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Fatty Acid Binding Protein-1 (FABP1) and the Human FABP1 T94A Variant: Roles in the Endocannabinoid System and Dyslipidemias

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Lipids

Abstract

The first discovered member of the mammalian FABP family, liver fatty acid binding protein (FABP1, L-FABP), occurs at high cytosolic concentration in liver, intestine, and in the case of humans also in kidney. While the rat FABP1 is well studied, the extent these findings translate to human FABP1 is not clear—especially in view of recent studies showing that endocannabinoids and cannabinoids represent novel rat FABP1 ligands and FABP1 gene ablation impacts the hepatic endocannabinoid system, known to be involved in non-alcoholic fatty liver (NAFLD) development. Although not detectable in brain, FABP1 ablation nevertheless also impacts brain endocannabinoids. Despite overall tertiary structure similarity, human FABP1 differs significantly from rat FABP1 in secondary structure, much larger ligand binding cavity, and affinities/specificities for some ligands. Moreover, while both mouse and human FABP1 mediate ligand induction of peroxisome proliferator activated receptor-α (PPARα), they differ markedly in pattern of genes induced. This is critically important because a highly prevalent human single nucleotide polymorphism (SNP) (26–38 % minor allele frequency and 8.3 ± 1.9 % homozygous) results in a FABP1 T94A substitution that further accentuates these species differences. The human FABP1 T94A variant is associated with altered body mass index (BMI), clinical dyslipidemias (elevated plasma triglycerides and LDL cholesterol), atherothrombotic cerebral infarction, and non-alcoholic fatty liver disease (NAFLD). Resolving human FABP1 and the T94A variant’s impact on the endocannabinoid and cannabinoid system is an exciting challenge due to the importance of this system in hepatic lipid accumulation as well as behavior, pain, inflammation, and satiety.

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Abbreviations

ACC:

Acetyl-CoA carboxylase

ACOX1:

Acyl-CoA oxidase 1, palmitoyl

AEA:

N-Arachidonoylethanolamide (anandamide)

2-AG:

2-Arachidonoylglycerol

ALB:

Albumin

ARA:

C20:4n-6 arachidonic acid

CB1 :

Cannabinoid receptor-1

CB2 :

Cannabinoid receptor-2

CPT1A:

Carnitine palmitoyl transferase IA, liver

CPT2:

Carnitine palmitoyl-CoA transferase II

DAGLα:

Diacylglycerol lipase-α

DAGLβ:

Diacylglycerol lipase-β

DAUDA:

11-(Dansylamino)undecanoic acid

DGAT2:

Diacylglycerol O-acyltransferase 2

DHA:

C22:6n-3 docosahexaenoic acid

EC:

Arachidonic acid-containing endocannabinoids (AEA, 2-AG)

EC*:

Non-ARA-containing N-acylethanolamides and 2-monoacylglycerols

EPA:

C20:5n-3 eicosapentaenoic acid

FAAH:

Fatty acid amide hydrolase

FABP1:

Liver fatty acid binding protein or FABP1

FABP1 T94A:

Human FABP1 T94A variant

FABP1 T94T:

Wild-type (WT) human FABP1

FABP3:

Heart fatty acid binding protein

FABP4:

Adipocyte fatty acid binding protein

FABP5:

Epidermal fatty acid binding protein

FABP7:

Brain fatty acid binding protein

FABP1 KO:

FABP1 gene ablated mouse on C57BL/6NCr background

FAS:

Fatty acid synthase

FF:

Fenofibrate

GPAM:

Glycerol-3-phosphate acyltransferase, mitochondrial

GPCR*:

G protein-coupled receptors other than CB1/CB2

GPR119:

G protein-coupled receptor 119

HDL:

High-density lipoprotein

HNF4α:

Hepatocyte nuclear factor-4α

LCFA:

Long chain fatty acids, unesterified

LCFA-CoA:

Long chain fatty acid-CoA thioester

LDL:

Low-density lipoprotein

LDL-C:

Low-density lipoprotein-C

LDLR:

Low-density lipoprotein (LDL) receptor

LPL:

Lipoprotein lipase

LSCM:

Laser scanning confocal microscopy

MAGL:

Monoacylglycerol lipase

MTTP:

Microsomal triglyceride transfer protein

NAAA:

N-Acylethanolamide acid amide hydrolase

NAFLD:

Non-alcohol fatty liver disease

NAPE-PLD:

N-Acyl phosphatidylethanolamine phospholipase D

NBD-AEA:

NBD-N-arachidonoylethanolamide or [20-[(7-nitro-2,1,3-benzoxadiazol-4-yl)amino] arachidonoylethanolamide

NBD-2-AG:

NBD-2-arachidonoylglycerol or 2-[20-[(7-nitro-2,1,3-benzoxadiazol-4-yl)amino] arachidonoyl glycerol

NBD-ARA:

NBD-arachidonic acid or [20-[(7-nitro-2,1,3-benzoxadiazol-4-yl)amino]arachidonic acid

NBD-cholesterol:

22-(N-(7-Nitrobenz-2-oxa-1,3-diazol-4-yl)-amino)-23,24-bisnor-5-cholen-3β-ol

NBD-stearic acid:

[12-N-Methyl-(7-nitrobenz-2-oxa-1,3-diazo)aminostearic acid]

OEA:

Oleoylethanolamide

2-OG:

2-Oleoylglycerol

PEA:

Palmitoylethanolamide

2-PG:

2-Palmitoylglycerol

PL:

Phospholipid

cis-PnCoA:

cis-Parinaroyl-CoA

PPARα, β/δ, or γ:

Peroxisome proliferator activated receptor alpha, beta/delta, or gamma

SCD1:

Stearoyl CoA desaturase

SCP-2:

Sterol carrier protein-2

SCP-x:

Sterol carrier protein-X

SNP:

Single nucleotide polymorphism

SRB1:

Scavenger receptor class B member 1

SREBP1c:

Sterol regulatory element binding protein-1c

TAG:

Triacylglycerol

VLDL:

Very-low-density lipoprotein

WT:

Wild-type C57BL/6NCr mouse

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Acknowledgments

This work was supported in part by the US Public Health Service/National Institutes of Health Grant R25 OD016574 (A.B.K.), Merial Veterinary Scholars Program, CVM (A.B.K.), and DA035923 and DA032232 (M.K.).

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Authors and Affiliations

  1. Department of Physiology and Pharmacology, Texas A&M University, TVMC, College Station, TX, 77843-4466, USA

    Friedhelm Schroeder, Avery L. McIntosh, Gregory G. Martin & Huan Huang

  2. Department of Pathobiology, Texas A&M University, TVMC, College Station, TX, 77843-4466, USA

    Danilo Landrock, Sarah Chung, Kerstin K. Landrock & Ann B. Kier

  3. Department of Biochemistry and Biophysics, Texas A&M University, TVMC, College Station, TX, 77843-4466, USA

    Lawrence J. Dangott

  4. Avanti Polar Lipids, 700 Industrial Park Dr., Alabaster, AL, 35007-9105, USA

    Shengrong Li

  5. Department of Anesthesiology, Stony Brook University, Stony Brook, NY, 11794, USA

    Martin Kaczocha

  6. Department of Pharmacology, Physiology, and Therapeutics and Chemistry, University of North Dakota, Grand Forks, ND, 58202-9037, USA

    Eric J. Murphy

  7. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, 48824, USA

    Barbara P. Atshaves

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  1. Friedhelm Schroeder
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  2. Avery L. McIntosh
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  13. Ann B. Kier
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Corresponding author

Correspondence to Friedhelm Schroeder.

Additional information

In conjunction with the Lipids 50th Anniversary Symposium, sponsored by Avanti Polar Lipids, at the 106th AOCS Annual Meeting.

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Schroeder, F., McIntosh, A.L., Martin, G.G. et al. Fatty Acid Binding Protein-1 (FABP1) and the Human FABP1 T94A Variant: Roles in the Endocannabinoid System and Dyslipidemias. Lipids 51, 655–676 (2016). https://doi.org/10.1007/s11745-016-4155-8

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  • DOI: https://doi.org/10.1007/s11745-016-4155-8

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