Golgi-associated cPLA2α regulates endothelial cell-cell junction integrity by controlling the trafficking of transmembrane junction proteins

Molecular Biology of the Cell

Volumn 20, Issue 19, 2009, Pages 4225-4234

  Regan Klapisz, Elsa ^a,b   Krouwer, Vincent ^a   Langelaar Makkinje, Miriam ^a   Nallan, Laxman ^c   Gelb, Michael ^c   Gerritsen, Hans ^b   Verkleij, Arie J ^a   Post, Jan Andries ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 5; OCCLUDIN; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2ALPHA; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; ANTIBODY; CADHERIN; CLDN5 PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN; PHOSPHOLIPASE A2 GROUP IV;

ARTICLE; CELL INTERACTION; CELL JUNCTION; CONTROLLED STUDY; CYTOPLASM; ENDOTHELIUM CELL; ENZYME ACTIVITY; GOLGI COMPLEX; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TIGHT JUNCTION; CELL CULTURE; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOLOGY; METABOLISM; PROTEIN TRANSPORT; RNA INTERFERENCE; WESTERN BLOTTING;

ADHERENS JUNCTIONS; ANTIBODIES; ANTIGENS, CD; BLOTTING, WESTERN; CADHERINS; CELLS, CULTURED; CYTOPLASM; ENDOTHELIAL CELLS; GOLGI APPARATUS; GROUP IV PHOSPHOLIPASES A2; HUMANS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; RNA INTERFERENCE; TIGHT JUNCTIONS;

EID: 70350214396     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-02-0210     Document Type: Article

References (51)

1. Adler, D. H., et al. (2008). Inherited human cPLA2α deficiency is associated with impaired eicosanoid biosynthesis, small intestinal ulceration, and platelet dysfunction. J. Clin. Invest. 118, 2121-2131.
2. Bazzoni, G., and Dejana, E. (2004). Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84, 869-901.
3. Braga, V. M., and Yap, A. S. (2005). The challenges of abundance: epithelial junctions and small GTPase signalling. Curr. Opin. Cell Biol. 17, 466-474.
4. Brown, W. J., Chambers, K., and Doody, A. (2003). Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 4, 214-221. (Pubitemid 36665382)
5. Bryant, D. M., and Stow, J. L. (2004). The ins and outs of E-cadherin trafficking. Trends Cell Biol. 14, 427-434.
6. Bunt, G., de Wit, J., van den Bosch, H., Verkleij, A. J., and Boonstra, J. (1997). Ultrastructural localization of cPLA2 in unstimulated and EGF/A23187-stimulated fibroblasts. J. Cell Sci. 110(Pt 19), 2449-2459. (Pubitemid 127699159)
7. Choukroun, G. J., Marshansky, V., Gustafson, C. E., McKee, M., Hajjar, R. J., Rosenzweig, A., Brown, D., and Bonventre, J. V. (2000). Cytosolic phospholipase A(2) regulates golgi structure and modulates intracellular trafficking of membrane proteins. J. Clin. Invest. 106, 983-993.
8. Clark, J. D., Lin, L. L., Kriz, R. W., Ramesha, C. S., Sultzman, L. A., Lin, A. Y., Milona, N., and Knopf, J. L. (1991). A novel arachidonic acid-selective cytosolic PLA2 contains a Ca(2+)-dependent translocation domain with homology to PKC and GAP. Cell 65, 1043-1051.
9. Corada, M., Liao, F., Lindgren, M., Lampugnani, M. G., Breviario, F., Frank, R., Muller, W. A., Hicklin, D. J., Bohlen, P., and Dejana, E. (2001). Monoclonal antibodies directed to different regions of vascular endothelial cadherin extracellular domain affect adhesion and clustering of the protein and modulate endothelial permeability. Blood 97, 1679-1684. (Pubitemid 32217233)
10. Darios, F., and Davletov, B. (2006). Omega-3 and omega-6 fatty acids stimulate cell membrane expansion by acting on syntaxin 3. Nature 440, 813-817.
11. Davletov, B., Connell, E., and Darios, F. (2007). Regulation of SNARE fusion machinery by fatty acids. Cell Mol. Life Sci. 64, 1597-1608.
12. de Figueiredo, P., Polizotto, R. S., Drecktrah, D., and Brown, W. J. (1999). Membrane tubule-mediated reassembly and maintenance of the Golgi complex is disrupted by phospholipase A2 antagonists. Mol. Biol. Cell 10, 1763-1782.
13. Dejana, E. (2004). Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5, 261-270.
14. Dessus-Babus, S., Knight, S. T., and Wyrick, P. B. (2000). Chlamydial infection of polarized HeLa cells induces PMN chemotaxis but the cytokine profile varies between disseminating and non-disseminating strains. Cell Microbiol. 2, 317-327. (Pubitemid 30612941)
15. Downey, P., Sapirstein, A., O'Leary, E., Sun, T. X., Brown, D., and Bonventre, J. V. (2001). Renal concentrating defect in mice lacking group IV cytosolic phospholipase A(2). Am. J. Physiol. Renal Physiol. 280, F607-F618.
16. Evans, C. E., Billington, D., and McEvoy, F. A. (1984). Prostacyclin production by confluent and non-confluent human endothelial cells in culture. Prostaglandins Leukot. Med. 14, 255-266.
17. Evans, J. H., and Leslie, C. C. (2004). The cytosolic phospholipase A2 catalytic domain modulates association and residence time at Golgi membranes. J. Biol. Chem. 279, 6005-6016.
18. Evans, J. H., Spencer, D. M., Zweifach, A., and Leslie, C. C. (2001). Intracellular calcium signals regulating cytosolic phospholipase A2 translocation to internal membranes. J. Biol. Chem. 276, 30150-30160.
19. Fukuhara, S., Sakurai, A., Sano, H., Yamagishi, A., Somekawa, S., Takakura, N., Saito, Y., Kangawa, K., and Mochizuki, N. (2005). Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol. Cell. Biol. 25, 136-146.
20. Ghosh, M., Loper, R., Ghomashchi, F., Tucker, D. E., Bonventre, J. V., Gelb, M. H., and Leslie, C. C. (2007). Function, activity, and membrane targeting of cytosolic phospholipase A2ζ in mouse lung fibroblasts. J. Biol. Chem. 282, 11676-11686.
21. Ghosh, M., Tucker, D. E., Burchett, S. A., and Leslie, C. C. (2006). Properties of the Group IV phospholipase A2 family. Prog. Lipid Res. 45, 487-510.
22. Grewal, S., Ponnambalam, S., and Walker, J. H. (2003). Association of cPLA2α and COX-1 with the Golgi apparatus of A549 human lung epithelial cells. J. Cell Sci. 116, 2303-2310. (Pubitemid 36722376)
23. Grimmer, S., Ying, M., Walchli, S., van Deurs, B., and Sandvig, K. (2005). Golgi vesiculation induced by cholesterol occurs by a dynamin- and cPLA2-dependent mechanism. Traffic 6, 144-156.
24. Herbert, S. P., Odell, A. F., Ponnambalam, S., and Walker, J. H. (2007). The confluence-dependent interaction of cytosolic phospholipase A2α with annexin A1 regulates endothelial cell prostaglandin E2 generation. J. Biol. Chem. 282, 34468-34478.
25. Herbert, S. P., Ponnambalam, S., and Walker, J. H. (2005). Cytosolic phospholipase A2α mediates endothelial cell proliferation and is inactivated by association with the Golgi apparatus. Mol. Biol. Cell 16, 3800-3809.
26. Hordijk, P. L., Anthony, E., Mul, F. P., Rientsma, R., Oomen, L. C., and Roos, D. (1999). Vascular-endothelial-cadherin modulates endothelial monolayer permeability. J. Cell Sci. 112(Pt 12), 1915-1923. (Pubitemid 29338816)
27. Jaffe, E. A., Nachman, R. L., Becker, C. G., and Minick, C. R. (1973). Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J. Clin. Invest. 52, 2745-2756.
28. Klapisz, E., Sorokina, I., Lemeer, S., Pijnenburg, M., Verkleij, A. J., and van Bergen en Henegouwen, P.M. (2002). A ubiquitin-interacting motif (UIM) is essential for Eps15 and Eps15R ubiquitination. J. Biol. Chem. 277, 30746-30753.
29. Kuroiwa, N., Nakamura, M., Tagaya, M., and Takatsuki, A. (2001). Arachidonyltrifluoromethy ketone, a phospholipase A(2) antagonist, induces dispersal of both Golgi stack- and trans Golgi network-resident proteins throughout the cytoplasm. Biochem. Biophys. Res. Commun. 281, 582-588.
30. Leslie, C. C. (2004). Regulation of the specific release of arachidonic acid by cytosolic phospholipase A2. Prostaglandins Leukot. Essent. Fatty Acids 70, 373-376.
31. Liebner, S., Cavallaro, U., and Dejana, E. (2006). The multiple languages of endothelial cell-to-cell communication. Arterioscler. Thromb. Vasc. Biol. 26, 1431-1438.
32. Mege, R. M., Gavard, J., and Lambert, M. (2006). Regulation of cell-cell junctions by the cytoskeleton. Curr. Opin. Cell Biol. 18, 541-548.
33. Mogelsvang, S., and Howell, K. E. (2006). Global approaches to study Golgi function. Curr. Opin. Cell Biol. 18, 438-443.
34. Myou, S., Leff, A. R., Myo, S., Boetticher, E., Meliton, A. Y., Lambertino, A. T., Liu, J., Xu, C., Munoz, N. M., and Zhu, X. (2003). Activation of group IV cytosolic phospholipase A2 in human eosinophils by phosphoinositide 3-kinase through a mitogen-activated protein kinase-independent pathway. J. Immunol. 171, 4399-4405. (Pubitemid 37238719)
35. Nakamura, N., Lowe, M., Levine, T. P., Rabouille, C., and Warren, G. (1997). The vesicle docking protein p115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner. Cell 89, 445-455. (Pubitemid 27220889)
36. Ni, Z., Okeley, N. M., Smart, B. P., and Gelb, M. H. (2006). Intracellular actions of group IIA secreted phospholipase A2 and group IVA cytosolic phospholipase A2 contribute to arachidonic acid release and prostaglandin production in rat gastric mucosal cells and transfected human embryonic kidney cells. J. Biol. Chem. 281, 16245-16255.
37. Ono, T., Yamada, K., Chikazawa, Y., Ueno, M., Nakamoto, S., Okuno, T., and Seno, K. (2002). Characterization of a novel inhibitor of cytosolic phospholipase A2alpha, pyrrophenone. Biochem. J. 363, 727-735. (Pubitemid 34526393)
38. Pulvirenti, T., et al. (2008). A traffic-activated Golgi-based signalling circuit coordinates the secretory pathway. Nat. Cell Biol 10, 912-922.
39. San Pietro, E., et al. (2009). Group IV phospholipase A2α controls the formation of inter-cisternal continuities involved in intra-Golgi transport. PLoS Biol. 7, e1000194.
40. Schaloske, R. H., and Dennis, E. A. (2006). The phospholipase A2 superfamily and its group numbering system. Biochim. Biophys. Acta 1761, 1246-1259.
41. Schievella, A. R., Regier, M. K., Smith, W. L., and Lin, L. L. (1995). Calcium-mediated translocation of cytosolic phospholipase A2 to the nuclear envelope and endoplasmic reticulum. J. Biol. Chem. 270, 30749-30754.
42. Seno, K., et al. (2000). Pyrrolidine inhibitors of human cytosolic phospholipase A(2). J. Med. Chem. 43, 1041-1044.
43. Seno, K., Okuno, T., Nishi, K., Murakami, Y., Yamada, K., Nakamoto, S., and Ono, T. (2001). Pyrrolidine inhibitors of human cytosolic phospholipase A2. Part 2, synthesis of potent and crystallized 4-triphenylmethylthio derivative 'pyrrophenone.' Bioorg. Med. Chem. Lett. 11, 587-590.
44. Shimojo, Y., Hosaka, S., Usuda, N., and Nagata, T. (1995). The induction of junctional complexes of HeLa cells by Agar culture. Med. Electron Microsc. 28, 57-62.
45. Silfani, T. N., and Freeman, E. J. (2002). Phosphatidylinositide 3-kinase regulates angiotensin II-induced cytosolic phospholipase A2 activity and growth in vascular smooth muscle cells. Arch Biochem. Biophys. 402, 84-93.
46. Taddei, A., Giampietro, C., Conti, A., Orsenigo, F., Breviario, F., Pirazzoli, V., Potente, M., Daly, C., Dimmeler, S., and Dejana, E. (2008). Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat. Cell Biol 10, 923-934.
47. van Nieuw Amerongen, G. P., and van Hinsbergh, V. W. (2002). Targets for pharmacological intervention of endothelial hyperpermeability and barrier function. Vascul. Pharmacol. 39, 257-272.
48. Whatley, R. E., Satoh, K., Zimmerman, G. A., McIntyre, T. M., and Prescott, S. M. (1994). Proliferation-dependent changes in release of arachidonic acid from endothelial cells. J. Clin. Invest. 94, 1889-1900.
49. Xiao, K., Oas, R. G., Chiasson, C. M., and Kowalczyk, A. P. (2007). Role of p120-catenin in cadherin trafficking. Biochim. Biophys. Acta 1773, 8-16.
50. Yap, A. S., Crampton, M. S., and Hardin, J. (2007). Making and breaking contacts: the cellular biology of cadherin regulation. Curr. Opin. Cell Biol. 19, 508-514.
51. Zimmerberg, J., and Kozlov, M. M. (2006). How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7, 9-19.