Endothelial Cell "Memory" of Inflammatory Stimulation: Human Venular Endothelial Cells Store Interleukin 8 in Weibel-Palade Bodies

doi:10.1084/jem.188.9.1757

This Article

	Full Text
	Full Text (PDF, 273K)
	PPT slides of all figures
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JEM
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Wolff, B.
	Articles by Rot, A.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Wolff, B.
	Articles by Rot, A.


Social Bookmarking

	What's this?

J. Exp. Med., Volume 188, Number 9, November 2, 1998 1757-1762

Endothelial Cell "Memory" of Inflammatory Stimulation: Human Venular Endothelial Cells Store Interleukin 8 in Weibel-Palade Bodies

By Barbara Wolff,^* Alan R. Burns, James Middleton,^* and Antal Rot^*

From the ^* Novartis Forschungsinstitut, A-1235 Vienna, Austria; and the Children's Nutrition Research Center, Baylor College of Medicine, Houston, Texas 77030-2600

The expression and secretion of interleukin (IL)-8, the prototype member of the C-X-C subfamily of chemokines, can be inducedby diverse inflammatory stimuli in many cells, including endothelialcells (EC). Upon de novo synthesis, IL-8 localizes intracellularlyin the Golgi apparatus, from where it is secreted. In additionto this constitutive secretory pathway, we describe a depot storageand separate regulated secretory pathway of IL-8 in EC.

The prolonged stimulation of primary human EC with inflammatory mediators resulted in the accumulation of IL-8 in Weibel-Paladebodies, where it colocalized with von Willebrand factor. IL-8was retained in these storage organelles for several days afterthe removal of the stimulus and could be released by EC secretagoguessuch as phorbol myristate acetate, the calcium ionophore A23187,and histamine. These findings suggest that storage of IL-8 inWeibel-Palade bodies may serve as the EC "memory" of a precedinginflammatory insult, which then enables the cells to secrete IL-8immediately without de novo protein synthesis.

Key words: interleukin 8; endothelial cell; inflammation; Weibel-Palade bodies; secretion

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Nightingale, T. D., Pattni, K., Hume, A. N., Seabra, M. C., Cutler, D. F. (2009). Rab27a and MyRIP regulate the amount and multimeric state of VWF released from endothelial cells. Blood 113: 5010-5018 [Abstract] [Full Text]
Kuo, M.-C., Patschan, D., Patschan, S., Cohen-Gould, L., Park, H.-C., Ni, J., Addabbo, F., Goligorsky, M. S. (2008). Ischemia-Induced Exocytosis of Weibel-Palade Bodies Mobilizes Stem Cells. J. Am. Soc. Nephrol. 19: 2321-2330 [Abstract] [Full Text]
Noubade, R., del Rio, R., McElvany, B., Zachary, J. F., Millward, J. M., Wagner, D. D., Offner, H., Blankenhorn, E. P., Teuscher, C. (2008). Von-Willebrand Factor Influences Blood Brain Barrier Permeability and Brain Inflammation in Experimental Allergic Encephalomyelitis. Am. J. Pathol. 173: 892-900 [Abstract] [Full Text]
Wagner, D. D., Frenette, P. S. (2008). The vessel wall and its interactions. Blood 111: 5271-5281 [Abstract] [Full Text]
Babich, V., Meli, A., Knipe, L., Dempster, J. E., Skehel, P., Hannah, M. J., Carter, T. (2008). Selective release of molecules from Weibel-Palade bodies during a lingering kiss. Blood 111: 5282-5290 [Abstract] [Full Text]
Metcalf, D. J., Nightingale, T. D., Zenner, H. L., Lui-Roberts, W. W., Cutler, D. F. (2008). Formation and function of Weibel-Palade bodies. J. Cell Sci. 121: 19-27 [Abstract] [Full Text]
Zhou, C., Chen, H., Lu, F., Sellak, H., Daigle, J. A., Alexeyev, M. F., Xi, Y., Ju, J., van Mourik, J. A., Wu, S. (2007). Cav3.1 ({alpha}1G) controls von Willebrand factor secretion in rat pulmonary microvascular endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 292: L833-L844 [Abstract] [Full Text]
De Meyer, S. F., Vanhoorelbeke, K., Chuah, M. K., Pareyn, I., Gillijns, V., Hebbel, R. P., Collen, D., Deckmyn, H., VandenDriessche, T. (2006). Phenotypic correction of von Willebrand disease type 3 blood-derived endothelial cells with lentiviral vectors expressing von Willebrand factor. Blood 107: 4728-4736 [Abstract] [Full Text]
Rondaij, M. G., Bierings, R., Kragt, A., van Mourik, J. A., Voorberg, J. (2006). Dynamics and Plasticity of Weibel-Palade Bodies in Endothelial Cells. Arterioscler. Thromb. Vasc. Bio. 26: 1002-1007 [Abstract] [Full Text]
Garrood, T., Lee, L., Pitzalis, C. (2006). Molecular mechanisms of cell recruitment to inflammatory sites: general and tissue-specific pathways. Rheumatology (Oxford) 45: 250-260 [Full Text]
Rondaij, M. G., Bierings, R., Kragt, A., Gijzen, K. A., Sellink, E., van Mourik, J. A., Fernandez-Borja, M., Voorberg, J. (2006). Dynein-Dynactin Complex Mediates Protein Kinase A-Dependent Clustering of Weibel-Palade Bodies in Endothelial Cells. Arterioscler. Thromb. Vasc. Bio. 26: 49-55 [Abstract] [Full Text]
Estelles, R., Milian, L., Nabah, Y. N. A., Mateo, T., Cerda-Nicolas, M., Losada, M., Ivorra, M. D., Issekutz, A. C., Cortijo, J., Morcillo, E. J., Blazquez, M. A., Sanz, M.-J. (2005). Effect of boldine, secoboldine, and boldine methine on angiotensin II-induced neurtrophil recruitment in vivo. J. Leukoc. Biol. 78: 696-704 [Abstract] [Full Text]
Matsushita, K., Morrell, C. N., Lowenstein, C. J. (2005). A Novel Class of Fusion Polypeptides Inhibits Exocytosis. Mol. Pharmacol. 67: 1137-1144 [Abstract] [Full Text]
Haberichter, S. L., Merricks, E. P., Fahs, S. A., Christopherson, P. A., Nichols, T. C., Montgomery, R. R. (2005). Re-establishment of VWF-dependent Weibel-Palade bodies in VWD endothelial cells. Blood 105: 145-152 [Abstract] [Full Text]
Matsushita, K., Yamakuchi, M., Morrell, C. N., Ozaki, M., O'Rourke, B., Irani, K., Lowenstein, C. J. (2005). Vascular endothelial growth factor regulation of Weibel-Palade-body exocytosis. Blood 105: 207-214 [Abstract] [Full Text]
Nabah, Y. N. A., Mateo, T., Estelles, R., Mata, M., Zagorski, J., Sarau, H., Cortijo, J., Morcillo, E. J., Jose, P. J., Sanz, M.-J. (2004). Angiotensin II Induces Neutrophil Accumulation In Vivo Through Generation and Release of CXC Chemokines. Circulation 110: 3581-3586 [Abstract] [Full Text]
Oynebraten, I., Bakke, O., Brandtzaeg, P., Johansen, F.-E., Haraldsen, G. (2004). Rapid chemokine secretion from endothelial cells originates from 2 distinct compartments. Blood 104: 314-320 [Abstract] [Full Text]
Bernardo, A., Ball, C., Nolasco, L., Moake, J. F., Dong, J.-f. (2004). Effects of inflammatory cytokines on the release and cleavage of the endothelial cell-derived ultralarge von Willebrand factor multimers under flow. Blood 104: 100-106 [Abstract] [Full Text]
Fiedler, U., Scharpfenecker, M., Koidl, S., Hegen, A., Grunow, V., Schmidt, J. M., Kriz, W., Thurston, G., 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 [Abstract] [Full Text]
Neely, G. G., Epelman, S., Ma, L. L., Colarusso, P., Howlett, C. J., Amankwah, E. K., McIntyre, A. C., Robbins, S. M., Mody, C. H. (2004). Monocyte Surface-Bound IL-15 Can Function as an Activating Receptor and Participate in Reverse Signaling. J. Immunol. 172: 4225-4234 [Abstract] [Full Text]
MONSINJON, T., GASQUE, P., CHAN, P., ISCHENKO, A., BRADY, J. J., FONTAINE, M. (2003). Regulation by complement C3a and C5a anaphylatoxins of cytokine production in human umbilical vein endothelial cells. FASEB J. 17: 1003-1014 [Abstract] [Full Text]
Romani de Wit, T., Rondaij, M. G., Hordijk, P. L., Voorberg, J., van Mourik, J. A. (2003). Real-Time Imaging of the Dynamics and Secretory Behavior of Weibel-Palade Bodies. Arterioscler. Thromb. Vasc. Bio. 23: 755-761 [Abstract] [Full Text]
Gao, J. F., Call, S. B., Fillmore, P. D., Watanabe, T., Meeker, N. D., Teuscher, C. (2003). Analysis of the Role of Bphs/Hrh1 in the Genetic Control of Responsiveness to Pertussis Toxin. Infect. Immun. 71: 1281-1287 [Abstract] [Full Text]
Klarenbach, S. W., Chipiuk, A., Nelson, R. C., Hollenberg, M. D., Murray, A. G. (2003). Differential Actions of PAR2 and PAR1 in Stimulating Human Endothelial Cell Exocytosis and Permeability: The Role of Rho-GTPases. Circ. Res. 92: 272-278 [Abstract] [Full Text]
Nemeth, Z. H., Deitch, E. A., Lu, Q., Szabo, C., Hasko, G. (2002). NHE blockade inhibits chemokine production and NF-kappa B activation in immunostimulated endothelial cells. Am. J. Physiol. Cell Physiol. 283: C396-C403 [Abstract] [Full Text]
Ma, R. Z., Gao, J., Meeker, N. D., Fillmore, P. D., Tung, K. S. K., Watanabe, T., Zachary, J. F., Offner, H., Blankenhorn, E. P., Teuscher, C. (2002). Identification of Bphs, an Autoimmune Disease Locus, as Histamine Receptor H1. Science 297: 620-623 [Abstract] [Full Text]
Epelman, S., Neely, G. G., Ma, L. L., Gjomarkaj, M., Pace, E., Melis, M., Woods, D. E., Mody, C. H. (2002). Distinct fates of monocytes and T cells directly activated by Pseudomonas aeruginosa exoenzyme S. J. Leukoc. Biol. 71: 458-468 [Abstract] [Full Text]
Qian, Z., Gelzer-Bell, R., Yang, S.-x., Cao, W., Ohnishi, T., Wasowska, B. A., Hruban, R. H., Rodriguez, E. R., Baldwin, W. M. III, Lowenstein, C. J. (2001). Inducible Nitric Oxide Synthase Inhibition of Weibel-Palade Body Release in Cardiac Transplant Rejection. Circulation 104: 2369-2375 [Abstract] [Full Text]
de Leeuw, H. P. J. C., Fernandez-Borja, M., Reits, E. A. J., Romani de Wit, T., Wijers-Koster, P. M., Hordijk, P. L., Neefjes, J., van Mourik, J. A., Voorberg, J. (2001). Small GTP-Binding Protein Ral Modulates Regulated Exocytosis of von Willebrand Factor by Endothelial Cells. Arterioscler. Thromb. Vasc. Bio. 21: 899-904 [Abstract] [Full Text]
Denis, C. V., André, P., Saffaripour, S., Wagner, D. D. (2001). Defect in regulated secretion of P-selectin affects leukocyte recruitment in von Willebrand factor-deficient mice. Proc. Natl. Acad. Sci. USA 10.1073/pnas.061307098v1 [Abstract] [Full Text]
Zhang, M., Zeng, C. Q.-Y., Morris, A. P., Estes, M. K. (2000). A Functional NSP4 Enterotoxin Peptide Secreted from Rotavirus-Infected Cells. J. Virol. 74: 11663-11670 [Abstract] [Full Text]
Rosenberg, J. B., Greengard, J. S., Montgomery, R. R. (2000). Genetic Induction of a Releasable Pool of Factor VIII in Human Endothelial Cells. Arterioscler. Thromb. Vasc. Bio. 20: 2689-2695 [Abstract] [Full Text]
Dewberry, R., Holden, H., Crossman, D., Francis, S. (2000). Interleukin-1 Receptor Antagonist Expression in Human Endothelial Cells and Atherosclerosis. Arterioscler. Thromb. Vasc. Bio. 20: 2394-2400 [Abstract] [Full Text]
Piqueras, L., Kubes, P., Alvarez, A., O'Connor, E., Issekutz, A. C., Esplugues, J. V., Sanz, M.-J. (2000). Angiotensin II Induces Leukocyte-Endothelial Cell Interactions In Vivo Via AT1 and AT2 Receptor-Mediated P-Selectin Upregulation. Circulation 102: 2118-2123 [Abstract] [Full Text]
Hop, C., Guilliatt, A., Daly, M., de Leeuw, H. P., Brinkman, H.-J. M., Peake, I. R., van Mourik, J. A., Pannekoek, H. (2000). Assembly of Multimeric von Willebrand Factor Directs Sorting of P-Selectin. Arterioscler. Thromb. Vasc. Bio. 20: 1763-1768 [Abstract] [Full Text]
Hippenstiel, S., Soeth, S., Kellas, B., Fuhrmann, O., Seybold, J., Krull, M., Eichel-Streiber, C. v., Goebeler, M., Ludwig, S., Suttorp, N. (2000). Rho proteins and the p38-MAPK pathway are important mediators for LPS-induced interleukin-8 expression in human endothelial cells. Blood 95: 3044-3051 [Abstract] [Full Text]
Charbonnier, A.-S., Kohrgruber, N., Kriehuber, E., Stingl, G., Rot, A., Maurer, D. (1999). Macrophage Inflammatory Protein 3{alpha} Is Involved in the Constitutive Trafficking of Epidermal Langerhans Cells. JEM 190: 1755-1768 [Abstract] [Full Text]
Sallusto, F., Lanzavecchia, A. (1999). Mobilizing Dendritic Cells for Tolerance, Priming, and Chronic Inflammation. JEM 189: 611-614 [Full Text]
Utgaard, J. O., Jahnsen, F. L., Bakka, A., Brandtzaeg, P., Haraldsen, G. (1998). Rapid Secretion of Prestored Interleukin 8 from Weibel-Palade Bodies of Microvascular Endothelial Cells. JEM 188: 1751-1756 [Abstract] [Full Text]
Denis, C. V., Andre, P., Saffaripour, S., Wagner, D. D. (2001). Defect in regulated secretion of P-selectin affects leukocyte recruitment in von Willebrand factor-deficient mice. Proc. Natl. Acad. Sci. USA 98: 4072-4077 [Abstract] [Full Text]
Mariscalco, M. M., Vergara, W., Mei, J., Smith, E. O'B., Smith, C. W. (2002). Mechanisms of decreased leukocyte localization in the developing host. Am. J. Physiol. Heart Circ. Physiol. 282: H636-H644 [Abstract] [Full Text]