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Partial Purification and Properties of a Plasminogen Activator from Human Erythrocytes

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Partial Purification and Properties of a Plasminogen Activator from Human Erythrocytes Partial purification and properties of a plasminogen activator from human erythrocytes M. Semar, … , L. Skoza, A. J. Johnson J Clin Invest. 1969;48(10):1777-1785. https://doi.org/10.1172/JCI106144. Research Article The lysis time of euglobulin clots made with whole blood (plasma and red cells) was very much shorter than that of clots made with plasma alone, indicating a fibrinolytic component in red cells. A plasminogen activator was found in the stroma-free hemolysate, and proteolytic activity was found in the stromal fraction. The plasminogen activator, purified by using diethylaminoethyl-cellulose (DEAE-cellulose) in a batch procedure followed by column chromatography, was called erythrokinase (EK). On preliminary characterization, EK appears to activate human and bovine plasminogen in a manner similar to urokinase (UK), as determined by fibrinolytic and caseinolytic assays. The two enzymes can be separated by DEAE chromatography and acrylamide-gel electrophoresis, however, and they hydrolyze acetyl-L-lysine methyl ester and benzoyl arginine methyl ester at different rates. Find the latest version: https://jci.me/106144/pdf Partial Purification and Properties of a Plasminogen Activator from Human Erythrocytes M. SEMAR, L. SKOZA, and A. J. JOHNSON From the Department of Medicine, New York University Medical Center, and the American National Red Cross Research Laboratory, New York 10016 A B S T R A C T The lysis time of euglobulin clots made research on the fibrinolytic components contained in with whole blood (plasma and red cells) was very much the red cell, or on the possible physiologic role of red shorter than that of clots made with plasma alone, in- cells in thrombolysis. dicating a fibrinolytic component in red cells. A plas- Kolmen, Guest, and Celander (8) showed that erythro- minogen activator was found in the stroma-free he- cytes may absorb UK and protect it from plasma in- molysate, and proteolytic activity was found in the stro- hibitors. Kunzer and Haberhausen (9) found "plasmin- mal fraction. The plasminogen activator, purified by like activity" in the red cell stroma. Back et al. (10) using diethylaminoethyl-cellulose (DEAE-cellulose) in extracted a fibrinolytic "potentiating agent" from hu- a batch procedure followed by column chromatography, man erythrocytes which appeared to increase the lytic was called erythrokinase (EK). On preliminary char- potential of a given dose of UK or UK-activated plas- acterization, EK appears to activate human and bovine minogen on human blood clots or thrombi. Tymin'ski and plasminogen in a manner similar to urokinase (UK), Czestochowska found a fibrinolytic, plasminogen-like as determined by fibrinolytic and caseinolytic assays. proenzyme and traces of an activating substance in the The two enzymes can be separated by DEAE chroma- hemolysate (11). tography and acrylamide-gel electrophoresis, however, This communication is concerned with the isolation and they hydrolyze acetyl-L-lysine methyl ester and and characterization of a new factor present in hu- benzoyl arginine methyl ester at different rates. man erythrocytes, a plasminogen activator of the uro- kinase type which will be called erythrokinase (EK). INTRODUCTION The new factor will also be physically and chemically The plasminogen activators streptokinase (SK), from distinguished from urokinase (UK). the hemolytic streptococcus, and urokinase (UK), from METHODS human urine, have been used under controlled condi- tions to man Sodium phosphate buffer (0.003 moles/liter, pH 7.0) was produce experimental thrombolysis in used unless noted otherwise. Diethylaminoethyl-cellulose (1, 2). However, it has been shown that thrombolysis (DEAE),' 1 mEq/g, was recycled for use by the method in vivo is influenced by the amounts of the various of Sober, Gutter, Wyckoff, and Peterson (12) and equili- fibrinolytic components in plasma (3), other body brated in phosphate buffer. The columns were 64 x 2.5 cm, fluids (4), various tissues (5), and by the components and the flow rate was set at 50 ml/hr with a positive-dis- placement pump.2 of the thrombus itself: fibrin stabilizing factor, fibrin, EK and UK were subjected to disc electrophoresis on platelets (6), white blood cells (7), and erythrocytes acrylamide gel, according to the method of Ornstein (13) (8). and Davis (14) in a Canalco3 disc electrophoresis appa- Although large numbers of erythrocytes are usually ratus. Continuous systems were run at pH 7.2 and pH 2.3, enmeshed in thrombi, there has been relatively limited as well as discontinuous systems described by Williams and Reisfeld (15) at pH 4.5 and pH 9.0, for 2 hr at 5 ma per A preliminary report of this work was presented at the tube, using 7%o acrylamide gel. The gels were stained with 10th Congress of the International Society of Hematology, Stockholm, Sweden, 1964. 'Whatman DEAE-Cellulose, H. Reeve Angel & Co., Inc., The present address of M. Semar and L. Skoza is Clifton, N. J. New York Medical College, New York 10029. 2Sigmamotor Pump, Model TM-20, Sigmamotor Inc., Received for publication 24 October 1968 and in revised Middleport, N. Y. form 16 June 1969. ' Canal Industries, Bethesda, Md. The Journal of Clinical Investigation Volume 48 1969 1777 100 U, 0 80 c E 60 1= n 40 z 0-o -J 0 20 w I I I IL -.. I.-. 0 0.2 0.5 0.7 1.0 1.2 1.5 HEMOLYZED RED CELLS ADDED, ml FIGURE 1 Effect of increasing amounts of red cells on plasma euglobulin lysis time. Varying amounts of washed, hemolyzed red cells from one subject were added to a constant amount of his plasma (0.7 ml), and the euglobulin precipitated from this mixture was reconstituted in saline phosphate buffer. aniline black or cut with a Canalco lateral gel slicer into Preparation of red cell hemolysate. Red cells were ob- discs 1.0 mm thick. The discs were eluted for assay with tained from outdated human blood (over 3 wk old) collected 1 M NaCl and dialyzed against 0.01 M phosphate-buffered by the American National Red Cross in acid-citrate dex- normal saline, pH 7.2. trose (ACD), 435 ml blood plus 65.25 ml ACD (Formula Measurement of fibrinolytic activity. The clot lysis time A of the NIH). The cells were washed at least three times was used to measure the fibrinolytic activity of euglobulin with an equal volume of cold isotonic saline (40C), cen- fractions from whole blood or plasma (16). The activity trifuged at 10,000 g for 15 min in a refrigerated centrifuge of column fractions was measured on heated and unheated after which the supernatant and leukocyte layer were dis- bovine fibrin plates (17) to differentiate activator and carded. The cells were hemolyzed by adding an equal vol- plasmin. The activator activity of UK' and partially puri- ume of distilled water at 4VC and freeze-thawing five times fied EK was determined by a standard clot fibrinolytic as- in an acetone-dry ice mixture. The hemolysate was then say system on intermediate- or high-purity soluble plasmi- diluted X 50 with 0.003 M phosphate buffer, pH 7.0. When nogen (with < 1% spontaneous plasmin activity) and a 5% dextrose was used in a settling tank to aggregate and caseinolytic assay system (alpha casein) (16, 18). Protein wash large volumes of red cells, the freeze-thawing step determinations were carried out on these materials by the was omitted. These stroma-containing solutions will be called biuret procedure (19). Esterase activity of UK and EK was the original hemolysate. measured by hydrolysis of benzoyl arginine methyl ester (BAMe)' and acetyl-L-lysine methyl ester (ALMe)' (20). RESULTS The effect of different fibrinolytic inhibitors on EK and UK was also determined (16, 21). These inhibitors in- The whole-blood euglobulin lysis time was previously cluded: epsilon aminocaproic acid (EACA),7 Trasylol,' found to be shorter than the plasma euglobulin lysis Iniprol,' and 4-aminomethylbenzoic acid.1 time at all levels of fibrinolytic activity (16). For ex- ample, the average lysis time for 33 normal men and 'Kindly supplied by Abbott Laboratories, North Chicago, women was 66 ±6 min (SE) for whole-blood euglobulin Ill., and Sterling-Winthrop Research Institute, a Division of Sterling Drug, Inc., Rensselaer, N. Y. and 162 ±24 min (SE) for plasma euglobulin. In view 'Mann Research Labs. Inc., New York. of this marked difference in activity, varying amounts °Cyclo Chemical Co., Los Angeles, Calif. added a volume 7Lederle Laboratories, Pearl River, N. Y. of hemolyzed red cells were to constant 'Farbenfabriken Bayer AG, Leverkusen, Germany; U. S. of plasma. The euglobulin fraction was prepared for distributor, FBA Pharmaceuticals Inc., New York. each dilution, and reconstituted to a final volume of 'Laboratoire Choay, Paris, France. 1.0 ml. Fig. 1 shows that lysis was enhanced by in- 10 Sterling-Winthrop Research Institute, a Division of Sterling Drug, Inc., Rensselaer, N. Y. creasing amounts of hemolyzed red cells. 1778 M. Semar, L. Skoza, and A. J. Johnson 3w0 F- W 2z E - 4 0 E 0. I005J cr.O2.0 z 0 CN 2 0 CM 44FE 'u z j 1.0 .50 M U IL. F 0 0. 0 -i IL. 0 z 0 O N 20 40 60 TUBE 0.5 M KCL -B - * NUMBER FIGURE 2 Separation of erythrocyte activator from hemolysate by DEAE cel- lulose chromatography. Original hemolysate was adsorbed on DEAE by batch methods and washed with 0.003 M phosphate buffer, pH 7.0, to remove the hemo- globin and the plasmin-like activity. This DEAE, with adsorbed activator, was placed on top of a previously prepared DEAE column and eluted with 0.5 M KC1. In view of this observation, attempts were made to moglobin-containing supernatant was decanted. Addi- isolate the erythrocyte factor responsible for the en- tional hemoglobin and the plasmin-like proteolytic ac- hanced fibrinolytic activity.
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