Procoagulant and prothrombotic activation of human erythrocytes by phosphatidic acid

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 299, Issue 2, 2010, Pages

  Noh, Ji Yoon ^a   Lim, Kyung Min ^a   Bae, Ok Nam ^a   Chung, Seung Min ^a   Lee, Sang Wook ^a   Joo, Kyung Mi ^b   Lee, Sin Doo ^a   Chung, Jin Ho ^a  

^a Seoul National University   (South Korea)

^b AmorePacific Corporation   (South Korea)

Author keywords

Phosphatidylserine; Procoagulant activation; Thrombus formation

Indexed keywords

CALCIUM ION; DIACYLGLYCEROL; LYSOPHOSPHATIDIC ACID; PHOSPHATIDATE PHOSPHATASE; PHOSPHATIDIC ACID; PHOSPHATIDYLSERINE; PHOSPHOLIPASE A2; PHOSPHOLIPASE D; PROTEIN KINASE C ALPHA; SCRAMBLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL ADHESION; CONTROLLED STUDY; ENZYME ACTIVITY; ERYTHROCYTE; ERYTHROCYTE AGGREGATION; HUMAN; HUMAN CELL; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; THROMBOGENESIS; VEIN THROMBOSIS;

ANIMALS; BLOOD COAGULATION; CALCIUM; CELL ADHESION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENZYME ACTIVATION; ENZYME INHIBITORS; ERYTHROCYTE AGGREGATION; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HUMANS; MALE; PHOSPHATIDATE PHOSPHATASE; PHOSPHATIDIC ACIDS; PHOSPHATIDYLSERINES; PHOSPHOLIPASE D; PHOSPHOLIPASES A2; PHOSPHOLIPID TRANSFER PROTEINS; PROTEIN KINASE C-ALPHA; RATS; RATS, SPRAGUE-DAWLEY; THROMBIN; THROMBOPLASTIN; THROMBOSIS; TIME FACTORS;

EID: 77955446701     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01144.2009     Document Type: Article

References (59)

1. Billah MM, Eckel S, Mullmann TJ, Egan RW, Siegel MI. Phosphatidylcholine hydrolysis by phospholipase D determines phosphatidate and diglyceride levels in chemotactic peptide-stimulated human neutrophils. Involvement of phosphatidate phosphohydrolase in signal transduction. J Biol Chem 264: 17069-17077, 1989.
2. Bocckino SB, Blackmore PF, Wilson PB, Exton JH. Phosphatidate accumulation in hormone-treated hepatocytes via a phospholipase D mechanism. J Biol Chem 262: 15309-15315, 1987.
3. Bocckino SB, Wilson PB, Exton JH. Phosphatidate-dependent protein phosphorylation. Proc Natl Acad Sci USA 88: 6210-6213, 1991.
4. Bonomini M, Sirolli V, Gizzi F, Di Stante S, Grilli A, Felaco M. Enhanced adherence of human uremic erythrocytes to vascular endothelium: role of phosphatidylserine exposure. Kidney Int 62: 1358-1363, 2002.
5. Bonomini M, Sirolli V, Settefrati N, Dottori S, Di Liberato L, Arduini A. Increased erythrocyte phosphatidylserine exposure in chronic renal failure. J Am Soc Nephrol 10: 1982-1990, 1999.
6. Buboltz JT, Feigenson GW. A novel strategy for the preparation of liposomes: rapid solvent exchange. Biochim Biophys Acta 1417: 232-245, 1999.
7. Butikofer P, Yee MC, Schott MA, Lubin BH, Kuypers FA. Generation of phosphatidic acid during calcium-loading of human erythrocytes. Evidence for a phosphatidylcholine-hydrolyzing phospholipase D. Eur J Biochem 213: 367-375, 1993.
8. Chen Y, Rodrik V, Foster DA. Alternative phospholipase D/mTOR survival signal in human breast cancer cells. Oncogene 24: 672-679, 2005.
9. Chung SM, Bae ON, Lim KM, Noh JY, Lee MY, Jung YS, Chung JH. Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 27: 414-421, 2007.
10. Daleke DL. Regulation of transbilayer plasma membrane phospholipid asymmetry. J Lipid Res 44: 233-242, 2003.
11. 2+-extrusion in individual red blood cells. Cytometry A 71: 693-699, 2007.
12. de Jong K, Rettig MP, Low PS, Kuypers FA. Protein kinase C activation induces phosphatidylserine exposure on red blood cells. Biochemistry 41: 12562-12567, 2002.
13. Demiroglu H. The importance of erythrocyte aggregation in blood rheology: considerations on the pathophysiology of thrombotic disorders. Blood 89: 4236, 1997.
14. Dumez H, Reinhart WH, Guetens G, de Bruijn EA. Human red blood cells: rheological aspects, uptake, and release of cytotoxic drugs. Crit Rev Clin Lab Sci 41: 159-188, 2004.
15. 3 integrin activation and shear-dependent thrombus formation in mice lacking phospholipase D1. Sci Signal 3: ra1, 2010.
16. Falk E, Shah PK, Fuster V. Coronary plaque disruption. Circulation 92: 657-671, 1995.
17. Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen J. Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294: 1942-1945, 2001.
18. Fourcade O, Simon MF, Viode C, Rugani N, Leballe F, Ragab A, Fournie B, Sarda L, Chap H. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell 80: 919-927, 1995.
19. Garcia-Garcia J, Corbalan-Garcia S, Gomez-Fernandez JC. Effect of calcium and phosphatidic acid binding on the C2 domain of PKCα as studied by Fourier transform infrared spectroscopy. Biochemistry 38: 9667-9675, 1999.
20. Gomez-Munoz A, Martens JS, Steinbrecher UP. Stimulation of phospholipase D activity by oxidized LDL in mouse peritoneal macrophages. Arterioscler Thromb Vasc Biol 20: 135-143, 2000.
21. Hilarius PM, Ebbing IG, Dekkers DW, Lagerberg JW, de Korte D, Verhoeven AJ. Generation of singlet oxygen induces phospholipid scrambling in human erythrocytes. Biochemistry 43: 4012-4019, 2004.
22. Holinstat M, Voss B, Bilodeau ML, Hamm HE. Protease-activated receptors differentially regulate human platelet activation through a phosphatidic acid-dependent pathway. Mol Pharmacol 71: 686-694, 2007.
23. Horne MK, 3rd, Cullinane AM, Merryman PK, Hoddeson EK. The effect of red blood cells on thrombin generation. Br J Haematol 133: 403-408, 2006.
24. Jerjes-Sanchez C. Venous and arterial thrombosis: a continuous spectrum of the same disease? Eur Heart J 26: 3-4, 2005.
25. Kaestner L, Tabellion W, Lipp P, Bernhardt I. Prostaglandin E2 activates channel-mediated calcium entry in human erythrocytes: an indication for a blood clot formation supporting process. Thromb Haemost 92: 1269-1272, 2004.
26. Kean LS, Brown LE, Nichols JW, Mohandas N, Archer DR, Hsu LL. Comparison of mechanisms of anemia in mice with sickle cell disease and β-thalassemia: peripheral destruction, ineffective erythropoiesis, and phospholipid scramblase-mediated phosphatidylserine exposure. Exp Hematol 30: 394-402, 2002.
27. Kempe DS, Akel A, Lang PA, Hermle T, Biswas R, Muresanu J, Friedrich B, Dreischer P, Wolz C, Schumacher U, Peschel A, Gotz F, Doring G, Wieder T, Gulbins E, Lang F. Suicidal erythrocyte death in sepsis. J Mol Med 85: 273-281, 2007.
28. 1-Adrenergic receptor-mediated increase in the mass of phosphatidic acid and 1,2-diacylglycerol in ischemic rat heart. Cardiovasc Res 42: 48-56, 1999.
29. Kurz T, Wolf RA, Corr PB. Phosphatidic acid stimulates inositol 1,4,5-trisphosphate production in adult cardiac myocytes. Circ Res 72: 701-706, 1993.
30. Kuypers FA, Larkin SK, Emeis JJ, Allison AC. Interaction of an annexin V homodimer (diannexin) with phosphatidylserine on cell surfaces and consequent antithrombotic activity. Thromb Haemost 97: 478-486, 2007.
31. Lang PA, Kempe DS, Tanneur V, Eisele K, Klarl BA, Myssina S, Jendrossek V, Ishii S, Shimizu T, Waidmann M, Hessler G, Huber SM, Lang F, Wieder T. Stimulation of erythrocyte ceramide formation by platelet-activating factor. J Cell Sci 118: 1233-1243, 2005.
32. Lehman N, Di Fulvio M, McCray N, Campos I, Tabatabaian F, Gomez-Cambronero J. Phagocyte cell migration is mediated by phospholipases PLD1 and PLD2. Blood 108: 3564-3572, 2006.
33. Lew VL, Daw N, Etzion Z, Tiffert T, Muoma A, Vanagas L, Bookchin RM. Effects of age-dependent membrane transport changes on the homeostasis of senescent human red blood cells. Blood 110: 1334-1342, 2007.
34. Lindner A, Hinds TR, Joly A, Schreiner GF. Neutral lipid from proteinuric rat urine is a novel inhibitor of the red blood cell calcium pump. J Am Soc Nephrol 10: 1170-1178, 1999.
35. Manodori AB, Kuypers FA. Altered red cell turnover in diabetic mice. J Lab Clin Med 140: 161-165, 2002.
36. Minetti M, Agati L, Malorni W. The microenvironment can shift erythrocytes from a friendly to a harmful behavior: pathogenetic implications for vascular diseases. Cardiovasc Res 75: 21-28, 2007.
37. Moolenaar WH, Kruijer W, Tilly BC, Verlaan I, Bierman AJ, de Laat SW. Growth factor-like action of phosphatidic acid. Nature 323: 171-173, 1986.
38. Neidlinger NA, Larkin SK, Bhagat A, Victorino GP, Kuypers FA. Hydrolysis of phosphatidylserine-exposing red blood cells by secretory phospholipase A2 generates lysophosphatidic acid and results in vascular dysfunction. J Biol Chem 281: 775-781, 2006.
39. Nishikimi A, Fukuhara H, Su W, Hongu T, Takasuga S, Mihara H, Cao Q, Sanematsu F, Kanai M, Hasegawa H, Tanaka Y, Shibasaki M, Kanaho Y, Sasaki T, Frohman MA, Fukui Y. Sequential regulation of DOCK2 dynamics by two phospholipids during neutrophil chemotaxis. Science 324: 384-387, 2009.
40. Ochi S, Hashimoto K, Nagahama M, Sakurai J. Phospholipid metabolism induced by Clostridium perfringens α-toxin elicits a hot-cold type of hemolysis in rabbit erythrocytes. Infect Immun 64: 3930-3933, 1996. (Pubitemid 26298729)
41. Parmentier JH, Pavicevic Z, Malik KU. ANG II stimulates phospholipase D through PKC-ζ activation in VSMC: implications in adhesion, spreading, and hypertrophy. Am J Physiol Heart Circ Physiol 290: H46-H54, 2006.
42. Parry MJ, Alakoskela JM, Khandelia H, Kumar SA, Jaattela M, Mahalka AK, Kinnunen PK. High-affinity small molecule-phospholipid complex formation: binding of siramesine to phosphatidic acid. J Am Chem Soc 130: 12953-12960, 2008.
43. Peyrou V, Lormeau JC, Herault JP, Gaich C, Pfliegger AM, Herbert JM. Contribution of erythrocytes to thrombin generation in whole blood. Thromb Haemost 81: 400-406, 1999.
44. Piagnerelli M, Boudjeltia KZ, Vanhaeverbeek M, Vincent JL. Red blood cell rheology in sepsis. Intensive Care Med 29: 1052-1061, 2003.
45. Rice GC, Brown PA, Nelson RJ, Bianco JA, Singer JW, Bursten S. Protection from endotoxic shock in mice by pharmacologic inhibition of phosphatidic acid. Proc Natl Acad Sci USA 91: 3857-3861, 1994.
46. 2+ pump ATPase of intact red blood cells. Free Radic Biol Med 18: 655-667, 1995.
47. Schmidt A, Wolde M, Thiele C, Fest W, Kratzin H, Podtelejnikov AV, Witke W, Huttner WB, Soling HD. Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature 401: 133-141, 1999.
48. Setty BN, Betal SG. Microvascular endothelial cells express a phosphatidylserine receptor: a functionally active receptor for phosphatidylserinepositive erythrocytes. Blood 111: 905-914, 2008.
49. Shi J, Pipe SW, Rasmussen JT, Heegaard CW, Gilbert GE. Lactadherin blocks thrombosis and hemostasis in vivo: correlation with platelet phosphatidylserine exposure. J Thromb Haemost 6: 1167-1174, 2008.
50. Sola E, Vaya A, Martinez M, Moscardo A, Corella D, Santaolaria ML, Espana F, Hernandez-Mijares A. Erythrocyte membrane phosphatidylserine exposure in obesity. Obesity (Silver Spring) 17: 318-322, 2009.
51. Sozzani S, Agwu DE, McCall CE, O'Flaherty JT, Schmitt JD, Kent JD, McPhail LC. Propranolol, a phosphatidate phosphohydrolase inhibitor, also inhibits protein kinase C. J Biol Chem 267: 20481-20488, 1992.
52. Tou JS, Gill JS. Lysophosphatidic acid increases phosphatidic acid formation, phospholipase D activity and degranulation by human neutrophils. Cell Signal 17: 77-82, 2005.
53. 3 integrin receptor activation and P-selectin expression during platelet recruitment: down-regulation by aspirin ex vivo. Blood 99: 3978-3984, 2002.
54. Wang KK, Villalobo A, Roufogalis BD. The plasma membrane calcium pump: a multiregulated transporter. Trends Cell Biol 2: 46-52, 1992.
55. Wang X, Devaiah SP, Zhang W, Welti R. Signaling functions of phosphatidic acid. Prog Lipid Res 45: 250-278, 2006.
56. Wang Y, Oram JF. Unsaturated fatty acids phosphorylate and destabilize ABCA1 through a phospholipase D2 pathway. J Biol Chem 280: 35896-35903, 2005.
57. 2+ and cardiac contractile force. Am J Physiol Heart Circ Physiol 271: H651-H659, 1996.
58. Yang Z, Asico LD, Yu P, Wang Z, Jones JE, Bai RK, Sibley DR, Felder RA, Jose PA. D5 dopamine receptor regulation of phospholipase D. Am J Physiol Heart Circ Physiol 288: H55-H61, 2005.
59. Zwaal RF, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 62: 971-988, 2005.