Sphingosine kinase 1 (Sphk1) negatively regulates platelet activation and thrombus formation

American Journal of Physiology - Cell Physiology

Volumn 307, Issue 10, 2014, Pages C920-C927

  Münzer, Patrick ^a   Schmid, Evi ^a   Walker, Britta ^a   Fotinos, Anna ^a   Chatterjee, Madhumita ^a   Rath, Dominik ^a   Vogel, Sebastian ^a   Hoffmann, Sascha M ^b   Metzger, Katja ^a   Seizer, Peter ^a   Geisler, Tobias ^a   Gawaz, Meinrad ^a   Borst, Oliver ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Platelet activation; Sphingosine kinase 1; Thrombus formation; Ca2+ i

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; COLLAGEN RELATED PEPTIDE; FIBRINOGEN; FURA 2; PEPTIDE; SPHINGOSINE KINASE 1; THROMBIN; UNCLASSIFIED DRUG; PHOSPHOTRANSFERASE; SPHINGOSINE KINASE;

ANIMAL CELL; ARTICLE; BLEEDING TIME; BLOOD CELL COUNT; BLOOD CLOTTING; CALCIUM CELL LEVEL; CONTROLLED STUDY; ENZYME REGULATION; FLOW CYTOMETRY; HEMATOLOGICAL PARAMETERS; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHEAR RATE; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBUS; ANIMAL; C57BL MOUSE; ENZYMOLOGY; FEMALE; KNOCKOUT MOUSE; MALE; PATHOLOGY; PHYSIOLOGY; THROMBOSIS;

MUS;

ANIMALS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PLATELET ACTIVATION; THROMBOSIS;

EID: 84922479936     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00029.2014     Document Type: Article

References (55)

1. Adam F, Kauskot A, Rosa JP, Bryckaert M. Mitogen-activated protein kinases in hemostasis and thrombosis. J Thromb Haemost 6: 2007-2016, 2008.
2. Allende ML, Sasaki T, Kawai H, Olivera A, Mi Y, van Echten-Deckert G, Hajdu R, Rosenbach M, Keohane CA, Mandala S, Spiegel S, Proia RL. Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J Biol Chem 279: 52487-52492, 2004.
3. Altmann C, Meyer Zu Heringdorf D, Boyukbas D, Haude M., Jakobs KH, Michel MC Sphingosylphosphorylcholine, a naturally occurring lipid mediator, inhibits human platelet function. Br J Pharmacol 138: 435-444, 2003.
4. Aslan JE, Baker SM, Loren CP, Haley KM, Itakura A, Pang J, Greenberg DL, David LL, Manser E, Chernoff J, McCarty OJ. The PAK system links Rho GTPase signaling to thrombin-mediated platelet activation. Am J Physiol Cell Physiol 305: C519-C528, 2013.
5. Banno Y, Kato M, Hara A, Nozawa Y. Evidence for the presence of multiple forms of Sph kinase in human platelets. Biochem J 335: 301-304, 1998.
6. Blom T, Bergelin N, Slotte JP, Tornquist K. Sphingosine kinase regulates voltage operated calcium channels in GH4C1 rat pituitary cells. Cell Signal 18: 1366-1375, 2006.
7. Borst O, Munzer P, Gatidis S, Schmidt EM, Schonberger T, Schmid E, Towhid ST, Stellos K, Seizer P, May AE, Lang F, Gawaz M. The inflammatory chemokine CXC motif ligand 16 triggers platelet activation and adhesion via CXC motif receptor 6-dependent phosphatidylinositide 3-kinase/Akt signaling. Circ Res 111: 1297-1307, 2012.
8. 2+signaling and thrombus formation in klothodeficient mice. FASEB J 28: 2108-2119, 2014.
9. Borst O, Schmidt EM, Munzer P, Schonberger T, Towhid ST, Elvers M, Leibrock C, Schmid E, Eylenstein A, Kuhl D, May AE, Gawaz M, Lang F. The serum- and glucocorticoid-inducible kinase 1 (SGK1) influences platelet calcium signaling and function by regulation of Orai1 expression in megakaryocytes. Blood 119: 251-261, 2012.
10. Borst O, Walker B, Munzer P, Russo A, Schmid E, Faggio C, Bigalke B, Laufer S, Gawaz M, Lang F. Skepinone-L, a novel potent and highly selective inhibitor of p38 MAP kinase, effectively impairs platelet activation and thrombus formation. Cell Physiol Biochem 31: 914-924, 2013.
11. Carr JM, Mahalingam S, Bonder CS, Pitson SM. Sphingosine kinase 1 in viral infections. Rev Med Virol 23: 73-84, 2013.
12. Di A, Kawamura T, Gao XP, Tang H, Berdyshev E, Vogel SM, Zhao YY, Sharma T, Bachmaier K, Xu J, Malik AB. A novel function of sphingosine kinase 1 suppression of JNK activity in preventing inflammation and injury. J Biol Chem 285: 15848-15857, 2010.
13. 3signals lead cofilin to accelerate platelet actin dynamics. Am J Physiol Cell Physiol 289: C819-C825, 2005.
14. Furuya H, Wada M, Shimizu Y, Yamada PM, Hannun YA, Obeid LM, Kawamori T. Effect of sphingosine kinase 1 inhibition on blood pressure. FASEB J 27: 656-664, 2013.
15. Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest 115: 3378-3384, 2005.
16. Goni FM, Alonso A. Membrane fusion induced by phospholipase C and sphingomyelinases. Biosci Rep 20: 443-463, 2000.
17. Heemskerk JW, Bevers EM, Lindhout T. Platelet activation and blood coagulation. Thromb Haemost 88: 186-193, 2002.
18. Heffernan-Stroud LA, Obeid LM. Sphingosine kinase 1 in cancer. Adv Cancer Res 117: 201-235, 2013.
19. Hla T, Galvani S, Rafii S, Nachman R. S1P and the birth of platelets. J Exp Med 209: 2137-2140, 2012.
20. Holopainen JM, Angelova MI, Kinnunen PK. Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys J 78: 830-838, 2000.
21. Hopson KP, Truelove J, Chun J, Wang Y, Waeber C. S1P activates store-operated calcium entry via receptor- and nonreceptor-mediated pathways in vascular smooth muscle cells. Am J Physiol Cell Physiol 300: C919-C926, 2011.
22. Jain S, Harris J, Ware J. Platelets: linking hemostasis and cancer. Arterioscler Thromb Vasc Biol 30: 2362-2367, 2010.
23. Jiang P, Smith AD, Li R, Rao JN, Liu L, Donahue JM, Wang JY, Turner DJ. Sphingosine kinase 1 overexpression stimulates intestinal epithelial cell proliferation through increased c-Myc translation. Am J Physiol Cell Physiol 304: C1187-C1197, 2013.
24. Jin S, Zhou F, Katirai F, Li PL. Lipid raft redox signaling: molecular mechanisms in health and disease. Antioxid Redox Signal 15: 1043-1083, 2011.
25. Karliner JS. Sphingosine kinase and sphingosine 1-phosphate in the heart: a decade of progress. Biochim Biophys Acta 1831: 203-212, 2013.
26. Lang F, Gawaz M, Borst O. The serum- & glucocorticoid-inducible kinase in the regulation of platelet function. Acta Physiol (Oxf) 2014 Jun 19 [Epub ahead of print].
27. 2+signalling in platelets. Thromb Haemost 110: 925-930, 2013.
28. Lang PA, Contaldo C, Georgiev P, El Badry AM, Recher M, Kurrer M, Cervantes-Barragan L, Ludewig B, Calzascia T, Bolinger B, Merkler D, Odermatt B, Bader M, Graf R, Clavien PA, Hegazy AN, Lohning M, Harris NL, Ohashi PS, Hengartner H, Zinkernagel RM, Lang KS. Aggravation of viral hepatitis by platelet-derived serotonin. Nat Med 14: 756-761, 2008.
29. 2+mobilization in RBL-2H3 cells: role of I(1,4,5)P3 and S1P and necessity of I(1,4,5)P3 production. Cell Calcium 38: 581-592, 2005.
30. Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol 30: 2341-2349, 2010.
31. 2+signals triggered by different phospholipid pathways in antigen stimulation of human mast cells. J Biol Chem 277: 17255-17262, 2002.
32. Mihai R, Lai T, Schofield G, Farndon JR. C2-Ceramide increases cytoplasmic calcium concentrations in human parathyroid cells. Biochem Biophys Res Commun 268: 636-641, 2000.
33. Munzer P, Borst O, Walker B, Schmid E, Feijge MA, Cosemans JM, Chatterjee M, Schmidt EM, Schmidt S, Towhid ST, Leibrock C, Elvers M, Schaller M, Seizer P, Ferlinz K, May AE, Gulbins E, Heemskerk JW, Gawaz M, Lang F. Acid sphingomyelinase regulates platelet cell membrane scrambling, secretion, and thrombus formation. Arterioscler Thromb Vasc Biol 34: 61-71, 2014.
34. Neubauer HA, Pitson SM. Roles, regulation and inhibitors of sphingosine kinase 2. FEBS J 280: 5317-5336, 2013.
35. Nugent D, Xu Y. Sphingosine-1-phosphate: characterization of its inhibition of platelet aggregation. Platelets 11: 226-232, 2000.
36. Ono Y, Kurano M, Ohkawa R, Yokota H, Igarashi K, Aoki J, Tozuka M, Yatomi Y. Sphingosine 1-phosphate release from platelets during clot formation: close correlation between platelet count and serum sphingosine 1-phosphate concentration. Lipids Health Dis 12: 20, 2013.
37. Orr Gandy KA, Obeid LM. Targeting the sphingosine kinase/sphingosine 1-phosphate pathway in disease: review of sphingosine kinase inhibitors. Biochim Biophys Acta 1831: 157-166, 2013.
38. Randriamboavonjy V, Badenhoop K, Schmidt H, Geisslinger G, Fisslthaler B, Fleming I. The S1P(2) receptor expressed in human platelets is linked to the RhoA-Rho kinase pathway and is down regulated in type 2 diabetes. Basic Res Cardiol 104: 333-340, 2009.
39. Rauch BH. Sphingosine 1-phosphate as a link between blood coagulation and inflammation. Cell Physiol Biochem 34: 185-196, 2014.
40. Ruggeri ZM. Platelets in atherothrombosis. Nat Med 8: 1227-1234, 2002.
41. 2+and permeability response to platelet-activating factor is mediated by acid sphingomyelinase and transient receptor potential classical 6. Am J Respir Crit Care Med 185: 160-170, 2012.
42. Schoenwaelder SM, Yuan Y, Josefsson EC, White MJ, Yao Y, Mason KD, O'Reilly LA, Henley KJ, Ono A, Hsiao S, Willcox A, Roberts AW, Huang DC, Salem HH, Kile BT, Jackson SP. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 114: 663-666, 2009.
43. Schwalm S, Pfeilschifter J, Huwiler A. Sphingosine-1-phosphate: a Janus-faced mediator of fibrotic diseases. Biochim Biophys Acta 1831: 239-250, 2013.
44. Shu X, Wu W, Mosteller RD, Broek D. Sphingosine kinase mediates vascular endothelial growth factor-induced activation of ras and mitogenactivated protein kinases. Mol Cell Biol 22: 7758-7768, 2002.
45. Siow D, Wattenberg B. The compartmentalization and translocation of the sphingosine kinases: mechanisms and functions in cell signaling and sphingolipid metabolism. Crit Rev Biochem Mol Biol 46: 365-375, 2011.
46. Tani M, Sano T, Ito M, Igarashi Y. Mechanisms of sphingosine and sphingosine 1-phosphate generation in human platelets. J Lipid Res 46: 2458-2467, 2005.
47. Totani L, Evangelista V. Platelet-leukocyte interactions in cardiovascular disease and beyond. Arterioscler Thromb Vasc Biol 30: 2357-2361, 2010.
48. Ulrych T, Bohm A, Polzin A, Daum G, Nusing RM, Geisslinger G, Hohlfeld T, Schror K, Rauch BH. Release of sphingosine-1-phosphate from human platelets is dependent on thromboxane formation. J Thromb Haemost 9: 790-798, 2011.
49. Watanabe N, Nakajima H, Suzuki H, Oda A, Matsubara Y, Moroi M, Terauchi Y, Kadowaki T, Suzuki H, Koyasu S, Ikeda Y, Handa M. Functional phenotype of phosphoinositide 3-kinase p85alpha-null platelets characterized by an impaired response to GP VI stimulation. Blood 102: 541-548, 2003.
50. Woulfe D, Jiang H, Morgans A, Monks R, Birnbaum M, Brass LF. Defects in secretion, aggregation, and thrombus formation in platelets from mice lacking Akt2. J Clin Invest 113: 441-450, 2004.
51. Xu Y, Zhu K, Hong G, Wu W, Baudhuin LM, Xiao Y, Damron DS. Sphingosylphosphorylcholine is a ligand for ovarian cancer G-proteincoupled receptor 1. Nat Cell Biol 2: 261-267, 2000.
52. Yatomi Y, Igarashi Y, Yang L, Hisano N, Qi R, Asazuma N, Satoh K, Ozaki Y, Kume S. Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J Biochem 121: 969-973, 1997.
53. Yatomi Y, Ruan F, Hakomori S, Igarashi Y. Sphingosine-1-phosphate: a platelet-activating sphingolipid released from agonist-stimulated human platelets. Blood 86: 193-202, 1995.
54. Zhang L, Orban M, Lorenz M, Barocke V, Braun D, Urtz N, Schulz C, von Bruhl ML, Tirniceriu A, Gaertner F, Proia RL, Graf T, Bolz SS, Montanez E, Prinz M, Muller A, von Baumgarten L, Billich A, Sixt M, Fassler R, von Andrian UH, Junt T, Massberg S. A novel role of sphingosine 1-phosphate receptor S1pr1 in mouse thrombopoiesis. J Exp Med 209: 2165-2181, 2012.
55. Zhang L, Urtz N, Gaertner F, Legate KR, Petzold T, Lorenz M, Mazharian A, Watson SP, Massberg S. Sphingosine kinase 2 (Sphk2) regulates platelet biogenesis by providing intracellular sphingosine 1-phosphate (S1P). Blood 122: 791-802, 2013.