The Epac-Rap1 signaling pathway controls cAMP-mediated exocytosis of Weibel-Palade bodies in endothelial cells

Journal of Biological Chemistry

Volumn 287, Issue 29, 2012, Pages 24713-24720

  Van Hooren, Kathinka W E M ^a   Van Agtmaal, Ellen L ^a   Fernandez Borja, Mar ^a   Van Mourik, Jan A ^a   Voorberg, Jan ^a   Bierings, Ruben ^a  

^a SANQUIN RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DOWN-REGULATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; INTRACELLULAR CA; OVER-EXPRESSION; PROTEIN KINASE A; SIGNALING PATHWAYS; VASCULAR LUMEN; WEIBEL-PALADE BODIES;

ENZYMES;

ENDOTHELIAL CELLS;

ADRENALIN; CARRIER PROTEIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; EXCHANGE PROTEIN ACTIVATED BY CAMP 1; RAP1 PROTEIN; SMALL INTERFERING RNA; THROMBIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; EXOCYTOSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WEIBEL PALADE BODY;

CELLS, CULTURED; CYCLIC AMP; ENDOTHELIAL CELLS; EXOCYTOSIS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; RAP1 GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UMBILICAL VEINS; WEIBEL-PALADE BODIES;

EID: 84863799076     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.321976     Document Type: Article

References (51)

1. Weibel, E. R., and Palade, G. E. (1964) New cytoplasmic components in arterial endothelia. J. Cell Biol. 23, 101-112
2. Metcalf, D. J., Nightingale, T. D., Zenner, H. L., Lui-Roberts, W. W., and Cutler, D. F. (2008) Formation and function of Weibel-Palade bodies. J. Cell Sci. 121, 19-27 (Pubitemid 351265699)
3. Rondaij, M. G., Bierings, R., Kragt, A., van Mourik, J. A., and Voorberg, J. (2006) Dynamics and plasticity of Weibel-Palade Bodies in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 26, 1002-1007 (Pubitemid 43732104)
4. Kaufmann, J. E., Oksche, A., Wollheim, C. B., Günther, G., Rosenthal, W., and Vischer, U. M. (2000) Vasopressin-induced von Willebrand factor secretion from endothelial cells involves V2 receptors and cAMP. J. Clin. Invest. 106, 107-116 (Pubitemid 30437246)
5. Vischer, U. M., and Wollheim, C. B. (1997) Epinephrine induces von Willebrand factor release from cultured endothelial cells. Involvement of cyclic AMP-dependent signaling in exocytosis. Thromb. Haemost. 77, 1182-1188 (Pubitemid 27311992)
6. Mannucci, P. M., Ruggeri, Z. M., Pareti, F. I., and Capitanio, A. (1977) 1-Deamino-8-D-arginine vasopressin. A new pharmacological approach to the management of hemophilia and von Willebrand diseases. Lancet 8017, 869-872 (Pubitemid 8079684)
7. Rickles, F. R., Hoyer, L. W., Rick, M. E., and Ahr, D. J. (1976) The effects of epinephrine infusion in patients with von Willebrand disease. J. Clin. Invest. 57, 1618-1625
8. Romani de Wit, T., Rondaij, M. G., Hordijk, P. L., Voorberg, J., and van Mourik, J. A. (2003) Real time imaging of the dynamics and secretory behavior of Weibel-Palade bodies. Arterioscler. Thromb. Vasc. Biol. 23, 755-761 (Pubitemid 36566163)
9. Rondaij, M. G., Bierings, R., Kragt, A., Gijzen, K. A., Sellink, E., van Mourik, J. A., Fernandez-Borja, M., and Voorberg, J. (2006) Dynein-dynactin complex mediates protein kinase A-dependent clustering of Weibel-Palade Bodies in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 26, 49-55 (Pubitemid 43732227)
10. de Leeuw, H. P., Wijers-Koster, P. M., van Mourik, J. A., and Voorberg, J. (1999) Small GTP-binding protein RalA associates with Weibel-Palade bodies in endothelial cells. Thromb. Haemost. 82, 1177-1181 (Pubitemid 29419739)
11. Rondaij, M. G., Bierings, R., van Agtmaal, E. L., Gijzen, K. A., Sellink, E., Kragt, A., Ferguson, S. S., Mertens, K., Hannah, M. J., van Mourik, J. A., Fernandez-Borja, M., and Voorberg, J. (2008) Guanine exchange factor RalGDS mediates exocytosis of Weibel-Palade bodies from endothelial cells. Blood 112, 56-63
12. Rondaij, M. G., Sellink, E., Gijzen, K. A., ten Klooster, J. P., Hordijk, P. L., van Mourik, J. A., and Voorberg, J. (2004) Small GTP-binding protein Ral is involved in cAMP-mediated release of von Willebrand factor from endothelial cells. Arterioscler. Thromb. Vasc. Biol. 24, 1315-1320 (Pubitemid 38880027)
13. Moskalenko, S., Tong, C., Rosse, C., Mirey, G., Formstecher, E., Daviet, L., Camonis, J., and White, M. A. (2003) Ral GTPases regulate exocyst assembly through dual subunit interactions. J. Biol. Chem. 278, 51743-51748 (Pubitemid 38020420)
14. Sugihara, K., Asano, S., Tanaka, K., Iwamatsu, A., Okawa, K., and Ohta, Y. (2002) The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat. Cell Biol. 4, 73-78 (Pubitemid 34071983)
15. Vitale, N., Mawet, J., Camonis, J., Regazzi, R., Bader, M. F., and Chasserot-Golaz, S. (2005) The small GTPase RalA controls exocytosis of large dense core secretory granules by interacting with ARF6-dependent phospholipase D1. J. Biol. Chem. 280, 29921-29928 (Pubitemid 41177070)
16. Disse, J., Vitale, N., Bader, M. F., and Gerke, V. (2009) Phospholipase D1 is specifically required for regulated secretion of von Willebrand factor from endothelial cells. Blood 113, 973-980
17. Branham, M. T., Mayorga, L. S., and Tomes, C. N. (2006) Calcium-induced acrosomal exocytosis requires cAMP acting through a protein kinase A-independent, Epac-mediated pathway. J. Biol. Chem. 281, 8656-8666 (Pubitemid 43847970)
18. 2+ release and exocytosis in pancreatic beta-cells. J. Biol. Chem. 278, 8279-8285
19. Vliem, M. J., Ponsioen, B., Schwede, F., Pannekoek, W. J., Riedl, J., Kooistra, M. R., Jalink, K., Genieser, H. G., Bos, J. L., and Rehmann, H. (2008) 8-pCPT-2′-O-Me-cAMP-AM. An improved Epac-selective cAMP analog. ChemBioChem. 9, 2052-2054
20. Poppe, H., Rybalkin, S. D., Rehmann, H., Hinds, T. R., Tang, X. B., Christensen, A. E., Schwede, F., Genieser, H. G., Bos, J. L., Doskeland, S. O., Beavo, J. A., and Butt, E. (2008) Cyclic nucleotide analogs as probes of signaling pathways. Nat. Methods 5, 277-278 (Pubitemid 351455143)
21. Stel, H. V., Sakariassen, K. S., Scholte, B. J., Veerman, E. C., van der Kwast, T. H., de Groot, P. G., Sixma, J. J., and van Mourik, J. A. (1984) Characterization of 25 monoclonal antibodies to factor VIII-von Willebrand factor. Relationship between ristocetin-induced platelet aggregation and platelet adherence to subendothelium. Blood 63, 1408-1415 (Pubitemid 14120388)
22. Price, L. S., Hajdo-Milasinovic, A., Zhao, J., Zwartkruis, F. J., Collard, J. G., and Bos, J. L. (2004) Rap1 regulates E-cadherin-mediated cell-cell adhesion. J. Biol. Chem. 279, 35127-35132 (Pubitemid 39100508)
23. Borchiellini, A., Fijnvandraat, K., ten Cate, J. W., Pajkrt, D., van Deventer, S. J., Pasterkamp, G., Meijer-Huizinga, F., Zwart-Huinink, L., Voorberg, J., and van Mourik, J. A. (1996) Quantitative analysis of von Willebrand factor propeptide release in vivo. Effect of experimental endotoxemia and administration of 1-deamino-8-D-arginine vasopressin in humans. Blood 88, 2951-2958 (Pubitemid 26357375)
24. Kootstra, N. A., Munk, C., Tonnu, N., Landau, N. R., and Verma, I. M. (2003) Abrogation of post-entry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc. Natl. Acad. Sci. U.S.A. 100, 1298-1303 (Pubitemid 36183996)
25. Dull, T., Zufferey, R., Kelly, M., Mandel, R. J., Nguyen, M., Trono, D., and Naldini, L. (1998) A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72, 8463-8471 (Pubitemid 28471781)
26. 2+-mediated activation of Rap1 in human platelets. EMBO J. 16, 252-259
27. Cullere, X., Shaw, S. K., Andersson, L., Hirahashi, J., Luscinskas, F. W., and Mayadas, T. N. (2005) Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GTPase. Blood 105, 1950-1955 (Pubitemid 40731777)
28. Kooistra, M. R., Corada, M., Dejana, E., and Bos, J. L. (2005) Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett. 579, 4966-4972 (Pubitemid 41242837)
29. Sehrawat, S., Cullere, X., Patel, S., Italiano, J., Jr., and Mayadas, T. N. (2008) Role of Epac1, an exchange factor for Rap GTPases, in endothelial microtubule dynamics and barrier function. Mol. Biol. Cell 19, 1261-1270 (Pubitemid 351481837)
30. Chen, A., Dong, L., Leffler, N. R., Asch, A. S., Witte, O. N., and Yang, L. V. (2011) Activation of GPR4 by acidosis increases endothelial cell adhesion through the cAMP/Epac pathway. PLoS ONE 6, e27586
31. Chepurny, O. G., Leech, C. A., Kelley, G. G., Dzhura, I., Dzhura, E., Li, X., Rindler, M. J., Schwede, F., Genieser, H. G., and Holz, G. G. (2009) Enhanced Rap1 activation and insulin secretagogue properties of an acetoxymethyl ester of an Epac-selective cyclic AMP analog in rat INS-1 cells. Studies with 8-pCPT-2′-O-Me-cAMP-AM. J. Biol. Chem. 284, 10728-10736
32. Øynebråten, I., Barois, N., Hagelsteen, K., Johansen, F. E., Bakke, O., and Haraldsen, G. (2005) Characterization of a novel chemokine-containing storage granule in endothelial cells. Evidence for preferential exocytosis mediated by protein kinase A and diacylglycerol. J. Immunol. 175, 5358-5369 (Pubitemid 41456422)
33. Crittenden, J. R., Bergmeier, W., Zhang, Y., Piffath, C. L., Liang, Y., Wagner, D. D., Housman, D. E., and Graybiel, A. M. (2004) CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat. Med. 10, 982-986 (Pubitemid 39273740)
34. de Leeuw, H. P., Fernandez-Borja, M., Reits, E. A., Romani de Wit, T., Wijers-Koster, P. M., Hordijk, P. L., Neefjes, J., van Mourik, J. A., and Voorberg, J. (2001) Small GTP-binding protein Ral modulates regulated exocytosis of von Willebrand factor by endothelial cells. Arterioscler. Thromb. Vasc. Biol. 21, 899-904 (Pubitemid 34168643)
35. 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 (Pubitemid 40039806)
36. Rubinfeld, B., Munemitsu, S., Clark, R., Conroy, L., Watt, K., Crosier, W. J., McCormick, F., and Polakis, P. (1991) Molecular cloning of a GTPase-activating protein specific for the Krev-1 protein p21rap1. Cell 65, 1033-1042 (Pubitemid 121001691)
37. 3-mediated cell adhesion in human megakaryocytes. J. Biol. Chem. 278, 22412-22417
38. López De Jesús, M., Stope, M. B., Oude Weernink, P. A., Mahlke, Y., Börgermann, C., Ananaba, V. N., Rimmbach, C., Rosskopf, D., Michel, M. C., Jakobs, K. H., and Schmidt, M. (2006) Cyclic AMP-dependent and Epac-mediated activation of R-Ras by G protein-coupled receptors leads to phospholipase D stimulation. J. Biol. Chem. 281, 21837-21847 (Pubitemid 44181887)
39. Dao, K. K., Teigen, K., Kopperud, R., Hodneland, E., Schwede, F., Christensen, A. E., Martinez, A., and Døskeland, S. O. (2006) Epac1 and cAMP-dependent protein kinase holoenzyme have similar cAMP affinity, but their cAMP domains have distinct structural features and cyclic nucleotide recognition. J. Biol. Chem. 281, 21500-21511 (Pubitemid 44121127)
40. Dodge-Kafka, K. L., Soughayer, J., Pare, G. C., Carlisle Michel, J. J., Langeberg, L. K., Kapiloff, M. S., and Scott, J. D. (2005) The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature 437, 574-578 (Pubitemid 41613557)
41. McConnachie, G., Langeberg, L. K., and Scott, J. D. (2006) AKAP signaling complexes. Getting to the heart of the matter. Trends Mol. Med. 12, 317-323 (Pubitemid 44110003)
42. Sehrawat, S., Ernandez, T., Cullere, X., Takahashi, M., Ono, Y., Komarova, Y., and Mayadas, T. N. (2011) AKAP9 regulation of microtubule dynamics promotes Epac1-induced endothelial barrier properties. Blood 117, 708-718
43. Nightingale, T. D., Pattni, K., Hume, A. N., Seabra, M. C., and Cutler, D. F. (2009) Rab27a and MyRIP regulate the amount and multimeric state of VWF released from endothelial cells. Blood 113, 5010-5018
44. Rojo Pulido, I., Nightingale, T. D., Darchen, F., Seabra, M. C., Cutler, D. F., and Gerke, V. (2011) Myosin Va acts in concert with Rab27a and MyRIP to regulate acute von Willebrand factor release from endothelial cells. Traffic 12, 1371-1382
45. Goehring, A. S., Pedroja, B. S., Hinke, S. A., Langeberg, L. K., and Scott, J. D. (2007) MyRIP anchors protein kinase A to the exocyst complex. J. Biol. Chem. 282, 33155-33167 (Pubitemid 350159327)
46. D'Silva, N. J., Jacobson, K. L., Ott, S. M., and Watson, E. L. (1998) β-Adrenergic-induced cytosolic redistribution of Rap1 in rat parotid acini: role in secretion. Am. J. Physiol. 274, C1667-C1673 (Pubitemid 28304205)
47. Kooistra, M. R., Dubé, N., and Bos, J. L. (2007) Rap1. A key regulator in cell-cell junction formation. J. Cell Sci. 120, 17-22 (Pubitemid 46206645)
48. Arthur, W. T., Quilliam, L. A., and Cooper, J. A. (2004) Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. J. Cell Biol. 167, 111-122 (Pubitemid 39363419)
49. Maillet, M., Robert, S. J., Cacquevel, M., Gastineau, M., Vivien, D., Bertoglio, J., Zugaza, J. L., Fischmeister, R., and Lezoualc'h, F. (2003) Crosstalk between Rap1 and Rac regulates secretion of sAPPα. Nat. Cell Biol. 5, 633-639 (Pubitemid 36818085)
50. Zaldua, N., Gastineau, M., Hoshino, M., Lezoualc'h, F., and Zugaza, J. L. (2007) Epac signaling pathway involves STEF, a guanine nucleotide exchange factor for Rac, to regulate APP processing. FEBS Lett. 581, 5814-5818 (Pubitemid 350245494)
51. Yang, S. X., Yan, J., Deshpande, S. S., Irani, K., and Lowenstein, C. J. (2004) Rac1 regulates the release of Weibel-Palade bodies in human aortic endothelial cells. Chin. Med. J. 117, 1143-1150 (Pubitemid 39199917)