ApoCIII-enriched LDL in type 2 diabetes displays altered lipid composition, increased susceptibility for sphingomyelinase, and increased binding to biglycan

Diabetes

Volumn 58, Issue 9, 2009, Pages 2018-2026

  Hiukka, Anne ^a   Ståhlman, Marcus ^b   Pettersson, Camilla ^b   Levin, Malin ^b   Adiels, Martin ^b   Teneberg, Susanne ^b   Leinonen, Eeva S ^a   Hultén, Lillemor Mattsson ^b   Wiklund, Olov ^b   Orešič, Matej ^c   Olofsson, Sven Olof ^b   Taskinen, Marja Riitta ^a   Ekroos, Kim ^d   Borén, Jan ^b  

^a HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^d Zora Biosciences   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B; APOLIPOPROTEIN C3; BIGLYCAN; CERAMIDE; CHOLESTEROL; CHOLESTEROL ESTER; ISOPROTEIN; LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLCHOLINE; SPHINGOMYELIN PHOSPHODIESTERASE; TRIACYLGLYCEROL;

ADULT; AGED; AORTA; ARTERY ENDOTHELIUM; ARTICLE; ATHEROGENESIS; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HYDROLYSIS; HYPERTRIGLYCERIDEMIA; INFLAMMATION; LIPID COMPOSITION; MAJOR CLINICAL STUDY; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SIALYLATION;

AGED; ANIMALS; APOLIPOPROTEIN C-III; APOLIPOPROTEINS B; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HUMANS; HYDROLYSIS; HYPERTRIGLYCERIDEMIA; LIPOPROTEINS, LDL; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; PROTEOGLYCANS; RISK FACTORS; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 70349120408     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0206     Document Type: Article

References (50)

1. Jong MC, Hofker MH, Havekes LM. Role of ApoCs in lipoprotein metabolism: functional differences between ApoC1, ApoC2, and ApoC3. Arterioscler Thromb Vasc Biol 1999;19:472-484
2. Campos H, Perlov D, Khoo C, Sacks FM. Distinct patterns of lipoproteins with apoB defined by presence of apoE or apoC-III in hypercholesterolemia and hypertriglyceridemia. J Lipid Res 2001;42:1239-1249 (Pubitemid 32744247)
3. Davidsson P, Hulthe J, Fagerberg B, Olsson BM, Hallberg C, Dahllof B, Camejo G. A proteomic study of the apolipoproteins in LDL subclasses in patients with the metabolic syndrome and type 2 diabetes. J Lipid Res 2005;46:1999-2006 (Pubitemid 41248497)
4. Sacks FM, Alaupovic P, Moye LA, Cole TG, Sussex B, Stampfer MJ, Pfeffer MA, Braunwald E. VLDL, apolipoproteins B, CIII, and E, and risk of recurrent coronary events in the Cholesterol and Recurrent Events (CARE) trial. Circulation 2000;102:1886-1892
5. Lee SJ, Campos H, Moye LA, Sacks FM. LDL containing apolipoprotein CIII is an independent risk factor for coronary events in diabetic patients. Arterioscler Thromb Vasc Biol 2003;23:853-858 (Pubitemid 36566177)
6. Pollin TI, Damcott CM, Shen H, Ott SH, Shelton J, Horenstein RB, Post W, McLenithan JC, Bielak LF, Peyser PA, Mitchell BD, Miller M, O'Connell JR, Shuldiner AR. A null mutation in human APOC3 confers a favorable plasma lipid profile and apparent cardioprotection. Science 2008;322:1702-1705
7. Wang C-S, McConathy WJ, Kloer HU, Alaupovic P. Modulation of lipoprotein lipase activity by apolipoproteins. Effect of apolipoprotein C-III. J Clin Invest 1985;75:384-390 (Pubitemid 15143476)
8. Kinnunen PKJ, Ehnholm C. Effect of serum and C-apoproteins from very low density lipoproteins on human postheparin plasma hepatic lipase. FEBS Lett 1976;65:354-357
9. Ebara T, Ramakrishnan R, Steiner G, Shachter NS. Chylomicronemia due to apolipoprotein CIII overexpression in apolipoprotein E-null mice. Apolipoprotein CIII-induced hypertriglyceridemia is not mediated by effects on apolipoprotein E. J Clin Invest 1997;99:2672-2681 (Pubitemid 27259814)
10. Zheng C, Khoo C, Ikewaki K, Sacks FM. Rapid turnover of apolipoprotein C-III-containing triglyceride-rich lipoproteins contributing to the formation of LDL subfractions J Lipid Res 2007;48:1190-1203
11. Cohn JS, Patterson BW, Uffelman KD, Davignon J, Steiner G. Rate of production of plasma and very-low-density lipoprotein (VLDL) apolipoprotein C-III is strongly related to the concentration and level of production of VLDL triglyceride in male subjects with different body weights and levels of insulin sensitivity. J Clin Endocrinol Metab 2004;89:3949-3955 (Pubitemid 39071498)
12. Kawakami A, Aikawa M, Alcaide P, Luscinskas FW, Libby P, Sacks FM. Apolipoprotein CIII induces expression of vascular cell adhesion molecule-1 in vascular endothelial cells and increases adhesion of monocytic cells. Circulation 2006;114:681-687 (Pubitemid 44252310)
13. Kawakami A, Aikawa M, Nitta N, Yoshida M, Libby P, Sacks FM. Apolipoprotein CIII-induced THP-1 cell adhesion to endothelial cells involves pertussis toxin-sensitive G protein- and protein kinase C α-mediated nuclear factor-κB activation. Arterioscler Thromb Vasc Biol 2007;27:219-225 (Pubitemid 46360402)
14. Olin-Lewis K, Krauss RM, La Belle M, Blanche PJ, Barrett PH, Wight TN, Chait A. ApoC-III content of apoB-containing lipoproteins is associated with binding to the vascular proteoglycan biglycan. J Lipid Res 2002;43:1969-1977 (Pubitemid 35315815)
15. Boren J, Olin K, Lee I, Chait A, Wight TN, Innerarity TL. Identification of the principal proteoglycan-binding site in LDL. A single-point mutation in apo-B100 severely affects proteoglycan interaction without affecting LDL receptor binding. J Clin Invest 1998;101:2658-2664 (Pubitemid 28294574)
16. Schissel SL, Jiang X, Tweedie-Hardman J, Jeong T, Camejo EH, Najib J, Rapp JH, Williams KJ, Tabas I. Secretory sphingomyelinase, a product of the acid sphingomyelinase gene, can hydrolyze atherogenic lipoproteins at neutral pH. Implications for atherosclerotic lesion development. J Biol Chem 1998;273:2738-2746 (Pubitemid 28133919)
17. Ahmad TY, Beaudet AL, Sparrow JT, Morrisett JD. Human lysosomal sphingomyelinase: substrate efficacy of apolipoprotein/sphingomyelin complexes. Biochemistry 1986;25:4415-4420
18. Ito Y, Breslow JL, Chait BT. Apolipoprotein C-III0 lacks carbohydrate residues: use of mass spectrometry to study apolipoprotein structure. J Lipid Res 1989;30:1781-1787 (Pubitemid 20024857)
19. Wopereis S, Grunewald S, Morava E, Penzien JM, Briones P, Garcia-Silva MT, Demacker PN, Huijben KM, Wevers RA. Apolipoprotein C-III isofocusing in the diagnosis of genetic defects in O-glycan biosynthesis. Clin Chem 2003;49:1839-1845 (Pubitemid 37340318)
20. Holdsworth G, Stocks J, Dodson P, Galton DJ. An abnormal triglyceride-rich lipoprotein containing excess sialylated apolipoprotein C-III. J Clin Invest 1982;69:932-939
21. Mann CJ, Troussard AA, Yen FT, Hannouche N, Najib J, Fruchart JC, Lotteau V, Andre P, Bihain BE. Inhibitory effects of specific apolipoprotein C-III isoforms on the binding of triglyceride-rich lipoproteins to the lipolysis-stimulated receptor. J Biol Chem 1997;272:31348-31354 (Pubitemid 28013269)
22. Mauger JF, Couture P, Bergeron N, Lamarche B. Apolipoprotein C-III isoforms: kinetics and relative implication in lipid metabolism. J Lipid Res 2006;47:1212-1218 (Pubitemid 43830713)
23. Hiukka A, Leinonen E, Jauhiainen M, Sundvall J, Ehnholm C, Keech AC, Taskinen MR. Long-term effects of fenofibrate on VLDL and HDL subspecies in participants with type 2 diabetes mellitus. Diabetologia 2007;50:2067-2075 (Pubitemid 47373844)
24. Taskinen MR, Kuusi T, Helve E, Nikkila EA, Yki-Jarvinen H. Insulin therapy induces antiatherogenic changes of serum lipoproteins in noninsulin-dependent diabetes. Arteriosclerosis 1988;8:168-177 (Pubitemid 18090925)
25. Griffin BA, Caslake MJ, Yip B, Tait GW, Packard CJ, Shepherd J. Rapid isolation of low density lipoprotein (LDL) subfractions from plasma by density gradient ultracentrifugation. Atherosclerosis 1990;83:59-67 (Pubitemid 20210746)
26. Boren J, Lee I, Zhu W, Arnold K, Taylor S, Innerarity TL. Identification of the low density lipoprotein receptor-binding site in apolipoprotein B100 and the modulation of its binding activity by the carboxyl terminus in familial defective apo-B100. J Clin Invest 1998;101:1084-1093 (Pubitemid 28125287)
27. Stahlman M, Davidsson P, Kanmert I, Rosengren B, Boren J, Fagerberg B, Camejo G. Proteomics and lipids of lipoproteins isolated at low salt concentrations in D2O/sucrose or in KBr. J Lipid Res 2008;49:481-490 (Pubitemid 351213633)
28. Skalen K, Gustafsson M, Rydberg EK, Hulten LM, Wiklund O, Innerarity TL, Boren J. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature 2002;417:750-754 (Pubitemid 34640629)
29. Ekroos K, Chernushevich IV, Simons K, Shevchenko A. Quantitative profiling of phospholipids by multiple precursor ion scanning on a hybrid quadrupole time-of-flight mass spectrometer. Anal Chem 2002;74:941-949 (Pubitemid 34203015)
30. Homan R, Anderson MK. Rapid separation and quantitation of combined neutral and polar lipid classes by high-performance liquid chromatography and evaporative light-scattering mass detection. J Chromatogr B Biomed Sci Appl 1998;708:21-26
31. Wang WQ, Gustafson A. Ganglioside extraction from erythrocytes: a comparison study. Acta Chem Scand 1995;49:929-936
32. Teneberg S, Hirst TR, Angstrom J, Karlsson KA. Comparison of the glycolipid-binding specificities of cholera toxin and porcine Escherichia coli heat-labile enterotoxin: identification of a receptor-active non-ganglioside glycolipid for the heat-labile toxin in infant rabbit small intestine. Glycoconj J 1994;11:533-540
33. Schissel SL, Tweedie-Hardman J, Rapp JH, Graham G, Williams KJ, Tabas I. Rabbit aorta and human atherosclerotic lesions hydrolyze the sphingomyelin of retained low-density lipoprotein. Proposed role for arterial-wall sphingomyelinase in subendothelial retention and aggregation of atherogenic lipoproteins. J Clin Invest 1996;98:1455-1464 (Pubitemid 26322072)
34. Oorni K, Posio P, Ala-Korpela M, Jauhiainen M, Kovanen PT. 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 (Pubitemid 41098940)
35. Flood C, Gustafsson M, Pitas RE, Arnaboldi L, Walzem RL, Boren J. 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 (Pubitemid 38326154)
36. Khoo C, Campos H, Judge H, Sacks FM. Effects of estrogenic oral contraceptives on the lipoprotein B particle system defined by apolipoproteins E and C-III content. J Lipid Res 1999;40:202-212 (Pubitemid 29069793)
37. Aviram M, Lund-Katz S, Phillips MC, Chait A. The influence of the triglyceride content of low density lipoprotein on the interaction of apolipoprotein B-100 with cells. J Biol Chem 1988;263:16842-16848 (Pubitemid 18268867)
38. Gupta AK, Rudney H. Sphingomyelinase treatment of low density lipoprotein and cultured cells results in enhanced processing of LDL which can be modulated by sphingomyelin. J Lipid Res 1992;33:1741-1752 (Pubitemid 23006651)
39. Ibdah JA, Lund-Katz S, Phillips MC. Molecular packing of high-density and low-density lipoprotein surface lipids and apolipoprotein A-I binding. Biochemistry 1989;28:1126-1133
40. Sola R, Baudet MF, Motta C, Maille M, Boisnier C, Jacotot B. Effects of dietary fats on the fluidity of human high-density lipoprotein: influence of the overall composition and phospholipid fatty acids. Biochim Biophys Acta 1990;1043:43-51 (Pubitemid 20083743)
41. Hevonoja T, Pentikinen MO, Hyvönen MT, Kovanen PT, Ala-Korpela M. Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochimica Biophysica Acta 2000;1488:189-210 (Pubitemid 30811892)
42. Gorska M, Baranczuk E, Dobrzyn A. Secretory Zn2+-dependent sphingomyelinase activity in the serum of patients with type 2 diabetes is elevated. Horm Metab Res 2003;35:506-507 (Pubitemid 37204569)
43. Ohvo H, Olsio C, Slotte JP. Effects of sphingomyelin and phosphatidylcholine degradation on cyclodextrin-mediated cholesterol efflux in cultured fibroblasts. Biochim Biophys Acta 1997;1349:131-141 (Pubitemid 27519555)
44. Van Heek M, Compton DS, France CF, Tedesco RP, Fawzi AB, Graziano MP, Sybertz EJ, Strader CD, Davis HR Jr. Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J Clin Invest 1997 99:385-390 (Pubitemid 27414794)
45. Oestvang J, Bonnefont-Rousselot D, Ninio E, Hakala JK, Johansen B, Anthonsen MW. Modification of LDL with human secretory phospholipase A(2) or sphingomyelinase promotes its arachidonic acid-releasing propensity. J Lipid Res 2004;45:831-838
46. Fanani ML, Maggio B. Mutual modulation of sphingomyelinase and phospholipase A2 activities against mixed lipid monolayers by their lipid intermediates and glycosphingolipids. Mol Membr Biol 1997;14:25-29 (Pubitemid 27219904)
47. Gesquiere L, Cho W, Subbaiah PV. Role of group IIa and group V secretory phospholipases A(2) in the metabolism of lipoproteins. Substrate specificities of the enzymes and the regulation of their activities by sphingomyelin. Biochemistry 2002;41:4911-4920
48. Bostrom MA, Boyanovsky BB, Jordan CT, Wadsworth MP, Taatjes DJ, de Beer FC, Webb NR. Group v secretory phospholipase A2 promotes atherosclerosis: evidence from genetically altered mice. Arterioscler Thromb Vasc Biol 2007;27:600-606
49. Sartipy P, Camejo G, Svensson L, Hurt-Camejo E. Phospholipase A(2) modification of low density lipoproteins forms small high density particles with increased affinity for proteoglycans and glycosaminoglycans. J Biol Chem 1999;274:25913-25920 (Pubitemid 129530773)
50. Lee SJ, Moye LA, Campos H, Williams GH, Sacks FM. Hypertriglyceridemia but not diabetes status is associated with VLDL containing apolipoprotein CIII in patients with coronary heart disease. Atherosclerosis 2003;167:293-302 (Pubitemid 36773529)