Sphingosine 1-phosphate is a ligand for peroxisome proliferator-activated receptor-γ that regulates neoangiogenesis

FASEB Journal

Volumn 29, Issue 9, 2015, Pages 3638-3653

  Parham, Kate A ^a,b,c   Zebol, Julia R ^a   Tooley, Katie L ^a,c   Sun, Wai Y ^a,b,c   Moldenhauer, Lachlan M ^a,c   Cockshell, Michaelia P ^a,c   Gliddon, Briony L ^a   Moretti, Paul A ^a   Tigyi, Gabor ^d   Pitson, Stuart M ^a,c   Bonder, Claudine S ^a,b,c  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c Department of Civil and Environmental Engineering   (Australia)

^d UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Endothelial; Neovascularization; Transcription factor

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; CD36 ANTIGEN; FATTY ACID BINDING PROTEIN 2; LUCIFERASE; MATRIGEL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PLASMINOGEN ACTIVATOR INHIBITOR 1; SPHINGOSINE 1 PHOSPHATE; CARRIER PROTEIN; LYSOPHOSPHOLIPID; PHOSPHOTRANSFERASE; PPARGC1A PROTEIN, MOUSE; PPARGC1B PROTEIN, HUMAN; PROTEASE NEXIN I; SERPINE1 PROTEIN, HUMAN; SERPINE2 PROTEIN, MOUSE; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1-PHOSPHATE; SPHINGOSINE KINASE; SPHINGOSINE KINASE 2, HUMAN; TRANSCRIPTION FACTOR;

ANGIOGENESIS; ARTICLE; BINDING ASSAY; COMPLEX FORMATION; COMPUTER MODEL; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; LIGAND BINDING; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; ANALOGS AND DERIVATIVES; ANIMAL; CYTOLOGY; GENETICS; HEK293 CELL LINE; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHYSIOLOGY; U937 CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; ANTIGENS, CD36; CARRIER PROTEINS; HEK293 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LYSOPHOSPHOLIPIDS; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PLASMINOGEN ACTIVATOR INHIBITOR 1; PPAR GAMMA; RECEPTORS, LYSOSPHINGOLIPID; SERPIN E2; SPHINGOSINE; TRANSCRIPTION FACTORS; U937 CELLS;

EID: 84942859158     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-261289     Document Type: Article

References (91)

1. Pitson, S. M. (2011) Regulation of sphingosine kinase and sphingolipid signaling. Trends Biochem. Sci. 36, 97-107
2. Yatomi, Y., Igarashi, Y., Yang, L., Hisano, N., Qi, R., Asazuma, N., Satoh, K., Ozaki, Y., and Kume, S. (1997) Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J. Biochem. 121, 969-973
3. García-Pacios, M., Collado, M. I., Busto, J. V., Sot, J., Alonso, A., Arrondo, J. L., and Goñi, F. M. (2009) Sphingosine-1-phosphate as an amphipathic metabolite: its properties in aqueous and membrane environments. Biophys. J. 97, 1398-1407
4. Hla, T., Venkataraman, K., and Michaud, J. (2008) The vascular S1P gradient-cellular sources and biological significance. Biochim. Biophys. Acta 1781, 477-482
5. Lin, C. I., and Chen, C. N., Lin, P. W., and Lee, H. (2007) Sphingosine 1-phosphate regulates inflammation-related genes in human endothelial cells through S1P1 and S1P3. Biochem. Biophys. Res. Commun. 355, 895-901
6. Bonder, C. S., and Sun, W. Y., Matthews, T., Cassano, C., Li, X., and Ramshaw, H. S., Pitson, S. M., Lopez, A. F., Coates, P. T., Proia, R. L., Vadas, M. A., and Gamble, J. R. (2009) Sphingosine kinase regulates the rate of endothelial progenitor cell differentiation. Blood 113, 2108-2117
7. Gamble, J. R., and Sun, W. Y., Li, X., Hahn, C. N., Pitson, S. M., Vadas, M. A., and Bonder, C. S. (2009) Sphingosine kinase-1 associates with integrin αVβ3 to mediate endothelial cell survival. Am. J. Pathol. 175, 2217-2225
8. Schwalm, S., Döll, F., Römer, I., Bubnova, S., Pfeilschifter, J., and Huwiler, A. (2008) Sphingosine kinase-1 is a hypoxia-regulated gene that stimulates migration of human endothelial cells. Biochem. Biophys. Res. Commun. 368, 1020-1025
9. Yan, G., Chen, S., You, B., and Sun, J. (2008) Activation of sphingosine kinase-1 mediates induction of endothelial cell proliferation and angiogenesis by epoxyeicosatrienoic acids. Cardiovasc. Res. 78, 308-314
10. Strub, G. M., Maceyka, M., Hait, N. C., Milstien, S., and Spiegel, S. (2010) Extracellular and intracellular actions of sphingosine-1-phosphate. Adv. Exp. Med. Biol. 688, 141-155
11. Barrett, J. M., and Parham, K. A., Pippal, J. B., Cockshell, M. P., Moretti, P. A., Brice, S. L., Pitson, S. M., and Bonder, C. S. (2011) Over-expression of sphingosine kinase-1 enhances a progenitor phenotype in human endothelial cells. Microcirculation 18, 583-597
12. Sun, W. Y., and Pitson, S. M., and Bonder, C. S. (2010) Tumor necrosis factor-induced neutrophil adhesion occurs via sphingosine kinase-1-dependent activation of endothelial α5β1 integrin. Am. J. Pathol. 177, 436-446
13. Sun, W. Y., and Abeynaike, L. D., Escarbe, S., Smith, C. D., Pitson, S. M., Hickey, M. J., and Bonder, C. S. (2012) Rapid histamine-induced neutrophil recruitment is sphingosine kinase-1 dependent. Am. J. Pathol. 180, 1740-1750
14. Limaye, V., Li, X., Hahn, C., Xia, P., and Berndt, M. C., Vadas, M. A., and Gamble, J. R. (2005) 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 105, 3169-3177
15. Hait, N. C., Allegood, J., Maceyka, M., Strub, G.M., and Harikumar, K. B., Singh, S. K., Luo, C., Marmorstein, R., Kordula, T., Milstien, S., and Spiegel, S. (2009) Regulation ofhistone acetylationin the nucleus by sphingosine-1-phosphate. Science 325, 1254-1257
16. Alvarez, S.E., Harikumar, K.B., and Hait, N. C., Allegood, J., Strub, G.M., Kim, E. Y., Maceyka, M., Jiang, H., Luo, C., Kordula, T., Milstien, S., and Spiegel, S. (2010) Sphingosine-1-phosphateis amissing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465, 1084-1088
17. Strub, G. M., Paillard, M., Liang, J., Gomez, L., and Allegood, J. C., Hait, N. C., Maceyka, M., Price, M. M., Chen, Q., Simpson, D. C., Kordula, T., Milstien, S., Lesnefsky, E.J., and Spiegel, S. (2011) Sphingosine-1-phosphate produced by sphingosine kinase 2 in mitochondria interacts with prohibitin 2 to regulate complex IV assembly and respiration. FASEB J. 25, 600-612
18. Harikumar, K. B., and Yester, J. W., Surace, M. J., Oyeniran, C., Price, M. M., Huang, W. C., Hait, N. C., Allegood, J. C., Yamada, A., Kong, X., Lazear, H. M., Bhardwaj, R., Takabe, K., Diamond, M. S., Luo, C., Milstien, S., Spiegel, S., and Kordula, T. (2014) K63-linked poly-ubiquitination of transcription factor IRF1 is essential for IL-1-induced production of chemokines CXCL10 and CCL5. Nat. Immunol. 15, 231-238
19. Tontonoz, P., and Spiegelman, B. M. (2008) Fat and beyond: the diverse biology of PPARgamma. Annu. Rev. Biochem. 77, 289-312
20. Michalik, L., Auwerx, J., Berger, J. P., Chatterjee, V. K., Glass, C. K., Gonzalez, F. J., Grimaldi, P. A., Kadowaki, T., Lazar, M. A., O'Rahilly, S., Palmer, C.N., Plutzky, J., Reddy, J.K., Spiegelman, B.M., Staels, B., and Wahli, W. (2006) International Union of Pharmacology. LXI. Peroxisome proliferator-activated receptors. Pharmacol. Rev. 58, 726-741
21. Mukherjee, R., Jow, L., Croston, G. E., and Paterniti, Jr., J. R. (1997) Identification, characterization, and tissue distribution of human peroxisome proliferator-activated receptor (PPAR) isoforms PPAR-gamma2 versus PPARgamma1 and activation with retinoid X receptor agonists and antagonists. J. Biol. Chem. 272, 8071-8076
22. Werman, A., Hollenberg, A., Solanes, G., Bjorbaek, C., Vidal-Puig, A. J., and Flier, J.S.(1997) Ligand-independent activation domain in the N terminus of peroxisome proliferator-activated receptor g (PPARgamma). Differential activity of PPARgamma1 and-2isoforms and influence of insulin. J. Biol. Chem. 272, 20230-20235
23. Asami-Miyagishi, R., Iseki, S., Usui, M., Uchida, K., Kubo, H., and Morita, I. (2004) Expression and function of PPARgamma in rat placental development. Biochem. Biophys. Res. Commun. 315, 497-501
24. Medina-Gomez, G., Virtue, S., Lelliott, C., Boiani, R., Campbell, M., Christodoulides, C., Perrin, C., Jimenez-Linan, M., Blount, M., Dixon, J., Zahn, D., Thresher, R. R., Aparicio, S., Carlton, M., Colledge, W. H., Kettunen, M. I., Seppänen-Laakso, T., Sethi, J. K., O'Rahilly, S., Brindle, K., Cinti, S., Oresic, M., Burcelin, R., and Vidal-Puig, A. (2005) The link between nutritional status and insulin sensitivity is dependent on the adipocyte-specific peroxisome proliferator-activated receptor-γ2 isoform. Diabetes 54, 1706-1716
25. Asano, T., Wakisaka, M., Yoshinari, M., Iino, K., Sonoki, K., Iwase, M., and Fujishima, M.(2000) Peroxisome proliferator-activated receptor γ1 (PPARgamma1) expresses in rat mesangial cells and PPAR-gamma agonists modulate its differentiation. Biochim. Biophys. Acta 1497, 148-154
26. Norazmi, M.N., Mohamed, R., and Nurul, A. A., and Yaacob, N.S.(2012) The modulation of PPARg1 and PPARg2 mRNA expression by ciglitazone in CD3/CD28-activated naïve and memory CD4+ T cells. Clin. Dev. Immunol. 2012, 849195
27. McIntyre, T. M., and Pontsler, A. V., Silva, A. R., St Hilaire A., Xu, Y., Hinshaw, J. C., Zimmerman, G. A., Hama, K., Aoki, J., Arai, H., and Prestwich, G.D.(2003) Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARgamma agonist. Proc. Natl. Acad. Sci. USA 100, 131-136
28. Lehmann, J. M., and Moore, L. B., Smith-Oliver, T. A., Wilkison, W. O., Willson, T. M., and Kliewer, S. A. (1995) An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor g (PPAR g). J. Biol. Chem. 270, 12953-12956
29. Pistrosch, F., Herbrig, K., Oelschlaegel, U., Richter, S., Passauer, J., Fischer, S., and Gross, P. (2005) PPARgamma-agonist rosiglitazone increases number and migratory activity of cultured endothelial progenitor cells. Atherosclerosis 183, 163-167
30. Werner, C., and Kamani, C. H., Gensch, C., Böhm, M., and Laufs, U. (2007) The peroxisome proliferator-activated receptor-g agonist pioglitazone increases number and function of endothelial progenitor cells in patients with coronary artery disease and normal glucose tolerance. Diabetes 56, 2609-2615
31. Wang, C. H., Ciliberti, N., Li, S. H., Szmitko, P. E., Weisel, R. D., Fedak, P. W., Al-Omran, M., Cherng, W. J., Li, R. K., Stanford, W. L., and Verma, S. (2004) Rosiglitazone facilitates angiogenic progenitor cell differentiation toward endothelial lineage: a new paradigm in glitazone pleiotropy. Circulation 109, 1392-1400
32. Cicha, I., Urschel, K., Daniel, W. G., and Garlichs, C. D. (2011) Telmisartan prevents VCAM-1 induction and monocytic cell adhesion to endothelium exposed to non-uniform shear stress and TNF-α. Clin. Hemorheol. Microcirc. 48, 65-73
33. Jung, Y., Song, S., and Choi, C. (2008) Peroxisome proliferator activated receptor γ agonists suppress TNFalpha-induced ICAM-1 expression by endothelial cells in a manner potentially dependent on inhibition of reactive oxygen species. Immunol. Lett. 117, 63-69
34. Kawabe-Yako, R., Masaaki, I., Masuo, O., Asahara, T., and Itakura, T. (2011) Cilostazol activates function of bone marrow-derived endothelial progenitor cell for re-endothelialization in a carotid balloon injury model. PLoS One 6, e24646
35. Xin, X., Yang, S., Kowalski, J., and Gerritsen, M. E. (1999) Peroxisome proliferator-activated receptor γ ligands are potent inhibitors of angiogenesis in vitro and in vivo. J. Biol. Chem. 274, 9116-9121
36. Appleby, S.L., Cockshell, M.P., Pippal, J.B., Thompson, E.J., Barrett, J. M., Tooley, K., Sen, S., and Sun, W. Y., Grose, R., Nicholson, I., Levina, V., Cooke, I., Talbo, G., Lopez, A. F., and Bonder, C. S. (2012) Characterization of a distinct population of circulating human non-adherent endothelial forming cells and their recruitment via intercellular adhesion molecule-3. PLoS One 7, e46996
37. Litwin, M., Clark, K., Noack, L., Furze, J., Berndt, M., Albelda, S., Vadas, M., and Gamble, J. (1997) Novel cytokine-independent induction of endothelial adhesion molecules regulated by platelet/endothelial cell adhesion molecule (CD31). J. Cell Biol. 139, 219-228
38. Gurnell, M., and Wentworth, J. M., Agostini, M., Adams, M., Collingwood, T. N., Provenzano, C., Browne, P. O., Rajanayagam, O., Burris, T. P., Schwabe, J. W., Lazar, M. A., and Chatterjee, V. K. (2000) A dominant-negative peroxisome proliferator-activated receptor γ (PPARgamma) mutant is a constitutive repressor and inhibits PPARgamma-mediated adipogenesis. J. Biol. Chem. 275, 5754-5759
39. Tsukahara, T., Tsukahara, R., Yasuda, S., Makarova, N., and Valentine, W. J., Allison, P., Yuan, H., Baker, D. L., Li, Z., Bittman, R., Parrill, A., and Tigyi, G. (2006) Different residues mediate recognition of 1-O-oleyllysophosphatidic acid and rosiglitazone in the ligand binding domain of peroxisome proliferator-activated receptor γ. J. Biol. Chem. 281, 3398-3407
40. Pitson, S. M., D'andrea, R. J., Vandeleur, L., Moretti, P. A., Xia, P., Gamble, J. R., Vadas, M. A., and Wattenberg, B. W. (2000) Human sphingosine kinase: purification, molecular cloning and characterization of the native and recombinant enzymes. Biochem. J. 350, 429-441
41. Pitson, S. M., and Moretti, P. A., Zebol, J. R., Zareie, R., Derian, C. K., Darrow, A. L., Qi, J., D'Andrea, R. J., Bagley, C. J., Vadas, M. A., and Wattenberg, B. W. (2002) The nucleotide-binding site of human sphingosine kinase 1. J. Biol. Chem. 277, 49545-49553
42. Trott, O., and Olson, A. J. (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-461
43. Mizugishi, K., Yamashita, T., Olivera, A., Miller, G. F., Spiegel, S., and Proia, R. L. (2005) Essential role for sphingosine kinases in neural and vascular development. Mol. Cell. Biol. 25, 11113-11121
44. Leclercq, T. M., and Moretti, P. A., Vadas, M. A., and Pitson, S. M. (2008) Eukaryotic elongation factor 1A interacts with sphingosine kinase and directly enhances its catalytic activity. J. Biol. Chem. 283, 9606-9614
45. Lee, M. J., Van Brocklyn, J. R., Thangada, S., Liu, C. H., Hand, A. R., Menzeleev, R., Spiegel, S., and Hla, T. (1998) Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 279, 1552-1555
46. Van Brocklyn, J. R., Jackson, C. A., Pearl, D. K., Kotur, M. S., Snyder, P. J., and Prior, T. W. (2005) Sphingosine kinase-1 expression correlates with poor survival of patients with glioblastoma multiforme: roles of sphingosine kinase isoforms in growth of glioblastoma cell lines. J. Neuropathol. Exp. Neurol. 64, 695-705
47. Nolte, R. T., and Wisely, G. B., Westin, S., Cobb, J. E., Lambert, M. H., Kurokawa, R., Rosenfeld, M. G., Willson, T. M., Glass, C. K., and Milburn, M. V. (1998) Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-γ. Nature 395, 137-143
48. Tontonoz, P., Nagy, L., Alvarez, J. G., Thomazy, V. A., and Evans, R. M. (1998) PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93, 241-252
49. Rival, Y., Stennevin, A., Puech, L., Rouquette, A., Cathala, C., Lestienne, F., Dupont-Passelaigue, E., Patoiseau, J.F., Wurch, T., and Junquéro, D. (2004) Human adipocyte fatty acid-binding protein (aP2) gene promoter-driven reporter assay discriminates nonlipogenic peroxisome proliferator-activated receptor γ ligands. J. Pharmacol. Exp. Ther. 311, 467-475
50. Voyta, J. C., and Via, D. P., Butterfield, C. E., and Zetter, B. R. (1984) Identification and isolation of endothelial cells based on their increased uptake of acetylated-low density lipoprotein. J. Cell Biol. 99, 2034-2040
51. Daugherty, A., and Cornicelli, J. A., Welch, K., Sendobry, S. M., and Rateri, D. L. (1997) Scavenger receptors are present on rabbit aortic endothelial cells in vivo. Arterioscler. Thromb. Vasc. Biol. 17, 2369-2375
52. Giaginis, C., Margeli, A., and Theocharis, S. (2007) Peroxisome proliferator-activated receptor-γ ligands as investigational modulators of angiogenesis. Expert Opin. Investig. Drugs 16, 1561-1572
53. Limaye, V.(2008) The roleofsphingosine kinase and sphingosine-1-phosphate in the regulation of endothelial cell biology. Endothelium 15, 101-112
54. Hla, T. (2004) Physiological and pathological actions of sphingosine 1-phosphate. Semin. Cell Dev. Biol. 15, 513-520
55. Hannun, Y. A., and Obeid, L. M. (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9, 139-150
56. Dentelli, P., Trombetta, A., Togliatto, G., Zeoli, A., Rosso, A., Uberti, B., Orso, F., Taverna, D., Pegoraro, L., and Brizzi, M. F. (2009) Formation of STAT5/PPARgamma transcriptional complex modulates angiogenic cell bioavailability in diabetes. Arterioscler. Thromb. Vasc. Biol. 29, 114-120
57. Trombetta, A., Togliatto, G., Rosso, A., Dentelli, P., Olgasi, C., Cotogni, P., and Brizzi, M. F. (2013) Increase of palmitic acid concentration impairs endothelial progenitor cell and bone marrow-derived progenitor cell bioavailability: role of the STAT5/PPARγ transcriptional complex. Diabetes 62, 1245-1257
58. Marx, N., Bourcier, T., Sukhova, G. K., Libby, P., and Plutzky, J. (1999) PPARgamma activation in human endothelial cells increases plasminogen activator inhibitor type-1 expression: PPARgamma as a potential mediator in vascular disease. Arterioscler. Thromb. Vasc. Biol. 19, 546-551
59. Bryan, L., and Paugh, B. S., Kapitonov, D., Wilczynska, K. M., Alvarez, S. M., Singh, S. K., Milstien, S., Spiegel, S., and Kordula, T. (2008) Sphingosine-1-phosphate and interleukin-1 independently regulate plasminogen activator inhibitor-1 and urokinase-type plasminogen activator receptor expression in glioblastoma cells: implications for invasiveness. Mol. Cancer Res. 6, 1469-1477
60. Handt, S., and Jerome, W. G., Tietze, L., and Hantgan, R. R. (1996) Plasminogen activator inhibitor-1 secretion of endothelial cells increases fibrinolytic resistance of an in vitro fibrin clot: evidence for a key role of endothelial cells in thrombolytic resistance. Blood 87, 4204-4213
61. Panetti, T. S. (2002) Differential effects of sphingosine 1-phosphate and lysophosphatidic acid on endothelial cells. Biochim. Biophys. Acta 1582, 190-196
62. Christiaens, V., Van Hul, M., Lijnen, H. R., and Scroyen, I. (2012) CD36 promotes adipocytedi fferentiation and adipogenesis. Biochim. Biophys. Acta 1820, 949-956
63. Dawson, D. W., and Pearce, S. F., Zhong, R., Silverstein, R. L., Frazier, W. A., and Bouck, N. P.(1997) CD36 mediates the In vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol. 138, 707-717
64. Swerlick, R. A., and Lee, K. H., Wick, T. M., and Lawley, T. J. (1992) Human dermal microvascular endothelial but not human umbilical vein endothelial cells express CD36 in vivo and in vitro. J. Immunol. 148, 78-83
65. Fu, Y., Luo, L., Luo, N., and Garvey, W. T. (2006) Lipid metabolism mediated by adipocyte lipid binding protein (ALBP/aP2) gene expression in human THP-1 macrophages. Atherosclerosis 188, 102-111
66. Ghelfi, E., and Yu, C. W., Elmasri, H., Terwelp, M., Lee, C. G., Bhandari, V., Comhair, S. A., Erzurum, S. C., Hotamisligil, G. S., Elias, J. A., and Cataltepe, S. (2013) Fatty acid binding protein 4 regulates VEGF-induced airway angiogenesis and inflammation in a transgenic mouse model: implications for asthma. Am. J. Pathol. 182, 1425-1433
67. Liu, C., and Lin, J. D. (2011) PGC-1 coactivators in the control of energy metabolism. Acta Biochim. Biophys. Sin. (Shanghai) 43, 248-257
68. Shen, Z., Liu, C., Liu, P., Zhao, J., and Xu, W. (2014) Sphingosine 1-phosphate(S1P) promotes mitochondrial biogenesis in Hep G2 cells by activating peroxisome proliferator-activated receptor γ coactivator 1α (PGC-1α). Cell Stress Chaperones 19, 541-548
69. Guo, Y., Fan, Y., Zhang, J., Chang, L., Lin, J.D., and Chen, Y.E.(2013) Peroxisome proliferator-activated receptor γ coactivator 1β (PGC-1β) protein attenuates vascular lesion formation by inhibition of chromatin loading of minichromosome maintenance complex in smooth muscle cells. J. Biol. Chem. 288, 4625-4636
70. Rowe, G. C., Jang, C., Patten, I. S., and Arany, Z. (2011) PGC-1b regulates angiogenesis in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 301, E155-E163
71. Chawla, A., Barak, Y., Nagy, L., Liao, D., Tontonoz, P., and Evans, R. M. (2001) PPAR-γ dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat. Med. 7, 48-52
72. Boujaoude, L. C., Bradshaw-Wilder, C., Mao, C., Cohn, J., Ogretmen, B., Hannun, Y. A., and Obeid, L. M. (2001) Cystic fibrosis transmembrane regulator regulates uptake of sphingoid base phosphates and lysophosphatidic acid: modulation of cellular activity of sphingosine 1-phosphate. J. Biol. Chem. 276, 35258-35264
73. Harmon, G. S., Dumlao, D.S., Ng, D. T., Barrett, K. E., Dennis, E. A., Dong, H., and Glass, C. K. (2010) Pharmacological correction of a defect in PPAR-γ signaling ameliorates disease severity in Cftr-deficient mice. Nat. Med. 16, 313-318
74. Bektas, M., Allende, M.L., Lee, B.G., Chen, W., Amar, M.J., and Remaley, A. T., Saba, J. D., and Proia, R. L. (2010) Sphingosine 1-phosphate lyase deficiency disrupts lipid homeostasis in liver. J. Biol. Chem. 285, 10880-10889
75. Koch, A., Völzke, A., Wünsche, C., MeyerzuHeringdorf, D., Huwiler, A., and Pfeilschifter, J. (2012) Thiazolidinedione-dependent activation of sphingosine kinase 1 causes an anti-fibrotic effect in renal mesangial cells. Br. J. Pharmacol. 166, 1018-1032
76. Ruckhäberle, E., Rody, A., Engels, K., Gaetje, R., von Minckwitz, G., Schiffmann, S., Grösch, S., Geisslinger, G., Holtrich, U., Karn, T., and Kaufmann, M. (2008) Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer. Breast Cancer Res. Treat. 112, 41-52
77. Kawamori, T., Kaneshiro, T., Okumura, M., Maalouf, S., Uflacker, A., Bielawski, J., Hannun, Y. A., and Obeid, L. M. (2009) Role for sphingosine kinase 1 in colon carcinogenesis. FASEB J. 23, 405-414
78. Johnson, K. R., and Johnson, K. Y., Crellin, H. G., Ogretmen, B., Boylan, A. M., Harley, R.A., and Obeid, L. M. (2005) Immunohistochemical distribution of sphingosine kinase 1 in normal and tumor lung tissue. J. Histochem. Cytochem. 53, 1159-1166
79. Mueller, E., Sarraf, P., Tontonoz, P., Evans, R. M., Martin, K. J., Zhang, M., Fletcher, C., Singer, S., and Spiegelman, B. M. (1998) Terminal differentiation of human breast cancer through PPAR γ. Mol. Cell 1, 465-470
80. Feilchenfeldt, J., Bründler, M. A., Soravia, C., Tötsch, M., and Meier, C. A. (2004) Peroxisome proliferator-activated receptors (PPARs) and associated transcription factors in colon cancer: reduced expression of PPARgamma-coactivator 1 (PGC-1). Cancer Lett. 203, 25-33
81. Segawa, Y., Yoshimura, R., Hase, T., Nakatani, T., Wada, S., Kawahito, Y., Kishimoto, T., and Sano, H. (2002) Expression of peroxisome proliferator-activated receptor (PPAR) in human prostate cancer. Prostate 51, 108-116
82. Sarraf, P., Mueller, E., Smith, W. M., Wright, H. M., Kum, J. B., Aaltonen, L. A., de la Chapelle, A., Spiegelman, B. M., and Eng, C. (1999) Loss-of-function mutationsin PPARγ associated with human colon cancer. Mol. Cell 3, 799-804
83. Gimbrone, Jr., M. A., Leapman, S. B., Cotran, R. S., and Folkman, J. (1972) Tumor dormancy in vivo by prevention of neovascularization. J. Exp. Med. 136, 261-276
84. Lee, O. H., and Kim, Y. M., Lee, Y. M., Moon, E. J., Lee, D. J., Kim, J. H., Kim, K.W., and Kwon, Y.G.(1999) Sphingosine 1-phosphateinduces angiogenesis: its angiogenic action and signaling mechanism in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 264, 743-750
85. Oyama, O., Sugimoto, N., Qi, X., Takuwa, N., Mizugishi, K., Koizumi, J., and Takuwa, Y. (2008) The lysophospholipid mediator sphingosine-1-phosphate promotes angiogenesis in vivo in ischaemic hindlimbs of mice. Cardiovasc. Res. 78, 301-307
86. Nagahashi, M., Ramachandran, S., Kim, E. Y., Allegood, J. C., Rashid, O. M., Yamada, A., Zhao, R., Milstien, S., Zhou, H., Spiegel, S., and Takabe, K. (2012) Sphingosine-1-phosphate produced by sphingosine kinase 1 promotes breast cancer progression by stimulating angiogenesis and lymphangiogenesis. Cancer Res. 72, 726-735
87. Gealekman, O., Guseva, N., Gurav, K., Gusev, A., Hartigan, C., Thompson, M., Malkani, S., and Corvera, S. (2012) Effect of rosiglitazone on capillary density and angiogenesis in adipose tissue of normoglycaemic humans in a randomised controlled trial. Diabetologia 55, 2794-2799
88. Margeli, A., Kouraklis, G., and Theocharis, S. (2003) Peroxisome proliferator activated receptor-g(PPAR-γ)ligands and angiogenesis. Angiogenesis 6, 165-169
89. Rosen, E. D., and Spiegelman, B. M. (2001) PPARgamma: a nuclear regulator of metabolism, differentiation, and cell growth. J. Biol. Chem. 276, 37731-37734
90. Basu, S.K., Goldstein, J.L., Anderson, G.W., and Brown, M.S.(1976) Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc. Natl. Acad. Sci. USA 73, 3178-3182
91. Chang, C. L., and Hsu, H. Y., Lin, H. Y., Chiang, W., and Lee, H. (2008) Lysophosphatidic acid-induced oxidized low-density lipoprotein uptake is class A scavenger receptor-dependent in macrophages. Prostaglandins Other Lipid Mediat. 87, 20-25