Molecular Biochemistry II Lipid Digestion & Transport Copyright © 1999-2005 by Joyce J. Diwan. All rights reserved. Lipid Digestion & Transport Digestion & transport of lipids poses unique problems relating to the insolubility of lipids in water. Enzymes that act on lipids are soluble proteins or membrane proteins at the aqueous interface. Lipids, and products of their digestion, must be transported through aqueous compartments within the cell as well as in the blood & tissue spaces. O Bile Acids C R1 O R2 CH3 CH3 HO OH R1 = OH or H H R2 = H or NHCH2COOH or NHCH2CH2SO3 Bile acids (bile salts) are polar derivatives of cholesterol, formed in liver and secreted into the gall bladder. They pass via the bile duct into the intestine, where they aid digestion of fats & fat-soluble vitamins. Bile acids are amphipathic, with detergent properties. O Bile Acids C R1 O R2 CH3 CH3 HO OH R1 = OH or H H R2 = H or NHCH2COOH or NHCH2CH2SO3 Bile acids emulsify fat globules into smaller micelles, increasing the surface area accessible to lipid-hydrolyzing enzymes. They also help to solubilize lipid breakdown products (e.g., mono- & diacylglycerols from hydrolysis of triacylglycerols). Secretion of bile salts & cholesterol into the bile by liver is the only mechanism by which cholesterol is excreted. Most cholesterol & bile acids are reabsorbed in the small intestine, returned to the liver via the portal vein, and may be re-secreted. This is the enterohepatic cycle. Agents that interrupt the enterohepatic cycle are used to treat high blood cholesterol. Examples: Synthetic resins, as well as soluble fiber (e.g., oat bran fiber and fruit pectin), that bind bile acids &/or cholesterol, prevent absorption/reabsorption. A recently introduced drug ezetimibe acts on cells lining the lumen of the small intestine to inhibit absorption of cholesterol. O H2C O C O O R1 HC O C O R2 H2C O C R3 triacylglycerol H2O H2C O HC O H2C C O R1 C R2 O O C R3 OH 1,2-diacylglycerol fatty acid Pancreatic lipase (secreted into the intestine), catalyzes hydrolysis of triacylglycerols at their 1 & 3 positions, forming 1,2-diacylglycerols, & then 2-monoacylglycerols (monoglycerides). A protein colipase is required to aid binding of the enzyme at the lipid-water interface. Monoacylglycerols and fatty acids are absorbed by intestinal epithelial cells. Within intestinal epithelial cells triacylglycerols are resynthesized. O Phospholipase A2 is secreted by the pancreas into the intestine. It hydrolyzes the ester linkage between the fatty acid & the hydroxyl on C2 of phospholipids. Lysophospholipids, the products of Phospholipase A2 reactions, are powerful detergents. O R2 C H2C O C C H O O CH2O R1 P O X O phospholipid H2O O HO H2C O C C H O CH2O P R1 O + O R2 C O X O lysophospholipid fatty acid Lysophospholipids, produced from phospholipids via Phospholipase A2, aid digestion of other lipids by breaking up fat globules into small micelles. Some phospholipid (lecithin) is secreted by the liver in the bile, presumably to provide substrate for Phospholipase A2 within the intestine and thus aid in fat digestion. Cobra & bee venoms contain Phospholipase A2. These venoms, injected into the blood, produce lysophospholipids that disrupt cell membranes and lyse blood cells. Cholesteryl Ester O R C O Within intestinal cells (and other body cells) some of the absorbed cholesterol is esterified to fatty acids, forming cholesteryl esters. (R = fatty acid hydrocarbon in diagram above) The enzyme that catalyzes cholesterol esterification is ACAT (Acyl CoA: Cholesterol Acyl Transferase). PDB 1ICM Within intestinal cells, fatty acids (which are poorly soluble & have detergent properties) are sequestered from the cytosol by being bound with intestinal fatty acid binding protein (I-FABP). I-FABP Fatty acid-binding proteins, which are in several cell types, have a ''b-clam" structure. A fatty acid is carried in a cavity between 2 approx. orthogonal b-sheets, each consisting of 5 antiparallel b-strands. Apoprotein B-100 Free fatty acids are transported in the blood bound to albumin, a serum protein secreted by liver. monolayer of phospholipid & cholesterol core: cholesteryl esters & some triacylglycerols LDL Most other lipids are transported in the blood as part of lipoproteins, complex particles whose structure includes: a core consisting of a droplet of triacylglycerols and/or cholesteryl esters a surface monolayer of phospholipid, cholesterol, & specific proteins (apolipoproteins), e.g., B-100. Lipoproteins differ in their contents of proteins and lipids. They are classified based on density. Chylomicron (largest; lowest in density due to high lipid/protein ratio; highest % weight triacylglycerols) VLDL (very low density lipoprotein; 2nd highest in triacylglycerols as % of weight) IDL (intermediate density lipoprotein) LDL (low density lipoprotein, highest in cholesteryl esters as % of weight) HDL (high density lipoprotein; highest in density due to high protein/lipid ratio) Apolipoproteins: Partial structures of some apolipoproteins are available. A common motif is amphipathic a-helices (polar along one surface & hydrophobic along the other side). These helices may float on the phospholipid surface of the lipoprotein. Other domains of apolipoproteins have roles in interaction of lipoproteins with cell surface receptors. PDB 1AV1 The lipid-binding domain of HDL apoprotein-A-I is an a-helix regularly interrupted by prolines to give a horseshoe shape. Lipid-binding domain of HDL Apolipoprotein A-I Hydrophobic residues run along one edge of the amphipathic a-helix. Antiparallel dimers form by association of hydrophobic residues, with chains offset to form an elliptical ring. Above right: hydrophobic = magenta; polar = cyan. Apoprotein-A-I dimers may wrap around the spherical HDL. Intestinal epithelial cells synthesize triacylglycerols, cholesteryl esters, phospholipids, free cholesterol, and apoproteins, and package them into chylomicrons. Chylomicrons are secreted by intestinal epithelial cells, and transported via the lymphatic system to the blood. Apoprotein CII on the chylomicron surface activates Lipoprotein Lipase, an enzyme attached to the lumenal surface of small blood vessels. Lipoprotein Lipase catalyzes hydrolytic cleavage of fatty acids from triacylglycerols of chylomicrons. Released fatty acids & monoacylglycerols are picked up by body cells for use as energy sources. As triacylglycerols are removed by hydrolysis, chylomicrons shrink in size, becoming chylomicron remnants with lipid cores having a relatively high concentration of cholesteryl esters. Chylomicron remnants are taken up by liver cells, via receptor-mediated endocytosis (to be discussed later). The process involves recognition of apoprotein E of the chylomicron remnant by receptors on the liver cell surface. Liver cells produce, and secrete into the blood, very low density lipoprotein (VLDL). The VLDL core has a relatively high triacylglycerol content. One of the apoproteins of VLDL is B-100. MTP (microsomal triglyceride transfer protein), in the lumen of the endoplasmic reticulum in liver, has an essential role in VLDL assembly. MTP facilitates transfer of lipids to apoprotein B-100 while B-100 is being translocated into the ER lumen during translation. Control of VLDL production: VLDL assembly is dependent on availability of lipids. Transcription of genes for enzymes that catalyze lipid synthesis is controlled by SREBP. Availability of apoprotein B-100 for VLDL assembly depends at least in part on regulated transfer of B-100 out of the ER for degradation via the proteasome. As VLDL particles are transported in the bloodstream, Lipoprotein Lipase catalyzes triacylglycerol removal by hydrolysis. With removal of triacylglycerols and some proteins, the % weight that is cholesteryl esters increases. VLDL are converted to IDL, and eventually to LDL. VLDL IDL LDL The lipid core of LDL is predominantly cholesteryl esters. Whereas VLDL contains 5 apoprotein types (B-100, C-I, C-II, C-III, & E), only one protein, apoprotein B-100, is associated with the surface monolayer of LDL. LDL extracellular space cytosol Cells take up LDL by receptor-mediated endocytosis. LDL receptor receptor-mediated endocytosis The cholesterol in LDL is then used by cells, e.g., for synthesis of cellular membranes. The LDL receptor was identified by M. Brown & J. Goldstein, who were awarded the Nobel prize. The LDL receptor is a single-pass transmembrane glycoprotein with a modular design. LDL extracellular space The cytosolic domain of the LDL receptor binds adapter proteins that mediate formation of a clathrin coat. cytosol This allows the receptor to be selected into budding vesicles. receptor-mediated endocytosis LDL receptor The LDL-binding domain on the exterior side of the plasma membrane recognizes & binds apoprotein B-100. Once the receptor with bound LDL is taken into a cell by endocytosis, the LDL-binding domain faces the lumen of the vesicle. The vesicle then fuses with an endosomal compartment. N- R1 R2 R3 R4 R5 R6 R7 EGF-A EGF-B b-propeller EGF-C GD TM Cyt -C Order of domains in primary structure of the LDL Receptor The N-terminal LDL-binding (apoprotein B-100binding) domain of the receptor consists of a series of cysteine-rich repeats (R1-R7), each of which is stabilized by 3 disulfide linkages and has a bound Ca++. Between the cysteine-rich repeats & the transmembrane (TM) segment are 3 epidermal growth factor-like domains (EGF-A, B, C) & a b-propeller. A domain subject to O-linked glysosylation (GD), between the innermost EGF domain & the transmembrane a-helix, may act as a spacer to extend the LDL-binding region out from the cell surface. PDB 1N7D b-propeller The long, flexible, modular structure allows association of N-terminal domains of the receptor with ligand on the surface of a lipoprotein that may vary in size. LDL receptor: LDL-binding domain Under acidic conditions of the endosome the b-propeller forms a complex with two of the cysteine-rich repeats. This causes the receptor to release LDL, which is then carried via a vesicle to a lysosome to be degraded. Regulation: Synthesis of LDL Receptor is suppressed by high intracellular cholesterol. This process involves decreased release of SREBP. Members of the SREBP family of transcription factors activate transcription of genes for the LDL receptor, as well as for enzymes essential to cholesterol synthesis such as HMG-CoA Reductase. The decreased synthesis of LDL receptor prevents excessive cholesterol uptake by cells. It has the deleterious consequence that excess dietary cholesterol remains in the blood as LDL. The lowered intracellular cholesterol that results from treatment with statin drugs, leads to activation of SREBP, increasing transcription of the gene for LDL receptor. Thus statins lower plasma cholesterol both by inhibiting HMG-CoA Reductase (decreasing cholesterol synthesis) and by promoting removal of LDL from the blood. Mutations affecting the LDL receptor are associated with the most common form of the disease familial hypercholesterolemia (high blood cholesterol). Cells lacking functional LDL receptors cannot take up LDL. As a result, the amount of circulating LDL increases, leading to enhanced risk of developing atherosclerosis. Other hereditary hypercholesterolemias relate to genetic defects in structure of apolipoproteins. E.g., familial defective apoprotein B100 leads to impaired binding of LDL to cell surface receptors, with elevated levels of circulating LDL. HDL (high density lipoprotein) is secreted as a small protein-rich particle by liver (and intestine). One HDL apoprotein, A-1, activates LCAT (LecithinCholesterol Acyl Transferase), which catalyzes synthesis of cholesteryl esters using fatty acids cleaved from the membrane lipid lecithin. The cholesterol is scavenged from cell surfaces & from other lipoproteins. HDL may transfer cholesteryl esters to other lipoproteins. Some remain associated with HDL, which may be taken up by liver & degraded. HDL thus transports cholesterol from tissues & other lipoproteins to the liver, which can excrete excess cholesterol as bile acids. High blood levels of HDL ("good" cholesterol) correlate with low incidence of atherosclerosis. Bacterial & viral infections, & some inflammatory disease states decrease HDL & increase VLDL production by the liver. These & other changes associated with inflammation can lead to increased risk of atherosclerosis if prolonged. blood vessel lumen elastic lamina endothelial cells smooth muscle cells Cell layers adjacent to the lumen of arterial blood vessel. Development of an atherosclerotic plaque: Various conditions can initiate formation of a lesion in the endothelium lining the arterial lumen. Inflammatory response, including cytokine production that may be activated by oxidized lipids present in LDL. Risk factors include elevated circulating LDL, high blood pressure, exposure to nicotine, etc. blood vessel lumen LDL endothelial cells foam cell smooth muscle cells Lipoproteins (e.g., LDL) leak across the endothelium and accumulate in the subendothelial space. Lipoproteins accumulate in part through binding to proteoglycans. Macrophages accumulate at the lesion and enter the subendothelial space. They ingest lipoproteins and appear as “foam cells” due to cytoplasmic lipid droplets. blood vessel lumen LDL endothelial cells foam cell smooth muscle cells Smooth muscle cells may also migrate into the subendothelial space & become foam cells. As foam cells eventually die, they may release harmful cellular contents that can contribute to rupturing of the plaque and development of blood clots.