FABP-1 gene ablation impacts brain endocannabinoid system in male mice

Journal of Neurochemistry

Volumn , Issue , 2016, Pages 407-422

  Martin, Gregory G ^a   Chung, Sarah ^a,b   Landrock, Danilo ^b   Landrock, Kerstin K ^b   Huang, Huan ^a   Dangott, Lawrence J ^b   Peng, Xiaoxue ^c   Kaczocha, Martin ^c   Seeger, Drew R ^d   Murphy, Eric J ^d   Golovko, Mikhail Y ^d   Kier, Ann B ^b   Schroeder, Friedhelm ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

brain; endocannabinoid; gene ablation; liver fatty acid binding protein; mouse

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ANANDAMIDE; ARACHIDONIC ACID; CANNABINOID RECEPTOR; FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 3; FATTY ACID BINDING PROTEIN 5; FATTY ACID BINDING PROTEIN 7; HEAT SHOCK PROTEIN 70; N OLEOYLETHANOLAMINE; PHOSPHOLIPID; STEROL CARRIER PROTEIN 2; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BRAIN LEVEL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ESTERIFICATION; LIPID ANALYSIS; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; UPREGULATION;

EID: 84979539124     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13664     Document Type: Article

References (144)

1. Alswat K. A. (2015) The role of endocannabinoid system in fatty liver disease and therapeutic potential. Saudi J. Gastroenterol. 19, 144–151.
2. Ashton C. H. (2001) Pharmacology and effects of cannabis: a brief review. Br. J. Psychiatry 178, 101–106.
3. Atshaves B. P., Petrescu A., Starodub O., Roths J., Kier A. B. and Schroeder F. (1999) Expression and intracellular processing of the 58 kDa sterol carrier protein 2/3-oxoacyl-CoA thiolase in transfected mouse L-cell fibroblasts. J. Lipid Res. 40, 610–622.
4. Atshaves B. P., McIntosh A. L., Lyuksyutova O. I., Zipfel W. R., Webb W. W. and Schroeder F. (2004a) Liver fatty acid binding protein gene ablation inhibits branched-chain fatty acid metabolism in cultured primary hepatocytes. J. Biol. Chem. 279, 30954–30965.
5. Atshaves B. P., Payne H. R., McIntosh A. L., Tichy S. E., Russell D., Kier A. B. and Schroeder F. (2004b) Sexually dimorphic metabolism of branched chain lipids in C57BL/6J mice. J. Lipid Res. 45, 812–830.
6. Atshaves B. P., McIntosh A. L., Payne H. R., Mackie J., Kier A. B. and Schroeder F. (2005) Effect of branched-chain fatty acid on lipid dynamics in mice lacking liver fatty acid binding protein gene. Am. J. Physiol. 288, C543–C558.
7. Atshaves B. P., McIntosh A. L., Landrock D., Payne H. R., Mackie J., Maeda N., Ball J. M., Schroeder F. and Kier A. B. (2007a) Effect of SCP-x gene ablation on branched-chain fatty acid metabolism. Am. J. Physiol. 292, 939–951.
8. Atshaves B. P., McIntosh A. L., Payne H. R., Gallegos A. M., Landrock K., Maeda N., Kier A. B. and Schroeder F. (2007b) Sterol carrier protein-2/sterol carrier protein-x gene ablation alters lipid raft domains in primary cultured mouse hepatocytes. J. Lipid Res. 48, 2193–2211.
9. Atshaves B. P., McIntosh A. L., Martin G. G. et al. (2009) Overexpression of sterol carrier protein-2 differentially alters hepatic cholesterol accumulation in cholesterol-fed mice. J. Lipid Res. 50, 1429–1447.
10. Atshaves B. P., Martin G. G., Hostetler H. A., McIntosh A. L., Kier A. B. and Schroeder F. (2010) Liver fatty acid binding protein (L-FABP) and Dietary Obesity. J. Nut. Bioche. 21, 1015–1032.
11. Avdulov N. A., Chochina S. V., Myers-Payne S., Hubbell T., Igbavboa U., Schroeder F. and Wood W. G. (1998) Expression and lipid binding of sterol carrier protein-2 and liver fatty acid binding proteins: differential effects of ethanol in vivo and in vitro, in Essential Fatty Acids and Eicosanoids: Invited Papers from the Fourth International Congress (Riemersma R. A., Armstrong R., Kelly R. W. and Wilson R., eds), pp. 324–327. American Oil Chemists Society Press, Champaign, IL.
12. Baumgardner J. N., Shankar K., Hennings L., Badger T. M. and Ronis M. J. J. (2007) A new model for nonalcoholic steatohepatitis in the rat utilizing total enteral nutrition to overfeed a high-polyunsaturated fat diet. Am. J. Physiol. Gastrointest. Liver Phys. 294, G27–G38.
13. Bazinet R. P. and Laye S. (2014) PUFA and their metabolites in brain function and disease. Nat. Rev. Neurosci. 15, 771–785.
14. Bennett E., Stenvers K. L., Lund P. K. and Popko B. (1994) Cloning and characterization of a cDNA encoding a novel fatty acid binding protein from rat brain. J. Neurochem. 63, 1616–1624.
15. Ben-Shabat S., Fride E., Sheskin T., et al. (1998) An entoruage effects: inactive endogenous fatty acid glycerol esters enhance 2-arachidonoyl-glycerol cannabinoid activity. Eur. J. Pharm. 353, 23–31.
16. Berger W. T., Ralph B. P., Kaczocha M., Sun J., Balius T. E., Rizzo R. C., Haj-Dahmane S., Ojima I. and Deutsch D. G. (2012) Targeting FABP anandamide transporters–a novel strategy for development of anti-inflammatory and anti-nociceptive drugs. PLoS ONE 7, e50968.
17. Blankman J. L., Simon G. M. and Cravatt B. F. (2007) Comprehensive profile of brain enzymes that hydrolyze endocannabinoid 2-arachidonoylglycerol. Chem. Biol. 14, 1347–1356.
18. Bradford M. (1976) 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.
19. Brose S. A. and Golovko M. Y. (2013) Eicosanoid post-mortem induction in kidney tissue is prevented by microwave irradiation. Prost. Leukot. Essen. Fatty Acids 89, 313–318.
20. Brose S., Baker A. and Golovko M. Y. (2013) A fast one-step extraction and UPLC-MS/MS Analysis for E2/D2 series prostaglandins and isoprostanes. Lipids 48, 411–419.
21. Chao H., Zhou M., McIntosh A., Schroeder F. and Kier A. B. (2003) Acyl CoA binding protein and cholesterol differentially alter fatty acyl CoA utilization by microsomal acyl CoA: cholesterol transferase. J. Lipid Res. 44, 72–83.
22. Charlton M., Viker K., Krishnan A. et al. (2009) Differential expression of lumican and fatty acid binding protein-1: new insights into the histologic spectrum of nonalcoholic fatty liver disease. Hepatology 49, 1375–1384.
23. Chen C. T., Domenichiello A. F., Trepanier M.-O., Liu Z., Masoodi M. and Bazinet R. P. (2013) Low levels of EPA in rat brain phospholipids are maintained via multiple redundant mechanisms. J. Lipid Res. 54, 2422.
24. Christie M. J. and Mallet C. (2009) Endocannabinoids can open the pain gate. Sciencesignaling 2, pe57.
25. Craft R. M., Marusich J. A. and Wiley J. L. (2013) Sex differences in cannabinoid pharmacology: a reflection of differences in endocannabinoid system? Life Sci. 92, 476–481.
26. D'Addario C., Di Francesco A., Pucci M., Agro A. F. and Maccarrone M. (2013) Epigenetic mechanisms and endocannabinoid signaling. FEBS J. 280, 1905–1917.
27. Dai R. and Ansar Ahmed S. (2014) Sexual dimorphism of miRNA expression: a new perspective in understanding the sex bias of autoimmune disease. Ther. Clin. Risk Manag. 10, 151–163.
28. De Petrocellis L., Melck D., Bisogno T. and Di Marzo V. (2000) Endocannabinoids and fatty acid amides in cancer, inflammation, and related disorders. Chem. Phys. Lip. 108, 191–209.
29. Di Marzo V., Bisogno T., Sugiura T., et al. (1998) The novel endogenous cannabinoid 2-AG is inactivated by neuronal- and basophil-like cells: connections with anandamide. Biochem. J. 331, 15–19.
30. Ellinghaus P., Wolfrum C., Assmann G., Spener F. and Seedorf U. (1999) Phytanic acid activates the peroxisome proliferator-activated receptor alpha (PPARalpha) in sterol carrier protein-2-/sterol carrier protein x-deficient mice. J. Biol. Chem. 274, 2766–2772.
31. Elmes M. W., Kaczocha M., Berger W. T. et al. (2015) Fatty acid binding proteins are intracellular carriers for delta-9-tetrahydrocannabinol (THC) and cannabidiol (CBD). J. Biol. Chem. 290, 8711–8721.
32. Erol E., Kumar L. S., Cline G. W., Shulman G. I., Kelly D. P. and Binas B. (2004) Liver fatty acid-binding protein is required for high rates of hepatic fatty acid oxidation but not for the action of PPAR-a in fasting mice. FASEB J. 18, 347–349.
33. Favretto F., Assfalg M., Gallo M., Cicero D. O., D'Onofrio M. and Molinari H. (2013) Ligand binding promiscuity and human liver fatty acid binding protein: structural and dynamic insights from an interaction study with glycocholate and oleate. ChemBioChem 14, 1807–1819.
34. Feng L., Hatten M. E. and Heintz N. (1994) Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12, 895–908.
35. Fine P. G. and Rosenfeld M. J. (2013) The endocannabinoid system, cannabinoids, and pain. Rambam Maimonides Med. J. 4, e0022.
36. Fowler C. J. (2013) Transport of endocannabinoids across plasma membrane and within the cell. FEBS J. 280, 1895–1904.
37. Franklin A., Parmentier-Batteur S., Walter L., Greenbert D. A. and Stella N. (2003) Palmitoylethanolamide increases after focal cerebral ischemia and potentiates microglial cell motility. J. Neurosci. 23, 7767–7775.
38. Frolov A. A. and Schroeder F. (1998) Acyl coenzyme A binding protein: conformational sensitivity to long chain fatty acyl-CoA. J. Biol. Chem. 273, 11049–11055.
39. Frolov A., Cho T. H., Billheimer J. T. and Schroeder F. (1996) Sterol carrier protein-2, a new fatty acyl coenzyme A-binding protein. J. Biol. Chem. 271, 31878–31884.
40. Frolov A., Cho T. H., Murphy E. J. and Schroeder F. (1997) Isoforms of rat liver fatty acid binding protein differ in structure and affinity for fatty acids and fatty acyl CoAs. Biochemistry 36, 6545–6555.
41. Fu J., Oveisi F., Gaetani S., Lin E. and Piomelli D. (2005) Oleoylethanolamine, an endogenous PPAR-a agonist, lowers body weight and hyperlipidemia in obese rats. Neuropharmacology 48, 1153.
42. Fuchs M., Hafer A., Muench C., Kannenberg F., Teichmann S., Scheibner J., Stange E. F. and Seedorf U. (2001) Disruption of the sterol carrier protein 2 gene in mice impairs biliary lipid and hepatic cholesterol metabolism. J. Biol. Chem. 276, 48058–48065.
43. Gajda A. M. and Storch J. (2015) Enterocyte fatty acid binding proteins (FABPs): different functions of liver and intestinal FABPs in the intestine. Prost. Leukot. Essen. Fatty Acids 93, 9–15.
44. Gonzalez S., Bisogno T., Wenger T., et al. (2000) Sex steroid influence on CB1 receptor mRNA and endocannabinoid levels in anterior pituitary gland. Biochem. Biophy. Res. Comm. 270, 260–266.
45. Goparaju S. K., Ueda N., Yamaguchi H. and Yamamoto S. (1989) Anandamide amidohydrolase reacting with 2-AG, another cannabinoid receptor ligand. FEBS Lett. 422, 69–73.
46. Grotenhermen F. (2003) Clin. Pharmacokinet. 42, 327–360.
47. Guasti L., Richardson D., Jhaveri M., et al. (2009) Minocycline treatment inhibits microglial activation and alters spinal levels of endocannabinoids in a rat model of neuropathic pain. Mol. Pain. 5, 1–10.
48. Gyamfi M. A., He L., French S. W., Damjanov I. and Wan Y.-J. Y. (2008) Hepatocyte retinoid X receptor alpha-dependent regulation of lipid homeostasis and inflammatory cytokine expression contributes to alcohol-induced liver injury. J. Pharm. Exp. Ther. 324, 443–453.
49. Hanhoff T., Wolfrum C., Ellinghaus P., Seedorf U. and Spener F. (2001) Pristanic acid is activator of PPARalpha. Eur. J. Lipid Sci. 103, 75–80.
50. Hanhoff T., Benjamin S., Borchers T. and Spener F. (2005) Branched-chain fatty acids as activators of peroxisome proliferators. Eur. J. Lip. Sci. Technol. 107, 716–729.
51. Havel R. J., Felts J. M. and Van Duyne C. M. (1962) Formation and fate of endogenous triglycerides in blood plasma of rabbits. J. Lipid Res. 3, 297–308.
52. Higuchi N., Kato M., Tanaka M., et al. (2011) Effects of insulin resistance and hepatic lipid accumulation on hepatic mRNA expression levels of apoB, MTP, and L-FABP in non-alcoholic fatty liver disease. Exp. Ther. Med. 2, 1077–1081.
53. Ho W. S. V. and Barrett D. A. R. (2008) Entourage effects of N-palmitoylethanolamide and N-oleoylethanolamide on vasorelaxaton to anandamide occur through TRPV1 receptors. Br. J. Pharmacol. 155, 837–846.
54. Huang H., Atshaves B. P., Frolov A., Kier A. B. and Schroeder F. (2005) Acyl-coenzyme A binding protein expression alters liver fatty acyl coenzyme A metabolism. Biochemistry 44, 10282–10297.
55. Huang H., McIntosh A. L., Martin G. G., Petrescu A. D., Landrock K., Landrock D., Kier A. B. and Schroeder F. (2013) Inhibitors of fatty acid synthesis induce PPARa-regulated fatty acid b-oxidative enzymes: synergistic roles of L-FABP and glucose. PPAR Res. 2013, 1–22.
56. Huang H., McIntosh A. L., Martin G. G., Landrock K., Landrock D., Gupta S., Atshaves B. P., Kier A. B. and Schroeder F. (2014) Structural and functional interaction of fatty acids with human liver fatty acid binding protein (L-FABP) T94A variant. FEBS J. 281, 2266–2283.
57. Huestis M. A. (2007) Human cannabinoid pharmacokinetics. Chem. Biodivers. 4, 1770–1804.
58. Ignatowska-Jankowska B. M., Ghosh S., Crowe M. S., et al. (2014) In vivo characterization of the highly selective inhibitor KML29: antinociceptive activity without cannabimimetic side effects. Br. J. Pharmacol. 171, 1392–1407.
59. Jackson A. R., Nagarkatti P. and Nagarkatti M. (2014) Anandamide attenuates Th-17 cell-mediated delayed type hypersensitivity response by triggering IL-10 production and consequent miRNA induction. PLoS ONE 9, e93954.
60. Jian W., Edom R., Weng N., Zannikos P., Zhang Z. and Wang H. (2010) Validation and application of an LC-MS/MS method for quantitation of three fatty acid ethanolamides as biomarkers for fatty acid hydrolase inhibitionin human placenta. J. Chrom. B. 878, 1687–1699.
61. Kaczocha M. (2009) Role of fatty acid binding proteins and FAAH-2 in endocannabinoid uptake and inactivation. Ph. D. Thesis, Stony Brook University.
62. Kaczocha L. M., Glaser S. T. and Deutsch D. G. (2009) Identification of intracellular carriers for the endocannabinoid anandamide. Proc. Natl Acad. Sci. USA 106, 6375–6380.
63. Kaczocha M., Vivieca S., Sun J., Glaser S. T. and Deutsch D. G. (2012) Fatty acid binding proteins transport N-acylethanolamines to nuclear receptors and are targets of endocannabinoid transport inhibitors. J. Biol. Chem. 287, 3415–3424.
64. Kaczocha M., Rebecchi M. J., Ralph B. P. et al. (2014) Inhibition of fatty acid binding protein elevates brain anandamide levels and produces analgesia. PLoS ONE 9, e94200.
65. Kaczocha M., Glaser S. T., Maher T., Clavin B., Hamilton J., O'Rourke J., Rebecchi M., Puopolo M., Owada Y. and Thanos P. K. (2015) Fatty acid binding protein deletion suppresses inflammatory pain through endocannabinoid/N-acylethanolamine-dependent mechanisms. Mol. Pain. 11, 52.
66. Kohout M., Kohoutova B. and Heimberg M. (1971) The regulaton of hepatic triglyceride metabolism by free fatty acids. J. Biol. Chem. 246, 5067–5074.
67. Kurtz A., Zimmer A., Schnutgen F., Bruning G., Spener F. and Muller T. (1994) The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial cell development. Development 120, 2637–2649.
68. Lagakos W. S., Gajda A. M., Agellon L. B., Binas B., Choi V., Mandap B., Russnak T., Zhou Y. X. and Storch J. (2011) Different functions of intestinal and liver-type fatty acid binding proteins in intestine and in whole body energy homeostasis. Am. J. Physiol. Gastrointest. Liver Phys. 300, G803–G814.
69. Leung K., Elmes M. W., Glaser S. T., Deutsch D. G. and Kaczocha M. (2013) Role of FAAH-like anandamide transporter in anandamide inactivation. PLoS ONE 8, e79355.
70. Liedhegner E. S., Vogt C. D., Sem D. S., Cunninham C. W. and Hillard C. J. (2014) Sterol carrier protein-2: binding protein for endocannabinoids. Mol. Neurobiol. 50, 149–158.
71. Long J. Z., Li W. and Booker L. et al. (2009) Selective blockade of 2-arachidonoyl hydrolysis produces cannabinoid behavioral effects. Nat. Chem. Biol. 5, 37–44.
72. Luongo L., Malcangio M., Salvemini D. and Starowicz K. (2015) Chronic pain: new insights in molecular and cellular mechanisms. BioMed Res. Int. 2015, 1–2. doi.10.1155/2015/676725.
73. Maccarrone M., Gasperi V., Catani M. V., Diep T. I., Dainese E., Hansen H. S. and Avigliano L. (2010) The endocannabinoid system and its relevance to nutrition. Annu. Rev. Nutr. 30, 423–440.
74. Martin G. G., Danneberg H., Kumar L. S., Atshaves B. P., Erol E., Bader M., Schroeder F. and Binas B. (2003a) Decreased liver fatty acid binding capacity and altered liver lipid distribution in mice lacking the liver fatty acid binding protein (L-FABP) gene. J. Biol. Chem. 278, 21429–21438.
75. Martin G. G., Huang H., Atshaves B. P., Binas B. and Schroeder F. (2003b) Ablation of the liver fatty acid binding protein gene decreases fatty acyl CoA binding capacity and alters fatty acyl CoA pool distribution in mouse liver. Biochem 42, 11520–11532.
76. Martin G. G., Atshaves B. P., McIntosh A. L., Mackie J. T., Kier A. B. and Schroeder F. (2005) Liver fatty acid binding protein (L-FABP) gene ablation alters liver bile acid metabolism in male mice. Biochem. J. 391, 549–560.
77. Martin G. G., Hostetler H. A., McIntosh A. L. et al. (2008) Structure and function of the sterol carrier protein-2 (SCP-2) N-terminal pre-sequence. Biochem 47, 5915–5934.
78. Martin G. G., Atshaves B. P., Huang H., McIntosh A. L., Williams B. W., Pai P.-J., Russell D. H., Kier A. B. and Schroeder F. (2009a) Hepatic phenotype of liver fatty acid binding protein (L-FABP) gene ablated mice. Am. J. Physiol. 297, G1053–G1065.
79. Martin G. G., Atshaves B. P., McIntosh A. L., Mackie J. T., Kier A. B. and Schroeder F. (2009b) Liver fatty acid binding protein gene ablation enhances age-dependent weight gain in male mice. Mol. Cell. Biochem. 324, 101–115.
80. Martin G. G., Atshaves B. P., Landrock K. K., Landrock D., Storey S. M., Howles P. N., Kier A. B. and Schroeder F. (2014) Ablating L-FABP in SCP-2/SCP-x null mice impairs bile acid metabolism and biliary HDL-cholesterol secretion. Am. J. Physiol. Gastrointest. Liver Phys. 307, G1130–G1143.
81. Martin G. G., Atshaves B. P., Landrock K. K., Landrock D., Schroeder F. and Kier A. B. (2015) Loss of L-FABP, SCP-2/SCP-x, or both Induces Hepatic Lipid Accumulation in Female Mice. Arch. Biochem. Biophys. 580, 41–49.
82. Mashek D. G. (2013) Hepatic fatty acid trafficking: multiple forks in the road. Adv. Nutr. 4, 697–710.
83. Matsuura J. E., George H. J., Ramachandran N., Alvarez J. G., Strauss J. F. I. and Billheimer J. T. (1993) Expression of the mature and the pro-form of human sterol carrier protein 2 in Escherichia coli alters bacterial lipids. Biochemistry 32, 567–572.
84. Mattes R. D., Shaw L. M., Edling-Owens J., Engelman K. and Elsohly M. A. (1993) Bypassing the first-pass effect for the therapeutic use of cannabinoids. Pharm. Biochem. Behavior 44, 745–747.
85. McArthur M. J., Atshaves B. P., Frolov A., Foxworth W. D., Kier A. B. and Schroeder F. (1999) Cellular uptake and intracellular trafficking of long chain fatty acids. J. Lipid Res. 40, 1371–1383.
86. McIntosh A. L., Atshaves B. P., Hostetler H. A., Huang H., Davis J., Lyuksyutova O. I., Landrock D., Kier A. B. and Schroeder F. (2009) Liver type fatty acid binding protein (L-FABP) gene ablation reduces nuclear ligand distribution and peroxisome proliferator activated receptor-alpha activity in cultured primary hepatocytes. Arch. Biochem. Biophys. 485, 160–173.
87. McIntosh A. L., Huang H., Atshaves B. P., Wellburg E., Kuklev D. V., Smith W. L., Kier A. B. and Schroeder F. (2010) Fluorescent n-3 and n-6 very long chain polyunsaturated fatty acids: three photon imaging and metabolism in living cells overexpressing liver fatty acid binding protein. J. Biol. Chem. 285, 18693–18708.
88. McIntosh A. L., Huang H., Storey S. M., Landrock K., Landrock D., Petrescu A. D., Gupta S., Atshaves B. P., Kier A. B. and Schroeder F. (2014) Human FABP1 T94A variant impacts fatty acid metabolism and PPARa activation in cultured human female hepatocytes. Am. J. Physiol. Gastrointest. Liver Phys. 307, G164–G176.
89. Mechoulam R., Fride E., Hanus L. et al. (1997) Anandamide may mediate sleep induction. Nature 389, 25–26.
90. Mitchell R. W. and Hatch G. M. (2011) Fatty acid transport into the brain: of fatty acid fables and lipid tails. Prost. Leukot. Essen. Fatty Acids 85, 293–302.
91. Mohnle P., Schutz S. V., Schmidt M., et al. (2014) miR-665 is invovled inteh regulation of the expression of the cardioprotective CB2 in patients with severe heart failure. Biochem. Biophy. Res. Comm. 451, 516–521.
92. Moreno-Sanz G., Sasso O., Guijarro A. and Piomelli D. (2012) Pharmacological characterization of the peripheral FAAH inhibitor URB937 in female rodents: interaction with the Abcg2 transporter in the blood-placenta barrier. Br. J. Pharmacol. 167, 1620–1628.
93. Morrow F. D., Allen C. E. and Martin R. J. (1979) Intracellular fatty acid-binding protein: hepatic levels in lean and obese rats. Fed. Proc. 38, 280.
94. Moulle V. S. F., Cansell C., Luquet S. and Cruciani-Guglielmacci C. (2012) Multiple roles of fatty acid handling proteins in brain. Front. Physiol. 3, 1–6.
95. Mukhopadyay B., Liu J., Osei-Hylaman D. and Kunos G. (2010) Transcriptional regulation of the cannabinoid receptor-1 expression in the liver by retinoid acid via retinoid acid receptor-g. J. Biol. Chem. 285, 19002–19011.
96. Murphy E. J. (1998) L-FABP and I-FABP expression increase NBD-stearate uptake and cytoplasmic diffusion in L-cells. Am. J. Physiol. 275, G244–G249.
97. Murphy E. J. (2015) Blood-brain barrier and brain fatty acid uptake: role of arachidonic acid and PGE2. J. Neurochem. 135, 845–848.
98. Murphy E. J. and Horrocks L. A. (1993) A model for compression trauma: pressure-induced injury in cell cultures. J. Neurotrauma 10, 431–444.
99. Murphy E. J., Prows D. R., Jefferson J. R., Incerpi S., Hertelendy Z. I., Heiliger C. E. and Schroeder F. (1996a) Cis-parinaric acid uptake in L-cells. Arch. Biochem. Biophys. 335, 267–272.
100. Murphy E. J., Prows D. R., Jefferson J. R. and Schroeder F. (1996b) Liver fatty acid binding protein expression in transfected fibroblasts stimulates fatty acid uptake and metabolism. Biochim. Biophys. Acta 1301, 191–198.
101. Murphy E. J., Edmondson R. D., Russell D. H., Colles S. M. and Schroeder F. (1999) Isolation and characterization of two distinct forms of liver fatty acid binding protein from the rat. Biochim. Biophys. Acta 1436, 413–425.
102. Murphy E. J., Owada Y., Kitanaka N., Kondo H. and Glatz J. F. C. (2005) Brain arachidonic acid incorportion is decreased in heart FABP gene ablated mice. Biochem. 44, 6350–6360.
103. Myers-Payne S., Fontaine R. N., Loeffler A. L., Pu L., Rao A. M., Kier A. B., Wood W. G. and Schroeder F. (1996a) Effects of chronic ethanol consumption on sterol transfer protein in mouse brain. J. Neurochem. 66, 313–320.
104. Myers-Payne S. C., Hubbell T., Pu L., Schnutgen F., Borchers T., Wood W. G., Spener F. and Schroeder F. (1996b) Isolation and characterization of two fatty acid binding proteins from mouse brain. J. Neurochem. 66, 1648–1656.
105. Naughton S. S., Mathai M. L., Hryciw D. H. and McAinch A. J. (2013) Fatty acid modulation of the endocannabinoid system and the effect on food intake and metabolism. Int. J. Endocrinol. ID 361895, 1–11.
106. Newberry E. P., Xie Y., Kennedy S., Buhman K. K., Luo J., Gross R. W. and Davidson N. O. (2003) Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid binding protein gene. J. Biol. Chem. 278, 51664–51672.
107. Nomura D. K., Morrison B. A. E., Blankman J. I., et al. (2011) Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation. Science 334, 809–813.
108. Oddi S., Fezza F., Pasquoriello N., et al. (2009) Molecular identification of albumin and Hsp70 as cytosolic anandamide binding proteins. Chem. Biol. 16, 624–632.
109. Owada Y. (2008) Fatty acid binding protein: localization and functional significance in brain. Tohoku J. Exp. Med. 214, 213–220.
110. Owada Y., Abdelwahab S. A., et al. (2006) Altered emotional behavioral responses in mice lacking brain type FABP gene. Eur. J. Neurosci. 24, 175–187.
111. Owada Y., Yoshimoto T. and Kondo H. (1996) Spatio-temporally differential expression of genes for three members of fatty acid binding proteins in developing and mature rat brains. J. Chem. Neuroanat. 12, 113–122.
112. Peng X.-E., Wu Y. L., Lu Q.-Q., Ju Z.-J. and Lin X. (2012) Two genetic variants in FABP1 and susceptibility to non-alcoholic fatty liver disease in a Chinese population. Gene 500, 54–58.
113. Petrescu A. D., Huang H., Martin G. G., McIntosh A. L., Storey S. M., Landrock D., Kier A. B. and Schroeder F. (2013) Impact of L-FABP and glucose on polyunsaturated fatty acid induction of PPARa regulated b-oxidative enzymes. Am. J. Physiol. Gastrointest. Liver Phys. 304, G241–G256.
114. Pignon J.-P., Bailey N. C., Baraona E. and Lieber C. S. (1987) Fatty acid-binding protein: a major contributor to the ethanol-induced increase in liver cytosolic proteins in the rat. Hepatology 7, 865–871.
115. Piomelli S. and Seaman C. (1993) Mechanism of red blood cell aging: relationship of cell density and cell age. [Review]. Am. J. Hematol. 42, 46–52.
116. Prows D. R., Murphy E. J. and Schroeder F. (1995) Intestinal and liver fatty acid binding proteins differentially affect fatty acid uptake and esterification in L-Cells. Lipids 30, 907–910.
117. Pu L., Foxworth W. B., Kier A. B., Annan R. S., Carr S. A., Edmondson R., Russell D., Wood W. G. and Schroeder F. (1998) Isolation and Characterization of 26- and 30-kDa Rat Liver Proteins Immunoreactive to Anti-Sterol Carrier Protein-2 Antibodies. Protein Expr. Purif. 13, 337–348.
118. Pu L., Annan R. S., Carr S. A., Frolov A., Wood W. G., Spener F. and Schroeder F. (1999a) Isolation and identification of a native fatty acid binding protein form mouse brain. Lipids 34, 363–373.
119. Pu L., Igbavboa U., Wood W. G., Roths J. B., Kier A. B., Spener F. and Schroeder F. (1999b) Expression of fatty acid binding proteins is altered in aged mouse brain. Mol. Cell. Biochem. 198, 69–78.
120. Rubino T. and Parolaro D. (2011) Sexually dimorphic effects of cannabinoid compounds on emotion and cognition. Front. Behav. Neurosci. 5, 1–5.
121. Sagar D. R., Burston J. J., Woodhams S. G. and Chapman V. (2012) Dynamic changes to the endocannabinoid system in models of chronic pain. Phil. Trans. R. Soc. B 367, 3300–3311.
122. Sailler S., Schmitz K., Jager E. and erreiros N. et al. (2014) Regulation of circulating endocannabinoids associated with cancer and metastases in mice and humans. Oncoscience 1, 272–282.
123. Sarchielli P., Pini L. A., Coppola F., et al. (2007) Endocannabinoids in chronic migraine: CSF findings suggest a system failure. Neuropsychopharmacology 32, 1384–1390.
124. Schlosburg J. E., Blankman J. I., Long J. Z., et al. (2010) Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat. Neurosci. 13, 1113–1119.
125. Schnutgen F., Borchers T., Muller T. and Spener F. (1996) Heterologous expression and characterization of mouse brain fatty acid binding protein. Biol. Chem. Hoppe-Seyler 377, 211–215.
126. Schroeder F., Jefferson J. R., Powell D. et al. (1993) Expression of rat L-FABP in mouse fibroblasts: role in fat absorption. Mol. Cell. Biochem. 123, 73–83.
127. Schroeder F., Jolly C. A., Cho T. H. and Frolov A. A. (1998) Fatty acid binding protein isoforms: structure and function. Chem. Phys. Lipids 92, 1–25.
128. Seedorf U., Raabe M., Ellinghaus P. et al. (1998) Defective peroxisomal catabolism of branched fatty acyl coenzyme A in mice lacking the sterol carrier protein-2/sterol carrier protein-x gene function. Genes Dev. 12, 1189–1201.
129. Smart D., Jonsson K.-O., Vanvoorde S., Lambert D. M. and Fowler C. J. (2002) Entourage effects of N-acyl ethanolamines at human vanilloid receptors. Comparison of effects upon anandamide-induced vanilloid receptor activation and upon anandamide metabolism. Br. J. Pharmacol. 136, 452–458.
130. Storey S. M., McIntosh A. L., Huang H., Martin G. G., Landrock K. K., Landrock D., Payne H. R., Kier A. B. and Schroeder F. (2012a) Loss of intracellular lipid binding proteins differentially impacts saturated fatty acid uptake and nuclear targeting in mouse hepatocytes. Am. J. Physiol. Gastrointest. Liver Phys. 303, G837–G850.
131. Storey S. M., McIntosh A. L., Huang H., Martin G. G., Landrock K. K., Landrock D., Payne H. R., Kier A. B. and Schroeder F. (2012b) Intracellular cholesterol binding proteins enhance HDL-mediated cholesterol uptake in cultured primary mouse hepatocytes. Am. J. Physiol. Gastrointest. Liver Phys. 302, G824–G839.
132. Stringer R. L., Laufer B. I., Klieber M. L. and Singh S. M. (2013) Reduced expression of brain Cnr1 is coupled with an increased complementary miR-26b in a mouse model of fetal alcohol spectrum disorders. Clinical Epigenetics 5, 14.
133. Thigpen J. E., Setchell K. D., Ahlmark K. B., Kocklear J., Spahr T., Caviness G. F., Goelz M. F., Haseman J. K., Newbold R. R. and Forsythe D. B. (1999a) Phytoestrogen content of purified, open- and closed-formula laboratory animal diets. Lab. An. Sci. 49, 530–536.
134. Thigpen J. E., Setchell K. D., Goelz M. F. and Forsythe D. B. (1999b) The phytoestrogen content of rodent diets. Envron. Health Persp. 107, A182–A183.
135. Trevaskis N. L., Shackleford D. M., Charman W. N., Edwards G. A., et al. (2009) Intestinal lymphatic transport enhances the post-prandial oral bioavailability of a novel cannabinoid receptor agonist via avoidance of first-pass metabolism. Pharm. Res. 26, 1486–1495.
136. Wang L., Liu J., Harvey-White J., Zimmer A. and Kunos G. (2003) Endocannabinoid signaling via cannabinoid receptor 1 is invovled in ethanol prference and its age-dpendent decline in mice. Proc. Natl Acad. Sci. USA 100, 1393–1398.
137. Witkamp R. (2015) Fatty acids, endocannabinoids, and inflammation. Eur. J. Pharmacol. doi:10.1016/j.ejphar.2015.08.051.
138. Wolfrum C., Buhlman C., Rolf B., Borchers T. and Spener F. (1999a) Variation of liver fatty acid binding protein content in the human hepatoma cell line HepG2 by peroxisome proliferators and antisense RNA affects the rate of fatty acid uptake. Biochim. Biophys. Acta 1437, 194–201.
139. Wolfrum C., Ellinghaus P., Fobker M., Seedorf U., Assmann G., Borchers T. and Spener F. (1999b) Phytanic acid is ligand and transcriptional activator of murine liver fatty acid binding protein. J. Lipid Res. 40, 708–714.
140. Wood J. T., Williams J. S. and Makriyannis A. (2010) Dietary DHA supplementation alters select physiological endocannabinoid system metabolites in brain and plasma. J. Lipid Res. 51, 1416–1423.
141. Yang S. Y., He X. Y. and Schulz H. (1987) Fatty acid oxidation in rat brain is limited by the low activity of 3-ketoacyl-coenzyme A thiolase. J. Biol. Chem. 262, 13027–13032.
142. Yu S., Levi L., Casadesus G., Kunos G. and Noy N. (2014) Fatty acid binding protein 5 (FABP5) regulates cognitive function both by decreasing anandamide levels and by activating the nuclear receptor peroxisome proliferator activated receptor b/d (PPARb/d) in the brain. J. Biol. Chem. 289, 12748–12758.
143. Zhang J., Teng Z., Tang Y.-P. and Chen C. (2014) Synaptic and cognitive improvements by inhibition of 2-AG metabolism are through upregualtion of miR-188-3p in a mouse model of Alzheimer's disease. J. Neurosci. 34, 1419–1433.
144. Zhou L., Vessby B. and Nilsson A. (2002) Quantitative role of plasma free fatty acids in the supply of arachidonic acid to extrahepatic tissues in rats. J. Nutr. 132, 2626–2631.