Sphingomyelinase-induced adhesion of eryptotic erythrocytes to endothelial cells

American Journal of Physiology - Cell Physiology

Volumn 303, Issue 9, 2012, Pages

  Abed, Majed ^a,b   Towhid, Syeda T ^a   Mia, Sobuj ^a   Pakladok, Tatsiana ^a   Alesutan, Ioana ^a   Borst, Oliver ^a   Gawaz, Meinrad ^a   Gulbins, Erich ^c   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b University of Al Furat   (Syrian Arab Republic)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Adhesion; CXCL16; Endothelium; Eryptosis; Phosphatidylserine

Indexed keywords

BACTERIAL ENZYME; CALCIUM ION; CERAMIDE; CXCL16 CHEMOKINE; GLUCOSE; IONOMYCIN; LIPOCORTIN 5; NEUTRALIZING ANTIBODY; PHOSPHATIDYLSERINE; SMALL INTERFERING RNA; SPHINGOMYELIN PHOSPHODIESTERASE;

ARTICLE; CELL ADHESION; CELL DEATH; CELL LABELING; CONTROLLED STUDY; ERYPTOSIS; ERYTHROCYTE; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; WESTERN BLOTTING;

ANNEXIN A5; ANTIBODIES, NEUTRALIZING; APOPTOSIS; CALCIUM; CALCIUM IONOPHORES; CELL ADHESION; CELL SIZE; CELLS, CULTURED; CERAMIDES; CHEMOKINES, CXC; ERYTHROCYTES; GENE SILENCING; GLUCOSE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IONOMYCIN; PHOSPHATIDYLSERINES; RECEPTORS, SCAVENGER; SPHINGOMYELIN PHOSPHODIESTERASE;

BACTERIA (MICROORGANISMS);

EID: 84868321858     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00239.2012     Document Type: Article

References (60)

1. Abel S, Hundhausen C, Mentlein R, Schulte A, Berkhout TA, Broadway N, Hartmann D, Sedlacek R, Dietrich S, Muetze B, Schuster B, Kallen KJ, Saftig P, Rose-John S, Ludwig A. The transmembrane CXC-chemokine ligand 16 is induced by IFN-gamma and TNF-alpha and shed by the activity of the disintegrin-like metalloproteinase ADAM10. J Immunol 172: 6362-6372, 2004.
2. Andrews DA, Low PS. Role of red blood cells in thrombosis. Curr Opin Hematol 6: 76-82, 1999.
3. Baranska P, Jerczynska H, Pawlowska Z, Koziolkiewicz W, Cierniewski CS. Expression of integrins and adhesive properties of human endothelial cell line EA. hy 926. Cancer Genomics Proteomics 2: 265-270, 2005.
4. Bhavsar SK, Bobbala D, Xuan NT, Foller M, Lang F. Stimulation of suicidal erythrocyte death by alpha-lipoic acid. Cell Physiol Biochem 26: 859-868, 2010.
5. Bhavsar SK, Eberhard M, Bobbala D, Lang F. Monensin induced suicidal erythrocyte death. Cell Physiol Biochem 25: 745-752, 2010.
6. Bhavsar SK, Gu S, Bobbala D, Lang F. Janus kinase 3 is expressed in erythrocytes, phosphorylated upon energy depletion and involved in the regulation of suicidal erythrocyte death. Cell Physiol Biochem 27: 547-556, 2011.
7. Bobbala D, Alesutan I, Foller M, Huber SM, Lang F. Effect of anandamide in Plasmodium Berghei-infected mice. Cell Physiol Biochem 26: 355-362, 2010.
8. Bombeli T, Schwartz BR, Harlan JM. Adhesion of activated platelets to endothelial cells: evidence for a GPIIbIIIa-dependent bridging mechanism and novel roles for endothelial intercellular adhesion molecule 1 (ICAM-1), alphavbeta3 integrin, and GPIbalpha. J Exp Med 187: 329-339, 1998.
9. 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.
10. 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.
11. Borst O, Abed M, Alesutan I, Towhid ST, Qadri SM, Foller M, Gawaz M, Lang F. Dynamic adhesion of eryptotic erythrocytes to endothelial cells via CXCL16/SR-PSOX. Am J Physiol Cell Physiol 302: C644-C651, 2012.
12. 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.
13. Closse C, Dachary-Prigent J, Boisseau MR. Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 107: 300-302, 1999.
14. Eberhard M, Ferlinz K, Alizzi K, Cacciato PM, Faggio C, Foller M, Lang F. FTY720-induced suicidal erythrocyte death. Cell Physiol Biochem 26: 761-766, 2010.
15. Felder KM, Hoelzle K, Ritzmann M, Kilchling T, Schiele D, Heinritzi K, Groebel K, Hoelzle LE. Hemotrophic mycoplasmas induce programmed cell death in red blood cells. Cell Physiol Biochem 27: 557-564, 2011.
16. Foller M, Braun M, Qadri SM, Lang E, Mahmud H, Lang F. Temperature sensitivity of suicidal erythrocyte death. Eur J Clin Invest 40: 534-540, 2010.
17. Gallagher PG, Chang SH, Rettig MP, Neely JE, Hillery CA, Smith BD, Low PS. Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 101: 4625-4627, 2003.
18. Gatidis S, Zelenak C, Fajol A, Lang E, Jilani K, Michael D, Qadri SM, Lang F. p38 MAPK activation and function following osmotic shock of erythrocytes. Cell Physiol Biochem 28: 1279-1286, 2011.
19. Ghashghaeinia M, Toulany M, Saki M, Bobbala D, Fehrenbacher B, Rupec R, Rodemann HP, Ghoreschi K, Rocken M, Schaller M, Lang F, Wieder T. The NFkB pathway inhibitors Bay 11-7082 and parthenolide induce programmed cell death in anucleated Erythrocytes. Cell Physiol Biochem 27: 45-54, 2011.
20. Gough PJ, Garton KJ, Wille PT, Rychlewski M, Dempsey PJ, Raines EW. A disintegrin and metalloproteinase 10-mediated cleavage and shedding regulates the cell surface expression of CXC chemokine ligand 16. J Immunol 172: 3678-3685, 2004.
21. Gujar SA, Marcato P, Pan D, Lee PW. Reovirus virotherapy overrides tumor antigen presentation evasion and promotes protective antitumor immunity. Mol Cancer Ther 9: 2924-2933, 2010.
22. Hara T, Katakai T, Lee JH, Nambu Y, Nakajima-Nagata N, Gonda H, Sugai M, Shimizu A. A transmembrane chemokine, CXC chemokine ligand 16, expressed by lymph node fibroblastic reticular cells has the potential to regulate T cell migration and adhesion. Int Immunol 18: 301-311, 2006.
23. Hermand P, Gane P, Huet M, Jallu V, Kaplan C, Sonneborn HH, Cartron JP, Bailly P. Red cell ICAM-4 is a novel ligand for plateletactivated alpha IIbbeta 3 integrin. J Biol Chem 278: 4892-4898, 2003.
24. Hofnagel O, Engel T, Severs NJ, Robenek H, Buers I. SR-PSOX at sites predisposed to atherosclerotic lesion formation mediates monocyte-endothelial cell adhesion. Atherosclerosis 217: 371-378, 2011.
25. Hundhausen C, Schulte A, Schulz B, Andrzejewski MG, Schwarz N, von Hundelshausen P, Winter U, Paliga K, Reiss K, Saftig P, Weber C, Ludwig A. Regulated shedding of transmembrane chemokines by the disintegrin and metalloproteinase 10 facilitates detachment of adherent leukocytes. J Immunol 178: 8064-8072, 2007.
26. 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: 269-277, 2007.
27. Lang E, Jilani K, Zelenak C, Pasham V, Bobbala D, Qadri SM, Lang F. Stimulation of suicidal erythrocyte death by benzethonium. Cell Physiol Biochem 28: 347-354, 2011.
28. Lang F, Gulbins E, Lang PA, Zappulla D, Foller M. Ceramide in suicidal death of erythrocytes. Cell Physiol Biochem 26: 21-28, 2010.
29. Lang F, Gulbins E, Lerche H, Huber SM, Kempe DS, Föller M. Eryptosis, a window to systemic disease. Cell Physiol Biochem 22: 373-380, 2008.
30. Lang KS, Myssina S, Brand V, Sandu C, Lang PA, Berchtold S, Huber SM, Lang F, Wieder T. Involvement of ceramide in hyperosmotic shockinduced death of erythrocytes. Cell Death Differ 11: 231-243, 2004.
31. Lang PA, Beringer O, Nicolay JP, Amon O, Kempe DS, Hermle T, Attanasio P, Akel A, Schafer R, Friedrich B, Risler T, Baur M, Olbricht CJ, Zimmerhackl LB, Zipfel PF, Wieder T, Lang F. Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J Mol Med 84: 378-388, 2006.
32. Lang PA, Kasinathan RS, Brand VB, Duranton C, Lang C, Koka S, Shumilina E, Kempe DS, Tanneur V, Akel A, Lang KS, Foller M, Kun JF, Kremsner PG, Wesselborg S, Laufer S, Clemen CS, Herr C, Noegel AA, Wieder T, Gulbins E, Lang F, Huber SM. Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency. Cell Physiol Biochem 24: 415-428, 2009.
33. 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.
34. Lang PA, Schenck M, Nicolay JP, Becker JU, Kempe DS, Lupescu A, Koka S, Eisele K, Klarl BA, Rubben H, Schmid KW, Mann K, Hildenbrand S, Hefter H, Huber SM, Wieder T, Erhardt A, Haussinger D, Gulbins E, Lang F. Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med 13: 164-170, 2007.
35. Lee N, Chan PK, Wong CK, Wong KT, Choi KW, Joynt GM, Lam P, Chan MC, Wong BC, Lui GC, Sin WW, Wong RY, Lam WY, Yeung AC, Leung TF, So HY, Yu AW, Sung JJ, Hui DS. Viral clearance and inflammatory response patterns in adults hospitalized for pandemic 2009 influenza A(H1N1) virus pneumonia. Antivir Ther 16: 237-247, 2011.
36. Lu Y, Cai Z, Xiao G, Keller ET, Mizokami A, Yao Z, Roodman GD, Zhang J. Monocyte chemotactic protein-1 mediates prostate cancerinduced bone resorption. Cancer Res 67: 3646-3653, 2007.
37. Manodori AB, Kuypers FA. Altered red cell turnover in diabetic mice. J Lab Clin Med 140: 161-165, 2002.
38. McCormick CJ, Craig A, Roberts D, Newbold CI, Berendt AR. Intercellular adhesion molecule-1 and CD36 synergize to mediate adherence of Plasmodium falciparum-infected erythrocytes to cultured human microvascular endothelial cells. J Clin Invest 100: 2521-2529, 1997.
39. Minami M, Kume N, Shimaoka T, Kataoka H, Hayashida K, Akiyama Y, Nagata I, Ando K, Nobuyoshi M, Hanyuu M, Komeda M, Yonehara S, Kita T. Expression of SR-PSOX, a novel cell-surface scavenger receptor for phosphatidylserine and oxidized LDL in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol 21: 1796-1800, 2001.
40. Nakayama T, Hieshima K, Izawa D, Tatsumi Y, Kanamaru A, Yoshie O. Cutting edge: profile of chemokine receptor expression on human plasma cells accounts for their efficient recruitment to target tissues. J Immunol 170: 1136-1140, 2003.
41. Nguyen DB, Wagner-Britz L, Maia S, Steffen P, Wagner C, Kaestner L, Bernhardt I. Regulation of phosphatidylserine exposure in red blood cells. Cell Physiol Biochem 28: 847-856, 2011.
42. Noh JY, Lim KM, Bae ON, Chung SM, Lee SW, Joo KM, Lee SD, Chung JH. Procoagulant and peothweombotic activation of human erythrocytes by phosphatidic acid. Am J Physiol Heart Circ Physiol 299: H347-H355, 2010.
43. Pandolfi A, Di Pietro N, Sirolli V, Giardinelli A, Di Silvestre S, Amoroso L, Di Tomo P, Capani F, Consoli A, Bonomini M. Mechanisms of uremic erythrocyte-induced adhesion of human monocytes to cultured endothelial cells. J Cell Physiol 213: 699-709, 2007.
44. Qadri SM, Bauer J, Zelenak C, Mahmud H, Kucherenko Y, Lee SH, Ferlinz K, Lang F. Sphingosine but not sphingosine-1-phosphate stimulates suicidal erythrocyte death. Cell Physiol Biochem 28: 339-346, 2011.
45. 2+-permeable cation channels triggering erythrocyte cell membrane scrambling. Cell Physiol Biochem 28: 857-864, 2011.
46. Schallhorn RA, Patel DN, Chandrasekar B, Mealey BL. Periodontal disease in association with systemic levels of interleukin-18 and CXC ligand 16 in patients undergoing cardiac catheterization. J Periodontol 81: 1180-1186, 2010.
47. Shimaoka T, Nakayama T, Fukumoto N, Kume N, Takahashi S, Yamaguchi J, Minami M, Hayashida K, Kita T, Ohsumi J, Yoshie O, Yonehara S. Cell surface-anchored SR-PSOX/CXC chemokine ligand 16 mediates firm adhesion of CXC chemokine receptor 6-expressing cells. J Leukoc Biol 75: 267-274, 2004.
48. Shimaoka T, Seino K, Kume N, Minami M, Nishime C, Suematsu M, Kita T, Taniguchi M, Matsushima K, Yonehara S. Critical role for CXC chemokine ligand 16 (SR-PSOX) in Th1 response mediated by NKT cells. J Immunol 179: 8172-8179, 2007.
49. Siraskar B, Ballal A, Bobbala D, Foller M, Lang F. Effect of amphotericin B on parasitemia and survival of plasmodium berghei-infected mice. Cell Physiol Biochem 26: 347-354, 2010.
50. Tohyama M, Sayama K, Komatsuzawa H, Hanakawa Y, Shirakata Y, Dai X, Yang L, Tokumaru S, Nagai H, Hirakawa S, Sugai M, Hashimoto K. CXCL16 is a novel mediator of the innate immunity of epidermal keratinocytes. Int Immunol 19: 1095-1102, 2007.
51. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J Immunol Methods 184: 39-51, 1995.
52. Wagsater D, Olofsson PS, Norgren L, Stenberg B, Sirsjo A. The chemokine and scavenger receptor CXCL16/SR-PSOX is expressed in human vascular smooth muscle cells and is induced by interferon gamma. Biochem Biophys Res Commun 325: 1187-1193, 2004.
53. Wandersee NJ, Olson SC, Holzhauer SL, Hoffmann RG, Barker JE, Hillery CA. Increased erythrocyte adhesion in mice and humans with hereditary spherocytosis and hereditary elliptocytosis. Blood 103: 710-716, 2004.
54. Wautier MP, El Nemer W, Gane P, Rain JD, Cartron JP, Colin Y, Le Van KC, Wautier JL. Increased adhesion to endothelial cells of erythrocytes from patients with polycythemia vera is mediated by laminin alpha5 chain and Lu/BCAM. Blood 110: 894-901, 2007.
55. Wood BL, Gibson DF, Tait JF. Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood 88: 1873-1880, 1996.
56. Yamauchi R, Tanaka M, Kume N, Minami M, Kawamoto T, Togi K, Shimaoka T, Takahashi S, Yamaguchi J, Nishina T, Kitaichi M, Komeda M, Manabe T, Yonehara S, Kita T. Upregulation of SR-PSOX/CXCL16 and recruitment of CD8+ T cells in cardiac valves during inflammatory valvular heart disease. Arterioscler Thromb Vasc Biol 24: 282-287, 2004.
57. Yang Y, Koo S, Lin CS, Neu B. Specific binding of red blood cells to endothelial cells is regulated by nonadsorbing macromolecules. J Biol Chem 285: 40489-40495, 2010.
58. Zagorski J, Sanapareddy N, Gellar MA, Kline JA, Watts JA. Transcriptional profile of right ventricular tissue during acute pulmonary embolism in rats. Physiol Genomics 34: 101-111, 2008.
59. Zappulla D. Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases? J Cardiometab Syndr 3: 30-34, 2008.
60. Zwaal RF, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 62: 971-988, 2005.