Fenretinide prevents lipid-induced insulin resistance by blocking ceramide biosynthesis

Journal of Biological Chemistry

Volumn 287, Issue 21, 2012, Pages 17426-17437

  Bikman, Benjamin T ^a,b   Guan, Yuguang ^b   Shui, Guanghou ^c   Siddique, M Mobin ^b   Holland, William L ^d   Kim, Ji Yun ^c   Fabriàs, Gemma ^e   Wenk, Markus R ^c   Summers, Scott A ^b,f  

^a BRIGHAM YOUNG UNIVERSITY   (United States)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e DEPARTMENT OF ENVIRONMENTAL CHEMISTRY   (Spain)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER; CELLULAR LIPID; CERAMIDES; CLINICAL TRIAL; DIHYDROCERAMIDE DESATURASE; GLUCOSE HOMEOSTASIS; GLUCOSE UPTAKE; HIGH-FAT DIET; IN-VITRO; INSULIN ACTION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPIDOMES; MECHANISM OF ACTION; MODEL SYSTEM; MYOTUBES; REACTION CATALYZED;

AMIDES; AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; ENZYMES; GLUCOSE; PHYSIOLOGY;

INSULIN;

CERAMIDE; DIHYDROCERAMIDE DESATURASE; ENZYME; FATTY ACID; FENRETINIDE; GLUCOSE; INSULIN; LIPIDOME; OLEIC ACID; PROTEIN KINASE B; SPHINGOLIPID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; DRUG TARGETING; ENZYME ACTIVATION; FATTY LIVER; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; HORMONE ACTION; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LIPOGENESIS; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MOUSE; MYOTUBE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE;

ANIMALS; ANTICARCINOGENIC AGENTS; CELL LINE; CERAMIDES; FENRETINIDE; GLUCOSE; HOMEOSTASIS; INSULIN RESISTANCE; LIPID METABOLISM; MALE; MICE; MULTIENZYME COMPLEXES; OXIDOREDUCTASES; PROTO-ONCOGENE PROTEINS C-AKT;

MUS;

EID: 84861208352     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.359950     Document Type: Article

References (38)

1. Antonoff, M. B., and D'Cunha, J. (2010) Teaching an old drug new tricks: metformin as a targeted therapy for lung cancer. Semin. Thorac. Cardiovasc. Surg. 22, 195-196
2. Heemskerk, J., Tobin, A. J., and Bain, L. J. (2002) Teaching old drugs new tricks: Meeting of the Neurodegeneration Drug Screening Consortium, 7-8 April 2002, Washington, DC, USA. Trends Neurosci. 25, 494-496
3. Bonanni, B., and Lazzeroni, M. (2009) Retinoids and breast cancer prevention. Recent Results Cancer Res. 181, 77-82
4. Wang, H., Charles, A. G., Frankel, A. J., and Cabot, M. C. (2003) Increasing intracellular ceramide: an approach that enhances the cytotoxic response in prostate cancer cells. Urology 61, 1047-1052 (Pubitemid 36547768)
5. Preitner, F., Mody, N., Graham, T. E., Peroni, O. D., and Kahn, B. B. (2009) Long-term fenretinide treatment prevents high-fat diet-induced obesity, insulin resistance, and hepatic steatosis. Am. J. Physiol. Endocrinol. Metab. 297, E1420-E1429
6. Yang, Q., Graham, T. E., Mody, N., Preitner, F., Peroni, O. D., Zabolotny, J. M., Kotani, K., Quadro, L., and Kahn, B. B. (2005) Serum retinol-binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436, 356-362 (Pubitemid 41065039)
7. Johansson, H., Gandini, S., Guerrieri-Gonzaga, A., Iodice, S., Ruscica, M., Bonanni, B., Gulisano, M., Magni, P., Formelli, F., and Decensi, A. (2008) Effect of fenretinide and low-dose tamoxifen on insulin sensitivity in premenopausal women at high risk for breast cancer. Cancer Res. 68, 9512-9518
8. Zheng, W. (2006) Fenretinide increases dihydroceramide and dihydrosphingolipids due to inhibition of dihydroceramide desaturase. Ph.D. thesis, Georgia Institute of Technology, Atlanta, GA
9. Holland, W. L., Bikman, B. T., Wang, L. P., Yuguang, G., Sargent, K. M., Bulchand, S., Knotts, T. A., Shui, G., Clegg, D. J., Wenk, M. R., Pagliassotti, M. J., Scherer, P. E., and Summers, S. A. (2011) Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J. Clin. Invest. 121, 1858-1870
10. 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
11. Munoz-Olaya, J. M., Matabosch, X., Bedia, C., Egido-Gabás, M., Casas, J., Llebaria, A., Delgado, A., and Fabriàs, G. (2008) Synthesis and biological activity of a novel inhibitor of dihydroceramide desaturase. ChemMed- Chem. 3, 946-953
12. Valsecchi, M., Aureli, M., Mauri, L., Illuzzi, G., Chigorno, V., Prinetti, A., and Sonnino, S. (2010) Sphingolipidomics of A2780 human ovarian carcinoma cells treated with synthetic retinoids. J. Lipid Res. 51, 1832-1840
13. Wang, H., Maurer, B. J., Liu, Y. Y., Wang, E., Allegood, J. C., Kelly, S., Symolon, H., Liu, Y., Merrill, A. H., Jr., Gouazé-Andersson, V., Yu, J. Y., Giuliano, A. E., and Cabot, M. C. (2008) N-(4-Hydroxyphenyl)retinamide increases dihydroceramide and synergizes with dimethylsphingosine to enhance cancer cell killing. Mol. Cancer Ther 7, 2967-2976
14. Brozinick, J. T., Jr., and Birnbaum, M. J. (1998) Insulin, but not contraction, activates Akt/PKB in isolated rat skeletal muscle. J. Biol. Chem. 273, 14679-14682
15. Vratilova, J., Frgala, T., Maurer, B. J., and Patrick Reynolds, C. (2004) Liquid chromatography method for quantifying N-(4-hydroxyphenyl-) retinamide and N-(4-methoxyphenyl)retinamide in tissues. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 808, 125-130 (Pubitemid 38952906)
16. Fei, W., Shui, G., Gaeta, B., Du, X., Kuerschner, L., Li, P., Brown, A. J., Wenk, M. R., Parton, R. G., and Yang, H. (2008) Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. J. Cell Biol. 180, 473-482 (Pubitemid 351240697)
17. Chan, R., Uchil, P. D., Jin, J., Shui, G., Ott, D. E., Mothes, W., and Wenk, M. R. (2008) Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides. J. Virol. 82, 11228-11238
18. Shui, G., Guan, X. L., Low, C. P., Chua, G. H., Goh, J. S., Yang, H., and Wenk, M. R. (2010) Toward one step analysis of cellular lipidomes using liquid chromatography coupled with mass spectrometry: application to Saccharomyces cerevisiae and Schizosaccharomyces pombe lipidomics. Mol. Biosyst. 6, 1008-1017
19. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
20. Chavez, J. A., Knotts, T. A., Wang, L. P., Li, G., Dobrowsky, R. T., Florant, G. L., and Summers, S. A. (2003) A role for ceramide, but not diacylglycerol, in the antagonism of insulin signal transduction by saturated fatty acids. J. Biol. Chem. 278, 10297-10303 (Pubitemid 36800291)
21. Chavez, J. A., Holland, W. L., Bär, J., Sandhoff, K., and Summers, S. A. (2005) Acid ceramidase overexpression prevents the inhibitory effects of saturated fatty acids on insulin signaling. J. Biol. Chem. 280, 20148-20153 (Pubitemid 41379546)
22. Yang, G., Badeanlou, L., Bielawski, J., Roberts, A. J., Hannun, Y. A., and Samad, F. (2009) Central role of ceramide biosynthesis in body weight regulation, energy metabolism, and the metabolic syndrome. Am. J. Physiol. Endocrinol. Metab. 297, E211-E224
23. Schmitz-Peiffer, C., Craig, D. L., and Biden, T. J. (1999) Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J. Biol. Chem. 274, 24202-24210
24. Zheng, W., Kollmeyer, J., Symolon, H., Momin, A., Munter, E., Wang, E., Kelly, S., Allegood, J. C., Liu, Y., Peng, Q., Ramaraju, H., Sullards, M. C., Cabot, M., and Merrill, A. H., Jr. (2006) Ceramides and other bioactive sphingolipid backbones in health and disease: lipidomic analysis, metabolism, and roles in membrane structure, dynamics, signaling, and autophagy. Biochim. Biophys. Acta 1758, 1864-1884 (Pubitemid 44879367)
25. Signorelli, P., Munoz-Olaya, J. M., Gagliostro, V., Casas, J., Ghidoni, R., and Fabriàs, G. (2009) Dihydroceramide intracellular increase in response to resveratrol treatment mediates autophagy in gastric cancer cells. Cancer Lett. 282, 238-243
26. Yetukuri, L., Katajamaa, M., Medina-Gomez, G., Seppänen-Laakso, T., Vidal-Puig, A., and Oresic, M. (2007) Bioinformatics strategies for lipidomics analysis: characterization of obesity-related hepatic steatosis. BMC Syst. Biol. 1, 12
27. Bijl, N., Scheij, S., Houten, S., Boot, R. G., Groen, A. K., and Aerts, J. M. (2008) The glucosylceramide synthase inhibitor N-(5-adamantane-1- ylmethoxy- pentyl)-deoxynojirimycin induces sterol regulatory elementbinding protein-regulated gene expression and cholesterol synthesis in HepG2 cells. J. Pharmacol. Exp. Ther. 326, 849-855
28. 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)
29. Zhao, H., Przybylska, M., Wu, I. H., Zhang, J., Maniatis, P., Pacheco, J., Piepenhagen, P., Copeland, D., Arbeeny, C., Shayman, J. A., Aerts, J. M., Jiang, C., Cheng, S. H., and Yew, N. S. (2009) Inhibiting glycosphingolipid synthesis ameliorates hepatic steatosis in obese mice. Hepatology 50, 85-93
30. Deevska, G. M., Rozenova, K. A., Giltiay, N. V., Chambers, M. A., White, J., Boyanovsky, B. B., Wei, J., Daugherty, A., Smart, E. J., Reid, M. B., Merrill, A. H., Jr., and Nikolova-Karakashian, M. (2009) Acid sphingomyelinase deficiency prevents diet-induced hepatic triacylglycerol accumulation and hyperglycemia in mice. J. Biol. Chem. 284, 8359-8368
31. Rahmaniyan, M., Curley, R. W., Jr., Obeid, L. M., Hannun, Y. A., and Kraveka, J. M. (2011) Identification of dihydroceramide desaturase as a direct in vitro target for fenretinide. J. Biol. Chem. 286, 24754-24764
32. Chavez, J. A., and Summers, S. A. (2003) Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Arch. Biochem. Biophys. 419, 101-109 (Pubitemid 37329976)
33. Henique, C., Mansouri, A., Fumey, G., Lenoir, V., Girard, J., Bouillaud, F., Prip-Buus, C., and Cohen, I. (2010) Increased mitochondrial fatty acid oxidation is sufficient to protect skeletal muscle cells from palmitate-induced apoptosis. J. Biol. Chem. 285, 36818-36827
34. Hu, W., Ross, J., Geng, T., Brice, S. E., and Cowart, L. A. (2011) Differential regulation of dihydroceramide desaturase by palmitate versus monounsaturated fatty acids: implications for insulin resistance. J. Biol. Chem. 286, 16596-16605
35. Bikman, B. T., and Summers, S. A. (2011) Sphingolipids and hepatic steatosis. Adv. Exp. Med. Biol. 721, 87-97
36. Wang, H., Maurer, B. J., Reynolds, C. P., and Cabot, M. C. (2001) N-(4- Hydroxyphenyl)retinamide elevates ceramide in neuroblastoma cell lines by coordinate activation of serine palmitoyltransferase and ceramide synthase. Cancer Res. 61, 5102-5105 (Pubitemid 32681541)
37. Li, X., Ling, W., Pennisi, A., Khan, S., and Yaccoby, S. (2009) Fenretinide inhibits myeloma cell growth, osteoclastogenesis, and osteoclast viability. Cancer Lett. 284, 175-181
38. Saeed, Z., Guilbault, C., De Sanctis, J. B., Henri, J., Marion, D., St-Arnaud, R., and Radzioch, D. (2008) Fenretinide prevents the development of osteoporosis in Cftr-KO mice. J. Cyst. Fibros. 7, 222-230 (Pubitemid 351650269)