Angiopoietin-2 secretion by endothelial cell exosomes: Regulation by the phosphatidylinositol 3-kinase (PI3K)/Akt/endothelial nitric oxide synthase (eNOS) and syndecan-4/syntenin pathways

Journal of Biological Chemistry

Volumn 289, Issue 1, 2014, Pages 510-519

  Ju, Rong ^a,b   Zhuang, Zhen W ^a   Zhang, Jiasheng ^a   Lanahan, Anthony A ^a   Kyriakides, Themis ^a   Sessa, William C ^a   Simons, Michael ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; PHYSIOLOGY; PIGMENTS;

ANGIOPOIETIN-2; ANGIOPOIETINS; CRITICAL SIGNALING PATHWAYS; EXTRACELLULAR PROTEINS; NITRIC-OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3-KINASE; SIGNALING PATHWAYS; VASCULAR GROWTHS;

ENDOTHELIAL CELLS;

ANGIOPOIETIN 2; ENDOTHELIAL NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SYNDECAN 4; SYNTENIN; AKT1 PROTEIN, MOUSE; NOS3 PROTEIN, MOUSE; SDC4 PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAPILLARY DENSITY; CELL LEVEL; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME REGULATION; EXOME; FLOW RATE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CYTOLOGY; EXOSOME; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

ANGIOPOIETIN-2; ANIMALS; CELLS, CULTURED; ENDOTHELIAL CELLS; EXOSOMES; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SYNDECAN-4; SYNTENINS;

EID: 84891699959     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.506899     Document Type: Article

References (33)

1. Augustin, H. G., Koh, G. Y., Thurston, G., and Alitalo, K. (2009) Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat. Rev. Mol. Cell Biol. 10, 165-177
2. 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 (Pubitemid 27010101)
3. Maisonpierre, P. C., Suri, C., Jones, P. F., Bartunkova, S., Wiegand, S. J., Radziejewski, C., Compton, D., McClain, J., Aldrich, T. H., Papadopoulos, N., Daly, T. J., Davis, S., Sato, T. N., and Yancopoulos, G. D. (1997) Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277, 55-60 (Pubitemid 27450643)
4. Yuan, H. T., Khankin, E. V., Karumanchi, S. A., and Parikh, S. M. (2009) Angiopoietin 2 is a partial agonist/antagonist of Tie2 signaling in the endothelium. Mol. Cell. Biol. 29, 2011-2022
5. Daly, C., Eichten, A., Castanaro, C., Pasnikowski, E., Adler, A., Lalani, A. S., Papadopoulos, N., Kyle, A. H., Minchinton, A. I., Yancopoulos, G. D., and Thurston, G. (2013) Angiopoietin-2 functions as a Tie2 agonist in tumor models, where it limits the effects of VEGF inhibition. Cancer Res. 73, 108-118
6. Fiedler, U., Scharpfenecker, M., Koidl, S., Hegen, A., Grunow, V., Schmidt, J. M., Kriz, W., Thurston, G., and Augustin, H. G. (2004) The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood 103, 4150-4156 (Pubitemid 38685356)
7. Tsigkos, S., Zhou, Z., Kotanidou, A., Fulton, D., Zakynthinos, S., Roussos, C., and Papapetropoulos, A. (2006) Regulation of Ang2 release by PTEN/PI3-kinase/Akt in lung microvascular endothelial cells. J. Cell. Physiol. 207, 506-511
8. Gross, J. C., Chaudhary, V., Bartscherer, K., and Boutros, M. (2012) Active Wnt proteins are secreted on exosomes. Nat. Cell Biol. 14, 1036-1045
9. Théry, C. (2011) Exosomes: secreted vesicles and intercellular communications. F1000 Biol. Rep. 3, 15
10. Hanson, P. I., and Cashikar, A. (2012) Multivesicular body morphogenesis. Annu. Rev. Cell Dev. Biol. 28, 337-362
11. Baietti, M. F., Zhang, Z., Mortier, E., Melchior, A., Degeest, G., Geeraerts, A., Ivarsson, Y., Depoortere, F., Coomans, C., Vermeiren, E., Zimmermann, P., and David, G. (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell Biol. 14, 677-685
12. Choi, Y., Chung, H., Jung, H., Couchman, J. R., and Oh, E. S. (2011) Syndecans as cell surface receptors: Unique structure equates with functional diversity. Matrix Biol. 30, 93-99
13. Gao, Y., Li, M., Chen, W., and Simons, M. (2000) Synectin, syndecan-4 cytoplasmic domain binding PDZ protein, inhibits cell migration. J. Cell. Physiol. 184, 373-379 (Pubitemid 30625501)
14. Grootjans, J. J., Zimmermann, P., Reekmans, G., Smets, A., Degeest, G., Dürr, J., and David, G. (1997) Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl. Acad. Sci. U. S. A. 94, 13683-13688 (Pubitemid 28009643)
15. Tkachenko, E., Elfenbein, A., Tirziu, D., and Simons, M. (2006) Syndecan-4 clustering induces cell migration in a PDZ-dependent manner. Circ. Res. 98, 1398-1404 (Pubitemid 43948064)
16. Elfenbein, A., Rhodes, J. M., Meller, J., Schwartz, M. A., Matsuda, M., and Simons, M. (2009) Suppression of RhoG activity is mediated by a syndecan 4-synectin-RhoGDI1 complex and is reversed by PKCα in a Rac1 activation pathway. J. Cell Biol. 186, 75-83
17. Zimmermann, P., Zhang, Z., Degeest, G., Mortier, E., Leenaerts, I., Coomans, C., Schulz, J., N'Kuli, F., Courtoy, P. J., and David, G. (2005) Syndecan recycling [corrected] is controlled by syntenin-PIP2 interaction and Arf6. Dev. Cell 9, 377-388 (Pubitemid 41235807)
18. Morgan, M. R., Hamidi, H., Bass, M. D., Warwood, S., Ballestrem, C, and Humphries, M. J. (2013) Syndecan-4 phosphorylation is a control point for integrin recycling. Dev. Cell 24, 472-485
19. Partovian, C., Ju, R., Zhuang, Z. W., Martin, K. A., and Simons, M. (2008) Syndecan-4 regulates subcellular localization of mTOR Complex2 and Akt activation in aPKCα-dependent manner in endothelial cells. Mol. Cell 32, 140-149
20. Ju, R., and Simons, M. (2013) Syndecan 4 regulation of PDK1-dependent Akt activation. Cell Signal 25, 101-105
21. Karar, J., and Maity, A. (2011) PI3K/AKT/mTOR Pathway in Angiogenesis. Front Mol. Neurosci. 4, 51
22. Ackah, E., Yu, J., Zoellner, S., Iwakiri, Y., Skurk, C., Shibata, R., Ouchi, N., Easton, R. M., Galasso, G., Birnbaum, M. J., Walsh, K., and Sessa, W. C. (2005) Akt1/protein kinase Bα is critical for ischemic and VEGF-mediated angiogenesis. J. Clin. Invest. 115, 2119-2127 (Pubitemid 41134153)
23. Chen, J., Somanath, P. R., Razorenova, O., Chen, W. S., Hay, N., Bornstein, P., and Byzova, T. V. (2005) Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat. Med. 11, 1188-1196 (Pubitemid 43093666)
24. Schleicher, M., Yu, J., Murata, T., Derakhshan, B., Atochin, D., Qian, L., Kashiwagi, S., Di Lorenzo, A., Harrison, K. D., Huang, P. L., and Sessa, W. C. (2009) The Akt1-eNOS axis illustrates the specificity of kinasesubstrate relationships in vivo. Sci. Signal. 2, ra41
25. Matsushita, K., Morrell, C. N., Cambien, B., Yang, S. X., Yamakuchi, M., Bao, C., Hara, M. R., Quick, R. A., Cao, W., O'Rourke, B., Lowenstein, J. M., Pevsner, J., Wagner, D. D., and Lowenstein, C. J. (2003) Nitric oxide regulates exocytosis by S-nitrosylation of N-ethylmaleimide-sensitive factor. Cell 115, 139-150 (Pubitemid 37329578)
26. Thery, C., Amigorena, S., Raposo, G., and Clayton, A. (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Current Protocols in Cell Biology, pp. 30:3. 22.1-3.22.29, Wiley and Sons, Hoboken, NJ
27. Ishiguro, K., Kadomatsu, K., Kojima, T., Muramatsu, H., Iwase, M., Yoshikai, Y., Yanada, M., Yamamoto, K., Matsushita, T., Nishimura, M., Kusugami, K., Saito, H., and Muramatsu, T. (2001) Syndecan-4 deficiency leads to high mortality of lipopolysaccharide-injected mice. J. Biol. Chem. 276, 47483-47488
28. Cho, H., Thorvaldsen, J. L., Chu, Q., Feng, F., and Birnbaum, M. J. (2001) Akt1/PKBα is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J. Biol. Chem. 276, 38349-38352
29. Tang, M., Li, J., Huang, W., Su, H., Liang, Q., Tian, Z., Horak, K. M., Molkentin, J. D., and Wang, X. (2010) Proteasome functional insufficiency activates the calcineurin-NFAT pathway in cardiomyocytes and promotes maladaptive remodelling of stressed mouse hearts. Cardiovasc. Res. 88, 424-433
30. Zagorchev, L., Oses, P., Zhuang, Z. W., Moodie, K., Mulligan-Kehoe, M. J., Simons, M., and Couffinhal, T. (2010) Micro computed tomography for vascular exploration. J Angiogenes. Res. 2, 7
31. Alexopoulou, A. N., Multhaupt, H. A., and Couchman, J. R. (2007) Syndecans in wound healing, inflammation and vascular biology. Int. J. Biochem. Cell Biol. 39, 505-528 (Pubitemid 46099032)
32. Fiedler, U., and Augustin, H. G. (2006) Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol. 27, 552-558 (Pubitemid 44780853)
33. Gerald, D., Chintharlapalli, S., Augustin, H. G., and Benjamin, L. E. (2013) Angiopoietin-2: an attractive target for improved antiangiogenic tumor therapy. Cancer Res. 73, 1649-1657