Sphingosine 1-phosphate (S1P) regulates glucose-stimulated insulin secretion in pancreatic beta cells

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 13457-13464

  Stanford, Jamie Cantrell ^a   Morris, Andrew J ^b   Sunkara, Manjula ^b   Popa, Gabriel J ^a   Larson, Kara L ^a   Özcan, Sabire ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDES; GLUCOSE-STIMULATED INSULIN SECRETIONS; INSULIN RESISTANCE; MIN6 CELLS; PANCREATIC BETA CELLS; PANCREATIC ISLET; PLASMA INSULIN LEVELS; SPHINGOLIPID METABOLISM; SPHINGOLIPIDS; SPHINGOMYELIN; SPHINGOSINE 1 PHOSPHATES; SPHINGOSINE KINASE; SPHINGOSINE KINASE 2; TYPE-2 DIABETES;

AMIDES; CYTOLOGY; ENZYME ACTIVITY; GLUCOSE; INSULIN; MAMMALS; PHOSPHOLIPIDS; PHYSIOLOGY;

CELLS;

CERAMIDE; ENZYME INHIBITOR; GLUCOSE; INSULIN; SMALL INTERFERING RNA; SPHINGOMYELIN; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 2; SPHINGOSINE KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPOSURE; GLUCOSE TOLERANCE TEST; IN VITRO STUDY; INSULIN BLOOD LEVEL; INSULIN RELEASE; LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

ANIMALS; CELL LINE, TUMOR; GLUCOSE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; INJECTIONS, INTRAPERITONEAL; INSULIN; INSULIN-SECRETING CELLS; INSULINOMA; LYSOPHOSPHOLIPIDS; MICE; MICE, INBRED C57BL; PANCREATIC NEOPLASMS; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RNA, SMALL INTERFERING; SPHINGOSINE;

MUS;

EID: 84859749965     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.268185     Document Type: Article

References (40)

1. Adams, J. M., 2nd, Pratipanawatr, T., Berria, R., Wang, E., DeFronzo, R. A., Sullards, M. C., and Mandarino, L. J. (2004) Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes 53, 25-31 (Pubitemid 38044694)
2. Summers, S. A. (2010) Sphingolipids and insulin resistance: the five Ws. Curr. Opin. Lipidol. 21, 128-135
3. Straczkowski, M., and Kowalska, I. (2008) The role of skeletal muscle sphingolipids in the development of insulin resistance. Rev. Diabet. Stud. 5, 13-24
4. Straczkowski, M., Kowalska, I., Baranowski, M., Nikolajuk, A., Otziomek, E., Zabielski, P., Adamska, A., Blachnio, A., Gorski, J., and Gorska, M. (2007) Increased skeletal muscle ceramide level in men at risk of developing type 2 diabetes. Diabetologia 50, 2366-2373 (Pubitemid 47512392)
5. Haus, J. M., Kashyap, S. R., Kasumov, T., Zhang, R., Kelly, K. R., Defronzo, R. A., and Kirwan, J. P. (2009) Plasma ceramides are elevated in obese subjects with type 2 diabetes and correlate with the severity of insulin resistance. Diabetes 58, 337-343
6. Pickersgill, L., Litherland, G. J., Greenberg, A. S., Walker, M., and Yeaman, S. J. (2007) Key role for ceramides in mediating insulin resistance in human muscle cells. J. Biol. Chem. 282, 12583-12589 (Pubitemid 47100630)
7. Boden, G. (2008) Ceramide: a contributor to insulin resistance or an innocent bystander? Diabetologia 51, 1095-1096
8. Aerts, J. M., Ottenhoff, R., Powlson, A. S., Grefhorst, A., van Eijk, M., Dubbelhuis, P. F., Aten, J., Kuipers, F., Serlie, M. J., Wennekes, T., Sethi, J. K., O'Rahilly, S., and Overkleeft, H. S. (2007) Pharmacological inhibition of glucosylceramide synthase enhances insulin sensitivity. Diabetes 56, 1341-1349 (Pubitemid 46715620)
9. Holland, W. L., Brozinick, J. T., Wang, L. P., Hawkins, E. D., Sargent, K. M., Liu, Y., Narra, K., Hoehn, K. L., Knotts, T. A., Siesky, A., Nelson, D. H., Karathanasis, S. K., Fontenot, G. K., Birnbaum, M. J., and Summers, S. A. (2007) Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated fat-, and obesity-induced insulin resistance. Cell Metab. 5, 167-179
10. Zhao, H., Przybylska, M., Wu, I. H., Zhang, J., Siegel, C., Komarnitsky, S., Yew, N. S., and Cheng, S. H. (2007) Inhibiting glycosphingolipid synthesis improves glycemic control and insulin sensitivity in animal models of type 2 diabetes. Diabetes 56, 1210-1218 (Pubitemid 46715599)
11. Kelpe, C. L., Moore, P. C., Parazzoli, S. D., Wicksteed, B., Rhodes, C. J., and Poitout, V. (2003) Palmitate inhibition of insulin gene expression is mediated at the transcriptional level via ceramide synthesis. J. Biol. Chem. 278, 30015-30021 (Pubitemid 36962391)
12. Guo, J., Qian, Y., Xi, X., Hu, X., Zhu, J., and Han, X. (2010) Blockage of ceramide metabolism exacerbates palmitate inhibition of pro-insulin gene expression in pancreatic beta cells. Mol. Cell. Biochem. 338, 283-290
13. Major, C. D., Gao, Z. Y., and Wolf, B. A. (1999) Activation of the sphingomyelinase/ ceramide signal transduction pathway in insulin-secreting beta cells: role in cytokine-induced beta cell death. Diabetes 48, 1372-1380 (Pubitemid 29297298)
14. Laychock, S. G., Sessanna, S. M., Lin, M. H., and Mastrandrea, L. D. (2006) Sphingosine 1-phosphate affects cytokine-induced apoptosis in rat pancreatic islet beta cells. Endocrinology 147, 4705-4712 (Pubitemid 44402178)
15. 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 HIT-T 15 cells and mouse islets. Endocr. J. 47, 261-269 (Pubitemid 30459111)
16. Kim, R. H., Takabe, K., Milstien, S., and Spiegel, S. (2009) Export and functions of sphingosine 1-phosphate. Biochim. Biophys. Acta 1791, 692-696
17. Pyne, N. J., Long, J. S., Lee, S. C., Loveridge, C., Gillies, L., and Pyne, S. (2009) New aspects of sphingosine 1-phosphate signaling in mammalian cells. Adv. Enzyme Regul. 49, 214-221
18. Laychock, S. G., Tian, Y., and Sessanna, S. M. (2003) Endothelial differentiation gene receptors in pancreatic islets and INS-1 cells. Diabetes 52, 1986-1993 (Pubitemid 36919790)
19. Hait, N. C., Allegood, J., Maceyka, M., Strub, G. M., Harikumar, K. B., Singh, S. K., Luo, C., Marmorstein, R., Kordula, T., Milstien, S., and Spiegel, S. (2009) Regulation of histone acetylation in the nucleus by sphingosine 1-phosphate. Science 325, 1254-1257
20. Pyne, S., Lee, S. C., Long, J., and Pyne, N. J. (2009) Role of sphingosine kinases and lipid phosphate phosphatases in regulating spatial sphingosine 1-phosphate signaling in health and disease. Cell. Signal. 21, 14-21
21. Taha, T. A., Hannun, Y. A., and Obeid, L. M. (2006) Sphingosine kinase: biochemical and cellular regulation and role in disease. J. Biochem. Mol. Biol. 39, 113-131
22. Maceyka, M., Milstien, S., and Spiegel, S. (2005) Sphingosine kinases, sphingosine 1-phosphate, and sphingolipidomics. Prostaglandins Other Lipid Mediat. 77, 15-22
23. Ma, M. M., Chen, J. L., Wang, G. G., Wang, H., Lu, Y., Li, J. F., Yi, J., Yuan, Y. J., Zhang, Q. W., Mi, J., Wang, L. Sh., Duan, H. F., and Wu, C. T. (2007) Sphingosine kinase 1 participates in insulin signaling and regulates glucose metabolism and homeostasis in KK/Ay diabetic mice. Diabetologia 50, 891-900 (Pubitemid 46355826)
24. Wang, L., Xing, X. P., Holmes, A., Wadham, C., Gamble, J. R., Vadas, M. A., and Xia, P. (2005) Activation of the sphingosine kinase signaling pathway by high glucose mediates the proinflammatory phenotype of endothelial cells. Circ. Res. 97, 891-899 (Pubitemid 41552674)
25. 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 (Pubitemid 40586674)
26. Miyazaki, J., Araki, K., Yamato, E., Ikegami, H., Asano, T., Shibasaki, Y., Oka, Y., and Yamamura, K. (1990) Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127, 126 -132
27. Olivera, A., Rosenthal, J., and Spiegel, S. (1996) Effect of acidic phospholipids on sphingosine kinase. J. Cell Biochem. 60, 529-537 (Pubitemid 26112065)
28. Mathews, T. P., Kennedy, A. J., Kharel, Y., Kennedy, P. C., Nicoara, O., Sunkara, M., Morris, A. J., Wamhoff, B. R., Lynch, K. R., and Macdonald, T. L. (2010) Discovery, biological evaluation, and structure-activity relationship of amidine-based sphingosine kinase inhibitors. J. Med. Chem. 53, 2766-2778
29. Andrali, S. S., Qian, Q., and Ozcan, S. (2007) Glucose mediates the translocation of NeuroD1 by O-linked glycosylation. J. Biol. Chem. 282, 15589-15596 (Pubitemid 47093263)
30. Vanderford, N. L., Andrali, S. S., and Ozcan, S. (2007) Glucose induces MafA expression in pancreatic beta cell lines via the hexosamine biosynthetic pathway. J. Biol. Chem. 282, 1577-1584 (Pubitemid 47076679)
31. Vanderford, N. L., Cantrell, J. E., Popa, G. J., and Ozcan, S. (2008) Multiple kinases regulate mafA expression in the pancreatic beta cell line MIN6. Arch. Biochem. Biophys. 480, 138-142
32. Buehrer, B. M., Bardes, E. S., and Bell, R. M. (1996) Protein kinase C-dependent regulation of human erythroleukemia (HEL) cell sphingosine kinase activity. Biochim. Biophys. Acta 1303, 233-242 (Pubitemid 26349043)
33. Takabe, K., Paugh, S. W., Milstien, S., and Spiegel, S. (2008) "Inside-out"signaling of sphingosine 1-phosphate: therapeutic targets. Pharmacol. Rev. 60, 181-195 (Pubitemid 351962008)
34. Rosen, H., Gonzalez-Cabrera, P. J., Sanna, M. G., and Brown, S. (2009) Sphingosine 1-phosphate receptor signaling. Annu. Rev. Biochem. 78, 743-768
35. Mastrandrea, L. D., Sessanna, S. M., Del Toro, A., and Laychock, S. G. (2010) ATP-independent glucose stimulation of sphingosine kinase in rat pancreatic islets. J. Lipid Res. 51, 2171-2180
36. Pitson, S. M., Moretti, P. A., Zebol, J. R., Lynn, H. E., Xia, P., Vadas, M. A., and Wattenberg, B. W. (2003) Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J. 22, 5491-5500 (Pubitemid 37279958)
37. Hait, N. C., Bellamy, A., Milstien, S., Kordula, T., and Spiegel, S. (2007) Sphingosine kinase type 2 activation by ERK-mediated phosphorylation. J. Biol. Chem. 282, 12058-12065 (Pubitemid 47100715)
38. Ding, G., Sonoda, H., Yu, H., Kajimoto, T., Goparaju, S. K., Jahangeer, S., Okada, T., and Nakamura, S. (2007) Protein kinase D-mediated phosphorylation and nuclear export of sphingosine kinase 2. J. Biol. Chem. 282, 27493-27502 (Pubitemid 47501982)
39. 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 (Pubitemid 41747151)
40. Pappu, R., Schwab, S. R., Cornelissen, I., Pereira, J. P., Regard, J. B., Xu, Y., Camerer, E., Zheng, Y. W., Huang, Y., Cyster, J. G., and Coughlin, S. R. (2007) Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine 1-phosphate. Science 316, 295-298 (Pubitemid 46633109)