Loss of sphingosine kinase 1 predisposes to the onset of diabetes via promoting pancreatic β-cell death in diet-induced obese mice

FASEB Journal

Volumn 27, Issue 10, 2013, Pages 4294-4304

  Qi, Yanfei ^a   Chen, Jinbiao ^a   Lay, Angelina ^a   Don, Anthony ^b,c   Vadas, Mathew ^a   Xia, Pu ^a,d  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d FUDAN UNIVERSITY   (China)

Author keywords

Apoptosis; Lipotoxicity; Sphingolipids; Type 2 diabetes

Indexed keywords

GLUCOSE; INSULIN; PALMITIC ACID; SPHINGOSINE KINASE 1; FAT INTAKE; PHOSPHOTRANSFERASE; SPHINGOSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; COMPARATIVE STUDY; CONTROLLED STUDY; DIET RESTRICTION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE LOSS; GENETIC PREDISPOSITION; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; HYPERINSULINEMIA; IN VIVO STUDY; INSULIN BLOOD LEVEL; LIPID DIET; LIPOTOXICITY; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; WILD TYPE; ANIMAL; COMPLICATION; CYTOLOGY; DIABETES MELLITUS; FAT INTAKE; GENETICS; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; PATHOLOGY; PHYSIOLOGY;

MUS;

ANIMALS; CELL DEATH; DIABETES MELLITUS; DIETARY FATS; GENETIC PREDISPOSITION TO DISEASE; INSULIN-SECRETING CELLS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; OBESITY; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR);

EID: 84885160207     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-230052     Document Type: Article

References (49)

1. Kahn, S. E., Hull, R. L., and Utzschneider, K. M. (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444, 840-846
2. 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. (Lond.) 112, 27-42
3. Giacca, A., Xiao, C., Oprescu, A. I., Carpentier, A. C., and Lewis, G. F. (2011) Lipid-induced pancreatic beta-cell dysfunction: focus on in vivo studies. Am. J. Physiol. Endocrinol. Metab. 300, E255-E262
4. 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
5. Xia, P., and Wadham, C. (2011) Sphingosine 1-phosphate, a key mediator of the cytokine network: juxtacrine signaling. Cytokine Growth Factor Rev. 22, 45-53
6. Hannun, Y. A., and Obeid, L. M. (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9, 139-150
7. Spiegel, S., and Milstien, S. (2007) Functions of the multifaceted family of sphingosine kinases and some close relatives. J. Biol. Chem. 282, 2125-2129
8. Cuvillier, O., Pirianov, G., Kleuser, B., Vanek, P. G., Gutkind, S., and Spiegel, S. (1996) Suppression of ceramidemediated programmed cell death by sphingosine-1-phosphate. Nature 381, 800-803
9. Xia, P., Wang, L., Gamble, J. R., and Vadas, M. A. (1999) Activation of sphingosine kinase by tumor necrosis factor-alpha inhibits apoptosis in human endothelial cells. J. Biol. Chem. 274, 34499-34505
10. Olivera, A., Kohama, T., Edsall, L., Nava, V., Poulton, S., and Spiegel, S. (1999) Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J. Cell Biol. 147, 545-558
11. Sarkar, S., Maceyka, M., Hait, N. C., Paugh, S. W., Milstien, S., and Spiegel, S. (2005) Sphingosine kinase 1 is required for migration, proliferation and survival of MCF-7 human breast cancer cells. FEBS Lett. 579, 5313-5317
12. Sukocheva, O., Wadham, C., Holmes, A., Albanese, N., Feng, F., Bernal, A., Derian, C. K., Ullrich, A., Vadas, M. A., and Xia, P. (2006) Estrogen transactivates EGFR via the sphingosine 1-phosphate receptor Edg-3: the role of sphingosine kinase-1. J. Cell Biol. 173, 301-310
13. Taha, T. A., Kitatani, K., El-Alwani, M., Bielawski, J., and Obeid, L. M. (2006) Loss of sphingosine kinase-1 activates the intrinsic pathway of programmed cell death: modulation of sphingolipid levels and the induction of apoptosis. FASEB J. 20, 482-484
14. 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. U. S. A. 95, 2498-2502
15. 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
16. Veret, J., Coant, N., Gorshkova, I. A., Giussani, P., Riccitelli, E., Skobeleva, A., Goya, J., Kassis, N., Natarajan, V., Portha, B., Berdyshev, E. V., and Le Stunff, H. (2013) Role of palmitate-induced sphingoid base-1-phosphate biosynthesis in INS-1 beta-cell survival. Biochim. Biophys. Acta 1831, 251-262
17. Laybutt, D. R., Preston, A. M., Akerfeldt, M. C., Kench, J. G., Biankin, A. V., and Biden, T. J. (2007) Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 50, 752-763
18. Sone, H., and Kagawa, Y. (2005) Pancreatic beta cell senescence contributes to the pathogenesis of type 2 diabetes in high-fat diet-induced diabetic mice. Diabetologia 48, 58-67
19. Sukocheva, O., Wang, L., Verrier, E., Vadas, M. A., and Xia, P. (2009) Restoring endocrine response in breast cancer cells by inhibition of the sphingosine kinase-1 signaling pathway. Endocrinology 150, 4484-4492
20. Xia, P., Wang, L., Moretti, P. A., Albanese, N., Pitson, S. M., D'Andrea, R. J., Gamble, J. R., and Vadas, M. A. (2002) Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J. Biol. Chem. 277, 7996-8003
21. Wong, J. W., Abuhusain, H. J., McDonald, K. L., and Don, A. S. (2012) MMSAT: automated quantification of metabolites in selected reaction monitoring experiments. Anal. Chem. 84, 470-474
22. Bonora, E., Moghetti, P., Zancanaro, C., Cigolini, M., Cacciatori, V., Corgnati, A., and Muggeo, M. (1989) Estimates of in vivo insulin action in man: comparison of insulin tolerance tests with euglycemic and hyperglycemic glucose clamp studies. J. Clin. Endocrinol. Metab. 68, 374-378
23. Ebato, C., Uchida, T., Arakawa, M., Komatsu, M., Komiya, K., Azuma, K., Hirose, T., Tanaka, K., Kominami, E., Kawamori, R., Fujitani, Y, and Watada, H. (2008) Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet. Cell Metab. 8, 325-332
24. Terauchi, Y., Takamoto, I., Kubota, N., Matsui, J., Komeda, K., Hara, A., Toyoda, Y, Miwa, I., Aizawa, S., Tsutsumi, S., Tsubamoto, Y, Hashimoto, S., Eto, K., Nakamura, A., Noda, M., Tobe, K., Aburatani, H., Nagai, R., and Kadowaki, T. (2007) Glucokinase and IRS-2 are required for compensatory beta cell hyperplasia in response to high-fat diet-induced insulin resistance. J. Clin. Invest. 117, 246-257
25. Qi, Y, and Xia, P. (2012) Cellular inhibitor of apoptosis protein-1 (cIAP1) plays a critical role in beta-cell survival under endoplasmic reticulum stress: promoting ubiquitination and degradation of C/EBP homologous protein (CHOP). J. Biol. Chem. 287, 32236-32245
26. Allagnat, F., Cunha, D., Moore, F., Vanderwinden, J. M., and Cardozo, A. K. (2011) Mcl-1 downregulation by pro-inflammatory cytokines and palmitate is an early event contributing to beta-cell apoptosis. Cell Death Differ. 18, 328-337
27. Cunha, D. A., Igoillo-Esteve, M., Gurzov, E. N., Germano, C. M., Marhfour, I., Fukaya, M., Vanderwinden, J. M., Gysemans, C, Mathieu, C., Marselli, L., Marchetti, P., Harding, H. P., Ron, D., Eizirik, D. L., and Cnop, M. (2012) Death protein 5 and p53-upregulated modulator of apoptosis mediate the endoplasmic reticulum stress-mitochondrial dialog triggering lipotoxic rodent and human beta-cell apoptosis. Diabetes 61, 2763-2775
28. Cerasi, E. (2011) β-Cell dysfunction vs insulin resistance in type 2 diabetes: the eternal "chicken and egg" question. Medicographia 33, 7
29. Okada, T., Liew, C. W., Hu, J., Hinault, C., Krtzfeldt, J., Yin, C, Holzenberger, M., Stoffel, M., and Kulkarni, R. N. (2007) Insulin receptors in beta-cells are critical for islet compensatory growth response to insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 104, 8977-8982
30. Sachdeva, M. M., Claiborn, K. C, Khoo, C, Yang, J., Groff, D. N., Mirmira, R. G., and Stoffers, D. A. (2009) Pdx1 (MODY4) regulates pancreatic beta cell susceptibility to ER stress. Proc. Natl. Acad. Sci. U. S. A. 106, 19090-19095
31. Ellacott, K. L., Morton, G. J., Woods, S. C., Tso, P., and Schwartz, M. W. (2010) Assessment of feeding behavior in laboratory mice. Cell Metab. 12, 10-17
32. Donath, M. Y, Ehses, J. A., Maedler, K., Schumann, D. M., Ellingsgaard, H., and Reinecke, M. (2005) Mechanisms of beta-cell death in type 2 diabetes. Diabetes 54(Suppl. 2), S108-S113
33. Ashcroft, F. M., and Rorsman, P. (2012) Diabetes mellitus and the beta cell: the last ten years. Cell 148, 1160-1171
34. Bonner-Weir, S., Li, W. C., Ouziel-Yahalom, L., Guo, L., and Sharma, A. (2010) Beta-cell growth and regeneration: replication is only part of the story. Diabetes 59, 2340-2348
35. Poitout, V., Amyot, J., Semache, M., Zarrouki, B., and Fontes, G. (2010) Glucolipotoxicity of the pancreatic beta cell. Biochim. Biophys. Acta 1801, 289-298
36. Butler, A. E., Janson, J., Bonner-Weir, S., Ritzel, R., and Butler, P. C. (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52, 102-110
37. Hasan, N. M., Longacre, M. J., Stoker, S. W., Kendrick, M. A., Laychock, S. G., Mastrandrea, L. D., and MacDonald, M. J. (2012) Sphingosine kinase 1 knockdown reduces insulin synthesis and secretion in a rat insulinoma cell line. Arch. Biochem. Biophys. 518, 23-30
38. Ma, M. M., Chen, J. L., Wang, G. G., Wang, H., Yi, J., Yuan, Y. J., Zhang, Q. W., Mi, J., Wang, L., Duan, H. F., and Wu, C. T. (2007) Sphingosine kinase 1 participates in insulin signalling and regulates glucose metabolism and homeostasis in KK/Ay diabetic mice. Diabetologia 50, 891-900
39. Bruce, C. R., Risis, S., Babb, J. R., Yang, C., Selathurai, A., Lee-Young, R. S., Weir, J. M., Yoshioka, K., Takuwa, Y, Meikle, P. J., Pitson, S. M., and Febbraio, M. A (2012) Overexpression of sphingosine kinase 1 prevents ceramide accumulation and ameliorates muscle insulin resistance in high-fat diet-fed mice. Diabetes 61, 3148-3155
40. Karaskov, E., Scott, C., Zhang, L., Teodoro, T., and Volchuk, A. (2006) Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 147, 3398-3407
41. Martinez, S. C., Tanabe, K., Cras-Meneur, C., Abumrad, N. A., and Permutt, M. A. (2008) Inhibition of Foxo1 protects pancreatic islet beta-cells against fatty acid and endoplasmic reticulum stress-induced apoptosis. Diabetes 57, 846-859
42. Shimabukuro, M., Higa, M., Zhou, Y. T., Wang, M. Y., 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
43. Lupi, R., Dotta, F., Marselli, L., Del Guerra, S., Santangelo, C., Patane, G., Boggi, U., Piro, S., Anello, M., Bergamini, E., Mosca, F., Di Mario, U., Del Prato, S., and Marchetti, P. (2002) Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 51, 1437-1442
44. Maedler, K., Oberholzer, J., Bucher, P., Spinas, G. A., and Donath, M. Y. (2003) Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 52, 726-733
45. Boslem, E., MacIntosh, G., Preston, A. M., Bartley, C., Fuller, M., Laybutt, D. R., Meikle, P. J., and Biden, T. J. (2011) A lipidomic screen of palmitate-treated MIN6 beta-cells links sphingolipid metabolites with endoplasmic reticulum (ER) stress and impaired protein trafficking. Biochem. J. 435, 267-276
46. Allende, M. L., Sasaki, T., Kawai, H., Olivera, A., Van Echten-Deckert, G., Hajdu, R., Rosenbach, M., Keohane, C. A., Mandala, S., Spiegel, S., and Proia, R. L. (2004) Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J. Biol. Chem. 279, 52487-52492
47. Olivera, A., Eisner, C., Kitamura, Y., Dillahunt, S., Tuymetova, G., Watford, W., Meylan, F., Diesner, S. C., Li, L., Schnermann, J., Proia, R. L., and Rivera, J. (2010) Sphingosine kinase 1 and sphingosine-1-phosphate receptor 2 are vital to recovery from anaphylactic shock in mice. J. Clin. Invest. 120, 1429-1440
48. Gurzov, E. N., and Eizirik, D. L. (2011) Bcl-2 proteins in diabetes: mitochondrial pathways of beta-cell death and dysfunction. Trends Cell Biol. 21, 424-431
49. Morales, A., Lee, H., Goni, F. M., Kolesnick, R., and Fernandez-Checa, J. C. (2007) Sphingolipids and cell death. Apoptosis 12, 923-939