Novel functional APOB mutations outside LDL-binding region causing familial hypercholesterolaemia

Human Molecular Genetics

Volumn 23, Issue 7, 2014, Pages 1817-1828

  Alves, Ana Catarina ^a,b   Etxebarria, Aitor ^c   Soutar, Anne Katherine ^d   Martin, Cesar ^c   Bourbon, Mafalda ^a,b  

^a NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B; FLUORESCENT DYE; GENOMIC DNA; KEXIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; LDLR PROTEIN, HUMAN; PCSK9 PROTEIN, HUMAN; SERINE PROTEINASE;

ADULT; ARTICLE; BINDING SITE; CELL GROWTH; CELL PROLIFERATION; CHILD; CONTROLLED STUDY; EXON; FAMILIAL HYPERCHOLESTEROLEMIA; FEMALE; FLOW CYTOMETRY; FLUORESCENCE; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; HEPG2 CELL LINE; HUMAN; INTERNALIZATION; LYMPHOCYTE; MAJOR CLINICAL STUDY; MALE; PROTEIN BINDING; PYROSEQUENCING; RELATIVE; SINGLE NUCLEOTIDE POLYMORPHISM; U937 CELL LINE; ADOLESCENT; AGED; ATHEROSCLEROSIS; BLOOD; CORONARY ARTERY DISEASE; DNA SEQUENCE; FAMILY; GENETIC PREDISPOSITION; GENETICS; MIDDLE AGED; MUTATION; NUCLEOTIDE SEQUENCE; TUMOR CELL LINE; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; APOLIPOPROTEINS B; ATHEROSCLEROSIS; BASE SEQUENCE; CELL LINE, TUMOR; CELL PROLIFERATION; CHILD; CHOLESTEROL, LDL; CORONARY DISEASE; FAMILY; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HEP G2 CELLS; HUMANS; HYPERLIPOPROTEINEMIA TYPE II; MALE; MIDDLE AGED; MUTATION; PROPROTEIN CONVERTASES; RECEPTORS, LDL; SEQUENCE ANALYSIS, DNA; SERINE ENDOPEPTIDASES; U937 CELLS; YOUNG ADULT;

EID: 84921305686     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt573     Document Type: Article

References (51)

1. Brown, M.S. and Goldstein, J.L. (1986) A receptor-mediated pathway for cholesterol homeostasis. Science, 232, 34-47.
2. Vrablík, M., Ceska, R. and Horínek, A. (2001) Major apolipoprotein B-100 mutations in lipoprotein metabolism and atherosclerosis. Physiol. Res., 50, 337-343.
3. Soutar, A.K. and Naoumova, R.P. (2007) Mechanisms of disease: genetic causes of familial hypercholesterolemia. Nat. Clin. Pract. Cardiovasc. Med., 4, 214-225.
4. Medeiros, A.M., Alves, A.C., Francisco, V. and Bourbon, M. (2010) Update of the Portuguese Familial Hypercholesterolaemia Study. Atherosclerosis, 212, 553-558.
5. Usifo, E., Leigh, S.E., Whittall, R.A., Lench, N., Taylor, A., Yeats, C., Orengo, C.A., Martin, A.C., Celli, J. and Humphries, S.E. (2012) Low-density lipoprotein receptor gene familial hypercholesterolemia variant database: update and pathological assessment. Ann. Hum. Genet., 76, 387-401.
6. Soutar, A.K. (2010) Rare genetic causes of autosomal dominant or recessive hypercholesterolaemia. IUBMB Life, 62, 125-131.
7. Miserez, A.R. and Keller, U. (1995) Differences in the phenotypic characteristics of subjects with familial defective apolipoprotein B-100 and familial hypercholesterolemia. Arterioscler. Thromb. Vasc. Biol, 15, 1719-1729.
8. März, W., Baumstark, M.W., Scharnagl, H., Ruzicka, V., Buxbaum, S., Herwig, J., Pohl, T., Russ, A., Schaaf, L. and Berg, A. (1993) Accumulation of "small dense" low density lipoproteins (LDL) in a homozygous patients with familial defective apolipoprotein B-100 results from heterogenous interaction of LDL subfractions with the LDL receptor. J. Clin. Invest., 92, 2922-2933.
9. Innerarity, T.L., Weisgraber, K.H., Arnold, K.S., Mahley, R.W., Krauss, R.M., Vega, G.L. and Grundy, S.M. (1987) Familial defective apolipoprotein B-100: low density lipoproteins with abnormal receptor binding. Proc. Natl. Acad. Sci. USA, 84, 6919-6923.
10. Chatterton, J.E., Schlapfer, P., Bütler, E., Gutierrez, M.M., Puppione, D.L., Pullinger, C.R., Kane, J.P., Curtiss, L.K. and Schumaker, V.N. (1995) Identification of apolipoprotein B100 polymorphisms that affect low-density lipoprotein metabolism: description of a new approach involving monoclonal antibodies and dynamic light scattering. Biochemistry, 34, 9571-9580.
11. Boren, J., Ekstrom, U., Agren, B., Nilsson-Ehle, P. and Innerarity, T.L. (2001) The molecular mechanism for the genetic disorder familial defective apolipoprotein B100. J. Biol. Chem., 276, 9214-9218.
12. Krisko, A. and Etchebest, C. (2007) Theoretical model of human apolipoprotein B100 tertiary structure. Proteins, 66, 342-358.
13. Prassl, R. and Laggner, P. (2009) Molecular structure of low density lipoprotein: current status and future challenges. Eur. Biophys. J., 38, 145-158.
14. Myant, N.B. (1993) Familial defective apolipoprotein B-100: a review, including some comparisons with familial hypercholesterolaemia. Atherosclerosis, 104, 1-18.
15. Meng, Q.H., Pajukanta, P., Ilmonen, M., Schuster, H., Schewe, C.K., Andersson, L.C. and Tikkanen, M.J. (1996) Analysis of novel apolipoprotein Bmutations using a modified U937 cell line LDL binding assay. Clin. Chim. Acta, 256, 27-36.
16. Pullinger, C.R., Gaffney, D., Gutierrez, M.M., Malloy, M.J., Schumaker, V.N., Packard, C.J. and Kane, J.P. (1999) The apolipoprotein B R3531C mutation. Characteristics of 24 subjects from 9 kindreds. J. Lipid Res., 40, 318-327.
17. Gaffney, D., Reid, J.M., Cameron, I.M., Vass, K., Caslake, M.J., Shepherd, J. and Packard, C.J. (1995) Independent mutations at codon 3500 of the apolipoprotein B gene are associated with hyperlipidemia. Arterioscler. Thromb. Vasc. Biol., 15, 1025-1029.
18. Motazacker, M.M., Pirruccello, J., Huijgen, R., Do, R., Gabriel, S., Peter, J., Kuivenhoven, J.A., Defesche, J.C., Kastelein, J.J.P., Hovingh, G.K. et al. (2012) Advances in genetics show the need for extending screening strategies for autosomal dominant hypercholesterolaemia. Eur. Heart J., 33, 1360-1366.
19. Abecasis, G.R., Altshuler, D., Auton, A., Brooks, L.D., Durbin, R.M., Gibbs, R.A., Hurles, M.E. and McVean, G.A. (2010) A map of human genome variation from population-scale sequencing. Nature, 467, 1061-1073.
20. Bourbon, M., Alves, A.C., Medeiros, A.M., Silva, S. and Soutar, A.K. (2008) Familial hypercholesterolaemia in Portugal. Atherosclerosis, 196, 633-642.
21. Marks, D., Thorogood, M., Neil, H.A. and Humphries, S.E. (2003)Areview on the diagnosis, natural history, and treatment of familial hypercholesterolaemia. Atherosclerosis, 168, 1-14.
22. Kusters, D.M., Huijgen, R., Defesche, J.C., Vissers, M.N., Kindt, I., Hutten, B.A. and Kastelein, J.J.P. (2011) Founder mutations in the Netherlands: geographical distribution of the most prevalent mutations in the low-density lipoprotein receptor and apolipoprotein B genes. Neth. Heart J., 19, 175-182.
23. Futema, M., Plagnol, V., Whittall, R.A., Neil, H.A.W. and Humphries, S.E. (2012) Use of targeted exome sequencing as a diagnostic tool for Familial Hypercholesterolaemia. J. Med. Genet., 49, 644-649.
24. Talmud, P.J., Shah, S., Whittall, R., Futema, M., Howard, P., Cooper, J.A., Harrison, S.C., Li, K., Drenos, F., Karpe, F. et al. (2013) Use of low-density lipoprotein cholesterol gene score to distinguish patients with polygenic and monogenic familial hypercholesterolaemia: a case-control study. Lancet, 381, 1293-1301.
25. Fouchier, S.W., Kastelein, J.J.P. and Defesche, J.C. (2005) Update of the molecular basis of familial hypercholesterolemia in The Netherlands. Hum. Mutat., 26, 550-556.
26. Abifadel, M., Guerin, M., Benjannet, S., Rabe`s, J.-P., Le Goff, W., Julia, Z., Hamelin, J., Carreau, V., Varret, M., Bruckert, E. et al. (2012) Identification and characterization of new gain-of-function mutations in the PCSK9 gene responsible for autosomal dominant hypercholesterolemia. Atherosclerosis, 223, 394-400.
27. Hooper, A.J., Nguyen, L.T., Burnett, J.R., Bates, T.R., Bell, D.A., Redgrave, T.G., Watts, G.F. and Van Bockxmeer, F.M. (2012) Genetic analysis of familial hypercholesterolaemia in Western Australia. Atherosclerosis, 224, 430-434.
28. Bertolini, S., Pisciotta, L., Rabacchi, C., Cefalu`, A.B., Noto, D., Fasano, T., Signori, A., Fresa, R., Averna, M. and Calandra, S. (2013) Spectrum of mutations and phenotypic expression in patients with autosomal dominant hypercholesterolemia identified in Italy. Atherosclerosis, 227, 342-348.
29. Futema, M., Whittall, R.A., Kiley, A., Steel, L.K., Cooper, J.A., Badmus, E., Leigh, S.E., Karpe, F. and Neil,H.A.W.(2013) Analysis of the frequency and spectrum of mutations recognised to cause familial hypercholesterolaemia in routine clinical practice in a UK specialist hospital lipid clinic. Atherosclerosis, 10.1016/j.atherosclerosis.2013.04.011.
30. Lank, S.M., Wiseman, R.W., Dudley, D.M. and O'Connor, D.H. (2010) A novel single cDNA amplicon pyrosequencing method for high-throughput, cost-effective sequence-based HLA class I genotyping. Hum. Immunol., 71, 1011-1017.
31. Michils, G., Hollants, S., Dehaspe, L., Van Houdt, J., Bidet, Y., Uhrhammer, N., Bignon, Y.-J., Vermeesch, J.R., Cuppens, H. and Matthijs, G. (2012) Molecular analysis of the breast cancer genes BRCA1 and BRCA2 using amplicon-based massive parallel pyrosequencing. J. Mol. Diagn., 14, 623-630.
32. Frostegard, J., Hamsten, A., Gidlund, M. and Nilsson, J. (1990) Low density lipoprotein-induced growth of U937 cells: a novel method to determine the receptor binding of low density lipoprotein. J. Lipid Res., 31, 37-44.
33. Van den Broek, A.J., Hollaar, L., Schaefer, H.I., Van der Laarse, A., Schuster, H., Defesche, J.C., Kastelein, J.J. and Van 't Hooft, F.M. (1994) Screening for familial defective apolipoprotein B-100 with improved U937 monocyte proliferation assay. Clin. Chem., 40, 395-399.
34. Nigon, F., Lesnik, P., Rouis, M. and Chapman, M.J. (1991) Discrete subspecies of human low density lipoproteins are heterogeneous in their interaction with the cellular LDL receptor. J. Lipid Res., 32, 1741-1753.
35. Mahley, R.W., Innerarity, T.L., Pitas, R.E., Weisgraber, K.H., Brown, J.H. and Gross, E. (1977) Inhibition of lipoprotein binding to cell surface receptors of fibroblasts following selective modification of arginyl residues in arginine-rich and B apoproteins. J. Biol. Chem., 252, 7279-7287.
36. Weisgraber, K.H., Innerarity, T.L. and Mahley, R.W. (1978) Role of lysine residues of plasma lipoproteins in high affinity binding to cell surface receptors on human fibroblasts. J. Biol. Chem., 253, 9053-9062.
37. Mahley, R.W., Weisgraber, K.H. and Innerarity, T.L. (1979) Interaction of plasma lipoproteins containing apolipoproteinsBandEwith heparin and cell surface receptors. Biochim. Biophys. Acta, 575, 81-91.
38. Brouwers, M.C.G.J., Van Greevenbroek, M.M.J., Stehouwer, C.D.A., De Graaf, J. and Stalenhoef, A.F.H. (2012) The genetics of familial combined hyperlipidaemia. Nat. Rev. Endocrinol., 8, 352-362.
39. Buch, S., Schafmayer, C., Völzke, H., Becker, C., Franke, A., Von Eller-Eberstein, H., Kluck, C., Bässmann, I., Brosch, M., Lammert, F. et al. (2007) A genome-wide association scan identifies the hepatic cholesterol transporter ABCG8 as a susceptibility factor for human gallstone disease. Nat. Genet., 39, 995-999.
40. Chen, Z.-C., Shin, S.-J., Kuo, K.-K., Lin, K.-D., Yu, M.-L. and Hsiao, P.-J. (2008) Significant association of ABCG8:D19H gene polymorphism with hypercholesterolemia and insulin resistance. J. Hum. Genet., 53, 757-763.
41. Srivastava, A., Srivastava, A., Srivastava, K., Choudhuri, G. and Mittal, B. (2010) Role of ABCG8 D19H (rs11887534) variant in gallstone susceptibility in northern India. J. Gastroenterol. Hepatol., 25, 1758-1762.
42. Den Dunnen, J.T. and Antonarakis, S.E. (2000) Mutation nomenclature extensions and suggestions to describe complex mutations: a discussion. Hum. Mutat., 15, 7-12.
43. Adzhubei, I.A., Schmidt, S., Peshkin, L., Ramensky, V.E., Gerasimova, A., Bork, P., Kondrashov, A.S. and Sunyaev, S.R. (2010) A method and server for predicting damaging missense mutations. Nat. Methods, 7, 248-249.
44. Ng, P.C. and Henikoff, S. (2003) SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res., 31, 3812-3814.
45. González-Pérez, A. and López-Bigas, N. (2011) Improving the assessment of the outcome of nonsynonymous SNVs with a consensus deleteriousness score, Condel. Am. J. Hum. Genet., 88, 440-449.
46. Schwarz, J.M., Rödelsperger, C., Schuelke, M. and Seelow, D. (2010) MutationTaster evaluates disease-causing potential of sequence alterations. Nat. Methods, 7, 575-576.
47. Grantham, R. (1974) Amino acid difference formula to help explain protein evolution. Science, 185, 862-864.
48. Etxebarria, A., Palacios, L., Stef, M., Tejedor, D., Uribe, K.B., Oleaga, A., Irigoyen, L., Torres, B., Ostolaza, H. and Martin, C. (2012) Functional characterization of splicing and ligand-binding domain variants in the LDL receptor. Hum. Mutat., 33, 232-243.
49. Catapano, A.L., Reiner, Z., De Backer, G., Graham, I., Taskinen, M.R., Wiklund, O., Agewall, S., Alegria, E., Chapman, M., Durrington, P. et al. (2011) ESC/EAS Guidelines for the management of dyslipidaemias The Task Force for themanagement of dyslipidaemias of the European Society of Cardiology (ESC) and the European Atherosclerosis Society (EAS). Atherosclerosis, 217, 3-46.
50. Marduel, M., Ouguerram, K., Serre, V., Bonnefont-Rousselot, D., Marques-Pinheiro, A., Erik Berge, K., Devillers, M., Luc, G., Lecerf, J.-M., Tosolini, L. et al. (2013) Description of a large family with autosomal dominant hypercholesterolemia associated with the APOE p.Leu167del mutation. Hum. Mutat., 34, 83-87.
51. Pollin, T.I., Damcott, C.M., Shen, H., Ott, S.H., Shelton, J., Horenstein, R.B., Post, W., McLenithan, J.C., Bielak, L.F., Peyser, P.A. et al. (2008) A null mutation in human APOC3 confers a favorable plasma lipid profile and apparent cardioprotection. Science, 322, 1702-1705.