. 211: 215-227.
56. Zhang, T., Chen, X., Qu, L., Wu, J., Cui, R., and Zhao, Y. 2004. Chrysin and its phosphate ester inhibit cell proliferation and induce apoptosis in Hela cells. Bioorg. Med. Chem. 12: 6097-6105.