Cooperation between β-and α-cytoplasmic actins in the mechanical regulation of endothelial microparticle formation

FASEB Journal

Volumn 27, Issue 2, 2013, Pages 672-683

  Latham, Sharissa L ^a   Chaponnier, Christine ^b   Dugina, Vera ^b   Couraud, Pierre Olivier ^c,d,e   Grau, Georges E R ^a   Combes, Valery ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c INSERM   (France)

^d CNRS   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Cytoskeleton; Neuroinflammation; Vesiculation

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ACTIN; BETA ACTIN; CYTOPLASM PROTEIN; CYTOSKELETON PROTEIN; F ACTIN; GAMMA ACTIN; TALIN; UNCLASSIFIED DRUG; VINCULIN; AMIDE; CALCIMYCIN; ENZYME INHIBITOR; GAMMA INTERFERON; LIPOPOLYSACCHARIDE; PEPTIDE FRAGMENT; PYRIDINE DERIVATIVE; RHO KINASE; THROMBIN RECEPTOR PEPTIDE (42 47); THROMBIN RECEPTOR PEPTIDE (42-47); TUMOR NECROSIS FACTOR ALPHA;

ACTIN FILAMENT; ARTICLE; CELL STIMULATION; CELLULAR DISTRIBUTION; CYTOSKELETON; ENDOTHELIAL MICROPARTICLE; ENDOTHELIUM CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SCANNING ELECTRON MICROSCOPY; STRESS FIBER; WESTERN BLOTTING; BIOLOGICAL MODEL; BIOMECHANICS; CELL LINE; DRUG ANTAGONISM; DRUG EFFECT; KINETICS; MEMBRANE MICROPARTICLE; PHYSIOLOGY; ULTRASTRUCTURE;

ACTINS; AMIDES; BIOMECHANICS; CALCIMYCIN; CELL LINE; CELL-DERIVED MICROPARTICLES; CYTOSKELETON; ENDOTHELIAL CELLS; ENZYME INHIBITORS; HUMANS; INTERFERON-GAMMA; KINETICS; LIPOPOLYSACCHARIDES; MICROSCOPY, ELECTRON, SCANNING; MODELS, BIOLOGICAL; PEPTIDE FRAGMENTS; PYRIDINES; RHO-ASSOCIATED KINASES; TUMOR NECROSIS FACTOR-ALPHA;

MLCS; MLOWN;

EID: 84873449897     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-216531     Document Type: Article

References (38)

1. Piccin, A., Murphy, W. G., and Smith, O. P. (2007) Circulating microparticles: pathophysiology and clinical implications. Blood Rev. 21, 157-171
2. Coltel, N., Combes, V., Wassmer, S. C., Chimini, G., and Grau, G. E. (2006) Cell vesiculation and immunopathology: implications in cerebral malaria. Microbes Infect. 8, 2305-2316
3. Combes, V., El-Assaad, F., Faille, D., Jambou, R., Hunt, N. H., and Grau, G. E. R. (2010) Microvesiculation and cell interactions at the brain-endothelial interface in cerebral malaria pathogenesis. Prog. Neurobiol. 91, 140-151
4. Leroyer, A. S., Tedgui, A., and Boulanger, C. M. (2008) Role of microparticles in atherothrombosis. J. Intern. Med. 263, 528-537
5. VanWijk, M. J., VanBavel, E., Sturk, A., and Nieuwland, R. (2003) Microparticles in cardiovascular diseases. Cardiovasc. Res. 59, 277-287
6. Combes, V., Simon, A. C., Grau, G. E., Arnoux, D., Camoin, L., Sabatier, F., Mutin, M., Sanmarco, M., Sampol, J., and Dignat-George, F. (1999) In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J. Clin. Invest. 104, 93-102
7. Mallat, Z., Benamer, H., Hugel, B., Benessiano, J., Steg, P. G., Freyssinet, J. M., and Tedgui, A. (2000) Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 101, 841-843
8. Minagar, A., Jy, W., Jimenez, J. J., Sheremata, W. A., Mauro, L. M., Mao, W. W., Horstman, L. L., and Ahn, Y. S. (2001) Elevated plasma endothelial microparticles in multiple sclerosis. Neurology 56, 1319-1324
9. Combes, V., Taylor, T. E., Juhan-Vague, I., Mege, J. L., Mwenechanya, J., Tembo, M., Grau, G. E., and Molyneux, M. E. (2004) Circulating endothelial microparticles in Malawian children with severe falciparum malaria complicated with coma. JAMA 291, 2542-2544
10. Mfonkeu, J. B. P., Gouado, I., Kuate, H. F., Zambou, O., Zollo, P. H. A., Grau, G. E. R., and Combes, V. (2010) Elevated cell-specific microparticles are a biological marker for cerebral dysfunctions in human severe malaria. Plos ONE 5
11. Amabile, N., Guerin, A. P., Leroyer, A., Mallat, Z., Nguyen, C., Boddaert, J., London, G. M., Tedgui, A., and Boulanger, C. M. (2005) Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. J. Am. Soc. Nephrol. 16, 3381-3388
12. Hamilton, K. K., Hattori, R., Esmon, C. T., and Sims, P. J. (1990) Complement proteins C5B-9 induce vesiculation of the endothelial plasma-membrane and expose catalytic surface for assembly of the prothrombinase enzyme complex. J. Biol. Chem. 265, 3809-3814
13. Sapet, C., Simoncini, S., Loriod, B., Puthier, D., Sampol, J., Nguyen, C., Dignat-George, F., and Anfosso, F. (2006) Thrombin-induced endothelial microparticle generation: identification of a novel pathway involving ROCK-II activation by caspase-2. Blood 108, 1868-1876
14. Patel, K. D., Zimmerman, G. A., Prescott, S. M., and McIntyre, T. M. (1992) Novel leukocyte agonists are released by endothelial-cells exposed to peroxide. J. Biol. Chem. 267, 15168-15175
15. Fu, Y. Y., Zhou, J., Li, H. B., Cao, F. L., Su, Y. H., Fan, S. J., Li, Y. H., Wang, S. Y., Li, L. M., Gilbert, G. E., and Shi, J. L. (2010) Daunorubicin induces procoagulant activity of cultured endothelial cells through phosphatidylserine exposure and microparticles release. Thrombosis Haemostasis 104, 1235-1241
16. Zwaal, R. F. A., and Schroit, A. J. (1997) Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 89, 1121-1132
17. Dacharyprigent, J., Freyssinet, J. M., Pasquet, J. M., Carron, J. C., and Nurden, A. T. (1993) Annexin-V as a probe of aminophospholipid exposure and platelet membrane vesiculation- A flowcytometry study showing a role for free sulfhydryl-groups. Blood 81, 2554-2565
18. Pasquet, J. M., DacharyPrigent, J., and Nurden, A. T. (1996) Calcium influx is a determining factor of calpain activation and microparticle formation in platelets. Eur. J. Biochem. 239, 647-654
19. Fox, J. E. B., Austin, C. D., Reynolds, C. C., and Steffen, P. K. (1991) Evidence that agonist-induced activation of calpain causes the shedding of procoagulant-containing microvesicles from the membrane of aggregating platelets. J. Biol. Chem. 266, 13289-13295
20. Wiedmer, T., Shattil, S. J., Cunningham, M., and Sims, P. J. (1990) Role of calcium and calpain in complement-induced vesiculation of the platelet plasma-membrane and in the exposure of the platelet factor VA receptor. Biochemistry 29, 623-632
21. Miyoshi, H., Umeshita, K., Sakon, M., ImajohOhmi, S., Fujitani, K., Gotoh, M., Oiki, E., Kambayashi, J., and Monden, M. (1996) Calpain activation in plasma membrane bleb formation during tert-butyl hydroperoxide-induced rat hepatocyte injury. Gastroenterology 110, 1897-1904
22. Cunningham, C. C., Gorlin, J. B., Kwiatkowski, D. J., Hartwig, J. H., Janmey, P. A., Byers, H. R., and Stossel, T. P. (1992) Actin-binding protein requirement for cortical stability and efficient locomotion. Science 255, 325-327
23. Coleman, M. L., Sahai, E. A., Yeo, M., Bosch, M., Dewar, A., and Olson, M. F. (2001) Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3, 339-345
24. Wojciak-Stothard, B., Entwistle, A., Garg, R., and Ridley, A. J. (1998) Regulation of TNF-alpha-induced reorganization of the actin cytoskeleton and cell-cell junctions by Rho, Rac, and Cdc42 in human endothelial cells. J. Cell. Physiol. 176, 150-165
25. Essler, M., Staddon, J. M., Weber, P. C., and Aepfelbacher, M. (2000) Cyclic AMP blocks bacterial lipopolysaccharide-induced myosin light chain phosphorylation in endothelial cells through inhibition of Rho/Rho kinase signaling. J. Immunol. 164, 6543-6549
26. Cunningham, C. C. (1995) Actin polymerization and intracellular solvent flow in cell-surface blebbing. J. Cell Biol. 129, 1589-1599
27. Laster, S. M., and Mackenzie, J. M. (1996) Bleb formation and F-actin distribution during mitosis and tumor necrosis factorinduced apoptosis. Microsc. Res. Tech. 34, 272-280
28. Dugina, V., Zwaenepoel, I., Gabbiani, G., Clement, S., and Chaponnier, C. (2009) Beta-and gamma-cytoplasmic actins display distinct distribution and functional diversity. J. Cell Sci. 122, 2980-2988
29. Chaponnier, C., and Gabbiani, G. (2004) Pathological situations characterized by altered actin isoform expression. J. Pathol. 204, 386-395
30. Yano, Y., Shiba, E., Kambayashi, J., Sakon, M., Kawasaki, T., Fujitani, K., Kang, J. H., and Mori, T. (1993) The effects of calpeptin (a calpain specific inhibitor) on agonist-induced microparticle formation from the platelet plasma-membrane. Thrombosis Res. 71, 385-396
31. Cerri, C., Chimenti, D., Conti, I., Neri, T., Paggiaro, P., and Celi, A. (2006) Monocyte/macrophage-derived microparticles upregulate inflammatory mediator synthesis by human airway epithelial cells. J. Immunol. 177, 1975-1980
32. Leeuwenberg, J. F. M., Smeets, E. F., Neefjes, J. J., Shaffer, M. A., Cinek, T., Jeunhomme, T., Ahern, T. J., and Buurman, W. A. (1992) E-selectin and intercellular-adhesion molecule-1 are released by activated human endothelial-cells invitro. Immunology 77, 543-549
33. Jimenez, J. J., Jy, W., Mauro, L. M., Soderland, C., Horstman, L. L., and Ahn, Y. S. (2003) Endothelial cells release phenotypically and quantitatively distinct microparticles in activation and apoptosis. Thrombosis Res. 109, 175-180
34. Pugin, J., Schurermaly, C. C., Leturcq, D., Moriarty, A., Ulevitch, R. J., and Tobias, P. S. (1993) Lipopolysaccharide activation of human endothelial and epithelial-cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc. Natl. Acad. Sci. U. S. A. 90, 2744-2748
35. Itakura, Y., Ogura, H., Tanaka, H., Koh, T., Fujita, K., Fujimi, S., Nakamori, Y., Shimazu, T., and Sugimoto, H. (2003) Paradoxical cytoskeleton and microparticle formation changes in monocytes and polymorphonuclear leukocytes in severe systemic inflammatory response syndrome patients. J. Trauma Inj. Infect. Crit. Care 55, 1125-1132
36. Basse, F., Gaffet, P., and Bienvenue, A. (1994) Correlation between inhibition of cytoskeleton proteolysis and anti-vesiculation effect of calpeptin during A23187-induced activation of human platelets-are vesicles shed by filopod fragmentation. Biochim. Biophys. Acta 1190, 217-224
37. Sebbagh, M., Renvoize, C., Hamelin, J., Riche, N., Bertoglio, J., and Breard, J. (2001) Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat. Cell Biol. 3, 346-352
38. Bernimoulin, M., Waters, E. K., Foy, M., Steele, B. M., Sullivan, M., Falet, H., Walsh, M. T., Barteneva, N., Geng, J. G., Hartwig, J. H., Maguire, P. B., and Wagner, D. D. (2009) Differential stimulation of monocytic cells results in distinct populations of microparticles. J. Thrombosis Haemostasis 7, 1019-1028