Abnormal splicing of ABCA1 pre-mRNA in Tangier disease due to a IVS2 +5G>C mutation in ABCA1 gene

Journal of Lipid Research

Volumn 44, Issue 2, 2003, Pages 254-264

  Altilia, Serena ^a   Pisciotta, Livia ^b   Garuti, Rita ^a   Tarugi, Patrizia ^a   Cantafora, Alfredo ^c   Calabresi, Laura ^d   Tagliabue, Jacopo ^e   Maccari, Sergio ^f   Bernini, Franco ^g   Zanotti, Ilaria ^g   Vergani, Carlo ^e   Bertolini, Stefano ^b   Calandra, Sebastiano ^d  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

^e FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^f Sant'Anna Hospital   (Italy)

^g NONE

Author keywords

ABCA1 minigenes; Donor splice site mutation; In vitro splicing

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A1; APOLIPOPROTEIN A1; APOLIPOPROTEIN A2; APOLIPOPROTEIN B; CYTOSINE; GUANINE; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; PEPTIDE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL CELL; AORTA DISSECTION; AORTA RUPTURE; ARTICLE; CELL LINE; CELL MEMBRANE; CHOLESTEROL TRANSPORT; CLINICAL ARTICLE; CONTROLLED STUDY; EXON; FEMALE; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTRON; MALE; MOUSE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PEDIGREE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; RNA SPLICING; SITE DIRECTED MUTAGENESIS; SKIN FIBROBLAST; TANGIER DISEASE; TRANSLATION INITIATION; WILD TYPE;

ADULT; AGED; ALTERNATIVE SPLICING; ATP-BINDING CASSETTE TRANSPORTERS; CELLS, CULTURED; CHILD; CHOLESTEROL; FEMALE; FIBROBLASTS; HAPLOTYPES; HUMANS; INTRONS; MALE; MIDDLE AGED; PEDIGREE; POINT MUTATION; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; TANGIER DISEASE;

EID: 10744222201     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M200248-JLR200     Document Type: Article

References (41)

1. Assmann, G., A. von Eckardstein. and B. H. Brewer, Jr. 2001. Familial Analphalipoproteinemia: Tangier Disease. In The Metabolic and Molecular Bases of Inherited Disease. 8th edition. C. R. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle, editors. McGraw-Hill, New York. 2937-2960.
2. Oram, J. F., and R. M. Lawn. 2001. ABCA1: the gatekeeper for eliminating excess of cholesterol. J. Lipid Res. 42: 1173-1179.
3. Attie, A. D., J. P. Kastelein, and M. R. Hyden. 2001. Pivotal role of ABCA1 in reverse cholesterol transport influencing HDL levels and susceptibility to atheroslerosis. J. Lipid Res. 42: 1717-1726.
4. Bodzioch, M., E. Orsò, J. Klucken, T. Langmann, A. Böttcher, W. Diederich, W. Drobnik, S. Barlage, C. Büchler, M. Porsch-Özcü rümez, W. E. Kaminski, H. W. Hahmann, K. Oette, G. Rothe, C. Aslanidis, K. J. Lackner, and G. Schmitz. 1999. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 22: 347-351.
5. Brooks-Wilson, A., M. Marcil, S. M. Clee, L-H. Zhang, K. Roomp, M. van Dam, L. Yu, C. Brewer, J. A. Collins, H. O. F. Molhuizen, O. Loubser, B. F. F. Ouelette, K. Fichter, K. J. D. Ashbourne-Excoffon, C. W. Sensen, S. Scherer, S. Mott, M. Denis, D. Martindale, J. Frohlich, K. Morgan, B. Koop, S. Pimstone, J. J. P. Kastelein, J. Genest, Jr., and M. R. Hayden. 1999. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nature Genet. 22: 336-45.
6. Lawn, R. M., D. P. Wade, M. R. Garvin, X. Wang, K. Schwartz, J. G. Porter, J. J. Seilhamer, A. M. Vaughan, and J. F. Oram. 1999. The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. J. Clin. Invest. 104: R25-R31.
7. Remaley, A. T., S. Rust, M. Rosier, C. Knapper, L. Naudin, C. Broccardo, K. M. Peterson, C. Koch, I. Arnould, C. Prades, N. Duverger, H. Funke, G. Assmann, M. Dinger, M. Dean, G. Chimini, S. Santamarina-Fojo, D. S. Fredrickson, P. Denefle, and H. B. Brewer, Jr. 1999. Human ATP-binding cassette transporter 1 (ABC1): genomic organization and identification of the genetic defect in the original Tangier disease kindred. Proc. Natl. Acad. Sci. USA. 96: 12685-90.
8. Rust, S., M. Rosier, H. Funke, J. Real, Z. Amoura,J-C. Piette, J-F. Deleuze, H. B. Brewer, N. Duverger, P. Denefle, and G. Assmann. 1999. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat. Genet. 22: 352-355.
9. Marcil, M., A. Brooks-Wilson, S. M. Clee, K. Roomp, L-H. Zhang, L. Yu, J. A. Collins, M. van Dam, H. O. F. Molhuizen, O. Loubster, B. F. F. Ouellette, C. W. Sensen, K. Fichter, S. Mott, M. Denis, B. Boucher, S. Pimstone, J. Genest, J. J. P. Kastelein, and M. R. Hayden. 1999. Mutations in the ABC1 gene in familial HDL deficiency with defective cholesterol efflux. Lancet. 354: 1341-1346.
10. Brousseau, M. E., E. J. Schaefer, J. Dupuis, B. Eustace, P. Van Eerdewegh, A. L. Goldkamp, L. M. Thurston, M. G. FitzGerald, D. Yasek-McKenna, G. O'Neill, G. P. Eberhart, B. Weiffenbach, J. M. Ordovas, M. W. Freeman, R. H. Brown, Jr., and J. Z. Gu. 2000. Novel mutations in the gene encoding ATP-binding cassette 1 in four Tangier disease kindreds. J. Lipid Res. 41: 433-41.
11. Wang, J., J. R. Burnett, S. Near, K. Young, B. Zinman, A. J. G. Hanley, P. W. Connelly, S. B. Harris, and R. A. Hegele. 2000. Common and rare ABCA1 variants affecting plasma HDL cholesterol. Arterioscler. Thromb. Vasc. Biol. 20: 1983-1989.
12. Clee, S. M., J. J. P. Kastelein, M. van Dam, M. Marcil, K. Roomp, K. Y. Zwarts, J. A. Collins, R. Roelants, N. Tamasawa, T. Stulc, T. Suda, R. Ceska, B. Boucher, C. Rondeau, C. DeSouich, A. Brooks-Wilson, H. O. F. Molhuizen, J. Frohlich, J. Genest, Jr., and M. R. Hayden. 2000. Age and residual cholesterol efflux affect HDL cholesterol levels and coronary artery disease in ABCA1 heterozygotes. J. Clin. Invest. 106: 1263-70.
13. Bertolini, S., L. Pisciotta, M. Seri, R. Cusano, A. Cantafora, L. Calabresi, G. Franceschini, R. Ravazzolo, and S. Calandra. 2001. A point mutation in ABC1 gene in a patient with severe premature coronary heart disease and mild clinical phenotype of Tangier Disease. Atherosclerosis. 154: 599-605.
14. Lapicka-Bodzioch, K., M. Bodzioch, M. Krüll, D. Kielar, M. Probst, B. Kiec, H. Andrikovics, A. Böttcher, J. Hubacek, C. Aslanidis, N. Suttorp, and G. Schmitz. 2001. Homogeneous assay based on 52 primer sets to scan for mutations of the ABCA1 gene and its application in genetic analysis of a new patient with familial high-density lipoprotein deficiency syndrome. Biochim. Biophys. Acta. 1537: 42-48.
15. Huang, W., K. Moriyama, T. Koga, H. Hua, M. Ageta, S. Kawabata, K. Mawatari, T. Imamura, T. Eto, M. Kawamura, T. Teramoto, and J. Sasaki. 2001. Novel mutations in ABCA1 gene in Japanese patients with Tangier disease and familial high lipoprotein deficiency with coronary heart disease. Biochim. Biophys. Acta. 1537: 71-78.
16. Nishida, Y., K. K. Hirano, K. Tsukamoto, M. Nagano, C. Ikegami, K. Roomp, M. Ishihara, N. Sakane, Z. Zhang, K. K. Tsujii, A. Matsuyama, T. Ohama, F. Matsuura, M. Ishigami, N. Sakai, H. Hiraoka, H. Hattori, C. Wellington, Y. Yoshida, S. Misugi, M. R. Hayden, T. Egashira, S. Yamashita, and Y. Matsuzawa. 2002. Expression and functional analyses of novel mutations of ATP-binding cassette transporter-1 in Japanese patients with high-density lipoprotein deficiency. Biochem. Biophys. Res. Commun. 290: 713-721.
17. Hong, S. H., J. Rhyne, K. Zeller, and M. Miller. 2002. Novel ABCA1 compound variant associated with HDL cholesterol deficiency. Biochim. Biophys. Acta. 1587: 60-64.
18. Santamarina-Fojo, S., K. Peterson, C. Knapper, Y. Qiu, L. Freeman, J. F. Cheng, J. Osorio, A. Remaley, X. P. Yang, C. Haudenschild, C. Prades, G. Chimini, E. Blackmon, T. Francois, N. Duverger, E. M. Rubin, M. Rosier, P. Deneflè, D. S. Fredickson, and B. H. Brewer, Jr. 2000. Complete genomic sequence of the human ABCA1 gene: analysis of the human and mouse ATP-binding cassette A promoter. J. Clin. Invest. 97: 7987-92.
19. Pullinger, C. R., H. Hakamata, N. Duchateau, C. Eng, B. E. Aouizerat, M. H. Cho, C. F. Fielding, and J. P. Kane. 2001. Analysis of hABC1 gene 5′ end: additional peptide sequence, promoter region, and four polymorphisms. Biochim. Biophys. Res. Commun. 271: 451-455.
20. Langmann, T., J. Klucken, M. Reil, G. Liebisch, M-F. Luciani, G. Chimini, W. E. Kaminski, and G. Schmitz. 1999. Molecular cloning of the human ATP-binding cassette transporter 1 (hABC1): evidence for sterol-dependent regulation in macrophages. Biochem. Biophys. Res. Commun. 257: 29-33.
21. Kozak, M. 1996. Interpreting cDNA sequences: some insights from studies on translation. Mamm. Genome. 7: 563-574.
22. 2-terminal signal anchor sequence that translocates the protein's first hydrophilic domain to the exoplasmic space. J. Biol. Chem. 276: 15137-15145.
23. Costet, P., Y. Luo, N. Wang, and A. R. Tall. 2000. Sterol-dependent transactivation of the ABCA1 promoter by the liver X receptor/retinoid X receptor. J. Biol. Chem. 276: 28240-28245.
24. Bellincampi, L., M. L. Simone, C. Motti, C. Cortese, S. Bernardini, S. Bertolini, and S. Calandra. 2001. Identification of an alternative transcript of ABCA1 gene in different human cell types. Biochim. Biophys. Res. Commun. 283: 590-597.
25. Cavelier, L. B., Y. Qiu, J. K. Bielicki, V. Afzal, J-F. Cheng, and E. M. Rubin. 2001. Regulation and activity of the human ABCA1 gene in transgenic mice. J. Biol. Chem. 276: 18046-18051.
26. Vergani, C. G., A. C. Plancher, M. Zuin, M. Cattaneo, C. Tramaloni, S. Maccari, P. Roma, and A. L. Catapano. 1984. Bile lipid composition and haematological variables in a case of high density lipoprotein deficiency (Tangier disease). Eur. J. Clin. Invest. 14: 49-54.
27. Tarugi, P., A. Lonardo, G. Ballerini, A. Grisendi, M. Pulvirenti, A. Bagni, and S. Calandra. 1996. Fatty liver in heterozygous hypobetalipoproteinemia caused by a novel truncated form of apolipoprotein B. Gastroenterology. 111: 1125-1133.
28. Calandra, S., P. Tarugi, and M. Ghisellini. 1984. Separation of the isoprotein forms of apoprotein A-I of rat, rabbit and human HDL by combined isoelectrofocusing and SDS-polyacrylamide gel electrophoresis. Atherosclerosis. 50: 209-221.
29. Boyum, A. 1984. Separation of lymphocytes, granulocytes and monocytes from human blood using iodinated density gradient medium. Method Enzymol. 108: 88-102.
30. Bortnick, A. E., G. H. Rothblat, G. W. Stoudt, K. L. Hoppe, J. R. Lori, J. McNeish, and O. Francone. 2000. The Correlation of ATP-binding cassette 1 mRNA levels with cholesterol efflux from various cell lines. J. Biol. Chem. 275: 28634-28640.
31. Sakr, S. W., D. L. Williams, G. W. Stoudt, M. C. Phillips, and G. H. Rothblat. 1999. Induction of cellular cholesterol efflux to lipid-free apolipoprotein AI by cAMP. Biochim. Biophys. Acta. 1438: 85-98.
32. Repa, J. J., S. D. Turley, J. M. A. Lobaccaro, J. Medina, L. Li, K. Lusting, K. Shan, R. A. Heyman, J. M. Dietschy, and D. J. Mangelsdorf. 2000. Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science. 289: 1524-1529.
33. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Wenz, H. M., J. M. Robertson, S. Menchen, F. Oaks, D. M. Demorest, D. Scheibler, B. B. Rosenblum, C. Wike, D. A. Gilbert, and J. W. Efcavitch. 1998. High precision genotyping by denaturing capillary electrophoresis. Genome Res. 8: 69-80.
35. Moriyama, K., J. Sasaki, Y. Takada, A. Matsunaga, J. Fukui, J. J. Albers, and K. Arakawa. 1996. A cysteine-containing truncated Apo A-I variant associated with HDL deficiency. Arterioscler. Thromb. Vasc. Biol 16: 1416-1423.
36. 171 → Stop). Atherosclerosis. 131: 85-95.
37. Webb, J., D. D. Patel, C. C. Shoulders, B. L. Knight, and A. K. Soutar. 1996. Genetic variation at a splicing branch point in intron 9 of the low density lipoprotein (LDL)-receptor gene: a rare mutation that disrupts mRNA splicing in a patients with familial hypercholesterolemia and a common polymorphism. Hum. Mol. Genet. 5: 1325-1331.
38. Serfaty-Lacrosniere, C., F. Civeira, A. Lanzberg, P. Isaia, J. Berg, E. D. Janus, M. P. Smith, Jr., P. H. Pritchard, J. Frohlich, R. S. Lees, G. F. Barnard, J. M. Ordovas, and E. J. Schaefer. 1994. Homozygous Tangier disease and cardiovascular disease. Atherosclerosis. 107: 85-98.
39. Cooper, D. N., and M. Krawczak. 1990. The mutational spectrum of single base-pair substitutions causing human genetic disease: patterns and predictions. Hum. Genet. 85: 55-74.
40. Cartegni, L., S. L. Chew, and A. R. Krainer. 2002. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet. 3: 285-298.
41. Shapiro, M. B., and P. Senapathy. 1987. RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acid Res. 15: 7155-7174.