Enhanced extracellular lipid accumulation in acidic environments

Current Opinion in Lipidology

Volumn 17, Issue 5, 2006, Pages 534-540

  Öörni, Katariina ^a   Kovanen, Petri T ^a  

^a WIHURI RESEARCH INSTITUTE   (Finland)

Author keywords

Acidic pH; Lipase; Lipoprotein; Protease; Proteoglycan

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ALPHA 1 ANTITRYPSIN; AMYLOID; AMYLOID BETA PROTEIN; APOLIPOPROTEIN; CD36 ANTIGEN; LOW DENSITY LIPOPROTEIN; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR A; SCAVENGER RECEPTOR BI; SERUM ALBUMIN; UNCLASSIFIED DRUG;

AGING; ATHEROMA; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CYTOTOXICITY; DIABETES MELLITUS; DIET; ENZYME MODIFICATION; HUMAN; INFLAMMATION; LIPID OXIDATION; MACROPHAGE ACTIVATION; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN GLYCOSYLATION; REVIEW;

ANOXIA; ATHEROSCLEROSIS; EXTRACELLULAR FLUID; HUMANS; HYDROGEN-ION CONCENTRATION; LIPASE; LIPID METABOLISM; LIPOPROTEINS, IDL; LIPOPROTEINS, LDL; LIPOPROTEINS, VLDL; OXIDATION-REDUCTION; PEPTIDE HYDROLASES; PROTEIN BINDING; PROTEOGLYCANS;

EID: 33748575321     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.mol.0000245259.63505.c2     Document Type: Review

References (54)

1. Öörni K, Pentikäinen MO, Ala-Korpela M, Kovanen PT. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J Lipid Res 2000; 41:1703-1714.
2. Nordestgaard BG, Wootton R, Lewis B. Selective retention of VLDL, IDL, and LDL in the arterial intima of genetically hyperlipidemic rabbits in vivo: molecular size as a determinant of fractional loss from the intima-inner media. Arterioscler Thromb Vasc Biol 1995; 15:534-542.
3. Skålen K, Gustafsson M, Rydberg EK, et al. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature 2002; 417:750-754.
4. Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol 1995; 15:551-561.
5. Williams KJ, Tabas I. The response-to-retention hypothesis of atherogenesis reinforced. Curr Opin Lipidol 1998; 9:471-474.
6. Pentikäinen MO, Oksjoki R, Öörni K, Kovanen PT. Lipoprotein lipase in the arterial wall: linking LDL to the arterial extracellular matrix and much more. Arterioscler Thromb Vasc Biol 2002; 22:211-217.
7. Björnheden T, Levin M, Evaldsson M, Wiklund O. Evidence of hypoxic areas within the arterial wall in vivo. Arterioscler Thromb Vasc Biol 1999; 19:870-876.
8. Leppänen O, Björnheden T, Evaldsson M, et al. ATP depletion in macrophages in the core of advanced rabbit atherosclerotic plaques in vivo. Atherosclerosis 2006; Jan 4 [Epub ahead of print] In this interesting study, bioluminescence imaging was used to map the concentrations of ATP, glucose, glycogen, and lactate and the presence of hypoxia in normal and atherosclerotic rabbit aortas in vivo. The article provides a metabolic link between hypoxia and increased lactate concentrations.
9. Khurana R, Simons M, Martin JF, Zachary IC. Role of angiogenesis in cardiovascular disease: a critical appraisal. Circulation 2005; 112:1813-1824.
10. Murdoch C, Muthana M, Lewis CE. Hypoxia regulates macrophage functions in inflammation. J Immunol 2005; 175:6257-6263. This excellent review article summarizes the many effects of hypoxia on macrophages in various inflamed, diseased tissues, including atherosclerotic plaques.
11. Leake DS. Does acidic pH explain why low density lipoprotein is oxidised in atherosclerotic lesions? Atherosclerosis 1997; 129:149-157.
12. Naghavi M, John R, Naguib S, et al. pH Heterogeneity of human and rabbit atherosclerotic plaques; a new insight into detection of vulnerable plaque. Atherosclerosis 2002; 164:27-35.
13. Björnheden T, Bondjers G. Oxygen consumption in aortic tissue from rabbits with diet-induced atherosclerosis. Arteriosclerosis 1987; 7:238-247.
14. Daugherty A, Dunn JL, Rateri DL, Heinecke JW. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J Clin Invest 1994; 94:437-444.
15. Maroudas A, Weinberg PD, Parker KH, Winlove CP. The distributions and diffusivities of small ions in chondroitin sulphate, hyaluronate and some proteoglycan solutions. Biophys Chem 1988; 32:257-270.
16. Punturieri A, Filippov S, Allen E, et al. Regulation of elastinolytic cysteine proteinase activity in normal and cathepsin K-deficient human macrophages. J Exp Med 2001; 192:789-799.
17. Öörni K, Posio P, Ala-Korpela M, et al. Sphingomyelinase induces aggregation and fusion of small very low-density lipoprotein and intermediate-density lipoprotein particles and increases their retention to human arterial proteoglycans. Arterioscler Thromb Vasc Biol 2005; 25:1678-1683. In this article, sphingomyelinase-induced particle aggregation was shown to enhance the binding of VLDL and IDL to proteoglycans, suggesting a novel mechanism for accumulation of these triglyceride-rich lipoproteins in atherosclerotic lesions.
18. Guyton JR, Klemp KF. Development of the atherosclerotic core region: chemical and ultrastructural analysis of microdissected atherosclerotic lesions from human aorta. Arterioscler Thromb 1994; 14:1305-1314.
19. Frank JS, Fogelman AM. Ultrastructure of the intima in WHHL and cholesterol-fed rabbit aortas prepared by ultra-rapid freezing and freeze-etching. J Lipid Res 1989; 30:967-978.
20. Hevonoja T, Pentikäinen MO, Hyvönen MT, et al. Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim Biophys Acta 2000; 1488:189-210.
21. Liu J, Sukhova GK, Sun JS, et al. Lysosomal cysteine proteases in atherosclerosis. Arterioscler Thromb Vasc Biol 2004; 24:1359-1366.
22. Dollery CM, Libby P. Atherosclerosis and proteinase activation. Cardiovasc Res 2006; 69:625-635. This comprehensive review article discusses the roles of various proteases, particularly matrix metalloproteinases, in atherosclerosis.
23. Jormsjö S, Wuttge DM, Sirsjö A, et al. Differential expression of cysteine and aspartic proteases during progression of atherosclerosis in apolipoprotein E-deficient mice. Am J Pathol 2002; 161:939-945.
24. Sukhova GK, Shi GP, Simon DI, et al. Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest 1998; 102:576-583.
25. Hakala JK, Oksjoki R, Laine P, et al. Lysosomal enzymes are released from cultured human macrophages, hydrolyze LDL in vitro, and are present extracellularly in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2003; 23:1430-1436.
26. Öörni K, Sneck M, Bromme D, et al. Cysteine protease cathepsin F is expressed in human atherosclerotic lesions, is secreted by cultured macrophages, and modifies low density lipoprotein particles in vitro. J Biol Chem 2004; 279:34776-34784.
27. Liu J, Sukhova GK, Yang JT, et al. Cathepsin L expression and regulation in human abdominal aortic aneurysm, atherosclerosis, and vascular cells. Atherosclerosis 2006; 184:302-311. The presence of cathepsin L in human atherosclerotic lesions was demonstrated in this study: the enzyme was found to colocalize with endothelial cells, smooth muscle cells, and macrophages in atherosclerotic lesions.
28. Reddy VY, Zhang QY, Weiss SJ. Pericellular modification of the tissue-destructive cysteine proteinases, cathepsins B, L, and S, by human monocyte-derived macrophages. Proc Natl Acad Sci U S A 1995; 92:3849-3853.
29. Shi GP, Sukhova GK, Grubb A, et al. Cystatin C deficiency in human atherosclerosis and aortic aneurysms. J Clin Invest 1999; 104:1191-1197.
30. Sukhova GK, Zhang Y, Pan JH, et al. Deficiency of cathepsin S reduces atherosclerosis in LDL receptor-deficient mice. J Clin Invest 2003; 111:897-906.
31. Sukhova GK, Wang B, Libby P, et al. Cystatin C deficiency increases elastic lamina degradation and aortic dilatation in apolipoprotein E-null mice. Circ Res 2005; 96:368-375.
32. Bengtsson E, To F, Grubb A, et al. Absence of the protease inhibitor cystatin C in inflammatory cells results in larger plaque area in plaque regression of apoE-deficient mice. Atherosclerosis 2005; 180:45-53.
33. Bengtsson E, To F, Håkansson K, et al. Lack of the cysteine protease inhibitor cystatin C promotes atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2005; 25:2151-2156. This study showed the atheroprotective role of an extracellular cysteine protease inhibitor, cystatin C, in apoE-deficient mice - a finding supporting the role of extracellular cysteine proteases in atherogenesis.
34. Liu J, Ma L, Yang J, et al. Increased serum cathepsin S in patients with atherosclerosis and diabetes. Atherosclerosis 2006; 186:411-419.
35. 2 in normal and atherosclerotic arteries: activity of the isolated enzyme on low-density lipoproteins. Arterioscler Thromb Vasc Biol 1997; 17:300-309.
36. Wooton-Kee CR, Boyanovsky BB, Nasser MS, et al. Group V sPLA2 hydrolysis of low-density lipoprotein results in spontaneous particle aggregation and promotes macrophage foam cell formation. Arterioscler Thromb Vasc Biol 2004; 24:762-767.
37. Rosengren B, Peilot H, Umaerus M, et al. Secretory phospholipase A2 group V. Lesion distribution, activation by arterial proteoglycans, and induction in aorta by a Western diet. Arterioscler Thromb Vasc Biol 2006; 26:1579-1585. This study compared PLA2 group IIa and group V in atherosclerosis. Interestingly, a Western diet was found to induce the expression of PLA2 group V and acute inflammation was found to increase the expression of PLA2 group IIa in mouse aortas.
38. Hanasaki K, Yamada K, Yamamoto S, et al. Potent modification of low density lipoprotein by group X secretory phospholipase A2 is linked to macrophage foam cell formation. J Biol Chem 2002; 277:29116-29124.
39. Ghesquiere SA, Gijbels MJ, Anthonsen M, et al. Macrophage-specific overexpression of group IIa sPLA2 increases atherosclerosis and enhances collagen deposition. J Lipid Res 2005; 46:201-210.
40. Menschikowski M, Hagelgans A, Siegert G. Secretory phospholipase A2 of group IIA: is it an offensive or a defensive player during atherosclerosis and other inflammatory diseases? Prostaglandins Other Lipid Mediat 2006; 79:1-33.
41. Boyanovsky BB, Van der Westhuyzen DR, Webb NR. Group V secretory phospholipase A2-modified low density lipoprotein promotes foam cell formation by a SR-A- and CD36-independent process that involves cellular proteoglycans. J Biol Chem 2005; 280:32746-32752.
42. 2+- stimulated sphingomyelinase is secreted by many cell types and is a product of the acid sphingomyelinase gene. J Biol Chem 1996; 271:18431-18436.
43. Marathe S, Kuriakose G, Williams KJ, Tabas I. Sphingomyelinase, an enzyme implicated in atherogenesis, is present in atherosclerotic lesions and binds to specific components of the subendothelial extracellular matrix. Arterioscler Thromb Vasc Biol 1999; 19:2648-2658.
44. Shamir R, Johnson WJ, Morlock-Fitzpatrick K, et al. Pancreatic carboxyl ester lipase: a circulating enzyme that modifies normal and oxidized lipoproteins in vitro. J Clin Invest 1996; 97:1696-1704.
45. Li F, Hui DY. Synthesis and secretion of the pancreatic-type carboxyl ester lipase by human endothelial cells. Biochem J 1998; 329:675-679.
46. Kodvawala A, Ghering AB, Davidson WS, Hui DY. Carboxyl ester lipase expression in macrophages increases cholesteryl ester accumulation and promotes atherosclerosis. J Biol Chem 2005; 280:38592-38598. The study provided a novel proatherogenic role for carboxyl ester lipase expressed in macrophages.
47. Han SR, Momeni A, Strach K, et al. Enzymatically modified LDL induces cathepsin H in human monocytes: potential relevance in early atherogenesis. Arterioscler Thromb Vasc Biol 2003; 23:661-667.
48. Torzewski M, Suriyaphol P, Paprotka K, et al. Enzymatic modification of lowdensity lipoprotein in the arterial wall: a new role for plasmin and matrix metalloproteinases in atherogenesis. Arterioscler Thromb Vasc Biol 2004; 24:2130-2136.
49. Öörni K, Pentikäinen MO, Annila A, Kovanen PT. Oxidation of low density lipoprotein particles decreases their ability to bind to human aortic proteoglycans: dependence on oxidative modification of the lysine residues. J Biol Chem 1997; 272:21303-21311.
50. Pfanzagl B. LDL oxidized with iron in the presence of homocysteine/cystine at acidic pH has low cytotoxicity despite high lipid peroxidation. Atherosclerosis 2006; 187:292-300.
51. Olin-Lewis K, Krauss RM, La Belle M, et al. ApoC-III content of apoB-containing lipoproteins is associated with binding to the vascular proteoglycan biglycan. J Lipid Res 2002; 43:1969-1977.
52. Anber V, Millar JS, McConnell M, et al. Interaction of very-low-density, intermediate-density, and low-density lipoproteins with human arterial wall proteoglycans. Arterioscler Thromb Vasc Biol 1997; 17:2507-2514.
53. Flood C, Gustafsson M, Pitas RE, et al. Molecular mechanism for changes in proteoglycan binding on compositional changes of the core and the surface of low-density lipoprotein-containing human apolipoprotein B100. Arterioscler Thromb Vasc Biol 2004; 24:564-570.
54. Sneck M, Kovanen PT, Öörni K. Decrease in pH strongly enhances binding of native, proteolyzed, lipolyzed, and oxidized low density lipoprotein particles to human aortic proteoglycans. J Biol Chem 2005; 280:37449-37454. Decrease in pH was found to enhance dramatically the binding of native and modified LDL to human aortic proteoglycans. This finding points to the possibility that lipoprotein retention is amplified at acidic pH.