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Activation of Human Complement by Immunoglobulin G Antigranulocyte Antibody

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Activation of Human Complement by Immunoglobulin G Antigranulocyte Antibody Activation of human complement by immunoglobulin G antigranulocyte antibody. P K Rustagi, … , M S Currie, G L Logue J Clin Invest. 1982;70(6):1137-1147. https://doi.org/10.1172/JCI110712. Research Article The ability of antigranulocyte antibody to fix the third component of complement (C3) to the granulocyte surface was investigated by an assay that quantitates the binding of monoclonal anti-C3 antibody to paraformaldehyde-fixed cells preincubated with Felty's syndrome serum in the presence of human complement. The sera from 7 of 13 patients with Felty's syndrome bound two to three times as much C3 to granulocytes as sera from patients with uncomplicated rheumatoid arthritis. The complement-activating ability of Felty's syndrome serum seemed to reside in the monomeric IgG-containing serum fraction. For those sera capable of activating complement, the amount of C3 fixed to granulocytes was proportional to the amount of granulocyte-binding IgG present in the serum. Thus, complement fixation appeared to be a consequence of the binding of antigranulocyte antibody to the cell surface. These studies suggest a role for complement-mediated injury in the pathophysiology of immune granulocytopenia, as has been demonstrated for immune hemolytic anemia and immune thrombocytopenia. Find the latest version: https://jci.me/110712/pdf Activation of Human Complement by Immunoglobulin G Antigranulocyte Antibody PRADIP K. RUSTAGI, MARK S. CURRIE, and GERALD L. LOGUE, Departments of Medicine, Duke University and Durham Veterans Administration Medical Centers, Durham, North Carolina 27710; Department of Medicine, State University of New York at Buffalo, Buffalo General Hospital, Buffalo, New York 14203 A B S T R A C T The ability of antigranulocyte antibody munoglobulin-mediated complement activation in cell to fix the third component of complement (C3) to the destruction is well understood in warm antibody au- granulocyte surface was investigated by an assay that toimmune hemolytic anemia (2), cold agglutinin he- quantitates the binding of monoclonal anti-C3 anti- molysis (2, 3), and quinidine purpura (4). Despite the body to paraformaldehyde-fixed cells preincubated apparent clinical analogy of immune granulocyto- with Felty's syndrome serum in the presence of human penia to immune hemolytic anemia and immune complement. The sera from 7 of 13 patients with thrombocytopenia, immunologic mechanisms directed Felty's syndrome bound two to three times as much against granulocytes are not well defined in immune C3 to granulocytes as sera from patients with uncom- granulocytopenia. Specifically, the ability of antigran- plicated rheumatoid arthritis. The complement-acti- ulocyte antibody to activate and fix human comple- vating ability of Felty's syndrome serum seemed to ment to granulocytes has not been explored. reside in the monomeric IgG-containing serum frac- Although cell-mediated immunity appears to be in- tion. For those sera capable of activating complement, volved in some patients with autoimmune granulo- the amount of C3 fixed to granulocytes was propor- cytopenia (5, 6), we and others have demonstrated that tional to the amount of granulocyte-binding IgG pres- patients with Felty's syndrome (FS)' often have in- ent in the serum. Thus, complement fixation appeared creased serum granulocyte-binding IgG (7-11). By to be a consequence of the binding of antigranulocyte analogy with immune hemolytic anemia and immune antibody to the cell surface. These studies suggest a thrombocytopenia, one might expect some FS sera to role for complement-mediated injury in the patho- bind complement to granulocytes. Membrane-bound physiology of immune granulocytopenia, as has been components of complement may modulate the host's demonstrated for immune hemolytic anemia and im- interaction with its own granulocytes by involving cells mune thrombocytopenia. with receptors for those components (12). The ability of antigranulocyte antibodies to fix complement to INTRODUCTION granulocytes may have implications for the type and subclass of immunoglobulin involved in granulocyte Binding of antibody to surface antigens and fixation destruction, in addition to providing information of complement to the surfaces of cells are two of a about the arrangement of granulocyte surface anti- variety of mechanisms that mediate immunologic in- gens. Consequently, we sought to determine whether jury to cells of patients with immune hemolytic anemia antibodies in the sera of patients with FS fixed com- and immune thrombocytopenia (1). The role of im- plement to granulocytes. In this study, we describe an assay system to detect This work was presented, in part, at the Southern Section and quantitate the third component of human com- Meeting of The American Federation of Clinical Research, New Orleans, LA, on 14 January, 1982. Address all correspondence to Dr. P. K. Rustagi, Hema- I Abbreviations used in this paper: anti-C3, 1251-labeled tology Laboratory, Buffalo General Hospital, Buffalo, NY anti-C3 antibody; C3, third component of human comple- 14203. ment; FS, Felty's syndrome; PFG, paraformaldehyde-fixed Received for publication 21 April 1982 and in revised granulocytes; RA, rheumatoid arthritis; SPA, 125I-labeled form 19 August 1982. staphylococcal protein A; VBS, veronal-buffered saline. J. Clin. Invest. (D The American Society for Clinical Investigation, Inc. * 0021-9738/82/12/1137/11 $1.00 1137 Volume 70 December 1982 1137-1147 plement (C3) on the granulocyte surface and provide mouse ascites fluid (Bethesda Research Laboratories, Inc., evidence for the ability of serum from patients with Gaithersburg, MD) by ammonium sulfate precipitation and DE52 (Whatman, Inc., Clifton, NJ) ion exchange column FS to activate complement and fix C3 to allogeneic chromatography according to the method of Parker et al. granulocytes. Most FS sera were able to fix greater (16). This antibody reacts with C3, C3b, C3bi, and C3c, but amounts of CS to granulocytes than sera from patients not C3d. Purity of the antibody was established by the pres- with uncomplicated rheumatoid arthritis (RA), and ence of only two distinct bands on sodium dodecyl sulfate to reside in the monomeric (SDS) reduced polyacrylamide gel electrophoresis. A single this ability appeared IgG- precipitin line was noted upon agarose gel immunodiffusion containing fraction of FS serum. For the majority of against goat anti-mouse whole serum and anti-mouse IgG2b patients, the amount of C3 fixed was directly related (Meloy Laboratories, Inc., Springfield, VA) and against pu- to the amount of granulocyte-binding IgG present. rified human C3 (gift of C. J. Parker) in a 5% (wt/vol) poly- ethylene glycol and 1% (wt/vol) agarose gel. The antibody was radioiodinated using the chloramine-T METHODS method (17). 1.0 mCi 1251 in sodium hydroxide (Amersham Corp., Arlington Heights, IL) was added to 100 ug antibody Patients. Sera from 13 patients with classic FS were ex- at 4°C. 10 ,Il chloramine-T (1 mg/ml in 0.2 M borate buff- amined. The group consisted of nine males and four females. ered isotonic saline pH 8.0 with 10 mg% (wt/vol) sodium There was no history of blood transfusion in 9 of the 13 azide) was added to initiate the reaction, which was ter- patients. Two patients, both males, had undergone splenec- minated after 30 min by the addition of 10 uIl potassium tomy, and one of them had responded with normalization iodide (1 M). 1251-Labeled anti-CS antibody (anti-C3) was of his granulocyte count. Both of these patients had been separated from unbound 125I by filtration through a Sephadex transfused preoperatively and serum for testing was obtained G-25M PD-10 column (Pharmacia Fine Chemicals, Inc., 5 yr after transfusion. Two other male patients had been Piscataway, NJ) in VBS at room temperature. Greater than transfused 4 and 2 yr before testing. All four females were 98% of the radioactivity in the initial peak was trichlor- over 55 yr of age and one was multiparous. All patients acetic acid-precipitable, indicating efficient separation. Spe- except one were granulocytopenic (granulocyte count cific activities of anti-CS preparations were 2.4 and 9.5 mil- < 1000/cm3) at the time of study. lion cpm/,ug. Protein concentration was 20 ,ig/ml by protein Sera and complement sources. Control sera from normal assay (Bio-Rad Laboratories, Richmond, CA). 0.1% (wt/vol) volunteers and patients without RA or immune granulocy- bovine serum albumin (Sigma Chemical Co.) was added to topenia, and test sera from patients with uncomplicated RA the final solution to minimize autoirradiation damage. and patients with FS were obtained from peripheral venous Measurement of surface-bound C3. In the standard as- blood that had been allowed to clot at room temperature. say, 200 ul PFG were added to a dilution of test serum or Following centrifugation at 800 g, the sera were stored at VBS followed by the addition of a dilution of type-compat- -50°C for up to 12 mo. Sera were obtained from healthy ible fresh normal serum as a source of complement. The volunteers for use in the fresh state as a source of comple- entire 600 gl reaction mixture was incubated at 370C (in- ment. Immediately before use, thawed test sera and fresh cubation 1) and the reaction terminated by ice bath tem- sera were centrifuged for 1.5 min in a Beckman Microfuge peratures. Reacted cells were washed twice at room tem- B miniature centrifuge (Beckman Instruments, Inc., Palo perature in VBS and resuspended in McCoy's Medium 5A, Alto, CA) and then diluted with veronal-buffered isotonic modified with L-glutamine and 15% fetal calf serum (B & saline pH 7.4 with 0.15 mM calcium chloride and 0.50 mM B Research Laboratories, Inc., Durham, NC). An aliquot was magnesium chloride (VBS) (13). removed for the determination of cell number by automatic Granulocytes. Peripheral venous blood from 0 blood blood cell counter (Coulter Electronics, Inc., Hialeah, FL) type normal male volunteers and from one splenectomized and the remainder was assayed in triplicate for the presence nongranulocytopenic patient with FS was drawn into hep- of surface-bound C3.
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