Cyclosporine induces endothelial cell release of complement-activating microparticles

Journal of the American Society of Nephrology

Volumn 24, Issue 11, 2013, Pages 1849-1862

  Renner, Brandon ^a   Klawitter, Jelena ^a   Goldberg, Ryan ^a   McCullough, James W ^a   Ferreira, Viviana P ^b   Cooper, James E ^a   Christians, Uwe ^a   Thurman, Joshua M ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3; COMPLEMENT FACTOR H; CYCLOSPORIN; REGULATOR PROTEIN; TACROLIMUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; CELL DAMAGE; CELL PROLIFERATION; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; ENDOTHELIAL MICROPARTICLE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; KIDNEY GRAFT; KIDNEY INJURY; MALE; MESANGIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 84887061991     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2012111064     Document Type: Article

References (37)

1. Noris M, Remuzzi G: Hemolytic uremic syndrome. J Am Soc Nephrol 16: 1035-1050, 2005 (Pubitemid 41710314)
2. Delvaeye M, Noris M, De Vriese A, Esmon CT, Esmon N.L., Ferrell G., Del-Favero J, Plaisance S, Claes B., Lambrechts D, Zoja C, Remuzzi G., Conway EM: Thrombomodulin mutations in atypical hemolytic-uremic syndrome. N Engl J Med 361: 345-357, 2009
3. Fang CJ, Fremeaux-Bacchi V, Liszewski M.K., Pianetti G., Noris M, Goodship TH, Atkinson JP: Membrane cofactor protein mutations in atypical hemolytic uremic syndrome (aHUS), fatal Stx-HUS, C3 glomerulonephritis, and the HELLP syndrome. Blood 111: 624-632, 2008
4. Noris M, Caprioli J, Bresin E., Mossali C, Pianetti G, Gamba S., Daina E, Fenili C, Castelletti F., Sorosina A, Piras R, Donadelli R., Maranta R, van der Meer I, Conway EM, Zipfel PF, Goodship TH, Remuzzi G: Relative role of genetic complement abnormalities in sporadic and familial aHUS and their impact on clinical phenotype. Clin J Am Soc Nephrol 5: 1844-1859, 2010
5. Noris M, Remuzzi G: Atypical hemolytic-uremic syndrome. N Engl J Med 361: 1676-1687, 2009
6. Anderson HC, Mulhall D, Garimella R: Role of extracellular membrane vesicles in the pathogenesis of various diseases, including cancer, renal diseases, atherosclerosis, and arthritis. Laboratory investigation; a journal of technical methods and pathology, 90: 1549-1557, 2010.
7. Beyer C, Pisetsky DS: The role of microparticles in the pathogenesis of rheumatic diseases. Nat Rev Rheumatol 6: 21-29, 2010
8. Sims PJ, Faioni EM, Wiedmer T, Shattil SJ: Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J Biol Chem 263: 18205-18212, 1988 (Pubitemid 19005097)
9. Moskovich O, Fishelson Z: Live cell imaging of outward and inward vesiculation induced by the complement c5b-9 complex. J Biol Chem 282: 29977-29986, 2007 (Pubitemid 350035280)
10. Nauta AJ, Trouw LA, Daha M.R., Tijsma O., Nieuwland R, Schwaeble WJ, Gingras A.R., Mantovani A., Hack EC, Roos A: Direct binding of C1q to apoptotic cells and cell blebs induces complement activation. Eur J Immunol 32: 1726-1736, 2002 (Pubitemid 34679160)
11. Naesens M, Kuypers DR, Sarwal M: Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 4: 481-508, 2009
12. Thurman JM, Kraus DM, Girardi G, Hourcade D., Kang HJ, Royer PA, Mitchell LM, Giclas P.C., Salmon J., Gilkeson G, Holers VM: A novel inhibitor of the alternative complement pathway prevents antiphospholipid antibody-induced pregnancy loss in mice. Mol Immunol 42: 87-97, 2005 (Pubitemid 39360930)
13. Renner B, Coleman K, Goldberg R., Amura C, Holland-Neidermyer A, Pierce K, Orth H.N., Molina H., Ferreira VP, Cortes C, Pangburn MK, Holers V.M., Thurman JM: The complement inhibitors Crry and factor H are critical for preventing autologous complement activation on renal tubular epithelial cells. J Immunol 185: 3086-3094, 2010
14. Nauta AJ, Castellano G, Xu W., Woltman AM, Borrias MC, Daha MR, van Kooten C, Roos A: Opsonization with C1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J Immunol 173: 3044-3050, 2004 (Pubitemid 39142010)
15. Biró E, Nieuwland R, Tak PP, Pronk LM, Schaap MC, Sturk A, Hack CE: Activated complement components and complement activator molecules on the surface of cell-derived microparticles in patients with rheumatoid arthritis and healthy individuals. Ann Rheum Dis 66: 1085-1092, 2007 (Pubitemid 47122324)
16. Ståhl A.L., Sartz L, Karpman D: Complement activation on plateletleukocyte complexes and microparticles in enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome. Blood 117: 5503-5513, 2011
17. Nielsen CT, Østergaard O, Stener L, Iversen LV, Truedsson L, Gullstr B, and Jacobsen S, Heegaard NH: Increased IgG on cell-derived plasma microparticles in systemic lupus erythematosus is associated with autoantibodies and complement activation. Arthritis Rheum 64: 1227-1236, 2012
18. Kim YO, Lim SW, Li C, Kang H.J., Ahn KO, Yang HJ, Ghee JY, Kim S.H., Kim JY, Choi BS, Kim J, Yang CW: Activation of intrarenal complement system in mouse model for chronic cyclosporine nephrotoxicity. Yonsei Med J 48: 517-525, 2007 (Pubitemid 47083099)
19. Ståhl A.L., Vaziri-Sani F, Heinen S., Kristoffersson AC, Gydell KH, Raafat R, Gutierrez A., Beringer O, Zipfel PF, Karpman D: Factor H dysfunction in patients with atypical hemolytic uremic syndrome contributes to complement deposition on platelets and their activation. Blood 111: 5307-5315, 2008
20. Mackman N: On the trail of microparticles. Circ Res 104: 925-927, 2009
21. Brodsky SV, Malinowski K, Golightly M., Jesty J, Goligorsky MS: Plasminogen activator inhibitor-1 promotes formation of endothelial microparticles with procoagulant potential. Circulation 106: 2372-2378, 2002 (Pubitemid 35244740)
22. Boilard E, Nigrovic PA, Larabee K, Watts G.F., Coblyn JS, Weinblatt M.E., Massarotti EM, Remold-O'Donnell E, Farndale RW, Ware J, Lee DM: Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 327: 580-583, 2010
23. Andre F, Schartz NE, Movassagh M, Flament C., Pautier P, Morice P, Pomel C., Lhomme C, Escudier B, LeChevalier T, Tursz T., Amigorena S, Raposo G, Angevin E., Zitvogel L: Malignant effusions and immunogenic tumour-derived exosomes. Lancet 360: 295-305, 2002 (Pubitemid 34874721)
24. Bianco NR, Kim SH, Morelli A.E., Robbins PD: Modulation of the immune response using dendritic cell-derived exosomes. Methods Mol Biol 380: 443-455, 2007 (Pubitemid 350183346)
25. Boulanger CM, Amabile N, Guérin AP, Pannier B., Leroyer AS, Mallat CN, Tedgui A, London GM: In vivo shear stress determines circulating levels of endothelial microparticles in end-stage renal disease. Hypertension 49: 902-908, 2007 (Pubitemid 351664206)
26. Jourde-Chiche N., Dou L, Sabatier F., Calaf R, Cerini C, Robert S., Camoin-Jau L, Charpiot P, Argiles A, Dignat-George F, Brunet P: Levels of circulating endothelial progenitor cells are related to uremic toxins and vascular injury in hemodialysis patients. J Thromb Haemost 7: 1576-1584, 2009
27. Trappenburg MC, van Schilfgaarde M, Frerichs FC, Spronk H.M., Ten Cate H, de Fijter CW, Terpstra WE, Leyte A: Chronic renal failure is accompanied by endothelial activation and a large increase in microparticle numbers with reduced procoagulant capacity. Nephrol Dial Transplant 27: 1446-1453, 2012
28. Huang PH, Huang SS, Chen Y.H., Lin CP, Chiang KH, Chen JS, Tsai H.Y., Lin FY, Chen JW, Lin SJ: Increased circulating CD31+/annexin V+ apoptotic microparticles and decreased circulating endothelial progenitor cell levels in hypertensive patients with microalbuminuria. J Hypertens 28: 1655-1665, 2010
29. Jimenez JJ, Jy W, Mauro L.M., Horstman LL, Soderland C, Ahn YS: Endothelial microparticles released in thrombotic thrombocytopenic purpura express von Willebrand factor and markers of endothelial activation. Br J Haematol 123: 896-902, 2003 (Pubitemid 37533302)
30. Bretelle F, Sabatier F, Desprez D., Camoin L, Grunebaum L, Combes V., D'Ercole C, Dignat-George F: Circulating microparticles: A marker of procoagulant state in normal pregnancy and pregnancy complicated by preeclampsia or intrauterine growth restriction. Thromb Haemost 89: 486-492, 2003 (Pubitemid 36329239)
31. Berckmans RJ, Nieuwland R, Tak P.P., Böing AN, Romijn F.P., Kraan MC, Breedveld FC, Hack CE, Sturk A: Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII-dependent mechanism. Arthritis Rheum 46: 2857-2866, 2002 (Pubitemid 35315876)
32. Mrvar-Brecko A., Sustar V, Jansa V., Stukelj R, Jansa R, Mujagic E., Kruljc P, Iglic A, Hägerstrand H, Kralj-Iglic V: Isolated microvesicles from peripheral blood and body fluids as observed by scanning electron microscope. Blood Cells Mol Dis 44: 307-312, 2010
33. Faul C, Donnelly M, Merscher-Gomez S, Chang Y.H., Franz S., Delfgaauw J, Chang JM, Choi H.Y., Campbell KN, Kim K, Reiser J, Mundel P: The actin cytoskeleton of kidney podocytes is a direct target of the antiproteinuric effect of cyclosporine A. Nat Med 14: 931-938, 2008
34. Rother RP, Rollins SA, Mojcik C.F., Brodsky RA, Bell L: Discovery and development of the complement inhibitor eculizumab for the treatment of paroxysmal nocturnal hemoglobinuria. Nat Biotechnol 25: 1256-1264, 2007 (Pubitemid 350076509)
35. Matsumoto M, Fukuda W, Circolo A., Goellner J, Strauss-Schoenberger J, Wang X, Fujita S., Hidvegi T, Chaplin DD, Colten HR: Abrogation of the alternative complement pathway by targeted deletion of murine factor B. Proc Natl Acad Sci U S A 94: 8720-8725, 1997 (Pubitemid 27335106)
36. Renner B, Strassheim D, Amura C.R., Kulik L., Ljubanovic D, Glogowska MJ, Takahashi K, Carroll M.C., Holers VM, Thurman JM: B cell subsets contribute to renal injury and renal protection after ischemia/reperfusion. J Immunol 185: 4393-4400, 2010
37. Christians U, Jacobsen W, Serkova N., Benet LZ, Vidal C, Sewing KF, Manns M.P., Kirchner GI: Automated, fast and sensitive quantification of drugs in blood by liquid chromatography-mass spectrometry with online extraction: immunosuppressants. J Chromatogr B Biomed Sci Appl 748: 41-53, 2000