Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo

Juhua Chen; Payaningal R Somanath; Olga Razorenova; William S Chen; Nissim Hay; Paul Bornstein; Tatiana V Byzova

doi:10.1038/nm1307

journal article Oct 16, 2005

Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo

Juhua Chen Payaningal R Somanath Olga Razorenova William S Chen Nissim Hay Paul Bornstein Tatiana V Byzova

Nature Medicine Vol. 11 No. 11 pp. 1188-1196 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/nm1307

Topics

No keywords indexed for this article. Browse by subject →

References

45

[1]

Risau, W. Mechanisms of angiogenesis. Nature 386, 671–674 (1997). 10.1038/386671a0

[2]

Folkman, J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1, 27–31 (1995). 10.1038/nm0195-27

[3]

Carmeliet, P. Angiogenesis in health and disease. Nat. Med. 9, 653–660 (2003). 10.1038/nm0603-653

[4]

Jiang, B.H., Zheng, J.Z., Aoki, M. & Vogt, P.K. Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc. Natl. Acad. Sci. USA 97, 1749–1753 (2000). 10.1073/pnas.040560897

[5]

Kandel, E.S. & Hay, N. The regulation and activities of the multifunctional serine/threonine kinase Akt/PKB. Exp. Cell Res. 253, 210–229 (1999). 10.1006/excr.1999.4690

[6]

Chen, W.S. et al. Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes Dev. 15, 2203–2208 (2001). 10.1101/gad.913901

[7]

Peng, X.D. et al. Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev. 17, 1352–1365 (2003). 10.1101/gad.1089403

[8]

O'neill, B.T. & Abel, E.D. Akt1 in the cardiovascular system: friend or foe? J. Clin. Invest. 115, 2059–2064 (2005). 10.1172/jci25900

[9]

Shiojima, I. et al. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J. Clin. Invest. 115, 2108–2118 (2005). 10.1172/jci24682

[10]

Byzova, T.V. et al. A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol. Cell 6, 851–860 (2000).

[11]

Ruoslahti, E. & Engvall, E. Integrins and vascular extracellular matrix assembly. J. Clin. Invest. 99, 1149–1152 (1997). 10.1172/jci119269

[12]

Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions

Peter Carmeliet, Lieve Moons, Aernout Luttun et al.

Nature Medicine 2001 10.1038/87904

[13]

Byzova, T.V. et al. Adenovirus encoding vascular endothelial growth factor-D induces tissue-specific vascular patterns in vivo. Blood 99, 4434–4442 (2002). 10.1182/blood.v99.12.4434

[14]

Tammela, T., Enholm, B., Alitalo, K. & Paavonen, K. The biology of vascular endothelial growth factors. Cardiovasc. Res. 65, 550–563 (2005). 10.1016/j.cardiores.2004.12.002

[15]

Thurston, G. et al. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 286, 2511–2514 (1999). 10.1126/science.286.5449.2511

[16]

The Lack of Thrombospondin-1 (TSP1) Dictates the Course of Wound Healing in Double-TSP1/TSP2-Null Mice

Azin Agah, Themis R. Kyriakides, Jack Lawler et al.

The American Journal of Pathology 2002 10.1016/s0002-9440(10)64243-5

[17]

Bornstein, P. Thrombospondins as matricellular modulators of cell function. J. Clin. Invest. 107, 929–934 (2001). 10.1172/jci12749

[18]

Chen, J. et al. Impaired platelet responses to thrombin and collagen in AKT-1 deficient mice. Blood 104, 1703–1710 (2004). 10.1182/blood-2003-10-3428

[19]

Ackah, E. et al. Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J. Clin. Invest. 115, 2119–2127 (2005). 10.1172/jci24726

[20]

Mazure, N.M., Chen, E.Y., Laderoute, K.R. & Giaccia, A.J. Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. Blood 90, 3322–3331 (1997). 10.1182/blood.v90.9.3322

[21]

Arsham, A.M., Plas, D.R., Thompson, C.B. & Simon, M.C. Akt and hypoxia-inducible factor-1 independently enhance tumor growth and angiogenesis. Cancer Res. 64, 3500–3507 (2004). 10.1158/0008-5472.can-03-2239

[22]

Yu, J. et al. Endothelial nitric oxide synthase is critical for ischemic remodeling, mural cell recruitment, and blood flow reserve. Proc. Natl. Acad. Sci. USA 102, 10999–11004 (2005). 10.1073/pnas.0501444102

[23]

van Hinsbergh, V.W., Collen, A. & Koolwijk, P. Role of fibrin matrix in angiogenesis. Ann. NY Acad. Sci. 936, 426–437 (2001). 10.1111/j.1749-6632.2001.tb03526.x

[24]

Aicher, A. et al. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat. Med. 9, 1370–1376 (2003). 10.1038/nm948

[25]

Hotary, K.B. et al. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114, 33–45 (2003). 10.1016/s0092-8674(03)00513-0

[26]

Puolakkainen, P.A., Brekken, R.A., Muneer, S. & Sage, E.H. Enhanced growth of pancreatic tumors in SPARC-null mice is associated with decreased deposition of extracellular matrix and reduced tumor cell apoptosis. Mol. Cancer Res. 2, 215–224 (2004). 10.1158/1541-7786.215.2.4

[27]

Visse, R. & Nagase, H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92, 827–839 (2003). 10.1161/01.res.0000070112.80711.3d

[28]

Simantov, R. & Silverstein, R.L. CD36: a critical anti-angiogenic receptor. Front. Biosci. 8, s874–s882 (2003). 10.2741/1168

[29]

Rodriguez-Manzaneque, J.C. et al. Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc. Natl. Acad. Sci. USA 98, 12485–12490 (2001). 10.1073/pnas.171460498

[30]

Armstrong, L.C. et al. Thrombospondin 2 inhibits microvascular endothelial cell proliferation by a caspase-independent mechanism. Mol. Biol. Cell 13, 1893–1905 (2002). 10.1091/mbc.e01-09-0066

[31]

Lange-Asschenfeldt, B. et al. Increased and prolonged inflammation and angiogenesis in delayed-type hypersensitivity reactions elicited in the skin of thrombospondin-2–deficient mice. Blood 99, 538–545 (2002). 10.1182/blood.v99.2.538

[32]

Bornstein, P., Agah, A. & Kyriakides, T.R. The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury. Int. J. Biochem. Cell Biol. 36, 1115–1125 (2004). 10.1016/j.biocel.2004.01.012

[33]

Shiojima, I. & Walsh, K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ. Res. 90, 1243–1250 (2002). 10.1161/01.res.0000022200.71892.9f

[34]

Sun, J.F. et al. Microvascular patterning is controlled by fine-tuning the Akt signal. Proc. Natl. Acad. Sci. USA 102, 128–133 (2005). 10.1073/pnas.0403198102

[35]

Nagoshi, T. et al. PI3K rescues the detrimental effects of chronic Akt activation in the heart during ischemia/reperfusion injury. J. Clin. Invest. 115, 2128–2138 (2005). 10.1172/jci23073

[36]

Reynolds, L.E. et al. Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat. Med. 8, 27–34 (2002). 10.1038/nm0102-27

[37]

Dong, Q.G. et al. A general strategy for isolation of endothelial cells from murine tissues. Characterization of two endothelial cell lines from the murine lung and subcutaneous sponge implants. Arterioscler. Thromb. Vasc. Biol. 17, 1599–1604 (1997). 10.1161/01.atv.17.8.1599

[38]

Byzova, T.V., Kim, W., Midura, R.J. & Plow, E.F. Activation of integrin alpha(V)beta(3) regulates cell adhesion and migration to bone sialoprotein. Exp. Cell Res. 254, 299–308 (2000). 10.1006/excr.1999.4765

[39]

De, S. et al. Molecular pathway for cancer metastasis to bone. J. Biol. Chem. 278, 39044–39050 (2003). 10.1074/jbc.m304494200

[40]

Narizhneva, N.V. et al. Thrombospondin-1 up-regulates expression of cell adhesion molecules and promotes monocyte binding to endothelium. FASEB J. 19, 1158–1160 (2005). 10.1096/fj.04-3310fje

[41]

De, S. et al. VEGF-integrin interplay controls tumor growth and vascularization. Proc. Natl. Acad. Sci. USA 102, 7589–7594 (2005). 10.1073/pnas.0502935102

[42]

Takahashi, T. et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat. Med. 5, 434–438 (1999). 10.1038/7434

[43]

Han, E.D., MacFarlane, R.C., Mulligan, A.N., Scafidi, J. & Davis, A.E., III. Increased vascular permeability in C1 inhibitor-deficient mice mediated by the bradykinin type 2 receptor. J. Clin. Invest. 109, 1057–1063 (2002). 10.1172/jci200214211

[44]

Stockton, R.A., Schaefer, E. & Schwartz, M.A. p21-activated kinase regulates endothelial permeability through modulation of contractility. J. Biol. Chem. 279, 46621–46630 (2004). 10.1074/jbc.m408877200

[45]

Soula-Rothhut, M. et al. The tumor suppressor PTEN inhibits EGF-induced TSP-1 and TIMP-1 expression in FTC-133 thyroid carcinoma cells. Exp. Cell Res. 304, 187–201 (2005). 10.1016/j.yexcr.2004.10.026

Cited By

371

Bevacizumab-Based Therapy Is Associated with Prolonged Progression-Free Survival in Patients with Peritoneal Mucinous Metastatic Colorectal Cancer

Süleyman Can, Veli Çakıcı · 2026

Journal of Clinical Medicine

Gegen Qinlian pills alleviate carrageenan-induced thrombosis in mice model by regulating the HMGB1/NF-κB/NLRP3 signaling

Xiaohan Wei, Feiyan Wei · 2022

Phytomedicine

Astrocyte-Derived Thrombospondin-2 Is Critical for the Repair of the Blood-Brain Barrier

Weiming Tian, Andrew Sawyer · 2011

The American Journal of Pathology

Metrics

371

Citations

45

References

Details

Published: Oct 16, 2005
Vol/Issue: 11(11)
Pages: 1188-1196
License: View

Authors

J

Juhua Chen

P

Payaningal R Somanath

O

Olga Razorenova

Division of Radiation and Cancer Biology, Department of Radiation Oncology, Center for Clinical Sciences Research, Department of Radiation Oncology, Stanford University, Stanford, California 94303-5152

Department of Biochemistry, University of Washington, Seattle, Wash. 98105; Department of Medicine, University of Washington, Seattle, Wash. 98105

T

Tatiana V Byzova

Cite This Article

Juhua Chen, Payaningal R Somanath, Olga Razorenova, et al. (2005). Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nature Medicine, 11(11), 1188-1196. https://doi.org/10.1038/nm1307

Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo

You May Also Like