Sphingosine 1-phosphate counteracts insulin signaling in pancreatic β-cells via the sphingosine 1-phosphate receptor subtype 2

FASEB Journal

Volumn 29, Issue 8, 2015, Pages 3357-3369

  Japtok, Lukasz ^a   Schmitz, Elisabeth I ^a   Fayyaz, Susann ^a   Krämer, Stephanie ^b   Hsu, Leigh J ^c   Kleuser, Burkhard ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^c Lpath Incorporated ^*  (United States)

Author keywords

Akt signaling; Proliferation; Sphingolipids; Survival; Type 2 diabetes mellitus

Indexed keywords

4 (2,6 DICHLORO 4 PYRIDINYL) 1 (1,3 DIMETHYL 4 ISOPROPYL 1H PYRAZOLO[3,4 B]PYRIDIN 6 YL)SEMICARBAZIDE; INSULIN; PALMITIC ACID; RECEPTOR SUBTYPE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; LYSOPHOSPHOLIPID; PROTEIN KINASE B; PYRAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DAMAGE; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; HOMEOSTASIS; LIPID DIET; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; DISEASE MODEL; DRUG EFFECTS; INSULIN RESISTANCE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PROCEDURES;

ANIMALS; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; LYSOPHOSPHOLIPIDS; MALE; MICE; MICE, OBESE; PROTO-ONCOGENE PROTEINS C-AKT; PYRAZOLES; PYRIDINES; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE;

EID: 84940109434     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-263194     Document Type: Article

References (44)

1. Reaven, G. (2004) Themetabolic syndrome or the insulin resistance syndrome? Different names, different concepts, and different goals. Endocrinol. Metab. Clin. North Am. 33, 283-303
2. Virally, M., Blicklé, J. F., Girard, J., Halimi, S., Simon, D., and Guillausseau, P. J. (2007) Type 2 diabetes mellitus: epidemiology, pathophysiology, unmet needs and therapeutical perspectives. DiabetesMetab. 33, 231-244
3. Newsholme, P., Keane, D., Welters, H. J., and Morgan, N. G. (2007) Life and death decisions of the pancreatic beta-cell: the role of fatty acids. Clin. Sci. 112, 27-42
4. Kluth, O., Mirhashemi, F., Scherneck, S., Kaiser, D., Kluge, R., Neschen, S., Joost, H. G., and Schürmann, A. (2011) Dissociation of lipotoxicity and glucotoxicity in amousemodel of obesity associated diabetes: role of forkhead boxO1 (FOXO1) in glucose-induced beta cell failure. Diabetologia 54, 605-616
5. Giacca, A., Xiao, C., Oprescu, A. I., Carpentier, A. C., and Lewis, G. F. (2011) Lipid-induced pancreatic β-cell dysfunction: focus on in vivo studies. Am. J. Physiol. Endocrinol. Metab. 300, E255-E262
6. Poitout, V., Amyot, J., Semache, M., Zarrouki, B., Hagman, D., and Fontés, G. (2010) Glucolipotoxicity of the pancreatic beta cell. Biochim. Biophys. Acta 1801, 289-298
7. Sommerweiss, D., Gorski, T., Richter, S., Garten, A., and Kiess, W. (2013) Oleate rescues INS-1E β-cells from palmitate-induced apoptosis by preventing activation of the unfolded protein response. Biochem. Biophys. Res. Commun. 441, 770-776
8. Chavez, J. A., and Summers, S. A. (2012) A ceramide-centric view of insulin resistance. Cell Metab. 15, 585-594
9. Galadari, S., Rahman, A., Pallichankandy, S., Galadari, A., and Thayyullathil, F. (2013) Role of ceramide in diabetes mellitus: evidence and mechanisms. Lipids Health Dis. 12, 98
10. Maceyka, M., and Spiegel, S. (2014) Sphingolipid metabolites in inflammatory disease. Nature 510, 58-67
11. Kohama, T., Olivera, A., Edsall, L., Nagiec, M. M., Dickson, R., and Spiegel, S. (1998) Molecular cloningand functional characterization of murine sphingosine kinase. J. Biol. Chem. 273, 23722-23728
12. Liu, H., Sugiura, M., Nava, V. E., Edsall, L. C., Kono, K., Poulton, S., Milstien, S., Kohama, T., and Spiegel, S. (2000) Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J. Biol. Chem. 275, 19513-19520
13. Maceyka, M., Harikumar, K. B., Milstien, S., and Spiegel, S. (2012) Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol. 22, 50-60
14. Kihara, Y., Maceyka, M., Spiegel, S., and Chun, J. (2014) Lysophospholipid receptor nomenclature review: IUPHAR Review 8. Br. J. Pharmacol. 171, 3575-3594
15. Kowalski, G. M., Carey, A. L., Selathurai, A., Kingwell, B. A., and Bruce, C. R. (2013) Plasma sphingosine-1-phosphate is elevated in obesity. PLoS ONE 8, e72449
16. Fox, T. E., Bewley, M. C., Unrath, K. A., Pedersen, M. M., Anderson, R. E., Jung, D. Y., Jefferson, L. S., Kim, J. K., Bronson, S. K., Flanagan, J. M., and Kester, M. (2011) Circulating sphingolipid biomarkers in models of type 1 diabetes. J. Lipid Res. 52, 509-517
17. Fayyaz, S., Henkel, J., Japtok, L., Krämer, S., Damm, G., Seehofer, D., Püschel, G. P., and Kleuser, B. (2014) Involvement of sphingosine 1-phosphate in palmitate-induced insulin resistance of hepatocytes via the S1P2 receptor subtype. Diabetologia 57, 373-382
18. Mastrandrea, L. D., Sessanna, S. M., DelToro, A., and Laychock, S. G. (2010) ATP-independent glucose stimulation of sphingosine kinase in rat pancreatic islets. J. Lipid Res. 51, 2171-2180
19. Qi, Y., Chen, J., Lay, A., Don, A., Vadas, M., and Xia, P. (2013) Lossof sphingosine kinase 1 predisposes to the onset of diabetes via promoting pancreatic β-cell death in diet-induced obese mice. FASEB J. 27, 4294-4304
20. Imasawa, T., Koike, K., Ishii, I., Chun, J., and Yatomi, Y. (2010) Blockadeof sphingosine 1-phosphate receptor 2 signaling attenuates streptozotocin-induced apoptosis of pancreatic beta-cells. Biochem. Biophys. Res. Commun. 392, 207-211
21. Blot, V., Jacquemard, U., Reissig, H. U., and Kleuser, B. (2009) Practical syntheses of sphingosine-1-phosphate and analogues. Synthesis-Stuttgart 5, 759-766
22. Japtok, L., Schaper, K., Bäumer, W., Radeke, H. H., Jeong, S. K., and Kleuser, B. (2012) Sphingosine 1-phosphate modulates antigen capture by murine Langerhans cells via the S1P2 receptor subtype. PLoS ONE 7, e49427
23. Assmann, A., Ueki, K., Winnay, J. N., Kadowaki, T., and Kulkarni, R. N. (2009) Glucose effects on beta-cell growth and survival require activation of insulin receptors and insulin receptor substrate 2. Mol. Cell. Biol. 29, 3219-3228
24. Müller, D., Jones, P. M., and Persaud, S. J. (2006) Autocrine antiapoptotic and proliferative effects of insulin in pancreatic beta-cells. FEBS Lett. 580, 6977-6980
25. Andreozzi, F., D'Alessandris, C., Federici, M., Laratta, E., DelGuerra, S., Del Prato, S., Marchetti, P., Lauro, R., Perticone, F., and Sesti, G. (2004) Activation of thehexosamine pathway leads to phosphorylation of insulin receptor substrate-1 on Ser307 and Ser612 and impairs the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin insulin biosynthetic pathway in RIN pancreatic beta-cells. Endocrinology 145, 2845-2857
26. Lanuza-Masdeu, J., Arévalo, M. I., Vila, C., Barberà, A., Gomis, R., and Caelles, C. (2013) In vivo JNK activation in pancreatic β-cells leads to glucose intolerance caused by insulin resistance in pancreas. Diabetes 62, 2308-2317
27. Fayyaz, S., Japtok, L., and Kleuser, B. (2014) Divergent role of sphingosine 1-phosphate on insulin resistance. Cell. Physiol. Biochem. 34, 134-147
28. Tao, C., Sifuentes, A., and Holland, W. L. (2014) Regulation of glucose and lipid homeostas is by adiponectin: effect sonhepatocytes, pancreatic β cells and adipocytes. Best Pract. Res. Clin. Endocrinol. Metab. 28, 43-58
29. Maris, M., Robert, S., Waelkens, E., Derua, R., Hernangomez, M. H., D'Hertog, W., Cnop, M., Mathieu, C., and Overbergh, L. (2013) Role of the saturated nonesterified fatty acid palmitate in beta cell dysfunction. J. Proteome Res. 12, 347-362
30. Lee, J. Y., Sohn, K. H., Rhee, S. H., and Hwang, D. (2001) Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 276, 16683-16689
31. Boslem, E., Meikle, P. J., and Biden, T. J. (2012) Roles of ceramide and sphingolipids in pancreatic β-cell function and dysfunction. Islets 4, 177-187
32. Zhu, Q., Shan, X., Miao, H., Lu, Y., Xu, J., You, N., Liu, C., Liao, D. F., and Jin, J. (2009) Acute activationof acidceramidase affects cytokineinduced cytotoxicity in rat islet beta-cells. FEBS Lett. 583, 2136-2141
33. Maedler, K., Spinas, G. A., Dyntar, D., Moritz, W., Kaiser, N., and Donath, M. Y. (2001) Distinct effects of saturated and monounsaturated fatty acids on beta-cell turnover and function. Diabetes 50, 69-76
34. Shimabukuro, M., Higa, M., Zhou, Y. T., Wang, M. Y., Newgard, C. B., and Unger, R. H. (1998) Lipoapoptosis in beta-cells of obese prediabetic fa/fa rats. Role of serine palmitoyltransferase overexpression. J. Biol. Chem. 273, 32487-32490
35. Shimabukuro, M., Zhou, Y. T., Levi, M., and Unger, R. H. (1998) Fatty acid-induced beta cell apoptosis: a link between obesity and diabetes. Proc. Natl. Acad. Sci. USA 95, 2498-2502
36. Cantrell Stanford, J., Morris, A. J., Sunkara, M., Popa, G. J., Larson, K. L., and Özcan, S. (2012) Sphingosine 1-phosphate (S1P) regulates glucose-stimulated insulin secretion in pancreatic beta cells. J. Biol. Chem. 287, 13457-13464
37. Shimizu, H., Okajima, F., Kimura, T., Ohtani, K., Tsuchiya, T., Takahashi, H., Kuwabara, A., Tomura, H., Sato, K., and Mori, M. (2000) Sphingosine 1-phosphate stimulates insulin secretion in HITT 15 cells and mouse islets. Endocr. J. 47, 261-269
38. Mastrandrea, L. D., Sessanna, S. M., and Laychock, S. G. (2005) Sphingosine kinase activity and sphingosine-1 phosphate production in rat pancreatic islets and INS-1 cells: response to cytokines. Diabetes 54, 1429-1436
39. Rütti, S., Ehses, J. A., Sibler, R. A., Prazak, R., Rohrer, L., Georgopoulos, S., Meier, D. T., Niclauss, N., Berney, T., Donath, M. Y., and von Eckardstein, A. (2009) Low- and high-density lipoproteinsmodulate function, apoptosis, and proliferation of primary human and murine pancreatic beta-cells. Endocrinology 150, 4521-4530
40. Véret, J., Coant, N., Gorshkova, I. A., Giussani, P., Fradet, M., Riccitelli, E., Skobeleva, A., Goya, J., Kassis, N., Natarajan, V., Portha, B., Berdyshev, E. V., and Le Stunff, H. (2013) Role of palmitateinduced sphingoid base-1-phosphate biosynthesis in INS-1 β-cell survival. Biochim. Biophys. Acta 1831, 251-262
41. Zhao, Z., Choi, J., Zhao, C., and Ma, Z. A. (2012) FTY720 normalizes hyperglycemia by stimulating β-cell in vivo regeneration in db/db mice through regulation of cyclin D3 and p57 (KIP2). J. Biol. Chem. 287, 5562-5573
42. Moon, H., Chon, J., Joo, J., Kim, D., In, J., Lee, H., Park, J., and Choi, J. (2013) FTY720 preserved islet β-cellmass by inhibiting apoptosis and increasing survival of β-cells in db/db mice. Diabetes Metab. Res. Rev. 29, 19-24
43. Schüppel, M., Kürschner, U., Kleuser, U., Schäfer-Korting, M., and Kleuser, B. (2008) Sphingosine 1-phosphate restrains insulinmediated keratinocyte proliferation via inhibition of Akt through the S1P2 receptor subtype. J. Invest. Dermatol. 128, 1747-1756
44. Green, J. A., Suzuki, K., Cho, B., Willison, L. D., Palmer, D., Allen, C. D., Schmidt, T. H., Xu, Y., Proia, R. L., Coughlin, S. R., and Cyster, J. G. (2011) The sphingosine 1-phosphate receptor S1P. maintains the homeostasis of germinal center B cells and promotes niche confinement. Nat. Immunol. 12, 672-680