Additive effects of insulin and muscle contraction on fatty acid transport and fatty acid transporters, FAT/CD36, FABPpm, FATP1, 4 and 6

FEBS Letters

Volumn 583, Issue 13, 2009, Pages 2294-2300

  Jain, Swati S ^a   Chabowski, A ^b   Snook, Laelie A ^a   Schwenk, Robert W ^c   Glatz, Jan F C ^c   Luiken, Joost J F P ^c   Bonen, Arend ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Electrical stimulation; Giant vesicle; GLUT4; Membrane translocation; Muscle; Plasma membrane

Indexed keywords

CD36 ANTIGEN; FATTY ACID; FATTY ACID BINDING PROTEIN; FATTY ACID TRANSPORTER; FATTY ACID TRANSPORTER 1; FATTY ACID TRANSPORTER 4; FATTY ACID TRANSPORTER 6; GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; PALMITIC ACID; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; ELECTROSTIMULATION; FATTY ACID TRANSPORT; GENE TRANSLOCATION; GLUCOSE TRANSPORT; MALE; MOUSE; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION;

ANIMALS; ANTIGENS, CD36; ASPARTATE AMINOTRANSFERASE, MITOCHONDRIAL; BIOLOGICAL TRANSPORT; FATTY ACID TRANSPORT PROTEINS; FATTY ACID-BINDING PROTEINS; GLUCOSE TRANSPORTER TYPE 4; HYPOGLYCEMIC AGENTS; INSULIN; MALE; MICE; MICE, INBRED C57BL; MUSCLE CONTRACTION;

EID: 67649502836     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.06.020     Document Type: Article

References (39)

1. Bonen A., Chabowski A., Luiken J.J.F.P., and Glatz J.F.C. Is membrane transport of FFA mediated by lipid, protein, or both? Mechanisms and regulation of protein-mediated cellular fatty acid uptake: molecular, biochemical, and physiological evidence (Invited review). Physiology (Bethesda) 22 (2007) 15-29
2. Abumrad N.A., El-Maghrabi M.R., Amri E.-Z., Lopez E., and Grimaldi P. Cloning of a rat adipocyte membrane protein implicated in binding or transport of long chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J. Biol. Chem. 268 (1993) 17665-17668
3. Coburn C.T., Knapp Jr. F.F., Febbraio M., Beets A.L., Silverstein R.L., and Abumrad N.A. Defective uptake and utilization of long chain fatty acids in muscle and adipose tissue of CD36 knockout mice. J. Biol. Chem. 275 (2000) 32523-32529
4. Ouwens D.M., et al. Cardiac contractile dysfunction in insulin-resistant rats fed a high fat diet is associated with elevated CD36-mediated fatty acid uptake and esterification. Diabetologia 50 (2007) 1938-1948
5. Han X.X., Chabowski A., Tandon N.N., Calles-Escandon J., Glatz J.F., Luiken J.J., and Bonen A. Metabolic challenges reveal impaired fatty acid metabolism and translocation of FAT/CD36 but not FABPpm in obese Zucker rat muscle. Am. J. Physiol. Endocrinol. Metab. 293 (2007) E566-E575
6. DiRusso C.C., Li H., Darwis D., Watkins P.A., Berger J., and Black P.N. Comparative biochemical studies of the murine fatty acid transport proteins (FATP) expressed in yeast. J. Biol. Chem. 280 (2005) 16829-16837
7. Hirsch D., Stahl A., and Lodish H.F. A family of fatty acid transporters conserved from mycobacterium to man. Proc. Natl. Acad. Sci. USA 95 (1998) 8625-8629
8. Doege H., and Stahl A. Protein-mediated fatty acid uptake: novel insights from in vivo models. Physiology (Bethesda) 21 (2006) 259-268
9. Gimeno R.E., Ortegon A.M., Patel S., Punreddy S., Ge P., Sun Y., Lodish H.F., and Stahl A. Characterization of a heart-specific fatty acid transport protein. J. Biol. Chem. 278 (2003) 16039-16044
10. Kim J.K., et al. Inactivation of fatty acid transport protein 1 prevents fat-induced insulin resistance in skeletal muscle. J. Clin. Invest. 113 (2004) 756-763
11. Wu Q., Ortegon A.M., Tsang B., Doege H., Feingold K.R., and Stahl A. FATP1 is an insulin-sensitive fatty acid transporter involved in diet-induced obesity. Mol. Cell Biol. 26 (2006) 3455-3467
12. Sakamoto K., and Goodyear L.J. Invited review: intracellular signaling in contracting skeletal muscle. J. Appl. Physiol. 93 (2002) 369-383
13. Bickerton A.S., et al. Preferential uptake of dietary fatty acids in adipose tissue and muscle in the postprandial period. Diabetes 56 (2007) 168-176
14. Kiens B. Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol. Rev. 86 (2006) 205-243
15. Bonen A., et al. Palmitate transport and fatty acid transporters in red and white muscles. Am. J. Physiol. 275 (1998) E471-E478
16. Bandyopadhyay G.K., Yu J.G., Ofrecio J., and Olefsky J.M. Increased malonyl-CoA levels in muscle from obese and type 2 diabetic subjects lead to decreased fatty acid oxidation and increased lipogenesis; thiazolidinedione treatment reverses these defects. Diabetes 55 (2006) 2277-2285
17. Bonen A., Luiken J.J.F.P., Arumugam Y., Glatz J.F.C., and Tandon N.N. Acute regulation of fatty acid uptake involves the cellular redistribution of fatty acid translocase. J. Biol. Chem. 275 (2000) 14501-14508
18. Koonen D.P.Y., Benton C.R., Arumugam Y., Tandon N.N., Calles-Escandon J., Glatz J.F.C., Luiken J.J.F.P., and Bonen A. Different mechanism can alter fatty acid transport when muscle contractile activity is chronically altered. Am. J. Physiol. Endocrinol. Metab. 286 (2004) 1042-1049
19. Schertzer J.D., Antonescu C.N., Bilan P.J., Jain S., Huang X., Liu Z., Bonen A., and Klip A. A transgenic mouse model to study glucose transporter 4myc regulation in skeletal muscle. Endocrinology 150 (2009) 1935-1940
20. Bonen A., Miskovic D., Tonouchi M., Lemieux K., Wilson M.C., Marette A., and Halestrap A.P. Abundance and subcellular distribution of MCT1 and MCT4 in heart and fast-twitch skeletal muscles. Am. J. Physiol. Endocrinol. Metab. 278 (2000) E10667-E10677
21. Tonouchi M., Hatta H., and Bonen A. Muscle contraction increases lactate transport while reducing sarcolemmal MCT4, but not MCT1. Am. J. Physiol. Endocrinol. Metab. 282 (2002) E1062-E1069
22. Lemieux K., Han X.-X., Dombrowski L., Bonen A., and Marette A. The transferrin receptor defines two distinct contraction-responsive GLUT4 vesicle populations. Diabetes 49 (2000) 183-189
23. Goodyear L.J., and Kahn B.B. Exercise, glucose transport, and insulin sensitivity. Ann. Rev. Med. 49 (1998) 235-261
24. Ploug T., Wojtaszewski J., Kristiansen S., Hespel P., Galbo H., and Richter E. Glucose transport and transporters in muscle giant vesicles: differential effects of insulin and contractions. Am. J. Physiol. 264 (1993) E270-E278
25. Alkhateeb H., Chabowski A., Glatz J.F., Luiken J., and Bonen A. Two phases of palmitate-induced insulin resistance in skeletal muscle: impaired GLUT4 translocation is followed by a reduced GLUT4 intrinsic activity. Am. J. Physiol. Endocrinol. Metab. 293 (2007) E783-E793
26. Isola L.M., Zhou S.L., Kiang C.L., Stump D.D., Bradbury M.W., and Berk P.D. 3T3 fibroblasts transfected with a cDNA for mitochondrial aspartate aminotransferase express plasma membrane fatty acid-binding protein and saturable fatty acid uptake. Proc. Natl. Acad. Sci. USA 92 (1995) 9866-9870
27. Schaffer J.E., and Lodish H.F. Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79 (1994) 427-436
28. Nickerson, J.G. et al. (2009). Greater transport efficiencies of the membrane fatty acid transporters FAT/CD36 and FATP4 compared with FABPpm and FATP1, and differential effects on fatty acid esterification and oxidation in rat skeletal muscle. J. Biol. Chem. doi:10.1074/jbc.M109.004788.
29. Jain, S., Glatz, J.F.C., Luiken, J.J.F.P. and Bonen, A. (2008) In: International Conference on Lipid Biology, Vol. abstract, Maastricht.
30. Turcotte L.P., Raney M.A., and Todd M.K. ERK1/2 inhibition prevents contraction-induced increase in plasma membrane FAT/CD36 content and FA uptake in rodent muscle. Acta Physiol. Scand. 184 (2005) 131-139
31. Nesher R., Karl I.E., and Kipnis D.M. Dissociation of effects of insulin and contraction on glucose transport in rat epitrochlearis muscle. Am. J. Physiol. (Cell Physiol) 249 (1985) C226-C232
32. Bonen A., Han X.-X., Habets D.D.J., Febbraio M., Glatz J.F.C., and Luiken J.J.F.P. A null mutation in skeletal muscle FAT/CD36 reveals its essential role in insulin-, and AICAR-stimulated fatty acid metabolism. Am. J. Physiol. Endocrinol. Metab. 292 (2007) E1740-E1749
33. Gimeno R.E., et al. Targeted deletion of fatty acid transport protein-4 results in early embryonic lethality. J. Biol. Chem. 278 (2003) 49512-49516
34. Herrmann T., et al. Mice with targeted disruption of the fatty acid transport protein 4 (Fatp 4, Slc27a4) gene show features of lethal restrictive dermopathy. J. Cell Biol. 161 (2003) 1105-1115
35. Hall A.M., Wiczer B.M., Herrmann T., Stremmel W., and Bernlohr D.A. Enzymatic properties of purified murine fatty acid transport protein 4 and analysis of acyl-CoA synthetase activities in tissues from FATP4 null mice. J. Biol. Chem. 280 (2005) 11948-11954
36. Lobo S., Wiczer B.M., Smith A.J., Hall A.M., and Bernlohr D.A. Fatty acid metabolism in adipocytes: functional analysis of fatty acid transport proteins 1 and 4. J. Lipid Res. 48 (2007) 609-620
37. Milger K., et al. Cellular uptake of fatty acids driven by the ER-localized acyl-CoA synthetase FATP4. J. Cell Sci. 119 (2006) 4678-4688
38. van Oort M.M., van Doorn J.M., Bonen A., Glatz J.F., van der Horst D.J., Rodenburg K.W., and Luiken J.J. Insulin-induced translocation of CD36 to the plasma membrane is reversible and shows similarity to that of GLUT4. Biochim. Biophys. Acta 1781 (2008) 61-71
39. Eyre N.S., Cleland L.G., and Mayrhof G. FAT/CD36 expression alone is insufficient to enhance cellular uptake of oleate. Biochem. Biophys. Res. Commun. 370 (2008) 404-409