Dysbetalipoproteinaemia: A mixed hyperlipidaemia of remnant lipoproteins due to mutations in apolipoprotein e

Critical Reviews in Clinical Laboratory Sciences

Volumn 51, Issue 1, 2014, Pages 46-62

  Marais, A D ^a,b,c   Solomon, G A E ^a,c   Blom, D J ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

^c SOUTH AFRICAN MEDICAL RESEARCH COUNCIL   (South Africa)

Author keywords

Apolipoprotein E; Dysbetalipoproteinaemia; Fredrickson type III hyperlipidaemia

Indexed keywords

APOLIPOPROTEIN B; APOLIPOPROTEIN E; CHOLESTEROL; CHYLOMICRON REMNANT; FIBRIC ACID DERIVATIVE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL;

CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; CLINICAL ASSESSMENT; DYSBETALIPOPROTEINAEMIA; DYSLIPIDEMIA; GENETIC COUNSELING; GLOMERULOPATHY; HUMAN; HYPERLIPIDEMIA; LIPOPROTEIN METABOLISM; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

APOLIPOPROTEINS E; HUMANS; HYPERLIPOPROTEINEMIA TYPE III; MUTATION;

EID: 84893035111     PISSN: 10408363     EISSN: 1549781X     Source Type: Journal    
DOI: 10.3109/10408363.2013.870526     Document Type: Review

References (155)

1. Mahley RW, Rall SC. Apolipoprotein E: far more than a lipid transport protein. Annu Review Genomics Hum Genet 2000;1: 507-37.
2. Mahley RW, Huang Y, Rall SC. Pathogenesis of type III hyperlipoproteinemia (dysbetalipoproteinemia): questions, quandaries and paradoxes. J Lipid Res 1999;40:1933-49. (Pubitemid 29523420)
3. Beaumont JL, Carlson LA, Cooper GR, et al. Classification of hyperlipidaemias and hyperlipoproteinaemias. Bull World Health Organ 1970;43:891-15.
4. Mahley RW, Rall SC. Type III hyperlipoproteinemia (dysbetalipoproteinemia): the role of apolipoprotein E in normal and abnormal lipoprotein metabolism. In: Scriver CR, Beaudet AL, Sly WS, et al. eds. The metabolic and molecular bases of inherited disease. 8th Ed. New York: McGraw Hill. Chapter 119; 2001. 2835-62.
5. McGinley J, Jones H, Gofman J. Lipoproteins and xanthomatous diseases. J Invest Dermatol 1952;19:71-82.
6. Fredrickson DS, Levy RI, Lindgren FT. A comparison of heritable abnormal lipoprotein patterns as defined by two different techniques. J Clin Invest 1968;47:2446-57.
7. Havel RJ, Kane JP. Primary dysbetalipoproteinemia: predominance of a specific apoprotein species in triglyceride-rich lipoproteins. Proc Natl Acad Sci USA 1973;70:2015-39.
8. Utermann G, Hees M, Steinmetz A. Polymorphism of apolipoprotein E and occurrence of dysbetalipoproteinaemia in man. Nature 1977;269:604-7.
9. Zannis VI, Breslow JL. Human very low density lipoprotein apolipoprotein E isoprotein polymorphism is explained by genetic variation and posttranslational modification. Biochemistry 1981; 20:1033-41. (Pubitemid 11097562)
10. Weisgraber KH, Innerarity TL, Mahley RW. Abnormal lipoprotein receptor-binding activity of the human E apoprotein due to cystein-arginine interchange at a single site. J Biol Chem 1982; 257:2518-21.
11. Zannis VI, Breslow JL, Utermann G, et al. Proposed nomenclature of apoE genotypes and phenotypes. J Lipid Res 1982;23:911-14. (Pubitemid 13244364)
12. Rall SC, Mahley RW. The role of apolipoprotein E genetic variation in lipoprotein disorders. J Intern Med 1992;231:653-9.
13. Hill IS, Pritchard PH. Improved phenotyping of apolipoprotein E. Application to population frequency distribution. Clin Chem 1990; 36:1871-4.
14. Hixson JE, Cox LA, Borenstein S. The baboon apolipoprotein E gene: structure, function, and linkage with the gene for apolipoprotein C-1. Genomics 1988;2:315-23.
15. Wilson C, Wardell MR, Weisgraber KH, et al. Salt bridge relay triggers defective LDL receptor binding by a mutant apolipoprotein. Structure 1994;2:713-18.
16. Georgiadou D, Chroni A, Vezeridis A, et al. Biophysical analysis of apolipoprotein E3 variants linked with development of type III hyperlipoproteinemia. PLoS One. 2011;6:e27037.
17. Kypreos KE, Morani P, van Dijk KW, et al. The amino-terminal 1-185 domain of apoE promotes the clearance of lipoprotein remnants in vivo. The carboxy-terminal domain is required for induction of hyperlipidemia in normal and apoE-deficient mice. Biochemistry 2001;40:6027-35. (Pubitemid 32466305)
18. Hoffmann MM, Scharnagl H, Köster W, et al. Apolipoprotein E1 Baden (Arg(180)!Cys). A new apolipoprotein E variant associated with hypertriglyceridemia. Clin Chim Acta 2001;303: 41-8. (Pubitemid 32121804)
19. de Beer F, van Dijk KW, Jong MC. Apolipoprotein E2 (Lys146-4Gln) causes hypertriglyceridemia due to an apolipoprotein E variant-specific inhibition of lipolysis of very low density lipoproteins-triglycerides. Arterioscler Thromb Vasc Biol 2000; 20:1800-6. (Pubitemid 30470597)
20. Sing CF, Davignon J. Role of the apolipoprotein E polymorphism in determining normal plasma lipid and lipoprotein variation. Am J Hum Genet 1985;37:268-85. (Pubitemid 15053161)
21. Davignon J, Gregg RE, Sing CF. Apolipoprotein E polymorphism and atherosclerosis. Arteriosclerosis 1988;8:1-21. (Pubitemid 18049171)
22. Le Couteur DG, Warren A, Cogger VC, et al. Old age and the hepatic sinusoid. The Anatomical Record 2008;291:672-83.
23. Huang Y, Liu XQ, Rall SC, Mahley RW. Apolipoprotein E2 reduces the low density lipoprotein level in transgenic mice by impairing lipoprotein lipase-mediated lipolysis of triglyceride-rich lipoproteins. J Biol Chem 1998; 273:17483-90. (Pubitemid 28355080)
24. Ooi EM, Janus ED, Grant SJ, et al. Effect of apolipoprotein E genotype on apolipoprotein B-100 metabolism. J Lipid Res 2010; 51:2413-21.
25. Weintraub MS, Eisenberg S, Breslow JL. Dietary fat clearance in normal subjects is regulated by genetic variation in apolipoprotein E. J Clin Invest 1987;80:1571-7. (Pubitemid 18007127)
26. de Beer F, Stalenhoef AFH, Hoogerbrugge N, et al. Expression of type III hyperlipidaemia in apoE2 (arg 158!cys) homozygotes is associated with hyperinsulinemia. Arterioscler Thromb Vasc Biol 2002;22:294-9. (Pubitemid 34127042)
27. Hoffmann MM, Scharnagl H, Köster W, et al. Apolipoprotein E1 Baden (arg180!cys). A new apolipoprotein E variant with hypertriglyceridaemia. Clin Chim Acta 2001;303:41-8. (Pubitemid 32121804)
28. Basaran A. Pregnancy-induced hyperlipoproteinemia: review of the literature. Reprod Sci 2009;16:431-7.
29. Krane-Gartiser K, Breum L, Glumrr C, et al. Prevalence of the metabolic syndrome in Danish psychiatric outpatients treated with antipsychotics. Nord J Psych 2011;65:345-52.
30. Sinnott BP, Mazzone T. Tuberous xanthomas associated with olanzapine therapy and hypertriglyceridemia in the setting of a rare apolipoprotein E mutation. Endocr Pract 2006;12: 183-7.
31. Holmes DT, Long P, Frohlich J. Dysbetalipoproteinemia and clomipramine. Am J Psychiatry 2005;162:1384-5.
32. Lister RK, Youle M, Nair DR, et al. Latent dysbetalipoproteinaemia precipitated by HIV-protease inhibitors. Lancet 1999;353: 1678. (Pubitemid 29224532)
33. Samaha FF, Ky B, Lo Re V. Type III hyperlipoproteinemia unmasked by HIV anti-retroviral therapy. Am J Med 2005;118: 691-2. (Pubitemid 40732713)
34. Huang Y, Liu XQ, Rall SC, et al. Overexpression and accumulation of apolipoprotein E as a cause of hypertriglyceridemia. J Biol Chem 1998;273:26388-93. (Pubitemid 28471643)
35. Huang Y, Ji ZS, Brecht WJ, et al. Overexpression of apolipoprotein E3 in transgenic rabbits causes combined hyperlipidemia by stimulating hepatic VLDL production and impairing VLDL lipolysis. Arterioscler Thromb Vasc Biol 1999; 19:2952-9. (Pubitemid 30029824)
36. Kuipers F, Jong MC, Lin Y, et al. Impaired secretion of very low density lipoprotein-triglycerides by apolipoprotein E-deficient mouse hepatocytes. J Clin Invest 1997;100:2915-22. (Pubitemid 28007563)
37. Kypreos KE, Li X, van Dijk KW, et al. Molecular mechanisms of type III hyperlipoproteinemia: the contribution of the carboxyterminal domain of ApoE can account for the dyslipidemia that is associated with the E2/E2 phenotype. Biochemistry 2003;42: 9841-53. (Pubitemid 37012860)
38. Retnakaran R, Connelly PW, Goguen J. Unmasking of type III hyperlipoproteinemia by hypothyroidism: a dramatic illustration of altered lipoprotein metabolism in a postpartum woman. Endocr Pract 2005;11:394-8.
39. Geisel J, Bunte T, Bodis M, et al. Apolipoprotein E2/E2 genotype in combination with mutations in the LDL receptor gene causes type III hyperlipoproteinemia. Clin Chem Lab Med 2002;40: 475-9. (Pubitemid 34693088)
40. Carmena R, Roy M, Roederer G, et al. Coexisting dysbetalipoproteinemia and familial hypercholesterolemia. Clinical and laboratory observations. Atherosclerosis 2000;148:113-24.
41. 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.
42. Burnside NJ, Alberta L, Robinson-Bostom L, Bostom A. Type III hyperlipoproteinemia with xanthomas and multiple myeloma. J Am Acad Dermatol 2005;53:S281-4. (Pubitemid 41443489)
43. Chee L, Spearing RL, Morris CM, et al. Acquired myelomaassociated Type III hyperlipidaemia treated by nonmyeloablative HLA-identical sibling allogeneic stem cell transplant using a donor with essential thrombocythaemia (ET): evidence of engraftment without manifestation of ET in recipient. Bone Marrow Transplant 2005;35:1213-14. (Pubitemid 40895179)
44. Evans D, Bode A, von der Lippe G, et al. Cerebrovascular atherosclerosis in type III hyperlipidemia is modulated by variation in the apolipoprotein A5 gene. Eur J Med Res 2011; 16:79-84.
45. Evans D, Seedorf U, Beil FU. Polymorphisms in the apolipoprotein A5 (APOA5) gene and type III hyperlipidemia. Clin Genet 2005;68:369-72. (Pubitemid 41341616)
46. Henneman P, van der Sman-de Beer F, Moghaddam PH, et al. The expression of type III hyperlipoproteinemia: involvement of lipolysis genes. Eur J Human Genetics 2009;17:620-8.
47. Mart?́n-Campos JM, Rico N, Bonet R, et al. Apolipoprotein A5 S19W may play a role in dysbetalipoproteinemia in patients with the ApoE2/E2 genotype. Clin Chem 2006;52:1974-5.
48. Hoffer MJV, Niththyananthan S, Naoumova RP, et al. Apolipoprotein E1 Hammersmith (Lys 146-Asn;Arg147-Trp) due to a dinucleotide substitution is associated with early manifestation of dominant type III hyperlipoproteinaemia. Atherosclerosis 1996;124:183-9. (Pubitemid 26228005)
49. De Knijff P, van den Maagdeburg AMJM, Stalenhoef AFH, et al. Familial dysbetalipoproteinemia associated with apolipoprotein E3 Leiden in an extended multigeneration pedigree. J Clin Invest 1991;88:643-55.
50. Feussner G, Albanese M, Mann WA, et al. Apolipoprotein E2 (Arg136!Cys), a variant of apolipoprotein E associated with late-onset dominance of type III hyperlipoproteinaemia. Eur J Clin Invest 1996;26:13-23.
51. Hubacek JA, Pitha J, Kodova Z, Poledne R. Rare variant of apolipoprotein E 2*(Arg136!Cys) in a subject with normal lipid values. Physiol Res 2002;51:107-8. (Pubitemid 34266450)
52. März W, Hoffman MM, Scharnagl H, et al. Apolipoprotein E2 (Arg136!Cys) mutation in the receptor binding domain of apoE is not associated with dominant type III hyperlipoproteinemia. J Lipid Res 1998;39:658-69. (Pubitemid 28158407)
53. Vrabl?́k M, Hor?́nek A, Ceska R, et al. Familial dysbetalipoproteinemia in three patients with apoE 2*(Arg136!Cys) gene variant. Physiol Res 2003;52:647-50.
54. Horie Y, Fazio S, Westerlund JR, et al. The functional characteristics of a human apolipoprotein E variant (E2 arg 142-leu) may explain its association with dominant expression of type III hyperlipoproteinemia. J Biol Chem 1992;267:1962-8.
55. Vezeridis AM, Drosatos K, Zannis VI. Molecular etiology of a dominant form of type III hyperlipoproteinemia caused by R142C substitution in apoE4. J Lipid Res 2011;52:45-56.
56. Baass A, Wassef H, Tremblay M, et al. Characterization of a new LCAT mutation causing familial LCAT deficiency (FLD) and the role of APOE as a modifier gene of the FLD phenotype. Atherosclerosis 2009;207:452-7.
57. Tsukamoto H, Hirose H, Dan K, et al. Apolipoprotein E deficiency associated with type III hyperlipoproteinemia-analysis of apolipoprotein E. Rinsho Byori 2006;54:121-5.
58. Tate JR, Hoffmann MM, Lovelock PK, et al. Identification of an apolipoprotein(e) variant associated with type III hyperlipoproteinaemia in an indigenous Australian. Ann Clin Biochem 2001; 38:46-53. (Pubitemid 32061616)
59. Dijck-Brouwer DA, van Doormaal JJ, Kema IP, et al. Discovery and consequences of apolipoprotein-epsilon(3Groningen): a G-insertion in codon 95/96 that is predicted to cause a premature stop codon. Ann Clin Biochem 2005;42:264-8. (Pubitemid 40961743)
60. 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;149:395-401. (Pubitemid 30145550)
61. Carlson LA, Holmquist L, Nilsson-Ehle P. Deficiency of hepatic lipase activity in post-heparin plasma in familial hyper-alphatriglyceridemia. Acta Med Scand 1986;219:435-47. (Pubitemid 16070894)
62. Whitman SC, Hazen SL, Miller DB, et al. Modification of type III VLDL, their remnants, and VLDL from ApoE-knockout mice by p-hydroxyphenylacetaldehyde, a product of myeloperoxidase activity, causes marked cholesteryl ester accumulation in macrophages. Arterioscler Thromb Vasc Biol 1999;19:1238-49. (Pubitemid 29227643)
63. Abela GS. Cholesterol crystals piercing the arterial plaque and intima trigger local and systemic inflammation. J Clin Lipidol 2010;4:156-64.
64. Sawka AM, Singh RJ, Hiddinga HJ, et al. Remnant lipoproteins induce endothelial plasminogen activator inhibitor-1. Biochem Biophys Res Commun 2001;285:15-19. (Pubitemid 32912503)
65. Tremblay K, Méthot J, Brisson D, Gaudet D. Etiology and risk of lactescent plasma and severe hypertriglyceridemia. J Clin Lipidol 2011;5:37-44.
66. Hopkins PN, Wu LL, Hunt SC, Brinton EA. Plasma triglycerides and type III hyperlipidemia are independently associated with premature familial coronary artery disease. J Am Coll Cardiol 2005;45:1003-12. (Pubitemid 40432430)
67. Zadelaar S, Kleemann R, Verschuren L, et al. Mouse models for atherosclerosis and pharmaceutical modifiers. Arterioscler Thromb Vasc Biol 2007;27:1706-21. (Pubitemid 47207165)
68. Vasquez EC, Peotta VA, Gava AL, et al. Cardiac and vascular phenotypes in the apolipoprotein E-deficient mouse. J Biomed Sci 2012;19:1-9.
69. Friedman O, Hockstein N, Willcox TO, Keane WM. Xanthoma of the temporal bone: a unique case of this rare condition. Ear Nose Throat J 2000;79:433-6. (Pubitemid 30415251)
70. Saito T, Oikawa S, Sato H, et al. Lipoprotein glomerulopathy: significance of lipoprotein and ultrastructural features. Kidney Int Suppl 1999;71:S37-41. (Pubitemid 29304810)
71. Oikawa S, Matsunaga A, Saito T, et al. Apolipoprotein E Sendai (arginine 145!proline): a new variant associated with lipoprotein glomerulopathy. J Am Soc Nephrol 1997;8:820-3.
72. Tokura T, Itano S, Kobayashi S, et al. A novel mutation ApoE2 Kurashiki (R158P) in a patient with lipoprotein glomerulopathy. J Atheroscler Thromb 2011;18:536-41.
73. Sam R, Wu H, Yue L, et al. Lipoprotein glomerulopathy: a new apolipoprotein E mutation with enhanced glomerular binding. Am J Kidney Dis 2006;47:539-48. (Pubitemid 43255189)
74. Luo B, Huang F, Liu Q, et al. Identification of apolipoprotein E Guangzhou (arginine 150 proline), a new variant associated with lipoprotein glomerulopathy. Am J Nephrol 2008;28:347-53.
75. Kinomura M, Sugiyama H, Saito T, et al. A novel variant apolipoprotein E Okayama in a patient with lipoprotein glomerulopathy. Nephrol Dial Transplant 2008;23:751-6. (Pubitemid 351767634)
76. Ando M, Sasaki J, Hua H, et al. A novel 18-amino acid deletion in apolipoprotein E associated with lipoprotein glomerulopathy. Kidney Int 1999;56:1317-23. (Pubitemid 29451239)
77. Konishi K, Saruta T, Kuramochi S, et al. Association of a novel 3-amino acid deletion mutation of apolipoprotein E (ApoE Tokyo) with lipoprotein glomerulopathy. Nephron 1999;83:214-18. (Pubitemid 29486399)
78. Matsunuga A, Sasaki J, Komatsu T, et al. A novel apolipoprotein E mutation, E2 (Arg25Cys), in lipoprotein glomerulopathy. Kidney Int 1999;561:421-7. (Pubitemid 29353139)
79. Sakatsume M, Kadomura M, Sakata I, et al. Novel glomerular lipoprotein deposits associated with apolipoprotein E2 homozygosity. Kidney Int 2001;59:1911-18. (Pubitemid 32336807)
80. Saito T. Abnormal lipid metabolism and renal disorders. Tohoku J Exp Med 1997;181:321-37. (Pubitemid 127471183)
81. Ishigaki Y, Oikawa S, Suzuki T, et al. Virus-mediated transduction of apolipoprotein E (ApoE)-sendai develops lipoprotein glomerulopathy in ApoE-deficient mice. J Biol Chem 2000;275: 31269-73.
82. Hoffmann MM, Scharnagl H, Panagiotou E, et al. Diminished LDL receptor and high heparin binding of apolipoprotein E2 Sendai associated with glomerulopathy. J Am Soc Nephrol 2001; 12:524-30. (Pubitemid 32180021)
83. Miyata T, Sugiyama S, Nangaku M, et al. ApoE2/E5 variants in lipoprotein glomerulopathy recurred in transplant kidney. J Am Soc Nephrol 1999;10:1590-5. (Pubitemid 29297535)
84. Hayakawa M, Okubo M, Kastori H, et al. A patient with apolipoprotein E2 variant Q187E without lipoprotein glomerulopathy. Am J Kidney Dis 2002;39:1-4.
85. Arai T, Yamashita S, Yamane M, et al. Disappearance of intraglomerular lipoprotein thrombi and marked improvement of nephrotic syndrome by bezafibrate treatment in a patient with lipoprotein glomerulopathy. Atherosclerosis 2003; 169:293-9. (Pubitemid 37297476)
86. Blom DJ, Byrnes P, Jones S, Marais AD. Non-denaturing polyacrylamide gradient gel electrophoresis for the diagnosis of dysbetalipoproteinemia. J Lipid Res 2003;44:212-17. (Pubitemid 36114787)
87. Kawashiri MA, Higashikata T, Takata M, et al. Type III hyperlipoproteinemia exaggerated by Sheehan's syndrome with advanced systemic atherosclerosis: a 28-year clinical course. Circ J 2005;69:746-51. (Pubitemid 40806116)
88. Jetha MM, Fiorillo L. Xanthomata and diabetes in an adolescent with familial dysbetalipoproteinemia 9 years after valproateinduced pancreatitis. Pediatr Diabetes 2012;13:444-7.
89. Blom DJ, Byrnes P, Jones S, Marais AD. Dysbetalipoproteinaemia-clinical and pathophysiological features. S Afr Med J 2002;92: 892-7.
90. Chuang TY, Chao CL, Lin BJ, Lu SC. Gestational hyperlipidemic pancreatitis caused by type III hyperlipoproteinemia with apolipoprotein E2/E2 homozygote. Pancreas 2009;38: 716-17.
91. Fung M, Hill J, Cook D, Frohlich J. Case series of type III hyperlipoproteinemia in children. BMJ Case Rep 2011; doi: 10.1136/bcr.02.2011. 3895.
92. Vivatrat N, Barshop BA, Jones KL. Severe hypertriglyceridemia and recurrent pancreatitis in a girl with type Ia glycogen storage disease and type III hyperlipoproteinemia. Am J Med Genet A 2009;149A:2557-9.
93. Krsek M, Ceska R, Horinek A, et al. Type III hyperlipoproteinaemia and primary amenorrhoea with severe hypothyroidism. Acta Paed 2000;89:1023-4. (Pubitemid 30643745)
94. Maheux P. Dermatology spot diagnosis. Postgrad Med J 2005;81: 497. (Pubitemid 41160591)
95. Sato-Matsumura KC, Matsumura T, Yokoshiki H, et al. Xanthoma striatum palmare as an early sign of familial type III hyperlipoproteinemia with an apoprotein E genotype epsilon2/epsilon2. Clin Exp Dermatol 2003;28:321-2. (Pubitemid 36713827)
96. Nagarajan DV, Boreham PA, Parfitt VJ. Palmar striated xanthomas. Postgrad Med J 2003;79:690. (Pubitemid 38134685)
97. Kashyap AS, Kashyap S. A young man with dry skin and nodules on elbows and buttocks. Postgrad Med J 2000;76:109-11. (Pubitemid 30069452)
98. Crook MA, Mukherjee A, Marshall K. Unusual presentations to a lipid clinic. Postgrad Med J 1999;75:633-4. (Pubitemid 29452603)
99. Bouwmans EM, Assouiki F. Diagnostic image. A woman with orange hands. Ned Tijdschr Geneesk 2009;153:B452.
100. Sharma D, Thirkannad S. Palmar xanthoma-an indicator of a more sinister problem. Hand 2010;5:210-12.
101. Blom DJ. Dysbetalipoproteinaemia-clinical and laboratory aspects, changes in lipoprotein composition and remnant metabolism associated with lipid lowering drugs [PhD Thesis]. Cape Town: University of Cape Town; 2007.
102. Todo Y, Kobayashi J, Higashikata T, et al. Detailed analysis of serum lipids and lipoproteins from Japanese type III hyperlipoproteinemia with apolipoprotein E2/2 phenotype. Clin Chim Acta 2004;348:35-40. (Pubitemid 39208998)
103. Vermeer BJ, van Gent CM, Goslings B, Polano MK. Xanthomatosis and other clinical findings in patients with elevated levels of very low density lipoproteins. Br J Dermatol 1979;100: 657-66. (Pubitemid 9250119)
104. Feussner G, Wagner A, Kohl B, Ziegler R. Clinical features of type III hyperlipoproteinemia: analysis of 64 patients. Clin Investig 1993;71:362-6. (Pubitemid 23142834)
105. Borrie P. Type 3 hyperlipoproteinaemia. Br Med J 1969;2:665-7.
106. Morganroth J, Levy RI, Fredrickson DS. The biochemical, clinical, and genetic features of type III hyperlipoproteinemia. Ann Intern Med 1975;82:158-74.
107. Stuyt PM, Van 't Laar A. Clinical features of type III hyperlipoproteinaemia. Neth J Med 1983;26:104-11. (Pubitemid 13089364)
108. Blom DJ, O'Neill FH, Marais AD. Screening for dysbetalipoproteinemia by plasma cholesterol and apolipoprotein B concentrations. Clin Chem 2005;51:904-7. (Pubitemid 40577931)
109. Sniderman A, Tremblay A, Bergeron J, et al. Diagnosis of type III hyperlipoproteinemia from plasma total cholesterol, triglyceride, and apolipoprotein B. J Clin Lipidol 2007;1:256-63. (Pubitemid 47370863)
110. Yuasa-Kawase M, Masuda D, Ketazume-Taneika R, et al. Apolipoprotein B-48 to triglyceride ratio is a novel and useful marker for detection of type III hyperlipidemia after antihyperlipidemic intervention. J Atheroscler Thromb 2012;19:862-71.
111. Miyauchi K, Kayahara N, Ishigami M, et al. Development of a homogeneous assay to measure remnant lipoprotein cholesterol. Clin Chem 2007;53:2128-35. (Pubitemid 350197296)
112. 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;45:1981-7. (Pubitemid 29522007)
113. Kido T, Kurata H, Matsumoto A, et al. Lipoprotein analysis using agarose gel electrophoresis and differential staining of lipids. J Atheroscler Thromb 2001;8:7-13.
114. Fredrickson DS, Morganroth J, Levy RI. Type III hyperlipoproteinemia: an analysis of two contemporary definitions. Ann Intern Med 1975;82:150-7.
115. Albers JJ, Warnick GR, Hazzard WR. Type III hyperlipoproteinemia: a comparative study of current diagnostic techniques. Clin Chim Acta 1977;75:193-204. (Pubitemid 8047076)
116. Hazzard WR, Porte Jr D, Bierman EL. Abnormal lipid composition of very low density lipoproteins in diagnosis of broad-beta disease (type 3 hyperlipoproteinemia). Metabolism 1972;21: 1009-19.
117. Mishkel MA, Nazir DJ, Crowther S. A longitudinal assessment of lipid ratios in the diagnosis of type III hyperlipoproteinaemia. Clin Chim Acta 1975;58:121-36.
118. Vessby B. Studies on the serum lipoprotein composition in 50-year-old men. A suggestion of chemical criteria for diagnosis of hyperlipoproteinaemia type III (Broad-beta disease). Clin Chim Acta 1976;69:29-42.
119. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972;18: 499-502.
120. Nauck M, Glatt L, März W, et al. Simple precipitation-based method for the screening of type IIIhyperlipoproteinemia. Clin Chem 1999;45:909-11. (Pubitemid 29266626)
121. Otvos JD, Collins D, Freedman DS, et al. Particle subclasses predict coronary events and are favorably changed by gemfibrozil therapy in the veterans affairs high-density lipoprotein intervention trial. Circulation 2006;113:1556-63. (Pubitemid 43739414)
122. Feussner G, Lohrmann J, Dobmeyer J. Clin Chem. Rapid and reliable identification of human apolipoprotein E1 (Gly127!Asp, Arg158!Cys) variant. Atherosclerosis 1996;124:183-9.
123. Mailly F, Xu CF, Xhignesse M, et al. Characterization of a new apolipoprotein E5 variant detected in two French-Canadian subjects. J Lipid Res 1991;32:613-20.
124. Ruzicka V, März W, Russ A, et al. Characterization of the gene for apolipoprotein E5-Frankfurt (Gln81!Lys, Cys112!Arg) by polymerase chain reaction, restriction isotyping, and temperature gradient gel electrophoresis. Electrophoresis 1993; 14:1032-7. (Pubitemid 23359590)
125. Feussner G, Scharnagl H, Scherbaum C, et al. Apolipoprotein E5 (Glu212!Lys): increased binding to cell surface proteoglycans but decreased uptake and lysosomal degradation in cultured fibroblasts. J Lipid Res 1996;37:1632-45. (Pubitemid 26275374)
126. Feussner G, Feussner V, Hoffmann MM, et al. Molecular basis of type III hyperlipoproteinaemia in Germany. Human Mutation 1998;11:417-23. (Pubitemid 28196714)
127. Stalenhoef AF. Dominant type III hyperlipoproteinaemia (familial dysbetalipoproteinaemia). Neth J Med 2013;71:50.
128. de Villiers WJS, van der Westhuyzen DR, Coetzee GA, et al. The apolipoprotein E2 (arg145cys) mutation causes autosomal dominant type III hyperlipoproteinemia with incomplete penetrance. Arterioscler, Thromb and Vasc Biol 1997;17: 865-72. (Pubitemid 27209263)
129. Abou Ziki MD, Strulovici-Barel Y, Hackett NR, et al. High prevalence of the apoE Arg145Cys dyslipidemia at risk polymorphism in African-derived populations. Am J Cardiol. doi: 10.1016/j.amjcard.2013.09.021.
130. Lin HP, Kao JT. Apolipoprotein epsilon 2/3 genotype and type III hyperlipoproteinemia among Taiwanese. Clin Chim Acta 2003; 330:173-8.
131. Hixson JE, Vernier DT. Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J Lipid Res 1990;31:545-8. (Pubitemid 20107994)
132. Marduel M, Ouguerram K, Serre V, et al. Description of a large family with autosomal dominant hypercholesterolemia associated with the APOE p.Leu167del mutation. Hum Mutat 2013;34:83-7.
133. Faivre L, Saugier-Veber P, Pais de Barros JP, et al. Variable expressivity of the clinical and biochemical phenotype associated with the apolipoprotein E p.Leu149del mutation. Eur J Hum Genet 2005;13:1186-9.
134. Nguyen TT, Kruckeberg KE, O'Brien JF, et al. Familial splenomegaly: macrophage hypercatabolism of lipoproteins associated with apolipoprotein E mutation [apolipoprotein E (delta149Leu)]. J Clin Endocrinol Metab 2000;85:4354-8. (Pubitemid 32055398)
135. Solanas-Barca M, de Castro-Orós I, Mateo-Gallego R, et al. Apolipoprotein E gene mutations in subjects with mixed hyperlipidemia and a clinical diagnosis of familial combined hyperlipidaemia. Atherosclerosis 2012;222:449-55.
136. Eto M, Saito M, Nakata H, et al. Type III hyperlipoproteinema with apolipoprotein E2/2 genotype in Japan. Clin Genet 2002;61: 416-22. (Pubitemid 36372678)
137. Retterstøl K, Hennig CB, Iversen PO. Improved plasma lipids and body weight in overweight/obese patients with type III hyperlipoproteinemia after 4 weeks on a low glycemic diet. Clin Nutr 2009;28:213-15.
138. Arad Y, Ramakrishnan R, Ginsberg HN. Lovastatin therapy reduces low density lipoprotein apoB levels in subjects with combined hyperlipidemia by reducing the production of apoBcontaining lipoproteins: implications for the pathophysiology of apoB production. J Lipid Res 1990;31:567-82. (Pubitemid 20167624)
139. Marais AD, Naoumova RP, Firth JC, et al. Decreased production of low density lipoprotein by atorvastatin after apheresis in homozygous familial hypercholesterolaemia. J Lipid Res 1997;38: 2071-8. (Pubitemid 27468015)
140. Ishigami M, Yamashita S, Sakai N, et al. Atorvastatin markedly improves type III hyperlipoproteinemia in association with reduction of both exogenous and endogenous apolipoprotein B-containing lipoproteins. Atherosclerosis 2003;168:359-66. (Pubitemid 36705541)
141. van Dam M, Zwart M, de Beer F, et al. Long term efficacy and safety of atorvastatin in the treatment of severe type III and combined dyslipidaemia. Heart 2002;88:234-8. (Pubitemid 34913502)
142. Blom DJ, Marais AD, Retterstøl K, et al. Rosuvastatin reduces non-high-density lipoprotein cholesterol and lipoprotein remnants in patients with dysbetalipoproteinemia (Fredrickson type III hyperlipoproteinemia). J Clin Lipidol 2008;2:418-25.
143. 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;412:1068-75.
144. 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; 138:156-62. (Pubitemid 29331137)
145. Post SM, Groenendijk M, Solaas K, et al. Cholesterol 7alphahydroxylase deficiency in mice on an APOE*3-Leiden background impairs very-low-density lipoprotein production. Arterioscler Thromb Vasc Biol 2004;24:768-74. (Pubitemid 38451618)
146. de Beer F, Smelt AH, van Vark LC, et al. The effect of tibolone on the lipoprotein profile of postmenopausal women with type III hyperlipoproteinemia. J Intern Med 2002;251:148-55. (Pubitemid 34146698)
147. Gillett MJ, Burnett JR, Yeap D. Clomiphene-associated combined hyperlipidaemia: a case report. J Reprod Med 2006; 51:587-90. (Pubitemid 44100003)
148. Cho EJ, Min YJ, Oh MS, et al. Disappearance of angina pectoris by lipid-lowering in type III hyperlipoproteinemia. Am J Cardiol 2011;107:793-6.
149. Cautero N, Di Benedetto F, De Ruvo N, et al. Novel genetic mutation in apolipoprotein E2 homozygosis and its implication in organ donation: a case report. Transplant Proc 2010;42:1349-51.
150. Schaefer JR. Unraveling hyperlipidemia type III (dysbetalipoproteinemia), slowly. Eur J Hum Genet 2009;17:541-2.
151. Evans D, Beil FU, Aberle J. Resequencing the apoE gene reveals that rare mutations are not significant contributory factors in the development of type III hyperlipidemia. J Clin Lipidol 2013;7:671-4.
152. Brahm A, Hegele RA. Hypertriglyceridemia. Nutrients 2013;5: 981-1001.
153. 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: 386-90.
154. Mann WA, Meyer N, Berg D, et al. Lipoprotein lipase compensates for the defective function of apo E variants in vitro by interacting with proteoglycans and lipoprotein receptors. Atherosclerosis 1999;145:61-9. (Pubitemid 29292701)
155. Handattu SP, Nayyar G, Garber DW, et al. Two apolipoprotein E mimetic peptides with similar cholesterol reducing properties exhibit differential atheroprotective effects in LDL-R null mice. Atherosclerosis 2012;227:58-64.