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Erschienen in: Current Atherosclerosis Reports 9/2014

01.09.2014 | Rare Diseases and Lipid Metabolism (JAG López, Section Editor)

Hyperlipoproteinemia Type 3: The Forgotten Phenotype

verfasst von: Paul N. Hopkins, Eliot A. Brinton, M. Nazeem Nanjee

Erschienen in: Current Atherosclerosis Reports | Ausgabe 9/2014

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Abstract

Hyperlipoproteinemia type 3 (HLP3) is caused by impaired removal of triglyceride-rich lipoproteins (TGRL) leading to accumulation of TGRL remnants with abnormal composition. High levels of these remnants, called β-VLDL, promote lipid deposition in tuberous xanthomas, atherosclerosis, premature coronary artery disease, and early myocardial infarction. Recent genetic and molecular studies suggest more genes than previously appreciated may contribute to the expression of HLP3, both through impaired hepatic TGRL processing or removal and increased TGRL production. HLP3 is often highly amenable to appropriate treatment. Nevertheless, most HLP3 probably goes undiagnosed, in part because of lack of awareness of the relatively high prevalence (about 0.2 % in women and 0.4–0.5 % in men older than 20 years) and largely because of infrequent use of definitive diagnostic methods.
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Zurück zum Zitat MacArthur JM, Bishop JR, Stanford KI, et al. Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J Clin Invest. 2007;117(1):153–64.PubMedCentralPubMed MacArthur JM, Bishop JR, Stanford KI, et al. Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J Clin Invest. 2007;117(1):153–64.PubMedCentralPubMed
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Zurück zum Zitat Stanford KI, Wang L, Castagnola J, et al. Heparan sulfate 2-O-sulfotransferase is required for triglyceride-rich lipoprotein clearance. J Biol Chem. 2010;285(1):286–94.PubMedCentralPubMed Stanford KI, Wang L, Castagnola J, et al. Heparan sulfate 2-O-sulfotransferase is required for triglyceride-rich lipoprotein clearance. J Biol Chem. 2010;285(1):286–94.PubMedCentralPubMed
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Zurück zum Zitat Chen K, Liu ML, Schaffer L, et al. Type 2 diabetes in mice induces hepatic overexpression of sulfatase 2, a novel factor that suppresses uptake of remnant lipoproteins. Hepatology. 2010;52(6):1957–67.PubMedCentralPubMed Chen K, Liu ML, Schaffer L, et al. Type 2 diabetes in mice induces hepatic overexpression of sulfatase 2, a novel factor that suppresses uptake of remnant lipoproteins. Hepatology. 2010;52(6):1957–67.PubMedCentralPubMed
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Zurück zum Zitat Moennig G, Wiebusch H, Enbergs A, et al. Detection of missense mutations in the genes for lipoprotein lipase and hepatic triglyceride lipase in patients with dyslipidemia undergoing coronary angiography. Atherosclerosis. 2000;149(2):395–401.PubMed Moennig G, Wiebusch H, Enbergs A, et al. Detection of missense mutations in the genes for lipoprotein lipase and hepatic triglyceride lipase in patients with dyslipidemia undergoing coronary angiography. Atherosclerosis. 2000;149(2):395–401.PubMed
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Zurück zum Zitat Hegele RA, Little JA, Vezina C, et al. Hepatic lipase deficiency. Clinical, biochemical, and molecular genetic characteristics. Arterioscler Thromb. 1993;13(5):720–8.PubMed Hegele RA, Little JA, Vezina C, et al. Hepatic lipase deficiency. Clinical, biochemical, and molecular genetic characteristics. Arterioscler Thromb. 1993;13(5):720–8.PubMed
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Zurück zum Zitat Zambon A, Deeb SS, Bensadoun A, Foster KE, Brunzell JD. In vivo evidence of a role for hepatic lipase in human apoB-containing lipoprotein metabolism, independent of its lipolytic activity. J Lipid Res. 2000;41(12):2094–9.PubMed Zambon A, Deeb SS, Bensadoun A, Foster KE, Brunzell JD. In vivo evidence of a role for hepatic lipase in human apoB-containing lipoprotein metabolism, independent of its lipolytic activity. J Lipid Res. 2000;41(12):2094–9.PubMed
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Zurück zum Zitat Matsunaga A, Saito T. Apolipoprotein E mutations: a comparison between lipoprotein glomerulopathy and type III hyperlipoproteinemia. Clin Exp Nephrol. 2014;18(2):220–4.PubMed Matsunaga A, Saito T. Apolipoprotein E mutations: a comparison between lipoprotein glomerulopathy and type III hyperlipoproteinemia. Clin Exp Nephrol. 2014;18(2):220–4.PubMed
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Zurück zum Zitat Civeira F, Pocovi M, Cenarro A, et al. Apo E variants in patients with type III hyperlipoproteinemia. Atherosclerosis. 1996;127(2):273–82.PubMed Civeira F, Pocovi M, Cenarro A, et al. Apo E variants in patients with type III hyperlipoproteinemia. Atherosclerosis. 1996;127(2):273–82.PubMed
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Zurück zum Zitat Abou Ziki MD, Strulovici-Barel Y, Hackett NR, et al. Prevalence of the apolipoprotein E Arg145Cys dyslipidemia at-risk polymorphism in African-derived populations. Am J Cardiol. 2014;113(2):302–8.PubMed Abou Ziki MD, Strulovici-Barel Y, Hackett NR, et al. Prevalence of the apolipoprotein E Arg145Cys dyslipidemia at-risk polymorphism in African-derived populations. Am J Cardiol. 2014;113(2):302–8.PubMed
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Zurück zum Zitat Pocovi M, Cenarro A, Civeira F, et al. Incomplete dominance of type III hyperlipoproteinemia is associated with the rare apolipoprotein E2 (Arg136 → Ser) variant in multigenerational pedigree studies. Atherosclerosis. 1996;122(1):33–46.PubMed Pocovi M, Cenarro A, Civeira F, et al. Incomplete dominance of type III hyperlipoproteinemia is associated with the rare apolipoprotein E2 (Arg136 → Ser) variant in multigenerational pedigree studies. Atherosclerosis. 1996;122(1):33–46.PubMed
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Zurück zum Zitat Foley EM, Gordts PL, Stanford KI, et al. Hepatic remnant lipoprotein clearance by heparan sulfate proteoglycans and low-density lipoprotein receptors depend on dietary conditions in mice. Arterioscler Thromb Vasc Biol. 2013;33(9):2065–74.PubMed Foley EM, Gordts PL, Stanford KI, et al. Hepatic remnant lipoprotein clearance by heparan sulfate proteoglycans and low-density lipoprotein receptors depend on dietary conditions in mice. Arterioscler Thromb Vasc Biol. 2013;33(9):2065–74.PubMed
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Zurück zum Zitat Jones C, Garuti R, Michaely P, et al. Disruption of LDL but not VLDL clearance in autosomal recessive hypercholesterolemia. J Clin Invest. 2007;117(1):165–74.PubMedCentralPubMed Jones C, Garuti R, Michaely P, et al. Disruption of LDL but not VLDL clearance in autosomal recessive hypercholesterolemia. J Clin Invest. 2007;117(1):165–74.PubMedCentralPubMed
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Zurück zum Zitat Hopkins PN, Wu LL, Schumacher MC, et al. Type III dyslipoproteinemia in patients heterozygous for familial hypercholesterolemia and apolipoprotein E2. Evidence for a gene-gene interaction. Arterioscler Thromb. 1991;11(5):1137–46.PubMed Hopkins PN, Wu LL, Schumacher MC, et al. Type III dyslipoproteinemia in patients heterozygous for familial hypercholesterolemia and apolipoprotein E2. Evidence for a gene-gene interaction. Arterioscler Thromb. 1991;11(5):1137–46.PubMed
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Zurück zum Zitat Hopkins PN, Stephenson S, Wu LL, Riley WA, Xin Y, Hunt SC. Evaluation of coronary risk factors in patients with heterozygous familial hypercholesterolemia. Am J Cardiol. 2001;87(5):547–53.PubMed Hopkins PN, Stephenson S, Wu LL, Riley WA, Xin Y, Hunt SC. Evaluation of coronary risk factors in patients with heterozygous familial hypercholesterolemia. Am J Cardiol. 2001;87(5):547–53.PubMed
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Zurück zum Zitat Carmena R, Roy M, Roederer G, Minnich A, Davignon J. Coexisting dysbetalipoproteinemia and familial hypercholesterolemia. Clinical and laboratory observations. Atherosclerosis. 2000;148(1):113–24.PubMed Carmena R, Roy M, Roederer G, Minnich A, Davignon J. Coexisting dysbetalipoproteinemia and familial hypercholesterolemia. Clinical and laboratory observations. Atherosclerosis. 2000;148(1):113–24.PubMed
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Zurück zum Zitat Olofsson SO, Bostrom P, Andersson L, Rutberg M, Perman J, Boren J. Lipid droplets as dynamic organelles connecting storage and efflux of lipids. Biochim Biophys Acta. 2009;1791(6):448–58.PubMed Olofsson SO, Bostrom P, Andersson L, Rutberg M, Perman J, Boren J. Lipid droplets as dynamic organelles connecting storage and efflux of lipids. Biochim Biophys Acta. 2009;1791(6):448–58.PubMed
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Zurück zum Zitat Yao Z, Zhou H, Figeys D, Wang Y, Sundaram M. Microsome-associated lumenal lipid droplets in the regulation of lipoprotein secretion. Curr Opin Lipidol. 2013;24(2):160–70.PubMed Yao Z, Zhou H, Figeys D, Wang Y, Sundaram M. Microsome-associated lumenal lipid droplets in the regulation of lipoprotein secretion. Curr Opin Lipidol. 2013;24(2):160–70.PubMed
75.•
Zurück zum Zitat Olofsson SO, Boren J. Apolipoprotein B secretory regulation by degradation. Arterioscler Thromb Vasc Biol. 2012;32(6):1334–8. This is a useful summary of newer understanding of VLDL assembly and secretion.PubMed Olofsson SO, Boren J. Apolipoprotein B secretory regulation by degradation. Arterioscler Thromb Vasc Biol. 2012;32(6):1334–8. This is a useful summary of newer understanding of VLDL assembly and secretion.PubMed
76.•
Zurück zum Zitat Qin W, Sundaram M, Wang Y, et al. Missense mutation in APOC3 within the C-terminal lipid binding domain of human ApoC-III results in impaired assembly and secretion of triacylglycerol-rich very low density lipoproteins: evidence that ApoC-III plays a major role in the formation of lipid precursors within the microsomal lumen. J Biol Chem. 2011;286(31):27769–80. This is an important advance in the understanding of APOC3 as a factor involved within hepatocytes that helps control secretion of VLDL. Relevance to HLP3 specifically remains unknown.PubMedCentralPubMed Qin W, Sundaram M, Wang Y, et al. Missense mutation in APOC3 within the C-terminal lipid binding domain of human ApoC-III results in impaired assembly and secretion of triacylglycerol-rich very low density lipoproteins: evidence that ApoC-III plays a major role in the formation of lipid precursors within the microsomal lumen. J Biol Chem. 2011;286(31):27769–80. This is an important advance in the understanding of APOC3 as a factor involved within hepatocytes that helps control secretion of VLDL. Relevance to HLP3 specifically remains unknown.PubMedCentralPubMed
77.•
Zurück zum Zitat Caron S, Verrijken A, Mertens I, et al. Transcriptional activation of apolipoprotein CIII expression by glucose may contribute to diabetic dyslipidemia. Arterioscler Thromb Vasc Biol. 2011;31(3):513–9. This is also an important study for understanding the role of APOC3 in determining VLDL secretion. It may provide understanding of the effects of poorly controlled diabetes on hypertriglyceridemia in general and possibly expression of HLP3.PubMed Caron S, Verrijken A, Mertens I, et al. Transcriptional activation of apolipoprotein CIII expression by glucose may contribute to diabetic dyslipidemia. Arterioscler Thromb Vasc Biol. 2011;31(3):513–9. This is also an important study for understanding the role of APOC3 in determining VLDL secretion. It may provide understanding of the effects of poorly controlled diabetes on hypertriglyceridemia in general and possibly expression of HLP3.PubMed
77.
Zurück zum Zitat Cohn JS, Tremblay M, Batal R, et al. Increased apoC-III production is a characteristic feature of patients with hypertriglyceridemia. Atherosclerosis. 2004;177(1):137–45.PubMed Cohn JS, Tremblay M, Batal R, et al. Increased apoC-III production is a characteristic feature of patients with hypertriglyceridemia. Atherosclerosis. 2004;177(1):137–45.PubMed
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Zurück zum Zitat Mendivil CO, Zheng C, Furtado J, Lel J, Sacks FM. Metabolism of very-low-density lipoprotein and low-density lipoprotein containing apolipoprotein C-III and not other small apolipoproteins. Arterioscler Thromb Vasc Biol. 2010;30(2):239–45.PubMedCentralPubMed Mendivil CO, Zheng C, Furtado J, Lel J, Sacks FM. Metabolism of very-low-density lipoprotein and low-density lipoprotein containing apolipoprotein C-III and not other small apolipoproteins. Arterioscler Thromb Vasc Biol. 2010;30(2):239–45.PubMedCentralPubMed
80.•
Zurück zum Zitat Verhague MA, Cheng D, Weinberg RB, Shelness GS. Apolipoprotein A-IV expression in mouse liver enhances triglyceride secretion and reduces hepatic lipid content by promoting very low density lipoprotein particle expansion. Arterioscler Thromb Vasc Biol. 2013;33(11):2501–8. This study provides insight into an intracellular role for APOA4 with regard to hypertriglyceridemia in general, but relevance to HLP3 expression awaits further study.PubMed Verhague MA, Cheng D, Weinberg RB, Shelness GS. Apolipoprotein A-IV expression in mouse liver enhances triglyceride secretion and reduces hepatic lipid content by promoting very low density lipoprotein particle expansion. Arterioscler Thromb Vasc Biol. 2013;33(11):2501–8. This study provides insight into an intracellular role for APOA4 with regard to hypertriglyceridemia in general, but relevance to HLP3 expression awaits further study.PubMed
80.
Zurück zum Zitat Blade AM, Fabritius MA, Hou L, Weinberg RB, Shelness GS. Biogenesis of apolipoprotein A-V and its impact on VLDL triglyceride secretion. J Lipid Res. 2011;52(2):237–44.PubMedCentralPubMed Blade AM, Fabritius MA, Hou L, Weinberg RB, Shelness GS. Biogenesis of apolipoprotein A-V and its impact on VLDL triglyceride secretion. J Lipid Res. 2011;52(2):237–44.PubMedCentralPubMed
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Zurück zum Zitat Grosskopf I, Shaish A, Afek A, Shemesh S, Harats D, Kamari Y. Apolipoprotein A-V modulates multiple atherogenic mechanisms in a mouse model of disturbed clearance of triglyceride-rich lipoproteins. Atherosclerosis. 2012;224(1):75–83. This study suggested an antiatherogenic role for APOA5 due to decreased VLDL production, but relevance to HLP3 expression awaits further study.PubMed Grosskopf I, Shaish A, Afek A, Shemesh S, Harats D, Kamari Y. Apolipoprotein A-V modulates multiple atherogenic mechanisms in a mouse model of disturbed clearance of triglyceride-rich lipoproteins. Atherosclerosis. 2012;224(1):75–83. This study suggested an antiatherogenic role for APOA5 due to decreased VLDL production, but relevance to HLP3 expression awaits further study.PubMed
83.•
Zurück zum Zitat Andreo U, Guo L, Chirieac DV, et al. Insulin-stimulated degradation of apolipoprotein B100: roles of class II phosphatidylinositol-3-kinase and autophagy. PLoS ONE. 2013;8(3):e57590. This provides important insights into control of VLDL secretion and the mechanism for inhibition of VLDL secretion, particularly VLDL1, by normal acute action of insulin and the adverse effect of insulin resistance. Importance in the setting of HLP3 remains unknown.PubMedCentralPubMed Andreo U, Guo L, Chirieac DV, et al. Insulin-stimulated degradation of apolipoprotein B100: roles of class II phosphatidylinositol-3-kinase and autophagy. PLoS ONE. 2013;8(3):e57590. This provides important insights into control of VLDL secretion and the mechanism for inhibition of VLDL secretion, particularly VLDL1, by normal acute action of insulin and the adverse effect of insulin resistance. Importance in the setting of HLP3 remains unknown.PubMedCentralPubMed
84.•
Zurück zum Zitat Maitin V, Andreo U, Guo L, Fisher EA. Docosahexaenoic acid impairs the maturation of very low density lipoproteins in rat hepatic cells. J Lipid Res. 2014;55(1):75–84. This provides a mechanistic explanation for the TG-lowering effects of fish oil or omega-3 fatty acids.PubMed Maitin V, Andreo U, Guo L, Fisher EA. Docosahexaenoic acid impairs the maturation of very low density lipoproteins in rat hepatic cells. J Lipid Res. 2014;55(1):75–84. This provides a mechanistic explanation for the TG-lowering effects of fish oil or omega-3 fatty acids.PubMed
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Zurück zum Zitat Al-Shayji IA, Gill JM, Cooney J, Siddiqui S, Caslake MJ. Development of a novel method to determine very low density lipoprotein kinetics. J Lipid Res. 2007;48(9):2086–95.PubMed Al-Shayji IA, Gill JM, Cooney J, Siddiqui S, Caslake MJ. Development of a novel method to determine very low density lipoprotein kinetics. J Lipid Res. 2007;48(9):2086–95.PubMed
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Zurück zum Zitat Adiels M, Olofsson SO, Taskinen MR, Boren J. Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler Thromb Vasc Biol. 2008;28(7):1225–36.PubMed Adiels M, Olofsson SO, Taskinen MR, Boren J. Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler Thromb Vasc Biol. 2008;28(7):1225–36.PubMed
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Zurück zum Zitat Sparks JD, Sparks CE, Adeli K. Selective hepatic insulin resistance, VLDL overproduction, and hypertriglyceridemia. Arterioscler Thromb Vasc Biol. 2012;32(9):2104–12.PubMed Sparks JD, Sparks CE, Adeli K. Selective hepatic insulin resistance, VLDL overproduction, and hypertriglyceridemia. Arterioscler Thromb Vasc Biol. 2012;32(9):2104–12.PubMed
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Zurück zum Zitat Verges B, Florentin E, Baillot-Rudoni S, et al. Effects of 20 mg rosuvastatin on VLDL1-, VLDL2-, IDL- and LDL-ApoB kinetics in type 2 diabetes. Diabetologia. 2008;51(8):1382–90.PubMed Verges B, Florentin E, Baillot-Rudoni S, et al. Effects of 20 mg rosuvastatin on VLDL1-, VLDL2-, IDL- and LDL-ApoB kinetics in type 2 diabetes. Diabetologia. 2008;51(8):1382–90.PubMed
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Zurück zum Zitat Duvillard L, Caslake MJ, Petit JM, Verges B, Gambert P, Packard CJ. Distinct patterns of heparin affinity chromatography VLDL1 and VLDL2 subfractions in the different dyslipidaemias. Atherosclerosis. 2008;199(1):27–33.PubMed Duvillard L, Caslake MJ, Petit JM, Verges B, Gambert P, Packard CJ. Distinct patterns of heparin affinity chromatography VLDL1 and VLDL2 subfractions in the different dyslipidaemias. Atherosclerosis. 2008;199(1):27–33.PubMed
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Zurück zum Zitat Palmer AM, Nova E, Anil E, et al. Differential uptake of subfractions of triglyceride-rich lipoproteins by THP-1 macrophages. Atherosclerosis. 2005;180(2):233–44.PubMed Palmer AM, Nova E, Anil E, et al. Differential uptake of subfractions of triglyceride-rich lipoproteins by THP-1 macrophages. Atherosclerosis. 2005;180(2):233–44.PubMed
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Zurück zum Zitat Bjorkegren J, Karpe F, Vitols S, Tornvall P, Hamsten A. Transient triglyceridemia in healthy normolipidemic men increases cellular processing of large very low density lipoproteins by fibroblasts in vitro. J Lipid Res. 1998;39(2):423–36.PubMed Bjorkegren J, Karpe F, Vitols S, Tornvall P, Hamsten A. Transient triglyceridemia in healthy normolipidemic men increases cellular processing of large very low density lipoproteins by fibroblasts in vitro. J Lipid Res. 1998;39(2):423–36.PubMed
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Zurück zum Zitat Kawakami A, Osaka M, Aikawa M, et al. Toll-like receptor 2 mediates apolipoprotein CIII-induced monocyte activation. Circ Res. 2008;103(12):1402–9.PubMedCentralPubMed Kawakami A, Osaka M, Aikawa M, et al. Toll-like receptor 2 mediates apolipoprotein CIII-induced monocyte activation. Circ Res. 2008;103(12):1402–9.PubMedCentralPubMed
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Zurück zum Zitat Demant T, Bedford D, Packard CJ, Shepherd J. Influence of apolipoprotein E polymorphism on apolipoprotein B-100 metabolism in normolipemic subjects. J Clin Invest. 1991;88:1490–501.PubMedCentralPubMed Demant T, Bedford D, Packard CJ, Shepherd J. Influence of apolipoprotein E polymorphism on apolipoprotein B-100 metabolism in normolipemic subjects. J Clin Invest. 1991;88:1490–501.PubMedCentralPubMed
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Zurück zum Zitat Batal R, Tremblay M, Barrett PH, et al. Plasma kinetics of apoC-III and apoE in normolipidemic and hypertriglyceridemic subjects. J Lipid Res. 2000;41(5):706–18.PubMed Batal R, Tremblay M, Barrett PH, et al. Plasma kinetics of apoC-III and apoE in normolipidemic and hypertriglyceridemic subjects. J Lipid Res. 2000;41(5):706–18.PubMed
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Zurück zum Zitat Ooi EM, Janus ED, Grant SJ, Sinclair LM, Barrett PHR. Effect of apolipoprotein E genotype on apolipoprotein B-100 metabolism in normolipidemic and hyperlipidemic subjects. J Lipid Res. 2010;51(8):2413–21.PubMedCentralPubMed Ooi EM, Janus ED, Grant SJ, Sinclair LM, Barrett PHR. Effect of apolipoprotein E genotype on apolipoprotein B-100 metabolism in normolipidemic and hyperlipidemic subjects. J Lipid Res. 2010;51(8):2413–21.PubMedCentralPubMed
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Zurück zum Zitat Evans D, Arzer J, Aberle J, Beil FU. Rare variants in the lipoprotein lipase (LPL) gene are common in hypertriglyceridemia but rare in type III hyperlipidemia. Atherosclerosis. 2011;214(2):386–90.PubMed Evans D, Arzer J, Aberle J, Beil FU. Rare variants in the lipoprotein lipase (LPL) gene are common in hypertriglyceridemia but rare in type III hyperlipidemia. Atherosclerosis. 2011;214(2):386–90.PubMed
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Zurück zum Zitat Murase T, Ebara T, Okubo M. Hepatic lipase activity is decreased in Japanese patients with type III hyperlipoproteinemia. Clin Chim Acta. 2012;414:185–7.PubMed Murase T, Ebara T, Okubo M. Hepatic lipase activity is decreased in Japanese patients with type III hyperlipoproteinemia. Clin Chim Acta. 2012;414:185–7.PubMed
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Zurück zum Zitat Henneman P, van der Sman-de BF, Moghaddam PH, et al. The expression of type III hyperlipoproteinemia: involvement of lipolysis genes. Eur J Hum Genet. 2009;17(5):620–8.PubMedCentralPubMed Henneman P, van der Sman-de BF, Moghaddam PH, et al. The expression of type III hyperlipoproteinemia: involvement of lipolysis genes. Eur J Hum Genet. 2009;17(5):620–8.PubMedCentralPubMed
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Zurück zum Zitat Johansen CT, Wang J, Lanktree MB, et al. An increased burden of common and rare lipid-associated risk alleles contributes to the phenotypic spectrum of hypertriglyceridemia. Arterioscler Thromb Vasc Biol. 2011;31(8):1916–26. This study and other studies from this group provide a comprehensive overview of the contribution of newly discovered lipid genes to severe forms of hypertriglyceridemia and HLP3.PubMedCentralPubMed Johansen CT, Wang J, Lanktree MB, et al. An increased burden of common and rare lipid-associated risk alleles contributes to the phenotypic spectrum of hypertriglyceridemia. Arterioscler Thromb Vasc Biol. 2011;31(8):1916–26. This study and other studies from this group provide a comprehensive overview of the contribution of newly discovered lipid genes to severe forms of hypertriglyceridemia and HLP3.PubMedCentralPubMed
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Zurück zum Zitat Wu LL, Warnick GR, Wu JT, Williams RR, Lalouel JM. A rapid micro-scale procedure for determination of the total lipid profile. Clin Chem. 1989;35(7):1486–91.PubMed Wu LL, Warnick GR, Wu JT, Williams RR, Lalouel JM. A rapid micro-scale procedure for determination of the total lipid profile. Clin Chem. 1989;35(7):1486–91.PubMed
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Zurück zum Zitat Schumaker VN, Puppione DL. Sequential flotation ultracentrifugation. Methods Enzymol. 1986;128:155–70.PubMed Schumaker VN, Puppione DL. Sequential flotation ultracentrifugation. Methods Enzymol. 1986;128:155–70.PubMed
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Zurück zum Zitat Miller WG, Myers GL, Sakurabayashi I, et al. Seven direct methods for measuring HDL and LDL cholesterol compared with ultracentrifugation reference measurement procedures. Clin Chem. 2010;56(6):977–86.PubMed Miller WG, Myers GL, Sakurabayashi I, et al. Seven direct methods for measuring HDL and LDL cholesterol compared with ultracentrifugation reference measurement procedures. Clin Chem. 2010;56(6):977–86.PubMed
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Zurück zum Zitat Lackner KJ, Schmitz G. β-VLDL of patients with type III hyperlipoproteinemia interferes with homogeneous determination of HDL-cholesterol based on polyethylene glycol-modified enzymes. Clin Chem. 1998;44(12):2546–8. Lackner KJ, Schmitz G. β-VLDL of patients with type III hyperlipoproteinemia interferes with homogeneous determination of HDL-cholesterol based on polyethylene glycol-modified enzymes. Clin Chem. 1998;44(12):2546–8.
105.
Zurück zum Zitat Chung BH, Wilkinson T, Geer JC, Segrest JP. Preparative and quantitative isolation of plasma lipoproteins: rapid, single discontinuous density gradient ultracentrifugation in a vertical rotor. J Lipid Res. 1980;21(3):284–91.PubMed Chung BH, Wilkinson T, Geer JC, Segrest JP. Preparative and quantitative isolation of plasma lipoproteins: rapid, single discontinuous density gradient ultracentrifugation in a vertical rotor. J Lipid Res. 1980;21(3):284–91.PubMed
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Zurück zum Zitat Marcoux C, Hopkins PN, Wang T, et al. Remnant-like particle cholesterol and triglyceride levels of hypertriglyceridemic patients in the fed and fasted state. J Lipid Res. 2000;41(9):1428–36.PubMed Marcoux C, Hopkins PN, Wang T, et al. Remnant-like particle cholesterol and triglyceride levels of hypertriglyceridemic patients in the fed and fasted state. J Lipid Res. 2000;41(9):1428–36.PubMed
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Zurück zum Zitat Wang T, Nakajima K, Leary ET, et al. Ratio of remnant-like particle-cholesterol to serum total triglycerides is an effective alternative to ultracentrifugal and electrophoretic methods in the diagnosis of familial type III hyperlipoproteinemia. Clin Chem. 1999;45(11):1981–7.PubMed Wang T, Nakajima K, Leary ET, et al. Ratio of remnant-like particle-cholesterol to serum total triglycerides is an effective alternative to ultracentrifugal and electrophoretic methods in the diagnosis of familial type III hyperlipoproteinemia. Clin Chem. 1999;45(11):1981–7.PubMed
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Zurück zum Zitat Hopkins PN, Wu LL, Williams RR, Leary ET, Wang T, Nakajima K. Type III hyperlipidemia and lipoprotein remnants in early onset familial coronary artery disease. Circulation. 1998;98(Suppl I):I–791. Hopkins PN, Wu LL, Williams RR, Leary ET, Wang T, Nakajima K. Type III hyperlipidemia and lipoprotein remnants in early onset familial coronary artery disease. Circulation. 1998;98(Suppl I):I–791.
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Zurück zum Zitat Schaefer EJ. Limitations of automated remnant lipoprotein cholesterol assay for diagnostic use. Clin Chem. 2009;55(11):2061–2. author reply 2062-3.PubMed Schaefer EJ. Limitations of automated remnant lipoprotein cholesterol assay for diagnostic use. Clin Chem. 2009;55(11):2061–2. author reply 2062-3.PubMed
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Zurück zum Zitat Civeira F, Cenarro A, Ferrando J, et al. Comparison of the hypolipidemic effect of gemfibrozil versus simvastatin in patients with type III hyperlipoproteinemia. Am Heart J. 1999;138(1 Pt 1):156–62.PubMed Civeira F, Cenarro A, Ferrando J, et al. Comparison of the hypolipidemic effect of gemfibrozil versus simvastatin in patients with type III hyperlipoproteinemia. Am Heart J. 1999;138(1 Pt 1):156–62.PubMed
111.•
Zurück zum Zitat Kawashiri MA, Kobayashi J, Nohara A, et al. Impact of bezafibrate and atorvastatin on lipoprotein subclass in patients with type III hyperlipoproteinemia: result from a crossover study. Clin Chim Acta. 2011;412(11–12):1068–75. This is one of the few studies directly comparing statin and fibrate in HLP3 patients.PubMed Kawashiri MA, Kobayashi J, Nohara A, et al. Impact of bezafibrate and atorvastatin on lipoprotein subclass in patients with type III hyperlipoproteinemia: result from a crossover study. Clin Chim Acta. 2011;412(11–12):1068–75. This is one of the few studies directly comparing statin and fibrate in HLP3 patients.PubMed
112.
Zurück zum Zitat Fazio S, Linton MF. The role of fibrates in managing hyperlipidemia: mechanisms of action and clinical efficacy. Curr Atheroscler Rep. 2004;6(2):148–57.PubMed Fazio S, Linton MF. The role of fibrates in managing hyperlipidemia: mechanisms of action and clinical efficacy. Curr Atheroscler Rep. 2004;6(2):148–57.PubMed
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Metadaten
Titel
Hyperlipoproteinemia Type 3: The Forgotten Phenotype
verfasst von
Paul N. Hopkins
Eliot A. Brinton
M. Nazeem Nanjee
Publikationsdatum
01.09.2014
Verlag
Springer US
Erschienen in
Current Atherosclerosis Reports / Ausgabe 9/2014
Print ISSN: 1523-3804
Elektronische ISSN: 1534-6242
DOI
https://doi.org/10.1007/s11883-014-0440-2

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