Trans-membrane uptake and intracellular metabolism of fatty acids in Atlantic salmon (Salmo salar L.) hepatocytes

Lipids

Volumn 45, Issue 4, 2010, Pages 301-311

  Zhou, Jishu ^a,b   Stubhaug, Ingunn ^b,c   Torstensen, Bente E ^b  

^a NORTHWEST A F UNIVERSITY   (China)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

^c CEMAGREF   (France)

Author keywords

Atlantic salmon; Fatty acid; Fatty acid binding protein in plasma membrane (FABPpm); Fatty acid translocase (FAT CD36); Fatty acid transport protein (FATP); Hepatocytes; Inhibitors; Passive diffusion; Trans membrane uptake; Transport

Indexed keywords

CARBON 14; DOCOSAPENTAENOIC ACID; ICOSAPENTAENOIC ACID; LINOLEIC ACID; OLEIC ACID; PHLORETIN;

ANIMAL CELL; ARTICLE; ATLANTIC SALMON; CELL MEMBRANE TRANSPORT; CELL METABOLISM; CHEMICAL LABELING; CONCENTRATION PROCESS; CONTROLLED STUDY; CULTURE OPTIMIZATION; FATTY ACID DESATURATION; FATTY ACID METABOLISM; FATTY ACID TRANSPORT; IN VITRO STUDY; INCUBATION TIME; LIVER CELL MEMBRANE; NONHUMAN; PASSIVE TRANSPORT; PROTEIN LIPID INTERACTION; TRANSPORT KINETICS;

ALPHA-LINOLENIC ACID; ANIMALS; CELL MEMBRANE; CELL SURVIVAL; FATTY ACIDS; FISH OILS; HEPATOCYTES; INTRACELLULAR SPACE; LIPID METABOLISM; METABOLISM; PLANT OILS; SALMO SALAR; TIME FACTORS;

SALMO SALAR;

EID: 77953292457     PISSN: 00244201     EISSN: 15589307     Source Type: Journal    
DOI: 10.1007/s11745-010-3396-1     Document Type: Article

References (59)

1. Jump DB (2004) Fatty acid regulation of gene transcription. Crit Rev Clin Lab Sci 41:41-78
2. Van der Vusse GJ, Glatz JFC, Stam HCG, Reneman RS (1992) Fatty acid nomeostasis in the normoxic and ischemic heart. Physiol Rev 72:881-940
3. Degrella RD, Light RJ (1980) Uptake and metabolism of fatty acids by dispersed adult rat heart myocytes. J Biol Chem 255:9739-9745
4. Hamilton JA (1998) Fatty acid transport: Difficult or easy? J Lipid Res 39:467-481
5. Hamilton JA, Kamp F (1999) How are free fatty acids transported in membranes? Diabetes 48:2255-2269
6. Hamilton JA, Johnson RA, Corkey B, Kamp F (2001) Fatty acid transport: The diffusion mechanism in model and biological membranes. J Mol Neurosci 16:99-108
7. Hamilton JA, Guo W, Kamp F (2002) Mechanisms of cellular uptake of long-chain fatty acids: Do we need cellular proteins? Mol Cell Biochem 239:17-23
8. Pownall HJ, Hamilton JA (2003) Energy translocation across cell membranes and membranemodels. Acta Physiol Scand 178:357-365
9. Kamp F, Guo W, Souto R, Pilch PF, Corkey BE, Hamilton JA (2003) Rapid flip-flop of oleic acid across the plasma membrane of adipocytes. J Biol Chem 278:7988-7995
10. Hamilton JA, Brunaldi K (2007) A model for fatty acid transport into the brain. J Mol Neurosci 33:12-17
11. Kampf JP, Kleinfeld AM (2004) Fatty acid transport in adipocytes monitored by imaging intracellular free fatty acid levels. J Biol Chem 279:35775-35780
12. Stremmel W, Strohmeyer G, Berk PD (1986) Hepatocellular uptake of oleate is energy dependent, sodium linked, and inhibited by an antibody to hepatocyte plasma membrane fatty acid binding protein. Proc Natl Acad Sci USA 83:3584-3588
13. Gimeno RE, Ortegon AM, Patel S, Punreddy S, Ge P, Sun Y, Lodish HF, Stahl A (2003) Characterization of a heart-specific fatty acid transport protein. J Biol Chem 278:16039-16044
14. Hirsch D, Stahl A, Lodish HF (1998) A family of fatty acid transporters conserved from Mycobacterium to man. Proc Natl Acad Sci USA 95:8625-8629
15. Schaffer JE, Lodish HF (1994) Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79:427-436
16. Schwieterman W, Sorrentino D, Potter BJ, Rand J, Kiang CL, Stump D, Berk PD (1988) Uptake of oleate by isolated rat adipocytes is mediated by a 40-kDa plasma membrane fatty acid binding protein closely related to that in liver and gut. Proc Natl Acad Sci USA 85:359-363
17. Stremmel W, Strohmeyer G, Borchard F, Kochwa S, Berk PD (1985) Isolation and partial characterization of a fatty acid binding protein in rat liver plasma membranes. Proc Natl Acad Sci USA 82:4-8
18. Abumrad NA, El-Maghrabi MR, Amri EZ, Lopez E, Grimaldi P (1993) 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 268:17665-17668
19. Jennings ML, Solomon AK (1976) Interaction between phloretin and the red blood cell membrane. J Gen Physiol 67:381-397
20. Coort SLM, Willems J, Coumans WA, van der Vusse GJ, Bonen A, Glatz JFC, Luiken JJFP (2002) Sulfo-N-succinimidyl esters of long chain fatty acids specifically inhibit fatty acid translocase (FAT/CD36)-mediated cellular fatty acid uptake. Mol Cell Biochem 239:213-219
21. Bonen A, Luiden JJFP, Liu S, Dyck DJ, Kiens B, Kristiansen S, Turcotte LP, Van der Vusse GJ, Glatz JFC (1998) Palmitate transport and fatty acid transporters in red and white muscles. Am J Physiol 275:E471-E478
22. Luiken JJFP, Turcotte LP, Bonen A (1999) Protein-mediated palmitate uptake and expression of fatty acid transport proteins in heart giant vesicles. J Lipid Res 40:1007-1016
23. Pohl J, Ring A, Korkmaz U, Ehehalt R, Stremmel W (2005) FAT/ CD36-mediated long-chain fatty acid uptake in adipocytes requires plasma membrane rafts. Mol Biol Cell 16:24-31
24. Abumrad NA, Park JH, Park CR (1984) Permeation of long-chain fatty acid into adipocytes. J Biol Chem 259:8945-8953
25. Richards JG, Bonen A, Heigenhauser GJF, Wood CM (2004) Palmitate movement across red and white muscle membranes of rainbow trout. Am J Physiol Regul Integr Comp Physiol 286:R46-R53
26. Ehehalt R, Sparla R, Kulaksiz H, Herrmann T, Fullekrug J, Stremmel W (2008) Uptake of long chain fatty acids is regulated by dynamic interaction of FAT/CD36 with cholesterol/sphingolipid enriched microdomains (lipid raft). BMC Cell Biol 9:45. doi:10.1186/1471-2121-9-45
27. Stubhaug I, Tocher DR, Bell JG, Dick JR, Torstensen BE (2005) Fatty acid metabolism in Atlantic salmon (Salmo salar L.) hepatocytes and influence of dietary vegetable oil. Biochim Biophys Acta 1734:277-288
28. Torstensen BE, Nanton DA, Olsvik PA, Sundvold H, Stubhaug I (2009) Gene expression of fatty acid-binding proteins, fatty acid transport proteins (cd36 and FATP) and β-oxidation-related genes in (Salmo salar L.) fed fish oil or vegetable oil.AquacNutr 15:440-451
29. Harmon CM, Luce P, Beth AH, Abumrad NA (1991) Labeling of adipocyte membranes by sulfo-N-succinimidyl derivatives of long-chain fatty acids: Inhibition of fatty acid transport. J Membr Biol 121:261-268
30. Staros JV (1982) N-Hydroxysulfosuccinimide active esters: Bis (N-hydroxysulfosuccinimide) esters of two dicarboxylic acids are hydrophilic, membrane-impermeant, protein cross-linkers. J Biochem 21:3950-3955
31. Dannevig BH, Berg T (1985) Endocytosis of galactose-terminated glycoproteins by isolated liver cells of the rainbow trout (Salmo gairdneri). Comp Biochem Physiol B 82:683-688
32. Ghioni C, Taher DR, Sargent JR (1997) The effect of culture on morphology, lipid and fatty acid composition, and polyunsaturated fatty acid metabolism of rainbow trout (Oncorhynchus mykiss) skin cells. Fish Physiol Biochem 16:499-513
33. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497-509
34. Tocher DR, Fonseca-Madrigal J, Bell JG, Dick JR, Henderson RJ, Sargent JR (2002) Effects of diets containing linseed oil on fatty acid desaturation and oxidation in hepatocytes and intestinal enterocytes in Atlantic salmon (Salmo salar). Fish Physiol Biochem 26:157-170
35. Ruyter B, Roesjoe C, Maesoeval K, Einen O, Thomassen MS (2000) Influence of dietary n-3 fatty acids on the desaturation and elongation of [1-super(14)C] 18:2 n-6 and [1-super(14)C] 18:3 n-3 in Atlantic salmon hepatocytes. Fish Physiol Biochem 23:151-158
36. Tocher DR, Bell JG, Dick JR, Crampton VO (2003) Effects of dietary vegetable oil on Atlantic salmon hepatocyte fatty acid desaturation and liver fatty acid compositions. Lipids 38:723-732
37. Torstensen BE, Stubhaug I (2004) Beta-oxidation of 18:3n-3 in Atlantic salmon (Salmo salar L.) hepatocytes treated with different fatty acids. Lipids 39:1-8
38. Vegusdal A, Gjøen T, Berge RK, Thomassen MS, Ruyter B (2005) Effect of 18:1n-9, 20:5n-3 and 22:6n-3 on lipid accumulation and secretion by Atlantic salmon hepatocytes. Lipids 40:477-486
39. Mashek DG, Coleman RA (2006) Cellular fatty acid uptake: The contribution of metabolism. Curr Opin Lipidol 17:274-278
40. Sorrentino D, Robinson RB, Kiang CL, Berk PD (1989) At physiological albumin/oleate concentrations oleate uptake by isolated hepatocytes, cardiac myocytes and adipocytes is a saturable function of the unbound oleate concentration. Uptake kinetics are consistent with the conventional theory. J Clin Invest 84:1325-1333
41. Turcotte LP, Kiens B, Richter EA (1991) Saturation kinetics of palmitate uptake in perfused skeletal muscle. FEBS Lett 279:327-329
42. Abumrad NA, Perkins RC, Park JH, Park CR (1981) Mechanism of long chain fatty acid permeation in the isolated adipocyte. J Biol Chem 256:9183-9191
43. Sorrentino D, Stump D, Potter BJ, Robinson RB, White R, Kiang CL, Berk PD (1988) Oleate uptake by cardiac myocytes is carrier mediated and involves a 40-Kd plasma membrane fatty acid binding protein similar to that in liver, adipose tissue, and gut. J Clin Invest 82:928-935
44. 14 C] oleat reflects membrane transport rather than intracellular metabolism or binding. Proc Natl Acad Sci USA 83:3086-3090
45. Tocher DR, Carr J, Sargent JR (1989) Polyunsaturated fatty acid metabolism in fish cells: Differential metabolism of (n-3) and (n-6) series acids by cultured cells originating from a freshwater teleost fish and from a marine teleost fish. Comp Biochem Physiol 94B:367-374
46. Igal RA, Wang S, Gonzalez-Baro M, Coleman RA (2001) Mitochondrial glycerol phosphate acyltransferase directs incorporation of exogenous fatty acids into triacylglycerol. J Biol Chem 276:42205-42212
47. Rose H, Hennecke T, Kammermeier H (1990) Sarcolemmal fatty acid transfer in isolated cardiomyocytes governed by albumin/ membrane-lipid partition. J Mol Cell Cardiol 22:883-892
48. Zakim D (1996) Fatty acids enter cells by simple diffusion. Proc Soc Exp Biol Med 212:5-14
49. DeGrella RF, Light RJ (1980) Uptake and metabolism of fatty acids by dispersed adult rat heart myocytes. I. Kinetics of homologous fatty acids. J Biol Chem 255:9731-9738
50. Luiken JJFP, van Nieuwenhoven FA, America G, van der Vusse GJ, Glatz JFC (1997) Uptake and metabolism of palmitate by isolated cardiac myocytes from adult rats: Involvement of sarcolemmal proteins. J Lipid Res 38:745-758
51. Frohnert BI, Bernlohr DA (2000) Regulation of fatty acid transporters in mammalian cells. Prog Lipid Res 39:83-107
52. Stremmel W (1988) Fatty acid uptake by isolated rat heart myocytes represents a carrier mediated transport process. J Clin Invest 81:844-852
53. Lefevre PG (1975) The present state of the carrier hypothesis. Curr Top Membr Transp 7:109-215
54. Andersen BL, Tarpley HL, Regen DM (1978) Characterization of β-hydroxybutyrate transport in rat erythrocytes and thymocytes. Biochim Biophys Acta 508:525-538
55. Torstensen BE, Bell JG, Rosenlund G, Henderson RJ, Graff JE, Tocher DR, Lie O, Sargent JR (2005) Tailoring of Atlantic salmon (Salmo salar L.) flesh lipid composition and sensory quality by replacing fish oil with a vegetable oil blend. J Agric Food Chem 53:10166-10178
56. Bonen A, Chabowski A, Luiken JJFP, Glatz JFC (2007) Mechanisms and regulation of protein-mediated cellular fatty acid uptake: Molecular, biochemical, and physiological evidence. Physiol 22:15-28
57. Chabowski A, Gorski J, Luiken JJP, Glatz JFC, Bonen A (2007) Evidence for concerted action of FAT/CD36 and FABPpm to increase fatty acid transport across the plasma membrane. Prostagland Leukot Essent Fatty acids 77:345-353
58. Ikonen E (2001) Roles of lipid rafts in membrane transport. Cell Biol 13:470-477
59. Storch J, Thumser AEA (2000) The fatty acid transport function of fatty acid-binding proteins. Biochim Biophys Acta 1486:28-44