Overexpression of CD36 and Acyl-CoA synthetases FATP2, FATP4 and ACSL1 increases fatty acid uptake in human hepatoma cells

International Journal of Medical Sciences

Volumn 8, Issue 7, 2011, Pages 599-614

  Krammer, Julia ^a   Digel, Margarete ^a   Ehehalt, Friedrich ^a   Stremmel, Wolfgang ^a   Füllekrug, Joachim ^a   Ehehalt, Robert ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Acyl CoA synthetases; CD36; Fatty acid transport; Nonalcoholic fatty liver disease; Nonalcoholic steatohepatitis

Indexed keywords

ACYL COA SYNTHASE 1; BODIPY C12 FATTY ACID; CD36 ANTIGEN; FATTY ACID; FATTY ACID TRANSPORTER 2; FATTY ACID TRANSPORTER 4; LONG CHAIN FATTY ACID COENZYME A LIGASE; OLEIC ACID; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; ENZYME REGULATION; FATTY ACID TRANSPORT; FATTY LIVER; FLUORESCENCE ACTIVATED CELL SORTING; HEPATOMA CELL; HUMAN; HUMAN CELL; LIPID METABOLISM; MITOCHONDRION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING;

EID: 80054745073     PISSN: 14491907     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijms.8.599     Document Type: Article

References (57)

1. Glatz JF, Luiken JJ, Bonen A: Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev 2010, 90(1):367-417.
2. Digel M, Ehehalt R, Stremmel W, Fullekrug J: Acyl-CoA syn-thetases: fatty acid uptake and metabolic channeling. Mol Cell Biochem 2009, 326(1-2):23-28.
3. Ehehalt R, Fullekrug J, Pohl J, Ring A, Herrmann T, Stremmel W: Translocation of long chain fatty acids across the plasma membrane--lipid rafts and fatty acid transport proteins. Mol Cell Biochem 2006, 284(1-2):135-140.
4. Su X, Abumrad NA: Cellular fatty acid uptake: a pathway under construction. Trends Endocrinol Metab 2009, 20(2):72-77.
5. Schwenk RW, Holloway GP, Luiken JJ, Bonen A, Glatz JF: Fatty acid transport across the cell membrane: regulation by fatty acid transporters. Prostaglandins Leukot Essent Fatty Acids 2010, 82(4-6):149-154.
6. Stahl A: A current review of fatty acid transport proteins (SLC27). Pflugers Arch 2004, 447(5):722-727.
7. Kampf JP, Kleinfeld AM: Is membrane transport of FFA medi-ated by lipid, protein, or both? An unknown protein mediates free fatty acid transport across the adipocyte plasma mem-brane. Physiology (Bethesda) 2007, 22:7-14.
8. Hamilton JA: New insights into the roles of proteins and lipids in membrane transport of fatty acids. Prostaglandins Leukot Essent Fatty Acids 2007, 77(5-6):355-361.
9. Lewis GF, Carpentier A, Adeli K, Giacca A: Disordered fat storage and mobilization in the pathogenesis of insulin re-sistance and type 2 diabetes. Endocr Rev 2002, 23(2):201-229.
10. Harrison SA, Diehl AM: Fat and the liver--a molecular over-view. Semin Gastrointest Dis 2002, 13(1):3-16.
11. Wahren J, Sato Y, Ostman J, Hagenfeldt L, Felig P: Turnover and splanchnic metabolism of free fatty acids and ketones in insulin-dependent diabetics at rest and in response to exercise. J Clin Invest 1984, 73(5):1367-1376.
12. Verna EC, Berk PD: Role of fatty acids in the pathogenesis of obesity and fatty liver: impact of bariatric surgery. Semin Liver Dis 2008, 28(4):407-426.
13. Hilden M, Christoffersen P, Juhl E, Dalgaard JB: Liver histology in a 'normal' population--examinations of 503 consecutive fatal traffic casualties. Scand J Gastroenterol 1977, 12(5):593-597.
14. Bellentani S, Saccoccio G, Masutti F, Croce LS, Brandi G, Sasso F, Cristanini G, Tiribelli C: Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med 2000, 132(2):112-117.
15. Silverstein RL, Febbraio M: CD36, a scavenger receptor in-volved in immunity, metabolism, angiogenesis, and behavior. Sci Signal 2009, 2(72):re3.
16. Engelmann B, Wiedmann MK: Cellular phospholipid uptake: flexible paths to coregulate the functions of intracellular lipids. Biochim Biophys Acta 2010, 1801(6):609-616.
17. Calvo D, Gomez-Coronado D, Suarez Y, Lasuncion MA, Vega MA: Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL. J Lipid Res 1998, 39(4):777-788.
18. Connelly MA, Klein SM, Azhar S, Abumrad NA, Williams DL: Comparison of class B scavenger receptors, CD36 and scaven-ger receptor BI (SR-BI), shows that both receptors mediate high density lipoprotein-cholesteryl ester selective uptake but SR-BI exhibits a unique enhancement of cholesteryl ester uptake. J Biol Chem 1999, 274(1):41-47.
19. Ehehalt R, Sparla R, Kulaksiz H, Herrmann T, Fullekrug J, Stremmel W: Uptake of long chain fatty acids is regulated by dynamic interaction of FAT/CD36 with cholester-ol/sphingolipid enriched microdomains (lipid rafts). BMC Cell Biol 2008, 9:45.
20. Pohl J, Ring A, Korkmaz U, Ehehalt R, Stremmel W: FAT/CD36-mediated long-chain fatty acid uptake in adipo-cytes requires plasma membrane rafts. Mol Biol Cell 2005, 16(1):24-31.
21. Cheung L, Andersen M, Gustavsson C, Odeberg J, Fernandez-Perez L, Norstedt G, Tollet-Egnell P: Hormonal and nutritional regulation of alternative CD36 transcripts in rat liv-er--a role for growth hormone in alternative exon usage. BMC Mol Biol 2007, 8:60.
22. Bechmann LP, Gieseler RK, Sowa JP, Kahraman A, Erhard J, Wedemeyer I, Emons B, Jochum C, Feldkamp T, Gerken G et al: Apoptosis is associated with CD36/fatty acid translocase up-regulation in non-alcoholic steatohepatitis. Liver Int 2010, 30(6):850-859.
23. Greco D, Kotronen A, Westerbacka J, Puig O, Arkkila P, Kiviluoto T, Laitinen S, Kolak M, Fisher RM, Hamsten A et al: Gene expression in human NAFLD. Am J Physiol Gastrointest Liver Physiol 2008, 294(5):G1281-1287.
24. Ellis JM, Frahm JL, Li LO, Coleman RA: Acyl-coenzyme A synthetases in metabolic control. Curr Opin Lipidol 2010, 21(3):212-217.
25. Watkins PA: Very-long-chain acyl-CoA synthetases. J Biol Chem 2008, 283(4):1773-1777.
26. Gimeno RE: Fatty acid transport proteins. Curr Opin Lipidol 2007, 18(3):271-276.
27. Mashek DG, Li LO, Coleman RA: Long-chain acyl-CoA syn-thetases and fatty acid channeling. Future Lipidol 2007, 2(4):465-476.
28. Stahl A, Hirsch DJ, Gimeno RE, Punreddy S, Ge P, Watson N, Patel S, Kotler M, Raimondi A, Tartaglia LA et al: Identification of the major intestinal fatty acid transport protein. Mol Cell 1999, 4(3):299-308.
29. Milger K, Herrmann T, Becker C, Gotthardt D, Zickwolf J, Ehehalt R, Watkins PA, Stremmel W, Fullekrug J: Cellular up-take of fatty acids driven by the ER-localized acyl-CoA synthe-tase FATP4. J Cell Sci 2006, 119(Pt 22):4678-4688.
30. Doege H, Stahl A: Protein-mediated fatty acid uptake: novel insights from in vivo models. Physiology (Bethesda) 2006, 21:259-268.
31. Hirsch D, Stahl A, Lodish HF: A family of fatty acid transport-ers conserved from mycobacterium to man. Proc Natl Acad Sci U S A 1998, 95(15):8625-8629.
32. Mashek DG, Li LO, Coleman RA: Rat long-chain acyl-CoA synthetase mRNA, protein, and activity vary in tissue distribu-tion and in response to diet. J Lipid Res 2006, 47(9):2004-2010.
33. Sandoval A, Fraisl P, Arias-Barrau E, Dirusso CC, Singer D, Sealls W, Black PN: Fatty acid transport and activation and the expression patterns of genes involved in fatty acid trafficking. Arch Biochem Biophys 2008, 477(2):363-371.
34. Falcon A, Doege H, Fluitt A, Tsang B, Watson N, Kay MA, Stahl A: FATP2 is a hepatic fatty acid transporter and peroxisomal very long-chain acyl-CoA synthetase. Am J Physiol Endocrinol Metab 2010, 299(3):E384-393.
35. Uchiyama A, Aoyama T, Kamijo K, Uchida Y, Kondo N, Orii T, Hashimoto T: Molecular cloning of cDNA encoding rat very long-chain acyl-CoA synthetase. J Biol Chem 1996, 271(48):30360-30365.
36. Kim JH, Lewin TM, Coleman RA: Expression and characteriza-tion of recombinant rat Acyl-CoA synthetases 1, 4, and 5. Selective inhibition by triacsin C and thiazolidinediones. J Biol Chem 2001, 276(27):24667-24673.
37. Ehehalt R, Keller P, Haass C, Thiele C, Simons K: Amyloido-genic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J Cell Biol 2003, 160(1):113-123.
38. Harder Z, Zunino R, McBride H: Sumo1 conjugates mitochon-drial substrates and participates in mitochondrial fission. Curr Biol 2004, 14(4):340-345.
39. Stremmel W, Berk PD: Hepatocellular influx of [14C]oleate reflects membrane transport rather than intracellular metabo-lism or binding. Proc Natl Acad Sci U S A 1986, 83(10):3086-3090.
40. Ehehalt R, Jochims C, Lehmann WD, Erben G, Staffer S, Reininger C, Stremmel W: Evidence of luminal phosphatidyl-choline secretion in rat ileum. Biochim Biophys Acta 2004, 1682(1-3):63-71.
41. Ehehalt R, Krautter M, Zorn M, Sparla R, Fullekrug J, Kulaksiz H, Stremmel W: Increased basolateral sorting of carcinoem-bryonic antigen in a polarized colon carcinoma cell line after cholesterol depletion-Implications for treatment of inflamma-tory bowel disease. World J Gastroenterol 2008, 14(10):1528-1533.
42. Tzircotis G, Thorne RF, Isacke CM: A new spreadsheet method for the analysis of bivariate flow cytometric data. BMC Cell Biol 2004, 5:10.
43. Hall AM, Smith AJ, Bernlohr DA: Characterization of the Acyl-CoA synthetase activity of purified murine fatty acid transport protein 1. J Biol Chem 2003, 278(44):43008-43013.
44. Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
45. Heinzer AK, Kemp S, Lu JF, Watkins PA, Smith KD: Mouse very long-chain acyl-CoA synthetase in X-linked adrenoleu-kodystrophy. J Biol Chem 2002, 277(32):28765-28773.
46. Steinberg SJ, Wang SJ, McGuinness MC, Watkins PA: Human liver-specific very-long-chain acyl-coenzyme A synthetase: cDNA cloning and characterization of a second enzymatically active protein. Mol Genet Metab 1999, 68(1):32-42.
47. Lobo S, Wiczer BM, Smith AJ, Hall AM, Bernlohr DA: Fatty acid metabolism in adipocytes: functional analysis of fatty acid transport proteins 1 and 4. J Lipid Res 2007, 48(3):609-620.
48. Lewin TM, Kim JH, Granger DA, Vance JE, Coleman RA: Acyl-CoA synthetase isoforms 1, 4, and 5 are present in differ-ent subcellular membranes in rat liver and can be inhibited in-dependently. J Biol Chem 2001, 276(27):24674-24679.
49. Li LO, Mashek DG, An J, Doughman SD, Newgard CB, Coleman RA: Overexpression of rat long chain acyl-coa syn-thetase 1 alters fatty acid metabolism in rat primary hepato-cytes. J Biol Chem 2006, 281(48):37246-37255.
50. Koonen DP, Jacobs RL, Febbraio M, Young ME, Soltys CL, Ong H, Vance DE, Dyck JR: Increased hepatic CD36 expression contributes to dyslipidemia associated with diet-induced obe-sity. Diabetes 2007, 56(12):2863-2871.
51. Coleman RA, Lewin TM, Muoio DM: Physiological and nutri-tional regulation of enzymes of triacylglycerol synthesis. Annu Rev Nutr 2000, 20:77-103.
52. Parkes HA, Preston E, Wilks D, Ballesteros M, Carpenter L, Wood L, Kraegen EW, Furler SM, Cooney GJ: Overexpression of acyl-CoA synthetase-1 increases lipid deposition in hepatic (HepG2) cells and rodent liver in vivo. Am J Physiol Endocrinol Metab 2006, 291(4):E737-744.
53. Ellis JM, Li LO, Wu PC, Koves TR, Ilkayeva O, Stevens RD, Watkins SM, Muoio DM, Coleman RA: Adipose acyl-CoA synthetase-1 directs fatty acids toward beta-oxidation and is required for cold thermogenesis. Cell Metab 2010, 12(1):53-64.
54. Blackburn C, Guan B, Brown J, Cullis C, Condon SM, Jenkins TJ, Peluso S, Ye Y, Gimeno RE, Punreddy S et al: Identification and characterization of 4-aryl-3,4-dihydropyrimidin-2(1H)-ones as inhibitors of the fatty acid transporter FATP4. Bioorg Med Chem Lett 2006, 16(13):3504-3509.
55. Ibrahimi A, Sfeir Z, Magharaie H, Amri EZ, Grimaldi P, Abumrad NA: Expression of the CD36 homolog (FAT) in fi-broblast cells: effects on fatty acid transport. Proc Natl Acad Sci U S A 1996, 93(7):2646-2651.
56. Febbraio M, Abumrad NA, Hajjar DP, Sharma K, Cheng W, Pearce SF, Silverstein RL: A null mutation in murine CD36 re-veals an important role in fatty acid and lipoprotein metabo-lism. J Biol Chem 1999, 274(27):19055-19062.
57. Bieghs V, Wouters K, van Gorp PJ, Gijbels MJ, de Winther MP, Binder CJ, Lutjohann D, Febbraio M, Moore KJ, van Bilsen M, et al: Role of scavenger receptor A and CD36 in diet-induced nonalcoholic steatohepatitis in hyperlipidemic mice. Gastroenterology 2010, 138(7):2477-2486.