Endothelial PI3K-C2α, a class II PI3K, has an essential role in angiogenesis and vascular barrier function

Nature Medicine

Volumn 18, Issue 10, 2012, Pages 1560-1569

  Yoshioka, Kazuaki ^a   Yoshida, Kotaro ^a   Cui, Hong ^a   Wakayama, Tomohiko ^a   Takuwa, Noriko ^a,b   Okamoto, Yasuo ^a   Du, Wa ^a   Qi, Xun ^a   Asanuma, Ken ^c   Sugihara, Kazushi ^d   Aki, Sho ^a   Miyazawa, Hidekazu ^a   Biswas, Kuntal ^a   Nagakura, Chisa ^a   Ueno, Masaya ^e   Iseki, Shoichi ^a   Schwartz, Robert J ^f   Okamoto, Hiroshi ^g   Sasaki, Takehiko ^c,h   Matsui, Osamu ^a   Asano, Masahide ^d   Adams, Ralf H ^i,j   Takakura, Nobuyuki ^e   Takuwa, Yoh ^a   more..

^a KANAZAWA UNIV SCHOOL OF MEDICINE   (Japan)

^b ISHIKAWA PREFECTURAL NURSING UNIVERSITY   (Japan)

^c AKITA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d KANAZAWA UNIVERSITY   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f University of Houston   (United States)

^g TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^h AKITA UNIVERSITY   (Japan)

ⁱ MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^j UNIVERSITY OF MÜNSTER   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 3 KINASE; VASCULAR ENDOTHELIAL CADHERIN;

ANAPHYLAXIS; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA DISSECTING ANEURYSM; ARTICLE; CELL JUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENDOSOME; ENDOTHELIUM CELL; ENZYME DEFICIENCY; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN ASSEMBLY;

ANGIOTENSIN II; ANIMALS; ANTIGENS, CD; BLOOD-AIR BARRIER; CADHERINS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CLATHRIN-COATED VESICLES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANS-GOLGI NETWORK;

EID: 84870299287     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2928     Document Type: Article

References (61)

1. Adams, R.H. & Alitalo, K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 8, 464-478 (2007).
2. Coultas, L. et al. Endothelial cells and VEGF in vascular development. Nature 438, 937-945 (2005).
3. Andrae, J. et al. Role of platelet-derived growth factor in physiology and medicine. Genes Dev. 22, 1276-1312 (2008).
4. Mehta, D. & Malik, A.B. Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 86, 279-367 (2006).
5. Dejana, E., Tournier-Lasserve, E. & Weinstein, B.M. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev. Cell 16, 209-221 (2009).
6. Yoshimura, K. et al. Regression of abdominal aortic aneurysm by inhibition of c-Jun N-terminal kinase. Nat. Med. 11, 1330-1338 (2005).
7. Satoh, K. et al. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat. Med. 15, 649-656 (2009).
8. Ferrara, N. & Kerbel, R.S. Angiogenesis as a therapeutic target. Nature 438, 967-974 (2005).
9. Carmeliet, P. Angiogenesis in life, disease and medicine. Nature 438, 932-936 (2005).
10. Engelman, J.A. et al. The evolution of phosphatidylinositol 3-kinases as regulator of growth and metabolism. Nat. Rev. Genet. 7, 606-619 (2006).
11. Takenawa, T. & Suetsugu, S. The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 8, 37-48 (2007).
12. Vanhaesebroeck, B. et al. The emerging mechanisms of isoform-specifc PI3K signaling. Nat. Rev. Mol. Cell Biol. 11, 329-341 (2010).
13. Graupera, M. et al. Angiogenesis selectively requires the p110α isoform of PI3K to control endothelial cell migration. Nature 453, 662-666 (2008).
14. Yuan, T.L. & Cantley, L.C. PI3K pathway alterations in cancer: variations on a theme. Oncogene 27, 5497-5510 (2008).
15. Funderburk, S.F. et al. The Beclin 1-Vps34 complex at the crossroads of autophagy and beyond. Trends Cell Biol. 20, 355-362 (2010).
16. Falasca, M. et al. The role of phosphoinositide 3-kinase C2α in insulin signaling. J. Biol. Chem. 282, 28226-28236 (2007).
17. Linassier, C. et al. Molecular cloning and biochemical characterization of a Drosophila phosphatidylinositol-specifc phosphoinositide 3-kinase. Biochem. J. 321, 849-856 (1997).
18. Domin, J. et al. The class II phosphoinositide 3-kinase PI3K-C2α is concentrated in the trans-Golgi network and present in clathrin-coated vesicles. J. Biol. Chem. 275, 11943-11950 (2000).
19. El Sheikh, S.S. et al. Topographical expression of class IA and class II phosphoinositide 3-kinase enzymes in normal human tissues is consistent with a role in differentiation. BMC Clin. Pathol. 3, 4 (2003).
20. 2+-induced, Rho-and Rho kinase-dependent regulation of myosin phosphatase and contraction in isolated vascular smooth muscle cells. Mol. Pharmacol. 71, 912-920 (2007).
21. Traer, C.J. et al. Are class II phosphoinositide 3-kinases potential targets for anticancer therapies? Bull. Cancer 93, E53-E58 (2006).
22. Gaidarov, I. et al. Individual phosphoinositide 3-kinase C2α domain activities independently regulate clathrin function. J. Biol. Chem. 280, 40766-40772 (2005).
23. Falasca, M. & Maffucci, T. Role of class II phosphoinositide 3-kinase in cell signalling. Biochem. Soc. Trans. 35, 211-214 (2007).
24. Wang, Y. et al. Class II phosphoinositide 3-kinase α-isoform regulates Rho, myosin phosphatase and contraction in vascular smooth muscle. Biochem. J. 394, 581-592 (2006).
25. Harris, D.P. et al. Requirement for class II phosphoinositide 3-kinase C2α in maintenance of glomerular structure and function. Mol. Cell. Biol. 31, 63-80 (2011).
26. Moses, K.A. et al. Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 31, 176-180 (2001).
27. Kisanuki, Y.Y. et al. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230, 230-242 (2001).
28. Wang, Y. et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486 (2010).
29. Pannekoek, W.J. et al. Cell-cell junction formation: the role of Rap1 and Rap1 guanine nucleotide exchange factors. Biochim. Biophys. Acta 1788, 790-796 (2009).
30. Gillooly, D.J. et al. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588 (2000).
31. Lindmo, K. & Stenmark, H. Regulation of membrane traffc by phosphoinositide 3-kinase. J. Cell Sci. 119, 605-614 (2006).
32. Di Paolo, G. & De Camilli, P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 (2006).
33. Bryan, B.A. et al. RhoA/ROCK signaling is essential for multiple aspects of VEGF-mediated angiogenesis. FASEB J. 24, 3186-3196 (2010).
34. Macia, E. et al. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850 (2006).
35. Cauwels, A. et al. Anaphylactic shock depends on PI3K and eNOS-derived NO. J. Clin. Invest. 116, 2244-2251 (2006).
36. Daugherty, A. & Cassis, L.A. Mouse models of abdominal aortic aneurysms. Arterioscler. Thromb. Vasc. Biol. 24, 429-434 (2004).
37. Di Gennaro, A. et al. Increased expression of leukotriene C4 synthase and predominant formation of cysteinyl-leukotrienes in human abdominal aortic aneurysm. Proc. Natl. Acad. Sci. USA 107, 21093-21097 (2010).
38. Wheeler, M. & Domin, J. The N-terminus of phosphoinositide 3-kinase-C2β regulates lipid kinase activity and binding to clathrin. J. Cell. Physiol. 206, 586-593 (2006).
39. Simonsen, A. & Tooze, S.A. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J. Cell Biol. 186, 773-782 (2009).
40. Johnson, E.E. et al. Gene silencing reveals a specifc function of hVps34 phosphatidylinositol 3-kinase in late versus early endosomes. J. Cell Sci. 119, 1219-1232 (2006).
41. Doherty, G.J. & McMahon, H.T. Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 31.1-31.46 (2009).
42. Zoncu, R. et al. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136, 1110-1121 (2009).
43. Palamidessi, A. et al. Endocytic traffcking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134, 135-147 (2008).
44. van Nieuw Amerongen, G.P. et al. Involvement of Rho kinase in endothelial barrier maintenance. Arterioscler. Thromb. Vasc. Biol. 27, 2332-2339 (2007).
45. Yamada, S. & Nelson, W.J. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 178, 517-527 (2007).
46. Harris, T.J.C. & Tepass, U. Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11, 502-514 (2010).
47. Abraham, S. et al. VE-cadherin-mediated cell-cell interaction suppresses sprouting via signaling to MLC2 phosphorylation. Curr. Biol. 19, 668-674 (2009).
48. Noda, K. et al. Vascular endothelial-cadherin stabilizes at cell-cell junctions by anchoring to circumferential actin bundles through α-and β-catenins in cyclic AMP-Epac-Rap1 signal-activated endothelial cells. Mol. Biol. Cell 21, 584-596 (2010).
49. Webb, D.J., Parsons, J.T. & Horwits, A.F. Adhesion assembly, disassembly and turnover in migrating cells\over and over and over again. Nat. Cell Biol. 4, E97-E100 (2002).
50. Mitra, S.K., Hanson, D.A. & Schlaepfer, D.D. Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol 6, 56-68 (2005).
51. Shivas, J.M. et al. Polarity and endocytosis: reciprocal regulation. Trends Cell Biol. 20, 445-452 (2010).
52. Sörensen, I., Adams, R.H. & Gossler, A. Dll1-mediated Notch activation regulates endothelial identity in mouse fetal arteries. Blood 113, 5680-5688 (2009).
53. Bazigou, E. et al. Integrin-α9 is required for fbronectin matrix assembly during lymphatic valve morphogenesis. Dev. Cell 17, 175-186 (2009).
54. Takakura, N. et al. Critical role of the TIE2 endothelial cell receptor in the development of defnitive hematopoiesis. Immunity 9, 677-686 (1998).
55. Benedito, R. et al. The Notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137, 1124-1135 (2009).
56. Compagni, A. et al. Control of skeletal patterning by ephrinB1-EphB interactions. Dev. Cell 5, 217-230 (2003).
57. Oyama, O. et al. The lysophospholipid mediator sphingosine-1-phosphate promotes angiogenesis in vivo in ischemic hindlimbs of mice. Cardiovasc. Res. 78, 301-307 (2008).
58. 2, the G protein-coupled receptor for sphingosine-1-phosphate, negatively regulates tumor angiogenesis and tumor growth in vivo in mice. Cancer Res. 70, 772-781 (2010).
59. Deng, G.G. et al. Urokinase-type plasminogen activator plays a critical role in angiotensin II-induced abdominal aortic aneurysm. Circ. Res. 92, 510-517 (2003).
60. Okamoto, H. et al. Inhibitory regulation of Rac activation, membrane ruffing, and cell migration by the G protein-coupled sphingosine-1-phosphate receptor EDG5 but not EDG1 or EDG3. Mol. Cell. Biol. 20, 9247-9261 (2000).
61. Sasaki, T. et al. Function of PI3Kγ in thymocyte development, T cell activation, and neutrophil migration. Science 287, 1040-1046 (2000).