Inhibition of lipolysis by palmitate, H2O2 and the sulfonylurea drug, glimepiride, in rat adipocytes depends on cAMP degradation by lipid droplets

Biochemistry

Volumn 47, Issue 5, 2008, Pages 1259-1273

  Müller, Günter ^a   Wied, Susanne ^a   Over, Sabine ^a   Frick, Wendelin ^a  

^a SANOFI AVENTIS DEUTSCHLAND GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTES; LIPOLYSIS; OBESITY; PATHOGENESIS;

DRUG PRODUCTS; FATTY ACIDS; GLYCEROL; LIPIDS; PHARMACOKINETICS; RATS;

HYDROGEN PEROXIDE;

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE DEAMINASE; ADENYLATE CYCLASE; BUCLADESINE; CILOSTAMIDE; CYCLIC AMP; FATTY ACID; FORSKOLIN; GLIMEPIRIDE; GLUCOSE OXIDASE; GLYCEROL; HORMONE SENSITIVE LIPASE; HYDROGEN PEROXIDE; INSULIN; ISOPRENALINE; LIPID; PALMITIC ACID; PERILIPIN; PERILIPIN A; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHODIESTERASE; PHOSPHOLIPASE C; PROTEIN KINASE B; ROLIPRAM; SULFONYLUREA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOSE TISSUE CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; IMMUNOBLOTTING; INHIBITION KINETICS; LIPOLYSIS; MALE; NEGATIVE FEEDBACK; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ADIPOCYTES; ANIMALS; CYCLIC AMP; CYTOSOL; HYDROGEN PEROXIDE; INSULIN; ISOPROTERENOL; LIPOLYSIS; LIPOSOMES; MALE; MODELS, BIOLOGICAL; PALMITIC ACID; PHOSPHODIESTERASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; SULFONYLUREA COMPOUNDS;

BACTERIA (MICROORGANISMS); MAMMALIA; RATTUS;

EID: 38849083368     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701413t     Document Type: Article

References (69)

1. Frayn, K. N. (2002) Adipose tissue as a buffer for daily lipid flux, Diabetologia 45, 1201-1210.
2. Langin, D. (2006) Adipose tissue lipolysis as a metabolic pathway to define pharmacological strategies against obesity and the metabolic syndrome, Pharmacol. Res. 53, 482-491.
3. Little, S. A., and de Haen, C. (1980) Effects of hydrogen peroxide on basal and hormone-stimulated lipolysis in perifused rat fat cells in relation to the mechanism of action of insulin, J. Biol. Chem. 255, 10888-10895.
4. Mukherjee, S. P. (1980) Mediation of the antilipolytic and lipogenic effects of insulin in adipocytes by intracellular accumulation of hydrogen peroxide, Biochem. Pharmacol. 29, 1239-1246.
5. Burns, T. W., Langley, P. E., Terry, B. E., and Robinson, G. A. (1978) The role of free fatty acids in the regulation of lipolysis by human adipose tissue cells, Metabolism 27, 1755-1762.
6. Müller, G., Wied, S., Wetekam, E.-M., Crecelius, A., Unkelbach, A., and Punter, J. (1994) Stimulation of glucose utilization in 3T3 adipocytes and rat diaphragm in vitro by the sulfonylureas, glimepiride and glibenclamide, is correlated with modulations of the cAMP regulatory cascade, Biochem. Pharmacol. 48, 985-996.
7. Müller, G. (2000) The molecular mechanism of the insulin-mimetic/sensitizing activity of the antidiabetic sulphonylurea drug amaryl, Mol. Med. 6, 907-933.
8. Müller, G. (2005) The mode of action of glimepiride-beyond insulin secretion, Curr. Med. Chem. 5, 499-518.
9. Müller, G., and Petry, S. (2005) Triacylglycerol, Storage and Mobilization of Human, in Encyclopedia in Biochemistry and Molecular Biology (Meyers, A., Ed.) Vol. 14, pp 621-704, Wley-VCH, Weinheim/Germany.
10. Egan, J. J., Greenberg, A. S., Chang, M.-K., Wek, S. A., Moos, M. C., and Londos, C. (1992) Mechanism of hormone-stimulated lipolysis in adipocytes: Translocation of hormone-sensitive lipase to the lipid storage droplet, Proc. Natl. Acad. Sci. U.S.A. 89, 8537-8541.
11. Sztalryd, C., Xu, G., Dorward, H., Tansey, J. T., Contreras, J. A., and Kimmel, A. R. (2003) Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation, J. Cell. Biol. 161, 1093-1103.
12. Rahn, T., Ridderstrale, M., Tornqvist, H., Manganiello, V., Fredrikson, G., Belfrage, P., and Degerman, E. (1994) Essential role of phosphatidylinositol 3-kinase in insulin-induced activation and phosphorylation of the cGMP-inhibited cAMP phosphodiesterase in rat adipocytes, FEBS Lett. 350, 314-318.
13. Degerman, E., Landstrom, T. R., Wijkander, J., Holst, L. S., Ahmad, F., and Belfrage, P. (1998) Phosphorylation and activation of hormone-sensitive adipocyte phosphodiesterase Type 3B, Methods 14, 43-53.
14. Wijkander, J., Landstrom, T. R., Manganiello, V., Belfrage, P., and Degerman, E. (1998) Insulin-induced phosphorylation and activation of phosphodiesterase 3B in rat adipocytes, possible role for protein kinase B but not mitogen-activated protein kinase or p70 S6 kinase, Endocrinology 139, 219-227.
15. Shakur, Y., Holst, L. S., Landstrom, T. R., Movsesian, M., Degerman, E., and Manganiello, V. (2001) Regulation and function of the cyclic nucleotide phosphodiesterase (PDE3) gene family, Prog. Nucleic Acid Res. Mol. Biol. 66, 241-277.
16. Cheung, P., Yang, G., and Boden, G. (2003) Milrinone, a selective PDE3 inhibitor, stimulates lipolysis, endogenous glucose production and insulin secretion, Metabolism 52, 1496-1500.
17. Choi, Y. H., Park, S., Hockman, S., Zmuda-Trzebiatowska, E., Svennelid, F., and Haluzik, M. (2006) Alterations in regulation of energy homestasis in cyclic nucleotide phosphodiesterase 3B-null mice, J. Clin. Invest. 116, 3240-3251.
18. Rahn Landstrom, T., Mei, J., Karlsson, M., Manganiello, V., and Degerman, E. (2000) Down-regulation of cyclic-nucleotide phosphodiesterase 3B in 3T3-L1 adipocytes induced by tumour necrosis factor alpha and cAMP, Biochem. J. 346, 337-343.
19. Mahadev, K., Wu, X., Zilbering, A., Zhu, L., Lawrence, J. T., and Goldstein, B. J. (2001) Hydrogen peroxide generated during cellular insulin stimulation is integral to activation of the distal insulin signaling cascade in 3T3-L1 adipocytes, J. Biol. Chem. 276, 48662-48669.
20. Goldstein, B. J., Mahadev, K., Wu, X., Zhu, L., and Motoshima, H. (2005) Role of insulin-induced reactive oxygen species in the insulin signaling pathway, Antioxid. Redox Signaling 7, 1021-1031.
21. Maragno, I., Dorigo, P., and Fassina, G. (1971) Effect of antimycin A on hormone-stimulated lipolysis in vitro, Biochem. Pharmacol. 20, 2149-2154.
22. Vallano, M. L., Lee, M. Y., and Sonenberg, M. (1983) Hormones modulate adipocyte membrane potential, ATP and lipolysis by free fatty acids, Am. J. Physiol. 245, E266-E272.
23. Abrahamsen, H., Baillie, G., Ngai, J., Vang, T., Nika, K., Ruppelt, A., Mustelin, T., Zaccolo, M., Houslay, M., and Tasken, K. (2004) TCR- and CD28-mediated recruitment of phosphodiesterase 4 to lipid rafts potentiates TCR signalling, J. Immunol. 173, 4847-4858.
24. Zhang, X., and Carey, G. B. (2004) Plasma membrane-bound cyclic AMP phosphodiesterase activity in 3T3-L1 adipocytes, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 137, 309-316.
25. Baillie, G. S., and Houslay, M. D. (2005) Arrestin times for compartmentalised cAMP signalling and phosphodiesterase-4 enzymes, Curr. Opin. Cell. Biol. 17, 129-134.
26. Willoughby, D. (2006) An anchored PKA and PDE4 complex regulates subplasmalemmal cAMP dynamics, EMBO J. 25, 2051-2061.
27. Müller, G., Hanekop, N., Kramer, W., Bandlow, W., and Frick, W. (2002) Interaction of phosphoinositolglycan(-peptides) with plasma membrane lipid rafts of rat adipocytes, Arch. Biochem. Biophys. 408, 17-32.
28. Müller, G., Hanekop, N., Wied, S., and Frick, W. (2002) Cholesterol depletion blocks redistribution of lipid raft components and insulin-mimetic signaling by glimepiride and phosphoinositolglycans in rat adipocytes, Mol. Med. 8, 120-136.
29. Müller, G., Schulz, A., Wied, S., and Frick, W. (2005) Regulation of lipid raft proteins by glimepiride- and insulin-induced glycosylphosphatidylinositol-specific phospholipase C in rat adipocytes, Biochem. Pharmacol. 69, 761-780.
30. Müller, G., Wetekam, E.-M., Jung, C., and Bandlow, W. (1994) Membrane association of lipoprotein lipase and a cAMP-binding ectoprotein in rat adipocytes, Biochemistry 33, 12149-12159.
31. Müller, G., and Wied, S. (1993) The sulfonylurea drug, glimepiride, stimulates glucose transport, glucose transporter translocation, and dephosphorylation in insulin-resistant rat adipocytes in vitro, Diabetes 42, 1852-1867.
32. Ngo, T. T., and Lenhoff, M. M. (1980) Assay for peroxidase and peroxidase-coupled reactions, Anal. Biochem. 105, 389-397.
33. Greenberg, A. S., Egan, J. J., Wek, S. A., Garty, N. B., Blanchette-Mackie, E. J., and Londos, C. (1991) Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets, J. Biol. Chem. 266, 11341-11346.
34. Wolins, N. E., Quaynor, B. K., Skinner, J. R., Schoenfish, M. J., Tzekov, A., and Bickel, P. E. (2005) S3-12, Adipophilin, and TIP47 package lipid in adipocytes, J. Biol. Chem. 280, 19146-19155.
35. Tauchi-Sato, K., Ozeki, S., Houjou, T., Taguchi, R., and Fujimoto, T. (2002) The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition, J. Biol. Chem. 277, 44507-44512.
36. Bartz, R., Li, W.-H., Venables, B., Zehmer, J. K., Roth, M. R., Welti, R., Anderson, G. W., Liu, P., and Chapman, K. D. (2007) Lipidomics reveals that adiposomes store ether lipids and mediate phospholipid traffic, J. Lipid Res. 48, 837-847.
37. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification, Can. J. Biochem. Physiol. 37, 911-917.
38. Folch, J., Lees, M., and Sloane-Stanley, G. H. (1957) A simple method for the isolation and purification of total lipids from animal tissues, J. Biol. Chem. 226, 497-509.
39. Müller, G., Jung, C., Wied, S., Welte, S., Jordan, H., and Frick, W. (2001) Redistribution of glycolipid raft domain components induces insulin-mimetic signaling in rat adipocytes, Mol. Cell. Biol. 21, 4553-4567.
40. Müller, G., Jordan, H., Jung, C., Kleine, H., and Petry, S. (2003) Analysis of lipolysis in adipocytes using a fluorescent fatty acid derivative, Biochimie 85, 1245-1256.
41. Vertesy, L., Beck, B., Brönstrup, M., Ehrlich, K., Kurz, M., Müller, G., Schummer, D., and Seibert, G. (2002) Cyclipostins, novel hormone-sensitive lipase inhibitors from Streptomyces sp. DSM 13381. II. Isolation, structure elucidation and biological properties, J. Antibiot. 55, 480-494.
42. Soares, A. F., Guichardant, M., Cozzone, D., Bernoud-Hubac, N., Bouzaidi-Tiali, N., Lagarde, M., and Geloen, A. (2005) Effects of oxidative stress on adiponectin secretion and lactate production in 3T3-L1 adipocytes, Free Radical Biol. Med. 38, 882-889.
43. Yeaman, S. J. (2003) Hormone-sensitive lipase - new roles for an old enzyme, Biochem. J. 379, 11-22.
44. Zechner, R., Strauss, J. G., Haemmerle, G., Lass, A., and Zimmermann, R. (2005) Lipolysis: pathway under construction, Curr. Opin. Lipidol. 16, 333-340.
45. Blanchette-Mackie, E. J., Dwyer, N. K., Barber, R. A., Coxey, T., Takeda, C. M., Rondinone, J. L., Theodorakis, J. L., Greenberg, A. S., and Londos, C. (1995) Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes, J. Lipid Res. 36, 1211-1226.
46. Brasaemle, D. L., Barber, T., Wolins, N. E., Serrero, G., Blanchette-Mackie, E. J., and Londos, C. (1997) Adipose differentiation-releated protein is an ubiquitously expressed lipid storage droplet-associated protein, J. Lipid Res. 38, 2249-2263.
47. Londos, C., Sztalryd, C., Tansey, J. T., and Kimmel, A. R. (2005) Role of PAT proteins in lipid metabolism, Biochimie 87, 45-49.
48. Wolins, D. E., Brasaemle, D. L., and Bickel, P. E. (2006) A proposed model of fat packaging by exchangeable lipid droplet proteins, FEBS Lett. 580, 5484-5491.
49. Wang, H., and Edens, N. K. (2007) mRNA expression and antilipolytic role of phosphodiesterase 4 in rat adipocytes in vitro, J. Lipid Res. 48, 1099-1107.
50. Snyder, P. B., Esselstyn, J. M., Loughney, K., Wolda, S. L., and Florio, V. A. (2005) The role of cyclic nucleotide phosphodiesterases in the regulation of adipocyte lipolysis, J. Lipid Res. 46, 494-503.
51. Orlean, P., and Menon, A. K. (2007) Thematic review series: lipid posttranslational modifications. GPI anchoring of protein in yeast and mammalian cells, or: how we learned to stop worrying and love glycophospholipids, J. Lipid Res. 48, 993-1011.
52. Buxton, I. L., and Brunton, L. L. (1983) Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes, J. Biol. Chem. 258, 10233-10239.
53. Cooper, D. M. F., and Crossthwaite, A. J. (2006) Higher-order organization and regulation of adenylyl cyclases, Trends Pharmacol. Sci. 27, 426-431.
54. McConnachie, G., Langeberg, L. K., and Scott, J. D. (2006) AKAP signaling complexes: getting to the heart of the matter, Trends Mol. Med. 12, 317-323.
55. 1 stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: role of compartmentalized phosphodiesterases, J. Cell. Biol. 175, 441-451.
56. Zaccolo, M., and Pozzan, T. (2002) Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes, Science 295, 1711-1715.
57. Mongillo, M. (2004) Fluorescence resonance energy transfer-based analysis of cAMP dynamics in live neonatal rat cardiac myocytes reveals distinct functions of compartmentalized phosphodiesterases, Circ. Res. 95, 67-75.
58. Zmuda-Trzebiatowska, E., Oknianska, A., Manganiello, V., and Degerman, E. (2006) Role of PDE3B in insulin-induced glucose uptake, GLUT4 translocation and lipogenesis in primary rat adipocytes, Cell. Signalling 18, 382-390.
59. Bender, A. T., and Beavo, J. A. (2006) Cyclic nucleotide phosphodiesterases: Molecular regulation to clinical use, Pharmacol. Rev. 58, 488-520.
60. Omori, K., and Kotera, J. (2007) Overview of PDEs and their regulation, Circ. Res. 100, 309-327.
61. Liu. H., and Maurice, D. H. (1998) Expression of cyclic GMP-inhibited phosphodiesterases 3A and 3B (PDE3A and PDE3B) in rat tissues: differential subcellular localization and regulated expression by cyclic AMP, Br. J. Pharmacol. 125, 1501-1510.
62. Fujimoto, Y., Itabe, H., Kinoshita, T., Homma, K. J., Onoduka, J., and Mori, M. (2007) Involvement of ACSL in local synthesis of neutral lipids in cytoplasmic lipid droplets in human hepatocyte HuH7, J. Lipid Res. 48, 1280-1292.
63. Brasaemle, D. L., Dolios, G., Shapiro, L., and Wang, R. (2004) Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes, J. Biol. Chem. 279, 46835-46842.
64. Wang, H., Reaves, L. A., and Edens, N. K. (2006) Ginseng extract inhibits lipolysis in rat adipocytes in vitro by activating phosphodiesterase 4, J. Nutr. 136, 337-342.
65. Jepson, C. A., and Yeaman, S. J. (1992) Inhibition of hormone-sensitive lipase by intermediary lipid metabolites, FEBS Lett. 310, 197-200.
66. Hu, L., Deeney, J. T., Nolan, C. J., Peyot, M.-L., Ao, A., Richard, A. M., Luc, E., Faergeman, N. J., Knudsen, J., Guo, W., Sorhede-Winzell, M., Prentki, M., and Corkey, B. E. (2005) Regulation of lipolytic activity by long-chain acyl-coenyme A in islets and adipocytes, Am. J. Physiol. Endocrinol. Metab. 289, E1085-E1092.
67. Bader, S., Kortholt, A., and Van Haastert, P. J. M. (2007) Seven Dictyostelium discoideum phosphodiesterases degrade three pools of cAMP and cGMP, Biochem. J. 402, 153-161.
68. Zacher, L. A., and Carey, G. B. (1999) Cyclic AMP metabolism by swine adipocyte microsomal and plasma membranes, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 124, 61-71.
69. Nilsson, R., Ahmad, F., Swärd, K., Andersson, U., Weston, M., Manganiello, V., and Degerman, E. (2006) Plasma membrane cyclic nucleotide phosphodiesterase 3B (PDE3B) is associated with caveolae in primary adipocytes, Cell. Signalling 18, 1713-1721.