Sphingosine kinase-1 enhances endothelial cell survival through a PECAM-1-dependent activation of PI-3K/Akt and regulation of Bcl-2 family members

Blood

Volumn 105, Issue 8, 2005, Pages 3169-3177

  Limaye, Vidya ^b   Li, Xiaochun ^b   Hahn, Chris ^b   Xia, Pu ^b   Berndt, Michael C ^b   Vadas, Mathew A ^b   Gamble, Jennifer R ^a  

^a INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; BISINDOLYLMALEIMIDE; CD31 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN KINASE B; SPHINGOSINE KINASE 1;

ARTICLE; CELL ADHESION; CELL INTERACTION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; UPREGULATION;

EID: 17044371645     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-02-0452     Document Type: Article

References (66)

1. Meredith JE Jr, Fazeli B, Schwartz MA. The extracellular matrix as a cell survival factor. Mol Biol Cell. 1993;4:953-961.
2. Ruoslahti E. Fibronectin and its integrin receptors in cancer. Adv Cancer Res. 1999;76:1-20.
3. Newman PJ. Switched at birth: a new family for PECAM-1. J Clin Invest. 1999;103:5-9.
4. Mamdouh Z, Chen X, Pierini LM, et al. Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis. Nature. 2003;421:748-753.
5. Noble KE, Wickremasinghe RG, De Cornet C, et al. Monocytes stimulate expression of the Bcl-2 family member, A1, in endothelial cells and confer protection against apoptosis. J Immunol. 1999;162:1376-1383.
6. Bird IN, Taylor V, Newton JP, et al. Homophilic PECAM-1(CD31) interactions prevent endothelial cell apoptosis but do not support cell spreading or migration. J Cell Sci. 1999;112:1989-1997.
7. Evans PC, Taylor ER, Kilshaw PJ. Signalling through CD31 protects endothelial cells from apoptosis. Transplantation. 2001;71:457-460.
8. Gao C, Sun W, Christofidou-Solomidou M, et al. PECAM-1 functions as aspecific and potent inhibitor of mitochondrial-dependent apoptosis. Blood. 2003;102:169-179.
9. Ferrera E, Belloni D, Contini P, et al. Transendothelial migration leads to protection from starvation-induced apoptosis in CD34+CD14+ circulating precursors: evidence for PECAM-1 involvement through Akt/PKB activation. Blood. 2003;101:186-193.
10. Carmeliet P, Lampugnani MG, Moons L, et al. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF- mediated endothelial survival and angiogenesis. Cell. 1999;98:147-157.
11. Gerber HP, Dixit V, Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J Biol Chem. 1998;273:13313-13316.
12. Nor JE, Christensen J, Mooney DJ, Polverini PJ. Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of Bcl-2 expression. Am J Pathol. 1999;154:375-384.
13. Mesri M, Morales-Ruiz M, Ackermann EJ, et al. Suppression of vascular endothelial growth factor-mediated endothelial cell protection by survivin targeting. Am J Pathol. 2001;158:1757-1765.
14. Fujio Y, Walsh K. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem. 1999;274:16349-16354.
15. Gerber HP, McMurtrey A, Kowalski J, et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway: requirement for Flk-1/KDR activation. J Biol Chem. 1998;273:30336-30343.
16. Karsan A, Yee E, Poirier GG, et al. Fibroblast growth factor-2 inhibits endothelial cell apoptosis by Bcl-2-dependent and independent mechanisms. Am J Pathol. 1997;151:1775-1784.
17. Kwon YG, Min JK, Kim KM, et al. Sphingosine 1-phosphate protects human umbilical vein endothelial cells from serum-deprived apoptosis by nitric oxide production. J Biol Chem. 2001;276: 10627-10633.
18. Hisano A, Yatomi Y, Satoh K, et al. Induction and suppression of endothejial cell apoptosis by sphingolipids: a possible in vitro model for cell-cell interactions between platelets and endothelial cells. Blood. 1999;93:4293-4299.
19. Panetti TS. Differential effects of sphingosine 1 -phosphate and lysophosphatidic acid on endothelial cells. Biochim Biophys Acta. 2002;1582:190-196.
20. Nofer J-R, Levkau B, Wolinska I, et al. Suppression of endothelial cell apoptosis by high density lipoproteins (HDL) and HDL-associated lysosphingolipids. J Biol Chem. 2001;276:34480-34485.
21. Yatomi Y, Ohmori T, Rile G, et al. Sphingosine-1-phosphate as a major bioactive lysophospholipid that is released from platelets and interacts with endothelial cells. Blood. 2000;96:3431-3438.
22. Spiegel S, Milstien S. Sphingolipid metabolites: members of a new class of lipid second messengers. J Membr Biol. 1995;146:225-237.
23. Spiegel S. Sphingosine 1-phosphate: a prototype of a new class of second messengers. J Leukoc Biol. 1999;65:341-344.
24. Spiegel S, Milstien S. Sphingosine-1-phosphate: signalling inside and out. FEBS Lett. 2000;476:55-57.
25. i-coupled receptor Edg-1 and intracellular to regulate proliferation and survival. J Cell Biol. 1998;142:229-240.
26. Pyne S, Pyne NJ. Sphingosine-1-phosphate signalling in mammalian cells. Biochem J. 2000;349:385-402.
27. Spiegel S, Milstien S. Sphingosine-1-phosphate, a key cell signalling molecule. J Biol Chem. 2002; 277:25851-25854.
28. Cuvillier O, Pirianov G, Kleuser B, et al. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature. 1996;381:800-803.
29. Edsall LC, Pirianov GG, Spiegel S. Involvement of sphingosine-1-phosphate in nerve growth factor-mediated neuronal survival and differentiation. J Neurosci. 1997;17:6952-6960.
30. Olivera A, Spiegel S. Sphingosine kinase: a mediator of vital cellular functions. Prostaglandins Other Lipid Mediat. 2001;64:123-134.
31. Xia P, Gamble JR, Wang L, et al. An oncogenic role of sphingosine kinase. Curr Biol. 2000;10:1527-1530.
32. Lee MJ, Van Brooklyn JR, Thangada S, et al. Sphingosine-1-phosphate as a ligand for the G-protein coupled receptor EDG-1. Science. 1998;279:1552-1555.
33. Lee MJ, Thangada S, Claffey KP, et al. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell. 1999;99:301-312.
34. 1-containing integrins. J Biol Chem. 2001;276:11830-11837.
35. Wang F, Van Brooklyn JR, Hobson JP, et al. Sphingosine 1-phosphate stimulates cell migration through a G(i)-coupled cell surface receptor: potential involvement in angiogenesis. J Biol Chem. 1999;274:35343-35350.
36. Kimura T, Watanabe T, Sato K, et al. Sphingosine 1-phosphate stimulates proliferation and migration of human endothelial cells possibly through the lipid receptors, Edg-1 and Edg-3. Biochem J. 2000;348:71-76.
37. Morales-Ruiz M, Lee MJ, Zollner S, et al. Sphingosine 1-phosphate activates Akt, nitric oxide production, and chemotaxis through a Gi protein/phosphoinositide 3-kinase pathway in endothelial cells. J Biol Chem. 2001;276:19672-19677.
38. Lee MJ, Thangada S, Paik JH, et al. Akt-mediated phosphorylation of the G protein-coupled receptor EDG-1 is required for endothelial cell chemotaxis. Mol Cell. 2001;8:693-704.
39. Liu Y, Wada R, Yamashita T, et al. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J Clin Invest. 2000;106:951-961.
40. Xia P, Gamble JR, Rye KA, et al. Tumor necrosis factor-alpha induces adhesion molecule expression through the sphingosine kinase pathway. Proc Natl Acad Sci U S A. 1998;95:14196-14201.
41. Xia P, Wang L, Gamble JR, Vadas MA. Activation of sphingosine kinase by tumor necrosis factor-alpha inhibits apoptosis in human endothelial cells. J Biol Chem. 1999;274:34499-34505.
42. Shiojima I, Walsh K. Role of Akt signalling in vascular homeostasis and angiogenesis. Circ Res. 2002;90:1243-1250.
43. Igarashi J, Bernier SG, Michel T. Sphingosine 1-phosphate and activation of endothelial nitric-oxide synthase: differential regulation of akt and map kinase pathways by edg and bradykinin receptors in vascular endothelial cells. J Biol Chem. 2001;276:12420-12426.
44. An S, Zheng Y, Bleu T. Sphingosine 1-phosphate-induced cell proliferation, survival, and related signalling events mediated by G protein-coupled receptors Edg3 and Edg5. J Biol Chem. 2000;275:288-296.
45. Cramer EM, Berger G, Berndt MC. Platelet α-granule and plasma membrane share two components: CD9 and PECAM-1. Blood. 1994;84:1722-1730.
46. Qbiogene Version 1.4 AdEasy Vector system manual. Carlsbad, CA.
47. Litwin M, Clark K, Noack L, et al. Novel cytokine-independent induction of endothelial adhesion molecules regulated by platelet/endothelial cell adhesion molecule (CD31). J Cell Biol. 1997;139:219-228.
48. rd, Spellberg JP, Karan-Tamir B, et al. Ligation of CD31/PECAM-1 modulates the function of lymphocytes, monocytes and neutrophils. Eur J Immunol 1998;28:1948-1958.
49. Ilan N, Mahooti S, Rimm DL, Madri JA. PECAM-1 (CD31) functions as a reservoir for and a modulator of tyrosine-phosphorylated β-catenin. J Cell Science. 1999;112:3005-3014.
50. Newman PJ, Newman DK. Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler Thromb Vasc Biol. 2003;23:953-964.
51. Muller WA, Weigl SA, Deng X, Philips DM. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med. 1993;178:449-460.
52. Papapetropoulos A, Fulton D, Mahboubi K, et al. Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/surviving pathway. J Biol Chem. 2000;275:9102-9105.
53. Gratton JP, Morales-Ruiz M, Kureishi Y, Fulton D, Walsh K, Sessa WC. Akt down-regulation of p38 signalling provides a novel mechanism of vascular endothelial growth factor-mediated cytoprotection in endothelial cells. J Biol Chem. 2001;276: 30359-30365.
54. Suhara T, Mano T, Oliveira BE, Walsh K. Phosphatidylinositol 3-kinase/Akt signalling controls endothelial cell sensitivity to Fas-mediated apoptosis via regulation of FLICE-inhibjtory protein (FLIP). Circ Res. 2001;89:13-19.
55. Hockenbery D, Nunez G, Milliman C, et al. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature. 1990;348: 334-336.
56. Strasser A, Puthalakath H, Bouillet P, et al. The role of bim, a proapoptotic BH3-only member of the Bcl-2 family in cell death control. Ann N Y Acad Sci. 2000;917:541-548.
57. Pitson SM, Moretti PAB, Zebol JR, et al. Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylafion. EMBOJ. 2003;22:5491-5500.
58. Kim DS, Kim SY, Lee JE, et al. Sphingosine-1-phosphate-induced ERK activation protects human melanocytes from UVB-induced apoptosis. Arch Pharm Res. 2003;26:739-746.
59. Grey A, Chen Q, Callon K, Xu X, Reid IR, Cornish J. The phospholipids sphingosine-1-phosphate and lysophosphatidic acid prevent apoptosis in osteoblastic cells via a signalling pathway involving G(i) proteins and phosphatidylinositol-3 kinase. Endocrinology. 2002;143:4755-4763.
60. Pellegatta F, Chierchia SL, Zocchi MR. Functional association of platelet endothelial cell adhesion molecule-1 and phosphoinositide 3-kinase in human neutrophils. J Biol Chem. 1998;273:27768-27771.
61. Esser S, Lampugnani MG, Corada M, et al. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci. 1998;111:1853-1865.
62. Ferrero E, Villa A, Ferrero ME, et al. Tumor necrosis factor α-induced vascular leakage involves PECAM1 phosphorylation. Cancer Res. 1996;56:3211-3215.
63. Lum H, Anderson TT, Siflinger-Birnboim A, et al. Thrombin receptor peptide inhibits thrombin-induced increase in endothelial permeability by receptor sensitization. J Cell Biol. 1993;120:1491-1499.
64. Gamble JR, Drew J, Trezise L, et al. Angiopoietin-1 is an anti-permeability and anti-inflammatory agent in vitro and targets cell junctions. Circ Res. 2000;87:603-607.
65. Gurubhagavatula I, Amrani Y, Pratico D, et al. Engagement of human PECAM-1 (CD31) on human endothelial cells increases intracellular calcium ion concentration and stimulates prostacyclin release. J Clin Invest. 1998;101:212-222.
66. Fukuda Y, Aoyama Y, Wada A, Igarashi Y. Identification of PECAM-1 association with sphingosine kinase 1 and its regulation by agonist-induced phosphorylation. Biochim Biophys Acta. 2004; 1636:12-21.