Modulation of Annexin II by Homocysteine: Implications for Atherothrombosis

Hajjar KA . The molecular basis of fibrinolysis. In: Nathan DG , Orkin SH , eds. Hematology of infancy and childhood. Philadelphia: WB Saunders Co, 1998:1557–73.

Carmeliet P , Schoonjans L , Kieckens L , Physiological consequences of loss of plasminogen activator gene function in mice. Nature 1994;368:419–24.

Dewerchin M , Van Nuffelen A , Wallays G , Generation and characterization of urokinase receptor-deficient mice. J Clin Invest 1996;97:870–8.

Juhan-Vague I , Alessi MC . PAI-1, obesity, insulin resistance, and risk of cardiovascular events. Thromb Haemost 1997;78:656–60.

Fay WP , Shapiro AD , Shih JL , Schleef RR , Ginsburg D. Complete deficiency of plasminogen activator inhibitor type 1 due to a frame-shift mutation. N Engl J Med 1992;327:1729–33.

Erickson LA , Fici GJ , Lund JE , Boyle TP , Polites HG , Marotti KR . Development of venous occlusions in transgenic mice for the plasminogen activator inhibitor-1 gene. Nature 1990;346:74–6.

Carmeliet P , Kieckens L , Schoonjans L , Plasminogen activator inhibitor-1 gene-deficient mice: I. Generation by homologous recombination and characterization. J Clin Invest 1993;92:2746–55.

Carmeliet P , Stassen JM , Schoonjans L , Plasminogen activator inhibitor-1 gene-deficient mice: II. Effects on hemostasis, thrombosis, and thrombolysis. J Clin Invest 1993;92:2756–60.

Aoki N , Moroi M , Sakata Y , Yoshida N , Matsuda M. Abnormal plasminogen: a hereditary molecular abnormality found in a patient with recurrent thrombosis. J Clin Invest 1978;61:1186–95.

Ichinose A , Espling ES , Takamatsu J , Two types of abnormal genes for plasminogen in families with a predisposition for thrombosis. Proc Natl Acad Sci USA 1991;88:115–9.

Bugge TH , Flick MJ , Daugherty CC , Degen JL . Plasminogen deficiency causes severe thrombosis but is compatible with development and reproduction. Genes Develop 1995;9:794–807.

Ploplis VA , Carmeliet P , Vazirzadeh S , Effects of disruption of the plasminogen gene on thrombosis, growth, and health in mice. Circulation 1995;92:2585–93.

Lijnen HR , Carmeliet P , Bouche A , Restoration of thrombolytic potential in plasminogen-deficient mice by bolus administration of plasminogen. Blood 1996;88:870–6.

Ploplis VA , French EL , Carmeliet P , Collen D , Plow EF . Plasminogen deficiency differentially affects recruitment of inflammatory cell populations in mice. Blood 1998;91:2005–9.

Carmeliet P , Moons L , Ploplis V , Plow EF , Collen D. Impaired arterial neointima formation in mice with disruption of the plasminogen gene. J Clin Invest 1997;99:200–8.

Xiao Q , Danton MJS , Witte DP , Plasminogen deficiency accelerates vessel wall disease in mice predisposed to atherosclerosis. Proc Natl Acad Sci USA 1997;94:10335–40.

Romer J , Bugge TH , Pyke C , Impaired wound healing in mice with a disrupted plasminogen gene. Nature Med 1996;2:287–92.

Bugge TH , Kombrinck KW , Flick MJ , Daugherty CC , Danton MJS , Degen JL . Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell 1996;87:709–19.

Coleman JL , Gebbia JA , Piesman J , Degen JL , Bugge TH , Benach JL . Plasminogen is required for efficient dissemination of B burfdorferi in ticks and for enhancement of spirochetemia in mice. Cell 1997;89:1111–9.

Chen ZL , Strickland S. Neuronal cell death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 1997;91:917–25.

Hajjar KA . Cellular receptors in the regulation of plasmin generation. Thromb Haemost 1995;74:294–301.

Burtin P , Chavanel G , Andre J. The plasmin system in human colonic tumours: an immunofluorescent study. Int J Cancer 1985;35:307–14.

Clavel C , Chavanel G , Birembaut P. Detection of the plasmin system in human mammary pathology using immunofluorescence. Cancer Res 1986;46:5743–7.

Burtin P , Chavanel G , Andre-Bougaran J , Gentile A. The plasmin system in human adenocarcinomas and their metastases. A comparative immunofluorescence study. Int J Cancer 1987;39:170–8.

Hajjar KA , Harpel PC , Jaffe EA , Nachman RL . Binding of plasminogen to cultured human endothelial cells. J Biol Chem 1986;261:11656–62.

Schafer A , Rodriguez R , Loscalzo J , Gimbrone MA . Inhibition of vascular endothelial cell prostacyclin synthesis by plasmin. Blood 1989;74:1015–20.

Holvoet P , Lijnen HR , Collen D. A monoclonal antibody specific for lys-plasminogen. J Biol Chem 1985;260:12106–11.

Hajjar KA , Nachman RL . Endothelial cell-mediated conversion of glu-plasminogen to lys-plasminogen: further evidence for assembly of the fibrinolytic system on the endothelial cell surface. J Clin Invest 1988:82:1769–78.

Beebe DB . Binding of tissue plasminogen activator to human umbilical vein endothelial cells. Thromb Res 1987;46:241–54.

Hajjar KA , Hamel NM , Harpel PC , Nachman RL . Binding of tissue plasminogen activator to cultured human endothelial cells. J Clin Invest 1987;80:1712–9.

Barnathan ES , Kuo A , Van der Keyl H , McCrae KR , Larsen GR , Cines DB . Tissue-type plasminogen activator binding to human endothelial cells: evidence for two distinct binding sites. J Biol Chem 1988;263:7792–9.

Sanzo MA , Howard SC , Wittwer AJ , Cochrane HM . Binding of tissue plasminogen activator to human aortic endothelial cells. Biochem J 1990;269:475–82.

Reilly TM , Whitfield MD , Taylor DS , Timmermans PB . Binding of tissue plasminogen activator to human aortic endothelial cells. Thromb Haemost 1989;61:454–8.

Beebe DB , Miles LA , Plow EF . A linear amino acid sequence involved in the interaction of t-PA with its endothelial cell receptor. Blood 1989;74:2034–7.

Hajjar KA , Hamel NM . Identification and characterization of human endothelial cell membrane binding sites for tissue plasminogen activator and urokinase. J Biol Chem 1990;265:2908–16.

Hajjar KA . The endothelial cell tissue plasminogen activator receptor: specific interaction with plasminogen. J Biol Chem 1991;266:21962–70.

Hajjar KA , Jacovina AT , Chacko J. An endothelial cell receptor for plasminogen and tissue plasminogen activator: I. Identity with annexin II. J Biol Chem 1994;269:21191–7.

Tressler RJ , Updyke TV , Yeatman TJ , Nicolson GL . Extracellular annexin is associated with divalent cation-dependent tumor cell adhesion of metastatic RAW 117 large-cell lymphoma cells. J Cell Biochem 1993;53:265–76.

Yeatman TJ , Updyke TV , Kaetzel MA , Dedman JR , Nicolson GL . Expression of annexins on the surfaces of nonmetastatic human and rodent tumor cells. Clin Exp Metastasis 1993;11:37–44.

Tressler RJ , Nicolson GL . Butanol-extractable and detergent-solubilized cell surface components from murine large cell lymphoma cells associated with adhesion to organ microvessel endothelial cells. J Cell Biochem 1992;48:162–71.

Menell JS , Cesarman GM , McLaughlin MA , Lev EA , Hajjar KA . Annexin II: potential role in the coagulocytic leukemia. J Investig Med 1995;43:376A.

Falcone DJ , Borth W , Matthew J , Guevara C , Hajjar KA . Annexin II, is a plasminogen recptor on THP-1 macrophages [abstract]. FASEB J 1995;9:2388A.

Chung CY , Erickson HP . Cell surface annexin II is a high affinity receptor for the alternatively spliced segment of tenascin-C. J Cell Biol 1994;126:539–48.

Wright JF , Kurosky A , Wasi S. An endothelial cell-surface form of annexin II binds human cytomegalovirus. Biochem Biophys Res Commun 1994;198:983–9.

Kassam G , Choi KS , Ghuman J , The role of annexin II tetramer in the activation of plasminogen. J Biol Chem 1998;273:4790–9.

Siever DA , Erickson HP . Extracellular annexin II. Int J Biochem Cell Biol 1997;29:1219–23.

Cesarman GM , Guevara CA , Hajjar KA . An endothelial cell receptor for plasminogen/tissue plasminogen activator: II. Annexin II-mediated enhancement of t-PA-dependent plasminogen activation. J Biol Chem 1994;269:21198–203.

Hajjar KA , Guevara CA , Lev E , Dowling K , Chacko J. Interaction of the fibrinolytic receptor, annexin II, with the endothelial cell surface: essential role of endonexin repeat 2. J Biol Chem 1996;271:21652–59.

Hajjar KA , Mauri L , Jacovina AT , Tissue plasminogen activator binding to the annexin II tail domain: direct modulation by homocysteine. J Biol Chem 1998;273:9987–93.

Scanu AM , Fless GM . Lipoprotein(a) heterogeneity and biologic relevance. J Clin Invest 1990;85:1709–15.

Utermann G. The mysteries of lipoprotein(a). Science 1989;246:904–10.

Loscalzo J. Lipoprotein(a), a unique risk factor for atherothrombotic disease. Arteriosclerosis 1990;10:672–9.

Hajjar KA , Nachman RL . The role of lipoprotein(a) in atherogenesis and thrombosis. Ann Rev Med 1996;47:423–42.

Bauer PI , Machovich R , Buki KG , Csonka E , Koch SA , Horvath I. Interaction of plasmin with endothelial cells. Biochem J 1984;218:119–24.

McLean JW , Tomlinson JE , Kuang WJ , cDNA sequence of human apolipoprotein(a) is homologous to plasminogen. Nature 1987;330:132–7.

Weitkamp LR , Guttormsen SA , Schultz JS . Linkage between the loci for the Lp(a) lipoprotein (Lp) and plasminogen (PLG). Hum Genet 1988;79:80–2.

Hajjar KA , Gavish D , Breslow J , Nachman RL . Lipoprotein(a) modulation of endothelial cell surface fibrinolysis and its potential role in atherosclerosis. Nature 1989;339:303–5.

Miles LA , Fless GM , Levin EG , Scanu AM , Plow EF . A potential basis for the thrombotic risks associated with lipoprotein(a). Nature 1989;339:301–3.

Gonzales-Gronow M , Edelberg JM , Pizzo SV . Further characterization of the cellular plasminogen binding site: evidence that plasminogen 2 and lipoprotein a compete for the same site. Biochemistry 1989;28:2374–7.

Grainger DJ , Kemp PR , Liu AC , Lawn RM , Metcalfe JC . Activation of transforming growth factor-beta is inhibited in transgenic apolipoprotein(a) mice. Nature 1994;370:460–2.

Palabrica TM , Liu AC , Aronovitz MJ , Furie B , Lawn RM , Furie BC . Antifibrinolytic activity of apolipoprotein(a) in vivo: human apolipoprotein(a) transgenic mice are resistant to tissue plasminogen activator-mediated thrombolysis. Nature Med 1995;1:256–9.

Lawn RM , Wade DP , Hammer RE , Chiesa G , Verstuyft JG , Rubin EM . Atherogenesis in transgenic mice expressing human apolipoprotein(a). Nature 1992;360:670–2.

Boonmark NW , Lou XJ , Schwartz K , Zhang JL , Rubin EM , Lawn RM . Modification of apolipoprotein(a) lysine binding site reduces atherosclerosis in transgenic mice. J Clin Invest 1997;100:558–64.

Mudd H , Levy HL , Skovby F. Disorders of transsulfuration. In: Scriver CR , Beaudet AL , Sly WS , Valle D , eds. The metabolic and molecular basis of inherited disease. New York: McGraw-Hill Inc, 1995:1279–327.

Mudd H , Skovby F , Levy HL , The natural history of homocystinuria due to cystathionine b-synthase deficiency. Am J Hum Gen 1985;37:1–31.

Kraus JP . Molecular basis of phenotype expression in homocystinuria. J Inherit Metab Dis 1994;17:383–90.

Frosst P , Blom HJ , Milos R , A candidate genetic risk factor for vascular disease: a common mutation in methylenetetrahydrofolate reductase. Nat Genet 1995;10:111–3.

Boushey CJ , Beresford SAA , Omenn GS , Motulsky AG . A quantitative assessment of plasma homocysteine as a risk factor for vascular disease. JAMA 1995;274:1049–57.

Refsum H , Ueland PM , Nygard O , Vollset SE . Homocysteine and cardiovascular disease. Ann Rev Med 1998;49:31–62.

Graham IM , Daly LE , Refsum HM , Plasma homocysteine as a risk factor for vascular disease: the European Concerted Action Project. JAMA 1997;277:1775–81.

Nygard O , Nordrehaug JE , Refsum H , Ueland PM , Farstad M , Vollset SE . Plasma homocysteine levels and mortality in patients with coronary artery disease. N Engl J Med 1997;337:230–6.

Selhub J , Jacques PF , Bostom AG , Association between plasma homocysteine concentrations and extracranial carotid-artery stenosis. N Engl J Med 1995;332:286–91.

Wang J , Dudman NPB , Wilcken DE . Effects of homocysteine and related compounds on prostacyclin production by cultured vascular endothelial cells. Thromb Haemost 1993;6:1047–52.

Rodgers GM , Kane WH . Activation of endogenous factor V by a homocysteine-induced vascular endothelial cell activator. J Clin Invest 1986;77:1909–16.

Rodgers GM , Conn MT . Homocysteine, an atherogenic stimulus, reduces protein C activation by arterial and venous endothelial cells. Blood 1990;75:895–901.

Lentz SR , Sadler JE . Inhibition of thrombomodulin surface expression and protein C activation by the thrombogenic agent homocysteine. J Clin Invest 1991;88:1906–14.

Hayashi T , Honda G , Suzuki K. An atherogenic stimulus homocysteine inhibits cofactor activity of thrombomodulin and enhances thrombomodulin expression in human umbilical vein endothelial cells. Blood 1992;79:2930–6.

Stamler JS , Osborne JA , Jaraki O , Adverse vascular effects of homocysteine are modulated by endothelium-derived relaxing factor and related oxides of nitrogen. J Clin Invest 1993;91:308–18.

Fryer RH , Wilson BD , Gubler DB , Fitzgerald LA , Rodgers GM . Homocysteine, a risk factor for premature vascular disease and thrombosis, induces tissue factor activity in endothelial cells. Arterioscler Thromb 1993;13:1327–33.

Nishinaga M , Ozawa T , Shimada K. Homocysteine, a thrombogenic agent, suppresses anticoagulant heparan sulfate expression in cultured porcine aortic endothelial cells. J Clin Invest 1993;92:1381–6.

Wang H , Yoshizumi M , Lai K , Inhibition of growth and p21ras methylation in vascular endothelial cells by homocysteine but not cysteine. J Biol Chem 1997;272:25380–5.

Lentz SR , Sobey CG , Piegers DJ , Vascular dysfunction in monkeys with diet-induced hyperhomocyst(e)inemia. J Clin Invest 1996;98:24–9.

Browning KS , Humphreys J , Hobbs W , Smith GB , Ravel JM . Determination of the amounts of the protein synthesis initiation and elongation factors in wheat germ. J Biol Chem 1990;265:17967–73.

Chacko G , Ling Q , Hajjar KA . Induction of acute translational response genes by homocysteine: elongation factors EF-1 alpha; beta, and delta. J Biol Chem. 1998;273:19840–6.

Tsai JC , Perrella MA , Yoshizumi M , Promotion of vascular smooth muscle cell growth by homocysteine: a link to atherosclerosis. Proc Natl Acad Sci USA 1994;91:6369–73.

Tsai JC , Wang H , Perrella MA , Induction of cyclin A gene expression by homocysteine in vascular smooth muscle cells. J Clin Invest 1996;97:146–53.

Hajjar KA . Homocysteine-induced modulation of tissue plasminogen activator to its endothelial cell membrane receptor. J Clin Invest 1993;91:2873–9.