Muscle-derived angiopoietin-like protein 4 is induced by fatty acids via peroxisome proliferator-activated receptor (PPAR)-δ and is of metabolic relevance in humans

Diabetes

Volumn 58, Issue 3, 2009, Pages 579-589

  Staiger, Harald ^a   Haas, Carina ^a   Machann, Jürgen ^a   Werner, Roman ^a   Weisser, Melanie ^a   Schick, Fritz ^a   Machicao, Fausto ^a   Stefan, Norbert ^a   Fritsche, Andreas ^a   Häring, Hans Ulrich ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN; ANGIOPOIETIN LIKE PROTEIN 4; C PEPTIDE; FATTY ACID; GLUCOSE; INSULIN; LIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; UNCLASSIFIED DRUG; ANGPTL4 PROTEIN, HUMAN; LINOLEIC ACID; MESSENGER RNA; PALMITIC ACID;

ADIPOSE TISSUE; ANGPTL4 GENE; ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CLAMP; COHORT ANALYSIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE; GENE EXPRESSION; GENE INDUCTION; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; HYPERINSULINEMIC EUGLYCEMIC CLAMP; IN VITRO STUDY; IN VIVO STUDY; INSULIN BLOOD LEVEL; LIPE GENE; LIPID BLOOD LEVEL; LIPOLYSIS; MAJOR CLINICAL STUDY; MICROARRAY ANALYSIS; MOUSE; MYOTUBE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ORAL GLUCOSE TOLERANCE TEST; PHENOTYPE; PPARD GENE; PPARG GENE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN INDUCTION; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING; BLOOD; DNA MICROARRAY; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GLUCOSE CLAMP TECHNIQUE; GLUCOSE TOLERANCE TEST; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE;

ANGIOPOIETINS; BLOOD GLUCOSE; C-PEPTIDE; GENE EXPRESSION REGULATION; GLUCOSE CLAMP TECHNIQUE; GLUCOSE TOLERANCE TEST; HUMANS; INSULIN; LINOLEIC ACID; LIPIDS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PALMITIC ACID; PPAR ALPHA; PPAR DELTA; RNA, MESSENGER;

EID: 62749136195     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db07-1438     Document Type: Article

References (48)

1. Moller DE, Kaufman KD: Metabolic syndrome: a clinical and molecular perspective. Annu Rev Med 56:45-62, 2005
2. Lee JS, Pinnamaneni SK, Eo SJ, Cho IH, Pyo JH, Kim CK, Sinclair AJ, Febbraio MA, Watt MJ: Saturated, but not n-6 polyunsaturated, fatty acids induce insulin resistance: role of intramuscular accumulation of lipid metabolites. J Appl Physiol 100:1467-1474, 2006
3. Ginsberg HN, Zhang YL, Hernandez-Ono A: Regulation of plasma triglycerides in insulin resistance and diabetes. Arch Med Res 36:232-240, 2005
4. Valera Mora ME, Scarfone A, Calvani M, Greco AV, Mingrone G: Insulin clearance in obesity. J Am Coll Nutr 22:487-493, 2003
5. Manco M, Calvani M, Mingrone G: Effects of dietary fatty acids on insulin sensitivity and secretion. Diabetes Obes Metab 6:402-413, 2004
6. Haag M, Dippenaar NG: Dietary fats, fatty acids and insulin resistance: short review of a multifaceted connection. Med Sci Monit 11:RA359-RA367, 2005
7. Weigert C, Brodbeck K, Staiger H, Kausch C, Machicao F, Haring HU, Schleicher ED: Palmitate, but not unsaturated fatty acids, induces the expression of interleukin-6 in human myotubes through proteasome- dependent activation of nuclear factor-kappaB. J Biol Chem 279:2394223952, 2004
8. Staiger H, Staiger K, Stefan N, Wahl HG, Machicao F, Kellerer M, Haring HU: Palmitate-induced interleukin-6 expression in human coronary artery endothelial cells. Diabetes 53:3209-3216, 2004
9. Staiger K, Staiger H, Weigert C, Haas C, Haring HU, Kellerer M: Saturated, but not unsaturated, fatty acids induce apoptosis of human coronary artery endothelial cells via nuclear factor-kappaB activation. Diabetes 55:31213126, 2006
10. Staiger H, Staiger K, Haas C, Weisser M, Machicao F, Haring HU: Fatty acid-induced differential regulation of the genes encoding peroxisome proliferator-activated receptor-gamma coactivator-1alpha and -1beta in human skeletal muscle cells that have been differentiated in vitro. Diabe- tologia 48:2115-2118, 2005
11. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC: PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267-273, 2003
12. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, Landaker EJ, Goldfine AB, Mun E, DeFronzo R, Finlayson J, Kahn CR, Mandarino LJ: Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 100:8466-8471, 2003
13. Kim I, Kim HG, Kim H, Kim HH, Park SK, Uhm CS, Lee ZH, Koh GY: Hepatic expression, synthesis and secretion of a novel fibrinogen/angio- poietin-related protein that prevents endothelial-cell apoptosis. Biochem J 346:603-610, 2000
14. Kersten S, Mandard S, Tan NS, Escher P, Metzger D, Chambon P, Gonzalez FJ, Desvergne B, Wahli W: Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J Biol Chem. 275:28488-28493, 2000
15. Yoon JC, Chickering TW, Rosen ED, Dussault B, Qin Y, Soukas A, Friedman JM, Holmes WE, Spiegelman BM: Peroxisome proliferator- activated receptor gamma target gene encoding a novel angiopoietin- related protein associated with adipose differentiation. Mol Cell Biol 20:5343-5349, 2000
16. Yoshida K, Shimizugawa T, Ono M, Furukawa H: Angiopoietin-like protein 4 is a potent hyperlipidemia-inducing factor in mice and inhibitor of lipoprotein lipase. J Lipid Res 43:1770-1772, 2002
17. Ge H, Yang G, Yu X, Pourbahrami T, Li C: Oligomerization state-dependent hyperlipidemic effect of angiopoietin-like protein 4. J Lipid Res 45:20712079, 2004
18. Xu A, Lam MC, Chan KW, Wang Y, Zhang J, Hoo RL, Xu JY, Chen B, Chow WS, Tso AW, Lam KS: Angiopoietin-like protein 4 decreases blood glucose and improves glucose tolerance but induces hyperlipidemia and hepatic steatosis in mice. Proc Natl Acad SciUSA102:6086-6091, 2005
19. Koster A, Chao YB, Mosior M, Ford A, Gonzalez-DeWhitt PA, Hale JE, Li D, Qiu Y, Fraser CC, Yang DD, Heuer JG, Jaskunas SR, Eacho P: Transgenic angiopoietin-like (angptl)4 overexpression and targeted disruption of angptl4 and angptl3: regulation of triglyceride metabolism. Endocrinology 146:4943-4950, 2005
20. Yu X, Burgess SC, Ge H, Wong KK, Nassem RH, Garry DJ, Sherry AD, Malloy CR, Berger JP, Li C: Inhibition of cardiac lipoprotein utilization by transgenic overexpression of Angptl4 in the heart. Proc Natl Acad Sci U S A 102:1767-1772, 2005
21. Mandard S, Zandbergen F, van Straten E, Wahli W, Kuipers F, Muller M, Kersten S: The fasting-induced adipose factor/angiopoietin-like protein 4 is physically associated with lipoproteins and governs plasma lipid levels and adiposity. J Biol Chem 281:934-944, 2006
22. Ge H, Cha JY, Gopal H, Harp C, Yu X, Repa JJ, Li C: Differential regulation and properties of angiopoietin-like proteins 3 and 4. J Lipid Res 46:14841490, 2005
23. Mandard S, Zandbergen F, Tan NS, Escher P, Patsouris D, Koenig W, Kleemann R, Bakker A, Veenman F, Wahli W, Muller M, Kersten S: The direct peroxisome proliferator-activated receptor target fasting-induced adipose factor (FIAF/PGAR/ANGPTL4) is present in blood plasma as a truncated protein that is increased by fenofibrate treatment. J Biol Chem 279:34411-34420, 2004
24. Abbot EL, McCormack JG, Reynet C, Hassall DG, Buchan KW, Yeaman SJ: Diverging regulation of pyruvate dehydrogenase kinase isoform gene expression in cultured human muscle cells. FEBS J 272:3004-3014, 2005
25. Motojima K, Passilly P, Peters JM, Gonzalez FJ, Latruffe N: Expression of putative fatty acid transporter genes are regulated by peroxisome prolif- erator-activated receptor alpha and gamma activators in a tissue- and inducer-specific manner. J Biol Chem 273:16710-16714, 1998
26. Brun S, Carmona MC, Mampel T, Vinas O, Giralt M, Iglesias R, Villarroya F: Activators of peroxisome proliferator-activated receptor-alpha induce the expression of the uncoupling protein-3 gene in skeletal muscle: a potential mechanism for the lipid intake-dependent activation of uncoupling pro- tein-3 gene expression at birth. Diabetes 48:1217-1222, 1999
27. Park KS, Ciaraldi TP, Lindgren K, Abrams-Carter L, Mudaliar S, Nikoulina SE, Tufari SR, Veerkamp JH, Vidal-Puig A, Henry RR: Troglitazone effects on gene expression in human skeletal muscle of type II diabetes involve up-regulation of peroxisome proliferator-activated receptor-gamma. JClin Endocrinol Metab 83:2830-2835, 1998
28. Ostrowski K, Rohde T, Zacho M, Asp S, Pedersen BK: Evidence that interleukin-6 is produced in human skeletal muscle during prolonged running. J Physiol 508:949-953, 1998
29. Stegall T, Krolick KA: Myocytes respond to both interleukin-4 and inter- feron-gamma: cytokine responsiveness with the potential to influence the severity and course of experimental myasthenia gravis. Clin Immunol 94:133-139, 2000
30. Nishizawa H, Matsuda M, Yamada Y, Kawai K, Suzuki E, Makishima M, Kitamura T, Shimomura I: Musclin, a novel skeletal muscle-derived secretory factor. J Biol Chem 279:19391-19395, 2004
31. Ge H, Yang G, Huang L, Motola DL, Pourbahrami T, Li C: Oligomerization and regulated proteolytic processing of angiopoietin-like protein 4. J Biol Chem 279:2038-2045, 2004
32. Tanaka T, Yamamoto J, Iwasaki S, Asaba H, Hamura H, Ikeda Y, Watanabe M, Magoori K, Ioka RX, Tachibana K, Watanabe Y, Uchiyama Y, Sumi K, Iguchi H, Ito S, Doi T, Hamakubo T, Naito M, Auwerx J, Yanagisawa M, Kodama T, Sakai J: Activation of peroxisome proliferator-activated receptor delta induces fatty acid beta-oxidation in skeletal muscle and attenuates metabolic syndrome. Proc Natl Acad Sci USA 100:15924-15929, 2003
33. Schafer S, Kantartzis K, Machann J, Venter C, Niess A, Schick F, Machicao F, Haring HU, Fritsche A, Stefan N: Lifestyle intervention in individuals with normal versus impaired glucose tolerance. Eur J Clin Invest 37:535543, 2007
34. Stefan N, Thamer C, Staiger H, Machicao F, Machann J, Schick F, Venter C, Niess A, Laakso M, Fritsche A, Haring HU: Genetic variations in PPARD and PPARGC1A determine mitochondrial function and change in aerobic physical fitness and insulin sensitivity during lifestyle intervention. J Clin Endocrinol Metab 92:1827-1833, 2007
35. Thamer C, Machann J, Stefan N, Haap M, Schafer S, Brenner S, Kantartzis K, Claussen C, Schick F, Haring H, Fritsche A: High visceral fat mass and high liver fat are associated with resistance to lifestyle intervention. Obesity (Silver Spring) 15:531-538, 2007
36. Weyrich P, Stefan N, Haring HU, Laakso M, Fritsche A: Effect of genotype on success of lifestyle intervention in subjects at risk for type 2 diabetes. J Mol Med 85:107-117, 2007
37. Stejskal D, Karpisek M, Reutova H, Humenanska V, Petzel M, Kusnierova P, Vareka I, Varekova R, Stejskal P: Angiopoietin-like protein 4: development, analytical characterization, and clinical testing of a new ELISA. Gen Physiol Biophys 27:59-63, 2008
38. Romeo S, Pennacchio LA, Fu Y, Boerwinkle E, Tybjaerg-Hansen A, Hobbs HH, Cohen JC: Population-based resequencing of ANGPTL4 uncovers variations that reduce triglycerides and increase HDL. Nat Genet 39:513516, 2007
39. Krutzfeldt J, Kausch C, Volk A, Klein HH, Rett K, Haring HU, Stumvoll M: Insulin signaling and action in cultured skeletal muscle cells from lean healthy humans with high and low insulin sensitivity. Diabetes 49:992-998,2000
40. Kausch C, Staiger H, Staiger K, Krutzfeldt J, Matthaei S, Haring HU, Stumvoll M: Skeletal muscle cells from insulin-resistant (non-diabetic) individuals are susceptible to insulin desensitization by palmitate. Horm Metab Res 35:570-576, 2003
41. Staiger H, Kaltenbach S, Staiger K, Stefan N, Fritsche A, Guirguis A, Peterfi C, Weisser M, Machicao F, Stumvoll M, Haring HU: Expression of adiponectin receptor mRNA in human skeletal muscle cells is related to in vivo parameters of glucose and lipid metabolism. Diabetes 53:2195-2201,2004
42. Staiger H, Stefan N, Machicao F, Fritsche A, Haring HU: PPARGC1A mRNA levels of in vitro differentiated human skeletal muscle cells are negatively associated with the plasma oleate concentrations of the donors. Diabeto- logia 49:212-214, 2006
43. Luquet S, Lopez-Soriano J, Holst D, Gaudel C, Jehl-Pietri C, Fredenrich A, Grimaldi PA: Roles of peroxisome proliferator-activated receptor delta (PPARdelta) in the control of fatty acid catabolism: a new target for the treatment of metabolic syndrome. Biochimie 86:833-837, 2004
44. Luquet S, Lopez-Soriano J, Holst D, Fredenrich A, Melki J, Rassoulzadegan M, Grimaldi PA: Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J 17:2299-2301,2003
45. Kannisto K, Chibalin A, Glinghammar B, Zierath JR, Hamsten A, Ehrenborg E: Differential expression of peroxisomal proliferator activated receptors alpha and delta in skeletal muscle in response to changes in diet and exercise. Int J Mol Med 17:45-52, 2006
46. Fritz T, Kramer DK, Karlsson HK, Galuska D, Engfeldt P, Zierath JR, Krook A: Low-intensity exercise increases skeletal muscle protein expression of PPARdelta and UCP3 in type 2 diabetic patients. Diabete Metab Res Rev 22:492-498, 2006
47. Wang YX, Lee CH, Tiep S, Yu RT, Ham J, Kang H, Evans RM: Peroxisome- proliferator-activated receptor delta activates fat metabolism to prevent obesity. Cell 113:159-170, 2003
48. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H, Evans RM: Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2:e294, 2004