Activation of the alternative pathway of complement by calcium-loaded erythrocytes resulting from loss of membrane phospholipid asymmetry

Journal of Laboratory and Clinical Medicine

Volumn 130, Issue 2, 1997, Pages 169-182

  Test, Samuel T ^a   Mitsuyoshi, Joyce ^a  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0031214844     PISSN: 00222143     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2143(97)90093-7     Document Type: Article

References (74)

1. Schroit AJ, Zwaal RFA. Transbilayer movement of phospholipids in red cell and platelet membranes. Biochim Biophys Acta 1991;1071:313-29.
2. Zachowski A. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem J 1993;294:1-14.
3. Mann KG, Nesheim ME, Church WR, Haley P, Krishnaswamy S. Surface-dependent reactions of the vitamin K-dependent enzyme complexes. Blood 1990;76:1-16.
4. Chiu D, Lubin B, Roelofsen B, van Deenen LLM. Sickled erythrocytes accelerate clotting in vitro: an effect of abnormal membrane lipid asymmetry. Blood 1981;58:398-401.
5. Connor J, Pak CC, Schroit AJ. Exposure of phosphatidylserine in the outer leaflet of human red blood cells: relationship to cell density, cell age, and clearance by mononuclear cells. J Biol Chem 1994;269:2399-404.
6. Diaz C, Morkowski J, Schroit AJ. Generation of phenotypically aged phosphatidylserine-expressing erythrocytes by dilauroylphosphatidylcholine-induced vesiculation. Blood 1996;87:2956-61.
7. Richards RL, Gewurz H, Osmand AP, Alving CR. Interactions of C-reactive protein and complement with liposomes. Proc Natl Acad Sci U S A 1977;74:5672-6.
8. Richards RL, Gewurz H, Siegel J, Alving CR. Interactions of C-reactive protein and complement with liposomes: II. Influence of membrane composition. J Immunol 1979;122: 1185-9.
9. Cunningham CM, Kingzette M, Richards RL, Alving CR, Lint TF, Gewurz H. Activation of human complement by liposomes: a model for membrane activation of the alternative pathway. J Immunol 1979;122:1237-42.
10. Mold C, Gewurz H. Activation of human complement by liposomes: serum factor requirement for alternative pathway activation. J Immunol 1980;125:696-700.
11. Okada N, Yasuda T, Tsumita T, Okada H. Activation of the alternative complement pathway of guinea-pig by liposomes incorporated with trinitrophenylated phosphatidylethanolamine. Immunology 1982;45:115-24.
12. Okada N, Yasuda T, Okada H. Restriction of alternative complement pathway activation by sialosylglycolipids. Nature 1982;299:261-3.
13. Okada N, Yasuda T, Tsumita T, Shinomiya H, Utsumi S, Okada H. Regulation by glycophorin of complement activation via the alternative pathway. Biochem Biophys Res Commun 1982;108:770-5.
14. Kovacsovics T, Tschopp J, Kress A, Isliker H. Antibody-independent activation of C1, the first component of complement, by cardiolipin. J Immunol 1985;135:2695-700.
15. Comis A, Easterbrook-Smith SB. Inhibition of serum complement haemolytic activity by lipid vesicles containing phosphatidylserine. FEBS Lett 1986;197:321-7.
16. Tomasko MA, Chudwin DS. Complement activation in sickle cell disease: a liposome model. J Lab Clin Med 1988;112:248-53.
17. Michalek MT, Bremer EG, Mold C. Effect of gangliosides on activation of the alternative pathway of human complement. J Immunol 1988;140:1581-7.
18. Mold C. Effect of membrane phospholipids on activation of the alternative complement pathway. J Immunol 1989;143: 1663-8.
19. Chonn A, Cullis PR, Devine DV. The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J Immunol 1991;146:4234-41.
20. Marjan J, Xie Z, Devine DV. Liposome-induced activation of the classical complement pathway does not require immunoglobulin. Biochim Biophys Acta 1994;1192:35-44.
21. Myher JJ, Kuksis A, Pind S. Molecular species of glycero-phospholipids and sphingomyelins of human erythrocytes: improved method of analysis. Lipids 1989;24:396-407.
22. Engelmann B, Schönthier UM, Richter WO, Duhm J. Changes of membrane phospholipid composition of human erythrocytes in hyperlipidemias. II. Increases in distinct molecular species of phosphatidylethanolamine and phosphatidylcholine containing arachidonic acid. Biochim Biophys Acta 1992;1165:38-44.
23. Wang RH, Phillips GJ, Medof ME, Mold C. Activation of the alternative complement pathway by exposure of phosphatidylethanolamine and phosphatidylserine on erythrocytes from sickle cell disease patients. J Clin Invest 1993;92:1326-35.
24. Bevers EM, Comfurius P, Zwaal RFA. Changes in membrane phospholipid distribution during platelet activation. Biochim Biophys Acta 1983;736:57-66.
25. Haest CW, Deuticke B. Experimental alteration of phospholipid-protein interactions within the human erythrocyte membrane: dependence on glycolytic metabolism. Biochim Biophys Acta 1975;401:468-80.
26. Haest CW, Deuticke B. Possible relationship between membrane proteins and phospholipid asymmetry in the human erythrocyte membrane. Biochim Biophys Acta 1976;436:353-65.
27. Haest CW, Plasa G, Kamp D, Deuticke B. Spectrin as a stabilizer of the phospholipid asymmetry in the human erythrocyte membrane. Biochim Biophys Acta 1978;509:21-32.
28. Franck PFH, Op den Kamp JAF, Roelofsen B, van Deenen LLM. Does diamide treatment of intact human erythrocytes cause a loss of phospholipid asymmetry? Biochim Biophys Acta 1986;857:127-30.
29. Middelkoop E, Van der Hoek EE, Bevers EM, Comfurius P, Slotboom AJ, Op den Kamp JAF, et al. Involvement of ATP-dependent aminophospholipid translocation in maintaining phospholipid asymmetry in diamide-treated human erythrocytes. Biochim Biophys Acta 1989;981:151-60.
30. Raval PJ, Allan D. Phospholipid asymmetry in the membranes of intact human erythrocytes and in spectrin-free microvesicles derived from them. Biochim Biophys Acta 1984;772:192-6.
31. Chandra R, Joshi PC, Bajpai VK, Gupta CM. Membrane phospholipid organization in calcium-loaded human erythrocytes. Biochim Biophys Acta 1987;902:253-62.
32. Bitbol M, Fellmann P, Zachowski A, Devaux PF. Ion regulation of phosphatidylserine and phosphatidylethanolamine outside-inside translocation in human erythrocytes. Biochim Biophys Acta 1987;904:268-82.
33. Comfurius P, Senden JMG, Tilly RHJ, Schroit AJ, Bevers EM, Zwaal RFA. Loss of membrane phospholipid asymmetry in platelets and red cells may be associated with calcium-induced shedding of plasma membrane and inhibition of aminophospholipid translocase. Biochim Biophys Acta 1990; 1026:153-60.
34. 2+ induces transbilayer redistribution of all major phospholipids in human erythrocytes. Biochemistry 1992;31: 6355-60.
35. Funakoshi T, Heimark RL, Hendrickson LE, McMullen BA, Fujikawa K. Human placental anticoagulant protein: isolation and characterization. Biochemistry 1987;26:5572-8.
36. Tait JF, Gibson D, Fujikawa K. Phospholipid binding properties of human placental anticoagulant protein-I, a member of the lipocortin family. J Biol Chem 1989;264:7944-9.
37. 2+-dependent phospholipid binding, vesicle aggregation and membrane fusion by annexins. Biochem J 1990;266:195-200.
38. Andree HAM, Reutelingsperger CPM, Hauptmann R, Hemker HC, Hermens WT, Willems GM. Binding of vascular anticoagulant α (VACα) to planar phospholipid bilayers. J Biol Chem 1990;265:4923-8.
39. Tait JF, Gibson D. Phospholipid binding of annexin V: effects of calcium and membrane phosphatidylserine content. Arch Biochem Biophys 1992;298:187-91.
40. Meers P, Mealy T. Calcium-dependent annexin V binding to phospholipids: stoichiometry, specificity, and the role of negative charge. Biochemistry 1993;32:11711-21.
41. Zachowski A, Favre E, Cribier S, Hervé P, Devaux PF. Outside-inside translocation of aminophospholipids in the human erythrocyte membrane is mediated by a specific enzyme. Biochemistry 1986;25:2585-90.
42. Dachary-Prigent J, Freyssinet J-M, Pasquet J-M, Carron J-C, Nurden AT. Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: a flow cytometry study showing a role for free sulfhydryl groups. Blood 1993;81:2554-65.
43. Scesney SM, Makrides SC, Gosselin ML, Ford PJ, Andrews BM, Hayman EG, et al. A soluble deletion mutant of the human complement receptor type 1, which lacks the C4b binding site, is a selective inhibitor of the alternative complement pathway. Eur J Immunol 1996;26:1729-35.
44. Thiagarajan P, Tait JF. Binding of annexin V/placental anticoagulant protein I to platelets. J Biol Chem 1990;265:17420-3.
45. Thiagarajan P, Tait JF. Collagen-induced exposure of anionic phospholipid in platelets and platelet-derived microparticles. J Biol Chem 1991;266:24302-7.
46. Tait JF, Gibson D. Measurement of membrane phospholipid asymmetry in normal and sickle-cell erythrocytes by means of annexin V binding. J Lab Clin Med 1994;123:741-8.
47. Yuan J, Kuypers FA, Lewis RA, Fucharoen S, Bunyaratvej A, Schrier SL. Membrane lipid asymmetry in thalassemic red blood cells. Blood 1994;84:259a.
48. Kuypers FA, Lewis RA, Hua M, Schott MA, Discher D, Ernst JD, et al. Detection of altered membrane phospholipid asymmetry in subpopulations of human red blood cells using fluorescently labeled annexin V. Blood 1996;87:1179-87.
49. Edens RE, Linhardt RJ, Weiler JM. Heparin is not just an anticoagulant anymore: six and one-half decades of studies on the ability of heparin to regulate complement activity. In: Cruse JM, Lewis REJ, editors. Complement today: complement profiles. Basel: Karger, 1993:96-120.
50. 2+-induced biochemical changes in human erythrocytes and their relation to microvesiculation. Biochem J 1981;198:433-40.
51. 2+-enriched human erythrocytes: an immunochemical study. J Biol Chem 1983;258:5300-5.
52. Schifferli JA, Ng YC, Peters DK. The role of complement and its receptor in the elimination of immune complexes. N Engl J Med 1986;315:488-95.
53. Seya T, Turner JR, Atkinson JP. Purification and characterization of a membrane protein (gp45-70) that is a cofactor for cleavage of C3b and C4b. J Exp Med 1986;163:837-55.
54. Nicholson-Weller A, Burge J, Fearon DT, Weller PF, Austen KF. Isolation of a human erythrocyte membrane glycoprotein with decay-accelerating activity for C3 convertases of the complement system. J Immunol 1982;129:184-9.
55. Ezzell JL, Wilcox LA, Bernshaw NJ, Parker CJ. Induction of the paroxysmal nocturnal hemoglobinuria phenotype in normal human erythrocytes: effects of 2-aminoethylisothiouronium bromide on membrane proteins that regulate complement. Blood 1991;77:2764-73.
56. Wilcox LA, Ezzell JL, Bernshaw NJ, Parker CJ. Molecular basis of the enhanced susceptibility of the erythrocytes of paroxysmal nocturnal hemoglobinuria to hemolysis in acidified serum. Blood 1991;78:820-9.
57. Weiler JM, Daha MR, Austen KF, Fearon DT. Control of the amplification convertase of complement by the plasma protein β1H. Proc Natl Acad Sci U S A 1976;73:3268-72.
58. Pangburn MK, Schreiber RD, Müller-Eberhard HJ. Human complement C3b inactivator: isolation, characterization, and demonstration of an absolute requirement for the serum protein β1H for cleavage of C3b and C4b in solution. J Exp Med 1977;146:257-70.
59. Men S, Pangburn MK. Discrimination between activators and nonactivators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H. Proc Natl Acad Sci U S A 1990;87:3982-6.
60. Test ST, Mitsuyoshi J. Calcium-loaded erythrocytes have a defect in complement regulation distinct from that resulting from exposure to 2-aminoethylisothiouronium bromide. Blood 1995;86:2799-806.
61. Bevers EM, Comfurius P, Zwaal RF. The nature of the binding site for prothrombinase at the platelet surface as revealed by lipolytic enzymes. Eur J Biochem 1982;122:81-5.
62. Mohandas N. The red cell membrane. In: Hoffman R, Benz EJ Jr, Shattil SJ, Furie B, Cohen HJ, Silberstein LE, editors. Hematology: basic principles and practice. 2nd ed. New York: McGraw-Hill, 1995:438-43.
63. Smirnov MD, Esmon CT. Phosphatidylethanolamine incorporation into vesicles selectively enhances factor Va inactivation by activated protein C. J Biol Chem 1994;269:816-9.
64. Neuenschwander PF, Bianco-Fisher E, Rezaie AR, Morrissey JH. Phosphatidylethanolamine augments factor VIIa-tissue factor activity: enhancement of sensitivity to phosphatidylserine. Biochemistry 1995;34:13988-93.
65. 2+-induced microvesiculation and deficient expression of procoagulant activity in erythrocytes from a patient with a bleeding disorder: a study of the red blood cells of Scott syndrome. Blood 1992;79:380-8.
66. Kazatchkine MD, Fearon DT, Silbert JE, Austen KF. Surface-associated heparin inhibits zymosan-induced activation of the human alternative complement pathway by augmenting the regulatory action of the control proteins on particle-bound C3b. J Exp Med 1979;150:1202-15.
67. Allan D, Hagelberg C, Kallen K-J, Haest CWM. Echinocytosis and microvesiculation of human erythrocytes induced by insertion of merocyanine 540 into the outer membrane leaflet. Biochim Biophys Acta 1989;986:115-22.
68. Brown EJ. Complement receptors, adhesion, and phagocytosis. Infect Agents Dis 1992;1:63-70.
69. Rigotti A, Acton SL, Krieger M. The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J Biol Chem 1995;270:16221-24.
70. Ramprasad MP, Fischer W, Witztum JL, Sambrano GR, Quehenberger O, Steinberg D. The 94- to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc Natl Acad Sci U S A 1995;92:9580-4.
71. Puente Navazo MD, Daviet L, Savill J, Ren Y, Leung LLK, McGregor JL. Identification of a domain (155-183) on CD36 implicated in the phagocytosis of apoptotic neutrophils. J Biol Chem 1996;271:15381-5.
72. Wilson WA, Thomas EJ, Sissons JGP. Complement activation in asymptomatic patients with sickle cell anaemia. Clin Exp Immunol 1979;36:130-9.
73. Chudwin DS, Korenblit AD, Kingzette M, Artrip S, Rao S. Increased activation of the alternative complement pathway in sickle cell disease. Clin Immunol Immunopathol 1985;37:93-7.
74. DeCeulaer K, Wilson WA, Morgan AG, Serjeant GR. Plasma haemoglobin and complement activation in sickle cell disease. J Clin Lab Immunol 1981;6:57-60.