Role of the urokinase plasminogen activator receptor in mediating impaired efferocytosis of anti-SSA/Ro-bound apoptotic cardiocytes implications in the pathogenesis of congenital heart block

Circulation Research

Volumn 107, Issue 3, 2010, Pages 374-387

  Briassouli, Paraskevi ^a   Komissarova, Elena V ^a   Clancy, Robert M ^a   Buyon, Jill P ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anti SSA Ro60; Apoptosis; Congenital heart block; UPA uPAR

Indexed keywords

CALRETICULIN; CD31 ANTIGEN; CD47 ANTIGEN; RIBONUCLEOPROTEIN; RIBONUCLEOPROTEIN ANTIBODY; RO 60 ANTIBODY; UNCLASSIFIED DRUG; UROKINASE; UROKINASE RECEPTOR; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY;

ANTIGEN BINDING; APOPTOSIS; ARTICLE; BINDING COMPETITION; COMPETITIVE INHIBITION; CONFOCAL MICROSCOPY; CONGENITAL HEART BLOCK; CONTROLLED STUDY; EFFEROCYTOSIS; ENZYME ACTIVITY; FEMALE; FETUS; FETUS HEART; FLOW CYTOMETRY; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE CONDUCTION SYSTEM; HUMAN; HUMAN CELL; HUMAN TISSUE; MACROPHAGE; MOLECULAR RECOGNITION; PATHOGENESIS; PHAGOCYTOSIS; PHAGOCYTOSIS AND RELATED PHENOMENA; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ANIMAL; CARDIOMYOPATHY; CHICKEN; DRUG ANTAGONISM; FETUS DISEASE; GENETICS; HEART BLOCK; IMMUNOLOGY; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; PREGNANCY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD31; ANTIGENS, CD47; APOPTOSIS; CALRETICULIN; CARDIOMYOPATHIES; CHICKENS; FEMALE; FETAL DISEASES; FETUS; FLOW CYTOMETRY; HEART BLOCK; HEART CONDUCTION SYSTEM; HUMANS; IMMUNOGLOBULIN G; MICE; MICROSCOPY, CONFOCAL; MYOCYTES, CARDIAC; PREGNANCY; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 77956643808     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.213629     Document Type: Article

References (57)

1. Buyon JP, Clancy RM, Friedman DM. Cardiac manifestations of neonatal lupus erythematosus: guidelines to management, integrating clues from the bench and bedside. Nat Clin Pract Rheumatol. 2009;5:139-148.
2. Casciola-Rosen LA, Anhalt G, Rosen A. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med. 1994;179:1317-1330.
3. Miranda-Carus ME, Askanase AD, Clancy RM, Di Donato F, Chou TM, Libera MR, Chan EK, Buyon JP. Anti-SSA/Ro and anti-SSB/La autoantibodies bind the surface of apoptotic fetal cardiocytes and promote secretion of TNF-alpha by macrophages. J Immunol. 2000;165:5345-5351.
4. Clancy RM, Askanase AD, Kapur RP, Chiopelas E, Azar N, Miranda-Carus ME, Buyon JP. Transdifferentiation of cardiac fibroblasts, a fetal factor in anti-SSA/Ro-SSB/La antibody-mediated congenital heart block. J Immunol. 2002;169:2156-2163.
5. Clancy RM, Neufing PJ, Zheng P, O'Mahony M, Nimmerjahn F, Gordon TP, Buyon JP. Impaired clearance of apoptotic cardiocytes is linked to anti-SSA/Ro and-SSB/La antibodies in the pathogenesis of congenital heart block. J Clin Invest. 2006;116:2413-2422.
6. Miranda ME, Tseng CE, Rashbaum W, Ochs RL, Casiano CA, Di Donato F, Chan EK, Buyon JP. Accessibility of SSA/Ro and SSB/La antigens to maternal autoantibodies in apoptotic human fetal cardiac myocytes. J Immunol. 1998;161:5061-5069.
7. Furukawa F, Itoh T, Wakita H, Yagi H, Tokura Y, Norris DA, Takigawa M. Keratinocytes from patients with lupus erythematosus show enhanced cytotoxicity to ultraviolet radiation and to antibody-mediated cytotoxicity. Clin Exp Immunol. 1999;118:164-170.
8. Brown S, Heinisch I, Ross E, Shaw K, Buckley CD, Savill J. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature. 2002;418:200-203.
9. Takeda K, Yu ZX, Nishikawa T, Tanaka M, Hosoda S, Ferrans VJ, Kasajima T. Apoptosis and DNA fragmentation in the bulbus cordis of the developing rat heart. J Mol Cell Cardiol. 1996;28:209-215.
10. Ucker DS. Death by suicide: one way to go in mammalian cellular development? New Biol. 1991;3:103-109.
11. Hale AJ, Smith CA, Sutherland LC, Stoneman VE, Longthorne VL, Culhane AC, Williams GT. Apoptosis: molecular regulation of cell death. Eur J Biochem. 1996;236:1-26.
12. Clancy RM, Kapur RP, Molad Y, Askanase AD, Buyon JP. Immunohistologic evidence supports apoptosis, IgG deposition, and novel macrophage/fibroblast crosstalk in the pathologic cascade leading to congenital heart block. Arthritis Rheum. 2004;50:173-182.
13. Blasi F, Sidenius N. Efferocytosis: another function of uPAR. Blood. 2009;114:752-753.
14. D'Mello V, Singh S, Wu Y, Birge RB. The urokinase plasminogen activator receptor promotes efferocytosis of apoptotic cells. J Biol Chem. 2009;284:17030-17038.
15. Park YJ, Liu G, Tsuruta Y, Lorne E, Abraham E. Participation of the urokinase receptor in neutrophil efferocytosis. Blood. 2009;114:860-870.
16. Mondino A, Resnati M, Blasi F. Structure and function of the urokinase receptor. Thromb Haemost. 1999;82(suppl 1):19-22.
17. D'alessio S, Blasi F. The urokinase receptor as an entertainer of signal transduction. Front Biosci. 2009;14:4575-4587.
18. Ragno P. The urokinase receptor: a ligand or a receptor? Story of a sociable molecule. Cell Mol Life Sci. 2006;63:1028-1037.
19. Blasi F, Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol. 2002;3:932-943.
20. Montuori N, Ragno P. Multiple activities of a multifaceted receptor: roles of cleaved and soluble uPAR. Front Biosci. 2009;14:2494-2503.
21. Alfano D, Franco P, Vocca I, Gambi N, Pisa V, Mancini A, Caputi M, Carriero MV, Iaccarino I, Stoppelli MP. The urokinase plasminogen activator and its receptor: role in cell growth and apoptosis. Thromb Haemost. 2005;93:205-211.
22. Mondino A, Blasi F. uPA and uPAR in fibrinolysis, immunity and pathology. Trends Immunol. 2004;25:450-455.
23. Stempien-Otero A, Plawman A, Meznarich J, Dyamenahalli T, Otsuka G, Dichek DA. Mechanisms of cardiac fibrosis induced by urokinase plasminogen activator. J Biol Chem. 2006;281:15345-15351.
24. Heymans S, Luttun A, Nuyens D, Theilmeier G, Creemers E, Moons L, Dyspersin GD, Cleutjens JPM, Shipley M, Angellilo A, Levi M, Nube O, Baker A, Keshet E, Lupu F, Herbert JM, Smits JFM, Shapiro SD, Baes M, Borgers M, Collen D, Daemen MJAP, Carmeliet P. Inhibition of plasminogen activators or matrix metalloproteinases prevents cardiac rupture but impairs therapeutic angiogenesis and causes cardiac failure. Nat Med. 1999;5:1135-1142.
25. Heymans S, Lupu F, Terclavers S, Vanwetswinkel B, Herbert JM, Baker A, Collen D, Carmeliet P, Moons L. Loss or inhibition of uPA or MMP-9 attenuates LV remodeling and dysfunction after acute pressure overload in mice. Am J Pathol. 2005;166:15-25.
26. Moriwaki H, Stempien-Otero A, Kremen M, Cozen AE, Dichek DA. Overexpression of urokinase by macrophages or deficiency of plasminogen activator inhibitor type 1 causes cardiac fibrosis in mice. Circ Res. 2004;95:637-644.
27. Cozen AE, Moriwaki H, Kremen M, DeYoung MB, Dichek HL, Slezicki KI, Young SG, Veniant M, Dichek DA. Macrophage-targeted overexpression of urokinase causes accelerated atherosclerosis, coronary artery occlusions, and premature death. Circulation. 2004;109:2129-2135.
28. Blasi F, Sidenius N. The urokinase receptor: Focused cell surface proteolysis, cell adhesion and signaling. FEBS Lett. 2010;584:1923-1930.
29. Sitrin RG, Pan PM, Harper HA, Todd RF III, Harsh DM, Blackwood RA. Clustering of urokinase receptors (uPAR; CD87) induces proinflammatory signaling in human polymorphonuclear neutrophils. J Immunol. Sep. 15. 2000;165:3341-3349.
30. Bernstein AM, Twining SS, Warejcka DJ, Tall E, Masur SK. Urokinase receptor cleavage: A crucial step in 14 fibroblast-to-myofibroblast differentiation. Mol Biol Cell. 2007;18:2716-2727.
31. Rao NK, Shi GP, Chapman HA. Urokinase receptor is a multifunctional protein: influence of receptor occupancy on macrophage gene expression. J Clin Invest. 1995;96:465-474.
32. Tseng CE, Miranda E, Di Donato F, Boutjdir M, Rashbaum W, Chan EK, Buyon JP. mRNA and protein expression of SSA/Ro and SSB/La in human fetal cardiac myocytes cultured using a novel application of the Langendorff procedure. Pediatr Res. 1999;45:260-269.
33. Grimsley C, Ravichandran KS. Cues for apoptotic cell engulfment: eat-me, don't eat-me and come-get-me signals. Trends Cell Biol. 2003;13:648-656.
34. Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM, Haslett C. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest. 1989;83:865-875.
35. Kuraishi T, Manaka J, Kono M, Ishii H, Yamamoto N, Koizumi K, Shiratsuchi A, Lee BL, Higashida H, Nakanishi Y. Identification of calreticulin as a marker for phagocytosis of apoptotic cells in Drosophila. Exp Cell Res. 2007;313:500-510.
36. Calreticulin serves as an "eat me" signal. Sci STKE. 2005;2005: tw375.
37. Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP. Role of CD47 as a marker of self on red blood cells. Science. 2000;288:2051-2054.
38. O'Mullane MJ, Baker MS. Loss of cell viability dramatically elevates cell surface plasminogen binding and activation. Exp Cell Res. 1998;242:153-164.
39. Shiratsuchi T, Ishibashi H, Shirasuna K. Inhibition of epidermal growth factor-induced invasion by dexamethasone and AP-1 decoy in human squamous cell carcinoma cell lines. J Cell Physiol. 2002;193:340-348.
40. Stahl A, Mueller BM. Binding of urokinase to its receptor promotes migration and invasion of human melanoma cells in vitro. Cancer Res. 1994;54:3066-3071.
41. Reed JH, Giannakopoulos B, Jackson MW, Krilis SA, Gordon TP. Ro 60 functions as a receptor for beta (2)-glycoprotein I on apoptotic cells. Arthritis Rheum. 2009;60:860-869.
42. Arnout J, Wittevrongel C, Vanrusselt M, Hoylaerts M, Vermylen J. Beta-2-glycoprotein I dependent lupus anticoagulants form stable bivalent antibody beta-2-glycoprotein I complexes on phospholipid surfaces. Thromb Haemost. 1998;79:79-86.
43. Dominguez M, Montes R, Paramo JA, Angles-Cano E. Bivalency of plasminogen monoclonal antibodies is required for plasminogen bridging to fibrin and enhanced plasmin formation. Biochem Biophys Acta. 2002;1598:165-176.
44. Felez J. Plasminogen binding to cell surfaces. Fibrinol Proteol. 1998;12:183-189.
45. Maxfield FR, Mayor S. Cell surface dynamics of GPI-anchored proteins. Adv Exp Med Biol. 1997;419:355-364.
46. Cunningham O, Andolfo A, Santovito ML, Iuzzolino L, Blasi F, Sidenius N. Dimerization controls the lipid raft partitioning of uPAR/CD87 and regulates its biological functions. EMBO J. 2003;22:5994-6003.
47. Mayor S, Rothberg KG, Maxfield FR. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 1994;264:1948-1951.
48. Gellert GC, Goldfarb RH, Kitson RP. Physical association of uPAR with the alphaV integrin on the surface of human NK cells. Biochem Biophys Res Commun. 2004;315:1025-1032.
49. Zhang F, Crise B, Su B, Hou Y, Rose JK, Bothwell A, Jacobson K. The lateral mobility of some membrane proteins is determined by their ectodomains. Biophys J. 1992;62:92-94.
50. Zhang F, Yang B, Odin JA, Shen Z, Lin CT, Unkeless JC, Jacobson K. Lateral mobility of Fc gamma RIIa is reduced by protein kinase C activation. FEBS Lett. 1995;376:77-80.
51. Fein M, Unkeless J, Chuang FY, Sassaroli M, da Costa R, Vaananen H, Eisinger J. Lateral mobility of lipid analogues and GPI-anchored proteins in supported bilayers determined by fluorescent bead tracking. J Membr Biol. 1993;135:83-92.
52. Park KJ, Lee SH, Kim TI, Lee HW, Lee CH, Kim EH, Jang JY, Choi KS, Kwon MH, Kim YS. A human scFv antibody against TRAIL receptor 2 induces autophagic cell death in both TRAIL-sensitive and TRAIL-resistant cancer cells. Cancer Res. 2007;67:7327-7334.
53. Gardai SJ, Bratton DL, Ogden CA, Henson PM. Recognition ligands on apoptotic cells: a perspective. J Leukoc Biol. 2006;79:896-903.
54. Bernstein AM, Greenberg RS, Taliana L, Masur SK. Urokinase anchors uPAR to the actin cytoskeleton. Invest Ophthalmol Vis Sci. 2004;45:2967-2977.
55. Lane JD, Allan VJ, Woodman PG. Active relocation of chromatin and endoplasmic reticulum into blebs in late apoptotic cells. J Cell Sci. 2005;118:4059-4071.
56. Clancy RM. When the levee doesn't break: a novel role of beta2-glycoprotein I to protect against congenital heart block. Arthritis Rheum. 2009;60:636-638.
57. Reed JH, Giannakopoulos B, Kaufman KM, Krilis SA, Gordon TP. Plasmin cleavage of beta2-glycoprotein I promotes maternal anti-Ro60 IgG opsonisation of apoptotic cells: a permissive factor in congenital heart block? Arthritis Rheum. 2009;60(10 Suppl): S254.