Autosomal Recessive Hypercholesterolemia: A Mild Phenotype of Familial Hypercholesterolemia: Insight from the Kinetic Study using Stable Isotope and Animal Studies

Journal of Atherosclerosis and Thrombosis

Volumn 22, Issue 1, 2015, Pages 1-9

  Tada, Hayato ^a   Kawashiri, Masa Aki ^a   Nohara, Atsushi ^b   Inazu, Akihiro ^b   Kobayashi, Junji ^c   Mabuchi, Hiroshi ^b   Yamagishi, Masakazu ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

^b KANAZAWA UNIVERSITY   (Japan)

^c KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

Autosomal recessive hypercholesterolemia; Familial hypercholesterolemia; LDL receptor adaptor protein 1

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; LIPID BINDING PROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; MEGALIN; PROTEIN AP 2; PROTEIN DAB2; STABLE ISOTOPE; STATIN (PROTEIN); UNCLASSIFIED DRUG;

ANALYTICAL PARAMETERS; APOB GENE; AUTOSOMAL RECESSIVE HYPERCHOLESTEROLEMIA; CHOLESTEROL BLOOD LEVEL; DYSLIPIDEMIA; ENDOCYTOSIS; FAMILIAL HYPERCHOLESTEROLEMIA; FRACTIONAL CATABOLIC RATE; GENE; GENE MUTATION; HUMAN; INTERNALIZATION; LDLRAP1 GENE; LIPOPROTEIN METABOLISM; NONHUMAN; PHENOTYPIC VARIATION; PLASMAPHERESIS; PRODUCTION RATE; REVIEW; ANIMAL; HYPERCHOLESTEROLEMIA; ISOTOPE LABELING; KINETICS; METABOLISM; MOUSE; PATHOLOGY; PHENOTYPE;

ANIMALS; HUMANS; HYPERCHOLESTEROLEMIA; HYPERLIPOPROTEINEMIA TYPE II; ISOTOPE LABELING; KINETICS; MICE; PHENOTYPE;

EID: 84921888221     PISSN: 13403478     EISSN: 18803873     Source Type: Journal    
DOI: 10.5551/jat.27227     Document Type: Review

References (46)

1. Goldstein JL, Hobbs HH, Brown MS. Familial hypercholesterolemia. In: Scriver CR, Beaudet AL, Sly WS, and Valle D,eds. The metabolic and molecular bases of inherited disease, ed 8, vol 2. New York: McGraw-Hill; 2001; 2863-2913
2. Soutar AK, Naoumova RP: Mechanisms of Disease: genetic causes of familial hypercholesterolemia. Nat Pract Cardiovasc Med, 2007; 4: 214-225
3. Rader DJ, Cohen J, Hobbs HH: Monogenic hypercholesterolemia: new insights in pathogenesis and treatment. J Clin invest, 2003; 111: 1795-1803
4. Mabuchi H, Koizumi J, Shimizu M, Takeda R: Development of coronary heart disease in familial hypercholesterolemia. Circulation, 1989; 79: 225-232
5. Abifadel M, Varret M, Rabès JP, Allard D, Ouguerram K, Devillers M, Cruaud C, Benjannet S, Wickham L, Erlich D, Derré A, Villéger L, Farnier M, Beucler I, Bruckert E, Chambaz J, Chanu B, Lecerf JM, Luc G, Moulin P, Weissenbach J, Prat A, Krempf M, Junien C, Seidah NG, Boileau C: Mutations in PCSK9 cause autosomal dominant hypercholesterolemia. Nat Genet, 2003; 34: 154-156
6. Mabuchi H, Nohara A, Noguchi T, Kobayashi J, Kawashiri MA, Tada H, Nakanishi C, Mori M, Yamagishi M, Inazu A, Koizumi J: Molecular genetic epidemiology of homozygous familial hypercholesterolemia in the Hokuriku district of Japan. Atherosclerosis, 2011; 214: 404-407
7. Noguchi T, Katsuda S, Kawashiri MA, Tada H, Nohara A, Inazu A, Yamagishi M, Kobayashi J, Mabuchi H: The E32K variant of PCSK9 exacerbates the phenotype of familial hypercholesterolemia by increasing PCSK9 function and concentration in the circulation. Atherosclerosis, 2010; 210: 166-172
8. Mabuchi H, Nohara A, Noguchi T, Kobayashi J, Kawashiri MA, Inoue T, Mori M, Tada H, Nakanishi C, Yagi K, Yamagishi M, Ueda K, Takegoshi T, Miyamoto S, Inazu A, Koizumi J: Genotypic and phenotypic features in homozygous familial hypercholesterolemia caused by proprotein convertase subtilisin/kexin type 9 (PCSK9) gain-of-function mutation. Atherosclerosis, 2014; 236: 54-61
9. Khachadurian AK, Uthman SM: Experiences with the homozygous familial hypercholesterolemia. A report of 52 patients. Nutr Metab, 1973; 15: 132-140
10. Harada-Shiba M, Tajima S, Yokoyama S, Miyake Y, Kojima S, Tsushima M, Kawakami M, Yamamoto A: Siblings with normal LDL receptor activity and severe hypercholesterolemia. Arterioscler Thromb, 1992; 12: 1071-1078
11. Tada H, Kawashiri MA, Ikewaki K, Terao Y, Nakanishi C, Tsuchida M, Takata M, Miwa K, Nohara A, Inazu A, Kobayashi J, Mabuchi H, Yamagishi M: Altered metabolism of Low-density Lipoprotein and Very Low-density Lipoprotein Remnant in Autosomal Recessive Hypercholesterolemia: Results from Stable Isotope Kinetic Study in vivo. Circ Cardiovasc Genet, 2012; 5: 35-41
12. Tada H, Kawashiri MA, Tanaka A, Nakano T, Nakajima K, Inoue T, Noguchi T, Nakanishi C, Konno T, Hayashi K, Nohara A, Inazu A, Kobayashi J, Mabuchi H, Yamagishi M: Post-prandial remnant lipoprotein metabolism in autosomal recessive hypercholesterolaemia. Eur J Clin Invest, 2012; 42: 1094-1099
13. Soria LF, Ludwig EH, Clarke HR, Vega GL, Grundy SM, McCarthy BJ: Association between a specific apolipoprotein B mutation and familial defective apolipoprotein B-100, Proc Natl Acad Sci U S A, 1989; 86: 587-591
14. Tada H, Kawashiri MA, Noguchi T, Mori M, Tsuchida M, Takata M, Nohara A, Inazu A, Kobayashi J, Yachie A, Mabuchi H, Yamagishi M: A novel method for determining functional LDL receptor activity in familial hypercholesterolemia: application of the CD3/CD28 assay in lymphocytes. Clin Chim Acta, 2009; 400: 42-47
15. He G, Gupta S, Michaely P, Hobbs HH, Cohen JC: ARH is a modular adaptor protein that interacts with the LDL receptor, clathrin and AP-2. J Biol Chem, 2002; 277: 44044-44049
16. Maurer ME, Cooper JA: The adaptor protein Dab2 sorts LDL receptors into coated pits independently of AP-2 and ARH. J Cell Sci, 2006; 119: 4235-4246
17. Eden ER, Sun XM, Patel DD, Soutar AK: Adaptor protein disabled-2 modulates low density lipoprotein receptor synthesis in fibroblasts from patients with autosomal recessive hypercholesterolaemia. Hum Mol Genet, 2007; 16: 2751-2759
18. Mishra SK, Watkins SC, Traub LM: The autosomal recessive hypercholesterolemia (ARH) protein interfaces directly with the clathrin-coat machinery. Proc Natl Acad Sci U S A, 2002; 99: 16099-16104
19. Eden ER, Patel DD, Sun XM, Burden JJ, Themis M, Edwards M, Lee P, Neuwirth C, Naoumova RP, Soutar AK: Restoration of LDL receptor function in cells from patients with autosomal recessive hypercholesterolemia by retroviral expression of ARH1. J Clin Invest, 2002; 110: 1695-1702
20. Norman D, Sun XM, Bourbon M, Knight BL, Naoumova RP, Soutar AK: Characterization of a novel cellular defect in patients with phenotypic homozygous familial hypercholesterolemia, J Clin Invest, 1999; 104: 619-628
21. Fang L, Garuti R, Kim BY, Wade JB, Welling PA: The ARH adaptor protein regulates endocytosis of the ROMK potassium secretory channel in mouse kidney. J Clin Invest, 2009; 119: 3278-3289
22. Sun XM, Patel DD, Acosta JC, Gil J, Soutar AK: Premature senescence in cells from patients with autosomal recessive hypercholesterolemia (ARH): evidence for a role for ARH in mitosis. Arterioscler Thromb Vasc Biol, 2011; 31: 2270-2277
23. Saito A, Pietromonaco S, Loo AK, Farquhar MG: Complete cloning and sequencing of rat gp330/”megalin,” a distinctive member of the low density lipoprotein receptor gene family. Proc Natl Acad Sci U S A, 1994; 91: 9725-9729
24. Oleinikov AV, Zhao J, Makker SP: Cytosolic adaptor protein Dab2 is an intracellular ligand of endocytic receptor gp600/megalin. Biochem J, 2000; 347: 613-621
25. Zuliani G, Arca M, Signore A, Bader G, Fazio S, Chianelli M, Bellosta S, Campagna F, Montali A, Maioli M, Pacifico A, Ricci G, Fellin R: Characterization of a New Form of Inherited Hypercholesterolemia: Familial Recessive Hypercholesterolemia. Arterioscler Thromb Vasc Biol, 1999; 19: 802-809
26. Garcia CK, Wilund K, Arca M, Zuliani G, Fellin R, Maioli M, Calandra S, Bertolini S, Grishin N, Barnes R, Cohen JC, Hobbs HH: Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science, 2001; 292: 1394-398
27. Arca M, Zuliani G, Wilund K, Campagna F, Fellin R, Bertolini S, Calandra S, Ricci G, Glorioso N, Maioli M, Pintus P, Carru C, Cossu F, Cohen JC, Hobbs HH: Autosomal recessive hypercholesterolaemia in Sardinia, Italy, and mutations in ARH: a clinical and molecular genetic analysis. Lancet, 2002; 359: 841-847
28. Naoumova RP, Neuwirth C, Lee P, Miller JP, Taylor KG, Soutar AK: Autosomal recessive hypercholesterolaemia: long-term follow up and response to treatment. Atherosclerosis, 2004; 174: 165-172
29. Wilund KR, Yi M, Campagna F, Arca M, Zuliani G, Fellin R, Ho YK, Garcia JV, Hobbs HH, Cohen JC: Molecular mechanisms of autosomal recessive hypercholesterolemia. Hum Mol Genet, 2002; 11: 3019-3030
30. Al-Kateb H, Bähring S, Hoffmann K, Strauch K, Busjahn A, Nürnberg G, Jouma M, Bautz EK, Dresel HA, Luft FC: Mutation in the ARH gene and a chromosome 13q locus influence cholesterol levels in a new form of digenicrecessive familial hypercholesterolemia. Circ Res, 2002; 90: 951-958
31. Barbagallo CM, Emmanuele G, Cefalù AB, Fiore B, Noto D, Mazzarino MC, Pace A, Broqna A, Rizzo M, Corsini A, Notarbartolo A, Travali S, Averna MR: Autosomal recessive hypercholesterolemia in a Sicilian kindred harboring the 432insA mutation of the ARH gene. Atherosclerosis, 2003; 166: 395-400
32. Canizales-Quinteros S, Aguilar-Salinas CA, Huertas- Vázquez A, Ordóñez-Sánchez ML, Rodríguez-Torres M, Venturas-Gallegos JL, Riba L, Ramírez-Jimenez S, Salas- Montiel R, Medina-Palacios G, Robles-Osorio L, Miliar- García A, Rosales-León L, Ruiz-Ordaz BH, Zentella- Dehesa A, Ferré-D’Amare A, Gómez-Pérez FJ, Tusié-Luna MT: A novel ARH splice site mutation in a Mexican kindred with autosomal recessive hypercholesterolemia. Hum Genet, 2005; 116: 114-120
33. Quagliarini F, Vallvé JC, Campagna F, Alvaro A, Fuentes- Jimenez FJ, Sirinian MI, Meloni F, Masana L, Arca M: Autosomal recessive hypercholesterolemia in Spanish kindred due to a large deletion in the ARH gene. Mol Genet Metab, 2007; 92: 243-248
34. Harada-Shiba M, Takagi A, Miyamoto Y, Tsushima M, Ikeda Y, Yokoyama S, Yamamoto A: Clinical features and genetic analysis of autosomal recessive hypercholesterolemia. J Clin Endocrinol Metab, 2003; 88: 2541-2547
35. Mabuchi H, Tatami R, Haba T, Ueda K, Ueda R, Kametani T, Itoh S, Koizumi J, Oota M, Miyamoto S, Takeda R, Takeshita H: Homozygous familial hypercholesterolemia in Japan. Am J Med, 1978; 65: 290-297
36. Tada H, Kawashiri MA, Noguchi T, Nakanishi C, Tsuchida M, Takata M, Nohara A, Inazu A, Kobayashi J, Mabuchi H, Yamagishi M: Clinical impact of heterozygous carrier of autosomal recessive hypercholesterolemia on asymptomatic hyperlipidemic patients: evidence from familial gene analysis. Circulation, 2008; 118: S405
37. Harada K, Miyamoto Y, Morisaki H, Ohta N, Yamanaka I, Kokubo Y, Makino H, Harada-Shiba M, Okayama A, Tomoike H, Okamura T, Saito Y, Yoshimasa Y, Morisaki T: A Novel Thr56Met Mutation of the Autosomal Recessive Hypercholesterolemia Gene Associated with Hypercholesterolemia. J Atheroscler Thromb, 2010; 17: 131-140
38. Tada H, Kawashiri MA, Ohtani R, Noguchi T, Nakanishi C, Konno T, Hayashi K, Nohara A, Inazu A, Kobayashi J, Mabuchi H, Yamagishi M: A novel type of familial hypercholesterolemia: Double heterozygous mutations in LDL receptor and LDL receptor adaptor protein 1 gene. Atherosclerosis, 2011; 219: 663-666
39. Jones C, Garuti R, Michaely P, Li WP, Maeda N, Cohen JC, Herz J, Hobbs HH: Disruption of LDL but notVLDL clearance in autosomal recessive hypercholesterolemia. J Clin Invest, 2007; 117: 165-174
40. Michaely P, Zhao Z, Li WP, Garuti R, Huang LJ, Hobbs HH, Cohen JC: Identification of a VLDL-induced, FDNPVY independent internalization mechanism for the LDLR. EMBO J, 2007; 26: 3273-3282
41. Altenburg M, Arbones-Mainar J, Johnson L, Wilder J, Maeda N: Human LDL receptor enhances sequestration of ApoE4 and VLDL remnants on the surface of hepatocytes but not their internalization in mice. Arterioscler Thromb Vasc Biol, 2008; 28: 1104-1110
42. Mahley RW, Huang Y: Atherogenic remnant lipoproteins: role for proteoglycans in trapping, transferring, and internalizing. J Clin Invest, 2007; 117: 94-98
43. Cabezas MC, de Bruin TW, Westerveld HE, Meijer E, Erkelens DW: Delayed chylomicron remnant clearance in subjects with heterozygous familial hypercholesterolaemia. J Intern Med, 1998; 244: 299-307
44. Mamo JC, Smith D, Yu KC, Kawaguchi A, HaradaShiba M, Yamamura T, Yamamoto A: Accumulation of chylomicron remnants in homozygous subjects with familial hypercholesterolaemia. Eur J Clin Invest, 1998; 28: 379-384
45. Twickler, TB, Dallinga-Thie GM, de Valk HW, Schreuder PC, Jansen H, Cabezas MC, Erkelens DW: High Dose of Simvastatin Normalizes Postprandial Remnant-like Particle Response in Patients with Heterozygous Familial Hypercholesterolemia. Arterioscler Thromb Vasc Biol, 2000; 20: 2422-2427
46. Kawashiri MA, Hayashi K, Konno T, Fujino N, Ino H, Yamagishi M. Current perspectives in genetic cardiovascular disorders: from basic to clinical aspects. Heart Vessels, 2014; 29: 129-141