Different functions of intestinal and liver-type fatty acid-binding proteins in intestine and in whole body energy homeostasis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 300, Issue 5, 2011, Pages

  Lagakos, William Stacy ^a,d   Gajda, Angela Marie ^a,d   Agellon, Luis ^b   Binas, Bert ^c   Choi, Victor ^a   Mandap, Bernadette ^a   Russnak, Timothy ^a   Zhou, Yin Xiu ^a   Storch, Judith ^a,d  

^a RUTGERS UNIVERSITY   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c Hanyang University   (South Korea)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

Chylomicron; Fatty acid; Gut; Lipid; Monoacylglycerol

Indexed keywords

FATTY ACID BINDING PROTEIN; MONOACYLGLYCEROL; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; INTESTINE; INTESTINE CELL; LIPID METABOLISM; LIPOGENESIS; LIVER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ANIMALS; BLOTTING, WESTERN; BODY COMPOSITION; BODY WEIGHT; EATING; ENERGY METABOLISM; ENTEROCYTES; FATTY ACID-BINDING PROTEINS; FATTY ACIDS; FECES; GENE EXPRESSION; GENOTYPE; HOMEOSTASIS; INTESTINAL MUCOSA; INTESTINES; LIPID METABOLISM; LIPIDS; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATION-REDUCTION;

EID: 79955559518     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00229.2010     Document Type: Article

References (50)

1. Agellon LB, Drozdowski L, Li L, Iordache C, Luong L, Clandinin MT, Uwiera RR, Toth MJ, Thomson AB. Loss of intestinal fatty acid binding protein increases the susceptibility of male mice to high fat diet-induced fatty liver. Biochim Biophys Acta 1771: 1283-1288, 2007.
2. Agellon LB, Li L, Luong L, Uwiera RR. Adaptations to the loss of intestinal fatty acid binding protein in mice. Mol Cell Biochem 284: 159-166, 2006.
3. Agellon LB, Toth MJ, Thomson AB. Intracellular lipid binding proteins of the small intestine. Mol Cell Biochem 239: 79-82, 2002.
4. Alpers DH, Bass NM, Engle MJ, DeSchryver-Kecskemeti K. Intestinal fatty acid binding protein may favor differential apical fatty acid binding in the intestine. Biochim Biophys Acta 1483: 352-362, 2000.
5. Alvaro A, Rosales R, Masana L, Vallve JC. Polyunsaturated fatty acids down-regulate in vitro expression of the key intestinal cholesterol absorption protein NPC1L1: no effect of monounsaturated nor saturated fatty acids. J Nutr Biochem 21: 518-525, 2010.
6. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
7. Chon SH, Zhou YX, Dixon JL, Storch J. Intestinal monoacylglycerol metabolism: developmental and nutritional regulation of monoacylglycerol lipase and monoacylglycerol acyltransferase. J Biol Chem 282: 33346-33357, 2007.
8. Drozdowski L, Clement L, Keelan M, Niot I, Clandinin MT, Agellon L, Wild G, Besnard P, Thomson AB. Dietary lipids modify intestinal lipid-binding protein RNA abundance in diabetic and control rats. Digestion 70: 192-198, 2004.
9. Erol E, Kumar LS, Cline GW, Shulman GI, Kelly DP, Binas B. Liver fatty acid binding protein is required for high rates of hepatic fatty acid oxidation but not for the action of PPARalpha in fasting mice. FASEB J 18: 347-349, 2004.
10. Fan YK, Croom WJ Jr, Eisen EJ, Daniel LR, Black BL, McBride BW. Selection for growth does not affect apparent energetic efficiency of jejunal glucose uptake in mice. J Nutr 126: 2851-2860, 1996.
11. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509, 1957.
12. Gangl A, Ockner RK. Intestinal metabolism of plasma free fatty acids. Intracellular compartmentation and mechanisms of control. J Clin Invest 55: 803-813, 1975.
13. Gordon JI, Elshourbagy N, Lowe JB, Liao WS, Alpers DH, Taylor JM. Tissue specific expression and developmental regulation of two genes coding for rat fatty acid binding proteins. J Biol Chem 260: 1995-1998, 1985.
14. Hsu KT, Storch J. Fatty acid transfer from liver and intestinal fatty acid-binding proteins to membranes occurs by different mechanisms. J Biol Chem 271: 13317-13323, 1996.
15. Lehner R, Kuksis A. Biosynthesis of triacylglycerols. Prog Lipid Res 35: 169-201, 1996.
16. Luxon BA, Milliano MT. Cytoplasmic transport of fatty acids in rat enterocytes: role of binding to fatty acid-binding protein. Am J Physiol Gastrointest Liver Physiol 277: G361-G366, 1999.
17. Mansbach CM 2nd. The origin of chylomicron phosphatidylcholine in the rat. J Clin Invest 60: 411-420, 1977.
18. Mansbach CM 2nd, Dowell RF. Uptake and metabolism of circulating fatty acids by rat intestine. Am J Physiol Gastrointest Liver Physiol 263: G927-G933, 1992.
19. Martin GG, Atshaves BP, McIntosh AL, Mackie JT, Kier AB, Schroeder F. Liver fatty-acid-binding protein (L-FABP) gene ablation alters liver bile acid metabolism in male mice. Biochem J 391: 549-560, 2005.
20. Martin GG, Atshaves BP, McIntosh AL, Mackie JT, Kier AB, Schroeder F. Liver fatty acid binding protein gene ablation potentiates hepatic cholesterol accumulation in cholesterol-fed female mice. Am J Physiol Gastrointest Liver Physiol 290: G36-G48, 2006.
21. Martin GG, Atshaves BP, McIntosh AL, Payne HR, Mackie JT, Kier AB, Schroeder F. Liver fatty acid binding protein gene ablation enhances age-dependent weight gain in male mice. Mol Cell Biochem 324: 101-115, 2009.
22. Martin GG, Danneberg H, Kumar LS, Atshaves BP, Erol E, Bader M, Schroeder F, Binas B. Decreased liver fatty acid binding capacity and altered liver lipid distribution in mice lacking the liver fatty acid-binding protein gene. J Biol Chem 278: 21429-21438, 2003.
23. Mathur SN, Watt KR, Field FJ. Regulation of intestinal NPC1L1 expression by dietary fish oil and docosahexaenoic acid. J Lipid Res 48: 395-404, 2007.
24. Murphy EJ. L-FABP and I-FABP expression increase NBD-stearate uptake and cytoplasmic diffusion in L cells. Am J Physiol Gastrointest Liver Physiol 275: G244-G249, 1998.
25. Nassir F, Wilson B, Han X, Gross RW, Abumrad NA. CD36 is important for fatty acid and cholesterol uptake by the proximal but not distal intestine. J Biol Chem 282: 19493-19501, 2007.
26. Neeli I, Siddiqi SA, Siddiqi S, Mahan J, Lagakos WS, Binas B, Gheyi T, Storch J, Mansbach CM 2nd. Liver fatty acid-binding protein initiates budding of pre-chylomicron transport vesicles from intestinal endoplasmic reticulum. J Biol Chem 282: 17974-17984, 2007.
27. Newberry EP, Kennedy SM, Xie Y, Sternard BT, Luo J, Davidson NO. Diet-induced obesity and hepatic steatosis in L-Fabp-/-mice is abrogated with SF, but not PUFA, feeding and attenuated after cholesterol supplementation. Am J Physiol Gastrointest Liver Physiol 294: G307-G314, 2008.
28. Newberry EP, Xie Y, Kennedy S, Han X, Buhman KK, Luo J, Gross RW, Davidson NO. Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acidbinding protein gene. J Biol Chem 278: 51664-51672, 2003.
29. Newberry EP, Xie Y, Kennedy SM, Luo J, Davidson NO. Protection against Western diet-induced obesity and hepatic steatosis in liver fatty acid-binding protein knockout mice. Hepatology 44: 1191-1205, 2006.
30. Ockner RK, Manning JA. Fatty acid-binding protein in small intestine. Identification, isolation, and evidence for its role in cellular fatty acid transport. J Clin Invest 54: 326-338, 1974.
31. Ockner RK, Manning JA. Fatty acid binding protein. Role in esterification of absorbed long chain fatty acid in rat intestine. J Clin Invest 58: 632-641, 1976.
32. Oxley A, Jutfelt F, Sundell K, Olsen RE. sn-2-Monoacylglycerol, not glycerol, is preferentially utilised for triacylglycerol and phosphatidylcholine biosynthesis in Atlantic salmon (Salmo salar L.) intestine. Comp Biochem Physiol B Biochem Mol Biol 146: 115-123, 2007.
33. Petit V, Arnould L, Martin P, Monnot MC, Pineau T, Besnard P, Niot I. Chronic high-fat diet affects intestinal fat absorption and postprandial triglyceride levels in the mouse. J Lipid Res 48: 278-287, 2007.
34. Phan CT, Tso P. Intestinal lipid absorption and transport. Front Biosci 6: D299-D319, 2001.
35. Prows DR, Murphy EJ, Moncecchi D, Schroeder F. Intestinal fatty acid-binding protein expression stimulates fibroblast fatty acid esterification. Chem Phys Lipids 84: 47-56, 1996.
36. Prows DR, Murphy EJ, Schroeder F. Intestinal and liver fatty acid binding proteins differentially affect fatty acid uptake and esterification in L-cells. Lipids 30: 907-910, 1995.
37. Richieri GV, Ogata RT, Kleinfeld AM. Equilibrium constants for the binding of fatty acids with fatty acid-binding proteins from adipocyte, intestine, heart, and liver measured with the fluorescent probe ADIFAB. J Biol Chem 269: 23918-23930, 1994.
38. Richieri GV, Ogata RT, Zimmerman AW, Veerkamp JH, Kleinfeld AM. Fatty acid binding proteins from different tissues show distinct patterns of fatty acid interactions. Biochemistry 39: 7197-7204, 2000.
39. Scow RO, Stein Y, Stein O. Incorporation of dietary lecithin and lysolecithin into lymph chylomicrons in the rat. J Biol Chem 242: 4919-4924, 1967.
40. Shi Y, Cheng D. Beyond triglyceride synthesis: the dynamic functional roles of MGAT and DGAT enzymes in energy metabolism. Am J Physiol Endocrinol Metab 297: E10-E18, 2009.
41. Storch J. Diversity of fatty acid-binding protein structure and function: studies with fluorescent ligands. Mol Cell Biochem 123: 45-53, 1993.
42. Storch J, Corsico B. The emerging functions and mechanisms of mammalian fatty acid-binding proteins. Annu Rev Nutr 28: 73-95, 2008.
43. Storch J, Veerkamp JH, Hsu KT. Similar mechanisms of fatty acid transfer from human anal rodent fatty acid-binding proteins to membranes: liver, intestine, heart muscle, and adipose tissue FABPs. Mol Cell Biochem 239: 25-33, 2002.
44. Storch J, Zhou YX, Lagakos WS. Metabolism of apical versus basolateral sn-2-monoacylglycerol and fatty acids in rodent small intestine. J Lipid Res 49: 1762-1769, 2008.
45. Thumser AE, Storch J. Liver and intestinal fatty acid-binding proteins obtain fatty acids from phospholipid membranes by different mechanisms. J Lipid Res 41: 647-656, 2000.
46. Trotter PJ, Storch J. Fatty acid uptake and metabolism in a human intestinal cell line (Caco-2): comparison of apical and basolateral incubation. J Lipid Res 32: 293-304, 1991.
47. Vassileva G, Huwyler L, Poirier K, Agellon LB, Toth MJ. The intestinal fatty acid binding protein is not essential for dietary fat absorption in mice. FASEB J 14: 2040-2046, 2000.
48. Veerkamp JH, van Moerkerk HT. Peroxisomal fatty acid oxidation in rat and human tissues. Effect of nutritional state, clofibrate treatment and postnatal development in the rat. Biochim Biophys Acta 875: 301-310, 1986.
49. Watford M, Lund P, Krebs HA. Isolation and metabolic characteristics of rat and chicken enterocytes. Biochem J 178: 589-596, 1979.
50. Windmueller HG, Spaeth AE. Identification of ketone bodies and glutamine as the major respiratory fuels in vivo for postabsorptive rat small intestine. J Biol Chem 253: 69-76, 1978.