Digestion, absorption, and transport of dietary lipids
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1 TG metabolism Utilization of dietary lipids Synthesis in liver and adipose tissue Fatty acid catabolism and synthesis Mobilization of TG to provide energetic needs β-oxidation of fatty acids De novo synthesis of fatty acid Ketone bodies Metabolism of phospholipids Metabolism of prostaglandin and leukotriene Cholesterol Metabolism Synthesis of cholesterol and its regulation Bile acid Biosynthesis of bile acids Enterohepatic circulation of bile acids and significance as a therapeutic modality Lipoprotein Characteristics of Lipoproteins and metabolism Therapeutics for hypercholesterolemia treatment Genetics of familial hypercholesterolemia 1 Digestion, absorption, and transport of dietary lipids 2
2 Lipases in tissues Lipoprotein lipase (LPL) bound to surface of endothelial cell derived from heart, muscle, and adipose tissue activated by apoc-ii and phosphatidylcholine insulin stimulates its synthesis Fate of free fatty acids Directly enter adjacent muscle cells or adipocytes In muscle, the fatty acids are oxidized for energy; in adipose tissue, they are re-esterified to produce TG for storage 3 Synthesis of TG Need to synthesize glycerol 3-phosphate 4
3 Sources of glycerol 3-phosphate The glycerol cannot be metabolized to G3P in adipocytes lacking glycerol kinase The majority of the G3P is derived from the glycolytic intermediate dihydroxyacetone phosphate by NADH-dependent G3P dehydrogenase Glycerol from diets can be phosphorylated to be G3P by glycerol kinase only in liver and kidney G3P can be converted to dihydroxyacetone phosphate by reversal of the glycerol dehydrogenase reaction 5 Synthesis of Triacylglycerols 1. Acyl-CoAs formed by acyl-coa synthetases, the same enzymes responsible for the activation of fatty acids for β-oxidation 2. Glycerol 3-phosphate acyltransferase (GPAT) 3. 1-Acyl-sn-glycerol 3-phosphate acyltransferase (AGPAT) 6
4 Synthesis of Triacylglycerols 1. Phosphatidic acd phosphatase (PAP) 2. Diacylglycerol acyltransferase (DGAT) 3. Glycerophospholipids are also derived from phosphatidic acid 7 Mobilization of fatty acids from stored triacylglycerol Hormone-sensitive lipase & Perilipin 8
5 Fatty acid oxidation Fatty acid activation Conversion of fatty acid to a fatty acyl-coa: activation acyl-coa synthetase Transport of acyl-coa into mitochondria β-oxidation of fatty acyl-coa in mitochondria 9 Transport of acyl-coa into mitochondria: Carnitine shuttle 10
6 Reactions of β-oxidation: Four reaction steps 1. Formation of a trans-α, β double bond through dehydrogenation by the flavoenzyme acyl-coa dehydrogenase 2. Hydration of the double bond by enoyl-coa hydratase to form a 3-L-hydroxylacyl-CoA 3. NAD + -dependent dehydrogenation of β- hydroxyacyl-coa by β-l-hydroxyacyl-coa dehydrogenase to for the corresponding β-ketoacyl-coa 4. C α -C β cleavage in a thiolysis reaction with CoA as catalyzed by β-ketoacyl-coa thiolase (acyl-coa acetyltransferase) to form acetyl-coa and a new acyl-coa containing two fewer C atoms than the original one 11 Energy-Yield from β-oxidation of Fatty Acid 12
7 Oxidation of mono-unsaturated fatty acids Problem 1: β, γ double bonds Enoyl-CoA isomerase converts the cis-δ 3 double bond to the trans-δ 2 form. 13 Oxidation of unsaturated fatty acids Problem 2: Δ 4 double bond inhibits enoyl-coa hydratase The presence of 2,4-dienoyl-CoA: NADPH-dependent 2,4-dienoyl-CoA reductase reduces the Δ4 double bond. 14
8 Peroxisomal β-oxidation Shortens very long chain fatty acids (>22 C atoms), which are then fully degraded by the mitochondrial β-oxidation system Requires only three enzymes: 1. Acyl-CoA oxidase 2. Enoyl-CoA hydratase and hydroxyacyl CoA dehydrogenase 3. Peroxisomal thiolase is almost inactive with acyl-coas of length C8 or less. 15 Regulation of fatty acid oxidaton 1. Malonyl CoA inhibits carnitine acyltransferase I 2. β-hydroxyacyl-coa dehydrogenase is inhibited by high [NADH/NAD + ] ratio 3. Thiolase inhibited by high concentration of acetyl-coa 16
9 Ketone Body The acetyl-coa produced by oxidation of fatty acid can be further oxidized via the citric acid cycle Importance of available oxaloacetate for acetyl-coa to enter TCA cycle Oxaloacetate is depleted when prolonged starvation for gluconeogenesis In liver mitochondria, a significant fraction of this acetyl-coa has another fate: by ketogenesis, acetyl CoA is converted to acetoacetate or β-dhydroxybutyrate. Acetoacetate β-d-hydroxybutyrate Acetone 17 Synthesis of ketone bodies from acetyl-coa in liver 18
10 Utilization of ketone bodies by the peripheral tissues In extrahepatic tissues, acetoacetate is activated to acetoacetyl-coa by transfer of CoA from succinyl-coa with the coupled synthesis of GTP in the succinyl-coa synthetase diverted from TCA cycle The liver actively produces ketone bodies, but cannot reconvert acetoacetate to acetoacetyl-coa lacks succinyl-coa:acetoacetate CoA transferase in liver 19 The Liver Is the Source of Ketone Bodies
11 De novo Fatty Acid Biosynthesis Fatty acids are synthesized de novo in cytosol from acetyl-coa (C2) Acetyl-CoA carboxylase and fatty acid synthase Requires ATP and NADPH Palmitate (C16) is the primary product Acetyl-CoA, the starting material, should be shuttled out of mitochondria - ATP-citrate lyase (ACLY) 21 Acetyl CoA Carboxylase (ACACA) Fatty acid biosynthesis occurs through condensation of C2 units. Both acetyl-coa and bicarbonate are required, and C3 unit, malony-coa is an intermediate of fatty acid biosynthesis. Requires biotin Synthesizes malonyl-coa from acetyl-coa 22
12 Fatty acid synthase (FASN) The four steps to lengthen a growing fatty acyl chain by two carbon 1. Condensation 2. Reduction of the carbonyl group 3. Dehydration 4. Reduction of the double bond KS: β-ketoacyl-acp synthase MAT: malony/acetyl-coa-acp transferase DH: β-hydroxyacyl-acp dehydratase ER: enoly-acp reductase KR: β-ketoacyl-acp reductase ACP: acyl-carrier protein TE: thioesterase 23 Priming Malonyl/acetyl-CoA ACP transacylase 24
13 1.Condensation KS: β-ketoacyl-acp synthase 2.Reduction KR: β-ketoacyl-acp reductase 3.Dehydration β-hydroxyacyl-acp dehydratase 4.Reduction Enoyl-ACP reductase 25 The overal process of palmitate synthesis 26
14 Elongase Fatty acid elongation system Long Chain Elongase (LCE) Present in both the mitochondria and the smooth ER. ER elongation involves the successive condensations of malonyl- CoA with acyl-coa. In most tissue, ER elongation synthesize almost exclusively stearate; in brain, longer chain acids (up to C24) synthesized needed for brain lipid 27 Desaturase Desaturation of fatty acids occurs in the endoplasmic reticulum: Mixed function oxidase Stearoyl-CoA desaturase (Δ9) Δ6-fatty acyl CoA desaturase Δ5-fatty acyl CoA desaturase Δ4-fatty acyl CoA desaturase 28
15 Sources of NADPH for Fatty Acid Synthesis Malic enzyme Pentose phosphate pathway NADP + -dependent isocitrate dehydrogenase 29 Regulation of Acetyl-CoA Carboxylase A. Hormonal regulation : Transcriptional 1. Insulin is a global signal to stimulate fatty acid synthesis by activating the carboxylase 2. Glucagon and epinephrine have the reverse effect of insulin B. Allosteric regulation 1. Palmitoyl CoA is a feedback inhibitor of enzyme activity 2. Citrate is an allosteric activator 30
16 Regulation of Acetyl-CoA Carboxylase Transcriptional regulation Induction of acetyl CoA carboxylase mrna by insulin and feeding (fasting/refeeding) an animal Increased amount of acetyl CoA carboxylase by insulin and feeding (fasting/refeeding) an animal 31 Coordinate regulation of FA synthesis and oxidation Phosphorylation & Dephosphorylation 32
17 Biosynthesis of Membrane Phospholipds Begin with phosphatidic acid or diacylglycerol Attach head group to C-3 OH group C-3 has OH; head group has OH new phospho-head group created when phosphoric acid condenses with these two alcohols eliminates two H 2 O Strategies for attaching phospholipid head groups Eukaryotes employ both strategies All in bacteria Anionic phospholipids in Eukaryotes phosphatidylglycerol, cardiolipin, & phosphatidylinositol Phosphatidylserine (PS) in yeast Phosphatidylethanolamine (PE) & phosphatidylcholine (PC) from CDPethanolamine & CDP-choline PS from PE or PC via head-group exchange in mammals 34
18 Summary 35 Eicosanoid: Prostaglandin and Leukotriene Hormones derived from arachidonic acids (C20:4, Δ 5,8,11,14 ) Act locally, unique to animal cells 1930s Ulf von Euler in Sweden PG discovered as oxygenated eicosanoid in human semen when injected into animals, they contract uterus and increase blood pressure The Nobel Prize in Physiology or Medicine, 1970 Sir Bernard Katz, Ulf von Euler, and Julius Axelrod "for their discoveries concerning the humoral transmittors in the nerve terminals and the mechanism for their storage, release and inactivation" Sune Bergstrom & Bengt Samuelsson from Sweden in 1960s Structure & metabolism of eicosanoids 1971 by John Vane Aspirin block the synthesis of PG The Nobel Prize in Physiology or Medicine, 1982 Sune Bergstrom, Bengt Samuelsson, Sir John Vane " for their discoveries concerning prostaglandins and related biologically active substances" 36
19 Synthesis of Prostaglandins by cyclooxygenase 37 Leukotrienes by lipoxygenase 38
20 Anti-inflammatory drugs Non-Steroidal Anti-inflammatory Drugs (NSAIDs) Aspirin - Irreversible inactivation of cyclooxygenase Ibuprofen/Naproxen - reversible inhibition of COX COX-1 or COX-2 isoenzyme specific inhibitors Celecoxib, Valdecoxib, Rofecoxib 39 Metabolism of cholesterol Metabolism of bile acids Metabolism of lipoprotein 40
21 Cholesterol Essential component of cell membrane Precursors for a variety of products Bile acid Steroid hormones Vitamin D Solubility <0.2 mg/100 ml water at 25 C actual conc. in plasma of normal adult: 150 ~ 200 mg/100 ml exists as plasma lipoprotein (LDL, VLDL) C3-hydroxyl is esterified with fatty acid (70%) Ring structure of cholesterol is not metabolized to CO 2 and H2O 41 Good cholesterol vs. Bad cholesterol An essential component of cell membranes for proper membrane permeability and fluidity Hypocholesterolemia: Low concentration of plasma cholesterol Hypercholesterolemia: High concentration of plasma cholesterol Does hypocholesterolemia cause any disease conditions? Not clear if a lower than average cholesterol level is directly harmful In inflammatory condition when inflammatory cells need to proliferate In cancer tissues when cancer cells need to proliferate 42
22 Bad Cholesterol vs. Good Cholesterol Circulation. 1999;99: Endogenous cholesterol synthesis from Acetyl CoA in cytosol 1. Synthesis of mevalonate from acetyl-coa Acetyl-CoA acetyl transferase (thiolase I) HMG-CoA synthase in cytosol An isoenzyme of HMG-CoA synthase in mitochondria for synthesis of ketone body HMG-CoA reductase The rate-limiting enzyme Sources of acetyl CoA & acetoacetyl-coa 1. the β-oxidation of fatty acids 2. the oxidation of ketogenic amino acids 3. the pyruvate dehydrogenase reaction 4. by acetyl-coa synthase (acetate thiokinase) from free acetate 44
23 2. Condensation of mevalonate to activated isoprene Mevalonate 5-phosphotransferase (ATP) Phosphomevalonate kinase (ATP) Pyrophosphomevalonate decarboxylase (ATP) Δ 3 -isopentenyl pyrophosphate Isopentenly pyrophosphate (IPP) isomerase Dimethylallyl pyrophosphate Prenyl: 3-methyl-but-2-ne-1-yl Δ 3 -isopentenyl pyrophosphate 45 Good? - Normal repertoire of cholesterol More than 20,000 isoprenoids in nature 46
24 3. Condensation of six activated isoprene units to form squalene Head-to-tail condensation of activated isoprenes (C5) Farnesyl pyrophosphate synthase (prenyl transferase) Geranyl pyrophosphate (C10) Farnesyl pyrophosphate (C15) 47 Prenylation (isoprenylation, lipidation) Addition of prenyl groups to a protein or chemical compounds Involves transfer of farnesyl or geranyl moiety to C-terminal cysteine of the target protein Related to longevity and cardiac health by decreasing specific protein prenylation by statins 48
25 3. Condensation of six activated isoprene units to form squalene Head-to-head condensation of farnesyl pyrophosphate Squalene synthetase Squalene Conversion of squalene to the four-ring steroid nucleus Squalene monooxygenase (NADPH) Squalene 2,3-epoxide Cyclase Lanosterol A series of about 20 reactions Cholesterol Sterol characteristic of animal cells 50
26 51 Fate of cholesterol Much of the cholesterol synthesis in vertebrates takes place in the liver Small fraction is incorporated into the membranes of hepatocytes But most of cholesterol is exported Bile acids Cholesteryl ester in lipoproteins: SOAC (Sterol O-acyltransferase) ACAT (acyl-coa:cholesterol acyltransferase) : 52
27 Synthesis of the primary bile acids from cholesterol 53 Bile acids & Bile salts Conjugation of bile acid with glycine and taurine 54
28 Bile acids & Bile salts Synthesis of the secondary bile acids from primary bile acids 55 Enterohepatic circulation of bile salts 56
29 Steroid hormones from cholesterol CH 3 CH 3 O CH 3 O Progesterone 57 Vitamin D Hydroxylation of C-25 in liver Hydroxylation of C-1 in Kidney 58
30 Lipid Transport 1. Four pathways of lipid transport in the human body: Exogenous path: dietary lipids from the intestine to other tissues Endogenous path: synthesized lipids from the liver to other tissues Reverse cholesterol transport from extrahepatic tissues to the liver Transport mediated by lipoproteins 2. The transport of fatty acids from adipose tissue to other tissues Unesterified ("free") fatty acids are transported in noncovalent binding to serum albumin 59 Lipoproteins 60
31 Lipoprotein and lipid transport 61 Exogenous pathway: Chylomicron Dietary fat digestion by pancreatic lipase and other digestive enzymes with help of bile acids Absorption of free fatty acids (FFA), 2-MG, cholesterol into intestinal enterocyte Formation of TG and cholesterol ester in enterocyte and assembly of chylomicron with apob-48, C-II, & E Chylomicron move out into lymphatic system and enter bloodstream 0 via the left subclavian vein ApoC-II activates lipoprotein lipase in the capillaries of adipose, heart, skeletal muscles, mammary glands, etc, allowing the release of FFA to these tissues Chylomicron returns ApoC-II to the HDL, but keeps apoe The most TG are delivered to peripheral tissues, but dietary cholesterol, phospholipids, and apolipoproteins (apoe and B-48) still remain in chylomicron The remnant of chylomicron is sequestered by being uptaken in liver via the chylomicron remnant receptor 62
32 Endogenous pathway: TG Liver is the major organ to synthesize TG, PL, and chol - - Chol is esterified by ACAT before assembly into VLDL, then secreted into blood apob-100, C-1, C-II, C-III, & E Lipoprotein lipase activated by apoc-ii FFA delivered to adipocytes and TG content in VLDL goes down to become IDL Further decrease in TG results in becoming LDL LDL carries cholesterol to peripheral tissues via the membrane LDL receptor that recognizes apob-100; LDL also delivers cholesterol to macrophage (not shown) 63 Finally LDL is taken up by liver via the LDL receptor Receptor mediated endocytosis of 64
33 Michael Brown & Joseph Goldstein Dept. Molecular Genetics, Univ. Texas Southwestern Medical Center, Dallas, TX Michael Brown and Joseph Goldstein The Nobel Prize in Medicine, 1985 "for their discoveries concerning the regulation of cholesterol metabolism 65 Reverse cholesterol transport: HDL Good cholesterol HDL originates in the liver as small, protein-rich particles, that contain relatively little cholesterol and no cholesteryl ester (nascent HDL) -contains apoa-i, A-II, C-I, C-II, C-III, & E Nascent HDL also contains LCAT (lecithin-cholesterol acyl transferase) which converts peripheral cholesterol (transfer via ABCA1/G1) to cholesterol ester, then becomes mature HDL Mature HDL returns to liver via Scavenger receptor type B1 (SR-BI) - Unloading of sterol via SR-BI does not involve endocytosis - Mediates partial and selective transfer of cholesterol and other lipids into cells, then depleted HDL recirculates and reused. Some of cholesteryl esters in HDL is transferred to LDL by cholesteryl ester transfer protein (CETP) 66
34 Classification of Lipoprotein Lipoprotein Density (g/ml) Source Apoproteins Particle diameter (nm) Chylomicron <0.95 Intestine B-48, A-I, A-IV, C-II, C-III, E 75-1,500 VLDL Liver IDL VLDL B-100, C-I, C-II, C-III, E LDL IDL HDL Liver, Intestine Chemical composition of the different plasma lipoprotein classes Lipoproteins Total protein (%) Total lipid (%) A-I, A-II, C-I, C-II, C-III, D, E, F, CETP Percent composition of lipid fraction PL CE C TG Chylomicron VLDL IDL LDL HDL Chemical composition of the different plasma lipoprotein classes Lipoproteins Total protein (%) Chylomicron Diameter (nm) 75-1,500 Total lipid (%) Total protein (%) Percent composition of lipid fraction PL CE C TG VLDL IDL LDL HDL
35 Two sources of cellular cholesterol Regulation of Cholesterol Metabolism 69 Overall balanced of cholesterol formation 70
36 Transcriptional Regulation: SREBPs (Sterol regulatory element-binding proteins) Horton et al., J Clin Invest 109 (2002) Transcriptional Regulation of Lipid Metabolism SREBPs (Sterol regulatory element-binding proteins) 72
37 Cholesterol biosynthesis is carefully regulated Statin drugs as inhibitors of HMG-CoA reductase, a rate-limiting enzyme of cholesterol biosynthesis 73 PCSK9: Proprotein convertase subtilisin/kexin type 9 74
38 Transcriptional regulation: LXR and RXR 75 DISORDERS OF LIPOPROTEIN METABOLISM Primary Hyperlipoproteinemias Caused by Known Single Gene Mutations Genetic Disorder Gene Defect Lipoproteins Elevated Lipoprotein lipase deficiency LPL (LPL) Chylomicrons Familial apolipoprotein C-II deficiency Familial hepatic lipase deficiency Familial dysbetalipoproteinemia Familial hypercholesterolemia Familial defective apob-100 Autosomal recessive hypercholesterolemia ApoC-II (APOC2) Hepatic lipase (LIPC) ApoE (APOE) LDL receptor (LDLR) ApoB-100 (APOB) Chylomicrons Clinical Findings Eruptive xanthomas, hepatosplenomegaly pancreatitis Eruptive xanthomas, hepatosplenomegalypancreatitis Genetics Estimated Incidence AR 1/1,000,000 AR <1/1,000,000 VLDL remnants Premature atherosclerosis AR <1/1,000,000 Chylomicron and VLDL remnants Palmar and tuberoeruptive xanthomas, CHD, PVD AR AD 1/10,000 LDL Tendon xanthomas, CHD AD 1/500 LDL Tendon xanthomas, CHD AD 1/1000 ARH (ARH) LDL Tendon xanthomas, CHD AR <1/1,000,000 Sitosterolemia ABCG5 or ABCG8 LDL Tendon xanthomas, CHD AR <1/1,000,000 Familial hypercholesterolemia 3 (FH3) PCSK9 LDL CHD AD? Note: AR, autosomal recessive; AD, autosomal dominant; VLDL, very low density lipoprotein; CHD, coronary heart disease; PVD, peripheral vascular disease; LDL, low-density lipoprotein. 76
39 DISORDERS OF LIPOPROTEIN METABOLISM Secondary Forms of Hyperlipidemia LDL HDL Elevated Reduced Elevated Reduced Hypothyroidism Nephrotic syndrome Cholestasis Acute intermittent porphyria Anorexia nervosa Hepatoma Drugs: thiazides, cyclosporine, tegretol Severe liver disease Malabsorption Malnutrition Gaucher disease Chronic infectious disease Hyperthyroidisim Drugs: niacin toxicity Alcohol Exercise Exposure to chlorinated hydrocarbons Drugs: estrogen Smoking DM type 2 Obesity Malnutrition Gaucher disease Drugs: anabolic steroids, beta blockers 77 DISORDERS OF LIPOPROTEIN METABOLISM Drug Major Drugs Used for the Treatment of Hyperlipidemia HMG-CoA reductase inhibitors (statins) Lovastatin, Pravastatin Simvastatin, Fluvastatin Atorvastatin, Rosuvastatin Bile acid sequestrants Cholestyramine Colestipol, Colesevelam Nicotinic acid Immediate-release Sustained-release Extended-release Fibric acid derivatives Gemfibrozil Fenofibrate Major Indications Elevated LDL Elevated LDL Elevated LDL, low HDL, elevated TG Elevated TG, elevated remnants Mechanism Cholesterol synthesis, VLDL production Bile acid excretion and LDL receptors VLDL hepatic synthesis LPL, VLDL synthesis Fish oils Severely elevated TG Chylomicron and VLDL production Cholesterol absorption inhibitors Elevated LDL Intestinal cholesterol absorption Ezetimibe (Zetia by Schering-Plough) 78
40 DISORDERS OF LIPOPROTEIN METABOLISM Summary of the Drugs in Clinical Trials for the Treatment of Hyperlipidemia Drug Squalene synthase inhibitor BMS (Bristol-Myers Squibb) ACAT inhibitor Avasimibe (Pfizer) C1999 CS-505 (Sankyo), F1394 (UCB), HL004 (Taisho) CETP inhibitor Torcetrapib (Pfizer) JTT-705 (Japan Tobacco) MTP inhibitor Implitapide (Bayer) PPAR delta agonist GW (GSK) Monoclonal antibody against PCSK9 AMG 145 (Evolocumab, Amgen) Regn727 (Alirocumab, Sanofi/Regeneron) RN316 (Pfizer) (Merk) 79 80
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